Clin J Gastroenterol (2013) 6:480–484 DOI 10.1007/s12328-013-0426-6
CASE REPORT
Postoperative isolated splenic metastasis from gallbladder cancer: report of a case Yusuke Taki • Teiichi Sugiura • Kazuya Matsunaga Hideyuki Kanemoto • Takashi Mizuno • Yukiyasu Okamura • Katsuhiko Uesaka
•
Received: 24 July 2013 / Accepted: 9 September 2013 / Published online: 25 September 2013 Ó Springer Japan 2013
Abstract We present a rare case of metachronous splenic metastasis from gallbladder cancer. A 65-year-old female with gallbladder cancer underwent a partial hepatectomy with en-bloc resection of the gallbladder and extrahepatic bile duct. Ten months later, she presented with isolated splenic metastasis and underwent splenectomy with distal pancreatectomy. The histological diagnosis confirmed metastatic adenocarcinoma from gallbladder cancer. She had no signs of recurrence 4 years after the second surgery. To the best of our knowledge, this is the first report of isolated splenic metastasis from gallbladder cancer. Keywords Gallbladder cancer Splenic metastasis Splenectomy
Introduction Splenic metastases are rare, and have been found in only 0.96 % of the reported metastatic cancer patients [1]. Because most splenic metastases are diagnosed as a part of multivisceral metastatic diseases, isolated splenic metastases are extremely rare [2]. We report a case of isolated splenic metastasis from gallbladder cancer, which was successfully treated by splenectomy with distal pancreatectomy.
Y. Taki T. Sugiura (&) K. Matsunaga H. Kanemoto T. Mizuno Y. Okamura K. Uesaka Division of Hepato-Biliary-Pancreatic Surgery, Shizuoka Cancer Center, 1007 Shimo-Nagakubo, Sunto-Nagaizumi, Shizuoka, Japan e-mail: [email protected]
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Case report A 65-year-old female experiencing back pain was diagnosed with gallbladder cancer and was therefore referred to our hospital for possible surgery. She had a medical history of mastectomy and chemotherapy for breast cancer 16 years previously. She had not experienced any signs of cancer recurrence. Computed tomography (CT) showed an irregular gallbladder mass involving the liver (Fig. 1). The lymph nodes along the bile duct were enlarged and suspected to contain metastatic lesions. The preoperative diagnosis was stage T3N1M0 gallbladder cancer according to the UICC classification [3]. The serum levels of tumor biomarkers, such as carcinoembryonic antigen and carbohydrate antigen 19-9 (CA19-9), were within the normal limits. A partial hepatectomy with en-bloc resection of the gallbladder and extrahepatic bile duct was performed. Lymph node dissection in the hepatoduodenal ligament and along the common hepatic artery was also performed. Macroscopically, the gallbladder tumor was 6 cm in size, with massive invasion into the liver (Fig. 2). Microscopic examination revealed poorly differentiated adenocarcinoma with lymph node metastases along the common bile duct. The final pathological stage was pT3N1M0, pStage IIB. Ten months after surgery, a follow-up CT scan showed a low density mass in the spleen (Fig. 3). The patient’s serum CA19-9 level was elevated to 127 U/ml. Fluorodeoxyglucose (FDG) positron emission tomography (FDGPET) revealed an abnormal FDG accumulation in the spleen, but not in any other organs. Isolated splenic metastasis from gallbladder cancer was highly suspected, and surgical resection was attempted. At laparotomy, no liver or peritoneal metastasis was observed. The intraoperative lavage cytology was also negative. Because tumor
Clin J Gastroenterol (2013) 6:480–484
Fig. 1 CT showed an increased wall thickness of the gallbladder and a low density irregular mass in the gallbladder involving the liver. The mass was diagnosed as gallbladder cancer invading into the liver
Fig. 2 The cut surface of the resected and fixed specimen after the first operation. The gallbladder tumor was 6 cm in size and had infiltrated into the liver
involvement of the pancreatic tail was suspected, a splenectomy with distal pancreatectomy was performed. Macroscopically, the splenic tumor was not exposed to the serosa, and was suspected to be a hematogenous metastasis rather than a peritoneal metastasis. The cut surface of the resected specimen revealed a whitish splenic mass, 2.7 cm in diameter (Fig. 4). Microscopically, the splenic tumor was poorly differentiated adenocarcinoma similar to the primary gallbladder cancer. An immunohistochemical study of the splenic tumor showed positive reactivity for cytokeratin 7, cytokeratin 19 and CA19-9, and negative reactivity for the estrogen receptor and progesterone receptor, thus indicating that the tumor represented metastasis from gallbladder cancer rather than breast cancer (Figs. 5, 6). She did not receive adjuvant chemotherapy in accordance with her wish, and
481
Fig. 3 The CT examination showed a 2 cm low density splenic mass, which was considered to be splenic metastasis
Fig. 4 The cut surface of the resected specimen from the second operation. A splenic tumor with a diameter of 2.7 cm was detected
has had no sign of recurrence 4 years after the second surgery.
