Morphologic changes in the elastic fibers of the temporomandibular joint after experimental disc perforation in the rabbit

J Oral Moxlllofac 56:753-758,

Surg 1998

Morphologic Changes in the Elastic Fibers of the Temporomandibular Joint After Experimental Disc Perforation in the Rabbit Shuichi

Sato, DDS, PhD, * Satoshi Goto, DOS,? Shinji Kamakura, WDS, PbD,f and Katsutoshi Motegi, MD, WDS, PbDJ

Elastic fibers in the attachment regions of the temporomandibular joint (TMJ) are considered important in the movements of the disc during jaw motion. This study was designed to determine whether there are change in the elastic fibers of the TMJ when the disc is perforated for a long period. Each TMJ of five rabbits was surgically exposed, and a mediolateral perforaMaterials and Methods: tion was made in the center of the articulating region of the disc with a scalpel. Five untreated
Elastic fibers are thought to be important for the normal function of various organs. In the attachment regions of the temporomandibular joint (TMJ), elastic tissuesare considered important in the movements of the disc during jaw motion. Perforation of the disc in the human TMJ is occasionally observed.1-7However, there have been few studies of the changes in the elastic fibers in the TMJ with a perforated disc, even though there have been many clinical and experimental studies of the changesin the bone and cartilage of the condyle and articular eminence.

The current study was designed to determine whether thcrc are changes in the elastic fibers of the TMJ when the disc is left perforated for a long time.

Materials

and

Methods

Thirteen male Japanese white rabbits, weighing between 3.0 and 3.5 kg, were used in this study. They were divided into three groups as follows: controls that did not undergone surgery of the right TMJ (n = 5); sham-operated rabbits (n = 3); and rabbits with disc perforation treated surgically (n = 5). SURGICALDISC PERFORATION

Received

from

the Department

Tohoku University *Lecturer.

School

of Oral and Maxillofacial

of Dentistry,

Surgery

Surgical disc perforation was done according to the method of Lang et aI8 General anesthesiawas induced and maintained with intravenous nembutal (30 mg/ kg). Right TMJ disc perforation was performed in five rabbits. After the skin between the right ear and eye was shaved, 1 mL 2% xylocaine with l:lOO,OOO epinephrine was infiltrated into the preauricular tissues for hemostasis. A horizontal skin incision was made over the right TMJ beginning behind the lateral canthus of the eye and extending approximately 2.0 cm posteriorly. Blunt and sharp dissection was used to

I,

Sendai, Japan.

iAssistant. *Assistant. “Professor. Address correspondence and reprint ment of Oral and Maxillofacial Surgery of Dentistry, D 1998

4-l Seiryo-machi,

American

Association

Aoba-ku,

of Oral

requests to Dr Sato: DepartI, Tohoku University School Sendai 98023575,

and Maxillofacial

Japan.

Surgeons

0278.2391/98/56060010$3.00/0

753

754 expose the lateral joint capsule. The superior joint space was entered by separation of the posterior discal attachment from the squamous temporal bone. The disc was identified, mobilized, and isolated. A mediolateral perforation was made in the central articulating region of the disc with a no. 15 scalpel blade and completed with microsurgical scissors. The perforation extended approximately 1.5 mm proximal to the mediolateral margins of the disc. Care was taken to avoid cutting the underlying condylar articular surface. Polyglactin (Vicryl; Ethicon, Somerville, NJ) 6-O continuous sutures were used to close the capsule, and 4-O polyglactin continuous sutures were used to close the muscle layer and skin. Three rabbits underwent a sham right TMJ operation in which the superior joint space was opened, the disc was identified, and then the capsule, muscle layer, and skin were closed. All rabbits were immediately placed on a regular diet and water. They were killed by intracardiac perfusion of 10% formalin at 10 months after disc perforation. Blocks of tissue containing the TMJ were removed and placed in 10% formalin for 3 weeks. The specimens were decalcified in a solution consisting of sodium citrate (20%) and formic acid (50%) for 8 weeks, and then embedded in paraflln. The paraffin blocks were sectioned at 4-pm thickness. The sections were oxidized by 0.3% KMn04 and 0.3% HaSO* and were stained with aldehyde fuchsin.

