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

Abstract

BackgroundTaenia 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 findingsWe 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/SignificanceOur 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.

Clustering of Necropsy-Confirmed Porcine Cysticercosis Surrounding Taenia solium Tapeworm Carriers in Peru

“…2 We later confirmed this finding of a 50 m radius of elevated prevalence using necroscopic examination of pigs as a gold-standard diagnostic. 4 In the current investigation, the observed clusters of pig infection were concentrated in the households of tapeworm carriers without extending to neighboring households.…”

“…In rural villages of Peru where T. solium is endemic, infected pigs (porcine cysticercosis) have been found to cluster spatially around human tapeworm carriers (taeniasis). [2][3][4] Our group has previously observed significant clustering of both seropositive pigs (based on enzyme-linked immunoelectrotransfer blot [EITB] for T. solium antibody response) 2 and pigs with viable cyst infection (based on necroscopic examination) 4 around human tapeworm carriers in rural areas of northern Peru. The incidence in these hotspots was strongest among pigs living within 50 m of identified carriers and did not depend on whether the tapeworm carrier was the pig's owner or a neighbor within 50 m. Collectively, these findings have provided evidence to support geographically targeted screening and treatment for human tapeworm carriers.…”

Understanding transmission and control of the pork tapeworm with CystiAgent: a spatially explicit agent-based model

“…Local variations in pig-raising practices, sanitation, diet, and migration all interact to create locally specific transmission patterns that differ from one endemic village to the next [20]. Even within villages, spatial heterogeneities caused by pig-roaming patterns and open defecation cause clustering that is important for a model to capture [21][22][23]. Importantly, incorporating underlying spatial and biological processes of T. solium transmission was highlighted in a recent report on the WHO 2030 goals [13], and there is evidence that models that fail to account for these heterogeneities are susceptible to overestimating the effect of control interventions [24] and yielding unrealistic predictions for achieving control and elimination targets [25].…”

Understanding transmission and control of the pork tapeworm with CystiAgent: a spatially explicit agent-based model

“…Local variations in pig-raising practices, sanitation, diet, and migration all interact to create locally speci c transmission patterns that differ from one endemic village to the next [17]. Even within villages, spatial heterogeneities caused by pig-roaming patterns and open defecation cause clustering that is important for a model to capture [18][19][20]. Importantly, incorporating underlying spatial and biological processes of T. solium transmission was highlighted in a recent report on the WHO 2030 goals [11], and there is evidence that models that fail to account for these heterogeneities are susceptible to overestimating the effect of control interventions [21] and yielding unrealistic predictions for achieving control and elimination targets [22].…”