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Unusual Splenic Metastasis from Renal Cell Carcinoma. A Case Report and Review of the Literature
PATHOLOGY
Teaching Case
RESEARCH AND PRACTICE © Urban & Fischer Verlag http://www.urbanfischer.de/journals/prp
Unusual Splenic Metastasis from Renal Cell Carcinoma. A Case Report and Review of the Literature Valentina Kugel1, Yoram Dekel1, Miriam Konichezky2, Jacob Baniel1, Pinchas M. Livne1, Rumelia Koren2 1 Department of Urology, Department of Pathology, Rabin Medical Center, Petah Tikva, and Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
2
Summary This is a short report on a splenic metastasis from renal cell carcinoma. Previously, the patient had renal carcinoma removed by nephrectomy. The diagnosis of metastasis was based on morphology and immunohistochemistry. It is certainly true that splenic metastases from renal cell carcinoma are rare. Nevertheless, they have been well described in the literature. A giant cell reaction to tumor is noted in a number of cancers and mainly represents an unusual phenotype. Key words: Renal cell carcinoma – Spleen – Metastases
Introduction Metastatic involvement of the spleen is rare compared with other parenchymatous organs. In autopsy series of cancer patients, splenic metastases are found in 7%, mostly as part of disseminated disease [3, 7, 10, 14]. Metastases in spleen originating from kidney cancer are extremely rare, although they have been described in the literature. If present, they generally occur in disseminated disease. Since 1966, only five cases of splenic metastasis from RCC have been reported [18, 22, 23]. In this report, we describe another case of solitary splenic metastasis from RCC established by histochemical and immunohistochemical staining, and review the literature. Pathol. Res. Pract. 199: 739–743 (2003)
Case History Clinical features and operative findings
A 72-year-old Caucasian man was admitted to our hospital for fever, night sweats, anemia, and weight loss (approximately 5 kg) during 3 months before hospitalization. Two years earlier, he underwent left radical nephrectomy for a renal mass. Preoperative computerized tomography (CT) revealed a left renal tumor measuring 6 cm in diameter and located in the lower half and lateral aspect of kidney; no invasion of adjacent organs was noted. The final histological diagnosis was renal cell carcinoma of the clear cell type (Fig. 1), nuclear grade 3 [5], and stage T2 [21]. The patient was routinely followed up with biannual physical examination, blood tests, sonar or CT scans, and chest x-rays, reported to be normal. Physical examination disclosed no abnormality. Laboratory studies revealed anemia (hematocrit = 25.8) and a raised erythrocyte sedimentation rate (98 mm/h). An ultrasound examination and computed tomography of the abdomen showed a mass in the spleen, 8 cm in diameter (Fig. 2). A thorough metastatic work-up was negative for additional involvement. Fine needle aspiration of the lesion revealed round cells with abundant clear cytoplasm and prominent nuclei, suspected to be of renal cancer origin. Splenectomy was performed.
Address for correspondence: Rumelia Koren, Department of Pathology, Hasharon Hospital, Petah Tikva, Israel. Fax: ++972-3-937 2349. E-mail: [email protected] 0344-0338/03/199/11-739 $15.00/0
740 · V. Kugel et al. Pathologic findings
Fig. 1. Primary renal cell carcinoma, clear type, H&E × 200.
Macroscopically, the spleen was 12 × 8 × 8 cm, with a smooth capsule, and its weight was 430 gram. The cut surface showed a solitary nodule, measuring 8 × 6 × 4.5 cm. There were large areas of ischemic, opaque, graywhite necrosis, foci of hemorrhagic discoloration, and areas of softening. The surgical specimen was fixed in 10% formalin. Samples were embedded in paraffin, and sections were stained with hematoxylin and eosin. The immunohistochemical staining included low-molecular weight cytokeratin, cytokeratins (CK 8/18, 7), vimentin, leukocyte common antigen, B-cell and T- cell markers, as well as CD 68, performed on selected sections.
