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Over-dispersed Trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern Argentina

BACKGROUND: The distribution of parasite load across hosts may modify the transmission dynamics of infectious diseases. Chagas disease is caused by a multi-host protozoan, Trypanosoma cruzi, but the association between host parasitemia and infectiousness to the vector has not been studied in sylvati...

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Autores principales: Enriquez, Gustavo Fabián, Bua, Jacqueline, Orozco, María Marcela, Macchiaverna, Natalia Paula, Otegui, Julián Antonio Alvarado, Argibay, Hernán Darío, Fernández, María del Pilar, Gürtler, Ricardo Esteban, Cardinal, Marta Victoria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8785451/
https://www.ncbi.nlm.nih.gov/pubmed/35073983
http://dx.doi.org/10.1186/s13071-022-05152-7
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author Enriquez, Gustavo Fabián
Bua, Jacqueline
Orozco, María Marcela
Macchiaverna, Natalia Paula
Otegui, Julián Antonio Alvarado
Argibay, Hernán Darío
Fernández, María del Pilar
Gürtler, Ricardo Esteban
Cardinal, Marta Victoria
author_facet Enriquez, Gustavo Fabián
Bua, Jacqueline
Orozco, María Marcela
Macchiaverna, Natalia Paula
Otegui, Julián Antonio Alvarado
Argibay, Hernán Darío
Fernández, María del Pilar
Gürtler, Ricardo Esteban
Cardinal, Marta Victoria
author_sort Enriquez, Gustavo Fabián
collection PubMed
description BACKGROUND: The distribution of parasite load across hosts may modify the transmission dynamics of infectious diseases. Chagas disease is caused by a multi-host protozoan, Trypanosoma cruzi, but the association between host parasitemia and infectiousness to the vector has not been studied in sylvatic mammalian hosts. We quantified T. cruzi parasite load in sylvatic mammals, modeled the association of the parasite load with infectiousness to the vector and compared these results with previous ones for local domestic hosts. METHODS: The bloodstream parasite load in each of 28 naturally infected sylvatic mammals from six species captured in northern Argentina was assessed by quantitative PCR, and its association with infectiousness to the triatomine Triatoma infestans was evaluated, as determined by natural or artificial xenodiagnosis. These results were compared with our previous results for 88 humans, 70 dogs and 13 cats, and the degree of parasite over-dispersion was quantified and non-linear models fitted to data on host infectiousness and bloodstream parasite load. RESULTS: The parasite loads of Didelphis albiventris (white-eared opossum) and Dasypus novemcinctus (nine-banded armadillo) were directly and significantly associated with infectiousness of the host and were up to 190-fold higher than those in domestic hosts. Parasite load was aggregated across host species, as measured by the negative binomial parameter, k, and found to be substantially higher in white-eared opossums, cats, dogs and nine-banded armadillos (range: k = 0.3–0.5) than in humans (k = 5.1). The distribution of bloodstream parasite load closely followed the “80–20 rule” in every host species examined. However, the 20% of human hosts, domestic mammals or sylvatic mammals exhibiting the highest parasite load accounted for 49, 25 and 33% of the infected triatomines, respectively. CONCLUSIONS: Our results support the use of bloodstream parasite load as a proxy of reservoir host competence and individual transmissibility. The over-dispersed distribution of T. cruzi bloodstream load implies the existence of a fraction of highly infectious hosts that could be targeted to improve vector-borne transmission control efforts toward interruption transmission. Combined strategies that decrease the parasitemia and/or host–vector contact with these hosts would disproportionally contribute to T. cruzi transmission control. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05152-7.
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spelling pubmed-87854512022-01-24 Over-dispersed Trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern Argentina Enriquez, Gustavo Fabián Bua, Jacqueline Orozco, María Marcela Macchiaverna, Natalia Paula Otegui, Julián Antonio Alvarado Argibay, Hernán Darío Fernández, María del Pilar Gürtler, Ricardo Esteban Cardinal, Marta Victoria Parasit Vectors Research BACKGROUND: The distribution of parasite load across hosts may modify the transmission dynamics of infectious diseases. Chagas disease is caused by a multi-host protozoan, Trypanosoma cruzi, but the association between host parasitemia and infectiousness to the vector has not been studied in sylvatic mammalian hosts. We quantified T. cruzi parasite load in sylvatic mammals, modeled the association of the parasite load with infectiousness to the vector and compared these results with previous ones for local domestic hosts. METHODS: The bloodstream parasite load in each of 28 naturally infected sylvatic mammals from six species captured in northern Argentina was assessed by quantitative PCR, and its association with infectiousness to the triatomine Triatoma infestans was evaluated, as determined by natural or artificial xenodiagnosis. These results were compared with our previous results for 88 humans, 70 dogs and 13 cats, and the degree of parasite over-dispersion was quantified and non-linear models fitted to data on host infectiousness and bloodstream parasite load. RESULTS: The parasite loads of Didelphis albiventris (white-eared opossum) and Dasypus novemcinctus (nine-banded armadillo) were directly and significantly associated with infectiousness of the host and were up to 190-fold higher than those in domestic hosts. Parasite load was aggregated across host species, as measured by the negative binomial parameter, k, and found to be substantially higher in white-eared opossums, cats, dogs and nine-banded armadillos (range: k = 0.3–0.5) than in humans (k = 5.1). The distribution of bloodstream parasite load closely followed the “80–20 rule” in every host species examined. However, the 20% of human hosts, domestic mammals or sylvatic mammals exhibiting the highest parasite load accounted for 49, 25 and 33% of the infected triatomines, respectively. CONCLUSIONS: Our results support the use of bloodstream parasite load as a proxy of reservoir host competence and individual transmissibility. The over-dispersed distribution of T. cruzi bloodstream load implies the existence of a fraction of highly infectious hosts that could be targeted to improve vector-borne transmission control efforts toward interruption transmission. Combined strategies that decrease the parasitemia and/or host–vector contact with these hosts would disproportionally contribute to T. cruzi transmission control. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05152-7. BioMed Central 2022-01-24 /pmc/articles/PMC8785451/ /pubmed/35073983 http://dx.doi.org/10.1186/s13071-022-05152-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Enriquez, Gustavo Fabián
Bua, Jacqueline
Orozco, María Marcela
Macchiaverna, Natalia Paula
Otegui, Julián Antonio Alvarado
Argibay, Hernán Darío
Fernández, María del Pilar
Gürtler, Ricardo Esteban
Cardinal, Marta Victoria
Over-dispersed Trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern Argentina
title Over-dispersed Trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern Argentina
title_full Over-dispersed Trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern Argentina
title_fullStr Over-dispersed Trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern Argentina
title_full_unstemmed Over-dispersed Trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern Argentina
title_short Over-dispersed Trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern Argentina
title_sort over-dispersed trypanosoma cruzi parasite load in sylvatic and domestic mammals and humans from northeastern argentina
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8785451/
https://www.ncbi.nlm.nih.gov/pubmed/35073983
http://dx.doi.org/10.1186/s13071-022-05152-7
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