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Scientific reports2019; 9(1); 11121; doi: 10.1038/s41598-019-47204-6

Dysbiosis associated with acute helminth infections in herbivorous youngstock – observations and implications.

Abstract: A plethora of data points towards a role of the gastrointestinal (GI) microbiota of neonatal and young vertebrates in supporting the development and regulation of the host immune system. However, knowledge of the impact that infections by GI helminths exert on the developing microbiota of juvenile hosts is, thus far, limited. This study investigates, for the first time, the associations between acute infections by GI helminths and the faecal microbial and metabolic profiles of a cohort of equine youngstock, prior to and following treatment with parasiticides (ivermectin). We observed that high versus low parasite burdens (measured via parasite egg counts in faecal samples) were associated with specific compositional alterations of the developing microbiome; in particular, the faecal microbiota of animals with heavy worm infection burdens was characterised by lower microbial richness, and alterations to the relative abundances of bacterial taxa with immune-modulatory functions. Amino acids and glucose were increased in faecal samples from the same cohort, which indicated the likely occurrence of intestinal malabsorption. These data support the hypothesis that GI helminth infections in young livestock are associated with significant alterations to the GI microbiota, which may impact on both metabolism and development of acquired immunity. This knowledge will direct future studies aimed to identify the long-term impact of infection-induced alterations of the GI microbiota in young livestock.
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Publication Date: 2019-07-31 PubMed ID: 31366962PubMed Central: PMC6668452DOI: 10.1038/s41598-019-47204-6Google 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.

This study investigates the impact of gastrointestinal (GI) helminths infections on the gut microbiota of young herbivorous animals. The researchers noted that animals with higher worm infection showed noticeable changes in their gut microbiome composition and metabolism which could potentially affect their immune system and overall health.

Study Overview

  • This research aimed to investigate the relationship between helminth infections and changes in the gut microbiota of young herbivorous livestock.
  • Previous research has suggested that the health and diversity of the gut microbiota can play a significant role in the development and regulation of the host’s immune system.
  • However, the effect of helminth infections on the developing gut microbiota, particularly in young animals, had not been extensively studied.

Methods and Findings

  • The researchers studied a group of young horses, examining their fecal microbial and metabolic profiles both before and after treatment with an anti-parasitic drug.
  • They found that animals with a higher worm infection showed marked alterations in the composition of their gut microbiota. Notably, these animals had a lower diversity of microorganisms present in their GI tract.
  • In addition, these animals showed changes in the relative abundance of bacterial taxa, particularly those bacteria which contribute to immune-moderating functions.
  • They also observed increased levels of amino acids and glucose in the feces of the same group of animals, suggesting the presence of intestinal malabsorption.

Implications and Future Research

  • The researchers concluded that GI helminth infections in young herbivorous livestock could significantly affect the composition of the GI microbiota, possibly impacting the formation of the host’s immune system and metabolism.
  • This conclusion provides a basis for further research on the long-term effects of helminth-induced microbiota changes, potentially leading to better prevention and treatment strategies for helminth infections in livestock.

Cite This Article

APA
Peachey LE, Castro C, Molena RA, Jenkins TP, Griffin JL, Cantacessi C. (2019). Dysbiosis associated with acute helminth infections in herbivorous youngstock – observations and implications. Sci Rep, 9(1), 11121. https://doi.org/10.1038/s41598-019-47204-6

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 9
Issue: 1
Pages: 11121
PII: 11121

Researcher Affiliations

Peachey, Laura E
  • Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom. laura.peachey@bristol.ac.uk.
  • Bristol Veterinary School, University of Bristol, Langford, United Kingdom. laura.peachey@bristol.ac.uk.
Castro, Cecilia
  • Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom.
Molena, Rebecca A
  • Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom.
Jenkins, Timothy P
  • Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom.
Griffin, Julian L
  • Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom.
Cantacessi, Cinzia
  • Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom. cc779@cam.ac.uk.

MeSH Terms

  • Animals
  • Dysbiosis / drug therapy
  • Dysbiosis / microbiology
  • Dysbiosis / parasitology
  • Feces / parasitology
  • Female
  • Gastrointestinal Microbiome / physiology
  • Helminthiasis / drug therapy
  • Helminthiasis / microbiology
  • Helminths / drug effects
  • Helminths / parasitology
  • Herbivory / physiology
  • Horses / parasitology
  • Ivermectin / pharmacology
  • Male

Grant Funding

  • MC_PC_13030 / Medical Research Council
  • MR/P01836X/1 / Medical Research Council
  • Biotechnology and Biological Sciences Research Council
  • MR/P011705/1 / Medical Research Council
  • Wellcome Trust
  • MC_UP_A090_1006 / Medical Research Council

