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First published online January 31, 2007
Journal of Experimental Biology 210, 628-641 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02683
Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints
1 Department of Pathology and Anatomical Sciences, University of Missouri
School of Medicine, M263 Medical Sciences Building, One Hospital Drive
DC055.07, Columbia, MO 65212, USA
2 Department of Cell and Molecular Biology, Northwestern University Feinberg
School of Medicine, Chicago, IL, USA
3 Department of Molecular Pharmacology and Biological Chemistry,
Northwestern University Feinberg School of Medicine, Chicago, IL,
USA
* Author for correspondence (e-mail: ravosam{at}missouri.edu)
Accepted 5 December 2006
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Summary |
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Here, we argue that a critical component of current and future research on adaptive plasticity in the skull, and especially cranial joints, should employ a multifaceted characterization of a functional system, one that incorporates data on myriad tissues so as to evaluate the role of altered load versus differential tissue response on the anatomical, cellular and molecular processes that contribute to the strength of such composite structures. Our study also suggests that the short-term duration of earlier analyses of cranial joint tissues may offer a limited notion of the complex process of developmental plasticity, especially as it relates to the effects of long-term variation in mechanical loads, when a joint is increasingly characterized by adaptive and degradative changes in tissue structure and composition. Indeed, it is likely that a component of the adaptive increases in rabbit TMJ and symphyseal proportions and biomineralization represent a compensatory mechanism to cartilage degradation that serves to maintain the overall functional integrity of each joint system. Therefore, while variation in cranial joint anatomy and performance among sister taxa is, in part, an epiphenomenon of interspecific differences in diet-induced masticatory stresses characterizing the individual ontogenies of the members of a species, this behavioral signal may be increasingly mitigated in over-loaded and perhaps older organisms by the interplay between adaptive and degradative tissue responses.
Key words: temporomandibular joint (TMJ), symphysis, mechanical properties, MicroCT, microanatomy, rabbit, masticatory stress/load, adaptive plasticity, functional adaptation, degradation
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Introduction |
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; Agrawal,
2001; Holden and Vogel,
2002; West-Eberhard,
2003). Adaptive plasticity refers to the ability of an organism to
respond ontogenetically to an altered environmental condition(s)
(Gotthard and Nylin, 1995).
Thus, it is intimately related to the concept of functional adaptation, which
typically refers to the dynamic coordinated series of cellular, tissue and
biochemical processes of modeling and remodeling that occur to maintain a
sufficient safety factor of a given element or system to routine peak stresses
(Lanyon and Rubin, 1985;
Biewener, 1993;
Bouvier and Hylander, 1996a;
Bouvier and Hylander, 1996b;
Vinyard and Ravosa, 1998;
Hamrick, 1999). In the case of
cortical bone, the link between altered loading patterns and functional
adaptation is reasonably well documented for vertebrate limb elements and the
mammalian mandibular corpus (Bouvier and
Hylander, 1981; Lanyon and
Rubin, 1985; Biewener et al.,
1986; Biewener and Bertram,
1993). Studies regarding the ontogeny of locomotor performance
have been equally fundamental for identifying behavioral, anatomical and
physiological adaptations and constraints specific to particular ages
(Carrier, 1996). A common goal
of these and other investigations is to analyze, under naturalistic
conditions, the range of behaviors an organism employs with a given morphology
as well as the role of adaptive plasticity in fine-tuning the fit between form
and behavior during an organism's lifespan
(Grant and Grant, 1989;
Losos, 1990). In doing so,
such analyses of the biological role of a feature or system directly address
one or more facets of the important inter-relationships among behavior,
morphology, performance, fitness and evolution, information critical for
understanding ontogenetic and interspecific variation in character-state
transformations (Bock and von Walhert,
1965; Losos, 1990;
Wainwright and Riley, 1994; Lauder,
1995).
For those interested in the evolution of craniomandibular variation, an
understanding of the short- and long-term effects of dynamic alterations in
masticatory stress is critically important for interpreting the behavioral
and/or ecological correlates of fossil form, functional adaptation in
routinely loaded systems/elements, as well as the onset and progression of
joint disease and dysfunction. Most information on plasticity in the mammalian
masticatory complex is derived from alert organisms subjected to variation in
jaw-loading patterns via the postnatal manipulation of dietary
properties (e.g. Bouvier and Hylander,
1981; Bouvier and Hylander,
1982; Bouvier and Hylander,
1984; Bouvier and Hylander,
1996a; Bouvier and Hylander,
1996b). This methodology has proven beneficial because masticatory
stresses due to jaw-adductor, bite and reaction forces are elevated during the
processing of relatively tough and/or resistant foods
(Herring and Scapino, 1973;
Thexton et al., 1980;
Weijs et al., 1987;
Weijs et al., 1989;
Gans et al., 1990;
Dessem and Druzinsky, 1992;
Hylander et al., 1992;
Hylander et al., 1998;
Hylander et al., 2000;
Hylander et al., 2005;
Ravosa et al., 2000), and
mammals with such diets typically possess relatively larger mandibular
dimensions (Freeman, 1979;
Freeman, 1981;
Freeman, 1988;
Hylander, 1979b;
Bouvier, 1986;
Daegling, 1989;
Daegling, 1992;
Ravosa, 1991a;
Ravosa, 1991b;
Ravosa, 1996;
Biknevicius and Ruff, 1992;
Ravosa and Hylander, 1994;
Spencer, 1995;
Biknevicius and Van Valkenburgh,
1996; Hogue, 2004;
Ravosa and Hogue, 2004).
