Spatial relationship between Taenia solium tapeworm carriers and necropsy cyst burden in pigs

Background Taenia solium, a parasite that affects humans and pigs, is the leading cause of preventable epilepsy in the developing world. Geographic hotspots of pigs testing positive for serologic markers of T. solium exposure have been observed surrounding the locations of human tapeworm carriers. This clustered pattern of seropositivity in endemic areas formed the basis for geographically targeted control interventions, which have been effective at reducing transmission. In this study, we further explore the spatial relationship between human tapeworm carriers and infected pigs using necroscopic examination as a quantitative gold-standard diagnostic to detect viable T. solium cyst infection in pigs. Methodology/Principal findings We performed necroscopic examinations on pigs from 7 villages in northern Peru to determine the number of viable T. solium cysts in each pig. Participating humans in the study villages were tested for T. solium tapeworm infection (i.e., taeniasis) with an ELISA coproantigen assay, and the distances from each pig to its nearest human tapeworm carrier were calculated. We assessed the relationship between proximity to a tapeworm carrier and the prevalence of light, moderate, and heavy cyst burden in pigs. The prevalence of pig infection was greatest within 50 meters of a tapeworm carrier and decreased monotonically as distance increased. Pigs living less than 50 meters from a human tapeworm carrier were 4.6 times more likely to be infected with at least one cyst than more distant pigs. Heavier cyst burdens, however, were not more strongly associated with proximity to tapeworm carriers than light cyst burdens. Conclusion/Significance Our study shows that human tapeworm carriers and pigs with viable T. solium cyst infection are geographically correlated in endemic areas. This finding supports control strategies that treat humans and pigs based on their proximity to other infected individuals. We did not, however, find sufficient evidence that heavier cyst burdens in pigs would serve as improved targets for geographically focused control interventions.
Author summary Taenia solium, the pork tapeworm, is a parasite transmitted between humans and pigs. The disease is most common in developing countries where access to sanitation is limited and domestic pigs are allowed to roam freely. Humans infected with the intestinal tapeworm release T. solium eggs into the environment when they defecate outside, and pigs become infected with the larval stage of the disease, cysticercosis, upon consuming these eggs in human feces. Prior work using serologic testing of pigs has shown that proximity to human tapeworm carriers is a possible risk factor for porcine cysticercosis. Our study investigated if proximity to human tapeworm carriers was associated with established cyst infection in pigs, and if proximity to tapeworm carriers also increased the degree of cyst infection in pigs (i.e., the number of T. solium cysts a pig was infected with). The results confirmed that human tapeworm carriers and infected pigs are geographically correlated, but did not uncover a stronger relationship for heavily infected pigs. It is important to continue to investigate this spatial relationship as some control strategies rely on the assumption that human tapeworm carriers will be found in close proximity to heavily infected pigs. Future control strategies would benefit from a precise knowledge of the degree of pig infection that best predicts for nearby tapeworm carriers.