Ontogeny of bone strain: the zygomatic arch in pigs
Department of Orthodontics, University of Washington, Seattle, WA 98195, USA
* Author for correspondence (e-mail: herring{at}u.washington.edu)
Accepted 4 October 2005
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Summary |
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Key words: bone strain, skull, mastication, weaning, pig
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Introduction |
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One explanation for ontogenetic shape changes in bone is that the young
skeleton is less mineralized than the mature skeleton and that infant bones
compensate by being geometrically more robust. Especially in limb bones, this
idea is buttressed by the common ontogenetic pattern among mammals and birds
of an initially stout bone becoming relatively more slender
(Carrier, 1983;
Carrier and Leon, 1990
;
Main and Biewener, 2004
). The
result of this process would be to preserve relatively constant strain
magnitudes at any given location, which has, in fact, been reported in growing
chicks and rats (Biewener et al.,
1986
; Keller and Spengler,
1989
). Like long bones, the cranium typically becomes more
elongated and less round during ontogeny. Morphological analyses have
suggested that these changes could maintain relatively constant strain
environments at given sites (Biknevicius
and Leigh, 1997
; Vinyard and
Ravosa, 1998
; Thompson et al.,
2003
).
An additional consideration is that even though infant muscles are
comparatively small and forceful behaviors are relatively rare, their motor
behavior is sometimes clumsy (Herring,
1985). Thus, variable, unpredictable and potentially large bone
strains could be encountered. The fact that infant limb bones are typically
straighter and rounder than adult bones
(Biewener and Bertram, 1994
;
Main and Biewener, 2004
;
Skedros et al., 2004
) also
suggests a less predictable loading environment
(Bertram and Biewener, 1988
).
Higher variability in strain of younger animal limb bones has, in fact, been
documented (Main and Biewener,
2004
). Although the magnitude of these strains would be moderated
by the increased robustness of infant bones
(Heinrich et al., 1999
), the
strain pattern should be more variable than in older animals, as suggested by
two studies on the cranium, one on anesthetized monkeys
(Iwasaki, 1989
) and one on
ex vivo pig heads (Fisher et al.,
1976
). Interestingly, the latter study applied loads to
different-aged skulls in a highly uniform manner intended to mimic masticatory
muscle contraction; thus, the variability of strain in the infant skulls did
not result from awkward movement but from the skulls themselves. Such a
finding (if real) implies that the young skulls were not yet adapted to the
simulated masticatory loads placed on them and that the older skulls reflected
growth changes that specifically adapted them for function.
The mammalian skull provides an opportunity to examine the influence of
function on ontogenetic changes in bone strain, because the feeding mechanism
of infants (suckling) is very different from that of adults (chewing). At the
feeding transition, there must be a radical change in both the magnitude and
pattern of loading. If skull shape during infancy is adapted for suckling,
then it is unlikely to be optimized for chewing. These considerations led us
to focus on the mammalian head at the time of weaning. In particular, we
examined the zygomatic arch, an element that is closely associated with the
masseter muscle both phylogenetically and mechanically. The masseter is the
predominant jaw-closing muscle of ungulate mammals
(Turnbull, 1970), including
our study species, the pig Sus scrofa (L.). The masseter has a strong
aponeurotic origin from the zygomatic bone
(Fig. 1) but affects the
squamosal only indirectly (Rafferty et
al., 2000
; Herring et al.,
2001
). Compared to its activity during suckling, the contractions
of the piglet masseter during chewing are longer in duration and asymmetrical
(Herring and Wineski, 1986
).
Strong electromyographic (EMG) activity can be produced in either feeding mode
(Herring and Wineski, 1986
;
Huang et al., 1994
).
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In part because its superficial location makes it accessible, a rich
database for strain in the zygomatic arch is available for the pig
(Herring and Mucci, 1991;
Herring et al., 1996
;
Rafferty et al., 2000
) and
other species (Iwasaki, 1989
;
Hylander and Johnson, 1997
).