Discussion Except for blood disorders, such as leukemia and lymphoma, the spleen is a rare target organ of cancer metastasis [1]. Splenic metastasis accounts for only 0.96 % of metastatic cancers, and 2.9–4.4 % of the autopsied cancer specimens [4, 5]. Most splenic metastases are accompanied with multivisceral metastases, and are commonly observed at the terminal stage of many cancers [2]. Melanoma [2, 6], breast cancer [2, 4–6], lung cancer [2, 4–6], stomach cancer [2, 5–8], colon cancer [2, 4–6] and gynecological malignancies [2, 5, 6, 9, 10] are known as primary diseases that can lead to splenic metastasis, but this form of metastasis
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Fig. 5 Histopathological characteristics including immunohistochemical study of the gallbladder tumor. a Poorly differentiated adenocarcinoma (H&E, 940). b Positive for cytokeratin-7 (940). c Positive for cytokeratin-19 (940). d Positive for CA19-9 (940)
from gallbladder cancer is extremely rare. To the best of our knowledge, this is the first report of isolated splenic metastasis from gallbladder cancer. The rarity of splenic metastases has been considered to be due to two different reasons [6]. First, mechanical factors of the spleen, such as the constant blood flow through the spleen, rhythmic contraction of the splenic capsule, the sharp angle of the splenic artery that branches from the celiac trunk, and the lack of afferent lymphatic vessels, may make the implantation of tumor cells and subsequent metastasis difficult. The other reason is that the splenic microenvironment may inhibit cancer cell growth. Miller et al. [11] reported an experimental study where they injected cancer cells directly into the liver and spleen of mice and compared the size and mitosis of the splenic metastases with those in the liver. After inoculation, the size and mitotic index (the mean number of mitoses per 1000 cells) of the liver metastases significantly increased compared to those of the spleen. Although the precise mechanism underlying such inhibition of cancer cell growth has not yet been investigated, the spleen may have some hostile immunological influence on tumor cells.
