Prevalence of extended-spectrum cephalosporinase (ESC)-producing Escherichia coli in Danish slaughter pigs and retail meat identified by selective enrichment and association with cephalosporin usage.

OBJECTIVES To investigate the prevalence of extended-spectrum cephalosporinase (ESC)-producing Escherichia coli in pigs at slaughter and retail meat, and possible associations with the consumption of third- and fourth-generation cephalosporins. METHODS During 2009, faecal samples from Danish pigs (n=786) were collected at slaughter, and 866 meat samples [Danish: pork (153), broiler meat (121) and beef (142); and imported: pork (173), broiler meat (193) and beef (84)] were randomly collected in retail stores and outlets. E. coli was isolated after enrichment in MacConkey broth with ceftriaxone (1 mg/L). ESC genotypes were detected using PCR, microtube array and sequencing. The MIC of cefotaxime was determined for 150 E. coli from the pigs and 606 E. coli from meat isolated without selective enrichment. RESULTS Eleven percent (86/786) of slaughter pigs contained ESC E. coli and a significantly higher prevalence was observed among pigs originating from farms with registered cephalosporin consumption in slaughter pigs (P=0.034). Among ESC E. coli from pigs, 66% contained bla(CTX-M-1). From meat, a high prevalence of ESC E. coli was found in imported broiler meat (36%) compared with 0.7%-3.3% in other meat types. ESC E. coli from imported broiler meat (n=69) contained bla(CMY-2) (48%), bla(CTX-M-1) (25%) and bla(SHV-12) (16%). Without selective enrichment, no ESC E. coli from pigs and only 4.1% from imported broiler meat were found. CONCLUSIONS The usage of cephalosporins for slaughter pigs may increase the prevalence of ESC E. coli in slaughter pigs. Meat may be a source of ESCs in humans, especially imported broiler meat. Selective enrichment should be considered as a supplementary surveillance method.

[1]  T. Hald,et al.  Association between antimicrobial resistance in Escherichia coli isolates from food animals and blood stream isolates from humans in Europe: an ecological study. , 2011, Foodborne pathogens and disease.

[2]  Birgitte Borck Høg,et al.  DANMAP 2010: DANMAP 2010 - Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark , 2011 .

[3]  M. Bonten,et al.  Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. , 2011, Clinical Microbiology and Infection.

[4]  A. Hammerum,et al.  Faecal carriage of extended-spectrum β-lactamase-producing and AmpC β-lactamase-producing bacteria among Danish army recruits. , 2011, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[5]  B. Söderquist,et al.  Molecular and phenotypic characterization of Escherichia coli and Klebsiella pneumoniae producing extended‐spectrum β‐lactamases with focus on CTX‐M in a low‐endemic area in Sweden , 2011, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[6]  J. Klena,et al.  CTX-M-15-producing Escherichia coli clinical isolates in Cairo (Egypt), including isolates of clonal complex ST10 and clones ST131, ST73, and ST405 in both community and hospital settings. , 2011, Microbial drug resistance.

[7]  N. Woodford,et al.  Cephalosporin resistance mechanisms in Escherichia coli isolated from raw chicken imported into the UK. , 2010, The Journal of antimicrobial chemotherapy.

[8]  F. Aarestrup,et al.  Evaluation of eight different cephalosporins for detection of cephalosporin resistance in Salmonella enterica and Escherichia coli. , 2010, Microbial drug resistance.

[9]  F. Aarestrup,et al.  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. , 2010, International journal of food microbiology.

[10]  J. Dewulf,et al.  Characterization of extended-spectrum beta-lactamases produced by Escherichia coli isolated from hospitalized and nonhospitalized patients: emergence of CTX-M-15-producing strains causing urinary tract infections. , 2010, Microbial drug resistance.

[11]  F. Aarestrup,et al.  Escherichia coli isolates from broiler chicken meat, broiler chickens, pork, and pigs share phylogroups and antimicrobial resistance with community-dwelling humans and patients with urinary tract infection. , 2010, Foodborne pathogens and disease.

[12]  L. Ng,et al.  Ceftiofur Resistance in Salmonella enterica Serovar Heidelberg from Chicken Meat and Humans, Canada , 2010, Emerging infectious diseases.

[13]  F. Aarestrup,et al.  Emergence of Multidrug-Resistant Salmonella Concord Infections in Europe and the United States in Children Adopted From Ethiopia, 2003–2007 , 2009, The Pediatric infectious disease journal.

[14]  H. Hasman,et al.  Characterization of genetic determinants of extended-spectrum cephalosporinases (ESCs) in Escherichia coli isolates from Danish and imported poultry meat. , 2009, The Journal of antimicrobial chemotherapy.

[15]  N. Woodford,et al.  Redefining extended-spectrum beta-lactamases: balancing science and clinical need. , 2008, The Journal of antimicrobial chemotherapy.

[16]  F. Aarestrup,et al.  Development of a miniaturised microarray-based assay for the rapid identification of antimicrobial resistance genes in Gram-negative bacteria. , 2008, International journal of antimicrobial agents.

[17]  F. Aarestrup,et al.  Molecular characterization and occurrence of extended-spectrum beta-lactamase resistance genes among Salmonella enterica serovar Corvallis from Thailand, Bulgaria, and Denmark. , 2006, Microbial drug resistance.

[18]  F. Aarestrup,et al.  First description of blaCTX-M-1-carrying Escherichia coli isolates in Danish primary food production. , 2006, The Journal of antimicrobial chemotherapy.

[19]  F. Aarestrup,et al.  First description of an oxyimino-cephalosporin-resistant, ESBL-carrying Escherichia coli isolated from meat sold in Denmark. , 2006, The Journal of antimicrobial chemotherapy.

[20]  F. Aarestrup,et al.  Resistant Salmonella Virchow in Quail Products , 2005, Emerging infectious diseases.

[21]  M. Kuskowski,et al.  Antimicrobial-resistant and extraintestinal pathogenic Escherichia coli in retail foods. , 2005, The Journal of infectious diseases.

[22]  M. Kaufmann,et al.  Community and hospital spread of Escherichia coli producing CTX-M extended-spectrum beta-lactamases in the UK. , 2004, The Journal of antimicrobial chemotherapy.

[23]  F. Aarestrup,et al.  International Spread of blaCMY-2-Mediated Cephalosporin Resistance in a Multiresistant Salmonella enterica Serovar Heidelberg Isolate Stemming from the Importation of a Boar by Denmark from Canada , 2004, Antimicrobial Agents and Chemotherapy.

[24]  E. Nelson,et al.  Molecular Basis of AmpC Hyperproduction in Clinical Isolates of Escherichia coli , 1999, Antimicrobial Agents and Chemotherapy.

[25]  Wenyaw Chan,et al.  Statistical Methods in Medical Research , 2013, Model. Assist. Stat. Appl..

[26]  T. Højbjerg,et al.  Emergence of third-generation cephalosporin-resistant Escherichia coli from bloodstream infections in Denmark: this is due to both clonal and non-clonal spread of CTX-M-15 , 2011 .

[27]  D. Paterson,et al.  Extended-spectrum and CMY-type beta-lactamase-producing Escherichia coli in clinical samples and retail meat from Pittsburgh, USA and Seville, Spain. , 2010, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[28]  Clinical,et al.  Performance Standards for Antimicrobial Susceptibility Testing; Eighteenth Informational Supplement , 2008 .

[29]  F. Aarestrup,et al.  Prevalence of beta-lactamases among ampicillin-resistant Escherichia coli and Salmonella isolated from food animals in Denmark. , 2004, Microbial drug resistance.