{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,5]],"date-time":"2026-11-05T20:09:22Z","timestamp":1793909362414,"version":"4.8.0"},"reference-count":40,"publisher":"BMJ","issue":"7","funder":[{"name":"Office of Medical Research, Department of Veterans Affairs, USA"},{"DOI":"10.13039\/100000054","name":"National Cancer Institute","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Pasto Cancer Registry, Centro de Estudios en Salud, Universidad de Nari\u00f1o"},{"name":"Intramural Research Program, U.S. National Institutes of Health, National Cancer Institute"}],"content-domain":{"domain":["bmj.com"],"crossmark-restriction":true},"short-container-title":["Gut"],"accepted":{"date-parts":[[2017,4,30]]},"published-print":{"date-parts":[[2018,7]]},"abstract":"<jats:sec>\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>\n                      To evaluate the long-term effect of cumulative time exposed to\n                      <jats:italic>Helicobacter pylori<\/jats:italic>\n                      infection on the progression of gastric lesions.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Design<\/jats:title>\n                    <jats:p>\n                      795 adults with precancerous gastric lesions were randomised to receive anti-\n                      <jats:italic>H. pylori<\/jats:italic>\n                      treatment at baseline. Gastric biopsies were obtained at baseline and at 3, 6, 12 and 16 years. A total of 456 individuals attended the 16-year visit. Cumulative time of\n                      <jats:italic>H. pylori<\/jats:italic>\n                      exposure was calculated as the number of years infected during follow-up. Multivariable logistic regression models were used to estimate the risk of progression to a more advanced diagnosis (versus no change\/regression) as well as gastric cancer risk by intestinal metaplasia (IM) subtype. For a more detailed analysis of progression, we also used a histopathology score assessing both severity and extension of the gastric lesions (range 1\u20136). The score difference between baseline and 16 years was modelled by generalised linear models.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Individuals who were continuously infected with\n                      <jats:italic>H. pylori<\/jats:italic>\n                      for 16 years had a higher probability of progression to a more advanced diagnosis than those who cleared the infection and remained negative after baseline (p=0.001). Incomplete-type IM was associated with higher risk of progression to cancer than complete-type (OR, 11.3; 95% CI 1.4 to 91.4). The average histopathology score increased by 0.20 units\/year (95%\u2009CI 0.12 to 0.28) among individuals continuously infected with\n                      <jats:italic>H. pylori<\/jats:italic>\n                      . The effect of cumulative time of infection on progression in the histopathology score was significantly higher for individuals with atrophy (without IM) than for individuals with IM (p&lt;0.001).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>\n                      Long-term exposure to\n                      <jats:italic>H. pylori<\/jats:italic>\n                      infection was associated with progression of precancerous lesions. Individuals infected with\n                      <jats:italic>H. pylori<\/jats:italic>\n                      with these lesions may benefit from eradication, particularly those with atrophic gastritis without IM. Incomplete-type IM may be a useful marker for the identification of individuals at higher risk for cancer.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1136\/gutjnl-2016-311685","type":"journal-article","created":{"date-parts":[[2017,6,24]],"date-time":"2017-06-24T20:20:17Z","timestamp":1498335617000},"page":"1239-1246","update-policy":"https:\/\/doi.org\/10.1136\/crossmarkpolicy","source":"Crossref","is-referenced-by-count":165,"title":["Dynamics of\n                    <i>Helicobacter pylori<\/i>\n                    infection as a determinant of progression of gastric precancerous lesions: 16-year follow-up of an eradication trial"],"prefix":"10.1136","volume":"67","author":[{"given":"Robertino M","family":"Mera","sequence":"first","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luis E","family":"Bravo","sequence":"additional","affiliation":[{"name":"Department of Pathology, Universidad del Valle School of Medicine, Cali, Colombia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M Constanza","family":"Camargo","sequence":"additional","affiliation":[{"name":"Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan C","family":"Bravo","sequence":"additional","affiliation":[{"name":"Department of Pathology, Universidad del Valle School of Medicine, Cali, Colombia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alberto G","family":"Delgado","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Judith","family":"Romero-Gallo","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria C","family":"Yepez","sequence":"additional","affiliation":[{"name":"Centro de Estudios en Salud, Universidad de Nari\u00f1o, Pasto, Colombia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jos\u00e9 L","family":"Realpe","sequence":"additional","affiliation":[{"name":"Centro de Estudios en Salud, Universidad de Nari\u00f1o, Pasto, Colombia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Barbara G","family":"Schneider","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Douglas R","family":"Morgan","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"suffix":"Jr","given":"Richard M","family":"Peek","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"},{"name":"Department of Cancer Biology, Vanderbilt University Medical Center, Nashville, Tennessee, USA"},{"name":"Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pelayo","family":"Correa","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Keith T","family":"Wilson","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"},{"name":"Department of Cancer Biology, Vanderbilt University Medical Center, Nashville, Tennessee, USA"},{"name":"Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee, USA"},{"name":"Center for Mucosal Inflammation and Cancer, Vanderbilt University Medical Center, Nashville, Tennessee, USA"},{"name":"Veterans Affairs Tennessee Valley Healthcare System, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M Blanca","family":"Piazuelo","sequence":"additional","affiliation":[{"name":"Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee, USA"},{"name":"Center for Mucosal Inflammation and Cancer, Vanderbilt University Medical Center, Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"239","published-online":{"date-parts":[[2017,6,24]]},"reference":[{"key":"2025121302314035000_67.7.1239.1","first-page":"177","article-title":"IARC working group on the evaluation of carcinogenic risks to humans. Schistosomes, liver flukes and Helicobacter pylori","volume":"61","year":"1994","journal-title":"IARC Monogr Eval Carcinog Risks Hum"},{"key":"2025121302314035000_67.7.1239.2","first-page":"6735","article-title":"Human gastric carcinogenesis: a multistep and multifactorial process\u2014first American Cancer Society award lecture on cancer epidemiology and prevention","volume":"52","author":"Correa","year":"1992","journal-title":"Cancer Res"},{"key":"2025121302314035000_67.7.1239.3","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(75)90498-5"},{"key":"2025121302314035000_67.7.1239.4","first-page":"4737","article-title":"Gastric precancerous process in a high risk population: cohort follow-up","volume":"50","author":"Correa","year":"1990","journal-title":"Cancer Res"},{"key":"2025121302314035000_67.7.1239.5","doi-asserted-by":"publisher","DOI":"10.1053\/j.gastro.2008.01.071"},{"key":"2025121302314035000_67.7.1239.6","doi-asserted-by":"publisher","DOI":"10.1136\/bmj.h3867"},{"key":"2025121302314035000_67.7.1239.7","doi-asserted-by":"publisher","DOI":"10.1016\/j.gtc.2013.02.001"},{"key":"2025121302314035000_67.7.1239.8","doi-asserted-by":"publisher","DOI":"10.1136\/gut.2003.034629"},{"key":"2025121302314035000_67.7.1239.9","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/djj264"},{"key":"2025121302314035000_67.7.1239.10","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/djs003"},{"key":"2025121302314035000_67.7.1239.11","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/dju116"},{"key":"2025121302314035000_67.7.1239.12","doi-asserted-by":"publisher","DOI":"10.1001\/jama.291.2.187"},{"key":"2025121302314035000_67.7.1239.13","doi-asserted-by":"publisher","DOI":"10.1053\/j.gastro.2016.01.028"},{"key":"2025121302314035000_67.7.1239.14","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/92.23.1881"},{"key":"2025121302314035000_67.7.1239.15","doi-asserted-by":"publisher","DOI":"10.1136\/gut.2005.072009"},{"key":"2025121302314035000_67.7.1239.16","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1179\/his.1985.8.1.15","article-title":"Modified Steiner for the demonstration of spirochetes","volume":"8","author":"Garvey","year":"1985","journal-title":"J Histotechnol"},{"key":"2025121302314035000_67.7.1239.17","doi-asserted-by":"publisher","DOI":"10.1007\/BF01002633"},{"key":"2025121302314035000_67.7.1239.18","first-page":"231","article-title":"Distribution of marker enzymes and mucin in intestinal metaplasia in human stomach and relation to complete and incomplete types of intestinal metaplasia to minute gastric carcinomas","volume":"65","author":"Matsukura","year":"1980","journal-title":"J Natl Cancer Inst"},{"key":"2025121302314035000_67.7.1239.19","doi-asserted-by":"publisher","DOI":"10.1038\/ajg.2009.728"},{"key":"2025121302314035000_67.7.1239.20","unstructured":"Lauwers GY , Franceschi S , Carneiro F , et al . Gastric carcinoma. In: Bosman FT , Carneiro F , Hruban RH , eds. WHO classification of tumours of the digestive system. 