Abstract
The principal objective of this study was to assess whether chicken eggshells may be contaminated by ESBL-producing E. coli (ESBLC). Additional analyses were carried out to determine if ESBLEC could be detected in other foodstuffs such as cooked poultry or fresh vegetables. Seventy-two eggshells from different supermarkets and stores as well as 32 salads, 30 samples of cooked poultry and six samples of chicken-based pet food samples were analysed. Characterization of ESBL was performed by PCR and sequencing. Antimicrobial resistance was determined by disk diffusion method. Phylogenetic group was assigned by multiplex-PCR. No ESBLEC was isolated from chicken eggshells, cooked chicken and pet food. One SHV-12-producing E. coli was isolated from a salad sample. This is the first study to analyse chicken eggs in an area where there is a high prevalence of ESBLEC in retail chicken meat.
Similar content being viewed by others
References
Blanc V, Mesa R, Saco M, Lavilla S, Prats G, Miro E, Navarro F, Cortes P, Llagostera M (2006) ESBL- and plasmidic class C beta-lactamase-producing E. coli strains isolated from poultry, pig and rabbit farms. Vet Microbiol 118:299–304
Bortolaia V, Guardabassi L, Bisgaard M, Larsen J, Bojesen AM (2010) Escherichia coli producing CTX-M-1, -2, and -9 group beta-lactamases in organic chicken egg production. Antimicrob Agents Chemother 54:3527–3528
Brinas L, Moreno MA, Zarazaga M, Porrero C, Saenz Y, Garcia M, Dominguez L, Torres C (2003) Detection of CMY-2, CTX-M-14, and SHV-12 beta-lactamases in Escherichia coli fecal-sample isolates from healthy chickens. Antimicrob Agents Chemother 47:2056–2058
Carattoli A, Lovari S, Franco A, Cordaro G, Di Matteo P, Battisti A (2005) Extended-spectrum beta-lactamases in Escherichia coli isolated from dogs and cats in Rome, Italy, from 2001 to 2003. Antimicrob Agents Chemother 49:833–835
Chavez C, Knape KD, Coufal CD, Carey JB (2002) Reduction of eggshell aerobic plate counts by ultraviolet irradiation. Poult Sci 81:1132–1135
Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558
Clinical and Laboratory Standards Institute (2009) Performance standards for antimicrobial susceptibility testing: 19th informational supplement. M100-S19. CLSI, Wayne, PA
Costa D, Poeta P, Brinas L, Saenz Y, Rodrigues J, Torres C (2004) Detection of CTX-M-1 and TEM-52 beta-lactamases in Escherichia coli strains from healthy pets in Portugal. J Antimicrob Chemother 54:960–961
Doi Y, Paterson DL, Egea P, Pascual A, Lopez-Cerero L, Navarro MD, Adams-Haduch JM, Qureshi ZA, Sidjabat HE, Rodriguez-Bano J (2010) Extended-spectrum and CMY-type beta-lactamase-producing Escherichia coli in clinical samples and retail meat from Pittsburgh, USA and Seville, Spain. Clin Microbiol Infect 16:33–38
Duan RS, Sit TH, Wong SS, Wong RC, Chow KH, Mak GC, Yam WC, Ng LT, Yuen KY, Ho PL (2006) Escherichia coli producing CTX-M beta-lactamases in food animals in Hong Kong. Microb Drug Resist 12:145–148
Huneau-Salaun A, Michel V, Huonnic D, Balaine L, Le Bouquin S (2010) Factors influencing bacterial eggshell contamination in conventional cages, furnished cages and free-range systems for laying hens under commercial conditions. Br Poult Sci 51:163–169
Jensen LB, Hasman H, Agerso Y, Emborg HD, Aarestrup FM (2006) First description of an oxyimino-cephalosporin-resistant, ESBL-carrying Escherichia coli isolated from meat sold in Denmark. J Antimicrob Chemother 57:793–794
Johnson JR, Murray AC, Gajewski A, Sullivan M, Snippes P, Kuskowski MA, Smith KE (2003) Isolation and molecular characterization of nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrob Agents Chemother 47:2161–2168
