Trypanosoma cruzi infection in Triatoma sordida before and after community-wide residual insecticide spraying in the Argentinean Chaco
Graphical abstract
Introduction
The role of various species of Triatominae as secondary vectors of Trypanosoma cruzi, the etiological agent of Chagas disease, remains controversial (Guhl et al., 2009). This controversy probably reflects the richness of species involved, their broad geographic range, the dynamic nature of the domestic invasion process, and the limited research efforts invested in sylvatic species of Triatominae. Triatoma sordida (Stäl, 1859) is a secondary vector of T. cruzi, exhibiting different degrees of domiciliation and colonization especially in areas where the main vector Triatoma infestans was suppressed (Forattini et al., 1982, Noireau et al., 1997). T. sordida is widely distributed across northern Argentina, eastern Bolivia, Paraguay and southeastern Brazil (Carcavallo et al., 1999). It is frequently found in tree holes, under bark, palm trees, bromeliads, small mammals’ burrows, and bird nests, and usually colonizes peridomestic chicken coops or nests (Diotaiuti et al., 1993). The prevalence of T. cruzi infection in T. sordida was usually less than 2% (Oscherov et al., 2003), and given that this species shows little anthropophily, it was considered of low epidemiological significance across most of its geographic range (Silveira, 2002) except in Bolivia where it reached 21% (Noireau et al., 1997, Brenière et al., 1998).
Domestic and sylvatic transmission cycles have been characterized according to host, vector species and habitats, and may be separated or overlap to various degrees. The six parasite genotypes identified (TcI–TcVI), called discrete typing units (DTUs), usually exhibit different distributions between transmissions cycles (Zingales et al., 2012). In domestic transmission cycles of the Argentine Chaco, TcV and TcVI were the predominant DTUs identified in T. infestans, domestic dogs, cats and humans (Diosque et al., 2003, Cardinal et al., 2008, Enriquez et al., 2013, Maffey et al., 2012). The main sylvatic reservoir hosts identified were Didelphis albiventris opossums infected with TcI, and armadillos and Conepatus chinga skunks infected with TcIII (Diosque et al., 2003, Orozco et al., 2013). Several rodent species exhibited subpatent infections only revealed by kDNA-PCR (Orozco et al., 2014). The putative sylvatic vectors of T. cruzi have not been conclusively identified yet in the Gran Chaco eco-region. Particularly, in Pampa del Indio (Argentine Chaco), T. sordida and Panstrongylus geniculatus captured in sylvatic habitats were not found to be infected (Alvarado-Otegui et al., 2012). The predominant DTUs identified in the very few (n = 9) OM-positive peridomestic T. sordida examined were TcVI (56%) and TcI (33%), leaving unclear the role of this species in the domestic transmission cycle (Maffey et al., 2012). These findings prompted us to further examine T. sordida bugs for T. cruzi infection, DTUs and bloodmeal sources using molecular methods to elucidate its role as a secondary vector across a diversity of rural villages, seasons and bug-control contexts. We included a sizable number of T. sordida specimens captured in peridomestic habitats and all the T. sordida captured in domiciles before and after full-coverage house spraying with insecticides. Our hypotheses were that T. sordida harbored subpatent infections with T. cruzi, and that D. albiventris opossums were the bloodmeal source of TcI-infected bugs.
Section snippets
Study area
The present study was carried out in a rural section (450 km2) of Pampa del Indio Municipality (25°55′S 56°58′W), Province of Chaco, Argentina, comprising 327 inhabited households belonging to 13 communities which have already been described elsewhere (Gurevitz et al., 2011).
Entomological surveys
A baseline (BL) survey was conducted in all households in the study area to assess triatomine infestation levels by timed manual searches (TMS) using a flushing-out agent in September–December 2007 (Gurevitz et al., 2011).
T. sordida infestation
A total of 518 and 281 T. sordida was collected using all methods at BL and 4 MPS, respectively. The prevalence of house infestation by T. sordida decreased significantly from 21.1% at BL to 13.5% at 4 MPS (Fisher’s exact test, p = 0.01). The median bug abundance per infested site was 2 (first–third quartiles: Q1–Q3 = 1–4) at BL and 1 (Q1–Q3 = 1–4) at 4 MPS. Most bugs were collected in peridomiciles. The most frequent sites of capture were ecotopes associated with chickens (63.5% at BL and 67.4% at 4
Discussion
Our study shows a sixfold increase of T. cruzi prevalence in T. sordida as determined by means of highly sensitive PCR tests relative to standard OM-based examination. The false-negative rate was very low, as expected from the very low prevalence of infection in this vector species. PCR-based analysis is to be preferred relative to OM for the diagnosis of T. cruzi infection in T. sordida. This species usually feeds on poultry blood, characterized by a lower nutritional value than mammalian
Financial support
This study was supported by awards from University of Buenos Aires (UBACYT 2011-2014), Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 2012-2015), Agencia Nacional de Promoción Científica y Tecnológica to R.E.G. (PICT 2011-2072, PICTO-Glaxo 2011-0062). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. M.V.C. and R.E.G. are members of CONICET Researcher’s Career. N.P.M. received an undergraduate
Acknowledgments
We thank Jorge Nasir and the Chagas Control Program of Chaco for support in field operations; Juan M. Gurevitz, M. Pilar Fernández, Leonardo A. Ceballos, Julián A. Alvarado-Otegui, Paula C. Ordoñez- Krasnowsi and Laura Peresán-Martinez for field and laboratory assistance; the villagers of Pampa del Indio for kindly welcoming us into their homes and cooperating with this investigation; and Fundación Mundo Sano for hospitality.
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