1887
  1. Home
  2. Eurosurveillance
  3. Volume 24, Issue 13, 28/Mar/2019
  4. Article
Research Open Access
Like 0
Download

Abstract

Introduction

Emergence of resistance determinants of and has undermined the antimicrobial effectiveness of the last line drugs carbapenems and colistin.

Aim

This work aimed to assess the prevalence of and in strains collected from food in Shenzhen, China, during the period 2015 to 2017.

Methods

Multidrug-resistant strains were isolated from food samples. Plasmids encoding or genes were characterised and compared with plasmids found in clinical isolates.

Results

Among 1,166 non-repeated cephalosporin-resistant strains isolated from 2,147 food samples, 390 and 42, respectively, were resistant to colistin and meropenem, with five strains being resistant to both agents. The rate of resistance to colistin increased significantly (p < 0.01) from 26% in 2015 to 46% in 2017, and that of meropenem resistance also increased sharply from 0.3% in 2015 to 17% in 2017 (p < 0.01). All meropenem-resistant strains carried a plasmid-borne gene. Among the colistin-resistant strains, three types of -bearing plasmids were determined. Plasmid sequencing indicated that these and -bearing plasmids were structurally similar to those commonly recovered from clinical isolates. Interestingly, both -bearing and -bearing plasmids were transferrable to strain J53 under selection by meropenem, yet only -bearing plasmids were transferrable under colistin selection.

Conclusion

These findings might suggest that mobile elements harbouring and have been acquired by animal strains and transmitted to our food products, highlighting a need to prevent a spike in the rate of drug resistant food-borne infections.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Closure
A corrected article has been published for this content:
Erratum for Euro Surveill. 2019;24(13)
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2019.24.13.1800113
2019-03-28
2024-04-25
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.13.1800113
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/24/13/eurosurv-24-13-4.html?itemId=/content/10.2807/1560-7917.ES.2019.24.13.1800113&mimeType=html&fmt=ahah

