Analyze Diet
iScience2023; 26(2); 106044; doi: 10.1016/j.isci.2023.106044

Species interactions, stability, and resilience of the gut microbiota – Helminth assemblage in horses.

Abstract: The nature and strength of interactions entertained among helminths and their host gut microbiota remain largely unexplored. Using 40 naturally infected Welsh ponies, we tracked the gut microbiota-cyathostomin temporal dynamics and stability before and following anthelmintic treatment and the associated host blood transcriptomic response. High shedders harbored 14 species of cyathostomins, dominated by . They exhibited a highly diverse and temporal dynamic gut microbiota, with butyrate-producing Clostridia likely driving the ecosystem steadiness and host tolerance toward cyathostomins infection. However, anthelmintic administration sharply bent the microbial community. It disrupted the ecosystem stability and the time-dependent network of interactions, affecting longer term microbial resilience. These observations highlight how anthelmintic treatments alter the triangular relationship of parasite, host, and gut microbiota and open new perspectives for adding nutritional intervention to current parasite management strategies.
Publication Date: 2023-01-25 PubMed ID: 36818309PubMed Central: PMC9929684DOI: 10.1016/j.isci.2023.106044Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

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 how the interaction between gut bacteria and intestinal worms in horses affects the stability of the gut’s ecosystem, particularly under anthelmintic (anti-parasite) treatment, providing new insights for possible nutrition-based parasite management strategies.

Study Context

  • The researchers aimed to understand the relationships between helminths (intestinal worms), the horse’s gut microbiota (microorganisms including bacteria and fungi), and the impact of anthelmintic treatments on this ecosystem.
  • Previous knowledge of these interactions is scant, so the study helps in filling a gap in the research.

Methodology

  • A total of 40 naturally infected Welsh ponies were included in the study.
  • The research team followed the dynamics and stability of the gut microbiota and cyathostomin (a type of helminth) before and after the administration of an anthelmintic treatment.
  • The researchers also analyzed the responses of the host’s blood transcriptome (the total set of transcripts in a given set of cells).

Findings

  • Ponies with high levels of parasites had 14 species of cyathostomins, primarily dominated by an unspecified species.
  • These high shedders displayed a diverse and temporally dynamic gut microbiota, with Clostridia, a group of bacteria known for butyrate production, possibly driving the stability of the ecosystem and host tolerance to cyathostomin infection.
  • However, the use of anthelmintic treatments considerably changed the bacterial community, disrupting the ecosystem’s stability and the temporal network of interactions, thereby affecting the microbial resilience in the long term.

Implications

  • This study underscores how anthelmintic treatments modify the interplay among the parasite, host, and gut microbiota.
  • The findings present new opportunities for utilizing nutritional interventions alongside traditional parasite management strategies, potentially offering a more holistic and balanced approach for maintaining the health and well-being of horses.

Cite This Article

APA
Boisseau M, Dhorne-Pollet S, Bars-Cortina D, Courtot É, Serreau D, Annonay G, Lluch J, Gesbert A, Reigner F, Sallé G, Mach N. (2023). Species interactions, stability, and resilience of the gut microbiota – Helminth assemblage in horses. iScience, 26(2), 106044. https://doi.org/10.1016/j.isci.2023.106044

Publication

ISSN: 2589-0042
NlmUniqueID: 101724038
Country: United States
Language: English
Volume: 26
Issue: 2
Pages: 106044
PII: 106044

Researcher Affiliations

Boisseau, Michel
  • , Université de Tours, INRAE, UMR1282 Infectiologie et Santé Publique, 37380 Nouzilly, France.
  • IHAP, Université de Toulouse, INRAE, ENVT, 31076 Toulouse, France.
Dhorne-Pollet, Sophie
  • Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350 Jouy-en-Josas, France.
Bars-Cortina, David
  • Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350 Jouy-en-Josas, France.
Courtot, Élise
  • , Université de Tours, INRAE, UMR1282 Infectiologie et Santé Publique, 37380 Nouzilly, France.
Serreau, Delphine
  • , Université de Tours, INRAE, UMR1282 Infectiologie et Santé Publique, 37380 Nouzilly, France.
Annonay, Gwenolah
  • INRAE, US UMR 1426, Genomic platform, 31326 Castanet-Tolosan, France.
Lluch, Jérôme
  • INRAE, US UMR 1426, Genomic platform, 31326 Castanet-Tolosan, France.
Gesbert, Amandine
  • INRAE, UE Physiologie Animale de l'Orfrasière, 37380 Nouzilly, France.
Reigner, Fabrice
  • INRAE, UE Physiologie Animale de l'Orfrasière, 37380 Nouzilly, France.
Sallé, Guillaume
  • , Université de Tours, INRAE, UMR1282 Infectiologie et Santé Publique, 37380 Nouzilly, France.
Mach, Núria
  • Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350 Jouy-en-Josas, France.
  • IHAP, Université de Toulouse, INRAE, ENVT, 31076 Toulouse, France.

