{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T08:47:26Z","timestamp":1790844446476,"version":"4.1.0"},"reference-count":52,"publisher":"SAGE Publications","issue":"4","license":[{"start":{"date-parts":[[2022,4,1]],"date-time":"2022-04-01T00:00:00Z","timestamp":1648771200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.sagepub.com\/page\/policies\/text-and-data-mining-license"}],"content-domain":{"domain":["journals.sagepub.com"],"crossmark-restriction":true},"short-container-title":["Microbial Drug Resistance"],"published-print":{"date-parts":[[2022,4,1]]},"abstract":"\n Aims:<\/jats:title>\n The aim of this study was to investigate the role of resident bacteriophages in hospital effluents, as a potential reservoir of extended-spectrum beta-lactamase (ESBL) genes.<\/jats:p>\n <\/jats:sec>\n \n Methods:<\/jats:title>\n Effluent samples were collected from four major medical centers in Azerbaijan. Phage enrichments were prepared and purified using standard subculturing, amplification, and phage purification protocols. DNA materials from phage stocks and bacterial isolates were examined for the presence of ESBL genes using polymerase chain reaction. Restriction fragment length polymorphism (RFLP) profiles were used for the construction of a dendrogram and cluster analysis.<\/jats:p>\n <\/jats:sec>\n \n Results:<\/jats:title>\n \n A total of 112 phage enrichments were obtained from 48 effluent samples against resident bacterial hosts. A total of 95 nonduplicate Gram-negative isolates were recovered from effluent samples. The most common isolate was\n Escherichia coli<\/jats:italic>\n (\n n<\/jats:italic>\n \u2009=\u200948), followed by\n Klebsiella pneumoniae<\/jats:italic>\n (\n n<\/jats:italic>\n \u2009=\u200918),\n Pseudomonas<\/jats:italic>\n spp. (\n n<\/jats:italic>\n \u2009=\u20099), and\n Enterobacter cloacae<\/jats:italic>\n (\n n<\/jats:italic>\n \u2009=\u20096). Thirty-two EcoRV-RFLP profiles consisting of \u223c4 to 20 bands were obtained for the 40\n E. coli<\/jats:italic>\n phage enrichments. ESBL genes were detected in 23 of 40 (57.5%)\n E. coli<\/jats:italic>\n phage enrichments, including\n bla<\/jats:italic>\n CTX-M<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u200915),\n bla<\/jats:italic>\n TEM<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u200914), and\n bla<\/jats:italic>\n SHV<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u20096). Detected genes in phage enrichments against resident hosts other than\n E. coli<\/jats:italic>\n include\n bla<\/jats:italic>\n TEM<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u20094),\n bla<\/jats:italic>\n CTX-M<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u20093), and\n bla<\/jats:italic>\n SHV<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u20091). A total of 63 (66.3%) bacterial isolates were positive for tested genes, including\n bla<\/jats:italic>\n CTX-M<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u200932),\n bla<\/jats:italic>\n TEM<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u200961), and\n bla<\/jats:italic>\n SHV<\/jats:sub>\n (\n n<\/jats:italic>\n \u2009=\u200912). The present research provides a strong evidence for the possible role of bacteriophages in antimicrobial resistance genes circulation in Azerbaijan clinical settings through generalized transduction.\n <\/jats:p>\n <\/jats:sec>\n \n Conclusions:<\/jats:title>\n Our results showed a remarkable occurrence of ESBL genes in bacteriophage and bacterial population of effluent discharge, which clearly indicates that bacteriophages are an important factor in ESBL genes exchange among bacterial population through generalized transduction.