Detection of Lyme Disease Spirochete, Borrelia burgdorferi Sensu Lato, Including Three Novel Genotypes in Ticks (Acari: Ixodidae) Collected from Songbirds (Passeriformes) Across Canada

ABSTRACT: Lyme disease is reported across Canada, but pinpointing the source of infection has been problematic. In this three-year, bird-tick-pathogen study (2004–2006), 366 ticks representing 12 species were collected from 151 songbirds (31 passerine species/subspecies) at 16 locations Canada-wide. Of the 167 ticks/pools tested, 19 (11.4%) were infected with Borrelia burgdorferi sensu lato (s.l.). Sequencing of the rrf-rrl intergenic spacer gene revealed four Borrelia genotypes: B. burgdorferi sensu stricto (s.s.) and three novel genotypes (BC genotype 1, BC genotype 2, BC genotype 3). All four genotypes were detected in spirochete-infected Ixodes auritulus (females, nymphs, larvae) suggesting this tick species is a vector for B. burgdorferi s.l. We provide first-time records for: ticks in the Yukon (north of 60° latitude), northernmost collection of Amblyomma americanum in North America, and Amblyomma imitator in Canada. First reports of bird-derived ticks infected with B. burgdorferi s.l. include: live culture of spirochetes from Ixodes pacificus (nymph) plus detection in I. auritulus nymphs, Ixodes scapularis in New Brunswick, and an I. scapularis larva in Canada. We provide the first account of B. burgdorferi s. l. in an Ixodes muris tick collected from a songbird anywhere. Congruent with previous data for the American Robin, we suggest that the Common Yellowthroat, Golden-crowned Sparrow, Song Sparrow, and Swainson's Thrush are reservoir-competent hosts. Song Sparrows, the predominant hosts, were parasitized by I. auritulus harboring all four Borrelia genotypes. Our results show that songbirds import B. burgdorferi s.l.-infected ticks into Canada. Bird-feeding I. scapularis subadults were infected with Lyme spirochetes during both spring and fall migration in eastern Canada. Because songbirds disperse millions of infected ticks across Canada, people and domestic animals contract Lyme disease outside of the known and expected range.

[1]  N. Rudenko,et al.  Delineation of a New Species of the Borrelia burgdorferi Sensu Lato Complex, Borrelia americana sp. nov , 2009, Journal of Clinical Microbiology.

[2]  J. Chatterton,et al.  Local Borrelia burgdorferi sensu stricto and Borrelia afzelii strains in a single mixed antigen improves western blot sensitivity , 2009, Journal of Clinical Pathology.

[3]  N. Rudenko,et al.  Borrelia carolinensis sp. nov., a New (14th) Member of the Borrelia burgdorferi Sensu Lato Complex from the Southeastern Region of the United States , 2008, Journal of Clinical Microbiology.

[4]  J. Miklossy,et al.  Persisting atypical and cystic forms of Borrelia burgdorferi and local inflammation in Lyme neuroborreliosis , 2008, Journal of Neuroinflammation.

[5]  N. Dobbs,et al.  Rickettsia amblyommii infecting Amblyomma americanum larvae. , 2008, Vector borne and zoonotic diseases.

[6]  M. Bigras-Poulin,et al.  Role of Migratory Birds in Introduction and Range Expansion of Ixodes scapularis Ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada , 2008, Applied and Environmental Microbiology.

[7]  N. Ogden,et al.  Blackbirds and Song Thrushes Constitute a Key Reservoir of Borrelia garinii, the Causative Agent of Borreliosis in Central Europe , 2007, Applied and Environmental Microbiology.

[8]  A. Guglielmone,et al.  Ticks collected on birds in the state of São Paulo, Brazil , 2007, Experimental and Applied Acarology.

[9]  G. Baranton,et al.  Multilocus sequence analysis of atypical Borrelia burgdorferi sensu lato isolates--description of Borrelia californiensis sp. nov., and genomospecies 1 and 2. , 2007, International journal of medical microbiology : IJMM.

[10]  S. Wright,et al.  Vertebrate hosts of Ixodes pacificus (Acari: Ixodidae) in California , 2007, Journal of vector ecology : journal of the Society for Vector Ecology.

