Collecting malaria mosquitoes

Kenea O, Balkew M, Tekie H, Gebre-Michael T, Deressa W, Loha E, Lindtjørn B, Overgaard HJ: Comparison of two adult mosquito sampling methods with human landing catches in south-central Ethiopia. Malaria Journal 2017, 16

Background  The human landing catch (HLC) is the standard reference method for measuring human exposure to mosquito bites. However, HLC is labour-intensive, exposes collectors to infectious mosquito bites and is subjected to collector bias. These necessitate local calibration and application of alternative methods. This study was undertaken to determine the relative sampling efficiency (RSE) of light traps with or without yeast-produced carbon dioxide bait vs. HLC in south-central Ethiopia.

Methods  The experiment was conducted for 39 nights in a 3 × 3 Latin square randomized design with Anopheles arabiensis as the target species in the period between July and November 2014 in Edo Kontola village, south-central Ethiopia. Center for Disease Control and Prevention light trap catches (LTC) and yeast-generated carbon dioxide-baited light trap catches (CB-LTC) were each evaluated against HLC. The total nightly mosquito catches for each Anopheles species in either method was compared with HLC by Pearson correlation and simple linear regression analysis on log-transformed [log10(x + 1)] values. To test if the RSE of each alternative method was affected by mosquito density, the ratio of the number of mosquitoes in each method to the number of mosquitoes in HLC was plotted against the average mosquito abundance.

Results  Overall, 7606 Anopheles females were collected by the three sampling methods. Among these 5228 (68.7%) were Anopheles ziemanni, 1153 (15.2%) An. arabiensis, 883 (11.6%) Anopheles funestus s.l., and 342 (4.5%) Anopheles pharoensis. HLC yielded 3392 (44.6%), CB-LTC 2150 (28.3%), and LTC 2064 (27.1%) Anopheles females. The RSEs of LTC and HLC for An. arabiensis were significantly correlated (p < 0.001) and density independent (p = 0.65). However, for outdoor collection of the same species, RSEs of LTC and CB-LTC were density dependent (p < 0.001). It was estimated that on average, indoor LTC and CB-LTC each caught 0.35 and 0.44 times that of indoor HLC for An. arabiensis respectively.

Conclusions  Results showed that HLC was the most efficient method for sampling An. arabiensis. LTC can be used for large-scale indoor An. arabiensis surveillance and monitoring when it is difficult to use HLC. CB-LTC does not substantially improve sampling of this major vector compared to LTC in this setting.

Reducing maternal deaths in Southwest Ethiopia

Lindtjørn B, Mitiku D, Zidda Z, Yaya Y (2017) Reducing Maternal Deaths in Ethiopia: Results of an Intervention Programme in Southwest Ethiopia. PLoS ONE 12(1): e0169304. doi:10.1371/journal.pone.0169304

Background  In a large population in Southwest Ethiopia (population 700,000), we carried out a complex set of interventions with the aim of reducing maternal mortality. This study evaluated the effects of several coordinated interventions to help improve effective coverage and reduce maternal deaths. Together with the Ministry of Health in Ethiopia, we designed a project to strengthen the health-care system. A particular emphasis was given to upgrade existing institutions so that they could carry out Basic (BEmOC) and Comprehensive Emergency Obstetric Care (CEmOC). Health institutions were upgraded by training non-clinical physicians and midwives by providing the institutions with essential and basic equipment, and by regular monitoring and supervision by staff competent in emergency obstetric work.

Results  In this implementation study, the maternal mortality ratio (MMR) was the primary outcome. The study was carried out from 2010 to 2013 in three districts, and we registered 38,312 births. The MMR declined by 64% during the intervention period from 477 to 219 deaths per 100,000 live births (OR 0.46; 95% CI 0.24–0.88). The decline in MMR was higher for the districts with CEmOC, while the mean number of antenatal visits for each woman was 2.6 (Inter Quartile Range 2–4). The percentage of pregnant women who attended four or more antenatal controls increased by 20%, with the number of women who delivered at home declining by 10.5% (P<0.001). Similarly, the number of deliveries at health posts, health centres and hospitals increased, and we observed a decline in the use of traditional birth attendants. Households living near to all-weather roads had lower maternal mortality rates (MMR 220) compared with households without roads (MMR 598; OR 2.72 (95% CI 1.61–4.61)).

