Habitat hydrology and geomorphology control the distribution of malaria vector larvae in rural Africa

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Hardy, Andrew J ^a,b   Gamarra, Javier G P ^c   Cross, Dónall E ^b,c   Macklin, Mark G ^a   Smith, Mark W ^d   Kihonda, Japhet ^b   Killeen, Gerry F ^b,e   Ling'ala, George N ^b   Thomas, Chris J ^c  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b IFAKARA HEALTH INSTITUTE   (Tanzania)

^c ABERYSTWYTH UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF LEEDS   (United Kingdom)

^e LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RAIN;

ANOPHELES ARABIENSIS; AQUATIC ENVIRONMENT; ARTICLE; BREEDING; CATCHMENT; CONTROLLED STUDY; GEOMORPHOLOGY; HYDROLOGY; LANDSCAPE; MALARIA; MONITORING; NONHUMAN; PARASITE TRANSMISSION; POPULATION ABUNDANCE; POPULATION PRODUCTIVITY; RIVER; RURAL AREA; SEASONAL VARIATION; SPECIES HABITAT; TANZANIA;

AFRICA; ANIMALS; ANOPHELES; ECOSYSTEM; HYDROLOGY; LARVA; MALARIA; MOSQUITO CONTROL; RAIN; RIVERS; RURAL POPULATION;

EID: 84891667414     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081931     Document Type: Article

References (82)

1. Ferguson HM, Domhaus A, Beeche A, Borgemeister C, Gottlieb M et al. (2010) Ecology: a prerequisite for malaria elimination and eradication. PLoS Med 7: 1-7. PubMed: 20689800.
2. Ndenga BA, Simbauni JA, Mbugi JP, Githeko AK, Fillinger U (2011) Productivity of Malaria Vectors from Different Habitat Types in the Western Kenya Highlands. PLOS ONE 6: e19473. doi:10.1371/journal.pone.0019473. PubMed: 21559301.
3. Gouagna LC, Rakotondranary M, Boyer S, Lemperiere G, Dehecq JS et al. (2012) Abiotic and biotic factors associated with the presence of Anopheles arabiensis immatures and their abundance in naturally occurring and man-made aquatic habitats. Parasites and Vectors 5.
4. Imbahale SS, Githeko A, Mukabana WR, Takken W (2012) Integrated mosquito larval source management reduces larval numbers in two highland villages in western Kenya. BMC Public Health 12: 362-. PubMed: 22607227.
5. Zhou G, Munga S, Minakawa N, Githeko AK, Yan G (2007) Spatial relationship between adult malaria vector abundance and environmental factors in western Kenya highlands. Am J Trop Med Hyg 77: 29-35. PubMed: 17620627.
6. Killeen GF, Seyoum AK, Knols BGJ (2004) Rationalizing Historical successes of malaria control in Africa in terms of mosquito resource availabilty management. American Journal of Tropical Medicine and Hygiene 71: 87-93.
7. Fillinger U, Lindsay SW (2006) Suppression of exposure to malaria vectors by an order of magnitude using microbial larvicides in rural Kenya. Trop Med Int Health 11: 1629-1642. doi:10.1111/j.1365-3156.2006.01733.x. PubMed: 17054742.
8. Killeen GF (2013) A second chance to tackle African malaria vector mosquitoes that avoid houses and don't take drugs. Am J Trop Med Hyg 88: 809-816. doi:10.4269/ajtmh.13-0065. PubMed: 23589532.
9. Gu W, Utzinger J, Novak RJ (2008) Habitat-based larval interventions: a new perspective for malaria control. Am J Trop Med Hyg 78: 2-6. PubMed: 18187774.
10. Kweka EJ, Zhou GF, Lee MC, Gilbreath TM, Mosha F et al. (2011) Evaluation of two methods of estimating larval habitat productivity in western Kenya highlands. Parasit Vectors 4: 110-. PubMed: 21682875.
11. Mutuku FM, Alaii JA, Bayoh MN, Gimnig JE, Vulule JM et al. (2006) Distribution, description, and local knowledge of larval habitats of Anopheles Gambiae s.l. in a village in Western Kenya. Am J Trop Med Hyg 74: 44-53. PubMed: 16407345.
