Temporomandibular joint osteoarthritis and crystal deposition diseases: a study of crystals in synovial fluid lavages in osteoarthritic temporomandibular joints

Copyright 9 Munksgaard 1998

Int. J. Oral Maxillofac. Surg. 1998; 27:268-273 Printed in Denmark. All rights reserved

lnm*'nauonalJoumal of

Ord Max ofacial Surgery ISSN 0901-5027

Aesthetic and reconstructivesurgery

Temporomandibular joint osteoarthritisand crystal deposition diseases: a study of crystals in synovial fluid lavages in osteoarthritic temporomandibular joints

Leonore C. Dijkgraaf 1, Robert S. B. Liem =, Lambert G. M. de Bont 1 1TMJ Research Group, Department of Oral and Maxillofacial Surgery, University Hospital Groningen; PI'MJ Research Group, Laboratory for Cell Biology and Electron Microscopy, University of Groningen, Groningen, The Netherlands

L. C. Dijkgraaf, R. S. B. Liem, L. G. M. de Bont: Temporomandibular joint osteoarthritis and crystal deposition diseases: a study of crystals in synovial fluid lavages in osteoarthritic temporomandibular joints. Int. J. Oral Maxillofac. Surg. 1998; 27." 268-273. 9 Munksgaard, 1998 Abstract. To study the presence of crystals in synovial fluid lavages of osteoarthritic temporomandibular joints (TMJs), in order to evaluate the possible role of these crystals in the osteoarthritic (OA) process, synovial fluid lavage samples of the upper joint compartment from 44 TMJs were obtained prior to arthroscopy. The OA group consisted of 32 TMJs. The control group consisted of 12 TMJs that had been diagnosed with other nonosteoarthritic conditions. The lavage samples were analysed as wet preparations, unstained and stained, with ordinary light, polarized light and compensated polarized light for the presence of crystals and white blood cells. One sample was prepared for subsequent electron microscopic (EM) examination. Synovial fluid lavage analysis of osteoarthritic TMJs did not show any monosodium urate monohydrate or calcium pyrophosphate dihydrate crystals. However, in three lavages, particles which possibly contained calcium were identified with alizarin red S staining. White blood cells were occasionally seen. Synovial fluid analysis of the lavages of the control TMJs did not reveal any crystals. EM examination of synovial fluid lavage from an osteoarthritic TMJ failed to clearly show crystal formation. Concurrence of TMJ crystal deposition and OA appears less prominent than in other synovial joints. We conclude that crystals probably do not play an important role in TMJ OA.

Concurrence of crystal deposition and osteoarthritis (OA) in synovial joints, in general, is well known 10,13,52. It is still unknown whether crystal deposition in OA is a result, a contributing factor, or possibly both. Three crystal types have been predominantly found: monosodium urate monohydrate (MSUM), cal-

cium pyrophosphate dihydrate (CPPD), and basic calcium phosphates (BCPs). BCPs encompass hydroxyapatite, tricalcium phosphate, and octacalcium phosphate. Deposits of MSUM, CPPD, and BCPs can also form in the absence of OA. These are clinically associated with acute or chronic gouty arthritis

Key words: temporomandibular joint; osteoarthritis; crystals; synovial fluid. Accepted for publication 6 January 1998

(MSUM deposition), acute pseudogout or chronic pyrophosphate arthropathy (CPPD deposition), and acute periarthritis or chronic destructive joint disease (BCP deposition) 14'43. However, mixtures of several different types of crystals are frequently found in crystal deposits 15. MSUM deposition is highly

