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    (a) Administrative map of the six zobas in Eritrea and the distribution of villages surveyed; (b) the distribution of malaria prevalence among villages surveyed.

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    Age and sex-specific prevalence rates by ecological strata.

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    Shililu J, Ghebremeskel T, Mengistu S, Fekadu H, Zerom M, Mbogo C, Githure J, Gu W, Novak R, Beier JC, 2003. Distribution of anopheline mosquitoes in Eritrea. Am J Trop Med Hyg 69 :295–302.

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    Shililu J, Ghebremeskel T, Seulu F, Mengistu S, Fekadu H, Zerom M, Ghebregziabiher A, Sintasath D, Mbogo C, Githure J, Brantly E, Novak R, Beier JC, 2004. Seasonal abundance, vector behavior, and malaria parasite transmission in Eritrea. J Am Mosq. Control Assoc 20 :155–164.

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MALARIA PREVALENCE AND ASSOCIATED RISK FACTORS IN ERITREA

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  • 1 Health and Child Survival Fellows Program, Johns Hopkins University, USAID/Eritrea; National Malaria Control Program, Ministry of Health, Asmara, Eritrea; Bureau for Global Health, USAID, Washington, D.C.; Environmental Health Project, Arlington, Virginia; International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, University of Miami School of Medicine, Miami, Florida

A parasitological cross-sectional survey was undertaken from September 2000 through February 2001 to estimate the prevalence of malaria parasitemia in Eritrea. A total of 12,937 individuals from 176 villages were screened for both Plasmodium falciparum and Plasmodium vivax parasite species using the OptiMal Rapid Diagnostic Test. Malaria prevalence was generally low but highly focal and variable with the proportion of parasitemia at 2.2% (range: 0.4% to 6.5%). Despite no significant differences in age or sex-specific prevalence rates, 7% of households accounted for the positive cases and 90% of these were P. falciparum. Multivariate regression analyses revealed that mud walls were positively associated with malaria infection (OR [odds ratio] = 1.6 [95% CI: 1.2, 2.2], P < 0.008). For countries with low and seasonal malaria transmission, such information can help programs design improved strategic interventions.

INTRODUCTION

Malaria in Eritrea is a major public health problem with 67% of the population living in areas at risk for the disease. Malaria has accounted for approximately one-quarter of all hospitalizations in Eritrea and has significant economic impact on the population, particularly as it is considered the leading cause of death among those 5 years and above and the third leading cause of death for under 5.1

In 1999, under the context of the Roll Back Malaria Initiative, the National Malaria Control Program (NMCP) developed a 5-year national plan to reduce malaria morbidity and mortality by 80% of 1999 levels.2 Employing an integrated and comprehensive approach that includes prompt and adequate case management, selective vector control, epidemic management and control, environmental management and personal protection through the use of insecticide-treated bed nets (ITBs), the NMCP is conscientious of the malaria burden in Eritrea and is devoted to achieving this ambitious target.

Despite recent research efforts to describe the distribution of malaria vectors,3,4 their behavior,5 and vector control measures in the country,6 extensive information regarding the epidemiology of malaria in Eritrea has been limited. The primary objectives of this study were to estimate the prevalence and distribution of malaria in the country using a rapid diagnostic test and to identify major risk factors associated with parasitemia. Having been evaluated in a number of field settings,79 the OptiMal rapid dipstick was used considering the scale of this national survey and the lack of manpower available to conduct adequate microscopic screening.

Eritrea is divided into six administrative regions: Anseba, Gash Barka, Debub, Maekel, Northern Red Sea (NRS), and Southern Red Sea (SRS). These zobas are further divided into smaller administrative sub-zobas. There are two main malaria transmission seasons in the country: one between September to November in the central, western, and southern parts of the country and the other from January to March along the coastal plains following their respective rainy seasons. Divided into three general epidemiologic zones, the western lowlands (700 to 1500 m above sea level) have highly seasonal malaria transmission, coinciding with the annual rains and agricultural activities. The coastal plains (0 to 1000 m above sea level) have limited malaria but pockets of sustained malaria transmission persist, particularly near irrigation dams and rain-fed agricultural areas. Finally, the central highlands (1500 to 2000 m above sea level) are generally free from malaria but are especially at risk for malaria epidemics due to low levels of immunity among these populations, as well as the potential introduction of malaria parasites through population movements and demobilization.

