The burden of malaria in Sudan: incidence, mortality and disability – adjusted life – years
© Abdalla et al; licensee BioMed Central Ltd. 2007
Received: 19 April 2007
Accepted: 28 July 2007
Published: 28 July 2007
Estimating the burden of malaria in Sudan is important for evidence-based planning of malaria control. Estimates of malaria burden in terms of DALYs (Disability Adjusted Life Years) were not developed locally. This study synthesized information from different sources to calculate malaria incidence, mortality and DALYs lost in Sudan in 2002.
A search for local studies and reports providing epidemiological data on malaria in Sudan was conducted. Preliminary estimates of incidence rate, case fatality rate and mortality rate were developed from the data found. The preliminary estimates were processed in the disease modelling computer software, DisMod II, to produce internally consistent mortality and incidence rates, which were used to calculate DALYs lost due to malaria.
Malaria incidence in Sudan was estimated to be about 9 million episodes in 2002 and the number of deaths due to malaria was about 44,000. 2,877,000 DALYs were lost in Sudan in 2002 due to malaria mortality, episodes, anaemia and neurological sequelae. Children under five years of age had the highest burden. Males had the highest incidence and mortality, but females lost more DALYs.
Formal health system data underestimated malaria burden. The burden estimates can be useful in informing decision making, although uncertainty around them needs to be quantified. Epidemiological research is needed to fill data gaps and update the estimates.
Estimating the burden of malaria is highly needed for evidence based planning of malaria control. In Sudan, malaria has been the subject of a large amount of epidemiological, entomological and biomedical research. Malaria surveillance, as part of the general reporting of health events from health facilities or specific surveillance for epidemic preparedness, provided a wide range of information. This resulted in multiple and diverse sources of information about malaria burden in Sudan, each source serving the purpose for which it was established. The problems with these sources are non-representativeness, variability of the sensitivity and specificity of the diagnostic criteria used and variability of the indices measured. Some may suffer from underreporting. These sources, therefore, could not directly provide a single valid national indicator of malaria burden. Official figures of incidence and mortality reflected cases reported only from the formal health system. Malaria health burden results from both disability and mortality, so that multiple statistics are needed to describe it. DALYs (Disability Adjusted Life Years) are composite indicators that summarize disability and mortality information in a single number . The DALYs approach would be suitable to express the burden of malaria resulting from fatal episodes as well as non fatal episodes and complications. It would also act as a common index to compare the burden of malaria with that of other diseases. Previous attempts to calculate the burden of malaria in Sudan were made as part of the GBD (Global Burden of Disease) study using different indirect methods [2, 3].
No local efforts have previously been made to measure the burden of malaria in terms of DALYs in Sudan, using locally-derived epidemiological data. As part of a project to measure the burden of diseases in Sudan, this study synthesized information about the epidemiology of malaria from different sources to calculate national incidence rate, mortality rate and DALYs lost due to malaria.
The study measured the burden of malaria in 2002 for all Sudan. The burden was attributed to mortality and disability from malaria episodes, anaemia and neurological sequelae, as defined in the GBD 2002 . Multiple levels of malaria endemicity are found in Sudan , and calculations were based on classification of the 26 states of Sudan into hypoendemic, mesoendemic and hyperendemic areas.
Relevant published and unpublished studies were found by electronic search in local databases and Pubmed, using the keywords: malaria, Sudan, Africa, case fatality, age distribution, sex distribution, anaemia, cerebral malaria, and neurological sequelae. Postgraduate thesis archives were hand-searched for thesis not indexed in local databases. Research institutes, governmental and non-governmental organizations were contacted and relevant reports obtained. Reference lists were examined for more research papers. Studies and reports were relevant if they provided at least one of the following: incidence, prevalence, mortality rate, case fatality ratio, age or sex distribution of cases or deaths, remission proportion, average duration and disability proportions. There was no restriction regarding the time of study. Studies identified were reviewed systematically and those selected for use in the calculations were the most representative and with the best methodological quality where applicable.
The total population by age and sex for Sudan in 2002 was interpolated from the 1998 and 2003 population projections of the Sudan Central Bureau of Statistics . Age- and sex-specific all cause mortality rates were obtained from life tables developed by the World Health Organization (WHO) for Sudan in 2002 using indirect demographic techniques . Total population estimates were used to calculate rates and together with all cause mortality rates served as input for computer based disease modelling.
Preliminary incidence of malaria
Preliminary case fatality and mortality rates
Development of internally consistent estimates
Age-sex specific preliminary incidence, mortality and case fatality rates were processed in DisMod II. This is a disease modelling software that uses input estimates to calculate an internally consistent set of epidemiological estimates . The output incidence rates, mortality rates and average duration were used in estimating the epidemiology of neurological sequelae and anaemia, and in calculating DALYs.
Adjusted odds ratios of cerebral malaria  were used to extrapolate proportions of cerebral malaria in hypoendemic and hyperendemic areas from the proportion reported in a mesoendemic area . Adjusted odds ratios of cerebral malaria by age were used to calculate age-specific proportions in each area. The overall proportions in each age group for Sudan were calculated in the same way as the case fatality ratios, and they were used to estimate the incidence of cerebral malaria. The incidence of neurological sequelae was derived by applying the proportion of cerebral malaria episodes that cause neurological sequelae. This proportion together with the remission rate of neurological sequelae was obtained from an African study . Assuming zero case fatality, the average duration was then calculated in DisMod II using the incidence, case fatality and remission rates.
