Effects of hypersensitivity disorders and environmental factors on the equine intestinal microbiota.
Abstract: Recent evidence suggests that an altered intestinal microbiota, specifically a reduction of bacterial diversity or a shift in microbial composition, is associated with the development of hypersensitivity disorders in humans, but this is unknown for horses. In this study we hypothesized that horses affected by either Culicoides hypersensitivity or severe equine asthma or both show a decreased diversity of their intestinal microbiota. We also investigated environmental effects. Rectal swab samples of a total of 140 horses were collected and the owners completed a detailed questionnaire about their horse. For each allergic horse, a healthy peer from the same stable was equally sampled as an environmentally matched control. Microbiota in the swabs was determined by assessing the V4 region of the bacterial 16S rRNA gene. Structures of bacterial communities were investigated by means of alpha and beta diversity indices. Group wise comparisons between healthy and allergic horses showed no significant differences regarding alpha (p = 0.9) and beta diversity (p = 0.5). However, the microbial structure was associated with environmental factors such as the type of stable (p = 0.001), access to pasture (p = 0.001) or the type of feeding (p = 0.003). There was also a strong location effect meaning that the microbiota was more similar within the same as compared between farms within this study. Our observations suggest that hypersensitivity disorders in adult horses are not associated with an alteration of the intestinal microbiota, but environmental and/or location factors strongly influence these bacteria.
Publication Date: 2020-03-20 PubMed ID: 32189583PubMed Central: PMC7170319DOI: 10.1080/01652176.2020.1745317Google Scholar: Lookup
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- 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 research article investigates whether horses affected by hypersensitivity disorders, such as Culicoides hypersensitivity or severe equine asthma, exhibit decreased diversity in their intestinal microbiota. The study also looks into how environmental factors may impact the gut bacteria. The primary finding suggests that hypersensitivity disorders in adult horses aren’t linked to changes in the intestinal microbiota, but the environment and location have a significant influence.
Research Methodology
- The researchers conducted the study with 140 horses in total. Samples from each horse’s rectum were collected through swabs.
- For each horse with an allergic condition, a swab was also collected from a healthy horse from the same stable. These samples acted as matched environmental controls to ensure consistent variables.
- A comprehensive questionnaire was filled out by each horse owner, detailing essential specifics about their horse.
- A snapshot of the microbiota in the swabs was achieved by examining the V4 region of the bacterial 16S rRNA gene.
- The team used alpha and beta diversity indices to scrutinize the structures of bacterial communities within the samples.
Findings and Conclusion
- Comparisons between healthy and allergic horses revealed no significant differences in terms of alpha and beta diversity. This suggests that hypersensitivity disorders don’t specifically contribute to alterations in the intestinal microbiota diversity of horses.
- Nevertheless, the research demonstrated that environmental factors had a significant impact on the microbial structure.
- Aspects such as the type of stable that a horse was kept in, their access to pasture, and their feeding system, all influenced the diversity and composition of their intestinal microbiota.
- Location also played a significant role, with horses from the same farm displaying more similarity in their microbiota than between horses at different farms. It means that location specific factors can significantly influence the gut microflora of the horses.
- In conclusion, the research emphasizes the environmental influence on the intestinal microbiota than the presence of hypersensitivity disorders in horses.
Cite This Article
APA
Kaiser-Thom S, Hilty M, Gerber V.
(2020).
Effects of hypersensitivity disorders and environmental factors on the equine intestinal microbiota.
Vet Q, 40(1), 97-107.
https://doi.org/10.1080/01652176.2020.1745317 Publication
Researcher Affiliations
- Swiss Institute of Equine Medicine (ISME), Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, and Agroscope, Bern, Switzerland.
- Institute for Infectious Diseases, University of Bern, Bern, Switzerland.
- Swiss Institute of Equine Medicine (ISME), Department of Clinical Veterinary Medicine, Vetsuisse Faculty, University of Bern, and Agroscope, Bern, Switzerland.
