Taye Gari’s PhD thesis: Malaria, anaemia and undernutrition in Ethiopia

Taye Gari. Malaria, anaemia and undernutrition in a drought-affected area of the Rift Valley of Ethiopia: Experiences from a trial to prevent malaria.  PhD. University of Bergen, 2018. Bergen

Summary of PhD thesis

Background: In Ethiopia, malaria, anaemia and undernutrition are common childhood health problems. The country is planning to reduce these conditions to a level where they are not a public health problem. Meanwhile, for the success of this aim, a description of the occurrence and interaction of malaria, anaemia and undernutrition could help contribute to design tailored, efficient and effective control strategies. This study was done in the context of malaria prevention trial, which aimed to measure the effect of combining long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) in reducing the malaria incidence compared to LLINs or IRS alone. The study area was affected by a serious drought and famine during the first year of the study.

Objectives: The overall aim of this thesis is to improve our understanding of the effect of malaria prevention on anaemia, and to assess the association between malaria, anaemia and undernutrition among children in a drought-affected area in south-central, Ethiopia.

Methods: A cohort of 5309 residents was followed-up for 16 weeks to measure the variations in malaria incidence among villages (Paper I), and the results were used as a baseline to calculate the sample size needed for the trial. We followed a cohort of children aged 6 to 59 months for one year to describe anaemia and changes in haemoglobin (Hb) concentration (Paper II). A cohort of 4468 children was followed-up for 89 weeks to measure the relationship between malaria and undernutrition (Paper III). Weekly home visits and patient self-referral were also used to identify malaria cases. We conducted Hb concentration (once a year) and anthropometry (twice a year) surveys.

Results: In Paper I, we observed a variation in malaria incidence among villages. On the other hand, the insecticide-treated nets ownership was low (27%), with the distance from the lake or river and younger age being the main risk factors for malaria. The findings of this study were used as a baseline to calculate the sample size for the trial. In Paper II, despite the malaria prevention effort in the community, we observed an unexpected increase in anaemia prevalence over the period of a year, which could be due to the drought and famine that affected the area. A higher incidence of anaemia was observed among children with stunting, malaria infection, young age and in poor families. However, no significant difference in anaemia prevalence was observed among the different trial arms (LLIN+IRS, LLINs alone, IRS alone and routine arm). In Paper III, malaria infection was a risk factor for stunting and wasting, although undernutrition was not a risk for malaria infection. Furthermore, an increase in the prevalence of stunting, but no significant change in a prevalence of wasting was observed over time.

Conclusions: We showed a large variation in malaria incidence among villages. Conducting trials in a drought-prone area may bring an unexpected challenge. We observed an unexpected increase in anaemia prevalence over a year. There was no significant difference in anaemia prevalence among the trial arms. Moreover, a close follow-up of the nutritional status of children with malaria infection may be needed. There could hence be a need to prioritize villages nearer to the main mosquito breeding sites for malaria control.

Trial registration: PACTR 201411000882128 (8 September, 2014)

The Thesis can be downloaded here

Malaria, anaemia and undernutrition

On Friday June 22, 2018 Taye Gari Anaya will defend his PhD thesis at the University of Bergen. 

The title of his thesis is: “Malaria, anaemia and undernutrition in a drought-affected area of the Rift Valley of Ethiopia: Experiences from a trial to prevent malaria”.

Malaria, anaemia and malnutrition are interconnected, and often coexist in prevalent areas such as in sub-Saharan Africa, including Ethiopia. Although individuals in all ages of life are affected by these conditions, children under the age of 5 represent the most vulnerable group. Ethiopia is planning to reduce these conditions to a level where they are not public health problems Meanwhile, for the success of this aim, a description of the occurrence and interaction of malaria, anaemia and undernutrition could help to design tailored, efficient and effective control strategies.  

This thesis measures the effect of malaria prevention on anaemia reduction, and assesses the association between malaria, anaemia and undernutrition among a cohort of children aged 6 to 59 months old followed in a drought-affected rural area in south-central, Ethiopia.

The study showed a large variation in malaria incidence among villages in the same district. Despite community wide malaria prevention effort, an unexpected increase in anaemia prevalence was observed over a year. Malaria infection was a risk factor for undernutrition, although undernutrition was not a risk for malaria infection. There could be a need to prioritise villages nearer to the main mosquito breeding sites for malaria control. Moreover, a close follow-up of the nutritional status of children with malaria infection may be needed. 


