Modeling larval malaria vector habitat locations using landscape features and cumulative precipitation measures

Springer Science and Business Media LLC - Tập 13 - Trang 1-12 - 2014
Robert S McCann1,2, Joseph P Messina3, David W MacFarlane4, M Nabie Bayoh5, John M Vulule5, John E Gimnig6, Edward D Walker7
1Department of Entomology, Michigan State University, East Lansing, USA
2Laboratory of Entomology, Wageningen University and Research Centre, Wageningen, Netherlands
3Department of Geography, Michigan State University, East Lansing, USA
4Department of Forestry, Michigan State University, East Lansing, USA
5Centre for Global Health Research, Kenya Medical Research Institute/Centers for Disease Control and Prevention, Kisumu, Kenya
6Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, USA
7Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, USA

Tóm tắt

Predictive models of malaria vector larval habitat locations may provide a basis for understanding the spatial determinants of malaria transmission. We used four landscape variables (topographic wetness index [TWI], soil type, land use-land cover, and distance to stream) and accumulated precipitation to model larval habitat locations in a region of western Kenya through two methods: logistic regression and random forest. Additionally, we used two separate data sets to account for variation in habitat locations across space and over time. Larval habitats were more likely to be present in locations with a lower slope to contributing area ratio (i.e. TWI), closer to streams, with agricultural land use relative to nonagricultural land use, and in friable clay/sandy clay loam soil and firm, silty clay/clay soil relative to friable clay soil. The probability of larval habitat presence increased with increasing accumulated precipitation. The random forest models were more accurate than the logistic regression models, especially when accumulated precipitation was included to account for seasonal differences in precipitation. The most accurate models for the two data sets had area under the curve (AUC) values of 0.864 and 0.871, respectively. TWI, distance to the nearest stream, and precipitation had the greatest mean decrease in Gini impurity criteria in these models. This study demonstrates the usefulness of random forest models for larval malaria vector habitat modeling. TWI and distance to the nearest stream were the two most important landscape variables in these models. Including accumulated precipitation in our models improved the accuracy of larval habitat location predictions by accounting for seasonal variation in the precipitation. Finally, the sampling strategy employed here for model parameterization could serve as a framework for creating predictive larval habitat models to assist in larval control efforts.

