CURRENT THERAPY

J Oral Maxillofac Surg

61:494-506, 2003

Structure and Function of the

Temporomandibular Joint Disc:
Implications for Tissue Engineering
Michael S. Detamore, BSChE,*
and Kyriacos A. Athanasiou, PhD, PE†

The temporomandibular joint (TMJ) disc is a little understood structure that, unfortunately, exhibits a
plethora of pathologic disorders. Tissue engineering approaches may be warranted to address TMJ disc
pathophysiology, but first a clear understanding of structure-function relationships needs to be devel-
oped, especially as they relate to the regenerative potential of the tissue. In this review, we correlate the
biochemical content of the TMJ disc to its mechanical behavior and discuss what this correlation infers
for tissue engineering studies of the TMJ disc. The disc of the TMJ exhibits a somewhat biconcave shape,
being thicker in the anterior and posterior bands and thinner in the intermediate zone. The disc, which
is certainly an anisotropic and nonhomogeneous tissue, consists almost entirely of type I collagen with
trace amounts of type II and other types. In general, collagen fibers in the intermediate zone appear to
run primarily in an anteroposterior direction and in a ringlike fashion around the periphery. Collagen
orientation is reflected in higher tensile stiffness and strength in the center anteroposteriorly than
mediolaterally and in the anterior and posterior bands than the intermediate zone mediolaterally. Tensile
tests have shown the disc is stiffer and stronger in the direction of the collagen fibers. Elastin fibers in
general appear along the collagen fibers and most likely function in restoring and retaining disc form after
loading. The 2 primary glycosaminoglycans of the disc by far are chondroitin sulfate and dermatan
sulfate, although their distribution is not clear. Compression studies are conflicting, but evidence
suggests the disc is compressively stiffest in the center. Only a few tissue engineering studies of the TMJ
disc have been performed to date. Tissue engineering studies must take advantage of existing information
for experimental design and construct validation, and more research is necessary to characterize the disc
to create a clearer picture of our goals in tissue engineering the TMJ disc.
© 2003 American Association of Oral and Maxillofacial Surgeons
J Oral Maxillofac Surg 61:494-506, 2003

Temporomandibular joint (TMJ) disorders (TMDs) are
multifactorial and complex.1 Epidemiologic surveys
report that 20% to 25% of the population have symp-
toms of a TMD,2 whereas patient studies show that
only 3% to 4% of the population (roughly one fifth of
those who exhibit symptoms) seek treatment.1
Received from the Department of Bioengineering, Rice University,
Houston, TX.
*Graduate Student.
†Professor.
This study was supported by the Whitaker Foundation, Arling-
ton, VA.
Address correspondence and reprint requests to Dr Athanasiou:
Department of Bioengineering, Rice University, 6100 Main, Keck
116, Houston, TX 77005; e-mail: athanasiou@rice.edu
© 2003 American Association of Oral and Maxillofacial Surgeons
0278-2391/03/6104-0018$30.00/0
doi:10.1053/joms.2003.50096
Signs and symptoms of TMD include limited mouth
opening, deviation of the jaw to one side on opening
and closing, clicking, locking, dislocation, and pain in
the masticatory muscles during jaw movement.3 Pain
is reported to be the most common reason for seeking
treatment.1,4,5 TMDs are often accompanied by recur-
rent headaches and neck pain.2,3 With such stagger-
ing numbers from epidemiologic studies and the mag-
nitude of associated signs and symptoms, it is
perplexing that so little is known about the identifi-
cation and correction of TMDs. The reason that the
disc of the TMJ is of particular interest is that, as
reviewed by Farrar and McCarty,6 almost 70% of pa-
tients with TMDs have disc displacement.
In this review, we provide a thorough review of
biochemical and mechanical studies of the TMJ disc in
the literature in an effort to establish a connection
between functional structure and molecular biology.
In addition, we explain how tissue engineers will

