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Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production

Nature Microbiology volume 2, Article number: 16260 (2017) Cite this article

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Abstract

By 2030, the global population will be 8.5 billion, placing pressure on international poultry production, of which China is a key producer1. From April 2017, China will implement the withdrawal of colistin as a growth promoter, removing over 8,000 tonnes per year from the Chinese farming sector2. To understand the impact of banning colistin and the epidemiology of multi-drug-resistant (MDR) Escherichia coli (using blaNDM and mcr-1 as marker genes), we sampled poultry, dogs, sewage, wild birds and flies. Here, we show that mcr-1, but not blaNDM, is prevalent in hatcheries, but blaNDM quickly contaminates flocks through dogs, flies and wild birds. We also screened samples directly for resistance genes to understand the true breadth and depth of the environmental and animal resistome. Direct sample testing for blaNDM and mcr-1 in hatcheries, commercial farms, a slaughterhouse and supermarkets revealed considerably higher levels of positive samples than the blaNDM- and mcr-1-positive E. coli, indicating a substantial segment of unseen resistome—a phenomenon we have termed the ‘phantom resistome’. Whole-genome sequencing identified common blaNDM-positive E. coli shared among farms, flies, dogs and farmers, providing direct evidence of carbapenem-resistant E. coli transmission and environmental contamination.

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Figure 1: Sampling diagram and transmission routes of blaNDM and mcr-1.
Figure 2: Detection of blaNDM and mcr-1 in the poultry-production environment.
Figure 3: Genomic analysis of CREC (n = 161) and CSEC (n = 13) isolates of various origins, as well as 12 international human CREC isolates.
Figure 4: Genetic environment of NDM in 161 CREC isolates.

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Acknowledgements

This work was supported in part by the National Natural Science Foundation of China (grant nos 31530076, 31422055 and 81661138002) and the National Key Basic Research Program of China (grant no. 2013CB127200). T.R.W. and J.M.T. were also supported by MRC grant DETER-XDR-CHINA (MR/P007295/1).

Author information

Author notes

  1. Yang Wang and Rongmin Zhang: These authors contributed equally to this work.

Authors and Affiliations

  1. Beijing Advanced Innovation Center for Food Nutrition and Human Health, College of Veterinary Medicine, China Agricultural University, Beijing, 100193, China

    Yang Wang, Rongmin Zhang, Jiyun Li, Wenjuan Yin, Shaolin Wang, Zhangqi Shen, Congming Wu & Jianzhong Shen

  2. College of Veterinary Medicine, Iowa State University, Ames, 50011-1134, Iowa, USA

    Zuowei Wu & Qijing Zhang

  3. Department of Veterinary Medicine, Institute of Microbiology and Epizootics, Freie Universität Berlin, 14163 Berlin, Germany

    Stefan Schwarz

  4. Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, 31535 Neustadt-Mariensee, Germany

    Stefan Schwarz

  5. Department of Medical Microbiology and Infectious Disease, Institute of Infection & Immunity, UHW Main Building, Heath Park Hospital, Cardiff, CF14 4XN, UK

    Jonathan M. Tyrrell, Mei Li & Timothy R. Walsh

  6. College of Engineering, China Agricultural University, Beijing, 100083, China

    Yongjun Zheng

  7. Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, China Agricultural University, Beijing, 100193, China

    Zhihai Liu, Jianye Liu, Lei Lei & Mei Li

  8. College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, Shandong, China

    Qidi Zhang

  9. The Key Laboratory of Food Safety Risk Assessment, Ministry of Health and China National Center for Food Safety Risk Assessment, Beijing, 100021, China

    Yongning Wu

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  1. Yang Wang
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Contributions

The study was planned and directed by J.S. and T.R.W. Experiments were conducted by Y.Wang, R.Z., J.Li, W.Y., Z.L., Z.S., L.L. and M.L. Sampling was conducted by Y.Wang, R.Z., J.Li, J.Liu and Q-d.Z. Data analysis was performed by Z.W., S.S., Y.Z., S.W., J.M.T., C.W., Q-j.Z. and Y.Wu. The manuscript was prepared by J.S., T.R.W., Y.Wang and R.Z.

Corresponding authors

Correspondence to Timothy R. Walsh or Jianzhong Shen.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1 and 2; Supplementary Tables 1, 3, 4, 6 and 7. (PDF 1453 kb)

Supplementary Tables 2 and 5

Supplementary Table 2: Characterization of genome-sequenced E. coli isolates (n = 174, 161 CREC and 13 CSEC); Supplementary Table 5: MIC values of all E. coli isolates (n = 216, 161 CREC and 55 CSEC). (XLSX 33 kb)

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Wang, Y., Zhang, R., Li, J. et al. Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production. Nat Microbiol 2, 16260 (2017). https://doi.org/10.1038/nmicrobiol.2016.260

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