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Scientific reports2021; 11(1); 14278; doi: 10.1038/s41598-021-93468-2

Integrative biology defines novel biomarkers of resistance to strongylid infection in horses.

Abstract: The widespread failure of anthelmintic drugs against nematodes of veterinary interest requires novel control strategies. Selective treatment of the most susceptible individuals could reduce drug selection pressure but requires appropriate biomarkers of the intrinsic susceptibility potential. To date, this has been missing in livestock species. Here, we selected Welsh ponies with divergent intrinsic susceptibility (measured by their egg excretion levels) to cyathostomin infection and found that their divergence was sustained across a 10-year time window. Using this unique set of individuals, we monitored variations in their blood cell populations, plasma metabolites and faecal microbiota over a grazing season to isolate core differences between their respective responses under worm-free or natural infection conditions. Our analyses identified the concomitant rise in plasma phenylalanine level and faecal Prevotella abundance and the reduction in circulating monocyte counts as biomarkers of the need for drug treatment (egg excretion above 200 eggs/g). This biological signal was replicated in other independent populations. We also unravelled an immunometabolic network encompassing plasma beta-hydroxybutyrate level, short-chain fatty acid producing bacteria and circulating neutrophils that forms the discriminant baseline between susceptible and resistant individuals. Altogether our observations open new perspectives on the susceptibility of equids to strongylid infection and leave scope for both new biomarkers of infection and nutritional intervention.
© 2021. The Author(s).
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Publication Date: 2021-07-12 PubMed ID: 34253752PubMed Central: PMC8275762DOI: 10.1038/s41598-021-93468-2Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

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 study investigates new biological markers, specific changes in blood cells, plasma metabolite levels, and fecal microbiota, that could potentially predict horses’ resistance or susceptibility to a type of worm infection. These findings offer new insights and suggest potential novel interventions for managing worm infection in horses.

Introduction and Objectives

  • This research aims to find biomarkers that indicate innate susceptibility to strongylid worm infections in horses. These worms are a common and significant health issue in horses, and a growing resistance to commonly applied treatments has triggered the need for new intervention strategies.
  • The key objective is to reduce the use of anthelmintic drugs, which currently play a key role in managing these infections, but widespread usage has led to drug resistance amongst worms.

Methodology

  • The researchers selectively isolated Welsh ponies with evident differences in susceptibility to cyathostomin infection, determined by their egg excretion levels and monitored over a 10-year period.
  • The variations between these selected horses, in terms of blood cell populations, plasma metabolites, and faecal microbiota, were monitored over a grazing season. The aim was to observe core differences in response when exposed to worm-free or naturally infected conditions.

Key Findings

  • The study identified three key indicators for the need for drug treatment in horses: a simultaneous increase in plasma phenylalanine level and faecal Prevotella abundance, and a decrease in circulating monocyte counts. These findings were apparent when egg excretion reached above 200 eggs/g, suggesting that these markers significantly correlate with the severity of infection.
  • The scientists discovered an immunometabolic network connecting plasma beta-hydroxybutyrate level, short-chain fatty acid producing bacteria and circulating neutrophils. This network was found to strongly discriminate between susceptible and resistant individuals.

Implications and Future Directions

  • The findings add a new dimension to knowledge on equine susceptibility to strongylid infection. Simultaneously, they provide potential new biomarkers to monitor and manage infection levels and explore the potential of nutritional interventions.
  • The scope of these findings implies that understanding the host’s responses and identifying biomarkers can lead to more targeted treatments, promoting animal health and reducing the imposition or overuse of anthelmintic drugs, thus combating drug resistance issues in nematodes.

Cite This Article

APA
Sallé G, Canlet C, Cortet J, Koch C, Malsa J, Reigner F, Riou M, Perrot N, Blanchard A, Mach N. (2021). Integrative biology defines novel biomarkers of resistance to strongylid infection in horses. Sci Rep, 11(1), 14278. https://doi.org/10.1038/s41598-021-93468-2

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 11
Issue: 1
Pages: 14278
PII: 14278

Researcher Affiliations

Sallé, Guillaume
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, 37380, Nouzilly, France. Guillaume.Salle@inrae.fr.
Canlet, Cécile
  • INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, UMR 1331 Toxalim, 31027, Toulouse, France.
Cortet, Jacques
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, 37380, Nouzilly, France.
Koch, Christine
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, 37380, Nouzilly, France.
Malsa, Joshua
  • INRAE, Université de Tours, UMR 1282 Infectiologie et Santé Publique, 37380, Nouzilly, France.
Reigner, Fabrice
  • INRAE, UE 1297 Physiologie Animale de l'Orfrasière, 37380, Nouzilly, France.
Riou, Mickaël
  • INRAE, UE 1277 Plateforme d'Infectiologie Expérimentale, 37380, Nouzilly, France.
Perrot, Noémie
  • INRAE, UE 1277 Plateforme d'Infectiologie Expérimentale, 37380, Nouzilly, France.
Blanchard, Alexandra
  • Pancosma, Rolle, Switzerland.
Mach, Núria
  • INRAE, Université Paris-Saclay, AgroParisTech, Génétique Animale et Biologie Intégrative, 78350, Jouy-en-Josas, France.

