Human Trypanosoma cruzi infection is driven by eco-social interactions in rural communities of the Argentine Chaco

Abstract

The transmission of Trypanosoma cruzi to humans is determined by multiple ecological, socio-economic and cultural factors acting at different scales. Their effects on human infection with T. cruzi have often been examined separately or using a limited set of ecological and socio-demographic variables. Herein, we integrated the ecological and social dimensions of human infection risk with the spatial distribution patterns of human and vector (Triatoma infestans) infection in rural communities of the Argentine Chaco composed of indigenous people (90% Qom) and a creole minority. We conducted serosurveys in 470 households aiming at complete population enumeration over 2012–2015. The estimated seroprevalence of T. cruzi prior to the implementation of an insecticide spraying campaign (2008) was 29.0% (N = 1,373 in 301 households), and was twice as large in Qom than creoles. Using generalized linear mixed models, human seropositive cases significantly increased with infected triatomine abundance, having a seropositive household co-inhabitant and household social vulnerability (a multidimensional index of poverty), and significantly decreased with increasing host availability in sleeping quarters (an index summarizing the number of domestic hosts for T. infestans). Vulnerable household residents were exposed to a higher risk of infection even at low infected-vector abundances. The risk of being seropositive increased significantly with house infestation among children from stable households, whereas both variables were not significantly associated among children from households exhibiting high mobility within the communities, possibly owing to less consistent exposures. Human infection was clustered by household and at a larger spatial scale, with hotspots of human and vector infection matching areas of higher social vulnerability. These results were integrated in a risk map that shows high-priority areas for targeted interventions oriented to suppress house (re)infestations, detect and treat infected children, and thus reduce the burden of future disease.

Long-term impact of a ten-year intervention program on human and canine Trypanosoma cruzi infection in the Argentine Chaco

“…The seroprevalence of T. cruzi in children aged �5 years has traditionally been used to monitor the impacts of vector control actions on domestic transmission (e.g., [47][48][49]. In our study, the seroprevalence of T. cruzi in children aged <5 years was 1.6% (95% CI, 0-9.1%), i.e., three, four and 11 times lower than the respective preintervention seroprevalence in Area III (5.4%), Area II and IV (6.1%), and Area I (17.9%) [13,31,37]. For example, Chile achieved a five-fold decrease in the seroprevalence of T. cruzi in children aged <5 years to 1.1% after 12 years of nation-wide vector control activities [50].…”

“…Whenever community-wide house spraying with insecticide is implemented without a consistent vector surveillance system, transient declines in the force of infection are followed by rapid recovery in the Argentine and Bolivian Chaco [14,85], and elsewhere [63]. Our current results, in a highly endemic area inhabited by vulnerable subgroups in heterogeneous rural communities [31], evince that interrupting vector-borne transmission of T. cruzi to humans in hyperendemic areas is feasible with the current means implemented systematically. Scaling up the intervention program, carefully tailored to local settings and paying due attention to the eventual emergence of pyrethroid resistance, is the next challenge.…”

“…House infestation with T. infestans decreased rapidly from 18.0-45.9% to 0.7-12.3% after community-wide spraying with pyrethroid insecticide, though the pace strongly differed among rural sections the municipality (i.e., Areas I-IV) [26][27][28][29][30]. Human seroprevalence with T. cruzi ranged from 29.0% in Area III (mainly inhabited by an indigenous people, the Qom) [31] to 39.8% in Area I, with a Creole majority [13]. The domestic abundance of T. cruzi-infected T. infestans at baseline and cohabiting with �3 seropositive people were significant risk factors for human infection [13,31].…”

“…Human seroprevalence with T. cruzi ranged from 29.0% in Area III (mainly inhabited by an indigenous people, the Qom) [31] to 39.8% in Area I, with a Creole majority [13]. The domestic abundance of T. cruzi-infected T. infestans at baseline and cohabiting with �3 seropositive people were significant risk factors for human infection [13,31]. The prevalence of T. cruzi infection in Area I dogs and cats was 26.0-28.7% at program onset [24].…”

“…Human seroprevalence with T . cruzi ranged from 29.0% in Area III (mainly inhabited by an indigenous people, the Qom) [ 31 ] to 39.8% in Area I, with a Creole majority [ 13 ]. The domestic abundance of T .…”