The 2008–2010 Colombian cysticercosis serosurvey generated unique and unprecedented information on exposure to T. solium cysticercosis at a national scale. The work presented here extends the original analysis of these data [14] by using contemporary geostatistical techniques to evaluate individual-level risk factors associated with seropositivity to T. solium cysticerci and, simultaneously, spatial clustering at a sub-national (municipality) scale. The results contribute important information on factors associated with exposure to T. solium cysticerci. They also indicate that similar large-scale epidemiological surveys will be needed if hyperendemic foci of transmission are to be identified and targeted for intensified interventions in 17 endemic countries, as per the WHO’s 2021–2030 NTD roadmap targets for taeniasis/cysticercosis [22].
Here, and in the original analysis of these data [14], women were more likely than men to be positive for T. solium cysticercus antibodies. This finding is consistent with the results of numerous other studies undertaken in Latin America [2, 9, 23,24,25,26,27]; by contrast, in other endemic regions, such as sub-Saharan Africa, being male is associated with an increased risk of exposure [28] and of antigen positivity [29, 30]. The mechanisms underlying these epidemiological patterns remain unclear. Different household roles associated with handling household-owned animals, food and water may be important, although many variables pertaining to these activities were accounted for in this analysis. Notwithstanding the underlying cause, women could be an important target for educational campaigns in Colombia, not just because of their apparent increased risk of exposure, but also because they are often being responsible for the majority of food handling and preparation activities, which would be all the more important if they were also tapeworm carriers.
The trend for increasing seropositivity with age is unsurprising given that T. solium cysticercus antibodies probably persist for several years. Seropositivity may thus be considered as an indicator of lifetime prior exposure. Praet et al. [31] explored age-dependent dynamics of T. solium cysticercus antibody positivity in more depth by fitting mathematical models to similar age–seroprevalence data collected in Ecuador. Their results suggested that higher antibody seroreversion rates occur following first exposure (representing the primary humoral response), followed by a lower seroreversion rate after the boosting effect of subsequent exposures (representing secondary humoral response), causing saturation in antibody seroprevalence with age. Hence, where transmission is relatively intense—and repeated exposures are common—one might expect to see similar saturating age–seroprevalence profiles. By contrast, in lower transmission settings, the effect of seroreversion following first exposure—and the less frequent boosting effect of subsequent exposures—may be more evident in seroprevalence profiles, possibly resulting in a decline in seropositivity in older age groups.
Exposure to T. solium is known to be greater for individuals with lower educational levels, those from lower socioeconomic strata [6, 32] and those facing social marginalisation [9, 33,34,35]. Our findings are consistent with these previously reported findings, with the odds of displaced people testing positive being almost twofold higher than people in the highest socioeconomic stratum. Internal displacement in Colombia is a major issue that often involves the poorest and most disadvantaged people [36], but if the control of T. solium is to become comprehensive, displaced people may require enhanced interventions. Health education could be one such option for control in specific populations using tools such as “The Vicious Worm” [37], as there is some evidence that health education campaigns specific to T. solium can impact transmission [38]. It is, however, likely that to achieve substantial, sustained reductions in the prevalence of T. solium or elimination, particularly in highly endemic areas, a One Health approach targeting the whole T. solium system, including infections in pigs, humans and the environment, will be required [39, 40], as recently shown by intervention trials in Peru and Zambia [41, 42].
The only variable related to food and water sources or hygiene practices that was significantly associated with seropositivity to T. solium cysticercus antibodies was the use of rainwater. Individuals in households using rainwater as opposed to water stored in wells or cisterns had a 1.6-fold higher odds of seropositivity. Waterborne cysticercosis transmission is supported in the literature, given that the eggs can survive in fresh, brackish and salt waters [32, 43,44,45] and can contaminate vegetables [45]. Other variables, such as open-field defecation or the use of unsanitary latrines [46, 47], that one might also expect to be associated with exposure to T. solium were not identified in our analysis as significant risk factors. We also found that the odds of seropositivity significantly decreased when individuals consumed partially cooked/raw pork meat once per week, an observation possibly confounded by wealth (i.e., wealthier individuals consuming more meat). One might expect that consumption of partially cooked/raw pork meat would be associated with increased odds of seropositivity, given that taeniasis (adult tapeworm) carriers are at risk of autoinfection. However, more research is needed to understand the relative contribution of this route of transmission to overall cysticercosis risk [48].
A particularly striking finding of our analysis was the association between owning dogs and significantly increased odds of test positivity. Dogs in Asia have been reported to test positive for T. solium antibodies [49, 50], potentially implicating them as alternative intermediate hosts. Transmission to humans has also been suggested to occur via the consumption of raw or uncooked canine meat [51], although this practice is thought to be extremely rare and not widely reported in Latin America. Moreover, the role of dogs as potential hosts for T. solium remains somewhat speculative. Given the coprophagic habits of dogs and their close interaction with humans, it is also possible (and perhaps more likely) that dogs act as mechanical vectors of T. solium eggs.
