GPS Tracking of Free-Ranging Pigs to Evaluate Ring Strategies for the Control of Cysticercosis/Taeniasis in Peru

Background Taenia solium, a parasitic cestode that affects humans and pigs, is the leading cause of preventable epilepsy in the developing world. T. solium eggs are released into the environment through the stool of humans infected with an adult intestinal tapeworm (a condition called taeniasis), and cause cysticercosis when ingested by pigs or other humans. A control strategy to intervene within high-risk foci in endemic communities has been proposed as an alternative to mass antihelminthic treatment. In this ring strategy, antihelminthic treatment is targeted to humans and pigs residing within a 100 meter radius of a pig heavily-infected with cysticercosis. Our aim was to describe the roaming ranges of pigs in this region, and to evaluate whether the 100 meter radius rings encompass areas where risk factors for T. solium transmission, such as open human defecation and dense pig activity, are concentrated. Methodology/Principal Findings In this study, we used Global Positioning System (GPS) devices to track pig roaming ranges in two rural villages of northern Peru. We selected 41 pigs from two villages to participate in a 48-hour tracking period. Additionally, we surveyed all households to record the locations of open human defecation areas. We found that pigs spent a median of 82.8% (IQR: 73.5, 94.4) of their time roaming within 100 meters of their homes. The size of home ranges varied significantly by pig age, and 93% of the total time spent interacting with open human defecation areas occurred within 100 meters of pig residences. Conclusions/Significance These results indicate that 100 meter radius rings around heavily-infected pigs adequately capture the average pig’s roaming area (i.e., home range) and represent an area where the great majority of exposure to human feces occurs

Non-local validated parametrization of an agent-based model of local-scale Taenia solium transmission in North-West Peru.

The pork tapeworm, Taenia solium, is the cause of a preventable zoonotic disease, cysticercosis, affecting both pigs and humans. Continued endemic transmission of T. solium is a major contributor of epilepsy and other neurologic morbidity, and the source of important economic losses, in many rural areas of developing countries. Simulation modelling can play an important role in aiding the design and evaluation of strategies to control or even eliminate transmission of the parasite. In this paper, we present a new agent based model of local-scale T. solium transmission and a new, non-local, approach to the model calibration to fit model outputs to observed human taeniasis and pig cysticercosis prevalence simultaneously for several endemic villages. The model fully describes all relevant aspects of T. solium transmission, including the processes of pig and human infection, the spatial distribution of human and pig populations, the production of pork for human consumption, and the movement of humans and pigs in and out in several endemic villages of the northwest of Peru. Despite the high level of uncertainty associated with the empirical measurements of epidemiological data associated with T. solium, the non-local calibrated model parametrization reproduces the observed prevalences with an acceptable precision. It does so not only for the villages used to calibrate the model, but also for villages not included in the calibration process. This important finding demonstrates that the model, including its calibrated parametrization, can be successfully transferred within an endemic region. This will enable future studies to inform the design and optimization of T. solium control interventions in villages where the calibration may be prevented by the limited amount of empirical data, expanding the possible applications to a wider range of settings compared to previous models

Seasonal Patterns in Risk Factors for Taenia Solium Transmission: a GPS Tracking Study of Pigs and Open Human Defecation in Northern Peru

Background: Taenia solium (cysticercosis) is a parasitic cestode that is endemic in rural populations where open defecation is common and free-roaming pigs have access to human feces. The purpose of this study was to examine the roaming patterns of free-range pigs, and identify areas where T. solium transmission could occur via contact with human feces. We did this by using GPS trackers to log the movement of 108 pigs in three villages of northern Peru. Pigs were tracked for approximately six days each and tracking was repeated in the rainy and dry seasons. Maps of pig ranges were analyzed for size, distance from home, land type and contact with human defecation sites, which were assessed in a community-wide defecation survey. Results: Consistent with prior GPS studies and spatial analyses, we found that the majority of pigs remained close to home during the tracking period and had contact with human feces in their home areas: pigs spent a median of 79% (IQR: 61–90%) of their active roaming time within 50 m of their homes and a median of 60% of their contact with open defecation within 100 m of home. Extended away-from-home roaming was predominately observed during the rainy season; overall, home range areas were 61% larger during the rainy season compared to the dry season (95% CI: 41–73%). Both home range size and contact with open defecation sites showed substantial variation between villages, and contact with open defecation sites was more frequent among pigs with larger home ranges and pigs living in higher density areas of their village. Conclusions: Our study builds upon prior work showing that pigs predominately roam and have contact with human feces within 50–100 m of the home, and that T. solium transmission is most likely to occur in these concentrated areas of contact. This finding, therefore, supports control strategies that target treatment resources to these areas of increased transmission. Our finding of a seasonal trend in roaming ranges may be useful for control programs relying on pig interventions, and in the field of transmission modeling, which require precise estimates of pig behavior and risk

