Determinants of Malaria Transmission at the Population Level

Abstract

Transmission of malaria from man to mosquito defines the human infectious reservoir of malaria. At the population level this is influenced by a variety of human, parasite, and mosquito vector factors some or all of which may vary depending on the epidemiological setting. Here, we review our current state of knowledge related to human infectiousness to mosquitoes and how current malaria control strategies might be adapted to focus on reducing this. While much progress has been made in malaria control, we argue that an improved understanding of human infectivity will allow more effective use of current control tools and make elimination a more feasible goal.

Figure 1.

Submicroscopic parasite carriage as a function of malaria transmission intensity. Prevalence of Plasmodium falciparum infections detected by nested polymerase chain reaction (nPCR, x-axis) or microscopy (y-axis) in the same individuals. Each data point and associated confidence intervals represent data from one cross-sectional survey. The dotted line shows the correlation that would be expected if the prevalence of infection detected by both methods was the same. The solid line with shaded area represents the best fit to the data and confidence interval (Okell et al. 2012). (Panel from Okell et al. 2012; adapted, with permission, from the authors.) The shaded arrows in the panel below shows (top) the intensity of malaria transmission, which is typically defined by microscopy and ranges from low to high transmission intensity; (middle) the average parasite density in infections that increases with transmission intensity; and (bottom) the proportion of infections that is submicroscopic. While the proportion of the population that is malaria-infected is lowest in low-endemic settings, the fraction of these infections that is submicroscopic (undetectable by microscopy and rapid diagnostic tests [RDTs]) (Wu et al. 2015) is largest in low-endemic settings.

Figure 2.

Parasite density and infectivity in relation to age in an area of intense malaria transmission. Each dot represents an individual in which parasite carriage was determined and quantified by a quantitative polymerase chain reaction (qPCR) (Hermsen et al. 2001) and onward malaria transmission was determined by membrane feeding assays. Open dots represent uninfected individuals (parasite density equals zero) or malaria-infected individuals who are not infectious to mosquitoes. Closed circles indicate infectious individuals. Parasite density and the likelihood of infecting mosquitoes are highest in children; onward transmission to mosquitoes is commonly observed at densities below the microscopic threshold for detection (Slater et al. 2015).

Figure 3.

The human infectious reservoir for malaria. Individuals in the figure are represented by circles in three age groups: <5 (dark gray), 5–15 (black), and >15 years (light gray). The age-stratified population (A) reflects the abundance of individuals in each group based on a simplified population age structure in sub-Saharan Africa. (B) Speckling within circles represents the presence of Plasmodium falciparum gametocytes by molecular methods. (C) Solid filled circles represent who are infectious to mosquitoes in membrane feeding assays. Many gametocytemic individuals are not infectious to mosquitoes at the moment of sampling. The top pie chart presents the proportional contribution of each age group to the human infectious reservoir for malaria after taking into account the demographic distributions in the population. The bottom pie chart presents the same contribution to the human infectious reservoir for malaria, taking into account differences in mosquito-biting frequency that are related to differences in behavior, protective measures, and attractiveness to mosquitoes because of body size and other host characteristics. (From data in Stone et al. 2015; adapted, with permission, from Elsevier © 2015.)