Covid-19 Research

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Molecular Detection of Anaplasma phagocytophilum, Babesia odocoilei, Babesia species and Borrelia burgdorferi Sensu Lato in Songbirds

Biology Group    Start Submission

John D Scott*, Elena McGoey, Ana Morales and Risa R Pesapane

Volume3-Issue12
Dates: Received: 2022-11-25 | Accepted: 2022-12-01 | Published: 2022-12-05
Pages: 1451-1459

Abstract

The blacklegged tick, Ixodes scapularis, is known to carry various tick-borne zoonotic pathogens with the potential to cause debilitating human and animal diseases. Juvenile I. scapularis parasitize songbirds and, perhaps, these avifauna are competent hosts of common microbial pathogens. We extracted brachial venous blood from 18 ground-foraging passerine birds that were parasitized by I. scapularis larvae and nymphs. Using molecular identification, namely PCR, DNA sequencing, and Basic Local Alignment Search Tool (BLAST), we targeted Anaplasma phagocytophilum, Babesia spp. and Borrelia burgdorferi sensu lato. Overall, 15 (83%) of 18 passerine birds were positive for 3 microbial zoonotic pathogens that comprised of A. phagocytophilum (n = 8), Babesia odocoilei (n = 6), Babesia spp. 20-5A74 (n = 1), and B. burgdorferi sensu lato (n = 9). The pathogen load consisted of 8 singles, 5 doubles, and 2 triples. One novel Babesia sp. (Babesia spp. 20-5A74) was found, and the remaining Babesia infections were B. odocoilei. Our findings reveal that ground-foraging, passerine birds are avian hosts of zoonotic pathogens. We provide the first-ever documentation that songbirds are hosts of B. odocoilei. Based on our data, B. odocoilei outnumbered other Babesia spp., and elucidated the authentic fact that B. odocoilei is the predominant Babesia sp. in North America. As avian hosts, passerine birds play a significant role in the enzootic transmission cycle of B. burgdorferi sensu lato, A. phagocytophilum, and Babesia species.

FullText HTML FullText PDF DOI: 10.37871/jbres1619


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Copyright

© 2022 Scott JD, et al. Distributed under Creative Commons CC-BY 4.0

How to cite this article

Scott JD, McGoey E, Morales A, Pesapane RR. Molecular Detection of Anaplasma phagocytophilum, Babesia odocoilei, Babesia species and Borrelia burgdorferi Sensu Lato in Songbirds. 2022 Dec 05; 3(12): 1451-1459. doi: 10.37871/jbresjbres1619, Article ID: JBRES1619, Available at: https://www.jelsciences.com/articles/jbres1619.pdf


