Acta Vet. Brno 2013, 82: 309-316

https://doi.org/10.2754/avb201382030309

Exercise-induced pulmonary haemorrhage in horses – review

Gabriel Morán1, Hugo Folch2

1Universidad Austral de Chile, Faculty of Veterinary Science, Department of Pharmacology, Valdivia, Chile
2Universidad Austral de Chile, Faculty of Medicine, Department of Immunology, Valdivia, Chile

References

1. Ainsworth D, Hackett R 2004: Disorders of the respiratory system. In: Reed SM, Bayly WM, Sellon DC (eds). Equine Internal Medicine. 2nd ed. Saunders, Philadelphia, USA, pp 289-353
2. Ainsworth DM 2008: Lower airway function: responses to exercise and training. In: Equine exercise physiology: The Science of exercise in the athletic horse, Eds: KW Hinchcliff, RJ Goer and AJ Kaneps, Elsevier Saunders, New York, 193 p.
3. Araya O, Palma P, Salvi M, Bustamante H, Vits L 2005: Endoscopic determination of exercise-induced pulmonary haemorrhage in Chilean Criollo horses. Vet J 169: 311-313 <https://doi.org/10.1016/j.tvjl.2004.02.002>
4. Art T, Duvivier D, Votion D, Anciaux N, Vandenput S, Bayly W, Lekeux P 1998: Does an acute COPD crisis modify the cardiorespiratory and ventilatory adjustment to exercise in horses? J Applied Physiol 84: 845-852 <https://doi.org/10.1152/jappl.1998.84.3.845>
5. Art T, Lekeux P 1994: Exercise induced pulmonary hemorrhage in horses: an enigma of equine medicine. Ann Méd Vét 138: 145-153
6. Bernard SL, Glenny RW, Erickson HH, Fedde MR. Polissar N, Basaraba RJ, Hlastala MP 1996: Minimal redistribution of pulmonary blood flow with exercise in racehorses. J Applied Physiol 81: 1062-1070 <https://doi.org/10.1152/jappl.1996.81.3.1062>
7. Birks EK, Shuler KM, Soma LR, Martin BB, Marconato L, Del Piero F, Teleis DC, Schar, D, Hessinger AE, Uboh CE 2002: EIPH: postrace endoscopic evaluation of standard breeds and thoroughbreds. Equine Vet J 34: 375-378 <https://doi.org/10.1111/j.2042-3306.2002.tb05451.x>
8. Boucher J 1989: Exercise-induced echinocytosis. In: Jones WE, Equine sports medicine Philadelphia, Lea and Febiger, USA, pp 43-51
9. Caillaud C, Connes P, Bouix D, Mercier J 2002: Does haemorhelogy the paradox of hipoxemia during exercise in elite athletes or thoroughbred horses. Clin Hemorheol Microcirc 26: 175-181
10. Cook WR 2002: Bit-induced asphyxia in the horse: elevation and dorsal displacement of the soft palate at exercise. J Equine Vet Sci 22: 7-14 <https://doi.org/10.1016/S0737-0806(02)70207-4>
11. Cook WR, Williams R, Kirker-Head C 1988: Upper airway obstruction partial asphyxia as possible cause of exercise-induced pulmonary hemorrhage in the horse: An hypothesis. Equine Vet J 8: 11-26 <https://doi.org/10.1016/S0737-0806(88)80103-5>
12. Costa MF, Ronchi FA, Ivanow A, Carmona AK, Casarini D, Slocombe RF 2011: Association between circulating angiotensin-converting enzyme and exercise-induced pulmonary haemorrhage in thoroughbred racehorses. Res Vet Sci 93: 993-994 <https://doi.org/10.1016/j.rvsc.2011.10.011>
13. Derksen FJ, Slocombe RF, Gray PR, Robinson NE 1992: Exercise induced pulmonary hemorrage in horses with experimentally induced allergic lung disease. Am J Vet Res 53: 15-21
14. Derksen FJ, Williams KJ, Pannirselvam RR, de Feijter-Rupp H, Steel CM, Robinson NE 2009: Regional distribution of collagen and haemosiderin in the lungs of horses with exercise-induced pulmonary haemorrhage. Equine Vet J 41: 586-591 <https://doi.org/10.2746/042516409X429419>
15. Derksen F, Williams K, Stack A 2011: Exercise-induced pulmonary hemorrhage in horses: the role of pulmonary veins. Compend Contin Educ Vet 33: E1-E6
