Metastasis of Rectal Adenocarcinoma to the Pancreas. Two Case Reports and a Review of the Literature
Jeannine Bachmann1, Christoph W Michalski1, Frank Bergmann2, Markus W Büchler1, Jörg Kleeff1, Helmut Friess1
Departments of 1General Surgery and 2Pathology. University of Heidelberg. Heidelberg, Germany
- *Corresponding Author:
- Helmut Friess
Department of General Surgery
University of Heidelberg
Im Neuenheimer Feld 110
E-mail: [email protected]
Received January 8th, 2007 - Accepted January 19th, 2007
Context The vast majority of pancreatic tumors are of pancreatic origin. Nonetheless, a variety of extrapancreatic tumors can involve the pancreas and may manifest with different clinicopathological characteristics. Case report We report on two patients with a history of rectal cancer who were referred to our department with a pancreatic mass: one patient 2 years after a low anterior resection (TNM stage: pT3 pN0 pM0), the other patient 2.5 years after an abdominoperineal resection (TNM stage: pT3 pN1 pM0). In the first case, computed tomography showed a cystic mass in the pancreas but fine-needle biopsy followed by cytopathological analysis revealed only necrotic tissue. In the other patient, magnetic resonance tomography showed a hypodense structure in the pancreatic body/tail. Suspecting pancreatic tumors, distal pancreatectomies were carried out. Subsequent histological examination revealed metastases of rectal cancer in both cases. Conclusion In patients with a history of a malignant tumor, a newly diagnosed mass in the pancreas - although rare - should raise the suspicion of metastatic disease. Surgical resection may be an option for a curative approach which can be offered to otherwise healthy patients if there is no evidence of other metastases.
Colorectal Neoplasms; Neoplasm Metastasis; Pancreatic Neoplasms; Surgery
Two patients were referred for explorative laparotomy and resection of the tumors in the pancreas.
A 61-year-old woman in good general condition presented to our department complaining of abdominal pain in the left upper quadrant. She had had the pain for at least one year. Past medical history revealed that a low anterior resection for a poorly differentiated (G3) rectal adenocarcinoma had been performed 2 years before presentation (TNM stage: pT3 pN0 pM0); neoadjuvant radiation therapy had been administered before that surgery and no adjuvant treatment had been given. Computed tomography of the abdomen showed a cystic structure in the pancreatic tail (Figure 1a,b); upon fine needle biopsy and cytopathological analysis, only necrotic tissue was detectable. Neither colonoscopy nor chest X-ray showed any signs of local recurrence or metastases of the rectal cancer. Routine laboratory testing, including blood count, levels of serum electrolytes as well as renal and liver function tests, did not show any significant changes. However, tumor markers CA 19-9 and CEA were elevated: CA 19-9: 541 U/mL (reference range: 0-37 U/mL), CEA: 128 μg/L (reference range: 0-2.5 μg/L).
Figure 1. Abdominal CT scan of case 1 which shows
the tumor mass (5.9x6.3 cm) in the tail of the pancreas
(arrows; a. b.). Resected specimen with pancreatic tail
and spleen (c.) and a closer view of the tumor in the
pancreatic tail (d.).
The second patient was a 64-year-old woman in good general condition who was referred to our department 2.5 years after surgery for rectal cancer performed in March 2003 and subsequent adjuvant radiochemotherapy. Histological examination at that time had shown a moderately differentiated (G2) adenocarcinoma with TNM stage pT3 pN1 pM0. At the end of 2004, the patient presented with metastases to the lungs, which were resected by a partial left lobectomy. In 2005, the patient presented with elevated tumor markers (CEA 24.4 μg/L; reference range: 0-2.5 μg/L). Magnetic resonance tomography showed hypodense structures in the pancreatic body/tail, suspicious for metastases of rectal cancer (Figure 2a,b).
Figure 2. Abdominal MRI scan of case 2: A 4x4 cm
hypointense mass in the pancreatic tail (arrows).
In the first patient, surgical exploration revealed a large mass with a diameter of 6 centimeters in the tail of the pancreas, in close proximity to the spleen and stomach. As there was no evidence of any metastatic disease to the liver or peritoneal cavity, a careful mobilization was carried out, followed by a distal pancreatectomy. In addition, a splenectomy and a wedge resection of the stomach were performed. Figure 1c,d shows the specimen and a closer view of the metastasis to the pancreas.
