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Dietary consistency and plasticity of masseter fiber architecture in postweaning rabbits.

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THE ANATOMICAL RECORD PART A 288A:1105–1111 (2006)
Dietary Consistency and Plasticity
of Masseter Fiber Architecture
in Postweaning Rabbits
ANDREA B. TAYLOR,1,2* KELLY E. JONES,1 RAVINDER KUNWAR,3
3
AND MATTHEW J. RAVOSA
1
Doctor of Physical Therapy Division, Department of Community and Family Medicine,
Duke University School of Medicine, Durham, North Carolina
2
Department of Biological Anthropology and Anatomy,
Duke University, Durham, North Carolina
3
Department of Cell and Molecular Biology, Northwestern University,
Feinberg School of Medicine, Chicago, Illinois
ABSTRACT
Dietary consistency has been shown to influence cross-sectional area
and fiber type composition of the masticatory muscles. However, little is
known about the effects of dietary consistency on masticatory muscle
fiber architecture. In this study, we explore the effects of dietary consistency on the internal architecture of rabbit masseter muscle. Because activity patterns of the rabbit chewing muscles show inter- and intramuscular heterogeneity, we evaluate if alterations in fiber architecture are homogeneous across various portions of the superficial masseter muscle. We
compared masseter muscle fiber architecture between two groups of
weanling rabbits raised on different diets for 105 days. One group was
raised on a diet of ground rabbit pellets to model underuse of the masticatory complex, while the other group was fed a diet of intact pellets and
hay blocks to model an overuse diet. In all portions of the superficial
masseter, physiological cross-sectional areas (PCSAs) are greater in
the overuse compared to underuse diet rabbits. Thus, the mechanical
demands for larger muscle and bite forces associated with early and prolonged exposure to a tough diet are met by an increase in PCSA of the superficial masseter. The larger PCSA is due entirely to increased muscle
mass, as the two rabbit groups show no differences in either fiber length
or angle of pinnation. Thus, increasing pinnation angle is not a necessary
biomechanical solution to improving muscle and bite force during growth.
The change in PCSA but not fiber length suggests that variation in dietary
consistency has an impact on maximum force production but not necessarily on excursion or contraction velocity. Anat Rec Part A, 288A:1105–1111,
2006. Ó 2006 Wiley-Liss, Inc.
Key words: masseter muscle; muscle fiber architecture; physiological cross-sectional area; fiber length; muscle
plasticity; diet; Oryctolagus cuniculus
*Correspondence to: Andrea B. Taylor, Doctor of Physical
Therapy Division, Department of Community and Family Medicine, Duke University School of Medicine, Duke University
Medical Center, Box 3907, Durham, NC 27710.
Fax: 919-668-3024. E-mail: andrea.taylor@duke.edu
Ó 2006 WILEY-LISS, INC.
Received 23 March 2006; Accepted 21 July 2006
DOI 10.1002/ar.a.20382
Published online 1 September 2006 in Wiley InterScience (www.
interscience.wiley.com).
1106
TAYLOR ET AL.
Food consistency has been shown to exert an influence
on the bony masticatory apparatus and associated musculature, including bone strain levels (Hylander, 1979),
cortical bone and cartilage proportions and properties
(Beecher and Corruccini, 1981; Bouvier and Hylander,
1981, 1982, 1984, 1996a, 1996b; Beecher et al., 1983;
Ravosa et al., 2006a, in press), and activity levels of the
jaw-closing muscles (Weijs and Dantuma, 1981; Langenbach and van Eijden, 2001). Some studies have further
shown that dietary-induced alterations in muscle activity are associated with changes in fiber size and composition, particularly during ontogeny (Kiliaridis et al.,
1988; Chang et al., 1995; Saito et al., 2004). Others have
demonstrated alterations in fiber type cross-sectional
area, but with no attendant changes in fiber composition
(e.g., Langenbach et al., 2003). Although dietary consistency has been shown to influence fiber type composition
of the masticatory muscles (e.g., Kiliaridis et al., 1988)
and the cross-sectional area of slow-contracting fibers in
the posterior deep masseter (Langenbach et al., 2003),
little is known about the effects of dietary consistency
on jaw muscle fiber architecture.
Muscle fiber architecture is an important determinant
of the contractile properties of whole muscle (Gans and
Bock, 1965; Muhl, 1982; Sacks and Roy, 1982; Lieber
et al., 1992; van Eijden et al., 1997; Taylor and Vinyard,
2004, in press). Furthermore, it is well appreciated that
the jaw-closing muscles in humans and other mammals
exhibit inter- and intramuscular variation in mass, fiber
orientation, and internal architecture (Gaspard et al.,
1973; Herring et al., 1979; Weijs and Dantuma, 1981;
Bredman et al., 1991; van Eijden et al., 1997; Antón, 1999).
