{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,21]],"date-time":"2026-07-21T03:20:13Z","timestamp":1784604013878,"version":"3.55.0"},"reference-count":21,"publisher":"Wiley","issue":"1","license":[{"start":{"date-parts":[[2025,2,26]],"date-time":"2025-02-26T00:00:00Z","timestamp":1740528000000},"content-version":"vor","delay-in-days":56,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000288","name":"Royal Society","doi-asserted-by":"publisher","award":["RGS\\R2\\192312"],"award-info":[{"award-number":["RGS\\R2\\192312"]}],"id":[{"id":"10.13039\/501100000288","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000289","name":"Cancer Research UK","doi-asserted-by":"publisher","award":["EDDPMA\u2010Nov21\\100008"],"award-info":[{"award-number":["EDDPMA\u2010Nov21\\100008"]}],"id":[{"id":"10.13039\/501100000289","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Helicobacter"],"published-print":{"date-parts":[[2025,1]]},"abstract":"ABSTRACT<\/jats:title>\n \n Background<\/jats:title>\n \n Stomach cancer is the fourth leading cause of cancer\u2010related deaths worldwide.\n \n Helicobacter pylori<\/jats:italic>\n <\/jats:styled-content>\n is the main risk factor for gastric adenocarcinoma (GAC), yet the precise mechanism underpinning this association remains controversial. Gastric intestinal metaplasia (GIM) represents the precancerous stage and follows\n \n H.\u2009pylori<\/jats:styled-content>\n \u2010\n <\/jats:italic>\n associated chronic gastritis (CG). Sequencing studies have revealed fewer\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n and more non\u2010\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n bacteria in GAC. However, the spatial organization of the gastric microbiota in health and disease is unknown.\n <\/jats:p>\n <\/jats:sec>\n \n Materials and Methods<\/jats:title>\n \n Here, we have combined RNA in\u00a0situ hybridization and immunohistochemistry to detect\n \n H.\u2009pylori<\/jats:styled-content>\n ,\n <\/jats:italic>\n non\u2010\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n bacteria, and host cell markers (E\u2010cadherin, Mucins 5AC and 2) on tissue sections from patients with CG (\n n<\/jats:italic>\n \u2009=\u200915) and GIM (\n n<\/jats:italic>\n \u2009=\u200917).\n <\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n \n Quantitative analysis of whole slide scans revealed significant correlations of\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n and other bacteria in CG and GIM. In contrast to sequencing studies, significantly fewer non\u2010\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n bacteria were detected in\n \n H.\u2009pylori<\/jats:styled-content>\n \u2010\n <\/jats:italic>\n negative patients. Importantly, whilst\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n exclusively colonized the gastric glands, non\u2010\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n bacteria invaded the lamina propria in 6\/9 CG and 8\/10 GIM\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n \u2010positive patients. A rapid and cost\u2010effective modified Gram stain was used to confirm these findings and enabled detection of non\u2010\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n bacteria in GIM samples.\n <\/jats:p>\n <\/jats:sec>\n \n Conclusions<\/jats:title>\n \n The invasion of the gastric lamina propria by non\u2010\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n bacteria during\n \n H.\u2009pylori<\/jats:styled-content>\n \u2010\n <\/jats:italic>\n associated CG and GIM represents an overlooked phenomenon in cancer progression. Further work must determine the mechanisms underlying the synergistic roles of\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n and other bacteria in carcinogenesis. This observation should redirect attempts to prevent, diagnose, and treat GAC.\n <\/jats:p>\n <\/jats:sec>","DOI":"10.1111\/hel.70016","type":"journal-article","created":{"date-parts":[[2025,3,12]],"date-time":"2025-03-12T04:02:50Z","timestamp":1741752170000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["The Gastric Microbiota Invade the Lamina Propria in\n Helicobacter pylori<\/i>\n \u2010Associated Gastritis and Precancer"],"prefix":"10.1111","volume":"30","author":[{"given":"Harriet J.","family":"Giddings","sequence":"first","affiliation":[{"name":"Institute of Microbiology and Infection University of Birmingham Birmingham UK"},{"name":"Department of Microbes, Infection and Microbiomes, School of Infection, Inflammation and Immunology, College of Medicine and Health University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"Teod\u00f3sio","sequence":"additional","affiliation":[{"name":"Birmingham Tissue Analytics, University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jordanne","family":"Jones","sequence":"additional","affiliation":[{"name":"Birmingham Tissue Analytics, University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jack L.","family":"McMurray","sequence":"additional","affiliation":[{"name":"Birmingham Tissue Analytics, University of Birmingham Birmingham UK"},{"name":"Rheumatology Research Group University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kelly","family":"Hunter","sequence":"additional","affiliation":[{"name":"Birmingham Tissue Analytics, University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Riad","family":"Alame","sequence":"additional","affiliation":[{"name":"Queen Elizabeth Hospital University Hospital Birmingham NHS Foundation Trust Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isaac","family":"Gardiner","sequence":"additional","affiliation":[{"name":"Institute of Microbiology and Infection University of Birmingham Birmingham UK"},{"name":"Department of Microbes, Infection and Microbiomes, School of Infection, Inflammation and Immunology, College of Medicine and Health University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zainab","family":"Abdawn","sequence":"additional","affiliation":[{"name":"Queen Elizabeth Hospital University Hospital Birmingham NHS Foundation Trust Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William","family":"Butterworth","sequence":"additional","affiliation":[{"name":"Department of Immunology and Immunotherapy, School of Infection, Inflammation and Immunology, College of Medicine and Health University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ian R.","family":"Henderson","sequence":"additional","affiliation":[{"name":"Institute for Molecular Biosciences University of Queensland Brisbane Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffrey A.","family":"Cole","sequence":"additional","affiliation":[{"name":"Institute of Microbiology and Infection University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claire D.","family":"Shannon\u2010Lowe","sequence":"additional","affiliation":[{"name":"Department of Immunology and Immunotherapy, School of Infection, Inflammation and Immunology, College of Medicine and Health University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8567-7998","authenticated-orcid":false,"given":"Amanda E.","family":"Rossiter\u2010Pearson","sequence":"additional","affiliation":[{"name":"Institute of Microbiology and Infection University of Birmingham Birmingham UK"},{"name":"Department of Microbes, Infection and Microbiomes, School of Infection, Inflammation and Immunology, College of Medicine and Health University of Birmingham Birmingham UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2025,2,26]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"publisher","DOI":"10.3322\/caac.21660"},{"key":"e_1_2_9_3_1","doi-asserted-by":"publisher","DOI":"10.1053\/j.gastro.2023.12.022"},{"issue":"24","key":"e_1_2_9_4_1","first-page":"6735","article-title":"Human Gastric Carcinogenesis: A Multistep and Multifactorial 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