Taye Gari Ayana is from Hawassa in south Ethiopia. He completed Master degree in Public Health from Addis Ababa University in Ethiopia. From 2013 he has been affiliated with the Centre for International Health as a PhD candidate. Now he is a lecturer at the School of Public Health, at Hawassa University in Ethiopia. His supervisors were Professor Bernt Lindtjørn, Dr Eskindir Loha and Dr Wakgari Deressa. 

Improved housing reduces malaria

Getawen SK, Ashine T, Massebo F, Woldeyes D, Lindtjorn B. Exploring the impact of house screening intervention on entomological indices and incidence of malaria in Arba Minch town, southwest Ethiopia: A randomized control trial. Acta Trop. 2018;181:84-94. Epub 2018/02/17. doi: 10.1016/j.actatropica.2018.02.009. PubMed PMID: 29452110

House is the major site for malaria infection where most human-vector contact takes place. Hence, improving housing might reduce the risk of malaria infection by limiting house entry of vectors. This study aimed to explore the impact of screening doors and windows with wire meshes on density and entomological inoculation rate (EIR) of malaria vector, and malaria incidence, and assess the acceptability, durability, and cost of the intervention. The susceptibility status of malaria vector was also assessed.

A two-arm randomized trial was done in Arba Minch Town, southwest Ethiopia. 92 houses were randomly included in the trial. The baseline entomological and malaria prevalence data were collected. The mosquito sampling was done twice per household per month by Centers for Diseases Control and Prevention (CDC) light traps for six months. The baseline prevalence of malaria was assessed by testing 396 (83% of the 447 study participants) household members in all the eligible houses. The 92 houses were then randomized into control and intervention groups using mosquito and malaria prevalence baseline data to make the two groups comparable except the intervention. Then, we put wire-mesh on doors and windows of 46 houses. Post-screening mosquito collection was done in each household twice per month for three months. Each household member was visited twice per month for six months to assess malaria episodes. The frequency of damage to different structure of screening was measured twice. In-depth interview was conducted with 24 purposely selected household heads from intervention group. Speciation of Anopheles mosquito was done by morphological key, and the circum-sporozoite proteins (CSPs) analysis was done using enzyme-linked immunosorbent assay. A generalized estimating equation with a negative binomial distribution was used to assess the impact of the intervention on the indoor density of vectors. Clinical malaria case data were analyzed using Poisson regression with generalized linear model.

Screening doors and windows reduced the indoor density of An. arabiensis by 48% (mean ratio of intervention to control = 0.85/1.65; 0.52) (P = .001). Plasmodium falciparum CSP rate was 1.6% (3/190) in the intervention houses, while it was 2.7% (10/372) in the control houses. The protective efficacy of screening intervention from CSP positive An. arabiensis was 41% (mean ratio of intervention to control = 1.6/2.7; 0.59), but was not statistically significant (P = .6). The EIR of An. arabiensis was 1.91 in the intervention group, whereas it was 6.45 in the control group. 477 participants were followed for clinical malaria (50.1% from intervention and 49.9% from the control group). Of 49 RDT positive cases, 45 were confirmed to be positive with microscopy. 80% (n = 36) cases were due to P. falciparum and the rest 20% (n = 9) were due to P. vivax. The incidence of P. falciparum in the intervention group was lower (IRR: 0.39, 95% CI: 0.2-0.80; P = .01) than in the control group. Using incidence of P. falciparum infection, the protective efficacy of intervention was 61% (95% CI: 18-83; P = .007). 97.9% of screened windows and 63.8% of screened doors were intact after eleven months of installation. Malaria mosquito was resistance (mortality rate of 75%) to the insecticide used for bed nets treatment. Almost all participants of intervention arm were willing to continue using screened doors and windows.

Screening doors and windows reduced the indoor exposure to malaria vectors. The intervention is effective, durable and well-accepted. Hence, the existing interventions can be supplemented with house screening intervention for further reduction and ultimately elimination of malaria by reducing insecticide pressure on malaria vectors. However, further research could be considered in broad setting on different housing improvement and in the way how to scale-up for wider community.


