Primate experiments in malocclusion and

bone induction Dr. Woodside

D. G. Woodside, G. Altuna, E. Hanrold, M. Herbert, and A. Mstaxas

Toronto, Ontario, Canada

It has been recognized for many years that muscle function influences bone formation and morphology. It is
hypothesized here that the movement of bone into new positions within a muscle system results in
rearrangement of the stress distribution and reorganization of shape and internal structure. To test the above
hypothesis, clinical and animal experiments involving the use of posterior occlusal bite blocks, Herb9 appliances,
and temporal and masseter muscle stimulation were undertaken. Chronic or continuous alteration in mandibular
position within the neuromuscular environment with the posterior occlusal bite block and the Herb& appliance in a
sample of monkeys produced extensive condylar remodeling and change in mandibular size. Short periods of
induced hyperactivity in the masseter and temporal muscles were associated with the production of malocclusion
symptoms. Excess induced temporal muscle activity of specific frequency and intensity may interfere with the
remodeling of bone grafts placed under the temporal muscle, while a lesser level of activity was associated with
bone remodeling.

Key words: Bone, muscle, function, growth, functional appliances

0 rthodontic treatment uses two basic ap-

proaches. In one the physical forces generated by me-
chanical devices, such as fixed orthodontic appliances,
are distributed to the teeth, while in the other neu-
romuscular activity generated by removable functional
orthodontic appliances is tapped to alter stress on teeth
and jawbones. The functional appliance accomplishes
this objective by the recruitment of additional or mod-
ified neuromuscular activity as well as by change in
soft-tissue tension. The efficiency of these appliances
depends on how readily they can facilitate a desired
change in bone-muscle interaction and thus produce a
specific change in morphology.
It has been recognized for many years that muscle
function influences bone formation and morphology.
The most often quoted explanations of this relationship
are Wolffs law (1899) and those modifications of it
proposed by Thomas (1907), Baker3 (1922), Wash-
bum4 (1947), Bassett5 (1972), and Harvold (1975).
Wolffs law states that the shape and structure of a
bone depends on the stress placed on the bone by the
musculature. Thus, not only does a bones external
shape vary in response to constant muscle tonus, but its
internal structure, as seen in the stress lines, will adapt
to this tonus as well.
Many experimental studies have shed light on the
Presented at the annual meeting of the European Orthodontic Society, Bonn,
Germany, June 4, 1982, and at the hvelfth biennial meeting of the Association
of Canadian Faculties of Dentis@y, Halifax, Nova Scotia, June 19, 1982.
close interaction between muscle function and the in-
ternal and external structure of bone.7-g Investigations
of the effects of removal of the muscles of mastica-
tion,lO-lg removal of parts of facial bones,O* 2oreduced
muscle activity, as in paralysis,** 14* 21, 22 immobil-
ization,, a and reduced physical consistency of diet24
have demonstrated that reduced muscle function re-
sults in changes in associated bone morphology, either
absence of associated bone or rudimentary bone forma-
tion. Conversely, experiments involving the creation of
hyperfimction and hypertrophy of muscle93 25 and
muscle-repositioning studies showing associated bone
enlargement and bone formation26, 27 have further clar-
ified this muscle-bone interplay. Most important,
works by Humphrey28 and Spyropoulos2g have sug-
gested that the presence of muscle tissue and activity
may itself be responsible for specific areas of bone
formation.
Unilateral muscle imbalance has also been shown to
be linked to facial asymmetry, regressive change in
the mandibular condyle associated with decreased uni-
lateral function of the lateral pterygoid muscle and con-
dylar enlargement on the contralateral side. One of us
has also demonstrated that artificially induced muscle
imbalance has both created (Fig. 1) and corrected spi-
nal curvature (Fig. 2) in association with histochemical
changes in muscle fiber type.30 In addition, varying
histochemical profiles have also been reported to exist
in the muscles of mastication of patients with vertical
maxillary dysplasias,31j 32 a finding that further sup-

