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Home / Equine Research Bank / Int J Parasitol Drugs Drug Resist / Chicory (Cichorium intybus) reduces cyathostomin egg excreti...
International journal for parasitology. Drugs and drug resistance2024; 24; 100523; doi: 10.1016/j.ijpddr.2024.100523

Chicory (Cichorium intybus) reduces cyathostomin egg excretion and larval development in grazing horses.

Abstract: Cyathostomins are the most prevalent parasitic nematodes of grazing horses. They are responsible for colic and diarrhea in their hosts. After several decades of exposure to synthetic anthelmintics, they have evolved to become resistant to most compounds. In addition, the drug-associated environmental side-effects question their use in the field. Alternative control strategies, like bioactive forages, are needed to face these challenges. Among these, chicory (Cichorium intybus, Puna II cultivar (cv.)) is known to convey anthelmintic compounds and may control cyathostomins in grazing horses. To challenge this hypothesis, we measured fecal egg counts and the rate of larval development in 20 naturally infected young saddle horses (2-year-old) grazing either (i) a pasture sown with chicory (n = 10) or (ii) a mesophile grassland (n = 10) at the same stocking rate (2.4 livestock unit (LU)/ha). The grazing period lasted 45 days to prevent horse reinfection. Horses in the chicory group mostly grazed chicory (89% of the bites), while those of the control group grazed mainly grasses (73%). Cyathostomins egg excretion decreased in both groups throughout the experiment. Accounting for this trajectory, the fecal egg count reduction (FECR) measured in individuals grazing chicory relative to control individuals increased from 72.9% at day 16 to 85.5% at the end of the study. In addition, larval development in feces from horses grazed on chicory was reduced by more than 60% from d31 compared to control individuals. Using a metabarcoding approach, we also evidenced a significant decrease in cyathostomin species abundance in horses grazing chicory. Chicory extract enriched in sesquiterpenes lactones was tested on two cyathostomins isolates. The estimated IC50 was high (1 and 3.4 mg/ml) and varied according to the pyrantel sensitivity status of the worm isolate. We conclude that the grazing of chicory (cv. Puna II) by horses is a promising strategy for reducing cyathostomin egg excretion and larval development that may contribute to lower the reliance on synthetic anthelmintics. The underpinning modes of action remain to be explored further.
Copyright © 2024 The Authors. Published by Elsevier Ltd.. All rights reserved.
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Publication Date: 2024-02-09 PubMed ID: 38368671PubMed Central: PMC10884488DOI: 10.1016/j.ijpddr.2024.100523Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper investigates the role of chicory, a type of plant, in reducing the amount of Cyathostomin eggs excreted and their development in horses. The study demonstrates that horses grazing on chicory had less Cyathostomin eggs in their excreta and slowed larval growth compared to control horses.

Study Background

  • Cyathostomins are nematodes, commonly called roundworms, which infect grazing horses. These parasites are responsible for colic symptoms and diarrhoea in infected horses.
  • After years of exposure to synthetic anthelmintics (drugs designed to combat worms), the parasites have adapted and now resist these treatments.
  • The side effects of these drugs, including the harm to the environment, highlights the need for alternative strategies, one of which is the use of bioactive forages.

Experiment Procedure

  • Twenty 2-year-old saddle horses, naturally infected with Cyathostomins, were split into two groups. Ten horses were made to graze on a pasture sown with chicory while the other ten grazed on a regular mesophile grassland.
  • The impact of the chicory feed on the egg excretion and the larval development of Cyathostomins was observed over a period of 45 days.
  • Horses in the chicory group consumed primarily chicory (89% of bites), while the control group horses fed largely on grass (73%).

Results

  • Cyathostomins egg excretion decreased in both groups throughout the experiment, but the group fed on chicory had a significantly higher reduction rate, increasing from 72.9% at day 16 to 85.5% at the end of the study.
  • The development of larvae in the feces of horses fed on chicory also decreased by more than 60% compared to the control group from the 31st day of the experiment.
  • A metabarcoding procedure showed a significant decrease in Cyathostomin species abundance in horses that grazed on chicory.

Conclusion

  • The study suggests that having horses graze on chicory could be an effective strategy in reducing Cyathostomin egg excretion and slowing larval development, ultimately helping to decrease reliance on synthetic anthelmintics.
  • While the exact mechanism of how chicory achieves this result is not yet clear and further studies are required to understand it in detail.

