Long-term reduction of Trypanosoma cruzi infection in sylvatic mammals following deforestation and sustained vector surveillance in northwestern Argentina

Abstract

Long-term variations in the dynamics and intensity of sylvatic transmission of Trypanosoma cruzi were investigated around eight rural villages in the semiarid Argentine Chaco in 2002–2004 and compared to data collected locally in 1984–1991. Of 501 wild mammals from 13 identified species examined by xenodiagnosis, only 3 (7.9%) of 38 Didelphis albiventris opossums and 1 (1.1%) of 91 Conepatus chinga skunks were infected by T. cruzi. The period prevalence in opossums was four-fold lower in 2002–2004 than in 1984–1991 (32–36%). The infection prevalence of skunks also decreased five-fold from 4.1–5.6% in 1984–1991 to 1.1% in 2002–2004. Infection in opossums increased with age and from summer to spring in both study periods. The force of infection per 100 opossum-months after weaning declined more than six-fold from 8.2 in 1988–1991 to 1.2 in 2002–2004. Opossums were mainly infected by T. cruzi lineage I and secondarily by lineage IId in 1984–1991, and only by T. cruzi I in 2002–2004; skunks were infected by T. cruzi IId in 1984–1991 and by IIc in 2002–2004. The striking decline of T. cruzi infection in opossums and skunks occurred in parallel to community-wide insecticide spraying followed by selective sprays leading to very low densities of infected Triatoma infestans in domestic and peridomestic habitats since 1992; to massive deforestation around one of the villages or selective extraction of older trees, and apparent reductions in opossum abundance jointly with increases in foxes and skunks. These factors may underlie the dramatic decrease of T. cruzi infection in wild reservoir hosts.

Introduction

Trypanosoma cruzi, the etiologic agent of Chagas disease, has been detected in some 180 species belonging to 25 families of mammals in the Americas, with marsupials, edentates, and rodents being the most frequent sylvatic hosts (World Health Organization, 2002). Domestic transmission cycles mainly include humans, dogs and cats, and several species of triatomine bugs adapted to human dwellings (Pinto Dias, 2000). Transmission cycles of T. cruzi display large spatial and structural heterogeneity (Diotaiuti et al., 1995).

The Gran Chaco, a natural landscape unit of about 1,000,000 km² crossing over northern Argentina, Bolivia, Paraguay and southwestern Brazil, is one of the most endemic regions for Chagas disease. Natural infection by T. cruzi has been reported for armadillos Chaetophractus vellerosus, C. villosus, Cabassous unicinctus, Dasypus novemcinctus, Euphractus sexcinctus, and Tolypeutes matacus; opossums Didelphis albiventris and Lutreolina crassicaudata; short-tailed opossums Monodelphis domestica; foxes Lycalopex culpaeus and L. gymnocercus griseus; coatis Nasua nasua, and mice Calomys musculinus and C. laucha (Carcavallo and Martínez, 1968, Yeo et al., 2005). In a well-defined area in the semiarid Argentine Chaco, the only wild mammals found infected with T. cruzi were D. albiventris opossums, a few Conepatus chinga skunks and one Galictis cuja ferret among 230 mammals from 20 species (Pietrokovsky et al., 1991, Wisnivesky-Colli et al., 1992). In the Bolivian Chaco, sylvatic Triatoma infestans, Triatoma sordida and Triatoma guasayana have been found infected with T. cruzi and may be the putative sylvatic vectors of T. cruzi (Noireau et al., 2000). In the Argentine Chaco, however, the sylvatic vector of T. cruzi has not been firmly established. Since the 1990's the Chaco has been undergoing accelerated deforestation and change of land use patterns which may have affected the relationship between the domestic and sylvatic transmission cycle of T. cruzi to an unknown extent.

T. cruzi has been classified into two major phylogenetic lineages, T. cruzi I (TCI) and T. cruzi II (TCII), and several sublineages within TCII designated as IIa, IIb, IIc, IId and IIe (Anon., 1999). These lineages appear to be distributed differentially between triatomine species and hosts throughout the Americas. TCI was originally described from sylvatic hosts and predominates in domestic transmission cycles to the north of the Amazon basin, whereas TCII predominates in domestic cycles but has sometimes been found in sylvatic mammals as well (Brisse et al., 2000, Yeo et al., 2005). In the Argentine and Paraguayan Chaco, TCI infects D. albiventris opossums and much less frequently humans and T. infestans, whereas TCII typically infects T. infestans, domestic dogs and cats, humans and skunks (Luca d’Oro et al., 1993, Diosque et al., 2003, Yeo et al., 2005, Marcet et al., 2006). Based on isoenzyme and molecular markers, two studies concluded that domestic and sylvatic transmission cycles of T. cruzi overlapped partially throughout Argentina and in two rural areas within the Chaco region (Wisnivesky-Colli et al., 1992, Luca d’Oro et al., 1993, Diosque et al., 2003). Opossums were suggested as a possible bridge between sylvatic and domestic transmission cycles (Schweigmann et al., 1999, Diosque et al., 2004). Temporal variations in the sylvatic cycle of transmission of T. cruzi in the presence of significant environmental changes have not been investigated.

As part of a longitudinal study on the eco-epidemiology of Chagas disease in a well-defined rural area in northwestern Argentina under sustained vector surveillance and selective insecticide sprays, the present study sought to assess the host range and prevalence of T. cruzi in a wide variety of wild mammals, and to identify the parasite sublineages circulating in them. Furthermore, to assess the existence of long-term variations in the dynamics and intensity of sylvatic transmission of T. cruzi, we compared our results with data collected in the same area between 1984 and 1991, before both massive deforestation around one of the villages and sustained vector surveillance in all villages was initiated in 1992.