{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T04:52:46Z","timestamp":1791175966549,"version":"4.1.0"},"reference-count":38,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T00:00:00Z","timestamp":1791072000000},"content-version":"vor","delay-in-days":33,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"},{"start":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T00:00:00Z","timestamp":1788220800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/100008700","name":"Centre International de Recherche sur le Cancer","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008700","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Helicobacter"],"published-print":{"date-parts":[[2026,9]]},"abstract":"ABSTRACT<\/jats:title>\n \n Background<\/jats:title>\n \n Characterizing the epidemiology of\n \n Helicobacter pylori<\/jats:italic>\n <\/jats:styled-content>\n (\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n ) infection and gastric atrophy (GA) is essential for informing preventive strategies in anticipation of the rising gastric cancer burden. The International Agency for Research on Cancer has initiated global studies to characterize these epidemiological patterns using a standardized framework, including in Uganda.\n <\/jats:p>\n <\/jats:sec>\n \n Materials and Methods<\/jats:title>\n \n This population\u2010based study included 700 individuals aged 1\u201369\u2009years, randomly selected from the General Population Cohort in rural Uganda, stratified by sex and age. Participants completed a structured questionnaire to assess risk factors related to\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n infection and GA, underwent anthropometric measurements, and provided blood samples. Anti\u2010\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n IgG antibodies were measured using enzyme\u2010linked immunosorbent assays (ELISA). In individuals aged \u2265\u200940\u2009years, plasma pepsinogen I (PG I) and pepsinogen II (PG II) concentrations were measured by ELISA to define gastric atrophy.\n <\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n \n The age\u2010standardized\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n seroprevalence was 76%. The crude seroprevalence was 63% in children aged 1\u20139\u2009years, rose to over 80% in individuals aged 10\u201339\u2009years, and then declined modestly in older age groups (73% in individuals aged \u2265\u200940). Men aged \u2265\u200940\u2009years had a lower\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n seroprevalence compared to women aged \u2265\u200940\u2009years (68% vs. 78%,\n p<\/jats:italic>\n \u2009<\u20090.05). Serologically defined GA was uncommon, with an overall prevalence of 6% (17\/301; 95% CI: 3%\u20139%) among individuals aged \u2265\u200940\u2009years. Obesity (aOR 6.0, 95% CI 1.6\u201320.9) and less than daily chili consumption (aOR 4.3, 95% CI 1.4\u201314.9) were associated with higher odds of GA among participants aged \u2265\u200940\u2009years, after adjustment for age and sex.\n <\/jats:p>\n <\/jats:sec>\n \n Conclusions<\/jats:title>\n \n In this population\u2010based study in rural southwestern Uganda,\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n infection was acquired early in life and was highly prevalent, whereas serologically defined gastric atrophy remained relatively uncommon. This distinct epidemiological pattern warrants further validation and investigation.\n <\/jats:p>\n <\/jats:sec>","DOI":"10.1111\/hel.70163","type":"journal-article","created":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T04:22:24Z","timestamp":1791174144000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Epidemiology of\n \n Helicobacter pylori<\/i>\n <\/scp>\n and Gastric Atrophy in Rural Southwestern Uganda: The\n ENIGMA<\/scp>\n Uganda Study"],"prefix":"10.1111","volume":"31","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0864-8990","authenticated-orcid":false,"given":"Yue","family":"Huang","sequence":"first","affiliation":[{"name":"Early Detection, Prevention and Infections Branch International Agency for Research on Cancer (IARC\/WHO) Lyon France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9646-2052","authenticated-orcid":false,"given":"Viktoria","family":"Knaze","sequence":"additional","affiliation":[{"name":"Early Detection, Prevention and Infections Branch International Agency for Research on Cancer (IARC\/WHO) Lyon France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph","family":"Mugisha","sequence":"additional","affiliation":[{"name":"Uganda Research Unit MRC\/UVRI and LSHTM Entebbe Uganda"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-9854-1114","authenticated-orcid":false,"given":"Anne\u2010Sophie","family":"Navionis","sequence":"additional","affiliation":[{"name":"Nutrition and Metabolism Branch International