Powassan Virus and Other Arthropod-Borne Viruses in Wildlife and Ticks in Ontario, Canada

Kathryn Smith Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada;
Canadian Wildlife Health Cooperative, University of Guelph, Guelph, Ontario, Canada;

Search for other papers by Kathryn Smith in
Current site
Google Scholar
PubMed
Close
,
Paul T. Oesterle Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada;
Canadian Wildlife Health Cooperative, University of Guelph, Guelph, Ontario, Canada;

Search for other papers by Paul T. Oesterle in
Current site
Google Scholar
PubMed
Close
,
Claire M. Jardine Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada;
Canadian Wildlife Health Cooperative, University of Guelph, Guelph, Ontario, Canada;

Search for other papers by Claire M. Jardine in
Current site
Google Scholar
PubMed
Close
,
Antonia Dibernardo National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Canada;

Search for other papers by Antonia Dibernardo in
Current site
Google Scholar
PubMed
Close
,
Chris Huynh National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Canada;

Search for other papers by Chris Huynh in
Current site
Google Scholar
PubMed
Close
,
Robbin Lindsay National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Canada;

Search for other papers by Robbin Lindsay in
Current site
Google Scholar
PubMed
Close
,
David L. Pearl Department of Population Medicine, University of Guelph, Guelph, Ontario, Canada;

Search for other papers by David L. Pearl in
Current site
Google Scholar
PubMed
Close
,
Angela M. Bosco-Lauth Department of Biomedical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado

Search for other papers by Angela M. Bosco-Lauth in
Current site
Google Scholar
PubMed
Close
, and
Nicole M. Nemeth Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada;
Canadian Wildlife Health Cooperative, University of Guelph, Guelph, Ontario, Canada;

Search for other papers by Nicole M. Nemeth in
Current site
Google Scholar
PubMed
Close
Restricted access

Powassan virus (POWV) is a tick-borne zoonosis maintained in natural enzootic cycles between ixodid ticks and wild mammals. Reported human cases have increased in recent years; these infections can be fatal or lead to long-term neurologic sequelae. However, both the geographic distribution and the role of common, potential mammalian hosts in POWV transmission are poorly understood, creating challenges to public health surveillance. We looked for evidence of POWV infection among candidate wildlife host species and ticks collected from mammals and birds in southern Ontario. Tissues (including blood) and ticks from trapped wild mammals were collected in the summers of 2015 and 2016. Ticks removed from dogs in 2015–2016 and wildlife diagnostic cases from 2011 to 2013 were also included. Tissue and tick (Ixodes spp.) homogenates were tested for POWV by reverse transcriptase–polymerase chain reaction (RT-PCR). In addition, sera from wild mammals were tested for antibodies to POWV, West Nile virus (WNV), and heartland virus (HRTV) by plaque reduction neutralization test. All 724 tissue samples were negative for POWV by RT-PCR. One of 53 pools of Ixodes cookei (among 98 total tick pools) was RT-PCR positive for deer tick virus (POWV) lineage. Antibodies to POWV and WNV were detected in 0.4% of 265 and 6.1% of 264 samples, respectively, and all of 219 serum samples tested negative for anti-HRTV antibodies. These results reveal low POWV detection rates in southern Ontario, while highlighting the challenges and need for continued efforts into understanding POWV epidemiology and targeted surveillance strategies.

Author Notes

Address correspondence to Nicole M. Nemeth, Southeastern Cooperative Wildlife Disease Study, University of Georgia, 589 D.W. Brooks Dr., Athens, GA 30602. E-mail: nmnemeth@uga.edu

Financial support: This research was funded by the Natural Sciences and Engineering Research Council of Canada with additional support from the Public Health Agency of Canada and the Canada Foundation for Innovation.

Authors’ addresses: Kathryn Smith and Paul T. Oesterle, Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada, E-mails: ksmith19@uoguelph.ca and oesterle@uoguelph.ca. Claire M. Jardine, Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada and Canadian Wildlife Health Cooperative, University of Guelph, Guelph, Ontario, Canada, E-mail: cjardi01@uoguelph.ca. Antonia Dibernardo, Chris Huynh, and L. Robbin Lindsay, National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada, E-mails: antonia.dibernardo@canada.ca, chris.huynh@canada.ca, and robbin.lindsay@canada.ca. David L. Pearl, Department of Population Medicine, University of Guelph, Guelph, Ontario, Canada, E-mail: dpearl@uoguelph.ca. Angela M. Bosco-Lauth, Department of Biomedical Sciences, College of Veterinary Medicine, Colorado State University, Fort Collins, CO, E-mail: mopargal@rams.colostate.edu. Nicole M. Nemeth, Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA, E-mail: nmnemeth@uga.edu.

