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An experimental analysis of temporomandibular joint reaction force in macaques.

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An Experimental Analysis of Temporomandibular Joint
Reaction Force in Macaques
WILLIAM L. HYLANDER
Departments of Anatomy and Anthropology, Duke University Medical Center,
Durham, North Carolina 2771 0
K E Y WORDS Bone strain
mandibular joint
.
Mandibular function
. J a w mechanics
-
Temporo.
ABSTRACT
Mandibular bone strain in the region immediately below the
temporomandibular ligament was analyzed in adult and sub-adult Macaca fascicularis and Macaca mulatta. Following recovery from the general anesthetic,
the monkeys were presented food objects, a wooden rod, or a specially designed
bite-force transducer. Bone strain was recorded during incisal biting and mastication of food, and also during isometric biting of the rod and/or the transducer.
The bone strain data suggest the following: The macaque TMJ is loaded by a
compressive reaction force during the power stroke of mastication and incision
of food, and during isometric molar and incisor biting. TMJ reaction forces are
larger on the contralateral side during both mastication and isometric molar
biting. Patterns of ipsilateral TMJ reaction force in macaques during isometric
biting vary markedly in response to the position of t h e bite point. During biting
along the premolars or first two molars a compressive reaction force acts about
the ipsilateral TMJ; however, when the bite point is positioned along the Mj,
the ipsilateral TMJ has either very little compressive stress, no stress, or it is
loaded in tension.
An understanding of the biomechanics of
mandibular function requires detailed information about (1) the gross and microscopic
anatomy of the masticatory apparatus, (2)
patterns of mandibular movement, and (3) the
nature of the various external forces (muscular and reaction) that act upon the mandible.
A good deal is known about the anatomy of the
mammalian masticatory apparatus (Schumacher, '61; Turnbull, '70), and about in vivo
patterns of mammalian mandibular movement (e.g., Crompton and Hiiemae, '70; Hiiemae and Kay, '73). However, with the exception of a number of studies on isometric biting
forces in humans, there have been few
experimental attempts to determine in vivo
external forces which act upon the masticatory apparatus, although masticatory muscle
forces have been analyzed indirectly by characterizing either patterns of muscle activity
(e.g., Moller, '66; deVree and Gans, '76) or the
histochemical and contractile properties of
these muscles (e.g., Ringquist, '74; Thexton
AM. J. PHYS. ANTHROP. (1979)51: 433-456.
and Hiiemae, '75; and Maxwell et al., '79). Although there is some information about bite
force magnitudes during mastication (Anderson, '561, there are no in vivo data on the direction of the bite force in mammals (except
for some preliminary experimental work on
humans by Graf "751 and Hylander "7811, or
on the direction or magnitude of reaction
forces that act upon the mammalian temporomandibular joint (TMJ).
Since in vivo TMJ reaction forces have
never been characterized experimentally,
there is a wide range of opinion regarding t h e
nature of these forces. Some workers categorically insist that the mammalian TMJ is
not a load-bearing joint, and therefore reaction forces are absent during mandibular
function (Wilson, '20, '21; Robinson, '46;
Scott, '55; Steinhardt, '58; Tattersall, '73;
Roberts and Tattersall, '74) ; others indicate
'Thm investigation was supported by the followng NIH Re
search Career Development Award (DE 00027J, NIH Research
Grant W E 4531) and a NSF Research Grant (BNS 76 11924)
433
434
WILLIAM L. HYLANDER
t h a t the TMJ is frequently heavily loaded, but
do not distinguish between ipsilateral and
contralateral sides (e.g., Sicher, '51; Smith
and Savage, '59; Davis, '64; Crompton and
Hiiemae. '69; Turnbull, '70; Bramble, ' 7 8 ) .
Those that have considered the ipsilateral and
contralateral sides separately are divided in
their opinion as to whether the two sides are
loaded equally (Roydhouse, '55) or differentially. Page ('54) suggests that only the ipsilateral side is loaded during mastication,
while Hekneby ('74) states that although both
joints are loaded, the ipsilateral TMJ is loaded
more than the contralateral TMJ; others suggest that the contralateral TMJ is loaded
more than the ipsilateral TMJ (Gysi, '21;
Hylander, '75; Smith, '781, and i t has even
been suggested that only the contralateral
TMJ is loaded (Walker, '78; Greaves, '78).
Ideally, to resolve this disagreement it
would be advantageous to measure directly
the direction and magnitude of the reaction
force between the mandibular condyle and the
articular eminence. Unfortunately, this approach would necessitate surgical exposure of
t h e TMJ and damage to the joint surfaces,
which would interfere with normal masticatory movements. In addition, it would be
technically difficult to build and implant a
transducer that would sense in vivo external
reaction force throughout the full range of
condylar rotation and translation.
Another approach, albeit indirect, is to
characterize external reaction force through
the joint by analyzing the pattern of in vivo
bone deformation in the immediate vicinity of
the TMJ, since the amount of bone deformation present presumably would be directly proportional to the magnitude of the external
forces. Although this approach does not permit one to determine the absolute amount of
reaction force along the TMJ, or its direction,
it should allow us to tell whether the TMJ is
loaded, which TMJ is loaded the most, and
when the maximum and minimum loadings
take place. The transducers necessary to measure bone deformation (strain gages) must
also be implanted surgically, and therefore
the subject will not be free of pain in the region overlying the joint. However, structures
of the TMJ are not damaged surgically with
this approach.
In spite of the limitations of this indirect
approach, it was decided to attempt to characterize in vivo reaction force along the TMJ by
measuring bone strain immediately below the
TMJ (the subcondylar region) during various
phases of mandibular function in Macaca
mulatta and Macaca fascicularis. This investigation was undertaken since an understanding of relative amounts of TMJ reaction force
would be useful for testing various models of
TMJ function.
Expected patterns of stress and strain
Let us consider what might be the expected
patterns of stress and strain in the macaque
subcondylar region during (1) the power
stroke of mastication and incisal biting under
conditions of no TMJ reaction force, and ( 2 )
under conditions of a reaction force which
presses the mandibular condyle against the
articular eminence. In addition, expected patterns of subcondylar stress and strain during
the opening stroke will also be considered. The
expected patterns of stress and strain were
originally deduced from anatomical, electromyographical, and jaw movement data.
They were also reproduced on a dry mandible
which had a rosette bonded to the subcondylar
region and upon which the various muscle and
reaction forces were simulated.
Fig. 1 Expected patterns of stress along the medial
and lateral aspects of the subcondylar region during the
opening stroke or during the power stroke, assuming TMJ
reaction forces are absent. During the power stroke, F, is
the medial component of force of the superior head of the
lateral pterygoid muscle and the medial component of
force of that portion of the temporalis which attaches to
the coronoid process. During the opening stroke, F, is the
medial component of force of the inferior head of the lateral pterygoid muscle. F, tends to bend the ramus on
each side towards the midline. This causes the lateral
aspect of the subcondylar region to experience tensile
stress (t), while the medial aspect experiences compressive stress (c). Expected patterns of strain during
such conditions are presented in figures 3A !power stroke)
and 8 (opening stroke). This figure is not meant to imply
that ipsilateral and contralateral muscle forces are of
equal magnitude during the opening stroke or during the
power stroke.
TMJ REACTION FORCE
Expected patterns of su bcondylar bone strain
in absence of TMJreaction force
(a) The effect of the temporalis and lateral
pterygoid muscles
Even if there is no compressive reaction
force acting through the TMJ during the
power stroke of mastication and incision, the
subcondylar region will still experience stress
and strain. For example, it has been shown
that in humans (or macaques) i t is theoretically possible to have powerful contraction
of the temporalis muscle during molar and incisor biting and a t the same time have no reaction force acting through the TMJ (Gingerich,
'71). Under these conditions, a square finiteelement of bone in the subcondylar region will
be deformed in various ways. First, since in
macaques there is a medial component of force
associated with the part of the temporalis
muscle that attaches to the coronoid process,
there will be a tendency for the mandibular
ramus on each side to bend towards the midline; i.e., the tips of the coronoid processes will
bend towards one another (fig. 1).This bending will result in tensile stress along the lateral surface of the subcondylar region and compressive stress along its medial surface. The
resulting pattern of deformation along the lateral aspect of the subcondylar region will be
like that in figures 2B or 3A; i.e., the maximum principal strain ( E , ) (tension) will be
oriented upwards and backwards (or downwards and forwards), while the minimum
Fig. 2 Expected patterns of subcondylar strain during
the power stroke in the absence of TMJ reaction force. Flp
and Ft represent the medial Component of force of the lateral pterygoid muscle and the medial component of force
of that portion of the temporalis muscle which attaches to
the coronoid process, respectively; the small arrows labeled c , and c 2 represent the direction of the maximum
(el) and minimum ( c J principal strains.
A As a first approximation, the macaque mandible is analogous to a curved bar that is bent sharply in the
midline (dashed lines).
B During the power stroke, the subcondylar region is bent by Fb and Flp. During the opening stroke, the
subcondylar region is bent by Flp (temporalis inactive a t
this time). This bending produces tensile stress along the
lateral aspect of the subcondylar region. The resulting
principal strains ( e l and g 2 , oriented as shown) would
deform a square finite-element into a rectangle as indicated.
