Costs and cost-effectiveness of vector control in Eritrea using insecticide-treated bed nets.

BACKGROUND: While insecticide-treated nets (ITNs) are a recognized effective method for preventing malaria, there has been an extensive debate in recent years about the best large-scale implementation strategy. Implementation costs and cost-effectiveness are important elements to consider when planning ITN programmes, but so far little information on these aspects is available from national programmes. METHODS: This study uses a standardized methodology, as part of a larger comparative study, to collect cost data and cost-effectiveness estimates from a large programme providing ITNs at the community level and ante-natal care facilities in Eritrea. This is a unique model of ITN implementation fully integrated into the public health system. RESULTS: Base case analysis results indicated that the average annual cost of ITN delivery (2005 USD 3.98) was very attractive when compared with past ITN delivery studies at different scales. Financing was largely from donor sources though the Eritrean government and net users also contributed funding. The intervention's cost-effectiveness was in a highly attractive range for sub-Saharan Africa. The cost per DALY averted was USD 13 - 44. The cost per death averted was USD 438-1449. Distribution of nets coincided with significant increases in coverage and usage of nets nationwide, approaching or exceeding international targets in some areas. CONCLUSION: ITNs can be cost-effectively delivered at a large scale in sub-Saharan Africa through a distribution system that is highly integrated into the health system. Operating and sustaining such a system still requires strong donor funding and support as well as a functional and extensive system of health facilities and community health workers already in place.

Effectiveness of malaria control during changing climate conditions in Eritrea, 1998-2003.

OBJECTIVE: To assess the effectiveness of impregnated mosquito nets, indoor residual spraying and larval control relative to the impacts of climate variability in the decline of malaria cases in Eritrea. METHODS: Monthly data on clinical malaria cases by subzoba (district) in three zobas (zones) of Eritrea for 1998-2003 were used in Poisson regression models to determine whether there is statistical evidence for reduction in cases by DDT, malathion, impregnated nets and larval control used over the period, while analysing the effects of satellite-derived climate variables in the same geographic areas. RESULTS: Both indoor residual spraying (with DDT or malathion) and impregnated nets were independently and significantly negatively associated with reduction in malaria cases, as was larval control in one zoba. Malaria cases were significantly positively related to differences in current and previous months' vegetation (NDVI) anomalies. The relationship to rainfall differences 2 and 3 months previously was also significant, but the direction of the effect varied by zoba. Standardized regression coefficients indicated a greater effect of climate in the zoba with less intense malaria transmission. CONCLUSION: The results support the view that both indoor residual spraying and impregnated nets have been independently effective against malaria, and that larval control was also effective in one area. Thus climate, while significant, is not the only explanation for the recent decline in malaria cases in Eritrea. If appropriate statistical approaches are used, routine surveillance data from cases attending health facilities can be useful for assessing control programme success and providing estimates of the effectiveness of individual control measures. Effectiveness estimates suitable for use in cost-effectiveness analysis have been obtained.

Costs and consequences of large-scale vector control for malaria.

BACKGROUND: Five large insecticide-treated net (ITN) programmes and two indoor residual spraying (IRS) programmes were compared using a standardized costing methodology. METHODS: Costs were measured locally or derived from existing studies and focused on the provider perspective, but included the direct costs of net purchases by users, and are reported in 2005 USD. Effectiveness was estimated by combining programme outputs with standard impact indicators. FINDINGS: Conventional ITNs: The cost per treated net-year of protection ranged from USD 1.21 in Eritrea to USD 6.05 in Senegal. The cost per child death averted ranged from USD 438 to USD 2,199 when targeting to children was successful.Long-lasting insecticidal nets (LLIN) of five years duration: The cost per treated-net year of protection ranged from USD 1.38 in Eritrea to USD 1.90 in Togo. The cost per child death averted ranged from USD 502 to USD 692.IRS: The costs per person-year of protection for all ages were USD 3.27 in KwaZulu Natal and USD 3.90 in Mozambique. If only children under five years of age were included in the denominator the cost per person-year of protection was higher: USD 23.96 and USD 21.63. As a result, the cost per child death averted was higher than for ITNs: USD 3,933-4,357. CONCLUSION: Both ITNs and IRS are highly cost-effective vector control strategies. Integrated ITN free distribution campaigns appeared to be the most efficient way to rapidly increase ITN coverage. Other approaches were as or more cost-effective, and appeared better suited to "keep-up" coverage levels. ITNs are more cost-effective than IRS for highly endemic settings, especially if high ITN coverage can be achieved with some demographic targeting.

