Endocrine tumours of the pancreas

Histopathology

Volumn 56, Issue 6, 2010, Pages 669-682

  Verbeke, Caroline S ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

Carcinoma; Endocrine; Pancreas; Pathology; Tumour

Indexed keywords

ACTIN; CD56 ANTIGEN; CHROMOGRANIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYTOKERATIN 19; DESMIN; EOSIN; GLUCAGON; HEMATOXYLIN; INSULIN; K RAS PROTEIN; KI 67 ANTIGEN; LIPOFUSCIN; MELAN A; PANCREAS POLYPEPTIDE; PROTEIN P16; PROTEIN P53; SMAD4 PROTEIN; SOMATOSTATIN; SYNAPTOPHYSIN;

ACINAR CELL CARCINOMA; CANCER CLASSIFICATION; CANCER GRADING; CANCER STAGING; DIFFERENTIAL DIAGNOSIS; DISEASE COURSE; ENDOCRINE TUMOR; FAMILY HISTORY; GENE MUTATION; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; LIVER METASTASIS; MICROADENOMA; MORPHOLOGY; MULTIPLE ENDOCRINE NEOPLASIA; NEUROFIBROMATOSIS; OUTCOME ASSESSMENT; PANCREAS CARCINOMA; PANCREAS RESECTION; PANCREAS TUMOR; PATIENT CARE; PERIVASCULAR EPITHELIOID CELL TUMOR; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; PSEUDOTUMOR; REVIEW; TUMOR LOCALIZATION; TUMOR VOLUME; VON HIPPEL LINDAU DISEASE; WORLD HEALTH ORGANIZATION; CLASSIFICATION; PANCREAS; PANCREAS ISLET; PATHOLOGY; TREATMENT OUTCOME;

ENDOCRINE GLAND NEOPLASMS; HUMANS; ISLETS OF LANGERHANS; NEOPLASM STAGING; PANCREAS; PROGNOSIS; TREATMENT OUTCOME; WORLD HEALTH ORGANIZATION;

EID: 77951745916     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/j.1365-2559.2010.03490.x     Document Type: Review

References (105)

