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Manual Therapy
in Children
Manual Therapy in Children presents a • Radi o l o gy in Manual Therapy: describes
comprehensive conceptual approach to the the functional radiology of the spine in the
subject of manual therapy for children of young child and how to take, interpret and
different ages. This approach considers the document radiographs in infants and young
relationship between the neuromusculoskeletal children.
structure and function at different stages of
development and places strong emphasis on • Making Sense of It All: outlines the clinical
the prevention of problems as the child picture including functional disorders (such
develops as well as on their safe and effective as KiSS syndrome), neurological and
treatment and management. Edited and largely biomechanical disorders, and looks at
written by a leading European orthopedic the long-term consequences of untreated
physician, the book also includes contributions functional disorders in the first year.
from over 20 leading practitioners in the field.
Manual Therapy in Children is soundly
The contents are grouped into 5 main sections: based on the latest evidence. Written by an
• The Basics: summarizes the essential established author with contributions from
theoretical base (anatomy and physiology, a large team of clinical experts, the text is
neuromotor development of the first 5 years - supplemented with almost 250 high quality
crawling to walking, surface anatomy). illustrations. It presents a fresh and well­
considered approach to the management
• Clinical Insights: looks at issues which
of a wide range of paediatric problems.
may affect the neuromotor development of
All practitioners working with children with
the child and approaches to management,
neuromusculoskeletal conditions will find this
e.g. birthing interventions, birth trauma,
a clinically relevant and practical resource.
differential diagnosis of central and
peripheral neurological disorders, asymmetry. Heiner Biedermann is a Practitioner in
• Pradical Aspects of Manual Therapy Conservative Orthopedics, Cologne, Gennany,
in Children: includes advice on interaction and Member of the European Workgroup for
with parents and children; guidance for Manual Medicine. He was fonnerly a surgeon
examination and treatment; considerations to at the Surgical Department of the University of
be bome in mind when treating different Witten-Herdecke and Schwerte Hospital,
joints and spinal regions. Germany.

This book is appropriate for:

• Manual therapists
• Pediatricans
• Osteopaths


• Orthopedic physicians
.I� iUi

Primary Care
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Manual Therapy
inCh i Id ren

Copyrighted Material
Manual Therapy

Child ren

Edited by

Heiner Biedermann MD
Practitioner in Conservative Orthopedics, Cologne, Germony, and Member of the European
Workgroup for Manual Medicine. Formerly Surgeon at the Surgical Department of the
University of Witten-Herdecke and Schwerte Hospital, Germany

..I� CHURCHill


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An imprint of Elsevier Limited

© 2004, Elsevier Limited. All rights reserved.

The right of Heiner Biedermann to be id e n ti fie d as editor of this work has been
asserted by him in accordance with the Copyr i gh t, De s igns and Patents Act 1988.

No part of this publication may be reproduced, stored in a retri eva l system, or

t rans m i tted in any form or by any means, electronic, mechanicaJ, photocopying,
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by selecting 'Customer Support' and then ' Obtaining Permissions'.

First published 2004

ISBN 0 443 10018 7

British Library Cataloguing in Publication Data

A catalogue record for this book is available from the British Library

Library of Congress Cataloging in Publication Data

A catalog record for this book is available from the Library of Congress

Medical knowledge is constantly ch angin g . Sta nda rd sa fety p r eca u tions must be
followed, but as new research and clinical experience broaden ou r kn ow l edg e ,
changes i.n treatment and drug t he rapy may become necessary or a pprop r ia te .

Readers are advised to check the most current product information provided by
the manufacturer of each drug to be administered to verify the recommended
dose, the method and duration of administration, and contraindications. [t is the
responsibility of the p ractit i o n e r, relying on experience and knowledge of the
patient, to determine dosages and the best treatment for each individual patient.
Neither the publishers nor the eclitor and contributors will be liable for any loss
or damage of any nature occasioned to or suffered by any person acting or
refraining from acting as a result of relia.nce on the material contained in t his

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Contributors vii 8. Birth trauma and its implications for

neuromotor development 85
Preface ix
1. Introduction: reviewing the history of
9. Differential diagnos i s of central and
manual therapy in children
peri phera l neurological disorders in
H. Biedermann
i nfants 99
L. Babino, H. Biedermann, S. lIiaeva
SECTION 1 The theoretical base 9
10. Manual thera py from a pediatrician s
2. Sensorimotor development of newborn and

viewpoint 113
children from the viewpoint of manual
therapy 11
H. Biedermann 11. The influence of the high cervical region
on the autonomic regulatory system in
3. Development and topographical anatomy
infants 125
of the cervical spine 15
L. E. Koch
R. Huang, B. Christ
12. Attention deficit disorder and the
4. Develop ment of the central nervous system 29
upper cervical spine 133
A. Hori
R. Theiler
5. Adaptive properties of motor behavior 45
13. Asymmet ry of the posture l ocomotion
J.-M. Ramirez

apparatus and dentition in children 145

6. N e uromoto r devel opment in infancy H. Korbmacher. L.E. Koch, B. Kahl-Nieke
and early childhood 57
S. Huber

SECTION 3 The different levels: practical

SECTION 2 Clinical insights 73 aspects of manual therapy in children 1 61

7. Birthing interventions and the newborn 14. Practicalities of manual therapy in

cervical spine 75 children 163
D. Ritzmann H. Biedermann

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15. Manual therapy of the sacroiliac joints and 21. Measuring it: different approaches to the
pelvic girdle in children 173 documentation of posture and
F Huguenin coordination 259
H. Biedermann, R. Radel, A. Friedrichs
1 6. Manual therapy of the thoracic spine
in ch i ldren 185
SECTION 5 Making sense of it all 273
H. Mohr, H. Biedermann
22. Complexity theory and its implications
17. Examination and treatment of the cervical
for manual therapy 275
spine in children 205
M. E. Hyland, H. Biedermann
H. Biedermann
23. The big, the small, and the beautiful 281
0. Gunturkun
SECTION 4 Radiology in manual therapy in
24. The KISS syndrome: symptoms and signs 285
children 213
H. Biedermann
18. Functional radiology of the cervical spine
25. KIDD: KISS - ind u ced dysgnosia and
in children 215
dyspraxia 303
H. Biedermann
H. Biedermann
19. The how-to of making radiographs
26. The family dimension 313
of newborns and children 235
H. Biedermann
H. Biedermann
27. Epilogue 321
20. Radiological examination of the spine in
H. Biedermann
children and adolescents: pictorial essay 243
Peter Waibel Index 327

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Lilia Babina, MD Susanne Huber Dipl Phys Dr rer nat

Professor, Neuropediatric Department, Pediatric Research Fellow, Friedrich-Miescher Laboratory of the
Rehabilitation Clinic, Pjatigorsk, Russia Max-Planck-Society, Tiibingen, Germany

Heiner Biedermann MD
Practitioner in Conservative Orthopedics, Cologne, Freddy Huguenin MD

Germany and Member of the European Workgroup for Former Consultant at the University Clinic of

Manual Medicine (EWMM). Formerly Surgeon at the Physical Medicine and Rehabilitation of Geneva,

Surgical Department of the University of Witten­ Switzerland

Herdecke and Schwerte Hospital, Germany

Michael E. Hyland BSe PhD BCPsyehol

Bodo E. A. Christ MD
Department of Psychology, University of Plymouth,
Professor, Institute of Anatomy and Cell Biology,
Plymouth, UK
University of Freiburg, Germany

Amd Friedrichs
S. Iliaeva MD
Friendly Sensors AG, Jena, Germany
Rehabilitative and Physical Medicine, Cologne,
Onur Giintiirkiin PhD(Psyehol)
Professor of Psychology, Faculty of Psychology,
Ruhr-University Bochum, Bochum, Germany Barbel Kahl-Nieke PhD DrMed(dentl
Chair of Department of Orthodontics, College of
Akira Hori MD Dentistry, University of Hamburg, Hamburg,
Professor, Research Institute for Neurology and Germany
Psychiatry, National Nishi- Tottori Hospital, Tottori,
L. E. Koch DrMed
Ruij in Huang PD DrMed General Practitioner and Member of the European
Institute of Anatomy and Cell Biology, University of Workgroup for Manual Medicine (EWMM),
Freiburg, Freiburg, Germany Eckernforde, Germany

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Heike M. Korbmacher DrMed(dent) Dorin Ritzmann DrMed FMH(Gynecology/Obstetrics)

Associate Professor, Department of Orthodontics, CertMedHypnosisTraumaTherapy (EMDRFrancineShapiro)

College of Dentistry, University of Hamburg, Zurich, Switzerland

Hamburg, Germany
R. Sacher MD
Hanne Kuhnen DrMed Private Practitioner and Member of the European
Pediatrician, Kevelaer, Germany Workgroup for Manual Medicine (EWMM),
Dortmund, Germany
H. Mohr
Physiotherapist and Member of the European Reinhard W. Theiler DrMed FMH
Workgroup for Manual Medicine (EWMM), Manual Pediatrician (neuro-rehabilitation) and Member of the
Therapist and Lecturer, Ede, The Netherlands European Workgroup for Manual Medicine
(EWMM), Trimbach, Switzerland
R. Radel MD
Orthopedic Surgeon, Herne, Germany Peter J. Waibel MD
Chief of Section, Radiology Department, Ostschweizer
Jan-Marino Ramirez PhD Kinderspital, St Gallen, Switzerland
Professor of Anatomy and Neurosciences, Department
of Anatomy, The University of Chicago, Chicago,
Illinois, USA

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'I don't like writing - I like having written' - took an interest in the potential of manual therapy
Dorothy Parker once said. This holds true for without actually practising it. Some of them con­
almost every writer and certainly for me. To com­ tributed material to this book, others offered valu­
prehend the pleasure felt at this moment (all the able hints and pointed out weaknesses in the
chapters have been sent to the publisher and the arguments.
only thing left to do is to write these short lines) The quest to be up to date is as unviable as the
might be difficult for somebody who was not (yet) search for the end of the rainbow - but both may
in this position. lead to insights not reached otherwise. T he
It is more than five years since English and inevitable delay between the submission of the
Dutch friends proposed writing a book on manual manuscript and the finished book has to be
therapy in children. Soon it became clear that this accepted stoically if one wants to avoid endless
rapidly developing field was too vast to be dealt addenda.
with by one author alone. The search for contribu­ The basic tenets of what is presented here have
tors willing to share their competence began, and stood the test of time and in publishing these find­
I am immensely grateful to all of those willing to ings, we hope to encourage others to comment
sacrifice their rare spare time to write their and criticize in order to use this as a base for fur­
chapters. ther improvements.
Almost as admirable was the patience of those All those around somebody working on a book
on the publisher 's side who waited unweary­ suffer - from the different forms of neglect the
ingly while the complex material was rearranged concentration on such a long-term project implies.
over and over again to gain a satisfactory form To thank one's wife and offspring for their com­
and structure. Needless to say the initial dead­ prehension is but a shallow recompense for it, and
line for this book was exceeded by many as formulaic as it may be, it inevitably opens the
months. 'thank you' section.
During these years, several congresses brought All the colleagues who helped with their advice
countless discussions. All those questions and and criticism come a close second, to be followed
criticisms helped to create a coherent concept out by the team at Elsevier who endured the long
of the observations of the practical work with chil­ delays and constant alterations. Representing the
dren. The friends and colleagues of the European first group Editha Halfmann, Uli Gohmann and
Workgroup for Manual Medicine are exemplary Bruno Maggi have to be mentioned; at Elsevier I
in that regard, but also all those pediatricians who want to thank especially Mary Law, Dinah Thorn

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and Joannah DW1can for patience and the entire tion and for making available all the material and
production team, encouragement and all their photos used in this book - their book, in a way.
helpful remarks. 'Tritt frisch auf - tu's Maul auf!- hor bald auf!'
Jenny Fox rendered the text a bit more compre­ Martin Luther once said; we tried to heed that
hensible with her 'native speaker' advice and her advice.
Last but not least I want to thank my young Heiner Biedermann
patients and their families for feedback, motiva- Antwerp 2004

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Chapter 1 --�------�--��-- ----�

Introduction: reviewing the history

of manual therapy in children
H. Biedermann



'Do you have to know philosophy to play the

'No, but it helps' might be an appropriate answer.
piano?' 1
And, translated into the lingo of manual therapy:
The lessons of MTC for manual therapy in
You do not have to know about the history of our
general 2
trade, about neurophysiology or anatomy to
The role of the therapist 4
manipulate - but to reach a certain professional
MTC influences body and soul 4
level, it helps - a lot.
The long tradition of MTC - and where we are
Nobody with any knowledge of music doubts
heading for 5
the idea that you need to understand the cultural
MTC depends on supporting therapies 6
and philosophical context of a piece of music you
want to interpret. If playing music was as simple
as copying the notes onto an instrument, you
could feed a given score to the computer and -
plop! - the perfect music is played. But it is the
interpretation of the player which turns a sterile
bit of notation into a work of art. And as the soci­
ety in which one plays one's tunes evolves, so
does the interpretation of the great compositions.
There will never be the 'ultimate' interpretation of
Beethoven's 9th or Schubert's Forellenquintett.
The same is true for manual therapy. The way
we interact with our patients is crucially depend­
ent on an exact appraisal of their physical and
psychological condition. Teclmiques that were
well established in the 1930s would be considered
a bit brutal today.
With small children the situation gets even
more complex, as we have to take into account an
entire family, i.e. the parents and siblings present

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at the consultation. How much of a success an ination. This may get a bit tiring sometimes -
individual treatment will be depends at least as but it is for them that this book is intended.
much on the good contact between therapist
and family as on the technical know-how of the
Any contact between two individuals has THERA PY IN GENERAL
effects on both of them. For the purposes of this
book, we can limit the scope by defining manual What we find is what we are looking for - this is
therapy as the deliberate touching of the patient nowhere more true than in medical research. As a
by a trained therapist with the intention of young student one enters the arena with the some­
improving the patient's condition. Seen from close what naive thought that what we are pursuing is
enough, manual therapy (and even more so man­ the truth, and nothing but the truth. But we are
ual therapy in children - MTC) is a simple mechan­ condemned to deviate from this noble goal from
ical procedure. One might be tempted to confine a the beginning, and have to embrace the constraints
treatise to the bare necessities, a 'how to' of the of our neurophysiological input capacity and the
different t�chniques available. This approach limits of our budget - to name but two of the more
would be an antidote to the sometimes lofty extreme obstacles on our way to 'the truth'.
explanations offered for some of the methods When trying to present a paper about a medical
available today. Quite a few books are organized problem, we end up more or less with the advice
according to such a scheme. The reader is offered the Economist's editor gave to a young employee
a short introduction about the history of the spe­ 'Simplify, then exaggerate!' . There seem to be two
cific method presented in the text, and then page ways out of this dilemma, and they have, almost
after page showing a therapist, his/her patient always, opposite directions. The traditional 'scien­
and the different positions possible. tific' approach is to partition the complexity of the
Such a Kama-Sutra of manual techniques has clinical picture till we arrive at a level where the
some merits - to remind the experienced of what task seems to be clear enough to be cast into a lin­
is possible - but it cannot replace the real thing, ear question of 'what if'. This is basically the realm
i.e. learning by observing and in close contact of the evidence-based medicine (Sackett et a11997)
with a proficient teacher. So we shall not avoid so much in vogue now. This approach is an excel­
those 'how-to' pictures entirely, but these parts lent tool to decide questions like 'If I want to treat
of the book are few and not the most important cystitis with an antibiotic, which one would be
ones. best?'
In teaching and demonstrating manual therapy One is reminded of the statement of the bio­
in children, one encounters two principal reactions: chemist A. Szent-Gyorgyi (1972): 'I moved from
anatomy to the study of tissues, then to electron
• One group of colleagues - the bigger one - microscopy and chemistry, and finally to quantum
watches and after an hour or two their body mechanics. This downward journey through the
language expresses very clearly the idea that scale of dimensions has its irony, for in my search
they have seen it all. As it looks so simple - just for the secret of life I ended up with atoms and
a little push on the side of the neck - why waste electrons which have no life at all. Somewhere
any more time! These guests leave the consulta­ along the line life has run out of my fingers.'
tion and my address book equally quickly. When we try to simplify - and simplify we
• A second, smaller group looks more closely and must in order to get to grips with the complexity
these colleagues more often than not start to ask of disease and disorder - we have to keep in mind
a lot of questions about the details of the exam- what we do. And we have to keep in mind that the

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Introduction 3

questions we can ask in a reductionist context are what we are confronted with is not necessarily the
not necessarily the most relevant. whole spectrum of complaints. And - as stated in
The second approach, as exemplified by manual the beginning - the socio-cultural context we are
therapy in the non-trivial sense (see Chapter 22), working in plays an important role, too.
aims at re-establishing a functional eq�ilibrium This dilemma occurs as soon as we look for
which renders its effects dependent on a multitude long-term effects of any given therapeutic inter­
of other influences, psychological as well as physi­ vention. Maybe this is the reason why that kind of
cal. Such an approach has to be based on the research has been so neglected. Applied to manual
results of reductionist research, but it takes into therapy this means that it is much easier to evalu­
account the complex interaction with other levels ate the effect of a lumbar manipulation on low
of maintaining the homeostasis and these mecha­ back pain than that of a cervical manipulation on
nisms are in most cases not quantifiable by 'hard' the wellbeing of a baby. But is it the most relevant
science. This is one reason why the treatment of question?
small children is of such importance to us. Here we The first studies we shall be able to complete
find a situation which we can define much better will be about problems that are suitable for a
than the far more complex pictures in older chil­ rather restricted protocol. And, yes, it is necessary
dren, let alone adolescents or adults. In babies we to do such research - not because the questions we
deal with a rather clear-cut pathology, the two can answer in such a way are the most pressing
main factors being genetic predisposition and the ones, but because it helps to breach the wall of
history up to the moment of the first examination incomprehension that separates the majority of
- which means in almost every case the details of pediatricians from manual therapy. If we can
delivery, if we do not take into account the tiny demonstrate the efficiency of MTC in such a nec­
number of cases with trauma after birth. essarily very restricted context, this first step
Therefore it is possible in these cases to bridge opens the possibility of entering into a construc­
the gap between a rigorous enquiry on the one tive discussion beyond those who are already con­
hand and the taking into account of all relevant vinced or at least interested.
factors on the other hand. In the context of manual therapy in children,
As soon as the individual history starts to two different but interrelated topics have to be
diversify, such a synthetic view becomes almost dealt with. On the one hand, there is a clinical
impossible. In order to gain meaningful state­ and pathophysiological concept which needs to
ments we have to simplify more than may be good be defined in order to become a useful diagnos­
for the task at hand. Take, for example, something tic tool. To this end, the two acronyms of KISS
as 'simple' as headache - an indication par excel­ and KIDD were proposed and will be discussed
lence for manual therapy and excruciatingly com­ in Chapters 24 and 25. On the other hand, one
plex in its web of causal dependencies. has to choose the optimal method to deal with
If we were honest and serious we would have such a disorder once the diagnosis has been
to take into account all the other contributing fac­ confirmed.
tors relevant for the development of these com­ It seems to be useful to make it clear from the
plaints. The professional and private situation is beginning that there is no stringent connection
but the most obvious one of these contributing between the diagnostic and the therapeutic level.
factors. Other medication, endocrinologic details Most forms of manual therapy propose one method
and quite simply the age and type of the patient as the best (and only) solution, very often dismiss­
playa role, too. Last but not least we have to take ing other, similar techniques as vastly inferior. For
into account that not everybody considers a given the naive observer it is sometimes astonishing to see
problem serious enough to go and see a doctor, so that the methods proposed by the different schools

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are indeed very similar and that a distinction is present on both sides - and it is a mistake to think
sometimes a little bit artificial, to put it mildly. one can empathize with everybody. Manual ther­
There is - on the other hand - indeed a cormec­ apy necessitates an intimate bodily contact
tion between the theoretical considerations and between two strangers and the therapist as well as
their practical realization inasmuch as certain pro­ the patient should have the right to refuse.
cedures seem to be more promising than others.
But the bottom line of all advice about the recom­
mended techniques for manual therapy in children MTC INFLUEI\lCES BODY AI\lD SOUL
should be: Do not touch the cervical spine too often!
The closer one gets to the occipito-cervical junction, Since the famous 'je pense, donc je suis' of the seven­
the more time this highly volatile system needs to teenth-century philosopher Descartes (15%-1650),
adapt to the - therapeutic, but nevertheless irritat­ exploration of the natural world has gradually been
ing - input. Speransky (1950) wrote extensively freed from the constraints of religious dogma,
about the 'second hit phenomenon'. He pointed out thus enabling the ever faster development of the
that a sensitive structure - today we would talk natural sciences we see today. It is on the basis of
about a network - can handle a quite severe trauma this liberating Renaissance thought that all our
once, but decompensates if a similar second, much research stands (and it should not be forgotten
weaker trauma is encountered too soon afterwards. that even Newton, living a generation later than
Descartes, still devoted the bulk of his writing to
parts of science like astrology, i.e. topics we do not
THE ROLE OF THE THERAPIST classify as such nowadays).
The liberating influence of the Renaissance on
Observing different practitioners of manual ther­ philosophy and science (till then considered as
apy - be it chiropractors, doctors or physiothera­ one) can hardly be overestimated. But it came at a
pists - one quickly realizes that there are almost as price. As a preventive measure to avoid too much
many techniques as people practicing them. Apart scrutiny from the church authorities, Descartes
from the purely physical level, there is the 'philo­ postulated the separation of the spiritual realm
sophical' level, too. A 2 meter tall man with a and the body - the latter being accessible to our
background of orthopedic surgery will use differ­ investigation. The eternal soul was said to be dis­
ent techniques from a petite woman of 1.6 meters connected from the body's function and thus
who trained initially as a neuropediatrician. beyond our reach. An invisible barrier fenced off
All these different people may pretend to fol­ everything connected to the 'soul'.
low the same procedures, but what a difference. In the nineteenth century another boost to the
And let us not forget that in order to succeed, scientific understanding of our body came with
manual therapy has to rest on a base of confidence the ideas of Virchow (1821-1902), a German
and trust. The empathy necessary to achieve such pathologist who founded cellular pathology, thus
a solid person-to-person contact should come postulating a microscopically detectable alteration
spontaneously, but has to be fostered. It is better of cells as the basis of any pathological process
not to treat somebody where one senses a lack of (Virchow 1865). This approach led to enormous
trust. Already, therefore, it is indispensable to progress in hy giene and in the understanding of
have more than MTC at your disposal. Such a sit­ infectious and degenerative diseases - but again
uation arises only very rarely, but I consider it to at a price: functional disorders had almost no
be of paramount importance to be able to shrink place in this system.
from applying a manipulation when this basic An examination of these two milestones of
trust seems to be missing. The empathy has to be Western thought regarding the health sciences is

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Introduction 5

beyond the scope of this chapter, but it helps to THE LON G TRADITION OF MTC - AND
be aware of the context we work (and argue) in. WHERE WE ARE HEADIN G FOR
Repercussions of the separation of body and
soul in Western thinking abound, and in connec­ Manual therapy in children is an old craft and part
tion with the postulate of a morphological of the caregiving in almost all cultures, albeit with­
pathology at the root of every medical problem out explicit mention as a treatment of spinal disor­
this creates an unconscious censorship. 'Hard­ ders. Leboyer (1976) published a beautiful book
ware problems' fit into this pattern of thinking, about Indian baby massage where many treatments
'software problems' much less - and to accept have a striking similarity to techniques of MTC or
that a functional disorder can lead to a morpho­ soft-tissue osteopathy. Andry'S seminal book on
logically fixed pathology requires an even orthopedics (published in 1741) contains entire
greater effort. chapters about the treatment of newborn babies with
A good example is the ongoing discussion postural asymmetries and similar practices are doc­
about 'difficult' children. One indicator of the umented in books about massage (Baum 1906) or
trickiness of this problem is the changing general healthcare (Cramer et aI1990).
nomenclature applied to these children: an With the 'scientification' of medicine in the
entire collection of three-and four-letter words nineteenth century the earlier oral history of 'Be­
has been proposed over the years (MCD - mini­ handlung' (the German word for therapy, literally
mal cerebral damage, POS - psycho-organic syn­ translated: 'something done with the hands') in
drome, etc. ). Now the fashionable label is ADHD the sense of manual therapy began to be recorded
(attention deficit hyperactivity disorder) and in textbooks, albeit under various headings such
again we encounter a field much too big to be as massage, kneading the nerves, improving cir­
handled exhaustively here. But the problems culation. At that time, most explanations were
associated with and labeled as ADHD have a based on mechanical models. At the end of the
close connection with many of the phenomena nineteenth century the paradigms used to under­
we observe in children with problems originat­ stand the effects of these therapies were based on
ing in functional spinal disorders. In treating hydraulic or electric schemas. In the second half of
these children successfully one can at least alle­ the twentieth century the accent shifted to cyber­
viate the situation and thus give the families a netic or rather 'informatical' models - small sur­
new perspective. prise. The Zeitgeist inspires fashion in science, too.
The appeal of seeing metabolic problems as the So if one looks hard enough, there are morsels of
basis of these disorders can be traced back to the MTC to be found even a few centuries back, and
elegant possibility of not looking into the interde­ these scattered pieces of a big mosaic have many
pendence of mind and body, of individual and resemblances to the kind of MTC we support today.
environment, of nature and nurture. This bigger The basic difference can be found in the conceptual
view involves the observer in the process, be it the frame. The idea of a certain subgroup of children
worried parents or the therapist trying to help. tending to react distinctively to functional disorders
As in the treatment of migraine, we cannot get of the cervical spine came only after observing many
to the structural roots of the problem - we influ­ babies and their families and taking into account
ence trigger mechanisms and aggravating circum­ their long-term development. We realized that the
stances. But in doing so, manual therapy can more same trauma does not at all cause the same reaction
often than not help these cruldren and their fami­ in every child (and even less so in adults). We called
lies and provide the leeway necessary for a turn­ these babies 'KISS kids' to indicate\ that their prob­
around. Theiler, in Chapter 12, deals with some of lems were at least partly systematic. The patterns
these observations. we found first took us back to the moment of birth

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as an important trigger for these pathologies. Later MTC DEPENDS ON SUPPORTING

on we realized that to understand the situation fully, THERAPIES
one has to go back further, i.e. take into accOlmt the
prenatal development and the disposition inherited In the following chapters we try to present those
from the parents too - genetic or epigenetic. parts of manual therapy in (small) children that
Alerted by the early onset of vertebrogenic disor­ are different from the manual therapy we know in
ders, we started systematically to screen the case his­ adults and to develop the rationale for the con­
tories of older children. The picture that evolved led ceptual framework we propose for MTC. The
us to the formulation of KIDD, i.e. a sensorimotor main emphasis is on the systemic impact of appro­
disorder based on an early (and untreated) KISS priately applied manual therapy, thus preparing
pathology. As these children are of school-age and the ground for (re- )educating the sensorimotor
have encountered many more external influences system by means of ancillary specialties such as
than the babies suffering from KISS, their web of speech therapy or 'classic' physiotherapy.
pathology is much more complex. Whereas the To a superficial observer this manual therapy
chapter about KISS (Chapter 24) deals with a rather does not look very different from other forms of
well-defined symptomatology, the KIDD chapter contact treatment. We shall try to explain the crucial
(Chapter 25) discusses a much more complex Gestalt. distinctions which necessitate, on one hand, a
Two pieces of circumstantial evidence make us much more precise evaluation of the patient to be
surmise that KISS and KIDD influence the later treated and, on the other hand, sufficient time for
course, too. We see a lot of parents with their prob­ the patient to adapt to this therapeutic impulse.
lems after the babies have been treated success­ There is no sharp distinction between this vari­
fully, and we see the same patterns in these ety of manual therapy and other therapies dealing
problems. It goes without saying that in adults the with small children and using the upper cervical
situation is even more complex and difficult to spine as a primary starting point - quite a lot of
decipher than in adolescents, but with the knowl­ what we have to say is valid for these methods,
edge of what we found in their children, some too. But it would be imprecise to put all these
details are more evident than if the parents were methods in one big bag and treat them as inter­
treated independently. changeable options. One of the most important
T he gender of the parent who comes to seek differences - not least from the viewpoint of the
treatment is by no means accidental- which is the family concerned - is our intention to minimize
second clue. When the baby is a boy it is far more the impact of manual therapy on the small chil­
probable for the father to come later on, and the dren we treat as much as possible. Any therapist
same is true for daughter and mother. Quite often has to strive to be as unobtrusive as possible.
this gender-related predisposition extends into After more than 20 years of practical experience
the entire clan, viz. the uncle or the grandfather of we can say with some confidence that in the great
a baby boy who shows up. majority of cases very few treatments suffice (see
These interesting observations are very difficult Chapter 17). This does not mean that there is no
to verify in the context of a private consultation. But additional therapy complementing the initial
they are so clear-cut that even then one cannot but effect of manual therapy; but these therapies fol­
notice them. Much research needs to be done along low different procedures and are better summa­
these lines and it seems more than probable that this rized under the broad label of re-education. These
might help us to align our indications for manual approaches do indeed need frequent and long­
therapy in general and MTC more particularly with term application . Often the parents (or to be more
the framework of mainstream pediatrics. honest: the mothers) are trained to treat their chil-

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Introduction 7

dren on a daily b asis in order to make these environment an equally amazing influence on
approaches work. the developing neuromotor organization. We are
The most important aspect of this is to keep in about to learn how much our epigenetic pattern
mind that the situation in newborn babies is fun­ is for med in the perinatal period and how these
damentally different from what we know about few months determine large parts of the biogra­
adults or even from the situation in adolescents or phy of an individu al (Lopuhaa et al 2000, Rose­
older children. We shall not be successful in the boom et al 2000). We shall have to go back to this
analysis and treatment of the problems of the phenomenon time and again, as it influences
newborn if we are not aware of this. nearly all aspects of our interaction with these
H is not only the anatomy that is radically dif­ small human beings.
ferent. The most important discriminating factor is This book tries to bridge the gap between the
the absence of all 'learned' p atterns apart from the 'small' push on one side of the upper cervic al
few acquired in utero and during birth. This clean spine of a child and the vast effects triggered by
slate is an opportunity and a threat at the same this intervention at a crucial spot and an equally
time, enabling the newborn infant to develop very crucial point in time. The broad r ange of contribu­
rapidly - in both good and bad directions. tors should give the interested a firm foundation
Neurophysiological research suggests that we from which to get to grips with this complex situ­
start life with a far greater amount of neurons ation. We leave a lot of loose ends, and in the 3
and synapses than those we use as an adult. The years it took to finalize the book, quite a few bits
structuring depends on the appropriate use and of new information and ideas turned up to com­
non-use of these connections ('use it or lose it'), plete - and sometimes even correct - the concept.
thus giving the newborn baby an amazing vari­ In that sense we present 'work in progress' - but
ety of possible developmental p aths and the in medicine, who doesn't?


Andry de Bois rega rd N 1741 L'orthopedie ou l'art de Roseboom T J, van der Meulen J H, Osmond C et al 2000
prevenir et de ca r riger dans les en£ants les difformites du Coronary heart di sease after p r ena ta l exposure to the
co rps Vv Alix, Paris
. Dutch famine, 1944-45. Heart 84:595-598
Bum A 1906 Handbuch der Massage und Heilgymnastik. Sackett D, Richardson W, Rosenberg W et al 1997 Evidence­
Urban & Schwarzenberg, Berlin/Vienna based Medicine. Elsevier S ci enc e, New York
Cramer A, Doering j, Gutmann G 1 9 90 Geschichte der Speransky A D 1950 Grundlage n der Theori e der Medizin.
manuellen Medizin. Springer, Berlin Verl ag Werner Saenger, Berlin
Leboyer F 1976 Shantal a , un Art tr adi ti onel : Ie massage des Szent-Gyorgyi A 1972 What is life? Biology Today 24-26
enfants. Seuil, Paris Virchow R 1 865 Die Cellularpathologie in wer B egr u n dung
Lopuhaa C E, Roseboom T J, Osm ond C et al2000 Atopy, auf physiologische und pathologische Gewebelehre. A
lung function, and obstructive a irw ay s disease after Hischwald, Berlin
prenatal ex posure to famine. Thorax 55:555-561

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The theoretical base


2. Sensorimotor development of newborn and children from the viewpoint of manual

therapy 11

3. Development and topographical anatomy of the cervical spine 15

4. Development of the central nervous system 29

5. Adaptive properties of motor behavior 45

6. Neuromotor development in infancy and early childhood 57

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Chapter 2

Sensorimotor devel o p m ent of

n e wborn and children from the
viewpoint of manual therapy
H. Biedermann

On oublie rien de rien,

on s'habitue, c'est tout ...
Jacques BreI

All neurological development falls into two broad

categories: pattern generation and pattern recogni­
tion. Most of the internal processes are dependent
on a base rhythm, be it breathing or digestion.
These are two examples with extremely different
frequencies, the latter being coupled with the diur­
nal pattern and the former dependent on an inter­
nally generated pattern which undergoes multiple
adaptive influences until it is finally carried out.
It is of basic importance to come to grips with
the complexities of such a system based on an
internal pattern generator and the external modi­
fiers acting on it. The chapter by Ramirez (Chap­
ter 5) takes us to the cutting edge research of
micro-neurophysiology, and tries to unravel some
of the intricacies of pattern generation.
These mechanisms are very old and shared
between most vertebrates with only minor differ­
ences. The contribution of Huber (Chapter 6) on
the other side deals with the complexities of pat­
tern recognition and the surprising proficiency of
very small children in decoding complex visual
clues. From Huber we learn how early these abili­
ties are trained and how a basic pattern recognition
is established quite early in childhood. It is not too
surprising that the research group Huber belongs
to has not y et taken into account the influence that

1 1
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the proper functioning of the upper cervical spine in situations where other forms of therapy would
has on proprioception and head movement - these not work because the amount of discipline and
insights have only just reached neuropediatric persistence they require is not likely to be forth­
research. But Huber's chapter gives us some clues coming from the families concerned.
as to how disturbances in proprioceptive input Immersed in the treadmill of our daily work we
complicate the computation of spatial information. tend to forget what we learned during our studies
In Chapter 25 we examine some of the implications - and are not even aware of all the new informa­
of this concept for the treatment of behavioral and tion produced since we left university. One moti­
neuromotor problems in schoolchildren. vation behind this part of the book was to help in
The basic phenomenon - and the reason why dis­ overcoming this. The chapters by Huang and
turbances in the early stages of neuromotor devel­ Christ (Chapter 3) and Hori (Chapter 4) present
opment exert such a wide-ranging influence -lies in the state-of-the-art information concerning embry­
the realization that we rarely 'unlearn' an acquired ological development in the cervical area and the
pattern. As Jacques Brei says in his famous 'chan­ central nervous system and its deviations.
son', we don't forget anything, we just get used to it. This information should enable a better under­
So patterns acquired in early childhood can influ­ standing of the context in which we are working. A
ence our behavior years and decades later. This solid knowledge of the basic facts about anatomy
makes the understanding of neuromotor develop­ and neurophy siology will help us to improve our
ment at the beginning of our life so important. The diagnoses and especially to develop the 'sixth-sense'
postnatal period is paramount for our understand­ which alerts the diagnostician when an unusual
ing of this process, as it is the first time we are able situation is encountered. In discussions with col­
actively and directly to influence these develop­ leagues about the - rare - occasions when they
ments. found severe problems while examining children,
Onto this basic level of interaction many other almost all of them admitted that before they actually
influences are added, from the primal needs of identified the diagnostic problem they had had a
food and drink, to warmth and support in the all­ hunch that something was not quite as it should be.
important immersion in a stable and loving atmos­ The information contained in the following pages
phere in the baby's home, with as much bodily should help to alert one to these unusual cases.
contact as possible (Cattaneo et a11998, Cleary et al Or to put it another way, the chapters in Sec­
1997, Feldman et al 2002, Fohe et al 2000, Luding ­ tion 1 can be seen as an antidote against too much
ton-Hoe et a11991, Simkiss 1999, Tessier et aI1998). confidence of the style '1 am so successful that I
To cast the net even wider, one has to evaluate the don't bother about the details'. If we keep remind­
socioeconomic status of the family and its social ing ourselves how much there is to know about the
integration in a local community (Wilkinson 1996, incredibly complex web of dependencies we will
Wolf and Bruhn 1997) - a dimension of wellbeing maintain a healthy fear of overlooking something.
often overlooked or underestimated. This is even more important in MTC than in other
Even if we were able to take these aspects into specialties as there are times when one 'simple'
account when evaluating the child's future, we case seems to follow another, and lulled into a false
would not be in a situation to do much about it. sense of security with our 'diagnostic auto pilot' we
The big advantage of manual therapy in early might overlook the small sign that should warn us.

childhood is that it gives us an opportunity to Last but not least, these chapters (and Hori's in
improve the situation of a child without interfer­ particular) remind us about the differential diag­
ing with the other forms of help available and - nosis of all the phenomena that may comprise
last but not least - without a big investment in KISS - but may be a sign of quite another under­
time and energy. We are able to help children even lying pathology, too.

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Sensorimotor development of newborn and children 13


Cattaneo A, D a v anzo R, B ergm an N et al1998 Ka ng ar oo Luding ton- H oe S M, Hadeed A J, And erson G C 1991
mother care in l ow - income countries. International Ph ysiologic responses to skin-to-skin contact in
Network in Kangaroo Mother Care. Journal of Tropical hosp ital ized prem a ture in fants. J ournal of Pe rinat ol ogy
Pediatrics 44(5):279-282 11(1):19-24
Cl ea r y G M, Spinner S S, Gibson E et al 1997 Skin-to-skin Simkiss D E 1999 Kangaroo mother care. J ournal of Tropical
parenta l contact with fragile pret e rm infants. J ournal of Pedi atrics 45(4):192-194
the American Oste op athi c Association 97(8):457-460 Tessier R, Cristo M, Velez S et al1998 Kan garoo mothe r care
Feldman R, WeUer A, Sirota Let al 2002 Skin-to-skin contact and th e b onding h yp oth es is . Pediatrics 102(2):e17
(Kangaroo care) promotes self- regulation in premat ure Wilkinson R G 1996 Unhealthy societies : the afflictions of
infants: sleep-wake cy clicity, arousal modulation, an d inequality. Routle dge, London
sustained expl oration. Developmental Psychology Wolf S, Bruhn JG 1997 The power of clan: the influence of
38(2): 194-207 human relationships on heart disease. Trans action,
F ohe K, Kropf S, Avenarius S 2000 S kin- to-skin contact London
improves gas exc hange in premature infants. Journal of
Perinatology 20(5):311-315

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Chapter 3 --------�-- �

Development and topographical

anatomy of the cervical spine
R. Huang, B. Christ

'The neck, cervix (collum), is a mobile connecting

CHAPTER CONTENTS structure between head and trunk. The supp or t ­
ing element of the neck is the cervical spine ( cer ­
Prenatal development 16
vical spinal column), the most cranial part of the
Primary segmentation and somite
vertebral column. The vertebral column and parts
format i on 16
of the cranium represent the axial structures of the
Secondary segmentation (resegmentation)
human body. The vertebral column comprises 33
and somite differentiation 18
vertebral segments, vertebrae, connected to each
Segmental identity 20
other by fibrocartilaginous intervertebral disks,
Postnatal development 21
ligaments and muscles. Its function is to support
Ossification of the cervical vertebrae 21
the trunk and protect the spinal cord. The cervical
Development of the uncovertebral joint 22
spine provides a morphological basis for an exten­
Development of curvatures of the
sive freedom of head movement. In addi tion, the
cervical spine 22
cervical vertebral column serves as a bridge for
Topography 23
numerous blood and l ymphati c vessels and
Conclusion 26
nerves, link ing head, trunk and upper limb.
Developmental abnormalities of the cervical
vertebral column can affect these functions. For
example, the Klip pel-Feil syndrome, in which a
short cervical vertebral column develops, is char­
acterized by a red uction of head mob ility, mig r a in e
headache and paresthesia of the ar m and hand.
Further examples of vertebral abnormalities are
cervical ribs and spina bifida, atlas assimilation
and fused vertebrae.
In the thoracic vertebral column, the costal
processes grow laterally to form a series of ribs.
The costal processes normally do not extend dis­
tally in the cervical vertebral column, but occa­
sionally they do so in the case of the seventh
cervical vertebra, even developing costovertebral

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joints. Such cervical ribs may even reach the ster­ 'vertebrae', the definitive structures of the verte­
num. Neural arches and their ligaments form a bral column. The development of the vertebral
protective roof over the vertebral canal for the column reveals a primary segmentation (the
spinal cord. Occasionally the coalescence of verte­ somite formation) and secondary segmentation
bral laminae is incomplete, a cleft of variable (resegmentation of the vertebral coluum). The
width being left through which dura and arach­ specification of the vertebrae is controlled by a
noid mater may protrude. Part of the spinal cord genetic program, namely the Hox genes. The pri­
with its pia mater also commonly projects, a con­ mary and secondary segmentation and the seg­
dition known as spina bifida. mental specification will be discussed in the next
The malformation is more common in the lum­ section.
bosacral regions, but may also occur at thoracic or
cervical levels. Fusion of two or more vertebrae Primary segmentation and somite
may occasionally be observed in the developing formation
vertebral column. The atlas, normally forming an
articulation between the cranial end of the verte­ The occipital bone, the vertebral column and their
bral column and the head, may fuse with the skeletal musculature develop commonly from a
occipital bone, so-called atlas assimilation or compartment of the intermediate layer (meso­
occipitalization of the first cervical vertebra. An derm) (Fig. 3.1). This can be divided into paraxial
understanding of normal development and mesoderm, intermediate mesoderm and the lat­
topography of the cervical vertebral column could eral plate mesoderm. The paraxial mesoderm
help in understanding the basis for such vertebral flanks the axial organs (neural tube and noto­
abnormalities and their symptoms. chord). It consists of a preotical part, located cra­
nially to the ear placode, and a postotical part,
extending caudally from the ear placode into the
PRENATAL DEVELOPMENT neck and the trunk. The postotical paraxial meso­
derm becomes segmented, while the prcotical part
The most specialized part of the cervical vertebral does not. Segmentation of the paraxial mesoderm
column is the cervico-occipital transitional region. is characterized by somite formation. The somites
Striking features of this region are already appar­ are the first clearly delineated segmental units.
ent during development. Although the posterior They are formed in pairs by epithelialization from
part of the cranium and the vertebral column the paraxial mesoderm. The first somite pair
derive from the same primordium, a boundary arises directly behind the ear placode and the fur­
develops between the head and the neck. The pri­ ther somites develop one by one in a craniocaudal
mordium located cranially to this boundary is direction. New mesenchymal cells enter the
included in the development of the head. The cer­ paraxial mesoderm at its caudal end as a conse­
vico-occipital transitional region represents a very quence of gastrulation. The newly formed parax­
special body part that not only provides the mate­ ial mesoderm is not immediately segmented. The
rial for the formation of the axial skeleton but also part of the paraxial mesoderm prior to somite for­
participates in the development of essential mation is called the segmental plate or presomitic
organs such as heart, gastrointestinal tract, and mesoderm.
kidney. The fundamental prerequisite for somite forma­
The vertebral column develops from somites, tion is the growth of the paraxial mesoderm. This
the first visible segmental units of the embryo. In growth is controlled by gastrulation genes and the
older papers the somites have been called 'pro­ fibroblast growth factor 8 (FGF-8) that is produced
tovertebrae' and therefore have been related to the in the caudal part of the segmental plate. The

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Develo p m ent and to p ographica l anato my of the c ervica l spin e 17

A c
Figure 3.1 A: Pax-l expressio n in t h e som ites of a 2-day-old chick embryo. The arrow marks the boun dary between
the newly formed so m ite and the seg m ental plate. B: Tran sverse section th roug h a cervical somite. C: Transverse
section thro u gh a 3-d ay-old chick embryo. Division of the somite in a derm omyotome (d m ) and a scleroto m e (sc).
Expression of Pax-l in sclerotome. ao, aorta; ec, ectoderm; en, endoderm; n c, notochord ; nt, neural tube; S, so m ite;
w, Wolff's duct; Ipm, lateral plate m esod erm .

quantity of FGF-8 secretion determines the size of each segmental plate cell before it becomes inte­
the developing somite (Dubrulle et al 2001). grated in a somite at its cranial end.
Segmentation was found to be controlled by a The gene oscillation leads to a maturation of
molecular mechanism called the 'segmentation the segmental plate. Morphologically, this matu­
clock' (Pourquie 20(0). This clock contains molec­ ration is characterized by a cell condensation and
ular oscillators that are characterized by the rhyth­ a mesenchymal-to-epithelial transition of the cells
mic production of mRNAs. The hai ry, lunatic
' in the cranial part of the segmental plate. The
fringe' gene and genes of the Delta-Notch signal­ epithelialization requires the ex p ressi on of the
ing pathway belong to these segmentation genes. bHLH gene paraxis (Burgess et al 1996). Epithe­
The expression pattern of these genes appears as lialization of the segmental plate mesoderm and
waves that roll through the segmental plate from somite formation are severely affected in para xis
its caudal to its cranial end, and each wave is initi­ n ull mutant mice. As a consequence, these mice

ated once during formation of one somite. This develop a vertebral column that is not regularly
means that these genes are expressed 12 times in segmented.

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Secondary segmentation expressed in the somitocoel cells and the ventral

(resegmentation) and somite somite half (Fig. 3.1). This leads to an epithelio­
differentiation mesenchymal transition of this somite part. Their
cells form the mesenchymal sclerotome which
Remak (1850), who was studying whole mount gives rise to basioccipital bone vertebrae, inter­

chick embryos, made the observation that the vertebral disks and ribs. Dorsal signals are
boundaries of the definitive vertebrae are shifted derived from both the surface ectoderm and the
one half segment as compared to those of the dorsal neural tube, which belongs to the Wnt fam­
'protovertebrae' (somites). This so-called 'Neug­ ily of genes. Wnt-l and Wnt-3a are expressed in
lieder ung (resegmentation) was observed in vari­
' the dorsal neural tube and Wnt-6 in the ectoderm.
ous species and was thought to be achieved by a These signals promote the devel opment of the
new combination of somite halves. A secondary dorsal compartment which keeps its epithelial
segmentation appears within each somite: an structure and forms the dermomyotome. Pax-3
intrasegmental fissure divides its ventral compart­ and Pax-7 are expressed by their cells. Cells
ment, the sclerotome, into a cranial and caudal located in the four edges of the dermomyotome
half and marks the boundary of the definitive ver­ de-epithelialize and elongate in a longitudinal
tebra. This means that the fusion of the caudal half direction. These cells differentiate into myogenic
of one sclerotome \vith the cranial half of the next cells and form a cell layer, the myotome, between
one forms one vertebra. Two neighboring verte­ dermomyotome and sclerotome. Both ventral
brae are thereafter articulated by an intervertebral ( Shh ) and dorsal signals (Wnt proteins) are
disk whose primordium is situated caud ally to an required for the specification of myogenic cells in
intrasegmental fissure, the so-called von Ebner fis­ the epaxial domain of the somite.
sure (von Ebner 1889). Muscle cells develop from The sclerotome divides into a cranial and a cau­
the dorsal compartment of the somite, the der­ dal half along the longit u dinal axis (Fig. 3.2).
momyotome, and are not affected by this craniocau­ Determination of this craniocaudal polarization is
da! subdivision. Muscles derived from one somite acquired prior to somite formation in the cranial
are therefore attached to two adjacent vertebrae. portion of the segmental plate and depends on the
This means that resegmentation is required for Delta/Notch signaling pathway. The prospective
appropriate movement of the vertebral column.
To form a functional vertebral column, so mites
undergo a dorsoventral and a craniocaudal com­
partmentalization. Newly formed somites are
masses of mesodermal cells with a small cavity in
the middle, the somitocoel (Fig. 3.1). The cells are
arranged epithelially and radially arround the
somitocoel, which is occupied by mese nchymal
cells. Extracellular matrix connects the somite to
adjacent structures (neu ral tube, notochord, ecto­
derm, endoderm, aorta, Wolffian duct). A continu­
ous cell layer connects the lateral portion of the
somite to the intermediate mesoderm and thus Figure 3.2 Sag ittal section s throu g h the m etam eric
primord ium of th e sp i nal gan g lia (A) an d the spinal
indi rectl y to the lateral plate mesoderm. Under
n e rve s (B). The nerve placod e is visualized with an tibody

the influence of ventralizing signals such as Sonic d m , dermomyotome; m, myotom e; the brackets mark the
hedgehog (Shh) from the notochord and the floor cau dal sclerotome ha l ve s an d th e arrows the bound ary
plate of the neural tube, Pax-l and Pax-9 become between two adjace n t somites.

