RESUMEN

BACKGROUND: The Gran Chaco ecoregion is a well-known hotspot of several neglected tropical diseases (NTDs) including Chagas disease, soil-transmitted helminthiasis and multiparasitic infections. Interspecific interactions between parasite species can modify host susceptibility, pathogenesis and transmissibility through immunomodulation. Our objective was to test the association between human co-infection with intestinal parasites and host parasitaemia, infectiousness to the vector and immunological profiles in Trypanosoma cruzi-seropositive individuals residing in an endemic region of the Argentine Chaco. METHODS: We conducted a cross-sectional serological survey for T. cruzi infection along with an intestinal parasite survey in two adjacent rural villages. Each participant was tested for T. cruzi and Strongyloides stercoralis infection by serodiagnosis, and by coprological tests for intestinal parasite detection. Trypanosoma cruzi bloodstream parasite load was determined by quantitative PCR (qPCR), host infectiousness by artificial xenodiagnosis and serum human cytokine levels by flow cytometry. RESULTS: The seroprevalence for T. cruzi was 16.1% and for S. stercoralis 11.5% (n = 87). We found 25.3% of patients with Enterobius vermicularis. The most frequent protozoan parasites were Blastocystis spp. (39.1%), Giardia lamblia (6.9%) and Cryptosporidium spp. (3.4%). Multiparasitism occurred in 36.8% of the examined patients. Co-infection ranged from 6.9% to 8.1% for T. cruzi-seropositive humans simultaneously infected with at least one protozoan or helminth species, respectively. The relative odds of being positive by qPCR or xenodiagnosis (i.e. infectious) of 28 T. cruzi-seropositive patients was eight times higher in people co-infected with at least one helminth species than in patients with no such co-infection. Trypanosoma cruzi parasite load and host infectiousness were positively associated with helminth co-infection in a multiple regression analysis. Interferon-gamma (IFN-γ) response, measured in relation to interleukin (IL)-4 among humans infected with T. cruzi only, was 1.5-fold higher than for T. cruzi-seropositive patients co-infected with helminths. The median concentration of IL-4 was significantly higher in T. cruzi-seropositive patients with a positive qPCR test than in qPCR-negative patients. CONCLUSIONS: Our results show a high level of multiparasitism and suggest that co-infection with intestinal helminths increased T. cruzi parasitaemia and upregulated the Th2-type response in the study patients.

Asunto(s)

Enfermedad de Chagas , Coinfección , Helmintiasis , Parasitosis Intestinales , Trypanosoma cruzi , Humanos , Trypanosoma cruzi/inmunología , Trypanosoma cruzi/genética , Trypanosoma cruzi/aislamiento & purificación , Coinfección/parasitología , Coinfección/epidemiología , Coinfección/inmunología , Enfermedad de Chagas/epidemiología , Enfermedad de Chagas/complicaciones , Enfermedad de Chagas/parasitología , Enfermedad de Chagas/sangre , Enfermedad de Chagas/inmunología , Animales , Adulto , Estudios Transversales , Masculino , Femenino , Parasitosis Intestinales/epidemiología , Parasitosis Intestinales/parasitología , Parasitosis Intestinales/complicaciones , Parasitosis Intestinales/inmunología , Persona de Mediana Edad , Helmintiasis/complicaciones , Helmintiasis/parasitología , Helmintiasis/epidemiología , Helmintiasis/inmunología , Adulto Joven , Adolescente , Argentina/epidemiología , Estudios Seroepidemiológicos , Strongyloides stercoralis/inmunología , Strongyloides stercoralis/aislamiento & purificación , Parasitemia/parasitología , Parasitemia/epidemiología , Células Th2/inmunología , Niño , Estrongiloidiasis/epidemiología , Estrongiloidiasis/parasitología , Estrongiloidiasis/complicaciones , Estrongiloidiasis/inmunología , Estrongiloidiasis/sangre , Anciano , Citocinas/sangre , Anticuerpos Antiprotozoarios/sangre

RESUMEN

BACKGROUND: The emergence of pyrethroid resistance has threatened the elimination of Triatoma infestans from the Gran Chaco ecoregion. We investigated the status and spatial distribution of house infestation with T. infestans and its main determinants in Castelli, a municipality of the Argentine Chaco with record levels of triatomine pyrethroid resistance, persistent infestation over 2005-2014, and limited or no control actions over 2015-2020. METHODS: We conducted a 2-year longitudinal survey to assess triatomine infestation by timed manual searches in a well-defined rural section of Castelli including 14 villages and 234 inhabited houses in 2018 (baseline) and 2020, collected housing and sociodemographic data by on-site inspection and a tailored questionnaire, and synthetized these data into three indices generated by multiple correspondence analysis. RESULTS: The overall prevalence of house infestation in 2018 (33.8%) and 2020 (31.6%) virtually matched the historical estimates for the period 2005-2014 (33.7%) under recurrent pyrethroid sprays. While mean peridomestic infestation remained the same (26.4-26.7%) between 2018 and 2020, domestic infestation slightly decreased from 12.2 to 8.3%. Key triatomine habitats were storerooms, domiciles, kitchens, and structures occupied by chickens. Local spatial analysis showed significant aggregation of infestation and bug abundance in five villages, four of which had very high pyrethroid resistance approximately over 2010-2013, suggesting persistent infestations over space-time. House bug abundance within the hotspots consistently exceeded the estimates recorded in other villages. Multiple regression analysis revealed that the presence and relative abundance of T. infestans in domiciles were strongly and negatively associated with indices for household preventive practices (pesticide use) and housing quality. Questionnaire-derived information showed extensive use of pyrethroids associated with livestock raising and concomitant spillover treatment of dogs and (peri) domestic premises. CONCLUSIONS: Triatoma infestans populations in an area with high pyrethroid resistance showed slow recovery and propagation rates despite limited or marginal control actions over a 5-year period. Consistent with these patterns, independent experiments confirmed the lower fitness of pyrethroid-resistant triatomines in Castelli compared with susceptible conspecifics. Targeting hotspots and pyrethroid-resistant foci with appropriate house modification measures and judicious application of alternative insecticides with adequate toxicity profiles are needed to suppress resistant triatomine populations and prevent their eventual regional spread.

