Schistosomiasis  remains   a   major    neglected   tropical Parasitic  disease,  particularly   in   Sub-Saharan   Africa, where around 80-90% of the cases are found (LoVerde, 2019). More than 240 million people are infected in 78 countries, especially in poor settings without access to safe drinking water and adequate sanitation (Steinmann et al., 2006; Colley et al., 2014). In Burkina Faso, Schistosoma mansoni and S. haematobium are present with variable levels of endemicity. But most of the reports on Schistosoma infections are related to urinary schistosomiasis (Poda et al., 2004). S. mansoni has been initially described in the Western and Southern parts of the country (Ouedraogo et al., 2016; Poda et al., 2004).

The current global strategy recommended by the World Health Organization (WHO) to control schistosomiasis is based on preventive chemotherapy or mass drug administration in at risk populations (Assaré et al., 2016; Fenwick and Jourdan, 2020). Since 2002, treatment based on Praziquantel (PZQ) was used for schistosomiasis in endemic countries in Africa. This treatment was supported by the Schistosomiasis Control Initiative Program (WHO, 2002). In Burkina Faso, the national program was focused on children in hyper-endemic areas (Ouedraogo et al., 2016).

Praziquantel (PZQ) treatment has been reported to enhance host protective immunity by exposing parasite antigens (Harnett and Kusel, 1986; Doenhoff et al., 2008). Thus, treatment allows the host immune systems to recognize Schistosoma adult worm antigens and to develop protective immunity (Mutapi et al., 2005). In addition, previous studies have shown tremendous variation in the changes in immune responses after chemotherapy between different human populations (Mutapi, 2001). Schistosoma specific antibodies appear to play an important role in this protective immunity after treatment. Schistosoma egg antigen-based tests have proven to be more sensitive than worm antigen-based tests (Mott et al., 1987; Hamilton et al., 1999). Their performance in a post-chemotherapy situation remains a subject of debate. Some studies have shown that antibodies against Schistosoma soluble eggs antigens (SEA) decline after treatment within few months (Rabello et al., 1997; Doenhoff et al., 2004 ; Hamilton et al., 1999). Here, we aim to monitor the different immunoglobulin IgG, IgG subclasses, IgM and IgA against SEA eggs and their correlation with egg excretion.

Socio-demographic characteristics of the study participants

Among the 928 participants enrolled, 216 (23.27%) were positive for S. mansoni infection based on microscopy examination. Of the 216 participants with S. mansoni infection, 52.78% were children (5-14 years) and 47.22 % were adults (>14 years). The majority of the positive participants had a light infection (77.31 %) with egp <100 (Table 1).

Parasite change evolution after treatment during the follow-up time

At the inclusion, the mean number of eggs was 26 ± 2.11 and during follow-up, there was a reduction of about two eggs at each visit and this reduction was statistically significant (p=0.0006) (Figure 1).

Factors associated with parasite egg load evolution during the follow-up time

The only factor associated with the reduction of the parasite egg count during follow-up was a high IgA titre. Indeed, at each visit, each increase of 1 unit in IgA titre was associated with a significant reduction in the parasite egg  load  of  50  eggs  (p =  0.002).  IgG1 and IgG4 were good markers of an increased parasite egg count. In fact, at each visit, the 1-unit increase in IgG1 and IgG4 titres was associated with a significant increase in the parasite egg count of 21 and 32, respectively (Table 2).

Immunoglobulins evolution after treatment during the follow-up time

The evolution of the different antibody titres during follow-up is shown in Figure 2. The immunoglobulins IgG, IgG1, IgG2 and IgG4 titres decreased significantly during the follow-up time (p<0.0001). In contrast, the titre of IgG3 increased significantly (p=<0.0001). The variation of IgA and IgM titres that was observed was not statically significant.

The  infection intensity reported in our study included light infection levels for most participants, as previously reported, in the same locality (Sorgho et al., 2005). Our results showed a significant decrease in the parasite egg load during the follow-up time. This result was expected, supporting the well-documented effect of PZQ in the significant reduction in egg load after intervention and during follow-up (Reta and Erko, 2013; Bajiro et al., 2016).

The immunoglobulin IgA response led to a reduced egg number, whereas IgG1 and IgG4 titres increased in response to egg excretion. This observation is supported by a previous study that observed a tendency for Schistosoma whole worm antigen–IgA (anti-WWA-IgA) levels to be elevated (Fukushige et al., 2019). IgA response led to a significant reduction in the egg number during the follow-up. Some subjects might have been re-infected during the follow up, which could have induced the increased response of IgA. Indeed, the participants in this study work in rice fields, which explains the continuous exposure to re-infection. It has been shown that the immunoglobulin IgA response increases after S. mansoni egg deposition in the intestines (Poulain-godefroy et al., 1996).

In addition, the increase of IgG1 and IgG4 titres is found to be associated with significant increases in the egg number in this study, which  might  be  related  to the presence of egg excretion by the parasite. The increased titres of IgG1 and IgG4 could be a response against re-infection after treatment. In addition, PZQ kills only mature worms, so immature worms may escape treatment. Thus, the time interval between each monitoring period could allow the immature worms to mature and explain the excretion of eggs or reinfection. Previous studies have shown that IgG4 response is associated with higher parasite burdens and susceptibility to reinfection post-treatment (Mutapi, 2001; Satti et al., 1996).

Regarding the evolution on antibody response, the significantly decreased level of IgG, IgG1, IgG2 and IgG4 titres during the follow-up time is associated with the reduction of parasite egg excretion after treatment. Similar observations have been reported previously (Fukushige et al., 2019). In contrast, IgG3 titres increased after treatment during the follow-up. This result is similar to a previous observation in one year post-treatment (Abebe et al., 2001). Immunoglobulin IgG3 response was observed to kill schistosomula in the presence of activated eosinophil (Chisango et al., 2019). The IgG3 responses could be a response to the parasite stage of those that escaped the PZQ treatment. The main limitation of our study was the loss of follow up during each  follow   up  visit.   Although,   to  our  knowledge  no further study has been carried out before now on the study area despite the fact that the data had been collected for a long time. Thus, data might be some indication of schistosomiasis situation in the study area.

Praziquantel treatment reduced the S. mansoni egg load one year post-treatment. Immune responses are potentials factors associated with a significant reduction in the parasite egg load. The titres of IgA, IgG1 and IgG4 are found to be associated with parasite egg load and could be a good marker for treatment efficacy. 

The authors have not declared any conflict of interests.

This research was funded by UNDP / World Bank / WHO Special Programme for Research and Training in Tropical Diseases (TDR). The authors would like to thank the district health workers at Kou Valley, and also the school and local community at Kou Valley.