Am. J. Trop. Med. Hyg., 69(3), 2003, pp. 295-302
Copyright © 2003 by The American Society of Tropical Medicine and Hygiene
DISTRIBUTION OF ANOPHELINE MOSQUITOES IN ERITREA
JOSEPHAT SHILILU,
TEWOLDE GHEBREMESKEL,
SOLOMON MENGISTU,
HELEN FEKADU,
MEHARI ZEROM,
CHARLES MBOGO,
JOHN GITHURE,
WEIDONG GU,
ROBERT NOVAK, AND
JOHN C. BEIER
National Malaria Control Program, Division of Communicable Diseases Control, Ministry of Health, Asmara, Eritrea; International Center of Insect Physiology and Ecology, Nairobi, Kenya; Centre for Geographic Medicine Research, Kenya Medical Research Institute, Kilifi, Kenya; Illinois Natural History Survey, Champaign, Illinois; Department of Epidemiology and Public Health, University of Miami School of Medicine, Miami, Florida
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ABSTRACT
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The spatial distribution of anopheline mosquito species was studied throughout Eritrea during the 1999–2001 malaria transmission seasons from October to December for the highlands and western lowlands and February to April for the coastal region. Of the 302 villages sampled, 59 were visited in both the first and second year. Overall, 13 anopheline species were identified, with the Anopheles gambiae complex predominating during the first year (75.6%, n = 861) and the second year (91.9%, n = 1,262). Intrazonal variation accounted for 90% of the total variation in mosquito distribution. Polymerase chain reaction results indicated that 99% (n = 1,309) of the An. gambiae s.l. specimens were An. arabiensis, indicating that this was the only member of the gambiae complex present. There was a high degree of aggregation of anophelines within zones and villages, with more than 80% of the total anophelines being collected from less than 20% of the villages and from only 10% of the houses sampled. At least 80% of the anopheline mosquitoes were collected from grass-thatched Agudo-type housing. Vector abundance showed an inverse relationship with elevation, with highest densities in the low-lying western lowlands. Multiple regression analysis of log-transformed mean density of An. arabiensis with rainfall and the normalized difference vegetation index (NDVI) (average NDVI, minimum NDVI, and maximum NDVI) showed that these independent variables were not significantly associated with mosquito densities (R2 = 0.058). Our study contributes to the basic understanding of the ecology and distribution of malaria vectors with respect to species composition and spatial heterogeneities both that could be used to guide vector control operations in Eritrea.
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INTRODUCTION
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Malaria accounts for more than 30% of the total outpatient morbidity in Eritrea and about 28% of all hospital admissions (Ministry of Health, unpublished data). The country is divided into three main epidemiologic strata. The first is the western lowlands at 500–1,500 meters above sea level. In this region, malaria is highly seasonal and the area is prone to epidemics. Transmission is perennial along rivers, valleys, and in irrigation projects. The second is the coastal plain along the Red Sea that experiences scanty rainfall and has generally low malaria endemicity. The third is the highlands with an average elevation of 2,000 meters above sea level that experiences generally very low levels of malaria. Almost 67% of the residents of Eritrea live in malaria-endemic areas.
Although malaria remains a major cause of mortality in Eritrea, especially among children less than five years of age, little is known about the Anopheles mosquito species responsible for transmission. The only recent data on vector species comes from studies conducted at five sites in western Eritrea along the Eritrea–Ethiopia border.1 These studies focused only on the Anopheles gambiae complex and were limited in geographic range. Some information on vector bionomics could be extrapolated from studies done in neighboring Ethiopia, but this would not describe the distribution of vectors in Eritrea due to ecologic differences between the two countries.2,3 Ecologic diversity plays an important role in determining how mosquito populations are structured since each mosquito species has a geographic range that is limited according to its physiologic tolerances to existing environmental conditions.
Early studies indicated that 34 Anopheles species were present in Ethiopia and that up to 19 species were present in Eritrea.4 The spatial patterns of these anopheline species would provide insight into the dynamics of malaria parasite transmission that are needed to guide vector control operations. The success of vector control largely depends on an understanding of the bionomics of the anopheline species responsible for malaria transmission.5 The present paper describes the first detailed study on the species composition and spatial distribution of Anopheles mosquitoes in Eritrea. These data are necessary for developing efficient and focused vector control strategies.
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MATERIALS AND METHODS
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Country profile.
