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Decreasing prevalence of contamination with extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E) in retail chicken meat in the Netherlands


Autoři: Pepijn Huizinga aff001;  Marjolein Kluytmans-van den Bergh aff001;  John W. Rossen aff005;  Ina Willemsen aff001;  Carlo Verhulst aff001;  Paul H. M. Savelkoul aff006;  Alexander W. Friedrich aff005;  Silvia García-Cobos aff005;  Jan Kluytmans aff001
Působiště autorů: Department of Infection Control, Amphia Hospital, Breda, the Netherlands aff001;  Laboratory for Medical Microbiology and Immunology, Elisabeth-TweeSteden Hospital, Tilburg, the Netherlands aff002;  Amphia Academy Infectious Disease Foundation, Amphia Hospital, Breda, the Netherlands aff003;  Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands aff004;  University of Groningen, University Medical Center Groningen, Department of Medical Microbiology and Infection Prevention, Groningen, the Netherlands aff005;  Maastricht University Medical Center, Caphri School for Public Health and Primary Care, Department of Medical Microbiology, Maastricht, the Netherlands aff006;  Amsterdam University Medical Center, Vrije Universiteit Amsterdam, Department of Medical Microbiology & Infection Control, Amsterdam, the Netherlands aff007
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226828

Souhrn

Retail chicken meat is a potential source of extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E). In the past decade, vast national efforts were undertaken to decrease the antibiotic use in the veterinary sector, resulting in a 58% decrease in antibiotic sales in the sector between 2009 and 2014. This decrease in antibiotic use was followed by a decrease in ESBL-E prevalence in broilers. The current study investigates the prevalence of contamination with ESBL-E in retail chicken meat purchased in the Netherlands between December 2013 and August 2015. It looks at associations between the prevalence of contamination with ESBL-E and sample characteristics such as method of farming (free-range or conventional), supermarket chain of purchase and year of purchase. In the current study, 352 chicken meat samples were investigated for the presence of ESBL-E using selective culture methods. Six samples were excluded due to missing isolates or problems obtaining a good quality sequence leaving 346 samples for further analyses. Of these 346 samples, 188 (54.3%) were positive for ESBL-E, yielding 216 ESBL-E isolates (Escherichia coli (n = 204), Klebsiella pneumoniae (n = 11) and Escherichia fergusonii (n = 1)). All ESBL-E isolates were analysed using whole-genome sequencing. The prevalence of contamination with ESBL-E in retail chicken meat decreased from 68.3% in 2014 to 44.6% in 2015, absolute risk difference 23.7% (95% confidence interval (CI): 12.6% - 34.1%). The ESBL-E prevalence was lower in free-range chicken meat (36.4%) compared with conventional chicken meat (61.5%), absolute risk difference 25.2% (95% CI: 12.9% - 36.5%). The prevalence of contamination with ESBL-E varied between supermarket chains, the highest prevalence of contamination was found in supermarket chain 4 (76.5%) and the lowest in supermarket chain 1 (37.8%). Pairwise isolate comparisons using whole-genome multilocus sequence typing (wgMLST) showed that clustering of isolates occurs more frequently within supermarket chains than between supermarket chains. In conclusion, the prevalence of contamination with ESBL-E in retail chicken in the Netherlands decreased over time; nevertheless, it remains substantial and as such a potential source for ESBL-E in humans.

Klíčová slova:

Agriculture – Antibiotics – Antimicrobial resistance – Enterobacteriaceae – Chickens – Livestock – Meat – Sequence analysis


Zdroje

1. Melzer M, Petersen I. Mortality following bacteraemic infection caused by extended spectrum beta-lactamase (ESBL) producing E. coli compared to non-ESBL producing E. coli. J Infect. 2007;55: 254–259. doi: 10.1016/j.jinf.2007.04.007 17574678

