Using evolution to generate sustainable malaria control with spatial repellents

eLife

Volumn 5, Issue OCTOBER2016, 2016, Pages

  Lynch, Penelope Anne ^a   Boots, Mike ^a,b  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSECT REPELLENT; INSECTICIDE;

ARTICLE; DISEASE TRANSMISSION; GENE FREQUENCY; HUMAN; INFECTION CONTROL; MALARIA; MALARIA CONTROL; MATHEMATICAL ANALYSIS; NONHUMAN; PHENOTYPE; PLASMODIUM MALARIAE; PREVALENCE; PUBLIC HEALTH; MOSQUITO CONTROL; PREVENTION AND CONTROL; PROCEDURES; TRANSMISSION;

DISEASE TRANSMISSION, INFECTIOUS; HUMANS; INSECT REPELLENTS; INSECTICIDES; MALARIA; MOSQUITO CONTROL;

EID: 84992700331     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15416     Document Type: Article

References (76)

1. Abiy E, Gebre-Michael T, Balkew M, Medhin G. 2015. Repellent efficacy of DEET, MyggA, neem (Azedirachta indica) oil and chinaberry (Melia azedarach) oil against Anopheles arabiensis, the principal malaria vector in Ethiopia. Malaria Journal 14:187. doi: 10.1186/s12936-015-0705-4
2. Achee NL, Bangs MJ, Farlow R, Killeen GF, Lindsay S, Logan JG, Moore SJ, Rowland M, Sweeney K, Torr SJ, Zwiebel LJ, Grieco JP. 2012. Spatial repellents: from discovery and development to evidence-based validation. Malaria Journal 11:164. doi: 10.1186/1475-2875-11-164
3. Asidi A, N’Guessan R, Akogbeto M, Curtis C, Rowland M. 2012. Loss of household protection from use of insecticide-treated nets against pyrethroid-resistant mosquitoes, benin. Emerging Infectious Diseases 18:1101-1106. doi: 10.3201/eid1807.120218
4. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI. 2013. The global distribution and burden of dengue. Nature 496:504-507. doi: 10.1038/nature12060
5. Boots M. 2015. The need for evolutionarily rational disease interventions: vaccination can select for higher virulence. PLoS Biology 13:e1002236. doi: 10.1371/journal.pbio.1002236
6. Bradley J, Matias A, Schwabe C, Vargas D, Monti F, Nseng G, Kleinschmidt I. 2012. Increased risks of malaria due to limited residual life of insecticide and outdoor biting versus protection by combined use of nets and indoor residual spraying on Bioko Island, Equatorial Guinea. Malaria Journal 11:242. doi: 10.1186/1475-2875-11-242
7. Brogdon WG, McAllister JC. 1998. Insecticide resistance and vector control. Emerging Infectious Diseases 4:605. doi: 10.3201/eid0404.980410
8. Castillo-Chavez C, Levin SA, Gould F. 1988. Physiological and behavioral adaptation to varying environments: a mathematical model. Evolution 42:986-994. doi: 10.2307/2408914
9. Chandre F, Darrier F, Manga L, Akogbeto M, Faye O, Mouchet J, Guillet P. 1999. Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bulletin of the World Health Organization 77:230-234.
10. Chandre F, Darriet F, Duchon S, Finot L, Manguin S, Carnevale P, Guillet P. 2000. Modifications of pyrethroid effects associated with kdr mutation in Anopheles gambiae. Medical and Veterinary Entomology 14:81-88. doi: 10.1046/j.1365-2915.2000.00212.x
11. Cooke MK, Kahindi SC, Oriango RM, Owaga C, Ayoma E, Mabuka D, Nyangau D, Abel L, Atieno E, Awuor S, Drakeley C, Cox J, Stevenson J. 2015. ‘A bite before bed’: exposure to malaria vectors outside the times of net use in the highlands of western Kenya. Malaria Journal 14:1-15. doi: 10.1186/s12936-015-0766-4
12. Curtis CF. 2002. Restoration of malaria control in the Madagascar highlands by DDT spraying. The American Journal of Tropical Medicine and Hygiene 66:1.
