Analyze Diet
Parasites & vectors2016; 9(1); 474; doi: 10.1186/s13071-016-1765-1

Host associations of mosquitoes at eastern equine encephalitis virus foci in Connecticut, USA.

Abstract: Eastern equine encephalitis virus (EEEV) is a highly pathogenic mosquito-borne arbovirus, with active transmission foci in freshwater hardwood swamps in eastern North America, where enzootic transmission is maintained between the ornithophilic mosquito, Culiseta melanura, and wild passerine birds. The role of other locally abundant mosquito species in virus transmission and their associations with vertebrate hosts as sources of blood meals within these foci are largely unknown but are of importance in clarifying the dynamics of enzootic and epidemic/epizootic transmission. Blood-engorged mosquitoes were collected from resting boxes at four established EEEV foci in Connecticut during 2010-2011. Mosquitoes were identified to species, and the identity of vertebrate hosts was determined based on mitochondrial cytochrome b and/or cytochrome c oxidase subunit I gene sequences of polymerase chain reaction products. The vertebrate hosts of 378 (50.3 % of engorged mosquitoes) specimens, representing 12 mosquito species, were identified. Culiseta morsitans (n = 54; 67.5 %), Culex restuans (n = 4; 66.7 %), and Cx. pipiens (n = 2; 100 %) acquired blood meals exclusively from avian hosts, whereas Aedes cinereus (n = 6; 66.7 %), Ae. canadensis (n = 2; 100 %), and Ae. stimulans (n = 1; 100 %) obtained blood meals solely from mammals. Species that fed opportunistically on both avian and mammalian hosts included: Ae. thibaulti (n = 21 avian, and n = 181 mammalian; 57.2 %), Anopheles punctipennis (n = 8 and n = 40; 44.0 %), An. quadrimaculatus (n = 1 and n = 23; 35.7 %), Coquillettidia perturbans (n = 3 and n = 3; 46.2 %) and Ae. abserratus (n = 1 and n = 2; 23.1 %). Culex territans obtained blood meals from avian and amphibian hosts (n = 18 and n = 5; 26.6 %). Mixed blood meals originating from both avian and mammalian hosts were identified in An. quadrimaculatus (n = 1), and Cx. territans (n = 2). Our findings indicate that wood thrush, tufted titmouse, and a few other avian species serve as hosts for mosquitoes, and likely contribute to amplification of EEEV. Our study supports the role of Cs. morsitans in enzootic transmission of EEEV among avian species. Culex territans will seek blood from multiple vertebrate classes, suggesting that this species may contribute to epizootic transmission of the virus. Our findings support roles for Cq. perturbans and An. quadrimaculatus as epidemic/epizootic vectors to humans, horses, and white-tailed deer. Despite its abundance, the potential of Ae. thibaulti to serve as a "bridge vector" for EEEV remains unclear in the absence of any definitive knowledge on its competency for the virus. The contribution of white-tailed deer to the dynamics of EEEV transmission is not fully understood, but findings indicate repeated exposure due to frequent feeding by vector competent mosquito species.
Publication Date: 2016-08-30 PubMed ID: 27577939PubMed Central: PMC5006286DOI: 10.1186/s13071-016-1765-1Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.
  • Research Support
  • U.S. Gov't
  • P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research study investigates the roles of various mosquito species in transmitting the Eastern equine encephalitis virus (EEEV) in Connecticut, USA. The virus, identified in mosquitoes that were collected and then identified to species, primarily transmits between a mosquito type and wild birds. This study’s findings reveal that many bird species host these mosquitoes and contribute to the spread of the virus, while various mosquito species were identified as possible transmission vectors to humans, horses, and deer.

Objective and Methodology of the Study

  • The primary aim of the research was to analyze the associations of different mosquito species with their vertebrate hosts, especially the ones that serve as direct sources of blood meals within transmission foci of EEEV.
  • Blood-engorged mosquitoes were collected from resting boxes at four established EEEV foci in Connecticut for two years (2010-2011).
  • The mosquitoes were then classified by species, and the identities of their vertebrate hosts were determined using gene sequences of polymerase chain reaction products.