  • 1.

    Ebel GD, 2010. Update on Powassan virus: emergence of a North American tick-borne flavivirus. Annu Rev Entomol 55: 95110.

  • 2.

    McLean DM, Donohue WL, 1959. Powassan virus: isolation of virus from a fatal case of encephalitis. Can Med Assoc J 80: 708711.

  • 3.

    Hermance ME, Thangamani S, 2017. Powassan virus: an emerging arbovirus of public health concern in North America. Vector Borne Zoonotic Dis 17: 453462.

    • Search Google Scholar
    • Export Citation
  • 4.

    Ebel GD, Kramer LD, 2004. Short report: duration of tick attachment required for transmission of Powassan virus by deer ticks. Am J Trop Med Hyg 71: 268271.

    • Search Google Scholar
    • Export Citation
  • 5.

    Hinten SR et al. 2008. Increased recognition of Powassan encephalitis in the United States, 1999–2005. Vector Borne Zoonotic Dis 8: 733740.

    • Search Google Scholar
    • Export Citation
  • 6.

    Artsob H, 1989. Powassan encephalitis. Monath TP, ed. The Arboviruses: Epidemiology and Ecology. Boca Raton, FL: CRC Press, 29–45.

  • 7.

    Keane DP, Little PB, Wilkie BN, Artsob H, Thorsen J, 1988. Agents of equine viral encephalomyeltis—correlation of serum and cerebrospinal fluid antibiotics. Can J Vet Res 52: 229235.

    • Search Google Scholar
    • Export Citation
  • 8.

    Little PB, Thorsen J, Moore W, Weninger N, 1985. Powassan virus encephalitis—a review and experimental studies in the horse and rabbit. Vet Pathol 22: 500507.

    • Search Google Scholar
    • Export Citation
  • 9.

    Artsob H, Spence L, Surgeoner G, McCreadie J, Thorsen J, Thng C, Lampotang V, 1984. Isolation of Francisella tularensis and Powassan virus from ticks (Acari, Ixodidae) in Ontario, Canada. J Med Entomol 21: 165168.

    • Search Google Scholar
    • Export Citation
  • 10.

    Artsob H, Spence L, Thng C, Lampotang V, Johnston D, Macinnes C, Matejka F, Voigt D, Watt I, 1986. Arbovirus infections in several Ontario mammals, 1975–1980. Can J Vet Res 50: 4246.

    • Search Google Scholar
    • Export Citation
  • 11.

    McLean DM, Best JM, Mahaling S, Chernesk MA, Wilson WE, 1964. Powassan virus: summer infection cycle, 1964. Can Med Assoc J 91: 13601362.

  • 12.

    McLean DM, Cobb C, Gooderham SE, Smart CA, Wilson AG, Wilson WE, 1967. Powassan virus: persistence of virus activity during 1966. Can Med Assoc J 96: 660664.

    • Search Google Scholar
    • Export Citation
  • 13.

    McLean DM, Crawford MA, Ladyman SR, Peers RR, Purvingo KW, 1970. California encephaitis and Powassan virus activity in British Columbia, 1969. Am J Med Entomol 92: 266272.

    • Search Google Scholar
    • Export Citation
  • 14.

    McLean DM, Devos A, Quantz EJ, 1964. Powassan virus: field investigations during the summer of 1963. Am J Trop Med Hyg 13: 747753.

  • 15.

    McLean DM, Larke RP, 1963. Powassan and Silverwater viruses: ecology of two Ontario arboviruses. Can Med Assoc J 88: 182185.

  • 16.

    Whitney E, Jamnback H, Means RG, Watthews TH, 1968. Arthropod-borne-virus survey in St. Lawrence County, New York. Am J Trop Med Hyg 17: 645650.

    • Search Google Scholar
    • Export Citation
  • 17.

