Analyze Diet
Parasites & vectors2014; 7; 586; doi: 10.1186/s13071-014-0586-3

Role of enhanced vector transmission of a new West Nile virus strain in an outbreak of equine disease in Australia in 2011.

Abstract: In 2011, a variant of West Nile virus Kunjin strain (WNVKUN) caused an unprecedented epidemic of neurological disease in horses in southeast Australia, resulting in almost 1,000 cases and a 9% fatality rate. We investigated whether increased fitness of the virus in the primary vector, Culex annulirostris, and another potential vector, Culex australicus, contributed to the widespread nature of the outbreak. Methods: Mosquitoes were exposed to infectious blood meals containing either the virus strain responsible for the outbreak, designated WNVKUN2011, or WNVKUN2009, a strain of low virulence that is typical of historical strains of this virus. WNVKUN infection in mosquito samples was detected using a fixed cell culture enzyme immunoassay and a WNVKUN- specific monoclonal antibody. Probit analysis was used to determine mosquito susceptibility to infection. Infection, dissemination and transmission rates for selected days post-exposure were compared using Fisher's exact test. Virus titers in bodies and saliva expectorates were compared using t-tests. Results: There were few significant differences between the two virus strains in the susceptibility of Cx. annulirostris to infection, the kinetics of virus replication and the ability of this mosquito species to transmit either strain. Both strains were transmitted by Cx. annulirostris for the first time on day 5 post-exposure. The highest transmission rates (proportion of mosquitoes with virus detected in saliva) observed were 68% for WNVKUN2011 on day 12 and 72% for WNVKUN2009 on day 14. On days 12 and 14 post-exposure, significantly more WNVKUN2011 than WNVKUN2009 was expectorated by infected mosquitoes. Infection, dissemination and transmission rates of the two strains were not significantly different in Culex australicus. However, transmission rates and the amount of virus expectorated were significantly lower in Cx. australicus than Cx. annulirostris. Conclusions: The higher amount of WNVKUN2011 expectorated by infected mosquitoes may be an indication that this virus strain is transmitted more efficiently by Cx. annulirostris compared to other WNVKUN strains. Combined with other factors, such as a convergence of abundant mosquito and wading bird populations, and mammalian and avian feeding behaviour by Cx. annulirostris, this may have contributed to the scale of the 2011 equine epidemic.
Publication Date: 2014-12-12 PubMed ID: 25499981PubMed Central: PMC4280035DOI: 10.1186/s13071-014-0586-3Google 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
  • Non-U.S. Gov't

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 study looked into the 2011 epidemic in southeast Australia caused by a variant of West Nile virus strain (WNVKUN), which affected horses, causing fatal neurological diseases. The researchers examined how the virus’s increased effectiveness within its primary vector, the mosquito species Culex annulirostris, as well as a potential vector, Culex australicus, could have contributed to the severity of the outbreak.

Research Method

  • The scientists exposed mosquitoes to infectious blood meals containing both the virus strain responsible for the outbreak (WNVKUN2011) and another version of the virus, WNVKUN2009, known for low virulence and typically found in historical instances of the disease.
  • The WNVKUN infection in the mosquito specimens was detected using enzyme immunoassay with a WNVKUN-specific monoclonal antibody.
  • To determine the vector’s susceptibility to infection, the researchers used Probit analysis. They compared the infection, dissemination, and transmission rates for selected days post-exposure using Fisher’s exact test.
  • The quantities of virus in body and saliva expectorates were compared using t-tests.

Findings

  • The researchers found no significant differences between the two strains in terms of infection susceptibility, virus replication kinetics, and transmission ability in Cx. annulirostris.
  • Both strains were first transmitted by Cx. annulirostris on the fifth day post-exposure. Transmission rates reached 68% for WNVKUN2011 on day 12 and 72% for WNVKUN2009 on day 14.
  • On days 12 and 14, infected mosquitoes expectorated significantly more WNVKUN2011 than WNVKUN2009.
  • The infection, dissemination, and transmission rates did not significantly vary between the two strains in Culex australicus. However, this species had lower transmission rates and expectorated less virus compared to Cx. annulirostris.

Conclusions and Implications

  • The higher amount of WNVKUN2011 expectorated by infected mosquitoes indicates that this strain is transmitted more efficiently by Cx. annulirostris than other WNVKUN strains.
  • This fact, combined with the abundance of mosquito and wading bird populations and their feeding behaviour on mammals and birds, could have contributed to the severity of the 2011 equine epidemic.

