Exercise Induced Pulmonary Hemorrhage in Horses: American College of Veterinary Internal Medicine Consensus Statement

Journal of Veterinary Internal Medicine

Volumn 29, Issue 3, 2015, Pages 743-758

  Hinchcliff, K W ^a   Couetil, L L ^b   Knight, P K ^c   Morley, P S ^d   Robinson, N E ^e   Sweeney, C R ^f   van Erck, E ^g  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF SYDNEY   (Australia)

^d Veterinary Dentistry and Oral Surgery   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g Equine Sports Medicine Practice   (Belgium)

Author keywords

Bleeding; Lungs; Physiology; Respiratory

Indexed keywords

ANIMALIA; CONGIOPODIDAE; EQUIDAE;

FUROSEMIDE;

ADVERSE EFFECTS; ANIMAL; ANIMAL EXPERIMENT; CONSENSUS; FEMALE; HEMORRHAGE; HORSE; HORSE DISEASES; LUNG DISEASES; MALE; VETERINARY; VETERINARY SPORTS MEDICINE;

ANIMALS; CONSENSUS; FEMALE; FUROSEMIDE; HEMORRHAGE; HORSE DISEASES; HORSES; LUNG DISEASES; MALE; PHYSICAL CONDITIONING, ANIMAL; VETERINARY SPORTS MEDICINE;

EID: 84929774226     PISSN: 08916640     EISSN: 19391676     Source Type: Journal    
DOI: 10.1111/jvim.12593     Document Type: Article

References (97)

