{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T02:56:29Z","timestamp":1790218589919,"version":"4.1.0"},"reference-count":71,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2020,2,6]],"date-time":"2020-02-06T00:00:00Z","timestamp":1580947200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Epstein\u2013Barr virus (EBV) and Helicobacter pylori (H. pylori) are two pathogens associated with the development of various human cancers. The coexistence of both microorganisms in gastric cancer specimens has been increasingly reported, suggesting that crosstalk of both pathogens may be implicated in the carcinogenesis process. Considering that chronic inflammation is an initial step in the development of several cancers, including gastric cancer, we conducted a systematic review to comprehensively evaluate publications in which EBV and H. pylori co-infection has been documented in patients with non-malignant gastroduodenal disorders (NMGDs), including gastritis, peptic ulcer disease (PUD), and dyspepsia. We searched the PubMed database up to August 2019, as well as publication references and, among the nine studies that met the inclusion criteria, we identified six studies assessing EBV infection directly in gastric tissues (total 949 patients) and three studies in which EBV infection status was determined by serological methods (total 662 patients). Due to the substantial methodological and clinical heterogeneity among studies identified, we could not conduct a meta-analysis. The overall prevalence of EBV + H. pylori co-infection in NMGDs was 34% (range 1.8% to 60%). A higher co-infection rate (EBV + H. pylori) was reported in studies in which EBV was documented by serological methods in comparison with studies in which EBV infection was directly assessed in gastric specimens. The majority of these studies were conducted in Latin-America and India, with most of them comparing NMGDs with gastric cancer, but there were no studies comparing the co-infection rate in NMGDs with that in asymptomatic individuals. In comparison with gastritis caused by only one of these pathogens, EBV + H. pylori co-infection was associated with increased severity of gastric inflammation. In conclusion, only relatively small studies testing EBV and H. pylori co-infection in NMGDs have been published to date and the variable report results are likely influenced by geographic factors and detection methods.<\/jats:p>","DOI":"10.3390\/pathogens9020104","type":"journal-article","created":{"date-parts":[[2020,2,7]],"date-time":"2020-02-07T03:13:27Z","timestamp":1581045207000},"page":"104","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":41,"title":["Epstein\u2013Barr Virus and Helicobacter Pylori Co-Infection in Non-Malignant Gastroduodenal Disorders"],"prefix":"10.3390","volume":"9","author":[{"given":"Rams\u00e9s","family":"D\u00e1vila-Collado","sequence":"first","affiliation":[{"name":"Faculty of Medicine, UNIDES University, Managua 11001, Nicaragua"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Oscar","family":"Jarqu\u00edn-Dur\u00e1n","sequence":"additional","affiliation":[{"name":"Faculty of Medicine, UNIDES University, Managua 11001, Nicaragua"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Le Thanh","family":"Dong","sequence":"additional","affiliation":[{"name":"Faculty of Medical Technology, Hanoi Medical University, Hanoi 116001, Vietnam"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1794-6666","authenticated-orcid":false,"given":"J. Luis","family":"Espinoza","sequence":"additional","affiliation":[{"name":"Faculty of Health Sciences, Kanazawa University, Kodatsuno 5-11-80, Kanazawa 920-0942, Ishikawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,2,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1380","DOI":"10.1053\/j.gastro.2016.02.011","article-title":"Gastroduodenal Disorders","volume":"150","author":"Stanghellini","year":"2016","journal-title":"Gastroenterology"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1853","DOI":"10.1056\/NEJMra1501505","article-title":"Functional Dyspepsia","volume":"373","author":"Talley","year":"2015","journal-title":"N. Engl. J. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1134","DOI":"10.1111\/apt.15191","article-title":"Review article: Treatment options for functional dyspepsia","volume":"49","author":"Masuy","year":"2019","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1159\/000485408","article-title":"Functional Dyspepsia and Irritable Bowel Syndrome: Beyond Rome IV","volume":"35","author":"Stanghellini","year":"2017","journal-title":"Dig. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"213","DOI":"10.23736\/S0031-0808.18.03541-3","article-title":"Irritable bowel syndrome: The clinical approach","volume":"60","author":"Adriani","year":"2018","journal-title":"Panminerva Med."},{"key":"ref_6","first-page":"227","article-title":"Helicobacter pylori-Induced Changes in Gastric Acid Secretion and Upper Gastrointestinal Disease","volume":"400","author":"Smolka","year":"2017","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Falkeis-Veits, C., and Vieth, M. (2019). Non-malignant Helicobacter pylori-Associated Diseases. Adv. Exp. Med. Biol.","DOI":"10.1007\/5584_2019_362"},{"key":"ref_8","first-page":"280","article-title":"Benign and malignant gastroduodenal diseases associated with Helicobacter pylori: A narrative review and personal remarks in 2018","volume":"64","year":"2018","journal-title":"Minerva Gastroenterol. Dietol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1016\/S0140-6736(16)32404-7","article-title":"Peptic ulcer disease","volume":"390","author":"Lanas","year":"2017","journal-title":"Lancet"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"C\u00e1rdenas-Mondrag\u00f3n, M.G., Carre\u00f3n-Talavera, R., Camorlinga-Ponce, M., Gomez-Delgado, A., Torres, J., and Fuentes-Panan\u00e1, E.M. (2013). Epstein Barr virus and Helicobacter pylori co-infection are positively associated with severe gastritis in pediatric patients. PLoS ONE, 8.","DOI":"10.1371\/annotation\/865eaad7-8547-49ac-a42d-47e9d0755bb3"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"301","DOI":"10.3390\/v6010301","article-title":"Evidence of Epstein-Barr virus association with gastric cancer and non-atrophic gastritis","volume":"6","author":"Torres","year":"2014","journal-title":"Viruses"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Zong, L., and Seto, Y. (2014). CpG island methylator phenotype, Helicobacter pylori, Epstein-Barr virus, and microsatellite instability and prognosis in gastric cancer: A systematic review and meta-analysis. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0086097"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"808","DOI":"10.1111\/apm.12725","article-title":"Cytokine expression associated with Helicobacter pylori and Epstein-Barr virus infection in gastric carcinogenesis","volume":"125","author":"Kim","year":"2017","journal-title":"APMIS"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Rugge, M., Genta, R.M., Di Mario, F., El-Omar, E.M., El-Serag, H.B., Fassan, M., Hunt, R.H., Kuipers, E.J., Malfertheiner, P., and Sugano, K. (2017). Gastric Cancer as Preventable Disease. Clin. Gastroenterol. Hepatol.","DOI":"10.1016\/j.cgh.2017.05.023"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e14124","DOI":"10.1097\/MD.0000000000014124","article-title":"Multiple infections by EBV, HCMV and Helicobacter pylori are highly frequent in patients with chronic gastritis and gastric cancer from Southwest Mexico: An observational study","volume":"98","year":"2019","journal-title":"Medicine (Baltimore)"},{"key":"ref_16","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_17","doi-asserted-by":"crossref","unstructured":"Khoder, G., Muhammad, J.S., Mahmoud, I., Soliman, S.S.M., and Burucoa, C. (2019). Prevalence of Helicobacter pylori and Its Associated Factors among Healthy Asymptomatic Residents in the United Arab Emirates. Pathogens, 8.","DOI":"10.3390\/pathogens8020044"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1158","DOI":"10.1056\/NEJMcp1710945","article-title":"Infection","volume":"380","author":"Crowe","year":"2019","journal-title":"N. Engl. J. Med."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3964","DOI":"10.3748\/wjg.v23.i22.3964","article-title":"Molecular mimicry in Helicobacter pylori infections","volume":"23","author":"Chmiela","year":"2017","journal-title":"World J. Gastroenterol."},{"key":"ref_20","first-page":"53","article-title":"Immune Evasion Strategies and Persistence of Helicobacter pylori","volume":"400","author":"Gerhard","year":"2017","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1038\/nrmicro3016","article-title":"Life in the human stomach: Persistence strategies of the bacterial pathogen Helicobacter pylori","volume":"11","author":"Salama","year":"2013","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1080\/23744235.2019.1588472","article-title":"Helicobacter pylori: Molecular basis for colonization and survival in gastric environment and resistance to antibiotics. A short review","volume":"51","author":"Fagoonee","year":"2019","journal-title":"Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"713","DOI":"10.3389\/fonc.2019.00713","article-title":"The Global Landscape of EBV-Associated Tumors","volume":"9","author":"Rickinson","year":"2019","journal-title":"Front. Oncol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1002\/pbc.24654","article-title":"Epstein-Barr virus (EBV) positive classical Hodgkin lymphoma of Iraqi children: An immunophenotypic and molecular characterization of Hodgkin\/Reed-Sternberg cells","volume":"60","author":"Talerico","year":"2013","journal-title":"Pediatric Blood Cancer"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Espinoza, J.L., Takami, A., Trung, L.Q., Kato, S., and Nakao, S. (2012). Resveratrol Prevents EBV Transformation and Inhibits the Outgrowth of EBV-Immortalized Human B Cells. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0051306"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1146\/annurev-immunol-032414-112326","article-title":"The immunology of Epstein-Barr virus-induced disease","volume":"33","author":"Taylor","year":"2015","journal-title":"Annu. Rev. Immunol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e792","DOI":"10.1097\/MD.0000000000000792","article-title":"Epstein-Barr virus infection and gastric cancer: A systematic review","volume":"94","author":"Chen","year":"2015","journal-title":"Medicine (Baltimore)"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1099\/jmm.0.46580-0","article-title":"Helicobacter pylori-associated oxidant monochloramine induces reactivation of Epstein-Barr virus (EBV) in gastric epithelial cells latently infected with EBV","volume":"55","author":"Gotoh","year":"2006","journal-title":"J. Med. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3706","DOI":"10.4049\/jimmunol.1200591","article-title":"Nucleotide oligomerization domain 1 enhances IFN-\u03b3 signaling in gastric epithelial cells during Helicobacter pylori infection and exacerbates disease severity","volume":"190","author":"Allison","year":"2013","journal-title":"J. Immunol."},{"key":"ref_30","first-page":"7069242","article-title":"Elevated levels of Interferon-\u03b3 are associated with Epstein-Barr virus reactivation in patients with the intestinal type of gastric cancer","volume":"2017","author":"Torres","year":"2017","journal-title":"J. Immunol. Res."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Dixon, B.R.E.A., Hossain, R., Patel, R.V., and Algood, H.M.S. (2019). Th17 Cells in Helicobacter pylori Infection: A Dichotomy of Help and Harm. Infect. Immun., 87.","DOI":"10.1128\/IAI.00363-19"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1089\/vim.2014.0129","article-title":"Epstein-Barr Virus and Human herpes virus 6 Type A DNA Enhance IL-17 Production in Mice","volume":"28","author":"Rahal","year":"2015","journal-title":"Viral Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1111\/j.1523-5378.2008.00629.x","article-title":"IL-17 is involved in Helicobacter pylori-induced gastric inflammatory responses in a mouse model","volume":"13","author":"Shiomi","year":"2008","journal-title":"Helicobacter"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Salloum, N., Hussein, H.M., Jammaz, R., Jiche, S., Uthman, I.W., Abdelnoor, A.M., and Rahal, E.A. (2018). Epstein-Barr virus DNA modulates regulatory T-cell programming in addition to enhancing interleukin-17A production via Toll-like receptor 9. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0200546"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"e01243-14","DOI":"10.1128\/mBio.01243-14","article-title":"Systems modeling of the role of interleukin-21 in the maintenance of effector CD4+ T cell responses during chronic Helicobacter pylori infection","volume":"5","author":"Carbo","year":"2014","journal-title":"MBio"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5957","DOI":"10.4049\/jimmunol.178.9.5957","article-title":"IL-21 is highly produced in Helicobacter pylori-infected gastric mucosa and promotes gelatinases synthesis","volume":"178","author":"Caruso","year":"2007","journal-title":"J. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"61","DOI":"10.5114\/ceji.2015.50835","article-title":"Mucosal interleukin-21 mRNA expression level is high in patients with Helicobacter pylori and is associated with the severity of gastritis","volume":"40","author":"Bagheri","year":"2015","journal-title":"Cent.-Eur. J. Immunol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1189\/jlb.5A0516-217RR","article-title":"Synovial IL-21\/TNF-producing CD4","volume":"101","author":"Lebre","year":"2017","journal-title":"J. Leukoc. Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1128\/CVI.00002-13","article-title":"Interleukin-21 overexpression dominates T cell response to Epstein-Barr virus in a fatal case of X-linked lymphoproliferative syndrome type 1","volume":"20","author":"Ortega","year":"2013","journal-title":"Clin. Vaccine Immunol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., and Group, P. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med., 6.","DOI":"10.1371\/journal.pmed.1000097"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"31","DOI":"10.5501\/wjv.v1.i1.31","article-title":"Serological diagnosis of Epstein-Barr virus infection: Problems and solutions","volume":"1","author":"Clerici","year":"2012","journal-title":"World J. Virol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"211","DOI":"10.3389\/fonc.2018.00211","article-title":"Epstein-Barr Virus Epidemiology, Serology, and Genetic Variability of LMP-1 Oncogene Among Healthy Population: An Update","volume":"8","author":"Smatti","year":"2018","journal-title":"Front. Oncol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1177\/2050640615610265","article-title":"Co-infection with Helicobacter pylori and Epstein-Barr virus in benign upper digestive diseases: An endoscopic and serologic pilot study","volume":"4","year":"2016","journal-title":"United Eur. Gastroenterol. J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1556\/OH.2013.29630","article-title":"Changing prevalence of Helicobacter pylori infection in the 9th district of Budapest. A retrospective endoscopic study, 1997\u20132012","volume":"154","author":"Lotz","year":"2013","journal-title":"Orv. Hetil."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1866","DOI":"10.1038\/bjc.2015.175","article-title":"Case\u2013control study of Epstein\u2013Barr virus and Helicobacter pylori serology in Latin American patients with gastric disease","volume":"112","author":"Torres","year":"2015","journal-title":"Br. J. Cancer"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1080\/00365520801909660","article-title":"Association of Helicobacter pylori and Epstein-Barr virus with gastric cancer and peptic ulcer disease","volume":"43","author":"Saxena","year":"2008","journal-title":"Scand. J. Gastroenterol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1002\/jmv.10215","article-title":"Epstein-Barr virus-associated gastric carcinoma in southern India: A comparison with a large-scale Japanese series","volume":"68","author":"Kattoor","year":"2002","journal-title":"J. Med. Virol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"6096","DOI":"10.3748\/wjg.v11.i39.6096","article-title":"Epstein-Barr virus-associated gastric carcinoma: Evidence of age-dependence among a Mexican population","volume":"11","author":"Akiba","year":"2005","journal-title":"World J. Gastroenterol."},{"key":"ref_49","first-page":"1","article-title":"Prevalence of Helicobacter pylori infection, ist virulent genotypes, and Epstein-Barr virus in Peruvian patients with chronic gastritis and gastric cancer","volume":"5","author":"Castaneda","year":"2019","journal-title":"J. Glob. Oncol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"de Souza, C.R., de Oliveira, K.S., Ferraz, J.J., Leal, M.F., Calcagno, D.Q., Seabra, A.D., Khayat, A.S., Montenegro, R.C., Alves, A.P., and Assump\u00e7\u00e3o, P.P. (2014). Occurrence of Helicobacter pylori and Epstein-Barr virus infection in endoscopic and gastric cancer patients from Northern Brazil. BMC Gastroenterol., 14.","DOI":"10.1186\/1471-230X-14-179"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1289","DOI":"10.1002\/jmv.23322","article-title":"Expression profile of latent and lytic transcripts of epstein-barr virus in patients with gastroduodenal diseases: A study from northern India","volume":"84","author":"Shukla","year":"2012","journal-title":"J. Med. Virol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/S1413-8670(11)70255-0","article-title":"Epstein-Barr virus DNA load and its association with Helicobacter pylori infection in gastroduodenal diseases","volume":"15","author":"Shukla","year":"2011","journal-title":"Braz. J. Infect. Dis."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"123","DOI":"10.5223\/pghn.2013.16.2.123","article-title":"Co-Infection with Cytomegalovirus and Helicobacter pylori in a Child with M\u00e9n\u00e9trier\u2019s Disease","volume":"16","author":"Yoo","year":"2013","journal-title":"Pediatric Gastroenterol. Hepatol. Nutr."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Crespo, P., Dias, N., Marques, N., and Saraiva da Cunha, J. (2015). Gastritis as a manifestation of primary CMV infection in an immunocompetent host. BMJ Case Rep., 2015.","DOI":"10.1136\/bcr-2014-206991"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"379","DOI":"10.4253\/wjge.v2.i11.379","article-title":"Cytomegalovirus gastritis","volume":"2","author":"Hokama","year":"2010","journal-title":"World J. Gastrointest. Endosc."