2. Rottier WC, Ammerlaan HSM, Bonten MJM. Effects of confounders and intermediates on the association of bacteraemia caused by extended-spectrum b -lactamase-producing Enterobacteriaceae and patient outcome: a meta-analysis. 2012; 1311–1320. doi: 10.1093/jac/dks065 22396430

3. Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A, Simonsen GS, et al. 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. 2018;3099: 1–11. doi: 10.1016/S1473-3099(18)30605-4 30409683

4. Tumbarello M, Spanu T, Di Bidino R, Marchetti M, Ruggeri M, Trecarichi EM, et al. Costs of bloodstream infections caused by Escherichia coli and influence of extended-spectrum-beta-lactamase production and inadequate initial antibiotic therapy. Antimicrob Agents Chemother. 2010;54: 4085–4091. doi: 10.1128/AAC.00143-10 20660675

5. Rottier WC, van Werkhoven CH, Bamberg YRP, Dorigo-Zetsma JW, van de Garde EM, van Hees BC, et al. Development of diagnostic prediction tools for bacteraemia caused by third-generation cephalosporin-resistant enterobacteria in suspected bacterial infections: a nested case-control study. Clin Microbiol Infect. Elsevier Ltd; 2018;24: 1315–1321. doi: 10.1016/j.cmi.2018.03.023 29581056

6. Rottier WC, Bamberg YRP, Dorigo-Zetsma JW, van der Linden PD, Ammerlaan HSM, Bonten MJM. Predictive value of prior colonization and antibiotic use for third-generation cephalosporin-resistant enterobacteriaceae bacteremia in patients with sepsis. Clin Infect Dis. 2015;60: 1622–30. doi: 10.1093/cid/civ121 25694654

7. Denis B, Lafaurie M, Donay J-L, Fontaine J-P, Oksenhendler E, Raffoux E, et al. Prevalence, risk factors, and impact on clinical outcome of extended-spectrum beta-lactamase-producing Escherichia coli bacteraemia: a five-year study. Int J Infect Dis. 2015;39: 1–6. doi: 10.1016/j.ijid.2015.07.010 26189774

8. European Centre for Disease Prevention and Control (ECDC). Antimicrobial resistance surveillance in Europe 2014. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). Stockholm: ECDC; 2015 [Internet]. 2015.

9. Stobberingh EE, Arends J, Hoogkamp-Korstanje JAA, Goessens WHF, Visser MR, Buiting AGM, et al. Occurrence of extended-spectrum beta-lactamases (ESBL) in Dutch hospitals. Infection. 1999;27: 348–354. doi: 10.1007/s150100050041 10624595

10. Livermore DM, Canton R, Gniadkowski M, Nordmann P, Rossolini GM, Arlet G, et al. CTX-M: Changing the face of ESBLs in Europe [Internet]. Journal of Antimicrobial Chemotherapy. 2007. pp. 165–174. doi: 10.1093/jac/dkl483 17158117

11. Bunt van den G, Pelt van W, Hidalgo L, Scharringa J, Greeff SC de, Schürch AC, et al. Prevalence, risk factors and genetic characterization of Extended-Spectrum Beta-Lactamase and Carbapenemase-producing Enterobacteriaceae (ESBL-E and CPE): a community-based repeated cross-sectional study in the Netherlands from 2014 to 2016. Eurosurveillance (forthcoming). 2019; eurosurveillance-D-18-00594R1

12. Cohen Stuart J, van den Munckhof T, Voets G, Scharringa J, Fluit A, Van Hall ML. Comparison of ESBL contamination in organic and conventional retail chicken meat. Int J Food Microbiol. Elsevier B.V.; 2012;154: 212–214. doi: 10.1016/j.ijfoodmicro.2011.12.034 22260927

13. Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, et al. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect. 2011;17: 873–880. doi: 10.1111/j.1469-0691.2011.03497.x 21463397

14. Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, et al. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg Infect Dis. 2011;17: 1216–1222. doi: 10.3201/eid1707.110209 21762575