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 136 references
  1. Rynkiewicz EC, Pedersen AB, Fenton A. An ecosystem approach to understanding and managing within-host parasite community dynamics.. Trends Parasitol 2015 May;31(5):212-21.
    doi: 10.1016/j.pt.2015.02.005pubmed: 25814004google scholar: lookup
  2. Hayes KS, Bancroft AJ, Goldrick M, Portsmouth C, Roberts IS, Grencis RK. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris.. Science 2010 Jun 11;328(5984):1391-4.
    doi: 10.1126/science.1187703pmc: PMC3428897pubmed: 20538949google scholar: lookup
  3. Reynolds LA, Smith KA, Filbey KJ, Harcus Y, Hewitson JP, Redpath SA, Valdez Y, Yebra MJ, Finlay BB, Maizels RM. Commensal-pathogen interactions in the intestinal tract: lactobacilli promote infection with, and are promoted by, helminth parasites.. Gut Microbes 2014 Jul 1;5(4):522-32.
    doi: 10.4161/gmic.32155pmc: PMC4822684pubmed: 25144609google scholar: lookup
  4. Leung JM, Graham AL, Knowles SCL. Parasite-Microbiota Interactions With the Vertebrate Gut: Synthesis Through an Ecological Lens.. Front Microbiol 2018;9:843.
    doi: 10.3389/fmicb.2018.00843pmc: PMC5960673pubmed: 29867790google scholar: lookup
  5. Cooper P, Walker AW, Reyes J, Chico M, Salter SJ, Vaca M, Parkhill J. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota.. PLoS One 2013;8(10):e76573.
  6. Lee SC, Tang MS, Lim YA, Choy SH, Kurtz ZD, Cox LM, Gundra UM, Cho I, Bonneau R, Blaser MJ, Chua KH, Loke P. Helminth colonization is associated with increased diversity of the gut microbiota.. PLoS Negl Trop Dis 2014 May;8(5):e2880.
  7. Jenkins TP, Rathnayaka Y, Perera PK, Peachey LE, Nolan MJ, Krause L, Rajakaruna RS, Cantacessi C. Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition.. PLoS One 2017;12(9):e0184719.
  8. Aivelo T, Norberg A. Parasite-microbiota interactions potentially affect intestinal communities in wild mammals.. J Anim Ecol 2018 Mar;87(2):438-447.
    doi: 10.1111/1365-2656.12708pubmed: 28555881google scholar: lookup
  9. Newbold LK, Burthe SJ, Oliver AE, Gweon HS, Barnes CJ, Daunt F, van der Gast CJ. Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota.. ISME J 2017 Mar;11(3):663-675.
    doi: 10.1038/ismej.2016.153pmc: PMC5322305pubmed: 27983724google scholar: lookup
  10. Knowles SC, Fenton A, Petchey OL, Jones TR, Barber R, Pedersen AB. Stability of within-host-parasite communities in a wild mammal system.. Proc Biol Sci 2013 Jul 7;280(1762):20130598.
    doi: 10.1098/rspb.2013.0598pmc: PMC3673050pubmed: 23677343google scholar: lookup
  11. Ling F, Steinel N, Weber J, Ma L, Smith C, Correa D, Zhu B, Bolnick D, Wang G. The gut microbiota response to helminth infection depends on host sex and genotype.. ISME J 2020 May;14(5):1141-1153.
    doi: 10.1038/s41396-020-0589-3pmc: PMC7174316pubmed: 32005978google scholar: lookup
  12. 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.
  13. Li RW, Wu S, Li W, Navarro K, Couch RD, Hill D, Urban JF Jr. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis.. Infect Immun 2012 Jun;80(6):2150-7.
    pmc: PMC3370577pubmed: 22493085doi: 10.1128/iai.00141-12google scholar: lookup
  14. Cortés A, Wills J, Su X, Hewitt RE, Robertson J, Scotti R, Price DRG, Bartley Y, McNeilly TN, Krause L, Powell JJ, Nisbet AJ, Cantacessi C. Infection with the sheep gastrointestinal nematode Teladorsagia circumcincta increases luminal pathobionts.. Microbiome 2020 Apr 30;8(1):60.
    doi: 10.1186/s40168-020-00818-9pmc: PMC7193420pubmed: 32354347google scholar: lookup
  15. Li RW, Wu S, Li W, Huang Y, Gasbarre LC. Metagenome plasticity of the bovine abomasal microbiota in immune animals in response to Ostertagia ostertagi infection.. PLoS One 2011;6(9):e24417.
  16. Li RW, Li W, Sun J, Yu P, Baldwin RL, Urban JF. The effect of helminth infection on the microbial composition and structure of the caprine abomasal microbiome.. Sci Rep 2016 Feb 8;6:20606.
    doi: 10.1038/srep20606pmc: PMC4757478pubmed: 26853110google scholar: lookup
  17. 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
  18. Peachey LE, Molena RA, Jenkins TP, Di Cesare A, Traversa D, Hodgkinson JE, Cantacessi C. The relationships between faecal egg counts and gut microbial composition in UK Thoroughbreds infected by cyathostomins.. Int J Parasitol 2018 May;48(6):403-412.
  19. 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
  20. Kunz IGZ, Reed KJ, Metcalf JL, Hassel DM, Coleman RJ, Hess TM, Coleman SJ. Equine Fecal Microbiota Changes Associated With Anthelmintic Administration.. J Equine Vet Sci 2019 Jun;77:98-106.
    doi: 10.1016/j.jevs.2019.01.018pubmed: 31133326google scholar: lookup
  21. 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
  22. Ramanan D, Bowcutt R, Lee SC, Tang MS, Kurtz ZD, Ding Y, Honda K, Gause WC, Blaser MJ, Bonneau RA, Lim YA, Loke P, Cadwell K. Helminth infection promotes colonization resistance via type 2 immunity.. Science 2016 Apr 29;352(6285):608-12.