Results There were no obvious differences between the histologic findings in the unoperated control and sham-operated control joints. Accordingly, the term control as used hereafter refers to both types of control joints. In the controls, the TMJ joint space was divided into the superior and inferior joint space by the disc. The surfaces of the condyle, the disc, and the articular eminence were smooth. The articular disc consisted of an anterior band, an intermediate thin zone, a posterior band, and anterior and posterior attachments (Fig 1). In contrast to the control joints, the TMJs from the rabbits with a perforated disc showed marked changes in the articular eminence, condyle, and disc. Focal areas of the bone of the articular eminence were denuded of their fibrous covering. Bone resorption with connective tissue replacement was observed. The condylar surface was flattened beneath the area of disc perforation (Fig 2). The control disc proper was composed of dense collagen bundles that ran parallel on the superior and inferior surfaces. Chondrocytes were present among these collagen bundles. The chondrocytes appeared rounded, contained round nuclei, and were surrounded with lacunae. The intermediate thin zone of

ELASTIC

FIBER

FIGURE 1. Sagittal condyle, the disc, and disc consists of the attachments (Aldehyde

OF THE

TMJ

WITH

PERFORATED

DISC

section of a control TM]. The surface of the the articular eminence are smooth. The articular disc proper and the anterior and posterior fuchsin, original magnification ~3).

the disc contained very few elastic fibers (Fig 3). However, in contrast to the control disks, the perforated discs contained many undjfferentiated cells close to the free margins of the perforation and disturbed collagen bundles. The intermediate thin zone of the disc contained very few elastic fibers, similar to the control disc (Fig 4). The posterior-inferior attachment in the control TMJ contained thick bundles of elastic fibers extending primarily in an anterioposterior direction (Fig 5). In contrast, the elastic fibers in the TMJs with a perforated disc appeared fragmented and patched. They did not form thick bundles, and their number was markedly reduced (Fig 6). The findings for the elastic fibers in the anterior-inferior attachment were the same as those in the posterior-inferior attachment in both the control TMJs and in those with a perforated disc (Figs 7,s).

FIGURE 2. Sagittal section of the TMJ with a perforated disc. bone of the articular eminence has been resorbed and replaced connective tissue. The condylar surface is flattened under the perforation (Aidehyde fuchsin, original magnification x3).

The with disc

SAT0 ET AL

FIGURE

3. Intermediate thin area of the disc in a control TMJ. The disc is composed of dense collagen bundles that extend horizontally. Chondrocytes are present among these collagen bundles. The disc contains very few elastic fibers (Aldehyde fuchsin, original magnification X 1201.

FIGURE Parallel, original

5. Posterior-inferior attachment darkly stained, fine, elastic fibers magnification X 120).

of the disc in a control TMJ. are seen. (Aldehyde fuchsin,

12). This fibrous tissue contained some elastic fibers

(Fig 13). In the control condyles, the articular zone, intermediate zone, and hypertrophic zone were well developed. They did not appear to contain elastic fibers (Fig 9). In contrast, in the condyles of the TMJs with the perforated discs, the articular zone, intermediate zone, and hypertrophic zone could not be distinguished. The surface of the condyle was composed of fibrous tissue containing a few chondrocytes, but it did not contain any fibroblasts, and in the portion beneath the surface layer, the chondrocytes formed clusters. The condyle did not appear to contain elastic fibers (Fig 10). In the control TMJs, the articular eminence was covered with fibrous tissue. Chondrocytes were seen under the fibrous tissue. Few elastic fibers were observed (Fig 11). In the TMJs with perforated discs, focal areas of denuded bone were observed on the articular eminence. Areas of bone resorption also were found under the thickened fibrous tissue (Fig

Perforation of the disc is thought to potentially lead to osteoarthritic changes in the condyle and articular eminence. Our results were similar to those observed in other experimental studies.7a9-11 Among these studies, that by Helmy et allo showed, as did this study, that the surface of the articular eminence was relatively more affected by the osteoarthritic changes than other structures. They speculated that the reason might be the excessive loading and pressure in this area after disc perforation. There have been many studies in which the changes in the cartilage on the condyle or articular eminence were examined in TMJs with perforated discs.l-l’ In the current study, loss of elastic fibers from the anterior and posterior attachments of the perforated disc was observed, but elastic fibers were observed in

FIGURE 4. Free mar in area undifferentiated cells, % ut very original magnification X 120).

elastic reduced

of a perforated disc. It contains many few elastic fibers [Aldehyde fuchsin,

Discussion

FIGURE

6. Posterior-inferior attachment of a perforated fibers appear fragmented and patched, and their (Aldehyde fuchsin, original magnification x 1201.

disc. The number is

756

ELASTIC

FIBER

OF THE

TMJ

WITH

PERFORATED

DISC

FIGURE

7. Anterior-inferior attachment of the disc in a control TMJ. Note the parallel, darkly stained, fine, elastic fibers (Aldehyde fuchsin, original magnification X 120).

