Correction: Urban vectors of Chagas disease in the American continent: A systematic review of epidemiological surveys.

[This corrects the article DOI: 10.1371/journal.pntd.0011003.].

Urban vectors of Chagas disease in the American continent: A systematic review of epidemiological surveys.

BACKGROUND: Chagas is a complex and multidimensional socio-environmental health phenomenon, in which different components converge and interact. Historically, this disease was associated with insect vectors found in the rural environment. However, in the Americas, we are currently facing a new paradigm, in which different scenarios allow maintaining the vectorial transmission of the parasite through triatomine populations that either occasionally enter the dwellings or colonize urban environments. METHODOLOGY/PRINCIPAL FINDINGS: Records of scientific reports available in the PubMed and LILACS search engines were retrieved, using three criteria according to the main triatomine genera of epidemiological importance and to the general scientific production on Chagas disease in urban contexts. Results showed that records on the occurrence of vectors in urban dwellings began to increase in the last three decades. Results also showed that the main species of triatomines collected inside dwellings (18 in total) belong mainly to the genera Triatoma and Panstrongylus, with most species (16/18, 88.8%) infected with the parasite, and that infestation of triatomine species occurs in all types of cities (small, medium and large, including megalopolises), from Argentina to the USA. CONCLUSIONS/SIGNIFICANCE: Urban Chagas represents a new challenge that adds a different dimension to the problem of Chagas disease due to the particular characteristics of the lifestyle in urban agglomerates. The new scenario will require adaptations of the programs of control of vector to this shift from rural to urban settlements.

Characterization of melanic and non-melanic forms in domestic and peridomestic populations of Triatoma infestans (Hemiptera: Reduviidae).

BACKGROUND: Melanic (dark) morphs have been barely reported in peridomestic and sylvatic conditions for Triatoma infestans, the most important vector of Chagas disease in the Southern Cone of South America. Adults with dark and small yellow markings on the connexivum were collected after manual searches conducted by technical personnel in 62 domiciliary units in Cruz del Eje, Córdoba Province, Argentina. The last community-wide insecticide spraying campaign before the study had been conducted three years earlier. We investigated if there was a measurable color morph variation (melanic and non-melanic) in wings and connexivum; we determined infestation, distribution of melanic and non-melanic forms, and correspondence of colorimetric variation with variations in morphology (wing size and shape and body length), development (wing fluctuating asymmetry), physiology (nutritional status) or behaviour (flight initiation). RESULTS: Forty-nine females, 54 males and 217 nymphs were collected in 24 domiciliary units. House infestation and colonization were 53% and 47%, respectively. Most of the T. infestans individuals (83.2%) were collected in chicken coops; intradomicile infestation was recorded in only one case. The chromatic cluster analysis showed two well-defined groups: melanic and non-melanic. The melanic group included 17 (35%) females and 25 (46%) males. Peridomestic infestation was lower for melanic than for non-melanic adults. Melanic morphs were collected in houses from several localities. Sexual dimorphisms were confirmed by morphometric measurements. Body length was large in melanic adults (P < 0.01 only for males). Differences between groups were significant for wing size and shape, but not for weight or weight/body length ratio. Melanic females and males showed significantly higher fluctuating asymmetry (FA) indices than their non-melanic counterparts. CONCLUSIONS: This is the second report of melanic forms of T. infestans in domestic and peridomestic habitats in the Dry Chaco region of Argentina. Although non-melanic adults exhibited a higher infestation rate, melanic adults were widespread in the area and were collected in the infested domicile and in most types of peridomestic annexes. Differences in morphometric variables between groups might be due to different ecological adaptations. The higher FA levels observed in melanic individuals suggest a higher developmental instability and a selective advantage of non-melanic individuals in domestic and peridomestic habitats.

Fluctuating asymmetry and exposure to pyrethroid insecticides in Triatoma infestans populations in northeastern Argentina.

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.

Occurrence of domestic and intrusive triatomines (Hemiptera: Reduviidae) in sylvatic habitats of the temperate Monte Desert ecoregion of Argentina.

The eco-epidemiology of Triatominae and Trypanosoma cruzi transmission has been little studied in the Argentinean Monte ecoregion. Herein, we provide a comprehensive description of domestic and intrusive triatomines to evaluate the risk of reinfestation of rural dwellings. Triatoma infestans, T. patagonica, T. garciabesi and T. eratyrusiformis were collected by active searches or light traps. None were infected with T. cruzi. One T. infestans male was collected at 1.3 km from the nearest infested house. The finding of intrusive and domestic triatomines in sylvatic foci emphasizes the need of implementing an effective vector surveillance system.

Morphometric variability among the species of the Sordida subcomplex (Hemiptera: Reduviidae: Triatominae): evidence for differentiation across the distribution range of Triatoma sordida.

