Fluralaner systemic treatment of chickens results in mortality in <i>Triatoma gerstaeckeri</i>, vector of the agent of Chagas disease

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Abstract

Background

Chagas disease remains a persistent vector-borne neglected tropical disease throughout the Americas and threatens both human and animal health. Diverse control methods have been used to target triatomine vector populations, with household insecticides being the most common. As an alternative to environmental sprays, host-targeted systemic insecticides (or endectocides) allow for application of chemicals to vertebrate hosts, resulting in toxic blood meals for arthropods (xenointoxication). In this study, we evaluated three systemic insecticide products for their ability to kill triatomines.

Methods

Chickens were fed the insecticides orally, following which triatomines were allowed to feed on the treated chickens. The insecticide products tested included: Safe-Guard® Aquasol (fenbendazole), Ivomec® Pour-On (ivermectin) and Bravecto® (fluralaner). Triatoma gerstaeckeri nymphs were allowed to feed on insecticide-live birds at 0, 3, 7, 14, 28 and 56 days post-treatment. The survival and feeding status of the T. gerstaeckeri insects were recorded and analyzed using Kaplan–Meier curves and logistic regression.

Results

Feeding on fluralaner-treated chickens resulted 50–100% mortality in T. gerstaeckeri over the first 14 days post-treatment but not later; in contrast, all insects that fed on fenbendazole- and ivermectin-treated chickens survived. Liquid chromatography tandem mass spectrometry (LC-QQQ) analysis, used to detect the concentration of fluralaner and fenbendazole in chicken plasma, revealed the presence of fluralaner in plasma at 3, 7, and 14 days post-treatment but not later, with the highest concentrations found at 3 and 7 days post-treatment. However, fenbendazole concentration was below the limit of detection at all time points.

Conclusions

Xenointoxication using fluralaner in poultry is a potential new tool for integrated vector control to reduce risk of Chagas disease.

Graphical Abstract

Supplementary Information

The online version contains supplementary material available at 10.1186/s13071-023-05805-1.

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Most cited references 46

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Chagas Disease: From Discovery to a Worldwide Health Problem

Kárita Cláudia Freitas Lidani, Fabiana Antunes Andrade, Lorena Bavia … (2019)

Carlos Chagas discovered American trypanosomiasis, also named Chagas disease (CD) in his honor, just over a century ago. He described the clinical aspects of the disease, characterized by its etiological agent (Trypanosoma cruzi) and identified its insect vector. Initially, CD occurred only in Latin America and was considered a silent and poorly visible disease. More recently, CD became a neglected worldwide disease with a high morbimortality rate and substantial social impact, emerging as a significant public health threat. In this context, it is crucial to better understand better the epidemiological scenarios of CD and its transmission dynamics, involving people infected and at risk of infection, diversity of the parasite, vector species, and T. cruzi reservoirs. Although efforts have been made by endemic and non-endemic countries to control, treat, and interrupt disease transmission, the cure or complete eradication of CD are still topics of great concern and require global attention. Considering the current scenario of CD, also affecting non-endemic places such as Canada, USA, Europe, Australia, and Japan, in this review we aim to describe the spread of CD cases worldwide since its discovery until it has become a global public health concern.

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Ivermectin: enigmatic multifaceted ‘wonder’ drug continues to surprise and exceed expectations

Andy CRUMP (2017)

Over the past decade, the global scientific community have begun to recognize the unmatched value of an extraordinary drug, ivermectin, that originates from a single microbe unearthed from soil in Japan. Work on ivermectin has seen its discoverer, Satoshi Ōmura, of Tokyo's prestigious Kitasato Institute, receive the 2014 Gairdner Global Health Award and the 2015 Nobel Prize in Physiology or Medicine, which he shared with a collaborating partner in the discovery and development of the drug, William Campbell of Merck & Co. Incorporated. Today, ivermectin is continuing to surprise and excite scientists, offering more and more promise to help improve global public health by treating a diverse range of diseases, with its unexpected potential as an antibacterial, antiviral and anti-cancer agent being particularly extraordinary.

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Evolution, Systematics, and Biogeography of the Triatominae, Vectors of Chagas Disease.

