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The cumulative cases, case fatality rate, and trend in the incidence and mortality rate of visceral leishmaniasis (VL) were investigated in Gadarif State, Eastern Sudan.
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During the 14-year study period (2002–2015), a total of 51 773 patients were registered in Gadarif State with clinical and laboratory evidence of proven VL.
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The trend in VL was considerably higher in the years 2003–2005 as compared to the last 5 years of 2011–2015.
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The highest fatality rate was observed in the year 2002 (4.8%) and it had declined in 2014 and 2015.
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Rural residence was statistically associated with death related to VL (p = 0.021).
•
Immediate interventions are needed in terms of health education and the implementation of preventive measures, with a specific focus on people residing in rural areas.
Summary
Background
Leishmaniasis is one of the neglected infectious diseases of the world. This disease largely affects individuals of low socio-economic level, mainly in developing countries.
Methods
The aim of this study was to investigate the cumulative number of cases, case fatality rate, and trend in incidence and mortality rate of visceral leishmaniasis (VL) in Eastern Sudan. A retrospective descriptive study was performed through analysis of the database managed by the Ministry of Health in Gadarif State, which includes all cases of VL.
Results
Over the 14-year study period (2002–2015), a total of 51 773 patients were registered in Gadarif State with clinical and laboratory evidence of proven VL. The trend in VL was considerably higher over the years 2003–2005 as compared to the last 5 years of 2011–2015. The highest fatality rate was observed in 2002 (4.8%) and it had declined in 2014 (1.1%) and 2015 (1.7%). Rural residence was statistically associated with death related to VL (p = 0.021).
Conclusions
This study showed a high number of cumulative cases of VL in Eastern Sudan. The fatality rate was found to be highest among rural residents and has declined in the last 5 years. Thus immediate interventions are needed in terms of health education and the implementation of preventive measures, with a specific focus on people residing in rural areas.
Leishmaniasis is one of the neglected infectious diseases of the world. It largely affects individuals of low socio-economic level, mainly in developing countries.
Clinically, the disease is characterized by a diverse spectrum of manifestations that develop after infection with protozoan parasites of the genus Leishmania. Features of the disease vary widely, but are often divided into three distinct clinical syndromes, namely visceral leishmaniasis (VL)/kala-azar with its dermatological sequelae (post kala-azar dermal leishmaniasis, PKDL), cutaneous leishmaniasis (CL), and mucosal leishmaniasis (ML).
VL places a huge burden on society in terms of morbidity, mortality, and economic burden. Worldwide, more than 90% of VL cases occur in six countries: Bangladesh, Brazil, Ethiopia, India, South Sudan, and Sudan.
VL is a disseminated protozoan infection, transmitted by sand fly bites, in which macrophages of the liver, spleen, and bone marrow are preferentially parasitized with intracellular replication.
Epidemiological and entomological studies have confirmed Phlebotomus orientalis to be the vector in several parts of Sudan, typically associated with Acacia seyal and Balanites aegyptiaca vegetation.
Sudan has a population of 36.4 million, VL is endemic in seven states and 17 localities, and all clinical forms exist (VL, PKDL, CL, ML). During the period 2002–2011, a total of 29 700 cases were reported, with a case fatality rate of 3.7%.
Gadarif State in Sudan is highly endemic for VL, thus the current study was performed to investigate the cumulative number of cases, case fatality rate, and the trend in incidence and mortality rate of VL, with the aim of providing program managers with the fundamental data necessary for interventions and the implementation of a strategic plan to reduce the incidence rate of this disease in Sudan.
2. Methods
2.1 Study area
Gadarif State is one of the most important states in Sudan and plays a significant role in the economic and agricultural activities of the country. It has a population of 1 727 401 residents, covers 75 000 km2, and lies between latitude 14 and 16 north and longitude 33 and 36 east. The average rainfall is 612 /millimeter. Four rivers pass through the state (Atbara, Elrahad, Saitit, and Basalam) and there are many forests, which provide an excellent environment for the sand fly vector. There are 10 centers for the diagnosis and treatment of VL in the State.
