Anaemia, drought and malaria in Ethiopia

Gari T, Loha E, Deressa W, Solomon T, Atsbeha H, Assegid M, Hailu A, Lindtjørn B. (2017) Anaemia among children in a drought affected community in south-central Ethiopia. PLoS ONE 12(3): e0170898. doi:10.1371/journal.pone.0170898

Introduction  As part of a field trial (PACTR201411000882128) to provide evidence on the combined use of long-lasting insecticidal nets and indoor residual spray for malaria prevention, we measured haemoglobin values among children aged 6 to 59 months. The aim of this study was to estimate the prevalence of anaemia, and to determine the risk factors of anaemia and change in haemoglobin value in Adami Tullu district in south-central Ethiopia.

Methods  Repeated cross-sectional surveys among 2984 children in 2014 and 3128 children in 2015; and a cohort study (malaria as exposure and anaemia as outcome variable) were conducted. The study area faced severe drought and food shortages in 2015. Anaemia was diagnosed using HemoCue Hb 301, and children with haemoglobin <11 g/dl were classified as anaemic. Multilevel and Cox regression models were applied to assess predictors of anaemia.

Results  The prevalence of anaemia was 28.2% [95% Confidence Interval (CI), 26.6–29.8] in 2014 and increased to 36.8% (95% CI, 35.1–38.5) in 2015 (P<0.001). The incidence of anaemia was 30; (95% CI, 28–32) cases per 100 children years of observation. The risk of anaemia was high (adjusted Hazard Ratio = 10) among children with malaria. Children from poor families [Adjusted Odds Ratio (AOR); 1.3; 95% CI, 1.1–1.6)], stunted children (AOR 1.5; 95% CI; 1.2–1.8), and children aged less than 36 months (AOR; 2.0; 95% CI, 1.6–2.4) were at risk of anaemia compared to their counterparts. There was no significant difference in risk of anaemia among the trial arms.

Conclusions  Young age, stunting, malaria and poverty were the main predictors of anaemia. An increase in the prevalence of anaemia was observed over a year, despite malaria prevention effort, which could be related to the drought and food shortage. Therefore, conducting trials in settings prone to drought and famine may bring unexpected challenges.

Entomological evaluation of vector control


Kena, O. 2017. Entomological impact of combined and separate use of indoor residual spraying and long-lasting insecticidal nets for malaria prevention in Adami Tullu district, South-Central Ethiopia. PhD thesis. Addis Ababa University.

Indoor residual spraying (IRS) and long-lasting insecticidal nets (LLINs) are the key frontline malaria prevention interventions in Ethiopia. Both target Anopheles arabiensis, the sole primary malaria vector. Universal coverage of both interventions has been promoted and there is a growing demand in combination of interventions for malaria control and elimination. However, available evidence is contradictory wether the combined intervention is better than either IRS or LLINs alone. To investigate whether IRS and LLINs combination provides added protective impact on An. arabiensis compared to either IRS or LLINs alone, a cluster randomized controlled trial was carried out in Adami Tullu district, south-central Ethiopia. Villages were randomly allocated to four study arms: IRS+LLINs, IRS, LLINs, and control. All households in the IRS+LLINs and LLINs arms were provided with LLINs (PermaNet 2.0) free of charge. Households in the IRS+LLINs and IRS arms were applied with propoxur before the main malaria transmission season in 2014 and 2015. Adult mosquitoes were collected in randomly selected villages in each arm using CDC light trap catch (LTC) set close to a sleeping person, pyrethrum spray catch (PSC), and artificial pit shelter (PIT), for measuring host-seeking density (HSD), indoor resting density (IRD), and outdoor resting density (ORD) of the anophelines. Human landing catch (HLC) was performed in selected villages to monitor the impact of the interventions on local mosquito biting behaviours (biting location, time and host preference).

Collected anophelines were identified to species by use of standard morphological keys and additional use of molecular methods to separate sibling species of the An. gambiae complex. Enzyme-linked immunosorbent assay (ELISA) was used to detect malaria infections in mosquitoes and the sources of mosquito blood meals. Mean densities were compared using incidence rate ratio (IRR) calculated by negative binomial regression. Parity rate (percentage of parous females) was also determined by ovarial dissection. Human blood index (HBI) was expressed as the proportion of mosquitoes with human blood divided by the total number of blood-fed mosquitoes tested.

