Temporal and micro-spatial heterogeneity in the distribution of Anopheles vectors of malaria along the Kenyan coast

Particle and Fibre Toxicology

Janet T Midega²  John C Beier⁴  Charles Mbogo⁵  Joseph M Mwangangi⁵  María-Gloria Basáñez³  Peter Winskill¹  Martin Walker³ 

[1] MRC Centre for Outbreak Analysis & Modelling, Department of Infectious Disease Epidemiology, Imperial College London, London W2 1PG, UK;Department of Life Sciences, Division of Cell & Molecular Biology, Imperial College, South Kensington Campus, London SW7 2AZ, UK;Department of Infectious Disease Epidemiology, School of Public Health, Faculty of Medicine (St Mary’s campus), Imperial College London, Norfolk Place, London W2 1PG, UK;Department of Public Health Sciences, Miller School of Medicine University of Miami, Miami, USA;Vector Biology Department, KEMRI/Wellcome Trust Research Programme, P.O. Box 230–80108, Kilifi, Kenya

关键词: Kenya;    Kilifi;    Malaria;    Mosquito density;    Larval habitats;    Household occupancy;    Temperature;    Rainfall;    Polynomial distributed lag generalized linear mixed models;    Anopheles funestus;    Anopheles gambiae;   

Others  :  824066
DOI  :  10.1186/1756-3305-6-311

 received in 2013-06-18, accepted in 2013-10-04,  发布年份 2013

【 摘 要 】

Background

The distribution of anopheline mosquitoes is determined by temporally dynamic environmental and human-associated variables, operating over a range of spatial scales. Macro-spatial short-term trends are driven predominantly by prior (lagged) seasonal changes in climate, which regulate the abundance of suitable aquatic larval habitats. Micro-spatial distribution is determined by the location of these habitats, proximity and abundance of available human bloodmeals and prevailing micro-climatic conditions. The challenge of analysing—in a single coherent statistical framework—the lagged and distributed effect of seasonal climate changes simultaneously with the effects of an underlying hierarchy of spatial factors has hitherto not been addressed.

Methods

Data on Anopheles gambiae sensu stricto and A. funestus collected from households in Kilifi district, Kenya, were analysed using polynomial distributed lag generalized linear mixed models (PDL GLMMs).

Results

Anopheline density was positively and significantly associated with amount of rainfall between 4 to 47 days, negatively and significantly associated with maximum daily temperature between 5 and 35 days, and positively and significantly associated with maximum daily temperature between 29 and 48 days in the past (depending on Anopheles species). Multiple-occupancy households harboured greater mosquito numbers than single-occupancy households. A significant degree of mosquito clustering within households was identified.

Conclusions

The PDL GLMMs developed here represent a generalizable framework for analysing hierarchically-structured data in combination with explanatory variables which elicit lagged effects. The framework is a valuable tool for facilitating detailed understanding of determinants of the spatio-temporal distribution of Anopheles. Such understanding facilitates delivery of targeted, cost-effective and, in certain circumstances, preventative antivectorial interventions against malaria.