Indeed, early research on masticatory plasticity observed that growing
monkeys raised on an over-use diet of hard/resistant items exhibit greater
cortical bone remodeling as well as greater mandibular depth and cortical bone
thickness (Bouvier and Hylander,
1981). Compared to the temporomandibular joint (TMJ) of
under-use/soft-diet macaques, over-use/hard-diet macaques of the same age also
develop a higher density of connective tissue and subchondral bone as well as
thicker condylar articular cartilage
(Bouvier and Hylander, 1982).
Similar patterns characterize condylar and craniofacial dimensions as well as
articular cartilage thickness in rats and rabbits raised postnatally on
different diets (Beecher and Corruccini,
1981; Bouvier and Hylander,
1984; Kiliardis et al.,
1985; Bouvier,
1987; Bouvier,
1988; Bouvier and Zimny,
1987; Block et al.,
1988). Increased alkaline phosphatase activity associated with
biomineralization of TMJ condylar tissues, and changes in osteoclastic and
osteoblastic activity also have been noted
(Bouvier, 1988;
Kim et al., 2003). In
addition, altering TMJ force application by varying masticatory loading
regime, tooth extraction, unilateral bite raise or corticotomy has been shown
to result in gene expression changes and elevated glycosaminoglycan (GAG)
content in condylar cartilage (Copray et
al., 1985; Carvalho et al.,
1995; Holmvall et al.,
1995; Pirttiniemi et al.,
1996; Mao et al.,
1998; Agarwal et al.,
2001; Huang et al.,
2002; Huang et al.,
2003). Lastly, changes in expression of type I and type II
collagen vary in response to joint loads, further supporting the hypothesis
that mechanotransduction signals changes in gene expression that alter tissue
proliferation, composition and function as a response to induced degeneration
of the cartilage matrix (Mizoguchi et al.,
1996; Pirttiniemi et al.,
1996; Grodzinsky et al.,
2000; Honda et al.,
2000; Lee et al.,
2000; Huang et al.,
2003; Kim et al.,
2003; Wong and Carter,
2003).
The use of naturalistic experimental approaches ensures that potential tissue, cellular and biochemical responses do not result from aberrant behaviors and/or surgical artifacts, thus facilitating the identification of a range of physiological responses or norms of reaction of joint components to variation in masticatory loads. However, despite the fact that an understanding of the performance and integrity of the mandibular symphysis and TMJ hinges on the ability of individual tissues of such composite structures to adapt to applied stresses, no comprehensive comparative data exist regarding the dynamic cascade of anatomical, biochemical and biomechanical responses of bone and cartilage tissues of these cranial joints vis-à-vis long-term alteration of masticatory loads. Moreover, due to the presence of considerable variation in loading conditions across various experimental studies to date as well as a dearth of evidence regarding adaptive plasticity in cranial arthroses such as the mammalian mandibular symphysis, it has been difficult to compare norms of reactions for different masticatory elements or systems.
In this regard, symphyseal and TMJ tissues from diet-modified rabbits were analyzed for changes in (i) joint proportions and cortical bone thickness associated with the ability to counter increased joint stresses; (ii) biomineralization via microcomputed tomography (microCT) of articular, subarticular and cortical bone linked to the compressive strength of bone; and (iii) histology and immunohistochemistry of articular cartilage extracellular matrix (ECM) composition related to a primary role of joint cartilage in resisting compressive loads. The underlying hypothesis is that dynamic alterations in masticatory stresses during chewing and biting will induce postweaning variation in gross proportions, bony and connective tissue anatomy, tissue properties and biochemistry, a series of changes which serve to maintain the strength and integrity of the mammalian symphysis and TMJ. In particular, rabbits subjected to elevated masticatory loads are predicted to develop: (i) relatively larger symphyses, condyles, corpora and jaw-adductor muscles; (ii) greater symphyseal cortical bone thickness; (iii) elevated bone-density levels along the symphysis and TMJ condyle; and (iv) increased type II collagen and proteoglycan expression in the symphyseal fibrocartilage (FC) pad and TMJ articular cartilage. These analyses address a related goal, which is to uniquely conduct a long-term study of adaptive plasticity and norms of reaction in comparable tissue types from two cranial joints in the same model organism subjected to the same loading conditions.
