Spatial Relationship between Adult Malaria Vector Abundance and Environmental Factors in Western Kenya Highlands

Guofa Zhou Program in Public Health, College of Health Sciences, University of California, Irvine, California; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan

Search for other papers by Guofa Zhou in
Current site
Google Scholar
PubMed
Close
,
Stephen Munga Program in Public Health, College of Health Sciences, University of California, Irvine, California; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan

Search for other papers by Stephen Munga in
Current site
Google Scholar
PubMed
Close
,
Noboru Minakawa Program in Public Health, College of Health Sciences, University of California, Irvine, California; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan

Search for other papers by Noboru Minakawa in
Current site
Google Scholar
PubMed
Close
,
Andrew K. Githeko Program in Public Health, College of Health Sciences, University of California, Irvine, California; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan

Search for other papers by Andrew K. Githeko in
Current site
Google Scholar
PubMed
Close
, and
Guiyun Yan Program in Public Health, College of Health Sciences, University of California, Irvine, California; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan

Search for other papers by Guiyun Yan in
Current site
Google Scholar
PubMed
Close
Restricted access

Information on the spatial relationships between disease vectors and environmental factors is fundamental to vector-borne disease control. Although it is well known that mosquito abundance is associated with the amount of rainfall and thus the number of larval breeding sites, the spatial relationship between larval habitat availability and adult mosquito abundance is not clear. We investigated the impact of environmental heterogeneity and larval habitats on the spatial distribution of Anopheles gambiae s. s. and An. funestus adult mosquitoes, the most important malaria vectors in the highlands of western Kenya. Mosquito sampling was conducted in May, August, and November 2002, and February 2003. Geographic information system layers of larval habitats, land use type, human population distribution, house structure, and hydrologic schemes were overlaid with adult mosquito abundance. Correlography was used to determine the spatial autocorrelation in adult mosquito abundance among houses and the cross-correlation between adult mosquito abundance and environmental factors. Getis’ Gi*(d) index was used to define focal adult mosquito abundance clusters. We found a significant autocorrelation in the vector population and a significant cross-correlation between the vector population and larval habitat availability. The threshold distances of both autocorrelation and cross-correlation were significantly varied among seasons. Focal clustering analysis revealed that the adult vector population was concentrated along the Yala River Valley where most larval habitats were found. Regression analysis found that distance of a house to the Yala River, age of the house, elevation, house structure, and tree canopy coverage significantly affected adult mosquito abundance. Our results suggest that vector control targeted at malaria transmission hotspots and supplemented by larval control may be an effective approach for epidemic malaria control in the western Kenya highlands.

Author Notes

Reprint requests: Guiyun Yan, Program in Public Health, College of Health Sciences, University of California, Irvine, CA 92697.
  • 1

    Mendis C, Gamage-Mendis AC, de Zoysa AP, Abhayawardena TA, Carter R, Herath PRJ, Mendis KN, 1990. Characteristics of malaria transmission in Kataragama, Sri Lanka: a focus for immmunoepidemiological studies. Am J Trop Med Hyg 42 :298–308.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Gamage-Mendis AC, Carter R, Mendis C, de Zoysa AP, Herath PR, Mendis KN, 1991. Clustering of malaria infections within an endemic population: risk of malaria associated with house construction type. Am J Trop Med Hyg 45 :77–85.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Carter R, Mendis KN, Roberts D, 2000. Spatial targeting of interventions against malaria. Bull World Health Organ 78 :1401–1411.

  • 4

    Brooker S, Clarke S, Njagi JK, Polack S, Mugo S, Estambale B, Muchiri E, Magnussen E, Cox J, 2004. Spatial clustering of malaria and associated risk factors during an epidemic in a highland area of western Kenya. Trop Med Int Health 9 :757–766.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Munyekenye OG, Githeko AK, Zhou G, Mushinzimana E, Minakawa N, Yan G, 2005. Plasmodium falciparum spatial analysis, western Kenya highlands. Emerg Infect Dis 10 :1571–1577.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    van der Hoek W, Konradsen F, Dijkstra DS, Amerasinghe PH, Amerasinghe FP, 1998. Risk factors for malaria: a microepidemiological study in a village in Sri Lanka. Trans R Soc Trop Med Hyg 92 :265–269.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Minakawa N, Pamela S, 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
    • Search Google Scholar
    • Export Citation
  • 8