C Since the twisting moment associated with Ft
probably exceeds the one associated with Fl, during the
power stroke, the subcondylar region is twisted as indicated by the curved arrows. The square finite-element is
deformed into a skewed parallelogram by this torsional
stress as shown by the directions of
and ep. Flp has not
been included in this figure. This figure is not meant to
imply that ipsilateral and contralateral muscle forces are
of equal magnitude during the power stroke.
435
principal strain (c2) (compression) will be oriented upwards and forwards (or downwards
and backwards). Second, the lateral aspect of
the subcondylar region will experience strain
due to contraction of the superior head of the
lateral pterygoid muscle, since in macaques
this muscle also contracts during the power
stroke of mastication (McNamara, '73). The
force of this muscle will also bend the mandibular ramus towards the midline so that the
subcondylar region experiences tensile stress
along its lateral surface, while the medial surface experiences compressive stress (fig. 1).
The deformation pattern in the lateral subcondylar region will also be similar to that
seen in figures 2B or 3A.
I--.
F,
436
WILLIAM L. HYLANDER
c2
A
B
u
C
Fig. 3 Expected patterns of strain of a square finiteelement along t h e lateral aspect of the subcondylar region
during t h e power stroke when there is no reaction force
across the TMJ. Ft is the resultant force from the temporalis muscle; Fb is the bite force; e l and c z are maximum and minimum principal strains. There are three
possible deformation patterns t h a t are superposed on one
another under the above conditions. These deformation
patterns are figured separately in A, B, and C.
A The subcondylar region experiences bending
stress because the medial component of the temporalis
muscle force bends the ramus towards the midline.
B The above force also twists t h e ramus so t h a t
the rostral border of the ramus inverts while the caudal
border everts.
C The ramus is bent in t h e sagittal plane by the
sagittal component of the temporalis muscle force (see
text for discussion).
Contraction of the temporalis and the lateral pterygoid’s superior head will also cause the
mandibular ramus to twist. Twisting which
results from the medial component of the temporalis muscle will result in a medial deflection of the rostral surface of the ramus and a
lateral deflection of its caudal surface, while
twisting produced by the superior head of the
lateral pterygoid muscle will have the opposite effect (fig. 4). Twisting from the temporalis muscle will normally exceed twisting
from the lateral pterygoid muscles because
the superior head of the lateral pterygoid muscle and its twisting moment arm are small relative to the size of the medial component of
t h e temporalis muscle and its twisting
moment arm. The net effect of this twisting
will result in 6 , being directed vertically and
c2 being directed horizontally (figs 2C or 3B).
The combined effect of the above twisting and
bending loads of the temporalis and lateral
pterygoid muscles is that e l will now be
aligned primarily upwards and slightly backwards, while will be aligned primarily backwards and slightly downwards, i.e., a combination between figures 3A and 3B.
Finally, the upwards and backwards pull of
the temporalis muscle will cause the ramus to
be loaded axially and to be bent in the sagittal
plane. Axial loading of the subcondylar region
will be tensile and the direction of will be in
line with the pull of the temporalis muscle, resulting in a pattern similar to the one seen in
figure 3A. Since the subcondylar region is not
in line with the resultant force of the temporalis muscle and bite force, the subcondylar
region will also be bent slightly in the sagittal
plane. The sagittal bending will result in tensile stress along the rostral portion of the
ascending ramus and compressive stress along
its most caudal portion; the resulting pattern
of deformation along the caudal aspect of the
subcondylar region for this type of loading will
be like that in figure 3C. In the more rostral
portion of the subcondylar region, which is
closer to the bending axis of neutrality for
sagittal bending, c 2 will be directed downwards and backwards and e l will be directed
upwards and backwards. Since the combined
strain pattern of bending towards the midline
(fig. 3A), twisting (fig. 3B) and axial loading
(fig. 3A) will be approximately opposite to the
pattern for sagittal bending (fig. 3 0 , i t is theoretically possible to have little or no subcondylar strain with no TMJ reaction force if the
amount of twisting, axial, and midline bend-
TMJ REACTION FORCE
437
and strain for sagittal bending is located along
the caudal edge of the mandibular ramus (i.e.,
as far away as possible from the bending axis
of neutrality).
(b) The effect of the medial pterygoid and
masseter muscles
Fig. 4 Expected patterns of stress during t h e power
stroke in the absence of TMJ reaction forces. The arrows
labeled Ft and F l p are described in figure 2. These forces
tend to bend t h e ramus on each side towards the midline.
In addition, Ft and F l p also have a tendency to twist the
ramus on each side in opposite directions (curved arrows).
However, since the twisting moment associated with Ft
probably exceeds the twisting moment associated with
Flp, twisting will result in inversion of the rostra1 border
of the mandibular ramus (in t h e direction of the curved
arrow along the rostra1 border of t h e mandibular ramus).
See figures 2 and 3 for associated patterns of strain along
the lateral aspect of the subcondylar region. This figure is
not meant to imply t h a t ipsilateral and contralateral muscle forces are of equal magnitude during the power stroke.
ing strain is equal to the amount of sagittal
bending strain. More likely, however, the net
deformation pattern will be similar to a combination of the patterns seen in figures 3A and
3B, since the amount of midline bending alone
will presumably exceed the amount of sagittal
bending. This is primarily because the section
modulus of a section through t h e subcondylar
region is much smaller for midline bending
than it is for sagittal bending, thus making it
much easier to bend the ramus towards the
midline.2 In addition, whereas the finite-element in the subcondylar region or figure 3 is
located in the region of maximum stress and
strain for midline bending, this is not the case
for sagittal bending, since maximum stress
In addition to the temporalis and lateral
pterygoid muscles, the masseter and medial
pterygoid muscles are also active during the
power stroke, and therefore they also have the
potential to deform the subcondylar region.
The medial pterygoid muscles will have a tendency to bend the angular processes of the
mandibular rami towards one another while
the masseter muscles will have a tendency to
bend them away from one another. However,
when acting together, they probably will have
little tendency to bend the mandibular rami in
either direction because even though t h e
masseter muscle in macaques is about twice
as large as the medial pterygoid muscle, t h e
medial pterygoid has a more transverse orientation (Schumacher, '61).The net effect of
muscle size and position probably will result
in nearly equal transverse bending moments
about each ramus. Even if transverse bending
were to occur from these muscles, they probably would not bend the subcondylar region
since only that portion of the mandible between the muscle attachment areas on the left
and right sides would be bent. For example, if
the left and right sides of the curved bar in
figure 2B were pressed together and the point
of applied force was below the square finiteelement, the finite-element would not be
stressed or strained. Only that portion of the
bar between the points of the applied forces
would experience bending stress and strain.
The medial pterygoid and masseter muscles
on each side will also have a tendency to twist
the mandibular ramus on each side. Whereas
the masseter will have a tendency to evert the
lower border of the mandible, the medial
pterygoid will have the opposite effect. When
acting together, however, they probably will
have little tendency to twist each ramus for
reasons similar to those outlined above in the
discussion of bending. In this instance, how_____
'The amount of bending stress in a member is inversely proportional to the section modulus. For midline hending of the ram-, t h e
section modulus for a section passing through the subcondylar region is directly proportional t o a%, where a is t h e medio-lateral
thickness of t h e ramus and h is the antero-posterior thickness nf t h e
ramus. For sagittal hending, the section modulus for the aame a e c ~
tion is directly proportional to h'a. A first-level approximation indicates t h a t t h e section modulus is about seven t i m e larger for aagittal bending than for midline bending.
438
WILLIAM L. HYLANDER
ever, i t is the twisting moments which will be
nearly equal. Even if some twisting were to occur from these muscles, they probably would
not twist the subcondylar region since only
A
Fig. 5 Expected patterns of strain of a square finiteelement along the lateral aspect of the ramus (deep to the
superficial masseter muscle) during the power stroke. The
same pattern will exist in the subcondylar region in the
absence of the TMJ reaction force (see text for discussion).
A
F.
A
B
Fig. 6 Expected patterns of strain of a square finiteelement along the lateral aspect of the subcondylar region
during the power stroke when there is a compressive reaction force acting along the TMJ. The reaction force (Fr) is
aligned vertically (not shown in B). In A the square finiteelement is positioned rostra1 to the reaction force and in B
the square finite-element is immediately below the reaction force. Patterns of strain will vary between these two
deformation patterns (see text for discussion).
that portion of the mandible between the muscle attachment areas on t h e left and right
sides would experience twisting stress. For
example, if the left and right sides of the
curved bar in figure 2C were twisted similarly
(i.e., the lower border on each side is everted),
and the point of application of the twisting
force was below the square finite-element, the
finite-element would not be stressed or
strained. Only that portion of the bar between
the points of the applied forces would experience twisting stress.
In summary then, the action of these two
muscles will probably not twist or bend the
subcondylar region to any appreciable extent.
