1887
  1. Home
  2. Eurosurveillance
  3. Volume 28, Issue 37, 14/Sep/2023
  4. Article
Research Open Access
Like 0
Download

Food as vehicle for AMR

Abstract

Background

In China, the gene has been recovered from human bacterial isolates since 2011. After 2014, detections of this gene in animal and food bacterial isolates have increasingly been reported.

Aim

We aimed to understand how -bearing bacteria could spread between humans, animals, and animal-derived food.

Methods

A total of 288 non-duplicate strains, including 130 -carrying and 158 -negative strains were collected from clinical (humans), food-producing animals (pigs) and food (retail pork) sources between 2015 and 2017. The strains were whole genome sequenced. Core-genome-multilocus-sequence-typing was conducted. To investigate if sequence types (STs) found in human, animal or food samples could have a prior origin in a clinical, animal or food-borne animal reservoir, discriminant analysis of principal components (DAPC) was used. Plasmids bearing were characterised.

Results

The 130 -carrying strains comprised a total of 60 STs, with ST167 (10/51), ST77 (6/33) and ST48 (6/46) being most prevalent in clinical, animal and food sources, respectively. Some ST10 and ST167 strains were respectively found among all three sources sampled, suggesting they might enable transfer of between sources. DAPC analysis indicated possible transmissions of ST167 from humans to animals and ST10 from animals to human. In 114 of 130 -carrying isolates, was located on an IncX3 plasmid.

Conclusion

This study in a Chinese context suggests that cross-species transmission of certain STs of harbouring on mobile elements, may facilitate the spread of carbapenem-resistant Enterobacteriaceae. Stringent monitoring of -bearing in ecosystems is important.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2023.28.37.2200925
2023-09-14
2024-04-29
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.37.2200925
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/28/37/eurosurv-28-37-4.html?itemId=/content/10.2807/1560-7917.ES.2023.28.37.2200925&mimeType=html&fmt=ahah

