Pathophysiology of Noncardiac Syncope in Athletes
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Abstract
The most frequent cause of syncope in young athletes is noncardiac etiology. The mechanism of noncardiac syncope (NCS) in young athletes is neurally-mediated (reflex). NCS in athletes usually occurs either as orthostasis-induced, due to a gravity-mediated reduced venous return to the heart, or in the context of exercise. Exercise-related NCS typically occurs after the cessation of an exercise bout, while syncope occurring during exercise is highly indicative of the existence of a cardiac disorder. Postexercise NCS appears to result from hypotension due to impaired postexercise vasoconstriction, as well as from hypocapnia. The mechanisms of postexercise hypotension can be divided into obligatory (which are always present and include sympathoinhibition, histaminergic vasodilation, and downregulation of cardiovagal baroreflex) and situational (which include dehydration, hyperthermia and gravitational stress). Regarding postexercise hypocapnia, both hyperventilation during recovery from exercise and orthostasis-induced hypocapnia when recovery occurs in an upright posture can produce postexercise cerebral vasoconstriction. Athletes have been shown to exhibit differential orthostatic responses compared with nonathletes, involving augmented stroke volume and increased peripheral vasodilation in the former, with possibly lower propensity to orthostatic intolerance.
Notes
Compliance with Ethical Standards
Funding
No sources of funding were used to assist in the preparation of this article.
Conflicts of interest
Georgios Christou, Konstantinos Christou and Dimitrios Kiortsis declare that they have no conflicts of interest relevant to the content of this review.
References
- 1.Colivicchi F, Ammirati F, Santini M. Epidemiology and prognostic implications of syncope in young competing athletes. Eur Heart J. 2004;25:1749–53.PubMedCrossRefGoogle Scholar
- 2.Calkins H, Seifert M, Morady F. Clinical presentation and long-term follow-up of athletes with exercise-induced vasodepressor syncope. Am Heart J. 1995;129:1159–64.PubMedCrossRefGoogle Scholar
- 3.Christou GA, Kouidi EJ, Anifanti MA, Sotiriou PG, Deligiannis AP. A novel strategy for evaluating tilt test in athletes with syncope. Eur J Prev Cardiol. 2016;23:1003–10.PubMedCrossRefGoogle Scholar
- 4.Moya A, Sutton R, Ammirati F, Blanc JJ, Brignole M, Dahm JB, et al. Guidelines for the diagnosis and management of syncope (version 2009). Eur Heart J. 2009;30:2631–71.PubMedPubMedCentralCrossRefGoogle Scholar
- 5.Thompson PD. Tilt table testing in the evaluation and management of athletes with recurrent exercise-induced syncope. Med Sci Sports Exerc. 1993;25:883.PubMedCrossRefGoogle Scholar
- 6.Smith JJ, Porth CM, Erickson M. Hemodynamic response to the upright posture. J Clin Pharmacol. 1994;34:375–86.PubMedCrossRefGoogle Scholar
- 7.Nardo CJ, Chambless LE, Light KC, Rosamond WD, Sharrett AR, Tell GS, et al. Descriptive epidemiology of blood pressure response to change in body position. The ARIC Study. Hypertension. 1999;33:1123–9.PubMedCrossRefGoogle Scholar
- 8.Bjurstedt H, Rosenhamer G, Balldin U, Katkov V. Orthostatic reactions during recovery from exhaustive exercise of short duration. Acta Physiol Scand. 1983;119:25–31.PubMedCrossRefGoogle Scholar
- 9.Sneddon JF, Scalia G, Ward DE, McKenna WJ, Camm AJ, Frenneaux MP. Exercise induced vasodepressor syncope. Br Heart J. 1994;71:554–7.PubMedPubMedCentralCrossRefGoogle Scholar
