Temporal Dynamics of Malaria Transmission in Two Rural Areas of Burkina Faso With Two Ecological Differences

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1 VECTOR/PATHOGEN/HOST INTERACTION, TRANSMISSION Temporal Dynamics of Malaria Transmission in Two Rural Areas of Burkina Faso With Two Ecological Differences ILBOUDO-SANOGO EDITH, 1 TIONO B. ALFRED, 1 SAGNON N FALÉ, 1 CUZIN OUATTARA NADINE, 1 NÉBIÉ ISSA, 1 AND SIRIMA SODIOMON B. 1,2 Centre National de Recherche et de Formation sur le Paludisme, 01 BP 2208 Ouagadougou 01, Burkina Faso J. Med. Entomol. 47(4): 618Ð624 (2010); DOI: /ME09102 ABSTRACT To determine the relationship between malaria transmission intensity, clinical malaria, immune response, plasmodic index, and to furthermore characterize a malaria vaccine trial site for potential malaria vaccines candidate testing, a study was conducted in Tensobtenga and Balonguen, two villages in Burkina Faso characterized by different malaria transmission levels. The study villages are located in a Sudan savanna area. Malaria transmission is seasonal and peaks in September in these villages. Tensobtenga and Balonguen are comparables in all aspects, except the presence of an artiþcial lake and wetlands in Tensobtenga. The mosquitoes sampling sites were randomly selected, taking into consideration the number of potential breeding sites, and the number of households in each village. Three times a week during 12 mo mosquitoes were collected by the Center for Disease Control and Prevention light traps in sentinel sites. To assess the infectivity the mosquitoes double ELISAs tests were performed on thoraces of female Anopheles gambiae s.l. (Giles) and Anopheles funestus. A total of 54,392 female Anopheles, representing 92.71% of the total mosquitoes, were collected. The peaks of aggressiveness because of either An. gambiae s.l. or An. funestus were observed in September in each of the villages. However, these peaks were lower in Balonguen compared with Tensobtenga. Malaria cumulative aggressiveness and transmission intensity because of both species peaked in September in each of the two villages, with lower values in Balonguen in comparison to Tensobtenga. From February to May, malaria transmission intensity is negligible in Balonguen and 1 bite/ person/mo is observed in Tensobtenga. These results have conþrmed the marked seasonality of malaria transmission in the study area. KEY WORDS rate malaria vectors, Anopheles gambiae s.l., Anopheles funestus entomological inoculation Malaria is a parasitic disease caused by protozoa of the genus Plasmodium; the most severe and life threatening form of malaria is associated with infection by Plasmodium falciparum (Welch 1897). In Burkina Faso, malaria transmission is seasonal, the main malaria vector is Anopheles gambiae s.l. (Giles). However, An. funestus also transmits the disease to a lesser extent. P. falciparum is the main malaria parasite transmitted by vectors. It is in cause for 95% of the malaria cases; the remaining 5% are because of P. Malariae, P. ovale, and mixed infections of P. falciparum and malariae. P. falciparum malaria accounts for over 33% of outpatients visits and hospital admissions in Burkina Faso. Pregnant women and children aged less than 5 yr are the most vulnerable segment of the population. It was estimated that malaria is the cause of 27Ð42% of deaths 1 Corresponding author, eisanogo@yahoo.fr. 2 Groupe de Recherche Action en Santé (GRAS), 06 BP Ouagadougou 06, Burkina Faso. with at least 50% occurring in children aged 5 yr (S. B. Sirima et al., unpublished data). Malaria control is based on three main strategies: early diagnosis and appropriate treatment of clinical cases, chemoprophylaxis for pregnant women and other vulnerable persons, and the use of insecticidetreated materials to reduce the contact between human and vectors. These strategies are most effective when adapted to local conditions. Malaria transmission intensity could vary within the same village depending on the environmental conditions (micro-climate). To assess the relationship between malaria transmission intensity and clinical malaria, immune response and plasmodic index, a study was conducted at the Centre National de Recherche et de Formation sur le Paludisme (CNRFP) in two villages characterized by different malaria transmission levels in Burkina Faso. Malaria transmission dynamics was assessed within this context to also further characterize the site foreseen as a probable malaria vaccine candidate trials site /10/0618Ð0624$04.00/ Entomological Society of America

