Gastric cancer and gastrin: on the interaction of Helicobacter pylori gastritis and acid inhibitory induced hypergastrinemia

References

• Karimi P, Islami F, Anandasabapathy S, et al. Gastric cancer: descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidem Biomar. 2014;23(5):700–713.
   PubMed Web of Science ®Google Scholar
• Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA. 2011;61(2):69–90.
   Google Scholar
• Anderson WF, Rabkin CS, Turner N, et al. The changing face of noncardia gastric cancer incidence among US Non-hispanic whites. J Natl Cancer I. 2018;110(6):608–615.
   PubMedGoogle Scholar
• Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet. 1984;1(8390):1311–1315.
   PubMed Web of Science ®Google Scholar
• Parsonnet J, Friedman GD, Vandersteen DP, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991;325(16):1127–1131.
   PubMed Web of Science ®Google Scholar
• Cheung KS, Chan EW, Wong AYS, et al. Long-term proton pump inhibitors and risk of gastric cancer development after treatment for Helicobacter pylori: a population-based study. Gut. 2018;67(1):28–35.
   PubMed Web of Science ®Google Scholar
• Waldum HL, Hauso O, Sordal OF, et al. Gastrin may mediate the carcinogenic effect of helicobacter pylori infection of the stomach. Dig Dis Sci. 2015;60(6):1522–1527.
   PubMed Web of Science ®Google Scholar
• Waldum HL, Sagatun L, Mjones P. Gastrin and Gastric Cancer. Front Endocrinol (Lausanne). 2017;8:1. DOI:10.3389/fendo.2017.00001
   PubMed Web of Science ®Google Scholar
• Morson BC. Intestinal metaplasia of the gastric mucosa. Br J Cancer. 1955;9(3):365–376.
   PubMed Web of Science ®Google Scholar
• Siurala M, Seppala K. Atrophic gastritis as a possible precursor of gastric carcinoma and pernicious anemia. Results of follow-up examinations. Acta Med Scand. 1960;166:455–474.
   PubMedGoogle Scholar
• Grossman MI, Kirsner JB, Gillespie IE. Basal and histalog-stimulated gastric secretion in control subjects and in patients with peptic ulcer or gastric cancer. Gastroenterology. 1963;45:14–26.
   PubMed Web of Science ®Google Scholar
• McGuigan JE, Trudeau WL. Serum and tissue gastrin concentrations in patients with carcinoma of the stomach. Gastroenterology. 1973;64(1):22–25.
   PubMed Web of Science ®Google Scholar
• Correa P. Human gastric carcinogenesis: a multistep and multifactorial process-First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res. 1992;52(24):6735–6740.
   PubMed Web of Science ®Google Scholar
• Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345(11):784–789.
   PubMed Web of Science ®Google Scholar
• El-Zimaity HM. Gastric atrophy, diagnosing and staging. World J Gastroentero. 2006;12(36):5757–5762.
   PubMed Web of Science ®Google Scholar
• Fossmark R, Sagatun L, Nordrum IS, et al. Hypergastrinemia is associated with adenocarcinomas in the gastric corpus and shorter patient survival. APMIS. 2015;123(6):509–514.
   PubMed Web of Science ®Google Scholar
• Venerito M, Varbanova M, Rohl FW, et al. Oxyntic gastric atrophy in Helicobacter pylori gastritis is distinct from autoimmune gastritis. J Clin Pathol. 2016;69(8):677–685.
   PubMed Web of Science ®Google Scholar
• Zamcheck N, Grable E, Ley A, et al. Occurrence of gastric cancer among patients with pernicious anemia at the Boston City Hospital. N Engl J Med. 1955;252(26):1103–1110.
   PubMed Web of Science ®Google Scholar
• Elsborg L, Mosbech J. Pernicious anaemia as a risk factor in gastric cancer. Acta Med Scand. 1979;206(4):315–318.
   PubMedGoogle Scholar
• Vannella L, Lahner E, Osborn J, et al. Systematic review: gastric cancer incidence in pernicious anaemia. Aliment Pharm Ther. 2013;37(4):375–382.
   PubMed Web of Science ®Google Scholar
• Graham DY, Zou WY. Guilt by association: intestinal metaplasia does not progress to gastric cancer. Curr Opin Gastroenterol. 2018;34(6):458–464.