The surgical exploration of the second patient revealed no evidence of any metastases to the peritoneal cavity, the liver or the pancreatic head. A tumor of approximately 5 cm was found in the body/tail of the pancreas, in close proximity to the splenic artery. Thus, a distal pancreatectomy with splenectomy was performed.
Pathologic examination of the operation specimen revealed a firm, solid mass in the pancreatic tail, measuring 6 cm at its largest diameter. The cut surface was white and contained multifocal foci of necrosis. The tumor showed invasion of the peripancreatic fatty tissue without well-defined margins. Furthermore, an intrapancreatic accessory spleen of 1.3 cm was found in the pancreatic tail. Microscopically, the tumor consisted of solid and sheet-like formations as well as irregular and distorted glandular formations of atypical epithelial cells (Figure 3ab). The tumor displayed marked necrosis. Immunohistochemically, the tumor cells showed expression of cytokeratin 20 and CDX2, while cytokeratin 7 did not stain the tumor cells. The tumor invaded the peripancreatic fatty tissue. Lymph node metastases were detected in 4 of 18 peripancreatic lymph nodes. The resection margins were free of tumor. The diagnosis was pancreatic metastasis of a poorly differentiated adenocarcinoma of intestinal differentiation (well compatible with a metastasis of the known rectal adenocarcinoma).
Figure 3. Histomorphological and immunohistochemical
findings in the pancreatic masses of case
1 (a. b.) and case 2 (c. d. e. f.): Both tumors displayed
irregular glandular formations of pleomorphic
epithelial cells with basophilic cytoplasm and
prominent nucleoli. There was mild to moderate
desmoplastic stromal reaction (a. b.) and marked
necrosis (c.). The tumor margins towards the pancreatic
tissue (a. pancreatic tissue depicted on the left) and
towards the peripancreatic fatty tissue were not welldefined.
Immunohistochemically, the tumor lacked
expression of cytokeratin 7 (d.). On the other hand, the
tumor cells showed expression of the intestinal markers
cytokeratin 20 (e.) and CDX2 (f.).
Case 2 At gross pathologic examination of case 2, a 5 cm solid, firm mass having a white to greyish cut surface was found in the pancreatic tail, infiltrating the peripancreatic fatty tissue, the spleen, and the wall of an adjacent gastric wedge resection specimen. Necroses were seen in the peritumoral soft tissue. Microscopically, the tumor displayed irregular glandular formations of atypical epithelial cells, containing abundant and frequently comedo-like necrosis (Figure 3c). Immunohistochemically, the tumor cells were negative for cytokeratin 7 (Figure 3d) but positive for cytokeratin 20 (Figure 3e) and CDX2 (Figure 3f). The tumor invaded the peripancreatic fatty tissue, the spleen, the adjacent gastric wall and two of nine peripancreatic lymph nodes. Acute inflammation and plurifocal necroses were seen in the pancreatic and fatty tissue surrounding the tumor. The resection margins were free of tumor. The diagnosis was pancreatic metastasis of a moderately differentiated adenocarcinoma of intestinal differentiation (well compatible with a metastasis of the known rectal adenocarcinoma).
The patient recovered postoperatively without any complications. The routinely placed drains were removed on the first postoperative day. The patient was discharged eight days after surgery. Adjuvant chemotherapy was refused by the patient. Six weeks later, the patient presented again with a palpable tumor in the skin of the chest wall which was also resected. Histopathology revealed a lesion which was also compatible with a metastasis of the rectal cancer.
The second patient also had a smooth postoperative course without any complications. The routinely placed drains were removed on the first postoperative day. The patient was discharged twelve days after surgery. Six months later, the patient presented with a metastasis to the liver which was resected. Thereafter, the patient was treated with 5-fluorouracil/folinic acid (5- FU/FA) and oxaliplatin (FOLFOX) for four months and, subsequently, with capecitabin (Xeloda®) and oxaliplatin.
REVIEW OF THE LITERATURE ON METASTASES TO THE PANCREAS
The majority of pancreatic tumors are primary [1, 2], and metastases to the pancreas are rare. A variety of extrapancreatic tumors can involve the pancreas secondarily and may manifest with different clinicopathological characteristics. The final diagnosis of metastatic disease to the pancreas can be confirmed either by operative resection and subsequent histopathological examination of the resected specimen or by fine needle aspiration.