- 10.Smith GD, Watson LP, Pavitt DV, Mathias CJ. Abnormal cardiovascular and catecholamine responses to supine exercise in human subjects with sympathetic dysfunction. J Physiol. 1995;484:255–65.PubMedPubMedCentralCrossRefGoogle Scholar
- 11.Christou GA, Christou KA, Christou EA, Kiortsis DN. Can noncardiac syncope occur during exercise? Cardiology. 2017;138:159–63.PubMedCrossRefGoogle Scholar
- 12.Holtzhausen LM, Noakes TD, Kroning B, de Klerk M, Roberts M, Emsley R. Clinical and biochemical characteristics of collapsed ultra-marathon runners. Med Sci Sports Exerc. 1994;26:1095–101.PubMedCrossRefGoogle Scholar
- 13.Edenfield KM, Stern AN, Dillon MC, Burkart TA, Clugston JR. A case of vasovagal syncope in a collegiate swimmer during competition. Curr Sports Med Rep. 2015;14:86–90.PubMedCrossRefGoogle Scholar
- 14.Murrell C, Cotter JD, George K, Shave R, Wilson L, Thomas K, et al. Influence of age on syncope following prolonged exercise: differential responses but similar orthostatic intolerance. J Physiol. 2009;587:5959–69.PubMedPubMedCentralCrossRefGoogle Scholar
- 15.Holtzhausen LM, Noakes TD. The prevalence and significance of post-exercise (postural) hypotension in ultramarathon runners. Med Sci Sports Exerc. 1995;27:1595–601.PubMedCrossRefGoogle Scholar
- 16.Mündel T, Perry BG, Ainslie PN, Thomas KN, Sikken EL, Cotter JD, et al. Postexercise orthostatic intolerance: influence of exercise intensity. Exp Physiol. 2015;100:915–25.PubMedCrossRefGoogle Scholar
- 17.Gratze G, Mayer H, Skrabal F. Sympathetic reserve, serum potassium, and orthostatic intolerance after endurance exercise and implications for neurocardiogenic syncope. Eur Heart J. 2008;29:1531–41.PubMedCrossRefGoogle Scholar
- 18.Smith GD, Watson LP, Mathias CJ. Cardiovascular and catecholamine changes induced by supine exercise and upright posture in vasovagal syncope. Comparisons with normal subjects and subjects with sympathetic denervation. Eur Heart J. 1996;17:1882–990.PubMedCrossRefGoogle Scholar
- 19.Murrell CJ, Cotter JD, George K, Shave R, Wilson L, Thomas K, et al. Syncope is unrelated to supine and postural hypotension following prolonged exercise. Eur J Appl Physiol. 2011;111:469–76.PubMedCrossRefGoogle Scholar
- 20.Ogoh S, Fisher JP, Purkayastha S, Dawson EA, Fadel PJ, White MJ, et al. Regulation of middle cerebral artery blood velocity during recovery from dynamic exercise in humans. J Appl Physiol. 1985;2007(102):713–21.Google Scholar
- 21.Ogoh S, Dalsgaard MK, Yoshiga CC, Dawson EA, Keller DM, Raven PB, et al. Dynamic cerebral autoregulation during exhaustive exercise in humans. Am J Physiol Heart Circ Physiol. 2005;288:H1461–7.PubMedCrossRefGoogle Scholar
- 22.Willie CK, Ainslie PN, Taylor CE, Eves ND, Tzeng YC. Maintained cerebrovascular function during post-exercise hypotension. Eur J Appl Physiol. 2013;113:1597–604.PubMedCrossRefGoogle Scholar
- 23.Sakaguchi S, Shultz JJ, Remole SC, Adler SW, Lurie KG, Benditt DG. Syncope associated with exercise, a manifestation of neurally mediated syncope. Am J Cardiol. 1995;75:476–81.PubMedCrossRefGoogle Scholar
- 24.Thomson HL, Lele SS, Atherton JJ, Wright KN, Stafford W, Frenneaux MP. Abnormal forearm vascular responses during dynamic leg exercise in patients with vasovagal syncope. Circulation. 1995;92:2204–9.PubMedCrossRefGoogle Scholar
