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.

[1]  P. Nouvellet,et al.  The Improbable Transmission of Trypanosoma cruzi to Human: The Missing Link in the Dynamics and Control of Chagas Disease , 2013, PLoS neglected tropical diseases.

[2]  R. Gilman,et al.  Epidemiology of and Impact of Insecticide Spraying on Chagas Disease in Communities in the Bolivian Chaco , 2013, PLoS neglected tropical diseases.

[3]  L. F. Chaves,et al.  Host Life History Strategy, Species Diversity, and Habitat Influence Trypanosoma cruzi Vector Infection in Changing Landscapes , 2012, PLoS neglected tropical diseases.

[4]  C. Zúniga,et al.  Chagas disease: assessing the existence of a threshold for bug infestation rate. , 2012, The American journal of tropical medicine and hygiene.

[5]  R. Gilman,et al.  Temporal differences in blood meal detection from the midguts of Triatoma infestans. , 2012, Revista do Instituto de Medicina Tropical de Sao Paulo.

[6]  S. Randolph,et al.  Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm , 2012, Parasitology.

[7]  U. Kitron,et al.  Factors Affecting Infestation by Triatoma infestans in a Rural Area of the Humid Chaco in Argentina: A Multi-Model Inference Approach , 2011, PLoS neglected tropical diseases.

[8]  L. F. Chaves,et al.  Ecological patterns of blood-feeding by kissing-bugs (Hemiptera: Reduviidae: Triatominae). , 2011, Memorias do Instituto Oswaldo Cruz.

[9]  I. Jamieson,et al.  Multimodel inference in ecology and evolution: challenges and solutions , 2011, Journal of evolutionary biology.

[10]  Kate E. Jones,et al.  Impacts of biodiversity on the emergence and transmission of infectious diseases , 2010, Nature.

[11]  O. Courtenay,et al.  Of Cattle, Sand Flies and Men: A Systematic Review of Risk Factor Analyses for South Asian Visceral Leishmaniasis and Implications for Elimination , 2010, PLoS neglected tropical diseases.

[12]  L. F. Chaves,et al.  Blood feeding patterns of mosquitoes: random or structured? , 2010, Frontiers in Zoology.

[13]  J. Ribeiro,et al.  Immunogenic Salivary Proteins of Triatoma infestans: Development of a Recombinant Antigen for the Detection of Low-Level Infestation of Triatomines , 2009, PLoS neglected tropical diseases.

[14]  U. Kitron,et al.  Strong Host-Feeding Preferences of the Vector Triatoma infestans Modified by Vector Density: Implications for the Epidemiology of Chagas Disease , 2009, PLoS neglected tropical diseases.

[15]  A. J. Goodchild.  SOME OBSERVATIONS ON GROWTH AND EGG PRODUCTION OP THE BLOOD‐SUCKING REDUVIIDS, RHODNIUS PROLIXUS AND TRIATOMA INFESTANS. , 2009 .

[16]  L. Stevens,et al.  A New Method for Forensic DNA Analysis of the Blood Meal in Chagas Disease Vectors Demonstrated Using Triatoma infestans from Chuquisaca, Bolivia , 2008, PloS one.

[17]  U. Kitron,et al.  Sustainable vector control and management of Chagas disease in the Gran Chaco, Argentina , 2007, Proceedings of the National Academy of Sciences.

[18]  U. Kitron,et al.  Impact of community-based vector control on house infestation and Trypanosoma cruzi infection in Triatoma infestans, dogs and cats in the Argentine Chaco. , 2007, Acta tropica.

[19]  M. Basáñez,et al.  Density-dependent host choice by disease vectors: epidemiological implications of the ideal free distribution. , 2007, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[20]  C. Costantini,et al.  Blood‐feeding behaviour of the malarial mosquito Anopheles arabiensis: implications for vector control , 2006, Medical and veterinary entomology.

[21]  J. Jannin,et al.  The future of Chagas disease control. , 2006, Trends in parasitology.

