{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,6]],"date-time":"2026-05-06T14:14:40Z","timestamp":1778076880051,"version":"3.51.4"},"reference-count":78,"publisher":"SAGE Publications","license":[{"start":{"date-parts":[[2026,5,1]],"date-time":"2026-05-01T00:00:00Z","timestamp":1777593600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"},{"start":{"date-parts":[[2026,5,1]],"date-time":"2026-05-01T00:00:00Z","timestamp":1777593600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.sagepub.com\/page\/policies\/text-and-data-mining-license"}],"funder":[{"DOI":"10.13039\/501100012131","name":"department of science and technology of liaoning province","doi-asserted-by":"publisher","award":["2023JH2\/101700099"],"award-info":[{"award-number":["2023JH2\/101700099"]}],"id":[{"id":"10.13039\/501100012131","id-type":"DOI","asserted-by":"publisher"}]},{"name":"the Independent Research Funding of General Hospital of Northern Theater Command","award":["ZZKY2024018"],"award-info":[{"award-number":["ZZKY2024018"]}]}],"content-domain":{"domain":["journals.sagepub.com"],"crossmark-restriction":true},"short-container-title":["Therap Adv Gastroenterol"],"published-print":{"date-parts":[[2026,5]]},"abstract":"<jats:sec>\n                    <jats:title>Background:<\/jats:title>\n                    <jats:p>\n                      Multiple meta-analyses have evaluated the effect of\n                      <jats:italic toggle=\"yes\">Helicobacter pylori<\/jats:italic>\n                      (\n                      <jats:italic toggle=\"yes\">H. pylori<\/jats:italic>\n                      ) infection on the risk of inflammatory bowel disease (IBD), but their findings remain inconsistent.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Objectives:<\/jats:title>\n                    <jats:p>\n                      To critically assess the existing meta-analyses regarding the effect of\n                      <jats:italic toggle=\"yes\">H. pylori<\/jats:italic>\n                      infection on the risk of IBD.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Data sources and methods:<\/jats:title>\n                    <jats:p>\n                      We systematically searched four electronic databases and manually screened the reference lists of relevant articles. A Measurement Tool to Assess systematic Reviews 2 (AMSTAR-2), Grade of Recommendation, Assessment, Development, and Evaluation (GRADE), and Graphical Representation of Overlap for OVErviews (GROOVE) tools were used to assess the methodological quality, evidence quality, and the overall overlap of primary studies among the included meta-analyses, respectively. A second-order meta-analysis was performed on primary studies derived from the included meta-analyses with very high overlap to explore the association of\n                      <jats:italic toggle=\"yes\">H. pylori<\/jats:italic>\n                      infection with IBD risk and identify the potential influencing factors. Risk ratios (RRs) were pooled.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results:<\/jats:title>\n                    <jats:p>\n                      Twelve meta-analyses encompassing 55 primary studies were included. The methodological quality was very low to low. The evidence quality was very low to high. Moderate- to high-quality evidence suggested that\n                      <jats:italic toggle=\"yes\">H. pylori<\/jats:italic>\n                      virulence factors and antibiotic exposure influenced the association of\n                      <jats:italic toggle=\"yes\">H. pylori<\/jats:italic>\n                      infection with IBD. The overall overlap of primary studies among the included meta-analyses was very high. A second-order meta-analysis demonstrated a negative association of\n                      <jats:italic toggle=\"yes\">H. pylori<\/jats:italic>\n                      infection with any type of IBD (RR: 0.60), Crohn\u2019s disease (RR: 0.53), ulcerative colitis (RR: 0.67), and IBD-unclassified (RR: 0.73). Subgroup analyses demonstrated that both IBD subtypes (\n                      <jats:italic toggle=\"yes\">P<\/jats:italic>\n                      <jats:sub>interaction<\/jats:sub>\n                      \u2009&lt;\u20090.01), regions (\n                      <jats:italic toggle=\"yes\">P<\/jats:italic>\n                      <jats:sub>interaction<\/jats:sub>\n                      \u2009&lt;\u20090.01), and study designs (\n                      <jats:italic toggle=\"yes\">P<\/jats:italic>\n                      <jats:sub>interaction<\/jats:sub>\n                      \u2009=\u20090.05) significantly influenced this association. Sensitivity analyses indicated that the results were robust across IBD subtypes and regions, but not across the study designs.