Assessment of mosquito larval productivity among different land use types for targeted malaria vector control in the western Kenya highlands

Particle and Fibre Toxicology

Guyuin Yan³  Andrew K. Githeko⁴  Yousif Himeidan²  Stephen Munga⁴  Eliningaya J. Kweka¹ 

[1] Pan African Mosquito Control Association (PAMCA), Dar es Salaam, Tanzania;Entomology Unit, Faculty of Agriculture and Natural Resources, University of Kassala, New Halfa, Sudan;Program in Public Health, University of California, Irvine 92697, CA, USA;Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

关键词: An. arabiensis;    Culex quinquefasciatus;    Anopheles gambiae s.s;    Land use;    Larval habitat;   

Others  :  1224181
DOI  :  10.1186/s13071-015-0968-1

 received in 2014-03-15, accepted in 2015-06-27,  发布年份 2015

【 摘 要 】

Background

Mosquito larval source management (LSM) is likely to be more effective when adequate information such as dominant species, seasonal abundance, type of productive habitat, and land use type are available for targeted sites. LSM has been an effective strategy for reducing malaria morbidity in both urban and rural areas in Africa where sufficient proportions of larval habitats can be targeted. In this study, we conducted longitudinal larval source surveillance in the western Kenya highlands, generating data which can be used to establish cost-effective targeted intervention tools.

Methods

One hundred and twenty-four (124) positive larval habitats were monitored weekly and sampled for mosquito larvae over the 85-week period from 28 July 2009 to 3 March 2011. Two villages in the western Kenya highlands, Mbale and Iguhu, were included in the study.

After preliminary sampling, habitats were classified into four types: hoof prints (n = 21; 17 % of total), swamps (n = 32; 26 %), abandoned goldmines (n = 35; 28 %) and drainage ditches (n = 36; 29 %). Positive habitats occurred in two land use types: farmland (66) and pasture (58). No positive larval habitats occurred in shrub land or forest.

Results

A total of 46,846 larvae were sampled, of which 44.1 % (20,907) were from abandoned goldmines, 30.9 % (14,469) from drainage ditches, 22.4 % (10,499) from swamps and 2.1 % (971) from hoof prints. In terms of land use types, 57.2 % (26,799) of the sampled larvae were from pasture and 42.8 % (20,047) were from farmland. Of the specimens identified morphologically, 24,583 (52.5 %) were Anopheles gambiae s.l., 11,901 (25.4 %) were Culex quinquefasciatus, 5628 (12 %) were An. funestus s.l. and 4734 (10.1 %) were other anopheline species (An. coustani, An. squamosus, An. ziemanni or An. implexus). Malaria vector dynamics varied seasonally, with An.gambiae s.s. dominating during wet season and An.arabiensis during dry season. An increased proportion of An. arabiensis was observed compared to previous studies.

Conclusion

These results suggest that long-term monitoring of larval habitats can establish effective surveillance systems and tools. Additionally, the results suggest that larval control is most effective in the dry season due to habitat restriction, with abandoned goldmines, drainage ditches and swamps being the best habitats to target. Both farmland and pasture should be targeted for effective larval control. An increased proportion of An. arabiensis in the An. gambiae complex was noticed in this study for the very first time in the western Kenya highlands; hence, further control tools should be in place for effective control of An. arabiensis.

【 授权许可】

   
2015 Kweka et al.

【 图 表 】

Fig. 1.

Fig. 2.