Fig. 2. Computed tomography scan showing a tumoral mass confined to the spleen.
Fig. 3. Metastatic renal cell carcinoma in the spleen. Neoplastic tissue replaces portion of the splenic parenchyma, H&E × 200.
Fig. 4. Few multinucleated giant cells around the tumor, H&E × 400.
Splenic Metastases from Renal Cell Carcinoma · 741 Light microscopy
The red and white pulp of the spleen was partially replaced by clear cells of round or polygonal shape with abundant clear cytoplasm. The nuclei were irregular, with large and prominent nucleoli, corresponding to grade 3 RCC (Fig. 3). Few multinucleated giant cells were noted around the tumor (Fig. 4). Immunohistochemically, the neoplastic cells were positive for low molecular weight cytokeratin, cytokeratin 8/18 and vimentin, and negative for cytokeratin 7, leukocyte common antigen, B-cells, T-cells, and CD 68. The multinucleated giant cells were positive for vimentin and CD 68 (Table 2). The diagnosis of splenic metastasis of renal cell carcinoma with giant cells was established on the basis of morphological and immunohistochemical features. Clinical follow-up
The patient refused adjuvant therapy and was well for 8 months until symptoms of weight loss and tiredness returned, and a raised erythrocyte sedimentation rate was noted. CT scan demonstrated hepatic metastasis. The patient underwent a 7-month immunotherapy, including interferon, cis retinoic acid, and prednisone with partial response.
As the disease progressed, therapy was aborted, and the patient died one year after splenectomy.
Discussion Metastases to the spleen originating from various neoplasms, for example of the breast and lung, as well as malignant melanoma, are usually discovered at autopsy [21]. The pattern of metastatic deposit in the spleen ranges from macroscopic (solitary nodule, multiple nodules, milliary or diffuse replacement) to microscopic [29]. In the latter, the tumor cells may be confined to the venous sinuses, red pulp, white pulp, or trabecular vessels, or are found in several of these components [27]. The spleen is considered to be resistant to cancerous implantation, because splenic metastases are very rare. This phenomenon has not been thoroughly investigated, and several theories have been proposed [8]. Explanations for this phenomenon are the presence of an antitumoral humoral factor, the constant flow of blood through the spleen avoiding implantation of cancer cells [10], and the sharp angle of splenic artery branching from the celiac artery; the scarcity of afferent lymphatic vessels limits tumor metastasis and the physiological actions of the spleen, including the rhythmic contraction, phagocytosis, and immunological antineoplastic action [21].
Table 1. Cases of splenic metastasis originating from renal cell carcinoma Author
Year
Age/Sex
Primary (kidney)
Diagnostic procedure
*Size/(cm)
Stage
Prognosis
Strum5 Murao7 Pal6 Suzuki7 Tatsuta7 Kugel
1984 1987 1995 1996 2001 2001
55/M 72/M 54/F 43 69 72/M
Right Left Left Left Left Left
CT CT CT CT CT CT
– 5 cm Small nodule 5 cm 6 cm 7 cm
unknown I unknown I II II
6 months/DOD 1 year, alive Unknown 9 years, alive 5 years 7 months, alive 1 year, DOD
*Size of spleen metastasis; DOD = died of disease
Table 2. Immunoreactivity of spleen with metastasis of RCC Marker
CK LMW CK 8/18 CK 7 Vimentin LCA B-cells T-cells (CD3) CD 68
Surse/Dilution
Zymed, USA 1:150 Zymed, USA 1:1 Dako, Denmark 1:300 Novocastra, UK 1:100 BioGenex, USA, 1:100 Zymed, USA 1:4 Zymed, USA 1:6 Zymed, USA R.U.
Spleen tissue
Negative Negative Negative Negative Positive Positive Positive Negative
Metastases Clear cells
Giant cells
Positive Positive Negative Positive Negative Negative Negative Negative
Negative Negative Negative Positive Negative Negative Negative Positive
742 · V. Kugel et al.
