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Sports Med 2004; 34 (14): 1005-1017

REVIEW ARTICLE 0112-1642/04/0014-1005/$31.00/0

 2004 Adis Data Information BV. All rights reserved.

Biomechanics and Pathophysiology of


Overuse Tendon Injuries
Ideas on Insertional Tendinopathy
Constantinos N. Maganaris,1 Marco V. Narici,1 Louis C. Almekinders2 and
Nicola Maffulli3
1 Institute for Biophysical and Clinical Research into Human Movement, Manchester
Metropolitan University, Alsager, UK
2 North Carolina Orthopaedic Clinic, Duke University Health System, Durham, North
Carolina, USA
3 Department of Trauma and Orthopaedic Surgery, Keele University School of Medicine, North
Staffordshire Hospital, Hartshill, Stoke-on-Trent, UK

Contents
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1005
1. Functional and Clinical Relevance of Tendon Tensile Behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1006
1.1 In Vitro Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1007
1.2 Disuse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008
1.3 Physical Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008
1.4 Aging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1008
1.5 Corticosteroids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1009
1.6 Limitations of In Vitro Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1009
1.7 In Vivo Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1009
2. Overuse Tendinopathy in Sports: the Biomechanical Issue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1011
2.1 Traditional Concepts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1012
2.2 Clinical Challenges to the Traditional Concept . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1013
2.3 Biomechanical Challenges to the Traditional Concept . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1013
2.4 Alternative Biomechanical Theories in Insertional Tendinopathy . . . . . . . . . . . . . . . . . . . . . . . . . 1014
3. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1014

Abstract Tendons behave viscoelastically and exhibit adaptive responses to conditions


of increased loading and disuse. High-resolution, real-time ultrasound scanning
confirms the applicability of these findings in human tendons in vivo. In addition,
recent biomechanical studies indicate that strain patterns in tendons may not be
uniform, as tendons show stress-shielded areas and areas subjected to compressive
loading at the enthesis. These areas correspond to the sites where tendinopathic
characteristics are typically seen. This indicates that some tendinopathies may,
paradoxically, be considered as ‘underuse’ lesions despite the common beliefs
that they are overuse injuries. Classic inflammatory changes are not frequently
seen in chronic athletic tendon conditions and histopathology features in tendi-
nopathic tendons are clearly different from normal tendons, showing an exagger-
ated dysfunctional repair response. Tendinopathies are traditionally considered
overuse injuries, involving excessive tensile loading and subsequent breakdown
of the loaded tendon. Biomechanical studies show that the strains within the
tendons near their insertion site are not uniform. If the material properties are
1006 Maganaris et al.

similar throughout the tendon, forces transferred through the insertion site prefer-
entially load the side of the tendon that is usually not affected initially in
tendinopathy. In that case, the side affected by tendinopathy is generally ‘stress
shielded’. Thus, the presence of differential strains opens the possibility of
alternative biomechanical explanations for the pathology found in these regions of
the tendon. The traditional concept of tensile failure may not be the essential
feature of the pathomechanics of insertional tendinopathy. Certain joint positions
are more likely to stress the area of the tendon commonly affected by tendi-
nopathy. Incorporating different joint position exercises may exert more con-
trolled stresses on these affected areas of the tendon, possibly allowing better
maintenance of the mechanical strength of that tendon region and, therefore,
prevent injury. Such exercises could stress a healing area of the tendon in a
controlled manner and thus stimulate healing once an injury has occurred.
Additional work is needed to prove whether such principles should be incorporat-
ed in current rehabilitation techniques.

