Skip to main content
SpringerLink
Log in

Revised classification of neuroendocrine tumours of the lung, pancreas and gut

  • Review Article
  • Published:
Virchows Archiv Aims and scope Submit manuscript

Abstract

In this article new classifications of the neuroendocrine tumours of the lung, pancreas and gut are proposed. These classifications use a common frame work and attempt to consider the morphological, functional as well as biological features of the tumours.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Ahlman H, Dahlstrom A, Enerbach L, Granerus G, Nilsson O, Persson S, Tissell LE (1988) Two cases of gastric carcinoids: diagnostic and therapeutic aspects. World J Surg 12:356–361

    Google Scholar 

  2. Alumets J, Hakanson R, Ingemansson S, Sundler F (1977) SP and 5-HT in granules isolated from an intestinal argentaffin carcinoid. Histochemistry 52:217–222

    Google Scholar 

  3. Alumets J, Alm P, Falkmer S, Hakanson R, Ljungberg H, Martenssen H, Sundler F, Tibblin S (1981) Immunohistochemical evidence of peptide hormones in endocrine tumours of the rectum. Cancer 48:2409–2415

    Google Scholar 

  4. Anderson JR, Wilson BG (1985) Carcinoid tumours of the appendix. Br J Surg 72:545–546

    Google Scholar 

  5. Arrigoni MG, Woolner LB, Bernatz PE (1972) Atypical carcinoid tumours of the lung. J Thoracic Carciovasc Surg 64:413–421

    Google Scholar 

  6. Aubock L, Ratzenhofer M (1982) “Extraepithelial enterochromaffin cell-nerve-fibre complexes” in the normal human appendix and in neurogenic appendicopathy. J Pathol 136:217–226

    Google Scholar 

  7. Azzoni C, Yu JY, Baggi MT, D'Adda T, Timson C, Polak JM, Bordi C (1992) Studies on co-localization of 7B2 and pancreatic hormones in normal and tumoural islet cells. Virchows Arch [A] 421:457–466

    Google Scholar 

  8. Barbareschi M, Frigo B, Aldovini D, Leonardi E, Christina S, Falleni M (1989) Duodenal gangliocytic paraganglioma. Report of a case and review of the literature. Virchows Arch [A] 416:81–89

    Google Scholar 

  9. Barbareschi M, Girlando S, Mauri FA, Arrigoni G, Laurino L, Palma PD, Doglioni C (1992) Tumour suppressor gene products, proliferation and differentiation markers in lung neuroendocrine neoplasms. J Pathol 166:343–350

    Google Scholar 

  10. Bates HR Jr (1962) Carcinoid tumours of the rectum. Dis Colon Rectum 5:270–280

    Google Scholar 

  11. Berardi RS (1972) Carcinoid tumours of the colon (exclusive of the rectum). Dis Colon Rectum 15:383–391

    Google Scholar 

  12. Bishop AE, Power RF, Polak JM (1988) Markers for neuroendocrine differentiation. Pathol Res Pract 183:119–128

    Google Scholar 

  13. Böhm J, Kacic V, Gais P, Präuer HW, Höfler H (1993) Prognostic value of nucleolar organizer regions in neuroendocrine tumours of the lung. Histochemistry 99:85–90

    Google Scholar 

  14. Bonato M, Cerati M, Pagani A, Papotti M, Bosi F, Bussolati G, Capella C (1992) Differential diagnostic patterns of lung neuroendocrine tumours. Virchows Arch 420:201–211

    Google Scholar 

  15. Bordi C, Pilato FP, D'Adda T (1988) Comparative study of seven neuroendocrine markers in pancreatic endocrine tumours. Virchows Arch [A] 413:387–398

    Google Scholar 

  16. Bordi C, Yu JY, Baggi MT, Davoli C, Pilato FP, Baruzzi G, Gardini A, Zamboni G, Franzin G, Papotti M, Bussolati G (1991) Gastric carcinoids and their precursors lesions. A histologic and immunohistochemical study of 23 cases. Cancer 67:663–672