The majority of pancreatic tumors are primary [1, 2], and metastases to the pancreas are rare. A variety of extrapancreatic tumors can involve the pancreas secondarily and may manifest with different clinicopathological characteristics. The final diagnosis of metastatic disease to the pancreas can be confirmed either by operative resection and subsequent histopathological examination of the resected specimen or by fine needle aspiration. In 4,955 adult autopsies and 973 pancreatic surgical specimens, the prevalence of different metastatic tumors in the pancreas was 1.6% of all examined autopsy cases and 3.9% of patients with pancreatic resections . These tumors had various origins, including the lung, gastrointestinal tract, kidney, breast, liver, ovary, and urinary bladder . In 690 autopsies of patients with a malignant primary tumor other than pancreatic cancer, a metastasis to the pancreas was diagnosed in 15% of cases . This study indicates that, in about one out of six autopsy cases of patients with malignant tumors, metastases to the pancreas can be found. In a Japanese study, the most common origin of the primary malignancy was the stomach, followed by the lung in 17% of cases and the extrahepatic bile duct in 13%; in this series, 18% of the secondary tumors in the pancreas were due to direct invasion by the primary tumor, including malignant stomach tumors (19%) and extrahepatic bile duct cancer (54%) . In Figure 4, the different primary tumors found in patients with metastases to the pancreas are shown, broken down by autopsy series and resection. The publications included are case reports and retrospective analyses.
Figure 4. Number of cases of metastasis to the
pancreas in autopsy series (a.) [1, 3] and surgical series
(b.) [2, 3, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19,
20, 21, 22, 23, 34, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34,
35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49,
50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64,
65, 66, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79,
80, 81, 82, 83, 84, 85, 86, 87, 88, 89, 90, 91, 92, 93, 94,
95, 96, 97, 98, 99, 100, 101, 102, 103].
Although metastases to the pancreas are rare, in patients with a pancreatic mass, metastatic disease may be considered, especially if the patient has a history of malignant disease. The most common sources of primary tumors generating such metastases are the kidney and the lungs; in a few cases, colorectal and breast cancer as well as melanomas are possible primaries. The published data show that, especially for metastases from kidney cancer, there may be a long time between resection of the primary tumor and the appearance of the metastases. In a series of 4,955 autopsy cases, 42% of the tumors in the pancreas were metastases from other organs  and, in a study of 690 autopsy cases in patients with malignant tumors, a metastasis to the pancreas was diagnosed in 15% of the cases . Metastases to the pancreas have various manifestations; they can present as solid tumors, cystic structures, and hypodense or hyperdense structures on computed tomography imaging [4, 5]. If there is doubt, an explorative laparotomy should be performed to confirm the diagnosis and to resect the tumor.
Immunohistochemical examinations may be helpful in establishing the diagnosis if clinical or histomorphological features indicate the possibility of a metastasis to the pancreas. Whereas only a few cases of colorectal adenocarcinoma show expression of cytokeratin 7, most of these tumors express cytokeratin 20 . An opposite staining pattern is found in pancreatic ductal adenocarcinoma . Furthermore, CDX2 is frequently expressed in colorectal carcinoma whereas it is only rarely expressed in pancreatic ductal adenocarcinoma . In cases such as the ones presented, the application of a combination of several antibodies may be especially helpful for diagnosis, although the expression of the detected proteins is not exclusively confined to one tumor entity or the other.
As shown in prospective analyses of patients resected for metastases of the pancreas, a median survival of up to 22 months and 5- year survival rates of 25% after resection of the metastatic disease are reported [8, 9]. Surgical resection may be offered to patients with metastatic disease to the pancreas, and they should be referred to centers with experience in pancreatic surgery.
