Skip to main content
PMC home page
CMAJ : Canadian Medical Association Journal logoLink to CMAJ : Canadian Medical Association Journal
. 1994 Jan 15;150(2):177–185.

Helicobacter pylori infection as a cause of gastritis, duodenal ulcer, gastric cancer and nonulcer dyspepsia: a systematic overview.

S J Veldhuyzen van Zanten 1, P M Sherman 1
PMCID: PMC1486230  PMID: 8287340

Abstract

OBJECTIVE: To evaluate current evidence for a causal relation between Helicobacter pylori infection and gastritis, duodenal ulcer, gastric cancer and nonulcer dyspepsia. DATA SOURCES: A MEDLINE search for articles published in English between January 1983 and December 1992 with the use of MeSH terms Helicobacter pylori, gastritis, duodenal ulcer, gastric cancer, dyspepsia and clinical trial; abstracts were excluded. Six journals and Current Contents were searched manually for pertinent articles published in that time frame. STUDY SELECTION: Original studies with at least 25 patients, case reports and reviews that examined the relation between H. pylori and the four gastrointestinal disorders; 350 articles were on gastritis, 122 on duodenal ulcer, 44 on gastric cancer and 96 on nonulcer dyspepsia. DATA EXTRACTION: The quality of the studies was rated independently on a four-point scale. The strength of the evidence was assessed using a six-point scale for each of the eight established guidelines for determining a causal relation. DATA SYNTHESIS: There was conclusive evidence of a causal relation between H. pylori infection and histologic gastritis. Koch's postulates for the identification of a microorganism as the causative agent of a disease were fulfilled for H. pylori as a causative agent of gastritis. There was strong evidence that H. pylori is the main cause of duodenal ulcers not induced by nonsteroidal anti-inflammatory drugs, but all of Koch's postulates were not fulfilled. There was moderate epidemiologic evidence of an association between chronic H. pylori infection and gastric cancer. There was a lack of convincing evidence of a causal association between H. pylori and nonulcer dyspepsia. CONCLUSIONS: The evidence supports a strong causal relation between H. pylori infection and gastritis and duodenal ulcer and a moderate relation between such infection and gastric cancer. Further studies are needed to clarify the role of H. pylori in these disorders. Thus far, there is no evidence of a causal relation between H. pylori and nonulcer dyspepsia.

Full text

PDF
177

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alam K., Schubert T. T., Bologna S. D., Ma C. K. Increased density of Helicobacter pylori on antral biopsy is associated with severity of acute and chronic inflammation and likelihood of duodenal ulceration. Am J Gastroenterol. 1992 Apr;87(4):424–428. [PubMed] [Google Scholar]
  2. Asaka M., Kimura T., Kudo M., Takeda H., Mitani S., Miyazaki T., Miki K., Graham D. Y. Relationship of Helicobacter pylori to serum pepsinogens in an asymptomatic Japanese population. Gastroenterology. 1992 Mar;102(3):760–766. doi: 10.1016/0016-5085(92)90156-s. [DOI] [PubMed] [Google Scholar]
  3. Barbara L., Camilleri M., Corinaldesi R., Crean G. P., Heading R. C., Johnson A. G., Malagelada J. R., Stanghellini V., Wienbeck M. Definition and investigation of dyspepsia. Consensus of an international ad hoc working party. Dig Dis Sci. 1989 Aug;34(8):1272–1276. doi: 10.1007/BF01537277. [DOI] [PubMed] [Google Scholar]
  4. Barnes R. J., Uff J. S., Dent J. C., Gear M. W., Wilkinson S. P. Long-term follow up of patients with gastritis associated with Helicobacter pylori infection. Br J Gen Pract. 1991 Jul;41(348):286–288. [PMC free article] [PubMed] [Google Scholar]
