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Extended-Spectrum β-Lactamase–Producing Enterobacteriaceae in Hospital Food: A Risk Assessment

Published online by Cambridge University Press:  10 May 2016

Andrew J. Stewardson
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Department of Medicine, University of Melbourne, Melbourne, Victoria, Australia
Gesuele Renzi
Affiliation:
Clinical Microbiology Laboratory, Service of Infectious Diseases, University of Geneva Hospitals, Geneva, Switzerland
Nathalie Maury
Affiliation:
Food Control Authority of Geneva, Geneva, Switzerland
Celia Vaudaux
Affiliation:
Catering Service, University of Geneva Hospitals, Geneva, Switzerland
Caroline Brassier
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Emmanuel Fritsch
Affiliation:
Staff Health Service, University of Geneva Hospitals, Geneva, Switzerland
Didier Pittet
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Max Heck
Affiliation:
National Institute for Public Health and the Environment, Bilthoven, the Netherlands
Kim van der Zwaluw
Affiliation:
National Institute for Public Health and the Environment, Bilthoven, the Netherlands
E. Ascelijn Reuland
Affiliation:
Department of Medical Microbiology and Infection Control, VU University Medical Centre, Amsterdam, the Netherlands
Thijs van de Laar
Affiliation:
Department of Medical Microbiology and Infection Control, VU University Medical Centre, Amsterdam, the Netherlands
Eveline Snelders
Affiliation:
Amphia Hospital, Breda, the Netherlands
Christina Vandenbroucke-Grauls
Affiliation:
Department of Medical Microbiology and Infection Control, VU University Medical Centre, Amsterdam, the Netherlands
Jan Kluytmans
Affiliation:
Department of Medical Microbiology and Infection Control, VU University Medical Centre, Amsterdam, the Netherlands Amphia Hospital, Breda, the Netherlands
Patrick Edder
Affiliation:
Food Control Authority of Geneva, Geneva, Switzerland
Jacques Schrenzel
Affiliation:
Clinical Microbiology Laboratory, Service of Infectious Diseases, University of Geneva Hospitals, Geneva, Switzerland
Stephan Harbarth
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Corresponding
E-mail address:

Abstract

Objective.

Determine the prevalence of extended-spectrum β-lactamase (ESBL)–producing Enterobacteriaceae (ESBL-PE) contamination of food and colonization of food handlers in a hospital kitchen and compare retrieved ESBL-PE strains with patient isolates.

Design.

Cross-sectional study.

Setting.

A 2,200-bed tertiary care university hospital in Switzerland.

Participants.

Food handlers.

Methods.

Raw and prepared food samples were obtained from the hospital kitchen, with a comparator group from local supermarkets. Fecal samples collected from food handlers and selectively pre-enriched homogenized food samples were inoculated onto selective chromogenic media. Phenotypic confirmation of ESBL production was performed using the double disk method. Representative ESBL-PE were characterized using polymerase chain reaction (PCR) and sequencing for bla CTX-M, bla SHV, and bla TEM genes, and Escherichia coli strains were typed using phylotyping, repetitive element palindromic PCR, and multilocus sequence typing. Meat samples were screened for antibiotic residues using liquid chromatography time-of-flight mass spectrometry.

Results.

Sixty (92%) of the raw chicken samples were ESBL-PE positive, including 30 (86%) of the hospital samples and all supermarket samples. No egg, beef, rabbit, or cooked chicken samples were ESBL-PE positive. No antibiotic residues were detected. Six (6.5%) of 93 food handlers were ESBL-PE carriers. ESBL-PE strains from chicken meat more commonly possessed bla CTX-M-1 and bla CTX-M-2, whereas bla CTX-M-14and bla CTX-M-15 were predominant among strains of human origin. There was partial overlap in the sequence type of E. coli strains of chicken and human origin. No E. coli ST131 strains or bla CTX-M-15 genes were isolated from meat.

Conclusions.

Although there is significant ESBL-PE contamination of delivered chicken meat, current preventive strategies minimize risks to food handlers, hospital staff, and patients.

