Synovial sarcoma (SS) most commonly involves the soft
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1 Primary Pleural Synovial Sarcoma A Case Report and Review of the Literature Siok Bian Ng, B,BS; Qasim Ahmed, D; Sim Leng Tien, RCPA; Christina Sivaswaren, PhD; Lai Ching Lau Synovial sarcoma (SS) is an uncommon soft tissue tumor that occurs primarily in the extremities of young adults, especially in the periarticular region. In this report, we describe the rare occurrence of primary SS of the pleura in a 15-year-old boy. Histologically, the tumor demonstrated monophasic morphologic findings and showed positive staining with vimentin and Bcl-2 and focally for cytokeratin CK7. luorescent in situ hybridization identified t(x;18) translocation. The patient developed recurrences 20 months following resection of the tumor. The literature on this uncommon entity is reviewed, and its histogenesis, differential diagnoses, and cytologic features are also discussed. (Arch Pathol Lab ed. 2003;127:85 90) Synovial sarcoma (SS) most commonly involves the soft tissue of the extremities; however, it is also reported to occur in the head and neck, mediastinum, heart, esophagus, lungs, abdominal wall, mesentery, and retroperitoneum. 1 4 Synovial sarcoma of the pleura more often represents metastatic disease from a primary soft tissue tumor. 3 The recognition of this tumor in an unexpected site, such as the pleura, is often difficult, and the monophasic variant of SS is often mistaken for other spindle cell tumors, including malignant peripheral nerve sheath tumor (PNST), mesothelioma, fibrosarcoma, solitary fibrous tumor (ST), and smooth muscle tumor. 3 A search of the English-language literature revealed only 14 cases of primary pleural SS reported so far. 1 4 We report an additional case of primary SS of the pleura, confirmed by immunohistochemical analysis and ultrastructural and cytogenetic studies, with review of the literature and discussion of the differential diagnoses at this uncommon site. REPORT O A CASE A 15-year-old Indian boy presented with right-sided pleuritic chest pain, low-grade fever, and dyspnea of 1-week duration. Physical examination revealed decreased breath sounds and dullness to percussion over the right lower lung. ull blood cell count, serum urea levels, and electrolyte levels were within normal limits. Blood and sputum cultures revealed no bacterial growth. Chest x-ray examination showed a right-sided hydropneumotho- Accepted for publication April 3, rom the Histopathology (Drs Ng and Ahmed) and Cytogenetic (Drs Tien and Sivaswaren and s Lau) Sections, Department of Pathology, Singapore General Hospital, Singapore. Reprints: Siok Bian Ng, BBS, Department of Pathology, Singapore General Hospital, Outram Road, Singapore , Singapore ( siokbian@hotmail.com). rax and an area of ill-defined soft tissue density in the lower half of the right lung. Computed tomography confirmed a mass lesion in the right posterior mediastinum. A transthoracic needle biopsy was performed, and the biopsy specimen revealed a spindle cell tumor. An open thoracotomy with resection of the pleural-based tumor was performed, and the patient received postoperative chemotherapy and radiotherapy. Twenty months later, the patient developed recurrent tumors in the right lung, right chest wall, and retroperitoneum. The tumors were excised, and further courses of chemotherapy were administered. ATERIALS A ETHODS resh tissue from the tumor was harvested for cytogenetic study. or ultrastructural analysis, fresh tumor tissue was fixed in 2.5% glutaraldehyde, and 100-nm, ultrathin sections were stained with saturated aqueous uranyl acetate followed by Reynold lead citrate. Scrape imprint smears prepared from fresh tumor tissue were stained with Papanicolaou and Diff-Quik. or histologic analysis, representative sections were taken from the tumor, fixed in 10% formaldehyde, and processed to paraffin blocks. Sections 4 m thick of the paraffin blocks were stained with hematoxylin-eosin. Immunohistochemical stains for cytokeratins CK7 (Dako Corporation, Carpinteria, Calif, 1:40) and AE1/3 (Dako, 1:50), epithelial membrane antigen (EA; Dako, 