16. Doucet M, Viel L 2002: Alveolar macrophages graded hemosiderin score from bronchoalveolar lavage in horses with exercise induced pulmonary hemorrhage and controls. J Vet Intern Med 16: 281-286 <https://doi.org/10.1111/j.1939-1676.2002.tb02370.x>
17. Erickson HH 1992: Pulmonary artery and aortic pressure changes during high intensity treadmill exercise in the horse: effect of furosemide and phentolamine. Equine Vet J 23: 434-437
18. Erickson HH, Bernard SL, Glenny RW, Fedde MR, Polissar NL, Basaraba RJ, Walther SM, Gaughan EM, McMurphy R, Hlastala MP 1999: Effect of furosamide on pulmonary blood flow distribution in resting and exercising horses. J Applied Physiol 86: 2034-2043 <https://doi.org/10.1152/jappl.1999.86.6.2034>
19. Epp TS, McDonough P, Padilla DJ, Gentile JM, Edwards KL, Erickson HH, Poole DC 2006: Exercise-induced pulmonary haemorrhage during submaximal exercise. Equine Vet J Supplement 36: 502-507 <https://doi.org/10.1111/j.2042-3306.2006.tb05595.x>
20. Erickson HH, Hildreth T, Poole DC, Cox J 2001: Management of exercise induced pulmonary hemorrhage in non racing performance horses. Compend Contin Educ Vet 23: 1090-1093
21. Fedde M, Wood S 1993: Rheological characteristics of horse blood: significance during exercise. Respir Physiol 94: 323-335 <https://doi.org/10.1016/0034-5687(93)90027-8>
22. Geor RJ, Ommundson L, Fenton G, Pagan JD 2001: Effects of an external nasal strips and furosemide on pulmonary hemorrhage in thoroughbreds following high-intensity exercise. Equine Vet J 33: 537-539
23. Goetz TE, Manohar M, Hassan AS, Baker GJ 2001: Nasal strips do not affect pulmonary gas exchange anaerobic metabolism, or EIPH in exercising thoroughbreds. J Applied Physiol 91: 2378-2385 <https://doi.org/10.1152/jappl.2001.90.6.2378>
24. Goetz TE, Manohar M, Magid JH 1999: Repeated administration of furosemide dose not offer an advantage over single dosing in attenuating exercise-induced pulmonary hypertension in thoroughbred horses. Equine Vet J 30: 539-545
25. Harkins JD, Mundy G, Stanley S, Harrinson L, Poonacha K, Williams N, Tobin T 1997: Exercise-induced pulmonary hemorrhage: review of etiology and pathogenesis. Vet Clin North Am Equine Pract 19: 22-28
26. Harkins JD, Tobin T 1995: Racing horses, nitroglycerin and exercise induced pulmonary hemorrhage. Equine Vet J 27: 240-241 <https://doi.org/10.1111/j.2042-3306.1995.tb03069.x>
27. Hinchcliff KW 2000: Counting red cells- is it an answer to EIPH. Equine Vet J 32: 979-984
28. Hinchcliff KW, Jackson MA, Morley PS, Brown JA, Dredge AE, O’Callaghan PA, McCaffrey JP, Slocombe RE, Clarke AE 2005: Association between exercise-induced pulmonary hemorrhage and performance in thoroughbred racehorses. J Am Vet Med Assoc 227: 768-774 <https://doi.org/10.2460/javma.2005.227.768>
29. Hinchcliff KW, Morley PS, Guthrie AJ 2009: Efficacy of furosemide for prevention of exercise-induced pulmonary hemorrhage in thoroughbred racehorses. J Am Vet Med Assoc 235: 76-82 <https://doi.org/10.2460/javma.235.1.76>
30. Hinchcliff KW, Morley PS, Jackson MA, Brown JA, Dredge AF, O’Callaghan, PA, McCaffrey JP, Slocombe RF, Clarke AF 2010: Risk factors for exercise-induced pulmonary haemorrhage in thoroughbred racehorses. Equine Vet J supplement 38: 228-234 <https://doi.org/10.1111/j.2042-3306.2010.00245.x>
31. Langsetmo I, Meyer MR, Erickson HH 2000: Relationship of pulmonary arterial pressure to pulmonary hemorrhage in exercise horses. Equine Vet J 32: 379-384 <https://doi.org/10.2746/042516400777591066>
