Skip to main content
Top
Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Bites before and after bedtime can carry a high risk of human malaria infection

Published in: Malaria Journal | Issue 1/2017

Login to get access

Abstract

Background

Understanding biting distribution of potentially infectious (parous) mosquitoes at various hours of the night would be useful in establishing the likely impact of bed nets on malaria transmission. Bed nets are highly effective at preventing biting by older malaria vectors, which occurs when most people are in bed. However, this behaviour is likely to vary across ecological settings and among mosquito populations.

Methods

Field experiments were conducted in Minepa village within Kilombero Valley. Two outdoor catching stations located approximately 50 m from each other were established for mosquito collection. On each experimental night, mosquitoes were collected using human landing catch (HLC) by a single adult male at each station from 18:00 to 07:00 h. To compare the distribution of mosquito biting and the composition of their age structure, mosquitoes were sorted and recorded according to the hour they were collected. A sub-sample of Anopheles arabiensis was dissected to determine their parity status. Insectary-reared An. arabiensis within the semi-field system (SFS) with known age were also released in the SFS (10 m × 20 m) and recaptured hourly using HLC to determine the effect of parity on biting distribution.

Results

Overall, there was no statistical association between the parity status and the biting time of An. arabiensis either in the field or in the SFS (P ≥ 0.05). The wild and insectary-reared An. arabiensis were observed to exhibit different hourly biting patterns.

