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 bednets: 4 to 6 years of follow-up. JAMA 291: 2571–2580.
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.
Miller JE, Lindsay SW, Armstrong JR, 1991. Experimental hut trials of bednets impregnated with synthetic pyrethroid or organophosphate insecticide for mosquito control in the Gambia. Med Vet Entomol 5: 465–476.
Bayoh M, Walker E, Kosgei J, Ombok M, Olang G, Githeko A, Killeen G, Otieno P, Desai M, Lobo N, Vulule J, Hamel M, Kariuki S, Gimnig J, 2014. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasit Vectors 7: 380.
Antonio-Nkondjio C, Kerah CH, Simard F, Awono-Ambene P, Chouaibou M, Tchuinkam T, Fontenille D, 2006. Complexity of the malaria vectorial system in Cameroon: contribution of secondary vectors to malaria transmission. J Med Entomol 43: 1215–1221.
Gillies MT, de Meillon B, 1968. The Anopheline of Africa South of the Sahara. Johannesburg, South Africa: South African Institute of Medical Research.
Coetzee M, Hunt RH, Wilkerson R, Torre AD, Coulibaly MB, Besansky NJ, 2013. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619: 246–274.
Koekemoer L, Kamau L, Hunt R, 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.
Collins FH, Paskewitz SM, 1996. A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Mol Biol 5: 1–9.
Coetzee M, Craig M, le Sueur D, 2000. Distribution of African malaria mosquitoes belonging to the Anopheles gambiae complex. Parasitol Today 16: 74–77.
Pates HV, Takken W, Curtis CF, Jamet H, 2006. Zoophilic Anopheles quadriannulatus species B found in a human habitation in Ethiopia. Ann Trop Med Parasitol 100: 177–179.
Fettene M, Hunt R, Coetzee M, Tessema F, 2004. Behaviour of Anopheles arabiensis and An. quadriannulatus sp. B mosquitoes and malaria transmission in southwestern Ethiopia. Afr Entomol 12: 83–87.
Petrarca V, Beier JC, Onyango F, Koros J, Asiago C, Koech DK, Roberts CR, 1991. Species composition of the Anopheles gambiae complex (Diptera: Culicidae) at two sites in western Kenya. J Med Entomol 28: 307–313.
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.
Sinka M, Bangs M, Manguin S, Coetzee M, Mbogo C, Hemingway J, 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.
Killeen G, Seyoum A, Sikaala C, Zomboko A, Gimnig J, Govella N, 2013. Eliminating malaria vectors. Parasit Vectors 6: 172.
Lwetoijera D, Harris C, Kiware S, Dongus S, Devine G, McCall P, Majambere S, 2014. Increasing role of Anopheles funestus and Anopheles arabiensis in malaria transmission in the Kilombero Valley, Tanzania. Malar J 13: 331.
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.
Rishikesh N, Di Deco MA, Petrarca V, Coluzzi M, 1985. Seasonal variations in indoor resting Anopheles gambiae and Anopheles arabiensis in Kaduna, Nigeria. Acta Trop 42: 165–170.
Mnzava AE, Rwegoshora RT, Wilkes TJ, Tanner M, Curtis CF, 1995. Anopheles arabiensis and An. gambiae chromosomal inversion polymorphism, feeding and resting behaviour in relation to insecticide house-spraying in Tanzania. Med Vet Entomol 9: 316–324.
Durnez L, Coosemans M, 2013. Residual Transmission of Malaria: An Old Issue for New Approaches. Rijeka, Croatia: InTech.
Pates H, Curtis C, 2005. Mosquito behavior and vector control. Annu Rev Entomol 50: 53–70.
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.
Kumar NP, Rajavel AR, Natarajan R, Jambulingam P, 2007. DNA barcodes can distinguish species of Indian mosquitoes (Diptera: Culicidae). J Med Entomol 44: 1–7.
Harbach RE, 2013. The phylogeny and classification of Anopheles. Manguin S, ed. Anopheles Mosquitoes—New Insights into Malaria Vectors. Rijeka, Croatia: InTech, 3–55.
Kelly-Hope L, Ranson H, Hemingway J, 2008. Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis 8: 387–389.
