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European Journal of Orthodontics 15 (1993) 89-96 ) 1993 European Orthodontic Society

Orthodontic tooth movement into edentulous areas with


reduced bone height. An experimental study in the dog
Birgitta Lindskog-StoklancT, Jan L Wennstrom**, Sture Nyman**, and Birgit
"Philander*
Departments of "Orthodontics and **Periodontology, Faculty of Odontology, University of Goteborg,
Sweden

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SUMMARY The present study was performed in order to test the hypothesis that the height of
supporting bone and connective tissue attachment will be maintained around teeth bodily moved
into areas of reduced bone height. During a pre-experimental period, areas with markedly reduced
bone height were produced in the mandible of 4 beagle dogs through extraction of the 4th
premolars and subsequent surgical reduction of the bone height in the extracted sites to a level
corresponding to half the root length of the 3rd premolar. Following healing, one of the third
premolars was bodily moved in a distal direction into the area of reduced bone height, while the
contralateral premolar served as a non-moved control. After 6 months of active tooth movement,
the teeth were retained in their new position for a further 2 months before biopsies of test and
control tooth sites were sampled. Radiographic evaluation showed that a bodily movement had
been achieved with no or only minimal vertical displacement of the teeth. The histological analysis
revealed that none of the teeth, orthodontically moved or not, had experienced loss of connective
tissue attachment. Although a greater distance between the cemento-enamel junction and the
bone crest was found on the pressure side of the orthodontically moved test teeth in comparison
to the contralateral, non-moved control teeth, the bone level at all test teeth was more coronally
positioned than the original, reduced bone level in the area into which the test teeth had been
moved. Hence, these findings indicate that a tooth with a normal height of periodontal support
can be orthodontically moved into an area of markedly reduced bone height with maintained
height of the supporting apparatus.

Introduction extrusion of teeth (Pontoriero et al., 1987;


Kozlowsky et al., 1988; Schwimer et al., 1990;
Orthodontic forces, induced for bodily tooth Berglundh et al., 1991). When the coronal
movement, will result in different reactions in portion of the fibre attachment was excised,
the periodontal tissues on the pressure and on the crestal part of the alveolar bone did not
the tension side. Bone resorption occurs on the follow the root during extrusion and, con-
pressure side as a consequence of trauma- sequently, the tooth movement resulted in an
induced reactions within the periodontal liga- increased distance between the cemento-enamel
ment tissue, while on the tension side a junction and the alveolar bone crest. In contrast,
continuous bone apposition will be seen teeth subjected to extrusion without concomit-
resulting in a maintained width of the period- ant fiberotomy, demonstrated a maintained
ontal ligament (for review see Rygh, 1985). relationship between the cemento-enamel junc-
However, the bone apposition on the tension tion and the bone crest, i.e. the bone followed
side will occur only if the alveolar bone is the tooth during the extrusion movement.
connected with the root by periodontal ligament The tissue changes occurring on the pressure
fibres (Poison et al., 1984). This fact is also side during orthodontic tooth movement are
supported by observations made in clinical and confined to the infrabony area of the root, i.e.
experimental studies on the effect of fiberotomy the area of supporting bone where the period-
on the periodontal tissues during orthodontic ontal ligament will be compressed between two
90 B. LINDSKOG-STOKLAND ET AL.

hard tissues. Hence, orthodontic tooth move- PRE-EXPERIMENTAL PERIOD


ment will not induce reactions in the supracres- EXTRACTION OF MANDIBULAR 4TH PREMOLARS
tal area resulting in loss of connective tissue
attachment (Karring et al., 1982; Thilander 2 months
et al., 1983; Wennstrom et al., 1987). The
applied forces will lead to demineralization of PREPARATION OF REDUCED BONE HEIGHT
the supporting bone, which in turn allows the (IN THE AREA OF THE 4TH PREMOLAR)
tooth to move in the direction of the forces. In
this respect it is noteworthy that the demineral- 2 months
ization of supporting bone induced, e.g. by
jiggling forces applied to a tooth positioned BASELINE EXAMINATION
within the boundaries of the alveolar process,
is reversible (Kantor et al., 1976). On the other ORTHODONTIC TOOTH MOVEMENT