Conclusion

The study has shown that mosquito biting time phenotype is not influenced by their parity status. These findings imply that the risk of human exposure to potentially infectious bites is equally distributed throughout the night, thus supplementary measures to protect people against bites in evening and morning are desirable.
Literature
1.
go back to reference Gillies MT, DeMeillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). Johannesburg: South African Institute for Medical Research; 1968. Gillies MT, DeMeillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). Johannesburg: South African Institute for Medical Research; 1968.
2.
go back to reference Gillies MT. Anopheline mosquitos: vector behaviour and bionomics. Edinburgh: Churchill Livingstone; 1988. Gillies MT. Anopheline mosquitos: vector behaviour and bionomics. Edinburgh: Churchill Livingstone; 1988.
3.
go back to reference MacDonald G. The epidemiology and control of malaria. London: Oxford University Press; 1957. MacDonald G. The epidemiology and control of malaria. London: Oxford University Press; 1957.
4.
go back to reference Garrett-Jones C. Prognosis for interruption of malaria transmission through assessment of the mosquito’s vectorial capacity. Nature. 1964;204:1173–5.CrossRefPubMed Garrett-Jones C. Prognosis for interruption of malaria transmission through assessment of the mosquito’s vectorial capacity. Nature. 1964;204:1173–5.CrossRefPubMed
5.
go back to reference Beier JC. Malaria parasite development in mosquitoes. Ann Rev Entomol. 1998;43:519–43.CrossRef Beier JC. Malaria parasite development in mosquitoes. Ann Rev Entomol. 1998;43:519–43.CrossRef
7.
go back to reference Dye C. The analysis of parasite transmission by bloodsucking insects. Ann Rev Entomol. 1992;37:1–19.CrossRef Dye C. The analysis of parasite transmission by bloodsucking insects. Ann Rev Entomol. 1992;37:1–19.CrossRef
8.
go back to reference Gillies MT, Wilkes TJ. A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bull Entomol Res. 1965;56:237–62.CrossRefPubMed Gillies MT, Wilkes TJ. A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bull Entomol Res. 1965;56:237–62.CrossRefPubMed
9.
go back to reference Charlwood JD, Wilkes TJ. Studies on the age composition of sample of Anopheles darlingi Root (Diptera: Culicidae) in Brazil. Bull Entomol Res. 1979;69:337–42.CrossRef Charlwood JD, Wilkes TJ. Studies on the age composition of sample of Anopheles darlingi Root (Diptera: Culicidae) in Brazil. Bull Entomol Res. 1979;69:337–42.CrossRef
10.
go back to reference Charlwood JD, Paru R, Dagoro H, Lagog M. Influence of moonlight and gonotrophic age on biting activity of Anopheles farauti (Diptera: Culicidae) from Papua New Guinea. J Med Entomol. 1986;23:132–5.CrossRefPubMed Charlwood JD, Paru R, Dagoro H, Lagog M. Influence of moonlight and gonotrophic age on biting activity of Anopheles farauti (Diptera: Culicidae) from Papua New Guinea. J Med Entomol. 1986;23:132–5.CrossRefPubMed
11.
go back to reference Gillies MT, Wilkes TJ. Observations on nulliparous and parous rates in populations of Anopheles funestus in East Africa. Ann Trop Med Parasitol. 1963;57:204–13.CrossRefPubMed Gillies MT, Wilkes TJ. Observations on nulliparous and parous rates in populations of Anopheles funestus in East Africa. Ann Trop Med Parasitol. 1963;57:204–13.CrossRefPubMed
12.
go back to reference Bockarie MJ, Alexander N, Bockarie F, Ibam E, Barnish G, Alpers M. The late biting habit of parous Anopheles mosquitoes and pre-bed exposure of humans to infective female mosquitoes. Trans R Soc Trop Med Hyg. 1996;90:23–5.CrossRefPubMed Bockarie MJ, Alexander N, Bockarie F, Ibam E, Barnish G, Alpers M. The late biting habit of parous Anopheles mosquitoes and pre-bed exposure of humans to infective female mosquitoes. Trans R Soc Trop Med Hyg. 1996;90:23–5.CrossRefPubMed
13.
go back to reference Gillies MT. Age grouping and the biting cycle in Anopheles gambiae. A preliminary investigation. Bull Entomol Res. 1957;48:553–9.CrossRef Gillies MT. Age grouping and the biting cycle in Anopheles gambiae. A preliminary investigation. Bull Entomol Res. 1957;48:553–9.CrossRef
