Development and distribution of elastic fibers in the mandibular joint of the mouse. A comparison of fetal suckling juvenile and adult stages

Development and Distribution of Elastic Fibers
in the Mandibular Joint of the Mouse
A COMPARISON OF FETAL, SUCKLING, JUVENILE
AND ADULT STAGES
'
JACK FROMMER AND CLYDE W. MONROE
Department of Anatomy, Tufts University Schools of Medicine and
Dental Medicine, Boston, Massachusetts
Development and distribution of elastic fibers were studied in mandibular joints of white Swiss mice which ranged from 15 days insemination age to three
months postnatal. Paraffin sections were stained with Weigert's resorcin-fuchsin and
Verhoeffs elastic tissue stain.
Elastogenesis does not begin until the major elements of the mandibular joint are
present. The &st distinct elastic elements appear as granules at the nineteenth to
twentieth day insemination age. Early sites of elastogenesis occur in the peripheral
portions of the articular disk, at the transition and continuation of fibrous disk tissue
with the periarticular tissues, and with the periosteum around the neck of the
mandible.
The concentration, length and caliber of fibers is increased markedly during the
suckling stage, especially in the walls of the medial and lateral recesses of the synovial cavities, and in the posterior continuation of the disk to form a fibroelastic band
of attachment to the squamosal bone. Prominent bands of long elastic fibers appear
in the epimysium of the lateral pterygoid and masseter muscles in the young adult.
The central portion of the disk and the articular surfaces of the mandibular
condyle and fossa contain no elastic fibers, confirming the contention that these
surfaces are not particularly stress-bearing. Stretch and shearing stresses are created,
however, which require extensive elastic fiber development in other joint tissues.
ABSTRACT
Numerous reports on the properties and
age changes of elastic fiber components
of arterial walls have resulted from a considerable interest in the etiology of vascular hypertension, but the elastic fibers
found in joint tissues have received relatively little attention. While the function
of elastic arteries remains essentially the
same throughout developmental stages, the
type and degree of movement in the compartments of the mandibular joint change
according to the functional requirements
of fetal, suckling, and masticatory stages.
The successful fulfillment of these requirements depends largely upon the response
of elastic fibers to compression, stretch
and shearing stresses.
The time of appearance, complete areas
of distribution, and structural and functional age changes of elastic fibers in
mandibular joint tissues are not well understood. Rees ('54), in a description of
the articular disk and its role in the function of the human temporomandibular
ANAT. REC.. 156: 333-346.
joint, reported the presence of elastic
tissue in the region of the bilaminar posterior attachment only. He stated that the
upper (temporal) stratum is composed of
loose fibroelastic tissue, while the lower
(mandibular) stratum is composed chiefly
of white fibrous tissue and contains relatively few elastic fibers. He noted that
when the mouth is opened the forward
excursion of the disk is limited by the degree of stretching of its posterior fibroelastic temporal attachment. Dixon ('62)
also reported that the upper zone of the
posterior part of the human disk contains
a considerable amount of elastic itssue.
He agreed with Rees that this band of
elastic tissue may play an important part
in retrusive movements of the disk during
jaw closure. Griffin and Sharpe ('62), relating the distribution of elastic fibers in
the human temporomandibular meniscus
1 Supported by grant DE 01578-03.from the Nationftl
Institute of Dental Research, United States Public
Health Service.
333
334
JACK FROMMER AND CLYDE W. MONROE
to compression and stress areas, observed
that thick oriented elastic fibers are usually confined to the superior stratum of
the posterior bilaminar zone and the lateral margin of the meniscus. They noted
that randomly distributed elastic fibers in
other portions of the disk would impart
the property of resiliency in an otherwise
non-resilient fibrous tissue. Miles and
Dawson (’62) observed abundant elastic
fibers in the articular fibrous tissue covering the bony surfaces of the temporomandibular joint of man and several other
species. Since the hyaline cartilage covering the bony surfaces of most joints is
lacking here, they suggested that the
elastic fibers provide the resilience which
would otherwise be provided by the high
chondroitin sulphate content of articular
cartilage.
