Human Schistosoma haematobium antifecundity immunity is dependent on transmission intensity and associated with immunoglobulin G1 to worm-derived antigens.

Shona Wilson,Govert J Van Dam,Moussa Sacko,Frances M Jones,Birgitte J Vennervald,Gilles Riveau,Paul L A M Corstjens,Colin M Fitzsimmons,David W Dunne

doi:10.1093/infdis/jiu374

Shona Wilson, Govert J Van Dam + Show 7 more

Open Access

https://doi.org/10.1093/infdis/jiu374

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Abstract

BackgroundImmunity that reduces worm fecundity and, in turn, reduces morbidity is proposed for Schistosoma haematobium, a parasite of major public health importance. Mathematical models of epidemiological trends suggest that antifecundity immunity is dependent on antibody responses to adult-worm-derived antigen.MethodsFor a Malian cohort (age, 5–29 years) residing in high-transmission fishing villages or a moderate-transmission village, worm fecundity was assessed using the ratio of urinary egg excretion to levels of circulating anodic antigen, a Schistosoma-specific antigen that is steadily secreted by adult worms. Fecundity was modeled against host age, infection transmission intensity, and antibody responses specific to soluble worm antigen (SWA), tegument allergen-like 1, and 28-kDa glutathione-S-transferase.ResultsWorm fecundity declined steadily until a host age of 11 years. Among children, host age and transmission were negatively associated with worm fecundity. A significant interaction term between host age and transmission indicates that antifecundity immunity develops earlier in high-transmission areas. SWA immunoglobulin G1 (IgG1) levels explained the effect of transmission on antifecundity immunity.ConclusionAntifecundity immunity, which is likely to be protective against severe morbidity, develops rapidly during childhood. Antifecundity immunity is associated with SWA-IgG1, with higher infection transmission increasing this response at an earlier age, leading to earlier development of antifecundity immunity.

Highlights

Immunity that reduces worm fecundity and, in turn, reduces morbidity is proposed for Schistosoma haematobium, a parasite of major public health importance
For a Malian cohort residing in high-transmission fishing villages or a moderatetransmission village, worm fecundity was assessed using the ratio of urinary egg excretion to levels of circulating anodic antigen, a Schistosoma-specific antigen that is steadily secreted by adult worms
soluble worm antigen (SWA) immunoglobulin G1 (IgG1) levels explained the effect of transmission on antifecundity immunity

Summary

Methods

For a Malian cohort (age, 5–29 years) residing in high-transmission fishing villages or a moderatetransmission village, worm fecundity was assessed using the ratio of urinary egg excretion to levels of circulating anodic antigen, a Schistosoma-specific antigen that is steadily secreted by adult worms. Two villages with high-intensity transmission, Kaladangan and Guenidaga (n = 140), are neighboring fishing settlements on the Niger River. A third village, with moderate-intensity transmission, Kalabougou ( population, 153 individuals), is located on a tributary of the main river and has a population with a diverse range of occupations, including fishing, farming, and pottery. Three urine samples were collected from each individual before treatment, and 10 mL of each was filtered to determine S. haematobium egg counts.

Results

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Conclusion