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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Indoor and outdoor malaria vector surveillance in western Kenya: implications for better understanding of residual transmission

Authors: Teshome Degefa, Delenasaw Yewhalaw, Guofa Zhou, Ming-chieh Lee, Harrysone Atieli, Andrew K. Githeko, Guiyun Yan

Published in: Malaria Journal | Issue 1/2017

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Abstract

Background

The widespread use of indoor-based malaria vector control interventions has been shown to alter the behaviour of vectors in Africa. There is an increasing concern that such changes could sustain residual transmission. This study was conducted to assess vector species composition, feeding behaviour and their contribution to indoor and outdoor malaria transmission in western Kenya.

Methods

Anopheles mosquito collections were carried out from September 2015 to April 2016 in Ahero and Iguhu sites, western Kenya using CDC light traps (indoor and outdoor), pyrethrum spray catches (PSCs) (indoor) and pit shelters (outdoor). Species within Anopheles gambiae s.l. and Anopheles funestus s.l. were identified using polymerase chain reaction (PCR). Enzyme-linked immunosorbent assay (ELISA) was used to determine mosquito blood meal sources and sporozoite infections.

Results

A total of 10,864 female Anopheles mosquitoes comprising An. gambiae s.l. (71.4%), An. funestus s.l. (12.3%), Anopheles coustani (9.2%) and Anopheles pharoensis (7.1%) were collected. The majority (61.8%) of the anopheline mosquitoes were collected outdoors. PCR result (n = 581) revealed that 98.9% An. arabiensis and 1.1% An. gambiae s.s. constituted An. gambiae s.l. in Ahero while this was 87% An. gambiae s.s. and 13% An. arabiensis in Iguhu. Of the 108 An. funestus s.l. analysed by PCR, 98.1% belonged to An. funestus s.s. and 1.9% to Anopheles leesoni. The human blood index (HBI) and bovine blood index (BBI) of An. arabiensis was 2.5 and 73.1%, respectively. Anopheles gambiae s.s. had HBI and BBI of 50 and 28%, respectively. The HBI and BBI of An. funestus was 60 and 22.3%, respectively. Forage ratio estimate revealed that An. arabiensis preferred to feed on cattle, An. gambiae s.s. showed preference for both human and cattle, while An. funestus preferred human over other hosts. In Ahero, the sporozoite rates for An. arabiensis and An. funestus were 0.16 and 1.8%, respectively, whereas in Iguhu, the sporozoite rates for An. gambiae s.s. and An. funestus were 2.3 and 2.4%, respectively. In Ahero, the estimated indoor and outdoor entomological inoculation rate (EIR) was 108.6 infective bites/person/year (79.0 from An. funestus and 29.6 from An. arabiensis) and 43.5 infective bites/person/year (27.9 from An. arabiensis and 15.6 from An. funestus), respectively. In Iguhu, the estimated indoor and outdoor EIR was 24.5 infective bites/person/year (18.8 from An. gambiae s.s. and 5.7 from An. funestus) and 5.5 infective bites/person/year (all from An. gambiae s.s.), respectively.

Conclusion

Anopheles gambiae s.s. showed an increasing tendency to feed on cattle. Anopheles arabiensis was highly zoophagic, whereas An. funestus showed anthropophagic behaviour. While the majority of malaria transmission occurred indoor, the magnitude of outdoor transmission was considerably high. Additional control tools that complement the existing interventions are required to control residual transmission.
Literature
1.
go back to reference WHO. World Malaria Report 2015. Geneva: World Health Organization; 2015. WHO. World Malaria Report 2015. Geneva: World Health Organization; 2015.