1. Klöppel G, Perren A, Heitz PU. The gastroenteropancreatic neuroendocrine cell system and its tumors: the WHO classification. Ann. NY Acad. Sci. 2004 1014 13 27.
2. Rindi G, Klöppel G, Alhman H et al. TNM staging of foregut(neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Arch. 2006 449 395 401.
3. The Royal College of Pathologists. Standards and datasets for reporting cancers. Dataset for endocrine tumours of the gastrointestinal tract including pancreas.
4. Halfdanarson TR, Rubin J, Farnell MB, Grant CS, Petersen GM. Pancreatic endocrine neoplasms: epidemiology and prognosis of pancreatic endocrine tumors. Endocr. Relat. Cancer 2008 15 409 427.
5. Yao JC, Hassan M, Phan A et al. One hundred years after "carcinoid": epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J. Clin. Oncol. 2008 26 3063 3072.
6. Grimelius L, Hultquist GT, Stenkvist B. Cytological differentiation of asymptomatic pancreatic islet cell tumours in autopsy material. Virchows Arch. A Pathol. Anat. Histol. 1975 365 275 288.
7. Kimura W, Kuroda A, Morioka Y. Clinical pathology of endocrine tumors of the pancreas. Analysis of autopsy cases. Dig. Dis. Sci. 1991 36 933 942.
8. Hochwald SN, Zee S, Conlon KC et al. Prognostic factors in pancreatic endocrine neoplasms: an analysis of 136 cases with a proposal for low-grade and intermediate-grade groups. J. Clin. Oncol. 2002 20 2633 2642.
9. Ferrone CR, Tang LH, Tomlinson J et al. Determining prognosis in patients with pancreatic endocrine neoplasms: Can the WHO classification system be simplified? J. Clin. Oncol. 2007 25 5609 5615.
10. Ekeblad S, Skogseid B, Dunder K, Öberg J, Eriksson B. Prognostic factors and survival in 324 patients with pancreatic endocrine tumour treated at a single institution. Clin. Cancer Res. 2008 14 7798 7803.
11. Ligneau B, Lombard-Bohas C, Partensky C et al. Cystic endocrine tumors of the pancreas. Clinical, radiologic, and histopathologic features in 13 cases. Am. J. Surg. Pathol. 2001 25 752 760.
12. Smith AE, Levi AW, Nadasdy T, Campbell KA, Fishman FK, Hruban RH. The pigmented "black" neuroendocrine tumor of the pancreas: a question of origin. Cancer 2001 92 1984 1991.
13. Singh R, Basturk O, Klimstra DS et al. Lipid-rich variant of pancreatic endocrine neoplasms. Am. J. Surg. Pathol. 2006 30 194 200.
14. Chetty R, El-Shinnawy I. Intraductal pancreatic neuroendocrine tumor. Endocr. Pathol. 2009 20 (4 262 266.
15. The Royal College of Pathologists. Standards and minimum datasets for reporting cancers. Minimum dataset for the histopathological reporting of pancreatic, ampulla of Vater and bile duct carcinoma
16. Verbeke CS. Resection margins and R1 rates in pancreatic cancer - are we there yet? Histopathology 2008 52 787 796.
17. Chetty R, Serra S. Spindle cell pancreatic endocrine tumor associated with Cushing's syndrome. Endocr. Pathol. 2005 16 145 151.
18. Volante M, La Rosa S, Catellano I, Finzi G, Capella C, Bussolati G. Clinico-pathological features of a series of 11 oncocytic endocrine tumors of the pancreas. Virchows Arch. 2006 448 545 551.
19. Chetty R, Asa SL. Pancreatic endocrine tumour with cytoplasmic keratin whorls. Is the term "rhabdoid" appropriate? J. Clin. Pathol. 2004 57 1106 1110.
20. Perez-Montiel MD, Frankel WL, Suster S. Neuroendocrine carcinomas of the pancreas with "rhabdoid" features. Am. J. Surg. Pathol. 2003 27 642 649.
21. Shia J, Erlandson RA, Klimstra DS. Whorls of intermediate filaments with entrapped neurosecretory granules correspond to the "rhabdoid" inclusions seen in pancreatic endocrine neoplasms. Am. J. Surg. Pathol. 2004 28 271 273.