MATERIALS AND METHODS

Sampling design.

A stratified and weighted sampling frame was developed to select more villages from sub-zobas that exhibited greater ecological diversity and population density. Five of the six administrative zobas of the country (Figure 1a) were included in the two-stage cluster, probability proportional to size (PPS) sampling frame. Due to the arid, remote conditions and relatively few endemic malaria cases of the southern coastal regions, SRS zoba was not included in the prevalence survey. Using historical data, the timing of the survey coincided with the expected peak of malaria transmission (i.e., September and October 2000 for Gash Barka, Anseba, Debub, and Maekel zobas, and February 2001 for NRS zoba, which has a different transmission season).

Sub-zobas within each larger administrative zoba were stratified using available altitude, rainfall, and average normalized difference vegetation indices (NDVI), resulting in five broad ecological strata: highlands (altitudes above 2000 m above sea level with 200 to 400 mm of annual rainfall and therefore a fairly high vegetation density); western wet lowlands (500 to 1000 m and rainfall averages above 400 mm annually); western escarpments and valleys (1000 to 2000 m and more than 200 mm annual rainfall); eastern escarpments (500 to 2000 m and more than 200 mm annual rainfall); and dry coastal lowlands (below 500 m and average annual rainfall less than 200 mm) (Bretas G and others, unpublished data).

Due to a lack of specific geographic data linking individual villages to specific ecological zones, sub-zobas with greater diversity were oversampled to increase the likelihood of including villages from each ecological zone. The PPS sampling methodology was used to select the primary sampling units (villages) so that villages with more households had higher probabilities of selection within each stratum.

A total of 52 and 46 villages were randomly selected in Anseba and NRS, respectively. In Gash Barka and Debub zobas where previous entomological work had been conducted at 12 sites, an additional 20 villages each were randomly selected, making a total of 32 villages from each zoba. A total of 15 villages were selected in Maekel zoba—7 of these villages were previous entomological sites, and 8 new villages were randomly selected. Based on the sample sizes for each administrative zoba, it would be expected that at least a 15% difference in malaria prevalence between any two groups (i.e., zobas) would be detected at the 95% confidence level.

Systematic randomization was conducted at the village level for the selection of households. Houses were selected by field teams as they moved from the center or periphery of the village following a designated path using the “spin the bottle” methodology. Every third house encountered was selected by the team for malaria parasite screening. If there were no respondents present or if the respondents refused to take part in the survey, the teams substituted it with an adjacent house.

Ethical review.

There was no formal ethical review body in Eritrea at the time of the survey. Informed consent was verbally obtained from respondents in conformance with U.S. Agency for International Development (USAID) regulations for survey research of this type. An ad hoc review process was undertaken with the Eritrean Ministry of Health and National Malaria Control Program to ensure appropriate informed consent procedures were applied by the interview teams.

Screening method.

The OptiMal Rapid Malaria Test (Flow Incorporated, Portland, OR) was used to screen for both Plasmodium falciparum and Plasmodium vivax malaria parasite species. This rapid diagnostic test uses an immunologic detection system for the parasite lactate dehydrogenase (pLDH) enzyme, which is present in and released from infected red blood cells. Mixed infections from both species were not distinguished. The administration of the OptiMal Rapid Malaria Test was performed according to the manufacturer’s protocol. Infected individuals were given antimalarial treatment according to national guidelines, and other serious ailments were referred to the nearest health facility for treatment. Young children less than 1 month of age were not screened.

Questionnaire format.