2.
go back to reference Shargie EB, Ngondi J, Graves PM, Getachew A, Hwang J, Gebre T, et al. Rapid increase in ownership and use of long-lasting insecticidal nets and decrease in prevalence of malaria in three regional States of Ethiopia (2006–2007). J Trop Med. 2010;2010:e750978.CrossRef Shargie EB, Ngondi J, Graves PM, Getachew A, Hwang J, Gebre T, et al. Rapid increase in ownership and use of long-lasting insecticidal nets and decrease in prevalence of malaria in three regional States of Ethiopia (2006–2007). J Trop Med. 2010;2010:e750978.CrossRef
3.
go back to reference Bhattarai A, Ali AS, Kachur SP, Mårtensson 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.CrossRefPubMedPubMedCentral Bhattarai A, Ali AS, Kachur SP, Mårtensson 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.CrossRefPubMedPubMedCentral
4.
go back to reference Otten M, Aregawi M, Were W, Karema C, Medin A, Bekele W, et al. Initial evidence of reduction of malaria cases and deaths in Rwanda and Ethiopia due to rapid scale-up of malaria prevention and treatment. Malar J. 2009;8:14.CrossRefPubMedPubMedCentral Otten M, Aregawi M, Were W, Karema C, Medin A, Bekele W, et al. Initial evidence of reduction of malaria cases and deaths in Rwanda and Ethiopia due to rapid scale-up of malaria prevention and treatment. Malar J. 2009;8:14.CrossRefPubMedPubMedCentral
5.
go back to reference Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P. Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6:e20318.CrossRefPubMedPubMedCentral Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P. Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6:e20318.CrossRefPubMedPubMedCentral
6.
go back to reference Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J. 2015;14:244.CrossRefPubMedPubMedCentral Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J. 2015;14:244.CrossRefPubMedPubMedCentral
7.
go back to reference Ndenga BA, Mulaya NL, Musaki SK, Shiroko JN, Dongus S, Fillinger U. Malaria vectors and their blood-meal sources in an area of high bed net ownership in the western Kenya highlands. Malar J. 2016;15:76.CrossRefPubMedPubMedCentral Ndenga BA, Mulaya NL, Musaki SK, Shiroko JN, Dongus S, Fillinger U. Malaria vectors and their blood-meal sources in an area of high bed net ownership in the western Kenya highlands. Malar J. 2016;15:76.CrossRefPubMedPubMedCentral
8.
go back to reference Ochomo EO, Bayoh NM, Walker ED, Abongo BO, Ombok MO, Ouma C, et al. The efficacy of long-lasting nets with declining physical integrity may be compromised in areas with high levels of pyrethroid resistance. Malar J. 2013;12:368.CrossRefPubMedPubMedCentral Ochomo EO, Bayoh NM, Walker ED, Abongo BO, Ombok MO, Ouma C, et al. The efficacy of long-lasting nets with declining physical integrity may be compromised in areas with high levels of pyrethroid resistance. Malar J. 2013;12:368.CrossRefPubMedPubMedCentral
9.
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
10.
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
11.
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
12.
go back to reference Derua YA, Alifrangis M, Hosea KM, Meyrowitsch DW, Magesa SM, Pedersen EM, et al. Change in composition of the Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in north-eastern Tanzania. Malar J. 2012;11:188.CrossRefPubMedPubMedCentral Derua YA, Alifrangis M, Hosea KM, Meyrowitsch DW, Magesa SM, Pedersen EM, et al. Change in composition of the Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in north-eastern Tanzania. Malar J. 2012;11:188.CrossRefPubMedPubMedCentral
13.
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
14.
go back to reference Durnez L, Coosemans M. Residual transmission of malaria: an old issue for new approaches. In: Manguin S, editor. Anopheles mosquitoes—new insights into malaria vectors; 2013. p. 671–704. Durnez L, Coosemans M. Residual transmission of malaria: an old issue for new approaches. In: Manguin S, editor. Anopheles mosquitoes—new insights into malaria vectors; 2013. p. 671–704.