Tendinopathies are common in elite and recrea- the sarcomeres operate in the ascending limb of the
tional athletes. Although acute traumatic conditions force-length relation, a more extensible tendon will
such as ligament and muscle tears receive much result in less contractile force. In contrast, if the
attention in the general literature, tendinopathies sarcomeres operate in the descending limb of the
account for much of the lost time in practice and force-length relation, a more extensible tendon will
competition.[1,2] The aetiology and much of the treat- result in greater contractile force.[3]
ment of tendinopathy is largely based on our under- Secondly, a non-rigid tendon may complicate the
standing of the biomechanical behaviour of tendons. control of joint position.[4] If one considers, for
This article reviews studies on the biomechanical example, an external oscillating force applied to a
behaviour of tendons. An understanding of tendon joint at a certain angle, trying to maintain the joint at
biomechanics is needed to understand the clinical a fixed position would require the generation of
features of tendinopathy and may allow us to move constant contractile force in the muscle. If the ten-
forward with new and innovative approaches to this don is very compliant, its length will be changed by
common problem. the external oscillating load, even if the muscle
length is held constant. This will result in failing to
1. Functional and Clinical Relevance of maintain the joint at the desired angle.
Tendon Tensile Behaviour
Thirdly, the work done to stretch a tendon is
The primary role of tendons is to transmit con- stored as elastic energy and most of this energy is
tractile forces to the skeleton to generate joint move- recovered once the tensile load is removed and the
ment. In doing so, however, tendons do not behave tendon recoils. This passive mechanism of energy
as rigid bodies but exhibit a time-dependent extensi- provision operates in some of the tendons of the
bility. This has important implications for muscle lower extremity of legged mammals during terrestri-
and joint function, as well as for the integrity of the al locomotion, thus saving metabolic energy other-
tendon itself. wise needed to displace the body ahead.[5] Energy is
Firstly, the elongation of a tendon during muscle also ‘dissipated’ in the form of heat, but this effect is
contraction will result in muscle shortening. For a small and does not endanger the integrity of a tendon
given contractile force, a more extensible tendon in a single stretch-recoil cycle. However, in tendons
will allow greater muscle shortening. The outcome that stretch and recoil repeatedly under physiologi-
of the resultant extra sarcomeric shortening on the cal conditions (for example, again, the lower-ex-
contractile force elicited would depend on the region tremity tendons of legged mammals during terrestri-
over which the sarcomeres of the muscle operate. If al locomotion), the heat lost may result in cumula-

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
Tendon Pathomechanics 1007

tive tendon thermal damage and injury, predisposing the tendon by reducing the crimp angle of the colla-
the tendon to ultimately rupture. Indeed, in vivo gen fibres at rest, but they do not cause further fibre
measurements and modelling-based calculations in- stretching. Hence, loading within the ‘toe’ region
dicate that spring-like tendons may develop during does not exceed the tendon elastic limit. Further
exercise temperature levels above the 42.5°C thresh- elongation brings the tendon into the ‘linear’ region
old for fibroblast viability.[6] These findings are in II, in which elongation results from stretching the
line with the degenerative lesions often observed in already aligned fibres by the load applied in the
the core of tendons acting as elastic energy stores, preceding ‘toe’ region. At the endpoint of this re-
indicating that hyperthermia may be involved in the gion, some fibres start to fail. Elongation beyond the
pathophysiology of exercise-induced tendon trau- ‘linear’ region brings the tendon into region III,
ma. where additional fibre failure occurs in an unpredict-
To quantify the tensile behaviour of tendons and able fashion. Further elongation brings the tendon
assess the above effects, numerous in vitro and in into region IV, where complete failure occurs.[7-13]
vivo studies have been performed. To account for inter-specimen dimensional dif-
ferences when interpreting force-elongation curves,
1.1 In Vitro Testing tendon forces are reduced to stress values (MPa) by
normalisation to the tendon cross-sectional area and
The mechanical properties of tendons have been tendon elongations are reduced to strain values (%)
studied mostly using tensile testing methodologies by normalisation to the tendon original length. The
in which isolated tendon specimens are stretched by stress-strain curve obtained is similar in shape to the
an external force, while both the specimen deforma- force-elongation curve, but it reflects the intrinsic
tion and the applied force are recorded.[7-9] Such material properties rather than the structural proper-
methodologies are considered to adequately mimic ties of the tendon specimen. The most common
the way that loading is imposed on several tendons material variables taken from a stress-strain curve
in real life. under elongation-to-failure conditions are the
The tensile tests produce a force-elongation Young’s modulus (GPa) and the ultimate stress
curve (figure 1). In force-elongation curves, slopes (MPa) and strain (%). Young’s modulus, the product
relate to stiffness (N/mm) and areas to energy (J). In of stiffness multiplied by the original length-to-
elongation-to-failure conditions, four different re- cross-sectional area ratio of the specimen, reaches
gions can be identified in the tendon force-elonga- 1–2 GPa at stresses exceeding 30 MPa.[8,14-16] Ulti-
tion curve (figure 1). Region I is the initial concave mate tendon stress (i.e. stress at failure) and strain
portion of the curve and it is referred to as the tendon (i.e. strain at failure) reach ~100 MPa and 4–10%,
‘toe’ region. Loads within the ‘toe’ region elongate respectively.[8,11,12,14,15]
IV
If a tendon is subjected to a tensile load, it does
I II III
not behave perfectly elastically, even if the load
applied is lower than that required to cause failure.
Because of the time-dependent properties of the
tendon’s collagen fibres and interfibre matrix,[17,18]
the entire tendon exhibits force-relaxation, creep
and mechanical hysteresis.[7-11] Force-relaxation
Force