A total of 1786 female anophelines of four species (An. arabiensis, An. pharoensis, An. ziemanni and An. funestus s.l.) were collected over two transmission seasons during the intervention period (2014-2015). Anopheles numbers were highest in the control arm (41.3% of total) followed by LLINs (25.4%), IRS (18.0%), and IRS+LLINs (15.8%). In most of the vector parameters estimated, the impact of IRS and LLINs combined and separate interventions were significantly higher in communities that recieved the interventions (in experimental groups) compared with untreated communities (control group). The mean HSD of An. arabiensis in the IRS+LLINs arm was similar to the IRS arm (0.03 vs. 0.03/ house/LTC/night) but lower than the LLINs arm (0.03 vs. 0.10/house/LTC/night, p=0.07) and so was the difference in IRD and ORD between the IRS+LLINs compared to the IRS arm. However, both IRD and ORD of An. arabiensis were higher in LLINs compared to IRS+LLINs (p < 0.001 for indoors). Parity rate of An. arabiensis were similar among the intervention arms. None of the 1786 samples of four species tested by ELISA was positive for P.  falciparum and P. vivax CSP infection in all of the study arms. Anopheles arabiensis preferred mainly bovine and human hosts for blood meal sources with high HBI in the LLIN alone. Indoor resting habit of An. arabiensis was less impacted by LLINs alone intervention compared to IRS + LLINs or IRS alone.

In conclusion, the IRS+LLINs and the IRS alone each was similarly most effective against An. arabiensis as compared to the LLINs alone. The IRS+LLINs provided added impact on An. arabiensis compared to LLINs alone. The LLINs alone had poor impact on densities and human biting rates of An. arabiensis in this study setting.

You can download the thesis here: Oljira-Kenea-thesis

New PhD: Malaria vectors in southern Ethiopia

fekadu-cover-pageMassebo F. Malaria vectors in southern Ethiopia. Some challenges and opportunities for vector control. PhD. University of Bergen, 2017. Bergen

Background: Malaria is a public health problem in Ethiopia, where more than 60% of the population lives in risky areas. Since 2005, malaria-related sicknesses and deaths have substantially decreased in the country, mainly due to the increasing coverage of vector control interventions and chemotherapy. On the other hand, resistance to most public health insecticides is widely spreading among the populations of the principal malaria vector Anopheles arabiensis. Therefore, assessing the susceptibility status of local malaria vectors is an essential activity to improve the effectiveness of the interventions, by introducing the appropriate insecticide resistance management strategies. There are also substantial gaps in knowledge regarding the entomological inoculation rate (EIR), which is an indicator of the intensity of malaria transmission, and are used to assess the impact of vector control interventions. Understanding the species composition, feeding and resting behaviours, parity rate, as well as human biting and sporozoite rates, are all important in evaluating the effectiveness of interventions and planning for supplementary vector control tools. Moreover, improving housing, such as screen doors and windows, and closing openings on walls and eaves, might reduce the entry of malaria vectors and provide protection from infectious bites of malaria vectors.

Objective: The study was carried out to help assess the species composition, age structure, feeding patterns, sporozoite infection rate, entomological inoculation rate and insecticide susceptibility status of An. arabiensis, and evaluate the impact of screened houses on its indoor density.

Methods: The study was done in the Chano Mille Kebele in southwestern Ethiopia. The longitudinal entomological study was conducted from May 2009-April 2010, whereas the house screening intervention was done between April-November 2011. Thirty houses (10 houses for each collection method) were randomly selected for biweekly Anopheles mosquito sampling. The Anopheles mosquitoes were collected by the Centers for Disease Control and Prevention (CDC) light traps, pyrethrum spray catches (PSC) and from artificial pit shelters by aspirating. Enzyme-linked-immunosorbent assay (ELISA) was used to analyse the blood meal origins and circumsporozoite proteins. The EIR of P. falciparum and P. vivax of An. arabiensis was calculated by multiplying the sporozoite and human biting rates from CDC light traps and PSC collections.

A randomized control trial was conducted to assess the impact of screening windows and doors with wire mesh, and closing openings on eaves and walls by mud on the indoor density of An. arabiensis. Baseline mosquito data was gathered biweekly from 40 houses by CDC light traps in March and April 2011 to randomize houses into both control and intervention groups. The windows and doors of 20 houses were screened by mosquito-proof wire mesh, and openings on the walls and eaves were closed by mud. The rest of the 20 houses were assigned to the control group. Mosquitoes were collected biweekly in October and November 2011 from both the control and intervention houses.