- 25.Thomson HL, Atherton JJ, Khafagi FA, Frenneaux MP. Failure of reflex venoconstriction during exercise in patients with vasovagal syncope. Circulation. 1996;93:953–9.PubMedCrossRefGoogle Scholar
- 26.Nobrega AC, O’Leary D, Silva BM, Marongiu E, Piepoli MF, Crisafulli A. Neural regulation of cardiovascular response to exercise: role of central command and peripheral afferents. Biomed Res Int. 2014;2014:478965.PubMedPubMedCentralCrossRefGoogle Scholar
- 27.Goldstein DS, Eisenhofer G, Kopin IJ. J Sources and significance of plasma levels of catechols and their metabolites in humans. Pharmacol Exp Ther. 2003;305:800–11.CrossRefGoogle Scholar
- 28.Olshansky B. A pepsi challenge. N Engl J Med. 1999;340:2006.PubMedCrossRefGoogle Scholar
- 29.Flugelman M, Halon DA, Goldblatt H. Golf syncope. Lancet. 1987;2:47.PubMedCrossRefGoogle Scholar
- 30.Krediet CT, Wilde AA, Wieling W, Halliwill JR. Exercise related syncope, when it’s not the heart. Clin Auton Res. 2004;14:25–36.PubMedCrossRefGoogle Scholar
- 31.Brown SP, Clemons JM, He Q, Liu S. Effects of resistance exercise and cycling on recovery blood pressure. J Sports Sci. 1994;12:463–8.PubMedCrossRefGoogle Scholar
- 32.Coats AJ, Conway J, Isea JE, Pannarale G, Sleight P, Somers VK. Systemic and forearm vascular resistance changes after upright bicycle exercise in man. J Physiol. 1989;413:289–98.PubMedPubMedCentralCrossRefGoogle Scholar
- 33.Jones H, George K, Edwards B, Atkinson G. Is the magnitude of acute post-exercise hypotension mediated by exercise intensity or total work done? Eur J Appl Physiol. 2007;102:33–40.PubMedCrossRefGoogle Scholar
- 34.Endo MY, Shimada K, Miura A, Fukuba Y. Peripheral and central vascular conductance influence on post-exercise hypotension. J Physiol Anthropol. 2012;31:32.PubMedPubMedCentralCrossRefGoogle Scholar
- 35.Bennett T, Wilcox RG, Macdonald IA. Post-exercise reduction of blood pressure in hypertensive men is not due to acute impairment of baroreflex function. Clin Sci (Lond). 1984;67:97–103.PubMedCrossRefGoogle Scholar
- 36.Isea JE, Piepoli M, Adamopoulos S, Pannarale G, Sleight P, Coats AJ. Time course of haemodynamic changes after maximal exercise. Eur J Clin Invest. 1994;24:824–9.PubMedCrossRefGoogle Scholar
- 37.Wilcox RG, Bennett T, Brown AM, Macdonald IA. Is exercise good for high blood pressure? Br Med J (Clin Res Ed). 1982;285:767–9.CrossRefGoogle Scholar
- 38.Wallace JP, Bogle PG, King BA, Krasnoff JB, Jastremski CA. The magnitude and duration of ambulatory blood pressure reduction following acute exercise. J Hum Hypertens. 1999;13:361–6.PubMedCrossRefGoogle Scholar
- 39.Cléroux J, Kouamé N, Nadeau A, Coulombe D, Lacourcière Y. After effects of exercise on regional and systemic hemodynamics in hypertension. Hypertension. 1992;19:183–91.PubMedCrossRefGoogle Scholar
- 40.Carvalho RS, Pires CM, Junqueira GC, Freitas D, Marchi-Alves LM. Hypotensive response magnitude and duration in hypertensives: continuous and interval exercise. Arq Bras Cardiol. 2015;104:234–41.PubMedPubMedCentralGoogle Scholar
- 41.Wieling, Harms MP, ten Harkel AD, van Lieshout JJ, Sprangers RL. Circulatory response evoked by a 3 s bout of dynamic leg exercise in humans. J Physiol. 1996;494:601–11.Google Scholar
- 42.Eicher JD, Maresh CM, Tsongalis GJ, Thompson PD, Pescatello LS. The additive blood pressure lowering effects of exercise intensity on post-exercise hypotension. Am Heart J. 2010;160:513–20.PubMedCrossRefGoogle Scholar
