Case study. 1. Introduction. Keywords: Mixed epithelial and stromal tumor of kidney; Rhabdoid
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1 Human Pathology (2007) 38, Case study Malignant mixed epithelial and stromal tumor of the kidney with rhabdoid features: report of a case including immunohistochemical, molecular genetic studies and comparison to morphologically similar renal tumors William R. Sukov MD a, John C. Cheville MD a, Donna J. Lager MD a, Jock R. Lewin MB, BCh, MMed (path), FFPath b, Thomas J. Sebo MD, PhD a, Matthew Lewin MD a, * a Mayo Clinic, Pathology, Rochester, MN 55905, USA b Department of Pathology, University of Mississippi, Jackson, MS 32916, USA Received 15 December 2006; revised 13 February 2007; accepted 19 March 2007 Keywords: Mixed epithelial and stromal tumor of kidney; Rhabdoid Summary Mixed epithelial stromal tumor of the kidney (MEST)/adult cystic nephroma (CN) is a lesion characterized by epithelial lined tubular or cystic structures interspersed within a variably prominent, distinctive spindle-cell stroma. Although typically benign, cases with malignant features have been reported. Herein, we report a MEST/CN with malignant stromal features and rhabdoid differentiation arising in the left kidney of an 84-year-old woman. Histologically, the tumor displayed multiple tubules and variably sized cystic structures lined by benign epithelium with an intervening malignant-appearing spindle-cell stroma. The malignant stroma displayed condensation in the regions surrounding the epithelial component consistent with the ovarian-like stroma typically observed in MEST/CN. In addition, the stromal cells displayed extensive rhabdoid differentiation. Immunohistochemical analysis revealed strong expression of cytokeratin 7, CAM 5.2, AE1/AE3, wide-spectrum keratin, and epithelial membrane antigen by the epithelial component. The stromal component displayed strong immunohistochemical expression of WT-1, CD-99, CD-56, INI1, and estrogen receptor; focal actin positivity; and was negative for desmin, myogenin, and progesterone receptor. Analysis by reverse transcriptase polymerase chain reaction failed to identify the SYT-SSX1 or SYT-SSX2 fusion transcripts characteristic of synovial sarcoma. To our knowledge, this represents the first report in the literature of malignant MEST with rhabdoid features and suggests that this entity should be considered in the diagnosis of renal stromal malignancies with prominent rhabdoid features Elsevier Inc. All rights reserved. 1. Introduction Corresponding author. address: lewin.matthew@mayo.edu (M. Lewin). Mixed epithelial and stromal tumor of the kidney (MEST)/cystic nephroma (CN) is a recently described neoplasm that predominantly affects perimenopausal women [1-3]. The tumor is typically solid and cystic, /$ see front matter 2007 Elsevier Inc. All rights reserved. doi: /j.humpath
2 Malignant mixed epithelial and stromal tumor of the kidney with rhabdoid features 1433 composed of admixed spindle-cell stroma and epithelial elements [1-4]. The epithelial component may display a tubular, microcystic, macrocystic, or complex branching architecture with a typical hobnail epithelial lining [1-4]. The stromal component consists of a bland spindle-cell proliferation of variable cellularity with occasional areas of myoid change, fascicular growth, and fibrosis. Although characterized by a benign histology and clinical course, malignant features of MEST and CN have recently been identified in a few cases [1,3,5-8]. We describe the histologic, immunohistochemical, and molecular genetic features of a case of malignant MEST with extensive rhabdoid differentiation. 2. Report of a case An 84-year-old woman was incidentally discovered to have a partially cystic tumor within the left kidney during evaluation for cholecystitis. She demonstrated no clinical abnormalities associated with her kidney lesion, and extensive further clinical evaluation showed the patient to have no other tumors. She subsequently underwent left radical nephrectomy. Follow-up studies of the patient showed no indication of recurrence or presence of other malignancies 17 months after nephrectomy. 3. Pathologic findings The left nephrectomy specimen contained a tan, partially hemorrhagic, partially cystic cm mass. The lesion involved the renal medulla and extended into the renal calyceal system as well as into the renal cortex. The tumor contained multiple, grossly obvious, loculated cysts, with the largest cyst measuring 2.5 cm in diameter. Histologically, the tumor was composed of epithelial lined cystic and tubular structures with an intervening malignant spindle-cell stroma (Fig. 1). The density of the epithelial component was variable with areas characterized by back to back cysts separated by only a thin fibrous capsule Fig. 1 Hematoxylin and eosin stained sections of malignant mixed epithelial stromal tumor of the kidney showing characteristic cystically dilated spaces with associated stroma (A). The cysts are lined by a single-cell layer of cuboidal to columnar eosinophilic cells with variable hobnail appearance (B). The malignant stromal condensation forms periepithelial cuffs. The stromal cells show marked atypia and brisk mitotic activity (C). The neoplastic stromal cells demonstrate focal rhabdoid morphology (D).
