Endothelial dysfunction and menopause: is exercise an effective countermeasure?

References

• Mozaffarian D, Benjamin EJ, Go AS, et al. Heart disease and stroke statistics–2015 update: a report from the American Heart Association. Circulation 2015;131:e29–322
   PubMed Web of Science ®Google Scholar
• Kaplan JR, Manuck SB. Ovarian dysfunction and the premenopausal origins of coronary heart disease. Menopause 2008;15:768–76
   PubMed Web of Science ®Google Scholar
• Rossi R, Nuzzo A, Origliani G, et al. Prognostic role of flow-mediated dilation and cardiac risk factors in post-menopausal women. J Am Coll Cardiol 2008;51:997–1002
   PubMed Web of Science ®Google Scholar
• Zeiher AM, Drexler H, Wollschlager H, et al. Endothelial dysfunction of the coronary microvasculature is associated with coronary blood flow regulation in patients with early atherosclerosis. Circulation 1991;84:1984–92
   PubMed Web of Science ®Google Scholar
• Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 2000;101:1899–906
   PubMed Web of Science ®Google Scholar
• Moreau KL, Hildreth KL, Meditz AL, et al. Endothelial function is impaired across the stages of the menopause transition in healthy women. J Clin Endocrinol Metab 2012;97:4692–700
   PubMed Web of Science ®Google Scholar
• Hildreth KL, Kohrt WM, Moreau KL. Oxidative stress contributes to large elastic arterial stiffening across the stages of the menopausal transition. Menopause 2014;21:624–32
   PubMed Web of Science ®Google Scholar
• Kretzschmar J, Babbitt DM, Diaz KM, et al. A standardized exercise intervention differentially affects premenopausal and postmenopausal African-American women. Menopause 2014;21:579–84
   PubMed Web of Science ®Google Scholar
• Moore DJ, Gonzales JU, Tucker SH, et al. Exercise-induced vasodilation is associated with menopause stage in healthy middle-aged women. Appl Physiol Nutr Metab 2012;37:418–24
   PubMed Web of Science ®Google Scholar
• Moreau KL, Stauffer BL, Kohrt WM, et al. Essential role of estrogen for improvements in vascular endothelial function with endurance exercise in postmenopausal women. J Clin Endocrinol Metab 2013;98:4507–15
   PubMed Web of Science ®Google Scholar
• Santos-Parker JR, Strahler TR, Vorwald VM, et al. Habitual aerobic exercise does not protect against micro- or macrovascular endothelial dysfunction in healthy estrogen-deficient postmenopausal women. J Appl Physiol 2017;122:11–19
   PubMed Web of Science ®Google Scholar
• Serviente C, Troy LM, de Jonge M, et al. Endothelial and inflammatory responses to acute exercise in perimenopausal and late postmenopausal women. Am J Physiol Regul Integr Comp Physiol 2016;311:R841–50
   PubMed Web of Science ®Google Scholar
• Roger VL, Go AS, Lloyd-Jones DM, et al. Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation 2011;123:e18–19
   PubMed Web of Science ®Google Scholar
• Ford ES, Ajani UA, Croft JB, et al. Explaining the decrease in U.S. deaths from coronary disease, 1980-2000. N Engl J Med 2007;356:2388–98
   PubMed Web of Science ®Google Scholar
• Gulati M, Shaw LJ, Bairey Merz CN. Myocardial ischemia in women: lessons from the NHLBI WISE study. Clin Cardiol 2012;35:141–8
   PubMed Web of Science ®Google Scholar
• Peters SA, Huxley RR, Woodward M. Diabetes as risk factor for incident coronary heart disease in women compared with men: a systematic review and meta-analysis of 64 cohorts including 858,507 individuals and 28,203 coronary events. Diabetologia 2014;57:1542–51
   PubMed Web of Science ®Google Scholar
• Huxley R, Barzi F, Woodward M. Excess risk of fatal coronary heart disease associated with diabetes in men and women: meta-analysis of 37 prospective cohort studies. BMJ 2006;332:73–8
   PubMed Web of Science ®Google Scholar
• Appelman Y, van Rijn BB, Ten Haaf ME, et al. Sex differences in cardiovascular risk factors and disease prevention. Atherosclerosis 2015;241:211–18
   PubMed Web of Science ®Google Scholar
• Chakrabarti S, Morton JS, Davidge ST. Mechanisms of estrogen effects on the endothelium: an overview. Can J Cardiol 2014;30:705–12
   PubMed Web of Science ®Google Scholar