【 授权许可】

   
2013 Walker et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Baily NTJ: The Biomathematics of Malaria. Bath: Pitman Press; 1982.
• [2]Service MW: Mosquito Ecology. Field Sampling Methods. 2nd edition. London: Chapman & Hall; 1993.
• [3]Texier G, Machault V, Barragti M, Boutin JP, Rogier C: Environmental determinant of malaria cases among travellers. Malar J 2013, 12:87. BioMed Central Full Text
• [4]Githeko AK, Lindsay SW, Confalonieri UE, Patz JA: Climate change and vector-borne diseases: a regional analysis. Bull World Health Organ 2000, 78:1136-1147.
• [5]Gage KL, Burkot TR, Eisen RJ, Hayes EB: Climate and vectorborne diseases. Am J Prev Med 2008, 35:436-450.
• [6]Craig MH, Snow RW, le Sueur D: A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol Today 1999, 15:105-111.
• [7]Ernst KC, Adoka SO, Kowuor DO, Wilson ML, John CC: Malaria hotspot areas in a highland Kenya site are consistent in epidemic and non-epidemic years and are associated with ecological factors. Malar J 2006, 5:78. BioMed Central Full Text
• [8]Kulkarni MA, Desrochers RE, Kerr JT: High resolution niche models of malaria vectors in northern Tanzania: a new capacity to predict malaria risk? PLoS ONE 2010, 5:e9396.
• [9]Cairns M, Roca-Feltrer A, Garske T, Wilson AL, Diallo D, Milligan PJ, Ghani AC, Greenwood BM: Estimating the potential public health impact of seasonal malaria chemoprevention in African children. Nat Commun 2012, 3:881.
• [10]Parham PE, Michael E: Modeling the effects of weather and climate change on malaria transmission. Environ Health Perspect 2010, 118:620-626.
• [11]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.
• [12]Gu W, Utzinger J, Novak RJ: Habitat-based larval interventions: a new perspective for malaria control. Am J Trop Med Hyg 2008, 78:2-6.
• [13]Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE, Sachs J: A global index representing the stability of malaria transmission. Am J Trop Med Hyg 2004, 70:486-498.
• [14]Githeko AK, Service MW, Mbogo CM, Atieli FK, Juma FO: Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya. Acta Trop 1994, 58:307-316.
• [15]Killeen GF, McKenzie FE, Foy BD, Bogh C, Beier JC: The availability of potential hosts as a determinant of feeding behaviours and malaria transmission by African mosquito populations. Trans R Soc Trop Med Hyg 2001, 95:469-476.
• [16]Midega JT, Smith DL, Olotu A, Mwangangi JM, Nzovu JG, Wambua J, Nyangweso G, Mbogo CM, Christophides GK, Marsh K, Bejon P: Wind direction and proximity to larval sites determines malaria risk in Kilifi District in Kenya. Nat Commun 2012, 3:674.
• [17]Takken W, Knols BG: Odor-mediated behaviour of Afrotropical malaria mosquitoes. Ann Rev Entomol 1999, 44:131-157.
• [18]Costantini C, Li SG, Della Torre A, Sagnon N, Coluzzi M, Taylor CE: Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a west African Sudan savanna village. Med Vet Entomol 1996, 10:203-219.
• [19]Parham PE, Pople D, Christiansen-Jucht C, Lindsay S, Hinsley W, Michael E: Modeling the role of environmental variables on the population dynamics of the malaria vector Anopheles gambiae sensu stricto. Malar J 2012, 11:271. BioMed Central Full Text
• [20]Hoshen MB, Morse AP: A weather-driven model of malaria transmission. Malar J 2004, 3:32. BioMed Central Full Text
• [21]Ermert V, Fink AH, Jones AE, Morse AP: Development of a new version of the Liverpool Malaria Model. I. Refining the parameter settings and mathematical formulation of basic processes based on a literature review. Malar J 2011, 10:35. BioMed Central Full Text
• [22]Ageep TB, Cox J, Hassan MM, Knols BG, Benedict MQ, Malcolm CA, Babiker A, El Sayed BB: Spatial and temporal distribution of the malaria mosquito Anopheles arabiensis in northern Sudan: influence of environmental factors and implications for vector control. Malar J 2009, 8:123. BioMed Central Full Text
