Background
Intestinal helminth infections are among the most common infections worldwide. Globally 4.5 billion people are estimated at risk and more than 2 million are ill as a result of soil-transmitted helminths (STHs) infections in areas where sanitation is inadequate and water supplies are unsafe [
1].
Schistosomiasis is also a common helminthiasis affecting more than 200 million people globally [
1]. The global disease burden caused by schistosomiasis alone is estimated at 4.5 million disability-adjusted life years (DALYs) [
2]. The disease is endemic in many countries of the world with over 90% of cases occurring in sub-Saharan Africa [
3,
4]. Among the world population, it has been estimated that approximately 779 million people are at risk of schistosome infection [
5‐
7].
Schistosomiasis is one of the major public health problems in Ethiopia. The two species of schistosome causing the disease in the country are
S. mansoni and
S. haematobium. Infections by the parasites usually occur in agricultural communities along small streams, irrigation schemes and lakes at altitudes ranging from 1300 to 2000 m above sea level (a.s.l) for
S. mansoni and below 800 m a.s.l for
S. haematobium [
8‐
10]. Regarding distribution of the two schistosome species in Ethiopia,
S. mansoni is widely distributed and
S. haematobium is confined to the lowland areas of the country [
9].
Presence of humans carrying the parasites and fresh water bodies harboring the snail intermediate hosts coupled with the suitable climatic conditions contribute to endemicity of both
S. mansoni and
S. haematobium infections in several localities in Ethiopia [
9‐
16]. Furthermore, population movement and expansion of water resource development projects are playing key roles in establishing the parasite transmission in new areas in the country [
9‐
11]. In Ethiopia,
S. mansoni is transmitted by
B. pfeifferi and
B. sudanica while
S. haematobium is transmitted by
Bulinus abyssinicus and
Bu. africanus snail intermediate hosts.
B. pfeifferi has a wider geographical distribution, whereas
B. sudanica is distributed in few low land areas of Ethiopia [
17,
18]. Even though about 10 bulinid species are reported to exist in Ethiopia, only
Bu. abyssinicus and
Bu. africanus are found naturally transmitting
S. haematobium in the country [
15]. It has been reported in previous studies that
Bu. Abyssinicus serves as the primary intermediate host for
S. heamatobium in Awash valley, whereas
Bu. africanus is dominant in Kurmuk (an area located near to Sudan) [
9].
Although several studies have been conducted on the distribution and prevalence of intestinal helminthiasis and schistosomiasis in other parts of Ethiopia [
9‐
19], only limited work was done to determine the prevalence and associated risk factors for these infections in rural villages in the present study area [
19]. No epidemiological studies focusing on the parasite and intermediate hosts have been conducted in the area to determine the establishment of
S. mansoni transmission. Therefore, the present epidemiological study aimed to assess the prevalence of
S. mansoni and other intestinal helminth infections among school children and determine the establishment of
S. mansoni transmission in the study area by conducting parasitological and malacological techniques as well as by establishing infections in lab-bred mice.
Discussion
Intestinal helminth infections are common public health problems in areas where sanitation is inadequate and water supplies are unsafe. Among these infections, soil transmitted helminthiasis due to
A. lumbricoides, hookworms and
T. trichiura, and schistosomiasis due to
S. haematobium and
S. mansoni are the most common in sub-Saharan Africa [
29] These infections also remain considerable public health problems in Ethiopia and knowledge of high-risk localities is required to inform control interventions in such areas. Even though the mapping of schistosomiasis and soil-transmitted-helminthiasis have already been done in Ethiopia, continuous survey of the disease is needed to accommodate recent discoveries of new transmission foci possibly associated with expansion of water development projects and human movement in the country [
14]. In line with this, there are recent reports on intestinal helminthiasis including schistosomiasis from the present study area [
19,
30]. In the present study, the prevalence of intestinal helminth infections was determined and the endemicity of
S. mansoni infection was established for the first time as evidenced by both parasitological and malacological surveys. The overall 72.3% prevalence of intestinal helminths including
S. mansoni infections found in this study showed that intestinal helminth infections represent a considerable health problem in the study area.
In this study, varying magnitude of prevalence of infections by
S. mansoni, hookworms
, A. lumbricoides, T. trichiura, Taenia species,
H. nana and
E. vermicularis were found. These infections occurred in almost all of the areas under study. The distribution of these parasites over the study sites might reflect the existence of comparatively similar level of intestinal helminth infection condition in the area. Regarding STH infection, hookworms and
A. lumbricoides were the major parasites identified in this study. The prevalence of hookworm infection (27.6%) found in this study is higher than the estimated national prevalence 16% [
31] and this is in line with previous studies done in the country [
30‐
37]. On the other hand, the prevalence of
A. lumbricoides (8.9%) is quite lower than the estimated national prevalence 37% [
31]. There are previous studies which reported higher prevalence of ascariasis in the country [
37‐
40]. Infections by
E. vermicularis (2.8%),
Taenia species (2.6%),
T. trichiura (1.2%)
and H. nana (0.6%) were also recorded at low prevalence in the present study. Such variations in prevalence of helminth infections are likely attributed to variations in appropriate water supplies, sanitation, hygiene (WASH), among other things.