means that the force required to cause a given elon-


gation decreases over time. The decrease in force
follows a predictable curvilinear pattern (figure 2).
Creep is the analogous phenomenon under constant-
Elongation
force conditions. In this case, deformation increases
Fig. 1. Typical force-elongation curve of a tendon pulled by a load
over time curvilinearly (figure 2). The presence of
exceeding the tendon elastic limit. I = toe region; II = linear region; mechanical hysteresis is evidenced in force-elonga-
III and IV = failure regions. tion and stress-strain plots during loading and subse-

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
1008 Maganaris et al.

a
the amount of elastic strain energy lost as heat upon
Stretch application recoil and it is usually expressed in relative terms
(%) with respect to the total work done on the
tendon during stretching. Mechanical hysteresis val-
ues in the range of 5–25% have been reported, with
most values concentrated around the value of
Force

10%.[14-16,19,20]
Several factors may alter the mechanical re-
sponse of tendons, the most important of which are
discussed in the following sections.

1.2 Disuse
Time
b Most studies show that limb immobilisation, sus-
pension and denervation decrease tendon stiffness,
ultimate strength and energy-to-failure.[8,21-24] These
changes are attributed to specimen atrophy and
changes in the specimen material properties. Disuse-
Elongation

induced changes in intrinsic material properties are


Force application
associated with increased collagen turnover and re-
ducible cross-linking, decreased glycosaminoglycan
and water content, and increased non-uniform orien-
tation of collagen fibrils.[8,12,13,21,23,25,26]

1.3 Physical Activity

c
Time Most of the studies report that long-term physical
activity improves the tensile mechanical properties
of tendons, yielding results opposite to those of
disuse.[8,21,24,27,28] Hypertrophy may partly account
Hysteresis
for these effects, but changes in the tendon Young’s
modulus also indicate training-induced changes in
Force

the tendon intrinsic material properties. Such bio-


chemical and structural changes include increased
glycosaminoglycan content, decreased collagen re-
ducible cross-linking and increased alignment of
collagen fibres.[8,12,13,21,23,25,26]

1.4 Aging
Elongation
Fig. 2. Force-relaxation (a), creep (b) and mechanical hysteresis Some cross-sectional studies have shown that
(c). The arrows on the bottom graph indicate loading and unloading aging may result in intrinsically stiffer, stronger and
directions. more resilient tendons,[15,29] while others have chal-
lenged these results.[30-33] This inconsistency may be
quent unloading of the specimen. Larger tendon partly accounted for by inter-study differences in the
deformations are taken during recoil than stretch at age of the younger group examined, with compara-
given loads, yielding a loop (the hysteresis loop) tive results involving very young animals,[15] poten-
between the curves in the loading and unloading tially representing the effect of biological matura-
directions (figure 2). The area of the loop represents tion and development rather than aging.

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
Tendon Pathomechanics 1009

Distal bone Proximal bone


1.5 Corticosteroids
Muscle
Corticosteroids have frequently been used for the Tendon

treatment of tendinopathy, despite the dubious ratio-


nale for their use in these conditions.[34] Intra-articu-
Markers
lar and intracollagenous injections of corticosteroid Stimulating
may reduce the stiffness, ultimate stress and energy- Load cell electrodes

