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

Particle and Fibre Toxicology

Laura D Kramer²  Richard S Ostfeld⁴  Richard C Falco⁵  Melissa A Prusinski¹  Ryan J Peters³  Alan P Dupuis II³ 

[1] Vector Ecology Laboratory, Bureau of Communicable Disease Control, New York State Department of Health, Albany, NY, 12237, USA;Department of Biomedical Sciences, School of Public Health, University at Albany, State University of New York, 1400 Western Ave, Albany, NY, 12222, USA;The Arbovirus Laboratories, Wadsworth Center, New York State Department of Health, 5668 State Farm Rd, Slingerlands, NY, 12159, USA;Cary Institute of Ecosystem Studies, 2801 Sharon Turnpike, Millbrook, NY, 12545, USA;Vector Ecology Laboratory, New York State Department of Health, Louis Calder Center, Fordham University, Armonk, NY, 10504, USA

关键词: Antibodies;    Serosurvey;    Birds;    Mammals;    Flavivirus;    Arbovirus;    Ticks;    Ixodes Scapularis;    Deer Tick Virus;    Powassan Virus;   

Others  :  1226158
DOI  :  10.1186/1756-3305-6-185

 received in 2013-04-16, accepted in 2013-06-13,  发布年份 2013

【 摘 要 】

Background

Deer tick virus, DTV, is a genetically and ecologically distinct lineage of Powassan virus (POWV) also known as lineage II POWV. Human incidence of POW encephalitis has increased in the last 15 years potentially due to the emergence of DTV, particularly in the Hudson Valley of New York State. We initiated an extensive sampling campaign to determine whether POWV was extant throughout the Hudson Valley in tick vectors and/or vertebrate hosts.

Methods

More than 13,000 ticks were collected from hosts or vegetation and tested for the presence of DTV using molecular and virus isolation techniques. Vertebrate hosts of Ixodes scapularis (black-legged tick) were trapped (mammals) or netted (birds) and blood samples analyzed for the presence of neutralizing antibodies to POWV. Maximum likelihood estimates (MLE) were calculated to determine infection rates in ticks at each study site.

Results

Evidence of DTV was identified each year from 2007 to 2012, in nymphal and adult I. scapularis collected from the Hudson Valley. 58 tick pools were positive for virus and/or RNA. Infection rates were higher in adult ticks collected from areas east of the Hudson River. MLE limits ranged from 0.2-6.0 infected adults per 100 at sites where DTV was detected. Virginia opossums, striped skunks and raccoons were the source of infected nymphal ticks collected as replete larvae. Serologic evidence of POWV infection was detected in woodchucks (4/6), an opossum (1/6), and birds (4/727). Lineage I, prototype POWV, was not detected.

Conclusions

These data demonstrate widespread enzootic transmission of DTV throughout the Hudson Valley, in particular areas east of the river. High infection rates were detected in counties where recent POW encephalitis cases have been identified, supporting the hypothesis that lineage II POWV, DTV, is responsible for these human infections.