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hand, no bone remineralization is seen adjacent
to a tooth that has been moved out. through
the bone plate and become positioned with part
6 months
of its root outside the alveolar process, i.e.
when an alveolar bone dehiscence has been
created (Steiner et al., 1981; Karring et al.,
1982; Thilander et al, 1983; Wennstrom et al.,
1987). However, when such a tooth is moved RE-EXAMINATION
back into the alveolar bone housing, bone
apposition will take place in the area of the RETENTION
previous dehiscence (Nyman et al., 1982;
Karring et al., 1982; Engelking and Zachrisson, 2 months
1982; Thilander et al., 1983). The results of
these studies indicate that the soft tissue, facial FINAL EXAMINATION AND BIOPSY
to a produced bone dehiscence, contains a bone
Figure 1 Experimental outline. Plaque control measures
matrix with the capacity to remineralize follow- were carried out during the entire course of the study.
ing repositioning of the tooth into the alveolar
process. It may thus be speculated that genetic
factors controlling the dimensions of the alve- Experimental animals
olar process may be the reason for the lack of
remineralization of the bone matrix buccal to Four female beagle dogs, around 2 years old,
a tooth moved into a prominent position in were utilized for the study. Clinical and radio-
the jaw bone. graphic examinations, performed at the initi-
ation of the study, revealed signs of gingival
Hence, based on the findings in the studies inflammation, but no periodontal tissue break-
referred to, it could be anticipated that, as long down in the premolar-molar tooth regions.
as orthodontic tooth movement is performed From the day of initial examination and
within the genetically determined boundaries of throughout the course of the study, mechanical
the jaw, a tooth, moved into a neighbouring plaque control measures were performed once
edentulous area with markedly reduced bone every 2-3 days. Intravenously injected Pentho-
height, will maintain the original height of the tal Sodium was used for sedation of the dogs
supporting apparatus, i.e. its connective tissue during experimental procedures. At the termina-
attachment level and its alveolar bone height. tion of the study, the animals were killed with
The present experiment in the beagle dog was an overdose of the sedation solution.
designed to test this hypothesis by ortho-
. dontically moving teeth into edentulous areas Pre-experimental period
with reduced bone height. A 4-month preparatory period preceded the
start of the orthodontic tooth movement. The
fourth premolar in both sides of the mandible
Materials and methods was extracted. After a healing period of 2
The design of the study is outlined in Fig. 1. months, a surgical procedure was performed in
TOOTH MOVEMENT INTO AREAS WITH REDUCED BONE HEIGHT

order to create a markedly reduced bone height root length of the 3rd premolar, i.e. the
in the areas of the extracted premolars (Fig. 2). reduction of the bone height amounted to
A vertical releasing incision was made 2 mm approximately 4-5 mm. In addition, 3-4 small
distal to the third premolar to demarcate the titanium markers to be used as reference points
mesial extension of the surgical field and to for radiographic assessments were placed in the
avoid interference with the periodontal support buccal cortical bone. The flaps were reposi-
of the tooth. Subsequently, a supracrestal tioned and sutured to complete coverage of the
incision, extending from the releasing incision alveolar bone. The sutures were removed after
to the mesial surface of the first molar, was one week of a 2-month healing period.
made to allow the elevation of buccal and
lingual mucoperiosteal flaps. The exposed bone Orthodontic tooth movement
crest in the edentulous areas of the 4th pre- Following healing, one of the third mandibular
molars was then reduced in height using a large premolars in each dog was bodily moved into

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round bur to a level corresponding to half the the area of reduced bone height (Fig. 2). The
contralateral premolar served as control and
was not subjected to orthodontic tooth move-
ment. The canine and the first molar on the
test side were fixed in an individually fabricated
silver splint to be used as anchorage (Fig. 3).
A sectional rectangular archwire (0.018 x 0.025)
was attached with standard tubes (0.018 x 0.025)
to the 3rd premolar and the 1st molar as well
as to the silver splint distal to the canine. A
closed coiled spring was applied for bodily
movement of the premolar. The force applied
was 0.3-0.5 N and the coiled spring was
reactivated every 3 weeks, at which time the
force had approached zero. The force used was
estimated to result in a tooth displacement of
approximately 1 mm/month, and the ortho-
dontic movement continued until the distal root
of the 3rd premolar had entered into the area
Figure 2 Schematic drawing illustrating the tooth displace- of reduced bone height, i.e. for a period of
ment achieved by bodily movement. about 6 months. The appliance was then used