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Development and topographical anatomy of the cervical spine 19

somitic halves can be identified by the expression form the dorsal mesenchyme which contributes to
domains of various genes. Delta 1, Mesp1,2 are the dorsal part of the neural arch and the spinous
expressed in the caudal half and EphA4 in the cra­ process. Msxl and Msx2 have been found to be
nial half of the prospective somites in the cranial expressed in this mesenchyme and to be con­
part of the segmental plate. The craniocaudal trolled by the roof plate of the neural tube and
compartmentalization is indispensable for the possibly the surface ectoderm via BMP4 signaling.
development of the metameric vertebral column Interruption of this cross-talk could be one of the
and for the secondary metamerism of the periph­ reasons for the malformations of the dorsal verte­
eral nervous system. Different genes are activated bral column, such as spina bifida. Pax-3 is
in the cranial and caudal sclerotome halves. The expressed in the dorsal neural tube and in Splotch
transmembrane protein ephrin and the Eph recep­ mice in which the homeobox domain of the Pax-3
tors are important molecules of these compart­ gene is mutated, the development of the dorsal
ments. Eph receptor is situated in the cell membrane neural tube is affected, resulting in the formation
of the migrating neural crest cells, while ephrin is of a spina bifida.
expressed exclusively in the caudal sclerotome The fate of the cells in the ventrolateral angle of
half. The interaction between ephrin and its recep­ the sclerotome remains to be studied. These cells
tor stops the migration of neural crest cells. So the are located in the transitional region of the parax­
axons of motor nerves and the neural crest cells ial to the intermediate mesoderm and might con­
forming the dorsal root ganglia invade the cranial tribute to kidney formation. In addition, these
half-segment whereas the caudal half-segment acts cells could represent a cell population that partic­
as a barrier to axon and neural crest cell invasion. ipates in the development of the ribs. Recent stud­
Uncx4.1 is expressed in the caudal sclerotome ies have suggested a two-stage model of rib
half and is essential for the formation of the neu­ development. In the first instance, Shh emanating
ral arch. When Uncx4.1 function is lost experi­ from the axial structures induces the development
mentally, the neural arch cannot be formed and of the sclerotome and also the expression of Fgf-S
the dorsal root ganglia fuse together to form an in the myotome. Secondly, the ventrolateral
unsegmented cell mass next to the spinal cord. domain of the sclerotome becomes expanded, con­
As discussed above, the sclerotome is the deriv­ trolled by FGFs secreted by myotome cells.
ative of the ventral half of the somite epithelium The vertebral disks located between adjacent
and the mesenchymal somitocoel cells. Ventral surfaces of vertebral bodies from C2 (axis) to the
signals are able to induce the expression of Pax-1 sacrum are the main junction between the verte­
and Pax-9 in the sclerotome. However, it has to be bral bodies. Each disk consists of an outer lami­
kept in mind that only the ventromedial part of nated annulus fibrosus and an inner nucleus
the sclerotome continues to express Pax-1 and Pax - pulposus. The intervertebral disk is derived from
9. Sclerotome cells that do not express these Pax­ somitocoel cells (Huang et a11994, 1996). The cells
genes are situated at the ventrolateral and the of the intervertebral disk still express Pax-I when
dorsomedial angles of the sclerotome. Pax-I-posi­ it is already downregulated in the vertebral body
tive cells of the ventromedial sclerotome migrate anlagen. Pax-1 expression is most likely to pro­
into the initially cell-free perinotochordal space to mote proliferation of disk cells (Wilting et aI1995).
form the mesenchymal perinotochordal tube, An early downregulation of Pax-expression is
which develops into the vertebral bodies and observed in the basioccipital germ, in which the
intervertebral disks. disk primodia degenera te leading to a fusion of
The fate of the cells in the dorsomedial angle is the chondrogenic vertebral anlagen. Pathologi­
not quite clear. Grafting experiments indicate that cally fused vertebrae can occasionally arise after
these cells migrate in a dorsomedial direction to an early downregulation of Pax-I expression. In

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the late development, the notochord disappears second (axis) have special features and differ
from the vertebral bodies and expands into the greatly from the other cervical vertebrae. The atlas
condensed mesenchymal primordia of the inter­ consists of two lateral masses connected by a short
vertebral disks. In the adult, the notochord persists anterior and a longer posterior arch. The trans­
as nucleus pulposus, while somitocoel-derived verse ligament retains the dens against the ante­
mesodermal cells form the annulus fibrosus of the rior arch. The transverse processes are longer than
in tervertebraldisk. those of all cervical vertebrae except the seventh
The morphogenesis of the vertebral column vertebra. They act as strong levers for the short
reflects the development of the vertebral motion neck muscles, making fine adjustments for keep­
segment. The vertebral motion segment is a func­ ing the head balanced. The axis is an axle for rota­
tional entity consisting of two adjacent vertebrae, tion of the atlas and head around the dens, which
the intervertebral disk, ligaments, and muscles projects cranially from the axis body. The third to
that act on the segment (Schmorl and Junghanns sixth cervical vertebrae have small, relatively
1968). Therefore, one vertebra is part of two adja­ broad vertebral bodies, and short and bifid spin­
cent motion segments. The motion segment also ous processes. The seventh cervical vertebra has a
includes spinal nerves and blood vessels. The rela­ long spinous process.
tionship between the somite and the motion seg­ As described above, each cervical vertebra has
ment has been investigated by using the biological its own identity, so-called segmental identity. The
cell tracing method of quail-chick chimeras segmental individualization of sclerotomal deriv­
(Huang et al 1996, 2000a, 2000b). Skeletal ele­ atives along the craniocaudal axis is already deter­
ments, ligaments, muscle, and connective tissue of mined in the segmental plate. When cervical
a motion segment originate from one somite. somites are grafted into the thoracic region, ribs
Somitocoel cells give rise to primordial material of and scapula do not develop in this thoracic region
the intervertebral disks and are positioned in the (Kieny et al 1972).
articulation part of the motion segment. The inter­ Each newly formed somite is identical to every
segmental muscle is made up of myogenic cells other somite, in so far as it gives rise to the same
from one somite, whereas the superficial segment­ cell types (muscle, bone, dermis, endothelial
overlapping muscle consists of myogenic cells cells). The developmental fate of somites at differ­
from several somites. ent axial levels has been found to be determined
by the Hox genes, which include at least 38 mem­
Segmental identity bers representing 13 paralogous groups aligned in
four clusters (a-d). Expression of the Hox genes
The vertebral column consists of 7 cervical, 12 tho­ begins dynamically in the prospective somites
racic, 5 lumbar, 5 sacral and 4 coccygeal vertebrae. and persists stably in the somite until the begin­
The cervical vertebrae show very special charac­ ning of chondrification in the primordia of the
teristics. For example, the seven cervical vertebrae vertebrae. Hox genes show a cranial-to-caudal
are typified by a foramen in each transverse expression pattern with a sequence of cranial expres­
process. The vertebral artery and its vein run sion boundaries that corresponds to their align­
through the foramina. Furthermore, the cervical ment on the chromosomes (Duboule and Dolle
pedicles and laminae enclose a large, roughly tri­ 1989). The identity of the vertebrae may be speci­
angular vertebral foramen, forming a channel for fied by a unique combination of Hox genes, called
the spinal cord. the Hox code (Kessel and Gruss 1991).
Comparing the seven cervical vertebrae with For example, in the mouse the atlas is charac­
each other, one can find conspicuous differences terized by the expression of Hoxb-l, Hoxa-1, Hoxa-
in size and shape. In particular, the first (atlas) and 3 and Hoxd-4. The axis is specified by these four,

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Deve l op m ent and top ographical anatomy of the cervica l s p ine 21

plus Hoxa-4 and Hoxb-4. Changes in Hox gene notochord between the basioccipital and the dens
expression lead to a homeotic transformation of axis forms a ligament, the apical ligament of dens.
the vertebrae. When Hox-l.l transgene was intro­ The third, fourth, fifth, sixth and seven cervical
duced into the germline of mice, the cranial part of vertebrae derive from sclerotome halves of two
the vertebral column was posteriorized. The base adjacent cervical somites, respectively.
of the occipital bone was transformed into a verte­
bra (proatlas), and the atlas was fused with its cen­
trum, resulting in an axis that did not possess an POSTNATAL DEVELOPMENT
odontoid process.
The question of how Hox genes are regulated The structure of the vertebral column undergoes
and how they act on the behavior of sclerotome progressive change in the postnatal period, affect­
cells remains to be studied. It has been shown that ing its growth and morphology. This process con­
retinoic acid controls the activity of Hox genes. tinues in adulthood. Vertebral column
Application of retinoic acid can cause cranial or morphology is influenced externally by mechani­
caudal level shifts in the overall segmental organ­ cal as well as environmental factors and internally
ization of the vertebrae. It has been suggested that by genetic, metabolic and hormonal factors. These
Hox genes regulate downstream genes that control all affect its ability to react to dynamic forces, such
the level-specific identity. These genes determine as compression, traction and shear. The postnatal
the proliferation, apoptosis, migration and differ­ development of the cervical spine will be dis­
entiation of sclerotome cells. cussed here from different aspects, such as ossifi­
As discussed above, the basioccipital bone and cation, uncovertebral articulation and curvatures.
spine generally develop from the somites. The
boundary between these two axial structures is Ossification of the cervical vertebrae
located in the middle of somite 5. Thus, sclero­
tome of the first 4.5 somites lose their segmental A typical cervical vertebra consists of hyaline car­
characteristic and fuse to form a skeletal mass, the tilage with three separate primary ossification
basioccipital bone. This process coincides with a centers, which appear in the ninth to tenth week
downregulation of Pax-l in the intervertebral after birth. One is located in each half of the verte­
disks (Wilting et al 1995). The atlas and the axis bral arch and the other one in the body. Centers in
differ not only in their morphology but also in the arches appear at the roots of the transverse
their development from the typical vertebra. The processes and from there the ossification spreads
typical vertebra is formed by two adjacent somite backwards, forwards, upwards, downwards and
halves. However, the atlas is formed only by the laterally into the adjacent parts of the vertebra.
caudal half of somite 5, while the axis arises from The major part of the body, the centrum, ossifies
three somites: the caudal half of somite 5, the from a primary center located dorsally to the noto­
whole of somite 6 and the cranial half of somite 7. chord.
So the axis can be considered as the result of the The atlas is normally ossified from three cen­
fusion of two vertebrae. The cranial part of the ters. Each lateral mass has one ossification center
axis derives from the caudal half of somite 5 and at about the seventh week. Both centers extend
the cranial half of somite 6, while the caudal part gradually into the posterior arch and fuse
originates from the caudal half of somite 6 and the together between the third and fourth year. The
cranial half of somite 7. The fusion of these two third center appears in the anterior arch at the
vertebrae is due to the degeneration of the original end of the first year and fuses with the lateral
intervertebral disk between them during develop­ masses between the sixth and eighth year. Ossifi­
ment (Huang et al 2000a, Wilting et al 1995). The cation of the axis is more complex (Ogden 1984).

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It has five primary and two secondary centers. fissure begins to form first at the age of 9 years.
Each vertebral arch and the body is ossified from The annulus fibrosus is torn in its lateral part
one center, as in a typical vertebra. The two cen­ under the influence of gliding by vertebral rota­
ters in the vertebral arch appear about the sev­ tion. This tearing occurs in normal tissue and can­
enth or eighth week, and the one in the body not be considered a degeneration phenomenon of
about the fourth or fifth month. The dens is ossi­ the intervertebral disk. It seems to be a prerequi­
fied from two primary and two secondary bilat­ site for the extensive cervical vertebral rotation.
eral centers. The primary centers of the dens The tear extends from the peripheral to central
appear about the sixth month and are separated region. Finally the cells of the nucleus pulposus
from the center in the vertebral body by a carti­ come out of the disk through the fissure. While at
laginous region. The primary centers of the dens the age of 18-20 years, one can still find intact
and the body most often fuse between the fifth intervertebral disks in the cervical vertebral col­
and eighth years, but sometimes even later, at umn, after the age of 20 years, each cervical inter­
about the twelfth year. Before fusion of these vertebral disk reveals a fissure.
three centers, the synchondrosis between them is The uncinate process develops almost synchro­
situated below the level of the atlantoaxial joints. nously with the uncovertebral fissure. At the age
It must be distinguished from a fracture, which of 9 years the bone tissue of the neural arch rises
usually spreads along this structure in infants and up adjacent to the lateral lip of the upper surface
children. Two secondary ossification centers, so­ of the vertebral body. At the end of the prolifera­
called ossiculum terminale, appear in the apex of tion period, the uncinate process has a shovel­
the dens at 8-10 years. Fusion of the ossiculum shaped bony ridge and fuses with the vertebral
terminale with the rest of the dens occurs body. Thus the superior surface of the vertebral
between the tenth and thirteenth years. body is saddle-shaped, while the inferior surface
is flat or minimally concave. The intervertebral
Development of the uncovertebral disk, which is split into cranial and caudal halves
joint by the uncovertebral fissure, forms a gliding sur­
face on the two adjacent vertebral bodies. So an
At birth the intervertebral disks are composed uncovertebral joint forms betvveen two adjacent
mainly of the nucleus pulposus. It is a large, soft, vertebral bodies. This articulation makes the
gelatinous structure of mucoid material with a extensive mobility of the cervical spine easier.
few multinucleated notochord cells, invaded also
by cells and fibers from the inner zone of the adja­ Development of curvatures of the
cent annulus fibrosus. Notochordal cells disap­ cervical spine
pear in the first decade, followed by gradual
replacement of mucoid material by fibrocartilage, In the normal vertebral column, there are no lat­
mainly derived from the annulus fibrosus and the eral curvatures, but 5-shaped curvatures are seen
hyaline cartilaginous plate adjoining vertebral in the sagittal plane. Curvatures appear as a
bodies. The nucleus pulposus becomes much response to fetal movements as early as 7 weeks in
reduced in the adult as the annulus fibrosus devel­ utero. Primary thoracic and pelvic curves are due
ops. A further characteristic feature of the devel­ to the bending posture of the embryo. Muscle
oping cervical vertebral column is a gradual development leads to the early appearance of sec­
appearance of a cross-fissure in the intervertebral ondary cervical and lumbar spinal curvatures.
disk (Tbndury 1958). After examination of over However, the vertebral column has no fixed cur­
150 cervical vertebral columns, Tondury made the vatures in the neonate. It is so flexible that when
observation that this so-called uncovertebral dissected free from the body it can easily be bent

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Development and topographical anatomy of the cervical spine 23

into a perfect half circle. The cervical curvature parts: splenius cervicis and splenius capitis. The
develops when the head can be held erect from 3 splenius cervicis muscle joins the levator scapulae
months of age onwards and the lumbar curvature muscle to share its attachments to the transverse
when walking starts from 1 y ear of age onwards. processes CCC4. The splenius capitis shares the
In adults, the cervical curve is bent forwards form­ attachments of the sternocleidomastoid muscle to
ing a lordosis. It extends from the atlas to the sec­ the superior nuchal line and the mastoid process.
ond thoracic vertebra, with its apex between the The semispinalis capitis muscle is located beneath
fourth and the fifth cervical vertebrae. the splenius muscle. The semispinalis capitis mus­
cle passes from the upper thoracic and lower cer­
vical transverse processes (C4 to T 5) to the
TOPOGRAPHY occipital bone between the superior and inferior
nuchal lines.
The neck is the bridge between head and trunk. The semispinalis cervicis and the suboccipital
Great vessels and nerves as well as the visceral muscles are located beneath the semispinalis capi­
structures run through the neck. The vertebral tis muscle (Fig. 3.3B). The semispinalis cervicis
arteries, the important arteries of the brain, are muscle arises from the transverse process of T 6-C7
topographically the closest vessels to the cervical and inserts into the cervical spinous processes
spine. The vertebral artery arises from the subcla­ (C6-C2)·
vian artery, ascends caudocraniaUy, and finally The suboccipital muscles are shown in Figure
enters the foramen transversarium of vertebra C6. 3.3B and C. The rectus capitis posterior minor
The artery passes through the foramina of the cer­ muscle arises from the posterior tubercle of the
vical transverse processes of CIi-C1, curves medi­ atlas, the rectus capitis posterior major muscle
ally behind the lateral mass of the atlas and then from the spinous process of the axis. These two
enters the cranium via the foramen magnum. muscles are attached side by side to the occipital
OccaSionally, it may enter the bone at the fourth, bone between the inferior nuchal line and the
fifth or seventh cervical transverse foramen. Its foramen magnum. The obliquus capitis inferior
vein passes through the same pathway as the muscle passes from the spinous process of the axis
artery. obliquely upward and forward to the tip of the
The cervical spinal nerves are also topographi­ transverse process of the atlas. The obliquus capi­
cally very closely related to the cervical spine. tis superior muscle passes from the tip of the
Their dorsal rami originate just beyond the spinal transverse process of the atlas obliquely upward
ganglion and pass backward on the side of the and backward to be inserted between the two
superior articular process. They supply the skin nuchal lines of the occipital bone.
and the deep (intrinsic) muscles of the back. Deep The four suboccipital muscles are very well
muscles of the back developed from the epaxial innervated (Voss 1958). They have many more
my otome (see above in the section on secondary muscle spindles than other neck muscles and are
segmentation and somite differentiation) are able to precisely inform the position of the head in
found dorsally to the cervical vertebral column. relation to the neck. These muscles are innervated
The topography of these muscles is shown in a by the suboccipital nerve, the dorsal ramus of the
dissection of a fetus (Fig. 3.3). The splenius muscle first cervical spinal nerve. It emerges between the
(Fig. 3.3A) wraps around the other deep muscles occipital bone and the atlas, and then reaches its
in the neck, as its name implies (Latin: splenius = target muscles.
a bandage). It arises from the lower half of the lig­ The great occipital nerve, the dorsal ramus of
amentum nuchae and from the upper thoracic the second cervical spinal nerve, emerges between
spinous processes. The muscle separates into two the posterior arch of the atlas and the lamina of

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the axis (Fig. 3.30), below the inferior oblique externa. Ca udally they have a discontinuous
muscle (Fig. 3.3C). It then ascends between the attachment to the clavicle. Both of them are
inferior oblique and semispinalis capitis muscles, enveloped in the superficial lamina of the cervical
and pierces the occipital attachments of the semi­ fascia.
spinalis capitis and the trapezius muscles. It sup­ The ventral rami of the upper four cervical
plies the skin of the scalp as far as the vertex. spinal nerves form the cervical plexus. It supplies
The trapezius and the sternocleidomastoid some neck muscles, the diaphragm and areas of
muscles are superficial cervical muscles of the the skin in the head, neck and chest. The superfi­
neck. Both of them are split from one sheet of cial branches of the cervical plexus perforate the
embryonic muscle that originates from the higher cervical fascia behind the sternocleidomastoid
cervical somites. Both muscles are innervated by muscle to supply the skin of the occipital and cer­
the accessory nerve. Cranially, these two muscles vical region, while the deep branches (ansa cervi­
have a continuous attachment extending from the calis and phrenicus nerve) supply infrahyoid and
mastoid process to the protuberantia occipitalis diaphragm muscles. The s uper ficial branches are

Figure 3.3 Dissection of a fetal neck. A: Semispinalis capitis muscle (1). B: Suboccipital muscles (4-7). C, D:
Topography of the great occipital nerve (arrows). 2, caudal part of transversally cut semispinalis capitis muscle;
3, semispinalis cervicis muscle; 4, rectus capitis posterior minor muscle; 5, rectus capitis posterior major muscle;
6, obliquus capitis inferior muscle; 7, obliquus capitis superior muscle; Ax, the spinous process of the axis; At, the
posterior arch of the atlas; 0, occipital bone; S, scapula.

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D e v e l op m ent a n d topogra ph i c a l ana tomy of the ce rvi c a l sp i ne 25

lesser occip i tal (C2), grea ter auricular (C2, C3), the p revertebral cerv ical fascia l a terally to the
transverse cu taneous nerve of the neck (C2, C3) omohyoid muscle. Our study of the developmen t
and supraclavicular nerves (C3, C4) . of avian tongue muscles showed th a t the inirahy­
The ventral rami of the lower four cervica l and oid muscles a re formed b y the myogenic cells
the first thoracic sp inal nerves tie into the brachial migrating from the occipital and higher cervical
plex us, which supplies the sho ulder gi rdle and somites, like the in trinsic tongue m uscles (Huang
upper limb muscles . The brachial p lexus emerges et al 1999). Th us they a re innerva ted by the
between the sca leni an terior and medius tha t arise hypoglossal nerve and the ansa cervica lis.
from the upper cervical transverse processes and The carotid shea th is a condensation of the pre­
descend to the fi rst rib . Inferior to the bra chial tracheal lamina of the cervical fascia a round the
plexus, the subclavian artery also p asses through common and internal carotid ar teries, the in ternal
the gap between the sca leni anterior an d med ius. j ugular vein, and the vagus nerve. The common
In the case of a cervical r ib the scaleni gap could carotid arteries originate from the brachiocephalic
become narrow, leading to a compression of the trunk (righ t carotid artery) and direc tly from the
brachial pl exus. aortic arch (left carotid artery). The carotid a r teries
While the dorsal neck muscula ture i s rela tively ascend to the thyroid car tila ge'S upper border,
compact, the ven tral one is d ivided into several where they divide in to ex ternal and internal
la yers and enveloped by three lamina o f the cervi­ carotid arteries. The internal j ugular vein collects
cal fa scia . The superficial lamina of the cervical blood from the skull, brain, face and neck . It begins
fascia is con tinuous with the ligamen tum nuchae. at the cranial base in the j ugular foramen and
It forms a thin covering for the trapezius muscle, descends in the caroti d shea th, j oining with the
covers the posterior triangle of the neck, encloses subclavian vein . The vagus nerve descends verti­
the s ternocleidomas toid musc le, covers the ante­ cally in the neck in the carotid sheath . After emerg­
rior triangle of the neck and reaches forwards to ing from the j u gular foramen the vagus has two
the midline . Here i t meets the corresponding lam­ enlargemen ts, the superior and inferior gangl ion .
ina from the opposite side. The prevertebral lamina of the cervical fascia
The pretracheal lamina of the cervical fa scia is covers the deep anterior vertebral m u scles and
very thin, and provides a fine fascial shea th for the exten d s la terally on the scalenus an teri or, scalenus
infra hyoid muscles. The fo ur paired infrahyoid medi u s and leva tor scapulae m u scles . Deep ante­
muscles a re dep ressors of the larynx and hyoid rior cervical m u scles a re the longus colli (cervicis)
bone. The sternohyoid and omohyoid muscles and longus capitis muscles. The longus colli m us­
a ttach side by side to the hyoid b ody. The s ter­ cle extends from the body o f the third thoracic ver­
nohyoid runs down to the posterior aspect of the tebra to the anterior tubercle of the a tlas, and i t is
capsu le of the sternoclav icular joint and adjacent a ttached to the bodies of the verteb rae in between .
bone. The omohyoid muscle leaves the s ternohy­ The longus capitis muscle arises from the third,
oid m uscle abruptly below the level of the cricoid fourth, fifth and six th anterior tubercles and
cartilage, passes benea th the sternocleidomastoid ascends to the basioccipital bone to b e a ttached
muscle, and crosses the posterior triangle to the behind the plane o f the pharyngeal tubercle.
upper border of the scapula. The th yrohyoid mus­ The cervical sympa thetic trunk is an upward
cle extends upward to the grea ter horn and the extension of the thoracic sympa thetic nerves . It
body of the hyoid bone . The sterno thyro id muscle ascends through the neck between the longus colli
converges on i ts fel low as i t descends, until their muscle and the prevertebra l lamina of the cervical
medial borders mee t at the cen ter of the posterior fascia. It has three in terconnected gangli a . The
surface of the manubri um. The pre tracheal cervi­ superior cervical ganglion is located at the level o f
cal fa scia envelops these m uscles and attaches to the second and third cervical verteb rae . The mi ddle

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one is usually found at the sixth cervical ver tebra cricoid cartilage corresponds to the level o f the
level. The third one i s the cervico-thoracic gan­ intervertebra l disk between the sixth and seventh
gl ion, which lies between the seventh cervical vertebrae. In childhood, the larynx is considerably
transverse process and the neck of the first rib . higher than in the a d u l t. Before birth the cricoid
The viscera cord, consisting o f the pharynx, cartilage corresp onds to the level of the fo urth cer­
esophagus, larynx and trachea as well as the thyroid vical verteb ra bo ttom . Owing to the grow th o f v is­
gland, runs through the space between the pretra­ cera l cranium and descen t of the thoracic and
cheal and prevertebral lamina. The whole larynx is cervical organs, the larynx descends du ring post­
located at the axial level between the hyoid bone nata l development. The descen t of the larynx is
and the cricoid cartilage in adult men. These three schema tically illus trated in F igure
3.4. In pu berty
structures e xtend over three cervical vertebrae (Fig. the larynx reaches the adult position .
3.4). The hyoid bone is a t the level of the interverte­
bral disk between the fourth and the fifth vertebral
bodies. The upper border of the laryn x is about one CONC LUSI ON
vertebral body deeper than the hyoid bone and thus
located at the level of the intervertebral d isk In summary, our review shows tha t the morpho­
between the fifth and the sixth vertebral bodies. The logical and topographical complexity of the cerv i­
lower b order of the cricoid cartilage is nearly a t the cal spine a ri ses from i ts regional specific and
level of the boundary between the cervical and tho­ gene ticallywell-coordinated development. This
racic vertebral column. leads to the ability for wide a n d p recise move­
The larynx of adul t w omen is placed a b i t ments and, on the other hand, guaran tees the
higher than i n m e n . The lower border of the function of the s tructures situated in it.


A Baby B 6-7 yea rs o l d

F i g u re 3 . 4 Position of the la rynx a t d i fferen t a g es ( a d a pted fro m von La n z a n d Wachsm u t h 1 9 55). Ax, a x i s ; C s ' t h e
fift h cervica l vertebra ; h , hyoid bone; T, thyro id ca rtila ge; m , m a n d ible.

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Deve l o p ment and to p ographic a l anatomy of the cerv i ca l s p i n e 27

o M

C 1 0- 1 2 y e a rs o l d o 1 5- 1 7 years o l d

F i g u re 3 . 4 Con tinued


B u rge ss R, Rawls A, Brow n DJ 1 996 R eq u i rement of the Kessel M, G r uss P 1 99 1 H o meoti c t r a n s for m a t i ons
pa r a x i s gene for somite form a tion and m us c uloskele ta l of mu rin e vertebrae and concomi tant a l teration
patterning. N a t u re 384(6609) : 570-573 of Hox codes ind uced by retinoic acid . Cel l 67( 1 ) :
Duboule D, Do l le P 1 9 89 The s t r uc t u ra l and functiona l 89- 1 04
organiza tion of the m u rine HOX gene fa mily res e mb les Kieny M, Manger A, Seng e l P 1 9 7 2 E a r l y region a l iza t ion of
tha t of D rosop hila homeotic genes . EM BO Journal the somite m e soder m a s s t udied by the d evel opment o f
8(5) : 1 497-1505 t h e a x i a l skeleton of the chi c k embryo. Developmenta l
Dubrulle J, McG rew M L Pourq u ie 0 2001 FG F s igna ling Biology 28 : 1 42-1 6 1
con trols som i te bo u n d a ry pos i tion and reg u l a tes Ogden J A 1984 Rad iology of postna ta l skele tal
seg men ta t ion clock control of sp a tiotem p o r a l Hox gen e development. XII. The second cerv i c a l verte b ra . Skeleta l
a c tiv a t i o n Cel l 1 06(2) :219-222
. Radiology 1 2(3) : 1 69-1 77
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and somi tocoele c e l l s in the forma t i o n of the vertebral Wirbeltiere. Reimer, Berlin
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155 :231-241 Wirbelsa ule im R bn tgen b i l d und KJ ini k . Thieme,
H u a ng R, Zhi Q, !zpisua-Be l m o n te ) -C et al 1 999 Origin an d Stuttgart
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Voss H 1958 Zahl und Anordnung def M uskelspindeln in Wilting J, Ebensberger C, M u ller TS et al 1995 Pax-l in the
den un teren Z ungenbeinmuskeln, dem development of the cerv ico-occi p ital transitional zone.
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ChaQter 4 ______����____���

Development of the central nervous

A. Hori

CHAPTER CONTENTS Maternal diabetes, hyperthermia and

Introduction 29 epilepsy 41
Early development of the CNS 30 Maternal infection and trauma 41
Neural tube formation 30 Intrauterine radiation exposure 42
Neural tube defect: dysraphism 30 Conclusion 42
Anencephaly and encephalocele: dysraphism
in the brain 31 I NTRO[)UCTI ON
Spinal dysraphism 32
Cerebral lateral differentiation 32 It is u s u ally possible to specify the critical time
Normal development of the forebrain 32 period of the onset of malformations of the central
Holoprosencephaly 34 nervous system (CNS) by morphological exami­
Migration and cellular differentiation in the nation. These anomalies can be induced by either
brain and its pathology 35 intrinsic or exogenous factors, or both.
Migration 35 The specificity of exogenous factors does not
Cortical differentiation, heterotopia, double u sually determine the type of CNS malformation
cortex, and agyria (lissencephaly) 36 but rather it is the time and/ or period of the influ­
Micropolygyria 36 ence of these factors that is decisive. This principle
Brain anomalies identifiable in the neonatal and is termed the teratogenetic determination period
infantile period 37 (the time span during which pathogens can influ­
Fetal brain disruption sequences and ence the development of a certain malformation) or
hydranencephaly 37 teratogenetic termination time (the time point after
Multicystic encephalopathy 39 which the effect of the pathogens can no longer
Porencephaly 39 result in a certain malformation). The experimental
Pathological myelination: status marmoratus administration of ethanol at different stages of
(marbled state) of the basal ganglia 39 pregnancy produced different types of brain mal­
Nuclear jaundice (kernicterus) 40 formations in fetuses of rats (Sakata-Haga et al
Embryofetopathy due to maternal disease or 2002). While the teratogenetic determination time
medication 40 is relatively easy to estimate, the pathogenic fac­
Fetal alcohol syndrome 40 tors are, on the other hand, not always identifiable
with modern diagnostic tools such as in situ

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hybridization or immlmohistochemistry due to that forms the neural groove, which is present
the complexity of both the intrauterine and post­ until the eighteenth gestational day, on the dorsal
nati11 environment . In addition, the mother often side of the embryo.
did not notice anything unusual or had not felt ill A scheme of neural tube formation during
at the teratogenetically suspicious period. ontogenesis of CNS is provided in Figure 4.1.
Endogenous disorders such as chromosomal The primary neural tube is formed from the
anomalies usually affect the brain heterochro­ neural plate via the neural groove between the
nously and result in typical, though not specific, twenty-second and the twenty-eighth gestational
morphological changes which do not provide any day (neurulation). Fusion of the dorsal raphe of the
clues to the teratogenetic determination period. neural groove, beginning at the level of the mes­
Recent advances in molecular genetics have encephalon, does not occur in a zipper fashion
shown that normal and pathological neuroembry­ uniformly along the entire spinal cord, but rather
onal developmental mechanisms at molecular lev­ at different points simultaneously. This explains
els are closely related to genes and their product the individually different sites of the spina bifida.
proteins. In this chapter, however, clinical neu­ Clinically well-known neural tube defects such as
ropathological aspects will be emphasized and the spina bifida or anencephaly may occur as early as
molecular genetic embryology will only be dealt in the fourth week of gestation.
with briefly. The dorsoventral differentiation of the neural
Malformations are easily understood by compar­ tube is an essential development of the CNS since
ison with the features of normal CNS development. the motor neurons arise from the ventral and the
Therefore, several malformations will be described sensory neurons from the dorsal part of the neural
after brief review of each embryofetal developmen­ tube. Both areas are sharply divided by the limit­
tal stage. The most frequent malformations are ing sulcus at the lateral wall of the central canal.
neural tube defects, disturbance of lateral differenti­ The development of the ventral part of the neural
ation of the brain, and migration disorders, which tube is inducted by sonic hedgehog protein (Shh),
we will review here. Further CNS anomalies, which is produced by the notochord, and later by
largely caused by environmental factors, will be the floor plate . Sensory motor differentiation is
described separately for the various developmental also regulated by several genes such as dorsalin-l
stages. Maternal factors or disorders which influ­ (drs-l ).
ence the environs of the embryo/fetus such as alco­
hol consumption, drug intake, state of nutrition, Neural tube defect: dysraphism
hormonal imbalance, diabetes mellitus, etc., may
result in unspecific malformations since the influ­ Dysraphism varies greatly in intensity. The most
ence of these exogenous factors is not limited to a common locations of dysraphism are the lumbar
certain period but usually continues throughout and lumbosacral areas at the spinal level, and
embryonal! fetal developmen t. the occipital area at the cranial level (Hori 1993).
Different manifestations of the dysraphism in
the cranial and spinal areas are summarized in
The morphogenesis of the dysraphism is con­
Neural tube formation sidered to be a disturbance of the closure of the
neural tube as proposed for the first time by von
The central nervous system (CNS) is the first organ Recklinghausen in 1886. This disturbance may
that appears in the embryonal stage. The nervous also be induced by a local amnion adhesion. The
system begins to develop from the neural plate classic observations by Marin-Padilla (1970) on

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Deve l o pm ent of t h e central nervous system 31

the reduction of the number of neuroblasts at the be one of the most important factors in neural tube
rim of the neural groove in normal human defect formation. Prophylactic evidence has been
embryos as well as by Patten (1952) on the 'over­ shown by giving folic acid to a group of women
growth of neuroectodermal tissue' (i.e. overpro­ at risk (see later section on maternal diabetes,
duction of neuroblasts) causing disturbance of the hyperthermia and epilepsy, p. 41).
neural tube closure, may be an anomaly of devel­
opmentally programed cell death (apoptosis). Anencephaly and encephalocele:
Another hypothesis on the morphogenesis of dys­ dysraphism in the brain
raphism is the secondary reopening of the dorsal
neuraJ tube after its closing by embryonal If the dysraphism occurs in the cranium (Fig.
'hydromelia' (Ikenouchi et a12002), which has also 4.28), the brain is exposed to the amniotic fluid ,
been induced experimentally by cyclophos­ an 'exencephaly'. Such a brain is also more or less
phamide, resulting in necrosis of the dorsal neural dysraphic and the basicranium (chondrocranium)
tube (Padmanabhan 1988). is usually dysmorphic. An exencephalic brain will
Although the causes of neuraJ tube defects are be destroyed during intrauterine life. Destroyed
still not clear, foEc acid deficiency is considered to tissue fragments are occasionally swallowed by

�+---+--H�- 3
--'I--'r--+-+-t-- 4

--+++---j-+--- 5

� E
o \:JG


3 4 5

Figure 4.1 Schema of an embryo at the later phase of neural tube formation. Different stages of the neural tube
formation are observed on the cut surfaces. 1, Neural plate structure; 2 and 3, neural groove structure (neural groove
does not close like a zip-fastener, but closes multilocularly); 4 and 5, complete neural tube structure. E, Ectoderm; G,
ganglion; NE, neuroectoderm; NCh, notochord; NC, neural crest; NT, neural tube.

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the continuing existence of the pharyngeal pitu­

Table 4.1 Neural tube defects in the cranial and
spinal region
itary (Hori et aI1999).
Encephalocele is a partial dysraphism in the
e NS Neural tube defect/dysraphism cranium, appearing as a protruding sac, usually
Brain Anencephaly
seen on the midline in the occipital or frontal
Exencephaly areas. The contents of the sac may be a part of the
Encephalocele brain tissue (encephalocele), or merely lep­
Meningocele tomeningeal tissue without protrusion of the
Brainstem Encephalocele
brain (meningocele). Encephalocele may occur in
Chiari anomaly type 2
the frontal base area , resulting in the protrusion of
Tectocerebellar dysraphy the cerebral tissue into the nasopharyngeal cavity.
Dandy-Walker anomaly This condition is often diagnosed as nasal glioma,
Spinal cord Myeloschisis not meaning a neoplasm, but a malformation.
Chiari anomaly type 3
Spinal dysraphism
Diastematomyelia The listed dysraphisms of the spinal regions differ
Dermal sinus only in the severity of the defects (Table 4.1 and
Spina bifida Fig. 4.2A). Myelocystocele is a type of myelocele
Cyst of the terminal ventricle
in which the contents of the cele sac include the
Tethered cord
dilated central canal of the spinal cord. If the sac
does not contain the spinal cord tissue but only
the leptomeninges and/ or dura, this is termed a
the fetus together with amniotic fluid, in some meningocele, analogous to that of the cranial
rare cases resulting in a heterotopic brain mass in region. The dysraphism may be limited within the
the buccal cavity, lung or gastrointestinal tract spinal col umn without protrusion of the spinal
(Okeda 1978). Exencephaly is most likely a pre­ cord tissue, which remains inside the dura in the
stage of anencephaly, although anencephaly can spinal canal. This condition is known as a spina
manifest without exencephalic stages. bifida occuita.
The destruction of the dysraphic brain is fol­ Patients with spina bifida occulta may occa­
lowed by tissue repair with intensive proliferation sionally complain of lumbago, motor disturbance
of the connective tissue, especially by vasculariza­ and other symptoms, but this condition can be
tion, resulting in the meshwork of proliferated clinically silent. The author knows personally an
vessels and remaining dysplastic brain tissues, athlete who has an asymptomatic spina bifida
called 'area cerebrovasculosa', which was earlier occulta. A focal trichosis or skin pigmentation on
incorrectly believed to be an angiomatous malfor­ the lumbosacral midline may indicate an occult
mation. In about 50% of anencephalic babies the dysraphism.
pituitary gland is lacking, with corresponding
adrenocortical hypoplasia and endocrinological
anomalies. The absence of the pituitary was also CEREBRAL LATERAL DIFFERENTIATION
incorrectly believed to be due to agenesis of the
pituitary. However, the pituitary is in fact also Normal development of the forebrain
destroyed during the intrauterine period in anen­
cephaly and replaced by connective tissue. Agen­ After neural tube formation , the brain vesicles at
esis of the pituitary in anencephaly is excluded by the oral end of the neural tube develop further,

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Development of the central nervous system 33

Figure 4.2 Examples of different eNS

diseases. A: Neural tube defect at the
spine: spina bifida aperta lumbosacralis.
B: Neural tube defect in the cranium:
anencephaly. C: Multicystic
encephalopathy with hydrocephalus
(frontal cut slices). D, E: Fetal brain
disruption sequences with microcephaly
and posthemorrhagic hydranencephaly in
a newborn resulting from a severe
maternal trauma in the later fetal phase.
F, Porencephaly (from Hori 1999, with
permission of Igaku-Shoin Ltd).
G: Microcephaly and cyclopia
(holoprosencephaly) in swine littermates
due to intrauterine mercury poisoning at
the gold mine region in Brazil (courtesy
of Dr S. U. Dani, Sao Paulo).

rendering telencephalic hemispheres (cerebrum), cephaly, rhombencephalosynapsis, agenesis of the

diencephalon, mesencephalon (midbrain), rhomben­ corpus callosum or cerebellar vermis develop,
cephalon (hind brain cerebellum and brainstem),
= namely anomaly of the brain organogenesis. The
and myelencephalon (spinal cord). It is during this correlation of normal organogenesis and its mal­
period that brain malformation such as holoprosen- formations in this phase is shown in Table 4.2. The

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Table 4.2 Brain organogenesis and possible malformation

Normal brain development An om a lies Subtypes of anomalies

Lateral differentiation of the forebrain Holoprosencephaly Alobar holoprosencephaly

(eighth week of gestation) Semilobar holoprosencephaly
Lobar holoprosencephaly ( according to
the severity)
Lateral differentiation of the Fusion of thalami
metencephalon ( fifth week of (unithalamus )
gestation )
Lateral differentiation of the Rhombencephalosynapsis Typical and incomplete forms of
rhombencephalon ( fifth week rhom bencephalosynapsis
of gestation)
Commissural fiber formation Agenesis of the corpus Total and partial agenesis with anomaly of the
(beginning at the fifth week of callosum gyral pattern of the medial surface of the
gestation, completed in the cerebral hemispheres
sixth month)
Differentiation of cerebellum Agenesis of the cerebellum Agenesis and hypoplasia of the cerebellum
Agenesis of a part of the Agenesis of the cerebellar vermis
Twin Duplication as an Craniopagus, including Janus anomaly
incomplete form of
Duplication of a part of the brain,
e.g. pituitary, cerebellum, brainstem and
spinal cord
Sulcus and gyral formation Lissencephaly ( agyria) Lissencephaly
Partial agyria

formation of the cerebral sulci and gyri also belongs synonymously - and incorrectly - termed arhi­
to organogenesis, but occurs much later (from the nencephaly.
fourteenth week of gestation, intensively after the Different craniofacial anomalies are frequently
twenty-first week). In this section, only holopros­ accompanied by holoprosencephaly. A typical
encephaly is reviewed. manifestation is a spectrum of hypotelorism,
including cyclopia or proboscis instead of a nose
Hol oprosencephaly (Table 4.3). Since a typical holoprosencephaly dis­
played typical facial anomalies, the principle 'face
Holoprosencephaly is a relatively common mal­ predicts brain anomaly' was proposed earlier.
formation of the brain which is due to distur­ However, because of the broad morphological
bance of its lateral differentiation, occurring spectrum of the intensity of the malformations in
around the eighth week of gestation. The brains craniofacial as well as brain anomalies, this princi­
of typical cases display no divided hemispheres ple is no longer of use. In our own archives there
and a single ventricular system. The meten­ are two cases of (lobar or semilobar) holopro­
cephalon (thalamus) is also not divided but is sencephaly without craniofacial anomalies. In
singular. The eye is also single, being termed holoprosencephaly, some non-obligatory facial
cyclopia. T he olfactory bulbs and tracts are anomalies may be complicated such as different
lacking. This was why holoprosencephaly was intensity of cheilopalatoschisis.

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Developm ent of th e central nervous system 35

Table 4.3 Morphological spectrum of the intensity of brain and craniofacial anomalies in holoprosencephaly

Slight anomaly Severe anomaly

Normal eyes Hypotelorism Synopia Cyclopia

Normal nose Only one opening of the nose No nose but nostril ( proboscis) above
Lobar holoprosencephaly Semilobar holoprosencephaly Alobar holoprosencephaly

Corresponding to the clinically broad spec­ MIGRATION AND CELLULAR

trum of the intensity of holoprosencephaly DIFFERENTIATION IN THE BRAIN
(Table 4.3), many different genes play a complex AND ITS PATHOLOGY
role in constructing this abnormal morphology.
Some of the genes of familial holoprosencephaly Migration of neuroblasts is an essential part of the
(,HPE' 1�5) are identified and located on the histogenesis of CNS. In principle, organogenesis is
chromosomes. For example, sonic hedgehog followed by histogenesis, although both phases
(5hh = HPE3), which was found to produce dou­ overlap. In the early phase of neurulation, a stem
ble formation in an individual, is located on cell wall attaches to the central canal side with one
chromosome 7q36. Haploinsufficiency for 5hh end and reaches the mantle side with the other
was considered to be one of the causes of holo­ end. The nuclei of these stem cells shuttle inside
prosencephaly (Roessler et a11996, 1997). A com­ the elongated cytoplasm between the central canal
ponent of the 5hh pathway, the receptor PTCH side and the mantle side (,elevator movement') in
(Patched-1), was recently identified, a mutation accordance with the cell cycle: the nuclei display
of which can cause holoprosencephaly (Ming et mitosis and division while they are situated in the
al 2002). central canal side (M phase) and DNA synthesis is
On the other hand, extrinsic factors may also active while they are located in the outer surface
cause holoprosencephaly as described in the litera­ side of the neural tube (S phase).
ture, for example anhepileptics taken by the mother
(Homes and Harv ey 1994, Kotzot et al 1993, Rosa Migration
1995), maternal alcohol abuse (Bonnemann and
Meinecke 1990b) or intrauterine cytomegalovirus During and after their production in the periven­
infection (Byrne et al 1987). In a gold mining dis­ tricular zone, the neuroblasts migrate along the
trict in Brazil, holoprosencephaly occurs fre­ radial glia towards the brain mantle in the phase
quently in cattle, probably due to the mercury of brain vesicle formation. The speed of the neu­
pollution (Fig. 4.2G), although intrauterine mer­ roblast migration is estimated at a maximum of 70
cury intoxication does not cause holoprosen­ �m/h in the region of the olfactory bulb (Tama­
cephaly in humans but developmental anomalies maki et aI1999). In the mantle zone, the cortical cell
of motoric nerve bundles and commissural bun­ layers are formed where neuroblasts differentiate
dles (e.g. fetal Minamata disease due to industrial to the nerve cells. The neuroblasts migrate along
pollution in Japan). the radiating glia from the subependymal zone in
Clinically, patients are severely or very severely the direction of the marginal mantle zone where
handicapped due to the prosencephalic malfor­ Cajal-Retzius cells are found. Cajal-Retzius cells,
mations. In less severe cases, it is possible to sur­ the first differentiated cells containing neurofibrils,
vive to adulthood. recognizable as early as the forty-third gestational

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day (Marin-Padilla and Marin-Padilla 1981) and ular nodular heterotopia, filamin 1 (FLN1) muta­
constantly observed from the fiftieth day on, pro­ tion was identified as a genetic defect causing the
duce the extracellular protein 'reelin' that inacti­ hereditary nodular heterotopia (Fox et al 1998).
vates the migration of the neuroblasts. The next Familial nodular heterotopia is linked to the gene
migrating neuroblasts pass over the neuroblasts located in chromosome Xq28 in females. In males,
that have already arrived at the cortex and ceased the same Xq28 gene is considered to be responsi­
to migrate, until they come in contact with reelin. ble for bilateral nodular heterotopia combined
In this manner the outer cortical layer is formed with frontonasal malformation (Guerrini and
by newcomer neuroblasts: 'inside-out law'. Dobyns 1998). Pathomechanisms of the migration
The Cajal-Retzius cells reduce in number by disturbance can be explained by the disruption of
apoptosis in the peri- and postnatal period. Exces­ the radial glia along which the neuroblasts
sive residual Cajal-Retzius cells were previously migrate from the subependymal to cortical zone
discussed as one of the possible causes of seizures (Santi and Golden 2001). This condition may
in epileptic patients. explain a non-hereditary occurrence of nodular
Disturbed migration results in heterotopically heterotopia.
located nerve cell groups; heterotopia refers to a Laminar (band) heterotopia is a diffuse arrest
nerve cell group that is found in anatomically of migration and is found in the (subcortical)
incorrect regions such as the subependyma or the white matter as an additional nerve cell layer
subcortical white matter and have either nodular (hence, double cortex syndrome). The gene DeX
or band form. These anomalies may be caused is located on the X chromosome and produces the
by genetic defects as well as by many kinds of protein named doublecortin. The mutation of this
extrinsic factors such as intrauterine exposure to single gene is the cause of two different types of
radiation (see section on intrauterine radiation expo­ migration disturbances: double cortex syndrome
sure, p. 42), fetal circulatory disturbance (see section in females and lissencephaly in males. In females
on micropolygyria below). (karyotype XX), mutant X disturbs the neuronal
migration; however, non-mutant X forwards the
Cortical differentiation , heterotopia, migration, i.e., some of the neurons migrate regu­
double cortex, and agyria larly but the migration of others is disturbed and
(l issencephaly) they therefore make up the subcortical hetero­
topia in a laminar form. This condition is termed
The neuroblasts that arrived in the cortex then dif­ 'double cortex syndrome'. In males (karyotype
ferentiate to the cortical nerve cells with a topo­ XY), the migration is completely disturbed by
graphically typical laminar structure, usually mutant X so that a severe form of lissencephaly
consisting of six layers. occurs, but no double cortex. Another
A migration anomaly results in nodular hetero­ lissencephaly, morphologically identical to the
topia (periventricular heterotopia), subcortical hereditary ones, is caused by the LIS1 gene,
laminar (band) heterotopia (double cortex syn­ located on chromosome 17.
drome), and agyriajpachygyria (lissencephaly) Clinically, lissencephaly and laminar heterotopia
(Schull et al 1992). Nodular heterotopia is a focal (double cortex synruome) form a morphological
arrest of migration, usually identified in the substrate for severe psychomotor retardation.
periventricular areas as single or multiple nodules
of nerve cell accumulation, and clinically may be a Micropolygyria
focus of epileptic discharge. In our experience,
there is silent single heterotopia in 0.7% of routine Micropolygyria (or polymicrogyria) is not a pre­
necropsy series. In X-linked dominant periventric- cise description although the term is generally

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Development of the central nervous system 37

accep ted since the cortical surface of this anomaly group of m us cle-eye-br a in d isea ses, Walker­
does not consist of small gyri. Warburg syndrome (linked mostlyto chromosome
The gyri them sel ves a re ra ther pachygyric and 17q) or the Fukuyama type of muscle dystrophy
the s u rface has the appea ra nce of a cobble stone (linked to chromosome 9q31-33), known as auto­
pavement. His tological ly, the cortical surfa ce is, somal recessive hereditary diseases, and is not
corresponding to its gross appearance, very irreg­ exogenous.
ularly configured and the s urface neurons inv a d e Clinical manifestations of microp olygyria gen­
randomly in t o the leptomeninges through the bro­ erally consist of psychomotor reta rda tion and
ken subpial l imitin g glia l membra ne. The co rtical typically seizures .
architecture is also abnormal, with small i slets of
neuronal mass, and the v ir tua l molecular la yers
are irregularly confluent. A no ther typical cortical BRAIN ANOMALIES I DENTIFIABLE IN THE
feature is a four-layer p a t tern due to an in terme­ NEONATAL AND INFANTILE PERIOD
diate nerve fiber la yer between the neuronal layer
(I, molec ula r layer; 2, ex ternal nerve cell layer; 3, Brain a n omalies recog ni z a b le in the postna tal
myelina ted nerve fiber l ayer; 4, internal nerve cell period may have occurred either d uring intrauter­
la yer) The abnormal
. cortical la yer may show a n ine life or in the perina tal as well as postnatal
ab rupt bound ary t o the intac t six-layered cortex. period. The majority of these anom alies a re due to
This sugges ts foca l injury and thus an ex ogenous an encephalocla s tic process of ex trinsic cau s e s, for
cause in micropolygyria, although end ogenous example birth trauma, perina ta l hypoxia, infec­
m i crop ol yg yr ia may also be focally limited. The tion , etc . Complica tions in twin concep tion ( such
lesions a re, in the m a j o ri ty of cases , not diffusely as fetofetal transfusion synd rome) may also be
distrib uted but localized or coex is tent with o ther incl uded in this group although they are not exoge­
lesions such as porencephaly (see later section on nous in the strict sense of the word . The disorders
porencephaly, p. 39). A representati ve case is that described in this section include different syndromes
of a 27-week-old fetus in which micropolygyria and diseases which are not grouped systematically
was limi ted to the dis turbed supplying area of the and which exclude brain malformations.
middle cerebral a rtery (Richman et al 1974). Fur­
ther reports of in trauterin e
CO intoxica tion at the Fetal brain disruption sequences an d
fifth gestational month or at the twenty-fourth hy dranencephal y
week (Bankl and Jellinger 1967) confirm an ex oge­
nous cause of micropolygyria. In tra uterine infec­ This clinical concept includes a ll encephalocl a s tic
tion with cytomegalovirus (CMV) is known to cause processes which involve a collapse of the skull
a brain malformation (micropolygyria, micren­ or microcephaly with organic brain da mage in
cephaly). However, there is other evidence that men t ally and physic a l l y h a n d i c apped b a b ies
micropolygyria in congenital CMV infection is a (Fig . 4 2 D).

result of circulatory disturbance (Marques Dias et al Etiopa thogenetically, these disorders may occur
1984). Small focal micropolygyria may also be in every embryofetal s tage from very differen t
observed in endogenous CNS anomalies such as causes, such as viral or parasi tic infection or circu­
thana tophoric dysplasia (Hori et al 1983). The ter­ la tory dis turb ances in la ter fetal stages, analogo u s
a togenic determination period is though t to be to hydranencep haly. The maj ority o f the rep orted
between 17 and 26 weeks of gestation (Golden 2001) . cases are
sporadic. However, Alexander repor ted
Micropolygyria accompanied by widespread anoccurrence in sisters, suggesting some gene tic
pachygyria (pachygyric micropolygyria) is termed componen t (A lexander et aI1995). In this con tex t,
lissencephaly type 2. This type 2 is typical in the a recessivel y inherited vasculopathy resul ting in

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hydranencephaly-hydrocephaly disorder (Harding tic processes. The brain shows only a contour of the
et a11995) should also be included in this group of cerebral mantle and is filled with cerebrospinal fluid
disorders. since the majority of the telencephalic structures are
Microcephaly or overlapping sutures is a typical destroyed and replaced by fluid (Fig. 4.2E). In
clinical manifestation (Fig. 4.20). The baby has a nor­ extreme cases, only the molecular layer and residual
mal craniofacial appearance. Hydrocephalus may parts of the cerebral cortex are preserved, but there
also occur but is not obligatory. Sonographic and is practically no white matter or internal structures.
radiological examination as well as transillumination The brain substance is destroyed by colliquation
of the head confirm the diagnosis. Neurological necrosis. If the brainstem is preserved, the fetus usu­
symptoms include seizures, spasticity, myoclonus, ally survives for a short time.
cortical blindness and optical atrophy. Prognosis is Hydranencephaly can occur after the fourth
very poor and most patients die shortly after birth. gestational month, though usually after the sev­
Surviving babies are severely handicapped. enth month (gestational week 28) when the brain
The brain changes largely include hydranen­ is formally 'completed' (though immature), since
cephaly (Fig. 4.2E) and/or cerebrocortical damage. cortical dysgenesis such as micropolygyria or
Hydranencephaly is essentially not a type of mal­ migration disturbances and other kinds of brain
formation but a residual state of the encephaloclas- malformations are usually lacking in hydranen-



30.2% N = 116

hemorrhage 2.6%

exogenous causes 6.0%

Figure 4.3 Different causes of hydranencephaly. based on the a n alys is of cases reported in the literature as well as
from the author's own archives. Note that a quarter of all cases of h yd ra n enc epha l y are caused by intrauterine
e n cephalit i s .

