Equine exercise-induced pulmonary hemorrhage: the role of high left-heart pressures secondary to exercise-induced hypervolemia, and high inspiratory pressures.
Abstract: Exercise-induced pulmonary hemorrhage (EIPH) is common in racehorses. Stress failure of the blood-gas barrier causes EIPH when the transmural pulmonary capillary (Pcap)-alveolar pressure difference (Ptm) exceeds the barrier's stress failure threshold. Why Pcap increases is incompletely understood. We hypothesized that alterations in blood volume (BV) could affect left ventricular (LV) and pulmonary arterial wedge (PAW) pressures and Pcap, and correspondingly affect EIPH severity. Six thoroughbreds with EIPH exercised at the same treadmill speed (≈11.9 m/s [11.1, 12.2]; median [IQR]) before (≈119% V̇o; B), 2 h after 14 L depletion of blood (≈132% V̇o; D), and 2 h after reinfusing the blood (≈111% V̇o; R). LV, pulmonary arterial (PAP), PAW, and intrapleural (Ppl) pressures were measured throughout exercise. Pcap = (PAP + PAW)/2 and Ptm = (Pcap - Ppl). EIPH severity was assessed 60 min postexercise by tracheoendoscopy (EIPHgrade) and bronchoalveolar lavage erythrocyte number (BALRBC). A mixed-effect model and Tukey post hoc test analyzed the effects of BV changes on LV, PAW, Pcap, Ppl, Ptm, and EIPH. ≤ 0.05 was significant. Peak intrapleural inspiratory pressure (Ppl) was high (-41 mmHg), unaffected by changes in BV ( = 0.44), and did not contribute to fluctuations in Ptm and EIPH severity, whereas changes in BV did (EIPHgrade: = 0.01, BALRBC: = 0.003). EIPH prevalence was 100% with B and R but 50% with D. MaxPtm was not different between B (146 mmHg [140, 151]) and R (151 mmHg [137, 160]) but was lower for D (128 mmHg [127, 130]; B: = 0.005, R: = 0.02). Vascular pressures and Ppl fluctuated constantly during exercise and independently influenced Ptm. Left ventricular end diastolic (LVED) pressure was correlated with Ptm ( = 0.90, = 0.03) and EIPH = 0.82, = 0.004). Exercise BV was strongly correlated with EIPH severity in racehorses ( = 0.86, = 0.009). Hypervolemia induced by the infusion of erythrocyte-rich blood stored in the spleen is normal in high-speed thoroughbred exercise and increases capillary-alveolar transmural pressure (Ptm), leading to exercise-induced pulmonary hemorrhage (EIPH). In this study, decreasing blood volume reduced Ptm and EIPH. Large negative inspiratory pressures also contribute to high Ptm and the occurrence of EIPH. Ptm is dynamic and oscillates constantly during exercise. A significant relationship existed between circulating blood volume and EIPH severity in racehorses.
Publication Date: 2024-10-10 PubMed ID: 39388286PubMed Central: PMC11573257DOI: 10.1152/japplphysiol.00575.2023Google Scholar: Lookup
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Cite This Article
APA
Bayly WM, Leguillette R, Sides RH, Massie S, Guigand C, Jones KB, Warlick LM, Thueson EL, Troudt TA, Slocombe RF, Jones JH.
(2024).
Equine exercise-induced pulmonary hemorrhage: the role of high left-heart pressures secondary to exercise-induced hypervolemia, and high inspiratory pressures.
J Appl Physiol (1985), 137(5), 1359-1373.
https://doi.org/10.1152/japplphysiol.00575.2023 Publication
Researcher Affiliations
- Department of Veterinary Clinical Sciences, Washington State University, College of Veterinary Medicine, Pullman, Washington, United States.
- Department of Veterinary Clinical and Diagnostic Sciences, Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada.
- Department of Veterinary Clinical Sciences, Washington State University, College of Veterinary Medicine, Pullman, Washington, United States.
- Department of Veterinary Clinical and Diagnostic Sciences, Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada.