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Discussion:<\/jats:title>\n                    <jats:p>\n                      <jats:italic toggle=\"yes\">H. pylori<\/jats:italic>\n                      infection seems to exhibit a protective effect against the risk of IBD. This association may be influenced by IBD subtypes, regions,\n                      <jats:italic toggle=\"yes\">H. pylori<\/jats:italic>\n                      virulence factors, and antibiotic exposure.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Design:<\/jats:title>\n                    <jats:p>This is an umbrella review.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Registration:<\/jats:title>\n                    <jats:p>The protocol was prospectively registered with the PROSPERO database (CRD42024559958).<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1177\/17562848261444293","type":"journal-article","created":{"date-parts":[[2026,5,4]],"date-time":"2026-05-04T09:24:01Z","timestamp":1777886641000},"update-policy":"https:\/\/doi.org\/10.1177\/sage-journals-update-policy","source":"Crossref","is-referenced-by-count":0,"title":["Effect of\n                    <i>Helicobacter pylori<\/i>\n                    infection on the risk of inflammatory bowel disease: an umbrella review and second-order meta-analysis"],"prefix":"10.1177","volume":"19","author":[{"given":"Xiaomin","family":"Wang","sequence":"first","affiliation":[{"name":"Department of Gastroenterology, General Hospital of Northern Theater Command (Teaching Hospital of Dalian Medical University), Shenyang, China"},{"name":"Postgraduate College, Dalian Medical University, Dalian, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Haonan","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, General Hospital of Northern Theater Command (Teaching Hospital of Dalian Medical University), Shenyang, China"},{"name":"Department of Life Sciences and Biopharmaceutics, Shenyang Pharmaceutical University, Shenyang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Honglu","family":"Yu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Juan","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, General Hospital of Northern Theater Command (Teaching Hospital of Dalian Medical University), Shenyang, China"},{"name":"Department of Life Sciences and Biopharmaceutics, Shenyang Pharmaceutical University, Shenyang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yongguo","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, General Hospital of Northern Theater Command (Teaching Hospital of Dalian Medical University), No. 83 Wenhua Road, Shenyang 110840, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiang","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, General Hospital of Northern Theater Command (Teaching Hospital of Dalian Medical University), No. 83 Wenhua Road, Shenyang 110840, China"},{"name":"Postgraduate College, Dalian Medical University, Dalian, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9448-6739","authenticated-orcid":false,"given":"Xingshun","family":"Qi","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, General Hospital of Northern Theater Command (Teaching Hospital of Dalian Medical University), No. 83 Wenhua Road, Shenyang 110840, China"},{"name":"Postgraduate College, Dalian Medical University, Dalian, China"},{"name":"Department of Life Sciences and Biopharmaceutics, Shenyang Pharmaceutical University, Shenyang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"179","published-online":{"date-parts":[[2026,5,4]]},"reference":[{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa2211807"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41572-023-00431-8"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1053\/j.gastro.2023.12.022"},{"key":"e_1_3_4_5_2","doi-asserted-by":"publisher","DOI":"10.2147\/IJGM.S308572"},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.1086\/516077"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.3748\/wjg.v20.i18.5461"},{"key":"e_1_3_4_8_2","article-title":"GWAS of peptic ulcer disease implicates Helicobacter pylori infection, other gastrointestinal disorders and depression","volume":"12","author":"Wu