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Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals

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,...

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Autores principales: Li, Jiyun, Bi, Zhenwang, Ma, Shizhen, Chen, Baoli, Cai, Chang, He, Junjia, Schwarz, Stefan, Sun, Chengtao, Zhou, Yuqing, Yin, Jia, Hulth, Anette, Wang, Yongqiang, Shen, Zhangqi, Wang, Shaolin, Wu, Congming, Nilsson, Lennart E., Walsh, Timothy R, Börjesson, Stefan, Shen, Jianzhong, Sun, Qiang, Wang, Yang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Environmental Health Perspectives 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6910777/
https://www.ncbi.nlm.nih.gov/pubmed/31642700
http://dx.doi.org/10.1289/EHP5251
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author Li, Jiyun
Bi, Zhenwang
Ma, Shizhen
Chen, Baoli
Cai, Chang
He, Junjia
Schwarz, Stefan
Sun, Chengtao
Zhou, Yuqing
Yin, Jia
Hulth, Anette
Wang, Yongqiang
Shen, Zhangqi
Wang, Shaolin
Wu, Congming
Nilsson, Lennart E.
Walsh, Timothy R
Börjesson, Stefan
Shen, Jianzhong
Sun, Qiang
Wang, Yang
author_facet Li, Jiyun
Bi, Zhenwang
Ma, Shizhen
Chen, Baoli
Cai, Chang
He, Junjia
Schwarz, Stefan
Sun, Chengtao
Zhou, Yuqing
Yin, Jia
Hulth, Anette
Wang, Yongqiang
Shen, Zhangqi
Wang, Shaolin
Wu, Congming
Nilsson, Lennart E.
Walsh, Timothy R
Börjesson, Stefan
Shen, Jianzhong
Sun, Qiang
Wang, Yang
author_sort Li, Jiyun
collection PubMed
description 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 [Formula: see text] –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 [Formula: see text] 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
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spelling pubmed-69107772019-12-16 Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals Li, Jiyun Bi, Zhenwang Ma, Shizhen Chen, Baoli Cai, Chang He, Junjia Schwarz, Stefan Sun, Chengtao Zhou, Yuqing Yin, Jia Hulth, Anette Wang, Yongqiang Shen, Zhangqi Wang, Shaolin Wu, Congming Nilsson, Lennart E. Walsh, Timothy R Börjesson, Stefan Shen, Jianzhong Sun, Qiang Wang, Yang Environ Health Perspect Research 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 [Formula: see text] –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 [Formula: see text] 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 Environmental Health Perspectives 2019-10-23 /pmc/articles/PMC6910777/ /pubmed/31642700 http://dx.doi.org/10.1289/EHP5251 Text en EHP is an open-access journal published with support from the National Institute of Environmental Health Sciences, National Institutes of Health. All content is public domain unless otherwise noted.
spellingShingle Research
Li, Jiyun
Bi, Zhenwang
Ma, Shizhen
Chen, Baoli
Cai, Chang
He, Junjia
Schwarz, Stefan
Sun, Chengtao
Zhou, Yuqing
Yin, Jia
Hulth, Anette
Wang, Yongqiang
Shen, Zhangqi
Wang, Shaolin
Wu, Congming
Nilsson, Lennart E.
Walsh, Timothy R
Börjesson, Stefan
Shen, Jianzhong
Sun, Qiang
Wang, Yang
Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals
title Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals
title_full Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals
title_fullStr Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals
title_full_unstemmed Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals
title_short Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals
title_sort inter-host transmission of carbapenemase-producing escherichia coli among humans and backyard animals
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6910777/
https://www.ncbi.nlm.nih.gov/pubmed/31642700
http://dx.doi.org/10.1289/EHP5251
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