Diagnosis of Synovial Sarcoma of the Pleura and Differentiation from Malignant Mesothelioma

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1 36 Diagnosis of Synovial Sarcoma of the Pleura and Differentiation from Malignant Mesothelioma Amy Powers and Michele Carbone Synovial sarcomas (SSs) are soft tissue tumors that occur primarily in adolescents and young adults between the ages of 15 and 40 (1). The tumors comprise 5% to 10% of all soft tissue sarcomas, and most commonly arise in extremities in the vicinity of large joints. Rare cases have also been reported in virtually every anatomic site, including the head and neck, lung, heart, mediastinum, abdominal wall, central nervous system (CNS), prostate, and pleura. Synovial sarcomas do not arise from synovium, as the name implies. Instead, they are thought to arise from primitive mesenchymal cells, which explains their development in locations devoid of synovium (1). Synovial sarcomas of the pleura usually represent metastatic disease, but more than 20 primary SSs of the pleura have been reported in the English-language literature, making these tumors a rare but important diagnostic consideration (Table 36.1) (2 10). The origin of pleural synovial sarcomas may be undifferentiated submesothelial mesenchyme, which could undergo differentiation toward epithelial or spindle cells. The rarity of primary synovial sarcoma of the pleura and its morphologic similarity to malignant mesothelioma (MM), the most common primary malignant pleural lesion, make it a difficult and easily overlooked diagnosis. This chapter discusses the differences between the two entities. Clinical History Clinical features can be useful in distinguishing between MM and SS of the pleura. However, because there is considerable overlap between these two entities, clinical findings alone are not always reliable in making a diagnosis of SS versus MM. Synovial sarcomas have no significant gender predilection, while mesotheliomas are more common in males (1). Synovial sarcomas also tend to occur in younger patients. Of 23 primary SSs of the pleura reported in the literature, the average age was 37 (range 9 77). Mesothe- 543

2 544 Chapter 36 Synovial Sarcoma of the Pleura Table Primary pleural synovial sarcomas: clinical and pathological features Author (reference) Patient age Sex Histopathology Molecular studies Jawahar et al (3) 18 F Biphasic t(x;18) Gaertner et al (4) 17 F Biphasic NP 17 F Biphasic NP 50 M Biphasic NP 9 M Biphasic NP 32 F Biphasic NP Aubry et al (2) 33 M Monophasic t(x;18) 41 M Monophasic t(x;18) 41 M Monophasic t(x;18) 49 F Monophasic t(x;18) 69 M Monophasic t(x;18) Nicholson et al (5) 42 M Biphasic NP 28 M Monophasic NP 42 M Monophasic NP Carbone et al (10) 74 M Biphasic t(x;18) Colwell et al (6) 39 M Monophasic Negative 23 F Monophasic t(x;18) 33 M Biphasic Indeterminant Essary et al (7) 30 M Monophasic NP 32 F Monophasic NP Hirano et al (9) 46 F Biphasic NP Ng et al (11) 15 M Monophasic t(x;18) Chan et al (8) 77 F Not Stated NP NP, not performed. liomas, in contrast, typically develop in patients 50 to 70 years of age and are rarely seen in adolescents and young adults. Occasional primary pleural SSs have been reported in older adults, however. Aubry et al (2) reported a monophasic SS in a 69-year-old man, and Carbone et al (10) detailed the development of a biphasic SS in a 74-year-old man. A primary pleural SS in an old individual was also reported by Chan et al (8), but the histologic subtype was not specified. Thus, a diagnosis of SS should not be ruled out based on old age alone. Chan et al suggested that SSs in older individuals (>60 years of age) are more likely to have unusual histologic patterns and poorly differentiated morphology, which can make diagnosis more challenging. In addition, these higher grade lesions are typically associated with aggressive behavior and frequent metastasis. Synovial sarcomas typically grow at a faster rate and present radiologically as a discrete, localized mass with or without associated pleural thickening. A pseudocapsule is occasionally present (4). In contrast, MMs grow slowly, more commonly present as diffuse pleural thickening or multiple pleural nodules, and do not have capsules or pseudocapsules. Localized MMs are extremely rare, and the presence of a localized pleural-based mass should instead raise suspicion of a soft tissue tumor. Pleural effusions, although more common in MM, have been reported in both malignancies and do not reliably rule out SS (4).