Findings of the Study

  • From the collected specimens, hosts of 378 mosquitoes from 12 species were identified.
  • Certain mosquito species, including Culiseta morsitans, Culex restuans, and Cx. pipiens, exclusively obtained blood meals from bird hosts.
  • Other species, such as Aedes cinereus, Ae. canadensis, and Ae. stimulans, only received blood meals from mammalian hosts.
  • Some mosquito species were found to feed freely on both birds and mammals. These include Ae. thibaulti, Anopheles punctipennis, An. quadrimaculatus, Coquillettidia perturbans, and Ae. abserratus.
  • Additionally, mixed blood meals from both birds and mammals were identified in An. quadrimaculatus and Cx. territans.
  • These findings highlight that species like wood thrush and tufted titmouse among others serve as hosts for mosquitoes and contribute to the amplification of EEEV.

Implications of the Findings

  • The research supports the role of the mosquito species Cs. morsitans in enzootic transmission of EEEV among bird species.
  • Moreover, it was suggested that Culex territans, due to its feeding habits on multiple classes of vertebrates, may contribute to epizootic transmission of the virus.
  • Similarly, Cq. perturbans and An. quadrimaculatus are proposed as epidemic/epizootic vectors because they can transmit the virus to humans, horses, and deer.
  • The role of Ae. thibaulti in EEEV transmission is indefinite without any definite knowledge of its competency for the virus.
  • The contribution of white-tailed deer to the transmission dynamic of EEEV is unclear, however, the research points towards frequent exposure due to repeated feeding by vectors.

Cite This Article

APA
Shepard JJ, Andreadis TG, Thomas MC, Molaei G. (2016). Host associations of mosquitoes at eastern equine encephalitis virus foci in Connecticut, USA. Parasit Vectors, 9(1), 474. https://doi.org/10.1186/s13071-016-1765-1

Publication

ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 9
Issue: 1
Pages: 474

Researcher Affiliations

Shepard, John J
  • Department of Environmental Sciences, and Center for Vector Biology & Zoonotic Diseases, The Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, CT, 06511, USA.
Andreadis, Theodore G
  • Department of Environmental Sciences, and Center for Vector Biology & Zoonotic Diseases, The Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, CT, 06511, USA.
  • Department of Epidemiology of Microbial Diseases, Yale School of Public Health, 60 College Street, P.O. Box 208034, New Haven, CT, 06520-8034, USA.
Thomas, Michael C
  • Department of Environmental Sciences, and Center for Vector Biology & Zoonotic Diseases, The Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, CT, 06511, USA.
Molaei, Goudarz
  • Department of Environmental Sciences, and Center for Vector Biology & Zoonotic Diseases, The Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, CT, 06511, USA. Goudarz.Molaei@ct.gov.
  • Department of Epidemiology of Microbial Diseases, Yale School of Public Health, 60 College Street, P.O. Box 208034, New Haven, CT, 06520-8034, USA. Goudarz.Molaei@ct.gov.

MeSH Terms

  • Animals
  • Bird Diseases / epidemiology
  • Bird Diseases / virology
  • Connecticut
  • Culicidae / classification
  • Culicidae / virology
  • Encephalitis Virus, Eastern Equine / physiology
  • Mammals / blood
  • Passeriformes / blood
  • Passeriformes / virology