However, if a square finite-element of bone is
analyzed along a portion of the mandible immediately deep to the superficial masseter
muscle, i.e., inferior to the subcondylar region,
this element will be deformed by masseter and
medial pterygoid muscle contraction, a s
shown in figure 5. The subcondylar region will
be deformed similarly except the magnitude of
the strains will be less. Note that this deformation pattern is similar to the pattern of
figure 3A.
In conclusion, under conditions of no reaction force along the TMJ during biting, the
net deformation pattern along the lateral
aspect of the macaque subcondylar region
probably will be similar to a combination of
figures 3A and 3B, due to midline bending,
twisting, and axial pull from the temporalis
muscle, midline bending due to the superior
head of the lateral pterygoid muscle, and compressive loading due to the masseter and medial pterygoid muscles.
Expected patterns of subcondylar bone strain
in the presence of TMJreaction force
If there is a tendency for the bony articular
surfaces of the TMJ to be pressed together
during normal function, two additional patterns of subcondylar bone strain could conceivably result. First, a square finite-element
of bone will be sheared as shown in figure 6A.
Note that under these conditions, C , is directed upwards and forwards while c2 is directed upwards and backwards. Second, if t h e
square finite-element is located immediately
below the reaction force (as in fig. 6B), the
finite-element will be simply compressed;
will be aligned horizontally, and e 2 will be
aligned vertically. In this instance the compressive strain is directly aligned with the
compressive reaction force. Due to different
TMJ REACTION FORCE
possible positions of the finite-element within
the subcondylar region, recorded strain patterns should vary between these two patterns,
but in general, one would expect that the direction of the principal strains will be a compromise between the patterns seen in figures
6A and 6B. Thus, the net subcondylar deformation pattern during TMJ loading is almost
opposite to the one hypothesized for no TMJ
reaction force during biting (figs. 3A,B).
The foregoing discussion of hypothetical
deformation patterns is based upon the assumption that if a TMJ reaction force is present, its resultant acts along the middle of the
articular surface of the mandible condyle. If
this force acts along the lateral aspect of the
condyle (fig. 71, the subcondylar region will
also be bent so that its lateral surface experiences compressive stress, while its the medial surface experiences tensile stress, i.e., the
two condyles will bend away from one another.
Under these conditions, the resultant pattern
of deformation will be similar to that seen in
figure 6B; the direction of e 2 will be primarily
vertical and E , will be primarily horizontal. If
the resultant reaction force acts about the medial aspect of the articular surface of the condyle (fig. 71, rather than the middle or lateral
aspect, strain patterns will be reversed since
under these conditions the medial surface will
experience compressive bending stress, while
the lateral surface experiences tensile bending stress. The resultant pattern of deformation under these circumstances will be similar
to the one in figure 3B.
In summary, we might expect that patterns
of deformation in the subcondylar region during TMJ reaction force will probably be a compromise between patterns seen in figures 6A
and 6B if the articular surface of the condyle
is loaded by a resultant force which acts along
the middle or lateral aspect of the mandibular
condyle. If the resultant reaction force acts
along the medial articular surface of the condyle, the pattern of deformation will be similar to that seen in figure 3B, which is also one
of the patterns hypothesized for no TMJ reaction force.
Expected patterns of subcondylar bone
strain duringjaw opening
Presumably there would also be subcondylar bone strain during wide opening of the jaw
and the opening stroke of mastication. Bone
strain a t this time will be due to contraction of
the inferior head of the lateral pterygoid mus-
439
cle which will cause the ramus t o bend
towards the midline. This bending will result
in compressive stress along the medial aspect
of the subcondylar region and tensile stress
along the lateral aspect (fig. 1).Therefore, the
expected deformation pattern along the lateral aspect of the subcondylar region will be the
Fig. 7 Expected patterns of stress during asymmetrical loading of t h e TMJ. The arrows indicate t h e point of
application of a TMJ reaction force; t and c represent tensile and compressive stress, respectively. If the mandibular condyle is loaded i n the middle of its articular surface,
t h e medial and lateral aspects of the subcondylar region
will be loaded in compression in this projection. If the condyle is loaded along its lateral aspect (right), t h e subcondylar region along its lateral aspect will experience compressive bending stress, while its medial aspect will experience tensile bending stress. If t h e condyle is loaded
along its medial aspect (left), the bending stress will be
reversed. This figure is not meant to imply that the above
loading patterns are occurring simultaneously on opposite
sides of t h e mandible.
Fig. 8 Expected patterns of strain of a square finiteelement along the lateral aspect of the subcondylar region
during wide opening or during the opening stroke. The
lateral pterygoid muscles bend t h e rami towards the midline and cause t h e above strain pattern (see fig. 2 and text
for discussion).
440
WILLIAM L. HYLANDER
following: E , is directed upwards and backwards while E ? is directed upwards and forwards. Figure 8 demonstrates the expected
strain patterns for jaw opening.
MATERIALS AND METHODS
Subjects
Four subadult male and one adult female
Macaca mulatta and one subadult male and
three adult female Macaca fascicularis served
as subjects. The relative stage of dental development of the subadult males can be seen
in the radiographic tracings of figures 10, 12,
13 and 15.
Each Macaca mulatta was used for one experiment (Experiments 1-5). Each Macaca
fascicularis was used for a t least two experiments (Experiments 6-13).
Bite force measurement apparatus
and procedure
The apparatus and procedure for measuring
bite force has been described elsewhere
(Hylander, '77, '79a). Only the three adult
female M. fascicularis were trained to bite the
force transducer. Without training, macaques
usually refuse to bite a force transducer more
than a few times.
Strain gage bondingprocedure and bone
strain measurement apparatus
Animals were food- and water-deprived for
24 hours and then general anesthesia was
induced with fluothane. A preauricular approach (Morgan, '75) was used to expose subcondylar cortical bone or cortical bone immediately below the subcondylar region, deep t o
the superficial masseter muscle. Extreme care
was taken not to traumatize any of the neurovascular structures during the surgical procedure. Since the bonding site is quite small in
area, particularly in Macaca fascicularis, the
smallest available 120-ohm foil rectangular
stacked rosettes (WA-06-030WR-120, MicroMeasurements) and 120-ohm single-element
strain gages (BAE-06-015CC-120 LE, William
T. Bean, Inc., Detroit, Michigan) were used.
The bonding procedure was like that described
previously (Hylander, '79a) except that the
lead wires were not stabilized by cementation
t o a screw embedded in mandibular bone. Instead, lead wires were stabilized by suturing
the wires and plug t o the macaque's skin
about 5 cm above its zygomatic arch. Either
sham surgical operations were performed on
the opposite side or strain gages were bonded
Fig. 9 Radiograph of t h e left half of a Macaca mulatta
mandible with a rosette bonded in the subcondylar region
(Experiment 5). The long axis of the thick wire indicates
t h e orientation of the middle strain gage element.
to both left and right sides. Although gages
were bonded bilaterally in some of the subjects, only one gage functioned properly in
these instances.
After all surgical wounds were sutured, a
lateral radiograph of the head was taken in
order to locate accurately the position of the
strain gage. Figure 9 is a radiograph of an isolated mandible and rosette strain gage bonded
along the subcondylar region. Following the
radiographic procedures, the animals were
given intramuscular administrations of benzathine penicillin G and procaine penicillin G
and placed in a restraining apparatus previously described (Hylander, '79a).
Recording procedure
Details of the recording procedure are the
same as those described previously (Hylander,
"79a). Once the animal recovered from the
general anesthetic, it was presented fresh apple, a small pine dowel (diameter = 5 mm)
and/or the force transducer.
When the animals masticated it was a simple matter to determine which side the animal
chewed on. This was done by simply observing
the subject's tongue position the apple bolus
along its left or right postcanine teeth. Immediately before and after each bout of mastication or isometric biting the zero level of bone
strain was determined. Due t o thermal
stability, there was no detectable baseline
drift during any bout of chewing or biting. Although untrained macaques will refuse to bite
a force transducer, some macaques will repeatedly bite a small pine dowel. The animals
were encouraged t o bite the dowel in order to
characterize subcondylar bone strain during
44 1
TMJ REACTION FORCE
I
r W
b
ioY
\\\
Exp.
5
Exp.12
Exp. 7
0
\
X
\
Exp. 13
Fig. 10 Tracings of lateral radiographs of the macaque mandibles. The black dots indicate the position of
the rosettes. The X axis is parallel to t h e A strain gage element (Hylander, '79a). The lines indicate only the
mean value for the direction of the minimum principal strain (compression) ( € 3during apple mastication and
incision; lines labeled b and w indicate contralateral (balancing) and ipsilateral (working) sides, respectively;
lines labeled i indicate incision and lines labeled o indicate wide opening. Thus, a single rosette in each of t h e
above experiments is used to characterize bone strain during t h e above behaviors.
isometric biting. Mandibular bone strain was
recorded during apple mastication or when
the macaque bit the dowel or transducer.
When animals bit on the dowel or the force
transducer, bone strain could be easily correlated with bite force values. To assist in monitoring simultaneous bone strain and timing of
portions of the masticatory cycle, the animal
and the chart recorder pens and output were
videotaped and analyzed as described elsewhere (Hylander, '79a).