Splenic involvement as a single metastatic site has been reported in cancers originating from melanoma [3, 13], squamous cell carcinoma of the esophagus [16, 26], gastric carcinoma [28, 30], colon carcinoma [24], rectal carcinoma [4], lung cancer [23], endometrial carcinoma [6], uterine cervical adenocarcinoma [25], ovarian cancer [12, 17], breast [1, 2], carcinoid [9], and pseudomyxoma peritonei [20]. Rarely, the metastatic tumor is confined to the trabecular lymphatics of the spleen, a phenomenon often interpreted as a retrograde permeation of splenic lymphatics, usually originating from tumor deposits in the hilum [27]. The natural history of renal cell carcinoma is unpredictable and even bizarre at times, including late metastasis and metastasis to unusual sites [19]. In a review of the literature, only 5 cases showing solitary splenic metastases from RCC have been documented (see Table 1) [18, 22]. Splenic metastases from solid tumors are unusual, with only occasional case reports on patients treated with splenectomy before 1987 [13]. Because of the risk of spontaneous rupture of the spleen, splenectomy is the treatment of choice [11]. The prognosis reported is variable. Three patients survived for 1–9 years, two patients died within one year, and, in one case, the disease status was not mentioned. Most of the solitary metastases to the spleen originated from RCC of the left kidney, probably because of the topographic relation to the spleen. The interesting feature in our case is the presence of giant cells reacting to the tumor. The cells were confirmed to be of histiocytic and not of tumoral origin by negative staining for low molecular weight cytokeratins, cytokeratin 8/18, cytokeratin 7, and leukocyte common antigen, B-cells, and T-cells. Positivity for vimentin and CD 68 was demonstrated by immunohistochemical staining. Most probably, this giant cell represents a host stromal reaction to the neoplasm. Interestingly, this giant cell reaction has not been noted in the primary tumor. The presence of giant cell reaction in RCC has been described previously, indicating a significantly lower survival rate [15]. To our knowledge, this type of metastasis with giant cell reaction represents an unusual phenotype that has not been described previously.
References 1. Baranyay F, Bethlen K (2002) Diffuse splenic metastasis of occult breast cancer with incompatible blood group antigenic determinants. Orv Hetil 143: 139–143 2. Barreca M, Angelini D, Gallo A, Puntillo F, Amodio PM, Fernandes E (2001) Single asymptomatic splenic metastasis of breast carcinoma: report of a clinical case. G Chir 22: 227–228 3. Berge T (1974) Splenic metastases. Frequencies and patterns. Acta Pathol Microbiol Scand (A) 8: 499–506
4. Capizzi PJ, Allen KB, Amerson JR, Skandalakis JE (1992) Isolated splenic metastasis from rectal carcinoma. South Med J 85: 1003–1005 5. Fuhrman SA, Lasky LC, Limas C (1992) Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 6: 655–660 6. Giuliani A, Caporale A, Di Bari M, Demoro M, Mingazzini P (1999) Isolated splenic metastasis from endometrial carcinoma. J Exp Clin Cancer Res 18: 93–96 7. Goerg C, Schwerk WB (1994) Color doppler imaging of focal splenic masses. Eur J Radiol 18: 214–219 8. Hamy A, Letessier E, Gaschignard N, Guillard Y, Paineau J, Visset J (1993) Splenic metastases. A propos of 4 cases. J Chir Paris 130: 467–469 9. Hsiao CW, Yu JC, Yu CY, Gao HW, Hsu HM, Kuo YL, Hsieh CB, Liu YC (2001) Carcinoid tumor of the spleen: report of a case. Surg Today 31:1107–1109 10. Klein B, Stein M, Kuten A, Steiner M, Barshalom