MeSH Terms

  • 3-Hydroxybutyric Acid / blood
  • Animals
  • Anthelmintics / therapeutic use
  • Biology / methods
  • Biomarkers / metabolism
  • Discriminant Analysis
  • Feces
  • Horse Diseases / parasitology
  • Horses
  • Magnetic Resonance Spectroscopy
  • Metabolomics
  • Nematoda
  • Parasite Egg Count / veterinary
  • Phenylalanine / blood
  • Seasons

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 83 references
  1. . Global, regional, and national disability-adjusted life-years (DALYs) for 333 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016.. Lancet 2017 Sep 16;390(10100):1260-1344.
    doi: 10.1016/S0140-6736(17)32130-Xpmc: PMC5605707pubmed: 28919118google scholar: lookup
  2. Nieuwhof GJ, Bishop SC. Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact.. Anim. Sci. 2005;81:23–29.
    doi: 10.1079/ASC41010023google scholar: lookup
  3. Kaplan RM, Vidyashankar AN. An inconvenient truth: global worming and anthelmintic resistance.. Vet Parasitol 2012 May 4;186(1-2):70-8.
    doi: 10.1016/j.vetpar.2011.11.048pubmed: 22154968google scholar: lookup
  4. Lyons E. Population-S benzimidazole- and tetrahydropyrimidine-resistant small strongyles in a pony herd in Kentucky (1977-1999): effects of anthelmintic treatment on the parasites as determined in critical tests.. Parasitol Res 2003 Nov;91(5):407-11.
    doi: 10.1007/s00436-003-0983-6pubmed: 14530968google scholar: lookup
  5. Näreaho A, Vainio K, Oksanen A. Impaired efficacy of ivermectin against Parascaris equorum, and both ivermectin and pyrantel against strongyle infections in trotter foals in Finland.. Vet Parasitol 2011 Dec 15;182(2-4):372-7.
    doi: 10.1016/j.vetpar.2011.05.045pubmed: 21689886google scholar: lookup
  6. Nielsen MK, Branan MA, Wiedenheft AM, Digianantonio R, Scare JA, Bellaw JL, Garber LP, Kopral CA, Phillippi-Taylor AM, Traub-Dargatz JL. Anthelmintic efficacy against equine strongyles in the United States.. Vet Parasitol 2018 Aug 15;259:53-60.
    doi: 10.1016/j.vetpar.2018.07.003pubmed: 30056984google scholar: lookup
  7. Sallé G, Cortet J, Bois I, Dubès C, Guyot-Sionest Q, Larrieu C, Landrin V, Majorel G, Wittreck S, Woringer E, Couroucé A, Guillot J, Jacquiet P, Guégnard F, Blanchard A, Leblond A. Risk factor analysis of equine strongyle resistance to anthelmintics.. Int J Parasitol Drugs Drug Resist 2017 Dec;7(3):407-415.
    doi: 10.1016/j.ijpddr.2017.10.007pmc: PMC5727347pubmed: 29149701google scholar: lookup
  8. Tzelos T, Barbeito JS, Nielsen MK, Morgan ER, Hodgkinson JE, Matthews JB. Strongyle egg reappearance period after moxidectin treatment and its relationship with management factors in UK equine populations.. Vet Parasitol 2017 Apr 15;237:70-76.
    doi: 10.1016/j.vetpar.2017.02.018pubmed: 28249767google scholar: lookup
  9. Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter?. Vet Parasitol 2014 Mar 17;201(1-2):1-8.
    doi: 10.1016/j.vetpar.2014.01.004pubmed: 24485565google scholar: lookup
  10. Debeffe L, McLoughlin PD, Medill SA, Stewart K, Andres D, Shury T, Wagner B, Jenkins E, Gilleard JS, Poissant J. Negative covariance between parasite load and body condition in a population of feral horses.. Parasitology 2016 Jul;143(8):983-97.
    doi: 10.1017/S0031182016000408pubmed: 27046508google scholar: lookup
  11. Rubenstein DI, Hohmann ME. Parasites and social behavior of island feral horses.. Oikos 1989;55:312.
    doi: 10.2307/3565589google scholar: lookup
  12. Nielsen MK, Martin AN, Scare JA, Steuer AE. Precision and spatial variation of cyathostomin mucosal larval counts.. Vet Parasitol 2021 Feb;290:109349.
    doi: 10.1016/j.vetpar.2021.109349pubmed: 33482426google scholar: lookup