Eritrea is situated in the horn of Africa and lies between longitudes 36°30'E and 43°20'E and latitudes 12°42'N and 18°2'N. It is bordered by Sudan to the north and northwest, Ethiopia to the south, Djibouti on the southeast, and the Red Sea to the east (Figure 1
). It has an area of approximately 124,000 km2, including the Dahlak Archipelago and the islands in the Red Sea. Rainfall is scanty and highly seasonal and ranges from 400 mm to 650 mm per year in the highlands and from 200 mm to 300 mm in the lowlands. Daytime temperatures range from 16°C to more than 40°C in different parts of the country. The rainy season occurs in the central highlands and the western lowlands between July and September and in the coastal plains from October to April. The peak malaria transmission is experienced at the end of the rainy season, and occurs in the coastal zone between February and April and in the central highlands and western lowlands from October to December. The country is divided into six administrative zones and 56 sub-zones containing approximately 1,500 villages. Villages are isolated due to the nucleated nature of settlement and houses within villages are generally close to each other. The estimated population is approximately 3.5 million, with about 10% of the population living in urban areas.
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FIGURE 1. Map of Eritrea showing the six administrative zones and the location of the study villages. Eritrea borders Ethiopia, Sudan, and Djibouti in the Horn of Africa, and lies at the northernmost limit of the distribution of malaria in east Africa, with transmission varying from stable to epidemic.
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Study sites.
Thirty villages were selected in each of five zones, i.e., Anseba, Debub, Maekel, Gash-Barka, and Northern Red Sea (NRS) in the first and second year of the survey, except for the Maekel zone, where only 15 villages were sampled during the second year and for the Southern Red Sea zone (SRS), where studies were conducted only in 17 villages during the first year. A total of 176 and 135 villages were surveyed during the first and second phases of the study, respectively (Figure 2). The selection of villages was based on the sub-zones, with at least two villages randomly selected from each sub-zone. Fifty-nine villages that reported either very high or low vector densities during the first year were sampled again during the second year. In each village, mosquito sampling was conducted in 10 randomly selected houses, 5 at the periphery of the village and 5 at the center. The houses comprised the four main housing types found in the country, i.e., Agudo, rectangular, Hudmo, and portable houses. Agudo houses are grass-thatched with mud walls. Rectangular houses are stonewalled with roofs made of tin. Hudmo houses are distinguished by their curved roofs that are made of wood and compacted soil. The portable house types are temporary, movable structures made of sticks covered with mats. The walls in the houses were made of mud, mats, plaster, stone, thatch, tin, or sticks.
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FIGURE 2. Spatial variation in the densities of Anopheles mosquitoes in Eritrea. Anopheles species are found throughout the country, with a highly aggregated spatial distribution (51.5% in the Gash-Barka zone and 34.5% in the Anseba zone).
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Mosquito sampling and processing.
The surveys were conducted over two malaria transmission seasons. In the Anseba, Debub, Gash-Barka and Maekel zones, sampling was conducted from October to December in 1999 and 2000, respectively, coinciding with the peak malaria transmission season. In the NRS and SRS zones, sampling was conducted between February and April in 2000 and 2001. Sampling of mosquitoes in each village was done only once. In each selected village, indoor resting anopheline mosquitoes were collected inside 10 randomly selected houses by pyrethrum spray catches conducted from 6:00 AM to 9:00 AM. The female anopheline mosquitoes were placed in petri dishes lined with moist cotton wool and filter paper and later identified to species by morphologic criteria.6,7
Polymerase chain reaction (PCR) and determination of sporozoite rate.
A proportion of the An. gambiae s.l specimens were identified to sibling species by a ribosomal DNA PCR using primers specific for An. arabiensis, An. gambiae, and An. quadriannulatus.8 DNA was extracted from wings and legs.9 The head and thorax of each mosquito was separated from the abdomen and tested for the presence of Plasmodium falciparum circumsporozoite protein.10 Mosquitoes were ground in 50 µl of boiled casein containing Nonidet 40, with the final volume brought to 250 µL with blocking buffer. Fifty microliters of the triturate was used in an enzyme-linked immunosorbent assay and positive reactions were determined visually.10
Statistical analysis.
