Effect of marrow perforation on the sheep temporomandibular joint

Research;development

Effect of marrow perforation on the sheep temporomandibular joint

J.-I. I s h i m a r u 1, K. Kurita 2, Y. H a n d a 3, A. N. G o s s 4 1Department of Stomatology, Gifu Municipal Hospital, ~Second Department of Oral and Maxillofacial Surgery, Aichigakuin University School of Dentistry, and aOral and Maxillofacial Surgery Gifu University School of Medicine, Japan; 4Oral and Maxillofacial Surgery Unit, The University of Adelaide, Australia

J.-I. Ishimaru, K. Kurita, Y, Handa, A. N. Goss: Effect o f marrow perforation on the sheep temporomandibular joint. Int. J. Oral Maxillofac. Surg. 1992; 21." 239-242. Abstract. The effect of surgically perforating the mandibular condyle to allow synovial fluid to contact the marrow was examined in 5 sheep temporomandibular joints. The surgical defect showed replacement of the marrow with fibroosseous tissue and subcortical cysts. A vertical, central osteophyte emerged from the perforation, causing attenuation or perforation of the disc and temporal surface proliferation. These changes were radiographically and histologically similar to advanced osteoarthritis. This supports the concept that intraarticular micro or macrofracture may result in osteoarthritis.

Osteoarthritis (OA) is a common joint disease which may involve many joints, including the temporomandibular. Despite its commonness, there is an ongoing debate about the aetiology, diagnosis and treatment. Generally, OA is characterized by 2 primary responses ~4, one is initial cartilage breakdown, and the other is subsequent peripheral osteophyte formation. Multiple factors have been believed responsible for OA ~7, and are broadly divided into 2 major factors, one systemic, and the other local. Aging, sex and hormones have been considered as systemic factors, while mechanical loading and trauma, as local factors 17. In orthopaedics, several aetiological hypotheses have been advocated for general OA. RAOlY & ROSE~8 hypothesized subchondral stiffness as a result of repeated loading was responsible for initial cartilage breakdown. Trauma may cause cartilage damage, which may lead to secondary osteoarthritis ~3. In parallel to such hypotheses, a number of arthritic animal models have been reported mainly involving knee and hip joints. Enzymatic correlationship to OA is also reported by many investigators 1'4.~, 16, and the degradative enzyme, papain, destroys cartilage. KoPP et al.H showed osteoarthritic changes by intraarticular papain injection using the guinea pig knee joint. PEI,LETIEg et al. 16 showed in-

creased collagenolytic activity in osteoarthritic cartilage, using dogs. In the temporomandibular joint (TMJ), TOLI~ER& GLYNN2° thought the ingress of synovial fluid into marrow space through microfractures would cause subsequent OA. Their hypothesis was, however, derived from a human cadaver morphological study, so it has not been confirmed by direct experiments. A recent arthroscopic study has shown marked arthritic changes in the articular surface following trauma to the TMJ 5. Microfracture and/or intraarticular fracture will occur in the condyle following trauma, which may allow synovial fluid to penetrate into the marrow space. In the bone marrow there are a number of inflammatory cells and mediators which can contribute to wound repair. Thus, when the condyle is damaged, involving the marrow space, healing may occur from there. Alternatively, the ingress of synovial fluid into the marrow space may result in osteoarthritis. 2° Histologically, in the TMJ, condylar cartilage consists of 4 layers: articular, proliferative, fibrocartilage and calcified cartilage. The proliferative layer, consisting of many packed, undifferentiated mesenchymal cells, is the most responsible for cartilage proliferation2. Once this proliferative layer is widely damaged, the cartilage loses its ability to proliferate. Recently, ISHIMARU& GOSS9

Key words: osteoarthritis; trauma; TMJ Accepted for publication 30 March 1992

demonstrated that mild surgical damage to mandibular cartilage leads to gross osteoarthritic changes in the sheep TMJ. The purpose of this study is to examine the effect of marrow perforation in sheep mandibular condyle. Material and methods Five pure bred merino sheep, approximately 60 kg body weight, were used, and their management followed our previously described techniquez, 3 All left joints were operated, right joints were not disturbed, and used as controls. Anaesthesia was induced by intravenous injection of between 500 mg and 1000 mg thiopental into the external juglar vein. Intubation was performed and anaesthesia maintained with 3% halothane, with oxygen and nitrous oxide. The preauricular area was shaved and prepared with antiseptic solution. The field was isolated with sterile drapes and the joint exposed via a preauricular incision. Only the inferior joint spaces were opened by a horizontal incision through the joint capsule. By lateral translation of the mandible, the condylar surface was exposed and the articular soft tissue cover gently removed. Laterally, marrow penetration was performed in the central part of the condyle, by dental drill l mm in diameter, to a depth of about 1 cm into the marrow space. The condylar surfaces were then irrigated with normal saline and the joint capsule and overlying tissues repaired in layers. The sheep were returned to field conditions approximately 1 week after the surgical procedure. Ninety days after the operation, the sheep

