Ovarian metastasis from renal clear cell carcinoma: a case report with an intraoperative, immunohistochemical study, and a review of the literature

This case report refers to ovarian metastases from renal clear cell carcinoma (RCC) in a 46-year-old woman with a history of abdominal pain and urinary incontinence. A pelvic ultrasound revealed a heterogeneous, large, right-sided solid/multi-cystic ovarian mass, suggesting diagnosis of borderline or malignant epithelial ovarian tumor. At staging, abdominal CT incidentally revealed an enlarged left kidney with a lesion, consistent with renal carcinoma. At the time of surgery, a frozen section of ovarian neoplasm was performed to confirm diagnosis of primary epithelial borderline ovarian tumor or metastatic renal carcinoma. Macroscopically, the right ovary had been entirely replaced by a multiloculated cystic lesion with clear serous fluid, solid septa, and centrally, a solid gray area. Imprint cytology, performed during an intraoperative study of the lesion, showed cohesive clusters of neoplastic cells with clear abundant and vacuolated cytoplasm, pleomorphic, medium or large nuclei, and evident nucleoli. Histological examination revealed an epithelial neoplasm, characterized by large cells with clear optically empty cytoplasm that lined the alveolar and cystic spaces. A prominent vascular component with sinusoidal features was also present. These findings and the clinical data of the simultaneous renal lesion were consistent with an intraoperative diagnosis of ovarian metastatic renal carcinoma. Permanent sections revealed that the ovarian lesion showed the same pathological features as those observed in frozen sections. Immunohistochemical analysis of the ovarian tumor showing positivity for CD10 and renal clear cell marker (RCC Ma), while the presence of RCC in a nephrectomy specimen confirmed ovarian metastatic renal carcinoma. In conclusion, although ovarian metastasis of RCC is very rare, diagnosis can be made by careful histological examination, immunohistochemical study, plus clinical data.

Renal clear cell carcinoma; Ovarian metastasis; Intraoperative diagnosis; Immunohistochemical analysis.

[1] Schouten L.J., Rutten J., Huveneers H.A.M., Twijnstra A.: “Incidence of brain metastases in a cohort of patients with carcinoma of the breast, colon, kidney, and lung and melanoma”. Cancer, 2002, 94, 2698.

[2] Mundy G.R.: “Metastasis to bone: causes, consequences and therapeutic opportunities”. Nat. Rev. Cancer, 2002, 2, 584.

[3] Berman A.T., Thukral A.D., Hwang W.T., Solin L.J., Vapiwala N.: “Incidence and patterns of distant metastases for patients with earlystage breast cancer after breast conservation treatment”. Clin. Breast Cancer, 2013, 13, 88.

[4] Sakamoto Y., Ohyama S., Yamamoto J., Yamada K., Seki M., Ohta K., et al.: “Surgical resection of liver metastases of gastric cancer: ann analysis of a 17-year experience with 22 patients”. Surg., 2003, 133, 507.

[5] Cavallari A., Vivarelli M., Bellusci R., Montalti R., De Ruvo N., Cucchetti A., et al.: “Liver metastases from colorectal cancer: present surgical approach”. Hepatogastroenterology, 2003, 50, 2067.

[6] Tas F.: “Metastatic behavior in melanoma: timing, pattern, survival, and influencing factors”. J. Oncol., 2012, 2012, 647684. doi: 10.1155/2012/647684. Epub 2012 Jun 27.

[7] de Waal Y.R., Thomas C.M., Oei A.L., Sweep F.C., Massuger L.F.: “Secondary ovarian malignancies: frequency, origin, and characteristics”. Int. J. Gynecol. Cancer, 2009, 19, 1160.

[8] Petru E., Pickel H., Heydarfadai M., Lahousen M., Haas J., Schaider H., Tamussino K.: “Nongenital cancers metastatic to the ovary”. Gynecol. Oncol., 1992, 44, 83.

[9] Yada-Hashimoto N., Yamamoto T., Kamiura S., Seino H., Ohira H., Sawai K., et al.: “Metastatic ovarian tumors: a review of 64 cases”. Gynecol. Oncol., 2003, 89, 314.

[10] Stadiem M.L.: “An ovarian hypernephroma”. Am. J. Surg., 1937, 37, 312.

[11] Martzloff K.H., Manlove C.H.: “Vaginal and ovarian metastases from hypernephroma: report of cases and review of literature”. Surg. Gynecol. Obstet., 1949, 88, 145.