T M J osteoarthritis and crystals related to hyperuricemia, i.e. a supersaturation for urate in serum, which is caused by a generalized metabolic abnormality 14,43. Urate is an endproduct of human purine metabolism. Although hyperuricemia predisposes individuals to gout, it should be noted that hyperuricemia may remain asymptomatic and does not necessarily result in M S U M deposition or clinical symptoms. Because hyperuricemia is a generalized disorder, precipitation of M S U M could occur anywhere. The site is decided by secondary local tissue factors that promote crystallization]a. In contrast to M S U M deposition, deposition of other crystal types is predominantly caused by a localized disorder, frequently a local increase in metabolic activity or loss of inhibition of crystallization. CPPD deposition is probably caused by an increased production of inorganic pyrophosphate by local chondrocytes. Inorganic pyrophosphate is produced in many intracellular reactions, including the pyrophosphorylysis of nucleotide triphosphates during biosynthesis of cell components and matrix-destined molecules43. Relatively little is known of BCP deposition. Research has been hampered by the small size of the crystals and their strong tendeney t o occur in mixtures with other crystals 14. In the temporomandibular joint (TMJ), crystal deposition appears to be quite rare. Only few reports on M S U M deposition4"23'26'27,32'39,48,54,55 and CPPD deposition t 1,12,16,17,30,32,36-3s,40,42,44,49-51, 57,58 have appeared in the literature. Recently, hydroxyapatite deposition has been described in the TMJ in a patient with renal failure 5. In synovial membrane of osteoarthritic TMJs, a few hydroxyapatite-like crystals were found in an ultrastructural study Is. Obvious concurrence of crystal deposition diseases and OA of the TMJ has never been reported. In synovial fluids of osteoarthritic knee joints, CPPD and BCP crystals have frequently been demonstrated 9,24,25,29,33,35,41,46,56. A mixture of CPPD and BCP crystals was found more often than either alone 33. CPPD and BCP crystals correlated with the patient's age and joint degeneration, respectively9'29'33'35'46. Although TMJ OA occurs at a young age (20s and 30s), arthroscopically and microscopically it is characterized by degeneration ]9,2~ The aim of this study was to study the presence of crystals in synovial fluid

lavages of osteoarthritic TMJs, in order to evaluate the concurrence of crystal deposition and OA and the possible role of these crystals in the osteoarthritic process. Material and methods SynovlMfluld 18v~ sampleu~ecth~n Synovial fluid lavage samples were obtained prior to arthroscopy of the upper joint compartment from 44 TMJs, including both osteoarthritic and nonosteoarthritic (control) TMJs. The OA group consisted of 32 TMJs (26 women, 6 men; mean age, 31.2_+9.3 years) that had been diagnosed with TMJ OA. The control group consisted of 12 TMJs (9 women, 3 men; mean age, 29.7• years) that had been diagnosed with other nonosteoarthritic conditions, including painful hypermobility and overloading. The sex ratio and mean age did not differ significantly between the OA and the control group. Exclusion criteria for both groups had included the presence of TMJ growth disorders, other forms of arthritis, the presence of systemic connective tissue disorders, as well as the presence of nonarticular disorders in the oral and maxillofacial area. Additional exclusion criteria were previous TMI surgery and intracapsular injections of corticosteroids. For each TMJ, the duration of clinical signs and symptoms was recorded. Arthroscopy was performed with the patients under general anaesthesia via nasoendotracheal intubation and under optimal neuromnscular relaxation. The joint anatomy was palpated during ventral-dorsal joint movement to identify the maximum concavity of the glenoid fossa. Subsequently, a 19-gauge needle on a l ml syringe was introduced into the posterior recess of the upper joint compartment, while the condyle was held in maximum ventral position. As lavage fluid, 1 ml water for injection (B. Braun Melsungen AG, Melsungen, Germany) was used. This sterile, bidistilled water was injected and aspirated at least five times, allowing sufficient intervening time for an equilibrium to arise. Lavage samples that macroscopically demonstrated contamination with blood were excluded from this study. Ten of the 32 synovial fluid lavages of ostcoarthritic TMJs and two of the 12 synovial fluid lavages of the control group were mixed immediately with a fixative containing 2% paraformaldehyde and 0.5% glutaraldehyde in a 0.1 M phosphate buffer (pH 7.4). All samples were refrigerated until analysis. Arthroscopically, the presence of various variables was recorded, including degeneration of the articular cartilage, and hypervascularity, hyperemia, and redundancy of the synovial tissues-.The synovial fluid lavage samples were analysed immediately postoperatively. Synovlal fluid lavage sample analysis Synovial fluid lavage samples were analysed as wet preparations, unstained and stained,

