Cardiac autonomic dysfunction in chronic stroke women is attenuated after submaximal exercise test, as evaluated by linear and nonlinear analysis

BMC Cardiovascular Disorders

Bruno Rodrigues⁶  Katia De Angelis³  Maria Cláudia Irigoyen⁴  Erico Chagas Caperuto²  Cristiano Mostarda¹  Oscar Albuquerque Moraes⁴  Kátia Bilhar Scapini⁴  Luís Mochizuki⁵  Aline Bigongiari²  Juliana Valente Francica² 

[1] Federal University of Maranhao (UFMA), São Luiz/MA, Brazil;Human Movement Laboratory, São Judas Tadeu University (USJT), São Paulo/SP, Brazil;Translational Physiology Laboratory, Universidade Nove de Julho (UNINOVE), São Paulo/SP, Brazil;Hypertension Unit, Heart Institute (InCor), Medical School of University of Sao Paulo, São Paulo/SP, Brazil;School of Arts, Sciences and Humanities, University of São Paulo, São Paulo/SP, Brazil;Faculty of Physical Education, University of Campinas (UNICAMP), Av. Érico Veríssimo, 701. Cidade Universitária “Zeferino Vaz”. Barão Geraldo, Campinas 13.083-851, SP. CEP, Brazil

关键词: Exercise test;    Symbolic analysis;    Spectral analysis;    Autonomic nervous system;    Stroke;   

Others  :  1227869
DOI  :  10.1186/s12872-015-0099-9

 received in 2015-03-18, accepted in 2015-09-18,  发布年份 2015

【 摘 要 】

Background

We evaluated cardiac autonomic modulation in women with chronic ischemic stroke (at least 4 years post-stroke) at rest and in response to submaximal exercise test.

Methods

Fourteen post-stroke women (S group) and 10 healthy women (C group) participated in this study. Autonomic modulation (using linear and nonlinear analysis), blood pressure and metabolic variables at rest were evaluated immediately after the exercise test and during the recovery period (20 min). All participants underwent submaximal exercise test on cycle ergometer with gas analysis.

Results

At rest, the S group displayed higher lactate concentration, systolic (SBP) and diastolic blood pressure (DBP) values when compared to C group. Furthermore, the S group had lower heart rate variability (HRV) in time domain (SDNN: S = 30 ± 5 vs. 40 ± 8 ms; rMSSD: S = 14 ± 2 vs. C = 34 ± 3 ms), decreased high frequency band of pulse interval (S = 8.4 ± 2 vs. 33.1 ± 9 %) and 2V pattern of symbolic analysis (S = 17.3 ± 1 vs. 30 ± 3 %) (both indicators of cardiac vagal modulation) when compared to C group. Immediately after exercise, S group presented higher values of lactate, SBP, DBP and double product when compared to C group, as well as decreased heart rate recovery (HRR) measured at the first, second and third minutes. At recovery time, all HRV parameters in time and frequency domains improved in the S group; however, HF band remained lower when compared to C group.

Conclusions

After the exercise test, women with chronic stroke presented reduced heart rate variability, reduced cardiac vagal modulation, as well as reduced HRR, while displayed an improvement of heart rate variability and cardiac vagal modulation when compared to their baseline. These results reinforce the importance of a physically active lifestyle for cardiovascular autonomic disorders observed in chronic stroke women.

【 授权许可】

   
2015 Francica et al.

【 图 表 】

Fig. 1.

Fig. 2.