Manfreda G, Cevoli C, Lucchi A, Pasquali F, Fabbri A, Franchini A (2010) Hot air treatment for surface decontamination of table eggs experimentally infected with Salmonella, Listeria, and Escherichia coli. Vet Res Commun 34(Suppl 1):S179–S182
Mesa RJ, Blanc V, Blanch AR, Cortes P, Gonzalez JJ, Lavilla S, Miro E, Muniesa M, Saco M, Tortola MT, Mirelis B, Coll P, Llagostera M, Prats G, Navarro F (2006) Extended-spectrum beta-lactamase-producing Enterobacteriaceae in different environments (humans, food, animal farms and sewage). J Antimicrob Chemother 58:211–215
Musgrove MT, Jones DR, Northcutt JK, Cox NA, Harrison MA (2004) Identification of Enterobacteriaceae from washed and unwashed commercial shell eggs. J Food Prot 67:2613–2616
Oteo J, Navarro C, Cercenado E, Delgado-Iribarren A, Wilhelmi I, Orden B, Garcia C, Miguelanez S, Perez-Vazquez M, Garcia-Cobos S, Aracil B, Bautista V, Campos J (2006) Spread of Escherichia coli strains with high-level cefotaxime and ceftazidime resistance between the community, long-term care facilities, and hospital institutions. J Clin Microbiol 44:2359–2366
Patterson PH, Ricke SC, Sunde ML, Schaefer DM (1990) Hatching eggs sanitized with chlorine dioxide foam: egg hatchability and bactericidal properties. Avian Dis 34:1–6
Rasheed JK, Jay C, Metchock B, Berkowitz F, Weigel L, Crellin J, Steward C, Hill B, Medeiros AA, Tenover FC (1997) Evolution of extended-spectrum beta-lactam resistance (SHV-8) in a strain of Escherichia coli during multiple episodes of bacteremia. Antimicrob Agents Chemother 41:647–653
Rodriguez-Romo LA, Yousef AE (2005) Inactivation of Salmonella enterica serovar Enteritidis on shell eggs by ozone and UV radiation. J Food Prot 68:711–717
Sabate M, Tarrago R, Navarro F, Miro E, Verges C, Barbe J, Prats G (2000) Cloning and sequence of the gene encoding a novel cefotaxime-hydrolyzing beta-lactamase (CTX-M-9) from Escherichia coli in Spain. Antimicrob Agents Chemother 44:1970–1973
Smet A, Martel A, Persoons D, Dewulf J, Heyndrickx M, Catry B, Herman L, Haesebrouck F, Butaye P (2008) Diversity of extended-spectrum beta-lactamases and class C beta-lactamases among cloacal Escherichia coli Isolates in Belgian broiler farms. Antimicrob Agents Chemother 52:1238–1243
Teshager T, Dominguez L, Moreno MA, Saenz Y, Torres C, Cardenosa S (2000) Isolation of an SHV-12 beta-lactamase-producing Escherichia coli strain from a dog with recurrent urinary tract infections. Antimicrob Agents Chemother 44:3483–3484
Warren RE, Ensor VM, O'Neill P, Butler V, Taylor J, Nye K, Harvey M, Livermore DM, Woodford N, Hawkey PM (2008) Imported chicken meat as a potential source of quinolone-resistant Escherichia coli producing extended-spectrum beta-lactamases in the UK. J Antimicrob Chemother 61:504–508
Acknowledgments
This study was supported by the Ministerio de Sanidad y Consumo, Instituto de Salud Carlos III - FEDER, Spanish Network for Research into Infectious Diseases (REIPI RD06/0008), Fondo de Investigación Sanitaria (FIS), Instituto de Salud Carlos III (PI070190), Consejerías de Salud e Innovación, Junta de Andalucía (PI-0048/2008 and CTS-5259) and the Ministerio de Educación y Ciencia (AGL-2008-02129). We thank Beatriz Muñoz Hurtado for her assistance in European and Spanish legislation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Egea, P., López-Cerero, L., Navarro, M.D. et al. Assessment of the presence of extended-spectrum beta-lactamase-producing Escherichia coli in eggshells and ready-to-eat products. Eur J Clin Microbiol Infect Dis 30, 1045–1047 (2011). https://doi.org/10.1007/s10096-011-1168-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10096-011-1168-3