Cite This Article

APA
van den Hurk AF, Hall-Mendelin S, Webb CE, Tan CS, Frentiu FD, Prow NA, Hall RA. (2014). Role of enhanced vector transmission of a new West Nile virus strain in an outbreak of equine disease in Australia in 2011. Parasit Vectors, 7, 586. https://doi.org/10.1186/s13071-014-0586-3

Publication

ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 7
Pages: 586

Researcher Affiliations

van den Hurk, Andrew F
  • Virology, Public and Environmental Health, Forensic and Scientific Services, Department of Health, Queensland Government, Brisbane, QLD, Australia. andrew.vandenhurk@health.qld.gov.au.
  • Australian Infectious Disease Research Centre, School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, QLD, Australia. andrew.vandenhurk@health.qld.gov.au.
Hall-Mendelin, Sonja
  • Virology, Public and Environmental Health, Forensic and Scientific Services, Department of Health, Queensland Government, Brisbane, QLD, Australia. sonja.hall-mendelin@health.qld.gov.au.
Webb, Cameron E
  • Department of Medical Entomology, University of Sydney and Pathology West - ICPMR Westmead, Westmead, NSW, Australia. Cameron.Webb@health.nsw.gov.au.
Tan, Cindy S E
  • Australian Infectious Disease Research Centre, School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, QLD, Australia. s.tan5@uq.edu.au.
Frentiu, Francesca D
  • Institute of Health and Biomedical Innovation and School of Biomedical Sciences, Queensland University of Technology, Kelvin Grove, QLD, Australia. francesca.frentiu@qut.edu.au.
Prow, Natalie A
  • Australian Infectious Disease Research Centre, School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, QLD, Australia. n.prow@uq.edu.au.
Hall, Roy A
  • Australian Infectious Disease Research Centre, School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, QLD, Australia. roy.hall@uq.edu.au.

MeSH Terms

  • Animals
  • Australia
  • Culex / physiology
  • Culex / virology
  • Disease Outbreaks
  • Horse Diseases / epidemiology
  • Horse Diseases / transmission
  • Horse Diseases / virology
  • Horses
  • Insect Vectors / physiology
  • Insect Vectors / virology
  • West Nile Fever / epidemiology
  • West Nile Fever / transmission
  • West Nile Fever / veterinary
  • West Nile Fever / virology
  • West Nile virus / physiology