<\/jats:p>\n <\/jats:sec>","DOI":"10.1089\/mdr.2021.0163","type":"journal-article","created":{"date-parts":[[2022,1,25]],"date-time":"2022-01-25T08:56:55Z","timestamp":1643101015000},"page":"436-443","update-policy":"https:\/\/doi.org\/10.1177\/sage-journals-update-policy","source":"Crossref","is-referenced-by-count":10,"title":["The Role of Bacteriophages as Important Reservoirs of Extended-Spectrum Beta-Lactamase Genes in Azerbaijan Hospitals"],"prefix":"10.1177","volume":"28","author":[{"given":"Sahar","family":"Mahdavi","sequence":"first","affiliation":[{"name":"Department of Microbiology, Zanjan Branch, Islamic Azad University, Zanjan, Iran."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohammadreza","family":"Sadeghi","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, Maku Branch, Islamic Azad University, Maku, Iran."},{"name":"Department of Clinical Microbiology, Faculty of Medical Sciences, Urmia Branch, Islamic Azad University, Urmia, Iran."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rasoul","family":"Shokri","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Zanjan Branch, Islamic Azad University, Zanjan, Iran."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Babak","family":"Sadegh","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, Faculty of Medical Sciences, Urmia Branch, Islamic Azad University, Urmia, Iran."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"179","published-online":{"date-parts":[[2022,4,18]]},"reference":[{"key":"e_1_3_5_2_2","doi-asserted-by":"publisher","DOI":"10.2147\/IDR.S55778"},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.4137\/PMC.S14459"},{"key":"e_1_3_5_4_2","doi-asserted-by":"publisher","DOI":"10.3390\/w12123313"},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.plasmid.2013.03.010"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.1128\/MMBR.00020-10"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2011.0207"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.71.12.8301-8304.2005"},{"key":"e_1_3_5_9_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00457-11"},{"key":"e_1_3_5_10_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.01435-07"},{"key":"e_1_3_5_11_2","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.057943-0"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1473-3099(18)30605-4"},{"key":"e_1_3_5_13_2","unstructured":"Scott R.D. 2009. The direct medical costs of healthcare-associated infections in US hospitals and the benefits of prevention. Available at https:\/\/www.cdc.gov\/hai\/pdfs\/hai\/scott costpaper.pdf."},{"key":"e_1_3_5_14_2","doi-asserted-by":"publisher","DOI":"10.1001\/jama.2009.1754"},{"key":"e_1_3_5_15_2","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.18.4.657-686.2005"},{"key":"e_1_3_5_16_2","unstructured":"Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States .2013. Available at www.cdc.gov\/drugresistance\/threat-report-2013\/pdf\/ar-threats-2013-508.pdf."},{"key":"e_1_3_5_17_2","first-page":"320","article-title":"Extended-spectrum \u03b2-lactamase-producing and third-generation cephalosporin-resistant Enterobacteriaceae in children","volume":"3","author":"Logan L.K.","year":"2014","unstructured":"Logan L.K., , Braykov N.P, , Weinstein R.A, , and Laxminarayan R.. 2014. Extended-spectrum \u03b2-lactamase-producing and third-generation cephalosporin-resistant Enterobacteriaceae in children. Trends in the United States, 1999\u20132011. J. Pediatr. Infect. Dis. Soc. 3:320\u2013328.","journal-title":"Trends in the United States, 1999\u20132011. J. Pediatr. Infect. Dis. Soc"},{"key":"e_1_3_5_18_2","doi-asserted-by":"publisher","DOI":"10.1089\/mdr.2009.0096"},{"key":"e_1_3_5_19_2","doi-asserted-by":"publisher","DOI":"10.5812\/jjm.31179"},{"key":"e_1_3_5_20_2","doi-asserted-by":"publisher","DOI":"10.3855\/jidc.488"},{"key":"e_1_3_5_21_2","volume-title":"Klebsiella pneumoniae","author":"Najar Peerayeh S.","unstructured":"Najar Peerayeh S., , Rostami E., , Eslami M., , and Ahangarzadeh Rezaee M.. 2016. High frequency of extended-spectrum \u03b2-lactamase-producing Klebsiella pneumoniae. and, Escherichia coli, isolates from male patients' urine. Arch. Clin. Infect. Dis. 11: e6, 0127."