First Detection of Lyme Disease Spirochete Borrelia burgdorferi in Ticks Collected from a Raptor in Canada
DOI:
https://doi.org/10.53607/wrb.v32.26Keywords:
Falconiformes, raptors, Cooper’s hawk, Accipiter cooperii, Canada, Lyme disease, Borrelia burgdorferi, ticks, Ixodes auritulusAbstract
During a pan‒Canadian tick‒host study, the authors detected the spirochetal bacterium Borrelia burgdorferi sensu lato, which causes Lyme disease, in ticks from a raptor. Lyme disease is one of a number of zoonotic, tick‒borne diseases causing morbidity and mortality worldwide. Larvae of the avian coastal tick, Ixodes auritulus, were collected by wildlife rehabilitators from a Cooper’s hawk, Accipter cooperii, on Vancouver Island, British Columbia. Using PCR [polymerase chain reaction] amplification of the linear plasmid ospA gene of B. burgdorferi, 4 (18%) of 22 larvae were positive. Since these engorged I. auritulus larvae had not had a previous blood meal and B. burgdorferi is rarely transmitted from infected female ticks to their progeny, authors propose that Cooper’s hawks are reservoir‒ competent hosts of B. burgdorferi. Authors’ tick‒host discovery provides the first report of bird‒feeding ticks on a Cooper’s hawk, and exhibits the premier record of B. burgdorferi‒positive ticks on a raptor. Not only are passerine (perching) and gallinaceous (chicken‒like) birds included in the wide dispersal of Lyme disease vector ticks, raptors also now are implicated in the dissemination of B. burgdorferi‒infected ticks. Although I. auritulus does not bite humans, this tick species plays an integral role in the four‒tick enzootic cycle of B. burgdorferi along the West Coast of America. In essence, raptors and I. auritulus ticks may help to amplify this infectious agent in nature, and increase the likelihood of people contracting Lyme Disease, especially in coastal areas.
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References
Anderson, J. F., and L. A. Magnarelli. 1984. Avian and Mammalian Hosts for Spirochete‒infected Ticks and Insects in a Lyme Disease Focus in Connecticut. Yale Journal of Biology and Medicine. 57: 627‒641.
Anderson, J. F., and L. A. Magnarelli. 1993. Epizootiology of Lyme Disease‒causing Borreliae. Clinics in Dermatology. 11: 339‒351.
Anderson, J. F., R. C. Johnson, L. A. Magnarelli, and F. W. Hyde. 1986. Involvement of Birds in the Epidemiology of the Lyme Disease Agent Borrelia burgdorferi. Infection and Immunity. 51(2): 394‒396.
Banerjee, S. N., M. Banerjee, J. A. Smith, and K. Fernando. 1994. Lyme Disease in British Columbia—An Update. Proceedings of the VII Annual Lyme Disease Foundation International Conference.
Barthold, S. W., E. Hodzic, D. M. Imai, S. Feng, X. Yang, et al. 2010. Ineffectiveness of Tigecycline Against Persistent Borrelia burgdorferi. Antimicrobial Agents and Chemotherapy. 54: 643‒651.
Bransfield, R. C., J. S. Wulfman, W. T. Harvey, and A. I. Usman. 2008. The Association Between Tick‒borne Infections, Lyme Borreliosis and Autism Spectrum Disorders. Medical Hypotheses. 70: 967‒974.
Burgdorfer, W., A. G. Barbour, S. F. Hayes, J. L. Benach, E. Grunwaldt, et al. 1982. Lyme Disease a Tick‒borne Spirochetosis? Science. 216: 1317‒1319.
Burgess, E. C. 1989. Experimental Inoculation of Mallard Ducks (Anas platyrhynchos platyrhynchos) with Borrelia burgdorferi. Journal of Wildlife Diseases. 25: 99‒102.
Casjens, S. R., C. M. Fraser‒Liggett, E. F. Mongodin, W. G. Qiu, J. J. Dunn, et al. 2011. Whole Genome Sequence of an Unusual Borrelia burgdorferi Sensu Lato Isolate. Journal of Bacteriology. 193: 1489‒1490.
Clark, K. L., B. Leydet, and S. Hartman. 2013. Lyme Borreliosis in Human Patients in Florida and Georgia, USA. International Journal of Medical Sciences. 10: 915‒931.
Crowder, C. D., H. E. Matthews, S. Schutzer, M. A. Rounds, B. J. Luft, et al. 2010. Genotypic Variation and Mixtures of Lyme Borrelia in Ixodes Ticks from North America and Europe. PLoS One. 5(5): e10650.