Recording sessions often lasted several
hours with frequent intermittent rest periods.
At the end of the recording period, the subjects were tranquilized with Ketamine hydrochloride and the strain gagek) were removed.
All animals were returned to their cages within 24 hours of the original surgical procedure
and all resumed eating after recovery from
the tranquilizer. The post-operative periods
were uneventful. Infections were never encountered in any of the subject^.^
Experimental Set A
The specific aim of Experimental Set A was
to analyze patterns of peak mandibular bone
strain along the subcondylar region and deep
to the superficial masseter muscle during incisal biting (incision) and mastication of food.
One aspect of this analysis was t o compare the
direction and magnitude of bone strain values
3All Macaca mulatta subjects were sacrificed a day or so following the hone-atrain experiments because they were experimental
controls for a study on vascular plaque formation in macaques on a
low and high cholesterol diet (Principal Investigator. Dr. Otto
Hagen, Department of Surgery, Duke University, NIH grant HL.
15448).
442
WILLIAM L. HYLANDER
A
B
C
11
J
a
ul
W
I-
4
Q
u
I2 ,
0
u
TENSION
COMPRESSION
0
W
rI-
F
Fig. 11 Chart recording of subcondylar bone strain recorded from the A, B, and C elements of a rosette during
apple mastication (Experiment 5). Bone strain scale is in
microstain units; time is in 1-second intervals. The zero
level of bone strain is indicated for each channel. In channel B, peaks t o the right correlate with the power stroke
and peaks to the left correlate with opening.
on the working or ipsilateral side of the mandible with bone strain values on the balancing
or contralateral side during mastication. Bone
strain values during incisal biting of whole apples were also compared t o the mastication
data. In addition, bone strain patterns during
jaw opening were also analyzed. The above
experimental set consisted of seven subcondylar bone strain experiments and two experiments on bone strain deep to the superficial
masseter.
Experimental Set B
The specific aim of Experimental Set B was
t o analyze patterns of peak mandibular bone
strain along the subcondylar region and deep
to the superficial masseter muscle during
isometric biting. An important part of this
analysis was to compare the direction and
magnitude of bone strain values on the ipsilatera1 side of the mandible with the bone strain
values on the contralateral side. This set of experiments is made up of two subsets. Subset 1
involved isometric biting on a wooden dowel
while subset 2 consists of isometric biting on a
force transducer. Subset 1consists of four subcondylar bone strain experiments and one experiment on bone strain below the superficial
masseter; subset 2 consists of one experiment
on subcondylar bone strain and one on bone
strain below the superficial masseter muscle.
The direction and magnitude of the maximum and minimum principal strain were calculated following Dally and Riley ('65). Descriptive statistics for bone strain and bite
force values were generated. Bone strain (the
dependent variable) and bite force (the independent variable) data were also analyzed
utilizing linear regression techniques (regression line fit by method of least squares).
Strain (€1, a dimensionless unit, equals the
change in length (AL) of an object divided by
the original length (L) of the object, i.e.,
E = &. The unit of strain is the microstrain
( ~ € 1Lwhich
, . equals 1 X
inchedinch or
millimeters/millimeter, etc. By convention,
tensile strain is a positive value and compressive strain is a negative value. In this
study the maximum principal strain (E ,) is the
largest tensile strain value whereas the minimum principal strain ( E J is the largest compressive strain value. The direction of e 2 is
given in degrees, and its direction is relative
to the long axis (the X axis) of one of the three
strain gage elements within a rectangular
rosette. Adding or subtracting 90" t o the direction of yields the direction of e l .
RESULTS AND DISCUSSION
In this section, emphasis is placed on both
the magnitude and direction of the maximum
amount of recorded compressive strain ( € 3 .
The values of the maximum amount of recorded tensile strain (E ,) are included in tables
1, 3 and 4 but will not be dealt with here.
Experimental Set A
1. Rosette analysis of bone strain during the
power stroke of mastication and incision
In these experiments, the rosette was posi-
443
TMJ REACTION FORCE
TABLE 1
Descriptive statistics of subcondylar bone strain values during incision and mastication of apples (rosette analysis)
Principal strains
Experiment
Maximum
Minimum
(6,)
Angle of minimum
principal strain ( c J
(6
S.D.
Mean
23
66
17
21.8
4.0
33.7
110.8
- 341
- 353
- 531
- 664
43
66
177
- 183
- 286
- 306
- 633
-544
- 981
84
- 130
N
Mean
Largest
S.D.
Mean
Largest
80
102
137
237
27
106
27
50
- 105
- 155
- 180
- 280
33
- 359
- 108
- 359
- 145
-
14
88
149
27
69
47
40
13
136
191
36
323
254
186
59
33
84
- 202
140
84
8
45
123
254
90
293
431
24
61
131
26
109
28
14
60
36
65
52
114
60
117
82
27
13
24
20
Range
S.D.
M. mulatta (3-82)
Experiment 1
Ipsilateral
Contralateral
Incision
Opening
(threat)
M. mulatta (6-20)
Experiment 2
Ipsilateral
Contralateral
Incision
M. mulatta (6-41)
Experiment 5
Ipsilateral
Contralateral
Incision
M.fascicularis (1)
Experiment 7
Ipsilateral
Contralateral
Incision
Opening
(threat)
M. fascicularis (4)
Experiment 12
Ipsilateral
Contralateral
Incision
M.fascicularis (4)
Experiment 13
Ipsilateral
Contralateral
Incision
Opening
(threat)
1
-
- 344
-
- 49
- 77
- 55
- 95
- 132
-
82
6.2to 34.0
2.7to 22.5
6.6
4.1
103.3to 124.3
5.9
67.5
81.2
58.2
45.8to 88.0
74.6to 90.3
37.7to 73.4
6.8
3.6
12.0
56
113
284
56.1
46.2
50.2
48.8to 80.8
35.3to 60.8
48.9to 51.8
4.2
4.6
1.1
24
19
26
20
89.4
76.8
101.5
103.4
77.7 to 100.2
51.8 to 104.5
86.0 to 111.7
91.6 to 111.5
7.1
-
-
-
5.8
6.0
6.6
-
-
-
-
-
-
-
-
-
-
11
4
36
146
85
203
28
66
- 85
- 226
- 153
- 347
43
123
61.6
68.3
49.lto 68.6
67.5to 69.3
5.3
1.0
134
97
35
16
60
77
46
128
189
186
145
234
31
45
45
50
- 74
- 99
- 283
- 213
- 207
- 753
- 47
34
44
167
14
3.6
8.5
41.8
109.4
-27.2to 27.7
6.4to 28.5
9.2to 81.0
100.8 to 115.4
7.8
5.6
18.9
4.1
-
22
-
Note: Bone strain values are in microstrain units. N = number of power strokes or the number of times mouth was opened wide. Angle values are in
degrees. Animal identification number in parentheses. See table 2 for additional data from Experiment 12.
tioned in the subcondylar region (Experiments 1,2, 5, 12, 13) or deep to the superficial
masseter muscle (Experiment 7). The location
of the rosette in each experiment is shown in
figure 10. A representative tracing of subcondylar bone strain during mastication is illustrated in figure 11.
(a) Bone strain magnitudes
When the rosette was positioned in the subcondylar region, the mean values of c 2 on the
contralateral side are larger than and differ
significantly from the corresponding ipsilateral-side values (p < 0.001) (table 1). In con-
trast to the above pattern, the mean value of
c 2 deep to the superficial masseter muscle (Experiment 7) on the ipsilateral side is larger
than and significantly different from the
mean value on the ipsilateral side (p < 0.001).
When the animals bit apples with their incisors, mean values of c 2 for the subcondylar
region generally exceed those values for mastication. In all but one instance these mean
values are significantly different from the
mastication mean values (p < 0.001). During
incisal biting the mean and maximum values
of bone strain below the superficial masseter
muscle are larger than and significantly dif-
444
WILLIAM L. HYLANDER
ferent from contralateral values (p < 0.001),
and virtually identical to ipsilateral values
during mastication (Experiment 7).
(b) Bone strain direction
In every instance during the power stroke of
mastication and incision, E ? in the subcondylar region is directed upwards and backwards
(or downwards and forwards). In contrast, the
direction of c 2 below the superficial masseter
muscle (Experiment 7) is directed upwards
and forwards. The mean values of the direction of e ? during incision and mastication
(ipsilateral and contralateral sides) are all
significantly different from one another within each experiment (p < 0.051, but in the subcondylar region these values show no consistent pattern from one experiment t o another.
Unlike patterns of bone strain in the corpus of
the macaque mandible (Hylander, '79a), in
some instances the ipsilateral values are directed more vertically than the contralateral
values, while in other instances the reverse
pattern is found.