   PubMed Web of Science ®Google Scholar
• Annibale B, Lahner E, Bordi C, et al. Role of Helicobacter pylori infection in pernicious anaemia. Digest Liver Dis. 2000;32(9):756–762.
   Web of Science ®Google Scholar
• Villanacci V, Casella G, Lanzarotto F, et al. Autoimmune gastritis: relationships with anemia and Helicobacter pylori status. Scand J Gastroentero. 2017;52(6–7):674–677.
   PubMed Web of Science ®Google Scholar
• Moreira-Silva H, Silva G, Costa E, et al. Insights into pediatric autoimmune gastritis: is there a role for helicobacter pylori infection? J Pediatr Gastr Nutr. 2019;68(6):e99–e104.
   PubMed Web of Science ®Google Scholar
• Havu N. Enterochromaffin-like cell carcinoids of gastric mucosa in rats after life-long inhibition of gastric secretion. Digestion. 1986;35(Suppl 1):42–55.
   PubMed Web of Science ®Google Scholar
• Poynter D, Selway SA, Papworth SA, et al. Changes in the gastric mucosa of the mouse associated with long lasting unsurmountable histamine H2 blockade. Gut. 1986;27(11):1338–1346.
   PubMed Web of Science ®Google Scholar
• Martinsen TC, Kawase S, Hakanson R, et al. Spontaneous ECL cell carcinomas in cotton rats: natural course and prevention by a gastrin receptor antagonist. Carcinogenesis. 2003;24(12):1887–1896.
   PubMed Web of Science ®Google Scholar
• Freston JW. Clinical significance of hypergastrinaemia: relevance to gastrin monitoring during omeprazole therapy. Digestion. 1992;51(Suppl 1):102–114.
   PubMed Web of Science ®Google Scholar
• Murphy G, Abnet CC, Choo-Wosoba H, et al. Serum gastrin and cholecystokinin are associated with subsequent development of gastric cancer in a prospective cohort of Finnish smokers. Int J Epidemiol. 2017;46(3):914–923.
   PubMed Web of Science ®Google Scholar
• Bordi C, D’Adda T, Pilato FP, et al. Carcinoid (ECL cell) tumor of the oxyntic mucosa of the stomach: a hormone-dependent neoplasm?. In: Fenoglio-Preiser CM, Wolff M, Rilke F, editors. Progress in Surgical Pathology. Berlin (Heidelberg): Springer; 1988. p. 177–195.
   Google Scholar
• Lauren P. The two histological main types of gastric carcinoma: Diffuse and so-called intestinal-type carcinoma. An attemt at a histo-clinical classification. Acta Pathol Mic Sc. 1965;64:31–49.
   PubMedGoogle Scholar
• Qvigstad G, Sandvik AK, Brenna E, et al. Detection of chromogranin A in human gastric adenocarcinomas using a sensitive immunohistochemical technique. Histochem J. 2000;32(9):551–556.
   PubMedGoogle Scholar
• Sordal O, Qvigstad G, Nordrum IS, et al. In situ hybridization in human and rodent tissue by the use of a new and simplified method. Appl Immunohistochem M M. 2013;21(2):185–189.
   Web of Science ®Google Scholar
• Waldum HL, Aase S, Kvetnoi I, et al. Neuroendocrine differentiation in human gastric carcinoma. Cancer. 1998;83(3):435–444.
   PubMed Web of Science ®Google Scholar
• Qvigstad G, Falkmer S, Westre B, et al. Clinical and histopathological tumour progression in ECL cell carcinoids (“ECLomas”). APMIS. 1999;107(12):1085–1092.
   PubMed Web of Science ®Google Scholar
• Qvigstad G, Qvigstad T, Westre B, et al. Neuroendocrine differentiation in gastric adenocarcinomas associated with severe hypergastrinemia and/or pernicious anemia. APMIS. 2002;110(2):132–139.
   PubMed Web of Science ®Google Scholar
• Bakkelund K, Fossmark R, Nordrum I, et al. Signet ring cells in gastric carcinomas are derived from neuroendocrine cells. J Histochem Cytochem. 2006;54(6):615–621.
   PubMed Web of Science ®Google Scholar
• Martinsen TC, Skogaker NE, Fossmark R, et al. Neuroendocrine cells in diffuse gastric carcinomas: an ultrastructural study with immunogold labeling of chromogranin A. Appl Immunohistochem M M. 2010;18(1):62–68.
