• 1

    Yohannes M, Haile M, Ghebreyesus T, Witten K, Getachew A, Byass P, Lindsay SW, 2005. Can source reduction of mosquito larval habitat reduce malaria transmission in Tigray, Ethiopia? Trop Med Int Health 10 :1274–1285.

    • Search Google Scholar
    • Export Citation
  • 2

    Oomen J, de Wolf J, Jobin W, 1990. Health and Irrigation. Incorporation of Disease-Control Measures in Irrigation, a Multi-Faceted Task in Design, Construction, Operation. Wageningen, The Netherlands: International Institute for Land Reclamation and Improvement.

  • 3

    Lacey L, Lacey C, 1990. The medical importance of riceland mosquitoes and their control using alternatives to chemical insecticides. J Am Mosq Contr Assoc 6 :3–93.

    • Search Google Scholar
    • Export Citation
  • 4

    International Irrigation Management Institute, 1986. Proceedings of the Workshop on Irrigation and Vector-Borne Disease Transmission. Colombo, Sri Lanka: International Irrigation Management Institute.

  • 5

    Oomen J, de Wolf J, Jobin W, 1988. Health and Irrigation: Incorporation of Disease-Control Measures in Irrigation, a Multi-Faceted Task in Design, Construction, Operation. Wageningen, The Netherlands: International Institute for Land Reclamation and Improvement.

  • 6

    Robert V, Van den Broek A, Stevens P, Slootweg R, Petrarca V, Coluzzi M, Le Goff G, Di Deco MA, Carnevale P, 1992. Mosquitoes and malaria transmission in irrigated rice-fields in the Benoue valley of northern Cameroon. Acta Trop 52 :201–204.

    • Search Google Scholar
    • Export Citation
  • 7

    Coosemans M, 1985. Comparison of malarial endemicity in a rice-growing zone and in a cotton-growing zone in the Rusizi Plain, Burundi. Ann Soc Belg Med Trop 65 :187–200.

    • Search Google Scholar
    • Export Citation
  • 8

    Sissoko MS, Dicko A, Briet OJT, Sissoko MS, Sagara I, Keita H, Sogoba M, Rogier C, Toure Y, Doumbo O, 2004. Malaria incidence in relation to rice cultivation in the irrigated Sahel of Mali. Acta Trop 89 :161–170.

    • Search Google Scholar
    • Export Citation
  • 9

    Robert V, Gazin P, Boudin C, 1985. The transmission of malaria in a wooded savanna zone and a rice-growing zone in the vicinity of Bobo Dioulasso (Burkina Faso). Ann Soc Belg Med Trop 65 :201–214.

    • Search Google Scholar
    • Export Citation
  • 10

    Ijumba JN, 1997. The Impact of Rice and Sugarcane Irrigation on Malaria Transmission in the Lower Moshi Area of Northern Tanzania. Copenhagen, Denmark: Department of Population Biology, Zoological Institute of Denmark, University of Copenhagen.

  • 11

    Ijumba J, Mosha F, Lindsay S, 2002. Malaria transmission risk variations derived from different agricultural practices in an irrigated area of northern Tanzania. Med Vet Entomol 16 :28–38.

    • Search Google Scholar
    • Export Citation
  • 12

    Githeko A, Service MW, Mbogo CM, Atieli FK, Juma FO, 1993. Plasmodium falciparum sporozoite and entomological inoculation rates at the Ahero rice irrigation scheme and the Miwani sugar-belt in western Kenya. Ann Trop Med Parasitol 87 :379–391.

    • Search Google Scholar
    • Export Citation
  • 13

    Faye O, Fontenille D, Gaye O, 1995. Malaria and rice growing in the Senegal River delta (Senegal). Ann Soc Belg Med Trop 75 :179–189.

  • 14

    Mutero C, Kabutha C, Kimani V, Kabuage L, Gitau G, Ssennyonga J, Githure J, Muthami L, Kaida A, Musyoka L, Kiarie E, Oganda M, 2004. A transdisciplinary perspective on the links between malaria and agroecosystems in Kenya. Acta Trop 89 :171–186.

    • Search Google Scholar
    • Export Citation
  • 15

    Muturi J, Shililu J, Jacob B, Githure J, Gu W, Novak R, 2006. Mosquito species diversity and abundance in relation to land use in a riceland agroecosystem in Mwea, Kenya. J Vector Ecol 31 :129–137.

    • Search Google Scholar
    • Export Citation
  • 16

    Muturi E, Shililu J, Gu W, Jacob B, Githure J, Novak R, 2007. Larval habitat dynamics and diversity of Culex mosquitoes in rice agroecosystem in Mwea, Kenya. Am J Trop Med Hyg 76 :95–102.

    • Search Google Scholar
    • Export Citation
  • 17

    Ijumba J, Mwangi R, Beier JC, 1990. Malaria transmission potential of Anopheles mosquitoes in the Mwea-Tebere irrigation scheme, Kenya. Med Vet Entomol 4 :425–432.

    • Search Google Scholar
    • Export Citation
  • 18

    Mutero CM, Blank H, Konradsen F, Hoek W, 2000. Water management for controling the breeding of Anopheles mosquitoes in rice irrigation schemes in Kenya. ICIPE, Nairobi. Acta Trop 76 :253–256.

    • Search Google Scholar
    • Export Citation
  • 19

    Muturi EJ, Mwangangi JM, Shililu J, Muriu S, Jacob B, Kabiru EW, Gu W, Mbogo C, Githure J, Novak R, 2007. Mosquito species succession and the physicochemical factors affecting their abundance in rice fields in Mwea, Kenya. J Med Entomol 44 :336–344.

    • Search Google Scholar
    • Export Citation
  • 20

    World Health Organization, 1975. Manual on Practical Entomology in Malaria. Part II. Methods and Techniques. Geneva: World Health Organization.

  • 21

    Edwards F, 1941. Mosquitoes of the Ethiopian Region. III. Culicine Adults and Pupae. London: British Museum of Natural History.

  • 22

    Gillies MT, Coetzee M, 1987. A Supplement to the Anophelinae of Africa South of the Sahara (Afro-Tropical Region). Johannesberg, South Africa: Publication of the South African Institute of Medical Research 55 :1–143.

    • Search Google Scholar
    • Export Citation
  • 23

    Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, Koech DK, 1988. Blood meal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol 25 :9–16.