MeSH Terms
- Animals
- Asthma / microbiology
- Asthma / veterinary
- Case-Control Studies
- Ceratopogonidae / immunology
- Environment
- Environmental Microbiology
- Farms
- Feces / microbiology
- Gastrointestinal Microbiome / genetics
- Horse Diseases / microbiology
- Horses
- Hypersensitivity / microbiology
- Hypersensitivity / veterinary
- RNA, Ribosomal, 16S / genetics
- Surveys and Questionnaires
Conflict of Interest Statement
The authors declare no competing interests.
References
This article includes 73 references
- 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.
- Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease.. Gastroenterology 2014 May;146(6):1564-72.
- Arrieta MC, Stiemsma LT, Amenyogbe N, Brown EM, Finlay B. The intestinal microbiome in early life: health and disease.. Front Immunol 2014;5:427.
- Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Müller G, Stokholm J, Smith B, Krogfelt KA. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age.. J Allergy Clin Immunol 2011 Sep;128(3):646-52.e1-5.
- Böttcher MF, Nordin EK, Sandin A, Midtvedt T, Björkstén B. Microflora-associated characteristics in faeces from allergic and nonallergic infants.. Clin Exp Allergy 2000 Nov;30(11):1590-6.
- Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis.. ISME J 2017 Dec;11(12):2639-2643.
- 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.
- Callahan BJ, Sankaran K, Fukuyama JA, McMurdie PJ, Holmes SP. Bioconductor Workflow for Microbiome Data Analysis: from raw reads to community analyses.. F1000Res 2016;5:1492.
- Campbell JH, Foster CM, Vishnivetskaya T, Campbell AG, Yang ZK, Wymore A, Palumbo AV, Chesler EJ, Podar M. Host genetic and environmental effects on mouse intestinal microbiota.. ISME J 2012 Nov;6(11):2033-44.
- Candela M, Biagi E, Maccaferri S, Turroni S, Brigidi P. Intestinal microbiota is a plastic factor responding to environmental changes.. Trends Microbiol 2012 Aug;20(8):385-91.
- Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.. Proc Natl Acad Sci U S A 2011 Mar 15;108 Suppl 1(Suppl 1):4516-22.
- Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis.. Nucleic Acids Res 2005 Jan 1;33(Database issue):D294-6.
- 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.
- Costa MC, Weese JS. The equine intestinal microbiome.. Anim Health Res Rev 2012 Jun;13(1):121-8.
- Couëtil LL, Cardwell JM, Gerber V, Lavoie JP, Léguillette R, Richard EA. Inflammatory Airway Disease of Horses--Revised Consensus Statement.. J Vet Intern Med 2016 Mar-Apr;30(2):503-15.
- Craig JM. Atopic dermatitis and the intestinal microbiota in humans and dogs.. Vet Med Sci 2016 May;2(2):95-105.
- Cunningham FM, Dunkel B. Equine recurrent airway obstruction and insect bite hypersensitivity: understanding the diseases and uncovering possible new therapeutic approaches.. Vet J 2008 Sep;177(3):334-44.
- David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ. Diet rapidly and reproducibly alters the human gut microbiome.. Nature 2014 Jan 23;505(7484):559-63.
- Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Newbold CJ. Identification of a core bacterial community within the large intestine of the horse.. PLoS One 2013;8(10):e77660.
- Fujimura KE, Lynch SV. Microbiota in allergy and asthma and the emerging relationship with the gut microbiome.. Cell Host Microbe 2015 May 13;17(5):592-602.
- Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, McCoy KD, Macpherson AJ. Intestinal bacterial colonization induces mutualistic regulatory T cell responses.. Immunity 2011 May 27;34(5):794-806.
- Gomez A, Luckey D, Taneja V. The gut microbiome in autoimmunity: Sex matters.. Clin Immunol 2015 Aug;159(2):154-62.