【 参考文献 】

• [1]Kweka E, Zhou G, Lee M-C, Gilbreath T, Mosha F, Munga S, Githeko A, Yan G. Evaluation of two methods of estimating larval habitat productivity in western Kenya highlands. Parasit Vectors. 2011; 4:110. BioMed Central Full Text
• [2]Chen H, Githeko A, Zhou G, Githure J, Yan G. New records of Anopheles arabiensis breeding on the Mount Kenya highlands indicate indigenous malaria transmission. Malar J. 2006; 5:17. BioMed Central Full Text
• [3]Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besansky N. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013; 3619:246-74.
• [4]Coetzee M, Craig M, le Sueur D. Distribution of African malaria mosquitoes belonging to the anopheles gambiae complex. Parasitol Today. 2000; 16:74-7.
• [5]Githeko A, Ayisi J, Odada P, Atieli F, Ndenga B, Githure J, Yan G. Topography and malaria transmission heterogeneity in western Kenya highlands: prospects for focal vector control. Malar J. 2006; 5:107. BioMed Central Full Text
• [6]Atieli H, Zhou G, Lee M-C, Kweka E, Afrane Y, Mwanzo I, Githeko A, Yan G. Topography as a modifier of breeding habitats and concurrent vulnerability to malaria risk in the western Kenya highlands. Parasit Vectors. 2011; 4:241. BioMed Central Full Text
• [7]Minakawa N, Munga S, Atieli F, Mushinzimana E, Zhou G, Githeko AK, Yan G. Spatial distribution of anopheline larval habitats in Western Kenyan highlands: effects of land cover types and topography. Am J Trop Med Hyg. 2005; 73:157-65.
• [8]Munga S, Minakawa N, Zhou G, Mushinzimana E, Barrack OO, Githeko AK, Yan G. Association between land cover and habitat productivity of malaria vectors in Western Kenyan highlands. Am J Trop Med Hyg. 2006; 74:69-75.
• [9]Munga S, Yakob L, Mushinzimana E, Zhou G, Ouna T, Minakawa N, Githeko A, Yan G. Land use and land cover changes and spatiotemporal dynamics of anopheline larval habitats during a four-year period in a highland community of Africa. Am J Trop Med Hyg. 2009; 81:1079-84.
• [10]Sovi A, Govoetchan R, Tokponnon F, Hounkonnou H, Aikpon R, Agossa F, Gnanguenon V, Salako A, Agossou C, Osse R, Oke M, Gbenou D, Massougbodji A, Akogbeto M. Impact of land-use on malaria transmission in the Plateau region, Southeastern Benin. Parasit Vectors. 2013; 6:352. BioMed Central Full Text
• [11]Kweka EJ, Zhou G, Munga S, Lee M-C, Atieli HE, Nyindo M, Githeko AK, Yan G. Anopheline larval habitats seasonality and species distribution: a prerequisite for effective targeted larval habitats control programmes. PLoS One. 2012; 7:e52084.
• [12]Tuno N, Okeka W, Minakawa N, Takagi M, Yan G. Survivorship of anopheles gambiae sensu stricto (Diptera: Culicidae) Larvae in Western Kenya highland forest. J Med Entomol. 2005; 42:270-7.
• [13]Zhou G, Munga S, Minakawa N, Githeko AK, Yan G. Spatial relationship between adult malaria vector abundance and environmental factors in Western Kenya highlands. Am J Trop Med Hyg. 2007; 77:29-35.
• [14]McCrae AW. Oviposition by African malaria vector mosquitoes. II. Effects of site tone, water type and conspecific immatures on target selection by freshwater Anopheles gambiae Giles, sensu lato. Ann Trop Med Parasitol. 1984; 78:307-18.
• [15]Zhou G, Minakawa N, Githeko AK, Yan G. Climate variability and malaria epidemics in the highlands of East Africa. Trends Parasitol. 2005; 21:54-6.
• [16]Himeidan Y, Zhou G, Yakob L, Afrane Y, Munga S, Atieli H, El-Rayah E-A, Githeko A, Yan G. Habitat stability and occurrences of malaria vector larvae in western Kenya highlands. Malar J. 2009; 8:234. BioMed Central Full Text
• [17]Omumbo J, Lyon B, Waweru S, Connor S, Thomson M. Raised temperatures over the Kericho tea estates: revisiting the climate in the East African highlands malaria debate. Malar J. 2011; 10:12. BioMed Central Full Text
• [18]Wanjala C, Waitumbi J, Zhou G, Githeko A. Identification of malaria transmission and epidemic hotspots in the western Kenya highlands: its application to malaria epidemic prediction. Parasit Vectors. 2011; 4:81. BioMed Central Full Text
• [19]Badu K, Siangla J, Larbi J, Lawson B, Afrane Y, Ong'echa J, Remoue F, Zhou G, Githeko A, Yan G. Variation in exposure to Anopheles gambiae salivary gland peptide (gSG6-P1) across different malaria transmission settings in the western Kenya highlands. Malar J. 2012; 11:318. BioMed Central Full Text