Tài liệu tham khảo

World Health Organization: World Malaria Report 2012. 2012, Geneva: World Health Organization, 1-276. Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IR, Johnston GL, Tatem AJ, Hay SI: A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J. 2011, 10: 378-10.1186/1475-2875-10-378. Greenwood BM: The microepidemiology of malaria and its importance to malaria control. Trans R Soc Trop Med Hyg. 1989, 83 (Suppl): 25-29. Gamage-Mendis AC, Carter R, Mendis C, De Zoysa AP, Herath PR, Mendis KN: Clustering of malaria infections within an endemic population: risk of malaria associated with the type of housing construction. Am J Trop Med Hyg. 1991, 45: 77-85. Trape J-F, Lefebvre-Zante E, Legros F, Ndiaye G, Bouganali H, Druilhe P, Salem G: Vector density gradients and the epidemiology of urban malaria in Dakar, Senegal. Am J Trop Med Hyg. 1992, 47: 181-189. Clark TD, Greenhouse B, Njama Meya D, Nzarubara B, Maiteki Sebuguzi C, Staedke SG, Seto E, Kamya MR, Rosenthal PJ, Dorsey G: Factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. J Infect Dis. 2008, 198: 393-400. 10.1086/589778. Cohen JM, Ernst KC, Lindblade KA, Vulule JM, John CC, Wilson ML: Local topographic wetness indices predict household malaria risk better than land-use and land-cover in the western Kenya highlands. Malar J. 2010, 9: 328-10.1186/1475-2875-9-328. Zhou G, Minakawa N, Githeko AK, Yan G: Spatial distribution patterns of malaria vectors and sample size determination in spatially heterogeneous environments: a case study in the West Kenyan highland. J Med Entomol. 2004, 41: 1001-1009. 10.1603/0022-2585-41.6.1001. Bogh C, Lindsay SW, Clarke SE, Dean A, Jawara M, Pinder M, Thomas CJ: High spatial resolution mapping of malaria transmission risk in the Gambia, west Africa, using LANDSAT TM satellite imagery. Am J Trop Med Hyg. 2007, 76: 875-881. Ribeiro JMC, Seulu F, Abose T, Kidane G, Teklehaimanot A: Temporal and spatial distribution of anopheline mosquitos in an Ethiopian village: implications for malaria control strategies. Bull World Health Organ. 1996, 74: 299-305. Coetzee M, Hunt RH, Wilkerson RC, Torre della A, Coulibaly MB, Besansky NJ: Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013, 3619: 246-274. Gimnig JE, Ombok M, Kamau L, Hawley WA: Characteristics of larval anopheline (Diptera: Culicidae) habitats in western Kenya. J Med Entomol. 2001, 38: 282-288. 10.1603/0022-2585-38.2.282. Minakawa N, Mutero CM, Githure JI, Beier JC, Yan G: Spatial distribution and habitat characterization of anopheline mosquito larvae in western Kenya. Am J Trop Med Hyg. 1999, 61: 1010-1016. Charlwood JD, Edoh D: Polymerase chain reaction used to describe larval habitat use by Anopheles gambiae complex (Diptera: Culicidae) in the environs of Ifakara, Tanzania. J Med Entomol. 1996, 33: 202-204. Mutuku FM, Alaii JA, Bayoh MN, Gimnig JE, Vulule JM, Walker ED, Kabiru E, Hawley WA: Distribution, description, and local knowledge of larval habitats of Anopheles gambiae s.l. in a village in western Kenya. Am J Trop Med Hyg. 2006, 74: 44-53. Mutuku F, Bayoh MN, Hightower A, Vulule JM, Gimnig JE, Mueke J, Amimo F, Walker ED: A supervised land cover classification of a western Kenya lowland endemic for human malaria: associations of land cover with larval Anopheles habitats. Int J Health Geogr. 2009, 8: 19-10.1186/1476-072X-8-19. Mushinzimana E, Munga S, Minakawa N, Li L, Feng C-C, Bian L, Kitron U, Schmidt C, Beck L, Zhou G, Githeko AK, Yan G: Landscape determinants and remote sensing of anopheline mosquito larval habitats in the western Kenya highlands. Malar J. 2006, 5: 13-10.1186/1475-2875-5-13. Beven KJ, Kirkby MJ: A physically based, variable contributing area model of basin hydrology. Hydrol Sci Bull. 1979, 24: 43-69. 10.1080/02626667909491834. Clennon JA, Kamanga A, Musapa M, Shiff C, Glass GE: Identifying malaria vector breeding habitats with remote sensing data and terrain-based landscapeindices in Zambia. Int J Health Geogr. 2010, 9: 58-10.1186/1476-072X-9-58. Li L, Bian L, Yakob L, Zhou G, Yan G: Analysing the generality of spatially predictive mosquito habitat models. Acta Trop. 2011, 119: 30-37. 10.1016/j.actatropica.2011.04.003. Nmor JC, 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: 14-10.1186/1756-3305-6-14. Bogh C, Clarke SE, Jawara M, Thomas CJ, Lindsay SW: Localized breeding of the Anopheles gambiae complex (Diptera: Culicidae) along the River Gambia, West Africa. Bull Entomol Res. 2003, 93: 279-287. Munga S, Yakob L, Mushinzimana E, Zhou G, Ouna T, Minakawa N, Githeko AK, 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: 1079-1084. 10.4269/ajtmh.2009.09-0156. Phillips-Howard PA, Nahlen BL, Alaii JA, ter FO K, Gimnig JE, Terlouw DJ, Kachur SP, Hightower AW, Lal AA, Schoute E, Oloo AJ, Hawley WA: 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. 