Zoonotic Bridge: Unraveling the Role of Wild Birds in Spreading the Bacterial Pathogenic Diseases

• Muhammad Shoaib Ramzan

  Department of Zoology, Division of Science and Technology, University of Education, Lahore, Pakistan

  Author

• Muhammad Irshad Ahmad

  Business School, Zhengzhou University, Zhengzhou, 450001, China.

  Author

  https://orcid.org/0000-0002-1642-4815

• Talha Bilal

  Department of Zoology, Division of Science and Technology, University of Education, Lahore, Pakistan

  Author

• Nimra Zafar

  Department of Zoology, Division of Science and Technology, University of Education, Lahore, Pakistan

  Author

• Neelam

  Department of Zoology, Division of Science and Technology, University of Education, Lahore, Pakistan

  Author

• Muhammad Ahsan Ashraf

  Department of Zoology, Division of Science and Technology, University of Education, Lahore, Pakistan

  Author

While wild birds contribute significantly to our ecosystem, they also act as carriers for various zoonotic diseases affecting humans. These diseases are often transmitted through international and local migrations, direct contact, and water sources, as well as through droppings and the excretion of spores in their feces. Over time, they present significant risks to the health of humans and animals by serving as carriers and hosts for new strains of pathogens. This review emphasizes the significant zoonotic diseases caused by birds, which include bacterial infections. These pose substantial health risks to both humans and animals. The review delves into their epidemiology and clinical manifestations. Of utmost significance, it underscores the pivotal function of birds as both distributors and reservoirs of potentially significant zoonotic diseases.

Ainslie-Garcia, M. H., Farzan, A., Jafarikia, M., & Lillie, B. N. (2018). Single nucleotide variants in innate immune genes associated with Salmonella shedding and colonization in swine on commercial farms. Veterinary Microbiology, 219, 171–177. https://doi.org/10.1016/j.vetmic.2018.04.017

Antilles, N., García-Bocanegra, I., Alba-Casals, A., López-Soria, S., Pérez-Méndez, N., Saco, M., González-Solís, J., & Cerdà-Cuéllar, M. (2021). Occurrence and antimicrobial resistance of zoonotic enteropathogens in gulls from southern Europe. The Science of the Total Environment, 763, 143018. https://doi.org/10.1016/j.scitotenv.2020.143018

Becker, N. S., Margos, G., Blum, H., Krebs, S., Graf, A., Lane, R. S., Castillo-Ramírez, S., Sing, A., & Fingerle, V. (2016). Recurrent evolution of host and vector association in bacteria of the Borrelia burgdorferi sensu lato species complex. BMC Genomics, 17(1), 734. https://doi.org/10.1186/s12864-016-3016-4

Bradley, C. A., & Altizer, S. (2007). Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution, 22(2), 95–102. https://doi.org/10.1016/j.tree.2006.11.001

Brenner, F. W., Villar, R. G., Angulo, F. J., Tauxe, R., & Swaminathan, B. (2000). Salmonella nomenclature. Journal of Clinical Microbiology, 38(7), 2465–2467. https://doi.org/10.1128/JCM.38.7.2465-2467.2000

Broman, T., Palmgren, H., Bergström, S., Sellin, M., Waldenström, J., Danielsson-Tham, M. L., & Olsen, B. (2002). Campylobacter jejuni in black-headed gulls (Larus ridibundus): Prevalence, genotypes, and influence on C. jejuni epidemiology. Journal of Clinical Microbiology, 40(12), 4594–4602. https://doi.org/10.1128/JCM.40.12.4594-4602.2002

Chanamé Pinedo, L., Mughini-Gras, L., Franz, E., Hald, T., & Pires, S. M. (2022). Sources and trends of human salmonellosis in Europe, 2015-2019: An analysis of outbreak data. International Journal of Food Microbiology, 379, 109850. https://doi.org/10.1016/j.ijfoodmicro.2022.109850

Connolly, J. H., Alley, M. R., Dutton, G. J., & Rogers, L. E. (2006). Infectivity and persistence of an outbreak strain of Salmonella enterica serotype Typhimurium DT160 for house sparrows (Passer domesticus) in New Zealand. New Zealand Veterinary Journal, 54(6), 329–332. https://doi.org/10.1080/00480169.2006.36719

Costa, D., & Iraola, G. (2019). Pathogenomics of emerging Campylobacter species. Clinical Microbiology Reviews, 32(4), e00072-18. https://doi.org/10.1128/CMR.00072-18

