Abstract
Exercise is a major challenge for cardiovascular apparatus since it recruits chronotropic, inotropic, pre-load, and afterload reserves. Regular physical training induces several physiological adaptations leading to an increase in both cardiac volume and mass. It appears that several genderrelated physiological and morphological differences exist in the cardiovascular adjustments and adaptations to dynamic exercise in humans. In this respect, gender may be important in determining these adjustments and adaptations to dynamic exercise due to genetic, endocrine, and body composition differences between sexes. Females seem to have a reduced vasoconstriction and a lower vascular resistance in comparison to males, especially after exercise. Significant differences exist also in the cardiovascular adaptations to physical training, with trained women showing smaller cardiac volume and wall thickness compared with male athletes. In this review, we summarize these differences.
Keywords: Sex hormones, blood pressure, stroke volume, cardiac output, training, exercise.
Graphical Abstract
[1]
Li Y, Kloner RA. Is there a gender difference in infarct size and arrhythmias following experimental coronary occlusion and reperfusion? J Thromb Thrombolysis 1995; 2(3): 221-5.
[2]
Leinwand LA. Sex is a potent modifier of the cardiovascular system. J Clin Invest 2003; 112: 302-4.
[3]
Santos RL, Marin EB, Gonçalves WL, Bissoli NS, Abreu GR, Moyses MR. Sex differences in the coronary vasodilation induced by 17 β-oestradiol in the isolated perfused heart from spontaneously hypertensive rats. Acta Physiol 2010; 200: 203-10.
[4]
Lagranha CJ, Deschamps A, Aponte A, Steenbergen C, Murphy E. Sex differences in the phosphorylation of mithocondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res 2010; 106: 1681-91.
[7]
Marongiu E, Crisafulli A. Gender differences in cardiovascular functions during exercise: A brief review. Sport Sci For Health 2015; 11: 235-41.
[8]
Jochmann N, Stangl K, Garbe E, Baumann G, Stangl V. Female-specific aspects in the pharmacotherapy of chronic cardiovascular diseases. Eur Heart J 2005; 26(16): 1585-95.
[9]
Vongpatanasin W. Autonomic regulation of blood pressure in menopause. Semin Reprod Med 2009; 27(4): 338-45.
[10]
Yamaguchi I, Komatsu E, Miyazawa K. Intersubject variability in cardiac output-O2 uptake relation of men during exercise. J Appl Physiol 1986; 61: 2168-74.
[11]
Stringer W, Hansen JE, Wasserman K. Cardiac output estimated noninvasively from oxygen uptake during exercise. J Appl Physiol 1997; 82: 908-12.
[12]
Proctor DN, Beck KC, Shen PH, Eickhoff TJ, Halliwill JR, Joyner MJ. Influence of age and gender on cardiac output-VO2 relationships during submaximal cycle ergometry. J Appl Physiol 1998; 84: 599-605.
[13]
Crisafulli A, Melis F, Tocco F, et al. Anaerobic Threshold and the oxygen consumption/cardiac output relationship during exercise. Sport Sci For Health 2005; 2: 75-80.
[14]
Crisafulli A, Tocco F, Pittau G, et al. Detection of lactate threshold by including haemodynamic and oxygen extraction data. Physiol Meas 2006; 27: 85-97.
[15]
Crisafulli A, Piras F, Chiappori P, et al. Estimating stroke volume from oxygen pulse during exercise. Physiol Meas 2007; 28: 1201-12.
[17]
Stringer W, Wasserman K, Casaburi R, Pŏrszăsz J, Maehara K, French W. Lactic acidosis as a facilitator of oxyhemoglobin dissociation during exercise. J Appl Physiol 1994; 76: 1462-7.
[18]
Wittenberg BA, Wittenberg JB. Transport of oxygen in muscle. Annu Rev Physiol 1989; 51: 857-78.
[19]
Ogawa T, Spina RJ, Martin WH, et al. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 1992; 86: 494-503.