It is the purpose of the present study to
describe the appearance and distribution
of elastic fibers in normal mandibular
joint tissues of mice at different ages, and
to discuss the functional significance of
the age changes.
MATERIALS AND METHODS
Twelve white Swiss female mice were
bred and sacrificed for removal of fetuses
at insemination ages of 15 to 20 days. In
addition, two postnatal mice were sacrificed daily throughout the first week and
at weekly intervals thereafter until the
age of three months. The heads were fixed
in 10% formalin or Zenker’s fluid. For
decalcification, which became necessary
at about four days postnatal, 5% tricholoroacetic acid was used. Paraffinembedded tissues were sectioned serially
in frontal and sagittal planes at 5-10 u.
Sections were stained with either Verhoeffs elastic tissue stain, Weigert’s resorcin-fuchsin elastic stain, or hematoxylin
and eosin. Safranin was used as a counterstain with resorcin-fuchsin; eosin was
used as a counterstain with Verhoeffs.
The ages selected to represent functional stages of the mandibular joint were
as follows: (1) 20 days insemination age
for the fetal, non-functioning stage, ( 2 )
one week old for the suckling stage, (3)
one month old for the juvenile, masticatory stage, and (4) three months old for
the adult, masticatory stage.
OBSERVATIONS
Fetal stage - 20 days insemination age
The elastic laminae of arteries stain intensely in young fetuses, but the first clear
evidence of elastic elements in mandibular
joint tissues, does not appear until late
fetal stages. At 20 days insemination age
they appear as fine beads or granules 10cated mostly in the loose mesenchymal
tissue posterolateral to the condyle (fig,
1). In this area, where the disk and condyle separate to form the lower synovial
cavity, pinpoint sections of the fine elastic
elements are most evident.
On the medial side of the condyle there
is a very sparse scattering of fine elastic
granules in the peripheral portion of the
disk and in the superior tendinous fiber5
of the lateral pterygoid muscle continuous
with the disk. There is no evidence of elastic fibers in the vicinity of the inferior
tendinous insertion of the muscle to the
medial surface of the condylar process.
The thick fibrous layer which lines the
articular surfaces of the mandibular fossa
and the condyle contains no elastic fibers
at this age. Nor are there any elastic fibers
in the thin articular portion of the disk.
Suckling stage -one week old
Observations of elastic fiber distribution
at the suckling stage show a complete absence of fibers from articular surfaces of
the joint. The fibroblastic mesenchymal
lining of the mandibular fossa, the lining
of the superior pole of the condyle, and the
articular disk proper have differentiated
into well organized fibrous connective tissue with densely arranged collagenous
fibers, but no elastic fibers.
A rapid development of elastic fibers in
localized areas outside the mandibular
joint tissues has occurred in such structures as the ear, pharynx, larynx and arterial elastic laminae. In the mandibular
joint tissues, where the diameter and total
number of fibers is increased, the distribution of elastic fibers is generally the same
as at the fetal stage.
A conspicuous concentration of elastic
fibers is seen in a narrow fibrous band extending from the zygoma to the loose synovial tissue within the posterolateral region
of the joint. This band, with the posterior
ELASTIC FIBERS IN THE MANDIBULAR JOINT
335
peripheral disk tissue, forms the postero- behind the condyle, where the upper layer
lateral boundary of the upper synovial cav- of the fibrous articular disk extends toity and contains numerous, coarse fibers ward the squamosal bone, the fibrous
attachment is heavily infiltrated with
(fig. 2 ) .
As in the fetus, there is much less evi- lengths of fine and coarse elastic fibers.
