{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T04:52:29Z","timestamp":1791175949116,"version":"4.1.0"},"reference-count":35,"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:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"},{"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"}],"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 Non\u2010\n \n Helicobacter pylori<\/jats:styled-content>\n Helicobacter\n <\/jats:italic>\n (NHPH) species are increasingly recognized as human gastric colonizers, yet their prevalence, species distribution, and clinical significance remain incompletely defined, particularly in patient cohorts in the Middle East.\n <\/jats:p>\n <\/jats:sec>\n \n Materials and Methods<\/jats:title>\n \n In this retrospective study, 830 formalin\u2010fixed paraffin\u2010embedded gastric biopsy samples collected from patients undergoing esophagogastroduodenoscopy at Tzafon Medical Center, northern Israel, between 2022 and 2024 were subjected to species\u2010specific PCR for\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n and NHPH species. Clinical, demographic, histopathological, and endoscopic data were correlated with PCR\u2010defined infection status.\n <\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n \n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n was detected in 643\/830 (77.5%), whereas at least one NHPH species was detected in 179 samples (21.6%).\n \n H. bizzozeronii<\/jats:italic>\n <\/jats:styled-content>\n was the predominant NHPH species, identified in 167\/830 samples (20.1%), while\n \n H.\u2009heilmannii<\/jats:italic>\n <\/jats:styled-content>\n ,\n \n H.\u2009felis<\/jats:italic>\n <\/jats:styled-content>\n , and\n H<\/jats:italic>\n .\u2009\n ailurogastricus<\/jats:italic>\n were rare (<\u20091%), and\n \n H.\u2009suis<\/jats:italic>\n <\/jats:styled-content>\n and\n \n H.\u2009salomonis<\/jats:italic>\n <\/jats:styled-content>\n were not detected. Co\u2010infection with\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n was common (18.2%), and was detected in 23.5% of all\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n \u2010positive samples and 84.4% of NHPH\u2010positive samples. NHPH prevalence was higher in females and demonstrated marked seasonality, peaking in autumn. Histopathological comparison showed a significant difference in foveolar hyperplasia rates across infection groups, with higher frequencies in NHPH\u2010only and PCR detected negative for all species samples than in\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n \u2010positive groups. In contrast, clinical symptoms and endoscopic findings were broadly comparable across infection strata.\n <\/jats:p>\n <\/jats:sec>\n \n Conclusions<\/jats:title>\n \n These findings provide the first large\u2010scale molecular characterization of gastric NHPH in Israel and show that NHPH, predominantly\n \n H.\u2009bizzozeronii<\/jats:italic>\n <\/jats:styled-content>\n , is relatively common in this population, is usually co\u2010detected with\n \n H.\u2009pylori<\/jats:italic>\n <\/jats:styled-content>\n , and is associated more strongly with distinct epidemiologic and histopathologic patterns than with a distinct clinical or endoscopic phenotype.\n <\/jats:p>\n <\/jats:sec>","DOI":"10.1111\/hel.70165","type":"journal-article","created":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T04:27:07Z","timestamp":1791174427000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Beyond\n Helicobacter pylori<\/i>\n : Prevalence, Coinfection, and Clinicopathologic Patterns of Non\u2010\n Helicobacter pylori Helicobacter<\/i>\n (NHPH) in Human Gastric Biopsies"],"prefix":"10.1111","volume":"31","author":[{"given":"Daniel","family":"Vizenblit","sequence":"first","affiliation":[{"name":"Azrieli Faculty of Medicine Bar Ilan University Safed Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0966-2575","authenticated-orcid":false,"given":"Maya","family":"Azrad","sequence":"additional","affiliation":[{"name":"Clinical Microbiology Laboratory Tzafon Medical Center, Poriya, Israel, Affiliated with Azriely Faculty of Medicine, Bar Ilan University Poriya Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Munir","family":"Nashashibi","sequence":"additional","affiliation":[{"name":"Clinical Microbiology Laboratory Tzafon Medical Center, Poriya, Israel, Affiliated with Azriely Faculty of Medicine, Bar Ilan University Poriya Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Halim","family":"Roshrosh","sequence":"additional","affiliation":[{"name":"Clinical Microbiology Laboratory Tzafon Medical Center, Poriya, Israel, Affiliated with Azriely