Abstract
Shiga toxin-producing Escherichia coli (STEC) strains are responsible for outbreaks of human intestinal diseases worldwide. Pigeons are distributed in public areas and are potential reservoirs for pathogenic bacteria. One hundred fifty-four fresh fecal samples were obtained from trapped pigeons in southeast of Iran and were cultured for isolation of E. coli. The isolates were examined to determine the prevalence of stx1, stx2, and eae genes, antimicrobial resistance, and their phylotypes. The confirmed E. coli isolates (138) belong to four phylogenetic groups: A (54.34%), B1 (34.05%), B2 (3.62%), and D (7.79%). Thirteen (9.42%) isolates were positive for one of the examined genes. Eight isolates (5.79%) were positive for eae, four (2.89%) for stx2, and one isolate (1.44%) for stx1 gene. Phylotyping assays showed that eight eae-positive isolates fall into three phylogroups; A (three isolates), B1 (three isolates), and D (two isolates), whereas four stx2-positive isolates belonged to the A (three isolates) and D (one isolate) groups. The stx1-positive isolate belonged to phylogroup A. One hundred six isolates (76.81%) showed resistance to at least one of the selected antibacterial agents. The maximum resistance rate was against oxytetracycline (73.91%), and the minimum was against flumequine (2.17%). Twenty different patterns of drug resistance were observed. According to the results, pigeons could be considered as carriers of STEC strains. However, E. coli isolates of pigeon feces increase the potential of these birds to act as a reservoir of multiple antibiotic resistant bacteria.
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Aidar, L., Penteado, A.S., Trabulsi, L.R., Blanco, J.E., Blanco, M., Blanco, J. and Pestana de Castro, A.F., 2000. Subtypes of intimin among non toxigenic Escherichia coil from diarrheic calves in Brazil. The Canadian Journal of Veterinary Research, 64, 15–20
Aidar-Ugrinovich, L., Blanco, J., Blanco, M., Blanco, J.E., Leomil, L., Dahbi, G., Mora, A., Onuma, D.L., Silveira, W.D. and Pestana de Castro, A.F., 2007. Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) isolated from calves in São Paulo, Brazil. International Journal of Food Microbiology, 115, 297–306
Cízek, A., Literák, I. and Scheer, P., 2000. Survival of Escherichia coli O157 in faeces of experimentally infected rats and domestic pigeons. Letters in Applied Microbiology, 31, 349–52
Clermont, O., Bonacorsi, S. and Bingen, E., 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology, 66, 4555–4558
CLSI (2004) Clinical Laboratory Standards Institute guidelines, 2004. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard M31-S1, Villanova, Pennsylvania.
Coombes, B.K., Gilmour, M.W. and Goodman, C.D., 2011. The evolution of virulence in non-O157 Shiga toxin-producing Escherichia coli. Frontiers in Microbiology, 2, 1–3
Dissanayake, D.R., Wijewardana, T.G., Gunawardena, G.A. and Poxton, I.R., 2008. Distribution of lipopolysaccharide core types among avian pathogenic Escherichia coli in relation to the major phylogenetic groups. Veterinary Microbiology, 132, 355–363
Dutta, T.K., Roychoudhury, P., Bandyopadhyay, S., Wani, S.A. and Hussain, I., 2011. Detection and characterization of shiga toxin producing Escherichia coli (STEC) and enteropathogenic Escherichia coli (EPEC) in poultry birds with diarrhoea. Indian Journal of Medical Research, 133, 541–545