494
DETAMORE AND ATHANASIOU
Table 1. WATER CONTENT OF THE TEMPOROMANDIBULAR JOINT DISC
Group Species
Nakano and Scott, 198924 Bovine
Nakano and Scott, 199617 Bovine
Sindelar et al, 200023 Porcine
*All errors are standard deviations.
incorporate this correlation into design and validation
of experiments.
The TMJ Patient Gender Paradox
It is widely known that more women than men are
treated for TMDs. Reports of the female-to-male pa-
tient prevalence vary from 3:1 to 8:1.1,2,7 As reviewed
by Warren and Fried,8 pain onset in TMD patients is
most prevalent in women aged 20 to 40 years. In
contrast to patient populations, Gray et al1 report that
epidemiologic surveys show that the numbers of men
and women with TMDs in the general population are
roughly equal. However, other studies have found
that about 10% to 15% more women than men expe-
rience signs and symptoms.2,3
If there is truly a significant difference between the
number of men and women affected by TMDs, then it
is possible that this difference can be attributed to
reactions of tissues to hormones. In baboons, estro-
gen receptors were found in the TMJ complex of
females but not of males.9,10 In addition, a larger
number of estrogen-positive and progesterone-posi-
tive receptors were found in discs of TMD patients
than in normal discs.11 In contrast, the results of
another study propose that the presence of estrogen
receptors does not contribute to TMDs in humans.7
However, more recent thinking suggests that it is
possible that female sex hormones play a role in pain
transmission,8,12 and because pain is the most com-
mon reason for seeking treatment, women may there-
fore be more likely to seek treatment.
It is possible that the epidemiology of TMDs is
disproportionate and/or that sex hormones may con-
tribute to TMDs, but the only undisputed evidence is
that there is a larger female patient population. What,
then, is the implication for the tissue engineer? The
answer is that it is too early right now to incorporate
gender differences into TMJ design. Further research
is needed in epidemiologic studies to conclusively
determine whether there really is a disproportionate
495
Region Water Content (%)*
Whole 76.5
Center 70.2 ⫾ 0.7
Periphery 66.4 ⫾ 4.9
Medial anterior 80.1 ⫾ 2.6
Lateral anterior 75.1 ⫾ 4.4
Medial intermediate 75.9 ⫾ 2.6
Lateral intermediate 79.3 ⫾ 1.7
Medial posterior 76.6 ⫾ 3.6
Lateral posterior 77.1 ⫾ 3.1
number of males and females in the general popula-
tion afflicted with signs and symptoms of TMDs. If
indeed there is a difference, then certainly further
research is needed to determine what influence gen-
der has on etiology. If and when this information
becomes available, the tissue engineering community
can fine-tune experimental designs to create a suc-
cessful construct that takes into account these gender
differences.
Structure of the Disc
For an introduction to TMJ anatomy, reports by
Dolwick,13 Piette,14 Rees15 and Werner et al16 are
recommended. In this section, we review studies of
the cells and extracellular matrix of the TMJ disc. We
first examine cellular and water content studies and
then discuss studies on collagen orientation and type,
before reviewing glycosaminoglycans (GAGs)/proteo-
glycans and elastin. Data from Nakano and Scott in
199617 (Tables 1 and 2) were provided via personal
communication (P.G. Scott, personal communication,
October, 2001) and represent mature adult specimens.
CELLS OF THE DISC
The cells of the TMJ disc resemble fibrocytes, fibro-
blasts, and fibrochondrocytes, but it would not be
appropriate to refer to these cells as chondro-
cytes.15,18-21 Milam et al20 report that cells of the disc
of the primate TMJ are primarily round chondrocyte-
like cells surrounded by lacunae. It is not known
whether these different cell types are all members of
one cell lineage. Moreover, there are conflicting re-
ports as to which is the predominant cell type. It
appears as though the distribution of cell types is
heterogeneous.21,22 Mills et al21 report that cells,
which are distributed throughout the primate disc,
are of higher density in the anterior and posterior
bands. Scapino et al22 report that cells in the rabbit
disc are relatively more numerous at the junction of
the intermediate zone with the band regions. There
496
are approximately 2.0 ⫻ 107 cells/g of tissue in the
bovine disc.19 In a comparison of bovine cells in
culture, disc cells proliferated approximately 60 times
faster than hyaline chondrocytes and approximately
27 times faster than osteoblasts.19
Berkovitz and Pacy18 characterized the cells of rat
and marmoset TMJ discs. Interestingly, the cytoplasm
of many cells contained microfilaments, giving an
appearance similar to myofibroblasts, which have
contractile properties due to actin filaments. Micro-
filaments in these discs were larger than actin (9 nm
compared with 5 to 7 nm) and thus are regarded as
intermediate filaments. It is probable that the primary
component on a mass basis of these filaments is vi-
mentin, which may have a microskeletal role.
WATER CONTENT
Reported values for water content from bovine and
porcine discs range from 66% to 80%17,23,24; Table 1
summarizes these values. Nakano and Scott17 showed
that water content seems to decrease slightly
with age.
COLLAGEN
The primary purpose of collagen in tissue is to
resist tensile forces. It is therefore important to char-
acterize the organization of collagen fibrils in the TMJ
disc to understand the behavior of the disc under
tension. In the intermediate zone of the disc, collagen
fibers run predominantly anteroposteriorly.22,25-30
These fibers exhibit abundant oblique and lateral
branching25,26,29 and abruptly turn superiorly, inferi-
orly, medially, and laterally as the intermediate zone
merges with the band regions.22,27 Surrounding the
predominantly anteroposteriorly aligned collagen
core of the intermediate zone, the collagen forms a
ringlike structure around the periphery of the
disc.29,30 This suggests that collagen fibers run primar-
ily anteroposteriorly in the medial and lateral re-
gions27 and run mediolaterally in the posterior and
anterior bands.29,30 However, the anterior band actu-
ally exhibits more anteroposterior fibers than medio-
lateral fibers.29 Collagen fibrils have larger diameters
in the periphery than in the center.27,31 Taguchi et al30
speculate that the outer rim may serve to sustain the
shape under tensile and compressive forces.
Collagen fibers appear wavy (undulant or crimped)
in the disc.22,25,27,29,30,32,33 Collagen in the disc is
crimped throughout the full thickness of the disc.32
The mean periodicity of this crimping has been re-
ported from 8 to 15 ␮m30 and from 15 to 23
␮m.22,32,33 Scanning electron microscopy of the rhe-
sus monkey disc revealed that the collagen fibers
were wavier and more numerous at the inferior sur-
face than at the superior surface, where the waviness
was diminished.30
TMJ DISC STRUCTURE, FUNCTION, AND REGENERATION
The collagen types identified in the TMJ disc hereto-
fore are I, II, III, VI, IX, and XII.19-21,34-39 Collagen in the
disc is almost entirely composed of type I collagen.20,21
Types II19-21,35 and III19,34,36-39 collagens are likely
present in trace amounts, as some studies detected them
but others did not. Types II and III collagen are likely
located primarily in the immediate vicinity of the cells.
Types VI, IX, and XII are likely present in very small
amounts.19,38 Further research is needed to quantify the
amounts of each of these types of collagen, especially of
types II and III. For those evaluating tissue engineered
constructs, it is important that it be understood that the
collagen in the TMJ disc is different from hyaline carti-
lage—primarily meaning that only looking for type II
collagen will serve no purpose. The collagen of the ideal
tissue-engineered disc construct will be almost entirely
type I.
GLYCOSAMINOGLYCANS AND PROTEOGLYCANS
Glycosaminoglycans
The GAG content of the TMJ disc lies between that
of hyaline cartilage and tendon and is more similar to
that of fibrocartilages like the knee meniscus.40 In
rabbits, the total GAG content in the disc is about 10%
of that in hyaline cartilage.40 Bovine TMJ disc cells
synthesize sulfated GAGs at a rate approximately 17
times slower than articular chondrocytes.19
The actual distribution of GAGs in the disc is not
clear. Kopp41 observed more sulfated GAGs in the
central region than in the anterior and posterior re-
gions but did not find a significant difference between
medial and lateral sides. Nakano and Scott17 reported
that GAGs are more concentrated in the center of the
disc than in the periphery, which appears to be in
agreement with Kopp.41 In contrast, Mills et al21 re-
port that sulfated GAGs are present in greater
amounts in the posterior band than in the anterior
band of the primate TMJ disc and to a much lesser
extent in the intermediate zone, a distribution in
direct opposition to that observed by Kopp41 and
Nakano and Scott.17 GAGs have been found primarily
in the pericellular matrix surrounding the cells.20,21,42
It is well established that dermatan sulfate and
chondroitin sulfate are the primary GAGs of the disc,
although there is controversy as to which of these 2 is
the primary GAG.17,24,40,43,44 Axelsson et al40,44 re-
ported from work with normal human discs that
chondroitin and dermatan sulfate collectively account
for 90% of the total GAG content in the anterior part
(including the intermediate zone) and 84% in the
posterior part. Hyaluronic acid is likely the next most
abundant GAG, which has ranged in reports from
5% to 20% of the total GAG content.17,24,40,43,44 Kera-
tan sulfate17,24,40,43,44 and heparan sulfate40,43,44 are
present in trace amounts.
 Table 2. QUANTIFIED EXTRACELLULAR MATRIX COMPONENTS IN THE TEMPOROMANDIBULAR JOINT DISC
DETAMORE AND ATHANASIOU