Dolan, M. C., E. H. Lacombe, and J. Piesman. 2000. Vector Competence of Ixodes affinis (Acari: Ixodidae) for Borrelia burgdorferi. Journal of Medical Entomology. 37: 766‒768.
Durden, L. A., and J. E. Keirans. 1996. Nymphs of the Genus Ixodes (Acari: Ixodidae) of the United States: Taxonomy, Identification Key, Distribution, Hosts, and Medical/veterinary Importance. Thomas Say Publications in Entomology. Entomological Society of America: Lanham, MD.
Durden, L. A., J. H. Oliver, Jr, and A. A. Kinsey. 2001. Ticks (Acari: Ixodidae) and Spirochetes (Spirochaetaceae: Spirochaetales) Recovered from Birds on a Georgia Barrier Island. Journal of Medical Entomology. 38: 231‒236.
Eisen, L., and R. S. Lane. 2002. Vectors of Borrelia burgdorferi Sensu Lato: Lyme Borreliosis: Biology, Epidemiology and Control. CABI Publishing: New York, NY.
Embers, M. E., S. W. Barthold, J. T. Borda, L. Bowers, L. Doyle, et al. 2012. Persistence of Borrelia burgdorferi in Rhesus Macaques Following Antibiotic Treatment of Disseminated Infection. PLoS One. 7(1): e29914. Doi: 10.1371/journal.pone.0029914.
Fein, L., and R. C. Tilton. 1997. Bone Marrow as a Source of Borrelia burgdorferi DNA. Journal of Spirochetal and Tick‒borne Diseases. 4: 58‒60.
Franke, J., A. Hildebrandt, and W. Dorn. 2013. Exploring Gaps in Our Knowledge on Lyme Borreliosis Spirochaetes—Updates on Complex Heterogeneity, Ecology, and Pathogenicity. Ticks and Tick‒borne Diseases. 4: 11‒25.
Frey, M., B. Jaulhac, Y. Piemont, L. Marcellin, P. M. Boohs, et al. 1998. Detection of Borrelia burgdorferi DNA in Muscle of Patients with Chronic Myalgia
Related to Lyme Disease. American Journal of Medicine. 104: 591‒594.
Gregson, J. D. 1956. The Ixodoidea of Canada: Publication 930. Science Service, Entomology Divison, Department of Agriculture, Canada.
Hamer, S. A., T. L. Goldberg, U. D. Kitron, J. D. Brawn, T. K. Anderson, et al. 2012. Wild Birds and Urban Ecology of Ticks and Tick‒borne Pathogens, Chicago, Illinois, USA, 2005‒2010. Emerging Infectious Diseases. 18: 1589‒1595.
Häupl, T., G. Hahn, M. Rittig, A. Krause, C. Schoerner, et al. 1993. Persistence of Borrelia burgdorferi in Ligamentous Tissue from a Patient with Chronic Lyme Borreliosis. Arthritis & Rheumatism. 36: 1621‒1626.
Kaiser, R. 2000. False‒negative Serology in Patients with Neuroborreliosis and the Value of Employing of Different Borrelial Strains in Serological Assays. Journal of Medical Microbiology. 49: 911‒915.
Keirans, J. E., and C. M. Clifford. 1978. The Genus Ixodes in the United States: A Scanning Electron Microscope Study and Key to the Adults. Journal of Medical Entomololgy, Supplement. 2: 1‒149.
Keirans, J. E., and R. S. Lane. 2008. Larval Keys to the Genera of Ixodidae (Acari) and Species of Ixodes (Latreille) Ticks Established in California. Pan‒Pacific Entomology. 84: 121‒142.
Klempner, M. S., R. Noring, and R. A. Rogers. 1993. Invasion of Human Skin Fibroblasts by the Lyme Disease Spirochete, Borrelia burgdorferi. Journal of
Infectious Diseases. 167(5): 1074‒1081.
Liegner, K.B., P. Duray, M. Agricola, C. Rosenkilde, L. A. Yannuzzi, et al. 1997. Lyme Disease and the Clinical Spectrum of Antibiotic Responsive Chronic Meningoencephalomyelitides. Journal of Spirochetal and Tick‒borne Diseases. 4: 61‒73.
MacDonald, A. B. 2006. Plaques of Alzheimer’s Disease Originate from Cysts of Borrelia burgdorferi, the Lyme Disease Spirochete. Medical Hypotheses. 67: 592‒600.
