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Animals : an open access journal from MDPI2024; 14(23); 3504; doi: 10.3390/ani14233504

Equine Asthma Diagnostics: Review of Influencing Factors and Difficulties in Diagnosing Subclinical Disease.

Abstract: This literature review focuses on diagnostics of equine asthma (EA), possible influencing factors on diagnostic techniques and latest developments in diagnosing horses during EA remission or with subclinical disease. Routine EA diagnostics include a clinical examination of the respiratory system with percussion and auscultation including a rebreathing examination, and clinical pathology including white blood cells and arterial blood gas analysis. Subsequent diagnostics include bronchoscopy to evaluate the amount and viscosity of respiratory secretion, bronchoalveolar lavage, and the cytology of tracheal aspirates (TAs) and bronchoalveolar lavage fluid (BALF). The grading of EA severity is built on respiratory effort at rest, which is increased in severe equine asthma. The inflammatory subtype is based on BALF cytology, while TA cytology helps to rule out previous bacterial infections. Different factors have an impact on the airways regarding the structure of the epithelium, cytology, and inflammatory markers possibly influencing the diagnosis of EA. Short-term exercise increases the total cell count and inflammatory mediators identified in the BALF of human patients, asymptomatic horses, and other species. Other factors involve cold or chlorinated air, long-term training effects, and concurrent additional respiratory disease, in particular exercise-induced pulmonary hemorrhage. As BALF cytology may be unremarkable during EA remission and low-grade disease, exercise tests and other factors stressing the bronchial epithelium may help to diagnose these patients.
Publication Date: 2024-12-04 PubMed ID: 39682469PubMed Central: PMC11640047DOI: 10.3390/ani14233504Google Scholar: Lookup
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  • Journal Article
  • Review

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.

The research article delves into equine asthma diagnostics with a particular emphasis on the challenges of diagnosing subclinical disease and the factors potentially influencing diagnostic techniques.

Overview of Equine Asthma Diagnostics

  • This paper presents a comprehensive analysis of the diagnosis methods used in detecting equine asthma. Regular diagnostic practices involve a clinical examination of the horse’s respiratory system, including an assessment of the horse’s blood for white blood cells and arterial blood gas analyses.
  • Additional diagnostics include the use of bronchoscopy to measure and monitor respiratory secretion, bronchoalveolar lavage, and the cytology (study of cells) of tracheal aspirate and bronchoalveolar lavage fluid.
  • The grading of equine asthma severity is done by observing a horse’s resting respiratory rate. High resting respiratory rates point to severe equine asthma.

Cytology and Inflammatory Markers

  • Inflammatory subtypes in horses with equine asthma are identified using bronchoalveolar lavage fluid cytology. Tracheal aspirate cytology, on the other hand, is utilized to rule out the presence of prior bacterial infections.
  • The structure of the epithelium (the tissue lining the bronchial tubes), cytology (study of cells), and inflammatory markers may potentially impact the diagnosis of equine asthma.

Impact of Exercise and Other Factors

  • Short-term exercise is found to increase the total cell count and inflammatory mediators in the bronchoalveolar lavage fluid. This observation holds in humans, asymptomatic horses, and other species.
  • Other factors which may affect diagnosis include exposure to cold or chlorinated air, long-term effects of training, and other concurrent respiratory conditions, specifically exercise-induced pulmonary hemorrhage.

Diagnosing Remission and Low-Grade Disease

  • For horses in equine asthma remission or with low-grade disease, bronchoalveolar lavage fluid cytology may show no noticeable changes prompting the need for other diagnostic techniques. Exercise tests and other variables that stress the bronchial epithelium can help in the diagnosis of these cases.

Cite This Article

APA
Lendl L, Barton AK. (2024). Equine Asthma Diagnostics: Review of Influencing Factors and Difficulties in Diagnosing Subclinical Disease. Animals (Basel), 14(23), 3504. https://doi.org/10.3390/ani14233504

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 14
Issue: 23
PII: 3504

Researcher Affiliations

Lendl, Lioba
  • Equine Clinic Hochmoor, Ruthmannstr. 10, 48712 Gescher, Germany.
Barton, Ann Kristin
  • Equine Clinic Hochmoor, Ruthmannstr. 10, 48712 Gescher, Germany.

Conflict of Interest Statement

The authors declare no conflicts of interest.