123
The diagnostic criteria for the imaging modalities used to detect splenic metastasis have not been well established. Although multi-modal imaging techniques, including CT [12], magnetic resonance imaging [13], ultrasonography [14], and FDG-PET [13], have been used for the diagnosis of splenic tumors, solitary splenic metastasis is still a diagnostic dilemma, and is difficult to differentiate from a primary tumor of the spleen. In the current case, lymphoma, vascular tumors, hamartoma, and inflammatory pseudo tumors were included in the differential diagnosis. However, the elevation of the serum CA19-9 level, abnormal FDG accumulation on PET, and the patient’s history of gallbladder cancer were highly suggestive of splenic metastasis. A fine-needle aspiration biopsy has been recommended for an accurate diagnosis of splenic metastasis by some researchers [15, 16]; however, we did not perform this because of concerns about potential hemorrhagic complications and cancer cell dissemination. Distant metastasis from gallbladder cancer is not usually an indication for surgery, but systemic chemotherapy is commonly used [17]. We performed a splenectomy with distal pancreatectomy in the current case in order to both
Clin J Gastroenterol (2013) 6:480–484
483
Fig. 6 Histopathological characteristics including immunohistochemical study of the splenic tumor. a Poorly differentiated adenocarcinoma similar to gallbladder cancer (H&E, 940). b Weakly positive for cytokeratin-7 (940). c Positive for cytokeratin-19 (940). d Positive for CA19-9 (940)
obtain a total biopsy and as the treatment. Although the patient did not undergo postoperative chemotherapy, she is still alive 4 years after surgery without any sign of recurrence. Some previous studies have reported long-term remission in patients with isolated metastasis treated by splenectomy alone [18–20]. These cases, and our present case, together suggest that isolated splenic metastasis may not necessarily be a sign of widespread cancer at the terminal stage. Although it is difficult to forecast the clinical course of solitary splenic metastasis, surgical resection may be the treatment of choice, especially in cases with a longterm recurrence-free period [6]. In conclusion, to our best knowledge, this is the first report of isolated splenic metastasis from gallbladder cancer. Although the imaging diagnosis of solitary splenic metastasis is difficult to differentiate from primary splenic tumors, the evaluation of serum tumor markers, FDG-PET, and medical history of the current case enabled us to approach the correct diagnosis. Splenectomy may be the treatment of choice for promoting longer survival in patients with isolated splenic metastasis from gallbladder cancer. Further accumulation of cases with this rare
condition will therefore be necessary to appraise the impact of splenectomy on survival. Acknowledgments type of support.
The authors declare no financial or any other
Disclosure Conflict of Interest: The authors declare that they have no conflict of interest. Human/Animal Rights: All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2008(5). Informed Consent: Informed consent was obtained from all patients for being included in the study.
References 1. Sauer J, Sobolewski K, Dommisch K. Splenic metastases–not a frequent problem, but an underestimate location of metastases: epidemiology and course. J Cancer Res Clin Oncol. 2009;135:667–71. 2. Lam KY, Tang V. Metastatic tumors to the spleen: a 25-year clinicopathologic study. Arch Pathol Lab Med. 2000;124:526–30. 3. Sobin LH, Gospodarowicz MK, Witterkind C, editors. TNM classification of malignant tumors. 7th ed. New York: WileyBlackwell; 2009.
123
484 4. Nash DA Jr, Sampson CC. Secondary carcinoma of the spleen. Its incidence in 544 cases and a review of the literature. J Natl Med Assoc. 1966;58:442–6. 5. Berge T. Splenic metastases. Frequencies and patterns. Acta Pathol Microbiol Scand A. 1974;82:499–506. 6. Comperat E, Bardier-Dupas A, Camparo P, Capron F, Charlotte F. Splenic metastases: clinicopathologic presentation, differential diagnosis, and pathogenesis. Arch Pathol Lab Med. 2007;131:965–9. 7. Kawasaki H, Kitayama J, Ishigami H, Hidemura A, Kaisaki S, Nagawa H. Solitary splenic metastasis from early gastric cancer: report of a case. Surg Today. 2010;40:60–3. 8. Yamanouchi K, Ikematsu Y, Waki S, Kida H, Nishiwaki Y, Gotoh K, et al. Solitary splenic metastasis from gastric cancer: report of a case. Surg Today. 2002;32:1081–4. 9. Alloni R, Garberini A, Caputo D, Coppola R. Solitary splenic metastasis of ovarian carcinoma: report of two cases. Surg Today. 2008;38:1144–7. 10. Yano H, Iwazawa T, Kinuta M, Nakano Y, Tono T, Matsui S, et al. Solitary splenic metastasis from ovarian cancer successfully treated by hand-assisted laparoscopic splenectomy: report of a case. Surg Today. 2002;32:750–2. 11. Miller JN, Milton GW. An experimental comparison between tumour growth in the spleen and liver. J Pathol Bacteriol. 1965;90:515–21. 12. Senturk S, Karcaaltincaba M, Akata D. CT diagnosis of intrasplenic metastasis from ovarian carcinoma. Eur J Radiol. 2012;81:1094–9.