    pmc: PMC4905769pubmed: 27080105doi: 10.1126/science.aaf3229google scholar: lookup
  23. Rosa BA, Snowden C, Martin J, Fischer K, Kupritz J, Beshah E, Supali T, Gankpala L, Fischer PU, Urban JF Jr, Mitreva M. Whipworm-Associated Intestinal Microbiome Members Consistent Across Both Human and Mouse Hosts.. Front Cell Infect Microbiol 2021;11:637570.
    doi: 10.3389/fcimb.2021.637570pmc: PMC7991909pubmed: 33777847google scholar: lookup
  24. Fricke WF, Song Y, Wang AJ, Smith A, Grinchuk V, Mongodin E, Pei C, Ma B, Lu N, Urban JF Jr, Shea-Donohue T, Zhao A. Type 2 immunity-dependent reduction of segmented filamentous bacteria in mice infected with the helminthic parasite Nippostrongylus brasiliensis.. Microbiome 2015 Sep 17;3:40.
    doi: 10.1186/s40168-015-0103-8pmc: PMC4574229pubmed: 26377648google scholar: lookup
  25. Holm JB, Sorobetea D, Kiilerich P, Ramayo-Caldas Y, Estellé J, Ma T, Madsen L, Kristiansen K, Svensson-Frej M. Chronic Trichuris muris Infection Decreases Diversity of the Intestinal Microbiota and Concomitantly Increases the Abundance of Lactobacilli.. PLoS One 2015;10(5):e0125495.
  26. 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
  27. Walshe N, Mulcahy G, Crispie F, Cabrera-Rubio R, Cotter P, Jahns H, Duggan V. Outbreak of acute larval cyathostominosis - A "perfect storm" of inflammation and dysbiosis.. Equine Vet J 2021 Jul;53(4):727-739.
    doi: 10.1111/evj.13350pmc: PMC8246859pubmed: 32920897google scholar: lookup
  28. Peachey LE, Jenkins TP, Cantacessi C. This Gut Ain't Big Enough for Both of Us. Or Is It? Helminth-Microbiota Interactions in Veterinary Species.. Trends Parasitol 2017 Aug;33(8):619-632.
    doi: 10.1016/j.pt.2017.04.004pubmed: 28506779google scholar: lookup
  29. Cortés A, Toledo R, Cantacessi C. Classic Models for New Perspectives: Delving into Helminth-Microbiota-Immune System Interactions.. Trends Parasitol 2018 Aug;34(8):640-654.
    doi: 10.1016/j.pt.2018.05.009pubmed: 29941205google scholar: lookup
  30. Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: Networks, competition, and stability.. Science 2015 Nov 6;350(6261):663-6.
    doi: 10.1126/science.aad2602pubmed: 26542567google scholar: lookup
  31. Walshe N, Mulcahy G, Hodgkinson J, Peachey L. No Worm Is an Island; The Influence of Commensal Gut Microbiota on Cyathostomin Infections.. Animals (Basel) 2020 Dec 5;10(12).
    doi: 10.3390/ani10122309pmc: PMC7762139pubmed: 33291496google scholar: lookup
  32. May RM. Will a large complex system be stable?. Nature 1972 Aug 18;238(5364):413-4.
    pubmed: 4559589doi: 10.1038/238413a0google scholar: lookup
  33. McNally L, Brown SP. Microbiome: Ecology of stable gut communities.. Nat Microbiol 2016 Jan 11;1:15016.
    doi: 10.1038/nmicrobiol.2015.16pubmed: 27571760google scholar: lookup
  34. Coyte KZ, Rakoff-Nahoum S. Understanding Competition and Cooperation within the Mammalian Gut Microbiome.. Curr Biol 2019 Jun 3;29(11):R538-R544.
    doi: 10.1016/j.cub.2019.04.017pmc: PMC6935513pubmed: 31163167google scholar: lookup
  35. McClemens J, Kim JJ, Wang H, Mao YK, Collins M, Kunze W, Bienenstock J, Forsythe P, Khan WI. Lactobacillus rhamnosus ingestion promotes innate host defense in an enteric parasitic infection.. Clin Vaccine Immunol 2013 Jun;20(6):818-26.
    doi: 10.1128/CVI.00047-13pmc: PMC3675974pubmed: 23536695google scholar: lookup
  36. Sugihara G, May R, Ye H, Hsieh CH, Deyle E, Fogarty M, Munch S. Detecting causality in complex ecosystems.. Science 2012 Oct 26;338(6106):496-500.
    doi: 10.1126/science.1227079pubmed: 22997134google scholar: lookup
  37. Houlden A, Hayes KS, Bancroft AJ, Worthington JJ, Wang P, Grencis RK, Roberts IS. Chronic Trichuris muris Infection in C57BL/6 Mice Causes Significant Changes in Host Microbiota and Metabolome: Effects Reversed by Pathogen Clearance.. PLoS One 2015;10(5):e0125945.
  38. Afrin T, Murase K, Kounosu A, Hunt VL, Bligh M, Maeda Y, Hino A, Maruyama H, Tsai IJ, Kikuchi T. Sequential Changes in the Host Gut Microbiota During Infection With the Intestinal Parasitic Nematode Strongyloides venezuelensis.. Front Cell Infect Microbiol 2019;9:217.
    doi: 10.3389/fcimb.2019.00217pmc: PMC6604662pubmed: 31293983google scholar: lookup
  39. Gaulke CA, Martins ML, Watral VG, Humphreys IR, Spagnoli ST, Kent ML, Sharpton TJ. A longitudinal assessment of host-microbe-parasite interactions resolves the zebrafish gut microbiome's link to Pseudocapillaria tomentosa infection and pathology.. Microbiome 2019 Jan 24;7(1):10.
    doi: 10.1186/s40168-019-0622-9pmc: PMC6346533pubmed: 30678738google scholar: lookup
  40. Wootton JT, Emmerson M. Measurement of interaction strength in nature. Annu. Rev. Ecol. Evol. Syst. 2005;36:419–444.