- 43.Hagberg JM, Montain SJ, Martin WH 3rd. Blood pressure and hemodynamic responses after exercise in older hypertensives. J Appl Physiol. 1985;1987(63):270–6.Google Scholar
- 44.Keese F, Farinatti P, Pescatello L, Monteiro W. A comparison of the immediate effects of resistance, aerobic, and concurrent exercise on postexercise hypotension. J Strength Cond Res. 2011;25:1429–36.PubMedCrossRefGoogle Scholar
- 45.Brito Ade F, de Oliveira CV, Brasileiro-Santos Mdo S, Santos Ada C. Resistance exercise with different volumes: blood pressure response and forearm blood flow in the hypertensive elderly. Clin Interv Aging. 2014;9:2151–8.PubMedGoogle Scholar
- 46.Figueiredo T, Rhea MR, Peterson M, Miranda H, Bentes CM, dos Reis VM, et al. Influence of number of sets on blood pressure and heart rate variability after a strength training session. J Strength Cond Res. 2015;29:1556–63.PubMedCrossRefGoogle Scholar
- 47.Cavalcante PA, Rica RL, Evangelista AL, Serra AJ, Figueira A Jr, Pontes FL Jr, et al. Effects of exercise intensity on postexercise hypotension after resistance training session in overweight hypertensive patients. Clin Interv Aging. 2015;10:1487–95.PubMedPubMedCentralCrossRefGoogle Scholar
- 48.de Freitas Brito A, Brasileiro-Santos Mdo S, Coutinho de Oliveira CV, Sarmento da Nóbrega TK, de Moraes Lúcia, Forjaz C, da Cruz Santos A. High-intensity resistance exercise promotes postexercise hypotension greater than moderate intensity and affects cardiac autonomic responses in women who are hypertensive. J Strength Cond Res. 2015;29:3486–93.CrossRefGoogle Scholar
- 49.Figueiredo T, Willardson JM, Miranda H, Bentes CM, Reis VM, Simão R. Influence of load intensity on postexercise hypotension and heart rate variability after a strength training session. J Strength Cond Res. 2015;29:2941–8.PubMedCrossRefGoogle Scholar
- 50.Moraes MR, Bacurau RF, Simões HG, Campbell CS, Pudo MA, Wasinski F, et al. Effect of 12 weeks of resistance exercise on post-exercise hypotension in stage 1 hypertensive individuals. J Hum Hypertens. 2012;26:533–9.PubMedCrossRefGoogle Scholar
- 51.Brito LC, Queiroz AC, Forjaz CL. Influence of population and exercise protocol characteristics on hemodynamic determinants of post-aerobic exercise hypotension. Braz J Med Biol Res. 2014;47:626–36.PubMedPubMedCentralCrossRefGoogle Scholar
- 52.Floras JS, Sinkey CA, Aylward PE, Seals DR, Thoren PN, Mark AL. Postexercise hypotension and sympathoinhibition in borderline hypertensive men. Hypertension. 1989;14:28–35.PubMedCrossRefGoogle Scholar
- 53.Halliwill JR, Taylor JA, Eckberg DL. Impaired sympathetic vascular regulation in humans after acute dynamic exercise. J Physiol. 1996;495:279–88.PubMedPubMedCentralCrossRefGoogle Scholar
- 54.Chen CY, Bonham AC. Postexercise hypotension: central mechanisms. Exerc Sport Sci Rev. 2010;38:122–7.PubMedPubMedCentralCrossRefGoogle Scholar
- 55.Buck TM, Romero SA, Ely MR, Sieck DC, Abdala PM, Halliwill JR. Neurovascular control following small muscle-mass exercise in humans. Physiol Rep. 2015;3:e12289.Google Scholar
- 56.Lockwood JM, Wilkins BW, Halliwill JR. H1 receptor-mediated vasodilatation contributes to postexercise hypotension. J Physiol. 2005;563:633–42.PubMedCrossRefGoogle Scholar
- 57.McCord JL, Beasley JM, Halliwill JR. H2-receptor-mediated vasodilation contributes to postexercise hypotension. J Appl Physiol. 1985;2006(100):67–75.Google Scholar
- 58.Somers VK, Conway J, LeWinter M, Sleight P. The role of baroreflex sensitivity in post-exercise hypotension. J Hypertens Suppl. 1985;3:S129–30.PubMedGoogle Scholar
