Background
Schistosomiasis is a neglected tropical disease which is highly prevalent in sub-Saharan Africa. An estimated 93% of the approximated 290 million people affected by the disease worldwide are living in the region [
1‐
3]. Approximately, 120 million people have schistosomiasis related symptoms and the disease accounts for over 2.8 million years lived with disabilities [
2]. In the region of sub-Saharan Africa, schistosomiasis is due to
Schistosoma mansoni causing intestinal schistosomiasis and
S. haematobium causing urogenital schistosomiasis [
4]. Intestinal schistosomiasis caused by
Schistosoma mansoni remains an important public health concern in Sub-Saharan Africa and is associated with significant morbidities [
3‐
5]. Chronic
S. mansoni infection is associated with hepatosplenic disease characterized by hepatomegaly, splenomegaly and progressive periportal fibrosis which can lead to portal hypertension, esophageal varices, liver surfaces irregularities, portal-systemic venous shunts and haemetemesis [
3,
6,
7]. Many of these
S. mansoni related morbidities can be detected and measured by ultrasonography and classified according to the World Health Organization grade scales using the Niamey protocol [
8,
9].
Available evidence indicates that an estimated 8.5 million cases of chronic hepatosplenic schistosomiasis are attributed to
S. mansoni infection in sub-Saharan Africa [
3,
4]. The underlying pathophysiology is the immunological response to
S. mansoni eggs which are carried to the liver by the blood stream. The eggs are trapped in the liver tissue around branches of the portal vein and provoke an inflammatory response mediated by CD4
+ T-lymphocytes. Finally, this results in small fibrotic scars and over time it leads to periportal fibrosis. This process is considered to be the main pathogenetic process of portal hypertension and other hepatosplenic complications of schistosomiasis due to
S. mansoni [
7,
10]. In contrast the habitat of adult
S. haematobium are the venous plexus of the urogenital organs which do not drain into the portal vein.
S. haematobium is not associated with periportal fibrosis therefore. It is worth noting that epidemiological and demographic factors such as duration of residence in endemic areas [
11,
12], involving in fishing activities [
12], parasitological factors (low versus heavy infection intensities) [
13], age (children versus adults) [
5] and genetic factors [
14] can contribute to development of hepatosplenic disease in endemic populations.
The World Health Organization data indicate that after Nigeria, Tanzania has the highest number of schistosomiasis cases in sub Saharan Africa [
15]. In 2012 it was estimated that about 52% of the Tanzanian population (23 million people) are infected with schistosomiasis [
15,
16]. The projected population of Tanzania currently stands at 55 million people [
17]. In Tanzania, schistosomiasis is caused by
S. mansoni and
S. haematobium [
5].
Schistosoma mansoni is focally distributed and commonly found along the large water bodies such as the Lake Victoria [
5]. Indeed, multiple studies indicate, that the species
S. mansoni is the by far predominant cause of schistosomiasis along the shoreline of Lake Victoria and on its islands [
5,
12,
13,
16,
18,
19,
20,
21,
22]. Communities living there are disproportionally highly affected by the
S. mansoni-specific pathology and a number of studies have reported a high prevalence of hepatosplenic morbidities in this region [
5,
12,
13,
23,
18]. A study among 360 school children on Ukerewe Island in Lake Vicctoria found splenomegaly in 90,7%, right liver lobe hepatomegaly in 89% and overt signs of periportal fibrosis in 5,4% of the participants [
5]. The disease is highly common among school children and adults [
19,
24], of recent, data have emerged showing that pre-school aged children are also infected and carry heavy infection intensities [
20].
At present, the main control approach against intestinal schistosomiasis in Tanzania focuses on mass drug administration (MDA) with praziquantel [
5]. The MDA approach mainly targets school aged children (SAC) or children attending primary schools and drugs are offered at the school environment [
25]. This approach has been advocated as very cost-effective, especially when drugs are distributed irrespective of the infection status. Repeated rounds of MDA have been reported to result in reduction of prevalence of infection, intensity of infection and reversibility of enlarged organs [
25,
26,
27]. It should be noted that despite the implementation of several rounds of annual MDA in Tanzania, the prevalence of the disease remains very high in many areas surrounding Lake Victoria [
5,
19,
20,
21]. It is unlikely that a control strategy based on MDA alone will result into the interruption of transmission and elimination of the disease in high prevalence areas. Understanding this, World Health Assembly (WHA) in its 2012 resolution 65.21 [
14] called for integrated control approaches which are mainly characterised by inclusion of public health education, access to clean water, improved sanitation and snail control into the MDA program [
24]. Following this concept, we launched a pilot study on Ijinga island in Lake Victoria where we combine an intensified MDA program with repeated health education and WASH interventions. In preparation of this 5-year project, we collected baseline data which will be useful for monitoring the impact of the implemented intervention measures at the study area. Thus, the present study reports data on