Farooq, S., Hussain, I., Mir, M.A., Bhat, M.A. and Wani, S.A., 2009. Isolation of atypical enteropathogenic Escherichia coli and shiga toxin 1 and 2f-producing Escherichia coli from avian species in India. Letters in Applied Microbiology, 48, 692–697
Fukuyama, M., Furuhata, K., Oonaka, K., Sakata, S., Hara, M., Kakuno, Y., Itoh, T., Kai, A., Obata, H. and Watanabe, T., 2003. Isolation and serotypes of Vero toxin-producing Escherichia coli (VTEC) from pigeons and crows. Kansenshogaku Zasshi, 77, 5–9
Ghanbarpour, R., Sami, M., Salehi, M. and Ouromiei, M., 2011. Phylogenetic background and virulence genes of Escherichia coli isolates from colisepticemic and healthy broiler chickens in Iran. Tropical Animal Health and Production, 43, 153–157
Gordon, D.M., Clermont, O., Tolley, H. and Denamur, E., 2008. Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environmental Microbiology, 10, 2484–2496
Grossmann, K., Weniger, B., Baljer, G., Brenig, B. and Wieler, L.H., 2005. Racing, ornamental and city pigeons carry shiga toxin producing Escherichia coli (STEC) with different shiga toxin subtypes, urging further analysis of their epidemiological role in the spread of STEC. Berliner und Munchener Tierarztliche, 118, 456–463
Johnson, J.R., Murray, A.C., Gajewski, A., Sullivan, M., Snippes, P., Kuskowski, M.A. and Smith, K.E., 2003. Isolation and molecular characterization of nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrobial Agents and Chemotherapy, 47, 2161–2168
Kawano, K., Ono, H., Iwashita, O., Kurogi, M., Haga, T., Maeda, K. and Goto, Y., 2011. stx Genotype and molecular epidemiological analyses of shiga toxin-producing Escherichia coli O157:H7/H− in human and cattle isolates. European Journal of Clinical Microbiology and Infectious Disease, DOI 10.1007/s10096-011-1283-1
Kimpe, A., Decostere, A., Martel, A., Haesebrouck, F. and Devriese, L.A., 2002. Prevalence of antimicrobial resistance among pigeon isolates of Streptococcus gallolyticus, Escherichia coli and Salmonella enterica serotype Typhimurium. Avian Pathology, 31, 393–397
Kobayashi, H., Pohjanvirta, T. and Pelkonan, S., 2002. Prevalence and characteristics of intimin and shigatoxin producing Escherichia coli from gulls, pigeons and broilers in Finland. Journal of Veterinary Medical Science, 64, 1071–1073
Lee K., French, N.P., Hara-Kudo, Y., Iyoda, S., Kobayashi, H., Sugita-Konishi, Y., Tsubone, H. and Kumagai, S., 2011. Multivariate analyses revealed distinctive features differentiating human and cattle isolates of shiga toxin-producing Escherichia coli O157 in Japan. Journal of Clinical Microbiology, 49, 1495–500
Martin, A. and Beutin, L., 2011. Characteristics of shiga toxin-producing Escherichia coli from meat and milk products of different origins and association with food producing animals as main contamination sources. International Journal of Food Microbiology, 146, 99–104
Morabito, S., Dell’Omo, G., Agrimi, U., Schmidt, H., Karch, H., Cheasty, T. and Caprioli, A., 2001. Detection and characterization of shiga toxin-producing Escherichia coli in feral pigeons. Veterinary Microbiology, 82, 275–283
Moreno, E., Prats, G., Sabate, M., Perez, T., Johnson, J.R. and Andreu, A., 2006. Quinolone, fluoroquinolone and trimethoprim/sulfamethoxazole resistance in relation to virulence determinants and phylogenetic background among uropathogenic Escherichia coli. Journal of Antimicrobial Chemotherapy, 57, 204–211
Moulin-Schouleur, M., Schouler, C., Tailliez, P., Kao, M.R., Bree, A., Germon, P., Oswald, E., Mainil, J., Blanco, M. and Blanco, J., 2006. Common virulence factors and genetic relationships between O18:K1:H7 Escherichia coli isolates of human and avian origin. Journal of Clinical Microbiology, 44, 3484–3492