In rabbit masseter, the physiological cross-sectional area
(PCSA) of the lateral portion of the superficial masseter
is three and a half times greater than the PCSA of the
medial portion, and more than six times greater than
the anterior deep masseter muscle (Weijs and Dantuma,
1981). Likewise, activity patterns of the rabbit chewing
muscles show inter- and intramuscular heterogeneity.
For example, during the power stroke of mastication,
the two superficial portions of the balancing-side superficial masseter begin firing, and peak, prior to the deep
portion of the superficial masseter (Weijs and Dantuma,
1981). In light of this structural and functional heterogeneity, an appreciation for how muscle compartments
respond to long-term alterations in dietary consistency
is important, as such alterations ultimately impact on
how the mandible is loaded during mastication and
incision.
In this study, we explore the effects of variation in dietary consistency on the internal architecture of rabbit
masseter. In addition, we assess whether alterations in
fiber architecture occur homogeneously across various
portions of the superficial masseter muscle. In rats
(Hurov et al., 1986) and rabbits (Weijs et al., 1987), the
jaw-closing musculature increases in size during growth
relative to the jaw-opening muscles, and the superficial
masseter comprises a substantially larger percentage of
the total jaw-closing muscle weight in adults (Schumacher
and Rehmer, 1960; Turnbull, 1970; Weijs and Dantuma,
1975, 1981; Weijs et al., 1987), affirming the importance
of the superficial masseter for generating bite force [as
well as facilitating jaw opening, e.g., Taylor and Vinyard
(2004)]. Therefore, the null hypothesis is that lateral
and medial portions of the superficial masseter do not
differ in their response to dietary consistency. The alternative hypothesis is that the masseter shows regional
(intramuscular) variation in response to differences in
dietary consistency.
MATERIALS AND METHODS
Samples
Twenty genetically similar male and female New Zealand domestic white rabbits (Oryctolagus cuniculus)
were randomly separated into two equal dietary groups
of 10 each. To ensure similarity in postnatal response to
dietary modification, and thus control for variation in
genetics and phylogeny, only siblings were selected. All
rabbits were obtained as 4-week-old healthy weanlings
and kept in the AALAC-accredited Center for Comparative Medicine (CCM; Northwestern University Feinberg
School of Medicine) under an IACUC-approved protocol.
Experimental Protocol
Two dietary cohorts of 10 rabbits each were entered
into the experimental protocol at weaning (4 weeks old)
(Sorensen et al., 1968; Yardin, 1974). The twofold advantage of this early timing is that it limits the postnatal
effects of other dietary inputs into the jaw adductor muscle system, thereby improving the likelihood that any
morphological differences can be reliably ascribed to variation in food material properties; and that it optimizes
the timing of the experimental protocol to coincide with
the postweaning period of marked ontogenetic plasticity
(Bouvier, 1988; Bouvier and Hylander, 1996a, 1996b;
Ravosa et al., 2006a, in press). One group of weanlings
was raised on a diet of ground rabbit pellets previously
soaked in water (Harlan TekLad Rabbit Pellets) to model
underuse (UU) of the masticatory complex, while the second group was fed a tough diet of intact pellets supplemented daily with two 2 cm hay blocks to model overuse
(OU) (Ravosa et al., 2006a, in press). The inclusion of
pellets in the diet of all postweaning rabbits ensures
adequate nutrition for normal growth (cf. Chang et al.,
1995). Rabbits were housed in plastic cages to reduce paramasticatory behaviors such as incisor wire gnawing.
Weanlings were raised on the UU or OU diets for a
period of 105 days and sacrificed as subadults (19 weeks
old). The skull was detached en masse at the vertebral
column, which facilitated fixation of the jaw muscles
with the mandible fully adducted. In this single-blind
analysis, muscles were coded such that the investigator
conducting the muscle fiber architecture analysis (A.B.T.)
was blind to the dietary status of the rabbits (M.J.R.).
Fiber Architecture Data Collection
Following fixation (10% buffered formalin), the left
masseter muscles were carefully dissected free of their
bony attachments, trimmed of excess tendon and fascia,
blotted dry, and weighed to the nearest 0.0001 g (MettlerToledo AB204-S). The masseter muscle was sectioned
along the length of the muscle belly into superior, middle,
and inferior segments (Fig. 1a). From these segments,
three portions of the superficial masseter muscle were
identified (Fig. 1b) (Weijs and Dantuma, 1981).