    • Search Google Scholar
    • Export Citation
  • 24

    Wirtz R, Zavala F, Graves P, Andre G, 1987. Field evaluation of ELISA for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol 24 :433–437.

    • Search Google Scholar
    • Export Citation
  • 25

    Charlwood JD, Smith T, Kihonda J, Heiz B, Billingsley PF, Takken W, 1995. Density independent feeding success of malaria vectors (Diptera: Culicidae) in Tanzania. Bull Entomol Res 85 :29–35.

    • Search Google Scholar
    • Export Citation
  • 26

    Beier JC, 2002. Vector incrimination and entomological inoculation rates. Methods Mol Med 72 :3–11.

  • 27

    Githeko A, Service M, Mbogo C, Atieli F, 1996. Resting behaviour, ecology and genetics of malaria vectors in large scale agricultural areas of Western Kenya. Parassitologia 38 :481–489.

    • Search Google Scholar
    • Export Citation
  • 28

    Briet J, Dossou-Yovo J, Akodo E, van de Giesen N, Teucher M, 2003. The relationship between Anopheles gambiae density and rice cultivation in the savannah and forest zone of Côte d’Ivoire. Trop Med Int Health 8 :439–448.

    • Search Google Scholar
    • Export Citation
  • 29

    Dolo G, Briet OJ, Dao A, Traore SF, Bouare M, Sogoba N, Niare O, Bagayogo M, Sangare D, Teuscher T, Toure YT, 2004. Malaria transmission in relation to rice cultivation in the irrigated Sahel of Mali. Acta Trop 89 :147–159.

    • Search Google Scholar
    • Export Citation
  • 30

    Marrama L, Rajaonarivelo E, Laventure S, Rabarison P, 1995. Anopheles funestus and rice culture on the Plateau of Madagascar. Cahiers Etudes Recherches Francophones Sante 5 :415–419.

    • Search Google Scholar
    • Export Citation
  • 31

    Ijumba J, Lindsay S, 2001. Impact of irrigation on malaria in Africa: paddies paradox. Med Vet Entomol 15 :1–11.

  • 32

    Robert V, Petrarca V, Coluzzi M, Boudin C, Carnevale P, Chippaux JP, Diomande L, 1991. Etude des taux de parturite et d’infection du complexe Anopheles gambiae dans la riziere de la Vallee du Kou, Burkina Faso. Robert V, Chippaux JP, Diomande L, eds. Le Paludisme en Afrique de l’Ouest: Etudes Entomologiques et Epidemiologiques en Zone Rizicole et en Milieu Urbain. Paris: Office de la Recherche Scientifique et Technique d’Outre-Mer, 17–35.

  • 33

    Marrama L, Jambou R, Rakotoarivony I, 2004. Malaria transmission in southern Madagascar: influence of the environment and hydro-agricultural works in sub-arid and humid regions. Part 1. Acta Trop 89 :193–203.

    • Search Google Scholar
    • Export Citation
  • 34

    Keiser J, Caldas de Castro M, Maltese MF, Bos R, Tanner M, Singer BH, Utzinger J, 2004. The effect of irrigation and large dams on the burden of malaria on global and regional scale. Am J Trop Med Hyg 72 :392–406.

    • Search Google Scholar
    • Export Citation
  • 35

    Garret-Jones C, Shidrawi GR, 1969. Malaria vectorial capacity of a population of Anopheles gambiae. Bull World Health Organ 40 :531–545.

    • Search Google Scholar
    • Export Citation
  • 36

    Diuk-Wasser MA, Toure MB, Dolo G, Bagayogo M, Sogoba N, Traore SF, Manoukis N, Taylor CE, 2005. Vector abundance and malaria transmission in rice-growing villages in Mali. Am J Trop Med Hyg 72 :725–731.

    • Search Google Scholar
    • Export Citation
  • 37

    Manoukis N, Toure MB, Sissoko I, Doumbia S, Traore SF, Diuk-Wasser MA, Taylor CE, 2006. Is vector body size the key to reduced malaria transmission in the irrigated region of Niono, Mali? J Med Entomol 43 :820–827.

    • Search Google Scholar
    • Export Citation
  • 38

    Kamau L, Koekemoer LL, Hunt RH, Coetzee M, 2003. Anopheles parensis: the main member of the Anopheles funestus (Diptera: Culicidae) species group found resting inside human dwellings in Mwea area of central Kenya. J Am Mosq Control Assoc 19 :130–133.

    • Search Google Scholar
    • Export Citation
  • 39

    Seyoum A, Balcha F, Balkew M, Ali A, Gebre-Michael T, 2002. Impact of cattle keeping on human biting rate of anopheline mosquitoes and malaria transmission around Ziway, Ethiopia. East Afr Med J 79 :485–490.

    • Search Google Scholar
    • Export Citation
  • 40

    Sota T, Mogi M, 1989. Effectiveness of zooprophylaxis in malaria control: a theoretical inquiry, with a model for mosquito populations with two bloodmeal hosts. Med Vet Entomol 3 :337–345.

    • Search Google Scholar
    • Export Citation
  • 41

    Bouma M, Rowland M, 1995. Failure of passive zooprophylaxis: cattle ownership in Pakistan is associated with a higher prevalence of malaria. Trans R Soc Trop Med Hyg 89 :351–353.

    • Search Google Scholar
    • Export Citation
  • 42

    Arunachalam N, Samuel P, Hiriyan J, Rajendran R, Dash A, 2005. Short report: observations on the multiple feeding behavior of Culex tritaeniorhynchus (Diptera: Culicidae), the vector of Japanese encephalitis in Kerala in Southern India. Am J Trop Med Hyg 72 :198–200.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Effect of Rice Cultivation on Malaria Transmission in Central Kenya

View More View Less
  • 1 Department of Medicine, William C. Gorgas Center for Geographic Medicine, University of Alabama at Birmingham, Birmingham, Alabama; Human Health Division, International Centre of Insect Physiology and Ecology, Nairobi, Kenya; Department of Zoology, Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya; Centre for Geographic Medicine Research-Coast, Kenya Medical Research Institute, Kilifi, Kenya

