{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T00:14:44Z","timestamp":1790036084681,"version":"4.0.1"},"reference-count":70,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2025,8,7]],"date-time":"2025-08-07T00:00:00Z","timestamp":1754524800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Al Ahliyya Amman University","award":["12\/05\/2023-2024"],"award-info":[{"award-number":["12\/05\/2023-2024"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Helicobacter pylori is a well-established causative agent of gastritis, peptic ulcers, gastric adenocarcinoma, and primary gastric lymphoma. It colonizes the human stomach and expresses numerous virulent factors that influence disease progression. Among these factors is the cytotoxin vacA gene, which encodes the vacuolating capacity of the cytotoxin and plays a key role in the bacterium\u2019s pathogenic potential. This study investigated the allelic diversity of the vacA among H. pylori strains infecting patients in Jordan with various gastric conditions and examined potential associations between vacA s-and m- genotypes, histopathological and endoscopic findings, and the development of gastric diseases. Gastric biopsies were collected from 106 patients at two hospitals in Jordan who underwent endoscopic examination. The collected biopsies for each patient were subjected to histopathological assessment, urease detection using the Rapid Urease Test (RUT), a diagnostic test for H. pylori, and molecular detection of the vacA gene and its s and m alleles. The histopathology reports indicated that 83 of 106 patients exhibited gastric disorders, of which 81 samples showed features associated with H. pylori infection. The RUT was positive in 76 of 106 with an accuracy of 93.8%. Real-time polymerase chain reaction (RT-PCR) targeting the 16S rRNA gene confirmed the presence of H. pylori in 79 of 81 histologically diagnosed cases as infected (97.5%), while the vacA gene was detected only in 75 samples (~95%). To explore genetic diversity, PCR-amplified fragments underwent sequence analysis of the vacA gene. The m-allele was detected in 58 samples (73%), the s-allele was detected in 45 (57%), while both alleles were not detected in 13% of samples. The predominant genotype combination among Jordanians was vacA s2\/m2 (50%), significantly linked to mild chronic gastritis, followed by s1\/m2 (35%) and s1\/m1 (11.8%) which are linked to severe gastric conditions including malignancies. Age-and gender-related differences in vacA genotype were observed with less virulent s2m2 and s1m2 genotypes predominating in younger adults specially males, while the more virulent m1 genotypes were found exclusively in females and middle-aged patients. Genomic sequencing revealed extensive diversity within H. pylori, likely reflecting its long-standing co-evolution with human hosts in Jordan. This genetic variability plays a key role in modulating virulence and influencing clinical outcomes. Comprehensive characterization of vacA genotypic variations through whole-genome sequencing is essential to enhance diagnostic precision, strengthen epidemiological surveillance, and inform targeted therapeutic strategies. While this study highlights the significance of the vacA\u00a0m and s alleles, future research is recommended in order to investigate the other vacA allelic variations, such as the i, d, and c alleles, to achieve a more comprehensive understanding of H. pylori pathogenicity and associated disease severity across different strains. These investigations will be crucial for improving diagnostic accuracy and guiding the development of targeted therapeutic strategies.