• [20]Badu K, Afrane Y, Larbi J, Stewart V, Waitumbi J, Angov E, Ong'echa J, Perkins D, Zhou G, Githeko A, Yan G. Marked variation in MSP-119 antibody responses to malaria in western Kenyan highlands. BMC Infect Dis. 2012; 12:50. BioMed Central Full Text
• [21]Atieli H, Zhou G, Afrane Y, Lee M-C, Mwanzo I, Githeko A, Yan G. Insecticide-treated net (ITN) ownership, usage, and malaria transmission in the highlands of western Kenya. Parasit Vectors. 2011; 4:113. BioMed Central Full Text
• [22]Zhou G, Afrane Y, Dixit A, Atieli H, Lee M-C, Wanjala C, Beilhe L, Githeko A, Yan G. Modest additive effects of integrated vector control measures on malaria prevalence and transmission in western Kenya. Malar. 2013; 12:256. BioMed Central Full Text
• [23]Asale A, Getachew Y, Hailesilassie W, Speybroeck N, Duchateau L, Yewhalaw D. Evaluation of the efficacy of DDT indoor residual spraying and long-lasting insecticidal nets against insecticide resistant populations of Anopheles arabiensis Patton (Diptera: Culicidae) from Ethiopia using experimental huts. Parasit Vectors. 2014; 7:131. BioMed Central Full Text
• [24]Kitau J, Oxborough R, Kaye A, Chen-Hussey V, Isaacs E, Matowo J, Kaur H, Magesa S, Mosha F, Rowland M, Logan J. Laboratory and experimental hut evaluation of a long-lasting insecticide treated blanket for protection against mosquitoes. Parasit Vectors. 2014; 7:129. BioMed Central Full Text
• [25]Fillinger U, Lindsay S. Larval source management for malaria control in Africa: myths and reality. Malar J. 2011; 10:353. BioMed Central Full Text
• [26]Worrall E, Fillinger U. Large-scale use of mosquito larval source management for malaria control in Africa: a cost analysis. Malar J. 2011; 10:338. BioMed Central Full Text
• [27]Smith DL, Perkins TA, Tusting LS, Scott TW, Lindsay SW. Mosquito population regulation and larval source management in heterogeneous environments. PLoS One. 2013; 8:e71247.
• [28]Tusting LS, Thwing J, Sinclair D, Fillinger U, Gimnig J, Bonner KE, Bottomley C, Lindsay SW. Mosquito larval source management for controlling malaria. Cochrane Database Syst Rev. 2013; 8:CD008923.
• [29]Geissbühler Y, Kannady K, Chaki PP, Emidi B, Govella NJ, Mayagaya V, Kiama M, Mtasiwa D, Mshinda H, Lindsay SW, Tanner M, Fillinger U, de Castro MC, Killeen GF. Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in urban Dar Es Salaam, Tanzania. PLoS ONE. 2009; 4:e5107.
• [30]Mwangangi J, Kahindi S, Kibe L, Nzovu J, Luethy P, Githure J, Mbogo C. Wide-scale application of Bti/Bs biolarvicide in different aquatic habitat types in urban and peri-urban Malindi, Kenya. Parasitol Res. 2011; 108:1355-63.
• [31]Gillies MT, Coetzee M. A Supplement to the Anophelinae of Africa, South of the Sahara, Publication of the South African Institute of International Medicine and Research No. 55. 1987.
• [32]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.
• [33]Koekemoer LL, Kamau L, Hunt RH, 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.
• [34]Wamae P, Githeko A, Menya D, Takken W. Shading by napier grass reduces malaria vector larvae in natural habitats in Western Kenya highlands. EcoHealth. 2010; 7:485-97.
• [35]Gouagna L, Rakotondranary M, Boyer S, Lemperiere G, Dehecq J-S, Fontenille D. Abiotic and biotic factors associated with the presence of Anopheles arabiensis immatures and their abundance in naturally occurring and man-made aquatic habitats. Parasit Vectors. 2012; 5:96. BioMed Central Full Text
• [36]Ndenga B, Githeko A, Omukunda E, Munyekenye G, Atieli H, Wamai P, Mbogo C, Minakawa N, Zhou G, Yan G. Population dynamics of malaria vectors in Western Kenya highlands. J Med Entomol. 2006; 43:200-6.
• [37]Sikaala C, Killeen G, Chanda J, Chinula D, Miller J, Russell T, Seyoum A. Evaluation of alternative mosquito sampling methods for malaria vectors in Lowland South - East Zambia. Parasit Vectors. 2013; 6:91. BioMed Central Full Text
• [38]Sinka M, Bangs M, Manguin S, Coetzee M, Mbogo C, Hemingway J, Patil A, Temperley W, Gething P, Kabaria C, Okara R, Van Boeckel T, Godfray HC, Harbach R, Hay S. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2010; 3:117. BioMed Central Full Text