15.
go back to reference Mutuku FM, King CH, Mungai P, Mbogo C, Mwangangi J, Muchiri EM, et al. Impact of insecticide-treated bed nets on malaria transmission indices on the south coast of Kenya. Malar J. 2011;10:356.CrossRefPubMedPubMedCentral Mutuku FM, King CH, Mungai P, Mbogo C, Mwangangi J, Muchiri EM, et al. Impact of insecticide-treated bed nets on malaria transmission indices on the south coast of Kenya. Malar J. 2011;10:356.CrossRefPubMedPubMedCentral
16.
go back to reference Lefèvre T, Gouagna L-C, Dabiré KR, Elguero E, Fontenille D, Renaud F, et al. Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am J Trop Med Hyg. 2009;81:1023–9.CrossRefPubMed Lefèvre T, Gouagna L-C, Dabiré KR, Elguero E, Fontenille D, Renaud F, et al. Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am J Trop Med Hyg. 2009;81:1023–9.CrossRefPubMed
17.
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
18.
go back to reference Meyers JI, Pathikonda S, Popkin-Hall ZR, Medeiros MC, Fuseini G, Matias A, et al. Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island. Malar J. 2016;15:239.CrossRefPubMedPubMedCentral Meyers JI, Pathikonda S, Popkin-Hall ZR, Medeiros MC, Fuseini G, Matias A, et al. Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island. Malar J. 2016;15:239.CrossRefPubMedPubMedCentral
19.
go back to reference Bayoh MN, Walker ED, Kosgei J, Ombok M, Olang GB, Githeko AK, et al. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasit Vectors. 2014;7:380.CrossRefPubMed Bayoh MN, Walker ED, Kosgei J, Ombok M, Olang GB, Githeko AK, et al. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasit Vectors. 2014;7:380.CrossRefPubMed
20.
go back to reference Githeko A, Ototo E, Guiyun Y. Progress towards understanding the ecology and epidemiology of malaria in the western Kenya highlands: opportunities and challenges for control under climate change risk. Acta Trop. 2012;121:19–25.CrossRefPubMed Githeko A, Ototo E, Guiyun Y. Progress towards understanding the ecology and epidemiology of malaria in the western Kenya highlands: opportunities and challenges for control under climate change risk. Acta Trop. 2012;121:19–25.CrossRefPubMed
21.
go back to reference Githeko A, Service M, Mbogo C, Atieli F, Juma F. Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya. Acta Trop. 1994;58:307–16.CrossRefPubMed Githeko A, Service M, Mbogo C, Atieli F, Juma F. Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya. Acta Trop. 1994;58:307–16.CrossRefPubMed
22.
go back to reference Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, Seroney IK, et al. Some observations on the biting behavior of Anopheles gambiae s.s, Anopheles arabiensis, and Anopheles funestus and their implications for malaria control. Exp Parasitol. 1996;82:306–15.CrossRefPubMed Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, Seroney IK, et al. Some observations on the biting behavior of Anopheles gambiae s.s, Anopheles arabiensis, and Anopheles funestus and their implications for malaria control. Exp Parasitol. 1996;82:306–15.CrossRefPubMed
23.
go back to reference Shililu J, Maier W, Seitz H, Orago A. Seasonal density, sporozoite rates and entomological inoculation rates of Anopheles gambiae and Anopheles funestus in a high altitude sugarcane growing zone in western Kenya. Trop Med Int Health. 1998;3:706–10.CrossRefPubMed Shililu J, Maier W, Seitz H, Orago A. Seasonal density, sporozoite rates and entomological inoculation rates of Anopheles gambiae and Anopheles funestus in a high altitude sugarcane growing zone in western Kenya. Trop Med Int Health. 1998;3:706–10.CrossRefPubMed
24.
go back to reference Munyekenye OG, Githeko AK, Zhou G, Mushinzimana E, Minakawa N, Yan G. Plasmodium falciparum spatial analysis, western Kenya highlands. Emerg Infect Dis. 2005;11:1571–7.CrossRefPubMedPubMedCentral Munyekenye OG, Githeko AK, Zhou G, Mushinzimana E, Minakawa N, Yan G. Plasmodium falciparum spatial analysis, western Kenya highlands. Emerg Infect Dis. 2005;11:1571–7.CrossRefPubMedPubMedCentral
25.