2.2 Study design
To investigate the cumulative number of cases, case fatality rate, and trend in the incidence and mortality rate of VL, a retrospective descriptive study was performed through an analysis of the database managed by the Ministry of Health of Gadarif State, which includes all cases of VL. This database is based on registration at the Department of Infectious Diseases of the Ministry of Health, Gadarif State, Eastern Sudan. The data include personal and social information, the clinical presentation, type of leishmaniasis, follow-up, and the outcome. The outcome is registered as complete recovery, relapse, lost during follow-up, or death; death is registered without further explanation (disease-related or not disease-related). All cases reported during a 14-year period (January 1, 2002 through December 31, 2015) were collected. For each case, the following data were retrieved: sex, age, residence, occupation, and outcome. In accordance with the Sudanese health system, patients aged ≤18 years were considered children.
2.3 Patient management
According to the World Health Organization (WHO), a case of visceral leishmaniasis is a person showing clinical signs of the disease (mainly prolonged irregular fever, splenomegaly, and weight loss) and with confirmation, based mainly on bone marrow aspiration, through direct microscopic visualization or PCR detection.
World Health Organization. Control of the leishmaniasis: report of a meeting of the WHO Expert Committee on the Control of Leishmaniases. Geneva, 22-26 March 2010. Geneva: WHO; 2010. Available at: http://whqlibdoc.who.int/trs/WHO_TRS_949_eng.pdf?ua=1. (Accessed 23 February 2014).
The WHO guidelines were applied for all identified leishmaniasis patients; these guidelines are based on the internationally agreed strategies for the control of the disease.
The recommended treatment regimen in Sudan consists of intravenous sodium stibogluconate 20 mg/kg plus intramuscular paromomycin 15 mg/kg for 17 days as the first-line therapy. In cases with severe side effects, liposomal amphotericin B (Ambisome 3 mg/kg for 10 days) is the second option.
2.4 Analysis
Data were entered into a computer database and SPSS version 16.0 software (SPSS Inc., Chicago, IL, USA) and double-checked before analysis. Trends in the incidence rates and mortality were analyzed by linear regression. Means and proportions of the socio-demographic characteristics were compared between the study groups (patients who died and those who survived), and p < 0.05 was considered significant.
2.5 Ethics
The study received ethical clearance from the Research Board Committee, Gadarif University.
3. Results
3.1 General characteristics
During the 14-year study period (2002–2015), a total of 51 773 patients were registered in Gadarif State with clinical and laboratory evidence of proven VL. Their mean age was 24.1 (standard deviation 18) years. The majority of these patients had less than a secondary level of education (49 201, 95%), were male (37 002, 71.4%), and lived in a rural area (35 611, 68.7%). More than half of the study sample were adults (29 183 adults (56.4%) and 22 590 children (43.6%)). With regard to environmental factors, the majority of the adult study subjects were farmers (75.2%); housewives made up the lowest percentage (7.7%). Out of the 51 773 VL cases, 48 395 (93.5%) recovered completely, 1686 (3.3%) died, 1581 (3%) relapsed, and 111 (0.2%) were lost during follow-up.
3.2 Cumulative number of cases and fatality rate
Table 1 shows the cumulative number of cases and the case fatality rates. The highest fatality rate was observed in the year 2002 (4.8%); this rate had declined in 2014 (1.1%) and 2015 (1.7%) (Figure 2).
Table 1Cumulative number of cases, new cases, and case fatality rate of visceral leishmaniasis in Gadarif State, Eastern Sudan—2002–2015
As seen in Figure 1, the trend in VL was considerably higher over the years 2003–2005 as compared to the last 5 years of 2011–2015. There were three incidence peaks at different intervals (2003, 2010, and 2014).
Figure 1Annual incidence of visceral leishmaniasis in Gadarif State, Eastern Sudan—2002–2015.