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Development of the central nervous system 39

cephaly. The cortical gyral structures are nor­ sis of the carotid arteries. However, the causes of
mally recognizable although the subcortical the cerebral circulatory disturbance resulting in
structures are totally or subtotally destroyed. multicystic encephalopathy are very different -
Normal configuration of the ventricular system is birth trauma, intrauterine viral infection, etc. Sev­
therefore radiologically or sonographically often eral twins with this condition have been recorded in
not detectable. the literature. The majority of patients are neonates
The causes of hydranencephaly vary greatly; for with different neurological manifestations since the
a majority of the cases, intrauterine encephalitis brain changes occur usually in the perinatal phase.
and trauma are responsible (Fig. 4.3). No matter Rarely, surviving 'shaken baby syndrome' patients
what the initial cause is, an additional circulatory also manifest multicystic encephalopathy together
disturbance of the brain followed by diffuse necro­ with other typical signs of the syndrome.
sis plays a major role in establishing hydranen­
cephaly. A recessively inherited vasculopathy is Porencephaly
another cause of hy dranencephaly, as already cited
(Harding et al 1995). In a few cases, hydranen­ In contrast to hydranencephaly and fetal brain
cephaly may occur after birth as a result of cerebral disruption sequences, porencephaly displays
infarction complicated by widespread meningitis congenital, partial cerebral destruction (Fig. 4.2F).
and/or intracerebral hemorrhage (Lindenberg Porencephaly is defined as a communication
and Swanson 1967). between the inter na l and external cerebrospinal
Neonatal (including perinatal) meningitis is spaces due to partial destruction of the brain,
often complicated by focal or multiple infarction, occurring in the middle and later fetal stages. Post­
followed by hydrocephalus due to absorption dis­ natal porencephaly is an exception (Cross et al
turbance of the cerebrospinal fluid if the patients 1992). The lesions are usually seen bilaterally and
survive the acute phase of the infection . Intrauter­ often in the central to parietal regions. The tissue of
ine meningitis is extremely rare. We observed one the lesion shows glial scar formation and sometimes
such case with evidence of the transplacental micropolygyric changes in the cortex at the mar­
infection (Hori and Fischer 1982). gin of the destructive lesion (Tominaga et aI1996).
Rarely heterotopic neurons are observed near the
Multicystic encephalopathy lesion. However, the micropolygyric or hetero­
topic changes are interpreted as secondary, since
Multicystic encephalopathy is one of the severest the encephaloclastic damage is thought to be a
cerebral disorders with multiple cavity formation result of extrinsic causes at the time of migration.
in the cerebral hemispheres due to encephaloclas­ In some cases of porencephaly, however, this con­
tic processes (Fig. 4.2C). This condition is usua lly dition is observed in successive generations or in
accompanied by hy drocephalus and lack of sep­ twins and a genetically defined etiopathogenesis
tum pellucidurn. The remaining cortical ribbon is has also been considered (Brewer et al 1996, Jung
very thin. Basal g ang l ia, thalamus or even brain­ et aI 1984).
stem may also show microcystic changes and there
is severe nerve cell depopulation or calcification of Pathological m yelination: status
dead nerve cells. As a result of the parenchymal m arm oratus (m arbled state)
destruction, glial scar formation (including ule­ of the basal ganglia
gyria) is usually observed.
Severe circulatory disturbance during the late Normal my elination begins in the second fetal
intrauterine and/or neona tal phase is the main trimester in the brainstem. In the spinal cord, the
pathogenesis of this condition, for example steno- sensory fascicles show earlier myelination than

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the motor fascicles, but the motor spinal roots are related to differences in the topographical devel­
myelinated earlier than the sensory spinal roots. opment of the blood-brain barrier. Choreoa­
The cerebral white matter myelination is com­ thetotic movement disorders and psychomotor
pleted by 1 postnatal year. The complete myelina­ retardation are major clinical manifestations of
tion of the reticular formation may be as late as this 'nuclear ' jaundice.
Status marmoratus (marbled state) of the basal
ganglia, occasionally also of the thalamus, repre­ EMBRYOFETOPATHY DUE TO MATERNAL
sents glial scars with irregular hypermyelination DISEASE OR MEDICATION
associated with neuronal loss. This indicates that
the disorder is not a congenital malformation but Fetal alcohol syndrome
an acquired condition. Since the myelination in
the basal ganglia commences at the sixth month of Maternal chronic or excessive alcohol consump­
postnatal life, the status marmoratus is thought to tion, in particular in the first trimester after the
occur around this period at the sites of the scars conception, can lead to the unspecific congenital
that may have occurred earlier than 6 months of anomaly of the baby, an (embryo)-fetal alcohol
age. The clinical features of patients prior to this syndrome. Not only ethanol itself, but also its
critical period include birth complications such as intermediate metabolite acetaldehyde is consid­
asphyxia as well as cyanosis, resuscitation and ered to be embryo toxic.
convulsions. These complications result in dam­ The newborn baby is small for dates, which
age to the basal ganglia and thalamic regions. In may be recognized during in utero examination,
older infants, rigidity or choreoathetosis is a com­ and shows craniofacial dysmorphism. Some
mon clinical manifestation. Mental retardation or authors describe the craniofacial anomalies in
movement disturbances such as spastic paraple­ fetal alcohol syndrome as typical: short eyelids,
gia may also manifest. The average life expectancy broad nasal root, flat and long philtrum, thin
of children with status marmoratus is approxi­ upper lip, occasionally blepharophimosis and
mately 12 years of age. anti-Down eyelids. Generalized malformations in
these patients are usually not remarkable. Slight
Nuclear jaundice (kernicterus) craniofacial dysmorphism may partly regress by
the time of adolescence; the body weight may also
Severe neonatal hyperbilirubinemia may result in normalize while the lower IQ remains unchanged.
'nuclear jaundice'. One of the major causes of this However, a long-term prognostic study showed
disorder is megakaryocytosis due to Rh incompat­ that adequate education may improve learning
ibility. However, the nuclear jaundice is merely an ability since the postnatal development of these
unspecific 'bilirubin encephalopathy', regardless patients varies (Streissguth et al 1991). Recorded
of the cause of hyperbilirubinemia. Since the brain anomalies are various and unspecific in con­
blood-brain barrier is still immature in neonates, trast to the relatively uniform craniofacial anom­
bilirubin reaches brain parenchyma so that the alies: hydrocephalus, cerebral heterotopia, agenesis
caudate nucleus, putamen, globus pallidus, sub­ of the corpus callosum, dysraphism, or poren­
thalamic nucleus, hippocampus, cerebellar den­ cephaly; even holoprosencephaly has been
tate nucleus and olivary nucleus are selectively recorded (Bonnemann and Meinecke 1990a).
and bilaterally yellowish colored and nerve cells Experimentally, reduction in the number of
undergo degeneration. The different distribution pyramidal nerve cells (Barnes and Walker 1981),
of the changes in patients of different ages may be depression of glutamate release and decrease in

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Develo p m e n t of t h e ce n t r a l n e rvous system 41

gl u ta m a te binding (Farr et a 1 1 988), and changes The incidence of malforma tion among infants of
in neu ro troph i c a c t i v i ty (Hea ton et a l 1 9 95) of epileptic m o thers who w ere not ta king antiepilep­
the hippocampus a re d emonstrated, the la tter tic drugs was 4 . 8 % . In trau terine head gro w th was
being an important a rea for memory fu nction. In correlated to the number of antiepileptic d rugs
animal experiments, d i fferent brain malforma­ taken by mothers (Battino et a l 1 992) . Serum and
tions were p r o d u c e d in b o th the c e reb r u m cerebrospinal fluid levels of folate were reduced in
(incl u d i n g leptomeningeal hete r o t o p i a ) and a high percen tage of epilep tic pa tients trea ted
cerebell u m by i n trau terine e x p o s u re t o e thanol. with antiepileptic drugs ( Raynolds 1973 ) . Fola te is
Sched u l e d alcohol c o n s u m p tion at d i ffe rent known to b e an important factor in p reventing the
times in the p regna ncy induced d i ffere n t types risk of neural tube defect, so tha t mothers who
of cereb ral malforma tion in fe tuses (Saka ta-Haga already have dys raphic babies are advised to take
e t al 2002 ). folic acid as a prophylaxis, even prior to the
planned conception . Therefore, it is likely tha t
Ma terna l dia betes, h ypert h erm i a a nd antiepi lep tic-drug-rela ted fa c tors predomina te
epilepsy over genetic predisposition as the cause of ma lfor­
mation in cases of ma ternal epilep sy. Howev er,
Ma ternal diabetes mellitus p ossibly influences the the m o ther ' s convulsion i tself should also be
m orphology of embry os / fetuses. Babies born to regarded as a possible teratogenic factor (Leppert
diabe tic mothers a re usually large for d a tes. A and Wieser 1 993) in a d d i tion to the genetic factors.
high incid ence of anomalies such as Down syn­
drome (Narchi and Kulayla t 1 997), preaxial poly­ M atern a l infection a nd traum a
d a c tyly (Slee and Goldblatt 1 997) or c a u d a l
regression syndrome (Passarge a n d Lenz 1966, In cases of ma ternal infection, virus or bacteria
Willia mson 197 0) have been recorded in the litera­ may be transported v ia the placenta to the fetus
tu re . O ther mal forma tions have also been sporad­ and feta l CNS . Cytomegalovirus is know n to
ically reported . Early in tellectual developmen t in cause micropolygyria wi th microcephaly; how­
children of diabe tic mo thers is p oorer than in ever, the teratogenic d e termin a tion period is lim­
those of non-diabetic mo thers (Yamashita et al i ted to the la ter migration phase ( till the end of the
1996). The tera togenic mechanism of m a ternal dia­ fourth gestational month; see sec tion on micro­
betes mell itus is not known; however, n o t only polygyria, p . 36) . O ther viral infections in the l a ter
d i abetes melli tus, b u t also the effect of medical fe tal period, e . g . herpes v irus, are known to cause
control of diabetes should be discussed. severe encephaloclas tic processes such as hydra­
Ma terna l hyperthermia is shown to result in nencephaly (see section on fe tal brain d isrup tion
embryofetal malformations experimentally (Shiota sequences and hydranencephaly, p . 37) . However,
1 988, Sh i o ta et al 1988) . Several case repo r ts other factors such as circulatory disturbances are
describe dysraphism or facial dysmo rphism in assumed to play a much more important role in
humans. the p a thological morphogenesis than the virus
Epileptic mothers have a risk of gi ving b irth to i tself.
malformed children with or without CNS anom­ Severe ma ternal trauma w i th u te r i ne inj u r y
a lies. According to the study by Canger et al a n d / or b l e e d i n g m a y also ca use fe tal anomaly.
( 1 999), the overall incidence of malformations (not Hydranencephaly is documented (in the litera­
only CNS malformations) in sib lings b orn to ture as well as in our archives) as one of the
epilep tic mothers was 9 . 7% . The maj o r i ty o f the re s u l ts of accidental s e v ere tra u m a to the
mothers were treated with an tiepilep tic drugs. mo ther.

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I ntra u terine radiation exposure CON C L USION

Therapeutic or accidental exposure to irrad iation Knowledge of the process of normal neuroembry­
as well as nuclear bomb exposure during embryo­ onal development helps in interpreting the malfor­
fe tal l ife may also cause CNS anomalies. mations of the cen tral nervous system, especially
Much traged y was seen in children born to sur­ in cases of neural tube defec ts (including anen­
viving pregnant victims of the atomic bombs (ion­ cephaly), holoprosencephaly and migration anom­
izing rad iati o n ) in Hiroshima and Nagasaki . alies such as lissencep haly or heterotopia. These
Significan tly, frequent men tal re tardation and anomalies can be induced endogenously by
microcephaly was observed in such children genetic errors and also by environmental (exoge­
(Otake e t al 1989) exposed to atomic bomb irradi­ nous) factors . Exogenous factors, such as infection,
ation before the twenty-six th ges tational week, trauma, in toxication and other maternal condi­
an d mostly b e tween the eighth and fifteen th tions, may ind uce differen t malformations, mostly
week . The children who were exposed in the independent of the factors but dependent on the
eighth and n in th weeks of gestation showed men­ pathogenically effec tive time p e r i o d . Chronic
tal re tardation as a result o f bilateral periv en tricu­ effects of exogenous fac tors or chromosomal
lar he tero topia which was ascertai ned by anomalies may produce unspecific though typical
magnetic resonance imaging. The fetuses that anomalies due to their heterochronous pathome­
were exposed to the atomic bomb during the chanis m . Clinically severe brain d isorders may be
twelfth / thirteen th week of ges tati on showed no produced by encephaloclastic processes due to
heterotopia b u t pachygyria. Even low-dose ioniz­ hypoxia, circulatory dis turbance, trauma, and
ing irradiati on in utero resulted experimentally in many o ther causes mos tly during the perinatal
migration anomalies (Fushiki et al 1994, 1996). phase as well as in the latest fe tal stage. Despite
Intrauterine X-i rradiation was expe rimen tall y having the same etiopathogenetic factors, pheno­
ascertained as the cause of a deceleration in the typically different brain anomalies may be pro­
m i gration of neuroblasts (including cortical duced depending on the time of onset of the
derangement) (Fushiki et aI 1997) . causes, for example a series of hydranencephaly,
Therapeutic or prophylactic X-ray irradiation to porencephaly and polycystic encephalopathy due
the head in leukemic children is known eventually to brain circulatory disturba nces. The search for
to resul t in meningiomas (or gliomas and other b rain possible causes of CNS anomalies should lead to
tumors) about 10 years later as a delayed side effect. the prevention of the d isorders.


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D e v e l o p m e n t o f t h e c e n t r a l n e rv o u s s y s t e m 43

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Ch a pter 5 ------------------�----���---------------- �

Ad a ptive p ro p e rti es of m oto r

b e h avi o r
J . - M . Ra m i rez


Introduction 45
The ability to walk and to maintain posture
Th e genera tion of rhythmi c activity: the concept
depends on a complex integration of many intrin­
of a central pa ttern generator ( C P G ) 46
sic and extri nsic fac tors . The basic w alking
The role of proprioceptive input in the
rhythm is generated by a neuronal network,
gene ra tion of rhythmic activity 48
which is located within the spinal cord (Kiehn and
Sta te-dependent modulation of reflex
Kj aerulff 1998). This network is capable of gener­
pa thw ays 50
ating reciprocal neural activity, which is sent via
Neuromodulation and reconfiguration of
motor neurons to the periphery where it activa tes
rhythm-genera ting networks within the
muscles that produce al terna ting limb move­
central nervous system 50
ments. Each of these l imb movements is the result
The development of motor neural networks 52
of a complex activation of numerous antagonis tic
Conclusion s 52
and agonistic muscles that lead to the genera tion
of a step, which consists of a swing and stance
phase . The exact timing and also the shape of ac ti­
vation of each of these muscles is highly influ­
enced by the properties of the muscles and the
activation of sense organs loca ted within the mus­
cles and tendons of each limb, the so-called pro­
p r iocep tors . The activa tion of proprioceptors
feeds back to the neuronal network located w i th i n
the central nervous system, which a djusts the
intrinsically genera ted motor activity in a cycle­
by-cycle manner to the constantly changing
extrinsic conditions, s uch as the surface of the
ground (McCrea 2001, Pearson and Ramirez 1997).
Besides these rapidly occurring adaptive
processes, long-term changes are also very charac­
teristic and essential for normal locomotor behav­
ior. The timing of proprioceptive feedback has to

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be adj usted to long-term changes in body size. In locomotion, but also other rhythmic behaviors.
the developing child, new locomotor m ovements Here I will summarize these genera l principles of
are learned, or exis ting movements are refined as rhythm generation, which are applica ble not only
the chi ld is growing . This motor learning will be to how the nervous system produces walking in
associa ted with a complex change in the activation particular, b u t rhythmic activity in genera l.
pa ttern of individual muscles (Okamoto et al
2001 ), in neuronal networks located within the
spinal cord (Nakayama e t al 2002), as well as com­ THE GEN E RATION OF R H YTHMIC
plex changes in the afferent feedback (Ronces­ A C T I VIT Y : T H E CONCEPT OF A C E NT RAL
valles and Woollacott 2000). Adaptive processes PATTERN GENERATOR ( C PG)
are not only cri tical during development, but also
important in the adult as body weigh t may change As mentioned above, the nervous system gener­
drastically over weeks and months (Barbeau and a tes not only w alking, but many forms of rhyth­
Fung 2001, Pearson 2000). Inj ury will also change mic activi ty, which dominate our daily l ife . When
the gain of propriocep tive reflexes over several we become tired in the evening, this is not only
mon ths, which will affect not only locomotion, but because we are physically exhau s ted. More likely,
also posture (Barbeau et al 2002, Bouyer et al 200 1, it is because our 'internal clock' tells us tha t it is
De Leon e t al 2001 , Rossignol 2000, Whelan and time to sleep (KulJer 2002, Zisapel 2001). In the
Pearson 1997) . Vice versa, changes in posture may morning we wake up, beca use our internal clock
affect s tep size and timing during locomotion. 'reminds' us, tha t it is time to get up . We do not
Many of these long- term changes may be necessarily wake up because we regained our
explained by changes in the response of the cen­ physical strength d uring the sleep, as everybody
tra l nervous system to afferent inpu ts from pro­ knows, who cannot go back to sleep in the morn­
priocep tors or by changes in the excita tory drive ing, even if the preceding night was highly dis­
to proprioceptors tha t derives from gamma motor turbed. A similarly common experience is the
neurons, which can change the gain of reflexes in jet-lag that affects people who travel overseas
a sta te-dependent manner (Lam and Pearson (Boulos et al 1995, Brown 1 994, Zisapel 2001), or
2002, Pearson 2000, 2001, Prochazka 1 989) . An the problems associated with sh ift work (Rajarat­
important role in these adaptive changes can be nam and Arend t 2001). The internal clock tha t is
attribu ted to neuromodula tors, which are sub­ responsible for these phenomena has been identi­
stances tha t alter membrane properties of neurons fied as a small neuronal network, loca ted in the
involved in the genera tion of rhythmic motor so-called supra-chiasma tic nucleus (SCN, Cheng
activi ty. In inj ury, for example, endorphins are et al 2002, Reppert and Weaver 2002). This net­
released . These peptides can potentially alter not work is both su fficient and necessary for generat­
only reflexes, but also membrane and synaptic ing the circadian rhythm . Isola ted from the
properties of neurons within the central nervous remaining central nervous system, the SCN main­
system, thus resul ting in long-term changes in tains a 24-hour rhythm even in a Petri dish
wa lking behavior. (Gille tte and Tischkau 1999, Weaver 1998) . This
This chapter will review concepts and princi­ experiment indicates tha t the SCN is sufficient to
ples tha t have been established in various animal genera te a 24-hour rhythm and that this rhy thmic
models in order to explain how the nervous sys­ activity is generated endogenously by the central
tem prod uces a locomotor behavior. Many of the nervous system, and does not depend on the pres­
principles tha t are directly relevant for human ence or absence of light. The SCN con trols various
locomo tion have been established in a v ariety of circadian rhy thms and is responsible, for example,
animal models, which were used to study not only for the generation of circadian fluctuations i n hor-

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A d apt i ve prope r t i es of motor beh a v i or 47

mone levels (e.g. the growth hormone) or for rational therap ies for t rea t in g epilepsy and men ta l
rhythmic changes in body temperature. Lesions of d i s orders .

the SCN abolish these circadian rhythms in other­ Various rhythm-generating networks also exist
wise in tact animals (Weaver 1998), ind ica ting that in the brainstem. Rhythms controlled b y the brain­
this network is necessary for generating circadian stem include chewing, licking, swallowing, vomit­
rhythms. Neural networks tha t are capable of gen ­ ing, sneezing, coughing and b re a thing. Best
erating rhy thmic activity in the absence of a sen­ understood is the neural network which controls
sory input (e.g. a visual input, light) are called breathing. Respiratory neurons are distributed in a
central pattern generators or CPGs (Marder and neuro nal colwnn within the ventrolateral medulla,
Calabrese 1996). which is called the 'ventral respiratory group', VRG
The SCN is only one of many central pattern (McCrimmon et aI 2000) . One area within the VRG
generators in the central nervous system. The thal­ that is of particular importance for the genera tion of
amus generates rhy th ic activity, which highly
m the respiratory rhythm is the so-called pre­
influences our cortical activity. The thalamic rhyth­ Bbtzinger complex (Smith et aI 1991) . As in the case
micity is s ta te depe nd ent, and associated with
- of the SCN, this nucleus is both sufficient and nec­
well-known changes in neuronal properties of essary for generating respiratory rhythmic activity.
thalamic neurons (McCormick 2002) . The transi­ Lesions of the pre-Bbtzinger complex in an intact
tion from being rhythmic to non-rhythmic is con­ animal abolish respiration, indicating its necessity
trolled by inputs from the brainstem and cortex, for breathing (Ramirez et al 1 998) . Isolation of the
which play important functions in regulating the pre-Bbtzinger complex in a brainstem slice prepara­
role of the thalamus as a relay nucleus in sensory tion retains respiratory rhythmic activ ity (Ramirez
processing. As described for the SCN, isolated et al 1996 , Smith et aI 1991), thus indicating that this
slices from the thalamus are still capable of gener­ nucle us is sufficient for generating a respiratory
ating rhythmic activity (McCormick and BaI 1997). rhythm (Fig. 5 . 1 ) .
Knowing how the thalamus generates rhythmic More recently it has been demonstrated that the
activity is not only important for understanding pre-Bbtzinger complex is important for the genera­
the transitions from wakefulness to sleep, but this tion of different forms of breathing including 'eup­
unde rsta nding is also clinically relevant. Rhythmic nea', gasping and sighing (Lieske et al 2000). The
ac t i v ity generated by the thalamus can be patho­ transition from eupnea to gasping and the genera­
physiological and thalamic oscillations have b een tion of the sigh are generated by the same neuronal
associated with the generation of absence seizures network, which is, however, reconfigured in a
(McCormick and Contreras 2001 ) . state-dependent manner (Lieske et al 2000).
The cortex also exh ibits various forms of As alre ad y mentioned in the introduction, the
rhythms, which can be used to characterize differ­ generation of the walking rhythm depends also on
ent states of sleeps and wakefulness (McCormick a neural network, which is located in the spinal
2002, Steriade 2001, Steriade and Amzica 1 998, cord (Kiehn an d Ki aerulff 1 998). The same princi­
Steriade et al 1 994) . The generation of rhythmic ples as established for other rhythm-generating
cortical activity has been associated with con­ neural networks also apply for the central pattern
sciousness, as well as psych ia tric d isorders (Llinas generator for walking. The rhythm-generating
et al 1999). As already mentioned for the thalamic network responsible for the generation of w al king
oscillations, pathophysiological forms of cortical can b e isolated in a sp i na l cord preparation from
rhy thms un d e r l i e various forms o f epileptic neonatal rats. Even after isolation , this network is
seizures (McC ormick 2002). Understanding how still capable of generating a 'fictive' locomotor
these rhythms are generated by the nervous sys­ rhythm (i.e. neuronal activity that represents a
tem is therefore essential to the development of locomotor rhythm in the absence of a c tu a l

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F i ctive i n s p i ratory activity

Fig u re 5. 1 M ed u l l a ry s l i ce g e n e rates fictive res p i ra t i o n . PBC, pre - B i:i t z i n g e r co m p l ex.

l o c o m ot or mo v e m en ts) , in di ca ting that the cir­ it must be emp hasi zed tha t thi s is only the case
cuitry loca ted within the spinal cord is sufficient under artificial conditions, for example following
for generating a locomotor rhyt h m (Fig. 5.2). deafferenta tion, or following t he isolation of a net­
Studying fictive lo co m ot o r acti v ity in these w o rk under in vitro conditions. In th e presence of
spinal cord preparations h a s led to important new actual movements, this is certainly not the case,
in s ig ht s into the mechanisms that underlie the and sensory feedback will highly influence the
gene ra tion of walking. For further d e tai ls see var­ generation of rhythmi c acti v ity In the example of

ious reviews (Hamm et a l 1999, Jordan et al 1 992, the circa d i an clock, da yl i gh t constantly resets the
Kiehn and Kiaerulff 1998, Kiehn and Tresch 2002, circadian rhy th m so we wake up in the m o r nin g,
Kiehn et al 2000, Schmidt and Jordan 2000). One when daylight shines int o our bedroom. Intense
i m p o rt a nt take-home message is that these ' in light exposure he lp s to overco me j e t-lag and it has
vitro' e x pe r imen ts indi cate tha t the isolated spinal been used t hera pe utic a lly in shift-workers t o h el p
cord is c ap ab le of generating locomotor activ ity in them overcome problems associated w it h con­
the absence of sensory (proprioceptive) inp u t. stant changes in the sleep-wake cycle. The lack of
sensory s timula tion is a maj o r p rob le m fo r blind
people, in whom d aylig ht does not constantly
THE ROL E OF PROPRIO CE PTIV E I N P U T I N reset the circadian clock. These individuals have
THE G ENERATIO N OF RHYTHMIC ACTIVITY maj o r p ro b le m s with their 'free-running' circadian
clocks. Circadian changes in b o d y temperature
Alth o ugh central pattern generators can genera te and in ho rm o ne levels are non-synchronized,
rhythmic ac ti vi ty in the absence of sensor y in pu t, which great ly a ffec ts the daily life of bl in d p eop l e

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A d a p t i v e p r o pert ies of m oto r b e ha v i or 49

N M DA, se roto n i n

F i g u re 5 . 2 Isolated brainst e m spinal cord g e n e rates fictive l oc o m o t i o n .

Sensory inp u ts a l so pl a y a very important role 'reflex-reversal' (Hess and Buschges 1 999, Kn o p et
in the genera tion of wal kin g (Rossignol 2000, Pear­ al 2001 , Pearson et al 1 998). This h a s important
so n and Ram irez 1 997) . It i s now well established implica tions as it indica tes tha t different regula­
tha t sensory inputs contribu te to the generation tory mechanisms contribute to the neura l control
and maintenance of the rhythmic activity. Phasic of posture and walking.
sensory inp u t initia tes major phase transitions In w alking , the regulation of phase tra nsitions
from swing to s tance and from stance to s win g and the dura tion of a step are directly correlated.
phase. Sensory inputs are important in re g ulatin g For example, electrica l s timulation of group
the mag nit u de of the ongoing motor activity. The I afferen ts from knee and ankle extensor muscles
concept that p ro p r i ocep tiv e in p u t can regulate the during the ex tensor phase, prolongs the s tance
transi tions from one ph ase to another has been phase in wal king, decerebrate c a ts (Pearson and
demonsh'a ted in various studies (Andersson and Ramirez 1 997) . The u nl o a din g of extensor muscles
Grillner 1 983, Grillner and Rossignol 1978, Kriel­ is therefore thought to be a necessary condi tion for
laars et aI 1994) . The propriocep tors responsible for the initiation of th e s w in g phase during normal
these phase transitions seem to be muscle spindle walking. This sensory signal is produced by a
afferents that are located i n hip flexor muscles decreased a ctiv ity in the tendon organs of extensor
(Hiebert and Pearson 1999, Hiebert et al 1996) . muscles.
However, Golg i tendon organs are also important The role of proprioceptors in re g u lating the
for reg u l a tin g phase transitions. Located in exten­ timin g of pha s e transitions is functionally very
sor muscles, input from these so-called Ib afferents a d a p t i ve. This regulatory mechanism guarantees
has, du ring locomotion, an excitatory effect on that p ha s e transi tions are p reci s el y timed accord­
extensor motor neurons (Pearson and Collins 1 993, ing to the specific in ternal and environmental con­
Pearson et aI 1998) . Interestingly, s timul a ti on of the d itions. Proprioceptors are ideal for a ssuming this
same tendon organs has an opposite effect in the role as they synthesize information from the sta te
standing animal, indic a ting tha t reflexes are state­ of the mov in g body and from t h e s ta te of the
dependent, a phenomenon tha t is also known as environmen t.

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STAT E - D E P E N D E N T M O D U LAT I O N O F brains tem (Kiehn et al 2000 ) . There are reasons to

R E F L E X PAT H WAYS believe that these find ings also apply to the ne u ral
control of walking in humans (Calancie et a 1 1 994,
The sta te-dependency of propriocep tive integra tion Dimitrij evic et a 1 1998, Duysens an d van de Crom­
was already mentioned in the contex t of the reflex mert 1 998, Lamb and Yang 2000) . If this is the ca se,
reversal. Increasing evidence indica tes that reflexes these fin dings have important impl ications for
are not as simple as initially thought. Reflexes can various for ms of spinal cord inj uries . In spina l
drastically change due to a direct modula tion by cord inj ured people, the in ability to walk is often
efferent ganuna-inn ervation, which is highly state­ due to the interruption of descending inp uts from
dependent (Prochazka 1 989). However, reflex path­ higher brain centers, which are necessary to in iti­
ways are also chemically modulated within the a te and ma intain locomotion . If the absence of
central nervous system. For the respira tory system these descending in pu ts is indeed responsible for
it has been demonstrated tha t pulmonary reflexes the loss of locomo tion, an impor tan t consequence
are transmi tted to the central respira tory network is tha t the spinal network responsible for generat­
via the nucleus tractus soli tarius (NTS), an area tha t ing the walking rhy thm sho u ld s till be 'in tact' .
contains numero us neuromodulatory substances Therefore, it sho uld theore tically be possible to
( Bonham 1 995, Maley 1 996, Moss and La ferriere replace these mi ssing descending inp u ts ph arma­
2002) known to play an important role in modulat­ cologically in order to a c tivate the dormant walk­
ing breathing. These modulatory substances (sero­ ing rhy t h m -genera ting ne twork. Important
tonin, substance P, ace tylcholine, endorphins, chemica l messengers released from descending
thyrotropin-releasing hormone (TRH)) are known neurons include sero tonin, dopamine and nora­
to affec t membrane proper ties of respiratory neu­ drenaline (norepinephrine) and, in theory, exoge­
rons ( Dekin et al 1 985, Telgkamp et al 2002) and nous applica tion of these amines sho uld ac tiv a te
hence transm ission of re flex p a thway s . When locomotion . It is well established tha t exogenous
released during hypoxia, the modula tors may con­ applica tion of either of these subs tances can evoke
tribute to an increased ventila tory drive by a ltering forms of locomo tion in cats following spin a l cord
transmission in reflex pathways from afferents of transection . And in fa c t it ,vas possible to ini ti ate
the carotid body (Wickstrom et aI 1 999) . s tepping movements in paraplegic pa tients using
aminergic substances ( Remy-Neris e t al 1 999,
Rossignol et a1 1 996, Wainberg et a I 1990).
N E U R O M O D U LAT I O N A N D Why is the rh ythm genera tor for walking inac­
R E C O N F I G U R AT I O N O F R H YT H M ­ tive in the absence of descending inp uts and how
G E N E R AT I N G N E TW O R KS W I T H I N T H E can amines activate a rhythm-genera ting neuronal
C E N T RA L N E RV O U S SYST E M network? One p ossible explanation is tha t descend­
ing inputs provide a tonic exci tation, which is nec­
Neuromodula tory processes also play important essary to activate the neural network for walking. If
roles in controlling the rhythm-generating network this were the case, any exci ta tory stimulus th at
within the central nervous syste m . Altho u gh, the depolarizes the membranes of locomotor neurons
spinal cord is cap able of genera ting fictive loco­ should initia te locomotion. This is, however, not the
motion in the absence of higher brain centers, they case. For example, raising the potassium concentra­
are not capable of genera ting l ocomotion sponta­ tion in an isola ted spinal cord would depola rize
neou sly. To ini tia te fic tive locomo tor activity it is locomotor neurons, but this trea tment will not initi­
necessary to apply sero tonin and NMDA exoge­ a te locomotion. It is necessary to apply aminergic
nously, presumably in order to compensa te for the substances in order to activate the rhythm-generat­
missing descending a minergic inp u t from the ing neural network . How could a mines such as

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A d apti ve prope rti es of m oto r b e havi or 51

serotonin or also dopamine lead to the activa tion of and are capable o f generating reciprocal rhythmic
a rhythm-generating network? There is a huge ac tivi ty. Indeed, comp utational models have
body of literature indicating that amines act as neu­ demonstrated tha t tw o groups of neurons can
romodula tors in neuronal network, leading to the generate rhythmic activity if the neurons contain
modulation of membrane properties and synaptic certain membrane proper ties, such as for example
transmission (Nusbau m et al 200 1 ) . Some of these the so-called Ih current (Sharp et al 1996). The
properties are known to play important roles in the concept of a half-center network has been very
generation of rhythmic activity. influential and has been adopted to explain the
Membrane properties that are very important genera tion of rhy thmic motor activities in many
for the generation of mos t rhythmic activities are motor sys tems, such as the swimming movements
the so-called plateau potentials or pacemaker in lamprey (GrilIner et al 2000), locomotion in
p roperties. P acemaker properties have been Xenopus (Tunstall et al 2002), and the breathing
demonstra ted in neu rons of the thalamus (Lu thi movements in mammals (Richter and Spyer 200 1 ) .
and McCormick 1 999) , SCN (Nitabach et al 2002, Similarly, reciprocal inhibition seems t o play a role
Wang et al 2002), cortex (Brumberg et aI 2002), and in establishing the differen t phases of locomotion
p re-Bo tzinger complex (Thoby-Brisson and in spinal cord preparation of neonatal rats. Synap­
Rami rez 2001; Thoby-Brisson et al 2000) . In many tic interac tions, such a s those necessary for estab­
cases, it has been demonstrated tha t these pace­ lishing rhythmic motor activity, are known to be
maker properties are dependent on the presence targets of neuromodulators like serotonin and
or absence of neuromodulators, such as serotonin dopamine (AyaJi et al 1998). Thus, it can be
(Pena and Ramirez 2002) . This is very well docu­ assumed tha t descending aminergic drive may
mented for rhythmic activity in thalamic relay influence the generation of walking by modulat­
neurons, which can be ind uced or suppressed ing synaptic in teraction between rhythm-genera t­
depending on the presence of sero tonin or adren­ ing neurons in the spinal cord .
aline (epinephrine) (McCormick and Pape 1990). An important concept derives from these and
Pacemaker properties can also be induced by many other findings obtained in rhythm-generating
NMDA . This has been demonstra ted in spinal neuronal networks (e.g. Pearson and Ramirez
cord neurons, thus explain ing the abi li ty to induce 1 997) : a rhythm genera ting neural network is not
fictive walking in isolated spinal cord prepara­ 'hard-wired', but flexible. In the p resence of neu­
tions (Parker and Grillner 1999 ) . romodula tors, pacemaker properties and synap tic
In many motor sys tems, it has a l s o been transmission can be modulated, changing the char­
demonstrated tha t amines can induce long-lasting acteris tics and connectivity of rhy thm-genera ting
constant discha rges, which are due to the activa­ networks . This is highly relev ant as we have to
tion of so-ca lled plateau-potentials. The induction envision tha t a rhythm-generating network is
of plateau-poten tials by serotonin has been embedded in a 'soup of neuromodulators' which
demonstra ted in spinal motor neurons (Houn­ are released in a state-dependent manner from
sgaard and Kiehn 1993) and there is good evi­ descending as well as local neurons and which
dence that these plateau-poten tials are important constantly change the properties of the network
for the control of posture (Kiehn and Eken 1997) . and the propriocep tive pathways as discussed in
Presumably the most important synaptic mech­ the previous paragraph. The exact composi tion of
anism for the genera tion of rhythmic activity is this 'soup of neuromodulators' will not only be
reciprocal inhibi tion . The so-called half-center state-dependent, b u t it will be highly variable in
model predicts that two groups of neurons, which different individuals and will also change dramat­
are connected via synap tic inh ibition and which ically du ring ontogenetic development. This
receive a tonic excitatory drive, become bi-stable characteristic may at least partly explain why the

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deta i l s of locomotion, and also the details of pos­ the ex ternal env ironment, in body size and in body
ture, will not be the same in any two individuals. weigh t . However, these changes may not only be
adap tive and one migh t specula te tha t a behavio r
may become maladap tive if any of these cha nges is
T H E DEVELO P M ENT O F M OTOR N E U RAL disturbed, either in i ts time course or in its magni­
NETWOR KS tu de. Such on togenetic changes at the molecular
level may explain why many d iseases are very
There is increasing evidence tha t synaptic and characteristic for a certain s tage of ontogenetic
membrane properties change drama tically during development. There a re numero us examples, such
p o s tn a ta l developmen t . For exa mple, the composi­ as sudden infan t d e a th synd rome (SIDS), schizo­
tion of the glycine receptor changes postna tally phrenia, manic disorders or Al zheimer ' s disease,
(Laube et al 2002). These changes are associ a ted which occur or begin typically in very specific age
with physiological changes in the properties of groups . Unders tanding which molecular fac tors
synap tic transmission . As the gl ycine receptor is are maladap tive will be one of the impor tant chal­
abundant in the spinal cord, these changes may lenges in fu ture medica l resea rch .
play an imp ortan t role in establishing reciprocal
a c tivity during walking. However, the changes in
the glycine recep tor are only one example, and CONCL USIONS
simi lar on togenetic changes have been described
for most o ther transmi tter recep tors and ion chan­ In this chapter, principles were summarized tha t
nels, indicating tha t presumabl y most neural net­ are relevant not only for the genera tion o f walk­
works undergo drama tic, ontogenetic changes. ing, but for the gen eration of rhythmic ac tivity in
This will presumably res u l t in stri kingly different genera l. One of the mos t important messages is
adaptive properties of most behaviors. However, tha t these networks are highly flex ible . In the case
we are far from understanding the details of how of the motor behavior, locomo tor c ircuits and
these postnatal changes at the molecula r level reflex pathways can rapidly adapt a mo tor behav­
transla te into changes in behavior. This lack of ior to changes i n the ex ternal environment. As
unders tanding is partly due to the complexity of imp ortant, however, are long- term changes tha t
developmental changes. For example, the time a l ter network properties an d reflex pathways to
course of any of the known postnatal changes d i f­ a dj us t a motor behavior to ch anges in body size
fers in different regions of the bra in . Postnatal and weight. In particular, d u ring on toge netic
changes described in one cortical layer may be d i f­ developmen t, these a djus tments are essen ti al to
feren t from postnatal changes that occur in another guaran tee a well-adapted mo tor behavior. Long­
layer of the cortex. The same p resumably applies term changes occur also in associa tion with motor
to all o ther parts of the cen tral nervous system . learning, a form of plastici ty tha t i s par ticu larly
Despite this complexi ty, and d espite the lack of relevan t for a developing chi l d . Th is chap ter has
a concrete understand ing of how these molecular summarized possible neural mechanisms tha t
and cellular changes translate into changes a t the c o u l d contribute t o long- term a n d short- term
behaviora l levels, these findings emphasize tha t changes and emphasized the po tential role of
t h e central nervous system h a s t o be considered as chemical modula tors in reg u l a ting membrane
a very pla s tic entity, which undergoes dra m a tic properties and syn a p tic tra nsmission. These mod­
short- term and long- term changes. These changes ulatory changes can res u l t in varying degrees o f
will res u l t in drama tic changes in behavior, which changes in the network configuration, which c a n
for the most part will be adaptive, adj usting the lea d t o a complete reconfiguration of a neural net­
organism to changes in postnatal development, in work, such as in the case of the resp ira tory net-

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Ad a p t i v e p ro p e r t i e s of m o t o r b e h a v i o r 53

work where i t c a n genera te s i g ni fi c antly differen t the developmental, in te rn a l and external cond i­
fo rms of b rea thin g, such as ga sping or sighing. tions. It i s therefore not surprising tha t the po st u re
Ne twork reconfi g u r a ti ons, howe ver, occur not and walking behavior of any ind i vidual will differ
only in re s p o n se to the release of neuromodula­ from that of a n o th e r individual. Given th e com­
tors . Dra m a tic ch anges can also occur as p a r t o f a p lexi t y and plasticity of these neural networks it is
genetic pr o g r am d u r in g on t oge n etic de v e l op­ indeed s ur p ri s ing tha t m ost in div id u a l s m an a ge
ment. It is ,·vell es t abl i shed tha t all mol ecul a r com­ t o prod uc e a we l l adapted 'normal' l ocomotor

ponents of a neural network u n de rg o dramatic behavior and p o s ture. This in dica te s t h a t s tro n g
changes a n d re o rgan i z a ti ons tha t translate into sel f re gula ting mechanisms must exist tha t con­

de v el o p men ta l chan g es of a m o t o r behavior. s tan tl y ad j u s t neuron a l network pro per ti es in

Thus, an imp o r ta n t lesson learned from these o r de r to avoid major deviations from a 'normal'
studies is tha t neuronal n e tw orks are amazingly beha v ior .

plastic and con tinuously changing depend in g on

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Chapter 6

Neuromotor development in
infancy and early childhood
s. Huber

I 'J.MI:I'


Introduction 57
Learning complex motor skills up to their virtuoso
Brain maturation and myelination 60 performance is a very long and protracted process
Development of motor skills 60
wh ich normally extends over several years. If

Biomechanics, practice and environment 61

we compare motor control in child ren and adults,
Perception and motor development 62
young adolescents still show substantial differ­
Eye-hand coordination in the first
ences in efficiency and accuracy of performance in
year of life 64
motor tasks. Even elementary motion sequences
Motor development beyond the first
like srnihng, grasping of an object, sitting, walking
year of life 68
and speaking take mon ths to years to be per­
Cognition and perception 69
formed efficiently. The movement of newborn s, in
Summary 70
contrast, appears very uncontrolled and variable.
For a long time, it was cons i dered as fact that
brain mat u ra ti on alone is responsible for the
development of motor skills. The theory of matu­
ration, which was predominant during the 1920s
to 1940s, was mainly developed and pushed for­
ward in the domain of motor develop ment by
Gesell (1933, 1946) and McGraw (1945, 1946).
They assumed that the regulari ties that can be
observed in the process of motor development
reflect the development of brain maturation, i.e.
the unfolding of a genetic program that was sup­
posed to be the same in all infants. The underlying
idea of their theo ry was that the maturation of
motor skills reflects the hierarchy of the central
nervous system: When an infant matures, higher
brain areas of the motor cortex take over the tasks
of the subcortex and inhibit the subcortex. Reflex­
ive and immature motion patterns are rep lace d by

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coordinated and directed movements controlled to be planned on a much more abstract level, as it
by the cortex. The theory of maturation also would be far too complex for the central nervous
assumed that there is a fixed sequence of motor system to program all the local and context­
development in which practice and the environ­ dependent, dynamic variables in advance.
ment play only a subordinate role. Bernstein thus described movement as a prob­
Phenomenological experiments have been con­ lem of coordination, i.e. as the coordination of a
ducted to support this view. Catalogues were cooperative interaction of many partners to gain a
developed with lists of stages (Gesell 1933, uniform result. The problem, according to Bern­
McGraw 1945, Shirley 1931) detailing age-specific stein, is how the organism with its almost indeter­
behavior as well as how children gain control over minable number of combinations of body segments
their movements. For throwing objects, for and positions finds a solution to enable all parts to
instance, 58 stages were specified, for rattling 53 work together harmoniously and efficiently, with­
stages, etc. One of the studies cited repeatedly as out every step being programed in advance. This
evidence for the maturation theory was a culture new way of thinking about movement control has
study, dating back to 1940, on the development of led to a rethinking of the principles of motor devel­
walking in infants of Hopi Indians (Dennis and opment, resulting in theories that put forward a

Dennis 1940). Infants from the Hopi community multicausal view of motor development (Newell
spend most of their first year of life wrapped up 1986, Thelen 2000). These theories assume a
tightly in a cradle and carried around on their dynamic system where the environment, the devel­
mothers' backs. According to this study, although opment of the perceptual system, biomechanics
these babies can hardly move, they learn to walk and muscle power complement the maturation of
only slightly later than infants from Western tradi­ the brain as principal components.
tions. The fact that these infants were only slightly These more recent theories (e.g. dynamic systems
delayed in learning to walk despite an apparent theory -Thelen 1995, 2000) assume that due to
lack of constant practice was cited as evidence that only few movement restrictions at the beginning
behavioral changes in motor control are directly of life, the infant can draw upon a large variety of
linked to changes in the brain. motion patterns to execute spontaneous move­
This view of a direct causal link between matu­ ments. This variety of motion patterns implies
ration of the brain and behavioral changes is that all possibilities of motor control can be
highly plausible and is still held today to some explored. At the same time it makes these patterns
extent. Until the mid 1980s, this view of motor suitable for a changing environment. The infant
development was actually predominant. It was learns to restrict this variability as more functional
onl y when Bernstein's new way of looking at motor programs develop.
motor coordination became known that a para­ Practice, as gained by the increasing experience
digm shift occurred (Bernstein 1967) (for review of the motor system as well as the sensory system,
see Sporns and Edelman 1993). plays a crucial role in the development of specific
Bernstein (1967) challenged the view of a 1 : 1 motor skills. Visual, vestibular and proprioceptive
mapping of neural code, firing of motor neurons information allows the infant to fine-tune balance,
and actual movement, which had been postulated head and body control as well as grasping move­
by brain maturation theories. He took a fresh look ments on the basis of visual, tactile and kinesthetic
at the problem of motor development, suggesting information. This integration of new motor strate­
that a movement can be caused by a variety of dif­ gies is brought about by a process of neural selec­
ferent motion patterns, and the pattern of how tion. At the beginning, the infant executes
movement is executed can, in tum, be executed in spontaneous movements which are subject to high
a variety of ways. This implies that movement has variability. Motion patterns can be evaluated via

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Neuromotor development in infancy and early childhood 59

sensory feedback and connections can be selected "'

which fulfill ClUrent needs or which seem to lead to Motor areas of the cerebral cortex

an important skill for the futlUe. Finally, neural con­ ,....

m- Primary motor cortex, supplemental
motor area, premotor cortex

nections that are related to the most efficient motor �. -.i

patterns are strengthened and others are inhibited.
But why does motor development take so long?
One reason is that motor control is only possible ( Thalamus
based on a highly complex nervous system with a
huge number of connections. These connections
send out motor signals, but provide a continuous
Basal ganglia
feedback about the ClUrent state of the system, too, nucleus caudatus,
during the movement being executed (Fig. 6.1). putamen,
globus pallidus,
Eliot (1999) illustrates the problem of move­
nucleus, subthalamicus,
ment control with a simple example: When a substantia nigra
straightforward arm movement is executed, the
biceps bends and the triceps is stretched at the
same time. The command of such a voluntary
movement is generated in the motor area of the
cerebral cortex. There are three motor areas which �( Cerebellum
, .
L Bramstem
are all located in the back part of the frontal lobe:
the primary motor cortex, the supplementary
motor area and the pre-motor cortex. The primary
{ Spinal cord r
motor cortex triggers voluntary movement, while
the other two operate on a higher level and control Sensory receptors j !
more complex sequences of motion. The motor
cortex -like the somatosensory cortex - contains a
distorted upside-down map of the body, the
homunculus: the lateral regions of this area con­ ( Muscle contraction ]
trol the muscles of the head and the face, the mid­ and movement

dle regions control the arms and hands, and the

Figure 6.1 Motor circuits involved in the execution of
medial regions are in control of the legs and feet
voluntary movements (Ghez 1991).
(Penfield and Rasmussen 1950). This distorted
map allocates bigger areas for those body parts - of the movement, the muscle undergoes changes
such as hands and the face - that possess more in tension and length, which again are perceived
muscles, since they have to execute more complex by special sensory neurons, the proprioceptors.
movements than for example the trunk or the legs. Proprioceptive information feeds back to the
If a voluntary movement of the arm is executed, spinal cord, where the firing of muscle motor neu­
the neurons of the arm region of the left motor cor­ rons is modified, and on to the cerebral cortex
tex send action potentials to the spinal cord, which where the arm position is perceived. Propriocep­
is connected via the corticospinal tract. In the tive information allows the movement of the arm
spinal cord, the neurons of the corticospinal tract to be felt and to be fine-tuned millisecond by mil­
excite motor neurons, which send out their axons lisecond. All this is most likely to happen parallel
via peripheral nerves to reach the muscle fibers in to hand and finger movements. In addition, infor­
the arm. The electrical excitation leads to a con­ mation is integrated from the visual system, which
traction of the relevant muscles. At the beginning provides information about the arm position to the

Copyrighted Material

motor cortex in order to control muscle contraction The higher areas of the brain are hardly devel­
and relaxation. Highly elaborate tasks, such as oped at birth. Maturation of the brain areas
walking or postural balance of the whole body, develops from caudal to cranial areas and from
where dozens of muscles are involved, are even dorsal to ventral areas (Grodd 1993, Staudt et al
more complex tasks for the motor control system. 2000): motor connections in the spinal cord
The cerebellum is mainly responsible for the mature first, long before birth, followed by the
precise coordination and timing of all these move­ neurons of the brainstem and the connections in
ments. It receives input from the motor cortex (i.e. the primary motor cortex. Finally, the higher
information about the kind of movement that is to brain areas located in the frontal lobe attain
be executed) as well as from different sensory sys­ maturation. The motor neurons which leave the
tems, such as vision, hearing, balance and pro­ spinal cord are among the first fibers in the brain
prioception (i.e. information about the actual to myelinate (by mid-gestation). Myelination of
movement). The cerebellum controls and times the the motor areas in the brainstem starts in the last
movements by comparing the incoming informa­ trimester of pregnancy. The fibers and connec­
tion, and modifies the motor commands to achieve tions of the primary motor cortex b eg in to myeli­
the best possible result for the execution of the nate around birth. Myelination in this area takes
movements. The basal ganglia play a central part about 2 years. The myelination in the frontal lobe
in movement control, too. Here motor actions and progresses very slowly. The fibers of the pre­
inhibiting involuntary movements are selected. motor cortex and the supplementary motor area,
Patients with Parkinson's disease or Huntington's for instance, do not begin to myelinate until about
disease, for instance (who show disorders in the the age of 6 months and then continue to do so for
basal ganglia), have great problems initiating vol­ several years.
untary movements. They often have difficulty talk­ With the brainstem maturing early, the order of
ing or walking, or their movements are very slow. motor development is from central to peripheral
In contrast to patients suffering from paralysis, body parts, since the muscles of the trunk and the
however, they move quite a lot, though most of head are mainly controlled by the motor connec­
their movements are involuntary. The basal gan­ tions in the brainstem, whereas the muscles of the
glia also have a strong connection to the thalamus, peripheral body segments are controlled by the
which receives sensory as weU as motor informa­ motor cortex. In fact, infants are able to control
tion (from the cerebellum, the spinal cord and the their trunk and their head muscles before they can
basal ganglia) and sends it on to the cortex. control their arms and legs or their hands and fin­
gers. The maturation of the primary motor cortex
also influences the sequence of motor develop­
BRAIN MATURATION AN D MYELIN ATION ment. Myelination and maturation start in the
lower areas of the primary motor cortex and
It cannot be denied that maturation of the central progress upwards, i.e. control over the muscles of
nervous system plays a crucial role in the devel­ the face is gained before that over ha nds or feet.
opment of motor skills, although it is clear today Infants, therefore, can tum their head and smile
that there is no exact mapping between the two before they learn to grasp, crawl and walk.
because of the environmental influences that have
just been described. The motor cortex undergoes a
great deal of modification during the first year. DEVELOPMEN T OF MOTOR SKILLS
The most important neuromotor changes, which
lead to a predictable sequence of development of Neuromotor development is a long-lasting
motor skills, are described below. process. It sets in some weeks after fertilization

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Neuromotor development in infancy and early childhood 61

and then continues several y ears after birth until maturation of the brain have an impact on motor
reaching completion during puberty. Thanks to development. The organism, biomechanics, and
the advanced use of ultrasonic imaging, there is muscle power are said to play an important role at
now a fairly clear and comprehensive under­ every step of motor development. Already in
standing of the prenatal development of motor 1931, Shirley documented that differences in
skills. infants' physical growth, muscle tone, and energy
The fetus is active from the 8th to 10th week of levels were related to differences in the onset of
gestation, showing spontaneous activity as well as various motor skills.
structured activity patterns from the very begin­ Physical dimensions, biomechanics and move­
ning (Prechtl 1985, 1993). Initially these are move­ ment styles are still seen as an important part of
ments of the whole fetus, spontaneous arches and motor development (Thelen 2000). The influence
curls, but very soon the limbs themselves move of biomechanics has been studied by Thelen and
and initiate entire body movements. Isolated arm her colleagues in a series of experiments testing
and leg movements start at about the 10th week, walking skills. If newborns are lifted up so that
finger movements set in 2 weeks later. From the their feet touch the ground while being supported
11th week onwards, the fetus starts to bring a under their arms, they will readily show step-like
hand to its head, but it only starts to suck its movements which have a close resemblance to the
thumbs after approximately 5 months. walking pattern of older infants. It is astonishing
Other astonishing motor skills which develop in how coordinated these movements are already in
the first 3 months are hiccups, stretching, yawning, newborns, who can hardly control their head.
swallowing and grasping. These movements are After a few weeks, this reflex disappears, only
already highly coordinated right from the start. In reappearing later in the year when the infant is
the second half of pregnancy, the fetus commences ready to learn to walk.
with continuous breathing movements. The lungs, Traditionally, the disappearance of the step-like
at this point still filled with liquid, start to expand movements, the so-called walking reflex, in new­
and compress together with the diaphragm and borns after just a few weeks was explained by the
thorax in a rhythmic and coordinated fashion. fact that the first subcortically driven reflex is
Sucking and swallowing become more coordi­ inhibited by the developing motor cortex
nated from the 28th week onwards. From week 33 (McGraw 1945). This inhibition is only suspended
onwards both swallowing and sucking are coordi­ if the motor cortex is mature enough to take over
nated with breathing movements. These processes control of the subcortically driven processes in a
seem to be at least in part an expression of the coordinated way.
launch of activity of the developing neural system. Investigations of the rhythmic kicking behavior
In addition, some of these behavioral patterns also of infants who are just a few months old and lying
fulfill functions of adaptation, provide behavioral on their back show, however, that the walking
patterns for later use (such as breathing and suck­ reflex does not disappear at all. The kicking move­
ing) or constitute precursors of later movement ments directly match the rhythmic step-like
patterns (Hall and Oppenheim 1987). movements of newborns. The only difference is
the position in which the infant's body experi­
ences the effect of gravity: infants lying on their
BIOMECHANICS. PRACTICE AND back can lift up their legs more easily than those in
ENVIRONMENT an upright position.
Thelen and her colleagues showed that infants
Recently, a number of studies have been con­ that seem to have lost their walking reflex also
ducted to show which other factors besides the start to show the pattern spontaneously when

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their legs are under water (Thelen et al 1984). However, only the infants with loosely tied legs
Underwater gravitation has less effect due to moved their legs in an increasingly simultaneous
buoyancy. They also demonstrated that younger pattern.
infants do not show this walking pattern if their The study suggests that infants at the age of 3
legs are made heavier with little weights (Adolph months can discover and learn a match between
and Avolio 2000, Thelen et al 1987). Infants, thus, inter-limb coordination patterns and a specific task.
seem to stop showing the stepping reflex because Acquisition of new motor skills, thus, seems to
their weight gain during the first months of life is depend on learning processes such as these, rather
not matched by an increase in muscle mass or than autonomous brain 'maturation' (Thelen 1994).
force, therefore depriving the infants of sufficient At the age of 3 months infants are already able to
power to lift the legs in an upright position. This quickly solve new tasks in which, for instance, cer­
interaction between intrinsic and environmental tain knee positions (such as bending and stretching
constraints has also been studied in the domain of of the knee) have gained positive feedback
reaching by Savelsbergh and van der Kamp (Angulo-Kinzler et al 2002). Another example
(1994). They showed that body orientation with comes from a study by Goldfield et al (1993). They
respect to gravity has an effect on the quantity and investigated how infants learn to use a Jolly Jumper
quality of infants' reaching behavior. (a baby seat attached to elastic ropes): infants
Besides the influence of biomechanics and body started with only a few bounces, which had irregu­
layout, important factors are the possibilities to lar amplitudes and periods. As the weeks passed,
practice motor control, and perceptual stimulation infants increased the number of bounces and at the
from the environment. New insights in motor same time decreased their period and amplitude
development strongly emphasize the role of explo­ variability, settling in on a frequency which was
ration and selection in the acquisition of new consistent with the predicted resonant frequency of
motor skills. The infants' first step is to discover the infant-bouncer-spring system.
configurations that enable them to perform a cer­
tain motor task; these must then be fine-tuned to
the required smoothness and efficiency. Thelen PERCEPTION AND MOTOR DEVELOPMENT
(1994) demonstrated that by the age of 3 months
infants can, given an appropriate and novel task, Recent advances in the understanding of human
already transform their seemingly spontaneous movement control have enabled developmental
kicking movements into new and efficient motor psychologists to discover unique patterns of
patterns. organization and control in infant motor behavior
Thelen and her colleagues investigated the and development, and triggered new interest in
kicking movements of 3-month-old infants who this topic. The tuning of movement patterns
were allowed to control the movement of an over­ shown in several examples above is most proba­
head mobile by means of a string attached to their bly established through repeated cycles of
legs. In one group, the infants additionally had perception and action as well as through the con­
their two legs tied loosely together at the ankles. sequences of the action in relation to the goal. We
The soft elastic allowed the infants to move their will come back to this in the next section where
legs in any coordinated pattern of alternating, sin­ we consider the development of eye-hand coor­
gle, or simultaneous kicks, but simultaneous kicks dination in detail. Besides perception influencing
provided the strongest activation of the mobile. the development of action, some researchers pos­
All infants kicked more often as well as faster tulate not only that motor development is sup­
when their kicks activated the mobile as com­ ported by perceptual development but also that
pared to when their kicks did not have any effect. motor development may play a predominant role

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Neuromotor development in infancy and early childhood 63

in determining developmental sequences or depth perception. In both cases, there is a high

'timetables'in the domain of perception (Bushnell degree of fit between the developmental
and Boudreau 1993). Specifically, they argue that sequence in which certain perceptual sensitivities
particular motor achievements may be integral to unfold and the age of onset of corresponding
the development in the domains of haptic and motor abilities (Fig. 6.2).

