The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases?

Abstract

Parasitic infections are widespread throughout the tropics and sub-tropics, and infection with multiple parasite species is the norm rather than the exception. Despite the ubiquity of polyparasitism, its public health significance has been inadequately studied. Here we review available studies investigating the nutritional and pathological consequences of multiple infections with Plasmodium and helminth infection and, in doing so, encourage a reassessment of the disease burden caused by polyparasitism. The available evidence is conspicuously sparse but is suggestive that multiple human parasite species may have an additive and/or multiplicative impact on nutrition and organ pathology. Existing studies suffer from a number of methodological limitations and adequately designed studies are clearly necessary. Current methods of estimating the potential global morbidity due to parasitic diseases underestimate the health impact of polyparasitism, and possible reasons for this are presented. As international strategies to control multiple parasite species are rolled-out, there is a number of options to investigate the complexity of polyparasitism, and it is hoped that that the parasitological research community will grasp the opportunity to understand better the health of polyparasitism in humans.

Figure 1. Conceptual framework

The negative cycle between polyparasitism, malnutrition and cognitive and physical development. Helminth and malaria infections impact upon host nutrition through a number of mechanisms, which may have additive or multiplicative impacts, especially in childhood. Helminth infections cause and/or aggravate malnutrition through worm-induced gastro-intestinal tract physiopathology and reduced food intake (Crompton & Nesheim, 2002), chronic blood-loss (Hotez et al., 2004) and intestinal inflammation (Stephenson et al., 2000b). Malaria may contribute to protein-energy malnutrition (PEM) through a number of mechanisms triggered by augmented levels of inflammatory cytokines, including anorexia and the induction of a catabolic response (Nyakeriga et al., 2004,Tracey & Cerami, 1992), and to reduced haemoglobin levels through increased rates of destruction and removal of RBCs and anaemia of inflammation. Sequestration of red blood cells in those with P.falciparum- and schistosome-associated splenomegaly can also contribute to anaemia (Friedman et al., 2005). Associations may also be due to the effect of undernourishment on the immune response, leading to an increased susceptibility to infection (Koski & Scott, 2001). PEM and anaemia associated with parasitic infection can result in decreased physical fitness, cognitive development and school achievement in children (Boivin & Giordani, 1993,Boivin et al., 1993,Bundy & Guyatt, 1996), and in decreased cognition and work capacity in adults (Guyatt, 2000,Haas & Brownlie, 2001); factors which are in turn associated with poor socio-economic status, in itself a risk factor for infection.

Figure 2. Age-associated prevalence and intensity profiles of STH, schistosome and malaria infections

typical age profiles for (a) prevalence and (b) intensity of infection with A.lumbricoides, schistosomiasis, hookworm and P.falciparum malaria; adapted from Bundy (1995) and Anderson and May (2001)