[11]  A. Macdonald Alzheimer's neuroborreliosis with trans-synaptic spread of infection and neurofibrillary tangles derived from intraneuronal spirochetes. , 2007, Medical hypotheses.

[12]  Robert P. Smith,et al.  Borrelia garinii in Seabird Ticks (Ixodes uriae), Atlantic Coast, North America , 2006, Emerging infectious diseases.

[13]  S. Campbell,et al.  Prevalence of Ehrlichia, Borrelia, and Rickettsial Agents in Amblyomma americanum (Acari: Ixodidae) Collected from Nine States , 2006, Journal of medical entomology.

[14]  S. Mak,et al.  Distribution and Characterization of Borrelia burgdorferi Isolates from Ixodes scapularis and Presence in Mammalian Hosts in Ontario, Canada , 2006, Journal of medical entomology.

[15]  S. Bergström,et al.  Migratory Passerine Birds as Reservoirs of Lyme Borreliosis in Europe , 2006, Emerging infectious diseases.

[16]  G. Beauchamp,et al.  Ixodes scapularis Ticks Collected by Passive Surveillance in Canada: Analysis of Geographic Distribution and Infection with Lyme Borreliosis Agent Borrelia burgdorferi , 2006, Journal of medical entomology.

[17]  B. Chomel,et al.  Co-detection of Bartonella henselae, Borrelia burgdorferi, and Anaplasma phagocytophilum in Ixodes pacificus ticks from California, USA. , 2006, Vector borne and zoonotic diseases.

[18]  G. Baranton,et al.  Delineation of Borrelia burgdorferi sensu lato species by multilocus sequence analysis and confirmation of the delineation of Borrelia spielmanii sp. nov. , 2006, International journal of systematic and evolutionary microbiology.

[19]  R. Eisen,et al.  Geographical Distribution Patterns and Habitat Suitability Models for Presence of Host-Seeking Ixodid Ticks in Dense Woodlands of Mendocino County, California , 2006, Journal of medical entomology.

[20]  J. Tucker,et al.  An Avian Contribution to the Presence of Ixodes pacificus (Acari: Ixodidae) and Borrelia burgdorferi on the Sutter Buttes of California , 2006, Journal of medical entomology.

[21]  L. Jenni,et al.  Prevalence of Borrelia burgdorferi Sensu Lato in Ticks Collected from Migratory Birds in Switzerland , 2006, Applied and Environmental Microbiology.

[22]  J. Piesman,et al.  Three Multiplex Assays for Detection of Borrelia burgdorferi sensu lato and Borrelia miyamotoi sensu lato in Field-Collected Ixodes Nymphs in North America , 2005, Journal of medical entomology.

[23]  M. Morshed,et al.  MIGRATORY SONGBIRDS DISPERSE TICKS ACROSS CANADA, AND FIRST ISOLATION OF THE LYME DISEASE SPIROCHETE, BORRELIA BURGDORFERI, FROM THE AVIAN TICK, IXODES AURITULUS , 2005, The Journal of parasitology.

[24]  S. Baptista,et al.  Lyme borreliosis in Portugal caused by Borrelia lusitaniae? Clinical report on the first patient with a positive skin isolate , 2005, Wiener klinische Wochenschrift.

[25]  L. Tomassone,et al.  Borrelia burgdorferi sensu lato Infection in Larval Ixodes ricinus (Acari: Ixodidae) Feeding on Blackbirds in Northwestern Italy , 2005, Journal of medical entomology.

[26]  J. Oliver,et al.  MOLECULAR CHARACTERIZATION OF BORRELIA ISOLATES FROM TICKS AND MAMMALS FROM THE SOUTHERN UNITED STATES , 2004, The Journal of parasitology.

[27]  A. Papa,et al.  Borrelia valaisiana in Cerebrospinal Fluid , 2004, Emerging Infectious Diseases.

[28]  O. Morozova,et al.  Characterization of Borrelia burgdorferi sensu lato from Novosibirsk region (West Siberia, Russia) based on direct PCR , 2002, European Journal of Epidemiology.