Conclusions  Our results show that it is possible to achieve substantial reductions in maternal mortality rates over a short period of time if the effective coverage of well-known interventions is implemented.

Presentation at 65th Annual meeting of the American Society of Tropical Medicine and Hygiene

Impact of combining Indoor Residual Spraying and Long-Lasting Insecticidal Nets on Anopheles arabiensis in Ethiopia: Preliminary findings of a randomized controlled trial

Oljira Kenea, Meshesha Balkew, Habte Tekie, Teshome Gebre-Michael, Wakgari Deressa, Eskindir Loha, Hans J. Overgaard, Bernt Lindtjørn


The current malaria vector control interventions, indoor residual spraying (IRS) and long-lasting insecticidal nets (LLINs) have been used in combination in sub-Saharan Africa with inconclusive evidence that the combined intervention is more effective than either IRS or LLINs alone. In Ethiopia, both interventions target Anopheles arabiensis, the sole primary malaria vector. This study compared the impact of combining IRS and LLINs with either intervention alone in south-central Ethiopia. Villages were randomly allocated to four study arms: IRS + LLIN, IRS, LLIN, and control. LLINs (PermaNet 2.0) were provided free of charge. IRS with propoxur was applied 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). Human landing catch (HLC) was performed in selected villages to monitor An. arabiensis biting behaviors. Mean densities were compared using incidence rate ratio (IRR) calculated by negative binomial regression. A total of 1786 female anophelines of four species was collected of which An. arabiensis (n=574) was highest in the control arm (51.4%) followed by LLIN (31.5%), IRS (9.2%), and IRS+LLIN (7.9%). The mean HSD of An. arabiensis in the IRS+LLIN arm was similar to either the IRS arm (0.03 vs. 0.03/ house/LTC/night) or the LLIN arm (0.03 vs. 0.10/house/LTC/night, p=0.07) and so was the difference in IRD and ORD between the IRS and LLIN compared to the IRS arm. However, both IRD and ORD were higher in LLIN compared to IRS+LLIN (p < 0.001 for indoors). In all study arms, An. arabiensis was actively biting indoors and outdoors throughout the night with an early night biting peak before the local people retire to bed. IRS+LLIN compared to IRS had equal powerful impact on resting density of An. arabiensis, but LLIN had the least impact.

Malaria control or elimination?

Malaria controlAbout ten years ago, the global health community was cautious about aiming at malaria eradication. The experiences from the 1960s and 1970s left some severe scars on such campaigns. Recently, the Gates Foundation has led the shift in approach and mobilised others to join efforts to end the disease. However, while malaria is preventable and treatable, eradication requires new tools (see figure).

A good vaccine would be highest on the agenda. Although vaccine trials show promising results, the vaccine efficacy is unfortunately too low to eradicate the disease.

Our recent study on the prevention of malaria in the Rift Valley of Ethiopia also shows some of the limited effects of insecticide-treated bed nets. In addition, we have observed that many of the mosquito bites take place at times when people do not use their bed nets. Our mosquito studies show that indoor residual spraying with insecticides can reduce the density of mosquitoes both inside the houses as well as outside the houses. Furthermore, a recent and unpublished study from south-west Ethiopia supporter previous findings that improving housing can reduce the entomological inoculation rates, which is a measure on how dangerous the mosquitoes are in transmitting malaria.

We, therefore, also support that several new tools are required. So, maybe the time is right to assess the combination of many interventions that would include active case finding, treatment, insecticide treated bed nets, indoor residual spraying, improved housing, and other vector control measures; such as reducing the out-door density of malaria mosquitoes.

Human-biting activities of Anopheles species in Ethiopia

Kenea O, Balkew M, Tekie H, Gebre-Michael T, Deressa W, Loha E, Lindtjørn B, Overgaard HJ: Human-biting activities of Anopheles species in south-central Ethiopia. Parasites & vectors 2016, 9(1):1-12.


Background    Indoor residual spraying (IRS) and long-lasting insecticidal nets (LLINs) are the key malaria vector control interventions in Ethiopia. The success of these interventions rely on their efficacy to repel or kill indoor feeding and resting mosquitoes. This study was undertaken to monitor human-biting patterns of Anopheles species in south-central Ethiopia.