<\/jats:p>","DOI":"10.3390\/microorganisms13081841","type":"journal-article","created":{"date-parts":[[2025,8,7]],"date-time":"2025-08-07T10:07:38Z","timestamp":1754561258000},"page":"1841","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Allelic Variation of Helicobacter pylori\u00a0vacA Gene and Its Association with Gastric Pathologies in Clinical Samples Collected in Jordan"],"prefix":"10.3390","volume":"13","author":[{"given":"Mamoon M.","family":"Al-Hyassat","sequence":"first","affiliation":[{"name":"Department of Medical Laboratory Sciences, Faculty of Allied Medical Sciences, Al-Ahliyya Amman University, Amman 19328, Jordan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6126-7209","authenticated-orcid":false,"given":"Hala I.","family":"Al-Daghistani","sequence":"additional","affiliation":[{"name":"Department of Medical Laboratory Sciences, Faculty of Allied Medical Sciences, Al-Ahliyya Amman University, Amman 19328, Jordan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1434-259X","authenticated-orcid":false,"given":"Lubna F.","family":"Abu-Niaaj","sequence":"additional","affiliation":[{"name":"Department of Agricultural and Life Sciences, John W. Garland College of Engineering, Science, Technology and Agriculture, Central State University, Wilberforce, OH 45384, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9505-5236","authenticated-orcid":false,"given":"Sima","family":"Zein","sequence":"additional","affiliation":[{"name":"Department of Pharmaceutical Biotechnology, Faculty of Allied Medical Sciences, Al-Ahliyya Amman University, Amman 19328, Jordan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3646-657X","authenticated-orcid":false,"given":"Talal","family":"Al-Qaisi","sequence":"additional","affiliation":[{"name":"Department of Medical Laboratory Sciences, Faculty of Allied Medical Sciences, Al-Ahliyya Amman University, Amman 19328, Jordan"},{"name":"Department of Biomedical Sciences, College of Health Sciences, Abu Dhabi University, Abu Dhabi P.O. Box 59911, United Arab Emirates"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,8,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Sarma, A., Medhi, D., Sarma, M.K., Saikia, L., Choudhury, B.N., Bhattacharya, M., and Sarma, V. (2025). Helicobacter pylori Genetic Landscape in Northeast India and Its Impact in Peptic Ulcer Disease and Gastric Cancer. Front. Bacteriol., 4.","DOI":"10.3389\/fbrio.2025.1589230"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Reyes, V.E. (2023). Helicobacter pylori and Its Role in Gastric Cancer. Microorganisms, 11.","DOI":"10.3390\/microorganisms11051312"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"104431","DOI":"10.1016\/j.meegid.2020.104431","article-title":"Which Genotype of Helicobacter pylori\u2014cagA or cagE\u2014Is Better Associated with Gastric Cancer Risk? Lessons from an Extremely High-Risk Area in Iran","volume":"85","author":"Bakhti","year":"2020","journal-title":"Infect. Genet. Evol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Barhoine, M., Moustaoui, F., Hammani, O., Aghrouch, M., Lemkhente, Z., Belhabib, Z., Bajaddoub, Z., Touyar, A., Aqoudad, N., and Rherissi, B. (2025). 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. Pathogens, 14.","DOI":"10.3390\/pathogens14030279"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1053\/j.gastro.2019.10.019","article-title":"Risk Factors and Incidence of Gastric Cancer after Detection of Helicobacter pylori Infection: A Large Cohort Study","volume":"158","author":"Kumar","year":"2020","journal-title":"Gastroenterology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"36","DOI":"10.5005\/jp-journals-10018-1310","article-title":"Helicobacter pylori Infection and Gastric Microbiota","volume":"10","author":"Ozbey","year":"2020","journal-title":"Euroasian J. Hepato-Gastroenterol."},{"key":"ref_7","first-page":"209","article-title":"Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries","volume":"71","author":"Sung","year":"2021","journal-title":"CA Cancer J. Clin."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"30","DOI":"10.25259\/IJMIO_8_2020","article-title":"Molecular Genetic Changes in Gastric Carcinoma","volume":"6","author":"Singh","year":"2021","journal-title":"Int. J. Mol. Immuno-Oncol."},{"key":"ref_9","unstructured":"(1994). Schistosomes, Live flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, Lyon, 7\u201314 June 1994. IARC Monogr. Eval. Carcinog. Risks Hum., 61, 1\u2013241."