22. Zee SY, Hochwald SN, Conlon KC, Brennan MF, Klimstra DS. Pleomorphic pancreatic endocrine neoplasms. A variant commonly confused with adenocarcinoma. Am. J. Surg. Pathol. 2005 29 1194 1200.
23. Ordóñez NG, Silva EG. Islet cell tumour with vacuolated lipid-rich cytoplasm: a new histological variant of islet cell tumour. Histopathology 1997 31 157 160.
24. Hoang MP, Hruban RH, Albores-Saavedra J. Clear cell endocrine pancreatic tumor mimicking renal cell carcinoma: a distinctive neoplasm of von Hippel-Lindau disease. Am. J. Surg. Pathol. 2001 25 602 609. (Pubitemid 32423357)
25. Lubensky IA, Pack S, Ault D et al. Multiple neuroendocrine tumors of the pancreas in von Hippel-Lindau disease patients: histopathological and molecular genetic analysis. Am. J. Pathol. 1998 153 223 231.
26. Hameed O, Xu H, Saddeghi S, Maluf H. Hepatoid carcinoma of the pancreas. A case report and literature review of a heterogeneous group of tumors. Am. J. Surg. Pathol. 2007 31 146 152.
27. Berkel S, Hummel F, Gaa J et al. Poorly differentiated small cell carcinoma of the pancreas. A case report and review of the literature. Pancreatology 2004 4 521 526.
28. Chetty R, Clark SP, Pitson GA. Primary small cell carcinoma of the pancreas. Pathology 1993 25 240 242.
29. Mao C, El Attar A, Domenico DR, Kim K, Howard JM. Carcinoid tumors of the pancreas. Status report based on two cases and review of the world's literature. Int. J. Pancreatol. 1998 23 153 164.
30. Deshpande V, Fernandez-del Castillo C, Muzikansky A et al. Cytokeratin 19 is a powerful predictor of survival in pancreatic endocrine tumors. Am. J. Surg. Pathol. 2004 28 1145 1153.
31. Schmitt AM, Anlauf M, Rousson V et al. WHO 2004 criteria and CK19 are reliable prognostic markers in pancreatic endocrin tumors. Am. J. Surg. Pathol. 2007 31 1677 1682.
32. Ohike N, Morohoshi T. Immunohistochemical analysis of cyclooxygenase (COX)-2 expression in pancreatic endocrine tumors: association with tumor progression and proliferation. Pathol. Int. 2001 51 770 777.
33. Rahman A, Maitra A, Ashfaq R, Yeo CJ, Cameron JL, Hansel DE. Loss of p27 nuclear expression in a prognostically favourable subset of well-differentiated pancreatic endocrine neoplasms. Am. J. Clin. Pathol. 2003 120 685 690.
34. Ali S, Serra SL, Chetty R. The predictive value of CK19 and CD99 in pancreatic endocrine tumors. Am. J. Surg. Pathol. 2006 30 1588 1594.
35. Zhang L, Smyrk TC, Oliveira AM et al. KIT is an independent prognostic marker for pancreatic endocrine tumors. A finding derived from analysis of islet cell differentiation markers. Am. J. Surg. Pathol. 2009 [Epub ahead of print].
36. Bilimoria KY, Talamonti MS, Tomlinson JS et al. Prognostic score predicting survival after resection of pancreatic endocrine tumors. Analysis of 3851 patients. Ann. Surg. 2008 247 490 500.
37. Fischer L, Kleeff J, Esposito I et al. Clinical outcome and long-term survival in 118 consecutive patients with neuroendocrine tumours of the pancreas. Br. J. Surg., 2008 95 627 635.
38. Phan GQ, Yeo CJ, Hruban RH, Lillemoe KD, Pitt HA, Cameron JL. Surgical experience with pancreatic and peripancreatic neuroendocrine tumours: review of 125 patients. J. Gastrointest. Surg. 1998 2 473 482.
39. Ballian N, Loeffler AG, Rajamanickam V, Nostedt PA, Weber SM, Cho CS. A simplified prognostic system for resected pancreatic neuroendocrine neoplasms. HPB (Oxford) 2009 11 422 428.
40. Solcia E, Klöppel G, Sobin LH. Histological typing of endocrine tumors.
41. DeLellis RA, Lloyd RV, Heitz PU, Eng C eds. World Health Organization classification of tumours. Pathology and genetics of tumours of endocrine organs.