- 59.Piepoli M, Coats AJ, Adamopoulos S, Bernardi L, Feng YH, Conway J, et al. Persistent peripheral vasodilation and sympathetic activity in hypotension after maximal exercise. J Appl Physiol. 1985;1993(75):1807–14.Google Scholar
- 60.Convertino VA, Adams WC. Enhanced vagal baroreflex response during 24 h after acute exercise. Am J Physiol. 1991;260:R570–5.PubMedCrossRefGoogle Scholar
- 61.Willie CK, Ainslie PN, Taylor CE, Jones H, Sin PY, Tzeng YC. Neuromechanical features of the cardiac baroreflex after exercise. Hypertension. 2011;57:927–33.PubMedCrossRefGoogle Scholar
- 62.Charkoudian N, Halliwill JR, Morgan BJ, Eisenach JH, Joyner MJ. Influences of hydration on post-exercise cardiovascular control in humans. J Physiol. 2003;552:635–44.PubMedPubMedCentralCrossRefGoogle Scholar
- 63.Davis JE, Fortney SM. Effect of fluid ingestion on orthostatic responses following acute exercise. Int J Sports Med. 1997;18:174–8.PubMedCrossRefGoogle Scholar
- 64.Endo MY, Kajimoto C, Yamada M, Miura A, Hayashi N, Koga S, et al. Acute effect of oral water intake during exercise on post-exercise hypotension. Eur J Clin Nutr. 2012;66:1208–13.PubMedCrossRefGoogle Scholar
- 65.Franklin PJ, Green DJ, Cable NT. The influence of thermoregulatory mechanisms on post-exercise hypotension in humans. J Physiol. 1993;470:231–41.PubMedPubMedCentralCrossRefGoogle Scholar
- 66.Wilkins BW, Minson CT, Halliwill JR. Regional hemodynamics during postexercise hypotension. II. Cutaneous circulation. J Appl Physiol. 1985;2004(97):2071–6.Google Scholar
- 67.Lucas SJ, Cotter JD, Murrell C, Wilson L, Anson JG, Gaze D, et al. Mechanisms of orthostatic intolerance following very prolonged exercise. J Appl Physiol. 1985;2008(105):213–25.Google Scholar
- 68.Ide K, Eliasziw M, Poulin MJ. Relationship between middle cerebral artery blood velocity and end-tidal PCO2 in the hypocapnic-hypercapnic range in humans. J Appl Physiol. 1985;2003(95):129–37.Google Scholar
- 69.Murrell CJ, Cotter JD, George K, Shave R, Wilson L, Thomas K, et al. Cardiorespiratory and cerebrovascular responses to head-up tilt II: influence of age, training status and acute exercise. Exp Gerontol. 2011;46:1–8.PubMedCrossRefGoogle Scholar
- 70.Lucas SJ, Lewis NC, Sikken EL, Thomas KN, Ainslie PN. Slow breathing as a means to improve orthostatic tolerance: a randomized sham-controlled trial. J Appl Physiol. 1985;2013(115):202–11.Google Scholar
- 71.Gisolf J, Wilders R, Immink RV, van Lieshout JJ, Karemaker JM. Tidal volume, cardiac output and functional residual capacity determine end-tidal CO2 transient during standing up in humans. J Physiol. 2004;554:579–90.PubMedCrossRefGoogle Scholar
- 72.Bőhm A, Kiss RG, Bachmann B, Duray GZ. Exercise-induced vasovagal syncope. Heart Rhythm. 2014;11:1089–90.PubMedCrossRefGoogle Scholar
- 73.Crisafulli A, Melis F, Orrù V, Lener R, Lai C, Concu A. Hemodynamic during a 3 postexertional asystolia in a healthy athlete: a case study. Med Sci Sports Exerc. 2000;32:4–9.PubMedCrossRefGoogle Scholar
- 74.Hirata T, Yano K, Okui T, Mitsuoka T, Hashiba K. Asystole with syncope following strenuous exercise in a man without organic heart disease. J Electrocardiol. 1987;20:280–3.PubMedCrossRefGoogle Scholar
- 75.Abe H, Iwami Y, Nakashima Y, Kohshi K, Kuroiwa A. Exercise-induced neurally mediated syncope. Jpn Heart J. 1997;38:535–9.PubMedCrossRefGoogle Scholar