In a section through the anterior pordence of elastic fiber development on the
medial side of the condyle than on the lat- tion of the articular structures, a few
eral side. The major increase medially has large, intensely stained, wavy elastic fibers
occurred in the connective tissue junction are present medially in the connective
of the disk with the fibrous condylar pen- tissue transition from the lateral pterygoid
chondrium, where these structures form muscle to its tendon. This small fibrothe medial fold of the lower synovial cav- elastic area comprises a part of the wall
ity. The elastic fibers here are more exten- of the medial recess of the lower synovial
sive and thicker than they were in the cavity. At the lateral portion of the disk
fetal stage. The medial fold of the upper there are fine, short fibers which become
synovial cavity contains sparse, fine fibers longer and more numerous at the periphin its wall. There is only slight evidence of ery. They are particularly dense in the'
elastic fibers at the condylar insertion of fibrous muscle attachments and in the
fibrous walls of the synovial cavity rethe lateral pterygoid muscle.
The upper lamina of the posterior at- cesses (fig. 4).
tachment of the disk contains numerous,
Adult stage -three months old
fine, elongated elastic fibers, few collagenIn addition to a general increase in
ous fibers, and many fibroblasts in a vascular mesenchyme. These characteristics diameter and quantity of elastic fibers in
indicate an early formation of elastic areas previously identified, a very conspicconnective tissue in the area posterior to uous development of fibers has occurred
anteriorly in the thick articular portion of
the condyle.
the disk during the young adult growth
Juvenile stage - one month old
period. The density of these fibers is greatMajor changes in development and dis- est on the inferior surface, in the subtribution of elastic fibers have occurred synovial fibrous tissue lining the inferior
from the suckling stage to the masticatory synovial cavity. On the opposing articular
stage of the juvenile mouse. At the fibrous surface of the condyle, however, there is
transition of perichondrium to periosteum, a conspicuous lack of fibers.
Farther posteriorly the thin articular
on the lateral surface of the condyle and
neck of the mandible, many fibers of vary- portion of the disk lacks elastic fibers coming thickness have appeared in the surface pletely, as do the opposing squamosal and
layers. At the neck area, where remodeling condylar surfaces.
resorption of the mandible is active, many
Posterior to the condyle the disk thickcoarse fibers turn inward to penetrate the ens and then separates into upper and
fibrous connective tissue quite deeply (fig. lower laminae of fibrous tissue. The upper
3). Descending from the lateral neck area lamina becomes heavily infiltrated with
for a short distance, the periosteum con- elastic fibers to form a fibroelastic band
tains short, thick fibers perpendicular to which splits around the loose, vascular
the surface and aligned like the teeth of connective tissue in the post-glenoid area
a comb.
anterior to the tympanic bulla. Superiorly
The articular disk, composed of dense it approaches the post-glenoid foramen,
fibrous tissue, is quite thick anteriorly. In while inferiorly it descends to contribute
this region it contains scattered beads or long elastic fibers to the epimysium on the
granules of elastic elements resembling posterior surface of the lateral pterygoid
those seen elsewhere in the joint tissues in muscle.
earlier stages of elastogenesis. Farther posThe inferior lamina, as it continues posteriorly, through sections of the thin avas- teriorly from the disk, contains many
cular portion of the disk, there are no elastic fibers interspersed in its fibrous
indications of elastic fibers. In the area tissue, but not enough to give it the fibro-
336
JACK FROMMER AND CLYDE W. MONROE
elastic appearance of the superior lamina.
As it descends it partially merges with the
connective tissue of the lateral pterygoid
muscle before inserting posteriorly on the
neck of the mandible.
At the lateral and medial periphery of
the disk the distribution of elastic fibers
is similar to that seen in the juvenile
mouse where short, fine fibers give way to
longer and more coarse fibers. The concentration and staining intensity of the
fibers has increased, however, particularly
on the lateral side (figs. 5 and 6 ) . From
the lateral periphery of the disk, two heavy
bands of elastic fibers diverge in a manner
similar to that which was observed in the
retro-condylar area. One band of elastic
fibers attaches with fibrous elements to
the periosteum of the neck of the mandible
immediately below the condyle (fig. 5 ) .
The other band sweeps around the posterior deep portion of the masseter muscle
to form a prominent component of its epimysium and to separate it from the adjacent loose, vascular connective tissue
(fig. 5).
