THE ROLE OF BIRDS IN THE TRANSMISSION OF LYME DISEASE

A literature review

Authors

  • Nadya Ivanova Aleksandrova NCIPD Author

DOI:

https://doi.org/10.58395/pipd.v48i3.44

Keywords:

birds, ticks, Borelia spp., reservoir competence

Abstract

During the vast distances in migration, sometimes through thousands of kilometers, the birds carry ticks very far away from their nesting sites. Up to this moment 136 species of hard ticks Ixodidae have been frequently found on birds. Larvae, nymphs and adults of 25 species of the genus Ixodes, parasitize on birds. By transporting of ticks infected with B. burgdorferi s.l., the birds introduce the infection indirectly to new geographical regions. Once imported, the spirochetes may adapt to the local ecological areas and reservoir hosts. Migratory birds which carry Borrelia spp. in their tissues or blood, are able to infect the ticks in the new area. This determines the reservoir competence of the birds and their participation in the ecology and the epidemiology of the Lyme disease. The selective transmission of Borrelia garinii from birds to ticks is detected; as well that migratory birds are able to carry Lyme disease as a latent infection for several months.

Downloads

Download data is not yet available.

References

Mannelli A, Bertolotti L, Gern L, Gray J. Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. FEMS Microbiol Rev. 2012; 36(4):837-861.

Schotthoefer AM, Frost HM. Ecology and epidemiology of Lyme Borreliosis. Clin Lab Med. 2015; 35(4):723-743.

Stanek G, Wormser GP, Gray J, Strle F. Lyme borreliosis. Lancet. 2012; 379 (9814):461-473.

Oliver JH, Jr. Biology and systematics of ticks (Acari:Ixodida). Annu. Rev. Eeol.Syst. 1989; 20(1):397-430.

Guglielmone AA, Nava S. Birds and hard ticks (Acari:Ixodidae), with discussions about hypotheses on tick evolution. Revista FAVE Secc. Cienc. Vet. Review article. 2017; 16(1):13-29.

Dvortsova IV, Moskvitina EA. The ecology of ticks of ixodes risinus species (literature review). Universum: Medicine and pharmacology: electronic scientific journal. 2013; 1(1):3-5. In Russian.

Arzamasov IT. Ixodid ticks, Pub’L BSSR Acad. Sci., Minsk, 1961. 48-49. In Russian.

Kaiser MN, Hoogstraal H. Ticks (Ixodoidea) on migrating birds in Cyprus, fall 1967 and spring 1968, and epidemiological considerations. Bulletin of Entomological Research. 1974; 64(1):97-110.

ZhiQing L, ZengJia L, JinXiu F, Ruo X, HongLin G, Feng Z, Too L, Guang Y. Investigation of Lyme disease natural epidemic focus in Shaanxi Province. Chinese Journal of Hygienic Insecticides and Equipments. 2010; 16(5):356-359.

Täilleklint L. Lyme borreliosis spirochetes in Ixodes ricinus and Haemaphysalis punctata ticks (Acari: Ixodidae) on three islands in the Baltic Sea. Exp Appl Acarol. 1996; 20(8):467-476.

Ulfstrand, S, Högstedt G. How many birds breed in Sweden? Anser 1976; 15:1–32. English summary.

Olsen B, Jaenson TG, Bergström S. Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Appl Environ Microbiol. 1995; 61(8):3082-3087.

Filippova, N.A., Ixodid Ticks of the Subfamily Ixodinae (Fauna of the USSR. Arachnida. Nauka, Leningrad, 1977;4(4):330. In Russian.

Korotkov Yu.S., Kislenko G.S. The demographic structure of the Taiga Tick (Ixodidae) population in dark valley forests of the Kemchug upland as of 1986–1991,” Parazitologiya 35(4), 265–274 (2001).

Korenberg EI. Comparative ecology and epidemiology of Lyme disease and tick-borne encephalitis in the former Soviet Union. Parasitology Today. 1994; 10 (4):157-160.