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 111 references
  1. Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system.. Science 2016 Apr 29;352(6285):539-44.
    doi: 10.1126/science.aad9378pmc: PMC5050524pubmed: 27126036google scholar: lookup
  2. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease.. Nat Rev Immunol 2009 May;9(5):313-23.
    doi: 10.1038/nri2515pmc: PMC4095778pubmed: 19343057google scholar: lookup
  3. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease.. Physiol Rev 2010 Jul;90(3):859-904.
    doi: 10.1152/physrev.00045.2009pubmed: 20664075google scholar: lookup
  4. Stewart CJ, Ajami NJ, O'Brien JL, Hutchinson DS, Smith DP, Wong MC, Ross MC, Lloyd RE, Doddapaneni H, Metcalf GA, Muzny D, Gibbs RA, Vatanen T, Huttenhower C, Xavier RJ, Rewers M, Hagopian W, Toppari J, Ziegler AG, She JX, Akolkar B, Lernmark A, Hyoty H, Vehik K, Krischer JP, Petrosino JF. Temporal development of the gut microbiome in early childhood from the TEDDY study.. Nature 2018 Oct;562(7728):583-588.
    doi: 10.1038/s41586-018-0617-xpmc: PMC6415775pubmed: 30356187google scholar: lookup
  5. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, Khan MT, Zhang J, Li J, Xiao L, Al-Aama J, Zhang D, Lee YS, Kotowska D, Colding C, Tremaroli V, Yin Y, Bergman S, Xu X, Madsen L, Kristiansen K, Dahlgren J, Wang J. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life.. Cell Host Microbe 2015 Jun 10;17(6):852.
    doi: 10.1016/j.chom.2015.04.004pubmed: 26308884google scholar: lookup
  6. Jami E, Israel A, Kotser A, Mizrahi I. Exploring the bovine rumen bacterial community from birth to adulthood.. ISME J 2013 Jun;7(6):1069-79.
    doi: 10.1038/ismej.2013.2pmc: PMC3660679pubmed: 23426008google scholar: lookup
  7. Costa MC, Stämpfli HR, Allen-Vercoe E, Weese JS. Development of the faecal microbiota in foals.. Equine Vet J 2016 Nov;48(6):681-688.
    doi: 10.1111/evj.12532pubmed: 26518456google scholar: lookup
  8. Dong TS, Gupta A. Influence of Early Life, Diet, and the Environment on the Microbiome.. Clin Gastroenterol Hepatol 2019 Jan;17(2):231-242.
    doi: 10.1016/j.cgh.2018.08.067pmc: PMC6422042pubmed: 30196160google scholar: lookup
  9. Adami AJ, Bracken SJ, Guernsey LA, Rafti E, Maas KR, Graf J, Matson AP, Thrall RS, Schramm CM. Early-life antibiotics attenuate regulatory T cell generation and increase the severity of murine house dust mite-induced asthma.. Pediatr Res 2018 Sep;84(3):426-434.
    doi: 10.1038/s41390-018-0031-ypmc: PMC6258300pubmed: 29967529google scholar: lookup
  10. Iizumi T, Battaglia T, Ruiz V, Perez Perez GI. Gut Microbiome and Antibiotics.. Arch Med Res 2017 Nov;48(8):727-734.
    doi: 10.1016/j.arcmed.2017.11.004pubmed: 29221800google scholar: lookup
  11. Yu M, Mu C, Zhang C, Yang Y, Su Y, Zhu W. Marked Response in Microbial Community and Metabolism in the Ileum and Cecum of Suckling Piglets After Early Antibiotics Exposure.. Front Microbiol 2018;9:1166.
    doi: 10.3389/fmicb.2018.01166pmc: PMC5989621pubmed: 29899739google scholar: lookup
  12. Sylvia KE, Deyoe JE, Demas GE. Early-life sickness may predispose Siberian hamsters to behavioral changes following alterations of the gut microbiome in adulthood.. Brain Behav Immun 2018 Oct;73:571-583.
    doi: 10.1016/j.bbi.2018.07.001pmc: PMC6607895pubmed: 29981426google scholar: lookup
  13. Schokker D, Zhang J, Vastenhouw SA, Heilig HG, Smidt H, Rebel JM, Smits MA. Long-lasting effects of early-life antibiotic treatment and routine animal handling on gut microbiota composition and immune system in pigs.. PLoS One 2015;10(2):e0116523.
    doi: 10.1371/journal.pone.0116523pmc: PMC4319779pubmed: 25658611google scholar: lookup
  14. Astbury S, Song A, Zhou M, Nielsen B, Hoedl A, Willing BP, Symonds ME, Bell RC. High Fructose Intake During Pregnancy in Rats Influences the Maternal Microbiome and Gut Development in the Offspring.. Front Genet 2018;9:203.
    doi: 10.3389/fgene.2018.00203pmc: PMC6018152pubmed: 29971089google scholar: lookup
