Malaria transmission at high altitudes in Ethiopia

Daygena TY, Massebo F, Lindtjorn B. Variation in species composition and infection rates of Anopheles mosquitoes at different altitudinal transects, and the risk of malaria in the highland of Dirashe Woreda, south Ethiopia. Parasites & vectors. 2017;10(1):343.

Background  The transmission of malaria is heterogeneous, and varies due to altitude. The information on whether the transmission of malaria is indigenous or imported to highland areas is scarce. Therefore, this study aimed to assess the species composition and infection rates of Anopheles at different altitudinal transects, and the risk of malaria if any in the highland of Dirashe Woreda, South Ethiopia.

Methods  This study was conducted in Gato (low altitude; average elevation of 1273 m), Onota (mid-altitude; average elevation of 1707 m) and Layignaw-Arguba (high altitude; average elevation of 2337 m) from August 2015 to April 2016. Anopheles mosquitoes were sampled using Centers for Disease Control and Prevention (CDC) light traps from thirty houses (ten houses from each village). The circum-sporozoite proteins (CSPs) rate and entomological inoculation rate (EIR) of Anopheles mosquitoes were estimated. For the epidemiological survey, malaria cases were collected from laboratory registration books of selected health facilities from (August 2015-April 2016). A cross-sectional survey was done to collect data on malaria vector control activities in each village (August-September 2015).

Results  One thousand two hundred sixty-eight Anopheles mosquitoes comprising Anopheles arabiensis, An. demeilloni, An. cinereus, An. pharoensis, An. funestus-group, An. pretoriensis, An. christyi, An. ardensis and An. tenebrosus were identified in the study area. Anopheles arabiensis was the dominant species in Gato, whereas An. demeilloni was the dominant species in Layignaw-Arguba. Five mosquitoes, three An. arabiensis from Gato and two An. demeilloni from Layignaw-Arguba, were positive for Plasmodium falciparum CSPs. Plasmodium falciparum CSP rate was 0.4% (95% CI: 0.08–1.15) for An. arabiensis in Gato, and it was 0.64% (95% CI: 0.08–2.3) for An. demeilloni from Layignaw-Arguba. The P. falciparum EIR of An. arabiensis was 8.6 (95% CI: 2.4–33.4) infectious bites/person/nine-months in Gato. Plasmodium falciparum was dominant in Gato (88%) and Onota (57.5%), whereas in Layignaw-Arguba P. vivax (59.4%) occurred most frequently. Increased malaria cases were observed in children age 5–14 years in Gato (P < 0.05), whereas in Onota and Layignaw-Arguba there was no statistically significant difference in malaria cases among the age groups. Households owning at least one long lasting insecticidal net were 92.7% in the study area, and 77.6% slept under the net during the preceding night of the survey. About 64.4% of the households in Gato were protected by the indoor residual spray. However, the spraying was done when the density of local malaria vectors was low.

Conclusion  Incrimination of Plasmodium CSP positive Anopheles species and the presence of malaria in children under five years in high altitude Layignaw-Arguba may justify the existence of indigenous malaria transmission and the need for effective malaria control. Further investigation and confirmation using more sensitive molecular techniques are however needed to consider An. demeilloni as a proven vector of malaria in Ethiopia.

Residual malaria transmission

Abraham M, Massebo F, Lindtjørn B: High entomological inoculation rate of malaria vectors in area of high coverage of interventions in southwest Ethiopia: Implication for residual malaria transmission. Parasite Epidemiology and Control 2017, 2:61-69.

In Ethiopia, vector control is the principal strategy to reduce the burden of malaria. The entomological indicators of malaria transmission such as density, sporozoite rate and entomological inoculation rate (EIR) are parameters used to assess the impact of the interventions and the intensity of malaria transmission. The susceptibility of malaria vectors also determines the effectiveness of insecticide based vector control tools. Hence, the aim of the study was to assess the species composition, sporozoite rate and EIR, and insecticide susceptibility status of malaria vectors.

33 houses (18 for Centre for Disease Control and Prevention (CDC) light traps and 15 for exit traps) were randomly selected to sample Anopheles mosquitoes from October 2015 to May 2016. Plasmodium circum-sporozoite proteins (CSPs) of An. arabiensis and An. pharoensis were determined using Enzyme-Linked Immuno-Sorbent Assay (ELISA).