Cite This Article

APA
Malsa J, Boudesocque-Delaye L, Wimel L, Auclair-Ronzaud J, Dumont B, Mach N, Reigner F, Guégnard F, Chereau A, Serreau D, Théry-Koné I, Sallé G, Fleurance G. (2024). Chicory (Cichorium intybus) reduces cyathostomin egg excretion and larval development in grazing horses. Int J Parasitol Drugs Drug Resist, 24, 100523. https://doi.org/10.1016/j.ijpddr.2024.100523

Publication

International journal for parasitology. Drugs and drug resistance
ISSN: 2211-3207
NlmUniqueID: 101576715
Country: Netherlands
Language: English
Volume: 24
Pages: 100523

Researcher Affiliations

Malsa, Joshua
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, Nouzilly, France. Electronic address: joshua.malsa@inrae.fr.
Boudesocque-Delaye, Leslie
  • Université de Tours, EA 7502 Synthèse et Isolement de Molécules Bioactives, Tours, France.
Wimel, Laurence
  • Institut Français Du Cheval et de L'équitation, Plateau Technique de Chamberet, Chamberet, France.
Auclair-Ronzaud, Juliette
  • Institut Français Du Cheval et de L'équitation, Plateau Technique de Chamberet, Chamberet, France.
Dumont, Bertrand
  • INRAE, Université Clermont Auvergne, VetAgro Sup, UMR 1213 Herbivores, Saint-Genès-Champanelle, France.
Mach, Núria
  • IHAP, Université de Toulouse, INRAE, ENVT, Toulouse, Cedex 3, 31076, France.
Reigner, Fabrice
  • INRAE, Unité Expérimentale de Physiologie Animale de L'Orfrasière, Nouzilly, France.
Guégnard, Fabrice
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, Nouzilly, France.
Chereau, Angélique
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, Nouzilly, France.
Serreau, Delphine
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, Nouzilly, France.
Théry-Koné, Isabelle
  • Université de Tours, EA 7502 Synthèse et Isolement de Molécules Bioactives, Tours, France.
Sallé, Guillaume
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, Nouzilly, France.
Fleurance, Géraldine
  • INRAE, Université Clermont Auvergne, VetAgro Sup, UMR 1213 Herbivores, Saint-Genès-Champanelle, France; Institut Français Du Cheval et de L'équitation, Pôle Développement, Innovation et Recherche, Saint-Genès-Champanelle, France.

MeSH Terms

  • Animals
  • Horses
  • Cichorium intybus
  • Anthelmintics / therapeutic use
  • Feces / parasitology
  • Parasite Egg Count / veterinary

Conflict of Interest Statement

Declaration of competing interest The authors declare no conflict of interest.