A 12-month field study was conducted between April 2004 and March 2005 to determine the association between irrigated rice cultivation and malaria transmission in Mwea, Kenya. Adult mosquitoes were collected indoors twice per month in three villages representing non-irrigated, planned, and unplanned rice agro-ecosystems and screened for blood meal sources and Plasmodium falciparum circumsporozoite proteins. Anopheles arabiensis Patton and An. funestus Giles comprised 98.0% and 1.9%, respectively, of the 39,609 female anophelines collected. Other species including An. pharoensis Theobald, An. maculipalpis Giles, An. pretoriensis Theobald, An. coustani Laveran, and An. rufipes Gough comprised the remaining 0.1%. The density of An. arabiensis was highest in the planned rice village and lowest in the non-irrigated village and that of An. funestus was significantly higher in the non-irrigated village than in irrigated ones. The human blood index (HBI) for An. arabiensis was significantly higher in the non-irrigated village compared with irrigated villages. For An. funestus, the HBI for each village differed significantly from the others, being highest in the non-irrigated village and lowest in the planned rice village. The sporozoite rate and annual entomologic inoculation rate (EIR) for An. arabiensis was 1.1% and 3.0 infective bites per person, respectively with no significant difference among villages. Sporozoite positive An. funestus were detected only in planned rice and non-irrigated villages. Overall, 3.0% of An. funestus samples tested positive for Plasmodium falciparum sporozoites. The annual EIR of 2.21 for this species in the non-irrigated village was significantly higher than 0.08 for the planned rice village. We conclude that at least in Mwea Kenya, irrigated rice cultivation may reduce the risk of malaria transmission by An. funestus but has no effect on malaria transmission by An. arabiensis. The zoophilic tendency of malaria vectors in irrigated areas accounts partly for low malaria transmission rates despite the presence of higher vector densities, highlighting the potential of zooprophylaxis in malaria control.

INTRODUCTION

Irrigated agriculture increases crop production by enabling the reclamation of arid and sub-arid lands, extending the crop-growing season, and reducing crop failure. For this reason many countries in sub-Saharan Africa have developed irrigation projects to provide food security, improved diet and increased income for a rapidly growing population.1 Unfortunately, water-related projects may aggravate the problem of mosquito-borne disease by increasing the number of larval habitats and extending the duration of transmission season.2 In particular, rice cultivation has received greater attention in Africa because it comprises one-third of all irrigated crops and requires flooded conditions that provide ideal habitats for at least 140 mosquito species worldwide.3

In general, irrigated areas support higher densities of malaria vectors than adjacent non-irrigated areas and the effect on malaria transmission and prevalence may vary depending on local ecologic conditions. In Sri Lanka, introduction of the Mahaweli Irrigation Scheme resulted in a five-fold increase in malaria incidence among the local population.4 Introduction and expansion of acreage under cotton, wheat, sorghum, and vegetable irrigation led to serious outbreaks of malaria in Gezira-Managil system in the Nile River valley.5 Development of dams for irrigation also increased malaria incidence in Benoue Valley, Cameroon,6 and Tigray, Ethiopia.1 In Rusizi Valley, Burundi vectorial capacity of Anopheles gambiae Giles s.l. was 150 times higher in the rice irrigation scheme than in adjacent cotton growing areas.7 In contrast, irrigated rice cultivation in Mali was associated with a reduction in the annual incidence of malaria8 and a 10-fold reduction in the sporozoite rate than was found in adjacent non-irrigated areas.9 In Lower Moshi Tanzania, malaria transmission and prevalence was significantly lower in irrigated than in neighboring sugarcane and cotton growing areas.10,11 Githeko and others12 reported that the sporozoite rate of An. gambiae s.l. was five times lower in the Ahero rice scheme than in the neighboring sugar cane growing area. The introduction of irrigated rice cultivation in the Senegal River delta did not alter malaria transmission.13 Collectively, these findings indicate that the relationship between irrigated rice cultivation and malaria transmission is complex and can only be understood through site-specific evaluation of local vectors and underlying ecologic and epidemiologic factors.

The Mwea Rice Irrigation Scheme is the largest of its kind in east Africa, covering an area of approximately 13,640 hectares. Recent studies have shown that the densities of An. arabiensis Patton are higher within the scheme than in the neighboring non-irrigated areas, and An. funestus Giles is more abundant in non-irrigated areas.14,15 Surprisingly, there has been no entomologic study to assess the impact of rice cultivation on malaria transmission in this area. Because malaria prevalence was shown to be lower within the scheme than in neighboring non-irrigated areas,14 it was our hypothesis that rice cultivation reduced the risk of malaria transmission in the area. We tested this hypothesis by comparing the risk of malaria transmission in three agro-ecosystems with different patterns of land use.

MATERIALS AND METHODS

Study sites.

The study was conducted in three villages (Mbuinjeru, Kiamachiri, and Murinduko) located in Mwea division, Kirinyaga District, 100 km northeast of Nairobi, Kenya. The study sites have been described in detail by Muturi and others.15,16 The study area has two annual rainfall seasons; the long rains in April–May and the short rains in October–November. Annual average rainfall is 950 mm. The average maximum temperature range is 16–26.5°C, and average relative humidity varies from 52% to 67%. Anopheles arabiensis is the dominant Anopheles species,15 the main vector of malaria,17 and the only sibling species of An. gambiae s.l. present within the Mwea Rice Scheme on the basis of cytotaxonomic17 and ribosomal DNA polymerase chain reaction studies.18,19 The prevalence of malaria in Mbuinjeru, Kiamachiri and Murinduko among children ≤ 9 years of age is 0%, 17%, and 54%, respectively.14

Mbuinjeru is within the Mwea Irrigation Scheme and more than 75% of the village land is under rice cultivation. Farmers in this village follow a defined rice cropping cycle as determined by the National Irrigation Board (planned rice cultivation). The typical rice cultivation cycle includes a land preparation–transplanting period (July–August), a growing period (August–November), and a post-harvest period (November–December). The second crop if planted is cultivated prior to the long rainy period between January and May. Human habitation occupies the remaining area with less than 10% used for vegetables and bananas.

Kiamachiri is immediately outside the scheme with approximately 20% of the area under rice cultivation. In this village, individual farmers decide their own cropping cycle depending on water availability. Consequently, rice is grown throughout the year as long as water is available in Gakungu River to irrigate the paddies (unplanned rice cultivation). The remaining 80% of the land is mainly planted with maize, beans, and bananas.

Murinduko is situated approximately 15 km from the scheme and is generally a non–rice-growing village mainly because of its hilly topography that renders much of the area (approximately 90%) unsuitable for rice cultivation. However, limited rice growing activity (< 5% of the total area) is conducted along one major river valley that runs along the edge of the village. Maize, beans, and bananas are the main crops cultivated but only on subsistence scale.

