Scorpion stings envenomation in Sudan: a retrospective study of hospital-based incidence

Abstract Scorpion stings are a common medical emergency in many parts of the world. However, no statistical records are available about the incidence of scorpion sting envenomation and related mortality rates in the Sudan. This study aimed to describe the burden in the Sudan and to highlight the most affected states. We extracted retrospective hospital-based data on scorpions’ stings envenomation for the years 2014–2018 from the annual statistical reports of the Federal Ministry of Health, Republic of the Sudan. Descriptive statistics were used to analyze the extracted data and elucidate the results. A total of 129,427 people were envenomed during 2014–2018 with a mean of 25,885 cases/year. More adults were stung compared to children. However, mortality was higher among children younger than 15 years old 4.7% (186/3974) than older victims 1% (56/5371). Envenomation was more frequent in males (56%) than females (44%). The Northern state reported the highest incidence of scorpion stings (344 per 100,000 population), followed by the River Nile state (240 per 100,000 population), and Khartoum state (174 per 100,000 population). Fatalities amongst hospitalized patients were 2.6% (242/9345) with the Northern state accounting for 34% (0.8/2.3) of total fatalities reported.


Background
Scorpion stings are a major public health problem in many parts of the world, especially Northern and sub-Saharan Africa, the Middle East, Southern Africa, Latin America, and South Asia.Worldwide, the annual estimated number of scorpion stings exceeds 1.2 million, leading to more than 3000 deaths [1].Although most scorpion stings cases are minor leading to localized pain without systemic envenomation, a third of stings cause severe and sometimes fatal envenomation especially amongst children [2][3][4][5].
Scorpions are predatory arachnids of the order Scorpiones.They are nocturnal animals commonly found in deserts and dry environments spending the day hidden under rocks and wood logs [6,7].Some species have shown a great adaptation to different environmental conditions and can live on most terrestrial environments extending from the central parts of America, Europe, and Asia to the southern parts of Latin America, Africa, and Australia [1].Worldwide, over 1500 species of scorpions have been identified; approximately, 30 species can cause life-threatening systematic envenomation.The most dangerous and medically important species belong to the Buthidae family [1, 3,8].
Most scorpion stings occur in summer, mainly during the night [1].Intense pain results from opening sodium (Nav1.7)channels and closing potassium channels [9][10][11][12].Scorpion envenomation may also have cardiovascular, respiratory, or hematologic effects [3,13].The severity of envenomation depends on the scorpion species, body mass of the victim, the volume of venom injected, the site of sting, and the health status of the victim [8,9].
In Sudan, data regarding the distribution of scorpions has been limited.However, the diverse ecosystems present in the country (the desert and the Nile valley in the North, the coastal regions in the East, and subtropical savannahs in the West and South) present suitable shelter for scorpions.In 1925, King [6] recorded 13 species of scorpions from Sudan representing five genera: Buthus, Nanobuthus, Parabuthus, Uroplectes, and Pandinus, although little was known about the dispersal of the 13 species recorded.A 2018 report listed seventeen scorpion species; including 15 Buthidae and two Scorpionidae [14].The most dangerous Sudanese scorpion species are Androctonus amoureuxi (African fat-tail scorpion), Androctonus australis (yellow fat-tailed scorpion), Parabuthus abyssinicus (Ethiopian thick-tail scorpion), and Leiurus quinquestriatus (death stalker) [15,16].
We describe the burden of scorpionism in the Sudan and highlight the most affected geographical areas.

Methods
We analyzed retrospective hospital-based data of scorpion stings cases from 2014 to 2018 to determine the incidence of scorpion stings envenomation and death in the Sudan.We extracted these data from the Ministry of Health's Annual Health Statistical Reports for the years 2014-2018.We acquired population estimations from the Central Bureau of Statistics in the Sudan according to the 2008 population census.We classified scorpion stings cases according to sex, age, geographical location, in-patient versus outpatient, and mortality rate.In this study, we considered the Kordofan region states (North, South, and West) and Darfur region states (North, South, East, West, and Central) as one state in each case in order to overcome the geopolitical and administrative changes and challenges related to political changes which had resulted in the creation of new states within the Darfur and Kordofan regions.We used descriptive statistics including percentages and incidence ratios to interpret the results using Excel Microsoft 2016 (Microsoft, Redmond, WA).We used Geographic Information System (GIS) methods using ArcMap software version 10.2 (Esri, Redlands, California, USA) to compare state-wise incidence of scorpion stings.