Density of anopheline mosquitoes was expressed as the number of female anophelines per house for each species. Log transformation [log10 (x + 1)] of the data was done to stabilize the variance. Statistical analyses were performed only for An. gambiae s.l., the predominant species (84.5% of the total specimens). An analysis of variance (ANOVA) examined the effects of zones, elevation, house type, wall type, and their interactions. We grouped houses into three categories of elevation, <500, 500–900, and >900 meters above sea level, as low, medium, and high, respectively. The analyses were performed using a general linear model (GLM) with SPSS version 11.5 software (SPSS Inc., Chicago, IL). Because of missing cells in interaction analyses, type IV (sums of squares) model was specified in the GLM. We excluded samples collected from Hudmo and portable houses because they were sampled in only two zones (Anseba and NRS). Similarly, the samples collected from houses with sticks or tin walls were not included in the analyses because a small number of houses with these types of walls were sampled. Multiple regression analysis examined relationships between An. gambiae s.l. densities and environmental variables. Rainfall data was derived from Government of Eritrea rainfall distribution maps from 1990 to 2000. The rainfall estimates were grouped into five categories (
200, 201–300, 301–400, 401–500, and >500 mm per year). The normalized difference vegetation index (NDVI) data was derived from the Famine Early Warning System using National Oceanic and Atmospheric Administration satellites.
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RESULTS
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Vector species composition and abundance.
A total of 2,513 adult female anopheline mosquitoes representing 13 species were collected during the two sampling periods (Table 1). Anopheles gambiae s.l. (84.5%) was the most abundant species, followed by An. d’thali (9.4%) and An. cinereus (3.4%). The rest of the 10 species comprised less than 3% of the total catch. The density of An. gambiae s.l., expressed as number of female mosquitoes per house, varied significantly among the four zones (Table 2). The highest density of An. gambiae s.l. was found in the areas covering the western escarpments, which comprised a large part of the Anseba zone, and the western lowlands of the Gash-Barka zone (Figure 2
). Anopheles d’thali was sampled predominantly from the Anseba zone (75%, n = 216), whereas a large proportion of An. cinereus (57%, n = 48) was found in the Maekel zone at elevations > 1,800 meters above sea level.
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TABLE 1 Species composition and relative abundance of adult Anopheles mosquitoes collected between October 1999 and April 2001 in Eritrea*
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TABLE 2 Analysis of variance examining variation in Anopheles arabiensis densities in the countrywide survey between October 1999 and April 2001 in Eritrea
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The Debub zone had the highest diversity of anopheline species. Of the 13 Anopheles species sampled, 8 were found in the Debub zone, 6 each in the Anseba and Maekel zones, and only 2 species in the Gash-Barka zone. Geographic variation in anopheline species composition is shown in Figure 3. In 59 villages where sampling was conducted in both the first and second years of the study, no significant difference in mean density of An. gambiae s.l. was found between years (t = 0.433, degrees of freedom = 58, P = 0.667). Anopheles d’thali was collected more frequently in the first year of the study than in the second year (Table 3).
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FIGURE 3. Spatial distribution of Anopheles species in Eritrea. The greatest diversity in Anopheles species was observed in the high altitude areas of the country, which encompasses the Debub and Anseba zones.
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TABLE 3 Summary of the total number of Anopheles mosquitoes collected in 59 villages sampled both in the first and second years of the countrywide survey in Eritrea*
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Analysis of An. gambiae s.l. sibling species by PCR.
To identify the An. gambiae s.l. species present, 1,446 specimens were analyzed by PCR using primers specific for An. gambiae s.s, An. arabiensis, and An. quadriannulatus. Of the total mosquitoes identified, more than 99% (n = 1,309) were An. arabiensis, indicating that this may be the only representative of the gambiae complex present. Specimens of the gambiae complex hereafter are referred to as An. arabiensis. Only one mosquito was identified as An. gambiae sensu stricto and no An. quadriannulatus was identified among the gambiae complex specimens tested.
Plasmodium falciparum sporozoite rates.
Of the 1,505 anopheline mosquitoes tested, only five were positive for P. falciparum circumsporozoite antigen, yielding a low sporozoite rate of 0.33%. Of the five positive anophelines, one positive An. cinereus was collected in the Maekel zone at an elevation of more than 2,000 meters, one An. d’thali was collected in the Anseba zone, and three An. arabiensis (0.2%) were collected in the Anseba (n = 1) and Gash Barka (n = 2) zones.
Spatial variation in Anopheles densities.
Our data showed that there was distinct aggregation of An. arabiensis within zones and villages. Overall, more than 80% of this species was sampled from less than 20% of the villages in all the zones. Within villages, 80% of the total An. arabiensis collected came from 1.8%, 2.0%, 8.5%, and 10.2% of the houses sampled in the NRS, Debub, Anseba, and Gash Barka zones, respectively. Anopheles d’thali and An. cinereus showed similar clumped distribution patterns, with more than 90% of the two species collected from only 2% of the 2,850 houses sampled countrywide.
