Analyze Diet
Animals : an open access journal from MDPI2021; 11(3); doi: 10.3390/ani11030755

A Comparison of the Colonic Microbiome and Volatile Organic Compound Metabolome of Anoplocephala perfoliata Infected and Non-Infected Horses: A Pilot Study.

Abstract: Anoplocephala perfoliata is a common equine tapeworm associated with an increased risk of colic (abdominal pain) in horses. Identification of parasite and intestinal microbiota interactions have consequences for understanding the mechanisms behind parasite-associated colic and potential new methods for parasite control. A. perfoliata was diagnosed by counting of worms in the caecum post-mortem. Bacterial DNA was extracted from colonic contents and sequenced targeting of the 16S rRNA gene (V4 region). The volatile organic compound (VOC) metabolome of colonic contents was characterised using gas chromatography mass spectrometry. Bacterial diversity (alpha and beta) was similar between tapeworm infected and non-infected controls. Some compositional differences were apparent with down-regulation of operational taxonomic units (OTUs) belonging to the symbiotic families of Ruminococcaceae and Lachnospiraceae in the tapeworm-infected group. Overall tapeworm burden accounted for 7-8% of variation in the VOC profile (permutational multivariate analysis of variance). Integration of bacterial OTUs and VOCs demonstrated moderate to strong correlations indicating the potential of VOCs as markers for bacterial OTUs in equine colonic contents. This study has shown potential differences in the intestinal microbiome and metabolome of A. perfoliata infected and non-infected horses. This pilot study did not control for extrinsic factors including diet, disease history and stage of infection.
Publication Date: 2021-03-09 PubMed ID: 33803473PubMed Central: PMC7999024DOI: 10.3390/ani11030755Google 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.

This study aims to compare the colonic microbiome and metabolome of horses infected with the common equine tapeworm, Anoplocephala perfoliata, with those of non-infected horses for better understanding of parasite-associated colic and possible measures for controlling the parasite.

Methodology

  • Diagnosis of Anoplocephala perfoliata infection was done by counting the number of worms in the horse’s caecum post-mortem.
  • Bacterial DNA was extracted from the colonic contents and sequenced, specifically targeting the V4 region of the 16S rRNA gene.
  • The volatile organic compound (VOC) metabolome of the colonic contents was characterised using gas chromatography mass spectrometry.

Results

  • There were similar bacterial diversities for both the tapeworm-infected horses and the non-infected ones. However, there were some compositional differences, with the symbiotic families of Ruminococcaceae and Lachnospiraceae being down-regulated in the infected group.
  • Tapeworm burden accounted for around 7-8% of the variation in the VOC profile. The integration of bacterial OTUs (operational taxonomic units) and VOCs displayed moderate to strong correlations, suggesting the potential of VOCs as markers for bacterial OTUs in equine colonic contents.

Conclusion

  • The research showed potential differences in the intestinal microbiome and metabolome between Anoplocephala perfoliata infected and non-infected horses. However, the pilot study did not control for external factors like diet, disease history and stage of infection, which may have had an influence on the results.
  • Understanding the interactions between parasite and intestinal microbiota can aid in understanding mechanisms behind parasite-associated colic in horses, and potentially give rise to new methods for parasite control.

Cite This Article

APA
Slater R, Frau A, Hodgkinson J, Archer D, Probert C. (2021). A Comparison of the Colonic Microbiome and Volatile Organic Compound Metabolome of Anoplocephala perfoliata Infected and Non-Infected Horses: A Pilot Study. Animals (Basel), 11(3). https://doi.org/10.3390/ani11030755