   Web of Science ®Google Scholar
• Sordal O, Qvigstad G, Nordrum IS, et al. The PAS positive material in gastric cancer cells of signet ring type is not mucin. Exp Mol Pathol. 2014;96(3):274–278.
   PubMed Web of Science ®Google Scholar
• Waldum HL, Haugen OA, Isaksen C, et al. Enterochromaffin-like tumour cells in the diffuse but not the intestinal type of gastric carcinomas. Scand J Gastroentero Sup. 1991;180:165–169.
   PubMedGoogle Scholar
• Waldum HL, Fossmark R. Types of gastric carcinomas. IJMS. 2018;19(12):4109.
   Web of Science ®Google Scholar
• Sigal M, Rothenberg ME, Logan CY, et al. Helicobacter pylori activates and expands Lgr5(+) stem cells through direct colonization of the gastric glands. Gastroenterology. 2015;148(7):1392–1404.e21.
   PubMed Web of Science ®Google Scholar
• Hansson LR, Engstrand L, Nyren O, et al. Prevalence of Helicobacter pylori infection in subtypes of gastric cancer. Gastroenterology. 1995;109(3):885–888.
   PubMed Web of Science ®Google Scholar
• Trudeau WL, McGuigan JE. Relations between serum gastrin levels and rates of gastric hydrochloric acid secretion. N Engl J Med. 1971;284(8):408–412.
   PubMed Web of Science ®Google Scholar
• Waldum HL, Sordal OF, Mjones PG. The Enterochromaffin-like [ECL] Cell-Central in gastric physiology and pathology. IJMS. 2019;20(10):2444.
   Web of Science ®Google Scholar
• Choi E, Roland JT, Barlow BJ, et al. Cell lineage distribution atlas of the human stomach reveals heterogeneous gland populations in the gastric antrum. Gut. 2014;63(11):1711–1720.
   PubMed Web of Science ®Google Scholar
• Levi S, Beardshall K, Haddad G, et al. Campylobacter pylori and duodenal ulcers: the gastrin link. Lancet. 1989;1(8648):1167–1168.
   PubMed Web of Science ®Google Scholar
• Hansson LE, Nyren O, Hsing AW, et al. The risk of stomach cancer in patients with gastric or duodenal ulcer disease. N Engl J Med. 1996;335(4):242–249.
   PubMed Web of Science ®Google Scholar
• Eriksson NK, Karkkainen PA, Farkkila MA, et al. Prevalence and distribution of gastric intestinal metaplasia and its subtypes. Digest Liver Dis. 2008;40(5):355–360.
   Web of Science ®Google Scholar
• Hwang YJ, Kim N, Lee HS, et al. Reversibility of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication - a prospective study for up to 10 years. Aliment Pharmacol Ther. 2018;47(3):380–390.
   PubMed Web of Science ®Google Scholar
• Song H, Ekheden IG, Zheng Z, et al. Incidence of gastric cancer among patients with gastric precancerous lesions: observational cohort study in a low risk Western population. BMJ. 2015;351:h3867.
   PubMed Web of Science ®Google Scholar
• Take S, Mizuno M, Ishiki K, et al. Seventeen-year effects of eradicating Helicobacter pylori on the prevention of gastric cancer in patients with peptic ulcer; a prospective cohort study. J Gastroenterol. 2015;50(6):638–644.
   PubMed Web of Science ®Google Scholar
• Kuipers EJ, Klinkenberg-Knol EC, Meuwissen SG. Helicobacter pylori, proton pump inhibitors and gastroesophageal reflux disease. Yale J Biol Med. 1999;72(2–3):211–218.
   PubMed Web of Science ®Google Scholar
• Gong EJ, Kim DH, Ahn JY, et al. Effects of proton pump inhibitor on the distribution of helicobacter pylori and associated gastritis in patients with gastric atrophy. Digestion. 2019. DOI: 10.1159/000499424
   Web of Science ®Google Scholar
• McGuigan JE. Immunochemical studies with synthetic human gastrin. Gastroenterology. 1968;54(6):1005–1011.
   PubMed Web of Science ®Google Scholar
• Stadil F, Rehfeld JF. Radioimmunoassay of gastrin in human serum. Scand J Gastroentero Sup. 1971;9:61–65.
   PubMedGoogle Scholar
• Yalow RS, Berson SA. Radioimmunoassay of gastrin. Gastroenterology. 1970;58(1):1–14.