- Adsay NV, Andea A, Basturk O, Kilinc N, NassarH, Cheng JD. Secondary tumors of the pancreas: an analysis of a surgical and autopsy database and review of the literature. Virchows Arch 2004; 444:527-35. [PMID 15057558]
- Hiotis SP, Klimstra DS, Conlon KC, Brennan MF. Results after pancreatic resection for metastatic lesions. Ann SurgOncol 2002; 9:675-9. [PMID 12167582]
- Nakamura E, Shimizu M, Itoh T, Manabe T. Secondary tumors of the pancreas: clinicopathologicalstudy of 103 autopsy cases of Japanese patients. PatholInt 2001; 51:686-90. [PMID 11696171]
- Chou YH, Chiou HJ, Hong TM, Tiu CM, ChiouSY, Su CH, Tsay SH. Solitary metastasis from renal cell carcinoma presenting as diffuse pancreatic enlargement. J Clin Ultrasound 2002; 30:499-502. [PMID 12242739]
- Kleeff J, FriessH, Buchler MW. What is the most accurate test to differentiate pancreatic cystic neoplasms? Nat ClinPractGastroenterolHepatol2004; 1:18-9. [PMID 16265037]
- Tot T. Adenocarcinomas metastatic to the liver: the value of cytokeratins 20 and 7 in the search for unknown primary tumors. Cancer 1999; 85:171-7.[PMID 9921990]
- De Lott LB, Morrison C, Suster S, Cohn DE, Frankel WL. CDX2 is a useful marker of intestinaltypedifferentiation: a tissue microarray-based study of 629 tumors from various sites. Arch Pathol Lab Med 2005; 129:1100-5. [PMID 16119980]
- Sperti C, PasqualiC, Liessi G, Pinciroli L, DecetG, Pedrazzoli S. Pancreatic resection for metastatic tumors to the pancreas. J SurgOncol 2003; 83:161-6. [PMID 12827684]
- Z'graggen K, Fernandez-del Castillo C, RattnerDW, Sigala H, Warshaw AL. Metastases to the pancreas and their surgical extirpation. Arch Surg1998; 133:413-7. [PMID 9565122]
- Abbas MA, Collins JM, Mulligan DC. Renal cell carcinoma metastatic to pancreas. Am J Surg 2001; 182:183-4. [PMID 11574093]
- Adachi K, Murabayashi K, Hayashi J, et al. A case of metastatic thyroid and pancreatic cancer from renal cell carcinoma. Tan to Sui 1992; 13:791-6.
- Aikou S, Tokura Y, Yamafuji K, et al. A resected case of pancreatic metastasis from renal cell carcinoma presenting with acute duodenal bleeding.J JpnSocClinSurg 1993; 54:2666-72.
- Amamiya H, Iizumi T, Yazaki T, et al. A solitary pancreatic metastasis from renal cell carcinoma.HinyoukiGeka 1998; 2:167-70.
- Andoh H, Kurokawa T, Yasui O, Shibata S, Sato T. Resection of a solitary pancreatic metastasis from renal cell carcinoma with a gallbladder carcinoma: report of a case. Surg Today 2004; 34:272-5. [PMID 14999544]
- Audisio RA, La Monica G. Solitary pancreatic metastasis occurring 20 years after nephrectomy for carcinoma of the kidney. Tumori 1985; 71:197-200.[PMID 4002351]
- Bachmann J, Kleeff J, Bergmann F, ShrikhandeSV, Hartschuh W, Buchler MW, Friess H. Pancreatic metastasis of Merkel cell carcinoma and concomitant insulinoma: case report and literature review. World J SurgOncol 2005; 3:58. [PMID 16137328]
- Bassi C, Butturini G, Falconi M, Sargenti M, Mantovani W, Pederzoli P. High recurrence rate after atypical resection for pancreatic metastases from renal cell carcinoma. Br J Surg 2003; 90:555-9. [PMID 12734861]
- Biset JM, Laurent F, de Verbizier G, Houang B, Constantes G, Drouillard J. Ultrasound and computed tomographic findings in pancreatic metastases. Eur J Radiol 1991; 12:41-4. [PMID 1999210]
- BoudgheneFP, Deslandes PM, LeBlanche AF, Bigot JM. US and CT imaging features of intrapancreatic metastases.J Comput Assist Tomogr1994; 18:905-10. [PMID 7962797]
- Butturini G, Bassi C, Falconi M, Salvia R, Caldiron E, Iannucci A, et al. Surgical treatment of pancreatic metastases from renal cell carcinomas. Dig Surg 1998; 15:241-6. [PMID 9845592]
- Carini M, Selli C, Barbanti G, Bianchi S, MuraroG. Pancreatic late recurrence of bilateral renal cell carcinoma after conservative surgery. EurUrol 1988; 14:258-60. [PMID 3383938]
- Derias NW, Chong WH. Fine needle aspiration diagnosis of a late solitary pancreatic metastasis of renal adenocarcinoma. Cytopathology 1993; 4:369-72.[PMID 8110977]
- Dousset B, Andant C, Guimbaud R, Roseau G, Tulliez M, Gaudric M, et al. Late pancreatic metastasis from renal cell carcinoma diagnosed by endoscopic ultrasonography.Surgery 1995; 117:591-4. [PMID 7740433]
- Faure JP, Tuech JJ, Richer JP, Pessaux P, Arnaud JP, Carretier M. Pancreatic metastasis of renal cell carcinoma: presentation, treatment and survival. J Urol2001; 165:20-2. [PMID 11125354]
- Fricke P, Schulz HU, Buhtz P, Lippert H. Multiple metachronous metastases of renal cell carcinoma in the pancreas. Case report and review of the literature.Chirurg 2000; 71:575-9. [PMID 10875018]
- Frilling A, Becker H, Ackermann R, Kantartzis M, Roher HD. Multilocular metastatic renal cell carcinoma. Chirurg 1992; 63:68-71. [PMID 1547650]
- Fujii M, Kogawa T, Matsuyama K, et al. A case ofmetastatic renal cell carcinoma to pancreas ten yearsafter nephrectomy. J Kyoto PrefUniv Med 1992; 101:589-96.
