{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,26]],"date-time":"2026-07-26T02:55:58Z","timestamp":1785034558704,"version":"3.55.0"},"reference-count":48,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2025,3,14]],"date-time":"2025-03-14T00:00:00Z","timestamp":1741910400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ibnou Zohr University","award":["Appel \u00e0 Projets 2018"],"award-info":[{"award-number":["Appel \u00e0 Projets 2018"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Helicobacter pylori (H. pylori) possess an arsenal of virulence genes that makes them the main etiological factor in gastric diseases. In this study, 120 southern Moroccan patients who were dyspeptic were profiled to investigate the potential association between disease severity and the combination of multiple virulence genes. Gastric biopsies were taken from patients, followed by histopathological evaluation and genotyping of H. pylori using PCR. H. pylori was detected in 58.3% of cases, and genotypes were distributed as follows: oipA (94.3%), cagA (62.9%), virB11 (60%), babA (55.7%), dupA (54.3%), cagE (51.4%), iceA1 (31.4%), iceA2 (45.7%), vacA\u00a0s2m2 (47.1%), vacA\u00a0s1m1 (30%), and vacA\u00a0s1m2 (7.1%). Statistically significant associations with males were observed for the cagA, cagE, and virB11 genes and multiple strain infections. Multivariate analysis revealed an association between cagE and heightened neutrophil activity, with an odds ratio (OR) of 4.99 (p = 0.03). The gene combination [cagA (+), cagE (+), virB11 (+), vacA\u00a0s1m1, and babA (+)] emerged as a predictive factor for gastric cancer (OR = 11.10, p = 0.046), while the combination [cagA (-), cagE (-), virB11 (-), vacA s2m2, babA (+)] was associated with gastric atrophy (OR = 10.25, p = 0.016). Age (\u226440 years) (OR = 5.87, p = 0.013) and moderate to severe bacterial density (OR = 15.38, p = 0.017) were identified as predictive factors for follicular gastritis. These findings underscore the significance of multigene profiling as a prognostic marker and emphasize the importance of age and sex in preventing adverse outcomes in severe gastric diseases.<\/jats:p>","DOI":"10.3390\/pathogens14030279","type":"journal-article","created":{"date-parts":[[2025,3,14]],"date-time":"2025-03-14T04:29:18Z","timestamp":1741926558000},"page":"279","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["The Effect of Helicobacter pylori Gene Combinations of cagA, cagE, virB11, vacA, and babA on the Outcome of Gastric Disease in a Southern Moroccan Population"],"prefix":"10.3390","volume":"14","author":[{"given":"Mariama","family":"Barhoine","sequence":"first","affiliation":[{"name":"Cell Biology and Molecular Genetics Laboratory, Faculty of Sciences, Ibnou Zohr University, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fatima","family":"Moustaoui","sequence":"additional","affiliation":[{"name":"Cell Biology and Molecular Genetics Laboratory, Faculty of Sciences, Ibnou Zohr University, Agadir 80000, Morocco"},{"name":"Medical Analysis Laboratory, Regional Hospital Centre Hassan II, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Omayma","family":"Hammani","sequence":"additional","affiliation":[{"name":"Cell Biology and Molecular Genetics Laboratory, Faculty of Sciences, Ibnou Zohr University, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed","family":"Aghrouch","sequence":"additional","affiliation":[{"name":"Medical Analysis Laboratory, Regional Hospital Centre Hassan II, Agadir 80000, Morocco"},{"name":"Medical-Surgical, Biomedicine and Infectiology Laboratory, Faculty of Medicine and Pharmacy, Ibnou Zohr University, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zohra","family":"Lemkhente","sequence":"additional","affiliation":[{"name":"Medical-Surgical, Biomedicine and Infectiology Laboratory, Faculty of Medicine and Pharmacy, Ibnou Zohr University, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zineb","family":"Belhabib","sequence":"additional","affiliation":[{"name":"Gastroenterology Practice, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zineb","family":"Bajaddoub","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Mokhtar Soussi