Different distribution of malaria parasite in left and right extremities of vertebrate hosts translates into differences in parasite transmission

Abstract

Malaria, a vector-borne disease caused by Plasmodium spp., remains a major global cause of mortality. Optimization of disease control strategies requires a thorough understanding of the processes underlying parasite transmission. While the number of transmissible stages (gametocytes) of Plasmodium in blood is frequently used as an indicator of host-to-mosquito transmission potential, this relationship is not always clear. Significant effort has been made in developing molecular tools that improve gametocyte density estimation and therefore prediction of mosquito infection rates. However a significant level of uncertainty around estimates remains. The weakness in the relationship between gametocyte burden, measured from a blood sample, and the mosquito infection rate could be explained by a non-homogeneous distribution of gametocytes in the bloodstream. The estimated gametocyte density would then only be a single snapshot that does not reflect the host infectivity. This aspect of Plasmodium infection, however, remains largely neglected. In both humans and birds, we found here that the gametocyte densities differed depending on which side of the body the sample was taken, suggesting that gametocytes are not homogeneously distributed within the vertebrate host. We observed a fluctuating asymmetry, in other words, the extremity of the body with the highest density of parasites is not always the same from one individual to another. An estimation of gametocyte density from only one blood sample, as is commonly measured, could, therefore, over-or underestimated the infectivity of gametocyte carriers. This might have important consequences on the epidemiology of the disease since we show that this variation influences host-to-mosquito transmission. Vectors fed on the least infected body part had a lower parasite burden than those fed on the most infected part. The heterogeneous distribution of gametocytes in bloodstream should be considered to improve diagnosis and test new malaria control strategies.

Impact of vertebrate host parasitaemia onPlasmodiumdevelopment within mosquitoes

“…The amount of parasite ingested by the vector during their infestation (usually a blood meal) can also generate infection heterogeneity (e.g., [31,32]). Indeed, parasite numbers vary between vertebrate hosts and also spatiotemporally within individuals [33,34]. Although a positive correlation is expected between the quantity of parasite present in the vertebrate host blood and the density of transmissible stages of the parasite found in vectors (after the incubation period), the relationship is not always obvious.…”

Last-come, best served? Mosquito biting order and Plasmodium transmission

“…Spatial aggregation of gametocytes in vertebrate blood could be partially responsible for the aggregated distribution of oocysts in mosquitoes. Recent work has shown that gametocyte density can change by more than 0.4-fold between blood collected from different human body parts ([ 37 ], but see [ 38 ]). Although the direct connection between spatial heterogeneity in vertebrate blood and overdispersion in mosquitoes has never been made, it has been reported that Plasmodium gametocytes show an aggregated distribution within mosquitoes that recently fed on a human host [ 39 ].…”