Kelly-Hope LA, Hemingway J, McKenzie FE, 2009. Environmental factors associated with the malaria vectors Anopheles gambiae and Anopheles funestus in Kenya. Malar J 8: 268.
Coetzee M, Fontenille D, 2004. Advances in the study of Anopheles funestus, a major vector of malaria in Africa. Insect Biochem Mol Biol 34: 599–605.
Gillies M, DeMeillon B, 1968. The Anophelinae South of the Sahara (Ethiopian Zoological Region). Johannesburg, South Africa: South African Institute for Medical Research.
Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M, 2000. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 14: 181–189.
Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH, Gething PW, Kabaria CW, Okara RM, Van Boeckel T, Godfray HC, Harbach RE, Hay SI, 2010. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasit Vectors 3: 117.
Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, Seroney IK, Ofulla AV, Atieli FK, Ondijo SO, Genga IO, Odada PK, Situbi PA, Oloo JA, 1996. Some observations on the biting behavior of Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus and their implications for malaria control. Exp Parasitol 82: 306–315.
Curtis CF, 1996. An overview of mosquito biology, behaviour and importance. Ciba Found Symp 200: 3–7.
Ndenga B, Githeko A, Omukunda E, Munyekenye G, Atieli H, Wamai P, Mbogo C, Minakawa N, Zhou G, Yan G, 2006. Population dynamics of malaria vectors in western Kenya highlands. J Med Entomol 43: 200–206.
Githeko AK, Ayisi JM, Odada PK, Atieli FK, Ndenga BA, Githure JI, Yan G, 2006. Topography and malaria transmission heterogeneity in western Kenya highlands: prospects for focal vector control. Malar J 5: 107.
Fontaine RE, Pull JH, Payne D, Pradhan GD, Joshi GP, Pearson JA, Thymakis MK, Camacho ME, 1978. Evaluation of fenitrothion for the control of malaria. Bull World Health Organ 56: 445–452.
Gimnig JE, Kolczak MS, Hightower AW, Vulule JM, Schoute E, Kamau L, Phillips-Howard PA, ter Kuile FO, Nahlen BL, Hawley WA, 2003. Effect of permethrin-treated bed nets on the spatial distribution of malaria vectors in western Kenya. Am J Trop Med Hyg 68: 115–120.
Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA, 2003. Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg 68: 16–22.
Killeen GF, Fillinger U, Knols BG, 2002. Advantages of larval control for African malaria vectors: low mobility and behavioural responsiveness of immature mosquito stages allow high effective coverage. Malar J 1: 8.
Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF, Beier JC, 2000. The potential impact of integrated malaria transmission control on entomologic inoculation rate in highly endemic areas. Am J Trop Med Hyg 62: 545–551.
Shililu J, Ghebremeskel T, Mengistu S, Fekadu H, Zerom M, Mbogo C, Githure J, Novak R, Brantly E, Beier JC, 2003. High seasonal variation in entomologic inoculation rates in Eritrea, a semi-arid region of unstable malaria in Africa. Am J Trop Med Hyg 69: 607–613.
Utzinger J, Tanner M, Kammen DM, Killeen GF, Singer BH, 2002. Integrated programme is key to malaria control. Nature 419: 431.
Norris LC, Norris DE, 2013. Heterogeneity and changes in inequality of malaria risk after introduction of insecticide-treated bed nets in Macha, Zambia. Am J Trop Med Hyg 88: 710–717.
Norris LC, Fornadel CM, Hung WC, Pineda FJ, Norris DE, 2010. Frequency of multiple blood meals taken in a single gonotrophic cycle by Anopheles arabiensis mosquitoes in Macha, Zambia. Am J Trop Med Hyg 83: 33–37.
Ngufor C, N'Guessan R, Boko P, Odjo A, Vigninou E, Asidi A, Akogbeto M, Rowland M, 2011. Combining indoor residual spraying with chlorfenapyr and long-lasting insecticidal bed nets for improved control of pyrethroid-resistant Anopheles gambiae: an experimental hut trial in Benin. Malar J 10: 343.
Giardina F, Kasasa S, Sie A, Utzinger J, Tanner M, Vounatsou P, 2014. Effects of vector-control interventions on changes in risk of malaria parasitaemia in sub-Saharan Africa: a spatial and temporal analysis. Lancet Glob Health 2: e601–e615.
West PA, Protopopoff N, Wright A, Kivaju Z, Tigererwa R, Mosha FW, Kisinza W, Rowland M, Kleinschmidt I, 2015. Enhanced protection against malaria by indoor residual spraying in addition to insecticide treated nets: is it dependent on transmission intensity or net usage? PLoS One 10: e0115661.