2. Single-element strain gage analysis of bone
strain during the power stroke of
mastication and incision
A single-element strain gage was positioned
either in the subcondylar region (Experiments
8, 9, 12) or deep to the superficial masseter
muscle (Experiment 4). The strain gage position and alignment are illustrated in figure
12. In the subcondylar experiments, mean
values of compressive subcondylar bone strain
during mastication are larger on the contralateral side than on the ipsilateral side (Experiments 8, 9,121, and these mean values are
significantly different from one another (p <
0.001) (table 2). Mean values of compressive
bone strain during incision exceed corresponding values during mastication (table 21,
although these values are not always significantly different from one another (contralatera1 and incision mean values are not significantly different from one another in Experiments 8 and 9).
Similar t o the rosette analysis of bone strain
deep to the superficial masseter muscle, a very
different pattern of bone strain occurs deep to
the superficial masseter. Whereas compression was sensed by the single-element gages in
the subcondylar region (Experiments 8,9,12),
the single-element gage deep t o the superficial masseter muscle sensed tensile strain
(Experiment 4) (table 2 and fig. 12).
Exp. 4
A
Exp. 9
Fig. 12 Tracings of lateral radiographs of the macaque
mandibles. The black dots indicate the position of the
single-element gages and the lines indicate the orientation of the long axis of each gage. In Experiment 12 the
lines labeled B and C represent the B and C elements of a
rosette.
3. A comparison of expected and recorded
patterns of strain during the power
stroke of mastication
and incision
Patterns of recorded subcondylar bone
strain support the hypothesis that a compressive reaction force is present along the
TMJ during the power stroke of mastication
and incision. Thus, the direction of the recorded principal strains (fig. 10) range between the theoretical patterns seen in figures
6A and 6B. Since eubcondylar strain levels are
always larger on the contralateral side, these
data further suggest that among macaques
(and by inference humans and all other anthropoids) the contralateral TMJ is loaded
more than the ipsilateral TMJ during mastication. This confirms the patterns predicted
TMJ REACTION FORCE
445
'CABLE 2
Descriptive statistics ofsubcondylar bone strain values during incision and mastication
ofapples (single-elementgage analysis)
Experiment
N
Mean
Largest
S.D
M. mulatta (6-17)
Experiment 4
Ipsilateral
Contralateral
Opening
(contralateralside)
-
-
-
132
200
27
29
- 258
- 420
42
103
87
-
43
38
63
162
222
33
- 146
102
83
16
-
105
100
26
- 65
- 175
- 237
90
M. fascicularis (2)
Experiment 8
Ipsilateral
Contralateral
Incision
M. fascicularis (2)
Experiment 9
Ipsilateral
Contralateral
Incision
M . fascicularis (4)
Experiment 12
Ipsilateral
Contralateral
Incision
- 181
- 204
- 420
42
- 83
- 190
- 63
-
68
-
113
19
37
24
Element B
- 134
- 380
- 514
23
81
145
Element C
Ipsilateral
Contralateral
Incision
105
100
26
- 70
- 182
- 256
- 146
434
- 560
-
28
86
166
Xote. Bone strain values are in microstrain units N = number of power strokes or openingstrokes. Animal identification num
ber in parentheses. In Experiment 12, one element of three-element rosette malfunctioned (A element) after a limited amount of
data were recorded (table 1).
for apes, macaques, and humans (Gysi, '21;
Hylander, '75, '79b; Hylander and Sicher, '79;
Smith, "78). These data make it unlikely that
in humans both joints ordinarily are loaded
equally during mastication (Roydhouse, '551,
or that in humans the ipsilateral side is loaded
more than the contralateral side (Hekneby,
'74). Since both sides are apparently loaded,
these data do not support the hypothesis that
TMJ reaction forces are only present on the
contralateral side (Walker, '78; Greaves, '78)
or ipsilateral side (Page, '54). Moreover, these
data are incompatible with the hypothesis
that TMJ reaction forces are absent during
mastication (Wilson, '20, '21; Robinson, '46;
Scott, '55; Steinhardt, '58; Tattersall, '73;
Roberts and Tattersall, '74).
Patterns of recorded bone strain deep to the
superficial masseter muscle are very similar
t o the expected patterns seen in figure 5 .
These data support the hypothesis that bone
strain in this region is due primarily to muscle
force from the medial pterygoid and masseter
muscles. In Experiment 7 bone strain along
the ipsilateral side exceeded contralateral-
side values during mastication, suggesting
that the ipsilateral-side muscle force exceeds
the contralateral-side muscle force during
unilateral mastication of apples. Further support for this possibility comes from EMG studies by Luschei and Goodwin ('74) which show
that the peak electrical activity of the masseter muscle in macaques is greater on the
ipsilateral side than on the contralateral side
during mastication. The strain data also are
consistent with EMG studies in humans
which demonstrate that masseter and medial
pterygoid muscles are more active on the ipsilateral side during mastication of soft food
objects (Moller, '66; Ahlgren, '66).
The findings here are also consistent with
the lever model of mandibular function. The
lever hypothesis predicts that reaction forces
are present along the TMJ during the power
stroke. An alternative model suggests the
mandible functions as a beam, rather than a
lever, during the power stroke (Smith, '78;
Walker, '78). This suggestion is apt to confuse
rather than enlighten, since every loaded
lever functions as a beam, i.e., a beam is a
446
WILLIAM L. HYLANDER
member subjected to transverse loads (loads
perpendicular to its long axis) (Arges and
Palmer, '63). When analyzing external forces
on the mandible (muscular, bite, and condylar
reaction forces) i t is appropriate to consider
whether or not the mandible functions as a
lever. When analyzing internal forces of the
mandible (i.e., those forces tending to resist
bone deformation), i t is appropriate to consider the mandible as a beam and to analyze
bending stress within it utilizing beam theory
if the mandible is being loaded transversely.
Stating that i t is more appropriate to consider
the mandible as a beam, rather than a lever, is
much like saying it is more appropriate to consider a macaque a mammal, rather than a primate. It of course all depends on the problem.
4. Rosette analysis of bone strain during
jaw opening
Bone strain data during wide opening are
presented in table 1.The magnitude of strains
recorded from the subcondylar region and
deep to the superficial masseter muscle during wide jaw opening is usually less than
strain magnitudes during the power stroke or
during isometric biting (Experiments 1, 13, 7).
Moreover, strain magnitudes are greater during wide opening than during the opening
stroke of mastication. The direction of E~ during wide opening is upwards and forwards in
both the subcondylar region and deep to the
superficial masseter muscle (fig. 10).The direction of t qduring the opening stroke of mastication is positioned similarly, although not
figured here.
5. A comparison of expected and recorded
patterns of bone strain during
jaw opening
The direction of the principal strains during
jaw opening are similar to the direction of
principal strains predicted if the subcondylar
region and the region deep to the superficial
masseter muscle were experiencing tensile
bending stress due to midline bending of the
mandibular ramus (fig. 8). This bending is presumably due to the force of the inferior head of
the lateral pterygoid muscle.
Experimental Set B
1. Rosette analysis of bone strain during
isometric biting on the wooden dowel
In these experiments the rosette was positioned in the subcondylar region (Experiments 1, 5, 11, 13) and deep to the superficial
Exp. 1
wx
w1
E x p . 11
n
E x p . 13
Fig. 13 Tracings of lateral radiographs of the macaque
mandibles. The black dots indicate the position of the
rosettes. The X axis is parallel to the A strain gage element. The lines indicate the mean value for the direction
of c 2 during isometric biting of the wooden dowel; lines labeled b and w indicate contralateral and ipsilateral aides,
respectively; lines labeled i indicate incisal biting. In Experiment 13, 1 and 3 indicate biting along the M1 and M3,
respectively.
masseter muscle (Experiment 7). The location
of the rosette in each experiment is shown in
figure 13.
(a) Bone strain magnitudes
When the rosette was positioned in the subcondylar region the mean value of e 2 on the
447
TMJ REACTION FORCE
TABLE 3
Descriptive statistics of subcondylar bone strain values during mnmetric bzting (rosette analysB)
Principal strains
Exprriment
Angle of minimum
principal strain
Minimum Ic,)
Maximum ( c j
N
Mean
Largest
SD
Mean
1,argest
SU
Mean
37
28
61
115
261
204
236
338
320
59
55
75
-109
-373
-243
-215
-472
-372
55
71
89
11.6
6.4
6.7
23
31
96
144
200
404
53
108
-224
-331
-360
-972
84
234
32
57
71
59
111
121
23
37
91
-105
-131
-183
7
23
42
5
109
200
43
115
- 48
-305
- 69
-857
16
105
247
72
20
22
7
99
146
92
168
509
166
68
121
64
Range
SD
M mulatta (3-82)
Experiment 1
Ipsilateral
Contralateral
Incisor
-14.5to
39.5
12.9
22.5
15.0
3.4
5.9
56.9
55.3
51.lto 63.8
48.7to 66.2
3.6
4.8
24
39
96.2
89.6
71.9 to 124.4
67.5 to 105.6
13.5
7.0
17
260
37.2
-13.3to
-263
72
14.3
-
-183
-768
-220
58
184
25
100.2
39.9
25.8
- 1.1to
- 1.7to
M. mulatta (6-41)
Experiment 5
Ipsilateral
Contralateral
M. fascicularis (1)
Experiment 7
Ipsilateral
Contralateral
~
M. fascicularis (3)
Experiment 11
Ipsilateral'
Contralateral
M. fascicularis (4)
Experiment 13
Ipsilateral (M1)
Ipsilateral (M3)
(strain reversal)
Contralateral
Incisor
-
86
-101
-410
-183
-
-
72.7
17.4
5.1to 47.0
16.7
77.8 to 129.3
28.9to 57.0
5.2to 55.8
111.9
7.8
23.6
Note: Bone strain values are In microstrain units. N = number of isometric bites. Angle values are in degrees. Animal identification number in
parentheses
*Accurate determination of minimum principal strain angles not possible due to low strain levels. The hite point is unilateral along the M1-MZ region
unless otherwise noted in parentheses.
contralateral side during molar biting exceeds
the corresponding ipsilateral-side value by a
considerable amount within each experiment
(table 3). In each instance, these mean values
are significantly different from one another (p
< 0.05). In contrast, although the mean value
of c 2 deep to the superficial masseter muscle is
larger on the contralateral side during molar
biting, these values are not significantly different from one another.