},{"key":"e_1_3_5_22_2","volume-title":"Escherichia coli","author":"Ghaderi R.S.","unstructured":"Ghaderi R.S., , Yaghoubi A., , Amirfakhrian R., , Hashemy S.I, , and Ghazvini K., . 2020. The prevalence of genes encoding Eamong clinical isolates of SBL. Escherichia coli. in Iran: a systematic review and meta-analysis. Gene. Rep. 18:10, 0562."},{"key":"e_1_3_5_23_2","first-page":"1257","article-title":"Molecular epidemiology of ESBL genes and multi-drug resistance in diarrheagenic Escherichia coli strains isolated from adults in Iran","volume":"14","author":"Ghorbani-Dalini S.","year":"2015","unstructured":"Ghorbani-Dalini S., , Kargar M., , Doosti A., , Abbasi P., , and Sarshar M.. 2015. Molecular epidemiology of ESBL genes and multi-drug resistance in diarrheagenic Escherichia coli strains isolated from adults in Iran. Iran. J. Pharm. Res. 14:1257\u20131262.","journal-title":"Iran. J. Pharm. Res"},{"key":"e_1_3_5_24_2","doi-asserted-by":"publisher","DOI":"10.1099\/jmm.0.000356"},{"key":"e_1_3_5_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jgar.2019.01.020"},{"key":"e_1_3_5_26_2","doi-asserted-by":"publisher","DOI":"10.34172\/ajcmi.2018.18"},{"key":"e_1_3_5_27_2","first-page":"536","volume":"19","author":"Nematolahi S.","year":"2016","unstructured":"Nematolahi S., , Mosadegh A., , Mardaneh J., , and Poorabbas B.. 2016. Identification of ESBL-producing and blaSHV gene harboring Enterobacter spp. isolated from bloodstream infections of hospitalized patients during 10 Years in south of Iran (Shiraz). BPUMS. 19:536\u2013548.","journal-title":"Identification of ESBL-producing and blaSHV gene harboring Enterobacter spp. isolated from bloodstream infections of hospitalized patients during 10 Years in south of Iran (Shiraz). BPUMS"},{"key":"e_1_3_5_28_2","first-page":"Iran","article-title":"Clonal relation and antimicrobial resistance pattern of extended-spectrum \u03b2-lactamase- and AmpC \u03b2-lactamase-producing Enterobacter spp","author":"Ghanavati R.","year":"2018","unstructured":"Ghanavati R., , Emaneini M., , Kalantar-Neyestanaki D., et al. 2018. Clonal relation and antimicrobial resistance pattern of extended-spectrum \u03b2-lactamase- and AmpC \u03b2-lactamase-producing Enterobacter spp. isolated from different clinical samples in, Tehran, Iran. Rev. Soc. Bras. Med. Trop. 51:88\u201393.","journal-title":"isolated from different clinical samples in"},{"key":"e_1_3_5_29_2","author":"Malekjamshidi M.R.","unstructured":"Malekjamshidi M.R., F. Shahcheraghi, and M.M. Feizabadi.2010. Detection and PFGE analysis of ESBL-producing isolates of Proteus species isolated from patients at Tehran hospitals. Med. Sci. Monit. 16:Br327\u2013Br332.","journal-title":"Proteus"},{"key":"e_1_3_5_30_2","author":"Bialvaei A.Z.","unstructured":"Bialvaei A.Z., T. Pourlak, M. Aghamali, M. Asgharzadeh, P. Gholizadeh, H.S. Kafil.2017. The prevalence of CTX-M-15 extended-spectrum \u03b2-Lactamases among Salmonella spp. and Shigella spp. Isolated from three Iranian Hospitals. Eur. J. Microbiol. Immunol. 7:133\u2013137.","journal-title":"Salmonella"},{"key":"e_1_3_5_31_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1004219"},{"key":"e_1_3_5_32_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.plasmid.2015.01.001"},{"key":"e_1_3_5_33_2","doi-asserted-by":"publisher","DOI":"10.1186\/s40168-020-00863-4"},{"key":"e_1_3_5_34_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.00173"},{"key":"e_1_3_5_35_2","first-page":"73","article-title":"Abundance of antibiotic resistance genes in bacteria and bacteriophages isolated from wastewater in Shiraz","volume":"10","author":"Zare S.","year":"2021","unstructured":"Zare S., , Derakhshandeh A., , Mohammadi A., , and Noshadi M.. 2021. Abundance of antibiotic resistance genes in bacteria and bacteriophages isolated from wastewater in Shiraz. Mol. Biol. Res. Commun. 