Asunto(s)

Enfermedad de Chagas , Resistencia a los Insecticidas , Insecticidas , Piretrinas , Triatoma , Animales , Triatoma/efectos de los fármacos , Triatoma/fisiología , Piretrinas/farmacología , Argentina , Insecticidas/farmacología , Enfermedad de Chagas/transmisión , Enfermedad de Chagas/epidemiología , Humanos , Estudios Longitudinales , Insectos Vectores/efectos de los fármacos , Insectos Vectores/fisiología , Vivienda , Ecosistema , Control de Insectos

RESUMEN

BACKGROUND: The Gran Chaco region is a major hotspot of Chagas disease. We implemented a 9-year program aimed at suppressing house infestation with Triatoma infestans and stopping vector-borne transmission to creole and indigenous (Qom) residents across Pampa del Indio municipality (Argentine Chaco). The aim of the present study was to assess the intervention effects on parasite-based transmission indices and the spatial distribution of the parasite, and test whether house-level variations in triatomine infection with Trypanosoma cruzi declined postintervention and were influenced by household ethnicity, persistent infestation linked to pyrethroid resistance and other determinants of bug infection. METHODS: This longitudinal study assessed house infestation and bug infection with T. cruzi before and after spraying houses with pyrethroids and implemented systematic surveillance-and-response measures across four operational areas over the period 2007-2016. Live triatomines were individually examined for infection by optical microscopy or kinetoplast DNA (kDNA)-PCR and declared to be infected with T. cruzi when assessed positive by either method. RESULTS: The prevalence of infection with T. cruzi was 19.4% among 6397 T. infestans examined. Infection ranged widely among the study areas (12.5-26.0%), household ethnicity (15.3-26.9%), bug ecotopes (1.8-27.2%) and developmental stages (5.9-27.6%), and decreased from 24.1% (baseline) to 0.9% (endpoint). Using random-intercept multiple logistic regression, the relative odds of bug infection strongly decreased as the intervention period progressed, and increased with baseline domestic infestation and bug stage and in Qom households. The abundance of infected bugs and the proportion of houses with ≥ 1 infected bug remained depressed postintervention and were more informative of area-wide risk status than the prevalence of bug infection. Global spatial analysis revealed sharp changes in the aggregation of bug infection after the attack phase. Baseline domestic infestation and baseline bug infection strongly predicted the future occurrence of bug infection, as did persistent domestic infestation in the area with multiple pyrethroid-resistant foci. Only 19% of houses had a baseline domestic infestation and 56% had ever had ≥ 1 infected bug. CONCLUSIONS: Persistent bug infection postintervention was closely associated with persistent foci generated by pyrethroid resistance. Postintervention parasite-based indices closely agreed with human serosurveys at the study endpoint, suggesting transmission blockage. The program identified households and population subgroups for targeted interventions and opened new opportunities for risk prioritization and sustainable vector control and disease prevention.

Asunto(s)

Enfermedad de Chagas , Piretrinas , Triatoma , Trypanosoma cruzi , Animales , Humanos , Triatoma/parasitología , Prevalencia , Estudios Longitudinales , Insectos Vectores/parasitología , Enfermedad de Chagas/epidemiología , Enfermedad de Chagas/prevención & control , Piretrinas/farmacología , ADN de Cinetoplasto , Argentina/epidemiología

RESUMEN

BACKGROUND: The elimination of Triatoma infestans, the main domestic vector of Trypanosoma cruzi, is lagging behind expectations in the Gran Chaco region. We implemented an insecticide-based intervention program and assessed its long-term effects on house infestation and bug abundance in a resource-constrained municipality (Pampa del Indio, northeastern Argentina) inhabited by creole and the Qom indigenous people (2007-2016). Key questions were whether district-wide data integration revealed patterns concealed at lower spatial levels; to what extent preintervention infestation and pyrethroid resistance challenged the effectiveness of insecticide-based control efforts, and how much control effort was needed to meet defined targets. METHODS: Supervised vector control teams i) georeferenced every housing unit at baseline (1,546); ii) evaluated house infestation using timed-manual searches with a dislodging aerosol across four rural areas designated for district-wide scaling up; iii) sprayed with pyrethroid insecticide 92.7% of all houses; iv) periodically monitored infestation and promoted householder-based surveillance, and v) selectively sprayed the infested houses, totaling 1,823 insecticide treatments throughout the program. RESULTS: Baseline house infestation (mean, 26.8%; range, 14.4-41.4%) and bug abundance plummeted over the first year postintervention (YPI). Timed searches at baseline detected 61.4-88.0% of apparent infestations revealed by any of the methods used. Housing dynamics varied widely among areas and between Qom and creole households. Preintervention triatomine abundance and the cumulative frequency of insecticide treatments were spatially aggregated in three large clusters overlapping with pyrethroid resistance, which ranged from susceptible to high. Persistent foci were suppressed with malathion. Aggregation occurred mainly at house compound or village levels. Preintervention domestic infestation and abundance were much greater in Qom than in creole households, whereas the reverse was recorded in peridomestic habitats. House infestation, rare (1.9-3.7%) over 2-6 YPI, averaged 0.66% (95% confidence interval, 0.28-1.29%) at endpoint. CONCLUSIONS: Upscale integration revealed multiple coupled heterogeneities (spatial, sociodemographic and biological) that reflect large inequalities, hamper control efforts, and provide opportunities for targeted, sustainable disease control. High-coverage, professional insecticide spraying combined with systematic surveillance-and-response were essential ingredients to achieve the quasi-elimination of T. infestans within 5 YPI and concomitant transmission blockage despite various structural threats and constraints.