- 76.Pedersen WR, Janosik DL, Goldenberg IF, Stevens LL, Redd RM. Post-exercise asystolic arrest in a young man without organic heart disease: utility of head-up tilt testing in guiding therapy. Am Heart J. 1989;18:410–3.CrossRefGoogle Scholar
- 77.Campagna JA, Carter C. Clinical relevance of the Bezold-Jarisch reflex. Anesthesiology. 2003;98:1250–60.PubMedCrossRefGoogle Scholar
- 78.Finlay JB, Hartman AF, Weir RC. Post-swim orthostatic intolerance in a marathon swimmer. Med Sci Sports Exerc. 1995;27:1231–7.PubMedCrossRefGoogle Scholar
- 79.Whyte G, Stephens N, Budgett R, Sharma S, Shave RE, McKenna WJ. Exercise induced neurally mediated syncope in an elite rower: a treatment dilemma. Br J Sports Med. 2004;38:84–5.PubMedPubMedCentralCrossRefGoogle Scholar
- 80.Schwabe K, Schwellnus M, Derman W, Swanevelder S, Jordaan E. Medical complications and deaths in 21 and 56 km road race runners: a 4-year prospective study in 65 865 runners – SAFER study I. Br J Sports Med. 2014;48:912–8.PubMedCrossRefGoogle Scholar
- 81.Schwabe K, Schwellnus MP, Derman W, Swanevelder S, Jordaan E. Less experience and running pace are potential risk factors for medical complications during a 56 km road running race: a prospective study in 26 354 race starters—SAFER study II. Br J Sports Med. 2014;48:905–11.PubMedCrossRefGoogle Scholar
- 82.Schwabe K, Schwellnus MP, Derman W, Swanevelder S, Jordaan E. Older females are at higher risk for medical complications during 21 km road race running: a prospective study in 39 511 race starters—SAFER study III. Br J Sports Med. 2014;48:891–7.PubMedCrossRefGoogle Scholar
- 83.Romero SA, Cooke WH. Hyperventilation before resistance exercise: cerebral hemodynamics and orthostasis. Med Sci Sports Exerc. 2007;39:1302–7.PubMedCrossRefGoogle Scholar
- 84.Pott F, Van Lieshout JJ, Ide K, Madsen P, Secher NH. Middle cerebral artery blood velocity during intense static exercise is dominated by a Valsalva maneuver. J Appl Physiol. 1985;2003(94):1335–44.Google Scholar
- 85.Pott F, van Lieshout JJ, Ide K, Madsen P, Secher NH. Middle cerebral artery blood velocity during a valsalva maneuver in the standing position. J Appl Physiol. 1985;2000(88):1545–50.Google Scholar
- 86.Compton D, Hill PM, Sinclair JD. Weight-lifters’ blackout. Lancet. 1973;2:1234–7.PubMedCrossRefGoogle Scholar
- 87.Wieling W, van Lieshout JJ. The fainting lark. Clin Auton Res. 2002;12:207.PubMedCrossRefGoogle Scholar
- 88.Asplund CA, O’Connor FG, Noakes TD. Exercise-associated collapse: an evidence-based review and primer for clinicians. Br J Sports Med. 2011;45:1157–62.PubMedCrossRefGoogle Scholar
- 89.Casa DJ, DeMartini JK, Bergeron MF, Csillan D, Eichner ER, Lopez RM, et al. National athletic trainers’ association position statement: exertional heat illnesses. J Athl Train. 2015;50:986–1000.PubMedPubMedCentralCrossRefGoogle Scholar
- 90.Schlader ZJ, Wilson TE, Crandall CG. Mechanisms of orthostatic intolerance during heat stress. Auton Neurosci. 2016;196:37–46.PubMedCrossRefGoogle Scholar
- 91.Howe AS, Boden BP. Heat-related illness in athletes. Am J Sports Med. 2007;35:1384–95.PubMedCrossRefGoogle Scholar
- 92.Johnson JM, Niederberger M, Rowell LB, Eisman MM, Brengelmann GL. Competition between cutaneous vasodilator and vasoconstrictor reflexes in man. J Appl Physiol. 1973;35:798–803.PubMedCrossRefGoogle Scholar
- 93.Wilson TE, Cui J, Zhang R, Crandall CG. Heat stress reduces cerebral blood velocity and markedly impairs orthostatic tolerance in humans. Am J Physiol Regul Integr Comp Physiol. 2006;291:R1443–8.PubMedPubMedCentralCrossRefGoogle Scholar