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References


  1. Nicholson WA, Sonenshine DE, Noden BH. Ticks (Ixodida). In Medical and Veterinary Entomology, 3rd ed. In: Mullen GR, Durden LA, Editors. London, UK: Academic Press/Elsevier: London, UK; 2019. p. 603–672. ISBN 978-0-12-814043-7.
  2. Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP: Lyme disease―a tick-borne spirochetosis? Science. 1982;216:1317−1319.
  3. Wilske B, Preac-Mursic V, Göbel UB, Graf B, Jauris S, Soutschek E, Schwab E, Zumstain G. An OspA serotyping system for Borrelia burgdorferi based on reactivity of monoclonal antibodies and OspA sequence analysis. J Clin Microbiol. 1993;31:340−350.
  4. Jobe DA, Lovrich SD, Oldenburg, DG, Kowalski TJ, Callister SM. Borrelia miyamotoi infection in patients from upper midwestern United States, 2014-2015. Emerg Infect Dis. 2016;22:1471−1473.
  5. Wagemakers A, Oei A, Fikrig MM, Miellet WR, Hovius JW. The relapsing fever spirochete Borrelia miyamotoi is cultivable in a modified Kelly-Petterkofer medium, and is resistant to human complement. Parasit Vectors. 2014;7:418.
  6. Narurkar R, Mamonska-Dyga A, Nelson JC, Liu D. Autoimmune hemolytic anemic associated with babesiosis. Biomark Res. 2017;5:14.
  7. Scott JD, Sajid MS, Pascoe EL, Foley JE. Detection of Babesia odocoilei in humans with babesiosis symptoms. Diagnostics. 2021;11:947.
  8. Michaud, S. Lyme, Anaplasma phagocytophilum, Bartonella henselae and possible Babesia odocoilei acute infections among 101 patients in a small community hospital in Quebec in 2021: A retrospective chart review. Proceedings of International Lyme and Associated Diseases Society, Orlando, Florida, USA, 2022.
  9. Dumler JS, Choi KS, Garcia-Garcia JC, Barat NS, Scorpio DG, Garyu JW, Grab DJ, Bakken JS. Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg Infect Dis. 2005;11:1828−1834.
  10. Kandhi S, Ghazanfar H, Qureshi ZA, Kalangi H, Jyala A, Perez, ESA. An atypical presentation of a severe case of Anaplasma phagocytophilum. Cureus. 2022;14: e23224.
  11. Pritt BS, Allerdice MEJ, Sloan LM, Paddock CD, Munderdoh UG, Rikihisa Y, Tajima T, Paskewitz SM, Neitzel DF, Johnson DKH, et al. Proposal to reclassify Ehrlichia muris as Ehrlichia muris subsp. muris subsp. nov. and description of Ehrlichia muris subsp. eauclairensis subsp. nov., a newly recognized tick-borne pathogen of humans. Int J Syst Evol Microbiol. 2017;67: 2121−2126.
  12. Campagnolo ER, Tewari D, Farone TS, Livengood JL, Mason KL: Evidence of Powassan/deer tick virus in adult blacklegged ticks (Ixodes scapularis) recovered for hunter-harvested white-tailed deer (Odocoileus virginianus) in Pennsylvania: A public health perspective. Zoonoses Public Health. 2018;65:e589−594.
  13. Knox KK, Thomm AM, Harrington YA, Ketter E, Patitucci JM, Carrigan DR. Powassan/deer tick virus and Borrelia burgdorferi infection in Wisconsin tick populations. Vector Borne Zoonotic Dis. 2017;17:463−466.
  14. Anderson JF, Armstrong PM. Prevalence and genetic characterization of Powassan virus strains infecting Ixodes scapularis in Connecticut. An J Trop Med Hyg. 2012;87:754−759.
  15. Scott JD, Pesapane RR. Detection of Anaplasma phagocytophilum, Babesia odocoilei, Babesia sp., Borrelia burgdorferi sensu lato, and Hepatozoon canis in Ixodes scapularis ticks collected in eastern Canada. Pathogens. 2021;10:1265.
  16. Anderson JF, Magnarelli LA. Avian and mammalian hosts for spirochete-infected ticks and insects in a Lyme disease focus in Connecticut. Yale J Biol Med. 1984;57:627641.
  17. Anderson JF, Johnson RC, Magnarelli LA, Hyde FW. Involvement of birds in the epidemiology of Lyme disease agent Borrelia burgdorferi. Infect Immun. 1986;51:394-396.
  18. Anderson JF, Magnarelli LA: Enzootiology of Borrelia burgdorferi in the northeastern and northcentral United States. In: Biology of Ixodes ricinus Complex Ticks and Lyme Disease. Acarology IX Symposia;Ohio Biological Survey: Columbus, OH, USA, 1999;2:385−389.
