Synovitis

* The clinical and aspiration cytologic details of a case of temporomandibular joint pigmented villonodular synovitis are presented and correlated with imaging, surgical, histopathologic, and clinical follow-up findings; the origin of such lesions is discussed. The lesion originally presented in a 36-year-old, otherwise healthy, white man as a unilateral mass involving the temporal fossa and temporomandibular joint region. The tumor's extent was defined by magnetic resonance imaging and computed tomographic scan; there was destruction of the temporomandibular joint and erosion of the temporal cranial bones by a lesion whose maximum dimensions were estimated by imaging to be 2.75 x 3.25 cm. The lesion was initially sampled and classified by computed tomography-guided fine-needle aspiration biopsy. Following complete resection, the original diagnosis was confirmed with both hematoxylin-eosin-stained paraffin sections and immunohistochemical staining. The patient remains free of disease 7 years postoperatively.

(Arch Pathol Lab Med. 2002;126:195-198)

Pigmented villonodular synovitis (PVNS) is an uncommon inflammatory, reactive, and pseudoneoplastic condition of unknown etiology affecting synovial-lined joints. Pigmented villonodular synovitis was originally described by Jaffe et all and is recognized as occurring in 2 forms: a diffuse variant, usually found in the knees; and the more common nodular version, found mainly in the hands and wrists.2 This lesion is exceedingly rare in the temporomandibular joint, with only 13 cases reported to date in the English literature.3 In only 3 other cases was the diagnosis made by fine-needle aspiration biopsy (FNAB) .5-7 We report the FNAB diagnosis of an additional case characterized by extensive local destruction of the right temporomandibular joint, extension through the regional skull into the cranial cavity, and with impingement on the dura mater. We discuss the challenge such lesions present to the aspiration cytopathologist and review the cytomorphology and clinical manifestations of the initial presentation. We also comment on the results of magnetic resonance imaging (MRI) and computed tomography (CT), the surgically demonstrated extent, as well as the histomorphology, key immunohistochemical staining characteristics, and the possible origins of this lesion.

REPORT OF A CASE

An otherwise healthy 36-year-old white man presented to his family doctor with a slowly enlarging, painless, right temporal area mass. He had experienced some hearing loss, an occasional popping sensation in the right ear, and a clicking noise in the right temporomandibular joint. No other data from the patient's medical history were pertinent. Physical examination revealed a fixed, nontender, firm mass in the right temporal fossa with extension into the infratemporal/preauricular/parotid region. The range of motion of the mandible and right temporomandibular joint was unaffected; the remainder of the physical examination was unremarkable. Magnetic resonance imaging and CT studies demonstrated a mass with a pushing border in the right temporal region with infratemporal fossa involvement (Figures 1 and 2). Temporal bone destruction permitted intracranial extension; there was concern about transgression of the dura.

The medical history, physical examination, and imaging studies all were thought to reveal a malignant process. A CT-guided FNAB done at presentation revealed a "giant cell-containing lesion" and an interpretation that the process was not malignant. An exact diagnostic classification of the lesion was not given, and PVNS was suggested as a possibility. The differential diagnosis for this cytomorphologically benign lesion included villonodular synovitis, giant cell reparative granuloma, and benign chondroblastoma. After the lesion was embolized, it was surgically exposed through a combined right frontal-temporal craniotomy and infratemporal approach. A light brown mass was found infiltrating the muscles of the pterygopalatine fossa and involving the joint capsule of the temporomandibular joint. The mass extended through the skull and was attached to the temporal dura and lateral wall of the eustachian tube. In spite of its extent, the lesion was completely excised. The patient's postoperative course was unremarkable; there were no functional losses, and he remains healthy and free of disease at 7 years after surgery.

MATERIALS AND METHODS

Cytologic smears of the CT-guided FNAB-obtained material were air-dried for initial evaluation using Diff-Quick stain (Dade-- Behring, Inc, Newark, Del); the counterparts of these slides were fixed with ethanol for Papanicolaou staining (Richard-Allan Scientific, Kalamazoo, Mich). Needle rinses in CytoLyt, subsequently fixed in 10% buffered zinc formalin, were used to make a cell block, sections from which were stained with hematoxylin-eosin. Fresh tissue obtained at the time of surgery was fixed in 10% buffered zinc formalin and routinely processed for sectioning and staining with hematoxylin-eosin. Representative sections of the surgical resection specimen were fixed in formalin, embedded in paraffin, and stained with hematoxylin-eosin, as well as immunohistochemically using a diaminobenzidine method, with antibodies directed against 5100 protein (used here as a marker for cells of chondrocytic origin), CD45 (leukocyte common antigen), and CD68 (a macrophage-monocyte marker).