2 July 2010 EDITH ET AL.: MALARIA TRANSMISSION IN RURAL BURKINA FASO 619 Fig. 1. Map of the village of Tensobtenga. Flags indicate mosquitoes breeding sites and the black place the artiþcial lake and wetlands. Materials and Methods Study Villages. The study was conducted in the villages of Tensobtenga and Balonguen situated 50 km east and south of Ouagadougou, respectively. These villages were mapped using Geographic Information System (GIS); households, larval breeding sites, and other wetlands and artiþcial lakes were located using Global Position System (GPS) (Figs. 1 and 2). These villages are in Sudan savannah area (annual rainfall 600 Ð1,000 mm; mean temperature range from 23 to 36 C). Malaria transmission is seasonal with a peak in September during the rainy season. Anopheles gambiae s.s. (Giles), Ae. arabiensis and An. funestus are the main malaria vectors and P. falciparum is the parasite specie transmitted in 90% of the cases. The socio demographic parameters of Tensobtenga and Balonguen are comparable with 1,493 and 1,318 inhabitants, respectively. In the two villages, 90% of the inhabitants belong to the Mossi ethnic group and 5% to Fulani. The inhabitants are adherents of three main religions (Christianity, Islam, and Indigenous African). The main activities are subsidence farming, livestock rearing, and small trade. Traditional dwellings constructed from mud with conical roofs are characteristic of both villages. The main notable difference between both villages is the presence of an artiþcial lake and wetlands in close proximity to Tensobtenga. This provides perennial breeding sites for mosquitoes. Balonguen on the contrary is relatively dry and devoid of a major water reservoir. Malaria is perceived as a major public health problem in both villages. At the time this study was conducted, the knowledge of the villagers about the cause and treatment of the disease was to a large extent based on indigenous beliefs and practices. Consequently, 65% of families used traditional treatments for febrile illness and where western medicines were used, the annual cost amounted to $4 U.S. per person. Mosquito Sampling. Mosquitoes were collected from 41 sentinel sites in both villages. These sites were randomly selected after a census, taking into consideration the number of potential breeding sites, and the number of households in each village, assuming that sampling effort must be greater in the low transmission village compared with the highest one. Thus, 28 collection sites in Balonguen and 13 in Tensobtenga were selected. Centers for Disease Control and Prevention (CDC) light traps were used to collect the mosquitoes. Mosquito collection was performed three times per week over a period of 12 mo by eight trained Þeld workers (four Þeld workers per village). The traps were switched on and off at h (GMT) and h (GMT), respectively. The mosquitoes collected were morphologically identiþed on site for species and

3 620 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 47, no. 4 Fig. 2. Map of the village of Balonguen. Flags indicate mosquitoes breeding sites. sex. Female Anopheles mosquitoes were stored into tubes containing silica gel for further processing. As part of the quality control of the Þeld activities, the collection and processing of the samples was supervised at regular intervals during the week by CNRFPs lab technicians. Mosquito Processing. Mosquitoes collected in the Þeld were transported to the CNRFP entomological lab for processing. Double ELISAs tests were performed on the heads and the prothoraces of female An. gambiae s.l. and An. funestus for Circumsporozoite protein antigen determination (Burkot et al. 1984, Wirtz et al. 1987). Meso/meta-thoraces and abdomens were not used. Statistical Analysis. Data were entered into excel sheet for analysis. The aggressiveness was expressed as number of bites per person per night while the entomological inoculation rate (EIR) was the product of the aggressiveness and the sporozoitic index. Ethical Approval. The study received ethical clearance from the Ministry of Health, Burkina Faso. Village meetings were held before the start of data collection during which the objectives of the study were explained. Oral consent was obtained from selected household heads before the deployment of the traps. Results Proportion of Anophelines Species in the Two Villages. During the longitudinal survey conducted from December 2000 to November 2001, a total of 54,392 female anopheles mosquitoes (92.7% of total mosquitoes) were collected. Culex, Aedes, and Mansonia genus accounted for the remaining 7.3%. Among the Anopheline mosquitoes caught, 84% were An. gambiae s.l., 15.0% An. funestus and 1.0% was constituted by An. rufipes, An. Pharoensis, and An. nili. Table 1 shows the total number of female Anopheles caught and the total processed by ELISA for CSP determination. Dynamic of An. gambiae s.l. and An. funestus s Aggressiveness. It was observed that the two major vectors, An. funestus and An. gambiae s.l., coexist in the village of Tensobtenga during the study period (Fig. 3). The maximum number of bites per person and per night associated with either An. funestus or An. gambiae s.l. was observed in Tensobtenga during the month of September. The maximum number of bites by An. funestus was four times lower than this of An. gambiae s.l. From January to May, less than one bite per night per person was because of An. gambiae; whereas for An. funestus, this range of bites was observed from January to June.

