Reversibility of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication - a prospective study for up to 10 years

Alimentary Pharmacology and Therapeutics

Volumn 47, Issue 3, 2018, Pages 380-390

  Hwang, Y J ^a   Kim, N ^a,b   Lee, H S ^a   Lee, J B ^a   Choi, Y J ^a   Yoon, H ^a   Shin, C M ^a   Park, Y S ^a   Lee, D H ^a,b  

^a Seoul National University Bundang Hospital   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; BISMUTH CITRATE; CLARITHROMYCIN; ESOMEPRAZOLE; METRONIDAZOLE; MOXIFLOXACIN; PROTON PUMP INHIBITOR; TETRACYCLINE;

AGED; ARTICLE; ATROPHIC GASTRITIS; CLINICAL FEATURE; DISEASE CLASSIFICATION; DISEASE ERADICATION; DRUG DOSE SEQUENCE; DRUG EFFECT; DRUG EFFICACY; ERADICATION THERAPY; FEMALE; FOLLOW UP; HELICOBACTER INFECTION; HISTOLOGY; HUMAN; HUMAN TISSUE; INTESTINE METAPLASIA; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROSPECTIVE STUDY; STOMACH ANTRUM; SYDNEY CLASSIFICATION; TREATMENT OUTCOME; ADOLESCENT; ADULT; COMPLICATION; CONVALESCENCE; HELICOBACTER PYLORI; INTESTINE; METAPLASIA; MICROBIOLOGY; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; PRECANCER; RISK FACTOR; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; FEMALE; FOLLOW-UP STUDIES; GASTRITIS, ATROPHIC; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INTESTINES; MALE; METAPLASIA; MIDDLE AGED; PRECANCEROUS CONDITIONS; RECOVERY OF FUNCTION; RISK FACTORS; YOUNG ADULT;

EID: 85040188732     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.14424     Document Type: Article

References (74)

1. Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359-E386.
2. Jung KW, Won YJ, Kong HJ, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2012. Cancer Res Treat. 2015;47:127-141.
3. Leung WK, Wu MS, Kakugawa Y, et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 2008;9:279-287.
4. Oh S, Kim N, Kwon J-W, et al. Effect of Helicobacter pylori Eradication and ABO Genotype on Gastric Cancer Development. Helicobacter. 2016;21:596-605.
5. Leung WK, Sung JJ. Chemoprevention of gastric cancer. Euro J Gastroenterol Hepatol. 2006;18:867-871.
6. Wu CY, Kuo KN, Wu MS, Chen YJ, Wang CB, Lin JT. Early Helicobacter pylori eradication decreases risk of gastric cancer in patients with peptic ulcer disease. Gastroenterology. 2009;137:8.
7. Chey WD, Wong BC. American College of Gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol. 2007;102:1808-1825.
8. Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784-789.
9. Peek RM, Crabtree JE. Helicobacter infection and gastric neoplasia. J Pathol. 2006;208:233-248.
10. Park YM, Kim JH, Baik SJ, Park JJ, Youn YH, Park H. Clinical risk assessment for gastric cancer in asymptomatic population after a health check-up: an individualized consideration of the risk factors. Medicine. 2016;95:e5351.
11. Li D, Bautista MC, Jiang SF, et al. Risks and predictors of gastric adenocarcinoma in patients with gastric intestinal metaplasia and dysplasia: a population-based study. Am J Gastroenterol. 2016;111:1104-1113.
12. Eslick GD, Lim LL, Byles JE, Xia HH, Talley NJ. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol. 1999;94:2373-2379.
13. Leung WK, Yu J, To KF, et al. Apoptosis and proliferation in Helicobacter pylori-associated gastric intestinal metaplasia. Aliment Pharmacol Ther. 2001;15:1467-1472.
14. Leung WK, Sung JJ. Review article: intestinal metaplasia and gastric carcinogenesis. Aliment Pharmacol Ther. 2002;16:1209-1216.
15. Rugge M, de Boni M, Pennelli G, et al. Gastritis OLGA-staging & gastric cancer risk: a twelve year clinico-pathological follow-up study. Aliment Pharmacol Ther. 2010;31:1104-1111.
16. Ford AC, Forman D, Hunt RH, Yuan Y, Moayyedi P. Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: systematic review and meta-analysis of randomised controlled trials. BMJ. 2014;348:g3174.
17. Lee YC, Chiang TH, Chou CK, et al. Association between Helicobacter pylori eradication and gastric cancer incidence: a systematic review and meta-analysis. Gastroenterology. 2016;150:1113-1124.e5.
18. Fock KM. Review article: the epidemiology and prevention of gastric cancer. Aliment Pharmacol Ther. 2014;40:250-260.
19. Nardone G, Staibano S, Rocco A, et al. Effect of Helicobacter pylori infection and its eradication on cell proliferation, DNA status, and oncogene expression in patients with chronic gastritis. Gut. 1999;44:789-799.
20. Orihara T, Wakabayashi H, Nakaya A, et al. Effect of Helicobacter pylori eradication on gastric mucosal phospholipid content and its fatty acid composition. J Gastroenterol Hepatol. 2001;16:269-275.
21. Xia HH, Talley NJ. Apoptosis in gastric epithelium induced by Helicobacter pylori infection: implications in gastric carcinogenesis. Am J Gastroenterol. 2001;96:16-26.
22. Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical guideline: treatment of Helicobacter pylori infection. Am J Gastroenterol. 2017;112:212-239.
23. Park JM, Hahm KB. The Korean perspective of Helicobacter pylori infection: lessons from the Japanese government’s policy to prevent gastric cancer. Dig Dis. 2014;32:290-294.
24. Chey WD. Helicobacter pylori. Curr Treat Options Gastroenterol. 1999;2:171-182.
25. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process-First American cancer society award lecture on cancer epidemiology and prevention. Cancer Res. 1992;52:6735-6740.
26. Kamada T, Hata J, Sugiu K, et al. Clinical features of gastric cancer discovered after successful eradication of Helicobacter pylori: results from a 9-year prospective follow-up study in Japan. Aliment Pharmacol Ther. 2005;21:1121-1126.
27. Meining A, Morgner A, Miehlke S, Bayerdorffer E, Stolte M. Atrophy-metaplasia-dysplasia-carcinoma sequence in the stomach: a reality or merely an hypothesis? Best Pract Res Clin Gastroenterol. 2001;15:983-998.