go back to reference Githeko AK, Ayisi JM, Odada PK, Atieli FK, Ndenga BA, Githure JI, et al. Topography and malaria transmission heterogeneity in western Kenya highlands: prospects for focal vector control. Malar J. 2006;5:107.CrossRefPubMedPubMedCentral Githeko AK, Ayisi JM, Odada PK, Atieli FK, Ndenga BA, Githure JI, et al. Topography and malaria transmission heterogeneity in western Kenya highlands: prospects for focal vector control. Malar J. 2006;5:107.CrossRefPubMedPubMedCentral
26.
go back to reference WHO. Manual on practical entomology in malaria. Geneva: World Health Organization; 1995. WHO. Manual on practical entomology in malaria. Geneva: World Health Organization; 1995.
27.
go back to reference Muirhead-Thomson R. A pit shelter for sampling outdoor mosquito populations. Bull World Health Organ. 1958;19:1116–8.PubMedPubMedCentral Muirhead-Thomson R. A pit shelter for sampling outdoor mosquito populations. Bull World Health Organ. 1958;19:1116–8.PubMedPubMedCentral
28.
go back to reference Gillies M, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara. Public South Afr Instit Med Res. 1987;55:1–143. Gillies M, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara. Public South Afr Instit Med Res. 1987;55:1–143.
29.
go back to reference Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.CrossRefPubMed Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.CrossRefPubMed
30.
go back to reference Koekemoer L, Kamau L, Hunt R, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.CrossRefPubMed Koekemoer L, Kamau L, Hunt R, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.CrossRefPubMed
31.
go back to reference Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D. Bloodmeal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. DTIC Doc. 1988;25:9–16. Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D. Bloodmeal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. DTIC Doc. 1988;25:9–16.
32.
go back to reference Beier JC, Perkins PV, Wirtz RA, Whitmire RE, Mugambi M. Field evaluation of an enzymelinked immunosorbent assay (ELISA) for Plasmodium falciparum sporozoite detection in anopheline mosquitoes from Kenya. DTIC Doc. 1987;36:459–68. Beier JC, Perkins PV, Wirtz RA, Whitmire RE, Mugambi M. Field evaluation of an enzymelinked immunosorbent assay (ELISA) for Plasmodium falciparum sporozoite detection in anopheline mosquitoes from Kenya. DTIC Doc. 1987;36:459–68.
33.
go back to reference Wirtz R, Burkot T, Graves P, Andre R. Field evaluation of enzyme-linked immunosorbent assays for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol. 1987;24:433–7.CrossRefPubMed Wirtz R, Burkot T, Graves P, Andre R. Field evaluation of enzyme-linked immunosorbent assays for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol. 1987;24:433–7.CrossRefPubMed
34.
go back to reference Garrett-Jones C. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ. 1964;30:241–61.PubMedPubMedCentral Garrett-Jones C. The human blood index of malaria vectors in relation to epidemiological assessment. Bull World Health Organ. 1964;30:241–61.PubMedPubMedCentral
35.
go back to reference Pappa V, Reddy M, Overgaard HJ, Abaga S, Caccone A. Estimation of the human blood index in malaria mosquito vectors in Equatorial Guinea after indoor antivector interventions. Am J Trop Med Hyg. 2011;84:298–301.CrossRefPubMedPubMedCentral Pappa V, Reddy M, Overgaard HJ, Abaga S, Caccone A. Estimation of the human blood index in malaria mosquito vectors in Equatorial Guinea after indoor antivector interventions. Am J Trop Med Hyg. 2011;84:298–301.CrossRefPubMedPubMedCentral
36.
go back to reference Hess A, Hayes RO, Tempelis C. The use of the forage ratio technique in mosquito host preference studies. Mosq News. 1968;28:386–9. Hess A, Hayes RO, Tempelis C. The use of the forage ratio technique in mosquito host preference studies. Mosq News. 1968;28:386–9.