14.
go back to reference Lengeler C. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev. 2004;363:CD000363. Lengeler C. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev. 2004;363:CD000363.
15.
go back to reference WHO. World Malaria Report 2014. Geneva: World Health Organization; 2014. WHO. World Malaria Report 2014. Geneva: World Health Organization; 2014.
16.
go back to reference O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet. 2008;372:1555–62.CrossRefPubMedPubMedCentral O’Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet. 2008;372:1555–62.CrossRefPubMedPubMedCentral
17.
go back to reference Battarai A, Ali AS, Kachur SP, Martensson A, Abbas AK, Khatib R, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007;4:e309.CrossRef Battarai A, Ali AS, Kachur SP, Martensson A, Abbas AK, Khatib R, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007;4:e309.CrossRef
18.
go back to reference Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet. 2012;379:413–31.CrossRefPubMed Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet. 2012;379:413–31.CrossRefPubMed
19.
go back to reference Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.CrossRefPubMedPubMedCentral Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.CrossRefPubMedPubMedCentral
20.
go back to reference Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, 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.CrossRefPubMedPubMedCentral Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, 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.CrossRefPubMedPubMedCentral
21.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
22.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
23.
go back to reference Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, 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.CrossRefPubMedPubMedCentral Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, 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.CrossRefPubMedPubMedCentral
24.
go back to reference Moiroux N, Gomez MB, Pennetier C, Elanga E, Djenontin A, Chandre F, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206:1622–9.CrossRefPubMed Moiroux N, Gomez MB, Pennetier C, Elanga E, Djenontin A, Chandre F, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206:1622–9.CrossRefPubMed
25.
go back to reference Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M, et al. Biting by Anopheles funestus in broad daytime after use of long-lasting insecticidal nets: a new challenge to malaria control. Malar J. 2014;13:125.CrossRefPubMedPubMedCentral Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M, et al. Biting by Anopheles funestus in broad daytime after use of long-lasting insecticidal nets: a new challenge to malaria control. Malar J. 2014;13:125.CrossRefPubMedPubMedCentral
26.
go back to reference Mwangangi JM, Mbogo CM, Orindi BO, Muturi EJ, Midega JT, Nzovu J, et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12:13.CrossRefPubMedPubMedCentral Mwangangi JM, Mbogo CM, Orindi BO, Muturi EJ, Midega JT, Nzovu J, et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12:13.CrossRefPubMedPubMedCentral
27.
go back to reference Ndiath MO, Mazenot C, Sohna C, Trape J-F. How the malaria vector Anopheles gambiae adapts to the use of insecticide-treated nets by African population. PLoS ONE. 2014;9:e97700.CrossRefPubMedPubMedCentral Ndiath MO, Mazenot C, Sohna C, Trape J-F. How the malaria vector Anopheles gambiae adapts to the use of insecticide-treated nets by African population. PLoS ONE. 2014;9:e97700.CrossRefPubMedPubMedCentral
28.
go back to reference Lwetoijera DW, Harris C, Kiware SS, Dongus S, Devine GJ, McCall PJ, et al. Increasing role of Anopheles funestus and Anopheles arabiensis in malaria transmission in the Kilombero Valley,Tanzania. Malar J. 2014;13:331.CrossRefPubMedPubMedCentral Lwetoijera DW, Harris C, Kiware SS, Dongus S, Devine GJ, McCall PJ, et al. Increasing role of Anopheles funestus and Anopheles arabiensis in malaria transmission in the Kilombero Valley,Tanzania. Malar J. 2014;13:331.CrossRefPubMedPubMedCentral
