Abstract

MCR-1-positve Escherichia coli (MCRPEC) have been reported in humans worldwide; however, thus far, their prevalence is low and potential sources for human mcr-1 carriage have not yet been identified. Here, we analyse a nationwide epidemiological dataset on MCRPEC in humans throughout China and assess the factors associated with MCRPEC carriage using natural and national anthropogenic data. We identified 774 non-duplicate MCRPEC isolates from 774 stool samples collected from 5,159 healthy individuals in 30 provinces and municipalities in 2016, with a prevalence of MCRPEC ranging from 3.7 to 32.7% (average: 15.0%)—substantially higher than previously reported. MCRPEC carriage was associated with provincial regions, the production of sheep and freshwater aquaculture, annual consumption of total meat, pork and mutton, and daily intake of aquaculture products. MCRPEC was significantly more prevalent in provinces with higher aquaculture industries. Whole-genome sequencing analysis revealed that the MCRPEC isolates were clustered into four distinct lineages, two of which were dominant and harboured most of the MCRPEC isolates. The high prevalence of MCRPEC in the community poses a substantial risk for colistin usage in clinical practice and suggests the need for intestinal screening of mcr-1 carriers in intensive care units in Chinese hospitals. Furthermore, our data suggest that aquaculture is a significant reservoir of mcr-1.

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Change history

  • 03 August 2018

    An incorrect Reporting Summary was originally published with this Article; this has now been replaced with the correct file.

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Acknowledgements

This work was supported in part by grants from the National Key Research and Development Program of China (2018YFD0500300), National Natural Science Foundation of China (81661138002 and 81772250) and Medical Research Council grant DETER-XDRE-CHINA (MR/P007295/1).

Author information

Author notes

  1. These authors contributed equally: Yingbo Shen, Hongwei Zhou.

Affiliations

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

    • Yingbo Shen
    • , Yongqiang Wang
    • , Bing Shao
    • , Congming Wu
    • , Lu Yang
    • , Zhangqi Shen
    • , Yanran Ou
    • , Shaolin Wang
    • , Jianzhong Shen
    •  & Yang Wang
  2. The Second Affiliated Hospital of Zhejiang University, Zhejiang University, Hangzhou, China

    • Hongwei Zhou
    • , Yanyan Hu
    • , Qiaoling Sun
    •  & Rong Zhang
  3. Institute for Nutrition and Health, Chinese Center for Disease Control and Prevention, Beijing, China

    • Jiao Xu
  4. College of Veterinary Medicine, Iowa State University, Ames, IA, USA

    • Qijing Zhang
    •  & Zuowei Wu
  5. Department of Medical Microbiology and Infectious Disease, Institute of Infection and Immunity, Cardiff, UK

    • Timothy R. Walsh
  6. Department of Clinical Laboratory, Shandong Provincial Hospital Affiliated to Shandong University, Jinan, China

    • Yueling Wang
  7. Key Laboratory of Food Safety Risk Assessment, Ministry of Health and China National Center for Food Safety Risk Assessment, Beijing, China

    • Yongning Wu
  8. Australia-China Joint Laboratory for Animal Health Big Data Analytics, School of Veterinary and Life Sciences, Murdoch University, Murdoch, Australia

    • Chang Cai
  9. State Key Laboratory of Infectious Disease Prevention and Control, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China

    • Juan Li
  10. Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, China

    • Jianzhong Shen
    •  & Yang Wang

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Contributions

Yang Wang, R.Z. and J.S. designed the study. Y.S., H.Z., J.X., Y.H., L.Y., Q.S., Y.O., Yue Wang and B.S. collected the data. Y.S., Yang Wang, Yong Wang, H.Z., R.Z., Q.Z., C.W., B.S., Z.S., Z.W., S.W., Y.Wu, C.C., J.L., T.R.W. and J.S. analysed and interpreted the data. Yang Wang, R.Z., Y.S. and T.R.W. wrote the manuscript. All authors reviewed, revised and approved the final report.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Jianzhong Shen or Rong Zhang or Yang Wang.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–5, Supplementary Tables 4 and 5.

  2. Reporting Summary

  3. Supplementary Table 1

    Prevalence of mcr-1-positive samples and corresponding selected isolates for sequencing from 30 provinces in China.

  4. Supplementary Table 2

    Precipitation and anthropogenic data of 30 provinces in China.

  5. Supplementary Table 3

    MIC profiles of MCRPEC.

  6. Supplementary Table 6

    Characterization of 287 sequenced mcr-1-positive E. coli isolates.

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DOI

https://doi.org/10.1038/s41564-018-0205-8