Methods   Human-biting patterns of anophelines were monitored for 40 nights in three houses using human landing catches (HLC) both indoors and outdoors between July and November 2014, in Edo Kontola village, south-central Ethiopia. This time coincides with the major malaria transmission season in Ethiopia, which is usually between September and November. Adult mosquitoes were collected from 19:00 to 06:00 h and identified to species. Comparisons of HLC data were done using incidence rate ratio (IRR) calculated by negative binomial regression. The nocturnal biting activities of each Anopheles species was expressed as mean number of mosquitoes landing per person per hour. To assess malaria infections in Anopheles mosquitoes the presence of Plasmodium falciparum and P. vivax circumsporozoite proteins (CSP) were determined by enzyme-linked immunosorbent assay (ELISA).

Results   Altogether 3,408 adult female anophelines were collected, 2,610 (76.6 %) outdoors and 798 (23.4 %) indoors. Anopheles zeimanni was the predominant species (66.5 %) followed by An. arabiensis (24.8 %), An. pharoensis (6.8 %) and An. funestus (s.l.) (1.8 %).

The overall mean anopheline density was 3.3 times higher outdoors than indoors (65.3 vs19.9/person/night, IRR: 3.3, 95 % CI: 1.1–5.1, P = 0.001). The mean density of An. zeimanniAn. pharoensis and An. funestus (s.l.) collected outdoors was significantly higher than indoors for each species (P < 0.05). However, the mean An. arabiensis density outdoors was similar to that indoors (11.8 vs 9.4/person/night, IRR: 1.3, 95 % CI: 0.8–1.9, P = 0.335). The mean hourly human-biting density of An. arabiensis was greater outdoors than indoors and peaked between 21:00 and 22:00 h. However, An. arabiensis parous population showed high indoor man biting activities during bedtimes (22:00 to 05:00 h) when the local people were indoor and potentially protected by IRS and LLINs. All mosquito samples tested for CSP antigen were found negative to malaria parasites.

Conclusions   Results show much greater mosquito human-biting activities occurring outdoors than indoors and during early parts of the night, implying higher outdoor malaria transmission potential in the area. However, high bedtime (22:00 to 05:00 h) indoor biting activities of parous An. arabiensissuggest high potential intervention impact of IRS and LLINs on indoor malaria transmission.

New information about malnutrition in Ethiopia

Seifu-thesis coverNew PhD: On September 16, Seifu Hagos Gebreyesus from Ethiopia, shall defend his PhD work at the University of Bergen:

Spatial variations in child undernutrition in Ethiopia: Implications for intervention strategies


Background: Ethiopia is one of the countries with the highest burden of undernutrition, with rates of stunting and underweight as high as 40% and 25%, respectively. National efforts are underway for an accelerated reduction of undernutrition by the year 2030. However, for this to occur, understanding the spatial variations in the distribution of undernutrition on a varying geographic scale, and its determinants will contribute a quite a bit to enhance planning and implementing nutrition intervention programmes.

Objectives: The aim of this thesis was to evaluate the large- and small-scale spatial variations in the distribution of undernutrition indicators, the underlying processes and the factors responsible for the observed spatial variations.

Methods: We used nationally available climate and undernutrition data to evaluate the macro-scale spatial pattern of undernutrition and its determinants. We applied a panel study design, and evaluated the effect of growing seasonal rainfall and temperature variability on the macro-scale spatial variations (Paper I). We conducted a repeated cross- sectional survey to assess the performance of the Household Food Insecurity Access Scale (HFIAS) developed internationally to measure household food insecurity. The results from this validation work were used to modify the HFIAS items for subsequent papers (Papers III and IV). We conducted a census on six randomly selected kebeles to evaluate the spatial patterns of undernutrition on a smaller scale (Paper III). For Paper IV, we conducted a cross-sectional survey on a representative sample, and employed a Bayesian geo-statistical model to help identify the risk factors for stunting, thereby accounting for the spatial structure (spatial dependency) of the data.