References

This article includes 114 references
  1. Couetil L, Cardwell JM, Leguillette R, Mazan M, Richard E, Bienzle D, Bullone M, Gerber V, Ivester K, Lavoie JP. Equine Asthma: Current Understanding and Future Directions. Front. Vet. Sci. 2020;7:450.
    doi: 10.3389/fvets.2020.00450pmc: PMC7438831pubmed: 32903600google scholar: lookup
  2. 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;30:503–515.
    doi: 10.1111/jvim.13824pmc: PMC4913592pubmed: 26806374google scholar: lookup
  3. Couëtil L. What Do We Know About the Pathophysiology of Equine Asthma?. AAEP Proc. 2021;67:460–464.
  4. Martin JG. Classification of Asthma. Proceedings of the 2nd Havemeyer Workshop on IAD 2014; Cabourg, Frankreich. 22 July 2014; pp. 11–13.
  5. Allen KJ, Tremaine WH. Prevalence of Inflammatory Airway Disease in National Hunt Horses Referred for Investigation of Poor Athletic Performance. Equine Vet. J. 2006;36:529–534.
  6. Robinson NE, Karmaus W, Holcombe SJ, Carr EA, Derksen FJ. Airway Inflammation in Michigan Pleasure Horses: Prevalence and Risk Factors. Equine Vet. J. 2006;38:293–299.
    doi: 10.2746/042516406777749281pubmed: 16866194google scholar: lookup
  7. 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;35:491–495.
    doi: 10.2746/042516403775600424pubmed: 12875328google scholar: lookup
  8. Pirie RS. Recurrent Airway Obstruction: A Review. Equine Vet. J. 2014;46:276–288.
    doi: 10.1111/evj.12204pubmed: 24164473google scholar: lookup
  9. Bosshard S, Gerber V. Evaluation of Coughing and Nasal Discharge as Early Indicators for An Increased Risk to Develop Equine Recurrent Airway Obstruction (RAO). J. Vet. Intern. Med. 2014;28:618–623.
    doi: 10.1111/jvim.12279pmc: PMC4858023pubmed: 24417562google scholar: lookup
  10. Bessonnat A, Hélie P, Grimes C, Lavoie J. Airway Remodeling in Horses with Mild and Moderate Asthma. J. Vet. Intern. Med. 2022;36:285–291.
    doi: 10.1111/jvim.16333pmc: PMC8783337pubmed: 34877706google scholar: lookup
  11. Leclere M, Lavoie-Lamoureux A, Gélinas-Lymburner É, David F, Martin JG, Lavoie JP. Effect of Antigenic Exposure on Airway Smooth Muscle Remodeling in an Equine Model of Chronic Asthma. Am. J. Respir. Cell Mol. Biol. 2011;45:181–187.
    doi: 10.1165/rcmb.2010-0300OCpubmed: 20935189google scholar: lookup
  12. Leclere M, Lavoie-Lamoureux A, Joubert P, Relave F, Setlakwe EL, Beauchamp G, Couture C, Martin JG, Lavoie JP. Corticosteroids and Antigen Avoidance Decrease Airway Smooth Muscle Mass in an Equine Asthma Model. Am. J. Respir. Cell Mol. Biol. 2012;47:589–596.
    doi: 10.1165/rcmb.2011-0363OCpubmed: 22721832google scholar: lookup
  13. Ceriotti S, Bullone M, Leclere M, Ferrucci F, Lavoie JP. Severe Asthma Is Associated with a Remodeling of the Pulmonary Arteries in Horses. PLoS ONE 2020;15:e0239561.
  14. Gerber V, Straub R, Marti E, Hauptman J, Herholz C, King M, Imhof A, Tahon L, Robinson NE. Endoscopic Scoring of Mucus Quantity and Quality: Observer and Horse Variance and Relationship to Inflammation, Mucus Viscoelasticity and Volume. Equine Vet. J. 2004;36:576–582.
    doi: 10.2746/0425164044864525pubmed: 15581321google scholar: lookup
  15. Couetil LL, Thompson CA. Airway Diagnostics. Vet. Clin. N. Am. Equine Pract. 2020;36:87–103.
    doi: 10.1016/j.cveq.2019.12.006pubmed: 32145836google scholar: lookup
  16. Cian F, Monti P, Durham A. Cytology of the Lower Respiratory Tract in Horses: An Updated Review. Equine Vet. Educ. 2015;27:544–553.
    doi: 10.1111/eve.12376google scholar: lookup
  17. Rossi H, Virtala A-M, Raekallio M, Rahkonen E, Rajamäki MM, Mykkänen A. Comparison of Tracheal Wash and Bronchoalveolar Lavage Cytology in 154 Horses With and Without Respiratory Signs in a Referral Hospital Over 2009−2015. Front. Vet. Sci. 2018;5:61.
    doi: 10.3389/fvets.2018.00061pmc: PMC5879091pubmed: 29632867google scholar: lookup
  18. Couëtil LL, Rosenthal FS, DeNicola DB, Chilcoat CD. Clinical Signs, Evaluation of Bronchoalveolar Lavage Fluid, and Assessment of Pulmonary Function in Horses with Inflammatory Respiratory Disease. Am. J. Vet. Res. 2001;62:538–546.