1. Heller B. Run Baby Run: What Every Owner, Breeder and Handicapper Should Know About Lasix in Racehorses. Neenah, WI: Russell Meerdink, 2002.
2. Guyatt GH, Oxman AD, Schünemann HJ, et al. GRADE guidelines: A new series of articles in the Journal of Clinical Epidemiology. J Clin Epidemiol 2011;64:380-382.
3. Group TGW. GRADE Working Group, 2013.
4. Guyatt G, Oxman AD, Akl EA, et al. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. J Clin Epidemiol 2011;64:383-394.
5. Guyatt GH, Oxman AD, Kunz R, et al. GRADE guidelines: 2. Framing the question and deciding on important outcomes. J Clin Epidemiol 2011;64:395-400.
6. Guyatt GH, Oxman AD, Santesso N, et al. GRADE guidelines: 12. Preparing Summary of Findings tables-binary outcomes. J Clin Epidemiol 2013;66:158-172.
7. Guyatt GH, Thorlund K, Oxman AD, et al. GRADE guidelines: 13. Preparing Summary of Findings tables and evidence profiles-continuous outcomes. J Clin Epidemiol 2013;66:173-183.
8. Hinchcliff KW. Tracheobronchoscopic assessment of exercise-induced pulmonary hemorrhage in horses. Am J Vet Res 2005;66:596.
9. Pascoe JR, Ferraro GL, Cannon JH, et al. Exercise-induced pulmonary hemorrhage in racing thoroughbreds: a preliminary study. Am J Vet Res 1981;42:703-707.
10. Christley RM, Hodgson DR, Rose RJ, et al. Coughing in thoroughbred racehorses: Risk factors and tracheal endoscopic and cytological findings. Vet Rec 2001;148:99-104.
11. O'Callaghan MW, Pascoe JR, O'Brien TR, et al. Exercise-induced pulmonary haemorrhage in the horse: Results of a detailed clinical, post mortem and imaging study. VI. Radiological/pathological correlations. Equine Vet J 1987;19:419-422.
12. Pascoe JR, O'Brien TR, Wheat JD, et al. Radiographic aspects of exercise-induced pulmonary hemorrhage in racing horses. Vet Radiol 1983;24:85-92.
13. Doucet MY, Viel L. Clinical, radiographic, endoscopic, bronchoalveolar lavage and lung biopsy findings in horses with exercise-induced pulmonary hemorrhage. Can Vet J 2002;43:195-202.
14. O'Callaghan MW, Goulden B. Radiographic changes in the lungs of horses with exercise-induced epistaxis. N Z Vet J 1982;30:117-118.
15. Ferrucci F. Specificity and sensitivity of ultrasonography and endoscopy for the diagnosis of exercise-induced pulmonary haemorrhage (EIPH) in 157 race horses. Vet Res Commun 2009;33:185.
16. Couetil LL, Denicola DB. Blood gas, plasma lactate and bronchoalveolar lavage cytology analyses in racehorses with respiratory disease. Equine Vet J 1999;31:77-82.
17. Davidson EJ, Harris M, Martin BB, et al. Exercising blood gas analysis, dynamic upper respiratory tract obstruction, and postexercising bronchoalveolar lavage cytology-a comparative study in poor performing horses. J Equine Vet Sci 2011;31:475-480.
18. Sanchez A, Couetil LL, Ward MP, et al. Effect of airway disease on blood gas exchange in racehorses. J Vet Intern Med 2005;19:87-92.
19. Courouce-Malblanc A, Pronost S, Fortier G, et al. Physiological measurements and upper and lower respiratory tract evaluation in French Standardbred Trotters during a standardised exercise test on the treadmill. Equine Vet J Suppl 2002;Suppl 34:402-407.
20. Boden LA, Charles JA, Slocombe RF, et al. Sudden death in racing Thoroughbreds in Victoria, Australia. Equine Vet J 2005;37:269-271.
21. Lyle CH. Sudden death in racing Thoroughbred horses: An international multicentre study of post mortem findings. Equine Vet J 2011;43:324.
22. Sullivan SL, Anderson GA, Morley PS, et al. Prospective study of the association between exercise-induced pulmonary haemorrhage and long-term performance in Thoroughbred racehorses. Equine Vet J 2015;47:350-357.
23. Langford JL, Langford PC, Thomson PK, et al. Epistaxis in racehorses: Risk factors and effects on career. Aust Vet J 2013;91:198-203.
24. O'Callaghan MW, Pascoe JR, Tyler WS, et al. Exercise-induced pulmonary haemorrhage in the horse: Results of a detailed clinical, post mortem and imaging study. V. Microscopic observations. Equine vet J 1987;19:411-418.
25. Derksen FJ. Pulmonary response to airway instillation of autologous blood in horses. Equine Vet J 2007;39:334.
26. McKane SA, Slocombe RF. Sequential changes in bronchoalveolar cytology after autologous blood inoculation. Equine Vet J Suppl 1999;30:126-130.
27. McKane SA, Slocombe RF. Alveolar fibrosis and changes in equine lung morphometry in response to intrapulmonary blood. Equine Vet J Suppl 2002;34:451-458.