3 1434 W. R. Sukov et al. as well as areas that were predominantly stroma. Cystic structures varied greatly in size; however, all showed a simple architecture without branching or papillation of the epithelial component. The appearance of the epithelial cells lining the cysts and tubules was flattened, cuboidal, or hobnail with eosinophilic cytoplasm. The epithelial cells demonstrated little or no atypia, only occasionally showed an increase in nuclear size or visible nucleoli. However, no mitotic activity was observed in the epithelial elements. The stroma was predominantly densely cellular with prominent ovarian-like stroma near the epithelial component forming subepithelial cuffs. In these cuffs, the spindle cells displayed a higher nuclear-to-cytoplasmic ratio with round to ovoid, vacuolated nuclei, prominent nucleoli, and extensive pleomorphism. The mitotic rate varied from 15 to 25 mitoses per 10 high-power fields (HPF). Away from epithelial structures, the cells assumed a more loose, haphazard arrangement and were characterized by vacuolated nuclei that tended to be ovoid to elongate with less conspicuous nucleoli. A high degree of pleomorphism was still evident but accompanied by a lower mitotic rate from 10 to 15 mitoses per HPF. Focal areas of myxoid change were evident as well as occasional vague, short fascicles. Extensive vascularization of the stroma was present, consisting of capillaries and small arterioles. Regional populations of cells displaying rhabdoid features were also present within both the ovarian-like stroma as well as the looser stroma away from epithelial structures. These cells were characterized by large intracytoplasmic eosinophilic inclusions. The rhabdoid cells displayed striking pleomorphism, prominent nucleoli, and a high mitotic rate (15-25 mitoses per 10 HPF). The stroma demonstrated extensive infiltration of the surrounding normal renal parenchyma, most prominent in regions displaying rhabdoid features. Along the infiltrative border, sclerotic glomeruli and atrophic renal tubules could be identified trapped within the tumor. A dense lymphocytic infiltrate within the normal renal parenchyma was often present at the margin of invasion Immunohistochemistry Immunohistochemistry (Fig. 2) was performed on formalin-fixed, paraffin-embedded tissue using antibodies directed against the following antigens: estrogen receptor Fig. 2 Immunohistochemical studies show the epithelial component to be strongly positive for CK7 (A). The malignant stroma shows strong positivity for estrogen receptor (B), WT-1 (C), and CD-99 (D).
4 Malignant mixed epithelial and stromal tumor of the kidney with rhabdoid features 1435 (Ventana, Tucson, AZ); progesterone receptor (Dako, Carpinteria, CA); CD56 (Monosan/Caltag, San Francisco, CA); WT-1 (Novocastra, Burlingame, CA); myogenin (Dako); muscle specific actin (Dako); melan-a (Novocastra); HMB-45 (Dako); desmin (Dako); wide spectrum keratin (Dako), AE1/AE3 (Zymed, South San Francisco, CA); CK7 (Dako); CK20 (Dako); CAM 5.2 (Becton/Dickinson, San Jose, CA); epithelial membrane antigen (EMA; Dako); INI1 (Becton/Dickenson). The epithelial component showed strong expression of cytokeratin 7, CAM 5.2, wide spectrum keratin, and EMA, whereas the stromal component failed to stain for these markers. The stromal component showed strong diffuse positivity for WT-1, CD 56, CD-99, and estrogen receptor and focal actin positivity. The epithelial and stromal components, including the areas with rhabdoid features, showed strong nuclear staining for INI1. No regions showed a decreased expression of INI1. The epithelial component was negative for expression of these markers. Both epithelial and stromal components were negative for cytokeratin 20, HMB-45, melan-a, desmin, myogenin, and progesterone receptor Molecular genetics Reverse transcriptase polymerase chain reaction (RT- PCR) assay to detect the chimeric fusion transcripts SYT- SSX1 and SYT-SSX2 performed on RNA extracted from formalin-fixed, paraffin-embedded tissue was negative Discussion In 1998, Michal and Syrucek [9] proposed the designation MEST as a distinct entity primary to the kidney. In their report, as well as in subsequent series, MEST displayed a characteristic biphasic solid and cystic morphology comprised of tubules or cystically dilated structures unevenly distributed within a spindle-cell