Improved housing reduces malaria

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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

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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

Abstract

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

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

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

Abstract
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 increases the risk of stunting and wasting

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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.

Abstract
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.

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

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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

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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.

Abstract

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

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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.

Abstract

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.

Malaria transmission at high altitudes in Ethiopia

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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

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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.

Abstract
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.

Anaemia, drought and malaria in Ethiopia

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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.