• Knowlton AA. Estrogen and cardiovascular disease: aging and estrogen loss at the heart of the matter? Future Cardiol 2012;8:9–12
   PubMedGoogle Scholar
• Kannel WB, Hjortland MC, McNamara PM, et al. Menopause and risk of cardiovascular disease: the Framingham study. Ann Intern Med 1976;85:447–52
   PubMed Web of Science ®Google Scholar
• Matthews KA, Crawford SL, Chae CU, et al. Are changes in cardiovascular disease risk factors in midlife women due to chronological aging or to the menopausal transition? J Am Coll Cardiol 2009;54:2366–73
   PubMed Web of Science ®Google Scholar
• Rivera CM, Grossardt BR, Rhodes DJ, et al. Increased cardiovascular mortality after early bilateral oophorectomy. Menopause 2009;16:15–23
   PubMed Web of Science ®Google Scholar
• Hu FB, Grodstein F, Hennekens CH, et al. Age at natural menopause and risk of cardiovascular disease. Arch Intern Med 1999;159:1061–6
   PubMed Web of Science ®Google Scholar
• Witteman JC, Grobbee DE, Kok FJ, et al. Increased risk of atherosclerosis in women after the menopause. BMJ 1989;298:642–4
   PubMed Web of Science ®Google Scholar
• El Khoudary SR, Santoro N, Chen HY, et al. Trajectories of estradiol and follicle-stimulating hormone over the menopause transition and early markers of atherosclerosis after menopause. Eur J Prev Cardiolog 2016;23:694–703
   PubMed Web of Science ®Google Scholar
• El Khoudary SR, Wildman RP, Matthews K, et al. Progression rates of carotid intima-media thickness and adventitial diameter during the menopausal transition. Menopause 2013;20:8–14
   PubMed Web of Science ®Google Scholar
• Lambrinoudaki I, Armeni E, Georgiopoulos G, et al. Subclinical atherosclerosis in menopausal women with low to medium calculated cardiovascular risk. Int J Cardiol 2013;164:70–6
   PubMed Web of Science ®Google Scholar
• Maturana MA, Franz RF, Metzdorf M, et al. Subclinical cardiovascular disease in postmenopausal women with low/medium cardiovascular risk by the Framingham risk score. Maturitas 2015;81:311–16
   PubMed Web of Science ®Google Scholar
• Zeiher AM, Drexler H, Wollschlager H, et al. Modulation of coronary vasomotor tone in humans. Progressive endothelial dysfunction with different early stages of coronary atherosclerosis. Circulation 1991;83:391–401
   PubMed Web of Science ®Google Scholar
• Brevetti G, Silvestro A, Schiano V, et al. Endothelial dysfunction and cardiovascular risk prediction in peripheral arterial disease: additive value of flow-mediated dilation to ankle-brachial pressure index. Circulation 2003;108:2093–8
   PubMed Web of Science ®Google Scholar
• Gokce N, Keaney JF Jr, Hunter LM, et al. Predictive value of noninvasively determined endothelial dysfunction for long-term cardiovascular events in patients with peripheral vascular disease. J Am Coll Cardiol 2003;41:1769–75
   PubMed Web of Science ®Google Scholar
• Yeboah J, Crouse JR, Hsu FC, et al. Brachial flow-mediated dilation predicts incident cardiovascular events in older adults: the Cardiovascular Health Study. Circulation 2007;115:2390–7
   PubMed Web of Science ®Google Scholar
• Green DJ, Dawson EA, Groenewoud HM, et al. Is flow-mediated dilation nitric oxide mediated?: a meta-analysis. Hypertension 2014;63:376–82
   PubMed Web of Science ®Google Scholar
• Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007;87:315–424
   PubMed Web of Science ®Google Scholar
• Celermajer DS, Sorensen KE, Gooch VM, et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992;340:1111–15
   PubMed Web of Science ®Google Scholar
• Takase B, Uehata A, Akima T, et al. Endothelium-dependent flow-mediated vasodilation in coronary and brachial arteries in suspected coronary artery disease. Am J Cardiol 1998;82:1535–9
   PubMed Web of Science ®Google Scholar
• Takase B, Hamabe A, Satomura K, et al. Close relationship between the vasodilator response to acetylcholine in the brachial and coronary artery in suspected coronary artery disease. Int J Cardiol 2005;105:58–66
   PubMed Web of Science ®Google Scholar
• Thijssen DH, Black MA, Pyke KE, et al. Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 2011;300:H2–12
