Schistosoma haematobium infection modulates Plasmodium falciparum parasite density and antimalarial antibody responses

Abstract

Aims Schistosomiasis and malaria are endemic in sub‐Saharan Africa where Schistosoma haematobium (Sh) and Plasmodium falciparum (Pf) coinfections are thus frequent. We explored the effect of Sh infection on antibody responses directed to Pf merozoite antigens and on malaria susceptibility in Beninese children. Methods and results A total of 268 children were followed during a malaria transmission season. Detection of Pf infection was performed by microscopy and rapid diagnostic tests. Sh infection was determined in urine by microscopy. Antimalarial antibody, cytokine and HLA‐G concentrations were quantified by ELISA. The expression of HLA‐G receptors by immune cells was assessed by flow cytometry. Children infected by Sh had higher concentrations of IgG1 directed to MSP3 and GLURPR0, IgG2 directed to GLURPR0 and IgG3 directed to MSP3, GLURPR0 and GLURPR2 and have lower Pf densities than those uninfected by Sh. No difference in cytokine and HLA‐G concentrations was observed between Sh egg carriers and non‐carriers. Conclusion Schistosoma haematobium modulates host immune responses directed to Pf antigens. The absence of immune downregulation usually observed during helminth infections is surprising in our study. We hypothesize that the stage of Sh development could partly explain the immune pathways leading to increased antibody levels that favour better control of Pf parasitemia.

Exploratory analysis of the effect of helminth infection on the immunogenicity and efficacy of the asexual blood-stage malaria vaccine candidate GMZ2

“…It should be noted that S . haematobium infection had no significant effect on the antibody responses directed to either MSP3 or GLURP, the two antigens combined in GMZ2, in contrast to the findings of a recent study [ 44 ], although the level of anti-GLURP IgG concentration was indeed higher in S . haematobium infected compared to uninfected individuals, but this difference was not statistically significant.…”

“…Moreover, S. haematobium could augment antibody production by influencing the biological environment through enhanced IL-4 production [6], favoring antimalarial antibody production [43]. It should be noted that S. haematobium infection had no significant effect on the antibody responses directed to either MSP3 or GLURP, the two antigens combined in GMZ2, in contrast to the findings of a recent study [44], although the level of anti-GLURP IgG concentration was indeed higher in S. haematobium infected compared to uninfected individuals, PLOS NEGLECTED TROPICAL DISEASES but this difference was not statistically significant. It is well known that MSP3 constitutes a less immunogenic component of GMZ2 [24,25], possibly explaining this observation.…”

Plasmodium falciparum and Helminth Coinfections Increase IgE and Parasite-Specific IgG Responses

“…On the contrary, we found that antigen-specific IgG and total IgE responses were higher in the coexposure/coinfection group compared to the single exposure/infection groups. For P. falciparum , this is consistent with previous studies that reported increased P. falciparum -specific IgG1, IgG2, and IgG3 responses in coinfection with Schistosoma haematobium ( 40 , 41 ). In contrast, other studies have reported a detrimental effect of coinfection with helminths in the humoral response to malaria with a reduction in P. falciparum -specific IgG ( 42 ), IgG1 and IgG3 ( 43 , 44 ), and an increase in the non-cytophilic IgG4 ( 43 ).…”

Plasmodium falciparumand helminth coinfections increase IgE and parasite-specific IgG responses

“…Thirdly, there was a trend for higher P. falciparum burden in the coexposure/coinfection group compared to the P. falciparum single exposure/infection group in children, which is consistent with other reports for P. falciparum and P. vivax (Easton et al, 2020), but contrary to others (Amoani et al, 2019;Tokplonou et al, 2020). The only significant association for helminths with regards to parasite burden was for T. trichiura, where having been exposed to or currently infected with P. falciparum seemed to have a protective effect.…”

“…On the contrary, we found that antigen-specific IgG and total IgE responses were higher in the coexposure/coinfection group compared to the single exposure/infection groups. For P. falciparum, this is consistent with previous studies that reported increased P. falciparum-specific IgG1, IgG2 and IgG3 responses in coinfection with S. haematobium (Diallo et al, 2010;Tokplonou et al, 2020). In contrast, other studies have reported a detrimental effect of coinfection with helminths in the humoral response to malaria with a reduction in P. falciparum-specific IgG (Ateba-Ngoa et al, 2016), IgG1 and IgG3 (Courtin et al, 2011;Roussilhon et al, 2010), and an increase in the non-cytophilic IgG4 (Roussilhon et al, 2010).…”