  19. Scott JD, Clark KL, Foley JE, Anderson JF, Bierman BC, Durden LA. Extensive distribution of the Lyme disease bacterium, Borrelia burgdorferi sensu lato, in multiple tick species parasitizing avian and mammalian hosts across Canada. Healthcare. 2018;6:131.
  20. Scott JD. First report of Ixodes scapularis ticks parasitizing a North American porcupine in Canada. Parasitologia. 2021;1:45−49.
  21. Scott JD, Clark KL, Durden LA. Presence of Babesia odocoilei and Borrelia burgdorferi sensu lato in a tick and dual parasitism of Amblyomma inornatum and Ixodes scapularis on a bird in Canada. Healthcare. 2019;7:46.
  22. Stricker RB. Lyme disease: a potential polymicrobial infection. ASM News. 2003;69:265.
  23. Sanchez-Vicente S, Tagliafierro T, Coleman JL, Benach JL, Tokarz R. Polymicrobial nature of tick-borne diseases. mBio. 2019;10:e02055-19.
  24. McLean RG, Ubico SR, Hughes CAN, Engstrom SM, Johnson RC. Isolation and characterization of Borrelia burgdorferi from blood of a bird captured in the Saint Croix River Valley. J Clin Microbiol. 1993;31:2038−2043.
  25. Scott JD, Lee MK, Fernando K, Durden LA, Jorgensen DR, Mak S, Morshed MG. Detection of Lyme disease spirochete, Borrelia burgdorferi sensu lato including three novel genotypes in ticks (Acari: Ixodidae) collected from songbirds (Passeriformes) across Canada. J Vect Ecol. 2010;35:124−139.
  26. Scott, JD, Anderson JF, Durden LA. Widespread dispersal of Borrelia burgdorferi-infected ticks collected from songbirds across Canada. J Parasitol. 2012;98:49−59.
  27. Richter D, Spielman A, Komar N, Matuschka FR. Competence of American Robins as reservoir hosts for Lyme disease spirochetes. Emerg Infect Dis. 2000;6:133−138.
  28. Dingler RJ, Wright, SA, Donohue AM, Macedo PA, Foley JE. Surveillance for Ixodes pacificus and the tick-borne pathogens Anaplasma phagocytophilum and Borrelia burgdorferi in birds from California’s inner coast range. Ticks Tick Borne Dis. 2014;5:436−445.
  29. Jia N, Zheng YC, Jiang JF, Jiang RR, Jiang BG, Wei R, Liu HB, Huo QB, Sun Y, Chu YL, et al. Human babesiosis caused by a Babesia crassa-like pathogen: A case series. Clin Infect Dis. 2018;67:1110−1119.
  30. Zintl A, Mulcahy G, Skerrett, HE, Taylor SM, Gray JS. Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin Microbiol Rev. 2003;16:622−636.
  31. Herwaldt BL, Persing DH, Precigout EA, Goff WL, Mathiesen DA, Taylor PW, Eberhard ML, Gorenflot AF. A fatal case of babesiosis in Missouri: Identification of another piroplasm that infects humans. Ann Intern Med. 1996;124:643−650.
  32. Conrad PA, Kjemtrup AM, Carreno RA, Thomford J, Wainwright K, Eberhard M, Quick R, Telford SR III, Herwaldt BL. Description of Babesia duncani n. sp. (Apicomplexa: Babesiidae) from humans and its differentiation from other piroplasms. Int J Parasitol. 2006;36:779−789.
  33. Gray JS, Weiss LM: Babesia microti. In Emerging Protozoan Pathogens; Chan N, editor. Abingdon, UK: Taylor and Francis, 2008. p. 303−349.
  34. Kim JY, Cho SH, Joo HN, Tsuji M, Cho SR, Park IJ, Chung GT, Ju JW, Cheun HI, Lee, HW, et al. First case of human babesiosis in Korea: Detection and characterization of a novel type of Babesia sp. (K01) similar to ovine Babesia. J Clin Microbiol. 2007;45:2084−2087.
  35. Man SQ, Qiao K, Cui J, Feng M, Fu YF, Cheng XJ. A case of human infection with a novel Babesia species in China. Infect Dis Poverty. 2016;5:28.
  36. Shih CM, Liu LP, Chung WC, Ong SJ, Wang CC. Human babesiosis in Taiwan: Asymptomatic infection with a Babesia microti-like organism in a Taiwanese woman. J Clin Microbiol. 1997;35:450−454.
  37. Kjemtrup AM, Conrad PA. Human babesiosis: An emerging tick-borne disease. Int J Parasitol. 2000;30:1323−1337.
  38. Herwaldt BL, Cacciò S, Gherlinzoni F, Aspöck H, Slemenda SB, Piccaluga P, Martinelli G, Edelhofer R, Hollenstein U, Poletti G, et al. Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerg Infect Dis. 2003;9:943−948.
  39. Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA. Babesia: A world emerging. Infect Genet Evol. 2012;8:1788−1809.
  40. Gray A, Capewell P, Zadoks R, Taggart MA, French AS, Katzer F, Shiels BR, Weir W. Wild deer in the United Kingdom are a potential reservoir for the livestock parasite Babesia divergens. Cur Res Parasitol Vector Borne Dis. 2021;1:100019.