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Clin J Gastroenterol (2013) 6:480–484 13. Soussan M, Pop G, Ouvrier MJ, Neuman A, Weinmann P. Diagnosis of synchronous isolated splenic metastasis from lung adenocarcinoma: complementary role of FDG PET/CT and diffusion-weighted MRI. Clin Nucl Med. 2011;36:707–9. 14. von Herbay A, Barreiros AP, Ignee A, Westendorff J, Gregor M, Galle PR, et al. Contrast-enhanced ultrasonography with SonoVue: differentiation between benign and malignant lesions of the spleen. J Ultrasound Med. 2009;28:421–34. 15. Cavanna L, Lazzaro A, Vallisa D, Civardi G, Artioli F. Role of image-guided fine-needle aspiration biopsy in the management of patients with splenic metastasis. World J Surg Oncol. 2007;5:13. 16. Duggal R, Garg M, Kalra N, Srinivasan R, Chawla Y. Spleen metastasis from hepatocellular carcinoma: report of a case with diagnosis by fine needle aspiration cytology. Acta Cytol. 2010;54:783–6. 17. Valle J, Wasan H, Palmer DH, Cunningham D, Anthoney A, Maraveyas A, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362:1273–81. 18. Agha-Mohammadi S, Calne RY. Solitary splenic metastasis: case report and review of the literature. Am J Clin Oncol. 2001;24:306–10. 19. Piardi T, D’Adda F, Giampaoli F, Pulcini G, Lancini GP, Pouche A. Solitary metachronous splenic metastases: an evaluation of surgical treatment. J Exp Clin Cancer Res. 1999;18:575–8. 20. de Wilt JH, McCarthy WH, Thompson JF. Surgical treatment of splenic metastases in patients with melanoma. J Am Coll Surg. 2003;197:38–43.
CASE REPORT
Postoperative isolated splenic metastasis from gallbladder cancer: report of a case Yusuke Taki • Teiichi Sugiura • Kazuya Matsunaga Hideyuki Kanemoto • Takashi Mizuno • Yukiyasu Okamura • Katsuhiko Uesaka
•
Received: 24 July 2013 / Accepted: 9 September 2013 / Published online: 25 September 2013 Ó Springer Japan 2013
Abstract We present a rare case of metachronous splenic metastasis from gallbladder cancer. A 65-year-old female with gallbladder cancer underwent a partial hepatectomy with en-bloc resection of the gallbladder and extrahepatic bile duct. Ten months later, she presented with isolated splenic metastasis and underwent splenectomy with distal pancreatectomy. The histological diagnosis confirmed metastatic adenocarcinoma from gallbladder cancer. She had no signs of recurrence 4 years after the second surgery. To the best of our knowledge, this is the first report of isolated splenic metastasis from gallbladder cancer. Keywords Gallbladder cancer Splenic metastasis Splenectomy
Introduction Splenic metastases are rare, and have been found in only 0.96 % of the reported metastatic cancer patients [1]. Because most splenic metastases are diagnosed as a part of multivisceral metastatic diseases, isolated splenic metastases are extremely rare [2]. We report a case of isolated splenic metastasis from gallbladder cancer, which was successfully treated by splenectomy with distal pancreatectomy.