Davis, R. S., Ramirez, R. A., Anderson, J. L., & Bernhardt, S. A. (2015). Distribution and habitat of Ixodes pacificus (Acari: Ixodidae) and prevalence of Borrelia burgdorferi in Utah. Journal of Medical Entomology, 52(6), 1361–1367. https://doi.org/10.1093/jme/tjv124

Dizon, C. Lysyk, T.J. Couloigner, I. & Cork, S.C. (2023) Ecology and epidemiology of lyme disease in Western North America. Zoonotic Diseases, 3, 20-37. https://doi.org/10.3390/zoonoticdis3010004

Dobbin, G., Hariharan, H., Daoust, P. Y., Hariharan, S., Heaney, S., Coles, M., Price, L., & Anne Muckle, C. (2005). Bacterial flora of free-living double-crested cormorant (Phalacrocorax auritus) chicks on Prince Edward Island, Canada, with reference to enteric bacteria and antibiotic resistance. Comparative Immunology, Microbiology and Infectious Diseases, 28(1), 71–82. https://doi.org/10.1016/j.cimid.2004.08.001

Epstein, J.H., McKee, J., Shaw, P., Hicks, V., Micalizzi, G., Daszak, P., Kilpatrick M.A., & Kaufman G. (2006). The Australian white ibis (Threskiornis molucca) as a reservoir of zoonotic and livestock pathogens. EcoHealth 3, 290–298. https://doi.org/10.1007/s10393-006-0064-2

Filippova, N.A. (1977) Ixodid ticks subfamily Ixodinae. (Fauna USSR). Arachnida, 4(4), 272–283, 316–330. [In Russian]

Foti, M., Daidone, A., Aleo, A., Pizzimenti, A., Giacopello, C., & Mammina, C. (2009). Salmonella bongori 48: Z35: - In migratory birds, Italy. Emerging Infectious Diseases, 15(3), 502–503. https://doi.org/10.3201/eid1503.080039

Gast, R.K. & Porter Jr., R.E. (2020) Salmonella Infections. In: Swayne, D.E., et al., Eds., Diseases of Poultry, John Wiley & Sons, Inc., Hoboken, 717-753. https://doi.org/10.1002/9781119371199.ch16

Grant, D., Todd, P.A., & Pennycott, T. (2007). Monitoring wild greenfinch (Carduelis chloris) for Salmonella enterica typhimurium. Ecological Research, 22(4): 571-574. https://doi.org/10.1007/s11284-006-0056-2

Haesendonck, R., Rasschaert, G., Martel, A., Verbrugghe, E., Heyndrickx, M., Haesebrouck, F., & Pasmans, F. (2016). Feral pigeons: A reservoir of zoonotic Salmonella enteritidis strains? Veterinary Microbiology, 195, 101–103. https://doi.org/10.1016/j.vetmic.2016.09.017

Hald, B., Skov, M. N., Nielsen, E. M., Rahbek, C., Madsen, J. J., Wainø, M., Chriél, M., Nordentoft, S., Baggesen, D. L., & Madsen, M. (2016). Campylobacter jejuni and Campylobacter coli in wild birds on Danish livestock farms. Acta Veterinaria Scandinavica, 58, 11. https://doi.org/10.1186/s13028-016-0192-9

Havelaar, A. H., Kirk, M. D., Torgerson, P. R., Gibb, H. J., Hald, T., Lake, R. J., Praet, N., Bellinger, D. C., de Silva, N. R., Gargouri, N., Speybroeck, N., Cawthorne, A., Mathers, C., Stein, C., Angulo, F. J., Devleesschauwer, B., & World Health Organization Food Borne Disease Burden Epidemiology Reference Group (2015). World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLoS Medicine, 12(12), e1001923. https://doi.org/10.1371/journal.pmed.1001923

Henderson, D. A., Courtney, B., Inglesby, T. V., Toner, E., & Nuzzo, J. B. (2009). Public health and medical responses to the 1957-58 influenza pandemic. Biosecurity and Bioterrorism: Biodefense Strategy, Practice, and Science, 7(3), 265–273. https://doi.org/10.1089/bsp.2009.0729

Hernández, J., Lindberg, P., Waldenström, J., Drobni, M., & Olsen, B. (2012). A novel Salmonella serovar isolated from Peregrine falcon (Falco peregrinus) nestlings in Sweden: Salmonella enterica enterica serovar Pajala (Salmonella pajala). Infection Ecology & Epidemiology, 2. https://doi.org/10.3402/iee.v2i0.7373

Hohmann E. L. (2001). Nontyphoidal salmonellosis. Clinical Infectious Diseases, 32(2), 263–269. https://doi.org/10.1086/318457

Houlihan, P. F. (2023). The birds of ancient Egypt (Vol. 15). Oxbow Books.