1:50), vimentin (Dako, 1:200), S100 protein (Dako, 1:1400), smooth muscle actin (SA; Sigma Chemical Company, St Louis, o, 1: 800), desmin (Dako, 1:40), CD34 (Novocastra, Newcastle upon Tyne, United Kingdom, 1:30), synaptophysin (Dako, 1:25), chromogranin A (Dako, 1:70), Bcl-2 (Dako, 1:50), CD99 (Dako, 1:80), calretinin (Neoarker, remont, Calif, 1:100), and thrombomodulin (Dako, 1:70) were performed using the streptavidin-biotin complex method. Cytogenetic analysis was performed on slides made according to standard cytogenetic techniques from 24-hour cultures. Slides were banded by routine Giemsa trypsin banding methods. Karyotypes were analyzed and described according to the International System for Human Cytogenetic Nomenclature. A minimum of 20 metaphases were analyzed. luorescent in situ hybridization (ISH) using commercially-available whole chromosome paint for chromosomes X and 18 was performed following manufacturer instructions (Oncor, Gaithersburg, d). PATHOLOGIC IINGS The tumor was received in several fragments, altogether measuring cm. Cut sections showed a soft, friable, grayish appearance with solid and cystic areas. Scattered foci of hemorrhage and myxoid change were noted in a background of firm fibrous areas. ocally, lung parenchyma was identified attached to the larger tumor fragments. Cytologically, imprint smears of the fresh tumor revealed spindle cells, with relatively uniform oval nuclei showing fine chromatin and inconspicuous nucleoli and scanty cytoplasm with small unipolar and bipolar cy- Arch Pathol Lab ed Vol 127, January 2003 Primary Pleural Synovial Sarcoma Ng et al 85
2 igure 1. Imprint cytologic analysis showing branching blood vessel and uniform spindle cells with unipolar and bipolar cytoplasmic processes (Papanicolaou, original magnification 200). 86 Arch Pathol Lab ed Vol 127, January 2003 Primary Pleural Synovial Sarcoma Ng et al
3 igure 3. a, Strong, diffuse positive immunoreactivity with Bcl-2 (original magnification 200). b, ocal immunoreactivity with cytokeratin CK7 (original magnification 200). c, Negative immunoreactivity with calretinin (original magnification 200). d, Negative immunoreactivity with thrombomodulin (original magnification 200). toplasmic processes (igure 1). Branching blood vessels were also noted. Histologically, the pleural tumor was predominantly composed of spindle cells with varying degree of cellularity. Hypercellular areas showing sweeping fascicles of spindle cells and focal herringbone arrangement (igure 2, a) were seen merging with less cellular foci where abundant myxoid ground substance separated the tumor cells, resulting in the formation of irregular cleftlike and cystic spaces (igure 2, b), the latter often rimmed by a condensed layer of neoplastic cells. ocal nodular collections of pale, plump epithelioid cells merging with surrounding spindle cells were identified (igure 2, c), and rare foci of calcifications were noted (igure 2, d). No hemangiopericytomatous pattern, necrosis, glandular differentiation, or heterologous elements was observed. The tumor cells displayed mild atypia and mitotic count of up to 15 per 10 high-power fields. There was tumor infiltration into underlying lung parenchyma with entrapment of bronchioles (igure 2, e). Immunohistochemical analysis revealed positive staining of the tumor cells for vimentin and Bcl-2 (igure 3, a). Rare cells were positive for cytokeratin CK7 (igure 3, b), and focal stain- igure 2. a, Hypercellular areas demonstrating spindle cells arrayed in herringbone growth pattern (hematoxylin-eosin [H&E], original magnification 100). b, Abundant myxoid ground substance separating the tumor cells with formation of irregular cleftlike and cystic spaces (H&E, original magnification 100). c, Nodular collection of plump epithelioid cells (inset), merging with surrounding spindle cells (H&E, original magnifications 100 and 200 [inset]). d, Epithelioid tumor cells with foci of calcifications (H&E, original magnification 200). e, Tumor infiltration into underlying lung parenchyma with entrapment of bronchioles (inset) (H&E, original magnifications 25 and 400 [inset]; arrow indicates cilia). Arch Pathol Lab ed Vol 127, January 2003 Primary Pleural Synovial Sarcoma Ng et al 87
