Clinical variability of equine asthma phenotypes and analysis of diagnostic steps in phenotype differentiation.
Bronchoalveolar lavage
Chronic obstructive bronchiolitis
Equine asthma
Phenotype
Journal
Acta veterinaria Scandinavica
ISSN: 1751-0147
Titre abrégé: Acta Vet Scand
Pays: England
ID NLM: 0370400
Informations de publication
Date de publication:
18 Sep 2024
18 Sep 2024
Historique:
received:
25
04
2024
accepted:
11
09
2024
medline:
19
9
2024
pubmed:
19
9
2024
entrez:
18
9
2024
Statut:
epublish
Résumé
Equine asthma is a common, non-infectious, chronic lung disease that affects up to 80% of the horse population. Strict phenotyping and identification of subclinically asthmatic horses can be challenging. The aim of this study was to describe equine asthma phenotypes (mild, moderate, and severe asthma) defined by BALF cytology and occurrence of clinical signs in a population of privately owned horses and to identify the variables and examination steps with best discriminative potential. The standardised examination protocol included clinical examinations, blood work, airway endoscopy with bronchoalveolar lavage fluid analysis, arterial blood gas analysis and radiography under clinical conditions performed by one veterinarian. Out of 26 horses, four were diagnosed with mild (subclinical), seven with moderate, and seven with severe asthma based on clinical examination and BALF cytology. Eight horses served as controls. Cough with history of coughing was the strongest variable in phenotype differentiation. Factor analysis revealed an increasing clinical variability with disease severity and an overlapping of clinical presentations between phenotypes. Elevated mast cell (4/4 horses) and neutrophil counts (3/4 horses) in bronchoalveolar lavage cytology differentiated mild asthmatic horses from healthy horses. Moderate and severe asthmatic horses were characterised by clinical signs and neutrophil counts. The results indicate that medical history, clinical examination and bronchoalveolar lavage cytology are minimum indispensable steps to diagnose equine asthma and that phenotypes are clinically overlapping. A differentiation of three phenotypes without neutrophil and mast cell counts in bronchoalveolar lavage cytology is not sufficient for clinical diagnostics. A comparably exact diagnosis cannot be achieved by relying on alternative examinations used in this study. Screenings of inconspicuous horses with bronchoalveolar lavage can aid in diagnosing subclinically affected animals, however, group size was small, the procedure is invasive and clinical relevance of slightly elevated cells in bronchoalveolar lavage remains unclear. Clinical relevance could not be clarified in this study, since follow-up examinations or lung function testing were not performed.
Sections du résumé
BACKGROUND
BACKGROUND
Equine asthma is a common, non-infectious, chronic lung disease that affects up to 80% of the horse population. Strict phenotyping and identification of subclinically asthmatic horses can be challenging. The aim of this study was to describe equine asthma phenotypes (mild, moderate, and severe asthma) defined by BALF cytology and occurrence of clinical signs in a population of privately owned horses and to identify the variables and examination steps with best discriminative potential. The standardised examination protocol included clinical examinations, blood work, airway endoscopy with bronchoalveolar lavage fluid analysis, arterial blood gas analysis and radiography under clinical conditions performed by one veterinarian.
RESULTS
RESULTS
Out of 26 horses, four were diagnosed with mild (subclinical), seven with moderate, and seven with severe asthma based on clinical examination and BALF cytology. Eight horses served as controls. Cough with history of coughing was the strongest variable in phenotype differentiation. Factor analysis revealed an increasing clinical variability with disease severity and an overlapping of clinical presentations between phenotypes. Elevated mast cell (4/4 horses) and neutrophil counts (3/4 horses) in bronchoalveolar lavage cytology differentiated mild asthmatic horses from healthy horses. Moderate and severe asthmatic horses were characterised by clinical signs and neutrophil counts.
CONCLUSIONS
CONCLUSIONS
The results indicate that medical history, clinical examination and bronchoalveolar lavage cytology are minimum indispensable steps to diagnose equine asthma and that phenotypes are clinically overlapping. A differentiation of three phenotypes without neutrophil and mast cell counts in bronchoalveolar lavage cytology is not sufficient for clinical diagnostics. A comparably exact diagnosis cannot be achieved by relying on alternative examinations used in this study. Screenings of inconspicuous horses with bronchoalveolar lavage can aid in diagnosing subclinically affected animals, however, group size was small, the procedure is invasive and clinical relevance of slightly elevated cells in bronchoalveolar lavage remains unclear. Clinical relevance could not be clarified in this study, since follow-up examinations or lung function testing were not performed.