Spatial Relationship Between \u3ci\u3eTaenia Solium\u3c/i\u3e 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 goldstandard 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

Assessing Ultrasonography as a Diagnostic Tool for Porcine Cysticercosis

Background Taenia solium inflicts substantial neurologic disease and economic losses on rural communities in many developing nations. Ring-strategy is a control intervention that targets treatment of humans and pigs among clusters of households (rings) that surround pigs heavily infected with cysticerci. These pigs are typically identified by examining the animal\u27s tongue for cysts. However, as prevalence decreases in intervened communities, more sensitive methods may be needed to identify these animals and to maintain control pressure. The purpose of this study was to evaluate ultrasonography as an alternative method to detect pigs heavily infected with T. solium cysts. Methodology/Principal Findings We purchased 152 pigs representing all seropositive animals villagers were willing to sell from eight communities (pop. 2085) in Piura, Peru, where T. solium is endemic. Tongue and ultrasound examinations of the fore and hind-limbs were performed in these animals, followed by necropsy with fine dissection as gold standard to determine cyst burden. We compared the sensitivity and specificity of ultrasonography with tongue examination for their ability to detect heavy infection (\u3e 100 viable cysts) in pigs. Compared to tongue examination, ultrasonography was more sensitive (100% vs. 91%) but less specific (90% vs. 98%), although these differences were not statistically significant. The greater sensitivity of ultrasound resulted in detection of one additional heavily infected pig compared to tongue examination (11/11 vs. 10/11), but resulted in more false positives (14/141 vs. 3/141) due to poor specificity. Conclusions/Significance Ultrasonography was highly sensitive in detecting heavily infected pigs and may identify more rings for screening or treatment compared to tongue examination. However, the high false positive rate using ultrasound would result in substantial unnecessary treatment. If specificity can be improved with greater operator experience, ultrasonography may benefit ring interventions where control efforts have stalled due to inadequate sensitivity of tongue examination

Validation of a Spatial Agent-Based Model for Taenia Solium Transmission (“cystiagent”) Against a Large Prospective Trial of Control Strategies in Northern Peru

Background: The pork tapeworm (Taenia solium) is a parasitic helminth that imposes a major health and economic burden on poor rural populations around the world. As recognized by the World Health Organization, a key barrier for achieving control of T. solium is the lack of an accurate and validated simulation model with which to study transmission and evaluate available control and elimination strategies. CystiAgent is a spatially-explicit agent based model for T. solium that is unique among T. solium models in its ability to represent key spatial and environmental features of transmission and simulate spatially targeted interventions, such as ring strategy. Methods/Principal findings: We validated CystiAgent against results from the Ring Strategy Trial (RST)–a large cluster-randomized trial conducted in northern Peru that evaluated six unique interventions for T. solium control in 23 villages. For the validation, each intervention strategy was replicated in CystiAgent, and the simulated prevalences of human taeniasis, porcine cysticercosis, and porcine seroincidence were compared against prevalence estimates from the trial. Results showed that CystiAgent produced declines in transmission in response to each of the six intervention strategies, but overestimated the effect of interventions in the majority of villages; simulated prevalences for human taenasis and porcine cysticercosis at the end of the trial were a median of 0.53 and 5.0 percentages points less than prevalence observed at the end of the trial, respectively. Conclusions/Significance: The validation of CystiAgent represented an important step towards developing an accurate and reliable T. solium transmission model that can be deployed to fill critical gaps in our understanding of T. solium transmission and control. To improve model accuracy, future versions would benefit from improved data on pig immunity and resistance, field effectiveness of anti-helminthic treatment, and factors driving spatial clustering of T. solium infections including dispersion and contact with T. solium eggs in the environment. Author summary: Neurocysticercosis, caused by the ingestion of Taenia solium eggs, is a major cause of human epilepsy around the world. A wide spectrum of tools to fight T. solium is are now available and include antiparasitic treatment for pigs and humans, porcine vaccines, and sanitation improvements; however, the ideal combination of interventions applied to populations to maximize effectiveness and feasibility is not known. Transmission models are one tool that can be used to compare and evaluate different intervention strategies, but no currently available T. solium models have been tested for accuracy. In this research, we validated our model (“CystiAgent”) by comparing simulations of the model to the results of a large-scale trial testing a variety of T. solium control interventions. The model was calibrated using observed epidemiological data from these villages and evaluated for its ability to reproduce the effect of T. solium control interventions. The validation showed that the model was able to reproduce the baseline levels of disease, but generally overestimated the effect that each intervention would have on transmission. These results will allow us to identify limitations of the current model to improve future versions, and represent a step forward in the creation of a tool to design and evaluate future programs to control and eliminate T. solium

Understanding Transmission and Control of the Pork Tapeworm with CystiAgent: A Spatially Explicit Agent‑Based Model