  15. Berer K, Martínez I, Walker A, Kunkel B, Schmitt-Kopplin P, Walter J, Krishnamoorthy G. Dietary non-fermentable fiber prevents autoimmune neurological disease by changing gut metabolic and immune status.. Sci Rep 2018 Jul 11;8(1):10431.
    doi: 10.1038/s41598-018-28839-3pmc: PMC6041322pubmed: 29993025google scholar: lookup
  16. Davis EC, Wang M, Donovan SM. The role of early life nutrition in the establishment of gastrointestinal microbial composition and function.. Gut Microbes 2017 Mar 4;8(2):143-171.
    doi: 10.1080/19490976.2016.1278104pmc: PMC5390825pubmed: 28068209google scholar: lookup
  17. Zhou X, Du L, Shi R, Chen Z, Zhou Y, Li Z. Early-life food nutrition, microbiota maturation and immune development shape life-long health.. Crit Rev Food Sci Nutr 2019;59(sup1):S30-S38.
    doi: 10.1080/10408398.2018.1485628pubmed: 29874476google scholar: lookup
  18. Francino MP. Birth Mode-Related Differences in Gut Microbiota Colonization and Immune System Development.. Ann Nutr Metab 2018;73 Suppl 3:12-16.
    doi: 10.1159/000490842pubmed: 30041189google scholar: lookup
  19. Wang J, Zheng J, Shi W, Du N, Xu X, Zhang Y, Ji P, Zhang F, Jia Z, Wang Y, Zheng Z, Zhang H, Zhao F. Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus.. Gut 2018 Sep;67(9):1614-1625.
    doi: 10.1136/gutjnl-2018-315988pmc: PMC6109274pubmed: 29760169google scholar: lookup
  20. Zimmermann P, Curtis N. Factors Influencing the Intestinal Microbiome During the First Year of Life.. Pediatr Infect Dis J 2018 Dec;37(12):e315-e335.
    doi: 10.1097/INF.0000000000002103pubmed: 29746379google scholar: lookup
  21. Valentine G, Chu DM, Stewart CJ, Aagaard KM. Relationships Between Perinatal Interventions, Maternal-Infant Microbiomes, and Neonatal Outcomes.. Clin Perinatol 2018 Jun;45(2):339-355.
    doi: 10.1016/j.clp.2018.01.00pubmed: 29747892google scholar: lookup
  22. Lundgren SN, Madan JC, Emond JA, Morrison HG, Christensen BC, Karagas MR, Hoen AG. Maternal diet during pregnancy is related with the infant stool microbiome in a delivery mode-dependent manner.. Microbiome 2018 Jul 5;6(1):109.
    doi: 10.1186/s40168-018-0490-8pmc: PMC6033232pubmed: 29973274google scholar: lookup
  23. Robertson RC, Kaliannan K, Strain CR, Ross RP, Stanton C, Kang JX. Maternal omega-3 fatty acids regulate offspring obesity through persistent modulation of gut microbiota.. Microbiome 2018 May 24;6(1):95.
    doi: 10.1186/s40168-018-0476-6pmc: PMC5968592pubmed: 29793531google scholar: lookup
  24. Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low gut microbiota diversity in early infancy precedes asthma at school age.. Clin Exp Allergy 2014 Jun;44(6):842-50.
    doi: 10.1111/cea.12253pubmed: 24330256google scholar: lookup
  25. Sozańska B. Microbiome in the primary prevention of allergic diseases and bronchial asthma.. Allergol Immunopathol (Madr) 2019 Jan-Feb;47(1):79-84.
    doi: 10.1016/j.aller.2018.03.005,pubmed: 29980403google scholar: lookup
  26. Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema.. J Allergy Clin Immunol 2012 Feb;129(2):434-40, 440.e1-2.
    doi: 10.1016/j.jaci.2011.10.025pubmed: 22153774google scholar: lookup
  27. Knutie SA, Wilkinson CL, Kohl KD, Rohr JR. Early-life disruption of amphibian microbiota decreases later-life resistance to parasites.. Nat Commun 2017 Jul 20;8(1):86.
    doi: 10.1038/s41467-017-00119-0pmc: PMC5519754pubmed: 28729558google scholar: lookup
  28. Bernstein CN, Burchill C, Targownik LE, Singh H, Roos LL. Events Within the First Year of Life, but Not the Neonatal Period, Affect Risk for Later Development of Inflammatory Bowel Diseases.. Gastroenterology 2019 Jun;156(8):2190-2197.e10.
    doi: 10.1053/j.gastro.2019.02.004pmc: PMC7094443pubmed: 30772341google scholar: lookup
  29. Ismail IH, Oppedisano F, Joseph SJ, Boyle RJ, Licciardi PV, Robins-Browne RM, Tang ML. Reduced gut microbial diversity in early life is associated with later development of eczema but not atopy in high-risk infants.. Pediatr Allergy Immunol 2012 Nov;23(7):674-81.
