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Exploiting Mosquito Sugar Feeding to Detect Mosquito-Borne Pathogens

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Exploiting Mosquito Sugar Feeding to Detect Mosquito-Borne Pathogens Exploiting mosquito sugar feeding to detect mosquito-borne pathogens Sonja Hall-Mendelina, Scott A. Ritchieb,c, Cheryl A. Johansend, Paul Zborowskia, Giles Cortise, Scott Dandridgef, Roy A. Halla, and Andrew F. van den Hurkg,a,1 aSchool of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, Queensland 4072, Australia; bSchool of Public Health and Tropical Medicine, James Cook University, Cairns, Queensland 4870, Australia; cTropical Population Health Unit Network, Queensland Health, Cairns, Queensland 4870, Australia; dDiscipline of Microbiology and Immunology, School of Biomedical, Biomolecular and Chemical Sciences, University of Western Australia, Nedlands, Western Australia 6009, Australia; ePrivate Contracting Engineer; fThe Shire of Harvey, Australind, Western Australia 6233, Australia; and gVirology, Queensland Health Forensic and Scientific Services, Coopers Plains, Queensland 4108, Australia Edited* by Barry J. Beaty, Colorado State University, Fort Collins, CO, and approved April 29, 2010 (received for review February 22, 2010) Arthropod-borne viruses (arboviruses) represent a global public viral RNA in, mosquitoes collected with a variety of trapping health problem, with dengue viruses causing millions of infections techniques. annually, while emerging arboviruses, such as West Nile, Japanese Although these surveillance strategies provide important infor- encephalitis, and chikungunya viruses have dramatically expanded mation regarding the distribution of arboviruses, each has limita- their geographical ranges. Surveillance of arboviruses provides tions. For instance, disease surveillance systems are hampered by vital data regarding their prevalence and distribution that may a similarity of disease signs and symptoms induced by different be utilized for biosecurity measures and the implementation of pathogens, the potentially low clinical to subclinical disease ratio, disease control strategies. However, current surveillance methods and the recognition of cases only after an outbreak has com- that involve detection of virus in mosquito populations or sero- menced. The disadvantages of sentinel animals include the need conversion in vertebrate hosts are laborious, expensive, and logis- for intensive animal husbandry and risk of injury to staff bleeding tically problematic. We report a unique arbovirus surveillance animals (7). Furthermore, sentinel animals may themselves be system to detect arboviruses that exploits the process whereby amplifying hosts of the virus, thus contributing to the transmission SCIENCES mosquitoes expectorate virus in their saliva during sugar feeding. cycle, and some closely related arboviruses are difficult to In this system, infected mosquitoes captured by CO2-baited updraft distinguish using current serological tests. Finally, processing APPLIED BIOLOGICAL box traps are allowed to feed on honey-soaked nucleic acid thousands of mosquitoes for virus detection is labor-intensive, preservation cards within the trap. The cards are then analyzed especially when presorting of mosquitoes is required, and often for expectorated virus using real-time reverse transcription-PCR. requires a cold-chain to preserve viral integrity in arthropods In field trials, this system detected the presence of Ross River collected from the field (7). and Barmah Forest viruses in multiple traps deployed at two loca- Tocircumvent these issues, we developed a unique surveillance tions in Australia. Viral RNA was preserved for at least seven days strategy for the detection of arboviruses that exploits the process on the cards, allowing for long-term placement of traps and con- whereby mosquitoes expel virus in their saliva during sugar feed- tinuous collection of data documenting virus presence in mosquito ing (8, 9). In this system, mosquitoes attracted to and captured by populations. Furthermore no mosquito handling or processing was specialized traps were provided with a sugar source in the form of required and cards were conveniently shipped to the laboratory a honey-soaked card, which preserves nucleic acids. Viral RNA, overnight. The simplicity and efficacy of this approach has the expectorated from any infected mosquito, was subsequently potential to transform current approaches to vector-borne disease detected by real-time reverse-transcriptase (RT)—PCR. The surveillance by streamlining the monitoring of pathogens in vector novelty of this concept lies in the detection of viral RNA directly populations. from the cards, rather than the mosquitoes, thus eliminating the costly and time-consuming analysis of mosquitoes. Furthermore, arboviruses ∣ disease control ∣ honey ∣ saliva ∣ surveillance traps were designed to run continuously, and the cards preserved viral RNA for at least 7 d and inactivated live virus, demonstrat- rthropod-borne viruses (arboviruses) are responsible for ing the suitability of this system for surveillance in remote areas. Asignificant global morbidity and mortality, with many ree- In