Faculty of Medicine, Bar Ilan University Poriya Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0005-1847","authenticated-orcid":false,"given":"Yaakov","family":"Maman","sequence":"additional","affiliation":[{"name":"Azrieli Faculty of Medicine Bar Ilan University Safed Israel"},{"name":"Laboratory of Genomic Instability and Cancer, Azrieli Faculty of Medicine Bar\u2010Ilan University Safed Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Avi","family":"Peretz","sequence":"additional","affiliation":[{"name":"Azrieli Faculty of Medicine Bar Ilan University Safed Israel"},{"name":"Clinical Microbiology Laboratory Tzafon Medical Center, Poriya, Israel, Affiliated with Azriely Faculty of Medicine, Bar Ilan University Poriya Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,10,4]]},"reference":[{"issue":"1","key":"e_1_2_9_2_1","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/S2468-1253(19)30328-0","article-title":"The Global, Regional, and National Burden of Stomach Cancer in 195 Countries, 1990\u20132017: A Systematic Analysis for the Global Burden of Disease Study 2017","volume":"5","author":"Etemadi A.","year":"2020","journal-title":"Lancet Gastroenterology & Hepatology"},{"key":"e_1_2_9_3_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpubh.2023.1202980","article-title":"Global, Regional, and National Burden of Digestive Diseases: Findings From the Global Burden of Disease Study 2019","volume":"11","author":"Wang F.","year":"2023","journal-title":"Frontiers in Public Health"},{"issue":"1","key":"e_1_2_9_4_1","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1038\/s41572-023-00431-8","article-title":"Helicobacter pylori\n Infection","volume":"9","author":"Malfertheiner P.","year":"2023","journal-title":"Nature Reviews. 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F. B.","year":"2023","journal-title":"World Journal of Gastroenterology"},{"issue":"2","key":"e_1_2_9_13_1","doi-asserted-by":"crossref","DOI":"10.3390\/jpm12020181","article-title":"Presence of Helicobacter Species in Gastric Mucosa of Human Patients and Outcome of Helicobacter Eradication Treatment","volume":"12","author":"Matos R.","year":"2022","journal-title":"Journal of Personalized Medicine"},{"key":"e_1_2_9_14_1","article-title":"Review\u2014Non\u2010\n Helicobacter pylori\n Helicobacters","volume":"3","author":"M\u00e9nard A.","year":"2021","journal-title":"Microbiota in Health and Disease"},{"issue":"3","key":"e_1_2_9_15_1","doi-asserted-by":"crossref","DOI":"10.1111\/hel.70051","article-title":"Roles of Gastric Non\u2010\n Helicobacter pylori\n Helicobacter Species in Gastric Disease Development: A Review","volume":"30","author":"Sugimoto M.","year":"2025","journal-title":"Helicobacter"},{"issue":"2","key":"e_1_2_9_16_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.anpede.2025.503928","article-title":"Gastric \n Helicobacter heilmannii\n Infection","volume":"103","author":"G\u00f3mez S\u00e1nchez R.","year":"2025","journal-title":"Anales de Pediatr\u00eda (English Edition)"},{"issue":"5","key":"e_1_2_9_17_1","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1016\/S0016-5085(00)70167-3","article-title":"Helicobacter heilmannii\n \u2013Associated Primary Gastric Low\u2010Grade MALT Lymphoma: Complete Remission After Curing the Infection","volume":"118","author":"Morgner A.","year":"2000","journal-title":"Gastroenterology"},{"issue":"6","key":"e_1_2_9_18_1","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/j.amjms.2023.08.012","article-title":"No Significant Association Between Non\u2010\n Helicobacter pylori\n Helicobacter Infection With Gastritis\u2010Related Indices and Gastric Cancer","volume":"366","author":"Abuduwaili M.","year":"2023","journal-title":"American Journal of the Medical Sciences"},{"issue":"47","key":"e_1_2_9_19_1","doi-asserted-by":"crossref","first-page":"17779","DOI":"10.3748\/wjg.v20.i47.17779","article-title":"Helicobacter heilmannii\n Sensu Lato: An Overview of the Infection in Humans","volume":"20","author":"Bento\u2010Miranda M.","year":"2014","journal-title":"World Journal of Gastroenterology"},{"key":"e_1_2_9_20_1","doi-asserted-by":"crossref","first-page":"4370","DOI":"10.1002\/cam4.2314","article-title":"Helicobacter suis\n Infection Is Associated With Nodular Gastritis\u2010Like Appearance of Gastric Mucosa\u2010Associated Lymphoid Tissue Lymphoma","volume":"8","author":"Takigawa H.","year":"2019","journal-title":"Cancer Medicine"},{"issue":"4","key":"e_1_2_9_21_1","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1007\/s10120-021-01172-x","article-title":"Involvement of Non\u2010\n Helicobacter pylori\n Helicobacter Infections