stroma [1,3,9,10]. Although displaying a regional variability, all reported cases have described the cystic and tubular structures to be lined by a low cuboidal epithelium with areas of hobnail-type epithelial cells with eosinophilic cytoplasm. The spindle-cell stroma of MEST typically contains at least focal areas with an ovarianlike appearance [1,3,9-11]. The stroma in these regions typically displays immunohistochemical reactivity for estrogen receptor and/or progesterone receptor. Hormone receptor expression by the ovarian-like stroma, in combination with the female predominance, has suggested a hormonal contribution to the pathogenesis of these tumors. Most cases of MEST exhibit a benign histologic picture and clinical course [1,3,9,11]. However, rare cases of malignantappearing MEST and adult CN have been reported [5-8]. In the present case, malignant cells were present solely within the stromal component. Despite mild atypical features such as occasional prominent nucleoli, the epithelial component could not be considered malignant. This is in agreement with the previous reports of malignant MEST, which also describe a benign epithelial component associated with malignant stroma [6-8]. Interestingly, a recent study by Picken and Fresco [12] suggests that the epithelial component of MEST may represent entrapped nonneoplastic tubules, which may explain our observation [13]. Malignantappearing cells were present throughout the stroma; curiously however, the regions of stromal condensation associated with the epithelial components, the ovarian-like regions, showed a greater degree of atypical cytologic features and more brisk mitotic activity relative to the regions more distant to the epithelial components where the stroma assumed a looser arrangement. In addition, the rhabdoid cells also demonstrated a greater association with the areas of stromal condensation suggesting that these ovarian-like regions give rise to these rhabdoid cells. In clear cell renal cell carcinoma, the presence of rhabdoid features has been associated with a higher tumor grade, tumor stage, and increased frequency of accompanying sarcomatoid features. However, such an association with increased tumor grade and stage has not been identified in other renal tumors demonstrating rhabdoid features. In the present case, areas showing rhabdoid features did display a substantial increase in mitotic activity as well as increased tendency toward infiltration of the adjacent renal parenchyma. The morphology of malignant MEST warrants a strong consideration of primary renal synovial sarcoma in the differential diagnosis. Several features of malignant MEST are also defining morphologic features observed in primary renal synovial sarcoma, specifically gross or microscopic cysts and tubules lined by hobnail epithelium, immunohistochemical positivity for cytokeratin in the epithelial component, a variable but often dense spindle-cell stroma with occasional short fascicles, and a moderate degree of mitotic activity [13-17]. Of note, in a recent series, Jun et al [18] presented 3 cases of primary renal synovial sarcoma in which the stromal cells displayed prominent rhabdoid features. In all cases presented in that series, the STY- SSX2 transcript was identified by RT-PCR confirming the diagnosis of synovial sarcoma. Our case failed to exhibit the SYT-SSX1 or SYT-SSX2 fusion transcript by RT-PCR, arguing strongly against the diagnosis of primary renal synovial sarcoma [2,19-23]. In addition, although significant morphologic overlap does exist between malignant MEST and synovial sarcoma, other features argue against such a diagnosis and for a diagnosis of malignant MEST in the present case. The prominent subepithelial condensation of the stroma, or ovarian-like stroma, is a distinctive feature of adult CN and MEST and is not observed in renal synovial sarcoma. In addition, strong immunohistochemical positivity for expression of estrogen receptor is distinctive feature of MEST and CN and not synovial sarcoma. The presence of rhabdoid features also suggests the possibility of adult rhabdoid tumor. Rhabdoid tumors characteristically demonstrate EMA positivity, which was also demonstrated in the present case. Morphologic and immunohistochemical features of the present tumor,