References

  1. Jeon JH, Lee JH, Lee JJ, Park KS, Karim AM, Lee C-R, 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 C-R, 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. Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A, Simonsen GS, et al. , Burden of AMR Collaborative Group. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis. 2019;19(1):56-66.  https://doi.org/10.1016/S1473-3099(18)30605-4  PMID: 30409683 
  4. Jean SS, Harnod D, Hsueh PR. Global Threat of Carbapenem-Resistant Gram-Negative Bacteria. Front Cell Infect Microbiol. 2022;12:823684.  https://doi.org/10.3389/fcimb.2022.823684  PMID: 35372099 
  5. Ma W, Zhu B, Wang W, Wang Q, Cui X, Wang Y, et al. Genetic and enzymatic characterization of two novel blaNDM-36, -37 variants in Escherichia coli strains. Eur J Clin Microbiol Infect Dis. 2023;42(4):471-80.  https://doi.org/10.1007/s10096-023-04576-y  PMID: 36810726 
  6. 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 
  7. Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-β-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 
  8. Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis. 2010;10(9):597-602.  https://doi.org/10.1016/S1473-3099(10)70143-2  PMID: 20705517 
  9. 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 
  10. Walsh TR, Weeks J, Livermore DM, Toleman MA. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis. 2011;11(5):355-62.  https://doi.org/10.1016/S1473-3099(11)70059-7  PMID: 21478057 
  11. Khan AU, Maryam L, Zarrilli R. Structure, Genetics and Worldwide Spread of New Delhi Metallo-β-lactamase (NDM): a threat to public health. BMC Microbiol. 2017;17(1):101.  https://doi.org/10.1186/s12866-017-1012-8  PMID: 28449650 
  12. Lin D, Xie M, Li R, Chen K, Chan EW-C, Chen S. IncFII conjugative plasmid-mediated transmission of blaNDM-1 elements among animal-borne Escherichia coli strains. Antimicrob Agents Chemother. 2016;61(1):e02285-16.  https://doi.org/10.1128/AAC.02285-16  PMID: 27821455 
  13. Sonnevend A, Al Baloushi A, Ghazawi A, Hashmey R, Girgis S, Hamadeh MB, et al. Emergence and spread of NDM-1 producer Enterobacteriaceae with contribution of IncX3 plasmids in the United Arab Emirates. J Med Microbiol. 2013;62(Pt 7):1044-50.  https://doi.org/10.1099/jmm.0.059014-0  PMID: 23579399 
  14. Zheng Z, Li R, Ye L, Chan EW, Chen S. Identification and characterization of IncA/C conjugative, blaNDM-1-bearing plasmid in Vibrio alginolyticus of food origin. Antimicrob Agents Chemother. 2018;62(12):e01897-18.  https://doi.org/10.1128/AAC.01897-18  PMID: 30224528 
  15. Yang L, Li P, Liang B, Hu X, Li J, Xie J, et al. Multidrug-resistant Citrobacter freundii ST139 co-producing NDM-1 and CMY-152 from China. Sci Rep. 2018;8(1):10653.  https://doi.org/10.1038/s41598-018-28879-9  PMID: 30006537 
  16. 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 
  17. Woodford N, Wareham DW, Guerra B, Teale C. Carbapenemase-producing Enterobacteriaceae and non-Enterobacteriaceae from animals and the environment: an emerging public health risk of our own making? J Antimicrob Chemother. 2014;69(2):287-91.  https://doi.org/10.1093/jac/dkt392  PMID: 24092657 
  18. Zhang R, Liu L, Zhou H, Chan EW, Li J, Fang Y, et al. Nationwide surveillance of clinical carbapenem-resistant Enterobacteriaceae (CRE) strains in China. EBioMedicine. 2017;19:98-106.  https://doi.org/10.1016/j.ebiom.2017.04.032  PMID: 28479289 
  19. 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 
  20. Wang X, Liu W, Zou D, Li X, Wei X, Shang W, et al. High rate of New Delhi metallo-β-lactamase 1-producing bacterial infection in China. Clin Infect Dis. 2013;56(1):161-2.  https://doi.org/10.1093/cid/cis782  PMID: 22955442 
  21. Guerra B, Fischer J, Helmuth R. An emerging public health problem: acquired carbapenemase-producing microorganisms are present in food-producing animals, their environment, companion animals and wild birds. Vet Microbiol. 2014;171(3-4):290-7.  https://doi.org/10.1016/j.vetmic.2014.02.001  PMID: 24629777 
  22. Lv D, Duan R, Fan R, Mu H, Liang J, Xiao M, et al. blaNDM and mcr-1 to mcr-5 Gene Distribution Characteristics in Gut Specimens from Different Regions of China. Antibiotics (Basel). 2021;10(3):233.  https://doi.org/10.3390/antibiotics10030233  PMID: 33669137 
  23. Michael GB, Freitag C, Wendlandt S, Eidam C, Feßler AT, Lopes GV, et al. Emerging issues in antimicrobial resistance of bacteria from food-producing animals. Future Microbiol. 2015;10(3):427-43.  https://doi.org/10.2217/fmb.14.93  PMID: 25812464 
  24. Kong L-H, Lei C-W, Ma S-Z, Jiang W, Liu B-H, Wang Y-X, et al. Various sequence types of Escherichia coli isolates coharboring bla NDM-5 and mcr-1 genes from a commercial swine farm in China. Antimicrob Agents Chemother. 2017;61(3):e02167-02116.  https://doi.org/10.1128/AAC.02167-16  PMID: 27993847 
  25. Yaici L, Haenni M, Saras E, Boudehouche W, Touati A, Madec J-Y. 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 
  26. 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 
  27. Zhang Q, Lv L, Huang X, Huang Y, Zhuang Z, Lu J, et al. Rapid increase in carbapenemase-producing Enterobacteriaceae in retail meat driven by the spread of the blaNDM-5-carrying IncX3 plasmid in China from 2016 to 2018. Antimicrob Agents Chemother. 2019;63(8):e00573-19.  https://doi.org/10.1128/AAC.00573-19  PMID: 31182541 
  28. Liu X, Geng S, Chan EW-C, Chen S. 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. Euro Surveill. 2019;24(13):1800113.  https://doi.org/10.2807/1560-7917.ES.2019.24.13.1800113  PMID: 30940314 
  29. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. CLSI; 2016.
  30. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-20.  https://doi.org/10.1093/bioinformatics/btu170  PMID: 24695404 