the fibrous tissue on the resorbed bone of the articular eminence above the perforated disc. Ali et all2 examined the morphologic alterations in the elastic fibers of the rabbit TMJ after experimentally induced anterior disc displacement. They observed the presence of elastic fibers in the osteoarthritic condylar cartilage. However, we observed few elastic fibers in the osteoarthritic condylar cartilage after disc perforation. Ali et all2 also observed the presence of elastic fibers in the fibrous tissuescovering the control rabbit condyle and disc. Conversely, we observed few elastic fibers in the fibrous tissuescovering the control rabbit condyle and disc. Ali et all2 used New Zealand white rabbits in their experiment, whereas we used Japanesewhite rabbits. The differences in appearance of elastic fibers in osteoarthritic condylar cartilage between the study of Ali et all2 and our study may be due to the difference in the kind of rabbit used in the experiment or the difference in the type of osteoarthritis induced by anterior disc displacement and induced disc perforation. The mechanism of elastic fiber reduction in the perforated disc is unclear. It has been reported that elastase digests the elastic fibers in the rabbit TMJ disc.‘3,l* It has also been reported that metalloprote-

FIGURE 8. Anterior-inferior attachment of a TMJ with a perforated disc. The elastic fibers appear fragmented and patched, and their number is reduced (Aldehyde fuchsin, original magnification x 120).

FIGURE 9. Condyle of a control TMJ. The fibrous zone, proliferating zone, mature cell zone, and hypertrophic cell zone are seen. They do not appear to contain elastic fibers (Aldehyde fuchsin, original magnification X 1201.

FIGURE 10. Condyle of a TMJ with a perforated disc. The fibrous zone, proliferating zone, mature cell zone, and hypertrophic cell zone cannot be distinguished. The surface of the condyle is covered by fibrous tissue that contains a few chondrocytes, but it does not contain any fibroblasts. The portion under the surface layer contains chondro c tes in the form of clusters. The condyle does not appear to contain eYastrc fibers. [AIdehyde fuchsin, original magnification x 1201.

SAT0 ET AL

FIGURE 11. Articular eminence of a control eminence is covered with fibrous tissue. Chondrocytes the fibrous tissue. Few elastic fibers are observed original magnification X 120).

TMJ.

The articular are seen under (Aldehyde fuchsin,

FIGURE 13.

Fibrous tissue replacin the resorbed bone of the articular eminence of the TMJ with a per 7orated disc. The fibrous tissue contains some elastic fibers [arrows) (Aldehyde fuchsin, original magnification X 120).

FIGURE 12. Articular eminence of a There is a focal area of denuded bone on of bone resorption are present under (Aldehyde fuchsin, original magnification

TMJ with a perforated the articular eminence. the thickened fibrous x 1 21.

disc. Areas tissue

ases, including elastase, are secreted by stimulated chondrocytes and synovial fibroblasts in the presence of interleukin-1 .15,16 The detection of interleukin-1 has been reported in degenerative joint disease.*7,1s The elastic fibers in the rabbit TMJ with a perforated disc may be degraded by a mechanism involving these phenomena. It is conceivable that the elastic tissue on the resorbed bone of the articular eminence above the perforated area of the disc absorbs shock during mandibular movement and serves as a substitute for the normal disc. It is known that fibroblasts secrete components of elastic fibers along with connective tissue collagen.19We believe that in the rabbits with perforated discs in our study the elastic fibers in the fibrous tissue on the resorbed bone of the articular eminence were formed by this mechanism. Savalle et al,*Owho examined the functional significance of the elastic fiber density in the rabbit, deduced that the fibroelastic attachments keep the disc pressed against the condyle in all positions. They observed that during opening the anterior attachment is greatly stretched and the posterior attachment is relaxed, whereas during closing the reverse set of phenomena prevail. In rabbits, the lateral movements

758

DISCUSSION

during mastication are very pronounced. During lateral rotation, the ipsilateral condyle slides posteriorly and slightly medially. Savalle et a120speculated that in such movements the elastic fibers in the posterior attachment of the disc are stretched and play a role in shock absorption. The loss of elastic fibers from the anterior-inferior and posterior-inferior attachments of the perforated disc of the rabbit may partially disrupt these functions. Our results show that experimental disc perforation changes the distribution and density of elastic fiber in the TMJ and also leads to osteoarthritis. This information may improve our understanding of the consequences of perforation of the disc.