Asunto(s)

Enfermedad de Chagas , Insecticidas , Piretrinas , Triatoma , Animales , Humanos , Triatoma/fisiología , Insecticidas/farmacología , Control de Insectos/métodos , Enfermedad de Chagas/epidemiología , Piretrinas/farmacología , Argentina/epidemiología

RESUMEN

The interruption of domestic vector-borne transmission of Trypanosoma cruzi in the Americas remains one of the main goals of the World Health Organization 2021-2030 road map for neglected tropical diseases. We implemented a longitudinal intervention program over 2015-2022 to suppress (peri)domestic Triatoma infestans in the municipality of Avia Terai, Chaco Province, Argentina and found that house infestation (3851 houses inspected) and triatomine abundance decreased over the first 2 years post-intervention (YPI), and remained stable thereafter associated to moderate pyrethroid resistant foci. Here we assessed selected components of transmission risk after interventions across the rural-to-urban gradient. We used multistage random sampling to select a municipality-wide sample of T. infestans. We examined 356 insects collected in 87 houses for T. cruzi infection using kDNA-PCR and identified their bloodmeal sources using an indirect ELISA. The overall prevalence of T. cruzi infection post-intervention was 1.7% (95% CI 0.7-3.6). Few houses (5.7%) (95% CI 2.5-12.8) harbored infected triatomines across the gradient. Infected triatomines were found in 5 peri­urban or rural dwellings over 1-4 years post-intervention. No infected insect was found in the urban area. The human blood index decreased from 66.2 at baseline to 42.8 at 1YPI and then increased to 92.9 at 4-5 YPI in the few infested domiciles detected. The percentage of houses with human-fed bugs displayed a similar temporal trend. Our results indicate marginal risks of domestic vector-borne transmission across the district after implementation of the intervention program. Ensuring sustainable vector surveillance coupled with human etiological diagnosis and treatment in hiperendemic areas like the Gran Chaco region, is urgently needed. 252 words.

Asunto(s)

Enfermedad de Chagas , Triatoma , Trypanosoma cruzi , Animales , Humanos , Insectos Vectores , Enfermedad de Chagas/epidemiología , Enfermedad de Chagas/prevención & control , Control de Insectos/métodos , Argentina/epidemiología

RESUMEN

BACKGROUND: Triatomine elimination efforts and the interruption of domestic transmission of Trypanosoma cruzi are hampered by pyrethroid resistance. Fluralaner, a long-lasting ectoparasiticide administered to dogs, substantially reduced site infestation and abundance of pyrethroid-resistant Triatoma infestans Klug (Heteroptera: Reduviidae) in an ongoing 10-month trial in Castelli (Chaco Province, Argentina). We assessed the effects of fluralaner on vector infection with T. cruzi and blood meal sources stratified by ecotope and quantified its medium-term effects on site infestation and triatomine abundance. METHODS: We conducted a placebo-controlled, before-and-after efficacy trial of fluralaner in 28 infested sites over a 22-month period. All dogs received either an oral dose of fluralaner (treated group) or placebo (control group) at 0 month post-treatment [MPT]. Placebo-treated dogs were rescue-treated with fluralaner at 1 MPT, as were all eligible dogs at 7 MPT. Site-level infestation and abundance were periodically assessed by timed manual searches with a dislodging aerosol. Vector infection was mainly determined by kDNA-PCR and blood meal sources were determined by enzyme-linked immunosorbent assay. RESULTS: In fluralaner-treated households, site infestation dropped from 100% at 0 MPT to 18-19% over the period 6-22 MPT while mean abundance plummeted from 5.5 to 0.6 triatomines per unit effort. In control households, infestation dropped similarly post-treatment. The overall prevalence of T. cruzi infection steadily decreased from 13.8% at 0-1 MPT (baseline) to 6.4% and subsequently 2.3% thereafter, while in domiciles, kitchens and storerooms it dropped from 17.4% to 4.7% and subsequently 3.3% thereafter. Most infected triatomines occurred in domiciles and had fed on humans. Infected-bug abundance plummeted after fluralaner treatment and remained marginal or nil thereafter. The human blood index of triatomines collected in domiciles, kitchens and storerooms highly significantly fell from 42.9% at baseline to 5.3-9.1% over the period 6-10 MPT, increasing to 36.8% at 22 MPT. Dog blood meals occurred before fluralaner administration only. The cat blood index increased from 9.9% at baseline to 57.9-72.7% over the period 6-10 MPT and dropped to 5.3% at 22 MPT, whereas chicken blood meals rose from 39.6% to 63.2-88.6%. CONCLUSION: Fluralaner severely impacted infestation- and transmission-related indices over nearly 2 years, causing evident effects at 1 MPT, and deserves larger efficacy trials.