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with ordinary fight, polarized light and compensated polarized light; A drop of lavage was placed on a precleaned slide, covered with a clean coverslip and examined with ordinary light microscopy (LM) and polarized LM without and with a first order red compensator to identify MSUM and CPPD crystals by their morphology and sign of birefringenee. For BCP crystal identification, a drop of iavage was mixed on a slide with a drop of filtered(0.22/an pore size) 2% alizarin red S stain solution (pH 4.2) and subsequently examined with ordinary LM. Wright's stain was used to identify crystals and white blood cells, whilst methylene blue stain was used to stain white blood cells. Each separate identification was performed at least five times by two investigators. Two samples of the unfixed and two of the fixed osteoarthritic synovial fluid lavages were centrifuged prior to analysis. Based on light microscopic fndings, one of the synovial fluid lavages containing alizarin red S positive staining was selected for subsequent electron microscopic examination. The remaining synovial fluid lavage was fixed with a fixativecontaining 2% paraformaldehyde and 0.5% glutaraldehyde in a 0.1 M phosphate buffer (pH 7.4), and centrifuged at 2000 rpm. After removal of the fixative, the pellet was washed with washing solution (0.1 M phosphate buffer, pH 7.4) in a water bath at 50~C. A few drops of 2% agar at 50~ were added to the pellet and shaken to suspend the pellet components into the agar, following which it was centrifuged. The newly formed pellet was cut into small blocks that were postfixed for one hour with 1% osmium tetroxide and embedded in Epon. Semithin sections of 1/an thickness were cut and studied by LM to identify the areas of interest. Subsequently, ultrathin sections 40-60 nm thick were cut with a diamond knife and mounted on copper grids. The sections were stained with uranyl acetate and lead citrate, and examined by electron microscopy (EM). A correlation between the presence of synovial fluid calcific material and arthroscopically scored cartilage degeneration was analysed with Cohen's Kappa. Results Synovial fluid analysis of the fixed and unfixed lavages of the osteoarthritic TMJs did not reveal any M S U M or CPPD crystals with ordinary or polarized light. Alizarin red S staining, however, demonstrated in three lavages (9%) several deeply stained clumps suggestive of calcium-containing particles. With polarized light, these particles were brightly birefringent (Fig. 1). White blood cell staining in the unfixed lavages showed only remnants of leukocytes. White blood cell staining in the fixed lavages did show several intact leukocytes, although no intracytoplasmic inclusions such as crystal-like

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D i j k g r a a f et al.

/

p

B Fig. 1. A) Alizarin red S positive stainjng, showing bright birdringcner (arrow) with polarized light (Alizarin red S stain x160). B) Same as

in (A), under compensated polarized light.

u

A

[3

Fig. 2. A) Alizarin redS negative staining, showing two highly bkefringent starehlike particles (arrowheads) with polarized light (Alizarin red

S stain • 160). B) Same as in (A), under compensated polarized light.

particles were found. Erythrocytes were generally observed in every lavage. Finally, in four samples, several particles were found with polarized light, showhag a strongly birefringent beach ball/ maltese cross appearance suggestive of starch globules (Fig. 2). In the centrifuged synovial fluid lavage samples, no identifications could be made because of the clustering of ceils and particles. Synovial fluid analysis of the lavages of the control TMJs did not reveal any crystals, but erythroeytes and occasional lenkocytes were observed. EM examination of one synovial fluid lavage of an osteoarthritic TMJ, demonstrating alizarin red S positive staining, did not convincingly show the presence of crystals. No correlation could be found be-

tween the presence of synovial fluid calcific particles and arthroscopically scored cartilage degeneration. Discussion

Synovial fluid lavage analysis of osteoarthritic TMJs did not show any MSUM or CPPD crystals, while with alizarin red S staining the presence of possibly calcium-containing particles was identified in only three lavages. Alizarin red S staining is nonspecific for individual crystal species but is a useful screening stain for calcitic material. Staining at acidic pH (4.2) increases its specificity for hydroxyapatite but is still insufficient for definite characterization. The presence of hydroxyapatite crystals, which are BCP crystals, in syn-

ovial fluids from osteoarthritic knee joints has been related to the severity of joint damage in OA 9'24'29'33'35'46. Yet the relative incidence of crystal deposition in OA, other joint diseases, and normal control groups has not yet been established ~3. Alizarin red positive particles, however, as well as birefringent crystals, have also been found in synovial fluids obtained from normal knee joints and even at a higher frequency than found in the lavages of osteoarthritic TMJs in the present study 24. Concurrence of TMJ crystal deposition and OA appears, therefore, less prominent than in other synovial joints and crystals probably do not play an important role in TMJ OA. Crystals in synovial fluid may have been derived from three possible