Results: In Paper I, we demonstrated spatial variations in the distribution of stunting across administrative zones in the country, which could be explained in part by rainfall. However, the models poorly explained the variation in stunting within an administrative zone during the study period. We indicated that a single model for all agro-ecologic zones may not be appropriate. In Paper II, we showed that the internal consistency of the HFIAS’ tools, as measured by Cronbach’s alpha, was adequate. We observed a lack of reproducibility in HFIAS score among rural households. Therefore, we modified the HFAIS tool, and used it for subsequent surveys in this thesis (Papers III and IV). In Paper III, spatial clustering on a smaller scale (within a kebele) was found for wasting and severe wasting. Spatial clustering on a higher scale (inter-kebele) was found for stunting and severe stunting. Children found within the identified cluster were 1.5 times more at risk of stunting, and nearly five times more at risk of wasting, than children residing outside this cluster. In Paper IV, we found a significant spatial heterogeneity in the distribution of stunting in the district. Using both the local Anselin Moran’s I (LISA) and the scan statistics, we identified statistically significant clusters of high value (hotspots) and a most likely significant cluster for stunting in the eastern part of the district. We found that the risk of stunting was higher among boys, children whose mother or guardian had no education and children who lived in a food-insecure household. We showed that including a spatial component (spatial structure of the data) into the Bayesian model improved the model fit compared with the model without this spatial component.

Conclusion: We demonstrated that stunting and wasting exhibited a spatial heterogeneity, both on a large and small scale, rather than being distributed randomly. We demonstrated that there is a tendency for undernourished cases (stunting and wasting) to occur near each other than to occur homogeneously. We demonstrated a micro-level spatial variation in risk and vulnerability to undernutrition in a district with a high burden of undernutrition. Identifying such areas where a population at risk lives is central in assisting a geographical targeting of intervention. We recommend further study, possibly using a trial design or implementation research approach, to help evaluate the feasibility and benefits of geographically targeting nutritional interventions.

The thesis can be downloaded here.

Important research on tuberculosis control

Mesay-thesis title

New PhD: On September 5, Mesay Hailu Dangisso from Ethiopia, shall defend his PhD work at the University of Bergen:

Tuberculosis control in Sidama in Ethiopia. Programme performance and spatial epidemiology

The Sustainable Development Goals are to end the TB epidemic by reducing the incidence of TB by 90 % and by reducing mortality by 95% by 2035 from what was in 2015. Globally, access to TB diagnostic and treatment facilities (DOTS) has improved, and millions of TB cases have been notified and treated, which has resulted in many lives being saved. In recent years in Ethiopia, TB control services have been substantially expanded and decentralized, which has improved access to TB care. Assessing trends in TB programme performance (case notification and treatment outcomes), as well as the spatial distribution and variations of the disease, could help in understanding the differentials in accessibility to TB control services, the distribution of disease burden and help in understanding the effectiveness of TB control programmes.

We assessed the distribution of- and accessibility to TB control facilities and trends in TB control programme performance in both urban and rural settings, by age category and by gender, and assessed the case notification rates of childhood TB over 10 years. We also assessed trends of the treatment outcomes of TB cases in order to identify high-risk groups for adverse treatment outcomes. Lastly, we explored spatial distribution and spatio-temporal clustering of the disease over 10 years to identify areas with the highest TB case notifications, and to identify the spatial variations in disease occurrence.

Over 10 years, the accessibility to- and coverage of TB control facilities has improved. Thus, TB control service coverage increased by 36%, and the proportion of locations within 10 km of the nearest TB diagnostic facility also increased. However, we noted variations in physical accessibility between areas in the study area. The mean distance from the nearest smear microscopy unit was 7.6 km in 2003 and declined to 3.2 km in 2012. The substantial expansion of primary health-care services, including TB control facilities and community-based intervention, has contributed to an increase in TB CNRs and treatment outcomes. From this finding, we suggest that a concerted effort be made to improve the accessibility to TB control facilities in areas with low case notification and poor accessibility.

An analysis of the trends of TB case notification and treatment outcomes in different settings based on the correct address, by age category and gender, and place of residence, could help understand the performance of TB control programmes and the epidemiology of TB within a community. We found that the CNRs for all forms of- and smear-positive TB increased steadily between 2003 and 2012. The CNR of smear-positive TB in the 45-year and above age groups rose by nearly fourfold. The disparity between men and women in CNR declined from 16 per 100,000 people in 2003 to eight per 100,000 people in 2012, with the male to female ratio also declining from 1.3:1 to 1.1:1. The increase in CNRs could be attributed to improved access to TB care and community-based interventions.