  5. Barthel J. S., Westblom T. U., Havey A. D., Gonzalez F., Everett E. D. Gastritis and Campylobacter pylori in healthy, asymptomatic volunteers. Arch Intern Med. 1988 May;148(5):1149–1151. [PubMed] [Google Scholar]
  6. Bayerdörffer E., Lehn N., Hatz R., Mannes G. A., Oertel H., Sauerbruch T., Stolte M. Difference in expression of Helicobacter pylori gastritis in antrum and body. Gastroenterology. 1992 May;102(5):1575–1582. doi: 10.1016/0016-5085(92)91716-h. [DOI] [PubMed] [Google Scholar]
  7. Bernersen B., Johnsen R., Bostad L., Straume B., Sommer A. I., Burhol P. G. Is Helicobacter pylori the cause of dyspepsia? BMJ. 1992 May 16;304(6837):1276–1279. doi: 10.1136/bmj.304.6837.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bertram T. A., Murray P. D., Morgan D. R., Jerdak G., Yang P., Czinn S. Gastritis associated with infection by Helicobacter pylori in humans: geographical differences. Scand J Gastroenterol Suppl. 1991;181:1–8. doi: 10.3109/00365529109093201. [DOI] [PubMed] [Google Scholar]
  9. Blaser M. J. Gastric Campylobacter-like organisms, gastritis, and peptic ulcer disease. Gastroenterology. 1987 Aug;93(2):371–383. doi: 10.1016/0016-5085(87)91028-6. [DOI] [PubMed] [Google Scholar]
  10. Borody T. J., George L. L., Brandl S., Andrews P., Jankiewicz E., Ostapowicz N. Smoking does not contribute to duodenal ulcer relapse after Helicobacter pylori eradication. Am J Gastroenterol. 1992 Oct;87(10):1390–1393. [PubMed] [Google Scholar]
  11. Burstein M., Monge E., León-Barúa R., Lozano R., Berendson R., Gilman R. H., Legua H., Rodriguez C. Low peptic ulcer and high gastric cancer prevalence in a developing country with a high prevalence of infection by Helicobacter pylori. J Clin Gastroenterol. 1991 Apr;13(2):154–156. doi: 10.1097/00004836-199104000-00007. [DOI] [PubMed] [Google Scholar]
  12. Cheng E. H., Bermanski P., Silversmith M., Valenstein P., Kawanishi H. Prevalence of Campylobacter pylori in esophagitis, gastritis, and duodenal disease. Arch Intern Med. 1989 Jun;149(6):1373–1375. [PubMed] [Google Scholar]
  13. Correa P., Yardley J. H. Grading and classification of chronic gastritis: one American response to the Sydney system. Gastroenterology. 1992 Jan;102(1):355–359. doi: 10.1016/0016-5085(92)91820-t. [DOI] [PubMed] [Google Scholar]
  14. Craanen M. E., Dekker W., Blok P., Ferwerda J., Tytgat G. N. Intestinal metaplasia and Helicobacter pylori: an endoscopic bioptic study of the gastric antrum. Gut. 1992 Jan;33(1):16–20. doi: 10.1136/gut.33.1.16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dobrilla G., Vallaperta P., Amplatz S. Influence of ulcer healing agents on ulcer relapse after discontinuation of acute treatment: a pooled estimate of controlled clinical trials. Gut. 1988 Feb;29(2):181–187. doi: 10.1136/gut.29.2.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dooley C. P., Cohen H., Fitzgibbons P. L., Bauer M., Appleman M. D., Perez-Perez G. I., Blaser M. J. Prevalence of Helicobacter pylori infection and histologic gastritis in asymptomatic persons. N Engl J Med. 1989 Dec 7;321(23):1562–1566. doi: 10.1056/NEJM198912073212302. [DOI] [PubMed] [Google Scholar]
  17. Dooley C. P., Cohen H. The clinical significance of Campylobacter pylori. Ann Intern Med. 1988 Jan;108(1):70–79. doi: 10.7326/0003-4819-108-1-70. [DOI] [PubMed] [Google Scholar]
  18. Drumm B., O'Brien A., Cutz E., Sherman P. Campylobacter pyloridis-associated primary gastritis in children. Pediatrics. 1987 Aug;80(2):192–195. [PubMed] [Google Scholar]