    doi: 10.1111/j.1399-3038.2012.01328.xpubmed: 22831283google scholar: lookup
  30. Korpela K, de Vos WM. Early life colonization of the human gut: microbes matter everywhere.. Curr Opin Microbiol 2018 Aug;44:70-78.
    doi: 10.1016/j.mib.2018.06.003pubmed: 30086431google scholar: lookup
  31. Broadhurst MJ, Ardeshir A, Kanwar B, Mirpuri J, Gundra UM, Leung JM, Wiens KE, Vujkovic-Cvijin I, Kim CC, Yarovinsky F, Lerche NW, McCune JM, Loke P. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon.. PLoS Pathog 2012;8(11):e1003000.
    doi: 10.1371/journal.ppat.1003000pmc: PMC3499566pubmed: 23166490google scholar: lookup
  32. Cattadori IM, Sebastian A, Hao H, Katani R, Albert I, Eilertson KE, Kapur V, Pathak A, Mitchell S. Impact of Helminth Infections and Nutritional Constraints on the Small Intestine Microbiota.. PLoS One 2016;11(7):e0159770.
    doi: 10.1371/journal.pone.0159770pmc: PMC4954658pubmed: 27438701google scholar: lookup
  33. Glendinning L, Nausch N, Free A, Taylor DW, Mutapi F. The microbiota and helminths: sharing the same niche in the human host.. Parasitology 2014 Sep;141(10):1255-71.
    doi: 10.1017/S0031182014000699pubmed: 24901211google scholar: lookup
  34. 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
  35. 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
  36. 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.
    doi: 10.1371/journal.pone.0125945pmc: PMC4418675pubmed: 25938477google scholar: lookup
  37. 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
  38. Dea-Ayuela MA, Rama-Iñiguez S, Bolás-Fernandez F. Enhanced susceptibility to Trichuris muris infection of B10Br mice treated with the probiotic Lactobacillus casei.. Int Immunopharmacol 2008 Jan;8(1):28-35.
    doi: 10.1016/j.intimp.2007.10.003pubmed: 18068097google scholar: lookup
  39. 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.
    doi: 10.1371/journal.pntd.0002880pmc: PMC4031128pubmed: 24851867google scholar: lookup
  40. 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.
    doi: 10.1016/j.ijpara.2017.11.003pmc: PMC5946844pubmed: 29432771google scholar: lookup
  41. Jenkins TP, Peachey LE, Ajami NJ, MacDonald AS, Hsieh MH, Brindley PJ, Cantacessi C, Rinaldi G. Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota.. Sci Rep 2018 Aug 13;8(1):12072.
    doi: 10.1038/s41598-018-30412-xpmc: PMC6089957pubmed: 30104612google scholar: lookup
  42. Jenkins TP, Formenti F, Castro C, Piubelli C, Perandin F, Buonfrate D, Otranto D, Griffin JL, Krause L, Bisoffi Z, Cantacessi C. A comprehensive analysis of the faecal microbiome and metabolome of Strongyloides stercoralis infected volunteers from a non-endemic area.. Sci Rep 2018 Oct 23;8(1):15651.
    doi: 10.1038/s41598-018-33937-3pmc: PMC6199319pubmed: 30353019google scholar: lookup
  43. 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.
    doi: 10.1371/journal.pone.0125495pmc: PMC4420551pubmed: 25942314google scholar: lookup
  44. McNeilly TN, Nisbet AJ. Immune modulation by helminth parasites of ruminants: implications for vaccine development and host immune competence.. Parasite 2014;21:51.
    doi: 10.1051/parasite/2014051pmc: PMC4189095pubmed: 25292481google scholar: lookup
  45. Ridler A. Disease threats to sheep associated with intensification of pastoral farming.. N Z Vet J 2008 Dec;56(6):270-3.
    doi: 10.1080/00480169.2008.36846pubmed: 19043463google scholar: lookup
  46. 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
  47. 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.
    doi: 10.1371/journal.pone.0024417pmc: PMC3170331pubmed: 21931709google scholar: lookup
  48. El-Ashram S, Al Nasr I, Abouhajer F, El-Kemary M, Huang G, Dinçel G, Mehmood R, Hu M, Suo X. Microbial community and ovine host response varies with early and late stages of Haemonchus contortus infection.. Vet Res Commun 2017 Dec;41(4):263-277.
