Abstract
Despite a lot of information about virulence and resistance of Escherichia coli (E. coli) in poultry, very limited data are currently available on its occurrence in pigeon isolates, although this poses a threat to human and animal health. Therefore, this study was conducted to explore the phylogenetic classification, antibiotic sensitivity, and virulence factors in E. coli isolated from cloacal swabs of domestic pigeons bred for meat (n = 47) and racing pigeons (n = 44). The most frequent phylogroup in racing pigeons was E (36, 82.00%), unlike domestic pigeons (B2- 19, 40.00%). The most abundant iron uptake system in both groups of bird was feoB (racing = 40, 90.90%; domestic = 44, 93.61%). The presence of ibeA (52, 57.10%) and kpsMTII (46, 50.50%) genes was detected in more than half of all strains belonging exclusively to phylogroups B2, D, E, F, clade I. Antibiotic resistance was higher in racing pigeons. All racing pigeon isolates were resistant to tetracycline and trimethoprim + sulphonamide. Resistance to ciprofloxacin was determined in three isolates (6.38%) of domestic and 33 isolates (75%) of racing pigeons. Aminoglycosides and β-lactamases resistance were also recorded. One of the important detected phenotypic mechanisms of resistance occurring in isolates from racing pigeons was AGL AAC(6´)I. Our study confirms that healthy pigeons are a reservoir of antibiotic-resistant E. coli containing an arsenal of virulence factors, thus capable of potentially causing infection. Pigeons with the option to fly to multiple places can transfer virulent and resistant bacteria. Direct contact with pigeons and their faeces and the contamination of water and food pose a threat of infection to humans and other animal species.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Aslantaş Ö, Gövce N (2020) Investigation of antimicrobial resistance in pigeons (Columba livia domestica) using indicator bacteria. J Hellenic Vet Med Soc 71(2):2095. https://doi.org/10.12681/jhvms.23632
Bessède E, Angla-gre M, Delagarde Y, Sep Hieng S, Ménard A, Mégraud F (2011) Matrix-assisted laser-desorption/ionization BIOTYPER: experience in the routine of a University hospital. Clin Microbiol Infect 17(4):533–538. https://doi.org/10.1111/j.1469-0691.2010.03274.x
Borges CA, Maluta RP, Beraldo LG et al (2017) Captive and free-living urban pigeons (Columba livia) from Brazil as carriers of multidrug-resistant pathogenic Escherichia coli. Vet J 219:65–67. https://doi.org/10.1016/j.tvjl.2016.12.015
Capita R, Cordero J, Molina-González D, Igrejas G, Poeta P, Alonso-Calleja C (2019) Phylogenetic diversity, Antimicrobial susceptibility and virulence characteristics of Escherichia coli isolates from Pigeon Meat. Antibiotics 8(4):259. https://doi.org/10.12681/jhvms.23632doi:10.3390/antibiotics8040259
Carvalho D, Kunert-Filho HC, Simoni C, de Moraes LB, Furian TQ, Borges KA, Breunig JG, Medeiros LP, Kobayashi RKT, de Brito KCT, de Brito BG (2020) Antimicrobial susceptibility and detection of virulence-associated genes of Escherichia coli and Salmonella spp isolated from domestic pigeons (Columba livia) in Brazil. Folia Microbiol 65(4):735–745. https://doi.org/10.1007/s12223-020-00781-w
Chrobak-Chmiel D, Kwiecien E, Golke A, Dolka B, Adamczyk K, Bieganska MJ, Spinu M, Binek M, Rzewuska M (2021) Pigeons as carriers of clinically relevant Multidrug-Resistant Pathogens—A clinical Case Report and Literature Review. Front Vet Sci 8:664226. https://doi.org/10.3389/fvets.2021.664226
Clermont O, Christenson JK, Denamur E, Gordon DM (2013) The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups: a new E. coli phylo-typing method. Environ Microbiol Reports 5(1):58–65. https://doi.org/10.1111/1758-2229.12019
Clermont O, Condamine B, Dion S, Gordon DM, Denamur E (2021) The E phylogroup of Escherichia coli is highly diverse and mimics the whole E. coli species population structure. Environ Microbiol 23(11):7139–7151. https://doi.org/10.1111/1462-2920.15742