Okara RM, Sinka ME, Minakawa N, Mbogo CM, Hay SI, Snow RW, 2010. Distribution of the main malaria vectors in Kenya. Malar J 9: 69.
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.
Carlson JC, Byrd BD, Omlin FX, 2004. Field assessments in western Kenya link malaria vectors to environmentally disturbed habitats during the dry season. BMC Public Health 4: 33.
Ototo EN, Githeko AK, Wanjala CL, Scott TW, 2011. Surveillance of vector populations and malaria transmission during the 2009/10 El Nino event in the western Kenya highlands: opportunities for early detection of malaria hyper-transmission. Parasit Vectors 4: 144.
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.
Minakawa N, Omukunda E, Zhou G, Githeko A, Yan G, 2006. Malaria vector productivity in relation to the highland environment in Kenya. Am J Trop Med Hyg 75: 448–453.
Wanjala CL, Waitumbi J, Zhou G, Githeko AK, 2011. Identification of malaria transmission and epidemic hotspots in the western Kenya highlands: its application to malaria epidemic prediction. Parasit Vectors 4: 81.
Atieli HE, Zhou G, Lee MC, Kweka EJ, Afrane Y, Mwanzo I, Githeko AK, Yan G, 2011. Topography as a modifier of breeding habitats and concurrent vulnerability to malaria risk in the western Kenya highlands. Parasit Vectors 4: 241.
Minakawa N, Munga S, Atieli F, Mushinzimana E, Zhou G, Githeko AK, Yan G, 2005. Spatial distribution of anopheline larval habitats in western Kenyan highlands: effects of land cover types and topography. Am J Trop Med Hyg 73: 157–165.
Stuckey EM, Stevenson JC, Cooke MK, Owaga C, Marube E, Oando G, Hardy D, Drakeley C, Smith TA, Cox J, Chitnis N, 2012. Simulation of malaria epidemiology and control in the highlands of western Kenya. Malar J 11: 357.
Stevenson J, St Laurent B, Lobo NF, Cooke MK, Kahindi SC, Oriango RM, Harbach RE, Cox J, Drakeley C, 2012. Novel vectors of malaria parasites in the western highlands of Kenya. Emerg Infect Dis 18: 1547–1549.
Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G, 2015. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J 14: 244.
Cooke MK, Kahindi SC, Oriango RM, Owaga C, Ayoma E, Mabuka D, Nyangau D, Abel L, Atieno E, Awuor S, Drakeley C, Cox J, Stevenson J, 2015. “A bite before bed”: exposure to malaria vectors outside the times of net use in the highlands of western Kenya. Malar J 14: 259.
Silver JB, 2007. Mosquito Ecology: Field Sampling Methods. Dordrecht, The Netherlands: Springer Science and Business Media.
Gillies T, Coetzee M, 1987. A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region), Vol. 55. Johannesburg, South Africa: South African Institute for Medical Research.
Burkot TR, Zavala F, Gwadz RW, Collins FH, Nussenzweig RS, Roberts DR, 1984. Identification of malaria-infected mosquitoes by a two-site enzyme-linked immunosorbent assay. Am J Trop Med Hyg 33: 227–231.
Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA, 1999. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg 60: 687–692.
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.
Hostetter G, Collins E, Varlan P, Edewaard E, Harbach PR, Hudson EA, Feenstra KJ, Turner LM, Berghuis BD, Resau JH, Jewell SD, 2014. Veterinary and human biobanking practices: enhancing molecular sample integrity. Vet Pathol 51: 270–280.
Beebe NW, Saul A, 1995. Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction–restriction fragment length polymorphism analysis. Am J Trop Med Hyg 53: 478–481.
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3: 294–299.
Katoh K, Standley DM, 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780.
Katoh K, Toh H, 2008. Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 9: 212.
Ronquist F, Huelsenbeck JP, 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
Norris LC, Norris DE, 2015. Phylogeny of anopheline (Diptera: Culicidae) species in southern Africa, based on nuclear and mitochondrial genes. J Vector Ecol 40: 16–27.
