Digestive Diseases and Sciences

, Volume 45, Issue 9, pp 1754–1762 | Cite as

Long-Term Effects of Helicobacter pylori Eradication on Intestinal Metaplasia in Patients with Duodenal and Benign Gastric Ulcers

  • Nayoung Kim
  • Seon Hee Lim
  • Kye Heui Lee
  • Shin Eun Choi
  • Hyun Chae Jung
  • In Sung Song
  • Chung Yong Kim


This study was conducted to investigate whether or not the eradication of H. pylori could lead to the regression of intestinal metaplasia (IM) in patients with either duodenal ulcer (DU) or benign gastric ulcer (BGU). The initial antral IM grade was 0.21 in the 72 patients of the H. pylori-eradicated DU group, this decreased to 0.17, 0.14, 0.13, and 0.09 after periods of four weeks, one year, two years, and four years, respectively, but without statistical significance. In the corpus of the DU group, where IM grade was low (0.02), there was no detectable change in IM. The initial antral IM grade of 0.69 in the 41 patients of the H. pylori-eradicated BGU group decreased substantially to 0.61, 0.44, and 0.39 after periods of four weeks and one and two years, respectively, but again without statistical significance. The initial corporal IM grade of the BGU group of 0.27 decreased to 0.20, 0.15, and 0.06 after periods of four weeks and one and two years, again without statistical significance. In contrast, the IM grades of the noneradicated DU group (N = 20) and the BGU group (N = 16) showed nearly no change in the antrum and corpus. Gastritis grades of antrum and corpus in the H. pylori-eradicated DU or BGU group significantly decreased with respect to time (P = 0.0001), but there were no significant changes in the corresponding noneradicated groups. Although there was no statistical significance, IM decreased in the antrum and corpus of the stomach with BGU and in antrum of those with DU over a two to four-year period after H. pylori eradication, suggesting the possible reversibility of IM.

