NONVIREMIC TRANSMISSION OF WEST NILE VIRUS: EVALUATION OF THE EFFECTS OF SPACE, TIME, AND MOSQUITO SPECIES

CHARLES E. McGEE Department of Pathology, University of Texas Medical Branch, Galveston, Texas

Search for other papers by CHARLES E. McGEE in
Current site
Google Scholar
PubMed
Close
,
BRADLEY S. SCHNEIDER Department of Pathology, University of Texas Medical Branch, Galveston, Texas

Search for other papers by BRADLEY S. SCHNEIDER in
Current site
Google Scholar
PubMed
Close
,
YVETTE A. GIRARD Department of Pathology, University of Texas Medical Branch, Galveston, Texas

Search for other papers by YVETTE A. GIRARD in
Current site
Google Scholar
PubMed
Close
,
DANA L. VANLANDINGHAM Department of Pathology, University of Texas Medical Branch, Galveston, Texas

Search for other papers by DANA L. VANLANDINGHAM in
Current site
Google Scholar
PubMed
Close
, and
STEPHEN HIGGS Department of Pathology, University of Texas Medical Branch, Galveston, Texas

Search for other papers by STEPHEN HIGGS in
Current site
Google Scholar
PubMed
Close
Restricted access

To evaluate the potential for nonviremic transmission (NVT) of West Nile virus (WNV) to occur in nature, we examined the effect of increasing spatial and temporal separation between co-feeding mosquitoes on the efficiency of nonviremic transmission and the potential of a West Nile virus bridge vector species, Aedes albopictus, to be infected via nonviremic transmission. West Nile virus-infected (donor) Culex pipiens quinquefasciatus were allowed to feed on a mouse for 5 minutes followed by non-infected (recipient) mosquitoes with increasing spatial (0, 10, 20, 30, 40, or 50 mm) or temporal (0, 15, 30, 45, or 60 min) separation from the site or time of donor feeding, respectively. Recipients became infected when feeding up to 40 mm from the donor and up to 45 minutes after donor feeding. Additionally, nonviremic transmission of West Nile virus from Cx. p. quinquefasciatus to Ae. albopictus was observed.

Author Notes

  • 1

    Apperson CS, Hassan HK, Harrison BA, Savage HM, Aspen SE, Farajollahi A, Crans W, Daniels TJ, Falco RC, Benedict M, Anderson M, McMillen L, Unnasch TR, 2004. Host feeding patterns of established and potential mosquito vectors of West Nile virus in the eastern United States. Vector-Borne Zoonotic Dis 4 :71–82.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Higgs S, Snow K, Gould EA, 2004. The potential for West Nile virus to establish outside of its natural range: a consideration of potential mosquito vectors in the United Kingdom. Trans R Soc Trop Med Hyg 98 :82–87.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Hubalek Z, Halouzka J, 1999. West Nile fever–a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis 5 :643–650.

  • 4

    Lillibridge KM, Parsons R, Randle Y, Travassos da Rosa AP, Guzman H, Siirin M, Wuithiranyagool T, Hailey C, Higgs S, Bala AA, Pascua R, Meyer T, Vanlandingham DL, Tesh RB, 2004. The 2002 introduction of West Nile virus into Harris County, Texas, an area historically endemic for St. Louis encephalitis. Am J Trop Med Hyg 70 :676–681.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Dohm DJ, Sardelis MR, Turell MJ, 2002. Experimental vertical transmission of West Nile virus by Culex pipiens (Diptera: Culicidae). J Med Entomol 39 :640–644.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Hribar LJ, Vlach JJ, Demay DJ, Stark LM, Stoner RL, Godsey MS, Burkhalter KL, Spoto MC, James SS, Smith JM, Fussell EM, 2003. Mosquitoes infected with West Nile virus in the Florida Keys, Monroe County, Florida, USA. J Med Entomol 40 :361–363.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Sardelis MR, Turell MJ, 2001. Ochlerotatus j. japonicus in Frederick County, Maryland: discovery, distribution, and vector competence for West Nile virus. J Am Mosq Control Assoc 17 :137–141.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Turell MJ, Dohm DJ, Sardelis MR, Oguinn ML, Andreadis TG, Blow JA, 2005. An update on the potential of north American mosquitoes (Diptera: Culicidae) to transmit West Nile Virus. J Med Entomol 42 :57–62.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Turell MJ, O’Guinn M, Oliver J, 2000. Potential for New York mosquitoes to transmit West Nile virus. Am J Trop Med Hyg 62 :413–414.