240

Ishimaru et aL Table 1

Stage

Fig. 1. Lateral X-ray

photograph of an operated TMJ showing a large osteophyte (arrow) on the central part of the condyle.

were anaesthetized again for synovial fluid and arthroscopic examination. The sheep were then killed by anaesthetic overdose and exsanguination. The joint area was removed en bloc with a band saw, and fixed in 10% neutral buffered formalin. Radiographs were taken of the joint blocks in the antero-posterior and lateral planes. The radiographs were examined in random order and under standardized conditions. The following features were assessed for the temporal and condylar surfaces: erosion, flattening, osteophytes, sclerosis and subcortical cysts. A morphological rating of 0 for no demonstrable change, 1 for mild, 2 for moderate, and 3 for severe change was used, so a maximum score of 60 could be assigned to a joint. A double determination was performed at 1 month. This methodology followed that used by MuIR & Goss 15 for human TMJ radiographs. The blocks were decalcified with 9.5% hydrochloric acid, 1% sodium acetate over saturated EDTA, and sectioned in the parasagittal plane, into lateral, central, and medial specimens. These were prepared histologically and stained using hematoxylin and eos-

in. The histological slides were assessed, using a modification of the method of HANSSONet al. 6 and RICHARDSet al. 19. Each joint had been divided into 3 blocks, lateral, central and medial. Each slide was assessed at its anterior, central and posterior aspects, thus, in effect, dividing the joint into 9 zones. Each zone was assessed both descriptively and by directly measuring the thickness of the soft tissue layers of the temporal component and the condyle. Each layer was measured perpendicular to the articular surface and at 4 separate sites. The average was determined for each region and each section was then assessed by osteoarthritic stage2° (Table 1). Results

The control joints showed no radiographic abnormalities and thus had a morphological rating of zero. The operated joints showed no radiographic abnormalities of temporal surfaces, but all condyles showed erosion and osteophyte formation (Fig. 1). Flattening was observed in 3 condyles, one sclerosis

Index

No change

0

Fibrillation

1

Denudation Eburnation

2

Flattening Erosion Subcortical cyst

3

Fibrous repair

4

and 2 subcortical cysts were observed, The average morphological rate was 10.25 (range 7-14). The concordance of double determination was 95%. Histologically, control joints showed no change. In operated joints, the temporal surface showed marked remodeling activity, and the condyle showed marked arthritic changes; all condyles showed osteophyte formation, 3 flattening, one subcortical cyst, one disc perforation and 4 disc to condylar adhesions. In the condyle, 2 types of osteophytes were observed, centrally and posteriorly. The surgically created hole in the condyle was filled with fibrous connective tissue, accompanied by capillary formation and new bone formation. In 3 specimens, the repairing tissue showed overgrowth from m a r r o w space to articular surface (Figs. 2, 3). These osteophytes were devoid of cartilage and irregular in shape, which caused disc attenuation and perforation at the corresponding area. The height of the osteophytes ranged from 0.92 m m to 3.31 m m (average 1.66 ram), and width

Fig. 2. Macroscopic appearance of condyle showing centrally formed

Fig. 3. Histological section of a central osteophyte showing fibro-

osteophyte (short arrow) accompanied by anterior and posterior bone remodelling (long arrows). T: temporal bone, C: condyle, HE, x 2.

osseous connective tissue accompanied by many capillaries inside the osteohyte and corresponding disc shearing. D: disc, C: condyle, HE, xlO.

