{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T18:40:38Z","timestamp":1792089638107,"version":"4.4.0"},"reference-count":28,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2020,8,13]],"date-time":"2020-08-13T00:00:00Z","timestamp":1597276800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"name":"Japanese Society of Helicobacter Research"},{"name":"JSPS KAKENHI","award":["22590690"],"award-info":[{"award-number":["22590690"]}]},{"name":"JSPS KAKENHI","award":["23790155"],"award-info":[{"award-number":["23790155"]}]},{"name":"JSPS KAKENHI","award":["2159049"],"award-info":[{"award-number":["2159049"]}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Helicobacter"],"published-print":{"date-parts":[[2020,10]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background<\/jats:title><jats:p>The clinical significance of non\u2010<jats:italic>Helicobacter pylori<\/jats:italic> Helicobacter (NHPH) is still unknown. There are many reports of NHPH\u2010infected patients suffering from gastric diseases. Here, we investigated the polymerase chain reaction (PCR) positivity of NHPH infection in gastric disease patients who were negative for <jats:italic>H.\u00a0pylori<\/jats:italic> (Hp) by the rapid urease test and by pathological observation.<\/jats:p><\/jats:sec><jats:sec><jats:title>Materials and methods<\/jats:title><jats:p>We collected the 296 endoscopically obtained gastric mucosal samples of Hp\u2010negative gastric disease patients diagnosed based on a rapid urease test and pathology from 17 hospitals in Japan from September 2013 to June 2019, and we analyzed the existence of Hp and NHPH by PCR. The samples were also treated by indirect immunohistochemistry using an anti\u2010<jats:italic>Helicobacter suis<\/jats:italic> VacA paralog antibody and were observed by confocal laser microscopy.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Among the 236 non\u2010Hp\u2010eradicated cases, 49 cases (20.8%) were positive for NHPH. Among them, 20 cases were positive for <jats:italic>Helicobacter suis<\/jats:italic>, 7 cases were positive for <jats:italic>Helicobacter heilmannii<\/jats:italic> sensu stricto\/ <jats:italic>Helicobacter ailurogastricus<\/jats:italic> (Hhss\/Ha), and the other 22 cases could not be identified. The regional differences in the infection rates were significant. Forty percent of the nodular gastritis cases, 24% of the MALT lymphoma, 17% of the chronic gastritis cases, and 33% of the gastroduodenal ulcer cases were NHPH positive. Forty\u2010five patients had been treated with one of the four types of combinations of a proton pump inhibitor and two antibiotics, and in all of these cases, the NHPH diagnosed by PCR was successfully eradicated. Immunohistochemistry using the <jats:italic>Helicobacter suis<\/jats:italic>\u2010specific HsvA antibody coincided well with the PCR results. Among the 29 post\u2010Hp eradication cases, three were NHPH positive, including one Hhss\/Ha\u2010positive case. Thus, approx. 20% of the Hp\u2010negative non\u2010Hp\u2010eradicated gastric disease patients treated at 17 hospitals in Japan were infected with NHPH.<\/jats:p><\/jats:sec>","DOI":"10.1111\/hel.12700","type":"journal-article","created":{"date-parts":[[2020,8,13]],"date-time":"2020-08-13T19:28:00Z","timestamp":1597346880000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":52,"title":["PCR analysis and specific immunohistochemistry revealing a high prevalence of non\u2010<i>Helicobacter pylori<\/i> Helicobacters in <i>Helicobacter pylori<\/i>\u2010negative gastric disease patients in Japan: High susceptibility to an Hp eradication regimen"],"prefix":"10.1111","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4893-1552","authenticated-orcid":false,"given":"Masahiko","family":"Nakamura","sequence":"first","affiliation":[{"name":"School of Pharmacy Kitasato University Tokyo Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4054-5884","authenticated-orcid":false,"given":"Anders","family":"\u00d8verby","sequence":"additional","affiliation":[{"name":"Center of Education in Kongsvinger Kongsvinger Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hirofumi","family":"Michimae","sequence":"additional","affiliation":[{"name":"Department of Clinical Medicine (Biostatistics) School of Pharmacy Kitasato University Tokyo Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7791-2356","authenticated-orcid":false,"given":"Hidenori","family":"Matsui","sequence":"additional","affiliation":[{"name":"Kitasato Institute for Life Sciences Kitasato University Tokyo Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8598-8366","authenticated-orcid":false,"given":"Shinichi","family":"Takahashi","sequence":"additional","affiliation":[{"name":"School of Medicine Kyorin University Mitaka Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katsuhiro","family":"Mabe","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology National Hospital Organization Hakodate National Hospital Hakodate Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9615-0000","authenticated-orcid":false,"given":"Tadashi","family":"Shimoyama","sequence":"additional","affiliation":[{"name":"Aomori General Health Examination Center Aomori Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Makoto","family":"Sasaki","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology Aichi Medical University Nagakute Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuici","family":"Terao","sequence":"additional","affiliation":[{"name":"Kakogawa Central City Hospital Kakogawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomoari","family":"Kamada","sequence":"additional","affiliation":[{"name":"Department of Health Care Medicine Kawasaki Medical School Kurashiki Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7967-5665","authenticated-orcid":false,"given":"Akinori","family":"Yanaka","sequence":"additional","affiliation":[{"name":"University of Tsukuba Hitachi Medical Education and Research Center University of Tsukuda Hitachi Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junichi","family":"Iwamoto","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology Tokyo Medical University Ibaraki Medical Center Amicho Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi","family":"Tanabe","sequence":"additional","affiliation":[{"name":"Department of Advanced Medicine Research and Development Center for New Medical Frontiers Kitasato University School of Medicine Sagamihara Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Akira","family":"Tari","sequence":"additional","affiliation":[{"name":"Sixth Department of Internal Medicine Hiroshima Red Cross Hospital &amp; Atomic\u2010bomb Survivors Hospital Hiroshima Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shinji","family":"Nasu","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology Ikeikai Inobe Hospital Oita Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8994-6163","authenticated-orcid":false,"given":"Hidekazu","family":"Suzuki","sequence":"additional","affiliation":[{"name":"Division of Gastroenterology and Hepatology Department of Internal Medicine Tokai University School of Medicine Isehara Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0610-1211","authenticated-orcid":false,"given":"Somay","family":"Yamagata Murayama","sequence":"additional","affiliation":[{"name":"Laboratory of Medical Microbiology School of Pharmacy Nihon University Funabashi Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2020,8,13]]},"reference":[{"key":"e_1_2_8_2_1","first-page":"861","article-title":"Histologischer Nachweis von CLO (Campylobacter Like Organisms) in Magenbiopsien","volume":"112","author":"Heilmann KL","year":"1987","journal-title":"Dtsch med Wschr"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1136\/jcp.42.6.585"},{"key":"e_1_2_8_4_1","first-page":"245","article-title":"Gastritis associated with Gastrospirillum hominis\u2013A zoonosis?","volume":"121","author":"Wegmann W","year":"1991","journal-title":"Schweizerische Medizinische Wochenschrift"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1159\/000431169"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.2169\/internalmedicine.55.5891"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.2169\/internalmedicine.8971-17"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.1136\/gut.32.2.137"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01968031"},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.1023\/A:1018854513056"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.1111\/hel.12201"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1111\/hel.12511"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1440-1827.1998.tb03941.x"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.01459-06"},{"key":"e_1_2_8_15_1","doi-asserted-by":"publisher","DOI":"10.1128\/genomeA.00934-16"},{"key":"e_1_2_8_16_1","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.39.4.1217-1220.2001"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0732-8893(02)00547-3"},{"key":"e_1_2_8_18_1","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.01300-15"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.1099\/ijs.0.63117-0"},{"key":"e_1_2_8_20_1","first-page":"148","article-title":"Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy","volume":"35","author":"Zamboni L","year":"1967","journal-title":"J Cell Biol"},{"key":"e_1_2_8_21_1","first-page":"121","article-title":"Development of the rapid diagnostic methods of Helicobacter suis infection","volume":"21","author":"Matsui H","year":"2020","journal-title":"Jpn J Helicobacter Res"},{"key":"e_1_2_8_22_1","unstructured":"The Kitasato Institute et al.Method for diagnosis of Helicobacter suis infection (not yet published). 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