13. Dabiré RK, Namountougou M, Sawadogo SP, Yaro LB, Toé HK, Ouari A, Gouagna LC, Simard F, Chandre F, Baldet T, Bass C, Diabaté A. 2012. Population dynamics of Anopheles gambiae s.l. in Bobo-Dioulasso city: bionomics, infection rate and susceptibility to insecticides. Parasites & Vectors 5:127. doi: 10.1186/1756-3305-5-127
14. Evans RG. 1993. Laboratory evaluation of the irritancy of bendiocarb, lambda-cyhalothrin and DDT to Anopheles gambiae. Journal of the American Mosquito Control Association 9:285-293.
15. Fang W, Azimzadeh P, St Leger RJ. 2012. Strain improvement of fungal insecticides for controlling insect pests and vector-borne diseases. Current Opinion in Microbiology 15:232-238. doi: 10.1016/j.mib.2011.12.012
16. Faulde MK, Albiez G, Nehring O. 2010. Insecticidal, acaricidal and repellent effects of DEET- and IR3535-impregnated bed nets using a novel long-lasting polymer-coating technique. Parasitology Research 106:957-965. doi: 10.1007/s00436-010-1749-6
17. Gatton ML, Chitnis N, Churcher T, Donnelly MJ, Ghani AC, Godfray HCJ, Gould F, Hastings I, Marshall J, Ranson H, Rowland M, Shaman J, Lindsay SW. 2013. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution 67:1218-1230. doi: 10.1111/evo.12063
18. Gautret P, Motard A. 1999. Periodic infectivity of Plasmodium gametocytes to the vector. A review. Parasite 6: 103-111. doi: 10.1051/parasite/1999062103
19. Georghiou GP, Taylor CE. 1977. Genetic and biological influences in the evolution of insecticide resistance. Journal of Economic Entomology 70:319-323. doi: 10.1093/jee/70.3.319
20. Gould F. 1984. Role of behavior in the evolution of insect adaptation to insecticides and resistant host plants. Bulletin of the Entomological Society of America 30:34-41. doi: 10.1093/besa/30.4.34
21. Govella NJ, Ogoma SB, Paliga J, Chaki PP, Killeen G. 2015. Impregnating hessian strips with the volatile pyrethroid transfluthrin prevents outdoor exposure to vectors of malaria and lymphatic filariasis in urban Dar es Salaam, Tanzania. Parasites & Vectors 8:1-9. doi: 10.1186/s13071-015-0937-8
22. Grieco JP, Achee NL, Andre RG, Roberts DR. 2000. A comparison study of house entering and exiting behavior of Anopheles vestitipennis (Diptera: Culicidae) using experimental huts sprayed with DDT or deltamethrin in the southern district of Toledo, Belize, C.A. Journal of Vector Ecology 25:62-73.
23. Grieco JP, Achee NL, Chareonviriyaphap T, Suwonkerd W, Chauhan K, Sardelis MR, Roberts DR. 2007. A new classification system for the actions of IRS chemicals traditionally used for malaria control. PLoS One 2:e716. doi: 10.1371/journal.pone.0000716
24. Hemingway J, Field L, Vontas J. 2002. An overview of insecticide resistance. Science 298:96-97. doi: 10.1126/science.1078052
25. Hemingway J, Ranson H. 2000. Insecticide resistance in insect vectors of human disease. Annual Review of Entomology 45:371-391. doi: 10.1146/annurev.ento.45.1.371
26. Jones CM, Machin C, Mohammed K, Majambere S, Ali AS, Khatib BO, McHa J, Ranson H, Kelly-Hope LA. 2012. Insecticide resistance in Culex quinquefasciatus from Zanzibar: implications for vector control programmes. Parasites & Vectors 5:78. doi: 10.1186/1756-3305-5-78
27. Jongsma MA, Gould F, Legros M, Yang L, van Loon JJA, Dicke M. 2010. Insect oviposition behavior affects the evolution of adaptation to Bt crops: consequences for refuge policies. Evolutionary Ecology 24:1017-1030. doi: 10.1007/s10682-010-9368-3