    doi: 10.2460/ajvr.2001.62.538pubmed: 11327461google scholar: lookup
  19. Hoffman AM. Bronchoalveolar Lavage: Sampling Technique and Guidelines for Cytologic Preparation and Interpretation. Vet. Clin. N. Am. Equine Pract. 2008;24:423–435.
    doi: 10.1016/j.cveq.2008.04.003pubmed: 18652963google scholar: lookup
  20. Derksen FJ, Brown CM, Sonea I, Darien BJ, Robinson NE. Comparison of Transtracheal Aspirate and Bronchoalveolar Lavage Cytology in 50 Horses with Chronic Lung Disease. Equine Vet. J. 1989;21:23–26.
  21. Malikides N, Hughes K, Hodgson D, Hodgson J. Comparison of Tracheal Aspirates and Bronchoalveolar Lavage in Racehorses 2. Evaluation of the Diagnostic Significance of Neutrophil Percentage. Aust. Vet. J. 2003;81:685–687.
  22. Hoffman AM. Bronchoalveolar Lavage Technique and Cytological Diagnosis of Small Airway Inflammatory Disease. Equine Vet. Educ. 1999;11:330–336.
  23. Orard M, Depecker M, Hue E, Pitel P-H, Couroucé-Malblanc A, Richard EA. Influence of Bronchoalveolar Lavage Volume on Cytological Profiles and Subsequent Diagnosis of Inflammatory Airway Disease in Horses. Vet. J. 2016;207:193–195.
    doi: 10.1016/j.tvjl.2015.09.027pubmed: 27152385google scholar: lookup
  24. Rennard SI, Basset G, Lecossier D, O’Donnell KM, Pinkston P, Martin PG, Crystal RG. Estimation of Volume of Epithelial Lining Fluid Recovered by Lavage Using Urea as Marker of Dilution. J. Appl. Physiol. 1986;60:532–538.
    doi: 10.1152/jappl.1986.60.2.532pubmed: 3512509google scholar: lookup
  25. McGorum BC, Dixon PM, Halliwell REW, Irving P. Evaluation of Urea and Albumen as Endogenous Markers of Dilution of Equine Bronchoalveolar Lavage Fluid. Res. Vet. Sci. 1993;55:52–56.
    doi: 10.1016/0034-5288(93)90033-Cpubmed: 8378613google scholar: lookup
  26. Pirie S. Performance and Airway Disease: A Bidirectional Relationship?. In Proceedings of the ECEIM Congress, Kopenhagen, Denmark, 14–16 November 2024.
  27. Mazan MR, Vin R, Hoffman AM. Radiographic Scoring Lacks Predictive Value in Inflammatory Airway Disease. Equine Vet. J. 2010;37:541–545.
    doi: 10.2746/042516405775314899pubmed: 16295932google scholar: lookup
  28. Simões J, Tilley P. Decision Making in Severe Equine Asthma—Diagnosis and Monitoring. Animals 2023;13:3872.
    doi: 10.3390/ani13243872pmc: PMC10740644pubmed: 38136909google scholar: lookup
  29. Tilley P, Sales Luis JP, Branco Ferreira M. 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;93:1006–1014.
    doi: 10.1016/j.rvsc.2011.10.024pubmed: 22136797google scholar: lookup
  30. Bullone M, Beauchamp G, Godbout M, Martin JG, Lavoie JP. Endobronchial Ultrasound Reliably Quantifies Airway Smooth Muscle Remodeling in an Equine Asthma Model. PLoS ONE 2015;10:e0136284.
  31. Lo Feudo C, Stucchi L, Alberti E, Stancari G, Conturba B, Zucca E, Ferrucci F. The Role of Thoracic Ultrasonography and Airway Endoscopy in the Diagnosis of Equine Asthma and Exercise-Induced Pulmonary Hemorrhage. Vet. Sci. 2021;8:276.
    doi: 10.3390/vetsci8110276pmc: PMC8619806pubmed: 34822649google scholar: lookup
  32. Lavoie-Lamoureux A, Leclere M, Lemos K, Wagner B, Lavoie JP. Markers of Systemic Inflammation in Horses with Heaves. J. Vet. Intern. Med. 2012;26:1419–1426.
  33. Bullone M, De Lagarde M, Vargas A, Lavoie JP. Serum Surfactant Protein D and Haptoglobin as Potential Biomarkers for Inflammatory Airway Disease in Horses. J. Vet. Intern. Med. 2015;29:1707–1711.
    doi: 10.1111/jvim.13602pmc: PMC4895656pubmed: 26289543google scholar: lookup
  34. Gy C, Leclere M, Vargas A, Grimes C, Lavoie J. Investigation of Blood Biomarkers for the Diagnosis of Mild to Moderate Asthma in Horses. J. Vet. Intern. Med. 2019;33:1789–1795.
    doi: 10.1111/jvim.15505pmc: PMC6639487pubmed: 31099114google scholar: lookup
  35. Miskovic Feutz M, Couetil LL, Riley CP, Zhang X, Adamec J, Raskin RE. Secretoglobin and Transferrin Expression in Bronchoalveolar Lavage Fluid of Horses with Chronic Respiratory Disease. J. Vet. Intern. Med. 2015;29:1692–1699.
