{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,28]],"date-time":"2026-03-28T06:00:29Z","timestamp":1774677629646,"version":"3.50.1"},"reference-count":22,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2020,6,18]],"date-time":"2020-06-18T00:00:00Z","timestamp":1592438400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["18K07148"],"award-info":[{"award-number":["18K07148"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Persistent gastric mucosal damage caused by Helicobacter pylori infection is a major risk factor for gastric cancer (GC). The Epstein\u2013Barr virus (EBV) is also associated with GC. Most patients with EBV-associated GC are infected with H. pylori in East Asia. However, very few reports have described where and when both H. pylori and EBV infect the gastric mucosa. To clarify this, old biopsy samples used for the rapid urease test (RUT) were applied to count EBV genomic DNA (gDNA) copies using DNA probe quantitative polymerase chain reaction. DNA extracted from the gastric biopsy samples of 58 patients with atrophic gastritis was used to analyze the correlation between the degree of atrophic gastritis and the copy number of EBV gDNA. EBV was detected in 44 cases (75.9%), with viral copy numbers ranging from 12.6 to 4754.6. A significant correlation was found between patients with more than 900 copies of EBV gDNA and those with a more severe grade of atrophic gastritis (p = 0.041). This study shows that EBV can be detected in RUT samples in a manner that reduces patient burden.<\/jats:p>","DOI":"10.3390\/microorganisms8060923","type":"journal-article","created":{"date-parts":[[2020,6,18]],"date-time":"2020-06-18T11:00:56Z","timestamp":1592478056000},"page":"923","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Application of Biopsy Samples Used for Helicobacter pylori Urease Test to Predict Epstein\u2013Barr Virus-Associated Cancer"],"prefix":"10.3390","volume":"8","author":[{"given":"Andy Visi","family":"Kartika","sequence":"first","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Shimane University, 89-1 Enya, Izumo, Shimane 693-8504, Japan"},{"name":"Department of Pathology Anatomy, Faculty of Medicine, University of Muslim Indonesia, Jl. Urip Sumoharjo KM.5, Makassar, Sulawesi 90231, Indonesia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9202-2666","authenticated-orcid":false,"given":"Hisashi","family":"Iizasa","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Shimane University, 89-1 Enya, Izumo, Shimane 693-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dan","family":"Ding","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Shimane University, 89-1 Enya, Izumo, Shimane 693-8504, Japan"},{"name":"Department of Neurobiology, Key Laboratory of Craniocerebral Disease, Ningxia Medical University, 1160 Shengli St, Xingqing District, Yinchuan 750004, Ningxia, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuichi","family":"Kanehiro","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Shimane University, 89-1 Enya, Izumo, Shimane 693-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yoshitsugu","family":"Tajima","sequence":"additional","affiliation":[{"name":"Department of digestive and general surgery, Faculty of Medicine, Shimane University, 89-1 Enya, Izumo, Shimane 693-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shunsuke","family":"Kaji","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Shimane University, 89-1 Enya, Izumo, Shimane 693-8504, Japan"},{"name":"Department of digestive and general surgery, Faculty of Medicine, Shimane University, 89-1 Enya, Izumo, Shimane 693-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hideo","family":"Yanai","sequence":"additional","affiliation":[{"name":"Department of Clinical Research, National Hospital Organization Kanmon Medical Center, 1-1 Chofu-Sotoura, Shimonoseki, Yamaguchi 752-8510, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7588-278X","authenticated-orcid":false,"given":"Hironori","family":"Yoshiyama","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Medicine, Shimane University, 89-1 Enya, Izumo, Shimane 693-8504, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,6,18]]},"reference":[{"key":"ref_1","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_2","doi-asserted-by":"crossref","first-page":"3456264","DOI":"10.1155\/2017\/3456264","article-title":"Status of Epstein-Barr virus coinfection with Helicobacter pylori in gastric cancer","volume":"2017","author":"Singh","year":"2017","journal-title":"J. Oncol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3420","DOI":"10.3390\/v4123420","article-title":"Epstein-Barr virus (EBV)-associated gastric carcinoma","volume":"4","author":"Iizasa","year":"2012","journal-title":"Viruses"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","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_5","doi-asserted-by":"crossref","first-page":"e00649-18","DOI":"10.1128\/mBio.00649-18","article-title":"Epigenetic regulation of tumor suppressors by Helicobacter pylori enhances