[22]  U. Kitron,et al.  Comparative Trial of Effectiveness of Pyrethroid Insecticides Against Peridomestic Populations of Triatoma infestans in Northwestern Argentina , 2006, Journal of medical entomology.

[23]  N. Horton.  Multilevel and Longitudinal Modeling Using Stata , 2006 .

[24]  R. Gürtler,et al.  Extinction of experimental Triatoma infestans populations following continuous exposure to dogs wearing deltamethrin-treated collars. , 2006, The American journal of tropical medicine and hygiene.

[25]  R. Ostfeld,et al.  Effects of species diversity on disease risk. , 2006, Ecology letters.

[26]  E. Dumonteil,et al.  Identification in triatomine vectors of feeding sources and Trypanosoma cruzi variants by heteroduplex assay and a multiplex miniexon polymerase chain reaction. , 2006, The American journal of tropical medicine and hygiene.

[27]  P. Billingsley.  The Biology of Blood-Sucking in Insects 2nd Edn. By M. Lehane, pp. 321. Cambridge University Press, 2005. ISBN 0 521 54395 9. Paperback £35.00 (US$ 60.00). , 2005, Parasitology.

[28]  Sophia Rabe-Hesketh,et al.  Multilevel and Longitudinal Modeling Using Stata , 2005 .

[29]  R. Gürtler,et al.  Feeding rates, nutritional status and flight dispersal potential of peridomestic populations of Triatomainfestans in rural northwestern Argentina. , 2005, Acta tropica.

[30]  R. Chuit,et al.  Incidence of trypanosoma cruzi infection among children following domestic reinfestation after insecticide spraying in rural northwestern Argentina. , 2005, The American journal of tropical medicine and hygiene.

[31]  A. Saul,et al.  Zooprophylaxis or zoopotentiation: the outcome of introducing animals on vector transmission is highly dependent on the mosquito mortality while searching , 2003, Malaria Journal.

[32]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[33]  S. Lindsay,et al.  Zooprophylaxis, artefact or reality? A paired-cohort study of the effect of passive zooprophylaxis on malaria in The Gambia. , 2002, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[34]  Oficina Técnica.  Enfermedad de Chagas , 2002 .

[35]  S. Lindsay,et al.  Effect of Passive Zooprophylaxis on Malaria Transmission in the Gambia , 2001, Journal of medical entomology.

[36]  R. Gürtler,et al.  Modeling Household Transmission of American Trypanosomiasis , 2001, Science.

[37]  S. Catalá,et al.  Feeding frequency and nutritional status of peridomestic populations of Triatoma infestans from Argentina. , 1999, Acta tropica.

[38]  J. Dujardin,et al.  The process of domestication in Triatominae. , 1999, Memorias do Instituto Oswaldo Cruz.

[39]  R. Gürtler,et al.  Effects of non-susceptible hosts on the infection with Trypanosoma cruzi of the vector Triatoma infestans: an experimental model. , 1999, Memorias do Instituto Oswaldo Cruz.

[40]  R. Chuit,et al.  Household prevalence of seropositivity for Trypanosoma cruzi in three rural villages in northwest Argentina: environmental, demographic, and entomologic associations. , 1998, The American journal of tropical medicine and hygiene.

[41]  R. Chuit,et al.  Influence of humans and domestic animals on the household prevalence of Trypanosoma cruzi in Triatoma infestans populations in northwest Argentina. , 1998, The American journal of tropical medicine and hygiene.

[42]  S. Catalá,et al.  Trypanosoma cruzi transmission risk index (TcTRI): an entomological indicator of Chagas disease vectorial transmission to humans. , 1997, Acta tropica.

[43]  R. Chuit,et al.  Effects of chickens on the prevalence of infestation and population density of Triatoma infestans in rural houses of north‐west Argentina , 1997, Medical and veterinary entomology.

[44]  R. Chuit,et al.  Shifting host choices of the vector of Chagas disease, Triatoma infestans, in relation to the availability of hosts in houses in north-west Argentina , 1997 .

[45]  D. Gorla,et al.  Vectorial transmission of Trypanosoma cruzi: an experimental field study with susceptible and immunized hosts. , 1992, The American journal of tropical medicine and hygiene.