    Google Scholar 

  17. Bowman GA, Rosenthal D (1983) Carcinoid tumours of the appendix. Am J Surg 146:700–703

    Google Scholar 

  18. Buffa R, Rindi G, Sessa F, Gini A, Capella C, Jahn R, Navone F, De Camilli P, Solcia E (1988) Synaptophysin immunoreactivity and small clear vesicles in neuroendocrine cells and related tumours. Mol Cell Probes 2:367–381

    Google Scholar 

  19. Burke AP, Federspiel BH, Sobin LH, Shekitka KM, Helwig EB (1989) Carcinoids of the duodenum. A histologic and immunohistochemical study of 65 tumours. Am J Surg Pathol 13:828–837

    Google Scholar 

  20. Capella C, Polak JM, Buffa R, Tapia FJ, Heitz PhU, Bloom SR, Solcia E (1983) Morphological patterns and diagnostic criteria of VIP-producing endocrine tumours. A histological histochemical, ultrastructural and biochemical study of 32 cases. Cancer 52:1860–1874

    Google Scholar 

  21. Capella C, Riva C, Rindi G, Sessa F, Usellini L, Chiaravalli A, Carnevali L, Solcia E (1991) Histopathology, hormone products, and clinicopathological profile of endocrine tumours of the upper small intestine: a study of 44 cases. Endocr Pathol 2:92–110

    Google Scholar 

  22. Carney JA, GO VLW, Fairbanks VF, Moore SB, Alport EC, Nora FE (1983) The syndrome of gastric argyrophil tumours and nonantral gastric atrophy. Ann Intern Med 99:761–766

    Google Scholar 

  23. Cassidy MA (1930) Abdominal carcinomatosis, with probable adrenal involvement. Proc R Soc Med 24:138–141

    Google Scholar 

  24. Chejfec G, Falkmer S, Askunsten U, Grimelius L, Gould VE (1988) Neuroendocrine tumours of the gastrointestinal tract. Pathol Res Pract 183:143–154

    Google Scholar 

  25. Chott A, Klöppel G, Buxbaum P, Heitz PhU (1987) Neuron specific enolase demonstration in the diagnosis of a solid-cystic (papillary cystic) tumour of the pancreas. Virchows Arch [A] 410:397–402

    Google Scholar 

  26. Corrin B, Gilby ED, Jones NF, Patrick J (1973) Oat cell carcinoma of the pancreas with ectopic ACTH secretion. Cancer 31:1523–1527

    Google Scholar 

  27. Cubilla AL, Hajdu SI (1975) Islet cell carcinoma of the pancreas. Arch Pathol 99:204–207

    Google Scholar 

  28. Danforth DN Jr, Gorden P, Brennan MF (1984) Metastatic insulin-secreting carcinoma of the pancreas. Clinical course and the role of surgery. Surgery 96:1027–1037

    Google Scholar 

  29. Dayal Y, Doos WG, O'Brien MJ, Nunnemacher G, DeLellis RA, Wolfe HJ (1983) Psammomatous somatostatinomas of the duodenum. Am J Surg Pathol 7:653–665

    Google Scholar 

  30. Dayal Y (1991) Endocrine Pathology of the Gut and Pancreas. CRC Press, Boca Raton Ann Arbor Boston

    Google Scholar 

  31. DeLellis RA, Dayal Y, Wolfe HJ (1984) Carcinoid tumours. Changing concepts and new perspectives. Am J Surg Pathol 8:295–300

    Google Scholar 

  32. DeLellis RA, Tischler AS (1990) The dispersed neuroendocrine cell system. In: Kovacs K, Asa S (eds) Functional endocrine pathology, chapter 18, vol 1. Blackwell, Boston, pp 493–508

    Google Scholar 

  33. Dische FE (1968) Argentaffin and non-argentaffin carcinoid tumours of the appendix. J Clin Pathol 21:60–66

    Google Scholar 

  34. Donow C, Baisch H, Heitz PhU, Klöppel G (1991) Nuclear DNA content in 27 pancreatic endocrine tumours: correlation with malignancy, survival and expression of glycoprotein hormone alpha chain. Virchows Arch [A] 419:463–468

    Google Scholar 

  35. Dookhan DB, Miettinen M, Finkel G, Gibas Z (1993) Recurrent duodenal gangliocytic paraganglioma with lymph node metastases. Histopathology 22:399–401