In addition to screening all household members for malaria parasites, the field teams used a closed-ended questionnaire format to inquire about overnight travel, febrile history, and antimalarial drug use within the last 2 weeks prior to the interview. Observations were also recorded regarding domicile characteristics, possible household risk factors for malaria (e.g., wall type, roof type, open or closed eaves, etc.), and methods of mosquito control. Each team of interviewers spent approximately 30 minutes per household.

Analysis.

Data collected from both the household and individual surveys were matched using a unique zoba/village/household/individual variable, resulting in 12,937 observations, or individuals who were screened for malaria parasites and completed the household questionnaire. To control for confounding factors such as ecological strata, multivariate logistic regression analyses were performed using the software program STATA 7.0 (College Station, TX).

RESULTS

A total of 2,779 households were interviewed, and 12,937 individuals were screened for malaria parasites with an acceptable overall response rate of 88.7%. Plasmodium falciparum was the predominant malaria parasite species detected using the OptiMal Malaria Test. Overall, the species distribution was 90.4% P. falciparum (95% confidence interval [CI]: 86.5, 93.9) and 9.6% P. vivax (95% CI: 6.1, 13.1).

Ecological strata.

Malaria was distributed in all five ecological strata, and analysis of proportion positives by ecological strata showed that there was a significant difference (F = 7.475, P < 0.0001) among the different strata. More specifically, the wet lowland portion of the country (i.e., southwest region bordering Ethiopia and Sudan) had a significantly higher proportion of malaria positives when compared with the other ecological zones (Table 1). Four of the five cases of malaria detected in the highlands of Eritrea (> 2000 m above sea level) were P. falciparum, though it should be noted that parasitemia was present at intermediate rates along the highland fringes of the eastern and western escarpments.

Village level.

A total of 176 villages were sampled with malaria prevalence varying from 0% to 35.8% (Figure 1b). Villages situated at higher elevations had fewer parasitemia (OR = 0.07 [0.02, 0.28], P < 0.0001) (Table 2), as well as those reported to ever having been sprayed with residual insecticide (either with DDT or malathion) (OR = 0.23 [0.10, 0.57], P < 0.001). The location of villages near streams (<500 m), one of the main larval habitats for Anopheles arabiensis in Eritrea, was not found to be associated with parasitemia within a village.

Household level.

A total of 2,779 households were interviewed, and the results indicated that 90% of the malaria positive cases were found in only 6.7% of households. Using an outcome variable of whether a household had at least one malaria case, multivariate analysis controlling for different ecological strata suggested that houses with mud walls increased a household’s risk of parasitemia (OR = 1.6 [1.2, 2.2], P < 0.006) compared with other types of construction materials used for walls (Table 3). Houses that had been sprayed with insecticide in the past were protected against parasitemia (OR = 0.26 [0.14, 0.48], P < 0.0001). Conversely, houses that were recently sprayed (i.e., within the previous 6 months) were five times more associated with parasitemia, suggesting that recent spraying was conducted more as a reactive measure against an increase of suspected malaria cases. In addition, households in sub-zobas with above average rainfall 1 month prior to being surveyed were three times more likely to suffer from parasitemia (OR = 2.9 [1.3, 6.4], P < 0.008) than those in areas with average or below-average rainfall.

Individual level.

Within each ecological stratum, parasitemia appeared to be similarly distributed across the different age groups (Figure 2). However, malaria prevalence rates were significantly higher for all age groups in the wet lowland ecological zone, with the exception of males in the under-5 age category. Individual malaria risk was essentially the same among those who reported having traveled and those who did not travel within the past 2 weeks (data not shown). Among the 285 individuals who tested positive for malaria parasitemia, only 125 (44%) reported having a fever within the past 2 weeks. Individuals who reported having slept under an insecticide-treated bed net (ITB) showed a slightly reduced risk of parasitemia (OR = 0.74 [0.47, 1.2], P < 0.205), though not statistically significant due to the few number of cases.

Health Management Information System.