    doi: 10.1111/jvim.13604pmc: PMC4895674pubmed: 26332291google scholar: lookup
  36. 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;21:149–156.
  37. Hansen S, Otten ND, Spang-Hanssen L, Bendorff C, Jacobsen S. Neutrophil Gelatinase-associated Lipocalin as a Potential Biomarker for Equine Asthma. Equine Vet. J. 2024;56:44–50.
    doi: 10.1111/evj.13939pubmed: 36977608google scholar: lookup
  38. Barton AK, Shety T, Bondzio A, Einspanier R, Gehlen H. Metalloproteinases and Their Tissue Inhibitors in Comparison between Different Chronic Pneumopathies in the Horse. Mediat. Inflamm. 2015;2015:569512.
    doi: 10.1155/2015/569512pmc: PMC4681803pubmed: 26770019google scholar: lookup
  39. Barton AK, Pelli A, Rieger M, Gehlen H. Procalcitonin as a Biomarker in Equine Chronic Pneumopathies. BMC Vet. Res. 2016;12:281.
    doi: 10.1186/s12917-016-0912-4pmc: PMC5148850pubmed: 27938364google scholar: lookup
  40. Janssen P, Tosi I, Hego A, Maréchal P, Marichal T, Radermecker C. Neutrophil Extracellular Traps Are Found in Bronchoalveolar Lavage Fluids of Horses With Severe Asthma and Correlate With Asthma Severity. Front. Immunol. 2022;13:921077.
    doi: 10.3389/fimmu.2022.921077pmc: PMC9326094pubmed: 35911691google scholar: lookup
  41. Art T, Franck T, Lekeux P, de Moffarts B, Couëtil L, Becker M, Kohnen S, Deby-Dupont G, Serteyn D. Myeloperoxidase Concentration in Bronchoalveolar Lavage Fluid from Healthy Horses and Those with Recurrent Airway Obstruction. Can. J. Vet. Res. 2006;70:291–296.
    pmc: PMC1562538pubmed: 17042382
  42. Bazzano M, Laghi L, Zhu C, Magi GE, Tesei B, Laus F. Respiratory Metabolites in Bronchoalveolar Lavage Fluid (BALF) and Exhaled Breath Condensate (EBC) Can Differentiate Horses Affected by Severe Equine Asthma from Healthy Horses. BMC Vet. Res. 2020;16:233.
    doi: 10.1186/s12917-020-02446-9pmc: PMC7346432pubmed: 32641035google scholar: lookup
  43. Giguère S, Viel L, Lee E, MacKay RJ, Hernandez J, Franchini M. Cytokine Induction in Pulmonary Airways of Horses with Heaves and Effect of Therapy with Inhaled Fluticasone Propionate. Vet. Immunol. Immunopathol. 2002;85:147–158.
    doi: 10.1016/S0165-2427(01)00420-2pubmed: 11943316google scholar: lookup
  44. Woodrow JS, Hines M, Sommardahl C, Flatland B, Lo Y, Wang Z, Sheats MK, Lennon EM. Initial Investigation of Molecular Phenotypes of Airway Mast Cells and Cytokine Profiles in Equine Asthma. Front. Vet. Sci. 2023;9:997139.
    doi: 10.3389/fvets.2022.997139pmc: PMC9875299pubmed: 36713876google scholar: lookup
  45. Gray PR, Derksen FJ, Robinson NE, Carpenter-Deyo LJ, Johnson HG, Roth RA. The Role of Cyclooxygenase Products in the Acute Airway Obstruction and Airway Hyperreactivity of Ponies with Heaves. Am. Rev. Respir. Dis. 1989;140:154–160.
    doi: 10.1164/ajrccm/140.1.154pubmed: 2502051google scholar: lookup
  46. Watson ED, Sweeney CR, Steensma KA. Arachidonate Metabolites in Bronchoalveolar Lavage Fluid from Horses with and without COPD. Equine Vet. J. 1992;24:379–381.
  47. Hare JE, Viel L, Conlon PD, Marshall JS. In vitro allergen-induced degranulation of pulmonary mast cells from horses with recurrent airway obsruction (heaves). Am. J. Vet. Res. 1999;60:841–847.
    doi: 10.2460/ajvr.1999.60.07.841pubmed: 10407477google scholar: lookup
  48. Christmann U, Hite RD, Witonsky SG, Buechner-Maxwell VA, Wood PL. Evaluation of Lipid Markers in Surfactant Obtained from Asthmatic Horses Exposed to Hay. Am. J. Vet. Res. 2019;80:300–305.
    doi: 10.2460/ajvr.80.3.300pubmed: 30801214google scholar: lookup
  49. Niedzwiedz A, Borowicz H, Januszewska L, Markiewicz-Gorka I, Jaworski Z. Serum 8-Hydroxy-2-Deoxyguanosine as a Marker of DNA Oxidative Damage in Horses with Recurrent Airway Obstruction. Acta Vet. Scand. 2015;58:38.
    doi: 10.1186/s13028-016-0215-6pmc: PMC4895991pubmed: 27267076google scholar: lookup
  50. Schmallenbach KH, Rahman I, Sasse HHL, Dixon PM, Halliwell REW, McGorum BC, Crameri R, Miller HRP. Studies on Pulmonary and Systemic Aspergillus Fumigatus-Specific IgE and IgG Antibodies in Horses Affected with Chronic Obstructive Pulmonary Disease (COPD). Vet. Immunol. Immunopathol. 1998;66:245–256.
