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Volume 19, Number 8—August 2013

Human Deaths and Third-Generation Cephalosporin use in Poultry, Europe

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To the Editor: Globally, antimicrobial drug resistance is rapidly rising, with resultant increased illness and death. Of particular concern is Escherichia coli, the most common bacterium to cause invasive disease in humans (1). In Europe, increasing proportions of bloodstream infections caused by E. coli are resistant to third-generation cephalosporins (1,2).

Resistant E. coli can be transmitted to humans from animals. A large proportion of resistant isolates causing human infections are derived from food animals (36). However, lack of data has made it difficult to quantify the proportion of antimicrobial drug resistant E. coli infecting persons through food sources and the resultant effects on human health. Recent data from the Netherlands now make such estimates possible (2,6). The additional illness and death among humans resulting from bloodstream infections caused by third-generation cephalosporin–resistant E. coli (G3CREC) has been calculated for Europe (2). In the Netherlands, there were 205 G3CREC cases during 2007 (4% of all E. coli bloodstream infections) (2). Another study in the Netherlands revealed that 56% of the resistance genes in G3CREC in humans were identical to genes derived from E. coli isolated from retail chicken samples (6). Using the findings of Overdevest et al. (6) and de Kraker et al. (2), we calculated that, in the Netherlands, infections in humans with G3CREC derived from poultry sources were associated with 21 additional deaths. G3CREC-related illness also resulted in 908 hospital bed-days needed to treat persons with these antimicrobial drug resistant bloodstream infections. If these values were extrapolated to all of Europe (i.e., if 56% of G3CREC were derived from poultry), 1,518 additional deaths and an associated increase of 67,236 days of hospital admissions would be counted as a result of cephalosporin and other antimicrobial drug use in poultry (Technical Appendix).

To more accurately estimate the associated increased deaths among persons resulting from third-generation cephalosporin use in poultry, detailed data from more countries is essential. Needed data include records of antimicrobial drug use and resistant bacterial strains found in food animals and domestic and imported foods. However, we already know that G3CREC is rapidly rising in many countries, and in Europe, the infection rate is likely to have tripled from 2007 to 2012 (2). Globally, billions of chickens receive third-generation cephalosporins in ovo or as day-old chicks to treat E. coli infection, a practice that has resulted in large reservoirs of resistant bacteria. In Canada, this practice has been associated with substantial increases in resistance to third-generation cephalosporins in Salmonella enterica serovar Heidelberg isolates detected in humans. (7). The United States Food and Drug Administration recently prohibited the off-label use of cephalosporins, including prophylactic uses, in major food animal species, including poultry (8).

The number of avoidable deaths and the costs of health care potentially caused by third-generation cephalosporin use in food animals is staggering. Considering those factors, the ongoing use of these antimicrobial drugs in mass therapy and prophylaxis should be urgently examined and stopped, particularly in poultry, not only in Europe, but worldwide.


Peter CollignonComments to Author , Frank M. Aarestrup, Rebecca Irwin, and Scott McEwen
Author affiliations: The Canberra Hospital, Garran, Canberra, Australian Capital Territory, Australia (P. Collignon); Australian National University, Woden, Australian Capital Territory, Australia (P. Collignon); EU Reference Laboratory for Antimicrobial Resistance. Copenhagen, Denmark (F.M. Aarestrup); World Health Organization Collaborating Centre for Antimicrobial Resistance in Foodborne Pathogens, Copenhagen (F.M. Aarestrup); Public Health Agency of Canada. Guelph, Ontario, Canada (R. Irwin); Ontario Veterinary College/University of Guelph, Guelph (S. McEwen)



  1. European Centre for Disease Prevention and Control. Antimicrobial resistance surveillance in Europe 2010. Annual report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). Stockholm: The Centre; 2011.
  2. de Kraker  ME, Davey  PG, Grundmann  H; BURDEN study group. Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe. PLoS Med. 2011;8:e1001104 and. Epub 2011 Oct 11. DOIPubMedGoogle Scholar
  3. Jakobsen  L, Spangholm  DJ, Pedersen  K, Jensen  LB, Emborg  HD, Agersø  Y, Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans and UTI patients. Int J Food Microbiol. 2010;142:26472. DOIPubMedGoogle Scholar
  4. Vieira  AR, Collignon  P, Aarestrup  FM, McEwen  SA, Hendriksen  RS, Hald  T, Association between antimicrobial resistance in Escherichia coli isolates from food animals and blood stream isolates from humans in Europe: an ecological study. Foodborne Pathog Dis. 2011;8:1295301. DOIPubMedGoogle Scholar
  5. Johnson  JR, Sannes  MR, Croy  C, Johnston  B, Clabots  C, Kuskowski  MA, Antimicrobial drug–resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004. Emerg Infect Dis. 2007;13:83846. DOIPubMedGoogle Scholar
  6. Overdevest  I, Willemsen  I, Rijnsburger  M, Eustace  A, Xu  L, Hawkey  P, Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg Infect Dis. 2011;17:121622. DOIPubMedGoogle Scholar
  7. Dutil  L, Irwin  R, Finley  R, Ng  LK, Avery  B, Boerlin  P, Ceftiofur resistance in Salmonella enterica serovar Heidelberg from chicken meat and humans, Canada. Emerg Infect Dis. 2010;16:4854. DOIPubMedGoogle Scholar
  8. US Food and Drug Administration. Cephalosporin order of prohibition goes into effect. April 6, 2012 [cited 2012 Apr 20].


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DOI: 10.3201/eid1908.120681

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Peter Collignon, Infectious Diseases and Microbiology, Canberra Hospital, PO Box 11, Woden. ACT 2607, Australia

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Page created: July 11, 2013
Page updated: July 11, 2013
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The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.