References

This article includes 69 references
  1. Athanasiadou S, Tzamaloukas O, Kyriazakis I, Jackson F, Coop R.L. Testing for direct anthelmintic effects of bioactive forages against Trichostrongylus colubriformis in grazing sheep. Vet. Parasitol. 2005;127:233–243.
    pubmed: 15710524
  2. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48.
  3. Boisseau M, Dhorne-Pollet S, Bars-Cortina D, Courtot É, Serreau D, Annonay G, Lluch J, Gesbert A, Reigner F, Sallé G, Mach N. Species interactions, stability, and resilience of the gut microbiota - helminth assemblage in horses. iScience 2023;26.
    pmc: PMC9929684pubmed: 36818309
  4. Callahan B.J, McMurdie P.J, Rosen M.J, Han A.W, Johnson A.J.A, Holmes S.P. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 2016;13:581–583.
    pmc: PMC4927377pubmed: 27214047
  5. Collas C, Sallé G, Dumont B, Cabaret J, Cortet J, Martin-Rosset W, Wimel L, Fleurance G. Are sainfoin or protein supplements alternatives to control small strongyle infection in horses?. Anim. Int. J. Anim. Biosci. 2018;12:359–365.
    pubmed: 28535838
  6. Cortés A, Rooney J, Bartley D.J, Nisbet A.J, Cantacessi C. Helminths, hosts, and their microbiota: new avenues for managing gastrointestinal helminthiases in ruminants. Expert Rev. Anti Infect. Ther. 2020;18:977–985.
    pubmed: 32530331
  7. Courtot É, Boisseau M, Dhorne-Pollet S, Serreau D, Gesbert A, Reigner F, Basiaga M, Kuzmina T, Lluch J, Annonay G, Kuchly C, Diekmann I, Krücken J, Samson-Himmelstjerna G. von, Mach N, Sallé G. Comparison of two molecular barcodes for the study of equine strongylid communities with amplicon sequencing. PeerJ 2023;11.
    pmc: PMC10105562pubmed: 37070089
  8. da Silva G.D, de Lima H.G, de Sousa N.B, de Jesus Genipapeiro I.L, Uzêda R.S, Branco A, Costa S.L, Batatinha M.J.M, Botura M.B. In vitro anthelmintic evaluation of three alkaloids against gastrointestinal nematodes of goats. Vet. Parasitol. 2021;296.
    pubmed: 34218173
  9. Dubois O, Allanic C, Charvet C.L, Guégnard F, Février H, Théry-Koné I, Cortet J, Koch C, Bouvier F, Fassier T, Marcon D, Magnin-Robert J.B, Peineau N, Courtot E, Huau C, Meynadier A, Enguehard-Gueiffier C, Neveu C, Boudesocque-Delaye L, Sallé G. Lupin (Lupinus spp.) seeds exert anthelmintic activity associated with their alkaloid content. Sci. Rep. 2019;9:9070.
    pmc: PMC6588613pubmed: 31227784
  10. Ferioli F, D'Antuono L.F. An update procedure for an effective and simultaneous extraction of sesquiterpene lactones and phenolics from chicory. Food Chem. 2012;135:243–250.
  11. Foster J.G, Cassida K.A, Sanderson M.A. Seasonal variation in sesquiterpene lactone concentration and composition of forage chicory (Cichorium intybus L.) cultivars. Grass Forage Sci. 2011;66:424–433.
  12. Foster J.G, Clapham W.M, Belesky D.P, Labreveux M, Hall M.H, Sanderson M.A. Influence of Cultivation site on sesquiterpene lactone composition of forage chicory (cichorium intybus L.). J. Agric. Food Chem. 2006;54:1772–1778.
    pubmed: 16506832
  13. Gasser R.B, Chilton N.B, Hoste H, Beveridge I. Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res. 1993;21:2525–2526.
    pmc: PMC309567pubmed: 8506152
  14. Gaudin E, Simon M, Quijada J, Schelcher F, Sutra J.-F, Lespine A, Hoste H. Efficacy of sainfoin (Onobrychis viciifolia) pellets against multi resistant Haemonchus contortus and interaction with oral ivermectin: implications for on-farm control. Vet. Parasitol. 2016;227:122–129.
    pubmed: 27523948
  15. Giles C.J, Urquhart K.A, Longstaffe J.A. Larval cyathostomiasis (immature trichonema-induced enteropathy): a report of 15 clinical cases. Equine Vet. J. 1985;17:196–201.
    pubmed: 4076127
  16. Hayes K.S, Bancroft A.J, Goldrick M, Portsmouth C, Roberts I.S, Grencis R.K. Exploitation of the intestinal microflora by the parasitic nematode trichuris muris. Science 2010;328:1391–1394.
    pmc: PMC3428897pubmed: 20538949