Male/ Dry/Wet
Group Component Region Amount (mg/g) Female Species Weight Diseased? Method

Gage et al, 199525 Total collagen Anterior attachment 365 ⫾ 18 Both Human Wet Yes Electrophoresis
Medial attachment 372 ⫾ 18
Lateral attachment 360 ⫾ 17
Posterior attachment 368 ⫾ 21
Posterior band 334 ⫾ 6
Anterior band 342 ⫾ 10
Gage et al, 199034 Total collagen Posterior attachment 377 ⫾ 21 Both Human Wet No Electrophoresis
Lateral attachment 372 ⫾ 18
Disc 304 ⫾ 5
Sindelar et al, Total GAG Disc (AM) 121.7 ⫾ 26.0 Female Porcine Dry No Histologic staining/
200023 Disc (AL) 82.6 ⫾ 10.6 absorbance
Disc (IM) 104.1 ⫾ 27.2
Disc (IL) 144.6 ⫾ 39.7
Disc (PM) 83.1 ⫾ 13.7
Disc (PL) 72.7 ⫾ 11.6
Nakano and Scott, Hyaluronic acid Disc center 2.1 ⫾ 0.7 NS Bovine Dry No Electrophoresis
199617 Disc periphery 1.1 ⫾ 0.3
Dermatan sulfate Disc center 9.4 ⫾ 1.5 Iduronic acid
Disc periphery 4.3 ⫾ 0.5 content
Chondroitin sulfate Disc center 27.0 ⫾ 7.3 Glucuronic acid
Disc periphery 2.7 ⫾ 1.1 content
Keratan sulfate Disc center 9.52 ⫾ 3.26 Inhibition ELISA
Disc periphery 0.0218 ⫾ 0.0092
497
 498

Table 2. QUANTIFIED EXTRACELLULAR MATRIX COMPONENTS IN THE TEMPOROMANDIBULAR JOINT DISC (Cont’d)

Male/ Dry/Wet
Group Component Region Amount (mg/g) Female Species Weight Diseased? Method

Okazaki et al, GAG (as Disc 3.24 Female Rat Dry No Electrophoresis
199643 glucuronic acid)
Axelsson et al, GAG* Anterior ⫹ intermediate 5.4 ⫾ 1.0 Both Human Dry No HPLC
1992†40 posterior 6.2 ⫾ 1.0
CS ⫹ DS* Anterior ⫹ intermediate 4.7 ⫾ 1.1
posterior 5.2 ⫾ 0.8
Hyaluronic acid* Anterior ⫹ intermediate 0.5 ⫾ 0.2
posterior 0.7 ⫾ 0.4
Heparan sulfate* Anterior ⫹ intermediate 0.2 ⫾ 0.2
posterior 0.3 ⫾ 0.2
Keratan sulfate* Anterior ⫹ intermediate ⬍0.01
posterior ⬍0.01
Nakano and Scott, Total GAG Anterior ⫹ intermediate 50 NS Bovine Dry No Ion-exchange
198924 Chondroitin sulfate 39.5 chromatography
Dermatan sulfate 7
Hyaluronic acid 2.5
Keratan sulfate 1
Gross et al, Elastic fibers Disc and bilaminar zone 0.339 ⫾ 0.060% v/v Female Human Wet Yes Histologic staining/
199954 computer imaging
O’Dell et al, Elastic fibers Disc 21 ⫾ 3/13 ⫾ 3 Female Hamster Dry No Radioimmunoassay
199050
Keith, 197952 Elastin Disc 30-70 NS Bovine Dry No Extraction
NOTE. Abbreviations: GAG, glycosaminoglycan; CS, chondroitin sulfate; DS, dermatan sulfate; ELISA, enzyme-linked immunosorbent assay; HPLC, high-performance liquid chromatography; NS, not
specified.
*mg hexosamine/g dry weight.
All errors are SDs except † not specified.
TMJ DISC STRUCTURE, FUNCTION, AND REGENERATION
DETAMORE AND ATHANASIOU 499

