{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,26]],"date-time":"2026-10-26T20:00:46Z","timestamp":1793044846251,"version":"4.5.0"},"reference-count":41,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2020,2,13]],"date-time":"2020-02-13T00:00:00Z","timestamp":1581552000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31900125"],"award-info":[{"award-number":["31900125"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Hospital sewage plays a key role in the dissemination of antibiotic-resistant genes (ARGs) by serving as an environmental antimicrobial resistance reservoir. In this study, we aimed to characterize the cephalosporin- and carbapenem-resistant isolates from hospital sewage and receiving rivers. The results showed that ESBL (blaCTX-M) and carbapenemase genes (blaNDM and blaKPC) were widely detected in a number of different bacterial species. These resistance genes were mainly harbored in Enterobacteriaceae, followed by Acinetobacter and Aeromonas isolates. More attention should be given to these bacteria as important vectors of ARGs in the environment. Furthermore, we showed that the multidrug resistance phenotype was highly prevalent, which was found in 85.5% Enterobacteriaceae and 75% Acinetobacter strains. Notably, the presence of carbapenemase genes in isolates from treated effluents and receiving rivers indicates that the discharges of wastewater treatment plants could be an important source for high-risk resistance genes propagation to the environment. In conclusion, this study shows a high prevalence of ESBL- and carbapenemase-producing bacteria in hospital sewage and receiving rivers in China. These findings have serious implications for human health, and also suggest the need for more efforts to control the dissemination of resistant bacteria from hospital sewage into the environment.<\/jats:p>","DOI":"10.3390\/ijerph17041183","type":"journal-article","created":{"date-parts":[[2020,2,14]],"date-time":"2020-02-14T10:09:57Z","timestamp":1581674997000},"page":"1183","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":64,"title":["The Prevalence and Characterization of Extended-Spectrum \u03b2-Lactamase- and Carbapenemase-Producing Bacteria from Hospital Sewage, Treated Effluents and Receiving Rivers"],"prefix":"10.3390","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6458-3530","authenticated-orcid":false,"given":"Luhua","family":"Zhang","sequence":"first","affiliation":[{"name":"Department of Pathogenic Biology, School of Basic Medical Sciences, Southwest Medical University, Luzhou 646000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinyue","family":"Ma","sequence":"additional","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Southwest Medical University, Luzhou 646000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Luo","sequence":"additional","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Southwest Medical University, Luzhou 646000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nan","family":"Hu","sequence":"additional","affiliation":[{"name":"Department of Pathogenic Biology, School of Basic Medical Sciences, Southwest Medical University, Luzhou 646000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiayao","family":"Duan","sequence":"additional","affiliation":[{"name":"Department of Pathogenic Biology, School of Basic Medical Sciences, Southwest Medical University, Luzhou 646000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhongjian","family":"Tang","sequence":"additional","affiliation":[{"name":"Department of Pathogenic Biology, School of Basic Medical Sciences, Southwest Medical University, Luzhou 646000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rujie","family":"Zhong","sequence":"additional","affiliation":[{"name":"Department of Pathogenic Biology, School of Basic Medical Sciences, Southwest Medical University, Luzhou 646000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Immunology, School of Basic Medical Sciences, Southwest Medical University, Luzhou 646000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,2,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1038\/nrmicro3380","article-title":"Molecular mechanisms of antibiotic resistance","volume":"13","author":"Blair","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/S1473-3099(08)70041-0","article-title":"Extended-spectrum \u03b2-lactamase-producing Enterobacteriaceae: An emerging public-health concern","volume":"8","author":"Pitout","year":"2008","journal-title":"Lancet Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Bonomo, R.A. (2017). Beta-Lactamases: A Focus on Current Challenges. Cold Spring Harb. Perspect. Med., 7.","DOI":"10.1101\/cshperspect.a025239"},{"key":"ref_4","first-page":"15","article-title":"Carbapenem resistance: Overview of the problem and future perspectives","volume":"3","author":"Meletis","year":"2016","journal-title":"Ther. Adv. Infect. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e01076-18","DOI":"10.1128\/AAC.01076-18","article-title":"Past and Present Perspectives on \u03b2-Lactamases","volume":"62","author":"Bush","year":"2018","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1028","DOI":"10.1128\/AAC.01020-07","article-title":"Predictors of Carbapenem-Resistant Klebsiella pneumoniae Acquisition among Hospitalized Adults and Effect of Acquisition on Mortality","volume":"52","author":"Schwaber","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"ofy150","DOI":"10.1093\/ofid\/ofy150","article-title":"Association Between Carbapenem Resistance and Mortality Among Adult, Hospitalized Patients With Serious Infections Due to Enterobacteriaceae: Results of a Systematic Literature Review and Meta-analysis","volume":"5","author":"Martin","year":"2018","journal-title":"Open Forum Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.drup.2016.09.002","article-title":"The rapid spread of carbapenem-resistant Enterobacteriaceae","volume":"29","author":"Potter","year":"2016","journal-title":"Drug Resist. Updated"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.molmed.2012.03.003","article-title":"Carbapenem resistance in Enterobacteriaceae: here is the storm!","volume":"18","author":"Nordmann","year":"2012","journal-title":"Trends Mol. Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3525","DOI":"10.1007\/s11356-015-5586-0","article-title":"Urban riverine environment is a source of multidrug-resistant and ESBL-producing clinically important Acinetobacter spp.","volume":"23","author":"Maravic","year":"2016","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1093\/jac\/dkx488","article-title":"Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae","volume":"73","author":"Rozwandowicz","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.tim.2017.09.005","article-title":"Antibiotic-Resistance Genes in Waste Water","volume":"26","author":"Karkman","year":"2018","journal-title":"Trends Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e02011","DOI":"10.1128\/mBio.02011-17","article-title":"Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance","volume":"9","author":"Weingarten","year":"2018","journal-title":"mBio"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"13906","DOI":"10.1021\/acs.est.7b03380","article-title":"Hospital Wastewater Releases of Carbapenem-Resistance Pathogens and Genes in Urban India","volume":"51","author":"Lamba","year":"2017","journal-title":"Environ. Sci. Technol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.ijantimicag.2017.08.032","article-title":"Hospital sewage water: A reservoir for variants of New Delhi metallo-beta-lactamase (NDM)- and extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae","volume":"51","author":"Parvez","year":"2018","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/j.envpol.2017.05.095","article-title":"Abundance of carbapenemase genes (blaKPC, blaNDM and blaOXA-48) in wastewater effluents from Tunisian hospitals","volume":"229","author":"Nasri","year":"2017","journal-title":"Environ. Pollut."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1016\/j.scitotenv.2019.03.428","article-title":"Hospital effluent: A reservoir for carbapenemase-producing Enterobacterales?","volume":"672","author":"Cahill","year":"2019","journal-title":"Sci. Total Environ."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1016\/j.scitotenv.2017.09.217","article-title":"Occurrence and characteristics of extended-spectrum beta-lactamase- and carbapenemase- producing bacteria from hospital effluents in Singapore","volume":"615","author":"Haller","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1016\/j.diagmicrobio.2012.02.007","article-title":"Enterobacteriaceae producing the KPC-2 carbapenemase from hospital sewage","volume":"73","author":"Zhang","year":"2012","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Zhang, C., Qiu, S., Wang, Y., Qi, L., Hao, R., Liu, X., Shi, Y., Hu, X., An, D., and Li, Z. (2014). Higher isolation of NDM-1 producing Acinetobacter baumannii from the sewage of the hospitals in Beijing. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0064857"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1093\/jac\/dkx355","article-title":"Emergence of mcr-1 and carbapenemase genes in hospital sewage water in Beijing, China","volume":"73","author":"Jin","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1093\/jac\/dks505","article-title":"blaNDM-1-carrying Acinetobacter johnsonii detected in hospital sewage","volume":"68","author":"Zong","year":"2013","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/j.jgar.2018.11.015","article-title":"Whole-genome sequencing of an NDM-1- and OXA-58-producing Acinetobacter towneri isolate from hospital sewage in Sichuan Province, China","volume":"16","author":"Jiang","year":"2019","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1016\/j.envpol.2017.12.084","article-title":"First detection and genomics analysis of KPC-2-producing Citrobacter isolates from river sediments","volume":"235","author":"Xu","year":"2018","journal-title":"Environ. Pollut."