Asunto(s)

Enfermedad de Chagas , Insecticidas , Piretrinas , Triatoma , Trypanosoma cruzi , Animales , Argentina/epidemiología , Enfermedad de Chagas/tratamiento farmacológico , Enfermedad de Chagas/prevención & control , Enfermedad de Chagas/veterinaria , Perros , Humanos , Insectos Vectores , Insecticidas/farmacología , Isoxazoles , Piretrinas/farmacología

RESUMEN

We assessed whether fluralaner administered to outbred healthy dogs reduced or supressed site infestation and abundance of pyrethroid-resistant populations of Triatoma infestans Klug (Heteroptera: Reduviidae). We conducted a placebo-controlled before-and-after efficacy trial in 28 infested sites in Castelli (Argentine Chaco) over 10 months. All 72 dogs initially present received either an oral dose of fluralaner (treated group) or placebo (control group) at month 0 posttreatment (MPT). Preliminary results justified treating all 38 control-house dogs with fluralaner 1 month later, and 71 of 78 existing dogs at 7 MPT. Site-level infestation and triatomine abundance were evaluated using timed manual searches with a dislodging aerosol. In the fluralaner-treated group, infestation dropped significantly from 100% at baseline to 19% over 6-10 MPT whereas mean abundance fell highly significantly from 5.5 to 0.8-0.9 triatomines per unit effort. In the placebo group, site infestation and mean abundance remained stable between 0 and 1 MPT, and strongly declined after fluralaner administration from 13.0-14.7 - triatomines at 0-1 MPT to 4.0-4.2 over 6-10 MPT. Only one of 81 noninfested sites before fluralaner treatment became infested subsequently. Fluralaner significantly reduced the site-level infestation and abundance of pyrethroid-resistant T. infestans and should be tested more widely in Phase III efficacy trials.

Asunto(s)

Enfermedad de Chagas , Enfermedades de los Perros , Insecticidas , Piretrinas , Triatoma , Trypanosoma cruzi , Animales , Argentina , Enfermedad de Chagas/prevención & control , Enfermedad de Chagas/veterinaria , Enfermedades de los Perros/prevención & control , Perros , Insectos Vectores , Insecticidas/farmacología , Isoxazoles , Piretrinas/farmacología

RESUMEN

We assessed whether fluralaner administered to outbred healthy dogs reduced or supressed site infestation and abundance of pyrethroid-resistant populations of Triatoma infestans Klug (Heteroptera: Reduviidae). We conducted a placebo-controlled before-and-after efficacy trial in 28 infested sites in Castelli (Argentine Chaco) over 10 months. All 72 dogs initially present received either an oral dose of fluralaner (treated group) or placebo (control group) at month 0 posttreatment (MPT). Preliminary results justified treating all 38 control-house dogs with fluralaner 1 month later, and 71 of 78 existing dogs at 7 MPT. Site-level infestation and triatomine abundance were evaluated using timed manual searches with a dislodging aerosol. In the fluralaner-treated group, infestation dropped significantly from 100% at baseline to 19% over 6-10 MPT whereas mean abundance fell highly significantly from 5.5 to 0.8-0.9 triatomines per unit effort. In the placebo group, site infestation and mean abundance remained stable between 0 and 1 MPT, and strongly declined after fluralaner administration from 13.0-14.7 - triatomines at 0-1 MPT to 4.0-4.2 over 6-10 MPT. Only one of 81 noninfested sites before fluralaner treatment became infested subsequently. Fluralaner significantly reduced the site-level infestation and abundance of pyrethroid-resistant T. infestans and should be tested more widely in Phase III efficacy trials.

Asunto(s)

Piretrinas , Resistencia a los Insecticidas , Enfermedad de Chagas , Control de Vectores de las Enfermedades , Isoxazoles

RESUMEN

We assessed whether fluralaner administered to outbred healthy dogs reduced or supressed site infestation and abundance of pyrethroid-resistant populations of Triatoma infestans Klug (Heteroptera: Reduviidae). We conducted a placebo-controlled before-and-after efficacy trial in 28 infested sites in Castelli (Argentine Chaco) over 10 months. All 72 dogs initially present received either an oral dose of fluralaner (treated group) or placebo (control group) at month 0 posttreatment (MPT). Preliminary results justified treating all 38 control-house dogs with fluralaner 1 month later, and 71 of 78 existing dogs at 7 MPT. Site-level infestation and triatomine abundance were evaluated using timed manual searches with a dislodging aerosol. In the fluralaner-treated group, infestation dropped significantly from 100% at baseline to 19% over 6-10 MPT whereas mean abundance fell highly significantly from 5.5 to 0.8-0.9 triatomines per unit effort. In the placebo group, site infestation and mean abundance remained stable between 0 and 1 MPT, and strongly declined after fluralaner administration from 13.0-14.7 - triatomines at 0-1 MPT to 4.0-4.2 over 6-10 MPT. Only one of 81 noninfested sites before fluralaner treatment became infested subsequently. Fluralaner significantly reduced the site-level infestation and abundance of pyrethroid-resistant T. infestans and should be tested more widely in Phase III efficacy trials.

Asunto(s)

Triatoma , Enfermedad de Chagas , Insecticidas , Enfermedad

RESUMEN

BACKGROUND: The sustainable elimination of Triatoma infestans in the Gran Chaco region represents an enduring challenge. Following the limited effects of a routine pyrethroid insecticide spraying campaign conducted over 2011-2013 (first period) in Avia Terai, an endemic municipality with approximately 2300 houses, we implemented a rapid-impact intervention package to suppress house infestation across the urban-to-rural gradient over 2015-2019 (second period). Here, we assess their impacts and whether persisting infestations were associated with pyrethroid resistance. METHODS: The 2011-2013 campaign achieved a limited detection and spray coverage across settings (< 68%), more so during the surveillance phase. Following community mobilization and school-based interventions, the 2015-2019 program assessed baseline house infestation using a stratified sampling strategy; sprayed all rural houses with suspension concentrate beta-cypermethrin, and selectively sprayed infested and adjacent houses in urban and peri-urban settings; and monitored house infestation and performed selective treatments over the follow-up. RESULTS: Over the first period, house infestation returned to pre-intervention levels within 3-4 years. The adjusted relative odds of house infestation between 2011-2013 and 2015-2016 differed very little (adj. OR: 1.17, 95% CI 0.91-1.51). Over the second period, infestation decreased significantly between 0 and 1 year post-spraying (YPS) (adj. OR: 0.36, 95% CI 0.28-0.46), with heterogeneous effects across the gradient. Mean bug abundance also dropped between 0 and 1 YPS and thereafter remained stable in rural and peri-urban areas. Using multiple regression models, house infestation and bug abundance at 1 YPS were 3-4 times higher if the house had been infested before treatment, or was scored as high-risk or non-participating. No low-risk house was ever infested. Persistent foci over two successive surveys increased from 30.0 to 59.3% across the gradient. Infestation was more concentrated in peridomestic rather than domestic habitats. Discriminating-dose bioassays showed incipient or moderate pyrethroid resistance in 7% of 28 triatomine populations collected over 2015-2016 and in 83% of 52 post-spraying populations. CONCLUSIONS: The intervention package was substantially more effective than the routine insecticide spraying campaign, though the effects were lower than predicted due to unexpected incipient or moderate pyrethroid resistance. Increased awareness and diagnosis of vector control failures in the Gran Chaco, including appropriate remedial actions, are greatly needed.