The Eritrean National Health Management Information System (NHMIS) routinely collects morbidity data for both clinically diagnosed and laboratory-confirmed malaria cases from all health facilities. Data collected through NHMIS and the prevalence survey for the same period showed a positive correlation between the two variables (r2 = 0.137), though it was not significant. Malaria morbidity reported through health stations (the primary level of health care provision) is generally clinically diagnosed and may have lessened the correlation between reported malaria cases at health facilities and parasitologic prevalence rates obtained from this survey. Furthermore, the fact that a village is only one part of the catchment area of a health facility may have also weakened this correlation.

DISCUSSION

Malaria is not uniformly distributed in Eritrea, possibly due to the tremendous ecological diversity within zobas and sub-zobas. It is generally regarded as a disease of poverty with many of the risk factors inversely related to a household’s socioeconomic wealth.1012 In areas of low endemicity, malaria risk can be widely varied between localities or even households1315 and it has been postulated that these differences may be due to specific characteristics of houses or their locations that may facilitate contact between humans and mosquitoes.16,17 Controlling for differences in ecological setting, analysis of domicile characteristics (i.e., roofing and wall materials used) suggested that walls made from mud, a common type of housing construction known as Agudo in the western lowlands of Eritrea, increased an individual’s risk for parasitemia compared with individuals living in houses with other types of construction materials. This association correlates with previous findings of increased risk of parasitemia in houses made with earth roofs among Tigray households in the Ethiopian highlands.18 These traditional types of housing construction provide microenvironments conducive for mosquitoes19 and may extend their chance of survival and feeding opportunities.

Selective indoor residual spraying (IRS) remains one of the key strategies of the NMCP, though primarily used for epidemic prevention and response. Indoor residual spraying with insecticide has been shown to be highly effective as a malaria control measure in reducing the incidence of malaria infections and deaths in a number of settings.20,21 Our findings support that IRS, primarily with DDT or malathion, was associated with fewer cases of parasitemia, though its actual impact on adult mosquito densities indoors was not evaluated. The strong positive association of parasitemia and houses having been recently sprayed within the previous 6 months seems to suggest that IRS may be used as a reactive measure. In other words, spraying of houses in target areas may be conducted in response to increases of vector populations and malaria cases rather than as a preventive measure. The use and appropriateness of selective IRS in epidemic-prone situations such as Eritrea may require further evaluation.

Our findings indicate that malaria risk in Eritrea was uniformly distributed across all age groups, contrary to the situation in much of Africa where malaria is considered a disease of children under 5 years and of pregnant women. Malaria transmission intensities in Africa are as diverse as its people, and it should not be assumed that the burden is restricted to certain target populations. Our findings support the argument that in areas with low natural immunity, health promotion should be provided to all age groups. It was interesting to note that males had a higher though not statistically significant risk of parasitemia compared with female counterparts. Despite the small number of malaria positives, occcupational exposure or cultural traditions may be interesting areas for further research in this setting.

Eritrea is at the northernmost limit of malaria distribution in East Africa,22 and this contributes to the highly seasonal and focal nature of the disease in the country. Besides geographical and altitudinal limits, malaria in Eritrea appears to be highly associated with temperature and rainfall. In fact, a recent study has found that the seasonality of malaria transmission risk in Eritrea can be determined using a model that incorporates temperature and the holding capacity of moisture in the soil.23

In addition to the seasonality of malaria transmission, Eritrea has another important advantage: limited larval habitats that can be identified and monitored. Environmental management (i.e., manual clearing or leveling of potential larval habitats) has long been an important strategy for malaria control in Eritrea. The arid environment found in most of the lowland regions of the country and the seasonal rainfall patterns result in fairly limited and temporary free-standing pools of water, making clearing and leveling an attractive and environmentally friendly option for Eritrea. Seasonal rainfall (generally 2 to 4 months of the year) and the low to moderate transmission of malaria make the Eritrean situation much more amenable to control than other African countries with intense year-round malaria transmission.