32. Langsetmo I, Weigle GE, Erickson HH, Fedde MR 1999: Influence of furosamide on dynamic cardiac variables during exercise. Equine Vet J 30: 170-173
33. Lapointe JM, Vrins A, McCarvill E 1994: A survey of exercise-induced pulmonary hemorrhage in Quebec standard breeds racehorses. Equine Vet J 6: 482-485 <https://doi.org/10.1111/j.2042-3306.1994.tb04054.x>
34. Markham G 1688: Markham’s master-piece revived: Containing all knowledge belonging to the Smith, FUFFieF of horse-leach. London: John Richardson for Tho. Passinger. p. 184
35. McKane SA, Canfield PJ, Rose RJ 1993: Equine bronchoalveolar lavage cytology: survey of thoroughbred racehorse in training. Australian Vet J 70: 401-404 <https://doi.org/10.1111/j.1751-0813.1993.tb06072.x>
36. McKane SA, Slocombe RF 2002: Alveolar fibrosis and changes in equine lung morphometry in response to intrapulmonary blood. Equine Vet J supplement 34: 451-458 <https://doi.org/10.1111/j.2042-3306.2002.tb05465.x>
37. Manohar M 1994: Pulmonary vascular pressures of thorougbreds increase rapidly and to higher level with rapid onset of high-intensity exercise than slow onset. Equine Vet J 26: 496-499 <https://doi.org/10.1111/j.2042-3306.1994.tb04057.x>
38. Manohar M, Goetz TE, Hassan AS 2001: Effect of prior high-intensity exercise on exercise-induced arterial hypoxemia in thoroughbred horses. J Applied Physiol 90: 2371-2377 <https://doi.org/10.1152/jappl.2001.90.6.2371>
39. Manohar M, Goetz TE, Rothenbaum P, Humphrey S 2000: Clenbuterol administration does not enhance the efficacy of furosemide in attenuating the exercise-induced pulmonary capillary hypertension in thoroughbred horses. J Vet Pharmacol Ther 23: 389-395 <https://doi.org/10.1046/j.1365-2885.2000.00293.x>
40. Manohar M, Hutchens E, Coney E 1993: Pulmonary hemodynamics in the exercising horses and their relationship to exercise-induce pulmonary hemorrhage. Br Vet J 149: 419-428 <https://doi.org/10.1016/S0007-1935(05)80108-3>
41. Michelotto PV Jr, Muehlmann LA, Zanatta AL, Bieberbach EW, Kryczyk M, Fernandes LC, Nishiyama A 2011: Pulmonary inflammation due to exercise-induced pulmonary haemorrhage in thoroughbred colts during race training. Vet J 190: e3-6 <https://doi.org/10.1016/j.tvjl.2010.08.009>
42. Moran G, Carrillo R, Campos B, Garcia C 2003: Endoscopic evaluation of exercise induced pulmonary hemorrhage in polo ponies. Arch Med Vet 35: 109-113
43. Newton JR, Rogers K, Marlin DJ, Wood JL, Williams RB 2005: 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 37: 402-411 <https://doi.org/10.2746/042516405774480049>
44. Newton J, Wood J 2002: Evidence of an association between inflammatory airway disease and EIPH in young thoroughbreds during training. Equine Vet J 34: 417-424 <https://doi.org/10.1111/j.2042-3306.2002.tb05459.x>
45. O’Callaghan MW, Hornof WJ, Fisher PE, Pascoe JR 1987: Exercise-induced pulmonary hemorrhage in the horse: results of a detailed clinical, post mortem and imaging study. VII. Ventilation/perfusion scintigraphy in horses with EIPH. Equine Vet J 19: 423-427 <https://doi.org/10.1111/j.2042-3306.1987.tb02635.x>
46. Oikawa M 1999: Exercise induced hemorrhage lesions in the dorsocaudal extremities of the caudal lobes of the lungs of young thoroughbred horses. J Comp Pathol 121: 339-347 <https://doi.org/10.1053/jcpa.1999.0331>
47. Pascoe JR 1996: Exercise-induced pulmonary hemorrhage: unifying concept. In Proceeding. 42nd Annual American Association of Equine Practitioner Convention, p 220-226
