Fecal microbiota of horses with colitis and its association with laminitis and survival during hospitalization

Abstract Background The association of microbiota with clinical outcomes and the taxa associated with colitis in horses remains generally unknown. Objectives Describe the fecal microbiota of horses with colitis and investigate the association of the fecal microbiota with the development of laminitis and survival. Animals Thirty‐six healthy and 55 colitis horses subdivided into laminitis (n = 15) and non‐laminitis (n = 39, 1 horse with chronic laminitis was removed from this comparison) and survivors (n = 27) and nonsurvivors (n = 28). Methods Unmatched case‐control study. The Illumina MiSeq platform targeting the V4 region of the 16S ribosomal RNA gene was used to assess the microbiota. Results The community membership (Jaccard index) and structure (Yue and Clayton index) were different (analysis of molecular variance [AMOVA]; P < .001) between healthy and colitis horses. The linear discriminant analysis effect size (LEfSe; linear discriminant analysis [LDA] >3; P < .05) and random forest analyses found Enterobacteriaceae, Lactobacillus, Streptococcus, and Enterococcus enriched in colitis horses, whereas Treponema, Faecalibacterium, Ruminococcaceae, and Lachnospiraceae were enriched in healthy horses. The community membership and structure of colitis horses with or without laminitis was (AMOVA; P > .05). Enterobacteriaceae, Streptococcus, and Lactobacillus were enriched in horses with laminitis (LDA > 3; P < .05). The community membership (AMOVA; P = .008) of surviving and nonsurviving horses was different. Nonsurviving horses had an enrichment of Enterobacteriaceae, Pseudomonas, Streptococcus, and Enterococcus (LDA >3; P < .05). Conclusion and Clinical Importance Differences in the microbiota of horses with colitis that survive or do not survive are minor and, similarly, the microbiota differences in horses with colitis that do or do not develop laminitis are minor.

[1]  F. Uzal,et al.  Bacterial and viral enterocolitis in horses: a review , 2021, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[2]  Xiaojun Yang,et al.  Effects of sepsis and its treatment measures on intestinal flora structure in critical care patients , 2021, World journal of gastroenterology.

[3]  D. Stefanovski,et al.  Risk factors for laminitis and nonsurvival in acute colitis: Retrospective study of 85 hospitalized horses (2011‐2019) , 2021, Journal of veterinary internal medicine.

[4]  V. Julliand,et al.  Sequential Modulation of the Equine Fecal Microbiota and Fibrolytic Capacity Following Two Consecutive Abrupt Dietary Changes and Bacterial Supplementation , 2021, Animals : an open access journal from MDPI.

[5]  Yunhe Fu,et al.  Changes of microbial and metabolome of the equine hindgut during oligofructose-induced laminitis , 2021, BMC Veterinary Research.

[6]  M. Surette,et al.  Luminal and Mucosal Microbiota of the Cecum and Large Colon of Healthy and Diarrheic Horses , 2020, Animals : an open access journal from MDPI.

[7]  J. Brady,et al.  Transporting and Exercising Unconditioned Horses: Effects on Microflora Populations. , 2020, Journal of equine veterinary science.

[8]  J. Murray,et al.  Factors Influencing Equine Gut Microbiota: Current Knowledge. , 2020, Journal of equine veterinary science.

[9]  D. Jenkins,et al.  The gut microbiome distinguishes mortality in trauma patients upon admission to the emergency department , 2020, The journal of trauma and acute care surgery.

[10]  M. Aleman,et al.  Clinical presentation, diagnostic findings, and outcome of adult horses with equine coronavirus infection at a veterinary teaching hospital: 33 cases (2012–2018) , 2019, The Veterinary Journal.

[11]  D. Jenkins,et al.  A prospective study in severely injured patients reveals an altered gut microbiome is associated with transfusion volume , 2019, The journal of trauma and acute care surgery.

[12]  S. Nicholson,et al.  Polytrauma independent of therapeutic intervention alters the gastrointestinal microbiome. , 2018, American journal of surgery.

[13]  E. Pamer,et al.  Interbacterial mechanisms of colonization resistance and the strategies pathogens use to overcome them , 2018, Mucosal Immunology.

[14]  H. Stämpfli,et al.  Diagnosis and Treatment of Undifferentiated and Infectious Acute Diarrhea in the Adult Horse , 2018, Veterinary Clinics of North America: Equine Practice.

[15]  C. Moinard,et al.  Head injury profoundly affects gut microbiota homeostasis: Results of a pilot study. , 2018, Nutrition.

[16]  J. Chen,et al.  Burn Injury Leads to Increase in Relative Abundance of Opportunistic Pathogens in the Rat Gastrointestinal Microbiome , 2017, Front. Microbiol..

[17]  B. Rittmann,et al.  pH-Mediated Microbial and Metabolic Interactions in Fecal Enrichment Cultures , 2017, mSphere.

[18]  P. Popovich,et al.  Gut dysbiosis impairs recovery after spinal cord injury , 2016, The Journal of experimental medicine.