In each experiment the mean value of e q
during incisor biting is larger than the mean
value on the ipsilateral side and smaller than
the mean value on the contralateral side during molar biting (Experiments 1, 13). These
values are significantly different from one
another (p < 0.01).
(b) Bone strain direction
Generally the direction of e 2 in the subcondylar region during molar biting is upwards
and backwards (Experiments 1, 5, 11, but see
Experiment 13 discussed below). In contrast,
the direction of c 2 deep t o the superficial
masseter muscle is upwards and forwards,
rather than upwards and backwards. All of
the mean values for the direction of e 2 within
each experiment are significantly different
from one another (p < 0.05) except as indicated in figure 13 (table 3).
In Experiment 1 3 the monkey was allowed
t o bite the dowel along its third molars (M3)
as well as the first molars ( M l ) , whereas only
M1-M2 biting data were obtained from the
other experiments. Whenever biting took
place along the M3 and when ipsilateral subcondylar bone strain was being monitored,
bone strain patterns suddenly were reversed
from the patterns which occurred during biting on the M1 (Experiment 13). This reversal
did not occur during M3 biting when subcondylar bone strain was being monitored along
the contralateral side. It also did not occur in
any of the experiments in which biting was restricted solely to the M1-M2. Since the two
strain patterns for the ipsilateral side in Ex-
448
WILLIAM L. HYLANDER
periment 13 are quite different, they are analyzed and presented separately. The mean
values for the magnitude of e 2 for these two
patterns are not significantly different from
one another, but the mean values for the direction of
are dramatically different. The
direction of e 2 during biting along the M1 is
upwards and backwards, as it is in the other
subcondylar bone strain experiments. In contrast, when biting occurred along the M3 the
direction of e 2 was shifted almost 90" (fig. 13).
2. A comparison of expected and recorded
patterns of strain during
isometric biting
With the exception of recorded subcondylar
bone strain patterns along the ipsilateral side
during biting on the M3 (Experiment 131,
subcondylar bone strain patterns during isometric biting suggest that the TMJ is loaded
by a compressive reaction force (compare fig.
13 with figs. 6A,B). Furthermore, since subcondylar strain levels are higher on the contralateral side, these data suggest that the
contralateral TMJ is loaded more than the ipsilateral TMJ.
Strain patterns deep to the superficial
masseter muscle indicate that this region is
deformed primarily by the medial pterygoid
and masseter muscles (note the similarity between fig. 13 and fig. 5). The data suggest that
the muscle forces on the ipsilateral and contralateral sides may not differ significantly
from one another during isometric biting.
These data are in accord with Blair's data
(cited in Luschei and Goodwin, '74) which
show that during isometric molar biting, EMG
activity patterns in the masseter muscle on
both ipsilateral and contralateral sides in macaques are very similar. Similar observations
on human subjects have been reported (Finn
et al., '79). This EMG and bone-strain pattern
is in contrast t o the pattern found during mastication of soft foods which suggest that the
masticatory muscles on the ipsilateral side
generate much more force than the muscles on
the contralateral side. Perhaps biting hard
objects or masticating tough foods requires
relatively more contralateral jaw muscle activity than chewing soft foods. Moller ('74)
notes that whereas the masseter and medial
pterygoid muscles are much more active on
the ipsilateral side than on the contralateral
side during gum chewing in humans, levels of
activity for both sides are nearly equal during
carrot mastication. Furthermore, Luschei and
Goodwin ('74) note that differences in peak
EMG amplitudes between masticatory muscles on each side usually are very small when
macaques chew monkey biscuits. In summary,
i t appears that among macaques (and perhaps
humans also?) a greater relative amount of
contralateral muscle force is generated during
isometric biting or powerful mastication, than
during the mastication of soft foods such as
apples.
Another notable feature of these data is the
fact that subcondylar bone strain during
isometric biting along the M3 suddenly reversed itself from the pattern seen during biting along the M1 (Experiment 13). Moreover,
whereas strain patterns during biting along
the M1 are very similar to expected patterns
associated with a compressive reaction force
along the TMJ (compare fig. 13 with fig. 6A),
the recorded strain pattern during biting
along the M3 is very similar to the pattern
seen in figure 3A. The strain reversal data
suggest a number of possible interpretations:
(11 Compressive reaction forces are very small
or absent along the ipsilateral TMJ during biting along the' M3; (2) Compressive reaction
forces are not only absent, but there is a tendency for the mandibular condyle t o lift off
the articular eminence on the ipsilateral side;
furthermore, this movement is checked by
the temporomandibular ligament (sphenomandibular and stylomandibular ligaments
also?), resulting in tensile stress across the
TMJ which contributes to the recorded strain
patterns. (3) The articular surface of the mandibular condyle is asymmetrically loaded, i.e.,
although there is still a compressive reaction
force across the TMJ, the resultant reaction
force acts along the medial aspect of the mandibular condyle rather than along the middle
or lateral portion. This latter type of loading
causes the subcondylar region t o be bent so
that the medial portion experiences compressive stress while the lateral portion experiences tensile stress, thereby causing the
recorded deformation pattern (fig. 7).
The available data do not allow any of the
above possibilities t o be confidently eliminated, but a mechanical analysis of the ipsilateral side of the mandible increases the
plausibility of the first two possibilities, i.e.,
either the existence of no compressive stress
or possibly tensile stress along the ipsilateral
TMJ during M3 biting.
As seen in figure 14, there are a t least three
forces acting on the ipsilateral side of the ma-
TMJ REACTION FORCE
caque mandible during unilateral isometric
biting. These are bite force (Fb), an ipsilateral
resultant muscle force (F,) and a force being
transmitted through the symphysis from the
contralateral t o the ipsilateral side (F,). The
last force is associated with the contralateral
muscle force. In order to simplify this analysis, only the vertical components of these
forces are considered here and no consideration is given to the effects they have on mandibular twisting.
If moments are taken about the bite point in
figure 14,then in order for there not to be a
reaction force through the TMJ during conditions of equilibrium, the moment associated
with F, must equal the moment associated
with F,, i.e., (FJ(y1 = (F,J(x). If (F,)(y) is
greater than (Fml(x),a tensile reaction force
will be present along the ipsilateral TMJ. If
(F,)(y) is less than (Fm)(x),a compressive
reaction force must be present along the ipsilateral TMJ. From the above analysis, it can
be seen that altering the bite point (i.e., shifting it from MI to M J should markedly change
the reaction force patterns along the ipsilatera1 TMJ since moving the bite point posteriorly decreases x and increases y while moving the bite point anteriorly has the opposite
effect.
This analysis also demonstrates that it is
theoretically possible t o have either no stress
or tensile stress acting across the ipsilateral
TMJ during unilateral molar biting. This possibility supports models of TMJ function
advanced by Walker ('78) and Greaves ('78).
In macaques, however, these models are only
supported by data during biting on the MB.
Models advanced by Gysi ('211, Hylander ('75,
'79b), Hylander and Sicher ('791, and Smith
('78) are also supported by these data since
these models predict either no stress or tensile
stress along the ipsilateral TMJ during biting
along the more posterior aspect of the tooth
row. Models advanced by Page ('54) (only
stress on ipsilateral TMJ), Hekneby ('74)
(more stress on ipsilateral TMJ), and Roydhouse ('55) (equal stress on ipsilateral and
contralateral TMJ), however, are not supported by these data. The possibility of tensile
stress across the ipsilateral TMJ correlates
with cinefluorographic observations by Koivumaa ('61). Koivumaa reported that the
mandible rotated about the bite point during
unilateral molar biting of a hard caramel in
several human subjects. At this time the mandibular incisors moved upwards while the ipsi-
449
Fig. 14 Mechanics of the ipsilateral side of t h e macaque mandible during unilateral isometric molar biting.
