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