Identifiants
pubmed: 39294710
doi: 10.1186/s13028-024-00773-7
pii: 10.1186/s13028-024-00773-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
51Informations de copyright
© 2024. The Author(s).
Références
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;30:503–15.
pubmed: 26806374
pmcid: 4913592
doi: 10.1111/jvim.13824
Bond S, Léguillette R, Richard EA, Couetil L, Lavoie JP, Martin JG, et al. Equine asthma: Integrative biologic relevance of a recently proposed nomenclature. J Vet Intern Med. 2018;32:2088–98.
pubmed: 30294851
pmcid: 6271326
doi: 10.1111/jvim.15302
Wasko AJ, Barkema HW, Nicol J, Fernandez N, Logie N, Léguillette R. Evaluation of a risk-screening questionnaire to detect equine lung inflammation: Results of a large field study. Equine Vet J. 2011;43:145–52.
pubmed: 21592207
doi: 10.1111/j.2042-3306.2010.00150.x
Davis KU, Sheats MK. Bronchoalveolar lavage cytology characteristics and seasonal changes in a herd of pastured teaching horses. Front Vet Sci. 2019;6:1–7.
doi: 10.3389/fvets.2019.00074
Ivester KM, Couëtil LL, Moore GE. An observational study of environmental exposures, airway cytology, and performance in racing thoroughbreds. J Vet Intern Med. 2018;32:1754–62.
pubmed: 30222207
pmcid: 6189343
doi: 10.1111/jvim.15226
Gerber V, Robinson NE, Luethi S, Marti E, Wampfler B, Straub R. Airway inflammation and mucus in two age groups of asymptomatic well-performing sport horses. Equine Vet J. 2003;35:491–5.
pubmed: 12875328
doi: 10.2746/042516403775600424
Smith KC, Wylie CE, Bacigalupo SA, Cardwell JM, Kinnison T, Couetil LL. Mild-moderate equine asthma: A scoping review of evidence supporting the consensus definition. Vet J. 2022;286: 105865.
pubmed: 35817389
doi: 10.1016/j.tvjl.2022.105865
Couetil L, Cardwell JM, Leguillette R, Mazan M, Richard E, Bienzle D, et al. Equine asthma: Current understanding and future directions. Front Vet Sci. 2020;7:450.
pubmed: 32903600
pmcid: 7438831
doi: 10.3389/fvets.2020.00450
Sheats MK, Davis KU, Poole JA. Comparative review of asthma in farmers and horses. Curr Allergy Asthma Rep. 2019;19:50.
pubmed: 31599358
pmcid: 9116535
doi: 10.1007/s11882-019-0882-2
Lavoie J-P. How to diagnose mild and moderate equine asthma as a cause of poor performance in sport horses. Proc Annu Conv AAEP. 2021;67:199–201.
Richard EA, Fortier GD, Lekeux PM, Van EE. Laboratory findings in respiratory fluids of the poorly-performing horse. Vet J. 2010;185:115–22.
pubmed: 19481964
doi: 10.1016/j.tvjl.2009.05.003
Fraipont A, Van Erck E, Ramery E, Richard E, Denoix JM, Lekeux P, et al. Subclinical diseases underlying poor performance in endurance horses: Diagnostic methods and predictive tests. Vet Rec. 2011;169:154.
pubmed: 21795311
doi: 10.1136/vr.d4142
Pirrone F, Albertini M, Clement MG, Lafortuna CL. Respiratory mechanics in Standardbred horses with sub-clinical inflammatory airway disease and poor athletic performance. Vet J. 2007;173:144–50.
pubmed: 16129634
doi: 10.1016/j.tvjl.2005.07.020
Couëtil LL. IAD: Cough, poor performance, mucus in the airways - What is so important about that? Proc Annu Conv AAEP. 2002;48:200–7.
