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. 1992 Nov-Dec;65(6):793–829.

Distinct patterns of chronic gastritis associated with carcinoid and cancer and their role in tumorigenesis.

E Solcia 1, G Rindi 1, R Fiocca 1, L Villani 1, R Buffa 1, L Ambrosiani 1, C Capella 1
PMCID: PMC2589778  PMID: 1341079

Abstract

A series of 60 gastric endocrine tumors comprised 44 body-fundus argyrophil carcinoids, of which 23 arose in a background of hypergastrinemia and type A chronic atrophic gastritis (A-CAG), mainly with histologic patterns suggestive of an autoimmune process. Only 22 percent (compared with 19 percent of 58 tumor-free A-CAG cases) of 36 carcinoids and 21 percent of 19 A-CAG carcinoids investigated had Helicobacter pylori (HP) colonization, against 50 percent of 14 CAG-associated neuroendocrine carcinomas or mixed endocrine-exocrine tumors, 84 percent of 150 cases with early gastric cancer (p < 0.001 versus carcinoids), mostly with B- or AB-type CAG, 76 percent of 97 tumor-free AB-CAG, and 95 percent of 151 tumor-free B-CAG cases. Secondary hypergastrinemia and local mechanisms activated by chronic autoimmune gastritis are among factors involved in the pathogenesis of relatively indolent CAG-associated carcinoids, whereas active HP gastritis in cooperation with environmental carcinogens may likely cause more severe epithelial transformation, leading to ordinary cancer and, possibly, to neuroendocrine carcinomas or mixed endocrine-exocrine tumors.