The prior pig data were derived from subadult animals, i.e. animals that were
still growing but relatively mature in muscle anatomy and in the performance
of mastication (Herring and Wineski,
1986
). The orientation of masticatory strains in the arch was
mimicked by stimulating the ipsilateral masseter muscle in anesthetized
animals (Herring et al.,
1996
). The squamosal bone typically experienced greater strain
magnitudes (shear strain averaging 974 µ
for masseter stimulation and
411 µ
for mastication) than the zygomatic bone (473 µ
for
stimulation and 298 µ
for mastication). Principal strains on the two
bones were approximately orthogonal to each other, with zygomatic tension
being oriented anterodorsal to posteroventral (the direction of masseteric
pull) and squamosal tension anteroventral to posterodorsal. Furthermore, the
lateral zygomatic surface showed a pattern of dorsal compression and ventral
tension, indicating bending in the parasagittal plane with the lower border
becoming more convex (Herring et al.,
1996
). By contrast, the major bending plane of the squamosal was
horizontal (medial-lateral), with the lateral surface tensed (becoming more
convex) and the medial surface compressed
(Rafferty et al., 2000
).
In the present study, we investigated whether this masseter-dominated pattern of strain would be apparent in piglets that had not yet been fully weaned to a hard-food diet. We hypothesized (1) that the magnitude of bone strain on infant arches would not differ from that of older pigs and (2) that strain on infant arches would vary more than that in older skulls, especially in orientation but possibly in magnitude as well. The first hypothesis implies that bones in infant animals are pre-adapted for their functional environment, but only in a general sense, so that they would be strong enough not to break under a variety of loading possibilities. The second hypothesis implies that the bones become more adapted to their specific functions by a process of differential growth.
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Materials and methods |
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The procedures followed were identical to those used on older juvenile pigs
(Herring et al., 1996). After
halothane/nitrous oxide anesthesia, the skin and periosteum overlying the left
zygomatic arch were incised and reflected to expose the lateral surface of the
zygomatic and squamosal bones. The center of each bone surface was cauterized,
sanded, degreased and dried. Either a three-element stacked rosette strain
gage (SA-06-030WR-120; Measurements Group, Raleigh, NC, USA) or a strip gage
with two or three parallel elements (SA or EA-06-031ME-120) was affixed to
each prepared surface (Fig. 2A;
Table 1) using cyanoacrylate
glue. Rosette gages give the orientation and magnitude of the principal
strains (tension and compression) at a single location. Strip gages do not
give such information but do indicate bending in the parasagittal plane. Strip
gages were roughly parallel to the occlusal plane and the middle elements of
rosette gages were perpendicular to the occlusal plane
(Fig. 2A). Lead wires were
connected to strain conditioner/amplifiers (2120A; Measurements Group) and the
periosteum and skin were separately sutured. EMG electrodes were inserted as
previously described (Huang et al.,
1994
). An analgesic (buprenorphine; 0.02 mg kg1
i.m.) was administered and the animals were allowed to recover from anesthesia
(520 min). Strain gage data were recorded during drinking of powdered
milk formula and mastication of commercial pig chow either softened with milk
(soft) or unsoftened (hard). Signals were recorded on magnetic tape (HP
recorder with FM modules, DC-1250 Hz) for off-line analysis.
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To determine which, if any, aspects of masticatory strain could be ascribed to masseter muscle contraction, the animals were re-anesthetized and placed prone with the teeth in occlusion. Needle electrodes were placed bilaterally in the posterodorsal and anteroventral aspects of each masseter muscle. Tetani were produced using 450 ms trains of 3 ms pulses delivered at 60 pulses s1 (Grass Model S48 and SIU; East Warwick, RI, USA). Stimulation voltage was administered to provide a supramaximal contraction of the masseter and zygomaticomandibularis (deep masseter) muscles without spread to adjacent muscles. Typically, 6070 V was used for bilateral stimulation and 3040 V was used for unilateral stimulation. Strain signals were displayed on a calibrated storage oscilloscope and photographed. At the termination of these procedures, animals were euthanized using intracardiac injections of sodium pentobarbital. After sacrifice, gages were inspected to verify their condition and to document their position.