37.
go back to reference Manly B, McDonald L, Thomas D, McDonald TL, Erickson WP. Resource selection by animals: statistical design and analysis for field studies. New York: Springer Science & Business Media; 2007. Manly B, McDonald L, Thomas D, McDonald TL, Erickson WP. Resource selection by animals: statistical design and analysis for field studies. New York: Springer Science & Business Media; 2007.
38.
go back to reference Lines J, Curtis C, Wilkes T, Njunwa K. Monitoring human-biting mosquitoes (Diptera: Culicidae) in Tanzania with light-traps hung beside mosquito nets. Bull Entomol Res. 1991;81:77–84.CrossRef Lines J, Curtis C, Wilkes T, Njunwa K. Monitoring human-biting mosquitoes (Diptera: Culicidae) in Tanzania with light-traps hung beside mosquito nets. Bull Entomol Res. 1991;81:77–84.CrossRef
39.
go back to reference Drakeley C, Schellenberg D, Kihonda J, Sousa C, Arez A, Lopes D, et al. An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Trop Med Int Health. 2003;8:767–74.CrossRefPubMed Drakeley C, Schellenberg D, Kihonda J, Sousa C, Arez A, Lopes D, et al. An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Trop Med Int Health. 2003;8:767–74.CrossRefPubMed
40.
go back to reference WHO. Malaria entomology and vector control: learner’s guide. Trial Edition HIV/AIDS, tuberculosis and malaria, roll back malaria. Geneva: World Health Organization; 2003. WHO. Malaria entomology and vector control: learner’s guide. Trial Edition HIV/AIDS, tuberculosis and malaria, roll back malaria. Geneva: World Health Organization; 2003.
41.
go back to reference Githeko A, Mbogo C, Atieli F, Juma F. Sampling Anopheles arabiensis, A. gambiae sensu lato and A. funestus (Diptera: Culicidae) with CDC light-traps near a rice irrigation area and a sugarcane belt in western Kenya. Bull Entomol Res. 1994;84:319–24.CrossRef Githeko A, Mbogo C, Atieli F, Juma F. Sampling Anopheles arabiensis, A. gambiae sensu lato and A. funestus (Diptera: Culicidae) with CDC light-traps near a rice irrigation area and a sugarcane belt in western Kenya. Bull Entomol Res. 1994;84:319–24.CrossRef
42.
go back to reference Minakawa N, Sonye G, Mogi M, Githeko A, Yan G. The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. J Med Entomol. 2002;39:833–41.CrossRefPubMed Minakawa N, Sonye G, Mogi M, Githeko A, Yan G. The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. J Med Entomol. 2002;39:833–41.CrossRefPubMed
43.
go back to reference Ndenga B, Githeko A, Omukunda E, Munyekenye G, Atieli H, Wamai P, et al. Population dynamics of malaria vectors in western Kenya highlands. J Med Entomol. 2006;43:200–6.CrossRefPubMed Ndenga B, Githeko A, Omukunda E, Munyekenye G, Atieli H, Wamai P, et al. Population dynamics of malaria vectors in western Kenya highlands. J Med Entomol. 2006;43:200–6.CrossRefPubMed
44.
go back to reference Kweka EJ, Munga S, Himeidan Y, Githeko AK, Yan G. Assessment of mosquito larval productivity among different land use types for targeted malaria vector control in the western Kenya highlands. Parasit Vectors. 2015;8:356.CrossRefPubMedPubMedCentral Kweka EJ, Munga S, Himeidan Y, Githeko AK, Yan G. Assessment of mosquito larval productivity among different land use types for targeted malaria vector control in the western Kenya highlands. Parasit Vectors. 2015;8:356.CrossRefPubMedPubMedCentral
45.