Mosquito larval habitats in a semiarid ecosystem in Eritrea: impact of larval habitat management on Anopheles arabiensis population.

This study investigated the impact of larval management and the temporal variation in larval productivity in Eritrea, a semiarid ecosystem. Results of this study show that mosquito breeding persists throughout the year mainly in stream bed pools. Anopheles arabiensis production in the ephemeral natural aquatic habitats such the streambed pools was high throughout the year and negatively associated with rainfall (r = -0.288, P = 0.047). High densities of An. arabiensis larvae were also recorded from canals and drainage channels at wells and communal water supply points. The numerous water supply locations and wells help sustain malaria transmission by serving as sources of anophelines where people aggregate. There was a strong association between larval production and adult emergent densities (r = 0.365, P = 0.011). The results of this study further show that implementation of larval control strategies in the study villages significantly reduced vector productivity as measured by both larval (F = 24.919, df = 1,178, P < 0.001) and adult An. arabiensis densities (F = 3.052, df = 1,119, P = 0.014) in the treated sites over the 24-month study period. The results of this semiarid larval management model suggests that 1) larval management backed by habitat identification, mapping, and surveillance is a feasible tactic for managing malaria vectors, 2) a special focus in such semiarid ecosystems should be targeted to the highly productive larval habitats along stream beds and others of periodic importance derived from human activities, and 3) public information and sensitization of communities to participate in controlling the pre-adult stages of anopheline mosquitoes is central for success.

Malaria stratification, climate, and epidemic early warning in Eritrea.

Eritrea has a successful malaria control program, but it is still susceptible to devastating malaria epidemics. Monthly data on clinical malaria cases from 242 health facilities in 58 subzobas (districts) of Eritrea from 1996 to 2003 were used in a novel stratification process using principal component analysis and nonhierarchical clustering to define five areas with distinct malaria intensity and seasonality patterns, to guide future interventions and development of an epidemic early warning system. Relationships between monthly clinical malaria incidence by subzoba and monthly climate data from several sources, and with seasonal climate forecasts, were investigated. Remotely sensed climate data were averaged over the same subzoba geographic administrative units as the malaria cases. Although correlation was good between malaria anomalies and actual rainfall from ground stations (lagged by 2 months), the stations did not have sufficiently even coverage to be widely useful. Satellite derived rainfall from the Climate Prediction Center Merged Analysis of Precipitation was correlated with malaria incidence anomalies, with a lead time of 2-3 months. NDVI anomalies were highly correlated with malaria incidence anomalies, particularly in the semi-arid north of the country and along the northern Red Sea coast, which is a highly epidemic-prone area. Eritrea has 2 distinct rainy seasons in different parts of the country. The seasonal forecasting skill from Global Circulation Models for the June/July/August season was low except for the Eastern border. For the coastal October/November/December season, forecasting skill was good only during the 1997-1998 El Niño event. For epidemic control, shorter-range warning based on remotely sensed rainfall estimates and an enhanced epidemic early-detection system based on data derived for this study are needed.

Interpreting household survey data intended to measure insecticide-treated bednet coverage: results from two surveys in Eritrea.

BACKGROUND: As efforts are currently underway to roll-out insecticide-treated bednets (ITNs) to populations within malarious areas in Africa, there is an unprecedented need for data to measure the effectiveness of such programmes in terms of population coverage. This paper examines methodological issues to using household surveys to measure core Roll Back Malaria coverage indicators of ITN possession and use. METHODS: ITN coverage estimates within Anseba and Gash Barka Provinces from the 2002 Eritrean Demographic and Health Survey, implemented just prior to a large-scale ITN distribution programme, are compared to estimates from the same area from a sub-national Bednet Survey implemented 18 months later in 2003 after the roll-out of the ITN programme. RESULTS: Measures of bednet possession were dramatically higher in 2003 compared to 2002. In 2003, 82.2% (95% confidence interval (CI) 77.4-87.0) of households in Anseba and Gash Barka possessed at least one ITN. RBM coverage indicators for ITN use were also dramatically higher in 2003 as compared to 2002, with 76.1% (95% CI 69.9-82.2) of children under five years old and 52.4% (95% CI 38.2-66.6) of pregnant women sleeping under ITNs. The ITN distribution programme resulted in a gross increase in ITN use among children and pregnant women of 68.3% and 48% respectively. CONCLUSION: Eritrea has exceeded the Abuja targets of 60% coverage for ITN household possession and use among children under five years old within two malarious provinces. Results point to several important potential sources of bias that must be considered when interpreting data for ITN coverage over time, including: disparate survey universes and target populations that may include non-malarious areas; poor date recall of bednet procurement and treatment; and differences in timing of surveys with respect to malaria season.