- Harlow BE, Lawrence LM, Hayes SH, Crum A, Flythe MD. Effect of Dietary Starch Source and Concentration on Equine Fecal Microbiota.. PLoS One 2016;11(4):e0154037.
- Hollister EB, Gao C, Versalovic J. Compositional and functional features of the gastrointestinal microbiome and their effects on human health.. Gastroenterology 2014 May;146(6):1449-58.
- Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system.. Science 2012 Jun 8;336(6086):1268-73.
- Hotchkiss JW, Reid SW, Christley RM. A survey of horse owners in Great Britain regarding horses in their care. Part 2: Risk factors for recurrent airway obstruction.. Equine Vet J 2007 Jul;39(4):301-8.
- Hua X, Goedert JJ, Pu A, Yu G, Shi J. Allergy associations with the adult fecal microbiota: Analysis of the American Gut Project.. EBioMedicine 2016 Jan;3:172-179.
- Jackson CA, Berney C, Jefcoat AM, Robinson NE. Environment and prednisone interactions in the treatment of recurrent airway obstruction (heaves).. Equine Vet J 2000 Sep;32(5):432-8.
- Julliand V, Grimm P. The impact of diet on the hindgut microbiome. J. Equine Vet Sci 52:23–28.
- Kalliomäki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing.. J Allergy Clin Immunol 2001 Jan;107(1):129-34.
- Kehrli D, Jandova V, Fey K, Jahn P, Gerber V. Multiple hypersensitivities including recurrent airway obstruction, insect bite hypersensitivity, and urticaria in 2 warmblood horse populations.. J Vet Intern Med 2015 Jan;29(1):320-6.
- Kelly D, Coutts AG. Early nutrition and the development of immune function in the neonate.. Proc Nutr Soc 2000 May;59(2):177-85.
- Kraemer JG, Ramette A, Aebi S, Oppliger A, Hilty M. Influence of Pig Farming on the Human Nasal Microbiota: Key Role of Airborne Microbial Communities.. Appl Environ Microbiol 2018 Mar 1;84(6).
- Lahti L, Shetty S. Microbiome R package. .
- Lanz S, Brunner A, Graubner C, Marti E, Gerber V. Insect Bite Hypersensitivity in Horses is Associated with Airway Hyperreactivity.. J Vet Intern Med 2017 Nov;31(6):1877-1883.
- Laumen E, Doherr MG, Gerber V. Relationship of horse owner assessed respiratory signs index to characteristics of recurrent airway obstruction in two Warmblood families.. Equine Vet J 2010 Mar;42(2):142-8.
- Leclere M, Lavoie-Lamoureux A, Lavoie JP. Heaves, an asthma-like disease of horses.. Respirology 2011 Oct;16(7):1027-46.
- Legatzki A, Rösler B, von Mutius E. Microbiome diversity and asthma and allergy risk.. Curr Allergy Asthma Rep 2014 Oct;14(10):466.
- Léguillette R. Recurrent airway obstruction--heaves.. Vet Clin North Am Equine Pract 2003 Apr;19(1):63-86, vi.
- Linneberg A. The allergic march in early childhood and beyond.. Clin Exp Allergy 2008 Sep;38(9):1419-21.
- Marsland BJ, Trompette A, Gollwitzer ES. The Gut-Lung Axis in Respiratory Disease.. Ann Am Thorac Soc 2015 Nov;12 Suppl 2:S150-6.
- Martinez Arbizu P. PairwiseAdonis: pairwise multilevel comparison using adonis. .
- McMurdie PJ, Holmes S. Waste not, want not: why rarefying microbiome data is inadmissible.. PLoS Comput Biol 2014 Apr;10(4):e1003531.
- Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans.. Science 2011 May 20;332(6032):970-4.
- Nissen SP, Kjaer HF, Høst A, Nielsen J, Halken S. The natural course of sensitization and allergic diseases from childhood to adulthood.. Pediatr Allergy Immunol 2013 Sep;24(6):549-55.