Demographic and meteorologic data.

A pre-study population census was done to provide basic human demographic data. This was accomplished by a house-to-house visit to determine the number of people residing in each village and family size. In addition, a census of domestic animals was also completed. This information was used to establish the human to cattle ratio. Before gathering the above information, the household head was briefed on the purpose of the study and his or her consent to provide the information requested.

The meteorologic data collected during the study period included rainfall, temperature, and relative humidity. Rain gauges (Tru-Chek®; Rain Gauge Division, Edwards Manufacturing Co. Albert Lea, MN) were placed in each of the three villages and rainfall was recorded daily throughout the study period from April 2004 to March 2005. Temperature and relative humidity for each of the village was obtained using temperature and relative humidity data loggers (Onset Computer Corporation, Bourne, MA).

Mosquito sampling and processing.

Adult mosquitoes were sampled twice per month between April 2004 and March 2005. The collections were done in 30 randomly selected houses between 7:00 AM and 11:00 AM using the pyrethrum spray catch (PSC) technique.20 In each study site, the location of each homestead was categorized as center or periphery and equal numbers of houses were selected from each category. Any homestead less than 15 meters from the village perimeter was classified as being at the periphery of the village. Mosquitoes were transported from the field to the laboratory where they were identified to species by morphologic characteristics.21,22 Each mosquito was scored as unfed, blood-fed, semi-gravid or gravid by visual abdominal examination under a dissecting microscope. The guts of a representative sample of blood fed anophelines collected at each village were analyzed using an enzyme-linked immunosorbent assay (ELISA)23 to identify the relative proportion of adult mosquito population feeding on humans and cattle. The heads and thoraces of another sample comprising all classes of mosquitoes (unfed, blood-fed, semi-gravid and gravid) was analyzed by ELISA for Plasmodium falciparum circumsporozoite proteins.24

Entomologic indices.

The human blood index (HBI) was determined as the proportion of blood-fed mosquitoes that had fed on humans of the total number tested. The feeding success was determined as the proportion of blood fed and semi-gravid mosquitoes in the total proportion presumed to have attempted to feed (all mosquitoes except gravids).25 The sporozoite index for a given species was calculated as the proportion of females carrying infective sporozoites in the head-thorax of the total number tested. The human biting rate was derived as the product of blood fed and semi-gravid females per person per night and the human blood index. The product of human biting rate and sporozoite index yielded the entomologic inoculation rate (EIR), a standard measure of transmission intensity.26 Githeko and others27 did not find any evidence of early exophily by rice land An. arabiensis and An. funestus. We therefore considered mosquito samples from PSC to be relatively good estimates of human biting rates and EIR.

Data analysis.

Data were analyzed using the SPSS version 11.5 statistical package (SPSS, Inc., Chicago, IL). Mosquito densities and biting rates were log-transformed before analysis to normalize the data. Analysis of variance was used to compare the differences in mosquito densities, human biting rates, and EIR among villages and the means were separated by Tukey test. The chi-square test was used to compare differences in feeding success and sporozoite rates of mosquito species among villages.

RESULTS

Demographic data.

The ratio of humans to cattle in both planned (Mbuinjeru) and unplanned (Kiamachiri) rice agro-ecosystems was 5:1 compared with a 12:1 in the non-irrigated village (Murinduko). The total precipitation for the period April 2004 to March 2005 was 810.4 mm, 679.8 mm, and 803.1 mm, for the planned, unplanned and non-irrigated agro-ecosystems, respectively. The rainfall pattern was bimodal with peaks in April and November. The average daily temperature for this period was 22.9°C and the average relative humidity was 71.0%.

Species composition and abundance.

A total of 39,609 female anophelines were collected between April 2004 and March 2005. Anopheles arabiensis was the dominant species comprising 98.0% of the total collection, followed by An. funestus at 1.9%. The remaining 0.1% was composed of An. pharoensis Theobald, An. maculipalpis Giles, An. pretoriensis Theobald, An. coustani Laveran, and An. rufipes Gough. The mosquito species diversity and abundance for the three study sites has been described in detail elsewhere.15

Vector density, feeding success, human blood index, and human biting rates.

The overall indices of malaria transmission at the three study sites are shown in Table 1. The mean ± SE number of An. arabiensis per person per night was 10.76 ± 0.60 in the planned rice agro-ecosystem (Mbuinjeru), which was two-fold higher than in the unplanned rice agro-ecosystem (Kiamachiri; 5.36 ± 0.45) and 12-fold higher than in the non-irrigated agro-ecosystem (Murinduko; 0.91 ± 0.09). Tukey’s honestly significant differences test showed that each agro-ecosystem differed significantly from the others (F = 85.33, degrees of freedom [df] = 2, 71, P < 0.001). The mean ± SE number of An. funestus per person per night in the planned and unplanned rice agro-ecosystems was 0.04 ± 0.00 and differed significantly from the value of 0.27 ± 0.01 for the non-irrigated agro-ecosystem (F = 5.054, df = 2, 71, P < 0.01). The average feeding success for An. arabiensis and An. funestus was 0.63 and 0.62, respectively, with no significant difference among agro-ecosystems. The human blood index of An. arabiensis was significantly higher in the non-irrigated agro-ecosystem (0.50) than in the planned (0.09) and unplanned (0.12) rice agro-ecosystems (χ2 = 158.361, df = 2, P < 0.001). For An. funestus, the human blood index was 0.72 in the non-irrigated site, 0.27 in the unplanned rice site, and 0.11 in the planned rice site. This difference was significant (χ2 = 26.438, df = 2, P < 0.001). In the non-irrigated agro-ecosystem, An. funestus was more anthropophilic than An. arabiensis2 = 8.555, df = 1 P < 0.01) but the difference was not significant for the other sites. The blood meals for An. coustani (n = 14), An. maculipalpis (n = 2), and An. rufipes (n = 2) were of bovine origin, but An. pharoensis (n = 7) and An. pretoriensis (n = 1) were not tested for blood meal sources because all the adults collected were unfed. The mean ± SE human biting rate per person per night for An. arabiensis in the non-irrigated site was 0.46 ± 0.02 and was significantly lower than the values of 0.97 ± 0.12 in the planned rice site and 0.64 ± 0.05 in the unplanned rice site (F = 39,421, df = 2, 71, P < 0.01). Similar values for An. funestus were 0.004 ± 0.00 and 0.011 ± 0.00 in the planned and unplanned rice sites, respectively, and these values were significantly lower than the value of 0.20 ± 0.01 SE in the non-irrigated site (F = 10.036, df = 2, 71, P < 0.01).

