Eco-epidemiological study of an endemic Chagas disease region in northern Colombia reveals the importance of Triatoma maculata (Hemiptera: Reduviidae), dogs and Didelphis marsupialis in Trypanosoma cruzi maintenance

Abstract

BackgroundIn Colombia, Rhodnius prolixus and Triatoma dimidiata are the main domestic triatomine species known to transmit T. cruzi. However, there are multiple reports of T. cruzi transmission involving secondary vectors. In this work, we carried out an eco-epidemiological study on Margarita Island, located in the Caribbean region of Colombia, where Chagas disease is associated with non-domiciliated vectors.MethodsTo understand the transmission dynamics of Trypanosoma cruzi in this area, we designed a comprehensive, multi-faceted study including the following: (i) entomological evaluation through a community-based insect-surveillance campaign, blood meal source determination and T. cruzi infection rate estimation in triatomine insects; (ii) serological determination of T. cruzi prevalence in children under 15 years old, as well as in domestic dogs and synanthropic mammals; (iii) evaluation of T. cruzi transmission capacity in dogs and Didelphis marsupialis, and (iv) genetic characterization of T. cruzi isolates targeting spliced-leader intergene region (SL-IR) genotypes.ResultsOut of the 124 triatomines collected, 94 % were Triatoma maculata, and 71.6 % of them were infected with T. cruzi. Blood-meal source analysis showed that T. maculata feeds on multiple hosts, including humans and domestic dogs. Serological analysis indicated 2 of 803 children were infected, representing a prevalence of 0.25 %. The prevalence in domestic dogs was 71.6 % (171/224). Domestic dogs might not be competent reservoir hosts, as inferred from negative T. cruzi xenodiagnosis and haemoculture tests. However, 61.5 % (8/13) of D. marsupialis, the most abundant synanthropic mammal captured, were T. cruzi-positive on xenodiagnosis and haemocultures.ConclusionsThis study reveals the role of peridomestic T. maculata and dogs in T. cruzi persistence in this region and presents evidence that D. marsupialis are a reservoir mediating peridomestic-zoonotic cycles. This picture reflects the complexity of the transmission dynamics of T. cruzi in an endemic area with non-domiciliated vectors where active human infection exists. There is an ongoing need to control peridomestic T. maculata populations and to implement continuous reservoir surveillance strategies with community participation.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-015-1100-2) contains supplementary material, which is available to authorized users.

Untangling the transmission dynamics of primary and secondary vectors of Trypanosoma cruzi in Colombia: parasite infection, feeding sources and discrete typing units

“…We observed a high invasion of domestic ecotopes by this species (Fig. 2), consistent with other studies in Colombia, Brazil and Venezuela where this species even presents morphological and genetic changes across individuals collected in domestic ecotopes [26, 27, 32–34]. Triatoma maculata has not been included in the vector control programs because its diet is mainly composed of bird blood [32, 35–37] and some studies have reported low frequency of infection in Brazil and Venezuela [36, 38].…”

“…By contrast, herein the frequency of T. cruzi infection was 67.6% and the percentage of feeding with human blood was 75.0% with the presence of TcIDom in some specimens collected in peridomiciliary habitats. Recent studies in Colombia and Venezuela have revealed infection frequencies between 38.0 and 75.0% and the presence of “TcIb” genotype that is associated with the peridomestic cycle [26, 27, 33, 34, 39, 40]. Regarding the DTUs herein detected, most of the specimens were infected with TcI and TcIII (sylvatic DTUs) and domestic specimens harbored TcIII suggesting how T. maculata can connect domestic and sylvatic transmision cycles (Fig.…”

“…This is of paramount relevance due to the impact of sylvatic T. cruzi in the acute phase and outbreaks of oral transmission. Additionally, statistically significant association between food sources (human and opossum) and T. cruzi infection reaffirms the potential of D. marsupialis as an important reservoir of the parasite [25, 26]. …”

Estudio de componentes hemolinfáticos de Rhodnius prolixus y Triatoma maculata alimentados con diferentes fuentes sanguíneas

“…En Venezuela T. maculata ha sido considerado tradicionalmente como un vector secundario del agente etiológico de la enfermedad de Chagas, ya que aunque se le ha encontrado infectado naturalmente por T. cruzi, se considera que está adaptado a hábitats peridomiciliarios y silvestres, siendo una especie principalmente ornitófaga, asociada con gallinas y palomas que raramente se alimenta del hombre 2,8 . Sin embargo recientemente ha estado emergiendo un nuevo escenario epidemiológico de esta especie en Venezuela 9-14 y países vecinos como Brasil 15,16 y Colombia 17,18 ya que ha sido encontrada domiciliada y en medios urbanos, lo cual impone la necesidad de revisar el carácter secundario en su capacidad de transmitir al agente etiológico de la enfermedad de Chagas. Pese a que todas las especies de triatominos son potencialmente vectores de T. cruzi 5 , la capacidad vectorial está sujeta a múltiples factores entre los que se encuentran por ejemplo la composición faunística local disponible al insecto, la competencia de transmisión del parásito a mamíferos domésticos, sinantrópicos y silvestres, la tasa de contacto hospedador-vector o la adaptación a diferentes fuentes sanguíneas.…”

Peer Review #1 of "Sylvatic host associations of Triatominae and implications for Chagas disease reservoirs: a review and new host records based on archival specimens (v0.2)"

“…Studies focusing on the host associations of such species could help to inform policies to limit their impact, for example, by identifying primary vertebrate hosts of sylvatic species. However, most existing studies have focused on known primary vector species and often targeted only domestic or peridomestic habitats where the transmission risk to humans is considered higher (e.g., [40,41] Manuscript to be reviewed broad or specific results for several sets of previously used primers listed in Table 1 (all those listed without asterisks). These primers amplified the corresponding DNA sequence of certain species of Triatominae or did not amplify DNA that should be present based on the results of other primer sets.…”