de Lastours V, Laouénan C, Royer G, Carbonnelle E, Lepeule R, Esposito-Farèse M, Clermont O, Duval X, Fantin B, Mentré F, Decousser JW, Denamur E, Lefort A (2020) Mortality in Escherichia coli bloodstream infections: antibiotic resistance still does not make it. J Antimicrob Chemother 75(8):2334–2343. https://doi.org/10.1093/jac/dkaa161
Dozois CM, Dho-Moulin M, Brée A, Fairbrother JM, Desautels C, Curtiss R (2000) Relationship between the Tsh Autotransporter and Pathogenicity of Avian Escherichia coli and Localization and Analysis of the tsh Genetic Region. O’Brien AD, ed. Infect Immun 68(7):4145–4154. https://doi.org/10.1128/IAI.68.7.4145-4154.2000
Escobar-Páramo P, Clermont O, Blanc-Potard AB, Bui H, Le Bouguénec C, Denamur E (2004) A specific genetic background is required for Acquisition and expression of virulence factors in Escherichia coli. Mol Biol Evol 21(6):1085–1094. https://doi.org/10.1093/molbev/msh118
Ewers C, Li G, Wilking H, Kiessling S, Alt K, Antáo EM, Laturnus C, Diehl I, Glodde S, Homeier T, Böhnke U, Steinrück H, Philipp HC, Wieler LH (2007) Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int J Med Microbiol 297(3):163–176. https://doi.org/10.1016/j.ijmm.2007.01.003
Gabale U, Peña Palomino PA, Kim H, Chen W, Ressl S (2020) The essential inner membrane protein YejM is a metalloenzyme. Sci Rep 10(1):17794. https://doi.org/10.1038/s41598-020-73660-6
Galardini M, Clermont O, Baron A, Busby B, Dion S, Schubert S, Beltrao P, Denamur E (2020) Major role of iron uptake systems in the intrinsic extra-intestinal virulence of the genus Escherichia revealed by a genome-wide association study. Didelot X, ed. PLoS Genet 16(10):e1009065. https://doi.org/10.1371/journal.pgen.1009065
Gattringer R, Niks M, Ostertag R, Ostertág R, Schwarz K, Medvedovic H, Graninger W, Georgopoulos A (2002) Evaluation of MIDITECH automated colorimetric MIC reading for antimicrobial susceptibility testing. J Antimicrob Chemother 49(4):651–659. https://doi.org/10.1093/jac/49.4.651
Germon P, Chen YH, He L et al (2005) The ibeA, a virulence factor of avian pathogenic Escherichia coli. Microbiology 51(4):1179–1186. https://doi.org/10.1099/mic.0.27809-0
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 harbouring antimicrobial resistance genes. J Global Antimicrob Resist 22:571–577. https://doi.org/10.1016/j.jgar.2020.02.015
Grenni P, Ancona V, Caracciolo AB (2018) Ecological effects of antibiotics on natural ecosystems: a review. Microchem J 136:25–39
Jeong J, Lee JY, Kang M, Lee H, Kang S, Lee OM, Kwon YK, Kim JH (2021) Comparative Characteristics and Zoonotic Potential of Avian Pathogenic Escherichia coli (APEC) Isolates from Chicken and Duck in South Korea. Microorganisms 9: 946. https://doi.org/10.3390/microorganisms9050946
Johnson JR, Stell AL (2000) Extended virulence genotypes of Escherichia coli strains from patients with Urosepsis in relation to phylogeny and host compromise. J Infect Dis 181(1):261–272. https://doi.org/10.1086/315217
Johnson JR, Russo TA, Tarr PI, Carlino U, Bilge SS, Vary JC Jr, Stell AL (2000) Molecular Epidemiological and Phylogenetic Associations of Two Novel Putative Virulence Genes, iha and iroN E. coli, among Escherichia coli Isolates from Patients with Urosepsis. Tuomanen EI, ed. Infect Immun 68(5):3040–3047. https://doi.org/10.1128/IAI.68.5.3040-3047.2000
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(7):2161–2168. https://doi.org/10.1128/AAC.47.7.2161-2168.2003
Johnson TJ, Wannemuehler Y, Doetkott C, Johnson SJ, Rosenberger SC, Nolan LK (2008) Identification of minimal predictors of avian pathogenic Escherichia coli Virulence for Use as a Rapid Diagnostic Tool. J Clin Microbiol 46(12):3987–3996. https://doi.org/10.1128/JCM.00816-08
Johnson JR, Johnston BD, Porter S, Thuras P, Aziz M, Price LB (2018) Accessory traits and phylogenetic background predict Escherichia coli Extraintestinal Virulence Better Than does ecological source. J Infect Dis Published online August 2. https://doi.org/10.1093/infdis/jiy459