Sporozoite rate and EIR.

The overall sporozoite rates and EIR values are shown in Table 1. Sporozoite-positive An. arabiensis samples were detected in all the three agro-ecosystems (range = 0.72–1.73) and the observed difference was not statistically significant (χ2 = 2.624, df = 2, P > 0.05). In the planned rice and non-irrigated sites, sporozoite-positive An. arabiensis was observed in December and March whereas in the unplanned rice site, they were detected in October and December. Sporozoite-positive An. funestus were only detected in planned rice (in December) and non-irrigated sites (in January and February) (Table 2). The calculated difference between the two sites was not statistically significant (χ2 = 1.014, df = 1, P > 0.05). None of the other species (An. pharoensis, An. coustani, An. maculipalpis, An. pretoriensis, and An. rufipes) were positive for P. falciparum circumsporozoite proteins.

The annual EIR for An. arabiensis ranged between 2.5 and 4.1 infective bites per person with no statistically significant difference among sites (F = 0.401, df = 2, 33, P > 0.05). Conversely, the annual EIR for An. funestus in the non-irrigated site was 26-fold higher than the corresponding value in the planned rice site (F = 8.082, df = 2, 33, P < 0.01). None of the 92 individuals of this species collected in the unplanned rice site was positive for P. falciparum circumsporozoite proteins (Table 1). The monthly distribution of EIR for both species was similar to the sporozoite index (Table 2).

DISCUSSION

Based on results of adult mosquito densities and human biting rates, An. arabiensis was strongly associated with rice cultivation and An. funestus was common in the non-irrigated agro-ecosystem. Even among irrigated rice agro-ecosystems, significantly higher densities of An. arabiensis were collected in the planned rice agro-ecosystem than in the unplanned rice agro-ecosystem. This was expected because the area under rice cultivation in planned rice agro-ecosystem was four-fold higher than in the unplanned rice agro-ecosystem. Many studies across the African continent have reported higher densities of An. gambiae s.l. in rice-cultivating areas than in neighboring non-irrigated areas.11,14,15,28,29 In contrast, except for the Ahero rice scheme, Kenya,12 and rice-growing areas of Madagascar,30 An. funestus is a rare species in irrigated rice agro-ecosystems of Africa. The reason for this is still unknown but could be the result of loss of larval habitats after transformation of natural habitats into rice fields.

It was apparent that in rice irrigated villages, only a small proportion of mosquitoes that entered the house actually fed on humans. Anthropophily for both species was lowest in the planned rice village, moderate in the unplanned rice village, and highest in the non-irrigated village. These findings suggest that the extent of rice cultivation has a significant impact on the blood-feeding behavior of malaria vectors. These findings are consistent with those of previous reports that rice cultivation decreases the degree of human-vector contact by diverting mosquitoes to other hosts.11,12,14 It has been suggested that rice cultivation empowers the surrounding communities economically, enabling them to protect themselves against mosquito bites.31 However, a recent study showed that the three villages had similar levels of poverty and social problems and that income could not explain the observed differences in the degree of anthropophily.14 Nonetheless, because of the greater number of mosquitoes entering the house in irrigated areas, the resulting nuisance was intolerable and many people recognized the need to sleep under bed nets compared with the low-density non-irrigated areas.14 High bed net use and large numbers of cattle in irrigated areas are likely to cause a shift from human to cattle feeding by mosquitoes. These findings are consistent with the previous idea that zooprophylaxis may be a potential malaria control strategy in the area.14 It has also been suggested that anthropophily in An. gambiae s.s. increases with age29 but in contrast, there are reports that cattle feeding increases the parity rate for this species.32 Neither of the two opposing factors was evaluated for An. arabiensis in the present study. Further studies are necessary to assess how various components of disease transmission influence the blood-feeding behavior of malaria vectors in similar areas.

There was no significant difference in the risk of malaria transmission by An. arabiensis among the three villages despite the greater variation in mosquito densities and biting rates. These results indicate that rice cultivation in Mwea has no effect on malaria transmission by this species. Many studies in rice irrigated areas of Africa have shown that malaria transmission can be higher,7,33 similar,9 or less11,12 than in neighboring non-irrigated areas. Because different areas may differ in many aspects even before introduction of water development projects, whether an irrigation project will alter malaria transmission dynamics depends on the local epidemiologic context, particularly the entomologic parameters.28,34 Our results suggest that the HBI and low vector density were among the factors partly accounting for the lack of a significant difference in the indices of malaria transmission among the three villages. The low HBI had a significant influence in irrigated villages whereas the low vector densities were a limiting factor in the non-irrigated village. Other factors that could have accounted for this observation but were not evaluated in this study include differences in daily survivorship and vectorial capacity.31,35 A recent study by Diuk-Wasser and others36 demonstrated a positive relationship between adult survival and vectorial capacity at low mosquito densities and a negative relationship between the two variables at higher mosquito densities. Further studies in the same region showed that adult survivorship was significantly higher in the non-irrigated than in irrigated areas.37 It is therefore likely that most mosquitoes that emerged from the high-density irrigated areas were short-lived and less efficient at transmitting malaria compared with those in the non-irrigated area.

In contrast with An. arabiensis, the risk of malaria transmission by An. funestus was significantly higher in the non-irrigated village than in the irrigated villages. This indicates that rice cultivation in the study area reduces the risk of malaria transmission by An. funestus. In a study to evaluate the impact of rice cultivation on malaria prevalence in the three study sites, the prevalence of malaria parasites among children ≤ 9 years of age was 0% (n = 21), 17% (n = 53), and 54% (n = 63), in Mbuinjeru, Kiamachiri, and Murinduko, respectively.14 In our study, infective mosquitoes were observed in all three study sites, an indication that both An. arabiensis and An. funestus play a significant role in malaria transmission in the area. Mutero and others14 collected their blood samples between December 2001 and February 2002, which were approximately the same months we observed detectable levels of transmission. Our findings indicate that despite its low density relative to An. arabiensis, An. funestus does play a significant role in malaria transmission, especially in the non-irrigated areas, because of its high degree of an-thropophily, making it worthy of attention to malaria control programs in this area. We did not determine which of the nine known members of the An. funestus22 complex were present in the study area. However, based on our HBI results and the findings of previous studies in the same area,38 it is likely that An. parensis was the dominant species of An. funestus s.l. within the rice scheme as opposed to An. funestus s.s. in the non-irrigated village.