12. Clark TD, Greenhouse B, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C et al. (2008) Factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. J Infect Dis 198: 393-400. doi:10.1086/589778. PubMed: 18522503.
13. Killeen GF, Tanner M, Mukabana WR, Kalongolela MS, Kannady K et al. (2006) Habitat targeting for controlling aquatic stages of malaria vectors in Africa. Am J Trop Med Hyg 74: 517-518. PubMed: 16606973.
14. Smith MW, Macklin MG, Thomas CJ (2013) Hydrological and geomorphological controls of malaria transmission. Earth Science Reviews 116: 109-127. doi:10.1016/j.earscirev.2012.11.004.
15. Githeko AK, Ototo EN, Yan GY (2012) 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 121: 19-25. doi:10.1016/j.actatropica.2011.10.002. PubMed: 22015426.
16. Cohen J, Ernst C, Lindblade K, Vulule J, John C et al. (2010) Local topographic wetness indices predict household malaria risk better than land-use and land-cover in the western Kenya highlands. Malar J 9: 1-10. doi:10.1186/1475-2875-9-S1-S1. PubMed: 20043863.
17. Zhang Y, Bi P, Hiller JE (2008) Climate change and the transmission of vector-borne diseases: a review. Asia Pac J Public Health 20: 64-76. doi:10.1177/1010539507308385. PubMed: 19124300.
18. Thomas CJ (2004) Malaria: a changed climate in Africa? Nature 427: 690-691. doi:10.1038/427690b. PubMed: 14973466.
19. Mordecai EA, Paaijmans KP, Johnson LR, Balzer C, Ben-Horin T et al. (2013) Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett 16: 22-30. doi:10.1111/ele.12015. PubMed: 23050931.
20. Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF et al. (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci U S A 107: 15135-15139. doi:10.1073/pnas. 1006422107. PubMed: 20696913.
21. Paaijmans KP, Read AF, Thomas MB (2009) Understanding the link between malaria risk and climate. Proc Natl Acad Sci U S A 106: 13844-13849. doi:10.1073/pnas.0903423106. PubMed: 19666598.
22. Small J, Goetz SJ, Hay SI (2003) Climatic suitability for malaria transmission in Africa, 1911-1995. Proceedings of the National Academy of Sciences of the USA 100: 15341-15345. doi:10.1073/pnas.2236969100.
23. Fillinger U, Sombroek H, Majambere S, Van Loon E, Takken W et al. (2009) Identifying the most productive breeding sites for malaria mosquitoes in The Gambia. Malar J 8: 62. doi: 10.1186/1475-2875-8-62. PubMed: 19361337.
24. Majambere S, Lindsay SW, Green C, Kandeh B, Fillinger U (2007) Microbial larvicides for malaria control in The Gambia. Malar J 6: 76. doi:10.1186/1475-2875-6-76. PubMed: 17555570.
25. Do Manh C, Beebe NW, Van Nguyen Thi Van TL, Quang CTL, Van Nguyen D, et al. (2010) Vectors and malaria transmission in deforested, rural communities in north-central Vietnam. Malaria Journal 9: 259.
26. Magalhães RJ, Langa A, Sousa-Figueiredo JC, Clements AC, Nery SV (2012) Finding malaria hot-spots in northern Angola: the role of individual, household and environmental factors within a meso-endemic area. Malar J 11: 1-12. doi:10.1186/1475-2875-11-S1-P1. PubMed: 22212246.
27. Bøgh C, Lindsay SW, Clarke SE, Dean A, Jawara M et al. (2007) High spatial resolution mapping of malaria transmission risk in the Gambia, West Africa, using Landsat TM satellite imagery. Am J Trop Med Hyg 76: 875-881. PubMed: 17488908.
28. Ageep TB, Cox J, M'oawia MH, Knols BGJ, Benedict MQ et al. (2009) Spatial and temporal distribution of the malaria mosquito Anopheles arabiensis in northern Sudan: influence of environmental factors and implications for vector control. Malar J 8: 123. doi:10.1186/1475-2875-8-123. PubMed: 19500425.