Estrada-Peña A, Jongejan F. Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol. 1999; 23:685-715.

Keirans JE, Hutcheson HJ, Durden LA, Klompen JS. Ixodes (Ixodes) scapularis (Acari: Ixodidae): redescription of all active stages, distribution hosts, geographical variation, and medical and veterinary importance. J. Med. Entomol. 1996; 33(3):297-318.

Anderson J F, Magnarelli LA. Avian and mammalian hosts for spirochete-infected ticks and insects in a Lyme disease focus in Connecticut. Yale J. Biol. Med. 1984; 57(4):627-641.

Battaly GR, Fish D, Dowler RC. The seasonal occurrence of Ixodes dammini and Ixodes dentatus (Acari: Ixodidae) on birds in a Lyme disease endemic area of southeastern New York state. J. N.Y. Entomol. Soc. 1987; 95(4):461-468.

Halsey SJ, Allan BF, Miller JR. The role of Ixodes scapularis, Borrelia burgdorferi and wildlife hosts in Lyme disease prevalence: A quantitative review. Ticks Tick-Borne Dis. 2018; 9(5):1103-1114.

Castro MB, Wright SA. Vertebrate hosts of Ixodes pacificus (Acari: Ixodidae) in California. J Vector Ecology. 2007; 32(1):140-149.

Humair PF, Turrian N, Aeschlimann A, Gern L. Borrelia burgdorferi in a focus of Lyme borreliosis: the epizootiologic contribution of small mammals. Folia Parasitol. 1993; 40(1):65-70.

Gern L, Siegenthaler M, Hu CM, Leuba-Garcia S, Humair PF, Moret J. Borrelia burgdorferi in rodents (Apodemus flavicollis and A. sylvaticus): Duration and enhancement of infectivity for Ixodes ricinus ticks. Eur. J Epidemiol. 1994; 10(1):75-80.

Anderson JF, Johnson RC, Magnarelli LA, Hyde FW. Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdorferi. Infection and immunity. 1986; 51(2):394-396.

Mclean RG, Ubico SR, Hughes CA, Engstrom SM, Jonson RC. Isolation and characterization of Borrelia burgdorferi from blood of a bird captured in the Saint Croix River Valley. J Clinical Microbiol. 1993; 31(8):2038-2043.

Weisbrod AR, Johnson RC. Lyme disease and migrating birds in the Saint Croix River Valley. Appl Environ Microbiol. 1989; 55(8):1921-1924.

Mather TN, Telford III SR, MacLachlan AB, Spielman A. Incompetence of catbirds as reservoirs for the Lyme disease spirochete (Borrelia burgdorferi). J. Parasitol. 1989; 75(1): 66-69.

Piesman J, Mather TN, Donahue JG, Levine F, Campbell JD, Karakahian S J, Spielman A. Comparative prevalence of Babesia microti and Borrelia burgdorferi in four populations of Ixodes dammini in eastern Massachusetts. Acta Tropica. 1986; 43(3): 263-270.

Comstedt P, Bergström S, Olsen B, Garpmo U, Marjavaara L, Mejlon H, Barbour AG, Bunikis J. Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerg Infect Dis. 2006; 12(7): 1087-1095.

Magnarelli LA, Anderson JF, Fish D. Transovarial transmission of Borrelia burgdorferi in Ixodes dammini (Acari:Ixodidae). J Infect Dis. 1987; 156(1):234-236.

Olsén B, Jaenson TG, Noppa L, Bunikis J, Bergström S. A Lyme borreliosis cycle in seabirds and Ixodes uriae ticks. Nature. 1993; 362(6418):340-342.

Olsen B, Duffy DC, Jaenson TG, Gylfe A, Bonnedahl J, Bergström S. Transhemispheric exchange of Lyme disease spirochetes by seabirds. J Clin Microbiol. 1995; 33(12): 3270-3274.