DISCUSSION
The site of the future mandibular joint
can be delineated as early as the fifteenth
day insemination age, but the first clear
evidence of elastic elements in the joint tissues does not appear until the nineteenth
to twentieth day insemination age. At this
age the articular disk exists as an arc of
condensed intra-articular mesenchyme between the mandibular fossa and the
superior pole of the condylar process. Cavitation to form the synovial cavities has
been initiated at the upper and lower surfaces of the disk, and vascular infiltration
in the peripheral regions of the disk has
accompanied the formation of loose, synovial mesenchyme which will later develop
into vascular synovial membranes and
folds (Frommer, ’64). It is apparent,
therefore, that elastogenesis does not begin
until the major elements of the mandibular joint are present. This should not be
construed as a response to mechanical or
functional demands since this early appearance occurs at a fetal, pre-suckling,
pre-masticatory age.
The first distinct elastic elements which
occur at this stage have a granular appear-
ance, not sufficiently elongated to be called
fibers (fig. 1). These elastic granules are
located mostly in the loose vascular mesenchyme posterolateral to the condyle, an
area which will develop very prominent
fibroelastic elements at later stages.
Whenever elastic fibers occur in the
mandibular joint tissues, their earliest appearance is in the form of granules or
beads. Fyfe and Gillman (’64),in reference to unpublished data of Gillman and
Oneson, stated that orcein-stained 1l-day
embryonic mouse aortae elastogenesis
started as fine orceinophilic “beads” at the
site of future internal elastic laminae
when observed by light microscopy. With
increasing embryonic age, the beads fused
into larger elastin masses. Fyfe and Gillman demonstrated these changes in aortic
elastogenesis by electron micrography in
11 to 20-day embryonic mice.
The early sites of elastogenesis in the
mandibular joint are in the peripheral portions of the articular disk, at the transition
and continuation of fibrous disk tissue
with the periarticular tissues, and with
the periosteum around the neck of the
mandible.
During the suckling stage there are no
new areas of elastogenesis except a few
fine fibers at the inferior tendinous insertion of the lateral pterygoid muscle to the
medial surface of the condylar process. In
areas where elastogenesis had already begun, however, the concentration, length
and caliber of fibers is increased. This is
especially evident in the walls of the medial and lateral recesses of the synovial
cavities, and in the posterior continuation
of the disk to form a fibroelastic band of
attachment to the squamosal bone.
Elastic elements do not appear in the
thick, anterior periphery of the disk until
the juvenile masticatory stage. In the
young adult this elastic fiber development
is quite conspicuous particularly along the
inferior surface of the anterior extension
of the disk.
In the mandibular joint of the adult
mouse, elastic fibers are especially evident
in the following locations: (1) The posterior fibroelastic band of the retrocondylar disk attachment. (2) The fibrous walls
of synovial cavity recesses. ( 3 ) The short
fibrous attachments of the disk to the neck
ELASTIC FIBERS IN THE MANDIBULAR JOINT
337
of the mandible. (4) The epimysium on vation or lateral excursion. Both mandibuthe surface of the lateral pterygoid and lar condyles are processes of the same
masseter muscles.
bone, and they can not act independently.
The thin, condensed, fibrous, central Consequently, multiple stretch and shearportion of the disk exhibits no elastic ing forces are created in the articular and
fibers at any age. The lack of stainable periarticular tissues. These stresses are
elastic elements is evident also in the ar- largely limited and reduced by elastic
ticular fibrous surfaces of the mandibular fibers and by occlusal contacts of the
fossa and the condyle. This observation is teeth, a factor of primary significance in
in disagreement with that of Miles and edentulous individuals with degenerative
Dawson ('62) who reported abundant changes in the articular tissues.
elastic fibers in the articular fibrous tissue
(4) The mandibular fossa is not very
of the human temporomandibular joint, deep in the anteroposterior plane in the
even at birth. They also found a simi- rodent. The squamosal surface provides a
lar distribution of elastic fibers in sev- shallow socket for the disk and condyle,
eral other mammalian species, including and there is no marked articular emirodents.