28. Williams KJ, Derksen FJ, Defeijter-Rupp HL, et al. Repeated blood instillation into the airway of the horse does not cause pulmonary fibrosis. Equine Vet J 2011;43:354-358.
29. McKane SA, Slocombe RF. Experimental mild pulmonary inflammation promotes the development of exercise-induced pulmonary haemorrhage. Equine Vet J Suppl 2010;42:Suppl 38:235-239.
30. Newton JR, Wood JL. Evidence of an association between inflammatory airway disease and EIPH in young Thoroughbreds during training. Equine Vet J Suppl 2002;Suppl 34:417-424.
31. Chapman PS, Green C, Main JP, et al. Retrospective study of the relationships between age, inflammation and the isolation of bacteria from the lower respiratory tract of thoroughbred horses. Vet Rec 2000;146:91-95.
32. Oikawa M. Exercise-induced haemorrhagic lesions in the dorsocaudal extremities of the caudal lobes of the lungs of young thoroughbred horses. J Comp Pathol 1999;121:339-347.
33. Williams KJ, Robinson NE, DeFeijter-Rupp H, et al. Distribution of venous remodeling in exercise-induced pulmonary hemorrhage of horses follows reported blood flow distribution in the equine lung. J Appl Physiol 2013;114:869-878.
34. West JB, Mathieu-Costello O, Jones JH, et al. Stress failure of pulmonary capillaries in racehorses with exercise-induced pulmonary hemorrhage. J Appl Physiol 1993;75:1097-1109.
35. Williams KJ, Derksen FJ, de Feuter-Rupp H, et al. Regional pulmonary veno-occlussion: A newly identified lesion of equine exercise-induced pulmonary hemorrhage. Vet Pathol 2008;45:316-326.
36. Hillidge CJ, Lane TJ, Johnson EL, et al. Preliminary investigations of exercise-induced pulmonary hemorrhage in racing Quarter Horses. J Equine Vet Sci 1984;4:21-23.
37. Raphel CF, Soma LR. Exercise-induced pulmonary hemorrhage in Thoroughbred after racing and breezing. Am J Vet Res 1982;43:1123-1127.
38. Hinchcliff KW, Morley PS, Jackson MA, et al. Risk factors for exercise-induced pulmonary haemorrhage in Thoroughbred racehorses. Equine Vet J 2010;42(Suppl. 38):228-234.
39. Newton JR, Rogers K, Marlin DJ, et al. Risk factors for epistaxis on British racecourses: Evidence for locomotory impact-induced trauma contributing to the aetiology of exercise-induced pulmonary haemorrhage. Equine Vet J 2005;37:402-411.
40. Takahashi T, Hiraga A, Ohmura H, et al. Frequency of and risk factors for epistaxis associated with exercise-induced pulmonary hemorrhage in horses: 251, 609 race starts (1992-1997). J Am Vet Med Assoc 2001;218:1462-1464.
41. Weideman H, Schoeman SJ, Jordaan GF, et al. Epistaxis related to exercise-induced pulmonary haemorrhage in south African Thoroughbreds. J S Afr Vet Assoc 2003;74:127-131.
42. Weideman H, Schoeman SJ, Jordaan GF. The inheritance of liability to epistaxis in the southern African Thoroughbred. J S Afr Vet Assoc 2004;75:158-162.
43. Velie BD, Raadsma HW, Wade CM, et al. Heritability of epistaxis in the Australian Thoroughbred racehorse population. Vet J 2014; 202: 274-278.
44. de Mello Costa MF, Thomassian A, Gomes TS, et al. Study of exercise induced pulmonary haemorrhage (EIPH) in flat racing Thoroughbred horses through 1889 respiratory endoscopies after races. Revista Brasileira de Ciência Veterinária 2005;12:89-91.
45. Hinchcliff KW, Jackson MA, Morley PS, et al. Association between exercise-induced pulmonary hemorrhage and performance in Thoroughbred racehorses. J Am Vet Med Assoc 2005;227:768-774.
46. Costa MFM, Thomassian A. Evaluation of race distance, track surface and season of the year on exercise-induced pulmonary haemorrhage in flat racing thoroughbreds in Brazil. Equine Vet J Suppl 2006;Suppl 36:87-89.
47. Birks EK, Shuler KM, Soma LR, et al. EIPH: Postrace endoscopic evaluation of Standardbreds and Thoroughbreds. Equine Vet J Suppl 2002;34:375-378.
48. Lapointe JM, Vrins A, McCarvill E. A survey of exercise-induced pulmonary haemorrhage in Quebec standardbred racehorses. Equine Vet J 1994;26:482-485.
49. MacNamara B, Bauer S, Iafe J. Endoscopic evaluation of exercise-induced pulmonary hemorrhage and chronic obstructive pulmonary disease in association with poor performance in racing Standardbreds. J Am Vet Med Assoc 1990;196:443-445.
50. Manohar M, Goetz TE, Rothenbaum P, et al. Clenbuterol administration does not enhance the efficacy of furosemide in attenuating the exercise-induced pulmonary capillary hypertension in Thoroughbred horses. J Vet Pharmacol Ther 2000;23:389-395.