3 A clinical history of asbestos exposure in an individual with a pleural-based tumor should raise the suspicion of an MM. However, pleural SSs have also been reported to occur in asbestos-exposed individuals, and one should be cautious not to jump to a diagnosis of MM based on history alone (10). Gross Pathology A thorough macroscopic examination must be performed when differentiating between these malignancies, as they tend to have distinct gross morphologies. Gross examination of 22 reported cases of pleural synovial sarcoma demonstrated both solid and cystic masses ranging in size from 4.5 to 25cm (2 7,9 11). Occasionally, pleural SSs have been reported to encase a lobe (2) or even an entire hemithorax (10), but they typically form localized, pleural-based masses with or without pedicles. In rare cases of SS, multifocal patterns have also been reported (6). Synovial sarcomas tend to be gray-white and fleshy, and frequently have associated hemorrhage, necrosis, and calcification. Pseudocapsulation was reported in several tumors. These tumors may have associated pleural thickening, and one tumor was associated with pleural plaques (10). Malignant mesotheliomas, in contrast, typically present as multiple nodules covering the pleura or as a diffuse sheet-like pleural thickening that can encase and compress the lungs (1). The tumor may extend superficially into the lungs, or along needle biopsy tracts. Localized, solitary discrete masses, in contrast to SS, are extremely rare. The appearance of MM is also typically gray-white, and can vary from firm and rubbery to soft and gelatinous. There may be foci of hemorrhage and necrosis, and this tumor is typically associated with pleural plaques due to its strong association with asbestos exposure (1). Histopathology Malignant mesotheliomas of the pleura typically have an epithelioid, biphasic, or sarcomatoid pattern. Synovial sarcomas, like MMs, also exhibit biphasic or sarcomatoid morphology. Theoretically, a monophasic epithelial SS should exist, but this variant could be reliably diagnosed only by using cytogenetic data (1). Since no monophasic epithelial SS of the pleura have been reported, only the biphasic and sarcomatoid variants of these tumors are considered in this discussion. Histologically, biphasic SS and biphasic MM exhibit subtle differences (4,12). Biphasic SS (Fig. 36.1) have a long interweaving spindled component that is compact and cellular, with little stromal collagen. Foci of hemiangiopericytomatous architecture (Figs. 36.1A and 36.2) and of microcalcification (Fig. 36.1D) are characteristic, and hyaline fibrosis can be present. Mast cells are often prominent, but glycogen is sparse. In contrast, the spindled component of biphasic MM consists of shorter, looser fascicles of blunt spindle cells with more stromal collagen. Hyaline fibrosis and hemangiopericytomatous architecture are A. Powers and M. Carbone 545

4 546 Chapter 36 Synovial Sarcoma of the Pleura Figure Histology of synovial sarcoma (SS). A: Hemgiopericytomatous appearance (100 ). B: Sarcomatoid SS. C: Biphasic SS, focus of epithelioid differentiation. D: Sarcomatoid SS, focus of microcalcification. Figure Histology of SS. Hemangiopericytomatous appearance at high magnification (400 ).