Over a decade, treatment success increased, whereas mortality and lost-to-follow-up declined. However, more deaths occurred among smear-negative TB cases, in children and among older patients. Targeted interventions are needed to address high-risk groups for adverse treatment outcomes.

The burden of childhood TB is one of the indicators used for assessing the ongoing transmission of the disease within a community. Assessing the case notification and treatment outcome of childhood TB could provide essential evidence to help understand the effectiveness of TB control programmes and the disease burden. Thus, we assessed childhood TB case notification and treatment outcomes over a decade. The mean CNRs for new cases of TB of all forms were 30 per 100,000 children, and no decline was observed in childhood TB cases over a 10-year study period. A community-based active case-finding intervention increased TB case notification in adults and in older children (10-14-year-olds); however, the case notification did not increase among younger children (less than five-years old). This could be explained by inadequate diagnostic facilities for childhood TB despite the community-based intervention, which focuses on symptomatic screening, followed by sputum-smear microscopy and the substantial expansion of TB control services. Better diagnostic facilities and interventions are required to increase case detection, and to improve treatment outcome among younger children.

The burden of TB varies between- and within countries because of differentials in health service performance and the varying distribution of risk factors that increase the transmission of- and susceptibility to the disease. An analysis of the disease burden in coarser geographic or administrative units could hide the burden of the disease at lower administrative units. Therefore, we assessed the distribution of the disease in different geographic settings in the study area, and looked for the pattern of the disease transmission over years, as well as for evidence of spatio- temporal clustering. We found spatial variations in both the disease distribution and spatial and space-time clustering of the disease in the central, northern and northwestern areas of the study area. This could be explained by sustained transmission, disproportionate distribution of risk factors, varying access to TB care and varying TB programme performance, all of which require targeted interventions.

In conclusion, in a population with a high prevalence of tuberculosis, we show that access to tuberculosis diagnostic and treatment facilities, in addition to the performance of TB control programmes, improved from 2003 to 2012. However, we identified areas with poor accessibility to diagnostic and treatment facilities. The low and constant case notification rate in childhood TB is an area of concern, and may indicate an underdiagnosis of childhood tuberculosis. Moreover, the distribution of tuberculosis has changed over time, and in different areas, thereby suggesting a high transmission or variable access to diagnosis and treatment. As a result, the variations in case notification rates, and in accessibility to tuberculosis control services represent challenges on how to improve the organization and performance of TB control.

To download the thesis please clic here.

Smallpox and eliminating other diseases

 Dr. Donald A. Henderson, who led the World Health Organization’s war on smallpox, administering a smallpox vaccination in Ethiopia, around 1972. The last known case was in 1977. (Photo WHO)



Dr. Donald A. Henderson was an American physician who coordinated the World Health Organisation’s efforts to eradicate smallpox. After smallpox had been declared eradicated in 1980, he returned to the US, and became the Dean of what is now the Johns Hopkins Bloomberg School of Public Health. Dr. Donald A. Henderson died this month and will be remembered as a great scientist and public health physician.

As a child in late 1950s I remember a smallpox epidemic in Dilla in Ethiopia. I was so fortunate to have met this remarkable man, and listen to a talk he had at WHO in Geneva. Because of the success in eradicating smallpox, many believe that it also should be possible to eliminate other diseases such as poliomyelitis, Guinea worm, measles, or even malaria. I find it interesting to read that Dr Henderson was rather skeptical about these new eradication initiatives. Both the characteristics of the diseases, as well as the efforts put into getting rid of the diseases differed from what was the strategy to eradicate smallpox.

Incidence of tuberculosis among school-going adolescents in South India

Uppada DR, Selvam S, Jesuraj N, Lau EL, Doherty TM, Grewal HMS, Vaz M, Lindtjørn B: Incidence of tuberculosis among school-going adolescents in South India. BMC Public Health 2016, 16:1-11.