4 July 2010 EDITH ET AL.: MALARIA TRANSMISSION IN RURAL BURKINA FASO 621 Table 1. Number of female Anopheles collected from Dec to Nov and number tested by ELISA in the study villages An. gambiae s.l. An. funestus s.l. Other Anopheles No. caught No. tested (%) No. caught No. tested (%) No. caught No. tested (%) Tensobtenga 30,143 4,998 (16.6) 6,448 2,963 (46.0) (0) Balonguen 15,451 4,351 (28.2) 1,837 1,286 (70.0) 89 0 (0) In the village of Balonguen, the vectors aggressiveness followed the same trends as the peaks in September in Tensobtenga village. However, these peaks were two to three times lower. From February to May, the number of bites per person per night because of An. gambiae s.l. was negligible. However, there was an increase from June to September. It again decreased from September to November and remained low until the next rainy season (Fig. 3). The number of An. funestus bites per person per night was close to zero from January to August. The highest number of bites per person per night by this specie occurred in September with a rapid decrease in October and November. The number of bites per person per night became very low or negligible from November up to the beginning of the next rainy season. Vector Infectivity in the Two Villages. Fig. 4 shows the proportion of infected females mosquitoes of both species in the two villages. In the village of Tensobtenga, infected An. gambiae s.l. was found every month during the study period except April and May. The highest proportion of infected An. gambiae (17%) was observed in October (Fig. 4). The highest proportion (22%) of infected An. funestus was observed in January. Infected female An. funestus were not found in February, March, May, and June. It is important to note that, infected females mosquitoes of both species were not found during the month of May in this village (Fig. 4). In Balonguen, the highest proportion of infected An. gambiae (37%) was also observed in October. However, the percentage of infected An. gambiae was higher in this village than in Tensobtenga. From February to May, no infected female An. gambiae s.l. was found in Balonguen. Infected An. funestus was observed from August to November, with a peak in August (16%). From December to July, we did not observe infected female An. funestus in this village (Fig. 4). Thus, it is important to highlight the absence of infected female of both species from February to May in this village during the study period. Dynamic of Malaria Transmission Intensity in the Two Villages. In the village of Tensobtenga, the peak of malaria transmission occurs in September at the same time when the mosquitoes display increased Fig. 3. Dynamic of the vectors agressivity (An. gambiae s.l. and An. funestus s.l.) in the study villages. Line with cross refer to An. gambiae s.l. and simple line to An. funestus. Dotted lines represent the village of Tensobtenga and plain lines of the village of Balonguen.

5 622 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 47, no. 4 Fig. 4. Sporozoõˆtic index for An. gambiae s.l. and An. funestus s.l. in the study villages. Line with cross refer to An. funestus s.l. and simple line to An. gambiae s.l. Dotted lines represent the village of Tensobtenga and plain lines of the village of Balonguen. aggressiveness. However, at this period, malaria transmissionõs peak because of An. funestus is lower than that of An. gambiae s.l.. In this village, An. funestus is involved in malaria transmission in December and January, and then, from July to November, while An. gambiae s.l. is mainly found from June to December. Malaria transmission is less than one infected bite per person per month between January and May (Fig. 5). In Balonguen, malaria transmission also peaks in September with low values for An. funestus compared with An. gambiae s.l. The contribution of An. funestus to malaria transmission is most signiþcant between Fig. 5. Entomological inoculation rate per night for An. gambiae s.l. and An. funestus s.l. in the study villages. Line with cross refer to An. gambiae s.l. and simple line to An. funestus. Dotted lines represent the village of Tensobtenga and plain lines of the village of Balonguen.