BACKGROUND: The Sordida subcomplex (Triatominae) comprises four species, Triatoma garciabesi, T. guasayana, T. patagonica and T. sordida, which differ in epidemiological importance and adaptations to human environments. Some morphological similarities among species make taxonomic identification, population differentiation and species delimitation controversial. Triatoma garciabesi and T. sordida are the most similar species, having been considered alternatively two and a single species until T. garciabesi was re-validated, mostly based on the morphology of male genitalia. More recently, T. sordida from Argentina has been proposed as a new cryptic species distinguishable from T. sordida from Brazil, Bolivia and Paraguay by cytogenetics. We studied linear and geometric morphometry of the head, wings and pronotum in populations of these species aiming to find phenotypic markers for their discrimination, especially between T. sordida and T. garciabesi, and if any set of variables that validates T. sordida from Argentina as a new species. RESULTS: Head width and pronotum length were the linear variables that best differentiated species. Geometric morphometry revealed significant Mahalanobis distances in wing shape between all pairwise comparisons. Triatoma patagonica exhibited the best discrimination and T. garciabesi overlapped the distribution of the other species in the morphometric space of the first two DFA axes. Head shape showed differentiation between all pairs of species except for T. garciabesi and T. sordida. Pronotum shape did not differentiate T. garciabesi from T. guasayana. The comparison between T. garciabesi and T. sordida from Argentina and T. sordida from Brazil and Bolivia revealed low differentiation based on head and pronotum linear measurements. Pronotum and wing shape were different between T. garciabesi and T. sordida from Brazil and Bolivia and T. sordida from Argentina. Head shape did not differentiate T. garciabesi from T. sordida from Argentina. CONCLUSIONS: Wing shape best delimited the four species phenotypically. The proposed cryptic species, T. sordida from Argentina, differed from T. sordida from Brazil and Bolivia in all measured shape traits, suggesting that the putative new species may not be cryptic. Additional studies integrating cytogenetic, phenotypic and molecular markers, as well as cross-breeding experiments are needed to confirm if these three entities represent true biological species.

Fine-scale genetic structure of Triatoma infestans in the Argentine Chaco.

The patterns of genetic structure in natural populations provide essential information for the improvement of pest management strategies including those targeting arthropod vectors of human diseases. We analyzed the patterns of fine-scale genetic structure in Triatoma infestans in a well-defined rural area close to Pampa del Indio, in the Argentine Arid-Humid Chaco transition, where a longitudinal study on house infestation and wing geometric morphometry is being conducted since 2007. A total of 228 insects collected in 16 domestic and peridomestic sites from two rural communities was genotyped for 10 microsatellite loci and analyzed. We did not find departures from Hardy-Weinberg expectations in collection sites, with three exceptions probably due to null alleles and substructuring. Domestic sites were more variable than peridomestic sites suggesting the presence of older bug populations in domestic sites or higher effective population sizes. Significant genetic structure was detected using F-statistics, a discriminant analysis of principal components and Bayesian clustering algorithms in an area of only 6.32 km(2). Microsatellite markers detected population structuring at a finer geographic scale (180-6300 m) than a previous study based on wing geometric morphometry (>4000 m). The spatial distribution of genetic variability was more properly explained by a hierarchical island than by an isolation-by-distance model. This study illustrates that, despite more than a decade without vector control interventions enhancing differentiation, genetic structure can be detected in T. infestans populations, particularly applying spatial information. This supports the potential of genetic studies to provide key information for hypothesis testing of the origins of house reinfestation.

Where do these bugs come from? Phenotypic structure of Triatoma infestans populations after control interventions in the Argentine Chaco.

House re-invasion by native triatomines after insecticide-based control campaigns represents a major threat for Chagas disease vector control. We conducted a longitudinal intervention study in a rural section (Area III, 407 houses) of Pampa del Indio, northeastern Argentina, and used wing geometric morphometry to compare pre-spray and post-spray (re-infestant bugs) Triatoma infestans populations. The community-wide spraying with pyrethroids reduced the prevalence of house infestation by T. infestans from 31.9% to < 1% during a four-year follow-up, unlike our previous studies in the neighbouring Area I. Two groups of bug collection sites differing in wing shape variables before interventions (including 221 adults from 11 domiciles) were used as a reference for assigning 44 post-spray adults. Wing shape variables from post-spray, high-density bug colonies and pre-spray groups were significantly different, suggesting that re-infestant insects had an external origin. Insects from one house differed strongly in wing shape variables from all other specimens. A further comparison between insects from both areas supported the existence of independent re-infestation processes within the same district. These results point to local heterogeneities in house re-infestation dynamics and emphasise the need to expand the geographic coverage of vector surveillance and control operations to the affected region.

Where do these bugs come from? Phenotypic structure of Triatoma infestans populations after control interventions in the Argentine Chaco

House re-invasion by native triatomines after insecticide-based control campaigns represents a major threat for Chagas disease vector control. We conducted a longitudinal intervention study in a rural section (Area III, 407 houses) of Pampa del Indio, northeastern Argentina, and used wing geometric morphometry to compare pre-spray and post-spray (re-infestant bugs) Triatoma infestans populations. The community-wide spraying with pyrethroids reduced the prevalence of house infestation by T. infestans from 31.9% to < 1% during a four-year follow-up, unlike our previous studies in the neighbouring Area I. Two groups of bug collection sites differing in wing shape variables before interventions (including 221 adults from 11 domiciles) were used as a reference for assigning 44 post-spray adults. Wing shape variables from post-spray, high-density bug colonies and pre-spray groups were significantly different, suggesting that re-infestant insects had an external origin. Insects from one house differed strongly in wing shape variables from all other specimens. A further comparison between insects from both areas supported the existence of independent re-infestation processes within the same district. These results point to local heterogeneities in house re-infestation dynamics and emphasise the need to expand the geographic coverage of vector surveillance and control operations to the affected region.