{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,11]],"date-time":"2026-10-11T03:33:48Z","timestamp":1791689628174,"version":"4.3.4"},"reference-count":57,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,4,28]],"date-time":"2022-04-28T00:00:00Z","timestamp":1651104000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the Government of Tanzania"},{"name":"the World bank"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>The interaction of rodents with humans and chicken in the household environment can facilitate transmission of multidrug-resistant (MDR) Escherichia coli (E. coli), causing infections that are difficult to treat. We investigated the presence of genes encoded for carbapenem, extended spectrum beta-lactamases (ESBL), tetracycline and quinolones resistance, and virulence among 50 MDR E. coli isolated from human (n = 14), chicken (n = 12), rodent (n = 10), and soil (n = 14) samples using multiplex polymerase chain reaction (PCR). Overall, the antimicrobial resistance genes (ARGs) detected were: blaTEM 23\/50 (46%), blaCTX-M 13\/50 (26%), tetA 23\/50 (46%), tetB 7\/50 (14%), qnrA 12\/50 (24%), qnrB 4\/50 (8%), blaOXA-48 6\/50 (12%), and blaKPC 3\/50 (6%), while blaIMP, blaVIM, and blaNDM-1 were not found. The virulence genes (VGs) found were: ompA 36\/50 (72%), traT 13\/50 (26%), east 9\/50 (18%), bfp 5\/50 (10%), eae 1\/50 (2%), and stx-1 2\/50 (4%), while hlyA and cnf genes were not detected. Resistance (blaTEM, blaCTX-M, blaSHV, tetA, tetB, and qnrA) and virulence (traT) genes were found in all sample sources while stx-1 and eae were only found in chicken and rodent isolates, respectively. Tetracycline resistance phenotypes correlated with genotypes tetA (r = 0.94), tetB (r = 0.90), blaKPC (r = 0.90; blaOXA-48 (r = 0.89), and qnrA (r = 0.96). ESBL resistance was correlated with genotypes blaKPC (r = 0.93), blaOXA-48 (r = 0.90), and qnrA (r = 0.96) resistance. Positive correlations were observed between resistance and virulence genes: qnrB and bfp (r = 0.63) also blaTEM, and traT (r = 0.51). Principal component analysis (PCA) indicated that tetA, tetB, blaTEM, blaCTX-M, qnrA, and qnrB genes contributed to tetracycline, cefotaxime, and quinolone resistance, respectively. While traT stx-1, bfp, ompA, east, and eae genes contributed to virulence of MDR E. coli isolates. The PCA ellipses show that isolates from rodents had more ARGs and virulence genes compared to those isolated from chicken, soil, and humans.<\/jats:p>","DOI":"10.3390\/ijerph19095388","type":"journal-article","created":{"date-parts":[[2022,4,28]],"date-time":"2022-04-28T12:06:01Z","timestamp":1651147561000},"page":"5388","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Molecular Epidemiology of Antibiotic Resistance Genes and Virulence Factors in Multidrug-Resistant Escherichia coli Isolated from Rodents, Humans, Chicken, and Household Soils in Karatu, Northern Tanzania"],"prefix":"10.3390","volume":"19","author":[{"given":"Valery Silvery","family":"Sonola","sequence":"first","affiliation":[{"name":"Department of Wildlife Management, College of Forestry, Wildlife and Tourism, Sokoine University of Agriculture, P.O. Box 3073, Morogoro 67125, Tanzania"},{"name":"Livestock Training Agency (LITA), Buhuri Campus, P.O. Box 1483, Tanga 21206, Tanzania"},{"name":"Africa Centre of Excellence for Innovative Rodent Pest Management and Biosensor Technology Development (ACE-IRPM & BTD), Pest Management Institute, Sokoine University of Agriculture, P.O. Box 3110, Morogoro 67125, Tanzania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abdul","family":"Katakweba","sequence":"additional","affiliation":[{"name":"Africa Centre of Excellence for Innovative Rodent Pest Management and Biosensor Technology Development (ACE-IRPM & BTD), Pest Management Institute, Sokoine University of Agriculture, P.O. Box 3110, Morogoro 67125, Tanzania"},{"name":"Institute of Pest Management, Sokoine University of Agriculture, P.O. Box 3110, Morogoro 67125, Tanzania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1827-6403","authenticated-orcid":false,"given":"Gerald","family":"Misinzo","sequence":"additional","affiliation":[{"name":"Department of Veterinary Microbiology, Parasitology and Biotechnology, College of Veterinary Medicine and Biomedical Sciences, Sokoine University of Agriculture, P.O. Box 