The prevalence of
S. mansoni infections in 503 school children of 5 selected primary schools in Wolaita Zone, southern Ethiopia was found out to be 58.6%. This finding is lower than the previous 81.3%
S. mansoni infection prevalence reported from one of the primary schools, Demba Girara, in a village of the present study area [
19]. The lower prevalence in the present study might be due to variation of localities from where the school children were sampled. The current finding on
S. mansoni infection prevalence was also lower than the 82.8% prevalence reported from Sanja area, northern Ethiopia [
35] and 73.7% from Bushulo village, southern Ethiopia [
36]. On the other hand, the current
S. mansoni infection prevalence is higher than similar studies done on school children [
37‐
42]. The higher
S. mansoni infection prevalence in the present study might be due to the absence of clean water supply, lack of awareness on the disease and hence the absence of schistosomiasis control measures in the study area. Inhabitants of the area largely depended on open water sources for domestic and recreational use. The fact that inhabitants of the study area have no awareness on the existence of schistosomiasis manifested in that the disease was highly neglected in the area. Open defecation near water sources might have also increased the transmission of
S. mansoni in the present study area.
The higher
S. mansoni prevalence among male children might be due to the observed higher frequency of contact with cercariae contaminated water bodies than females. This finding is in agreement with previous studies done elsewhere in the country [
19,
43‐
46]. The increased
S. mansoni infection among male children could also be due to herding cattle near cercariae contaminated water bodies as this is an outdoor activity which is mostly practiced by male children in the study area. Similar explanation was given by the study done previously around the present study area [
19]. The variation in
S. mansoni infection prevalence (ranged 5.1% to 75%) among the primary schools might be due to the differences in altitude, microclimate and level of dependency in open water sources of the localities. The lower prevalence (5.1%) at Ello primary school might be due to relatively lower altitude (1400 m above sea level) of the area. In area with lower altitudes where the water environments experience relatively higher temperature which may affect survival of snail hosts and parasites [
47].
All three classes of intensity of infection by
S. mansoni were found in the present study with highest heavy infection intensities observed in the 10-14 years age group from age category, males from sex category, Motala from school category, those who had frequent water contact and those who swam in infectious water sources. The reason for finding higher heavy infection in these specified categories of children could be due to the frequent exposure to
S. mansoni infection [
18,
46,
48]. The age-specific association of infection intensity in current study is also in agreement with the finding of previous study done in a village close to the present study area [
19]. The highest heavy infection intensity observed in Motala primary school might be attributed to the absolute dependency of inhabitants on Bisare stream which was highly infested with infected snails. The sanitary condition of water environment was also very poor as high fecal contamination was observed along the course of the stream in general and several human-water contact points in particular at Bisare.
The present study showed that the frequency of water contact was the most associated risk factor for
S. mansoni infection in that school children who swam in rivers and streams were three times more likely to be infected with
S. mansoni than those who did not swim. Other previous studies also found swimming to be a common risk factor for
S. mansoni infection. Although herding cattle near streams and rivers was significantly associated risk factor to
S. mansoni infection in the previous study done in a village of the study area [
19], the present study found no statistically significant association with the activity.
S. mansoni endemicity speculated in earlier study [
19] was confirmed by the present study through survey of snail intermediate host, shedding of
S. mansoni cercaria from the
B. pfeifferi snails and identification of the parasite in mice infection model. Survey for
B. pfeifferi was conducted at water sources of areas where schistosomiasis is determined. The snail survey showed more abundant
B. pfeifferi in Bisare and Kote streams than in Himbecho irrigation canal. Presence of less abundant
B. pfeifferi in Himbecho irrigation canal might be due to sparse vegetation coverage of the canal. The slow water flow and abundant aquatic vegetation made Bisare and Kote streams favorable habitats for
B. pfeifferi and other snails including
Bulinus species and
Lymnaea natalensis [
16]. Even though Woibo and Adacha rivers were suspected for
S. mansoni infection, only few young
B. pfeifferi snails were observed along these rivers. The absence of adult
B. pfeifferi snails could be due to the reason that the survey was made a week after unexpected heavy rainfall in the area due to the El Nino effect. Among the physical variables of water environment, substrate, vegetation density and water velocity are the strongest predictors of snail presence [
49]. During the rains, snail occurrence and density are even more affected in relatively large streams and rivers [
49]. In contrast to the high
S. mansoni infection prevalence (58.6%) found in this study, a very low proportion of
B. pfeifferi snails collected in the present survey were shedding
S. mansoni cercariae. This finding is in agreement with other studies done in endemic areas with high transmission where few or none of the snail hosts collected shed any schistosome cercariae [
50,
51]. In a previous study done in Msambweni area, coastal province of Kenya, where high prevalence of human schistosomiasis occurred, it was observed that very low proportion of snails were found shedding schistosome cercariae [
52]. Therefore, the higher schistosomiasis transmission in an area may not always coincide with the greater proportion of host snails shedding schistosome cercariae. The possible explanation given for this unexpected low cercariae shedding from the snail intermediate hosts, as mentioned in previous studies, could be the variation in percentage of infected snail, focal nature of schistosomiasis, dispersed distribution of infected snails and seasonal differences [
51,
52].
Acknowledgements
The authors would like to thank Wolaita Sodo University (WSU) for hosting the study. We also acknowledge Aklilu Lemma Institute of Pathobiology (ALIPB), Addis Ababa University, for collaborative work on snail identification, cercariae shedding and mice infection and definite identification of the schistosome species. We are thankful to the laboratory and field technicians of WSU and ALIPB for their assistance during field and laboratory work. Mr. Sisay Dessie of ALIPB deserves a particular appreciation for his technical assistance in collecting and maintaining snails and mice in the laboratories. Our gratitude is also extended to the health and education offices of Wolaita Zone and their respective district administrators for their cooperation during the study period.