Kallonen T, Brodrick HJ, Harris SR, Corander J, Brown NM, Martin V, Peacock SJ, Parkhill J (2017) Systematic longitudinal survey of invasive Escherichia coli in England demonstrates a stable population structure only transiently disturbed by the emergence of ST131. Genome Res 27(8):1437–1449. https://doi.org/10.1101/gr.216606.116
Karim SJI, Islam M, Sikder T, Rubaya R, Halder J, Alam J (2020) Multidrug-resistant Escherichia coli and Salmonella spp. isolated from pigeons. Vet World 13(10):2156–2165. https://doi.org/10.14202/vetworld.2020.2156-2165
Le Bouguénec C, Archambaud M, Labigne A (1992) Rapid and specific detection of the pap, afa, and sfa adhesin-encoding operons in uropathogenic Escherichia coli strains by polymerase chain reaction. J Clin Microbiol 30(5):1189–1193. https://doi.org/10.1128/jcm.30.5.1189-1193.1992
Lescat M, Clermont O, Woerther PL, Glodt J, Dion S, Skurnik D, Djossou F, Dupont C, Perroz G, Picard B, Catzeflis F, Andremont A, Denamur E (2013) Commensal Escherichia coli strains in Guiana reveal a high genetic diversity with host-dependant population structure: commensal Escherichia coli population structure. Environ Microbiol Rep 5(1):49–57. https://doi.org/10.1111/j.1758-2229.2012.00374.x
Li Y, Dai J, Zhuge X, Wang H, Hu L, Ren J, Chen L, Li D, Tang F (2016) Iron-regulated gene ireA in avian pathogenic Escherichia coli participates in adhesion and stress-resistance. BMC Vet Res 12(1):167. https://doi.org/10.1186/s12917-016-0800-y
Mageiros L, Méric G, Bayliss SC et al (2021) Genome evolution and the emergence of pathogenicity in avian Escherichia coli. Nat Commun 12(1):765. https://doi.org/10.1038/s41467-021-20988-w
Maluta RP, Logue CM, Casas MRT, Meng T, Guastalli EAL, Rojas TCG, Montelli AC, Sadatsune T, de Carvalho Ramos M, Nolan LK, da Silveira WD (2014) Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS ONE 9:e105016. https://doi.org/10.1371/journal.pone.0105016
Mercat M, Clermont O, Massot M, Ruppe E, de Garine-Wichatitsky M, Miguel E, Valls Fox H, Cornelis D, Andremont A, Denamur E, Caron A (2016) Escherichia coli Population Structure and Antibiotic Resistance at a Buffalo/Cattle Interface in Southern Africa. Elkins CA, ed. Appl Environ Microbiol 82(5):1459–1467. https://doi.org/10.1128/AEM.03771-15
Paixão AC, Ferreira AC, Fontes M, Themudo P, Albuquerque T, Soares MC, Fevereiro M, Martins L, de Sá MIC (2016) Detection of virulence-associated genes in pathogenic and commensal avian Escherichia coli isolates. Poult Sci 95(7):1646–1652. https://doi.org/10.3382/ps/pew087
Petit F, Clermont O, Delannoy S, Servais P, Gourmelon M, Fach P, Oberlé K, Fournier M, Denamur E, Berthe T (2017) Change in the structure of Escherichia coli Population and the pattern of virulence genes along a rural aquatic continuum. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.00609
Picard B, Garcia JS, Gouriou S, Duriez P, Brahimi N, Bingen E, Elion J, Denamur E (1999) The Link between Phylogeny and Virulence in Escherichia coli Extraintestinal Infection. Moore RN, ed. Infect Immun 67(2):546–553. https://doi.org/10.1128/IAI.67.2.546-553.1999
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: antibiotic-resistant bacteria in pigeons. J Appl Microbiol. https://doi.org/10.1111/j.1365-2672.2010.04797.x
Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Nolan LK (2005) Characterizing the APEC pathotype. Vet Res 36(2):241–256. https://doi.org/10.1051/vetres:2004057
Runyen-Janecky LJ, Reeves SA, Gonzales EG, Payne SM (2003) Contribution of the Shigella flexneri Sit, Iuc, and Feo Iron Acquisition Systems to Iron Acquisition In Vitro and in Cultured Cells. Infect Immun 71(4):1919–1928. https://doi.org/10.1128/IAI.71.4.1919-1928.2003
Russo TA, Carlino UB, Johnson JR (2001) Identification of a New Iron-Regulated Virulence Gene, ireA, in an Extraintestinal Pathogenic Isolate of Escherichia coli. DiRita VJ, ed. Infect Immun 69(10):6209–6216. https://doi.org/10.1128/IAI.69.10.6209-6216.2001