Bone strains during mastication were digitized and analyzed using AcqKnowlege (Biopac Systems, Goleta, CA, USA) software. Rosette data were used to calculate the peak principal strains for each feeding cycle. The angle of the maximum principal strain (tension) was expressed relative to the occlusal plane (0°=180°) with positive values measured clockwise from the left and negative values measured counterclockwise from the left (Fig. 1B). Highly variable individual differences in angle presented a problem for analysis. We decided to express values as either positive (e.g. 107°) or negative (e.g. 73°) in order to minimize variation of the sample as a whole. Strip gage data were scored qualitatively by comparing the peak values of each element in the array. Higher compression in the dorsal element than in the ventral element indicates bending such that the dorsal surface of the bone becomes more concave. Conversely, if strain in the dorsal element is more tensile than that in the ventral element, the bone is bent such that its dorsal surface becomes more convex. Strains from stimulations were measured directly from the scaled photographs. Data were organized using Excel spreadsheets, and principal strains were calculated following the formulae provided by Rosette-Plus (Measurements Group).
For morphometric comparisons, 45 skulls of Hanford pigs of known age
(Fig. 2AC), including
five from the present sample and three from the previous study of juveniles
(Herring et al., 1996), were
measured using digital calipers (±0.01 mm). Condylobasal length was
used as an index of skull size. In addition to antero-posterior lengths of
arch components, medio-lateral thicknesses and dorso-ventral heights of the
zygomatic and squamosal bones were measured at the level of the strain gages
(Fig. 2D,E). As a rough measure
of curvature in the parasagittal plane, the deviation of the most ventral
point from a straightedge placed along each bone's long axis was measured and
expressed as a percentage of antero-posterior length
(Fig. 2F). Measurements on 11
of the skulls were repeated two weeks later to test for measurement error,
calculated as
where d is
the difference between the first and the second measurement and N is
the number of subjects. Paired t-tests indicated no systematic error,
and measurement error ranged from 0.15 to 0.65 mm (mean, 0.32±0.13 mm).
Proportions (thickness and height relative to length, curvature) were
calculated and transformed with the arcsin function in order to spread out the
distribution (Snedecor and Cochran,
1967
). Reduced major axis regressions against condylobasal length
were performed using RMA 1.17 software
(http://www.bio.sdsu.edu/pub/andy/RMA.html)
to assess whether the arch becomes less robust with age and to explore its
changes in shape. The software calculated confidence intervals by
bootstrapping over cases (20 000 replicates) using random sampling with
replacement. Parameters were considered to differ significantly if 95%
confidence intervals did not overlap.
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Results |
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During drinking, and to a lesser extent feeding on soft chow, low strains were observed in the strip gages, with no clear evidence of bending in the parasagittal plane. However, when piglets were masticating hard chow, the strip gages showed obvious bending in most bones (Table 3). Patterns of bending were surprisingly variable among pigs, and some animals also showed different patterns for ipsilateral and contralateral chewing. For the squamosal bone, most piglets showed the same pattern regardless of chewing side but, of these, two evinced concave-downward bending, one showed concave-upward bending and one showed no bending with all areas under tension. One animal showed concave-downward bending for ipsilateral cycles but concave-upward bending for contralateral cycles. For the zygomatic bone, three animals showed concave-downward bending (with one changing to no bending with compression for contralateral chewing), while the fourth always had concave-upward bending.
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Masseter stimulation
Rosette strain gage data for muscle stimulations are presented in
Table 4 and illustrated in
Fig. 4A. Intra-individual
variation was negligible for stimulated tetanus, thus standard deviations are
presented only for the sample as a whole. When the ipsilateral masseter (with
or without the contralateral masseter) was contracting, the magnitudes of the
principal strains were strikingly larger than for mastication
(Table 2), typically 3-fold
higher (all comparisons between bilateral stimulation and ipsilateral
mastication statistically significant at P<0.010.05). Even
stimulations of the opposite-side masseter resulted in strains that were
usually higher (although not significantly different) than during mastication.
Orientations of the mean principal strains were rotated somewhat clockwise
relative to those of mastication (as seen from the left, compare Figs
3A and
4A) but were not statistically
different from those of mastication.