28. Kennedy GG, Gould F, Deponti OMB, Stinner RE. 1987. Ecological, agricultural, genetic, and commercial considerations in the deployment of insect-resistant germplasm. Environmental Entomology 16:327-338. doi: 10.1093/ee/16.2.327
29. Kennedy JS. 1947. The excitant and repellent effects on mosquitos of sub-lethal contacts with DDT. Bulletin of Entomological Research 37:593-607. doi: 10.1017/S0007485300030091
30. Killeen GF, Chitnis N, Moore SJ, Okumu FO. 2011. Target product profile choices for intra-domiciliary malaria vector control pesticide products: repel or kill? Malaria Journal 10:207. doi: 10.1186/1475-2875-10-207
31. Le Menach A, Takala S, McKenzie FE, Perisse A, Harris A, Flahault A, Smith DL. 2007. An elaborated feeding cycle model for reductions in vectorial capacity of night-biting mosquitoes by insecticide-treated nets. Malaria Journal 6:10. doi: 10.1186/1475-2875-6-10
32. Lefèvre T, Gouagna LC, Dabiré KR, Elguero E, Fontenille D, Renaud F, Costantini C, Thomas F. 2009. Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. American Journal of Tropical Medicine and Hygiene 81:1023-1029. doi: 10.4269/ajtmh.2009.09-0124
33. Licciardi S, Herve JP, Darriet F, Hougard JM, Corbel V. 2006. Lethal and behavioural effects of three synthetic repellents (DEET, IR3535 and KBR 3023) on Aedes aegypti mosquitoes in laboratory assays. Medical and Veterinary Entomology 20:288-293. doi: 10.1111/j.1365-2915.2006.00630.x
34. Loyola EG, Rodríguez MH, González L, Arredondo JI, Bown DN, Vaca MA. 1990. Effect of indoor residual spraying of DDT and bendiocarb on the feeding patterns of Anopheles pseudopunctipennis in Mexico. Journal of the American Mosquito Control Association 6:635-640.
35. Lynch PA, Grimm U, Thomas MB, Read AF. 2012. Prospective malaria control using entomopathogenic fungi: comparative evaluation of impact on transmission and selection for resistance. Malaria Journal 11:383. doi: 10.1186/1475-2875-11-383
36. Malima RC, Oxborough RM, Tungu PK, Maxwell C, Lyimo I, Mwingira V, Mosha FW, Matowo J, Magesa SM, Rowland MW. 2009. Behavioural and insecticidal effects of organophosphate-, carbamate- and pyrethroid-treated mosquito nets against African malaria vectors. Medical and Veterinary Entomology 23:317-325. doi: 10.1111/j.1365-2915.2009.00837.x
37. Mandal S, Sarkar RR, Sinha S. 2011. Mathematical models of malaria-a review. Malaria Journal 10:202. doi: 10.1186/1475-2875-10-202
38. Menger DJ, Omusula P, Wouters K, Oketch C, Carreira AS, Durka M, Derycke JL, Loy DE, Hahn BH, Mukabana WR, Mweresa CK, van Loon JJ, Takken W, Hiscox A. 2016. Eave screening and push-pull tactics to reduce house entry by vectors of malaria. American Journal of Tropical Medicine and Hygiene 94:868-878. doi: 10.4269/ajtmh.15-0632
39. Mideo N, Reece SE, Smith AL, Metcalf CJ. 2013. The Cinderella syndrome: why do malaria-infected cells burst at midnight? Trends in Parasitology 29:10-16. doi: 10.1016/j.pt.2012.10.006
40. Miller JR, Siegert PY, Amimo FA, Walker ED. 2009. Designation of chemicals in terms of the locomotor responses they elicit from insects: an update of Dethier et al. (1960). Journal of Economic Entomology 102: 2056-2060. doi: 10.1603/029.102.0606
41. Mnyone LL, Koenraadt CJ, Lyimo IN, Mpingwa MW, Takken W, Russell TL. 2010. Anopheline and culicine mosquitoes are not repelled by surfaces treated with the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana. Parasites & Vectors 3:80. doi: 10.1186/1756-3305-3-80
42. Mouchet J, Hamon J. 1963. Difficulties in Malaria Eradication Campaigns Due to the Behaviour of the Vectors. Geneva: World Health Organization.