460

Fig. 1. Production of scoliosis curvature by percutaneous
lation of perispinal muscle in rabbit. Radiograph
shows curve produced after 6 weeks of stimulation.
used to prevent animal from breaking the leads.
ports the idea that muscle imbalances are related to
abnormalities of skeletal structures.
All this experimentation reinforces the view that a
distinctive feature of the orofacial unit is the interaction
between neuromuscular activity and bone formation
and morphology. The bone-muscle system in this area
is extremely complex; there are twenty-four muscles
attached to the mandible, and all participate in the rela-
tively independent functions of mastication, speech,
and posture. In addition, all may be related to stress
distribution in the bone and thus to bone morphology
and internal structure. To approach such a complex
system experimentally, it may be arranged into two
separate sets of factors. The neuromuscular system is
assumed to act on the metabolic system, causing bone
formation and remodeling in specific circumstances;
thus, factors involved in bone-stressing neuromuscular
activity are placed in one group, while all those in-
volved in tissue metabolism are placed in the other. If
we are dealing with a normal metabolic system, this
may be considered as constant. The assumption makes
it possible to study varying modes and levels of neu-
romuscular activity in the control of bone formation
and developmenP4 (Fig. 3).
Primate experiments in malocclusion and bone induction 461
Fig. 2. Use of electrical stimulation of paraspinal muscles to
treat scoliosis in female patient 8 years 9 months of age. The
implanted stimulator is visible on the right side of the spine.
stimu- Four years later the curve has been reduced from an initial 38
(top right) degrees to 26 degrees, when it would have increased to a much
Chariot is higher level without therapy.
CONDYLAR GROWTH INDUCTION
Bassettj has modified Wolffs law to state that
bone elements place or displace themselves in the
direction of functional pressure and increase or de-
crease their mass to deflect the amount of functional
force. If we accept Wolffs law and its modifications,
we may also make the following statement: Moving a
bone to a new position within a muscle system results in
rearrangement of the stress distribution and reorgani-
zation of shape and internal structure. This statement
has been tested by two of US,~33 using a sample of
sixteen juvenile and adult cynomolgus monkeys.33 Dur-
ing the control period for each animal, minimal re-
modeling of the mandible occurred when cephalometric
tracings were superimposed on metallic implants. Fol-
lowing the placement of posterior occlusal blocks vary-
ing between 4.0 and 12.0 mm. in thickness, which
created a continuous inferior and posterior mandibular
rotation within the neuromuscular system, extensive
remodeling of the gonial and condylar areas was seen in
both juvenile and adult animals, with these results re-
maining stable 1 year later. It should be pointed out that
in this experiment the effective length of the mandible
was increased up to 5.0 mm. in both young and adult
animals as the condyle remodeled in a superior and
462 Woodside et al. Am. J. Orthod.
June 1983

HERBST APPLIANCE
#978 $hvmile

Fig. 3. All factors involved in neuromuscular activity to create

stress on bone are placed in one group, while all factors in-
volved in tissue metabolism are placed in a separate group. The
assumption is that the neuromuscular system acts on the meta- CONTROL PERIOD: 45 weeks
bolic system
specific
bolic system,
to cause bone stress
circumstances.
and bone formation
If we are dealing with a normal
this may be considered as constant.
under
meta-
The assump-
0A . . . . . . . . . Control
-_---- Control
I: 24 weeks
2: 2 I weeks
HERBST APPLIANCE
tion makes it possible to study varying levels of neuromuscular
activity in the control of bone formation and development. #978 juvenile

EXPERIMENTAL PERIOD 13 weeks

330
---_------
9 ADULT (AGE 48-6OM)
DENTAL STATUS: PERMANENT DENTITION
BITE BLOCK OPENING:
-
12.0 tm.
START OF CONTROL
0B 13 weeks

..... END OF CONTROL 14 WEEKS Fig. 5. During a 45week control period the mandibular tracing
----- END OF EXPERIMENT 18 WEEKS
superimposed on metallic implants showed that the condylar
process remodeled in a posterior direction. However, after
Fig. 4. A posterior occiusal bite block, 12.00 mm. thick, was
placement of a Herbst appliance for a 18week period, a small
placed in an adult monkey. There was remodeling of the con-
amount of remodeling in the condylar area resulted in a superior
dyle in a superior and posterior direction at the end of the 18-
condylar direction.
week experimental period, as compared to 14-week control
period.