Y","year":"2021","unstructured":"Wu Y, Murray GK, Byrne EM, et al. GWAS of peptic ulcer disease implicates Helicobacter pylori infection, other gastrointestinal disorders and depression. Nat Commun 2021; 12: 1146.","journal-title":"Nat Commun"},{"key":"e_1_3_4_9_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.med.49.1.289"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.3748\/wjg.v20.i18.5191"},{"key":"e_1_3_4_11_2","doi-asserted-by":"publisher","DOI":"10.1136\/postgradmedj-2021-141127"},{"key":"e_1_3_4_12_2","doi-asserted-by":"publisher","DOI":"10.1177\/20406223221117971"},{"key":"e_1_3_4_13_2","doi-asserted-by":"publisher","DOI":"10.1155\/2023\/5521239"},{"key":"e_1_3_4_14_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.canep.2024.102626"},{"key":"e_1_3_4_15_2","doi-asserted-by":"publisher","DOI":"10.1136\/gutjnl-2015-310545"},{"key":"e_1_3_4_16_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMra020831"},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.1038\/540S97a"},{"key":"e_1_3_4_18_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(17)32448-0"},{"key":"e_1_3_4_19_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41575-020-00360-x"},{"key":"e_1_3_4_20_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41575-022-00593-y"},{"key":"e_1_3_4_21_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature06005"},{"key":"e_1_3_4_22_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature10209"},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.1097\/MCG.0000000000001415"},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.1080\/19490976.2023.2265028"},{"key":"e_1_3_4_25_2","doi-asserted-by":"publisher","DOI":"10.3748\/wjg.v29.i30.4604"},{"key":"e_1_3_4_26_2","doi-asserted-by":"publisher","DOI":"10.3748\/wjg.v30.i47.5097"},{"key":"e_1_3_4_27_2","doi-asserted-by":"publisher","DOI":"10.1093\/ibd\/izy107"},{"key":"e_1_3_4_28_2","doi-asserted-by":"publisher","DOI":"10.22207\/JPAM.16.1.75"},{"key":"e_1_3_4_29_2","doi-asserted-by":"publisher","DOI":"10.1053\/j.gastro.2019.04.016"},{"key":"e_1_3_4_30_2","article-title":"Association between H. pylori infection and health outcomes: an umbrella review of systematic reviews and meta-analyses","volume":"10","author":"Li L","year":"2020","unstructured":"Li L, Tan J, Liu L, et al. Association between H. pylori infection and health outcomes: an umbrella review of systematic reviews and meta-analyses. BMJ Open 2020; 10: e031951.","journal-title":"BMJ Open"},{"key":"e_1_3_4_31_2","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2024.1410506"},{"key":"e_1_3_4_32_2","doi-asserted-by":"publisher","DOI":"10.1136\/bmj-2022-070849"},{"key":"e_1_3_4_33_2","article-title":"AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both","volume":"358","author":"Shea BJ","year":"2017","unstructured":"Shea BJ, Reeves BC, Wells G, et al. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ 2017; 358: j4008.","journal-title":"BMJ"},{"key":"e_1_3_4_34_2","doi-asserted-by":"publisher","DOI":"10.1007\/s12325-023-02430-3"},{"key":"e_1_3_4_35_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1398-9995.2009.01973.x"},{"key":"e_1_3_4_36_2","doi-asserted-by":"publisher","DOI":"10.1002\/jrsm.1557"},{"key":"e_1_3_4_37_2","doi-asserted-by":"publisher","DOI":"10.1186\/s12889-024-21257-3"},{"key":"e_1_3_4_38_2","doi-asserted-by":"publisher","DOI":"10.1097\/JS9.0000000000000822"},{"key":"e_1_3_4_39_2","doi-asserted-by":"publisher","DOI":"10.11124\/JBIES-22-00125"},{"key":"e_1_3_4_40_2","doi-asserted-by":"publisher","DOI":"10.1097\/MD.0000000000034882"},{"key":"e_1_3_4_41_2","doi-asserted-by":"publisher","DOI":"10.34172\/aim.2021.44"},{"key":"e_1_3_4_42_2","first-page":"485","article-title":"The relationship between inflammatory bowel disease and Helicobacter pylori across East Asian, European and Mediterranean countries: a meta-analysis","volume":"33","author":"Imawana RA","year":"2020","unstructured":"Imawana RA, Smith DR, Goodson ML. The relationship between inflammatory bowel disease and Helicobacter pylori across East Asian, European and Mediterranean countries: a meta-analysis. Ann Gastroenterol 2020; 33: 485\u2013494.","journal-title":"Ann Gastroenterol"},{"key":"e_1_3_4_43_2","first-page":"10509","article-title":"Correlation between Helicobacter pylori infection and Crohn\u2019s disease: a meta-analysis","volume":"23","author":"Wang WL","year":"2019","unstructured":"Wang WL, Xu XJ. Correlation between Helicobacter pylori infection and Crohn\u2019s disease: a meta-analysis. Eur Rev Med