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Selected References

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  1. Borch K. Epidemiologic, clinicopathologic, and economic aspects of gastroscopic screening of patients with pernicious anemia. Scand J Gastroenterol. 1986 Jan;21(1):21–30. doi: 10.3109/00365528609034616. [DOI] [PubMed] [Google Scholar]
  2. Borch K., Renvall H., Liedberg G. Gastric endocrine cell hyperplasia and carcinoid tumors in pernicious anemia. Gastroenterology. 1985 Mar;88(3):638–648. doi: 10.1016/0016-5085(85)90131-3. [DOI] [PubMed] [Google Scholar]
  3. Bordi C., Yu J. Y., Baggi M. T., Davoli C., Pilato F. P., Baruzzi G., Gardini G., Zamboni G., Franzin G., Papotti M. Gastric carcinoids and their precursor lesions. A histologic and immunohistochemical study of 23 cases. Cancer. 1991 Feb 1;67(3):663–672. doi: 10.1002/1097-0142(19910201)67:3<663::aid-cncr2820670323>3.0.co;2-l. [DOI] [PubMed] [Google Scholar]
  4. Capella C., Frigerio B., Cornaggia M., Solcia E., Pinzon-Trujillo Y., Chejfec G. Gastric parietal cell carcinoma--a newly recognized entity: light microscopic and ultrastructural features. Histopathology. 1984 Sep;8(5):813–824. doi: 10.1111/j.1365-2559.1984.tb02397.x. [DOI] [PubMed] [Google Scholar]
  5. Carney J. A., Go V. L., Fairbanks V. F., Moore S. B., Alport E. C., Nora F. E. The syndrome of gastric argyrophil carcinoid tumors and nonantral gastric atrophy. Ann Intern Med. 1983 Dec;99(6):761–766. doi: 10.7326/0003-4819-99-6-761. [DOI] [PubMed] [Google Scholar]
  6. Caruso M. L., Pilato F. P., D'Adda T., Baggi M. T., Fucci L., Valentini A. M., Lacatena M., Bordi C. Composite carcinoid-adenocarcinoma of the stomach associated with multiple gastric carcinoids and nonantral gastric atrophy. Cancer. 1989 Oct 1;64(7):1534–1539. doi: 10.1002/1097-0142(19891001)64:7<1534::aid-cncr2820640730>3.0.co;2-h. [DOI] [PubMed] [Google Scholar]
  7. Cornaggia M., Capella C., Riva C., Finzi G., Solcia E. Electron immunocytochemical localization of pepsinogen I (PgI) in chief cells, mucous-neck cells and transitional mucous-neck/chief cells of the human fundic mucosa. Histochemistry. 1986;85(1):5–11. doi: 10.1007/BF00508647. [DOI] [PubMed] [Google Scholar]
  8. Correa P., Sasano N., Stemmermann G. N., Haenszel W. Pathology of gastric carcinoma in Japanese populations: comparisons between Miyagi prefecture, Japan, and Hawaii. J Natl Cancer Inst. 1973 Nov;51(5):1449–1459. doi: 10.1093/jnci/51.5.1449. [DOI] [PubMed] [Google Scholar]
  9. Creutzfeldt W., Lamberts R. Is hypergastrinaemia dangerous to man? Scand J Gastroenterol Suppl. 1991;180:179–191. doi: 10.3109/00365529109093198. [DOI] [PubMed] [Google Scholar]
  10. De Aizpurua H. J., Cosgrove L. J., Ungar B., Toh B. H. Autoantibodies cytotoxic to gastric parietal cells in serum of patients with pernicious anemia. N Engl J Med. 1983 Sep 15;309(11):625–629. doi: 10.1056/NEJM198309153091102. [DOI] [PubMed] [Google Scholar]
  11. Deveney C. W., Freeman H., Way L. W. Experimental gastric carcinogenesis in the rat: effects of hypergastrinemia and acid secretion. Am J Surg. 1980 Jan;139(1):49–54. doi: 10.1016/0002-9610(80)90229-9. [DOI] [PubMed] [Google Scholar]
  12. Fiocca R., Cornaggia M., Villani L., Capella C., Solcia E., Samloff I. M. Expression of pepsinogen II in gastric cancer. Its relationship to local invasion and lymph node metastases. Cancer. 1988 Mar 1;61(5):956–962. doi: 10.1002/1097-0142(19880301)61:5<956::aid-cncr2820610517>3.0.co;2-c. [DOI] [PubMed] [Google Scholar]
  13. Fiocca R., Villani L., Tenti P., Cornaggia M., Finzi G., Capella C., Prat M., Bussolati G., Solcia E. Widespread expression of intestinal markers in gastric carcinoma: a light and electron microscopic study using BD-5 monoclonal antibody. J Clin Pathol. 1988 Feb;41(2):178–187. doi: 10.1136/jcp.41.2.178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fiocca R., Villani L., Tenti P., Cornaggia M., Finzi G., Riva C., Capella C., Bara J., Samloff I. M., Solcia E. The foveolar cell component of gastric cancer. Hum Pathol. 1990 Mar;21(3):260–270. doi: 10.1016/0046-8177(90)90225-t. [DOI] [PubMed] [Google Scholar]
  15. Forman D., Sitas F., Newell D. G., Stacey A. R., Boreham J., Peto R., Campbell T. C., Li J., Chen J. Geographic association of Helicobacter pylori antibody prevalence and gastric cancer mortality in rural China. Int J Cancer. 1990 Oct 15;46(4):608–611. doi: 10.1002/ijc.2910460410. [DOI] [PubMed] [Google Scholar]
  16. Furihata C., Tatematsu M., Miki K., Katsuyama T., Sudo K., Miyagi N., Kubota T., Jin S. S., Kodama K., Ito N. Gastric- and intestinal-type properties of human gastric cancers transplanted into nude mice. Cancer Res. 1984 Feb;44(2):727–733. [PubMed] [Google Scholar]
  17. Grigioni W. F., Caletti G. C., Gabrielli M., Marrano D., Villanacci V., Mancini A. Gastric carcinoids of ECL cells. Pathological and clinical analysis of eight cases. Acta Pathol Jpn. 1985 Mar;35(2):361–375. [PubMed] [Google Scholar]
  18. Ihamäki T., Kekki M., Sipponen P., Siurala M. The sequelae and course of chronic gastritis during a 30- to 34-year bioptic follow-up study. Scand J Gastroenterol. 1985 May;20(4):485–491. doi: 10.3109/00365528509089685. [DOI] [PubMed] [Google Scholar]