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 11
Issue: 3

Researcher Affiliations

Slater, Rachael
  • Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Crown Street, Liverpool L69 3GE, UK.
Frau, Alessandra
  • Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Crown Street, Liverpool L69 3GE, UK.
Hodgkinson, Jane
  • Institute of Infection, Veterinary and Ecological Science, University of Liverpool, Leahurst Campus, Chester High Road, Wirral CH64 7TE, UK.
Archer, Debra
  • Institute of Infection, Veterinary and Ecological Science, University of Liverpool, Leahurst Campus, Chester High Road, Wirral CH64 7TE, UK.
Probert, Chris
  • Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Crown Street, Liverpool L69 3GE, UK.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 84 references
  1. Tomczuk K, Kostro K, Szczepaniak KO, Grzybek M, Studzińska M, Demkowska-Kutrzepa M, Roczeń-Karczmarz M. Comparison of the sensitivity of coprological methods in detecting Anoplocephala perfoliata invasions.. Parasitol. Res. 2014;113:2401–2406.
    doi: 10.1007/s00436-014-3919-4pmc: PMC4031382pubmed: 24777342google scholar: lookup
  2. 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;50:125–132.
    doi: 10.1016/j.ijpara.2019.11.004pubmed: 31981673google scholar: lookup
  3. Owen RA, Jagger DW, Quan-Taylor R. Caecal intussusceptions in horses and the significance of Anoplocephala perfoliata.. Vet. Rec. 1989;124:34–37.
    doi: 10.1136/vr.124.2.34pubmed: 2644733google scholar: lookup
  4. Proudman CJ, French NP, Trees AJ. Tapeworm infection is a significant risk factor for spasmodic colic and ileal impaction colic in the horse.. Equine Vet. J. 1998;30:194–199.
  5. Proudman CJ, Holdstock NB. Investigation of an outbreak of tapeworm-associated colic in a training yard.. Equine Vet. J. 2000;32:37–41.
  6. Ryu SH, Bak UB, Kim JG, Yoon HJ, Seo HS, Kim JT, Park JY, Lee CW. Cecal rupture by Anoplocephala perfoliata infection in a thoroughbred horse in Seoul Race Park, South Korea.. J. Vet. Sci. 2001;2:189–193.
    doi: 10.4142/jvs.2001.2.3.189pubmed: 12441687google scholar: lookup
  7. Boswinkel M, Sloet van Oldruitenborgh-Oosterbann M. Correlation between colic and antibody levels against Anoplocephala perfoliata in horses in The Netherlands.. Tijdschr. Diergeneeskd. 2007;132:508–512.
    pubmed: 17649747
  8. Nielsen M, Reinemeyer C, Donecker J, Leathwick D, Marchiondo A, Kaplan R. Anthelmintic resistance in equine parasites—Current evidence and knowledge gaps.. Vet. Parasitol. 2014;204:55–63.
    doi: 10.1016/j.vetpar.2013.11.030pubmed: 24433852google scholar: lookup
  9. Nielsen MK. Equine tapeworm infections: Disease, diagnosis and control.. Equine Vet. Educ. 2015;28:388–395.
    doi: 10.1111/eve.12394google scholar: lookup
  10. Lyons E, Bellaw J, Dorton A, Tolliver S. Efficacy of moxidectin and an ivermectin-praziquantel combination against ascarids, strongyles, and tapeworms in Thoroughbred yearlings in field tests on a farm in Central Kentucky in 2016.. Vet. Parasitol. Reg. Stud. Rep. 2017;8:123–126.
    doi: 10.1016/j.vprsr.2017.03.006pubmed: 31014628google scholar: lookup
  11. Lightbody KL, Davis PJ, Austin CJ. Validation of a novel saliva-based ELISA test for diagnosing tapeworm burden in horses.. Vet. Clin. Pathol. 2016;45:335–346.
    doi: 10.1111/vcp.12364pubmed: 27218436google scholar: lookup
  12. Proudman C, Trees A. Use of excretory/secretory antigens for the serodiagnosis of Anoplocephala perfoliata cestodosis.. Vet. Parasitol. 1996;61:239–247.
    doi: 10.1016/0304-4017(95)00837-3pubmed: 8720562google scholar: lookup
  13. Abbott JB, Mellor DJ, Barrett EJ, Proudman CJ, Love S. Serological changes observed in horses infected with Anoplocephala perfoliata after treatment with praziquantel and natural reinfection.. Vet. Rec. 2008;162:50–53.