   PubMed Web of Science ®Google Scholar
• Sandvik AK, Waldum HL. CCK-B (gastrin) receptor regulates gastric histamine release and acid secretion. Am J Physiol. 1991;260(6 Pt 1):G925–8.
   PubMed Web of Science ®Google Scholar
• Brenna E, Waldum HL. Trophic effect of gastrin on the enterochromaffin like cells of the rat stomach: establishment of a dose response relationship. Gut. 1992;33(10):1303–1306.
   PubMed Web of Science ®Google Scholar
• Blair AJ, 3rd, Richardson CT, Walsh JH, et al. Variable contribution of gastrin to gastric acid secretion after a meal in humans. Gastroenterology. 1987;92(4):944–949.
   PubMed Web of Science ®Google Scholar
• Sjoblom SM, Sipponen P, Karonen SL, et al. Mucosal argyrophil endocrine cells in pernicious anaemia and upper gastrointestinal carcinoid tumours. J Clin Pathol. 1989;42(4):371–377.
   PubMed Web of Science ®Google Scholar
• Calvete O, Reyes J, Zuniga S, et al. Exome sequencing identifies ATP4A gene as responsible of an atypical familial type I gastric neuroendocrine tumour. Hum Mol Genet. 2015;24(10):2914–2922.
   PubMed Web of Science ®Google Scholar
• Fossmark R, Calvete O, Mjones P, et al. ECL-cell carcinoids and carcinoma in patients homozygous for an inactivating mutation in the gastric H(+) K(+) ATPase alpha subunit. APMIS. 2016;124(7):561–566.
   PubMed Web of Science ®Google Scholar
• Yucel O. Prevention of Helicobacter pylori infection in childhood. World J Gastroenterol. 2014;20(30):10348–10354.
   PubMed Web of Science ®Google Scholar
• Sandvik AK, Waldum HL. Rat gastric histamine release: a sensitive gastrin bioassay. Life Sci. 1990;46(6):453–459.
   PubMed Web of Science ®Google Scholar
• Antonodimitrakis P, Tsolakis A, Welin S, et al. Gastric carcinoid in a patient infected with Helicobacter pylori: a new entity? WJG. 2011;17(25):3066–3068.
   PubMed Web of Science ®Google Scholar
• Sato Y, Iwafuchi M, Ueki J, et al. Gastric carcinoid tumors without autoimmune gastritis in Japan: a relationship with Helicobacter pylori infection. Dig Dis Sci. 2002;47(3):579–585.
   PubMed Web of Science ®Google Scholar
• Stockbrugger R, Larsson LI, Lundqvist G, et al. Antral gastrin cells and serum gastrin in achlorhydria. Scand J Gastroentero. 1977;12(2):209–213.
   PubMed Web of Science ®Google Scholar
• Tahara T, Shibata T, Horiguchi N, et al. A possible link between gastric mucosal atrophy and gastric cancer after helicobacter pylori eradication. PloS one. 2016;11(10):e0163700.
   PubMed Web of Science ®Google Scholar
• Zhou L, Lin S, Ding S, et al. Relationship of Helicobacter pylori eradication with gastric cancer and gastric mucosal histological changes: a 10-year follow-up study. Chinese Med J (Engl). 2014;127(8):1454–1458.
   PubMed Web of Science ®Google Scholar
• Fossmark R, Sordal O, Jianu CS, et al. Treatment of gastric carcinoids type 1 with the gastrin receptor antagonist netazepide (YF476) results in regression of tumours and normalisation of serum chromogranin A. Aliment Pharmacol Ther. 2012;36(11–12):1067–1075.
   PubMed Web of Science ®Google Scholar
• Sagatun L, Mjones P, Jianu CS, et al. The gastrin receptor antagonist netazepide (YF476) in patients with type 1 gastric enterochromaffin-like cell neuroendocrine tumours: review of long-term treatment. Eur J Gastroen Hepat. 2016;28(11):1345–1352.
   PubMed Web of Science ®Google Scholar
• Niikura R, Hayakawa Y, Hirata Y, et al. Long-term proton pump inhibitor use is a risk factor of gastric cancer after treatment for Helicobacter pylori: a retrospective cohort analysis. Gut. 2018;67(10):1908–1910.
   PubMed Web of Science ®Google Scholar
• Wang TC, Dangler CA, Chen D, et al. Synergistic interaction between hypergastrinemia and Helicobacter infection in a mouse model of gastric cancer. Gastroenterology. 2000;118(1):36–47.