    doi: 10.1007/s11259-017-9698-5pubmed: 29098532google scholar: lookup
  49. Almeida ML, Feringer WH Júnior, Carvalho JR, Rodrigues IM, Jordão LR, Fonseca MG, Carneiro de Rezende AS, de Queiroz Neto A, Weese JS, Costa MC, Lemos EG, Ferraz GC. Intense Exercise and Aerobic Conditioning Associated with Chromium or L-Carnitine Supplementation Modified the Fecal Microbiota of Fillies.. PLoS One 2016;11(12):e0167108.
    doi: 10.1371/journal.pone.0167108pmc: PMC5147854pubmed: 27935992google scholar: lookup
  50. Blackmore TM, Dugdale A, Argo CM, Curtis G, Pinloche E, Harris PA, Worgan HJ, Girdwood SE, Dougal K, Newbold CJ, McEwan NR. Strong stability and host specific bacterial community in faeces of ponies.. PLoS One 2013;8(9):e75079.
    doi: 10.1371/journal.pone.0075079pmc: PMC3770578pubmed: 24040388google scholar: lookup
  51. Costa MC, Arroyo LG, Allen-Vercoe E, Stämpfli HR, Kim PT, Sturgeon A, Weese JS. Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene.. PLoS One 2012;7(7):e41484.
    doi: 10.1371/journal.pone.0041484pmc: PMC3409227pubmed: 22859989google scholar: lookup
  52. 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
  53. Costa MC, Stämpfli HR, Arroyo LG, Allen-Vercoe E, Gomes RG, Weese JS. Changes in the equine fecal microbiota associated with the use of systemic antimicrobial drugs.. BMC Vet Res 2015 Feb 3;11:19.
    doi: 10.1186/s12917-015-0335-7pmc: PMC4323147pubmed: 25644524google scholar: lookup
  54. Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease.. Vet Clin North Am Equine Pract 2018 Apr;34(1):1-12.
    doi: 10.1016/j.cveq.2017.11.005pubmed: 29402480google scholar: lookup
  55. 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
  56. Daly K, Proudman CJ, Duncan SH, Flint HJ, Dyer J, Shirazi-Beechey SP. Alterations in microbiota and fermentation products in equine large intestine in response to dietary variation and intestinal disease.. Br J Nutr 2012 Apr;107(7):989-95.
    doi: 10.1017/S0007114511003825pubmed: 21816118google scholar: lookup
  57. Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Geor RJ, Nielsen BD, Schott HC 2nd, Elzinga S, Newbold CJ. Characterisation of the faecal bacterial community in adult and elderly horses fed a high fibre, high oil or high starch diet using 454 pyrosequencing.. PLoS One 2014;9(2):e87424.
    doi: 10.1371/journal.pone.0087424pmc: PMC3913607pubmed: 24504261google scholar: lookup
  58. Dougal K, Harris PA, Edwards A, Pachebat JA, Blackmore TM, Worgan HJ, Newbold CJ. A comparison of the microbiome and the metabolome of different regions of the equine hindgut.. FEMS Microbiol Ecol 2012 Dec;82(3):642-52.
    doi: 10.1111/j.1574-6941.2012.01441.xpubmed: 22757649google scholar: lookup
  59. Ericsson AC, Johnson PJ, Lopes MA, Perry SC, Lanter HR. A Microbiological Map of the Healthy Equine Gastrointestinal Tract.. PLoS One 2016;11(11):e0166523.
    doi: 10.1371/journal.pone.0166523pmc: PMC5112786pubmed: 27846295google scholar: lookup
  60. Fernandes KA, Kittelmann S, Rogers CW, Gee EK, Bolwell CF, Bermingham EN, Thomas DG. Faecal microbiota of forage-fed horses in New Zealand and the population dynamics of microbial communities following dietary change.. PLoS One 2014;9(11):e112846.
    doi: 10.1371/journal.pone.0112846pmc: PMC4226576pubmed: 25383707google scholar: lookup
  61. Leng J, Proudman C, Darby A, Blow F, Townsend N, Miller A, Swann J. Exploration of the Fecal Microbiota and Biomarker Discovery in Equine Grass Sickness.. J Proteome Res 2018 Mar 2;17(3):1120-1128.
    doi: 10.1021/acs.jproteome.7b00784pubmed: 29364680google scholar: lookup
  62. Mach N, Foury A, Kittelmann S, Reigner F, Moroldo M, Ballester M, Esquerré D, Rivière J, Sallé G, Gérard P, Moisan MP, Lansade L. The Effects of Weaning Methods on Gut Microbiota Composition and Horse Physiology.. Front Physiol 2017;8:535.
    doi: 10.3389/fphys.2017.00535pmc: PMC5524898pubmed: 28790932google scholar: lookup