Asunto(s)

Enfermedad de Chagas/transmisión , Control de Insectos/normas , Insectos Vectores/efectos de los fármacos , Resistencia a los Insecticidas , Insecticidas/farmacología , Piretrinas/farmacología , Triatoma/parasitología , Animales , Argentina/epidemiología , Enfermedad de Chagas/parasitología , Ciudades/estadística & datos numéricos , Ecosistema , Vivienda/estadística & datos numéricos , Humanos , Control de Insectos/métodos , Insectos Vectores/parasitología , Población Rural/estadística & datos numéricos

RESUMEN

BACKGROUND: Interruption of domestic vector-borne transmission of Trypanosoma cruzi is still an unmet goal in several American countries. In 2007 we launched a long-term intervention program aimed to suppress house infestation with the main domestic vector in southern South America (Triatoma infestans) and domestic transmission in Pampa del Indio, a resource-constrained, hyperendemic municipality with 1446 rural houses inhabited by Creole and indigenous people, in the Argentine Chaco ecoregion. Here, we assessed whether the 10-year insecticide-based program combined with community mobilization blocked vector-borne domestic transmission of T. cruzi to humans and dogs. METHODS: We carried out two municipality-wide, cross-sectional serosurveys of humans and dogs (considered sentinel animals) during 2016-2017 to compare with baseline data. We used a risk-stratified random sampling design to select 273 study houses; 410 people from 180 households and 492 dogs from 151 houses were examined for antibodies to T. cruzi using at least two serological methods. RESULTS: The seroprevalence of T. cruzi in children aged <16 years was 2.5% in 2017 (i.e., 4- to 11-fold lower than before interventions). The mean annual force of child infection (λ) sharply decreased from 2.18 to 0.34 per 100 person-years in 2017. One of 102 children born after interventions was seropositive for T. cruzi; he had lifetime residence in an apparently uninfested house, no outside travel history, and his mother was T. cruzi-seropositive. No incident case was detected among 114 seronegative people of all ages re-examined serologically. Dog seroprevalence was 3.05%. Among native dogs, λ in 2016 (1.21 per 100 dog-years) was 5 times lower than at program onset. Six native adult dogs born after interventions and with stable lifetime residence were T. cruzi-seropositive: three had exposure to T. infestans at their houses and one was an incident case. CONCLUSIONS: These results support the interruption of vector-borne transmission of T. cruzi to humans in rural Pampa del Indio. Congenital transmission was the most likely source of the only seropositive child born after interventions. Residual transmission to dogs was likely related to transient infestations and other transmission routes. Sustained vector control supplemented with human chemotherapy can lead to a substantial reduction of Chagas disease transmission in the Argentine Chaco.

Asunto(s)

Enfermedad de Chagas/prevención & control , Enfermedades de los Perros/parasitología , Trypanosoma cruzi/inmunología , Adolescente , Adulto , Anciano , Anciano de 80 o más Años , Animales , Anticuerpos Antiprotozoarios/sangre , Argentina , Enfermedad de Chagas/transmisión , Enfermedad de Chagas/veterinaria , Niño , Preescolar , Estudios Transversales , Enfermedades de los Perros/prevención & control , Perros , Femenino , Humanos , Lactante , Control de Insectos , Insectos Vectores , Masculino , Persona de Mediana Edad , Estudios Seroepidemiológicos , Triatoma

RESUMEN

BACKGROUND: Peri-urban and urban settings have recently gained more prominence in studies on vector-borne transmission of Trypanosoma cruzi due to sustained rural-to-urban migrations and reports of urban infestations with triatomines. Prompted by the finding of Triatoma infestans across the rural-to-urban gradient in Avia Terai, an endemic municipality of the Argentine Chaco, we assessed selected components of domestic transmission risk in order to determine its variation across the gradient. METHODS: A baseline vector survey was conducted between October 2015 and March 2016, following which we used multistage random sampling to select a representative sample of T. infestans at the municipal level. We assessed T. cruzi infection and blood-feeding sources of 561 insects collected from 109 houses using kinetoplast DNA-PCR assays and direct enzyme-linked immunosorbent assays, respectively. We stratified triatomines according to their collection site (domestic or peridomestic), and we further categorized peridomestic sites in ecotopes of low- or high-risk for T. cruzi infection. RESULTS: The overall adjusted prevalence of T. cruzi-infected T. infestans was 1.8% (95% confidence interval [CI] 1.3-2.3) and did not differ between peri-urban (1.7%) and rural (2.2%) environments. No infection was detected in bugs captured in the urban setting; rather, infected triatomines were mainly collected in rural and peri-urban domiciles, occurring in 8% of T. infestans-infested houses. The main blood-feeding sources of domestic and peridomestic triatomines across the gradient were humans and chickens, respectively. The proportion of triatomines that had fed on humans did not differ between peri-urban (62.5%) and rural (65.7%) domiciles, peaking in the few domestic triatomines collected in urban houses and decreasing significantly with an increasing proportion of chicken- and dog- or cat-fed bugs. The relative odds ratio (OR) of having a T. cruzi infection was nearly threefold higher in bugs having a blood meal on humans (OR 3.15), dogs (OR 2.80) or cats (OR: 4.02) in a Firth-penalized multiple logistic model. CONCLUSIONS: Trypanosoma cruzi transmission was likely occurring both in peri-urban and rural houses of Avia Terai. Widespread infestation in a third of urban blocks combined with high levels of human-triatomine contact in the few infested domiciles implies a threat to urban inhabitants. Vector control strategies and surveillance originally conceived for rural areas should be tailored to peri-urban and urban settings in order to achieve sustainable interruption of domestic transmission in the Chaco region.