5 A. Powers and M. Carbone 547 Figure Desmoplastic mesothelioma. Compare with histology of sarcomatoid SS shown in Figure rare. Mast cells are also fewer in number, but glycogen is abundant (4,12). The epithelial component of biphasic SS typically consists of epithelial cells forming cleft-like glandular spaces and tubulopapillary structures. The epithelial component of well-differentiated biphasic mesotheliomas can also be tubulopapillary, but there is typically a gradual transition between the sarcomatous and epithelial elements in these tumors, while there is a sharp abutment of these areas in SS (1). Sarcomatoid MMs, similar to the spindle component in biphasic variants, usually consist of short blunt fascicles of pleomorphic tumor cells (Fig. 36.3). The fascicles may be poorly formed, and cells can have abundant eosinophilic cytoplasm. Sarcomatoid MM rarely displays a fibrosarcomatous or hemangipericytomatous pattern. This is distinct from monophasic SSs, which are composed of longer interweaving fascicles of densely packed, mildly pleomorphic, and overlapping spindle cells with a high mitotic rate. Moreover, abundant dense collagen deposition among sparse sarcomatoid and/or gland-like epithelioid structures, characteristic of desmoplastic mesothelioma (Fig. 36.3), is not seen in SS. Monophasic SSs may exhibit a fibrosarcomatous or hemangiopericytomatous pattern, and the presence of either of these two patterns in a pleural-based lesion should immediately raise suspicion for SS (1,12). Mucin Mucin staining is typically not performed in the differentiation between pleural SS and MM, but some authors have observed useful differences in staining. In contrast to MM, pleural SSs contain secretions

6 548 Chapter 36 Synovial Sarcoma of the Pleura that are mucicarmine positive and hyaluronidase resistant, and periodic acid-schiff (PAS) positive and diastase resistant. Rare MM may exhibit mucicarmine or PAS staining, but it is eliminated with hyaluronidase or diastase digestion (4,12). Immunohistochemistry Immunohistochemistry (IHC) plays a limited role in the distinction of SS from MM, since there are presently no immune markers that are unique for either entity. We recommend that a panel of markers be used to support a diagnosis of either of these tumors, which should include cytokeratins, calretinin, WT-1, Bcl-2, CD56, and CD99. Both SS and MM display immunoreactivity for vimentin and pancytokeratin. The former, although nonspecific is useful to verify the immunoreactivity of the tissue (i.e., almost everything stains for vimentin, Fig. 36.4A). It is our experience and that of others that nearly 100% of MMs are diffusely positive for cytokeratin (10,13); >90% of SSs (Fig. 36.4B) also display focal reactivity, which is most pronounced in the epithelioid component (1). While poorly differentiated SSs are less likely to exhibit cytokeratin positivity, as many as 50% have been Figure Immunoreactivity of SS. A: Vimentin, positive (200 ). B: Cytokeratin 5/6. Note positivity of superficial and entrapped reactive mesothelial cells. Tumor cells are mostly negative (100 ). C1: CD99, positive (400 ). C2: Bcl-2, focally positive on spindle tumor cells (200 ). D1: WT-1, negative (200 ). D2: WT-1, fibrous MM positive control (200 ).