4 Clinicopathological eatures of Primary Synovial Sarcomas* Source, y Age, y Sex Symptoms Radiologic indings Gross indings icroscopy Jawahar et al, Dyspnea, cough, chest pain Pleural mass 17 cm, solid Nicholson et al, Case 1 42 Dyspnea 12 cm, cystic Case 2 28 Dyspnea, chest pain 12 cm, solid onophasic Case 3 42 Chest pain NA onophasic Gaertner et al, Case 1 Case Chest pain, dysphagia Chest pain Pleural mass 21 cm, solid cystic, pleural thickening 9 cm, solid cystic, pleural thicking Case 3 50 Chest pain Left upper lobe mass 16 cm, solid cystic Case 4 9 Chest pain, dyspnea, fever Pleural mass 5 cm, solid cystic Case 5 32 Spontaneous pneumothorax Right middle lobe mass 9 cm, solid Aubry et al, Case 1 Case 2 Case 3 Case 4 Case Chest pain, cough Pleural effusion Pleural effusion Chest pain, cough, dyspnea Incidental Present case 15 Chest pain, cough, fever Unknown cm, solid localized masses involving pleura predominantly; in 1 case, tumor extended into lung onophasic onophasic onophasic onophasic onophasic Hydropneumothorax, mass 20 cm, solid cystic onophasic * NA indicates not known;, not done; NED, no evidence of disease; DOD, dead of disease; and AWD, alive with disease. ing for CD99 was also noted. No immunoreactivity with cytokeratin AE1/3, EA, S100 protein, chromogranin A, synaptophysin, desmin, SA, CD34, calretinin (igure 3, c), and thrombomodulin (igure 3, d) were observed. Electron microscopy revealed oval-to-spindle cells with occasional single cytoplasmic processes in the intercellular spaces and focal discontinuous segments of external lamina. Poorly formed cell junctions were also noted infrequently. Cytogenetic analysis and ISH identified a t(x; 18)(p11.2;q11.2) translocation (igure 4, a and b). Other structural and numerical chromosomal abnormalities included unbalance of chromosomes 9 and 17, addition of chromosomes X, 2, 4, 9, 12, 17, and 18, and loss of chromosomes 3, 8, and 22. COENT In this case, the presence of a solitary pleural-based mass with relatively little lung involvement and the absence of an extrapleural primary tumor are compatible with primary SS originating from the pleura. Primary pleural SS is rare, and only 14 cases have been reported in the English-language literature so far (Table). 1 4 The patients ranged in age from 9 to 69 years and 57% were male. Chest pain was the most frequent complaint followed by dyspnea, cough, pleural effusion, and pneumothorax. Radiologically, a mass and/or pleural effusion was present in most cases. acroscopically, the tumors ranged from 4.5 to 21 cm in size and were mostly solid and localized pleural-based masses. Areas of necrosis, hemorrhage, calcification, and cystic change were commonly described. A total of 50% of the cases were biphasic tumors, which contained a variable component of epithelial cells forming cleftlike glandular spaces and tubulopapillary structures. The spindle cell component in both biphasic and monophasic tumors was composed of hypercellular, densely packed sheets and interweaving fascicles of spindle cells. Herringbone and hemangiopericytoma-like growth patterns were commonly seen. Other features included dense hyaline fibrosis, myxoid change, and epithelioid cells with features transitional between the epithelial and spindle morphologic findings. Pleural SS demonstrates similar immunohistochemical and ultrastructural features to SS at other sites. Except for a subset of monophasic tumors, most SS shows positive staining with cytokeratin, EA, vimentin, and CD Recent studies 3 have described positive bcl-2 staining in all cases of SS. It has also been increasingly recognized that monophasic SS can rarely show S100 protein expression. 6 In addition, immunoreactivity for CD56 7 and other nerve sheath associated markers, including type IV col- 88 Arch Pathol Lab ed Vol 127, January 2003 Primary Pleural Synovial Sarcoma Ng et al