References

This article includes 44 references
  1. Kramer LD, Styer LM, Ebel GD. A global perspective on the epidemiology of West Nile virus. Ann Rev Entomol 2008;53:61–81.
  2. Petersen LR, Brault AC, Nasci RS. West Nile virus: review of the literature. JAMA 2013;310:308–315.
    doi: 10.1001/jama.2013.8042pmc: PMC4563989pubmed: 23860989google scholar: lookup
  3. Hall RA, Broom AK, Smith DW, Mackenzie JS. The ecology and epidemiology of Kunjin virus. Curr Top Microbiol Immunol 2002;267:253–269.
    pubmed: 12082993
  4. Marshall ID. Murray Valley and Kunjin Encephalitis. 1988. pp. 151–189.
  5. Roche SE, Wicks R, Garner MG, East IJ, Paskin R, Moloney BJ, Carr M, Kirkland P. Descriptive overview of the 2011 epidemic of arboviral disease in horses in Australia. Aust Vet J 2013;91:5–13.
    doi: 10.1111/avj.12018pubmed: 23356366google scholar: lookup
  6. Frost MJ, Zhang J, Edmonds JH, Prow NA, Gu X, Davis R, Hornitzky C, Arzey KE, Finlaison D, Hick P, Read A, Hobson-Peters J, May FJ, Doggett SL, Haniotis J, Russell RC, Hall RA, Khromykh AA, Kirkland PD. Characterization of virulent West Nile virus Kunjin strain, Australia, 2011. Emerg Infect Dis 2012;18:792–800.
    doi: 10.3201/eid1805.111720pmc: PMC3358055pubmed: 22516173google scholar: lookup
  7. Ostlund EN, Crom RL, Pedersen DD, Johnson DJ, Williams WO, Schmitt BJ. Equine West Nile encephalitis, United States. Emerg Infect Dis 2001;7:665–669.
    doi: 10.3201/eid0704.017412pmc: PMC2631754pubmed: 11589171google scholar: lookup
  8. Williams SA, Richards JS, Faddy HM, Leydon J, Moran R, Nicholson S, Perry F, Paskin R, Catton M, Lester R, Mackenzie JS. Low seroprevalence of Murray Valley encephalitis and Kunjin viruses in an opportunistic serosurvey, Victoria 2011. Aust N Z J Public Health 2013;37:427–433.
    doi: 10.1111/1753-6405.12113pubmed: 24090325google scholar: lookup
  9. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M. Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 2003;9:311–322.
    doi: 10.3201/eid0903.020628pmc: PMC2958552pubmed: 12643825google scholar: lookup
  10. Steele KE, Linn MJ, Shoepp RJ, Komar N, Geisbert TW, Manduca RM, Calle PP, Raphael BL, Clippinger TL, Larsen T, Smith J, Lanciotti RS, Panella NA, McNamara TS. Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York. Vet Path 2000;37:208–224.
    doi: 10.1354/vp.37-3-208pubmed: 10810985google scholar: lookup
  11. Bureau of Meteorology . Record-Breaking La Niña Events. Melbourne, Australia: Bureau of Meteorology; 2012.
  12. Doggett S, Clancy J, Haniotis J, Webb C, Russell RC, Hueston L, Dwyer DE. The New South Wales Arbovirus Surveillance and Mosquito Monitoring Program 2010–2011 Annual Report. Westmead, Australia: Department of Medical Entomology, ICPMR, Westmead Hospital; 2011.
  13. Ebel GD, Carricaburu J, Young D, Bernard KA, Kramer LD. Genetic and phenotypic variation of West Nile virus in New York, 2000–2003. Am J Trop Med Hyg 2004;71:493–500.
    pubmed: 15516648
  14. Moudy RM, Meola MA, Morin LL, Ebel GD, Kramer LD. A newly emergent genotype of west nile virus is transmitted earlier and more efficiently by Culex mosquitoes. Am J Trop Med Hyg 2007;77:365–370.
    pubmed: 17690414
  15. Savage HM, Ceianu C, Nicolescu G, Karabatsos N, Lanciotti R, Vladimirescu A, Laiv L, Ungureanu A, Romanca C, Tsai TF. Entomologic and avian investigations of an epidemic of West Nile fever in Romania in 1996, with serologic and molecular characterization of a virus isolate from mosquitoes. Am J Trop Med Hyg 1999;61:600–611.
    pubmed: 10548295
  16. Turell MJ, Dohm DJ, Sardelis MR, Oguinn ML, Andreadis TG, Blow JA. An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. J Med Entomol 2005;42:57–62.
  17. Russell RC. A review of the status and significance of the species within the Culex pipiens group in Australia. J Am Mosq Control Assoc 2012;28:24–27.
    doi: 10.2987/8756-971X-28.4s.24pubmed: 23401942google scholar: lookup
  18. Rohe D, Fall RP. A miniature battery powered CO2 baited light trap for mosquito borne encephalitis surveillance. Bull Soc Vector Ecol 1979;4:24–27.
  19. Goddard LB, Roth AE, Reisen WK, Scott TW. Vector competence of California mosquitoes for West Nile virus. Emerg Infect Dis 2002;8:1385–1391.
    doi: 10.3201/eid0812.020536pmc: PMC2738502pubmed: 12498652google scholar: lookup
  20. Aitken THG. An in vitro feeding technique for artificially demonstrating virus transmission by mosquitoes. Mosq News 1977;37:130–133.
  21. Turell MJ, Gargan TP II, Bailey CL. Replication and dissemination of Rift Valley fever virus in Culex pipiens. Am J Trop Med Hyg 1984;33:176–181.
    pubmed: 6696176
  22. Broom AK, Hall RA, Johansen CA, Oliveira N, Howard MA, Lindsay MD, Kay BH, Mackenzie JS. Identification of Australian arboviruses in inoculated cell cultures using monoclonal antibodies in ELISA. Pathology 1998;30:286–288.
    doi: 10.1080/00313029800169456pubmed: 9770194google scholar: lookup