Humphrey, S., Chaloner, G., Kemmett, K., Davidson, N., Williams, N., Kipar, A., Humphrey, T., & Wigley, P. (2014). Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare. mBio, 5(4), e01364-14. https://doi.org/10.1128/mBio.01364-14

Jijón, S., Wetzel, A., & LeJeune, J. (2007). Salmonella enterica isolated from wildlife at two Ohio rehabilitation centers. Journal of Zoo and Wildlife Medicine,38(3), 409–413. https://doi.org/10.1638/1042-7260(2007)38[409:SEIFWA]2.0.CO;2

Jurado-Tarifa, E., Torralbo, A., Borge, C., Cerdà-Cuéllar, M., Ayats, T., Carbonero, A., & García-Bocanegra, I. (2016). Genetic diversity and antimicrobial resistance of Campylobacter and Salmonella strains isolated from decoys and raptors. Comparative Immunology, Microbiology and Infectious Diseases, 48, 14–21. https://doi.org/10.1016/j.cimid.2016.07.003

Kaakoush, N. O., Castaño-Rodríguez, N., Mitchell, H. M., & Man, S. M. (2015). Global epidemiology of campylobacter infection. Clinical Microbiology Reviews, 28(3), 687–720. https://doi.org/10.1128/CMR.00006-15

Kaiser, M. N., Hoogstraal, H., & Watson, G. E. (1974). Ticks (Ixodoidea) on migrating birds in Cyprus, fall 1967 and spring 1968, and epidemiological considerations. Bulletin of Entomological research, 64(1), 97-110.

Keirans, J. E., Hutcheson, H. J., Durden, L. A., & Klompen, J. S. (1996). Ixodes (Ixodes) scapularis (Acari:Ixodidae): redescription of all active stages, distribution, hosts, geographical variation, and medical and veterinary importance. Journal of Medical Entomology, 33(3), 297–318. https://doi.org/10.1093/jmedent/33.3.297

Keithlin, J., Sargeant, J., Thomas, M. K., & Fazil, A. (2014). Systematic review and meta-analysis of the proportion of Campylobacter cases that develop chronic sequelae. BMC Public Health, 14, 1203. https://doi.org/10.1186/1471-2458-14-1203

Kipp, S., Goedecke, A., Dorn, W., Wilske, B., & Fingerle, V. (2006). Role of birds in Thuringia, Germany, in the natural cycle of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete. International Journal of Medical Microbiology, 296(40), 125–128. https://doi.org/10.1016/j.ijmm.2006.01.001

Kirk, M. D., Fullerton, K. E., Hall, G. V., Gregory, J., Stafford, R., Veitch, M. G., & Becker, N. (2010). Surveillance for outbreaks of gastroenteritis in long-term care facilities, Australia, 2002-2008. Clinical Infectious, 51(8), 907–914. https://doi.org/10.1086/656406

Kirk, M. D., Pires, S. M., Black, R. E., Caipo, M., Crump, J. A., Devleesschauwer, B., Döpfer, D., Fazil, A., Fischer-Walker, C. L., Hald, T., Hall, A. J., Keddy, K. H., Lake, R. J., Lanata, C. F., Torgerson, P. R., Havelaar, A. H., & Angulo, F. J. (2015). World Health Organization estimates of the global and regional disease burden of 22 foodborne Bacterial, protozoal, and viral diseases, 2010: A data synthesis. PLoS Medicine, 12(12), e1001921. https://doi.org/10.1371/journal.pmed.1001921

Korotkov, I.uS., & Kislenko, G. S. (2001). Demographic structure of the population of taiga tick (Ixodidae) in coniferous forests of the Kemchug upland in 1986-1991. Parazitologiia, 35(4), 265–274.

Kumar, A., Sharma, D., & Kumar, R. (2018). Zoonoses at the human-avian interface: a review. BAOJ Veterinary Science, 2(1)005.