  19. Forman D., Newell D. G., Fullerton F., Yarnell J. W., Stacey A. R., Wald N., Sitas F. Association between infection with Helicobacter pylori and risk of gastric cancer: evidence from a prospective investigation. BMJ. 1991 Jun 1;302(6788):1302–1305. doi: 10.1136/bmj.302.6788.1302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Graham D. Y., Alpert L. C., Smith J. L., Yoshimura H. H. Iatrogenic Campylobacter pylori infection is a cause of epidemic achlorhydria. Am J Gastroenterol. 1988 Sep;83(9):974–980. [PubMed] [Google Scholar]
  22. Graham D. Y. Campylobacter pylori and peptic ulcer disease. Gastroenterology. 1989 Feb;96(2 Pt 2 Suppl):615–625. doi: 10.1016/s0016-5085(89)80057-5. [DOI] [PubMed] [Google Scholar]
  23. Graham D. Y., Lew G. M., Evans D. G., Evans D. J., Jr, Klein P. D. Effect of triple therapy (antibiotics plus bismuth) on duodenal ulcer healing. A randomized controlled trial. Ann Intern Med. 1991 Aug 15;115(4):266–269. doi: 10.7326/0003-4819-115-4-266. [DOI] [PubMed] [Google Scholar]
  24. Graham D. Y., Lew G. M., Klein P. D., Evans D. G., Evans D. J., Jr, Saeed Z. A., Malaty H. M. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer. A randomized, controlled study. Ann Intern Med. 1992 May 1;116(9):705–708. doi: 10.7326/0003-4819-116-9-705. [DOI] [PubMed] [Google Scholar]
  25. Graham D. Y., Lidsky M. D., Cox A. M., Evans D. J., Jr, Evans D. G., Alpert L., Klein P. D., Sessoms S. L., Michaletz P. A., Saeed Z. A. Long-term nonsteroidal antiinflammatory drug use and Helicobacter pylori infection. Gastroenterology. 1991 Jun;100(6):1653–1657. doi: 10.1016/0016-5085(91)90665-8. [DOI] [PubMed] [Google Scholar]
  26. Gregson D. B., Low D. E., Cohen M. M., Cooter N. B., Connon J. J., Wolman S. L., Simor A. E. The prevalence of Campylobacter pylori gastritis among asymptomatic adults. CMAJ. 1989 Jun 15;140(12):1449–1453. [PMC free article] [PubMed] [Google Scholar]
  27. Holcombe C. Helicobacter pylori: the African enigma. Gut. 1992 Apr;33(4):429–431. doi: 10.1136/gut.33.4.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hui W. M., Ho J., Lam S. K. Pathogenetic role of Helicobacter pylori in duodenal ulcer disease. Multivariate analysis of factors affecting relapse. Dig Dis Sci. 1991 Apr;36(4):424–430. doi: 10.1007/BF01298869. [DOI] [PubMed] [Google Scholar]
  29. Kang J. Y., Tay H. H., Wee A., Guan R., Math M. V., Yap I. Effect of colloidal bismuth subcitrate on symptoms and gastric histology in non-ulcer dyspepsia. A double blind placebo controlled study. Gut. 1990 Apr;31(4):476–480. doi: 10.1136/gut.31.4.476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Karttunen T., Niemelä S., Lehtola J. Helicobacter pylori in dyspeptic patients: quantitative association with severity of gastritis, intragastric pH, and serum gastrin concentration. Scand J Gastroenterol Suppl. 1991;186:124–134. doi: 10.3109/00365529109103999. [DOI] [PubMed] [Google Scholar]
  31. Kekki M., Maaroos H. I., Sipponen P., Uibo R., Tammur R., Tamm A., Villako K. Grade of Helicobacter pylori colonisation in relation to gastritis: a six-year population-based follow-up study. Scand J Gastroenterol Suppl. 1991;186:142–150. [PubMed] [Google Scholar]
  32. Krakowka S., Morgan D. R., Kraft W. G., Leunk R. D. Establishment of gastric Campylobacter pylori infection in the neonatal gnotobiotic piglet. Infect Immun. 1987 Nov;55(11):2789–2796. doi: 10.1128/iai.55.11.2789-2796.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lambert J. R., Dunn K., Borromeo M., Korman M. G., Hansky J. Campylobacter pylori--a role in non-ulcer dyspepsia? Scand J Gastroenterol Suppl. 1989;160:7–13. doi: 10.3109/00365528909091728. [DOI] [PubMed] [Google Scholar]
