Domestic (re)infestation risk with the main vector Triatoma infestans increases with surrounding green vegetation and social vulnerability in the Argentine Chaco.

BACKGROUND: Chagas disease, caused by Trypanosoma cruzi, is still a public health problem in Latin America and in the Southern Cone countries, where Triatoma infestans is the main vector. We evaluated the relationships among the density of green vegetation around rural houses, sociodemographic characteristics, and domestic (re)infestation with T. infestans while accounting for their spatial dependence in the municipality of Pampa del Indio between 2007 and 2016. METHODS: The study comprised sociodemographic and ecological variables from 734 rural houses with no missing data. Green vegetation density surrounding houses was estimated by the normalized difference vegetation index (NDVI). We used a hierarchical Bayesian logistic regression composed of fixed effects and spatial random effects to estimate domestic infestation risk and quantile regressions to evaluate the association between surrounding NDVI and selected sociodemographic variables. RESULTS: Qom ethnicity and the number of poultry were negatively associated with surrounding NDVI, whereas overcrowding was positively associated with surrounding NDVI. Hierarchical Bayesian models identified that domestic infestation was positively associated with surrounding NDVI, suitable walls for triatomines, and overcrowding over both intervention periods. Preintervention domestic infestation also was positively associated with Qom ethnicity. Models with spatial random effects performed better than models without spatial effects. The former identified geographic areas with a domestic infestation risk not accounted for by fixed-effect variables. CONCLUSIONS: Domestic infestation with T. infestans was associated with the density of green vegetation surrounding rural houses and social vulnerability over a decade of sustained vector control interventions. High density of green vegetation surrounding rural houses was associated with households with more vulnerable social conditions. Evaluation of domestic infestation risk should simultaneously consider social, landscape and spatial effects to control for their mutual dependency. Hierarchical Bayesian models provided a proficient methodology to identify areas for targeted triatomine and disease surveillance and control.

Human infectiousness and parasite load in chronic patients seropositive for Trypanosoma cruzi in a rural area of the Argentine Chaco.

A key parameter in the transmission of vector-borne infections, including Chagas disease, is the ability of the different host species to transmit the parasite to the vector (infectiousness). Here, we determined infectiousness to the vector of Trypanosoma cruzi-seropositive humans examined by artificial xenodiagnosis (XD), established its relationship with T. cruzi DNA levels (a surrogate of intensity of parasitemia) quantified by real-time PCR (qPCR), and assessed whether infectiousness was associated with the body mass index (BMI), age, ethnic background and parasite genotype. XD was performed to 117 T. cruzi-seropositive residents from Pampa del Indio and parasite load was quantified in 81 of them. Using optical microscopy (OM) 33.6% of the seropositive people tested were infectious and this fraction nearly doubled (66.0%) when XD triatomines were examined by kDNA-PCR. The mean infectiousness (defined as the percentage of all infected triatomines detected by OM at any time point among the total number of insects examined by OM 30 days post-feeding) was 5.2%, and the mean parasite load was 0.51 parasite equivalents per ml. Infectiousness to the vector was associated negatively with age and BMI, and positively with the detection of parasitemia by kDNA-PCR, and parasite load by qPCR in bivariate analysis. Patients with a positive XD by OM exhibited a significantly higher mean parasite load. Using multiple regression, infectiousness was associated with parasite load (positively) and with the household presence of T. infestans and Qom ethnic group (negatively); no significant association was observed with age or its interaction with ethnicity. We did not find significant associations between identified DTUs and infectiousness or parasite load. Infectiousness was aggregated: 18% of the people examined by XD generated 80% of the infected triatomines. Detecting and treating the super-infectious fraction of the infected human would disproportionally impact on domestic transmission risks. Nonetheless, treatment of all eligible infected people who meet the inclusion criteria regardless of their parasitemia should be ensured to improve their prognosis.

Chagas disease vector control and Taylor's law.

BACKGROUND: Large spatial and temporal fluctuations in the population density of living organisms have profound consequences for biodiversity conservation, food production, pest control and disease control, especially vector-borne disease control. Chagas disease vector control based on insecticide spraying could benefit from improved concepts and methods to deal with spatial variations in vector population density. METHODOLOGY/PRINCIPAL FINDINGS: We show that Taylor's law (TL) of fluctuation scaling describes accurately the mean and variance over space of relative abundance, by habitat, of four insect vectors of Chagas disease (Triatoma infestans, Triatoma guasayana, Triatoma garciabesi and Triatoma sordida) in 33,908 searches of people's dwellings and associated habitats in 79 field surveys in four districts in the Argentine Chaco region, before and after insecticide spraying. As TL predicts, the logarithm of the sample variance of bug relative abundance closely approximates a linear function of the logarithm of the sample mean of abundance in different habitats. Slopes of TL indicate spatial aggregation or variation in habitat suitability. Predictions of new mathematical models of the effect of vector control measures on TL agree overall with field data before and after community-wide spraying of insecticide. CONCLUSIONS/SIGNIFICANCE: A spatial Taylor's law identifies key habitats with high average infestation and spatially highly variable infestation, providing a new instrument for the control and elimination of the vectors of a major human disease.