- Department of Veterinary Clinical and Diagnostic Sciences, Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada.
- Department of Veterinary Clinical Sciences, Washington State University, College of Veterinary Medicine, Pullman, Washington, United States.
- Department of Veterinary Clinical Sciences, Washington State University, College of Veterinary Medicine, Pullman, Washington, United States.
- Department of Veterinary Clinical Sciences, Washington State University, College of Veterinary Medicine, Pullman, Washington, United States.
- Department of Veterinary Clinical Sciences, Washington State University, College of Veterinary Medicine, Pullman, Washington, United States.
- School of Veterinary and Agricultural Science, University of Melbourne, Werribee, Victoria, Australia.
- Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA, United States.
MeSH Terms
- Animals
- Horses
- Physical Conditioning, Animal / physiology
- Hemorrhage / physiopathology
- Blood Volume / physiology
- Male
- Lung Diseases / physiopathology
- Lung Diseases / etiology
- Lung / physiopathology
- Female
- Pulmonary Wedge Pressure / physiology
- Horse Diseases / physiopathology
- Inhalation / physiology
- Blood Pressure / physiology
- Ventricular Function, Left / physiology
Grant Funding
- The Grayson-Jockey Club Research Foundation
- The Washington State Equine Research Fund
- The Calgary Chair in Sports Medicine
Conflict of Interest Statement
No conflicts of interest, financial or otherwise, are declared by the authors.
References
This article includes 69 references
- Hinchcliff K, Couetil L, Knight P, Morley P, Robinson N, Sweeney C, van Erck E. Exercise-induced pulmonary hemorrhage in horses: American College of Veterinary Internal Medicine consensus statement. J Vet Intern Med 29: 743–758, 2015. doi: 10.1111/jvim.12593.
- Pascoe JR, Ferraro GL, Cannon JH, Arthur RM, Wheat JD. Exercise-induced pulmonary hemorrhage in racing Thoroughbreds: a preliminary study. Am J Vet Res 42: 703–707, 1981.
- Whitwell KE, Greet TRC. Collection and evaluation of tracheobronchial washes in the horse. Equine Vet J 16: 499–508, 1984. doi: 10.1111/j.2042-3306.1984.tb02000.x.
- Erickson HH, O'Dea JC, Pascoe J, Robinson NE, Sweeney CR. Exercise-induced pulmonary hemorrhage (EIPH). J Equine Vet Sci 15: 464–466, 1995. doi: 10.1016/S0737-0806(06)81813-7.
- Lopez Sanchez CM, Gold JR, Kogan C, Bayly WM. Relationship between tracheobronchoscopic score and bronchoalveolar lavage red blood cell number in the diagnosis of exercise-induced pulmonary hemorrhage in horses. J Vet Intern Med 34: 322–329, 2020. doi: 10.1111/jvim.15676.
- Bonomo CCM, Michelotto PV, Viccino C, Barussi FCM, Fernandes WR. Occurrence of exercise-induced pulmonary haemorrhage in show jumping horses. Vet J 248: 91–94, 2019. doi: 10.1016/j.tvjl.2019.05.003.
- Sweeney CR, Soma LR. Exercise-induced pulmonary hemorrhage in horses after different competitive exercises. In: Equine Exercise Physiology, edited by Snow DH, Persson SGB, Rose RJ. Cambridge, UK: Granta Editions, 1983, p. 51–56.
- West JB, Mathieu-Costello O, Jones JH, Birks EK, Logemann RB, Pascoe JR, Tyler WS. Stress failure of pulmonary capillaries in racehorses with exercise-induced pulmonary hemorrhage. J Appl Physiol (1985) 75: 1097–1109, 1993. doi: 10.1152/jappl.1993.75.3.1097.
- Birks EK, Mathieu-Costello O, Fu Z, Tyler WS, West JB. Comparative aspects of the strength of pulmonary capillaries in rabbit, dog, and horse. Respir Physiol 97: 235–246, 1994. doi: 10.1016/0034-5687(94)90029-9.
