Аntibiotic resistance of bacterial cultures isolated from the feral pigeon (Columba livia) and starling (Sturnus vulgaris) at a solid waste landfill

  • Y. Y. Dementieieva H. S. Skovoroda Kharkiv National Pedagogical University
  • N. Muzyka Institute of Experimental and Clinical Veterinary Medicine
  • D. Muzyka Institute of Experimental and Clinical Veterinary Medicine
  • A. B. Chaplygina H. S. Skovoroda Kharkiv National Pedagogical University
Keywords: synanthropic birds; birds as potential reservoirs of pathogens; zoochory; resistance to antibiotics; trophic connections


Resistance to antibiotics is well-known global phenomenon. There are places contributing to the development of antibiotic resistance such as waste landfills, especially ones that accept medical waste which did not undergo disinfection and livestock waste with bacteria not sensitive to antibiotics. An extensive system of transfer of antibiotic resistant microorganisms is formed on these territories (zoochory, groundwater, transport etc.). The aim of the research was to determine the species composition of bacteria isolated from birds of Derhachi municipal solid waste landfills in Kharkiv city, Ukraine. Also, we determine the sensitivity of bacterial isolates to a number of standard antibiotic drugs. We collected droppings of feral pigeons (Columba livia Gmelin, 1789; Columbidae) and starlings (Sturnus vulgaris Linnaeus, 1758; Sturnidae) during the winter period in 2020/2021; both species are dominants of waste landfills. We isolated 15 bacteria species of 4 families by bacteriological methods (growing on simple and selective media and identification by biochemical properties): Enterobacteriaceae (Enterobacter asburiae, E. dissolvens, E. cancerogenus, E. cloacae, E. sakazakii, Escherichia coli, Klebsiella terrigena, K. ornithinolytica, Citrobacter freundii, Proteus mirabilis), Yersiniaceae (Serratia ficaria, S. rubidaea, S. entomophila), Morganellaceae (Providencia stuartii) and Pseudomonadaceaе (Pseudomonas aeruginosa). Sensitivity was determined by the disk-diffusion method to 18 antibiotics. Ten isolates turned out to be multiresistant-resistant to three or more classes of antimicrobial drugs. A promising direction for future research is the determination of the pathogenicity of the isolates and checking the roles of birds of Derhachi solid waste landfills as reservoirs of pathogens. Currently, it can be assumed that large concentrations of synanthropic birds (especially those that forage on solid waste landfills) with a high probability are reservoirs of many bacteria, in particular those that have developed resistance to drugs.


Agga, G. E., Arthur, T. M., Durso, L. M., Harhay, D. M., & Schmidt, J. W. (2015). Antimicrobial-resistant bacterial populations and antimicrobial resistance genes obtained from environments impacted by livestock and municipal waste. PLoS One, 10(7), e0132586.

Ahlstrom, C. A., Bonnedahl, J., Woksepp, H., Hernandez, J., Olsen, B., & Ramey, A. M. (2018). Acquisition and dissemination of cephalosporin-resistant E. coli in migratory birds sampled at an Alaska landfill as inferred through genomic analysis. Scientific Reports, 8, 7361.

Blanco, G., & Bautista, L. M. (2020). Avian scavengers as bioindicators of antibiotic resistance due to livestock farming intensification. International Journal of Environmental Research and Public Health, 17(10), 3620.

Brezgunova, O. A. (2013). Night roosts of wintering starlings (Sturnus vulgaris) in Kharkiv city. Branta, 16, 120–126.

Carlson, J. C., Chandler, J. C., Bisha, B., LeJeune, J. T., & Wittum, T. E. (2020). Bird-livestock interactions associated with increased cattle fecal shedding of ciprofloxacin-resistant Escherichia coli within feedlots in the United States. Scientific Reports, 10, 10174.