The density of An. arabiensis varied significantly with elevation (Table 2), being most abundant between 500 and 900 meters above sea level. This elevation covers the western escarpments, which comprise a large part of the Anseba zone and the western lowlands of the Gash-Barka zone. Low numbers were found in villages more than 900 meters above sea level, although 4.4% (n = 110) of the An. arabiensis specimens were collected in villages located more than 1,800 meters above sea level. The ANOVA model used to examine the effects of zones, elevation, house type, and wall type on vector densities showed significant two-way interactions (Table 2). Collections of An. arabiensis made at high elevations were similar to those from low elevations. However, in the Gash-Barka zone, collections at high elevations were significantly greater than those from low elevations (Figure 4A). Similarly, the difference in An. arabiensis densities between the Agudo and rectangular house types was only significant in the Gash-Barka zone (Figure 4B). Captures of An. arabiensis in Agudo houses were generally greater than in rectangular houses except in houses with thatched walls (Figure 4C). Among houses with different wall types, An. arabiensis densities were generally lower in stone walled houses at low and medium elevations, but at high elevations, stone walled houses had more An. arabiensis (Figure 4D).
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FIGURE 4. Plots of the two-way analysis of variance interactions between A, Zone and elevation; B, Zone and house type; C, Elevation and wall type; and D, House type and wall type for Anopheles arabiensis in Eritrea. The y-axes show estimated means of An. arabiensis adjusted for other factors. *No observations for some combination of the factors. NRS = Northern Red Sea.
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We conducted multiple regression analysis of log-transformed mean density of An. arabiensis with rainfall and NDVI (average, minimum, and maximum) as independent variables. The low amount of variation (R2 = 0.058) in the dependent variable explained by the combination of the independent variables (rainfall and NDVI summaries) in the regression model indicated that the two variables were not good predictors of An. arabiensis density (Table 4). Rainfall was the only significant variable in the model, though independently, it had low explanatory power.
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DISCUSSION
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A total of 13 anopheline species were collected from indoor resting sites representing the ecologic diversity present in Eritrea. The country can be divided roughly into five ecologic zones, i.e., western lowlands, western escarpments, central highlands, eastern escarpments, and coastal plains. Each of these zones present specific ecologic conditions arising from differences in elevation, rainfall, and temperature, which favor the survival of the wide range of anopheline species. Intrazonal variability in ecologic conditions would further explain the diversity in anopheline species composition observed in specific zones such as the Anseba and Debub zones. Anopheles d’thali and An. cinereus were the second and third most abundant species. The low sporozoite infection rate of 0.33% determined in the present study may explain the low levels of malaria endemicity experienced in the country. However, coupled with high biting rates at specific times of the year and vector bionomics, appreciable levels of malaria in the population could be maintained.11 Because An. d’thali and An. cinereus, which were not previously incriminated as vectors of malaria in Eritrea, were positive for P. falciparum circumsporozoite antigens, this suggests that there is need to monitor the abundance of these two species in space and time. The changes in ecologic conditions associated with human influences and global climate changes may affect the abundance and possibly the vector potential of such rare species.
The PCR assays on more than 30% of the An. gambiae s.l. specimens indicated that An. arabiensis was the only member of the gambiae complex present in Eritrea. This result is consistent with findings from preliminary studies conducted in five villages in western Eritrea, along the border with Ethiopia and Sudan, in which An. arabiensis was documented as the only member of the An. gambiae complex through cytogenetic studies.12 Anopheles arabiensis has been documented as the predominant member of the An. gambiae complex and the main vector of P. falciparum malaria in neighboring provinces of Ethiopia and the Sudan.13,14 Eritrea generally is semi-arid and receives scanty rainfall (<500 mm per year), within a short rainy season that lasts no more than three months. Previous findings on the bionomics and habitat preferences show that An. arabiensis would normally predominate under such dry climatic conditions.15–17 In Eritrea, this species is associated with river systems, with breeding maintained in stream bed pools throughout the year and in transient pools such as roadside ditches during the rainy season.18
Almost 90% of the total mosquitoes were sampled from only 10% of the houses. This heterogeneity in distribution may have important operational significance because vector control operations would be designed to target villages within zones where high densities of malaria vectors are found. For example, a greater risk of malaria infection and intensity of malaria transmission is likely in specific sites in the Gash-Barka zone based on the vector density recorded. A risk-stratified approach to vector control would save on effort and cost in situations where resources are limited as is the case in most malaria-endemic areas in sub-Saharan Africa. The significant interactions between house-related factors revealed by the ANOVA model are useful for designing sampling plans and show the need to focus on house type in implementing vector control measures.