[20]
Farinatti P, Monteiro W, Oliveira R, Crisafulli A. Cardiorespiratory responses and myocardial function within incremental exercise in healthy unmedicated older vs. young men and women. Aging Clin Exp Res 2018; 30(4): 341-9.
[21]
Hossack KF, Bruce RA. Maximal cardiac function in sedentary normal men and women: comparison of age-related changes. J Appl Physiol 1982; 53: 799-804.
[22]
Higginbotham MB, Morris KG, Williams RS, McHale PA, Coleman RE, Cobb FR. Regulation of stroke volume during submaximal and maximal upright exercise in normal man. Circ Res 1986; 58: 281-91.
[23]
Nóbrega ACL, O’Leary DS, 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.Article ID 478965
[24]
Crisafulli A, Marongiu E, Ogho S. Cardiovascular reflexes activity and their interaction during exercise. BioMed Res Int 2015.Article ID 394183
[25]
Green AL, Paterson DJ. Identification of the neurocircuitry controlling cardiovascular function in humans using functional neurosurgery: Implications for exercise control. Exp Physiol 2008; 93: 1022-8.
[26]
O’Leary DS. Autonomic mechanisms of muscle metaboreflex control of heart rate. J Appl Physiol 1993; 74: 1748-54.
[27]
Kaur J, Spranger MD, Hammond RL, et al. Muscle metaboreflex activation during dynamic exercise evokes epinephrine release resulting in β2-mediated vasodilation. Am J Physiol Heart Circ Physiol 2015; 308: H524-9.
[28]
Crisafulli A. The impact of cardiovascular diseases on cardiovascular regulation during exercise in humans: Studies on metaboreflex activation elicited by the post-exercise muscle ischemia method. Curr Cardiol Rev 2017; 13(4): 293-300.
[29]
Fadel PJ, Ogoh S, Watenapaugh DE, et al. Carotid baroreflex regulation of sympathetic nerve activity during dynamic exercise in humans. Am J Physiol Heart Circ Physiol 2001; 280: H1383-90.
[30]
Sheriff DD. Baroreflex resetting during exercise: Mechanisms and meaning. Am J Physiol Heart Circ Physiol 2006; 290: H1406-7.
[31]
Raven PB, Fadel PJ, Ogoh S. Arterial baroreflex resetting during exercise: A current perspective. Exp Physiol 2006; 91: 37-49.
[32]
Blomquist CG, Salting B. Cardiovascular adaptations to physical training. Annu Rev Physiol 1983; 45: 169-89.
[33]
Maron BJ. Structural features of the athletes heart as defined by echocardiography. J Am Coll Cardiol 1986; 7: 190-203.
[35]
Sharma S. Athlete’s heart – effect of age, sex, ethnicity and sporting discipline. Exp Physiol 2003; 88: 665-9.
[36]
Bassareo PP, Saba L, Solla P, Barbanti C, Marras AR, Mercuro G. Factors influencing adaptation and performance at physical exercise in complex congenital heart diseases after surgical repair. BioMed Res Int 2014; 2014862372
[37]
Penna C, Tullio F, Merlino A, et al. Postconditioning cardioprotection against infarct size and post-ischemic systolic dysfunction is influenced by gender. Basic Res Cardiol 2009; 104: 390-402.
[38]
Christou DD, Jones PP, Jordan J, Diedrich A, Robertson D, Seals DR. Women have lower tonic autonomic support of arterial blood pressure and less effective baroreflex buffering than men. Circulation 2005; 111(4): 494-8.
[39]
Schmitt JA, Joyner MJ, Charkoudian N, Wallin BG, Hart EC. Sex differences in alpha-adrenergic support of blood pressure. Clin Auton Res 2010; 20(4): 271-5.
[40]
Convertino VA. Gender differences in autonomic function associated with blood pressure regulation. Am J Physiol 1998; 275: 1909-20.
[41]
Carter R, Watenpaugh DE, Smith ML. Selected contribution: Gender differences in cardiovascular regulation during recovery from exercise. J Appl Physiol 2001; 91: 1902-7.