Results: Anopheles species, comprised of An. arabiensis, An. marshalli, An. garnhami, An. funestus group, An. pharoensis, An. tenebrosus, An. rhodensiensis, An. flavicosta, An. longipalpis, An. daniculicus, An. pretoriensis, An. chrysti, An. moucheti, An. distinctus and An. zeimanni, were documented in the area. Anopheles arabiensis was by far the most dominant species.

The overall human blood index (HBI) of An. arabiensis, including the mixed blood meals, was 44%, whereas the bovine blood index (BBI), including mixed blood meals, was 69%. The majority of An. arabiensis (65%) from the indoor-resting collection had bovine blood meal, which was unexpected. The higher proportion (75%) of indoor host-seeking An. arabiensis collected by CDC light traps had contact with humans. Only 13% An. arabiensis from pit shelters had human blood meal, while 68% had bovine blood meal. Anopheles arabiensis showed a consistently higher feeding pattern on cattle than on humans, regardless of collection sites and the high number of the human population. The human and bovine feeding patterns of An. arabiensis showed little change due to the number of cattle to human ratio of each household. Anopheles marshalli and An. garnhami showed similar feeding patterns.

Anopheles arabiensis was highly resistant to four pyrethroid insecticides tested (lambdacyhalothrin, cyfluthrin, alphacypermethrin and deltamethrin) and DDT, with a maximum mortality rate of 56% due to lambdacyhalothrin and a minimum of 10% due to DDT.

The circumsporozoite protein ELISA test revealed 11 P. falciparum infections out of 14 sporozoite positive An. arabiensis (the other three were P. vivax), thereby confirming that this species is the principal vector of P. falciparum and P. vivax parasites. The P. falciparum sporozoite rate of An. arabiensis was 0.32% for CDC light traps, 0.28% for pit shelters and 0.23% for PSCs. The overall estimated annual P. falciparum EIR of An. arabiensis from CDC light traps was 17.1 infectious bites/person/year (ib/p/y), but it varied between houses, from a 0 EIR in 60% of houses to 73.2 in a house close to the major breeding site. Hence, those houses nearest to the mosquito breeding sites had a higher risk of exposure to infectious bites. The P. falciparum EIR of An. arabiensis was 2.4 in the dry season and 14.7 in the wet season, indicating 6.1-fold more infectious bites in the wet- than in the dry season. The P. falciparum and P. vivax EIR of An. arabiensis from PSC was 0.1ib/p/y, while the P. vivax EIR of An. arabiensis from CDC light traps was 2.41ib/p/y.

The screening of doors and windows with wire mesh, and closing the openings on eaves and walls by mud, significantly reduced the indoor density of host-seeking An. arabiensis by 40%. The intervention was cheap, and can be incorporated into malaria vector control programmes by local communities.

Conclusion: Anopheles arabiensis showed a consistently higher feeding pattern on cattle than on humans regardless of collection sites and the high number of human population. It was the most abundant and the principal vector of P. falciparum and P. vivax, while An. marshalli and An. garnhami were the second and third most abundant species, but neither of them was positive for CSPs. The transmission of malaria is heterogeneous; those houses nearest to the mosquito breeding sites (hot spots) had a higher risk of exposure to the infectious bites of An. arabiensis. Anopheles arabiensis was resistant to pyrethroid insecticides, the only class of insecticides recommended for LLINs treatment; as a result, there should be an action programme to manage insecticide resistance. Finally, supplementary methods of vector control, such as the screening of houses, could be included to help improve malaria control in the area based on the principle of integrated vector management.

The thesis can be downloaded here.

Strengthening malaria and climate research in Ethiopia

Lindtjorn-Malaria conference posterLindtjorn B, Loha E, Deressa W, Balkew M, Gebremichael T, Sorteberg A, Woyessa A, Animut A, Diriba K, Massebo F, et al: Strengthening malaria and climate research in Ethiopia. Malaria Journal 2014, 13:P56.

Poster presentation

The project “Ethiopian Malaria Prediction System” implemented from 2007 to 2012 combined new population-based malaria transmission information with climate and land use variability data to develop an early warning tool to predict malaria epidemics in Ethiopia. Scientists from Ethiopia and Norway collaborated to incorporate climate variability and forecast information for malaria epidemics.