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Burz, C., Pop, V., Silaghi, C., Lupan, I., and Samasca, G. (2024). Helicobacter pylori Infection in Patients with Gastric Cancer: A 2024 Update. Cancers, 16.","DOI":"10.3390\/cancers16111958"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Shirani, M., Pakzad, R., Haddadi, M.H., Akrami, S., Asadi, A., Kazemian, H., Moradi, M., Kaviar, V.H., Zomorodi, A.R., and Khoshnood, S. (2023). The Global Prevalence of Gastric Cancer in Helicobacter pylori-Infected Individuals: A Systematic Review and Meta-Analysis. BMC Infect. Dis., 23.","DOI":"10.1186\/s12879-023-08504-5"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/hel.12165","article-title":"Epidemiology of Helicobacter pylori Infection","volume":"19","author":"Eusebi","year":"2014","journal-title":"Helicobacter"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Borka Balas, R., Meli\u021b, L.E., and M\u0103rginean, C.O. (2022). Worldwide Prevalence and Risk Factors of Helicobacter pylori Infection in Children. Children, 9.","DOI":"10.37247\/PAMED4ED.4.22.22"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Jarzab, M., and Skorko-Glonek, J. (2024). There Are No Insurmountable Barriers: Passage of the Helicobacter pylori VacA Toxin from Bacterial Cytoplasm to Eukaryotic Cell Organelle. Membranes, 14.","DOI":"10.3390\/membranes14010011"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"12767","DOI":"10.3748\/wjg.v20.i36.12767","article-title":"Effect of Helicobacter pylori on Gastric Epithelial Cells","volume":"20","author":"Alzahrani","year":"2014","journal-title":"World J. Gastroenterol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/j.canlet.2013.08.016","article-title":"Helicobacter pylori-Induced Gastric Inflammation and Gastric Cancer","volume":"345","author":"Wang","year":"2014","journal-title":"Cancer Lett."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1016\/j.bpg.2014.09.004","article-title":"Clinical Relevance of Helicobacter pylori vacA and cagA Genotypes in Gastric Carcinoma","volume":"28","author":"Ferreira","year":"2014","journal-title":"Best Pract. Res. Clin. Gastroenterol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Jones, K.R., Whitmire, J.M., and Merrell, D.S. (2010). A Tale of Two Toxins: Helicobacter pylori CagA and VacA Modulate Host Pathways That Impact Disease. Front. Microbiol., 1.","DOI":"10.3389\/fmicb.2010.00115"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Nimri, L.F., Matalka, I., Bani Hani, K., and Ibrahim, M. (2006). Helicobacter pylori Genotypes Identified in Gastric Biopsy Specimens from Jordanian Patients. BMC Gastroenterol., 6.","DOI":"10.1186\/1471-230X-6-27"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Brasil-Costa, I., Souza, C.D.O., Monteiro, L.C.R., Santos, M.E.S., Oliveira, E.H.C.D., and Burbano, R.M.R.H. (2022). pylori Infection and Virulence Factors cagA and vacA (s and m Regions) in Gastric Adenocarcinoma from Par\u00e1 State, Brazil. Pathogens, 11.","DOI":"10.3390\/pathogens11040414"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Foegeding, N.J., Caston, R.R., McClain, M.S., Ohi, M.D., and Cover, T.L. (2016). An Overview of Helicobacter pylori VacA Toxin Biology. Toxins, 8.","DOI":"10.3390\/toxins8060173"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ansari, S., and Yamaoka, Y. (2019). Helicobacter pylori Virulence Factors Exploiting Gastric Colonization and Its Pathogenicity. Toxins, 11.","DOI":"10.3390\/toxins11110677"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Palframan, S.L., Kwok, T., and Gabriel, K. (2012). Vacuolating Cytotoxin A (VacA), a Key Toxin for Helicobacter pylori Pathogenesis. Front. Cell. Infect. Microbiol., 2.","DOI":"10.3389\/fcimb.2012.00092"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e4","DOI":"10.1017\/erm.2017.4","article-title":"Helicobacter pylori as an Oncogenic Pathogen, Revisited","volume":"9","author":"Miftahussurur","year":"2017","journal-title":"Expert Rev. Mol. Med."