Carlson, J. C., Hyatt, D. R., Bentler, K., Mangan, A. M., Russell, M., Piaggio, A. J., & Linz, G. M. (2015). Molecular characterization of Salmonella enterica isolates associated with starling–livestock interactions. Veterinary Microbiology, 179, 109–118.

Carroll, D., Wang, J., Fanning, S., & McMahon, B. J. (2015). Antimicrobial resistance in wildlife: Implications for public health. Zoonoses and Public Health, 62(7), 534–542.

Chandler, J. C., Anders, J. E., Blouin, N. A., Carlson, J. C., LeJeune, J. T., Goodridge, L. D., Wang, B., Day, L. A., Mangan, A. M., Reid, D. A., Coleman, S. M., Hopken, M. W., & Bisha, B. (2020). The role of European starlings (Sturnus vulgaris) in the dissemination of multidrug-resistant Escherichia coli among concentrated animal feeding operations. Scientific Reports, 10, 8093.

Clayton, D. H., & Price, R. D. (1999). Taxonomy of New World Columbicola (Phthiraptera: Philopteridae) from the Columbiformes (Aves), with descriptions of five new species. Annals of the Entomological Society of America, 92(5), 675–685.

Colles, F. M., McCarthy, N. D., Howe, J. C., Devereux, C. L., Gosler, A. G., & Maiden, M. C. J. (2009). Dynamics of Campylobacter colonization of a natural host, Sturnus vulgaris (European Starling). Environmental Microbiology, 11(1), 258–267.

Cunha, M. P. V., Oliveira, M. C. V., Oliveira, M. G. X., Menão, M. C., & Knöbl, T. (2019). CTX-M-producing Escherichia coli isolated from urban pigeons (Columba livia domestica) in Brazil. The Journal of Infection in Developing Countries, 13(11), 1052–1056.

de Oliveira, M. C. V., Camargo, B. Q., Cunha, M. P. V., Saidenberg, A. B., Teixeira, R. H. F., Matajira, C. E. C., Moreno, L. Z., Gomes, V. T. M., Christ, A. P. G., Barbosa, M. R. F., Sato, M. I. Z., Moreno, A. M., & Knöbl, T. (2018). Free-ranging synanthropic birds (Ardea alba and Columba livia domestica) as carriers of Salmonella spp. and diarrheagenic Escherichia coli in the vicinity of an urban zoo. Vector-Borne and Zoonotic Diseases, 18(1), 65–69.

Dementieieva, Y. Y. (2021). Ornithofauna of solid waste landfills of the Kharkov city. Visnyk Cherkaskogo Universytetu, 1, 26–36.

García, J., García-Galán, M. J., Day, J. W., Boopathy, R., White, J. R., Wallace, S., & Hunter, R. G. (2020). A review of emerging organic contaminants (EOCs), antibiotic resistant bacteria (ARB), and antibiotic resistance genes (ARGs) in the environment: Increasing removal with wetlands and reducing environmental impacts. Bioresource Technology, 307, 123228.

Gladkov, N. A., & Rustamov, A. K. (1965). The main problems of studying birds of the cultural landscape. In: Modern problems of ornithology. Frunze. Р. 111–156 (in Russian).

Gliebova, K. V. (2014). The role of the wild birds as natural sources of bacterial diseases. Scientific and Technical Bulletin оf State Scientific Research Control Institute of Veterinary Medical Products and Fodder Additives аnd Institute of Animal Biology, 15(2–3), 119–122.

Gostev, V. V., & Sidorenko, S. V. (2010). Bacterial biofilms and infections. Journal Infectology, 2(3), 4–15.

Guenther, S., Grobbel, M., Lübke-Becker, A., Goedecke, A., Friedrich, N. D., Wieler, L. H., & Ewers, C. (2010). Antimicrobial resistance profiles of Escherichia coli from common European wild bird species. Veterinary Microbiology, 144, 219–225.

