Autonomic cardiovascular damage during post-menopause: The role of physical training

Aging and Disease

Volumn 4, Issue 6, 2013, Pages 320-328

  Souza, Hugo C D ^a   Tezini, Geisa C S V ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Aging; Cardiovascular autonomic control; Menopause; Physical training

Indexed keywords

EID: 84916878166     PISSN: None     EISSN: 21525250     Source Type: Journal    
DOI: 10.14336/AD.2013.0400320     Document Type: Review

References (129)

1. Report of a WHO Scientific Group (1996). Research on the menopause in the 1990s. World Health Organ Tech Rep Ser, 866: 1-107.
2. Kalantaridou SN, Naka KK, Bechlioulis A, Makrigiannakis A, Michalis L, et al. (2006). Premature ovarian failure, endothelial dysfunction and estrogen-progestogen replacement. Trends Endocrinol Metab, 17: 101-109.
3. Chang SH, Kim C-S, Lee K-S, Kim H, Yim SV, et al. (2007). Premenopausal factors influencing premature ovarian failure and early menopause. Maturitas, 58: 19-30.
4. Coulam CB, Adamson SC, Annegers JF (1986). Incidence of premature ovarian failure. Obstet Gynecol, 67: 604-606.
5. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, et al. (2013). Heart disease and stroke statistics--2013 update: a report from the American Heart Association. Circulation, 127: e6-e245.
6. Nichols M, Townsend N, Scarborough P, Luengo-Fernandez R, Leal J, et al. (2012). European Cardiovascular Disease Statistics. Brussels: European Heart Network, Sophia Antipolis: European Society of Cardiology.
7. Nichols M, Townsend N, Scarborough P, Rayner M (2013). Trends in age-specific coronary heart disease mortality in the European Union over three decades: 1980-2009. Eur Heart J. [Epub ahead of print].
8. Becker RC, Corrao JM (1990). Cardiovascular disease in women: scope of the problem. Cardiology, 77 Suppl 2: 6-7.
9. Tunstall-Pedoe H, Kuulasmaa K, Amouyel P, Arveiler D, Rajakangas AM, et al. (1994). Myocardial infarction and coronary deaths in the World Health Organization MONICA Project. Registration procedures, event rates, and case-fatality rates in 38 populations from 21 countries in four continents. Circulation, 90: 583-612.
10. Wenger NK, Speroff L, Packard B (1993). Cardiovascular health and disease in women. N Engl J Med, 329: 247-256.
11. Golden SH, Maguire A, Ding J, Crouse JR, Cauley JA, et al. (2002). Endogenous postmenopausal hormones and carotid atherosclerosis: a case-control study of the atherosclerosis risk in communities cohort. Am J Epidemiol, 155: 437-445.
12. Mosca L, Edelman D, Mochari H, Christian AH, Paultre F, et al. (2006). Waist circumference predicts cardiometabolic and global Framingham risk among women screened during National Woman's Heart Day. J Womens Health (Larchmt), 15: 24-34.
13. Gholizadeh L, Davidson P (2008). More similarities than differences: an international comparison of CVD mortality and risk factors in women. Health Care Women Int, 29: 3-22.
14. Gordon T, Kannel WB, Hjortland MC, McNamara PM (1978). Menopause and coronary heart disease. The Framingham Study. Ann Intern Med, 89: 157-161.
15. Kannel WB, Hjortland MC, McNamara PM, Gordon T (1976). Menopause and risk of cardiovascular disease: the Framingham study. Ann Intern Med, 85: 447-452.
16. Utian WH (1989). Biosynthesis and physiologic effects of estrogen and pathophysiologic effects of estrogen deficiency: a review. Am J Obstet Gynecol, 161: 1828-1831.
17. La Vecchia C, Decarli A, Franceschi S, Gentile A, Negri E, et al. (1987). Menstrual and reproductive factors and the risk of myocardial infarction in women under fifty-five years of age. Am J Obstet Gynecol, 157: 1108-1112.