  17. Heckendorn F, Häring D.A, Maurer V, Senn M, Hertzberg H. Individual administration of three tanniferous forage plants to lambs artificially infected with Haemonchus contortus and Cooperia curticei. Vet. Parasitol. 2007;146:123–134.
    pubmed: 17336459
  18. Heckendorn F, Häring D.A, Maurer V, Zinsstag J, Langhans W, Hertzberg H. Effect of sainfoin (Onobrychis viciifolia) silage and hay on established populations of Haemonchus contortus and Cooperia curticei in lambs. Vet. Parasitol. 2006;142:293–300.
    pubmed: 16934938
  19. Jung S, Rickert D.A, Deak N.A, Aldin E.D, Recknor J, Johnson L.A, Murphy P.A. Comparison of kjeldahl and dumas methods for determining protein contents of soybean products. J. Am. Oil Chem. Soc. 2003;80:1169–1173.
  20. Kaplan R.M. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol. 2004;20:477–481.
    pubmed: 15363441
  21. Kaplan R.M. Anthelmintic resistance in nematodes of horses. Vet. Res. 2002;33:491–507.
    pubmed: 12387486
  22. Kaplan R.M, Denwood M.J, Nielsen M.K, Thamsborg S.M, Torgerson P.R, Gilleard J.S, Dobson R.J, Vercruysse J, Levecke B. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) guideline for diagnosing anthelmintic resistance using the faecal egg count reduction test in ruminants, horses and swine. Vet. Parasitol. 2023;318.
    pubmed: 37121092
  23. Love S, Duncan J.L. The development of naturally acquired cyathostome infection in ponies. Vet. Parasitol. 1992;44:127–142.
    pubmed: 1441184
  24. Love S, Murphy D, Mellor D. Pathogenicity of cyathostome infection. Vet. Parasitol. 1999;85:113–121. discussion 121-122, 215–225.
    pubmed: 10485358
  25. Lumaret J.-P, Errouissi F, Floate K, Römbke J, Wardhaugh K. A review on the toxicity and non-target effects of macrocyclic lactones in terrestrial and aquatic environments. Curr. Pharm. Biotechnol. 2012;13:1004–1060.
    pmc: PMC3409360pubmed: 22039795
  26. Mach N, Midoux C, Leclercq S, Pennarun S, Le Moyec L, Rué O, Robert C, Sallé G, Barrey E. Mining the equine gut metagenome: poorly-characterized taxa associated with cardiovascular fitness in endurance athletes. Commun. Biol. 2022;5:1032.
    pmc: PMC9529974pubmed: 36192523
  27. Malsa J, Courtot É, Boisseau M, Dumont B, Gombault P, Kuzmina T.A, Basiaga M, Lluch J, Annonay G, Dhorne-Pollet S, Mach N, Sutra J.-F, Wimel L, Dubois C, Guégnard F, Serreau D, Lespine A, Sallé G, Fleurance G. Effect of sainfoin (Onobrychis viciifolia) on cyathostomin eggs excretion, larval development, larval community structure and efficacy of ivermectin treatment in horses. Parasitology 2022;149:1439–1449.
    pmc: PMC10090777pubmed: 35929352
  28. Manolaraki F, Sotiraki S, Stefanakis A, Skampardonis V, Volanis M, Hoste H. Anthelmintic activity of some Mediterranean browse plants against parasitic nematodes. Parasitology 2010;137:685–696.
    pubmed: 19961649
  29. Marley C.L, Cook R, Keatinge R, Barrett J, Lampkin N.H. The effect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally infected with helminth parasites. Vet. Parasitol. 2003;112:147–155.
    pubmed: 12581592
  30. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. Eur. Mol. Biol. Netw. 2011;17:10–12.
  31. Matthews J.B. Anthelmintic resistance in equine nematodes; pp. 310–315. Int. J. Parasitol. Drugs Drug Resist., Includes Articles from Two Meetings: “Anthelmintics: from Discovery to Resistance”, Pp. 218--315, and “Global Challenges for New Drug Discovery against Tropical Parasitic Diseases” 2014. 316--357 4.
  32. McMurdie P.J, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013;8.
    pmc: PMC3632530pubmed: 23630581
  33. Mésochina P, Martin-Rosset W, Peyraud J.-L, Duncan P, Micol D, Boulot S. Prediction of the digestibility of the diet of horses: evaluation of faecal indices. Grass Forage Sci. 1998;53:189–196.
  34. Mitchell C.J, O'Sullivan C.M, Pinloche E, Wilkinson T, Morphew R.M, McEwan N.R. Using next-generation sequencing to determine diversity of horse intestinal worms: identifying the equine “nemabiome.”. J. Equine Sci. 2019;30:1–5.