[42]
Senitko AN, Charchoudian N, Halliwill JR. Influence of endurance exercise training status and gender on postexercise hypotension. J Appl Physiol 2002; 92: 2368-74.
[43]
Reckelhoff JF. Gender differences in regulation of blood pressure. Hypertension 2001; 37: 1199-208.
[44]
Ogola BO, Zimmerman MA, Clark GL, et al. New insights into arterial stiffening: Does sex matter? Am J Physiol Heart Circ Physiol 2018; 315(5): H1073-87.
[45]
Dimpka U, Ugwu A, Oshi D. Assessment of sex differences in systolic blood pressure responses to exercise in healthy, non-athletic young adultsJEP online 2008; 11: 18-25
[46]
Wheatley CM, Snyder EM, Johnson BD, Olson TP. Sex differences in cardiovascular function during submaximal exercise in humans. Springerplus 2014; 3: 445.
[47]
O’Toole ML. Gender differences in the cardiovascular response to exercise. Cardiovasc Clin 1989; 19: 17-33.
[48]
Maruf FA, Ogochukwu UN, Dim PA, Alada AR. Absence of sex differences in systolic blood pressure and heart rate responses to exercise in healthy young adults. Niger J Physiol Sci 2012; 27: 95-100.
[49]
Gardin JM, Savage DD, Ware JH, Henry WL. Effect of age, sex, and body surface area on echocardiographic left ventricular wall mass in normal subjects. Hypertension 1987; 9: 36-9.
[50]
Hutchinson PL, Cureton KJ, Outz H, Wilson G. Relationship of cardiac size to maximal oxygen uptake and body size in men and women. Int J Sports Med 1991; 12: 369-73.
[51]
Fu Q, Levine BD. Cardiovascular response to exercise in women. Med Sci Sports Exerc 2005; 37: 1433-5.
[52]
Sullivan MJ, Cobb FR, Higginbotham MB. Stroke volume increases by similar mechanisms during upright exercise in normal men and women. Am J Cardiol 1991; 67: 1147-54.
[53]
Poliner LR, Dehmer GJ, Lewis SE, Parkey RW, Blomqvist CG, Willerson JT. Left ventricular performance in normal subjects: a comparison of the responses to exercise in the upright and supine positions. Circulation 1980; 62: 528-34.
[54]
Higginbotham MB, Morris KG, Coleman RE, Cobb FR. Sex-related differences in the normal cardiac response to upright exercise. Circulation 1984; 70: 357-66.
[55]
Steingart RM, Wexler J, Slagle S, Scheuer J. Radionuclide ventriculographic responses to graded supine and upright exercise: Critical role of the Frank-Starling mechanism at submaximal exercise. Am J Cardiol 1984; 53: 1671-7.
[56]
Adams KF, Vincent LM, McAllister SM, El-Ashnmawy H, Sheps DS. The influence of age and gender on left ventricular response to supine exercise in asymptomaticnormal subjects. Am Heart J 1987; 113: 732-42.
[57]
Hanley PC, Zinsmeister AR, Clements IP, Bove AA, Brown ML, Gibbson RJ. Gender related differences in cardiac response to supine exercise assessed by radionuclide angiography. J Am Coll Cardiol 1989; 13: 624-9.
[58]
Gledhill N, Cox D, Jamnik R. Endurance athletes’ stroke volume does not plateau: major advantage is diastolic function. Med Sci Sports Exerc 1994; 26: 1116-21.
[59]
Zhou B, Conlee RK, Jensen R, Fellingham GW, George JD, Fisher AG. Stroke volume does not plateau during graded exercise in elite male distance runners. Med Sci Sports Exerc 2001; 33: 1849-54.
[60]
Vella CA, Robergs RA. A review of the stroke volume response to upright exercise in healthy subjects. Br J Sports Med 2005; 39(4): 190-5.
[61]
Wang E, Solli GS, Nyberg SK, Hoff J, Helgerud J. Stroke volume does not plateau in female endurance athletes. Int J Sports Med 2012; 33: 734-9.