D, Robinson E, Gal D (1987) Splenomegaly and solitary spleen metastasis in solid tumors. Cancer 60: 100–102 11. Kyzer S, Koren R, Klein B, Chaimoff C (1998) Giant splenomegaly caused by splenic metastases of melanoma. Eur J Surg Oncol 24: 336–337 12. Lauro S, Trasatti L, Capalbo C, Conti A, Ricci F, Mingazzini PL, Vecchione A (2002) Solitary splenic recurrence of epithelial ovarian cancer: a case report and review. Anticancer Res 22: 3643–3645 13. Lee SS, Morgenstern L, Phillips EH, Hiatt JR, Margulies DR (2000) Splenectomy for splenic metastases: a changing clinical spectrum. Am Surg 66: 837–840 14. Morgenstern L, Rosenberg J, Geller SA (1985) Tumors of the spleen.World J Surg 9: 468–476 15. Moreno Cerro AM, Martinez Tello FJ, Leiva Galvis O, Caballero Alcantara J, Carrero Lopez V, Usera Sarraga G (1992) Clinico-pathologic study of renal cell carcinoma. Actas Urol Esp 16: 705–714 16. Murthy SK, Prabhakaran PS, Rao SR, Kumar RV (1991) Unusual splenic metastasis from oesophageal cancer. Indian J Cancer 28: 81–83 17. Nelson BE, Rose PG, Reale FR (1993) Isolated parenchymal splenic metastasis in epithelial ovarian cancer. Gynecol Oncol 50: 124–127 18. Pal KK, Guha D, Banerjee D (1995) Early splenic metastasis in a case of renal adenocarcinoma. J Indian Med Assoc 93: 276–277 19. Paz A, Koren R, Gal R, Wolloch Y (1996) Late solitary pancreatic metastasis from renal cell carcinoma. Isr J Med Sci 32: 1319–1321 20. Shimoyama S, Kuramoto S, Kawahara M, Yamasaki K, Endo H, Murakami T, Kaminishi M (2001) A rare case of pseudomyxoma peritonei presenting an unusual inguinal hernia and splenic metastasis. J Gastroenterol Hepatol 6: 825–829 21. Sternberg S S. Diagnostic Surgical Pathology – 3rd ed, NY, Lippincott Williams &Wilkins, 1999: 790–799 22. Strum WB (1984) Remote recurrence of renal cell carcinoma. Urology 23: 68–70 23. Tatsuta M, Shiozaki K, Masutani S, Tatsuta M, Shiozaki K, Masutani S, Hashimoto K, Imamura H, Ikeda M, Miya A, Ishida H, Kawasaki T, Furukawa H, Satomi T, Hoshida
Splenic Metastases from Renal Cell Carcinoma · 743
24. 25. 26. 27.
Y (2001) Splenic and pulmonary metastases from renal cell carcinoma: report of a case. Surg Today 31: 463–465 Thomas SM, Fitzgerald JB, Pollock RE, Evans DB (1993) Isolated splenic metastases from colon carcinoma. Eur J Surg Oncol 19: 485–490 Valls C, Serra J (1992) Isolated splenic metastasis from uterine cervical adenocarcinoma. AJR Am J Roentgenol 158: 919–920 Vyas SJ, Chitale AR, Deshpande RK (2002) Late splenic metastasis after curative resection for oesophageal carcinoma. Eur J Cardiothorac Surg 22:1011–1013 Warnke RA, Weiss LM, Chan JKC, et al. (1995) Tumors of the lymph nodes and spleen. AFIP: 508–510
28. Williams L, Kumar A, Aggarwal S (1995) Calcified splenic metastasis from gastric carcinoma. Abdom Imaging 20: 312–314 29. Wolf BC, Neiman RS. Disorders of the spleen. In: Bennington TL (Ed.) Major problems in pathology. Philadelphia, WB Saunders, 1989:199–202 30. Yamanouchi K, Ikematsu Y, Waki S, Kida H, Nishiwaki Y, Gotoh K, Ozawa T, Uchimura M (2002) Solitary splenic metastasis from gastric cancer: report of a case. Surg Today 32: 1081–1084 Received: March 28, 2003 Accepted: September 3, 2003
Teaching Case
RESEARCH AND PRACTICE © Urban & Fischer Verlag http://www.urbanfischer.de/journals/prp
Unusual Splenic Metastasis from Renal Cell Carcinoma. A Case Report and Review of the Literature Valentina Kugel1, Yoram Dekel1, Miriam Konichezky2, Jacob Baniel1, Pinchas M. Livne1, Rumelia Koren2 1 Department of Urology, Department of Pathology, Rabin Medical Center, Petah Tikva, and Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