- Birks EK, Mathieu-Costello O, Fu Z, Tyler WS, West JB. Very high pressures are required to cause stress failure of pulmonary capillaries in Thoroughbred racehorses. J Appl Physiol (1985) 82: 1584–1592, 1997. doi: 10.1152/jappl.1997.82.5.1584.
- Olsen SC, Coyne CP, Lowe BS, Pelletier N, Raub EM, Erickson HH. Influence of frusemide on hemodynamic responses during exercise in horses. Am J Vet Res 53: 742–747, 1992.
- Manohar M, Hutchens E, Coney E. Pulmonary haemodynamics in the exercising horse and their relationship to exercise-induced pulmonary haemorrhage. Br Vet J 149: 419–428, 1993. doi: 10.1016/S0007-1935(05)80108-3.
- Sinha AK, Gleed RD, Hakim TS, Dobson A, Shannon KJ. Pulmonary capillary pressure during exercise in horses. J Appl Physiol (1985) 80: 1792–1798, 1996. doi: 10.1152/jappl.1996.80.5.1792.
- Erickson BK, Erickson HH, Coffman JR. Pulmonary artery, aortic and oesophageal pressure changes during high intensity treadmill exercise in the horse: a possible relation to exercise-induced pulmonary haemorrhage. Equine Vet J Suppl 9: 47–52, 1990. doi: 10.1111/j.2042-3306.1990.tb04734.x.
- Meyer TS, Fedde MR, Gaughan EM, Langsetmo I, Erickson HH. Quantification of exercise-induced pulmonary haemorrhage with bronchoalveolar lavage. Equine Vet J 30: 284–288, 1998. doi: 10.1111/j.2042-3306.1998.tb04098.x.
- Langsetmo I, Fedde MR, Meyer TS, Erickson HH. Relationship of pulmonary arterial pressure to pulmonary haemorrhage in exercising horses. Equine Vet J 32: 379–384, 2000. doi: 10.2746/042516400777591066.
- West JB. Left ventricular filling pressures during exercise: a cardiological blind spot? Chest 113: 1695–1697, 1998. doi: 10.1378/chest.113.6.1695.
- Oudiz RJ. Pulmonary hypertension associated with left-sided heart disease. Clin Chest Med 28: 233–241, 2007. doi: 10.1016/j.ccm.2006.12.001.
- Bayly WM, Gabel AA, Barr SA. Cardiovascular effects of submaximal aerobic training on a treadmill in Standardbred horses using a standardized exercise test. Am J Vet Res 44: 544–553, 1983.
- Jones J, Smith B, Birks E, Pascoe J, Hughes T. Left atrial and pulmonary arterial pressures in exercising horses. FASEB J 6: A2020, 1992.
- Slocombe R, Leguillette R, Jones J, Sides R, Bayly W. Left cardiac chamber pressures at rest and during exercise. Comp Ex Physiol 14 Suppl 1: S85, 2018.
- Manohar M. Pulmonary artery wedge pressure increases with high-intensity short-term exertion in horses. Am J Vet Res 54: 142–146, 1993. doi: 10.2460/ajvr.1993.54.01.142.
- Mielniczuk LM, Lamas GA, Flaker GC, Mitchell G, Smith SC, Gersh BJ, Solomon SD, Moyé LA, Rouleau JL, Rutherford JD, Pfeffer MA. Left ventricular end-diastolic pressure and risk of subsequent heart failure in patients following an acute myocardial infarction. Congest Heart Fail 13: 209–214, 2007. doi: 10.1111/j.1527-5299.2007.06624.x.
- nPersson SGB. On blood volume and working capacity in horses. Studies of methodology and physiological and pathological variations. Acta Vet Scandn19, : 9–189, 1967. n
- Hiraga A, Hobo S, Birks EK, Takahashi T, Hada T, Smith BL, Carr EA, Pascoe JR, Jones JH. Changes in left ventricular dynamics during graded exercise. Equine Vet J Suppl 31: 122–125, 1999. doi: 10.1111/j.2042-3306.1999.tb05201.x.
