Most outdoor malaria transmission by behaviourally-resistant Anopheles arabiensis is mediated by mosquitoes that have previously been inside houses

Malaria Journal

Volumn 15, Issue 1, 2016, Pages

  Killeen, Gerry F ^a,b   Govella, Nicodem J ^a   Lwetoijera, Dickson W ^a   Okumu, Fredros O ^a,c  

^a IFAKARA HEALTH INSTITUTE   (Tanzania)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

Anopheles; Malaria; Mosquito; Plasmodium; Residual transmission; Vector control

Indexed keywords

ANOPHELES ARABIENSIS; ARTICLE; BED NET; BOVINE; ENVIRONMENTAL EXPOSURE; HUMAN; INSECT BITE; MALARIA; NONHUMAN; PARASITE TRANSMISSION; PARASITE VECTOR; POPULATION RESEARCH; VECTOR CONTROL; ANIMAL; ANOPHELES; BIOLOGICAL MODEL; FEEDING BEHAVIOR; HOUSING; INSECT VECTOR; MOSQUITO CONTROL; PARASITOLOGY; PHYSIOLOGY; PROCEDURES; TRANSMISSION;

ANIMALS; ANOPHELES; CATTLE; FEEDING BEHAVIOR; HOUSING; HUMANS; INSECT VECTORS; MALARIA; MODELS, BIOLOGICAL; MOSQUITO CONTROL;

EID: 84966263498     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-016-1280-z     Document Type: Article

References (48)