43. Murray NE, Quam MB, Wilder-Smith A. 2013. Epidemiology of dengue: past, present and future prospects. Clinical Epidemiology 5:299-309. doi: 10.2147/CLEP.S34440
44. Müller GC, Junnila A, Butler J, Kravchenko VD, Revay EE, Weiss RW, Schlein Y. 2009. Efficacy of the botanical repellents geraniol, linalool, and citronella against mosquitoes. Journal of Vector Ecology 34:2-8. doi: 10.1111/j.1948-7134.2009.00002.x
45. N’Guessan R, Corbel V, Akogbéto M, Rowland M. 2007. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerging Infectious Diseases 13:199-206. doi: 10.3201/eid1302.060631
46. N’guessan R, Knols BG, Pennetier C, Rowland M. 2008. DEET microencapsulation: a slow-release formulation enhancing the residual efficacy of bed nets against malaria vectors. Transactions of the Royal Society of Tropical Medicine and Hygiene 102:259-262. doi: 10.1016/j.trstmh.2007.10.012
47. N’Guessan R, Rowland M, Moumouni TL, Kesse NB, Carnevale P. 2006. Evaluation of synthetic repellents on mosquito nets in experimental huts against insecticide-resistant anopheles gambiae and culex quinquefasciatus mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 100:1091-1097. doi: 10.1016/j.trstmh.2006.04.005
48. Nauen R. 2007. Insecticide resistance in disease vectors of public health importance. Pest Management Science 63:628-633. doi: 10.1002/ps.1406
49. Ndiath MO, Mazenot C, Sokhna C, Trape JF. 2014. How the malaria vector anopheles gambiae adapts to the use of insecticide-treated nets by african populations. PLoS One 9:e97700. doi: 10.1371/journal.pone.0097700
50. Ndiath MO, Sougoufara S, Gaye A, Mazenot C, Konate L, Faye O, Faye O, Sokhna C, Trape JF. 2012. Resistance to DDT and pyrethroids and increased kdr mutation frequency in an. gambiae after the implementation of permethrin-treated nets in senegal. PLoS One 7:e31943. doi: 10.1371/annotation/855f784c-b8db-449c-9de8-83b6404a049d
51. O’Donnell AJ, Schneider P, McWatters HG, Reece SE. 2011. Fitness costs of disrupting circadian rhythms in malaria parasites. Proceedings of the Royal Society B 278:2429-2436. doi: 10.1098/rspb.2010.2457
52. Ochomo E, Bayoh NM, Kamau L, Atieli F, Vulule J, Ouma C, Ombok M, Njagi K, Soti D, Mathenge E, Muthami L, Kinyari T, Subramaniam K, Kleinschmidt I, Donnelly MJ, Mbogo C. 2014. Pyrethroid susceptibility of malaria vectors in four Districts of western Kenya. Parasites & Vectors 7:310. doi: 10.1186/1756-3305-7-310
53. Ogoma SB, Ngonyani H, Simfukwe ET, Mseka A, Moore J, Maia MF, Moore SJ, Lorenz LM. 2014. The mode of action of spatial repellents and their impact on vectorial capacity of Anopheles gambiae sensu stricto. PLoS One 9:e110433. doi: 10.1371/journal.pone.0110433
54. Patrick M. 1900. Experimental proof of the mosquitomalaria theory. BMJ 2:949. doi: 10.1136/bmj.2.2074.949
55. Pennetier C, Corbel V, Boko P, Odjo A, N’Guessan R, Lapied B, Hougard JM. 2007. Synergy between repellents and non-pyrethroid insecticides strongly extends the efficacy of treated nets against Anopheles gambiae. Malaria Journal 6:1-7. doi: 10.1186/1475-2875-6-38
56. Read AF, Lynch PA, Thomas MB. 2009. How to make evolution-proof insecticides for malaria control. PLoS Biology 7:e58. doi: 10.1371/journal.pbio.1000058
57. Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, Slotman MA. 2011. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on bioko island, equatorial guinea. Malaria Journal 10:184. doi: 10.1186/1475-2875-10-184
58. Revay EE, Kline DL, Xue RD, Qualls WA, Bernier UR, Kravchenko VD, Ghattas N, Pstygo I, Müller GC. 2013. Reduction of mosquito biting-pressure: spatial repellents or mosquito traps? A field comparison of seven commercially available products in Israel. Acta Tropica 127:63-68. doi: 10.1016/j.actatropica.2013.03.011