- 94.Jimenez C, Fortrat JO, Delapierre B, Melin B. Moderate exercise effects on orthostatic intolerance while wearing protective clothing. Aviat Space Environ Med. 2012;83:570–6.PubMedCrossRefGoogle Scholar
- 95.Adler GK, Bonyhay I, Failing H, Waring E, Dotson S, Freeman R. Antecedent hypoglycemia impairs autonomic cardiovascular function: implications for rigorous glycemic control. Diabetes. 2009;58:360–6.PubMedPubMedCentralCrossRefGoogle Scholar
- 96.Madden KM, Lockhart CK, Potter TF, Cuff DJ, Meneilly GS. Short-term aerobic exercise reduces nitroglycerin-induced orthostatic intolerance in older adults with type 2 diabetes. J Cardiovasc Pharmacol. 2011;57:666–71.PubMedPubMedCentralCrossRefGoogle Scholar
- 97.Mtinangi BL, Hainsworth R. Effects of moderate exercise training on plasma volume, baroreceptor sensitivity and orthostatic tolerance in healthy subjects. Exp Physiol. 1999;84:121–30.PubMedCrossRefGoogle Scholar
- 98.Mtinangi BL, Hainsworth R. Increased orthostatic tolerance following moderate exercise training in patients with unexplained syncope. Heart. 1998;80:596–600.PubMedPubMedCentralCrossRefGoogle Scholar
- 99.Takahagi VC, Costa DC, Crescêncio JC, Gallo Junior L. Physical training as non-pharmacological treatment of neurocardiogenic syncope. Arq Bras Cardiol. 2014;102:288–94.PubMedPubMedCentralGoogle Scholar
- 100.Winker R, Barth A, Bidmon D, Ponocny I, Weber M, Mayr O, et al. Endurance exercise training in orthostatic intolerance: a randomized, controlled trial. Hypertension. 2005;45:391–8.PubMedCrossRefGoogle Scholar
- 101.Allen SC, Taylor CL, Hall VE. A study of orthostatic insufficiency by the tiltboard method. Am J Physiol. 1945;143:11–20.Google Scholar
- 102.Brilla LR, Stephens AB, Knutzen KM, Caine D. Effect of strength training on orthostatic hypotension in older adults. J Cardiopulm Rehabil. 1998;18:295–300.PubMedCrossRefGoogle Scholar
- 103.Howden R, Lightfoot JT, Brown SJ, Swaine IL. The effects of isometric exercise training on resting blood pressure and orthostatic tolerance in humans. Exp Physiol. 2002;87:507–15.PubMedCrossRefGoogle Scholar
- 104.Mack GW, Convertino VA, Nadel ER. Effect of exercise training on cardiopulmonary baroreflex control of forearm vascular resistance in humans. Med Sci Sports Exerc. 1993;25:722–6.PubMedCrossRefGoogle Scholar
- 105.Conboy EE, Fogelman AE, Sauder CL, Ray CA. Endurance training reduces renal vasoconstriction to orthostatic stress. Am J Physiol Renal Physiol. 2010;298:F279–84.PubMedCrossRefGoogle Scholar
- 106.Fu Q, Vangundy TB, Galbreath MM, Shibata S, Jain M, Hastings JL, et al. Cardiac origins of the postural orthostatic tachycardia syndrome. J Am Coll Cardiol. 2010;55:2858–68.PubMedPubMedCentralCrossRefGoogle Scholar
- 107.George SA, Bivens TB, Howden EJ, Saleem Y, Galbreath MM, Hendrickson D, et al. The international POTS registry: evaluating the efficacy of an exercise training intervention in a community setting. Heart Rhythm. 2016;13:943–50.PubMedCrossRefGoogle Scholar
- 108.Rubinshtein R, Ciubotaru M, Elad H, Bitterman H. Severe orthostatic hypotension following weight reduction surgery. Arch Intern Med. 2001;161:2145–7.PubMedCrossRefGoogle Scholar
- 109.DeHaven J, Sherwin R, Hendler R, Felig P. Nitrogen and sodium balance and sympathetic-nervous-system activity in obese subjects treated with a low-calorie protein or mixed diet. N Engl J Med. 1980;302:477–82.PubMedCrossRefGoogle Scholar