29. Oesterholt MJ, Bousema JT, Mwerinde OK, Harris C, Lushino P et al. (2006) Spatial and temporal variation in malaria transmission in a low endemicity area in northern Tanzania. Malar J 5: 98. doi:10.1186/1475-2875-5-98. PubMed: 17081311.
30. Thomson MC, Mason SJ, Phindela T, Connor SJ (2005) Use of rainfall and sea surface temperature monitoring for malaria early warning in Botswana. Am J Trop Med Hyg 73: 214-221. PubMed: 16014862.
31. Paaijmans KP, Wandago MO, Githeko AK, Takken W (2007) Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLOS ONE 2: e1146. doi:10.1371/journal.pone.0001146. PubMed: 17987125.
32. Balls MJ, Bødker R, Thomas CJ, Kisinza W, Msangeni HA et al. (2004) Effect of topography on the risk of malaria infection in the Usambara Mountains, Tanzania. Trans R Soc Trop Med Hyg 98: 400-408. doi: 10.1016/j.trstmh.2003.11.005. PubMed: 15138076.
33. Bomblies A, Duchemin J-B, Eltahir EAB (2008) Hydrology of malaria: Model development and application to a Sahelian village. Water Resources Research 44: W12445.
34. Shaman J, Stieglitz M, Stark C, Le Blancq S, Cane M (2002) Using a dynamic hydrology model to predict mosquito abundances in flood and swamp water. Emerg Infect Dis 8: 6-13. PubMed: 11749741.
35. Charlwood JD, Vij R, Billingsley PF (2000) Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of East Africa. Am J Trop Med Hyg 62: 726-732. PubMed: 11304064.
36. Temple P, Sundborg A (1972) The Rufiji River, Tanzania hydrology and sediment transport. Geografiska Annaler 54: 345-368. doi: 10.2307/520773.
37. Charlwood JD, Kihonda J, Sama S, Billingsley PF, Hadji H et al. (1995) The rise and fall of Anopheles arabiensis (Diptera: Culicidae) in a Tanzanian village. Bulletin of Entomological Research 85: 37-44. doi:10.1017/ S0007485300051993.
38. Killeen GF, Tami A, Kihonda J, Okumu, Kotas M, et al. (2007) Cost-sharing strategies combining targeted public subsidies with private-sector delivery achieve high bednet coverage and reduced malaria transmission in Kilombero Valley, southern Tanzania. BMC Infectious Diseases 7.
39. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP et al. (2011) Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J 10: 80. doi:10.1186/1475-2875-10-80. PubMed: 21477321.
40. Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T et al. (2012) A global map of dominant malaria vectors. Parasites and Vectors 5: 1-11.
41. Russell TL, Lwetoijera D, Maliti D, Chipwaza B, Kihonda J et al. (2010) 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. Malaria Journal 9.
42. Charlwood J, Smith T, Kihonda J, Billingsley P, Takken W (1995) Density independent feeding success of malaria vectors (Diptera: Culicidae) in Tanzania. Bulletin of Entomological Research 85: 29-36. doi:10.1017/S0007485300051981.
43. Haji H, Smith T, Charlwood JD, Meuwissen JH (1996) Absence of relationships between selected human factors and natural infectivity of Plasmodium falciparum to mosquitoes in an area of high transmission. Parasitology 113: 425-432. doi:10.1017/S0031182000081488. PubMed: 8893528.
44. Bracken LJ, Cox NJ, Shannon J (2008) The relationship between rainfall inputs and flood generation in south-east Spain. Hydrological Processes 22: 683-696. doi:10.1002/hyp.6641.
45. Minakawa N, Seda P, Yan G (2002) Influence of host and larval habitat distribution on the abundance of African malaria vectors in western Kenya. Am J Trop Med Hyg 67: 32-38. PubMed: 12363061.
46. Minakawa N, Munga S, Atieli F, Mushinzimana E, Zhou G et al. (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. PubMed: 16014851.
47. Atieli HE, Zhou G, Lee M-C, Kweka EJ, Afrane Y et al. (2011) Topography as a modifier of breeding habitats and concurrent vulnerability to malaria risk in the western Kenya highlands. Parasit Vectors 4: 241. doi:10.1186/1756-3305-4- 241. PubMed: 22196078.