Agency for Research on Cancer Lyon France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6846-1204","authenticated-orcid":false,"given":"Sabina","family":"Rinaldi","sequence":"additional","affiliation":[{"name":"Nutrition and Metabolism Branch International Agency for Research on Cancer Lyon France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7534-333X","authenticated-orcid":false,"given":"Gary M.","family":"Clifford","sequence":"additional","affiliation":[{"name":"Early Detection, Prevention and Infections Branch International Agency for Research on Cancer (IARC\/WHO) Lyon France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2491-5099","authenticated-orcid":false,"given":"Jin Young","family":"Park","sequence":"additional","affiliation":[{"name":"Early Detection, Prevention and Infections Branch International Agency for Research on Cancer (IARC\/WHO) Lyon France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert","family":"Newton","sequence":"additional","affiliation":[{"name":"Uganda Research Unit MRC\/UVRI and LSHTM Entebbe Uganda"},{"name":"University of York York UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,10,4]]},"reference":[{"issue":"3","key":"e_1_2_11_2_1","first-page":"229","article-title":"Global Cancer Statistics 2022: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries","volume":"74","author":"Bray F.","year":"2024","journal-title":"CA: A Cancer Journal for Clinicians"},{"key":"e_1_2_11_3_1","unstructured":"International Agency for Research on Cancer \u201cGlobal Cancer Observatory\u201d(2025) https:\/\/gco.iarc.who.int\/en."},{"issue":"5","key":"e_1_2_11_4_1","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1038\/s41571-023-00747-0","article-title":"Global Burden of Gastric Cancer: Epidemiological Trends, Risk Factors, Screening and Prevention","volume":"20","author":"Thrift A. P.","year":"2023","journal-title":"Nature Reviews. Clinical Oncology"},{"issue":"9","key":"e_1_2_11_5_1","doi-asserted-by":"crossref","first-page":"3020","DOI":"10.1038\/s41591-025-03793-6","article-title":"Global Lifetime Estimates of Expected and Preventable Gastric Cancers Across 185 Countries","volume":"31","author":"Park J. Y.","year":"2025","journal-title":"Nature Medicine"},{"issue":"24","key":"e_1_2_11_6_1","first-page":"6735","article-title":"Human Gastric Carcinogenesis: A Multistep and Multifactorial Process \u2013 First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention","volume":"52","author":"Correa P.","year":"1992","journal-title":"Cancer Research"},{"issue":"1","key":"e_1_2_11_7_1","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1172\/JCI30111","article-title":"Inflammation, Atrophy, and Gastric Cancer","volume":"117","author":"Fox J. G.","year":"2007","journal-title":"Journal of Clinical Investigation"},{"issue":"7","key":"e_1_2_11_8_1","doi-asserted-by":"crossref","first-page":"1090","DOI":"10.1111\/j.1572-0241.1998.00335.x","article-title":"Correlation of Ratio of Serum Pepsinogen I and II With Prevalence of Gastric Cancer and Adenoma in Japanese Subjects","volume":"93","author":"Yoshihara M.","year":"1998","journal-title":"American Journal of Gastroenterology"},{"issue":"4","key":"e_1_2_11_9_1","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1007\/s10120-006-0397-0","article-title":"Gastric Cancer Screening Using the Serum Pepsinogen Test Method","volume":"9","author":"Miki K.","year":"2006","journal-title":"Gastric Cancer"},{"issue":"1","key":"e_1_2_11_10_1","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1159\/000441742","article-title":"Gastric Cancer Screening by Combined Assay for Serum Anti\u2010\n Helicobacter pylori\n IgG Antibody and Serum Pepsinogen Levels\u2013The ABC Method","volume":"93","author":"Yamaguchi Y.","year":"2016","journal-title":"Digestion"},{"issue":"7","key":"e_1_2_11_11_1","doi-asserted-by":"crossref","first-page":"405","DOI":"10.2183\/pjab.87.405","article-title":"Gastric Cancer Screening by Combined Assay for Serum Anti\u2010\n Helicobacter pylori\n IgG Antibody and Serum Pepsinogen Levels\u2013ABC Method","volume":"87","author":"Miki K.","year":"2011","journal-title":"Proceedings of the Japan Academy. Series B, Physical and Biological Sciences"},{"key":"e_1_2_11_12_1","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1186\/1471-230X-10-62","article-title":"Helicobacter pylori\n In Apparently Healthy Children Aged 0\u201012\u2009Years in Urban Kampala, Uganda: A Community\u2010Based Cross Sectional Survey","volume":"10","author":"Hestvik E.","year":"2010","journal-title":"BMC Gastroenterology"},{"issue":"1","key":"e_1_2_11_13_1","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.trstmh.2011.09.001","article-title":"The Seroprevalence of Helicobacter Pylori and Its Relationship to Malaria in Ugandan Children","volume":"106","author":"Gupta