Domestic Animal Hosts Strongly Influence Human-Feeding Rates of the Chagas Disease Vector Triatoma infestans in Argentina

Background

The host species composition in a household and their relative availability affect the host-feeding choices of blood-sucking insects and parasite transmission risks. We investigated four hypotheses regarding factors that affect blood-feeding rates, proportion of human-fed bugs (human blood index), and daily human-feeding rates of Triatoma infestans, the main vector of Chagas disease.

Methods

A cross-sectional survey collected triatomines in human sleeping quarters (domiciles) of 49 of 270 rural houses in northwestern Argentina. We developed an improved way of estimating the human-feeding rate of domestic T. infestans populations. We fitted generalized linear mixed-effects models to a global model with six explanatory variables (chicken blood index, dog blood index, bug stage, numbers of human residents, bug abundance, and maximum temperature during the night preceding bug catch) and three response variables (daily blood-feeding rate, human blood index, and daily human-feeding rate). Coefficients were estimated via multimodel inference with model averaging.

Findings

Median blood-feeding intervals per late-stage bug were 4.1 days, with large variations among households. The main bloodmeal sources were humans (68%), chickens (22%), and dogs (9%). Blood-feeding rates decreased with increases in the chicken blood index. Both the human blood index and daily human-feeding rate decreased substantially with increasing proportions of chicken- or dog-fed bugs, or the presence of chickens indoors. Improved calculations estimated the mean daily human-feeding rate per late-stage bug at 0.231 (95% confidence interval, 0.157–0.305).

Conclusions and Significance

Based on the changing availability of chickens in domiciles during spring-summer and the much larger infectivity of dogs compared with humans, we infer that the net effects of chickens in the presence of transmission-competent hosts may be more adequately described by zoopotentiation than by zooprophylaxis. Domestic animals in domiciles profoundly affect the host-feeding choices, human-vector contact rates and parasite transmission predicted by a model based on these estimates.     

Multi-year evolutionary dynamics of West Nile virus in suburban Chicago,USA, 2005–2007

West Nile virus has evolved in concert with its expansion across North America, but little is known about the evolutionary dynamics of the virus on local scales. We analysed viral nucleotide sequences from mosquitoes collected in 2005, 2006, and 2007 from a known transmission ‘hot spot’ in suburban Chicago, USA. Within this approximately 11 × 14 km area, the viral envelope gene has increased approximately 0.1% yr⁻¹ in nucleotide-level genetic diversity. In each year, viral diversity was higher in ‘residential’ sites characterized by dense housing than in more open ‘urban green space’ sites such as cemeteries and parks. Phylodynamic analyses showed an increase in incidence around 2005, consistent with a higher-than-average peak in mosquito and human infection rates that year. Analyses of times to most recent common ancestor suggest that WNV in 2005 and 2006 may have arisen predominantly from viruses present during 2004 and 2005, respectively, but that WNV in 2007 had an older common ancestor, perhaps indicating a predominantly mixed or exogenous origin. These results show that the population of WNV in suburban Chicago is an admixture of viruses that are both locally derived and introduced from elsewhere, containing evolutionary information aggregated across a breadth of spatial and temporal scales.     

Detection of “<Emphasis Type="Italic">Candidatus</Emphasis> Rickettsia sp. strain Argentina”and <Emphasis Type="Italic">Rickettsia bellii</Emphasis> in <Emphasis Type="Italic">Amblyomma</Emphasis> ticks (Acari: Ixodidae) from Northern Argentina

Ixodid ticks were collected from vegetation and from humans, wild and domestic mammals in a rural area in the semi-arid Argentine Chaco in late spring 2006 to evaluate their potential role as vectors of Spotted Fever Group (SFG) rickettsiae. A total of 233 adult ticks, identified as Amblyomma parvum, Amblyomma tigrinum and Amblyomma pseudoconcolor, was examined for Rickettsia spp. We identified an SFG rickettsia of unknown pathogenicity, “Candidatus Rickettsia sp. strain Argentina”, in A. parvum and A. pseudoconcolor by PCR assays targeting gltA, ompA, ompB and 17-kDa outer membrane antigen rickettsial genes. Rickettsia bellii was detected in a host-seeking male of A. tigrinum. Amblyomma parvum is widespread in the study area and is a potential threat to human health.     

