World Health Organization, 2012. World Malaria Report 2012. Geneva: World Health Organization, 60–62.
Feachem RG, Phillips AA, Hwang J, Cotter C, Wielgosz B, Greenwood BM, Sabot O, Rodríguez MH, Abeyasinghe RR, Ghebreyesus TA, Snow RW, 2010. Shrinking the malaria map: progress and prospects. Lancet 376: 1566–1578.
Nájera JA, González-Silva M, Alonso PL, 2011. Some lessons for the future from the Global Malaria Eradication Programme (1955–1969). PLoS Med 8: e1000412.
Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, Himeidan YE, Minakawa N, Githeko AK, Yan G, 2011. Changing patterns of malaria epidemiology between 2002 and 2010 in western Kenya: the fall and rise of malaria. PLoS ONE 6: e20318.
Hamel MJ, Adazu K, Obor D, Sewe M, Vulule JM, Williamson JM, Slutsker L, Feikin DR, Laserson KF, 2011. A reversal in reductions of child mortality in western Kenya, 2003–2009. Am J Trop Med Hyg 85: 597–605.
Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, Vulule JM, Hawley WA, Hamel MJ, Walker ED, 2010. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9: 62.
Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M, Nahlen BL, Gimnig JE, Kariuki SK, Kolczak MS, Hightower AW, 2003. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg 68 (Suppl 4): 121–127.
Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V, 2011. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 91–98.
Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Touré-Baldé A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C, 2011. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis 11: 925–932.
Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, Whitmire RE, Koech DK, Roberts CR, 1990. Characterization of malaria transmission by Anopheles (Diptera: Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol 27: 570–577.
Taylor KA, Koros JK, Nduati J, Copeland RS, Collins FH, Brandling-Bennett AD, 1990. Plasmodium falciparum infection rates in Anopheles gambiae, An. arabiensis, and An. funestus in western Kenya. Am J Trop Med Hyg 43: 124–129.
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 (Suppl 4): 16–22.
Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, ter Kuile FO, Hawley WA, Wannemuehler KA, Phillips-Howard PA, Rosen DH, Nahlen BL, Terlouw DJ, Adazu K, Vulule JM, Slutsker L, 2004. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bed nets: 4 to 6 years of follow-up. JAMA 291: 2571–2580.
Vulule JM, Beach RF, Atieli FK, Roberts JM, Mount DL, Mwangi RW, 1994. Reduced susceptibility of Anopheles gambiae to permethrin associated with the use of permethrin-impregnated bednets and curtains in Kenya. Med Vet Entomol 8: 71–75.
Mathias DK, Ochomo E, Atieli FK, Ombok M, Bayoh MN, Olang G, Muhia D, Kamau L, Vulule JM, Hamel MJ, Hawley WA, Walker ED, Gimnig JE, 2011. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in western Kenya. Malar J 10: 10.
Ochomo E, Bayoh MN, Brogdon WG, Gimnig JE, Ouma C, Vulule JM, Walker ED, 2013. Pyrethroid resistance in Anopheles gambiae s.s. and Anopheles arabiensis in western Kenya: phenotypic, metabolic and target site characterizations of three populations. Med Vet Entomol 27: 156–164.
Coetzee M, Hunt RH, Wilkerson RC, della Torre A, Coulibaly MB, Besansky NJ, 2013. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619: 246–274.
Coetzee M, Koekemoer LL, 2013. Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. Annu Rev Entomol 58: 393–412.
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.
Phillips-Howard PA, Nahlen BL, Alaii JA, ter Kuile FO, Gimnig JE, Terlouw DJ, Kachur SP, Hightower AW, Lal AA, Schoute E, Oloo AJ, Hawley WA, 2003. 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 68 (Suppl 4): 3–9.
Gimnig JE, Walker ED, Otieno P, Kosgei J, Olang G, Ombok M, Williamson J, Marwanga D, Abong'o D, Desai M, Kariuki S, Hamel MJ, Lobo NF, Vulule JM, Bayoh MN, 2013. Incidence of malaria among mosquito collectors conducting human landing catches in western Kenya. Am J Trop Med Hyg 88: 301–308.
Odiere M, Bayoh MN, Gimnig JE, Vulule JM, Irungu L, Walker ED, 2007. Sampling outdoor, resting Anopheles gambiae and other mosquitoes (Diptera: Culicidae) in western Kenya with clay pots. J Med Entomol 44: 14–22.
Noor AM, Amin AA, Akhwale WS, Snow RW, 2007. Increasing coverage and decreasing inequity in insecticide-treated bed net use among rural Kenyan children. PLoS Med 4: e255.
Division of Malaria Control, 2009. National Malaria Strategy 2009–2017. Nairobi, Kenya: Ministry of Public Health and Sanitation, 25.
Wong J, Bayoh MN, Olang G, Killeen GF, Hamel MJ, Vulule JM, Gimnig JE, 2013. Standardizing operational vector sampling techniques for measuring malaria transmission intensity: evaluation of six mosquito collection methods in western Kenya. Malar J 12: 143.