tern (Fig. 5). During a 45week control period in a

posterior direction (Fig. 4), although the condyle trans-
lated anteriorly with placement of the occlusal bite
block. The experiment demonstrated that mandibular
advancement is not a necessary prerequisite for exten-
sive condylar remodeling.
Additional experiments by us, using the Herbst
appliance, also produced a method for continuous al-
teration of bone position within the neuromuscular sys-
juvenile cynomolgus monkey, the mandibular tracing
superimposed on metallic implants showed that the
condylar process remodeled in a superior and posterior
direction, with moderate posterior remodeling of the
ramus. However, after the placement of a Herbst
appliance for a 13-week experimental period in which a
Class III malocclusion was created, a small amount of
remodeling in the condylar area occurred in a superior
Volume 83 Primate experiments in malocclusion and bone induction 463
Number 6

Fig. 6. The condyle of a juvenile cynomolgus monkey after

wearing of a 12 mm. bite block for an 18-week experimental
period. Note that the proliferation of the condylar cartilage is no
Fig. 6. Vital staining with alizarin red S showed extensive bone longer evident. (Hematoxylin and eosin stain. Magnification,
formation at the anterior border of the ramus after the place- x3.0.)
ment of a Herbst appliance in a juvenile monkey (No. 978) for a
13-week experimental period. C, Cuspid. A4, Molar.

-Pre-treatment
Fig. 7. Condyle and glenoid fossa of a juvenile animal (No. 978)
- ----After 6 months Herbst appliance the1raw
after 13week Herbst appliance treatment. Extensive bone for-
mation on the postglenoid tubercle (6) and the posterior and
.--...--.After 7.5 months observation
anterior surfaces of the condyle. Prechondroblastic and chon- Fig. 9. Patient R. R. Superimposition of tracings of mandible to
droblastic layers are showing a width increase. M, Lateral show changes due to treatment and growth. The condylar
pterygoid muscle attachment. (Hematoxylin and eosin stain. growth direction is posterior and superior after 6 months treat-
Magnification, x3.0.) ment with the Herbst appliance.

direction only. Vital staining with alizarin red S
showed extensive bone remodeling at the anterior areas
of the ramus (Fig. 6). Ground sections with tetracycline
vital staining and decalcified sections stained with he-
matoxylin and eosin showed bone formation on the sur-
face and interior of both the condyle and the glenoid
fossa. The glenoid fossa also showed extensive bone
formation in the posterior region after 13 weeks (Fig.
7), with continuous forward posturing of the mandible.
Decalcified sections from another experiment, in which
posterior occlusal bite blocks were used to rotate the
mandible down and back, show hyperplasia of the pre-
chondroblastic and chondroblastic cartilage layers after
4 weeks of the experiment, as compared with the nor-
mal width of the same areas in a control animal. After an
l&week experimental period, this difference did not
exist; the proliferative chondroblastic zone had been
remodeled into a trabecular bone and now showed pre-
chondroblastic and chondroblastic layers of normal
width (Fig. 8). The ground sections in the Herbst ap-
464 Woodside et al. Am. .I. Orthod.
June 1983

Fig. 10. Highly miniaturized self-powered muscle stimulators

developed in the Surgical Research Department at the Hospital
for Sick Children, Toronto (M. Herbert), and modified in the
Department of Development Laboratory, University of Califor-
nia, San Francisco (R. Vreeland). Fig. 12. Tracings superimposed on metallic implants to show
incisor protrusion, upward tipping of the palate, and minor re-
modeling changes following bilateral stimulation of the masse-
ter and temporal muscles once every 3 seconds for 4 weeks.

Fig. 11. Malocclusion produced following 4 weeks, bilateral

stimulation of the masseter and temporal muscles to contract
once every 3 seconds. Model B after 4 weeks stimulation.
Model C shows the condition 12 months poststimulation.