  31. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455-77.  https://doi.org/10.1089/cmb.2012.0021  PMID: 22506599 
  32. 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(D1);D206-14.  https://doi.org/10.1093/nar/gkt1226  PMID: 24293654 
  33. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640-4.  https://doi.org/10.1093/jac/dks261  PMID: 22782487 
  34. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895-903.  https://doi.org/10.1128/AAC.02412-14  PMID: 24777092 
  35. Kwong JC, Mercoulia K, Tomita T, Easton M, Li HY, Bulach DM, et al. Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J Clin Microbiol. 2016;54(2):333-42.  https://doi.org/10.1128/JCM.02344-15  PMID: 26607978 
  36. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26(7):1641-50.  https://doi.org/10.1093/molbev/msp077  PMID: 19377059 
  37. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016;44(W1):W242-5.  https://doi.org/10.1093/nar/gkw290  PMID: 27095192 
  38. Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol. 2013;30(5):1224-8.  https://doi.org/10.1093/molbev/mst028  PMID: 23408797 
  39. Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11(1):94.  https://doi.org/10.1186/1471-2156-11-94  PMID: 20950446 
  40. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 2014;15(11):524.  https://doi.org/10.1186/s13059-014-0524-x  PMID: 25410596 
  41. European Food Safety Authority (EFSA). Scientific Opinion on Carbapenem resistance in food animal ecosystems. EFSA J. 2013;11(12):3501.
  42. Wang M-G, Zhang R-M, Wang L-L, Sun R-Y, Bai S-C, Han L, et al. Molecular epidemiology of carbapenemase-producing Escherichia coli from duck farms in south-east coastal China. J Antimicrob Chemother. 2021;76(2):322-9.  https://doi.org/10.1093/jac/dkaa433  PMID: 33057710 
  43. Ikhimiukor OO, Odih EE, Donado-Godoy P, Okeke IN. A bottom-up view of antimicrobial resistance transmission in developing countries. Nat Microbiol. 2022;7(6):757-65.  https://doi.org/10.1038/s41564-022-01124-w  PMID: 35637328 
  44. Rabello RF, Bonelli RR, Penna BA, Albuquerque JP, Souza RM, Cerqueira AMF. Antimicrobial Resistance in Farm Animals in Brazil: An Update Overview. Animals (Basel). 2020;10(4):552.  https://doi.org/10.3390/ani10040552  PMID: 32224900 
  45. Dyar OJ, Zhang T, Peng Y, Sun M, Sun C, Yin J, et al. Knowledge, attitudes and practices relating to antibiotic use and antibiotic resistance among backyard pig farmers in rural Shandong province, China. Prev Vet Med. 2020;175:104858.  https://doi.org/10.1016/j.prevetmed.2019.104858  PMID: 31835205 
  46. Wu W, Feng Y, Tang G, Qiao F, McNally A, Zong Z. NDM metallo-β-lactamases and their bacterial producers in health care settings. Clin Microbiol Rev. 2019;32(2):e00115-8.  https://doi.org/10.1128/CMR.00115-18  PMID: 30700432 
  47. Grönthal T, Österblad M, Eklund M, Jalava J, Nykäsenoja S, Pekkanen K, et al. Sharing more than friendship - transmission of NDM-5 ST167 and CTX-M-9 ST69 Escherichia coli between dogs and humans in a family, Finland, 2015. Euro Surveill. 2018;23(27):1700497.  https://doi.org/10.2807/1560-7917.ES.2018.23.27.1700497  PMID: 29991384 
  48. Duggett N, Ellington MJ, Hopkins KL, Ellaby N, Randall L, Lemma F, et al. Detection in livestock of the human pandemic Escherichia coli ST131 fimH30(R) clone carrying blaCTX-M-27. J Antimicrob Chemother. 2021;76(1):263-5.  https://doi.org/10.1093/jac/dkaa407  PMID: 33068401 
  49. Shen Y, Hu F, Wang Y, Yin D, Yang L, Chen Y, et al. Transmission of carbapenem resistance between human and animal NDM-positive Escherichia coli strains. Engineering (Beijing). 2022;15:24-33.  https://doi.org/10.1016/j.eng.2021.07.030 
  50. Guo X, Chen R, Wang Q, Li C, Ge H, Qiao J, et al. Global prevalence, characteristics, and future prospects of IncX3 plasmids: A review. Front Microbiol. 2022;13:979558.  https://doi.org/10.3389/fmicb.2022.979558  PMID: 36147856 
  51. 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 
  52. Politi L, Gartzonika K, Spanakis N, Zarkotou O, Poulou A, Skoura L, et al. Emergence of NDM-1-producing Klebsiella pneumoniae in Greece: evidence of a widespread clonal outbreak. J Antimicrob Chemother. 2019;74(8):2197-202.  https://doi.org/10.1093/jac/dkz176  PMID: 31065697 
Deciphering mechanisms of blaNDM gene transmission between human and animals: a genomics study of bacterial isolates from various sources in China, 2015 to 2017
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Kaichao+Chen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chen Kaichao</a>, <a href="/search?value1=Miaomiao+Xie&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Xie Miaomiao</a>, <a href="/search?value1=Ning+Dong&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Dong Ning</a>, <a href="/search?value1=Edward+Wai+Chi+Chan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chan Edward Wai Chi</a>, <a href="/search?value1=Rong+Zhang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zhang Rong</a>, <a href="/search?value1=Sheng+Chen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chen Sheng</a></span>. Deciphering mechanisms of blaNDM gene transmission between human and animals: a genomics study of bacterial isolates from various sources in China, 2015 to 2017. <a href="/content/ecdc">Euro Surveill.</a> 2023;28(37):pii=2200925. <a href="https://doi.org/10.2807/1560-7917.ES.2023.28.37.2200925" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2023.28.37.2200925</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 28 Nov 2022;&nbsp;&nbsp; <span class="generated">Accepted</span>: 15 Apr 2023 </span> </p>
/content/10.2807/1560-7917.ES.2023.28.37.2200925
/content/10.2807/1560-7917.ES.2023.28.37.2200925
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