    Google Scholar 

  36. Ellison EH, Wilson SD (1964) The Zollinger-Ellison syndrome: reappraisal and evolution of 260 registered cases. Ann Surg 160:512–528

    Google Scholar 

  37. El-Naggar AK, Ballance W, Abdul Karim FW, Ordonez NG, McLemore D, Giacco GG, Batsakis JG (1991) Typical and atypical bronchopulmonary carcinoids. Am J Clin Pathol 95:828–834

    Google Scholar 

  38. Erspamer V, Asero B (1952) Identification of enteroamine, the specific hormone of the enterochromaffin cell system, as 5-hydroxytryptamine. Nature 169:800–801

    Google Scholar 

  39. Federspiel BH, Burke AP, Sobin LH, Shekitka KM (1990) Rectal and colonic carcinoids: a clinicopathologic study of 84 cases. Cancer 65:135–140

    Google Scholar 

  40. Fiocca R, Capella C, Buffa R, Fontana P, Solcia E, Hage E, Chance RE, Moody RL (1980) Glucagon, glicentin-and pancreatic polypeptide-like immunoreactivities in rectal carcinoids and related colorectal cells. Am J Pathol 100:81–92

    Google Scholar 

  41. Fiocca R, Rindi G, Capella C, Grimelius L, Polak JM, Yanaihara N, Solcia E (1987) Glucagon, glicentin, proglucagon, PYY, PP and pro-PP-icosapeptide immunoreactivities of rectal carcinoid tumours and related nontumour cells. Regul Rept 29:9–29

    Google Scholar 

  42. Fukayama M, Hayashi Y, Shiozawa Y, Okabe S, Kolke M (1989) Human chorionic gonadotropin alpha-subunit in rectal carcinoids. Am J Pathol 135:1065–1072

    Google Scholar 

  43. Glasser CM, Bhagavan BS (1980) Carcinoid tumours of the appendix. Arch Pathol Lab Med 104:272–275

    Google Scholar 

  44. Godwin JD (1975) Carcinoid tumours: an analysis of 2837 cases. Cancer 36:560–569

    Google Scholar 

  45. Gould VE, Chejfec G (1978) Neuroendocrine carcinomas of the colon. Am J Surg Pathol 2:31–38

    Google Scholar 

  46. Gould VE, Linnoila RI, Memoli VA, Warren WH (1983) Neuroendocrine cells and neuroendocrine neoplasms of the lung. Pathol Annu 18(II):287–330

    Google Scholar 

  47. Gould VER, Linnoila I, Memoli VA, Warren WH (1983) Neuroendocrine cells and neuroendocrine neoplasms of the lung. Lab Invest 49:519–539

    Google Scholar 

  48. Gould VE, Tomanova R, Monson R, Shen J, Gooch G, Warren WH (1994) Immunophenotypic subsets of large cell pulmonary carcinomas. Mod Pathol 7:150A879

    Google Scholar 

  49. Gronstad K, Grimelius L, Ekman R, Kewenter J, Ahlman H (1992) Disseminated rectal carcinoid tumour with production of immunoreactive motilin. Endocr Pathol 3:194–200

    Google Scholar 

  50. Guillausseau PJ, Guillausseau C, Villet R (1982) Les glucagonomes. Aspects cliniques, biologiques, anatomopathologiques et thérapeutiques (revue générale de 130 cases). Gastroenterol Clin Biol 6:1029–1041

    Google Scholar 

  51. Hajdu S, Winawer SJ, Myers WPL (1974) Carcinoid tumours. A study of 204 cases. Am J Clin Pathol 61:521–528

    Google Scholar 

  52. Hamid QA, Bishop AE, Rode J, Dhillon AP, Rosenberg BF, Reed RJ, Sibley RK, Polak JM (1986) Duodenal gangliocytic paragangliomas: A study of 10 cases with immunocytochemical neuroendocrine markers. Hum Pathol 17:1151–1157

    Google Scholar 

  53. Harvey RF, Bradshaw MJ, Davidson CM, Wilkinson SP, Davies PS (1985) Multifocal gastric carcinoid tumours, achlorhydria, and hypergastrinaemia. Lancet 951–954