S. mansoni prevalence, intensity of infection, related hepatosplenic morbidities and their associated factors.
Discussion
The findings from this study indicated that Ijinga Island is highly endemic for S. mansoni infection. The prevalence of S. mansoni and its related intensity of infection is high in all age groups. Furthermore, our findings noted a difference in case detection of S. mansoni infection between Kato Katz (KK) technique and point-of-care Circulating Cathodic Antigen test. The POC-CCA test detected more cases of the disease than KK technique. The findings further noted that S. mansoni related hepatosplenic morbidities are also common in all age groups and both sexes. Heavy intensity of S. mansoni infection was associated with hepatomegaly and splenomegaly. A number of demographic and epidemiological factors were noted to be partly contributing to the development S. mansoni related hepatosplenic morbidities in the study area.
Findings on the prevalence of
S. mansoni infection on Ijinga Island corroborate the results of previous studies which demonstrated that communities along the southern shore line of Lake Victoria and its Islands carry the highest burden of the disease [
12,
13,
18,
19,
23,
35]. Our findings noted a very high prevalence using both KK technique and POC-CCA test. Based on KK technique, the prevalence of
S. mansoni observed in this study was lower than the 78% [
18] and 86.3% [
13] recorded at the nearby Island of Ukerewe north-western Tanzania. Other previous studies in the same area have recorded lower prevalences [
19,
23] than in the present study. A possible explanation could be the low rate of participation in previous MDA campaigns (12.8% acc. to the questionnaire) of the Ijinga community. The age and sex differences in
S. mansoni infection status recorded in this present study were comparable to results of previous similar studies conducted in schistosomiasis endemic areas [
18,
36,
37]. The variations in
S. mansoni prevalence between age groups and sex is mainly explained by varying patterns of exposure to risk areas (water contacts) and development of acquired partial immunity [
13,
36,
38]. The high prevalence of > 50% of
S. mansoni infection in all the age groups based on KK technique and POC-CCA test indicate that Ijinga island is an old focus for
S. mansoni transmission and for successful control of the disease and its related hepatosplenic morbidities, the entire community should receive at least two rounds of MDA per year according to WHO recommendation [
39].
Of note to our findings is the high prevalence of
S. mansoni infection in pre-school age children (≤6 years) based on both KK technique and POC-CCA test. The age group had also high intensity of
S. mansoni infection compared to the older age group. These findings indicate that,
S. mansoni infections starts at an early age and with heavy infection intensities, the age group is likely to start developing hepatosplenic disease at early age. At the time these children reach maturity if left untreated, are likely to end up with severe hepatosplenic disease [
40]. Similar studies in East Africa have recently reported a high prevalence and intensity of infection of
S. mansoni in the same age group using both KK technique and POC-CCA test [
20,
22]. It is worthwhile noting that the use of KK technique alone in PSAC children results into underestimation of the prevalence of the infection. Therefore, it remains important to combine this technique with a more sensitive diagnostic technique such as POC-CCA test to increase the detection of true cases of the disease in this age group [
20,
41,
42]. In our present study, almost 41% of the pre-school children were missed by KK technique. Taking into account that the peadiatric formulation of praziquantel will be available in the near future [
40,
43], which will allow including of PSAC into the MDA program, it is important to include a more sensitive diagnostic test for case detection in this age group and for monitoring of drug efficacy [
40].
The results of the present study show that ultrasound detectable hepatosplenic morbidities are common among our study population and almost exclusively are attributed to
S. mansoni infection. Our results confirm the findings of the previous studies conducted in the same region which noted different patterns of organ morbidities in communities living along the shoreline of the lake and on islands [
12,
13,
18,
21]. The common hepatosplenic morbidities detected in the present study population were periportal fibrosis (PPF), hepatomegaly, splenomegaly, hepatosplenomegaly and gall bladder wall thickening. The prevalence of PPF observed in the present study was lower than the 41% [
18] and 42% [
33] reported from Kome and Msozi village at Ukerewe district respectively. However, other similar studies in the same region have reported lower prevalences than what was recorded in this area [
12,
21]. In the same region, hepatomegaly and splenomegaly related to
S. mansoni infection is a common observation, for instance on Ukerewe Island, 35 and 80% of the studied population had left liver lobe hepatomegaly and splenomegaly [
13]. In the nearby region of Mara, 28.5 and 29.6% of the study participants had splenomegaly and hepatomegaly [
21] while on Kome Island, 68 and 55% of the adult individuals were ultrasonographically detected to have hepatomegaly and splenomegaly [
33]. Authors in previous similar studies have described a number of demographic and epidemiologic factors which partly could explain the variation in prevalence of ultrasound detectable
S. mansoni related morbidities between communities living in different transmission settings [
11,
12,
36,
37].