    doi: 10.1136/vr.162.2.50pubmed: 18192657google scholar: lookup
  14. Proudman C, Trees A. Correlation of antigen specific IgG and IgG(T) responses with Anoplocephala perfoliata infection intensity in the horse.. Parasite Immunol. 1996;18:499–506.
  15. Proudman C, Edwards G. Validation of a centrifugation/floatation technique for the diagnosis of equine cestodiasis.. Vet. Rec. 1992;131:71–72.
    doi: 10.1136/vr.131.4.71pubmed: 1529504google scholar: lookup
  16. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species.. Physiol. Rev. 1990;70:567–590.
    doi: 10.1152/physrev.1990.70.2.567pubmed: 2181501google scholar: lookup
  17. Daly K, Stewart CS, Flint HJ, Shirazi-Beechey SP. Bacterial diversity within the equine large intestine as revealed by molecular analysis of cloned 16S rRNA genes.. FEMS Microbiol. Ecol. 2001;38:141–151.
  18. 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;5:522–532.
    doi: 10.4161/gmic.32155pmc: PMC4822684pubmed: 25144609google scholar: lookup
  19. Zaiss MM, Harris NL. Interactions between the intestinal microbiome and helminth parasites.. Parasite Immunol. 2016;38:5–11.
    doi: 10.1111/pim.12274pmc: PMC5019230pubmed: 26345715google scholar: lookup
  20. Brosschot TP, Reynolds LA. The impact of a helminth-modified microbiome on host immunity.. Mucosal Immunol. 2018;11:1039–1046.
    doi: 10.1038/s41385-018-0008-5pubmed: 29453411google scholar: lookup
  21. 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
  22. Peachey L, Molena R, Jenkins T, Di Cesare A, Traversa D, Hodgkinson J, Cantacessi C. The relationships between faecal egg counts and gut microbial composition in UK Thoroughbreds infected by cyathostomins.. Int. J. Parasitol. 2018;48:403–412.
  23. 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;9:11121.
    doi: 10.1038/s41598-019-47204-6pmc: PMC6668452pubmed: 31366962google scholar: lookup
  24. 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;49:489–500.
    doi: 10.1016/j.ijpara.2019.02.003pubmed: 30986403google scholar: lookup
  25. 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;2:1–14.
    doi: 10.1186/s42523-020-00056-2pmc: PMC7807906pubmed: 33499996google scholar: lookup
  26. Korpi A, Järnberg J, Pasanen AL. Microbial volatile organic compounds.. Crit. Rev. Toxicol. 2009;39:139–193.
    doi: 10.1080/10408440802291497pubmed: 19204852google scholar: lookup
  27. Proudman C, Hunter JO, Darby AC, Escalona EE, Batty C, Turner C. Characterisation of the faecal metabolome and microbiome of Thoroughbred racehorses.. Equine Vet. J. 2014;47:580–586.
    doi: 10.1111/evj.12324pubmed: 25041526google scholar: lookup
  28. Salem SE, Hough R, Probert C, Maddox TW, Antczak P, Ketley JM, Williams NJ, Stoneham SJ, Archer DC. A longitudinal study of the faecal microbiome and metabolome of periparturient mares.. PeerJ. 2019;7:e6687.
    doi: 10.7717/peerj.6687pmc: PMC6451438pubmed: 30976468google scholar: lookup
  29. Walshe N, Mulcahy G, Hodgkinson J, Peachey L. No Worm is an island; the influence of commensal gut microbiota on cyathostomin infections.. Animals. 2020;10:2309.
    doi: 10.3390/ani10122309pmc: PMC7762139pubmed: 33291496google scholar: lookup
  30. Costa M, Silva G, Ramos R, Staempfli H, Arroyo L, Kim P, Weese J. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses.. Vet. J. 2015;205:74–80.
    doi: 10.1016/j.tvjl.2015.03.018pubmed: 25975855google scholar: lookup
  31. 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;82:642–652.
  32. Pearson GR, Davies LW, White AL, O’Brien JK. Pathological lesions associated with Anoplocephala perfoliata at the ileo-caecal junction of horses.. Vet. Rec. 1993;132:179–182.