5 1436 W. R. Sukov et al. however, argue against the diagnosis. Morphologically, subepithelial condensation of ovarian-like stoma and tubular and cystic structures lined by hobnail epithelium are not characteristic of rhabdoid tumor [24]. In addition, adult rhabdoid tumor would not be expected to show strong estrogen receptor positivity by immunohistochemistry as was demonstrated in this case. Malignant rhabdoid tumors of the central nervous system, kidney, and soft tissue have been associated with inactivation of the INI1/hSNF5 gene at chromosome band 22q11.2 [25]. This inactivation is usually the result of deletion or mutation and ultimately leads to a decrease or loss in expression of the INI1 protein. A tumor suppressor and member of the SWI/ SNF chromatin-remodeling complex, the INI1 protein is normally expressed in all tissues [27]. Although in the present case we did not perform fluorescence in situ hybridization to identify chromosomal alterations involving the SMARCB1/INI1 gene, previous studies have demonstrated the use of immunohistochemical staining for INI1 protein as a means of identifying loss of INI1 protein expression in rhabdoid tumors of various locations including kidney [21,26]. Normal expression of the INI1 protein can be demonstrated by immunohistochemistry, which shows a strong nuclear staining pattern. Alterations of the SMARCB1/INI1 gene resulting in loss of INI1 protein expression result in a lack of INI1 nuclear staining [21,26]. In the present case, immunohistochemical staining of the tumor with antibodies directed against the INI1 protein showed a strong nuclear staining pattern indicating normal INI1 protein expression and arguing strongly against the diagnosis of adult rhabdoid tumor. Another consideration for the diagnosis in this particular case would be a primary renal sarcoma not otherwise specified. Sarcomas involving the kidney tend to entrap existing renal tubules sometimes causing them to dilate and form cystic structures. Therefore, one may argue that the findings in the current case are nonspecific. Although there were no areas of typical benign mixed epithelial tumor to prove that the lesion reported is a malignant transformation in a MEST, the peculiar hypercellular stroma cuffing epithelial lined cyst is remarkably reminiscent of the histology of MESTs. In addition, the stroma did focally resemble ovarianlike stroma and was estrogen receptor positive, recapitulating the findings one typically sees in benign MEST. Diagnosis of the present lesion by percutaneous renal biopsy may be particularly difficult because of sampling limitations. Given the rarity of the lesions, the consideration of malignant MEST would obviously follow the exclusion of the more common entities expected on renal biopsy. The presence of characteristic epithelial elements with associated stromal cuffing in the biopsy material would be an especially useful clue to suggest the diagnosis of malignant MEST. However, a sample lacking such elements may be difficult to distinguish from other renal stromal malignancies or a sarcomatoid renal cell carcinoma with rhabdoid differentiation. In such a situation, the morphologic character of the stroma may suggest a diagnosis of malignant MEST. Although showing high-grade cytologic features, the stroma should show evidence of the characteristic ovarian stromalike pattern, which would likely differ from the more disordered pattern expected with a sarcomatoid renal cell carcinoma. Immunohistochemistry would also be integral in the interpretation of the biopsy material. In summary, we present a unique case of malignant mixed epithelial stromal tumor of the kidney with rhabdoid features. We suggest that this entity should be considered in the diagnosis of renal stromal malignancies displaying rhabdoid features. References [1] Adsay NV, Eble JN, Srigley JR, et al. Mixed epithelial and stromal tumor of the kidney. Am J Surg Pathol 2000;24: [2] Eble JN. Mixed epithelial and stromal tumour. In: Eble JN, Sauter G, Epstain II, et al, editors. World Heath Organization classification of tumours: tumours of the urinary system and male genital organs. Lyons (France): IARC Press; p [3] Michal M, Hes O, Bisceglia M, et al. Mixed epithelial and stromal tumors of the kidney. A report of 22 cases. Virchows Arch 2004;445: [4] Bisceglia M, Galliani CA, Senger C, et al. Renal cystic diseases. Adv Anat Pathol 2006;13: [5] Clark