    Doughty CT, Yawetz S, Lyons J, 2017. Emerging causes of arbovirus encephalitis in North America: Powassan, chikungunya, and Zika viruses. Curr Neurol Neurosci Rep 17: 12.

    • Search Google Scholar
    • Export Citation
  • 18.

    Piantadosi A et al. 2016. Emerging cases of Powassan virus encephalitis in New England: clinical presentation, imaging, and review of the literature. Clin Infect Dis 62: 707713.

    • Search Google Scholar
    • Export Citation
  • 19.

    Ogden NH, Maarouf A, Barker IK, Bigras-Poulin M, Lindsay LR, Morshed MG, O’Callaghan CJ, Ramay F, Waltner-Toews D, Charron DF, 2006. Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. Int J Paritisol 36: 6370.

    • Search Google Scholar
    • Export Citation
  • 20.

    Farkas MJ, Surgeoner GA, 1990. Incidence of Ixodes cookei (Acari, Ixodidae) on groundhogs, Marmota monax, in southwestern Ontario. Proc Entomol Soc Ont 121: 105110.

    • Search Google Scholar
    • Export Citation
  • 21.

    Johnson HN, 1987. Isolation of Powassan virus from a spotted skunk in California. J Wildl Dis 23: 152153.

  • 22.

    Root JJ, Oesterle PT, Nemeth NM, Klenk K, Gould DH, McLean RG, Clark L, Hall JS, 2006. Experimental infection of fox squirrels (Sciurus niger) with West Nile virus. Am J Trop Med Hyg 75: 697701.

    • Search Google Scholar
    • Export Citation
  • 23.

    Dupuis AP, Peters RJ, Prusinski MA, Falco RC, Ostfeld RS, Kramer LD, 2013. Isolation of deer tick virus (Powassan virus, Lineage II) from Ixodes scapularis and detection of antibody in vertebrate hosts sampled in the Hudson Valley, New York State. Parasit Vectors 6: 185.

    • Search Google Scholar
    • Export Citation
  • 24.

    Lindquist EE, Galloway TD, Artsob H, Lindsay LR, Drebot M, Wood H, Robbins RG, 2016. A Handbook to the Ticks of Canada (Ixodida: Ixodidae, Argasidae). Ottawa, Ontario, Canada: Biological Survey of Canada.

  • 25.

    Ebel GD, Foppa I, Spielman A, Telford SR, 1999. A focus of deer tick virus transmission in the northcentral United States. Emerg Infect Dis 5: 570574.

    • Search Google Scholar
    • Export Citation
  • 26.

    Jukes TH, Cantor CR, 1969. Evolution of protein molecules. Munro H, ed. Mammalian Protein Metabolism. New York, NY: Academic Press, 21–132.

  • 27.

    Kumar S, Stecher G, Tamura K, 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 18701874.

    • Search Google Scholar
    • Export Citation
  • 28.

    Larkin MA et al. 2007. Clustal W and clustal X version 2.0. Bioinformatics 23: 29472948.

  • 29.

    Clarke DH, Casals J, 1958. Techniques for hemagglutination and hemagglutination-inhibition with arthropod-borne viruses. Am J Trop Med Hyg 7: 561573.

    • Search Google Scholar
    • Export Citation
  • 30.

    Bailey TN, 1971. Biology of striped skunks on a southwestern Lake Erie marsh. Am Midl Nat 85: 196207.

  • 31.

    Blitvich BJ, Marlenee NL, Hall RA, Calisher CH, Bowen RA, Roehrig JT, Komar N, Langevin SA, Beaty BJ, 2003. Epitope-blocking enzyme-linked immunosorbent assays for the detection of serum antibodies to West Nile virus in multiple avian species. J Clin Microbiol 41: 10411047.

    • Search Google Scholar
    • Export Citation
  • 32.

    Bosco-Lauth AM et al. 2015. Serological investigation of heartland virus (Bunyaviridae: Phlebovirus) exposure in wild and domestic animals adjacent to human case sites in Missouri 2012–2013. Am J Trop Med Hyg 92: 11631167.

    • Search Google Scholar
    • Export Citation
  • 33.

    Tavakoli NP, Wang H, Dupuis M, Hull R, Ebel GD, Gilmore EJ, Faust PL, 2009. Brief report: fatal case of deer tick virus encephalitis. N Engl J Med 360: 20992107.