  41. He F, Zhai J, Zhang L, Liu D, Ma Y, Rong K, Xu Y, Ma J. Variations in gut microbiota and fecal metabolic phenotype associated with Fenbendazole and Ivermectin Tablets by 16S rRNA gene sequencing and LC/MS-based metabolomics in Amur tiger.. Biochem Biophys Res Commun 2018 May 15;499(3):447-453.
    doi: 10.1016/j.bbrc.2018.03.158pubmed: 29596832google scholar: lookup
  42. Pedersen AB, Antonovics J. Anthelmintic treatment alters the parasite community in a wild mouse host.. Biol Lett 2013 Aug 23;9(4):20130205.
    doi: 10.1098/rsbl.2013.0205pmc: PMC3730629pubmed: 23658004google scholar: lookup
  43. Budischak SA, Hoberg EP, Abrams A, Jolles AE, Ezenwa VO. Experimental insight into the process of parasite community assembly.. J Anim Ecol 2016 Sep;85(5):1222-33.
    doi: 10.1111/1365-2656.12548pubmed: 27174037google scholar: lookup
  44. Yang CA, Liang C, Lin CL, Hsiao CT, Peng CT, Lin HC, Chang JG. Impact of Enterobius vermicularis infection and mebendazole treatment on intestinal microbiota and host immune response.. PLoS Negl Trop Dis 2017 Sep;11(9):e0005963.
  45. Schneeberger PHH, Coulibaly JT, Gueuning M, Moser W, Coburn B, Frey JE, Keiser J. Off-target effects of tribendimidine, tribendimidine plus ivermectin, tribendimidine plus oxantel-pamoate, and albendazole plus oxantel-pamoate on the human gut microbiota.. Int J Parasitol Drugs Drug Resist 2018 Dec;8(3):372-378.
  46. Ogbourne CP. The prevalence, relative abundance and site distribution of nematodes of the subfamily Cyathostominae in horses killed in Britain.. J Helminthol 1976 Sep;50(3):203-14.
    pubmed: 993579doi: 10.1017/s0022149x00027760google scholar: lookup
  47. Bucknell DG, Gasser RB, Beveridge I. The prevalence and epidemiology of gastrointestinal parasites of horses in Victoria, Australia.. Int J Parasitol 1995 Jun;25(6):711-24.
    pubmed: 7657457doi: 10.1016/0020-7519(94)00214-9google scholar: lookup
  48. Kuzmina TA, Kharchenko VA, Starovir AI, Dvojnos GM. Analysis of the strongylid nematodes (Nematoda: Strongylidae) community after deworming of brood horses in Ukraine.. Vet Parasitol 2005 Aug 10;131(3-4):283-90.
    doi: 10.1016/j.vetpar.2005.05.010pubmed: 15979240google scholar: lookup
  49. 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
  50. Ang L, Vinderola G, Endo A, Kantanen J, Jingfeng C, Binetti A, Burns P, Qingmiao S, Suying D, Zujiang Y, Rios-Covian D, Mantziari A, Beasley S, Gomez-Gallego C, Gueimonde M, Salminen S. Gut Microbiome Characteristics in feral and domesticated horses from different geographic locations.. Commun Biol 2022 Feb 25;5(1):172.
    doi: 10.1038/s42003-022-03116-2pmc: PMC8881449pubmed: 35217713google scholar: lookup
  51. Gilroy R, Leng J, Ravi A, Adriaenssens EM, Oren A, Baker D, La Ragione RM, Proudman C, Pallen MJ. Metagenomic investigation of the equine faecal microbiome reveals extensive taxonomic diversity.. PeerJ 2022;10:e13084.
    doi: 10.7717/peerj.13084pmc: PMC8957277pubmed: 35345588google scholar: lookup
  52. 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 Oct 3;5(1):1032.
    doi: 10.1038/s42003-022-03977-7pmc: PMC9529974pubmed: 36192523google scholar: lookup
  53. Plancade S, Clark A, Philippe C, Helbling JC, Moisan MP, Esquerré D, Le Moyec L, Robert C, Barrey E, Mach N. Unraveling the effects of the gut microbiota composition and function on horse endurance physiology.. Sci Rep 2019 Jul 3;9(1):9620.
    doi: 10.1038/s41598-019-46118-7pmc: PMC6610142pubmed: 31270376google scholar: lookup
  54. Mach N, Lansade L, Bars-Cortina D, Dhorne-Pollet S, Foury A, Moisan MP, Ruet A. Gut microbiota resilience in horse athletes following holidays out to pasture.. Sci Rep 2021 Mar 3;11(1):5007.
    doi: 10.1038/s41598-021-84497-ypmc: PMC7930273pubmed: 33658551google scholar: lookup
  55. Mach N, Ruet A, Clark A, Bars-Cortina D, Ramayo-Caldas Y, Crisci E, Pennarun S, Dhorne-Pollet S, Foury A, Moisan MP, Lansade L. Priming for welfare: gut microbiota is associated with equitation conditions and behavior in horse athletes.. Sci Rep 2020 May 20;10(1):8311.
    doi: 10.1038/s41598-020-65444-9pmc: PMC7239938pubmed: 32433513google scholar: lookup
  56. Stewart HL, Pitta D, Indugu N, Vecchiarelli B, Engiles JB, Southwood LL. Characterization of the fecal microbiota of healthy horses.. Am J Vet Res 2018 Aug;79(8):811-819.
    doi: 10.2460/ajvr.79.8.811pubmed: 30058849google scholar: lookup
  57. O' Donnell MM, Harris HM, Jeffery IB, Claesson MJ, Younge B, O' Toole PW, Ross RP. The core faecal bacterial microbiome of Irish Thoroughbred racehorses.. Lett Appl Microbiol 2013 Dec;57(6):492-501.
    doi: 10.1111/lam.12137pubmed: 23889584google scholar: lookup
  58. Costa MC, Weese JS. The equine intestinal microbiome.. Anim Health Res Rev 2012 Jun;13(1):121-8.
    doi: 10.1017/S1466252312000035pubmed: 22626511google scholar: lookup
  59. Poissant J, Gavriliuc S, Bellaw J, Redman EM, Avramenko RW, Robinson D, Workentine ML, Shury TK, Jenkins EJ, McLoughlin PD, Nielsen MK, Gilleard JS. A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses.. Int J Parasitol 2021 Feb;51(2-3):183-192.