    doi: 10.1136/vr.132.8.179pubmed: 8451801google scholar: lookup
  33. Christie M, Jackson F. Specific identification of strongyle eggs in small samples of sheep faeces.. Res. Vet. Sci. 1982;32:113–117.
    doi: 10.1016/S0034-5288(18)32448-2pubmed: 7201151google scholar: lookup
  34. Blackmore TM, Dugdale A, Argo CM, Curtis G, Pinloche E, Harris PA, Worgan HJ, Girdwood SE, Dougal K, Newbold CJ. Strong stability and host specific bacterial community in faeces of ponies.. PLoS ONE. 2013;8:e75079.
  35. D’Amore R, Ijaz UZ, Schirmer M, Kenny JG, Gregory R, Darby AC, Shakya M, Podar M, Quince C, Hall N. A comprehensive benchmarking study of protocols and sequencing platforms for 16S rRNA community profiling.. BMC Genom. 2016;17:55.
    doi: 10.1186/s12864-015-2194-9pmc: PMC4712552pubmed: 26763898google scholar: lookup
  36. Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N. Examining the global distribution of dominant archaeal populations in soil.. ISME J. 2010;5:908–917.
    doi: 10.1038/ismej.2010.171pmc: PMC3105767pubmed: 21085198google scholar: lookup
  37. Hough R, Archer D, Probert C. A comparison of sample preparation methods for extracting volatile organic compounds (VOCs) from equine faeces using HS-SPME.. Metabolomics. 2018;14:19.
    doi: 10.1007/s11306-017-1315-7pmc: PMC5754382pubmed: 29367839google scholar: lookup
  38. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads.. EMBnet J. 2011;17:10–12.
    doi: 10.14806/ej.17.1.200google scholar: lookup
  39. . Sickle: A Sliding-Window, Adaptive, Quality-Based Trimming Tool for FastQ Files.. .
  40. Mahé F, Rognes T, Quince C, De Vargas C, Dunthorn M. Swarm v2: Highly-scalable and high-resolution amplicon clustering.. PeerJ. 2015;3:e1420.
    doi: 10.7717/peerj.1420pmc: PMC4690345pubmed: 26713226google scholar: lookup
  41. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. Uchime improves sensitivity and speed of chimera detection.. Bioinformatics. 2011;27:2194–2200.
  42. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI. QIIME allows analysis of high-throughput community sequencing data.. Nat. Methods. 2010;7:335–336.
    doi: 10.1038/nmeth.f.303pmc: PMC3156573pubmed: 20383131google scholar: lookup
  43. Edgar RC. Search and clustering orders of magnitude faster than BLAST.. Bioinformatics. 2010;26:2460–2461.
    doi: 10.1093/bioinformatics/btq461pubmed: 20709691google scholar: lookup
  44. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools.. Nucleic Acids Res. 2012;41:590–596.
    doi: 10.1093/nar/gks1219pmc: PMC3531112pubmed: 23193283google scholar: lookup
  45. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: A fexible tool for aligning sequences to a template alignment.. Bioinformatics. 2010;26:266–267.
  46. Price MN, Dehal PS, Arkin AP. FastTree 2—Approximately maximum-likelihood trees for large alignments.. PLoS ONE. 2010;5:e9490.
  47. Ijaz UZ, Sivaloganathan L, McKenna A, Richmond A, Kelly C, Linton M, Stratakos AC, Lavery U, Elmi A, Wren BW. Comprehensive longitudinal microbiome analysis of the chicken cecum reveals a shift from competitive to environmental drivers and a window of opportunity for campylobacter.. Front. Microbiol. 2018;9:2452.
    doi: 10.3389/fmicb.2018.02452pmc: PMC6196313pubmed: 30374341google scholar: lookup
  48. Oksanen J, Blanchet F, Kindt R, Legendre P, Michen P, O’Hara R, Simpson G, Solymos P, Stevens M, Wagner H. Vegan: Ordination Methods, Diversity Analysis and Other Functions for Community and Vegetation Ecologists.. .
  49. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol. 2014;15:550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  50. Aggio R, Villas-Bôas SG, Ruggiero K. Metab: An R package for high-throughput analysis of metabolomics data generated by GC-MS.. Bioinformatics. 2011;27:2316–2318.