References

This article includes 62 references
  1. Morris CD. Eastern equine encephalomyelitis. 1988. pp. 1–20.
  2. Howard JJ, Morris CD, Emord DE, Grayson MA. Epizootiology of eastern equine encephalitis virus in upstate New York, USA. VII. Virus surveillance 1979–1985, description of 1983 outbreak, and series conclusions. J Med Entomol 1988;25:501–14.
    doi: 10.1093/jmedent/25.6.501pubmed: 2905010google scholar: lookup
  3. Armstrong PM, Andreadis TG. Eastern equine encephalitis virus-old enemy, new threat. N Engl J Med 2013;368:1670–3.
    doi: 10.1056/NEJMp1213696pubmed: 23635048google scholar: lookup
  4. Howard JJ, Grayson MA, White DJ, Oliver J. Evidence of multiple foci of eastern equine encephalitis virus (Togaviridae: Alphavirus) in central New York state. J Med Entomol 1996;33:421–32.
    doi: 10.1093/jmedent/33.3.421pubmed: 8667390google scholar: lookup
  5. Armstrong PM, Andreadis TG. Eastern equine encephalitis virus in mosquitoes and their role as bridge vectors. Emerg Infect Dis 2010;16:1869–74.
    doi: 10.3201/eid1612.100640pmc: PMC3294553pubmed: 21122215google scholar: lookup
  6. Saxton-Shaw KD, Ledermann JP, Kenney JL, Berl E, Graham AC, Russo JM. The first outbreak of eastern equine encephalitis in Vermont: outbreak description and phylogenetic relationships of the virus isolate. PLoS One 2015;10:e0128712.
  7. Lubelczyk C, Mutebi JP, Robinson S, Elias SP, Smith LB, Juris SA. An epizootic of eastern equine encephalitis virus, Maine, USA in 2009: outbreak description and entomological studies. Am J Trop Med Hyg 2013;88:95–102.
    doi: 10.4269/ajtmh.2012.11-0358pmc: PMC3541751pubmed: 23208877google scholar: lookup
  8. Nelson R, Ciesielski T, Andreadis T, Armstrong P. Human case of eastern equine encephalitis - Connecticut, 2013. Conn Epidemiologist 2014;34:9–10.
  9. Oliver J, Lukacik G, Kramer LD, Backenson PB, Sherwood JA, Howard JJ. Geography and timing of cases of eastern equine encephalitis in New York state from 1992 to 2012. Vector Borne Zoonotic Dis 2016;16:283–9.
    doi: 10.1089/vbz.2015.1864pubmed: 26901637google scholar: lookup
  10. Crans WJ, Caccamise DF, McNelly JR. Eastern equine encephalomyelitis virus in relation to the avian community of a coastal cedar swamp. J Med Entomol 1994;31:711–8.
    doi: 10.1093/jmedent/31.5.711pubmed: 7966175google scholar: lookup
  11. Howard JJ, Oliver J, Grayson MA. Antibody response of wild birds to natural infection with alphaviruses. J Med Entomol 2004;41:1090–103.
    doi: 10.1603/0022-2585-41.6.1090pubmed: 15605649google scholar: lookup
  12. Molaei G, Oliver J, Andreadis TG, Armstrong PM, Howard JJ. Molecular identification of blood-meal sources in Culiseta melanura and Culiseta morsitans from an endemic focus of eastern equine encephalitis virus in New York. Am J Trop Med Hyg 2006;75:1140–7.
    pubmed: 17172382
  13. Molaei G, Andreadis TG, Armstrong PM, Thomas MC, Deschamps T, Cuebas-Incle E. Vector-host interactions and epizootiology of eastern equine encephalitis virus in Massachusetts. Vector Borne Zoonotic Dis 2013;13:312–23.
    doi: 10.1089/vbz.2012.1099pubmed: 23473221google scholar: lookup
  14. Molaei G, Armstrong PM, Abadam CF, Akaratovic KI, Kiser JP, Andreadis TG. Vector-host interactions of Culiseta melanura in a focus of eastern equine encephalitis virus activity in southeastern Virginia. PLoS One 2015;10:e0136743.
  15. Molaei G, Armstrong PM, Graham AC, Kramer LD, Andreadis TG. Insights into the recent emergence and expansion of eastern equine encephalitis virus in a new focus in the Northern New England USA. Parasit Vectors 2015;8:516.