[12] Hobbs JE, Vorder Bruegge CF, Wegner CR, Wintemute RW. Bilateral ovarian metastasis from renal adenocarcinoma: report of a case and discussion of pathogenesis. Obstet Gynecol 1957; 9:198-205

[13] Johansson H. Clinical aspects of metastatic ovarian cancer of extragenital origin. Acta Obstet Gynecol Scand 1960; 39:681-97

[14] Stefani P, Selli C, Nicita G, Turini D. Angiographic aspects of renal clear cell carcinoma metastatic to the female genitalia. Cardiovasc Intervent Radiol 1981; 4:183-86

[15] Buller R., Braga C., Tanagho E.A., Miller T.: “Renal cell carcinoma metastatic to the ovary: a case report”. J. Reprod. Med., 1983, 28, 217.

[16] Young R.H., Hart W.R.: “Renal cell carcinoma metastatic to the ovary: a report of three cases emphasizing possible confusion with ovarian clear cell adenocarcinoma”. Int. J. Gynecol. Pathol., 1992, 11, 96.

[17] Spencer J., Eriksen B., Garnett J.E.: “Metastatic renal tumor presenting as an ovarian clear cell carcinoma”. Urology, 1993, 41, 582.

[18] Adachi Y., Sasagawa I., Nakada T.S., Saitoh M., Mitobe K., Ohta T., et al.: “Bilateral ovarian metastasis from left renal cell carcinoma”. Urol. Int., 1994, 52, 169.

[19] Fields S., Libson E., Lavie O., Beller U.: “Renal cell carcinoma metastatic to the ovary. Ultrasound and CT appearance”. Clin. Imaging, 1996, 20, 42.

[20] Vara A., Madrigal B., Veiga M., Diaz A., García J., Calvo J.: “Bilateral ovarian metastasis from renal cell carcinoma”. Acta Oncol., 1998, 37, 379.

[21] Hammock L., Ghorab Z., Gomez-Fernadez C.R.: “Metastatic renal cell carcinoma to the ovary: a case report and discussion of different diagnosis”. Arch. Pathol. Lab. Med., 2003, 127, e123.

[22] Insabato L., De Rosa G., Franco R., D'Onofrio V., Di Vizio D. Ovarian metastasis from renal cell carcinoma: a report of three cases. Int J. Surg. Pathol., 2003; 11: 309-12

[23] Valappil S., Toon P., Anandaram P.S.: “Ovarian metastasis from primary renal cell carcinoma: report of a case and review of the literature”. Gynecol. Oncol., 2004, 94, 846.

[24] Stolnicu S., Borda A., Radulescu D., Puscasiu L., Berger N., Nogales F.F.: “Metastasis from papillary renal cell tumor”. Pathol. Res. Practice, 2007, 203, 819.

[25] Anagnostou V., Tiniakos D., Chorti M., Kiagia M., Tourkantonis I., Alamara C., et al.: “Right sited renal cell carcinoma metastasizing to the contralateral ovary: case report and review of the literature”. Pathol. Oncol. Res., 2009, 15, 123.

[26] Toquero L., Aboumarzouk O.M., Abbasi Z.: “Renal cell carcinoma metastasis to the ovary: a case report”. Cases J., 2009, 2, 7472.

[27] Guney S., Guney N., Ozcan D., Sayilgan T., Ozakin E.: “Ovarian metastasis of a primary renal cell carcinoma: case report and review of literature”. Eur. J. Gynaecol. Oncol., 2010, 31, 339.

[28] Luyckx M., Donnez J., Delos M.,. Kerger J., Donnez O.: “Ovarian metastasis after nephrectomy for primary renal clear cell carcinoma: a diagnostic challenge”. Gynecol. Surg., 2011, 8, 93.

[29] Decoene J., Ameye F., Lerut E., Oyen R., Van Poppel H., Joniau S.: “Renal cell carcinoma with synchronous metastasis to the calcaneus and metachronous metastases to the ovary and gallbladder”. Case Rep. Med., 2011, 2011, 671645. doi: 10.1155/2011/671645. Epub 2011 Oct 19.

[30] Udoji E., Herts B.R.: “Renal cell carcinoma metastatic to the ovary”. J. Urol., 2012, 188, 603.

