Dietary consistency and plasticity of masseter fiber architecture in postweaning rabbits.код для вставкиСкачать
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: firstname.lastname@example.org 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. 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