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, 1–143.
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.
Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, Esser KM, Beaudoin RL, Andre RG, 1987. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ 65: 39.
Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Walker ED, 2008. Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile Virus to humans. J Med Entomol 45: 125–128.
World Health Organization, 1998. Test Procedures for Insecticide Resistance Monitoring in Malaria Vectors, Bio-Efficacy and Persistence of Insecticides on Treated Surfaces. Report of the WHO Informal Consultation. Geneva: World Health Organization, 1–46.
Evans AM, Symes CB, 1937. Anopheles funestus and its allies in Kenya. Ann Trop Med Parasitol 31: 105–112.
Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, ter Kuile FO, Vulule JM, Slutsker L, 2006. Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol 43: 428–432.
Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS, 2010. Pyrethroid resistance in an Anopheles funestus population from Uganda. PLoS ONE 5: e11872.
Busvine JR, Pal R, 1969. The impact of insecticide-resistance on control of vectors and vector-borne diseases. Bull World Health Organ 40: 731–744.
Garrett-Jones C, 1964. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ 30: 241–261.
Takken W, Verhulst NO, 2013. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol 58: 433–453.
World Health Organization, 2004. Global Strategic Framework for Integrated Vector Management. Geneva: World Health Organization, 1–12.
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Abstract Views | 2296 | 1877 | 415 |
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Historically, the malaria vectors in western Kenya have been Anopheles funestus, Anopheles gambiae s.s., and Anopheles arabiensis. Of these species, An. funestus populations declined the most after the introduction of insecticide-treated bed nets (ITNs) in the 1990s in Asembo, and collections of An. funestus in the region remained low until at least 2008. Contrary to findings during the early years of ITN use in Asembo, the majority of the Anopheles collected here in 2010 and 2011 were An. funestus. Female An. funestus had characteristically high Plasmodium falciparum sporozoite rates and showed nearly 100% anthropophily. Female An. funestus were found more often indoors than outdoors and had relatively low mortality rates during insecticide bioassays. Together, these results are of serious concern for public health in the region, indicating that An. funestus may once again be contributing significantly to the transmission of malaria in this region despite the widespread use of ITNs/long-lasting insecticidal nets (LLINs).
Financial support: This study was supported by a National Science Foundation Ecology of Infectious Diseases grant (grant no. EF-0723770) and NIAID Grant U01AI0508542 with additional support from the Rhodes Thompson Memorial Fellowship Fund.
Authors' addresses: Robert S. McCann, Department of Entomology, Michigan State University, East Lansing, MI, E-mail: mccannr3@msu.edu. Eric Ochomo and M. Nabie Bayoh, Kenya Medical Research Institute/Centers for Disease Control and Prevention Research and Public Health Collaboration, Kisumu, Kenya, E-mails: eochomo@kemricdc.org and nbayoh@kemricdc.org. John M. Vulule, Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya, E-mail: jvulule@kemricdc.org. Mary J. Hamel, John E. Gimnig, and William A. Hawley, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: mhamel@cdc.gov, jgimnig@cdc.gov, and whawley@cdc.gov. Edward D. Walker, Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, E-mail: walker@msu.edu.
World Health Organization, 2012. World Malaria Report 2012. Geneva: World Health Organization, 60–62.
Feachem RG, Phillips AA, Hwang J, Cotter C, Wielgosz B, Greenwood BM, Sabot O, Rodríguez MH, Abeyasinghe RR, Ghebreyesus TA, Snow RW, 2010. Shrinking the malaria map: progress and prospects. Lancet 376: 1566–1578.
Nájera JA, González-Silva M, Alonso PL, 2011. Some lessons for the future from the Global Malaria Eradication Programme (1955–1969). PLoS Med 8: e1000412.
Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, Himeidan YE, Minakawa N, Githeko AK, Yan G, 2011. Changing patterns of malaria epidemiology between 2002 and 2010 in western Kenya: the fall and rise of malaria. PLoS ONE 6: e20318.
Hamel MJ, Adazu K, Obor D, Sewe M, Vulule JM, Williamson JM, Slutsker L, Feikin DR, Laserson KF, 2011. A reversal in reductions of child mortality in western Kenya, 2003–2009. Am J Trop Med Hyg 85: 597–605.
Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, Vulule JM, Hawley WA, Hamel MJ, Walker ED, 2010. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9: 62.
Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M, Nahlen BL, Gimnig JE, Kariuki SK, Kolczak MS, Hightower AW, 2003. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg 68 (Suppl 4): 121–127.
Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V, 2011. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 27: 91–98.
Trape J-F, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A, Sarr FD, Mazenot C, Touré-Baldé A, Raoult D, Druilhe P, Mercereau-Puijalon O, Rogier C, Sokhna C, 2011. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis 11: 925–932.
Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, Whitmire RE, Koech DK, Roberts CR, 1990. Characterization of malaria transmission by Anopheles (Diptera: Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol 27: 570–577.
Taylor KA, Koros JK, Nduati J, Copeland RS, Collins FH, Brandling-Bennett AD, 1990. Plasmodium falciparum infection rates in Anopheles gambiae, An. arabiensis, and An. funestus in western Kenya. Am J Trop Med Hyg 43: 124–129.
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 (Suppl 4): 16–22.
Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, ter Kuile FO, Hawley WA, Wannemuehler KA, Phillips-Howard PA, Rosen DH, Nahlen BL, Terlouw DJ, Adazu K, Vulule JM, Slutsker L, 2004. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bed nets: 4 to 6 years of follow-up. JAMA 291: 2571–2580.
Vulule JM, Beach RF, Atieli FK, Roberts JM, Mount DL, Mwangi RW, 1994. Reduced susceptibility of Anopheles gambiae to permethrin associated with the use of permethrin-impregnated bednets and curtains in Kenya. Med Vet Entomol 8: 71–75.
Mathias DK, Ochomo E, Atieli FK, Ombok M, Bayoh MN, Olang G, Muhia D, Kamau L, Vulule JM, Hamel MJ, Hawley WA, Walker ED, Gimnig JE, 2011. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in western Kenya. Malar J 10: 10.
Ochomo E, Bayoh MN, Brogdon WG, Gimnig JE, Ouma C, Vulule JM, Walker ED, 2013. Pyrethroid resistance in Anopheles gambiae s.s. and Anopheles arabiensis in western Kenya: phenotypic, metabolic and target site characterizations of three populations. Med Vet Entomol 27: 156–164.
Coetzee M, Hunt RH, Wilkerson RC, della Torre A, Coulibaly MB, Besansky NJ, 2013. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619: 246–274.
Coetzee M, Koekemoer LL, 2013. Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. Annu Rev Entomol 58: 393–412.
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.
Phillips-Howard PA, Nahlen BL, Alaii JA, ter Kuile FO, Gimnig JE, Terlouw DJ, Kachur SP, Hightower AW, Lal AA, Schoute E, Oloo AJ, Hawley WA, 2003. 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 68 (Suppl 4): 3–9.
Gimnig JE, Walker ED, Otieno P, Kosgei J, Olang G, Ombok M, Williamson J, Marwanga D, Abong'o D, Desai M, Kariuki S, Hamel MJ, Lobo NF, Vulule JM, Bayoh MN, 2013. Incidence of malaria among mosquito collectors conducting human landing catches in western Kenya. Am J Trop Med Hyg 88: 301–308.
Odiere M, Bayoh MN, Gimnig JE, Vulule JM, Irungu L, Walker ED, 2007. Sampling outdoor, resting Anopheles gambiae and other mosquitoes (Diptera: Culicidae) in western Kenya with clay pots. J Med Entomol 44: 14–22.
Noor AM, Amin AA, Akhwale WS, Snow RW, 2007. Increasing coverage and decreasing inequity in insecticide-treated bed net use among rural Kenyan children. PLoS Med 4: e255.
Division of Malaria Control, 2009. National Malaria Strategy 2009–2017. Nairobi, Kenya: Ministry of Public Health and Sanitation, 25.
Wong J, Bayoh MN, Olang G, Killeen GF, Hamel MJ, Vulule JM, Gimnig JE, 2013. Standardizing operational vector sampling techniques for measuring malaria transmission intensity: evaluation of six mosquito collection methods in western Kenya. Malar J 12: 143.
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, 1–143.
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.
Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, Esser KM, Beaudoin RL, Andre RG, 1987. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ 65: 39.
Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Walker ED, 2008. Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile Virus to humans. J Med Entomol 45: 125–128.
World Health Organization, 1998. Test Procedures for Insecticide Resistance Monitoring in Malaria Vectors, Bio-Efficacy and Persistence of Insecticides on Treated Surfaces. Report of the WHO Informal Consultation. Geneva: World Health Organization, 1–46.
Evans AM, Symes CB, 1937. Anopheles funestus and its allies in Kenya. Ann Trop Med Parasitol 31: 105–112.
Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, ter Kuile FO, Vulule JM, Slutsker L, 2006. Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol 43: 428–432.
Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS, 2010. Pyrethroid resistance in an Anopheles funestus population from Uganda. PLoS ONE 5: e11872.
Busvine JR, Pal R, 1969. The impact of insecticide-resistance on control of vectors and vector-borne diseases. Bull World Health Organ 40: 731–744.
Garrett-Jones C, 1964. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ 30: 241–261.
Takken W, Verhulst NO, 2013. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol 58: 433–453.
World Health Organization, 2004. Global Strategic Framework for Integrated Vector Management. Geneva: World Health Organization, 1–12.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 2296 | 1877 | 415 |
Full Text Views | 520 | 18 | 3 |
PDF Downloads | 170 | 16 | 0 |