Figure 3 Clinical photograph showing the design of the orthodontic appliance used for bodily movement of the third
premolar. Arrow indicates the direction of tooth movement.
92 B. LINDSKOG-STOKLAND ET AL.

to retain the tooth in its new position for a (Fig. 4) were measured (magn. x 40) and
further 2 months. expressed in millimetres:
Clinical assessments (1) the cemento-enamel junction (CEJ) to the
At the start of orthodontic tooth movement, coronal level of the connective tissue attach-
at the time of retention and at the termination ment (AL), i.e. the connective tissue attach-
of the experiment, the presence or absence of ment level;
visible plaque deposits and gingival inflamma- (2) CEJ to the alveolar bone crest adjacent to
tion (bleeding on pocket probing) was deter- the root (BC), i.e. the height of supporting
mined at all test and control teeth. At each bone;
examination, the position of the 3rd premolar (3) the gingival margin (GM) to the apical
in relation to the 1st molar was assessed by level of the junctional epithelium (aJE), i.e.
measuring the distance to the nearest 0.1 mm

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the pocket depth.
between the proximal prominence of the two
teeth with the use of a calliper.
Radiographic assessments Results
At the same time intervals as for clinical Clinical assessments
assessments, periodic reproducible radiographs The initial signs of gingival inflammation
were obtained using a modification of the decreased during the course of the study at
Eggen technique (Eggen, 1969). The radio- both test and control sites as a result of the
graphs were transformed to paper copies (magn.
x 4) on which tracings were made of the test/
control tooth (3rd premolar), the anchorage
tooth (1st molar) and the alveolar bone crest. GM-r
The titanium markers were used as reference
points when superimposing the tracings from
the various examinations to assess tooth dis-
placement. The long axis through the distal
root of the 3rd premolar and a line perpendic-
ular to the long axis at the apex of the root
together with a line, drawn through the titanium
implants, were used to determine the accuracy
of the bodily tooth movement. CEJ--
Histological preparation and assessments
Following the death of the dogs, the mandibular BC--
jaw was removed and placed in a 10% neutral
formalin fixative and decalcified in EDTA for
subsequent histological preparation. Tissue
blocks containing test or control specimens
were dissected and further processed for embed-
ding in paraffin. Sections 8 fim thick of the
teeth with surrounding periodontal tissues were
cut in the mesio-distal plane parallel to the
long axis of the distal root. The sections were
stained in haematoxylin and eosin or van
Gieson's connective tissue stain. From each test
and control tooth, three sections, 100 fim apart Figure 4 Schematic drawing illustrating the reference
and representing the central portion of the points used to measure the various linear distances
distal root of the 3rd premolar, were used for in the histological specimens; GM = gingival margin;
aJE = apical termination of the dentogingival epithelium;
detailed examination by light microscope. In AL = coronal level of the connective tissue attachment;
each section, the following linear distances BC = alveolar bone crest.
TOOTH MOVEMENT INTO AREAS WITH REDUCED BONE HEIGHT 93
plaque control programme exercised. None of all dogs with no or only minimal vertical
the sites exhibited bleeding on probing at the displacement (Fig. 5). The horizontal distance
time of retention and at the termination of of root displacement showed a mean movement
the experiment. The clinical assessment of the of 5.0 mm (range 4.5-5.5 mm), i.e. in all dogs
position of the 3rd premolars in relation to the the distal root surface of the 3rd premolar was
1st molars showed that the orthodontically located at least 2 mm within the area of reduced
moved premolars had been displaced distally bone height.
on average 5.5 mm (range 4.5-6.5 mm), while
no displacement of the control teeth had Histological observations and assessments
occurred. The histological analysis of the biopsy material
revealed that the orthodontically moved test
Radiographic assessments teeth as well as the non-moved control teeth
The radiographic evaluation of the displacement showed only minimal infiltration of inflammat-

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of the orthodontically moved test teeth revealed ory cells in the connective tissue adjacent to
that a bodily movement had been achieved in the dentogingival epithelium.

t ici

A
Figure 5 Radiographs obtained at the start of the orthodontic tooth movement (A) and at the termination of the experiment
(B) of a test tooth and the contralateral control tooth. Note the difference in radiographic bone height between the test and
the control tooth at the termination of the experiment (arrows).
94 B. LINDSKOG-STOKLAND ET AL.

Table 1 Results from histometric analysis of orthodontically moved test teeth and non-moved control teeth
in the four animals (mm).