- 110.Christou GA, Kiortsis DN. The effects of body weight status on orthostatic intolerance and predisposition to noncardiac syncope. Obes Rev. 2017;18:370–9.PubMedCrossRefGoogle Scholar
- 111.Stevens GH, Foresman BH, Shi X, Stern SA, Raven PB. Reduction in LBNP tolerance following prolonged endurance exercise training. Med Sci Sports Exerc. 1992;24:1235–44.PubMedCrossRefGoogle Scholar
- 112.Convertino VA, Sather TM, Goldwater DJ, Alford WR. Aerobic fitness does not contribute to prediction of orthostatic intolerance. Med Sci Sports Exerc. 1986;18:551–6.PubMedCrossRefGoogle Scholar
- 113.Frey MA, Mathes KL, Hoffler GW. Aerobic fitness in women and responses to lower body negative pressure. Aviat Space Environ Med. 1987;58:1149–52.PubMedGoogle Scholar
- 114.Christou GA, Kouidi EJ, Anifanti MA, Sotiriou PG, Koutlianos NA, Deligiannis AP. Pathophysiological mechanisms of noncardiac syncope in athletes. Int J Cardiol. 2016;224:20–6.PubMedCrossRefGoogle Scholar
- 115.Convertino VA. Blood volume: its adaptation to endurance training. Med Sci Sports Exerc. 1991;23:1338–48.PubMedCrossRefGoogle Scholar
- 116.Arbab-Zadeh A, Dijk E, Prasad A, Fu Q, Torres P, Zhang R, et al. Effect of aging and physical activity on left ventricular compliance. Circulation. 2004;110:1799–805.PubMedCrossRefGoogle Scholar
- 117.Galderisi M, Cardim N, D’Andrea A, Bruder O, Cosyns B, Davin L, et al. The multi-modality cardiac imaging approach to the Athlete’s heart: an expert consensus of the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging. 2015;16:353.PubMedCrossRefGoogle Scholar
- 118.Formes K, Zhang P, Tierney N, Schaller F, Shi X. Chronic physical activity mitigates cerebral hypoperfusion during central hypovolemia in elderly humans. Am J Physiol Heart Circ Physiol. 2010;298:H1029–37.PubMedCrossRefGoogle Scholar
- 119.Hernandez JP, Franke WD. Age- and fitness-related differences in limb venous compliance do not affect tolerance to maximal lower body negative pressure in men and women. J Appl Physiol. 1985;2004(97):925–9.Google Scholar
- 120.Louisy F, Jouanin JC, Guezennec CY. Filling and emptying characteristics of lower limb venous network in athletes. Study by postural plethysmography. Int J Sports Med. 1997;18:26–9.PubMedCrossRefGoogle Scholar
- 121.Sugawara J, Komine H, Miyazawa T, Imai T, Ogoh S. Influence of regular exercise training on post-exercise hemodynamic regulation to orthostatic challenge. Front Physiol. 2014;5:229.PubMedPubMedCentralCrossRefGoogle Scholar
- 122.Convertino VA, Mathes KL, Lasley ML, Tomaselli CM, Frey MA, Hoffler GW. Hemodynamic and hormonal responses to lower body negative pressure in men with varying profiles of strength and aerobic power. Eur J Appl Physiol Occup Physiol. 1993;67:492–8.PubMedCrossRefGoogle Scholar
- 123.Smith ML, Graitzer HM, Hudson DL, Raven PB. Baroreflex function in endurance- and static exercise-trained men. J Appl Physiol. 1985;1988(64):585–91.Google Scholar
- 124.Ifuku H, Shiraishi Y. Assessment of cardiovascular regulation during head-up tilt and suspension in swimmers. Med Sci Sports Exerc. 2004;36:155–9.PubMedCrossRefGoogle Scholar
- 125.Frederiks J, Swenne CA, Bruschke AV, van der Velde ET, Maan AC, TenVoorde BJ, et al. Correlated neurocardiologic and fitness changes in athletes interrupting training. Med Sci Sports Exerc. 2000;32:571–5.PubMedCrossRefGoogle Scholar