2
Summary This is a short report on a splenic metastasis from renal cell carcinoma. Previously, the patient had renal carcinoma removed by nephrectomy. The diagnosis of metastasis was based on morphology and immunohistochemistry. It is certainly true that splenic metastases from renal cell carcinoma are rare. Nevertheless, they have been well described in the literature. A giant cell reaction to tumor is noted in a number of cancers and mainly represents an unusual phenotype. Key words: Renal cell carcinoma – Spleen – Metastases
Introduction Metastatic involvement of the spleen is rare compared with other parenchymatous organs. In autopsy series of cancer patients, splenic metastases are found in 7%, mostly as part of disseminated disease [3, 7, 10, 14]. Metastases in spleen originating from kidney cancer are extremely rare, although they have been described in the literature. If present, they generally occur in disseminated disease. Since 1966, only five cases of splenic metastasis from RCC have been reported [18, 22, 23]. In this report, we describe another case of solitary splenic metastasis from RCC established by histochemical and immunohistochemical staining, and review the literature. Pathol. Res. Pract. 199: 739–743 (2003)
Case History Clinical features and operative findings
A 72-year-old Caucasian man was admitted to our hospital for fever, night sweats, anemia, and weight loss (approximately 5 kg) during 3 months before hospitalization. Two years earlier, he underwent left radical nephrectomy for a renal mass. Preoperative computerized tomography (CT) revealed a left renal tumor measuring 6 cm in diameter and located in the lower half and lateral aspect of kidney; no invasion of adjacent organs was noted. The final histological diagnosis was renal cell carcinoma of the clear cell type (Fig. 1), nuclear grade 3 [5], and stage T2 [21]. The patient was routinely followed up with biannual physical examination, blood tests, sonar or CT scans, and chest x-rays, reported to be normal. Physical examination disclosed no abnormality. Laboratory studies revealed anemia (hematocrit = 25.8) and a raised erythrocyte sedimentation rate (98 mm/h). An ultrasound examination and computed tomography of the abdomen showed a mass in the spleen, 8 cm in diameter (Fig. 2). A thorough metastatic work-up was negative for additional involvement. Fine needle aspiration of the lesion revealed round cells with abundant clear cytoplasm and prominent nuclei, suspected to be of renal cancer origin. Splenectomy was performed.
Address for correspondence: Rumelia Koren, Department of Pathology, Hasharon Hospital, Petah Tikva, Israel. Fax: ++972-3-937 2349. E-mail: [email protected] 0344-0338/03/199/11-739 $15.00/0
740 · V. Kugel et al. Pathologic findings
Fig. 1. Primary renal cell carcinoma, clear type, H&E × 200.
Macroscopically, the spleen was 12 × 8 × 8 cm, with a smooth capsule, and its weight was 430 gram. The cut surface showed a solitary nodule, measuring 8 × 6 × 4.5 cm. There were large areas of ischemic, opaque, graywhite necrosis, foci of hemorrhagic discoloration, and areas of softening. The surgical specimen was fixed in 10% formalin. Samples were embedded in paraffin, and sections were stained with hematoxylin and eosin. The immunohistochemical staining included low-molecular weight cytokeratin, cytokeratins (CK 8/18, 7), vimentin, leukocyte common antigen, B-cell and T- cell markers, as well as CD 68, performed on selected sections.
Fig. 2. Computed tomography scan showing a tumoral mass confined to the spleen.