• [23]Mbogo CM, Mwangangi JM, Nzovu J, Gu W, Yan G, Gunter JT, Swalm C, Keating J, Regens JL, Shililu JI, Githure JI, Beier JC: Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg 2003, 68:734-742.
• [24]Ribeiro JM, 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.
• [25]Peterson AT: Shifting suitability for malaria vectors across Africa with warming climates. BMC Infect Dis 2009, 9:59. BioMed Central Full Text
• [26]Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH, Gething PW, Kabaria CW, Okara RM, Van Boeckel T, Godfray HC, Harbach RE, Hay SI: The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis. Parasit Vectors 2010, 3:117. BioMed Central Full Text
• [27]Kristan M, Abeku TA, Beard J, Okia M, Rapuoda B, Sang J, Cox J: Variations in entomological indices in relation to weather patterns and malaria incidence in East African highlands: implications for epidemic prevention and control. Malar J 2008, 7:231. BioMed Central Full Text
• [28]Tanser FC, Sharp B, le Sueur D: Potential effect of climate change on malaria transmission in Africa. Lancet 2003, 362:1792-1798.
• [29]Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D, Killeen GF: Ecology: a prerequisite for malaria elimination and eradication. PLoS Med 2010, 7:e1000303.
• [30]Garske T, Ferguson NM, Ghani AC: Estimating air temperature and its influence on malaria transmission across Africa. PLoS ONE 2013, 8:e56487.
• [31]Russell TL, Lwetoijera DW, Knols BG, Takken W, Killeen GF, Kelly-Hope LA: Geographic coincidence of increased malaria transmission hazard and vulnerability occurring at the periphery of two Tanzanian villages. Malar J 2013, 12:24. BioMed Central Full Text
• [32]Teklehaimanot HD, Schwartz J, Teklehaimanot A, Lipsitch M: Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia II. Weather-based prediction systems perform comparably to early detection systems in identifying times for interventions. Malar J 2004, 3:44. BioMed Central Full Text
• [33]Jones AE, Morse AP: Application and validation of a seasonal ensemble prediction system using a dynamic malaria model. J Clim 2010, 23:4202-4215.
• [34]Teklehaimanot HD, Lipsitch M, Teklehaimanot A, Schwartz J: Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia I. Patterns of lagged weather effects reflect biological mechanisms. Malar J 2004, 3:41. BioMed Central Full Text
• [35]Patz JA, Strzepek K, Lele S, Hedden M, Greene S, Noden B, Hay SI, Kalkstein L, Beier JC: Predicting key malaria transmission factors, biting and entomological inoculation rates, using modelled soil moisture in Kenya. Trop Med Int Health 1998, 3:818-827.
• [36]Cottrell G, Kouwaye B, Pierrat C, le Port A, Bouraima A, Fonton N, Hounkonnou MN, Massougbodji A, Corbel V, Garcia A: Modeling the influence of local environmental factors on malaria transmission in Benin and its implications for cohort study. PLoS ONE 2012, 7:e28812.
• [37]Yé Y, Hoshen M, Kyobutungi C, Louis VR, Sauerborn R: Local scale prediction of Plasmodium falciparum malaria transmission in an endemic region using temperature and rainfall. Glob Health Action 2009., 2doi: 10.3402/gha.v2i0.1923
• [38]Bayoh MN, Lindsay SW: Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae). Bull Entomol Res 2003, 93:375-381.
• [39]Kirby MJ, Lindsay SW: Effect of temperature and inter-specific competition on the development and survival of Anopheles gambiae sensu stricto and An. arabiensis larvae. Acta Trop 2009, 109:118-123.
• [40]Lyons CL, Coetzee M, Chown SL: 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
• [41]Patz JA, Olson SH: Malaria risk and temperature: influences from global climate change and local land use practices. Proc Natl Acad Sci U S A 2006, 103:5635-5636.
• [42]Galardo AKR, Zimmerman RH, Lounibos LP, Young LJ, Galardo CD, Arruda M, Couto AARD: Seasonal abundance of anopheline mosquitoes and their association with rainfall and malaria along the Matapi River, Amapi, Brazil. Med Vet Entomol 2009, 23:335-349.