Handrova, L., & Kmet, V. (2019). Antibiotic resistance and virulence factors of Escherichia coli from eagles and goshawks. Journal of Environmental Science and Health, Part B, 54(7), 605–614.

Hiltunen, T., Virta, M., & Laine, A.-L. (2017). Antibiotic resistance in the wild: An eco-evolutionary perspective. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 1712.

Höfle, U., Jose Gonzalez-Lopez, J. Camacho, M. C., Solà-Ginés, M., Moreno-Mingorance, A., Manuel Hernández, J., De La Puente, J., Pineda-Pampliega, J., Aguirre, J. I., Torres-Medina, F., Ramis, A., Majó, N., Blas, J., & Migura-Garcia, L. (2020). Foraging at solid urban waste disposal sites as risk factor for cephalosporin and colistin resistant Escherichia coli carriage in white storks (Ciconia ciconia). Frontiers in Microbiology, 11, 01397.

Hoult, J., Kryga, N., & Snyt, P. (1997). Determinant of Berghi bacteria. Mir, Moscow. Vol. 1.

Hussein, I., Abdel-Shafy, M., & Mansour, S. M. (2018). Solid waste issue: Sources, composition, disposal, recycling, and valorization. Egyptian Journal of Petroleum, 27(4), 1275–1290.

Jing, W., Ma, Z.-B., Zeng, Z.-L., Yang, X.-W., Huang, Y., & Liu, J.-H. (2017). The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zoological Research, 38(2), 55–80.

Kauffman, M. D., & LeJeune, J. (2011). European starlings (Sturnus vulgaris) challenged with Escherichia coli O157 can carry and transmit the human pathogen to cattle. Letters in Applied Microbiology, 53(6), 596–601.

Kwon, M. J., Yun, S.-T., Ham, B., Lee, J.-H., Oh, J.-S., & Jheong, W.-W. (2017). Impacts of leachates from livestock carcass burial and manure heap sites on groundwater geochemistry and microbial community structure. PLoS One, 12(8), 0182579.

Literak, I., Dolejska, M., Janoszowska, D., Hrusakova, J., Meissner, W., Rzyska, H., Bzoma, S., & Cizek, A. (2010). Antibiotic-resistant Escherichia coli bacteria, including strains with genes encoding the extended-spectrum beta-lactamase and QnrS, in waterbirds on the Baltic Sea coast of Poland. Applied and Environmental Microbiology, 76(24), 8126–8134.

Lyulin, Р., & Fedorova, O. (2016). Prevalence, seasonal and age-related dynamics of Pigeons’ ascaridosis in Kharkiv and its suburbs. Theoretical and Applied Veterinary Medicine, 4(2), 68–73.

Marcelino, V. R., Wille, M., Hurt, A. C., González-Acuña, D., Klaassen, M., Schlub, T. E., Eden, J.-S., Shi, M., Iredell, J. R., Sorrell, T. C., & Holmes, E. C. (2019). Meta-transcriptomics reveals a diverse antibiotic resistance gene pool in avian microbiomes. BMC Biology, 17, 31.

Martín-Maldonado, B., Vega, S., Mencía-Gutiérrez, A., Lorenzo-Rebenaque, L., de Frutos, C., González, F., Revuelta, L., & Marin, C. (2020). Urban birds: An important source of antimicrobial resistant Salmonella strains in Central Spain. Comparative Immunology, Microbiology and Infectious Diseases, 72, 101519.

Mikheev, A. O. (2018). Bird migrations and the spread of infectious diseases (literature review). World Science, 6(34), 6–13.

Muzyka, D. V. (2013). Wild birds as one of the main distribution factors of birds, animals and people pathogens. Veterinary Medicine, 97, 34–36.

Muzyka, D. V., & Stegniy, B. T. (2012). Wild birds as one of the main factors of distribution of agents of avian, animal and human infections. Veterinary Medicine, 96, 222–224.