The low anthopophily of An. arabiensis, especially in irrigated areas, may account for the low rates of malaria transmission within the rice scheme despite its higher densities. This information warrants the need to explore the possibility of using zooprophylaxis as a malaria control tactic for similar areas. Zooprophylaxis controls vector-borne diseases by attracting vectors to domestic animals that can act as dead-end hosts.39 This technique can be an effective strategy for controlling malaria.40 However, domestic animals may also increase mosquito density, thereby enhancing rather than reducing malaria transmission.41 In other diseases such as Rift valley fever and Japanese encephalitis, introduction of animals may facilitate amplification and transmission of infection.42 These findings highlight the need to understand the role of domestic animals in disease transmission in similar areas before adopting zooprophylaxis as a mosquito-borne disease control strategy.

In conclusion, An. arabiensis and An. funestus were the two prominent vectors of malaria in the study sites. Our study suggests that in Mwea, there is no difference in malaria transmission by An. arabiensis between irrigated and non-irrigated areas but in contrast, there is less malaria transmission by An. funestus in irrigated than in non-irrigated areas. Among the reasons accounting for this observation was increased zoophily of mosquitoes in irrigated areas and low vector densities in the non-irrigated area. Our findings support the idea that well-studied zooprophylaxis could be an efficient tactic to aid in management of malaria and other mosquito-borne diseases in similar areas.

Table 1

Entomologic indices of Anopheles arabiensis and An. funestus in non-irrigated and planned and unplanned rice agro-ecosystems in Mwea, Kenya*

SpeciesTransmission indicesMbuinjeru (planned)Kiamachiri (unplanned)Murinduko (non-irrigated)
* EIR = entomologic inoculation rate. Values with different superscript letters within a column are significantly different at P < 0.05.
† Indicates indices of malaria transmission in which significant differences were observed.
An. arabiensisTotal collected26,39910,9831,446
Mean no./person/night†10.76a5.36b0.91c
Feeding success0.630.600.66
Human blood index†0.09a (n= 812)0.12a (n = 334)0.50b (n = 131)
Bovine blood index0.780.750.44
Human biting rate/night†0.97a0.64a0.46b
Sporozoite rates (%)0.72 (n = 832)1.73 (n = 347)1.5 (n = 133)
Annual EIR2.554.062.50
An. funestusTotal collected8792560
Mean no./person/night†0.04a0.04a0.27b
Feeding success0.600.590.68
Human blood index†0.11a (n = 19)0.27b (n = 11)0.72c (n = 65)
Bovine blood index0.740.640.09
Sporozoite rates (%)5.260.003.08
Human biting rate/night†0.004a0.011a0.197b
Annual EIR†0.08a0.002.21b
Table 2

Monthly entomologic parameters of Anopheles arabiensis and An. funestus in non-irrigated and planned and unplanned rice agro-ecosystems in Mwea, Kenya*

An. arabiensisAn. funestus
SiteMonth and yearDensityHBRSPEIRDensityHBRSPEIR
* Density = mosquitoes per person per night; HBR = human biting rate; SP = sporozoite index; EIR = entomologic inoculation rate; Mbuinjeru = planned rice; Kiamachiri = unplanned rice; Murinduko = non-irrigated.
MbuinjeruApr 20044.690.110.000.000.000.000.000.00
May 20044.330.200.000.000.250.030.000.00
Jun 20042.870.080.000.000.250.030.000.00
Jul 20043.510.120.000.000.380.040.000.00
Aug 20047.990.750.000.000.670.070.000.00
Sep 200426.101.450.000.000.750.080.000.00
Oct 200412.661.520.000.000.000.000.000.00
Nov 200414.251.240.000.000.500.050.000.00
Dec 20049.120.950.060.060.670.070.140.01
Jan 200524.386.040.000.000.670.070.000.00
Feb 20059.823.930.000.000.000.000.000.00
Mar 20055.790.460.010.010.130.010.000.00
KiamachiriApr 20047.042.010.000.000.360.100.000.00
May 20042.700.120.000.000.780.210.000.00
Jun 20041.670.310.000.000.530.150.000.00
Jul 20045.050.000.000.000.470.130.000.00
Aug 20044.111.030.000.000.210.060.000.00
Sep 20042.380.320.000.000.330.090.000.00
Oct 20043.920.290.100.031.000.270.000.00
Nov 200411.131.010.000.000.440.120.000.00
Dec 20045.280.180.070.010.790.220.000.00
Jan 20058.140.630.000.000.260.070.000.00
Feb 20057.970.660.000.001.000.270.000.00
Mar 20053.410.130.000.000.000.000.000.00
MurindukoApr 20040.430.030.000.000.220.000.000.00
May 20040.420.080.000.001.611.610.000.00
Jun 20040.350.140.000.000.980.750.000.00
Jul 20040.910.000.000.000.430.000.000.00
Aug 20040.350.280.000.000.230.000.000.00
Sep 20041.810.880.000.000.320.000.000.00
Oct 20040.490.000.000.000.450.000.000.00
Nov 20040.330.210.000.000.880.380.000.00
Dec 20041.481.480.080.110.630.630.000.00
Jan 20051.341.070.000.001.060.880.080.07
Feb 20050.800.640.000.000.520.170.330.06
Mar 20051.230.450.040.020.480.000.000.00

*

Address correspondence to Ephantus J. Muturi, Department of Medicine, William C. Gorgas Center for Geographic Medicine, University of Alabama at Birmingham, 206C Bevill Biomedical Research Building, 845 19th Street South, Birmingham AL 35294. E-mail: emuturi@uab.edu

Authors’ addresses: Ephantus J. Muturi, Benjamin G. Jacob, and Robert J. Novak, Department of Medicine, William C. Gorgas Center for Geographic Medicine, University of Alabama at Birmingham, 206C Bevill Biomedical Research Building, 845 19th Street South, Birmingham AL 35294. Simon Muriu, Josephat Shililu, and John Githure, Human Health Division, International Centre of Insect Physiology and Ecology, PO Box 30772, Nairobi, Kenya. Joseph Mwangangi and Charles Mbogo, Center for Geographic Medicine Research-Coast, Kenya Medical Research Institute, PO Box 428, Kilifi, Kenya.