Malaria prevalence and associated risk factors in Eritrea.

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.

Distribution of anopheline mosquitoes in Eritrea.

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.

High seasonal variation in entomologic inoculation rates in Eritrea, a semi-arid region of unstable malaria in Africa.

Entomologic studies were conducted in eight villages to investigate the patterns of malaria transmission in different ecologic zones in Eritrea. Mosquito collections were conducted for 24 months between September 1999 and January 2002. The biting rates of Anopheles arabiensis were highly seasonal, with activity concentrated in the wet season between June and October in the highlands and western lowlands, and between December and March in the coastal region. The biting rates in the western lowlands were twice as high as in the western escarpment and 20 times higher than in the coastal region. Sporozoite rates were not significantly different among villages. The risk of infection ranged from zero on the coast to 70.6 infective bites per year in the western lowlands. The number of days it would take for an individual to receive an infective bite from an infected An. arabiensis was variable among villages (range = 2.8-203.1 days). The data revealed the presence of only one main malaria transmission period between July and October for the highlands and western lowlands. Peak inoculation rates were recorded in August and September (range = 0.29-43.6 infective bits/person/month) at all sites over the two-year period. The annual entomologic inoculation rates (EIRs) varied greatly depending on year. The EIR profiles indicated that the risk of exposure to infected mosquitoes is highly heterogeneous and seasonal, with high inoculation rates during the rainy season, and with little or no transmission during the dry season. This study demonstrates the need to generate spatial and temporal data on transmission intensity on smaller scales to guide targeted control of malaria operations in semi-arid regions. Furthermore, EIR estimates derived in the present study provide a means of quantifying levels of exposure to infected mosquitoes in different regions of the country and could be important for evaluating the efficacy of vector control measures, since Eritrea has made significant steps in reducing the burden of malaria based on the Roll Back Malaria initiative of the World Health Organization.

Larval habitat diversity and ecology of anopheline larvae in Eritrea.

Studies on the spatial distribution of anopheline mosquito larvae were conducted in 302 villages over two transmission seasons in Eritrea. Additional longitudinal studies were also conducted at eight villages over a 24-mo period to determine the seasonal variation in anopheline larval densities. Eight anopheline species were identified with Anopheles arabiensis predominating in most of the habitats. Other species collected included: An. cinereus, An. pretoriensis, An. d'thali, An. funestus, An. squamosus, An. adenensis, and An. demeilloni. An. arabiensis was found in five of the six aquatic habitats found positive for anopheline larvae during the survey. Anopheles larvae were sampled predominantly from stream edges and streambed pools, with samples from this habitat type representing 91.2% (n = 9481) of the total anopheline larval collection in the spatial distribution survey. Other important anopheline habitats included rain pools, ponds, dams, swamps, and drainage channels at communal water supply points. Anopheline larvae were abundant in habitats that were shallow, slow flowing and had clear water. The presence of vegetation, intensity of shade, and permanence of aquatic habitats were not significant determinants of larval distribution and abundance. Larval density was positively correlated with water temperature. Larval abundance increased during the wet season and decreased in the dry season but the timing of peak densities was variable among habitat types and zones. Anopheline larvae were collected all year round with the dry season larval production restricted mainly to artificial aquatic habitats such as drainage channels at communal water supply points. This study provides important information on seasonal patterns of anopheline larval production and larval habitat diversity on a countrywide scale that will be useful in guiding larval control operations in Eritrea.

Seasonal abundance, vector behavior, and malaria parasite transmission in Eritrea.