    doi: 10.1186/s13071-015-1145-2pmc: PMC4600208pubmed: 26453283google scholar: lookup
  16. Molaei G, Thomas MC, Muller T, Medlock J, Shepard JJ, Armstrong PM, Andreadis TG. Dynamics of vector-host interactions in avian communities in four eastern equine encephalitis virus foci in the northeastern U.S.. PLoS Negl Trop Dis 2016;10:e0004347.
  17. Crans WJ, McNelly J, Schulze TL, Main A. Isolation of eastern equine encephalitis virus from Aedes sollicitans during an epizootic in southern New Jersey. J Am Mosq Control Assoc 1986;2:68–72.
    pubmed: 2853203
  18. Crans WJ, Schulze TL. Evidence incriminating Coquillettidia perturbans (Diptera: Culicidae) as an epizootic vector of eastern equine encephalitis. I. Isolation of EEE virus from Cq. perturbans during an epizootic among horses in New Jersey. Bull Soc Vector Ecol 1986;11:178–84.
  19. Vaidyanathan R, Edman JD, Cooper LA, Scott TW. Vector competence of mosquitoes (Diptera: Culicidae) from Massachusetts for a sympatric isolate of eastern equine encephalomyelitis virus. J Med Entomol 1997;34:346–52.
    doi: 10.1093/jmedent/34.3.346pubmed: 9151501google scholar: lookup
  20. Moncayo AC, Edman JD. Toward the incrimination of epidemic vectors of eastern equine encephalomyelitis virus in Massachusetts: abundance of mosquito populations at epidemic foci. J Am Mosq Control Assoc 1999;15:479–92.
    pubmed: 10612612
  21. Komar N, Dohm DJ, Turell MJ, Spielman A. Eastern equine encephalitis virus in birds: relative competence of European starlings (Sturnus vulgaris). Am J Trop Med Hyg 1999;60:387–91.
    pubmed: 10466964
  22. Molaei G, Andreadis TG, Armstrong PM, Diuk-Wasser M. Host-feeding patterns of potential mosquito vectors in Connecticut, U.S.A.: molecular analysis of bloodmeals from 23 species of Aedes, Anopheles, Culex, Coquillettidia, Psorophora, and Uranotaenia. J Med Entomol 2008;45:1143–51.
  23. Morris CD. A structural and operational analysis of diurnal resting shelters for mosquitoes (Diptera: Culicidae). J Med Entomol 1981;18:419–24.
    doi: 10.1093/jmedent/18.5.419google scholar: lookup
  24. Komar N, Pollack RJ, Spielman A. A nestable fiber pot for sampling resting mosquiotes. J Am Mosq Control Assoc 1995;11:463–7.
    pubmed: 8825509
  25. Andreadis TG, Thomas MC, Shepard JJ. Identification guide to the mosquitoes of Connecticut. Bull Conn Agric Exp Stn 2005;966:173.
  26. Darsie RF Jr, Ward RA. Identification and geographical distribution of the mosquitoes of North America, north of Mexico. 1981. p. 313.
  27. Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR. Host feeding patterns of Culex mosquitoes and west nile virus transmission, northeastern United States. Emerg Infect Dis 2006;12:468–74.
    doi: 10.3201/eid1203.051004pmc: PMC3291451pubmed: 16704786google scholar: lookup
  28. Molaei G, Andreadis TG. Identification of avian- and mammalian-derived bloodmeals in Aedes vexans and Culiseta melanura (Diptera: Culicidae) and its implication for West Nile virus transmission in Connecticut USA. J Med Entomol 2006;43:1088–93.
  29. Hebert PDN, Cywinska A, Ball SL, de Waard JR. Biological identifications through DNA barcodes. Proc R Soc Lond B Biol Sci 2003;270:313–21.
    doi: 10.1098/rspb.2002.2218pmc: PMC1691236pubmed: 12614582google scholar: lookup
  30. Bartlett-Healy K, Crans W, Gaugler R. Vertebrate hosts and phylogenetic relationships of amphibian trypanosomes from a potential invertebrate vector, Culex territans Walker (Diptera: Culicidae). J Parasitol 2009;95:381–7.
    doi: 10.1645/GE-1793.1pubmed: 18850768google scholar: lookup
  31. National Center for Biotechnology Information. The BLAST Sequence Analysis Tool. Accessed 28 July 2016.