Fig. 3. Metastatic renal cell carcinoma in the spleen. Neoplastic tissue replaces portion of the splenic parenchyma, H&E × 200.
Fig. 4. Few multinucleated giant cells around the tumor, H&E × 400.
Splenic Metastases from Renal Cell Carcinoma · 741 Light microscopy
The red and white pulp of the spleen was partially replaced by clear cells of round or polygonal shape with abundant clear cytoplasm. The nuclei were irregular, with large and prominent nucleoli, corresponding to grade 3 RCC (Fig. 3). Few multinucleated giant cells were noted around the tumor (Fig. 4). Immunohistochemically, the neoplastic cells were positive for low molecular weight cytokeratin, cytokeratin 8/18 and vimentin, and negative for cytokeratin 7, leukocyte common antigen, B-cells, T-cells, and CD 68. The multinucleated giant cells were positive for vimentin and CD 68 (Table 2). The diagnosis of splenic metastasis of renal cell carcinoma with giant cells was established on the basis of morphological and immunohistochemical features. Clinical follow-up
The patient refused adjuvant therapy and was well for 8 months until symptoms of weight loss and tiredness returned, and a raised erythrocyte sedimentation rate was noted. CT scan demonstrated hepatic metastasis. The patient underwent a 7-month immunotherapy, including interferon, cis retinoic acid, and prednisone with partial response.
As the disease progressed, therapy was aborted, and the patient died one year after splenectomy.
Discussion Metastases to the spleen originating from various neoplasms, for example of the breast and lung, as well as malignant melanoma, are usually discovered at autopsy [21]. The pattern of metastatic deposit in the spleen ranges from macroscopic (solitary nodule, multiple nodules, milliary or diffuse replacement) to microscopic [29]. In the latter, the tumor cells may be confined to the venous sinuses, red pulp, white pulp, or trabecular vessels, or are found in several of these components [27]. The spleen is considered to be resistant to cancerous implantation, because splenic metastases are very rare. This phenomenon has not been thoroughly investigated, and several theories have been proposed [8]. Explanations for this phenomenon are the presence of an antitumoral humoral factor, the constant flow of blood through the spleen avoiding implantation of cancer cells [10], and the sharp angle of splenic artery branching from the celiac artery; the scarcity of afferent lymphatic vessels limits tumor metastasis and the physiological actions of the spleen, including the rhythmic contraction, phagocytosis, and immunological antineoplastic action [21].
Table 1. Cases of splenic metastasis originating from renal cell carcinoma Author
Year
Age/Sex
Primary (kidney)
Diagnostic procedure
*Size/(cm)
Stage
Prognosis
Strum5 Murao7 Pal6 Suzuki7 Tatsuta7 Kugel
1984 1987 1995 1996 2001 2001
55/M 72/M 54/F 43 69 72/M
Right Left Left Left Left Left
CT CT CT CT CT CT
– 5 cm Small nodule 5 cm 6 cm 7 cm
unknown I unknown I II II
6 months/DOD 1 year, alive Unknown 9 years, alive 5 years 7 months, alive 1 year, DOD
*Size of spleen metastasis; DOD = died of disease
Table 2. Immunoreactivity of spleen with metastasis of RCC Marker
CK LMW CK 8/18 CK 7 Vimentin LCA B-cells T-cells (CD3) CD 68
Surse/Dilution
Zymed, USA 1:150 Zymed, USA 1:1 Dako, Denmark 1:300 Novocastra, UK 1:100 BioGenex, USA, 1:100 Zymed, USA 1:4 Zymed, USA 1:6 Zymed, USA R.U.
Spleen tissue
Negative Negative Negative Negative Positive Positive Positive Negative
Metastases Clear cells
Giant cells
Positive Positive Negative Positive Negative Negative Negative Negative
Negative Negative Negative Positive Negative Negative Negative Positive
742 · V. Kugel et al.
