Skip to main content
    • Aa
    • Aa

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

  • Andrew J. Stewardson (a1) (a2), Gesuele Renzi (a3), Nathalie Maury (a4), Celia Vaudaux (a5), Caroline Brassier (a1), Emmanuel Fritsch (a6), Didier Pittet (a1), Max Heck (a7), Kim van der Zwaluw (a7), E. Ascelijn Reuland (a8), Thijs van de Laar (a8), Eveline Snelders (a9), Christina Vandenbroucke-Grauls (a8), Jan Kluytmans (a8) (a9), Patrick Edder (a4), Jacques Schrenzel (a3) and Stephan Harbarth (a1)...

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.


Cross-sectional study.


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


Food handlers.


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 blaCTX-M, blaSHV, and blaTEM 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.


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 blaCTX-M-1 and blaCTX-M-2, whereas blaCTX-M-14and blaCTX-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 blaCTX-M-15 genes were isolated from meat.


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

Corresponding author
Infection Control Program, University of Geneva Hospitals, and Faculty of Medicine, 4 Rue Gabrielle-Perret-Gentil, 1211 Geneva 14, Switzerland (
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

1.ME de Kraker , M Wolkewitz , PG Davey , 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.

2.S Wiklund , U Hallberg , G Kahlmeter , A Tammelin . Living with extended-spectrum beta-lactamase: a qualitative study of patient experiences. Am J Infect Control 2013;41:723727.

4.ME de Kraker , V Jarlier , JC Monen , OE Heuer , N van de Sande , H Grundmann . The changing epidemiology of bacteraemias in Europe: trends from the European Antimicrobial Resistance Surveillance System. Clin Microbiol Infect 2012;19:860868.

5.BM Marshall , SB Levy . Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 2011;24:718733.

6.JA Kluytmans , IT Overdevest , I Willemsen , 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.

7.E Liebana , A Carattoli , TM Coque , 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.

8.I Overdevest , I Willemsen , M Rijnsburger , et al.Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg Infect Dis 2011;17:12161222.

9.MA Leverstein-van Hall , CM Dierikx , I Cohen Stuart , et al.Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 2011;17:873880.

10.J Richards , E Parr , P Riseborough . Hospital food hygiene: the application of Hazard Analysis Critical Control Points to conventional hospital catering. J Hosp Infect 1993;24:273282.

13.MH Samore , C Tonnerre , EL Hannah , et al.Impact of Out-patient antibiotic use on carriage of ampicillin-resistant Escherichia coli. Antimicrob Agents Chemother 2011;55:11351141.

15.EA Reuland , IT Overdevest , N Al Naiemi , et al.High prevalence of ESBL-producing Enterobacteriaceae carriage in Dutch community patients with gastrointestinal complaints. Clin Microbiol Infect 2013;19:542549.

16.M Doumith , MI Day , R Hope , J Wain , N Woodford . Improved multiplex PCR strategy for rapid assignment of the four major Escherichia coli phylogenetic groups. J Clin Microbiol 2012;50:31083110.

17.T Wirth , D Falush , R Lan , et al.Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006;60:11361151.

18.E Ojer-Usoz , D Gonzalez , Al Vitas , et al.Prevalence of extended-spectrum beta-lactamase-producing Enterobacteriaceae in meat products sold in Navarra, Spain. Meat Sci 2013;93:316321.

19.N Silva , L Costa , A Goncalves , 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.

20.P Egea , L Lopez-Cerero , MD Navarro , J Rodriguez-Bano , A Pascual . 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.

21.J Cohen Stuart , T van den Munckhof , G Voets , J Scharringa , A Fluit , ML Hall . Comparison of ESBL contamination in organic and conventional retail chicken meat. Int J Food Microbiol 2012;154:212214.

22.A Kola , C Kohler , Y Pfeifer , 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.

23.A Endimiani , A Rossano , D Kunz , G Overesch , V Perreten . First countrywide survey of third-generation cephalosporin-resistant Escherichia coli from broilers, swine, and cattle in Switzerland. Diagn Microbiol Infect Dis 2012;73:3138.

24.N Geser , R Stephan , H Hachler . 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.

25.K Grave , C Greko , MK Kvaale , et al.Sales of veterinary anti-bacterial agents in nine European countries during 2005–09: trends and patterns. J Antimicrob Chemother 2012;67:30013008.

27.HW Walker , JC Ayres . Antibiotic residuals and microbial resistance in poultry treated with tetracyclines. Journal of Food Science 1958;23:525531.

29.S Lavilla , JJ Gonzalez-Lopez , E Miro , et al.Dissemination of extended-spectrum beta-lactamase-producing bacteria: the food-borne outbreak lesson. J Antimicrob Chemother 2008;61:12441251.

30.R del Campo , P Ruiz-Garbajosa , MP Sanchez-Moreno , 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.

31.E Calbo , N Freixas , M Xercavins , et al.Foodborne nosocomial outbreak of SHVI and CTX-M-15-producing Klebsiella pneumoniae: epidemiology and control. Clin Infect Dis 2011;52:743749.

32.Y Luo , S Cui , J Li , et al.Characterization of Escherichia coli isolates from healthy food handlers in hospital. Microb Drug Resist 2011;17:443448.

33.N Geser , R Stephan , BM Korczak , L Beutin , H Hachler . Molecular identification of extended-spectrum-beta-lactamase genes from Enterobacteriaceae isolated from healthy human carriers in Switzerland. Antimicrob Agents Chemother 2012;56:16091612.

34.MT Nuesch-Inderbinen , H Abgottspon , K Zurfluh , HJ Nuesch , R Stephan , H Hachler . Cross-sectional study on fecal carriage of Enterobacteriaceae with resistance to extended-spectrum cephalosporins in primary care patients. Microb Drug Resist 2013;19:362369.

36.EL Hannah , JR Johnson , F Angulo , B Haddadin , J Williamson , MH Samore . 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.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Infection Control & Hospital Epidemiology
  • ISSN: 0899-823X
  • EISSN: 1559-6834
  • URL: /core/journals/infection-control-and-hospital-epidemiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score