There were clear limitations with this study. First, this was a cross-sectional survey conducted during a period of expected peak malaria transmission, when in fact the entire horn of Africa region was experiencing drought conditions, which may be have contributed to the low prevalence rates detected. Furthermore, malaria incidence has been exhibiting a decreasing trend since 1999—but this could also be due to the scaling up of numerous activities of the NMCP (including the updating of the national drug policy, distribution and large-scale re-impregnation of bed nets, etc.). Second, the data obtained from this type of study does not provide temporal information to determine risk throughout the year or from one year to the next. Third, the questionnaire design did not enable us to evaluate fully the socioeconomic factors that may be inherently associated with malaria risk. And finally, it is acknowledged that there are some sensitivity and specificity issues regarding the use of rapid dipsticks for epidemiologic screening of malaria in field conditions.24 However, routine microscopy, often considered the gold standard, is highly dependent on the skills of the microscopists, storage and quality of the stains and reagents, as well as the workload of the individual. The lack of skilled manpower to perform microscopy on 13,000 individuals in this study made the slight loss of sensitivity seem justifiable.

Evidence-based targeting of interventions for malaria control in selected areas is obviously an attractive strategy for developing countries with limited human and capital resources. In Eritrea, a small country with tremendous ecological diversity and variation, malaria risk stratification based on traditional determinants such as rainfall and altitude remains an important tool for prioritizing operational activities. Our findings suggest that above average rainfall can be a useful proxy for malaria risk in areas of unstable malaria transmission. Furthermore, understanding the determinants of malaria risk, including housing construction, may enable the tailoring of malaria control interventions for different ecological zones. Given the manageable size of the country, the limited malaria transmission season and rainfall, and the overwhelming determination of its people, it should be feasible for Eritrea, with sustained momentum, to roll back malaria significantly in a relatively short period of time.

Table 1

Proportion of positives at village, household, and individual levels by ecological strata

Proportion positive (%)
Ecological strataVillageHouseholdIndividual95% CI*
* 95% confidence interval for individual proportion positive estimates.
Highlands3/23 (13)5/274 (1.8)5/1286 (0.4)0, 0.7
Wet lowlands19/25 (76)54/292 (18.5)93/1429 (6.5)5.2, 7.8
Western escarpments21/49 (43)36/791 (4.6)71/3591 (2.0)1.5, 2.4
Eastern escarpments14/36 (39)31/639 (4.9)35/2825 (1.2)0.8, 1.7
Dry lowlands22/43 (51)60/783 (7.7)81/3806 (2.1)1.7, 2.6
Total79/176 (45)186/2779 (6.7)285/12937 (2.2)2.0, 2.5
Table 2

Multivariate logistic regression for village risk factors and parasitemia among 176 observations

Village risk factorCases/exposedOdds ratio95% CIP value
* Significant at P < 0.05.
Ecological strata
    Eastern escarpment13/311.00
    Western escarpment20/471.03
    Dry lowland19/401.25
    Wet lowland18/234.981.47, 16.90.010*
Altitude (m)
    0–50026/421.00
    501–180050/1060.55
    > 18003/280.070.02, 0.280.0001*
Near river (< 500 m)
    No44/981.00
    Yes35/780.610.13, 2.900.533
Above average rain
    No12/221.00
    Yes9/141.960.32, 11.90.464
Village sprayed
    No56/1071.00
    Yes23/690.230.10, 0.570.001*
Table 3

Multivariate logistic regression for household risk factors and parasitemia among 2,779 observations

Household risk factorCases/exposedOdds ratio95% CIP value
* Significant at P < 0.05.
Ecological strata
    Eastern escarpment31/6391.00
    Western escarpment36/7910.94
    Dry lowland60/7831.631.04, 2.540.033*
    Wet lowland54/2924.452.79, 7.090.0001*
Wall type
    Other105/18251.00
    Mud78/9221.601.15, 2.240.006*
Eaves
    Closed114/19451.00
    Open68/8031.170.84, 1.630.357
House sprayed
    No173/21331.00
    Yes12/5920.260.14, 0.480.0001*
House sprayed (within 6 months)
    No7/5101.00
    Yes5/825.011.47, 17.00.010*
Near river (< 500 m)
    No110/15411.00
    Yes76/12370.750.55, 1.030.076
Above average rain
    No36/4471.00
    Yes22/1782.911.32, 6.390.008*
Figure 1.
Figure 1.