Splenic involvement as a single metastatic site has been reported in cancers originating from melanoma [3, 13], squamous cell carcinoma of the esophagus [16, 26], gastric carcinoma [28, 30], colon carcinoma [24], rectal carcinoma [4], lung cancer [23], endometrial carcinoma [6], uterine cervical adenocarcinoma [25], ovarian cancer [12, 17], breast [1, 2], carcinoid [9], and pseudomyxoma peritonei [20]. Rarely, the metastatic tumor is confined to the trabecular lymphatics of the spleen, a phenomenon often interpreted as a retrograde permeation of splenic lymphatics, usually originating from tumor deposits in the hilum [27]. The natural history of renal cell carcinoma is unpredictable and even bizarre at times, including late metastasis and metastasis to unusual sites [19]. In a review of the literature, only 5 cases showing solitary splenic metastases from RCC have been documented (see Table 1) [18, 22]. Splenic metastases from solid tumors are unusual, with only occasional case reports on patients treated with splenectomy before 1987 [13]. Because of the risk of spontaneous rupture of the spleen, splenectomy is the treatment of choice [11]. The prognosis reported is variable. Three patients survived for 1–9 years, two patients died within one year, and, in one case, the disease status was not mentioned. Most of the solitary metastases to the spleen originated from RCC of the left kidney, probably because of the topographic relation to the spleen. The interesting feature in our case is the presence of giant cells reacting to the tumor. The cells were confirmed to be of histiocytic and not of tumoral origin by negative staining for low molecular weight cytokeratins, cytokeratin 8/18, cytokeratin 7, and leukocyte common antigen, B-cells, and T-cells. Positivity for vimentin and CD 68 was demonstrated by immunohistochemical staining. Most probably, this giant cell represents a host stromal reaction to the neoplasm. Interestingly, this giant cell reaction has not been noted in the primary tumor. The presence of giant cell reaction in RCC has been described previously, indicating a significantly lower survival rate [15]. To our knowledge, this type of metastasis with giant cell reaction represents an unusual phenotype that has not been described previously.
References 1. Baranyay F, Bethlen K (2002) Diffuse splenic metastasis of occult breast cancer with incompatible blood group antigenic determinants. Orv Hetil 143: 139–143 2. Barreca M, Angelini D, Gallo A, Puntillo F, Amodio PM, Fernandes E (2001) Single asymptomatic splenic metastasis of breast carcinoma: report of a clinical case. G Chir 22: 227–228 3. Berge T (1974) Splenic metastases. Frequencies and patterns. Acta Pathol Microbiol Scand (A) 8: 499–506
4. Capizzi PJ, Allen KB, Amerson JR, Skandalakis JE (1992) Isolated splenic metastasis from rectal carcinoma. South Med J 85: 1003–1005 5. Fuhrman SA, Lasky LC, Limas C (1992) Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 6: 655–660 6. Giuliani A, Caporale A, Di Bari M, Demoro M, Mingazzini P (1999) Isolated splenic metastasis from endometrial carcinoma. J Exp Clin Cancer Res 18: 93–96 7. Goerg C, Schwerk WB (1994) Color doppler imaging of focal splenic masses. Eur J Radiol 18: 214–219 8. Hamy A, Letessier E, Gaschignard N, Guillard Y, Paineau J, Visset J (1993) Splenic metastases. A propos of 4 cases. J Chir Paris 130: 467–469 