CEJ-AL CEJ-BC GM-aJE

Test Control Diff. Test Control Diff. Test Control Diff.

Dog 1 0 0 0 3.36 2.40 0.96 2.52 2.44 0.08


Dog 2 0 0 0 2.24 1.40 . 0.84 2.48 2.32 0.16
Dog 3 0 0 0 3.76 1.32 2.44 2.08 2.28 -0.20
Dog 4 0 0 0 2.24 2.08 0.16 1.88 2.36 -0.48

Mean 0 0 0 2.90 1.80 1.10 2.24 2.35 -0.11


SD 0.77 0.53 0.48 0.32 0.07 0.29

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CEJ-AL = the connective tissue attachment level; CEJ-BC = the height of supporting bone; GM-aJE = the histological
pocket depth.

Table 1 describes the results of the histometric bone height with maintained height of the
assessments, performed at the distal aspect of supporting apparatus, i.e. maintained connect-
test and control teeth. None of the teeth, ive tissue attachment level and in all essentials
orthodontically moved or not, showed loss of also maintained alveolar bone support. It was
connective tissue attachment. Hence, at all also observed that the newly established period-
teeth, the most apical cells of the junctional ontal ligament exhibited a normal width both
epithelium were located at the cemento-enamel on the pressure and on the tension side of the
junction (CEJ). displaced teeth.
The distance between the CEJ and the With regard to the bone support, certain
alveolar bone crest adjacent to the pressure differences were noted between the tension and
side of the distal root was in all dogs numerically pressure side of the orthodontically moved
larger at the test teeth than at the control teeth teeth. On the tension side, i.e. at the mesial
(mean difference 1.10 mm, range 0.16-2.44). aspect of the root, both the original height and
However, at all test teeth, but to a varying width of the supporting bone were fully main-
degree, the bone level adjacent to the root tained, which is in accordance with results
surface was more coronally positioned than the presented by Zander and Miihlemann (1956),
bone level created during the pre-experimental Reitan (1964, 1967, 1969), and Poison et al.
period in the edentulous area, and into which (1984).
the test teeth had been orthodontically moved On the pressure side, on the other hand,
(Fig. 6). The histological picture of the bone supporting alveolar bone was also present
tissue in the coronal portion of the root showed extending far coronal to the surrounding,
a high number of cells in contrast to the experimentally created bone level, but not
compact appearance of the more apically loc- reaching the complete height and not the same
ated bone. width as the original supporting bone. The
At the tension side of the roots, the full explanation for this finding can only be specu-
height of the bone support had been maintained lated on. It seems reasonable to assume,
adjacent to all orthodontically displaced teeth. however, that the biological course of tissue
With respect to the assessment of the pocket events is similar to that occurring around teeth
depth at the distal aspect of the 3rd premolars, subjected to jiggling forces. Experimental stud-
no differences were found between test and ies in monkeys and dogs (Kantor et al., 1976;
control teeth. Nyman et al., 1982) have shown that the bone
loss, induced by such forces, is reversible. As
previously discussed by Karring et al. (1982)
Discussion and Nyman et al. (1982), a likely explanation
The results of the present study indicate that a for this reversion is that only the inorganic
tooth with normal periodontal support can be component of the alveolar bone is lost as a
orthodontically moved into an area of reduced consequence of the biological response to
TOOTH MOVEMENT INTO AREAS WITH REDUCED BONE HEIGHT

Test
..** Control

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Figure 6 Specimens from the test and the control tooth shown in Fig. 5. The thin bone along the pressure side of the test
tooth was not visualized in the radiograph.

traumatic forces and that the organic compon- It is quite obvious, when analysing the
ent is maintained, liable to remineralization of histological sections (Fig. 6), that the supporting
the bone when the forces are discontinued. bone on the pressure side of the test teeth was
Hence, it could very well be that the organic much thinner than the original bone. One
component of the supporting bone on the reason for this could be that the bone remin-
pressure side of the experimental teeth in the eralization is confined to that part of the bone
present study has been brought with the tooth tissue which is anchored to the root by means
during the orthodontic movement into the area of ligament fibres ('the bundle bone'). However,
of reduced bone height. When the orthodontic it cannot be ruled out that additional remin-
forces were eliminated, i.e. when the teeth were eralization, and regaining of bone height and
stabilized in their new position, remineralization bone width might have been obtained if the
of the alveolar bone took place. In this context retention period of the teeth in their new
it is interesting to note that following similar positions had been prolonged.
tooth movement in a facial direction, resulting It could, of course, be argued that the
in a tooth position with part of the root located supporting bone, found on the pressure side of
outside the boundaries of the jaw, i.e. when an the test teeth, represents coronal growth of
alveolar bone dehiscence has been created, no bone from the surrounding reduced level of
bone remineralization will be found (Steiner bone. This seems, however, in the opinion of
et al., 1981; Karring et al, 1982; Thilander the present authors unlikely, since the soft
et al, 1983; Wennstrom el al, 1987). tissue adjacent to the root is an 'intact' tissue
96 B. LINDSKOG-STOKLAND ET AL.