Nguyen, T.D., Thanh, T.V. and Vu-Khac, H., 2011. Virulence factors in Escherichia coli isolated from calves with diarrhea in Vietnam. Journal of Veterinary Science, 12, 159–164 O U R N A L O F
Parreira, V.R. and Gyles, C.L., 2002. Shiga toxin genes in avian Escherichia coli. Veterinary Microbiology, 87, 341–352
Paton, J.C. and Paton, A.W., 1998. Detection and characterization of shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfb O111 , and rfb O157 . Journal of Clinical Microbiology, 36, 598–602
Pedersen, K., Clark, L., Andelt, W.F. and Salman, M.D., 2006. Prevalence of shiga toxin-producing Escherichia coli and Salmonella enterica in rock pigeons captured in Fort Collins, Colorado. Journal of Wildlife Disease, 42, 46–55
Radimersky, T., Frolkova, P., Janoszowska, D., Dolejska, M., Svec, P., Roubalova, E., Cikova, P., Cizek, A. and Literak, I., 2010. Antibiotic resistance in faecal bacteria (Escherichia coli, Enterococcus spp.) in feral pigeons. Journal of Applied Microbiology, 109, 1687–95
Rodriguez-Siek, K.E., Giddings, C.W., Doetkott, C., Johnson, T.J., Fakhr M.K. and Nolan, L.K., 2005. Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology, 151, 2097–2110
Salehi, M. and Ghanbarpour R., 2010. Phenotypic and genotypic properties of Escherichia coli isolated from colisepticemic cases of Japanese quail. Tropical Animal Health and Production, 42, 1497–1504
Schaffzin, J.K., Dumas, N.B., Root, T.P., Halse, T.A., Schoonmaker-Bopp, D.J., Lurie, M.M. Nicholas, D., Gerzonich, B., Johnson, G.S., Wallace, B.J. and Musser, K.A., 2011. Public health approach to detection of non-O157 shiga toxin-producing Escherichia coli: summary of two outbreaks and laboratory procedures. Epidemiology and Infection, DOI:10.1017/S0950268811000719
Schmidt, H., Morabito, S., Caprioli, A., Wieler, L.H. and Karch, H., 2000. A new shiga toxin 2 variant (Stx2f) from Escherichia coli isolated from pigeons. Applied and Environmental Microbiology, 66, 1205–1208
Silva, V.L., Nicoli, J.R., Nascimento, T.C. and Diniz, C.G., 2009. Diarrheagenic Escherichia coli trains recovered from urban pigeons (Columba livia) in Brazil and their antimicrobial susceptibility patterns. Current Microbiology, 59, 302–308
Sonntag, A.K., Zenner, E., Karch, H. and Bielaszewska, M., 2005. Pigeons as a possible reservoir of shiga toxin 2f-producing Escherichia coli pathogenic to humans. Berliner und Munchener Tierarztliche, 118, 464–470
Tanaka, C., Miyazawa, T., Watarai, M. and Ishiguro, N., 2005. Bacteriological survey of feces from feral pigeons in Japan. Journal of Veterinary Medical Science, 67, 951–953
Tramuta, C., Robino, P. and Nebbia, P., 2008. Phylogenetic background of attaching and effacing Escherichia coli isolates from animals. Veterinary Research Communication, 32, 433–437
Acknowledgments
The authors are grateful to Prof. Eric Oswald (Ecole Nationale Vétérinaire, Toulouse, France) for providing the reference strains. This work was supported by a grant from the Shahid Bahonar University of Kerman.
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Ghanbarpour, R., Daneshdoost, S. Identification of shiga toxin and intimin coding genes in Escherichia coli isolates from pigeons (Columba livia) in relation to phylotypes and antibiotic resistance patterns. Trop Anim Health Prod 44, 307–312 (2012). https://doi.org/10.1007/s11250-011-0021-0
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DOI: https://doi.org/10.1007/s11250-011-0021-0