Herszberg B, Ramos-Barbón D, Tamaoka M, Martin JG, Lavoie J-P. Heaves, an asthma-like equine disease, involves airway smooth muscle remodeling. J Allergy Clin Immunol. 2006;118:382–8.
pubmed: 16890762
doi: 10.1016/j.jaci.2006.03.044
Barton AK, Gehlen H. Pulmonary remodeling in equine asthma: What do we know about mediators of inflammation in the horse? Mediators Inflamm. 2016;2016:1–12.
doi: 10.1155/2016/5693205
Leduc L, Leclère M, Gauthier LG, Marcil O, Lavoie JP. Severe asthma in horsed is associated with increased airway innervation. J Vet Intern Med. 2024;38:485–94.
pubmed: 38054207
doi: 10.1111/jvim.16941
R Core Team. R: A language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria: https://www.R-project.org/ ; 2023.
Le S, Josse J, Husson F. FactoMineR: An R package for multivariate analysis. J Stat Softw. 2008;25:1–18.
doi: 10.18637/jss.v025.i01
Therneau T, Atkinson B, Ripley B. rpart: Recursive partitioning and regression trees. https://CRAN.R-project.org/package=rpart ; 2022.
Bullone M, Lavoie JP. Science-in-brief: Equine asthma diagnosis: Beyond bronchoalveolar lavage cytology. Equine Vet J. 2017;49:263–5.
pubmed: 28387029
doi: 10.1111/evj.12679
Olave CJ, Ivester KM, Couëtil LL, Kritchevsky JE, Tinkler SH, Mukhopadhyay A. Dust exposure and pulmonary inflammation in Standardbred racehorses fed dry hay or haylage: A pilot study. Vet J. 2021;271: 105654.
pubmed: 33840486
doi: 10.1016/j.tvjl.2021.105654
Westerfeld R, Payette F, Dubuc V, Manguin E, Picotte K, Beauchamp G, et al. Effects of soaked hay on lung function and airway inflammation in horses with severe asthma. J Vet Intern Med. 2023;38:469–76.
pubmed: 37930110
pmcid: 10800199
doi: 10.1111/jvim.16919
Golding E, Neavyn Neita A, Walshe N, Hanlon A, Mulcahy G, Duggan V. Survey of the knowledge and perceptions of horse owners in Ireland of common clinical conditions and their impact. Equine Vet J. 2023;55:270–81.
pubmed: 35575027
doi: 10.1111/evj.13589
Ramseyer A, Gaillard C, Burger D, Straub R, Jost U, Boog C, et al. Effects of genetic and environmental factors on chronic lower airway disease in horses. J Vet Intern Med. 2007;21:149–56.
pubmed: 17338163
doi: 10.1111/j.1939-1676.2007.tb02941.x
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;42:142–8.
pubmed: 20156250
doi: 10.2746/042516409X479586
Robins TJ, Bedenice D, Mazan M. A longitudinal analysis of equine asthma presentation and response to treatment using lung function testing and BAL cytology analysis in combination with owner perception. Animals. 2023;13:3387.
pubmed: 37958142
pmcid: 10649418
doi: 10.3390/ani13213387
Rettmer H, Hoffman AM, Lanz S, Oertly M, Gerber V. Owner-reported coughing and nasal discharge are associated with clinical findings, arterial oxygen tension, mucus score and bronchoprovocation in horses with recurrent airway obstruction in a field setting. Equine Vet J. 2015;47:291–5.
pubmed: 24761754
doi: 10.1111/evj.12286
Simões J, Tilley P. Decision making in severe equine asthma—Diagnosis and monitoring. Animals. 2023;13:3872.
pubmed: 38136909
pmcid: 10740644
doi: 10.3390/ani13243872
Beling JCF, Santos DMSA, Ferreira MP, Silva PCAR, Costa MFM, Lessa DAB. Post-exercise endoscopic and cytologic diagnosis of equine asthma syndrome in asymptomatic Brazilian pacers. Equine Vet Educ. 2022;35:355–61.
doi: 10.1111/eve.13418
Hansen S, Honoré ML, Riihimaki M, Pringle J, Ammentorp AH, Fjeldborg J. Seasonal variation in tracheal mucous and bronchoalveolar lavage cytology for adult clinically healthy stabled horses. J Equine Vet Sci. 2018;71:1–5.