18. Van der Graaf Y, De Kleijn MJ, Van der Schouw YT (1997). Menopause and cardiovascular disease. J Psychosom Obstet Gynaecol, 18: 113-120.
19. Jacobsen BK, Knutsen SF, Fraser GE (1999). Age at natural menopause and total mortality and mortality from ischemic heart disease: the Adventist Health Study. J Clin Epidemiol, 52: 303-307.
20. Mondul AM, Rodriguez C, Jacobs EJ, Calle EE (2005). Age at natural menopause and cause-specific mortality. Am J Epidemiol, 162: 1089-1097.
21. Rivera CM, Grossardt BR, Rhodes DJ, Brown RD Jr, Roger VL, et al. (2009). Increased cardiovascular mortality after early bilateral oophorectomy. Menopause, 16: 15-23.
22. Van der Schouw YT, Van der Graaf Y, Steyerberg EW, Eijkemans JC, Banga JD(1996). Age at menopause as a risk factor for cardiovascular mortality. Lancet, 347: 714-718.
23. Atsma F, Bartelink M-LEL, Grobbee DE, Van der Schouw YT (2006). Postmenopausal status and early menopause as independent risk factors for cardiovascular disease: a meta-analysis. Menopause, 13: 265-279.
24. Lobo RA (2007). Surgical menopause and cardiovascular risks. Menopause, 14: 562-566.
25. Tezini GCSV, Dias DPM, Souza HCD (2013). Aerobic physical training has little effect on cardiovascular autonomic control in aging rats subjected to early menopause. Exp Gerontol, 48: 147-153.
26. Miller VM, Duckles SP (2008). Vascular actions of estrogens: functional implications. Pharmacol Rev, 60: 210-241.
27. Kleiger RE, Miller JP, Bigger JT Jr, Moss AJ (1987). Decreased heart rate variability and its association with increased mortality after acute myocardial infarction. Am J Cardiol, 59: 256-262.
28. Malliani A, Pagani M, Lombardi F, Cerutti S (1991). Cardiovascular neural regulation explored in the frequency domain. Circulation, 84: 482-492.
29. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996). Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation, 93: 1043-1065.
30. La Rovere MT, Pinna GD, Hohnloser SH, Marcus FI, Mortara A, et al. (2001). Baroreflex sensitivity and heart rate variability in the identification of patients at risk for life-threatening arrhythmias: implications for clinical trials. Circulation, 103: 2072-2077.
31. Tezini GCSV, Silveira LCR, Villa-Clé PG Jr, Jacinto CP, Di Sacco THR, et al. (2009). The effect of aerobic physical training on cardiac autonomic control of rats submitted to ovariectomy. Menopause, 16: 110-116.
32. Huikuri HV, Pikkujämsä SM, Airaksinen KE, Ikäheimo MJ, Rantala AO, et al. (1996). Sex-related differences in autonomic modulation of heart rate in middle-aged subjects. Circulation, 94: 122-125.
33. Saleh TM, Connell BJ (1999). Centrally mediated effect of 17beta-estradiol on parasympathetic tone in male rats. Am J Physiol, 276: R474-481.
34. Saleh MC, Connell BJ, Saleh TM (2000). Autonomic and cardiovascular reflex responses to central estrogen injection in ovariectomized female rats. Brain Res, 879: 105-114.
35. Dart AM, Du X-J, Kingwell BA (2002). Gender, sex hormones and autonomic nervous control of the cardiovascular system. Cardiovasc Res, 53: 678-687.
36. Lipsitz LA, Connelly CM, Kelley-Gagnon M, Kiely DK, Morin RJ (1995). Effects of chronic estrogen replacement therapy on beat-to-beat blood pressure dynamics in healthy postmenopausal women. Hypertension, 26: 711-715.
37. Davy KP, DeSouza CA, Jones PP, Seals DR (1998). Elevated heart rate variability in physically active young and older adult women. Clin Sci, 94: 579-584.