    pmc: PMC6445754pubmed: 30944540
  35. Mohamed T.A, Hegazy M.-E.F, Abd El Aty A.A, Ghabbour H.A, Alsaid M.S, Shahat A.A, Paré P.W. Antimicrobial sesquiterpene lactones from Artemisia sieberi. J. Asian Nat. Prod. Res. 2017;19:1093–1101.
    pubmed: 28361549
  36. Nielsen M.K. Anthelmintic resistance in equine nematodes: current status and emerging trends. Int. J. Parasitol. Drugs Drug Resist. 2022;20:76–88.
    pmc: PMC9630620pubmed: 36342004
  37. Niezen J.H, Waghorn T.S, Raufaut K, Robertson H.A, McFarlane R.G. Lamb weight gain and faecal egg count when grazing one of seven herbages and dosed with larvae for six weeks. Proc. N. Z. Soc. Anim. Prod. 1994;54:15–18.
  38. Oksanen J, Blanchet F.G, Kindt R, Legendre P, Minchin P, O'Hara B, Simpson G, Solymos P, Stevens H, Wagner H. Vegan: community ecology package. R Package Version 2015;22–1(2):1–2.
  39. Paolini V, De La Farge F, Prevot F, Dorchies P, Hoste H. Effects of the repeated distribution of sainfoin hay on the resistance and the resilience of goats naturally infected with gastrointestinal nematodes. Vet. Parasitol. 2005;127:277–283.
    pubmed: 15710528
  40. Paolini V, Dorchies P, Hoste H. Effects of sainfoin hay on gastrointestinal nematode infections in goats. Vet. Rec. 2003;152:600–601.
    pubmed: 12762491
  41. Paolini V, Fouraste I, Hoste H. In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology 2004;129:69–77.
    pubmed: 15267113
  42. Peña-Espinoza M, Boas U, Williams A.R, Thamsborg S.M, Simonsen H.T, Enemark H.L. Sesquiterpene lactone containing extracts from two cultivars of forage chicory (Cichorium intybus) show distinctive chemical profiles and in vitro activity against Ostertagia ostertagi. Int. J. Parasitol. Drugs Drug Resist. 2015;5:191–200.
    pmc: PMC4847107pubmed: 27120066
  43. Peña-Espinoza M, Thamsborg S.M, Desrues O, Hansen T.V.A, Enemark H.L. Anthelmintic effects of forage chicory (Cichorium intybus) against gastrointestinal nematode parasites in experimentally infected cattle. Parasitology 2016;143:1279–1293.
    pmc: PMC4988272pubmed: 27173405
  44. Peña-Espinoza M, Valente A.H, Thamsborg S.M, Simonsen H.T, Boas U, Enemark H.L, López-Muñoz R, Williams A.R. Antiparasitic activity of chicory (Cichorium intybus) and its natural bioactive compounds in livestock: a review. Parasites Vectors 2018;11:475.
    pmc: PMC6106872pubmed: 30134991
  45. Peña-Espinoza M, Williams A.R, Thamsborg S.M, Simonsen H.T, Enemark H.L. Anthelmintic effects of forage chicory (Cichorium intybus) against free-living and parasitic stages of Cooperia oncophora. Vet. Parasitol. 2017;243:204–207.
    pubmed: 28807295
  46. Penning P. Animal-based techniques for estimating herbage intake. Herb. Intake Handb. 2004:53–93.
  47. Peregrine A.S, Molento M.B, Kaplan R.M, Nielsen M.K. Anthelmintic resistance in important parasites of horses: does it really matter?. Vet. Parasitol. 2014;201:1–8.
    pubmed: 24485565
  48. Poissant J, Gavriliuc S, Bellaw J, Redman E.M, Avramenko R.W, Robinson D, Workentine M.L, Shury T.K, Jenkins E.J, McLoughlin P.D, Nielsen M.K, Gilleard J.S. A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses. Int. J. Parasitol. 2021;51:183–192.
    pubmed: 33242465
  49. R Core Team. R: A Language and Environment for Statistical Computing. 2023.
  50. Raynaud J.-P, William G, Brunault G. Etude de l’efficacité d’une technique de coproscopie quantitative pour le diagnostic de routine et le contrôle des infestations parasitaires des bovins, ovins, équins et porcins. Ann. Parasitol. Hum. Comp. 1970;45:321–342.
    pubmed: 5531507
  51. Reinemeyer C.R, Smith S.A, Gabel A.A, Herd R.P. The prevalence and intensity of internal parasites of horses in the. U.S.A.. Vet. Parasitol. 1984;15:75–83.
    pubmed: 6237483
  52. Reynolds L.A, Smith K.A, Filbey K.J, Harcus Y, Hewitson J.P, Redpath S.A, Valdez Y, Yebra M.J, Finlay B.B, Maizels R.M. Commensal-pathogen interactions in the intestinal tract. Gut Microb. 2014;5:522–532.
    pmc: PMC4822684pubmed: 25144609