  54. Hatzitheoklitos E, Büchler MW, Friess H, Poch B, Ebert M, Mohr W, Imaizumi T, Beger HG (1994) Carcinoid of the ampulla of Vater. Clinical characteristics and morphological features. Cancer 73:1580–1588

    Google Scholar 

  55. Heitz PhU, Polak JM, Timson CM, Pearse AGE (1976) Enterochromaffin cells as the endocrine source of gastrointestinal substance P. Histochemistry 49:343–347

    Google Scholar 

  56. Heitz PhU (1984) Pancreatic endocrine tumours. In: Klöppel G, Heitz PhU (eds) Pancreatic pathology. Churchill-Living-stone, Edinburgh, pp 206–232

    Google Scholar 

  57. Heitz PhU, Roth J, Zuber Chr, Komminoth P (1991) Markers for neural and endocrine cells in pathology. In: Gratzl M, Langley L (eds) Markers for neural and endocrine cells. VCH, Weinheim, pp 203–216

    Google Scholar 

  58. Iwafuchi M, Watanabe H, Ajioka Y, Shunoda T, Iwashida A, Ito S (1990) Immunohistochemical and ultrastructural studies of twelve argentaffin and six argyrophil carcinoids of the appendix vermiformis. Hum Pathol 21:773–780

    Google Scholar 

  59. Jetmore AB, Ray JE, Gathright JB jr, Mc-Mullen K, Hicks T, Timmcke AE (1992) Rectal carcinoids: the most frequent carcinoid tumour. Dis Colon Rectum 35:717–725

    Google Scholar 

  60. Kent RB, van Heerden JA, Weiland LH (1981) Nonfunctioning islet cell tumours. Ann Surg 193:185–190

    Google Scholar 

  61. Klöppel G, In't Veld P (1990) Neural and endocrine markers as diagnostic tools in pancreatic and gastrointestinal endocrine tumours. Acta Histochemica [Suppl]-Band XXXVIII: S. 93–98

    Google Scholar 

  62. Klöppel G, Höfler H, Heitz PhU (1993) Pancreatic endocrine tumours in man. In: Polak JM (ed): Diagnostic histopathology of neuroendocrine tumours, chapter 5. Churchill Livingstone, Edinburgh, pp 91–121

    Google Scholar 

  63. Komminoth P, Roth J, Lackie PM, Bitter-Suermann D, Heitz PhU (1991) Polysialic acid of the neural cell adhesion molecule distinguishes small cell lung carcinoma from carcinoids. Am J Pathol 139:297–304

    Google Scholar 

  64. Krisch K, Horvat G, Krisch I, Wengler G, Alibeik HH, Neuhold N, Ulrich W, Braun O, Hochmeister M (1988) Immunochemical characterization of a novel secretory protein (defined by monoclonal antibody HISL-19) of peptide hormone producing cells which is distinct from chromogranin A, B, and C. Lab Invest 58:411–420

    Google Scholar 

  65. Lasson A, Alwmark A, Nobin A, Sundler F (1983) Endocrine tumours of the duodenum. Clinical characteristics and hormone content. Ann Surg 197:393–398

    Google Scholar 

  66. Lembeck F (1953) 5-hydroxytryptamine in a carcinoid tumour. Nature 172:910–911

    Google Scholar 

  67. Liu TH, Tseng HC, Zhu Y, Zong SX, Chen Y, Cui QC (1985) Insulinoma. An Immunocytochemical and morphological anylsis of 95 cases. Cancer 56:1420–1429

    Google Scholar 

  68. Lloyd RV, Mervak T, Schmidt K, Warner TFCS, Wilson BS (1984) Immunohistochemical detection of chromogranin and neuron-specific enolase in pancreatic endocrine neoplasms. Am J Surg Pathol 8:607–614

    Google Scholar 

  69. Lohmann D, Pütz B, Reich U, Böhm J, Präuer H, Höfler H (1993) Mutational spectrum of the p53 gene in human small-cell lung cancer and relationship to clinicopathological data. Am J Pathol 142:907–915