Asunto(s)

Enfermedad de Chagas/epidemiología , Enfermedad de Chagas/transmisión , Insectos Vectores/parasitología , Triatoma , Trypanosoma cruzi , Adulto , Animales , Argentina/epidemiología , Gatos , Pollos , Perros , Ensayo de Inmunoadsorción Enzimática , Conducta Alimentaria , Femenino , Cabras , Humanos , Masculino , Ratones , Factores de Riesgo , Población Rural

RESUMEN

Background: The sustainable elimination of Triatoma infestans in the Gran Chaco region represents an enduring challenge. Following the limited effects of a routine pyrethroid insecticide spraying campaign conducted over 2011­2013 (first period) in Avia Terai, an endemic municipality with approximately 2300 houses, we implemented a rapid-impact intervention package to suppress house infestation across the urban-to-rural gradient over 2015­2019 (second period). Here, we assess their impacts and whether persisting infestations were associated with pyrethroid resistance. Methods: The 2011­2013 campaign achieved a limited detection and spray coverage across settings (< 68%), more so during the surveillance phase. Following community mobilization and school-based interventions, the 2015­2019 program assessed baseline house infestation using a stratified sampling strategy; sprayed all rural houses with suspension concentrate beta-cypermethrin, and selectively sprayed infested and adjacent houses in urban and peri-urban settings; and monitored house infestation and performed selective treatments over the follow-up. Results: Over the first period, house infestation returned to pre-intervention levels within 3­4 years. The adjusted relative odds of house infestation between 2011­2013 and 2015­2016 differed very little (adj. OR: 1.17, 95% CI 0.91­1.51). Over the second period, infestation decreased significantly between 0 and 1 year post-spraying (YPS) (adj. OR: 0.36, 95% CI 0.28­0.46), with heterogeneous effects across the gradient. Mean bug abundance also dropped between 0 and 1 YPS and thereafter remained stable in rural and peri-urban areas. Using multiple regression models, house infestation and bug abundance at 1 YPS were 3­4 times higher if the house had been infested before treatment, or was scored as high-risk or non-participating. No low-risk house was ever infested. Persistent foci over two successive surveys increased from 30.0 to 59.3% across the gradient. Infestation was more concentrated in peridomestic rather than domestic habitats. Discriminating-dose bioassays showed incipient or moderate pyrethroid resistance in 7% of 28 triatomine populations collected over 2015­2016 and in 83% of 52 post-spraying populations. Conclusions: The intervention package was substantially more effective than the routine insecticide spraying campaign, though the effects were lower than predicted due to unexpected incipient or moderate pyrethroid resistance. Increased awareness and diagnosis of vector control failures in the Gran Chaco, including appropriate remedial actions, are greatly needed.

Asunto(s)

Enfermedad de Chagas , Insecticidas , Resistencia a los Insecticidas , Enfermedad , Triatominae

RESUMEN

BACKGROUND: The occurrence of the major vectors of Chagas disease has historically been linked to poor rural housing, but urban or peri-urban infestations are increasingly being reported. We evaluated a simple risk index to detect houses infested with Triatoma infestans and tested whether house infestation and vector abundance increased across the urban-to-rural gradient in Avia Terai, an endemic municipality of the Argentine Chaco; whether the association between infestation and selected ecological determinants varied across the gradient; and whether urban and peri-urban infestations were associated with population settlement history. METHODS: We conducted a screening survey of house infestation in 2296 urban, peri-urban and rural dwellings to identify high-risk houses based on a simple index, and then searched for triatomines in all high-risk houses and in a systematic sample of low-risk houses. RESULTS: The risk index had maximum sensitivity and negative predictive value, and low specificity. The combined number of infested houses in peri-urban and urban areas equalled that in rural areas. House infestation prevalence was 4.5%, 22.7% and 42.4% across the gradient, and paralleled the increasing trend in the frequency of domestic animals and peridomestic structures. Multiple logistic regression analysis showed that house infestation was positively and significantly associated with the availability of poultry and bug refuges in walls, and was negatively associated with domestic insecticide use. Several pieces of evidence, including absence of spatial aggregation of house infestation, support that T. infestans has been a long-established occupant of urban, peri-urban and rural settings in Avia Terai. CONCLUSIONS: An integrated vector management strategy targeting chicken coops and good husbandry practices may provide more cost-effective returns to insecticide-based vector elimination efforts.