    doi: 10.1016/j.ijpara.2020.09.003pubmed: 33242465google scholar: lookup
  60. Malsa J, Courtot É, Boisseau M, Dumont B, Gombault P, Kuzmina TA, Basiaga M, Lluch J, Annonay G, Dhorne-Pollet S, Mach N, Sutra JF, 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 Sep;149(11):1439-1449.
    doi: 10.1017/S0031182022000853pubmed: 35929352google scholar: lookup
  61. Sargison N, Chambers A, Chaudhry U, Costa Júnior L, Doyle SR, Ehimiyein A, Evans M, Jennings A, Kelly R, Sargison F, Sinclair M, Zahid O. Faecal egg counts and nemabiome metabarcoding highlight the genomic complexity of equine cyathostomin communities and provide insight into their dynamics in a Scottish native pony herd.. Int J Parasitol 2022 Nov;52(12):763-774.
    doi: 10.1016/j.ijpara.2022.08.002pubmed: 36208676google scholar: lookup
  62. Nielsen MK. Anthelmintic resistance in equine nematodes: Current status and emerging trends.. Int J Parasitol Drugs Drug Resist 2022 Dec;20:76-88.
  63. Bellaw JL, Nielsen MK. Meta-analysis of cyathostomin species-specific prevalence and relative abundance in domestic horses from 1975-2020: emphasis on geographical region and specimen collection method.. Parasit Vectors 2020 Oct 12;13(1):509.
    doi: 10.1186/s13071-020-04396-5pmc: PMC7552500pubmed: 33046130google scholar: lookup
  64. Collobert-Laugier C, Hoste H, Sevin C, Dorchies P. Prevalence, abundance and site distribution of equine small strongyles in Normandy, France.. Vet Parasitol 2002 Dec 11;110(1-2):77-83.
    doi: 10.1016/S0304-4017(02)00328-Xpubmed: 12446091google scholar: lookup
  65. Kuzmina TA, Dzeverin I, Kharchenko VA. Strongylids in domestic horses: Influence of horse age, breed and deworming programs on the strongyle parasite community.. Vet Parasitol 2016 Aug 30;227:56-63.
    doi: 10.1016/j.vetpar.2016.07.024pubmed: 27523938google scholar: lookup
  66. Jiang P, Lai S, Wu S, Zhao XM, Chen WH. Host DNA contents in fecal metagenomics as a biomarker for intestinal diseases and effective treatment.. BMC Genomics 2020 May 11;21(1):348.
    doi: 10.1186/s12864-020-6749-zpmc: PMC7216530pubmed: 32393180google scholar: lookup
  67. Olsson LM, Boulund F, Nilsson S, Khan MT, Gummesson A, Fagerberg L, Engstrand L, Perkins R, Uhlén M, Bergström G, Tremaroli V, Bäckhed F. Dynamics of the normal gut microbiota: A longitudinal one-year population study in Sweden.. Cell Host Microbe 2022 May 11;30(5):726-739.e3.
    doi: 10.1016/j.chom.2022.03.002pubmed: 35349787google scholar: lookup
  68. Clark T, Ye H, Isbell F, Deyle ER, Cowles J, Tilman GD, Sugihara G. Spatial convergent cross mapping to detect causal relationships from short time series.. Ecology 2015 May;96(5):1174-81.
    doi: 10.1890/14-1479.1pubmed: 26236832google scholar: lookup
  69. Ye SH, Siddle KJ, Park DJ, Sabeti PC. Benchmarking Metagenomics Tools for Taxonomic Classification.. Cell 2019 Aug 8;178(4):779-794.
    doi: 10.1016/j.cell.2019.07.010pmc: PMC6716367pubmed: 31398336google scholar: lookup
  70. Nielsen MK, Betancourt A, Lyons ET, Horohov DW, Jacobsen S. Characterization of the inflammatory response to anthelmintic treatment of ponies with cyathostominosis.. Vet J 2013 Nov;198(2):457-62.
    doi: 10.1016/j.tvjl.2013.08.012pubmed: 24035469google scholar: lookup
  71. Claro da Silva T, Polli JE, Swaan PW. The solute carrier family 10 (SLC10): beyond bile acid transport.. Mol Aspects Med 2013 Apr-Jun;34(2-3):252-69.
    doi: 10.1016/j.mam.2012.07.004pmc: PMC3602841pubmed: 23506869google scholar: lookup
  72. Steuer AE, Anderson HP, Shepherd T, Clark M, Scare JA, Gravatte HS, Nielsen MK. Parasite dynamics in untreated horses through one calendar year.. Parasit Vectors 2022 Feb 8;15(1):50.
    doi: 10.1186/s13071-022-05168-zpmc: PMC8822790pubmed: 35135605google scholar: lookup
  73. Reid SW, Mair TS, Hillyer MH, Love S. Epidemiological risk factors associated with a diagnosis of clinical cyathostomiasis in the horse.. Equine Vet J 1995 Mar;27(2):127-30.
  74. Herbert DR, Lee JJ, Lee NA, Nolan TJ, Schad GA, Abraham D. Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice.. J Immunol 2000 Oct 15;165(8):4544-51.
    doi: 10.4049/jimmunol.165.8.4544pubmed: 11035095google scholar: lookup
  75. Cortés A, Peachey L, Scotti R, Jenkins TP, Cantacessi C. Helminth-microbiota cross-talk - A journey through the vertebrate digestive system.. Mol Biochem Parasitol 2019 Oct;233:111222.
  76. Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, Zhu D, Koya JB, Wei L, Li J, Chen ZS. Microbiota in health and diseases.. Signal Transduct Target Ther 2022 Apr 23;7(1):135.
    doi: 10.1038/s41392-022-00974-4pmc: PMC9034083pubmed: 35461318google scholar: lookup