Type
Original Article
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2014

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References

1. de Kraker, ME, Wolkewitz, M, Davey, PG, et al. Burden of antimicrobial resistance in European hospitals: excess mortality and length of hospital stay associated with bloodstream infections due to Escherichia coli resistant to third-generation cephalosporins. J Antimicrob Chemother 2011;66:398407.CrossRefGoogle ScholarPubMed
2. Wiklund, S, Hallberg, U, Kahlmeter, G, Tammelin, A. Living with extended-spectrum beta-lactamase: a qualitative study of patient experiences. Am J Infect Control 2013;41:723727.CrossRefGoogle ScholarPubMed
3. Stewardson, A, Fankhauser, C, De Angelis, G, et al. Burden of bloodstream infection caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae determined using multi-state modeling at a Swiss University Hospital and a nationwide predictive model. Infect Control Hosp Epidemiol 2013;34:133143.CrossRefGoogle Scholar
4. de Kraker, ME, Jarlier, V, Monen, JC, Heuer, OE, van de Sande, N, Grundmann, H. The changing epidemiology of bacteraemias in Europe: trends from the European Antimicrobial Resistance Surveillance System. Clin Microbiol Infect 2012;19:860868.CrossRefGoogle ScholarPubMed
5. Marshall, BM, Levy, SB. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 2011;24:718733.CrossRefGoogle ScholarPubMed
6. Kluytmans, JA, Overdevest, IT, Willemsen, I, et al. Extended-spectrum beta-lactamase-producing Escherichia coli from retail chicken meat and humans: comparison of strains, plasmids, resistance genes, and virulence factors. Clin Infect Dis 2013;56:478487.CrossRefGoogle ScholarPubMed
7. Liebana, E, Carattoli, A, Coque, TM, et al. Public health risks of enterobacterial isolates producing extended-spectrum beta-lactamases or AmpC beta-lactamases in food and food-producing animals: an EU perspective of epidemiology, analytical methods, risk factors, and control options. Clin Infect Dis 2013;56:10301037.CrossRefGoogle ScholarPubMed
8. Overdevest, I, Willemsen, I, Rijnsburger, M, et al. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg Infect Dis 2011;17:12161222.CrossRefGoogle ScholarPubMed
9. Leverstein-van Hall, MA, Dierikx, CM, Cohen Stuart, I, et al. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 2011;17:873880.CrossRefGoogle Scholar
10. Richards, J, Parr, E, Riseborough, P. Hospital food hygiene: the application of Hazard Analysis Critical Control Points to conventional hospital catering. J Hosp Infect 1993;24:273282.CrossRefGoogle ScholarPubMed
11. US Food and Drug Administration (FDA). FDA bacteriological analytical manual. http://www.fda.gov/Food/ScienceResearch/LaboratoryMethods/BacteriologicalAnalyticalManualBAM/default.htm. Accessed February 26, 2011.Google Scholar
12. Fankhauser, C, Zingg, W, Francois, P, et al. Surveillance of extended-spectrum-beta-lactamase-producing Enterobacteriaceae in a Swiss Tertiary Care Hospital. Swiss Med Wkly 2009;139:747751.Google Scholar
13. Samore, MH, Tonnerre, C, Hannah, EL, et al. Impact of Out-patient antibiotic use on carriage of ampicillin-resistant Escherichia coli . Antimicrob Agents Chemother 2011;55:11351141.CrossRefGoogle Scholar
14. Huttner, B, Haustein, T, Uckay, I, et al. Decolonization of intestinal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae with oral colistin and neomycin: a randomized, double-blind, placebo-controlled trial. J Antimicrob Chemother 2013;68:23752382.Google ScholarPubMed
15. Reuland, EA, Overdevest, IT, Al Naiemi, N, et al. High prevalence of ESBL-producing Enterobacteriaceae carriage in Dutch community patients with gastrointestinal complaints. Clin Microbiol Infect 2013;19:542549.CrossRefGoogle ScholarPubMed
16. Doumith, M, Day, MI, Hope, R, Wain, J, Woodford, N. Improved multiplex PCR strategy for rapid assignment of the four major Escherichia coli phylogenetic groups. J Clin Microbiol 2012;50:31083110.CrossRefGoogle ScholarPubMed
17. Wirth, T, Falush, D, Lan, R, et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006;60:11361151.CrossRefGoogle Scholar
18. Ojer-Usoz, E, Gonzalez, D, Vitas, Al, et al. Prevalence of extended-spectrum beta-lactamase-producing Enterobacteriaceae in meat products sold in Navarra, Spain. Meat Sci 2013;93:316321.CrossRefGoogle ScholarPubMed
