{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,30]],"date-time":"2026-03-30T03:07:12Z","timestamp":1774840032684,"version":"3.50.1"},"reference-count":47,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2022,2,23]],"date-time":"2022-02-23T00:00:00Z","timestamp":1645574400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Diagnostics"],"abstract":"<jats:p>Duodenogastric reflux (DGR) causes bile reflux gastritis (BRG) and may develop into gastric cancer. DGR is classified as primary in non-operated stomachs or secondary to surgical intervention. Primary DGR and Helicobacter pylori (H. pylori) infection are reportedly related. However, the mechanism is not fully understood. This study aimed to elucidate the relationship between H. pylori infection and pyloric incompetence in a non-operated stomach. A total of 502 non-operated participants who underwent an upper intestinal endoscopy were prospectively enrolled. Endoscopic findings (EAC, endoscopic atrophy classification; nodular gastritis; xanthoma; fundic gland polyp; and incompetence of pylorus), sex, age, gastrin, pepsinogen (PG) I and PG II levels were evaluated. PG I\/PG II ratio, anti-H. pylori-Ab positivity, and atrophic gastritis status were significantly different between the normal and incompetent pylori (p = 0.043, &lt;0.001, and 0.001, respectively). Open-type atrophic gastritis was significantly higher in the incompetent pylori. Incompetence of the pylorus and EAC were moderately correlated (Cramer\u2019s V = 0.25). Multivariate analysis revealed that the presence of anti-H. pylori-Ab was the only independent factor associated with the incompetence of the pylorus, with an adjusted odds ratio of 2.70 (95% CI: 1.47\u20134.94, p = 0.001). In conclusion, pyloric incompetence was associated with H. pylori infection and moderately correlated to the severity of atrophic gastritis in non-operated stomachs.<\/jats:p>","DOI":"10.3390\/diagnostics12030572","type":"journal-article","created":{"date-parts":[[2022,2,23]],"date-time":"2022-02-23T09:34:38Z","timestamp":1645608878000},"page":"572","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Pyloric Incompetence Associated with Helicobactor pylori Infection and Correlated to the Severity of Atrophic Gastritis"],"prefix":"10.3390","volume":"12","author":[{"given":"Takuki","family":"Sakaguchi","sequence":"first","affiliation":[{"name":"Department of Gastroenterology and Nephrology, Faculty of Medicine, Tottori University, Yonago 683-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0522-1884","authenticated-orcid":false,"given":"Takaaki","family":"Sugihara","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Nephrology, Faculty of Medicine, Tottori University, Yonago 683-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7091-5244","authenticated-orcid":false,"given":"Ken","family":"Ohnita","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Nagasaki University Hospital, Nagasaki 852-8501, Japan"},{"name":"Shunkaikai Inoue Hospital, Nagasaki 850-0045, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daisuke","family":"Fukuda","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Nagasaki University Hospital, Nagasaki 852-8501, Japan"},{"name":"Department of Surgical Oncology, Graduate School of Biological Sciences, Nagasaki University, Nagasaki 852-8501, Japan"},{"name":"Fukuda Yutaka Clinic, Nagasaki 852-8107, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tetsuro","family":"Honda","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Nagasaki Harbor Medical Center, Nagasaki 850-8555, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ryohei","family":"Ogihara","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Nephrology, Faculty of Medicine, Tottori University, Yonago 683-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hiroki","family":"Kurumi","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Nephrology, Faculty of Medicine, Tottori University, Yonago 683-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kazuo","family":"Yashima","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Nephrology, Faculty of Medicine, Tottori University, Yonago 683-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hajime","family":"Isomoto","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Nephrology, Faculty of Medicine, Tottori University, Yonago 683-8504, Japan"},{"name":"Department of Gastroenterology, Nagasaki University Hospital, Nagasaki 852-8501, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,2,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1007\/s11605-008-0754-x","article-title":"Hiatal hernia, lower esophageal sphincter incompetence, and effectiveness of nissen fundoplication in the spectrum of gastroesophageal reflux disease","volume":"13","author":"Lord","year":"2009","journal-title":"J. Gastrointest. Surg."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1007\/BF02208607","article-title":"Fiberoptic technique for 24-hour bile reflux monitoring: Standards and normal values for gastric monitoring","volume":"41","author":"Fein","year":"1996","journal-title":"Dig. Dis. Sci."},{"key":"ref_3","first-page":"796","article-title":"Clinical value of endoscopy and histology in the diagnosis of duodenogastric reflux disease","volume":"112","author":"Stein","year":"1992","journal-title":"Surgery"},{"key":"ref_4","first-page":"40","article-title":"Importance of duodeno-gastro-esophageal reflux in the medical outpatient practice","volume":"46","author":"Vaezi","year":"1999","journal-title":"Hepatogastroenterology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1016\/0016-5085(81)90498-4","article-title":"Duodenogastric reflux in humans: Its relationship to fasting antroduodenal motility and gastric, pancreatic, and biliary secretion","volume":"81","author":"Keane","year":"1981","journal-title":"Gastroenterology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"103168","DOI":"10.1016\/j.amsu.2021.103168","article-title":"Bile reflux gastropathy: Prevalence and risk factors after therapeutic biliary interventions: A retrospective cohort study","volume":"72","author":"Othman","year":"2021","journal-title":"Ann. Med. Surg."