Static contact Enclosure

(temperature) (volume and size)

Lateral motion Pressure

(texture) (hardness)

Unsupported holding Contour following

(weight) (exact shape)

Figure 6.2 Hand movement patterns which have been found to be most suitable for apprehending specific object
properties (from Lederman and Klatzky 1987, with permission of Elsevier Science).

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Figure 6.3
Experimental setup and stimulus material in an experiment on haptic perception
(from Streri and Spelke
1988, with permission of Elsevier Science).

Evidence for these connections is found, for see also Wilkening and Krist 1998). Eye-hand
instance, in experiments conducted by Streri and coordination undergoes profound development
Spelke (1988; Streri et al 1993). They investigated throughout the first year of life , when children
4.5-month-old infants' perception of the unity learn how to grasp for objects and how to manipu­
and boundaries of haptically presented objects late them. Besides the development of efficient
(Fig. 6.3) . When infants actively explored the two motor programs, the development of object percep­
handles of an unseen o bjec t assembly, perception tion as well as proprioceptive and visual perception
of the un ity of the assembly depended on the han­ of the hand play important roles in developing
dles' motion. Infants perceived a single, connected skilled motor control of the arm, hand and fingers.
object if the handles moved rigidly together, and For newborns, arm and hand movements are
they perceived two distinct objects if the handles closely linked. The bending and stretching of the
underwent vertical or horizontal motion. arm is often accompanied by the bending and
stretching of the hand. Only at about the age of 2
months does this coupling disappear. At this age,
EYE-HAND COORDINATION IN THE FIRST the hand is mostly formed to a fist when the arm
YEAR OF LIFE is stretched. Especially at this age (2 to 4 months),
the hand possesses an important function for per­
In this section we take a closer look at the devel­ ception, i.e. in the haptic experience of objects.
opment of a special skill , eye-hand coordination, Hand and eye work more or less independently
which is probably the most intensively investi­ from each other at this age. Infants often fixate one
gated field in motor development (for an overview object with their eyes and investigate another

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Neuromotor development in infancy and early childhood 65

one with their hands (Hatwell 1987). At the age of low the hand with their gaze (Piaget 1973, 1975b,
3 months, infants resume opening their hand White et al 1964).
while stretching the arm, when they fixate an Only from the age of 5 months onwards do
object. But infants younger than 4 months are gen­ infants, when reaching for an object, show a better
erally not able to target and grasp a seen object. result if they can see not only the target but also
Infants, on the other hand, who are about to start the grasping hand (Lasky 1977, McDonnell 1975).
grasping are not interested anymore in just hapti­ This is not to mean, however, that coordinated
cally exploring the target object (HatweU1987). grasping attempts are executed solely under the
Because of this developmental sequence, the visual guidance of the hand. Important empirical
belief was widely shared for a long time that evidence comes from a number of studies on
initially eye and hand are controlled independ­ grasping in the dark and grasping for moving
ently from another. Only at about the age of 3 or 4 objects. Infants aged 4 to 7 months can grasp
months, when infants begin to grasp, does the for objects in the dark even if they can only be
coordination of eyes and hands start. However, located by sound, if they glow in the dark or if they
recent studies show this view not to be correct. were located before it got dark (Clifton et aI 1973).
Although the spontaneous arm movements of new­ Nevertheless, if continuous sight of the object is
borns seem to be aimless under supporting condi­ available, infants use vision during the reach. How­
tions - one of which is support of the body of the ever, they can still reach for an illuminated object
infant - studies show that the movements depend even if it is darkened during the reach (McCarty
on the direction of the visual goal. Von Hofsten and Ashmead 1999). These results are astonishing
(1982) was able to demonstrate that 5--9-day-old in light of the fact that infants from this age until
infants already show a rudimentary eye-hand the age of 8-9 months do not reach for an object if
coordination. As the arm movements of new­ it disappears behind another object in front of their
borns typically consist of several uncoordinated eyes (Piaget 1975b). Diamond showed that it seems
sub-movements, von Hofsten chose only the sub­ to be important that the object can be reached on a
movements that brought the hand nearest to the direct path without having to plan detours (Dia­
aimed target. He compared the direction of move­ mond 1990). Taken together these results indicate
ments where the infants fixated the target with their that infants do not necessarily have to guide their
eyes with direction of movements where they did hand visually when reaching for an object.
not fixate the target. The results showed that infants Experiments on reaching for moving objects
miss the target with fixation by on average 320 and have been conducted mainly by von Hofsten and
without fixating the target by about 5T Thus, eye co-workers (von Hofsten 1980, 1983, 2002). Von
and hand do not work independently of each other Hofsten and Lindhagen (1979) examined infants
in newborns. between 12 and 30 weeks of age once every 3
Eye-hand coordination is, however, only rudi­ weeks as to their development in reaching for
mentary in newborn infants. Newborns direct the moving objects. An object was moved back and
arm approximately by fixing the goal. This ballistic forth in front of the infant such that it got into
movement is triggered by the visual input. Infants reaching distance for a certain amount of time. At
at the age of 5 months, on the other hand, start to the same time as infants learned to reach for static
move their hand under constant visual control objects, they successfully reached for moving
and systematically move their hand nearer to the objects. At the age of 18 weeks, they successfully
target. The movement is visually guided (Bushnell grasped for objects that moved at about 30 cm/s.
1985). Before infants start to guide their move­ At this speed, they had to start the reaching move­
ments visually, it can be observed that they show ment before the object was in reaching distance.
an increased tendency to fixate their hand and fol- Thus, the infants at this early age anticipated the

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intersection point and pl ann ed the movement behavior was still present when confronting the
accordingly. The visually triggered movement that infants several times with the non-linear object
is observable in adults when they grasp accurately movement. Further s tudies show that infants from
for all k inds of obj ects is, therefore, already present the age of 5 to 7.5 m on ths reach for moving objects
in infants and does not devel op from visually that glow in the dark. Thus, even in such a com­
guided reaching. Von Hofsten (1983) also showed plex reaching task the p rop rioceptive information
that at 34 to 36 weeks of age, infants can already and the sight of the obj e ct are sufficient for an

catch an object, even if it moves at 120 cm/s. infant to successfull y reach for the object. Again
Recent studies investigated which critical vari­ the reaching movement is directed towards an
ables guide the e x tr apolation of object movement a n ticip ated intersection point (Rob in et aI1996).
(von Hofsten et al 1998). Six-month-old children In follow -up studies, von Hofsten et al investi­
were sitting in front of a screen when objects were gated what happ ens if the target is occl u d ed at the
presented to them which came into grasping dis­ point of crossing in the b rief period before it
tance on four different paths (Fig. 6.4); two were comes within reach (von Hofsten et al 1994).
linear and crossed each other in the middle of the Infants now either tended to reac h for the object
screen and two contained an ab rup t chan ge in the only rarely or they interrupted the grasping move­
direction of the crossing. The reaching movements ment very often. When presented with the same
a nd gaze direction of the children showed that the movement several times in a row (in a linear or
infants ex trapol a ted the object motion alon g a lin­ non-linear fashion ), 6- month-old infants showed a

ear p ath, acc o rd in g to the laws of inertia. This predictive gaze behavior after just a few trials for

Plotter -----_+_

Screen ------\:\

Plotter head ---�

Object -------

Infant seat ---\:- Schematic view of display screen showing

four different motion paths and reaching
areas (dashed elipses)

The experimental apparatus (side view) Top view of a subject reaching for the object

Figure 6.4 Experimental setup in a grasping experiment (from von Hofsten et al 1998, with permission of Elsevier

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Neuromotor development in infancy and early childhood 67

linear object motion (von Hofsten et al 2000), Apart from the tendency to grasp for an object
whereas the ability to predict non-linear object that is accidentally touched, systemic one- or two­
motion is only learnt slowly. handed motor tendencies in the reaching behavior
Further studies have shown that reaching of infants seem to be in conflict with the develop­
behavior did not improve if the occluder was ment of efficient grasping skills. Corbetta et al
transparent such that the object could be seen (2000) addressed this issue by investigating 5- to
behind the occluder. Thus, reaching behavior was 9-month-old infants' reaching and grasping
not reduced due to perceiving the occluder as a behavior for objects of different sizes and textures.
barrier for reaching (Spelke and von Hofsten 2001). Only infants older than 8 months were able to
The influence of the visual control of the hand scale their actions according to the visual and hap­
wanes during the second half of the first year in tic information available to them about the object.
favor of pre-programed movements, but it does Younger infants seemed to be locked into one
not disappear completely. During this phase, motor pattern: they could not select and switch
infants, just like adults, use the visually perceived between one- and two-handed reaching behavior.
relation between hand and target to reach for the A number of studies show that the ability to
target precisely in the final phase of the movement pre-program anticipatory hand and finger move­
and to compensate for unexpected replacements ments develops mainly in the second half of the
of the target (Ashmead et al 1993). The more pre­ year. At that time infants not only learn to open
cisely the reach can be pre-programed by the and close their hand at the right moment but they
infants the less dependent they are on other cor­ also start to consider the orientation of the hand
rection mechanisms. In fact, after already a few with respect to the object and other spatia-temporal
months of reaching practice, the infant is able to aspects of the movement (Lockman 1990, von
reach for objects with one quick arm movement. Hofsten 1989, von Hofsten and Ri:inquist 1988).
Nevertheless, difficulties may still arise if For example, they start to use a two-finger grip at
increasing demands are made on the motor skill. about the age of 9 to 10 months. Infants at this
It has been confirmed time and again that infants point in time are able to coordinate thumb and
of 5 to 6 months can reach and grasp for a free­ index finger such that a small object can be
standing object, but fail to retrieve the same object grasped and lifted between the finger tips.
if it is mounted on top of a larger object. Studies by The role of postural adjustment during sponta­
Diamond and Lee (2000) suggest that the findings neous and goal-directed reaching behavior has
can be explained by the lack of fully developed been investigated for example by van der Fits et al
motor skills. If infants reached for the upper object (1999). They investigated particularly whether the
but - due to an imprecise movement - touched the immature postural control of newborns and
lower object, they could not inhibit the reflex of young infants is responsible for the relatively poor
grasping the lower object instead of continuing to quality of pre-reaching movements.
reach for the upper object. If the demands on the Parallel to the development of the reaching and
motor skill, however, were reduced by decreasing grasping behavior, changes in postural control can
the possibility of the infant accidentally touching be observed. Newborns are already able to adapt
the base object (by just using smaller base objects), their posture to the current position, 3-month-old
infants successfully retrieved the upper object. infants can stabilize head and trunk and by the age
These new results replaced the long accepted view of 6 to 7 months, infants can sit upright with the
according to which infants do not understand help of arm support. At the age of 9 months, infants
conceptually that the object continues to exist sit upright even without support. In lying and sit­
when placed on another object and, therefore, stop ting adults, voluntary arm movements are accom­
grasping for it. panied, in particular, by activity in the neck and

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trunk muscles. The neck and upper tnmk muscles ing the movement's execution . Both spa tial and
seem to be responsible for opposing reaction forces temporal accuracy as well as speed of the move­
which a re generated by the reaching movements ment seem to improve with age. However, there
and the lower trunk muscles serve to stabilize the are some notable excep tions for certain tasks
center of mass. Fits et al fOlmd that in pre-reaching which are related to qual itative changes in the
in fan ts the spontaneous arm movemen ts are way of con trolling the movement, as these quali­
accompanied by postural muscle activity which is tative changes seem to be correlated to s tra tegic
highly variable (van der Fits et al 1 999) . changes in movement control (Connolly 1968,
As the infa nts get older, successful reaching Ha y 1 984) . Hay tested 5-, 7-, 9- an d ll -year-old
and adult-like temporal characteris tics of the pos­ children in a pointing task (Hay 1 984) . Children
tural adj ustment seem to emerge in parallel . These had to point to one of several target points which
results suggest a fundamental coupling between lit up randomly on a horizontal line, the view of
arm movements and pos tural control . hand and arm being occl u ded by a screen . Chil­
dren, thus, had to pre-program the arm movement
or use proprioceptive informa tion to adj ust arm
MOTOR DEVELO P M ENT B EYO N D THE and hand position with respect to the target.
FIR ST YEAR OF LI FE Mean accuracy was high for 5- a nd ll-year-old
children but low for 7- and 9-year-old chi ldren .
The abil ity to pre-program and execute the move­ How ever, 5-year-olds produced a high intra­
ment efficiently increases up to young adoles­ individual variabili ty, which decreased consider­
cence continuously (see also Wilkening and Krist ably with age. Taking movement time into account
1998) . Firstly, this is due to increased speed of as well, it can be seen that the movement pattern
planning, preparing and performing movements. prod uced by the d ifferen t age groups differs con­
Secondly, this is closely connected to the ability to siderably (Fig. 6.5). Five-year-olds produced a bal­
plan the movemen t accurately. The more accurate listic-like pattern with very sudden acceleration
the pre-programming, the fewer and less signifi­ and decelera tion phases. A t the age of 7 and still at
cant are the correc tions tha t have to be made dur- the age of 9 years, the poin ting movement consists

/...... ,
/ ' II
60 ....
50 JI

............. ... . . . . . . . . . .. . . . .... . .......



O �-----'----r--
o 5 7 9 11
Age (yea rs)
F i g u re 6.5 Pe rce n ta g e of e a c h type of vel ocity patte rn per age (from Hay 1 984, with pe rm i ss i o n of S p ring e r-Ve rlag ,
© Spri n g e r-Ve rl ag).

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Neuromotor development in infa n cy a n d ear l y chil dhood 69

of several sub-movements with braking activity and visual field decreased between 6 and 8 yea rs and
processing of (proprioceptive) feedback, whereas increased afterwards. Reaction time and move­
some 9-year-olds and especiaUy the ll-year-olds men t time decreased with age, except at the age of
again produce a ballistic movement in which feed­ 8 years when both tended to increase.
back control is now concentrated a t the end of the The same children participated in two control
movement sequence and all parts of the movement tasks which showed that the non-monotonic trend
are better coordinated. is not present if reacti on time is tested where no
Another experiment with 6- to 1 0-year-old chil­ spatial processing is required and vice versa
dren and ad ults on sequential pointing revealed a if spatial processing is tested but reaction time is
simila r non-linear development (Badan et al 2000 ) . not a constraint. The authors concluded that this
Badan et a l manipula ted the task difficulty b y asymmetry in the d ata seems to be due to differ­
changing the number, size and spacing of the tar­ ent processes involved in each task and tha t these
gets in the sequences. Children's temporal and processes undergo a quali ta tive change at the age
spatial parameters of the motor sequences showed of 8 years. Moreover their results seem to suggest
large age-dependent trends, but did not reach the tha t the prevailing processes tha t are transformed
adult values. This is consistent with the view tha t are loca ted in the left cerebral hemisphere
the neurophysiological mechanisms med ia ting (Pellizzer and Hauert 1996) . In fact, this observed
percep tual and motor functions are well devel­ asymmetry is compatible with studies indica ting
oped at the age of 6 and improvements are due to that homologous regions of both cerebral hemi­
a continuing process of fine-tuning the system. spheres develop asynchronously (Rabinowicz et
However, the au thors also found tha t increasing a1 1977, Thatcher et a l 1987) .
the difficulty of the task did not affect behavior in
a similarly uniform fashion. The performance of
the 7-year-olds, in particu lar, showed tha t the COGNITION AND P ERCE PTION
motor planning stra tegy characteristic of older
children seems to emerge at this age, though it has For many years, motor skills and cognition were
not yet superseded the less effective planning believed to be unrela ted, since many studies have
mode adop ted a t earlier s tages of development. shown only a modest correlation between motor
Thus, i t seems tha t motor development is not a and intellectual development (Piaget 1 975a,
lmiform fine-tuning of stable stra tegies. Instead, Shirley 193 1 ) . Piaget, on the o ther hand, believed
each stage of development is best characterized by that cognition comes about from perception and
a set of strategic components potenti ally available action. Nowadays it is agreed tha t the cognitive
at that stage, and by the age-dependent rules for development of children also plays an important
the selection of components in a given con text. role in the development of motor skills. This is par­
Pellizzer and Ha uert (1996) conducted a study ticularly true with complex skills where not only
to gain in forma tion abou t the origin of the tempo­ practice of a single movement is essential, but
rary decrease in visuo-manual performance occur­ other factors, too, such as general leaming ability,
ring around the age of 7 and 8 years. They assumed the ability to use feedback, processing capacities,
tha t cha nges occurring on a behavioral level are planning stra tegies, making decisions on which
consequences of those taking place on the neu­ information is essential and which is not, etc.
ronal level . They tested children between the age The rela tionship between percep tion, action
of 6 and 10 years in a visuo-manual aiming task. and cognition is rather complex and not comple tely
Results showed non-monotonic changes, which understoo d . Sometimes there a re aston ishing
were linked to age, spa tial accuracy, reaction time discrepancies between percep tual-motor compe­
and movement time. Spa tial accuracy in the right tencies and the corresponding cognitive knowl-

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70 T H E T H E O R ET I CA L B A S E

edge (Frick e t al
2003, Huber e t al 2003, Kr i s t e t a l direction; these chi ldren released the ball clearly
1993), whereas
in o ther cases cognition a n d con­ be fore being exac tly above the ta rge t .
cepts guide our ac tions (Krist 200 1 ) .
The ques tions t o be raised are whether concep­
tual knowledge guides a c tions, whether con­ S U MMARY
cep tual knowledge is derived from actions (as Piaget
would a rgue) and whether j udgments and ac tions Maj or developmental changes in motor control are
represent forms of knowledge that are insepara­ observed in p articular d uring the first 2 years of life.
ble. One field where these questions were inten­ This is mainly due to the fast progression of neural
sively studied is the field of intuitive physics ( i . e . development during this time. We have seen, for
people's intui tive c oncep ts a b o u t simple phenom­ instance, that maturation and myelination of partic­
ena o f motion), where knowledge expressed in ular brain areas are strongly related to the develop­
perceptual-mo tor tasks can easily be assesse d . ment of motor control over specific body segments.
Kris t et al ( 1 993) investigated, f o r instance, chil­ Motor development in children and young adoles­
dren's knowledge about projectile motion. They cents can best be characterized as a fine-tuning of
asked children from the age of 5 years onwards to accuracy and speed of movement, but also as a
propel a ball from various heights onto a target on development of movement control s tra tegies which
the floor at various distances . Besides the action cause characteristic qualita tive changes .
condition, a j udgment condition was used in For the dev elopmen t of specific motor skills i t
which, for each c ombination of platform height h a s been claimed that sensory stimulation and
and targe t dis tance, the speed of the ball had to be practice are as essential for the development of
j u d ged on a graphic rating scale. According to the neural p a thways as brain maturation i tse lf. This
laws of physics, speed in this si tuation is a direct new multic ausal view of motor development has
function of distance ( the farther, the faster), and an opened a rich field of research investigating the
inverse function o f height ( the higher, the slower) . different influences and effects of various environ­
Child ren's speed prod uctions reflected these mental, biomechanical, cogni tive, percep tual, an d
principles very well, with virtually no age trend neural factors on motor dev elopment.
from the youngest children up to adults. In the However, a profound understanding of the ir
j u d gment condition, however, 5-year-olds failed to rel a tive impor tance is sti l l missing . In this respect,
in tegra te the relevant dimensions, and many 1 0- the field of developmental cognitive neuroscience
year-olds ( and even several a d ults) showed strik­ is a particularly vigorous and rapidly growing
ing misconcep tion s . Most of these children seemed field of research (Nelson 200 1 ) . Scientists have
to hold an inverse-height heuristic : tha t the ball used various approaches for a be tter understa nd­
should fall fa ster the higher the platform of release. ing of neural correla tes of motor developmen t.
In o ther tasks, however, children used their Neuroimaging techniques are not well adapted to
concep ts to drive their a c tions . Krist con d u c ted a the study of movement skills and they are often
study in which children moving at constant speed not s u i table for studying normal young human
were a sked to hi t a target on the floor by dropping subjects. Therefore researchers study, for exa mple,
a ball (Krist 200 1 ) . Those children who held the infants (many of whom are born prem a turely)
concept ( assessed in a j u d gment condi tion) tha t an who have suffered perinatal brain lesions (Thelen
o bj e c t d ropping from a moving carrier fa lls 2000). These infan ts do not always atta in full
straight down, dropped the ball significantly l a ter recovery of function, nevertheless many of them
(above the target) than those who had the correct show considerable functional o u tcomes ( see
knowledge tha t the object falls in the forward Elman et al 1996 for a review ) .

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N e uromotor deve l opment in i nfancy and early ch ild h ood 71

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Clinical insights


7. Birthing interventions and the newborn cervical spine 75

8. Birth trauma and its implications for neuromotor development 85

9. Differential diagnosis of central and peripheral neurological disorders in infants 99

10. Manual therapy from a pediatrician's viewpoint 113

11. The influence of the high cervical region on the autonomic regulatory system in
infants 125

12. Attention deficit disorder and the upper cervical spine 133

13. Asymmetry of the posture, locomotion apparatus and dentition in children 145

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Birthing interventions and the
newborn cervical spine
D. Ritzmann

': li,I" I , i " , I


Introduction 75
Why shoul d an obstetrician write a chapter in a
Short history of European obstetrical research
book about manual therapy? As we know today,
and inventions 76
problems in newborn babies, children and adults
The gynecoid pelvis 77
can have their roots in pregnancy and birth, and
the risk of damage to the newborn brain durin g
The android pelvis 77
birth has been the ta rget of research for many
The anthropoid pelvis 77
The platypeloid pelvis 77
years. Amongst manual therap ists and obstetri ­
cians, pat holo gis ts and neurologists there is now
Research about the function of the
growing interest in th e newborn cervical spine
female pelvis 77
and its possible damage during birth.
Risky situations during birth 78
This introductory section outlines different
Arrested parturition 78
vie ws on childbirth; the next two sections describe
Extremely rapid delivery 78
the development of obstetric research and inven­
Breech delivery 79
The delivery of children with deflected
tionsin Europ e and the research on the function of
heads 79
the p el vis during birth. This is followed by an
explanation of r isky situations and in terventions
Risky interventions during birth 79
Pressure from above 79
during birth. T he final section looks at the special
Traction from beneath 79
anatomical and physiological situation of the
newborn head and spine and the possible damage
Rotatory forces 80
to these structures during birth.
The dangers for the newborn cervical spine 80
Pressure forces 80
To give birth and to go through birth is a funda­
Traction forces 81
mental experience for both mother and child. We
know today that successful childbirth depends on
Rotatory forces 81
other factors as well as the a n a tomy of the pelvis,
Conclusion 82
the diamete rs of the child's head and the power
and timin g of the contractions. For more than a
hundred years, researchers have been working on
the function of the pelvis during birth, the move­
ments of the j oints, the stretching of the ligaments

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and the interdependent changes in the move­ obstetricians entered this field which until then
ments of the mother and the unborn child. More had been the domain of 'wise women' (the French
recently, researchers have also been looking at the term for midwife 'sage-femme' - 'wise woman'
psychological dimensions of giving birth and of literally translated - reflects this). New instru­
being born. We are learning more and more about ments were invented and introduced. At the end
this subtle teamwork between mother and unborn of the seventeenth century, two members of the
child, especially how to empower and how not to English family Chamberlen (Hugh and Paul)
disturb it. spoke of an instrument that would enable every
There are many different views on giving birth. woman to give birth to a living child, but there is
Some of the most important are the following three: no picture of this instrument. In 1721 the
renowned Belgian surgeon Johannes P. Palfijn
• Giving birth and being born is fundamentally a
(1650-1730) showed a new instrument, which was
mechanical problem between the pelvis of the
called 'the iron hands of Palfijn'. It was the first
mother and the head or breech of the child (tra­
known and depicted obstetric forceps.
ditionally European).
During the eighteenth century there was a
• Giving birth and being born is fundamentally a
growing interest in the medical community in
p rob le m of rhythm and of disturbances of
learning more about the female pelvis during
rhytlun (traditionally shamanistic approach).
birth. William Smellie (1697-1763) wrote in 1754
• Giving birth and being born is fundamentally a
about the possibility of learning more about the
problem of not being disturbed (new and very
inner pelvis by touching during birth. He
old views of Christian belief).
described how it was possible to turn the child's
Because this chapter is concerned with birthing head with gentle pressure during birth. He also
interventions and their effects on the newborn cer­ postulated that the unborn child usually enters
vical spine, we will concentrate on the traditional the pelvis transversally, the only person to do so
Western view of mechanics . All the same we for about 150 years. This fact was not accepted
should not forget that in practical obstetrics the until the beginning of the tvventieth century, when
rhythm and the absence of disturbances is much Christian Kielland (1871-1941) came to the same
more important. Gradually this finding has led to conclusion (Parry Jones 1952). His instrument, the
the now more widely held view that there is no Kielland forceps, is still used today.
sense in measuring the outer pelvis with a In 1934 Dr Eugene W. Caldwell (1870-1918),
pelvimeter, or the inner pelvis using hands, X-ray professor of radiology in New York, used X-rays to
or MRI (magnetic resonance imaging) to assess the prove that Smellie and Kielland were correct. Dur­
prospects for giving birth. It is only in the situation ing the nineteenth century, especially in France, a

of a breech presentation that cliin cs number of obstetricians tried to construct better

or MRI of the pelvis to help in planning the birth. forceps to obtain the best traction direction. There
was much sophisticated work in this field. But the
same famous men did not accept the minimal
SHORT HISTORY OF EUROPEAN hygienic standards proposed by Dr Ignaz Semmel­
OBSTETRICAL RESEARCH AND weis, the famous trailblazer for hygiene in surgical
INVENTIONS wards, nor did the high mortality of mother and
child in connection with interventions lead them to
In Europe, a change occurred in obstetric practice be careful in promoting their use.
during the sixteenth and seventeenth centuries. As pathology and radiology developed, the
Alongside a decline in female knowledge as a female pelvis became a target of research. Four
result of politics and church prosecution, male types of female pelvic forms have been described

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Birthing i nt er v en t i on s and the newborn cervical spine 77

since the nineteenth century, and were classified narrow in the sagitt al diameter. It is found in vary­
in 1934 by Caldwell and Moloy: the gynecoid ing frequencies from 1 to 56% (note, again, the
type, the android type, the plat ypeloid type and wide range of reported incidences). Often the
the anthropoid type. This classi fic ation of female baby's he ad cannot enter the pelvis, as the radi ­
pelvic types is still used today. ographic analysis might sugge st . If it c an enter, it
lies in the o bli que diamete r.
The gynecoid pelvis Research on the different forms of female pelvis
decreased as cesarean sections became more fre­
This is the t ypical transversally l arge inlet. The quent. Some special pelvic forms have been
b aby 's head enters the pelvis in the transverse thought to be associated with special risks during
position. In obstetric books, it is considered the birth, for example the so-called long pelvis
most usual female pel vis. Nevertheless Borell and described by Kirchhoff. Later srudies showed that
Fernstr om found it in onl y 25-30% of a northern these pel vic fo rms are frequent in normal births as
European popula tion du rin g birth. We can see well, so the postulated risk is not proven (Borell
here the t ypical way of e ntering the pelvis trans­ and Fernstrom 1957) With the reduction in rickets
versally in Homo sapiens sapiens. It seems that for 4 and poliomyelitis in Europe, the pelvis is very sel­
million years starting with Australopithecus the dom a problem for birth.
pelvis has been get ting a transversal l y larger inlet
in females. With this usual birth position at the
pelvic inlet the unborn baby has to rum 90 degrees RESEARCH ABOUT THE FUNCTION OF THE
with head, shoulders and rump. This sc rewing FEMALE PELVIS
movement is typical for hu man birth. In four­
footed animals the pelvis is s tr ai ght and no screw­ At the end of the nineteenth cenrury, researchers
ing movement is necessary. started to describe the function of the pelvis, and
were p artic ularly interested in the joints and liga­
The android pelvis ments. Walcher (1889) and von Kiittner (1898)
described a s agittal opening of the pelvis of about
This is the typical male pelvis. Borell and Fern­ 8 to 12 mm through stretching and bending of the
strom found it in about 10-20% of women during hips of dead mothers (Borell and Fernstrom 1981).
birth. The b a by ' s head enters the pelvis in the The y concluded that the sacroiliac joints allow this
oblique di a meter. opening. Du ring pregnancy there is a relaxation of
the sacroiliac joints which can lead to recurrent
The anthropoid pelvis blockages of these joints with p a i nful conse­
quences. To study these joint movements d urin g
Anthropoid relates to the primates who have this birth is nowadays n e ar ly impossible. From
typic a l large sagi tt a l inlet of the pelvis. Rad iolo gi­ manip ulations during birth to get blocked sacroil­
cally it is found in between 5 and 73%, the wide iac joints back to their normal function we can
range indicating the clashes of opi n ion on how to assume that the movement in the sacroiliac joints
de fine it. The baby's head enters the pelvi s in the is important for a norm al birth. In h uman birth, all
sa gittal diameter. the space between the pelvis and head of the baby
is needed. When a joint cannot move smoothly the
The platypeloid pelvis birth can be distur bed.
The relaxation of the pelvic li gaments and
This is the typical flat pelvis, found in women joints is triggered by the hormone relaxin. This
with rickets. It has a gynecoid form, but is very hormone also has an influence on the ripening of

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the cervix and on the connective tissue in vessels Risky situations are:
and the skin (Sherwood 1994). Radiological
• arrested parturition
examinations in the middle of the twentieth cen­
• extremely rapid delivery
tury demonstrated a relaxation of the sacroiliac
• breech delivery
joints of some millimeters and a relaxation of the
• delivery of children with deflected heads.
symphysal joint from about 4 mm to usually 8
mm at the end of pregnancy (Borell and Fern­
Arrested parturition
strom 1981). This is reversible 3 to 5 months after
Arrested parturition is a very frequent situation,
The movements of the pelvis during birth are
especially in obstetric clinics. Often it leads to inter­
described by Borell and Fernstrom: when the
ventions such as hormone injections to accelerate
baby's head enters the pelvis, the symphysal joint
the frequency of contractions or to instrumental or
descends. In mid pelvis the symphysal joint
cesarean deliveries. Different underlying problems
moves cranially and at the pelvic outlet even
can lead to an arrest , but often the cause is not clear.
more. This cranial movement can reach several
In this situation the obstetrician uses the term 'dis­
cen timeters.
proportion between pelvis and head'. More
To allow the pelvis to move in such a way dur­
research is needed in this field. Often it is not clear
ing birth it is essential that the mother is as undis­
why the contraction forces vanish, why the unborn
turbed as possible. It seems that the Indian way of
baby does not enter deeper into the pelvis or why a
birthing (described by Moyses Paciornik in 1985)
normal birth turns suddenly into an arrest.
in the squatting position reduces the necessity for
Could factors such as changes in staff, lack of inti­
interventions to a minimum. Paciornik reports a
macy, or ongoing disruption of this very intimate
frequency of under 5% for forceps delivery. In the
process of giving birth due to the technical controls
squatting position the pelvis is 'freely hanging'. It
and the emotionally uninvolved staff be the cause of
is logical that the joint movements can work
the immense problem of disturbed births?
undisturbed in this pOSition.
There is always an underlying problem that
The movement of the pelvis during birth seems
leads to an arrest of birth. This could be a mater­
to be related to the posture of the mother and to
nal problem such as:
the tightness of the muscles, which are influenced
by fear and psychological tension. This would • weak labor (exhausted mothers, mothers in fear
explain why it is important to give support or grief, disturbed mothers)
throughout birth so that the level of operative • uncoordinated labor pains (induced births,
interventions is kept to a minimum. preterm births, pain and fear)
• anatomical problems of the pelvis (seldom).

Arrested birth can also be due to a problem con­

cerning the unborn baby sllch as:

To give birth and to go through birth is a funda­ • transverse or breech presentation

mental experience for both mother and child. • dorsoposterior presentation
There are situations that by themselves are risky • a deflected head.
for mother and child or are followed by risky
maneuvers by the obstetricians or midwives. We Extremely rapid delivery
now take a closer look at the impact of these
situations and interventions, especially for the Extremely rapid delivery can cause problems to
newborn cervical spine. the baby because of the immense power the con-

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Birthing interventions and the newborn cervical spine 79

tractions exert on the baby's head and neck. The RISKY INTERVENTIONS DURING BIRTH
baby can rush through the pelvis, pushed by con­
tinuous contractions. A certain percentage of babies All interventions during birth are risky, if not
with problems related to the cervical spine have done carefully and with respect for the special
this birth history. situation of the mother and the unborn child.
Risky interventions are the following:
Breech delivery
• pressure from above
• traction from beneath
Breech deliveries are special deliveries. Even in
• all rotatory forces.
communities far away from modern obstetrics (as
e.g. in the country side of Nepal) women do not
give birth alone with mother and husband if there Pressure from above
is a breech delivery. A midwife will be present at
birth in this situation. Pressure from above can increase in fast deliveries,
The risk of a higher morbidity and mortality but also through all kinds of interventions in
relates not only to the baby but also to the mother, arrested births. These interventions can be the
especially in poorer countries where no antibiotics traditionally exerted external direct forces by
or instrumental interventions are available. Breech means of cords and bags, in Western obstetrics the
deliveries are often more protracted than vertex so-called 'Kristeller fundal pressure'. Initially
deliveries and have a higher risk of arrest and Samuel Kristeller (1820-1900) proposed a soft
damage to the baby. pressure by hand, nowaday s it is most often a very
Interestingly, Leonardo da Vinci drew only dead powerful pressure. In the original publication, this
mothers with unborn babies in breech presentation maneuver was advocated as an aid for multiparae
because he had to base his anatomical research on where the abdominal muscles were atrophied and
autopsies of mothers who died during childbirth. thus not functioning normally any more. The most
frequently used augmentation of contraction
The delivery of children with forces nowadays is labor-inducing medication.
deflected heads
Traction from beneath
Unborn babies with deflected heads usually lie in
the dorsoposterior vertex presentation. The dorso­ Traction from beneath has a long history: Before
posterior presentation describes an unborn baby 1700 there had been nets and strings to get the
with its spine turned towards the mother's spine. child from beneath. In the early eighteenth cen­
In this position the head is often deflected and is tury the newly invented obstetric forceps some­
less able to bend during parturition. Quite often times replaced these older traction forces. In 1954
the birth takes much longer than usual or is even­ Tage G. Malmstrom proposed a new traction
tually arrested. In this unfavorable situation the instrument, the vacuum extractor. This instrument
labor forces cause more stress to the unborn baby is now replacing the obstetric forcipes.
and the risk of injury increases. Frequently it is At the begirming of the twentieth century,
necessary to deliver the baby by forceps, so the Hermann
risks of this intervention augment the overall risk John Martin Munro Kerr (1868--1960) invented
of the deflected head. Babies in breech presenta­ new surgical techniques to make cesarean sections
tion with deflected heads have a very high risk of safer. At the end of the same century, Michael
morbidity. Nowadays this is an indication for a Stark proposed a shorter and less traumatic surgi­
cesarean delivery. cal option, the so-called 'soft cesarean'.

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All these different interventions have their par­ THE DANGERS FOR THE NEWBORN
ticular risks to the newborn spine and head, even CERVICAL SPINE
the cesarean section. Problems with the newborn
spine can result from a long birthing process which We can differentiate between pressure forces, trac­
in the end is terminated by an instrumental deliv­ tion forces and bending forces. These different
ery or a cesarean section, but there are also some­ types of forces have different effects on the new­
times problems if the baby has been delivered by a born cervical spine and head.
planned cesarean section. Often to get the baby out
of the uterus the incision needs quite a powerful Pressure forces
pressure from above. So even this intervention can
be harmful to the baby. It would be best to prevent During normal birth the unborn baby is protected
all types of interventions, but here we need more from direct forces by the amniotic fluid. The fluid
research. causes a distribution of the uterine muscle forces.
With the opening of the amniotic cavity, by itself
Rotatory forces or by intervention, the forces exerted on the baby
lead to a direct pressure on head and neck in the
Rotatory forces are now seldom exerted. If the vertex presentation. If the baby is turning cor­
head of the unborn baby does not turn in the best rectly through the pelvis, it will not get stuck and
position and stays in the wrong diameter, it may will move slowly downwards. If there is an arrest
be possible to turn the head by hand as Smellie in labor, the contraction forces will press the spine
proposed in the seventeenth century or by Kiel­ against the suboccipital region.
land forceps as proposed in the early twentieth These pressure forces, whether due to strong
century, but this must be done without force. If contractions, manual pressure (Kristeller), or hor­
any force is exerted on the head, the cervical monal augmentation of the natural contractions,
spine can be injured and the result can be delete­ can occasionally lead to a subluxation of the atlas
rious. Rotatory interventions are difficult and into the foramen magnum with disruption of the
dangerous. cerebellum. The atlas of the neonate is much
Today the distribution of modern techniques smaller in relation to the foramen magnum than in
depends more on politics and tradition than on adults. With pressure, it can protrude into the
medical reasoning. The cesarean section rate foramen magnum.
varies from under 6% in Italy to over 50% in Axial pressure is the force usually encountered
Brazil; it also varies from region to region and in a normal birth. The neonate's anatomy and bio­
from hospital to hospital. The vaginal interven­ mechanics correspond to the special requirements
tion rate is 1-2% in Italy but more than 15% in of birth. The cervical spine has horizontal joint
Switzerland. T here are countries with low inter­ facets, enabling better adaptation to bending
vention rates and others with higher rates but forces; the small processi uncinati do not hinder
with similar newborn morbidity or mortality the compensating movements of the vertebrae
rates. during birth. The center of rotation of the cervical
There has been an overall lowering of newborn spine in sagittal movements is the high cervi­
mortality and morbidity in the last century, but cal regionC2-C4, not the deeper one as in adults -
independently of the frequency of instrumental CS-C6 (see Chapter 3). This situation allows the
interventions. It seems more connected to the unborn baby to hold the neck quite stretched with
health situation of women in rich Western a flexed head. On the other hand, the region C2-C4
countries. is more vulnerable to traction and rotatory forces

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Birthing interventions and the newborn cervical spine 81

in the newborn baby. if the head is in an extremely the spinal cord can only withstand 0.7 cm exten­
flexed position (as in dorsoposterior flexed vertex sion before it ruptures. It is about 100 years since
presentation) the high cervical region is under we saw fractured vertebrae during childbirth, but
massive pressure (Sacher 2002; see also Chapter 8). spinal cord damage is nonetheless possible. A
If other forces than axial pressure are exerted description of spinal cord injuries without radi­
during birth - e.g. rotatory or traction forces - the ographic abnormality in children has been pub­
weak ligaments cannot prevent the spinal cord, lished by Osenbach and Menezes (1989).
the vessels and nerves from being damaged. The
ligament of the dens axis is weak and cannot pro­ Rotatory forces
tect the brainstem from extension.
The special anatomy of the newborn cannot pro­
Traction forces tect the spinal cord, the vessels and nerves from
rotatory forces. These are the most dangerous
Traction forces during birth.can lead to damage to manipulations
the spinal cord, the spinal nerves, the vessels of The horizontal joint facets of the cervical verte­
the cervical spine and the brain. Often no damage brae allow more movement possibilities during
to the osseous structures is seen on radiography, birth, but are not adapted at all to rotatory move­
but there is extensive damage to the soft tissue of ments. The interconnected nerves and vessels in
the spinal cord, the nerves, vessels or even the the cervical spine and the weak ligaments can lead
brain. Modern techniques of MRl or PET can to a disruption or stretching of these structures.
reveal these lesions more precisely. The arteriae basilares are especially at risk from
The arteriae cerebri mediae and the sinusoidal rotatory forces. If stretched or ruptured, subdural
veins are at special risk under traction forces. They and intracerebral bleeding can result .
can rupture and cause intracerebral and subdural As different structures may be involved in
bleeding. If this happens, they can bleed profusely cervical spine injury and brains tern damage,
or create adhesions, which can squeeze the spinal the symptoms vary in signs and extent. The main
cord. symptoms of intracerebral bleeding are early
What extent of traction power is exerted on the death, breathing depression and epileptic cramps.
newborn cervical spine? Nowadays ultrasound of the brain allows early
Few physicians since Samuel Kristeller have diagnosis.
investigated this question. Kristeller, in 1861, The leading symptom complex of spinal cord
measured an average traction power of 15.9 kg by injuries is the so-called 'spinal shock'. Early symp­
forceps. A hundred years later Laufe (1969) toms can be early neonatal death, respiratory
reported an average of 7.7 to a maximum of 19 kg depression, gasping and hypotonic muscles. Late
by forceps. Interestingly in 1990 Justus Hofmeyr symptoms can be spasticity, paraplegia and an
reported exactly the same traction force by the atonic bladder. Injuries of the upper cervical spine
metal suction cap of the vacuum extractor as can also lead to gastrointestinal kinetic problems
Samuel Kristeller: 15.8 kg (Hofmeyr et al 1990). such as spasms of the pylorus, gastroesophageal
The weaker silicon suction cap exerted a some­ back flow and hypotonic jejunum. A possible effect
what smaller power. can be relapsing pneumonia, a symptom that can
In 1874 Duncan examined the spines of new­ lead to the diagnosiS of high cervical injury (see
born dead babies and reported the following data: Chapter 8).
the vertebral spine of a newborn dead child can If the spinal nerves are stretched or rup­
suffer an extension of 5.6 cm before it breaks, but tmed, paralysis of the plexus brachialis (cervical

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plexopathy) can result, very often combined with breech presentations, twins, arrested births and
torticollis on the same side (Suzuki et al 1984). deflected heads during birth (Buchmann and
They are the main symptoms of damage in the BUlow 1983, Seifert 1975, Biedermann 1999).
upper cervical spine. This can be the more fre­
quent Erb-Duchenne upper plexopathy with
injuries to neural structures CS/C6 or the less fre­ CON CLUSION
quent Klumpke caudal plexopathy with injuries
to spinal nerves C7/T1, sometimes combined with We begin to understand how vulnerable the
a Horner syndrome. structure of the newborn cervical spine is. Further
The real incidence of damage to the upper cer­ insight into this complex problem will surely
vical spine and brainstem structures is not known. influence the way we regard birthing. Giving birth
Some authors have published data on the fre­ under water or in a squatting position, for exam­
quency of missed diagnosis in child neurology ple, alters the stress exerted on the cervical spine.
a nd pathology, which are quite high (10% to over Not to disturb the rhythm and the intimacy of giv­
50%) (Towbin 1964, Rossitch and Oakes 1992). ing birth is an important issue in reducing the
Studies of newborn babies that had a special inter­ incidence of arrested births and therefore the risk
est in high cervical function revealed a high fre­ of damage to the newborn. These are just two of
quency (about 30%) of functional impai rment . many areas where the work of obstetricians inter­
This seems to be connected with traction forces sects with the work of those engaged in manual
and special risks as mentioned above such as therapy.


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Birthing interventions and the newborn cervical spine 83

Further reading

Achanna S et al 1994 Outcome of forceps delivery versus GlazenerC M A et al 1995 Postnatal maternal morbidity:
vacuum extraction. Singapore Medical Journal extent, causes, prevention and treatment. British Journal
35:605-608 of Obstetrics and Gynaecology102:282-287
Annibale D J et al1995 Comparative neonatal morbidity of Govaert P et al1992 Vacuum extraction, bone injury and
abdominal and vaginal deliveries after uncomplicated neonatal subgaleal b leeding . European journal of
pregnancies. Archives of Pediatric and Adolescent Pediatrics151:532-535
Medicine 149:862-867 Govaert P et a11992 Traumatic neonatal intracranial
Avrahami E et al1993 CT demonstration of intracranjal bl eeding and stroke. Archives of Disease in Childhood
haemorrhage in term newborn following vacuum 67:840-845
extractor delivery. Neuroradiology35:107-108 Gra ig W S1983 Intracranial hemorrhage in the newborn.
Bhagwanani S G et a l 1 973 Risks and prevention of cervical A study of diagnosis and differential diagnosis based
cord injury in the management of breech presentation upon pathological and cLirucal findings in 126 cases.
with hyperextension of the fetal head. American Journal Archives of Disease in Childhood13 :89-123
of Obstetrics and Gynecol ogy 115(8):1159-1161 Greis J Bet al1981 Comparison of maternal and fetal effects
Biedermann H. 1993 Das KlSS-Syndrom der Neugeborenen of vacuum extraction with forceps or caesarean
und K1einkinder. Manuelle Medizin31:97-107 deliveries. Obstetrics and Gynecology57:571-577
Bjerre I et al1974 The long term development of child ren Hibbard B M et al1990 The obstetric forceps- are we using
delivered by vacuum extraction. Developmental the appropriate tools? British Journal of Obstetrics and
Medicine andChild Neurology16:378 Gy naecology97:374-380
Bresnan M Jet al1974 Neonatal spinal cord transection HillierC EM et al1994 Worldwide survey of assisted
secondary to intrauterine hyperextension of the neck in vaginal delivery. International Journal of Gynecology
breech presentation. Journal of Pediatrics84(5):734-737 and Obstetrics47:109-114
Brey J et al 1956 Vacuum extractor with special reference to Jensen T S et al 1988 Perinatal risk factors and first year
earl y and late infantile injuries. Gebhilfe und vocalizations: influence on preschool language and
Frauenheilkunde 22:550 motor performance. Developmental M edicine andChild
Buchmann J et al 1992 Asymmetrien in der Neurology30:153-161
Kopfgelenkbeweglichkeit von Kindem. Manuelle Johanson R et al1989 North Staffordshire/Wigan assisted
Medizin30 9
: 3-95 delivery trial. British Journal of Obstetrics and
Cardozo L D et al1983 Should we abandon Kielland's Gynaecology96:537-544
forceps? British Medical Journal287:315-317 Johanson Ret al1993 A randomjsed prospective study
Carmody F et al 1986 Follow-up of babies delivered in a comparing the new vacuum extractor policy with forceps
randomised comparison of vaculun extraction and delivery. British Journal of Obstetrics and Gynaecology
forceps delivery. Acta Obstetrica Gynecologica 100:524-530
Scandinavic� 65:763-766 Johanson R et al1999 Maternal and child health after
Chalmers j A 1989 Commentaries(The obstetric vacuum assisted vaginal delivery:
extractor is the instrument of first choice for operative randomised controlled study comparing forceps and
vaginal delivery). British Journal of Obstetrics and ventouse. British Journal of Obstetrics and Gynaecology
Gynaecology 96:505-509 106:544-549
Chiswick M L 1979 KieUand's forceps association with Johnson N et al1995 Variation in caesarean and
neonatal morbidity and mo rtality. British Medical instrumental delivery rates in New Zealand hospitals.
joumal i7
: -9 Australia and New Zealand Journal of Obstetrics and
Dell DL et al1985 Soft cup vacuum extraction: a comparison Gynaecology35:6--11
of outlet delivery. Obstetrics and Gynecology 66:624-628 Lasbrey A H et a11964 A study of the relative merits and
Drife j 0 1996 Commentaries(Choice and instrumental scope for vacuum extraction as opposed to forceps
delivery). British Journal of Obstetrics and Gynaecology delivery. South African Journal of Obstetrics and
103:608-611 Gynaecology 2:1-3
FaU 0 et al1986 Forceps or vacuum extraction? Acta Lasker M R et al1991 Neonatal diagnosis of spinal cord
Obstetrica Gyn ecol ogica Scandinavica65:75-80 transsection. Clirucal Pediatrics30(5 ):322-324
Gachiri J Ret al Fa'till and maternal outcome of vacuum Leijon 11980 Neurology and behaviour of newborn infants
extraction. East Africa Medical Journal1991; 68:539-546 delivered by vacuum extraction on maternal indication.
Garcia J et al 1985 Views of women and their medical and Acta Paediatrica Scandinavica69 :625-631
midwifery attendants about instrumental delivery. Ludwig B et al 1980 PostpartumCT examination of the head
Journal of Psychosomatic Obstetetrics and Gynaecology of full term infants. Neuroradiology20:145-154
4:1-9 MacArthurC et al1991 Commentaries(Health after
GiUes F H et al1979 Infantile atlantoccipital instability. Childbirth) British Journal of Obstetrics and
American Journal of Diseases ofChildren 133:30-37 Gynaecology98:1193-1195

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84 C L I N I CA L I N S I G H T S

MacA rthur C et a l 1997 Faecal incon tinence a f te r chi l db i r th . Pu sey J et a l 1991 Ma terna l im p r es s i o n s of fo rceps and
Bri tish J o u rn a l ofObstetrics and G yn a e co logy 104:46-50 s i l c - cup . British J o u rn a l o f Obs te tri cs and G ynaecology
MacK innon J A et a l 1 993 Sp ina l co rd inj u ry at birth : 98:4887-4888
d ia gn o sti c a n d p r o g nos tic d a ta in tw e n ty-two patients. Ru gg ie ri M et a l 1999 Spin a l cord i n s u l ts in the p rena tal,
J o u rnal of Pediatrics 122(3):431-437 p e r ina ta l a nd neonatal periods. Dev e l o p m en ta l M ed i cine
M a r tyn C 1 996 Not q u i te as r a nd o m as I p re t end ed . Lancet and Chi ld N eu ro l og y 4 1 : 3 1 1-3 1 7
3347:70 Shah P M 1991 Prevention o f menta.! handicaps in c hi l d ren
Meniru G I e t al 1 996 An a n a ly s i s of rec ent trends in in prim a ry h e a l th ca re. WHO B u l letin OMS 69:
v a c uu m ex trac tion and forceps delivery in t he U n i ted 779-789
Kin g d om . Bri t i sh J o u r n a l of Obs te t r i c s an d G yna e colo g y Simon L e t a l 1 999 Letters to the E d i to r ( C l in ical and
1 03 : 1 68-1 70 r a d i ol og i ca l d i agnosis of the s pi na l cord b i r th inj u r y ) .
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in n e o n a tes d e l ivered w i th fo rc e ps : report o f 15 c a ses . Edition 81:F235-236
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infa n ts d e li v e red by a Sw e d is h ventouse. Rev 329 : 1 905-1 9 1 1
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M i d d le C et al 1995 La b o ur a nd delivery of n orm a l a r tery at the a tlantoa xial j oi n t : is i t truly p h ys i olog i c a l ?
p r i mi p a ro u s w om e n . B r i tis h J o u r n a l of Obs tetrics and N e u rorad io logy 36:273-275
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M oo l goa k e r A A 1979 Compa rison of d i ffe re n t methods of the n e c k a n d in tr a u te rine d i sloca tion of ce r v i ca l
i nstru mental d el iv e r y ba sed on e l ec tro nic m e a s ure me n ts v ertebrae. America n J o u rn a l of Obstetrics a nd
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Chapter 8 ------�------�----�------------�---- �

Birth trauma and its implications

for neuromotor development
R. Sacher

We begin by outlining the risks to the infant cervi­

CHAPTER CONTENTS cal spine as a result of birth trauma from the gyne­
cological point of view, and then proceed to
The infant cervical spine 85
examine aspects of manual therapy
Anatomical aspects 85
When considering injuries and dysfunctions of
Biomechanical aspects 87
the spine and its associated structures, the signifi­
'Classical' injuries to the (cervical) spine from
cance of birth trauma is often underestimated, and
birth trauma 87
the resulting symptoms frequently misinter­
Frequency of occurrence 87
preted. The consequences of trauma to the baby
Mode of delivery 88
during birth and in the months immediately pre­
Additional risk factors 88
ceding and following the birth are thus of concern
The clinical picture 89
not only to gynecologists and pediatricians, but
Diagnosis and differential diagnosis . 89
also to practitioners of manual therapy in a wide
Functional biomechanical disorders of the
range of specialties, who have begun to study the
upper cervical spine 90
risks associated with pregnancy and delivery
Craniocervical blockages in newborn and
The aspects to be considered therefore include
infants 91
not only the specific stresses on the infant spine
The craniocervical transition zone in
associated with pregnancy and birth, its particular
embryology and developmental
anatomical and biomechanical features, and the
anatomy 91
neurophysiological mechanisms of the cervical
Neurophysiological aspects of upper
region, but also such matters as developmental
cervical dysfunctions 92
Clinical investigations 92
Spontaneous birth 92
Extraction aids 93
Cesarean section 93
Additional risk factors 93
Anatomical aspects
Conclusion 95
Implications for practice 96
The spine of the fetus and yOlmg child has a num­
ber of special biomechanical and anatomical fea­
tures to enable it to adapt to the physiological

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demands of the birth process. It is largely carti­ condyles in the newborn and in early infancy is
laginous. The size and weight of the head after about 50% of the adult measurement, and the
birth result in an increased inertia load on the axial angle of the atlanto-occipital joint (Fig. 8.1) is
upper cervical spine (Baily 1952, Fielding 1984, consequently considerably flatter than in adults
Papavasilou 1978, Townsend and Rowe 1952). But (1530 versus 1240 in men and 127" in women)
during birth, too, the large head inevitably means (Sacher in press, Schmidt and Fischer 1960). The
an increase in the leverage exerted on the cranio­ angle formed by the axis of the atlanto-occipital
cervical transition zone and in the demands joint with the sagittal plane (the average orienta­
placed on it, which may involve rotation, anteflex­ tion) is markedly more obtuse (Fig. 8.2) (Lang
ion and retroflexion (cephalic presentation of 1979).
occiput or face).
The horizontal orientation of the joint surfaces
in the frontal plane, especially in the upper cervi­
cal region, allows greater translational mobility
(CateU and Filtzer 1965, Melzak 1969, Papavasilou
1978). In the sagittal plane, however, the joint sur­
faces - in terms of the individual vertebrae - in the
newborn are more steeply aligned than in the
young child, resulting in a more inclined position­
ing of the cervical spine (von Kortzfleisch 1993).
Meanwhile, the articulating surfaces of the verte­ Figure 8.1 Angle of condyloid joint axis CoIC1
bral bodies, and the jOints, are still relatively small
and so increase segmental instability. The wedge
shape of the vertebral bodies and the still incom­
pletely formed uncinate processes give greater
adaptability to the demands imposed by the

mechanics of the birth process, but these features, •

combined with the weak muscles and ligaments •

of the newborn, produce a greater tendency to
b ..
subluxation (Babyn et al 1988, Catell and Filtzer •

1965, Fielding 1984, Menezes 1987). The spinal •

cord structures and meninges are eight times as
vulnerable as the postural connective tissue struc­
tures, owing to a lack of elasticity during longitu­
dinal traction (Leventhal 1960), a force that is not
anticipated in the physiological features designed
to withstand the birth process. This may be one of
the reasons that many injuries of the spinal cord
from birth trauma produce radiographic studies
with no visible evidence of injury to the spinal col­
umn (spinal cord injury without radiographic

abnormality - ScrWORA (Osenbach and Menezes

1989». Figure 8.2 Atlanto-occipital axis in the sagittal plane;
The suboccipital region also has various special dotted lines show situation in the adult (a = 35Sl. black
morphological features; the height of the occipital in the newborn (b = 28').