Five Anopheles species were identified from CDC Light traps and exit traps. An. arabiensis (80.2%) was the predominant species, followed by An. pharoensis (18.5%). An. pretoriensis, An. tenebrosus and An. rhodesiensis were documented in small numbers. 1056 Anopheles mosquitoes were tested for CSPs. Of which nine (eight An. arabiensis and one An. pharoensis) were positive for CSPs with an overall CSP rate of 0.85% (95% CI: 0.3–1.4). Five Anopheles mosquitoes were positive for P. falciparumand four were positive for P.vivax_210. P. falciparum CSP rate of An. arabiensis was 0.46% (95% CI: 0.13–1.2) and it was 0.54% (95% CI: 0.01–2.9) for An. pharoensis. The overall EIR of An. arabiensis was 5.3 infectious bites per/person (ib/p)/eight months. An. arabiensis was resistant to dieldrin (mortality rate of 57%) and deltamethrin with mortality rates of 71% but was fully susceptible to propoxur and bendiocarb. Based on the EIR of An. arabiensis, indoor malaria transmission was high regardless of high coverage of indoor-based interventions.

Finally, there was an indoor residual malaria transmission in a village of high coverage of bed nets and where the principal malaria vector is susceptibility to propoxur and bendiocarb; insecticides currently in use for indoor residual spraying. The continuing indoor transmission of malaria in such village implies the need for new tools to supplement the existing interventions and to reduce indoor malaria transmission.

New PhD: Malaria vectors in southern Ethiopia


Massebo 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.

Highland malaria in Ethiopia

Abebe Animut Ayele defenAbebe [1]ds on Friday 15 January 2016 his PhD degree at the University of Bergen with a dissertation:

“Anopheles species and malaria transmission risk in a highland area, south-central Ethiopia.” 

Anopheles arabiensis is the primary malaria vector in the lowlands of Ethiopia. In the highland Butajira area, a typical area of highland Ethiopia, the entomological aspects of the disease remain poorly described.

The study describes the entomological aspects of malaria transmission by highlighting on the abundance, host feeding preferences, entomological inoculation rates (EIRs) and risk of households’ exposure to malaria infectious Anopheles bites over two years. The study was done at three different altitudes ranging from 1800 to 2300 m.

Ten species of larval stages and nine species of adult stages of anophelines occurred in the area. The streams were the main breeding habitats of the anophelines. Anopheles arabiensis was the most prevalent species, and was found to feed on human and cattle with a similar preference. Plasmodium falciparum and Plasmodium vivax infected Anopheles arabiensis and Plasmodium vivax infected Anopheles pharoensis were caught in the low- and mid-altitude villages. Also, houses with open eaves had higher density of malaria infectious Anopheles arabiensis.

Abebe Animut Ayele was born in 1968 in Gojjam in Ethiopia. He completed his bachelor’s degree in biology and his master’s degree in medical parasitology from Addis Ababa University where he works as a lecturer. He started his PhD training at the Centre for International Health, University of Bergen in 2008 with Professor Bernt Lindtjørn as main supervisor and Associate Professor Teshome Gebre-Michael as co-supervisor.

Abebe-coverThe thesis can be downloaded here 

The publications in his thesis include:

Animut A, Gebre-Michael T, Balkew M, Lindtjorn B. Abundance and dynamics of anopheline larvae in a highland malarious area of south-central Ethiopia. Parasit Vectors. 2012;5:117.

Animut A, Balkew M, Gebre-Michael T, Lindtjorn B. Blood meal sources and entomological inoculation rates of anophelines along a highland altitudinal transect in south-central Ethiopia. Malar J 2013; 12(1): 76.

Animut A, Balkew M, Lindtjorn B. Impact of housing condition on indoor-biting and indoor-resting Anopheles arabiensis density in a highland area, central Ethiopia. Malaria journal 2013;12(1):393.

Cattle and Control of Malaria

Massebo F, Balkew M, Gebre-Michael T, Lindtjorn B. Zoophagic behaviour of anopheline mosquitoes in southwest Ethiopia: opportunity for malaria vector control. Parasites & vectors 2015; 8(1): 645.


Increased understanding of the feeding behaviours of malaria vectors is important to determine the frequency of human-vector contact and to implement effective vector control interventions. Here we assess the relative feeding preferences of Anopheles mosquitoes in relation to cattle and human host abundance in southwest Ethiopia.


We collected female Anopheles mosquitoes bi-weekly using Centers for Disease Control and prevention (CDC) light traps, pyrethrum spray catches (PSCs) and by aspirating from artificial pit shelters, and determined mosquito blood meal origins using a direct enzyme-linked immunosorbent assay (ELISA).


Both Anopheles arabiensis Patton and An. marshalli (Theobald) showed preference of bovine blood meal over humans regardless of higher human population sizes. The relative feeding preference of An. arabiensis on bovine blood meal was 4.7 times higher than that of human blood. Anopheles marshalli was 6 times more likely to feed on bovine blood meal than humans. The HBI of An. arabiensis and An. marshalli significantly varied between the collection methods, whereas the bovine feeding patterns was not substantially influenced by collection methods. Even though the highest HBI of An. arabiensis and An. marshalli was from indoor CDC traps collections, a substantial number of An. arabiensis (65 %) and An. marshalli (63 %) had contact with cattle. Anopheles arabiensis (44 %) and An. marshalli (41 %) had clearly taken bovine blood meals outdoors, but they rested indoors.


