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Comparative analysis of the anthelmintic efficacy of European heather extracts on Teladorsagia circumcincta and Trichostrongylus colubriformis egg hatching and larval motility

BACKGROUND: Gastrointestinal nematode (GIN) control is traditionally achieved with the use of anthelmintic drugs, however due to regulations in organic farming and the rise in anthelmintic resistance, alternatives are sought after. A promising alternative is the use of bioactive plant feeding due to...

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Autores principales: Shepherd, Francesca, Chylinski, Caroline, Hutchings, Michael R., Lima, Joana, Davidson, Ross, Kelly, Robert, Macrae, Alastair, Salminen, Juha-Pekka, Engström, Marica T., Maurer, Veronika, Steinshamn, Håvard, Fittje, Susanne, Perez, Angela Morell, García, Rocío Rosa, Athanasiadou, Spiridoula
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9636748/
https://www.ncbi.nlm.nih.gov/pubmed/36333822
http://dx.doi.org/10.1186/s13071-022-05531-0
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author Shepherd, Francesca
Chylinski, Caroline
Hutchings, Michael R.
Lima, Joana
Davidson, Ross
Kelly, Robert
Macrae, Alastair
Salminen, Juha-Pekka
Engström, Marica T.
Maurer, Veronika
Steinshamn, Håvard
Fittje, Susanne
Perez, Angela Morell
García, Rocío Rosa
Athanasiadou, Spiridoula
author_facet Shepherd, Francesca
Chylinski, Caroline
Hutchings, Michael R.
Lima, Joana
Davidson, Ross
Kelly, Robert
Macrae, Alastair
Salminen, Juha-Pekka
Engström, Marica T.
Maurer, Veronika
Steinshamn, Håvard
Fittje, Susanne
Perez, Angela Morell
García, Rocío Rosa
Athanasiadou, Spiridoula
author_sort Shepherd, Francesca
collection PubMed
description BACKGROUND: Gastrointestinal nematode (GIN) control is traditionally achieved with the use of anthelmintic drugs, however due to regulations in organic farming and the rise in anthelmintic resistance, alternatives are sought after. A promising alternative is the use of bioactive plant feeding due to the presence of plant secondary metabolites (PSMs) such as proanthocyanidins (PAs). This study focussed on the perennial shrub heather (Ericaceae family), a plant rich in PAs, highly abundant across Europe and with previously demonstrated anthelmintic potential. METHODS: In vitro assays were used to investigate heather’s anthelmintic efficacy against egg hatching and larval motility. Heather samples were collected from five European countries across two seasons, and extracts were tested against two GIN species: Teladorsagia circumcincta and Trichostrongylus colubriformis. Polyphenol group-specific ultraperformance liquid chromatography-tandem mass spectrometry analysis was performed to identify relevant polyphenol subgroups present, including the PA concentration and size and ratio of the subunits. Partial least squares analysis was performed to associate efficacy with variation in PSM composition. RESULTS: Heather extracts reduced egg hatching of both GIN species in a dose-dependent manner by up to 100%, while three extracts at the highest concentration (10 mg/ml) reduced larval motility to levels that were not significantly different from dead larvae controls. PAs, particularly the procyanidin type, and flavonol derivatives were associated with anthelmintic activity, and the particular subgroup of polyphenols associated with the efficacy was dependent on the GIN species and life stage. CONCLUSIONS: Our results provide in vitro evidence that heather, a widely available plant often managed as a weed in grazing systems, has anthelmintic properties attributed to various groups of PSMs and could contribute to sustainable GIN control in ruminant production systems across Europe. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05531-0.
