Circulating Cytokine Profiles of Polyparasitized Individuals in Gabon.

Abstract

Background Malaria, blood-borne filarial worms and intestinal parasites are all endemic in Gabon. This geographical co-distribution leads to polyparasitism and, consequently, the possibility of immune-mediated interactions between different parasite species. Intestinal protozoa and helminths could modulate anti-malarial immunity, for example, thereby potentially increasing susceptibility to malaria.Methods Blood and stool samples were collected during cross-sectional surveys in five provinces of Gabon. Parasitological diagnosis was performed to detect plasmodial parasites, Loa loa and Mansonella perstans, intestinal helminths (STH) and protozoan parasites. Nested PCR was used to detect submicroscopic plasmodial infection in individuals with negative blood smears. Cytometric Bead Array was used to quantify interleukin (IL)-6, IL-10 and Tumor Necrosis Factor (TNF)-α in plasma of subjects with different parasitological profiles i.e. malaria only, filariasis only, intestinal protozoan only, soil-transmitted helminths (STH) only, malaria/filariasis, malaria/STH, malaria/intestinal protozoa co-infections and in uninfected individuals/control group.Results Median IL-6 (124.5 [36.9–433.9] pg/mL) and IL-10 (224.5 [78.0–657.9] pg/mL) levels and the median IL-10/TNF-α (69.9 [12.5–140-7]) ratio were all significantly higher among individuals with Plasmodium falciparum infection compared to other groups (p < 0.0001). The median TNF-α level (6.5 [3.5–11.7] pg/mL) and IL-10/IL-6 ratio (3.6 [2.0–11.9]) were higher in subjects with STH (p = 0.09) and P. falciparum-intestinal protozoa co-infection (p = 0.04), respectively. IL-6 (rho=-0.37; p < 0.01) and IL-10 (rho=-0.37; p < 0.01) levels, and the IL-10/TNF-α ratio (rho=-0.36; p < 0.01) correlated negatively with age, independently of infectious status. Among children under five years old, the IL-10/TNF-α and IL-10/IL-6 ratios were higher in those with intestinal protozoan infections compared to uninfected children. The IL-10/TNF-α ratio was also higher in children aged 5–15 years and in adults harbouring blood-borne filariae compared to their control counterparts, whereas the IL-10/IL-6 ratio was lower in those aged 5–15 years with filariae and intestinal parasites but higher in adults with intestinal parasitic infections.Conclusions Asymptomatic malaria is associated with a strong polarization towards a regulatory immune response, reflected by high circulating levels of IL-10. Co-infections with P. falciparum and intestinal protozoa are associated with an enhanced IL-10 response. Immunity against malaria could differ according to age and carriage of other parasites.