Trypanosoma cruzi infection in Triatoma sordida before and after community-wide residual insecticide spraying in the Argentinean Chaco.

Triatoma sordida is a secondary vector of Trypanosoma cruzi in the Gran Chaco and Cerrado eco-regions where it frequently infests peridomestic and domestic habitats. In a well-defined area of the humid Argentine Chaco, very few T. sordida were found infected when examined by optical microscopic examination (OM). In order to further assess the role of T. sordida and the relative magnitude of subpatent bug infections, we examined the insects for T. cruzi infection, parasite Discrete Typing Units (DTUs) and bloodmeal sources using various molecular techniques. Among 205 bugs with a negative or no OM-based diagnosis, the prevalence of infection determined by kDNA-PCR was nearly the same in bugs captured before (6.3%) and 4 months after insecticide spraying (6.4%). On average, these estimates were sixfold higher than the prevalence of infection based on OM (1.1%). Only TcI was identified, a DTU typically associated with opossums and rodents. Chickens and turkeys were the only bloodmeal sources identified in the infected specimens and the main local hosts at the bugs' capture sites. As birds are refractory to T. cruzi infection, further studies are needed to identify the infectious bloodmeal hosts. The persistent finding of infected T. sordida after community-wide insecticide spraying highlights the need of sustained vector surveillance to effectively prevent T. cruzi transmission in the domestic and peridomestic habitats.

Microcavia australis (Caviidae, Rodentia), a new highly competent host of Trypanosoma cruzi I in rural communities of northwestern Argentina.

Rodents are well-known hosts of Trypanosoma cruzi but little is known on the role of some caviomorph rodents. We assessed the occurrence and prevalence of T. cruzi infection in Microcavia australis ("southern mountain, desert or small cavy") and its infectiousness to the vector Triatoma infestans in four rural communities of Tafí del Valle department, northwestern Argentina. Parasite detection was performed by xenodiagnosis and polymerase chain reaction amplification of the hyper-variable region of kinetoplast DNA minicircles of T. cruzi (kDNA-PCR) from blood samples. A total of 51 cavies was captured in traps set up along cavy paths in peridomestic dry-shrub fences located between 25 and 85 m from the nearest domicile. We document the first record of M. australis naturally infected by T. cruzi. Cavies presented a very high prevalence of infection (46.3%; 95% confidence interval, CI=33.0-59.6%). Only one (4%) of 23 cavies negative by xenodiagnosis was found infected by kDNA-PCR. TcI was the only discrete typing unit identified in 12 cavies with a positive xenodiagnosis. The infectiousness to T. infestans of cavies positive by xenodiagnosis or kDNA-PCR was very high (mean, 55.8%; CI=48.4-63.1%) and exceeded 80% in 44% of the hosts. Cavies are highly-competent hosts of T. cruzi in peridomestic habitats near human dwellings in rural communities of Tucumán province in northwestern Argentina.

Trans-sialidase inhibition assay detects Trypanosoma cruzi infection in different wild mammal species.

The detection of Trypanosoma cruzi infection in mammals is crucial for understanding the eco-epidemiological role of the different species involved in parasite transmission cycles. Xenodiagnosis (XD) and hemoculture (HC) are routinely used to detect T. cruzi in wild mammals. Serological methods are much more limited because they require the use of specific antibodies to immunoglobulins of each mammalian species susceptible to T. cruzi. In this study we detected T. cruzi infection by trans-sialidase (TS) inhibition assay (TIA). TIA is based on the antibody neutralization of a recombinant TS that avoids the use of anti-immunoglobulins. TS activity is not detected in the co-endemic protozoan parasites Leishmania spp and T. rangeli. In the current study, serum samples from 158 individuals of nine wild mammalian species, previously tested by XD, were evaluated by TIA. They were collected from two endemic areas in northern Argentina. The overall TIA versus XD co-reactivity was 98.7% (156/158). All 18 samples from XD-positive mammals were TIA-positive (co-positivity, 100%) and co-negativity was 98.5% (138/140). Two XD-negative samples from a marsupial (Didelphis albiventris) and an edentate (Dasypus novemcinctus) were detected by TIA. TIA could be used as a novel tool for serological detection of Trypanosoma cruzi in a wide variety of sylvatic reservoir hosts.

Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of spliced-leader genes.