TMJ marrow perforation

One disc was completely perforated and the other 4 discs were attenuated corresponding to the central osteophytes. The inferior joint space was narrower, due to disc-condylar adhesions. In most of these adhesions, articular soft tissue on the condylar surface was incorporated into disc fibrous tissue (Fig. 6). This was seen in all specimens. The temporal surface showed marked progressive remodeling changes, and as a result was thicker than that of controls (Table 3). Osteoarthritic stage in various areas on the condyle is presented in Table 2. The arthritic changes were consistent with those seen in human cadaver studies 2°. There was a statistically significant difference between the experimental and control groups. Discussion Fig. 4. Histological section showing chondro-

cyte proliferation in lacunae (arrow) at the margin of the bone perforation. HE, x 10. ranged from 1.60 mm to 7.32 mm (average 4.26 mm). Only one specimen showed chondrocyte proliferation in lacunae at the superficial perforated bone margin, but there was no cartilage adjacent to the chondrocytes (Fig. 4). Posteriorly formed osteophytes were observed in 3 specimens, oval in shape with thicker cartilage stratification than normal. The height ranged from 0.46 mm to 2.70 mm (average 1.94 mm), and width ranged from 1.54 mm to 5.74 mm (average 3.92 mm). These posteriorly formed osteophytes were usually accompanied by underlying gross bone remodeling (Fig. 5).

This study showed that a surgically created marrow perforation in the mandibular condyle results in gross arthritic changes in the condyle, attenuation or perforation of the disc, and marked progressive remodeling of the temporal surface. The surgically created hole in the condyle was replaced by fibro-osseous connective tissue, associated with new blood vessel formation. These repairing tissues originated from marrow space. This effect was consistent with the report by MARCIANI et al. 12 Only one specimen showed chondrocyte proliferation in the lacunae at the superficial margin of the perforation, and there was no cartilage layer adjacent to the chondrocytes. Thus, the chondrocytes were probably differentiated from the marrow. This supports

Fig. 5. Histological section showing peripheral osteophyte at the

posterior aspect of the condyle. T: temporal bone, C: condyle, HE, ×2.

241

Table 2. Osteoarthritic score location in joint showing total change by stage of 5 joints

anterior I

0 medial

I 0.4

0.4

0 I 0.4 0.2 0.2

0.2 0.2

lateral

posterior Histological scoring (control) anterior 0 2.8

2.2

3.4

3.2

3.2

3.0

2.2

0.8

2.4 medial

lateral

~osterior Histological scoring (operated) The scoring on the experimental (operated) side is statisticallysignificantly different from control (p < 0.001).

the previous concept that residual articular cartilage has less potential for wound repair, b u t greater potential exists in the bone marrow. HOCHMAN & LASKIN7, however, using rabbits, reported that surgical defects of the mandibular condyle were completely repaired by both adjacent cartilage and repairing tissue from the marrow space. The difference in the repairing process is attributable to different characteristics of the animals: rabbits have a greater potential for intrinsic repair of bone and cartilage defect, while humans have less 1°. In this respect sheep are similar to humans, therefore the choice of animal is important in these experi-

Fig. 6. Histological appearance of a disc-condylar adhesion showing capillary formation in the adhesion. D: disc, C: condyle, HE, x 10.

242

Ishimaru et aL

Table 3. Thickness of articular soft tissue in temporal bone Anterior

Central

Posterior

Lateral operated control

0.62 0.42-1.22) 0.21 0.19-0.34)

0.56 (0.30 0.84) 0.16 (0.12-0.23)

0.55 (0.23 0.81) 0.10 (0.04-0.74)

Center operated control

0.38 9.24-0.69) 0.18 0.12-0.25)

0.39 (0.20 0.84) 0.19 (0.11-0.28)

0.41 (0.20 0.70) 0.13 (0.04-0.19)

Medial operated control

0.48 0.27-0.72) 0.13 0.10 0.15)

(0.44 (0.27-0.68) 0.15 (0.12-0.22)

0.56 (0.23-0.74) 0.15 (0.08 0.30)

Measurement in ram, n = 5. There was increased thickness of the articular surface on the experimental (operated) side compared to the control side (p < 0.001).

ments, so t h a t the biological changes parallel h u m a n disease. This study illustrates the effect o f a situation similar to i n t r a a r t i c u l a r fracture of the condyle, either m i c r o f r a c t u r e f r o m repeated overloading, o r fracture from acute m a n d i b u l a r t r a u m a . T h e defect in the c o n d y l a r surface allows the ingress o f synovial fluid, u n d e r pressure, into the m a r r o w space. This results in a reaction in the m a r r o w space, w i t h destruction of cancellous b o n e a n d form a t i o n o f subcortical cysts. D u r i n g the repair process osteophytes which emerge f r o m the p e r f o r a t i o n are formed, a n d either a t t e n u a t e or perforate the previously n o r m a l disc. T h e r e are also reactive changes in the t e m p o r a l surface. A n o t h e r effect of surgical penet r a t i o n in the m a r r o w was m a r k e d b o n e remodeling. Such b o n e r e m o d e l i n g was observed at the periphery, a n d was the m a i n cause of the d e v i a t i o n in the f o r m of the condyle. Similar changes are seen in h u m a n T M J OA. This experiment shows t h a t intraarticular fracture, w i t h leakage o f synovial fluid into the m a r r o w space, results in severe o s t e o a r t h r i t i c changes. Some healing occurs p r e d o m i n a n t l y f r o m the m a r r o w space, b u t the resultant j o i n t s show considerable deviation, b o t h in f o r m a n d function, f r o m normal. References 1. ALTMAN RD, HOWELL DS, MUNIZ OE, DEAN DD. The effect of glycosaminoglycan polysulfuric acid ester on articular