Man S. M. (2011). The clinical importance of emerging Campylobacter species. Nature Reviews. Gastroenterology & hepatology, 8(12), 669–685. https://doi.org/10.1038/nrgastro.2011.191

Mencía-Gutiérrez, A., Martín-Maldonado, B., Pastor-Tiburón, N., Moraleda, V., González, F., García-Peña, F. J., Pérez-Cobo, I., Revuelta, L., & Marín, M. (2021). Prevalence and antimicrobial resistance of Campylobacter from wild birds of prey in Spain. Comparative Immunology, Microbiology and Infectious Diseases, 79, 101712. https://doi.org/10.1016/j.cimid.2021.101712

Mohamed-Yousif, I.M. (2021) Wild birds as possible source of Campylobacter jejuni. Approaches in Poultry, Dairy and Veterinary Sciences, 8,791-793.

Newell, D. G., Elvers, K. T., Dopfer, D., Hansson, I., Jones, P., James, S., Gittins, J., Stern, N. J., Davies, R., Connerton, I., Pearson, D., Salvat, G., & Allen, V. M. (2011). Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Applied & Environmental Microbiology, 77(24), 8605–8614. https://doi.org/10.1128/AEM.01090-10

Norte, A. C., Margos, G., Becker, N. S., Albino Ramos, J., Núncio, M. S., Fingerle, V., Araújo, P. M., Adamík, P., Alivizatos, H., Barba, E., Barrientos, R., Cauchard, L., Csörgő, T., Diakou, A., Dingemanse, N. J., Doligez, B., Dubiec, A., Eeva, T., Flaisz, B., Grim, T., … Lopes de Carvalho, I. (2020). Host dispersal shapes the population structure of a tick-borne bacterial pathogen. Molecular Ecology, 29(3), 485–501. https://doi.org/10.1111/mec.15336

Olsen, A. L., Smith, V. J., Bergstrom, J. O., Colling, J. C., & Clark, A. L. (1997). Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence. Obstetrics and Gynecology, 89(4), 501–506. https://doi.org/10.1016/S0029-7844(97)00058-6

Phalen, D. N., Drew, M. L., Simpson, B., Roset, K., Dubose, K., & Mora, M. (2010). Salmonella enterica subsp. Enterica in cattle egret (Bubulcus ibis) chicks from central Texas: prevalence, serotypes, pathogenicity, and epizootic potential. Journal of Wildlife Diseases, 46(2), 379–389. https://doi.org/10.7589/0090-3558-46.2.379

Popa, G. L., & Papa, M. I. (2021). Salmonella spp. infection - A continuous threat worldwide. Germs, 11(1), 88–96. https://doi.org/10.18683/germs.2021.1244

Rosenberg, R., Lindsey, N. P., Fischer, M., Gregory, C. J., Hinckley, A. F., Mead, P. S., Paz-Bailey, G., Waterman, S. H., Drexler, N. A., Kersh, G. J., Hooks, H., Partridge, S. K., Visser, S. N., Beard, C. B., & Petersen, L. R. (2018). Vital Signs: Trends in Reported Vectorborne Disease Cases - United States and Territories, 2004-2016. Morbidity and Mortality Weekly Report, 67(17), 496–501. https://doi.org/10.15585/mmwr.mm6717e1

Ryan, M. P., O'Dwyer, J., & Adley, C. C. (2017). Evaluation of the complex nomenclature of the clinically and veterinary significant pathogen Salmonella. BioMed Research International, 2017, 3782182. https://doi.org/10.1155/2017/3782182

Sahin, O., Fitzgerald, C., Stroika, S., Zhao, S., Sippy, R. J., Kwan, P., Plummer, P. J., Han, J., Yaeger, M. J., & Zhang, Q. (2012). Molecular evidence for zoonotic transmission of an emergent, highly pathogenic Campylobacter jejuni clone in the United States. Journal of Clinical Microbiology, 50(3), 680–687. https://doi.org/10.1128/JCM.06167-11

Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., Jones, J. L., & Griffin, P. M. (2011). Foodborne illness acquired in the United States--major pathogens. Emerging Infectious Diseases, 17(1), 7–15. https://doi.org/10.3201/eid1701.p11101

Schwartz, A. M., Hinckley, A. F., Mead, P. S., Hook, S. A., & Kugeler, K. J. (2017). Surveillance for Lyme Disease - United States, 2008-2015. Morbidity and mortality weekly report. Surveillance summaries (Washington, D.C. : 2002), 66(22), 1–12. https://doi.org/10.15585/mmwr.ss6622a1

Scott, J., Durden, L., & Anderson, J. (2015) Infection prevalence of Borrelia burgdorferi in ticks Collected from songbirds in far-Western Canada. Open Journal of Animal Sciences 5, 232-241. https://doi.org/10.4236/ojas.2015.53027.