The intergenic region of spliced-leader (SL-IR) genes from 105 Trypanosoma cruzi I (Tc I) infected biological samples, culture isolates and stocks from 11 endemic countries, from Argentina to the USA were characterised, allowing identification of 76 genotypes with 54 polymorphic sites from 123 aligned sequences. On the basis of the microsatellite motif proposed by Herrera et al. (2007) to define four haplotypes in Colombia, we could classify these genotypes into four distinct Tc I SL-IR groups, three corresponding to the former haplotypes Ia (11 genotypes), Ib (11 genotypes) and Id (35 genotypes); and one novel group, Ie (19 genotypes). Genotypes harbouring the Tc Ic motif were not detected in our study. Tc Ia was associated with domestic cycles in southern and northern South America and sylvatic cycles in Central and North America. Tc Ib was found in all transmission cycles from Colombia. Tc Id was identified in all transmission cycles from Argentina and Colombia, including Chagas cardiomyopathy patients, sylvatic Brazilian samples and human cases from French Guiana, Panama and Venezuela. Tc Ie gathered five samples from domestic Triatoma infestans from northern Argentina, nine samples from wild Mepraia spinolai and Mepraia gajardoi and two chagasic patients from Chile and one from a Bolivian patient with chagasic reactivation. Mixed infections by Tc Ia+Tc Id, Tc Ia+Tc Ie and Tc Id+Tc Ie were detected in vector faeces and isolates from human and vector samples. In addition, Tc Ia and Tc Id were identified in different tissues from a heart transplanted Chagas cardiomyopathy patient with reactivation, denoting histotropism. Trypanosoma cruzi I SL-IR genotypes from parasites infecting Triatoma gerstaeckeri and Didelphis virginiana from USA, T. infestans from Paraguay, Rhodnius nasutus and Rhodnius neglectus from Brazil and M. spinolai and M. gajardoi from Chile are to our knowledge described for the first time.

Rapid detection of Trypanosoma cruzi in human serum by use of an immunochromatographic dipstick test.

We evaluated a commercially available immunochromatographic dipstick test to detect Trypanosoma cruzi infection in 366 human serum samples with known serological results from Argentina, Ecuador, Mexico, and Venezuela. One hundred forty-nine of 366 (40.7%) and 171/366 (46.7%) samples tested positive by dipstick and serology, respectively. Dipstick sensitivity was calculated to be 84.8% (range between countries, 77.5 to 95%), and specificity was 97.9% (95.9 to 100%).

Molecular epidemiology of domestic and sylvatic Trypanosoma cruzi infection in rural northwestern Argentina.

Genetic diversity of Trypanosoma cruzi populations and parasite transmission dynamics have been well documented throughout the Americas, but few studies have been conducted in the Gran Chaco ecoregion, one of the most highly endemic areas for Chagas disease, caused by T. cruzi. In this study, we assessed the distribution of T. cruzi lineages (identified by PCR strategies) in Triatoma infestans, domestic dogs, cats, humans and sylvatic mammals from two neighbouring rural areas with different histories of transmission and vector control in northern Argentina. Lineage II predominated amongst the 99 isolates characterised and lineage I amongst the six isolates obtained from sylvatic mammals. T. cruzi lineage IIe predominated in domestic habitats; it was found in 87% of 54 isolates from Tr. infestans, in 82% of 33 isolates from dogs, and in the four cats found infected. Domestic and sylvatic cycles overlapped in the study area in the late 1980s, when intense domestic transmission occurred, and still overlap marginally. The introduction of T. cruzi from sylvatic into domestic habitats is likely to occur very rarely in the current epidemiological context. The household distribution of T. cruzi lineages showed that Tr. infestans, dogs and cats from a given house compound shared the same parasite lineage in most cases. Based on molecular evidence, this result lends further support to the importance of dogs and cats as domestic reservoir hosts of T. cruzi. We believe that in Argentina, this is the first time that lineage IIc has been isolated from naturally infected domestic dogs and Tr. infestans.

A prospective study of the effects of sustained vector surveillance following community-wide insecticide application on Trypanosoma cruzi infection of dogs and cats in rural Northwestern Argentina.

Domestic dogs were used as natural sentinels to assess prospectively the long-term impact of selective, community-based spraying with pyrethroid insecticides after community-wide spraying on transmission of Trypanosoma cruzi in rural villages under surveillance between 1992 and 2002. In 2000 and 2002 light infestations by Triatoma infestans were recorded, and 523 dogs and cats were examined serologically or by xenodiagnosis. The prevalence of T. cruzi infection in dogs decreased from 65% at baseline to 8.9% and 4.7% at 7.5 and 10 years after sustained vector surveillance, respectively. The average annual force of infection dropped 260-fold from 72.7 per 100 dog-years at baseline to <0.3% in 2002, as determined prospectively and retrospectively from the age-prevalence curve of native dogs born during surveillance. Multiple logistic regression analysis showed that prevalent cases in dogs in 2000 and 2002 were associated positively and significantly with the peak number of T. infestans caught in domestic areas at the dog's compound during its lifetime. The sustained decline in T. cruzi infections in dogs and cats is the result of selective, community-based insecticide spraying that kept the abundance of infected T. infestans at marginal levels, fast host population turnover, and low immigration rates from areas with active transmission.

Use of an immunochromatographic dipstick test for rapid detection of Trypanosoma cruzi in sera from animal reservoir hosts.

We evaluated an immunochromatographic dipstick test to detect Trypanosoma cruzi in canine serum samples from areas of endemicity (n = 141) and nonendemicity (n = 28) for Chagas' disease with known serological and xenodiagnostic test results. The dipstick test had a specificity of at least 94% and a sensitivity of at least 96%. The dipstick tested could become the first choice for screening purposes in disease surveillance or intervention programs.