  23. Reed LJ, Meunch H. A simple method for estimating fifty percent end points. Am J Hyg 1938;27:493–497.
  24. GraphPad Software . GraphPad Prism. Version 6. San Diego, CA: GraphPad Software, Inc; 2012.
  25. Reisen WK, Fang Y, Martinez VM. Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission. J Med Entomol 2005;42:367–375.
  26. Styer LM, Bernard KA, Kramer LD. Enhanced early West Nile virus infection in young chickens infected by mosquito bite: effect of viral dose. Am J Trop Med Hyg 2006;75:337–345.
    pubmed: 16896145
  27. VanDalen KK, Hall JS, Clark L, McLean RG, Smeraski C. West Nile virus infection in American Robins: new insights on dose response. PLoS One 2013;8:e68537.
  28. Prow NA, Setoh YX, Biron RM, Sester DP, Kim KS, Hobson-Peters J, Hall RA, Bielefeldt-Ohmann H. The West Nile-like flavivirus Koutango is highly virulent in mice due to delayed viral clearance and the induction of a poor neutralizing antibody response. J Virol 2014;88:9947–9962.
    doi: 10.1128/JVI.01304-14pmc: PMC4136322pubmed: 24942584google scholar: lookup
  29. Audsley M, Edmonds J, Liu W, Mokhonov V, Mokhonova E, Melian EB, Prow N, Hall RA, Khromykh AA. Virulence determinants between New York 99 and Kunjin strains of West Nile virus. Virology 2011;414:63–73.
    doi: 10.1016/j.virol.2011.03.008pmc: PMC3089702pubmed: 21477835google scholar: lookup
  30. Kramer LD, Ebel GD. Dynamics of flavivirus infection in mosquitoes. Adv Virus Res 2003;60:187–232.
    doi: 10.1016/S0065-3527(03)60006-0pubmed: 14689695google scholar: lookup
  31. Kay BH. Age structure of populations of Culex annulirostris (Diptera: Culicidae) at Kowanyama and Charleville, Queensland. J Med Entomol 1979;16:309–316.
    pubmed: 541806
  32. Russell RC. Population age composition and female longevity of the arbovirus vector Culex annulirostris Skuse near Echuca, Victoria, in the Murray Valley of southeastern Australia 1979–1985. Aust J Exp Biol Med Sci 1986;64:595–606.
    doi: 10.1038/icb.1986.63pubmed: 3593125google scholar: lookup
  33. Kay BH. Towards prediction and surveillance of Murray Valley encephalitis activity in Australia. Aust J Exp Biol Med Sci 1980;58:67–76.
    doi: 10.1038/icb.1980.7pubmed: 6255919google scholar: lookup
  34. Jansen CC, Webb CE, Graham GC, Craig SB, Zborowski P, Ritchie SA, Russell RC, van den Hurk AF. Blood sources of mosquitoes collected from urban and peri-urban environments in eastern Australia with species-specific molecular analysis of avian blood meals. Am J Trop Med Hyg 2009;81:849–857.
    doi: 10.4269/ajtmh.2009.09-0008pubmed: 19861621google scholar: lookup
  35. Marshall ID. Epidemiology of Murray Valley encephalitis in eastern Australia - patterns of arbovirus activity and strategies of arbovirus survival. Arbovirus Res Aust 1979;2:47–53.
  36. Kay BH, Boreham PFL, Fanning ID. Host-feeding patterns of Culex annulirostris and other mosquitoes (Diptera: Culicidae) at Charleville, southwestern Queensland, Australia. J Med Entomol 1985;22:529–535.
    pubmed: 2864452
  37. Kay BH, Boyd AM, Ryan PA, Hall RA. Mosquito feeding patterns and natural infection of vertebrates with Ross river and Barmah Forest viruses in Brisbane, Australia. Am J Trop Med Hyg 2007;76:417–423.
    pubmed: 17360861
  38. Miller BR, Monath TP, Tabachnick WJ, Ezike VI. Epidemic yellow fever caused by an incompetent mosquito vector. Trop Med Parasitol 1989;40:396–399.
    pubmed: 2623418
  39. Turell MJ, O’Guinn ML, Dohm DJ, Jones JW. Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol 2001;38:130–134.
    doi: 10.1603/0022-2585-38.2.130pubmed: 11296813google scholar: lookup
  40. Jansen CC, Webb CE, Northill JA, Ritchie SA, Russell RC, van den Hurk AF. Vector competence of Australian mosquito species for a North American strain of West Nile virus. Vector Borne Zoonotic Dis 2008;8:805–811.
    doi: 10.1089/vbz.2008.0037pubmed: 18973445google scholar: lookup
  41. Kassim NFA, Webb CE, Wang QN, Russell RC. Australian distribution, genetic status and seasonal abundance of the exotic mosquito Culex molestus (Forskal) (Diptera: Culicidae). Aust J Entomol 2013;52:185–198.
    doi: 10.1111/aen.12021google scholar: lookup
  42. Jansen CC, Ritchie SA, van den Hurk AF. The role of Australian mosquito species in the transmission of endemic and exotic West Nile virus strains. Int J Environ Res Public Health 2013;10:3735–3752.
    doi: 10.3390/ijerph10083735pmc: PMC3774466pubmed: 23965926google scholar: lookup
  43. Doggett S, Clancy J, Haniotis J, Webb C, Russell RC, Hueston L, Dwyer DE. The New South Wales Arbovirus Surveillance and Mosquito Monitoring Program 2011–2012 Annual Report. Westmead, Australia: Department of Medical Entomology, ICPMR, Westmead Hospital; 2012.
  44. Prow NA. The changing epidemiology of Kunjin virus in Australia. Int J Environ Res Public Health 2013;10:6255–6272.
    doi: 10.3390/ijerph10126255pmc: PMC3881112pubmed: 24287851google scholar: lookup