cartilage in experimental arthritis. J Rheumatol (Suppl.) 1987: 14:112%9. 2. BOSANQUET A, [SHIMARU JI, Goss AN. Effect of experimental disc perforation in sheep temporomandibular joints. Int J Oral Maxillofac Surg 1991: 20: 170-5. 3. BOSANQUETAG, Goss AN. The sheep as a model for temporomandibular joint surgery. Int J Oral Maxillofac Surg 1987: 16:600 3. 4. EHRLICH MG. Degenerative enzyme systems in osteoarthritic cartilage. J Orthop Res 1985: 3:170 84. 5. Goss AN, BOSANQUETAG. The arthroscopic appearance of acute temporomandibular joint trauma. J Oral Maxillofac Surg 1900: 48: 780-3. 6. HANSSONT, NORDSTROMB. Thickness of the soft tissue layers and articular disc in temporomandibular joints with deviation in form. Acta Odont Scand 1977: 35: 281 8. 7. HOCHMAN LS, LASKIN DM. Repair of surgical defects in the articular surface of the rabbit mandibular condyle. Oral Surg 1965: 19: 534-42. 8. HOWELL DS, CARRENO MR, PELLETIER JP, MUNIZ OE. Articular cartilage breakdown in a lapin model of osteoarthritic cartilage. J Orthop Res 1985: 3: 17~84. 9. ISHIMARU J-I, GOSS AN. A preconditioned osteoarthritic temporomandibular joint model. J Oral Maxillofac Surg 1991 (in press). 10. ISHIMARUJ-I, KURITA K, HANDA Y, GOSS AN. Temporomandibular joint osteoarthritis. Literature review and experimental animal models. Hosp Dent (Tokyo) 1991: 3: 64-8. 11. KoPP S, MEJERSJ()C, CLEMENSSONE. Induction of osteoarthrosis in the guinea pig knee by papain. Oral Surg 1983: 55: 259 66. 12. MARCIANI RD, WHITE DK, TRAURIGHH,

ROTH GI. Healing following condylar shave in the moneky temporomandibular joint. J Oral Maxillofac Surg 1988: 46: 1071-6. 13. MEACHIM G, BROOKE G. The pathology of osteoarthritis. In: MOSKOWlTZRW, ed. Osteoarthritis: diagnosis and management. Philadelphia: WB Saunders, 1984: 2942. 14. MOSKOWITZRW. Introduction. In: MOSKOWlTZ RW, ed. Osteoarthritis: diagnosis and management. Philadelphia: WB Saunders, 1984: 1-6. 15. MUIR C, Goss AN. The radiological morphology of painful temporomandibular joints. Oral Surg 1990: 70: 355-9. 16. PELLETIER JP, MARTEL-PELLET1ER J, ALTMAN RD, GNANDUR-MNAYMEH L, HOWELL DS, WOESSNERJF. Collagenolytic activity and collagen matrix breakdown of articular cartilage in the PondNuki model of osteoarthritis. Arthritis Rheum 1983: 26:866 74. 17. PEYRON JG. The epidemiology of osteoarthritis. In: MOSKOWITZRW, ed. Osteoarthritis: diagnosis and management. Philadelphia: WB Saunders, 1984: 9-27. 18. RADIN EL, ROSE RM. Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop 1986: 213: 34-40. 19. RICHARD LC, LAU E, WILSON DF. Histopathology of mandibular condyle. J Oral Pathol 1984: 14: 624-30. 20. TOLLER PA, GLYNN LE. Degenerative disease of the mandibular joint. In: COHEN B, KRAMMER IRH, eds. Scientific foundation of dentistry. London: Heineman, 1976:605 16.

Address: Prof. A. N. Goss Oral and Maxillofacial Surgery Unit Department of Dentistry The University o f Adelaide G.P.O. Box 498 Adelaide 5001 South Australia