MacDonald, A. B. 2007. Alzheimer’s Neuroborreliosis with Trans‒synaptic Spread of Infection and Neurofibrillary Tangles Derived from Intraneuronal Spirochetes. Medical Hypotheses. 68: 822‒825.
MacDonald, A. B. 2013. Borrelia burgdorferi Tissue Morphologies and Imaging Methodologies. European Journal of Clinical Microbiology and Infectious Diseases. 32: 1077‒1082.
Maloney, E. L. 2009. The Need for Clincial Judgement in the Diagnosis and Treatment of Lyme Disease. Journal of American Physicians and Surgeons. 14:82‒89.
Mathers, A., R. P. Smith, B. Cahill, C. Lubelczyk, S. P. Elias, et al. 2011. Strain Diversity of Borrelia burgdorferi in Ticks Dispersed in North America by Migratory Birds. Journal of Medical Microbiology. 36: 24‒29.
Mayne, P. J. 2011. Emerging Incidence of Lyme Borreliosis, Babesiosis, Bartonellosis, and Granulocytic Ehrlichiosis in Australia. International Journal of General Medicine. 4: 845‒852.
Mayne, P. J. 2012. Investigation of Borrelia burgdorferi Genotypes in Australia Obtained from Erythema Migrans Tissue. Journal of Clinical, Cosmetic and Investigational Dermatology. 5: 69‒78.
Miklossy, J. 2011. Alzheimer’s Disease—A Neurospirochetosis. Analysis of the Evidence Following Koch’s and Hill’s Criteria. Journal of Neuroinflammation. 8: 90.
Miklossy, J., S. Kasas, A. D. Zurn, S. McCall, S. Yu, et al. 2008. Persisting Atypical and Cystic Forms of Borrelia burgdorferi and Local Inflammation in Lyme Neuroborreliosis. Journal of Neuroinflammation. 5: 40.
Morshed, M. G., J. D. Scott, K. Fernando, L. Beati, D. F. Mazerolle, et al. 2005. Migratory Songbirds Disperse Ticks across Canada, and First Isolation of the Lyme Disease Spirochete, Borrelia burgdorferi, from the Avian Tick, Ixodes Auritulus. Journal of Parasitology. 91: 780‒790.
Müller, K. E. 2012. Damage of Collagen and Elastic Fibres by Borrelia burgdorferi—Known and New Clinical and Histopathological Aspects. The Open Neurology Journal. 6: 179‒186.
Nicholson, W. L., D. E. Sonenshine, R. S. Lane, and G. Uilenberg. 2009. Ticks (Ixodoidea): Medical and Veterinary Entomology, 2nd edition. Elsevier Inc: Amsterdam, Netherlands.
Ogden, N. H., L. R. Lindsay, K. Hanincová, I. K. Barker, M. Bigras‒Poulin, et al. 2008. Role of Migratory Birds in Introduction and Range Expansion of Ixodes Scapularis Ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Applied and Environmental Microbiology. 74: 1780‒1790.
Oksi, J., H. Kalimo, R. J. Marttila, M. Marjamäki, P. Sonninen, et al. 1996. Inflammatory Brain Changes in Lyme Borreliosis: A Report on Three Patients and Review of Literature. Brain. 119: 2143‒2154.
Oksi, J., J. Mertsola, M. Reunanen, M. Marjamäki, and M. K. Viljanen. 1994. Subacute Multiple‒site Osteomyelitis Caused by Borrelia burgdorferi. Clinical Infectious Diseases. 19: 891‒896.
Oliver, J. H., Jr, T. Lin, L. Gao, K. L. Clark, C. W. Banks, et al. 2003. An Enzootic Transmission Cycle of Lyme Borreliosis Spirochetes in the Southeastern United States. Proceedings of the National Academy of Sciences, USA. 100: 11642‒11645.
Persing, D. H., TS. R. Telford, III, A. Spielman, S. W. Barthold. 1990. Detection of Borrelia burgdorferi Infection in Ixodes dammini Ticks with the Polymerase Chain Reaction. Journal of Clinical Microbiology. 28(3): 566‒572.
Persing, D. H., S. R.Telford, III, P. N. Rys, D. E. Dodge, T. J. White, et al. 1990. Detection of Borrelia burgdorferi DNA in Museum Specimens of Ixodes dammini Ticks. Science. 249: 1420‒1423.
Peterson, T. P. 2010. Peterson Field Guide to Birds of Western North America, 4th edition. Houghton Mifflin Harcourt Publishing Company: Boston, MA.