Gylfe A, Olsen B, Strasevicius D, Ras, NM, Weihe P, Noppa L, Ostberg Y, Baranton G, Bergsrrorru S. Isolation of Lyme disease Borrelia from puffins (Fratercula arctica) and seabird ticks (Ixodes uriae) on the Faeroe Islands. J Clin Microbiol. 1999; 37(4):890-896.

Gern L, Estrada-Pena A, Frandsen F, Gray JS, Jaenson TG, Jongejan F, Kahl O, Korenberg E, Mehl R, Nuttall PA. European reservoir hosts of Borrelia burgdorferi sensu lato. Zentbl. Bakteriolog. 1998; 287(3):196-204.

Richter D, Spielman A, Komar N, Matuschka FR. Competence of American robins as reservoir hosts for Lyme disease spirochetes. Emerg. Infect. Dis. 2000; 6(2): 659-662.

Nakao M, Miyamoto K, Fukunaga M. Lyme disease spirochetes in Japan: enzootic transmission cycles in birds, rodents, and Ixodes persulcatus ticks. J. Infect. Dis. 1994; 170(4): 878-882.

Ishiguro F, Takada N, Masuzawa T, Fukui T. Prevalence of Lyme Disease Borrelia spp. in ticks from migratory birds on the Japanese mainland. Appl Environ Microbiol. 2000; 66(3):982-986.

Kurtenbach K, Peacey M, Rijpkema SG, Hoodless AN, Nuttall PA, Randolph SE. Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl Environ Microbiol. 1998; 64(4):1169-1174.

Barbour AG. Isolation and cultivation of Lyme disease spirochetes. Yale. J. Biol. Med. 1984; 57(4):521-525.

Welty JC, Baptista L. The life of birds. Saunders college publishing, New York, USA. 1988; 581.

Hubálek Z, Halouzka J, Heroldová M. Growth temperature ranges of Borrelia burgdorferi sensu lato strains. J. Med. Microbiol. 1998; 47(10):929-932.

Heylen D, Matthysen E, Fonville M, Sprong H. Songbirds as general transmitters but selective amplifiers of Borrelia burgdorferi sensu lato genotypes in Ixodes ricinus ticks. Environ. Microbiol. 2014; 16(9):2859-2868.

Gryczyńska A, Welc-Falęciak R. Long-term study of the prevalence of Borrelia burgdorferi s.l. infection in ticks (Ixodes ricinus) feeding on blackbirds (Turdus merula) in NE Poland. Exp Appl Acarol. 2016; 70(3):381-394.

Franke J, Moldenhauer A, Hildebrandt A, Dorn W. Are birds reservoir hosts for Borrelia afzelii? Ticks Tick-Borne Dis. 2010; 1(2):109-112.

Estrada-Peña A, Osácar JJ, Pichon B, Gray JS. Hosts and pathogen detection for immature stages of Ixodes ricinus (Acari: Ixodidae) in North-Central Spain. Exp Appl Acarol. 2005; 37(3-4):257-268.

Poupon MA, Lommano E, Humair PF, Douet V, et al. Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl Environ Microbiol. 2006; 72(1):976-979.

Michelis S, Sewell HS, Collares-Pereira M, Santos-Reis M, Schouls LM, et.al. Genetic diversity of Borrelia burgdorferi sensu lato in ticks from mainland Portugal. J. Clin. Microbiol. 2000; 38(6):2128-2133.

Younsi H, Sarih MH, Jouda F, Godfroid E, Gern L, et.al. Characterization of Borrelia lusitaniae isolates collected in Tunisia and Morocco. J. Clin. Microbiol. 2005; 43(4):1587-1593.

Christova I. Studies on the etiological diagnosis and spread of tick-borne and other infections in Bulgaria. Dissertation abstract for DMSc. NCIPD, Sofia. 2012; 20. In Bulgarian.

Humair PF, Postic D, Wallich R, Gern L. An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralbl Bakteriol. 1998; 287(4):521-38.