References

  1. Jeon JH, Lee JH, Lee JJ, Park KS, Karim AM, Lee CR, et al. Structural basis for carbapenem-hydrolyzing mechanisms of carbapenemases conferring antibiotic resistance. Int J Mol Sci. 2015;16(5):9654-92.  https://doi.org/10.3390/ijms16059654  PMID: 25938965 
  2. Lee CR, Lee JH, Park KS, Kim YB, Jeong BC, Lee SH. Global dissemination of carbapenemase-producing Klebsiella pneumoniae: epidemiology, genetic context, treatment options, and detection methods. Front Microbiol. 2016;7:895.  https://doi.org/10.3389/fmicb.2016.00895  PMID: 27379038 
  3. Fu Y, Du X, Ji J, Chen Y, Jiang Y, Yu Y. Epidemiological characteristics and genetic structure of blaNDM-1 in non-baumannii Acinetobacter spp. in China. J Antimicrob Chemother. 2012;67(9):2114-22.  https://doi.org/10.1093/jac/dks192  PMID: 22604448 
  4. Ou W, Cui L, Li Y, Zheng B, Lv Y. Epidemiological characteristics of blaNDM-1 in Enterobacteriaceae and the Acinetobacter calcoaceticus-Acinetobacter baumannii complex in China from 2011 to 2012. PLoS One. 2014;9(12):e113852.  https://doi.org/10.1371/journal.pone.0113852  PMID: 25469701 
  5. Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 2009;53(12):5046-54.  https://doi.org/10.1128/AAC.00774-09  PMID: 19770275 
  6. Poirel L, Dortet L, Bernabeu S, Nordmann P. Genetic features of blaNDM-1-positive Enterobacteriaceae. Antimicrob Agents Chemother. 2011;55(11):5403-7.  https://doi.org/10.1128/AAC.00585-11  PMID: 21859933 
  7. Pfeifer Y, Wilharm G, Zander E, Wichelhaus TA, Göttig S, Hunfeld KP, et al. Molecular characterization of blaNDM-1 in an Acinetobacter baumannii strain isolated in Germany in 2007. J Antimicrob Chemother. 2011;66(9):1998-2001.  https://doi.org/10.1093/jac/dkr256  PMID: 21693460 
  8. Ho PL, Lo WU, Yeung MK, Lin CH, Chow KH, Ang I, et al. Complete sequencing of pNDM-HK encoding NDM-1 carbapenemase from a multidrug-resistant Escherichia coli strain isolated in Hong Kong. PLoS One. 2011;6(3):e17989.  https://doi.org/10.1371/journal.pone.0017989  PMID: 21445317 
  9. Yang Q, Fang L, Fu Y, Du X, Shen Y, Yu Y. Dissemination of NDM-1-producing Enterobacteriaceae mediated by the IncX3-type plasmid. PLoS One. 2015;10(6):e0129454.  https://doi.org/10.1371/journal.pone.0129454  PMID: 26047502 
  10. Liu Y-Y, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, et al. 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(2):161-8.  https://doi.org/10.1016/S1473-3099(15)00424-7  PMID: 26603172 
  11. Quan J, Li X, Chen Y, Jiang Y, Zhou Z, Zhang H, et al. Prevalence of mcr-1 in Escherichia coli and Klebsiella pneumoniae recovered from bloodstream infections in China: a multicentre longitudinal study. Lancet Infect Dis. 2017;17(4):400-10.  https://doi.org/10.1016/S1473-3099(16)30528-X  PMID: 28139430 
  12. Liu X, Li R, Zheng Z, Chen K, Xie M, Chan EW, et al. Molecular characterization of Escherichia coli isolates carrying mcr-1, fosa3, and extended-spectrum-β-lactamase genes from food samples in China. Antimicrob Agents Chemother. 2017;61(6):61.  https://doi.org/10.1128/AAC.00064-17  PMID: 28373188 
  13. Skov RL, Monnet DL. Plasmid-mediated colistin resistance (mcr-1 gene): three months later, the story unfolds. Euro Surveill. 2016;21(9):30155.  https://doi.org/10.2807/1560-7917.ES.2016.21.9.30155  PMID: 26967914 
  14. Li R, Xie M, Zhang J, Yang Z, Liu L, Liu X, et al. Genetic characterization of mcr-1-bearing plasmids to depict molecular mechanisms underlying dissemination of the colistin resistance determinant. J Antimicrob Chemother. 2017;72(2):393-401.  https://doi.org/10.1093/jac/dkw411  PMID: 28073961 
  15. Malhotra-Kumar S, Xavier BB, Das AJ, Lammens C, Butaye P, Goossens H. Colistin resistance gene mcr-1 harboured on a multidrug resistant plasmid. Lancet Infect Dis. 2016;16(3):283-4.  https://doi.org/10.1016/S1473-3099(16)00012-8  PMID: 26774247 
  16. Xavier BB, Lammens C, Butaye P, Goossens H, Malhotra-Kumar S. Complete sequence of an IncFII plasmid harbouring the colistin resistance gene mcr-1 isolated from Belgian pig farms. J Antimicrob Chemother. 2016;71(8):2342-4.  https://doi.org/10.1093/jac/dkw191  PMID: 27261261 
  17. Zhong LL, Zhang YF, Doi Y, Huang X, Zhang XF, Zeng KJ, et al. Coproduction of MCR-1 and NDM-1 by colistin-resistant Escherichia coli isolated from a healthy individual. Antimicrob Agents Chemother. 2016;61(1):61. PMID: 27821458 
  18. Yang RS, Feng Y, Lv XY, Duan JH, Chen J, Fang LX, et al. Emergence of NDM-5- and MCR-1-producing Escherichia coli clones ST648 and ST156 from a single muscovy duck (Cairina moschata). Antimicrob Agents Chemother. 2016;60(11):6899-902.  https://doi.org/10.1128/AAC.01365-16  PMID: 27550364 