  13. Gibson TE. The effect of repeated anthelmintic treatment with phenothiazine on the faecal egg counts of housed horses, with some observations on the life cycle of Trichonema spp. in the horse.. J. Helminthol. 1953;27:29–40.
    doi: 10.1017/S0022149X00023488google scholar: lookup
  14. Giles CJ, Urquhart KA, Longstaffe JA. Larval cyathostomiasis (immature trichonema-induced enteropathy): a report of 15 clinical cases.. Equine Vet J 1985 May;17(3):196-201.
    doi: 10.1111/j.2042-3306.1985.tb02469.xpubmed: 4076127google scholar: lookup
  15. Sallé G, Guillot J, Tapprest J, Foucher N, Sevin C, Laugier C. Compilation of 29 years of postmortem examinations identifies major shifts in equine parasite prevalence from 2000 onwards.. Int J Parasitol 2020 Feb;50(2):125-132.
    doi: 10.1016/j.ijpara.2019.11.004pubmed: 31981673google scholar: lookup
  16. Kornaś S, Sallé G, Skalska M, David I, Ricard A, Cabaret J. Estimation of genetic parameters for resistance to gastro-intestinal nematodes in pure blood Arabian horses.. Int J Parasitol 2015 Mar;45(4):237-42.
    doi: 10.1016/j.ijpara.2014.11.003pubmed: 25592965google scholar: lookup
  17. Scheuerle MC, Stear MJ, Honeder A, Becher AM, Pfister K. Repeatability of strongyle egg counts in naturally infected horses.. Vet Parasitol 2016 Sep 15;228:103-107.
    doi: 10.1016/j.vetpar.2016.08.021pubmed: 27692309google scholar: lookup
  18. Gold S, Regan CE, McLoughlin PD, Gilleard JS, Wilson AJ, Poissant J. Quantitative genetics of gastrointestinal strongyle burden and associated body condition in feral horses.. Int J Parasitol Parasites Wildl 2019 Aug;9:104-111.
    doi: 10.1016/j.ijppaw.2019.03.010pmc: PMC6462499pubmed: 31011533google scholar: lookup
  19. Stear MJ, Park M, Bishop SC. The key components of resistance to Ostertagia circumcincta in lambs.. Parasitol Today 1996 Nov;12(11):438-41.
    doi: 10.1016/0169-4758(96)10069-7pubmed: 15275277google scholar: lookup
  20. Nielsen MK, Baptiste KE, Tolliver SC, Collins SS, Lyons ET. Analysis of multiyear studies in horses in Kentucky to ascertain whether counts of eggs and larvae per gram of feces are reliable indicators of numbers of strongyles and ascarids present.. Vet Parasitol 2010 Nov 24;174(1-2):77-84.
    doi: 10.1016/j.vetpar.2010.08.007pubmed: 20850927google scholar: lookup
  21. Bishop SC, Stear MJ. Modeling of host genetics and resistance to infectious diseases: understanding and controlling nematode infections.. Vet Parasitol 2003 Jul 25;115(2):147-66.
    doi: 10.1016/S0304-4017(03)00204-8pubmed: 12878420google scholar: lookup
  22. Råberg L, Graham AL, Read AF. Decomposing health: tolerance and resistance to parasites in animals.. Philos Trans R Soc Lond B Biol Sci 2009 Jan 12;364(1513):37-49.
    doi: 10.1098/rstb.2008.0184pmc: PMC2666700pubmed: 18926971google scholar: lookup
  23. Sallé G, Jacquiet P, Gruner L, Cortet J, Sauvé C, Prévot F, Grisez C, Bergeaud JP, Schibler L, Tircazes A, François D, Pery C, Bouvier F, Thouly JC, Brunel JC, Legarra A, Elsen JM, Bouix J, Rupp R, Moreno CR. A genome scan for QTL affecting resistance to Haemonchus contortus in sheep.. J Anim Sci 2012 Dec;90(13):4690-705.
    doi: 10.2527/jas.2012-5121pubmed: 22767094google scholar: lookup
  24. Kemper KE, Emery DL, Bishop SC, Oddy H, Hayes BJ, Dominik S, Henshall JM, Goddard ME. The distribution of SNP marker effects for faecal worm egg count in sheep, and the feasibility of using these markers to predict genetic merit for resistance to worm infections.. Genet Res (Camb) 2011 Jun;93(3):203-19.
    doi: 10.1017/S0016672311000097pubmed: 24725775google scholar: lookup