Rybak B, Krawczyk B, Furmanek-Blaszk B, Wysocka M, Fordon M, Ziolkowski P, Meissner W, Stepniewska K, Sikorska K (2022) Antibiotic resistance, virulence, and phylogenetic analysis of Escherichia coli strains isolated from free-living birds in human habitats. Palusinska-Szysz M, ed. PLoS ONE 17(1):e0262236. https://doi.org/10.1371/journal.pone.0262236
Spurbeck RR, Dinh PC, Walk ST, Stapleton AE, Hooton TM, Nolan LK, Kim KS, Johnson JR, Mobley HL (2012) Escherichia coli Isolates That Carry vat, fyuA, chuA, and yfcV Efficiently Colonize the Urinary Tract. Bäumler AJ, ed. Infect Immun 80(12):4115–4122. https://doi.org/10.1128/IAI.00752-12
Starčič Erjavec M, Žgur-Bertok D (2015) Virulence potential for extraintestinal infections among commensal Escherichia coli isolated from healthy humans—the trojan horse within our gut. FEMS Microbiol Lett 362(5). https://doi.org/10.1093/femsle/fnu061
Stromberg ZR, Johnson JR, Fairbrother JM, Kilbourne J, Van Goor A, Curtiss R, Rd, Mellata M (2017) Evaluation of Escherichia coli isolates from healthy chickens to determine their potential risk to poultry and human health. DebRoy C, ed. PLoS ONE 12(7):e0180599. https://doi.org/10.1371/journal.pone.0180599
Subedi M, Luitel H, Devkota B, Bhattarai RK, Phuyal S, Panthi P, Shrestha A, Chaudhary DK (2018) Antibiotic resistance pattern and virulence genes content in avian pathogenic Escherichia coli (APEC) from broiler chickens in Chitwan, Nepal. BMC Vet Res 14(1):113. https://doi.org/10.1186/s12917-018-1442-z
Tenaillon O, Skurnik D, Picard B, Denamur E (2010) The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8(3):207–217. https://doi.org/10.1038/nrmicro2298
Vasconcelos RH, Teixeira RS, de Silva C, Lopes ING, de Maciel E (2018) WC Feral pigeons (Columba livia) as potential reservoirs of Salmonella sp and Escherichia coli. Arq Inst Biol 85(0). https://doi.org/10.1590/1808-1657000412017
Wang Y, Tang C, Yu X, Xia M, Yue H (2010) Distribution of serotypes and virulence-associated genes in pathogenic Escherichia coli isolated from ducks. Avian Pathol 39(4):297–302. https://doi.org/10.1080/03079457.2010.495742
EUCAST (European Committee of Antimicrobial Susceptibility Testing). Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 11.0, Valid from 1 January 2021. https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_11.0_Breakpoint_Tables.pdf
Acknowledgements
The authors wish to thank DVM František Zigo for collecting samples from pigeons.
Funding
This work was supported by the Slovak scientific agency VEGA grant (Vedecká grantová agentúra Ministerstva školstva, vedy, výskumu a športu Slovenskej republiky a Slovenskej akadémie vied) number 2/0010/21.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by [Tímea Kocúreková], [Lívia Karahutová] and [Dobroslava Bujňáková]. The first draft of the manuscript was written by [Tímea Kocúreková], [Dobroslava Bujňáková] and [Lívia Karahutová] and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
All procedures involving animals were in accordance with standard veterinary practices according Slovak legislation no. 377/2012.
Consent to participate and consent for publication
All authors agreed to participate in this work. They also approved the content of the research and the submission of the manuscript to the Veterinary Research Communication journal.
Conflict of interest
The authors declare no conflict of interest.
Disclosure statement
No competing financial interest exists.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bujňáková, D., Kocúreková, T. & Karahutová, L. Distribution of virulence-associated genes, antibiotic resistance and phylogenetic groups in Escherichia coli isolated from domestic and racing pigeons. Vet Res Commun 47, 1697–1705 (2023). https://doi.org/10.1007/s11259-023-10126-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-023-10126-w