【 授权许可】

   
2013 Dupuis et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Mandl CW, Holzmann H, Kunz C, Heinz FX: Complete genomic sequence of Powassan virus: evaluation of genetic elements in tick-borne versus mosquito-borne flaviviruses. Virology 1993, 194:173-184.
• [2]Grard G, Moureau G, Charrel RN, Lemasson JJ, Gonzalez JP, Gallian P, Gritsun TS, Holmes EC, Gould EA, de L X: Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy. Virology 2007, 361:80-92.
• [3]Mclean DM, Donahue W: Powassan virus: isolation of virus from a fatal case of encephalitis. Can Med Assoc J 1959, 80:708.
• [4]Ebel GD, Spielman A, Telford SR III: Phylogeny of North American Powassan virus. J Gen Virol 2001, 82:1657-1665.
• [5]Kuno G, Artsob H, Karabatsos N, Tsuchiya KR, Chang GJ: Genomic sequencing of deer tick virus and phylogeny of Powassan-related viruses of North America. AmJTrop Med Hyg 2001, 65:671-676.
• [6]Brackney DE, Nofchissey RA, Fitzpatrick KA, Brown IK, Ebel GD: Stable prevalence of Powassan virus in Ixodes scapularis in a northern Wisconsin focus. AmJTrop Med Hyg 2008, 79:971-973.
• [7]Mclean DM, Best JM, Mahalingam S, Chernesky MA, Wilson WE: Powassan virus: summer infection cycle, 1964. Can Med Assoc J 1964, 91:1360-1362.
• [8]Whitney E, Jamnback H: The first isolations of Powassan virus in New York State. Proc Soc Exp Biol Med 1965, 119:432-435.
• [9]Mclean DM, Smith PA, Livingstone SE, Wilson WE, Wilson AG: Powassan virus: vernal spread during 1965. Can Med Assoc J 1966, 94:532-536.
• [10]Artsob H: Powassan encephalitis. In The arboviruses. Edited by Monath TP. Boca Raton: CRC Press; 1989:29-49.
• [11]Telford SR III, Armstrong PM, Katavolos P, Foppa I, Garcia AS, Wilson ML, Spielman A: A new tick-borne encephalitis-like virus infecting New England deer ticks, Ixodes dammini. Emerg Infect Dis 1997, 3:165-170.
• [12]Anderson JF, Armstrong PM: Prevalence and genetic characterization of Powassan virus strains infecting Ixodes scapularis in Connecticut. AmJTrop Med Hyg 2012, 87:754-759.
• [13]Ebel GD, Foppa I, Spielman A, Telford SR: A focus of deer tick virus transmission in the northcentral United States. Emerg Infect Dis 1999, 5:570-574.
• [14]Thomas LA, Kennedy RC, Eklund CM: Isolation of a virus closely related to Powassan virus from Dermacentor andersoni collected along North Cache la Poudre River, Colo. Proc Soc Exp Biol Med 1960, 104:355-359.
• [15]Beasley DW, Suderman MT, Holbrook MR, Barrett AD: Nucleotide sequencing and serological evidence that the recently recognized deer tick virus is a genotype of Powassan virus. Virus Res 2001, 79:81-89.
• [16]L’Vov DK, Leonova GN, Gromashevskii VL, Belikova NP, Berezina LK: Isolation of the Powassan virus from Haemaphysalis neumanni Donitz, 1905 ticks in the Maritime Territory (in Russian). Vopr Virusol 1974, 19:538-541.
• [17]Leonova GN, Kondratov IG, Ternovoi VA, Romanova EV, Protopopova EV, Chausov EV, Pavlenko EV, Ryabchikova EI, Belikov SI, Loktev VB: Characterization of Powassan viruses from Far Eastern Russia. Arch Virol 2009, 154:811-820.
• [18]Reeves WC, Mariotte CO, Johnson HN, Scrivani RE: Encuesta serologica sobre los virus transmitidos por artropodos en la zona de Hermosillo, Mexico. Reimpreso del Boletin de la Oficina Sanitaria Panamericana 1962, LII:228-229.
• [19]Ebel GD, Campbell EN, Goethert HK, Spielman A, Telford SR III: Enzootic transmission of deer tick virus in New England and Wisconsin sites. AmJTrop Med Hyg 2000, 63:36-42.
• [20]Birge J, Sonnesyn S: Powassan virus encephalitis, Minnesota, USA. Emerg Infect Dis 2012, 18:1669-1671.
• [21]Tavakoli NP, Wang H, Dupuis M, Hull R, Ebel GD, Gilmore EJ, Faust PL: Fatal case of deer tick virus encephalitis. N Engl J Med 2009, 360:2099-2107.
• [22]Tokarz R, Jain K, Bennett A, Briese T, Lipkin WI: Assessment of polymicrobial infections in ticks in New York state. Vector Borne Zoonotic Dis 2010, 10:217-221.
• [23]El Khoury MY, Hull RC, Bryant PW, Escuyer KL, St GK, Wong SJ, Nagaraja A, Kramer L, Dupuis AP, Purohit T, Shah T, Wormser GP: Diagnosis of acute deer tick virus encephalitis. Clin Infect Dis 2013, 56:e40-e47.