[29]  S. Rijpkema,et al.  The distribution and prevalence of B. burgdorferi genomospecies in Ixodes ricinus ticks in Ireland , 2004, European Journal of Epidemiology.

[30]  T. Damrow,et al.  Vector competence of Ixodes angustus (Acari: Ixodidae) for Borrelia burgdorferi sensu stricto , 2004, Experimental & Applied Acarology.

[31]  I. Ivanov,et al.  Detection and typing of Borrelia burgdorferi sensu lato genospecies in Ixodes persulcatus ticks in West Siberia, Russia. , 2003, FEMS microbiology letters.

[32]  L. Eisen,et al.  Vector Competence of Ixodes pacificus and I. spinipalpis (Acari: Ixodidae), and Reservoir Competence of the Dusky-Footed Woodrat (Neotoma fuscipes) and the Deer Mouse (Peromyscus maniculatus), for Borrelia bissettii , 2003, Journal of medical entomology.

[33]  R. Hails,et al.  Association of Borrelia garinii and B. valaisiana with Songbirds in Slovakia , 2003, Applied and Environmental Microbiology.

[34]  J. Meece,et al.  Birds, migration and emerging zoonoses: west nile virus, lyme disease, influenza A and enteropathogens. , 2003, Clinical medicine & research.

[35]  F. Strle,et al.  Solitary borrelial lymphocytoma in adult patients. , 2002, Wiener klinische Wochenschrift.

[36]  F. Liang,et al.  An Immune Evasion Mechanism for Spirochetal Persistence in Lyme Borreliosis , 2002, The Journal of experimental medicine.

[37]  S. Etti,et al.  Host association of Borrelia burgdorferi sensu lato--the key role of host complement. , 2002, Trends in microbiology.

[38]  A. Alekseev,et al.  Evidence of Ehrlichiosis Agents Found in Ticks (Acari: Ixodidae) Collected from Migratory Birds , 2001, Journal of medical entomology.

[39]  M. Morshed,et al.  Birds Disperse Ixodid (Acari: Ixodidae) and Borrelia burgdorferi-Infected Ticks in Canada , 2001, Journal of medical entomology.

[40]  D. Postic,et al.  [The first isolation of Borrelia burgdorferi sensu stricto in Russia]. , 2001, Zhurnal mikrobiologii, epidemiologii, i immunobiologii.

[41]  J. Oliver,et al.  Ticks (Acari: Ixodidae) and Spirochetes (Spirochaetaceae: Spirochaetales) Recovered from Birds on a Georgia Barrier Island , 2001, Journal of medical entomology.

[42]  N. Takada,et al.  Characterization and Identification of Borrelia Isolates as Borrelia valaisiana in Taiwan and Kinmen Islands , 2000, Microbiology and immunology.

[43]  M. Miller,et al.  Ecology of Borrelia burgdorferi in Ticks (Acari: Ixodidae), Rodents, and Birds in the Sierra Nevada Foothills, Placer County, California , 2000, Journal of medical entomology.

[44]  J. Piesman,et al.  Vector Competence of Ixodes muris (Acari: Ixodidae) for Borrelia burgdorferi , 2000, Journal of medical entomology.

[45]  Z. Amr,et al.  Records of ticks (Acari: Ixodidae) parasitizing birds (Aves) in Rhode Island, USA , 2000 .

[46]  A. Spielman,et al.  Competence of American robins as reservoir hosts for Lyme disease spirochetes. , 2000, Emerging infectious diseases.

[47]  P. Duray,et al.  Physician-diagnosed erythema migrans and erythema migrans-like rashes following Lone Star tick bites. , 1998, Archives of dermatology.

[48]  L. Durden,et al.  Illustrated key to nymphs of the tick genus Amblyomma (Acari: Ixodidae) found in the United States. , 1998, Journal of medical entomology.

[49]  J. Ficker,et al.  Participation of birds (Aves) in the emergence of Lyme disease in southern Maine. , 1998, Journal of medical entomology.

[50]  D. Postic,et al.  An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. , 1998, Zentralblatt fur Bakteriologie : international journal of medical microbiology.