   PubMed Web of Science ®Google Scholar
• Sugizaki K, Tari A, Kitadai Y, et al. Anti-Helicobacter pylori therapy in localized gastric mucosa-associated lymphoid tissue lymphoma: A prospective, nationwide, multicenter study in Japan. Helicobacter. 2018;23(2):e12474.
   PubMed Web of Science ®Google Scholar
• Stathis A, Chini C, Bertoni F, et al. Long-term outcome following Helicobacter pylori eradication in a retrospective study of 105 patients with localized gastric marginal zone B-cell lymphoma of MALT type. Ann Oncol. 2009;20(6):1086–1093.
   PubMed Web of Science ®Google Scholar
• Rauws ET. Helicobacter Pylori in duodenal and gastric ulcer disease In: Calam J, editor. Helicobacter pylori. Volume 9. London (UK): Bailliere Tindall W.B. Saunders Company Ltd; 1995. p. 529–547.
   Google Scholar
• Mjones P, Nordrum IS, Sordal O, et al. Expression of the Cholecystokinin-B receptor in neoplastic gastric cells. Horm Cancer-US. 2018;9(1):40–54.
   PubMed Web of Science ®Google Scholar
• Lahner E, Esposito G, Pilozzi E, et al. Gastric cancer in patients with type I gastric carcinoids. Gastric Cancer. 2015;18(3):564–570.
   PubMed Web of Science ®Google Scholar
• Lahner E, Esposito G, Pilozzi E, et al. Occurrence of gastric cancer and carcinoids in atrophic gastritis during prospective long-term follow up. Scand J Gastroenterology. 2015;50(7):856–865.
   PubMed Web of Science ®Google Scholar
• Jianu CS, Fossmark R, Viset T, et al. Gastric carcinoids after long-term use of a proton pump inhibitor. Aliment Pharmacol Ther. 2012;36(7):644–649.
   PubMed Web of Science ®Google Scholar
• Lahner E, Pilozzi E, Esposito G, et al. Gastric carcinoid in the absence of atrophic body gastritis and with low Ki67 index: a clinical challenge. Scand J Gastroenterology. 2014;49(4):506–510.
   PubMed Web of Science ®Google Scholar
• Cavalcoli F, Zilli A, Conte D, et al. Gastric neuroendocrine neoplasms and proton pump inhibitors: fact or coincidence? Scand J Gastroenterol. 2015;50(11):1397–1403.
   PubMed Web of Science ®Google Scholar
• Ukleja A, Alkhairi B, Bejarano P, et al. De novo development of hamartomatous duodenal polyps in a patient with short bowel syndrome during teduglutide therapy: a case report. JPEN J Parenter Enteral Nutr. 2018;42(3):658–660.
   PubMed Web of Science ®Google Scholar
• George AT, Leong M, Shokouh-Amiri M, et al. Accelerated colorectal polyposis in an immunosuppressed patient with a small bowel transplant treated with teduglutide: case report and review of literature. Clin Colorectal Canc. 2019;18(3):e275-e279. DOI:10.1016/j.clcc.2019
   PubMed Web of Science ®Google Scholar
• Waldum HL, Oberg K, Sordal OF, et al. Not only stem cells, but also mature cells, particularly neuroendocrine cells, may develop into tumours: time for a paradigm shift. Therap Adv Gastroenterol. 2018;11:1756284818775054.
   Web of Science ®Google Scholar
• Hur K, Kwak MK, Lee HJ, et al. Expression of gastrin and its receptor in human gastric cancer tissues. J Cancer Res Clin Oncol. 2006;132(2):85–91.
   PubMed Web of Science ®Google Scholar
• Goetze JP, Eiland S, Svendsen LB, et al. Characterization of gastrins and their receptor in solid human gastric adenocarcinomas. Scand J Gastroenterology. 2013;48(6):688–695.
   PubMed Web of Science ®Google Scholar
• Friis-Hansen L, Sundler F, Li Y, et al. Impaired gastric acid secretion in gastrin-deficient mice. Am J Physiol. 1998;274(3):G561–8.
   PubMed Web of Science ®Google Scholar
• Friis-Hansen L, Rieneck K, Nilsson HO, et al. Gastric inflammation, metaplasia, and tumor development in gastrin-deficient mice. Gastroenterology. 2006;131(1):246–258.
   PubMed Web of Science ®Google Scholar