• [24]Ostfeld RS, Keesing F: Biodiversity and disease risk: the case of Lyme disease. Conserv Biol 2000, 14:722-728.
• [25]Ostfeld RS, Hazler KR, Cepeda OM: Temporal and spatial dynamics of Ixodes scapularis (Acari: Ixodidae) in a rural landscape. J Med Entomol 1996, 33:90-95.
• [26]Ostfeld RS, Canham CD, Oggenfuss K, Winchcombe RJ, Keesing F: Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biol 2006, 4:e145.
• [27]Keesing F, Brunner J, Duerr S, Killilea M, LoGiudice K, Schmidt K, Vuong H, Ostfeld RS: Hosts as ecological traps for the vector of Lyme disease. Proc Biol Sci 2009, 276:3911-3919.
• [28]Hinten SR, Beckett GA, Gensheimer KF, Pritchard E, Courtney TM, Sears SD, Woytowicz JM, Preston DG, Smith RP Jr, Rand PW, Lacombe EH, Holman MS, Lubelczyk CB, Kelso PT, Beelen AP, Stobierski MG, Sotir MJ, Wong S, Ebel G, Kosoy O, Piesman J, Campbell GL, Marfin AA: Increased recognition of Powassan encephalitis in the United States, 1999–2005. Vector Borne Zoonotic Dis 2008, 8:733-740.
• [29]LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F: The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci U S A 2003, 100:567-571.
• [30]LoGiudice K, Duerr ST, Newhouse MJ, Schmidt KA, Killilea ME, Ostfeld RS: Impact of host community composition on Lyme disease risk. Ecology 2008, 89:2841-2849.
• [31]Pyle P: Identification Guide to North American Birds, Part I. 2nd edition. Bolinas, California: Slate Creek Press; 1997.
• [32]Lindsey HS, Calisher CH, Matthews JH: Serum dilution neutralization test for California group virus identification and serology. J Clin Microbiol 1976, 4:503-510.
• [33]Kokernot RH, Radivojevic B, Anderson RJ: Susceptibility of wild and domesticated mammals to four arboviruses. Am J Vet Res 1969, 30:2197-2203.
• [34]Jones LD, Davies CR, Steele GM, Nuttall PA: A novel mode of arbovirus transmission involving a nonviremic host. Science 1987, 237:775-777.
• [35]Labuda M, Nuttall PA, Kozuch O, Eleckova E, Williams T, Zuffova E, Sabo A: Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 1993, 49:802-805.
• [36]Labuda M, Kozuch O, Zuffova E, Eleckova E, Hails RS, Nuttall PA: Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts 66. Virology 1997, 235:138-143.
• [37]Nonaka E, Ebel GD, Wearing HJ: Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes. PLoS One 2010, 5:e11745.
• [38]Costero A, Grayson MA: Experimental transmission of Powassan virus (Flaviviridae) by Ixodes scapularis ticks (Acari: Ixodidae). AmJTrop Med Hyg 1996, 55:536-546.
• [39]Anderson JF, Magnarelli LA: Vertebrate host relationships and distribution of ixodid ticks (Acari: Ixodidae) in Connecticut, USA. J Med Entomol 1980, 17:314-323.
• [40]Reid HW, Duncan JS, Phillips JD, Moss R, Watson A: Studies of louping-ill virus (Flavivirus group) in wild red grouse (Lagopus lagopus scoticus). J Hyg (Lond) 1978, 81:321-329.
• [41]Ernek E, Kozuch O, Lichard M, Nosek J: The role of birds in the circulation of tick-borne encephalitis virus in the Tribec region. Acta Virol 1968, 12:468-470.
• [42]Whitney E: Serologic evidence of group A and B arthropod-borne virus activity in New York State. AmJTrop Med Hyg 1963, 12:417-424.
• [43]Mclean DM, Bergman SK, Goddard EJ, Graham EA, Purvin-Good KW: North–south distribution of arbovirus reservoirs in British Columbia, 1970. Can J Public Health 1971, 62:120-124.
• [44]Morshed MG, Scott JD, Fernando K, Beati L, Mazerolle DF, Geddes G, Durden LA: Migratory songbirds disperse ticks across Canada, and first isolation of the Lyme disease spirochete, Borrelia burgdorferi, from the avian tick, Ixodes auritulus 12. J Parasitol 2005, 91:780-790.
• [45]Ogden NH, Lidsay LR, Hanincova K, Barker IK, Bigras-Poulin M, Charron DF, Heagy A, Francis CM, O’Callaghan CJ, Schwartz I, Thompson RA: Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol 2008, 74:1780-1790.
• [46]Ebel GD, Kramer LD: Short report: duration of tick attachment required for transmission of Powassan virus by deer ticks. AmJTrop Med Hyg 2004, 71:268-271.