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Birth trauma and its implications for neuromotor development 87

Biomechanical aspects

There are four main biomechanical features:

• on lateroflexion (frontal plane) the atlas does

not normally move into the concavity as it does
in adults, but into the convexity (Biedermann
• the infant cervical spine appears much more
extended in the sagittal piane (von Kortzfleisch
• the main pivot for movements in the sagittal
plane is not in theCS/C6 segment as in the
adult, but at C/C3/C4 (Catell and Filtzer 1965,
Hill et a11984, Nitecki and Moir 1994)
• paradoxical tipping of the atlas: anteflexion of
the head occurs only in the craniocervical joints
when nodding, accompanied by ventral sliding
Figure 8.3 Occipitoposterior presentation.
of the atlas (Biedermann 1999).

This biomechanical adaptation must have the pur­

There are also particular features associated
pose of providing protective mechanisms for the
with breech presentations, owing to the increased
associated nerve structures. The question as to
traction stresses on the spinal structures. Since the
whether such features are already effective in the
upper cervical spine mainly has to deal with the
newborn has been little investigated as yet. How­
biomechanical demands of the head position, it is
ever, the radiological findings of Ratner and
now the cervico-thoracic transition zone that has
Michailov (1992) suggest the existence of such a link.
to respond to the demands placed on it by the
The cranial shifting of the main pivot for move­
presenting parts of the fetal anatomy. Again the
ments in the sagittal plane enables optimum
decisive factor is the higher location of the rota­
transmission of forces during labor, exerted by the
tional axis for anteflexion and retroflexion. The
axially directed contractions on the head as it
spinal structures of the lower cervical spine and
moves downwards in cephalic presentations. This
the cervico-thoracic transition zone have only so
enables a much more extended positioning of the
much resilience, and the limits are soon reached.
lower cervical spine. Meanwhile, increased ante­
Additional traction or rotation will quickly
flexion at C2/C3 causes increased ventral tipping
exhaust the reserves of tension in this area. The
of the dens axis, which makes it necessary for the
most unfavorable situation is that of breech pres­
atlas to slide ventrally.
entation with hyperextension of the head.
The upper cervical spine has to absorb directly the
adaptations in head position brought about by the
dynamics of the birth process and at the same time 'CLASSICAL' INJURIES TO THE (CERVICAL)
to transmit the major part of the expulsion forces to SPINE FROM BIRTH TRAUMA
the head. The direction producing the greatest tissue
tension of the cervical spine is anteflexion of the Frequency of occurrence
head, while retroflexion produces the least. The upper
cervical spine is therefore subjected to particular The incidence of injuries to the spinal column and
stress in the occipitoposterior presentation (Fig. 8.3). spinal cord from birth tr auma is still not fully

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known. One reason for this may be the clinical pic­ cance of damage to the thoracolumbar spinal cord.
ture, as the diagnosis is not always easy (Men­ Over 55% of the children in their patient cohort
ticoglou 1995). Rossitch and Oakes (1992) have developed inj u ri es to the spinal cord in the tho­
documented how rarely trauma to the structures racic and lumbar regions of the spine. This, how­
of the spinal column is considered. They report ever, included children who had undergone
false diagnoses (including pediatric neurology) in catheteriza tion of the umbilical artery that could
four out of five cases where there was severe have caused damage to the spinal cord by throm­
injur y to the spinal cord. The fact that the struc­ boembohsm.
tures of the spinal cord are also not routinely Injuries to spinal structures at the lower cervi­
included in autopsy is equally surprising (Ratner cal or upper dorsal levels are more frequently
1991b , Towbin 1969). Towbin (1970), in an autopsy found in breech deliveries (Bresnan and Abroms
study on this question (N = 600), found relevant 1973, Caterini et al 1975, MacKinnon et al 1993).
injuries to the spinal cord and brainstem in 10% of The hyperextension of the fetal head plays a par­
cases. These consisted of spinal epidural hemor­ ticular role in these injuries, and is seen in about
rhages, meningeal tears and injuries to blood ves­ 5% of all breech deliveries. Up to 25% of these
sels, the muscles and ligaments, and the nerve and vaginally delivered babies developed spinal cord
bone structures. injuries (Bhgwanani et al 1973, Bresnan and
Damage of this sort can also be observed in Abroms 1973, Caterini et al 1975). E ven when the
normal births, where it is hardly expected to child was delivered by cesarean section, a small
occur (Ratner 1991b). There is considerable varia­ proportion suffered serious complications at the
tion in the pattern of clinical symptoms on upper cervical level (Cattamanchi et al 1981,
account of the vascularization in the region of the Maekawa et a11976, Weinstein et aI1983). In these
vertebral artery, and for this reason it is easily cases it remains to be shown how far intrauterine
overlooked. injuries res ult ing from subluxation an d disloca­
tion in the upper cervical region could have
Mode of delivery caused blood vessel damage to the vertebral arter­
ies (Gilles et al 1979, Maekawa et al 1976, Wein­
The spinal column is subj ected to a variety of dif­ stein et aI1983).
ferent sh'esses by longitudinal traction or compres­ Forceps deliveries may involve an increased
sion of the spinal column and associated structures, risk of injury to the upper cervical spinal column
especially if combined with torsion, flexion and and spinal cord (Mackinnon et al 1993, Pschyrem­
hyperextension, depending on the mode of deliv­ bel 1966, Rossitch and Oakes 1992, Ruggieri et al
ery (Towbin 1964). It is not possible at the present 1999). The misapplication of these and similar
time to distinguish with certainty the role played extraction aids (forced traction/rotation; in the
by the 'normal stress' of the particular delivery worst case, rotation in the wrong dire ction ) can
mode and that of inadeq uate or inappropriate tech­ cause upper cervical complications.
ni que in assisting delivery. There is presumably a limit to iatrogenic struc­
Approximately 30% of the peripartum spinal tural damage caused by vacuum extraction, as the
column injuries described in t h e literature were vacuum device becomes dislodged if too much
observed in deliveries of cephalic presentations force is applied.
(Allen 1970 , Shulman et aI1971).
A major British/Irish study (Ruggieri et al Additional risk factors
1999) found no significant differences with regard
to mode of de liver y and the location of spinal col­ Further risk factors for spinal column and spinal
umn injuries. It also drew attention to the signifi - cord injuries occurring at or around the time of

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Birth trauma and its implications for neuromotor development 89

birth appear to be: intrauterine position, prema­ In their clin.ical and aruma I studies, Michailov
ture birth, precipitate delivery, multiple fetuses, and Aberkov (1989) found associated gastrointesti­
limb prolapse, shoulder dystocia, hypoxia, birth­ nal signs in cases of upper cervical birth traumas.
weight above 4000 g and postmaturity (De Souza Disruptions of vertebrobasilar circulation produce
and Davis 1974, Hasanov 1992, Menticoglou et al secondary spastic-hypotonic dyskinesia of the
1995, Ratner and Michailov 1992, Ruggieri et al small intestine, pylorospasm and g a stroesophag eal
1999, Towbin 1969). reflux. Michailov and Aberkov found swallowing
disorders, constant regurgitation and frequent
The clinical picture nausea as well as aspiration pneumonia. Where
there are recurr ing infections of the respiratory
The extent and location of the spinal cord injury system, the possibility of a spinal cord lesion
determine the clinical picture (Adams et al 1988, should therefore be considered. The same applies
Allen 1970, Babyn et a11988, Bresnan and Abroms to repeated infections of the urogenital tract.
1973, Mackinnon et a11993, Ratner and Michailov Significant lesions of the upper cervical spin a l
1992, Ratner 1 991a). Severe injury to the upper column and cord are associated with a high post­
cervical spinal cord is associated in particular with natal mortality (Babyn et a11988, MacKinnon et al
respiratory insufficiency, hypotonia, quadriplegia, 1993, Menticoglou et aI1995). Infants who survive
absence of pain reactions in the derma tomes this type of trauma of the spiml medulla develop
below the lesion, areflexia, and in certain cases related n eurol og ica l patterns over a period of
also insufficiency of the anal sphincter after months suggesting involvement of the first and
birth. Absence of the g r a sping , s uckin g and second motor neuron. The neurological diagnosis
corneal reflexes may indicate involvement of the indicates the segment involved.
brainstem. It is for example possible to diagnose conditions
Towbin (1964) points out that newborn babies involving the area of the trig e mina l nuclei (extend­
are not necessarily dependent on the presence and ing to C2/C3) and injuries to the upper brachial
function of the brain, s i n ce anencephalic infants plexus (Erb-Duchenne palsy) (Fig. 8.4), where the
can live for weeks and even months. The decisive Cs and C6 nerve roots are damaged, immediately
factor is the integrity of the upper cervically after birth. Lesions of the lower plexus (C7-T1)
located vital centers. (Klumpke's palsy) are rarer and sometimes occur
Brea thing dysfunction during the first 4 weeks together with lesions of the sympathetic nervous
of life is therefore seen as the cardinal symptom of system (Horner's syndrome - Fig 8.5). .

inju ries in this location. If segment C4 is involved, T horburn's pos ture represents a particular
paralysis of the phrenic nerve with raised form, in which a lesion of the lower cervical cord
diaphragm can occur. also leads to hypertonia of the interscapular mus­
Hypoxia following trauma in the cervico­ cles - or to bilateral abduction of the upper arm
occipital transition zone has been described in and weakness of elbow flexion (Renault and
other states as well as birth tr au m a. Around three­ Duprey 1989).
quarters of deaths following sh aking traumas
were caused by apnea (Coghlan 2001). (The Apgar Diagnosis and differential diagnosis
score to assess respiratory effort, heart rate, mus­
cle tone, response to stimulation, etc. in the deliv­ T he significance of spinal cord injuries for differ­
ery room is in essence a neurological assessment, ential diagnosis in peripartum asphyxias and the
primarily to test the irritability of or the presence development of cerebral paresis has been empha­
of inj u r ies to the brainstem and upper spinal cord sized by several authors (Clancy et al 1989, Mor­
(Towbin 1964).) gan and Newell 2001, Sladk y and Rorke 1986).

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Figure 8.4 Erb-Duchenne palsy (right hand side). Figure 8.5 Klumpke's palsy and Horner's syndrome
(from Bing 1953).

The pediatric neurological examination is useful FUNCTIONAL BIOMECHANICAL

across a wide range of conditions and the neuro­ DISORDERS OF THE UPPER CERVICAL
logical patterns observed can be identified with SPINE
increasing precision with the advancing age of the
child. Laboratory tests, muscle biopsies and elec­ The spine has a number of functions: support,
tromyography (Allen 1970, Lanska et a11990, Rug­ posture, perception, movement and protection.
gieri et al 1999) are mainly of use in differential This means that peripartum traumas to the sp i ne
diagnosis. may have either a direct effect, by destroying
Opinions are divided on the use of imaging skeletal structures, or an indirect effect by causing
procedures. Plain film X-rays, my elo gr a phy and secondary reactions in the spine.
computed tomography (CT) (Adams et al 1988), It must at least be concluded that pronounced
magnetic resonance i maging (MRl) and ultra­ hemorrhage (8abyn et al 1988, MacKinnon et al
sound are all used. Lanska et al (1990) emphasize 1993, Menticoglou et aI1995), atlanto-occipital dis­
the value of MRl, whereas Rossitch and Oakes locations (Adams et al 1988, Allen 1970, Men­
(1992) p oint to false negative results obtained by ticoglou et al 1995, Rossitch and Oakes 1992),
MRI. An ultrasound examination of the peri­ ruptures of the spinal cord (8abyn et a11988, Lan­
medullary structures should be carried out to pro­ ska et al 1990, Menticoglou et al 1995) and dislo­
vide additional information or as an alternative cated fractures of the spinal column (MacKinnon
(8 ab yn et al 1988, De Vries et al 1995, MacKinnon et al 1993, Menticoglou et a11995) will lead to local
et al 1993, Simon et aI1999). muscular reactions and in certain cases forced pos-

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Birth trauma and its implications for neuromotor development 91

tures. Although such neuro-orthopedic findings Biedermann (1999) was also able to demon­
have not been described, it is not clear whether strate a connection between birth traumas or
such symptoms were not present or simply not forced intrauterine positions and the occurrence of
recorded. Ratner (1991b) is the only author to reversible arthrogenous dysfunctions of the spine
report forced attitudes (torticollis) and paraverte­ in infants and the newborn in the course of his
bral muscular reactions in association with moder­ extensive investigations. Artificial means of
ate and mild lesions of the spinal column and cord. assisted delivery (forceps, vacuwn extraction),
We must also ask whether the special anatomi­ multiple pregnancies, breech presentations, pro­
cal and biomechanical characteristics of the infant longed expulsion period and transverse lie are
cervical spine with which we began might not, in particular risk factors.
combination with the problems of childbirth and
assisted delivery mentioned above, be capable of The craniocervical transition zone in
causing isolated injuries and/or dysfunctions of embryology and developmental
the spine. anatomy
Slate et al (1993), in a study of congenital mus­
cular torticollis, describe 12 cases with upper cer­ A brief look at the phylogeny of the craniocervi­
vical subluxations and negative neurological cal joints will help give an insight into their
findings. The authors traced these subluxations to nature.
problems of intrauterine position or birth trauma. Vertebrates evolved in water, and at that stage
However, no details were given of the timing of they possessed a comparatively unarticulated
the neurological examination. notochord or spine rigidly connected to the head
with no intervening joint. Head and body formed
Craniocervical blockages In newborn a single functional unit, and the control of func­
and infants tions such as orientation and balance was entirely
directed by the sense organs located in the head
Mechanical obstructions of the functioning of ver­ (Hassenstein 1970). As differentiation progressed
tebral joints, termed 'blockages', occur in all age and the joint connection between trunk and body
groups, with infants and the newborn being no developed, it became necessary to acquire propri­
exception. Among this group, injuries from birth oceptive information about the relative position of
trauma are most frequently discussed as the cause. head and body, and to integrate control mecha­
Seifert (1975) found 298 individuals with dys­ nisms. This task fell primarily to the craniocervical
functions in the craniocervical region among 1093 region, which includes the occipital condyles,
randomly selected newborn infants. A significant atlas, axis and the C2/C3 motor segment together
correlation with postural asymmetries was found. with its associated structures. In humans, the spe­
Buchmann and Bulow (1983) found upper cer­ cial place of the craniocervical transition zone is
vical dysfunctions in about one-third of newborn partly a consequence of embryonic development.
infants (N 683) studied. The incidence of cranio­
= Cells from the neural crests of this zone colonize
cervical blockages in those with forceps deliveries parts of the gastrointestinal tract, the primordial
was greater than can be accounted for by chance. heart, the urogenital tract (Wolff's duct), and the
Information on problems of intrauterine position thymus. A similar process underlies the develop­
or indications for cesarean delivery was not avail­ ment of the musculature of the tongue, pharynx,
able. This, together with the small number of larynx, esophagus and thoracic girdle (Christ et
cases, makes it difficult to draw even a cautious al 1988). Numerous special features are also
conclusion about the connection between the birth found in the neurophysiology of this region
process and dysfunction of the spinal col umn . (Abrahams et al 1990, Tayler and McCloskey

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1988, Traccis et al 1987, Wolff 1996, Zenker and CLINICAL INVESTIGATIONS

Neuhu bber 1994). In this context the exception­
al l y dense provision of muscle spindles in the A study involving 403 infants confirmed that the
suboccipital musculature and the close link with risk prof iles given above for the class i cal cervical
the sy mpat hetic trunk (superior cervical gan­ spine injuries caused by birth trauma are also
glion) and the tri gem inal nuclei (extending to responsible for causing craniocervical blockages
C2/C3) are relevant. of ear l y infancy i n s y mp tom a tic individuals
(Sacher 2003).
The details recorded included the route (vagi­
Neurophysiological aspects of upper nal/ cesarean section) and mode of d el iv ery (spon­
cervical dysfunctions taneous / assisted extraction; elective/ emergency
cesarean section), birthweight >4000 g, post-term
The spontaneous motor development that takes (>41 weeks) or premature birth (<37 weeks),
place in the first year of lif e involves tactile, pro­ abnorm al fetal position during pregnancy or
prioceptive and vestibular information, since birth, occipitoposterior cephalic presentation,
these typ e s of perception are directly connected short expulsion period, prolonged l abor (>24
with movement, as well as for ming the basis for hours), and use of Kristeller's maneuver.
establishing the ideal pattern of movement and
proprioception, and for subsequent differentia­ Spontaneous birth
tion, not only of the motor system but of the sen­
sory system, too. The afferent imp ulses of the Barely 30% of the infants with craniocervical
cervical receptor region are integrated into the blockages who fell into this category had no pre­
motor system for control of body support (Wolff viously suspected risk factors. Th ree infants in this
1996). For infants, including the newborn, these group had fractures of the clavicle as evidence of
tonic reflexes of position and support are pa rticu­ force affecting the fetus during birth, one in com ­
la rly impo rtan t (other aspects of perception being bination with Erb's palsy and one with cephalhe­
still immature). These reflexes are an expression of matoma. Two further infants had pronounced
the genetically programed motor repertoire on cephalhematomas. Spontaneous birth does there­
which individual learning is based. fore hold a potential for trauma that should not be
The neurophysiological system here, together underestimated, even when there are no other
with the immaturity of the sensorimotor system in known risk fac tors .

(early) infancy, means that craniocervical block­ Risk factors were found in more than two-thirds
ages in infants and the newborn have special of the spontaneous deliveries. The main risk factor
potency. There is an association with reactions of was the use of Kristeller's maneuver, which was
the afferent aspect of proprioception, in which the applied in more than half the deliveries in this cat­
im p airm e nt of receptive performance and the dif­ egory. This maneuver was origi nally designed to
ference in the flow of information to the receptors be used in multiparous women whose lax abdom­
from each side caused by the blockage must play inal wall (dia st as is recti abdominis) meant that
a part (as is the case in the labyrinths) (Hii lse et al they were no longer able to exert proper abdomi­
1998). Blockage also leads to the known nocicep­ nal muscular pressure. It is dangero us to apply it
tive, vegetative and myofascial reactions and to a uterus that is not in labor or where the abdom­
effects on joint mechanics. Predisposed infants inal wall is tensed hard (Rockenschaub 2001).
develop a set of symptoms that extends beyond The effect of Kriste ll er's maneuver is to increase
the local effects of craniocervical blockage, known the intra-abdominal expulsion pressure to such an
as KISS syndrome. extent that the presenting pa r t of the fetus is

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Birth traum a and its i m p l ications for neuro m otor d e v e l o pment 93

pushed out past any hindrances or resistance that cesarean section of 18-19% in Germany (Schiick­
may be present. In a normal birth with no extra­ ing 1999), an above-average number of infants
corporeal augmentation of pressure, the head delivered by cesarean section appeared in the
passes through the birth canal by means of slight study cohort. The large number of cases of abnor­
repetitive sideways inclination of the head which mal fetal position may account for this.
forces it gradually deeper - a physiological Another reason for the high proportion of
process known as asynclitism (Rockenschaub cesarean sections is the vulnerability of the upper
2001). If Kristeller's maneuver is applied, this cervical structures when traction tension is
gradual, force-reducing downward movement of applied. The physiology of the birth process does
the presenting fetal part will no longer happen, not allow for traction in the upper cervical area,
and the potential for trauma rises. and so the human fetus does not have adequate
High birthweight and short expulsion period protective mechanisms for this. However, every
were further risk factors frequently encountered. cesarean section involves considerable traction
Five infants suffered trauma consisting of lesions force on the spine and its associated structures,
of the upper brachial plexus as a consequence of regardless of whether the fetus is taken out by the
spontaneous delivery; two of these infants were head or the legs.
above normal birthweight, two were born after a The conclusion must be drawn that elective
short expulsion period, with shoulder dystocia in cesarean section seems to increase rather than
one case. Kristeller's maneuver was used in the reduce the risk of developing craniocervical block­
delivery of one infant with an upper brachial ages of infancy (as opposed to severe upper cervi­
plexus lesion. cal injuries).
The most severe birth injuries were observed
Extraction aids with emergency cesarean section. During the
delivery of one post-term infant with excess birth­
In 38 cases it was necessary to use artificial means weight, the uterus was ruptured when Kristeller's
of extraction for vaginal deliveries. It is worthy of maneu ver was performed and an emergency
note that Kristeller's maneuver was applied in cesarean followed. One infant was later found to
71% of these cases. have a brainstem hemorrhage. Another infant was
The risk of birth trauma appears to increase delivered by emergency cesarean section without
when extraction aids are used, especially if there any further risk factors being present, yet peri­
are additional risk factors. Three newborns (two partum upper cervical trauma was strongly
with birthweight >4000 g) had fractures of the suspected.
clavicle. Kristeller's maneuver had been used.
Additional risk factors
Cesarean section
Additional risk factors were present in a large
Cesarean delivery had been performed in 35% of number of births.
the cases.
The main risk factor in elective section was
Breech presentations
abnormal fetal position, which occurred in 40% of
the infants delivered by this means. However, 30% First deliveries appear to be a predisposing factor
of the group under study exhibited none of the for breech presentations (Boos 1994, Rayl et al
assumed risk factors (e.g. elective cesarean sec­ 1996). It is therefore assumed that the firm abdom­
tion) but still developed dysfunctions of the cran­ inal wall of primiparous women and the fact that
iocervical joint. Assuming an average rate of the uterus has not previously been stretched make

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spontaneous turning more difficult. Multiparous mechanical stress for the fetus (e.g. abnormalities of
women are at similar risk for the opposite reason: the pelvis or of engagement) (Schmitt-Matthiesen
low tension of the uterus wall and too little pres­ 1992) and so involve greater risk to the craniocer­
sure from the abdominal wall muscles offer too lit­ vical transition zone.
tle resistance to support the turning movement,
aided by the extremities (Feige and Krause 1998).
Short expulsion period (<10 minutes)
Abnormal fetal position is often associated with
intrauterine forced positions on account of lack of Here, too, an increase in the mechanical stress on
space, which can lead to dysfunctions in the cran­ the fetus is probably brought about by strong con­
iocervical transition zone (Biedermann 1999). tractions (Schmitt-Matthiesen 1992), exerted par­
However, four infants with such abnormalities of ticularly on the presenting parts of the fetus and
lie during pregnancy were delivered sponta­ the upper cervical transition zone. There is no
neously and without complications with cephalic exact quantitative time definition of precipitate
presentations. They nevertheless had craniocervi­ birth with a short expulsion period, with reference
cal blockages. It is interesting to note in this con­ simply being made to delivery with 'few labor
nection a circumstance that has been known for pains' (Martius and Rath 1998). In establishing a
some years: that breech delivery infants have history it is difficult to verify such details of the
often developed 'congenital torticollis'. In these final stage of childbirth, and the solution chosen
cases, too, the cause was assumed to be intrauter­ when recording the data was to use information
ine forced positions (Martius 1964). The author about the length of the expulsion period.
further believes that the Mauriceau-Smellie-Veit
maneuver in vaginal deliveries predisposes to
Birthweight above 4000 g
developing tills type of birth injury.
Another explanation may be that the different More than 13% of the infants with craniocervical
birth presentation in hIm affects the mode of deliv­ blockages had a birthweight in excess of 4000 g,
ery and adds a potential further risk to the upper and delivery of these infants was more often arti­
cervical transition zone. Almost 80% of the 48 cases ficially assisted or carried out by emergency sec­
of abnormal fetal position during pregnancy or tion, in line with the percentage of these high
birth were delivered by cesarean section. birthweight infants within the particular mode of
delivery. High birthweight was the only risk factor
for half the infants assessed as being in the high
weight category.
When infants have been intubated after birth, the
procedure (i.e. intubation) itself and the resultant
Premature births
trauma can be considered as possible causes of
craniocervical blockages. Also, problems of respi­ Premature birth was recorded in 42 cases (approx­
ratory distress may signal the presence of a lesion imately 10%). Assuming a premature birth rate of
of the cervical spine caused by birth trauma 6-8% in German-speaking countries (Goerke and
and/or the consequence of other types of central Valet 2000, Pschyrembel and Dudenhausen 1991),
nervous damage. this represents only a slightly increased rate in the
study cohort. The proportion of infants who had
been bom prematurely and had craniocervical
Prolonged labor (>24 hours)
blockages after elective cesarean section was rela­
Prolonged delivery is frequently associated with tively high. This is pOSSibly connected with the
increased birth risks that can result in an abnormal indications for elective section as opposed to vagi-

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Birth t r a u m a and its i m p l ica tions for neu r o m oto r d e v e l o p m e nt 95

nal delivery, which are fairly generously framed this group was therefore recorded together. Most of
for the premature birth group. Another point is the 10 cases assigned to this group must have
that four premature infants were intubated involved uncomplicated instances, since the care
following elective section, making postnatal records did not document the fact. The compara­
causes a possibility. tively high incidence (2.5%) of this feature in our
Children born considerably before term spend study cohort was, however, surprising. Such events
some time without full head control. Increased are described as happening in 0.05-0.1% of all births
postnatal inertia load on the upper cervical struc­ (MandIe et al 1995). Infants born to multiparae are
tures can therefore be considered in such cases. reported to be particularly affected.
However, the small number of premature babies
delivered spontaneously and without further risk Conclusion
factors contradicts this as an explanation. At 5%
this percentage was within the expected range for In conclusion, each mode of delivery contains its
premature births. It is more probable that infants own specific risks to the upper cervical region,
whose gestation period is markedly shorter are irrespective of the presence of additional risk
more likely to develop craniocervical blockages factors.
on account of the risks associated with this. Additional risk factors for the development of
craniocervical blockages in infancy could be
assumed in more than two-thirds of all sympto­
Post-term births
matic infants. These include the use of Kristeller's
Normal term was exceeded in just 11 cases. This maneuver, high birthweight (>4000 g), short
risk factor was only encountered once on its own in expulSion period, intrauterine forced or abnormal
combination with elective cesarean section; in most positions, occipitoposterior position or prolonged
instances these post-term births were accompanied delivery (>24 hours), prolapse or presentation of
by high birthweight (a total of 4) or the delivery an extremity, shoulder dystocia and postpartal
called for manual and/ or artificial assistance. traumas such as intubation. Premature birth, post­
term delivery and twin pregnancies appear to be
co-factors that often occur together with the above
Occipitoposterior position
risk factors.
A total of 10 infants presented in the occipitoposte­ The contention that birth trauma plays the pre­
rior position, a figure that was just 3% of all included dominant role in the pathogenesis of craniocervical
infants with cephalic presentations. However, from blockages of early infancy (i.e. that perinatal trau­
its incidence in the average population, one would mas are the main cause) is not without its critics
expect to find the occipitoposterior position in (Buchmann and Bulow 1983). As in adults, other
0.5-1 % of all cephalic presenta tions (Pschyrembel causes for dysfunctions of this type are logically
and Dudenhausen 1991). Since the position is unfa­ pOSSible and may in fact be responsible. In particu­
vorable for the upper cervical region, this aspect lar, the cause may be reactions that are visceral or
may once more constitute a predisposing factor here. static-dy namic in nature; or the dysfunctions may
stem from cerebral errors in the control of the
motorsensory system. The young age of the study
Limb prolapse/presentation
cohort, however, makes these causes less likely.
It was difficult when taking the history to differen­ If the risk profile for the development of classi­
tiate between actual prolapse of arm or hand and cal upper cervical lesions, which was mentioned
presentation of the extremity, or between complete at the beginning, is compared with the risk factors
and incomplete prolapse of the fetal extremity, and presented here for the occurrence of reversible

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a rti cular dysfunctions of the craniocervical joints rics, cal ling fo r a p p ropria te obs tetric sk i l l .
in symptoma tic infants, the common elements Kno wledge of these risks makes i t p ossible to
cannot be ignored. Where the causative mecha­ avoid them in the context of p reven tive obstet­
nism is the same, only the degree of trauma or rics, and also enables imp rov ed assessmen t of the
a d d i ti onal ind ividual factors will determine the birth trauma inv olved, w i th the necessary type of
extent of the cervical lesion . a ftercare .
Birth is a ttended by risk of tra uma independently
of the mechanism of childbirth and even obstetric
I M P L I CAT I O N S F O R P R A CT I C E practice in s trict conformity with accepted principles
can do no more than minimize the risk. Seen in this
Each mode o f d e l ivery carries ind iv i d ual risks, light, obstetrics becomes both the price of our evolu­
b o th in i tself and in the implica tions for obstet- tion and the challenge with which it presents us.

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Chapter 9------�----�

Differential diagnosis of central

and peripheral neurological
disorders in infants
L. Babina. H. Biedermann. S. Iliaeva

Small children, before undergoing manual ther­

CHAPTER CONTENTS apy, have to be thoroughly examined as their
symptoms are so diverse at the time of the first
Medical history 101
encounter. One of the biggest problems for those
Jack be nimble, Jack be quick: observation and
active in this field is to achieve a valid differential
appraisal of movement and posture 102
diagnosis in order to distinguish between a func­
Examination in the dorsal position 103
tional and/ or truly central (i.e. cerebrospinal) origin
Examination in the ventral position 104
of the clinically observed situation. Neuropediatric
Examination of cranial nerves and eye
and nemo-orthopedic procedures can help to
muscles 104
improve the level of this still difficult distinction.
Testing the muscular tonus 105
We have to accept the fact that most of the small
Vojta's reactions 107
children we examine and treat suffer from a com­
The differential diagnosis: functional
bination of those two types of problems. Com­
vertebrogenic versus central/spinal 109
bined with the injuries and irritations acquired
Conclusion: standing on two legs 111
d u ring delivery or in utero are genetically deter­
mined ailments and other morphologically fixed
A sharp separation between the three groups
(genetic, central and functional) is by no means as
simple as one would like it to be, but up to a point
we are able to define probabilities which help to
sort out those children with a mainly central (i.e.
neuromorphological) problem and those where
the predominant part of the pathology can be
attributed to a functional disorder in the arthro­
vertebral region. This differentiation does not
i mply that children with a primarily neuromor­
phological disorder calU10t be treated with man­
ual therapy and profit from such a treatment. As
we point out in Chapter 25, patients with cerebral
palsy improve markedly after manual therapy.

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But the primary cause of a given problem has to • perinatal injury of the spinal cord
be evaluated as well as possible in order to define • perinatal injury of the vertebral spine
our treatment goals realistically. • lesion of a peripheral nerve
This diagnostic canon does not yet exist. One of • neuromuscular disorder
the main reasons is the fact that most neurologists • endocrine disorder.
and pediatricians do not recognize that functional
Differentiation between these possibilities is not
disorders of the vertebral spine may make an
easy with the standard tests, let illone an assess­
important contribution to their patients' prob­
ment of where the problem originates. Here the
lems. Until now it was the cerebrum where one
work of Ratner comes into play. Until his prema­
looked in order to find the cause of neurological
ture death in 1992 he was head of the neuropedi­
problems. As the role of the spinal system has
atric clinic in Kazan (Ratner and Bondarchuk
been neglected there is no incentive to pay much
1990, Ratner and Michailov 1992) a nd published
attention to this differential diagnosis. This is the
prolifically on pediatric neurology and perinatal
situation in the West, at least until very recently. In
injuries of the spinal column. Based on this work
Russia, on the other hand, a long-established tra­
a more precise procedure is possible.
dition exists of examining this area situated
Assigning a neurological finding to a neurope­
between neurology and orthopedics.
diatric category or a neurological syndrome
To establish a diagnostic base we use observa­
and/ or a functional vertebrogenic disorder offers
tion of the spontaneous movements, examination
some important possibilities to a manual thera­
of the primitive reflexes and Vojta's screening tests
pist, as it is the base from which to decide about
(Fig. 9.1) (Vojta and Peters 1992). These tests show
further diagnostic tests and the ensuing therapy.
abnormal movement patterns with a multitude of
To compile this information, neurologists, pediatri­
cians and manual therapists have to work together.
• disharmonious maturation of an otherwise This is easier said than done, as these different spe­
intact cerebrum cialties use a different vocabulary. Here we have
• cerebral trauma tried to bridge this gap and offer an in i ti al version .

Figure 9.1 A: Peiper­

Isbert-reaction. B: Vojta test.
The correct interpretation of
these tests has to take into
account the developmental age
of the child. The two pictures
show a norma I reaction pattern
for a 3-month-old.

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Different diagnosis of neurological disorders 101

We do hope to improve on this using the com­ centralproblem often have retarded psychic
ments of our readers. development, too. In KISS children there is often a
marked difference between the apparently normal
mental and the slower sensorimotor side of devel­
MEDICAL HISTORY opment. Parents often talk about the unhappiness
of their (KISS) children who want to do things
The history starts with the family history and the they cannot achieve, thus becoming discontented,
health situation of the mother. One main focus is unhappy and angry.
on the risk factors before and during pregnancy: There are many variants in the motor develop­
ment which are interp r eted di fferen tly depending
• Which (if any) medications and/or drugs were
on the viewpoi nt of the examiner.
ta k en ?
Most neuropediatric specialists tend to con­
• lnfectious diseases, e.g. cytomegalic inclusion
sider a child's preference to shove on the buttocks
disease and rubella, or endocrine disorders, e.g.
(Fig. 9.2) instead of crawling a normal variant of
hyperthyroidism, dysfunction of the suprarenal
motor dev elopm ent. Seen from the viewpoint of
gland. The third group are cardiovascular prob­
manual therapy, this preference indicates prob­
lems, e.g. valvular defects. Problems in these
lems with the sacroiliac (SI) joints and /or the
fields increase the p robability of a more 'cen­
occipitocervical (OC) r eg ion.
tral' neurological problem.
For most parents the moment when their child
Problems immediately before or during birth: starts walking is much more i m portant than the
period during which the child crawled. Almost all
• premature labor
professionals, on the other hand, put the emphasis
• transverse presentation
• placental anomalies
• delayed delivery
• twin pregnancies
• lengthy labor
• oversized child
• vacuum extraction, forceps or other extrac­
tion aids.

All these items make functional problems more

Our questionnaire covers these items and the
completion of this form hel ps the parents to
remember these details. It is astonishing (and
has to be taken into account in the evaluation of
the questionnaire) the extent to which the
details of the deli v e r y are fo rgotten by the par­
ents - and how sketchy the documentation of
the delivery often is. We saw several callused
clavicular fractures in children whose birth was Figure 9.2 Shoving on the buttocks. This movement
pattern is often used by babies who cannot master the
described by parents and documentation as
difficulties of crawling. Its pathological significance is
'quite normal'.
often underestimated. These children are able to develop
Sensorimotor development of the child: chil­ normally, but having left out the crawling phase makes
dren w ith retarded motor dev elopment due to a them susceptible to other coordinative disturbances.

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on this detail of motor development, as it is a very conditions are not always met . It is important that
good indicator of a child's motor competence. the child is well rested and neither hungry nor ill.
Crawling is by far the most important step in the An experienced therapist starts grasping vital
acguisition of bipedal gait and - skipped over - diagnostic information the moment the family
the lack of this coordination level tends to render comes into the room - which is one of the reasons
the further coordinative successes more fragile we strongly advise being present when the baby is
(Birrer and Levine 1987, Loovis and Butterfield brought into the examination room. This enables
1993, Patel et al 2002). So it is important to get the therapist to evaluate the reaction of the child
information about other 'milestones' (Ayres 1979) to the room's setting and to use this background
in the child's development as well. information to gauge the reaction to the tests per­
All these observations should be comple­ formed on and with the child.
mented by reports of others, especially those who The first aim in dealing with a new yOLUlg
are already in professional contact with the child, patient should be to open up to the Gestalt of the
e.g. physiotherapists or creche staff. Another aid disorder, i.e. use one's professional prejudices.
to verify the statements of the parents are photo­ This is an intentionally provocative remark, but -
graphs. To that end we ask the parents to bring especially for the beginner - the over-supply of
pictures of the first years of their child. The gual­ available tests tends to hide the basic truth that a
ity of these photographs varies widely, but more clinical diagnOSis was and will be an act of intu­
often than not they offer at least a base for further ition. If this was not the case we could indeed pro­
guestions to the parents. Quite a few parents are gram computers to take care of diagnostics - and
themselves surprised to what an extent one can treatment, too, for good measure. But this first
see a stereotype posture in these albums. impression needs to be verified, guestioned and
Sometimes when you look at the siblings and fine-tuned to the individual situation in order to
remark on their individual postural pattern the give us a meaningful base to proceed from.
ensuing discussion leads to the discovery of Our examination of the small child has to be
related problems in these children. guicker than the evaporation of patience of the lit­
tle patient - which takes place guite rapidly. It is
not realistic to ask all relevant tests to be applied
JACK BE NI MBLE, JACK BE QUICK: in order to get a valid diagnosis. Having gained a
OBSERVATION AND APPRAISAL OF first hunch by observing the child on the arm of its
MOVE MENT AND POSTURE parent, we apply the most important tests first
and continue from there as far as the patient
Almost all books on pediatric neurology offer a allows us to go, keeping in mind that we need a
fairly comprehensive overview of the tests and minimum of compliance for the treatment, too.
observations appropriate for a specific age, and The observation of the child's spontaneous
this is not the place to list them (Dubowitz et al movements is the principal source of information
1999, Fenichel 2001, Swaiman 1994). It should be for the examiner; all tests serve to standardize
emphaSized that the neurological examination of the hunches one gets from the examination of the
all children, and especially newborn and toddlers, baby before one even touches it. And the more
has to be smooth and as guick as possible in order the child is in distress, the more the watching par­
to succeed. Before one even touches the baby, a ents will get nervous - which feeds back onto the
calm and trustful atmosphere has to be estab­ child's behavior immediately. The amount of dis­
lished. Enough space, no external noise and a tress is of diagnostic interest, too, and one should
well-lit and warm environment may sound like a keep in mind at what time of day the child is pre­
matter of course, but in practice these basic pre- sented. The younger the child, the more the diur-

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Different diagnosis of neurological disorders 103

nal rhythm plays a part, and at noon almost every Adduction and pronation of the arms and/or
child is much more irritable than between 9 and 11 extension and inside rotation of the legs are
a.m . So it does make sense to note the time of the symptoms of central nervous problems. KISS chil­
examination routinely. dren, on the other hand, often show unilateral fist­
It is useful to make the transition of the baby ing, mostly on the concave side of the body,
from the parent's lap into our hands as smooth together with fewer (or less differentiated) move­
as possible. At the end of the initial conversation ments of the extremities on that side. After manip­
we sit next to the parents and help them to ulation, this often changes rather quickly and the
undress the child while it is still on their lap. ability to grasp things improves.
How far we go with this undressing is open to Children in whom there is a risk of cerebral
discussion: in the beginning of our work with palsy do not show such an improvement.
small children we routinely undressed them We also look to see if there is a 'cervical' pattern
completely, the way we were taught at univer­ to the child's symptoms. Facial asymmetry, unilat­
sity. Later on we realized that there is a trade-off eral enophthalmos, marked folding of the neck
between the area of skin visible and the mood of skin (often clammy) and a laterally fixed posture
the little patient. So we use a bit of realpolitik and of the head are signs which direct our attention
mostly leave the underwear on, at least in the towards a functional problem of the (cervical)
beginning. It is easier to examine a moderately spine. In children 'with a fixed retroflexion (KISS
cooperative baby in its underwear than a naked II) a marked persistence of the Moro test is typical.
baby stiff with anger. These children react with a marked and Moro-like
movement to noise and change of position well
Examination in the dorsal position beyond the age of 5 months.

We start the examination in a dorsal position, try­

ing to get into visual contact with the child. Some
important points: does the child seem to be happy,
relaxed'? Were we able to pick it up from the par­
ent's lap without too much adverse reaction?
Sometimes a total lack of negative reaction is a
pathological sign, too. How does the child react?
Does it avert its gaze or do the eyes follow move­
ments? If we get eye contact, does the child follow
with its gaze in all directions?
From mon th 4 on we can offer toys to grasp and
We observe if there are appropriate motion pat­
terns, stereotype gesturing, tremor or myoclonal
How is the posture on the examination table? Is Figure 9.3 Moro reaction. This reaction is physiological
there a constant or intermittent opisthotonos? till the third month. Later on its persistence is

How does the child react to noise (Moro test pathological. The differential diagnosis between a
functional or central origin is not easy. Persistence till
and similar maneuvers, Fig. 9.3).
adolescence may be one reason for coordination
Examination of the head should consider the fol­
disorders ( Goddard Blythe and Hyland 1998). In this case
lowing: micro- or macrocephaly, fontanelle promi­ the lack of head support and the asymmetry of the
nent or caved in, how are the cranial sutures? hands are pathological.

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Examination of the form of the thorax and the Sometimes the child compensates for the
abdomen is important, too. Children with a paretic restricted range of movement by bfting the shoul­
diaphragm have a retracted lower rib case which is der. By pulling up the shoulder the distance
fixed in an exhalation position. A reduced muscle between origin and insertion of the sternocleido­
tone of the abdominal muscles can have a multi­ mastoid muscle is mi.nirrUzed. In those cases where
tude of different origins which have to be checked. - through treatment or by its own means - the child
is unable to overcome this condition, there is a
Examination in the ventral position chance that the muscle reacts to this long-term
shortening by fibrotic transformation. This transfor­
Next is the examination in the ventral position mation of the muscle results in a thin, piano-wire
(Fig. 9.4). First and foremost we are interested in like remnant of the sternocleidomastoid. These
the posture and movement of the head and the cases cannot be effectively treated by means of a
coordination of the arm muscles. From the age of functional therapy, be it manual therapy or other
4 months the child can support head and shoul­ physiotherapeutic means. In most cases a myotomy
ders, albeit still a bit wobbly, in a neutral and sym­ offers the best chances of improvement.
metrical position and is able to direct head and Children with a basically functional problem
eyes towards a stimulus. display a mild form of absence of head control; a
KISS I (fixed lateroflexion) children often have basic muscular tonus is present and this tonus can
delayed head control and an asymmetrical pos­ be reinforced by repeatedly testing it. If the muscu­
ture. If the stimulus comes from the 'right' - i.e. lar tonus is severely reduced or completely absent,
convex - side they are able to fixate the stimulus a central origin of this condition is probable.
and they will follow it with their eyes till the point KISS II children display hyperextension of the
when the limited movement range of their cervical head in the ventral position and a fixated thoracic
joints prevents further following. If the baby is in a hyperkyphosis. Because of the hyperactivity of the
mood to be sufficiently cooperative this allows for neck extensors, the shoulders are often protracted
a repetitive test of the range of movement. It is evi­ and the child cannot bring the elbows into a ven­
dent that this restriction of movement is frustrat­ tral position (see p. 287). We call this posture 'the
ing (and painful) for the child and one reason for dying swan' (Vasilyeva et al 2001). An additional
the fits of rage these children sometimes display. test is to check for hypersensitivity of the neck
area, especially the insertions at the occiput.
It is essential to distinguish between the hyper­
extension due to functional and arthrogenic prob­
lems and the classic opisthotonos caused by central
nervous problems, e.g. meningitis.

Examination of cranial nerves

and eye muscles

We also examine the quality of the cranial nerves

and the functioning of the eye muscles. Eye move­
ment can be tested by establishing eye contact and
moving one's head in front of the child. Alterna­
tively a toy or a colored object might be moved in
Figure 9.4 Ventral examination: inadequate prop of the
shoulders. This baby cannot bring the right arm into a front of the child's eyes. A strabismus convergens
supportive position. (nervus abducens) or divergens (nervus oculomo-

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Different diagnosis of neurological disorders 105

torius) has to be excluded. The optico-facial reflex In the quite frequent case of a combination of IS
gives a rough idea about the strength of vision blockage and a dysfunction of the central nervous
(nervus opticus), as the auro-palpebral reflex system, the normalization of the joint function
allows testing of the infant's hearing. leaves the reduced abduction as the persisting
The evaluation of the functioning of the facial 'central' sign.
nerve distinguishes between a central paresis
affecting the muscles of the lower half of the face
Muscle reflexes
and a distal paresis which affects the entire face.
The caudal group can onJy be examined and evalu­ The routine control starts with ASR (LS / S1 ),
ated indirectly (nervus vagus, nervus glossopha­ PSR(L3 /L4 ), BSR(C s / C 6 ) and TSR(C7/ C8) . We reg­
ryngeus, nervus hypoglossus.). In a newborn baby ister the amount of response, and possible
with swallowing difficulties, injury to these nerves enlargement of the zone, and compare the reac­
has to be considered after other possibilities have tions on both sides.
been excluded. Positive Babinski and Rossolimo reactions are
pathological from the fourth month on. KISS
Testing the muscul ar tonus children without neurological problems display
normal and symmetrical reflexes without these
The neonatal au tomatisms and the muscular signs.
tonus are the next steps in the test battery.
First and foremost we are interested in whether
Primitive reflexes
the different muscle groups display a regular
muscular tonus, comparing the upper and lower For the examination of the primitive reflexes we
extremities and the left and right side as well as use Ratner 's methodology (Ratner and Bon­
the tonus of the ventral and dorsal muscle groups. darchuk 1990).
The tonus can be normo-, hyper- or hypotonic and
regionally different. KISS children without addi­
Search reflex
tional neurological problems have a normal
muscular pattern. Slight touch of a cheek induces a search move­
If an elevated muscular tonus is found we have ment of the mouth and slight rotation of the head
to look for articular disorders. A hip dysplasia to the side of the stimulus. The neuronal chain
with reduced abduction results in a heightened includes the nervus trigeminus as its afferent and
muscular tonus of the adductor and the psoas the nervus facialis (mouth movement) and the
muscles, but a blockage of the iliosacral (IS) joint nerves of the upper cervical segments (head rota­
can cause the same phenomena. Additional differ­ tion) as the efferent part. If the child does not
ential diagnosis is always necessary in these cases. sense the touch we suspect a cerebral problem; if
A hip dysplasia can be verified by sonography the head rotation is reduced a cervical disorder is
and / or radiography, an IS blockage is associated most probable.
with local trigger points and a palpable dysfunction
of the joint; it should subside shortly after success­
Sucking reflex
ful treatment, either locally or at the OC junction.
If these two causes can be excluded, a central If a nipple or a finger is found with the mouth, a
coordination disorder becomes the mos t probable sucking movement begins. This neuronal chain
reason. In this case we expect to find additional goes via nervus trigeminus. nervus facialis,
signs, e.g. fixed extension and inversion of the nervus vagus and nervus hypoglossus. This reflex
foot! feet and spasticity of the biceps surae muscle. is purely cerebral.