which can hardly be invaded by foreign types Engelking G, Zachrisson B U 1982 Effects of incisor reposi-
of tissue cells. tioning on monkey periodontium after expansion through
the cortical plate. American Journal of Orthodontics 82:
It should be understood that additional 23-32
studies are required to substantiate the present Kantor M, Poison A M, Zander H A 1976 Alveolar bone
findings and speculations. In addition, studies regeneration after removal of inflammatory and traumatic
should be performed in order to evaluate factors. Journal of Periodontology 47: 687-695
whether the bone component of the supporting Karring T, Nyman S, Thilander B, Magnusson I 1982 Bone
tissues is also maintained at the buccal/lingual regeneration in orthodontically produced alveolar bone
aspects of teeth when moved into edentulous dehiscences. Journal of Periodontal Research 17: 309-315
jaw areas with reduced buccolingual bone Kozlowsky A, Tal H, Liebermann M 1988 Forced eruption
dimension. If this holds true, the treatment combined with gingival fiberotomy. Journal of Clinical
modality used in the present study may have Periodontology 15: 534-538
obvious clinical implications. A tooth with Nyman S, Karring T, Bergenholtz G 1982 Bone regenera-

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normal periodontal tissue support, located adja- tion in alveolar bone dehiscences produced by jiggling
forces. Journal of Clinical Periodontology 7: 316-322
cent to an edentulous area with reduced bone
volume, could be orthodontically moved with Poison A, Caton J, Poison A P, Nyman S, Novak J, Reed B
1984 Periodontal response after tooth movement into
maintained support into such an area and used infrabony defects. Journal of Periodontology 55: 197-202
as abutment for a fixed partial denture. This
Pontoriero R, Celenza F, Ricci G, Carnevale G 1987 Rapid
could replace, e.g. the insertion of dental extrusion with fiber resection; a combined orthodontic-
implants which also per se is often problematic periodontic treatment modality. International Journal of
in posterior jaw areas with reduced bone Periodontics and Restorative Dentistry 7: 31-43
volume. Reitan K 1964 Effects of force magnitude and direction of
tooth movement on different alveolar bone types. Angle
Address for correspondence Orthodontist 34: 244-255
Reitan K 1967 Clinical and histologic observations on tooth
Dr Jan L. Wennstrom movement during and after orthodontic treatment. Amer-
Department of Periodontology ican Journal of Orthodontics 53: 721-745
Faculty of Odontology Reitan K 1969 Biomechanical principles and reactions. In:
University of Goteborg Graber T M (ed.) Current orthodontic concepts and
Medicinaregatan 12 techniques, Vol. 1. WB Saunders, Philadelphia,
pp. 56-159
S-413 90 Gothenburg
Sweden Rygh P 1985 Orthodontic forces and tissue reactions. In:
Thilander B, Ronning O (eds) Introduction to orthodont-
ics. Tandlakarforlaget, Stockholm, pp. 206-224
Acknowledgements Schwimer C W, Rosenberg E S, Schwimer D H 1990 Rapid
extrusion with fiberotomy. Journal of Esthetic Dentistry
Financial support for this study was obtained 2: 82-88
from the Colgate-Palmolive Company, Piscata- Steiner G G, Pearson J K, Ainamo J 1981 Changes of the
way, NJ, USA, the Swedish Dental Society and marginal periodontium as a result of labial tooth move-
the Swedish Medical Research Council (grant ment in monkeys. Journal of Periodontology 52: 314-320
no. B92-24X-05006-15A). Thilander B, Nyman S, Karring T, Magnusson I 1983 Bone
regeneration in alveolar bone dehiscences related to
orthodontic tooth movements. European Journal of
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