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Investigation of antimicrobial resistance in pigeons (Columba livia domestica) using indicator bacteria

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The aim of this study was to determine the prevalence of antibiotic resistance as well as presence of resistance-associated genes in Escherichia coli and Enterococcus spp. strains isolated from pigeons. One hundred and fifty cloacal swabs were collected from apparently healthy pigeons in Hatay, Turkey, between March 2014 and June 2014. Antimicrobial susceptibilities of the isolates were tested with disc diffusion method, and resistance genes were investigated by polymerase chain reaction (PCR). E. coli were isolated from 94.7% (142) of the examined cloacal swab samples. E. coli isolates revealed higher resistance rates to tetracycline (51.4%) and ampicillin (50%), followed by

nalidixic acid (19.7%), streptomycin (12.7%), amoxycillin-clavulanic acid (15.5%), trimethoprim-sulfamethoxazole (10.6%), cephalothin (7.0%), ciprofloxacin (6.3%), kanamycin (4.9%), gentamicin (4.2%), tobramycin (4.2%), ceftazidime (4.2%), cefotaxime (4.2%), chloramphenicol (2.8%), aztreonam (2.8%), and cefoxitin (0.7%), respectively. Twentyeight (%19.7) E. coli isolates were susceptible to all tested antimicrobials. A total of 136 (90.7%) Enterococcus spp. were isolated and species distribution of the isolates was determined by species-specific PCR. The isolates were identified as 64 (47.1%) E. hirae, 17 (12.5%) E. faecium, 8 (5.9%) E. faecalis, 4 (2.9%) E. columbea, and 2 (1.5%) E. durans. The rest of the isolates (30.1%) were identified as Enterococcus spp. with the used primers. Enterococcus spp. were resistant to tetracycline (67.6%), erythromycin (23.5%), rifampicin (17.6%), chloramphenicol (6.6%) and ciprofloxacin (5.9%). By contrast, 38 (27.9%) Enterococcus spp. were sensitive to all tested antimicrobials. The data obtained in the study showed that pigeons were carriers of antimicrobial resistant E. coli and Enterococcus spp. in their intestinal microbiota, and may pose public health risk due to not only transmission of these resistant bacteria to humans but also contamination of the environment. The current status of antimicrobial resistance in different animal species should be continuosly monitored and control measures should also be taken.


Pigeon; antimicrobial resistance; Escherichia coli; Enterococcus spp.

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Aarestrup FM, Agrees Y, Gerner-Smith P, Madsen M, Jensen LB (2000) Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers and pigs in Denmark. Diagn Microbiol Infect Dis 37:127–137.

Aslantaş Ö (2018) Antimicrobial Resistance among Commensal Escherichia coli from Broilers in Turkey. Isr J Vet Med 73:19-25.

Aşkar Ş, Sakarya F, Yıldırım M (2011) The Potential Risk in Epizootiology

of Bacterial Zoonozis: Pigeon (Columba livia domestica) Feces. Kafkas Univ Vet Fak Derg 17(Suppl A): S13-S16.

Baele M, Devriese LA, Butaye P, Haesebrouck F (2002) Composition of enterococcal and streptococcal flora from pigeon intestines. J Appl Microbiol 92:348–351.

Blake DP, Humphry RW, Scott KP, Hillman K, Fenlon DR, Low JC (2003) Influence of tetracycline exposure on tetracycline resistance and the carriage of tetracycline resistance genes within commensal Escherichia coli populations. J Appl Microbiol 94:1087-1097.

Blanco-Peña K, Esperón F, Torres-Mejía AM, de la Torre A, de la Cruz E, Jiménez-Soto M (2017) Antimicrobial Resistance Genes in Pigeons from Public Parks in Costa Rica. Zoonoses Public Health. 64:e23-e30.

Cheng AC, Turnidge J, Collignon P, Looke D, Barton M, Gottlieb T (2012) Control of fluoroquinolone resistance through successful regulation, Australia. Emerg Infect Dis. 18:1453-1460.