    doi: 10.1016/S0165-2427(98)00202-5pubmed: 9880102google scholar: lookup
  51. Calzetta L, Rogliani P, Page C, Roncada P, Pistocchini E, Soggiu A, Piras C, Urbani A, Matera MG. Clinical Effect of Corticosteroids in Asthma-affected Horses: A Quantitative Synthesis. Equine Vet. J. 2018;50:594–601.
    doi: 10.1111/evj.12815pubmed: 29393535google scholar: lookup
  52. Gehlen H, Oey L, Rohn K, Bilzer T, Stadler P. Pulmonary Dysfunction and Skeletal Muscle Changes in Horses with RAO. J. Vet. Intern. Med. 2008;22:1014–1021.
  53. Ferro E, Ferrucci F, Zucca E, Di Fabio V, Castoldi S. Arterial Blood Gas Analysis in 53 Racehorses with a Diagnosis of Small Airway Inflammatory Disease (SAID). J. Equine Vet. Sci. 2002;22:165–168.
  54. Simões J, Batista M, Tilley P. The Immune Mechanisms of Severe Equine Asthma—Current Understanding and What Is Missing. Animals 2022;12:744.
    doi: 10.3390/ani12060744pmc: PMC8944511pubmed: 35327141google scholar: lookup
  55. Lavoie JP, Phan ST, Blais D. Effects of a combination of detomidine and butorphanol on respiratory function in horses with or without chronic obstructive pulmonary disease. Am. J. Vet. Res. 1996;57:705–709.
    doi: 10.2460/ajvr.1996.57.05.705pubmed: 8723886google scholar: lookup
  56. Nyman G, Marntell S, Edner A, Funkquist P, Morgan K, Hedenstierna G. Effect of Sedation with Detomidine and Butorphanol on Pulmonary Gas Exchange in the Horse. Acta Vet. Scand. 2009;51:22.
    doi: 10.1186/1751-0147-51-22pmc: PMC2694811pubmed: 19422714google scholar: lookup
  57. Marntell S, Nyman G, Funkquist P, Hedenstierna G. Effects of Acepromazine on Pulmonary Gas Exchange and Circulation during Sedation and Dissociative Anaesthesia in Horses. Vet. Anaesth. Analg. 2005;32:83–93.
  58. Durando MM, Martin BB, Davidson EJ, Birks EK. Correlations between Exercising Arterial Blood Gas Values, Tracheal Wash Findings and Upper Respiratory Tract Abnormalities in Horses Presented for Poor Performance. Equine Vet. J. 2006;38:523–528.
  59. Wagner PD, Gillespie JR, Landgren GL, Fedde MR, Jones BW, DeBowes RM, Pieschl RL, Erickson HH. Mechanism of Exercise-Induced Hypoxemia in Horses. J. Appl. Physiol. 1989;66:1227–1233.
    doi: 10.1152/jappl.1989.66.3.1227pubmed: 2496088google scholar: lookup
  60. Nolen-Walston RD, Harris M, Agnew ME, Martin BB, Reef VB, Boston RC, Davidson EJ. Clinical and Diagnostic Features of Inflammatory Airway Disease Subtypes in Horses Examined Because of Poor Performance: 98 Cases (2004–2010). J. Am. Vet. Med. Assoc. 2013;242:1138–1145.
    doi: 10.2460/javma.242.8.1138pubmed: 23547679google scholar: lookup
  61. Miller AB, Harris PA, Barker VD, Adams AA. Short-Term Transport Stress and Supplementation Alter Immune Function in Aged Horses. PLoS ONE 2021;16:e0254139.
  62. Art T, Lekeux P. Ventilatory and Arterial Blood Gas Tension Adjustments to Strenuous Exercise in Standardbreds. Am. J. Vet. Res. 1995;56:1332–1337.
    doi: 10.2460/ajvr.1995.56.10.1332pubmed: 8928951google scholar: lookup
  63. Padilla DJ, McDonough P, Kindig CA, Erickson HH, Poole DC. Ventilatory Dynamics and Control of Blood Gases after Maximal Exercise in the Thoroughbred Horse. J. Appl. Physiol. 2004;96:2187–2193.
  64. Kozłowska N, Wierzbicka M, Jasiński T, Domino M. Advances in the Diagnosis of Equine Respiratory Diseases: A Review of Novel Imaging and Functional Techniques. Animals 2022;12:381.
    doi: 10.3390/ani12030381pmc: PMC8833607pubmed: 35158704google scholar: lookup
  65. 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.
    doi: 10.3390/ani13213387pmc: PMC10649418pubmed: 37958142google scholar: lookup
  66. Agustí A, Celli BR, Criner GJ, Halpin D, Anzueto A, Barnes P, Bourbeau J, Han MK, Martinez FJ, Montes De Oca M. Global Initiative for Chronic Obstructive Lung Disease 2023 Report: GOLD Executive Summary. Eur. Respir. J. 2023;61:2300239.