in \n Helicobacter pylori\n \u2010Negative Gastric MALT Lymphoma Pathogenesis and Efficacy of Eradication Therapy","volume":"24","author":"Takigawa H.","year":"2021","journal-title":"Gastric Cancer"},{"key":"e_1_2_9_22_1","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1111\/hel.12201","article-title":"Prevalence of Coinfection With Gastric Non\u2010\n Helicobacter pylori\n Helicobacter (NHPH) Species in \n Helicobacter pylori\n \u2010Infected Patients Suffering From Gastric Disease in Beijing, China","volume":"20","author":"Liu J.","year":"2014","journal-title":"Helicobacter"},{"issue":"6","key":"e_1_2_9_23_1","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.3201\/eid3106.241315","article-title":"Prospective Multicenter Surveillance of Non\u2010\n Helicobacter pylori\n Helicobacter Infections During Medical Checkups, Japan","volume":"31","author":"Tokunaga K.","year":"2025","journal-title":"Emerging Infectious Diseases"},{"key":"e_1_2_9_24_1","doi-asserted-by":"crossref","DOI":"10.3390\/microorganisms13071684","article-title":"Prevalence and Diagnostic Comparison of Helicobacter Pylori and Non\u2010\n Helicobacter pylori\n Helicobacter Infections in Patients Undergoing Upper Gastrointestinal Endoscopy With Gastric Biopsy in Algarve, Portugal","volume":"13","author":"Cortez Nunes F.","year":"2025","journal-title":"Microorganisms"},{"issue":"4","key":"e_1_2_9_25_1","doi-asserted-by":"crossref","DOI":"10.1111\/hel.12811","article-title":"Prevalence, Clinical Features, and Esophagogastroduodenoscopy (EGD) Findings of Non\u2010\n Helicobacter pylori\n Helicobacter Infection: A Study of 50 Cases at a Single Facility in Japan","volume":"26","author":"Tsukadaira T.","year":"2021","journal-title":"Helicobacter"},{"issue":"1","key":"e_1_2_9_26_1","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1292\/jvms.13-0223","article-title":"Determination of the Prevalence of \n Helicobacter heilmannii\n \u2010Like Organisms Type 2 (HHLO\u20102) Infection in Humans and Dogs Using Non\u2010Invasive Genus\/Species\u2010Specific PCR in Korea","volume":"76","author":"Chung T. H.","year":"2014","journal-title":"Journal of Veterinary Medical Science"},{"key":"e_1_2_9_27_1","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/s13567-022-01059-4","article-title":"Gastric Helicobacter Species Associated With Dogs, Cats and Pigs: Significance for Public and Animal Health","volume":"53","author":"Taillieu E.","year":"2022","journal-title":"Veterinary Research"},{"issue":"10","key":"e_1_2_9_28_1","doi-asserted-by":"crossref","DOI":"10.3390\/ani12101254","article-title":"Helicobacter Species and Their Association With Gastric Pathology in a Cohort of Dogs With Chronic Gastrointestinal Signs","volume":"12","author":"Husnik R.","year":"2022","journal-title":"Animals"},{"issue":"6","key":"e_1_2_9_29_1","doi-asserted-by":"crossref","first-page":"1036","DOI":"10.3201\/eid0706.010622","article-title":"A Cultured Strain of \n Helicobacter heilmannii\n , a Human Gastric Pathogen, Identified as \n H. bizzozeronii\n : Evidence for Zoonotic Potential of Helicobacter","volume":"7","author":"Jalava K.","year":"2001","journal-title":"Emerging Infectious Diseases"},{"key":"e_1_2_9_30_1","unstructured":"Ministry of Agriculture and Rural Development (Israel) \u201cMinistry of Agriculture Publishes the Statistics on Dogs in Israel 2021 \u201dJerusalem: Ministry of Agriculture and Rural Development (2022) cited March 28 2026 https:\/\/www.gov.il\/en\/pages\/ministry_of_agriculture_publishes_the_statistics_on_dogs_in_israel_2021."},{"issue":"3","key":"e_1_2_9_31_1","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1097\/00042737-199803000-00011","article-title":"Gastric Ulcers and \n Helicobacter heilmannii","volume":"10","author":"Debongnie J. 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L.","year":"2023","journal-title":"Digestive Medicine Research"}],"container-title":["Helicobacter"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/hel.70165","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/hel.70165","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/hel.70165","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T04:27:13Z","timestamp":1791174433000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/hel.70165"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9]]},"references-count":35,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2026,9]]}},"alternative-id":["10.1111\/hel.70165"],"URL":"https:\/\/doi.org\/10.1111\/hel.70165","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":"2026-04-23","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":"e70165"}}