[46]  A. J. Hall.  Infectious diseases of humans: R. M. Anderson & R. M. May. Oxford etc.: Oxford University Press, 1991. viii + 757 pp. Price £50. ISBN 0-19-854599-1 , 1992 .

[47]  S. Catalá.  The biting rate of Triatoma infestans in Argentina , 1991, Medical and veterinary entomology.

[48]  M. Lehane,et al.  The biology of blood-sucking in insects , 1991 .

[49]  D. Gorla,et al.  Seasonal changes in infectivity of domestic populations of Triatoma infestans. , 1990, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[50]  M. Mogi,et al.  Effectiveness of zooprophylaxis in malaria control: a theoretical inquiry, with a model for mosquito populations with two bloodmeal hosts , 1989, Medical and veterinary entomology.

[51]  J. Núñez,et al.  Blood temperature and feeding behavior in Triatoma infestans (Heteroptera: Reduviidae) , 1989 .

[52]  G. Schaub.  Does Trypanosoma cruzi stress its vectors? , 1989, Parasitology today.

[53]  K. Kloter,et al.  Manual on environmental management for mosquito control with special emphasis on malaria vectors. , 1983, WHO offset publication.

[54]  C. Tempelis,et al.  The biology and behavior of Triatoma barberi (Hemiptera: Reduviidae) in Mexico. II. Influence of a single versus a double feeding on the time that blood meal antigens remain serologically detectable. , 1981, Journal of medical entomology.

[55]  Edmundo Juarez.  Comportamento do Triatoma infestans sob várias condições de laboratório , 1970 .

[56]  S. Maddrell.  EXCRETION IN THE BLOOD-SUCKING BUG, RHODNIUS PROLIXUS STAL. II. THE NORMAL COURSE OF DIURESIS AND THE EFFECT OF TEMPERATURE. , 1964, The Journal of experimental biology.

[57]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[58]  O. M. D. L. Salud.  Control de la enfermedad de chagas , 2002 .

[59]  R. Chuit,et al.  Factors limiting the domestic density of Triatoma infestans in north-west Argentina: a longitudinal study. , 1998, Bulletin of the World Health Organization.

[60]  R. Chuit,et al.  Host-feeding patterns of domiciliary Triatoma infestans (Hemiptera: Reduviidae) in Northwest Argentina: seasonal and instar variation. , 1996, Journal of medical entomology.

[61]  R. Gürtler,et al.  Density estimates of the domestic vector of Chagas disease, Rhodnius prolixus Stål (Hemiptera: Reduviidae), in rural houses in Venezuela. , 1995, Bulletin of the World Health Organization.

[62]  José Milei,et al.  Enfermedad de Chagas , 1994 .

[63]  C. Dye.  The analysis of parasite transmission by bloodsucking insects. , 1992, Annual review of entomology.

[64]  G. Schaub,et al.  The effects of trypanosomatids on insects. , 1992, Advances in parasitology.

[65]  M. Service.  Agricultural development and arthropod-borne diseases: a review. , 1991, Revista de saude publica.

[66]  C. Wisnivesky-Colli,et al.  Probability of transmission of Chagas disease by Triatoma infestans (Hemiptera: Reduviidae) in an endemic area of Santiago del Estero, Argentina. , 1990, Bulletin of the World Health Organization.

[67]  C. P. Pant.  BLOODMEAL IDENTIFICATION IN VECTORS , 1987 .

[68]  S. Montenegro.  Consumo y utilizacion del alimento en adultos de triatoma infestans klug, 1834 (hemiptera, reduviidae) , 1984 .

[69]  C. Schofield.  Nutritional status of domestic populations of Triatoma infestans. , 1980, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[70]  J. Rabinovich,et al.  Domiciliary biting frequency and blood ingestion of the Chagas's disease vector Rhodnius prolixus Ståhl (Hemiptera: Reduviidae), in Venezuela. , 1979, Transactions of the Royal Society of Tropical Medicine and Hygiene.