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Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals
Beijing Advanced Innovation Center for Food Nutrition and Human Health, College of Veterinary Medicine, China Agricultural University, Beijing, China College of Veterinary Medicine, Hunan Agricultural University, Changsha, Hunan, China.
Shandong Academy of Clinical Medicine, Shandong Provincial Hospital, Jinan, Shandong, China.
Beijing Advanced Innovation Center for Food Nutrition and Human Health, College of Veterinary Medicine, China Agricultural University, Beijing, China.
Shandong Provincial Key Laboratory of Infectious Disease Control and Prevention, Shandong Center for Disease Control and Prevention, Jinan, Shandong, China.
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2019 (English)In: Journal of Environmental Health Perspectives, ISSN 0091-6765, E-ISSN 1552-9924, Vol. 127, no 10, article id 107009Article in journal (Refereed) Published
Abstract [en]

BACKGROUND: The rapidly increasing dissemination of carbapenem-resistant Enterobacteriaceae (CRE) in both humans and animals poses a global threat to public health. However, the transmission of CRE between humans and animals has not yet been well studied.

OBJECTIVES: We investigated the prevalence, risk factors, and drivers of CRE transmission between humans and their backyard animals in rural China.

METHODS: We conducted a comprehensive sampling strategy in 12 villages in Shandong, China. Using the household [residents and their backyard animals (farm and companion animals)] as a single surveillance unit, we assessed the prevalence of CRE at the household level and examined the factors associated with CRE carriage through a detailed questionnaire. Genetic relationships among human- and animal-derived CRE were assessed using whole-genome sequencing-based molecular methods.

RESULTS: A total of 88 New Delhi metallo beta lactamasesmetallo-β-lactamases–type carbapenem-resistant Escherichia coli (NDM-EC), including 17 from humans, 44 from pigs, 12 from chickens, 1 from cattle, and 2 from dogs, were isolated from 65 of the 746 households examined. The remaining 12 NDM-EC were from flies in the immediate backyard environment. The NDM-EC colonization in households was significantly associated with a) the number of species of backyard animals raised/kept in the same household, and b) the use of human and/or animal feces as fertilizer. Discriminant analysis of principal components (DAPC) revealed that a large proportion of the core genomes of the NDM-EC belonged to strains from hosts other than their own, and several human isolates shared closely related core single-nucleotide polymorphisms and bla sub NDMblaNDM 

genetic contexts with isolates from backyard animals.

CONCLUSIONS: To our knowledge, we are the first to report evidence of direct transmission of NDM-EC between humans and animals. Given the rise of NDM-EC in community and hospital infections, combating NDM-EC transmission in backyard farm systems is needed. https://doi.org/10.1289/EHP5251.

Place, publisher, year, edition, pages
U.S. Department of Health and Human Services, National Institute of Environmental Health Sciences , 2019. Vol. 127, no 10, article id 107009
Keywords [en]
Animals; Animals, Domestic; Bacterial Proteins; beta-Lactamases; Carbapenem-Resistant Enterobacteriaceae; Cattle; China; Dogs; Drug Resistance, Multiple, Bacterial; Escherichia coli; Humans; Swine; Zoonoses
National Category
Microbiology in the medical area Microbiology
Identifiers
URN: urn:nbn:se:oru:diva-107630DOI: 10.1289/EHP5251ISI: 000492748900009PubMedID: 31642700Scopus ID: 2-s2.0-85073762497OAI: oai:DiVA.org:oru-107630DiVA, id: diva2:1788390
Funder
Swedish Research Council, D0879801Medical Research Council of Southeast Sweden (FORSS)
Note

This study is funded by the National Natural Science Foundation of China (grants 81361138021, 81861138051, and 81661138002), National Key Research and Development Program of China (2018YFD0500300), the Swedish Research Council (Grant D0879801), and the Medical Research Council (MR/P007295/1). 

Available from: 2023-08-16 Created: 2023-08-16 Last updated: 2023-12-29Bibliographically approved

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