    doi: 10.1093/bioinformatics/btr379pubmed: 21697128google scholar: lookup
  51. 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;13:e1005752.
  52. Steelman SM, Chowdhary BP, Dowd S, Suchodolski J, Janečka JE. Pyrosequencing of 16S rRNA genes in fecal samples reveals high diversity of hindgut microflora in horses and potential links to chronic laminitis.. BMC Vet. Res. 2012;8:231.
    doi: 10.1186/1746-6148-8-231pmc: PMC3538718pubmed: 23186268google scholar: lookup
  53. 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. 2014;47:641–649.
    doi: 10.1111/evj.12361pubmed: 25257320google scholar: lookup
  54. Duarte AM, Jenkins TP, Latrofa MS, Giannelli A, Papadopoulos E, De Carvalho LM, Nolan MJ, Otranto D, Cantacessi C. Helminth infections and gut microbiota—A feline perspective.. Parasites Vectors. 2016;9:625.
    doi: 10.1186/s13071-016-1908-4pmc: PMC5135779pubmed: 27912797google scholar: lookup
  55. 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;6:20606.
    doi: 10.1038/srep20606pmc: PMC4757478pubmed: 26853110google scholar: lookup
  56. Šlapeta J, Dowd SE, Alanazi AD, Westman ME, Brown GK. Differences in the faecal microbiome of non-diarrhoeic clinically healthy dogs and cats associated with Giardia duodenalis infection: Impact of hookworms and coccidia.. Int. J. Parasitol. 2015;45:585–594.
    doi: 10.1016/j.ijpara.2015.04.001pubmed: 25934152google scholar: lookup
  57. 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:e24417.
  58. 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:e0125945.
  59. 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;8:12072.
    doi: 10.1038/s41598-018-30412-xpmc: PMC6089957pubmed: 30104612google scholar: lookup
  60. 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:e0159770.
  61. Arrazuria R, Elguezabal N, Juste RA, Derakhshani H, Khafipour E. Mycobacterium avium subspecies paratuberculosis infection modifies gut microbiota under different dietary conditions in a rabbit model.. Front. Microbiol. 2016;7:446.
    doi: 10.3389/fmicb.2016.00446pmc: PMC4815054pubmed: 27065994google scholar: lookup
  62. 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. 2011;107:989–995.
    doi: 10.1017/S0007114511003825pubmed: 21816118google scholar: lookup
  63. Biddle AS, Stewart L, Blanchard JL, Leschine S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities.. Diversity. 2013;5:627–640.
    doi: 10.3390/d5030627google scholar: lookup
  64. Wu S, Li RW, Li W, Beshah E, Dawson HD, Urban JF. Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection.. PLoS ONE. 2012;7:e35470.
  65. Nagpal D, Prakash S, Bhat K, Singh G. Detection and comparison of Selenomonas sputigena in subgingival biofilms in chronic and aggresive periodontitis patients.. Indian Soc. Periodontol. 2016;20:286–291.
    pmc: PMC4976549pubmed: 27563202
  66. Shirazi-Beechey SP. Molecular insights into dietary induced colic in the horse.. Equine Vet. J. 2008;40:414–421.
    doi: 10.2746/042516408X314075pubmed: 18487108google scholar: lookup
  67. Williamson R, Gasser R, Middleton D, Beveridge I. The distribution of Anoplocephala perfoliata in the intestine of the horse and associated pathological changes.. Vet. Parasitol. 1997;73:225–241.
    doi: 10.1016/S0304-4017(97)00123-4pubmed: 9477509google scholar: lookup
  68. Barrett EJ, Blair CW, Farlam J, Proudman CJ. Postdosing colic and diarrhoea in horses with serological evidence of tapeworm infection.. Vet. Rec. 2005;156:252–253.
    doi: 10.1136/vr.156.8.252pubmed: 15751572google scholar: lookup
  69. Dougal K, De La Fuente G, Harris PA, Girdwood SE, Pinloche E, Geor RJ, Nielsen BD, Schott HC, 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:e87424.