Background: The pork tapeworm, Taenia solium, is a serious public health problem in rural low-resource areas of Latin America, Africa and Asia, where the associated conditions of nuerocysticercosis (NCC) and porcine cysticercosis cause substantial health and economic harms. An accurate and validated transmission model for T. solium would serve as an important new tool for control and elimination, as it would allow for comparison of available intervention strategies, and prioritization of the most effective strategies for control and elimination efforts. Methods: We developed a spatially-explicit agent-based model (ABM) for T. solium (“CystiAgent”) that differs from prior T. solium models by including a spatial framework and behavioral parameters such as pig roaming, open human defecation, and human travel. In this article, we introduce the structure and function of the model, describe the data sources used to parameterize the model, and apply sensitivity analyses (Latin hypercube sampling-partial rank correlation coefficient (LHS-PRCC)) to evaluate model parameters. Results: LHS-PRCC analysis of CystiAgent found that the parameters with the greatest impact on model uncertainty were the roaming range of pigs, the infectious duration of human taeniasis, use of latrines, and the set of “tuning” parameters defining the probabilities of infection in humans and pigs given exposure to T. solium. Conclusions: CystiAgent is a novel ABM that has the ability to model spatial and behavioral features of T. solium transmission not available in other models. There is a small set of impactful model parameters that contribute uncertainty to the model and may impact the accuracy of model projections. Field and laboratory studies to better understand these key components of transmission may help reduce uncertainty, while current applications of CystiAgent may consider calibration of these parameters to improve model performance. These results will ultimately allow for improved interpretation of model validation results, and usage of the model to compare available control and elimination strategies for T. solium

GPS Tracking of Free-Ranging Pigs to Evaluate Ring Strategies for the Control of Cysticercosis/Taeniasis in Peru

<div><p>Background</p><p><i>Taenia solium</i>, a parasitic cestode that affects humans and pigs, is the leading cause of preventable epilepsy in the developing world. <i>T</i>. <i>solium</i> eggs are released into the environment through the stool of humans infected with an adult intestinal tapeworm (a condition called taeniasis), and cause cysticercosis when ingested by pigs or other humans. A control strategy to intervene within high-risk foci in endemic communities has been proposed as an alternative to mass antihelminthic treatment. In this ring strategy, antihelminthic treatment is targeted to humans and pigs residing within a 100 meter radius of a pig heavily-infected with cysticercosis. Our aim was to describe the roaming ranges of pigs in this region, and to evaluate whether the 100 meter radius rings encompass areas where risk factors for <i>T</i>. <i>solium</i> transmission, such as open human defecation and dense pig activity, are concentrated.</p><p>Methodology/Principal Findings</p><p>In this study, we used Global Positioning System (GPS) devices to track pig roaming ranges in two rural villages of northern Peru. We selected 41 pigs from two villages to participate in a 48-hour tracking period. Additionally, we surveyed all households to record the locations of open human defecation areas. We found that pigs spent a median of 82.8% (IQR: 73.5, 94.4) of their time roaming within 100 meters of their homes. The size of home ranges varied significantly by pig age, and 93% of the total time spent interacting with open human defecation areas occurred within 100 meters of pig residences.</p><p>Conclusions/Significance</p><p>These results indicate that 100 meter radius rings around heavily-infected pigs adequately capture the average pig’s roaming area (i.e., home range) and represent an area where the great majority of exposure to human feces occurs.</p></div

Data file including CystiAgent simulation results, observed results from the Ring Strategy Trial, and all intervention settings for each village evaluated (n = 21 villages).

Data file including CystiAgent simulation results, observed results from the Ring Strategy Trial, and all intervention settings for each village evaluated (n = 21 villages)

Evaluating the Role of Corrals and Insects in the Transmission of Porcine Cysticercosis: A Cohort Study

The widespread dispersion of pigs infected with cysticercosis across endemic villages, low cyst burden among infected pigs, and low prevalence of taeniasis all suggest that pig ingestion of human feces is not the only mode of transmission for Taenia solium. Our objective was to evaluate the risk of porcine cysticercosis associated with exposure to human feces, dung beetles, and flies in an endemic community setting. We used a cluster-randomized cohort design to compare the risk of developing antibodies and infection among 120 piglets raised in either free-roaming (FR), standard corral (SC), or netted corral environments (NC). We collected monthly blood samples to detect serum antibodies and necropsied all pigs after 10 months to identify cysts. A total of 66 piglets developed antibodies with the relative risk of seropositivity in FR vs. all corralled pigs increasing significantly after 18 weeks. Of 108 necropsied pigs, 15 had T. solium cysts, all belonging to the FR group. Corrals were protective against infection but less so against seropositivity. NC, which did not completely exclude insects, did not provide added protection against seropositivity as compared to SC. The results of this study suggest that dung beetles and flies do not play an important role in infection