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Inter-host transmission of carbapenemase-producing Escherichia coli among humans and backyard animals

Jiyun Li, Zhenwang Bi, Shizhen Ma, Baoli Chen, Chang Cai, Junjia He (UGent) , Stefan Schwarz, Chengtao Sun, Yuqing Zhou, Jia Yin, et al.
(2019) ENVIRONMENTAL HEALTH PERSPECTIVES. 127(10).
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Abstract
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-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(NDM)( )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.
Keywords
PIG PRODUCTION, RESISTANCE, SWINE, RESIDUES, POULTRY, MCR-1, CHINA

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MLA
Li, Jiyun, et al. “Inter-Host Transmission of Carbapenemase-Producing Escherichia Coli among Humans and Backyard Animals.” ENVIRONMENTAL HEALTH PERSPECTIVES, vol. 127, no. 10, US  Dept Health Human Sciences Public Health Science, 2019, doi:10.1289/EHP5251.
APA
Li, J., Bi, Z., Ma, S., Chen, B., Cai, C., He, J., … Wang, Y. (2019). Inter-host transmission of carbapenemase-producing Escherichia coli among humans and backyard animals. ENVIRONMENTAL HEALTH PERSPECTIVES, 127(10). https://doi.org/10.1289/EHP5251
Chicago author-date
Li, Jiyun, Zhenwang Bi, Shizhen Ma, Baoli Chen, Chang Cai, Junjia He, Stefan Schwarz, et al. 2019. “Inter-Host Transmission of Carbapenemase-Producing Escherichia Coli among Humans and Backyard Animals.” ENVIRONMENTAL HEALTH PERSPECTIVES 127 (10). https://doi.org/10.1289/EHP5251.
Chicago author-date (all authors)
Li, Jiyun, Zhenwang Bi, Shizhen Ma, Baoli Chen, Chang Cai, Junjia He, Stefan Schwarz, Chengtao Sun, Yuqing Zhou, Jia Yin, Anette Hulth, Yongqiang Wang, Zhangqi Shen, Shaolin Wang, Congming Wu, Lennart E. Nilsson, Timothy R. Walsh, Stefan Borjesson, Jianzhong Shen, Qiang Sun, and Yang Wang. 2019. “Inter-Host Transmission of Carbapenemase-Producing Escherichia Coli among Humans and Backyard Animals.” ENVIRONMENTAL HEALTH PERSPECTIVES 127 (10). doi:10.1289/EHP5251.
Vancouver
1.
Li J, Bi Z, Ma S, Chen B, Cai C, He J, et al. Inter-host transmission of carbapenemase-producing Escherichia coli among humans and backyard animals. ENVIRONMENTAL HEALTH PERSPECTIVES. 2019;127(10).
IEEE
[1]
J. Li et al., “Inter-host transmission of carbapenemase-producing Escherichia coli among humans and backyard animals,” ENVIRONMENTAL HEALTH PERSPECTIVES, vol. 127, no. 10, 2019.
@article{01J3W3VRYHEXKC92C4T1W1M99Q,
  abstract     = {{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-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(NDM)( )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.}},
  articleno    = {{107009}},
  author       = {{Li, Jiyun and  Bi, Zhenwang and  Ma, Shizhen and  Chen, Baoli and  Cai, Chang and He, Junjia and  Schwarz, Stefan and  Sun, Chengtao and  Zhou, Yuqing and  Yin, Jia and  Hulth, Anette and  Wang, Yongqiang and  Shen, Zhangqi and  Wang, Shaolin and  Wu, Congming and  Nilsson, Lennart E. and  Walsh, Timothy R. and  Borjesson, Stefan and  Shen, Jianzhong and  Sun, Qiang and  Wang, Yang}},
  issn         = {{0091-6765}},
  journal      = {{ENVIRONMENTAL HEALTH PERSPECTIVES}},
  keywords     = {{PIG PRODUCTION,RESISTANCE,SWINE,RESIDUES,POULTRY,MCR-1,CHINA}},
  language     = {{eng}},
  number       = {{10}},
  pages        = {{11}},
  publisher    = {{US  Dept Health Human Sciences Public Health Science}},
  title        = {{Inter-host transmission of carbapenemase-producing Escherichia coli among humans and backyard animals}},
  url          = {{http://doi.org/10.1289/EHP5251}},
  volume       = {{127}},
  year         = {{2019}},
}
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