Entomological studies were conducted over a 24-month period in 8 villages to establish the behavior patterns, seasonal densities, and variation in entomological inoculation rates (EIRs) of Anopheles arabiensis, the main vector of malaria in Eritrea. A total of 5,683 anopheline mosquitoes were collected through indoor sampling (1,613), human-landing catches (2,711), and outdoor pit shelters (1,359). Overall, An. arabiensis was the predominant species at all of the study sites, with its population density increasing during the rainy season. Peak indoor-resting densities was observed during September and October. Human landing indices for An. arabiensis averaged 1.9 and 3.8 per person per night in October and September, respectively. Peak biting and landing rates occurred between 2000-2200 h and 0100-0300 h. Of the total number of bites, 44.7% occurred between 1800 and 2300 h, and at least 56.5% of the total bites occurred outdoors, indicating that the species was partially exophagic. The fed to gravid ratio for An. arabiensis in indoor-resting collections was 2:1, indicating some degree of exophily. The sporozoite rates (SRs) for An. arabiensis ranged from 0.54% in the Anseba zone to 1.3% in the Gash-Barka zone. One mosquito each of An. d'thali (SR = 0.45%) and An. cinereus (SR = 2.13%) was found to be positive. Of the total positive An. arabiensis (n = 64), 18.2% came from human-landing collections outdoors. Blood-meal analysis by enzyme-linked immunosorbent assay for An. arabiensis indicated that this species was partially zoophilic with a human to bovine ratio of 2:1 being recorded. The EIR profiles indicated that malaria transmission is highly seasonal, increasing during the wet season and declining drastically during the dry season. On average, the greatest risk of infection occurs in Hiletsidi, in the Gash-Barka zone (6.5 infective bites per month). The exophilic behavior and early evening biting of An. arabiensis present obstacles for control with treated bed-nets and indoor residual spraying within the context of integrated malaria control, and call for greater focus on strategies such as larval control.

Evaluating indoor residual spray for reducing malaria infection prevalence in Eritrea: results from a community randomized control trial.

This paper examines the relationship between indoor residual spray (IRS) and malaria parasite infection in Gash Barka Zone, Eritrea, an area with near universal coverage of insecticide treated bednets (ITN) and already low malaria parasite prevalence. A community randomized control trial was conducted in 2009. Malaria parasite infection prevalence was 0.5% [95% confidence interval (CI): 0.37-0.78%], with no significant difference detected between treatment and control areas. ITN possession remains high, with over 70% of households reporting ITN ownership [95% CI: 68.4-72.9]. ITN use among individuals within ITN-owning households was just under half [46.7% (95% CI: 45.4-48.0)]. Slight differences in ITN possession and use were detected between treatment and control areas. There was no significant difference in malaria parasite infection prevalence among individuals in households with ≥1 ITN compared to those in households without ITNs, nor among individuals reporting ITN use. Among individuals in ITN-owning households, sleeping under an ITN offered no statistically significant protection from malaria parasite infection. Community participation in environmental and larval habitat management activities was low: 17.9% (95% CI: 16.0-19.7). It is likely that IRS, larval habitat management and ITN distribution alone may be insufficient to interrupt transmission without corresponding high ITN use, sustained IRS application in areas where infections are clustered, and promptly seeking laboratory diagnosis and treatment of all fevers. Eritrea is ready for elimination, irrespective of inconclusive impact evaluation results.

Rolling out insecticide treated nets in Eritrea: examining the determinants of possession and use in malarious zones during the rainy season.

OBJECTIVE: This paper describes determinants of insecticide treated net (ITN) ownership and use in malarious areas of Eritrea. With ITN distribution and re-treatment now free for all living in these areas, we examine barriers (other than cost) to access and use of ITNs. We explore the differences between use of an ITN as a proportion of all households in the survey (the roll back malaria indicator), and use of an ITN as a proportion of those households who already own an ITN. METHODS: A modified two-stage cluster design was used to collect data from a sample of households (n = 2341) in the three most malarious administrative zobas (zones or provinces). Logistic regression was used to analyse the data. RESULTS: Our findings suggest environmental heterogeneity among zobas (including program effects specific to each zoba), perception of risk, and proximity to a clinic are important predictors of ITN possession and use. Among households with at least one ITN, 17.0% reported that children under five were not under an ITN the night before the survey, while half of all such households did not have all occupants using them the night before the survey. The number of ITNs, as well as zoba, was also significant determinants of use in these households with at least one ITN. CONCLUSION: Current efforts to disseminate ITNs to vulnerable populations in Eritrea are working, as suggested by high ITN ownership and net-to-person ratios inside households. However, the gap between ITN ownership and use, given ownership, is large, and may represent lost opportunities to prevent infection. Closing this gap requires concerted efforts to change behaviour to ensure that all household members use ITNs as consistently and correctly as possible during and following the rains.