RESULTS

The FNAB preparations contained sheets of round, spindled, and multinucleated cells; the individual round to oval cells had sparse cytoplasm surrounding slightly eccentrically placed nuclei. The nuclei, in all 3 cell types, had a diffuse chromatin pattern without atypia. A few cells had cytoplasm containing granular golden-brown pigment (Figures 3 through 5). The multinucleated giant cells contained variable numbers of small round to oval, bland nuclei. Atypia and mitoses were not present.

The formalin-fixed, paraffin-embedded, hematoxylineosin-stained sections of the resected lesion revealed polygonal to spindle-shaped stromal cells with admixed multinucleated giant cells (Figure 6). The giant cells were variable in size and concentration throughout the lesion and contained 10 to 70 nuclei per cell. Mitotic activity was inconspicuous in both the stromal and the giant cells. Collagen bands divided the lesion into nodules, and bone was found entrapped within the lesion. Hemosiderin was focally prominent in some fields but was absent in others. In some areas, the stromal cells appeared to reside within lacunae embedded in a hyalinized matrix, focally producing a remarkable similarity to chondroblastoma. There was no reaction with antibodies directed against S100 protein and leukocyte common antigen, while staining with the monocyte-macrophage marker CD68 was globally strongly positive in both the stromal and giant cells. A postoperative CT scan revealed apparent complete excision of the lesion (Figure 7).

COMMENT

Pigmented villonodular synovitis is a relatively rare lesion preferentially affecting selected synovial joints. The lesions name was originally proposed by Jaffe et al in 1941; in an attempt to clarify the relationship between similar lesions of the tendon sheath, bursa, and synovium. Pigmented villonodular synovitis occurs in nodular and diffuse forms. .2 Synonyms for the more common nodular variants are xanthoma, xanthogranuloma, giant cell tumor, and myeloplaxoma; these lesions generally affect only a small areas of the synovium. Grossly, the lesion is typically a yellowish-brown sessile or stalked outgrowth of the synovium. Many cases of the nodular lesion are located in the hand or finger.2

The diffuse form tends to affect the entire synovial membrane and has variously been called chronic hemorrhagic villous synovitis, giant cell fibrohemangioma, and benign polymorphocellular tumor of the synovium.14 It is most often found in the knee and grossly consists of a red-brown, shaggy, matlike growth composed of fine, long, tangled villous structures. In the diffuse form, round, spindled, and multinucleated giant cells are observed either singly or in sheets. Cellular atypia and mitoses typically are absent in both types. Coarse intracytoplasmic hemosiderin-- like pigment may be present in the round or oval cells.

The histopathology of both forms is essentially similar and explains what is observed in cytologic preparations. A lining of synovial cells covers the villi and may vary in thickness from 1 to 3 cell layers. The concentration of the stromal cells beneath this synovial lining varies within the lesion. In areas of increased cellularity the stromal cells are usually polygonal and contain round vesicular nuclei. In areas of sparse cellularity, the stromal cells have a more spindled shape and the extracellular matrix can be hyalinized or chondroid.12 Mitoses may be found, especially in areas of higher cellularity, but atypism does not occur in benign lesions.12 Multinucleated giant cells in varying numbers are a characteristic feature. Hemosiderin pigment is present as well and is usually found concentrated in the stromal cells. Immunohistochemical analysis demonstrates that most of the stromal cells, including the multinucleated giant cells, are of the mononuclear/macrophage lineage,-10 even though some investigators dispute this conclusion and consider the lesion to be of "synovial" origin."