  63. Metcalf JL, Song SJ, Morton JT, Weiss S, Seguin-Orlando A, Joly F, Feh C, Taberlet P, Coissac E, Amir A, Willerslev E, Knight R, McKenzie V, Orlando L. Evaluating the impact of domestication and captivity on the horse gut microbiome.. Sci Rep 2017 Nov 14;7(1):15497.
    doi: 10.1038/s41598-017-15375-9pmc: PMC5686199pubmed: 29138485google scholar: lookup
  64. Proudman CJ, Hunter JO, Darby AC, Escalona EE, Batty C, Turner C. Characterisation of the faecal metabolome and microbiome of Thoroughbred racehorses.. Equine Vet J 2015 Sep;47(5):580-6.
    doi: 10.1111/evj.12324pubmed: 25041526google scholar: lookup
  65. Schoster A, Mosing M, Jalali M, Staempfli HR, Weese JS. Effects of transport, fasting and anaesthesia on the faecal microbiota of healthy adult horses.. Equine Vet J 2016 Sep;48(5):595-602.
    doi: 10.1111/evj.12479pubmed: 26122549google scholar: lookup
  66. Schoster A, Staempfli HR, Guardabassi LG, Jalali M, Weese JS. Comparison of the fecal bacterial microbiota of healthy and diarrheic foals at two and four weeks of life.. BMC Vet Res 2017 May 30;13(1):144.
    doi: 10.1186/s12917-017-1064-xpmc: PMC5450145pubmed: 28558788google scholar: lookup
  67. 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
  68. Weese JS, Holcombe SJ, Embertson RM, Kurtz KA, Roessner HA, Jalali M, Wismer SE. Changes in the faecal microbiota of mares precede the development of post partum colic.. Equine Vet J 2015 Nov;47(6):641-9.
    doi: 10.1111/evj.12361pubmed: 25257320google scholar: lookup
  69. Zhao Y, Li B, Bai D, Huang J, Shiraigo W, Yang L, Zhao Q, Ren X, Wu J, Bao W, Dugarjaviin M. Comparison of Fecal Microbiota of Mongolian and Thoroughbred Horses by High-throughput Sequencing of the V4 Region of the 16S rRNA Gene.. Asian-Australas J Anim Sci 2016 Sep;29(9):1345-52.
    doi: 10.5713/ajas.15.0587pmc: PMC5003997pubmed: 26954132google scholar: lookup
  70. Matthews JB. Facing the threat of equine parasitic disease.. Equine Vet J 2011 Mar;43(2):126-32.
    doi: 10.1111/j.2042-3306.2010.00356.xpubmed: 21592204google scholar: lookup
  71. Love S, Murphy D, Mellor D. Pathogenicity of cyathostome infection.. Vet Parasitol 1999 Aug 31;85(2-3):113-21; discussion 121-2, 215-25.
    doi: 10.1016/S0304-4017(99)00092-8pubmed: 10485358google scholar: lookup
  72. Willing B, Vörös A, Roos S, Jones C, Jansson A, Lindberg JE. Changes in faecal bacteria associated with concentrate and forage-only diets fed to horses in training.. Equine Vet J 2009 Dec;41(9):908-14.
    doi: 10.2746/042516409X447806pubmed: 20383990google scholar: lookup
  73. Warzecha CM, Coverdale JA, Janecka JE, Leatherwood JL, Pinchak WE, Wickersham TA, McCann JC. Influence of short-term dietary starch inclusion on the equine cecal microbiome.. J Anim Sci 2017 Nov;95(11):5077-5090.
    doi: 10.2527/jas2017.1754pmc: PMC6095290pubmed: 29293739google scholar: lookup
  74. Martínez I, Maldonado-Gomez MX, Gomes-Neto JC, Kittana H, Ding H, Schmaltz R, Joglekar P, Cardona RJ, Marsteller NL, Kembel SW, Benson AK, Peterson DA, Ramer-Tait AE, Walter J. Experimental evaluation of the importance of colonization history in early-life gut microbiota assembly.. Elife 2018 Sep 18;7.
    doi: 10.7554/eLife.36521pmc: PMC6143339pubmed: 30226190google scholar: lookup
  75. de Aquino SG, Abdollahi-Roodsaz S, Koenders MI, van de Loo FA, Pruijn GJ, Marijnissen RJ, Walgreen B, Helsen MM, van den Bersselaar LA, de Molon RS, Avila Campos MJ, Cunha FQ, Cirelli JA, van den Berg WB. Periodontal pathogens directly promote autoimmune experimental arthritis by inducing a TLR2- and IL-1-driven Th17 response.. J Immunol 2014 May 1;192(9):4103-11.
    doi: 10.4049/jimmunol.1301970pubmed: 24683190google scholar: lookup
  76. Larsen JM. The immune response to Prevotella bacteria in chronic inflammatory disease.. Immunology 2017 Aug;151(4):363-374.
    doi: 10.1111/imm.12760pmc: PMC5506432pubmed: 28542929google scholar: lookup
  77. Brosschot TP, Reynolds LA. The impact of a helminth-modified microbiome on host immunity.. Mucosal Immunol 2018 Jul;11(4):1039-1046.