59. Roberts D. 1993. Insecticide Repellency in Malaria Vector Control: A Position Paper. VBC Project report No 81131.
60. Roberts DR, Alecrim WD, Hshieh P, Grieco JP, Bangs M, Andre RG, Chareonviriphap T. 2000. A probability model of vector behavior: effects of DDT repellency, irritancy, and toxicity in malaria control. Journal of Vector Ecology 25:48-61.
61. Roberts DR, Alecrim WD. 1991. Behavioral response of Anopheles darlingi to DDT-sprayed house walls in Amazonia. Bulletin of the Pan American Health Organization 25:210-217.
62. Roberts DR, Laughlin LL, Hsheih P, Legters LJ. 1997. DDT, global strategies, and a malaria control crisis in South America. Emerging Infectious Diseases 3:295-302. doi: 10.3201/eid0303.970305
63. Roberts DR, Manguin S, Mouchet J. 2000. DDT house spraying and re-emerging malaria. The Lancet 356:330-332. doi: 10.1016/S0140-6736(00)02516-2
64. Roberts DR. 2010. Impact of anti-DDT campaigns on malaria control. Outlooks on Pest Management 21:4-11. doi: 10.1564/21feb02
65. Roll Back Malaria Vector Control Working Group. 2015. Housing and malaria consensus statement.
66. Rosenheim J, Tabashnik BE. 1990. Evolution of pesticide resistance: interactions between generation time and genetic, ecological, and operational factors. Journal of Economic Entomology 83:1184-1193. doi: 10.1093/jee/83.4.1184
67. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. 2011. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malaria Journal 10:80. doi: 10.1186/1475-2875-10-80
68. Syafruddin D, Bangs MJ, Sidik D, Elyazar I, Asih PB, Chan K, Nurleila S, Nixon C, Hendarto J, Wahid I, Ishak H, Bøgh C, Grieco JP, Achee NL, Baird JK. 2014. Impact of a spatial repellent on malaria incidence in two villages in Sumba, Indonesia. American Journal of Tropical Medicine and Hygiene 91:1079-1087. doi: 10.4269/ajtmh.13-0735
69. Tananchai C, Tisgratog R, Grieco JP, Chareonviriyaphap T. 2012. Pyrethroid induced behavioral responses of Anopheles dirus, a vector of malaria in Thailand. Journal of Vector Ecology 37:187-196. doi: 10.1111/j.1948-7134.2012.00216.x
70. Thomas MB, Read AF. 2007. Can fungal biopesticides control malaria? Nature Reviews Microbiology 5:377-383. doi: 10.1038/nrmicro1638
71. University of Notre Dame. 2016. Spatial repellents for control of vector-borne disease. http://ndigd.nd.edu/projects/data/spatial-repellents-for-control-of-vector-borne-disease/.
72. White MT, Lwetoijera D, Marshall J, Caron-Lormier G, Bohan DA, Denholm I, Devine GJ. 2014. Negative cross resistance mediated by co-treated bed nets: a potential means of restoring pyrethroid-susceptibility to malaria vectors. PLoS One 9:e95640. doi: 10.1371/journal.pone.0095640
73. WHO. 2015a. Global Technical Strategy for Malaria 2016-2030.
74. WHO. 2015b. Vector control and insecticide resistance. http://www.who.int/malaria/areas/vector_control/en/.
75. Xue R, Ali A, Barnard DR. 2003. Scientific notes-laboratory evaluation of toxicity of 16 insect repellents in aerosol sprays to adult mosquitoes. Journal of the American Mosquito Control Association. 19:271-274.
76. Yakob L, Dunning R, Yan G. 2011. Indoor residual spray and insecticide-treated bednets for malaria control: theoretical synergisms and antagonisms. Journal of the Royal Society Interface 8:799-806. doi: 10.1098/rsif.2010.0537