48. Pascoe JR 1997: Exercise-induced pulmonar. In: Robinson NE. Current therapy in equine medicine. 4nd ed. Saunders, Philadelphia, USA, p 441-443
49. Pascoe JR, McCabe AE, Franti CE, Arthur RM 1981: Efficacy of furosemide in the treatment of exercise-induced pulmonary hemorrhage in thoroughbred racehorses. Am J Vet Res 42: 703-707
50. Poole DC, Epp TS, Erickson HH 2007: Exercise-induced pulmonary haemorrhage (EIPH): mechanistic bases and therapeutic interventions. Equine Vet J 39: 292-293 <https://doi.org/10.2746/042516407X204078>
51. Robertson JB 1913: The heredity of blood-vessel breaking in the thoroughbred. Bloodstock Breeders’ Rev 2: 265-281
52. Schroter RC, Leeming A, Denny E, Bharath A Marlin DJ 1999: Modelling impact-initiated wave transmission through lung parenchyma in relation to the etiology of exercise-induced pulmonary hemorrhage. Equine Vet J Supplement 30: 34-38
53. Shroter RC, Marlin DJ, Denny E 1998: Exercise induced hemorrhage pulmonary (EIPH) in horses results from locomotory impact induced trauma novel, unifying concept. Equine Vet J 30: 186-192 <https://doi.org/10.1111/j.2042-3306.1998.tb04486.x>
54. Soma LR, Birks EK, Uboh CE, May L, Teleis D, Martini J 2000: The effects of furosemide on racing time of Standardbred pacers. Equine Vet J 32: 334-340 <https://doi.org/10.2746/042516400777032264>
55. Soma LR, Uboh CE 1998: Review of furosemide in horses racing: its effects and regulation. J Vet Pharmacol Ther 21: 228-240 <https://doi.org/10.1046/j.1365-2885.1998.00132.x>
56. Sweeney C 1991: Exercise-induced pulmonary hemorrhage. Vet Clin North Am Equine Pract 7: 93-104 <https://doi.org/10.1016/S0749-0739(17)30518-7>
57. Takahashi T, Hiraga A, Ohmura H, Kai M, Jones JH 2001: Frequency of and risk factors for epistaxis associated with exercise induced pulmonary hemorrhage in horse. J Am Vet Med Assoc 218: 1462-1464 <https://doi.org/10.2460/javma.2001.218.1462>
58. West JB, Mathieu-Costello O 1994: Stress failure of pulmonary capillaries as a mechanism for exercise induced pulmonary hemorrhage in the horse. Equine Vet J 26: 441-447 <https://doi.org/10.1111/j.2042-3306.1994.tb04047.x>
59. West JB, Mathieu-Costello O 1995: Stress failure of pulmonary capillaries as limiting factor for maximal exercise. Eur J Appl Physiol 70: 99-108 <https://doi.org/10.1007/BF00361536>
60. West JB, Mathieu-Costello O 1998: Stress-induced injury of pulmonary capillaries. Proc Assoc Am Physicians 110: 506-512
61. West JB, Mathieu-Costello O, Jones JH, Birks EK, Logemann RB, Pascoe JR, Tyler WS 1993: Stress failure of pulmonary capillaries in racehorses with exercise-induced pulmonary hemorrhage. J Applied Physiol 75: 1097-109 <https://doi.org/10.1152/jappl.1993.75.3.1097>
62. Weiss DJ, Geor RJ, Smith CM Jr 1994: Effects of echinocytosis on hemorrheologic values and exercise performance in horses. Am J Vet Res 55: 204-210
63. Weiss DJ, Smith CM Jr 1998: Haemorrheogical alterations associated with competitive racing activity in horses: implications for exercise-induce pulmonary hemorrhage (EIPH). Equine Vet J 30: 7-12 <https://doi.org/10.1111/j.2042-3306.1998.tb04082.x>
64. Williams KJ, Derksen FJ, de Feijter-Rupp H, Pannirselvam RR, Steel CM, Robinson, NE 2008: Regional pulmonary veno-occlusion: a newly identified lesion of equine exercise-induced pulmonary hemorrhage. Vet Pathol 45: 316-326 <https://doi.org/10.1354/vp.45-3-316>
front cover
  • ISSN 0001-7213 (printed)
  • ISSN 1801-7576 (electronic)

Current issue

Archive