Background  Tuberculosis (TB) incidence data in vaccine target populations, particularly adolescents, are important for designing and powering vaccine clinical trials. Little is known about the incidence of tuberculosis among adolescents in India. The objective of current study is to estimate the incidence of pulmonary tuberculosis (PTB) disease among adolescents attending school in South India using two different surveillance methods (active and passive) and to compare the incidence between the two groups.

Methods  The study was a prospective cohort study with a 2-year follow-up period. The study was conducted in Palamaner, Chittoor District of Andhra Pradesh, South India from February 2007 to July 2010. A random sampling procedure was used to select a subset of schools to enable approximately 8000 subjects to be available for randomization in the study. A stratified randomization procedure was used to assign the selected schools to either active or passive surveillance. Participants who met the criteria for being exposed to TB were referred to the diagnostic ward for pulmonary tuberculosis confirmation. A total number of 3441 males and 3202 females between the ages 11 and less than 18 years were enrolled into the study.

Results  Of the 3102 participants in the active surveillance group, four subjects were diagnosed with definite tuberculosis, four subjects with probable tuberculosis, and 71 subjects had non-tuberculous Mycobacteria (NTM) isolated from their sputum. Of the 3541 participants in the passive surveillance group, four subjects were diagnosed with definite tuberculosis, two subjects with probable tuberculosis, and 48 subjects had non-tuberculosis Mycobacteria isolated from their sputum. The incidence of definite + probable TB was 147.60 / 100,000 person years in the active surveillance group and 87 / 100,000 person years in the passive surveillance group.

Conclusion  The incidence of pulmonary tuberculosis among adolescents in our study is lower than similar studies conducted in South Africa and Eastern Uganda – countries with a higher incidence of tuberculosis and human immunodeficiency virus (HIV) than India. The study data will inform sample design for vaccine efficacy trials among adolescents in India.

Primary and secondary anti-tuberculosis drug resistance in Ethiopia

Hamusse S, Teshome D, Hussen M, Demissie M, Lindtjorn B. Primary and secondary anti-tuberculosis drug resistance in Hitossa District of Arsi Zone, Oromia Regional State, Central Ethiopia. BMC Public Health 2016; 16(1):

Background: Multidrug-resistant tuberculosis (MDR-TB) drugs which is resistant to the major first-line anti-TB drugs, Isoniazid and Rifampicin, has become a major global challenge in tuberculosis (TB) control programme. However, its burden at community level is not well known. Thus, the aim of study was to assess the prevalence of primary and secondary resistance to any first line anti-TB drugs and MDR TB in Hitossa District of Oromia Regional State, Central Ethiopia.

Methods: Population based cross- sectional study was conducted on individuals aged ≥15 years. Those with symptoms suggestive of TB were interviewed and two sputum specimens were collected from each and examined using Lowenstein-Jensen (LJ) culture medium. Further, the isolates were confirmed by the Ziehl-Neelsen microscopic examination method. Drug susceptibility test (DST) was also conducted on LJ medium using a simplified indirect proportion method. The resistance strains were then determined by percentage of colonies that grew on the critical concentration of Isoniazid, Streptomycin, Rifampicin and Ethambutol.

Results: The overall resistance of all forms of TB to any first-line anti-TB drug was 21.7 %. Of the total new and previously treated culture positive TB cases, 15.3 and 48.8 % respectively were found to be a resistant to any of the first-line anti-TB drugs. Further, of all forms of TB, the overall resistance of MDR-TB was 4.7 %. However, of the total new TB cases, 2.4 % had primary while 14.3 % had secondary MDR-TB. Resistance to any of the first-line anti-TB drugs (adjusted odd ratio (AOR), 8.1; 95 % CI: 2.26–29.30) and MDR-TB (AOR), 7.1; 95 % CI: 2.6–43.8) was found to be linked with previous history of anti-TB treatment.

Conclusions: The study has identified a high rate of primary and secondary resistance to any of the first-line anti-TB drugs and MDR-TB in the study area. The resistance may have resulted from sub-optimal performance of directly observed treatment short-course (DOTS) programme in the detecting infectious TB cases and cure rates in the study area. Anti-TB drug resistance is linked with previous TB treatment. There is a need to strengthen DOTS and DOTS-Plus programmes and expand MDR-TB diagnostic facilities in order to timely diagnose MDR-TB cases and provide appropriate treatment to prevent the spread of MDR-TB in Ethiopia.