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Volume 9, Issue 3

The risk of pig and chicken farming for carriage and transmission of containing extended-spectrum beta-lactamase (ESBL) and mobile colistin resistance () genes in Thailand Open Access

Abstract

South-East Asian countries report a high prevalence of extended-spectrum cephalosporin- (ESC-) and colistin-resistant (Col-R-). However, there are still few studies describing the molecular mechanisms and transmission dynamics of ESC-R- and, especially, Col-R-. This study aimed to evaluate the prevalence and transmission dynamics of containing extended spectrum beta-lactamases (ESBL) and mobile colistin resistance () genes using a 'One Health' design in Thailand. The ESC-R- and Col-R- isolates of human stool samples (69 pig farmers, 155 chicken farmers, and 61 non-farmers), rectal swabs from animals (269 pigs and 318 chickens), and the intestinal contents of 196 rodents were investigated. Resistance mechanisms and transmission dynamics of isolates (=638) were studied using short and long read sequencing. We found higher rates of ESBL- isolates among pig farmers (=36; 52.2%) than among chicken farmers (=58; 37.4 %; <0.05) and the control group (=61; 31.1 %; <0.05). with co-occurring ESBL and genes were found in 17 (6.0 %), 50 (18.6 %) and 15 (4.7 %) samples from humans, pigs and chickens, respectively. We also identified 39 (13.7 %) human samples with non-identical containing ESBL and . We found higher rates of ESBL- in particular CTX-M-55 isolates among pig farmers than among non-pig farmers (<0.01). 'Clonal' animal-human transmission of ESBL- and with genes was identified but rare as we overall found a heterogenous population structure of . The Col-R- from human and animal samples often carried -1.1 on conjugative IncX4 plasmids. The latter has been identified in of many different clonal backgrounds.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): clonal transmission , Extended-spectrum beta-lactamase , mobile colistin resistance , occupational exposure , One Health and pig farm
Funding
This study was supported by the:
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Award IZJFZ3-177614)
    • Principle Award Recipient: AnneOppliger
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Award IZJFZ3-177614)
    • Principle Award Recipient: MarkusHilty
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2023-03-23
2024-05-03
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References

  1. Seiffert SN, Hilty M, Perreten V, Endimiani A. Extended-spectrum cephalosporin-resistant Gram-negative organisms in livestock: an emerging problem for human health?. Drug Resist Updat 2013; 16:22–45 [View Article] [PubMed]
     [Google Scholar]
  2. Smyth C, Leigh RJ, Delaney S, Murphy RA, Walsh F. Shooting hoops: globetrotting plasmids spreading more than just antimicrobial resistance genes across One Health. Microb Genom 2022; 8:mgen000858 [View Article]
     [Google Scholar]
  3. Amuasi JH, Lucas T, Horton R, Winkler AS. Reconnecting for our future: the lancet one health commission. Lancet 2020; 395:1469–1471 [View Article]
     [Google Scholar]
  4. Ludden C, Raven KE, Jamrozy D, Gouliouris T, Blane B et al. One health genomic surveillance of Escherichia coli demonstrates distinct lineages and mobile genetic elements in isolates from humans versus livestock. mBio 2019; 10:e02693-18 [View Article]
     [Google Scholar]
  5. Furuya-Kanamori L, Stone J, Yakob L, Kirk M, Collignon P et al. Risk factors for acquisition of multidrug-resistant Enterobacterales among international travellers: a synthesis of cumulative evidence. J Travel Med 2020; 27:taz083 [View Article]
     [Google Scholar]
  6. Pitout JDD, Laupland KB. Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008; 8:159–166 [View Article] [PubMed]
     [Google Scholar]
  7. Kiratisin P, Chattammanat S, Sa-Nguansai S, Dansubutra B, Nangpatharapornthawee P et al. A 2-year trend of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Thailand: an alert for infection control. Trans R Soc Trop Med Hyg 2008; 102:460–464 [View Article] [PubMed]
     [Google Scholar]
  8. Olaitan AO, Diene SM, Kempf M, Berrazeg M, Bakour S et al. Worldwide emergence of colistin resistance in Klebsiella pneumoniae from healthy humans and patients in Lao PDR, Thailand, Israel, Nigeria and France owing to inactivation of the PhoP/PhoQ regulator mgrB: an epidemiological and molecular study. Int J Antimicrob Agents 2014; 44:500–507 [View Article] [PubMed]