Fernando Araujo Monteiro, Christiane Weirauch, Márcio Felix … (2018)

In this chapter, we review and update current knowledge about the evolution, systematics, and biogeography of the Triatominae (Hemiptera: Reduviidae)-true bugs that feed primarily on vertebrate blood. In the Americas, triatomines are the vectors of Trypanosoma cruzi, the etiological agent of Chagas disease. Despite declining incidence and prevalence, Chagas disease is still a major public health concern in Latin America. Triatomines occur also in the Old World, where vector-borne T. cruzi transmission has not been recorded. Triatomines evolved from predatory reduviid bugs, most likely in the New World, and diversified extensively across the Americas (including the Caribbean) and in parts of Asia and Oceania. Here, we first discuss our current understanding of how, how many times, and when the blood-feeding habit might have evolved among the Reduviidae. Then we present a summary of recent advances in the systematics of this diverse group of insects, with an emphasis on the contribution of molecular tools to the clarification of taxonomic controversies. Finally, and in the light of both up-to-date phylogenetic hypotheses and a thorough review of distribution records, we propose a global synthesis of the biogeography of the Triatominae. Over 130 triatomine species contribute to maintaining T. cruzi transmission among mammals (sometimes including humans) in almost every terrestrial ecoregion of the Americas. This means that Chagas disease will never be eradicated and underscores the fact that effective disease prevention will perforce require stronger, long-term vector control-surveillance systems.

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Author and article information

Contributors

Cassandra Durden: durdencj@tamu.edu

Yuexun Tian: yuexun.tian@ag.tamu.edu

Koyle Knape: chickenman97@tamu.edu

Cory Klemashevich: klem24@tamu.edu

Keri N. Norman: knorman@cvm.tamu.edu

John B. Carey: jcarey@poultry.tamu.edu

Sarah A. Hamer: shamer@cvm.tamu.edu

Gabriel L. Hamer: gabe.hamer@ag.tamu.edu

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 2 June 2023

Publication date PMC-release: 2 June 2023

Publication date Collection: 2023

Volume: 16

Electronic Location Identifier: 178

Affiliations

[1 ]GRID grid.264756.4, ISNI 0000 0004 4687 2082, Department of Veterinary Integrative Biosciences, , Texas A&M University, ; College Station, USA

[2 ]GRID grid.264756.4, ISNI 0000 0004 4687 2082, Schubot Center for Avian Health, Department of Veterinary Pathobiology, , Texas A&M University, ; College Station, USA

[3 ]GRID grid.264756.4, ISNI 0000 0004 4687 2082, Department of Entomology, , Texas A&M University, ; College Station, USA

[4 ]GRID grid.264756.4, ISNI 0000 0004 4687 2082, Department of Poultry Science, , Texas A&M University, ; College Station, USA

[5 ]GRID grid.264756.4, ISNI 0000 0004 4687 2082, Integrated Metabolomics Analysis Core, , Texas A&M University, ; College Station, USA

Article

Publisher ID: 5805

DOI: 10.1186/s13071-023-05805-1

PMC ID: 10236763

PubMed ID: 37268980

SO-VID: b9920887-a902-4f7c-8a98-517fc5525a8e

License:

Open Access This 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/. The Creative Commons Public Domain Dedication waiver ( http://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.

History

Date received : 9 February 2023

Date accepted : 10 May 2023

Funding

Funded by: Schubot Center for Avian Health, Texas A&M University

Funded by: FundRef http://dx.doi.org/10.13039/100005825, National Institute of Food and Agriculture;

Award ID: Animal Health and Disease Research Capacity Funding

Funded by: Texas A&M AgriLife Research

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ScienceOpen disciplines: Parasitology

Keywords: xenointoxication,endectocide,integrated vector control,triatomine,poultry

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ScienceOpen disciplines: Parasitology

Keywords: xenointoxication, endectocide, integrated vector control, triatomine, poultry

Fluralaner systemic treatment of chickens results in mortality in Triatoma gerstaeckeri, vector of the agent of Chagas disease

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Abstract

Background

Methods

Results

Conclusions

Graphical Abstract

Supplementary Information

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Vector Biology

Most cited references 46

Chagas Disease: From Discovery to a Worldwide Health Problem

Ivermectin: enigmatic multifaceted ‘wonder’ drug continues to surprise and exceed expectations

Evolution, Systematics, and Biogeography of the Triatominae, Vectors of Chagas Disease.

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