Rubinoff D, Cameron S, Will K, 2006. A genomic perspective on the shortcomings of mitochondrial DNA for “barcoding” identification. J Hered 97: 581–594.
Lin CP, Danforth BN, 2004. How do insect nuclear and mitochondrial gene substitution patterns differ? Insights from Bayesian analyses of combined datasets. Mol Phylogenet Evol 30: 686–702.
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.
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.
Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, Sochantha T, Coosemans M, 2011. False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector incrimination. Malar J 10: 195.
Fillinger U, Ndenga B, Githeko A, Lindsay SW, 2009. Integrated malaria vector control with microbial larvicides and insecticide-treated nets in western Kenya: a controlled trial. Bull World Health Organ 87: 655–665.
Kawada H, Dida GO, Sonye G, Njenga SM, Mwandawiro C, Minakawa N, 2012. Reconsideration of Anopheles rivulorum as a vector of Plasmodium falciparum in western Kenya: some evidence from biting time, blood preference, sporozoite positive rate, and pyrethroid resistance. Parasit Vectors 5: 230.
Brady OJ, Godfray HCJ, Tatem AJ, Gething PW, Cohen JM, McKenzie FE, Alex Perkins T, Reiner RC, Tusting LS, Scott TW, Lindsay SW, Hay SI, Smith DL, 2015. Adult vector control, mosquito ecology and malaria transmission. Int Health 7: 121–129.
|Past two years||Past Year||Past 30 Days|
|Full Text Views||579||247||15|
The success of mosquito-based malaria control is dependent upon susceptible bionomic traits in local malaria vectors. It is crucial to have accurate and reliable methods to determine mosquito species composition in areas subject to malaria. An unexpectedly diverse set of Anopheles species was collected in the western Kenyan highlands, including unidentified and potentially new species carrying the malaria parasite Plasmodium falciparum. This study identified 2,340 anopheline specimens using both ribosomal DNA internal transcribed spacer region 2 and mitochondrial DNA cytochrome oxidase subunit 1 loci. Seventeen distinct sequence groups were identified. Of these, only eight could be molecularly identified through comparison to published and voucher sequences. Of the unidentified species, four were found to carry P. falciparum by circumsporozoite enzyme-linked immunosorbent assay and polymerase chain reaction, the most abundant of which had infection rates comparable to a primary vector in the area, Anopheles funestus. High-quality adult specimens of these unidentified species could not be matched to museum voucher specimens or conclusively identified using multiple keys, suggesting that they may have not been previously described. These unidentified vectors were captured outdoors. Diverse and unknown species have been incriminated in malaria transmission in the western Kenya highlands using molecular identification of unusual morphological variants of field specimens. This study demonstrates the value of using molecular methods to compliment vector identifications and highlights the need for accurate characterization of mosquito species and their associated behaviors for effective malaria control.
Financial support: This project was funded by the Bill & Melinda Gates Foundation under the Malaria Transmission Consortium grant no. 45114. This article has been approved by the Director of the Kenya Medical Research Institute.
Authors' addresses: Brandyce St. Laurent, Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, and Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, E-mail: email@example.com. Mary Cooke, Chris Drakeley, and Jonathan Cox, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom, E-mails: firstname.lastname@example.org, email@example.com, and firstname.lastname@example.org. Sindhu M. Krishnankutty, Western Triangle Research Center, Montana State University, Conrad, MT, E-mail: email@example.com. Puji Asih, Department of Malaria, Eijkman Institute for Molecular Biology, Jakarta, Indonesia, E-mail: firstname.lastname@example.org. John D. Mueller, Julie Thumloup, Frank H. Collins, and Neil F. Lobo, Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, E-mails: email@example.com, firstname.lastname@example.org, email@example.com, and firstname.lastname@example.org. Samuel Kahindi, Elizabeth Ayoma, and Robin M. Oriango, Centre for Global Health Research, Kenya Medical Research Institute/Centers for Disease Control and Prevention, Kisumu, Kenya, E-mails: email@example.com, firstname.lastname@example.org, and email@example.com. Jennifer C. Stevenson, Johns Hopkins School of Public Health, Malaria Research Institute, E-mail: firstname.lastname@example.org.