   PubMed Web of Science ®Google Scholar
• Shimbo D, Grahame-Clarke C, Miyake Y, et al. The association between endothelial dysfunction and cardiovascular outcomes in a population-based multi-ethnic cohort. Atherosclerosis 2007;192:197–203
   PubMed Web of Science ®Google Scholar
• Yeboah J, Sutton-Tyrrell K, McBurnie MA, et al. Association between brachial artery reactivity and cardiovascular disease status in an elderly cohort: the cardiovascular health study. Atherosclerosis 2008;197:768–76
   PubMed Web of Science ®Google Scholar
• Modena MG, Bonetti L, Coppi F, et al. Prognostic role of reversible endothelial dysfunction in hypertensive postmenopausal women. J Am Coll Cardiol 2002;40:505–10
   PubMed Web of Science ®Google Scholar
• Kitta Y, Nakamura T, Kodama Y, et al. Endothelial vasomotor dysfunction in the brachial artery is associated with late in-stent coronary restenosis. J Am Coll Cardiol 2005;46:648–55
   PubMed Web of Science ®Google Scholar
• Kitta Y, Obata JE, Nakamura T, et al. Persistent impairment of endothelial vasomotor function has a negative impact on outcome in patients with coronary artery disease. J Am Coll Cardiol 2009;53:323–30
   PubMed Web of Science ®Google Scholar
• Chan SY, Mancini GB, Kuramoto L, et al. The prognostic importance of endothelial dysfunction and carotid atheroma burden in patients with coronary artery disease. J Am Coll Cardiol 2003;42:1037–43
   PubMed Web of Science ®Google Scholar
• Green DJ, Jones H, Thijssen D, et al. Flow-mediated dilation and cardiovascular event prediction: does nitric oxide matter? Hypertension 2011;57:363–9
   PubMed Web of Science ®Google Scholar
• Green DJ, Eijsvogels T, Bouts YM, et al. Exercise training and artery function in humans: nonresponse and its relationship to cardiovascular risk factors. J Appl Physiol 2014;117:345–52
   PubMed Web of Science ®Google Scholar
• Celermajer DS, Sorensen KE, Spiegelhalter DJ, et al. Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 1994;24:471–6
   PubMed Web of Science ®Google Scholar
• Taddei S, Virdis A, Ghiadoni L, et al. Menopause is associated with endothelial dysfunction in women. Hypertension 1996;28:576–82
   PubMed Web of Science ®Google Scholar
• Jensen-Urstad K, Johansson J. Gender difference in age-related changes in vascular function. J Intern Med 2001;250:29–36
   PubMed Web of Science ®Google Scholar
• Miller VM, Duckles SP. Vascular actions of estrogens: functional implications. Pharmacol Rev 2008;60:210–41
   PubMed Web of Science ®Google Scholar
• Usselman CW, Stachenfeld NS, Bender JR. The molecular actions of oestrogen in the regulation of vascular health. Exp Physiol 2016;101:356–61
   PubMed Web of Science ®Google Scholar
• Kassi E, Spilioti E, Nasiri-Ansari N, et al. Vascular inflammation and atherosclerosis: the role of estrogen receptors. Curr Med Chem 2015;22:2651–65
   PubMed Web of Science ®Google Scholar
• Gavin KM, Seals DR, Silver AE, et al. Vascular endothelial estrogen receptor alpha is modulated by estrogen status and related to endothelial function and endothelial nitric oxide synthase in healthy women. J Clin Endocrinol Metab 2009;94:3513–20
   PubMed Web of Science ®Google Scholar
• Wagner AH, Schroeter MR, Hecker M. 17beta-estradiol inhibition of NADPH oxidase expression in human endothelial cells. Faseb J 2001;15:2121–30
   PubMed Web of Science ®Google Scholar
• Peterson TE, Poppa V, Ueba H, et al. Opposing effects of reactive oxygen species and cholesterol on endothelial nitric oxide synthase and endothelial cell caveolae. Circ Res 1999;85:29–37
   PubMed Web of Science ®Google Scholar
• Kuzkaya N, Weissmann N, Harrison DG, et al. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J Biol Chem 2003;278:22546–54
   PubMed Web of Science ®Google Scholar
• Blake GJ, Ridker PM. Novel clinical markers of vascular wall inflammation. Circ Res 2001;89:763–71
   PubMed Web of Science ®Google Scholar
• Stork S, van der Schouw YT, Grobbee DE, et al. Estrogen, inflammation and cardiovascular risk in women: a critical appraisal. Trends Endocrinol Metab 2004;15:66–72
   PubMed Web of Science ®Google Scholar