15. Dierikx C, van der Goot J, Fabri T, van Essen-Zandbergen A, Smith H, Mevius D. Extended-spectrum-β-lactamase- and AmpC-β-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J Antimicrob Chemother. 2013;68: 60–67. doi: 10.1093/jac/dks349 22949623

16. Liu CM, Stegger M, Aziz M, Johnson TJ, Waits K, Nordstrom L, et al. Escherichia coli ST131-H22 as a Foodborne Uropathogen. MBio. 2018;9: 1–11. doi: 10.1128/mBio.00470-18 30154256

17. Muloi D, Ward MJ, Pedersen AB, Fèvre EM, Woolhouse MEJ, van Bunnik BAD. Are Food Animals Responsible for Transfer of Antimicrobial-Resistant Escherichia coli or Their Resistance Determinants to Human Populations? A Systematic Review. Foodborne Pathog Dis. 2018;15: 467–474. doi: 10.1089/fpd.2017.2411 29708778

18. Dorado-García A, Smid JH, van Pelt W, Bonten MJM, Fluit AC, van den Bunt G, et al. Molecular relatedness of ESBL/AmpC-producing Escherichia coli from humans, animals, food and the environment: a pooled analysis. J Antimicrob Chemother. 2018;73: 339–347. doi: 10.1093/jac/dkx397 29165596

19. Kluytmans JAJW, Overdevest ITMA, Willemsen I, Den Bergh MFQK, Van Der Zwaluw K, Heck M, et al. Extended-Spectrum β -Lactamase–Producing Escherichia coli From Retail Chicken Meat and Humans : Comparison of Strains, Plasmids, Resistance Genes, and Virulence Factors. 2013;56: 478–487. doi: 10.1093/cid/cis929 23243181

20. Veldman K, Mevius D. Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2017 (MARAN 2018) [Internet]. 2018. https://www.wur.nl/en/show/Maran-rapport-2018.htm

21. Bergevoet R, van Asseldonk M, Bondt N, van Horne P, Hoste R, de Lauwere C, et al. Economics of antibiotic usage on Dutch farms—The impact of antibiotic reduction on economic results of pig and broiler farms in the Netherlands [Internet]. 2019. https://edepot.wur.nl/475403

22. Terluin I, Verhoog D, Dagevos H, van Horne P, Hoste R. Vleesconsumptie per hoofd van de bevolking in Nederland, 2005–2016 [Internet]. Wageningen; 2017.

23. Nielsen. Markets and Finances. In: Markets and Finances [Internet]. 2017 [cited 14 Oct 2019]. https://www.nielsen.com/nl/nl/insights/article/2017/nielsen-release-market-shares/

24. Netherlands Society for Medical Microbiology. NVMM Guideline Laboratory detection of highly resistant microorganisms, version 2.0, 2012. Leeuwarden, Netherlands. 2012; http://www.nvmm.nl/system/files/2012.11.15richtlijnBRMO%2528version2.0%2529-RICHTLIJN.pdf

25. European Committee on Antimicrobial Susceptibility Testing. Guidelines for detection of resistance mechanisms and specific resistance of clinical and/or epidemiological importance. Version 2.0 [Internet]. 2017. www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Resistance_mechanisms/EUCAST_detection_of_resistance_mechanisms_170711.pdf

26. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters, version 7.1 [Internet]. 2017. http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_7.1_Breakpoint_Tables.pdf

27. Kluytmans-van den Bergh MFQ, Rossen JWA, Bruijning-Verhagen PCJ, Bonten MJM, Friedrich AW, Vandenbroucke-Grauls CMJE, et al. Whole genome multilocus sequence typing of extended-spectrum beta-lactamase-producing Enterobacteriaceae. J Clin Microbiol. 2016;54: 2919–2927. doi: 10.1128/JCM.01648-16 27629900

28. Larsen MV., Cosentino S, Lukjancenko O, Saputra D, Rasmussen S, Hasman H, et al. Benchmarking of methods for genomic taxonomy. J Clin Microbiol. 2014;52: 1529–1539. doi: 10.1128/JCM.02981-13 24574292