Hanincová K, Taragelová V, Koci J, Schäfer SM, et.al. Association of Borrelia garinii and B. valaisiana with Songbirds in Slovakia. Appl Environ Microbiol. 2003; 69(5):2825-2830.

Geller J, Nazarova L, Katargina O, Leivits A, et.al. Tick-borne pathogens in ticks feeding on migratory passerines in Western part of Estonia. Vector Borne Zoonotic Dis. 2013; 13(10):1-6.

Dubska L, Literak I, Kocianova E, Taragelova V, Sychra O. Differential role of passerine birds in distribution of Borrelia spirochetes, based on data from ticks collected from birds during the postbreeding migration period in Central Europe. Appl Environ Microbiol. 2009; 75(3):596-602.

Gryczyńska A, Zgódka A, Płoski R, Siemia˛tkowski M. Borrelia burgdorferi sensu lato infection in passerine birds from the Mazurian Lake region (Northeastern Poland). Avian Pathology. 2004; 33(1):69-75.

Kipp S, Goedecke A, Dorn W, Wilske B, Fingerle V. Role of birds in Thuringia, Germany, in the natural cycle of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete. Int. J. Med. Microbiol. Suppl. 2006; 296 (S1):125-128.

Norte AC, Margos G, Becker NS, et.al. Host dispersal shapes the population structure of a tick-borne bacterial pathogen. Molecular Ecology. 2020; 29(3):485-501.

Kurtenbach K, Carey D, Hoodless AN, Nuttall PA, Randolph SE. Competence of pheasants as reservoirs for Lyme disease spirochetes. J. Med. Entomol. 1998; 35(1):77-81.

Ginsberg HS, Buckley PA, Balmforth MG, Zhioua E, et. al. Reservoir Competence of Native North American Birds for the Lyme Disease Spirochete, Borrelia burgdorferi. J. Med. Entomol. 2005; 42(3): 445-449.

Gylfe A, Bergström S, Lundström J, Olsen B. Reactivation of Borrelia infection in birds. Nature. 2000; 403 (6771):724-725.

Georgieva G. In regard to species composition of the ticks of family Ixodidae on birds and small mammals from the coastal strip of Burgas region. Bulletin DDD. 1977; 8(3-4):66-73. In Bulgarian.

Zlatanova-Levi V. Investigation of the ticks of family Ixodidae in an outbreak of Crimean hemorrhagic fever in Pazardzhik region. Dissertation Medical Academy-CIPD. Sofia.1974; 40-44. In Bulgarian.

Gladnishka T. Microbiological studies on vectors and reservoirs of some tick-borne bacterial infections in humans. Dissertation. NCIPD. Sofia 2008; 92-105. In Bulgarian

Wijngaard CC, Hofhuis A, Simões M, Rood E, et. al. Surveillance perspective on Lyme borreliosis across the European Union and European economic area. Euro Surveill. 2017; 22(27):30569.

Mysterud A, Heylen DJA, Matthysen E, Garcia AL, et.al. Lyme neuroborreliosis and bird populations in northern Europe. P Roy Soc B-Biol Sci. 2019; 286(1903):20190759.

Gunnar H, Gunnar AB, Midthjell L, Røed KH, Leinaas HP. Transport of Ixodes ricinus infected with Borrelia species to Norway by northward-migrating passerine birds. J Ticks and Tick-borne Diseases. 2011; 2(1):37-43.

Pedersen BN, Jenkins A, Kjelland V. Tick-borne pathogens in Ixodes ricinus ticks collected from migratory birds in southern Norway. PLoS ONE. 2020; 15(4):e0230579.

Downloads

Published

2020-12-17

Issue

Section

Articles

How to Cite

(1)
Ivanova Aleksandrova, N. THE ROLE OF BIRDS IN THE TRANSMISSION OF LYME DISEASE: A Literature Review. Probl Infect Parasit Dis 2020, 48 (3), 36-42. https://doi.org/10.58395/pipd.v48i3.44.

Most read articles by the same author(s)