• Hashimoto M, Akishita M, Eto M, et al. Modulation of endothelium-dependent flow-mediated dilatation of the brachial artery by sex and menstrual cycle. Circulation 1995;92:3431–5
   PubMed Web of Science ®Google Scholar
• Williams MR, Westerman RA, Kingwell BA, et al. Variations in endothelial function and arterial compliance during the menstrual cycle. J Clin Endocrinol Metab 2001;86:5389–95
   PubMed Web of Science ®Google Scholar
• Pinto S, Virdis A, Ghiadoni L, et al. Endogenous estrogen and acetylcholine-induced vasodilation in normotensive women. Hypertension 1997;29:268–73
   PubMed Web of Science ®Google Scholar
• Lieberman EH, Gerhard MD, Uehata A, et al. Estrogen improves endothelium-dependent, flow-mediated vasodilation in postmenopausal women. Ann Intern Med 1994;121:936–41
   PubMed Web of Science ®Google Scholar
• Gilligan DM, Badar DM, Panza JA, et al. Acute vascular effects of estrogen in postmenopausal women. Circulation 1994;90:786–91
   PubMed Web of Science ®Google Scholar
• Sherwood A, Bower JK, McFetridge-Durdle J, et al. Age moderates the short-term effects of transdermal 17beta-estradiol on endothelium-dependent vascular function in postmenopausal women. Arterioscler Thromb Vasc Biol 2007;27:1782–7
   PubMed Web of Science ®Google Scholar
• Rossouw JE, Prentice RL, Manson JE, et al. Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause. JAMA 2007;297:1465–77
   PubMed Web of Science ®Google Scholar
• Bassuk SS, Manson JE. The timing hypothesis: Do coronary risks of menopausal hormone therapy vary by age or time since menopause onset? Metab Clin Exp 2016;65:794–803
   PubMed Web of Science ®Google Scholar
• Howard BV, Rossouw JE. Estrogens and cardiovascular disease risk revisited: the Women’s Health Initiative. Curr Opin Lipidol 2013;24:493–9
   PubMed Web of Science ®Google Scholar
• Harman SM. Menopausal hormone treatment cardiovascular disease: another look at an unresolved conundrum. Fertil Steril 2014;101:887–97
   PubMed Web of Science ®Google Scholar
• Stuenkel CA, Davis SR, Gompel A, et al. Treatment of symptoms of the menopause: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab 2015;100:3975–4011
   PubMed Web of Science ®Google Scholar
• Klawitter J, Hildreth KL, Christians U, et al. A relative L-arginine deficiency contributes to endothelial dysfunction across the stages of the menopausal transition. Phy 2 2017;5:e13409
   Google Scholar
• Moreau KL, Meditz A, Deane KD, et al. Tetrahydrobiopterin improves endothelial function and decreases arterial stiffness in estrogen-deficient postmenopausal women. Am J Physiol Heart Circ Physiol 2012;302:H1211–18
   PubMed Web of Science ®Google Scholar
• Nyberg M, Seidelin K, Andersen TR, et al. Biomarkers of vascular function in premenopausal and recent postmenopausal women of similar age: effect of exercise training. Am J Physiol Regul Integr Comp Physiol 2014;306:R510–17
   PubMed Web of Science ®Google Scholar
• Di Francescomarino S, Sciartilli A, Di Valerio V, et al. The effect of physical exercise on endothelial function. Sports Med 2009;39:797–812
   PubMed Web of Science ®Google Scholar
• Moreau KL, Hildreth KL. Vascular aging across the menopause transition in healthy women. Adv Vasc Med 2014;2014:204390
   PubMedGoogle Scholar
• Green DJ, Maiorana A, O’driscoll G, et al. Effect of exercise training on endothelium-derived nitric oxide function in humans. J Physiol (Lond) 2004;561:1–25
   Google Scholar
• Hambrecht R, Adams V, Erbs S, et al. Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 2003;107:3152–8
   PubMed Web of Science ®Google Scholar
• Schuler G, Adams V, Goto Y. Role of exercise in the prevention of cardiovascular disease: results, mechanisms, and new perspectives. Eur Heart J 2013;34:1790–9
   PubMed Web of Science ®Google Scholar
• Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 2000;87:840–4
   PubMed Web of Science ®Google Scholar
• Hollander J, Fiebig R, Gore M, et al. Superoxide dismutase gene expression is activated by a single bout of exercise in rat skeletal muscle. Pflugers Arch 2001;442:426–34
   PubMed Web of Science ®Google Scholar