29. 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: 2640–2644. doi: 10.1093/jac/dks261 22782487

30. 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: 3895–903. doi: 10.1128/AAC.02412-14 24777092

31. Thomsen MCF, Ahrenfeldt J, Cisneros JLB, Jurtz V, Larsen MV, Hasman H, et al. A Bacterial Analysis Platform: An Integrated System for Analysing Bacterial Whole Genome Sequencing Data for Clinical Diagnostics and Surveillance. PLoS One. 2016;11: e0157718. doi: 10.1371/journal.pone.0157718 27327771

32. Seemann T. mlst. In: https://github.com/tseemann/mlst.

33. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, et al. Sex and virulence in Escherichia coli: An evolutionary perspective. Mol Microbiol. 2006;60: 1136–1151. doi: 10.1111/j.1365-2958.2006.05172.x 16689791

34. Alikhan NF, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018;14: 1–13. doi: 10.1371/journal.pgen.1007261 29621240

35. Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O. ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb genomics. 2018;4. doi: 10.1099/mgen.0.000192 29916797

36. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: Improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep. 2013; doi: 10.1111/1758-2229.12019 23757131

37. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2007;23: 127–8. doi: 10.1093/bioinformatics/btl529 17050570

38. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. Oxford University Press; 2019;47: W256–W259. doi: 10.1093/nar/gkz239 30931475

39. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4: 406–25. Available: http://www.ncbi.nlm.nih.gov/pubmed/3447015 doi: 10.1093/oxfordjournals.molbev.a040454

40. Agresti A, Coull BA. Approximate is better than “Exact” for interval estimation of binomial proportions. Am Stat. 1998;52: 119–126. doi: 10.1080/00031305.1998.10480550

41. Knol MJ, Le Cessie S, Algra A, Vandenbroucke JP, Groenwold RHH. Overestimation of risk ratios by odds ratios in trials and cohort studies: Alternatives to logistic regression. Cmaj. 2012;184: 895–899. doi: 10.1503/cmaj.101715 22158397

42. Zhang J, Yu KF. What’s the relative risk? A method of correcting the odds ratio in cohort studies of common outcomes. JAMA. 1998;280: 1690–1. Available: http://www.ncbi.nlm.nih.gov/pubmed/9832001 doi: 10.1001/jama.280.19.1690

43. Schmidt CO, Kohlmann T. When to use the odds ratio or the relative risk? Relative Risk and odds ratio in epidemiology. Int J Public Heal. 2008;5308: 165–167.

44. Veldman K, Mevius D. Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2016 (MARAN 2017) [Internet]. 2017. https://www.wur.nl/upload_mm/c/8/4/50343a1f-a2ad-4389-8208-d0e595b9a946_Maranreport2017.pdf

45. Veldman K, Dierikx C, Mevius D. Monitoring of antimicrobial resistance and antibiotic asage in animals in the Netherlands in 2014 (MARAN 2015) [Internet]. 2015. https://www.wur.nl/upload_mm/1/3/3/53df1fe1-ca3d-4050-a4ad-a1fde4ed158b_NethmapMaran2015.pdf

46. Mevius D, Dierikx C, Wit B, van Pelt W, Heederik D. Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2013 (MARAN 2014) [Internet]. 2014. https://www.wur.nl/upload_mm/4/a/4/46c626bf-5ccb-4996-a294-3e9ef4843355_NethMap-MARAN2014.pdf

47. Veldman K, Kant A, Dierikx C, van Essen-Zandbergen A, Wit B, Mevius D. Enterobacteriaceae resistant to third-generation cephalosporins and quinolones in fresh culinary herbs imported from Southeast Asia. Int J Food Microbiol. Elsevier B.V.; 2014;177: 72–77. doi: 10.1016/j.ijfoodmicro.2014.02.014 24607424