Intended and non-intended use of bed nets for malaria protection

Doda Z, Solomon T, Loha E, Gari T and Lindtjørn B. A qualitative study of use of long-lasting insecticidal nets (LLINs) for intended and unintended purposes in Adami Tullu, East Shewa Zone, Ethiopia. Malaria Journal 2018;17:69  https://doi.org/10.1186/s12936-018-2209-5


Background  Malaria poses a significant public health threat globally, across Africa and in Ethiopia. The use of long-lasting insecticidal nets (LLINs) is currently a proven prevention mechanism. Evidence is building on what happens to LLINs following mass distribution campaigns, with mixed results from different studies, some reporting very low use for intended purposes, others an encouraging level of using for intended purposes. In Ethiopia, between 2005 and 2015, about 64 million LLINs were distributed through periodic mass campaigns with the aims to achieve 100% coverage and 80% utilization. However, studies from rural Ethiopia showed variable LLINs coverage and utilization rate. The MalTrial Project, a collaborative venture between Hawassa University, Ethiopia and NROAID, Norway, has started a trial project in 2014 in Adami Tullu District of central Ethiopia. Quantitative surveys have established evidence on LLINs ownership and utilization, but the behavioural, sociocultural and socioeconomic dynamics of why LLINs’ use for intended purposes is low or why they are employed for other purposes remained elusive. The present qualitative study, building on the quantitative findings and framework, therefore, attempted to fill gaps in these areas using qualitative methods in selected localities of the district.

Methods  The study employed 7 focus groups, 16 individual interviews and observation to undertake data collection in January 2017. The data were analysed using NVivo Version 11 (QSR International) to transcribe, code and identify themes using thematic analysis approach.

Results  The study found out that certain households were more likely to use nets for intended needs in proper ways; a range of factors, notably socio-cultural and poverty, highly influence users’ ideas about the right ways and decisions to use and care for the nets; knowledge gaps and wrong perception exist regarding the purposes and life cycle of the nets; LLINs are employed for repurposed uses once they are considered non-viable, old, or lose their physical integrity; existence of misuse was acknowledged and understood as wrong; and values about gender roles further shape uses, misuses and repurposed use of the nets.

Conclusions  Behavioural, socio-cultural, economic and ecological conditions coupled with deficiencies in perceived bed net design and distribution policies; weak education, communication and social support structures were important in understanding and accounting for why a low level of intended use and a rampant misuse and repurposed use in Adami Tullu community of Ethiopia. A major nexus to address in order to improve intended use of LLINs lies, first and foremost, in economic poverty and socio-cultural factors that underlie much of the misuse and repurposed use of the nets.

Keywords  LLINs Malaria; Intended uses; Misuses; Repurposed uses; Collateral benefits of LLINs


Malaria increases the risk of stunting and wasting

Gari T, Loha E, Deressa W, Solomon T, Lindtjørn B (2018) Malaria increased the risk of stunting and wasting among young children in Ethiopia: Results of a cohort study. PLoS ONE 13(1): e0190983.

Introduction  Given the high prevalence of malnutrition in a malaria-endemic setting, improving nutritional status could serve as a tool to prevent malaria. However, the relationship between the two conditions remains unclear. Therefore, this study assessed the association between under-nutrition and malaria among a cohort of children aged 6 to 59 months old.

Methods  Two cohorts of children were followed for 89 weeks in a rural Rift Valley area of Ethiopia. In the first approach (malaria-malnutrition), a cohort of 2,330 non-stunted and 4,204 non-wasted children were included to assess under-nutrition (outcome) based on their previous malaria status (exposure). In the second approach (malnutrition–malaria), a cohort of 4,468 children were followed-up to measure malaria (outcome), taking under-nutrition as an exposure. A weekly home visit was carried out to identify malaria cases. Four anthropometry surveys were conducted, and generalized estimating equation (GEE) method was used to measure the association between undernutrition and malaria.

Results  The prevalence of stunting was 44.9% in December 2014, 51.5% in August 2015, 50.7% in December 2015 and 48.1% in August 2016. We observed 103 cases with 118 episodes of malaria, 684 new stunting and 239 new wasting cases. The incidence rate per 10,000 weeks of observation was 3.8 for malaria, 50.4 for stunting and 8.2 for wasting. Children with malaria infection, [Adjusted Odds Ratio (AOR) = 1.9; 95% Confidence Interval (CI), 1.2–2.9)] and younger age (AOR = 1.3; 95% CI, 1.1–1.5) were more likely to be stunted. Furthermore, children with malaria infection (AOR = 8.5; 95% CI, 5.0–14.5) and young age group (AOR = 1.6; 95% CI, 1.2–2.1) were more likely to be wasted. However, stunting and wasting were not risk factors of subsequent malaria illness.