Acknowledgments: We are grateful to Professor Christian Borgemeister (Director General, International Centre of Insect Physiology and Ecology) for his strong support of this project. We acknowledge the technical support provided by James Wauna, Peter Barasa, Enock Mpanga, Peter M. Mutiga, William Waweru, Nelson Maingi, Martin Njigoya, Paul K. Mwangi, Christine W. Maina, Gladys Karimi, Irene Kamau, Nicholus Gachoki, and Naftaly Gichuki. We also thank Raphael Wanjogu (National Irrigation Board) for providing us with laboratory space to conduct the study.

Financial support: This study was supported by National Institutes of Health/National Institute of Allergy and Infectious Diseases grant no. U01A1054889 to Robert Novak.

REFERENCES

  • 1

    Yohannes M, Haile M, Ghebreyesus T, Witten K, Getachew A, Byass P, Lindsay SW, 2005. Can source reduction of mosquito larval habitat reduce malaria transmission in Tigray, Ethiopia? Trop Med Int Health 10 :1274–1285.

    • Search Google Scholar
    • Export Citation
  • 2

    Oomen J, de Wolf J, Jobin W, 1990. Health and Irrigation. Incorporation of Disease-Control Measures in Irrigation, a Multi-Faceted Task in Design, Construction, Operation. Wageningen, The Netherlands: International Institute for Land Reclamation and Improvement.

  • 3

    Lacey L, Lacey C, 1990. The medical importance of riceland mosquitoes and their control using alternatives to chemical insecticides. J Am Mosq Contr Assoc 6 :3–93.

    • Search Google Scholar
    • Export Citation
  • 4

    International Irrigation Management Institute, 1986. Proceedings of the Workshop on Irrigation and Vector-Borne Disease Transmission. Colombo, Sri Lanka: International Irrigation Management Institute.

  • 5

    Oomen J, de Wolf J, Jobin W, 1988. Health and Irrigation: Incorporation of Disease-Control Measures in Irrigation, a Multi-Faceted Task in Design, Construction, Operation. Wageningen, The Netherlands: International Institute for Land Reclamation and Improvement.

  • 6

    Robert V, Van den Broek A, Stevens P, Slootweg R, Petrarca V, Coluzzi M, Le Goff G, Di Deco MA, Carnevale P, 1992. Mosquitoes and malaria transmission in irrigated rice-fields in the Benoue valley of northern Cameroon. Acta Trop 52 :201–204.

    • Search Google Scholar
    • Export Citation
  • 7

    Coosemans M, 1985. Comparison of malarial endemicity in a rice-growing zone and in a cotton-growing zone in the Rusizi Plain, Burundi. Ann Soc Belg Med Trop 65 :187–200.

    • Search Google Scholar
    • Export Citation
  • 8

    Sissoko MS, Dicko A, Briet OJT, Sissoko MS, Sagara I, Keita H, Sogoba M, Rogier C, Toure Y, Doumbo O, 2004. Malaria incidence in relation to rice cultivation in the irrigated Sahel of Mali. Acta Trop 89 :161–170.

    • Search Google Scholar
    • Export Citation
  • 9

    Robert V, Gazin P, Boudin C, 1985. The transmission of malaria in a wooded savanna zone and a rice-growing zone in the vicinity of Bobo Dioulasso (Burkina Faso). Ann Soc Belg Med Trop 65 :201–214.

    • Search Google Scholar
    • Export Citation
  • 10

    Ijumba JN, 1997. The Impact of Rice and Sugarcane Irrigation on Malaria Transmission in the Lower Moshi Area of Northern Tanzania. Copenhagen, Denmark: Department of Population Biology, Zoological Institute of Denmark, University of Copenhagen.

  • 11

    Ijumba J, Mosha F, Lindsay S, 2002. Malaria transmission risk variations derived from different agricultural practices in an irrigated area of northern Tanzania. Med Vet Entomol 16 :28–38.

    • Search Google Scholar
    • Export Citation
  • 12

    Githeko A, Service MW, Mbogo CM, Atieli FK, Juma FO, 1993. Plasmodium falciparum sporozoite and entomological inoculation rates at the Ahero rice irrigation scheme and the Miwani sugar-belt in western Kenya. Ann Trop Med Parasitol 87 :379–391.

    • Search Google Scholar
    • Export Citation
  • 13

    Faye O, Fontenille D, Gaye O, 1995. Malaria and rice growing in the Senegal River delta (Senegal). Ann Soc Belg Med Trop 75 :179–189.

  • 14

    Mutero C, Kabutha C, Kimani V, Kabuage L, Gitau G, Ssennyonga J, Githure J, Muthami L, Kaida A, Musyoka L, Kiarie E, Oganda M, 2004. A transdisciplinary perspective on the links between malaria and agroecosystems in Kenya. Acta Trop 89 :171–186.

    • Search Google Scholar
    • Export Citation
  • 15

    Muturi J, Shililu J, Jacob B, Githure J, Gu W, Novak R, 2006. Mosquito species diversity and abundance in relation to land use in a riceland agroecosystem in Mwea, Kenya. J Vector Ecol 31 :129–137.

    • Search Google Scholar
    • Export Citation
  • 16

    Muturi E, Shililu J, Gu W, Jacob B, Githure J, Novak R, 2007. Larval habitat dynamics and diversity of Culex mosquitoes in rice agroecosystem in Mwea, Kenya. Am J Trop Med Hyg 76 :95–102.

    • Search Google Scholar
    • Export Citation
  • 17

    Ijumba J, Mwangi R, Beier JC, 1990. Malaria transmission potential of Anopheles mosquitoes in the Mwea-Tebere irrigation scheme, Kenya. Med Vet Entomol 4 :425–432.

    • Search Google Scholar
    • Export Citation
  • 18

    Mutero CM, Blank H, Konradsen F, Hoek W, 2000. Water management for controling the breeding of Anopheles mosquitoes in rice irrigation schemes in Kenya. ICIPE, Nairobi. Acta Trop 76 :253–256.

    • Search Google Scholar
    • Export Citation
  • 19

    Muturi EJ, Mwangangi JM, Shililu J, Muriu S, Jacob B, Kabiru EW, Gu W, Mbogo C, Githure J, Novak R, 2007. Mosquito species succession and the physicochemical factors affecting their abundance in rice fields in Mwea, Kenya. J Med Entomol 44 :336–344.