• [43]Alemu A, Abebe G, Tsegaye W, Golassa L: Climatic variables and malaria transmission dynamics in Jimma town. South West Ethiopia. Parasit Vectors 2011, 4:30. BioMed Central Full Text
• [44]Zacarias OP, Andersson M: Spatial and temporal patterns of malaria incidence in Mozambique. Malar J 2011, 10:189. BioMed Central Full Text
• [45]Diggle P, Heagerty P, Liang K-Y, Zeger S: Analysis of Longitudinal Data. Oxford: Oxford University Press; 2002.
• [46]McCullagh P, Nelder JA: Generalized Linear Models. 2nd edition. London: Chapman & Hall; 1989.
• [47]Paterson S, Lello J: Mixed models: getting the best use of parasitological data. Trends Parasitol 2003, 19:370-375.
• [48]Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MH, White JS: Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 2009, 24:127-135.
• [49]Mosha FW, Mutero CM: Separation of Anopheles merus from freshwater Anopheles gambiae by salinity tolerance test and morphological characters. Parassitologia 1982, 24:255-264.
• [50]Mosha FW, Petrarca V: Ecological studies on Anopheles gambiae complex sibling species on the Kenya coast. Trans R Soc Trop Med Hyg 1983, 77:344-345.
• [51]Mbogo CN, Baya NM, Ofulla AV, Githure JI, Snow RW: The impact of permethrin-impregnated bednets on malaria vectors of the Kenyan coast. Med Vet Entomol 1996, 10:251-259.
• [52]Mbogo CN, Glass GE, Forster D, Kabiru EW, Githure JI, Ouma JH, Beier JC: Evaluation of light traps for sampling anopheline mosquitoes in Kilifi, Kenya. J Am Mosq Control Assoc 1993, 9:260-263.
• [53]Mbogo CN, Kabiru EW, Muiruri SK, Nzovu JM, Ouma JH, Githure JI, Beier JC: Bloodfeeding behavior of Anopheles gambiae s.l. and Anopheles funestus in Kilifi District, Kenya. J Am Mosq Control Assoc 1993, 9:225-227.
• [54]Mbogo CNM, Snow RW, Khamala CPM, Kabiru EW, Ouma JH, Githure JI, Marsh K, Beier JC: Relationships between Plasmodium falciparum transmission by vector populations and the incidence of severe disease at 9 sites on the Kenyan coast. Am J Trop Med Hyg 1995, 52:201-206.
• [55]Mwangangi JM, Mbogo CM, Nzovu JG, Kabiru EW, Mwambi H, Githure JI, Beier JC: Relationships between body size of Anopheles mosquitoes and Plasmodium falciparum sporozoite rates along the Kenya coast. J Am Mosq Control Assoc 2004, 20:390-394.
• [56]Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, Olotu A, Osier FH, Hay SI, Färnert A, Marsh K: Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med 2010, 7:e1000304.
• [57]Okiro EA, Alegana VA, Noor AM, Snow RW: Changing malaria intervention coverage, transmission and hospitalization in Kenya. Malar J 2010, 9:285. BioMed Central Full Text
• [58]O'Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, Newton CR, Marsh K: Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 2008, 372:1555-1562.
• [59]Mwangangi JM, Mbogo CM, Orindi BO, Muturi EJ, Midega JT, Nzovu J, Gatakaa H, Githure J, Borgemeister C, Keating J, Beier JC: Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J 2013, 12:13. BioMed Central Full Text
• [60]World Health Organization: Manual on Practical Entomology in Malaria. Part 2: Methods and Techniques. Geneva: World Health Organization; 1975.
• [61]Gillies MT, Coetzee M: Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region). Johannesburg: South African Institute of Medical Research; 1987.
• [62]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, 49:520-529.
• [63]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, 66:804-811.
• [64]R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2011.
• [65]Elston DA, Moss R, Boulinier T, Arrowsmith C, Lambin X: Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 2001, 122:563-569.
• [66]Bolker BM: Ecological Models and Data in R. Prinecton: Princeton University Press; 2008.
• [67]Almon S: The distributed lag between capital appropriations and net expenditure. Econometrica 1965, 33:178-196.