Asunto(s)

Enfermedad de Chagas/transmisión , Vivienda/estadística & datos numéricos , Insectos Vectores/fisiología , Triatoma/fisiología , Urbanización , Animales , Argentina/epidemiología , Enfermedad de Chagas/epidemiología , Ciudades/epidemiología , Composición Familiar , Humanos , Control de Insectos/estadística & datos numéricos , Dinámica Poblacional , Medición de Riesgo , Trypanosoma cruzi

RESUMEN

BACKGROUND: We conducted a matched-pairs trial of three methods for detecting house infestation with triatominae bugs in a well-defined endemic rural area in the Argentine Chaco. METHODS: The three methods included a simple double-sided adhesive tape (ST) installed near host resting sites; timed-manual collections with a dislodging aerosol (TMC, the reference method used by vector control programmes), and householders' bug notifications (HN). Triatomine infestations were evaluated in 103 sites of 54 houses, including domiciles, kitchens and storerooms. RESULTS: In domiciles where Triatoma infestans was collected, sensitivity of each single method decreased from 79% by ST and 77% by HN, to 57% by TMC, and increased to 92% when ST was combined with HN. In peridomestic kitchens and storerooms, TMC was relatively as sensitive as ST and significantly more sensitive than HN. On average, the number of bugs recovered by ST was 0.94 times that collected by TMC. The ST mainly collected early-instar nymphs whereas TMC yielded late (larger) stages. Triatomines caught by ST had significantly lower mean weight-to-length ratios and lower blood-feeding rates than those caught by TMC, suggesting the ST intercepted and trapped vectors seeking a blood meal host. CONCLUSIONS: The ST may effectively replace TMC for detecting T. infestans in domiciles, and is especially apt for early detection of low-density domestic infestations in the frame of community-based surveillance or elimination programmes; decision making on whether an area should be targeted for full-coverage insecticide spraying, and to corroborate that extant conditions are compatible with the interruption of vector-borne transmission.

Asunto(s)

Enfermedad de Chagas/transmisión , Vivienda , Insectos Vectores/fisiología , Triatoma/fisiología , Aerosoles , Animales , Argentina/epidemiología , Enfermedad de Chagas/epidemiología , Estudios Transversales , Humanos , Insecticidas/administración & dosificación , Enfermedades Desatendidas/epidemiología , Piretrinas/administración & dosificación , Población Rural

RESUMEN

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.

Asunto(s)

Enfermedad de Chagas/epidemiología , Enfermedad de Chagas/transmisión , Transmisión de Enfermedad Infecciosa , Relaciones Interpersonales , Población Rural , Adolescente , Adulto , Anciano , Anciano de 80 o más Años , Animales , Argentina/epidemiología , Niño , Preescolar , Economía , Etnicidad , Femenino , Humanos , Lactante , Masculino , Persona de Mediana Edad , Estudios Seroepidemiológicos , Topografía Médica , Triatominae/crecimiento & desarrollo , Adulto Joven

RESUMEN

Fluctuating asymmetry (FA), a phenotypic marker used as indicator of developmental stress or instability, is sometimes associated with insecticide application and resistance. Here we investigated the occurrence and amount of wing size and wing shape FA in Triatoma infestans females and males collected before and 4 months after a community-wide pyrethroid spraying campaign in a well-defined rural area of Pampa del Indio, Argentina. Moderate levels of pyrethroid resistance were previously confirmed for this area, and postspraying house infestation was mainly attributed to this condition. In the absence of insecticide-based selective pressures over the previous 12 years, we hypothesized that 1- if postspraying triatomines were mostly survivors to insecticide spraying (pyrethroid resistant), they would have higher levels of FA than prespraying triatomines. 2- if postspraying triatomines have a selective advantage, they would have lower FA levels than their prespraying counterparts, whereas if postspraying infestation was positively associated with immigrants not exposed to the insecticide, prespraying and postspraying triatomines would display similar FA levels. For 243 adult T. infestans collected at identified sites before insecticide spraying and 112 collected 4 months postspraying, wing size and wing shape asymmetry was estimated from landmark configurations of left and right sides of each individual. At population level, wing size and shape FA significantly decreased in both females and males after spraying. Males displayed greater wing size and shape FA than females. However, at a single peridomestic site that was persistently infested after spraying, FA declined similarly in females whereas the reverse pattern occurred in males. Our results suggest differential survival of adults with more symmetric wings. This pattern may be related to a selective advantage of survivors to insecticide spraying, which may be mediated or not by their pyrethroid-resistant status or to lower triatomine densities after insecticide spraying and the concomitant increase in feeding success.

Asunto(s)

Resistencia a los Insecticidas , Insecticidas/efectos adversos , Piretrinas/efectos adversos , Triatoma/crecimiento & desarrollo , Animales , Argentina , Femenino , Control de Insectos , Masculino , Tamaño de los Órganos/efectos de los fármacos , Dinámica Poblacional , Triatoma/efectos de los fármacos , Alas de Animales/efectos de los fármacos , Alas de Animales/crecimiento & desarrollo

RESUMEN

BACKGROUND: The social determinants of health (SDHs) condition disease distribution and the ways they are handled. Socio-economic inequalities are closely linked to the occurrence of neglected tropical diseases, but empirical support is limited in the case of Chagas disease, caused by the protozoan Trypanosoma cruzi. Herein we assessed the relationship between key structural SDHs and the risk of T. cruzi vector-borne transmission in rural communities of the Argentine Chaco occupied by creoles and an indigenous group (Qom). We used multiple correspondence analysis to quantify the household-level socio-economic position (social vulnerability and assets indices), access to health and sanitation services, and domestic host availability. We identified the most vulnerable population subgroups by comparing their demographic profiles, mobility patterns and distribution of these summary indices, then assessed their spatial correlation and household-level effects on vector domiciliary indices as transmission risk surrogates. RESULTS: Qom households had higher social vulnerability and fewer assets than creoles, as did local movers and migrant households compared with non-movers. We found significantly positive effects of social vulnerability and domestic host availability on infected Triatoma infestans abundance, after adjusting for ethnicity. Access to health and sanitation services had no effect on transmission risk. Only social vulnerability displayed significant global spatial autocorrelation up to 1 km. A hotspot of infected vectors overlapped with an aggregation of most vulnerable households. CONCLUSIONS: This synthetic approach to assess socio-economic related inequalities in transmission risk provides key information to guide targeted vector control actions, case detection and treatment of Chagas disease, towards sustainability of interventions and greater reduction of health inequalities.