    Google Scholar 

  70. Lundqvist M, Wilander E (1987) A study of the histopathogenesis of carcinoid tumours of the small intestine and appendix. Cancer 60:201–206

    Google Scholar 

  71. MacGillivray D, Heaton KB, Rushin JM; Cruess DF (1992) Distant metastases from a carcinoid tumour of the appendix less than one centimeter in size. Surgery 111:466–471

    Google Scholar 

  72. Märtensson H, Nobin A, Sundler F, Falkmer S (1985) Endocrine tumours of the ileum. Cytochemical and clinical aspects. Pathol Res Pract 180:356–363

    Google Scholar 

  73. Masson P (1928) Carcinoids (argentaffin-cell tumours) and nerve hyperplasia of the appendicular mucosa. Am J Pathol 4:181–211

    Google Scholar 

  74. Matsui K, Kitagawa M, Miwa A, Kuroda Y, Tsuji M (1991) Small cell carcinoma of the stomach: a clinicopathologic study of 17 cases. Am J Gastroenterol 86:1167–1175

    Google Scholar 

  75. Mills SE, Allen MS Jr, Cohen AR (1983) Small cell undifferentiated carcinoma of the colon. Am J Surg Pathol 7:643–651

    Google Scholar 

  76. Mizuma K, Shibuya H, Totsuka M, Hayasaka H (1983) Carcinoid of the stomach: a case report and review of 100 cases reported in Japan. Ann Chir Gynaecol 72:23–27

    Google Scholar 

  77. Moertel CG, Sauer G, Dockerty MB, Baggenstoss AH (1961) Life history of the carcinoid tumour of the small intestine. Cancer 14:901–912

    Google Scholar 

  78. Moertel CG, Dockerty MB, Judd ES (1968) Carcinoid tumour of the vermiform appendix. Cancer 21:270–278

    Google Scholar 

  79. Moertel CG, Weiland LH, Nagorney DM, Dockerty MB (1987) Carcinoid tumours of the appendix: treatment and prognosis. N Engl J Med 317:1699–1701

    Google Scholar 

  80. Morgan JG, Marks C, Heam D (1974) Carcinoid tumours of the gastrointestinal tract. Ann Surg 180:720–727

    Google Scholar 

  81. Moyana TN, Satkunam N (1993) Crypt cell proliferative micronests in rectal carcinoids. An immunohistochemical study. Am J Surg Pathol 17:350–356

    Google Scholar 

  82. Nauck M, Creutzfeldt W (1991) Insulin producing tumours and the insulinoma syndrome. In: Dayal Y (ed) Endocrine pathology of the gut and pancreas. CRC Press, Boca Raton, pp 195–226

    Google Scholar 

  83. Naunheim KS, Zeitels J, Kaplan EL, Sugimoto J, Shen KL, Lee GH, Straus FH (1983) Rectal carcinoid tumours. Treatment and prognosis Surgery 94:670–676

    Google Scholar 

  84. Nemeth J, Galian A, Mikol J, Cochand-Priollet B, Wassef M, Lavergne A (1987) Neuron-specific enolase and malignant lymphomas (23 cases). Virchows Arch [A] 412:89–93

    Google Scholar 

  85. Oberndorfer S (1907) Karzinoide Tumoren des Dünndarms. Frankf Z Path 1:426–432

    Google Scholar 

  86. O'Briain DS, Tischler AS, Dayal Y, Bendon R, De Lellis RA, Wolfe HJ (1982) Rectal carcinoids as tumours of the hindgut endocrine cells: a morphological and immunohistochemical analysis. Am J Surg Pathol 6:131–142

    Google Scholar 

  87. O'Connor TP, Wade TP, Sunwoo YC, Raimers HJ, Palmer DC, Silverberg AB, Johnson FE (1992) Small cell undifferentiated carcinoma of the pancreas. Report of a patient with tumour marker studies. Cancer 70:1514–1519

    Google Scholar 

  88. Orloff MY (1971) Carcinoid tumours of the rectum. Cancer 28:175–180

    Google Scholar 

  89. Papadaki L, Rode J, Dhillon AP, Dische FE (1983) Fine structure of a neuroendocrine complex of the mucosa of the appendix. Gastroenterology 84:490–497