  19. Ihamäki T., Sipponen P., Varis K., Kekki M., Siurala M. Characteristics of gastric mucosa which precede occurrence of gastric malignancy: results of long-term follow-up of three family samples. Scand J Gastroenterol Suppl. 1991;186:16–23. doi: 10.3109/00365529109103982. [DOI] [PubMed] [Google Scholar]
  20. Karnes W. E., Jr, Samloff I. M., Siurala M., Kekki M., Sipponen P., Kim S. W., Walsh J. H. Positive serum antibody and negative tissue staining for Helicobacter pylori in subjects with atrophic body gastritis. Gastroenterology. 1991 Jul;101(1):167–174. doi: 10.1016/0016-5085(91)90474-y. [DOI] [PubMed] [Google Scholar]
  21. Loveridge N., Bitensky L., Chayen J., Hausamen T. U., Fisher J. M., Taylor K. B., Gardner J. D., Bottazzo G. F., Doniach D. Inhibition of parietal cell function by human gammaglobulin containing gastric parietal cell antibodies. Clin Exp Immunol. 1980 Aug;41(2):264–270. [PMC free article] [PubMed] [Google Scholar]
  22. Matsui K., Kitagawa M., Miwa A., Kuroda Y., Tsuji M. Small cell carcinoma of the stomach: a clinicopathologic study of 17 cases. Am J Gastroenterol. 1991 Sep;86(9):1167–1175. [PubMed] [Google Scholar]
  23. Mattsson H., Havu N., Bräutigam J., Carlsson K., Lundell L., Carlsson E. Partial gastric corpectomy results in hypergastrinemia and development of gastric enterochromaffinlike-cell carcinoids in the rat. Gastroenterology. 1991 Feb;100(2):311–319. doi: 10.1016/0016-5085(91)90197-s. [DOI] [PubMed] [Google Scholar]
  24. Morris D. L., Watson S. A., Durrant L. G., Harrison J. D. Hormonal control of gastric and colorectal cancer in man. Gut. 1989 Apr;30(4):425–429. doi: 10.1136/gut.30.4.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nomura A., Stemmermann G. N., Chyou P. H., Kato I., Perez-Perez G. I., Blaser M. J. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med. 1991 Oct 17;325(16):1132–1136. doi: 10.1056/NEJM199110173251604. [DOI] [PubMed] [Google Scholar]
  26. Nylander O., Berglindh T., Obrink K. J. Prostaglandin interaction with histamine release and parietal cell activity in isolated gastric glands. Am J Physiol. 1986 May;250(5 Pt 1):G607–G616. doi: 10.1152/ajpgi.1986.250.5.G607. [DOI] [PubMed] [Google Scholar]
  27. Ohgaki H., Tomihari M., Sato S., Kleihues P., Sugimura T. Differential proliferative response of gastric mucosa during carcinogenesis induced by N-methyl-N'-nitro-N-nitrosoguanidine in susceptible ACI rats, resistant Buffalo rats, and their hybrid F1 cross. Cancer Res. 1988 Sep 15;48(18):5275–5279. [PubMed] [Google Scholar]
  28. Parsonnet J., Friedman G. D., Vandersteen D. P., Chang Y., Vogelman J. H., Orentreich N., Sibley R. K. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991 Oct 17;325(16):1127–1131. doi: 10.1056/NEJM199110173251603. [DOI] [PubMed] [Google Scholar]
  29. Parsonnet J., Vandersteen D., Goates J., Sibley R. K., Pritikin J., Chang Y. Helicobacter pylori infection in intestinal- and diffuse-type gastric adenocarcinomas. J Natl Cancer Inst. 1991 May 1;83(9):640–643. doi: 10.1093/jnci/83.9.640. [DOI] [PubMed] [Google Scholar]
  30. Reinhart W. H., Müller O., Halter F. Influence of long-term 16,16-dimethyl prostaglandin E2 treatment on the rat gastrointestinal mucosa. Gastroenterology. 1983 Nov;85(5):1003–1010. [PubMed] [Google Scholar]
  31. Sipponen P., Kekki M., Siurala M. Atrophic chronic gastritis and intestinal metaplasia in gastric carcinoma. Comparison with a representative population sample. Cancer. 1983 Sep 15;52(6):1062–1068. doi: 10.1002/1097-0142(19830915)52:6<1062::aid-cncr2820520622>3.0.co;2-p. [DOI] [PubMed] [Google Scholar]
  32. Sjöblom S. M., Sipponen P., Karonen S. L., Järvinen H. J. Mucosal argyrophil endocrine cells in pernicious anaemia and upper gastrointestinal carcinoid tumours. J Clin Pathol. 1989 Apr;42(4):371–377. doi: 10.1136/jcp.42.4.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sjövall M., Lindstedt G., Olbe L., Lundell L. Effect of parietal cell vagotomy and cholinergic blockade on gastrin release in man induced by gastrin-releasing peptide. Digestion. 1990;46(2):114–120. doi: 10.1159/000200340. [DOI] [PubMed] [Google Scholar]
  34. Solcia E., Bordi C., Creutzfeldt W., Dayal Y., Dayan A. D., Falkmer S., Grimelius L., Havu N. Histopathological classification of nonantral gastric endocrine growths in man. Digestion. 1988;41(4):185–200. doi: 10.1159/000199786. [DOI] [PubMed] [Google Scholar]
  35. Solcia E., Capella C., Fiocca R., Rindi G., Rosai J. Gastric argyrophil carcinoidosis in patients with Zollinger-Ellison syndrome due to type 1 multiple endocrine neoplasia. A newly recognized association. Am J Surg Pathol. 1990 Jun;14(6):503–513. doi: 10.1097/00000478-199006000-00001. [DOI] [PubMed] [Google Scholar]
  36. Solcia E., Capella C., Sessa F., Rindi G., Cornaggia M., Riva C., Villani L. Gastric carcinoids and related endocrine growths. Digestion. 1986;35 (Suppl 1):3–22. doi: 10.1159/000199378. [DOI] [PubMed] [Google Scholar]
  37. Tielemans Y., Håkanson R., Sundler F., Willems G. Proliferation of enterochromaffinlike cells in omeprazole-treated hypergastrinemic rats. Gastroenterology. 1989 Mar;96(3):723–729. [PubMed] [Google Scholar]

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