Co-Occurrence of Equine Asthma and Pharyngeal Lymphoid Hyperplasia in Pleasure Horses
Abstract
:1. Introduction
2. Materials and Methods
2.1. Horses
2.2. Detailed Respiratory Tract Examination and Resting Endoscopy
2.3. Tracheal Wash and Bronchoalveolar Lavage Fluid
2.4. Classification of Equine Asthma
2.5. Classification of Pharyngeal Lymphoid Hyperplasia
2.6. Statistical Analysis
2.6.1. Descriptive Statistics
2.6.2. Co-Occurrence of EA with PLH
2.6.3. Severity of Clinical Symptoms
2.6.4. Tracheal and Nasopharyngeal Mucus Accumulation
2.6.5. Correlations with Age and Environmental Descriptors
3. Results
3.1. Descriptive Statistics Results
3.2. Co-Occurrence of EA with PLH
3.3. Severity of Clinical Symptoms
3.4. Tracheal and Nasopharyngeal Mucus Accumulation
3.5. Correlations with Age and Environmental Descriptors
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Grossman, J. One Airway, One Disease. Chest 1997, 111, 11S–16S. [Google Scholar] [CrossRef]
- Giovannini-Chami, L.; Paquet, A.; Sanfiorenzo, C.; Pons, N.; Cazareth, J.; Magnone, V.; Lebrigand, K.; Chevalier, B.; Vallauri, A.; Julia, V.; et al. The “One Airway, One Disease” Concept in Light of Th2 Inflammation. Eur. Respir. J. 2018, 52, 1800437. [Google Scholar] [CrossRef]
- Chang, C.C. Sinusitis, rhinitis, asthma, and the single airway hypothesis. In Diseases of the Sinuses: A Comprehensive Textbook of Diagnosis and Treatment; Springer Science+Business Media: New York, NY, USA, 2014; pp. 173–194. [Google Scholar] [CrossRef]
- Plaschke, P.P.; Janson, C.; Norrman, E.; Björnsson, E.; Ellbjär, S.; Järvholm, B. Onset and Remission of Allergic Rhinitis and Asthma and the Relationship with Atopic Sensitization and Smoking. Am. J. Respir. Crit. Care Med. 2000, 162, 920–924. [Google Scholar] [CrossRef]
- Fokkens, W.; Lund, V.; Mullol, J. European Position Paper on Rhinosinusitis and Nasal Polyps group European Position Paper on Rhinosinusitis and Nasal Polyps 2007. Rhinol. Suppl. 2007, 20, 1–136. [Google Scholar]
- Joó, K.; Povázsai, Á.; Nyerges-Bohák, Z.; Szenci, O.; Kutasi, O. Asthmatic Disease as an Underlying Cause of Dorsal Displacement of the Soft Palate in Horses. J. Equine Vet. Sci. 2021, 96, 103308. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Lo Feudo, C.M.; 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. [Google Scholar] [CrossRef]
- King, D.S.; Tulleners, E.; Martin, B.B.; Parente, E.J.; Boston, R. Clinical Experiences with Axial Deviation of the Aryepiglottic Folds in 52 Racehorses. Vet. Surg. 2001, 30, 151–160. [Google Scholar] [CrossRef]
- Couroucé, A.; Geffroy, O.; Barrey, E.; Auvinet, B.; Rose, R.J. Comparison of Exercise Tests in French Trotters under Training Track, Racetrack and Treadmill Conditions. Equine Vet. J. Suppl. 1999, 31, 528–532. [Google Scholar] [CrossRef]
- Van Erck, E. Dynamic Respiratory Videoendoscopy in Ridden Sport Horses: Effect of Head Flexion, Riding and Airway Inflammation in 129 Cases. Equine Vet. J. 2011, 43, 18–24. [Google Scholar] [CrossRef]