to-failure of collagenous tissue, predisposing the Fig. 3. Experimental set-up to measure the mechanical properties
user to tendon injuries even after short-term admin- of animal tendons in situ. The proximal and distal bones are
clamped and loading is imposed by stimulation. The resultant
istration.[35-37] forces are measured by a load cell placed in series with the muscle-
tendon complex. The resultant elongation in the tendon is obtained
1.6 Limitations of In Vitro Testing from displacement measurements of markers attached on the ten-
don.
Although in vitro tests clearly show that tendons
behave viscoelastically on tension, reference to the ties of a tendon? Also, how long does it take before
quantitative results of such tests when interpreting in the mechanical properties of an immobilised tendon
vivo function should be treated with caution. This is start to deteriorate? Moreover, an in vivo method
because: (i) the forces exerted by maximal tendon might be of direct clinical use. Consider, for exam-
loading under in vivo conditions may not reach the ple, surgical procedures involving limb lengthening
‘linear’ region in which stiffness and Young’s mod- and tendon transfer. Any change in the resting-state
ulus measurements are taken under in vitro condi- length of the tendon will alter its extensibility and
tions; (ii) to perform a tensile test in vitro, clamping this will clearly affect the function of the in-series
of the specimen is necessary. Fixing a fibrous struc- muscle. Therefore, protocols for assessing the me-
ture with clamps is inevitably associated with fibre chanical properties of a tendon in vivo could provide
slippage and/or stress concentration that may result crucial help for optimising the outcome of a correc-
in premature rupture; (iii) many in vitro experiments tive surgery. For example, they could be used for
have been performed using preserved tendons, measurements in the tendon of the contralateral
which may have altered properties.[38,39] healthy limb of a patient, thus providing reference
Some of the above problems have been circum- values that could then be used to guide clinical
vented by testing animal tendons in situ, after the decision making.
animal has been killed or anaesthetised.[40,41] This
has been achieved by surgically releasing the tendon 1.7 In Vivo Testing
from its surrounding tissues, maintaining the proxi-
mal end of the tendon attached to the in-series Adapting similar principles to those used under
muscle and gripping the distal bone of the muscle- in situ material testing has recently allowed the
tendon unit with a clamp interfaced to a load cell. development of a non-invasive method for assessing
The in situ muscle preparation is made to contract by the mechanical properties of human tendons in vivo.
electrical stimulation, thus pulling on the tendon, The in vivo method is based on real-time ultrasound
which lengthens as a function of the contractile scanning of a reference point along the tendon dur-
force applied to its proximal end in a similar fashion ing static contraction of the in-series muscle (figure
to that obtained when the actuator of a tensile ma- 4). The limb is fixed on the load cell of a dynamom-
chine pulls an isolated specimen (figure 3). Clearly, eter to record changes in joint moment occurring
however, such in situ protocols are inapplicable to during activation and subsequent relaxation in a
humans. To overcome this problem, the develop- maximal isometric contraction. The joint moments
ment of an in vivo non-invasive method is needed. recorded correspond to muscle forces that can be
This would allow the design of longitudinal studies calculated from the moment equilibrium equation.
aimed to answer fundamental questions with clinical The muscle forces generated by activation pull the
implications. For example, which training regime is tendon proximally and cause a longitudinal defor-
most effective in enhancing the mechanical proper- mation, which is measured by the recorded displace-

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
1010 Maganaris et al.

TA tendon ment of a reference landmark in the tendon. On


relaxation following activation, the tendon recoils
and the reference landmark traced shifts distally
a (figure 4). The force-elongation plots obtained dur-
ing loading-unloading can be reduced to the respec-
tive stress-strain plots by normalisation to the
dimensions of the tendon, which can also be mea-
sured using ultrasonography. Coefficient of varia-
b tion values of <12% have been obtained in repeated
measures using the in vivo method.[42-49]
By following the above steps, we showed that: (i)
young adult Achilles and tibialis anterior tendons
have similar values of Young’s modulus (~1.2 GPa)
c and mechanical hysteresis (18%);[42-44] (ii) Achilles
tendons in young adults are liable to increasing
elongations in the initial few cycles or repeated
loading-unloading;[50,51] (iii) the Achilles tendons of
older people (69–80 years) are intrinsically more
d
compliant by 14% than the same tendons in young
adults;[52] (iv) 90 days of bed rest reduces the
Young’s modulus of Achilles tendons in young
adults by ~30%;[53] (v) strength training in old age
(68–79 years) increases the Young’s modulus of the
patellar tendon by ~70%, which results in increasing
e
the rate of force development by 27% and decreases
the mechanical hysteresis of the tendon by
27%.[54,55]
In interpreting finding (i), it should be stressed
the tibialis anterior and Achilles tendons are subject-
f
ed to different physiological forces. The tibialis
anterior tendon is subjected to the forces generated
by controlling plantarflexion in the early stance
phase of gait and the Achilles tendon to the high
forces generated in late stance. In vivo measure-
g ments of tendon force indicate that the Achilles
1cm tendon may carry up to 110 MPa in each stride
Distal end Proximal end during running.[56] This stress not only exceeds the
Fig. 4. Typical in vivo sonographs of the human tibialis anterior (TA) tendon stress during maximal muscle contraction in
tendon. The white arrows point to the TA tendon origin. The black
double arrows point to the shadow generated by an echoabsorptive
our experiments (~30 MPa), but it also exceeds the
marker glued on the skin to identify any displacements of the scan- average ultimate tensile stress of 100 MPa reported,
ning probe during muscle contraction-relaxation. The tendon origin thus highlighting the possibility of Achilles tendon
displacement is larger during relaxation compared with contraction rupture in a single pull in real life. Epidemiological
at each loading level, indicating the presence of mechanical hyster-
esis in the tendon (reproduced from Maganaris and Paul,[43] with
studies of spontaneous tendon rupture verify these
permission). (a) resting state; (b) 40% of maximal loading during theoretical considerations.[57] Another difference be-
contraction; (c) 80% of maximal loading during contraction; (d) tween the two tendons concerns their ability to pro-
100% of maximal loading during contraction; (e) 80% of maximal vide mechanical work. In contrast to the tibialis
loading during relaxation; (f) 40% of maximal loading during relaxa-
tion; (g) 0% of maximal loading during relaxation. anterior tendon, the Achilles tendon acts as energy
provider during locomotion. Most of the work im-