Table 3. TENSILE PROPERTIES OF THE TEMPOROMANDIBULAR JOINT DISC

Ultimate
Modulus of Tensile Strain
Elasticity Strength Equilibrium Rate
Group* Direction Region (MPa) (MPa) Modulus? (mm/min) Species Male/Female

Beatty et al, 200162 Mediolateral Center 3.2 ⫾ 0.4 1.6 ⫾ 0.2 No 500 Porcine NS
76.4 ⫾ 3.3 37.4 ⫾ 1.8
27.3 -- 0.5
Tanaka et al, 200160 Anteroposterior Medial 25.9 ⫾ 2.6 -- No 62.4 Bovine Female
Central 22.9 ⫾ 3.1
Lateral 24.0 ⫾ 2.6
Tanne et al, 199159 Anteroposterior Medial 91.9 ⫾ 10.4 -- No 0.1 N/s Dog NS
Middle 101.1 ⫾ 22.5
Lateral 83.7 ⫾ 16.0
Shengyi et al, Mediolateral Anterior band 30 46.7 ⫾ 17.2 Yes NS Dog Both
199161 Posterior band 30.1 69.7 ⫾ 30.8
Intermediate zone 18.4 14.7 ⫾ 5.9

Abbreviation: NS, not specified.

*All errors are SDs, except Beatty et al report SEMs.

Proteoglycans branched elastic fibers of mean diameter 0.5 ␮m run-

The large chondroitin sulfate proteoglycan (CSPG)
of the TMJ disc is similar to aggrecan with respect to
its amino acid composition and tendency to aggregate
with hyaluronic acid,17 as well as its inclusion of
keratan sulfate.45 This proteoglycan has a high molec-
ular weight (⬎106 Da) and is predominantly chon-
droitin-6-sulfate.45 In the bovine disc, the ratio of wide
to narrow filaments of CSPGs is higher in the center
(79:21) than in the periphery (27:73).31 Immunohis-
tochemical studies for CSPG with the rat disc showed
weak staining in the intermediate zone and more
intense staining toward the periphery, especially at
the boundary between the anterior band and
attachment.46
Dermatan sulfate proteoglycans (DSPGs) are a
group of small proteoglycans that include biglycan
(DS-PGI) and decorin (DS-PGII).47,48 DSPGs have been
discovered in bovine discs.49 Immunohistochemical
investigation of the rat disc revealed weak and fairly
even staining for biglycan throughout the disc, al-
though the most intense staining was in the posterior
band.46 Decorin staining was most intense at the an-
terior and posterior junctions between the band and
attachment and was more intense in the peripheral
region than in the central region. Moreover, the an-
terior band contained more decorin than the poste-
rior band and the superior surface more than the
inferior surface. Decorin was virtually absent from the
intermediate zone and the central part of the poste-
rior band.
ELASTIN
Elastic fibers (elastin) generally run along, in be-
tween, and parallel to the collagen fibers of the
disc.26,36,50-53 Keith52 observed straight, thin, un-
ning predominantly anteroposteriorly but occasion-
ally mediolaterally and superoinferiorly. Reports of
elastin content range from 0.339%54 to 3% to 7%52
(Table 2). Elastic fiber distribution is inhomoge-
neous.50,51,54,55 The superior layer of the disc contains
more elastic fibers than the inferior layer by a ratio of
about 60% to 40% overall,54 and the number of elastic
fibers increases dramatically from the center toward
the periphery.50,54,55 Elastic fibers are more dense in
the bilaminar zone than in the disc itself.51,54
Mechanical Functional Characteristics
of the Disc
The TMJ disc is a viscoelastic material,56,57 meaning
that its stress profile depends on its strain history, and
its mechanical behavior is characterized by hysteresis,
stress relaxation, and creep.58 In this section, we
examine the behavior of the disc under tension and
compression to identify regional and directional vari-
ation in its functional mechanical properties. The
studies characterizing this behavior vary greatly in
their methods—whether the tissue was hydrated,
whether specimens were stressed incrementally to
obtain a relaxed modulus, different species, different
temperatures, different strain rates, and different gen-
ders—and thus for our purposes it better serves to
compare results within individual studies than to
make comparisons between different studies. There-
fore, we limit our review to studies that tested the
disc in different locations or directions and studies
that examined biochemical changes under loading.
Values obtained from tension tests are summarized in
Table 3, and values obtained from compression tests
are summarized in Table 4. It would be appropriate to
500 TMJ DISC STRUCTURE, FUNCTION, AND REGENERATION

