Spatial repellents: from discovery and development to evidence-based validation

Nicole L Achee, Michael J Bangs, Robert Farlow, Gerry F Killeen, Steve Lindsay, James G Logan, Sarah J Moore, Mark Rowland, Kevin Sweeney, Steve J Torr, Laurence J Zwiebel, John P Grieco, Nicole L Achee, Michael J Bangs, Robert Farlow, Gerry F Killeen, Steve Lindsay, James G Logan, Sarah J Moore, Mark Rowland, Kevin Sweeney, Steve J Torr, Laurence J Zwiebel, John P Grieco

Abstract

International public health workers are challenged by a burden of arthropod-borne disease that remains elevated despite best efforts in control programmes. With this challenge comes the opportunity to develop novel vector control paradigms to guide product development and programme implementation. The role of vector behaviour modification in disease control was first highlighted several decades ago but has received limited attention within the public health community. This paper presents current evidence highlighting the value of sub-lethal agents, specifically spatial repellents, and their use in global health, and identifies the primary challenges towards establishing a clearly defined and recommended role for spatial repellent products in disease control.

Figures

Figure 1
Figure 1
The general concept of spatial repellency is clear: to prevent an arthropod from entering a space occupied by a potential human host to reduce encounters between humans and vectors thereby eliminating or reducing the probability (risk) of pathogen transmission to either insect or human.
Figure 2
Figure 2
The fundamental choice between killing mosquitoes and deterring them: mosquitoes that abort attacks on humans because of sub-toxic exposure are, by definition, not exposed to toxic levels that kill them (Killeen GF and Moore SJ with permission).
Figure 3
Figure 3
An outdoor role for spatial repellents? Mathematical models show that the best strategy for application of spatial repellents depends on the vector. Indoors and outdoors use is best for those vectors least susceptible to LLINs/IRS, while use of spatial repellents outdoors is best to complement LLINs/IRS in areas where vectors feed indoors on humans (Killeen, GF and Moore, SJ with permission).