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Pajavand, H., Alvandi, A., Mohajeri, P., Bakhtyari, S., Bashiri, H., Kalali, B., and Abiri, R. (2015). High Frequency of vacA s1m2 Genotypes among Helicobacter pylori Isolates from Patients with Gastroduodenal Disorders in Kermanshah, Iran. Jundishapur J. Microbiol., 8.","DOI":"10.5812\/jjm.25425"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1186\/s13099-021-00434-4","article-title":"Geographic Distribution of the cagA, vacA, iceA, oipA and dupA Genes of Helicobacter pylori Strains Isolated in China","volume":"13","author":"Xue","year":"2021","journal-title":"Gut Pathog."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.micpath.2018.06.023","article-title":"CagA and vacA Allelic Combination of Helicobacter pylori in Gastroduodenal Disorders","volume":"122","author":"Sheikh","year":"2018","journal-title":"Microb. Pathog."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1038\/16495","article-title":"Genomic-Sequence Comparison of Two Unrelated Isolates of the Human Gastric Pathogen Helicobacter pylori","volume":"397","author":"Alm","year":"1999","journal-title":"Nature"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/S0966-842X(99)01505-X","article-title":"Evolution of Helicobacter pylori: The Role of Recombination","volume":"7","author":"Suerbaum","year":"1999","journal-title":"Trends Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1693","DOI":"10.1099\/00221287-147-6-1693","article-title":"Population Genetics of Helicobacter pylori in the Southern Part of Switzerland Analysed by Sequencing of Four Housekeeping Genes (atpD, glnA, scoB and recA) and by vacA, cagA, iceA and IS605 Genotyping","volume":"147","author":"Solca","year":"2001","journal-title":"Microbiology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"S1","DOI":"10.1111\/apt.16592","article-title":"Epidemiology of Helicobacter pylori","volume":"55","author":"Sonnenberg","year":"2022","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1046\/j.1365-2036.2002.0160s1003.x","article-title":"Review Article: Natural History and Epidemiology of Helicobacter pylori Infection","volume":"16","author":"Go","year":"2002","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_33","first-page":"1582","article-title":"Traces of Human Migrations in Helicobacter pylori Populations","volume":"292","author":"Falush","year":"2001","journal-title":"Science"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1093\/infdis\/174.3.631","article-title":"Multiple Strain Colonization and Metronidazole Resistance in Helicobacter pylori-Infected Patients: Identification from Sequential and Multiple Biopsy Specimens","volume":"174","author":"Jorgensen","year":"1996","journal-title":"J. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/nrgastro.2010.154","article-title":"Mechanisms of Disease: Helicobacter pylori Virulence Factors","volume":"7","author":"Yamaoka","year":"2010","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"201","DOI":"10.4103\/1319-3767.54743","article-title":"Helicobacter pylori Infection in Developing Countries: The Burden for How Long?","volume":"15","author":"Salih","year":"2009","journal-title":"Saudi J. Gastroenterol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1002\/path.1868","article-title":"Helicobacter Infection and Gastric Neoplasia","volume":"208","author":"Peek","year":"2006","journal-title":"J. Pathol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"8184","DOI":"10.1038\/s41467-023-43562-y","article-title":"The Helicobacter pylori Genome Project: Insights into H. pylori Population Structure from Analysis of a Worldwide Collection of Complete Genomes","volume":"14","author":"Thorell","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Baj, J., Forma, A., Sitarz, M., Portincasa, P., Garruti, G., Krasowska, D., and Maciejewski, R. (2020). Helicobacter pylori Virulence Factors\u2014Mechanisms of Bacterial Pathogenicity in the Gastric Microenvironment. Cells, 10.","DOI":"10.3390\/cells10010027"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1128\/CMR.00011-10","article-title":"Helicobacter pylori and Gastric Cancer: Factors That Modulate Disease Risk","volume":"23","author":"Wroblewski","year":"2010","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"139","DOI":"10.33899\/mmed.2020.164156","article-title":"Helicobacter