9. Hsiao CW, Yu JC, Yu CY, Gao HW, Hsu HM, Kuo YL, Hsieh CB, Liu YC (2001) Carcinoid tumor of the spleen: report of a case. Surg Today 31:1107–1109 10. Klein B, Stein M, Kuten A, Steiner M, Barshalom D, Robinson E, Gal D (1987) Splenomegaly and solitary spleen metastasis in solid tumors. Cancer 60: 100–102 11. Kyzer S, Koren R, Klein B, Chaimoff C (1998) Giant splenomegaly caused by splenic metastases of melanoma. Eur J Surg Oncol 24: 336–337 12. Lauro S, Trasatti L, Capalbo C, Conti A, Ricci F, Mingazzini PL, Vecchione A (2002) Solitary splenic recurrence of epithelial ovarian cancer: a case report and review. Anticancer Res 22: 3643–3645 13. Lee SS, Morgenstern L, Phillips EH, Hiatt JR, Margulies DR (2000) Splenectomy for splenic metastases: a changing clinical spectrum. Am Surg 66: 837–840 14. Morgenstern L, Rosenberg J, Geller SA (1985) Tumors of the spleen.World J Surg 9: 468–476 15. Moreno Cerro AM, Martinez Tello FJ, Leiva Galvis O, Caballero Alcantara J, Carrero Lopez V, Usera Sarraga G (1992) Clinico-pathologic study of renal cell carcinoma. Actas Urol Esp 16: 705–714 16. Murthy SK, Prabhakaran PS, Rao SR, Kumar RV (1991) Unusual splenic metastasis from oesophageal cancer. Indian J Cancer 28: 81–83 17. Nelson BE, Rose PG, Reale FR (1993) Isolated parenchymal splenic metastasis in epithelial ovarian cancer. Gynecol Oncol 50: 124–127 18. Pal KK, Guha D, Banerjee D (1995) Early splenic metastasis in a case of renal adenocarcinoma. J Indian Med Assoc 93: 276–277 19. Paz A, Koren R, Gal R, Wolloch Y (1996) Late solitary pancreatic metastasis from renal cell carcinoma. Isr J Med Sci 32: 1319–1321 20. Shimoyama S, Kuramoto S, Kawahara M, Yamasaki K, Endo H, Murakami T, Kaminishi M (2001) A rare case of pseudomyxoma peritonei presenting an unusual inguinal hernia and splenic metastasis. J Gastroenterol Hepatol 6: 825–829 21. Sternberg S S. Diagnostic Surgical Pathology – 3rd ed, NY, Lippincott Williams &Wilkins, 1999: 790–799 22. Strum WB (1984) Remote recurrence of renal cell carcinoma. Urology 23: 68–70 23. Tatsuta M, Shiozaki K, Masutani S, Tatsuta M, Shiozaki K, Masutani S, Hashimoto K, Imamura H, Ikeda M, Miya A, Ishida H, Kawasaki T, Furukawa H, Satomi T, Hoshida
Splenic Metastases from Renal Cell Carcinoma · 743
24. 25. 26. 27.
Y (2001) Splenic and pulmonary metastases from renal cell carcinoma: report of a case. Surg Today 31: 463–465 Thomas SM, Fitzgerald JB, Pollock RE, Evans DB (1993) Isolated splenic metastases from colon carcinoma. Eur J Surg Oncol 19: 485–490 Valls C, Serra J (1992) Isolated splenic metastasis from uterine cervical adenocarcinoma. AJR Am J Roentgenol 158: 919–920 Vyas SJ, Chitale AR, Deshpande RK (2002) Late splenic metastasis after curative resection for oesophageal carcinoma. Eur J Cardiothorac Surg 22:1011–1013 Warnke RA, Weiss LM, Chan JKC, et al. (1995) Tumors of the lymph nodes and spleen. AFIP: 508–510
28. Williams L, Kumar A, Aggarwal S (1995) Calcified splenic metastasis from gastric carcinoma. Abdom Imaging 20: 312–314 29. Wolf BC, Neiman RS. Disorders of the spleen. In: Bennington TL (Ed.) Major problems in pathology. Philadelphia, WB Saunders, 1989:199–202 30. Yamanouchi K, Ikematsu Y, Waki S, Kida H, Nishiwaki Y, Gotoh K, Ozawa T, Uchimura M (2002) Solitary splenic metastasis from gastric cancer: report of a case. Surg Today 32: 1081–1084 Received: March 28, 2003 Accepted: September 3, 2003