42. Bettini R, Boninsegna L, Mantovani W et al. Prognostic factors at diagnosis and value of WHO classification in a mono-institutional series of 180 non-functioning pancreatic endocrine tumours. Ann. Oncol. 2008 19 903 908.
43. Boninsegna L, Bettini R, Crippa S et al. Survival and prognostic factors at diagnosis in non-functioning pancreatic endocrine tumors: analysis of 180 patients. JOP 2007 8 645 696.
44. Schindl M, Kaczirek K, Kaserer K, Niederle B. Is the new classification of neuroendocrine pancreatic tumors of clinical help? World J. Surg. 2000 24 1312 1318.
45. Sobin LH, Wittekind C eds. International Union Against Cancer TNM classification of malignant tumours, 6th edn
46. Pape U-F, Jann H, Müller-Nordhorn J et al. Prognostic relevance of a novel TNM classification system for upper gastroenteropancreatic neuroendocrine tumors. Cancer 2008 113 256 265.
47. Oien K. Pathologic evaluation of unknown primary cancer. Semin. Oncol. 2009 36 8 37.
48. Chu PG, Lau SK, Weiss LM. Keratin expression in endocrine organs and their neoplasms. Endocr. Pathol. 2009 20 1 10.
49. Spigel D, Hainsworth J, Greco F. Neuroendocrine carcinoma of unknown primary site. Semin. Oncol. 2009 36 52 59.
50. Saqi A, Alexis D, Remotti F, Bhagat G. Usefulness of CDX2 and TTF-1 in differentiating gastrointestinal from pulmonary carcinoids. Am. J. Clin. Pathol. 2005 123 394 404.
51. Srivastava A, Hornick JL. Immunohistochemical staining for CDX-2, PDX-1, NESP-55, and TTF-1 can help distinguish gastrointestinal carcinoid tumors from pancreatic endocrine and pulmonary carcinoid tumors. Am. J. Surg. Pathol. 2009 33 626 632.
52. Jagirdar J. Application of immunohistochemistry to the diagnosis of primary and metastatic carcinoma to the lung. Arch. Pathol. Lab. Med. 2008 132 384 396.
53. Jaffee IM, Rahmani M, Singhal MG, Younes M. Expression of the intestinal transcription factor CDX2 in carcinoid tumors is a marker of midgut origin. Arch. Pathol. Lab. Med. 2006 130 1522 1526.
54. Moskaluk CA, Zhang H, Powell SM, Cerilli LA, Hampton GM, Frierson HF Jr. Cdx2 protein expression in normal and malignant human tissues: an immunohistochemical survey using tissue microarrays. Mod. Pathol. 2003 16 913 919.
55. Schmitt AM, Riniker F, Anlauf M et al. Islet 1 (Isl1) expression is a reliable marker for pancreatic endocrine tumors and their metastases. Am. J. Surg. Pathol. 2008 32 420 425.
56. Carpelan-Holmström M, Nordling S, Pukkala E et al. Does anyone survive pancreatic ductal adenocarcinoma? A nationwide study re-evaluating the data of the Finnish Cancer Registry. Gut 2005 54 385 387.
57. Deschamps L, Handra-Luca A, O'Toole D et al. CD10 expression in pancreatic endocrine tumors: correlation with prognostic factors and survival. Hum. Pathol. 2006 37 802 808.
58. Ramuz O, Lelong B, Giovannini M et al. "Sugar" tumor of the pancreas: a rare entity that is diagnosable on preoperative fine-needle biopsies. Virchows Arch. 2005 446 555 559.
59. Martignoni G, Pea M, Reghellin D, Zamboni G, Bonetti F. PEComas: the past, the present and the future. Virchows Arch. 2008 452 119 132.
60. Bismar TA, Basturk O, Gerald WL, Schwarz K, Adsay NV. Desmoplastic small cell tumor in the pancreas. Am. J. Surg. Pathol. 2004 28 808 812.
61. Movahedi-Lankarani S, Hruban RH, Westra WH, Klimstra DS. Primitive neuroectodermal tumors of the pancreas. A report of seven cases of a rare neoplasm. Am. J. Surg. Pathol. 2002 26 1040 1047.
62. Perek S, Perek A, Sarman K, Tuzun H, Buyukunal E. Primitive neuroectodermal tumor of the pancreas. A case report of an extremely rare tumor. Pancreatology 2003 3 352 356.
63. Hamilton SR, Aaltonen LA, eds. World Health Organization classification of tumours. Pathology and genetics of tumours of the digestive system.
