Coinfection with malaria alters the fecundity and within-host persistence of an intestinal nematode.

Infections with soil transmitted helminths (STHs) are highly prevalent in humans living in the intertropical region. While, in most cases, STHs can establish chronic infections, the dynamics of the infection can be altered when other parasites exploit the same host. These changes can have consequences in terms of the health of the host, the epidemiology of the disease (e.g., the duration of the infection and the inter-host transmission success) and the fitness of the parasite. Here, we investigated if the coinfection with Plasmodium yoelii alters the dynamics (fecundity and with-host persistence) of the murine nematode Heligmosomoides polygyrus. We found that, compared to single infected mice, coinfected hosts excreted more worm eggs, while the worm biomass in the intestine did not differ between single infected and coinfected mice. Moreover, the increase in egg excretion was also observed when Plasmodium infected hosts that had been harboring the nematode during the past four weeks (i.e., when the population size of adult worms can only decrease due to mortality). Therefore, the enhanced shedding of eggs reflects a plastic adjustment of worm fecundity to the environment provided by a coinfected host. This plastic response was modulated by the host Th2 immunity, as coinfection inhibited IL-4 and IL-13 gene expression, plasma levels of IL-5 and IL-13, and the expansion of GATA-3+ CD4+ T cells in the spleen. In agreement with this, experimentally neutralizing IL-13 with monoclonal antibodies reproduced the results observed in coinfected mice (an increase in egg excretion), while the administration of recombinant IL-13 reduced egg shedding. Interestingly, coinfection extended the patent period of Heligmosomoides polygyrus (longer within-host persistence); moreover, a higher cumulative number of eggs was excreted, up to 99 days post-infection, in coinfected hosts. Although the gene expression of Th2 cytokines was lower at day 99 p.i., coinfected mice still had a downregulated expression compared to single infected hosts. These results offer a proof of concept that coinfection with Plasmodium has the potential to affect the epidemiology of STHs by increasing the number of eggs excreted over the whole infectious period and maintaining a larger environmental reservoir of transmissible stages.