- Matter CM, Mandinov L, Kaufmann PA, Vassalli G, Jiang Z, Hess OM. Effect of NO donors on LV diastolic function in patients with severe pressure-overload hypertrophy. Circulation 99: 2396–2401, 1999. doi: 10.1161/01.cir.99.18.2396.
- Luks AM, Robertson HT, Swenson ER. An ultracyclist with pulmonary edema during the Bicycle Race Across America. Med Sci Sports Exerc 39: 8–12, 2007. doi: 10.1249/01.mss.0000235885.79110.79.
- Ekelund LG, Holmgren A. Central hemodynamics during exercise. Circ Res 30: 133–143, 1967.
- Hopkins SR, Schoene RB, Henderson WR, Spragg RG, Martin TR, West JB. Intense exercise impairs the integrity of the pulmonary blood-gas barrier in elite athletes. Am J Respir Crit Care Med 155: 1090–1094, 1997. doi: 10.1164/ajrccm.155.3.9116992.
- Mandinov L, Eberli FR, Seiler C, Hess OM. Diastolic heart failure. Cardiovasc Res 45: 813–825, 2000. doi: 10.1016/s0008-6363(99)00399-5.
- Huston TP, Puffer JC, Rodney WM. The athletic heart syndrome. N Engl J Med 313: 24–32, 1985. doi: 10.1056/NEJM198507043130106.
- nBayly W, Sides R. Comparison of V̇Omax and measures of ventilation during racetrack and treadmill exercise. Comp Ex Physioln14 Suppl 1: S80, 2018.
- Slocombe RF, Covelli G, Bayly WM. Respiratory mechanics of horses during stepwise treadmill exercise tests: the effect of clenbuterol pretreatment. Aust Vet J 69: 221–225, 1992. doi: 10.1111/j.1751-0813.1992.tb09929.x.
- Bayly WM, Slocombe RF, Schott IIH, Hines MT, Sides RH, Hakala JE. Effects of inhalation of albuterol sulphate, ipratroprium bromide, and frusemide on breathing mechanics and gas exchange in healthy exercising horses. Equine Vet J 33: 302–310, 2001. doi: 10.2746/042516401776249741.
- Hinchcliff KW, Jackson MA, Brown JA, Dredge AF, O'Callaghan PA, McCaffrey JP, Morley PS, Slocombe RF, Clarke AF. Tracheobronchoscopic assessment of exercise-induced pulmonary hemorrhage in horses. Am J Vet Res 66: 596–598, 2005. doi: 10.2460/ajvr.2005.66.596.
- Young LE, Rogers K, Wood JLN. Left ventricular size and systolic function in Thoroughbred racehorses and their relationships to race performance. J Appl Physiol (1985) 99: 1278–1285, 2005. doi: 10.1152/japplphysiol.01319.2004.
- nRose RJ, Hodgson DR, Bayly WM, Gollnick PD. V̇Omax, and V̇O kinetics in the horse: comparison of exercise protocols. Equine Vet J Suppln9: 39–42, 1990. doi: 10.1111/j.2042-3306.1990.tb04732.x. n
- Naylor JRJ, Bayly WM, Schott HC 2nd, Gollnick PD, Hodgson DR. Equine plasma and blood volumes decrease with dehydration but subsequently increase with exercise. J Appl Physiol (1985) 75: 1002–1008, 1993. doi: 10.1152/jappl.1993.75.2.1002.
- Buchholz BM, Murdock A, Bayly WM, Sides RH. Effects of intravenous aminocaproic acid on exercise-induced pulmonary haemorrhage (EIPH). Equine Vet J Suppl 42: 256–260, 2010. doi: 10.1111/j.2042-3306.2010.00247.x.
- Bhattacharya J, Nanjo S, Staub NC. Micropuncture measurement of lung microvascular pressure during 5-HT infusion. J Appl Physiol Respir Environ Exerc Physiol 52: 634–637, 1982. doi: 10.1152/jappl.1982.52.3.634.
- Glantz SA, Slinker BK, Neilands TB. Applied Regression & Analysis of Variance. New York, NY: McGraw-Hill, 2016, p. 623–633.
