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Volume 22, Number 9—September 2016
Letter

Possible Transmission of mcr-1–Harboring Escherichia coli between Companion Animals and Human

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To the Editor: Plasmid-mediated, colistin-resistance mechanism gene mcr-1 was first identified in Escherichia coli isolates from food, food animals, and human patients in November 2015 (1). Reports on detection of mcr-1 in Enterobacteriaceae from humans and food animals soon followed from ≈12 countries (25). Here we report detection of mcr-1 in colistin-resistant E. coli isolated from companion animals and the possible transmission of mcr-1–harboring E. coli between companion animals and a person.

Three mcr-1–harboring E. coli clinical isolates were identified from specimens of 3 patients admitted to a urology ward of a hospital in Guangzhou, China. E. coli isolate EC07 was identified in the urine of a 50-year-old male patient with glomerulonephritis in October 2015. Isolate EC08 was cultured from the urine of a 48-year-old male patient with prostatitis in December 2015. Isolate EC09 was identified in the blood of an 80-year-old male patient with bladder cancer 3 weeks after EC08 was identified.

Review of medical records identified the patient carrying E. coli isolate EC07 as a worker at a pet shop. In light of this finding, we collected a total of 53 fecal samples from 39 dogs and 14 cats in the pet shop where the man worked. We isolated and identified colonies consistent with E. coli from fecal samples on MacConkey agar plates (Thermo Fisher, Beijing, China) and API 20E system (bioMérieux, Durham, NC, USA). We prepared crude DNA samples of isolates for PCR testing by boiling cells in water. Among them, 6 were positive for mcr-1 by PCR and sequencing (4 from dogs and 2 from cats). All 6 isolates were resistant to colistin, polymyxin B, cephalosporin, gentamicin, and ciprofloxacin by using the agar dilution method, in accordance with the European Committee on Antimicrobial Susceptibility Testing (http://www.eucast.org) for colistin and polymyxin B and Clinical and Laboratory Standards Institute guidelines (http://www.clsi.org) for the other antimicrobial drugs. We identified various resistance genes accounting for the multidrug resistance in these 9 mcr-1–positive isolates (6,7) (Table). We noted that E. coli isolate EC09 was also resistant to carbapenems and positive for blaIMP-4. We observed co-production of mcr-1 and IMP-type metallo-β-lactamase in E. coli.

We subjected all isolates to multilocus sequence typing, in accordance with the protocol described at http://mlst.warwick.ac.uk/mlst/dbs/Ecoli, and pulsed-field gel electrophoresis as described previously (810). We identified 5 mcr-1–positive isolates from 4 dogs (PET02–04 and PET06) and isolate EC07 as sequence type (ST) 354. Isolates PET01 and PET05, identified from cats, belonged to ST93 and a new ST strain, respectively. Isolates EC08 and EC09, from the patients who shared the same hospital room with the pet shop worker, were ST156 (Table). Results of pulsed-field gel electrophoresis were consistent with multilocus sequence typing results and showed that isolates consisted of 5 types (types I to V; Technical Appendix). Isolate EC07 was clonally related to 4 E. coli strains from dogs, according criteria described by Tenover et al. (10), suggesting possible transmission of mcr-1–harboring E. coli between dogs and the patient. Colistin resistance was successfully transferred to E. coli C600 through conjugation in all isolates, suggesting that mcr-1 was located on transferable plasmids.

These findings suggest that mcr-1–producing E. coli can colonize companion animals and be transferred between companion animals and humans. The findings also suggest that, in addition to food animals and humans, companion animals can serve as a reservoir of colistin-resistant E. coli, adding another layer of complexity to the rapidly evolving epidemiology of plasmid-mediated colistin resistance in the community.

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Acknowledgments

We sincerely thank the patients and the owners of companion animals for giving written consent for publication.

This work was supported by research grants from the National Natural Science Foundation of China (no. 81471988), the 111 Project (nos. B13037 and B12003), the Guangdong Natural Science Foundation (no. S2013010015810), and the Program of Science and Technology New Star of Guangzhou (no. 2014J2200038).

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Xue-Fei Zhang, Yohei Doi, Xi Huang, Hong-Yu Li, Lan-Lan Zhong, Kun-Jiao Zeng, Yan-Fen Zhang, Sandip Patil, and Guo-Bao TianComments to Author 
Author affiliations: Sun Yat-Sen University Zhongshan School of Medicine, Guangzhou, China (X.-.F Zhang, X. Huang, L.-L. Zhong, K.-J. Zeng, Y.-F. Zhang, S. Patil, G.-B. Tian); Ministry of Education Key Laboratory of Tropical Diseases Control, Guangzhou (X.-F. Zhang, X. Huang, L.-L. Zhong, K.-J. Zeng, Y.-F. Zhang, S. Patil, G.-B. Tian); University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA (Y. Doi); Sun Yat-Sen University Memorial Hospital, Guangzhou (H.-Y. Li)

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References

  1. Liu  Y-Y, Wang  Y, Walsh  TR, Yi  L-X, Zhang  R, Spencer  J, Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 2016;16:1618. DOIPubMedGoogle Scholar
  2. Nordmann  P, Lienhard  R, Kieffer  N, Clerc  O, Poirel  L. Plasmid-mediated colistin-resistant Escherichia coli in bacteremia in Switzerland. Clin Infect Dis. 2016 Mar 1:ciw124.
  3. Falgenhauer  L, Waezsada  SE, Yao  Y, Imirzalioglu  C, Käsbohrer  A, Roesler  U, Colistin resistance gene mcr-1 in extended-spectrum β-lactamase–producing and carbapenemase-producing Gram-negative bacteria in Germany. Lancet Infect Dis. 2016;16:2823. DOIPubMedGoogle Scholar
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Cite This Article

DOI: 10.3201/eid2209.160464

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Table of Contents – Volume 22, Number 9—September 2016

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Please use the form below to submit correspondence to the authors or contact them at the following address:

Guo-Bao Tian, Program of Immunology, Institute of Human Virology, Institute of Tuberculosis Control, Zhongshan School of Medicine, Sun Yat-Sen University, 74 Zhongshan 2nd Rd, Guangzhou 510080, China

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Page created: August 16, 2016
Page updated: August 16, 2016
Page reviewed: August 16, 2016
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
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