Our study shows that the association between weather and malaria is complex. Statistical models can predict malaria for large areas. However, as malaria transmission varies and depends on local environmental conditions, we need to have good and local knowledge about each area. However, weather variability is the main driver of malaria in Ethiopia.

While the generation of precipitation depends on local ascent and cooling of the air, our research provided new data on the transport of moisture into the country that may improve weather forecasting. We developed a new classification of climate zones, have mapped drought episodes in Ethiopia during the last decades, and have improved seasonal weather forecasting. Our hydrology studies show that potential climate change differs among the Ethiopian river basins, with river flows being sensitive to variations in rainfall, and less to temperature changes.

The computer model, Open Malaria Warning, incorporates hydrological, meteorological, mosquito-breeding, land-use data, and cattle densities to find out when and where outbreaks are likely to occur. We validated the model with data for malaria transmission in the highlands and lowlands, characterizing malaria transmission over some years in both highlands and lowlands. This provided us with new knowledge on malaria transmission in Ethiopia, how intense the seasonal transmission is, and how malaria occurs in different populations and areas. Our study showed that indigenous malaria transmission during a non-epidemic year takes place above 2000 m altitude. We also showed the ideal temperature for malaria transmission is about 25°C, underlining that global warming may lead to increased risk of malaria in highland areas, and less in the lowlands with already high average temperatures. However, to validate such models, there is a need for several years of active monitoring of malaria cases and mosquito densities. Unfortunately, such data is rare in Africa, and we need to invest in long-term monitoring of malaria transmission.

Lindtjorn-Malaria conference poster

Climate, food production and malnutrition

Seifu Hagos, Torleif Lunde, Damen H Mariam, Tassew Woldehanna and Bernt Lindtjørn. Climate change, crop production and child under nutrition in Ethiopia; a longitudinal panel study. BMC Public Health 2014, 14:884 doi:10.1186/1471-2458-14-884

Background  The amount and distribution of rainfall and temperature influences household food availability, thus increasing the risk of child undernutrition. However, few studies examined the local spatial variability and the impact of temperature and rainfall on child undernutrition at a smaller scale (resolution). We conducted this study to evaluate the effect of weather variables on child under nutrition and the variations in effects across the three agroecologies of Ethiopia.

Methods  A longitudinal panel study was conducted. We used crop productions (cereals and oilseeds), livestock, monthly rainfall and temperature, and child under nutrition data for the period of 1996, 1998, 2000 and 2004. We applied panel regression fixed effects model.

Results  The study included 43 clusters (administrative zones) and 145 observations. We observed a spatiotemporal variability of rainfall, stunting and underweight. We estimated that for a given zone, one standard deviation increase in rainfall leads to 0.242 standard deviations increase in moderate stunting. Additionally, a one standard deviation increase temperature leads to 0.216 standard deviations decrease in moderate stunting. However, wasting was found to be poorly related with rainfall and temperature. But severe wasting showed a positive relationship with the quadratic term of rainfall.

Conclusions  We conclude that rainfall and temperature are partly predicting the variation in child stunting and underweight. Models vary in predicting stunting and underweight across the three agroecologic zones. This could indicate that a single model for the three agroecologies may not be not applicable.

Ownership and use of long-lasting insecticidal nets for malaria prevention in Ethiopia

Woyessa A, Deressa W, Ali A, Lindtjorn B. Ownership and use of long-lasting insecticidal nets for malaria prevention in Butajira area, south-central Ethiopia: complex samples data analysis. BMC public health 2014; 14: 99.

BACKGROUND: Despite the encroaching of endemic malaria to highland-fringe areas above 2000 meters above sea level in Ethiopia, there is limited information on ownership and use of mosquito nets for malaria prevention. Thus, this study was designed to assess long-lasting insecticidal nets (LLIN) possession and use for malaria prevention in highland-fringe of south-central Ethiopia.

METHODS: A multi-stage sampling technique was employed to obtain household data from randomly selected households using household head interview in October and November 2008. Household LLIN possession and use was assessed using adjusted Odds Ratio obtained from complexsamples logistic regression analysis.