28. Park YH, Kim N. Review of atrophic gastritis and intestinal metaplasia as a premalignant lesion of gastric cancer. J Cancer Prev. 2015;20:25-40.
29. Correa P. A human model of gastric carcinogenesis. Cancer Res. 1988;48:3554-3560.
30. Wong BC, Lam SK, Wong WM, et al. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA. 2004;291:187-194.
31. 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. 1997;92:1844-1848.
32. Sung JJ, Lin SR, Ching JY, et al. Atrophy and intestinal metaplasia one year after cure of H. pylori infection: a prospective, randomized study. Gastroenterology. 2000;119:7-14.
33. Leung WK, Lin SR, Ching JY, et al. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut. 2004;53:1244-1249.
34. Kodama M, Okimoto T, Ogawa R, Mizukami K, Murakami K. Endoscopic atrophic classification before and after H. pylori eradication is closely associated with histological atrophy and intestinal metaplasia. Endosc Int Open. 2015;3:E311-7.
35. Lu B, Chen MT, Fan YH, Liu Y, Meng LN. Effects of Helicobacter pylori eradication on atrophic gastritis and intestinal metaplasia: a 3-year follow-up study. World J Gastroenterol. 2005;11:6518-6520.
36. Malfertheiner P, Megraud F, O’Morain CA, et al. Management of Helicobacter pylori infection-the Maastricht IV/Florence Consensus Report. Gut. 2012;61:646-664.
37. Zhou L, Sung JJ, Lin S, et al. A five-year follow-up study on the pathological changes of gastric mucosa after H. pylori eradication. Chin Med J (Engl). 2003;116:11-14.
38. Cho SJ, Choi IJ, Kook MC, et al. Randomised clinical trial: the effects of Helicobacter pylori eradication on glandular atrophy and intestinal metaplasia after subtotal gastrectomy for gastric cancer. Aliment Pharmacol Ther. 2013;38:477-489.
39. Kiriyama Y, Tahara T, Shibata T, et al. Gastric-and-intestinal mixed intestinal metaplasia is irreversible point with eradication of Helicobacter pylori. O J Pathol. 2016;6:93.
40. Kang JM, Kim N, Shin CM, et al. Predictive factors for improvement of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication: a three-year follow-up study in Korea. Helicobacter. 2012;17:86-95.
41. Lahner E, Bordi C, Cattaruzza MS, et al. Long-term follow-up in atrophic body gastritis patients: atrophy and intestinal metaplasia are persistent lesions irrespective of Helicobacter pylori infection. Aliment Pharmacol Ther. 2005;22:471-481.
42. World Medical Association Declaration of Helsinki. Ethical principles for medical research involving human subjects. Nurs Ethics. 2002;9:105-109.
43. Dinis-Ribeiro M, Kuipers EJ. Identification of gastric atrophic changes: from histopathology to endoscopy. Endoscopy. 2015;47:533-537.
44. Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161-1181.
45. Kim SE, Park YS, Kim N, et al. Effect of Helicobacter pylori eradication on functional dyspepsia. J Neurogastroenterol Motil. 2013;19:233-243.
46. Wang YK, Kuo FC, Liu CJ, et al. Diagnosis of Helicobacter pylori infection: current options and developments. World J Gastroenterol. 2015;21:11221-11235.
47. Kiyohira K, Yoshihara M, Ito M, Haruma K, Tanaka S, Chayama K. Serum pepsinogen concentration as a marker of Helicobacter pylori infection and the histologic grade of gastritis; evaluation of gastric mucosa by serum pepsinogen levels. J Gastroenterol. 2003;38:332-338.
48. Huang RG, Xiao HL, Zhou B, et al. Serum pepsinogen levels are correlated with age, sex and the level of Helicobacter pylori infection in healthy individuals. Am J Med Sci. 2016;352:481-486.
49. Kang JM, Kim N, Yoo JY, et al. The role of serum pepsinogen and gastrin test for the detection of gastric cancer in Korea. Helicobacter. 2008;13:146-156.
50. Kim HJ, Kim N, Yoon H, et al. Comparison between resectable Helicobacter pylori-negative and-positive gastric cancers. Gut Liv. 2016;10:212-219.
51. Calvet X, Ramirez Lazaro MJ, Lehours P, Megraud F. Diagnosis and epidemiology of Helicobacter pylori infection. Helicobacter. 2013;18:5-11.
52. Lash JG, Genta RM. Adherence to the Sydney system guidelines increases the detection of Helicobacter gastritis and intestinal metaplasia in 400738 sets of gastric biopsies. Aliment Pharmacol Ther. 2013;38:424-431.