Mukonka VM, Chanda E, Haque U, Kamuliwo M, Mushinge G, Chileshe J, Chibwe KA, Norris DE, Mulenga M, Chaponda M, Muleba M, Glass GE, Moss WJ, 2014. High burden of malaria following scale-up of control interventions in Nchelenge District, Luapula Province, Zambia. Malar J 13: 153.
Gillies MT, Coetzee M, 1987. A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region). Johannesburg, South Africa: South African Institute for Medical Research.
Kent RJ, Norris DE, 2005. Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg 73: 336–342.
Cohuet A, Simard F, Toto JC, Kengne P, Coetzee M, Fontenille D, 2003. Species identification within the Anopheles funestus group of malaria vectors in Cameroon and evidence for a new species. Am J Trop Med Hyg 69: 200–205.
Koekemoer LL, Kamau L, Hunt RH, Coetzee M, 2002. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg 66: 804–811.
Scott JA, Brogdon WG, Collins FH, 1993. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49: 520–529.
Spillings BL, Brooke BD, Koekemoer LL, Chiphwanya J, Coetzee M, Hunt RH, 2009. A new species concealed by Anopheles funestus Giles, a major malaria vector in Africa. Am J Trop Med Hyg 81: 510–515.
Favia G, Lanfrancotti A, Spanos L, Siden-Kiamos I, Louis C, 2001. Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Mol Biol 10: 19–23.
Kent RJ, Thuma PE, Mharakurwa S, Norris DE, 2007. Seasonality, blood feeding behavior, and transmission of Plasmodium falciparum by Anopheles arabiensis after an extended drought in southern Zambia. Am J Trop Med Hyg 76: 267–274.
Fornadel CM, Norris LC, Glass GE, Norris DE, 2010. Analysis of Anopheles arabiensis blood feeding behavior in southern Zambia during the two years after introduction of insecticide-treated bed nets. Am J Trop Med Hyg 83: 848–853.
Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, Thaithong S, Brown KN, 1993. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61: 315–320.
Fornadel CM, Norris LC, Franco V, Norris DE, 2011. Unexpected anthropophily in the potential secondary malaria vectors Anopheles coustani s.l. and Anopheles squamosus in Macha, Zambia. Vector Borne Zoonotic Dis 11: 1173–1179.
Fornadel CM, Norris LC, Norris DE, 2010. Centers for Disease Control light traps for monitoring Anopheles arabiensis human biting rates in an area with low vector density and high insecticide-treated bed net use. Am J Trop Med Hyg 83: 838–842.
Magbity EB, Lines JD, Marbiah MT, David K, Peterson E, 2002. How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets? Bull Entomol Res 92: 71–76.
Mathenge EM, Omweri GO, Irungu LW, Ndegwa PN, Walczak E, Smith TA, Killeen GF, Knols BG, 2004. Comparative field evaluation of the Mbita trap, the Centers for Disease Control light trap, and the human landing catch for sampling of malaria vectors in western Kenya. Am J Trop Med Hyg 70: 33–37.
Mboera LE, 2005. Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rate. Tanzan Health Res Bull 7: 117–124.
Das S, Henning TC, Simubali L, Hamapumbu H, Nzira L, Mamini E, Makuwaza A, Muleba M, Norris DE, Stevenson JC, 2015. Underestimation of foraging behaviour by standard field methods in malaria vector mosquitoes in southern Africa. Malar J 14: 12.
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Nchelenge District in Luapula Province, northern Zambia, experiences holoendemic malaria despite implementation of vector control programs. The major Anopheles vectors that contribute to Plasmodium falciparum transmission in this area had not previously been well defined. Three collections performed during the 2012 wet and dry seasons and the 2013 wet season revealed Anopheles funestus sensu stricto and Anopheles gambiae sensu stricto as the main vectors, where 80–85% of each collection was composed of An. funestus. Both vectors were found to be highly anthropophilic, and An. funestus has higher sporozoite infection rates (SIRs) and entomological inoculation rates (EIRs) year-round compared with An. gambiae: SIRs of 1.8–3.0% and 0–2.5%, respectively, and EIRs of 3.7–41.5 infectious bites per 6-month period (ib/p/6mo) and 0–5.9 ib/p/6mo, respectively. Spatial and temporal changes in each vector's dynamics and bionomics were also observed. Anopheles funestus was the predominant vector in the villages near Kenani Stream in both wet and dry seasons, whereas An. gambiae was found to be the main vector in areas near Lake Mweru during the wet season. The vector data illustrate the need for broader temporal and spatial sampling in Nchelenge and present unique opportunities to further our understanding of malarial transmission and implications for malarial control in high-risk areas.