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Morphometrics
Before examining shape changes within bones, the dimensions were compared
with skull (condylobasal) length to assess overall allometry. The lengths of
the individual bones increased approximately isometrically with skull length
for both the squamosal [slope=0.15 (0.98 for logged data),
r2=0.96] and zygomatic [slope=0.14 (0.84 for logged data),
r2=0.97]. Zygomatic height was almost isometric with skull
length (slope=0.12, r2=0.93), but squamosal height showed
a significantly lower slope (0.07, r2=0.86). Thickness was
also negatively allometric, more so for the squamosal (slope=0.001,
r2=0.18) than for the zygomatic bone (slope=0.003,
r2=0.67). Thus, bone length and zygomatic height keep pace
with skull length, while bone thickness and squamosal height do not.
Bone shape was assessed by plotting height and thickness relative to bone
length against total skull length. Greater relative height and thickness were
considered to indicate the robustness of the arch bones. In both bones,
relative height was found to increase with increasing skull length, but much
more dramatically for the zygomatic than for the squamosal bone
(Fig. 5A;
Table 6). Zygomatic height was
approximately 40% of zygomatic length in the smallest animals, increasing to
80% in the largest, whereas squamosal height increased from approximately 25%
to approximately 40% of squamosal length. The difference in reduced major axis
slope between the bones was statistically significant at P<0.01.
By contrast, relative bone thickness slightly decreased in the squamosal
(Fig. 5B) from 25% to
15% of bone length. This decrease can be ascribed in part to the medial
shelf of the squamosal bone's articular eminence, which often extended to the
strain gage location in the smaller but not the larger skulls
(Fig. 2D). In the zygomatic
bone, relative thickness remained roughly constant at approximately 30% of
bone length. Despite the fact that the squamosal bone showed a significantly
negative slope and the zygomatic bone did not, the slopes of the two bones did
not differ at the 0.05 level. In summary, the smallest pigs had zygomatic
arches with the roundest cross sections and the largest pigs had arches
elongated vertically. With growth, the arch became more `robust' in the
parasagittal plane but not in the horizontal plane. These changes were more
marked in the zygomatic than in the squamosal bone.
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Reduced major axis analysis of relative curvature in the parasagittal plane (Fig. 2F), with or without arcsin transformation of the proportional data, indicated that the zygomatic bone was more curved than the squamosal bone, which actually had an intercept near zero (i.e. no curvature). However, both bones became significantly more curved with age, with no difference in slope (Fig. 5C; Table 6).
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Discussion |
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The differences between foods of varying hardness paled in comparison to
the variability within each food. Inaccurate reporting could have accounted
for some of the variabilitywe considered cycles to be `drinking' if the
animal had its snout in the bowl of liquid, but occasionally a bolus of chow
could have been in the mouth at the time. For the most part, however, the
variability appears to reflect real differences in the performance of feeding.
Inter-individual variability was most obvious in the parasagittal bending
direction as deduced from the strip gages
(Table 3) and was much greater
than in juvenile pigs (Herring et al.,
1996). Inter-individual variation was also substantial for rosette
data, but in this case older animals were variable too. F-tests
comparing the variances from the present study with those of the juveniles
were not significant for strain magnitude, but squamosal strain orientation
was more variable in the piglets (P<0.001) and zygomatic strain
orientation tended in the same direction (P=0.10). The rosette data
also showed remarkably high intra-individual variability in piglets. When
individuals were analyzed separately, piglets were far less consistent in
their performance than older animals, with individual coefficients of
variation in the 4060% range for strain magnitude in five out of the
eight piglets (calculated from Table
2), in contrast to 2030% for individual older animals
(Herring et al., 1996
). These
same five piglets had standard deviations of 2064° for orientation,
in contrast to less than 15° for older animals
(Herring et al., 1996
) and the
remaining three piglets. The variability within individuals was equally high
for all foodstuffs.
High inter- and intra-individual variability suggests that none of these
feeding behaviors was fully hardwired and that the young animals had not yet
learned a stereotyped motor program. In particular, piglets were not adept at
dealing with the hard food. Our previous analysis of mastication in these
infant animals (Huang et al.,
1994) revealed that, compared with older animals, they chewed more
slowly with longer and more variable bursts of closing muscle activity, used a
larger number of cycles to process a bolus, were less regular in alternation
of side and had more equal working to balancing side muscle activity. Because
the piglets had just one pair of occluding molars, bolus position and hence
loading might have been unpredictable, producing an unstable masticatory
stroke. More variable and inefficient feeding behavior in younger individuals
has also been described in other mammalian species
(Binder and Van Valkenburgh,
2000
).