Table 4. COMPRESSIVE PROPERTIES OF THE TEMPOROMANDIBULAR JOINT DISC

Modulus of Equilibrium
Group Region Elasticity† Modulus? Species Male/Female

Kim et al, 2002 64 Anterior (superior) 18.8 ⫾ 4.7 kPa Yes Porcine Female
Anterior (inferior) 16.3 ⫾ 4.8 kPa
Central (superior) 18.6 ⫾ 5.2 kPa
Central (inferior) 15.3 ⫾ 3.6 kPa
Lateral (superior) 16.3 ⫾ 2.1 kPa
Lateral (inferior) 12.8 ⫾ 5.3 kPa
Medial (superior) 28.9 ⫾ 12.3 kPa
Medial (inferior) 23.0 ⫾ 10.1 kPa
Posterior (superior) 22.1 ⫾ 6.5 kPa
Posterior (inferior) 14.8 ⫾ 4.9 kPa
Beek et al, 200163 Posterior 20 MPa No Human Not specified
Intermediate zone 60 MPa
Anterior 30 MPa
*All errors are standard deviations.

quickly define a few terms at this point. The modulus
is a property of a material that characterizes its stiff-
ness; it can be obtained from the material’s stress
(force divided by cross-sectional area) versus strain
(deformation divided by initial length) plot as the
slope of the linear portion of the curve. The modulus
can be obtained from both tension and compression
testing. The ultimate tensile strength (UTS) is simply
the maximum stress the material can withstand be-
fore failure in a tensile test. Poisson’s ratio is a mea-
sure of compressibility, relating the lateral strain to
longitudinal strain. Values from Poisson’s ratio range
from 0 to 0.5, tending toward incompressibility
near 0.5.
TENSION
Tanne et al59 tested regional tensile variations in
canine discs. The medial, middle, and lateral parts of
the disc were examined in the anteroposterior direc-
tion. The stress-strain curve obtained here was in the
nonlinear “toe”58 region (maximum stress of 3.5
MPa), so the elastic modulus was approximated by
performing a linear regression of stress-strain data for
the range 1.5 to 3.5 MPa. The middle region had the
highest elastic modulus, followed by the medial and
lateral regions, respectively. The difference between
the middle region and lateral region moduli was sta-
tistically significant, but the modulus of the medial
region was not significantly different from either of
the other 2. In a more recent study by the same
group, tensile testing was performed in the antero-
posterior direction on bovine discs.60 Specimens from
the same 3 regions were immersed in saline and
exposed to a step stress of 1.0 or 1.5 MPa, and the
modulus was obtained by dividing the stress by the
resulting strain after 1 second. The modulus was high-
est in the medial region and lowest in the central
region, with the difference between these regions
being significant.
Shengyi et al61 examined regional tensile variations
in the mediolateral direction in canine discs, compar-
ing the anterior band, intermediate zone, and poste-
rior band. Both equilibrium modulus and UTS were
obtained. The UTS of the anterior and posterior bands
was significantly higher than the intermediate zone,
but the difference between the anterior and posterior
bands was not significant. The equilibrium moduli of
the anterior and posterior bands were almost identi-
cal, and they were both significantly higher than the
elastic modulus of the intermediate zone.
Beatty et al62 tested the center of the porcine disc
under tension in the anteroposterior and mediolateral
directions. Discs were loaded at continuous displace-
ment rates of 0.5, 50, and 500 mm/min. Variation in
strain rate had little effect on tensile data in the
mediolateral direction; however, this variation had a
marked affect in the anteroposterior direction. At 500
mm/min, the elastic modulus and UTS in the antero-
posterior direction were both more than 20 times
what they were in the mediolateral direction.
COMPRESSION
Beek et al63 examined seven human discs under
compression at the anterior band, intermediate zone,
and posterior band. The discs were compressed be-
tween 2 flat-faced cylinders of diameter 3.94 mm.
They reported that the modulus of the intermediate
zone was approximately 2 and 3 times the modulus of
the anterior and posterior bands, respectively. How-
ever, locations on the disc were varied in the medio-
lateral direction, which may have resulted in slightly
skewed results. They speculated that fluid flow is
directed primarily anteroposteriorly through the disc
DETAMORE AND ATHANASIOU
under compressive load under the guidance of colla-
gen fibers.
In our group—in ongoing experiments and in Kim
et al64—we obtained compressive mechanical prop-
erties of the porcine disc in different regions via
indentation and finite element modeling with equa-
tions of biphasic theory. The disc was examined at 5
sites each on both the superior and inferior surfaces:
anterior, posterior, central, medial, and lateral. Values
were reported for thickness, recovery, creep, elastic
modulus, Poisson’s ratio, and permeability. Values
obtained for the elastic modulus are listed in Table 4.
Interestingly, the elastic modulus measured at the
medial site was much larger than that at the lateral
site. Moduli were higher on the superior side, most
noticeably in the posterior band. The modulus of the
central region did not appear to be higher than any
other site with the possible exception of the lateral
region. Values for Poisson’s ratio ranged from 0.014
to 0.068. Permeability ranged from 15 ⫻ 10⫺15 to
87 ⫻ 10⫺15 m4/N/s, appearing to be much higher on
the inferior side than on the superior side.
Nickel and McLachlan65 examined the porcine disc
under compression. Ten indenters were placed on
the superior surface of the intermediate zone of the
disc across the mediolateral axis. They found that the
peak stresses were higher in the central zone than in
the medial and lateral regions. In addition, they ob-
served higher peak stresses in thicker discs.
The following 2 studies examined the effects of
compression on ultrastructure or biochemical activi-
ties. Scapino et al22 loaded the rabbit disc under com-
pression using 4.8-mm-diameter stainless-steel balls
on the superior and inferior surfaces, which resulted
in significant compression in the intermediate zone
and reduction in collagen crimping but very little
change in general collagen fiber alignment. Carvalho
et al66 report that loading the rat disc under dynamic
compression via a vacuum-controlled membrane re-