pylori in Gastric Biopsy: A Histochemical and Immunohistochemical Assessment","volume":"41","author":"Aziz","year":"2019","journal-title":"Ann. Coll. Med. Mosul"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"D\u0103nil\u0103, C., Cardos, I.A., Pop-Crisan, A., Marc, F., Hoza, A., Chirla, R., Pascal\u0103u, A., Magheru, C., and Cavalu, S. (2022). Correlations Between Endoscopic and Histopathological Assessment of Helicobacter pylori-Induced Gastric Pathology: A Cross-Sectional Retrospective Study. Life, 12.","DOI":"10.3390\/life12122096"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e12572","DOI":"10.1111\/hel.12572","article-title":"First Nationwide Seroepidemiology and Risk Factors Report of Helicobacter pylori in Jordan","volume":"24","author":"Obaidat","year":"2019","journal-title":"Helicobacter"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Alaridah, N., Jarrar, R.F., Joudeh, R.M., Aljarawen, M., Jum\u2019ah, M., Nassr, H., AlHmoud, R.R., Allouzi, A., Wadi, E.M., and Abu-Humaidan, A.H. (2023). Knowledge and Information Sources Towards Helicobacter pylori in Jordan. PLoS ONE, 18.","DOI":"10.1371\/journal.pone.0278078"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Kim, J.M. (2016). H. pylori virulence factors: Toxins (CagA, VacA, DupA, OipA, IceA). Helicobacter pylori, Springer.","DOI":"10.1007\/978-981-287-706-2_5"},{"key":"ref_46","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_47","doi-asserted-by":"crossref","unstructured":"Shanjana, A., and Archana, A. (2003). Cytotoxic Isolates of Helicobacter pylori from Peptic Ulcer Diseases Decrease K+-Dependent ATPase Activity in HeLa Cells. BMC Gastroenterol., 3.","DOI":"10.1186\/1471-230X-3-31"},{"key":"ref_48","first-page":"817","article-title":"The Infection by Helicobacter pylori Strains Expressing CagA Is Highly Prevalent in Women with Autoimmune Thyroid Disorders","volume":"50","author":"Figura","year":"1999","journal-title":"J. Physiol. Pharmacol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1179\/000349804225003190","article-title":"Prevalence of Helicobacter pylori Infection among Adult Dyspeptic Patients in Ethiopia","volume":"98","author":"Asrat","year":"2004","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"7279","DOI":"10.19082\/7279","article-title":"Prevalence and Factors Associated with H. pylori Infection in Saudi Patients with Dyspepsia","volume":"10","author":"Akeel","year":"2018","journal-title":"Electron. Physician"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1016\/j.dld.2017.03.019","article-title":"Sex-Differences in the Prevalence of Helicobacter pylori Infection in Pediatric and Adult Populations: Systematic Review and Meta-Analysis of 244 Studies","volume":"49","author":"Ibrahim","year":"2017","journal-title":"Dig. Liver Dis."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e14359","DOI":"10.2196\/14359","article-title":"Survival Rate of Gastric Cancer Patients in Jordan: Secondary Data Analysis","volume":"6","author":"Aqel","year":"2020","journal-title":"JMIR Public Health Surveill."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"31146","DOI":"10.18632\/oncotarget.25757","article-title":"Helicobacter pylori-Associated Factors in the Development of Gastric Cancer with Special Reference to the Early-Onset Subtype","volume":"9","author":"Machlowska","year":"2018","journal-title":"Oncotarget"},{"key":"ref_54","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 Patients: An Association with Histopathological Parameters","volume":"35","author":"Lima","year":"2011","journal-title":"Cancer Epidemiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"e85","DOI":"10.1016\/j.ijid.2009.11.022","article-title":"Molecular Characterization and Susceptibility Testing of Helicobacter pylori Strains Isolated in Western Argentina","volume":"14","author":"Vega","year":"2010","journal-title":"Int. J. Infect. Dis."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"125","DOI":"10.4103\/1319-3767.48971","article-title":"A Study of Helicobacter pylori Associated Gastritis Patterns in Iraq and Their Association with Strain Virulence","volume":"15","author":"Hussein","year":"2009","journal-title":"Saudi J. Gastroenterol."