Evidence on anatomical, structural and biochemical patterns of variation are used to address several additional outstanding issues regarding masticatory function in mammals: (i) the absence of data on adaptive plasticity for cranial arthroses (symphysis), joints with highly disparate functional and structural constraints as compared to synovial joints (TMJs) and syndesmoses (sutures); (ii) the correlational nature of in vivo and morphological support for models of symphyseal fusion, and a related claim that symphyseal strength is unrelated to variation in fusion; and (iii) the preponderance of experimental information on symphyseal fusion for members of only a single mammalian order (Primates). Therefore, in identifying dynamic determinants of joint growth, form and function in a model organism, this experimental research develops an integrative, ontogenetic framework for investigating important inter-relationships among mechanobiology, adaptive plasticity and performance in the mammalian skull and masticatory system.
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; Yardin,
1974). To control for variation in genetics and thus ensure the
response to loading modification occurred postnatally, only siblings were
used. Two dietary cohorts of ten rabbits each were established to induce
postweaning variation in jaw-adductor activity and masticatory loads. Weaning
was chosen as the starting point for dietary manipulation because plasticity
may decrease with age (Bouvier,
1988) and because we sought to minimize the confounding influence
of postweaning diets other than those utilized herein. Weanlings were fed
ad lib either a `soft' diet of ground pellets to model under-use (U)
of the chewing complex or a `tough/hard' diet of Harlan TekLad (Madison, WI,
USA) rabbit pellets supplemented daily with two 2-cm hay blocks to model
over-use (O). The inclusion of pellets in the diet of all weanling rabbits
ensured adequate nutrition for normal growth. In this regard, behavioral
analyses and observations indicate that U-diet rabbits did not exhibit failure
to thrive nor did they develop incisor malocclusions; 90% of the U-diet sample
is within the skull–length range for ten O-diet rabbits. Procedures for
dietary alteration, animal monitoring and euthanasia under heavy sedation were
conducted in accordance with an ACUC-approved protocol for M.J.R.
A major benefit of domestic white rabbits is that considerable in
vivo data exist regarding jaw-adductor muscle activity, jaw-kinematic and
jaw-loading patterns, masticatory function during ontogeny, and the link
between masticatory behaviors and diet
(Weijs et al., 1987;
Weijs et al., 1989;
Langenbach et al., 1991;
Langenbach et al., 1992;
Langenbach et al., 2001;
Langenbach and van Eijden,
2001). Similar to a variety of mammals, rabbit jaw-adductor
activity patterns vary with dietary properties, such that harder, more
resistant foods (pellets) and more non-brittle, tough foods with higher
elastic moduli (hay) require absolutely larger jaw-adductor forces during
biting and chewing (Weijs et al.,
1989; Hylander et al.,
1992; Hylander et al.,
2000; Hylander et al.,
2005). In rabbits and other mammals, this results in elevated peak
strains along the mandible and higher TMJ reaction forces
(Weijs and de Jongh, 1977;
Hylander, 1979a;
Hylander, 1979b;
Hylander, 1979c;
Hylander, 1992;
Hylander et al., 1998;
Ravosa et al., 2000). Like
marsupials, rodents, carnivorans, artiodactyls and primates, rabbits exhibit
postnatal variation in the size and conformation of the articular surface and
connective tissues of the symphysis, beginning as an amphiarthrosis (unfused)
in neonates and developing into a synarthrosis (partially fused) by adulthood
(Trevisan and Scapino, 1976a;
Trevisan and Scapino, 1976b;
Beecher, 1977;
Beecher, 1979;
Hirschfeld et al., 1977;
Scapino, 1981;
Weijs and Dantuma, 1981;
Ravosa and Simons, 1994;
Ravosa, 1996;
Ravosa, 1999;
Hogue and Ravosa, 2001;
Hogue, 2004).
Material properties of experimental foods
Using a portable food tester (Darvell
et al., 1996; Lucas et al.,
2001), the material properties of pellets and hay were assessed
(Table 1) and were routinely
monitored to ensure consistency
(Wainright et al., 1976;
Vincent, 1992;
Lucas, 1994;
Currey, 2002). The elastic, or
Young's, modulus (E) is the stress/strain ratio at small
deformations, characterizing the stiffness or resistance to elastic
deformation. Toughness (R) is an energetic property describing the
work performed propagating a crack through an item. Hardness (H) is
used to quantify indentation. While the properties of crushed pellets differ
little from intact pellets, the latter entail greater repetitive loading due
to a longer processing time. Thus, the sequence from crushed pellets to whole
pellets (only) to pellets with hay tracks diets with longer preparation time
and progressively greater elastic moduli, hardness and toughness (well known
to result in increasingly elevated masticatory stresses – see above). As
the between-cohort comparisons largely accentuate the duration of oral
processing (i.e. crushed pellets exhibit similar properties to whole pellets),
U-diet rabbits are posited to more closely resemble normal/non-pathological
loading conditions. Indeed, unlike the anatomy of O-diet rabbits, masticatory
joints of U-diet rabbits are similar to those for a limited number of 6-month
old adult rabbits raised on a `normal/control' diet of intact pellets (M.J.R.,
unpublished observation).