EBV-induced proliferation of gastric epithelial cells","volume":"9","author":"Pandey","year":"2018","journal-title":"mBio"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Nishikawa, J., Shuto, T., Yanagi, A., Takagi, T., Ogawa, R., Sasaki, S., Goto, A., Hamabe, K., Hashimoto, S., and Okamoto, T. (2020). Epstein-Barr virus-associated gastric carcinomas developed after successful eradication of Helicobacter pylori. Clin. J. Gastroenterol., 1\u20136.","DOI":"10.1007\/s12328-020-01094-8"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1097\/00004836-199907000-00010","article-title":"Epstein-Barr virus-associated gastric carcinoma and atrophic gastritis","volume":"29","author":"Yanai","year":"1999","journal-title":"J. Clin. Gastroenterol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"11450","DOI":"10.3748\/wjg.v21.i40.11450","article-title":"Dysbiotic infection in the stomach","volume":"21","author":"Iizasa","year":"2015","journal-title":"World J. Gastroenterol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"9131","DOI":"10.1073\/pnas.91.19.9131","article-title":"Gastric carcinoma: Monoclonal epithelial malignant cells expressing Epstein-Barr virus latent infection protein","volume":"91","author":"Imai","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"E431","DOI":"10.1055\/a-0859-7233","article-title":"Epstein-Barr virus detection using gastric biopsy specimens after rapid urease test for Helicobacter pylori","volume":"7","author":"Yanai","year":"2019","journal-title":"Endosc. Int. Open"},{"key":"ref_11","first-page":"39","article-title":"Quantitative analysis of Epstein-Barr virus load by using a real-time PCR assay","volume":"29","author":"Kimura","year":"1999","journal-title":"J. Clin. Microbiol."},{"key":"ref_12","first-page":"154","article-title":"Epstein-Barr virus episome stability is coupled to a delay in replication timing","volume":"85","author":"Zhou","year":"2009","journal-title":"J. Virol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1385\/IJGC:34:2-3:087","article-title":"Evaluation of Epstein-Barr virus DNA load in gastric mucosa with chronic atrophic gastritis using a real-time quantitative PCR assay","volume":"34","author":"Hirano","year":"2003","journal-title":"Int. J. Gastrointest. Cancer"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2373","DOI":"10.1099\/0022-1317-82-10-2373","article-title":"Roles of Epstein-Barr virus glycoproteins gp350 and gp25 in the infection of human epithelial cells","volume":"82","author":"Maruo","year":"2001","journal-title":"J. Gen. Virol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1055\/s-0028-1098086","article-title":"An endoscopic recognition of the atrophic border and its significance in chronic gastritis","volume":"3","author":"Kimura","year":"1969","journal-title":"Endoscopy"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"3547","DOI":"10.1182\/blood-2012-09-454694","article-title":"Plasma Epstein-Barr virus DNA predicts outcome in advanced Hodgkin lymphoma: Correlative analysis from a large North American cooperative group trial","volume":"121","author":"Kanakry","year":"2013","journal-title":"Blood"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.1002\/jmv.24161","article-title":"Large-scale multiplex polymerase chain reaction assay for diagnosis of viral reactivations after allogeneic hematopoietic stem cell transplantation","volume":"87","author":"Inazawa","year":"2015","journal-title":"J. Med. Virol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1261\/rna.042507.113","article-title":"Tissue-specific gene silencing monitored in circulating RNA","volume":"20","author":"Sehgal","year":"2014","journal-title":"RNA"},{"key":"ref_19","first-page":"9064952","article-title":"Diagnosis of helicobacter pylori using invasive and noninvasive approaches","volume":"2018","author":"Abadi","year":"2018","journal-title":"J. Pathog."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"110","DOI":"10.4103\/1319-3767.61238","article-title":"Accuracy of rapid urease test in diagnosing Helicobacter pylori infection in patients using NSAIDs","volume":"16","author":"Foroutan","year":"2010","journal-title":"Saudi J. Gastroenterol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"84","DOI":"10.4103\/1319-3767.74441","article-title":"Inefficiency of rapid urease test for confirmation of Helicobacter pylori","volume":"17","author":"Abadi","year":"2011","journal-title":"Saudi J. Gastroenterol."},{"key":"ref_22","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."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/8\/6\/923\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:40:30Z","timestamp":1760175630000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/8\/6\/923"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,18]]},"references-count":22,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2020,6]]}},"alternative-id":["microorganisms8060923"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms8060923","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,6,18]]}}}