Asunto(s)

Enfermedad de Chagas/transmisión , Grupos de Población , Determinantes Sociales de la Salud/etnología , Factores Socioeconómicos , Adolescente , Adulto , Anciano , Animales , Argentina , Enfermedad de Chagas/etnología , Niño , Preescolar , Composición Familiar , Femenino , Humanos , Control de Insectos , Insectos Vectores/parasitología , Masculino , Persona de Mediana Edad , Factores de Riesgo , Población Rural , Encuestas y Cuestionarios , Triatoma/parasitología , Trypanosoma cruzi , Adulto Joven

RESUMEN

Fluctuating asymmetry (FA), a phenotypic marker used as indicator of developmental stress or instability, is sometimes associated with insecticide application and resistance. Here we investigated the occurrence and amount of wing size and wing shape FA in Triatoma infestans females and males collected before and 4 months after a community-wide pyrethroid spraying campaign in a well-defined rural area of Pampa del Indio, Argentina. Moderate levels of pyrethroid resistance were previously confirmed for this area, and postspraying house infestation was mainly attributed to this condition. In the absence of insecticide-based selective pressures over the previous 12 years, we hypothesized that 1- if postspraying triatomines were mostly survivors to insecticide spraying (pyrethroid resistant), they would have higher levels of FA than prespraying triatomines. 2- if postspraying triatomines have a selective advantage, they would have lower FA levels than their prespraying counterparts, whereas if postspraying infestation was positively associated with immigrants not exposed to the insecticide, prespraying and postspraying triatomines would display similar FA levels. For 243 adult T. infestans collected at identified sites before insecticide spraying and 112 collected 4 months postspraying, wing size and wing shape asymmetry was estimated from landmark configurations of left and right sides of each individual. At population level, wing size and shape FA significantly decreased in both females and males after spraying. Males displayed greater wing size and shape FA than females. However, at a single peridomestic site that was persistently infested after spraying, FA declined similarly in females whereas the reverse pattern occurred in males. Our results suggest differential survival of adults with more symmetric wings. This pattern may be related to a selective advantage of survivors to insecticide spraying, which may be mediated or not by their pyrethroid-resistant status or to lower triatomine densities after insecticide spraying and the concomitant increase in feeding success.

Asunto(s)

Piretrinas , Triatoma , Alas de Animales , Resistencia a los Insecticidas , Enfermedad de Chagas

RESUMEN

BACKGROUND: Insecticide spraying campaigns designed to suppress the principal vectors of the Chagas disease usually lack an active surveillance system that copes with house reinvasion. Following an insecticide campaign with no subsequent surveillance over a 12-year period, we implemented a longitudinal intervention programme including periodic surveys for Triatoma infestans, full-coverage house spraying with insecticides, and selective control in a well-defined rural area of the Argentinean Chaco inhabited by Creoles and one indigenous group (Qom). Here, we conducted a cross-sectional study and report the age-specific seroprevalence of human T. cruzi infection by group, and examine the association between human infection, the onset of the intervention, the relative density of infected domestic bugs, and the household number of infected people, dogs, or cats. RESULTS: The seroprevalence of infection among 691 residents examined was 39.8% and increased steadily with age, reaching 53-70% in those older than 20 years. The mean annual force of infection was 2.5 per 100 person-years (95% CI: 1.8-3.3%). Infection in children younger than 16 years born before the intervention programme was two to four times higher in houses with infected T. infestans than in houses without them and was six times higher when there were both infected dogs or cats and bugs than when they were absent. The model-averaged estimate of the intervention effect suggests that the odds of seropositivity were about nine times smaller for those born after the onset of the intervention than for those born before it, regardless of ethnic background, age, gender, household wealth, and cohabitation with T. cruzi-infected vectors or human hosts. Human infection was also closely associated with the baseline abundance of infected domestic triatomines and the number of infected cohabitants. Two of 43 children born after interventions were T. cruzi-seropositive; since their mothers were seropositive and both resided in apparently uninfested houses they were attributed to vertical transmission. Alternatively, these cases could be due to non-local vector-borne transmission. CONCLUSIONS: Our study reveals high levels of human infection with T. cruzi in the Argentinean Chaco, and the immediate impact of sustained vector surveillance and selective control actions on transmission.

Asunto(s)

Animales Domésticos/parasitología , Enfermedad de Chagas/epidemiología , Enfermedades de los Perros/parasitología , Insectos Vectores/parasitología , Triatominae/parasitología , Adolescente , Adulto , Animales , Argentina/epidemiología , Enfermedades de los Gatos/epidemiología , Enfermedades de los Gatos/microbiología , Enfermedades de los Gatos/parasitología , Enfermedades de los Gatos/transmisión , Gatos , Enfermedad de Chagas/inmunología , Enfermedad de Chagas/parasitología , Enfermedad de Chagas/veterinaria , Niño , Preescolar , Estudios Transversales , Enfermedades de los Perros/epidemiología , Enfermedades de los Perros/prevención & control , Enfermedades de los Perros/transmisión , Perros , Composición Familiar , Femenino , Humanos , Lactante , Insectos Vectores/efectos de los fármacos , Insecticidas/administración & dosificación , Insecticidas/farmacología , Masculino , Estudios Seroepidemiológicos , Trypanosoma cruzi/inmunología , Trypanosoma cruzi/aislamiento & purificación , Adulto Joven