    Google Scholar 

  90. Pelosi G, Zamboni G, Doglioni C, Rodella S, Bresaola E, Iacono C, Serio G, Iannucci A, Scarpa A (1992) Immunodetection of proliferating cell nuclear antigen assesses the growth fraction and predicts malignancy in endocrine tumours of the pancreas. Am J Surg Pathol 116:1215–1125

    Google Scholar 

  91. Peskin GW, Orloff MJ (1959) A clinical study of 25 patients with carcinoid tumours of the rectum. Surg Gynec Obstet 109:673–681

    Google Scholar 

  92. Pipeleers-Marichal M, Somers G, Willems G, Foulis A, Imrie C, Bishop AE, Polak JM Häcki WH, Stamm B, Heitz PU, Klöppel G (1990) Gastrinomas in the duodenums of patients with multiple endocrine neoplasia type 1 and the Zollinger-Ellison syndrome. N Engl J Med 322:723–727

    Google Scholar 

  93. Pipeleers-Marichal M, Donow C, Heitz PhU, Klöppel G (1993) Pathologic aspects of gastrinomas in patients with Zollinger-Ellison syndrome with and without multiple endocrine neoplasia type 1. World J Surg 17:481–488

    Google Scholar 

  94. Polak JM (1993) Diagnostic Histopathology of Neuroendocrine Tumours. Churchill Livingstone, Edinburgh

    Google Scholar 

  95. Reyes CV, Wang T (1981) Undifferentiated small cell carcinoma of the pancreas: a report of five cases. Cancer 47:2500–2502

    Google Scholar 

  96. Ricci JL (1993) Carcinoid of the ampulla of Vater. Local resection or pancreaticoduodenectomy. Cancer 71:686–690

    Google Scholar 

  97. Rindi G, Buffa R, Sessa F, Tortora O, Solcia E (1986) Chromogranin A, B and C immunoreactivities of mammalian endocrine cells. Histochemistry 85:19–28

    Google Scholar 

  98. Rindi G, Luinetti O, Cornaggia M, Capella C, Solcia E (1993) Three subtypes of gastric argyrophil carcinoid and the gastric neuroendocrine carcinoma: a clinicopthologic study. Gastroenterology 104:994–1006

    CAS  PubMed  Google Scholar 

  99. Rode J, Dhillon AP, Doran JF, Jackson P, Thompson RJ (1985) PGP9.5, a new marker for human neuroendocrine tumours. Histopathology 9:147–158

    Google Scholar 

  100. Rüschoff J, Willemer S, Brunzel M, Trautmann ME, Frank M, Arnold R, Klöppel G (1993) Nucleolar organizer regions and glycoprotein-hormone alpha-chain reaction as markers of malignancy in endocrine tumours of the pancreas. Histopathology 22:51–57

    Google Scholar 

  101. Ruttmann E, Klöppel G, Bommer G, Kiehn M, Heitz PhU (1980) Pancreatic glucagonomas with and without syndrome. Virchows Arch [A] 388:51–67

    Google Scholar 

  102. Saarsfield P, Anthony PP (1990) Small cell undifferentiated (neuroendocrine) carcinoma of the colon. Histopathology 16:357–363

    Google Scholar 

  103. Sanchez-Sosa S, Angeles A, Orozco H, Larriva-Sahd J (1991) Neuroendocrine carcinoma of the ampulla of Vater. A case of absence of somatostatin in a vasoactive intestinal polypeptide-, bombesin-, and cholecystokinin-producing tumour. Am J Clin Pathol 95:51–54

    Google Scholar 

  104. Solcia E, Bordi C, Creutzfeldt W, Dayal Y, Dayan AD, Falkmer S, Grimelius C, Havu N (1988) Histological classification of nonantral gastric endocrine growths in man. Digestion 41:185–200

    CAS  PubMed  Google Scholar 

  105. Solcia E, Capella C, Fiocca R, Rindi G, Rosai J (1990) Gastric argyrophil carcinoidosis in patients with Zollinger-Ellison syndrome due to type 1 multiple endocrine neoplasia. A newly recognized association. Am J Surg Pathol 14:503–513