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In a few cases the sucking response this test. In KISS II children this reflex persists for a
improved very quickly after cervical manipula­ long time, disappearing rapidly after successful
tion. A possible explanation might be found in treatment (i.e. 1-3 days later).
an increased perfusion of the vertebral artery
with a consequent improvement of brainstem
Galant reaction
During this test the child is held in a ventral- and
strictly horizontal - position supported under its
Babkin reflex
belly by the hand of the examiner. Starting from
The baby is in a dorsal position and the palms of the lower scapular angle the paravertebral skin is
its hands are pushed with the thumb of the exam­ stimulated by gently stroking it. This elicits in nor­
iner. The normal reaction is an opening of the mal cases a slight contraction of the muscles of
mouth. This is a purely central reflex. this side resulting in a side-bending of the trunk to
this side. The head follows this movement.
If the Galant reflex is missing a spinal lesion is
Grasping reflex
probable; central lesions do not seem to influence
The forefinger touches the palm of the hand, corning this test. We often see a asymmetrical reaction in
from the wrist. The ensuing grasp reflex is assessed KISS I children.
qualitatively and in comparison with the other side.
The neurological chain of this reflex uses the seg­
Foot-grasp reflex
ment levels Cs-Cs' This reflex is purely spinal and a
cerebral or high cervical lesion leads to a marked The examiner places his thumb on the sole of the
amplification of the response on the traumatized baby's foot close to the toes. More or less rapidly a
side. In cases of plexus paresis and lesion of the 'grasping' reflex is elicited. The quality of this
lower cervical structures, this reflex is attenuated. reaction can be classified as normal, intensified or
KISS I children without signs of neurological reduced. The neural chain of this reflex involves
impairment often show a diminished reaction to the lumbar segments LS-S2.
that stimulus on the side where the muscles are This reflex is attenuated in cases of cerebral palsy
shortened, a phenomenon we explain by the and more frequently due to lesions of the lumbar
reduction in muscular strength on the concave spinal cord, e.g. in babies born in the breech posi­
side due to the inhibition of these muscles on the tion.
segmental level.

Walking automatism
Moro reaction (see Fig. 9.3)
The reflex chain of this test runs along the spinal
The child is placed in a half-sitting position and segments; in spasticity and after trauma to the
fixated at the back and the head. A slight passive lumbar spinal cord this reflex is diminished. In
retroflexion of the head sets off a generalized cases of athetosis, this automatism persists after
movement of the arms. The neuronal chain of this the third month.
reflex runs through the cervical level CS/C7. Atten­
uation of this reaction can be the result of a central
The tonic neck reflex
muscular hypertension, a lesion of the lower cervi­
cal area or a trauma to the plexus brachialis. KISS I The elucidation of this reflex peaks between the
children without additional neurological problems second and third months, but it can be found ear­
show, in most cases, an asymmetrical reaction to lier. If it persists after the third month, this is con-

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Different diagnosis of neurological disorders 107

sidered to be a si gn of a central lesion, and cer­ KISS I children often show an asy mme tric pos­
tainly if present afterthe sixth month. We see this ture of the head (Fig. 9.5), less frequently a weak­
reflex in chi ldren with KISS aged 6 months and ness of these muscles. KISS II children show a
older wi thout any other signs of a central lesion characteristic reaction pattern. Recognizing this
and the pathological pattern subsides after man­ pattern can make it easier to find a functional dis­
ual therapy of the su b occipital struc tures . order of the OC junction even when other signs
are less clearly discernible.
Vojta's reactions The anteflexion of the head proceeds in two
phases. Initially the nodding movement is initi­
These standardized tests (Vojta 1988) are a handy ated by the activation of the short flexors of the
screening tool when examining the state of the neck. This movement takes place exclusively in
sensorimotor system during the first y ear. Our the upper cervical spine (i e. . CO/C2) without any
im pression is that we have to re-evaluate the sig­ involvement of the rest of the cer vical spine,
nificance of these tests according to the influence which becomes activated in the second phase of
of the suboccipi ta l structures on the smooth func­ the anteflexion. Now the long flexors and the
tioning of the motor patterns involved. To illus­ entire cervical colu.mn (i.e. to T3) take part in the
trate these considerations we shall focus on the movement. These muscles are innervated by the
first four tests. spinal nerves caudal to C3. The short flexors are
innervated via nerves originating in the craniocer­
vical junction, which renders them irritable by dis­
Traction reaction
turbances of the functional equilibrium of this
This test figures centrally in our examination of level. This irritab i li ty is twofold, as it can be
small children. The trac tion reaction yields a lot of caused directly by mechanical irritation of the
information about the degree of coordination in local nerve fibers and via the spinal/pontal pro­
the dorsal position Especially interesting are the
. cessing of faulty inpu t from thi s region, a phe­
posture of the head and the legs and the relative nomenon we could validate experimentally
movements of shoulder and pelviS. (Vasilyeva et al 2001). This makes it especially
Any analysi s of the functioning of the muscles important to examine the two pha s es of head
supportin g the head can at the most be summary. anteflexion separately.

Figure 9.5 Traction reaction. This child has a marked weakness in supporting its head in the first phase (A) pulling
the chin to the chest. Afterwards the head is thrown back (B) and pulled forward asymmetrically (C). Differential
diagnosis with a central tonus disorder: the muscular tonus of the rump is normal, only the short flexors of the neck
are weakened. Together with the asymmetry of the head posture in C, this is typical for KISS.

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For this differentiated examination we use are in hyperlordosis. The head founders after a
Janda's method (Janda 1983), which we modified few minutes toward the support. The dystonia
slightly for the examination of small children: between the attenuated flexors and the hyperac­
To examine the function of the short flexors of tive extensors which we found in KISS II children
the neck the child is put on its back and a bright (Vasilyeva et al 2001) helps to explain this pattern.
toy is held in front in such a way as to attract the
child's attention. After the child has fixed the toy
Axillary suspension response
with its eyes we move it cranially in order to force
the child's neck into a retroflexion. Only then is The child is held in a vertical position with its back
the toy moved caudally; the child will react to that to the examiner. To get reliable results one has to
by activating the short flexors (nodding) and later take care to hold the trunk without irritation of the
on by using the entire neck muscles to bend the trapezius muscle (this would provoke an exten­
head forward in order to follow the moving toy sion of the lower limbs).
with its eyes. A blockage of the IS joint results in an increased
Babies with a fixed retroflexion cannot nod. In or diminished flexion of the relevant leg, depend­
the first phase of the anteflexion the head is ing on the relative position of the sacrum and
instead hyperextended or not included in the ilium. Fixed extension of the legs with scissoring
movement at all. We call this a dove's move and toe stance are certain signs of a spastic lesion.
(Vasilyeva et al 2001). In the second phase the
child catches up and in using the long flexors the
Vojta reaction (lateral tilt maneuver) (see
head is indeed brought up.
Fig. 9 . 1 B)
If the baby has a unilateral blockage of an IS joint
we observe an asyrrunetry of the bending phase of The child is initially held in a vertical position
the legs or an asynunetry of the rotation of the legs. from which it is tilted laterally into a horizontal
This movement pattern has to be distinguished position. Care should be taken to have the child's
from the early signs of a cerebral palsy. The latter hands open when starting the tilt, as closed hands,
shows a fixed extension of the leg in inner rotation especially in early infancy, might provoke an arti­
of the leg at the affected side. Here the leg is held in ficially abnormal flexed posture of the arm.
an extended posture with predominance of the tri­ In examining the reaction of the child we have
ceps surae muscle, and scissoring of the legs and toe to pay attention to the upper half of the body, i.e.
stance. Sometimes a similar picture can be observed the posture of the trunk and head and the upper
in children with a bilateral blockage of the IS two extremities. KISS I children have an asym­
joints. In these cases the fixation of such a posture metrical posture of head and body. The position­
diminishes soon after the successful manipulation. ing of the head is markedly clumsy on the side of
the dysfunction, the hand often in a fisted position
on the opposite side. The posture of the legs is
Landau reaction
mostly asymmetrical, too.
We look at the posture of the spine as a whole KISS alone does not lead to adduction of the
together with the positioning of head and extrem­ l e gs or forced extension of the feet. If these signs
ities. In cases of KISS I the asymmetry of the neck are present, an at least partially central genesis of
and skull is immediately distinguishable. A hypo­ the problem is very likely.
tonia of the trunk is rather rare in these cases. Children with a KISS II symptomatology may
KISS II children show a typical position, too. show a Moro-like reaction after the age of 5
The shoulders are retracted and the edges of the months. Hyperextension of the head, retraction of
shoulder blades approach each other, the head is the shoulders and a (reactive) hypotonia of the
hyperextended and the cervical and dorsal spine trunk are part of this clinical picture, too.

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Different diagnosis of neurological disorders 109

THE DIFFERENTIAL DIAGNOSIS: This is by no means a request to drop diagnos­

FUNCTIONAL VERTEBROGENIC VERSUS tics and fall back on a purely pragmatic 'how-to'
CENTRAL/S PINAL approach to rehabilitation - far from it. But one
should keep in mind that the eventual result of all
Having completed the whole neuropediatric exam­ these therapeutic efforts cannot be predicted with
ination, we have the necessary means at our dis­ any precision.
posal to reach a conclusion as to how many This caveat should be kept in mind when one
symptoms are caused by a functional vertebrogenic gives a long-term prognosis to the parents, who
problem (i.e. a KISS sensu stricto), by a more cen­ do naturally enough insist on it. The justified
trally situated disorder or by a traumatic lesion of a request of 'tell us everything' has to elicit a bal­
region of the spinal cord. It should not be forgotten anced response which avoids the pitfalls of draw­
that this differential diagnosis, necessary as it may ing too dark a picture or seeking refuge in an all
be for our assessment of the long-term prognosis of too rosy future. The former extreme is more com­
that child, does not alter the actual therapy too fortable for the doctor involved, as it is always
much. The combination of rehabilitative measures possible then to say 'I told you so' - but there is a
is more determined by the response of the young high probability that this pessimistic picture dis­
patient to the different therapeutic approaches than courages and demotivates family and caregivers,
by the eventual diagnosis. thus weakening the support our young patients
The one paramount conundrum of neuropedi­ need so urgently. If we are too optimistic, on the
atrics Jies in the fact that an exquisite arsenal of other hand, we are in danger of losing the confi­
diagnostic tools -even correctly used -leads more dence of the parents and with it any influence and
often than not to roughly the same therapeutic compliance.
protocols. Ultimately the outcome depends more A central coordination disturbance in combina­
on the initiative and personality of the individual tion with functional vertebrogenic disorders is
therapist and the supportive environment at probable if the following dysfunctions are observed
home than on the fine print of this diagnosis. (see also Table 9.1):

Table 9.1 Differential diagnosis

Clinical symptomatology 2 3

Asymmetry of movements + + +
Dysfunctioning of cranial nerves +
Muscular hypotonia + +
Increased muscular tonus or asymmetry + +
Asymmetry of myotatic reflexes + +
Persistence of Babinski and Rossolimo/Starling sign + +
Asymmetry of primitive reflexes + + +
Persist!"nce of primitive reflexes + ±
Vojta tests: asymmetry
In execution +b +b

1, KISS without neurological co-symptoms.

2, Combination of KISS and a central coordination disorder.
3, KISS combined with a cervical/spinal irritation.
a Besides Moro sign and ATNR.

b 'Functional' pattern.

C 'Central' (i.e. spastic) or hypotonic pattern.

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1 10 C L I N I CA L I N S I G H T S

• dysfunctions of cranial nerves tha t a trauma of the spinal cord during delivery
• missing early childhood reflexes or their results in a rather variable clin ical pictu re.
persis tence (with the exception of the Moro On the cervical level the situation resembles
reaction, the asymmetric tonic neck reflex closely tha t of cerebral palsy. A close examina tion
(ATNR) i n KISS II children) of the delivery history (forceps, vacuum extractor,
• seizures of a ll types breech presentation) and the presence of other
• central muscular hypotonia signs of cervical irritation may help to clarify the
• reta rdation of psychological development predominant cause of the problems observed.
• re tardation of language acquisition Signs of an irrita tion of the cervical part of the
• central disturbances of movement, e . g . spinal sympathetic nerve can be present, too . This group
p alsy or disorders of the pyra midal tracts of symptoms comprises unila teral enophthalrnia,
• dyskinesia and ex trapyramid a l and / or microsomia and flattening of the occipital part of
cerebel lar motion disorders . the skull.
In most cases of KISS I we find an irrita tion of
In our daily contact with these children we the cervical autonomous system on the contralat­
became aware of the fac t tha t a spastic dystonia is eral side of the functional impairment. In cases of
in many cases accompanied by a func tional prob­ KISS II this observation is very rare. To this day
lem of the OC j unction on the side of the hemiple­ we do not have the corresponding scientific inves­
gia . In cases of tetraplegia the blockage of the OC tigations at our d isposal, but some in teresting
junction is mostly found on the side of the more details are starting to emerge. In papers on sud­
pronounced symptoms. Due to this combina tion it den infant death syndrome (SIDS), Doppler sono­
can be difficult to distinguish between a mostly graphic research showed tha t rota tion and
functional vertebrogenic problem and an athetotic / ­ reclination of the head often leads to a decreased
dyskinetic disorder. Of course, children with a perfusion of the contrala tera l vertebral artery; this
central disorder can have problems of this kind a t might be a starting point for further research
the same time. From the viewpoint of manual (Sa ternus 1982) .
therapy it seems to be practical to check if there is Trauma tic lesions of the lower cervical seg­
a func tional problem with a vertebrogenic origin, ments (CS / C7) show another clinical picture. If it
as this can be dealt with much more eaSily. is only the motor neurons in the anterior horn that
These vertebrogenic components of the clinical are involved, the child shows a peripheral mono­
picture are peripheral to the main problem, but in or paraparesis of the arm(s) . The di fferentia l diag­
the context of a centrally triggered disorder, these nosis of a plexus lesion, Erb-Duchenne, needs to
functional problems gain a disproportiona te be excluded in these cases. If further neurological
impact on the clinical situ a tion. The role of man­ examination reveals signs of spastic symptoms,
ual therapy in these cases is not central - physio­ the diagnosis of a medullar base of the ensuing
therapy and training have a more important role. problems is facilitated . Our experience with these
But manual therapy offers an uncomplicated adju­ cases indicates tha t vertebrogenic functional dis­
vant therapy which in some cases is prerequisite orders and the mechanical irrita tion of the spinal
to a successful rehabilitation effort using physio­ cord are etio-pathogenetically intertwined, which
therapeutic techniques. is why manua l therapy is the most comprehensive
In many cases we found a combination of func­ approach in these cases.
tional vertebrogenic disorders with an irritation of Most of the symp toms are grea tly alleviated 2-3
the spinal cord . Ta king into account the ana tomi­ weeks after treatment. As this therapy does not
cal situation and the close proximity and in terd e­ demand a lot of effort or cooperation from chil­
pendence of these structures, it seems plausible d ren and parents, we recommend s tarting with a

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Di fferent d i agnos i s of ne u ro l o g i ca l d i sord ers 1 1 1

tes t m anipula tion as soon as acute destruc tive C O N C L U S I O N : STA N D I N G O N T W O L E G S

processes or tumors have been excl u d e d . Mini­
mizin g the in fluence of func tional vertebrogenic We hope to have shown here that the manual ther­
problems cla rifies the clinical p icture and helps to apy approach differs somewhat from that o f tradi­
optim i ze the rehabilita tion, at least in part because tional neurology. In examining newborn ba bies
of the enco u r a gement the improved situa tion con­ and to ddlers the a d d i tional information obtained
veys to the p a rents and therapists. b y looking for signs of b i r th trauma in the spin a l
Inj uries of the thoracic medulla are very rare a t s tructures opens the view to a wider r a n g e of pos­
birth. The defects are more often situa ted m ore sible p a thologies than the 'classic' approach wh ich
caudal ly, i.e. at the lumbar level and here involving a ttribu tes a l most every thing to d isorders of the
the pyramidal tra cts. This leads to a spastic paresis in tracranial s truc ture s .
of one or both legs. Other probable ca uses (spinal Manual therapy - applied spa ringly - can e a s e
s tenosis, tumors or a n isolated p ara-sagittal cere­ rehab ilitation and thus motiva te everyb o d y
bral trauma) a re much less frequen tly found . in volved i n this long- term endeavor. I t is qui te
The more massive traumas o f the lumbar spinal com mon to find a clearer clinical picture after the
cord a re quite as rare as those of the thora cic level. fun c tional problems of vertebrogenic origin have
These children display a mono- or diparesis of the been taken care of - at lea s t temporarily.
legs . In most cases, a typical anamnesis can be If the neurological component of the problem a t
found with breech (pelvic) presenta tion and a diffi­ hand i s dominant w e have t o s urmise tha t the
cult and / or forced delivery. treatment has to b e repea ted. In our experience i t
In both cases, these p rimarily central neurolog­ s u ffices t o d o that 2-3 times a year, a t least in the
ical lesions a re accompanied b y blockages of the continen tal E u ropean con te x t of a close-kni t col­
OC and IS joints. These func tional d isorders are labora tion b e tween man u a l therapy, physio ther­
not at the roo t of the clinical problem, b u t aggra­ apy a nd rehabilitation ( e . g . logoped ics, remedial
vate the situa tion fur ther. Their trea tmen t can education) .
fa cilitate the 'classic' rehabi lita tion and has to be A d d ing this new dimension to the therape u tic
repea ted regularly ( i . e . 3-4 times a year). This arsenal improves the fu ture prospects o f our
accompanying therapy is very motiva ting for the young p a tients w i thout imposing too much effort
fa mi lies and for the physi o therapists, as it makes on them - and in many cases we can provide the
p rogress possible w h i c h o therwise w o u l d b e l i t tle s tep forward th a t was missing.
beyond the reach o f the therapists .


Ayres A J 1979 Se nso ry in tegration and the c hil d . Western J anda V 1 9 8 3 On the concept o f pos t u r a l m uscles and
Psycho logica l Services, Los Angeles post u re . A ustr a l ian Journal of Physiotherapy 29:83
Birrer R B, Levine R 1987 Performance p a r a me t e rs in Loov is E M, B utterfield S A 1 993 I nfluence of a ge, sex,
c hi l d ren a nd adolescent athletes. Spor ts Medicine balance, an d sport pa rticipa tion on de ve l o p men t o f
4(3) : 2 1 1 -227 ca tching by chi ld ren g r a d e s K-8. Perce p t u a l a n d Motor
Dubowitz L, Dub owi t z V, Merc u ri E 1999 The neurological Sk ills 77( P t 2 ) : 1 267-1 273
assessment o f the p re term and fu ll - te rm newborn infan t. Patel D R, Pratt H D, Gre yda n u s D E 2002 Ped ia tric
C linics in Developmenta l Medicine 1 4 8 : 1 -155 neu rodevelopment and s ports participa tion. When a re
Fenichel G 200 1 C l i n ic a l p ed i a t r ic ne urology. Saunders, chi ldren read y to play s po r t s ? Pedia tric Clinics of North
Phila d e lphia A merica 49: 505-531
God d ard B l y t he 5, Hyland D 1998 Screening for neurological Ratner A, B on d a rc huk S V 1 990 [Neurologic evaluation of
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Journal of Occupa tion a l Therapy 61(10):459-464 4 :38-41

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112 C L I N I CA L I N S I G H TS

Ra tner A J, M ichai lov M K 1 992 Klinisch-rbn tgenologische Va si lyeva L F, lIewa S, Biedermann H 2001 EMG -
Befunde bei geburtstrau m a tischen Verletzungen der Veranderungen bei der ManuaJ therapie von
Halswirbelsaule. Kinderarzt 23 :811 -822 KJeinkindem. Manue Ue Thera pie 5 : 1 22-126
Satemus K-S 1982 Lageabhangige zirk u l a tionsbedingte Voj ta V 1988 Der zerebralen Beweg ungsstbrungen im
cerebrale Hypoxamie - eine ErkJarungsmbglichkeit des Saugl ingsal ter. Enke, Stu ttgart
p lb tz li che n Kindstodes. Zentralblatt Rechsmedizin 24:635 Voj ta V, Peters A 1 992 Das Vojta-Prinzi p . Springer, Berlin
Swaiman K 1994 P ed i a t ri c neurology. Mosby, St Lo u is

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Chapter 10

Manual therapy from a

pediatrician's viewpoint
H. KLihnen

I work as a pediatrician in a semi-rural area of

CHAPTER CONTENTS Germany close to the Dutch border. Our task is
the primary provision of pediatric care. This
Methods 114
brings a lot of children to our practice whose
Case history of the parents or caregiver 114
diverse problems were not easily attributable to
Neurological examination 114
our standard classification of pediatric problems.
Clinical examination 114
These cases included many children who were
Case studies 117
classified as 'hyperactive' or 'having problems
Statistical results 122
with their sensory integration'. In quite a few
cases , I accompanied these young patients
through the years without being really able to
offer specific help and the only resort was to
send these children to a physiotherapist. It was
through this contact that my attention was ori­
ented towards manual therapy as a specific treat­
ment for these problem cases. After some quite
impressive improvements achieved by manual
therapy (Kiihnen 1999) more and more of these
schoolchildren were referred to us. I thus had the
opportunity to examine the development of chil­
dren who display symptoms of KISS but had not
yet been specifically treated.
In our practice, the sensorimotor development
of the children was documented routinely during
the first years while performing the regular pre­
ventive medical check-ups. These files provided
the database for a retrospective evaluation of
those cases where we decided to apply manual
therapy at a later time. After getting to know
more about manual therapy, I noticed astonish­
ing changes with infants in their sensorimotor

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Case history of the parents or

Table 10.1 The routine checks on children during
their first years caregiver

Check-up number Age at check-up Review of the documentation, which was made

Ul At birth
during the preventive medical check-ups during

U2 3rd to 10th day the first y ear of the child, plus additional checks
U3 4th to 6th week (Vojta Schedule (Vojta and Peters 1992), M uen ch ­

U4 3rd to 4th month ener Funktionelle Entwicklungsdiagnostik (Allhoff

U5 6th to 7th month
and Rennen-Allhoff 1984), Denver (VanDevoort
U6 10th to 12th month
and Lee 1984, Fleming 1981), test battery for the
U7 21st to 24th month
U8 3 to 4 years diagnosis of minimal cerebral motor disorders
U9 after the 5th birthday (Pediatric Center, Munich)).

Neurological examination

development. Now I was curious to know what Included are the results of physiotherapy, occupa­
had happened to all the children with KISS who tional therapy and orthopedic examination. Also
had not been treated. taken into account are the vestibular function,
In Germany there are five obligatory preven­ proprioception, tactile perception, coordination
tive medical check-ups during the first year of a and auditory perception.
child. Another check-up is done at the end of the
second year, one during the fourth and one in
Clinical examination
the fifth year (Table 10.1). I especially focused on
schoolchildren who came to se e me because of
abnormal behavior, problems in school or per­
ception disorders. These children had difficulties Task: catch the ball with both hands and throw it
in writing and reading, struggled in minute with one hand.
motor activities (fine motor manipulations) and Observation: eye movement, ability to focus on

had difficulties in concentrating. Often they the ball, catching with both hands or with sup­
were outsiders in school, 'daydreamers', hyper­ port of the forearms and the whole body, sup­
active and enjoyed neither sports nor play ing po rting the posture by holding the arms c lose to
games. They had difficulties in their social sur­ the body, crossing the middle-line, ability to
rounding, struggled with social contacts or they stand firm, but at the same time to change
were loners. Often they were only focused on positions.
one single friend. Clumsiness and slowness pre­
vail in these cases and the technical term used is
dy spraxia.
Task: kick the ball with one leg.
Observation: which leg kicks, hemispheric special­
METHODS ization, associated movements, does the child
need support, does he have to hold on to some­
To assess the problem at hand we use a standard th ng, is he able to deal with a moving ball or does

procedure which consists of the followi ng he have to set up the ball in a certain position
i t e ms . before kicking it .

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Manual therapy from a pediatrician's viewpoint 115

without eye contact; movements should be done

one after another.
Task: first, move one foot after the other forward. Observation: reJiability of thumb-finger opposition,
Second, walk the same way backward, walk for­ progression, posture of fingers.
ward again, but without looking down to the line.
Observation: does the child walk with feet pointing
Standing on one leg
inward or outward, oscillation and posture of
arms, asymmetry, posture of the spine, shoulders Task: stand on one leg for as long as possible.
and pelvis (stretch or flex), posture of the head, Then do the same thing with outstretched
associated movements. hands and finally with closed eyes. A 4-year-old
should be able to stand on one leg for at least
10 seconds.
Shoving on knees
Observation: asymmetries, constant asymmetrical
Observation: movement of the pelvis, ability to bent of the body to one side, regardless of the leg
stretch and flex the pelvis, movement pattern of engaged, synkinetic movements, e.g. closed hands
feet, lifting up of the lower leg, fixed posture of or hands in palmar flexion with extended fingers,
the head, associated movements. athetoid movements, posture of the uncharged
leg, ability to hold the balance, preference of
one leg.

Observation: asymmetries, especially with eyes

Jumping on one leg
closed, posture of spine and shoulders.
Observation: jumping on one leg, on the same spot
(for small children) and for children 4 years and
Alternation of the weight load on both
older we look at jumping on one leg backwards
and forwards.
Task: whi le kneeling, move the bottom alternately We look at the way of jumping and of charging
to the right and to the left. the foot. Does the child jump with a flat foot or
Observation: flexibility of the pelvis, posture of the does he bounce or walk on tiptoes; associated
body, the feet and lower legs, heel. movements, such as posture of head and shoul­
ders, integrating the hand and showing a mimical
reaction, on one or both sides.
Diadochokinesia exercise

Task: circle with the hand around your ""rist. 1his

movement is supposed to be quick and easy and
shows the ability alternately to supinate and pronate. Observation: posture of the upper part of the body,
Observation: isolated movements of the wrist, with­ tension of shoulders, lifting of shoulders unilater­
out engaging the rest of the arm, position of the arm, ally or on both sides, posture of the head, associ­
posture of the head and associated movements. ated movements of hands and fingers.

Thumb-Finger-test Heel-walk

Task: press y our thumb against each finger of the Observation: narrow or wide based, tension of legs,
same hand, backwards and forwards, with and posture of pelvis and body, moving the mouth,

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opening the mouth, tongue showing, posture of Then still st anding, turn head to the right a n d to
arms and hands, associated movements. the left, backwards and forw ards .

Observation: asy mmetries, does the head stay on a

middle-line while moving forwards and back­

Jumping jack
wards, do the hands stay in the same position
Task: s tretching the arms while straddle jumping and while the head is moving .

brin ging the arms back in aga in while jumping.

Observation: posture of knees, head, coordination. The ne x t test batte ry is done on the examination


Task: march, goose-stepping.

Sitting upright

Observation: movements of the arms, either reciprocal Task: sitting on a bench with legs stretched out.
or homony mous hand at the same time moving Observation: postu re of body, legs and feet, is the
ahead of the leg. child able to sit up straight alone, does he integrate
shoulder movements, lift ing up of shoulders,

Movements with both hands asymmetries, do legs and knees stay stretched,
abduction and bending of knee j o i nts, plan­
Task: sweep wi th one hand and tap with the other tar flex ion of feet, differences in effective len gth of
hand .
Observation: is the child able to do different move­
ments at the same time, nu ances of musc ul ar ten­
sion, nuances of the movement. Supine

Observation: asymmetries in posture of head, lor­

Standing dosis in the lumbar part of spine, difference in
effective length of legs.
Task: stand up straight, with hand stretched out in
Observation: posture of body, shoulders, head, asy m­ Lasegue
metries in posture and/or fo rward tilt of pelvis,
kyphosis, lordosis, side-bending of the spine, con­
Task: the examiner lifts up the stretched leg in
stant asymmetries, posture of feet, toes and knees.
Observation: bending of knee j oint to 90 degrees,
rotation of leg, asymmetries.

Task: bend body forward with stretched knees.

Suboccipital trigger points
Observation: s i de bend of the spine,
- distance
between fingertips and surface, development of Singly or bilaterally hyperesthetic evaluation of
spine, pain when the spine is tapped. the pain t hresho l d in the craniocervical area .

Romberg test Sitting with dangling legs

Task: stret ching out forward, hand and arms in Observation: post ure of body and head, asy mme­
su p ine position, with eyes closed and eyes open . tries, w e ight carried on both b uttoc k s.

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Manual therapy from a pediatrician's viewpoint 117

• signs of problems with the sensorimotor sys­

Flexibility of the tongue
tem, most often with a distinct 'sidedness'.
Observation: reaction of the pupils, nystagmus,
esotropia, eye movement while head moving In our experience it is often worthwhile to test
around, associated movements, integrated move­ the effect of manual therapy, even more so as the
ments in mouth area, lower jaw and tongue outcome can be evaluated after one, or at the most
movements. two treatments. We tried for y ears to develop a
score in order to have a simple tool for the evalu­
ation of candidates for manual therapy, but in real
life this does not work and the decision has do be
Symmetry of teeth, overbite, open bite, crossbite, done on a case-by-case basis.
prognathia, progenia, difficulty swallowing.

Case studies
Testing of auditory abilities

• Clapping: two beats, three beats, syncopes, Maik (age 8 years, 5 months)
longer sequences. The pregnancy was without pathological findings; the
• Nonsense verses: repeat for example, 'sim sal­ presentation was cephalic, right hand coming first;
abim bamba sal ad u .' there was extensive episiotomy because of narrowness
• Numbers: repeat: up to five numbers. of the birth channel.
Maik was very anxious as an infant, always kept
These tests are the standard procedure for almost all close to his mother and was often ill with infections
children and their documentation allows us to com­ of the upper respiratory tract.
pare the development of these children in compari­ Clinical findings: the traction reaction test showed
son with others of their age group, but also their delayed head control. At the age of 6 weeks the
individual development without manual therapy Landau reaction was still completely hypotonic. There
and later on when manual therapy was applied. were slight signs of a hemiplegia on the right side, the
Some of these children are presented in the fol­ Voj ta reaction on the right side was retarded, and
lowing case histories. there was retraction of the shoulders during the
By giving the following examples we would Landau test. He often cried during examinations in
like to demonstrate the connection between the the consulting room. Maik liked crawling and started
observations of development during the infant to walk after 14 months.
years and sensorimotor problems at school age. At the age of 4-5 the notes of the preventive
There is no such thing as a definitive test which medical check-up (U8 and U9) included the following
gives a clear-cut decision as to where to apply man­ entries: Maik showed conspicuous deficits in sensory
ual therapy and where not. Several factors influ­ integration and had problems with his proprioception
ence this decision, and these items have to be seen and balance. Nonetheless, he did not have any
and evaluated together. Three 'markers' stand out problems getting good grades in school, but he did
in this context: struggle on the social interaction level. Because of his
weak body posture, physiotherapy was prescribed
• problems during labor (which he did not like at all) . He even refused to swim.
• non-standard development during the first Examination at the age of 8: limited ability to turn
year, especially skipping of the crawling head to the left, limited head anteflexion, hypotonia
phase of the abdominal muscles.

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Line-walking: his legs were rotating outwards, crawl much, but started walking at the age of
without looking at the line, he made big steps with 1 year.
supporting steps in between, very unsteadily. Shortly after his fourth birthday (UB): weak balance
Standing on one leg was better on the right leg and problems with kinesthesia. He could only stand on
than on the left. With closed eyes he nearly one leg if he was holding onto something. He was just
stumbled. Examined in standing position, the able to jump on one leg one or two times and fell
thoracic area of the spine displayed a left bend with over doing the jumping jack test. Walking along the
counterswing at the lumbar level. Suboccipital pain line backwards was only possible for him by looking at
points on both sides. the line.
Because of his clumsiness and postural problems he At that age we prescribed psychomotor therapy.
was sent for examination (and treatment) by a A good year later he came for the next routine
specialist in manual therapy. check-up (U9): His general posture was hypotonic and
Three weeks after his treatment we examined he had problems balancing.
him again. Maik was much more relaxed and At the age of 6, he could not walk along the
more easygoing with his family and in school. He line without problems, legs were pointing inward. He
was less aggressive. His mother was delighted that had to 'feel' his way, especially with the left foot.
it was possible for her to hug her son for the first time. Standing on one leg was better on the right, as was
Maik's movement patterns were much smoother, jumping on one leg. He walked very clumsily, with a
his energy is much more focused now and he has got slapping movement of his feet. In standing, his spine
himself much better under control. He stops now as showed a left-side deviation in the thoracic region. He
soon as he gets tired and he is able to walk along the had difficulties sitting with his legs straight. In a sitting
line without looking at it. Although standing on one position he had a pronounced thoracic kyphosis. If
leg is still better on the right leg than on the left, his asked to sit straight, his legs were rotated inwards.
overall performance improved markedly. He still has a Hypotony of the abdominal muscles.
slight asymmetry and a weak posture. Changes after therapy: Florian now plays more
Conclusion: Maik's problem was his asymmetry independently, he has much more patience with his
and his weak posture. Lego. His hoarseness after kindergarten disappeared
and he can control his articulation better. Before he
Florian (age 6 years, 4 months) needed to build up his muscular tonus by shouting;
The pregnancy was without pathological findings; obviously he does not need this any more.
face presentation. The delivery was very quick, so
that the father nearly missed the birth. Afterwards Jonas (age 7 years, 1 month)
Florian suffered from colic with lots of vomiting, Jonas was a 'restless baby' during pregnancy so that his
regular respiratory infections with asthmatic mother could hardly sleep at night. The delivery took a
bronchitis, eczema, sleep disorders with trouble long time. Weight after birth was 4260 grams, height
falling asleep. was 59 cm and his head circumference was 37 cm.
At the age of 6 weeks, there was retarded head Jonas was already lifting up his shoulders while in
control on the traction reaction test, and retraction the incubator and he did not like to be touched.
of the shoulders on the Landau test. At the age of During his infant years he cried a lot. hardly moved
1B weeks, there was orofacial hypotonia on the and drank very hastily. He had to be carried around a
traction test and fisting on the Vojta test. The collis lot and the stroller had to be rocked almost
horizontalis test (to assess the reaction of the trunk constantly. Jonas was very demanding on his mother
and extremities when the infant is lifted) showed a and the rest of the family. His sister frankly said one
slight lateralization to the left. Later on he did not time it would be best to give him back.

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Manual therapy from a pediatrician's viewpoint 119

At the routine check at the age of 6 months he dyspraxia improved and he was able to concentrate
showed several signs of clumsiness, e.g. on the Vojta much longer. He has his hair longer now and does not
test and the axillary suspension. His period of crawling wear only black clothes anymore. At the school's
was very short, and he started walking at 9'12 months. sports meeting, he was the best of his school in long
At the age of 2 years his behavior was difficult and jump. And now he even thinks about joining the
often very aggressive; he often tumbled. He shouted soccer team.
frequently and had a very loud voice. Check-up 4 months later: standing on one leg is
At 3 years, he was still walking clumsily with a very absolutely fine and so is the jumping jack. He is able
stamping gait and a lot of associated movements. He to cross in the midline, his level of sensory integration
was very attached to his mother. In addition, he kept is completely age-appropriate now. The coordination
throwing himself on the ground in fits of tantrum. At of his movements is very good.
that age we started out with sensory integration He does not need any additional information
therapy, which could not be continued because of his anymore, like for example visual clues, higher
mother's new pregnancy. muscular tonus or other additional stimuli. A
A few months later at the routine check (U8): while slightly higher muscular tonus on the left side has
line-walking, his legs pointed inwards. He did not like persisted.
walking backwards. When asked to sit with his legs in Especially surprising is the success of the therapy
front of him, he was not able to sit straight. While regarding general behavior and complex movement
jumping on one leg, he pulled his knee up very high. patterns. These improvements were not achieved with
He had many proprioception difficulties. Even though any other form of therapy.
he started physiotherapy before going to primary
school he still had these difficulties, especially with Simon (age 15 years, 6 months)
memorizing certain activity patterns. Pregnancy and delivery were without pathological
Starting at primary school was a stressful time. findings, apart from the mother having insomnia
Intellectually, Jonas was absolutely ready to enter during the pregnancy. Up to the fifth month, Simon
school, but his sensory integration was not up to the did not move or turn around and he was very weak. In
exertions of school. Nonetheless, he got through the the traction reaction test the head control lagged
first year of school, but only with hard work. He was behind; in the Landau maneuver he did not straighten
very aggressive during that time at home. He was sad up completely.
about himself, cried a lot and also complained about During his sixth month his development speeded up
his dyspraxia. and he started to show signs of verticalization. He
Examination at the age of 7: He could not talk and started crawling at 8 months, and also started pulling
play with the ball at the same time. His way of doing himself up until he was able to stand up and slowly
the jumping jack was very uncoordinated. Walking started walking, but always had to hold onto
along the line, his right shoulder was pointing forward. something. At 10 months he was able to walk
He could only do it by looking at the line and only very independently. No asymmetries noticed.
fast. He stopped walking as soon as he hit something. At the U8 check-up, there were anomalies in doing
While standing on one leg, he lifted the other out to the diadochokinesia exercises and with standing on
the back, as though imitating an airplane. one leg. His anxious and jealous behavior was
The manual therapy started a few months later described as rather cute during his infant years and it
(two sessions). The changes in Jonas' behavior were was tolerated while he was in kindergarten. In school,
very impressive: he was now able to do two things at Simon became an outsider, was very lonely due to his
the same time. His movements became quicker and hyperkinetic behavior. He had no friends and was very
more fluent. He acted more spontaneously. His aggressive; he even hurt himself.

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He had a very bad reputation in school, the hemiparesis on the right side. She was prone to
teachers gave up on him and threatened to expel him tantrums, did not like to get dressed, but she liked
from school. Simon started psychotherapy, remedial to be touched.
education, and the family tried methylphenidate At t he age of 2, Elisabeth was still very anxious,
medication in combination with occupational therapy her lan guage development was retarded, especially
over many years. compared to other aspects of her development.
At the age of 15, Simon had an excessive thoracal Considering her personality as a whole, Elisabeth
kyphosis when sitting with outstretched legs, a seemed to be quite clever, even though she did not
misaligned spine and could not cross the middle line achieve 'good' scores in some of the tests.
in his movements. On examination a marked At 4 years, she only played by imitating others and
hyperesthesia on the suboccipital points came to was not very creative or very sensitive. She was scared
attention. of everything new, everything needed to be explained
His situation escalated when his half-brother to her. She had weak posture, she stood
committed suicide. Because Simon was in an identity knock-kneed and with a hollow back. There was a
crisis and he was suicidal, too, the parents planned to conspicuous Romberg reaction as she moved her
send him to a psychiatric hospital. arms when turning her trunk. She needed a lot of
Coincidentally, it was possible to apply man ual visual control and encouragement from her
therapy just before his hospitalization, which had to mother.
be scheduled a long time in advance. After one I examined Elisabeth again when she was in the
manual treatment his behavior changed completely. third grade of primary school. She had above all
He became much more talkative and easygoing. At problems with logical thinking. She was amazed by
home as well as in school, he became much more things whic h she should have known already. So
stable. He also now avoids contact with drug addicts. she was very inflexible, rigid, with a very constricted
This was a tremendous change, not only for Simon, train of thoughts. She had insomn ia (especially
but also for his parents, who were quite skeptical of difficulties falling asleep) an d hardly ever slept
the manual therapy at first. through the night. She was very unbalanced in her
It was the combination of his hyperactivity and eating habits and there were a lot of tensions
the persistently conspicuous findings during the during meals. Elisabeth had problems sharing things
routine check-ups which induced us to propose this with others and mostly kept the bigger part for
last-minute attempt. herself. At 83/4 she still needed a lot of motivation
from her mother.
Elisabeth (age 9 years, 4 month s ) Her posture was still marked by an excessive
Elisabeth is the fifth child in her family. The lumbar lordosis; balancing on one leg was much
pregnancy was quite complicated, because of easier on the right than on the left leg, as was
premature labor, pelvic presentation with rotation jumping on one leg. When doing the diadochokinesia
immediately prior to delivery. Weight after birth was exercises, she moved her other hand as well. There
3200 grams, height was 51 cm an d head was hypotony of the abdominal muscles. While sitting
circumference 34 cm. with straight legs, her back was bent in a dorsal right­
At the age of 6 weeks, respiratory infection with shift of the spine, and there were pronounced trigger
obstructive bronchitis began. At 9'12 weeks, a near SID points suboccipitally.
(sudden infant death): weak, cyanotic whining while Because of the difficulties in school there had
lying in face-down position in the stroller, apparently already been a psychological examination. Both of
found just in time. Elisabeth's parents were very skeptical about
Elisabeth cried a lot as an infant. Her muscular manual therapy, but as a last resort they agreed
tonus was low and there were sign s of a to it.

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Manual therapy from a pediatrician's viewpoint 12 1

After the manual therapy (two sessions) they percussion over the thoracic spine and at the
were very surprised how much Elisabeth's behavior suboccipital trigger points. While walking along the
had changed and how fast her attitudes matured. line, she dropped her left shoulder. Standing on one
Her mother described the changes as Elisabeth leg was better on her right leg than on the left;
being much more awake and open than before. jumping on one leg was still very clumsy. She could
Even her teacher at school noticed the only do the jumping jack after practising it a few
differences. times and even then she did it very slowly and stiffly,
At the neurological check-up, Elisabeth still had a with her mouth open. The thumb-finger test on her
slight difference of the muscular tonus and an left side was very weak.
asymmetry in her posture, but her improvement She started with the manual therapy at almost
continued. She graduated successfully from secondary 12 years of age. Within 4 weeks, she had changed
school without further intervention. completely. All of a sudden she was able to get up
Cone! usion: a II the symptoms, such as the early in the morning. She had more self-esteem.
asymmetry of posture, the restlessness, the details of Her writing was much better, she was not
the case history (near SIOS) and the weakness in her frightened of exams any more, and her grades got
posture, were symptoms of a functional vertebrogenic better. These improvements lasted without further
disorder - and the impact of the manual therapy therapy.
astonished everyone.
Sarah (age 6 years, 11 m o n t h s)
Kath ri n (age 11 years, B months) Sarah was the first child and the pregnancy was
Kathrin was the first child; her mother was early in inconspicuous. As the mother had an asymmetrical
labor and had to stay in bed to avoid premature labor. pelvis as a consequence of a car accident, a cesarean
Towards the end of the pregnancy the pelvic section was planned even though the child was in a
presentation turned into a face presentation. The normal position.
delivery took 5 hours; during the extrusion phase the After birth she cried a lot and had to be carried
mother had two to four travails. Weight at birth was around in a vertical position to soothe her, which was
3600 grams, her length was 53 cm and head so time-intensive that the parents took shifts. The
circumference 33 cm. diagnosis of a pes equinovarus led to the prescription
Kathrin was a very calm baby, and she slept a lot. of physiotherapy at the age of 5 months. She was
At 3 months, a tendency for fisting was noticed. On a very mobile child with a strong tendency
her baby pictures, Kathrin's head always tended to to verticalize. She crawled for only a very short
lean to the left, she had very big, open eyes and time and started walking at the age of 11 months.
enjoyed sitting up. From the beginning, Sarah had problems with
In kindergarten (5 years) she integrated a lot falling asleep which led to the establishment of
of mimic movements into her regular movements. elaborate 'sleep-rituals'; her linguistic development
Nonetheless, she had difficulties in understanding was rather delayed - 'she took her time'. As a whole
certain words and had a deficit in visual awareness, she appeared to be a bit behind in her general
especially in three-dimensional perspectives. development, active, but cautious and guarded.
Even though she got enrolled in primary school In kindergarten she had many friends and was very
a year later than usual, she still struggled. Her popular.
story-telling was sometimes incomplete, and she At the age of 5 another series of physiotherapy
was not very flexible. She had very low self-esteem. exercises was prescribed as her motor patterns still
At the neurological check-up at the age of 10, seemed to be a bit lateralized. In general her motor
Kathrin had asymmetry with left-side deviation of the development was described as clumsy, with a lot of
spine. She also had hypersensitivity to midline falling and stumbling.

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In primary school she tired quickly during lessons, the iliosacral and occipitocervical junctions. After
and after the third lesson she was hardly able to their removal the headaches subsided and the school
concentrate. Sarah had problems splitting her situation improved.
attention between two things. At the beginning she
wrote in mirror image, then from left to right, letters
as much as digits; in itially she had problems in STATISTICAL RESULTS
dealing with numbers up to 20.
At that point in time she was sent to a specialist Between 1996 and 1998 we examined 104 school­
in manual therapy. The radiograph showed a bifid children. All of them were examined and treated
arch of C, and the functional examination a with manual therapy. Out of these 104 children, 69
blockage at the level C,/C2. The ensuing manual showed a definite improvement, i.e. no more
therapy was administered even more carefully than treatment was necessary and they had a success­
usual. ful school career. They had clearly i mproved
A follow-up 1 year later showed a markedly when we examined them again at the neurological
improved situation with no signs of postural check up .

asymmetry. The situation in school was much more With 22 of the children we could not do the fol­
relaxed and her mathematical capabilities improved. low-up examination, because they never got back
Homework, before a big stress, was done well and to us.
without complaints. Thirteen children did not show any improve­
A year later she fell from her double-decker bed ments at all.
and hurt her neck. A short time later she complained All the children examined were conspicuou s
of headaches and a neurological and ophthalmological during their infant years: the y all had postural
examination was sought which produced no asymme t ry with either fixed lateralization or
pathological findings (EEG, CT, etc.). l\Jo further retroflexion of the head. We looked for signs and
treatment ensued. symptoms of functional v er te brogenic disorders
A few months later she came back to see me in the case histories of these children. This was the
because of the restlessness in her legs. She could not main clue for thinking of m an ual therapy as a pos­
find sleep anymore and complained of dysesthesia in sible solution to the children's pro bl ems .

her elbow and knees. Her father had a history of The cases presen t ed here are meant to give an
restless leg complaints. idea of which combination of anamnestic and clin­
The examination showed a marked hyperlordosis of i cal findings are suggestive of functional problems
the lumbar spine, a high muscular tonus of the pelvic of the vertebral spine as at least a contr i b uting fac­
area and a blockage of both iliosacral joints. There tor in a particu lar case. In almost every case, these
were no signs of irritation of a segmental nerve but verte bro ge nic problems were not the only on e s,
there was bilateral impairment of the Lasegue-sign often not even the most important ones. But their
indicating contraction of the hamstrings. The mother successful trea t ment gave these children more
reported that her handwriting had got worse and she room to maneuver and thus ena bled them to over­
had concentration problems in school. come their otherwise insurmountable difficu l ties .

The functional examination of the spine In all these cases, two to three sessions of manual
revealed - almost as expected - a blockage of both therapy sufficed.

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Manual therapy from a pediatrician's viewpoint 123


Allhoff P, Rennen-AILhoff B 1984 [Problems with Kilhnen H 1999 Erfahrungen mit der Manualmedizin in der
developmental diagnostic procedlliesJ. Monatsschrift neuropadiatrischen Landpraxis. In: Biedermann H (ed)
Kinderheilkunde 132(9):674-679 Manualtherapie bei Kindem. Enke, Stuttgart, p 187-198
Flem.ing J 1981 An evaluation of the use of the Denver VanDervoort R L, Lee E B 1984 Use of Denver
Developmental Screening Test. Nursing Research Developmental Screenin g Test. Pediatrics 74(3):445-446
30(5):290-293 Vojta V, Peters A 1992 Das Vojta-Prinzip. Springe r, Berlin

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Chapter 11 ------ �

The influence of the high cervical

region on the autonomic regulatory
system in infants
L. E. Koch

The craniocervical region plays a very important
Introduction 125
role in human ontogeny, especially in sensorimo­
Patients and methods 126
tor development. Disturbances of this region in
Characterization of the vegetative
infancy are manifold and their influence on the
responses 127
smooth progress of the biomechanical capabilities
Results 127
of the newborn can hardly be overestimated. It
Discussion 130
reaches far beyond the mobility of head and neck,
influencing basic regulatory mechanisms situated
in the brainstem (Ramirez 1998).
To distinguish between a purely central (neuro­
logical) and primarily peripheral (functional) eti­
ology is difficult. If a peripheral origin of the
pathology is established and the appropriate man­
ual therapy is applied to the upper cervical spine,
marked vegetative (autonomic) reactions can fre­
quently be observed. Alterations in the heart rate
and other vegetative reactions (flush, apnea and
sweating) were monitored after the application of
a unilateral impulse to the high cervical spinal
cord (manual therapy). One of the main benefits
of manual therapy in newborn babies is situated
precisely at this transition zone between motional
and regulatory control. A sound and undisturbed
sleep or a baby who does not over-react to any
unexpected sensory stimulus after successful
treatment - these effects show the impact of a dys­
functional craniocervical junction on the auto­
nomic regulatory system. In many regards, these
results of our therapy are more important to the

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child and parents than an improvement in the cause a bradycardia or other vegetative reactions.
range of head mobility. A mechanical stimulation of the atlanto-occipital
While treating the babies we encountered region is essential in manual therapy in newborn
sometimes quite intense vegetative reactions fol­ and the study of its effects on the autonomic sys­
lowing manipulation of the suboccipital struc­ tem could therefore provide insights into the age­
tures. Although we never saw any severe side dependence of these processes.
effects while manipulating babies following the A marked sensitivity of the atlanto-occipital
guidelines of the European Workgroup for Man­ region was first noticed during routine manual
ual Medicine (more than 20000 babies treated by therapy of newborn babies. This therapy included
our members - Schmitz and Ewers 2002), these an impulse applied to the atlanto-occipital region
reactions aroused our interest and we decided to which was often associated with vegetative
set up a study. responses. Our study included only infants that
U s ing observations from case reports, a system­ were diagnosed with asymmetries in the horizon­
atic study of these effects was designed. This tal and sagittal plane of body posture and motion
study is based on a survey of 695 infants between (Biedermann 1991, 1992, 1996, Buchmann et al
the ages of 1 and 12 months. A notable change in 1992). The diagnosis and therapy was performed
the heart rate was evident in 47.2% of all exam­ according to the guidelines set by the European
ined infants. In 40.1 % of these infants the change Workgroup for Manual Medicine (EWMM) and
in heart rate was characterized by a heart rate the German Society for Manual Medicine
decrease of 15-83% compared to control condi­ (DGMM).
tions. Infants in their first 3 months of life
responded more often with a severe bradycardia PATIENTS AND METHODS
(50-83% decrease), older infants (7-12 months)
more often with a mild bradycardia (15--49.9% We evaluated the impulse-induced changes in the
decrease). In 12. 1% (n = 84) of the infants the heart rate, the occurrence of flush and apnea in a
bradycardia was accompanied by a temporary group of children ranging from 1 to 12 months of
apnea. age. The study included only infants with the
We know that anatomical and functional mech­ diagnosis of KISS (365 males and 330 females).
anisms are involved in the development of dis­ The infants examined here were born between the
turbed postural and motor patterns and that these 28th and the 42nd week of pregnancy; 100 were
mechanisms have a specific component originat­ born before the 37th week (premature), 176 were
ing from the upper cervical spine. In addition to born after the 40th week of pregnancy. The weight
that we have a non-specific reaction which is char­ at birth ranged from l.3 to 5. 1 kg, and body size
acterized as a change in vegetative reaction pat­ from 41 to 57 cm. At the time of therapy the
terns. The quantity and quality of these reactions weight ranged from 4.0 to 11.5 kg, and body size
are difficult to define, but it seems probable that a from 59 to 80 cm.
mechanical irritation of the upper cervical region All infants showed some kind of deficits in neu­
serves as a trigger (a long-term potentiation (LTP) romuscular coordination as well as asymmetry
(Aroniadou-Anderjaska and Keller 1995) and has such as wryneck and C-scoliosis. Asymmetry in
great influence on the organization of optimal the atlanto-occipital CO/C2 region was determined
movement patterns, the development of sensory following X-ray examination using the technique
capabilities and the proper functioning of the described by Gutm ann and Biedermann (1984).
autonomic regulatory system. X-ray analysis revealed a slight predominance of
In this study we examined whether a mechani­ left-sided asymmetry (382 left, 313 right) in the
cal irritation of the atlanto-occipital region can examined infants. Those examined also showed a

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Influence of the high cervical region on the autonomic regulatory system 127

pathological pattern of neuromuscular develop­ The stable frequency at the beginning was defined
ment tests (Vojta and Peters 1992). One hundred as 100%. Change in frequency after impulse was
and twenty infants experienced an intrauterine measured and set in relation to the frequency at
mal-posture; 305 of the 695 infants had some sort the beginning. Changes of less than 15% were
of traumatic birth (vacuum extraction, forceps excluded.
delivery, Kristeller's maneuver, cesarean section, Mild bradycardia was defined as a decrease
prolonged labor, etc .); 83 infants suffered from ranging from 15% to 49.9% and severe bradycar­
developmental disorders of the hip and feet. dia, a decrease of 50.0% upwards. Parallel to these
Hypertonia of paravertebral back muscles was measurements we qualitatively observed also the
common (575 of the 695). Infants with neurologi­ presence of flush and apnea. A flush was defined
cal disorders were excluded from the study (idio­ as an increased blood flow resulting in an initial
pathic cerebral palsy, floppy babies, vitium cordis, facial reddening, which then spread further down
basilar impression, assimilation of atlas, or other to other body parts. A minor and localized red­
anomaly of the spinal column and spinal cord). dening of the cheeks was not considered a flush.
The therapeutic impulse used to treat KISS con­ Usually the flush occurred almost instantaneously
sisted of a short, gentle thrust administered onto following the mechanical impulse. A flush and the
the suboccipital region with the inner side of the crying of the infant was usually associated with
interphalangeal portion of the second digit. Rep­ the outbreal< of sweating. Sweating started in the
resentative impulses were measured as ranging head and then spread out from there to the rest of
between 30 and 70 N (Koch and Girnus 1998). It the body.
should be noted in this context that so far no seri­ Apnea (temporary respiratory arrest) usually
ous incidents have been reported (more than occurred with a delay of several seconds follow­
20 000 babies treated by members of the EWMM­ ing irritation of the high cervical region. For ethi­
Schmitz and Ewers 2002). cal reasons and because this study was strictly a
For the manual therapy the infants were posi­ by-product of chiropratic therapy we did not wait
tioned on their back while the chiropractor was for the spontaneous termination of the apnea.
sitting perpendicular to the child's head. Great Instead we restored normal breathing immedi­
care was taken that the infant was comfortable ately after the onset of the apnea by blowing air
before administering the impulse. The child's onto the baby's face. Therefore we defined apnea
body was relaxed and any rotation of the spine not as a cessation of breathing lasting for more
was avoided. The impulse was applied to the side than 8-10 seconds, but rather as a respiratory
of the asymmetry. arrest that exceeded the duration of one normal
breathing cycle (Ramirez 1998).
Characterization of the vegetative
In every case, changes in heart rate, blood pres­
sure, frequency of breathing, oxygen saturation AU infants (1-12 months) that were treated in Eck­
and the peripheral temperature were measured ernforde (Germany) for signs of KISS during the
using a standard monitor (Datex from Engstrom period from September 1998 to April 2000 were
Ltd). The frequency of breathing as well as the included in this study. No attempt was made to
peripheral temperature were often unreliable obtain an even age distribution for our study. As
because of movement artifacts. Therefore these demonstrated in Figure n.1A, the distribution has
values were not further evaluated and we concen­ a relatively sharp rise at the second month and
trated in this study on changes in the heart rate. starts to diminish after the sixth month, which

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reflects the age distribution of KISS cases in our onds, in rare cases up to 25 seconds, after which
consultation and may not be representative of the heart rate recovered to the same or higher fre­
occurrence of KISS elsewhere. The increased num­ quency than the initial heart rate.
ber of younger children in our study suggests that In the histogram shown in Figure 11.2 we plot­
these children suffered more severely from asym­ ted for all 695 infants the percentage heart rate
metry-related symptoms. Therefore they were changes. The changes were not normally distrib­
brought more often for treatment compared to uted. There was a high percentage of children
their older counterparts. Slightly more girls than with bradycardia, but there was no obvious popu­
boys were treated in the later months (9-12), but lation of infants that exhibited a tachycardia. The
otherwise there was no obvious bias in the gender average heart rate change was -14.1%. An
distribution (Fig. 11.18). increased heart rate of more than 15% occurred ill
Measurements of the heart rate were successful only 7.3% of the children, whereas 40.1% of the
in all 695 infants. In these children we compared children showed a heart rate decrease of more
the heart rate before (resting heart rate), during than 15%.
and following the impulse. Normally the brady­ Figures 11.3A and 11.38 show an example of the
cardia showed a standard curve: 2-14 seconds bradycardic responses to the manual impulse in
after the impulse there was a sharp decrease in one child. The child exhibited severe bradycardia
heart rate. The bradycardia lasted for 3-10 sec- (77.8%) and responded after 7 seconds. This
bradycardia was associated with apnea, flush and
loss of muscle tone for 6 seconds. The heart rate
recovered within 13 seconds.
As a next step we examined whether the occur­
80 rence of bradycardia was associated with a partic­
60 ular age. Figures 11.4A, 8 and C show the age
% distribution of all children who exhibited a brady­
cardia (>15% heart rate decrease).
The severity of bradycardia was assessed
O-+�--r-+-��-.�rL�,-�� for different ages by comparing the number of
1 2 3 4 5 6 7 8 9 10 11 12
A Age (months)


Girls Q:; 30
r---' r---
Z 20
% 50 -

r-rrr- -- r--
I----c 10

o -'---'L.UJ.Ll.l.I
1 2 3 4 5 6 7 8 9 10 11 12 -90-80-70-60-50-40-30-20-100 10203040

B Age (months) Percentage of heart rate change (%)

Figure 11.1 Age (A) and sex (B) distribution of the Figure 11.2 Distribution of percentage heart rate
infants in the study. changes of the infants in the study.