Disease-driven reduction in human mobility influences human-mosquito contacts and dengue transmission dynamics

Heterogeneous exposure to mosquitoes determines an individual’s contribution to vector-borne pathogen transmission. Particularly for dengue virus (DENV), there is a major difficulty in quantifying human-vector contacts due to the unknown coupled effect of key heterogeneities. To test the hypothesis that the reduction of human out-of-home mobility due to dengue illness will significantly influence population-level dynamics and the structure of DENV transmission chains, we extended an existing modeling framework to include social structure, disease-driven mobility reductions, and heterogeneous transmissibility from different infectious groups. Compared to a baseline model, naïve to human pre-symptomatic infectiousness and disease-driven mobility changes, a model including both parameters predicted an increase of 37% in the probability of a DENV outbreak occurring; a model including mobility change alone predicted a 15.5% increase compared to the baseline model. At the individual level, models including mobility change led to a reduction of the importance of out-of-home onward transmission (R, the fraction of secondary cases predicted to be generated by an individual) by symptomatic individuals (up to -62%) at the expense of an increase in the relevance of their home (up to +40%). An individual’s positive contribution to R could be predicted by a GAM including a non-linear interaction between an individual’s biting suitability and the number of mosquitoes in their home (>10 mosquitoes and 0.6 individual attractiveness significantly increased R). We conclude that the complex fabric of social relationships and differential behavioral response to dengue illness cause the fraction of symptomatic DENV infections to concentrate transmission in specific locations, whereas asymptomatic carriers (including individuals in their pre-symptomatic period) move the virus throughout the landscape. Our findings point to the difficulty of focusing vector control interventions reactively on the home of symptomatic individuals, as this approach will fail to contain virus propagation by visitors to their house and asymptomatic carriers.     

Ecological patterns of blood-feeding by kissing-bugs (Hemiptera: Reduviidae: Triatominae)

Host use by vectors is important in understanding the transmission of zoonotic diseases, which can affect humans, wildlife and domestic animals. Here, a synthesis of host exploitation patterns by kissing-bugs, vectors of Chagas disease, is presented. For this synthesis, an extensive literature review restricted to feeding sources analysed by precipitin tests was conducted. Modern tools from community ecology and multivariate statistics were used to determine patterns of segregation in host use. Rather than innate preferences for host species, host use by kissing-bugs is influenced by the habitats they colonise. One of the major limitations of studies on kissing-bug foraging has been the exclusive focus on the dominant vector species. We propose that expanding foraging studies to consider the community of vectors will substantially increase the understanding of Chagas disease transmission ecology. Our results indicate that host accessibility is a major factor that shapes the blood-foraging patterns of kissing-bugs. Therefore, from an applied perspective, measures that are directed at disrupting the contact between humans and kissing-bugs, such as housing improvement, are among the most desirable strategies for Chagas disease control.     

Key Source Habitats and Potential Dispersal of Triatoma infestans Populations in Northwestern Argentina: Implications for Vector Control

Background

Triatoma infestans —the principal vector of the infection that causes Chagas disease— defies elimination efforts in the Gran Chaco region. This study identifies the types of human-made or -used structures that are key sources of these bugs in the initial stages of house reinfestation after an insecticide spraying campaign.

Methodology and Principal Findings

We measured demographic and blood-feeding parameters at two geographic scales in 11 rural communities in Figueroa, northwest Argentina. Of 1,297 sites searched in spring, 279 (21.5%) were infested. Bug abundance per site and female fecundity differed significantly among habitat types (ecotopes) and were highly aggregated. Domiciles (human sleeping quarters) had maximum infestation prevalence (38.7%), human-feeding bugs and total egg production, with submaximal values for other demographic and blood-feeding attributes. Taken collectively peridomestic sites were three times more often infested than domiciles. Chicken coops had greater bug abundance, blood-feeding rates, engorgement status, and female fecundity than pig and goat corrals. The host-feeding patterns were spatially structured yet there was strong evidence of active dispersal of late-stage bugs between ecotopes. Two flight indices predicted that female fliers were more likely to originate from kitchens and domiciles, rejecting our initial hypothesis that goat and pig corrals would dominate.