Clinical and Laboratory Standards Institute (CLSI, 2012) Performance standards for antimicrobial susceptibility testing; eighteenth informational supplement. CLSI Document M100-S22.

da Silva VL, Caçador NC, da Silva Cdos S, Fontes CO, Garcia GD, Nicoli JR, Diniz CG (2012) Occurrence of multidrug-resistant and toxic-metal tolerant enterococci in fresh feces from urban pigeons in Brazil. Microbes Environ 27:179-85.

da Silva VL, Nicoli JR, Nascimento TC, Diniz CG (2009) Diarrheagenic Escherichia coli strains recovered from urban pigeons (Columba livia) in Brazil and their antimicrobial susceptibility patterns. Curr Microbiol 9:302-308.

del Campo R, Tenorio C, Rubio C, Castillo J, Torres C, Gómez-Lus R. (2000) Aminoglycoside-modifying enzymes in high-level streptomycin and gentamicin resistant Enterococcus spp. in Spain. Int J Antimicrob Agents 15:221-226.

Depardieu F, Perichon B, Courvalin P (2004) Detection of the van alphabet and identification of enterococci and staphylococci at the species level by multiplex PCR. J Clin Microbiol 42: 5857-5860.

Filazi A, Yurdakök Dikmen B, Kuzukıran Ö (2017) The usage of antimicrobial agents in poultry. Turkiye Klinikleri J Vet Sci Pharmacol Toxicol-Special Topics 3:181-187.

Frye JG, Jackson CR (2013) Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from U.S. food animals. Front Microbiol 4:135.

Ghanbarpour R, Aflatoonian MR, Askari A, Abiri Z, Naderi Z, Bagheri M, Jajarmi M, Shobeiri S, Molaei R, Askari N (2020) Domestic and game pigeons as reservoirs for Escherichia coli harboring antimicrobial resistance genes. J Glob Antimicrob Resist

Harada K, Asai T, Kojima A, Ishihara K, Takahashi T (2006) Role of coresistance in the development of resistance to chloramphenicol in Escherichia coli isolated from sick cattle and pigs. Am J Vet Res 67:230-235.

Jacoby GA, Hooper DC (2009) Prevalence of plasmid-mediated quinolone

resistance determinants over a 9-year period. Antimicrob Agents Chemother 53:639-645.

Jarlier V, Nicolas MH, Fournier G, Philippon A (1988) Extended broad-spectrum β-lactamases conferring transferable resistance to newer β-lactam agents in Enterobacteriaceae: Hospital prevalence and susceptibility patterns. Rev Infect Dis 10:867-878.

Kim HB, Park CH, Kim CJ, Kim EC, Jacoby GA, Hooper DC (2009) Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother. 53:639-45.

Kimpe A, Decostere A, Martel A, Haesebrouck F, Devriese LA (2002) Prevalence of antimicrobial resistance among pigeon isolates of Streptococcus gallolyticus, Escherichia coli and Salmonella enterica serotype Typhimurium. Avian Pathol 31:393-397.

Kojima A, Asai T, Ishihara K, Morioka A, Akimoto K, Sugimoto Y, Sato T, Tamura Y, Takahashi T (2009) National monitoring for antimicrobial resistance among indicator bacteria isolated from food-producing animals in Japan. J Vet Med Sci 71:1301-1308.

Kozak GK, Boerlin P, Janecko N, Reid-Smith RJ, Jardine C (2009) Antimicrobial resistance in Escherichia coli isolates from swine and wild

small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl Environ Microbiol 75:559-566.

Layton BA, Walters SP, Lam LH, Boehm AB (2010) Enterococcus species distribution among human and animal hosts using multiplex PCR. J Appl Microbiol 109:539-547.

Malhotra-Kumar S, Lammens C, Piessens J, Goossens H (2005) Multiplex

PCR for simultaneous detection of macrolide and tetracycline resistance determinants in streptococci. Antimicrob Agents Chemother 49:4798–4800.

Marothi YA, Agnihotri H, Dubey D (2005): Enterococcal resistance-an overview. Indian J Med Microbiol 23:214-219.

Maynard C, Bekal S, Sanschagrin F, Levesque RC, Brousseau R, Masson L, Larivière S, Harel J (2004) Heterogeneity among virulence and antimicrobial resistance gene profiles of extraintestinal Escherichia coli

isolates of animal and human origin. J Clin Microbiol 42:5444-5452.

Mehdi Y, Létourneau-Montminy MP, Gaucher ML, Chorfi Y, Suresh G, Rouissi T, Brar SK, Côté C, Ramirez AA, Godbout S (2018) Use of antibiotics in broiler production: Global impacts and alternatives. Anim Nutr 4:170-178.

Monstein HJ, Ostholm-Balkhed A, Nilsson MV, Nilsson M, Dornbusch K, Nilsson LE (2007) Multiplex PCR amplification assay for the detection of blaSHV, blaTEM and blaCTX-M genes in Enterobacteriaceae. APMIS 115:1400-1408.