doi: 10.1016/j.jevs.2018.09.001
Gerber V, Straub R, Marti E, Hauptman J, Herholz C, King M, et al. Endoscopic scoring of mucus quantity and quality: Observer and horse variance and relationship to inflammation, mucus viscoelasticity and volume. Equine Vet J. 2004;36:576–82.
pubmed: 15581321
doi: 10.2746/0425164044864525
Koch C, Straub R, Ramseyer A, Widmer A, Robinson NE, Gerber V. Endoscopic scoring of the tracheal septum in horses and its clinical relevance for the evaluation of lower airway health in horses. Equine Vet J. 2007;39:107–12.
pubmed: 17378438
doi: 10.2746/042516407X158764
Gerber V, King M, Schneider DA, Robinson NE. Tracheobronchial mucus viscoelasticity during environmental challenge in horses with recurrent airway obstruction. Equine Vet J. 2000;32:411–7.
pubmed: 11037263
doi: 10.2746/042516400777591183
Tilley P, Sales Luis JP, Branco FM. Correlation and discriminant analysis between clinical, endoscopic, thoracic X-ray and bronchoalveolar lavage fluid cytology scores, for staging horses with recurrent airway obstruction (RAO). Res Vet Sci. 2012;93:1006–14.
pubmed: 22136797
doi: 10.1016/j.rvsc.2011.10.024
Rodrigues Costa LR, Seahorn TL, Moore RM, Taylor HW, Gaunt SD, Beadle RE. Correlation of clinical score, intrapleural pressure, cytologic findings of bronchoalveolar fluid, and histopathologic lesions of pulmonary tissue in horses with summer pasture-associated obstructive pulmonary disease. Am J Vet Res. 2000;61:167–73.
doi: 10.2460/ajvr.2000.61.167
Amstrup C, Larsen M, Fjeldborg J, et al. Associations between clinical signs, endoscopic and cytological findings in equine bronchoalveolar lavage samples. Authorea, May 30, 2023. https://doi.org/10.22541/au.168544982.24601772/v1
Varegg MS, Kløverød KM, Austnes MK, Siwinska N, Slowikowska M, Zak A, et al. The effect of single pretreatment with salbutamol on recovery of bronchoalveolar lavage fluid in horses with suspected or confirmed severe equine asthma. J Vet Intern Med. 2019;33:976–80.
pubmed: 30707780
pmcid: 6430915
doi: 10.1111/jvim.15359
Shimoda M, Tanaka Y, Morimoto K, Abe T, Asaga R, Nakajima K, et al. Analysis of predicted factors for bronchoalveolar lavage recovery failure: An observational study. PLoS ONE. 2022;17: e0275377.
pubmed: 36178919
pmcid: 9524652
doi: 10.1371/journal.pone.0275377
Pacheco AP, Paradis MRR, Hoffman AMM, Sanchez A, Nadeau M, Tufts M, et al. Age effects on blood gas, spirometry, airway reactivity, and bronchoalveolar lavage fluid cytology in clinically healthy horses. J Vet Intern Med. 2014;28:603–8.
pubmed: 24528225
pmcid: 4857999
doi: 10.1111/jvim.12318
Simões J, Sales Luís J, Tilley P. Contribution of lung function tests to the staging of severe equine asthma syndrome in the field. Res Vet Sci. 2019;123:112–7.
pubmed: 30616173
doi: 10.1016/j.rvsc.2018.12.014
Mazan MR, Vin R, Hoffman AM. Radiographic scoring lacks predictive value in inflammatory airway disease. Equine Vet J. 2005;37:541–5.
pubmed: 16295932
doi: 10.2746/042516405775314899
Greim E, Naef J, Mainguy-Seers S, Lavoie JP, Sage S, Dolf G, et al. Breath characteristics and adventitious lung sounds in healthy and asthmatic horses. J Vet Intern Med. 2024;38:495–504.
pubmed: 38192117
pmcid: 10800186
doi: 10.1111/jvim.16980
Leclere M, Lavoie-Lamoureux A, Joubert P, Relave F, Setlakwe EL, Beauchamp G, et al. Corticosteroids and antigen avoidance decrease airway smooth muscle mass in an equine asthma model. Am J Respir Cell Mol Biol. 2012;47:589–96.