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Morphometry of masticatory elements
Following euthanasia, rabbit skulls were detached at the vertebral column
and jaw-adductor muscles exposed and carefully dissected from their
attachments. Left and right mandibles were detached from the skull and fixed
in 10% buffered formalin. All specimens were weighed (to 0.01 g), with digital
calipers used to obtain mandible length/breadth, symphysis length/width,
corpus height/width, condyle width/length and masseter mass
(Ravosa, 1991b;
Nicholson et al., 2006). Such
morphometric data also were used to control for size-related variation in the
skull and masticatory apparatus in comparisons of loading cohorts
(Bouvier and Hylander, 1981;
Bouvier and Hylander, 1982;
Bouvier and Hylander, 1984).
Subsequently, symphyseal and TMJ samples were employed in microcomputed
tomography (microCT) analyses of biomineralization and cortical bone
thickness, followed by histology and immunohistochemistry.
MicroCT analysis of skeletal biomineralization
Intra- and between-group variation in joint structure was assessed
via microCT (Wong et al.,
1995; Nuzzo et al.,
2002; Patel et al.,
2003; Stock et al.,
2003; Morenko et al.,
2004; Nicholson et al.,
2006; Ravosa et al.,
2007a; Ravosa et al.,
2007b). Using a Scanco Medical MicroCT 40 (PA, USA), the
microfocus X-ray tube was operated at 70 kV and 57 µA, and the beam passed
through a 0.13 mm thick beryllium window on the X-ray tube and through a 0.50
mm thick aluminum filter before encountering a sample. With this cone beam
system, data from fixed specimens were collected with the longest integration
time (0.30 s per view) and the highest sensitivity mode (1000 projections over
180°, 2048 samples per projection). Reconstruction was with 8 µm voxels
(volume elements). The linear attenuation coefficient (µ) was measured in
reconstructed slices parallel to the coronal plane: five equidistant sites per
symphysis (labial, anterior, middle, posterior, lingual) and three equidistant
sites per TMJ (anterior, middle, posterior). For each joint site, 40
contiguous slices covering 0.31 mm were imaged, with one such slice chosen to
represent a given site. At each symphyseal site, µ was sampled at a total
of nine locations: five equidistant points along the articular surface and
four equidistant points along the external cortical bone
(Fig. 1A). At each condylar
site, µ was sampled a total of 15 locations: five equidistant points along
the articular surface, four equidistant subchondral points and three
equidistant points per side along cortical bone of the condylar neck
(Fig. 1B). Values of linear
attenuation were pooled for each specimen and used to characterize
between-group variation in biomineralization or local tissue mineral density
along the symphysis and TMJ (Fig.
1) (Nicholson et al.,
2006; Ravosa et al.,
2007a; Ravosa et al.,
2007b). For symphyseal coronal sections, linear data on joint
height and width as well as articular surface thickness and three measures of
cortical bone thickness were collected in each slice.
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). A
sample of aluminum of known composition (and roughly the same linear
attenuation coefficients, 2.92<µ<2.96 cm–1, as the
TMJ, 2.6<µ<3.3 cm–1, at 70 kV) was used to determine
the effective energy. Using the NIST tabulation of mass attenuation
coefficients (Hubbell and Selzer,
2001), the effective energy for Northwestern University's Scanco
MicroCT 40 operated at 70 kV is about 30 keV.
Histology and immunohistochemistry of cartilage composition
Histological and immunohistochemical analysis of symphyseal and TMJ tissues
followed standard procedures (Scapino,
1981; Trevisan and Scapino,
1976a; Trevisan and Scapino,
1976b; Beecher,
1977; Beecher,
1979; Hirschfeld et al.,
1977; Bouvier and Hylander,
1982; Bouvier and Hylander,
1984; Bouvier,
1987; Bouvier,
1988; Kiernan,
1999; Huang et al.,
2002; Kim et al.,
2003; Ravosa and Hogue,
2004). Joints were fixed in 10% neutral buffered formalin. Once
analyzed via microCT, a specimen was decalcified via formic
acid and sodium citrate. The oxalate test was used to verify the endpoint of
decalcification. Subsequently, a joint was dehydrated in a series of
increasingly concentrated ethanol baths, washed in xylene, and then embedded
in paraffin. Special care was exercised to maintain symphyseal and TMJ, and
ultimately section, orientation parallel to the surface of the paraffin block.
At five equidistant sites per symphysis (labial, anterior, middle, posterior,
lingual) and at three equidistant sites per TMJ (anterior, middle, posterior),
4–6 µm sections were obtained with a Reichert–Jung autocut
microtome in the coronal plane, i.e. orthogonal to craniomandibular long axis.
Once floated on a water bath, collected on a coated slide, dried and finally
deparaffinized, each section then was stained by one of several methods.