7 shown to express focal keratin positivity (14). Thus, it appears that while the value of cytokeratin alone is limited in differentiating between these two tumors, focal positivity, rather than diffuse staining, is suggestive of SS. Like the cytokeratins, the use of calretinin to differentiate between these two tumors is limited. It is well established that both epithelioid and sarcomatoid MM express calretinin. Aubry et al (2) observed calretinin reactivity in 44 of 44 mesotheliomas (36 epithelial, five biphasic, and four sarcomatoid). In biphasic mesotheliomas, staining was seen in both the epithelial (3 4+) and spindle cells (2+). Like MM, SS can also express this marker. Miettinen et al (15) demonstrated calretinin positivity in 71% of biphasic SS, 52% of monophasic SS, and 56% of poorly differentiated SS. While both SS and MM express calretinin, it has been suggested that this marker may be of some value in differentiating between biphasic variants of these tumors. Cappello and Barnos (12) observed calretinin reactivity (2 3+) in the epithelial component of four of four biphasic MMs. The spindled component was negative in four of four MMs. In contrast, they observed staining (1 2+) in the spindled component in four of four biphasic SSs, while the epithelial component was weakly positive (1+) in only one of four. Thus, they concluded that strong diffuse calretinin staining in the epithelial component of a biphasic tumor with or without staining of the spindle cells is more indicative of an MM than an SS. In contrast to cytokeratin and calretinin, WT-1 appears to be a more useful marker in differentiating between SS and MM (Fig. 36.4D1,2). Miettinen et al (15) found that none of 18 biphasic SSs, none of 31 monophasic SSs, and none of 11 poorly differentiated SSs expressed WT-1. In contrast, 12 of 17 epithelioid MMs expressed WT-1. Similarly, Amin et al (16) found that 95% of MMs expressed WT-1, including sarcomatous variants. Thus, WT-1 reactivity supports a diagnosis of MM rather than SS. Like WT-1, Bcl-2, a protein involved in apoptosis, appears useful in discriminating between MM and SS of the pleura. Bcl-2 staining was found in the spindle component of 79% to 100% of SSs (Fig. 36.4C2) but only in 0 to 10% of MMs (12). In a direct comparision, Cappello and Barnes (12) observed Bcl-2 reactivity (3+) in the spindle component of four of four biphasic SSs, but only weak positivity (1 2+) in four of four biphasic MMs. The epithelial component of two of four SSs and four of four MMs was also positive (1 2+). Cappello and Barnes suggested that strong spindle cell Bcl-2 staining is more indicative of SS. The use of Ber-Ep4 is controversial. Reports of Ber-Ep4 staining in MM are variable. Gaffey et al (17) studied 49 MMs, including epithelioid and biphasic variants, and found that 10 (20%) exhibited focal (<25%) epithelioid staining. In contrast, Sheibani et al (18) found that of 115 MMs (including epithelioid, biphasic, and sarcomatoid variants), only one (0.9%) biphasic tumor stained with Ber-Ep4. Cappello and Barnes (12) found that four of four biphasic MMs were negative for Ber-Ep4, while two of four biphasic SSs displayed focal positivity in the epithelioid component. In the study by Gaetner et al (4), five of five A. Powers and M. Carbone 549

8 550 Chapter 36 Synovial Sarcoma of the Pleura pleural-based biphasic SSs exhibited epithelioid staining with Ber-Ep4, while four of five showed staining in the spindle cell component. HBME-1 is of limited value in the distinction between SS and MM, as HBME-1 positivity is seen in epithelioid components of MM as well as biphasic and monophasic SS (15). Staining for epithelial membrane antigen (EMA) may also be seen in both, and occasional S-100 positivity is also seen in SS and MM (4). CD99 (Fig. 36.4C1), the product of the MIC2 gene, has been observed at similar frequencies in both SS and MM (5). CD56 staining is frequent in SS (1). Both SS and MM typically demonstrate no reactivity with B72.3, LeuM1, or CD34. Overall, the use of immunohistochemistry in the distinction between MM and SS of the pleura is challenging and limited at best. Panels of markers are recommended since no single marker is diagnostic of either MM or SS. However, coexpression of Bcl-2, CD56, and CD99 with negative staining for calretinin, WT-1, and focal cytokeratin positivity strongly suggests the diagnosis of SS rather than MM. Electron Microscopy Ultrastructurally, MMs are characterized by several unique features that can be useful when trying to differentiate these tumors from SSs. Classically, biphasic and epithelioid MMs are characterized by long, slender, tortuous branching microvilli (Fig. 36.5A), but this finding may be diminished or lost in poorly differentiated neoplasms. Abundant intracytoplasmic glycogen is also seen. SSs, in contrast, have shorter blunt microvilli (Fig. 36.5B), and glycogen is sparse to absent (1,9,10). Molecular Studies Overall, while clinical history, gross and microscopic examination, and IHC may suggest a diagnosis of pleural SS, molecular diagnostic studies are considered the only definite way to differentiate SS from MM of the pleura. Regardless of histologic subtype, the chromosomal translocation t(x;18)(p11.2;q11.2) is characteristic of synovial sarcomas (10). A variety of techniques have been used to detect this translocation including conventional and molecular cytogenetics and reverse-transcription polymerase chain reaction (RT-PCR). While this translocation has been occasionally reported in other tumor types, particularly fibrosarcomas and malignant fibrous histiocytomas, these cases more likely represent misdiagnosed SS (1). The characteristic translocation results in fusion of the SYT gene on chromosome 18 to the SSX gene on chromosome X (Fig. 36.6). This translocation has been convincingly demonstrated in primary pleural SSs. Aubry et al (2), using RT-PCR, confirmed the presence of this translocation in five of five sarcomatoid primary SSs of the pleura. Carbone et al (10) and Ng et al (11) also confirmed the presence of this translocation in biphasic and monophasic pleural SSs, respectively. Overall, of 11 cases of primary pleural SS, nine (82%) contained the