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spelling pubmed-96367482022-11-06 Comparative analysis of the anthelmintic efficacy of European heather extracts on Teladorsagia circumcincta and Trichostrongylus colubriformis egg hatching and larval motility Shepherd, Francesca Chylinski, Caroline Hutchings, Michael R. Lima, Joana Davidson, Ross Kelly, Robert Macrae, Alastair Salminen, Juha-Pekka Engström, Marica T. Maurer, Veronika Steinshamn, Håvard Fittje, Susanne Perez, Angela Morell García, Rocío Rosa Athanasiadou, Spiridoula Parasit Vectors Research BACKGROUND: Gastrointestinal nematode (GIN) control is traditionally achieved with the use of anthelmintic drugs, however due to regulations in organic farming and the rise in anthelmintic resistance, alternatives are sought after. A promising alternative is the use of bioactive plant feeding due to the presence of plant secondary metabolites (PSMs) such as proanthocyanidins (PAs). This study focussed on the perennial shrub heather (Ericaceae family), a plant rich in PAs, highly abundant across Europe and with previously demonstrated anthelmintic potential. METHODS: In vitro assays were used to investigate heather’s anthelmintic efficacy against egg hatching and larval motility. Heather samples were collected from five European countries across two seasons, and extracts were tested against two GIN species: Teladorsagia circumcincta and Trichostrongylus colubriformis. Polyphenol group-specific ultraperformance liquid chromatography-tandem mass spectrometry analysis was performed to identify relevant polyphenol subgroups present, including the PA concentration and size and ratio of the subunits. Partial least squares analysis was performed to associate efficacy with variation in PSM composition. RESULTS: Heather extracts reduced egg hatching of both GIN species in a dose-dependent manner by up to 100%, while three extracts at the highest concentration (10 mg/ml) reduced larval motility to levels that were not significantly different from dead larvae controls. PAs, particularly the procyanidin type, and flavonol derivatives were associated with anthelmintic activity, and the particular subgroup of polyphenols associated with the efficacy was dependent on the GIN species and life stage. CONCLUSIONS: Our results provide in vitro evidence that heather, a widely available plant often managed as a weed in grazing systems, has anthelmintic properties attributed to various groups of PSMs and could contribute to sustainable GIN control in ruminant production systems across Europe. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05531-0. BioMed Central 2022-11-04 /pmc/articles/PMC9636748/ /pubmed/36333822 http://dx.doi.org/10.1186/s13071-022-05531-0 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
Shepherd, Francesca
Chylinski, Caroline
Hutchings, Michael R.
Lima, Joana
Davidson, Ross
Kelly, Robert
Macrae, Alastair
Salminen, Juha-Pekka
Engström, Marica T.
Maurer, Veronika
Steinshamn, Håvard
Fittje, Susanne
Perez, Angela Morell
García, Rocío Rosa
Athanasiadou, Spiridoula
Comparative analysis of the anthelmintic efficacy of European heather extracts on Teladorsagia circumcincta and Trichostrongylus colubriformis egg hatching and larval motility
title Comparative analysis of the anthelmintic efficacy of European heather extracts on Teladorsagia circumcincta and Trichostrongylus colubriformis egg hatching and larval motility
title_full Comparative analysis of the anthelmintic efficacy of European heather extracts on Teladorsagia circumcincta and Trichostrongylus colubriformis egg hatching and larval motility
title_fullStr Comparative analysis of the anthelmintic efficacy of European heather extracts on Teladorsagia circumcincta and Trichostrongylus colubriformis egg hatching and larval motility
title_full_unstemmed Comparative analysis of the anthelmintic efficacy of European heather extracts on Teladorsagia circumcincta and Trichostrongylus colubriformis egg hatching and larval motility
title_short Comparative analysis of the anthelmintic efficacy of European heather extracts on Teladorsagia circumcincta and Trichostrongylus colubriformis egg hatching and larval motility
title_sort comparative analysis of the anthelmintic efficacy of european heather extracts on teladorsagia circumcincta and trichostrongylus colubriformis egg hatching and larval motility
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9636748/
https://www.ncbi.nlm.nih.gov/pubmed/36333822
http://dx.doi.org/10.1186/s13071-022-05531-0
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