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"400","DOI":"10.5056\/jnm20102","article-title":"Bile reflux gastropathy and functional dyspepsia","volume":"27","author":"Lake","year":"2021","journal-title":"J. Neurogastroenterol. Motil."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1136\/gut.38.1.15","article-title":"Helicobacter pylori may induce bile reflux: Link between H. pylori and bile induced injury to gastric epithelium","volume":"38","author":"Ladas","year":"1996","journal-title":"Gut"},{"key":"ref_9","first-page":"2352","article-title":"The results of the surgical treatment of alkaline reflux gastritis","volume":"59","author":"Tireli","year":"2012","journal-title":"Hepatogastroenterology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1016\/S0039-6060(99)70198-4","article-title":"Gastric symptoms and duodenogastric reflux in patients referred for gastroesophageal reflux symptoms and endoscopic esophagitis","volume":"125","author":"Romagnoli","year":"1999","journal-title":"Surgery"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1111\/apt.12031","article-title":"Reactive gastropathy is associated with inflammatory conditions throughout the gastrointestinal tract","volume":"36","author":"Maguilnik","year":"2012","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/S0002-9343(01)00827-0","article-title":"Duodenogastroesophageal reflux and methods to monitor nonacidic reflux","volume":"111","author":"Vaezi","year":"2001","journal-title":"Am. J. Med."},{"key":"ref_13","first-page":"59","article-title":"The effect of laparoscopic cholecystectomy on the development of alkaline reflux gastritis and intestinal metaplasia","volume":"59","author":"Atak","year":"2012","journal-title":"Hepatogastroenterology"},{"key":"ref_14","first-page":"269","article-title":"Endoscopical and histological features in bile reflux gastritis","volume":"46","author":"Vere","year":"2005","journal-title":"Rom. J. Morphol. Embryol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"758771","DOI":"10.3389\/fmed.2021.758771","article-title":"Analysis of risk factors and establishment of a prediction model for endoscopic primary bile reflux: A single-center retrospective study","volume":"8","author":"Chen","year":"2021","journal-title":"Front. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1136\/gut.14.7.555","article-title":"Pyloric reflux and the healing of gastric ulcers","volume":"14","author":"Cocking","year":"1973","journal-title":"Gut"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1007\/s00431-003-1259-y","article-title":"Primary duodenogastric reflux in children and adolescents","volume":"162","author":"Hermans","year":"2003","journal-title":"Eur. J. Pediatr."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0016-5085(68)80001-0","article-title":"Destruction of the gastric mucosal barrier by detergents and urea","volume":"54","author":"Davenport","year":"1968","journal-title":"Gastroenterology"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0016-5085(19)33895-8","article-title":"Increased reflux of bile into the stomach in patients with gastric ulcer","volume":"57","author":"Rhodes","year":"1969","journal-title":"Gastroenterology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/BF01072064","article-title":"The incompetent pyloric sphincter. Bile and mucosal ulceration","volume":"21","author":"Rovelstad","year":"1976","journal-title":"Am. J. Dig. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1136\/gut.11.9.735","article-title":"Pyloric regurgitation and gastric ulcer","volume":"11","author":"Flint","year":"1970","journal-title":"Gut"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1136\/bmj.3.5875.313","article-title":"Effect of cigarette smoking on competence of the pylorus: Preliminary study","volume":"3","author":"Read","year":"1973","journal-title":"BMJ"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/S0016-5085(76)80481-7","article-title":"Manometric studies on the human pyloric sphincter: Effect of cigarette smoking, metoclopramide, and atropine","volume":"70","author":"Valenzuela","year":"1976","journal-title":"Gastroenterology"},{"key":"ref_24","first-page":"645","article-title":"On pyloric sphincter incompetence in man","volume":"59","author":"Code","year":"1970","journal-title":"Gastroenterology"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1007\/BF02233838","article-title":"Antral motility in patients with gastric ulcer","volume":"11","author":"Garrett","year":"1966","journal-title":"Am. J. Dig. Dis."},{"key":"ref_26","first-page":"1273","article-title":"Unidentified curved bacilli on gastric epithelium in active chronic gastritis","volume":"1","author":"Warren","year":"1983","journal-title":"Lancet"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1111\/1751-2980.12858","article-title":"The relationship between gastric cancer, its precancerous lesions and bile reflux: A retrospective study","volume":"21","author":"Li","year":"2020","journal-title":"J. Dig. Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"766","DOI":"10.3892\/etm.2021.10198","article-title":"Helicobacter pylori infection over bile reflux: No influence on the severity of endoscopic or premalignant gastric lesion development","volume":"22","author":"Mocan","year":"2021","journal-title":"Exp. Ther. Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"E139","DOI":"10.1055\/s-0043-120830","article-title":"Deep learning analyzes Helicobacter pylori infection by upper gastrointestinal endoscopy images","volume":"6","author":"Itoh","year":"2018","journal-title":"Endosc. Int. Open"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"4061","DOI":"10.3748\/wjg.v24.i35.4061","article-title":"Serum anti-Helicobacter pylori antibody titer and its association with gastric nodularity, atrophy, and age: A cross-sectional study","volume":"24","author":"Toyoshima","year":"2018","journal-title":"World J. Gastroenterol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Terasawa, T., Nishida, H., Kato, K., Miyashiro, I., Yoshikawa, T., Takaku, R., and Hamashima, C. (2014). Prediction of gastric cancer development by serum pepsinogen test and Helicobacter pylori seropositivity in eastern Asians: A systematic review and meta-analysis. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0109783"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1093\/gastro\/gov004","article-title":"Hypergastrinemia","volume":"3","author":"Dacha","year":"2015","journal-title":"Gastroenterol. Rep."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1111\/j.1572-0241.2000.01704.x","article-title":"H. pylori in the pathogenesis of duodenal ulcer: Interaction between duodenal acid load, bile, and H. pylori","volume":"95","author":"Graham","year":"2000","journal-title":"Am. J. Gastroenterol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1136\/jcp.46.3.235","article-title":"Bile reflux and intestinal metaplasia in gastric mucosa","volume":"46","author":"Sobala","year":"1993","journal-title":"J. Clin. Pathol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1111\/den.12030","article-title":"Relation between bile acid reflux into the stomach and the risk of atrophic gastritis and intestinal metaplasia: A multicenter study of 2283 cases","volume":"25","author":"Matsuhisa","year":"2013","journal-title":"Dig. Endosc."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1053\/j.gastro.2021.06.078","article-title":"AGA clinical practice update on the diagnosis and management of atrophic gastritis: Expert review","volume":"161","author":"Shah","year":"2021","journal-title":"Gastroenterology"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1007\/s11894-020-00775-1","article-title":"Current perspectives in atrophic gastritis","volume":"22","author":"Lahner","year":"2020","journal-title":"Curr. Gastroenterol. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1158\/1940-6207.CAPR-19-0238","article-title":"Smoking, Helicobacter pylori serology, and gastric cancer risk in prospective studies from China, Japan, and Korea","volume":"12","author":"Butt","year":"2019","journal-title":"Cancer Prev. Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1111\/jgh.15177","article-title":"Endoscopic grading of gastric atrophy on risk assessment of gastric neoplasia: A systematic review and meta-analysis","volume":"36","author":"Xiao","year":"2021","journal-title":"J. Gastroenterol. Hepatol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1581","DOI":"10.1111\/jgh.13764","article-title":"Association between gastric cancer and the Kyoto classification of gastritis","volume":"32","author":"Shichijo","year":"2017","journal-title":"J. Gastroenterol. Hepatol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1159\/000368807","article-title":"Relationship between the degree of endoscopic atrophy of the gastric mucosa and carcinogenic risk","volume":"91","author":"Masuyama","year":"2015","journal-title":"Digestion"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"\u00d6ztekin, M., Y\u0131lmaz, B., A\u011fag\u00fcnd\u00fcz, D., and Capasso, R. (2021). Overview of Helicobacter pylori infection: Clinical features, treatment, and nutritional aspects. Diseases, 9.","DOI":"10.3390\/diseases9040066"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1590\/s0004-2803.202100000-85","article-title":"Helicobacter pylori cagA virulence gene and severe esogastroduodenal diseases: Is there an association?","volume":"54","author":"Oliveira","year":"2021","journal-title":"Arq. Gastroenterol."},{"key":"ref_44","first-page":"72","article-title":"Is a bile reflux an additional cancerogenic factor in peptic ulcer, associated with Helicobacter pylori infection?","volume":"49","author":"Vdovychenko","year":"2004","journal-title":"Rocz. Akad. Med. Bialymst."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1053\/j.gastro.2017.04.022","article-title":"Global prevalence of Helicobacter pylori infection: Systematic review and meta-analysis","volume":"153","author":"Hooi","year":"2017","journal-title":"Gastroenterology"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1111\/den.13486","article-title":"Validity of endoscopic features for the diagnosis of Helicobacter pylori infection status based on the Kyoto classification of gastritis","volume":"32","author":"Yoshii","year":"2020","journal-title":"Dig. Endosc."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Lim, H.-J., Kim, H.D., Soh, J.S., Kim, S.-Y., Jung, Y.-J., Lim, H., Kang, H.S., and Kim, J.H. (2021). Discrete terminal ileal ulcers in patients diagnosed with ulcerative colitis: Clinical significance and natural course. BMC Gastroenterol., 21.","DOI":"10.1186\/s12876-021-01866-7"}],"container-title":["Diagnostics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4418\/12\/3\/572\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:26:07Z","timestamp":1760135167000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4418\/12\/3\/572"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,23]]},"references-count":47,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2022,3]]}},"alternative-id":["diagnostics12030572"],"URL":"https:\/\/doi.org\/10.3390\/diagnostics12030572","relation":{},"ISSN":["2075-4418"],"issn-type":[{"value":"2075-4418","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,23]]}}}