Fiber length and angle of pinnation for the masseter
were measured in each portion following Taylor and Vinyard (2004). Specifically, a muscle segment was oriented
Fig. 1. Schematic of a rabbit skull in lateral view and left masseter
muscle (adapted from Russell, 1998). a: The left masseter was carefully
dissected from its attachments to the skull and trisected from superficial
to deep along anteroposterior lines of stress visible on the epimysium,
depicted by the two dotted lines. b: Superior view of the multipinnate rabbit masseter, inferior segment. Fasciculus measurements were taken from
the myotendinous junction (MTJ) to the tendon of muscle attachment
along the region of the zygomatic arch (ZTMA), from MTJ to MTJ, and
from the MTJ to the tendon of muscle attachment along the mandible
(MTMA). The stars at the anterior and posterior ends of the MTJ mark the
sampling sites for anterior and posterior fibers, respectively. The symbols
in the callout represent three portions of the superficial masseter (following Weijs and Dantuma, 1981): open circle, lateral masseter 1; triangle,
lateral masseter 2; filled circle, medial superficial masseter 3 (see Table 1).
1108
TAYLOR ET AL.
muscle mass (English et al., 1999), a one-way factorial
analysis of variance was performed to test for significant
group, sex, and interaction effects. Based on an a priori
significance level of P < 0.05, results revealed significant
group effects (P ¼ 0.002), but no significant sex or interaction effects (P > 0.05). Therefore, the sexes were combined and Student’s t-tests were used to assess whether
the OU diet and UU diet groups differ significantly in
masseter fiber architectural variables. Prior research
(e.g., Langenbach et al., 2003) leads to the expectation
that rabbits fed harder foods should demonstrate an
increase in whole masseter PCSA. Therefore, a onetailed test was performed for this analysis. However,
because there is little evidence for or against the hypothesis that fiber architecture differences should be expressed uniformly across all portions of the superficial
masseter muscle, two-tailed tests were determined to
provide the most suitable approach to assess regional
differences between groups.
Fig. 2. Schematic of a muscle segment depicting the measurements taken in this study (adapted from Anapol and Barry, 1996).
These measurements include fasciculus length (lf) and the perpendicular distance from proximal myotendinous junction to tendon of distal
muscle attachment (a). Angle of pinnation (y) was computed as the
arcsin of a/lf.
on its perpendicular to expose the individual fasciculi and
their proximal and distal attachments to tendon. Each
segment was pinned to a styrofoam block and placed
under a five-diopter magnifier lamp. Anterior and posterior sampling sites were chosen along the length of each
muscle segment corresponding to the three muscle portions. Anterior fibers were sampled consecutively by
choosing a fiber from the anteriormost portion of the myotendinous junction (MTJ) and proceeding posteriorly, and
posterior fibers were sampled in reverse fashion beginning at the posterior portion of the MTJ and proceeding
anteriorly (Fig. 1b). At each sampling site, a maximum of
12 adjacent fasciculi was measured.
Measurements taken for each fasciculus include fasciculus length, between the proximal and the distal myotendinous junctions (lf); and the perpendicular distance
from the tendon of insertion to the proximal attachment
of the fasciculus (a). The angle of pinnation (y) was calculated as the arcsin of a/lf (Fig. 2). Using the aforementioned measurements, the following architectural variables were computed for each muscle compartment, and
for the whole masseter muscle, separately by diet group.
Mean fiber length for each muscle compartment was
calculated as the average fiber length of the compartmental anterior and posterior fasciculi, respectively. Mean
fiber length for whole masseter was calculated as the
average of all fiber lengths from the superficial compartments along with fibers sampled from the deep masseter.
Physiological cross-sectional area by muscle compartment and for whole masseter was calculated as follows:
PCSA (cm2) ¼ [muscle mass (g) 3 cosy]/[lf (cm) 3 1.0564 g/
cm3], where 1.0564 g/cm3 is the specific density of muscle
(Murphy and Beardsley, 1974).