6 July 2010 EDITH ET AL.: MALARIA TRANSMISSION IN RURAL BURKINA FASO 623 Fig. 6. Cumulative EIR and number of bites in the study villages. Lines with cross refer to number of bites (agressivity) and simple line to the EIR. Dotted lines represent the village of Tensobtenga and plain lines the village of Balonguen. August and November (Fig. 5). An. gambiae s.l. is the main vector of malaria in this village and accounts for majority of the transmission from June to January. Malaria transmission is nil between February and May. Dynamics of Malaria Cumulative Aggressiveness and EIR. The highest number of bites (58.6 bites) per person per night because of both An. gambiae s.l. and An. funestus species was recorded in September in Tensobtenga. During the same period, the number of infective bites per person per night because of the two species was 5.73 (Fig. 6). In Balonguen, the peaks of aggressiveness and EIR also are observed in September but with lower values compared with those of Tensobtenga (26.7 bites/person/ night and 4.30 infective bites/person/night) (Fig. 6). Discussion Proportion of Anopheline Species in the Two Villages. Our results show that Anopheline mosquitoes are the main genus encountered in the study area. In general, in Burkina Faso, Anopheles mosquitoes are important in rural areas, especially during the rainy season; breeding sites with polluted water that are favorable to the Culex species are rare. This observation is concordant with our clinical results that show that malaria incidences are 16 and 36 episodes for 1,000 children/day at risk in the high and low transmission villages, respectively. Malaria is a main public health problem in these villages. Dynamic of An. gambiae s.l. and An. funestus s Aggressiveness. This study demonstrated that the dynamic of An. funestusõs aggressiveness follow the same pattern as those of An. gambiae s.l. in Tensobtenga. In Burkina Faso, An. funestus is anecdotally generally considered a runner on the malaria transmission relay team with An. gambiae s.l.; it appears during the second half of the rainy season (end of August, September, October, and November) and contributes to malaria transmission during the dry season (Darriet et al. 1984, Rossi et al. 1986, Robert et al. 1988). The quasi-permanent coexistence of An. funestus with An. gambiae s.l. in this village can be explained by the existence of an artiþcial lake and other bodies of retained water, which favor the development of An. funestus and maintain it during the same period as An. gambiae s.l. In Balonguen, An. funestus appears in the second half of the year but it does not seem to Þll a gap for An. gambiae s.l. in malaria transmission. In fact, this species appears in September and start disappearing in November when An. gambiae s.l. is still active. Balonguen is a dry village where shady permanent and semi permanent deep waters, favorite breeding sites for funestus are rare even in the rainy season. Vectors Infectivity in the Two Villages. From our study it appears that between 7 and 37% of An. gambiae s.l. are infected in Balonguen compared with 1Ð17% in Tensobtenga. The surrounding bodies of water make Tensobtenga good breeding sites with high productivity. Herd aggressiveness is common in young vectors populations. Consequently, the proportion of infected females is lower than that observed in the more arid village of Balonguen. In Balonguen, the circulating vector population is old and may have been infected by malaria parasites. Our results are concordant with studies conducted in irrigated rice Þelds compared with nonirrigated Þelds; a study conducted by Robert et al. (1986a) in the Kou Valley of Burkina Faso reported that the high Anopheles density suggest a high intra-speciþc competition that favor an adaptive strategy with a diminution of vector longevity. A cytogenetic study showed that under these conditions, An. gambiae s.s that carried the inversion 2Ru had low