  53. Reza M.M, Redoy M.R.A, Rahman M.A, Ety S, Alim M.A, Cheng L, Al-Mamun M. Response of plantain (Plantago lanceolata L.) supplementation on nutritional, endo-parasitic, and endocrine status in lambs. Trop. Anim. Health Prod. 2021;53:82.
    pubmed: 33411066
  54. Ritz C, Baty F, Streibig J.C, Gerhard D. Dose-response analysis using R. PLoS One 2015;10.
    pmc: PMC4696819pubmed: 26717316
  55. Rumball W. Grasslands Puna’ chicory (cichorium intybus L.). N. Z. J. Exp. Agric. 1986;14:105–107.
  56. Rynkiewicz E.C, Pedersen A.B, Fenton A. An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends Parasitol. 2015;31:212–221.
    pubmed: 25814004
  57. Santos F.O, Cerqueira A.P.M, Branco A, Batatinha M.J.M, Botura M.B. Anthelmintic activity of plants against gastrointestinal nematodes of goats: a review. Parasitology 2019;146:1233–1246.
    pubmed: 31104640
  58. Scales G.H, Knight T.L, Saville D.J. Effect of herbage species and feeding level on internal parasites and production performance of grazing lambs. N. Z. J. Agric. Res. 1995;38:237–247.
  59. Street R.A, Sidana J, Prinsloo G. Cichorium intybus: traditional uses, phytochemistry, pharmacology, and toxicology. Evid. Based complement. Alternat. Med. 2013;2013.
    pmc: PMC3860133pubmed: 24379887
  60. Tombak K.J, Hansen C.B, Kinsella J.M, Pansu J, Pringle R.M, Rubenstein D.I. The gastrointestinal nematodes of plains and Grevy's zebras: phylogenetic relationships and host specificity. Int. J. Parasitol. Parasites Wildl. 2021;16:228–235.
    pmc: PMC8529100pubmed: 34712556
  61. Traversa D, Castagna G, von Samson-Himmelstjerna G, Meloni S, Bartolini R, Geurden T, Pearce M.C, Woringer E, Besognet B, Milillo P, D'Espois M. Efficacy of major anthelmintics against horse cyathostomins in France. Vet. Parasitol. 2012;188:294–300.
    pubmed: 22538094
  62. Tzamaloukas O, Athanasiadou S, Kyriazakis I, Jackson F, Coop R.L. The consequences of short-term grazing of bioactive forages on established adult and incoming larvae populations of Teladorsagia circumcincta in lambs. Int. J. Parasitol. 2005;35:329–335.
    pubmed: 15722084
  63. Valente A.H, de Roode M, Ernst M, Peña-Espinoza M, Bornancin L, Bonde C.S, Martínez-Valladares M, Ramünke S, Krücken J, Simonsen H.T, Thamsborg S.M, Williams A.R. Identification of compounds responsible for the anthelmintic effects of chicory (Cichorium intybus) by molecular networking and bio-guided fractionation. Int. J. Parasitol. Drugs Drug Resist. 2021;15:105–114.
    pmc: PMC7907819pubmed: 33618233
  64. Van Soest P.J, Robertson J.B, Lewis B.A. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 1991;74:3583–3597.
    pubmed: 1660498
  65. Vercruysse J, Dorny P, Hong C, Harris T.J, Hammet N.C, Smith D.G, Weatherley A.J. Efficacy of doramectin in the prevention of gastrointestinal nematode infections in grazing cattle. Vet. Parasitol., Special Issue: Doramectin - a novel avermectin 1993;49:51–59.
    pubmed: 8236739
  66. Verdú J.R, Lobo J.M, Sánchez-Piñero F, Gallego B, Numa C, Lumaret J.-P, Cortez V, Ortiz A.J, Tonelli M, García-Teba J.P, Rey A, Rodríguez A, Durán J. Ivermectin residues disrupt dung beetle diversity, soil properties and ecosystem functioning: an interdisciplinary field study. Sci. Total Environ. 2018;618:219–228.
    pubmed: 29128770
  67. Wang C, Paul M, Isler T, Furrer R. eggCounts: Hierarchical Modelling of Faecal Egg Counts. 2022.
  68. Williams A.R, Andersen-Civil A.I.S, Zhu L, Blanchard A. Dietary phytonutrients and animal health: regulation of immune function during gastrointestinal infections. J. Anim. Sci. 2020;98 skaa030.
    pmc: PMC7105063pubmed: 31999321
  69. Williams A.R, Peña-Espinoza M.A, Boas U, Simonsen H.T, Enemark H.L, Thamsborg S.M. Anthelmintic activity of chicory (Cichorium intybus): in vitro effects on swine nematodes and relationship to sesquiterpene lactone composition. Parasitology 2016;143:770–777.
    pubmed: 26935644
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