Elevation greatly influenced mosquito densities due to its modifying effect on temperature and humidity. Anopheline mosquitoes were present at altitudes greater than 2,000 meters, indicating that such areas would not remain free of malaria in the light of the modifying effects to the ecosystem associated with human influences on both local and global scale.5 Fairly high densities of anophelines also were sampled at altitudes between 1,400 and 1,800 meters above sea level. These fringe areas may be prone to malaria epidemics since the highest density of the non-immune population in Eritrea is also found within these areas.
No significant association was found between NDVI summaries, rainfall, and An. arabiensis density in the regression model. This could be attributed to the complex nature of interactions between these ecologic variables, which may have specific time lags that may not have been captured by the present analyses. Rainfall independently was significantly associated with the An. arabiensis population. This occurrence confirms the seasonal nature of malaria transmission in Eritrea, which coincides with the one short rainy season experienced in all ecologic regions of the country. In the drier regions of Africa, such as the Sahelian belt, it has been observed that even relatively small differences in rainfall and soil moisture content can influence substantial changes in the ecology of an area and consequent differences in the composition of mosquito vector species.19 For instance, chromosomal variants of An. gambiae have been shown to be commonly associated with prevailing ecologic conditions of a given region.20 The small area variations in rainfall amounts in the semi-arid situation experienced in Eritrea could therefore significantly affect mosquito density and composition. It is likely that systematic monitoring of rainfall amounts under such semi-arid conditions can provide a sensitive surveillance tool for forecasting malaria transmission in the country.
The present study is the first to provide information on the vector species diversity in Eritrea on a countrywide scale. The intra-zonal variations observed in the present study show that heterogeneities in risk status have to be addressed even within a small ecologic area. Strengthening of vector surveillance mechanisms to monitor surges in vector densities would be central in making informed vector control decisions.
Received December 30, 2002.
Accepted for publication June 10, 2003.
Acknowledgments: This work was performed by the Eritrea National Malaria Control Program to improve the knowledge base for malaria vector control decisions. We thank the program’s headquarters staff (Yohannes Bein, Fessahaye Seulu, Asmelash G. Egzibiher, and David Sintasath) for technical support, and the zonal staff for conducting the field surveys. We acknowledge the valuable support received from Saleh Meky (Honorable Minister of Health), Dr. Andom Ogbamariam (Director of Communicable Diseases Control), the Chief, Health Strengthening Office, the United States Agency for International Development (USAID)/Asmara, Linda Lou Kelley, and Eugene Brantly (Activity Manager, Environmental Health Project).
Financial support: The study was funded by the USAID through a mechanism for cooperation with the Ministry of Health, Eritrea, and with technical support from the USAID Environmental Health Project.
Authors’ addresses: Josephat Shililu, National Malaria Control Program, Division of Communicable Diseases Control, Ministry of Health, PO Box 212 Asmara, Eritrea and International Centre of Insect Physiology and Ecology, PO Box 30772, Nairobi, Kenya. Tewolde Ghebremeskel, Solomon Mengistu, Helen Fekadu, and Mehari Zerom, National Malaria Control Program, Division of Communicable Diseases Control, Ministry of Health, PO Box 212 Asmara, Eritrea. Charles Mbogo and John Githure, International Centre of Insect Physiology and Ecology, PO Box 30772, Nairobi, Kenya, Telephone: 254-2-861-680, Fax: 254-2-860110. Weidong Gu and Robert Novak, Illinois Natural History Survey, 607 E. Peabody, Champaign, IL, Telephone: 217-333-1186, Fax: 217-333-2359. John C. Beier, Department of Epidemiology and Public Health, University of Miami School of Medicine, Highland Professional Building, 1801 NW 9th Avenue, Suite 300 (D-93), Miami, FL 33136, Telephone: 305-243-2977, Fax: 305-243-3324.
Reprint requests: Josephat Shililu, National Malaria Control Program, Division of Communicable Diseases Control, Ministry of Health, PO Box 212, Asmara, Eritrea. Telephone: 291-1-125-529, Fax: 291-1-122-899 or 291-1-125835, E-mail: shililu{at}gemel.com.er.
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ABSTRACT
INTRODUCTION