A further striking finding is that among the 10.8% (n = 3,154) of individuals owning pigs, we did not find a significantly increased odds of seropositivity, only a non-significant increase in those owning fewer than 10 pigs (possibly indicative of smallholder, subsistence farmers, compared to individuals owning > 10 pigs, which may represent wealthier farmers). A further sub-analysis of pig owners (Additional file 1: Text S2) found no association between seropositivity and pig management practices (e.g. free roaming, feeding wastes, drinking free water, among others). These findings contrast with those reported in other studies in Latin America and other geographical settings, in which human cysticercosis has been associated with owning pigs [2, 33, 52]. Some farming practices, such as using waste or water and mix concentrate as feed, and the lack of drainage systems were non-significantly associated with increased seropositivity. However, because this sub-analysis was based on a much smaller sample (n = 3154) with only 388 seropositive individuals, there was limited power to detect significant associations.
In addition to exploring individual and household risk factors associated with exposure to T. solium, our geostatistical approach enabled identification of spatial clusters where seropositivity was higher, so-called hotspots (in the north and south of Colombia), or lower (in the central and western areas of the country) than could be explained by the included covariates (Fig. 2). Hotspots where seropositivity was higher than could be explained by the covariates coincided with areas with higher seroprevalence (16‒40%) in the northern coastal area and areas bordering Venezuela (Departments of Atlántico, Magdalena, Cesar, La Guajira), in the northern-central region (Departments of Antioquia and Bolívar), in Vaupés (south-east, bordering Brazil) and in the south, in regions bordering Peru and Brazil (Department of Amazonas; Fig. 1). Neither human nor pig population density was explicitly included in the model and, therefore, these variables could help to explain some of this clustering (because of the potential for increased contamination of the environment with T. solium eggs where humans and pigs are abundant). While population densities are heterogeneous across Colombia, some of the highest human population densities are generally found in the north and north-east of the country [53], alongside the highest pig population in the Pacific (east costal), Andean (north-east/north-west) and Caribbean regions (north), as estimated from the Gridded Livestock Database in 2007 [54]. Furthermore, it should be noted that given the level of spatial analysis, we were only able to detect spatial variation at the municipality level.
Local climatic, environmental and ecological conditions may also play a role in the observed clustering. In a recent systematic review, Jansen et al. [45] identified that Taenia spp. eggs can survive in the environment for up to 1 year in favourable conditions of high humidity, moderate temperatures (5‒25 °C) and presence of surface water. Moreover, invertebrates, including dung beetles (Ammophorus rubripes), can also act as mechanical vectors for the dispersal of Taenia spp eggs [55, 56]. Hence, it is highly likely that local conditions—unaccounted for in our statistical model—will influence spatial patterns of exposure.
Although the serosurvey data analysed here are unique in presenting a picture of exposure to T. solium cysticercosis at a national scale, geographical coverage is incomplete and the sampling approach may have introduced some biases. In particular, the selection of municipalities with > 5000 individuals and a health centre is likely to have created a bias towards sampling in more densely populated urban areas. This led to an underrepresentation of rural communities, which may typically have had less access to health care and possibly lower overall health. In addition, nine departments were excluded from sampling (due to logistical and resource constraints) and overall, only a relatively small fraction (12%) of Colombia’s municipalities were sampled (133/1122). Women are highly represented, and this is likely due to the decision of randomizing only the individuals present at the interview for inclusion in the study. Also, the data were collected in 2008–2010, over a decade ago, and may therefore not reflect precisely contemporary epidemiological conditions. Nonetheless, we believe that, in the absence of wide-spread national control efforts, the distribution and endemic situation of T. solium are unlikely to have changed substantively over the past decade and, therefore, the data provide a useful snapshot of endemic conditions across the country. Due to the nature of surveys, other forms of bias and reverse causation are also possible.
Moreover, it cannot be excluded that any of the encountered associations are confounded by unmeasurable or unknown risk factors and that the a priori decision to drop a certain number of variables might have increased the model residuals, not including possible confounders. On the other hand, the unstructured nature of some variables or the probable collinearity with other exposures made this choice desirable. Despite the lack of data concerning some geographical areas in Colombia, the authors still consider the study outcomes as valuable and indicative of the situation of cysticercosis in the country. In addition, the information provided in the current study could be further used to build models that can spatially predict the disease seroprevalence in non-sampled areas [17], offering a cost-effective tool for decision-makers in places where direct sampling did not take place.
Mapping the distribution and seroprevalence of T. solium in endemic countries is a crucial next step in realising the WHO’s goals of implementing intensified control in hyperendemic areas of 17 countries by 2030 [22]. Currently, country-wide data on the transmission of T. solium, such as those analysed here for Colombia, are scarce, and thus there is a great deal of work to be done to identify hyperendemic areas in which to implement intensified interventions. Moreover, although working definitions of ‘hyperendemicity’ have been proposed [57], there is not yet a consensus on the definition of endemicity levels for T. solium infection. Geostatistical approaches will play an important role in identifying areas of high transmission, particularly if they can be parameterized to identify likely areas of high transmission using Geographical Information System (GIS) data that have comprehensive global coverage. Although our study focused on the identification of risk factors associated with exposure to T. solium and residual degrees of spatial clustering, similar geostatistical and machine learning approaches can be used that focus on predicting the spatial distribution of disease using GIS data [17]. Such approaches, conducted at national and global scales, will be crucial in assisting progress towards the WHO’s 2030 goals [22, 58].