pliance experiment show that a similar process had

taken place, with the decalcified sections showing nor-
mal width of prechondroblastic and chondroblastic
layers after 13 weeks of the experiment (Fig. 7).
These experiments illustrate the principle that con-
sistent changes in bone shape and internal structure
are obtained when the alteration in neuromuscular ac-
tivity is continuous.
Functional orthodontic appliances also change man- Fig. 13. A, A bone graft taken from the iliac crest is placed
dibular position relative to the neuromuscular system, under the temporal muscle flap and fastened to the cranium
but only the Herbst appliance is able to achieve a truly with a 0.1 mm. steel ligature. 6, The muscle flap is held down
over the graft by silk ligature ligation to the midsagittal
chronic or continuous change in jaw position. Other
aponeurosis.
functional appliances permit the mandible to return to
its original position when they are removed for eating
and other purposes, and hence yield an intermittent ated with functional appliance therapy have not been
change in jaw position. Accordingly, although human shown.
investigations have documented small mean increases These experiments also illustrate a major problem
in mandibular length of up to 1.O mm.,34 clini- in orthodontics. The changes seen at the condyle in
cally useful amounts of condylar remodeling associ- human studies of Herbst appliance therapy, 36 show a
Volume 83 Primate experiments in malocclusion and bone induction 465
Number 6

Table 1. Malocclusion induction by stimulated muscle activity in juvenile and adult monkeys
Muscles stimulated Malocclusion

Duration of Temporal Masseter

Serial experiment
no. Sex Age (days) Pulse frequency Right Lefr Right Left Dental Skeletal

925 M Adult 160 Every 3 seconds X No No

926 M Adult 96 Every 3 seconds X No No
9.57 F Juvenile 56 Every 3 seconds X x No No
973 F Juvenile 34 Every 3 seconds X X X X Yes; space incisors, Yes; palate and
both arches; maxilla up
crossbite, labial and forward
inclined incisor
915 F Juvenile 30 Every 3 seconds X X X X Yes; space incisors, Yes; maxilla
both arches over- forward
bite; labial in-
clined incisor

