The Global Burden of Human Parasites: Who and Where are They? How are They Transmitted?

With ‘‘This Wormy World,’’ Norman Stoll (1947) 65 years ago in a Presidential Address to the American Society of Parasitologists, achieved the first comprehensive estimate of the human burden of parasitic diseases. There have been updates (e.g., Bundy, 1997; Crompton, 1999), and even the global atlas of helminth diseases, www.thiswormyworld.org, adopting Stoll’s pithy phrase. Here, I will view this still critically important concern from a more ecological and evolutionary perspective. Adding basic biological concepts to this global human health issue may reveal additional reasons, beyond the economic, social, infrastructural, colonial, and governance contributions to human disease (Bonds et al., 2010), as to why this has been such an intractable problem. Roman philosophers provided a formula for investigation of a problem, the 5 Qs (and a C and a U). Answering them offers necessary and sufficient insight for a scientific investigation as well as for quality journalism. From an ecological and evolutionary standpoint, for human parasitic diseases these questions might be: Who (taxonomically) are the infectious agents? What are the functional relationships (adaptive strategies) of these parasites? Where (geographically) do these diseases occur? When, in the course of the life cycle of the parasite, are humans the host? How are they transmitted? What features contribute to their prevalence and severity? With these questions answered to a first approximation, we can proceed to ask: Why do these patterns occur? How can this information inform public health strategies? Humans are almost certainly the best-surveyed animal species for infectious agents. Human evolutionary history and population sizes and movements are also very well known. This comprehensive knowledge base, including many rare parasite species, enables an investigation as to the global nature of human host–parasite relationships. It also permits an evolutionarily analysis of the operationally defined distinctive infectious strategies (adaptive syndromes) (Kuris and Lafferty, 2000; Lafferty and Kuris, 2002). This information can be synthesized over geographic space and through evolutionary and historic time. Here, I first ask what sorts of parasitic diseases currently affect humans? I consider this from a taxonomic perspective and from the perspective of parasite infectious strategies. For instance, are there more protozoan, helminth, or arthropod parasitic species of humans? Are there more pathogens or macroparasites? Do these proportions change if we only include prevalent parasites that inflict morbidity? This is a matter of tabulation and accounting, but requires careful consideration of sources and rules of inclusion. Specifically, I ask how important are zoonotic diseases compared to diseases that depend on humans to persist. I also summarize basic patterns of transmission for the parasites of humans and note some implications for general control strategies. After tabulating human diseases by type, I attempt a more difficult task, sorting out the implications of geographic patterns of human parasitic diseases. To this extent, I consider the concept of the poverty trap and how it applies to sub-Saharan Africa. It is apparent that the world’s poor suffer the most from disease. But it is less clear to what extent poverty leads to disease or disease leads to poverty (Bonds et al., 2010). Clearly, a heavily parasitized population suffers economically and socially (Farmer, 2001; Bonds et al., 2010). But, it is equally reasonable to expect that economically disadvantaged, weakly organized communities will experience more infectious disease than an otherwise advantaged community (Gallup and Sachs, 2001; Bloom et al., 2003). A cycling of cause and effect can result in a ‘‘poverty trap’’ where sick people become poor, which predisposes them to further exposure to infectious disease (Bowles et al., 2007). Of course, poverty and disease could be correlated simply due to associations with other causal factors. A comprehensive statistical analysis conducted by Bonds et al. (2012) shows that after an extensive list of socioeconomic factors have been factored out, sub-Saharan African countries still fall significantly below other disadvantaged nations in terms of public health. Is there a distinct geography of disease to match the geography of poverty? If so, in this ratchet what comes first, poverty or disease? Here, I offer the possibility that it is not just that Africa has a high total disease burden but that Africa experiences, for evolutionary and historic reasons, a distinctive subset of human parasites and that these are, on average and in aggregate, more vexing than the array of parasitic diseases in other biogeographic regions. In other words, Africa retains the long list of ancestral human infectious diseases. Those human lineages that did not leave Africa continue to suffer this burden, and this traps them in a cycle of poverty and disease. To develop this view, I briefly depict the geography of human parasitic disease and offer an analysis informed by the parasites’ trophic strategies, transmission mechanisms, and the extent to which they are zoonotic. The modern spread of originally sub-Saharan African diseases is also briefly discussed.