  34. Lanza F. L., Evans D. G., Graham D. Y. Effect of Helicobacter pylori infection on the severity of gastroduodenal mucosal injury after the acute administration of naproxen or aspirin to normal volunteers. Am J Gastroenterol. 1991 Jun;86(6):735–737. [PubMed] [Google Scholar]
  35. Lee A., Fox J. G., Otto G., Murphy J. A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology. 1990 Nov;99(5):1315–1323. doi: 10.1016/0016-5085(90)91156-z. [DOI] [PubMed] [Google Scholar]
  36. Levi S., Beardshall K., Haddad G., Playford R., Ghosh P., Calam J. Campylobacter pylori and duodenal ulcers: the gastrin link. Lancet. 1989 May 27;1(8648):1167–1168. doi: 10.1016/s0140-6736(89)92752-9. [DOI] [PubMed] [Google Scholar]
  37. Li Y. Y., Hu P. J., Du G. G., Hazell S. L. The prevalence of Helicobacter pylori infection in the Peoples Republic of China. Am J Gastroenterol. 1991 Apr;86(4):446–449. [PubMed] [Google Scholar]
  38. Maaroos H. I., Kekki M., Sipponen P., Salupere V., Villako K. Grade of Helicobacter pylori colonisation, chronic gastritis and relative risks of contracting high gastric ulcers: a seven-year follow-up. Scand J Gastroenterol Suppl. 1991;186:65–72. doi: 10.3109/00365529109103989. [DOI] [PubMed] [Google Scholar]
  39. Maaroos H. I., Kekki M., Villako K., Sipponen P., Tamm A., Sadeniemi L. The occurrence and extent of Helicobacter pylori colonization and antral and body gastritis profiles in an Estonian population sample. Scand J Gastroenterol. 1990 Oct;25(10):1010–1017. doi: 10.3109/00365529008997627. [DOI] [PubMed] [Google Scholar]
  40. Marshall B. J., Armstrong J. A., McGechie D. B., Glancy R. J. Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med J Aust. 1985 Apr 15;142(8):436–439. doi: 10.5694/j.1326-5377.1985.tb113443.x. [DOI] [PubMed] [Google Scholar]
  41. Marshall B. J. Campylobacter pyloridis and gastritis. J Infect Dis. 1986 Apr;153(4):650–657. doi: 10.1093/infdis/153.4.650. [DOI] [PubMed] [Google Scholar]
  42. Marshall B. J., Goodwin C. S., Warren J. R., Murray R., Blincow E. D., Blackbourn S. J., Phillips M., Waters T. E., Sanderson C. R. Prospective double-blind trial of duodenal ulcer relapse after eradication of Campylobacter pylori. Lancet. 1988 Dec 24;2(8626-8627):1437–1442. doi: 10.1016/s0140-6736(88)90929-4. [DOI] [PubMed] [Google Scholar]
  43. McColl K. E., Fullarton G. M., Chittajalu R., el Nujumi A. M., MacDonald A. M., Dahill S. W., Hilditch T. E. Plasma gastrin, daytime intragastric pH, and nocturnal acid output before and at 1 and 7 months after eradication of Helicobacter pylori in duodenal ulcer subjects. Scand J Gastroenterol. 1991 Mar;26(3):339–346. doi: 10.3109/00365529109025052. [DOI] [PubMed] [Google Scholar]
  44. McNulty C. A., Watson D. M. Spiral bacteria of the gastric antrum. Lancet. 1984 May 12;1(8385):1068–1069. doi: 10.1016/s0140-6736(84)91469-7. [DOI] [PubMed] [Google Scholar]
  45. Miller J. P., Faragher E. B. Relapse of duodenal ulcer: does it matter which drug is used in initial treatment? Br Med J (Clin Res Ed) 1986 Nov 1;293(6555):1117–1118. doi: 10.1136/bmj.293.6555.1117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Miller J. P., Faragher E. B. The potential impact of Campylobacter pylori on the treatment of duodenal ulcer disease. Scand J Gastroenterol Suppl. 1989;160:39–45. doi: 10.3109/00365528909091734. [DOI] [PubMed] [Google Scholar]
  47. Morris A., Nicholson G. Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH. Am J Gastroenterol. 1987 Mar;82(3):192–199. [PubMed] [Google Scholar]