[62]
Astrand PO, Cuddy TE, Saltin B, Stenberg J. Cardiac output during submaximal and maximal work. J Appl Physiol 1964; 19: 268-74.
[63]
Fleg JL, O’Connor F, Gernstenblith G, et al. Impact of age on the cardiovascular response to dynamic upright exercise in healthy men and women. J Appl Physiol 1995; 78: 890-900.
[64]
Fitzgerald MD, Tanaka H, Tran ZV, Seals DR. Age-related decline in maximal aerobic capacity in regularly exercising vs. sedentary females: A meta-analysis. J Appl Physiol 1997; 83: 160-5.
[65]
Charkoudian N. Influences of female reproductive hormones on sympathetic control of the circulation in humans. Clin Auton Res 2001; 11: 295-301.
[66]
Wallin BG, Hart EC, Wehrwein EA, Charkoudian N, Joyner MJ. Relationship between breathing and cardiovascular function at rest: sex-related differences. Acta Physiol 2010; 200: 193-200.
[67]
Raemakers D, Ector H, Aubert AE, Rubens A. Van de Werf. Heart rate variability and heart rate in healthy volunteers. Is the female autonomic nervous system cardioprotective? Eur Heart J 1998; 19: 1334-41.
[68]
Barnett SR, Morin RJ, Kiely DK, et al. Effects of age and gender on autonomic control of blood pressure dynamics. Hypertension 1999; 33: 301-6.
[69]
Evans JM, Zielgler MG, Patwardhan AR, et al. Gender differences in autonomic cardiovascular regulation: Spectral, hormonal, and hemodynamics indexes. J Appl Physiol 2001; 91: 2611-8.
[70]
Fisher JP, Adlan AM, Shantsila A, Secher FJ, Sørensen H, Secher NH. Muscle metaboreflex and autonomic regulation of heart rate in humans. J Physiol 2013; 591: 3777-88.
[71]
Carter III R, Watenpaugh DE, Wasmund WL, Wasmund SL, Smith ML. Muscle pump and central command during recovery from exercise in humans. J Appl Physiol 1999; 87: 1463-9.
[72]
Crisafulli A, Melis F, Orrù V, Lener R, Lai C, Concu A. Hemodynamics during a postexertional asystolia in a healthy athlete: A case study. Med Sci Sports Exerc 2000; 32: 4-9.
[73]
Cote AT, Phillips AA, Foulds HJ, et al. Sex differences in cardiac function after prolonged strenuous exercise. Clin J Sport Med 2015; 25(3): 276-83.
[74]
Macey PM, Rieken NS, Ogren JA, Macey KE, Kumar R, Harper RM. Sex differences in insular cortex gyri responses to a brief static handgrip challenge. Biol Sex Differ 2017; 8: 13.
[75]
Ettinger SM, Silber DH, Collins BG, et al. Influences of gender on sympathetic nerve responses to static exercise. J Appl Physiol 1996; 80(1): 245-51.
[76]
Lalande S, Barron CC, Shoemaker JK. Sex difference in the influence of central blood volume mobilization on the exercise pressor response. Eur J Appl Physiol 2015; 115(12): 2653-60.
[77]
Minahan C, O’Neill H, Sikkema N, Joyce S, Larsen B, Sabapathy S. Oral contraceptives augment the exercise pressor reflex during isometric handgrip exercise. Physiol Rep 2018; 6(5)
[http://dx.doi.org/10.14814/phy2.13629]
[http://dx.doi.org/10.14814/phy2.13629]
[78]
Parmar HR, Sears J, Molgat-Seon Y, et al. Oral contraceptives modulate the muscle metaboreflex in healthy young women. Appl Physiol Nutr Metab 2018; 43(5): 460-6.
[79]
Ives SJ, McDaniel J, Witman MA, Richardson RS. Passive limb movement: evidence of mechanoreflex sex specificity. Am J Physiol Heart Circ Physiol 2013; 304(1): H154-61.
[80]
Abdel-Rahman AR, Merrill RH, Wooles WR. Gender-related differences in the baroreceptor reflex control of heart rate in normotensive humans. J Appl Physiol 1994; 77(2): 606-13.
