Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa

Bernadette Huho, Olivier Briët, Aklilu Seyoum, Chadwick Sikaala, Nabie Bayoh, John Gimnig, Fredros Okumu, Diadier Diallo, Salim Abdulla, Thomas Smith, Gerry Killeen, Bernadette Huho, Olivier Briët, Aklilu Seyoum, Chadwick Sikaala, Nabie Bayoh, John Gimnig, Fredros Okumu, Diadier Diallo, Salim Abdulla, Thomas Smith, Gerry Killeen

Abstract

Background: Insecticide-treated nets (ITNs) and indoor residual spraying (IRS) are highly effective tools for controlling malaria transmission in Africa because the most important vectors, from the Anopheles gambiae complex and the A. funestus group, usually prefer biting humans indoors at night.

Methods: Matched surveys of mosquito and human behaviour from six rural sites in Burkina Faso, Tanzania, Zambia, and Kenya, with ITN use ranging from 0.2% to 82.5%, were used to calculate the proportion of human exposure to An. gambiae sensu lato and An. funestus s.l. that occurs indoors (πi), as an indicator of the upper limit of personal protection that indoor vector control measures can provide. This quantity was also estimated through use of a simplified binary analysis (π(i)(B)) so that the proportions of mosquitoes caught indoors (Pi), and between the first and last hours at which most people are indoors (Pfl) could also be calculated as underlying indicators of feeding by mosquitoes indoors or at night, respectively.

Results: The vast majority of human exposure to Anopheles bites occurred indoors (π(i)(B)= 0.79-1.00). Neither An. gambiae s.l. nor An. funestus s.l. strongly preferred feeding indoors (P(i) = 0.40-0.63 and 0.22-0.69, respectively), but they overwhelmingly preferred feeding at times when most humans were indoors (P(fl) = 0.78-1.00 and 0.86-1.00, respectively).

Conclusions: These quantitative summaries of behavioural interactions between humans and mosquitoes constitute a remarkably consistent benchmark with which future observations of vector behaviour can be compared. Longitudinal monitoring of these quantities is vital to evaluate the effectiveness of ITNs and IRS and the need for complementary measures that target vectors outdoors.

Figures

Figure 1
Figure 1
Map of Africa showing locations of study sites
Figure 2
Figure 2
Hourly biting pattern of Anopheles gambiae sensu lato (panels on left) and Anopheles funestus sensu lato (panels on right) occurring both indoors (solid lines) and outdoors (dashed lines) at different study sites. The grey area represents the proportion of the human population predominantly spending time indoors during the times shown on the abscissa of each graph
Figure 3
Figure 3
Profiles of biting by both Anopheles gambiae sensu latu (panels on left) and Anopheles funestus sensu lato (panels on right) experienced by human population at different study sites. Pie charts illustrate the amount of exposure occurring indoors and outdoors. The light grey areas in the graphs and pie charts represent outdoor human exposure and the dark grey areas represent indoor human exposure