    Google Scholar 

  106. Solcia E, Sessa F, Rindi G, Bonato M, Capella C (1991) Pancreatic endocrine tumours: nonfunctioning tumours and tumours with uncommon function. In: Dayal Y (ed) Endocrine pathology of the gut and pancreas. CRC Pres, Boca Raton, pp 105–132

    Google Scholar 

  107. Solcia E, Rindi G, Fiocca R, Villani L, Buffa R, Ambrosiani L, Capella C (1992) Distinct patterns of chronic gastritis associated with carcinoid and cancer and their role in tumourigenesis. Yale J Biol Med 65:793–804

    Google Scholar 

  108. Solcia E, Rindi G, Sessa F, Fiocca R, Luinetti O, Bosi F (1993) Endocrine tumours of the gastrointestinal tract. In: Polak JM (ed) Diagnostic Histopathology of Neuroendocrine Tumours., chapter 6. Churchill Livingstone, Edinburgh, pp 123–149

    Google Scholar 

  109. Solcia E, Fiocca R, Rindi G, Villani L, Cornaggia M, Capella C (1993) The pathology of the gastrointestinal endocrine system. In: Vinik AL (ed) Gastrointestinal hormones in medicine. Endocrinol Metab Clin North Am, vol 22, pp 795–821

    Google Scholar 

  110. Spencer H (1955) Pancreatic islet-cell adenomata. J Pathol Bacteriol 69:259

    Google Scholar 

  111. Stamm B, Hacki WH, Klöppel G, Heitz PU (1991) Gastrin-producing tumours and the Zollinger-Ellison syndrome. In: Dayal Y (ed) Endocrine pathology of the gut and pancreas. CRC Press, Boca Raton, pp 155–194

    Google Scholar 

  112. Stefanini P, Carboni M, Patrassi N (1974) Beta islet cell tumours of the pancreas: results of a statistical study on 1067 cases collected. Surgery 75:597–609

    Google Scholar 

  113. Stephens M, Williams GT, Jasani B, Williams ED (1987) Synchronous duodenal neuroendocrine tumours in von Recklinghausen's disease — a case report of co-existing gangliocytic paraganglioma and somatostatin-rich glandular carcinoid. Histopathology 11:1331–1340

    Google Scholar 

  114. Stolte M, Ebert D, Seifert E, Schulte F, Rode J (1988) Zur Prognose der Karzinoidtumoren des Magens. Leber Magen Darm 5:246–256

    Google Scholar 

  115. Suzuki H, Ghatei MA, Williams SJ (1986) Production of pituitary protein 7B2 immunoreactivity by endocrine tumours and its possible diagnostic value. J Clin Endocrinol Metab 63:758–765

    Google Scholar 

  116. Syracuse DC, Perzin KH, Price JB, Weidel PD, Mesa-Tejada R (1979) Carcinoid tumours of the appendix. Mesoappendiceal extension and nodal metastases. Ann Surg 190:58–63

    Google Scholar 

  117. Tapia FJ, Barbosa AJA, Marangos PJ, Polak JM, Bloom SR, Dermody C (1981) Neuron-specific enolase is produced by neuroendocrine tumours. Lancet ii:808–811

    Google Scholar 

  118. Thirlby RC, Kasper CS, Jones RC (1984) Metastatic carcinoid tumour of the appendix: report of a case and review of the literature. Dis Colon Rectum 27:42–46

    Google Scholar 

  119. Thompson RJ, Doran JF, Jackson P, Dhillon AP, Rode J (1983) PGP9.5 — a new marker for vertebrate neurons and neuroendocrine cells. Brain Res 278:224–228

    Google Scholar 

  120. Thompson GB, van Heerden HA, Martin JK, Schutt AJ, Ilstrup DM, Carney JA (1985) Carcinoid tumours of the gastrointestinal tract: presentation, management, and prognosis. Surgery: 1054–1063

  121. Tischler AS, Mobtaker H, Mann K, Nunnemacher G, Jason WJ, Dayal Y, DeLellis RA, Adelman L, Wolfe HJ (1986) Anti-Lymphocyte antibody Leu-7 (HNK-1) recognizes a constituent of neuroendocrine granule matrix. J Histochem Cytochem 34:1213–1216