sulted in a significant increase in chondroitin-6-sulfate
synthesis, a slight decrease in hyaluronic acid synthe-
sis, and no change in dermatan sulfate synthesis.
These discs were loaded at 25%, 75%, and 100% of the
time, and whereas chondroitin-6-sulfate synthesis was
significantly higher in the 75% and 100% groups com-
pared with both the 25% and unloaded controls, syn-
thesis in the 25% group was not significantly higher
than in the unloaded controls.
In a 3-dimensional finite element model of the hu-
man disc, static loading at the closed jaw position
predicted loading was primarily located in the inter-
mediate zone with higher values toward the lateral
side.67 In this model, finite deformation theory was
used to calculate Cauchy stresses and logarithmic
strains. The elastic modulus was varied from 8 to 80
MPa, and Poisson’s ratio was assumed to be 0.30 or
501
0.47. At the time of this study, reports on the elastic
modulus were extremely scarce and information on
regional variation of the compressive elastic modulus
was not available. Furthermore, empirical data for the
Poisson’s ratio had not yet been obtained. The disc
was assumed to be linearly elastic and initial loads
were assumed to be zero. Friction, deformation of the
surfaces of the condyle and fossa-eminence, and disc
attachments were neglected. As reviewed by Mizogu-
chi et al,46 other finite element studies have suggested
that the central region of the disc is mainly subjected
to compression and the peripheral region is subjected
to tension.
Identification of Structure-Function
Relationships
In this section, we identify relationships between
the biochemical organization and observed mechani-
cal properties. We first review collagen orientation
and its implication on tensile properties. We then
explore how GAG and proteoglycan distributions may
be manifested in observed mechanical, especially
compressive, properties.
Collagen fibers are known to contribute to resisting
tensile forces. Therefore, we expect that the disc will
behave anisotropically under tension due to its inho-
mogeneous collagen distribution. We expect that seg-
ments taken from the disc will be stiffer and stronger,
that is, have a higher Young’s modulus and tensile
strength, when pulled in the direction of the collagen
fibers. We can draw from the aforementioned studies
on collagen orientation and distribution to make pre-
dictions as to how the disc will behave under tension.
First, we expect the disc to be stiffer and stronger in
the anteroposterior direction than in the mediolateral
direction in the intermediate zone. We also expect
higher values for the modulus and tensile strength in
the mediolateral direction in the posterior band than
in the anterior band, which in turn we expect to be
higher than in the intermediate zone. Anteroposteri-
orly, it is not clear from collagen orientation studies
how to interpret the medial, central, and lateral sec-
tions in terms of tensile characteristics. In addition,
the presence of crimping needs to be considered
when interpreting responses of the disc to tensile
loading.32,56,59,68,69 Collagen crimping results in the
initial “toe” region observed in tensile stress-strain
curves, as reviewed by Berkovitz.32,33 The low-strain
toe region is of exponential character, followed at
higher strains by a linear portion of the stress-strain
curve.
Results from tension tests correlate well with what
we expect based on collagen fiber orientation. Due to
the predominantly anteroposterior fibers through the
intermediate zone, we expect the disc to be stiffer
502
and stronger in the anteroposterior direction than in
the mediolateral direction in the center of the disc,
which is exactly what was observed by Beatty et al.62
In the mediolateral direction, we expect the disc to
be much stronger and stiffer in the posterior and
anterior bands than in the intermediate zone and for
the posterior band to be only slightly stronger and
stiffer than the anterior band, all due to the peripheral
collagen ring and central anteroposterior fibers that
extend somewhat into the anterior band. This is es-
sentially what Shengyi et al61 observed in their exper-
iments, as the anterior and posterior bands were in-
deed stronger and stiffer than the intermediate zone
and similar to each other, with the posterior band
being slightly stronger than the anterior band. It was
difficult to make a strong prediction for anteroposte-
rior tension, as the anteroposterior fibers of the pe-
ripheral ring are weighed against the central antero-
posterior core. As Tanne et al59 observed, the disc was
stiffer in the center than laterally, but overall there
were no especially dramatic differences. These exper-
imental results may suggest a higher number of colla-
gen fibers or a higher degree of anteroposterior orga-
nization of collagen fibers in the center of the disc or
may simply reflect specimen preparation. However,
Tanaka et al60 found the central region to be the least
stiff, which would suggest otherwise. Further re-
search is necessary to better elucidate this relation-
ship for anteroposterior tension.
Elastic fibers are small in number in the disc and are
not likely to contribute sufficiently to tensile
strength21 or more generally to the load-bearing prop-
erties of the disc.22 As reviewed by Scapino et al,22
elastic fibers provide little resistance to elongation
even up to 50% strain. Instead, elastic fibers are prob-
ably more important in restoring and retaining resting
disc form and position after loading.21,55 Therefore,
elastin content likely does not manifest itself in tradi-
tional mechanical properties, such as the modulus or
tensile strength, but rather may serve as an indicator
of disc regions more prone to stretching and recovery
during jaw movement.
It is widely known that aggrecan, which is similar
to the CSPG of the TMJ disc, contributes to the com-
pressive strength of articular hyaline cartilage. By
analogy, we assume that CSPG contributes to the
compressive strength of the disc. Therefore, we ex-
pect regions of higher CSPG (or simply chondroitin
sulfate GAG) concentration to have a higher compres-
sive modulus. In the bovine disc, the ratio of wide to
thin CSPG filaments was approximately 3 times