  67. Evans DL, Kiddell L, Smith CL. Pulmonary Function Measurements Immediately after Exercise Are Correlated with Neutrophil Percentage in Tracheal Aspirates in Horses with Poor Racing Performance. Res. Vet. Sci. 2011;90:510–515.
    doi: 10.1016/j.rvsc.2010.07.003pubmed: 20678784google scholar: lookup
  68. Hoffman AM, Mazan MR. How to Test for Airway Hyper-Reactivity: Toward a Better Diagnosis of Inflammatory Airway Disease. AAEP Proc. 2005;51:265–269.
  69. 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;22:1022–1028.
  70. Nolen-Walston RD, Kuehn H, Boston RC, Mazan MR, Wilkins PA, Bruns S, Hoffman AM. Reproducibility of Airway Responsiveness in Horses Using Flowmetric Plethysmography and Histamine Bronchoprovocation. J. Vet. Intern. Med. 2009;23:631–635.
  71. Van Erck E, Votion D, Art T, Lekeux P. Measurement of Respiratory Function by Impulse Oscillometry in Horses. Equine Vet. J. 2004;36:21–28.
    doi: 10.2746/0425164044864714pubmed: 14756367google scholar: lookup
  72. Frerichs I, Amato MBP, Van Kaam AH, Tingay DG, Zhao Z, Grychtol B, Bodenstein M, Gagnon H, Böhm SH, Teschner E. Chest Electrical Impedance Tomography Examination, Data Analysis, Terminology, Clinical Use and Recommendations: Consensus Statement of the TRanslational EIT developmeNt stuDy Group. Thorax 2017;72:83–93.
  73. Secombe C, Adler A, Hosgood G, Raisis A, Mosing M. Can Bronchoconstriction and Bronchodilatation in Horses Be Detected Using Electrical Impedance Tomography?. J. Vet. Intern. Med. 2021;35:2035–2044.
    doi: 10.1111/jvim.16152pmc: PMC8295671pubmed: 33977584google scholar: lookup
  74. Wang YM, Sun XM, Zhou YM, Chen JR, Cheng KM, Li HL, Yang YL, Zhang L, Zhou JX. Use of Electrical Impedance Tomography (EIT) to Estimate Global and Regional Lung Recruitment Volume (VREC) Induced by Positive End-Expiratory Pressure (PEEP): An Experiment in Pigs with Lung Injury. Med. Sci. Monit. 2020;26:e922609.
    doi: 10.12659/MSM.922609pmc: PMC7094060pubmed: 32172276google scholar: lookup
  75. Herteman N, Mosing M, Waldmann AD, Gerber V, Schoster A. Exercise-induced Airflow Changes in Horses with Asthma Measured by Electrical Impedance Tomography. J. Vet. Intern. Med. 2021;35:2500–2510.
    doi: 10.1111/jvim.16260pmc: PMC8478024pubmed: 34505734google scholar: lookup
  76. Hoffman AM. Clinical Application of Pulmonary Function Testing in Horses. International Veterinary Information Service; Ithaca, NY, USA: 2002.
  77. Lavoie JP, Pascoe JR, Kurpershoek JC. Effect of head and neck position on respiratory mechanics in horses sedated with xylazine. Am. J. Vet. Res. 1992;53:1652–1657.
    doi: 10.2460/ajvr.1992.53.09.1652pubmed: 1416371google scholar: lookup
  78. Richard EA, Fortier GD, Denoix JM, Art T, Lekeux PM, Erck VV. Influence of Subclinical Inflammatory Airway Disease on Equine Respiratory Function Evaluated by Impulse Oscillometry. Equine Vet. J. 2009;41:384–389.
    doi: 10.2746/042516409X366121pubmed: 19562901google scholar: lookup
  79. Wichtel M, Gomez D, Burton S, Wichtel J, Hoffman A. Relationships between Equine Airway Reactivity Measured by Flowmetric Plethysmography and Specific Indicators of Airway Inflammation in Horses with Suspected Inflammatory Airway Disease. Equine Vet. J. 2016;48:466–471.
    doi: 10.1111/evj.12482pubmed: 26174367google scholar: lookup
  80. Cullimore A, Secombe C, Lester G, Robertson I. Bronchoalveolar Lavage Fluid Cytology and Airway Hyper-reactivity in Clinically Normal Horses. Aust. Vet. J. 2018;96:291–296.
    doi: 10.1111/avj.12721pubmed: 30129032google scholar: lookup
  81. 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;34:355–361.
    doi: 10.1111/eve.13418google scholar: lookup
  82. Benamou AE, Art T, Marlin DJ, Roberts CA, Lekeux P. Effect of exercise on concentrations of immunoreactive endothelin in bronchoalveolar lavage fluid of normal horses and horses with chronic obstructive pulmonary disease. Equine Vet. J. 1999;31:92–95.
  83. Malikides N, Hughes K, Hodgson J. Comparison of Tracheal Aspirates before and after High-speed Treadmill Exercise in Racehorses. Aust. Vet. J. 2007;85:414–419.