[81]
Laitinen T, Hartikainen J, Vanninen E, Niskanen L, Geelen G, Länsimies E. Age and gender dependency of baroreflex sensitivity in healthy subjects. J Appl Physiol 1998; 84(2): 576-83.
[82]
Cooke WH, Ludwig DA, Hogg PS, Eckberg DL, Convertino VA. Does the menstrual cycle influence the sensitivity of vagally mediated baroreflexes? Clin Sci (Lond) 2002; 102(6): 639-44.
[83]
Tank J, Diedrich A, Szczech E, Luft FC, Jordan J. Baroreflex regulation of heart rate and sympathetic vasomotor tone in women and men. Hypertension 2005; 45(6): 1159-64.
[84]
Fisher JP, Kim A, Hartwich D, Fadel PJ. New insights into the effects of age and sex on arterial baroreflex function at rest and during dynamic exercise in humans. Auton Neurosci 2012; 172(1-2): 13-22.
[85]
Kingsley JD, Tai YL, Marshall EM, et al. Autonomic modulation and baroreflex sensitivity after acute resistance exercise: Responses between sexes. J Sports Med Phys Fitness 2018 (at press).
[86]
Kim A, Deo SH, Fisher JP, Fadel PJ. Effect of sex and ovarian hormones on carotid baroreflex resetting and function during dynamic exercise in humans. J Appl Physiol 2012; 112(8): 1361-71.
[87]
Teixeira AL, Ritti-Dias R, Antonino D, Bottaro M, Millar PJ, Vianna LC. Sex differences in cardiac baroreflex sensitivity after isometric handgrip exercise. Med Sci Sports Exerc 2018; 50(4): 770-7.
[88]
Samora M, Teixeira AL, Sabino-Carvalho JL, Vianna LC. Spontaneous cardiac baroreflex sensitivity is enhanced during post-exercise ischemia in men but not in women Eur J Appl Physiol 2018 (at press)
[89]
Pelliccia A, Maron B, Culasso F, Spataro A, Caselli G. Athlete’s heart in women. Echocardiographic characterisation of highly trained elite female athletes. JAMA 1996; 276: 211-5.
[90]
Sharma S, Maron BJ, Whyte G, Firoozi S, Elliott PM, McKenna WJ. Physiologic limits of left ventricular hypertrophy in junior elite athletes: relevant to differential diagnosis of athlete’s heart and hypertrophic cardiomyopathy. J Am Coll Cardiol 2002; 40: 1431-6.
[91]
Rowland T, Roti M. Influence of sex on the “Athlete’s Heart” in trained cyclists. J Sci Med Sport 2010; 13(5): 475-8.
[92]
Whyte GP, George K, Sharma S, et al. The upper limit of physiological cardiac hypertrophy in elite male and female athletes: The British experience. Eur J Appl Physiol 2004; 92(4-5): 592-7.
[93]
Whyte GP, George K, Nevill A, Shave R, Sharma S, McKenna WJ. Left ventricular morphology and function in female athletes: A meta-analysis. Int J Sports Med 2004; 25(5): 380-3.
[94]
Bernardo BC, Weeks KL, Pretorius L, McMullen JR. Molecular distinction between physiological and pathological cardiac hypertrophy: Experimental findings and therapeutic strategies. Pharmacol Ther 2010; 128(1): 191-227.
[95]
Foryst-Ludwig A, Kintscher U. Sex differences in exercise-induced cardiac hypertrophy. Pflugers Arch 2013; 465(5): 731-7.
[96]
Petersen SE, Wiesmann F, Hudsmith LE, et al. Functional and structural vascular remodeling in elite rowers assessed by cardiovascular magnetic resonance. J Am Coll Cardiol 2006; 48(4): 790-7.
[97]
Giraldeau G, Kobayashi Y, Finocchiaro G, et al. Gender differences in ventricular remodeling and function in college athletes, insights from lean body mass scaling and deformation imaging. Am J Cardiol 2015; 116(10): 1610-6.
Article Metrics
3