nence. The resultant condylar hypermoInterpretations of the role of elastic bility requires more joint stabilization
fibers in functions of the mandibular joint from structures other than skeletal. This
must take into consideration the unusual stabilization is provided largely by the
nature of this diarthrodial joint, especially muscles which move the joint. In the
mouse, where the lateral temporomandibuin reference to the following:
( 1 ) The articular surfaces are lined lar ligament is lacking, additional stability
with fibrous connective tissue rather than and control must be provided by the poshyaline cartilage. The lack of articular terior deep portion of the masseter muscle
cartilage might require an alternate source (Frommer and Monroe, '66).
of resilience in the stress-bearing articular
Although the late appearance and slight
areas, as postulated by Griffin and Sharpe development of elastic elements in the
('62), and Miles and Dawson ('62). These mandibular joint during embryogenesis
investigators felt that elastic fibers im- reflect the lack of functional requirements
parted this resilience to the articular during this stage, they show an adequate
fibrous tissue. With the evidence available preparedness for the mandibular activity
at present, it is not firmly established that of the neonatal suckling stage. The rethe articular surfaces of the mandibular quirements for elasticity are not very exjoint are particularly stress-bearing, that tensive until the onset of masticatory
these fibrous surfaces contain elastic activity. The response of elastic fiber
fibers, or that resilience of the articular development to meet this requirement consurfaces is an essential requirement of tinues until the peak of stretching and
this joint.
shearing forces is reached in the young
(2) A fibrous articular disk is inter- adult mouse.
posed between the mandibular condyle
The development of elastic fibers as an
and the fossa, thus creating two joint cav- adaptation to stretching forces occurs prinities and a double articulation. Two basic cipally at the peripheral extensions of the
movements occur; a sliding movement in articular disk. This is particularly evident
the upper compartment between the disk posteriorly, where the fibroelastic band of
and the mandibular fossa, and a hinge the retrodiscal pad is stretched as the disk
movement in the lower compartment be- slides forward with the condyle during
tween the condyle and the disk. Since the protrusive mandibular movements. The
variety of articular movements is in- degree of extensibility of the elastic lamcreased, the structural adaptations should ina limits the forward excursion of the
also increase.
disk and is instrumental in returning the
( 3 ) The right and left mandibular disk to the resting position when contracjoints must act bilaterally and simultane- tion of the lateral pterygoid muscle ceases.
ously in any mandibular action whether
The shape of the synodal cavities
it is protrusion, retrusion, depression, ele- changes constantIy during mandibular
338
JACK FROMMER AND CLYDE W. MONROE
activity. Elastic fibers mingled with the
collagenous fibers of the subsynovial layer
prevent excessive distortion and allow the
return to the normal resting condition of
villi and folds without undue stress on the
synovial lining. Tension on the walls of
the joint cavities is especially strong at the
peripheral recesses adjacent to the fibrous
attachments of muscles to the disk and
neck of the mandible.
The presence of elastic fibers in the
short fibrous attachments of the disk to
the mandible might serve two additional
functions: ( 1 ) Although the hinge movement in the lower compartment requires
little extensibility of the compartment
walls, there is some stretching of the taut,
fibrous wall tissue in the rotatory movement of the condyle. ( 2 ) If the condyle of
the mouse continues its forward excursion
beyond the maximum normal forward excursion of the disk, as described for the
human joint by Rees (’54), the short
fibrous attachments of the posterior mandibular lamina might indeed require elastic fibers to prevent damage during excessive excursion. Although Rees noted that
the posterior mandibular attachment in
man was not stretchable and contained
little elastic tissue, our observations revealed a concentration of elastic fibers
within this lamina in the mouse adequate
to account for a moderate degree of stretch
and elastic recoil.
