The potential of canine sentinels for reemerging Trypanosoma cruzi transmission

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Abstract

Background

Chagas disease, a vector-borne disease transmitted by triatomine bugs and caused by the parasite Trypanosoma cruzi, affects millions of people in the Americas. In Arequipa, Peru, indoor residual insecticide spraying campaigns are routinely conducted to eliminate Triatoma infestans, the only vector in this area. Following insecticide spraying, there is risk of vector return and reinitiation of parasite transmission. Dogs are important reservoirs of T. cruzi and may play a role in reinitiating transmission in previously sprayed areas. Dogs may also serve as indicators of reemerging transmission.

Methods

We conducted a cross-sectional serological screening to detect T. cruzi antibodies in dogs, in conjunction with an entomological vector collection survey at the household level, in a disease endemic area that had been treated with insecticide 13 years prior. Spatial clustering of infected animals and vectors was assessed using Ripley’s K statistic, and the odds of being seropositive for dogs proximate to infected colonies was estimated with multivariate logistic regression.

Results

There were 106 triatomine-infested houses (41.1%), and 45 houses infested with T. cruzi-infected triatomine insects (17.4%). Canine seroprevalence in the area was 12.3% (n = 154); all seropositive dogs were 9 months old or older. We observed clustering of vectors carrying the parasite, but no clustering of seropositive dogs. The age- and sex-adjusted odds ratio between seropositivity to T. cruzi and proximity to an infected triatomine (≤50 m) was 5.67 (95% CI: 1.12–28.74; p = 0.036).

Conclusions

Targeted control of reemerging transmission can be achieved by improved understanding of T. cruzi in canine populations. Our results suggest that dogs may be useful sentinels to detect re-initiation of transmission following insecticide treatment. Integration of canine T. cruzi blood sampling into existing interventions for zoonotic disease control (e.g., rabies vaccination programs) can be an effective method of increasing surveillance and improving understanding of disease distribution.

Introduction

Chagas disease is a zoonotic and vector-borne disease caused by Trypanosoma cruzi, and is arguably the most important parasitic disease in the Americas (World Health Organization, 2008), where 8 million people are infected (World Health Organization, 2014). The parasite is transmitted primarily by triatomine bugs and control programs are focused on reducing or eliminating vector populations through insecticide application (Dias, 2007). The insecticide effect passes after some months and, after this occurs, reinfestation with the vector often initiates (Cecere et al., 2006), and re-emergence of T. cruzi transmission may occur (Delgado et al., 2011). Vector reinfestation is a serious problem for Chagas control; a systematic review concluded: “reinfestation of dwelling by native vector species is common, spatially widespread, and temporally persistent” (Abad-Franch et al., 2011). Recurrence of this process of vector reinfestation and transmission re-emergence may threaten current achievements of Chagas disease control programs. Animal sentinels could be used to detect early re-emergence of transmission and thereby signal the need for additional control activities to prevent transmission to humans.

T. cruzi can infect a variety of animals. Several mammal species have been identified as reservoirs and/or carriers of the parasite. Wild mammals such as opossums, raccoons, skunks, armadillos, mice, rats and other rodents have been reported as T. cruzi reservoirs (Alvarado-Otegui et al., 2012, Brown et al., 2010, Pinto et al., 2006). Among domestic animals, dogs have been implicated in several studies as reservoirs of T. cruzi (Cardinal et al., 2008, Fujita et al., 1994, Gürtler et al., 2007, Jimenez-Coello et al., 2010) and may play an important intermediary role in the transmission of the parasite to humans (Gürtler et al., 2005), particularly in those T. cruzi systems where there is a high degree of intradomiciliary transmission. Infection of dogs with the parasite occurs by vectorial transmission as well as by the oral route (dogs eating insects or infected mammals) (Cardinal et al., 2006, Reithinger et al., 2005), triatomine insects show a preference to feed on dogs (Gürtler et al., 2009a), and dogs tend to live more proximate to humans compared to other animals, such as cattle or poultry. These facts make it likely that, in the process of re-emergence of T. cruzi transmission, dogs may become infected earlier than humans. Therefore, identification of infected dogs and the factors that promote or hinder their infection can be useful for preventing human infection. Here we investigate the potential role of dogs as early indicators of reemerging transmission.