  • 10

    Turell MJ, O’Guinn ML, Dohm DJ, Jones JW, 2001. Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol 38 :130–134.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Turell MJ, O’Guinn ML, Dohm DJ, Webb JP Jr, Sardelis MR, 2002. Vector competence of Culex tarsalis from Orange County, California, for West Nile virus. Vector-Borne Zoonotic Dis 2 :193–196.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Harrison BA, Turell MJ, O’Guinn ML, Sardelis MR, Dohm DJ, 2000. Preparing for West Nile virus and multidirectional surveillance and control. Wing Beats Winter 2000 :14–15.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Granwehr BP, Lillibridge KM, Higgs S, Mason PW, Aronson JF, Campbell GA, Barrett AD, 2004. West Nile virus: where are we now? Lancet Infect Dis 4 :547–556.

  • 14

    Lord CC, Higgs S, Tabachnick WJ, 2005. The impact of non-systemic transmission on arbovirus epidemiology. 54th Annual Meeting of the American Society for Tropical Medicine and Hygiene: 158.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Higgs S, Schneider BS, Vanlandingham DL, Klingler KA, Gould EA, 2005. Nonviremic transmission of West Nile virus. Proc Natl Acad Sci USA 102 :8871–8874.

  • 16

    Risi GF, 2006. Nonviremic transmission of West Nile virus: a novel observation with significant potential implications. Contagion 3 :98–100.

  • 17

    Jones LD, Davies CR, Steele GM, Nuttall PA, 1987. A novel mode of arbovirus transmission involving a nonviremic host. Science 237 :775–777.

  • 18

    Jones LD, Gaunt M, Hails RS, Laurenson K, Hudson PJ, Reid H, Henbest P, Gould EA, 1997. Transmission of louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Med Vet Entomol 11 :172–176.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Nuttall LDJaPA, 1990. The effect of host resistance to tick infestation on the trasnmission of thogoto virus by ticks. J Gen Virol 71 :1039–1043.

  • 20

    Labuda M, Austyn JM, Zuffova E, Kozuch O, Fuchsberger N, Lysy J, Nuttall PA, 1996. Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology 219 :357–366.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Labuda M, Jones LD, Williams T, Danielova V, Nuttall PA, 1993. Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. J Med Entomol 30 :295–299.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Labuda M, Kozuch O, Zuffova E, Eleckova E, Hails RS, Nuttall PA, 1997. Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235 :138–143.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Patrican LA, 1997. Acquisition of Lyme disease spirochetes by cofeeding Ixodes scapularis ticks. Am J Trop Med Hyg 57 :589–593.

  • 24

    Lawrie CH, Uzcategui NY, Gould EA, Nuttall PA, 2004. Ixodid and argasid tick species and West Nile virus. Emerg Infect Dis 10 :653–657.

  • 25

    Mead DG, Ramberg FB, Besselsen DG, Mare CJ, 2000. Transmission of vesicular stomatitis virus from infected to noninfected black flies co-feeding on nonviremic deer mice. Science 287 :485–487.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Randolph SE, Miklisova D, Lysy J, Rogers DJ, Labuda M, 1999. Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118 :177–186.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Lord CC, Tabachnick WJ, 2002. Influence of nonsystemic transmission on the epidemiology of insect borne arboviruses: a case study of vesicular stomatitis epidemiology in the western United States. J Med Entomol 39 :417–426.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Jones LD, Nuttall PA, 1989. Non-viraemic transmission of Thogoto virus: influence of time and distance. Trans R Soc Trop Med Hyg 83 :712–714.