The cationic dye Safranin O was used to evaluate relative GAG content in
the symphyseal fibrocartilaginous pad and TMJ articular/hyaline cartilage
(Kiernan, 1999;
Huang et al., 2002). Primary
antibodies directed at variation in cartilage type II collagen were employed
to assess collagen and proteoglycan relative expression pattern (i.e. change
in staining localization) as a function of masticatory loads (Type II Collagen
Staining Kit; Chondrex Inc., Redmond, WA, USA). Lastly, tunel-staining was
employed to track variation in DNA fragmentation and chondrocyte apoptosis in
response to joint loading (Apoptosis Detection Kit; Chemicon Inc., Temecula,
CA, USA). Although not presented here, H&E was utilized to distinguish the
FC pad and ligaments of the symphysis as well as the articular cartilage
layers of the TMJ. Definitions of progressively deeper zones of TMJ articular
cartilage are as follows: articular, filamentous network of elongate cells
densely packed and tangentially arranged (high H2O, low
proteoglycan, collagen rich); proliferative, ovoid or circular cells random in
distribution (proteoglycan/protein production area); chondroblastic, large
cell bundles arranged in columns (tidemark separates this from subjacent
layer); hypertrophic chondrocyte/calcified, cells heavily encrusted in
apatitic salts (Mankin et al.,
1971; Newton and Nunamaker,
1985; Ostergaard et al.,
1999). To facilitate a characterization of the integrated suite of
dynamic adaptive and degradative responses of skeletal and connective tissues
to altered mechanical loads, similar sample sections and locations were used
for microCT, histology and immunohistochemistry.
Statistical analysis and predictions
The first step in the analysis of the linear data on symphyseal and TMJ
proportions from morphometry and microCT was to adjust for variation in
masticatory or body/skull size between loading cohorts. This occurred by
calculating the ratio of a given linear dimension, or cube root of a
volumetric measure, versus jaw length
(Bouvier and Hylander, 1981;
Bouvier and Hylander, 1982;
Bouvier and Hylander, 1984;
Bouvier, 1986;
Ravosa and Hylander, 1994;
Ravosa and Hogue, 2004). To
facilitate the comparison of specific masticatory parameters and to
characterize the magnitude of difference between dietary cohorts, all
between-group differences in metric and microCT data were tested via
non-parametric ANOVA (Mann–Whitney U-test, P<0.05);
in the case of metric data, this consisted of analyses of size-adjusted
masticatory proportions (means, s.d.). To provide a confirmatory, multivariate
characterization of differences in bone-density levels between loading
cohorts, discriminant function analysis was employed. This procedure was used
to evaluate if, based on a series of biomineralization parameters, a given
joint was correctly identified as belonging to its dietary cohort, thus
offering a quantitative measure of overall morphological distinctness and
adaptive plasticity between loading groups
(Nicholson et al., 2006;
Ravosa et al., 2007a).
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MicroCT
The influence of routine joint over-use and under-use on symphyseal and TMJ
biomineralization, and on internal symphyseal proportions, was evaluated
via microCT. MicroCT analyses of the articular surface, subarticular
bone and cortical bone along the symphysis and TMJ condyle indicate that
significant variation develops in joint density and anatomy between O-diet and
U-diet rabbits, with the former group exhibiting significantly higher levels
of biomineralization (Table 3,
Table 4). Using linear
attenuation coefficients (µ) for 9 symphyseal and 15 TMJ sites,
discriminant function analysis was performed for each joint to summarize
patterns of variation in bone-density levels between U-diet and O-diet
rabbits. Much as expected based on the univariate ANOVAs, these multivariate
analyses of biomineralization for each joint correctly classified all members
of each dietary group (as such, these redundant results are not presented).
ANOVAs also indicate the presence of significantly thicker cortical bone along
the symphyseal outer and articular surfaces in O-diet rabbits
(Fig. 2;
Table 2). These findings
underscore the significant influence of dietary material properties on
adaptive plasticity in masticatory proportions, tissue structure and bone
mineral density.
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Histology and immunohistochemistry
Sulfated GAGs are expressed in tissues regularly exposed to loads, and rat
TMJ chondrocytes have been shown to increase GAG synthesis in response to
mechanical force (Copray et al.,
1985; Carvalho et al.,
1995). Strong Safranin O staining is indicative of keratan
sulfate-containing proteoglycans and chondroitin sulfate, which in turn
increases the viscoelastic ability of cartilage for resisting compressive
stresses. Type II collagen has a distinct fibrillar organization and
associates strongly with water and proteoglycans, important for tissues
subjected to compression, tension and shear, such as the symphyseal FC pad and
TMJ articular cartilage (Mizoguchi et al.,
1996; Pirttiniemi et al.,
1996; Benjamin and Ralphs,
1998; Tanaka et al.,
2000).