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
Tendon Pathomechanics 1011

posed on the tendon by the initial ground force is • to have a truly valid association between the
recovered as elastic strain energy during push-off, tendon force estimated and the elongation mea-
which results in plantar-flexing the ankle and thus sured, the reference point whose displacement is
accelerating the body forward at no metabolic traced must be within the free (extramuscular)
cost.[5] Notwithstanding the above differences be- part of the tendon.
tween the two tendons, the Achilles tendon was Such points are the tendon origin in the my-
found to be neither intrinsically stiffer nor more otendinous junction,[42-44] the osteotendinous junc-
rebound resilient than the tibialis anterior tendon, tion (for example, in the patellar tendon[54,55]), or the
which agrees with in vitro findings.[16,58] Thus, it echo generated by artificial markers inserted in the
seems likely that adjustments in tendon structural tendon.[59] If, instead, an anatomical point within the
properties to physiological loading are accom- intramuscular aponeurosis is selected, the above as-
plished by adding or removing material rather than sociation becomes invalid because the contractile
altering the material intrinsic properties. force by which the intramuscular marker is pulled is
Finding (ii) is also in agreement with in vitro clearly less than that exerted by the whole muscle.
results. The relevant phenomenon is referred to as These two important points have often been ne-
‘conditioning’ and it has been considered as an glected (see table I). However, even if measure-
artifact because of specimen slippage in the ments are taken appropriately, some inherent prob-
clamps.[9] In contrast, our in vivo results show that lems cannot be avoided. The two most important
conditioning is an actual physical property of the limitations are:
tendon. A consequence of the increasing elongation • the application of non-homogeneous stress
of the tendon was that the fascicles of the in-series across the tendon by a contraction of increasing
muscle shortened by ~12%. Calculations based on or decreasing intensity;
the cross-bridge model indicated that the resultant • incorporation of heat losses by surface friction
changes in myofilament overlap might reduce the between the tendon and adjacent tissues, which
force-generating potential of the muscle by ~10%, a would be reflected in the area of the hysteresis
decrease that could be mistaken for evidence of loop.
neuromuscular fatigue. In fact, the average mechanical hysteresis esti-
The findings (iii), (iv) and (v) have implications mates obtained in vivo (18–25%) are higher than the
for locomotor function and exercise rehabilitation in average value of ~10% obtained from tensile tests
the elderly and other frail populations. They high- on isolated tendons.[9,14,16] However, we do not
light the deteriorating effects of aging and disuse on know whether the above discrepancy can be entirely
tendon function, but they also indicate that training accounted for by heat losses from sources other than
may be an effective countermeasure to regain or the tendon or whether it partly reflects differences in
prevent loss of functional integrity. Stiffening of the tendon material properties between in vivo and in
tendon by training would allow transmission of con- vitro conditions.
tractile forces to the skeleton more rapidly, as indi-
cated by the increased rate of force development, 2. Overuse Tendinopathy in Sports: the
which might be crucial when reacting to a trip, slip Biomechanical Issue
or other fall-related accident.
Two methodological issues require particular at- Biopsy studies have shown that classic inflam-
tention when obtaining the tensile response of a matory changes are not frequently seen in chronic
human tendon in vivo: tendon conditions and that histopathology features
• to accurately estimate the force acting along the in tendinopathic tendons are clearly different from
tendon studied, the presence of synergist and normal tendons.[61-63] The exact pathophysiological
antagonist muscles that span the relevant joint processes that can occur within tendons have yet to
must be accounted for by appropriate corrections be determined. Several different forms of tendi-
of the net joint torque recorded by the dynamom- nopathy have been described, and the anatomical
eter; location of a given lesion within the tendon plays a