  25. McRae KM, McEwan JC, Dodds KG, Gemmell NJ. Signatures of selection in sheep bred for resistance or susceptibility to gastrointestinal nematodes.. BMC Genomics 2014 Jul 30;15(1):637.
    doi: 10.1186/1471-2164-15-637pmc: PMC4124167pubmed: 25074012google scholar: lookup
  26. Sallé G, Moreno C, Boitard S, Ruesche J, Tircazes-Secula A, Bouvier F, Aletru M, Weisbecker JL, Prévot F, Bergeaud JP, Trumel C, Grisez C, Liénard E, Jacquiet P. Functional investigation of a QTL affecting resistance to Haemonchus contortus in sheep.. Vet Res 2014 Jun 17;45(1):68.
    doi: 10.1186/1297-9716-45-68pmc: PMC4077151pubmed: 24939584google scholar: lookup
  27. Terefe G, Lacroux C, Andreoletti O, Grisez C, Prevot F, Bergeaud JP, Penicaud J, Rouillon V, Gruner L, Brunel JC, Francois D, Bouix J, Dorchies P, Jacquiet P. Immune response to Haemonchus contortus infection in susceptible (INRA 401) and resistant (Barbados Black Belly) breeds of lambs.. Parasite Immunol 2007 Aug;29(8):415-24.
    doi: 10.1111/j.1365-3024.2007.00958.xpubmed: 17650183google scholar: lookup
  28. Slusarewicz P, Pagano S, Mills C, Popa G, Chow KM, Mendenhall M, Rodgers DW, Nielsen MK. Automated parasite faecal egg counting using fluorescence labelling, smartphone image capture and computational image analysis.. Int J Parasitol 2016 Jul;46(8):485-93.
    doi: 10.1016/j.ijpara.2016.02.004pubmed: 27025771google scholar: lookup
  29. Relf VE, Morgan ER, Hodgkinson JE, Matthews JB. A questionnaire study on parasite control practices on UK breeding Thoroughbred studs.. Equine Vet J 2012 Jul;44(4):466-71.
    doi: 10.1111/j.2042-3306.2011.00493.xpubmed: 22050130google scholar: lookup
  30. Lester HE, Bartley DJ, Morgan ER, Hodgkinson JE, Stratford CH, Matthews JB. A cost comparison of faecal egg count-directed anthelmintic delivery versus interval programme treatments in horses.. Vet Rec 2013 Oct 19;173(15):371.
    doi: 10.1136/vr.101804pubmed: 24068698google scholar: lookup
  31. Sallé G, Cortet J, Koch C, Reigner F, Cabaret J. Economic assessment of FEC-based targeted selective drenching in horses.. Vet Parasitol 2015 Nov 30;214(1-2):159-66.
    doi: 10.1016/j.vetpar.2015.09.006pubmed: 26414907google scholar: lookup
  32. Murphy D, Love S. The pathogenic effects of experimental cyathostome infections in ponies.. Vet Parasitol 1997 Jun;70(1-3):99-110.
    doi: 10.1016/S0304-4017(96)01153-3pubmed: 9195714google scholar: lookup
  33. Andersen UV, Reinemeyer CR, Toft N, Olsen SN, Jacobsen S, Nielsen MK. Physiologic and systemic acute phase inflammatory responses in young horses repeatedly infected with cyathostomins and Strongylus vulgaris.. Vet Parasitol 2014 Mar 17;201(1-2):67-74.
    doi: 10.1016/j.vetpar.2014.01.011pubmed: 24529577google scholar: lookup
  34. Clark A, Sallé G, Ballan V, Reigner F, Meynadier A, Cortet J, Koch C, Riou M, Blanchard A, Mach N. Strongyle Infection and Gut Microbiota: Profiling of Resistant and Susceptible Horses Over a Grazing Season.. Front Physiol 2018;9:272.
    doi: 10.3389/fphys.2018.00272pmc: PMC5871743pubmed: 29618989google scholar: lookup
  35. Peachey LE, Castro C, Molena RA, Jenkins TP, Griffin JL, Cantacessi C. Dysbiosis associated with acute helminth infections in herbivorous youngstock - observations and implications.. Sci Rep 2019 Jul 31;9(1):11121.
    doi: 10.1038/s41598-019-47204-6pmc: PMC6668452pubmed: 31366962google scholar: lookup
  36. Walshe N, Duggan V, Cabrera-Rubio R, Crispie F, Cotter P, Feehan O, Mulcahy G. Removal of adult cyathostomins alters faecal microbiota and promotes an inflammatory phenotype in horses.. Int J Parasitol 2019 May;49(6):489-500.
    doi: 10.1016/j.ijpara.2019.02.003pubmed: 30986403google scholar: lookup