  • 29

    Girard YA, Klingler KA, Higgs S, 2004. West Nile virus dissemination and tissue tropisms in orally infected Culex pipiens quinquefasciatus. Vector-Borne Zoonotic Dis 4 :109–122.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Girard YA, Popov V, Wen J, Han V, Higgs S, 2005. Ultrastructural study of West Nile virus pathogenesis in Culex pipiens quin-quefasciatus (Diptera: Culicidae). J Med Entomol 42 :429–444.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Vanlandingham DL, Schneider BS, Klingler K, Fair J, Beasley D, Huang J, Hamilton P, Higgs S, 2004. Real-time reverse transcriptase-polymerase chain reaction quantification of West Nile virus transmitted by Culex pipiens quinquefasciatus. Am J Trop Med Hyg 71 :120–123.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Beasley DW, Davis CT, Guzman H, Vanlandingham DL, Travassos da Rosa AP, Parsons RE, Higgs S, Tesh RB, Barrett AD, 2003. Limited evolution of West Nile virus has occurred during its southwesterly spread in the United States. Virology 309 :190–195.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Higgs S, Olson KE, Kamrud KI, Powers AM, Beaty BJ, 1997. Viral expression systems and viral infections in insects. Crampton JM, Beard CB, Louis C (ed). The Molecular Biology of Disease Vectors: A Methods Manual. UK: Chapman and Hall, 459–484.

    • PubMed
    • Export Citation
  • 34

    Karber G, 1931. Bietrag zur Kllktiven Behandlung Pharmakologischer Reiheversuche. Arch Exp Pathol Pharmakol 162 :480–483.

  • 35

    Reno HE, Novak RJ, 2005. Characterization of apyrase-like activity in Ochlerotatus triseriatus, Ochlerotatus hendersoni, and Aedes aegypti.Am J Trop Med Hyg 73 :541–545.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Girard YA, Schneider BS, McGee CE, Wen J, Han VC, Popov V, Mason PW, Higgs S, 2006. Salivary gland morphology and virus transmission during long-term cytopathologic West Nile virus infection in Culex mosquitoes. Am J Trop Med Hyg 76 :118–128.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Styer LM, Bernard KA, Kramer LD, 2006. Enhanced early West Nile virus infection in young chickens infected by mosquito bite: effect of viral dose. Am J Trop Med Hyg 75 :337–345.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Mahmood F, Fang Y, Chiles RE, Reisen WK, 2004. Methods for studying the vector competence of Culex tarsalis for western equine encephalomyelitis virus. J Am Mosq Control Assoc 20 :277–282.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Weaver SC, Lorenz LH, Scott TW, 1993. Distribution of western equine encephalomyelitis virus in the alimentary tract of Culex tarsalis (Diptera: Culicidae) following natural and artificial blood meals. J Med Entomol 30 :391–397.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Lord CC, Rutledge CR, Tabachnick WJ, 2006. Relationships between host viremia and vector susceptibility for arboviruses. J Med Entomol 43 :623–630.

  • 41

    Whitfield SG, Murphy FA, Sudia WD, 1973. St. Louis encephalitis virus: an ultrastructural study of infection in a mosquito vector. Virology 56 :70–87.

  • 42

    Komar N, 2003. West Nile virus: epidemiology and ecology in North America. Adv Virus Res 61 :185–234.

  • 43

    Reisen WK, Fang Y, Martinez VM, 2005. Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission. J Med Entomol 42 :367–375.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Apperson CS, Harrison BA, Unnasch TR, Hassan HK, Irby WS, Savage HM, Aspen SE, Watson DW, Rueda LM, Engber BR, Nasci RS, 2002. Host-feeding habits of Culex and other mosquitoes (Diptera: Culicidae) in the Borough of Queens in New York City, with characters and techniques for identification of Culex mosquitoes. J Med Entomol 39 :777–785.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR, 2006. Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerg Infect Dis 12 :468–474.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P, 2006. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol 4 :e82.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Condotta SA, Hunter FF, Bidochka MJ, 2004. West Nile virus infection rates in pooled and individual mosquito samples. Vector-Borne Zoonotic Dis 4 :198–203.

Past two years Past Year Past 30 Days
Abstract Views 46 46 5
Full Text Views 340 14 0
PDF Downloads 66 8 0
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save