this paper, we describe the laboratory development and field merging or appearing in new geographic regions. The continued evaluation of the system and prove its utility in the detection of disease burden of dengue throughout the tropics, the widespread the alphaviruses, Ross River virus (RRV), Barmah Forest virus establishment of West Nile virus (WNV) in North America fol- (BFV), and CHIKV, as well as the flavivirus, WNV virus (Kunjin lowing its introduction in 1999, and the chikungunya virus subtype). (CHIKV) pandemic that afflicted nations in the western Indian Ocean, India, and Italy between 2004 and 2007 graphically illus- Results trate the impact of arboviruses on human and animal populations Detection of Viral RNA in Honey-Soaked Substrates Fed on by Infected (1, 2). The implementation of timely and effective control Mosquitoes. It was essential to use a substrate that preserved viral strategies, such as mosquito control and/or vaccination, can be RNA for at least 7 d under field conditions and rapidly inacti- highly dependent on data generated by surveillance systems. vated infectious virus to ensure integrity of the samples and then Accordingly, a number of strategies have been employed to de- tect arbovirus activity, but most are based on clinical diagnosis of Author contributions: S.H.-M., S.A.R., C.A.J., R.A.H., and A.F.v.d.H. designed research; symptoms and/or detection of the virus or virus-specific antibo- S.H.-M., P.Z., S.D., and A.F.v.d.H. performed research; S.H.-M., S.A.R., C.A.J., R.A.H., and dies in vertebrates or detection of the virus in arthropod vectors A.F.v.d.H. analyzed data; G.C. contributed new reagents/analytic tools; and S.H.-M., (3). Sentinel animals, such as chickens for WNV, St. Louis ence- S.A.R., C.A.J., R.A.H., and A.F.v.d.H. wrote the paper. phalitis virus, and Murray Valley encephalitis virus surveillance, The authors declare no conflict of interest. or pigs for Japanese encephalitis virus surveillance, are often *This Direct Submission article had a prearranged editor. deployed to provide an early warning system for an impending 1To whom correspondence should be addressed: E-mail: [email protected]. – outbreak or to detect an incursion (4 6). Virus surveillance using This article contains supporting information online at www.pnas.org/lookup/suppl/ arthropods is based on virus isolation from, or detection of doi:10.1073/pnas.1002040107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1002040107 PNAS Early Edition ∣ 1of5 Downloaded by guest on October 1, 2021 Table 1. Detection of West Nile, Ross River and chikungunya viruses on honey-baited substrates (FTA® cards or FP cards) and saliva collected from infected Cx. annulirostris and Ae. aegypti % surviving mosquitoes that % substrates had fed on % positive that had % detection Virus Substrate type positive* substrate† fed on substrate‡ in saliva§ West Nile FTA® card 83 (25∕30)60(6∕10) 100 (6∕6)90(9∕10) FP card 83 (25∕30)83(19∕23)89(17∕19) 100 (23∕23) Ross River FTA® card 90 (27∕30)56(9∕16) 100 (9∕9)69(11∕16) FP card 70 (21∕30)100(13∕13) 100 (13∕13)31(4∕13) Chikungunya FTA® card 75 (21∕28)0(0∕28)0(0∕0)52(14∕27) Mosquitoes were processed 12 days post exposure for WNV and RRV in Cx. annulirostris, and 14 days for CHIKV in Ae. aegypti. *Percentage of the total number of substrates positive for virus (number positive/number infected mosquitoes). †Percentage of surviving mosquitoes in which blue food dye was observed, indicating that the mosquito had imbibed honey from the substrate (number with blue dye/number surviving). ‡Percentage of mosquitoes that had imbibed honey from the substrate and expectorated virus (number positive/number that had imbibed the honey). §Percentage of saliva expectorates from surviving mosquitoes in which viral RNA was detected by TaqMan RT-PCR (number saliva expectorates positive/ number tested). safe handling by field staff. Flinders Technology Associates filter or WNV (P ¼ 1.000, Fisher’s exact test). The viral detection rates paper (FTA®) cards have previously been used to inactivate and in saliva expectorates collected using a standard capillary tube preserve viral RNA, including rabies viruses (10) and infectious method (12) ranged from 31% to 100% and were not significantly bursal disease virus (11). Preliminary experiments demonstrated different from the detection rates for either of the honey-soaked that both honey-soaked FTA® cards and untreated filter paper substrates (P>0.05, Fisher’s exact test), except in the case of (FP) cards were able to bind RRV RNA and preserve it at 23 °C RRV from the FP cards (P ¼ 0.022, Fisher’s exact test). for at least 28 d (Table S1). Furthermore, the FTA® cards inac- Interestingly, in some cases, virus was detected on the tivated both RRVand WNVon contact, while infectious virus was ≤6 honey-baited substrates, although there was no evidence that still present on the FP cards hr post inoculation (SI Text). the mosquito had imbibed any of the honey (i.e., blue color The ability to detect viral RNA expectorated on these honey- was not observed in the mosquito). This was particularly evident soaked substrates by individual infected mosquitoes was assessed.
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