Until lately, the precise nature of the cells comprising PVNS has remained obscure. Recent studies of the histogenesis of PVNS, using electron microscopy and further immunohistochemical analysis, support the concept that these lesions are of monocyte/macrophage origin." This study revealed the tumor cells are macrophages ultrastructurally, and that they express epitopes detected by antibodies to CD68, HAM56, and vimentin, but not with antibodies to cytokeratins, epithelial membrane antigen, 5100, HMB-45, leukocyte common antigen, CD34, desmin, or smooth muscle actin.9-11 Recent cytogenetic studies of a PVNS-like "tenosynovial giant cell tumor" in the shoulder region of a young woman revealed a clonal population characterized as 45XX,t(1:2)(pter-p22::q24-pter, t(1: 14)(qter-pl3::q13-ter).12 In addition, Layfield et a113 studied 2 cases of apparently malignant PVNS and found consistent aneuploidies involving chromosomes 5 and 7. Whether either one of these cytogenetic findings is true of all PVNS, and of temporomandibular joint PVNS in particular, remains to be seen.

The cytologic findings of PVNS are distinctive enough to permit suspicion for the lesion, if not its outright recognition; these characteristics have been discussed by Wakely and Frable,14 as well as by Layfield.15 In FNAB smears, there is considerable cellularity and cohesion. Stromal cells are round or oval, with foamy cytoplasm, a rounded nucleus with a vesicular chromatin pattern, and a small nucleolus. Variable numbers of cells will have intracytoplasmic granular, golden, hemosiderin-like pigment. Smaller, spindled stromal cells augment the background. Variable numbers of multinucleated giant cells of various sizes, apparently derived from the mononucleated stromal cells, are present. These cytomorphologic findings are the counterparts of this lesions histopathology. Also, these findings are virtually identical with FNAB material obtained from so-called giant cell tumor of tendon sheath origin.10 Using cytologic material, immunohistochemical marker studies also confirm the histomorphological and immunohistochemical suspicion that the stromal cells are of mononuclear/macrophage rather than chondroblast origin. This distinction is important, as PVNS can be associated with synovial chondromatosis," the latter apparently being a metaplastic response to chronic injury.

While these cytomorphologic features are shared with giant cell tumors of bone, which are bona fide neoplastic lesions, the distinction usually can be made between these 2 entities based on the mitotic rate of the stromal component, which can be quite high in giant cell tumors of bone. Pigmented villonodular synovitis also shows a more variable distribution of the giant cells. Reparative granulomas are typically characterized by a loose collagenous stroma with increased small vascular structures, features not seen in our material. As with all bone and joint lesions, clinicopathologic correlation with imaging studies is essential to proper diagnosis. Clearly, bone and joint lesions with such cytomorphologic features require at least the inclusion of PVNS in the differential diagnosis.

Pigmented villonodular synovitis of the temporomandibular joint is rarely discussed in the radiology literature.3,16 From the radiologists perspective, PVNS more commonly affects large joints, usually the knee. The appearance of PVNS on MRI is often characteristic; it presents as a heterogeneous synovial process that extends away from the joint space. A long TR/TE sequence will accentuate the low signal intensity contained within the mass because of the shortening of T2 relation time of hemosiderin. As with the cytomorphologic features, MRI signal intensity characteristics of PVNS and giant cell tumor of tendon sheath are similar. 17 While the MRI appearance of the temporal mass in this case is in keeping with PVNS, the location and extent made the diagnosis unclear, prompting the CT-guided FNA study.

Temporomandibular joint PVNS is exceedingly rare. The first 2 cases were reported in 1973 by Lapayowker et al.3 Since then, an additional 10 cases have been reported,4 most of which were reviewed by Eisig et al.111 Prior to our report, we are aware of only 3 other reports of FNAB-- diagnosed temporomandibular joint PVNS, -7 as well as 1 FNAB diagnosis of the morphologically similar giant cell tumor of tendon sheath origin." Herein, we report an additional example presenting as a large, seemingly malignant, destructive, temporal/infratemporal mass.

Our experience, as well as that of others, suggests that FNAB is an important alternative to open biopsy prior to surgery because it provides reliable and valuable information at minimum cost and with limited invasiveness. Therefore, FNAB is an approach likely to be used with increasing frequency. In this case, the technique provided a differential diagnosis composed of benign lesions, whereas medical history, physical examination, and imaging findings indicated a malignant process. Obviously, the type of surgery planned is altered significantly when a lesion such as this is recognized as benign. Such preoperative information will alleviate much of a patient's anxiety.

Accepted for publication July 12, 2001.

References

1. Jaffe HL, Lichtenstein L, Sutro CJ. Pigmented villonodular synovitis, bursitis and tenosynovitis: a discussion of the synovial and bursal equivalents of the tenosynovial lesion commonly denoted as xanthoma, xanthogranuloma, giant cell tumor or myeloplaxoma of the tendon sheath, with some consideration of this tendon sheath lesion itself. Arch Pathol. 1941;31:731-765.