  32. Magnarelli LA. Host feeding patterns of Connecticut mosquitoes (Diptera: Culicidae). Am J Trop Med Hyg 1977;26:547–52.
    pubmed: 17310
  33. Nasci RS, Edman JD. Blood-feeding patterns of Culiseta melanura (Diptera: Culicidae) and associated sylvan mosquitoes in southeastern Massachusetts eastern equine encephalitis enzootic foci. J Med Entomol 1981;18:493–500.
    doi: 10.1093/jmedent/18.6.493google scholar: lookup
  34. Apperson CS, Hassan HK, Harrison BA, Savage HM, Aspen SE, Farajollahi A. Host-feeding patterns of established and potential mosquito vectors of West Nile virus in the eastern United States. Vector Borne Zoonotic Dis 2004;4:71–82.
    doi: 10.1089/153036604773083013pmc: PMC2581457pubmed: 15018775google scholar: lookup
  35. Andreadis TG, Armstrong PM, Anderson JF, Main AJ. Spatial-temporal analysis of Cache Valley virus infection in Anopheline and Culicine mosquitoes in the northeastern United States, 1997–2012. Vector Borne Zoonotic Dis 2014;14:763–73.
    doi: 10.1089/vbz.2014.1669pmc: PMC4208611pubmed: 25325321google scholar: lookup
  36. Massachusetts Dept. of Public Health. Arbovirus surveillance summary. 2012. Accessed 17 March 2016.
  37. Crans WJ, Rockel EG. The mosquitoes attracted to turtles. Mosq News 1968;28:332–7.
  38. Cohen SB, Lewoczko K, Huddleston DB, Moody E, Mukherjee S, Dunn JR. Host feeding patterns of potential vectors of eastern equine encephalitis virus at an epizootic focus in Tennessee. Am J Trop Med Hyg 2009;81:452–6.
    pubmed: 19706914
  39. Estep LK, McClure CJ, Burkett-Cadena ND, Hassan HK, Hicks TL, Unnasch TR. A multi-year study of mosquito feeding patterns on avian hosts in a southeastern focus of eastern equine encephalitis virus. Am J Trop Med Hyg 2011;84:718–26.
    doi: 10.4269/ajtmh.2011.10-0586pmc: PMC3083738pubmed: 21540380google scholar: lookup
  40. Main AJ, Anderson KS, Maxfield HK, Rosenau B, Oliver C. Duration of Alphavirus neutralizing antibody in naturally infected birds. Am J Trop Med Hyg 1988;38:208–17.
    pubmed: 2829638
  41. Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO. Host selection by Culex pipiens mosquitoes and west nile virus amplification. Am J Trop Med Hyg 2009;80:268–78.
    pubmed: 19190226
  42. Farajollahi A, Fonseca DM, Kramer LD, Kilpatrick AM. “Bird biting” mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol 2011;11:1577–85.
  43. Andreadis TG, Anderson JF, Tirrell-Peck SJ. Multiple isolations of eastern equine encephalitis and highlands J viruses from mosquitoes (Diptera: Culicidae) during a 1996 epizootic in southeastern Connecticut. J Med Entomol 1998;35:296–302.
    doi: 10.1093/jmedent/35.3.296pubmed: 9615549google scholar: lookup
  44. Crans WJ. The blood feeding habits of Culex territans Walker. Mosq News 1970;30:445–7.
  45. Burkett-Cadena ND, Graham SP, Hassan HK, Guyer C, Eubanks MD. Blood feeding patterns of potential arbovirus vectors of the genus Culex targeting ectothermic hosts. Am J Trop Med Hyg 2008;79:809–15.
    pmc: PMC4138019pubmed: 18981528
  46. Burkett-Cadena ND, Bingham AM, Hunt B, Morse G, Unnasch TR. Ecology of Culiseta melanura and other mosquitoes (Diptera: Culicidae) from Walton County, FL, during winter period 2013–2014. J Med Entomol 2015;52:1074–82.
    doi: 10.1093/jme/tjv087pmc: PMC4668758pubmed: 26336227google scholar: lookup
  47. Bingham AM, Graham SP, Burkett-Cadena ND, White GS, Hassan HK, Unnasch TR. Detection of eastern equine encephalomyelitis virus RNA in North American snakes. Am J Trop Med Hyg 2012;87:1140–4.
    doi: 10.4269/ajtmh.2012.12-0257pmc: PMC3516089pubmed: 23033405google scholar: lookup