Platonov, A. E., L. S. Karan, N. M. Kolyasnikova, N. A. Makhneva, M. G. Toporkova, et al. 2011. Humans Infected with Relapsing Fever Spirochete
Borrelia miyamotoi, Russia. Emerging Infectious Diseases. 17:1816‒1823.
Preac‒Mursic, V., H. W. Pfister, H. Spiegel, R. Burk, B. Wilske, et al. 1993. First Isolation of Borrelia
burgdorferi from an Iris Biopsy. Journal of Clinical Neuro‒ophthalmology. 13: 155‒161.
Ramesh, G., J. T. Borda, J. Dufour, D. Kaushal, R. Ramamoorthy, et al. 2008. Interaction of the Lyme Disease Spirochete Borrelia burgdorferi with Brain Parenchyma Elicits Inflammatory Mediators from Glial Cells as well as Glial and Neuronal Apoptosis. The American Journal of Pathology. 173: 1415‒1427.
Ramesh, G., L. Santana‒Gould, F. M. Inglis, J. D. England, and M. T. Philipp. 2013. The Lyme Disease Spirochete Borrelia burgdorferi Induces Inflammation and Apoptosis in Cells from Dorsal Root Ganglia. Journal of Neuroinflammation. 10: 88.
Reed, K. D., J. K. Meece, J. S. Henkel, and S. K. Shukla. 2003. Birds, Migration and Emerging Zoonoses: West Nile Virus, Lyme Disease, Influenza A, and Enteropathogens. Clinical Medicine & Research. 1: 5‒12.
Rollend, L., D. Fish, and J. E. Childs. 2013. Transovarial Transmission of Borrelia spirochetes by Ixodes scapularis: A Summary of the Literature and Recent Observations. Ticks and Tick‒borne Diseases. 4(1 &2): 46‒51.
Sapi, E., A. B. MacDonald, K. Eisendle, H. Mueller, and B. Zelger. 2008. Biofilms of Borrelia burgdorferi in Chronic Borreliosis. American Journal of Clinical Pathology. 129: 988‒990.
Sapi, E., S. L. Bastian, C. M. Mpoy, S. Scott, A. Rattelle, et al. 2012. Characterization of Biofilm Formation by Borrelia burgdorferi In Vitro. PLoS One. 7: e48277.
Savely, V. 2010. Lyme Disease: A Diagnostic Dilemma. The Nurse Practioner. 35: 44‒50.
Schwarzová, K., T. Betáková, J. Neméth, and A. Mizáková A. 2006. Detection of Borrelia burgdorferi Sensu Lato and Chlamydophila psittaci in Throat and Cloacal Swabs from Birds Migrating through Slovakia. Folia Microbiol (Praha). 51: 653‒658.
Scott, J. D, J. F. Anderson, and L. A. Durden. 2012. Widespread Dispersal of Borrelia burgdorferi Infected Ticks Collected from Songbirds across Canada. Journal of Parasitology. 98: 49–59.
Scott, J. D., K. Fernando, S. N. Banerjee, L. A. Durden, S. K. Byrne, et al. 2001. Birds Disperse Ixodid (Acari: Ixodidae) and Borrelia burgdorferi‒ infected Ticks in Canada. Journal of Medical Entomology. 38: 493‒500.
Scott, J. D., M. K. Lee, K. Fernando, L. A. Durden, D. R. Jorgensen, et al. 2010. Detection of Lyme Disease Spirochete, Borrelia burgdorferi Sensu Lato, Including Three Novel Genotypes in Ticks (Acari: Ixodidae) Collected from Songbirds (Passeriformes) Across Canada. Journal of Vector Ecology. 35: 124‒139.
Sperling, J., M. Middelveen, D. Klein, and F. Sperling. 2012. Evolving Perspectives on Lyme Borreliosis in Canada. The Open Neurology Journal. 6: 94‒103.
Stafford, K. C., and U. Kitron. 2002. Environmental Management for Lyme Borreliosis Control: Lyme Borreliosis: Biology, Epidemiology and Control. CAB International: Oxon, Wallingford, UK.
Straubinger, R. K. 2000. PCR‒based Quantification of Borrelia burgdorferi Organisms in Canine Tissues over a 500‒Day Postinfection Period. Journal of Clinical Microbiology. 38(6): 2191‒2199.
Stricker, R. B., and L. Johnson. 2013. Borrelia burgdorferi Aggrecanase Activity: More Evidence for Persistent Infection in Lyme Disease. Frontiers in Cellular and Infection Microbiology. 3: 40.
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