Financial support: This work was supported in part, through funding from the Southern Africa International Centers of Excellence for Malaria Research (U19AI089680-01) to Douglas E. Norris. Smita Das was supported by a National Institutes of Health T32 Grant (2T32AI007417-16) and the Martin Frobisher Fellowship Fund from the W. Harry Feinstone Department of Molecular Microbiology and Immunology, a Johns Hopkins Malaria Research Institute Fellowship from the Johns Hopkins Malaria Research Institute, and a Johns Hopkins Global Health Established Field Placement Award from the Johns Hopkins Center for Global Health, Johns Hopkins University Bloomberg School of Public Health.
Authors' addresses: Smita Das and Douglas E. Norris, W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, E-mails: smita.das988@gmail.com and douglas.norris@jhu.edu. Mbanga Muleba, Tropical Disease Research Centre, Ndola Central Hospital, Ndola, Zambia, E-mail: MulebaM@tdrc.org.zm. Jennifer C. Stevenson, W. Harry Feinstone Department of Molecular Microbiology and Immunology, The Johns Hopkins Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, and Macha Research Trust, Choma, Zambia, E-mail: jennyc.stevenson@macharesearch.org.
Kelly-Hope LA, Hemingway J, McKenzie FE, 2009. Environmental factors associated with the malaria vectors Anopheles gambiae and Anopheles funestus in Kenya. Malar J 8: 268.
Coetzee M, Fontenille D, 2004. Advances in the study of Anopheles funestus, a major vector of malaria in Africa. Insect Biochem Mol Biol 34: 599–605.
Gillies M, DeMeillon B, 1968. The Anophelinae South of the Sahara (Ethiopian Zoological Region). Johannesburg, South Africa: South African Institute for Medical Research.
Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M, 2000. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 14: 181–189.
Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH, Gething PW, Kabaria CW, Okara RM, Van Boeckel T, Godfray HC, Harbach RE, Hay SI, 2010. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasit Vectors 3: 117.
Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, Seroney IK, Ofulla AV, Atieli FK, Ondijo SO, Genga IO, Odada PK, Situbi PA, Oloo JA, 1996. Some observations on the biting behavior of Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus and their implications for malaria control. Exp Parasitol 82: 306–315.
Curtis CF, 1996. An overview of mosquito biology, behaviour and importance. Ciba Found Symp 200: 3–7.
Ndenga B, Githeko A, Omukunda E, Munyekenye G, Atieli H, Wamai P, Mbogo C, Minakawa N, Zhou G, Yan G, 2006. Population dynamics of malaria vectors in western Kenya highlands. J Med Entomol 43: 200–206.
Githeko AK, Ayisi JM, Odada PK, Atieli FK, Ndenga BA, Githure JI, Yan G, 2006. Topography and malaria transmission heterogeneity in western Kenya highlands: prospects for focal vector control. Malar J 5: 107.
Fontaine RE, Pull JH, Payne D, Pradhan GD, Joshi GP, Pearson JA, Thymakis MK, Camacho ME, 1978. Evaluation of fenitrothion for the control of malaria. Bull World Health Organ 56: 445–452.
Gimnig JE, Kolczak MS, Hightower AW, Vulule JM, Schoute E, Kamau L, Phillips-Howard PA, ter Kuile FO, Nahlen BL, Hawley WA, 2003. Effect of permethrin-treated bed nets on the spatial distribution of malaria vectors in western Kenya. Am J Trop Med Hyg 68: 115–120.
Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA, 2003. Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg 68: 16–22.
Killeen GF, Fillinger U, Knols BG, 2002. Advantages of larval control for African malaria vectors: low mobility and behavioural responsiveness of immature mosquito stages allow high effective coverage. Malar J 1: 8.
Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF, Beier JC, 2000. The potential impact of integrated malaria transmission control on entomologic inoculation rate in highly endemic areas. Am J Trop Med Hyg 62: 545–551.
Shililu J, Ghebremeskel T, Mengistu S, Fekadu H, Zerom M, Mbogo C, Githure J, Novak R, Brantly E, Beier JC, 2003. High seasonal variation in entomologic inoculation rates in Eritrea, a semi-arid region of unstable malaria in Africa. Am J Trop Med Hyg 69: 607–613.
Utzinger J, Tanner M, Kammen DM, Killeen GF, Singer BH, 2002. Integrated programme is key to malaria control. Nature 419: 431.