• [68]le Sueur D, Sharp BL: Temperature-dependent variation in Anopheles merus larval head capsule width and adult wing length: implications for anopheline taxonomy. Med Vet Entomol 1991, 5:55-62.
• [69]Rueda LM, Patel KJ, Axtell RC, Stinner RE: Temperature-dependent development and survival rates of Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). J Med Entomol 1990, 27:892-898.
• [70]Draper NR, Smith H: Applied Regression Analysis. New York: John Wiley & Sons; 1998.
• [71]Kirkwood BR, Sterne JAC: Essential Medical Statistics. 2nd edition. Oxford: Blackwell Science; 2003.
• [72]Kelly-Hope LA, Hemingway J, McKenzie FE: Environmental factors associated with the malaria vectors Anopheles gambiae and Anopheles funestus in Kenya. Malar J 2009, 8:268. BioMed Central Full Text
• [73]Lyons CL, Coetzee M, Terblanche JS, Chown SL: Thermal limits of wild and laboratory strains of two African malaria vector species, Anopheles arabiensis and Anopheles funestus. Malar J 2012, 11:226. BioMed Central Full Text
• [74]Koenraadt CJ, Githeko AK, Takken W: The effects of rainfall and evapotranspiration on the temporal dynamics of Anopheles gambiae s.s. and Anopheles arabiensis in a Kenyan village. Acta Trop 2004, 90:141-153.
• [75]Sinka ME, Bangs MJ, Manguin S, Chareonviriyaphap T, Patil AP, Temperley WH, Gething PW, Elyazar IR, Kabaria CW, Harbach RE, Hay SI: The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic précis. Parasit Vectors 2011, 4:89. BioMed Central Full Text
• [76]Lindsay SW, Parson L, Thomas CJ: Mapping the ranges and relative abundance of the two principal African malaria vectors, Anopheles gambiae sensu stricto and An. arabiensis, using climate data. Proc Biol Sci 1998, 265:847-854.
• [77]Okech BA, Gouagna LC, Killeen GF, Knols BG, Kabiru EW, Beier JC, Yan G, Githure JI: Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in western Kenya. J Med Entomol 2003, 40:657-663.
• [78]Kirby MJ, Lindsay SW: Responses of adult mosquitoes of two sibling species, Anopheles arabiensis and A. gambiae s.s. (Diptera: Culicidae), to high temperatures. Bull Entomol Res 2004, 94:441-448.
• [79]Platt RB, Collins CL, Witherspoon JP: Reactions of Anopheles quadrimaculatus Say to moisture, temperature and light. Ecol Monogr 1957, 27:303-324.
• [80]Amek N, Bayoh N, Hamel M, Lindblade KA, Gimnig JE, Odhiambo F, Laserson KF, Slutsker L, Smith T, Vounatsou P: Spatial and temporal dynamics of malaria transmission in rural Western Kenya. Parasit Vectors 2012, 5:86. BioMed Central Full Text
• [81]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.
• [82]Gillies MT: The role of carbon-dioxide in host-finding by mosquitos (Diptera, Culicidae) - a review. Bull Entomol Res 1980, 70:525-532.
• [83]Winskill P, Rowland M, Mtove G, Malima RC, Kirby MJ: Malaria risk factors in north-east Tanzania. Malar J 2011, 10:98. BioMed Central Full Text
• [84]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.
• [85]Mboera LE, Senkoro KP, Mayala BK, Rumisha SF, Rwegoshora RT, Mlozi MR, Shayo EH: Spatio-temporal variation in malaria transmission intensity in five agro-ecosystems in Mvomero district, Tanzania. Geospat Health 2010, 4:167-178.
• [86]Carter R, Mendis KN, Roberts D: Spatial targeting of interventions against malaria. Bull World Health Organ 2000, 78:1401-1411.
• [87]O'Meara WP, Mangeni JN, Steketee R, Greenwood B: Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis 2010, 10:545-555.
• [88]Noor AM, Amin AA, Akhwale WS, Snow RW: Increasing coverage and decreasing inequity in insecticide-treated bed net use among rural Kenyan children. PLoS Med 2007, 4:e255.
• [89]Noor AM, Mutheu JJ, Tatem AJ, Hay SI, Snow RW: Insecticide-treated net coverage in Africa: mapping progress in 2000–07. Lancet 2009, 373:58-67.
• [90]Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, Ter Kuile FO, Vulule JM, Slutsker L: Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol 2006, 43:428-432.