Conclusions  Malaria infection was a risk factor for stunting and wasting, but stunting or wasting was not associated with subsequent malaria illness. As our study shows that malaria is a risk factor for stunting and wasting, a close follow-up of the nutritional status of such children may be needed.

Use of epidemiological and entomological tools in the control and elimination of malaria in Ethiopia

Animut A and Lindtjørn B. Use of epidemiological and entomological tools in the control and elimination of malaria in EthiopiaMalaria Journal 2018; 17:26.

Malaria is the leading public health problem in Ethiopia where over 75% of the land surface is at risk with varying intensities depending on altitude and season. Although the mortality because of malaria infection has declined much during the last 15–20 years, some researchers worry that this success story may not be sustainable. Past notable achievements in the reduction of malaria disease burden could be reversed in the future. To interrupt, or even to eliminate malaria transmission in Ethiopia, there is a need to implement a wide range of interventions that include insecticide-treated bed nets, indoor residual spraying, improved control of residual malaria transmission, and improved diagnostics, enhanced surveillance, and methods to deal with the emergence of resistance both to drugs and to insecticides. Developments during the past years with increasing awareness about the role of very low levels of malaria prevalence can sustain infections, may also demand that tools not used in the routine control efforts to reduce or eliminate malaria, should now be made available in places where malaria transmission occurs.

Malaria Conference in Hawassa

On December 13, 2017, the MalTrials project, a joint venture between Hawassa University, Addis Ababa University, and University of Bergen held International Research Seminar on Malaria. The conference was held at Haile Resort in Hawassa. The Maltrials project, Combining long-lasting insecticidal nets and indoor residual spraying for malaria prevention in Ethiopia: a cluster randomized controlled trial, started in 2013, and the main results were presented at the conference.

More information, and pictures from the conference can be viewed at the website of Hawassa University: International Research Seminar on Malaria Control held at Hawassa

Combining long-lasting insecticidal nets and indoor residual spraying for malaria prevention in Ethiopia: a cluster randomized controlled trial

Session 161 – Malaria: Epidemiology – Measuring Changes

Presentation on November 8th, 2017 at the Annual Meeting of the American Society of Tropical Medicine and Hygiene

Eskindir Loha1, Wakgari Deressa2, Taye Gari1, Meshesha Balkew2, Oljira Kenea2, Tarekegn Solomon1, Alemayehu Hailu2, Bjarne Robberstad3, Meselech Assegid2, Hans J. Overgaard4, Bernt Lindtjørn3
1Hawassa University, Hawassa, Ethiopia, 2Addis Ababa University, Addis Ababa, Ethiopia, 3University of Bergen, Bergen, Norway, 4Norwegian University of Life Sciences, Aas, Norway

Background Long lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) are effective tools to prevent malaria, but the effectiveness of combining the two are not yet fully understood. This study compared the separate versus combined effect of LLINs and IRS on malaria incidence and anemia.

Methods This cluster randomized controlled trial was done in the Adami Tullu district in south-central Ethiopia for 119 weeks, from September 2014 to January 2017. Prior to the trial, we did a pilot study to estimate the sample size, and registered 8 malaria episodes per 10,000 person-weeks of observation (PWO). 6072 households (HHs) were randomly assigned to four intervention arms: LLINs + IRS, LLINs, IRS, and no intervention implemented by the project (control). The primary outcome was malaria incidence. Analysis was based on an intention-to-treat principle. Each arm had 44 clusters with an average of 35 HHs per cluster; the total population was 34,548. PermaNet 2.0 LLINs were distributed in September 2014, and IRS (with propoxur) was carried out yearly. Active and passive case detection were done weekly. Malaria was diagnosed using a rapid diagnostic test (CareStartTM). Anemia was assessed through yearly surveys on children. The yearly rainfall was 60% of expected in 2015 (El Nino effect), entomological studies were simultaneously conducted.

Results The overall malaria incidence was 2.91 per 10,000 PWO (37% of pre-intervention incidence), and similar in the four arms with 2.99 (LLINs + IRS), 2.92 (LLINs), 3.01 (IRS) and 2.72 (control). Generalized estimation equation showed that LLINs did not provide individual protection. Entomological findings showed greater outdoor mosquito human-biting activities than indoor. The yearly mean hemoglobin concentrations were similar among the trial arms.