  41. Armstrong PMP, Katavolos P, Caporale DA, Smith RP. Spielman A, Telford SR III. Diversity of Babesia infecting deer ticks (Ixodes dammini). Am J Trop Med Hyg. 1998;58:739−742.
  42. Steiner FE, Pinger RR, Vann CN, Abley MJ, Sullivan B, Grindle N, Clay K, Fuqua C: Detection of Anaplasma phagocytophilum and Babesia odocoilei DNA in Ixodes scapularis (Acari: Ixodidae) collected in Indiana. J Med Entomol. 2006;43:437−442.
  43. Steiner FE, Pinger RR, Vann CN, Grindle N, Civitello D, Clay K, Fuqua C. Infection and co-infection rates of Anaplasma phagocytophilum variants, Babesia spp., Borrelia burgdorferi, and the rickettsial endosymbiont in Ixodes scapularis (Acari: Ixodidae) from sites in Indiana, Maine, Pennsylvania and Wisconsin. J Med Entomol. 2008;45:289−297.
  44. Hamer SA, Roy PL, Hickling GJ, Walker ED, Foster ES, Barber CC, Tsao JI. Zoonotic pathogens in Ixodes scapularis, Michigan. Emerg Infect Dis. 2007;13:1131−1133.
  45. Schoelkopf L, Hutchinson CE, Bendele KG, Goff WL, Willette M, Rasmussen JM, Holman PJ. New ruminant hosts and wider geographic range identified for Babesia odocoilei (Emerson and Wright 1970). J Wildl Dis. 2005;41:683−690.
  46. Holman PJ, Madeley J, Craig TM, Allsopp BA, Allsopp MT, Petrini KR, Waghela SD, Wagner GG. Antigenic, phenotypic and molecular characterization confirms Babesia odocoilei isolated from three cervids. J Wildl Dis. 2000;36:518−530.
  47. Waldrup KA, Kocan AA, Qureshi T, Davis DS, Baggett D, Wagner GG. Serological prevalence and isolation of Babesia odocoilei among white-tailed deer (Odocoileus virginianus) in Texas and Oklahoma. J Wildl Dis. 1989;25:194−201.
  48. Shock BC, Moncayo A, Cohen S, Mitchell EA, Williamson PC, Lopez G, Garrison LE, Yabsley MJ. Diversity of piroplasms detected in blood-fed and questing ticks from several states in the United States. Ticks Tick Borne Dis. 2014;5:373−380.
  49. Livengood J, Hutchinson ML, Thirumalapura N, Tewari D. Detection of Babesia, Borrelia, Anaplasma, and Rickettsia spp. in adult black-legged ticks (Ixodes scapularis) from Pennsylvania, United States, with a Luminex multiplex bead assay. Vector Borne Zoonotic Dis. 2020;20:406−411.
  50. Emerson HR and Wright WT: The isolation of a Babesia in white-tailed deer. Bull Wild Dis Assoc. 1968;4:142−143.
  51. Emerson HR, Wright WT: Correction. J Wildl Dis. 1970;6:519.
  52. Perry BD, Nichols DK, Cullom ES. Babesia odocoilei Emerson and Wright, 1970 in white-tailed deer, Odocoileus virginianus (Zimmermann), in Virginia. J Wildl Dis. 1985;21:149−152.
  53. Eshoo MW, Carolan HE, Massire C, Chou DM, Crowder CD, Rounds MA, Phillipson CA, Schutzer SE, Ecker DJ. Survey of Ixodes pacificus ticks in California reveals a diversity of microorganisms and a novel and widespread Anaplasmataceae species. PLoS ONE. 2015;10:e0135828.
  54. Pattullo KM, Wobeser G, Lockerbie BP, Burgess HJ. Babesia odocoilei infection in a Saskatchewan elk (Cervus elaphus canadensis) herd. J Veter Diagn Invest. 2013;25:535−540.
  55. Scott JD, McGoey E, Pesapane RR. Tick-Borne pathogens Anaplasma phagocytophilum, Babesia odocoilei, and Borrelia burgdorferi sensu lato in blacklegged ticks widespread across eastern Canada. J Biomed Res Environ Sci. 2022;3:1249−1256.
  56. Scott JD, Clark KL, Coble NM, Ballantyne, TR. Detection and transstadial passage of Babesia species and Borrelia burgdorferi sensu lato in ticks collected from avian and mammalian hosts in Canada. Healhcare. 2019;7:155.
  57. Scott JD, Pascoe EL, Sajid MS, Foley JE. Detection of Babesia odocoilei in Ixodes scapularis ticks collected from songbirds in Ontario and Quebec, Canada. Pathogens. 2020;9:781.
  58. Scott JD, Pascoe E, Sajid MS, Foley J. Monitoring of nesting songbirds detects established population of blacklegged ticks and associated Lyme disease endemic area in Canada. Healthcare. 2020;8:59.
  59. Scott JD, Pascoe EL, Sajid MS, Foley JE. Detection of Babesia odocoilei in Ixodes scapularis ticks collected in southern Ontario, Canada. Pathogens. 2021;10:327.