    • Search Google Scholar
    • Export Citation
  • 34.

    Cavanaugh CE, Muscat PL, Telford SR III, Goethert H, Pendlebury W, Elias SP, Robich R, Welch M, Lubelczyk CB, Smith RP, 2017. Fatal deer tick virus infection in Maine. Clin Infect Dis 65: 10431046.

    • Search Google Scholar
    • Export Citation
  • 35.

    Tutolo JW, Staples JE, Sosa L, Bennett N, 2017. Powassan virus disease in an infant—Connecticut, 2016. MMWR Morb Mortal Wkly Rep 66: 408409.

  • 36.

    Nofchissey RA et al. 2013. Seroprevalence of Powassan virus in New England deer, 1979–2010. Am J Trop Med Hyg 88: 11591162.

  • 37.

    Kokernot RH, Radivoje B, Anderson RJ, 1969. Susceptibility of wild and domestic mammals to four arboviruses. Am J Vet Res 30: 21972203.

  • 38.

    Mlera L, Meade-White K, Saturday G, Scott D, Bloom ME, 2017. Modeling Powassan virus infection in Peromyscus leucopus, a natural host. PLoS Negl Trop Dis 11: 119.

    • Search Google Scholar
    • Export Citation
  • 39.

    Zarnke RL, Yuill TM, 1981. Powassan virus infection in snowshoe hares (Lepus americanus). J Wildl Dis 17: 303310.

  • 40.

    Casey GA, Webster WA, 1975. Age and sex determination of striped skunks (Mephitis mephitis) from Ontario, Manitoba, and Quebec. Can J Zool 53: 223226.

    • Search Google Scholar
    • Export Citation
  • 41.

    Grizzell RA, 1955. A study of the southern woodchuck, Marmota monax monax. Am Midl Nat 53: 257293.

  • 42.

    Nelder MP, Russell C, Lindsay LR, Dhar B, Patel SN, Johnson S, Moore S, Kristjanson E, Li Y, Ralevski F, 2014. Population-based passive tick surveillance and detection of expanding foci of blacklegged ticks Ixodes scapularis and the Lyme disease agent Borrelia burgdorferi in Ontario, Canada. PLoS One 9: e105358.

    • Search Google Scholar
    • Export Citation
  • 43.

    Brackney DE, Nofchissey RA, Fitzpatrick KA, Brown IK, Ebel GD, 2008. Stable prevalence of Powassan virus in Ixodes scapularis in a northern Wisconsin focus. Am J Trop Med Hyg 79: 971973.

    • Search Google Scholar
    • Export Citation
  • 44.

    Brownstein JS, Holford TR, Fish D, 2005. Effect of climate change on Lyme disease risk in North America. EcoHealth 2: 3846.

  • 45.

    Drebot MA, Lindsay R, Barker IK, Buck PA, Fearon M, Hunter F, Sockett P, Artsob H, 2003. West Nile virus surveillance and diagnostics: a Canadian perspective. Can J Infect Dis 14: 105114.

    • Search Google Scholar
    • Export Citation
  • 46.

    Public Health Ontario, 2017. West Nile Virus Surveillance. Available at: https://www.publichealthontario.ca/en/DataAndAnalytics/Pages/WNV.aspx. Accessed July 20, 2017.

  • 47.

    Thompson M, Berke O, 2017. Evaluation of the control of West Nile virus in Ontario: did risk patterns change from 2005 to 2012? Zoonoses Public Health 64: 100105.

    • Search Google Scholar
    • Export Citation
  • 48.

    Root JJ, Bentler KT, Nemeth NM, Gidlewski T, Spraker TR, Franklin AB, 2010. Experimental infection of raccoons (Procyon lotor) with West Nile virus. Am J Trop Med Hyg 83: 803807.

    • Search Google Scholar
    • Export Citation
  • 49.

    Root JJ, 2013. West Nile virus associations in wild mammals: a synthesis. Arch Virol 158: 735752.

  • 50.

    Vasconcelos PFC, Calisher CH, 2016. Emergence of human arboviral diseases in the Americas, 2000–2016. Vector Borne Zoonotic Dis 16: 295301.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 72 72 9
Full Text Views 1580 250 4
PDF Downloads 274 67 3
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save