3297, Morogoro 67125, Tanzania"},{"name":"SACIDS Foundation for One Health, Sokoine University of Agriculture, P.O. Box 3297, Morogoro 67125, Tanzania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6900-1533","authenticated-orcid":false,"given":"Mecky Isaac","family":"Matee","sequence":"additional","affiliation":[{"name":"SACIDS Foundation for One Health, Sokoine University of Agriculture, P.O. Box 3297, Morogoro 67125, Tanzania"},{"name":"Department of Microbiology and Immunology, Muhimbili University of Health and Allied Sciences, P.O. Box 65001, Dar es Salaam 11103, Tanzania"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,4,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1117","DOI":"10.1016\/j.psj.2019.10.044","article-title":"Prevalence and characteristics of multidrug-resistant mcr-1-positive Escherichia coli isolates from broiler chickens in Tai\u2019an, China","volume":"99","author":"Song","year":"2020","journal-title":"Poult. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1016\/j.psj.2019.10.047","article-title":"Molecular characterization of avian pathogenic Escherichia coli from broiler chickens with colibacillosis","volume":"99","author":"Kim","year":"2020","journal-title":"Poult. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"76","DOI":"10.4103\/jms.jms_25_17","article-title":"World health organization releases global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics","volume":"32","author":"Shrivastava","year":"2018","journal-title":"J. Med. Soc."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/s13099-019-0290-0","article-title":"Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: Recent reports","volume":"11","author":"Sarowska","year":"2019","journal-title":"Gut Pathog."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.2147\/IDR.S241073","article-title":"Prevalence of virulence genes and their association with antimicrobial resistance among pathogenic E. coli isolated from Egyptian patients with different clinical infections","volume":"13","author":"Ibrahim","year":"2020","journal-title":"Infect. Drug. Resist."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3472","DOI":"10.1016\/j.jmb.2019.04.002","article-title":"\u03b2-Lactamases and \u03b2-Lactamase Inhibitors in the 21st Century","volume":"431","author":"Tooke","year":"2019","journal-title":"J. Mol. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Masoud, S.M., El-Baky, A., Mahmoud, R., Aly, S.A., and Ibrahem, R.A. (2021). Co-Existence of Certain ESBLs, MBLs and Plasmid Mediated Quinolone Resistance Genes among MDR E. coli Isolated from Different Clinical Specimens in Egypt. Antibiotics, 10.","DOI":"10.3390\/antibiotics10070835"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"116","DOI":"10.5001\/omj.2013.30","article-title":"Prevalence of extended-spectrum \u03b2-lactamases-producing Escherichia coli from Hospitals in Khartoum State, Sudan","volume":"28","author":"Ibrahim","year":"2013","journal-title":"Oman Med. J."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Yano, H., Uemura, M., Endo, S., Kanamori, H., Inomata, S., Kakuta, R., Ichimura, S., Ogawa, M., Shimojima, M., and Ishibashi, N. (2013). Molecular characteristics of extended-spectrum \u03b2-lactamases in clinical isolates from Escherichia coli at a Japanese tertiary hospital. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0064359"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1128\/CMR.00001-07","article-title":"Carbapenemases: The versatile \u03b2-lactamases","volume":"20","author":"Queenan","year":"2007","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_11","first-page":"218","article-title":"The impact of carbapenemases on antimicrobial development and therapy","volume":"3","author":"Livermore","year":"2002","journal-title":"Curr. Opin. Investig. Drugs (Lond. Engl. 2000)"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2503","DOI":"10.1128\/AEM.70.4.2503-2507.2004","article-title":"Frequency and distribution of tetracycline resistance genes in genetically diverse, nonselected, and nonclinical Escherichia coli strains isolated from diverse human and animal sources","volume":"70","author":"Bryan","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"24","DOI":"10.3389\/fmicb.2012.00024","article-title":"Plasmid-mediated quinolone resistance; interactions between human, animal, and environmental ecologies","volume":"3","author":"Poirel","year":"2012","journal-title":"Front. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"6235","DOI":"10.3390\/ijerph10126235","article-title":"Escherichia coli in Europe: An overview","volume":"10","author":"Allocati","year":"2013","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref_15","first-page":"141","article-title":"Are Escherichia coli pathotypes still relevant in the era of whole-genome sequencing?","volume":"6","author":"Holt","year":"2016","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.bjm.2016.10.015","article-title":"Diarrheagenic Escherichia coli","volume":"47","author":"Gomes","year":"2016","journal-title":"Braz. J. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1007\/s10393-019-01415-5","article-title":"Critical importance of a one health approach to antimicrobial resistance","volume":"16","author":"White","year":"2019","journal-title":"EcoHealth"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4314\/thrb.v8i1.14262","article-title":"Observations on the endemicity of plague in Karatu and Ngorongoro, northern Tanzania","volume":"8","author":"Kilonzo","year":"2006","journal-title":"Tanzan. J. Health Res."},{"key":"ref_19","unstructured":"Makundi, R.H., Massawe, A.W., Mulungu, L.S., Katakweba, A., Mbise, T.J., and Mgode, G. (2022, February 02). Potential mammalian reservoirs in a bubonic plague outbreak focus in Mbulu District, northern Tanzania, in 2007. Available online: https:\/\/www.degruyter.com\/document\/doi\/10.1515\/MAMM.2008.038\/pdf."},{"key":"ref_20","first-page":"4","article-title":"Plague in Tanzania: An overview","volume":"15","author":"Ziwa","year":"2013","journal-title":"Tanzan. J. Health Res."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Guenther, S., Bethe, A., Fruth, A., Semmler, T., Ulrich, R.G., Wieler, L.H., and Ewers, C. (2012). Frequent combination of antimicrobial multiresistance and extraintestinal pathogenicity in Escherichia coli isolates from urban rats (Rattus norvegicus) in Berlin, Germany. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0050331"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/s11252-013-0305-4","article-title":"The secret life of the city rat: A review of the ecology of urban Norway and black rats (Rattus norvegicus and Rattus rattus)","volume":"17","author":"Feng","year":"2014","journal-title":"Urban Ecosyst."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e259","DOI":"10.1016\/S2542-5196(19)30083-X","article-title":"Clinically relevant antimicrobial resistance at the wildlife\u2013livestock\u2013human interface in Nairobi: An epidemiological study","volume":"3","author":"Hassell","year":"2019","journal-title":"Lancet Planet. Health"},{"key":"ref_24","first-page":"1900149","article-title":"Urban brown rats (Rattus norvegicus) as possible source of multidrug-resistant Enterobacteriaceae and meticillin-resistant Staphylococcus spp., Vienna, Austria, 2016 and 2017","volume":"24","author":"Ruppitsch","year":"2019","journal-title":"Eurosurveillance"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Sonola, V.S., Katakweba, A.S., Misinzo, G., and Matee, M.I. (2021). Occurrence of Multi-Drug-Resistant Escherichia coli in Chickens, Humans, Rodents and Household Soil in Karatu, Northern Tanzania. Antibiotics, 10.","DOI":"10.3390\/antibiotics10091137"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Cepas, V., and Soto, S.M. (2020). Relationship between Virulence and Resistance among Gram-Negative Bacteria. Antibiotics, 9.","DOI":"10.3390\/antibiotics9100719"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Yao, M., Zhang, X., Gao, Y., Song, S., Xu, D., and Yan, L. (2019). Development and application of multiplex PCR method for simultaneous detection of seven viruses in ducks. BMC Vet. Res., 15.","DOI":"10.1186\/s12917-019-1820-1"},{"key":"ref_28","unstructured":"(2022, February 02). United Republic of Tanzania, 2012 Population and Housing Census-Population Distribution by Administrative Areas. Available online: http:\/\/tanzania.countrystat.org\/fileadmin\/user_upload\/countrystat_fenix\/congo\/docs\/Census%20General%20Report-2012PHC.pdf."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_30","unstructured":"(2022, February 02). R: A Language and Environment for Statistical Computing. Available online: https:\/\/www.eea.europa.eu\/data-and-maps\/indicators\/oxygen-consuming-substances-in-rivers\/r-development-core-team-2006."