48. Mushinzimana E, Munga S, Minakawa N, Li L, Feng C-c et al. (2006) Landscape determinants and remote sensing of anopheline mosquito larval habitats in the western Kenya highlands. Malar J 5: 1-11. doi:10.1186/1475-2875-5-1. PubMed: 16420686.
49. Nmor JC, Sunahara T, Goto K, Futami K, Sonye G et al. (2013) Topographic models for predicting malaria vector breeding habitats: potential tools for vector control managers. Parasit Vectors 6: 14. PubMed: 23324389.
50. Amerasinghe PH, Amerasinghe FP, Konradsen F, Fonseka KT, Wirtz RA (1999) Malaria vectors in a traditional dry zone village in Sri Lanka. Am J Trop Med Hyg 60: 421-429. PubMed: 10466971.
51. Van Der Hoek W, Konradsen F, Amerasinghe PH, Perera D, Piyaratne MK et al. (2003) Towards a risk map of malaria for Sri Lanka: the importance of house location relative to vector breeding sites. Int J Epidemiol 32: 280-285. doi:10.1093/ije/dyg055. PubMed: 12714550.
52. Mala AO, Irungu LW, Shililu JI, Muturi EJ, Mbogo CC et al. (2011) Dry season ecology of Anopheles gambiae complex mosquitoes at larval habitats in two traditionally semi-arid villages in Baringo, Kenya. Parasit Vectors 4: 1-11. PubMed: 21352608.
53. Gillies MT, De Meillon B (1968) The Anophelinae of Africa South of the Sahara. Johannesburg: South African Institute for Medical Research.
54. Fillinger U, Kannady K, William G, Vanek MJ, Dongus S et al. (2008) A tool box for operational mosquito larval control: preliminary results and early lessons from the Urban Malaria Control Programme in Dar es Salaam, Tanzania. Malar J 7: 20. doi:10.1186/1475-2875-7-20. PubMed: 18218148.
55. Cheng P, Chaapel C (October/November2001) Automatic DEM generation. Geoinformatics October/November: 34-39.
56. Exelis (2012) ENVI. Version 5.0 ed. McLean, VA: Exelis Visual Information Solutions
57. Costantini C, Li SG, Torre AD, Sagnon NF, Coluzzi M et al. (1996) Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a West African Sudan savanna village. Med Vet Entomol 10: 203-219. doi:10.1111/j.1365-2915.1996.tb00733.x. PubMed: 8887330.
58. Mwangangi JM, Shililu J, Muturi EJ, Muriu S, Jacob B et al. (2010) Anopheles larval abundance and diversity in three rice agro-village complexes Mwea irrigation scheme, central Kenya. Malar J 9: 228. doi:10.1186/1475-2875-9- 228. PubMed: 20691120.
59. 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. PubMed: 8214283.
60. 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. PubMed: 12224596.
61. Bayoh MN, Akhwale W, Ombok M, Sang D, Engoki SC et al. (2011) Malaria in Kakuma refugee camp, Turkana, Kenya: facilitation of Anopheles arabiensis vector populations by installed water distribution and catchment systems. Malar J 10: 149. doi:10.1186/1475-2875-10-149. PubMed: 21639926.
62. Dongus S, Nyika D, Kannady K, Mtasiwa D, Mshinda H et al. (2009) Urban agriculture and Anopheles habitats in Dar es Salaam, Tanzania. Geospat Health 3: 189-210. PubMed: 19440962.
63. Ndenga BA, Simbauni JA, Mbugi JP, Githeko AK (2012) Physical, Chemical and Biological Characteristics in Habitats of High and Low Presence of Anopheline Larvae in Western Kenya Highlands. PLOS ONE 7: e47975. doi:10.1371/journal.pone.0047975. PubMed: 23110145.
64. Halekoh U, Højsgaard S, Yan J (2006) The R package geepack for generalized estimating equations. Journal of Statistical Software 15: 1-11.