- FullartonGM, Burgoyne M. Gallbladder and pancreatic metastases from bilateral renal carcinoma presenting with hematobilia and anemia. Urology 1991; 38:184-6. [PMID 1877140]
- Furukawa T, Hattori R, Ohtake H, et al. A resectable case of pancreatic head metastasis from renal cell carcinoma.HinyoukiGeka 1991; 4:111-4.
- Ghavamian R, Klein KA, Stephens DH, Welch TJ, LeRoy AJ, Richardson RL, et al. Renal cell carcinoma metastatic to the pancreas: clinical and radiological features. Mayo ClinProc 2000; 75:581-5. [PMID 10852418]
- Gillet M, Camelot G, Runser C, Clement D. Duodeno-pancreatic metastasis of kidney cancer revealed by digestive hemorrhage and treated by cephalic duodenopancreatectomy. Chirurgie 1974; 100:226-30. [PMID 4548014]
- Gohji K, Matsumoto O, Kamidono S. Solitary pancreatic metastasis from renal cell carcinoma. Hinyokika Kiyo 1990; 36:677-81. [PMID 2239559]
- Guttman FM, Ross M, Lachance C. Pancreatic metastasis of renal cell carcinoma treated by total pancreatectomy. Arch Surg 1972; 105:782-4. [PMID 5081552]
- Hashimoto M, Watanabe G, Matsuda M, Dohi T, TsurumaruM. Management of the pancreatic metastases from renal cell carcinoma: report of four resected cases. Hepatogastroenterology 1998; 45:1150- 4. [PMID 9756024]
- Hermanutz KD,Sonnenberg GE. Late matastasisof a hypernephroid kidney carcinoma to the pancreas with tumor invasion to the duodenum.Rofo 1977; 127:595-7. [PMID 146014]
- Hirano M, Douden K, Bantou H, et al. Solitary pancreatic metastasis occurring 10 years after nephrectomy for carcinoma of the kidney. Tan to Sui 1988; 9:233-7.
- Hirota T, Tomida T, Iwasa M, Takahashi K, Kaneda M, Tamaki H. Solitary pancreatic metastasis occurring eight years after nephrectomy for renal cell carcinoma. A case report and surgical review.Int J Pancreatol 1996; 19:145-53. [PMID 8723558]
- Ishikawa T, Horimi T, Majima K. A resected case of pancreatic tumor metastasized from renal cell carcinoma. A review of 11 cases in the Japanese and 13 cases of the foreign literature.J JpnSocClinSurg1993; 54:1642-7.
- Iwamoto I, Fujino T, Higashi Y, Tsuji T, Nakamura N, Komokata T, Douchi T. Metastasis of uterine leiomyosarcoma to the pancreas. J ObstetGynaecol Res 2005; 31:531-4. [PMID 16343254]
- Iwanami M, Nakayoshi A, Yagi H, et al. A resected case of the asymptomatic pancreatic metastasis in the body and tail of the pancreas from renal cell carcinoma .J JpnPancSoc 1989; 4:100-6.
- Jarufe N, McMaster P, Mayer AD, Mirza DF, Buckels JA, OrugT, et al. Surgical treatment of metastases to the pancreas. Surgeon 2005; 3:79-83. [PMID 15861941]
- Jingu K, Watanabe K, Yamamoto H, Fujita Y, Honda I, Watanabe S, et al. Surgical treatment of a solitary pancreatic metastasis from renal cell carcinoma: report of a case. Surg Today 1998; 28:91-4.[PMID 9505325]
- Kassabian A, Stein J, Jabbour N, Parsa K, Skinner D, Parekh D, et al. Renal cell carcinoma metastatic to the pancreas: a single-institution series and review of the literature. Urology 2000; 56:211-5. [PMID 10925080]
- Kawaguchi T, Tsunoda T, Tanaka Y,et al. A case of resection of a solitary pancreatic metastasis of renal cell carcinoma occurring 5 years after nephrectomy.J JpnPancSoc 1993; 8:189-95.