51. Manohar M, Goetz TE, Sullivan E, et al. Pulmonary vascular pressures of strenuously exercising Thoroughbreds after administration of varying doses of frusemide. Equine Vet J 1997;29:298-304.
52. Sweeney CR, Soma LR. Exercise-induced pulmonary hemorrhage in thoroughbred horses: Response to furosemide or hesperidin-citrus bioflavinoids. J Am Vet Med Assoc 1984;185:195-197.
53. Geor RJ, Ommundson L, Fenton G, et al. Effects of an external nasal strip and frusemide on pulmonary haemorrhage in Thoroughbreds following high-intensity exercise. Equine Vet J 2001;33:577-584.
54. Kindig CA, McDonough P, Fenton G, et al. Efficacy of nasal strip and furosemide in mitigating EIPH in Thoroughbred horses. J Appl Physiol 2001;91:1396-1400.
55. Hinchcliff KW. Efficacy of furosemide for prevention of exercise-induced pulmonary hemorrhage in Thoroughbred racehorses. J Am Vet Med Assoc 2009;235:76.
56. Pascoe JR, McCabe AE, Franti CE, et al. Efficacy of furosemide in the treatment of exercise-induced pulmonary hemorrhage in Thoroughbred racehorses. Am J Vet Res 1985;46:2000-2003.
57. Manohar M. Furosemide attenuates the exercise-induced increase in pulmonary artery wedge pressure in horses. Am J Vet Res 1993;54:952-958.
58. Manohar M, Goetz TE, Rothenbaum P, et al. Intravenous pentoxifylline does not enhance the pulmonary haemodynamic efficacy of frusemide in strenuously exercising thoroughbred horses. Equine Vet J 2001;33:354-359.
59. Magid JH, Manohar M, Goetz TE, et al. Pulmonary vascular pressures of thoroughbred horses exercised 1, 2, 3 and 4 h after furosemide administration. J Vet Pharmacol Ther 2000;23:81-89.
60. Gleed FD, Ducharme NG, Hackett RP, et al. Effects of frusemide on pulmonary capillary pressure in horses exercising on a treadmill. Equine Vet J Suppl 1999;31:102-106.
61. Manohar M. Pulmonary vascular pressures of strenuously exercising thoroughbreds after administration of flunixin meglumine and furosemide. Am J Vet Res 1994;55:1308-1312.
62. Manohar M, Hutchens E, Coney E. Frusemide attenuates the exercise-induced rise in pulmonary capillary blood pressure in horses. Equine Vet J 1994;26:51-54.
63. Olsen SC, Coyne CP, Lowe BS, et al. Influence of furosemide on hemodynamic responses during exercise in horses. Am J Vet Res 1992;53:742-747.
64. Gleed FD, Ducharme NG, Hackett RP, et al. Effects of frusemide on pulmonary capillary pressure in horses exercising on a treadmill. Equine Vet J Suppl 1999;30:102-106.
65. O'Callaghan MW, Pascoe JR, Tyler WS, et al. Exercise-induced pulmonary haemorrhage in the horse: Results of a detailed clinical, post mortem and imaging study. II. Gross lung pathology. Equine Vet J 1987;19:389-393.
66. Buchholz BM, Murdock A, Bayly WM, et al. Effects of intravenous aminocaproic acid on exercise-induced pulmonary haemorrhage (EIPH). Equine Vet J 2010;42:256-260.
67. Epp TS, Edwards KL, Poole DC, et al. Effects of conjugated oestrogens and aminocaproic acid upon exercise-induced pulmonary haemorrhage (EIPH). Comp Exer Physiol 2008;5:95-103.
68. Manohar M, Goetz TE, Rothenbaum P, et al. Clenbuterol administration does not attenuate the exercise-induced pulmonary arterial, capillary or venous hypertension in strenuously exercising Thoroughbred horses. Equine Vet J 2000;32:546-550.
69. Walker HJ, Evans DL, Slocombe RF, et al. Effect of corticosteroid and bronchodilator therapy on bronchoalveolar lavage cytology following intrapulmonary blood inoculation. Equine Vet J Suppl 2006;Suppl 34:516-522.
70. Sweeney CR, Soma LR, Bucan CA, et al. Exercise-induced pulmonary hemorrhage in exercising Thoroughbreds: Preliminary results with pre-exercise medication. Cornell Vet 1984;74:263-268.
71. Manohar M, Goetz TE, Hassan AS, et al. Anti-inflammatory agent, dexamethasone, does not affect exercise-induced arterial hypoxemia in Thoroughbreds. J Appl Physiol 2002;93:99-106.
72. Manohar M, Goetz TE, Griffin R, et al. Pulmonary vascular pressures of strenuously exercising thoroughbreds after administration of phenylbutazone. Am J Vet Res 1996;57:1354-1358.
73. Manohar M, Goetz TE, Rothenbaum P, et al. Intravenous pentoxifylline does not affect the exercise-induced pulmonary arterial, capillary or venous hypertension in Thoroughbred horses. J Vet Pharmacol Ther 2000;23:317-322.