higher in the center than in the periphery.31 From
Nakano and Scott17 in Table 2, we see that chon-
droitin sulfate GAG in the bovine disc is an order of
magnitude more concentrated in the center than the
periphery. In the rat, CSPG was more concentrated in
TMJ DISC STRUCTURE, FUNCTION, AND REGENERATION
the periphery than in the intermediate zone.46 The
bovine study suggests the disc is stiffer under com-
pression in the center, whereas the rat study suggests
that the disc is stiffer under compression in the pe-
riphery. One might assume that the bovine model
better represents humans, but nonetheless it is clear
that there is a real dearth of data regarding the topo-
graphic distribution of chondroitin sulfate GAG and
CSPG.
A function of DSPGs may be to increase collagen
fibril diameters to create a higher resistance to ten-
sion, as suggested by the following studies. Poole et
al70 suggest that decorin is intimately associated with
collagen fibrils. Danielson et al71 concluded that
decorin plays a fundamental role in regulating colla-
gen fiber formation, after observing markedly reduced
tensile strength of skin and altered collagen morphol-
ogy, including significant changes in collagen fibril
mass and coarser and irregular fiber outlines in
decorin-deficient mice. Scott et al48 found that the
median diameter of collagen type I fibrils was 50% to
60% greater when formed in the presence of biglycan
than in its absence and that biglycan did not cause
significant inhibition of collagen fibrillogenesis. Kuc
and Scott47 report that collagen fibrils formed in vitro
in the presence of decorin from the TMJ disc had
larger diameters than controls: 63 nm versus 40 nm.
However, collagen fibrillogenesis was reduced at least
2-fold by the inclusion of decorin. An important dif-
ference to note between CSPG and DSPG is that
CSPGs have several GAG side chains whereas DSPGs
have only 1 (decorin) or 2 (biglycan). This is signifi-
cant because the ability of CSPGs to resist compres-
sion resides in its several highly negatively charged
GAG chains that trap water. DSPGs by design do not
offer the same level of compressive resistance and
may rely more on the biological activity of the protein
than the mechanical influence of the GAG side chain.
Another significant implication is that measurement
of total proteoglycan content or sulfated GAG content
may not be as effective in assessing the compressive
strength of the TMJ disc as it is in hyaline cartilage,
where the primary proteoglycan is aggrecan. With
such a large fraction of dermatan sulfate, whose pro-
teoglycan may not contribute to compressive
strength, it is preferable to replace total proteoglycan
and sulfated GAG content assays with CSPG and chon-
droitin sulfate GAG assays in drawing parallels be-
tween biochemical content and compressive strength
in the TMJ disc.
If dermatan sulfate does indeed function to increase
tensile strength, then we would expect regions
higher in DSPG (or simply dermatan sulfate GAG)
concentration to be stronger and stiffer under ten-
sion. DSPG data for the rat show that the anterior and
posterior junctions between the band and attachment
DETAMORE AND ATHANASIOU
contain much more DSPG than the intermediate zone.
However, from Nakano and Scott17 in Table 2, we see
that dermatan sulfate in the bovine disc is approxi-
mately twice as abundant in the center than in the
periphery. We make the same observations as with
chondroitin sulfate. We again assume that the bovine
model more closely resembles humans and acknowl-
edge the dearth of data regarding dermatan sulfate
distribution. Another role of dermatan sulfate may be
to regulate growth factors because dermatan sulfate
has been shown to be a strong promoter of basic
fibroblast growth factor-2 (bFGF-2) function,72 a
widely used growth factor in tissue engineering ef-
forts. Therefore, DSPG may have another indirect
effect on mechanical behavior, modulated through
bFGF-2.
Correlating compression data to biochemical con-
tent is not as straightforward as tensile correlations.
The results obtained by Carvalho et al66 support the
notion that chondroitin sulfate is involved in com-
pression and dermatan sulfate is not. However, we
have contradictory information regarding the chon-
droitin sulfate distribution in the disc. If we assume
that the bovine study provides a better model than
the rat study, then we would say that there is a much
higher concentration of chondroitin sulfate in the
center of the disc than the periphery. The results of
Beek et al63 and Nickel and McLachlan65 directly sup-
port this assumption showing higher compressive
moduli in the center than the medial, lateral, anterior,
and posterior regions. In addition, finite element stud-
ies have identified the center of the disc as being
primarily subjected to compression. In contrast, Kim
et al64 report that it is the medial region and, to a
certain extent, the posterior region that is stiffest.
There is more evidence suggesting that the central
region of the disc is the stiffest under compression,
but further research on chondroitin sulfate/CSPG dis-
tribution and the variation of compressive properties
by location is needed before any comprehensive state-
ments can be made here.
In summary, collagen orientation studies provide a
good idea of what to expect from tensile studies, but
the lack of information on topographic distribution of
chondroitin sulfate and dermatan sulfate prevents us
from reaching any meaningful predictions, notably on
compressive behavior. More studies need to be per-
formed to describe how these 2 GAGs are distributed
in the TMJ disc. We have the understanding that the
disc is both inhomogeneous and anisotropic. Further-
more, we understand that the disc functions under
compression and under tension. However, it is not
entirely clear how tensile forces and compressive
forces are related. Scapino et al22 found that compres-
sion reduced crimping but insignificantly changed
collagen fiber alignment, suggesting that compression
503
does indeed alter the tensile behavior of the disc.
Indeed, the disc is subjected to many different forces
in a complex manner. This complex integration of
compressive, tensile, and even shear forces is key in