    • Search Google Scholar
    • Export Citation
  • 20

    World Health Organization, 1975. Manual on Practical Entomology in Malaria. Part II. Methods and Techniques. Geneva: World Health Organization.

  • 21

    Edwards F, 1941. Mosquitoes of the Ethiopian Region. III. Culicine Adults and Pupae. London: British Museum of Natural History.

  • 22

    Gillies MT, Coetzee M, 1987. A Supplement to the Anophelinae of Africa South of the Sahara (Afro-Tropical Region). Johannesberg, South Africa: Publication of the South African Institute of Medical Research 55 :1–143.

    • Search Google Scholar
    • Export Citation
  • 23

    Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, Koech DK, 1988. Blood meal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol 25 :9–16.

    • Search Google Scholar
    • Export Citation
  • 24

    Wirtz R, Zavala F, Graves P, Andre G, 1987. Field evaluation of ELISA for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol 24 :433–437.

    • Search Google Scholar
    • Export Citation
  • 25

    Charlwood JD, Smith T, Kihonda J, Heiz B, Billingsley PF, Takken W, 1995. Density independent feeding success of malaria vectors (Diptera: Culicidae) in Tanzania. Bull Entomol Res 85 :29–35.

    • Search Google Scholar
    • Export Citation
  • 26

    Beier JC, 2002. Vector incrimination and entomological inoculation rates. Methods Mol Med 72 :3–11.

  • 27

    Githeko A, Service M, Mbogo C, Atieli F, 1996. Resting behaviour, ecology and genetics of malaria vectors in large scale agricultural areas of Western Kenya. Parassitologia 38 :481–489.

    • Search Google Scholar
    • Export Citation
  • 28

    Briet J, Dossou-Yovo J, Akodo E, van de Giesen N, Teucher M, 2003. The relationship between Anopheles gambiae density and rice cultivation in the savannah and forest zone of Côte d’Ivoire. Trop Med Int Health 8 :439–448.

    • Search Google Scholar
    • Export Citation
  • 29

    Dolo G, Briet OJ, Dao A, Traore SF, Bouare M, Sogoba N, Niare O, Bagayogo M, Sangare D, Teuscher T, Toure YT, 2004. Malaria transmission in relation to rice cultivation in the irrigated Sahel of Mali. Acta Trop 89 :147–159.

    • Search Google Scholar
    • Export Citation
  • 30

    Marrama L, Rajaonarivelo E, Laventure S, Rabarison P, 1995. Anopheles funestus and rice culture on the Plateau of Madagascar. Cahiers Etudes Recherches Francophones Sante 5 :415–419.

    • Search Google Scholar
    • Export Citation
  • 31

    Ijumba J, Lindsay S, 2001. Impact of irrigation on malaria in Africa: paddies paradox. Med Vet Entomol 15 :1–11.

  • 32

    Robert V, Petrarca V, Coluzzi M, Boudin C, Carnevale P, Chippaux JP, Diomande L, 1991. Etude des taux de parturite et d’infection du complexe Anopheles gambiae dans la riziere de la Vallee du Kou, Burkina Faso. Robert V, Chippaux JP, Diomande L, eds. Le Paludisme en Afrique de l’Ouest: Etudes Entomologiques et Epidemiologiques en Zone Rizicole et en Milieu Urbain. Paris: Office de la Recherche Scientifique et Technique d’Outre-Mer, 17–35.

  • 33

    Marrama L, Jambou R, Rakotoarivony I, 2004. Malaria transmission in southern Madagascar: influence of the environment and hydro-agricultural works in sub-arid and humid regions. Part 1. Acta Trop 89 :193–203.

    • Search Google Scholar
    • Export Citation
  • 34

    Keiser J, Caldas de Castro M, Maltese MF, Bos R, Tanner M, Singer BH, Utzinger J, 2004. The effect of irrigation and large dams on the burden of malaria on global and regional scale. Am J Trop Med Hyg 72 :392–406.

    • Search Google Scholar
    • Export Citation
  • 35

    Garret-Jones C, Shidrawi GR, 1969. Malaria vectorial capacity of a population of Anopheles gambiae. Bull World Health Organ 40 :531–545.

    • Search Google Scholar
    • Export Citation
  • 36

    Diuk-Wasser MA, Toure MB, Dolo G, Bagayogo M, Sogoba N, Traore SF, Manoukis N, Taylor CE, 2005. Vector abundance and malaria transmission in rice-growing villages in Mali. Am J Trop Med Hyg 72 :725–731.

    • Search Google Scholar
    • Export Citation
  • 37

    Manoukis N, Toure MB, Sissoko I, Doumbia S, Traore SF, Diuk-Wasser MA, Taylor CE, 2006. Is vector body size the key to reduced malaria transmission in the irrigated region of Niono, Mali? J Med Entomol 43 :820–827.

    • Search Google Scholar
    • Export Citation
  • 38

    Kamau L, Koekemoer LL, Hunt RH, Coetzee M, 2003. Anopheles parensis: the main member of the Anopheles funestus (Diptera: Culicidae) species group found resting inside human dwellings in Mwea area of central Kenya. J Am Mosq Control Assoc 19 :130–133.

    • Search Google Scholar
    • Export Citation
  • 39

    Seyoum A, Balcha F, Balkew M, Ali A, Gebre-Michael T, 2002. Impact of cattle keeping on human biting rate of anopheline mosquitoes and malaria transmission around Ziway, Ethiopia. East Afr Med J 79 :485–490.

    • Search Google Scholar
    • Export Citation
  • 40

    Sota T, Mogi M, 1989. Effectiveness of zooprophylaxis in malaria control: a theoretical inquiry, with a model for mosquito populations with two bloodmeal hosts. Med Vet Entomol 3 :337–345.

    • Search Google Scholar
    • Export Citation
  • 41

    Bouma M, Rowland M, 1995. Failure of passive zooprophylaxis: cattle ownership in Pakistan is associated with a higher prevalence of malaria. Trans R Soc Trop Med Hyg 89 :351–353.

    • Search Google Scholar
    • Export Citation
  • 42

    Arunachalam N, Samuel P, Hiriyan J, Rajendran R, Dash A, 2005. Short report: observations on the multiple feeding behavior of Culex tritaeniorhynchus (Diptera: Culicidae), the vector of Japanese encephalitis in Kerala in Southern India. Am J Trop Med Hyg 72 :198–200.

    • Search Google Scholar
    • Export Citation
Save