Helicobacter pylori intestinal metaplasia eradication duodenal ulcer gastric ulcer 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Kuipers EJ, Uyterlinde AM, Pena AS, Roosendaal R, Pals G, Nelis GF, Festen HPM: Long-term sequelae of Helicobacter pylori gastritis. Lancet 345:1525-1528, 1995Google Scholar
  2. 2.
    Correa P: Human gastric carcinogenesis: A multistep and multifactorial process. Cancer Res 52:6735-6740, 1992Google Scholar
  3. 3.
    Sipponen P, Kekki M, Siurala M: Age-related trends of gastritis and intestinal metaplasia in gastric carcinoma patients and in controls representing the population at large. Br J Cancer 49:521-530, 1984Google Scholar
  4. 4.
    Watanabe T, Tada M, Nagai H, Sasaki S, Nakao M: Helicobacter pylori infection induces gastric cancer in Mongolian gerbils. Gastroenterology 115:642-648, 1998Google Scholar
  5. 5.
    Witteman EM, Mravunac M, Becx MJCM, Hopman WPM, Verschoor JSC, Tytgat GNJ, de Koning RW: Improvement of gastric inflammation and resolution of epithelial damage one year after eradication of Helicobacter pylori. J Clin Pathol 48:250-256, 1995Google Scholar
  6. 6.
    Stolte M, Eidt S: Helicobacter pylori and the evolution of gastritis. Scand J Gastroenterol 31(suppl 214):13-16, 1996Google Scholar
  7. 7.
    Bianchi Porro G, Lazzaroni M, Bargiggia S, Maconi G, Trespi E, Perego M, Alvisi C, Villani L, Luinetti O, Fiocca R, Franceschi M, Cesana B, Solcia E: Omeprazole coupled with two antibiotics for Helicobacter pylori eradication and prevention of ulcer recurrence. Am J Gastroenterol 91:695-700, 1996Google Scholar
  8. 8.
    Kim N, Lim SH, Lee KH, Choi SE: Long-term effect of Helicobacter pylori eradication on gastric metaplasia in patients with duodenal ulcer. J Clin Gastroenterol 27:246-252, 1998Google Scholar
  9. 9.
    Forbes GM, Warren JR, Glaser ME, Cullen DJ, Marshall BJ, Collins BJ: Long-term follow-up of gastric histology after Helicobacter pylori eradication. J Gastroenterol Hepatol 11:670-673, 1996Google Scholar
  10. 10.
    Genta RM, Lew GM, Graham DY: Changes in the gastric mucosa following eradication of Helicobacter pylori. Mod Pathol 6:281-289, 1993Google Scholar
  11. 11.
    Maconi G, Lazzaroni M, Sangaletti O, Bargiggia S, Vago L, Bianchi Porro G: Effect of Helicobacter pylori eradication on gastric histology, serum gastrin and pepsinogen I levels, and gastric emptying in patients with gastric ulcer. Am J Gastroenterol 92:1844-1848, 1997Google Scholar
  12. 12.
    Ciok J, Dzieniszewski J, Lucer C: Helicobacter pylori eradication and antral intestinal metaplasia-two years follow-up study. J Physiol Pharmacol 48(suppl 4):115-122, 1997Google Scholar
  13. 13.
    van der Hulst RW, van der Ende A, Dekker FW, Ten Kate FJ, Weel JF, Keller JJ, Kruizinga SP, Dankert J, Tytgat GN: Effect of Helicobacter pylori eradication on gastritis in relation to cagA: A prospective 1-year follow-up study. Gastroenterology 113:25-30, 1997Google Scholar
  14. 14.
    El-Omar EM, Oien K, El-Nujumi A, Gillen D, Wirz A, Dahill S, Williams C, Ardill JE, McColl KE: Helicobacter pylori infection and chronic gastric acid hyposecretion. Gastroenterology 113:15-24, 1997Google Scholar
  15. 15.
    Tytgat GNJ, Rauws EAJ: The role of Campylobacter pylori in gastroduodenal diseases. A “believer”'s point of view. First Meeting of the European Campylobacter pylori Study Group. Bordeaux 1988. Gastroenterol Clin Biol 13:118B-121B, 1989Google Scholar
  16. 16.
    Graham DY: Campylobacter pylori and peptic ulcer disease. Gastroenterology 96(2 Pt 2 suppl):615-625, 1989Google Scholar
  17. 17.
    Dixon MF: Helicobacter pylori and peptic ulceration: histopathological aspects. J Gastroenterol Hepatol 6:125-130, 1991Google Scholar
  18. 18.
    Sipponen P, Seppala K, Aarynen M, Helske T, Kettunen P: Chronic gastritis and gastroduodenal ulcer: A case control study on risk of coexisting duodenal or gastric ulcer in patients with gastritis. Gut 30:922-929, 1989Google Scholar
  19. 19.
    Mielke S, Bayerdorffer E, Meining A, Stolte M, Malfertheiner P: Identifying persons at risk for gastric cancer? Helicobacter 2(suppl 1):S61-S66, 1997Google Scholar
  20. 20.
    Kim N, Lim SH, Lee KH, Jung HC, Song IS, Kim CY: Helicobacter pylori reinfection rate and duodenal ulcer recurrence in Korea. J Clin Gastroenterol 27:321-326, 1998Google Scholar
  21. 21.
    Price AB: The Sydney system: Histological division. J Gastroenterol Hepatol 6:209-222, 1991Google Scholar
  22. 22.
    Dixon MF, Genta RM, Yardley JH, Correa P: Classification and grading of gastritis: The updated Sydney system. Am J Surg Pathol 20:1161-1181, 1996Google Scholar
  23. 23.
    Correa P: Chronic gastritis: A clinico-pathological classification. Am J Gastroenterol 83:504-509, 1988Google Scholar
  24. 24.
    Kimura K: Chronological transition of the fundic-pyloric border determined by stepwise biopsy of the lesser and greater curvatures of the stomach. Gastroenterology 63:584-592, 1972Google Scholar
  25. 25.