go back to reference Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G. Life-table analysis of Anopheles arabiensis in western Kenya highlands: effects of land covers on larval and adult survivorship. Am J Trop Med Hyg. 2007;77:660–6.PubMed Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G. Life-table analysis of Anopheles arabiensis in western Kenya highlands: effects of land covers on larval and adult survivorship. Am J Trop Med Hyg. 2007;77:660–6.PubMed
46.
go back to reference Okumu FO, Kiware SS, Moore SJ, Killeen GF. Mathematical evaluation of community level impact of combining bed nets and indoor residual spraying upon malaria transmission in areas where the main vectors are Anopheles arabiensis mosquitoes. Parasit Vectors. 2013;6:17.CrossRefPubMedPubMedCentral Okumu FO, Kiware SS, Moore SJ, Killeen GF. Mathematical evaluation of community level impact of combining bed nets and indoor residual spraying upon malaria transmission in areas where the main vectors are Anopheles arabiensis mosquitoes. Parasit Vectors. 2013;6:17.CrossRefPubMedPubMedCentral
47.
go back to reference Cooke 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.CrossRefPubMedPubMedCentral Cooke 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.CrossRefPubMedPubMedCentral
48.
go back to reference Overgaard HJ, Reddy VP, Abaga S, Matias A, Reddy MR, Kulkarni V, et al. Malaria transmission after five years of vector control on Bioko Island, Equatorial Guinea. Parasit Vectors. 2012;5:253.CrossRefPubMedPubMedCentral Overgaard HJ, Reddy VP, Abaga S, Matias A, Reddy MR, Kulkarni V, et al. Malaria transmission after five years of vector control on Bioko Island, Equatorial Guinea. Parasit Vectors. 2012;5:253.CrossRefPubMedPubMedCentral
49.
go back to reference Lehmann T, Licht M, Elissa N, Maega B, Chimumbwa J, Watsenga F, et al. Population structure of Anopheles gambiae in Africa. J Hered. 2003;94:133–47.CrossRefPubMed Lehmann T, Licht M, Elissa N, Maega B, Chimumbwa J, Watsenga F, et al. Population structure of Anopheles gambiae in Africa. J Hered. 2003;94:133–47.CrossRefPubMed
50.
go back to reference Mwangangi JM, Mbogo CM, Nzovu JG, Githure JI, Yan G, Beier JC. Blood-meal analysis for anopheline mosquitoes sampled along the Kenyan coast. J Am Mosq Control Assoc. 2003;19:371–5.PubMed Mwangangi JM, Mbogo CM, Nzovu JG, Githure JI, Yan G, Beier JC. Blood-meal analysis for anopheline mosquitoes sampled along the Kenyan coast. J Am Mosq Control Assoc. 2003;19:371–5.PubMed
51.
go back to reference Derua YA, Alifrangis M, Magesa SM, Kisinza WN, Simonsen PE. Sibling species of the Anopheles funestus group, and their infection with malaria and lymphatic filarial parasites, in archived and newly collected specimens from northeastern Tanzania. Malar J. 2015;14:104.CrossRefPubMedPubMedCentral Derua YA, Alifrangis M, Magesa SM, Kisinza WN, Simonsen PE. Sibling species of the Anopheles funestus group, and their infection with malaria and lymphatic filarial parasites, in archived and newly collected specimens from northeastern Tanzania. Malar J. 2015;14:104.CrossRefPubMedPubMedCentral
52.
go back to reference Kweka EJ, Kamau L, Munga S, Lee M-C, Githeko AK, Yan G. A first report of Anopheles funestus sibling species in western Kenya highlands. Acta Trop. 2013;128:158–61.CrossRefPubMedPubMedCentral Kweka EJ, Kamau L, Munga S, Lee M-C, Githeko AK, Yan G. A first report of Anopheles funestus sibling species in western Kenya highlands. Acta Trop. 2013;128:158–61.CrossRefPubMedPubMedCentral
53.
