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      Common Host-Derived Chemicals Increase Catches of Disease-Transmitting Mosquitoes and Can Improve Early Warning Systems for Rift Valley Fever Virus

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          Abstract

          Rift Valley fever (RVF), a mosquito-borne zoonosis, is a major public health and veterinary problem in sub-Saharan Africa. Surveillance to monitor mosquito populations during the inter-epidemic period (IEP) and viral activity in these vectors is critical to informing public health decisions for early warning and control of the disease. Using a combination of field bioassays, electrophysiological and chemical analyses we demonstrated that skin-derived aldehydes (heptanal, octanal, nonanal, decanal) common to RVF virus (RVFV) hosts including sheep, cow, donkey, goat and human serve as potent attractants for RVFV mosquito vectors. Furthermore, a blend formulated from the four aldehydes and combined with CO 2-baited CDC trap without a light bulb doubled to tripled trap captures compared to control traps baited with CO 2 alone. Our results reveal that (a) because of the commonality of the host chemical signature required for attraction, the host-vector interaction appears to favor the mosquito vector allowing it to find and opportunistically feed on a wide range of mammalian hosts of the disease, and (b) the sensitivity, specificity and superiority of this trapping system offers the potential for its wider use in surveillance programs for RVFV mosquito vectors especially during the IEP.

          Author Summary

          Enzootic transmission of arboviral diseases such as Rift Valley Fever (RVF) continues to occur at a low intensity among mosquito vectors in Kenya, which may remain undetected by most monitoring programs unless very sensitive tools are employed to detect virus activity before an outbreak occurs. Here, we report a more sensitive and mosquito-specific surveillance trapping system for RVF virus (RVFV) mosquito vectors based on mammalian-skin derived semiochemicals. We show that RVFV mosquito vectors detect similar components (heptanal, octanal, nonanal, decanal) in the skin of RVFV mammalian hosts. In field trials, each of these compounds when combined with CO 2 increased captures of these mosquito vectors in a dose-dependent manner. Additionally, a blend formulated from optimal attractive dose of each of these compounds combined with CO 2 significantly increased trap captures compared to control traps baited with CO 2 alone. The four-component blend attracted multiple mosquito vectors of the disease under field conditions suggesting that a trapping system based on this formulation offers opportunity for its use as a tool for RVFV vector surveillance.

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          Most cited references28

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          Rift Valley fever virus (family Bunyaviridae, genus Phlebovirus). Isolations from Diptera collected during an inter-epizootic period in Kenya.

          A total of 134 876 Diptera collected in Kenya during a 3-year period were tested in 3383 pools for Rift Valley fever (RVF) virus. Nineteen pools of unengorged mosquitoes were found positive for RVF. All isolations were made from specimens collected at or near the naturally or artificially flooded grassland depressions that serve as the developmental sites for the immature stages of many mosquito species. The isolation of virus from adult male and female A. lineatopennis which had been reared from field-collected larvae and pupae suggests that transovarial transmission of the virus occurs in this species.
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            An Outbreak of Rift Valley Fever in Northeastern Kenya, 1997-98

            In December 1997, 170 hemorrhagic fever-associated deaths were reported in Carissa District, Kenya. Laboratory testing identified evidence of acute Rift Valley fever virus (RVFV). Of the 171 persons enrolled in a cross-sectional study, 31(18%) were anti-RVFV immunoglobulin (Ig) M positive. An age-adjusted IgM antibody prevalence of 14% was estimated for the district. We estimate approximately 27,500 infections occurred in Garissa District, making this the largest recorded outbreak of RVFV in East Africa. In multivariate analysis, contact with sheep body fluids and sheltering livestock in one’s home were significantly associated with infection. Direct contact with animals, particularly contact with sheep body fluids, was the most important modifiable risk factor for RVFV infection. Public education during epizootics may reduce human illness and deaths associated with future outbreaks.
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              Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant.

              West Nile virus, which is transmitted by Culex mosquitoes while feeding on birds and humans, has emerged as the dominant vector borne disease in North America. We have identified natural compounds from humans and birds, which are detected with extreme sensitivity by olfactory receptor neurons (ORNs) on the antennae of Culex pipiens quinquefasciatus (Cx. quinquefasciatus). One of these semiochemicals, nonanal, dominates the odorant spectrum of pigeons, chickens, and humans from various ethnic backgrounds. We determined the specificity and sensitivity of all ORN types housed in different sensilla types on Cx. quinquefasciatus antennae. Here, we present a comprehensive map of all antennal ORNs coding natural ligands and their dose-response functions. Nonanal is detected by a large array of sensilla and is by far the most potent stimulus; thus, supporting the assumption that Cx. quinquefasciatus can smell humans and birds. Nonanal and CO(2) synergize, thus, leading to significantly higher catches of Culex mosquitoes in traps baited with binary than in those with individual lures.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                January 2013
                10 January 2013
                : 7
                : 1
                : e2007
                Affiliations
                [1 ]International Centre of Insect Physiology and Ecology ( icipe, ), Nairobi, Kenya
                [2 ]Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa
                [3 ]Centre for Virus Research, Kenya Medical Research Institute (KEMRI), Nairobi, Kenya
                [4 ]USDA/ARS-Center for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, United States of America
                DVBNTD/CWRU/Emory University, Kenya
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DPT RS BT. Performed the experiments: DPT. Analyzed the data: DPT. Contributed reagents/materials/analysis tools: DPT RS CB BT. Wrote the paper: DPT RS CLS ADSB PEAT CB BT.

                Article
                PNTD-D-12-00999
                10.1371/journal.pntd.0002007
                3542179
                23326620
                dac86f56-9403-47d5-809f-410f13ed1005
                Copyright @ 2013

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 8 August 2012
                : 29 November 2012
                Page count
                Pages: 11
                Funding
                The support through a scholarship to DPT by the German Academic Exchange Service (DAAD) is greatly acknowledged. This research was funded by Google.org, the philanthropic arm of Google. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Chemistry

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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