  37. Daniels SP, Leng J, Swann JR, Proudman CJ. Bugs and drugs: a systems biology approach to characterising the effect of moxidectin on the horse's faecal microbiome.. Anim Microbiome 2020 Oct 14;2(1):38.
    doi: 10.1186/s42523-020-00056-2pmc: PMC7807906pubmed: 33499996google scholar: lookup
  38. Wang Y, Xiao SH, Xue J, Singer BH, Utzinger J, Holmes E. Systems metabolic effects of a necator americanus infection in Syrian hamster.. J Proteome Res 2009 Dec;8(12):5442-50.
    doi: 10.1021/pr900711jpubmed: 19810771google scholar: lookup
  39. Wu JF, Holmes E, Xue J, Xiao SH, Singer BH, Tang HR, Utzinger J, Wang YL. Metabolic alterations in the hamster co-infected with Schistosoma japonicum and Necator americanus.. Int J Parasitol 2010 May;40(6):695-703.
    doi: 10.1016/j.ijpara.2009.11.003pubmed: 19951707google scholar: lookup
  40. Globisch D, Moreno AY, Hixon MS, Nunes AA, Denery JR, Specht S, Hoerauf A, Janda KD. Onchocerca volvulus-neurotransmitter tyramine is a biomarker for river blindness.. Proc Natl Acad Sci U S A 2013 Mar 12;110(11):4218-23.
    doi: 10.1073/pnas.1221969110pmc: PMC3600455pubmed: 23440222google scholar: lookup
  41. Lagatie O, Njumbe Ediage E, Batsa Debrah L, Diels L, Nolten C, Vinken P, Debrah A, Dillen L, Silber S, Stuyver LJ. Evaluation of the diagnostic potential of urinary N-Acetyltyramine-O,β-glucuronide (NATOG) as diagnostic biomarker for Onchocerca volvulus infection.. Parasit Vectors 2016 May 23;9(1):302.
    doi: 10.1186/s13071-016-1582-6pmc: PMC4877973pubmed: 27216752google scholar: lookup
  42. Lee AH, Shannon CP, Amenyogbe N, Bennike TB, Diray-Arce J, Idoko OT, Gill EE, Ben-Othman R, Pomat WS, van Haren SD, Cao KL, Cox M, Darboe A, Falsafi R, Ferrari D, Harbeson DJ, He D, Bing C, Hinshaw SJ, Ndure J, Njie-Jobe J, Pettengill MA, Richmond PC, Ford R, Saleu G, Masiria G, Matlam JP, Kirarock W, Roberts E, Malek M, Sanchez-Schmitz G, Singh A, Angelidou A, Smolen KK, Brinkman RR, Ozonoff A, Hancock REW, van den Biggelaar AHJ, Steen H, Tebbutt SJ, Kampmann B, Levy O, Kollmann TR. Dynamic molecular changes during the first week of human life follow a robust developmental trajectory.. Nat Commun 2019 Mar 12;10(1):1092.
    doi: 10.1038/s41467-018-07882-8pmc: PMC6414553pubmed: 30862783google scholar: lookup
  43. Klassen P, Fürst P, Schulz C, Mazariegos M, Solomons NW. Plasma free amino acid concentrations in healthy Guatemalan adults and in patients with classic dengue.. Am J Clin Nutr 2001 Mar;73(3):647-52.
    doi: 10.1093/ajcn/73.3.647pubmed: 11237944google scholar: lookup
  44. Gevers D, Kugathasan S, Denson LA, Vázquez-Baeza Y, Van Treuren W, Ren B, Schwager E, Knights D, Song SJ, Yassour M, Morgan XC, Kostic AD, Luo C, González A, McDonald D, Haberman Y, Walters T, Baker S, Rosh J, Stephens M, Heyman M, Markowitz J, Baldassano R, Griffiths A, Sylvester F, Mack D, Kim S, Crandall W, Hyams J, Huttenhower C, Knight R, Xavier RJ. The treatment-naive microbiome in new-onset Crohn's disease.. Cell Host Microbe 2014 Mar 12;15(3):382-392.
    doi: 10.1016/j.chom.2014.02.005pmc: PMC4059512pubmed: 24629344google scholar: lookup
  45. Xiao L, Herd RP, Majewski GA. Comparative efficacy of moxidectin and ivermectin against hypobiotic and encysted cyathostomes and other equine parasites.. Vet Parasitol 1994 May;53(1-2):83-90.
    doi: 10.1016/0304-4017(94)90020-5pubmed: 8091622google scholar: lookup
  46. Wannemacher RW Jr. Key role of various individual amino acids in host response to infection.. Am J Clin Nutr 1977 Aug;30(8):1269-80.
    doi: 10.1093/ajcn/30.8.1269pubmed: 407785google scholar: lookup