• [39]Juliano SA. Species interactions among larval mosquitoes: context dependence across habitat gradients. Ann Rev Entomol. 2009; 54:37-56.
• [40]Nmor J, Sunahara T, Goto K, Futami K, Sonye G, Akweywa P, Dida G, Minakawa N. Topographic models for predicting malaria vector breeding habitats: potential tools for vector control managers. Parasit Vectors. 2013; 6:14. BioMed Central Full Text
• [41]Munga S, Vulule J, Kweka E. Response of anopheles gambiae s.l. (Diptera: Culicidae) to larval habitat age in western Kenya highlands. Parasit Vectors. 2013; 6:13. BioMed Central Full Text
• [42]Killeen GF, Fillinger U, Kiche I, Gouagna LC, Knols BGJ. Eradication of Anopheles gambiae from Brazil: lessons for malaria control in Africa? Lancet Infect Dis. 2002; 2:618-27.
• [43]Bayoh MN, Mathias D, Odiere M, Mutuku F, Kamau L, Gimnig J, Vulule J, Hawley W, Hamel M, Walker E. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J. 2010; 9:62. BioMed Central Full Text
• [44]Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC, Magesa SM, Bruce J, Mosha FW, Rowland MW. Species shifts in the Anopheles gambiae complex: do LLINs successfully control Anopheles arabiensis? PLoS One. 2012; 7:e31481.
• [45]Mejia P, Teklehaimanot H, Tesfaye Y, Teklehaimanot A. Physical condition of Olyset(R) nets after five years of utilization in rural western Kenya. Malar J. 2013; 12:158. BioMed Central Full Text
• [46]Antonio-Nkondjio C, Demanou M, Etang J, Bouchite B. Impact of cyfluthrin (Solfac EW050) impregnated bed nets on malaria transmission in the city of Mbandjock: lessons for the nationwide distribution of long-lasting insecticidal nets (LLINs) in Cameroon. Parasit Vectors. 2013; 6:10. BioMed Central Full Text
• [47]Futami K, Dida G, Sonye G, Lutiali P, Mwania M, Wagalla S, Lumumba J, Kongere J, Njenga S, Minakawa N. Impacts of insecticide treated bed nets on Anopheles gambiae s.l. populations in Mbita district and Suba district, Western Kenya. Parasit Vectors. 2014; 7:63. BioMed Central Full Text
• [48]Imbahale S, Paaijmans K, Mukabana W, van Lammeren R, Githeko A, Takken W. A longitudinal study on Anopheles mosquito larval abundance in distinct geographical and environmental settings in western Kenya. Malar J. 2011; 10:81. BioMed Central Full Text
• [49]Paaijmans KP, Wandago MO, Githeko AK, Takken W. Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS One. 2007; 2:e1146.
• [50]McCrae AW. Oviposition by African malaria vector mosquitoes. I. Temporal activity patterns of caged, wild-caught, freshwater Anopheles gambiae Giles sensu lato. Ann Trop Med Parasitol. 1983; 77:615-25.
• [51]Gilbreath T, Kweka E, Afrane Y, Githeko A, Yan G. Evaluating larval mosquito resource partitioning in western Kenya using stable isotopes of carbon and nitrogen. Parasit Vectors. 2013; 6:353. BioMed Central Full Text
• [52]Lyons C, Coetzee M, Chown S. Stable and fluctuating temperature effects on the development rate and survival of two malaria vectors: anopheles arabiensis and Anopheles funestus. Parasit Vectors. 2013; 6:104. BioMed Central Full Text
• [53]Walker K, Lynch M. Contributions of Anopheles larval control to malaria suppression in tropical Africa: review of achievements and potential. Med Vet Entomol. 2007; 21:2-21.
• [54]Chaki P, Dongus S, Fillinger U, Kelly A, Killeen G. Community-owned resource persons for malaria vector control: enabling factors and challenges in an operational programme in Dar es Salaam, United Republic of Tanzania. Hum Resour Health. 2011; 9:21. BioMed Central Full Text
• [55]Mukabana W, Kannady K, Kiama GM, Ijumba J, Mathenge E, Kiche I, Nkwengulila G, Mboera L, Mtasiwa D, Yamagata Y, van Schayk I, Knols B, Lindsay S, de Castro M, Mshinda H, Tanner M, Fillinger U, Killeen G. Ecologists can enable communities to implement malaria vector control in Africa. Malar J. 2006; 5:9. BioMed Central Full Text
• [56]Chaki P, Govella N, Shoo B, Hemed A, Tanner M, Fillinger U, Killeen G. Achieving high coverage of larval-stage mosquito surveillance: challenges for a community-based mosquito control programme in urban Dar es Salaam, Tanzania. Malar J. 2009; 8:311. BioMed Central Full Text