48. Miranda JM, Guarddon M, Vázquez BI, Fente CA, Barros-Velázquez J, Cepeda A, et al. Antimicrobial resistance in Enterobacteriaceae strains isolated from organic chicken, conventional chicken and conventional turkey meat: A comparative survey. Food Control. 2008;19: 412–416. doi: 10.1016/j.foodcont.2007.05.002

49. Davis GS, Waits K, Nordstrom L, Grande H, Weaver B, Papp K, et al. Antibiotic-resistant Escherichia coli from retail poultry meat with different antibiotic use claims. BMC Microbiol. 2018;18: 174. doi: 10.1186/s12866-018-1322-5 30390618

50. Ellen H, Leenstra F, van Emous R, Groenestein K, van Ham J, van Horne P, et al. Vleeskuikenproductiesystemen in Nederland [Internet]. Livestock Research. Lelystad, the Netherland; 2012. https://www.wageningenur.nl/nl/Publicatie-details.htm?publicationId=publication-way-343237323531

51. Ceccarelli D, Kant A, van Essen-Zandbergen A, Dierikx C, Hordijk J, Wit B, et al. Diversity of Plasmids and Genes Encoding Resistance to Extended Spectrum Cephalosporins in Commensal Escherichia coli From Dutch Livestock in 2007–2017. Front Microbiol. 2019;10: 1–9.

52. Van Der Bij AK, Peirano G, Goessens WHF, Van Der Vorm ER, Van Westreenen M, Pitout JDD. Clinical and molecular characteristics of extended-spectrum-beta-lactamase-producing Escherichia coli causing bacteremia in the Rotterdam Area, Netherlands. Antimicrob Agents Chemother. 2011;55: 3576–3578. doi: 10.1128/AAC.00074-11 21502612

53. Börjesson S, Bengtsson B, Jernberg C, Englund S. Spread of extended-spectrum beta-lactamase producing Escherichia coli isolates in Swedish broilers mediated by an incl plasmid carrying bla(CTX-M-1). Acta Vet Scand. 2013;55: 3. doi: 10.1186/1751-0147-55-3 23336334

54. Ludden C, Moradigaravand D, Jamrozy D, Gouliouris T, Blane B, Naydenova P, et al. A One Health study of the genetic relatedness of Klebsiella pneumoniae and their mobile elements in the East of England. Clin Infect Dis. 2019; 1–28. doi: 10.1093/cid/ciz174 30840764

55. Hayashi W, Ohsaki Y, Taniguchi Y, Koide S, Kawamura K, Suzuki M, et al. High prevalence of blaCTX-M-14among genetically diverse Escherichia coli recovered from retail raw chicken meat portions in Japan. Int J Food Microbiol. Elsevier; 2018;284: 98–104. doi: 10.1016/j.ijfoodmicro.2018.08.003 30096596

56. Jouini A, Ben Slama K, Klibi N, Ben Sallem R, Estepa V, Vinué L, et al. Lineages and virulence gene content among extended-spectrum β-lactamase-producing Escherichia coli strains of food origin in Tunisia. J Food Prot. 2013;76: 323–7. doi: 10.4315/0362-028X.JFP-12-251 23433382

57. Kluytmans-van den Bergh MFQ, Verhulst C, Willemsen LE, Verkade E, Bonten MJM, Kluytmans JAJW. Rectal Carriage of Extended-Spectrum-Beta-Lactamase-Producing Enterobacteriaceae in Hospitalized Patients: Selective Preenrichment Increases Yield of Screening. J Clin Microbiol. 2015;53: 2709–12. doi: 10.1128/JCM.01251-15 25994164

58. Overdevest ITMA, Willemsen I, Elberts S, Verhulst C, Kluytmans JAJW. Laboratory detection of extended-spectrum-beta-lactamase-producing Enterobacteriaceae: evaluation of two screening agar plates and two confirmation techniques. J Clin Microbiol. 2011;49: 519–22. doi: 10.1128/JCM.01953-10 21123527

59. Jolley KA, Maiden MCJ. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics. 2010;11: 595. doi: 10.1186/1471-2105-11-595 21143983


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