  84. Martin BB, Beech J, Parente EJ. Cytologic Examination of Specimens Obtained by Means of Tracheal Washes Performed before and after High-Speed Treadmill Exercise in Horses with a History of Poor Performance. J. Am. Vet. Med. Assoc. 1999;214:673–677.
    doi: 10.2460/javma.1999.214.05.673pubmed: 10088017google scholar: lookup
  85. Lee TH, Walport MJ. Exercise-Induced Release of Hisbmine and Neutrophil Chemotactic Factor in Atopic Asthmatics. J. Allergy Clin. Immunol. 1982;70:73–81.
    doi: 10.1016/0091-6749(82)90232-9pubmed: 6178768google scholar: lookup
  86. Zietkowski Z, Skiepko R, Tomasiak-Lozowska MM, Mroczko B, Szmitkowski M, Bodzenta-Lukaszyk A. Changes in High-Sensitivity C-Reactive Protein in Serum and Exhaled Breath Condensate after Intensive Exercise in Patients with Allergic Asthma. Int. Arch. Allergy Immunol. 2010;153:75–85.
    doi: 10.1159/000301582pubmed: 20357488google scholar: lookup
  87. Bikov A, Gajdócsi R, Huszár É, Szili B, Lázár Z, Antus B, Losonczy G, Horvath I. Exercise Increases Exhaled Breath Condensate Cysteinyl Leukotriene Concentration in Asthmatic Patients. J. Asthma. 2010;47:1057–1062.
    doi: 10.1080/02770903.2010.512690pubmed: 20868319google scholar: lookup
  88. Kivity S, Argaman A, Onn A, Shwartz Y, Man A, Greif J, Fireman E. Eosinophil Influx into the Airways in Patients with Exercise-Induced Asthma. Respir. Med. 2000;94:1200–1205.
    doi: 10.1053/rmed.2000.0951pubmed: 11192956google scholar: lookup
  89. Hallstrand TS, Moody MW, Aitken ML, Henderson WR Jr. Airway Immunopathology of Asthma with Exercise-Induced Bronchoconstriction. J. Allergy Clin. Immunol. 2005;116:586–593.
    doi: 10.1016/j.jaci.2005.04.035pmc: PMC2040056pubmed: 16159628google scholar: lookup
  90. Elkhatib SK, Alley J, Jepsen M, Smeins L, Barnes A, Naik S, Ackermann MR, Verhoeven D, Kohut ML. Exercise duration modulates upper and lower respiratory fluid cellularity, antiviral activity, and lung gene expression. Physiol. Rep. 2021;9:e15075.
    doi: 10.14814/phy2.15075pmc: PMC8531599pubmed: 34676696google scholar: lookup
  91. Araneda OF, Carbonell T, Tuesta M. Update on the Mechanisms of Pulmonary Inflammation and Oxidative Imbalance Induced by Exercise. Oxid. Med. Cell. Longev. 2016;2016:4868536.
    doi: 10.1155/2016/4868536pmc: PMC4736402pubmed: 26881028google scholar: lookup
  92. Chimenti L, Morici G, Paternò A, Santagata R, Bonanno A, Profita M, Riccobono L, Bellia V, Bonsignore MR. Bronchial epithelial damage after a half-marathon in nonasthmatic amateur runners. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2010;298:L857–L862.
    doi: 10.1152/ajplung.00053.2010pubmed: 20363849google scholar: lookup
  93. Taylor SD, Ivester KM, Stewart C, Page AE, Horohov DW, Couetil LL. The Effect of Lower Airway Inflammation on Inflammatory Cytokine Gene Expression in Bronchoalveolar Lavage Fluid and Whole Blood in Racing Thoroughbreds. Vet. Immunol. Immunopathol. 2021;237:110266.
    doi: 10.1016/j.vetimm.2021.110266pubmed: 33991760google scholar: lookup
  94. McKANE SA, Rose RJ. Effects of exercise intensity and training on bronchoalveolar lavage cytology. Equine Vet. J. 1995;27:58–62.
  95. McKANE S, Canfield P, Rose R. Equine Bronchoalveolar Lavage Cytology: Survey of Thoroughbred Racehorses in Training. Aust. Vet. J. 1993;70:401–404.
  96. Clark C, Lester G, Vetro T, Rice B. Bronchoalveolar Lavage in Horses: Effect of Exercise and Repeated Sampling on Cytology. Aust. Vet. J. 1995;72:249–252.
  97. Sweeney CR, Kassier Y, Ziemer EL, Lindborg S. Effects of Hing Site and Fluid Volume on Results of Bronchoalveolar Lavage Fluid Analysis in Horses. Am. J. Vet. Res. 1992;53:1376–1379.
    doi: 10.2460/ajvr.1992.53.08.1376pubmed: 1510313google scholar: lookup
  98. Romberg K, Tufvesson E, Bjermer L. Asthma symptoms, mannitol reactivity and exercise-induced bronchoconstriction in adolescent swimmers versus tennis players. J. Asthma Allergy. 2017;10:249–260.
    doi: 10.2147/JAA.S134794pmc: PMC5633302pubmed: 29042799google scholar: lookup