- Cook, W.R.; Williams, R.M.; Kirker-Head, C.A.; Verbridge, D.J. Upper Airway Obstruction (Partial Asphyxia) as the Possible Cause of Exercise-Induced Pulmonary Hemorrhage in the Horse: An Hypothesis. J. Equine Vet. Sci. 1988, 8, 11–26. [Google Scholar] [CrossRef]
- McKane, S.A.; Slocombe, R.F. Experimental Mild Pulmonary Inflammation Promotes the Development of Exercise-Induced Pulmonary Haemorrhage. Equine Vet. J. Suppl. 2010, 42, 235–239. [Google Scholar] [CrossRef]
- Couetil, L.; Cardwell, J.M.; Leguillette, R.; Mazan, M.; Richard, E.; Bienzle, D.; Bullone, M.; Gerber, V.; Ivester, K.; Lavoie, J.-P.; et al. Equine Asthma: Current Understanding and Future Directions. Front. Vet. Sci. 2020, 7, 450. [Google Scholar] [CrossRef]
- Ivester, K.M.; Couëtil, L.L.; Moore, G.E. An Observational Study of Environmental Exposures, Airway Cytology, and Performance in Racing Thoroughbreds. J. Vet. Intern. Med. 2018, 32, 1754–1762. [Google Scholar] [CrossRef]
- Wasko, A.J.; Barkema, H.W.; 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, 145–152. [Google Scholar] [CrossRef]
- Couëtil, L.L.; Cardwell, J.M.; Gerber, V.; Lavoie, J.-P.; Léguillette, R.; Richard, E.A. Inflammatory Airway Disease of Horses--Revised Consensus Statement. J. Vet. Intern. Med. 2016, 30, 503–515. [Google Scholar] [CrossRef]
- Bhaskar, B.; Fraser, J.F. Negative Pressure Pulmonary Edema Revisited: Pathophysiology and Review of Management. Saudi J. Anaesth. 2011, 5, 308–313. [Google Scholar] [CrossRef]
- Holcombe, S.J.; Robinson, N.E.; Derksen, F.J.; Bertold, B.; Genovese, R.; Miller, R.; de Feiter Rupp, H.; Carr, E.A.; Eberhart, S.W.; Boruta, D.; et al. Effect of Tracheal Mucus and Tracheal Cytology on Racing Performance in Thoroughbred Racehorses. Equine Vet. J. 2006, 38, 300–304. [Google Scholar] [CrossRef]
- Koblinger, K.; Nicol, J.; McDonald, K.; Wasko, A.; Logie, N.; Weiss, M.; Léguillette, R. Endoscopic Assessment of Airway Inflammation in Horses. J. Vet. Intern. Med. 2011, 25, 1118–1126. [Google Scholar] [CrossRef]
- Sullivan, E.K.; Parente, E.J. Disorders of the Pharynx. Vet. Clin. Equine Pract. 2003, 19, 159–167. [Google Scholar] [CrossRef]
- Holcombe, S.; Ducharme, N. Disorders of the Nasopharynx and Soft Palate. In Equine Respiratory Medicine and Surgery; Saunders Elsevier: Philadelphia, PA, USA, 2007; pp. 437–457. ISBN 978-0-7020-2759-8. [Google Scholar]
- Lo Feudo, C.M.; Stancari, G.; Collavo, F.; Stucchi, L.; Conturba, B.; Zucca, E.; Ferrucci, F. Upper and Lower Airways Evaluation and Its Relationship with Dynamic Upper Airway Obstruction in Racehorses. Animals 2022, 12, 1563. [Google Scholar] [CrossRef]
- Tessier, C. The Equine Nasopharynx in Dynamic Upper Airway Disorders: An Update. Pferdeheilkunde 2006, 22, 565–568. [Google Scholar] [CrossRef]
- Saulez, M.N.; Gummow, B. Prevalence of Pharyngeal, Laryngeal and Tracheal Disorders in Thoroughbred Racehorses, and Effect on Performance. Vet. Rec. 2009, 165, 431–435. [Google Scholar] [CrossRef]
- Hobo, S.; Matsuda, Y.; Yoshida, K. Prevalence of Upper Respiratory Tract Disorders Detected with a Flexible Videoendoscope in Thoroughbred Racehorses. J. Vet. Med. Sci. 1995, 57, 409–413. [Google Scholar] [CrossRef]