38. Ribeiro TF, Azevedo GD, Crescêncio JC, Marães VR, Papa V, et al. (2001). Heart rate variability under resting conditions in postmenopausal and young women. Braz J Med Biol Res, 34: 871-877.
39. Neves VFC, Silva de Sá MF, Gallo L Jr, Catai AM, Martins LEB, et al (2007). Autonomic modulation of heart rate of young and postmenopausal women undergoing estrogen therapy. Braz J Med Biol Res, 40: 491-499.
40. Vongpatanasin W (2009). Autonomic regulation of blood pressure in menopause. Semin Reprod Med, 27: 338-345.
41. Lee JO, Kang SG, Kim SH, Park SJ, Song SW (2011). The Relationship between Menopausal Symptoms and Heart Rate Variability in Middle Aged Women. Korean J Fam Med, 32: 299-305.
42. Thawornkaiwong A, Preawnim S, Wattanapermpool J (2003). Upregulation of beta 1-adrenergic receptors in ovariectomized rat hearts. Life Sci, 72: 1813-1824.
43. Kam KWL, Qi JS, Chen M, Wong TM (2004). Estrogen reduces cardiac injury and expression of beta1-adrenoceptor upon ischemic insult in the rat heart. J Pharmacol Exp Ther, 309: 8-15.
44. Sherwood A, Park SB, Hughes JW, Blumenthal JA, Hinderliter A, et al. (2010). Cardiovascular hemodynamics during stress in premenopausal versus postmenopausal women. Menopause, 17: 403-409.
45. Bush TL, Barrett-Connor E, Cowan LD, Criqui MH, Wallace RB, et al. (1987). Cardiovascular mortality and noncontraceptive use of estrogen in women: results from the Lipid Research Clinics Program Follow-up Study. Circulation, 75: 1102-1109.
46. The Writing Group for the PEPI Trial (1995). Effects of estrogen or estrogen/progestin regimens on heart disease risk factors in postmenopausal women. The Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial. JAMA, 273: 199-208.
47. Grodstein F, Stampfer MJ, Colditz GA, Willett WC, Manson JE, et al. (1997). Postmenopausal hormone therapy and mortality. N Engl J Med, 336: 1769-1775.
48. Harman SM, Brinton EA, Cedars M, Lobo R, Manson JE, et al. (2005). KEEPS: The Kronos Early Estrogen Prevention Study. Climacteric, 8: 3-12.
49. Liu CC, Kuo TBJ, Yang CCH (2003). Effects of estrogen on gender-related autonomic differences in humans. Am J Physiol Heart Circ Physiol, 285: H2188-2193.
50. El-Mas MM, Abdel-Rahman AA (2009). Longitudinal assessment of the effects of oestrogen on blood pressure and cardiovascular autonomic activity in female rats. Clin Exp Pharmacol Physiol, 36: 1002-1009.
51. Christ M, Seyffart K, Tillmann H-C, Wehling M (2002). Hormone replacement in postmenopausal women: impact of progestogens on autonomic tone and blood pressure regulation. Menopause, 9: 127-136.
52. Dias DPM, Oliveira M, Salgado HC, Fazan R Jr (2010). Ovariectomy does not affect the cardiac sympathovagal balance of female SHR but estradiol does. Braz J Med Biol Res, 43: 969-975.
53. Hulley S, Grady D, Bush T, Furberg C, Herrington D, et al. (1998). Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. JAMA, 280: 605-613.
54. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, et al. (2002). Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA, 288: 321-333.
55. Windler E, Zyriax B-C, Eidenmüller B, Boeing H (2007). Hormone replacement therapy and risk for coronary heart disease. Data from the CORA-study--a case-control study on women with incident coronary heart disease. Maturitas, 57: 239-246.
56. Morelli V, Naquin C (2002). Alternative therapies for traditional disease states: menopause. Am Fam Physician, 66: 129-134.
57. Paschoal MA, Polessi EA, Simioni FC (2008). Evaluation of heart rate variability in trained and sedentary climacteric women. Arq Bras Cardiol, 90: 74-79.