Histological analyses of U-diet and O-diet subadults indicate more intense
Safranin O staining in the symphyseal FC pad (compare `A' vs `B' in
Fig. 3) and TMJ condylar
articular cartilage of the U-diet rabbit (compare `A' vs `B' in
Fig. 4). Lower proteoglycan
content throughout the FC pad and in the lower two layers of the condylar
cartilage of O-diet rabbits mirrors findings for the articular surface of
mammal limb elements, where age-related onset of cartilage degradation is
linked to decreases in proteoglycan content
(Mankin et al., 1971;
Newton and Nunamaker, 1985;
Haskin et al., 1995;
Ostergaard et al., 1999). Due
to the elevated viscoelasticity of proteoglycan-rich tissues in joints
subjected to cumulatively low postnatal stresses (i.e. U-diet), analyses
suggest that articular cartilage and fibrocartilage of such organisms are able
to resist greater compressive stresses than that of repetitively over-loaded
cranial joints. As proteoglycan content is most pronounced in the two
innermost layers of TMJ articular cartilage (chondroblastic and
hypertrophic/calcified chondrocyte), this suggests it is critical to account
for regional variation in this and other ECM components in evaluating the
biomechanical significance of cartilage properties and proportions.
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Immunohistochemical data for U-diet versus O-diet subadult rabbits demonstrate a more widespread distribution of type II collagen in the symphyseal FC pad and TMJ condylar articular cartilage of U-diet rabbits (Fig. 5, Fig. 6). Expression of collagen II has been noted in the ECM of mature chondrocytes and inner cartilage layers such as the hypertrophic and chondroblastic zones of the TMJ. Type II collagen has a distinct fibrillar organization and associates more strongly with proteoglycans, and both ECM components are important in tissues subjected to compressive loads during biting and chewing. These comparisons suggest that, much as the case for the well-documented TMJ, symphyseal adaptive plasticity is characterized by similar of patterns of postweaning variation in type II collagen and proteoglycan content (Figs 2, 3).
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). Thus, increased numbers of apoptotic hypertrophic
chondrocytes appear related to advance of the subchondral mineralizing
front.
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Discussion |
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; Ravosa,
1996; Ravosa,
1999; Ravosa and Hogue,
2004). Once weaned, mammals ingest `adult' food items (e.g.
Watts, 1985;
Tarnaud, 2004) and develop
`adult' jaw-adductor activity patterns
(Herring and Wineski, 1986;
Weijs et al., 1987;
Herring et al., 1991;
Iinuma et al., 1991;
Langenbach et al., 1991;
Langenbach et al., 1992;
Langenbach et al., 2001;
Westneat and Hall, 1992;
Huang et al., 1994), with
associated skeletal and soft-tissue responses to `adult' jaw-loading regimes
(Ravosa, 1991a;
Ravosa, 1992;
Ravosa, 1996;
Ravosa, 1999;
Cole, 1992;
Biknevicius and Leigh, 1997;
Vinyard and Ravosa, 1998;
Taylor et al., 2006).
Early experimental studies of postweaning plasticity in the mammalian
masticatory apparatus often focused on the mandibular corpus and TMJ articular
cartilage (cf. Bouvier and Hylander,
1981; Bouvier and Hylander,
1982; Bouvier and Hylander,
1984). More recent work provides considerable support for the
hypothesis that cartilage of the mandibular condyle and TMJ articular disc is
affected by local biomechanical effects. Indeed, chondrocytes are highly
sensitive to 3-D microenvironment and exhibit changes in differentiation
status in response to environmental cues (Lemare et al., 1988;
Goldring, 2004a;
Goldring, 2004b), with
expression of cartilage ECM elements likely reflecting regional variation due
to differential loading patterns in distinct joint regions
(Bayliss et al., 1983;
Nakano and Scott, 1989;
Mow et al., 1990;
Hamrick, 1999;
Tanaka et al., 2000). In this
regard, it is interesting that collagen- and proteoglycan-degrading
proteinases have been reported in TMJ tissues and synovial fluids
(Kiyoshima et al., 1993;
Kiyoshima et al., 1994;
Marchetti et al., 1999;
Puzas et al., 2001;
Srinivas et al., 2001).
A general conclusion is that growth responses of the mandibular condyle
following alteration of local biomechanical conditions (both increased and
decreased loads) can lead to hyperplastic or hypoplastic changes in TMJ
cartilage and bone (Bouvier and Hylander,
1984; Nicholson et al.,
2006). Based largely on short experimental periods in growing
mammals (<2 months), these studies support the hypothesis that altered,
excessive and/or repetitive forces induce secondary osteonal remodeling of
mandibular cortical bone and chondroblastic activity of articular cartilage, a
suite of physiological responses or functional adaptations that maintain a
sufficient safety factor for the tissues of a cranial element or joint complex
to routine peak masticatory loads (cf.
Lanyon and Rubin, 1985;
Biewener, 1993;
Bouvier and Hylander, 1996a;
Bouvier and Hylander, 1996b;
Vinyard and Ravosa, 1998;
Hamrick, 1999;
Ravosa et al., 2000). These
investigations also suggest that a minimum loading level and frequency is
required for the growth and maintenance of normal adult skull form and
function (Beecher et al., 1983;
Bouvier and Hylander, 1984).