7 624 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 47, no. 4 longevity compared with those with the 2Rbc inversion (Robert et al. 1986a). Baldet et al. (2003), in the same area, observed that the great nuisance is not because of infected females. Dolo et al. (2004), showed that the high densities of mosquitoes were correlated with low anthropophily, low sporozoite rates, and probably low survival rates in an irrigated area of Mali. Our results on the sporozoite index for An. funestus seem to be related to the existence of breeding sites. Dynamics of Malaria Transmission Intensity in the Two Villages. Our results of the occurrence of the peaks of malaria transmission in September are concordant with those of previous studies conducted in Burkina Faso (Robert et al. 1985, 1986b, Ilboudo- Sanogo 2001). The contribution of An. funestus to malaria transmission, with less infected bites than An. gambiae s.l. indicates the secondary role it plays in the transmission. The lack of data on malaria transmission during some months of the study period does not mean that there is no transmission, but that, perhaps our sampling methods were not powered to detect very low presence of infected females. Dynamics of Malaria Cumulative Aggressiveness and EIR in the Two Villages. Our results showing the peaks of malaria transmission intensity and aggressiveness in September in the two study areas were not surprising because the peak of aggressiveness and transmission for each species was observed in September. These results are concordant with previous observations and studies conducted in Burkina Faso (Robert et al 1985, 1986b, Ilboudo-Sanogo 2001). In conclusion, this study shows that An. gambiae s.l. is the main vector involved in malaria transmission in both areas. The peaks of malaria transmission coincide with the one of An. gambiae s.l. maximum aggressiveness in September. If during the dry season, malaria transmission is quasi undetectable in the village with lower transmission intensity, vectors activities remained appreciable in the area with higher transmission, mainly lead by An. funestus. For most of the malaria vaccines candidates, it is suitable to complete the immunization of the volunteers before the start of the natural transmission season. This indeed permits a clear observation of the immunological effect of the vaccine outside any natural boosting. This study has shown that the month of May is the latest time window vaccine must be given before the start of the transmission season. Acknowledgments We are grateful to the residents of the study area for their help and cooperation with the study. This work was supported Þnancially by the Multilateral Initiative on Malaria (MIM) through the Tropical Disease Research Program of the World Health Organization grant. References Cited Baldet, T., A. Diabate, and T. R. Guiguemde Malaria transmission in 1999 in the rice Þeld area of the Kou valley (Bama). (Burkina Faso) Santé 13: 55Ð60. Burkot, T. R., J. L. Williams, and I. Schneider IdentiÞcation of Plasmodium falciparum-infected mosquitoes by a double-antibody enzyme-linked immunosorbent assay. Am. J. Trop. Med. Hyg. 33: 783Ð788. Darriet, F., V. Robert, N. Tho Vien, and P. Carnevale Evaluation de lõefþcacité sur les vecteurs du paludisme de la perméthrine en imprégnation sur des moustiquaires intactes et trouées, Organisation Mondiale de la Santé WHO/VBC/84.899, WHO/MAL/ Dolo, G., O. J. Biet, A. Dao, S. F. Traore, M. Bouare, N. Sogoba, O. Niare, M. Bagayogo, D. Sangare, T. Teuscher, and Y. T. Toure Malaria transmission in relation to rice cultivation in the irrigated Sahel of Mali. Acta Trop. 89: 147Ð159. Ilboudo-Sanogo, E Inßuence des rideaux imprégnés dõinsecticide sur les paramètres entomologiques de la transmission du paludisme en zone rurale au Burkina Faso. Thèse unique de doctorat en sciences biologiques appliquées, option entomologie médicale, Université de Ouagadougou, Burkina Faso. Robert, V., P. Carnevale, V. Ouedraogo, V. Petrarca, and M. Coluzzi La transmission du paludisme humain dans un village de savane du sud-ouest du Burkina Faso. Ann. Soc. belge Méd. trop. 68: 107Ð121. Robert, V., P. Gazin, C. Boudin, J. F. Molez, V. Ouédraogo, and P. Carnevale La transmission du paludisme en zone de savane arborée et en zone rizicole des environs de Bobo-Dioulasso (Burkina Faso). Ann. Soc. belge Méd. trop. 65(suppl.): 201Ð214. Robert, V., P. Gazin, V. Ouédraogo, and P. Carnevale. 1986b. Le paludisme urbain à Bobo-Dioulasso. Etude entomologique de la transmission, Cah ORSTOM. Série Entomol. Méd. Parasitol. XXIV: 121Ð128. Robert, V., V. Petrarca, P. Carnevale, and M. Coluzzi. 1986a. Le particularisme de la transmission du paludisme dans la zone rizicole de la valée du Kou (Burkina Faso); lõapport de lõétude cytogénétique des vecteurs à lõépidémiologie. Parasitologia 28: Rossi, P., A. Belli, L. Mancini, and G. Sabatinelli Enquête entomologique longitudinale sur la transmission du paludisme à Ouagadougou (Burkina Faso), Parassitologia 28: 1Ð15. Wirtz, R. A., F. Zavala, Y. Charoenvit, G. H. Campbell, T. R. Burkot, I. Schneider, K. M. Esser, R. L. Beaudoin, and R. G. Andre Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull. World Health Organ. 65(1): 39Ð45. Received 24 April 2009; accepted 14 November 2009.