  48. Graham SP, Hassan HK, Chapman T, White G, Guyer C, Unnasch TR. Serosurveillance of eastern equine encephalitis virus in amphibians and reptiles from Alabama, USA. Am J Trop Med Hyg 2012;86:540–4.
    doi: 10.4269/ajtmh.2012.11-0283pmc: PMC3284378pubmed: 22403333google scholar: lookup
  49. Morris CD, Whitney E, Bast TF, Deibel R. An outbreak of eastern equine encephalomyelitis in upstate New York during 1971. Am J Trop Med Hyg 1973;22:561–6.
    pubmed: 4146219
  50. Rhode Island Department of Environmental Management. Press Release 13 October 2004. Accessed 17 March 2016.
  51. Morris CD, Zimmerman RH. Epizootiology of eastern equine encephalomyelitis virus in upstate New York, USA. III. Population dynamics and vector potential of adult Culiseta morsitans (Diptera: Culicidae). J Med Entomol 1981;18:313–6.
    doi: 10.1093/jmedent/18.4.313pubmed: 7265134google scholar: lookup
  52. Hayes RO. Host preferences of Culiseta melanura and allied mosquitoes. Mosq News 1961;21:179–87.
  53. Edman JD. Host-feeding patterns of Florida mosquitoes I. Aedes, Anopheles, Coquillettidia, Mansonia and Psorophora. J Med Entomol 1971;8:687–95.
    doi: 10.1093/jmedent/8.6.687pubmed: 4403447google scholar: lookup
  54. Cupp EW, Klingler K, Hassan HK, Viguers LM, Unnasch TR. Transmission of eastern equine encephalomyelitis virus in central Alabama. Am J Trop Med Hyg 2003;68:495–500.
    pmc: PMC2575747pubmed: 12875303
  55. Cupp EW, Tennessen KJ, Oldland WK, Hassan HK, Hill GE, Katholi CR. Mosquito and arbovirus activity during 1997–2002 in a wetland in northeastern Mississippi. J Med Entomol 2004;41:495–501.
    doi: 10.1603/0022-2585-41.3.495pmc: PMC2581464pubmed: 15185956google scholar: lookup
  56. Molaei G, Farajollahi A, Armstrong PM, Oliver J, Howard JJ, Andreadis TG. Identification of bloodmeals in Anopheles quadrimaculatus and Anopheles punctipennis from eastern equine encephalitis virus foci in northeastern USA. Med Vet Entomol 2009;23:350–6.
  57. Schmitt SM, Cooley TM, Fitzgerald SD, Bolin SR, Lim A, Schaefer SM. An outbreak of eastern equine encephalitis virus in free-ranging white-tailed deer in Michigan. J Wildl Dis 2007;43:635–44.
    doi: 10.7589/0090-3558-43.4.635pubmed: 17984258google scholar: lookup
  58. Mutebi JP, Lubelczyk C, Eisen R, Panella N, MacMillan K, Godsey M. Using wild white-tailed deer to detect eastern equine encephalitis virus activity in Maine. Vector Borne Zoonotic Dis 2011;11:1403–9.
    doi: 10.1089/vbz.2011.0643pubmed: 21736489google scholar: lookup
  59. Berl E, Eisen RJ, MacMillan K, Swope BN, Saxton-Shaw KD, Graham AC. Serological evidence for eastern equine encephalitis virus activity in white-tailed deer, Odocoileus virginianus, in Vermont, 2010. Am J Trop Med Hyg 2013;88:103–7.
    doi: 10.4269/ajtmh.2012.12-0236pmc: PMC3541719pubmed: 23208886google scholar: lookup
  60. Tate CM, Howerth EW, Stallknecht DE, Allison AB, Fischer JR, Mead DG. Eastern equine encephalitis in a free-ranging white-tailed deer (Odocoileus virginianus). J Wildl Dis 2005;41:241–5.
    doi: 10.7589/0090-3558-41.1.241pubmed: 15827230google scholar: lookup
  61. Kiupel M, Fitzgerald SD, Pennick KE, Cooley TM, O’Brien DJ. Distribution of eastern equine encephalomyelitis viral protein and nucleic acid within central nervous tissue lesions in white-tailed deer (Odocoileus virginianus). Vet Pathol 2013;50:1058–62.
    doi: 10.1177/0300985813488956pubmed: 23686767google scholar: lookup
  62. Lord CC, Rutledge CR, Tabachnick WJ. Relationships between host viremia and vector susceptibility for arboviruses. J Med Entomol 2006;43:623–30.
    doi: 10.1093/jmedent/43.3.623pmc: PMC2814772pubmed: 16739425google scholar: lookup