- Noverr MC, Huffnagle GB. The 'microflora hypothesis' of allergic diseases.. Clin Exp Allergy 2005 Dec;35(12):1511-20.
- Oksanen J, Blanchet FG, Friendly M. Vegan: community ecology package. .
- Oliveira-Filho JP, Fabris VE, Goncalves RC, Amorim RM, Chiacchio SB, Borges AS. Clinical and histopathological aspects of the insect bite hypersensitivity in horses. Sem Ci Agr 33(3):1113–1122.
- Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, Adams H, van Ree R, Stobberingh EE. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study.. Gut 2007 May;56(5):661-7.
- 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 2013 Jan;41(Database issue):D590-6.
- R Core Team. R: a language and environment for statistical computing. Vienna, Austria.
- Ramseyer A, Gaillard C, Burger D, Straub R, Jost U, Boog C, Marti E, Gerber V. Effects of genetic and environmental factors on chronic lower airway disease in horses.. J Vet Intern Med 2007 Jan-Feb;21(1):149-56.
- Rutten NB, Gorissen DM, Eck A, Niers LE, Vlieger AM, Besseling-van der Vaart I, Budding AE, Savelkoul PH, van der Ent CK, Rijkers GT. Long Term Development of Gut Microbiota Composition in Atopic Children: Impact of Probiotics.. PLoS One 2015;10(9):e0137681.
- Salem SE, Maddox TW, Berg A, Antczak P, Ketley JM, Williams NJ, Archer DC. Variation in faecal microbiota in a group of horses managed at pasture over a 12-month period.. Sci Rep 2018 May 31;8(1):8510.
- Sanders CJ, Shortall CR, Gubbins S, Burgin L, Gloster J, Harrington R, Reynolds DR, Mellor PS, Carpenter S. Influence of season and meteorological parameters on flight activity of culicoides biting midges. J. Appl. Ecol 48(6):1355–1364.
- Schaffartzik A, Hamza E, Janda J, Crameri R, Marti E, Rhyner C. Equine insect bite hypersensitivity: what do we know?. Vet Immunol Immunopathol 2012 Jun 30;147(3-4):113-26.
- Sommer F, Bäckhed F. The gut microbiota--masters of host development and physiology.. Nat Rev Microbiol 2013 Apr;11(4):227-38.
- Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, Gordon JI, Fierer N, Knight R. Cohabiting family members share microbiota with one another and with their dogs.. Elife 2013 Apr 16;2:e00458.
- Spergel JM. From atopic dermatitis to asthma: the atopic march.. Ann Allergy Asthma Immunol 2010 Aug;105(2):99-106; quiz 107-9, 117.
- 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 Nov 27;8:231.
- Stiemsma LT, Reynolds LA, Turvey SE, Finlay BB. The hygiene hypothesis: current perspectives and future therapies.. Immunotargets Ther 2015;4:143-57.
- Strachan DP. Hay fever, hygiene, and household size.. BMJ 1989 Nov 18;299(6710):1259-60.
- Suchodolski JS, Ruaux CG, Steiner JM, Fetz K, Williams DA. Assessment of the qualitative variation in bacterial microflora among compartments of the intestinal tract of dogs by use of a molecular fingerprinting technique.. Am J Vet Res 2005 Sep;66(9):1556-62.
- Tamburini S, Shen N, Wu HC, Clemente JC. The microbiome in early life: implications for health outcomes.. Nat Med 2016 Jul 7;22(7):713-22.
- Terán-Ventura E, Roca M, Martin MT, Abarca ML, Martinez V, Vergara P. Characterization of housing-related spontaneous variations of gut microbiota and expression of toll-like receptors 2 and 4 in rats.. Microb Ecol 2010 Oct;60(3):691-702.
- Thoene-Reineke C, Fischer A, Friese C, Briesemeister D, Göbel UB, Kammertoens T, Bereswill S, Heimesaat MM. Composition of intestinal microbiota in immune-deficient mice kept in three different housing conditions.. PLoS One 2014;9(11):e113406.