10:73\u201383.","journal-title":"Mol. Biol. Res. Commun"},{"key":"e_1_3_5_36_2","unstructured":"Center for Phage Technology Texas A&University M. 2011. Phage enrichments. Available at https:\/\/cpt.tamu.edu\/wordpress\/wp-content\/uploads\/2011\/12\/Phage-enrichments-07-12-2011.pdf."},{"key":"e_1_3_5_37_2","unstructured":"Clinical and Laboratory Standards Institute. 2021. Performance Standards for Antimicrobial Susceptibility Testing. 31st ed. CLSI document M100. Wayne PA."},{"key":"e_1_3_5_38_2","unstructured":"Center for Phage Technology Texas A&University M. 2011. Subculturing phage isolates. Available at https:\/\/cpt.tamu.edu\/wordpress\/wp-content\/uploads\/2011\/12\/Subculturing-phage-isolates-07-12-2011.pdf."},{"key":"e_1_3_5_39_2","first-page":"1919","volume":"106","author":"Oliveira A.","year":"2009","unstructured":"Oliveira A., , Sillankorva S., , Quinta R., , Henriques A., , Sereno R., , and Azeredo J.. 2009. Isolation and characterization of bacteriophages for avian pathogenic E. coli strains. J. Appl. Microbiol. 106:1919\u20131927.","journal-title":"Isolation and characterization of bacteriophages for avian pathogenic E. coli strains. J. Appl. Microbiol"},{"key":"e_1_3_5_40_2","doi-asserted-by":"publisher","DOI":"10.1093\/jac\/dkp498"},{"key":"e_1_3_5_41_2","unstructured":"National Center for Biotechnology Information. Available at https:\/\/www.ncbi.nlm.nih.gov\/pathogens\/antimicrobial-resistance\/AMRFinder\/"},{"key":"e_1_3_5_42_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.watres.2016.03.006"},{"key":"e_1_3_5_43_2","doi-asserted-by":"publisher","DOI":"10.1128\/AAC.00535-11"},{"key":"e_1_3_5_44_2","doi-asserted-by":"publisher","DOI":"10.1111\/1469-0691.12446"},{"key":"e_1_3_5_45_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijantimicag.2016.04.028"},{"key":"e_1_3_5_46_2","doi-asserted-by":"publisher","DOI":"10.1099\/jgv.0.000639"},{"key":"e_1_3_5_47_2","doi-asserted-by":"publisher","DOI":"10.1038\/ismej.2016.90"},{"key":"e_1_3_5_48_2","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.8.4.557"},{"key":"e_1_3_5_49_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.envint.2014.07.003"},{"key":"e_1_3_5_50_2","doi-asserted-by":"publisher","DOI":"10.1128\/AAC.01684-13"},{"key":"e_1_3_5_51_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2012.00110"},{"key":"e_1_3_5_52_2","doi-asserted-by":"publisher","DOI":"10.2147\/IDR.S160720"},{"key":"e_1_3_5_53_2","first-page":"79","article-title":"Prevalence and antimicrobial susceptibility patterns of ESBL, AmpC and carbapenemase-producing Enterobactericeae isolated from hospitalized patients in Azerbaijan, Iran","volume":"17","author":"Ghotaslou R.","year":"2018","unstructured":"Ghotaslou R., , Sadeghi M.R, , Akhi M.T, , Hasani A., , and Asgharzadeh M.. 2018. Prevalence and antimicrobial susceptibility patterns of ESBL, AmpC and carbapenemase-producing Enterobactericeae isolated from hospitalized patients in Azerbaijan, Iran. Iran. J. Pharm. Res. 17:79\u201388.","journal-title":"Iran. J. Pharm. Res"}],"container-title":["Microbial Drug Resistance"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.sagepub.com\/doi\/full-xml\/10.1089\/mdr.2021.0163","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1089\/mdr.2021.0163","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1089\/mdr.2021.0163","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,1]],"date-time":"2026-05-01T20:39:36Z","timestamp":1777667976000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.sagepub.com\/doi\/10.1089\/mdr.2021.0163"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,1]]},"references-count":52,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2022,4,1]]}},"alternative-id":["10.1089\/mdr.2021.0163"],"URL":"https:\/\/doi.org\/10.1089\/mdr.2021.0163","relation":{},"ISSN":["1076-6294","1931-8448"],"issn-type":[{"value":"1076-6294","type":"print"},{"value":"1931-8448","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,1]]}}}