References

    1. Lengeler C. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev. 2004;2:CD000363.
    1. Pluess B, Tanser FC, Lengeler C, Sharp BL. Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev. 2010;4:CD006657.
    1. Hii JLK, Smith T, Vounatsou P, et al. Area effects of bednet use in a malaria-endemic area in Papua New Guinea. Trans R Soc Trop Med Hyg. 2001;95:7–13.
    1. Robert V, Carnevale P. Influence of deltamethrin treatment of bed nets on malaria transmission in the Kou valley, Burkina Faso. Bull World Health Organ. 1991;69:735–40.
    1. Magesa SM, Wilkes TJ, Mnzava AEP, et al. Trial of pyrethroid impregnated bednets in an area of Tanzania holoendemic for malaria. Part 2: Effects on the malaria vector population. Acta Tropica. 1991;49:97–108.
    1. Pates H, Curtis C. Mosquito behavior and vector control. Annu Rev Entomol. 2005;50:53–70.
    1. Maxwell CA, Msuya E, Sudi M, Njunwa KJ, Carneiro IA, Curtis CF. Effect of community-wide use of insecticide-treated nets for 3–4 years on malarial morbidity in Tanzania. Trop Med Int Health. 2002;7:1003–08.
    1. Howard SC, Omumbo J, Nevill CG, Some ES, Donnelly CA, Snow RW. Evidence for a mass community effect of insecticide treated bednets on the incidence of malaria on the Kenyan coast. Trans R Soc Trop Med Hyg. 2000;94:357–60.
    1. Lindsay SW, Adiamah JH, Armstrong JRM. The effect of permethrin-impregnated bed nets on house entry by mosquitoes in The Gambia. Bull Entomol Res. 1992;82:49–55.
    1. Lindsay SW, Adiamah JH, Miller JE, Armstrong JRM. Pyrethroid-treated bednet effects on mosquitoes of the Anopheles gambiae complex. Med Vet Entomol. 1991;5:477–83.
    1. Gillies MT, DeMeillon B. The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region) Johannesburg: South African Institute for Medical Research; 1968.
    1. Gillies MT. Anopheline mosquitos: vector behaviour and bionomics. In: Wernsdorfer WH, McGregor I, editors. Malaria: Principles and Practice of Malariology. Edinburgh: Churchill Livingstone; 1988.
    1. Russell TL, Lwetoijera DW, Maliti D, 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.
    1. Bayoh MN, Mathias DK, Odiere MR, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J. 2010;9:62.
    1. Gillies MT, Smith A. The effect of a residual house-spraying campaign in East Africa on species balance in the Anopheles funestus group. The replacement of A. funestus Giles by A. rivulorum Leeson. Bull Entomol Res. 1960;51:243–52.
    1. Gillies MT. A new species of the Anopheles funestus complex (Diptera: Culicidae) from East Africa. Proc R Entomol Soc London. 1962;31:81–86.
    1. Gillies MT, Furlong M. An investigation into the behaviour of Anopheles parensis Gillies at Malindi on the Kenya coast. Bull Entomol Res. 1964;55:1–16.
    1. Bugoro H, Cooper R, Butafa C, et al. Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination. Malar J. 2011;10:133.
    1. 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.
    1. Reddy MR, Overgaard HJ, Abaga S, et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011;10:184.
    1. Ranson H, N’Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011;27:91–98.
    1. Griffin JT, Hollingsworth TD, Okell LC, et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 2010;7:1–27.
    1. Killeen G, Chitnis N, Moore SJ, Okumu F. Target product profile choices for intra-domiciliary malaria vector control pesticide products: repel or kill. Malar J. 2011;10:207.
    1. Killeen GF, Moore SJ. Target product profiles for protecting against outdoor malaria transmission. Malar J. 2012;11:17.
    1. Eckhoff PA. A malaria transmission-directed model of mosquito life cycle and ecology. Malar J. 2011;10:303.
    1. 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.
    1. Hamel MJ, Otieno P, Bayoh N, et al. The combination of indoor residual spraying and insecticide-treated nets provides added protection against malaria compared with insecticide-treated nets alone. Am J Trop Med Hyg. 2011;85:1080–86.
    1. Service MW. A critical review of procedures for sampling populations of adult mosquitoes. Bull Entomol Res. 1977;67:343–82.
    1. Killeen GF, Kihonda J, Lyimo EO, et al. Quantifying behavioural interactions between humans and mosquitoes: Evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006;6:161.
    1. Seyoum A, Sikaala CH, Chanda J, et al. Human exposure to anopheline mosquitoes occurs primarily indoors, even for users of insecticide-treated nets in Luangwa Valley, South-east Zambia. Parasit Vectors. 2012;5:101.
    1. 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.
    1. Kiware SS, Chitnis N, Moore SJ, et al. Simplified models of vector control impact upon malaria transmission by zoophagic mosquitoes. PLoS One. 2012;7:e37661.
    1. Kiware SS, Chitnis N, Devine GJ, Moore SJ, Majambere S, Killeen GF. Biologically meaningful coverage indicators for eliminating malaria transmission. Biol Lett. 2012;8:874–77.
    1. Collett D. Modelling Binary Data. 2nd edn. Boca Raton, FL: Chapman & Hall; 2002.