- Thomas CL, Fernández-Peñas P. The microbiome and atopic eczema: More than skin deep.. Australas J Dermatol 2017 Feb;58(1):18-24.
- Tremblay J, Singh K, Fern A, Kirton ES, He S, Woyke T, Lee J, Chen F, Dangl JL, Tringe SG. Primer and platform effects on 16S rRNA tag sequencing.. Front Microbiol 2015;6:771.
- Venable EB, Bland SD, McPherson JL, Francis J. Role of the gut microbiota in equine health and disease. Anim Front 6(3):43–49.
- Wershil BK, Furuta GT. 4. Gastrointestinal mucosal immunity.. J Allergy Clin Immunol 2008 Feb;121(2 Suppl):S380-3; quiz S415.
- Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI. Human gut microbiome viewed across age and geography.. Nature 2012 May 9;486(7402):222-7.
- Zheng H, Liang H, Wang Y, Miao M, Shi T, Yang F, Liu E, Yuan W, Ji ZS, Li DK. Altered Gut Microbiota Composition Associated with Eczema in Infants.. PLoS One 2016;11(11):e0166026.
- Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota.. Gut 2008 Nov;57(11):1605-15.
Citations
This article has been cited 9 times.- Klier J, Fuchs S, Winter G, Gehlen H. Inhalative Nanoparticulate CpG Immunotherapy in Severe Equine Asthma: An Innovative Therapeutic Concept and Potential Animal Model for Human Asthma Treatment. Animals (Basel) 2022 Aug 16;12(16).
- Cvitas I, Oberhaensli S, Leeb T, Marti E. Equine keratinocytes in the pathogenesis of insect bite hypersensitivity: Just another brick in the wall?. PLoS One 2022;17(8):e0266263.
- Simões J, Batista M, Tilley P. The Immune Mechanisms of Severe Equine Asthma-Current Understanding and What Is Missing. Animals (Basel) 2022 Mar 16;12(6).
- Kaiser-Thom S, Hilty M, Ramseyer A, Epper P, Gerber V. The relationship between equine pastern dermatitis, meteorological factors, and the skin microbiota. Vet Dermatol 2022 Apr;33(2):165-e48.
- Theelen MJP, Luiken REC, Wagenaar JA, Sloet van Oldruitenborgh-Oosterbaan MM, Rossen JWA, Zomer AL. The Equine Faecal Microbiota of Healthy Horses and Ponies in The Netherlands: Impact of Host and Environmental Factors. Animals (Basel) 2021 Jun 12;11(6).
- Zhu Y, Jiang W, Holyoak R, Liu B, Li J. Investigation of Oral Microbiome in Donkeys and the Effect of Dental Care on Oral Microbial Composition. Animals (Basel) 2020 Nov 30;10(12).
- Jentsch MC, Keilhaue A, Wagner B, Rhyner C, Lübke S, Karagulyan M, Arnold C, Lohmann KL, Schnabel CL. Aspergillus fumigatus binding IgA and IgG1 are increased in bronchoalveolar lavage fluid of horses with neutrophilic asthma. Front Immunol 2024;15:1406794.
- Jentsch MC, Lübke S, Schrödl W, Volke D, Krizsan A, Hoffmann R, Kaiser-Thom S, Gerber V, Marti E, Wagner B, Schnabel CL. Immunoproteomics enable broad identification of new Aspergillus fumigatus antigens in severe equine asthma. Front Immunol 2024;15:1347164.
- Schnabel CL, Jentsch MC, Lübke S, Kaiser-Thom S, Gerber V, Vrtala S, Huang HJ, Rhyner C, Wagner B, Hoffmann R, Volke D. Immunoproteomics reveal increased serum IgG3/5 binding to Dermatophagoides and yeast protein antigens in severe equine asthma in a preliminary study. Front Immunol 2023;14:1293684.
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