1. WHO. Guidance Note-Control of residual malaria parasite transmission. Geneva: World Health Organization, Global Malaria Programme; 2014:5.
2. WHO. Global Technical Strategy for Malaria for 2016-2030. Geneva: World Health Organization, Global Malaria Programme; 2015:32.
3. Durnez L, Coosemans M. Residual transmission of malaria: an old issue for new approaches. In: Manguin S, editor. Anopheles mosquitoes-new insights into malaria vectors. Rijeka: Intech; 2013. p. 671-704.
4. Killeen GF. Characterizing, controlling and eliminating residual malaria transmission. Malar J. 2014;13:330.
5. Govella NJ, Ferguson HM. Why use of interventions targetting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Front Physiol. 2012;3:199.
6. Russell TL, Beebe NW, Cooper RD, Lobo NF, Burkot TR. Successful malaria elimination strategies require interventions that target changing vector behaviours. Malar J. 2013;12:56.
7. Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M, et al. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J. 2014;13:125.
8. Moiroux N, Damien GB, Egrot M, Djenontin A, Chandre F, Corbel V, et al. Human exposure to early morning Anopheles funestus biting behavior and personal protection provided by long-lasting insecticidal nets. PLoS ONE. 2014;9:e104967.
9. Kiware SS, Chitnis N, Devine GJ, Moore SJ, Majambere S, Killeen GF. Biologically meaningful coverage indicators for eliminating malaria transmission. Biol Lett. 2012;8:874-7.
10. Kiware SS, Chitnis N, Moore SJ, Devine GJ, Majambere S, Killeen GF. Simplified models of vector control impact upon malaria transmission by zoophagic mosquitoes. PLoS ONE. 2012;7:e37661.
11. Killeen GF, Kiware SS, Seyoum A, Gimnig JE, Corliss GF, Stevenson J, et al. Comparative assessment of diverse strategies for malaria vector population control based on measured rates at which mosquitoes utilize targeted resource subsets. Malar J. 2014;13:338.
12. Killeen GF, Seyoum A, Gimnig JE, Stevenson JC, Drakeley CJ, Chitnis N. Made-to-measure malaria vector control strategies: rational design based on insecticide properties and coverage of blood resources for mosquitoes. Malar J. 2014;13:146.
13. Govella NJ, Chaki PP, Killeen GF. Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations. Malar J. 2013;12:124.
14. Killeen GF, Chitnis N. Potential causes and consequences of behavioural resilience and resistance in malaria vector populations: a mathematical modelling analysis. Malar J. 2014;13:97.
15. Elliott R. The influence of vector behaviour upon malaria transmission. Am J Trop Med Hyg. 1972;21:755-63.
16. Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC, Magesa SM, et al. Species shifts in the Anopheles gambiae complex: do LLINs successfully control Anopheles arabiensis? PLoS ONE. 2012;7:e31481.
17. Okumu FO, Kiware SS, Moore SJ, Killeen GF. Mathematical evaluation of community level impact of combining bed nets and indoor residual spraying upon malaria transmission in areas where the main vectors are Anopheles arabiensis mosquitoes. Parasit Vectors. 2013;6:17.
18. Okumu FO, Mbeyela E, Ligamba G, Moore J, Ntamatungiro AJ, Kavishe DR, et al. Comparative evaluation of combinations of long lasting insecticidal nets and indoor residual spraying, relative to either method alone, for malaria vector control in an area dominated by Anopheles arabiensis. Parasit Vectors. 2013;6:46.
19. Asale A, Getachew Y, Hailesilassie W, Speybroeck N, Duchateau L, Yewhalaw D. Evaluation of the efficacy of DDT indoor residual spraying and long-lasting insecticidal nets against insecticide resistant populations of Anopheles arabiensis Patton (Diptera: Culicidae) from Ethiopia using experimental huts. Parasit Vectors. 2014;7:131.
20. Huho BJ, Briët O, Seyoum A, Sikaala CH, Bayoh N, Gimnig JE, et al. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235-47.
21. Bayoh MN, Walker ED, Kosgei J, Ombok M, Olang GB, Githeko AK, et al. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasit Vectors. 2014;7:380.
22. Bradley J, Lines J, Fuseini G, Schwabe C, Monti F, Slotman MA, et al. Outdoor biting by Anopheles mosquitoes on Bioko Island does not currently impact on malaria control. Malar J. 2015;14:170.
23. Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T, Coetzee M, et al. A global map of dominant malaria vectors. Parasit Vectors. 2012;5:69.
24. Govella NJ, Okumu FO, Killeen GF. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg. 2010;82:415-9.
25. Russell TL, 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.
26. Yohannes M, Boelee E. Early biting rhythm in the afro-tropical vector of malaria, Anopheles arabiensis, and challenges for its control in Ethiopia. Med Vet Entomol. 2012;26:103-5.
27. White GB. Anopheles gambiae complex and disease transmission in Africa. Trans R Soc Trop Med Hyg. 1974;68:279-301.
28. Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). Johannesburg: South African Medical Research Institute; 1987.
29. Muirhead-Thomson RC. The significance of irritability, behaviouristic avoidance and allied phenomena in malaria eradication. Bull World Health Organ. 1960;22:721-34.
30. Kouznetsov RL. Malaria control by application of indoor spraying of residual insecticides in tropical Africa and its impact on community health. Trop Doct. 1977;7:81-93.
31. Russell TL, Lwetoijera DW, Maliti D, Chipwaza B, Kihonda J, Charlwood JD, et al. Impact of promoting longer-lasting insecticide treatment of bed nets upon malaria transmission in a rural Tanzanian setting with pre-existing high coverage of untreated nets. Malar J. 2010;9:187.
32. Kabula B, Tungu P, Matowo J, Kitau J, Mweya C, Emidi B, et al. Susceptibility status of malaria vectors to insecticides commonly used for malaria control in Tanzania. Trop Med Int Health. 2012;17:742-50.
33. Killeen GF. A second chance to tackle African malaria vector mosquitoes that avoid houses and don't take drugs. Am J Trop Med Hyg. 2013;88:809-16.
34. Mayagaya VS, Nkwengulila G, Lyimo IN, Kihonda J, Mtambala H, Ngonyani H, et al. The impact of livestock on the abundance, resting behaviour and sporozoite rate of malaria vectors in southern Tanzania. Malar J. 2015;14:17.
35. Charlwood JD, Smith T, Kihonda J, Heiz B, Billingsley PF, Takken W. Density independent feeding success of malaria vectors (Diptera: Culicidae) in Tanzania. Bull Entomol Res. 1995;85:29-35.
36. Killeen GF, Chitnis N, Moore SJ, Okumu FO. Target product profile choices for intra-domiciliary malaria vector control pesticide products: repel or kill? Malar J. 2011;10:207.
37. Killeen GF, Seyoum A, Knols BGJ. Rationalizing historical successes of malaria control in Africa in terms of mosquito resource availability management. Am J Trop Med Hyg. 2004;71(Supplement 2):87-93.
38. Killeen GF, McKenzie FE, Foy BD, Bogh C, Beier JC. The availability of potential hosts as a determinant of feeding behaviours and malaria transmission by mosquito populations. Trans R Soc Trop Med Hyg. 2001;95:469-76.
39. Okumu FO, Moore SJ. Combining indoor residual spraying and insecticide-treated nets for malaria control in Africa: a review of possible outcomes and an outline of suggestions for the future. Malar J. 2011;10:208.
40. Achee NL, Bangs MJ, Farlow R, Killeen GF, Lindsay S, Logan JG, et al. Spatial repellents: from discovery and development to evidence-based validation. Malar J. 2012;11:164.
41. Chaccour C, Killeen GF. Mind the gap: residual malaria transmission, veterinary endectocides and livestock as targets for malaria vector control. Malar J. 2016;15:24.
42. Kiswewski AE, Mellinger A, Spielman A, Malaney P, Sachs SE, Sachs J. A global index representing the stability of malaria transmission. Am J Trop Med Hyg. 2004;70:486-98.
43. Oxborough RM, Kitau J, Jones R, Feston E, Matowo J, Mosha FW, et al. Long-lasting control of Anopheles arabiensis by a single spray application of micro-encapsulated pirimiphos-methyl (Actellic® 300 CS). Malar J. 2014;13:37.
44. Yakob L, Dunning R, Yan G. Indoor residual spray and insecticide-treated bednets for malaria control: theoretical synergisms and antagonisms. J R Soc Interface. 2011;8:799-806.
45. Okumu FO, Madumla EP, John AN, Lwetoijera DW, Sumaye RD. Attracting, trapping and killing disease-transmitting mosquitoes using odor-baited stations - The Ifakara Odor-Baited Stations. Parasit Vectors. 2010;3:12.
46. Mnyone LL, Lyimo IN, Lwetoijera DW, Mpingwa MW, Nchimbi N, Hancock PA, et al. Exploiting the behaviour of wild malaria vectors to achieve high infection with fungal biocontrol agents. Malar J. 2012;11:87.
47. Andriessen R, Snetselaar J, Suer RA, Osinga AJ, Deschietere J, Lyimo IN, et al. Electrostatic coating enhances bioavailability of insecticides and breaks pyrethroid resistance in mosquitoes. Proc Natl Acad Sci USA. 2015;112:12081-6.
48. Diabate A, Bilgo E, Dabire RK, Tripet F. Environmentally friendly tool to control mosquito populations without risk of insecticide resistance: the Lehmann's funnel entry trap. Malar J. 2013;12:196.