58. Heeren MV, De Sousa LE, Mostarda C, Moreira E, Machert H, et al. (2009). Exercise improves cardiovascular control in a model of dislipidemia and menopause. Maturitas, 62: 200-204.
59. Higashi Y, Yoshizumi M (2004). Exercise and endothelial function: role of endothelium-derived nitric oxide and oxidative stress in healthy subjects and hypertensive patients. Pharmacol Ther, 102: 87-96.
60. Daley AJ, Stokes-Lampard HJ, Macarthur C (2009). Exercise to reduce vasomotor and other menopausal symptoms: a review. Maturitas, 63: 176-180.
61. Nualnim N, Parkhurst K, Dhindsa M, Tarumi T, Vavrek J, et al. (2012). Effects of swimming training on blood pressure and vascular function in adults >50 years of age. Am J Cardiol, 109: 1005-1010.
62. Arakawa K (1993). Hypertension and exercise. Clin Exp Hypertens, 15: 1171-1179.
63. Kelley G, McClellan P (1994). Antihypertensive effects of aerobic exercise. A brief meta-analytic review of randomized controlled trials. Am J Hypertens, 7: 115-119.
64. Billman GE, Kukielka M (2006). Effects of endurance exercise training on heart rate variability and susceptibility to sudden cardiac death: protection is not due to enhanced cardiac vagal regulation. J Appl Physiol, 100: 896-906.
65. Silveira LCR, Tezini GCSV, Schujmann DS, Porto JM, Rossi BRO, et al. (2011). Comparison of the effects of aerobic and resistance training on cardiac autonomic adaptations in ovariectomized rats. Auton Neurosci, 162: 35-41.
66. Brum PC, Da Silva GJ, Moreira ED, Ida F, Negrão CE, et al. (2000). Exercise training increases baroreceptor gain sensitivity in normal and hypertensive rats. Hypertension, 36: 1018-1022.
67. De Angelis K, Wichi RB, Jesus WRA, Moreira ED, Morris M, et al. (2004). Exercise training changes autonomic cardiovascular balance in mice. J Appl Physiol, 96: 2174-2178.
68. Irigoyen M-C, Paulini J, Flores LJF, Flues K, Bertagnolli M, et al. (2005). Exercise training improves baroreflex sensitivity associated with oxidative stress reduction in ovariectomized rats. Hypertension, 46: 998-1003.
69. Sant'Ana JE, Pereira MGAG, Dias da Silva VJ, Dambrós C, Costa-Neto CM, et al. (2011). Effect of the duration of daily aerobic physical training on cardiac autonomic adaptations. Auton Neurosci, 159: 32-37.
70. La Rovere MT, Bersano C, Gnemmi M, Specchia G, Schwartz PJ (2002). Exercise-induced increase in baroreflex sensitivity predicts improved prognosis after myocardial infarction. Circulation, 106: 945-949.
71. Martinez DG, Nicolau JC, Lage RL, Toschi-Dias E, Matos LDNJ de, et al. (2011). Effects of Long-Term Exercise Training on Autonomic Control in Myocardial Infarction Patients. Hypertension, 58: 1049-1056.
72. Takeda N, Dominiak P, Türck D, Rupp H, Jacob R (1985). The influence of endurance training on mechanical catecholamine responsiveness, beta-adrenoceptor density and myosin isoenzyme pattern of rat ventricular myocardium. Basic Res Cardiol, 80: 88-99.
73. Hammond HK, Ransnas LA, Insel PA (1988). Noncoordinate regulation of cardiac Gs protein and beta-adrenergic receptors by a physiological stimulus, chronic dynamic exercise. J Clin Invest, 82: 2168-2171.
74. Spina RJ, Ogawa T, Coggan AR, Holloszy JO, Ehsani AA (1992). Exercise training improves left ventricular contractile response to beta-adrenergic agonist. J Appl Physiol, 72: 307-311.