J, Rocques PJ, Crew AJ, et al. Identification of novel genes, SYT and SSX, involved in the t(x;18)(p11.2;q11.2) translocation found in human synovial sarcoma. Nat Genet 1994;7: [6] Nakagawa T, Kanai Y, Fujimoto H, et al. Malignant mixed epithelial and stromal tumours of the kidney: a report of the first two cases with a fatal clinical outcome. Histopathology 2004;44: [7] Svec A, Hes O, Michal M, et al. Malignant mixed epithelial and stromal tumor of the kidney. Virchows Arch 2001;439: [8] Yap YS, Coleman M, Olver I. Aggressive mixed epithelial-stromal tumor of the kidney treated with chemotherapy and radiotherapy. Lancet Oncol 2004;12: [9] Michal M, Syrucek M. Benign mixed epithelial and stromal tumor of the kidney. Pathol Res Pract 1998;194: [10] Jevremovic D, Lager DJ, Lewin M. Cystic nephroma (multilocular cyst) and mixed epithelial and stromal tumor of the kidney: a spectrum of the same entity? Ann Diagn Pathol 2006;10: [11] Hiraga H, Nojima T, Abe S, et al. Diagnosis of synovial sarcoma with the reverse transcriptase-polymerase chain reaction: analyzes of 84 soft tissue and bone tumors. Diagn Mol Pathol 1998;7: [12] Picken MM, Fresco R. Mixed epithelial and stromal tumor of the kidney: preliminary immunohistochemical and electron microscopic studies of the epithelial component. Ultrastruct Pathol 2005;29: [13] Shannon BA, Murch A, Cohen RJ. Primary renal synovial sarcoma confirmed by cytogenetic analysis: a lesion distinct from sarcomatoid renal cell carcinoma. Arch Pathol Lab Med 2005;29: [14] Argani P, Faria PA, Epstein JI, et al. Primary renal synovial sarcoma: molecular and morphologic delineation of an entity previously included among embryonal sarcomas of the kidney. Am J Surg Pathol 2000;24: [15] Kim DH, Sohn JH, Lee MC, et al. Primary synovial sarcoma of the kidney. Am J Surg Pathol 2000;24: [16] Koyama S, Morimitsu Y, Morokuma F, et al. Primary synovial sarcoma of the kidney: report of a case confirmed by molecular detection of SYT-SSX2 fusion transcripts. Pathol Int 2001;51: [17] Tornkvist M, Wejde J, Ahlen J, et al. A novel case of synovial sarcoma of the kidney: impact of SS18/SSX analysis of renal hemangiopericytoma-like tumors. Diagn Mol Pathol 2004;13:47-51.
6 Malignant mixed epithelial and stromal tumor of the kidney with rhabdoid features 1437 [18] Jun SY, Choi J, Kang GH, et al. Synovial sarcoma of the kidney with rhabdoid features: report of three cases. Am J Surg Pathol 2004;28: [19] Argani P, Zakowski MF, Klimstra DS, Rosai J, Ladanyi M. Detection of the SYT-SSX chimeric RNA of synovial sarcoma in paraffinembedded tissue and its application in problematic cases. Mod Pathol 1998;11: [20] de Leeuw B, Balemans M, Olde Weghuis D, Geurts van Kessel A. Identification of two alternative fusion genes, SYT-SSX1 and SYT- SSX2, in t(x;18)(p11.2;q11.2)-positive synovial sarcomas. Hum Mol Genet 1995;4: [21] Hoot AC, Russo P, Judkins AR, et al. Immunohistochemical analysis of hsnf5/ini1 distinguishes renal and extra-renal malignant rhabdoid tumors from other pediatric soft tissue tumors. Am J Surg Pathol 2004;28: [22] Lasota J, Jasinski M, Debiec-Rychter M, Szadowska A, Limon J, Miettinen M. Detection of the SYT-SSX fusion transcripts in formaldehyde-fixed, paraffin-embedded tissue: a reverse transcription polymerase chain reaction amplification assay useful in the diagnosis of synovial sarcoma. Mod Pathol 1998;11: [23] Tsuji S, Hisaoka M, Morimitsu Y, et al. Detection of SYT-SSX fusion transcripts in synovial sarcoma by reverse transcription-polymerase chain reaction using archival paraffin-embedded tissues. Am J Pathol 1998;153: [24] Murphy WM, Grignon DJ, Perlman EJ. AFIP Atlas f tumor pathology: tumors of the kidney, bladder, and related urinary structures. Washington, DC: American Registry of Pathology; [25] Biegel JA, Allen CS, Kawasaki K, et al. Narrowing the critical region for a rhabdoid tumor locus in 22q11. Genes Chromosomes Cancer 1996;16: [26] Sigauke E, Rakheja D, Maddow DL, et al. Absence of expression of SMARCB1/INI1 in malignant rhabdoid tumors of the central nervous system, kidneys and soft tissue: an immunohistochemical study with implications for diagnosis. Mod Pathol 2006;19: [27] Versteege I, Medjkane S, Rouillard D, et al. Truncating mutations of hsnf5/ini1 in aggressive paediatric cancer. Nature 1998;394:203-6.
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