4th ed. Lyon: International Agency for Research on Cancer (IARC), 2010:48\u201358."},{"key":"2025121302314035000_67.7.1239.21","doi-asserted-by":"publisher","DOI":"10.1097\/00000478-199610000-00001"},{"key":"2025121302314035000_67.7.1239.22","doi-asserted-by":"publisher","DOI":"10.1097\/00000478-200002000-00001"},{"key":"2025121302314035000_67.7.1239.23","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1318093111"},{"key":"2025121302314035000_67.7.1239.24","doi-asserted-by":"publisher","DOI":"10.1016\/j.gie.2009.12.029"},{"key":"2025121302314035000_67.7.1239.25","doi-asserted-by":"publisher","DOI":"10.1016\/j.dld.2008.02.030"},{"key":"2025121302314035000_67.7.1239.26","doi-asserted-by":"publisher","DOI":"10.1111\/j.1572-0241.2007.01393.x"},{"key":"2025121302314035000_67.7.1239.27","doi-asserted-by":"publisher","DOI":"10.1136\/gutjnl-2016-312288"},{"key":"2025121302314035000_67.7.1239.28","doi-asserted-by":"publisher","DOI":"10.1136\/gutjnl-2015-309252"},{"key":"2025121302314035000_67.7.1239.29","doi-asserted-by":"publisher","DOI":"10.1053\/j.gastro.2005.02.066"},{"key":"2025121302314035000_67.7.1239.30","doi-asserted-by":"publisher","DOI":"10.1158\/0008-5472.CAN-07-6786"},{"key":"2025121302314035000_67.7.1239.31","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/dju148"},{"key":"2025121302314035000_67.7.1239.32","doi-asserted-by":"publisher","DOI":"10.1136\/gutjnl-2012-302240"},{"key":"2025121302314035000_67.7.1239.33","first-page":"297","article-title":"Carcinoma and intestinal metaplasia of the stomach in colombian migrants","volume":"44","author":"Correa","year":"1970","journal-title":"J Natl Cancer Inst"},{"key":"2025121302314035000_67.7.1239.34","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejca.2010.12.012"},{"key":"2025121302314035000_67.7.1239.35","doi-asserted-by":"crossref","first-page":"1104","DOI":"10.1111\/j.1365-2036.2010.04277.x","article-title":"Gastritis OLGA-staging and gastric cancer risk: a twelve-year clinico-pathological follow-up study","volume":"31","author":"Rugge","year":"2010","journal-title":"Aliment Pharmacol Ther"},{"key":"2025121302314035000_67.7.1239.36","doi-asserted-by":"publisher","DOI":"10.1136\/gut.2006.106666"},{"key":"2025121302314035000_67.7.1239.37","doi-asserted-by":"publisher","DOI":"10.1002\/ijc.2910570306"},{"key":"2025121302314035000_67.7.1239.38","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1111\/jgh.13249","article-title":"Incomplete type of intestinal metaplasia has the highest risk to progress to gastric cancer: results of the Spanish follow-up multicenter study","volume":"31","author":"Gonz\u00e1lez","year":"2016","journal-title":"J Gastroenterol Hepatol"},{"key":"2025121302314035000_67.7.1239.39","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1002\/ijc.28003","article-title":"Utility of subtyping intestinal metaplasia as marker of gastric cancer risk. A review of the evidence","volume":"133","author":"Gonz\u00e1lez","year":"2013","journal-title":"Int J Cancer"},{"key":"2025121302314035000_67.7.1239.40","doi-asserted-by":"publisher","DOI":"10.1016\/j.humpath.2010.12.017"}],"container-title":["Gut"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1136\/gutjnl-2016-311685","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,13]],"date-time":"2025-12-13T10:31:51Z","timestamp":1765621911000},"score":1,"resource":{"primary":{"URL":"https:\/\/gut.bmj.com\/lookup\/doi\/10.1136\/gutjnl-2016-311685"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,6,24]]},"references-count":40,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2018,6,7]]},"published-print":{"date-parts":[[2018,7]]}},"alternative-id":["10.1136\/gutjnl-2016-311685"],"URL":"https:\/\/doi.org\/10.1136\/gutjnl-2016-311685","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.727748722.793546691","asserted-by":"object"}]},"ISSN":["0017-5749","1468-3288"],"issn-type":[{"value":"0017-5749","type":"print"},{"value":"1468-3288","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,6,24]]}}}