64. Cavallini A, Falconi M, Bortesi L, Crippa S, Barugola G, Butturini G. Pancreatoblastoma in adults: a review of the literature. Pancreatology 2009 9 73 80.
65. Panzuto F, Nasoni S, Falconi M et al. Prognostic factors and survival in endocrine tumor patients: comparison between gastrointestinal and pancreatic localization. Endocr. Relat. Cancer 2005 12 1083 1092.
66. Metz DC, Jensen RT. Gastrointestinal neuroendocrine tumors: pancreatic endocrine tumors. Gastroenterology 2008 135 1469 1492.
67. Strosberg J, Gardner N, Kvols L. Survival and prognostic factor analysis in patients with metastatic pancreatic endocrine carcinomas. Pancreas 2009 38 255 258.
68. Plöckinger U, Wiedenmann B. Treatment of gastroenteropancreatic neuroendocrine tumors. Virchows Arch. 2007 451 (Suppl. 1 S71 S80.
69. Falconi M, Plöckinger U, Kwekkeboom DJ et al. Well-differentiated pancreatic non-functioning tumors/carcinoma. Neuroendocrinology 2006 84 196 211.
70. De Herder WW, Niederle B, Scoazec JY et al. Well-differentiated pancreatic tumor/carcinoma: insulinoma. Neuroendocrinology 2006 84 183 188.
71. Jensen RT, Niederle B, Mitry F et al. Gastrinoma (duodenal and pancreatic). Neuroendocrinology 2006 84 173 182.
72. O'Toole D, Salazar R, Falconi M et al. Rare functioning pancreatic endocrine tumors. Neuroendocrinology 2006 84 189 195.
73. Butturini G, Bettini R, Missiaglia E et al. Predictive factors of efficacy of the somatostatin analogue octreotide as first line therapy for advanced pancreatic endocrine carcinoma. Endocr. Relat. Cancer 2006 13 1213 1221.
74. Vilar E, Salazar R, Pérez-García J, Cortes J, Öberg K, Tabernero J. Chemotherapy and role of the proliferation marker Ki-67 in digestive neuroendocrine tumors. Endocr. Relat. Cancer 2007 14 221 232.
75. Nilsson O, Van Cutsem E, Delle Fave G et al. Poorly differentiated carcinomas of the foregut (gastric, duodenal and pancreatic). Neuroendocrinology 2006 84 212 215.
76. Shia J, Tang LH, Weiser MR et al. Is nonsmall cell type high-grade neuroendocrine carcinoma of the tubular gastrointestinal tract a distinct disease entity? Am. J. Surg. Pathol. 2008 32 719 731.
77. Capelli P, Martignoni G, Pedica F et al. Endocrine neoplasms of the pancreas. Pathologic and genetic features. Arch. Pathol. Lab. Med. 2009 133 350 364.
78. Antonello D, Gobbo S, Corbo V, Sipos B, Lemoine NR, Scarpa A. Update on the molecular pathogenesis of pancreatic tumors other than common ductal adenocarcinoma. Pancreatology 2009 9 25 33.
79. Perren A, Komminoth P, Heitz PU. Molecular genetics of gastroenteropancreatic endocrine tumors. Ann. NY Acad. Sci. 2004 1014 199 208.
80. Speel EJ, Richter J, Moch H et al. Genetic differences in pancreatic endocrine tumor subtypes detected by comparative genomic hybridization. Am. J. Pathol. 1999 155 1787 1794.
81. Zhao J, Moch H, Scheidweiler AF et al. Genomic imbalances in the progression of endocrine pancreatic tumors. Genes Chromosomes Cancer 2001 32 364 372.
82. Moore PS, Orlandini S, Zamboni G et al. Pancreatic tumours: molecular pathways implicated in ductal cancer are involved in ampullary but not in exocrine nonductal or endocrine tumorigenesis. Br. J. Cancer 2001 84 253 262.
83. Duerr EM, Chung DC. Molecular genetics of neuroendocrine tumors. Best Pract. Res. Clin. Endocrinol. Metab. 2007 21 1 14.
84. Moore PS, Missiaglia E, Antonello D et al. Role of disease-causing genes in sporadic pancreatic endocrine tumors: MEN1 and VHL. Genes Chromosomes Cancer 2001 32 177 181.