29.
go back to reference Matowo NS, Moore J, Mapua S, Madumla EP, Moshi IR, Kaindoa EW, et al. Using a new odour-bated device to explore options for luring and killing outdoor-biting malaria vectors: a report on design and field evaluation of the Mosquito Landing Box. Parasit Vectors. 2013;6:137.CrossRefPubMedPubMedCentral Matowo NS, Moore J, Mapua S, Madumla EP, Moshi IR, Kaindoa EW, et al. Using a new odour-bated device to explore options for luring and killing outdoor-biting malaria vectors: a report on design and field evaluation of the Mosquito Landing Box. Parasit Vectors. 2013;6:137.CrossRefPubMedPubMedCentral
30.
go back to reference NBS. Tanzania HIV/AIDS and Malaria Indicator Survey 2011–2012. Tanzania: National Bureau of Statistics; 2013. p. 1–229. NBS. Tanzania HIV/AIDS and Malaria Indicator Survey 2011–2012. Tanzania: National Bureau of Statistics; 2013. p. 1–229.
31.
go back to reference Killeen GF, Tami A, Kihonda J, Okumu FO, Kotas ME, Grundmann H, et al. Cost-sharing strategies combining targeted public subsidies with private-sector delivery achieve high bednet coverage and reduced malaria transmission in Kilombero valley, southern Tanzania. BMC Infect Dis. 2007;7:121.CrossRefPubMedPubMedCentral Killeen GF, Tami A, Kihonda J, Okumu FO, Kotas ME, Grundmann H, et al. Cost-sharing strategies combining targeted public subsidies with private-sector delivery achieve high bednet coverage and reduced malaria transmission in Kilombero valley, southern Tanzania. BMC Infect Dis. 2007;7:121.CrossRefPubMedPubMedCentral
32.
go back to reference Kreppel K, Johnson PCD, Govella NJ, Pombi M, Maliti DF, Ferguson H. Comparative evaluation of the Sticky-Resting-Box-Trap, the standardised resting-bucket-trap and indoor aspiration for sampling malaria vectors. Parasit Vectors. 2015;8:462.CrossRefPubMedPubMedCentral Kreppel K, Johnson PCD, Govella NJ, Pombi M, Maliti DF, Ferguson H. Comparative evaluation of the Sticky-Resting-Box-Trap, the standardised resting-bucket-trap and indoor aspiration for sampling malaria vectors. Parasit Vectors. 2015;8:462.CrossRefPubMedPubMedCentral
33.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
34.
go back to reference NBS. Tanzania HIV/AID malaria indicator survey 2007-2008. Dar es Salaam: National Bureau of Statistics; 2008. p. 1–127. NBS. Tanzania HIV/AID malaria indicator survey 2007-2008. Dar es Salaam: National Bureau of Statistics; 2008. p. 1–127.
35.
go back to reference Mboera LEG. Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rates. Tanzan Health Res Bull. 2005;7:117–24.PubMed Mboera LEG. Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rates. Tanzan Health Res Bull. 2005;7:117–24.PubMed
36.
go back to reference Service MW. Mosquito ecology: field sampling methods. 2nd ed. London: Elsevier applied Science; 1993.CrossRef Service MW. Mosquito ecology: field sampling methods. 2nd ed. London: Elsevier applied Science; 1993.CrossRef
37.
go back to reference Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). Johannesburg: South African Medical Research Institute; 1987. Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). Johannesburg: South African Medical Research Institute; 1987.
38.
go back to reference Detinova TS. Age-grouping methods in Diptera of medical importance, with special reference to some vectors of malaria. Geneva: World Health Organization; 1962. Detinova TS. Age-grouping methods in Diptera of medical importance, with special reference to some vectors of malaria. Geneva: World Health Organization; 1962.
39.
go back to reference Scott JA, Brogdon WG, Collins FH. Identification of single specimens of Anopheles gambiae complex by polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.PubMed Scott JA, Brogdon WG, Collins FH. Identification of single specimens of Anopheles gambiae complex by polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.PubMed
40.