- Gerber, V.; Straub, R.; Marti, E.; Hauptman, J.; Herholz, C.; King, M.; Imhof, A.; Tahon, L.; Robinson, N.E. 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. [Google Scholar] [CrossRef]
- Holcombe, S.J.; Jackson, C.; Gerber, V.; Jefcoat, A.; Berney, C.; Eberhardt, S.; Robinson, N.E. Stabling Is Associated with Airway Inflammation in Young Arabian Horses. Equine Vet. J. 2001, 33, 244–249. [Google Scholar] [CrossRef]
- Léguillette, R.; Lavoie, J.-P. Effects of the Bronchoalveolar Lavage Procedure on Lung Function in Horses with Clinical Exacerbation of Recurrent Airway Obstruction. Am. J. Vet. Res. 2006, 67, 1929–1933. [Google Scholar] [CrossRef]
- Tilley, P.; Sales Luis, J.P.; 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. [Google Scholar] [CrossRef]
- Wysocka, B.; Kluciński, W. Usefulness of the Assessment of Discharge Accumulation in the Lower Airways and Tracheal Septum Thickening in the Differential Diagnosis of Recurrent Airway Obstruction (RAO) and Inflammatory Airway Disease (IAD) in the Horse. Pol. J. Vet. Sci. 2014, 17, 247–253. [Google Scholar] [CrossRef] [PubMed]
- Gerber, V.; Lindberg, Å.; Berney, C.; Robinson, N.E. Airway Mucus in Recurrent Airway Obstruction– Short-Term Response to Environmental Challenge. J. Vet. Intern. Med. 2004, 18, 92–97. [Google Scholar] [CrossRef] [PubMed]
- Sliwinski, H.; Krabisch, P.; Rosenberger, E.; Schwarz, F.J. Hygienic Quality of Different Forages and Concentrates for Horses. Pferdeheilkunde Equine Med. 2005, 21, 26. [Google Scholar] [CrossRef]
- Intemann, S.; Reckels, B.; Schubert, D.C.; Wolf, P.; Kamphues, J.; Visscher, C. The Microbiological Quality of Concentrates for Horses—A Retrospective Study on Influencing Factors and Associations with Clinical Symptoms Reported by Owners or Referring Vets. Vet. Sci. 2022, 9, 413. [Google Scholar] [CrossRef] [PubMed]
- Vandenput, S.; Istasse, L.; Nicks, B.; Lekeux, P. Airborne Dust and Aeroallergen Concentrations in Different Sources of Feed and Bedding for Horses. Vet. Q. 1997, 19, 154–158. [Google Scholar] [CrossRef]
- Bagshaw, J.; Sanz, M.; Wang, Y.; Shoemaker, S.; Bayly, W. Severity and Effects of Pharyngeal Lymphoid Hyperplasia Vary with Age and Racetrack Location in Thoroughbred Racehorses. Comp. Exerc. Physiol. 2023, 1, 1–12. [Google Scholar] [CrossRef]
- Clarke, A.F.; Madelin, T.M.; Allpress, R.G. The Relationship of Air Hygiene in Stables to Lower Airway Disease and Pharyngeal Lymphoid Hyperplasia in Two Groups of Thoroughbred Horses. Equine Vet. J. 1987, 19, 524–530. [Google Scholar] [CrossRef]
- Van Cleemput, J.; Poelaert, K.C.K.; Laval, K.; Impens, F.; Van den Broeck, W.; Gevaert, K.; Nauwynck, H.J. Pollens Destroy Respiratory Epithelial Cell Anchors and Drive Alphaherpesvirus Infection. Sci. Rep. 2019, 9, 4787. [Google Scholar] [CrossRef]
- Cook, W.R. Some Observations on Diseases of the Ear, Nose and Throat in the Horse, and Endoscopy Using a Flexible Fibreoptic Endoscope. Vet. Rec. 1974, 94, 533–541. [Google Scholar] [CrossRef] [PubMed]