    Stolte M, Eidt S, Ohnsmann A: Differences in Helicobacter pylori associated gastritis in the antrum and body of the stomach. Z Gastroenterol 28:229-233, 1990Google Scholar
  26. 26.
    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 86:285-291, 1991Google Scholar
  27. 27.
    Kim N, Choi WR, Song CH, Sheen DH, Yang SS, Lee JY, Han YJ, Lim SH, Lee KH, Choi SE: Difference in the distribution pattern of Helicobacter pylori and grade of gastritis in the antrum and in the body between duodenal ulcer and benign gastric ulcer patients. Kor J Intern Med (15:32-36, 2000)Google Scholar
  28. 28.
    Eidt S, Stolte M: Prevalence of intestinal metaplasia in Helicobacter pylori gastritis. Scand J Gastroenterol 29:607-610, 1994Google Scholar
  29. 29.
    Sobala GM, Pignatelli B, Schorah CJ, Bartsch H, Sanderson M, Dixon MF, Shires S, King RF, Axon AT: Levels of nitrite, nitrate, N-nitroso compounds, ascorbic acid, and total bile acids in the gastric juice of patients with and without precancerous conditions of the stomach. Carcinogenesis 12:193-198, 1991Google Scholar
  30. 30.
    Correa P: A human model of gastric carcinogenesis. Cancer Res 48:3554-3560, 1988Google Scholar
  31. 31.
    Craanen ME, Dekker W, Blok P, Ferwerda J, Tytgat GN: Intestinal metaplasia and Helicobacter pylori: An endoscopic bioptic study of the gastric antrum. Gut 33:16-20, 1992Google Scholar
  32. 32.
    Meining A, Behrens R, Lehn N, Bayerdorffer E, Stolte M: Different expression of Helicobacter pylori gastritis in children-evidence for a specific pediatric disease? Helicobacter 1:92-97, 1996Google Scholar
  33. 33.
    Scott N, Landsdown M, Diament R, Rathbone B, Murday V, Wyatt JI, McMahou M, Dixon MF, Quirke P: Helicobacter pylori and intestinal metaplasia in a gastric cancer family. Lancet 335:728, 1990Google Scholar
  34. 34.
    Shousha S, el-Sherif AM, el-Guneid A, Arnaout AH, Murray-Lyon IM: Helicobacter pylori and intestinal metaplasia: Comparison between British and Yemeni patients. Am J Gastroenterol 88:1373-1376, 1993Google Scholar
  35. 35.
    Louw JA, Falck V, van Rensburg C, Zak J, Adams G, Marks IN: Distribution of Helicobacter pylori colonisation and associated gastric inflammatory changes: Difference between patients with duodenal and gastric ulcers. J Clin Pathol 46:754-756, 1993Google Scholar
  36. 36.
    Hansson L-E, Engstrand L, Nyren O, Evans DJ Jr, Lindgren A, Bergstrom R, Andersson B, Athlin L, Bendtsen O, Tracz P: Helicobacter pylori infection: Independent risk indicator of gastric carcinoma. Gastroenterology 105:1098-1103, 1993Google Scholar
  37. 37.
    Sipponen P, Kosunen TU, Valle J, Riihela M, Seppala K: Helicobacter pylori infection and chronic gastritis in gastric cancer. J Clin Pathol 45:319-323, 1992Google Scholar
  38. 38.
    Correa P, Haenszel W, Cuello C, Zavala D, Fontham E, Zarama G, Tannenbaum S, Collazos T, Ruiz B: Gastric precancerous process in a high risk population; cross sectional studies. Cancer Res 50:4731-4736, 1990Google Scholar
  39. 39.
    Correa P, Haenszel W, Cuello C, Zavala D, Fontham E, Zarama G, Tannenbaum S, Collazos T, Ruiz B: Gastric precancerous process in a high risk population; cohort follow-up. Cancer Res 50:4737-4740, 1990Google Scholar
  40. 40.
    Morson BC, Sobin LH, Grundmann E, Johansen A, Nagayo T, Serck-Hanssen A: Precancerous conditions and epithelial dysplasia in the stomach. J Clin Pathol 33:711-721, 1980Google Scholar
  41. 41.
    Hattori T: Development of adenocarcinomas in the stomach. Cancer 57:1528-1534, 1986Google Scholar
  42. 42.
    Kim HS, Lee YC, Lee HW, Yoo HM, Lee CG, Kim JM, Lee KJ, Kim PS, Moon BS, Park HJ, Kim DY, Lee KS, Kim WH, Chung JB, Chon CY, Lee SI, Moon YM, Kang JK, Park IS: Seroepidemiologic study of Helicobacter pylori infection in Korea. Kor J Gastroenterol 33:170-182, 1999Google Scholar
  43. 43.
    Baik S-C, Kim J-B, Cho M-J, Kim Y-C, Park C-K, Ryou H-H, Choi H-J, Rhee K-H: Prevalence of infection among normal Korean adults. J Kor Soc Microbiol 25:455-462, 1990Google Scholar
  44. 44.
    Parsonnet J, Friedman GD, Vandersteen D, Chang Y, Vogelman JH, Orentreich N, Sibley RK: Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325:1127-1131, 1991Google Scholar
  45. 45.
    Rugge M, Farinati F, Di Mario F, Babba R, Valiante F, Cardin F: Gastric epithelial dysplasia: A prospective multicenter follow-up study from the Interdisciplinary Group on Gastric Epithelial Dysplasia. Hum Pathol 22:1002-1008, 1991Google Scholar

Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • Nayoung Kim
    • 1
    • 2
  • Seon Hee Lim
    • 1
    • 2
  • Kye Heui Lee
    • 1
    • 2
  • Shin Eun Choi
    • 1
    • 2
  • Hyun Chae Jung
    • 1
    • 2
  • In Sung Song
    • 1
    • 2
  • Chung Yong Kim
    • 1
    • 2
  1. 1.Departments of Internal Medicine and Anatomical PathologyKangnam General Hospital, Public CorporationKorea
  2. 2.Department of Internal MedicineSeoul National University College of Medicine and Liver Research InstituteSeoulKorea

Personalised recommendations