pubmed: 22721832
doi: 10.1165/rcmb.2011-0363OC
Olave C. The effect of low-dust forages and the role of pro-resolving lipid mediators in mild-moderate Equine asthma. Purdue University Graduate School. Thesis. 2020. https://doi.org/10.25394/PGS.12563690.v1
Shaba JJ, Behan Braman A, Robinson NE. Plasma cortisol concentration increases within 6 hours of stabling in RAO-affected horses. Equine Vet J. 2014;46:642–4.
pubmed: 24164413
doi: 10.1111/evj.12201
Orard M, Hue E, Couroucé A, Bizon-Mercier C, Toquet MP, Moore-Colyer M, et al. The influence of hay steaming on clinical signs and airway immune response in severe asthmatic horses. BMC Vet Res. 2018;14:345.
pubmed: 30442129
pmcid: 6236910
doi: 10.1186/s12917-018-1636-4
Mönki J, Saastamoinen M, Karikoski N, Rajamäki M, Raekallio M, Junnila J, et al. Effects of bedding material on equine lower airway inflammation: A crossover study comparing peat and wood shavings. Front Vet Sci. 2021;8: 656814.
pubmed: 33898547
pmcid: 8062776
doi: 10.3389/fvets.2021.656814
Couëtil L, Chilcoat C, DeNicola D, Glickman L. Randomized, controlled study of inhaled fluticasone propionate, oral administration of prednisone, and environmental management of horses with recurrent airway obstruction. Am J Vet Res. 2005;66:1665–74.
pubmed: 16273895
doi: 10.2460/ajvr.2005.66.1665
Gy C, Leclere M, Vargas A, Grimes C, Lavoie JP. Investigation of blood biomarkers for the diagnosis of mild to moderate asthma in horses. J Vet Intern Med. 2019;33:1789–95.
pubmed: 31099114
pmcid: 6639487
doi: 10.1111/jvim.15505
Couroucé A. Field exercise testing for assessing fitness in French standardbred trotters. Vet J. 1999;157:112–22.
pubmed: 10204407
doi: 10.1053/tvjl.1998.0302
Munsters CCBM, van Iwaarden A, van Weeren R, Sloet van Oldruitenborgh-Oosterbaan MM. Exercise testing in Warmblood sport horses under field conditions. Vet J. 2014;202:11–9.
pubmed: 25172838
doi: 10.1016/j.tvjl.2014.07.019
Couroucé-Malblanc A, van Erck-Westergren E. Exercise testing in the field. In: Hinchcliff KW, Kaneps AJ, Geor RJ, editors. Equine sports medicine and surgery. 2nd ed. Philadelphia: Saunders Ltd.; 2013. p. 25–42.
Malikides N, Hughes KJ, Hodgson JL. Comparison of tracheal aspirates before and after high-speed treadmill exercise in racehorses. Aust Vet J. 2007;85:414–9.
pubmed: 17903129
doi: 10.1111/j.1751-0813.2007.00167.x
Evans DL, Rose RJ. Cardiovascular and respiratory responses in thoroughbred horses during treadmill exercise. J exp Biol. 1988;134:397–408.
pubmed: 3356965
doi: 10.1242/jeb.134.1.397
Couroucé-Malblanc PA, Fortier G, Pronost S, Corde R, Rossignol F, Deniau V. Physiological parameters and evaluation of the upper and lower respiratory airways in French Standardbred Trotters during a standardised exercise on a treadmill. Equine Vet J. 2008;161:351–8.
Bedenice D, Mazan MR, Hoffman AM. Association between cough and cytology of bronchoalveolar lavage fluid and pulmonary function in horses diagnosed with inflammatory airway disease. J Vet Intern Med. 2008;22:1022–8.
pubmed: 18498325
doi: 10.1111/j.1939-1676.2008.0109.x
Swiderski CE, Hunter CL, Bowser JE, Costa LR, Cooley AJ, Claude A, et al. Deciphering the role of bronchial hyper-responsiveness in equine pasture asthma. J Equine Vet Sci. 2017;52:29–35.
doi: 10.1016/j.jevs.2017.03.219
Cullimore AM, Secombe CJ, Lester GD, Robertson ID. Bronchoalveolar lavage fluid cytology and airway hyper-reactivity in clinically normal horses. Aust Vet J. 2018;96:291–6.
pubmed: 30129032
doi: 10.1111/avj.12721