Munita JM, Arias CA (2016) Mechanisms of Antibiotic Resistance. Review. Microbiol Spectr 4(2).

Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209–215.

Osman KM, Badr J, Orabi A, Elbehiry A, Saad A, Ibrahim MDS, Hanafy MH (2019) Poultry as a vector for emerging multidrug resistant Enterococcus

spp.: First report of vancomycin (van) and the chloramphenicol-florfenicol (cat-fex-cfr) resistance genes from pigeon and duck faeces. Microb Pathog 128:195-205.

Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC (2006) Prevalence

in the United States of aac(6)-Ib-cr encoding a ciprofloxacin modifying enzyme. Antimicrob Agents Chemother 50: 3953–3955.

Perez-Sancho M, García-Seco T, Porrero C, García N, Gomez-Barrero S, Cámara JM, Domínguez L, Álvarez J (2020) A ten-year-surveillance program of zoonotic pathogens in feral pigeons in the City of Madrid (2005-2014): The importance of a systematic pest control. Res VetSci 128:293-298.

Persoons D, Dewulf J, Smet A, Herman L, Heyndrickx M, Martel A, Catry

B, Butaye P, Haesebrouck F (2010) Prevalence and persistence of antimicrobial resistance in broiler indicator bacteria. Microb Drug Resist 16:67-74.

Radhouani H, Poeta P, Gonçalves A, Pacheco R, Sargo R, Igrejas G (2012)

Wild birds as biological indicators of environmental pollution: antimicrobial resistance patterns of Escherichia coli and enterococci isolated from common buzzards (Buteo buteo). J Med Microbiol 61:837-843.

Radimersky T, Frolkova P, Janoszowska D, Dolejska M, Svec P, Roubalova

E, Cikova P, Cizek A, Literak I (2010) Antibiotic resistance in faecal bacteria (Escherichia coli, Enterococcus spp.) in feral pigeons. J Appl Microbiol 109:1687-1695.

Santos T, Silva N, Igrejas G, Rodrigues P, Micael J, Rodrigues T, Resendes

R, Gonçalves A, Marinho C, Gonçalves D, Cunha R, Poeta P (2013) Dissemination of antibiotic resistant Enterococcus spp. And Escherichia coli from wild birds of Azores Archipelago. Anaerobe 24:25-31.

Skold O (2001) Resistance to trimethoprim and sulfonamides. Vet Res


van den Bogaard AE, Stobberingh EE (2000) Epidemiology of resistance

to antibiotics. Links between animals and humans. Int J Antimicrob

Agents 14:327-35.

Stenzel T, Bancerz-Kisiel A, Tykałowski B, Smiałek M, Pestka D, Koncicki

A (2014) Antimicrobial resistance in bacteria isolated from pigeons

in Poland. Pol J Vet Sci 17:169-71.

Vakulenko SB, Donabedian SM, Voskresenskiy AM, Zervos MJ, Lerner

SA, Chow JW (2003) Multiplex PCR for detection of aminoglycoside

resistance genes in enterococci. Antimicrob Agents Chemother.


Vasconcelos RH, de Castro Teixeira RS, da Silva ING, de Souza Lopes E,

Maciel WC (2018) Feral pigeons (Columba livia) as potential reservoirs

of Salmonella sp. and Escherichia coli. Arq Inst Biol 85:1-6.

Wang G, Clark CG., Rodgers FG (2002) Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. J Clin Microbiol 40:3613-3619.

World Health Organisation (WHO) (2012) Critically important antimicrobials for human medicine. 3rd revision 2011, 31. http://apps.who.int/iris/bitstream/10665/77376/1/9789241504485_eng.pdf [accessed 22 January 2019].

Wray C, Gnanou JC (2000) Antibiotic resistance monitoring in bacteria of

animal origin: analysis of national monitoring programs. Int J Antimicrob

Agents 14:291-294.

Zhao S, White DG, Mc Dermott PF, Friedman S, EnglishL, Ayers S, Meng

J, Maurer J, Holland R, Walker RD (2001) Identification and expression of cephamycinase blaCMY genes in Escherichia coli and Salmonella isolates from food animals and ground meat. Antimcrob. Agents Chemother 45:3647-3650.

Zigo F, Takac L, Zigova M, Takacova J, Vasi M (2017) Occurrence of antibiotic-resistant bacterial strains isolated in carrier pigeons during the race season. J Chem Pharm Res 10:10-13.


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