  47. Peters A, Krumbholz P, Jäger E, Heintz-Buschart A, Çakir MV, Rothemund S, Gaudl A, Ceglarek U, Schöneberg T, Stäubert C. Metabolites of lactic acid bacteria present in fermented foods are highly potent agonists of human hydroxycarboxylic acid receptor 3.. PLoS Genet 2019 May;15(5):e1008145.
    doi: 10.1371/journal.pgen.1008145pmc: PMC6532841pubmed: 31120900google scholar: lookup
  48. Husted AS, Trauelsen M, Rudenko O, Hjorth SA, Schwartz TW. GPCR-Mediated Signaling of Metabolites.. Cell Metab 2017 Apr 4;25(4):777-796.
    doi: 10.1016/j.cmet.2017.03.008pubmed: 28380372google scholar: lookup
  49. Iljazovic A, Roy U, Gálvez EJC, Lesker TR, Zhao B, Gronow A, Amend L, Will SE, Hofmann JD, Pils MC, Schmidt-Hohagen K, Neumann-Schaal M, Strowig T. Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation.. Mucosal Immunol 2021 Jan;14(1):113-124.
    doi: 10.1038/s41385-020-0296-4pmc: PMC7790746pubmed: 32433514google scholar: lookup
  50. Villarino NF, LeCleir GR, Denny JE, Dearth SP, Harding CL, Sloan SS, Gribble JL, Campagna SR, Wilhelm SW, Schmidt NW. Composition of the gut microbiota modulates the severity of malaria.. Proc Natl Acad Sci U S A 2016 Feb 23;113(8):2235-40.
    doi: 10.1073/pnas.1504887113pmc: PMC4776451pubmed: 26858424google scholar: lookup
  51. Ajibola O, Rowan AD, Ogedengbe CO, Mshelia MB, Cabral DJ, Eze AA, Obaro S, Belenky P. Urogenital schistosomiasis is associated with signatures of microbiome dysbiosis in Nigerian adolescents.. Sci Rep 2019 Jan 29;9(1):829.
    doi: 10.1038/s41598-018-36709-1pmc: PMC6351658pubmed: 30696838google scholar: lookup
  52. Stolzenbach S, Myhill LJ, Andersen LO, Krych L, Mejer H, Williams AR, Nejsum P, Stensvold CR, Nielsen DS, Thamsborg SM. Dietary Inulin and Trichuris suis Infection Promote Beneficial Bacteria Throughout the Porcine Gut.. Front Microbiol 2020;11:312.
    doi: 10.3389/fmicb.2020.00312pmc: PMC7064446pubmed: 32194529google scholar: lookup
  53. Helmby H, Takeda K, Akira S, Grencis RK. Interleukin (IL)-18 promotes the development of chronic gastrointestinal helminth infection by downregulating IL-13.. J Exp Med 2001 Aug 6;194(3):355-64.
    doi: 10.1084/jem.194.3.355pmc: PMC2193471pubmed: 11489954google scholar: lookup
  54. Reynolds LA, Harcus Y, Smith KA, Webb LM, Hewitson JP, Ross EA, Brown S, Uematsu S, Akira S, Gray D, Gray M, MacDonald AS, Cunningham AF, Maizels RM. MyD88 signaling inhibits protective immunity to the gastrointestinal helminth parasite Heligmosomoides polygyrus.. J Immunol 2014 Sep 15;193(6):2984-93.
    doi: 10.4049/jimmunol.1401056pmc: PMC4157852pubmed: 25114104google scholar: lookup
  55. Kelly B, Pearce EL. Amino Assets: How Amino Acids Support Immunity.. Cell Metab 2020 Aug 4;32(2):154-175.
    doi: 10.1016/j.cmet.2020.06.010pubmed: 32649859google scholar: lookup
  56. Wellendorph P, Hansen KB, Balsgaard A, Greenwood JR, Egebjerg J, Bräuner-Osborne H. Deorphanization of GPRC6A: a promiscuous L-alpha-amino acid receptor with preference for basic amino acids.. Mol Pharmacol 2005 Mar;67(3):589-97.
    doi: 10.1124/mol.104.007559pubmed: 15576628google scholar: lookup
  57. Quandt D, Rothe K, Baerwald C, Rossol M. GPRC6A mediates Alum-induced Nlrp3 inflammasome activation but limits Th2 type antibody responses.. Sci Rep 2015 Nov 25;5:16719.
    doi: 10.1038/srep16719pmc: PMC4658484pubmed: 26602597google scholar: lookup
  58. Youm YH, Nguyen KY, Grant RW, Goldberg EL, Bodogai M, Kim D, D'Agostino D, Planavsky N, Lupfer C, Kanneganti TD, Kang S, Horvath TL, Fahmy TM, Crawford PA, Biragyn A, Alnemri E, Dixit VD. The ketone metabolite β-hydroxybutyrate blocks NLRP3 inflammasome-mediated inflammatory disease.. Nat Med 2015 Mar;21(3):263-9.
    doi: 10.1038/nm.3804pmc: PMC4352123pubmed: 25686106google scholar: lookup