Hospital, Taroudant 83000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anass","family":"Touyar","sequence":"additional","affiliation":[{"name":"Gastroenterology Unit, Hassan II Hospital, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nourdin","family":"Aqoudad","sequence":"additional","affiliation":[{"name":"Faculty of Medicine and Pharmacy of Agadir, Ibnou Zohr University, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bouchra","family":"Rherissi","sequence":"additional","affiliation":[{"name":"Cell Biology and Molecular Genetics Laboratory, Faculty of Sciences, Ibnou Zohr University, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7032-9704","authenticated-orcid":false,"given":"Nadia","family":"El Kadmiri","sequence":"additional","affiliation":[{"name":"Geo-Bio-Environment Engineering and Innovation Laboratory, Polydisciplinary Faculty, Ibnou Zohr University, Taroudant 83000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2768-9376","authenticated-orcid":false,"given":"Youssef","family":"Idaghdour","sequence":"additional","affiliation":[{"name":"Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi P.O. Box 129188, United Arab Emirates"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fatima","family":"Boubrik","sequence":"additional","affiliation":[{"name":"Cell Biology and Molecular Genetics Laboratory, Faculty of Sciences, Ibnou Zohr University, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2553-8387","authenticated-orcid":false,"given":"Ahmed","family":"Belmouden","sequence":"additional","affiliation":[{"name":"Cell Biology and Molecular Genetics Laboratory, Faculty of Sciences, Ibnou Zohr University, Agadir 80000, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,3,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Mobley, H.L.T., Mendz, G.L., and Hazell, S.L. (2001). Pathology of Gastritis and Peptic Ulceration. Helicobacter Pylori: Physiology and Genetics, ASM Press.","DOI":"10.1128\/9781555818005"},{"key":"ref_2","first-page":"158","article-title":"Asociaci\u00f3n de Los Genotipos CagA, VacA e IceA de H. Pylori Con La Gastritis Cr\u00f3nica y Folicular En Una Poblaci\u00f3n Colombiana Con Alto Riesgo de C\u00e1ncer G\u00e1strico","volume":"84","author":"Rosero","year":"2019","journal-title":"Rev. Gastroenterol. Mex."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Cheok, Y.Y., Lee, C.Y.Q., Cheong, H.C., Vadivelu, J., Looi, C.Y., Abdullah, S., and Wong, W.F. (2021). An Overview of Helicobacter Pylori Survival Tactics in the Hostile Human Stomach Environment. Microorganisms, 9.","DOI":"10.3390\/microorganisms9122502"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1678-9199-20-1","article-title":"Association among H. Pylori Virulence Markers DupA, CagA and VacA in Brazilian Patients","volume":"20","author":"Pereira","year":"2014","journal-title":"J. Venom. Anim. Toxins Incl. Trop. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.1007\/s12029-021-00734-7","article-title":"Potential Non-Invasive Biomarkers of Helicobacter Pylori-Associated Gastric Cancer","volume":"53","author":"Boubrik","year":"2022","journal-title":"J. Gastrointest. Cancer"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Oktem-Okullu, S., Tiftikci, A., Saruc, M., Cicek, B., Vardareli, E., Tozun, N., Kocagoz, T., Sezerman, U., Yavuz, A.S., and Sayi-Yazgan, A. (2015). Multiplex-PCR-Based Screening and Computational Modeling of Virulence Factors and T-Cell Mediated Immunity in Helicobacter Pylori Infections for Accurate Clinical Diagnosis. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0136212"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/1757-4749-2-13","article-title":"Systematic Review and Meta-Analysis: The Relationship between the Helicobacter Pylori DupA Gene and Clinical Outcomes","volume":"2","author":"Shiota","year":"2010","journal-title":"Gut Pathog."},{"key":"ref_8","first-page":"4611","article-title":"Analysis of Virulence Diversity of 73 Helicobacter pylori Strains Isolated in Guizhou Province, China","volume":"18","author":"Yin","year":"2018","journal-title":"Mol. Med. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1921","DOI":"10.1007\/s42770-021-00553-9","article-title":"Helicobacter Pylori Virulence DupA Gene: Risk Factor or Protective Factor?","volume":"52","author":"Oliveira","year":"2021","journal-title":"Braz. J. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.micpath.2017.02.018","article-title":"Prevalence of Helicobacter Pylori VacA, CagA, CagE, OipA, IceA, BabA2 and BabB Genotypes in Iranian Dyspeptic Patients","volume":"105","author":"Dabiri","year":"2017","journal-title":"Microb. Pathog."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"12758","DOI":"10.1111\/hel.12758","article-title":"Helicobacter Pylori Adhesins: HpaA a Potential Antigen in Experimental Vaccines for H. Pylori","volume":"26","author":"Lei","year":"2021","journal-title":"Helicobacter"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1007\/s10620-014-3319-8","article-title":"Correlation of Helicobacter Pylori Genotypes with Gastric Histopathology in the Central Region of a South-European Country","volume":"60","author":"Almeida","year":"2015","journal-title":"Dig. Dis. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"El Khadir, M., Alaoui Boukhris, S., Benajah, D.-A., El Rhazi, K., Ibrahimi, S.A., El Abkari, M., Harmouch, T., Nejjari, C., Mahmoud, M., and Benlemlih, M. (2017). VacA and CagA Status as Biomarker of Two Opposite End Outcomes of Helicobacter Pylori Infection (Gastric Cancer and Duodenal Ulcer) in a Moroccan Population. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0170616"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Shariq, M., Kumar, N., Kumari, R., Kumar, A., Subbarao, N., and Mukhopadhyay, G. (2015). Biochemical Analysis of CagE: A VirB4 Homologue of Helicobacter Pylori Cag-T4SS. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0142606"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e00849-19","DOI":"10.1128\/mBio.00849-19","article-title":"In Situ Molecular Architecture of the Helicobacter Pylori Cag Type IV Secretion System","volume":"10","author":"Hu","year":"2019","journal-title":"mBio"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1111\/j.1523-5378.1997.06b09.x","article-title":"For the International Workshop on the Histopathology of Gast Histological Classif Ication of Gastritis and Helicobacter Pylori Infection: An Agreement at Last?","volume":"2","author":"Dixon","year":"1997","journal-title":"Helicobacter"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"7533","DOI":"10.1073\/pnas.130079797","article-title":"A M r 34,000 Proinflammatory Outer Membrane Protein (OipA) of Helicobacter Pylori","volume":"97","author":"Yamaoka","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2979","DOI":"10.1128\/JCM.37.9.2979-2982.1999","article-title":"Simple and Accurate PCR-Based System for Typing Vacuolating Cytotoxin Alleles of Helicobacter Pylori","volume":"37","author":"Atherton","year":"1999","journal-title":"J. Clin. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2274","DOI":"10.1128\/JCM.37.7.2274-2279.1999","article-title":"Relationship between Helicobacter Pylori IceA, CagA, and VacA Status and Clinical Outcome: Studies in Four Different Countries","volume":"37","author":"Yamaoka","year":"1999","journal-title":"J. Clin. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"17771","DOI":"10.1074\/jbc.270.30.17771","article-title":"Mosaicism in Vacuolating Cytotoxin Alleles of Helicobacter Pylori. Association of Specific VacA Types with Cytotoxin Production and Peptic Ulceration","volume":"270","author":"Atherton","year":"1995","journal-title":"J. Biol. Chem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e32","DOI":"10.1016\/j.canep.2011.02.017","article-title":"Prevalence of Helicobacter Pylori Genotypes (VacA, CagA, CagE and VirB11) in Gastric Cancer in Brazilian\u2019s Patients: An Association with Histopathological Parameters","volume":"35","author":"Lima","year":"2011","journal-title":"Cancer Epidemiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1128\/JCM.43.2.791-795.2005","article-title":"Simple Method for Determination of the Number of Helicobacter Pylori CagA Variable-Region EPIYA Tyrosine Phosphorylation Motifs by PCR","volume":"43","author":"Argent","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1007\/s10482-014-0234-0","article-title":"Prevalence