     [Google Scholar]
  9. Liu W, Liu Z, Yao Z, Fan Y, Ye X et al. The prevalence and influencing factors of methicillin-resistant Staphylococcus aureus carriage in people in contact with livestock: a systematic review. Am J Infect Control 2015; 43:469–475 [View Article]
     [Google Scholar]
  10. Luvsansharav U-O, Hirai I, Nakata A, Imura K, Yamauchi K et al. Prevalence of and risk factors associated with faecal carriage of CTX-M β-lactamase-producing Enterobacteriaceae in rural Thai communities. J Antimicrob Chemother 2012; 67:1769–1774 [View Article] [PubMed]
     [Google Scholar]
  11. Niumsup PR, Tansawai U, Na-Udom A, Jantapalaboon D, Assawatheptawee K et al. Prevalence and risk factors for intestinal carriage of CTX-M-type ESBLs in Enterobacteriaceae from a Thai community. Eur J Clin Microbiol Infect Dis 2018; 37:69–75 [View Article] [PubMed]
     [Google Scholar]
  12. Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R 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; 16:161–168 [View Article]
     [Google Scholar]
  13. Moser AI, Kuenzli E, Campos-Madueno EI, Büdel T, Rattanavong S et al. Antimicrobial-resistant Escherichia coli strains and their plasmids in people, poultry, and chicken meat in laos. Front Microbiol 2021; 12:708182 [View Article]
     [Google Scholar]
  14. Shen Y, Zhou H, Xu J, Wang Y, Zhang Q et al. Anthropogenic and environmental factors associated with high incidence of mcr-1 carriage in humans across China. Nat Microbiol 2018; 3:1054–1062 [View Article] [PubMed]
     [Google Scholar]
  15. Malchione MD, Torres LM, Hartley DM, Koch M, Goodman JL. Carbapenem and colistin resistance in Enterobacteriaceae in Southeast Asia: review and mapping of emerging and overlapping challenges. Int J Antimicrob Agents 2019; 54:381–399 [View Article]
     [Google Scholar]
  16. Sudatip D, Chasiri K, Kritiyakan A, Phanprasit W, Thinphovong C et al. A One Health approach to assessing occupational exposure to antimicrobial resistance in Thailand: the farmresist project. PLoS One 2021; 16:e0245250 [View Article]
     [Google Scholar]
  17. Sudatip D, Tiengrim S, Chasiri K, Kritiyakan A, Phanprasit W et al. One health surveillance of antimicrobial resistance phenotypes in selected communities in Thailand. Antibiotics 2022; 11:556 [View Article]
     [Google Scholar]
  18. Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 2016; 32:3047–3048 [View Article] [PubMed]
     [Google Scholar]
  19. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article]
     [Google Scholar]
  20. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
     [Google Scholar]
  21. Zankari E, Allesøe R, Joensen KG, Cavaco LM, Lund O et al. PointFinder: a novel web tool for WGS-based detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens. J Antimicrob Chemother 2017; 72:2764–2768 [View Article] [PubMed]
     [Google Scholar]
  22. Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 2018; 34:i142–i150 [View Article] [PubMed]
     [Google Scholar]
  23. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  24. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
     [Google Scholar]
  25. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article]
     [Google Scholar]
  26. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2:e000056 [View Article]
     [Google Scholar]
  27. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. Fast hierarchical Bayesian analysis of population structure. Nucleic Acids Res 2019; 47:5539–5549 [View Article] [PubMed]
     [Google Scholar]
  28. Moor J, Aebi S, Rickli S, Mostacci N, Overesch G et al. Dynamics of extended-spectrum cephalosporin-resistant Escherichia coli in pig farms: a longitudinal study. Int J Antimicrob Agents 2021; 58:106382 [View Article]
     [Google Scholar]
  29. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article]
     [Google Scholar]
  30. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article] [PubMed]
     [Google Scholar]
  31. Falgenhauer L, Imirzalioglu C, Oppong K, Akenten CW, Hogan B et al. Detection and characterization of ESBL-producing Escherichia coli from humans and poultry in Ghana. Front Microbiol 2018; 9:3358 [View Article]
     [Google Scholar]