go back to reference Tanga M, Ngundu W, Tchouassi P. Daily survival and human blood index of major malaria vectors associated with oil palm cultivation in Cameroon and their role in malaria transmission. Trop Med Int Health. 2011;16:447–57.CrossRefPubMed Tanga M, Ngundu W, Tchouassi P. Daily survival and human blood index of major malaria vectors associated with oil palm cultivation in Cameroon and their role in malaria transmission. Trop Med Int Health. 2011;16:447–57.CrossRefPubMed
54.
go back to reference Das S, Henning TC, Simubali L, Hamapumbu H, Nzira L, Mamini E, et al. Underestimation of foraging behaviour by standard field methods in malaria vector mosquitoes in southern Africa. Malar J. 2015;14:12.CrossRefPubMedPubMedCentral Das S, Henning TC, Simubali L, Hamapumbu H, Nzira L, Mamini E, et al. Underestimation of foraging behaviour by standard field methods in malaria vector mosquitoes in southern Africa. Malar J. 2015;14:12.CrossRefPubMedPubMedCentral
55.
go back to reference Mzilahowa T, Hastings IM, Molyneux ME, McCall PJ. Entomological indices of malaria transmission in Chikhwawa district, Southern Malawi. Malar J. 2012;11:380.CrossRefPubMedPubMedCentral Mzilahowa T, Hastings IM, Molyneux ME, McCall PJ. Entomological indices of malaria transmission in Chikhwawa district, Southern Malawi. Malar J. 2012;11:380.CrossRefPubMedPubMedCentral
56.
go back to reference Dadzie SK, Brenyah R, Appawu MA. Role of species composition in malaria transmission by the Anopheles funestus group (Diptera: Culicidae) in Ghana. J Vector Ecol. 2013;38:105–10.CrossRefPubMed Dadzie SK, Brenyah R, Appawu MA. Role of species composition in malaria transmission by the Anopheles funestus group (Diptera: Culicidae) in Ghana. J Vector Ecol. 2013;38:105–10.CrossRefPubMed
57.
go back to reference Mwangangi JM, Muturi EJ, Muriu SM, Nzovu J, Midega JT, Mbogo C. The role of Anopheles arabiensis and Anopheles coustani in indoor and outdoor malaria transmission in Taveta District, Kenya. Parasit Vectors. 2013;6:114.CrossRefPubMedPubMedCentral Mwangangi JM, Muturi EJ, Muriu SM, Nzovu J, Midega JT, Mbogo C. The role of Anopheles arabiensis and Anopheles coustani in indoor and outdoor malaria transmission in Taveta District, Kenya. Parasit Vectors. 2013;6:114.CrossRefPubMedPubMedCentral
58.
go back to reference Taye B, Lelisa K, Emana D, Asale A, Yewhalaw D. Seasonal dynamics, longevity, and biting activity of anopheline mosquitoes in southwestern Ethiopia. J Insect Sci. 2016;16:6.CrossRefPubMedPubMedCentral Taye B, Lelisa K, Emana D, Asale A, Yewhalaw D. Seasonal dynamics, longevity, and biting activity of anopheline mosquitoes in southwestern Ethiopia. J Insect Sci. 2016;16:6.CrossRefPubMedPubMedCentral
59.
go back to reference Antonio-Nkondjio C, Kerah CH, Simard F, Awono-Ambene P, Chouaibou M, Tchuinkam T, et al. Complexity of the malaria vectorial system in Cameroon: contribution of secondary vectors to malaria transmission. J Med Entomol. 2006;43:1215–21.CrossRefPubMed Antonio-Nkondjio C, Kerah CH, Simard F, Awono-Ambene P, Chouaibou M, Tchuinkam T, et al. Complexity of the malaria vectorial system in Cameroon: contribution of secondary vectors to malaria transmission. J Med Entomol. 2006;43:1215–21.CrossRefPubMed
60.