2003, 68: 3-9. Hamel MJ, Adazu K, Obor D, Sewe M, Vulule JM, Williamson JM, Slutsker L, Feikin DR, Laserson KF: A reversal in reductions of child mortality in western Kenya, 2003-2009. Am J Trop Med Hyg. 2011, 85: 597-605. 10.4269/ajtmh.2011.10-0678. Hurlbert SH: Pseudoreplication and the design of ecological field experiments. Ecol Monogr. 1984, 54: 187-211. 10.2307/1942661. Taylor KA, Koros JK, Nduati J, Copeland RS, Collins FH, Brandling-Bennett AD: Plasmodium falciparum infection rates in Anopheles gambiae, An. arabiensis, and An. funestus in western Kenya. Am J Trop Med Hyg. 1990, 43: 124-129. Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, Whitmire RE, Koech DK, Roberts CR: Characterization of malaria transmission by Anopheles (Diptera: Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol. 1990, 27: 570-577. Odiere M, Bayoh MN, Gimnig JE, Vulule JM, Irungu L, Walker ED: Sampling outdoor, resting Anopheles gambiae and other mosquitoes (Diptera: Culicidae) in western Kenya with clay pots. J Med Entomol. 2007, 44: 14-22. 10.1603/0022-2585(2007)44[14:SORAGA]2.0.CO;2. Gillies MT, Coetzee M: A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region). 1987, Johannesburg, South Africa: South African Institute for Medical Research, 1-143. Sombroek WG, Braun HMH, van der Pouw BJA: Exploratory Soil Map and Agro-Climatic Zone Map of Kenya, 1980. Scale 1: 1,000,000. 1982, Nairobi, Kenya: Kenya Soil Survey MacQueen J: Some methods for classification and analysis of multivariate observations. Proceedings of the fifth Berkeley symposium on mathematical statistics and probability, Volume 1. 1967, 281-297. Hightower AW, Ombok M, Otieno R, Odhiambo R, Oloo AJ, Lal AA, Nahlen BL, Hawley WA: A geographic information system applied to a malaria field study in western Kenya. Am J Trop Med Hyg. 1998, 58: 266-272. Ombok M, Adazu K, Odhiambo F, Bayoh MN, Kiriinya R, Slutsker L, Hamel MJ, Williamson J, Hightower A, Laserson KF, Feikin DR: Geospatial distribution and determinants of child mortality in rural western Kenya 2002-2005. Trop Med Int Health. 2010, 15: 423-433. 10.1111/j.1365-3156.2010.02467.x. Tarboton DG: A new method for the determination of flow directions and upslope areas in grid digital elevation models. Water Resour Res. 1997, 33: 309-319. 10.1029/96WR03137. Breiman L: Random forests. Mach Learn. 2001, 45: 5-32. 10.1023/A:1010933404324. Guisan A, Zimmermann NE: Predictive habitat distribution models in ecology. Ecol Model. 2000, 135: 147-186. 10.1016/S0304-3800(00)00354-9. Hernández J, Núñez I, Bacigalupo A, Cattan PE: Modeling the spatial distribution of Chagas disease vectors using environmental variables and people's knowledge. Int J Health Geogr. 2013, 12: 29-10.1186/1476-072X-12-29. Bisrat SA, White MA, Beard KH, Richard Cutler D: Predicting the distribution potential of an invasive frog using remotely sensed data in Hawaii. Divers Distrib. 2011, 18: 648-660. Breiman L, Friedman JH, Olshen RA, Stone CJ: Classification and Regression Trees (CART). 1984, Belmont, CA, USA: Wadsworth International Group Liaw A, Wiener M: Classification and regression by randomForest. R News. 2002, 2: 18-22. Liu C, Berry PM, Dawson TP, Pearson RG: Selecting thresholds of occurrence in the prediction of species distributions. Ecography. 2005, 28: 385-393. 10.1111/j.0906-7590.2005.03957.x. Swets JA: Measuring the accuracy of diagnostic systems. Science. 1988, 240: 1285-1293. 10.1126/science.3287615. Package “SDMTools”.http://cran.r-project.org/web/packages/SDMTools/SDMTools.pdf, Grabs T, Seibert J, Bishop K, Laudon H: Modeling spatial patterns of saturated areas: a comparison of the topographic wetness index and a dynamic distributed model. J Hydrol. 2009, 373: 15-23. 10.1016/j.jhydrol.2009.03.031. Amek N, Bayoh MN, Hamel M, Lindblade KA, Gimnig JE, Odhiambo F, Laserson KF, Slutsker L, Smith TA, Vounatsou P: Spatial and temporal dynamics of malaria transmission in rural Western Kenya. Parasit Vectors. 2012, 5: 1-10.1186/1756-3305-5-1. Omumbo JA, Hay SI, Snow RW, Tatem AJ, Rogers DJ: Modelling malaria risk in East Africa at high-spatial resolution. Trop Med Int Health. 2005, 10: 557-566. 10.1111/j.1365-3156.2005.01424.x. Moiroux N, Djènontin A, Bio-Bangana AS, Chandre F, Corbel V, Guis H: Spatio-temporal analysis of abundances of three malaria vector species in southern Benin using zero-truncated models. Parasit Vectors. 2014, 7: 103-10.1186/1756-3305-7-103. Jacob BG, Muturi E, Halbig P, Mwangangi J, Wanjogu RK, Mpanga E, Funes J, Shililu JI, Githure J, Regens JL, Novak RJ: Environmental abundance of Anopheles (Diptera: Culicidae) larval habitats on land cover change sites in Karima Village, Mwea Rice Scheme, Kenya. Am J Trop Med Hyg. 2007, 76: 73-80. Strauss B, Biedermann R: Evaluating temporal and spatial generality: how valid are species–habitat relationship models?. Ecol Model. 2007, 204: 104-114. 10.1016/j.ecolmodel.2006.12.027.