  77. White EC, Houlden A, Bancroft AJ, Hayes KS, Goldrick M, Grencis RK, Roberts IS. Manipulation of host and parasite microbiotas: Survival strategies during chronic nematode infection.. Sci Adv 2018 Mar;4(3):eaap7399.
    doi: 10.1126/sciadv.aap7399pmc: PMC5851687pubmed: 29546242google scholar: lookup
  78. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K, Kim S, Fritz JV, Wilmes P, Ueha S, Matsushima K, Ohno H, Olle B, Sakaguchi S, Taniguchi T, Morita H, Hattori M, Honda K. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota.. Nature 2013 Aug 8;500(7461):232-6.
    doi: 10.1038/nature12331pubmed: 23842501google scholar: lookup
  79. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, Taniguchi T, Takeda K, Hori S, Ivanov II, Umesaki Y, Itoh K, Honda K. Induction of colonic regulatory T cells by indigenous Clostridium species.. Science 2011 Jan 21;331(6015):337-41.
    doi: 10.1126/science.1198469pmc: PMC3969237pubmed: 21205640google scholar: lookup
  80. Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, Harmsen HJM, Faber KN, Hermoso MA. Short Chain Fatty Acids (SCFAs)-Mediated Gut Epithelial and Immune Regulation and Its Relevance for Inflammatory Bowel Diseases.. Front Immunol 2019;10:277.
    doi: 10.3389/fimmu.2019.00277pmc: PMC6421268pubmed: 30915065google scholar: lookup
  81. Heinken A, Ravcheev DA, Baldini F, Heirendt L, Fleming RMT, Thiele I. Systematic assessment of secondary bile acid metabolism in gut microbes reveals distinct metabolic capabilities in inflammatory bowel disease.. Microbiome 2019 May 15;7(1):75.
    doi: 10.1186/s40168-019-0689-3pmc: PMC6521386pubmed: 31092280google scholar: lookup
  82. Lindenberg F, Krych L, Fielden J, Kot W, Frøkiær H, van Galen G, Nielsen DS, Hansen AK. Expression of immune regulatory genes correlate with the abundance of specific Clostridiales and Verrucomicrobia species in the equine ileum and cecum.. Sci Rep 2019 Sep 3;9(1):12674.
    doi: 10.1038/s41598-019-49081-5pmc: PMC6722064pubmed: 31481726google scholar: lookup
  83. Zaiss MM, Rapin A, Lebon L, Dubey LK, Mosconi I, Sarter K, Piersigilli A, Menin L, Walker AW, Rougemont J, Paerewijck O, Geldhof P, McCoy KD, Macpherson AJ, Croese J, Giacomin PR, Loukas A, Junt T, Marsland BJ, Harris NL. The Intestinal Microbiota Contributes to the Ability of Helminths to Modulate Allergic Inflammation.. Immunity 2015 Nov 17;43(5):998-1010.
  84. Reinemeyer CR, Smith SA, Gabel AA, Herd RP. The prevalence and intensity of internal parasites of horses in the U.S.A.. Vet Parasitol 1984 Jul;15(1):75-83.
    doi: 10.1016/0304-4017(84)90112-2pubmed: 6237483google scholar: lookup
  85. Rausch S, Midha A, Kuhring M, Affinass N, Radonic A, Kühl AA, Bleich A, Renard BY, Hartmann S. Parasitic Nematodes Exert Antimicrobial Activity and Benefit From Microbiota-Driven Support for Host Immune Regulation.. Front Immunol 2018;9:2282.
    doi: 10.3389/fimmu.2018.02282pmc: PMC6186814pubmed: 30349532google scholar: lookup
  86. Rafaluk-Mohr C, Gerth M, Sealey JE, Ekroth AKE, Aboobaker AA, Kloock A, King KC. Microbial protection favors parasite tolerance and alters host-parasite coevolutionary dynamics.. Curr Biol 2022 Apr 11;32(7):1593-1598.e3.
    doi: 10.1016/j.cub.2022.01.063pmc: PMC9355892pubmed: 35148861google scholar: lookup
  87. Lin CH, Chen MC, Lin LL, Christian DA, Min B, Hunter CA, Lu LF. Gut epithelial IL-27 confers intestinal immunity through the induction of intraepithelial lymphocytes.. J Exp Med 2021 Nov 1;218(11).
    doi: 10.1084/jem.20210021pmc: PMC8480671pubmed: 34554189google scholar: lookup
  88. Steinbach T, Bauer C, Sasse H, Baumgärtner W, Rey-Moreno C, Hermosilla C, Damriyasa IM, Zahner H. Small strongyle infection: consequences of larvicidal treatment of horses with fenbendazole and moxidectin.. Vet Parasitol 2006 Jun 30;139(1-3):115-31.
    doi: 10.1016/j.vetpar.2006.03.028pubmed: 16675126google scholar: lookup
  89. Betancourt A, Lyons ET, Horohov DW. Characterisation of the inflammatory cytokine response to anthelmintic treatment in ponies.. Equine Vet J 2015 Mar;47(2):240-4.
    doi: 10.1111/evj.12280pubmed: 24750265google scholar: lookup
  90. 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
  91. 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.
    pubmed: 8091622doi: 10.1016/0304-4017(94)90020-5google scholar: lookup
  92. Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE. Interactions between multiple helminths and the gut microbiota in wild rodents.. Philos Trans R Soc Lond B Biol Sci 2015 Aug 19;370(1675).
    doi: 10.1098/rstb.2014.0295pmc: PMC4528493pubmed: 26150661google scholar: lookup
  93. Hu D, Chao Y, Zhang B, Wang C, Qi Y, Ente M, Zhang D, Li K, Mok KM. Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski's horses in China.. PLoS One 2021;16(5):e0251512.
  94. Nielsen MK. Universal challenges for parasite control: a perspective from equine parasitology.. Trends Parasitol 2015 Jul;31(7):282-4.
    doi: 10.1016/j.pt.2015.04.013pubmed: 26143301google scholar: lookup