Interestingly, the magnitude of such responses appears to be age-dependent and
may be underlain by genetic and epigenetic factors that vary systemically and
interspecifically (Bouvier,
1988; Bouvier and Hylander,
1996a; Bouvier and Hylander,
1996b).
Employing an animal model for which considerable in vivo data on
feeding behavior are available, we performed a series of integrative
experiments to probe the longer-term dynamic links among mechanical loading,
tissue adaptive plasticity, norms of reaction and performance in two mammalian
masticatory joint systems. The mandibular symphysis and TMJ are highly
specialized joints capable of both rotational and translational movements, and
thus encounter multidirectional compressive, shear and tensile forces during
biting and chewing (Rigler and Mlinsek,
1968; Beecher,
1977; Beecher,
1979; Hylander,
1979a; Hylander,
1979b; Hylander,
1979c; Hylander,
1992; Scapino,
1981; Ravosa and Hogue,
2004). In addition to cortical and trabecular bone, TMJs and
symphyses are composed of cartilage, ligaments and dense fibrous tissue
containing proteoglycans and collagens (Figs
2,
3,
4,
5,
6,
7,
8). As the symphyseal FC pad
and TMJ articular cartilage are anchored into subarticular bone, their stress
distributions are constrained respectively by movements between dentaries
(symphysis) or between the mandibular condyle and temporal bone (TMJ).
Analyses of rabbits represent the first case where plasticity is assessed
at two different joints in the same model organism. In this experimental
model, symphyses and TMJs of over-loaded joints develop larger joint
proportions and higher bone-density levels, coupled with lower proteoglycan
content, lower type II collagen and greater chondrocyte apoptosis.
Interestingly, although symphyseal fibrocartilage is more acellular, it
exhibits responses similar to that for hyaline cartilage of the TMJ articular
surface. However, while the gross anatomical and bone biomineralization data
are much as predicted, findings for the ECM composition of joint cartilage
seemingly contradict shorter-term experimental studies cited above. In light
of this earlier work, it is reasonable to interpret the rabbit cartilage
patterns as the result of degradative changes due to long-term joint
over-loading. Thus, we do not and cannot refute the fact that cartilage
exhibits a compensatory adaptive response to joint over-loading. Rather, the
duration of dietary manipulation in our study greatly exceeds that of previous
investigations and it is well known that cartilage exhibits accelerated
degradation in response to elevated and/or repetitive loading
(Guerne et al., 1994;
Guerne et al., 1995;
Bae et al., 1998). Such changes
in cartilage composition reflect the early onset and progression of
degenerative effects that compromise the structural integrity of a joint
(Mankin et al., 1971;
Newton and Nunamaker, 1985;
Haskin et al., 1995;
Kamelchuk and Major, 1995;
Ishibashi et al., 1996;
Ostergaard et al., 1999;
Fujimura et al., 2005). This
interpretation is consistent with patterns of change noted for rabbit TMJ
connective tissues. In fact, it is likely that a component of the adaptive
changes in mammalian joint proportions and biomineralization represents a
compensatory mechanism to cartilage degradation that maintains the overall
functional integrity of such composite tissue systems.
In the case of the rabbit symphysis, the development of bony rugosities,
larger joint surfaces due to thicker cortical bone and greater bone density,
all represent adaptive responses to joint over-loading (Tables
2,
3; Figs
2,
3,
5). However, repetitive joint
over-loading results in the FC pad eventually becoming less viscoelastic,
which diminishes its ability to resist compressive stresses. As joint
ossification clearly does not compromise symphyseal function as it would with
the TMJ, the disparate long-term responses of symphyseal soft versus
hard tissues may explain a common (but poorly understood) intraspecific trend
of older mammals developing increased fusion (cf.
Beecher, 1977;
Beecher, 1979;
Scapino, 1981;
Ravosa and Simons, 1994;
Ravosa, 1996;
Ravosa, 1999;
Hogue and Ravosa, 2001). Thus,
age-related changes in fusion, especially in old adults, may represent a
compensatory osteogenic response to load-induced degradation of the FC pad and
perhaps other connective tissues.
The rabbit findings are similar to recent analyses of myostatin-deficient
mice documenting greater differentiation of symphyseal parameters in response
to elevated physiological loads (Ravosa
et al., 2007a), which is suggestive of greater tissue plasticity
or norms of reaction for this joint versus elsewhere in the
masticatory system (Tables 2,
3,
4). It is thus interesting that
the symphysis experiences relatively higher bone-strain levels during biting
and chewing, and is characterized by strong positive allometry of joint
proportions (Hylander, 1979a;
Hylander, 1979b;
Ravosa, 1991a;
Ravosa, 1991b;
Ravosa, 1992;
Ravosa, 1996;
Ravosa and Hylander, 1994;
Hylander et al., 1998;
Vinyard and Ravosa, 1998;
Hogue and Ravosa, 2001;
Hogue, 2004;
Ravosa and Hogue, 2004;
Ravosa et al., 2000), two
additional factors that likely contribute to the potential for increased
symphyseal plasticity.