Y. Taki T. Sugiura (&) K. Matsunaga H. Kanemoto T. Mizuno Y. Okamura K. Uesaka Division of Hepato-Biliary-Pancreatic Surgery, Shizuoka Cancer Center, 1007 Shimo-Nagakubo, Sunto-Nagaizumi, Shizuoka, Japan e-mail: [email protected]
123
Case report A 65-year-old female experiencing back pain was diagnosed with gallbladder cancer and was therefore referred to our hospital for possible surgery. She had a medical history of mastectomy and chemotherapy for breast cancer 16 years previously. She had not experienced any signs of cancer recurrence. Computed tomography (CT) showed an irregular gallbladder mass involving the liver (Fig. 1). The lymph nodes along the bile duct were enlarged and suspected to contain metastatic lesions. The preoperative diagnosis was stage T3N1M0 gallbladder cancer according to the UICC classification [3]. The serum levels of tumor biomarkers, such as carcinoembryonic antigen and carbohydrate antigen 19-9 (CA19-9), were within the normal limits. A partial hepatectomy with en-bloc resection of the gallbladder and extrahepatic bile duct was performed. Lymph node dissection in the hepatoduodenal ligament and along the common hepatic artery was also performed. Macroscopically, the gallbladder tumor was 6 cm in size, with massive invasion into the liver (Fig. 2). Microscopic examination revealed poorly differentiated adenocarcinoma with lymph node metastases along the common bile duct. The final pathological stage was pT3N1M0, pStage IIB. Ten months after surgery, a follow-up CT scan showed a low density mass in the spleen (Fig. 3). The patient’s serum CA19-9 level was elevated to 127 U/ml. Fluorodeoxyglucose (FDG) positron emission tomography (FDGPET) revealed an abnormal FDG accumulation in the spleen, but not in any other organs. Isolated splenic metastasis from gallbladder cancer was highly suspected, and surgical resection was attempted. At laparotomy, no liver or peritoneal metastasis was observed. The intraoperative lavage cytology was also negative. Because tumor
Clin J Gastroenterol (2013) 6:480–484
Fig. 1 CT showed an increased wall thickness of the gallbladder and a low density irregular mass in the gallbladder involving the liver. The mass was diagnosed as gallbladder cancer invading into the liver
Fig. 2 The cut surface of the resected and fixed specimen after the first operation. The gallbladder tumor was 6 cm in size and had infiltrated into the liver
involvement of the pancreatic tail was suspected, a splenectomy with distal pancreatectomy was performed. Macroscopically, the splenic tumor was not exposed to the serosa, and was suspected to be a hematogenous metastasis rather than a peritoneal metastasis. The cut surface of the resected specimen revealed a whitish splenic mass, 2.7 cm in diameter (Fig. 4). Microscopically, the splenic tumor was poorly differentiated adenocarcinoma similar to the primary gallbladder cancer. An immunohistochemical study of the splenic tumor showed positive reactivity for cytokeratin 7, cytokeratin 19 and CA19-9, and negative reactivity for the estrogen receptor and progesterone receptor, thus indicating that the tumor represented metastasis from gallbladder cancer rather than breast cancer (Figs. 5, 6). She did not receive adjuvant chemotherapy in accordance with her wish, and
481
Fig. 3 The CT examination showed a 2 cm low density splenic mass, which was considered to be splenic metastasis
Fig. 4 The cut surface of the resected specimen from the second operation. A splenic tumor with a diameter of 2.7 cm was detected
has had no sign of recurrence 4 years after the second surgery.