- Kelekis NL, Semelka RC, Siegelman ES. MRI of pancreatic metastases from renal cancer.J Comput Assist Tomogr 1996; 20:249-53. [PMID 8606232]
- Kishimoto H, Nimura Y, Okamoto K, TsuchieK,Yamase H, Maeda S, et al. A case of resected renal cell carcinoma with massive pancreatic metastases.Gan No Rinsho 1985; 31:91-6. [PMID 3981807]
- Klein KA, Stephens DH, Welch TJ. CT characteristics of metastatic disease of the pancreas.Radiographics 1998; 18:369-78. [PMID 9536484]
- Komeda H, Fujimoto Y, Horie M, et al. Metastatic renal cell carcinoma to the pancreas and adrenal gland was diagnosed before surgical treatment: A case report. HinyoukiGeka 1990; 3:765-8.
- Kubo K, Morita J, Mizoe J, et al. Renal cell carcinoma metastatic to the pancreas 8 years following nephrectomy. Jpn J ClinRadiol 1991; 36:509-12.
- Law CH, Wei AC, Hanna SS, Al-Zahrani M, Taylor BR, Greig PD, et al. Pancreatic resection for metastatic renal cell carcinoma: presentation, treatment, and outcome. Ann SurgOncol 2003; 10:922-6. [PMID 14527912]
- Lawson LJ, Holt LP, Rooke HW.Recurrent duodenal haemorrhagefrom renal carcinoma.Br J Urol1966; 38:133-7. [PMID 5295908]
- Le Borgne J, Partensky C, Glemain P, Dupas B, de Kerviller B. Pancreaticoduodenectomy for metastatic ampullary and pancreatic tumors.Hepatogastroenterology 2000; 47:540-4. [PMID 10791233]
- Marquand J, Giraud B, Maliakas S. Pancreatic metastasis revealing a kidney neoplasm. J UrolNephrol (Paris) 1971; 77:595-601. [PMID 5314914]
- Marrano D, Campione O, Casadei R, et al. I tumoriesocrini delpancreas . In: Mazzeo F FP ed. Trattato di chirurgiaoncologica. Padova: PiccinNuovaLibraria; 2003:1-22.
- Marusch F, Koch A, Dietrich F, Hoschke B, Gastinger I. Singular late metastasis of renal cellcarcinoma in the pancreas. An unusual pancreatic tumor.ZentralblChir 2001; 126:391-5. [PMID 11396249]
- Medina-Franco H, Urist MM, Fiveash J, HeslinMJ, Bland KI, Beenken SW. Multimodality treatment of Merkel cell carcinoma: case series and literature review of 1024 cases. Ann SurgOncol 2001; 8:204-8. [PMID 11314935]
- Motoyama S, Terashima H, Matsuoka T, et al. A case of renal cell carcinoma metastasizing to pancreas and skin 19 years after nephrectomy.Jpn J GastroenterolSurg 1993; 26:2863.
- Moussa A,Mitry E, Hammel P, Sauvanet A, Nassif T, Palazzo L, et al. Pancreatic metastases: a multicentricstudy of 22 patients. GastroenterolClinBiol 2004; 28:872-6. [PMID 15523224]
- MuranakaT, Teshima K, Honda H, Nanjo T, Hanada K, Oshiumi Y. Computed tomography and histologic appearance of pancreatic metastases from distant sources. ActaRadiol 1989; 30:615-9. [PMID 2631949]
- Nakagawa K, Tsuchiya T, Momono S, et al. A case of pancreatic metastasis of renal cell carcinoma.Jpn J GastroenterolSurg 1992; 25:2200-4.
- Nan Y, Kuno N, Kurimoto K, Nakamura T ,Kobayashi S. A resected case of pancreatic tumor metastasized from renal cell carcinoma diagnosed by endoscopic biopsy through the main pancreatic duct. GastroenterolEndosc 1993; 35:1380-5.
- Oda K, Itoh J, Hachisuka K, Yamaguchi A, IsogaiM, Utsunomiya H, et al. Value of computer image analysis in improving ERCP images in metastatic tumor of the pancreas. AJR Am J Roentgenol 1993; 161:885-6. [PMID 8372781]
- Oka H, Hatayama T, Taki Y, Ueyama H, Hida S, Noguchi M. A resected case of renal cell carcinoma with metastasis to pancreas.Hinyokika Kiyo 1991; 37:1531-4. [PMID 1767775]
- Opocher E, Galeotti F, Spina GP, Battaglia G, Hernandez C. Diagnosis of secondary tumors of the pancreas. Analysis of 13 cases. Minerva Med 1982; 73:577-81. [PMID 7063125]
- Orita M, Morita N, Hiraoka H, et al. A case of resected pancreatic metastasis from renal cell carcinoma 14 years after radical nephrectomy.J JpnPancSoc 1995; 10:63-8.