19. Silva, N, Costa, L, Goncalves, A, et al. Genetic characterisation of extended-spectrum beta-lactamases in Escherichia coli isolated from retail chicken products including CTX-M-9 containing isolates: a food safely risk factor. Br Poult Sci 2012;53:747755.CrossRefGoogle Scholar
20. Egea, P, Lopez-Cerero, L, Navarro, MD, Rodriguez-Bano, J, Pascual, A. Assessment of the presence of extended-spectrum beta-lactamase-producing Escherichia coli in eggshells and ready-to-ea products. Eur J Clin Microbiol Infect Dis 2011;30:10451047.CrossRefGoogle ScholarPubMed
21. Cohen Stuart, J, van den Munckhof, T, Voets, G, Scharringa, J, Fluit, A, Hall, ML. Comparison of ESBL contamination in organic and conventional retail chicken meat. Int J Food Microbiol 2012;154:212214.CrossRefGoogle ScholarPubMed
22. Kola, A, Kohler, C, Pfeifer, Y, et al. High prevalence of extended-spectrum-beta-lactamase-producing Enterobacteriaceae in organic and conventional retail chicken meat, Germany. J Antimicrob Chemother 2012;67:26312634.CrossRefGoogle ScholarPubMed
23. Endimiani, A, Rossano, A, Kunz, D, Overesch, G, Perreten, V. First countrywide survey of third-generation cephalosporin-resistant Escherichia coli from broilers, swine, and cattle in Switzerland. Diagn Microbiol Infect Dis 2012;73:3138.CrossRefGoogle Scholar
24. Geser, N, Stephan, R, Hachler, H. Occurrence and characteristics of extended-spectrum beta-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res 2012;8:21.CrossRefGoogle ScholarPubMed
25. Grave, K, Greko, C, Kvaale, MK, et al. Sales of veterinary anti-bacterial agents in nine European countries during 2005–09: trends and patterns. J Antimicrob Chemother 2012;67:30013008.CrossRefGoogle ScholarPubMed
26. ARCH-Vet 2012: Report on the sales of antibiotics for veterinary use and antibiotic resistance monitoring of livestock in Switzerland, 2011. Bern, Switzerland: Federal Veterinary Office, 2012.Google Scholar
27. Walker, HW, Ayres, JC. Antibiotic residuals and microbial resistance in poultry treated with tetracyclines. Journal of Food Science 1958;23:525531.CrossRefGoogle Scholar
28. Food Safety and Inspection Service. 2011 US National Residue Program Data (“Red Book”). Washington, DC: US Department of Agriculture, 2013.Google Scholar
29. Lavilla, S, Gonzalez-Lopez, JJ, Miro, E, et al. Dissemination of extended-spectrum beta-lactamase-producing bacteria: the food-borne outbreak lesson. J Antimicrob Chemother 2008;61:12441251.CrossRefGoogle ScholarPubMed
30. del Campo, R, Ruiz-Garbajosa, P, Sanchez-Moreno, MP, et al. Antimicrobial resistance in recent fecal enterococci from healthy volunteers and food handlers in Spain: genes and phenotypes. Microb Drug Resist 2003;9:4760.CrossRefGoogle ScholarPubMed
31. Calbo, E, Freixas, N, Xercavins, M, et al. Foodborne nosocomial outbreak of SHVI and CTX-M-15-producing Klebsiella pneumoniae: epidemiology and control. Clin Infect Dis 2011;52:743749.CrossRefGoogle Scholar
32. Luo, Y, Cui, S, Li, J, et al. Characterization of Escherichia coli isolates from healthy food handlers in hospital. Microb Drug Resist 2011;17:443448.CrossRefGoogle ScholarPubMed
33. Geser, N, Stephan, R, Korczak, BM, Beutin, L, Hachler, H. Molecular identification of extended-spectrum-beta-lactamase genes from Enterobacteriaceae isolated from healthy human carriers in Switzerland. Antimicrob Agents Chemother 2012;56:16091612.CrossRefGoogle Scholar
34. Nuesch-Inderbinen, MT, Abgottspon, H, Zurfluh, K, Nuesch, HJ, Stephan, R, Hachler, H. Cross-sectional study on fecal carriage of Enterobacteriaceae with resistance to extended-spectrum cephalosporins in primary care patients. Microb Drug Resist 2013;19:362369.CrossRefGoogle ScholarPubMed
35. Redmond, EC, Griffith, CJ. Consumer food handling in the home: a review of food safety studies. J Food Prot 2003;66:130161.CrossRefGoogle ScholarPubMed
36. Hannah, EL, Johnson, JR, Angulo, F, Haddadin, B, Williamson, J, Samore, MH. Molecular analysis of antimicrobial-susceptible and -resistant Escherichia coli from retail meats and human stool and clinical specimens in a rural community setting. Foodborne Pathog Dis 2009;6:285295.CrossRefGoogle Scholar

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