Nuket, S., Bagcigil, A. F., Celik, B., Azaz, D., & Gungor, Y. (2019). The antibiotic resistance genes in Escherichia coli isolates from narman landfill (nl) area in Erzurum, Turkey. Fresenius Environmental Bulletin, 28(2), 803–808.

Panikar, I., Susol, R., & Kolomak, I. (2018). Morphological changes in colibacillosis of pigeons. Bulletin of SNAU, 42, 64–67.

Romanyshyna, J. R., & Skrypnyk, V. G. (2014). The discovery of Chlamydia avium in synanthropic pigeons in Ukraine. Veterynarna Virusologija ta Mikrobiologija, Problemy Biobezpeky ta Biozahystu, 99, 65–68.

Rusev, I. T., Zakusylo, V. N., & Vynnyk, V. D. (2011). Ecological and faunistic background of arboviruses circulation in north-west coast of Black Sea. Visnyk of Dnipropetrovsk University, Biology, Medicine, 2(2), 95–109.

Shriner, S. A., & Root, J. J. (2020). A review of avian influenza A virus associations in synanthropic birds. Viruses, 12(11), 1209.

Smith, O. M., Snyder, W. E., & Owen, J. P. (2020). Are we overestimating risk of enteric pathogen spillover from wild birds to humans? Biological Reviews, 95(3), 652–679.

Somov, N. N. (1897). Ornithological fauna of the Kharkov Province. Kharkov, A. Darre.

Soroka, N. I., & Sidorenko, I. V. (2013). Fauna of chewing lice of the order Phthiraptera, suborders Ischnocera and Amblycera, of the rock pigeon (Columba livia) in Ukraine. Vestnik Zoologii, 47(3), 211–217.

Stephens, R., Myers, G., Eppinger, M., & Bavoil, P. (2009). Divergence without difference: Phylogenetics and taxonomy of Chlamydia resolved. FEMS Immunology and Medical Microbiology, 55, 115–119.

Swirski, A. L., Pearl, D. L., Williams, M. L., Homan, H. J., Linz, G. M., Cernicchiaro, N., & LeJeune, J. T. (2013). Spatial epidemiology of Escherichia coli O157:H7 in dairy cattle in relation to night roosts of Sturnus vulgaris (European starling) in Ohio, USA (2007–2009). Zoonoses and Public Health, 61(6), 427–435.

Tang, X., Shen, M., Zhang, Y., Zhu, D., Wang, H., Zhao, Y., & Kang, Y. (2021). The changes in antibiotic resistance genes during 86 years of the soil ripening process without anthropogenic activities. Chemosphere, 266, 128985.

Torres, R. T., Carvalho, J., Cunha, M. V., Serrano, E., Palmeira, J. D., & Fonseca, C. (2020). Temporal and geographical research trends of antimicrobial resistance in wildlife – A bibliometric analysis. One Health, 11, 100198.

Vorobyov, A. A., & Bykov, A. S. (2003). Atlas of medical microbiology, virology and immunology. Medical Information Agency, 60, 236.

Yu, X., Sui, Q., Lyu, S., Zhao, W., Liu, J., Cai, Z., Yu, G., & Barcelo, D. (2020). Municipal solid waste landfills: An underestimated source of pharmaceutical and personal care products in the water environment. Environmental Science and Technology, 54(16), 9757–9768.

Zon, G. A., & Ivanovskaya, L. B. (2018). Current epizootic state on leptospirosis of cattle in Sumy Oblast. Veterinary Biotechnology, 32(2), 193–201.

How to Cite
Dementieieva, Y. Y., Muzyka, N., Muzyka, D., & Chaplygina, A. B. (2022). Аntibiotic resistance of bacterial cultures isolated from the feral pigeon (Columba livia) and starling (Sturnus vulgaris) at a solid waste landfill . Regulatory Mechanisms in Biosystems, 13(4), 443-448. https://doi.org/10.15421/022258