Shanker, S., Lee, A., & Sorrell, T. C. (1990). Horizontal transmission of Campylobacter jejuni amongst broiler chicks: experimental studies. Epidemiology and Infection, 104(1), 101–110. https://doi.org/10.1017/s0950268800054571

Shyaka, A., Kusumoto, A., Chaisowwong, W., Okouchi, Y., Fukumoto, S., Yoshimura, A., & Kawamoto, K. (2015). Virulence characterization of Campylobacter jejuni isolated from resident wild birds in Tokachi area, Japan. The Journal of Veterinary Medical Science, 77(8), 967–972. https://doi.org/10.1292/jvms.15-0090

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 of the Cambridge Philosophical Society, 95(3), 652–679. https://doi.org/10.1111/brv.12581

Tack, D. M., Ray, L., Griffin, P. M., Cieslak, P. R., Dunn, J., Rissman, T., Jervis, R., Lathrop, S., Muse, A., Duwell, M., Smith, K., Tobin-D'Angelo, M., Vugia, D. J., Zablotsky Kufel, J., Wolpert, B. J., Tauxe, R., & Payne, D. C. (2020). Preliminary incidence and trends of infections with pathogens transmitted commonly through food - foodborne diseases active surveillance network, 10 U.S. sites, 2016-2019. Morbidity And Mortality Weekly Report, 69(17), 509–514. https://doi.org/10.15585/mmwr.mm6917a1

Tawakol, M. M., Nabil, N. M., Samir, A., M, H. H., Yonis, A. E., Shahein, M. A., & Elsayed, M. M. (2023). The potential role of migratory birds in the transmission of pathogenic Campylobacter species to broiler chickens in broiler poultry farms and live bird markets. BMC Microbiology, 23(1), 66. https://doi.org/10.1186/s12866-023-02794-0

Thomas, V. G., Pain, D. J., Kanstrup, N., & Green, R. E. (2020). Setting maximum levels for lead in game meat in EC regulations: An adjunct to replacement of lead ammunition. Ambio, 49(12), 2026–2037. https://doi.org/10.1007/s13280-020-01336-6

Tresse, O., Alvarez-Ordóñez, A., & Connerton, I. F. (2017). Editorial: About the foodborne pathogen Campylobacter. Frontiers in Microbiology, 8, 1908. https://doi.org/10.3389/fmicb.2017.01908

van den Wijngaard, C. C., Hofhuis, A., Harms, M. G., Haagsma, J. A., Wong, A., de Wit, G. A., Havelaar, A. H., Lugnér, A. K., Suijkerbuijk, A. W., & van Pelt, W. (2015). The burden of Lyme borreliosis expressed in disability-adjusted life years. European Journal of Public Health, 25(6), 1071–1078. https://doi.org/10.1093/eurpub/ckv091

Vlahović, K., Matica, B., Bata, I., Pavlak, M., Pavičić, Ž., Popović, M., Nejedli, S., & Dovč, A. (2004). Campylobacter, Salmonella and Chlamydia in free-living birds of Croatia. European Journal of Wildlife Research, 50(3), 127-132.

Vogt, N. A., Stevens, C. P. G., Pearl, D. L., Taboada, E. N., & Jardine, C. M. (2020). Generalizability and comparability of prevalence estimates in the wild bird literature: Methodological and Epidemiological considerations. Animal Health Research Reviews, 21(1), 89–95. https://doi.org/10.1017/S1466252320000043

Wright, S. A., Lane, R. S., & Clover, J. R. (1998). Infestation of the southern alligator lizard (Squamata: Anguidae) by Ixodes pacificus (Acari: Ixodidae) and its susceptibility to Borrelia burgdorferi. Journal of Medical Entomology, 35(6), 1044–1049. https://doi.org/10.1093/jmedent/35.6.1044

Xiong, D., Song, L., Pan, Z., & Jiao, X. (2018). Identification and discrimination of Salmonella enterica Serovar Gallinarum Biovars Pullorum and Gallinarum Based on a One-Step Multiplex PCR Assay. Frontiers in Microbiology, 9, 1718. https://doi.org/10.3389/fmicb.2018.01718

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