74. Perez-Moreno CI, Couetil LL, Pratt SM, et al. Effect of furosemide and furosemide-carbazochrome combination on exercise-induced pulmonary hemorrhage in Standardbred racehorses. Can Vet J 2009;50:821-827.
75. Epp TS, McDonough P, Myers DE, et al. The effectiveness of immunotherapy in treating exercise-induced pulmonary hemorrhage. J Equine Vet Sci 2009;29:527-532.
76. Padilla DJ, Epp TS, McDonough P, et al. Effects of a specific endothelin-1A antagonist on exercise-induced pulmonary haemorrhage (EIPH) in thoroughbred horses. Equine Vet J Suppl 2006;Suppl 34:198-203.
77. Manohar M, Goetz TE. Arterial hypoxemia in exercising thoroughbreds is not affected by pre-exercise nedocromil sodium inhalation. Respir Physiol Neurobiol 2003;134:145-154.
78. Kindig CA, McDonough P, Finley MR, et al. NO inhalation reduces pulmonary arterial pressure but not hemorrhage in maximally exercising horses. J Appl Physiol 2001;91:2674-2678.
79. Colahan PT, Jackson CA, Rice B, et al. The effect of sildenafil citrate administration on selected physiological parameters of exercising Thoroughbred horses. Equine Vet J Suppl 2010;Suppl 38:606-612.
80. Goetz TE, Manohar M, Hassan AS, et al. Nasal strips do not affect pulmonary gas exchange, anaerobic metabolism, or EIPH in exercising Thoroughbreds. J Appl Physiol 2001;90:2378-2385.
81. Poole DC, Kindig CA, Fenton G, et al. Effects of external nasal support on pulmonary gas exchange and EIPH in the horse. J Equine Vet Sci 2000;20:579-585.
82. Valdez SC, Nieto JE, Spier SJ, et al. Effect of an external nasal dilator strip on cytologic characteristics of bronchoalveolar lavage fluid in Thoroughbred racehorses. J Am Vet Med Assoc 2004;224:558-561.
83. Epp TS. The effect of herbal supplementation on the severity of exercise-induced pulmonary haemorrhage. Equine Comp Exer Physiol 2005;2:17.
84. Sweeney CR, Hall J, Fisher JR, et al. Efficacy of water vapor-saturated air in the treatment of exercise-induced pulmonary hemorrhage in Thoroughbred racehorses. Am J Vet Res 1988;49:1705-1707.
85. Gross DK, Morley PS, Hinchcliff KW, et al. Effect of furosemide on performance of Thoroughbreds racing in the United States and Canada. J Am Vet Med Assoc 1999;215:670-675.
86. Lester G, Clark C, Rice B, et al. Effect of timing and route of administration of furosemide on pulmonary hemorrhage and pulmonary arterial pressure in exercising thoroughbred racehorses. Am J Vet Res 1999;60:22-28.
87. Milne DW, Gabel AA, Muir WW, et al. Effects of furosemide on cardiovascular function and performance when given prior to simulated races: A double-blind study. Am J Vet Res 1980;41:1183-1189.
88. Soma LR, Birks EK, Uboh CE, et al. The effects of frusemide on racing times of Standardbred pacers. Equine Vet J 2000;32:334-340.
89. Soma LR, Laster L, Oppenlander F, et al. Effects of furosemide on the racing times of horses with exercise-induced pulmonary hemorrhage. Am J Vet Res 1985;46:763-768.
90. Sweeney CR, Soma LR, Maxson AD, et al. Effects of furosemide on the racing times of Thoroughbreds. Am J Vet Res 1990;51:772-778.
91. Bayly WM, Slocombe RF, Schott HC 2nd, et al. Effect of intravenous administration of furosemide on mass-specific maximal oxygen consumption and breathing mechanics in exercising horses. Am J Vet Res 1999;60:1415-1422.
92. McDonough P, Kindig CA, Hildreth TS, et al. Effect of furosemide and the equine nasal strip on exercise-induced pulmonary haemorrhage and time-to-fatigue in maximally exercising horses. Equine Comp Exer Physiol 2004;1:177-184.
93. Zawadzkas XA, Sides RH, Bayly WM. Is improved high speed performance following frusemide administration due to diuresis-induced weight loss or reduced severity of exercise-induced pulmonary haemorrhage? Equine Vet J Suppl 2006;36:291-293.
94. Hinchcliff KW, McKeever KH, Muir WW 3rd, et al. Effect of furosemide and weight carriage on energetic responses of horses to incremental exertion. Am J Vet Res 1993;54:1500-1504.
95. Hinchcliff KW, McKeever KH, Muir WW, et al. Furosemide reduces accumulated oxygen deficit in horses during brief intense exertion. J Appl Physiol 1996;81:1550-1554.
96. Guyatt GH, Oxman AD, Sultan S, et al. GRADE guidelines: 9. Rating up the quality of evidence. J Clin Epidemiol 2011;64:1311-1316.
97. Derksen FJ. Regional distribution of collagen and haemosiderin in the lungs of horses with exercise-induced pulmonary haemorrhage. Equine Vet J 2009;41:586.