65. Canty A, Ripley B (2012) Boot: bootstrap R (S-Plus) functions. R package version 1.3-7.
66. R Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
67. Zou GY (2008) On the estimation of additive interaction by use of the four-by-two table and beyond. Am J Epidemiol 168: 212-224. doi:10.1093/aje/ kwn104. PubMed: 18511428.
68. Smith T, Charlwood JD, Takken W, Tanner M, Spiegelhalter DJ (1995) Mapping the densities of malaria vectors within a single village. Acta Trop 59: 1-18. doi:10.1016/0001-706X(94)00082-C. PubMed: 7785522.
69. Kiware SS, Chitnis N, Moore SJ, Devine GJ, Majambere S et al. (2012) Simplified models of vector control impact upon malaria transmission by zoophagic mosquitoes. PLOS ONE 7: e37661. doi:10.1371/journal.pone.0037661. PubMed: 22701527.
70. Kitau J, Oxborough RM, Tungu PK, Matowo J, Malima RC et al. (2012) Species shifts in the Anopheles gambiae complex: do LLINs successfully control Anopheles arabiensis? PLOS ONE 7: e31481. doi:10.1371/journal.pone.0031481. PubMed: 22438864.
71. Okumu FO, Mbeyela E, Lingamba G, Moore J, Ntamatungiro AJ et al. (2013) Comparative field evaluation of combinations of long-lasting insecticide treated nets and indoor residual spraying, relative to either method alone, for malaria prevention in an area where the main vector is Anopheles arabiensis. Parasites and Vectors 6: 46.
72. Govella NJ, Chaki PP, Killeen GF (2013) Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations. Malar J 12: 124. doi:10.1186/1475-2875-12-124. PubMed: 23577656.
73. Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE et al. (2004) A global index representing the stability of malaria transmission. Am J Trop Med Hyg 70: 486-498. PubMed: 15155980.
74. Gimnig JE, Ombok M, Kamau L, Hawley WA (2001) Characteristics of larval anopheline (Diptera: Culicidae) habitats in Western Kenya. J Med Entomol 38: 282-288. doi:10.1603/0022-2585-38.2.282. PubMed: 11296836.
75. Tuno N, Githeko A, Yan G, Takagi M (2007) Interspecific variation in diving activity among Anopheles gambiae Giles, An. arabiensis Patton, and An. funestus Giles (Diptera: Culicidae) larvae. Journal of Vector Ecology 32: 112-117.
76. Jacob BG, Arheart KL, Griffith DA, Mbogo CM, Githeko AK et al. (2005) Evaluation of environmental data for identification of Anopheles (Diptera: Culicidae) aquatic larval habitats in Kisumu and Malindi, Kenya. J Med Entomol 42: 751-755. Available online at: doi:10.1603/0022-2585(2005)042[0751:EOEDFI]2. 0.CO;2. PubMed: 16365996
77. Dukeen MY, Omer S (1986) Ecology of the malaria vector Anopheles arabiensis Patton(Diptera: Culicidae) by the Nile in northern Sudan. Bulletin of Entomological Research 76: 451-467. doi:10.1017/S0007485300014942.
78. Shousha AT (1948) Species-eradication: The Eradication of Anopheles gambiae from Upper Egypt, 1942-1945. Bull World Health Organ 1: 309-352. PubMed: 20603927.
79. Himeidan YE, Elzaki MM, Kweka EJ, Ibrahim M, Elhassan IM (2011) Pattern of malaria transmission along the Rahad River basin, Eastern Sudan. Parasit Vectors 4: 1-9. PubMed: 21679459.
80. Craig M, Snow R, Le Sueur D (1999) A climate-based distribution model of malaria transmission in sub-Saharan. Africa - Parasitology Today 15: 105-111. doi:10.1016/S0169-4758(99)01396-4.
81. Hoshen MB, Morse AP (2004) A weather-driven model of malaria transmission. Malar J 3: 32. doi:10.1186/1475-2875-3-32. PubMed: 15350206.
82. Thomson MC, Doblas-Reyes FJ, Mason SJ, Hagedorn R, Connor SJ et al. (2006) Malaria early warnings based on seasonal climate forecasts from multi-model ensembles. Nature 439: 576-579. doi:10.1038/nature04503. PubMed: 16452977.