the development of the observed biochemical con-
tent and organization, which in turn define the ob-
served mechanical properties.
Tissue Engineering Implications
It is absolutely vital that researchers attempting to
tissue engineer the TMJ disc are aware of the bio-
chemical, mechanical, and cellular characterization
studies that have been performed before delving into
their experiments. These characterization studies are
quite literally the design criteria of our engineering
efforts. A tissue engineer oblivious to these character-
ization studies working to design a TMJ disc is analo-
gous to a civil engineer designing a bridge without
knowing the number of lanes or the length and
weight requirements. However, characterization stud-
ies, while plentiful, are often contradictory and leave
a lot of uncertainty in the engineers’ design criteria.
Therefore, although general guidelines and under-
standing have been established, more research will be
necessary to create a true “gold standard” for tissue
engineers.
Although tissue engineering as a field is maturing
and progressing in great strides, tissue engineering of
the TMJ structures is in its extreme infancy. We are
aware of only a few tissue engineering studies perti-
nent to the TMJ. Moreover, we are not aware of any
such studies that have drawn on knowledge of TMJ
structures at the biochemical, cellular, or mechanical
level. The earliest such study was performed by
Thomas et al,73 who cultured rabbit disc cells in
collagen I meshes. Puelacher et al74 later engineered
hyaline cartilage in the shape of a human TMJ disc.
Four years later, Girdler75 cultured condylar cartilage
cells as an effort to approximate the disc, where he
likely harvested many hyaline cartilage cells along
with chondroprogenitor cells. Recently, Springer et
al76 cultured human and porcine disc cells and cul-
tured them in 2 dimensions on expanded polytetra-
fluoroethylene monofilaments, polyglycolic acid
monofilaments, polyamide monofilaments, and natu-
ral bone mineral blocks.
In only 2 of these 4 studies were cells actually
harvested from the disc, and none of these studies
capitalized on the details of structure and function
reviewed here. Three of these 4 studies tested only
for type II collagen, a common practice in hyaline
cartilage tissue engineering studies. However, testing
for and finding type II collagen do not really mean
anything with the TMJ disc unless there is a great deal
of it, in which case the tissue is most likely too
504
hyaline-like. From this type of error, the need for
understanding the composition of the native disc for
validation becomes clear. If we do not know what the
disc is made of, then how do we know whether we
have made a disc? A thorough tissue engineering
study would characterize the collagen, chondroitin
sulfate (or CSPG), and dermatan sulfate (or DSPG)
content and distribution in addition to obtaining me-
chanical properties and characterizing the cells as a
validation. Collagen, chondroitin sulfate, and derma-
tan sulfate should be examined because they are the
primary components of the extracellular matrix and
are known to contribute to the mechanical perfor-
mance. A more thorough validation would even in-
clude elastin, which contributes to restoration of
form after loading, and even other GAGs such as
hyaluronic acid and keratan sulfate. Mechanical stud-
ies should quantify the tensile modulus and strength
in different locations and directions (anteroposterior
and mediolateral) and the compressive modulus in
different locations (medial, lateral, central, anterior,
and posterior). Requirements for cellular characteriza-
tion are less clear, as we do not know whether the
different cell types are distributed homogeneously or
are of the same lineage.
In addition to validation, tissue engineering studies
must look to the structure and function of the disc for
more strategic design of experiments. Future research
is needed to determine whether the different cell
types are distributed homogeneously and whether
they are of the same lineage. From this information,
we may determine that it is necessary to culture the
subpopulations of cells separately and combine them,
or we may just be able to culture the cells in a mixed
fashion. We may find that cell-scaffold constructs cul-
tured in the absence of mechanical forces meet our
validation requirements, as is done in the tissue engi-
neering of skin, and form a functional disc. On the
other hand, we may find that application of mechan-
ical forces is a requirement, as with tissue-engineered
hyaline cartilage. In the case that we must apply
mechanical forces, we draw from the knowledge that
the disc functions under both compression and ten-
sion in designing bioreactors. We would need to de-
sign bioreactors such that we can regenerate the
architecture of the extracellular matrix of the disc.
Structurally, the disc exhibits properties that differ
from location to location and as a function of direc-
tion. The disc of the TMJ has a fairly well character-
ized collagen network, and tensile studies to date
have correlated well with the orientation of the col-
lagen fibers. The distribution of GAGs and proteogly-
cans has not been well characterized, but it is known
that chondroitin and dermatan sulfates are the pri-
mary GAGs. In addition, it has been suggested that the
large CSPG functions in compression, whereas the
TMJ DISC STRUCTURE, FUNCTION, AND REGENERATION
DSPGs function in tension by modulating collagen.
Compression studies are not in agreement, but so far
there is more evidence suggesting that the disc is
stiffer under compression in the center. Tissue engi-
neering studies should draw from this body of knowl-
edge of the structure and function of the disc to
strategically design experiments and validate engi-
neered constructs.
We need to better understand the topographic dis-
tribution of GAGs and collagen types. Tissue engi-
neers will need to know which growth factors and
scaffolds have desirable effects on the cells of the disc
and which scaffolds will be most suitable for biocom-
patibility and the mechanical requirements of the
disc.
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