• Kojda G, Hambrecht R. Molecular mechanisms of vascular adaptations to exercise. Physical activity as an effective antioxidant therapy? Cardiovasc Res 2005;67:187–97
   PubMed Web of Science ®Google Scholar
• Santos-Parker JR, LaRocca TJ, Seals DR. Aerobic exercise and other healthy lifestyle factors that influence vascular aging. Adv Physiol Educ 2014;38:296–307
   PubMed Web of Science ®Google Scholar
• Black MA, Cable NT, Thijssen DH, et al. Impact of age, sex, and exercise on brachial artery flow-mediated dilatation. Am J Physiol Heart Circ Physiol 2009;297:H1109–16
   PubMed Web of Science ®Google Scholar
• Swift DL, Weltman JY, Patrie JT, et al. Predictors of improvement in endothelial function after exercise training in a diverse sample of postmenopausal women. J Womens Health (Larchmt) 2014;23:260–6
   PubMed Web of Science ®Google Scholar
• Pierce GL, Eskurza I, Walker AE, et al. Sex-specific effects of habitual aerobic exercise on brachial artery flow-mediated dilation in middle-aged and older adults. Clin Sci 2011;120:13–23
   PubMed Web of Science ®Google Scholar
• Swift DL, Earnest CP, Blair SN, et al. The effect of different doses of aerobic exercise training on endothelial function in postmenopausal women with elevated blood pressure: results from the DREW study. Br J Sports Med 2012;46:753–8
   PubMed Web of Science ®Google Scholar
• Casey DP, Pierce GL, Howe KS, et al. Effect of resistance training on arterial wave reflection and brachial artery reactivity in normotensive postmenopausal women. Eur J Appl Physiol 2007;100:403–8
   PubMed Web of Science ®Google Scholar
• Klonizakis M, Moss J, Gilbert S, et al. Low-volume high-intensity interval training rapidly improves cardiopulmonary function in postmenopausal women. Menopause 2014;21:1099–105
   PubMed Web of Science ®Google Scholar
• Sanders K, Maresh CM, Ballard KD, et al. Habitual exercise may maintain endothelium-dependent dilation in overweight postmenopausal women. J Aging Physical Activity 2015;23:40–6
   PubMed Web of Science ®Google Scholar
• Harvey P, Morris B, Kubo T, et al. Hemodynamic after-effects of acute dynamic exercise in sedentary normotensive postmenopausal women. J Hypertens 2005;23:285–92
   PubMed Web of Science ®Google Scholar
• Harvey P, Picton P, Su W, et al. Exercise as an alternative to oral estrogen for amelioration of endothelial dysfunction in postmenopausal women. Am Heart J 2005;149:291–7
   PubMed Web of Science ®Google Scholar
• Yoo JK, Pinto MM, Kim HK, et al. Sex impacts the flow-mediated dilation response to acute aerobic exercise in older adults. Exp Gerontol 2017;91:57–63
   PubMed Web of Science ®Google Scholar
• Claudio ER, Endlich PW, Santos RL, et al. Effects of chronic swimming training and oestrogen therapy on coronary vascular reactivity and expression of antioxidant enzymes in ovariectomized rats. PLoS One 2014;8:e64806
   PubMed Web of Science ®Google Scholar
• Braga VA, Couto GK, Lazzarin MC, et al. Aerobic exercise training prevents the onset of endothelial dysfunction via increased nitric oxide bioavailability and reduced reactive oxygen species in an experimental model of menopause. PLoS One 2015;10:e0125388
   PubMed Web of Science ®Google Scholar
• Bechlioulis A, Kalantaridou SN, Naka KK, et al. Endothelial function, but not carotid intima-media thickness, is affected early in menopause and is associated with severity of hot flushes. J Clin Endocrinol Metab 2010;95:1199–206
   PubMed Web of Science ®Google Scholar
• Thurston RC, Johnson BD, Shufelt CL, et al. Menopausal symptoms and cardiovascular disease mortality in the Women’s Ischemia Syndrome Evaluation (WISE). Menopause 2017;24:126–32
   PubMed Web of Science ®Google Scholar
• Thurston RC, Chang Y, Barinas-Mitchell E, et al. Physiologically assessed hot flashes and endothelial function among midlife women. Menopause 2017;24:886–93
   PubMed Web of Science ®Google Scholar
• Mandrup CM, Egelund J, Nyberg M, et al. Effects of high-intensity training on cardiovascular risk factors in premenopausal and postmenopausal women. Am J Obstet Gynecol 2017;216:384e1–11
   Web of Science ®Google Scholar