61.
go back to reference Atieli HE, Zhou G, Afrane Y, Lee M-C, Mwanzo I, Githeko AK, et al. Insecticide-treated net (ITN) ownership, usage, and malaria transmission in the highlands of western Kenya. Parasit Vectors. 2011;4:113.CrossRefPubMedPubMedCentral Atieli HE, Zhou G, Afrane Y, Lee M-C, Mwanzo I, Githeko AK, et al. Insecticide-treated net (ITN) ownership, usage, and malaria transmission in the highlands of western Kenya. Parasit Vectors. 2011;4:113.CrossRefPubMedPubMedCentral
62.
go back to reference Wamae P, Githeko A, Otieno G, Kabiru E, Duombia S. Early biting of the Anopheles gambiae s.s and its challenges to vector control using insecticide treated nets in western Kenya highlands. Acta Trop. 2015;150:136–42.CrossRefPubMed Wamae P, Githeko A, Otieno G, Kabiru E, Duombia S. Early biting of the Anopheles gambiae s.s and its challenges to vector control using insecticide treated nets in western Kenya highlands. Acta Trop. 2015;150:136–42.CrossRefPubMed
63.
go back to reference Stevenson J, Laurent BS, Lobo NF, Cooke MK, Kahindi SC, Oriango RM, et al. Novel vectors of malaria parasites in the western highlands of Kenya. Emerg Infect Dis. 2012;18:1547–50.CrossRefPubMedPubMedCentral Stevenson J, Laurent BS, Lobo NF, Cooke MK, Kahindi SC, Oriango RM, et al. Novel vectors of malaria parasites in the western highlands of Kenya. Emerg Infect Dis. 2012;18:1547–50.CrossRefPubMedPubMedCentral
64.
go back to reference Laurent BS, Cooke M, Krishnankutty SM, Asih P, Mueller JD, Kahindi S, et al. Molecular characterization reveals diverse and unknown malaria vectors in the western Kenyan highlands. Am J Trop Med Hyg. 2016;94:327–35.CrossRef Laurent BS, Cooke M, Krishnankutty SM, Asih P, Mueller JD, Kahindi S, et al. Molecular characterization reveals diverse and unknown malaria vectors in the western Kenyan highlands. Am J Trop Med Hyg. 2016;94:327–35.CrossRef
65.
go back to reference Stevenson JC, Simubali L, Mbambara S, Musonda M, Mweetwa S, Mudenda T, et al. Detection of Plasmodium falciparum infection in Anopheles squamosus (Diptera: Culicidae) in an area targeted for malaria elimination, southern Zambia. J Med Entomol. 2016;53:1482–7.CrossRefPubMedPubMedCentral Stevenson JC, Simubali L, Mbambara S, Musonda M, Mweetwa S, Mudenda T, et al. Detection of Plasmodium falciparum infection in Anopheles squamosus (Diptera: Culicidae) in an area targeted for malaria elimination, southern Zambia. J Med Entomol. 2016;53:1482–7.CrossRefPubMedPubMedCentral
66.
go back to reference Degefa T, Zeynudin A, Godesso A, Michael YH, Eba K, Zemene E, et al. Malaria incidence and assessment of entomological indices among resettled communities in Ethiopia: a longitudinal study. Malar J. 2015;14:24.CrossRefPubMedPubMedCentral Degefa T, Zeynudin A, Godesso A, Michael YH, Eba K, Zemene E, et al. Malaria incidence and assessment of entomological indices among resettled communities in Ethiopia: a longitudinal study. Malar J. 2015;14:24.CrossRefPubMedPubMedCentral
Metadata
Title
Indoor and outdoor malaria vector surveillance in western Kenya: implications for better understanding of residual transmission
Authors
Teshome Degefa
Delenasaw Yewhalaw
Guofa Zhou
Ming-chieh Lee
Harrysone Atieli
Andrew K. Githeko
Guiyun Yan
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-2098-z

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