9 A. Powers and M. Carbone 551 A Figure Electron microscopy characteristics of mesothelioma (A) characterized by long branching microvilli (12,000 ) and of SS (B) showing short blunt microvilli (8,000 ). B

10 552 Chapter 36 Synovial Sarcoma of the Pleura Figure X;18 translocation. A: The different possible molecular rearrangements described in this type of translocation. The translocation detected in this particular tumor involves the SYT gene on chromosome 18, and the SSX2 gene on chromosome X. B: Southern blot hybridization showing the X:18 translocation detected in this tumor. Lane 1: Patient RNA extraction purified on Qiagen column. Lane 3: RNA extraction not purified; (10 ml). Lane 5: RNA extraction not purified (2 ml). Lane 7: SS-positive control (courtesy of Dr. Lasota). Lanes 9, 11, 13: Negative controls. Lane 14: Molecular weight. Lanes 15 and 19: SSpositive controls from our collection of SS. Lane 17: MM negative control. Lanes 2, 4, 6, 8, 10, 12, 16, and 18 are empty. RT-PCR. translocation, one (9%) did not, and one (9%)was indeterminant. While MM can harbor multiple cytogenetic abnormalities, including partial loss of chromosome 1 (1p11 p22), chromosome 3 (3p14 p25), and chromosome 9 (9p), there have been no reports of the X;18 translocation in MM (1,10). Thus, molecular diagnostics is currently an extremely valuable tool in the differential diagnosis of a pleural-based mass when there is suspicion of SS. The type of SYT-SSX fusion gene detected in SS appears to correlate with both tumor morphology and prognosis. Kawai et al (19) observed that biphasic morphology correlated with the SYT-SSX2 fusion transcript, and monophasic morphology correlated with the SYT-SSX1 fusion transcript. Furthermore, those patients with biphasic tumors expressing the SYT-SSX2 fusion transcript had a better survival rate than those with SYT-SSX1 monophasic SS. Nilsson et al (20) also found that SS containing the SYT-SSX1 fusion transcripts had poorer outcomes.

11 A. Powers and M. Carbone 553 Conclusion The true incidence of primary SS of the pleura is unknown. Although it is a rare tumor, it is likely underdiagnosed and frequently mistaken for MM, the most common malignant pleural lesion. Diagnosis of pleural SS can be extremely challenging. The apparent rarity of the tumor in this location makes it an easily overlooked diagnosis. In addition, this tumor can be reliably distinguished from a MM only by using cytogenetics, since these entities have overlapping clinical, gross, histologic, and immunohistochemical features. This diagnostic problem has been compounded by the fact that the molecular tools to diagnose the unique X;18 translocation have only recently become available. Furthermore, few laboratories have the resources in place to identify this translocation (4,10,12,15). While challenging, the distinction between MM and SS of the pleura is essential, since these entities have distinct treatments and prognosis. Synovial sarcomas can be responsive to chemotherapy, particularly to ifosfamide-based regimens, while sarcomatoid mesotheliomas are chemoresistant (1,21). As a result, synovial sarcomas are treated aggressively, while patients with sarcomatoid mesotheliomas are often given supportive therapy only. Furthermore, patients with MM have an average survival of less than 12 months, while patients with SS can have longer survival rates. In a series of primary biphasic SS of the pleura (4), patients survived an average of 35 months, with a range of 12 to more than 96 months. With chemotherapy, some authors have reported 5-year survivals as high as 57% in patients with SS (6). Finally, a diagnosis of MM often has important legal consequences, due to its strong association with asbestos exposure; SS has not been associated with asbestos, and when mistaken for a MM, it can result in unnecessary legal fees and settlements. References 1. Weiss SW, Goldblum JR, eds. Soft Tissue Tumors, 4th ed. St. Louis: Mosby, Aubry MC, Bridge JA, Wickert R, Tazelaar HD. Primary monophasic synovial sarcoma of the pleura. Am J Surg Pathol 2001;25: Jawahar DA, Vuletin JC, Gorecki P, Persechino F, Macera M, Magazeh P. Primary biphasic synovial sarcoma of the pleura. Respir Med 1997;91: Gaertner E, Zeren H, Fleming M, Colby T, Travis W. Biphasic synovial sarcomas arising in the pleural cavity. A clinicopathologic study of five cases. Am J Surg Pathol 1996;20: Nicholson AG, Goldstraw P, Fisher C. Synovial sarcoma of the pleura and its differentiation from other primary pleural tumors: a clinicopathological and immunohistochemical review of three cases. Histopathology 1998;33: Colwell AS, D Cunta J, Vargas S, et al. Synovial sarcoma of the pleura: a clinical and pathologic study of three cases. J Thorac Cardiovasc Surg 2002; 124:

12 554 Chapter 36 Synovial Sarcoma of the Pleura 7. Essary LR, Vargas SO, Fletcher CD. Primary pleuropulmonary synovial sarcoma: reappraisal of a recently described anatomic subset. Cancer 2002;94: Chan JA, McMenamin ME, Fletcher CDM. Synovial sarcoma in older patients: clinicopathological analysis of 32 cases with emphasis on unusual histological features. Histopathology 2003;43: Hirano H, Kizaki T, Sashikata T, et al. Synovial sarcoma arising from the pleura: a case report with ultrastructural and immunohistochemical studies. Med Electron Microsc 2002;35: Carbone M, Rizzo P, Powers A, et al. Molecular analyses, morphology and immunohistochemistry together differentiate pleural synovial sarcomas from mesotheliomas: clinical implications. Anticancer Res 2002;22: Ng SB, Ahmed Q, Tien SL, et al. Primary pleural synovial sarcoma. A case report and review of the literature. Arch Pathol Lab Med 2003;127: Cappello F, Barnes L. Synovial sarcoma and malignant mesothelioma of the pleura: review, differential diagnosis and possible role of apoptosis. Pathology 2001;33: Battifora H, McCaughey WTE. Atlas of Tumor Pathology. Tumors of the Serous Membrane. Washington, DC: Armed Forces Institute of Pathology, 1995: Folpe AL, Schmidt RA, Chapman D, Gown AM. Poorly differentiated synovial sarcoma: immunohistochemical distinction from primitive neuroectodermal tumors and high grade malignant peripheral nerve sheath tumors. Am J Surg Pathol 1998;22: Miettinen M, Limon J, Niezabitowski A, Lasota J. Calretinin and other mesothelioma markers in synovial sarcoma. Am J Surg Pathol 2001;25: Amin KM, Litzky LA, Smythe WR, et al. Wilms tumor 1 susceptibility (WT1) gene products are selectively expressed in malignant mesothelioma. Am J Pathol 1995;146: Gaffey MJ, Milles SE, Swanson PE, et al. Immunoreactivity for Ber-Ep4 in adenocarcinomas, adenomatoid tumors, and malignant mesotheliomas. Am J Surg Pathol 1992;18: Sheibani K, Shin SS, Kezirian J, et al. Ber-Ep4 antibody as a discriminant in the differential diagnosis of malignant mesothelioma versus adenocarcinoma. Am J Surg Pathol 1991;15: Kawai A, Woodruff J, Healey JH, et al. SYT-SSX gene fusion as a determinant of morphology and prognosis in synovial sarcoma. N Engl J Med 1998;228: Nilsson G, Skytting B, Xie Y, et al. The SYT-SSX1 variant of synovial sarcoma is associated with a high rate of tumor cell proliferation and poor clinical outcome. Cancer Res 1999;59: Pass HI, Robinson BW, Testa JR, Carbone M. Emerging translational therapies for mesothelioma. Chest 1999;116:455S 460S.

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