  48. Mégraud F., Brassens-Rabbé M. P., Denis F., Belbouri A., Hoa D. Q. Seroepidemiology of Campylobacter pylori infection in various populations. J Clin Microbiol. 1989 Aug;27(8):1870–1873. doi: 10.1128/jcm.27.8.1870-1873.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. 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]
  50. O'Connor H. J., Newbold K. M., Alexander-Williams J., Thompson H., Drumm J., Donovan I. A. Effect of Roux-en-Y biliary diversion on Campylobacter pylori. Gastroenterology. 1989 Oct;97(4):958–964. doi: 10.1016/0016-5085(89)91504-7. [DOI] [PubMed] [Google Scholar]
  51. Ormand J. E., Talley N. J., Shorter R. G., Conley C. R., Carpenter H. A., Fich A., Wilson W. R., Phillips S. F. Prevalence of Helicobacter pylori in specific forms of gastritis. Further evidence supporting a pathogenic role for H. pylori in chronic nonspecific gastritis. Dig Dis Sci. 1991 Feb;36(2):142–145. doi: 10.1007/BF01300747. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Patchett S., Beattie S., Leen E., Keane C., O'Morain C. Eradicating Helicobacter pylori and symptoms of non-ulcer dyspepsia. BMJ. 1991 Nov 16;303(6812):1238–1240. doi: 10.1136/bmj.303.6812.1238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Patchett S., Beattie S., Leen E., Keane C., O'Morain C. Helicobacter pylori and duodenal ulcer recurrence. Am J Gastroenterol. 1992 Jan;87(1):24–27. [PubMed] [Google Scholar]
  55. Peterson W. L. Helicobacter pylori and peptic ulcer disease. N Engl J Med. 1991 Apr 11;324(15):1043–1048. doi: 10.1056/NEJM199104113241507. [DOI] [PubMed] [Google Scholar]
  56. Rabeneck L., Ransohoff D. F. Is Helicobacter pylori a cause of duodenal ulcer? A methodologic critique of current evidence. Am J Med. 1991 Dec;91(6):566–572. doi: 10.1016/0002-9343(91)90207-e. [DOI] [PubMed] [Google Scholar]
  57. Rauws E. A., Langenberg W., Houthoff H. J., Zanen H. C., Tytgat G. N. Campylobacter pyloridis-associated chronic active antral gastritis. A prospective study of its prevalence and the effects of antibacterial and antiulcer treatment. Gastroenterology. 1988 Jan;94(1):33–40. [PubMed] [Google Scholar]
  58. Rauws E. A., Royen E. A., Langenberg W., Woensel J. V., Vrij A. A., Tytgat G. N. 14C-urea breath test in C pylori gastritis. Gut. 1989 Jun;30(6):798–803. doi: 10.1136/gut.30.6.798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rauws E. A., Tytgat G. N. Cure of duodenal ulcer associated with eradication of Helicobacter pylori. Lancet. 1990 May 26;335(8700):1233–1235. doi: 10.1016/0140-6736(90)91301-p. [DOI] [PubMed] [Google Scholar]
  60. Rokkas T., Pursey C., Uzoechina E., Dorrington L., Simmons N. A., Filipe M. I., Sladen G. E. Campylobacter pylori and non-ulcer dyspepsia. Am J Gastroenterol. 1987 Nov;82(11):1149–1152. [PubMed] [Google Scholar]
  61. Satoh K., Kimura K., Yoshida Y., Kasano T., Kihira K., Taniguchi Y. A topographical relationship between Helicobacter pylori and gastritis: quantitative assessment of Helicobacter pylori in the gastric mucosa. Am J Gastroenterol. 1991 Mar;86(3):285–291. [PubMed] [Google Scholar]
  62. Schubert T. T., Schubert A. B., Ma C. K. Symptoms, gastritis, and Helicobacter pylori in patients referred for endoscopy. Gastrointest Endosc. 1992 May-Jun;38(3):357–360. doi: 10.1016/s0016-5107(92)70432-5. [DOI] [PubMed] [Google Scholar]
  63. Sipponen P., Kosunen T. U., Valle J., Riihelä M., Seppälä K. Helicobacter pylori infection and chronic gastritis in gastric cancer. J Clin Pathol. 1992 Apr;45(4):319–323. doi: 10.1136/jcp.45.4.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Sipponen P., Varis K., Fräki O., Korri U. M., Seppälä K., Siurala M. Cumulative 10-year risk of symptomatic duodenal and gastric ulcer in patients with or without chronic gastritis. A clinical follow-up study of 454 outpatients. Scand J Gastroenterol. 1990 Oct;25(10):966–973. doi: 10.3109/00365529008997621. [DOI] [PubMed] [Google Scholar]