Whatever the cause, these data indicate that, like young limb bones
(Main and Biewener, 2004), the
skulls of infant animals show variable, even erratic strains. Thus, they do
not appear adapted to the functional loads produced by mastication.
Strain magnitude and pattern in comparison with older animals
Tables 7 and
8 compare rosette data from the
piglets with those of the previous study on juveniles in which the gages were
in equivalent locations (Herring et al.,
1996). Data from other locations in juveniles
(Liu and Herring, 2000
;
Rafferty et al., 2000
)
indicate that there are (opposite) anteriorposterior gradients of
strain magnitude in both arch bones; this restricts statistical comparison to
the 1996 study. During mastication, piglets and juveniles had similar strain
magnitudes (Table 7;
Fig. 3B). This similarity
actually suggests that the arch is less stiff in the piglets, because although
EMG levels are comparable (Huang et al.,
1994
), the piglet masseter muscles are relatively smaller and less
forceful than those of juveniles (Herring
and Wineski, 1986
; Anapol and
Herring, 1989
). Low stiffness of the piglet arch under masseteric
contraction is even more clearly implied by the results of muscle stimulation.
During same-side masseter tetanus, piglets evinced vastly higher strains than
juveniles (Table 8;
Fig. 4). As far as we can
determine, these strains, ranging up to 4000 µ
shear strain (maximum
minus minimum principal strain), are the highest ever recorded from the
mammalian skull and rival those recently reported for biting alligators
(Metzger et al., 2005
).
Assuming that ultimate compressive strain for the zygomatic arch is in the
order of 2% (Skedros et al.,
2003
), the safety factor for full recruitment of the masseter
would be less than 10. Even stimulation of the opposite-side masseter produced
strains in the same order of magnitude as did chewing (except for #145;
Table 4). By contrast, in the
juvenile arch, masseter tetanus seldom produced strains more than twofold the
magnitude of masticatory strain, and stimulation of the opposite masseter
produced only negligible strain (Table
8). These findings indicate that the only reason that masticatory
bone strain magnitudes are similar in piglets and in juveniles is that the
piglets recruit proportionately much less muscle force. This agrees with the
ex vivo simulation experiments of Fisher et al.
(1976
) showing that equivalent
muscle contraction resulted in higher strains in younger skulls.
Beyond magnitude, there are three major differences of strain pattern
between piglets and juveniles (Figs
3B,
4). First, in piglets, tensile
and compressive strains were roughly coequal on both bones, but in older
animals the squamosal showed little or no compression on its lateral surface
(Herring et al., 1996;
Liu and Herring, 2000
;
Rafferty et al., 2000
).
Therefore, the bending in the horizontal plane that characterizes the older
squamosal does not occur in piglets. Instead, the infant squamosal is either
twisted such that its anterior ventral border moves medially, or sheared such
that its anterior extremity is forced ventrally
(Fig. 6). Both of these loads
could arise from the ventral and medial pull of the masseter on the zygomatic,
transferred to the squamosal at the suture
(Herring et al., 1996
;
Hylander and Johnson, 1997
;
Rafferty et al., 2000
), but
this does not explain why bending in the horizontal plane did not occur in the
piglets. This problem is addressed further below. Interestingly, the infant
strain pattern is the same as that reported for the posterior arch (i.e.
squamosal bone) of Macaca
(Iwasaki, 1989
;
Hylander and Johnson, 1997
);
thus, in this regard piglets more closely resemble higher primates than they
do older pigs.