75. Spina RJ, Turner MJ, Ehsani AA (1998). Beta-adrenergic-mediated improvement in left ventricular function by exercise training in older men. Am J Physiol, 274: H397-404.
76. MacDonnell SM, Kubo H, Crabbe DL, Renna BF, Reger PO, et al. (2005). Improved myocardial beta-adrenergic responsiveness and signaling with exercise training in hypertension. Circulation, 111: 3420-3428.
77. Moore RL, Riedy M, Gollnick PD (1982). Effect of training on beta-adrenergic receptor number in rat heart. J Appl Physiol, 52: 1133-1137.
78. Werle EO, Strobel G, Weicker H (1990). Decrease in rat cardiac beta 1- and beta 2-adrenoceptors by training and endurance exercise. Life Sci, 46: 9-17.
79. Barbier J, Rannou-Bekono F, Marchais J, Berthon P-M, Delamarche P, et al. (2004). Effect of training on beta1 beta2 beta3 adrenergic and M2 muscarinic receptors in rat heart. Med Sci Sports Exerc, 36: 949-954.
80. Barbier J, Reland S, Ville N, Rannou-Bekono F, Wong S, et al. (2006). The effects of exercise training on myocardial adrenergic and muscarinic receptors. Clin Auton Res, 16: 61-65.
81. Levy WC, Cerqueira MD, Harp GD, Johannessen KA, Abrass IB, et al. (1998). Effect of endurance exercise training on heart rate variability at rest in healthy young and older men. Am J Cardiol, 82: 1236-1241.
82. Schuit AJ, Van Amelsvoort LG, Verheij TC, Rijneke RD, Maan AC, et al. (1999). Exercise training and heart rate variability in older people. Med Sci Sports Exerc, 31: 816-821.
83. Jurca R, Church TS, Morss GM, Jordan AN, Earnest CP (2004). Eight weeks of moderate-intensity exercise training increases heart rate variability in sedentary postmenopausal women. Am Heart J, 147: e21.
84. Asikainen T-M, Kukkonen-Harjula K, Miilunpalo S (2004). Exercise for health for early postmenopausal women: a systematic review of randomised controlled trials. Sports Med, 34: 753-778.
85. Simpson DM, Wicks R (1988). Spectral analysis of heart rate indicates reduced baroreceptor-related heart rate variability in elderly persons. J Gerontol, 43: M21-24.
86. Lipsitz LA, Mietus J, Moody GB, Goldberger AL (1990). Spectral characteristics of heart rate variability before and during postural tilt. Relations to aging and risk of syncope. Circulation, 81: 1803-1810.
87. Ferrari AU, Daffonchio A, Albergati F, Mancia G (1991). Differential effects of aging on the heart rate and blood pressure influences of arterial baroreceptors in awake rats. J Hypertens, 9: 615-621.
88. Veerman DP, Imholz BP, Wieling W, Karemaker JM, Van Montfrans GA (1994). Effects of aging on blood pressure variability in resting conditions. Hypertension, 24: 120-130.
89. Parati G, Frattola A, Di Rienzo M, Castiglioni P, Pedotti A, et al. (1995). Effects of aging on 24-h dynamic baroreceptor control of heart rate in ambulant subjects. Am J Physiol, 268: H1606-1612.
90. Lavi S, Nevo O, Thaler I, Rosenfeld R, Dayan L, et al. (2007). Effect of aging on the cardiovascular regulatory systems in healthy women. Am J Physiol Regul Integr Comp Physiol, 292: R788-793.
91. Tanaka H, Dinenno FA, Monahan KD, Clevenger CM, DeSouza CA, et al. (2000). Aging, habitual exercise, and dynamic arterial compliance. Circulation, 102: 1270-1275.
92. Sugawara J, Inoue H, Hayashi K, Yokoi T, Kono I (2004). Effect of low-intensity aerobic exercise training on arterial compliance in postmenopausal women. Hypertens Res, 27: 897-901.
