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Modeling the impact of xenointoxication in dogs to halt Trypanosoma cruzi transmission

BACKGROUND: Chagas disease, a vector-borne parasitic disease caused by Trypanosoma cruzi, affects millions in the Americas. Dogs are important reservoirs of the parasite. Under laboratory conditions, canine treatment with the systemic insecticide fluralaner demonstrated efficacy in killing Triatoma...

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Autores principales: Rokhsar, Jennifer L., Raynor, Brinkley, Sheen, Justin, Goldstein, Neal D., Levy, Michael Z., Castillo-Neyra, Ricardo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10194993/
https://www.ncbi.nlm.nih.gov/pubmed/37155680
http://dx.doi.org/10.1371/journal.pcbi.1011115
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author Rokhsar, Jennifer L.
Raynor, Brinkley
Sheen, Justin
Goldstein, Neal D.
Levy, Michael Z.
Castillo-Neyra, Ricardo
author_facet Rokhsar, Jennifer L.
Raynor, Brinkley
Sheen, Justin
Goldstein, Neal D.
Levy, Michael Z.
Castillo-Neyra, Ricardo
author_sort Rokhsar, Jennifer L.
collection PubMed
description BACKGROUND: Chagas disease, a vector-borne parasitic disease caused by Trypanosoma cruzi, affects millions in the Americas. Dogs are important reservoirs of the parasite. Under laboratory conditions, canine treatment with the systemic insecticide fluralaner demonstrated efficacy in killing Triatoma infestans and T. brasiliensis, T. cruzi vectors, when they feed on dogs. This form of pest control is called xenointoxication. However, T. cruzi can also be transmitted orally when mammals ingest infected bugs, so there is potential for dogs to become infected upon consuming infected bugs killed by the treatment. Xenointoxication thereby has two contrasting effects on dogs: decreasing the number of insects feeding on the dogs but increasing opportunities for exposure to T. cruzi via oral transmission to dogs ingesting infected insects. OBJECTIVE: Examine the potential for increased infection rates of T. cruzi in dogs following xenointoxication. DESIGN/METHODS: We built a deterministic mathematical model, based on the Ross-MacDonald malaria model, to investigate the net effect of fluralaner treatment on the prevalence of T. cruzi infection in dogs in different epidemiologic scenarios. We drew upon published data on the change in percentage of bugs killed that fed on treated dogs over days post treatment. Parameters were adjusted to mimic three scenarios of T. cruzi transmission: high and low disease prevalence and domestic vectors, and low disease prevalence and sylvatic vectors. RESULTS: In regions with high endemic disease prevalence in dogs and domestic vectors, prevalence of infected dogs initially increases but subsequently declines before eventually rising back to the initial equilibrium following one fluralaner treatment. In regions of low prevalence and domestic or sylvatic vectors, however, treatment seems to be detrimental. In these regions our models suggest a potential for a rise in dog prevalence, due to oral transmission from dead infected bugs. CONCLUSION: Xenointoxication could be a beneficial and novel One Health intervention in regions with high prevalence of T. cruzi and domestic vectors. In regions with low prevalence and domestic or sylvatic vectors, there is potential harm. Field trials should be carefully designed to closely follow treated dogs and include early stopping rules if incidence among treated dogs exceeds that of controls.
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spelling pubmed-101949932023-05-19 Modeling the impact of xenointoxication in dogs to halt Trypanosoma cruzi transmission Rokhsar, Jennifer L. Raynor, Brinkley Sheen, Justin Goldstein, Neal D. Levy, Michael Z. Castillo-Neyra, Ricardo PLoS Comput Biol Research Article BACKGROUND: Chagas disease, a vector-borne parasitic disease caused by Trypanosoma cruzi, affects millions in the Americas. Dogs are important reservoirs of the parasite. Under laboratory conditions, canine treatment with the systemic insecticide fluralaner demonstrated efficacy in killing Triatoma infestans and T. brasiliensis, T. cruzi vectors, when they feed on dogs. This form of pest control is called xenointoxication. However, T. cruzi can also be transmitted orally when mammals ingest infected bugs, so there is potential for dogs to become infected upon consuming infected bugs killed by the treatment. Xenointoxication thereby has two contrasting effects on dogs: decreasing the number of insects feeding on the dogs but increasing opportunities for exposure to T. cruzi via oral transmission to dogs ingesting infected insects. OBJECTIVE: Examine the potential for increased infection rates of T. cruzi in dogs following xenointoxication. DESIGN/METHODS: We built a deterministic mathematical model, based on the Ross-MacDonald malaria model, to investigate the net effect of fluralaner treatment on the prevalence of T. cruzi infection in dogs in different epidemiologic scenarios. We drew upon published data on the change in percentage of bugs killed that fed on treated dogs over days post treatment. Parameters were adjusted to mimic three scenarios of T. cruzi transmission: high and low disease prevalence and domestic vectors, and low disease prevalence and sylvatic vectors. RESULTS: In regions with high endemic disease prevalence in dogs and domestic vectors, prevalence of infected dogs initially increases but subsequently declines before eventually rising back to the initial equilibrium following one fluralaner treatment. In regions of low prevalence and domestic or sylvatic vectors, however, treatment seems to be detrimental. In these regions our models suggest a potential for a rise in dog prevalence, due to oral transmission from dead infected bugs. CONCLUSION: Xenointoxication could be a beneficial and novel One Health intervention in regions with high prevalence of T. cruzi and domestic vectors. In regions with low prevalence and domestic or sylvatic vectors, there is potential harm. Field trials should be carefully designed to closely follow treated dogs and include early stopping rules if incidence among treated dogs exceeds that of controls. Public Library of Science 2023-05-08 /pmc/articles/PMC10194993/ /pubmed/37155680 http://dx.doi.org/10.1371/journal.pcbi.1011115 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Rokhsar, Jennifer L.
Raynor, Brinkley
Sheen, Justin
Goldstein, Neal D.
Levy, Michael Z.
Castillo-Neyra, Ricardo
Modeling the impact of xenointoxication in dogs to halt Trypanosoma cruzi transmission
title Modeling the impact of xenointoxication in dogs to halt Trypanosoma cruzi transmission
title_full Modeling the impact of xenointoxication in dogs to halt Trypanosoma cruzi transmission
title_fullStr Modeling the impact of xenointoxication in dogs to halt Trypanosoma cruzi transmission
title_full_unstemmed Modeling the impact of xenointoxication in dogs to halt Trypanosoma cruzi transmission
title_short Modeling the impact of xenointoxication in dogs to halt Trypanosoma cruzi transmission
title_sort modeling the impact of xenointoxication in dogs to halt trypanosoma cruzi transmission
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10194993/
https://www.ncbi.nlm.nih.gov/pubmed/37155680
http://dx.doi.org/10.1371/journal.pcbi.1011115
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