Discussion Except for blood disorders, such as leukemia and lymphoma, the spleen is a rare target organ of cancer metastasis [1]. Splenic metastasis accounts for only 0.96 % of metastatic cancers, and 2.9–4.4 % of the autopsied cancer specimens [4, 5]. Most splenic metastases are accompanied with multivisceral metastases, and are commonly observed at the terminal stage of many cancers [2]. Melanoma [2, 6], breast cancer [2, 4–6], lung cancer [2, 4–6], stomach cancer [2, 5–8], colon cancer [2, 4–6] and gynecological malignancies [2, 5, 6, 9, 10] are known as primary diseases that can lead to splenic metastasis, but this form of metastasis
123
482
Clin J Gastroenterol (2013) 6:480–484
Fig. 5 Histopathological characteristics including immunohistochemical study of the gallbladder tumor. a Poorly differentiated adenocarcinoma (H&E, 940). b Positive for cytokeratin-7 (940). c Positive for cytokeratin-19 (940). d Positive for CA19-9 (940)
from gallbladder cancer is extremely rare. To the best of our knowledge, this is the first report of isolated splenic metastasis from gallbladder cancer. The rarity of splenic metastases has been considered to be due to two different reasons [6]. First, mechanical factors of the spleen, such as the constant blood flow through the spleen, rhythmic contraction of the splenic capsule, the sharp angle of the splenic artery that branches from the celiac trunk, and the lack of afferent lymphatic vessels, may make the implantation of tumor cells and subsequent metastasis difficult. The other reason is that the splenic microenvironment may inhibit cancer cell growth. Miller et al. [11] reported an experimental study where they injected cancer cells directly into the liver and spleen of mice and compared the size and mitosis of the splenic metastases with those in the liver. After inoculation, the size and mitotic index (the mean number of mitoses per 1000 cells) of the liver metastases significantly increased compared to those of the spleen. Although the precise mechanism underlying such inhibition of cancer cell growth has not yet been investigated, the spleen may have some hostile immunological influence on tumor cells.
123
The diagnostic criteria for the imaging modalities used to detect splenic metastasis have not been well established. Although multi-modal imaging techniques, including CT [12], magnetic resonance imaging [13], ultrasonography [14], and FDG-PET [13], have been used for the diagnosis of splenic tumors, solitary splenic metastasis is still a diagnostic dilemma, and is difficult to differentiate from a primary tumor of the spleen. In the current case, lymphoma, vascular tumors, hamartoma, and inflammatory pseudo tumors were included in the differential diagnosis. However, the elevation of the serum CA19-9 level, abnormal FDG accumulation on PET, and the patient’s history of gallbladder cancer were highly suggestive of splenic metastasis. A fine-needle aspiration biopsy has been recommended for an accurate diagnosis of splenic metastasis by some researchers [15, 16]; however, we did not perform this because of concerns about potential hemorrhagic complications and cancer cell dissemination. Distant metastasis from gallbladder cancer is not usually an indication for surgery, but systemic chemotherapy is commonly used [17]. We performed a splenectomy with distal pancreatectomy in the current case in order to both
Clin J Gastroenterol (2013) 6:480–484
483
Fig. 6 Histopathological characteristics including immunohistochemical study of the splenic tumor. a Poorly differentiated adenocarcinoma similar to gallbladder cancer (H&E, 940). b Weakly positive for cytokeratin-7 (940). c Positive for cytokeratin-19 (940). d Positive for CA19-9 (940)
obtain a total biopsy and as the treatment. Although the patient did not undergo postoperative chemotherapy, she is still alive 4 years after surgery without any sign of recurrence. Some previous studies have reported long-term remission in patients with isolated metastasis treated by splenectomy alone [18–20]. These cases, and our present case, together suggest that isolated splenic metastasis may not necessarily be a sign of widespread cancer at the terminal stage. Although it is difficult to forecast the clinical course of solitary splenic metastasis, surgical resection may be the treatment of choice, especially in cases with a longterm recurrence-free period [6]. In conclusion, to our best knowledge, this is the first report of isolated splenic metastasis from gallbladder cancer. Although the imaging diagnosis of solitary splenic metastasis is difficult to differentiate from primary splenic tumors, the evaluation of serum tumor markers, FDG-PET, and medical history of the current case enabled us to approach the correct diagnosis. Splenectomy may be the treatment of choice for promoting longer survival in patients with isolated splenic metastasis from gallbladder cancer. Further accumulation of cases with this rare
condition will therefore be necessary to appraise the impact of splenectomy on survival. Acknowledgments type of support.
The authors declare no financial or any other
Disclosure Conflict of Interest: The authors declare that they have no conflict of interest. Human/Animal Rights: All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2008(5). Informed Consent: Informed consent was obtained from all patients for being included in the study.