  95. Martin I, Djuardi Y, Sartono E, Rosa BA, Supali T, Mitreva M, Houwing-Duistermaat JJ, Yazdanbakhsh M. Dynamic changes in human-gut microbiome in relation to a placebo-controlled anthelminthic trial in Indonesia.. PLoS Negl Trop Dis 2018 Aug;12(8):e0006620.
  96. Zaneveld JR, McMinds R, Vega Thurber R. Stress and stability: applying the Anna Karenina principle to animal microbiomes.. Nat Microbiol 2017 Aug 24;2:17121.
    doi: 10.1038/nmicrobiol.2017.121pubmed: 28836573google scholar: lookup
  97. Fassarella M, Blaak EE, Penders J, Nauta A, Smidt H, Zoetendal EG. Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health.. Gut 2021 Mar;70(3):595-605.
    doi: 10.1136/gutjnl-2020-321747pubmed: 33051190google scholar: lookup
  98. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, Rosenbaum M, Gordon JI. The long-term stability of the human gut microbiota.. Science 2013 Jul 5;341(6141):1237439.
    doi: 10.1126/science.1237439pmc: PMC3791589pubmed: 23828941google scholar: lookup
  99. Dai W, Chen J, Xiong J. Concept of microbial gatekeepers: Positive guys?. Appl Microbiol Biotechnol 2019 Jan;103(2):633-641.
    doi: 10.1007/s00253-018-9522-3pubmed: 30465305google scholar: lookup
  100. Williams AR, Peña-Espinoza MA, Boas U, Simonsen HT, Enemark HL, Thamsborg SM. Anthelmintic activity of chicory (Cichorium intybus): in vitro effects on swine nematodes and relationship to sesquiterpene lactone composition.. Parasitology 2016 May;143(6):770-7.
    doi: 10.1017/S0031182016000287pubmed: 26935644google scholar: lookup
  101. Schneeberger PHH, Gueuning M, Welsche S, Hürlimann E, Dommann J, Häberli C, Frey JE, Sayasone S, Keiser J. Different gut microbial communities correlate with efficacy of albendazole-ivermectin against soil-transmitted helminthiases.. Nat Commun 2022 Feb 25;13(1):1063.
    doi: 10.1038/s41467-022-28658-1pmc: PMC8881608pubmed: 35217670google scholar: lookup
  102. Mshelia ES, Adamu L, Wakil Y, Turaki UA, Gulani IA, Musa J. The association between gut microbiome, sex, age and body condition scores of horses in Maiduguri and its environs.. Microb Pathog 2018 May;118:81-86.
    doi: 10.1016/j.micpath.2018.03.018pubmed: 29530806google scholar: lookup
  103. Francisco I, Arias M, Cortiñas FJ, Francisco R, Mochales E, Dacal V, Suárez JL, Uriarte J, Morrondo P, Sánchez-Andrade R, Díez-Baños P, Paz-Silva A. Intrinsic Factors Influencing the Infection by Helminth Parasites in Horses under an Oceanic Climate Area (NW Spain).. J Parasitol Res 2009;2009.
    doi: 10.1155/2009/616173pmc: PMC2915776pubmed: 20721327google scholar: lookup
  104. Sallé G, Kornaś S, Basiaga M. Equine strongyle communities are constrained by horse sex and species dipersal-fecundity trade-off.. Parasit Vectors 2018 May 2;11(1):279.
    doi: 10.1186/s13071-018-2858-9pmc: PMC5930759pubmed: 29716644google scholar: lookup
  105. Mitchell MC, Tzelos T, Handel I, McWilliam HE, Hodgkinson JE, Nisbet AJ, Kharchenko VO, Burgess ST, Matthews JB. Development of a recombinant protein-based ELISA for diagnosis of larval cyathostomin infection.. Parasitology 2016 Jul;143(8):1055-66.
    doi: 10.1017/S0031182016000627pubmed: 27174468google scholar: lookup
  106. Papaiakovou M, Littlewood DTJ, Doyle SR, Gasser RB, Cantacessi C. Worms and bugs of the gut: the search for diagnostic signatures using barcoding, and metagenomics-metabolomics.. Parasit Vectors 2022 Apr 1;15(1):118.
    doi: 10.1186/s13071-022-05225-7pmc: PMC8973539pubmed: 35365192google scholar: lookup
  107. 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
  108. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    pmc: PMC4302049pubmed: 25516281doi: 10.1186/s13059-014-0550-8google scholar: lookup
  109. Murali A, Bhargava A, Wright ES. IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences.. Microbiome 2018 Aug 9;6(1):140.
    doi: 10.1186/s40168-018-0521-5pmc: PMC6085705pubmed: 30092815google scholar: lookup
  110. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.. PLoS One 2013;8(4):e61217.
  111. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
  112. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression.. Nat Methods 2017 Apr;14(4):417-419.
    doi: 10.1038/nmeth.4197pmc: PMC5600148pubmed: 28263959google scholar: lookup
  113. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Software 2015;67:1–48.
    doi: 10.18637/jss.v067.i01google scholar: lookup
  114. Dixon P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 2003;14:927–930.
  115. Baselga A, Orme D, Villeger S, De Bortoli J, Leprieur F. betapart: Partitioning Beta Diversity into Turnover and Nestedness Components. 2013. R pakcage version 1.3.
  116. Mallick H, Rahnavard A, McIver LJ, Ma S, Zhang Y, Nguyen LH, Tickle TL, Weingart G, Ren B, Schwager EH, Chatterjee S, Thompson KN, Wilkinson JE, Subramanian A, Lu Y, Waldron L, Paulson JN, Franzosa EA, Bravo HC, Huttenhower C. Multivariable association discovery in population-scale meta-omics studies.. PLoS Comput Biol 2021 Nov;17(11):e1009442.