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"518","DOI":"10.4314\/eamj.v78i10.8960","article-title":"Antimicrobial susceptibility and plasmids from Escherichia coli isolated from rats","volume":"78","author":"Gakuya","year":"2001","journal-title":"East Afr. Med. J."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1038\/ismej.2016.103","article-title":"The antibiotic resistome of swine manure is significantly altered by association with the Musca domestica larvae gut microbiome","volume":"11","author":"Wang","year":"2017","journal-title":"ISME J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1128\/microbiolspec.ARBA-0026-2017","article-title":"Antimicrobial resistance in Escherichia coli","volume":"6","author":"Poirel","year":"2018","journal-title":"Microbiol. Spectr."},{"key":"ref_34","unstructured":"(2022, February 02). Comparison of Antibiotic Resistant Escherichia coli Obtained from Drinking Water Sources in Northern Tanzania: A Cross-Sectional Study. Available online: https:\/\/www.researchgate.net\/publication\/309765672_Comparison_of_antibiotic_resistant_Escherichia_coli_obtained_from_drinking_water_sources_in_northern_Tanzania_a_cross-sectional_study."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"(2022, February 02). Antimicrobial Resistance Profiles of Escherichia coli Isolated from Broiler and Layer Chickens in Arusha and Mwanza, Tanzania. Available online: https:\/\/www.hindawi.com\/journals\/ijmicro\/2021\/6759046\/.","DOI":"10.1155\/2021\/6759046"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"(2022, February 02). Sale of Fluoroquinolones in Northern Tanzania: A Potential Threat for Fluoroquinolone Use in Tuberculosis Treatment. Available online: https:\/\/academic.oup.com\/jac\/article\/65\/1\/145\/727526?login=false#.","DOI":"10.1093\/jac\/dkp413"},{"key":"ref_37","unstructured":"(2022, February 02). Comparison of the Prevalence of Antibiotic-Resistant Escherichia coli Isolates from Commercial-Layer and Free-Range Chickens in Arusha District, Tanzania. Available online: https:\/\/www.researchgate.net\/publication\/308594993_Comparison_of_the_prevalence_of_antibiotic-resistant_Escherichia_coli_isolates_from_commercial-layer_and_free-range_chickens_in_Arusha_district_Tanzania."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1038\/s41467-019-13995-5","article-title":"Antimicrobial resistant enteric bacteria are widely distributed amongst people, animals and the environment in Tanzania","volume":"11","author":"Subbiah","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_39","unstructured":"(2022, February 02). Genetic Relatedness of Multidrug Resistant Escherichia coli Isolated from Humans, Chickens and Poultry Environments. Available online: https:\/\/aricjournal.biomedcentral.com\/articles\/10.1186\/s13756-021-00930-x."},{"key":"ref_40","unstructured":"Mahmoud, N.E., Altayb, H.N., and Gurashi, R.M. (2022, February 02). Detection of Carbapenem-Resistant Genes in Escherichia coli Isolated from Drinking Water in Khartoum, Sudan, Available online: https:\/\/pubmed.ncbi.nlm.nih.gov\/32612664\/."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"136499","DOI":"10.1016\/j.scitotenv.2020.136499","article-title":"Winter is coming\u2013Impact of temperature on the variation of beta-lactamase and mcr genes in a wastewater treatment plant","volume":"712","author":"Schages","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"164","DOI":"10.2174\/138161213804070320","article-title":"\u03b2-Lactamase-mediated resistance: A biochemical, epidemiological and genetic overview","volume":"19","author":"Gutkind","year":"2013","journal-title":"Curr. Pharm. Des."