of the Helicobacter Pylori BabA2 Gene and Correlation with the Degree of Gastritis in Infected Slovenian Children","volume":"106","author":"Homan","year":"2014","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"12778","DOI":"10.1073\/pnas.96.22.12778","article-title":"Clinical Relevance of the Helicobacter Pylori Gene for Blood-Group Antigen-Binding Adhesin","volume":"96","author":"Gerhard","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3206","DOI":"10.1002\/ijc.33158","article-title":"VacA Genotypes and cagA-EPIYA-CMotifs of Helicobacter Pylori and Gastric Histopathological Lesions","volume":"147","author":"Benajah","year":"2020","journal-title":"Int. J. Cancer"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Subsomwong, P., Miftahussurur, M., Uchida, T., Vilaichone, R., Ratanachu-ek, T., Mahachai, V., and Yamaoka, Y. (2017). Prevalence, Risk Factors, and Virulence Genes of Helicobacter Pylori among Dyspeptic Patients in Two Different Gastric Cancer Risk Regions of Thailand. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0187113"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"368","DOI":"10.4014\/jmb.2101.01023","article-title":"Increased Risk of Severe Gastric Symptoms by Virulence Factors VacAs1c, AlpA, BabA2, and Hop Z in Helicobacter Pylori Infection","volume":"31","author":"Lee","year":"2021","journal-title":"J. Microbiol. Biotechnol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/j.micpath.2019.01.018","article-title":"Virulence Factor Genotyping of Helicobacter Pylori Isolated from Costa Rican Dyspeptic Patients","volume":"128","author":"Une","year":"2019","journal-title":"Microb. Pathog."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Ben Mansour, K., Fendri, C., Zribi, M., Masmoudi, A., Labbene, M., Fillali, A., Ben Mami, N., Najjar, T., Meherzi, A., and Sfar, T. (2010). Prevalence of Helicobacter Pylori VacA, CagA, IceA and OipA Genotypes in Tunisian Patients. Ann. Clin. Microbiol. Antimicrob., 9.","DOI":"10.1186\/1476-0711-9-10"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1111\/j.1523-5378.2006.00461.x","article-title":"Prevalence of Helicobacter Pylori VacA, CagA, CagE, IceA, BabA2 Genotypes and Correlation with Clinical Outcome in Turkish Patients with Dyspepsia","volume":"11","author":"Erzin","year":"2006","journal-title":"Helicobacter"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"55","DOI":"10.3103\/S0891416817010074","article-title":"Lack of Association between the Presence of DupA and BabA 2 Genes in Helicobacter Pylori and Gastroduodenal Disorders","volume":"32","author":"Jalilian","year":"2017","journal-title":"Mol. Genet. Microbiol. Virol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e750","DOI":"10.1016\/j.ijid.2013.03.004","article-title":"Genotyping of Helicobacter Pylori Virulence-Associated Genes Shows High Diversity of Strains Infecting Patients in Western Venezuela","volume":"17","author":"Chiurillo","year":"2013","journal-title":"Int. J. Infect. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Akeel, M., Shehata, A., Elhafey, A., Elmakki, E., Aboshouk, T., Ageely, H., and Mahfouz, M. (2019). Helicobacter Pylori VacA, CagA and IceA Genotypes in Dyspeptic Patients from Southwestern Region, Saudi Arabia: Distribution and Association with Clinical Outcomes and Histopathological Changes. BMC Gastroenterol., 19.","DOI":"10.1186\/s12876-019-0934-z"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Idowu, A., Mzukwa, A., Harrison, U., Palamides, P., Haas, R., Mbao, M., Mamdoo, R., Bolon, J., Jolaiya, T., and Smith, S. (2019). Detection of Helicobacter Pylori and Its Virulence Genes (CagA, DupA, and VacA) among Patients with Gastroduodenal Diseases in Chris Hani Baragwanath Academic Hospital, South Africa. BMC Gastroenterol., 19.","DOI":"10.1186\/s12876-019-0986-0"},{"key":"ref_35","first-page":"261","article-title":"The CagA, CagE, VacA, DupA and IceA1 Genes of Helicobacter Pylori in Sudanese Gastritis Patients: Distribution and Relationship with Clinical Outcomes and Histological Alterations","volume":"18","author":"Elnosh","year":"2022","journal-title":"Malays. J. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1016\/j.ejmhg.2017.04.003","article-title":"Detection of Helicobacter Pylori VacA, CagA and IceA1 Virulence Genes Associated with Gastric Diseases in Egyptian Patients","volume":"18","author":"Diab","year":"2017","journal-title":"Egypt. J. Med. Hum. Genet."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"7521913","DOI":"10.1155\/2016\/7521913","article-title":"Mixed Infections of Helicobacter Pylori Isolated from Patients with Gastrointestinal Diseases in Taiwan","volume":"2016","author":"Lai","year":"2016","journal-title":"Gastroenterol. Res. Pract."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1007\/s42770-020-00292-3","article-title":"Genetic Variation in the Cag Pathogenicity Island of Helicobacter Pylori Strains Detected from Gastroduodenal Patients in Thailand","volume":"51","author":"Boonyanugomol","year":"2020","journal-title":"Braz. J. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"4870","DOI":"10.3748\/wjg.v25.i33.4870","article-title":"Helicobacter Pylori Virulence Genes","volume":"25","author":"Jarc","year":"2019","journal-title":"World J. Gastroenterol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Garc\u00eda-G\u00f3mez, E., Gonz\u00e1lez-Pedrajo, B., and Camacho-Arroyo, I. (2013). Role of Sex Steroid Hormones in Bacterial-Host Interactions. Biomed. Res. Int., 2013.","DOI":"10.1155\/2013\/928290"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1111\/j.1574-6968.2011.02239.x","article-title":"Steroid Hormones as Bactericidal Agents to Helicobacter Pylori","volume":"318","author":"Hosoda","year":"2011","journal-title":"FEMS Microbiol Lett"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"101404","DOI":"10.1016\/j.eclinm.2022.101404","article-title":"The Current and Future Incidence and Mortality of Gastric Cancer in 185 Countries, 2020\u201340: A Population-Based Modelling Study","volume":"47","author":"Morgan","year":"2022","journal-title":"EClinicalMedicine"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"682","DOI":"10.1016\/j.tim.2020.02.004","article-title":"The Helicobacter Pylori Cag Type IV Secretion System","volume":"28","author":"Cover","year":"2020","journal-title":"Trends Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e07610","DOI":"10.1016\/j.heliyon.2021.e07610","article-title":"Frequency of Virulence-Associated Genotypes of Helicobacter Pylori and Their Correlation with Clinical Outcome and Histological Parameters in Infected Patients","volume":"7","author":"Ahmadi","year":"2021","journal-title":"Heliyon"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1099\/jmm.0.001123","article-title":"Presence of CagPAI Genes and Characterization of VacA s, i and m Regions in Helicobacter Pylori Isolated from Alaskans and Their Association with Clinical Pathologies","volume":"69","author":"Miernyk","year":"2020","journal-title":"J. Med. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Chen, R., Li, Y., Chen, X., Chen, J., Song, J., Yang, X., Ye, L., Wu, Z., Xie, P., and Zhong, Q. (2023). DupA+H. Pylori Reduces Diversity of Gastric Microbiome and Increases Risk of Erosive Gastritis. Front. Cell. Infect. Microbiol., 13.","DOI":"10.3389\/fcimb.2023.1103909"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"14944","DOI":"10.1073\/pnas.1100959108","article-title":"Carcinogenic Bacterial Pathogen Helicobacter Pylori Triggers DNA Double-Strand Breaks and a DNA Damage Response in Its Host Cells","volume":"108","author":"Toller","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1909","DOI":"10.1111\/cas.15357","article-title":"Helicobacter Pylori-induced DNA Double-stranded Break in the Development of Gastric Cancer","volume":"113","author":"Hatakeyama","year":"2022","journal-title":"Cancer Sci."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/14\/3\/279\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T16:53:27Z","timestamp":1760028807000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/14\/3\/279"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,14]]},"references-count":48,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025,3]]}},"alternative-id":["pathogens14030279"],"URL":"https:\/\/doi.org\/10.3390\/pathogens14030279","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3,14]]}}}