Condylar reactions are not included here. This is a firstlevel approximation since only the vertical components of
the (1) bite force (Fb), (2) ipsilateral muscle force (Fm),
and (3) force transmitted from contralateral to ipsilateral
sides (F,), are considered. If moments are taken about the
bite point, Y and X are t h e distances between the bite
point and F, and F,, respectively. In order to satisfy conditions of equilibrium and not have reaction force along
t h e TMJ. F,
X must equal F, . Y. If F,, X is larger or
smaller than F, Y, there will be a compressive or tensile
reaction force along the TMJ, respectively. Moving the
bite point caudally increases Y and decreases X. Moving
t h e bite m i n t rostrallv has the omosite effect (see text for
discussion).
.
.
.
I.
lateral mandibular condyle lifted off the articular eminence several millimeters. Perhaps at
this time the temporomandibular ligament
checked further condylar movement, resulting in tensile stress across the ipsilateral
TMJ.
3. Comparison between isometric biting data
and mastication data
In general, the isometric biting data are
very similar t o the mastication and incision
data in that (1) mean compressive bone strain
values in the subcondylar region on the contralateral side exceed ipsilateral-side values;
(2) mean values for the direction of c 2 in the
subcondylar region are generally upwards and
backwards; and (3) mean values for the direction of e* deep to the superficial masseter
muscle are upwards and forwards. Mastication and incision data differ from isometric
biting data in the following respects: (1) bone
strain values tend to be larger during
isometric molar biting; (2) in contrast t o mastication the difference between bone strain
values on the ipsilateral and contralateral
sides during isometric molar biting is larger;
(3) whereas subcondylar bone strain values
450
WILLIAM L. HYLANDER
during apple incision generally exceed subcondylar bone strain values during apple mastication, bone strain values during isometric
incisor biting do not generally exceed bone
strain values during isometric molar biting;
and (4) subcondylar bone strain reversals on
the ipsilateral side were not encountered during mastication, as they were during isometric
molar biting.
It is not surprising that bone strain values
during isometric biting exceed bone strain
values during mastication. A soft object like
an apple does not require a powerful bite, and
therefore is not associated with powerful muscular and reaction forces. There are two possible reasons why isometric molar biting results
in larger bone strain differences between ipsilateral and contralateral sides. First, in contrast to apple mastication, powerful isometric
molar biting might be associated with larger
relative amounts of muscle force on the contralateral side. Second, the bite point during
isometric molar biting (usually along the M I M,region) might be slightly caudal to the resultant bite point during mastication (position unknown). Both of these possibilities
have the effect of increasing F,. y relative to
F,.x (fig. 141, and therefore they will both
reduce the amount of compressive reaction
force along the ipsilateral TMJ, which will result in larger differences in reaction force between ipsilateral and contralateral sides. Furthermore, increasing the amount of muscle
force along the contralateral side will directly
increase the compressive reaction force along
the contralateral TMJ, contributing to a
larger difference between ipsilateral and contralateral sides.
As noted above, in contrast to apple mastication, incisal biting of apples, involves larger
amounts of subcondylar bone strain. In addition to obvious mechanical factors which
should favor larger condylar reaction forces
during incisal biting, this observation probably also reflects the relative ease of apple mastication as opposed to incisal biting of apples.
A similar pattern was found while recording
bone strain in the mandibular corpus during
apple incision and mastication (Hylander,
'79a). Isometric biting on the incisors, however, usually results in lower subcondylar
strain values than during isometric molar biting. This observation probably indicates relatively low incisor bite force values. In macaques, a single incisor tooth and its periodontium is not nearly as well adapted as a molar
tooth and its periodontium to withstand large
X
Exp. 7
Fig. 15 Tracings of lateral radiographs of two macaque mandibles. The black dots indicate the position of
the rosettes. The X axis is parallel to the A strain gage
element. The lines indicate only the mean value for the direction of c 2 during transducer biting; lines labeled b and
w indicate contralateral and ipsilateral sides, respectively; p indicates premolar biting and 1 and 3 indicate biting
along the M1 and M3, respectively.
biting forces. Perhaps isometric incisor bite
force values are low in order to avoid pain in
the periodontium of the one or two incisors
involved in biting a dowel. In contrast, when
several incisors are loaded simultaneously, as
in apple incision, larger muscle, bite, and TMJ
reaction forces can be generated without discomfort.
Finally, it is not surprising that strain
reversals were only encountered during isometric molar biting; during mastication, the
moment (F,) (x) probably always exceeds
(F,) (y) because the resultant bite force is
located in the M,-Mz region (fig. 14).On the
other hand, altering the position of the bite
point to the M 3during isometric biting results
in large values of y and small values of x, causing the moment (F,) (XIto be exceeded by (or
equal to) the moment (FJ (y). If this occurs,
tensile stress (or no stress), rather than compressive stress, will act across the joint.
4. Rosette and single-elementstrain gage
analysis of bone strain during
isometric transducer biting
In these experiments, a rosette or single-element strain gage was positioned in the sub-
451
TMJ REACTION FORCE
Y
t
contralateral
Confralotcml
r=-077
Slops = - 3 0 . 5
: # . .* ..
r : -0.96
(1
G -400-
a
E
g
... .
- ...- . .
. .... . . . .
. ...-..*:-.
. .....
- -200-
-
. . . . . *. .
x : * .....
.
- . . *. .
~
slope: -15.0
-100-
* I
-200-
&
i
a
0-
.. . . .
-3
-
f
In
s
a..
-300-
-4001
Exp.il
-600-
*
I
Ex0.9
0
0
4
12
8
Bite Farce (kgl
.
-5
J
8
24
16
16
32
Bite Force lkgl
OC.
r--060
Slope--l5.4
. .
* *
lpsllateral
r: -0.53
s1o.e: -1.7
.
t
5
.. :
..
-300-
E
*-
-400
0
4
8
Bite Force 1kq)
12
I
16
-looj
0
Elp9
8
*
16
24
32
B i l e Force I k g l
Fig. 16 Scattergram of bite force and subcondylar
bone strain values in Experiment 9; r is Pearson's product-moment correlation coefficient.
Fig. 17 Scattergram of bite force and subcondylar
values of c 2 in Experiment 11 during transducer biting; r
is Pearson's product-moment correlation coefficient.
condylar region (Experiments 8, 9, 11) and
deep to the superficial masseter muscle (Experiment 7 ) .The location of the rosette for Experiments 7 and 11 is shown in figure 15, and
the location and alignment of the single-element gage for Experiments 8 and 9 is shown in
figure 12.
side than on the ipsilateral side during molar
biting. Ipsilateral bone strain in the subcondylar region was also recorded for premolar biting (Experiment 111, and it was found that
bone strain on the ipsilateral side was relatively greater during premolar biting than
during molar biting since the slope value for
premolar biting is twice as large as, and significantly different from, the slope value for
molar biting (p < 0.01) (table 4).
In the one experiment measuring bone
strain deep to the superficial masseter muscle
during isometric transducer biting (Experiment 7), the slope values for the ipsilateral
and contralateral sides are not significantly
different from one another, and are much
smaller than the slope values associated with
the subcondylar rosette values.
(a) Bone strain magnitude
Both descriptive statistics and the regression analysis of bone strain (dependent variable) and bite force (independent variable)
values are presented in tables 4 and 5. Plots of
bite force versus bone strain are presented in
figures 16 and 17 for Experiments 9 and 11. In
the three subcondylar bone strain experiments the slope values for the regression analysis of molar bite force and bone strain on the
contralateral side always exceed the slope
values for the regression of molar bite force
and bone strain on the ipsilateral side, and
these values are significantly different from
one another (p < 0.01) (Experiments 8, 9, 11).
These data clearly demonstrate that for a
given amount of molar bite force, there is
usually more bone strain on the contralateral
(b) Bone strain direction
The direction of the strains in the transducer biting experiments exhibit certain similarities encountered in previous experiments.
For example, the gages in Experiments 8 and 9
both sensed compressive subcondylar bone
strain during transducer biting, as they did
452
WILLIAM L. HYLANDER
during apple mastication (tables 2,5). In addition, the direction of t 2deep to the superficial
masseter muscle during transducer biting is
similar to its direction during both apple mastication and isometric biting on the dowel (ExIn one experiment,
periment 7) (tables 1,2,4).
however, the direction of E during transducer
biting was unlike anything previously encountered for the analysis of bone strain in the
subcondylar region (Experiment 11).Whereas
c 2 in all previous subcondylar experiments is
directed upwards and backwards (except for
strain reversals in Experiment 13 during
isometric dowel-biting along the M3), the direction of t 2 i n Experiment l l during
transducer biting is upwards and forwards
(fig. 15). In contrast, the direction of c 2 in Experiment 11 during isometric biting on the
dowel is quite different (compare fig. 13 with
fig. 15); the comparison between the mean
values of the direction of t 2 on the contralatera1 side for transducer biting and isometric
dowel biting reveals a difference of 33" ( <
0.001).
Similar to isometric dowel biting along the
MB,strain reversals were encountered whenever the transducer was bitten along the M 3
(Experiment 11).The two strain patterns are
presented separately in table 4 and figure 15.
Unlike Experiment 13, however, the direction
of c 2during the strain reversal in Experiment
11 is upwards and backwards, rather than
upwards and forwards.