- Blakeslee, J.R., Jr.; Olsen, R.G.; McAllister, E.S.; Fassbender, J.; Dennis, R. Evidence of Respiratory Tract Infection Induced by Equine Herpesvirus, Type 2, in the Horse. Can. J. Microbiol. 1975, 21, 1940–1946. [Google Scholar] [CrossRef]
- Holcombe, S.J.; Derksen, F.J.; Berney, C.; Becker, A.C.; Horner, N.T. Effect of Topical Anesthesia of the Laryngeal Mucosa on Upper Airway Mechanics in Exercising Horses. Am. J. Vet. Res. 2001, 62, 1706–1710. [Google Scholar] [CrossRef]
- Raker, C.W. Diseases of the Pharynx. Mod. Vet. Pract. 1976, 57, 396–400. [Google Scholar]
- Simões, J.; Tilley, P. Decision Making in Severe Equine Asthma—Diagnosis and Monitoring. Animals 2023, 13, 3872. [Google Scholar] [CrossRef] [PubMed]
- Hansen, S.; Honoré, M.L.; Riihimaki, M.; Pringle, J.; Ammentorp, A.H.; 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. [Google Scholar] [CrossRef]
- Gerber, V.; Robinson, N.E.; 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. [Google Scholar] [CrossRef] [PubMed]
- Phipps, R.J.; Richardson, P.S. The Effects of Irritation at Various Levels of the Airway upon Tracheal Mucus Secretion in the Cat. J. Physiol. 1976, 261, 563–581. [Google Scholar] [CrossRef] [PubMed]
- Rothe, T.; Karrer, W. Functional Upper Airway Obstruction and Chronic Irritation of the Larynx. Eur. Respir. J. 1998, 11, 498–500. [Google Scholar] [CrossRef]
- Auer, D.E.; Wilson, R.G.; Groenendyk, S. Pharyngeal Lymphoid Hyperplasia in Thoroughbred Racehorses in Training. Aust. Vet. J. 1985, 62, 124–126. [Google Scholar] [CrossRef]
Clinical Signs | Descriptor | Score |
---|---|---|
Respiratory rate | <16 | 0 |
17–20 | 1 | |
21–30 | 2 | |
>30 | 3 | |
Nasal discharge | none | 0 |
serous | 1 | |
mucopurulent/epistaxis | 2 | |
Tracheal auscultation | normal tracheal sounds | 0 |
slight increase | 1 | |
clearly audible increased | 2 | |
crackles and wheezing present | 3 | |
Thorax auscultation | normal pulmonary sounds | 0 |
slight increased pulmonary sounds | 1 | |
clearly audible increased pulmonary sounds | 2 | |
crackles and wheezing present | 3 | |
Nostril flare | none | 0 |
present | 1 | |
Cough score | none | 0 |
coughs at specific times of day (feeding/exercising/making beds) | 1 | |
frequent cough | 2 | |
Abdominal lift | none | 0 |
slight flattening of ventral flank | 1 | |
obvious abdominal lift and “heave line” | 2 | |
Maximum score | 16 |
Endoscopic Signs | Descriptor | Score |
---|---|---|
Neutrophil percentage in BALf | <5% | 0 |
5–20 | 1 | |
20–60% | 2 | |
>60% | 3 | |
Neutrophil percentage in TW | <20% | 0 |
20–60% | 1 | |
>60% | 2 | |
Tracheal mucus accumulation | None | 0 |
little, multiple small blobs | 1 | |
moderate, larger blobs | 2 | |
confluent or stream–forming thick white to yellow | 3 | |
pool forming mucus | 4 | |
profuse amounts of mucus | 5 |
Endoscopic Signs | Descriptor | Scores |
---|---|---|
Nasopharyngeal mucosa | no visible lymphoid tissue | 0 |
few small white follicles over the dorsal wall | 1 | |
numerous small follicles on the dorsal and lateral nasopharyngeal wall | 2 | |