T M J osteoarthritis and crystals sources ~3. First, the crystals may be wear particles from the normally calcified cartilage zone or underlying bone that has been exposed through tissue damage in OA. Second, the crystals may have originated from abnormal cartilage mineralization and subsequent shedding. In osteoarthritic articular cartilage, active chondrocytes have been shown to form matrix vesicles that act as nucleation sites for aggregates of apatite crystals 2. In the deeper layers of TMJ osteoarthritic cartilage, matrix vesicles have been shown to contain apatite crystals 6. These were predominantly found in the region adjoining the calcified cartilage zone as well as in this calcified cartilage zone itself. In normal articular cartilage, mineralization is inhibited by several factors, including avascnlarity ~4. In this respect, the arthroscopic finding of angiogenesis 19, i.e. neovascularization, of the articular eminence is quite si~ificant. Third, crystals in synovial fluid may have been derived from areas of metaplasia in the synovial membrane or joint capsule, but there is little evidence to support this concept. A recent study, however, of so-called rice bodies, which are supposedly synovium-derived endoarticnlar loose bodies, in synovial fluid from osteoarthritic knee joints, showed that these were composed of fibrin as well as numerous intra- and extracellular apatite and CPPD crystals s. They contained synovial intima cells and few inflammatory ceils, as well as collagen fibres, chondrocytes and other cartilage components. A study of loose endoarticnlar bodies in pathologic TMJ synovial fluid, however, failed to demonstrate the presence of hydroxyapatite in these bodies, but showed that they were composed of calcite 47. In our opinion the presence of crystals in loose bodies in the synovial fluid does not directly imply synovial or capsular metaplasia until the origin of these bodies has been identified. A correlation between the presence of calcific material in the TMJ synovial fluid lavages and arthroscopically scored cartilage degeneration could not be demonstrated in this study. This was probably caused by the limited number of lavages demonstrating these crystals. One of the two problems with this study was the dilution of TMJ synovial fluid through the lavage. The average volume of synovial fluid of pathologic TMJs is 37/zl 1. Because this volume is too small for fluid to be aspirated, lavage of the

joint was the only way to obtain the TMJ synovial fluid. In this study, 1 ml water for injection was used as lavage fluid rather than saline to prevent de novo sodium chloride crystal precipitation in the slides. Inherent to the use of lavage fluid is the considerable dilution of synovial fluid, which may result in crystal dissolution. It has also yet to be determined what concentration of crystals in TMJ synovial fluid would be considered clinically significant since these crystals have also been found in the synovial fluid of other normal joints. In addition to the dilution problem, an underdiagnosis may have occurred due to the low threshold of reliable crystal identification by LM 31,56. Until now, two methods have been proposed to determine the dilution factor in TMJ synovial fluid lavages m, but both have limitations 2~. In future TMJ synovial fluid analysis for crystals, this dilution problem should be solved and the concentration of crystals that has a clinical relevance should be established. For this reason, the use of additional analytical techniques may be necessary, e.g. nuclide binding 34 or hypochlorite solution 45. Based on the findings in this study, we believe that crystals play only a limited role in the osteoarthritic proceSS.

The second problem with this study was the lapse of time between the moment of lavage and synovial fluid analysis (2-4 hours). It has been shown that leukocyte counts drop after one hour, whereas after six hours they may have been reduced by as much as 50% 53. This may explain why white blood cell staining in the unfixed lavages in this study showed only remnants of leukocytes. However, this could also have been caused by the use of pure water rather than saline as lavage fluid and the consequent difference in osmotic pressure. Overall, only few leukocytes were found. White blood cell counts of less than 2000/mm 3 are generally considered noninflammatory 2s. A white blood cell count was not performed in this study because of the dilution problem mentioned above, and because the leukocytes observed in the lavages may have been derived from blood that had contaminated the lavage due to the manlpnlation of the needle. The presence of erythrocytes, as well as the presence of leukocytes in the control lavages may support this possibility. The absence of increased numbers of leukocytes in the synovial fluid of osteoarthritic TMJs is

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in concurrence with the relative absence of inflammatory cells in the synovial membrane of these TMJs ~. An unexpected finding in the synovial fluid lavages was the presence of starchlike globules, which probably derived from the use of rubber gloves during the arthroscopy. Although starch contamination might have occurred after the lavage, we support the recommendation by BRONS~IN7 regarding glove washing in order to prevent the occurrence of iatrogenically induced starch synovitis. Acknowledgments. The authors wish to thank Dr G. Zardeneta, Department of Oral and Maxillofaeial Surgery, University of Texas Health Science Center at San Antonio, Texas, USA, for his editorial input. References

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Address: Leonore C. Dijkgraaf, DDS, PhD The University of Texas Health Science Center at San Antonio Department of Oral and Maxillofacial Surgery 7703 Floyd Curl Drive San Antonio, T X 78284 USA

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