V.","year":"2012","journal-title":"Transactions of the Royal Society of Tropical Medicine and Hygiene"},{"key":"e_1_2_11_14_1","doi-asserted-by":"crossref","DOI":"10.1186\/s13104-015-1184-y","article-title":"Prevalence of \n Helicobacter pylori\n in Dyspeptic Patients at a Tertiary Hospital in a Low Resource Setting","volume":"8","author":"Oling M.","year":"2015","journal-title":"BMC Research Notes"},{"issue":"2","key":"e_1_2_11_15_1","doi-asserted-by":"crossref","first-page":"135","DOI":"10.4314\/ahs.v22i2.16","article-title":"Prevalence and Factors Associated With \n Helicobacter pylori\n Infection Among Children With Sickle Cell Anemia Attending Mulago Hospital, in Uganda","volume":"22","author":"Mubiru I. S.","year":"2022","journal-title":"African Health Sciences"},{"key":"e_1_2_11_16_1","doi-asserted-by":"crossref","DOI":"10.1186\/1471-2458-14-915","article-title":"Helicobacter pylori\n Infection in Pregnant Women in Four Districts of Uganda: Role of Geographic Location, Education and Water Sources","volume":"14","author":"Baingana R. K.","year":"2014","journal-title":"BMC Public Health"},{"issue":"8","key":"e_1_2_11_17_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pntd.0001780","article-title":"Common Coinfections of Giardia Intestinalis and \n Helicobacter pylori\n in Non\u2010Symptomatic Ugandan Children","volume":"6","author":"Ankarklev J.","year":"2012","journal-title":"PLoS Neglected Tropical Diseases"},{"key":"e_1_2_11_18_1","doi-asserted-by":"crossref","DOI":"10.1155\/2019\/9303072","article-title":"Prevalence and Risk Factors of \n Helicobacter pylori\n Infection Among Children Aged 1 to 15\u2009Years at Holy Innocents Children's Hospital, Mbarara, South Western Uganda","volume":"2019","author":"Aitila P.","year":"2019","journal-title":"Journal of Tropical Medicine"},{"issue":"1","key":"e_1_2_11_19_1","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1007\/s42770-023-01190-0","article-title":"Prevalence and Associated Risk Factors of \n Helicobacter pylori\n Infection in East Africa: A Systematic Review and Meta\u2010Analysis","volume":"55","author":"Mnichil Z.","year":"2024","journal-title":"Brazilian Journal of Microbiology"},{"issue":"3","key":"e_1_2_11_20_1","doi-asserted-by":"crossref","first-page":"222","DOI":"10.23736\/S1121-421X.18.02464-9","article-title":"Helicobacter pylori\n Infection in Africa: 2018 Literature Update","volume":"64","author":"Smith S. I.","year":"2018","journal-title":"Minerva Gastroenterologica e Dietologica"},{"issue":"9","key":"e_1_2_11_21_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0237515","article-title":"Regional Variations in \n Helicobacter pylori\n Infection, Gastric Atrophy and Gastric Cancer Risk: The ENIGMA Study in Chile","volume":"15","author":"Herrero R.","year":"2020","journal-title":"PLoS One"},{"issue":"1","key":"e_1_2_11_22_1","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1093\/ije\/dys234","article-title":"The General Population Cohort in Rural South\u2010Western Uganda: A Platform for Communicable and Non\u2010Communicable Disease Studies","volume":"42","author":"Asiki G.","year":"2013","journal-title":"International Journal of Epidemiology"},{"key":"e_1_2_11_23_1","volume-title":"National Population and Housing Census 2024: Final Report","author":"Uganda Bureau of Statistics","year":"2024"},{"issue":"10431","key":"e_1_2_11_24_1","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1016\/S0140-6736(23)02750-2","article-title":"Worldwide Trends in Underweight and Obesity From 1990 to 2022: A Pooled Analysis of 3663 Population\u2010Representative Studies With 222 Million Children, Adolescents, and Adults","volume":"403","author":"NCD Risk Factor Collaboration (NCD\u2010RisC)","year":"2024","journal-title":"Lancet"},{"key":"e_1_2_11_25_1","unstructured":"World Health Organization \u201cBody Mass Index\u2010for\u2010Age (BMI\u2010for\u2010Age)\u201d(2026) https:\/\/www.who.int\/toolkits\/child\u2010growth\u2010standards\/standards\/body\u2010mass\u2010index\u2010for\u2010age\u2010bmi\u2010for\u2010aged."},{"issue":"3","key":"e_1_2_11_26_1","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1080\/02841860701843035","article-title":"Different Etiological Role of \n Helicobacter pylori\n (Hp) Infection in Carcinogenesis Between Differentiated and Undifferentiated Gastric Cancers: A Nested Case\u2010Control Study Using IgG Titer Against Hp Surface Antigen","volume":"47","author":"Tatemichi M.","year":"2008","journal-title":"Acta Oncologica"},{"issue":"8","key":"e_1_2_11_27_1","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.1086\/343808","article-title":"Helicobacter pylori\n CagA Seropositivity and Gastric Carcinoma Risk in a Japanese American Population","volume":"186","author":"Nomura A. M.","year":"2002","journal-title":"Journal of Infectious