5 Extended Genetics Treatment Outcome t(x;18) SYT/SSX2 SYT/SSX1 SYT/SSX1 SYT/SSX1 SYT/SSX2 t(x;18) Surgery, radiotherapy Surgery, chemotherapy Surgery, chemotherapy Chemotherapy Surgery Surgery, chemotherapy, radiotherapy Surgery, chemotherapy, radiotherapy Surgery, chemotherapy, radiotherapy Suregry, chemotherapy, phototherapy, chemoimmunotherapy Surgery performed in all cases; 1 case given radiotherapy and 1 case given chemotherapy Surgery, chemotherapy Local recurrence at 5 mo, alive 16 mo after diagnosis NED 12 mo NED 9 mo NED 5 mo DOD 12 mo DOD 18 mo DOD 12 mo AWD 8 y, regional metastatic disease DOD approximately 30 mo NED 13 mo NED 4 mo Unknown NED 6 mo NED 12 mo AWD 21 mo multiple recurrent tumors lagen, CD57, and p75ntr, has been reported. 6 In addition, SS is CD34, desmin, and SA negative. Ultrastructural evidence of epithelial differentiation can be demonstrated in both the epithelial and spindle cell components, which include intercellular spaces and junctions, microvilli, continuous or discontinuous basal lamina, and intermediate filament aggregates. 8 In this case, the presence of poorly formed cell junctions, focal basal lamina, and occasional single cytoplasmic processes are compatible with the diagnosis of SS. The t(x;18)(p11.2;q11.2) translocation is present in more than 90% of these neoplasms, regardless of the histologic subtype and site. 3,5,6,9 This translocation results in the fusion of the SYT gene on chromosome 18 to either the SSX1 or SSX2 genes on chromosome X, and the translocation can be detected by conventional cytogenetic analysis, ISH, or reverse transcription polymerase chain reaction assay. 3,5,9 The SYT-SSX chimeric proteins are thought to be involved in the transcriptional deregulation of specific but as yet unknown target genes. 5 Although highly specific for SS, this translocation has also been reported to occur in other types of tumor, including fibrosarcoma, malignant fibrous histiocytoma, and rare cases of PNST. 6 Although the t(x;18) translocation is often the sole abnormality, other additional chromosomal aberrations are sometimes present. 9 The histogenesis of SS remains an intriguing issue. The occurrence of this tumor in extra-articular locations and the presence of epithelial differentiation, which is not present in normal synovium, cast doubts on the postulation that SS originates from synovium or specialized arthrogenous mesenchyme. 4 Alternatively, it has been suggested that these neoplasms arise from pluripotential mesenchyme with the potential for epithelial and/or spindle cell differentiation or represent either true carcinomas or carcinosarcomas. 4,8 olpe et al 6 suggested the concept that SS may be a tumor displaying combined neuroepithelial and nerve sheath differentiation. The diagnosis of monophasic tumors occurring in unusual sites such as the pleura remains challenging, and the differential diagnoses include ST, PNST, fibrosarcoma, smooth muscle tumor, sarcomatoid carcinoma, sarcomatous malignant mesothelioma, pleuropulmonary blastoma, and thymoma. 2,3 Patients with STs usually remain asymptomatic, and unlike SS, virtually all STs are positive for CD34 and negative for cytokeratin and EA. Sarcomatoid mesotheliomas occur predominantly in older patients with a history of asbestos exposure, and most present with multiple pleural nodules or diffuse pleural thickening. 3 Unlike SS, they rarely display fibrosarcomatous growth pattern, and one of the most important characteristic features that distinguish mesotheliomas from other pleural sarcomas is the consistent diffuse immunoreactivity with pankeratin, which is not present in our case. Calretinin is a less reliable mesothelial marker than cytokeratin because it is not always positive in sarcomatoid mesotheliomas. In addition, 52% of monophasic SS contains foci of calretinin-positive cells. 10 The t(x;18) translocation has not been described in mesotheliomas. 3 onophasic SS can be distinguished from PNSTs and other spindle cell tumors by differences in histologic and immunohistochemical features. 