The age-specific proportions of severe anaemia amongst severe malaria cases were calculated using adjusted odds ratios of severe anaemia in the same way as neurological sequelae. Studies reported the ratio of severe anaemia to mild and moderate anaemia [20–22], and the median of these ratios was applied to the proportion of severe anaemia to compute the proportion of episodes developing all degrees of anaemia. Incidence of anaemia was calculated from DisMod II incidence output and the proportion of episodes developing all degrees of anaemia. The case fatality ratio of severe anaemia in children  was used to derive the number of deaths due to severe anaemia. This, together with the number of anaemia episodes in 2002, was used to calculate the case fatality rate. Anaemia remission rate was computed assuming 100% remission of mild and moderate anaemia and 30% remission of severe anaemia in 4 weeks . Age-sex specific incidence, remission and case fatality rates of malarial anaemia were processed in DisMod II to calculate the average duration.
YLLs (Years of Life Lost), YLDs (Years Lived with Disability) and DALYs
According to GBD methods , DisMod II output incidence, mortality and average duration were used to calculate YLLS, YLDs and DALYs, using the following formulas:
• YLL = number of deaths X standard life expectancy at the average age of death
• YLD = number of incident cases/episodes X average duration X disability weights
• DALY = YLL + YLD
Results and discussion
Age and sex specific incidence of malaria per 1000 population in Sudan in 2002
In both males and females the highest incidence was in children 5 – 14 years of age. It declined afterwards and increased again in males in the age group 45 – 59. The incidence was higher in males than in females in all age groups. These age and sex patterns reflect the original patterns in the studies used in estimation of the preliminary incidence rates.
Age and sex specific mortality of malaria per 100,000 population in Sudan in 2002
The total number of deaths in 2002 was estimated to be about 44,000, far exceeding the numbers reported from the formal health system (2,125 deaths) in the same year . This was expected since the formal health system registration did not capture all deaths in the population. Demographic calculations showed that all-cause death registration completeness in Sudan in 2002 was 4.8% . The number of deaths in this study was higher than that estimated in the GBD 2002 , where country specific estimates were based on an analysis by Snow et al .
YLLs, YLDs and DALYs lost due to malaria in Sudan in 2002
The comparability of the results to results of similar studies in other countries was limited by the different methods, case definitions and disability weights used
Role of computer modelling
DisMod II ensured that the estimates used in the final burden calculations were internally consistent. However, large discrepancies were previously found when an empirical data set was compared to DisMod II results and were attributed to data inaccuracies and past disease trends . This emphasized the importance of judgement and expert opinion in processing the input and revising the output of the disease modelling software.
Sources of uncertainty in the estimates
The validity of the results of this study depends on the validity of the data used in their synthesis. Although the best sources available were used, inadequate reports sometimes limited proper study appraisal. In some instances, no single study proved to be the best or most representative, and the results of all the available studies were summarized in one estimate.
The data sources used ranged from health facility based studies to nationally representative population based studies. The former were not representative of the population concerned and some population based studies, NGO surveillance data and national surveys did not cover all the country. Some figures were borrowed from studies in other African countries. However, non representative and non local studies were resorted to only where no local estimates could be found or were too unreliable to use.
Sudan states were classified by endemicity level although administrative boundaries between states did not coincide with boundaries between the different endemicity areas, according to a climate-based distribution model .
Most of the studies used were conducted before or after 2002. This could have affected the validity of the results because their use was based on the assumption of a stable epidemiological and demographic status, which cannot be assumed about malaria in Sudan.
Information about neurological sequelae due to malaria was found only for children less than nine years of age. The findings were generalized from these groups to all age groups due the lack of studies on the other age groups. Findings from northern Sudan were generalized to southern Sudan for the same reason.
Disability weights reflect societal preferences for health states. In spite of the extensive analysis in the GBD to ensure that the disability weights developed were highly reliable , they are expected to vary by the method of health state valuation, by the type of group conducting it and between different populations. Moreover, the case definitions used in the health state valuation of anaemia and neurological sequelae did not always match those of the studies used in the analysis. Uncertainties from these sources were carried over to the burden estimates. The use of extensive calculations in this study emphasized the need for quantifying uncertainty around the results. The complexity in the calculations of epidemiological estimates of malaria in Sudan arose from the complexity of malaria epidemiology. Sudan includes all levels of endemicity, and the variation in clinical presentation and age distribution with endemicity of malaria entailed extensive calculations to estimate age-sex specific rates.
The search conducted in this study revealed the lack of representative and acceptably valid mortality data as well as representative data on case fatality, remission and complications of malaria in Sudan.
The study revealed underreporting of malaria episodes and deaths to the formal health system, with the consequent underestimation of malaria burden. Children less than five years of age had the highest mortality rate and DALYs, emphasizing the known effect of malaria on this population group. Females lost more DALYs than males in all age groups, which altered the picture displayed by the incidence rates alone. The epidemiological estimates and DALYs calculations in this study form a basis for comparing interventions that affect mortality and morbidity differently, by comparing the amount of burden averted by them. The DALYs would mark the position of malaria among the rest of the diseases, if compared to DALYs due to other diseases. Uncertainty around the estimates should be considered when using them for decision making and further work should quantify this uncertainty to facilitate utilisation of the results. The data gaps revealed in this study call for more epidemiological research to fill them. This will allow regular updating of the burden estimates by replicating the calculations using updated input data.
We would like to thank the data collectors and all those who supported this work and supplied data: Planning directorate of the Federal Ministry of Health, University of Khartoum libraries, individual researchers and non governmental organizations. We are grateful for the WHO/Global Programme on Evidence for Health Policy for providing free access to DisMod II, spreadsheets and other helpful material.
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