go back to reference Wirtz RA, Duncan JF, Njelesani EK, Schneider I, Brown AE, Oster CN, et al. ELISA method for detecting Plasmodium falciparum circumsporozoite antibody. Bull World Health Organ. 1989;67:535–42.PubMedPubMedCentral Wirtz RA, Duncan JF, Njelesani EK, Schneider I, Brown AE, Oster CN, et al. ELISA method for detecting Plasmodium falciparum circumsporozoite antibody. Bull World Health Organ. 1989;67:535–42.PubMedPubMedCentral
41.
go back to reference Burkot TR, Graves PM, Cattani JA, Wirtz RW, Gibson FD. The efficiency of sporozoite transmission in the human malarias, Plasmodium falciparum and P. vivax. Bull World Health Organ. 1987;65:375–80.PubMedPubMedCentral Burkot TR, Graves PM, Cattani JA, Wirtz RW, Gibson FD. The efficiency of sporozoite transmission in the human malarias, Plasmodium falciparum and P. vivax. Bull World Health Organ. 1987;65:375–80.PubMedPubMedCentral
42.
go back to reference Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, et al. False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector elimination. Malar J. 2011;10:195.CrossRefPubMedPubMedCentral Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, et al. False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector elimination. Malar J. 2011;10:195.CrossRefPubMedPubMedCentral
43.
go back to reference Ferguson HM, Ng’habi KR, Walder T, Kadungula D, Moore SJ, Lyimo I, et al. Establishment of a large semi-field system for experimental study of African malaria vector ecology and control in Tanzania. Malar J. 2008;7:158.CrossRefPubMedPubMedCentral Ferguson HM, Ng’habi KR, Walder T, Kadungula D, Moore SJ, Lyimo I, et al. Establishment of a large semi-field system for experimental study of African malaria vector ecology and control in Tanzania. Malar J. 2008;7:158.CrossRefPubMedPubMedCentral
44.
go back to reference Ng’habi KR, Mwasheshi D, Knols BG, Ferguson HM. Establishment of a self-propagating population of the African malaria vector Anopheles arabiensis under semi-field conditions. Malar J. 2010;9:356.CrossRefPubMedPubMedCentral Ng’habi KR, Mwasheshi D, Knols BG, Ferguson HM. Establishment of a self-propagating population of the African malaria vector Anopheles arabiensis under semi-field conditions. Malar J. 2010;9:356.CrossRefPubMedPubMedCentral
45.
go back to reference Mascari TM, Foil LD. Laboratory evaluation of the efficacy of fluorescent biomarkers for sugar-feeding sand flies (Diptera: Psychodidae). J Med Entomol. 2010;47:664–9.CrossRefPubMed Mascari TM, Foil LD. Laboratory evaluation of the efficacy of fluorescent biomarkers for sugar-feeding sand flies (Diptera: Psychodidae). J Med Entomol. 2010;47:664–9.CrossRefPubMed
46.
go back to reference Stewart ZP, Oxborough RM, Tungu PK, Kirby MJ, Rowland MW, Irish SR. Indoor application of attractive toxic sugar bait (ATSB) in combination with mosquito nets for control of pyrethroid-resistant mosquitoes. PLoS ONE. 2013;8:e84168.CrossRefPubMedPubMedCentral Stewart ZP, Oxborough RM, Tungu PK, Kirby MJ, Rowland MW, Irish SR. Indoor application of attractive toxic sugar bait (ATSB) in combination with mosquito nets for control of pyrethroid-resistant mosquitoes. PLoS ONE. 2013;8:e84168.CrossRefPubMedPubMedCentral
47.
go back to reference Charlwood JD, Graves PM, Birley MH. Capture-recapture studies with mosquitoes of the group Anopheles punctulatus Donitz (Diptera: Culicidae) from Papua New Guinea. Bull Entomol Res. 1986;76:211–27.CrossRef Charlwood JD, Graves PM, Birley MH. Capture-recapture studies with mosquitoes of the group Anopheles punctulatus Donitz (Diptera: Culicidae) from Papua New Guinea. Bull Entomol Res. 1986;76:211–27.CrossRef
48.
go back to reference Achee NL, Grieco JP, Andre RG, Rejmankova E, Roberts DR. A mark-release -recapture study to define the flight behaviors of Anopheles vestitipennis and Anopheles albimanus in Belize, Central America. J Am Mosq Control Assoc. 2007;23:276–82.CrossRefPubMed Achee NL, Grieco JP, Andre RG, Rejmankova E, Roberts DR. A mark-release -recapture study to define the flight behaviors of Anopheles vestitipennis and Anopheles albimanus in Belize, Central America. J Am Mosq Control Assoc. 2007;23:276–82.CrossRefPubMed
49.