2. Docken WP. Pigmented villonodular synovitis: a review with illustrative case reports. Semin Arthritis Rheum. 1979;9:1-22.

3. Lapayowker MS, Miller WT, Levy WM, Harwick RD. Pigmented villonodular synovitis of the temporomandibular joint. Radiology. 1973;108:313-316.

4. Barnard JDW. Pigmented villonodular synovitis in the temporomandibular joint: a case report. Br] Oral Surg. 1975;13:183-187.

5. Dawiskiba S, Eriksson L, Elner A, Johansen CC, Hansson LG, Westesson PL. Diffuse pigmented villonodular synovitis of the temporomandibular joint diagnosed by fine needle aspiration cytology. Diagn CytopathoL 1989;5:301-304.

6. Yu GH, Staerkel GA, Kershisnik MM, Varma DG. Fine-needle aspiration of pigmented villonodular synovitis of the temporomandibular joint masquerading as a primary parotid gland lesion. Diagn Cytopathol. 1997;16:47-50.

7. Tanaka K, Suzuki M, Nameki H, Sugiyama H. Pigmented villonodular synovitis of the temporomandibular joint. Arch Otolaryngol Head Neck Surg. 1997; 123:536-539.

8. Jozsa L. Immunohistochemische Befunde bei pigmentierter villonodularer Synovialitis (Immunohistochemical characterization of pigmented villonodular synovitis]. Zentralbl Pathol. 1992;138:119-123.

9. Nielsen AL, Kiaer T. Malignant giant cell tumor of synovium and locally destructive pigmented villonodular synovitis: ultrastructural and immunohistochemical study and review of the literature. Hum Pathol. 1989;20:765-771.

10. Somerhausen NS, Fletcher CD. Diffuse-type giant cell tumor: clinicopathologic and immunohistochemical analysis of 50 cases with extraarticular disease. Am J Surg Pathol. 2000;24:479-492.

11. O'Connell JX, Fanburg JC, Rosenberg AE. Giant cell tumor of tendon sheath and pigmented villonodular synovitis: immunophenotype suggests a synovial origin. Hum Pathol. 1995;26:771-775.

12. Layfield LJ, Meloni-Ehrig A, Shepard R, Harrelson JM. Malignant giant cell tumor of synovium (malignant pigmented villonodular synovitis). Arch Pathol Lab Med. 2000;124:1636-1641.

13. Gonzalez-Campora R, Salas Herrero E, Otal-Salaverri C, et al. Diffuse tenosynovial giant cell tumor of soft tissues: report of a case with cytologic and cytogenetic findings. Acta Cytol. 1995;39:770-776.

14. Wakely PE Jr, Frable WJ. Fine-needle aspiration biopsy cytology of giant-- cell tumor of tendon sheath. Am J Clin Pathol. 1994;102:87-90.

15. Layfield LJ. Aspiration cytologic diagnosis of bone tumors: morphology and clinical-radiographic correlates. In: Schmidt WA, ed. Cytopathology Annual. Vol 4. Chicago, III: ASCP Press; 1996.

16. Song MY, Heo MS, Lee SS, et al. Diagnostic imaging of pigmented villonodular synovitis of the temporomandibular joint associated with condylar expansion. Dentomaxillofac Radiol. 1999;28:386-390.

17. Spritzer CE, Dalinka MK, Kressel HY. Magnetic resonance imaging of pigmented villonodular synovitis: a report of two cases. Skel Radiol. 1987;16:316319.

18. Eisig S, Dorfman HD, Cusamano RJ, Kantrowitz AB. Pigmented villonodular synovitis of the temporomandibular joint: case report and review of the literature. Oral Surg Oral Med Oral Pathol. 1992;73:328-333.

Steven L. Shapiro, MD; Sean O. McMenomey, MD; Priscilla Alexander, MD; Waldemar A. Schmidt, PhD, MD

From the Departments of Pathology (Drs Shapiro and Schmidt), Otolaryngology (Dr McMenomey), and Radiology (Dr Alexander), School of Medicine, Oregon Health Sciences University, Portland, Ore. Dr Shapiro is now with the Queen's Medical Examiners' Office, New York, NY.

Reprints not available from the authors.

Copyright College of American Pathologists Feb 2002
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