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
1012 Maganaris et al.

Table I. Ultrasound-based results and protocols regarding the tensile response of several human tendons in vivo
Tendon Load (MPa) Elongation (%) Marker Synergistic Antagonistic Reference
actiona actiona
Tibialis anterior 12.4 4.3 IMF Yes No 60
25 2.5 MTJ Yes Yes 43
Vastus lateralis 31.9–33.4b IMF Yes No 45
5843c 12.7b IMF Yes No 49
Patellar tendon 40–42 5.9–9.9 OTJ Yes Yes 53
Triceps surae 41.6 4.4–5.6 IMF No Yes 48
Achilles tendon 36.5 8 ITM No Yes 59
Gastrocnemius 398–406c 8.1–8.6 IMF Yes No 46
32.4 4.9 MTJ Yes Yes 44
a ‘Yes’ and ‘no’ denote incorporation and non-incorporation, respectively, of the relevant effect in the calculation of tendon load.
b Expressed in absolute terms (mm).
c Expressed as force (N).
IMF = intramuscular fascicle; ITM = intratendon marker; MTJ = myotendinous junction; OTJ = osteotendinous junction.

role in determining the type of tendinopathy. Chron- retically occur in several ways. Training errors have
ic tendon abnormalities consistent with tendi- frequently been considered as being an aetiological
nopathy can be found in the main body of the factor.[68,69] A given tendon has a baseline mechani-
tendon, its insertion site on bone (the enthesis) and cal strength, dependent on the loading history of the
the structures surrounding the tendon. These differ- tendon, as the tendon will adapt to the loads placed
ent abnormalities can co-exist within the same ten- upon it. If the loading has been low, or of limited
don. frequency or duration, the tendon mechanical
All tendons can be affected by tendinopathies.[64] strength will be relatively limited. If a rapid increase
The supraspinatus, common wrist extensor, quadri- in training load, frequency and/or duration occurs,
ceps, patellar, posterior tibialis and Achilles tendons the tendon may not be able to adapt fast enough to
are probably the most commonly affected tendons. this increase. The mechanical strength of the tendon
Insertional tendinopathy (or enthesiopathy) is one of may be exceeded and a small injury may ensue,
the most common forms of tendinopathy. In particu- although it is not well understood how this small
lar, the supraspinatus, common wrist extensor, injury progresses. Theoretically, repeated microin-
quadriceps and patellar tendon are almost exclusive- juries may occur and the tendon may be able to heal
ly affected by insertional tendinopathy. The Achilles a certain level of microinjury. However, as training
tendon, on the other hand, can present tendinopathy and heavy loading of the tendon continues, this
of the main body of the tendon, paratendinopathy healing process may be overwhelmed and a greater
and insertional tendinopathy, each with different injury ensues. At some point, the injury becomes
clinical features and management implications. Re- clinically apparent through pain in the involved ten-
cent reviews on tendinopathy of the main body of don.
major tendons have been published.[65,66] Sections
2.1 to 2.4 focus on insertional tendinopathy and Other factors besides training errors may lead to
discuss the possible pathomechanics in the aetiology increased loading of the tendon, such as poor tech-
of these tendon disorders. nique[70,71] or inadequate athletic equipment.[72,73]
Also, intrinsic factors, such the status of the mus-
2.1 Traditional Concepts cles, ligaments and bones surrounding the tendon,
may alter the level of the load on the tendon. Some
Tendinopathies are typically considered overuse of these factors, such as muscle strength and flexi-
injuries. This concept involves excessive loading of bility of the ligaments and muscle-tendon units, are
the tendon and subsequent mechanical breakdown variable. Lack of flexibility and muscle imbalances
of the loaded tendon.[67] Excessive loading can theo- are frequently mentioned in the aetiology of tendi-