Diseases"},{"issue":"3","key":"e_1_2_11_28_1","doi-asserted-by":"crossref","DOI":"10.1111\/hel.13096","article-title":"Nationwide Survey of \n Helicobacter pylori\n Seropositivity and Gastric Atrophy in Zambia","volume":"29","author":"Kayamba V.","year":"2024","journal-title":"Helicobacter"},{"issue":"1","key":"e_1_2_11_29_1","doi-asserted-by":"crossref","DOI":"10.3892\/mco.2023.2649","article-title":"Trends in the Prevalence of Atrophic Gastritis and \n Helicobacter pylori\n Infection Over a 10\u2010Year Period in Japan: The ROAD Study 2005\u20102015","volume":"19","author":"Inoue I.","year":"2023","journal-title":"Molecular and Clinical Oncology"},{"key":"e_1_2_11_30_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.canep.2022.102309","article-title":"Prevalence and Factors Associated With Atrophic Gastritis and Intestinal Metaplasia: A Multivariate, Hospital\u2010Based, Statistical Analysis","volume":"82","author":"Chitapanarux T.","year":"2023","journal-title":"Cancer Epidemiology"},{"issue":"3","key":"e_1_2_11_31_1","doi-asserted-by":"crossref","first-page":"259","DOI":"10.3109\/00365521.2013.869352","article-title":"Serum Anti\u2010\n Helicobacter pylori\n Immunoglobulin G Titer Correlates With Grade of Histological Gastritis, Mucosal Bacterial Density, and Levels of Serum Biomarkers","volume":"49","author":"Tu H.","year":"2014","journal-title":"Scandinavian Journal of Gastroenterology"},{"issue":"5","key":"e_1_2_11_32_1","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1007\/s10120-025-01629-3","article-title":"Positive Association Between Anti\u2010\n Helicobacter pylori\n IgG Antibody Titers and Atrophic Gastritis in a Latvian Cohort","volume":"28","author":"Lim J. H.","year":"2025","journal-title":"Gastric Cancer"},{"issue":"5","key":"e_1_2_11_33_1","doi-asserted-by":"crossref","DOI":"10.14309\/ctg.0000000000000833","article-title":"Nomogram Prediction for Gastric Cancer Development","volume":"16","author":"Lim J. H.","year":"2025","journal-title":"Clinical and Translational Gastroenterology"},{"key":"e_1_2_11_34_1","doi-asserted-by":"crossref","DOI":"10.1155\/2015\/156719","article-title":"Helicobacter pylori\n Antibody Titer and Gastric Cancer Screening","volume":"2015","author":"Kishikawa H.","year":"2015","journal-title":"Disease Markers"},{"issue":"2","key":"e_1_2_11_35_1","doi-asserted-by":"crossref","DOI":"10.1111\/hel.12463","article-title":"Seroprevalence of \n Helicobacter pylori\n in Korea: A Multicenter, Nationwide Study Conducted in 2015 and 2016","volume":"23","author":"Lee J. H.","year":"2018","journal-title":"Helicobacter"},{"key":"e_1_2_11_36_1","volume-title":"Population\u2010Based Helicobacter pylori Screen\u2010and\u2010Treat Strategies for Gastric Cancer Prevention: Guidance on Implementation","author":"International Agency for Research on Cancer","year":"2025"},{"issue":"1","key":"e_1_2_11_37_1","doi-asserted-by":"crossref","DOI":"10.1186\/s12876-024-03187-x","article-title":"Endoscopic Diagnosis of Gastric and Oesophageal Cancer in Lusaka, Zambia: A Retrospective Analysis","volume":"24","author":"Kayamba V.","year":"2024","journal-title":"BMC Gastroenterology"},{"issue":"12","key":"e_1_2_11_38_1","doi-asserted-by":"crossref","DOI":"10.1016\/S2214-109X(20)30358-2","article-title":"Burden of Non\u2010Communicable Diseases From Infectious Causes in 2017: A Modelling Study","volume":"8","author":"Coates M. M.","year":"2020","journal-title":"Lancet Global Health"},{"issue":"5","key":"e_1_2_11_39_1","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1007\/s00394-023-03132-w","article-title":"Association Between Salt Intake and Gastric Atrophy by \n Helicobacter pylori\n Infection: First Results From the Epidemiological Investigation of Gastric Malignancy (ENIGMA)","volume":"62","author":"Knaze V.","year":"2023","journal-title":"European Journal of Nutrition"}],"container-title":["Helicobacter"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/hel.70163","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/hel.70163","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/hel.70163","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T04:22:32Z","timestamp":1791174152000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/hel.70163"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9]]},"references-count":38,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2026,9]]}},"alternative-id":["10.1111\/hel.70163"],"URL":"https:\/\/doi.org\/10.1111\/hel.70163","archive":["Portico"],"relation":{},"ISSN":["1083-4389","1523-5378"],"issn-type":[{"value":"1083-4389","type":"print"},{"value":"1523-5378","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9]]},"assertion":[{"value":"2026-06-16","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-08-31","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-10-04","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e70163"}}