Analyses
Assumptions of normality were met based on the
Shapiro-Wilk test, justifying the use of parametric statistical analysis. Because of possible sex differences in
RESULTS
Behavioral analysis and observation of a pilot sample
fed ad lib indicate that OU diet rabbits regularly
ingested a daily supply of two hay blocks; UU diet rabbits did not exhibit failure to thrive, nor did they develop incisor malocclusions; and 90% of the UU diet
sample falls within the skull length range for 10 similar-aged OU diet rabbits. Average muscle mass is 6.75 g
6 0.79 and 5.35 g 6 0.89 for the OU diet and UU diet
rabbits, respectively. Whole muscle mass is significantly
greater in the OU diet rabbits (df ¼ 1,17; F ¼ 12.90; P ¼
0.002). On the other hand, there are no group differences in fiber length or pinnation angle (Table 1). The OU
diet rabbits demonstrate a significant difference in
whole muscle PCSA and in the PCSAs of the lateral
and medial portions of the superficial masseter (Fig. 3,
Table 1). The percentage difference in PCSA ranges
between 16.0% and 20.0%, with the greatest percentage
differences accruing to the deeper portions of the superficial masseter (superficial masseter portions 2 and 3).
DISCUSSION
Results of this study show that variation in food consistency produces alterations in the masseter muscle.
Postweaning rabbits fed whole pellets and hay blocks
showed an increase in PCSA compared to rabbits raised
on a diet of crushed pellets alone. Pellets are hard and
brittle, whereas hay is tough (Ravosa et al., in press).
Both foods require the generation of large muscle and
bite forces, but whole pellets and hay entail more repetitive loading of the jaws to process than pellets soaked
in water and pulverized. Thus, the increase in
PCSA observed in the OU diet rabbits likely derives
from the combined effect of both large and repetitive jaw
loads.
The differences in PCSA are largely a function of
increase in muscle mass, as average masseter muscle
weights differ significantly, but fiber lengths and pinnation angles do not. Findings from this study are consistent with previous work demonstrating that variation in
dietary consistency induces significant changes in relative masseter muscle mass (Kiliaridis et al., 1988; Chang
1109
DIETARY CONSISTENCY
TABLE 1. Means, standard deviations (SD), and results of statistical tests for differences in fiber
architectural variables between the overuse diet (OU) and underuse diet (UU) rabbits.a,b,c,d
OU-diet fed rabbits (n ¼ 9)
y
Lf
Lateral masseter 1 (*)
Lateral masseter 2 (~)
Medial masseter 3 (l)
Whole masseter
6.0
8.6
4.6
6.1
(0.63)
(1.4)
(1.2)
(0.81)
37.8
22.4
40.3
36.3
(5.4)
(4.4)
(10.0)
(4.2)
UU-diet fed rabbits (n ¼ 10)
PCSA
8.3
6.9
10.5
8.4
(0.53)
(0.73)
(1.0)
(0.34)
y
Lf
5.8
8.4
4.4
5.8
(0.72)
(2.2)
(0.95)
(0.70)
36.7
24.3
42.7
36.4
(4.1)
(6.5)
(12.2)
(4.4)
PCSA
7.0
5.5
8.4
7.0
(0.79)
(0.75)
(1.5)
(0.58)
Lf, fiber length (mm); y, pinnation angle (degrees); PCSA, physiological cross-sectional area (cm2).
One muscle in the OU-diet group was damaged and was therefore excluded from data analysis.
c
Lateral masseter 1 represents the superficial masseter fibers running from the myotendinous junction to the zygomatic
arch; Lateral masseter 2 represents the superficial masseter fibers running between the superficial and deep myotendinous
junctions; Medial masseter 3 represents the fibers running from the deep myotendinous junction to the mandible. Symbols
designating each portion of the superficial masseter are depicted in Figure 1b, following Weijs and Dantuma (1981).
d
Boldfaced values indicate significant differences (P 0.01) in PCSA between groups. No other differences were significant.
a
b
et al., 1995) and fiber cross-sectional area (Langenbach
et al., 2003). Average masseter fiber lengths for the subadult OU diet rabbits, though slightly smaller, are close
to values reported by previous investigators for normalfed adult rabbits (e.g., Schumacher and Rehmer, 1960;
Weijs and Dantuma, 1981). Any inconsistencies in absolute values among these studies are likely accounted for
by differences in developmental age at the time of measurement.
The OU-fed rabbits exhibit an increase in PCSA of
the superficial masseter compared to the UU-fed rabbits
(Table 1). This increase is observed in all portions of the
superficial masseter muscle. Thus, despite functional heterogeneity in the masseter muscle (e.g., the balancingside superficial portions fire first, followed by the deeper
portions) (Weijs and Dantuma, 1981), larger muscle and
bite forces are required throughout both the superficial
(Fig. 3, Table 1) and deep (e.g., Langenbach et al., 2003)
masseter in order to generate adequate bite forces for
mastication of a tougher diet. These findings are also
empirically congruent with previous experimental study
(Weijs and Dantuma, 1981) demonstrating that in rabbit
masseter, all muscle portions (both superficial and deep)
reach maximum activity levels during ipsilateral chewing
of hay compared to mastication of pellets or carrots.