Conclusions and Significance

Chicken coops and domiciles were key source habitats fueling rapid house reinfestation. Focusing control efforts on ecotopes with human-fed bugs (domiciles, storerooms, goat corrals) would neither eliminate the substantial contributions to bug population growth from kitchens, chicken coops, and pig corrals nor stop dispersal of adult female bugs from kitchens. Rather, comprehensive control of the linked network of ecotopes is required to prevent feeding on humans, bug population growth, and bug dispersal simultaneously. Our study illustrates a demographic approach that may be applied to other regions and triatomine species for the design of innovative, improved vector control strategies.     

Historical biogeography of the genus Rhadinaea (Squamata: Dipsadinae)

Multiple geological and climatic events have created geographical or ecological barriers associated with speciation events, playing a role in biological diversification in North and Central America. Here, we evaluate the influence of the Neogene and Quaternary geological events, as well as the climatic changes in the diversification of the colubrid snake genus Rhadinaea using molecular dating and ancestral area reconstruction. A multilocus sequence dataset was generated for 37 individuals of Rhadinaea from most of the biogeographical provinces where the genus is distributed, representing 19 of the 21 currently recognized species, and two undescribed species. Our analyses show that the majority of the Rhadinaea species nest in two main clades, herein identified as “Eastern” and “Southern”. These clades probably diverged from each other in the early Miocene, and their divergence was followed by 11 divergences during the middle to late Miocene, three divergences during the Pliocene, and six divergences in the Pleistocene. The ancestral distribution of Rhadinaea was reconstructed across the Sierra Madre del Sur. Our phylogenetic analyses do not support the monophyly of Rhadinaea. The Miocene and Pliocene geomorphology, perhaps in conjunction with climate change, appears to have triggered the diversification of the genus, while the climatic changes during the Miocene probably induced the diversification of Rhadinaea in the Sierra Madre del Sur. Our analysis suggests that the uplifting of the Trans‐Mexican Volcanic Belt and Chiapan–Guatemalan highlands in this same period resulted in northward and southward colonization events. This was followed by more recent, independent colonization events in the Pliocene and Pleistocene involving the Balsas Basin, Chihuahuan Desert, Pacific Coast, Sierra Madre Occidental, Sierra Madre Oriental, Sierra Madre del Sur, Trans‐Mexican Volcanic Belt, and Veracruz provinces, probably driven by the climatic fluctuations of the time.     

Factors affecting infestation by Triatoma infestans in a rural area of the humid Chaco in Argentina: a multi-model inference approach

Background

Transmission of Trypanosoma cruzi by Triatoma infestans remains a major public health problem in the Gran Chaco ecoregion, where understanding of the determinants of house infestation is limited. We conducted a cross-sectional study to model factors affecting bug presence and abundance at sites within house compounds in a well-defined rural area in the humid Argentine Chaco.

Methodology/Principal Findings

Triatoma infestans bugs were found in 45.9% of 327 inhabited house compounds but only in 7.4% of the 2,584 sites inspected systematically on these compounds, even though the last insecticide spraying campaign was conducted 12 years before. Infested sites were significantly aggregated at distances of 0.8–2.5 km. The most frequently infested ecotopes were domiciles, kitchens, storerooms, chicken coops and nests; corrals were rarely infested. Domiciles with mud walls and roofs of thatch or corrugated tarred cardboard were more often infested (32.2%) than domiciles with brick-and-cement walls and corrugated metal-sheet roofs (15.1%). A multi-model inference approach using Akaike''s information criterion was applied to assess the relative importance of each variable by running all possible (17,406) models resulting from all combinations of variables. Availability of refuges for bugs, construction with tarred cardboard, and host abundance (humans, dogs, cats, and poultry) per site were positively associated with infestation and abundance, whereas reported insecticide use showed a negative association. Ethnic background (Creole or Toba) adjusted for other factors showed little or no association.

Conclusions/Significance

Promotion and effective implementation of housing improvement (including key peridomestic structures) combined with appropriate insecticide use and host management practices are needed to eliminate infestations. Fewer refuges are likely to result in fewer residual foci after insecticide spraying, and will facilitate community-based vector surveillance. A more integrated perspective that considers simultaneously social, economic and biological processes at local and regional scales is needed to attain effective, sustainable vector and disease control.