    Google Scholar 

  122. Travis WD, Linnoila I, Tsokos MG, Hitchcock C, Cutler GB, Nieman L, Chrousos G, Pass H, Doppman J (1991) Neuroendocrine tumours of the lung with proposed criteria for large-cell neuroendocrine carcinoma. Am J Surg Pathol 15:529–553

    Google Scholar 

  123. Tsioulias G, Muto T, Kubota Y, Masaki T, Suzuki K, Akasu T, Morioka Y (1991) DNA ploidy pattern in rectal carcinoid tumours. Dis Colon Rectum 34:31–36

    Google Scholar 

  124. Vinores SA, Bonnin JM, Rubinstein LJ, Marangos PJ (1984) Immunohistochemical demonstration of neuron-specific enolase in neoplasms of the CNS and other tissues. Arch Pathol Lab Med 108:536–540

    Google Scholar 

  125. Weiler R, Fischer-Colbrie R, Schmid KW, Feichtinger H, Bussolati G, Grimelius L, Krisch K, Kerl H, O'Connor D, Winkler H (1988) Immunological studies on the occurrence and properties of chromogranin A and B and secretogranin II in endocrine tumours. Am J Surg Pathol 12:877–884

    Google Scholar 

  126. Wick M, Weatherby RP, Weiland LH (1987) Small cell neuroendocrine carcinoma of the colon and rectum. Hum Pathol 18:9–21

    Google Scholar 

  127. Wiedenmann B, Franke WW, Kuhn C, Moll R, Gould VE (1986) Synaptophysin: a marker protein for neuroendocrine cells and neoplasms. Proc Natl Acad Sci USA 83:3500–3504

    Google Scholar 

  128. Wiedenmann B, Huttner W (1989) Synaptophysin and chromogranins/secretogranins-widespread constituents of distinct types of neuroendocrine vesicles and new tools in tumour diagnosis. Virchows Arch [B] 58:95–121

    Google Scholar 

  129. Wilander E, El-Salhy M, Pitkanen P (1984) Histopathology of gastric carcinoids: a survey of 42 cases. Histopathology 8:182–193

    Google Scholar 

  130. Williams ED, Sandler M (1963) The Classification of carcinoid tumours. Lancet 1:238–239

    Google Scholar 

  131. Yang K, Ulich T, Cheng L, Lewin KJ (1983) The neuroendocrine products of intestinal carcinoids: an immunoperoxidase study of 35 carcinoid tumours. Cancer 51:1018–1026

    Google Scholar 

  132. Yoshida A, Yano M, Yutaka F, Sano C, Mori H, Yoshida H, Fukunushi H (1981) Argentaffin carcinoid tumour of the rectum. Cancer 48:2103–2106

    Google Scholar 

  133. Zamboni G, Franzin G, Bonetti F, Scarpa A, Chilosi M, Colombari R, Menestrina F, Pea M, Iacono C, Serio G, Fiore-Donati L (1990) Small-cell neuroendocrine carcinoma of the ampullary region. A clinicopathologic, immunohistochemical, and ultrastructural study of three cases. Am J Surg Pathol 14:703–713

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology, University of Pavia at Varese, Italy

    C. Capella

  2. Department of Pathology, University of Zürich, Zürich, Switzerland

    P. U. Heitz

  3. Department of Pathology, Technical University of Munich, Munich, Germany

    H. Höfler

  4. Department of Pathology, University of Pavia, Pavia, Italy

    E. Solcia

  5. Department of Pathology, Academic Hospital Jette, Free University of Brussels, Laarbeeklaan 101, B-1090, Brussels, Belgium

    G. Klöppel

Authors
  1. C. Capella
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. U. Heitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Höfler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Solcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Klöppel
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

A modified version of this article will appear in Digestion with permission of Karger publishers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Capella, C., Heitz, P.U., Höfler, H. et al. Revised classification of neuroendocrine tumours of the lung, pancreas and gut. Vichows Archiv A Pathol Anat 425, 547–560 (1995). https://doi.org/10.1007/BF00199342

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00199342

Key words

Search

Navigation