go back to reference Gimnig JE, Walker ED, Otieno P, Kosgei J, Olang G, Omboki M, et al. Incidence of malaria among mosquito collectors conducting human landing catches in western Kenya. Am J Trop Med Hyg. 2013;88:301–8.CrossRefPubMedPubMedCentral Gimnig JE, Walker ED, Otieno P, Kosgei J, Olang G, Omboki M, et al. Incidence of malaria among mosquito collectors conducting human landing catches in western Kenya. Am J Trop Med Hyg. 2013;88:301–8.CrossRefPubMedPubMedCentral
50.
go back to reference Lindsay S, Ansell J, Selman C, Cox V, Hamilton K, Walraven G. Effect of pregnancy on exposure to malaria mosquitoes. Lancet. 2000;355:1972.CrossRefPubMed Lindsay S, Ansell J, Selman C, Cox V, Hamilton K, Walraven G. Effect of pregnancy on exposure to malaria mosquitoes. Lancet. 2000;355:1972.CrossRefPubMed
51.
go back to reference Omolo MO, Njiru B, Ndiege IO, Musau RM, Hassannali A. Differential attractiveness of human foot odours to Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) and variation in their chemical composition. Acta Trop. 2013;128:144–8.CrossRefPubMed Omolo MO, Njiru B, Ndiege IO, Musau RM, Hassannali A. Differential attractiveness of human foot odours to Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) and variation in their chemical composition. Acta Trop. 2013;128:144–8.CrossRefPubMed
52.
go back to reference Lindsay SW, Adiamah JH, Miller JE, Pleass RJ, Armstrong JRM. Variation in the attractiveness of human subjects to malaria mosquitoes (Diptera: Culicidae) in The Gambia. J Med Entomol. 1993;30:368–73.CrossRefPubMed Lindsay SW, Adiamah JH, Miller JE, Pleass RJ, Armstrong JRM. Variation in the attractiveness of human subjects to malaria mosquitoes (Diptera: Culicidae) in The Gambia. J Med Entomol. 1993;30:368–73.CrossRefPubMed
53.
go back to reference Cook MK, Kahindi SC, Oriango RM, Owaga C, Ayoma E, Mabuka D, et al. A bite before bed’: exposure to malaria vectors outside the times of net use in the highlands of western Kenya. Malar J. 2015;14:259.CrossRef Cook MK, Kahindi SC, Oriango RM, Owaga C, Ayoma E, Mabuka D, et al. A bite before bed’: exposure to malaria vectors outside the times of net use in the highlands of western Kenya. Malar J. 2015;14:259.CrossRef
54.
go back to reference Maxwell CA, Wakibara J, Tho S, Curtis CF. Malaria-infective biting at different hours of the night. Med Vet Entomol. 1998;12:325–7.CrossRefPubMed Maxwell CA, Wakibara J, Tho S, Curtis CF. Malaria-infective biting at different hours of the night. Med Vet Entomol. 1998;12:325–7.CrossRefPubMed
55.
go back to reference Msellemu D, Namango HI, Mwakalinga VM, Ntamatungiro AJ, Mlacha Y, Mtema ZJ, et al. The epidemiology of residual Plasmodium falciparum malaria transmission and infection burden in an African city with high coverage of multiple vector control measures. Malar J. 2016;15:288.CrossRefPubMedPubMedCentral Msellemu D, Namango HI, Mwakalinga VM, Ntamatungiro AJ, Mlacha Y, Mtema ZJ, et al. The epidemiology of residual Plasmodium falciparum malaria transmission and infection burden in an African city with high coverage of multiple vector control measures. Malar J. 2016;15:288.CrossRefPubMedPubMedCentral
56.
go back to reference Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, et al. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J. 2015;14:209.CrossRefPubMedPubMedCentral Tusting LS, Ippolito MM, Willey BA, Kleinschmidt I, Dorsey G, Gosling RD, et al. The evidence for improving housing to reduce malaria: a systematic review and meta-analysis. Malar J. 2015;14:209.CrossRefPubMedPubMedCentral
57.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
58.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
60.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
61.
go back to reference Wilson AL, Chen-Hussey V, Logan JG, Lindsay SW. Are topical insect repellents effective against malaria in endemic populations? A systematic review and meta-analysis. Malar J. 2014;13:446.CrossRefPubMedPubMedCentral Wilson AL, Chen-Hussey V, Logan JG, Lindsay SW. Are topical insect repellents effective against malaria in endemic populations? A systematic review and meta-analysis. Malar J. 2014;13:446.CrossRefPubMedPubMedCentral