  65. Sobala G. M., Crabtree J. E., Dixon M. F., Schorah C. J., Taylor J. D., Rathbone B. J., Heatley R. V., Axon A. T. Acute Helicobacter pylori infection: clinical features, local and systemic immune response, gastric mucosal histology, and gastric juice ascorbic acid concentrations. Gut. 1991 Nov;32(11):1415–1418. doi: 10.1136/gut.32.11.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Soll A. H., Kurata J., McGuigan J. E. Ulcers, nonsteroidal antiinflammatory drugs, and related matters. Gastroenterology. 1989 Feb;96(2 Pt 2 Suppl):561–568. doi: 10.1016/s0016-5085(89)80051-4. [DOI] [PubMed] [Google Scholar]
  67. Strauss R. M., Wang T. C., Kelsey P. B., Compton C. C., Ferraro M. J., Perez-Perez G., Parsonnet J., Blaser M. J. Association of Helicobacter pylori infection with dyspeptic symptoms in patients undergoing gastroduodenoscopy. Am J Med. 1990 Oct;89(4):464–469. doi: 10.1016/0002-9343(90)90377-p. [DOI] [PubMed] [Google Scholar]
  68. Talley N. J., Phillips S. F. Non-ulcer dyspepsia: potential causes and pathophysiology. Ann Intern Med. 1988 Jun;108(6):865–879. doi: 10.7326/0003-4819-108-6-865. [DOI] [PubMed] [Google Scholar]
  69. Talley N. J., Zinsmeister A. R., Weaver A., DiMagno E. P., Carpenter H. A., Perez-Perez G. I., Blaser M. J. Gastric adenocarcinoma and Helicobacter pylori infection. J Natl Cancer Inst. 1991 Dec 4;83(23):1734–1739. doi: 10.1093/jnci/83.23.1734. [DOI] [PubMed] [Google Scholar]
  70. Taylor D. N., Blaser M. J. The epidemiology of Helicobacter pylori infection. Epidemiol Rev. 1991;13:42–59. doi: 10.1093/oxfordjournals.epirev.a036078. [DOI] [PubMed] [Google Scholar]
  71. Tucci A., Corinaldesi R., Stanghellini V., Tosetti C., Di Febo G., Paparo G. F., Varoli O., Paganelli G. M., Labate A. M., Masci C. Helicobacter pylori infection and gastric function in patients with chronic idiopathic dyspepsia. Gastroenterology. 1992 Sep;103(3):768–774. doi: 10.1016/0016-5085(92)90004-i. [DOI] [PubMed] [Google Scholar]
  72. Tytgat G. N., Rauws E. A. Campylobacter pylori and its role in peptic ulcer disease. Gastroenterol Clin North Am. 1990 Mar;19(1):183–196. [PubMed] [Google Scholar]
  73. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1983 Jun 4;1(8336):1273–1275. [PubMed] [Google Scholar]
  74. Veldhuyzen van Zanten S. J. Helicobacter pylori, causation, change in natural history, and why Helicobacter-positive duodenal ulcers should not be routinely treated. Scand J Gastroenterol Suppl. 1991;187:98–104. doi: 10.3109/00365529109098231. [DOI] [PubMed] [Google Scholar]
  75. Walker S. J., Birch P. J., Stewart M., Stoddard C. J., Hart C. A., Day D. W. Patterns of colonisation of Campylobacter pylori in the oesophagus, stomach and duodenum. Gut. 1989 Oct;30(10):1334–1338. doi: 10.1136/gut.30.10.1334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Wotherspoon A. C., Ortiz-Hidalgo C., Falzon M. R., Isaacson P. G. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet. 1991 Nov 9;338(8776):1175–1176. doi: 10.1016/0140-6736(91)92035-z. [DOI] [PubMed] [Google Scholar]
  77. Wyatt J. I., Rathbone B. J., Sobala G. M., Shallcross T., Heatley R. V., Axon A. T., Dixon M. F. Gastric epithelium in the duodenum: its association with Helicobacter pylori and inflammation. J Clin Pathol. 1990 Dec;43(12):981–986. doi: 10.1136/jcp.43.12.981. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from CMAJ: Canadian Medical Association Journal are provided here courtesy of Canadian Medical Association

RESOURCES