  60. Seutin G, White BN, Boag PT: Preservation of avian blood and tissue samples for DNA analysis. Can J Zool. 1991;69:82-90.
  61. Barbour AG, Bunikis J, Travinsky B, Hoen AG, Diuk-Wasser MA, Fish D, Tsao JI. Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species. Am J Trop Med Hyg. 2009;81:1120-1131.
  62. Drazenovich N, Foley J, Brown RN. Use of real-time quantitative PCR targeting the msp2 protein gene to identify cryptic Anaplasma phagocytophilum infections in wildlife and domestic animals. Vector Borne Zoonotic Dis. 2006;6:83-90.
  63. Jalovecka M, Sojka D, Ascencio M, Schnittger L. Babesia life cycle―when phylogeny meets biology. Trends Parasitol. 2019;35:356-368.
  64. Burgess EC: Experimental inoculation of mallard ducks (Anas platyrhynchos platyrhynchos) with Borrelia burgdorferi. J Wildl Dis. 1989;25:99-102.
  65. Haninová K, Taragelová V, Koci J, Schäfer SM, Hails R, Ullmann AJ, Piesman J, Lubuda M, Kurtenbach K. Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Appl Environ Microbiol. 2003;69:2825-2830.
  66. Kitsou C, Foor SD, Dutta S, Bista S, Pa U. Tick gut barriers impacting tick-microbe interactions and pathogen persistence. Mol Microbiol. 2021;116:1241-1248.
  67. Bonnet SI, Pollet T. Update on the intricate tango between tick microbiomes and tick-borne pathogens. Parasite Immunol. 2021;43:e12813.
  68. Aivelo T, Norberg A, Tschirren B. Bacterial microbiota composition of Ixodes ricinus ticks: The role of environmental variation, tick characteristics and microbial interactions. PeerJ. 2019;7:e8217.
  69. Durand J, Herrmann C, Genné D, Sarr A, Gern L, Voordouw MJ: Multistrain infections with Lyme borreliosis pathogens in the tick vector. Appl Environ Microbiol. 2017;83:e02552-16.
  70. Swanson KI, Norris DE. Co-circulation of microorganisms in questing Ixodes scapularis nymphs in Maryland. J Vector Ecol. 2007;32:243-251.
  71. Waldrup KA, Kocan AA, Barker RW, Wagner GG. Transmission of Babesia odocoilei in white-tailed deer (Odocoileus virginianus) by Ixodes scapularis (Acari: Ixodidae). J Wildl Dis. 1990;26:390-391.
  72. O’Connor RM, Long JA, Allred DR. Cytoadherence of Babesia bovis-infected erythrocytes to bovine brain capillary endothelial cells provides an in vitro model for sequestration. Infect Immun. 1999;67:3921-3928.
  73. Schetters TP, Kleuskens J, Scholtes N, Gorenflot A. Parasite localization and dissemination in the Babesia-infected host. Ann Trop Med Parasitol. 1998;92:513-519.
  74. Allred DR, Al-Khedery B. Antigenic variation and cytoadhesion in Babesia bovis and Plasmodium falciparum: Different logics achieve the same goal. Mol Biochem Parasitol. 2004;134:27-35.
  75. Selig T, IIyas S, Theroux C, Lee J. Fatal babesiosis in an immunocompetent patient. R I Med J. 2022;105:20-23.
  76. Schetters T: Mechanisms involved in the persistence of Babesia canis infection in dogs. Pathogens. 2019;8:94.
  77. Bosman AM, Oosthuizen MC, Venter EH, Steyl JC, Gous TA, Penzhorn BL. Babesia lengau associated with cerebral and haemolytic babesiosis in two domestic cats. Parasit Vectors. 2013;6:128.
  78. Mosqueda J, Olvera-Ramirez A, Aguilar-Tipacamu G, Canto GJ. Current advances in detection and treatment of babesiosis. Curr Med Chem. 2012;19:1504-1518.
  79. Pirahanchi Y, Jessu, R, Aeddula NR. Physiology, sodium potassium pump. StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. 2022 Jan-. NCBI Bookshelf. National Library of Medicine, National Institutes of Health.
  80. Schwarz S, Mohr A, Knauth M, Wildemann B, Storch-Hagenlocher B. Acute disseminated encephalomyelitis: A follow-up study of 40 adult patients. Neurology. 2001;56:1313.
  81. Fox LM, Wingerter S, Ahmed A, Chou J, Phein L, Levy O. Neonatal babesiosis: case report and review of the literature. Pediatr Infect Dis J. 2006;25:169-73.
  82. Iyer S, Goodman K. Congenital babesiosis from maternal exposure: A case report. J Emerg Med. 2019;56:e39−e41.
  83. Walker S, Coray E, Ginsberg-Peltz J, Smith L. A five-week-old twin with profound anemia: A case report of asymmetric congenital babesiosis. Cureus. 2022;14;e22774.


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