[19]  D. Brough,et al.  Brain injury induces specific changes in the caecal microbiota of mice via altered autonomic activity and mucoprotein production , 2016, Brain, Behavior, and Immunity.

[20]  J. Weese,et al.  Effects of transport, fasting and anaesthesia on the faecal microbiota of healthy adult horses. , 2016, Equine veterinary journal.

[21]  Edoardo Pasolli,et al.  Machine Learning Meta-analysis of Large Metagenomic Datasets: Tools and Biological Insights , 2016, PLoS Comput. Biol..

[22]  William A. Walters,et al.  Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys , 2015, mSystems.

[23]  M. Delmée,et al.  Faecal microbiota characterisation of horses using 16 rdna barcoded pyrosequencing, and carriage rate of clostridium difficile at hospital admission , 2015, BMC Microbiology.

[24]  Na-Ri Shin,et al.  Proteobacteria: microbial signature of dysbiosis in gut microbiota. , 2015, Trends in biotechnology.

[25]  R. Gamelli,et al.  Burn Injury Alters the Intestinal Microbiome and Increases Gut Permeability and Bacterial Translocation , 2015, PloS one.

[26]  B. Stecher The Roles of Inflammation, Nutrient Availability and the Commensal Microbiota in Enteric Pathogen Infection. , 2015, Microbiology spectrum.

[27]  C. Vaishnavi Translocation of gut flora and its role in sepsis. , 2013, Indian journal of medical microbiology.

[28]  L. Rigottier-Gois,et al.  Dysbiosis in inflammatory bowel diseases: the oxygen hypothesis , 2013, The ISME Journal.

[29]  L. Arroyo,et al.  Physicochemical interpretation of acid-base abnormalities in 54 adult horses with acute severe colitis and diarrhea. , 2013, Journal of veterinary internal medicine.

[30]  A. Klindworth,et al.  Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies , 2012, Nucleic acids research.

[31]  David J. Edwards,et al.  Hypothesis Testing and Power Calculations for Taxonomic-Based Human Microbiome Data , 2012, PloS one.

[32]  Emma Allen-Vercoe,et al.  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 , 2012, PloS one.

[33]  C. Quince,et al.  Dirichlet Multinomial Mixtures: Generative Models for Microbial Metagenomics , 2012, PloS one.

[34]  C. Huttenhower,et al.  Metagenomic biomarker discovery and explanation , 2011, Genome Biology.

[35]  O. Tasaki,et al.  Altered Gut Flora Are Associated with Septic Complications and Death in Critically Ill Patients with Systemic Inflammatory Response Syndrome , 2010, Digestive Diseases and Sciences.

[36]  C. Pollitt,et al.  Microbial events in the hindgut during carbohydrate-induced equine laminitis. , 2010, The Veterinary clinics of North America. Equine practice.

[37]  C. Pollitt,et al.  Microbial ecology of the equine hindgut during oligofructose-induced laminitis , 2008, The ISME Journal.

[38]  C. Pollitt,et al.  Streptococcus henryi sp. nov. and Streptococcus caballi sp. nov., isolated from the hindgut of horses with oligofructose-induced laminitis. , 2008, International journal of systematic and evolutionary microbiology.

[39]  A. V. van Eps,et al.  Fluorescence in situ hybridization analysis of hindgut bacteria associated with the development of equine laminitis. , 2007, Environmental microbiology.

[40]  R. Boston,et al.  Risk factors for development of acute laminitis in horses during hospitalization: 73 cases (1997-2004). , 2007, Journal of the American Veterinary Medical Association.

[41]  M. Hahn,et al.  Differences in structure and dynamics of Polynucleobacter communities in a temperate and a subtropical lake, revealed at three phylogenetic levels. , 2006, FEMS microbiology ecology.

[42]  S. Bailey,et al.  Gastrointestinal derived factors are potential triggers for the development of acute equine laminitis. , 2006, The Journal of nutrition.

[43]  J. Madigan,et al.  Molecular characterization of Clostridium difficile isolates from horses in an intensive care unit and association of disease severity with strain type. , 2006, Journal of the American Veterinary Medical Association.

[44]  B. LeRoy,et al.  Risk factors associated with renal insufficiency in horses with primary gastrointestinal disease: 26 cases (2000-2003). , 2006, Journal of the American Veterinary Medical Association.

[45]  Kazuhisa Yoshiya,et al.  Altered gut flora and environment in patients with severe SIRS. , 2006, The Journal of trauma.

[46]  C. Marr,et al.  The effects of vasoactive amines found in the equine hindgut on digital blood flow in the normal horse. , 2010, Equine veterinary journal.

[47]  J. Weese,et al.  A prospective study of the roles of clostridium difficile and enterotoxigenic Clostridium perfringens in equine diarrhoea. , 2010, Equine veterinary journal.

[48]  N. Cohen,et al.  Characteristics and risk factors for failure of horses with acute diarrhea to survive: 122 cases (1990-1996). , 1999, Journal of the American Veterinary Medical Association.

[49]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[50]  H. Garner,et al.  Changes in the caecal flora associated with the onset of laminitis. , 1978, Equine veterinary journal.