[51]  J. Oliver,et al.  First Isolation and Cultivation of Borrelia burgdorferi Sensu Lato from Missouri , 1998, Journal of Clinical Microbiology.

[52]  L. Patrican Absence of Lyme disease spirochetes in larval progeny of naturally infected Ixodes scapularis (Acari:Ixodidae) fed on dogs. , 1997, Journal of medical entomology.

[53]  J. Oliver,et al.  Unusual strain of Borrelia burgdorferi isolated from Ixodes dentatus in central Georgia. , 1996, The Journal of parasitology.

[54]  F. Strle,et al.  Patient isolates of Borrelia burgdorferi sensu lato with genotypic and phenotypic similarities of strain 25015. , 1996, The Journal of infectious diseases.

[55]  L. Durden,et al.  Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: taxonomy, identification key, distribution, hosts, and medical/veterinary importance. , 1996 .

[56]  S. Bergström,et al.  Transhemispheric exchange of Lyme disease spirochetes by seabirds , 1995, Journal of clinical microbiology.

[57]  R. Lane,et al.  Evidence implicating nymphal Ixodes pacificus (Acari: ixodidae) in the epidemiology of Lyme disease in California. , 1995, The American journal of tropical medicine and hygiene.

[58]  L. Magnarelli,et al.  Ticks (Acari: Ixodidae) infesting wild birds (Aves) and white-footed mice in Lyme, CT. , 1995, Journal of medical entomology.

[59]  G. Baranton,et al.  Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons. , 1994, International journal of systematic bacteriology.

[60]  G. Maupin,et al.  Discovery of an enzootic cycle of Borrelia burgdorferi in Neotoma mexicana and Ixodes spinipalpis from northern Colorado, an area where Lyme disease is nonendemic. , 1994, The Journal of infectious diseases.

[61]  R. C. Johnson,et al.  Isolation and characterization of Borrelia burgdorferi from blood of a bird captured in the Saint Croix River Valley , 1993, Journal of clinical microbiology.

[62]  S. G. Bennett,et al.  The larval ticks of the genus Ixodes Latreille (Acari: Ixodidae) of California. , 1990 .

[63]  J. Anderson,et al.  BIRD-FEEDING TICKS TRANSSTADIALLY TRANSMIT BORRELIA BURGDORFERI THAT INFECT SYRIAN HAMSTERS , 1990, Journal of wildlife diseases.

[64]  R. C. Johnson,et al.  Lyme disease and migrating birds in the Saint Croix River Valley , 1989, Applied and environmental microbiology.

[65]  T. Damrow,et al.  Is Ixodes (ixodiopsis) angustus a vector of Lyme disease in Washington State? , 1989, The Western journal of medicine.

[66]  R. C. Johnson,et al.  Antigenically variable Borrelia burgdorferi isolated from cottontail rabbits and Ixodes dentatus in rural and urban areas , 1989, Journal of clinical microbiology.

[67]  J. Anderson,et al.  New Borrelia burgdorferi antigenic variant isolated from Ixodes dammini from upstate New York , 1988, Journal of clinical microbiology.

[68]  M. Bissett,et al.  Characterization of Borrelia burgdorferi strains isolated from Ixodes pacificus ticks in California , 1987, Journal of clinical microbiology.

[69]  A. Spielman,et al.  Transovarially acquired Lyme disease spirochetes (Borrelia burgdorferi) in field-collected larval Ixodes dammini (Acari: Ixodidae). , 1986, Journal of medical entomology.

[70]  W. Burgdorfer,et al.  The western black-legged tick, Ixodes pacificus: a vector of Borrelia burgdorferi. , 1985, The American journal of tropical medicine and hygiene.

[71]  Anderson Jf,et al.  Avian and mammalian hosts for spirochete-infected ticks and insects in a Lyme disease focus in Connecticut. , 1984 .

[72]  H. Hoogstraal,et al.  Ticks from European-Asiatic Birds Migrating through Egypt into Africa , 1961, Science.

[73]  J. Gregson,et al.  The ixodoidea of Canada , 1956 .