  59. Goldberg EL, Asher JL, Molony RD, Shaw AC, Zeiss CJ, Wang C, Morozova-Roche LA, Herzog RI, Iwasaki A, Dixit VD. β-Hydroxybutyrate Deactivates Neutrophil NLRP3 Inflammasome to Relieve Gout Flares.. Cell Rep 2017 Feb 28;18(9):2077-2087.
    doi: 10.1016/j.celrep.2017.02.004pmc: PMC5527297pubmed: 28249154google scholar: lookup
  60. Sina C, Gavrilova O, Förster M, Till A, Derer S, Hildebrand F, Raabe B, Chalaris A, Scheller J, Rehmann A, Franke A, Ott S, Häsler R, Nikolaus S, Fölsch UR, Rose-John S, Jiang HP, Li J, Schreiber S, Rosenstiel P. G protein-coupled receptor 43 is essential for neutrophil recruitment during intestinal inflammation.. J Immunol 2009 Dec 1;183(11):7514-22.
    doi: 10.4049/jimmunol.0900063pubmed: 19917676google scholar: lookup
  61. Wu S, Li RW, Li W, Beshah E, Dawson HD, Urban JF Jr. Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection.. PLoS One 2012;7(4):e35470.
    doi: 10.1371/journal.pone.0035470pmc: PMC3332011pubmed: 22532855google scholar: lookup
  62. Jiao J, Zhou C, Guan LL, McSweeney CS, Tang S, Wang M, Tan Z. Shifts in Host Mucosal Innate Immune Function Are Associated with Ruminal Microbial Succession in Supplemental Feeding and Grazing Goats at Different Ages.. Front Microbiol 2017;8:1655.
    doi: 10.3389/fmicb.2017.01655pmc: PMC5582421pubmed: 28912767google scholar: lookup
  63. Heeb LEM, Egholm C, Impellizzieri D, Ridder F, Boyman O. Regulation of neutrophils in type 2 immune responses.. Curr Opin Immunol 2018 Oct;54:115-122.
    doi: 10.1016/j.coi.2018.06.009pubmed: 30015087google scholar: lookup
  64. Allen JE, Sutherland TE, Rückerl D. IL-17 and neutrophils: unexpected players in the type 2 immune response.. Curr Opin Immunol 2015 Jun;34:99-106.
    doi: 10.1016/j.coi.2015.03.001pubmed: 25794823google scholar: lookup
  65. Sorobetea D, Svensson-Frej M, Grencis R. Immunity to gastrointestinal nematode infections.. Mucosal Immunol 2018 Mar;11(2):304-315.
    doi: 10.1038/mi.2017.113pubmed: 29297502google scholar: lookup
  66. Michels CE, Scales HE, Saunders KA, McGowan S, Brombracher F, Alexander J, Lawrence CE. Neither interleukin-4 receptor alpha expression on CD4+ T cells, or macrophages and neutrophils is required for protective immunity to Trichinella spiralis.. Immunology 2009 Sep;128(1 Suppl):e385-94.
    doi: 10.1111/j.1365-2567.2008.02987.xpmc: PMC2753907pubmed: 19191917google scholar: lookup
  67. Al-Qaoud KM, Pearlman E, Hartung T, Klukowski J, Fleischer B, Hoerauf A. A new mechanism for IL-5-dependent helminth control: neutrophil accumulation and neutrophil-mediated worm encapsulation in murine filariasis are abolished in the absence of IL-5.. Int Immunol 2000 Jun;12(6):899-908.
    doi: 10.1093/intimm/12.6.899pubmed: 10837417google scholar: lookup
  68. Bonne-Année S, Kerepesi LA, Hess JA, O'Connell AE, Lok JB, Nolan TJ, Abraham D. Human and mouse macrophages collaborate with neutrophils to kill larval Strongyloides stercoralis.. Infect Immun 2013 Sep;81(9):3346-55.
    doi: 10.1128/IAI.00625-13pmc: PMC3754234pubmed: 23798541google scholar: lookup
  69. Anthony RM, Urban JF Jr, Alem F, Hamed HA, Rozo CT, Boucher JL, Van Rooijen N, Gause WC. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites.. Nat Med 2006 Aug;12(8):955-60.
    doi: 10.1038/nm1451pmc: PMC1955764pubmed: 16892038google scholar: lookup
  70. Lavoie-Lamoureux A, Moran K, Beauchamp G, Mauel S, Steinbach F, Lefebvre-Lavoie J, Martin JG, Lavoie JP. IL-4 activates equine neutrophils and induces a mixed inflammatory cytokine expression profile with enhanced neutrophil chemotactic mediator release ex vivo.. Am J Physiol Lung Cell Mol Physiol 2010 Oct;299(4):L472-82.