- Osaka Y, Kato H, Nakamura F, et al. Solitary pancreatic metastasis from renal cell carcinoma. Jpn J GastroenterolSurg 1994; 27:130-4.
- Pappo I, Feigin E, Uziely B, Amir G. Biliary and pancreatic metastases of breast carcinoma: is surgical palliation indicated? J SurgOncol 1991; 46:211-4.[PMID 1707119]
- Pingpank JF Jr, Hoffman JP, Sigurdson ER, Ross E, Sasson AR, Eisenberg BL. Pancreatic resection for locally advanced primary and metastatic nonpancreaticneoplasms. Am Surg 2002; 68:337-40. [PMID 11952243]
- Robbins EG 2nd, FranceschiD, Barkin JS. Solitary metastatic tumors to the pancreas: a case report and review of the literature. Am J Gastroenterol1996; 91:2414-7. [PMID 8931428]
- Roland CF, van Heerden JA. Nonpancreaticprimary tumors with metastasis to the pancreas.SurgGynecolObstet 1989; 168:345-7. [PMID 2928909]
- Rumancik WM, Megibow AJ, Bosniak MA, Hilton S. Metastatic disease to the pancreas: evaluation by computed tomography. J Comput Assist Tomogr1984; 8:829-34. [PMID 6470248]
- Rypens F, Van Gansbeke D, Lambilliotte JP, Van Regemorter G, Verhest A, Struyven J. Pancreatic metastasis from renal cell carcinoma. Br J Radiol1992; 65:547-8. [PMID 1628191]
- Sahin M, Foulis AA, Poon FW, Imrie CW. Late focal pancreatic metastasis of renal cell carcinoma. Dig Surg 1998; 15:72-4. [PMID 9845567]
- Sauvanet A, Barthes T, Levy P, Flejou JF, Delcenserie R, Bernades P, Belghiti J. Late pancreatic metastasis from renal cell carcinoma. Pancreas 1993; 8:742-4. [PMID 8255891]
- Saxon A, Gottesman J, Doolas A. Bilateral hypernephroma with solitary pancreatic metastasis. J SurgOncol 1980; 13:317-22. [PMID 7374163]
- Sharma SK, Kumar A, Madhusoodnan P, Banerjee CK, Suri S, Dhar ML. Solitary pancreatic metastasis from renal cell carcinoma. A rare metastatic site.Indian J Cancer 1988; 25:29-32. [PMID 3181987]
- Shinagawa Y, Suzuki T, Hamanaka Y, Nishihara K, Takahasi M. Solitary pancreatic metastasis of malignant fibroushistiocytoma treated by distal pancreatectomy.Pancreas 1992; 7:726-30. [PMID 1333081]
- Simpson NS, Mulholland CK, Lioe TF, Spence RA. Late, solitary metastatic renal carcinoma in the pancreas.Ulster Med J 1989; 58:198-9. [PMID 2603277]
- Skaarup P, Jorgensen T, Larsen S. Asynchronous metastasizing renal cell carcinoma associated with progressive immune complex glomerulonephritis and proteinuria. Scand J UrolNephrol 1984; 18:351-6.[PMID 6239372]
- Sobesky R, Duclos-Vallee JC, Prat F, Pelletier G, Encaoua R, Boige V, et al. Acute pancreatitis revealingdiffuse infiltration of the pancreas by melanoma.Pancreas 1997; 15:213-5. [PMID 9260209]
- Stankard CE, Karl RC. The treatment of isolated pancreatic metastases from renal cell carcinoma: a surgical review. Am J Gastroenterol 1992; 87:1658-60.[PMID 1442695]
- Strijk SP. Pancreatic metastases of renal cell carcinoma: report of two cases. GastrointestRadiol1989; 14:123-6. [PMID 2651194]
- Tabata T, Kuroda Y, Nishimatsu S, et al. A resected case of pancreatic tumor metastasized from renal cell carcinoma. J JpnPancSoc 1991; 6:245-50.