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The third difference in strain pattern between infant and juvenile pigs is
that in the infants, neither the squamosal nor the zygomatic bone showed
consistent bending in the parasagittal plane during feeding. Masseter
stimulation, however, usually bent the squamosal concave downward and the
zygomatic concave upward, the same patterns seen in juveniles during both
feeding and stimulation. Thus, the muscle does cause parasagittal bending, but
the strong contractions required are not produced under normal functional
conditions. As argued for older pigs
(Herring et al., 1996), the
concave-upward zygomatic bending is most likely a result of the masseter's
ventral pull on the zygomatic bone, which is supported at its anterior and
posterior ends by sutures with the maxillary and squamosal bones, basically a
three-point bending load. The concave-downward bending of the squamosal is
explained by the existence of only two important loads, the ventrad force of
the zygomatic bone anteriorly and the dorsad joint force posteriorly
(Herring et al., 1996
).
All of these findings strongly suggest that, unlike juveniles, feeding
strains on the zygomatic arch of weanling pigs are not dominated by the
masseter muscle. Previous work indicates that the temporalis is relatively
more important and the masseter less important in very young than in older
animals (Herring, 1977). Less
forceful chewing, alternate muscle use and a larger role for the more
proximate occlusion all probably contributed to the patterns observed as well
as their variability.
Although it is agreed that different skeletal sites are under unique strain
regimes (Biewener et al., 1986;
Hylander and Johnson, 1997
),
the long bone literature suggests that, for a given site, both the pattern and
the magnitude of strain are maintained at a relatively constant level by bone
modeling (Biewener et al.,
1986
; Keller and Spengler,
1989
; Biewener and Bertram,
1993
). Similarly, measurements of the mandibular symphysis of
Macaca indicated that postnatal growth could maintain functional
equivalence in bone strain (Vinyard and
Ravosa, 1998
). By contrast, our findings in piglets clearly show
that the pattern of strain was not constant but changed with growth.
Specifically, squamosal compression was elevated and zygomatic strain was
differently oriented in infants as compared with juveniles. The difference in
strain pattern was not due to the changeover from liquid to solid food,
because the strain patterns were identical for all foods offered. These data
indicate that functional equivalence in the pig zygomatic arch does not extend
to strain pattern.
Ontogenetic shape changes in the zygomatic arch
The exceptionally high strains that were produced by stimulation of
relatively small (Herring and Wineski,
1986) muscles suggest that, like infant long bones
(Carrier and Leon, 1990
;
Heinrich et al., 1999
;
Skedros et al., 2004
), piglet
arches have low stiffness. Indeed, the entire piglet skull is probably
relatively compliant, as indicated by the substantial strains produced on the
arch by a distant load, the contralateral masseter. Unlike long bones, however
(Main and Biewener, 2004
),
infant zygomatic arches were not more robust overall than those of older
animals. Although there was a slight age decrease in relative transverse
dimension, the relative vertical dimension increased strongly
(Fig. 5), making older animals
better buttressed for bending in the parasagittal plane. Thus, piglet arches
were weak in geometric as well as in material properties, at least for
dorsalventral loading. Functional strain magnitudes that were
age-invariant resulted from low muscle activity in the piglets, not bone
adaptation.
Like infant limb bones (Biewener and
Bertram, 1994; Main and
Biewener, 2004
; Skedros et
al., 2004
), piglet zygomatic arches were straighter and rounder
than those of juveniles. This geometry undoubtedly contributed to the high
intra- and inter-individual variability we observed in bone strain, because
the bending direction of a straight cylinder is more sensitive to slight
variations in loading direction than that of a curved cylinder or a beam
(Bertram and Biewener, 1988
).
At a more detailed level, the shapes of the two bones were different at the
start and changed differently during growth. At birth, the zygomatic bone was
relatively taller than the squamosal and this difference became more
accentuated with age. The piglet zygomatic bone was also slightly thicker and
more curved than the squamosal, whereas the squamosal was the rounder,
straighter bone. These differences were maintained.
In long bones and the mandible, ovate cross sections and curvatures develop
in relation to mechanical loading from muscle contraction and weight bearing
(Lanyon, 1980;
Hall and Herring, 1990
;
Biewener and Bertram, 1994
;
Skedros et al., 2004
). The
growth changes in the zygomatic bone are clearly adaptive for the
parasagittal-plane bending that predominated in older animals but was not seen
during function in the piglets. The dramatically increased height creates a
beam-like structure that would strongly resist both the ventral pull of the
masseter and the dorsal shear imposed by occlusal force. The increasing
curvature is in the same (concave-upward) direction as the parasagittal
bending, which should greatly increase the predictability of deformation.