Anopheles mosquitoes are zoophagic and mainly feed on bovine blood meals than humans. Hence, it is important to consider treatment of cattle with appropriate insecticide to control the zoophagic malaria vectors in southwest Ethiopia. Systemic insecticides like ivermectin and its member eprinomectin could be investigated to control the pyrethroid insecticides resistant vectors.

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

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 complex samples 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.

Diriba Korecha Dadi’s PhD on Predicting Seasonal Climate in Ethiopia

On April 25, 2014 Diriba Korecha Dadi defended his PhD at the University of Bergen. Diriba was a part of the research programme “Ethiopian Malaria Prediction System”.

The Abstract of the thesis is found at:

His thesis, Characterizing the Predictability of Seasonal Climate in Ethiopia, can be downloaded

Validation of seasonal rainfall forecast in Ethiopia

Korecha, D., and A. Sorteberg (2013), Validation of operational seasonal rainfall forecast in Ethiopia, Water Resour. Res., 49, doi:10.1002/2013WR013760.

Operational rainfall forecasts using the analog method have been issued in Ethiopia since 1987. We evaluate the performance of the forecast system for February–May and June–September rainy seasons over the period 1999–2011. Verification is performed using rainfall data obtained from Ethiopian meteorological stations covering eight homogeneous rainfall regions used in the forecasts. The results reveal that forecasts issued by the National Meteorological Agency (NMA) of Ethiopia, for the past 12 years have a weak positive skill for all eight regions compared with climatology. In terms of ranked probability skill scores, the values are all lower than 10% indicating that the forecast skill is modest. The results further suggest that the forecasting system has bias toward forecasting near-normal conditions and has problems in capturing below average events. In contrast, the forecast has some positive skills in ranking the wet years of February–May season, particularly over the regions where there is high seasonal rainfall variability with significantly positive rank correlations for the above average years. For the main season, however, the forecast is not able to rank wet years or dry years. The extreme low and high rainfall events are mostly missed by the forecast scheme. The results indicate rather low forecast skill for extreme rainfall events in both seasons. Generally, the results indicate that NMA’s forecasts have low but positive skill as it is common with results from other forecasting systems for the Greater Horn of Africa region. The underforecasting of dry events is the most serious shortcoming of the system.

Housing and Anopheles arabiensis density in Ethiopia

Animut A, Balkew M, Lindtjorn B. Impact of housing condition on indoor-biting and indoor-resting Anopheles arabiensis density in a highland area, central Ethiopia. Malaria journal 2013;12(1):393.

Exposure of individuals to malaria infection may depend on their housing conditions as houses serve as biting and resting places of vectors. This study describes the association of housing conditions with densities of indoor-biting and indoor-resting Anopheles arabiensis in Hobe, Dirama and Wurib villages of a highland area in central Ethiopia.

Data on housing conditions, including presence of house apertures, number of occupants and number and the type of domestic animal tethered inside, were collected. Indoor-biting mosquitoes were sampled using Centers for Disease Control (CDC) light traps and indoor-resting mosquitoes sampled with pyrethrum spray catches (PSCs) monthly for two years (July 2008 to June 2010). Female anophelines were identified to species and processed. Univariate and general linear estimating equation allowing for repeated measures were used to assess the contribution of housing conditions for indoor-biting and indoor-resting An. arabiensis.

About 96% (4,597/4,788) of anophelines were caught inside residential houses. Nine anopheline species were identified, among which An. arabiensis was most prevalent (2,489; 52%). Vectors entering houses were higher in those situated at low (β = 4.475; 95% CI = 3.475-5.476; p <0.001; β = strength of the association) and medium (β = 2.850; 95% CI = 1.975-3.724; p <0.001) altitudes compared to high altitude, and where houses have no windows (β = -0.570; 95% CI = -1.047-0.094; p = 0.019) compared with those that have. Numbers of indoor-resting vectors were higher in those situated at low (β = 6.100; 95% CI = 4.571-7.629; p <0.001) and medium (β = 4.411; 95% CI = 2.284-6.537; p <0.001) altitudes compared to high altitudes, and where houses had open eaves (β =1.201; 95% CI = 0.704-1.698; p <0.001) compared with those that had closed eaves.

Housing conditions such as presence of open eaves, absence of window, location at low and mid altitudes, were strong predictors of indoor exposure to An. arabiensis bite in a highland area of south-central Ethiopia.