  19. Wang Y, Zhang R, Li J, Wu Z, Yin W, Schwarz S, et al. Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production. Nat Microbiol. 2017;2(4):16260.  https://doi.org/10.1038/nmicrobiol.2016.260  PMID: 28165472 
  20. Liu BT, Song FJ, Zou M, Hao ZH, Shan H. Emergence of colistin resistance gene mcr-1 in Cronobacter sakazakii producing NDM-9 and in Escherichia coli from the same animal. Antimicrob Agents Chemother. 2017;61(2):61. PMID: 27855074 
  21. Clinical Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; 28th informational supplement. CLSI document M100-S28. Wayne, PA: CLSI 2018. Available from: http://www.iacld.ir/DL/public/CLSI-2018-M100-S28.pdf
  22. Lin D, Xie M, Li R, Chen K, Chan EW, Chen S. IncFII conjugative plasmid-mediated transmission of blandm-1 elements among animal-borne Escherichia coli strains. Antimicrob Agents Chemother. 2016;61(1):61. PMID: 27821455 
  23. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014;42(Database issue):D206-14.  https://doi.org/10.1093/nar/gkt1226  PMID: 24293654 
  24. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011;27(7):1009-10.  https://doi.org/10.1093/bioinformatics/btr039  PMID: 21278367 
  25. Anjum MF, Duggett NA, AbuOun M, Randall L, Nunez-Garcia J, Ellis RJ, et al. Colistin resistance in Salmonella and Escherichia coli isolates from a pig farm in Great Britain. J Antimicrob Chemother. 2016;71(8):2306-13.  https://doi.org/10.1093/jac/dkw149  PMID: 27147305 
  26. Doumith M, Godbole G, Ashton P, Larkin L, Dallman T, Day M, et al. Detection of the plasmid-mediated mcr-1 gene conferring colistin resistance in human and food isolates of Salmonella enterica and Escherichia coli in England and Wales. J Antimicrob Chemother. 2016;71(8):2300-5.  https://doi.org/10.1093/jac/dkw093  PMID: 27090630 
  27. Chen Y, Zhou Z, Jiang Y, Yu Y. Emergence of NDM-1-producing Acinetobacter baumannii in China. J Antimicrob Chemother. 2011;66(6):1255-9.  https://doi.org/10.1093/jac/dkr082  PMID: 21398294 
  28. Huang Y, Yu X, Xie M, Wang X, Liao K, Xue W, et al. Widespread dissemination of carbapenem-resistant Escherichia coli sequence type 167 strains harboring blaNDM-5 in clinical settings in China. Antimicrob Agents Chemother. 2016;60(7):4364-8.  https://doi.org/10.1128/AAC.00859-16  PMID: 27114282 
  29. He T, Wang Y, Sun L, Pang M, Zhang L, Wang R. Occurrence and characterization of blaNDM-5-positive Klebsiella pneumoniae isolates from dairy cows in Jiangsu, China. J Antimicrob Chemother. 2017;72(1):90-4.  https://doi.org/10.1093/jac/dkw357  PMID: 27621177 
  30. Yaici L, Haenni M, Saras E, Boudehouche W, Touati A, Madec JY. blaNDM-5-carrying IncX3 plasmid in Escherichia coli ST1284 isolated from raw milk collected in a dairy farm in Algeria. J Antimicrob Chemother. 2016;71(9):2671-2.  https://doi.org/10.1093/jac/dkw160  PMID: 27165785 
  31. Wang R, Liu Y, Zhang Q, Jin L, Wang Q, Zhang Y, et al. The prevalence of colistin resistance in Escherichia coli and Klebsiella pneumoniae isolated from food animals in China: coexistence of mcr-1 and blaNDM with low fitness cost. Int J Antimicrob Agents. 2018;51(5):739-44.  https://doi.org/10.1016/j.ijantimicag.2018.01.023  PMID: 29409993 
  32. Zhao ZC, Xu XH, Liu MB, Wu J, Lin J, Li B. Fecal carriage of carbapenem-resistant Enterobacteriaceae in a Chinese university hospital. Am J Infect Control. 2014;42(5):e61-4.  https://doi.org/10.1016/j.ajic.2014.01.024  PMID: 24773806 
Increased prevalence of Escherichia coli strains from food carrying blaNDM and mcr-1-bearing plasmids that structurally resemble those of clinical strains, China, 2015 to 2017
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Xiaobo+Liu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Liu Xiaobo</a>, <a href="/search?value1=Shu+Geng&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Geng Shu</a>, <a href="/search?value1=Edward+Wai-Chi+Chan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chan Edward Wai-Chi</a>, <a href="/search?value1=Sheng+Chen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chen Sheng</a></span>. Increased prevalence of Escherichia coli strains from food carrying blaNDM and mcr-1-bearing plasmids that structurally resemble those of clinical strains, China, 2015 to 2017. <a href="/content/ecdc">Euro Surveill.</a> 2019;24(13):pii=1800113. <a href="https://doi.org/10.2807/1560-7917.ES.2019.24.13.1800113" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2019.24.13.1800113</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 12 Mar 2018;&nbsp;&nbsp; <span class="generated">Accepted</span>: 07 Jul 2018 </span> </p>
/content/10.2807/1560-7917.ES.2019.24.13.1800113
/content/10.2807/1560-7917.ES.2019.24.13.1800113
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error