Interestingly, these geometric changes do not predict altered strain
magnitudes on the zygomatic bone. Although deepening of the zygomatic bone
would be expected to make it stiffer and decrease strain magnitudes, its
increasing curvature should increase bending and strain magnitudes. Because
maximal (stimulation) strains decreased with age, the stiffening effect may
have been the more important one. In summary, the zygomatic bone shows some
pre-adaptation for its eventual loading regime but becomes much better adapted
to it with age, both in terms of robustness and predictability.
The squamosal bone of piglets was not bent in the horizontal plane, in contrast to older animals, even when the masseter was stimulated. This absence is surprising, given the fact that otherwise the strain pattern of the squamosal in response to the masseter was similar to that of older animals. One likely explanation is the presence of the medial shelf (Fig. 2D), which buttresses the squamosal in the medial-lateral direction. Our strain gage position for piglets was usually just opposite this shelf. During growth, the elongation of the squamosal is not accompanied by elongation of the medial shelf, and therefore the gage position in the older sample was not opposite to it. In addition, the longer expanse of unsupported squamosal bone would be more subject to cantilever bending. Thus, the diminishing presence of the medial shelf should make the older squamosal more prone than the younger to bending in the horizontal plane. Casual observations on Macaca skulls suggest that a medial shelf is present, which would explain why piglets were more similar in their squamosal strain pattern to these primates than to older pigs. The pig squamosal showed no growth adaptation that would strengthen it against bending in the horizontal plane; in fact, decreasing thickness would weaken it in this direction. However, the disappearance of the shelf from most of the medial surface would make horizontal-plane bending more predictable.
In the parasagittal plane, bending of the squamosal was inconsistent during
piglet function, but even in older pigs this mode of deformation was less
important than for the zygomatic (Herring
et al., 1996). The growth adaptations of the squamosal in the
parasagittal plane were less striking than those of the zygomatic. Both the
modest increase in height (Fig.
5A) and the increase in upward concavity (which is the reverse of
the concave-downward bending caused by the masseter) would tend to stiffen the
squamosal against parasagittal-plane bending. In short, for its major strain
regime, bending in the horizontal plane, the squamosal bone resembles limb
bones in that it is more robust in infants and more predictable in older
animals. For its minor regime of bending in the parasagittal plane, it becomes
more robust and possibly less predictable.
Testing of hypotheses
We had hypothesized that strain levels in weanling pigs would be roughly
comparable to those in older animals because of compensating factors. In
particular, we expected the newly increased muscle loads and the poorly
mineralized tissue to be countered by more robust geometry of the bones. The
hypothesis was supported in that, during mastication, piglet strain levels
were about the same as those of juveniles. However, the reasons for this were
not as anticipated. When the muscles were supramaximally stimulated, the
piglet strain levels were very much higher than those of the juveniles.
Therefore, the similar masticatory strain levels were not primarily due to the
robust geometry of the bones but to the fact that the piglets do not recruit
muscles as fully as do juveniles during feeding. Indeed, we found that the
piglet zygomatic arches were less geometrically robust than those of older
animals, at least for bending in the parasagittal plane.
We also hypothesized that piglet strain patterns would be more variable than those of juveniles, in part because of a less adaptive bone geometry that would result in unpredictable deformation. This hypothesis was strongly supported. Intra-individual variation during piglet feeding was especially high, and the bones of the arch were straighter and rounder in younger pigs. Changes in geometry, in particular the increasing curvature of the bones in the parasagittal plane and their relative increase in height but not thickness, would all contribute to greater predictability of bone deformation in older pigs. However, bone geometry was not the only cause of strain variability in the infants. Other important contributing factors included less stereotyped chewing behavior with less reliance on the masseter muscle and greater proximity of the occluding molars to the zygomatic bone compared with older animals.
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Acknowledgments |
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Footnotes |
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Present address: 1 West Ashland Avenue, Glenolden, PA 19036, USA
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References |
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