superior and posterior direction of remodeling (Fig. 9),
while the primate experiments with bite block therapy
and Herbst appliance therapy show, on the one hand,
superior and posterior remodeling and, on the other,
superior remodeling only. Clearly, the direction of
condylar remodeling may be influenced by therapy, but
at present functional appliances are employed for this
purpose without our knowing either the type of muscle
activity or the positions in which the mandible should
be placed in order to obtain the desired change in shape
and structure.
INDUCTION OF MALOCCLUSION
Further experiments have clarified the effect of in-
creased muscle activity on jaw morphology and tooth
positioning. Our goal was to change contraction fre-
quency in selected muscles of mastication without
severing nerves and muscles or damaging tissue. Stud-
ies of this kind call for long-term in vivo muscle
stimulation .37 To achieve this, highly miniaturized,
self-powered muscle stimulators were devised for im-
plantation under the skin of a monkeys back (Fig. 10).
Eleven-centimeter lengths of bipolar cardiac pacemaker
leads, set in tunnels under each animals skin, were
connected to electrodes implanted in the muscles to be
stimulated. They delivered a 4.5-volt pulse lasting 1
millisecond every 3 seconds. The result was a visible
twitch in the muscle, with associated jaw closing, in the
two adult and three juvenile animals used (Table I). No
malocclusion resulted from unilateral stimulation of the
temporal and masseter muscles for periods lasting from
1 to 5 months, while bilateral and simultaneous stimu-
lation of the temporal and masseter muscles in the early
transitional dentition was associated with malocclusion
symptoms which increased steadily during the 12
months after stimulation. These symptoms consisted of
spaced and labially inclined incisors, open bite, over-
jet, and partial crossbite when compared with control
animals (Fig. 11). The tracings show that this was as-
sociated with bone remodeling changes in the palate,
which normally descends (Fig. 12). These experiments
clearly demonstrate that changing the muscle activity
will affect bone morphology.
EFFECT OF MUSCLE ACTIVITY ON BONE
INDUCTION
Induced changes in neuromuscular activity may
take the form either of increased rate and intensity of
muscle contraction or of increased tone. While the
previous experiments confirm that changes in neu-
romuscular activity may affect bone morphology, it is
not known whether the activity responsible for the ob-
served bone changes is phasic or tonic. Harvold,37
therefore, developed another experimental model based
on the following observations of muscle attachment and
reattachment:
1. When bone grafts are placed on the skull bone,
new bone is formed on the exterior and in the marrow
spaces of the graft and the graft is progressively re-
sorbed.
2. When bone grafts are placed on the skull bone
and the overlying muscle is removed, no new bone
forms external to the graft, but only in the medullary
spaces and between the graft and the skull base.
3. If a muscle is detached and left in close proxim-
ity to the bone (3.0 mm.), the muscle will reattach.
4. In the above situation, new bone will form be-
tween the bone surface and the end of the muscle.%
5. If the muscle endings are left beyond a certain
distance from bone, no bone will be formed at either
the bone surface or the muscle ends.3g
These observations indicate that formation of new
bone depends on the presence of both old bone and
muscles in reasonable proximity to each other. They
466 Woodside et al.
Fig. 14.Adult animal. The temporal muscle on the experimental
side was stimulated every second for 16 days. There
evidence of any bone formation on either experimental
control (A) side. (Hematoxylin and eosin stain. Magnification,
x25.)
also indicate that new bone may form under the in-
fluence of some as yet unidentified muscle activity. It
appears that the environment in which bone will form is
closely related to existing bone; this may indicate de-
pendence on the physical micro-environment close to
the bone surface or on factors associated with bone
substance itself.40
On the basis of these observations, an experimental
model designed by Harvold37 was employed to provide
a region outside the skull where the tissue was rela-
tively sheltered from physical movement except for ac-
tivity in the temporal muscle. The activity in this mus-
cle could be monitored and also stimulated. The goal
was to get a clearer idea of the nature of the stimuli
originating in the musculature which affect bone for-
mation and remodeling. The instrumentation used for
muscle stimulation was developed by Vreeland and as-
sociates.41
A 60-watt-output, AC-powered radio transmitter
was mounted on top of the monkey cage. It was keyed
by a B-volt negative pulse from a conventional labora-
tory pulse generator. The transmitting antenna was a
Am. J. Orthod.
June 1983
Fig. 15. Adult animal. The temporal muscle on the experimental
side was stimulated every 5 seconds for 14 days. The control
is no
side (A) shows extensive bone formation, and there is a small
(B) or
amount of bone formation on the experimental side (B). (Hema-
toxylin and eosin stain. Magnification, x25.)
25inch inductively loaded dipole, mounted inside a
vertical 4-inch (diameter) polyvinyl chloride pipe in the
center of the cage. Transmitter and antenna were tuned
to the 13.560 mhz diathermy frequency.
The receiver implanted under the animals skin
(Fig. 10) was powered by a pair of Matshushita BR
2323 3-volt lithium batteries, which fitted inside the
tuning coil and provided many months of power. Such
radio-triggered stimulators are ideal because the stimu-
lus pulse width and repetition rate can be remote con-
trolled. A l-millisecond pulse was used, with its fre-
quency varying from once a second to once every 5
seconds, depending on the experiment.
Sites for our study of bone-muscle interaction were
located on the right and left frontal and parietal bones
below the linea temporalis. The side on which temporal
muscle activity was modified by the muscle stimulator
was the experimental side, and the other was the con-
trol side.
A 5.0 by 1.0 cm. graft was removed from the iliac
crest and cut into pieces to provide grafts for both ex-
perimental and control sides. The superior part of the
 Primate e,ymments in malocclmion and hone induction 67

temporal muscle was exposed, and sufficient muscle extensive condylar remodeling and change in
flaps were lifted from the skull on each side. The inci- mandibular size.
sion was made within 2.0 mm. of the muscle origin to 2. Downward and backward mandibular rotation
ensure that the graft was in contact with the muscle. To may produce large increases in mandibuhr
avoid mobility, the grafts were tightly bound with liga- length.
ture wire to holes drilled in the skull. The free end of 3. Short periods of induced hyperactivity in the
the muscle flap was reattached to the skull by suturing muscles of mastication are associated with
to the remaining tissue at the linea temporalis (Fig. 13). the production of long-lasting malocclusion
The telemetry unit was then activated to begin the symptoms.
muscle twitch at the required rate of repetition. Exper- 4. Muscle activity beyond certain limits may intl:r-
iments have ranged in length from 7 to 42 days with, to fere with bone remodeling.
date, six animals out of eleven having had two to four The original work presented in this study was made p:~s-
pairs of grafts for sequential removal after 14, 2 1, 35, sible, in part, through Grant MA7362 from the Medical Re-
and 42 days. search Council of Canada and Grant DE05397 from the PJa-
In a 42-day sham-operated control animal, exten- tional Institutes of Health, Bethesda, Md.
sive bone formation occurred on both the control and
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