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Influence of the high cervical region on the autonomic regulatory system 129

Number of heartbeats
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45
O �������-+��r+�+-r+�+-r+�+-r+��




� 0.8

c: 1.2




Figure 11.3 Example of a typical bradycardia. A: ECG obtained from a 5-month-old infant born prematurely and
delivered by cesarean section. The child had the following clinical symptoms: asymmetry of motion and posture
(wryneck to the left, C-scoliosis to the right), hypertension in the back muscles, positive Galant sign on the left side,
Peiper-Isbert test positive, incomplete Vojta test to the left side, weak head control, circle-like loss of hair at the back
of the cranium. Drinking disturbance, slobbering. Diagnosis was confirmed with an X-ray (anterior-posterior) which
showed an offset at the level of C1/C2 to the right as referred to the occiput. Frequency before therapy was 150
heartbeats per minute. A moderate impulse was administered contralateral to the offset (in the left direction). During
the impulse the infant was lying in a supine position. It responded after 7 seconds with bradycardia (77.8%) which was
associated with apnea, flush and loss of tension for 6 seconds. Heart rate recovered to 165 beats per minute. B: The
heart rate reaction shown diagramatically.

occurrences of mild versus severe bradycardia in showed 0.196 wi th a significance of 0.0005;

children during their first 3 months (n =99) and Table 11.1).
in children aged 4-12 months (n = 180). This The occurrence of a bradycardia was often
comparison revealed a significantly increased accompanied by other vegetative responses, such
occurrence of severe bradycardia in the younger as apnea and flush. It was interesting tha t a com­
age group compared to the group of children bination of bradycardia, flush and apnea showed
older than 3 months (chi-squared of 9.87, df = 1 an age distribution similar to that seen in sudden
and a significance of 0.0017; the Kendall tau-b infant death syndrome (Fig. llAC).

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Table 11.1 Statistical data concerning mild/severe
bradycardia 80

Age of patients Mild Severe Total %
1-3 months 56 43 99
4-12 months 136 44 180 20

Chi-squared 9.B7, df 1, significance 0.0017.

= = =
Kendall tau-b 0.196, significance 0.0005.
2 3 4 5 6 7 8 9 10 11 12
= =

A Age (months)


The mechanical impulse to the suboccipital region
led in a significant number of cases to a decrease 60
in the heart rate (40.1%). The distribution (classes: 40
mild/severe) among the young infants (1 to 3 20
months) differs significantly from that in older
infants (4-12 months).
In the young infants the number of cases of 2 3 4 5 6 7 8 9 10 11 12

severe bradycardia is higher. Most bradycardia B Age (months)

led to a fast recovery which was associated with a
short period of tachycardia, suggest ing that this 100
sequence of events constitutes a normal and phys­
iological response to the mechanical irritation of
the suboccipital region.
The observation of this vegetative response 40
leads to an important safety issue. How safe is 20
manual treatment for young infants? The manual
therapy has proven to be a successful technique
2 3 4 5 6 7 8 9 10 1 1 12
which can be used to treat disorders, especially
disturbances of motor patterns of various etiology C Age (months)
(w ryneck C-scoliosis, irritation of the plexus
Figure 11.4 Age distribution of infants exhibiting

brachialis), sensorimotor disturbances of integra­ bradycardia. A: All bradycardia. B: Severe bradycardia.

C: Bradycardia combined with flush and apnea.
tion ability (retardation of sensation and coordina­
tion), as well as pain-related entities such as
excessive crying with '3 month colic' or hyperac­
tivity with sleeplessness. cessful method for treating such disorders. It is
In older children, disturbances of this kind are therefore increasingly popular as a fast and effi­
known as retardation of development in motor cient treatment.
patterns as well as in sensory abilities. The epi­ Although retrospective studies about complica­
derniological prevalence of such disturbances has tions in manual therapy are available for adults,
been estimated to be as high as 16.8-17.8% (Boyle no data for children are available. There is a need
et a1 1994, Goodman and McGrath 1 991) In many . for empirical analysis and if possible prospective
cases, manual therapy seems to be the most suc- as well as retrospective studies, but one has to add

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Influence of the high ce rvical region on the autonomic regulatory system 131

that no serious complications have been reported marked bradycardia than the older infants (fourth
up to now. Those members of the EWNIM special­ to twelfth month), who were more likely to exhibit
izing in the treatment of babies and infants report only a mild bradycardia. This finding indicates
about more than 20 000 children treated without that an irritation of the cervical region will more
serious complications (Schmitz and Ewers 2002). likely lead to a severe bradycardia in the first 3
We observed that the younger infants (first to months. All children treated recovered rapidly
third month) were more likely to respond with a «25 seconds) from the bradycardia.


Aroniadou-Anderjaska V, Keller A 1995 LTP in the barrel Gutmann G, Bieder m a nn H (eds) 1984 Die Halswirbelsaule.
cortex of adult rats. Neuroreport 6:2297-2300 Part 2: AUgemeine hmktionelle Pathologie und kl inische
Bieder m arul H 1991 Kopfgelenk-induzierte Synd rome . Fischer, Stuttgart
Symmetriest6rungen bei KJeinkindem. Kinderarzt Koch L E, Gimus U 1998 Kraftmessung be i Anwendung der
22:1475-1482 Impulstechnik in der Chirotherapie. M a nu elle Medizin
Biedermann H 1992 Manuelle Thera p ie bei KJeinkindem. 36(1 ): 21-26
Orthop Pra x is 28:380-385 Ramirez J 1998 The neuronal control of breathing: New
Biedermann H 1996 Kl SS- Kinder. Enke, Stuttgart insights and ex perimen ta l approaches with implications
Boyle C A, Decoufle p, Yeargin-Allsopp M 1994 Prevalence for the investigation of sudden infant death (SID). In:
and health imp ac t of devel opmenta l disabilities in US Satemus K, Kamirow S (eds) Sauglingssterblichkeit­
children . Pediatrics 93(3):399-403 PI6tzlicher Kindstod (SID), Schmidt-Rbmhild, Lu bec k ,
Buchmann J, Btdow B, Pohlmann B 1992 Asymrnetrien der p 53-65
Kopfgelenksbeweglichkeit von Kindem. ManueJle Schmitz H, Ewers J 2002 EWMM-Workshop Antwerpen .
Medizin 30: 93-95 Manuelle Medizin 40:253-254
Goodman J E, McGrath P J 1991 The epidemiology of pain Voj ta V, Peters A 1992 Das Vojta-Prinzip. Springer, B erl i n
in ch i ld ren and adolescents: a review. Pa in 46(3):247-264

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Chapter 12
------�-- ------�--��--�-��-

Attention deficit disorder and

the upper cervical spine
R. Theiler

In recent y ears there has been a notable increase in

CHAPTER CONTENTS work aimed at shedding light on attention deficit
disorder (ADD). Neurological examination, with
Evaluation 133
Investigation 134 particular attention to motor function, plays a fun­
damental part in such work, and includes the
Results 134
need to examine both body posture and the atti­
Discussion of results 136
tude of the trunk in detail.
KIDD 137
Even where there is no obvious evidence of
Case stud ies 139
abnormality, careful examination of preschool and
school-age children frequently reveals indications
of movement deficits of the upper cervical spine
consistent with kinematic imbalances due to sub­
occipital strain (KISS). Such findings are also very
frequent in children with suspected ADD or simi­
lar problems, primarily involving clumsiness of
gross motor function and, more especially, fine
motor function, difficulty in concentrating, and
functional and behavioral difficulties.
During the early stages of our observation of
child cases involving a combination of KISS and
ADD, manual medical treatment was given solely
to correct poshlral asymmetry. Following success­
ful treatment of KISS, we found in many cases that
improvement had occurred not only in those
aspects relating directly to the postural deficit, but
also in concentration and cognitive abilities.


These findings led us to explore what exactly was

being improved. We carried out a neurological

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motor examination and neuropyschological follow-up examination after manual therapy was
examination of children with suspected ADD. The clinical only; no radiological follow-up was per­
aspects considered in the neuropsychological formed.
examination were derived from various psycho­ Box 12.1 summarizes the components of the
logical screening instruments (Frostig, Mottier neurological and neurophysiological examina­
test, Wettstein logopedic language comprehension tions (tests). In addition to the tests listed in Box
test, etc.). Ruf-Bachtiger took, developed and 12.1, basal neural status was also examined.
applied various of these tests, creating an investi­ Social maturity / competence, impulsivity / sup­
gation procedure with 64 items (Ruf-Bachtiger pression of impulses, sustained effort, ability to
and Baumann 1997) which was relatively simple sustain attention, and ability to concentrate were
to use. The procedure for arriving at the ADD assessed as observation criteria for the purposes
diagnosis also made considerable use of the Con­ of these examinations, rather than by means of
ners questionnaires for parents and teachers (Con­ specific tests, and were included in the study as a
ners et al 1998), but these were not used in the means of judging the overall success of treatment.
subsequent evaluation of the success of treatment. The study was designed as a straightforward
When conducting the neurological examination, investigation. It was carried out in the context of
particular attention was paid in assessing body the normal day-to-day activity of a specialized
posture in relation to symptoms associated with pediatric practice. It was not possible to run a con­
KISS syndrome. trol group because of a lack of comparable placebo

Manual therapy was given to 48 children (aged
61/2 to 12 years, of whom 27 were boys) with ADD The results are summarized in Tables 12.1, 12.2
according to the DSM-IV criteria, and confirmed and 12.3.
KISS syndrome. Follow-up began by testing the
free mobility of the cervical spine, and then inves­
tigating those neuropsychological and neuromo­ Box 12.1 Tests (the items with an asterisk (0)
tor findings from the initial examination that were were validated for determining the age group)
not age-related. If the chnd had recouped the
developmental delay to a greater degree than • Tactile-kinesthetic perception: gross and fine
motor coordination, graphomotor test'.
could be accounted for by the time lapse since ini­
graphesthesia imitation, graphesthesia choice·,
tial examination, or if the child's performance had Affolter tower
become normal for his or her age, this was evalu­ • Visual perception: reproduction of forms, dot
ated as improvement. The time intervals varied picture', vexing image, grasping of
because in many cases differing amounts of time simultaneously presented points', imitation of
point sequences', building after a photographic
were needed between initial examination and the
example, mosaic dice·, discrimination test
successful conclusion of manual therapy. The clin­ figure-background (Frostig 7a/8a', recognizing
ical diagnosis of KISS was based on segmental a fingerprint, Lang stereotest I I), Visus testing
testing of cervical spine mobility. The radiological • Language perception: repetition of nonsense
examinations consisted of Gutmann-Sandberg syllables', choice of nonsense syllables',
anteroposterior radiographs of the atlanto-occipi­ repetition of sentences
• Acoustic perception: imitation of tonal
tal area and conventional lateral radiographs of
patterns', if necessary audiogram
the cervical spine (see Chapters 18 and 19). The

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Attention deficit disorder and t he upper cervical spine 135

dren accepted into the study were performing at a

Table 12.1 Results of the neuropsychological
examination before manipulation (N 48) =
level appropriate to children 2 or more years
below their actual age.
Before manipulation: deficit in Abnormal performance was mainly found in
years/number of children items involving tasks that called upon several dif­
Impairment >2 years > 1 year <1 year ferent modalities. Performance was most nega­
tively affected if they were related to verbal, visual
Tactile-ki nesthetic 20 12 16
Visual 20 15 13 and tactile-kinesthetic perception (in that order),
Verbal 25 17 6 and least affected if they related to acoustic/ audi­
Acoustic 6 9 33 tory perception. All the children had difficulty
For the examination techniques used, see the corresponding with motor coordination, but a majority were
section in the main text. found to have retardation amounting to less than
2 years in this area.
The results were particularly striking for
For the purposes of the study, the diagnosis of items in which the information perce ived then
ADD involved retardation in two or more fields of had to be translated into motor activity: repeti­
perception in the neuropsychological examination tion of nonsense syl lables (Mottier test, modified
(Ruf-Bachtiger 1995, Ruf-Bacht iger and Baumann by Ruf-Bachtiger), gr ap hesthesia imitation, and
1997). A deficit of up to 1 year was regarded as still the imitation of series of dots. Marked retarda­
being within the normal range, so that the chil- tion in these items is often found in ADD, as

Table 12.2 Results of the neuropsychological examination after successful manipulation (children with
deficits of >2 years - first row of Table 12.1)

After manipulation: deficit in years/number of children

Impairment Before manipulation on >2 years >2 years >1 year <1 year Normalized

Tactile-ki nesthetic 20 4 10 5 1
Visual 20 3 7 5 5
Verbal 25 4 6 10 5
Acoustic 6 2 3 0

Table 12.3 Results of the neuropsychological examination after successful manipulation (children with
deficits of 1-2 years - second row of Table 12.1)

After manipulation: deficit in years/number of children

Impairment Before manipulation 1 -2 years > 1 year <1 year Normalized

Tacti Ie-kinesthetic 12 4 6 2
Visual 15 3 8 4
Verbal 17 3 9 5
Acoustic 9 5 3

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these tasks demonstrate particularly clearly any A number of children who were not thereafter
difficulties in the processing of information. included in the study later showed deterioration
However, these three tests were also the ones in some or all areas that had previously been
that showed the best response to manipulation. abnormal. A recurrence of KISS was found in all
The performance of some of the children was but a few of these cases. The improvements
normal after manipulation therapy (Tables 12.2 recorded previously returned after manipulation
and 12.3). Differences were most often evident in therapy was repeated.
the modified Mottier test and imitation of series After the first follow-up tests to the manipula­
of dots. Ten children with reduced visual concen­ tion therapy, the impreSSion grew that younger
tration span had reading difficulties. Following children were deriving more benefit from the
completion of manipulation therapy they treatment than older ones. However, at the end,
achieved an oral reading fluency appropriate for the percentage of successful treatments was
their age, usually in the days immediately follow­ roughly equally distributed across the age groups.
ing therapy. These children in particular reached The proportion of children between the ages of
a normal level of achievement in all the tasks that 6\1, and 8 was greater, but this was not statistically
demanded normal visual intake capacity. significant in view of the small numbers
It appears from the results obtained that a involved.
small proportion of the children (7 out of 48) were
exhibiting considerable negative effects due to the
atlanto-cervical misalignment alone. Following DISCUSSION OF RESULTS
manipulation therapy they performed normally
in everyday situations, achieving levels at least One of the main findings of the neuropsychologi­
appropriate to their age in concentration, sus­ cal examination in ADS is the reduced capacity for
tained effort, and control of impulses, and also processing information (Miller 1956); there is a
(for the most part) motor function. Following reduced intake concentration span in two or more
manipulation therapy, their concentration span fields of perception. This is an expression of defi­
was completely normal. ciencies in executive functions, which are carried
In the neurological examination we found an out in the dopamine-dependent structures of the
improvement in coordination, with more pro­ frontal lobe and corpus striatum and its links to
nounced improvement in gross than fine motor the limbic system. The reduced capacity for pro­
function. This correlated with the findings in the cessing information also affects the direction of
graphesthesia imitation test, where the retardation impulses. The reduced ability to perceive or take
in performance decreased by at least 1 y ear. in information makes it impossible to achieve the
Overall, no marked improvements in results periods of concentration and sustained attention
were found for acoustic/ auditory perception fol­ appropriate to the age of the child.
lowing manipulation therapy. According to this study, the main result follow­
Parents reported that in general the children's ing successful manipulation therapy for KISS was
ability to concentrate, sustained effort, ability to an improvement in intake concentration span,
sustain attention, and impulsivity had improved especially in verbal and visual perception. The
considerably, and that their children seemed deficit in terms of age usually diminished within a
'more mature' ('less childish'). The follow-up tests short period by several times the measured inter­
tended to confirm this, with the children working val between treatment and follow-up examina­
more quickly and confidently. More detailed tion. The progress could not therefore simply be
quantification of these observations was not car­ due to maturation of the brain. Some of the chil­
ried out, for the reasons given above. dren recovered 2 or more years' performance

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Attention deficit disorder and t he upper cervical spi n e 137

deficit in the course of a few weeks or months, tative improvement in the processing of informa­
while the majority achieved a smaller but still con­ tion received.
siderable degree of improvement. Parents reported In the present study the clearest differences in
that these improvements were often already findings occurred in those items of the examina­
observable in everyday life on the day that manip­ tion that required information to be processed
ulation therapy had taken place, or within a using a variety of modalities. In these tests, sen­
few days. sory information had to be translated into the per­
The model of the 'capacity for processing infor­ formance of a motor task: repeating sounds,
mation' offers an explanation for this improve­ drawing series of dots, or tracing out with the fin­
ment in cognitive performance through orthopedic ger a line traced on the back of the hand (graphes­
treatment. This assumes that the brain has a set thesia imitation). An everyday example of such a
capacity to process information, and that this difference was that the reading performance of
capacity must be available if it is to process the children with difficulty in reading aloud became
information received through the various means normal in what was for the parents an astonish­
of perception. This capacity can be compared to ingly short time.
the processing memory of a computer in that it On the other hand, the developmental deficit
limits in just the same sort of way the amount of before and after therapy was considerably less in
information from all areas of perception that can procedures requiring choice (and sometimes was
be processed. This means that it determines how not demonstrable at all). To perform these proce­
well and how quickly the constant stream of stim­ dures correctly, the children needed to show good
uli of perception can be translated into appropriate perceptive ability, but the demands placed on
action. their capacities appear to have been less if all the
As with an overloaded computer memory, so in children had to do was to identify differences
ADD with kinematic imbalance-related dys­ between pieces of information they had heard or
praxia/ dysgnosia (KIDD) only part of the body of felt.
information is processed at the required time, For the majority of the children, KISS caused a
leading eventually to the moment of total over­ considerable limitation of information processing
load with decompensation due to excessive capacity; more importantly, this was an additional
demand. limitation of capacity. Manipulation therapy helped
In the combination of KISS and ADD, the child these children to some degree, but did not funda­
has a further overload factor: in addition to hav­ mentally improve the underlying problem. T hese
ing a 'processing memory' that is too small for its children therefore needed further types of treat­
age, the child has to correct the information dis­ ment, in most cases medical stimulant therapy
torted by the malpositioning of the head, and this together with supporting therapy for motor
corrective work probably plays a decisive role. function or behavior.
This malpositioning means that visual informa­
tion is received crookedly, and either the infor­
mation has to be straightened out in the system of KIDD
visual perception, or the position of the head must
constantly be corrected by controlling the angle of If they remain untreated, infants with KISS grow
the trunk, both solutions requiring information into children with KISS, with more or less pro­
processing capacity. Successful manipulation ther­ nounced associated symptoms. They exhibit not
apy brings head and trunk correction back within only problems of posture with neck and / or back
normal range, freeing up capacity to be used for pain, but further difficulties that cannot be clearly
cognitive processing and bringing about a quanti- traced to posture. These mainly involve motor

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clumsiness of varying severity, ranging all the therefore provides a method of distinguishing
way up to ataxic movement disorder. The main 'KIDD' (Biedermann 1999) from 'KISS with ADD'.
problem is motor coordination, in particular fine This in turn means that these children can be
motor function, with difficulties in graphic motor helped without recourse to drug treatment, while
function. Other problems include variable concen­ the others can be helped by long-term therapies.
tration ability, which understandably results in In its various degrees the pattern of symptoms
variable performance at school and in everyday that appears in children with KIDD is often diffi­
life (behavior). Inconsistency in intensity is a par­ cult to differentiate from the problems of chHdren
ticular feature of behavior. The form taken by the with ADD. From our experience as described
behavioral difficulty depends on the individual above we have developed the following procedure
child, but seldom varies for any one individ­ for examining children with ADS (Fig. 12.1):
ual. Observation shows that decompensation may
be aggressive, destructive or resigned. If the symptoms of ADD are accompanied by
If the difficulties in behavior and perception are limited movement of the cervical spine
caused by poor positioning of the atlanto-cervical attributable to KISS, the manual medical
joint, we apply the description 'kinematic imbal­ therapy procedure is followed (radiological
ance-related dyspraxia / dysgnosia which is suboc­ examination and manipulation therapy).
cipital in origin' (KIDD). Follow-up takes place about 4 to 8 weeks
The possibility that children whose cognitive after manipulation therapy. If that examina­
performance becomes normal after manipulation tion reveals normal mobility of the cervica I
therapy might be suffering from an associated spine ('suboccipital region normal'), we eval­
dopamine deficiency of the frontal lobe and uate the effect on the ADD symptoms and
frontal limbic structures is remote. Such therapy discuss the implications for subsequent

Rx cervical spine Manipulation Control mobility

Yes a.p. and lateral C,/C2 (HIO) cervical spine



Yes KISS persists?


Therapy No

Yes No
ADD symptoms

Figure 1 2.1 Diagnosis and therapy of KISS and ADD.

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Attention deficit disorder and the upper cervical spine 139

therapy. If it reveals further abnormality, we and the muscular force insufficiently measured out.
recommend that manipulation be performed Finger-thumb opposition was clumsily achieved
a second time. and accompanied by tonic contralateral
If the suboccipital region is normal and the ADD Neuropsychological findings were as follows: if not
symptoms have either disappeared or been occupied she was constantly moving around; while
reduced to a minimum, this is interpreted as KIDD. solving problems she became momentarily more calm,
If ADD persists when the suboccipital region is nor­ but this did not l ast long and she got increasingly
mal, we describe this as ADD with KlSS. fidgety. Her concentration span was short and she
was very impulsive in tackling the assigned tasks. Her
behavior got increasingly evasive with the mounting
Case studies degree of difficulty of the job at hand. She tired
A.M. (female, 7 ye a rs 2
, months) Imitation of body posture was imprecise on the
Pregnancy was uneventful, with a fast spontaneous right side, and appropriate for her age on the left. She
delivery at the expected date with a birthweight of was unable to solve the graphesthesia imitation test
3300 g and a l ength of 47 cm. (devel opmental age less than 5 years). repetition of
The initial development was inconspicuous: she nonsense syllables succeeded for groups of 3, was
walked at her first birthday, spoke her first faulty in 4-5 (phonetic reproduction) and groups of 6
sentences at her second birthday and had no major syllables could not be reproduced at all. Repetition of
accidents or operations, apart from a fall from a sentences with complex content was incomplete.
swing. Imitation of lines of points, differentiation of
The diagnosis of attention deficit hyperactivity figure background and perception of forms was
disorder (ADHD) was made by a regional center for performed according to age, and acoustic perception,
pediatric psychiatry: there was a very variable level of too.
concentration depending on her interest in the topic Our diagnosis was ADHD.
at hand, sudden changes of mood and low frustration Functional examination of spine revealed a marked
threshold. She showed possessive and dominant impairment of the inclination of the head to the right
behavior while playing and in the classroom, and the rotation to the left with a blockage of (1/(2
disturbing other children or clowning around in on the left as well as a blockage of the left SI joint.
stressful circumstances at school or in private. As she The cervical spine was in a right convexity and the
showed insufficient gross and fine motor functions, thoracic spine in a left convex posture. Pelvis and
too, the psychotherapy was combined with a shoulders stood horizontally. The radiograph showed a
psychomotor therapy. She was referred for our hyperextension of the cervical spine and a
consultation because of a persistent postural lateralization of (1 and (2 to the left.
asymmetry after 1 year of this therapy schedule. Treatment consisted of (1/(2 left (impulse
On clinical examination, we found a normal technique).
muscular tonus; lively and symmetrical muscular In the fol l owing 3-4 days the girl complained of
reflexes without pyramidal signs. In testing tiptoeing giddiness. Shortly afterwards the family remarked that
and walking on the heels, the synkinesis of the arms her gait and posture became straighter and more
was notably awkward. Walking on a line was harmonious; motor coordination improved.
performed clumsily; she put her feet next to the line Three weeks after the treatment the girl was
and tiptoed intermittentl y. In the one leg standing examined again. In the motor tests she showed
test the arms were used excessively to sustain marked improvement while still having difficulties
balance. Jumping and clapping was uncoordinated, walking on a line. Bimanual coordination improved,

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though with inadequate control of power. Jumping birthweight of 3750 g, and a length of 48 cm. Her
was now performed effortlessly. mother said that she was somewhat lazy drinking
The neuropsychological tests still showed a short while being breast-fed, and when she was older
attention span, some impulsiveness in the search for always ate only what she felt like.
solutions and much less evasiveness with improved At examination she appeared to be a bit
perseverance. Memory span and processing capacity overweight. The psychomotor development appeared
for tactile and kinesthetic tasks was at a level of 2 to be age-appropriate. Already at the age of 4, her
years less than her age, but verbal capacities were clumsiness had been remarked. The development of
now normal and the visual component better than an her drawing lagged behind, with scribbling at the age
8-year-old, i.e. '-2 years advanced in comparison of 5, and simple 'head-and-feet' figures at the age of
with her age group ( Fig. 12.2). 6. Remedial education was applied for the second
Two years later the family contacted us again as kindergarten year for 1 year. She could not use
her behavior showed a relapse with increased scissors properly or fasten her shoes. Concentration
impulsiveness, worsening of the always problematic span for things she was interested in was very good
concentration span and increased distractibility. In the and it was almost impossible to divert her, but she did
meantime, an examination in pediatric psychiatry had not have much stamina, especially for unfamiliar
shown her to be highly gifted. We found a recurrence tasks, and she was prone to retreat when confronted
of a cervical blockage and the consequent with frustrating experiences or failure. She had
reoccurrence of the KISS symptoms. After the difficulties sticking to the rules.
successful removal of the functional cervical disorders, Clinical examination showed a chubby child with a
her concentration span and control of her impulsive reduced muscular tonus and normal and symmetrical
behavior improved again and her integration in the reflex behavior, and no pyramidal pathology. Gross
peer group was facilitated. motor function was slightly disturbed. Jumping on one
Her performance in different tests in comparison to leg was impossible for her. Fine motor tasks were
the age average is shown in Figure' 2.2. tackled with difficulty and tactile and kinesthetic
processing was at the level of a 5-year-old (i.e.
W.S. (female, 6 years, 5 months) retardation of '8 months) .
Pregnancy was normal. She was born in the 42nd Neuropsychological findings showed a calm,
week with a clavicle fracture intrapartum, with withdrawn girl without too much energy. When the


o Age average
• 1st examination

6 o 2nd examination

3 -j''--'---

Figure 12.2 Case A.M.: performance in different tests in comparison to the age average .

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Attention deficit disorder and the upper cervical spine 141

tests got more complex she became more impulsive, A.K. (female, 11 years,S months)
and lost concentration and perseverance. Memory This girl was examined shortly before she was to enter
and processing capacity in all areas of perception high school ('Gymnasium'). Since her fifth school-year
was 1.5 years below age average. Raven Colored it had become increasingly evident that she had
Progressive Matrices (CPM) corresponded to an age trouble delivering consistent results in her tests. Even
of 8.4-9.0 years. Summary diagnosis: ADD, accomplishing sufficient results to ensure her
inattention variant. 'survival' in primary school seemed to be imperiled.
Functional examination of the spine revealed This compelled the parents to seek an evaluation as to
impaired side-bending of the head on the right side whether or not ADD-related problems were
and reduction of the rotation on the left. In the contributing to these difficulties.
sitting position, there was excessive thoracic kyphosis The girl's situation in school was characterized
with reclination of the head. The orthopedic status by concentration problems and a lack of long-term
was otherwise unremarkable. The radiograph showed attention to a given topic. In mathematics, for
a lateral displacement of C1/C2 to the right. example, she had mostly very satisfying results with
Treatment comprised manual therapy combining a quite a few bad grades interspersed. With
sagittal impulse on C1 and a HIO C1/C2 from the right languages she fared even better and here the bad
side (impulse manipulation). results were less frequent. Her behavior in school
Two months after the manipulation, the child came and at home was in accordance with her age and
back for a check-up just after her seventh birthday. her contact with her peers unremarkable - with the
The mother reported no change in any aspect. normal pre-puberty edginess.
The head movements were now completely The neurological examination showed a normal
unhindered. muscular tonus, lively and symmetrical spinal reflexes,
Neurologically, there was no significant and no signs of pyramidal disorders. Gross motor
change, albeit a few minor improvements (she was capacities were normal; fine motor coordination
able to jump at least a bit on one leg now, degraded with increasing speed. The graph motor
for example). performance showed a similar pattern: initially normal
Neuropsychologically, she showed a more and with a harmonious grip of the stylus, the grasp of
considered way of working and was less impulsive. the pen became more tensed with speedier writing
She was able to criticize and correct completed tasks and the pressure on the paper more pronounced.
and she could concentrate for longer. Visual memory Neuropsychologically, she cooperated well
and processing capacity were still 6 months below throughout the entire examination. The rate of errors
her age, tactile-kinesthetic processing and increased with the time it took to accomplish a test,
three-dimensional orientation 1 year below her age, even if the level of testing was lowered. When trying
and verbal memory now on the level of a 9-year-old to solve a more difficult task she showed more
(+2 years). impulsive behavior and had more problems in noticing
Comparing the two test results, it is clear that the and correcting her mistakes.
girl had managed to catch up with her age group. In In copying lines of dots and in repeating nonsense
some aspects (e.g. visual performance) she was even syllables, her performance was at the level of an
able to outdo her age group considerably. Comment 8-8'h-year-old. The dice mosaic was copied with
from the mother (after having compared the test some effort, and losing track, she had to solve this
results): 'It seems to have been effective anyway, task bit by bit. Tactile-kinesthetic perception and
after all!' processing were age-appropriate.
Further therapy involved psychomotor therapy. The clinical picture showed a scoliotic posture with
Her performance in different tests in comparison to a cervical-thoracic left convexity and a counterswing
the age average is shown in Figure 12.3. at the thoracolumbar level. The pelvis was in a

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10 -,------

9 �------_,_.-

8 �------�

7 �------�1r--�,_r_,_--_1_,

Tactile-kinesthetic Visual Verbal 3D-orientaton

Age average at D Age average at

• 1st examination D 2nd examination

Figure 12.3 Case WS.: performance in different tests in comparison to the age average.

horizontal position with a blockage of the right The mother wanted to resume the medication
SI joint. anyway, hoping to further improve the situation.
The head-tilt to the right was impaired and on the After 4 days the course of medication was stopped
segmental level C1/C2 blocked on the right side. The as it did not result in any perceptible gains. Th ese
radiological examination showed an offset of the atlas improvements lasted well into the new school year,
to the right. and she was able to function satisfactorily in the
We interpreted these results as an attention deficit new school with grades a bit under the class
disorder with reduced impulse control, but without average.
hyperactivity. This case study shows how KISS can lead to an
As the imminent change of school seemed to be impaired level of attention and execution typical for
endangered, the family decided to use Ritalin therapy. ADD. We have not yet found reliable tests to
The performance in school stabilized immediately and differentiate between cases of ADD with and without
her grades improved markedly. The teachers felt that a cervical factor. It is often in combination with
she gained self-assurance and stability. reduced executive capabilities that we see difficulties
During the last weeks of the school year, the of coping with conflicts which may lead to behavioral
manual therapy was applied, based on the radiological disturbances and phobias, in milder cases to impaired
examination (i.e. C1 R). After this manipulation the self-confidence.
SI joint regained normal mobility without direct As in this case, we are in favor of examining and
manipulation. Simultaneously the medication was treating functional problems of the (cervical) spine in
stopped. these children, especially after we found signs of
After a week the girl said spontaneously that she postural asymmetry of movement restrictions, even if
did not think she would need Ritalin any more. a pharmacotherapy seemed to have already resolved
Now she was able to function normally in school and the problem at hand.
she was able to do her homework without problems.

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Attention deficit disorder and t he upper cervical spine 143


Biedermann H 1999 Yom KTSS zum KIDD. In: Miller G 1956 The magical number seven, plus or minus
Manualtherapie bei Kindem. Indikationen und t.vo: some limits on our c apa c i ty for processing
Erfahrungen: ein Q ue rsc hni t t. Enke, Stuttgart information. Psychological Review 63:81-97
Biedermann H 2001 K I SS Ki nder. Enke,
- Ruf-Bachtiger L 1995 Das friilikindliche psychoorganische
S t uttgar t Synd rom: Minima Ie ze rebral e Dysfunktion; Diagnostik
Conners C K et al1998 TIle revised Conne rs Parent Rating
' und Therapie. Thieme , S t u tt gar t
Scale (CPRS-R): factor structure, reliability, and criterion Ruf-Bachtiger L, B a u mann T 1997 Neuromotorische­
validity. Jo u rn a l of Abnormal Child Ps ych o logy neuropsychologische U nters uch un g des gesunde n Kindes
26(4):257-268 (Course in examination methods CD-ROM). Thieme

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Chapter 13��--�----���--�-�-

Asymmetry of the posture,

locomotion apparatus and dentition
in children
H. Korbmacher, L. E. Koch, B. Kahl-Nieke

Perfect symmetry of the body is Lmcommon in

CHAPTER CONTENTS nature. In a st u d y of children aged 9-18 years, who
Animal experiments 146 clinically did not reveal a facial asymmetry, Vig
Diagnostic records 147 and Hewitt (1975) analyzed the posterior-anterior
Orthodontic records 147 cephalograms. Astonishingly, the cephalometric
Radiographic examination 147 analysis revealed an overall asymmetry in most
Clinical examination 147 children, indicating that the left side of the face
Examination of the soft tissues 149 was generally larger than the right.
Orthopedic records 149 FLmctional and morphological asymmetry is to
Review of orthodontic discrepancies in children some extent physiological. Pirttiniemi (1994) differ­
wit h orthopedic disorders 150 entiates normal craniofacial asymmetry into normal
Sa gittal plane 150 asymmetry of a directional or fluctuating nature.
Vertical plane 151 Directional asymmetry can be fOLmd in the ante­
Tra nsversal plane 151 rior/posterior, the cranio/caudal and left/right
Scoliosis a nd tortico lli s 151 dimension. Asymmetries in the anterior/posterior
General orthodontic fi nd ings 152 and cranio/caudal dimension are embryonically
Atlas deviation 153 rooted and thus a result of the asymmetry in the
Soft tissue 153 central nervous system (ZiUes et aI1996). Advances
Interdisciplinary trea tment approach in children in molecular genetics suggest a genetic backgroLmd
with KISS syndrome 153 for lateraJity (Collignon et al 1996). Examples of
Interactive system of functional boxes 154 directional asymmetry are the asymmetrical struc­
Conclusion 155 ture of the brain, a consistent laterality in internal
Glossary 157 organs and left/right handedness. Another type of
asymmetry is the fluctuating asymmetry that is
related to stress (Siegel and Doyle 1975). Genetically
coded tissues such as the enamel of teeth are most
often affected (Manning and Chamberlain 1994).
One of the major etiological causes of asymmetrical
orofacial findings is the side difference in muscular
function. The latest scientific data shows that den­
tal occlusion is an important factor in symmetrical

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development of facial structures in early life specialization in medicine led to a focus on the
(Bishara et al 1994, Kiliaridis et al 1996a, 1996b, discipline's characteristic features and the overall
Raadsheer et aI1996). understanding of the chain of events is often
How is asymmetry defined? In clinical terms, missed.
symmetry means balance whereas an imbalance As an anatomically and functionally complex
of a system results in asymmetry (Pirttiniemi system, head and vertebrae have been the focus of
1998). A similar viewpoint is described by Rude scientific interest (Christ 1993, Gutmann 1981,
(1987) who examined 500 skulls in terms of asym­ Ridder 1998). Studies of this interdisciplinary
metric structures. Under normal conditions, many issue have been carried out for more than 6 cen­
different factors influence the morphology of the turies. But a clear statement of the relation
skull. These factors can be divided into three cate­ between orthopedic and orthodontic disorders is
gories such as forces driving from the vertebral still missing. Most studies are based on clinical
column, especially the occipitocervical region impressions and have anecdotal features. Only a
(OCR), cranial factors and environmental local few controlled studies exist so far. Some cephalo­
factors such as tongue, adenoids and perioral metric studies have shown that anatomical fea­
muscles. Under physiological circumstances, all tures of the craniocervical junction are associated
three categories of forces form a balance of power. with head posture, mandibular growth and angu­
Under pathological conditions one group gains lation of the cranial base.
more influence than the others and the balance of In general, there seems to be an association
power is destroyed. Imbalance and asymmetry between Angle class II - i.e. distal position of the
occurs. mandible in the skull - and lordosis, as well as a
The idea of an interdisciplinary treatment is one high incidence of lateral crossbite in patients with
of early prevention (Huggare 1998, Pirttiniemi et scoliosis and torticol1is.
al 1990). Recent scientific data shows that apart
from genetically rooted development, muscular
balance and dental occlusion are the keys of a nor­ ANIMAL EXPERIMENTS
mal symmetrical development of orofacial struc­
tures. In addition to the support of the trunk The results of experiments with guinea pigs and
muscles, head posture is the result of a complex rabbits suggest interaction between occlusal
muscle system that includes the lip muscles and plane, craniofacial growth, head posture and car­
the hyoidontic motor system (Aragao 1991). The diac function. Unilateral grinding of the occlusal
postural muscles contribute to the tension and plane evoked changes in the posture of the upper
function of the orofacial and deglutition muscles. cervical spine as well as many reactions of the
Based on this muscular interaction the logical con­ motor and autonomic nervous system. The
sequence is a contribution of the muscles of the changes observed were an abnormal mobility of
craniocervical region to facial development. the tongue, a different posture of the cervical
Besides the preventive character, the motivation spine, loss of hair as well as changes in the ECG in
of interdisciplinary cooperation between orthope­ terms of an inverted T wave (Festa et al 1997).
dists and orthodontists is to optimize the treatment Those changes became evident one week after
results and to avoid relapse. Relapse is one indica­ unilateral manipulation of the vertical plane. The
tor of an incomplete diagnosis (Balters 1964, Rude evoked reactions normalized after the reconstruc­
1987). Delaire (1977) interpreted a relapse of an tion of the original occlusion plane (Azuma et al
orthodontically corrected mesial position of the 1999). These results indicate that changes in the
lower jaw as the result of a therapeutically neg­ dental occlusion interact with the masticatory
lected cervical lordosis in the patient. Further muscles and head posture as well as the trigemi-

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As y m m e try of the postu re. l oco m ot i on a n d d entit i on in c h i l dre n 147

nal system that controls heart and wellbeing. Fur­ jaw. After drawing references points and planes,
thermore dental occlusion is one cofactor of cran­ intersectional relations between occiput, atlas and
iofacial growth. As Poikela et al (1995, 1997) axis were taken.
proved, unilateral masticatory function caused In a cervico-cephalometric examination Hirsch­
asymmetric craniofacial growth in rabbits. felder and Hirschfelder (1982b, 1991) found signifi­
cant differences in craniovertical and craniocervical
parameters between the registration in standard­
DIAGNOSTIC RECORDS ized cephalograms and a lateral cephalogram taken
in a natural head position. The natural head posi­
Not every asymmetry must be treated. Under tion is more proclined than the fixed standardized
physiological conditions the body compensates position. During orthodontic diagnosis, routinely
for a certain degree of asynunetry. Unfavorable taken lateral cephalometric X-rays do not aUow a
environmental factors can accumulate and reduce reproducible realistic analysis of craniocervical and
the level of compensation. Discomfort appears vertical parameters. In order to investigate asym­
and asymmetry becomes obvious (Pirttiniemi metry of the upper cervical spine, radiological
1994). examination should be based on the head position
An investigation of clinically healthy male of the orthopedic registration in the neutral posi­
pilots demonstrates the tolerance of the body to a tion (Gutmann 1981).
certain degree of asymmetry. Although clinically
the examined pilots were not asymmetrical in Clinical examination
function and morphology and did not show any
discomfort, the investigation revealed a high inci­ An orthodontic disorder can be dental and/ or
dence of asymmetrical structure of the high cervi­ skeletal (Kahl-Nieke 2001). Loss of space, crowd­
cal spine (OCR). ing, labial or lingual inclination of the incisors, an
In order to treat any asymmetry correctly it is infraposition or a supraposition, a dental midline
important to diagnose not only the asymmetrical shift and rotations all belong to dental disorders
structure itself, but also the cofactors that con­ and should be corrected by movements of the
tribute to the final decompensation of asynunetry. teeth. A transversal mandibular shift, a more pos­
terior or anterior position of one or both jaws as
well as other vertical discrepancies are the most
ORTHODONTIC RECORDS common skeletal problems. If there is still ongoing
growth, a skeletal disorder can be corrected by
Radiographic examination guiding and influencing growth to a certain
degree. If the skeletal discrepancy is too signifi­
As one basic diagnostic record in orthodontics, a cant or there is no developmental growth remain­
lateral cephalogram is taken in order to analyze ing, orthodontists can compensate for the skeletal
the relationship between the sagittal position of problem by moving teeth or correct the anomaly
the upper and lower jaw and the direction of in combination with surgery.
mandibular growth. The mandibular growth can In the 1890s E.H. Angle, an American ortho­
evolve in two directions: a clockwise and a coun­ dontic pioneer, published his 'Angle class' classifi­
terclockwise rotation. Different craniofacial angles cation with the maxilla as a fixed skeletal structure
can determine the quality of growth. As the verte­ within the skull. The correct relationship between
brae are clearly visible, orthodontists have taken upper and lower jaw was defined as Angle class I:
these X-rays in order to investigate the spine a neutral position of the lower jaw and dentition
parameters in relation to the growth of the lower in comparison to the upper jaw and dentition. The

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teeth occlude alternately and upper incisors are cephalometric analysis, this neutral position can be
overlapping the lower ones. The pathologic Angle measured by different angles. Consequently, skele­
class II describes a more distal position of the tal class II is the more posterior position of the
lower teeth in comparison to Angle class I, which lower jaw to the maxilla. This can be due to a more
is measured in width of premolars (equivalent 7-8 forward position of the maxilla than normal
mm). In an Angle class III the mandible and the and/ or to a more posterior pOSition of the lower
lower teeth are positioned more mesially, in most jaw. The opposite is defined by the skeletal class
cases in combination with an anterior crossbite. III configuration (Fig. 13.2).
Since 1932, following the publications on lateral Under normal conditions, the incisors of the
cephalometric analysis by Hofrath (1931) and mandible and maxilla occlude with each other.
Broadbent (1931), the skeletal position of the jaws This occlusal relation is described by the overjet
has been classified differently from the above­ and overbite. The overjet is defined as the distance
mentioned Angle classes (Fig. 13.1). between the lower incisors and upper ones in the
Cephalometric analysis revealed that even the sagittal plane, whereas the incisors' distance in
maxilla alters in its position to the skull. Therefore the vertical plane is called overbite (Fig. 13.3). In
a skeletal class I is defined as the neutral position addition the midlines of the upper and lower cen­
of the jaws to each other. Based on the lateral tral incisors should be identical.

Figure 13.1 The relationship of the teeth as well as the

jaws is defined by three different classes. In most cases
dental occlusion and sagittal jaw configuration are
consistent with each other. (Al demonstrates a dental
and skeletal class I relation: the maxilla is in advance to
the lower jaw, teeth occlude alternately by an overbite of
the upper incisors to the lower ones. A skeletal and
dental class I I (B) occurs when the upper jaw and
occlusion is in advance to the lower jaw and occlusion
compared to a skeletal class I. As (e) reveals, a skeletal
class I I I is the opposite of a class I I . The lower jaw and
teeth are in advance to the upper jaw and teeth.

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Asy mmetry of t h e p ost u re, l o c o m otion a n d d ent iti o n in chi l d ren 149

Figure 13.2 For therapeutic reasons it is important to

analyze the individual skeletal position of the upper and
Figure 13.3 The position of the upper and lower
lower jaw by a lateral cephalogram. S, sella - midpoint
incisors is defined by the sagittal and vertical distance
of the sella turcica; N, nasion - most anterior point on
between the incisors. An overjet of 2 mm is
frontonasal suture; A, A point - position of the deepest
physiological. The distance in the vertical plane, the
concavity on anterior profile of the maxilla; B, B point -
overbite, should be 2 mm as well. An increased overbite
position of the deepest concavity on anterior profile of
(>2 mm) is called an anterior deep bite, whereas a
the mandibular symphysis. (From Kahl-Nieke 2001, with
reduced overbite (<2 mm) is called an open bite.
permission of Urban and Fischer.)

In order to prove the clinical situation, extra­ to the orthostatic posture. Furthermore, lip s and
and intraoral pictures are taken in a standardized nose shouldbe investigated as they gi ve evidence
fixation. For bett er diagnosis, three-dimensional of the mode of breathing. Intraorally, the tongue
plaster models reflect the intraoral s ituat i on. A position and the sw a llowing pattern should be
panoramic X ray gives an overall idea of possible
- observed. Habits and disorders in speech such as
dental disorders. The analysis of the above-men­ sigmatism (lisp ing) should be detected. If treat­
tioned lateral cephalogram provides evidence of ment is required, patients should be referred to a
sk el eta l problems. m y ofunctional therapist.

Examination of the soft tissues

An i n spec ti o n of p eriora l soft t is sues
is essential
for a good orthodontic di agno si s The examina­
. An orthop edic disorder can be muscular, func­
tion should start with an investigation of the pos­ tional or skeletal in nature. If there is a visible
ture: The head and neck muscles, the per i oral and asymmetry in the occipitocervical region it is not
masticatory muscles as well as the muscles of a pathology by i ts elf. Only in combination with a
the supra- and infrahyoid region all contribute disturbed function may one talk of an orthopedic

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disorder. The functional approach is often under­ In functional orthopedics, which is a funda­
estimated. But function is as real as anatomy. mental orthodontic treatment philosophy that
The neck motion can be evaluated by palpation, takes advantage of the patients' muscle forces to
inspection, additional radiological records and correct orthodontic disorders, many possible rela­
functional analysis of the region (Biedermann tions between spine and jaw have been discussed.
1991, Biedermann and Koch 1996, Koch and Gra­ Schwarz (1926) was convinced of an interaction
mann-Brunt 1999). An asymmetry in the range of between head posture and jaw position. He was
lateral motion of the head in anteflexion can imply particularly certain that during sleep the head
an asymmetry. A detailed description of orthope­ posture influences the mode of respiration and the
dic diagnosis is given in other chapters of this pathology of orthodontic anomalies. BaIters (1964)
book. proclaimed Angle class characteristic head pos­
tures. His statement is well known in orthodontic
literature, although it lacks any scientific evidence.
REVIEW OF ORTHODONTIC According to Baiters' clinical observation, patients
DISCREPANCIES IN CHILDREN WITH with an Angle class II tend to a hyperlordosis of the
ORTHOPEDIC DISORDERS spine while patients with anomalies of Angle class
III show a kyphotic posture. Posture and lower jaw
Sagittal plane seem to interact.
Gresham and Smithells (1954) showed that chil­
Many authors have investigated the correlation dren with a bad posture have a high percentage of
between the sagittal jaw relationship and orthopedic Angle class II occlusion, a long-face syndrome and
parameters. Although there are disagreements, there a significant increase in lordosis of the spine. Dif­
seems to be a tendency for a change in position of the ferent working groups (Nobili and Adversi 1996,
upper cervical spine when the patients show a distal von Treuenfels 1983) revealed relations betvveen
jaw relationship (Angle class IT) (Fig. 13.4). characteristic findings, such as a hyperlordosis of
the spine and Angle class II as well. In some cases
a relationship between an increased overjet and a
more backwardly inclined spine was detected.
Mertensmeier and Diedrich (1992) obsen1ed a
correction of the concavity of the spine after ortho­
dontic therapy. Critically, it must be taken into
account that a curved spine straightens with age.
Many other studies have refuted Angle class char­
acteristic orthopedic findings (Hirschfelder and
Hirschfelder 1987, Sterzik et al 1992). Sterzik et al
(1992) studied 127 lateral cephalograms of untreated
children. They could not find any causal relations
between sagittal position of the jaws, atlas position
Figure 13.4 Clinically this patient shows an Angle class I I and head posture. Hi.rschfelder and Hirschfelder
relationship o f 4 m m !'h width o f premolars). The occlusal
(1987) did not detect any correlation between spe­
discrepancy results in a tooth-to-one-tooth relation which
cific Angle classes in children with orthopedic disor­
can be caused by different pathological factors: mesial
movement of the upper teeth and/or distal movement of ders, but observed a high incidence of postnormal
the lower teeth and/or anterior position of the maxilla occlusion (Hirschfelder and Hirschfelder 1982a).
and/or posterior position of the lower jaw. The skeletal In addition to the afore-mentioned publications
causes can only be detected by a lateral cephalogram. Hirschfelder and Hirschfelder observed in chil-

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Asy m m etry of t h e p o s t u re. l oc o m ot i o n a n d dent i t i o n in c h i l dren 15 1

dren with disorders of the upper cervical spine a Scoliosis and torticoll is
high prevalence of postnormal occlusion. About
two-thirds of the children w ho w ere tr eate d with Scoliosis and tort icol lis are two orthopedic disor­
m anual therapy showed dental anomalies. A sta­ ders in which many inte rdiscip linary approaches
tistica lly significant higher prevalen ce of Angle h a ve been p ubli she d Except for Wa chs ma nn

class II malocclusion could not be confirmed. ( 1960 ) all authors observed a signif ican t ly higher
incidence of crossbite (26-55% prevalence) in these
Vertical plane pat ients than in any control group. Prager (1980)
concluded that the crossbite demonstrates the
A similar position of the atlas is seen in patients observed asymmetrical posture. Muller-Wachen­
with an anterior open bite (von Treuenfels 1984). dorf (1 96 1 ) considered the high prev al ence of cross­
These fi ndings were interpreted as the cause of a bite to be a res ult of the weak connective and
reclined head post ure and habitual mouth breath­ supporting tissue and not a consequence of the sco­
ing (Fig. 13.5). liosis itself. Hirschfelder and Hirschfelder (1987)
interpreted the results of the examination of 101
Transversal pl ane scoliotic patients as an interaction of the corporal
scoliosis with the facial scoliosis. Pirttiniemi et al
There is still con troversy as to whether children (1989) found a high prevalence of lateral malocclu­
with skeletal transverse asymm e tries of the de ntal sion in pa tients with torticollis. The observed lateral
arch tend to have sp eci fic orthopedi c disorders discrepan cies, i.e. dental arch asymmetry and mid­
(Fig. 13.6). line deviation, were diagnosed in most cases in the
In a stud y of 57 children DuBIer and co workers - upper arch (Alavi et al1988, Lundstrom 1961).
(2002) observed no corr elation between orthodon ­ A general a gre em ent exists that early treatment
tic asymmetry and any or thoped ic disorder. Chil­ for pati en ts with systematic orthope dic distur­
dren with or thodont ic a symm etry did not show a bances is most effective (Lukanowa-Skopakowa
specific incidence of or thopedic pa thologies. 1987, Muller-Wachendorff 1961). In a lon gitudina l
On th e other hand, Lippold et al (2000) recom­ st udy, Pecina et al (1991) showed a posi tive rela­
mended an interdisciplinary tr e a tm en t approach tion ship b etw een heredi tary orthodontic anom­
in patients wi th midline discrepancies since they
alies and idiopathic scoliosis. Since orthodontic
observed a highe r prevalence of orthop edi c disor­
der in combin ation with midline discre panc y.