Conclusions The malaria incidence was low and similar in the intervention arms. The severe drought might have contributed in too few malaria cases to evaluate the interventions. However, residual transmission could be an important cause of malaria transmission in the area. Our results could be relevant for situations with low malaria incidence.

The economic burden of malaria is high, — mainly to the poor rural households in Ethiopia

Hailu A, Lindtjørn B, Deressa W, Gari T, Loha E, Robberstad B. Economic burden of malaria and predictors of cost variability to rural households in south-central Ethiopia. PLoS ONE 2017; 12(10): e0185315.


Background  While recognizing the recent remarkable achievement in the global malaria reduction, the disease remains a challenge to the malaria endemic countries in Africa. Beyond the huge health consequence of malaria, policymakers need to be informed about the economic burden of the disease to the households. However, evidence on the economic burden of malaria in Ethiopia is scanty. The aims of this study were to estimate the economic burden of malaria episode and to identify predictors of cost variability to the rural households.

Methods  A prospective costing approach from a household perspective was employed. A total of 190 malaria patients were enrolled to the study from three health centers and nine health posts in Adami Tullu district in south-central Ethiopia, in 2015. Primary data were collected on expenditures due to malaria, forgone working days because of illness, socioeconomic and demographic situation, and households’ assets. Quantile regression was applied to predict factors associated with the cost variation. Socioeconomic related inequality was measured using concentration index and concentration curve.

Results  The median cost of malaria per episode to the household was USD 5.06 (IQR: 2.98–8.10). The direct cost accounted for 39%, while the indirect counterpart accounted for 61%. The history of malaria in the last six months and the level of the facility visited in the health system predominantly influenced the direct cost. The indirect cost was mainly influenced by the availability of antimalarial drugs in the health facility. The concentration curve and the concentration index for direct cost indicate significant pro-rich inequality. Plasmodium falciparum is significantly more costly for households compared to Plasmodium vivax.

Conclusion  The economic burden of malaria to the rural households in Ethiopia was substantial—mainly to the poor—indicating that reducing malaria burden could contribute to the poverty reduction as well.

Plasmodium vivax infection in South Ethiopia

Nissen A, Cook J, Loha E, Lindtjørn B: Proximity to vector breeding site and risk of Plasmodium vivax infection: a prospective cohort study in rural Ethiopia. Malaria Journal 2017, 16.


Background  Despite falling incidence and mortality since the turn of the century, malaria remains an important global health challenge. In the future fight against malaria, greater emphasis will have to be placed on understanding and addressing malaria caused by the Plasmodium vivax parasite. Unfortunately, due to years of neglect and underfunding, there are currently many gaps in knowledge of P. vivax malaria. The aims of the present study were to explore the association between distance to vector breeding site and P. vivax infection in rural Ethiopia, and, secondarily, to test whether this association varies with age.

Methods  A prospective, cohort study of all residents in the Chano Mille Kebele in southern Ethiopia from April 2009 to March 2011 (n = 8121). Weekly household follow up visits included screening for febrile cases (active surveillance). Participants were also asked to contact the local health centre if they experienced subjective fever between visits (passive surveillance). Plasmodium vivax infection was confirmed using microscopy by two independent readers. Information was collected on demographics and household characteristics including GPS-determined distance to vector breeding site. Data was analysed using Cox regression modelling.

Results  Overall the P. vivax infection rate was 12.3/1000 person-years (95% CI 10.5–14.5). Mean household distance to breeding site was 2449 m (range 1646–3717 m). Fully adjusted results showed very strong evidence of an association between proximity to breeding site and P. vivax infection: rate ratio = 3.47 (95% CI 2.15–5.60; P < 0.001) comparing the group closest to the breeding site (distance < 2100 m; n = 1383) to the group furthest away (distance > 2700 m; n = 2460). There was no evidence that age was an effect modifier in the association.

Conclusion  Results showed strong evidence that household proximity to vector breeding site is positively associated with P. vivax infection in rural Ethiopia, and that this association is constant across age groups. The findings might influence how net-distribution and indoor residual spraying campaigns are planned, help guide strategies on water resource development by highlighting potential health effects of man-made dams near human habitats, and add to current educational information given to people living close to breeding sites.