(a) Administrative map of the six zobas in Eritrea and the distribution of villages surveyed; (b) the distribution of malaria prevalence among villages surveyed.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 72, 6; 10.4269/ajtmh.2005.72.682

Figure 2.
Figure 2.

Age and sex-specific prevalence rates by ecological strata.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 72, 6; 10.4269/ajtmh.2005.72.682

Authors’ addresses: David M. Sintasath, Johns Hopkins Bloomberg School of Public Health, 615 N. Wolfe Street, Box 1382, Baltimore, MD 21205, E-mail: dsintasa@jhsph.edu. Tewolde Gebremeskel, Ministry of Health, P.O. Box 212, Asmara, Eritrea, E-mail: tewolali@gemel.com.er. Matthew Lynch, Office of Health, Infectious Diseases, and Nutrition, Bureau for Global Health, Washington, DC 20523-3700, E-mail: mlynch@usaid.gov. Eckhard Kleinau, Gustavo Bretas, and Eugene Brantly, Environmental Health Project, 1611 N. Kent St, Ste 300, Arlington, VA 22209, E-mails: kleinauef@ehproject.org, gbretas@hotmail.com, epb@rti.org. Patricia M. Graves, 1400 W Oak St, Fort Collins, CO 80521, E-mail: patriciagraves@attglobal.net. Josephat Shililu, International Centre for Insect Physiology and Ecology (ICIPE), P.O. Box 30772, Nairobi, Kenya, E-mail: jshililu@icipe.org. John C. Beier, Global Public Health Program, University of Miami, South Campus, 12500 SW 152nd Street, Building B, Miami, FL 33177, E-mail: jbeier@med.miami.edu.

Acknowledgments: The authors thank all the technical staff and interviewers at the zobal and sub-zobal levels for conducting the field surveys. We acknowledge the valuable support from the staff at the Ministry of Health, including the Minister, Director General of Health Services, and Director of the Communicable Diseases and Control. Special thanks to Mehari Zerom, Fessahaye Seulu, Asmelash G/Ezgher, Helen Fekadu, and Solomon Mengistu who provided immense operational support and to Linda Lou Kelley, Team Leader for the Health Strengthening Office USAID/Eritrea.

Financial support: This work was supported by the Johns Hopkins University Health and Child Survival Fellows Program. This work is based on activities funded by USAID under the Environmental Health Project contract no. HRN-I-00-99-00011-00.

Disclaimer: The views expressed by the authors do not necessarily reflect the views of the U.S. Agency for International Development nor the U.S. Government generally.

REFERENCES

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    Ministry of Health, State of Eritrea. Eritrean Health Profile, 2000.

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    Ministry of Health, State of Eritrea. National Malaria Control Program 5-year RBM Strategic Plan of Action, Mendefera, 1998.

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    Shililu J, Ghebremeskel T, Seulu F, Mengistu S, Fekadu H, Zerom M, Ghebregziabiher A, Sintasath D, Bretas G, Mbogo C, Githure J, Brantly E, Novak R, Beier JC, 2003. Larval habitat diversity and ecology of Anopheline larvae in Eritrea. J Med Entomol 40 :921–929.

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    Shililu J, Ghebremeskel T, Mengistu S, Fekadu H, Zerom M, Mbogo C, Githure J, Gu W, Novak R, Beier JC, 2003. Distribution of anopheline mosquitoes in Eritrea. Am J Trop Med Hyg 69 :295–302.

    • Search Google Scholar
    • Export Citation
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