Pharmacol Sci 2019; 23: 10509\u201310516.","journal-title":"Eur Rev Med Pharmacol Sci"},{"key":"e_1_3_4_44_2","doi-asserted-by":"publisher","DOI":"10.1111\/apt.15306"},{"key":"e_1_3_4_45_2","doi-asserted-by":"publisher","DOI":"10.3748\/wjg.v21.i15.4750"},{"key":"e_1_3_4_46_2","doi-asserted-by":"publisher","DOI":"10.1177\/2050640615580889"},{"key":"e_1_3_4_47_2","doi-asserted-by":"publisher","DOI":"10.11569\/wcjd.v21.i15.1468"},{"key":"e_1_3_4_48_2","doi-asserted-by":"publisher","DOI":"10.1002\/ibd.21116"},{"key":"e_1_3_4_49_2","doi-asserted-by":"publisher","DOI":"10.1093\/ecco-jcc\/jjw113"},{"key":"e_1_3_4_50_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1083-4389.2004.00223.x"},{"key":"e_1_3_4_51_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2036.2011.04969.x"},{"key":"e_1_3_4_52_2","doi-asserted-by":"publisher","DOI":"10.1097\/CM9.0000000000002008"},{"key":"e_1_3_4_53_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0100362"},{"key":"e_1_3_4_54_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41419-018-0982-2"},{"key":"e_1_3_4_55_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2024.1479941"},{"key":"e_1_3_4_56_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.micres.2018.09.011"},{"key":"e_1_3_4_57_2","doi-asserted-by":"publisher","DOI":"10.1053\/j.gastro.2009.07.049"},{"key":"e_1_3_4_58_2","doi-asserted-by":"publisher","DOI":"10.1097\/MIB.0000000000000811"},{"key":"e_1_3_4_59_2","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.01212"},{"key":"e_1_3_4_60_2","doi-asserted-by":"publisher","DOI":"10.5217\/ir.2019.09154"},{"key":"e_1_3_4_61_2","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.156.12.4729"},{"key":"e_1_3_4_62_2","doi-asserted-by":"publisher","DOI":"10.1155\/2015\/981328"},{"key":"e_1_3_4_63_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.micpath.2018.06.033"},{"key":"e_1_3_4_64_2","doi-asserted-by":"publisher","DOI":"10.1111\/codi.14114"},{"key":"e_1_3_4_65_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(07)61602-X"},{"key":"e_1_3_4_66_2","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.00011-10"},{"key":"e_1_3_4_67_2","article-title":"Clinical characteristics of ulcerative colitis patients with different types of Helicobacter pylori infection","volume":"12","author":"Liu W","year":"2024","unstructured":"Liu W, Jiang Q, Xue S, et al. Clinical characteristics of ulcerative colitis patients with different types of Helicobacter pylori infection. Microbiol Spectr 2024; 12: e0355423.","journal-title":"Microbiol Spectr"},{"key":"e_1_3_4_68_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2024.1384285"},{"key":"e_1_3_4_69_2","doi-asserted-by":"publisher","DOI":"10.3748\/wjg.v20.i21.6374"},{"key":"e_1_3_4_70_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cgh.2024.02.010"},{"key":"e_1_3_4_71_2","doi-asserted-by":"publisher","DOI":"10.1016\/S2468-1253(20)30267-3"},{"key":"e_1_3_4_72_2","doi-asserted-by":"publisher","DOI":"10.1136\/gutjnl-2022-327845"},{"key":"e_1_3_4_73_2","doi-asserted-by":"publisher","DOI":"10.1097\/CM9.0000000000002546"},{"key":"e_1_3_4_74_2","doi-asserted-by":"publisher","DOI":"10.14309\/ajg.0000000000002968"},{"key":"e_1_3_4_75_2","doi-asserted-by":"publisher","DOI":"10.3748\/wjg.v29.i4.692"},{"key":"e_1_3_4_76_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.lanmic.2024.100975"},{"key":"e_1_3_4_77_2","doi-asserted-by":"publisher","DOI":"10.1136\/gutjnl-2023-329792"},{"key":"e_1_3_4_78_2","doi-asserted-by":"publisher","DOI":"10.4065\/74.7.727"},{"key":"e_1_3_4_79_2","doi-asserted-by":"publisher","DOI":"10.1093\/ibd\/izad035"}],"container-title":["Therapeutic Advances in Gastroenterology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1177\/17562848261444293","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/full-xml\/10.1177\/17562848261444293","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1177\/17562848261444293","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,6]],"date-time":"2026-05-06T13:17:52Z","timestamp":1778073472000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.sagepub.com\/doi\/10.1177\/17562848261444293"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,5]]},"references-count":78,"alternative-id":["10.1177\/17562848261444293"],"URL":"https:\/\/doi.org\/10.1177\/17562848261444293","relation":{},"ISSN":["1756-2848","1756-2848"],"issn-type":[{"value":"1756-2848","type":"print"},{"value":"1756-2848","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,5]]},"article-number":"17562848261444293"}}