    Cano J, Descalzo MA, Moreno M, Chen Z, Nzambo S, Bobuakasi L, Buatiche JN, Ondo M, Micha F, Benito A, 2006. Spatial variability in the density, distribution and vectorial capacity of anopheline species in a high transmission village (Equatorial Guinea). Malaria J 5 :21.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Khaemba BM, Mutani A, Bett MK, 1994. Studies of anopheline mosquitoes transmitting malaria in a newly developed highland urban area: a case study of Moi University and its environs. East Afr Med J 71 :159–164.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Mouchet J, Manguin S, Sircoulon K, Lavnevale S, Faye S, Onapa AW, Carnevale P, Julvez J, Fontenille D, 1998. Evolution of malaria in Africa for the past 40 years: impact of climatic and human factors. J Am Mosq Control Assoc 14 :121–130.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Shililu JI, Maier WA, Seitz HM, Orago AS, 1998. 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 3 :706–710.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Lindblade KA, Walker ED, Onapa AW, Katungu J, Wilson ML, 2000. Land-use change alters malaria transmission parameters by modifying temperature in a highland area of Uganda. Trop Med Int Health 5 :263–274.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Minakawa N, Munga S, Atieli F, Mushinzimana E, Zhou G, Gethiko A, Yan G, 2005. Spatial distribution of anopheline larval habitats in western Kenya highlands: Effects of land cover types and topography. Am J Trop Med Hyg 73 :157–165.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Minakawa N, Omukunda E, Zhou G, Githeko AK, Yan G, 2006. Malaria vector productivity in relation to the highland environment in Kenya. Am J Trop Med Hyg 75 :448–453.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Munga S, Minakawa N, Zhou G, Mushinzimana E, Barrack OJ, Githeko AK, Yan G, 2006. Association between landcover and production of malaria vectors in the western Kenyan highland. Am J Trop Med Hyg 74 :69–75.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Lindsay SW, Martens WJ, 1998. Malaria in the African highlands: past, present and future. Bull World Health Organ 76 :33–45.

  • 17

    Malakooti MA, Biomndo K, Shanks GD, 1998. Reemergnece of epidemic malaria in the highlands of western Kenya. Emerg Infect Dis 4 :671–676.

  • 18

    Cox J, Craig M, le Sueur D, Sharp B, 1999. Mapping Malaria Risk in the Highlands of Africa. MARA/ARMA Technical Report. Durban, South Africa: MARA/ARMA.

    • PubMed
    • Export Citation
  • 19

    Githeko AK, Ndegwa W, 2001. Predicting malaria epidemics in the Kenyan highlands using climate data: a tool for decision makers. Glob Change Hum Health 2 :45–63.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Hay SI, Cox J, Rogers DJ, Randolph SE, Stern DI, Shanks GD, Myers MF, Snow RW, 2002. Climate change and the resurgence of malaria in the East African highlands. Nature 415 :905–909.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Shanks GD, Biomndo K, Hay HI, Snow RW, 2000. Changing patterns of clinical malaria since 1965 among a tea estate population located in the Kenyan highlands. Trans R Soc Trop Med Hyg 94 :253–255.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Shanks GD, Biomndo K, Maguire J, 2004. Travel as a risk factor for malaria requiring hospitalization on a highland tea plantation in western Kenya. J Travel Med 11 :354–357.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Shanks GD, Hay SI, Omumbo JA, Snow RW, 2005. Malaria in Kenya’s western highlands. Emerg Infect Dis 11 :1425–1432.

  • 24

    Zhou G, Minakawa N, Githeko A, Yan G, 2004. Association between climate variability and malaria epidemics in the East African highlands. Proc Natl Acad Sci U S A 101 :2375–2380.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Pascual M, Ahumada JA, Chaves F, Rodo X, Bouma M, 2006. Malaria resurgence in the east African highlands: temperature trends revisited. Proc Natl Acad Sci U S A 103 :5829–5834.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Round-Turner D, 1994. Kakamega Forest, the Official Guide 1994. Nairobi, Kenya: Kenya Indigenous Forest Conservation Programme.

    • PubMed
    • Export Citation
  • 27

    Food and Agriculture Organization, 2005. Global Forest Resources Assessment 2005: Progress towards Sustainable Forest Management. Rome: Food and Agricultural Organization. Forestry paper 147.