hyperemic follicles over the entire dorsal and lateral wall | 3 | |
large edematous hyperemic follicles coalesce broad-based polypoid aggregate | 4 | |
Nasopharyngeal mucus accumulation | no visible mucus | 0 |
little blobs of mucus presented ventrally and abaxially to the epiglottis | 1 | |
confluent mucus presented ventrally and dorsally to the epiglottis | 2 | |
large amount of dense mucus | 3 |
EA | EA-Free | MEA | SEA | Total | |
---|---|---|---|---|---|
PLH | Grade 0 | 6 (60.0%; 7.5%) | 2 (8.7%; 2.5%) | 0 | 8 (10.0%) |
Grade 1 | 4 (40.0%; 5.0%) | 8 (34.8%; 10.0%) | 11 (23.4%; 13.8%) | 23 (28.8%) | |
Grade 2 | 0 | 11 (47.8%; 13.8%) | 19 (40.4%; 23.8%) | 30 (37.5%) | |
Grade 3 | 0 | 2 (8.7%; 2.5%) | 17 (36.2%; 21.3%) | 19 (23.8%) | |
Total | 10 (100%; 12.5%) | 23 (100%; 28.8%) | 47 (100%; 58.8%) | 80 (100%; 100%) | |
EA-free/MEA/SEA: Chi-square test; p < 0.0001 | MEA/SEA: Chi-square test; p = 0.025 |
Age and Environment | Detail Descriptors | Clinical Symptoms | EA | PLH | TM | NM |
---|---|---|---|---|---|---|
Age | ρ = 0.32; p = 0.004 | ρ = 0.32; p = 0.004 | - | ρ = 0.26; p = 0.01 | - | |
Feeding regimen | hay and concentrates | - | - | - | - | - |
soaked hay and concentrates | - | - | - | - | - | |
only hay | - | - | - | - | - | |
only soaked hay | ρ = −0.32; p = 0.003 | ρ = −0.40; p = 0.002 | ρ = −0.33; p = 0.003 | ρ = −0.29; p = 0.007 | ρ = −0.26; p = 0.02 | |
Housing type | boxes & outside or window | - | - | ρ = −0.24; p = 0.03 | - | ρ = −0.23; p = 0.04 |
boxes & corridor | - | - | - | - | - | |
free-range stable | - | - | - | - | - | |
Stable ventilation | very good | - | - | - | - | ρ = −0.19; p = 0.04 |
good | - | - | - | - | ρ = −0.24; p = 0.03 | |
poor | - | - | - | - | - | |
bad | ρ = 0.27; p = 0.01 | - | - | ρ = 0.28; p = 0.01 | - | |
Stable cleaning | >twice a day | - | - | - | - | - |
twice a day | - | - | ρ = −0.26; p = 0.02 | - | ρ = −0.25; p = 0.01 | |
once a day | - | - | - | - | - | |
<once a day | ρ = 0.31; p = 0.005 | - | - | - | ρ = 0.30; p = 0.007 | |
Hay and straw storage | building outside the stable | - | - | ρ = −0.24; p = 0.03 | - | ρ = −0.23; p = 0.04 |
in stable in separate box/storage space | - | - | - | - | - | |
in stable in the attic | - | - | - | - | ρ = 0.23; p = 0.04 | |
Daily access to the paddock | grassy pasture | - | - | - | - | - |
sandy paddock | - | - | - | - | - |
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Kozłowska, N.; Wierzbicka, M.; Jasiński, T.; Domino, M. Co-Occurrence of Equine Asthma and Pharyngeal Lymphoid Hyperplasia in Pleasure Horses. Agriculture 2024, 14, 1157. https://doi.org/10.3390/agriculture14071157
Kozłowska N, Wierzbicka M, Jasiński T, Domino M. Co-Occurrence of Equine Asthma and Pharyngeal Lymphoid Hyperplasia in Pleasure Horses. Agriculture. 2024; 14(7):1157. https://doi.org/10.3390/agriculture14071157
Chicago/Turabian StyleKozłowska, Natalia, Małgorzata Wierzbicka, Tomasz Jasiński, and Małgorzata Domino. 2024. "Co-Occurrence of Equine Asthma and Pharyngeal Lymphoid Hyperplasia in Pleasure Horses" Agriculture 14, no. 7: 1157. https://doi.org/10.3390/agriculture14071157