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1128\/CMR.00117-13","article-title":"OXA \u03b2-lactamases","volume":"27","author":"Evans","year":"2014","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"5463","DOI":"10.1016\/j.watres.2010.06.058","article-title":"Large scale analysis of virulence genes in Escherichia coli strains isolated from Avalon Bay, CA","volume":"44","author":"Hamilton","year":"2010","journal-title":"Water Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"103303","DOI":"10.1016\/j.fm.2019.103303","article-title":"Inhibition of Escherichia coli O157: H7 and Salmonella enterica virulence factors by benzyl isothiocyanate","volume":"86","author":"Patel","year":"2020","journal-title":"Food Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"148","DOI":"10.3389\/fcimb.2021.633573","article-title":"Abundance and Expression of Shiga Toxin Genes in Escherichia coli at the Recto-Anal Junction Relates to Host Immune Genes","volume":"11","author":"Pan","year":"2021","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1080\/1040-840291046687","article-title":"Enteroaggregative Escherichia coli heat-stable enterotoxin 1 (EAST1): A new toxin with an old twist","volume":"28","author":"Dubreuil","year":"2002","journal-title":"Crit. Rev. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1203\/00006450-200205000-00003","article-title":"Role of OmpA and IbeB in Escherichia coli K1 invasion of brain microvascular endothelial cells in vitro and in vivo","volume":"51","author":"Wang","year":"2002","journal-title":"Pediatr. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.ijid.2014.03.1393","article-title":"Detection of virulence genes in Escherichia coli isolated from patients with cystitis and pyelonephritis","volume":"29","author":"Firoozeh","year":"2014","journal-title":"Int. J. Infect. Dis."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1128\/AAC.01632-13","article-title":"Severe sepsis facilitates intestinal colonization by extended-spectrum-\u03b2-lactamase-producing Klebsiella pneumoniae and transfer of the SHV-18 resistance gene to Escherichia coli during antimicrobial treatment","volume":"58","author":"Guan","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"340506","DOI":"10.1155\/2011\/340506","article-title":"Gene expression during survival of Escherichia coli O157: H7 in soil and water","volume":"2011","author":"Duffitt","year":"2011","journal-title":"Int. J. Microbiol."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Cooley, M.B., Jay-Russell, M., Atwill, E.R., Carychao, D., Nguyen, K., Qui\u00f1ones, B., Patel, R., Walker, S., Swimley, M., and Pierre-Jerome, E. (2013). Development of a robust method for isolation of Shiga toxin-positive Escherichia coli (STEC) from fecal, plant, soil and water samples from a leafy greens production region in California. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0065716"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1292\/jvms.19-0697","article-title":"Antibiotic-resistant Escherichia coli isolated from urban rodents in Hanoi, Vietnam","volume":"82","author":"Koizumi","year":"2020","journal-title":"J. Vet. Med. Sci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"589","DOI":"10.7589\/2014-09-242","article-title":"Prevalence and characteristics of Escherichia coli and Salmonella spp. in the feces of wild urban Norway and black rats (Rattus norvegicus and Rattus rattus) from an inner-city neighborhood of Vancouver, Canada","volume":"51","author":"Himsworth","year":"2015","journal-title":"J. Wildl. Dis."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1016\/j.scitotenv.2016.06.228","article-title":"Elucidating selection processes for antibiotic resistance in sewage treatment plants using metagenomics","volume":"572","author":"Hammaren","year":"2016","journal-title":"Sci. Total Environ."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1543","DOI":"10.1007\/s10096-011-1258-2","article-title":"Acquisition of a pathogenicity island in an Escherichia coli clinical isolate causing febrile urinary tract infection","volume":"30","author":"Soto","year":"2011","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1046\/j.1365-2958.1997.3101672.x","article-title":"Pathogenicity islands of virulent bacteria: Structure, function and impact on microbial evolution","volume":"23","author":"Hacker","year":"1997","journal-title":"Mol. Microbiol."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/9\/5388\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:03:30Z","timestamp":1760137410000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/9\/5388"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,28]]},"references-count":57,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["ijerph19095388"],"URL":"https:\/\/doi.org\/10.3390\/ijerph19095388","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,28]]}}}