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Al Mutawa, O.A., Izhari, M.A., Alharbi, R.A., Sindi, A.A.A., Alqarni, A.M., Alotaibi, F.E., Gosady, A.R.A., Dardari, D.M.M., Almutairi, A.M., and Alshehri, M. (2023). Helicobacter pylori (H. pylori) Infection-Associated Anemia in the Asir Region, Saudi Arabia. Diagnostics, 13.","DOI":"10.3390\/diagnostics13142404"},{"key":"ref_58","first-page":"576","article-title":"Gastric Cancer in Iran: Epidemiology and Risk Factors","volume":"12","author":"Malekzadeh","year":"2009","journal-title":"Arch. Iran. Med."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1320","DOI":"10.21037\/atm-22-5553","article-title":"Correlation Analysis of Gastric Mucosal Lesions with Helicobacter pylori Infection and Its Virulence Genotype in Guiyang, Guizhou Province, China","volume":"10","author":"Hu","year":"2022","journal-title":"Ann. Transl. Med."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3226","DOI":"10.3748\/wjg.v16.i26.3226","article-title":"Helicobacter pylori and Gastric Cancer in the Middle East: A New Enigma?","volume":"16","author":"Hussein","year":"2010","journal-title":"World J. Gastroenterol."},{"key":"ref_61","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_62","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.ajg.2016.04.001","article-title":"Study of the Clinical Relevance of Helicobacter pylori Virulence Genes to Gastric Diseases among Egyptian Patients","volume":"17","author":"Rahman","year":"2016","journal-title":"Arab J. Gastroenterol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2622","DOI":"10.1128\/JCM.40.7.2622-2625.2002","article-title":"Virulence Genes in Helicobacter pylori Strains from West Bengal Residents with Overt H. pylori-Associated Disease and Healthy Volunteers","volume":"40","author":"Chattopadhyay","year":"2002","journal-title":"J. Clin. Microbiol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"46","DOI":"10.14740\/gr947w","article-title":"Analysis of Helicobacter pylori Genotypes amongst Jordanians\u2019 Dental Plaque Samples","volume":"11","author":"Alzoubi","year":"2018","journal-title":"Gastroenterol. Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1128\/CDLI.6.4.489-493.1999","article-title":"Detection of Anti-VacA Antibody Responses in Serum and Gastric Juice Samples Using Type s1\/m1 and s2\/m2 Helicobacter pylori VacA Antigens","volume":"6","author":"Peek","year":"1999","journal-title":"Clin. Diagn. Lab. Immunol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"20","DOI":"10.55145\/ajbms.2023.1.2.004","article-title":"Correlation between H. pylori Infection and Serum Levels of Inflammatory Markers: A Retrospective Study","volume":"2","author":"Rasool","year":"2023","journal-title":"Al-Salam J. Med. Sci."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1039\/D4MD00511B","article-title":"Azo Derivatives of Monoterpenes as Anti-Helicobacter pylori Agents: From Synthesis to Structure-Based Target Investigation","volume":"16","author":"Melfi","year":"2024","journal-title":"RSC Med. Chem."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"132","DOI":"10.4103\/jpbs.jpbs_850_21","article-title":"In Silico and In Vitro Investigation of Anti Helicobacter Activity of Selected Phytochemicals","volume":"14","author":"Aburjai","year":"2022","journal-title":"J. Pharm. Bioallied Sci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1724","DOI":"10.1136\/gutjnl-2022-327745","article-title":"Management of Helicobacter pylori Infection: The Maastricht VI\/Florence Consensus Report","volume":"71","author":"Malfertheiner","year":"2022","journal-title":"Gut"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Nguyen, T.K.C., Do, H.D.K., Nguyen, T.L.P., Pham, T.T., Mach, B.N., Nguyen, T.C., Pham, T.L., Katsande, P.M., Hong, H.A., and Duong, H.T. (2024). Genomic and Vaccine Preclinical Studies Reveal a Novel Mouse-Adapted Helicobacter pylori Model for the hpEastAsia Genotype in Southeast Asia. J. Med. 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