3.4 Socio-demographic factors associated with death related to VL
With regard to the socio-demographic factors associated with death related to VL, this study revealed that there was no significant difference in age, education level, or sex between those who died and those who survived. However residence in a rural area was statistically associated with death related to VL (p = 0.021) (Table 2).
Table 2Socio-demographic characteristics and death related to visceral leishmaniasis in Gadarif State, Eastern Sudan
This study provides a 14-year review of the epidemiological trends and patient characteristics of leishmaniasis in Eastern Sudan. This appears to be the largest report of VL for the country. The main finding of this study was the high number of cumulative cases of VL in Eastern Sudan. There was a clear decline in the fatality rate from the year 2002 to the year 2015. The disease was observed to be more prevalent among adults and males, and the number of deaths was higher among those living in a rural area. This indicates that Gadarif State is an area endemic for leishmaniasis. The disease is also endemic in neighboring countries bordering Sudan, including Ethiopia, Kenya, and South Sudan.
The current study showed three incidence peaks at different intervals (2003, 2010, and 2014). The variation in the number of cumulative cases of VL and the incidence peaks may be due to the variations in rainfall during the study period. The difference in rainfall is a factor recognized to be associated with a person's vulnerability to infection.
This study showed that the case fatality rates were higher in the first 9 years and declined in 2011–2015. This could be due to patient awareness, the adoption of new treatment guidelines, the introduction of nutritional supplements for all kala-azar patients, and the expansion of treatment facilities, among others.
In line with the present results, VL has been shown to be more prevalent among males in many reports and this is explained by the greater exposure of males than females to the sand fly vector due to differences in occupation.
Usefulness of the rK39-immunochromatographic test, direct agglutination test, and leishmanin skin test for detecting asymptomatic Leishmania infection in children in a new visceral leishmaniasis focus in Amhara State, Ethiopia.
Furthermore, in neighboring Ethiopia, Ali et al. and Alvar et al. reported that the majority of VL cases occur in males, a pattern caused by increased exposure to the sand fly vector during agricultural work and other work in the field.
The association between rural residence and death related to VL may be attributed to poverty, low immunity, food insecurity, malnutrition, and limited access to treatment services and thus late presentation.
One of the major limitations of this study is that the nutritional status and socio-economic status were not assessed due to logistical constraints. Also there were no data available on HIV or other co-infections with VL. Therefore it is necessary to conduct studies to investigate whether the patient's nutritional status or socio-economic status predisposes them to VL infection and whether these constitute a risk factor for death related to VL.
In conclusion, this study showed a high number of cumulative cases of VL in Eastern Sudan. The vast majority of infected people were male and adult. The fatality rate was highest among rural residents, and it declined over the last 5 years of the study. Thus immediate interventions are needed in terms of health education and the implementation of preventive measures, with a specific focus on people living in rural areas.
Acknowledgements
We are grateful to the staff of the Ministry of Health, Gadarif State, Department of Infectious Diseases for their great assistance and cooperation. The authors also acknowledge the Kala-azar Research Centre (KRC) at Gadarif University for consistent and high-level support of operations research in the context of visceral leishmaniasis.
Funding: None.
Conflict of interest: We declare that we have no conflicts of interest.
References
Alvar J.
Vélez I.D.
Bern C.
Herrero M.
Desjeux P.
Cano J.
et al.
Leishmaniasis worldwide and global estimates of its incidence.
World Health Organization. Control of the leishmaniasis: report of a meeting of the WHO Expert Committee on the Control of Leishmaniases. Geneva, 22-26 March 2010. Geneva: WHO; 2010. Available at: http://whqlibdoc.who.int/trs/WHO_TRS_949_eng.pdf?ua=1. (Accessed 23 February 2014).
Usefulness of the rK39-immunochromatographic test, direct agglutination test, and leishmanin skin test for detecting asymptomatic Leishmania infection in children in a new visceral leishmaniasis focus in Amhara State, Ethiopia.
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