Norris LC, Norris DE, 2013. Heterogeneity and changes in inequality of malaria risk after introduction of insecticide-treated bed nets in Macha, Zambia. Am J Trop Med Hyg 88: 710–717.
Norris LC, Fornadel CM, Hung WC, Pineda FJ, Norris DE, 2010. Frequency of multiple blood meals taken in a single gonotrophic cycle by Anopheles arabiensis mosquitoes in Macha, Zambia. Am J Trop Med Hyg 83: 33–37.
Ngufor C, N'Guessan R, Boko P, Odjo A, Vigninou E, Asidi A, Akogbeto M, Rowland M, 2011. Combining indoor residual spraying with chlorfenapyr and long-lasting insecticidal bed nets for improved control of pyrethroid-resistant Anopheles gambiae: an experimental hut trial in Benin. Malar J 10: 343.
Giardina F, Kasasa S, Sie A, Utzinger J, Tanner M, Vounatsou P, 2014. Effects of vector-control interventions on changes in risk of malaria parasitaemia in sub-Saharan Africa: a spatial and temporal analysis. Lancet Glob Health 2: e601–e615.
West PA, Protopopoff N, Wright A, Kivaju Z, Tigererwa R, Mosha FW, Kisinza W, Rowland M, Kleinschmidt I, 2015. Enhanced protection against malaria by indoor residual spraying in addition to insecticide treated nets: is it dependent on transmission intensity or net usage? PLoS One 10: e0115661.
Mukonka VM, Chanda E, Haque U, Kamuliwo M, Mushinge G, Chileshe J, Chibwe KA, Norris DE, Mulenga M, Chaponda M, Muleba M, Glass GE, Moss WJ, 2014. High burden of malaria following scale-up of control interventions in Nchelenge District, Luapula Province, Zambia. Malar J 13: 153.
Gillies MT, Coetzee M, 1987. A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region). Johannesburg, South Africa: South African Institute for Medical Research.
Kent RJ, Norris DE, 2005. Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg 73: 336–342.
Cohuet A, Simard F, Toto JC, Kengne P, Coetzee M, Fontenille D, 2003. Species identification within the Anopheles funestus group of malaria vectors in Cameroon and evidence for a new species. Am J Trop Med Hyg 69: 200–205.
Koekemoer LL, Kamau L, Hunt RH, Coetzee M, 2002. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg 66: 804–811.
Scott JA, Brogdon WG, Collins FH, 1993. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49: 520–529.
Spillings BL, Brooke BD, Koekemoer LL, Chiphwanya J, Coetzee M, Hunt RH, 2009. A new species concealed by Anopheles funestus Giles, a major malaria vector in Africa. Am J Trop Med Hyg 81: 510–515.
Favia G, Lanfrancotti A, Spanos L, Siden-Kiamos I, Louis C, 2001. Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Mol Biol 10: 19–23.
Kent RJ, Thuma PE, Mharakurwa S, Norris DE, 2007. Seasonality, blood feeding behavior, and transmission of Plasmodium falciparum by Anopheles arabiensis after an extended drought in southern Zambia. Am J Trop Med Hyg 76: 267–274.
Fornadel CM, Norris LC, Glass GE, Norris DE, 2010. Analysis of Anopheles arabiensis blood feeding behavior in southern Zambia during the two years after introduction of insecticide-treated bed nets. Am J Trop Med Hyg 83: 848–853.
Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, Thaithong S, Brown KN, 1993. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61: 315–320.
Fornadel CM, Norris LC, Franco V, Norris DE, 2011. Unexpected anthropophily in the potential secondary malaria vectors Anopheles coustani s.l. and Anopheles squamosus in Macha, Zambia. Vector Borne Zoonotic Dis 11: 1173–1179.
Fornadel CM, Norris LC, Norris DE, 2010. Centers for Disease Control light traps for monitoring Anopheles arabiensis human biting rates in an area with low vector density and high insecticide-treated bed net use. Am J Trop Med Hyg 83: 838–842.
Magbity EB, Lines JD, Marbiah MT, David K, Peterson E, 2002. How reliable are light traps in estimating biting rates of adult Anopheles gambiae s.l. (Diptera: Culicidae) in the presence of treated bed nets? Bull Entomol Res 92: 71–76.
Mathenge EM, Omweri GO, Irungu LW, Ndegwa PN, Walczak E, Smith TA, Killeen GF, Knols BG, 2004. Comparative field evaluation of the Mbita trap, the Centers for Disease Control light trap, and the human landing catch for sampling of malaria vectors in western Kenya. Am J Trop Med Hyg 70: 33–37.
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