- Crispe EJ, Secombe CJ, Perera DI, Manderson AA, Turlach BA, Lester GD. Exercise-induced pulmonary haemorrhage in Thoroughbred racehorses: a longitudinal study. Equine Vet J 51: 45–51, 2019. doi: 10.1111/evj.12957.
- West JB, Mathieu-Costello O. Vulnerability of pulmonary capillaries in heart disease. Circulation 92: 622–631, 1995. doi: 10.1161/01.cir.92.3.622.
- McKeever KH, Hinchcliff KW, Reed SM, Hamlin RL. Splenectomy alters blood pressure response to incremental exercise in horses. Am J Physiol Regul Integr Comp Physiol 265: R409–R413, 1993. doi: 10.1152/ajpregu.1993.265.2.R409.
- Kline H, Foreman JH. Heart and spleen weights as a function of breed and somatotype. In: Equine Exercise Physiology 3, edited by Persson SGB, Jeffcott LB. Davis, CA: ICEEP Pubs, 1991, p. 17–21.
- Persson SGB, Ekman L, Lydin G, Tufvesson G. Circulatory Effects of Splenectomy in the Horse I. Effect on red-cell distribution and variability of haematocrit in the peripheral blood. Zentralbl Veterinarmed A 20: 441–455, 1973.
- Argenzio RA, Lowe JE, Pickard DW, Stevens CE. Digesta passage and water exchange in the equine large intestine. Am J Physiol 226: 1035–1042, 1974. doi: 10.1152/ajplegacy.1974.226.5.1035.
- Saltin B, Larsen H, Terrados N, Bangsbo J, Bak T, Kim CK, Svedenhag J, Rolf CJ. Aerobic exercise capacity at sea level and at altitude in Kenyan boys, junior and senior runners compared with Scandinavian runners. Scandinavian Med Sci Sports 5: 209–221, 1995. doi: 10.1111/j.1600-0838.1995.tb00037.x.
- Persson SGB, Lydin G. Circulatory effects of splenectomy in the horse. III. Effect on pulse-work relationship. Zentralbl Veterinarmed A 20: 521–530, 1973.
- Wagner P, Erickson BK, Kubo K, Hiraga A, Kai M, Yamaya Y, Richardson R, Seaman J. Maximum oxygen utilization before and after splenectomy. Equine Vet J Suppl 18: 82–89, 1995. doi: 10.1111/j.2042-3306.1995.tb04895.x.
- Wood P. An appreciation of mitral stenosis. I. Br Med J 1: 1051–1063, 1954. doi: 10.1136/bmj.1.4870.1051.
- Thomas AM, Turner RE, Tenholder MF. Esophageal pressure measurements in cardiopulmonary exercise testing. Chest 112: 829–832, 1997. doi: 10.1378/chest.112.3.829.
- Ainsworth DM, Smith CA, Henderson KS, Dempsey JA. Beathing during exercise in dogs – passive or active? J Appl Physiol 81: 586–595, 1996.
- Newton JR, Wood JL. Evidence of an association between inflammatory airway disease and EIPH in young Thoroughbreds during training. Equine Vet J Suppl 34: 417–424, 2002. doi: 10.1111/j.2042-3306.2002.tb05459.x.
- Jackson JA, Ducharme NG, Hackett RP, Rehder RS, Ainsworth DM, Shannon KJ, Erickson BK, Erb HN, Jansson N, Soderholm LV, Thorson LM. Effects of airway obstruction on transmural pulmonary artery pressure in exercising horses. Am J Vet Res 58: 897–903, 1997.
- Tsukimoto K, Mathieu-Costello O, Prediletto R, Elliott AR, West JB. Ultrastructural appearances of pulmonary capillaries at high transmural pressures. J Appl Physiol (1985) 71: 573–582, 1991. doi: 10.1152/jappl.1991.71.2.573.