- Takeuchi H, Konaga E, Harano M, Watanabe K, Takeuchi Y, Hara M, Mano S. Solitary pancreatic metastasis from renal cell carcinoma. Acta Med Okayama 1993; 47:63-6. [PMID 8460557]
- Tanabe S, Soeda S, Mukai T, Oki S, Yun K, Miyahara S. A case report of pancreatic metastasis of an intracranial angioblastic meningioma (hemangiopericytoma) and a review of metastatic tumor to the pancreas.J SurgOncol 1984; 26:63-8.[PMID 6727388]
- Temellini F, Bavosi M, Lamarra M, Quagliarini P, Giuliani F. Pancreatic metastasis 25 years after nephrectomy for renal cancer. Tumori 1989; 75:503-4.[PMID 2603224]
- Terashima M, Abe H, Suga K, et al. Two cases of renal cell carcinoma metastasized to the pancreas and to the gallbladder.Jpn J GastroenterolSurg 1990; 23:1952-6.
- Thompson LD, Heffess CS. Renal cell carcinoma to the pancreas in surgical pathology material. Cancer 2000; 89:1076-88. [PMID 10964338]
- Torres-Villalobos G, Podgaetz E, Anthon FJ, Remes-Troche JM, Robles-Diaz G, Nunez CC. Single pancreatic metastasis from a previously resected carcinoma of the cecum: a case report. CurrSurg 2004; 61:328-30. [PMID 15165777]
- Tutton MG, George M, Hill ME, Abulafi AM. Solitary pancreatic metastasis from a primary colonic tumor detected by PET scan: report of a case. Dis Colon Rectum 2001; 44:288-90. [PMID 11227949]
- Uemura T, Kurita A, Nishimura R, Ishizaki M, Takashima S. Solitary pancreatic metastasis from renal cell carcinoma concomitant with early gastric cancer 17 years after nephrectomy: report of a case. SurgToday 2003; 33:395-8. [PMID 12734740]
- Vergara V, Marucci M, Marcarino C, Brunello F, Capussotti L. Metastatic involvement of the pancreas from renal cell carcinoma treated by surgery. Ital J Gastroenterol 1993; 25:388-90. [PMID 7904193]
- Volmar KE, Jones CK, Xie HB. Metastases in the pancreas from nonhematologic neoplasms: report of 20 cases evaluated by fine-needle aspiration. DiagnCytopathol 2004; 31:216-20. [PMID 15452907]
- Weerdenburg JP, Jurgens PJ. Late metastases of a hypernephroma to the thyroid and the pancreas.Diagn Imaging Clin Med 1984; 53:269-72. [PMID 6567496]
- Wehrschutz M,Stoger H, Ploner F, Hofmann G, Wolf G, Hofler G, et al. Seminoma metastases mimicking primary pancreatic cancer. Onkologie 2002; 25:371-3. [PMID 12232490]
- Wente MN, Bergmann F, Frohlich BE, Schirmacher P, Buchler MW, Friess H. Pancreatic metastasis from gastric carcinoma: a case report. World J SurgOncol 2004; 2:43. [PMID 15585066]
- Wente MN, KleeffJ, Esposito I, Hartel M, Muller MW, Frohlich BE, et al. Renal cancer cell metastasis into the pancreas: a single-center experience and overview of the literature. Pancreas 2005; 30:218-22. [PMID 15782097]
- Wernecke K, Peters PE, Galanski M. Pancreatic metastases: US evaluation. Radiology 1986; 160: 399- 402. [PMID 3523591]
- Yamamoto H, Watanabe K, Nagata M, Honda I, Watanabe S, Soda H,Tatezaki S. Surgical treatment for pancreatic metastasis from soft-tissue sarcoma: report of two cases. Am J ClinOncol 2001; 24:198- 200. [PMID 11319298]
- Yamamoto S,Tobinaga K, Taketomi K, et al. Pancreatic metastasis of renal cell carcinoma occurring 17 years after nephrectomy. J JpnSocClinSurg 1991; 52:3006-11.
- Yanagisawa T, Nakayama K, Kashiwagi M, et al. Three cases of resectable pancreatic metastases from renal cell carcinoma.GekaShinryo 1993; 35:651-5.
- Yazaki T, Ishikawa S, Ogawa Y, Takahashi S, Nemoto S, Rinsho K, et al. Silent pancreatic metastasis from renal cell carcinoma diagnosed at arteriography. ActaUrolJpn 1981; 12:1517-21.
- Yu PC, Lin YC, Chen HM, Chen MF. Malignant phyllodes tumor of the breast metastasizing to the pancreas: case report. Chang Gung Med J 2000;23:503-7. [PMID 11039254]