References 1. Sauer J, Sobolewski K, Dommisch K. Splenic metastases–not a frequent problem, but an underestimate location of metastases: epidemiology and course. J Cancer Res Clin Oncol. 2009;135:667–71. 2. Lam KY, Tang V. Metastatic tumors to the spleen: a 25-year clinicopathologic study. Arch Pathol Lab Med. 2000;124:526–30. 3. Sobin LH, Gospodarowicz MK, Witterkind C, editors. TNM classification of malignant tumors. 7th ed. New York: WileyBlackwell; 2009.
123
484 4. Nash DA Jr, Sampson CC. Secondary carcinoma of the spleen. Its incidence in 544 cases and a review of the literature. J Natl Med Assoc. 1966;58:442–6. 5. Berge T. Splenic metastases. Frequencies and patterns. Acta Pathol Microbiol Scand A. 1974;82:499–506. 6. Comperat E, Bardier-Dupas A, Camparo P, Capron F, Charlotte F. Splenic metastases: clinicopathologic presentation, differential diagnosis, and pathogenesis. Arch Pathol Lab Med. 2007;131:965–9. 7. Kawasaki H, Kitayama J, Ishigami H, Hidemura A, Kaisaki S, Nagawa H. Solitary splenic metastasis from early gastric cancer: report of a case. Surg Today. 2010;40:60–3. 8. Yamanouchi K, Ikematsu Y, Waki S, Kida H, Nishiwaki Y, Gotoh K, et al. Solitary splenic metastasis from gastric cancer: report of a case. Surg Today. 2002;32:1081–4. 9. Alloni R, Garberini A, Caputo D, Coppola R. Solitary splenic metastasis of ovarian carcinoma: report of two cases. Surg Today. 2008;38:1144–7. 10. Yano H, Iwazawa T, Kinuta M, Nakano Y, Tono T, Matsui S, et al. Solitary splenic metastasis from ovarian cancer successfully treated by hand-assisted laparoscopic splenectomy: report of a case. Surg Today. 2002;32:750–2. 11. Miller JN, Milton GW. An experimental comparison between tumour growth in the spleen and liver. J Pathol Bacteriol. 1965;90:515–21. 12. Senturk S, Karcaaltincaba M, Akata D. CT diagnosis of intrasplenic metastasis from ovarian carcinoma. Eur J Radiol. 2012;81:1094–9.
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Clin J Gastroenterol (2013) 6:480–484 13. Soussan M, Pop G, Ouvrier MJ, Neuman A, Weinmann P. Diagnosis of synchronous isolated splenic metastasis from lung adenocarcinoma: complementary role of FDG PET/CT and diffusion-weighted MRI. Clin Nucl Med. 2011;36:707–9. 14. von Herbay A, Barreiros AP, Ignee A, Westendorff J, Gregor M, Galle PR, et al. Contrast-enhanced ultrasonography with SonoVue: differentiation between benign and malignant lesions of the spleen. J Ultrasound Med. 2009;28:421–34. 15. Cavanna L, Lazzaro A, Vallisa D, Civardi G, Artioli F. Role of image-guided fine-needle aspiration biopsy in the management of patients with splenic metastasis. World J Surg Oncol. 2007;5:13. 16. Duggal R, Garg M, Kalra N, Srinivasan R, Chawla Y. Spleen metastasis from hepatocellular carcinoma: report of a case with diagnosis by fine needle aspiration cytology. Acta Cytol. 2010;54:783–6. 17. Valle J, Wasan H, Palmer DH, Cunningham D, Anthoney A, Maraveyas A, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362:1273–81. 18. Agha-Mohammadi S, Calne RY. Solitary splenic metastasis: case report and review of the literature. Am J Clin Oncol. 2001;24:306–10. 19. Piardi T, D’Adda F, Giampaoli F, Pulcini G, Lancini GP, Pouche A. Solitary metachronous splenic metastases: an evaluation of surgical treatment. J Exp Clin Cancer Res. 1999;18:575–8. 20. de Wilt JH, McCarthy WH, Thompson JF. Surgical treatment of splenic metastases in patients with melanoma. J Am Coll Surg. 2003;197:38–43.