    doi: 10.1152/ajplung.00135.2009pubmed: 20639353google scholar: lookup
  71. R Core Team. R: A Language and Environment for Statistical Computing.. .
  72. Boersema JH, Eysker M, van der Aar WM. The reappearance of strongyle eggs in the faeces of horses after treatment with moxidectin.. Vet Q 1998 Jan;20(1):15-7.
    doi: 10.1080/01652176.1998.9694828pubmed: 9477529google scholar: lookup
  73. Raynaud JP. [Study of the efficiency of a quantitative coproscopic technic for the routine diagnosis and control of parasitic infestations of cattle, sheep, horses and swine].. Ann Parasitol Hum Comp 1970 May-Jun;45(3):321-42.
    doi: 10.1051/parasite/1970453321pubmed: 5531507google scholar: lookup
  74. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.. Nat Biotechnol 2019 Aug;37(8):852-857.
    doi: 10.1038/s41587-019-0209-9pmc: PMC7015180pubmed: 31341288google scholar: lookup
  75. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads.. EMBnet.J. 2011;17:10.
    doi: 10.14806/ej.17.1.200google scholar: lookup
  76. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data.. Nat Methods 2016 Jul;13(7):581-3.
    doi: 10.1038/nmeth.3869pmc: PMC4927377pubmed: 27214047google scholar: lookup
  77. Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis.. ISME J 2017 Dec;11(12):2639-2643.
    doi: 10.1038/ismej.2017.119pmc: PMC5702726pubmed: 28731476google scholar: lookup
  78. Jansen JJ, Hoefsloot HCJ, van der Greef J, Timmerman ME, Smilde AK. Multilevel component analysis of time-resolved metabolic fingerprinting data.. Anal. Chim. Acta. 2005;530:173–183.
    doi: 10.1016/j.aca.2004.09.074google scholar: lookup
  79. Smilde AK, Jansen JJ, Hoefsloot HC, Lamers RJ, van der Greef J, Timmerman ME. ANOVA-simultaneous component analysis (ASCA): a new tool for analyzing designed metabolomics data.. Bioinformatics 2005 Jul 1;21(13):3043-8.
    doi: 10.1093/bioinformatics/bti476pubmed: 15890747google scholar: lookup
  80. Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis.. Nucleic Acids Res 2018 Jul 2;46(W1):W486-W494.
    doi: 10.1093/nar/gky310pmc: PMC6030889pubmed: 29762782google scholar: lookup
  81. Rohart F, Gautier B, Singh A, Lê Cao KA. mixOmics: An R package for 'omics feature selection and multiple data integration.. PLoS Comput Biol 2017 Nov;13(11):e1005752.
    doi: 10.1371/journal.pcbi.1005752pmc: PMC5687754pubmed: 29099853google scholar: lookup
  82. Singh A, Shannon CP, Gautier B, Rohart F, Vacher M, Tebbutt SJ, Lê Cao KA. DIABLO: an integrative approach for identifying key molecular drivers from multi-omics assays.. Bioinformatics 2019 Sep 1;35(17):3055-3062.
    doi: 10.1093/bioinformatics/bty1054pmc: PMC6735831pubmed: 30657866google scholar: lookup
  83. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes.. Nucleic Acids Res 2000 Jan 1;28(1):27-30.
    doi: 10.1093/nar/28.1.27pmc: PMC102409pubmed: 10592173google scholar: lookup

Citations

This article has been cited 3 times.
  1. 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 Feb 17;26(2):106044.
    doi: 10.1016/j.isci.2023.106044pubmed: 36818309google scholar: lookup
  2. Boisseau M, Mach N, Basiaga M, Kuzmina T, Laugier C, Sallé G. Patterns of variation in equine strongyle community structure across age groups and gut compartments. Parasit Vectors 2023 Feb 11;16(1):64.
    doi: 10.1186/s13071-022-05645-5pubmed: 36765420google scholar: lookup
  3. Wen X, Luo S, Lv D, Jia C, Zhou X, Zhai Q, Xi L, Yang C. Variations in the fecal microbiota and their functions of Thoroughbred, Mongolian, and Hybrid horses. Front Vet Sci 2022;9:920080.
    doi: 10.3389/fvets.2022.920080pubmed: 35968025google scholar: lookup
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