    1. Geissbühler Y, Chaki P, Emidi B, et al. Interdependence of domestic malaria prevention measures and mosquito-human interactions in urban Dar es Salaam, Tanzania. Malar J. 2007;6:126.
    1. Robert V, Carnevale P, Ouedraogo V, Petrarca V, Coluzzi M. La transmission du paludisme humain dans un village de savane du Sud-Ouest du Burkina Faso [The transmission of human malaria in a village in the south-west savannah of Burkina Faso] Ann Soc Belge Méd Trop. 1988;68:107–21.
    1. Gillies MT, Coetzee M. A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region) Johannesburg: South African Medical Research Institute; 1987.
    1. Dabire KR, Baldet T, Diabate A, et al. Anopheles funestus (Diptera: Culicidae) in a humid savannah area of western Burkina Faso: Bionomics, insecticide resistance status, and role in malaria transmission. J Med Entomol. 2007;44:990–97.
    1. Ilboudo-Sanogo E, Cuzin-Ouattara N, Diallo DA, et al. Insecticide-treated materials, mosquito adaptation and mass effect: entomological observations after five years of vector control in Burkina Faso. Trans R Soc Trop Med Hyg. 2001;95:353–60.
    1. Matola YG, ljumba JN, Magayuka SA, Kopakopa SB. Epidemiological of impact of lambdacyhalothrin (OMS-3021) on the transmission of malaria in a rural area in Tanzania. Bull Soc Fr Parasitol. 1990;8:1201–02.
    1. World Health Organization. Insecticide-Treated Mosquito Nets: A Position Statement. Geneva: WHO; 2007.
    1. Flaxman AD, Fullman N, Otten MW, et al. Rapid scaling up of insecticide-treated bed net coverage in Africa and its relationship with development assistance for health: a systematic synthesis of supply, distribution, and household survey data. PLoS Med. 2010;7:e1000328.
    1. Ferguson HM, Dornhaus A, Beeche A, et al. Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010;7:e1000303.
    1. Phillips-Howard PA, Nahlen BL, Alaii JA, et al. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya I. Development of infrastructure and description of study site. Am J Trop Med Hyg. 2003;68:3–9.
    1. Hawley WA, ter Kuile FO, Steketee RS, et al. Implications of the Western Kenya permethrin-treated bed net study for policy, program implementation, and future research. Am J Trop Med Hyg. 2003;68(Suppl 4):168–73.
    1. Lindblade KA, Eisele TP, Gimnig JE, et al. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bednets. JAMA. 2004;291:2571.
    1. Eisele TP, Lindblade AK, Wannemuehler AK, et al. Effects of sustained insecticide-treated bednet use on all-cause child mortality in areas of intense malaria transmission in western Kenya. Am J Trop Med Hyg. 2005;73:149–56.
    1. Shah M, Kariuki S, Eng JV, et al. Effect of transmission reduction by insecticide-treated bednets (ITNs) on antimalarial drug resistance in western Kenya. PLoS One. 2011;6:e26746.
    1. Yohanne 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;26:103–05.
    1. Kleinschmidt I, Schwabe C, Shiva M, et al. Combining indoor residual spraying and insecticide-treated net interventions. Am J Trop Med Hyg. 2009;81:519–24.
    1. Meyrowitsch DW, Pedersen EM, Alifrangis M, et al. Is the current decline in malaria burden in sub-Saharan Africa due to a decrease in vector population? Malar J. 2011;10:188.
    1. 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.
    1. Elliott R. The influence of vector behaviour upon malaria transmission. Am J Trop Med Hyg. 1972;21:755–63.
    1. Muirhead-Thomson RC. Mosquito Behaviour in Relation to Malaria Transmission and Control in the Tropics. London: Edward Arnold & Co.; 1951.
    1. Muirhead-Thomson RC. The significance of irritability, behaviouristic avoidance and allied phenomena in malaria eradication. Bull World Health Organ. 1960;22:721–34.
    1. Trung HD, Van Bortel W, Sochantha T, Keokenchanh K, Briët OJ, Coosemans M. Behavioural heterogeneity of Anopheles species in ecologically different localities in Southeast Asia: a challenge for vector control. Trop Med Int Health. 2005;10:251–62.
    1. Van Bortel W, Trung HD, Hoi LX, et al. Malaria transmission and vector behaviour in a forested malaria focus in central Vietnam and the implications for vector control. Malar J. 2010;9:373.
    1. Trape JF, Tall A, Diagne N, et al. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis. 2011;11:925–32.
    1. Moiroux N, Gomez MB, Pennetier C, et al. Changes in Anopheles funestus biting behaviour following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206:1622–29.
    1. World Health Organization. Malaria Vector Control and Personal Protection: Technical Report. Geneva: World Health Organization; 2006.
    1. Kigadye ESP, Nkwengulila G, Magesa SM, Abdulla S. Diversity, spatial and temporal abundance of Anopheles gambiae complex in the Rufiji River basin, south-eastern Tanzania. Tanzanian J Health Res. 2010;12:68–72.
    1. Killeen GF, Smith TA, Ferguson HM, et al. Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets. PLoS Med. 2007;4:e229.

Source: PubMed

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