The differential increase in muscle weight and PCSA
over fiber length corresponds with previous studies demonstrating that in mammalian pinnate-fibered muscles,
postnatal growth is characterized by increases in muscle
width, either by increasing myofibril number, diameter,
or both, while longitudinal growth is completed early in
ontogeny (Carlson, 1983; Stickland, 1983; Herring and
Wineski, 1986; Woittiez et al., 1986; Langenbach and
Weijs, 1990). Weijs and Dantuma (1987) observed a 15%
increase in fiber length from weanling to adult rabbits,
compared to a fivefold increase in muscle weight during
the same period of growth. Although increase in pinnation angle can improve muscle (and hence bite) force
(Herring et al., 1979; Gans, 1982), results of this study
suggest that augmenting pinnation angle is not a biomechanical solution to improving muscle force during
growth, as the OU-fed rabbits demonstrated an increase
in PCSA solely as a function of increase in masseter
muscle mass. The finding that OU and UU of the masticatory complex during growth largely influences muscle
mass suggests that alterations in dietary consistency
have an impact on masticatory force production, but not
Fig. 3. Box plot comparing PCSA in the OU diet (light gray) and
UU diet (dark gray) rabbits. The center line represents the median, the
boundary of the box represents the 25th and 75th percentiles, and the
whiskers represent the 10th and 90th percentiles. In all muscle portions and whole rabbit masseter, PCSA is significantly greater in the
OU diet rabbits.
necessarily on jaw movement or excursion. By contrast,
increase in masseter and temporalis muscle fiber length,
accompanied by a reduction in pinnation angle, has been
associated with requirements for increased muscle
stretch in animals generating wide jaw gapes during
feeding (Taylor and Vinyard, 2004, in press; Eng et al.,
2005). However, the extent to which these observed differences in fiber length occur during growth remains
unknown.
It has been previously demonstrated (Langenbach
et al., 2003) that dietary consistency influences the
cross-sectional area of posterior deep masseter fibers,
but not of superficial masseter fibers. However, in the
Langenbach et al. (2003) study, animals were entered
into the experimental dietary protocol as subadults
(16 weeks of age). Therefore, the preexperimental diet
may have influenced masseter muscle growth (e.g., Weijs
et al., 1987), so that the extent to which differences
between the two rabbit groups can be attributed to
variation in dietary consistency remains somewhat ambiguous. Moreover, age-related decreases in plasticity
have been shown to characterize bony, cartilaginous,
1110
TAYLOR ET AL.
and muscular tissues of the masticatory and other systems (Bouvier, 1988; Chang et al., 1995; Bouvier and
Hylander, 1996a, 1996b; Welle et al., 2000; Narici et al.,
2004; Kim et al., 2005; Ravosa et al., 2006a, in press).
Indeed, differences in the timing of implementation of
experimental protocols may account in part for the disparity in findings between the Langenbach et al. (2003)
study, which showed no changes in fiber composition,
and those of other investigators who initiated specialized
diets soon after weaning (e.g., Kiliaridis et al., 1988).
Although beyond the scope of this study, the observed
increase in PCSA of the superficial masseter suggests
it would be worthwhile to reevaluate the influence of
dietary consistency on masseter fiber composition early
in ontogeny (i.e., at or near weaning).
In summary, it can be concluded that dietary consistency influences rabbit masseter PCSA, but not fiber
length or pinnation angle. Specifically, rabbits masticating tougher foods are characterized by an increase in
masseter PCSA, largely accounted for by increase in
muscle mass, compared to genetically similar rabbits
masticating a less tough diet. Moreover, all portions of
the superficial masseter muscle exhibit increases in
PCSA, indicating that improved muscle and bite force
occurs homogeneously throughout the superficial masseter. Results presented here suggest that alterations in
muscle fiber architecture are facilitated during early
growth due to variation in dietary consistency.
ACKNOWLEDGMENTS
Supported by the Department of Cell and Molecular
Biology, Northwestern University (to M.J.R.) and the
National Science Foundation (BCS-0412153; to A.B.T.).
Barth Wright kindly performed the analyses of rabbit
food material properties. Two anonymous reviewers provided useful comments that improved the quality of this
manuscript.
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architecture, fiber, dietary, rabbits, masseter, plasticity, postweaning, consistency
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