Figure 13.6 In most cases a skeletal mandibular

midline shift is combined with a unilateral crossbite. As a

consequence of the width discrepancy of upper and

Figure 13.5 An anterior open bite caused by infraposition lower jaw. the lower jaw shifted to the right side with a
of upper and lower incisors to the occlusal plane. right-sided crossbite.

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disorders can be diagnosed at a younger age, the cervical angle indicates a posterior rotation of the
later development of scoliosis may be revealed by a mandible, an increased anterior facial height
close collaboration between orthopedics and ortho­ reduced sagittal jaw dimensions and a steeper
dontics. Children with a scoliosis bigger than 10° inclination of the lower jaw. Patients with a small
should be examined orthodontically. Pirttiniemi et craniocervical angle show a reduced lower facial
al (1989) suggested a routine orthodontic investiga­ height; the sagittal jaw dimensions are larger and
tion of children with suspected torticollis. The aim the inclination of the mandible less steep. The only
of early orthodontic treatment is to contribute to orthodontic factor that indicated an orthopedic
the normalization of natural posture. association with the craniocervical posture was a

One reason supporting early surgery in chil­ lack of space in the anterior segment of the dental
dren with torticollis is the attempt to prevent the arches (Solow and Sonnesen 1998).
development of facial asymmetries. Solow and Tallgren (1977) explained the results
of their work using the soft tissue stretching
General orthodontic findings hypothesis. The soft tissue layer covering the neck
and head has a restraining influence on the for­
For over 30 years, Solow and co-workers (Solow ward growth of the facial skeleton. An extension
and Siersbaek-Nielsen 1992, Solow and Sandham of the craniocervical posture leads to a caudally
2002) have investigated the relationships between orientated traction on the soft tissue layer of the
natural posture and development of the head. T he face. Due to the anatomy of the facial skeleton, the
posture of the upper cervical spine is related to the passive stretching of the soft tissue layer results in
growth of the lower jaw (Fig. 13.7). A large cranio- dorsal forces to the dentofacial structures.

Figure 13.7 Relationship between craniocervical angle, rotation of the mandible, and anterior facial height ( based on
Solow B, Sandham A 2002 Craniocervical posture: a factor in the development and function of the dentofacial
structures. European Journal of Orthodontics 24: 467-456, by permission of Oxford University Press ) . A: A large
craniocervical angle indicates an increased posterior rotation of the mandible and anterior facial height. B: A reduced
anterior facial height is most often related to a small craniocervical angle and an anterior rotation of the mandible.

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Asy m m etry of the posture , l oco motio n a n d d e n tit i o n i n c h il d re n 153

The hypothesis has been confirmed by other Similar observations have been made in
studies. Hellsing et al (1987) demonstrated an patients with obstructive sleep apnea (Solow et al
association between lip pressure and posture of 1984), in children with enlarged tonsils (Behlfelt
the head. With elevation of the head, the lip pres­ 1990, Behlfelt et al 1989), an d in children with
sure increases. Other investigations in children nasal allergy.
with impaired nose breathing showed an increase In physiotherapy, special treatment phases try
in craniocervical angle (Solow et aI1984). to normalize the function of head and neck in
order to establish an orthostatic stability of the
Atlas deviation skull with the spine. A good muscle tonicity in the
orofacial region supports an undisturbed posture
As a result of various radiological studies (Howard of the craniocervical region and furthermore of
1983, Sandikcioglu et a11994), the height of the pos­ the spine (Aragao 1991, Rocabado 1987, Rocabado
terior arch of the atlas has been fOLmd to be correlated et a11982, Schupp and Zcrnial 1997).
to different orthodontic discrepancies. In an adenoid
group of 43 children aged 4-15, the posterior height
of the dorsal arch of the atlas was significantly INTERDISCIPLINARY TREATMENT
reduced (Huggare 1989). A negative correlation APPROACH IN CHILDREN WITH KISS
between the height of the dorsal arch of the atlas and SYNDROME
the craniocervical angle was found. Furthermore in
non-orthodonticJlly treated children with an Angle Since November 2001 an interdisciplinary consul­
class I, Huggare (1989) showed that the height of the tation has been established at the Department of
dorsal arch could predict the growth of the lower Orthodontics at the University of Hamburg. So
jaw. The taller the posterior arch of the atlas the far, 282 chi ld ren aged 2-10 years (male: female =

greater the tendency that growth would produce a 2: 1) have been examined at the Department of
square facial type. There seemed to be a general asso­ Orthodontics and at the clinic for manual therapy
ciation between vertical development of the cervical in children in Eckernfbrde. A clinical and radio­
colurrm and face (Huggare and Houghton 1995, logical orthopedic examination was performed
1996, Kylamarkula and Huggare 1985). with particular attention to posture. T he medical
history of the examined children revealed at least
Soft tissue one of the following symptoms: retarded motor
patterns, retarded speech development, bad pos­
In children with reduced muscle tonicity, a higher ture and vegetative illness such as headache. The
prevalence of orthodontic anomalies has been evaluation of functional motion analysis as well as
investigated (Ouyzings 1955, Wachsmann 1960). a radiological examination revealed in all children
Mouth breathing is thought to lead to postural an anatomical and functional asymmetry of the
changes such as a clockwise rotation of the cervical spine. After applying manual therapy,
mandible, a lowered position of the tongue, and a intra- and extraoral records and orofacial dysfunc­
reclinahon of the head (Bahnemann 1981, Krakauer tion were evaluated in aU patients at the Depart­
and Guilherme 2000, Rubin 1980). These postural ment of Orthodontics. Seventy-six percent of the
changes may relate to characteristic morphological children showed orthodontic disorders. No corre­
changes (Harvold et a11973, von Treuenfels 1985). lations could be detected between the individual
The appearance of a habitual mouth breather is orthodontic records such as midline shift, sagittal
described as 'facies adenoidea'. The term 'long face jaw relationship, side of the crossbite and ortho­
syndrome' reflects the extraoral characteristic fea­ pedic pathologies. A high percentage of orofacial
tures of a patient with habitual mouth breathing. dy sfunction was diagnosed in these children: 62%

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of the children had weak orofacial muscles, and

in 89% an abnormal swallowing pattern was
found; 72% breathed habitually through the
mouth. Although those children were undergoing
treatment, myofunctional therapy had so far been
neglected . Myofunctional therapy was started in
two-thirds of the children and early orthodontic
treatment in one-third of them. The authors con­
cluded that the soft tissues and orofacial function
seem to influence the pathology of malocclusion
and orthopedic disorders. The high percentage of
orthodontic treatment needed in children with
orthopedic pathologies suggests an interaction of
the hard tissues - jaw and spine - as well.

Figure 13.8 The interactive system of the functional

boxes is a model to better understand the interactions of
the different anatomical regions of the skull. Although
each box is a system of its own, impeded function can
The soft tissues and orofacial function/ dysfunc­ lead to disorders within a different box. Successful
tion seem to be important factors in the pathology treatment can only be achieved by taking the whole

of malocclusion and orthopedic disorders. The system into account.

combination of orthodontic disorders and ortho­

pedic pathologies suggests that there is an interac­ Lip closure is thought to be one important con­
tion of the hard tissues - jaw and spine. Early dition for establishing nose breathing and
orthodontic screening of children should therefore somatic tongue function.
also focus on symmetric posture and function as • The oral cavity with the tongue and dental
well as on the balance of orofacial power. occlusion. Swallowing and speech are the two
To provide an explanation the following model important functions within this box.
was set up to describe the observed correlation • The infra- and suprahyoid muscles that con­
between orofacial function and diagnostic find­ tribute to an orthostatic equilibrium of the low­
ings: The orofacial and craniocervical region is est part of the skull.
anatomically divided into different boxes that are • The upper cervical vertebrae for the stabilization
combined by function (Fig. 13.8). Dysfunction and movement of the head.
within one box could lead to disorder in another
box. Therefore, the different boxes with different Under normal conditions, the different boxes
functions are combined interactively. interact in function and support each other. An
Some interactions have been proven so far, but equilibrium is established, and normal develop­
the overall view has not yet been revealed. ment is possible.
The functional boxes are defined as follows: If the balance of power between the different
boxes is disturbed or destroyed and bodily com­
• The nose with the important role of habitual pensation is not possible, normal function and
nose breathing. development is impaired. Therefore, it is very
• The lips as the entrance to the mouth are impor­ important for each medical specialty not only to
tant for nasal respiration and tongue function. examine the specific box but also to have an over-

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Asymmetry of the posture. locomotion and dentition in children 155

all view of the whole system. Only by doing so picion of an orthopedic disorder such as torticollis
can stable treatment results be achieved by main­ or scoliosis can be confirmed by orthodontic diag­
taining the balance of power. nosis of a crossbite.
Further clinical investigation is being con­ Some authors propose a routine dental exami­
ducted in order to provide scientific evidence for nation in cases of deviant head posture in order to
the interaction between the different boxes. start treatment at an early age. A proper treatment
approach in young children should consider any
condition affecting head posture and the develop­
CONCLUSION ment of the high upper cervical spine.
Radiological examination in two planes
Even though many different working groups have reveals skeletal deviations and clinical inspection
conducted an interdisciplinary treatment approach confirms symmetry in function. A tool for clinical
in children with orthopedic disorders, no clear examination of the orofacial region can be offered
therapeutic recommendations based on scientific by the system of functional boxes. Each medical
evidence have been established so far. specialty should extend the clinical view. In cases
Early treatment is recommended for children of extreme deviations the patient should be
with severe orthopedic anomalies such as torticol­ referred to the corresponding medical specialty
lis and scoliosis: in order to harmonize facial and as early as possible in order to harmonize the
postural symmetry an early bilateral treatment proper development of the orofacial and cervical
approach should be sought. In some cases the sus- region.


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A sy m m e t ry of t h e p o s t u r e , l o c o m ot i o n a n d d e n t i t i o n i n c h i l d r e n 157

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between craniofaci a l and condyle path asym metry in in the development and fun c t i on of th e den tofac i a l
u n i la tera l c rossb i te pa t ien ts. E uropean Journal o f st(ll c t ures. E uropean Journal of Orthodontics 24: 44.7-456
Orthod on tics 1 2: 408-4 1 3 Solow S, S i ersbcek - N i e lsen S 1 992 Cervical and
Poikela A , Kantomaa T, Tuominen M et a l 1 995 Effec t of craniocervica l postu re as p red ictors o f cra n i o facia l
unila teral masticatory function on c raniofa c i a l grow th in grow th . A merican Journal of Orthodontics and
the ra b b i t . E u ropean Journa l of Ora l Sciences 1 03 : 106-111 Den tofacial Orthoped ics 1 0 1 :449-458
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asym metry i n v a rious spec ies o f rodents. G row th


analys is of lateral cephalograms the tracing of po s it i on : the p atie nt is fixed by ear olives an d
the lateral cephalogram p ro v id e s information a glabella rod . A radiograph tak en in tlUs way

of the skeletal p attern, i . e. the q ual i ty of does not reveal a rep r o d u ci b le p osition of the
mandib ular growth (clockwise or cou nter­ head an d does not demon strate the natural
clockwise direct ion ) and sagittal position of head position.
the upper a nd lower j aw within the skulL Lat­ Angle class I normal rel ation ship of the molars,
eral cephal ograms are taken in a standardized premolars and canines, which means that the

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mesiobuccal cusp of the upper molar occludes lowing pattern, mouth breathing, etc. Habits are
in the buccal groove of the lower molar. physiological to a certain age in early childhood.
Angle class II sagittal malocclusion: the lower first Depending on the intenSity of the dysfunction
molar is positioned distally to the upper and age of the patient, a persisting habit can lead
first molar in comparison to the Angle class I to dental and skeletal disorders.
occlusion. long face syndrome excessive lower anterior
Angle class III sagittal malocclusion: the lower facial height.
first molar is positioned mesially to the upper mesial describes the direction in the sagittal plane
first molar in comparison to the Angle class I towards the frontal midline.
occlusion. midline discrepancies inconsistency of upper and
crossbite a deviation from the normal bucco­ lower midline, which can be skeletal or dental
lingual relation of the teeth. A crossbite in nature.
can be located frontal, lateral, bilateral and midline shift of the mandible skeletal discrep­
unilatera!. ancy in the transversal plane.
deep bite an increased overjet. In severe cases the occlusal plane defined by the buccal cusps of the
lower incisors occlude traumatically with the upper premolars and the mesio-buccal cusps of
palatal mucosa. the upper first molars.
dental malocclusion disorder due to dental mal­ open bite although the lateral teeth are in occlu­
position. Dental malocclusion can be corrected sion the incisors do not contact.
at any age. overjet distance between the upper and lower
dental midline shift midline discrepancy due to incisors in the horizontal plane.
dental deviations of the midline, i.e. an asym­ overbite overlap of the incisors in the vertical plane.
metrical extraction of a tooth can lead to dental posterior-anterior cephalogram gives an assess­
midline shift. ment of the skeletal situation in the transversal
distal the opposite of a mesial direction. and vertical plane.
early orthodontic treatment normal orthodontic protrusion a proclined inclination of the incisors.
treatment starts with the eruption of canines and retrusion a retruded inclination of the incisors.
premolars (late mixed dentition), which normally sagittal jaw position position of the upper/lower
begins at the age of 10 years. Early orthodontic jaw within the skull. It is of therapeutic interest
treatment may start directly after birth (i.e. in to know the cause of a skeletal deviation in
patients with cleft lip and palate), in the primary order to treat efficiently: i.e. a skeletal class III
dentition or during the early mixed dentition, can be caused by a pathological mesial position
when incisors change and the first molars erupt. of the lower jaw and/or by a distal position of
The aim of early interceptive treatment is to har­ the upper jaw.
monize the development of the different jaws to sigmatism disturbances in the articulation of's'.
each other. One indication of early orthodontic skeletal anomaly three-dimensional deviations of
treatment is the correction of a lateral crossbite. the position of the upper and lower jaw which
facies adenoidea the extraoral manifestation of should be treated skeletally. During growth,
patients with facies adenoidea includes narrow skeletal anomalies can be corrected to a certain
width dimensions, protruded incisors, incom­ extent orthopedically by the orthodontist. In
petent lips/no lips closure. The clinical appear­ adolescence, skeletal problems can be corrected
ance has often been attributed to habitual surgically or by dental compensation.
mouth breathing. skeletal class I normal balanced relationship
habit a dy sfunction of an unconscious nature such between upper and lower jaw which can
as a sucking habit, tongue thrust, abnormal swal- be assessed by analysis of the lateral cephalo-

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Asymmetry of the posture, locomotion and dentition in children 159

gram in terms of an angle or the distance cases the landmark of the mandible is ahead of
between a defined landmark at the maxilla the landmark of the maxilla. Consequences of this
and mandible. skeletal discrepancy are a decrease in the overjet
skeletal class II increased (positive) sagittal and a concave profile.
distance between maxilla and mandible.
skeletal class III decreased (negative) sagittal
distance between maxilla and mandible. In severe

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The different levels:

practical aspects of manual
therapy in children


14. Practicalities of manual therapy in children 163

15. Manual therapy of the sacroiliac j oints and pelvic girdle in children 173

16. Manual therapy of the thoracic spine in children 185

17. Examination and treatment of the cervical spine in children 205

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Chapter 14--�------��--�-

Practicalities of manual therapy in

Interacti o n w i th pare nts and children, tricks
and tips for diagnosis and follow-up

H. Biedermann

A lot of things happen before we see a child and
Communication problems 163
the family for the first time. The most important
Leaflet for KISS children 164
step is to draw the family's attention to the fact
Leaflet for KI DD children, i.e.
that manual therapy may have something to offer
schoolchildren 166
in resolving their particular problem.
The man drawing test 168
The professionals we interact with can be
Leaflet on postural problems 169
divided in two broad groups. The larger group
An ongoing process 171
comprises the 'classic' pediatricians whose world­
view is that of an internist, i.e. predominantly
patho-morphologically oriented. The smaller
group is made up of neuropediatricians, physio­
therapists and other caregivers who - through
their professional experience - are already in con­
tact with the possibilities of functional pathology.
These two groups have big problems commu­
nicating with each other. They may know about
the other 's language, but even then understand­
ing does not come naturally.
Most of the pediatricians we collaborate with
are social pediatricians and neuropediatricians,
doctors trained in rehabilitation and care of dis­
abled children. Because they use physiotherapy
extensively in their planning, they have at least
a notion of the possibilities such an approach
can offer. The functional approach is not new to

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In most cases the first patients referred to us Based on this extensive experience we came to some
are those h clear 'mechanical' problems, i.e. a
w it general conclusions.
postural asymmetry or muscular imbalance. The most important problem regarding the spine
After the first contact, these colleagues are as a and the neck is the KISS syndrome, Kinematic
rule very astonished that other - in their eyes Imbalances due to Suboccipital Strain. The main
non-related - problems have been resolved, too. symptoms we encounter in these cases are:
Chapter 10, by Kuhnen, provides a few such case
• wry neck
• fixed a nd bent tru n k
The communication with physiotherapists is
• asymmetry of the face
easier. They know first-hand how much interac­
• flattened back of the head
tion there is between the muscular system and the
• asymmetrical use of arms and legs.
autonomic system, to name but two, and they are
aware of the power of the functional approach. At Often these problems coincide with sleeping
least in Germany they depend on referrals from disorders, difficulties of breastfeeding on one side,
medical doctors, and they cannot refer patients colic or incessant crying.
directly, at least not officially. In reality there often We do not know beforehand how much we can
is such a trusting relationship between the moth­ help in individual cases by treating the upper part
ers and the physiotherapists that they have more of the spine, but in two-thirds of our patients, one
influence than is apparent at first sight. treatment is sufficient to achieve a thorough
However, it cannot hurt to explain one's point improvement or at least a more solid base for
of view as clearly as possible, which is one reason further physiotherapy, simplifying future
why we have drawn up several leaflets for parents treatments.
concerning the main indications for manual ther­ Comparing our young patients to the general
apy in children. statistics available we found some risk factors: a
difficult birth with the use of vacuum extractors
or forceps, prolonged labor and/or breech position
of the unborn increase the probability of KISS. We
see twins much more frequently, too. If one of
your children has already had successful
We send the following leaflet to parents in prepa­
treatment for KISS the likelihood of similar
ration for the first visit.
problems is much greater if the newborn is of
You will bring your baby to us for treatment in the the same sex.
next week, most probably after a conversation with All these observations are based on statistical
your pediatrician or physiotherapist. To analysis, which means that we have to examine
complement the information you received there we every individual case separately, albeit with a
would like to give you some explanation regarding bigger chance of finding the corresponding results.
our diagnosis and treatment.
During more than twenty years of treating Radiographs:
children and babies we have discovered how To examine the baby thoroughly a radiograph of
problems of fixed posture and unbalanced symmetry the cervical spine is essential. Without this we
can be improved by an adapted therapy of the spinal cannot come to a firm decision as to whether your
column at the neck. My friend and teacher Gutmann baby needs treatment or not. During the first year,
started this in the 1950s and we have been able to one plate is sufficient in most cases; if ever we
systematize this since. Meanwhile we have treated need more plates we shall explain the reasons to
more than 25 000 infants under the age of two. you. In children who are older than 2 years, we

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Practical ities of manual therapy in children 165

need two plates, one from the side and one frontal concern, in almost every case, improper techniques,
pictu reo repeated manipulations and superficial
As technology of films has improved examination prior to treatment.
considerably during the last decades the amount of
radiation needed for a plate is about 10-20% of What do the pa rents tell us?
what was necessary in the 1970s and 1980s. Most parents mention some (but not a II) of the
Digital equipment has reduced this further. following items in their case history:
Compared to a plate of the lungs and thorax the
• fixed posture of the head to one side or to the
dose used for the neck is negligible. Having said
that I want to accentuate that we do not order
• insufficient control of the head
these plates thoughtlessly. We think that the
• fixed retroflexion of the head with arms pulled
information obtainable from them more than ,
back ( parachutisf)
warrants the necessary exposure.
• fixed posture while sleeping, with head bent
If ever you have any more questions don't
hesitate to ask us.
• difficulties getting the child to sleep
• often waking up at night, crying
The treatment:
• asymmetry of the movements and use of arms
As we found out in analyzing our treatments the
and legs
success rate is much higher when we can make sure
• asymmetry of the posture of the trunk
that the babies were not treated elsewhere in the 2
• uneven maturation of the hip joints
weeks preceding your first visit. Accidents
• pes adductus (i.e. a bent and curved foot)
immediately prior to this date, or an acute infection
• highly irritable neck; the baby does not want to
with fever, are not a good base for examination and
be touched there
treatment, either. In this case do not hesitate to
• 'head banging' - the baby bangs its head against
phone us, and we can postpone your date. It is
the sides of the bed
better for the child to wait a few days and be seen
• asymmetry of the facial features
in the best possible circumstances.
• flattened and asymmetrical back of the head
Based on the evaluation of the radiographs, your
• asymmetrical position of the ears
report and the examination of the baby, we come
• colic
to a decision about the best treatment. In most
• incessant crying.
cases this will consist of a manipulation of one or
several levels of the spinal column. The exact These complaints can have a lot of different
technique used in an individual case depends on a causes, but when they are found in combination -
lot of factors, e.g. the age and mood of the baby. and when there is a prompt improvement after
We shall ask your permission to treat beforehand, our therapy - it seems fair to say that problems
as the best way to proceed is to move on smoothly of the cervical spine were at least partly responsible.
from examination to the treatment - not least to Some remarks about further development:
spare the mother's additional stress. Most parents Three to four weeks after our treatment your
are not aware of the moment of manipulation and child should be examined by a proficient specialist
are a bit astonished (and relieved) to get the baby at home, be it the pediatrician or a physiotherapist.
back so soon. These colleagues determine if and what further
Nobody should be so arrogant to exclude any treatment is necessary. If they decide that you
risk 100%, but to our knowledge there have never ought to come back to us for a check-up (which is
been any serious complications in manual therapy the case in about 15%) we would like to see your
of babies. Incidences in the treatment of adults child 6-8 weeks after the first visit.

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We strongly advise some rest for the cervical spine does not help to see the connection with a
after our treatment. Therefore we would like to ask biomechanical base of the situation.
you to stop any physiotherapy during that time. We Babies with a family where scoliosis or other
also would like you to refrain from any sport or orthopedic problems occur should be screened
exercise which might put stress on the neck, i.e. a more thoroughly than other children, be it at home
header or head dive, etc. After these 3 weeks it is by their pediatrician or at a specialist clinic.
much easier to judge if and what kind of additional
treatment is necessary. About a third of the babies
will need additional help, mostly physiotherapy. LEAFLET FOR KIDD CHILDREN.
Manual therapy and physiotherapy can and i.e. schoolchildren
should be comb ined. A baby who is successfully
treated w ith manual therapy profits more from Today you came for the first time with your child
physiotherapy or speech therapy and the to be examined and treated. Most probably you
professional attent ion of these specialists helps have already talked with your pediatrician and/or
to control the outcome of our efforts, too. Any physiotherapist about it. To complement their
rush in adding as much as possible information we would like to give you some
therapeutically worsens the result, and the information about the kind of therapy we provide
necessary patience is something which has to be and its possibilities (and limits). This leaflet should
learnt conscientiously. help you to formulate further questions.
Parents who have seen the sometimes dramatic During the last decades we have learned to look
improvement due to manual therapy tend to be at many problems of schoolchildren from the
overly concerned afterwards. We do not have to viewpoint of spinal disorder. Think. for example, of
exaggerate; in almost every case there are no headaches: most have their main origin in disorders
special precautions necessary after manual therapy. of the spine. The prime candidates for such an
It suffices to avoid direct irritation of the neck examination of the spine are problems of posture
during these 2-3 weeks. and maladroit movements.
If the child catches a cold, a temporary relapse One example may help in understanding how
into the old postural pattern is possible. If this lasts these problems can go much further than that.
only a few days, no further measures are necessary. A child cannot move its head freely - and often
If it lasts for more than a week it might be fitting this problem started very early on. The constraints of
to consult us or another specialist, e.g. your neck mobility have to be compensated further down,
physiotherapist at home. If in doubt, do not i.e. at the thoracic level. An untrained observer
hesitate to contact us by phone or email. might not notice much about the restrictions of the
Our experience has shown that a routine neck mobility due to this compensation mechanism,
check-up at the age of 3 is very useful. We often but the eye-hand coordination depends on it as
find minor dysfunctions which were not apparent much as the equilibrium and the ability to orient
earlier but could cause more trouble if left alone oneself in a given space.
too long. This malfunctioning confronts the child with
The next check-up is usefully scheduled around many difficulties when the causal connection
the first school year. This marks the transition from with the spinal apparatus is not obvious at first
the free-wheeling baby period to the more sight:
sedentary lifestyle of a schoolchild. Any functional
problem of the musculoskeletal system tends to be • Early on (in the months after birth) we can find
aggravated by this reduction of exercise and these a fixed posture, colic, incessant crying and a
disorders often manifest themselves in a way that non-standard motor development.

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Practicalities of manual therapy in children 167

• Later on these children often have problems Our therapy aims at restoring the function of
learning to bicycle or walking on stilts. the entire spine. The most important areas are the
• Lack of confidence in their own perception junctions of the spine with the head and the pelvis,
often leads to fear of heights and being afraid i.e. the suboccipital region and the iliosacral joints.
of unknown situations. Beginning here the entire spinal apparatus is
• Bad coordination results in clumsiness - they examined and if necessary treated.
are regarded as fools (and sometimes these At the first session we normally find quite a few
children cultivate a clown image to conceal of these blockages all over the spine. Most of them
their inabilities). vanish after the 'big' problems are taken care of.
• With poor spatial orientation comes a hearing Once the upper cervical spine moves freely again
impairment, especially in filtering out most blockages in lower regions of the cervical spine
background noises and concentrating on one and the thorax subside spontaneously, so we do not
person. These children seem to lack have to treat every blockage we find on the way.
concentration when, in fact. they are just tired Once the functioning of the spine is restored, we
of having to concentrate too much. strongly advise allowing the body enough time to
• With such a difficult base for their perception reorganize its motor patterns. Years ago we
these children become as frustrated as we rea Iized that the results of our treatment were
adults would be in such a situation; they are better when the manipulation was not immediately
easily annoyed and irritable. They acquire a followed by another therapy. So we advise that
reputation of being impatient, aggressive and children be given 2-3 weeks to adapt, before
that 'they never listen'. further evaluation of the situation by the
• Too slow, too timid, too clumsy - many of these physiotherapist who knows the condition of the
children withdraw and avoid situations where patient. In some cases we propose modifications to
they fear not being up to the task. Those around the exercises applied, but mostly we leave these
them often reinforce this attitude through their decisions to the pediatricians and physiotherapists
refusal to play with them, or to help them over who already know the child. Equally important is to
minor problems - and a vicious circle sets in. avoid unnecessary stress to the neck, i.e.
somersaults or headers. During the week after
The broad spectrum of the situation described manipulation we would advise you to refrain from
here makes it evident that it fits many cases. Almost sport completely, as the skills might be temporarily
every child has a phase where one or more of these diminished and a certain amount of roughness is
items fit in, certainly those children with the label almost unavoidable in any sport.
'hyperactive'. But this little cascade of events shows, In quite a few cases children complain about
too, how minor problems of motor coordination can aching muscles and headaches. Some mention that
get built up till they reach serious proportions and 'my head seems to sit differently on my shoulders'
influence the entire life of such a child and its family. or 'my neck feels lighter tha n before'. Such
When does it make sense to think of a problem comments show how far the reorganization of the
of the vertebral spine as being at the root of these motor system goes. The best strategy is to wait and
disorders? Basically always when coordination leave the child alone. Some analgesics may be
problems, headaches and postural imbalances are necessary, but in most cases a bit of sympathy and
involved. If one finds an impairment of function in a warm compress is sufficient.
these children, a test manipulation should be made The best interval between the treatment and the
to decide if and how much the spine is part of the check-up seems to be 6-8 weeks. It helps to have
problem. It is not for nothing that the word some time after the treatment to enable you to
'posture' has a double meaning. . . judge the effects on your child.

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The opinion of the ( nursery- ) school teachers, already done one of these tests. We do not want to
coaches and physiotherapists is very important to confront them with yet another of these question­
us. Try to get their opinion before you come back naires as such an enquiry reflects on the child's
for the check-up. Based on your report and the self-perception, too.
examination we shall discuss the developments and On one hand we have at our disposal enough
what was achieved. Then we can see what other information to come to a qualified j udgment of the
measures have to be taken - if any. In quite a few child's sensorimotor and intellectual development
cases it suffices to monitor the development of the - at least in most cases. On the other hand these
child rather loosely, i.e. once or twice a year. If ever data are not comparable and to assess the effects
something happens that worries you, these check­ of our therapy we would have to repeat the same
ups can be brought forward. questionnaires or ask the specialists who did the
The following questionnaire [see Figs 14.1-14.3] first tests to repeat them. This is in most cases not
is based on a well-established protocol. The practicable.
questions are necessarily vague, but we shall ask To minimize the impact of such a standard test
you to fil l out such a questionnaire every time you on children and to keep the necessary time within
come back. This has proved very useful for the the constraints of a consultation, we opted for a
follow-up. mixed approach. We ask the parents to fill in the
questionnaire shown in Figures 14.1-14.3 - which
can be done very quickly - and ask the children to
THE MAN DRAWING TEST do a drawing containing a house, a tree and a per­
To assess the actual situation of a schoolchild, a Some examples of the 'before and after ' are
lot of different tests are on offer. Most of them shown in Figures 14.4 and 14.5, and needless to
require quite some time and the aid of a qualified say, not all of the drawings depict these amazing
helper. Most children coming to see us have improvements. The combination of the two types

Grading the activity

Observation Tick the appropriate box (how often)

Not at all A little bit Rather often Always

(0) (1) (2) (3)


Disturbs other children

Short attention span, does not finish the work

Constant fidgeting

Inattentive, easily divertible

Cannot wait. easily disappointed

Cries quickly

Mood changes quickly and drastically

Prone to fits of rage

Starts a lot and does not finish the work

Figure 14.1 Parents' questionnaire. Based on Conners Parent Rating Scale (Sorensen et al 1982).

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Practicalities of manual therapy in children 169

Observation Grading the activity Observation Grading the activity

0 2 3 0 2 3

Restless X Restless X X

Impulsive X Impulsive X

Disturbs other children X Disturbs other children X

Short attention span, Short attention span,
does not finish his work
)( does not finish his work

Constant fidgeting X Constant fidgeting X

Inattentive, easily
)( Inattentive, easily X
divertible divertible

Cannot wait, quickly Cannot wait, quickly

disappointed disappointed

Cries quickly X Cries quickly X

Mood changes quickly Mood changes quickly

and drastically and drastically

Prone to fits of rage X Prone to fits of rage X

Figure 14.2 Completed parents' questionnaire - Figure 14.3 Completed parents' questionnaire -
example 1 ( Daniel, 9 years) . White crosses: parents' example 2 ( Simon, 9 years ) . White crosses: parents'
comments before treatment. Black crosses: parents' comments before treatment. Black crosses: parents'
comments after treatment. comments after treatment.

of information gives us nevertheless some insight the parents to refrain from helping and it is prob­
into the direction of the development since the ably better not to use colors. On one hand one
first visit. Quite often the parents tell us that 'noth­ learns a lot from the use of colors, e.g. if the child
ing really changed' and the comparison of the list is able to limit the coloring to borders. On the
and the drawing says something di tfe rent In put­ . other hand this additional dimension distracts
ting the first and second drawing or questionnaire from the 'hard' information - both arguments
next to each o ther we can use them to discuss with have their merits and we have not yet made any
the parents if their initial comment holds true. We definite decisions about this.
have to keep in mind that some of these develop­
ments are rather slow and that it is difficult for the
parents to be aware of such a gradual improve­ LEAFLET ON POSTURAL PROBLEMS
ment, as they are in contact with their children
every day. Quite frequently these improvements Dear parents,
are more easily seen by an aunt who visits the We all know the situation depicted here [see
family only every few months than by the mother Figs 14.6 and 14.7] - and we all know that it does
or father. not help a lot to tell the child to 'sit straight'.
We started asking for these drawin gs about Twenty to twenty-five seconds later the old posture
4 years ago and in doing so we realized that some is back. Unconscious support of the head during
details have to be standardized, too. The children school lessons is another well-known problem.
have to h ave a good table to sit at, we have to ask Many children in such circumstances start to fidget

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, -------

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,00 00 0 �Q�
I 0
o 0
, � CJ � 00 .. ,. . .

�O 0
00 0
OClOO 00 •
'7 0 CA

t'od � 090)- •
�o��€i2� :
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Figure 14.4 The snowman: these two drawings were

sent by a mother with the comment: 'My son always
drew persons or trees not straight. I got so used to it
that I did not notice it any more. A few days after the
treatment he suddenly was able to draw straight! So I
asked him to make a second drawing of a snowman, Figure 14.5 Two drawings : these two drawings were
which I include here: made 5 weeks apart by a 6-year-old boy.

and wriggle on their chairs. Before we label them patients we found 'special constructions' at the
as 'hyperactive' it might help to think about how neck vertebrae which complicate the situation even
much sitting still we ask of them at a time when further. As long as this posture is only assumed for
mother nature wants them to move around freely. a few moments it does not matter too much. But
The support for the head shown here is in itself in doing homework, children have to sit like that
not bad; the child tries to minimize the stress on for lengthy periods of time - and concentrate on
the passive support structures of the head and we the task at hand, which aggravates the situation
have to be alert to this. A child in such a position further. This stress is not felt as pain by most of the
has to push up to improve its situation. younger children; they tend to complain about
A lot of money is spent on seats, but often the headache or tiredness and less about neck pain.
desk is overlooked. You can do a little experiment During lessons such a tilt desk is not so very
yourself: look at somebody who reads a book or a important, as the attention shifts from the
newspaper which is flat in front of him at a table blackboard and the teacher to the exercise book.
and you can watch how the back of the neck Only during tests should we see to it that the
suffers. Once the book is tilted and in a slightly surface is tilted, too.
sloping position the reader immediately sits Many parents want to do well and buy desks for
straighter. This stress of the support structures is their children which can be tilted entirely. In most
even stronger in people who have soft ligaments - cases, this is a waste of money. Homework is done
as all children do. In quite a few of our young in the living-room, the kitchen or the terrace, but

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Practicalities of manual therapy in children 171

keyboard is often too high, which forces children

to lift their shoulders and overload the neck
muscles. If the children work with material
alongside the screen we should take care that
these papers or books are positioned correctly. If a
book is put next to the keyboard and the gaze
shifts back and forth, the head has to do a
diagonal movement which only the more robust
can handle. Again, this is not that important if
the session lasts only a few minutes. Once
children are in front of a PC for more than 10
minutes these considerations should be taken into
F i gure 14.6 Illustration in po s t u ral problems leaflet
( from a children's book published in 1886).
It is especially important to sit right in front of
the screen. This demand seems superfluous - till
you actually watch your children. You'll be
surprised what you find. ..


The leaflets reproduced above are some of the

material we use to communicate with families , but
it is certainly not everything . The selection pre­
sented here is to give an idea of how to avoid
some of the pitfalls in communication which - if
Figure 14.7 Illustration in pos t u ral p ro b lems lea fl et . not taken care of - may complicate the interaction
needlessly, thus endangering the intended out­
seldom at the - expensive - tilt desk. Even if the come of the treatment.
desk is used, most children refuse to tilt it as The way we interact with families and doctors
everything slides down when they do so. has changed considerably during recent years.
Our proposal is therefore to supply a removable Due to the thousands of children who profited
tilt top which can be carried to where the work is from our treatment we enjoy an amount of good­
done. Children accept it as soon as they realize will (from the doctors) and positive expectations
how much better they can get on with their (from the families) inconceivable some years ago.
homework when such a desktop is used. An angle Some of the leaflets we gave out in the 1980s and
of 200 seems to be optimal. 1990s would be far too timid nowadays, and the
Working with computers: questions asked then ('My GP at home told me
Nowadays, most children start working with there were cases of paraplegia after manual ther­
computers in primary school. Whereas the posture apy in children') do not come up any more, thank­
while working at a computer is in principle better fully. As Gandhi once said, 'First they ignore you,
than at a typewriter, there are quite a few aspects then they laugh at you, then they fight you, then
which can be annoying, from reflections on the you win'. Let us say we are past stage three, but
screen or a flickering screen to a jamming not yet at stage four. This reflects in the way one
keyboard. The height of the support for the has to interact professionally. The question is no

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longer: 'Does this work at all?' but more if and So we do like to stress the point that children
when manual therapy is best applied. should not be given additional treatment immedi­
And, naturally enough, quite a few of those ately after having undergone manual th e rapy In

who ridiculed the potential of manual therapy ini­ order to make parents comprehend that this is nei­
tially switch their position somewhat astonish­ ther out of disregard for the other healing profes­
ingly and tell their patients that there is no need to sions nor to make our contribution more
see a specialist as they are able to do that little bit important than it is, we have to tackle this sensi­
of pushing and cracking themselves. tive subject on a case-by -case basis - so no leaflet
Luckily, parents are quite picky about what and for this (important) subject.
who gets dose to their children, so to protect them To find a balance between these competing
from these self-appointed specialists is the lesser urges - of the parents (to do whatever it takes to
problem. The bigger problem seems to be to con­ help their children) and the manual therapist (who
vince these parents not to do too much. knows that quite frequently less is more) - needs a
T he majority of patients think the quality of an lot of tact and sensitivity. These qualities are as elu­
operation depends only on the skill of the surgeon sive as they are essential to achieve a good thera­
- and the outcome of manual therapy on the tal­ peutic result, and whatever advice one can give is
ents of the specialist. In both cases, the 'before' and only a small and ephemeral detail in a big picture.
'after' are almost as important as the treatment So this quote from Antoine de St Exupery may be
itself. And in both cases, it helps to give the indi­ appropriate to dose this chapter: 'Perfection is
vidual who underwent the treatment time to react achieved, not when there is nothing more to add,
and not start any additional therapy too early. but when there is nothing left to take away'.


SorensenJ L, Hargreaves W A, Friedlander S 1982 Child functioning in a large mental health system. Evaluation
global rating scales: selecting a measure of client Program Planning 5(4):337-347.

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Chapter 15

Manual therapy of the sacroiliac

joints and pelvic girdle in children
Freddy Huguenin

To understand the biomechanics of the pelvic gir­
Introduction 173
dle one must understand its dysfunctions and
Anatomical reminders 173
determine the axes of treatment. T he functional
Analysis of articular stress 176
anatomy includes actual sacroiliac articulations,
Axes of mobility of the pelvic girdle 177
axial sacroiliac articula tion and the pubic bones
Points of diagnosis 178
which constitute the elements of the pelvic gir­
Clinical cases 180
dle. Therapeutic actions, always limited to the
Treatment of the j oints of the pelvic girdle 181
physiological articular interaction, will respond
Direct treatment of the symphysis 182
to a precise palpatory diagnosis based on exami­
nation of the areas of sacroiliac and pubic
irri tation.


Contours of the cartilaginous surfaces of the

sacroiliac articulation. The contour of carti­
lage in vivo has the following fea tures (Fig. 15.1):

• On the iliac side: depression of upper and lower

limbs, depression of the middle anterior
pole .
• On the sacraL side: elevations corresponding to
the depressions of the iliac side.

The consequence of these articular poles - which

bring about an interlocking of cartilage - is that
only sliding movements are possible. A reduced
range of rotation is only possible at the price of a
light opening of articulation.

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Figure 15.1 Elevations and

depressions on the articular .

surface of the sacroiliac joint, ......

.. ..

according to H. Weisl. 1, Elevations

of the sacra I su rface. 2,
Depressions of the iliac surface
(adapted with permission from
Weisl H 1954 The articular
surfaces of the sacroiliac joint and
their relation to the movement of
the sacrum. Acta Anatomica
(S. Karger AG, Basel) 22:1-14).

Elevations of the sacral surface

Depressions of the iliac surface

Fig ure 15.2 Axial sacroiliac joint

according to Bakland. S, sacral
cavity; P, prominence (pyramide .--'

iliaque) (adapted from Bakland 0,

Hansen J.H 1984 The axial sacro­
iliac joint. Anatomica Clinica 6:

S - Sacral cavity
P - Prominence (pyramide ilia que)

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Manual therapy of the sacroiliac joints and pelvic girdle 175

Axial sacroiliac j oint. The sacroiliac articula­

tions are certainly among the most complex artic­
ulations of the locomotive system. Their classic
anatomical description most often ignores the
axial sacroiliac articulation, the 'Nebengelenk­
flache am Kreuz-und Huftbein' (accessory joints
at the sacrum and ilium) of the German literature
(Luschka 1858). Without going into too much
detail we can look back to 1753 to find the descrip­
tion by Albinus of an articular surface of the sacnun
corresponding to a tubercle of the iliac bone. In 1864
Luschka described articular surfaces in sockets on Figure 15.4 Sacral cavity (creux socrel and iliac
the sacral side raised on the iliac side which can be prominence (pyramide ilioque) (from Rouviere 1932).
considered as a transversarius accessorius process
of the second sacral vertebra. Petersen in 1905, without an articular capsule (Figs 15.2-15.4). This
Derry in 1911, Jazuta in 1 9 29, Seligmann in 1935, axial sacroiliac articulation has limited mobility
Trotter in 1940 and 1964, Hadley in 1952 and 1973, (Fig. 15.5). Its ligament (the axial ligament) goes
and Bakland in 1984, gave detailed descriptions of from the iliac pyramid to the first joint tubercle
the axial sacroiliac articulation. Bakland and I (Fig. 15.6).
even tried to understand the role that it could play
in the biomechanics of the pelvic girdle. The pubic bones. The pubic bones are part of the
The iliac prominence (pyramide iliaque in articular system of the pelvic girdle. The y have
French), described a long time ago by anatomists all the characteristics of an articulation and are
(Testut and Jacob 1893, Rouviere 1932), is articu­
lated with a sacral cavity, encrusted with cartilage,

Figure 15.5 Limitations of mobility of the sacroiliac
joint( red ra w n from O. Bakland's dra w i ng , kindly authorized
Figur e 15.3 The iliac prominence (pyramide iliaque) by the author). 1, Depth of sacral cavity; 2, height of
(from Rouviere 1932). prom inence; 3, cephalic joint p l ay; 4 caud a l joint play.

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Figure 15.7 Stresses. K, weight of the body; X-X, plane

of the pelvic ring; Y-Y, plane perpendicular to X-X; Kx
Figure 15.6 The axial ligament (from Testut and Jacob and Kv components of the action of the weight of the
1893). body on the pelvis (from Testut and Jacob 1893).

made up of ligaments, which c orr esp ond to frena fold: shea ring, compression and ventralization
of movement. (Figs15.8 and 15.9).
These obse rv ati ons according to Pau w ell s (1948)
Ligaments. Th e entire sacroiliac and pubic bones match clinical findings: if one of thes e components
ligament system responds to cons train ts described is blocked, the conditions of functional pa tholog y
by P auwel s (1948), in the standing pos ition as well are met. The treatment m ust aim at correcting these
as in monopodal s upp o rt (Figs 15.7-15.9). impaired movements according to the laws of
mobili ty of the pelvic girdle. The s acro i li ac j oint
must therefore be con side red as a four-pole articu­
ANALYSIS OF ARTICULAR STRESS lation (Fig. 15.2). The actual sacroiliac a rt i culat i on is
limited to sliding movements. The axial sacroiliac
Stresses at the sacroili ac level are compressions in articulation limits the movements of flexion and
their lower pa r t a nd o p enin gs in the upper part extension of the sacrum and iliac wings and allows
thereby bringing ab o u t the c ond i ti ons of a sl iding for minimum rotation. Articulation of the pubic
rotation at each monopodal supp ort . (Fig. 15.8). At bones is involved in all movements of the iliac
the level of the pubic bones, the stresses are three- w ings in relation to one an other .

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Manual therapy of the sacroiliac joints and pelvic girdle 177

Figure 15.8 Joint stresses in t he Y plane. Figure 15.9 Joint stresses according to the X plane.

AXES OF MOBILITY OF THE axis passes in front of the left ischio-pubic leg,
PELVIC GIRDLE under the right sciatic indentation, behind the
right iliac wing.
In order to understand diagnostic maneuvers and Extending the thigh (counter-nutation of the
manipulations of the pelvic girdle, it was necessary corresponding iliac wing, Fig. 15. 12): at a rotation
to experiment with the axes of mobility. This is what of 2°, the axis of extension passes in front of the
Lavignolle et al did, firstly on cadavers, then in vivo right ischio-pubic leg, over the left ischio-pubic
(Lavignolle et aI1983). The results of their research leg, behind the ilium, and at the level of the coty­
exactly match clinical work and agree with the loid brow of the left acetabular socket.
methods of treatment proposed here. The determi­ Mobility of the iliac wings in relation to one
nation of working axes, bending the right thigh at another (Fig. 15.13): the relative rotation of the
60° and extending the left thigh at ISO, has to be iliac wings is 10°. The left-right iliac wing axis
perfomed before measuring the ranges of rotation passes across the left obturator hole, behind the
(Fig. 15.10). two ischio-pelvic legs, and at the level of the coty­
Experiments on humans show the following loid brow of the right acetabular socket.
results. Crossing of the working axes (Fig. 15.14): all the
Bending the thigh (nutation of the correspon­ axes cross one another at the level of the pubic
ding iliac wing, Fig. 15.11) at a rotation of 12°: the bones at a point that Lavignolle calls the instanta-

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60° Flexion

System of

System of
measurement ::::-
l-----4:::--- i-r=---

' - -:-:-.

15° Extension

Figure 15.10 Experimental data retrieval of Lavignolle et al (1983).

neous center of rotation in the sagittal plane. and become painful This fact led to our palpation

The axes of rotation have a quasi-constant posi­ examination of the pu bic quadrilaterals, since a
tion in relation to each other. lockmg always appears as the support of a part of
Previous rotations of the pubic quadrilaterals the quadrilateral that was previously moved.
(Fig. 15.15): Lavignolle et al (1983) found a move­
ment of anterior rotation of the pelvic quadrilat­
eral of about 6 mm from the side with the bend, 4 POINTS OF DIAGNOSIS
mm from the side with the extension. The result
between the two iliac wings is 2 mm from the At the sacroiliac level (Fig. 15.16) direct palpation
right pubic quadrilateral (Fig. 15.15). These rota­ is not possible. On the contrary, during a dysfunc­
tions are physiological when they are reversible tion the multifidus muscle (spinal crossing) which
during movements. They become significant with joins the sacrum at Ls and L4 presents a tendinosis
respect to functional pathology when they persist which corresponds to one of the poles of the dys-

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Manual therapy of the sacroiliac joints and pe lvic girdle 179


Figure 15.13 Mobility of the iliac wings in relation to

Figure 15.11 Bending the thigh: a rotation of 12°. The one another: the relative rotation of the iliac wings is
bending axis passes in front of the left ischia-pubic leg, 10°. The left-right iliac wing axis passes across the left
under the right sciatic indentation, behind the right obtu rator hole, behind the two ischia-pelvic legs, and at
iliac wing. the level of the cotyloid brow of the right acetabular
socket. F, flexion; E, extension.

Figure 15.12 Extending the thigh: a rotation of 2°. The

axis of extension passes in front of the right ischia-pubic Instantaneous centre of rotation
leg, over the left ischia-pubic leg, behind the ilium, at in sagittal plane
the level of the cotyloid brow of the left acetabular
Fig u re 15.14 Crossing of the working axes:
instantaneous center of rotation.

functional sacroiliac. These points, described by muscle. It is probable that insertions into the sacro­
Max Su tter (1973, 1975), are situated on the back­ tuberale ligament are also sensitive to palpation on
side of the sacrum, exactly on the intersecting line the free edge of the sacrum and on the posterior
of the insertions into the aponeurosis of the large superior iliac spine.
buttock with the insertions into the multifidus

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F 12°

--,-L -- s
J'-_--f--- S1
1t'\,....;iJ.--+--- S2

R 2mm L

Figure 15.15 Previous rotations of the pubic

quadrilaterals. The result between the two iliac wings is
a prominence of 2 mm from the right pubic quadrilateral Aponeurosis: • Areas of sacroiliac
(right 6 mm - left 4 mmJ . • Multifidus irritations zone

• Gluteus maximus o Ls Irritation zone

• Gluteus medius • Tendinosis in the

middle buttock
These pa lpa t i on points designated 51' 52' and Q Sacrotuberale ligament
53 are what we call the areas of irritation. It is Fig ur e 15.16 Areas of sacroiliac irritation of the Ls'
also interesting to note that painfu l points on tendinosis of the middle buttock corresponding to the
insertions into the average buttock can move dysfu nctions from Ls to T12 (D1J m, multifidus muscle;
G, gluteus maximus; M, gluteus medius; S,
thoracic-lumbar dysfunctions from T12 to Ls
sacrotuberale ligament.
(Fig. 15.16).
At the pubic quadrilateral level (Fig. 15.17) the
palpati on is done on the internal edge of the right
Treatment of the pelvic girdle and of the
and left quadrilateral which, in functional atlanto-occipital dysfunction immediately allowed
pathologies, is backward, anterior, irritating the the child to kee p his balance. Only one treatment
transversal anter io r ligament system which is felt
was necessary.
by the pa tie nt as a needle prick for a pressure of
100 grams. These points of palpa tion named PI' P2 Eight-year-old boy: His behavior did not lead us to
and P3 are what we call areas of irritation. It must
suspect any anomaly. But when the child tried to
be noted that a stretching 'block' is expressed by
maintain his balance on a wooden fence and to
PI' that of bending by P3, and that a conflict
walk on it, he rapidly lost his balance. A clinical
between the two il i a c wings is a P2'
examination revealed a dysfunction of the pelvic
girdle. The treatment according to the pubic bones
of P3 corrected functionality and the child could
walk the 10 meters of the fence without losing his