  32. Shen C, Zhong L-L, Yang Y, Doi Y, Paterson DL et al. Dynamics of mcr-1 prevalence and mcr-1-positive Escherichia coli after the cessation of colistin use as a feed additive for animals in China: a prospective cross-sectional and whole genome sequencing-based molecular epidemiological study. Lancet Microbe 2020; 1:e34–e43 [View Article]
     [Google Scholar]
  33. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. Gigascience 2021; 10:giab008 [View Article]
     [Google Scholar]
  34. Carattoli A, Hasman H. Plasmidfinder and in silico pMLST: identification and typing of plasmid replicons in Whole-Genome Sequencing (WGS). Methods Mol Biol 2020; 2075:285–294 [View Article]
     [Google Scholar]
  35. Dohmen W, Bonten MJM, Bos MEH, van Marm S, Scharringa J et al. Carriage of extended-spectrum β-lactamases in pig farmers is associated with occurrence in pigs. Clin Microbiol Infect 2015; 21:917–923 [View Article] [PubMed]
     [Google Scholar]
  36. Hounmanou YMG, Bortolaia V, Dang STT, Truong D, Olsen JE et al. ESBL and AmpC β-Lactamase encoding genes in E. coli from Pig and Pig farm workers in Vietnam and their association with mobile genetic elements. Front Microbiol 2021; 12:629139 [View Article]
     [Google Scholar]
  37. Olaitan AO, Dandachi I, Baron SA, Daoud Z, Morand S et al. Banning colistin in feed additives: a small step in the right direction. Lancet Infect Dis 2021; 21:29–30 [View Article] [PubMed]
     [Google Scholar]
  38. Hallenberg GS, Jiwakanon J, Angkititrakul S, Kang-Air S, Osbjer K et al. Antibiotic use in pig farms at different levels of intensification-Farmers’ practices in northeastern Thailand. PLoS One 2020; 15:e0243099 [View Article] [PubMed]
     [Google Scholar]
  39. Tangkoskul T, Thamthaweechok N, Seenama C, Thamlikitkul V. Antibiotic-resistant bacteria and antibiotic residue contamination in fresh raw foods sold at wholesale markets in Thailand. J Med Assoc Thai 2021; 104:654–662 [View Article]
     [Google Scholar]
  40. Sadek M, Ortiz de la Rosa JM, Abdelfattah Maky M, Korashe Dandrawy M, Nordmann P et al. Genomic features of MCR-1 and extended-spectrum β-Lactamase-producing Enterobacterales from retail raw chicken in Egypt. Microorganisms 2021; 9:195 [View Article]
     [Google Scholar]
  41. Lo W-U, Chow K-H, Law PY, Ng K-Y, Cheung Y-Y et al. Highly conjugative IncX4 plasmids carrying blaCTX-M in Escherichia coli from humans and food animals. J Med Microbiol 2014; 63:835–840 [View Article] [PubMed]
     [Google Scholar]
  42. Irrgang A, Roschanski N, Tenhagen BA, Grobbel M, Skladnikiewicz-Ziemer T et al. Prevalence of mcr-1 in E. coli from livestock and food in Germany, 2010-2015. PLoS One 2016; 11:e0159863 [View Article]
     [Google Scholar]
  43. Zurfluh K, Nüesch-Inderbinen M, Klumpp J, Poirel L, Nordmann P et al. Key features of mcr-1-bearing plasmids from Escherichia coli isolated from humans and food. Antimicrob Resist Infect Control 2017; 6:91 [View Article]
     [Google Scholar]
  44. Sadek M, Ortiz de la Rosa JM, Ramadan M, Nordmann P, Poirel L. Molecular characterization of extended-spectrum ß-lactamase producers, carbapenemase producers, polymyxin-resistant, and fosfomycin-resistant Enterobacterales among pigs from Egypt. J Glob Antimicrob Resist 2022; 30:81–87 [View Article] [PubMed]
     [Google Scholar]
  45. Dhaouadi S, Soufi L, Hamza A, Fedida D, Zied C et al. Co-occurrence of mcr-1 mediated colistin resistance and β-lactamase-encoding genes in multidrug-resistant Escherichia coli from broiler chickens with colibacillosis in Tunisia. J Glob Antimicrob Resist 2020; 22:538–545 [View Article] [PubMed]
     [Google Scholar]
  46. Haenni M, Poirel L, Kieffer N, Châtre P, Saras E et al. Co-occurrence of extended spectrum β lactamase and MCR-1 encoding genes on plasmids. Lancet Infect Dis 2016; 16:281–282 [View Article] [PubMed]
     [Google Scholar]
  47. Pires J, Kuenzli E, Kasraian S, Tinguely R, Furrer H et al. Polyclonal intestinal colonization with extended-spectrum cephalosporin-resistant Enterobacteriaceae upon traveling to India. Front Microbiol 2016; 7:1069 [View Article]
     [Google Scholar]
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The risk of pig and chicken farming for carriage and transmission of Escherichia coli containing extended-spectrum beta-lactamase (ESBL) and mobile colistin resistance (mcr) genes in Thailand
M Gen 9, 000951 (2023); https://doi.org/10.1099/mgen.0.000951
/content/journal/mgen/10.1099/mgen.0.000951
/content/journal/mgen/10.1099/mgen.0.000951
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