- Fu Z, Costello ML, Tsukimoto K, Prediletto R, Elliott AR, Mathieu-Costello O, West JB. High lung volume increases stress failure in pulmonary capillaries. J Appl Physiol (1985) 73: 123–133, 1992. doi: 10.1152/jappl.1992.73.1.123.
- Elliott AR, Fu Z, Tsukimoto K, Prediletto R, Mathieu-Costello O, West JB. Short-term reversibility of ultrastructural changes in pulmonary capillaries caused by stress failure. J Appl Physiol (1985) 73: 1150–1158, 1992. doi: 10.1152/jappl.1992.73.3.1150.
- Schroter RC, Marlin DJ, Denny E. Exercise-induced pulmonary haemorrhage (EIPH) in horses results from locomotory impact induced trauma—a novel, unifying concept. Equine Vet J 30: 186–192, 1998. doi: 10.1111/j.2042-3306.1998.tb04486.x.
- Newton JR, Rogers K, Marlin DJ, Wood JLN, Williams RB. Risk factors for epistaxis on British racecourses: evidence fo rlocomotory impact-induced trauma contributing to the aetiology of exercise-induced pulmonary haemorrhage. Equine vet J 37: 402–411, 2005. doi: 10.2746/042516405774480049.
- Epp TS, McDonough P, Padilla DJ, Gentile JM, Edwards KL, Erickson HH, Poole DC. Exercise-induced pulmonary haemorrhage during submaximal exercise. Equine Vet J Suppl 30: 502–507, 2006. doi: 10.1111/j.2042-3306.2006.tb05595.x.
- Hillidge CJ, Lane TJ, Johnson EL, Asquith RL. Preliminary investigations of exercise-induced pulmonary hemorrhage in racing quarter horses. J Equine Vet Sci 4: 21–23, 1984. doi: 10.1016/S0737-0806(84)80099-4.
- Léguillette R, Steinmann M, Bond SL, Stanton B. Tracheobronchoscopic assessment of exercise-induced pulmonary hemorrhage and airway inflammation in Barrel racing horses. J Vet Intern Med 30: 1327–1332, 2016. doi: 10.1111/jvim.13959.
- Gold JR, Knowles DP, Coffey T, Bayly WM. Exercise-induced pulmonary hemorrhage in barrel racing horses in the Pacific Northwest region of the United States. J Vet Intern Med 32: 839–845, 2018. doi: 10.1111/jvim.15066.
- Persson SGB. The significance of haematological data in the evaluation of soundness and fitness in the horse. In: Equine Exercise Physiology, edited by Snow DH, Persson SGB, Rose RJ. Cambridge, UK: Granta Editions, 1983, p. 324–327.
- Snow DH, Mason DK, Ricketts SW, Douglas TA. Post-race blood biochemistry in thoroughbreds. In: Equine Exercise Physiology, edited by Snow DH, Persson SGB, Rose RJ. Cambridge, UK: Granta Editions, 1983, p. 389–399.
- Sinclair SE, McKinney S, Glenny RW, Bernard SL, Hlastala MP. Exercise alters fractal dimension and spatial correlation of pulmonary blood flow in the horse. J Appl Physiol (1985) 88: 2269–2278, 2000. doi: 10.1152/jappl.2000.88.6.2269.
- O’Callaghan MW, Pascoe JR, Tyler WS, Mason DK. Exercise-induced pulmonary haemorrhage in the horse: results of a detailed clinical, post mortem and imaging study. II. Gross lung pathology. Equine Vet J 19: 389–393, 1987. doi: 10.1111/j.2042-3306.1987.tb02628.x.
- Jones JH, Cox KS, Takahashi T, Hiraga A, Yarbrough TB, Pascoe JR. Heterogeneity of intrapleural pressures during exercise. Equine Vet J Suppl 34: 391–396, 2002. doi: 10.1111/j.2042-3306.2002.tb05454.x.
Citations
This article has been cited 1 times.- Park T, Hong S, Murray L, Lee J, Shah A, Mesa JC, Lee H, Couetil L, Lee CH. Wearable smart textile band for continuous equine health monitoring.. Biosens Bioelectron 2026 Jan 15;292:118073.
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