  99. Bonsignore MR, Morici G, Vignola AM, Riccobono L, Bonanno A, Profita M, Abate P, Scichilone N, Amato G, Bellia V. Increased airway inflammatory cells in endurance athletes: What do they mean?. Clin. Exp. Allergy. 2003;33:14–21.
  100. Bonsignore MR, Morici G, Riccobono L, Insalaco G, Bonanno A, Profita M, Paternò A, Vassalle C, Mirabella A, Vignola AM. Airway Inflammation in Nonasthmatic Amateur Runners. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2001;281:L668–L676.
  101. Chimenti L, Morici G, Paternò A, Bonanno A, Siena L, Licciardi A, Veca M, Guccione W, Macaluso F, Bonsignore G. Endurance Training Damages Small Airway Epithelium in Mice. Am. J. Respir. Crit. Care Med. 2007;175:442–449.
    doi: 10.1164/rccm.200608-1086OCpubmed: 17185648google scholar: lookup
  102. Davis M, McKenzie E, Royer C, Williamson K, Payton M, Nelson S. Effect of training and recovery on airway inflammation in an animal model of ‘ski asthma’. Equine Comp. Exerc. Physiol. 2005;2:133–138.
    doi: 10.1079/ECP200558google scholar: lookup
  103. Sue-Chu M. Winter Sports Athletes: Long-Term Effects of Cold Air Exposure. Br. J. Sports Med. 2012;46:397–401.
    doi: 10.1136/bjsports-2011-090822pubmed: 22267570google scholar: lookup
  104. Bougault V, Turmel J, St-Laurent J, Bertrand M, Boulet L-P. Asthma, Airway Inflammation and Epithelial Damage in Swimmers and Cold-Air Athletes. Eur. Respir. J. 2009;33:740–746.
    doi: 10.1183/09031936.00117708pubmed: 19129276google scholar: lookup
  105. Davis MS, Malayer JR, Vandeventer L, Royer CM, McKenzie EC, Williamson KK. Cold Weather Exercise and Airway Cytokine Expression. J. Appl. Physiol. 2005;98:2132–2136.
  106. Mahalingam-Dhingra A, Bedenice D, Mazan MR. Bronchoalveolar Lavage Hemosiderosis in Lightly Active or Sedentary Horses. J. Vet. Intern. Med. 2023;37:1243–1249.
    doi: 10.1111/jvim.16692pmc: PMC10229344pubmed: 36975043google scholar: lookup
  107. Sundman EA, Chigerwe M, Hunyadi LM. A retrospective study of bronchoalveolar lavage fluid analysis in barrel racing horses with exercise-induced pulmonary hemorrhage and asthma in Texas from 2016 to 2018. Res. Vet. Sci. 2020;132:338–341.
    doi: 10.1016/j.rvsc.2020.07.001pubmed: 32738730google scholar: lookup
  108. McKANE SA, Slocombe RF. Experimental mild pulmonary inflammation promotes the development of exercise-induced pulmonary haemorrhage. Equine Vet. J. 2010;42:235–239.
  109. Michelotto PV, Muehlmann LA, Zanatta AL, Bieberbach EWR, Kryczyk M, Fernandes LC, Nishiyama A. Pulmonary inflammation due to exercise-induced pulmonary haemorrhage in Thoroughbred colts during race training. Vet. J. 2011;190:e3–e6.
    doi: 10.1016/j.tvjl.2010.08.009pubmed: 22108190google scholar: lookup
  110. Hooi KS, Defarges AM, Jelovcic SV, Bienzle D. Bronchoalveolar lavage hemosiderosis in dogs and cats with respiratory disease. Vet. Clin. Pathol. 2019;48:42–49.
    doi: 10.1111/vcp.12698pubmed: 30657606google scholar: lookup
  111. DeHeer HL, McManus P. Frequency and severity of tracheal wash hemosiderosis and association with underlying disease in 96 cats: 2002–2003. Vet. Clin. Pathol. 2005;34:17–22.
  112. Eldem İ, İleri T, İnce E, Asarcikli F, Pekpak E, Çakmakli HF, Ceyhan K, Uysal Z. Idiopathic Pulmonary Hemosiderosis With Allergic Asthma Diagnosis in a Pediatric Patient. J. Pediatr. Hematol. Oncol. 2015;37:e435–e437.
    doi: 10.1097/MPH.0000000000000412pubmed: 26241728google scholar: lookup
  113. Hansen S, Otten ND, Nissen SD, Carstensen H, Hopster-Iversen C, Fjeldborg J, Staun SH, Fenner M, Hesselkilde EM, Buhl R. Atrial Fibrillation as a Risk Factor for Exercise-induced Pulmonary Haemorrhage Following a Standardised Exercise Test. Equine Vet. J. 2024;56:552–561.
    doi: 10.1111/evj.13995pubmed: 37654233google scholar: lookup
  114. Burns JJ, MacMillan KM, John E. Prevalence of Exercise-Induced Pulmonary Hemorrhage, Tracheal Mucus and Recurrent Laryngeal Neuropathy in Competitive Draft Pulling Horses. J. Equine Vet. Sci. 2023;129:104895.
    doi: 10.1016/j.jevs.2023.104895pubmed: 37517672google scholar: lookup

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