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
Tendon Pathomechanics 1013

nopathies.[74,75] Other intrinsic factors, such as limb in the supraspinatus (rotator cuff tendinopathy),
alignment and body habitus, are more or less fixed. common wrist extensor (lateral epicondylitis), patel-
Regardless of the factors involved in the develop- lar (jumper’s knee) and Achilles tendons. All these
ment of a tendinopathy, the traditional concept cen- tendons are relatively thick, they insert at an oblique
tres around increased tensile loads on the tendon as a angle in the bone and have a broad insertion
result of these. Excessive tensile loads are capable of site.[88-92] Initial or partial tearing of the supras-
causing plastic deformation and eventually rupture pinatus is found generally on the humeral side rather
of the tendon.[76] In tendinopathy, the tensile loads than bursal side.[92] Lateral epicondylitis and
are presumed to be large enough to cause some jumper’s knee can be approached from the joint side
plastic deformation, the biomechanical equivalent with arthroscopic techniques.[93,94] Finally, tendon
of a microinjury, but not complete failure. Repeated pathology in insertional Achilles tendinopathy is
episodes of minor plastic deformation may add up to generally found at the calcaneal side.[95] Thus, the
a clinically significant macroinjury. pathology is predominantly found at the joint side of
the enthesis.
2.2 Clinical Challenges to the The enthesis transfers the mechanical tensile
Traditional Concept loads generated by the muscle-tendon unit onto the
bone through a thick tendon, which inserts at a
The traditional view of a tendon overuse injury as varying, oblique angle, depending on the position of
a result of tensile overload appears plausible. How- the joint. The architecture of these tendon insertion
ever, although this view is widely accepted, the sites is complex, with a cartilaginous transition zone
clinical and scientific bases for this concept do not most pronounced on the joint side of the tendon.[96]
stand close scientific scrutiny. Without a prospec- Recent work on the increase of proteoglycans within
tive design and adequate control groups, any conclu- the posterior tibialis tendon indicates that cartilagi-
sion regarding the aetiological role of factors such as nous metaplasia can occur as an adaptive response
training errors, poor technique, inadequate equip- to mechanical compression on the tendon.[97] These
ment, inflexibility and muscle imbalance remains histological findings question whether the tendon
speculative. Only a few studies have attempted to insertion site is uniformly subjected to tensile loads.
study these factors in a controlled, prospective man- This has led to various biomechanical studies on the
ner and have shown conflicting results.[77-83] strains near the tendon insertion sites.
Epidemiological studies have also made some
Strains in the supraspinatus insertion onto the
interesting observations. For example, overuse inju-
greater tuberosity were measured at various gle-
ries, including tendon problems, are significantly
nohumeral positions using a magnetic resonance
more common in elderly athletes compared with
image-based technique.[98] In general, the strain of
young athletes.[84,85]
the supraspinatus tendon on the joint side of the
2.3 Biomechanical Challenges to the
insertion was significantly lower than the values
Traditional Concept
found on the bursal side.
In a biomechanical study of the patellar tendon
Biomechanical studies on failure modes of mus- origin near the inferior pole, the tendon was instru-
cle-tendon units have clearly shown that failure will mented with strain gauges and taken through a range
occur within the muscle near the muscle-tendon of motion while the tendon itself was loaded.[99] The
junction,[86,87] not in the tendon. Although these highest tensile strains measured just distal to the
load-to-failure experiments do not study repetitive inferior pole of the patella were found on the anteri-
submaximal loads, they do point out how a healthy or aspect of the tendon. The lowest strains were
tendon is biomechanically ‘over-engineered’ com- found on the posterior, joint-side aspect of the ten-
pared with its attached muscle. In insertional tendi- don, the site where the changes of classical patellar
nopathy, the pathological tendon lesion lies at or tendinopathy, or jumper’s knee, are found. Basso et
very close to the insertion site of the tendon, the al.[100] measured strain over the length of the tendon,
enthesis. Insertional tendinopathy is commonly seen rather than locally.[99] In this manner, the strains

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
1014 Maganaris et al.