62.
go back to reference Maia MF, Onyango SP, Thele M, Simfukwe E, Turner E, Moore SJ. Do topical repellents divert mosquitoes within a community? Health equity implications of topical repellents as a mosquito bite prevention tool. PLoS ONE. 2013;8:e84875.CrossRefPubMedPubMedCentral Maia MF, Onyango SP, Thele M, Simfukwe E, Turner E, Moore SJ. Do topical repellents divert mosquitoes within a community? Health equity implications of topical repellents as a mosquito bite prevention tool. PLoS ONE. 2013;8:e84875.CrossRefPubMedPubMedCentral
63.
go back to reference Govella NJ, Ogoma SB, Paliga J, Chaki PP, Killeen GF. Impregnating hessian strips with the volatile pyrethroid transfluthrin prevents outdoor exposure to vectors of malaria and lymphatic filariasis in urban Dar es Salaam. Parasit Vectors. 2015;8:322.CrossRefPubMedPubMedCentral Govella NJ, Ogoma SB, Paliga J, Chaki PP, Killeen GF. Impregnating hessian strips with the volatile pyrethroid transfluthrin prevents outdoor exposure to vectors of malaria and lymphatic filariasis in urban Dar es Salaam. Parasit Vectors. 2015;8:322.CrossRefPubMedPubMedCentral
64.
go back to reference Chaccour CJ, Rabinovich NR, Slater H, Canavati SE, Bousema T, Lacerda M, et al. Establishment of the Ivermectin research for malaria elimination network: updating the research agenda. Malar J. 2015;14:243.CrossRefPubMedPubMedCentral Chaccour CJ, Rabinovich NR, Slater H, Canavati SE, Bousema T, Lacerda M, et al. Establishment of the Ivermectin research for malaria elimination network: updating the research agenda. Malar J. 2015;14:243.CrossRefPubMedPubMedCentral
65.
go back to reference Xue RD, Barnard DR. Human host avidity in Aedes albopictus. influence of mosquito body size, age, parity, and time of day. J Am Mosq Control Assoc. 1996;12:58–63.PubMed Xue RD, Barnard DR. Human host avidity in Aedes albopictus. influence of mosquito body size, age, parity, and time of day. J Am Mosq Control Assoc. 1996;12:58–63.PubMed
66.
67.
go back to reference Govella NJ, Chaki PP, Killeen GF. Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations. Malar J. 2013;12:124.CrossRefPubMedPubMedCentral Govella NJ, Chaki PP, Killeen GF. Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations. Malar J. 2013;12:124.CrossRefPubMedPubMedCentral
68.
go back to reference Maliti DF, Marsden CD, Main BJ, Govella NJ, Yamasaki Y, Collier TC, et al. Investigating associations between biting time in the malaria vector Anopheles arabiensis Patton and single nucleotidepolymorphisms in circadian clock genes: support for sub-structure among An. arabiensis in the Kilombero valley of Tanzania. Parasit Vectors. 2016;9:109.CrossRefPubMedPubMedCentral Maliti DF, Marsden CD, Main BJ, Govella NJ, Yamasaki Y, Collier TC, et al. Investigating associations between biting time in the malaria vector Anopheles arabiensis Patton and single nucleotidepolymorphisms in circadian clock genes: support for sub-structure among An. arabiensis in the Kilombero valley of Tanzania. Parasit Vectors. 2016;9:109.CrossRefPubMedPubMedCentral
69.
go back to reference Kampango A, Cuamba N, Charlwood JD. Does moonlight influence the biting behaviour of Anopheles funestus. Med Vet Entomol. 2011;25:240–6.CrossRefPubMed Kampango A, Cuamba N, Charlwood JD. Does moonlight influence the biting behaviour of Anopheles funestus. Med Vet Entomol. 2011;25:240–6.CrossRefPubMed
70.
go back to reference Davies JB. Moonlight and the biting activity of Culex (Melanoconion) portesi Senevet & Abonnenc aud C. (M.) taeniopus D. & K. (Diptera, Culicidae) in Trinidad forests. Bull Entomol Res. 1975;65:81–96.CrossRef Davies JB. Moonlight and the biting activity of Culex (Melanoconion) portesi Senevet & Abonnenc aud C. (M.) taeniopus D. & K. (Diptera, Culicidae) in Trinidad forests. Bull Entomol Res. 1975;65:81–96.CrossRef
Metadata
Title
Bites before and after bedtime can carry a high risk of human malaria infection
Publication date
01-12-2017
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1740-0

Other articles of this Issue 1/2017

Malaria Journal 1/2017 Go to the issue