    • PubMed
    • Export Citation
  • 28

    Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G, 2006. Effects of microclimatic changes due to deforestation on the survivorship and reproductive fitness of Anopheles gambiae in western Kenya highlands. Am J Trop Med Hyg 74 :772–778.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Afrane YA, Lawson BW, Githeko AK, Yan G, 2005. Effects of microclimatic changes caused by land use and land cover on duration of gonotrophic cycles of Anopheles gambiae (Diptera: Culicidae) in western Kenya highlands. J Med Entomol 42 :974–980.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Minakawa N, Sonye G, Mogi M, Githeko A, Yan G, 2002. The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. J Med Entomol 39 :833–841.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Mushinzimana E, Munga S, Minakawa N, Li L, Feng C, Bian L, Kitron U, Schmidt C, Beck L, Zhou G, Githeko AK, Yan G, 2006. Comparison of three remote sensors for identification of anopheline mosquito larval habitats in western Kenya highlands. Malaria J 5 :13.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Ndenga B, Githeko A, Omukunda E, Munyekenye G, Atieli H, Wamai P, Mbogo C, Minakawa N, Zhou G, Yan G, 2006. Population dynamics of malaria vectors in western Kenya highlands. J Med Entomol 43 :200–206.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    World Health Organization, 1975. Manual on Practical Entomology in Malaria. Part II. Methods and Techniques. No. 13. Geneva: World Health Organization.

    • PubMed
    • Export Citation
  • 34

    Gillies MT, de Meillon B, 1968. The Anophelinae of Africa South of the Sahara. Johannesburg: The South African Institute for Medical Research.

    • PubMed
    • Export Citation
  • 35

    Campbell J, 1996. Introduction to Remote Sensing. London: The Guildford Press.

    • PubMed
    • Export Citation
  • 36

    Liebhold AM, Rossi RE, Kemp WP, 1993. Geostatistics and geographic information systems in applied insect ecology. Annu Rev Entomol 38 :303–327.

  • 37

    Lichstein JW, Simons TR, Shriner SA, Franzreb KE, 2002. Spatial autocorrelation and autoregressive models in ecology. Ecol Monogr 72 :445–463.

  • 38

    Clennon JA, King CH, Muchiri EM, Kariuki CH, Ouma JH, Mungai P, Kitron U, 2004. Spatial patterns of urinary schistosomiasis infection in a highlay endemic area of coastal Kenya. Am J Trop Med Hyg 70 :443–448.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Getis A, Morrison AC, Gray K, Scott T, 2003. Characteristics of the spatial pattern of the Dengue vector, Aedes aegypti, in Iquitos, Peru. Am J Trop Med Hyg 69 :494–505.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Ord JK, Getis A, 1995. Local spatial autocorrelation statistics: distributional issues and an application. Geog Anal 27 :286–306.

  • 41

    Getis A, 1990. Screening for spatial dependence in regression analysis. Pap Reg Sci Assoc 69 :69–81.

  • 42

    Costantini C, Li SG, Della-Torre A, Sagnon N, Coluzzi M, Taylor CE, 1996. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a west African Sudan savanna village. Med Vet Entomol 10 :203–219.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Toure YT, Dolo G, Petrarca V, Traore SF, Bouare M, Dao A, Carnahan J, Taylor CE, 1998. Mark-release-recapture experiments with Anopheles gambiae s.l. in Banambani Village, Mali, to determine population size and structure. Med Vet Entomol 12 :74–83.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Ribeiro JM, Seulu F, Abose T, Kidane G, Teklehaimanot A, 1996. Temporal and spatial distribution of anopheline mosquitoes in an Ethiopian village: implications for malaria control strategies. Bull World Health Organ 74 :299–305.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Gunawardena DM, Wickremasinghe AR, Muthuwatta L, 1998. Malaria risk factors in an endemic region of Sri Lanka, and the impact and cost implications of risk factor-based interventions. Am J Trop Med Hyg 58 :533–542.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Konradsen F, Amerasinghe P, van der Hoek W, Amerasinghe F, Perera D, Piyaratne M, 2003. Strong association between house characteristics and malaria vectors in Sri Lanka. Am J Trop Med Hyg 68 :177–181.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Lindsay SW, Jawara M, Paine K, Pinder M, Walraven GE, Emerson PM, 2003. Changes in house design reduce exposure to malaria mosquitoes. Trop Med Int Health 8 :512–517.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48

    Yé Y, Hoshen M, Louis V, Séraphin S, Traoré I, Sauerborn R, 2006. Housing conditions and Plasmodium falciparum infection: protective effect of iron-sheet roofed houses. Malar J 5 :8.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 2878 2705 919
Full Text Views 232 18 1
PDF Downloads 76 15 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save