The interposition of a fibrous meniscus
between two fibrous-lined bony surfaces,
rather than the firm, cartilaginous, articular surfaces found in most other joints,
supports the contention that this is not
a pressure-exerting articulation requiring
highly resilient surfaces. The configuration of tissues, including elastic fibers,
appears to be oriented toward the facilitation of mobility and the accommodation
of stretch and shearing forces while not
allowing these forces to become excessive.
ACKNOWLEDGMENT
The authors wish to express their
sincere appreciation to Dr. W. D. Belt for
his valuable assistance in the preparation
of the photomicrographs.
LITERATURE CITED
Dixon, A. D. 1962 Structure and functional
significance of the intra-articular disc of the
human temporomandibular joint. Oral Surg.,
15: 48-61.
Frommer, J. 1964 Prenatal development of the
mandibular joint i n mice. Anat. Rec., 150:
449462.
Frommer, J., and C. W. Monroe 1966 The
nature of the peri-articular tissues of the mandibular joint i n the mouse and rat. Arch. Oral
Biol., 11: 947-948.
Fyfe, F. W.,and T. Gillman 1964 Electron
microscopy of commencing elastogenesis in
embryonic mouse aorta. J. Anat., 98: 682
( Abstr. ) .
Griffin, C. J., and C. J. Sharpe 1962 Distribution of elastic tissue in the human temporomandibular meniscus especially in respect to
“compression” areas. Austral. Dent. J., 7: 7278.
Miles, A. E. W., and J. A. Dawson 1962 Elastic
fibers in the articular fibrous tissue of some
joints. Arch. Oral Biol., 7: 249-252.
Rees, L. A. 1954 The structure and function
of the mandibular joint. Brit. Dent. J., 96:
125-133.
PLATES
Abbreviations
C, condyle
D, articular disk
EG, elastic granules
M, masseter muscle
NM, neck of the mandible
U, upper synovial cavity
PLATE 1
EXPLANATION OF FIGURES
1 Frontal section through the loose vascular mesenchyme posterolateral to the condyle at 20 days insemination age. The elastic
elements appear at this age as fine granules in the area where disk
and condyle separate to form the lower synovial cavity. Resorcinfuchsin stain. Safranin counterstain. x 376.
2
340
Frontal section through the lateral retrocondylar region of the joint
to show elastic fiber condensations i n the walls of the posterior recess
of the upper synovial cavity. One week old suckling age. Verhoeff
stain. Eosin counterstain. x 376.
ELASTIC FIBERS IN THE MANDIBULAR JOINT
jack Frommer and Clyde W. Monroe
PLATE 1
341
PLATE 2
EXPLANATION OF FIGURES
3
Frontal section through the lateral neck region in the midcondylar
plane where many coarse elastic fibers, descending from the perichondrium, turn inward to penetrate the periosteum. One month old
juvenile age. Verhoeff stain. Eosin counterstain. x 376.
4 Lateral joint tissues in a frontal plane through the posterior portion
of the condyle. The articular disk joins with the periarticular tissue
to form the lateral recess of the upper synovial cavity. An extensive
distribution of coarse and fine elastic fibers is seen in the walls. One
month old juvenile age. Resorcin-fuchsin stain. Safranin counterstain. X 376.
342
ELASTIC FIBERS IN THE MANDIBULAR JOINT
Jack Frommer and Clyde W. Monroe
PLATE 2
343
PLATE 3
E X P L A N A T I O N OF F I G U R E S
344
5
Elastic fiber distribution i n the lateral joint tissues of a three month
old mouse. The frontal plane of section is through the midcondylar
region. TWObands of elastic fibers diverge from the lateral periphery
of the disk; one toward the neck of the mandible, the other around
the posterior deep portion of the masseter muscle. Resorcin-fuchsin
stain. Safranin counterstain. x 88.
6
A portion of figure 5 more highly magnified to show the heavy concentration of elastic fibers i n the lateral peripheral portion of the
articular disk. Resorcin-fuchsin stain. Safranin counterstain. X 376.
ELASTIC FIBERS IN THE MANDIBULAR JOINT
Jack Frommer and Clyde W. Monroe
PLATE 3
345