},{"key":"ref_56","first-page":"49","article-title":"Epstein-Barr virus-associated gastric carcinoma in Lima, Peru","volume":"24","author":"Yoshiwara","year":"2005","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1002\/ijc.23420","article-title":"Variation in the prevalence of gastric cancer in Per\u00fa","volume":"123","author":"Mendoza","year":"2008","journal-title":"Int. J. Cancer"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1590\/S0074-02762012000400021","article-title":"Helicobacter pylori vacA and cagA genotypes in patients from northeastern Brazil with upper gastrointestinal diseases","volume":"107","author":"Cavalcante","year":"2012","journal-title":"Mem. Inst. Oswaldo. Cruz."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"97","DOI":"10.3961\/jpmph.15.068","article-title":"Epstein-Barr Virus and Gastric Cancer Risk: A Meta-analysis With Meta-regression of Case-control Studies","volume":"49","author":"Bae","year":"2016","journal-title":"J. Prev. Med. Public Health"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1073\/pnas.0711183105","article-title":"Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse","volume":"105","author":"Ohnishi","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1186\/s12964-015-0111-0","article-title":"Helicobacter pylori virulence factor CagA promotes tumorigenesis of gastric cancer via multiple signaling pathways","volume":"13","author":"Yong","year":"2015","journal-title":"Cell Commun. Signal."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1016\/j.chom.2014.02.008","article-title":"Helicobacter pylori CagA and gastric cancer: A paradigm for hit-and-run carcinogenesis","volume":"15","author":"Hatakeyama","year":"2014","journal-title":"Cell Host Microbe"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"3916","DOI":"10.3748\/wjg.v20.i14.3916","article-title":"DNA methylation in gastric cancer, related to Helicobacter pylori and Epstein-Barr virus","volume":"20","author":"Matsusaka","year":"2014","journal-title":"World J. Gastroenterol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1002\/path.4731","article-title":"Combinatorial epigenetic deregulation by Helicobacter pylori and Epstein-Barr virus infections in gastric tumourigenesis","volume":"239","author":"Wu","year":"2016","journal-title":"J. Pathol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1007\/978-981-10-7230-7_20","article-title":"Gastritis-Infection-Cancer Sequence of Epstein-Barr Virus-Associated Gastric Cancer","volume":"1045","author":"Fukayama","year":"2018","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"16026","DOI":"10.1038\/nmicrobiol.2016.26","article-title":"Host SHP1 phosphatase antagonizes Helicobacter pylori CagA and can be downregulated by Epstein-Barr virus","volume":"1","author":"Saju","year":"2016","journal-title":"Nat. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Cui, H., Jin, Y., Chen, F., Ni, H., Hu, C., Xu, Y., Xuan, H., Hu, D., Deng, W., and Zhang, Y. (2019). Clinicopathological evidence of Hepatitis B Virus infection in the development of gastric adenocarcinoma. J. Med. Virol.","DOI":"10.1002\/jmv.25584"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.canlet.2017.11.009","article-title":"Gastric microbiota: An emerging player in Helicobacter pylori-induced gastric malignancies","volume":"414","author":"Espinoza","year":"2018","journal-title":"Cancer Lett."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1136\/gutjnl-2017-314281","article-title":"Mucosal microbiome dysbiosis in gastric carcinogenesis","volume":"67","author":"Coker","year":"2018","journal-title":"Gut"},{"key":"ref_70","first-page":"253","article-title":"Impact of the Microbiota and Gastric Disease Development by Helicobacter pylori","volume":"400","author":"Llorca","year":"2017","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Wakabayashi, R., Nakahama, Y., Nguyen, V., and Espinoza, J.L. (2019). The Host-Microbe Interplay in Human Papillomavirus-Induced Carcinogenesis. Microorganisms, 7.","DOI":"10.3390\/microorganisms7070199"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/2\/104\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T08:55:27Z","timestamp":1760172927000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/2\/104"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,6]]},"references-count":71,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2020,2]]}},"alternative-id":["pathogens9020104"],"URL":"https:\/\/doi.org\/10.3390\/pathogens9020104","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,6]]}}}