85. Capurso G, Lattimore S, Cmogorac-Jurcevic T et al. Gene expression profiles of progressive pancreatic endocrine tumours and their liver metastases reveal potential novel markers and therapeutic targets. Endocr. Relat. Cancer 2006 13 541 558.
86. Rindi G, Villanacci V, Ubiali A, Scarpa A. Endocrine tumors of the digestive tract and pancreas: histogenesis, diagnosis and molecular basis. Expert Rev. Mol. Diagn. 2001 1 323 333.
87. Maioli M, Ciccarese M, Pacificio A et al. Familial insulinoma: description of 2 cases. Acta Diabetol. 1992 29 38 40.
88. Jensen RT, Berna MJ, Bingham DB, Norton JA. Inherited pancreatic endocrine tumor syndromes: advances in molecular pathogenesis, diagnosis, management, and controversies. Cancer 2008 113 (7 Suppl. 1807 1843.
89. Schnepp RW, Chen YX, Wang H et al. Mutation of tumor suppressor gene Men1 acutely enhances proliferation of pancreatic islet cells. Cancer Res. 2006 66 5707 5715.
90. Karnik SK, Hughes CM, Gu X et al. Menin regulates pancreatic islet growth by promoting histone methylation and expression of genes encoding p27Kip1 and p18INK4c. Proc. Natl Acad. Sci. USA 2005 102 14659 14664.
91. Karnik SK, Chen H, McLean GW et al. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 2007 318 806 809.
92. Triponez F, Dosseh D, Goudet P et al. Epidemiology data on 108 MEN 1 patients from the GTE with isolated non-functioning tumors of the pancreas. Ann. Surg. 2006 243 265 272.
93. Triponez F, Goudet P, Dosseh D et al. French Endocrine Tumor Study Group. Is surgery beneficial for MEN1 patients with small (< or = 2 cm), non-functioning pancreaticoduodenal endocrine tumor? An analysis of 65 patients from the GTE. World J. Surg. 2006 30 654 662.
94. Dean PG, van Heerden JA, Farley DR et al. Are patients with multiple endocrine neoplasia type 1 prone to premature death? World J. Surg. 2000 24 1437 1441.
95. Bartsch DK, Langer P, Wild A et al. Pancreaticoduodenal endocrine tumors in multiple endocrine neoplasia type 1: surgery or surveillance? Surgery 2000 128 958 966.
96. Hes F, van der Luijt R, Lips C. Clinical management of von Hippel-Lindau disease. Neth. J. Med. 2001 59 225 234.
97. Mao C, Shah A, Hanson DJ, Howard JM. Von Recklinghausen's disease associated with duodenal somatostatinoma: contrast of duodenal versus pancreatic somatostatinomas. J. Surg. Oncol. 1995 59 67 73.
98. Ilgren EB, Westmoreland D. Tuberous sclerosis: unusual associations in 4 cases. J. Clin. Pathol. 1984 37 272 278.
99. Merritt JL, Davis DM, Pittelkow MR et al. Extensive acrochordons and pancreatic islet-cell tumors in tuberous sclerosis associated with TSC2 mutations. Am. J. Med. Genet. A 2006 140 1669 1672.
100. Périgny M, Hammel P, Corcos O et al. Pancreatic endocrine microadenomatosis in patients with von Hippel-Lindau disease. Am. J. Surg. Pathol. 2009 33 730 748.
101. Anlauf M, Schlenger R, Perren A et al. Microadenomatosis of the endocrine pancreas in patients with and without the Multiple Endocrine Neoplasia Type 1 syndrome. Am. J. Surg. Pathol. 2006 30 560 574.
102. Albazaz R, Da Costa PE, Verbeke CS. Pancreatic polypeptide cell hyperplasia of the pancreas. J. Clin. Pathol. 2006 59 1087 1090.
103. Henopp T, Anlauf M, Schmitt A et al. Glucagon cell adenomatosis: a newly recognized disease of the endocrine pancreas. J. Clin. Endocrinol. Metab. 2009 94 213 217.
104. Yu R, Nissen NN, Dhall D, Heaney AP. Nesidioblastosis and hyperplasia of a cells, microglucagonoma, and non-functioning islet cell tumor of the pancreas: review of the literature. Pancreas 2008 36 428 431.
105. Ramage JK, Davies AH, Ardill J et al. Guidelines for the management of gastroenteropancreatic neuroendocrine (including carcinoid) tumours. Gut 2005 54 (Suppl. 4 iv1 iv16.