    doi: 10.1038/s41385-018-0008-5pubmed: 29453411google scholar: lookup
  78. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G. Environmental and gut bacteroidetes: the food connection.. Front Microbiol 2011;2:93.
    doi: 10.3389/fmicb.2011.00093pmc: PMC3129010pubmed: 21747801google scholar: lookup
  79. Ley RE. Gut microbiota in 2015: Prevotella in the gut: choose carefully.. Nat Rev Gastroenterol Hepatol 2016 Feb;13(2):69-70.
    doi: 10.1038/nrgastro.2016.4pubmed: 26828918google scholar: lookup
  80. Zhang XS, Li J, Krautkramer KA, Badri M, Battaglia T, Borbet TC, Koh H, Ng S, Sibley RA, Li Y, Pathmasiri W, Jindal S, Shields-Cutler RR, Hillmann B, Al-Ghalith GA, Ruiz VE, Livanos A, van 't Wout AB, Nagalingam N, Rogers AB, Sumner SJ, Knights D, Denu JM, Li H, Ruggles KV, Bonneau R, Williamson RA, Rauch M, Blaser MJ. Antibiotic-induced acceleration of type 1 diabetes alters maturation of innate intestinal immunity.. Elife 2018 Jul 25;7.
    doi: 10.7554/eLife.37816pmc: PMC6085123pubmed: 30039798google scholar: lookup
  81. 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
  82. 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.
    doi: 10.1126/science.aaf3229pmc: PMC4905769pubmed: 27080105google 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.
    doi: 10.1016/j.immuni.2015.09.012pmc: PMC4658337pubmed: 26522986google scholar: lookup
  84. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells.. Nature 2013 Dec 19;504(7480):446-50.
    doi: 10.1038/nature12721pubmed: 24226770google scholar: lookup
  85. Nakazawa F, Sato M, Poco SE, Hashimura T, Ikeda T, Kalfas S, Sundqvist G, Hoshino E. Description of Mogibacterium pumilum gen. nov., sp. nov. and Mogibacterium vescum gen. nov., sp. nov., and reclassification of Eubacterium timidum (Holdeman et al. 1980) as Mogibacterium timidum gen. nov., comb. nov.. Int J Syst Evol Microbiol 2000 Mar;50 Pt 2:679-688.
    doi: 10.1099/00207713-50-2-679pubmed: 10758875google scholar: lookup
  86. Lourenςo TGB, Spencer SJ, Alm EJ, Colombo APV. Defining the gut microbiota in individuals with periodontal diseases: an exploratory study.. J Oral Microbiol 2018;10(1):1487741.
    doi: 10.1080/20002297.2018.1487741pmc: PMC6032013pubmed: 29988721google scholar: lookup
  87. Heitkemper MM, Cain KC, Shulman RJ, Burr RL, Ko C, Hollister EB, Callen N, Zia J, Han CJ, Jarrett ME. Stool and urine trefoil factor 3 levels: associations with symptoms, intestinal permeability, and microbial diversity in irritable bowel syndrome.. Benef Microbes 2018 Apr 25;9(3):345-355.
    doi: 10.3920/BM2017.0059pmc: PMC6366941pubmed: 29633639google scholar: lookup
  88. Hollister EB, Cain KC, Shulman RJ, Jarrett ME, Burr RL, Ko C, Zia J, Han CJ, Heitkemper MM. Relationships of Microbiome Markers With Extraintestinal, Psychological Distress and Gastrointestinal Symptoms, and Quality of Life in Women With Irritable Bowel Syndrome.. J Clin Gastroenterol 2020 Feb;54(2):175-183.
    pmc: PMC6387862pubmed: 30148765doi: 10.1097/MCG.0000000000001107google scholar: lookup
  89. Altomare A, Putignani L, Del Chierico F, Cocca S, Angeletti S, Ciccozzi M, Tripiciano C, Dalla Piccola B, Cicala M, Guarino MPL. Gut mucosal-associated microbiota better discloses inflammatory bowel disease differential patterns than faecal microbiota.. Dig Liver Dis 2019 May;51(5):648-656.
    pubmed: 30573380doi: 10.1016/j.dld.2018.11.021google scholar: lookup
  90. 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
  91. Taylor SL, Leong LEX, Choo JM, Wesselingh S, Yang IA, Upham JW, Reynolds PN, Hodge S, James AL, Jenkins C, Peters MJ, Baraket M, Marks GB, Gibson PG, Simpson JL, Rogers GB. Inflammatory phenotypes in patients with severe asthma are associated with distinct airway microbiology.. J Allergy Clin Immunol 2018 Jan;141(1):94-103.e15.
    doi: 10.1016/j.jaci.2017.03.044pubmed: 28479329google scholar: lookup
  92. 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