Results
A total number of 129,427 people were envenomed during 2014-2018 with an average of 25,885 cases/ year.Figure 1 illustrates the incidence of scorpion sting envenomation per 100,000 populations.Scorpion stings were more frequent amongst people aged ≥ 15 years (68%) compared to children younger than 15 years old (32%), with the age group (15-24 years old) demonstrating the highest proportion of envenomation (28%) (Figure 2).Males more frequently received stings (56%) (Figure 3).
A total of 9345 patients were admitted to the hospital between 2014 and 2018 due to scorpion stings envenomation, with a mean of 1869 admitted patients per year.Children younger than 15 years old constituted 42.5% of all admissions (3974/9345), with 5371 patients older than 15 years of age admitted.Fatalities reported among inpatient cases were 2.6% (242/9345) of all admissions (Figure 4).Of these 242 deaths, 186 deaths were in children younger than 15 years old representing 77% of all fatalities (Figure 5).A higher proportion of deaths of 4.7% (186/3974) were recorded amongst admitted children compared to 1% (56/5371) amongst older patients.
Analysis of the geographical distribution of scorpion stings cases revealed that the Northern state had the highest incidence of envenomation (344/100,000 population), followed by the River Nile state (240/100,000 population), and the capital, Khartoum state (174/100,000 population).The regions of Kordofan and Darfur states had the lowest incidence of envenomation, according to hospital records (Figures 6 and  7).Fatality amongst inpatients due to scorpion stings envenomation was highest in the Northern state accounting approximately 34% of total reported scorpion sting fatalities in the country, followed by Kassala state (30%) (Figure 7).

Discussion
Data on scorpion stings epidemiology are poorly documented in the Sudan despite the high estimated incidence [11].To our knowledge, there are no previous published studies describing the incidence of scorpion stings envenomation throughout the Sudan,      based on hospital records.However, hospital-based records might underestimate the burden of scorpion envenomation, as the majority of scorpion stings cases result in localized pain without systemic envenomation [1,11,17,18] and do not require hospital admission.In addition, the shortage of medical facilities, particularly in the rural and peripheral regions of the Sudan, has led residents to resort to traditional healers and methods for treatment.Therefore, hospital-based records may not reflect the true burden of scorpion sting envenomation in the country.
We identified the highest incidence of scorpion stings in the Northern and River Nile states.The two states are semi-desert to poor savanna, and traversed by the River Nile, thereby presenting a suitable habitat for scorpions.L. quinquestriatus and A. amoureuxi inflict the majority of stings in these two states [15].Furthermore, the construction of the Merowe hydroelectricity dam in 2009, affected areas of the Northern and River Nile states through changes to the local ecology and displacement of scorpion populations from their natural habitats to nearby human populations.Moreover, the expansion of artisanal gold mining activities in both states may have contributed to the increased incidence of scorpion stings due to the increased human scorpion contact in these desert mining sites and the disturbance of local scorpions' habitats and populations.
A. amoureuxi, P. abyssinicus, and L. quinquestriatus are most common in Khartoum state.Conditions that may favor scorpion envenomations include the annual flooding of the River Nile displacing scorpions from the river banks and expansion of the urban area into scorpion habitats [15,25].Other factors that play include the urban expansion of the capital city Khartoum, which has encroached on and disturbed previous natural scorpion habitats.However, the estimated scorpion sting mortality in Khartoum state (0.1/100,000 population) compared to the rate of incidence is low, and this might be a reflection of relatively better medical care in the capital city, compared to the more rural and underdeveloped regions of the country.
Kassala state came in fourth place regarding scorpion sting envenomation while reporting the second place for inpatient fatality after the Northern state.The two medically important species recorded in this state are Leiurus quinquestriatus, and Parabuthus abyssinicus [15].The higher fatality rate seen in Kassala may result from delays to reaching health care.
The regions of Kordofan and Darfur documented the lowest cases of hospital-based envenomation despite the wide distribution of Androctonus amoureuxi and Leiurus quinquestriatus in the two regions [15].Military action and insecurity in western regions in Sudan may have affected the quality of statistical records.
Throughout Sudan, factors contributing to morbidity and mortality of scorpionism include poverty and insufficient health care resources [26].
Limitations of this study include retrospective data collection only from hospital records.These data likely underestimate the true incidence of scorpionism.Hospital records often lacked information on the scorpion species, the severity of symptoms, and the use of antivenom.

Conclusion
An average of 25,885 people per year was envenomed secondary to scorpion stings in the Sudan between 2014 and 2018.Males were more likely to be stung than females.More adults sustained scorpion stings compared to children but the fatality rate amongst children was higher.The geographical distribution of scorpion envenomation demonstrates the highest incidence in northern Nile riverine states in addition to Kassala state, Eastern Sudan.

Figure 1 .
Figure 1.incidence of recorded scorpion stings in sudan through the years 2014-2018.

Figure 2 .
Figure 2. The percentage of scorpion envenomation according to age groups.

Figure 3 .
Figure 3. scorpion stings cases through the years 2014-2018 according to age and sex.

Figure 4 .
Figure 4. scorpion stings cases and death among inpatients during the years 2014-2018.

Figure 5 .
Figure 5.The percentage of death due to scorpion envenomation according to age groups among inpatients.

Figure 7 .
Figure 7. incidence and deaths due to scorpion stings in sudanese states through the years 2014-2018.