References

    1. WHO [World Health Organization] World malaria report. , ; 2008. .
    1. WHO [World Health Organization] Dengue and dengue haemorrhagic fever. 2009. .
    1. WHO [World Health Organization] WHO recommended insecticides for indoor residual spraying against malaria vectors. 2009a. .
    1. WHO [World Health Organization] WHO recommended insecticide products treatment of mosquito nets for malaria vector control. 2009b. .
    1. Hemingway J, Beaty BJ, Rowland M, Scott TW, Sharp BL. The Innovative Vector Control Consortium: improved control of mosquito-borne diseases. Trends Parasitol. 2006;22:308–312. doi: 10.1016/j.pt.2006.05.003.
    1. N’Guessan R, Corbel V, Bonnet J, Yates A, Asidi A, Boko P, Odjo A, Akogbeto M, Rowland M. Evaluation of indoxacarb, an oxadiazine insecticide for the control of pyrethroid resistant Anopheles gambiae s.s. (Diptera: Culicidae) J Med Entomol. 2007;44:270–276. doi: 10.1603/0022-2585(2007)44[270:EOIAOI];2.
    1. N’Guessan R, Boko P, Odjo A, Knols B, Akogbeto M, Rowland M. Control of pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus mosquitoes with chlorfenapyr in Benin. Trop Med Int Health. 2009;14:389–395. doi: 10.1111/j.1365-3156.2009.02245.x.
    1. WHO [World Health Organization] Report of the informal consultation on the evaluation and testing of insecticides. 1996. .
    1. Muirhead-Thomson RC. Mosquito behavior in relation to malaria transmission and control in the tropics. Edward Arnold and Co., London; 1953.
    1. Gabaldon A. The nation-wide campaign against malaria in Venezuela: Part II. Trans R Soc Trop Med Hyg. 1949;43:133–164.
    1. Gabaldon A. The effect of DDT on the population of anopheline vectors in Venezuela. Riv Parasitol. 1952;8:24–41.
    1. Kennedy JS. The excitant and repellent effects on mosquitoes of sublethal contacts with DDT. Bull Entomol Res. 1947;37:593–607. doi: 10.1017/S0007485300030091.
    1. De Zulueta J, Cullen JR. Deterrent effect of insecticides on malaria vectors. Nature. 1963;200:860–861. doi: 10.1038/200860a0.
    1. Smith A, Webley DJ. A verandah trap for studying the house-frequenting habits of mosquitoes and for assessing insecticides. Part 3. The effect of DDT on behavior and mortality. Bull Entomol Res. 1969;59:33–46. doi: 10.1017/S000748530000300X.
    1. Grieco JP, Achee NL, Andre RG, Roberts DR. A comparison study of house entering and exiting behavior of Anopheles vestitipennis using experimental huts sprayed with DDT or deltamethrin in the southern district of Toledo, Belize, C.A. J Vector Ecol. 2000;25:62–73.
    1. Grieco JP, Achee NL, Chareonviriyaphap T, Suwonkerd W, Chauhan K, Sardelis MR, Roberts DR. A new classification system for the actions of IRS chemicals traditionally used for malaria control. PLoS One. 2007;2:e716. doi: 10.1371/journal.pone.0000716.
    1. Roberts DR. DDT and house spraying and re-emerging malaria. Lancet. 2000;356:330–332. doi: 10.1016/S0140-6736(00)02516-2.
    1. Roberts DR, Alecrim WD, Hshieh P, Grieco JP, Bangs M, Andre RG, Chareonviriyaphap T. A probability model of vector behavior: effects of DDT repellency, irritancy, and toxicity in malaria control. J Vector Ecol. 2000;25:48–61.
    1. Killeen GF, Smith TA. Exploring the contributions of bed nets, cattle, insecticides and excitorepellency to malaria control: a deterministic model of mosquito host-seeking behaviour and mortality. Trans R Soc Trop Med Hyg. 2007;101:867–880. doi: 10.1016/j.trstmh.2007.04.022.
    1. Lindsay SW, Emerson PM, Charlwood JD. Reducing malaria by mosquito-proofing houses. Trends Parasitol. 2002;18:510–514. doi: 10.1016/S1471-4922(02)02382-6.
    1. Ogoma SB, Lweitoijera DW, Ngonyani H, Furer B, Russell TL, Mukabana WR, Killeen GF, Moore SJ. Screening mosquito house entry points as a potential method for integrated control of endophagic filariasis, arbovirus and malaria vectors. PLoS Negl Trop Dis. 2010;4(8):e773. doi: 10.1371/journal.pntd.0000773.
    1. Hill N, Lenglet A, Arnez AM, Carneiro I. Plant based insect repellent and insecticide treated bed nets to protect against malaria in areas of early evening biting vectors: double blind randomized placebo controlled clinical trial in the Bolivian Amazon. BMJ. 2007;335:1023. doi: 10.1136/bmj.39356.574641.55.
    1. Cook S, Khan ZR, Pickett JA. The use of push-pull strategies in integrated pest management. Ann Rev Entomol. 2007;52:375–400. doi: 10.1146/annurev.ento.52.110405.091407.
    1. The “Repellent and Consumer Product” working group of the Vector Control Consultation Workshop held in Seattle, WA July 2008 organized by the Bill & Melinda Gates Foundation; The “Identification of Current Spatial Repellent Research” meeting held in New Orleans, LA at the 2008 ASTMH conference; The “Outlining Behavioral Terminology Related to Spatial Repellency Research” meeting held in New Orleans, LA at the 2009 AMCA conference; and the “Advancing Repellents to Recommendation (ARR)” meeting held in London, UK at the London School of Tropical Health and Medicine May 2009
    1. WHOPES [World Health Organization Pesticide Evaluation Scheme]
    1. White GW. In: Insect Repellents. Debboun M, Frances SP, Strickman D, editor. CRC Press, Boca Rotan; 2007. Terminology of Insect Repellents; pp. 31–46.
    1. Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, Bousema T, Drakeley CJ, Ferguson NM, Basáñez MG, Ghani AC. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 2010;7:e1000324. doi: 10.1371/journal.pmed.1000324.
    1. Hao H, Wei J, Dai J, Du J. Host-seeking and blood-feeding behavior of Aedes albopictus (Diptera: Culcidae) exposed to vapors of geraniol, citral, citronellal, eugenol or anisaldehyde. J Med Entomol. 2008;45:533–539. doi: 10.1603/0022-2585(2008)45[533:HABBOA];2.
    1. Roberts DR, Tren R. The Excellent Powder, DDT’s Political and Scientific History. DogEar Publishing, Indianapolis, IN; 2010.
    1. WHO [World Health Organization] The use of DDT in malaria vector control. 2007. .
    1. Sharma SN, Shukla RP, Raghavendra K, Subbarao SK. Impact of DDT spraying on malaria transmission in Bareilly District, Uttar Pradesh, India. J Vect Borne Dis. 2005;42:54–60.
    1. Boston Consulting Group. Market assessment for public health pesticide products. 2006.
    1. Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D, Killeen G. Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010;7:e1000303. doi: 10.1371/journal.pmed.1000303.
    1. Govella NJ, Okumu FO, Killeen G. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. AmJTrop Med Hyg. 2010;82:415–419.
    1. Russell T, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80. doi: 10.1186/1475-2875-10-80.
    1. Liu C, Pitts RJ, Bohbot JD, Jones PL, Wang G, Zwiebel LJ. Distinct olfactory signaling mechanisms in the malaria vector mosquito Anopheles gambiae. PLoS Biol. 2010;8:e1000467. doi: 10.1371/journal.pbio.1000467.
    1. Logan JG, Birkett MA, Clark SJ, Powers S, Seal NJ, Wadhams LJ, Mordue AJ, Pickett JA. Identification of human-derived volatile chemicals that interfere with attraction of Aedes aegypti mosquitoes. J Chem Ecol. 2008;34:308–322. doi: 10.1007/s10886-008-9436-0.
    1. Pickett JA, Birkett MA, Logan JG. DEET repels ORNery? Mosquitoes. Proc Natl Acad Sci USA. 2008;105:12195–13196.
    1. Syed Z, Leal W. Mosquitoes smell and avoid the insect repellent DEET. Proc Natl Acad Sci USA. 2008;105:13195–13196. doi: 10.1073/pnas.0807167105.
    1. Ditzen M, Pellegrino M, Vosshall LB. Insect odorant receptors are molecular targets of the insect repellent DEET. Science. 2008;319:1838–1842. doi: 10.1126/science.1153121.
    1. Stanczyk NM, Brookfield JFY, Ignell R, Logan JG, Field LM. Behavioural insensitivity to DEET in Ae. aegypti: a genetically determined trait residing in changes in sensillum function. Proc Natl Acad Sci USA. 2010;42:8575–8580.
    1. Torr SJ, Mangwiro TNC, Hall DR. Shoo fly, don’t bother me! Efficacy of traditional methods of protecting cattle from tsetse. Med Vet Entomol. 2011;25:192–201. doi: 10.1111/j.1365-2915.2010.00942.x.
    1. Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C. et al.A Research Agenda to Underpin Malaria Eradication. PLoS Med. 2010;8(1):e1000406. doi: 10.1371/journal.pmed.1000406.

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다