3 Detection of t(x;18) translocation can be exceedingly useful in instances of overlapping histologic and immunohistochemical features or when the sample size is small. According to Akerman et al, 11 the diagnosis of SS may be suggested on fine needle aspiration biopsy specimens, but adjunctive methods are necessary for a definitive diagnosis. The most frequently encountered cytologic features include cellular aspirates, mixture of irregular celltight tumor tissue fragments and dispersed cells with stripped nuclei, branching vessels, small to medium cells with a mixture of round, ovoid, or spindle-shaped nuclei, bland nuclei with inconspicuous nucleoli, and scanty unipolar or bipolar cytoplasmic processes. The differential diagnoses on cytologic testing include hemangiopericytoma and fibrosarcoma. 11 Although generally regarded as a high-grade sarcoma, not all SSs share the same poor outcome. 12 In a multicentric study of 128 patients with localized primary SS, Trassard et al 12 noted that the UICC/AJCC stage, tumor size, histologic grade (which depends on necrosis and mitotic activity), vascular invasion, and pathologic resection margins were significant predictors of outcome. The 5-year disease-specific survival rate was 62.9%. rom the data available on pleural SS (Table), 5 (33%) of 15 cases died of the disease. However, the follow-up period was limited in some cases and ranged from 4 months to 8 years. In summary, primary SSs of the pleura are rare neoplasms that need to be distinguished from other biphasic and spindle cell tumors using immunohistochemical, ul- Arch Pathol Lab ed Vol 127, January 2003 Primary Pleural Synovial Sarcoma Ng et al 89
6 igure 4. a, luorescent in situ hybridization with whole chromosome paint for chromosomes X (green) and 18 (red). Two chromosomes with red and green paint represent the product of the reciprocal translocation t(x; 18). In addition, there is trisomy 18. b, Cytogenetic karyotype showing reciprocal translocation between chromosomes X and 18 (arrows) and chromosome 18 trisomy. trastructural, and cytogenetic studies. Its prognosis appears to be similar to that of localized primary SS at other sites in the body. References 1. Jawahar DA, Vuletin JC, Gorecki P, et al. Primary biphasic synovial sarcoma of the pleura. Respir ed. 1997;91: Nicholson AG, Goldstraw P, isher 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: Aubry -C, Bridge JA, Wickert R, et al. Primary monophasic synovial sarcoma of the pleura: five cases confirmed by the presence of SYT-SSX fusion transcript. Am J Surg Pathol. 2001;25: Gaertner E, Zeren H, leming V, et al. synovial sarcomas arising in the pleural cavity: a clinicopathologic study of five cases. Am J Surg Pathol. 1996;20: Antonescu CR, Kawai A, Leung DH, et al. Strong association of SYT-SSX fusion type and morphologic epithelial differentiation in synovial sarcoma. Diagn ol Pathol. 2000;9: olpe AL, Schmidt RA, Chapman D, et al. Poorly differentiated synovial sarcoma: immunohistochemical distinction from primitive neuroectodermal tumors and high-grade malignant peripheral nerve sheath tumors. Am J Surg Pathol. 1998;22: olpe AL, Gown A. Immunohistochemistry for analysis of soft tissue tumors. In: Weiss SW, Goldblum JR, eds. Enzinger and Weiss s Soft Tissue Tumors. 4th ed. St Louis, o: osby Inc; 2001: Lopes J, Bjerkehagen B, Sobrinho-Simoes, et al. The ultrastructural spectrum of synovial sarcomas: a study of the epithelial type differentiation of primary tumors, recurrences, and metastases. Ultrastruct Pathol. 1993;17: Kaplan A, Goodman D, Satish J, et al. Primary pulmonary sarcoma with morphologic features of monophasic synovial sarcoma and chromosome translocation t(x;18). Am J Clin Pathol. 1996;105: iettinen, Limon J, Niezabitowski A, et al. Calretinin and other mesothelioma markers in synovial sarcoma: analysis of antigenic similarities and differences with malignant mesothelioma. Am J Surg Pathol. 2001;25: Akerman, Willen H, Carlen B, et al. ine needle aspiration (NA) of synovial sarcoma: a comparative histological-cytological study of 15 cases, including immunohistochemical, electron microscopic and cytogenetic examination and DNA-ploidy analysis. Cytopathology. 1996;7: Trassard, Doussal VL, Hacene K, et al. Prognostic factors in localized primary synovial sarcomas: a multicentric study of 128 adult patients. J Clin Oncol. 2001;19: Arch Pathol Lab ed Vol 127, January 2003 Primary Pleural Synovial Sarcoma Ng et al
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