93. Hart EC, Charkoudian N, Wallin BG, Curry TB, Eisenach J, et al. (2011). Sex and ageing differences in resting arterial pressure regulation: the role of the β-adrenergic receptors. J Physiol (Lond), 589: 5285-5297.
94. Hernández I, Delgado JL, Díaz J, Quesada T, Teruel MJ, et al. (2000). 17beta-estradiol prevents oxidative stress and decreases blood pressure in ovariectomized rats. Am J Physiol Regul Integr Comp Physiol, 279: R1599-1605.
95. Chappell MC, Gallagher PE, Averill DB, Ferrario CM, Brosnihan KB (2003). Estrogen or the AT1 antagonist olmesartan reverses the development of profound hypertension in the congenic mRen2. Lewis rat. Hypertension, 42: 781-786.
96. Flues K, Paulini J, Brito S, Sanches IC, Consolim-Colombo F, et al. (2010). Exercise training associated with estrogen therapy induced cardiovascular benefits after ovarian hormones deprivation. Maturitas, 65: 267-271.
97. Taddei S, Virdis A, Ghiadoni L, Mattei P, Sudano I, et al. (1996). Menopause is associated with endothelial dysfunction in women. Hypertension, 28: 576-582.
98. Schunkert H, Danser AH, Hense HW, Derkx FH, Kürzinger S, et al. (1997). Effects of estrogen replacement therapy on the renin-angiotensin system in postmenopausal women. Circulation, 95: 39-45.
99. Matsukawa T, Sugiyama Y, Watanabe T, Kobayashi F, Mano T (1998). Gender difference in age-related changes in muscle sympathetic nerve activity in healthy subjects. Am J Physiol, 275: R1600-1604.
100. Tostes RC, Nigro D, Fortes ZB, Carvalho MHC (2003). Effects of estrogen on the vascular system. Braz J Med Biol Res, 36: 1143-1158.
101. Sartori-Valinotti JC, Iliescu R, Fortepiani LA, Yanes LL, Reckelhoff JF (2007). Sex differences in oxidative stress and the impact on blood pressure control and cardiovascular disease. Clin Exp Pharmacol Physiol, 34: 938-945.
102. Yanes LL, Reckelhoff JF (2011). Postmenopausal hypertension. Am J Hypertens, 24: 740-749.
103. Véras-Silva AS, Mattos KC, Gava NS, Brum PC, Negrão CE, et al. (1997). Low-intensity exercise training decreases cardiac output and hypertension in spontaneously hypertensive rats. Am J Physiol, 273: H2627-2631.
104. Cornelissen VA, Fagard RH (2005). Effects of endurance training on blood pressure, blood pressure-regulating mechanisms, and cardiovascular risk factors. Hypertension, 46: 667-675.
105. Sugawara J, Komine H, Hayashi K, Yoshizawa M, Otsuki T, et al. (2007). Systemic alpha-adrenergic and nitric oxide inhibition on basal limb blood flow: effects of endurance training in middle-aged and older adults. Am J Physiol Heart Circ Physiol, 293: H1466-1472.
106. MacMahon S, Peto R, Cutler J, Collins R, Sorlie P, et al. (1990). Blood pressure, stroke, and coronary heart disease. Part 1, Prolonged differences in blood pressure: prospective observational studies corrected for the regression dilution bias. Lancet, 335: 765-774.
107. Wieling W, Van Brederode JF, De Rijk LG, Borst C, Dunning AJ (1982). Reflex control of heart rate in normal subjects in relation to age: a data base for cardiac vagal neuropathy. Diabetologia, 22: 163-166.
108. Akselrod S, Gordon D, Ubel FA, Shannon DC, Berger AC, et al. (1981). Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science, 213: 220-222.
109. Pomeranz B, Macaulay RJ, Caudill MA, Kutz I, Adam D, et al. (1985). Assessment of autonomic function in humans by heart rate spectral analysis. Am J Physiol, 248: H151-153.
110. Rubin PC, Scott PJ, McLean K, Reid JL (1982). Noradrenaline release and clearance in relation to age and blood pressure in man. Eur J Clin Invest, 12: 121-125.