Interestingly, our findings noted a degree of hepatosplenic morbidities among children aged < 5 years. The main hepatosplenic morbidities observed in the children was mainly left liver lobe enlargement, splenomegaly and only a small proportion of the children had signs of PPF. It should be noted that at such young age, is difficult to precisely classify the liver image pattern/grades as detected by ultrasound [
22]. An intensive inflammatory response due to the accumulation of
S. mansoni eggs in the liver tissue, especially the left liver lobe could partly explain the liver size enlargement in this age group [
7,
38]. Studies have reported an association between the enlargement of the left liver lobe and
S. mansoni infection and its intensity [
11,
36,
37]. The main concern here, is the development of
S. mansoni related hepatosplenic morbidities at such young age and the fact that, to date this age group is not considered for MDA with praziquantel [
40,
43,
44]. At the time when these children will be attending primary school, they are at risk of having already developed advanced stages of hepatosplenic disease. A recent study from Uganda, has pointed out the growing problem of hepatosplenic disease among pre-school aged children living in different transmission settings for
S. mansoni infection [
22]. In this study, PSAC were noticed to have already developed liver image grades suggestive of PPF (Symmer’s pipe stems fibrosis) at six years of age [
22]. This observation is commonly seen in adult population with long-standing infection with
S. mansoni [
18,
45]. Cumulatively, our observation and that of other authors in Uganda [
22] on the development of hepatosplenic disease in this young age group suggest that the period from infection to the development of hepatosplenic morbidities is short compared to previous knowledge based on adult. It seems that
S. mansoni hepatosplenic morbidities in the PSAC have been underestimated if not overlooked in many studies. It is high time now for this age group to be considered for appropriate treatment [
44].
In the present study, the main risk factors associated with PPF were being a male, aged above 16 years and having heavy intensity of infection. The association of male sex with PPF mainly depicts the level of exposure and high infection intensity observed among male individuals in endemic areas [
14,
18,
37]. The relationship between increased age and observation of chronic hepatosplenic morbidities in older ages mainly signifies that,
S. mansoni is a chronic infection which requires time for the overt related morbidities such as PPF, hepatomegaly and splenomegaly to develop [
11,
14,
37]. Risk factors such as village of residence, age, occupation (being fisherman), being male has been shown by previous studies to be associated with PPF in
S. mansoni endemic areas [
11,
36,
37]. Heavy intensity of
S. mansoni infection was also noted in this present study to be associated with PPF. Similar studies have repeatedly described this observation in individuals with severe PPF grades [
14,
37].
On the other hand, our findings noted a significant correlation between the heights adjusted length of the left liver lobe with
S. mansoni intensity of infection, female individuals and age groups. Similarly, young age groups, having detectable
S. mansoni eggs in stool sample and being male were associated with enlargement of the spleen. These explanatory factors have been previous described to interact in causing
S. mansoni related hepatosplenic disease characterized by hepatomegaly, splenomegaly and hepatosplenomegaly in different settings [
11,
36,
37]. In endemic areas, male individuals and children in young age groups are more exposed to water sources than other members of their communities and therefore accumulate heavy intensities of infection with increasing age. This partly explains the high prevalence of some of the hepatosplenic morbidities, for instance PPF and left liver lobe hepatomegaly among male individuals compared to females [
14]. In the young age groups, left liver lobe hepatomegaly and splenomegaly have been noted to correlate with heavy intensities of
S. mansoni infection [
22,
36,
37]. It is worthwhile noting that, in schistosomiasis endemic areas,
P. falciparum malaria is also a cause of hepatomegaly and splenomegaly and differential diagnosis especially in young age groups is a requirement [
46].
The following limitation have to be discussed when interpretation of our results is done. The use of single stool sample for examination may have underestimated the intensity of S. mansoni infection taking into account the day to day variability of parasites eggs output. Also, we did not screen for malaria parasites especially in the young age groups, which could confound our findings on the enlargement of the left liver lobe and spleen.
The prevalence of Hepatitis B surface antigen positive chronic hepatitis B among the adult population of Tanzania is about 7% [
47]. It has to be assumed that co-infections with
S. mansoni are common and chronic viral hepatitis contributes to the severity of liver disease. Nevertheless, the ultrasound patterns of liver cirrhosis or mixed pathology were not detected among our study participants. A screening for HBs-antigen would have required to take a blood sample what we considered to be an obstacle for a high rate of voluntary participation.
Our findings reflect the situation of schistosomiasis in many of the communities living on the islands of Lake Victoria, north-western Tanzania and we consider the conclusions drawn as transferable.
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