  70. Yamano H, Koike S, Kobayashi Y, Hata H. Phylogenetic analysis of hindgut microbiota in Hokkaido native horses compared to light horses.. Anim. Sci. J. 2008;79:234–242.
  71. 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;11:19.
    doi: 10.1186/s12917-015-0335-7pmc: PMC4323147pubmed: 25644524google scholar: lookup
  72. Schirmer M, Franzosa EA, Lloyd-Price J, McIver LJ, Schwager R, Poon TW, Ananthakrishnan AN, Andrews E, Barron G, Lake K. Dynamics of metatranscription in the inflammatory bowel disease gut microbiome.. Nat. Microbiol. 2018;3:337–346.
    doi: 10.1038/s41564-017-0089-zpmc: PMC6131705pubmed: 29311644google scholar: lookup
  73. De Raad M, Fischer CR, Northen TR. High-throughput platforms for metabolomics.. Curr. Opin. Chem. Biol. 2016;30:7–13.
    doi: 10.1016/j.cbpa.2015.10.012pubmed: 26544850google scholar: lookup
  74. Gromski PS, Muhamadali H, Ellis DI, Xu Y, Correa E, Turner ML, Goodacre R. A tutorial review: Metabolomics and partial least squares-discriminant analysis—a marriage of convenience or a shotgun wedding.. Anal. Chim. Acta. 2015;879:10–23.
    doi: 10.1016/j.aca.2015.02.012pubmed: 26002472google scholar: lookup
  75. Bijlsma S, Bobeldijk I, Verheij ER, Ramaker R, Kochhar S, Macdonald IA, Van Ommen B, Smilde AK. Large-scale human metabolomics studies: A strategy for data (pre-) processing and validation.. Anal. Chem. 2006;78:567–574.
    doi: 10.1021/ac051495jpubmed: 16408941google scholar: lookup
  76. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, Rostron T, Cerundolo V, Pamer EG, Abramson SB. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis.. eLife. 2013;2:e01202.
    doi: 10.7554/eLife.01202pmc: PMC3816614pubmed: 24192039google scholar: lookup
  77. Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, Peaper DR, Bertin J, Eisenbarth SC, Gordon JI. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis.. Cell. 2011;145:745–757.
    doi: 10.1016/j.cell.2011.04.022pmc: PMC3140910pubmed: 21565393google scholar: lookup
  78. Effmert U, Kalderás J, Warnke R, Piechulla B. Volatile mediated interactions between bacteria and fungi in the soil.. J. Chem. Ecol. 2012;38:665–703.
    doi: 10.1007/s10886-012-0135-5pubmed: 22653567google scholar: lookup
  79. Hertel M, Hartwig S, Schütte E, Gillissen B, Preissner R, Schmidt-Westhausen AM, Paris S, Kastner I, Preissner S. Identification of signature volatiles to discriminate Candida albicans, glabrata, krusei and tropicalis using gas chromatography and mass spectrometry.. Mycoses. 2016;59:117–126.
    doi: 10.1111/myc.12442pubmed: 26667499google scholar: lookup
  80. Hoffmann C, Dollive S, Grunberg S, Chen J, Li H, Wu GD, Lewis JD, Bushman FD. Archaea and fungi of the human gut microbiome: Correlations with diet and bacterial residents.. PLoS ONE. 2013;8:e66019.
  81. Nielsen M, Baptiste K, Tolliver S, Collins S, Lyons E. 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;174:77–84.
    doi: 10.1016/j.vetpar.2010.08.007pubmed: 20850927google scholar: lookup
  82. Dowdall SMJ, Matthews JB, Mair T, Murphy D, Love S, Proudman CJ. Antigen-specific IgG(T) responses in natural and experimental cyathostominae infection in horses.. Vet. Parasitol. 2002;106:225–242.
    doi: 10.1016/S0304-4017(02)00085-7pubmed: 12062511google scholar: lookup
  83. Tzelos T, Geyer KK, Mitchell MC, McWilliam HEG, Kharchenko VO, Burgess STG, Matthews JB. Characterisation of serum IgG(T) responses to potential diagnostic antigens for equine cyathostominosis.. Int. J. Parasitol. 2020;50:289–298.
    doi: 10.1016/j.ijpara.2020.01.004pubmed: 32171845google scholar: lookup
  84. 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;33:619–632.
    doi: 10.1016/j.pt.2017.04.004pubmed: 28506779google scholar: lookup