References 1. Bronstein SL, Tomasetti BJ, Ryan DE: Internal derangement of the temporomandibular joint: Correlation of arthrography with surgical findings. J Oral Surg 39:572, 1981 2. Doyle T, Hase M: The use of arthrography in the management of temporomandibular joint problems. Aust Dent J 28:9, 1983 3. Graham GS, Ferraro NF, Simms DA: Perforations of the temporomandibular joint meniscus: Arthrographic, surgical and clinical findings. J Oral Maxillofac Surg 42:35, 1984 4. Helms CA, Katzberg RW, Dolwick MF, et al: Arthrotomographic diagnosis of meniscus perforation in the temporomandibular joint. BrJ Radio1 46:283, 1980 5. Holmlund A, Hellsing G: Arthroscopy of temporomandibular joint: An autopsy study. lnt J Oral Maxillifac Surg 14:169, 1985 6. Ioannides C, Scaf J: Perforation of the intra-articular disc diagnosed by arthrotomography of the temporomandibular joint. J Oral Maxillifac Surg 13:28, 1985 7. Leidberg J, Westesson P-L: Diagnostic accuracy of upper compartment arthroscopy of the temporomandibular joint: Correlation with post mortem morphology, Oral Surg Oral Med Oral Path01 62:618, 1985

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P: Experimental temporoman8. Lang TC, Zimny ML, Vijayagopal dibular joint disc perforation in the rabbit: A gross morphologic, biochemical and ultrastructural analysis. J Oral Maxillofac Surg 51:1115, 1994 disc 9. Bosanquet A, Ishimaru Jl, Goss AN: Effect of experimental perforation in sheep temporomandibular joint. Int J Oral Maxillofac Surg 20:177, 1991 10. Helmy E, Bays R, Sharawy M: Osteoarthrosis of the temporomandibular joint following experimental disc perforation in macaca fascicularis. J Oral Maxillofac Surg 5 1:979, 1988 degenerative temporomandibular joint 11. Lekkas C: Experimental diseases. Int J Oral Maxillofac Surg 23:423, 1994 12. Ali AM, Sharawy M, O’Dell NL, et al: Morphological alterations in the elastic fibers of the rabbit cranlomandibular joint following experimentally induced anterior disk displacement. Acta Anat 147:159, 1993 13. O’Dell NL, Sharawy M, Starcher BC, et al: In vitro effects of elastase on rabbit craniomandibular joint articular disks. Acta Anat 145:229, 1992 CB, et al: Effects of elastase 14. Sharawy M, O’Dell NL, Pennington on the rabbit craniomandibular articular disk. J Dent Res 71:237, 1992 (suppl) J, Zafarullah M, Kodama S, et al: In vitro effects 15. Martel-Pelleti& of interleukin 1 on the synthesis of metalloproteases, TIMP, plasminogen activators and inhibitors in human articular cartilage. J Rheumatol 18:80, 199i (suppl2n 16. Towle CA, Trite ME, Olllvierre F, et al: Regulation of cartilage remodeling by IL-l: Evidence for autocrine synthesis of IL-1 by chondrocytes. J Rheumatol14:11, 1987 (suppl14) J, Hoerrner LA, Lark MW, et al: Recombinant human 17. McDonnell interleukin-1 P-induced increase in levels of proteoglycans, stromelysin and leukocytes in rabbit synovial fluid. Arthritis Rheum 35:799,1992 18. Witsch-Prehm P, Karbowskl A, Ober B, et al: Influence of continuous infusion of interleukin-la on the core protein fragments of the small prteoglycan decorin in cartilage. J Orthop Res 10:276,1992 F: Textbook of Histology (ed 1). Copenhagen, 19. Geneser Munksgaard, 1986, p 161 20. Savalle WPM, Weijis WA, James J, et al: Elastic and collageous fibers in the temporomandibular joint capsule of the rabbit and their functional relevance. Anat Ret 227:159, 1990

Surg

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1998

Discussion Morphologic Changes in the Elastic Fibers of the Temporomandibular Joint Afier Experimental Disc Perforation in the Rabbit Mohamed Professor, of Georgia,

Sharawy

Department Augusta,

of Oral Georgia

BDS, PhD Biology/Anatomy,

Medical

College

Emad Helmy, BDS, PhD Lecturer, Department of Dentistry, Cairo,

This

a model

study to

of Oral Egypt

used the rabbit

Surgery,

Cairo

craniomandibular

University

School

joint

study the effect of disc perforation

(CMJ)

as

on elastin

content of the disc. In evaluating the results one has to be aware of the differences between the elastin distribution in the rabbit and human joints. The studies of Savalle et al,’ O’Dell et al,2 and Ali et al3 have indicated the absence of elastic fibers in the superior portion of the bikninar zone (BZ) in the rabbit in contradistinction to their abundance in the superiorstratumof human BZ, suggesting that there are significant functional differences between human and rabbit joints. However, regardless of these differences, the selective abundance of elastin in the BZ tissues is important to the function of both the human temporomandibular joint (TMJ) and rabbit CMJ. Although numerous studies have used aldehyde fuchsin stain to show elastic fibers, one should be aware that it is a selective and not a specific stain for elastic fibers. It also has been shown that aldehyde fuchsinstain damages collagen as