Many species of triatomine bugs are able to transmit T. cruzi (Zeledón and Rabinovich, 1981), but in the southern department of Arequipa, Peru, Triatoma infestans is the only insect vector for the parasite (Levy et al., 2006). In the 1990s the Ministry of Health (MoH) of Peru began systematic campaigns of insecticide spraying in areas affected by triatomines (Dias and Schofield, 1999, Náquira and Cabrera, 2009). These campaigns, like many in Latin America, were conducted without comprehensive information on the extent of T. cruzi transmission in the area (Dias and Schofield, 1999). In the district of La Joya, Arequipa, our study team found that parasite transmission was interrupted in 1995 (Delgado et al., 2011). However, in the years leading up to 2008, dwellers of La Joya reported vector reinfestation in the area. In 2008, the MoH conducted an insecticide spraying campaign and, in collaboration with the MoH, our study team captured 2070 triatomine vectors in human dwellings and 7487 triatomine vectors in peridomestic areas. Remarkably, 96.7% of T. cruzi-carrying triatomine insects were captured in peridomestic areas (unpublished data). We also found that out of more than 500 humans 18 years or younger, only 5 were infected in this area (Delgado et al., 2011). These findings suggest that after vector reinfestation was established in La Joya, T. cruzi transmission was initiated in the peridomiciliary areas, where several domestic animal species, including dogs, can be found.

The objectives of this study were to (i) estimate the seroprevalence of T. cruzi in domestic dogs in an area where T. cruzi transmission was reemerging after insecticide spraying, and (ii) to characterize the spatial association of infected dogs with the distribution of T. cruzi-infected T. infestans.

Section snippets

Ethical statement

All protocols that involved animals were reviewed and approved by the Institutional Animal Care and Use Committee of the Universidad Peruana Cayetano Heredia.

Location and study population

The study was conducted in a village within the district of La Joya, a district located 30.7 km west (Euclidean distance) of the city of Arequipa, the capital of the department of the same name. La Joya sits at an altitude of 1617 m, has an average temperature of 18 °C (range 10–35 °C), humidity ranging between 20% and 85%, and a marked rainy

Statistical methods

Household locations were mapped to visualize the distribution of sampled, unsampled, and seropositive dogs. The location of pens and rooms where entomological surveys were conducted were also mapped to visualize the distribution of surveyed enclosures, infested enclosures, and T.cruzi-infected colonies. The ratios of the spatial intensity of seropositive dogs versus seronegative dogs and positive insect colonies versus negative insect colonies were evaluated with quartic kernels with bandwidths

Results

One hundred and seventy-five dogs lived in the study area and were distributed across 150 households. We obtained blood samples from 154 dogs distributed in 127 households (sampled dogs = 88.0%; household participation rate = 84.7%). Dog age was negatively associated with participation in blood sampling. The sampled dogs were distributed over the study area and participation did not appear to be aggregated in a particular area in this study. Of 258 households in the study area, 253 (98.1%)

Discussion

We document here a relatively high seroprevalence of T. cruzi in dogs in a peri-rural area of Arequipa, Peru. There is a wide range in canine seroprevalence in The Americas, and the seroprevalence of 12.3% estimated in the study village in La Joya, Arequipa lays in the middle of that range (Balan et al., 2011, Bonfante-cabarcas et al., 2011, Cardinal et al., 2007, Gürtler et al., 2007, Kjos et al., 2008, Pineda et al., 2011, Rosypal et al., 2007), and was very similar to that estimated by

Conclusions

Thirteen years after a little-documented vector control campaign, T. cruzi-seroprevalence in dogs was high, suggesting ongoing parasite transmission in the area. By contrast, the patterns of seroprevalence in humans in the same area might be interpreted as evidence that vector-borne transmission had been halted.

Dogs may be useful sentinels to detect re-emergence of T. cruzi transmission and should be considered in surveillance programs. T. cruzi-seropositive dogs are spatially associated with

Acknowledgements

We thank our field and laboratory teams in Arequipa, and the laboratory staff at UPCH-LID. We gratefully acknowledge the work of the following organizations that have organized and conducted the Chagas disease control program in Arequipa: Ministerio de Salud del Perú (MINSA), the Dirección General de Salud de las Personas (DGSP), the Estrategia Sanitaria Nacional de Prevención y Control de Enfermedades Metaxénicas y Otras Transmitidas por Vectores (ESNPCEMOTVS), the Dirección General de Salud

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