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.watres.2017.04.073","article-title":"Characterization of OXA-48-like-producing Enterobacteriaceae isolated from river water in Algeria","volume":"120","author":"Tafoukt","year":"2017","journal-title":"Water Res."},{"key":"ref_26","first-page":"1063","article-title":"Emergence of Klebsiella variicola positive for NDM-9, a variant of New Delhi metallo-\u03b2-lactamase, in an urban river in South Korea","volume":"72","author":"Di","year":"2017","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1016\/j.scitotenv.2018.11.433","article-title":"Environmental fate of pharmaceutical compounds and antimicrobial-resistant bacteria in hospital effluents, and contributions to pollutant loads in the surface waters in Japan","volume":"657","author":"Azuma","year":"2019","journal-title":"Sci. Total Environ."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2241","DOI":"10.1007\/s10096-018-3365-9","article-title":"Related carbapenemase-producing Klebsiella isolates detected in both a hospital and associated aquatic environment in Sweden","volume":"37","author":"Khan","year":"2018","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_29","unstructured":"Lane, D.J. (1991). 16S\/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics, Wiley."},{"key":"ref_30","unstructured":"CLSI (2019). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [29th ed.]. CLSI Supplement M100."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Sivalingam, P., Pote, J., and Prabakar, K. (2019). Environmental Prevalence of Carbapenem Resistance Enterobacteriaceae (CRE) in a Tropical Ecosystem in India: Human Health Perspectives and Future Directives. Pathogens, 8.","DOI":"10.3390\/pathogens8040174"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1186\/s40168-019-0710-x","article-title":"Sewage effluent from an Indian hospital harbors novel carbapenemases and integron-borne antibiotic resistance genes","volume":"7","author":"Marathe","year":"2019","journal-title":"Microbiome"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e00115-18","DOI":"10.1128\/CMR.00115-18","article-title":"NDM metallo-\u03b2-lactamases and their bacterial producers in health care settings","volume":"32","author":"Wu","year":"2019","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1021\/acs.estlett.6b00036","article-title":"Propagation of New Delhi Metallo-\u03b2-lactamase Genes (blaNDM-1) from a Wastewater Treatment Plant to Its Receiving River","volume":"3","author":"Yang","year":"2016","journal-title":"Environ. Sci. Technol. Lett."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1946","DOI":"10.1016\/j.scitotenv.2018.10.111","article-title":"Occurrence of super antibiotic resistance genes in the downstream of the Yangtze River in China: Prevalence and antibiotic resistance profiles","volume":"651","author":"Wang","year":"2019","journal-title":"Sci. Total Environ."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.scitotenv.2016.12.063","article-title":"Discharge of KPC-2 genes from the WWTPs contributed to their enriched abundance in the receiving river","volume":"581","author":"Yang","year":"2017","journal-title":"Sci. Total Environ."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.1007\/s11274-015-1897-z","article-title":"Emergence of KPC-2-producing Escherichia coli isolates in an urban river in Harbin, China","volume":"31","author":"Xu","year":"2015","journal-title":"World J. Microbiol. Biotechnol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"863","DOI":"10.3389\/fmicb.2017.00863","article-title":"Occurrence and Variety of beta-Lactamase Genes among Aeromonas spp. Isolated from Urban Wastewater Treatment Plant","volume":"8","author":"Piotrowska","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.scitotenv.2018.01.100","article-title":"The prevalence of multidrug-resistant Aeromonas spp. in the municipal wastewater system and their dissemination in the environment","volume":"626","author":"Harnisz","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1111\/1758-2229.12772","article-title":"Potential KPC-2 carbapenemase reservoir of environmental Aeromonas hydrophila and Aeromonas caviae isolates from the effluent of an urban wastewater treatment plant in Japan","volume":"11","author":"Sekizuka","year":"2019","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1016\/j.envpol.2017.10.006","article-title":"Prevalence of antibiotic resistance genes from effluent of coastal aquaculture, South Korea","volume":"233","author":"Jang","year":"2018","journal-title":"Environ. Pollut."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/17\/4\/1183\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T08:57:19Z","timestamp":1760173039000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/17\/4\/1183"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,13]]},"references-count":41,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2020,2]]}},"alternative-id":["ijerph17041183"],"URL":"https:\/\/doi.org\/10.3390\/ijerph17041183","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,13]]}}}