111. Esler MD, Turner AG, Kaye DM, Thompson JM, Kingwell BA, et al. (1995). Aging effects on human sympathetic neuronal function. Am J Physiol, 268: R278-285.
112. Iwase S, Mano T, Watanabe T, Saito M, Kobayashi F (1991). Age-related changes of sympathetic outflow to muscles in humans. J Gerontol, 46: M1-5.
113. Ng AV, Callister R, Johnson DG, Seals DR (1993). Age and gender influence muscle sympathetic nerve activity at rest in healthy humans. Hypertension, 21: 498-503.
114. Parati G, Frattola A, Di Rienzo M, Castiglioni P, Mancia G (1997). Broadband spectral analysis of blood pressure and heart rate variability in very elderly subjects. Hypertension, 30: 803-808.
115. Miao C-Y, Xie H-H, Zhan L-S, Su D-F (2006). Blood pressure variability is more important than blood pressure level in determination of end-organ damage in rats. J Hypertens, 24: 1125-1135.
116. Sollers JJ 3rd, Merritt MM, Silver RA, Evans MK, Zonderman AB, et al. (2005). Understanding blood pressure variability: spectral indices as a function of gender and age. Biomed Sci Instrum, 41: 43-47.
117. Shepherd JT (1990). Franz Volhard lecture. Increased systemic vascular resistance and primary hypertension: the expanding complexity. J Hypertens, Suppl 8: S15-27.
118. Pelletier G, Liao N, Follea N, Govindan MV (1988). Mapping of estrogen receptor-producing cells in the rat brain by in situ hybridization. Neurosci Lett, 94: 23-28.
119. Simonian SX, Herbison AE (1997). Differential expression of estrogen receptor and neuropeptide Y by brainstem A1 and A2 noradrenaline neurons. Neuroscience, 76: 517-529.
120. Saleh TM, Connell BJ (2003). Estrogen-induced autonomic effects are mediated by NMDA and GABAA receptors in the parabrachial nucleus. Brain Res, 973: 161-170.
121. Saleh TM, Connell BJ, Cribb AE (2005). Sympathoexcitatory effects of estrogen in the insular cortex are mediated by GABA. Brain Res, 1037: 114-122.
122. Hunt BE, Taylor JA, Hamner JW, Gagnon M, Lipsitz LA (2001). Estrogen replacement therapy improves baroreflex regulation of vascular sympathetic outflow in postmenopausal women. Circulation, 103: 2909-2914.
123. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, et al. (2003). Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension, 42: 1206-1252.
124. Zucker IH, Patel KP, Schultz HD, Li Y-F, Wang W, et al. (2004). Exercise training and sympathetic regulation in experimental heart failure. Exerc Sport Sci Rev, 32: 107-111.
125. Zheng H, Li Y-F, Cornish KG, Zucker IH, Patel KP (2005). Exercise training improves endogenous nitric oxide mechanisms within the paraventricular nucleus in rats with heart failure. Am J Physiol Heart Circ Physiol, 288: H2332-2341.
126. Higa-Taniguchi KT, Silva FCP, Silva HMV, Michelini LC, Stern JE (2007). Exercise training-induced remodeling of paraventricular nucleus (nor)adrenergic innervation in normotensive and hypertensive rats. Am J Physiol Regul Integr Comp Physiol, 292: R1717-1727.
127. Michelini LC, Stern JE (2009). Exercise-induced neuronal plasticity in central autonomic networks: role in cardiovascular control. Exp Physiol, 94: 947-960.
128. Martins-Pinge MC (2011). Cardiovascular and autonomic modulation by the central nervous system after aerobic exercise training. Braz J Med Biol Res, 44: 848-854.
129. Flores LJ, Figueroa D, Sanches IC, Jorge L, Irigoyen M-C, et al. (2010). Effects of exercise training on autonomic dysfunction management in an experimental model of menopause and myocardial infarction. Menopause, 17: 712-717.