  93. 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
  94. Wells JM. Immunomodulatory mechanisms of lactobacilli.. Microb Cell Fact 2011 Aug 30;10 Suppl 1(Suppl 1):S17.
    doi: 10.1186/1475-2859-10-S1-S17pmc: PMC3231924pubmed: 21995674google scholar: lookup
  95. Schoster A, Weese JS, Guardabassi L. Probiotic use in horses - what is the evidence for their clinical efficacy?. J Vet Intern Med 2014 Nov-Dec;28(6):1640-52.
    doi: 10.1111/jvim.1245pmc: PMC4895607pubmed: 25231539google scholar: lookup
  96. Knutie SA, Shea LA, Kupselaitis M, Wilkinson CL, Kohl KD, Rohr JR. Early-Life Diet Affects Host Microbiota and Later-Life Defenses Against Parasites in Frogs.. Integr Comp Biol 2017 Oct 1;57(4):732-742.
    doi: 10.1093/icb/icx028pmc: PMC5886343pubmed: 28662573google scholar: lookup
  97. Sepehri S, Kotlowski R, Bernstein CN, Krause DO. Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease.. Inflamm Bowel Dis 2007 Jun;13(6):675-83.
    doi: 10.1002/ibd.20101pubmed: 17262808google scholar: lookup
  98. Ott SJ, Schreiber S. Reduced microbial diversity in inflammatory bowel diseases.. Gut 2006 Aug;55(8):1207.
    pmc: PMC1856277pubmed: 16849351
  99. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach.. Gut 2006 Feb;55(2):205-11.
    doi: 10.1136/gut.2005.073817pmc: PMC1856500pubmed: 16188921google scholar: lookup
  100. Giacomin P, Zakrzewski M, Croese J, Su X, Sotillo J, McCann L, Navarro S, Mitreva M, Krause L, Loukas A, Cantacessi C. Experimental hookworm infection and escalating gluten challenges are associated with increased microbial richness in celiac subjects.. Sci Rep 2015 Sep 18;5:13797.
    doi: 10.1038/srep13797pmc: PMC4585380pubmed: 26381211google scholar: lookup
  101. McSorley HJ, Maizels RM. Helminth infections and host immune regulation.. Clin Microbiol Rev 2012 Oct;25(4):585-608.
    doi: 10.1128/CMR.05040-11pmc: PMC3485755pubmed: 23034321google scholar: lookup
  102. 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
  103. Goldansaz SA, Guo AC, Sajed T, Steele MA, Plastow GS, Wishart DS. Livestock metabolomics and the livestock metabolome: A systematic review.. PLoS One 2017;12(5):e0177675.
    doi: 10.1371/journal.pone.0177675pmc: PMC5439675pubmed: 28531195google scholar: lookup
  104. Christie M, Jackson F. Specific identification of strongyle eggs in small samples of sheep faeces.. Res Vet Sci 1982 Jan;32(1):113-7.
    pubmed: 7201151
  105. Rehbein S, Lindner T, Visser M, Winter R. Evaluation of a double centrifugation technique for the detection of Anoplocephala eggs in horse faeces.. J Helminthol 2011 Dec;85(4):409-14.
    doi: 10.1017/S0022149X10000751pubmed: 21138608google scholar: lookup
  106. Mattiello F, Verbist B, Faust K, Raes J, Shannon WD, Bijnens L, Thas O. A web application for sample size and power calculation in case-control microbiome studies.. Bioinformatics 2016 Jul 1;32(13):2038-40.
    doi: 10.1093/bioinformatics/btw099pubmed: 27153704google scholar: lookup
  107. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data.. Nat Methods 2010 May;7(5):335-6.
    doi: 10.1038/nmeth.f.303pmc: PMC3156573pubmed: 20383131google scholar: lookup
  108. 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
  109. Zakrzewski M, Proietti C, Ellis JJ, Hasan S, Brion MJ, Berger B, Krause L. Calypso: a user-friendly web-server for mining and visualizing microbiome-environment interactions.. Bioinformatics 2017 Mar 1;33(5):782-783.
    doi: 10.1093/bioinformatics/btw725pmc: PMC5408814pubmed: 28025202google scholar: lookup
  110. Anderson MJ, Ellingsen KE, McArdle BH. Multivariate dispersion as a measure of beta diversity.. Ecol Lett 2006 Jun;9(6):683-93.
    doi: 10.1111/j.1461-0248.2006.00926.xpubmed: 16706913google scholar: lookup
  111. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation.. Genome Biol 2011 Jun 24;12(6):R60.
    doi: 10.1186/gb-2011-12-6-r60pmc: PMC3218848pubmed: 21702898google scholar: lookup

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