RESULTS: Only less than a quarter (23.1%) of 739 households interviewed owned LLINs with more differences between low (54.2%) high (3.5%) altitudes (Χ2 =253, P < 0.001). Higher LLIN ownership was observed in illiterate (adj.OR 35.1 [10.6-116.2]), male-headed (adj.OR 1.7 [1.051-2.89]), owning two or more beds (adj.OR 2.7 [1.6-4.6]), not doing draining/refilling of mosquito breeding sites (adj.OR 3.4 [2.1-5.5]) and absence of rivers or streams (adj.OR 6.4 [3.5-11.8]) of household variables. The presence of ≥2 LLINs hanging (adj.OR 21.0 [5.2-85.1]), owning two or more LLINs (adj.OR 4.8 [1.3-17.5]), not doing draining/refilling of mosquito breeding sites (adj.OR 4.2 [1.3-13.6]), low wealth status (adj.OR 3.55 [1.04-12.14]), and < 1 km distance from absence of rivers or streams (adj.OR 3.9 [1.2-12.1]) of households was associated with more likely use of LLIN. The LLIN ownership was low in the highlands, and most of the highland users bought the bed nets themselves.

CONCLUSIONS: This study found a low household LLIN ownership and use in the highland-fringe rural area. Therefore, improving the availability and teaching effective use of LLIN combined with removal of temporary mosquito breeding places should be prioritized in highland-fringe areas.

Eskindir Loha defended his PhD thesis

On Tuesday September 3, 2013, Eskindir Loha defended his PhD thesis.

The title of the work is: “Variation in malaria transmission in southern Ethiopia: The impact of prevention strategies and a need for targeted intervention”.

Summary of Thesis

In Ethiopia, 60 per cent of the population is at risk of malaria. The transmission of the disease is unstable, and hence, the possibility of epidemics demanded continuous vigilance and preparedness of the health system. Meanwhile, the complexity of the transmission of the disease has become an impediment to retain the effectiveness of prevention and control strategies. Understanding factors that play role in disease transmission at different locations, the pattern of disease transmission, the impact of prevention and control strategies and challenges in control efforts were deemed crucial for the way forward.

This thesis analysed the local variations in the link between potential determinants of transmission – meteorological factors and malaria incidence. For this, we used datasets from 35 locations found in the Southern Nations and Nationalities People’s Region and registered within the period 1998 to 2007. The findings implied that the variability in the models to be principally attributed to regional differences, and a single model that fits all locations was not found. Although there is a biological link between meteorological factors and malaria transmission, the link is affected by local conditions and non-meteorological factors.

With the understanding of a need to incorporate non-meteorological factors, in an attempt to predict disease incidence, a detailed investigation was carried out in Chano Mille Kebele – one of the malarious Kebeles of Arba Minch Zuria district, Gamo Gofa zone, south Ethiopia. A prospective cohort study was conducted for two years with a weekly visit to each of 1,388 households. The findings showed that rainfall increased and indoor residual spraying with Deltamethrin reduced falciparum malaria incidence. Higher disease incidence was observed among males, children 5–14 years old, insecticide-treated net non-users, the poor, and people who lived closer to vector breeding site. Meanwhile, we identified spatio-temporal clusters of high disease rates within a 2.4 area of the Kebele.

Mass distribution of insecticide-treated nets neither showed community-wide benefit nor influenced the spatio-temporal clustering of malaria, though proved to be protective at the individual level. Further analysis on insecticide-treated nets showed that the proportion of insecticide-treated net use reached a maximum of 69 per cent despite a near universal coverage (98.4 per cent) was achieved. Sleeping under the insecticide-treated nets was influenced by gender, age and proximity to the vector breeding site. Factor compromising the usable life of insecticide-treated nets and a lack of convenient space to hang more than one net were reported.

The local variations in meteorology-malaria link, the heterogeneous risk carried by different population segments and the observed effect of prevention strategies may help to revisit the approaches towards malaria – for which I forwarded specific recommendations.

Two new malaria articles

Our malaria research group recently published two new articles about malaria in south Ethiopia:

Massebo F, Balkew M, Gebre-Michael T, Lindtjorn B. Entomologic Inoculation Rates of Anopheles arabiensis in Southwestern Ethiopia. Am J Trop Med Hyg 2013.

Woyessa A, Deressa W, Ali A, Lindtjørn B. Malaria risk factors in Butajira area, south-central Ethiopia: a multilevel analysis. Malaria Journal 2013, 12:273.