  117. Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Müller M. pROC: an open-source package for R and S+ to analyze and compare ROC curves.. BMC Bioinformatics 2011 Mar 17;12:77.
    doi: 10.1186/1471-2105-12-77pmc: PMC3068975pubmed: 21414208google scholar: lookup
  118. Wang C, Torgerson PR, Kaplan RM, George MM, Furrer R. Modelling anthelmintic resistance by extending eggCounts package to allow individual efficacy.. Int J Parasitol Drugs Drug Resist 2018 Dec;8(3):386-393.
  119. Ye H, Clark A, Deyle E, Munch S, Keyes O, Cai J, White E, Cowles J, Stagge J, Daon Y. Redm: applications of empirical dynamic modeling from time series. Zenodo 2018.
    doi: 10.5281/zenodo.1294063google scholar: lookup
  120. Animal Physiology Facility. 2018.
  121. Sallé G, Canlet C, Cortet J, Koch C, Malsa J, Reigner F, Riou M, Perrot N, Blanchard A, Mach N. Integrative biology defines novel biomarkers of resistance to strongylid infection in horses.. Sci Rep 2021 Jul 12;11(1):14278.
    doi: 10.1038/s41598-021-93468-2pmc: PMC8275762pubmed: 34253752google scholar: lookup
  122. Gokbulut C, Nolan AM, McKellar QA. Pharmacokinetic disposition and faecal excretion of pyrantel embonate following oral administration in horses.. J Vet Pharmacol Ther 2001 Feb;24(1):77-9.
  123. Nielsen MK. Parasite faecal egg counts in equine veterinary practice. Equine Vet. Educ. 2022;34:584–591.
    doi: 10.1111/eve.13548google scholar: lookup
  124. 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.
    pubmed: 5531507
  125. Costa MC, Silva G, Ramos RV, Staempfli HR, Arroyo LG, Kim P, Weese JS. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses.. Vet J 2015 Jul;205(1):74-80.
    doi: 10.1016/j.tvjl.2015.03.018pubmed: 25975855google scholar: lookup
  126. Gasser RB, Chilton NB, Hoste H, Beveridge I. Rapid sequencing of rDNA from single worms and eggs of parasitic helminths.. Nucleic Acids Res 1993 May 25;21(10):2525-6.
    doi: 10.1093/nar/21.10.2525pmc: PMC309567pubmed: 8506152google scholar: lookup
  127. Courtot E, Boisseau M, Dhorne-pollet S, Serreau D, Reigner F, Basiaga M, Kuzmina T, Kuchly C, Diekmann I, Mach N. Evaluation of the nemabiome approach for the study of equine strongylid communities. bioRxiv 2022.
    doi: 10.1101/2022.07.22.501098google scholar: lookup
  128. Nielsen MK, Steuer AE, Anderson HP, Gavriliuc S, Carpenter AB, Redman EM, Gilleard JS, Reinemeyer CR, Poissant J. Shortened egg reappearance periods of equine cyathostomins following ivermectin or moxidectin treatment: morphological and molecular investigation of efficacy and species composition.. Int J Parasitol 2022 Nov;52(12):787-798.
    doi: 10.1016/j.ijpara.2022.09.003pubmed: 36244428google scholar: lookup
  129. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 2011;17:10.
  130. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing.. Nat Methods 2013 Jan;10(1):57-9.
    doi: 10.1038/nmeth.2276pmc: PMC3531572pubmed: 23202435google scholar: lookup
  131. Nielsen MK, von Samson-Himmelstjerna G, Kuzmina TA, van Doorn DCK, Meana A, Rehbein S, Elliott T, Reinemeyer CR. World association for the advancement of veterinary parasitology (WAAVP): Third edition of guideline for evaluating the efficacy of equine anthelmintics.. Vet Parasitol 2022 Mar;303:109676.
    doi: 10.1016/j.vetpar.2022.109676pubmed: 35164972google scholar: lookup
  132. Ushio M, Hsieh CH, Masuda R, Deyle ER, Ye H, Chang CW, Sugihara G, Kondoh M. Fluctuating interaction network and time-varying stability of a natural fish community.. Nature 2018 Feb 15;554(7692):360-363.
    doi: 10.1038/nature25504pubmed: 29414940google scholar: lookup
  133. Mohr S, Liew CC. The peripheral-blood transcriptome: new insights into disease and risk assessment.. Trends Mol Med 2007 Oct;13(10):422-32.
    doi: 10.1016/j.molmed.2007.08.003pubmed: 17919976google scholar: lookup
  134. Hoffman GE, Roussos P. Dream: powerful differential expression analysis for repeated measures designs.. Bioinformatics 2021 Apr 19;37(2):192-201.
  135. Xiao Y, Hsiao TH, Suresh U, Chen HI, Wu X, Wolf SE, Chen Y. A novel significance score for gene selection and ranking.. Bioinformatics 2014 Mar 15;30(6):801-7.
  136. Kolberg L, Raudvere U, Kuzmin I, Vilo J, Peterson H. gprofiler2 -- an R package for gene list functional enrichment analysis and namespace conversion toolset g:Profiler.. F1000Res 2020;9.

Citations

This article has been cited 1 times.
  1. 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, von Samson-Himmelstjerna G, Mach N, Sallé G. Comparison of two molecular barcodes for the study of equine strongylid communities with amplicon sequencing.. PeerJ 2023;11:e15124.
    doi: 10.7717/peerj.15124pubmed: 37070089google scholar: lookup