5. A comparison of expected and recorded
patterns of strain during transducer
biting
One of the isometric transducer-biting experiments is somewhat a t variance with other
transducer-biting experiments and with the
previously presented mastication and isometric biting data. That is, in Experiments 8
and 9 the long axis of each single-element
gage is aligned upwards and backwards (fig.
12) and both of these gages sensed compressive bone strain during transducer biting.
These data support the hypothesis that the
mandibular condyle is loaded by a compressive
reaction force and furthermore are very similar to the mastication data. In one experiment, however, the direction of t 2 during
transducer biting is upwards and forwards,
rather than upwards and backwards as it was
during isometric dowel biting (Experiment
11). The directional data in the transducerbiting experiment support the existence of one
TMJ REACTION FORCE
453
TABLE 5
Descriptiue statistics and regression analysis ofsubcondylar bone strain duringtransducer
biting (single-elementgage analysis)
Bite values (kg)
Experiment
Compressive strain
N
Mean
Largest
S.D.
Mean
Largest
S.D.
Slope
175
233
15
11.6
8.0
2.9
34.4
26.4
4.8
8.8
6.0
1.5
-145
-249
-118
-320
-980
-238
65
233
76
- 1.5 -0.20
-34.8
-36.4
99
160
10.8
12.0
32.5
31.0
8.0
9.1
-
63
-161
-114
-474
26
143
-15.0
r
M. fascicularis (2)
Experiment 8
Ipsilateral
Contralateral
Incisor
M fascicularis (2)
Experiment 9
Ipsilateral
Contralateral
-
-0.90
-0.69
1.7 -0.53
-0.96
Note: Bone strain values are in microstrain units. N = number of bites un the transducer; r = Pearson's product-moment correlation coefficient; all values of r are significantly different from zero (p < 0.05).The bite point is unilateral along the M1-MZ repion.
of two possible situations. In some subjects variability may be partly related to object size
during transducer biting either there is (1)no since the height of the transducer block is 10
TMJ reaction force on either ipsilateral or mm while the dowel is only 2-5 mm thick
contralateral sides or (2) the mandibular con- (depending on how much the animal crushed
dyle is loaded along its medial aspect, rather the dowel during biting). Perhaps the wider
than along its middle or lateral aspect, result- gape during transducer biting which is correing in compressive bending stress and strain lated with greater rotation and translation of
along the medial aspect of the subcondylar re- the mandibular condyle somehow resulted in
gion and tensile stress and strain along the altered TMJ loading patterns.
lateral aspect (fig. 7). The regression analysis
Recorded bone strain patterns deep t o the
of bite force and bone strain magnitudes tends superficial masseter muscle during transto support the hypothesis that a TMJ reaction ducer biting are quite similar to expected patforce is present in Experiment 11. For exam- terns (compare fig. 5 with fig. 15) (Experiple, there is much more subcondylar bone ment 7). The regression analysis of bite force
strain (per unit bite force) along the contra- and bone strain values in this experiment suglateral side than along the ipsilateral side dur- gest that peak magnitude of the ipsilateral
ing molar biting. This is similar to the data for and contralateral muscle force of the masseter
mastication and isometric dowel biting. In and medial pterygoid muscles are not signifiaddition, there is more subcondylar bone cantly different from one another during
strain on the ipsilateral side during premolar isometric transducer biting.
biting than during molar biting. These findMorphological and experimental evidence
ings correlate with what would be expected if
for differential TMJloading
reaction forces are both present and vary with
bite point position (fig. 14).
Many workers have noted that although the
Similar to isometric biting of the dowel, a TMJ differs from a typical synovial joint, its
subcondylar bone strain reversal was encoun- articular surfaces are nonetheless well
tered along the ipsilateral side when the sub- adapted to bear stress (see Hylander, '75, for a
jects were allowed to bite a transducer along review). In most primates, the presumed
their M,. There is no apparent explanation as stress-bearing articular surfaces of the joint
to why the direction of t 2is upwards and back- are confined primarily t o the articular emiwards at this time. Unfortunately, there is nence of the temporal bone and the mandibuonly one experiment on the direction of E~ lar condyle. There is evidence that the reacalong the subcondylar region during trans- tion forces within the stress-bearing region of
ducer biting. Until more data are collected, the primate TMJ during the power stroke of
the only conclusion to be drawn is that among mastication and incision are not always equalsome subjects the direction of e 2during trans- ly distributed. This evidence comes from exducer biting varies from its direction during perimental studies of jaw movement and manmastication and isometric dowel biting. This dibular bone strain in primates, patterns of re-
454
WILLIAM L. HYLANDER
modeling in the human TMJ, and pathological
changes in the human TMJ.
I t has been demonstrated cinefluorographically that during the power stroke of
mastication the mandibular corpus of galagos
rotates about its long axis (Hiiemae and Kay,
'73). This rotation or twisting which is mediated by an unfused mandibular symphysis,
causes the lower border of the galago mandible to evert and the alveolar and coronoid
processes to invert. Since the galago mandibular condyle maintains contact with the temporal bone during the power stroke of mastication (via the interposed articular disc), the
lateral surface of the galago condyle must
press against the intervening disc and temporal bone, while the medial surface of the
mandibular condyle, disc, and temporal bone
are slightly separated. Presumably then,
among galagos (and all other mammals whose
dentaries rotate as described above) only the
lateral aspect of the TMJ is loaded during certain portions of the masticatory cycle.
The mandible of macaques and other anthropoids does not rotate visibly during the
power stroke because the mandibular symphysis is fused; therefore, the medial aspect of the
mandibular condyle does not necessarily lose
contact with the articular eminence and intervening disc during the power stroke. Nevertheless, because of the similar organization
of the galago and macaque masticatory apparatus, differential loading within the TMJ
probably also takes place among macaques. A
stress analysis of the mandible supports this
assumption by demonstrating that the mandibular corpus of macaques is twisted about
its long axis during the power stroke of mastication (as among galagos) (Hylander, '79a). If
the macaque TMJ is loaded by a compressive
reaction force during the power stroke (as the
data in this study suggest), and if the macaque mandible is simultaneously twisted (as
the data presented by Hylander, '79a indicate), then the macaque TMJ should also be
loaded differentially so long as the twisting
moment associated with the bite force does
not completely counter the twisting moment
associated with the ipsilateral resultant muscle force. Moreover, differential joint loading
will be more pronounced within the ipsilateral
TMJ among both galagos and macaques, since
twisting is much more pronounced on the ipsilateral side than on the contralateral side
(Hylander, '79a). Therefore, specific portions
of the ipsilateral TMJ are perhaps stressed
more (i.e., transmit more force per unit area)
than the contralateral joint, although the
data in this study suggest that among macaques the largest overall net reaction forces
ordinarily will exist on the contralateral side.
This latter finding is in contrast t o experimental evidence which suggests that in galagos
the ipsilateral TMJ is loaded with a larger net
reaction force than is the contralateral TMJ
during isometric molar biting (Hylander,
'79b).
Patterns of TMJ remodelling also suggest
differential loading within the joint. For
example, Moffett et al. ('64) have shown that
the lateral aspect of the adult human TMJ remodels differently from the medial aspect,
and although these remodelling patterns do
not directly indicate the nature of the loading
pattern, they do suggest differences in mechanical loading patterns within the TMJ.
In a recent study of the human TMJ (Oberg
et al., '71) a number of cases were found with
degenerative TMJ changes, most of which
were associated with the lateral aspect of the
joint. For example, in 13 of 14 individuals with
perforations of the articular disc, the perforations were restricted t o the lateral aspect of
the joint. (In the fourteenth case, the perforation was restricted t o the middle aspect.) Kopp
et al. ('76) also noted degenerative changes
along the lateral aspect of the human TMJ.
Since pathologic changes in joints are often
related t o local mechanical factors (i.e., excessive or highly repetitive stresses), these
data suggest that the lateral aspect of the
human TMJ experiences more stress, and
therefore more "wear-and-tear,'' than the medial aspect.
CONCLUSIONS
In vivo bone strain data from the subcondylar region of macaques suggest the following:
The macaque TMJ is loaded by a compressive
reaction force during the power stroke of mastication and incision, and during isometric
molar and incisor biting. TMJ reaction forces
are larger on the contralateral side during
both mastication and isometric molar biting.
Patterns of ipsilateral TMJ reaction force in
macaques during isometric biting vary
markedly in response to the position of the
bite point. During biting along the premolars
or first two molars a compressive reaction
force acts about the ipsilateral TMJ; however,
when the bite point is positioned along the M3,
the ipsilateral TMJ has either very little com-
TMJ REACTION FORCE
pressive stress, no stress, or it is loaded in
tension.
ACKNOWLEDGMENTS
I am grateful to Dr. R. Bays, for without his
surgical expertise this study would not have
been possible. I would also like to thank
Marianne Bouvier, Matt Cartmill, Karen
Hiiemae, Richard F. Kay, George Lauder, and
Jack Stern for reading and commenting on
various drafts of this manuscripts, and helping to prepare the figures. Finally, I am grateful to Dr. Otto Hagen, Department of Surgery,
Duke University, for allowing me to use his
experimental animals (NIH grant HL-15448).
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