[31] Ibrahim A., Al-Jafari M.S.: “Metastatic renal cell carcinoma in an ovarian benign mixed mucinous cystadenoma and brenner tumour: a case report”. Case. Rep. Pathol., 2012, 2012, 523231. doi: 10.1155/2012/523231. Epub 2012 Nov 27.

[32] Bauerová L., Dundr P., Fischerová D., Pešl M., Zikán M., Burgetová A.: “Ovarian metastasis of clear cell renal cell carcinoma: A case report”. Can. Urol. Assoc J., 2014, 8, E188-92

[33] Masago T., Morizane S., Watanabe T., Nakamoto S., Sejima T., Takenaka A.: “A case of renal cell carcinoma metastatic to the ovary: a case report and review of the literature”. Int. Canc. Conf. J., 2015, 4, 94.

[34] Kostrzewa M., Zyła M., Władziński J., Stetkiewicz T., Stachowiak G., Wilczyński J.R.: “Metastases of renal clear cell carcinoma to ovary--case report and review of the literature”. Eur. J. Gynaecol. Oncol., 2015, 36, 219.

[35] Liang L., Huang H., Dadhania V., Zhang J., Zhang M., Liu J.: “Renal cell carcinoma metastatic to the ovary or fallopian tube: a clinicopathological study of 9 cases”. Hum. Pathol., 2016, 51, 96.

[36] Fowler C.: “The kidneys and ureters”. In: Russel R., Williams N., Bulstrode C. (eds). Short practice of surgery. 24thed. New York: Hodder Arnold, 2004, 1330.

[37] Sadler G., Anderson M., Moss M., Ilson P.G.: “Metastases from renal cell carcinoma presenting as gastrointestinal bleeding: two case reports and a review of the literature”. BMC Gastroenterol., 2007, 7, 4.

[38] Sheth S., Scatarige J.C., Horton K.M., Corl F.M., Fishman E.K.: “Current concepts in the diagnosis and management of renal cell carcinoma: role of multidetector CT and three-dimensional CT”. Radiographics, 2001, 21, Spec No:S237

[39] González J., Angulo J., Ciancio G.: “Surgical management of renal cell cancer with tumour thrombus through an exclusive transabdominal approach”. Arch. Esp. Urol., 2011, 64, 297.

[40] Li W., Wang H., Wang J., L V F., Zhu X., Wang Z.: “Ovarian metastases resection from extragenital primary sites: outcome and prognostic factor analysis of 147 patients”. BMC Cancer, 2012, 12, 278.

[41] Gavallos G., Tawfik O., Langenstroer P.: “Renal-ovarian axis: a case report and review”. Urol., 2003, 62, 749.

[42] Kennedy A.W., Biscotti C.V., Hart W.R., Webster K.D.: “Ovarian clear cell adenocarcinoma”. Gynecol. Oncol., 1989, 32, 342.

[43] Scully R.E., Young R.H., Clement P.B.: “Dysgerminoma” In: Atlas of tumor Pathology. Tumors of the Ovary, Maldeveloped Gonads, Fallopian Tube, and Broad Ligament”. Washington: Armed Forces Institute of Pathology, Third Series, 1996, 239.

[44] Haroon S., Idrees R., Fatima S., Memon A., Kayani N.: “Ovarian steroid cell tumor, not otherwise specified: a clinicopathological and immunohistochemical experience of 12 cases”. J. Obstet. Gynaecol. Res., 2015, 41, 424.

[45] Lifschitz-Mercer B., Walt H., Kushnir I., Jacob N., Diener P.A., Moll R., et al.: “Differentiation potential of ovarian dysgerminoma: an immunohistochemical study of 15 cases”. Hum. Pathol., 1995, 26, 62.

[46] Niehans G.A., Manivel J.C., Copland G.T., Scheithauer B.W., Wick M.R.: “Immunohistochemistry of germ cell and trophoblastic neoplasms”. Cancer, 1988, 62, 1113.

[47] Tsuura Y., Hiraki H., Watanabe K., Igarashi S., Shimamura K., Fukuda T., et al.: “Preferential localization of c-kit product in tissue mast cells, basal cells of skin, epithelial cells of breast, small cell lung carcinoma and seminoma/dysgerminoma in human: immunohistochemical study on formalin-fixed, paraffin-embedded tissues”. Virchows Arch., 1994, 424, 135.

[48] Szyfelbein W.M., Young R.H., Scully R.E.:” Struma ovarii simulating ovarian tumors of other types. A report of 30 cases”. Am. J. Surg. Pathol., 1995, 19, 21.