53. Rugge M, Correa P, Dixon MF, et al. Gastric mucosal atrophy: interobserver consistency using new criteria for classification and grading. Aliment Pharmacol Ther. 2002;16:1249-1259.
54. Lee JY, Kim N, Kim MS, et al. Factors affecting first-line triple therapy of Helicobacter pylori including CYP2C19 genotype and antibiotic resistance. Dig Dis Sci. 2014;59:1235-1243.
55. Gisbert JP, Calvet X. Review article: the effectiveness of standard triple therapy for Helicobacter pylori has not changed over the last decade, but it is not good enough. Aliment Pharmacol Ther. 2011;34:1255-1268.
56. Lee JW, Kim N, Kim JM, et al. A comparison between 15-day sequential, 10-day sequential and proton pump inhibitor-based triple therapy for Helicobacter pylori infection in Korea. Scand J Gastroenterol. 2014;49:917-924.
57. Huang J, Zhou L, Geng L, et al. Randomised controlled trial: sequential vs. standard triple therapy for Helicobacter pylori infection in Chinese children-a multicentre, open-labelled study. Aliment Pharmacol Ther. 2013;38:1230-1235.
58. Rokkas T, Pistiolas D, Sechopoulos P, Robotis I, Margantinis G. The long-term impact of Helicobacter pylori eradication on gastric histology: a systematic review and meta-analysis. Helicobacter. 2007; 12:32-38.
59. Salih BA, Abasiyanik MF, Saribasak H, Huten O, Sander E. A followup study on the effect of Helicobacter pylori eradication on the severity of gastric histology. Dig Dis Sci. 2005;50:1517-1522.
60. Pittayanon R, Rerknimitr R, Klaikaew N, et al. The risk of gastric cancer in patients with gastric intestinal metaplasia in 5-year follow-up. Aliment Pharmacol Ther. 2017;46:40-45.
61. Wang J, Xu L, Shi R, et al. Gastric atrophy and intestinal metaplasia before and after Helicobacter pylori eradication: a meta-analysis. Digestion. 2011;83:253-260.
62. Kong YJ, Yi HG, Dai JC, Wei MX. Histological changes of gastric mucosa after Helicobacter pylori eradication: a systematic review and meta-analysis. World J Gastroenterol. 2014;20:5903-5911.
63. de Vries AC, Kuipers EJ, Rauws EA. Helicobacter pylori eradication and gastric cancer: when is the horse out of the barn? Am J Gastroenterol. 2009;104:1342-1345.
64. Correa P, Houghton J. Carcinogenesis of Helicobacter pylori. Gastroenterology. 2007;133:659-672.
65. Sonnenberg A. Review article: historic changes of Helicobacter pyloriassociated diseases. Aliment Pharmacol Ther. 2013;38:329-342.
66. Houghton J, Stoicov C, Nomura S, et al. Gastric cancer originating from bone marrow-derived cells. Science. 2004;306:1568-1571.
67. Houghton J, Wang TC. Helicobacter pylori and gastric cancer: a new paradigm for inflammation-associated epithelial cancers. Gastroenterology. 2005;128:1567-1578.
68. Kim N, Park YS, Cho SI, et al. Prevalence and risk factors of atrophic gastritis and intestinal metaplasia in a Korean population without significant gastroduodenal disease. Helicobacter. 2008;13:245-255.
69. Shin CM, Kim N, Chang H, Kim JS, Lee DH, Jung HC. Follow-up study on CDX1 and CDX2 mRNA expression in noncancerous gastric mucosae after Helicobacter pylori eradication. Dig Dis Sci. 2016;61:1051-1059.
70. Leung WK, Sung JJ. Pathogenesis of pre-neoplastic lesions of the stomach: targets for prevention. Dig Dis. 2004;22:306-312.
71. Kang JM, Lee BH, Kim N, et al. CDX1 and CDX2 expression in intestinal metaplasia, dysplasia and gastric cancer. J Korean Med Sci. 2011;26:647-653.
72. Hong SJ, Sung IK, Kim JG, et al. Failure of a randomized, doubleblind, placebo-controlled study to evaluate the efficacy of H. pylori eradication in H. pylori-infected patients with functional dyspepsia. Gut. Liver. 2011;5:468-471.
73. Lee JY, Kim N, Nam RH, et al. No correlation of inflammation with colonization of Helicobacter pylori in the stomach of mice fed highsalt diet. J Cancer Preven. 2014;19:144-151.
74. Hiroi S, Sugano K, Tanaka S, Kawakami K. Impact of health insurance coverage for Helicobacter pylori gastritis on the trends in eradication therapy in Japan: retrospective observational study and simulation study based on real-world data. BMJ Open 2017;7: e015855.