As alluded to above, our research uniquely suggests that the short-term duration of earlier analyses of cranial joint tissues may offer a limited notion of the complex process of developmental plasticity, especially as it relates to the effects of long-term alterations in mechanical loads, when a joint is increasingly characterized by adaptive and degradative changes in tissue structure, composition and function. Perhaps not surprisingly, we also sound a cautionary note that the assessment of masticatory plasticity based solely on external joint proportions can under-represent the amount of change in individual tissues. For instance, the magnitude of the plasticity response differs between loading cohorts according to the level of analysis, e.g. external joint proportions vary less between dietary groups (Table 2) than in comparisons of skeletal biomineralization (Tables 3, 4).
Adaptive plasticity and symphyseal function
Though it is well known that in vivo information is best for
detailing how an animal functions during normal behaviors such as biting and
chewing (Bock and von Walhert,
1965; Hylander,
1979a; Hylander,
1979b; Wake,
1992; Wainright and Reilly,
1994; Lauder,
1995), there is perhaps one shortcoming of the evidence for
symphyseal fusion based on studies of craniomandibular bone strain and
jaw-adductor muscle activity. Apart from sound theoretical arguments, the best
in vivo support for a functional link between symphyseal stress and
symphyseal fusion is essentially correlational, in linking character-state
variation to the way an adult organism loads, or is posited to load, a
masticatory structure (Ravosa and Hogue,
2004). While this does not invalidate or diminish the unique and
important role of in vivo data for testing hypotheses regarding the
biological role and performance of cranial elements, it does imply that when
evaluating masticatory function during growth or across a clade, presently one
must assume that variation in symphyseal fusion corresponds to specific
differences in jaw-loading and jaw-adductor muscle patterns. Indeed, this gap
in our knowledge has abetted arguments that variation in symphyseal fusion is
unrelated to variation in symphyseal loading levels during mastication, with
an unfused joint being sufficiently strong to routinely counter significant
stresses (Dessem, 1989;
Lieberman and Crompton, 2000).
It follows from such an interpretation that the tissues of an unfused
symphysis would be unresponsive to postnatal variation in long-term,
repetitive loads.
This controversy exists because an integrative biomechanical, cellular and
biochemical analysis of adaptive plasticity heretofore had been applied only
to cranial synovial joints (TMJ) (Bouvier
and Hylander, 1982; Bouvier
and Hylander, 1984; Huang et
al., 2002; Huang et al.,
2003) and syndesmoses (sutures)
(Byron et al., 2004). To this
end, data on tissue plasticity for a cranial arthrosis (rabbit symphysis)
offer a novel perspective on the dynamic inter-relationships among symphyseal
fusion, joint performance and feeding behaviors. In support of prior research
(Hylander, 1979a;
Hylander, 1979b;
Hylander et al., 1998;
Hylander et al., 2000;
Hylander et al., 2005;
Ravosa and Hylander, 1994),
our analyses where both rabbit cohorts used their incisors similarly, but
differed largely in diet-related forces experienced during postcanine chewing
and biting, highlights the significant role of stresses during mastication on
postnatal and phylogenetic variation in symphyseal anatomy across diverse
mammal clades (e.g. Tables 2,
3). Moreover, evidence
regarding functional adaptation in symphyseal proportions, morphology and bony
properties supports the hypothesis that dynamic alterations in masticatory
loads positively influence developmental variation in symphyseal joint
strength, integrity and performance. As argued elsewhere, these findings are
inconsistent with alternative claims that fusion occurs to stiffen, rather
than strengthen, the symphyseal joint during mastication
(Hogue and Ravosa, 2001;
Ravosa and Hogue, 2004).
Conclusion
By selecting similar section/site samples for morphometric, microCT,
immunohistochemical and histological comparisons, our experimental research
facilitated a characterization of the coordinated series of dynamic functional
adaptations as well as the onset of degradative responses of cranial joint
tissues vis-à-vis altered masticatory stresses. Results
suggest that evolutionary variation in symphysis and TMJ morphology, and thus
by inference joint performance, among sister taxa is in part an epiphenomenon
of interspecific differences in (diet-induced) jaw-loading patterns
characterizing the individual ontogenies of the members of a species
(Vinyard and Ravosa, 1998;
Ravosa and Hogue, 2004).
However, this interspecific behavioral signal may be increasingly mitigated
among aging adults by the (potentially species-specific) interplay between
adaptive and degradative tissue responses. Therefore, current and future
research on adaptive plasticity in the skull, and especially joints, should
employ a multifaceted characterization of a given functional network, one that
incorporates data on myriad tissues so as to evaluate the role of altered
loading versus differential tissue response on functional adaptation
of such composite structures. As tissue degradation is the failure of the
adaptive process to adequately respond to altered and/or excessive loading
conditions, this integrative perspective is also fundamental for unraveling
the etiology of joint disease.
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