were actually greater posteriorly in the tendon and The cartilage-like changes in the enthesis in
failure occurred at higher strains posteriorly. How- many ways can be considered a physiological adap-
ever, this may not reflect what is actually occurring tation to the compressive loads. However, even car-
close to the insertion site where the pathology is tilaginous metaplasia may not allow the tendon to
almost exclusively found. Basso et al.,[101] studying maintain its ability to withstand the high tensile
the compressive load in the patellar tendon as it loads in that region. It seems possible that in athletes
courses over the inferior pole of the patella, found occasionally certain joint positions will still place
significant compressive loads at this location. They high tensile loads on the enthesis. As the stress
felt that the bone of the inferior pole of the patella shielding may have led to tensile weakening over
exerted this compressive load through an impinge- time, an ‘injury’ may occur more easily in this
ment on the tendon. region. In this manner, insertional tendinopathy
In a study on the Achilles tendon insertion could be considered as being an overuse injury, but
site,[102] the tendon was instrumented with strain predisposed by pre-existing weakening of the ten-
gauges just proximal to the calcaneus. Again, the don.
lowest strains were found on the calcaneal side, Finally, as the joint changes position, strains in
where the pathological changes of Achilles inser- one section of the tendon could be changing in
tional tendinopathy are generally found. opposite directions. Internal shear forces and heat
Although not all biomechanical studies report could be generated, producing injury to the cellular
exactly the same results, a consistent pattern appears and/or matrix components of the tendon. Accumula-
to emerge: the strains within the tendons near their tion of these injuries could lead to the intratendinous
insertion site are not uniform. If we assume that the degeneration seen in tendinopathy.
material properties are similar throughout the ten-
don, this would mean that any muscle force trans- 3. Conclusions
ferred through the insertion site preferentially loads The aetiology of tendinopathy is likely to be
the side of the tendon that is usually not affected multifactorial, including some of the traditional fac-
initially in tendinopathy. In that case, the side affect- tors such as overuse, inflexibility and equipment
ed by tendinopathy is generally ‘stress shielded’. problems. However, other factors also need to be
Thus, the presence of differential strains opens the considered, such as age-related tendon degeneration
possibility of alternative biomechanical explana- and biomechanical considerations as outlined in this
tions for the pathology found in these regions of the review. Recent in vivo and in vitro studies have shed
tendon. The traditional concept of tensile failure some light on the biomechanics of the main body of
may not be the essential feature of the pathomechan- tendon, but more research is needed to determine the
ics. significance of tensional loads, stress shielding and
compression in tendinopathy. The current bi-
2.4 Alternative Biomechanical Theories in
omechanical studies indicate that certain joint posi-
Insertional Tendinopathy
tions are more likely to stress the area of the tendon
The recent biomechanical data reported above commonly affected by tendinopathy. These joint
suggest a different biomechanical aetiology of inser- positions seem to be different from the traditional
tional tendinopathy. The stress-shielded side of the positions advocated in stretching exercises used for
enthesis shows a distinct tendency to develop carti- prevention and rehabilitation of tendinopathies. In-
lage-like and/or atrophic changes in response to the corporating different joint position exercises may
lack of tensile load.[95-97] Over long periods, this exert more controlled stresses on these affected ar-
process may induce a primary degenerative lesion in eas of the tendon, possibly allowing better mainte-
that area of the tendon. This may explain why the nance of the mechanical strength of that region of
tendinopathy is not always clearly activity-related, the tendon and, therefore, prevent injury. Alterna-
but sometimes more strongly correlated with age. In tively, this practice could stress a healing area of the
this manner, tendinopathy would be a result of stress tendon in a controlled manner and thus stimulate
shielding rather than overuse injury. healing once an injury has occurred. Additional

 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (14)
Tendon Pathomechanics 1015

work will have to prove whether such principles 21. Woo SL-Y, Gomez MA, Woo Y-K, et al. Mechanical properties
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should be incorporated in current rehabilitation tion and exercise on tissue remodelling. Biorheology 1982; 19:
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22. Savolainen J, Myllyla V, Myllyla R, et al. Effects of denervation
and immobilization on collagen synthesis in rat skeletal muscle
Acknowledgements and tendon. Am J Physiol 1984; 254: R897-902
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No sources of funding were received to assist in the tendon to prolonged hindlimb suspension in rats. J Appl Physi-
ol 1988; 65: 373-6
preparation of this manuscript. The authors have no conflicts
24. Loitz BJ, Zernicke RF, Vailas AC, et al. Effects of short-term
of interest that are directly relevant to the content of this immobilization versus continuous passive motion on the bi-
manuscript. omechanical and biochemical properties of rat tendon. Clin
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