【 参考文献 】

• [1]Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, et al.: Heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation 2014, 129:e28-e292.
• [2]Roth EJ: Heart disease in patients with stroke: incidence, impact, and implications for rehabilitation. Part 1: Classification and prevalence. Arch Phys Med Rehabil 1993, 74:752-60.
• [3]Korpelainen JT, Nieminen P, Myllylä VV: Sexual Functioning Among Stroke Patients and Their Spouses. Stroke 1999, 30:715-9.
• [4]McLaren A, Kerr S, Allan L, Steen IN, Ballard C, Allen J, et al.: Autonomic Function Is Impaired in Elderly Stroke Survivors. Stroke 2005, 36:1026-30.
• [5]Muslumanoglu L, Akyuz G, Aki S, Karsidag S, Us O: Evaluation of autonomic nervous system functions in post-stroke patients. Am J Phys Med Rehabil 2002, 81:721-5.
• [6]Colivicchi F, Bassi A, Santini M, Caltagirone C: Cardiac autonomic derangement and arrhythmias in right-sided stroke with insular involvement. Stroke 2004, 35:2094-8.
• [7]Sykora M, Diedler J, Turcani P, Hacke W, Steiner T: Baroreflex: A New Therapeutic Target in Human Stroke? Stroke 2009, 40:e678-e82.
• [8]Korpelainen JT, Sotaniemi KA, Huikuri HV, Myllylä VV: Abnormal Heart Rate Variability as a Manifestation of Autonomic Dysfunction in Hemispheric Brain Infarction. Stroke 1996, 27:2059-63.
• [9]Malik M: Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation 1996, 93:1043-65.
• [10]Watanabe J, Thamilarasan M, Blackstone EH, Thomas JD, Lauer MS: Heart Rate Recovery Immediately After Treadmill Exercise and Left Ventricular Systolic Dysfunction as Predictors of Mortality: The Case of Stress Echocardiography. Circulation 2001, 104:1911-6.
• [11]Imai K, Sato H, Hori M, Kusuoka H, Ozaki H, Yokoyama H, et al.: Vagally mediated heart rate recovery after exercise is accelerated in athletes but blunted in patients with chronic heart failure. J Am Coll Cardiol 1994, 24:1529-35.
• [12]Jouven X, Empana J-P, Schwartz PJ, Desnos M, Courbon D, Ducimetière P: Heart-Rate Profile during Exercise as a Predictor of Sudden Death. N Engl J Med 2005, 352:1951-8.
• [13]Nishime E, Cole CR, Blackstone EH, Pashkow FJ, Lauer MS: HEart rate recovery and treadmill exercise score as predictors of mortality in patients referred for exercise ecg. JAMA 2000, 284:1392-8.
• [14]Drawz PE, Babineau DC, Brecklin C, He J, Kallem RR, Soliman EZ, et al.: Heart Rate Variability Is a Predictor of Mortality in Chronic Kidney Disease: A Report from the CRIC Study. Am J Nephrol 2013, 38:517-28.
• [15]May O, Arildsen H: Long-term predictive power of heart rate variability on all-cause mortality in the diabetic population. Acta Diabetol 2011, 48:55-9.
• [16]Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, et al.: Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension 2003, 42:1206-52.
• [17]Malliani A, Pagani M, Lombardi F, Cerutti S: Cardiovascular neural regulation explored in the frequency domain. Circulation 1991, 84:482-92.
• [18]Francica JV, Heeren MV, Tubaldini M, Sartori M, Mostarda C, Araujo RC, et al.: Impairment on cardiovascular and autonomic adjustments to maximal isometric exercise tests in offspring of hypertensive parents. Eur J Prev Cardiol 2013, 20:480-5.
• [19]Porta A, Gnecchi-Ruscone T, Tobaldini E, Guzzetti S, Furlan R, Malliani A, et al.: editors. Symbolic analysis of short-term heart period variability during graded head-up tilt. Comput Cardiol 2006, 33:109-12.
• [20]Guzzetti S, Borroni E, Garbelli PE, Ceriani E, Della Bella P, Montano N, et al.: Symbolic dynamics of heart rate variability: a probe to investigate cardiac autonomic modulation. Circulation 2005, 112:465-70.
• [21]Tang A, Sibley KM, Thomas SG, McIlroy WE, Brooks D: Maximal exercise test results in subacute stroke. Arch Phys Med Rehabil 2006, 87:1100-1105.
• [22]Billinger SA, Arena R, Bernhardt J, Eng JJ, Franklin BA, Johnson CM, et al.: Physical activity and exercise recommendations for stroke survivors: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2014, 45:2532-2553.
• [23]Gadidi V, Katz-Leurer M, Carmeli E, Bornstein NM: Long-term outcome poststroke: predictors of activity limitation and participation restriction. Arch Phys Med Rehabil 2011, 92:1802-1808.
• [24]Ryan AS, Dobrovolny CL, Silver KH, Smith GV, Macko RF: Cardiovascular fitness after stroke: Role of muscle mass and gait deficit severity. J Stroke Cerebrovasc Dis 2000, 9:185-91.
• [25]Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko RF: Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil 2002, 83:1703-7.
• [26]Scherbakov N, Doehner W: Sarcopenia in stroke-facts and numbers on muscle loss accounting for disability after stroke. J Cachexia Sarcopenia Muscle 2011, 2:5-8.
• [27]Dutsch M, Burger M, Dorfler C, Schwab S, Hilz MJ: Cardiovascular autonomic function in poststroke patients. Neurology 2007, 69:2249-55.
• [28]Gobel FL, Norstrom LA, Nelson RR, Jorgensen CR, Wang Y: The rate-pressure product as an index of myocardial oxygen consumption during exercise in patients with angina pectoris. Circulation 1978, 57:549-56.
• [29]Nelson RR, Gobel FL, Jorgensen CR, Wang K, Wang Y, Taylor HL: Hemodynamic predictors of myocardial oxygen consumption during static and dynamic exercise. Circulation 1974, 50:1179-89.
• [30]Coyle EF, Martin WH 3rd, Sinacore DR, Joyner MJ, Hagberg JM, Holloszy JO: Time course of loss of adaptations after stopping prolonged intense endurance training. J Appl Physiol Respir Environ Exerc Physiol 1984, 57:1857-1864.
• [31]Hughson RL, Shoemaker JK: Autonomic responses to exercise: deconditioning/inactivity. Auton Neurosci 2015, 188:32-35.
• [32]Grassi G, Turri C, Dell’Oro R, Stella ML, Bolla GB, Mancia G: Effect of chronic angiotensin converting enzyme inhibition on sympathetic nerve traffic and baroreflex control of the circulation in essential hypertension. J Hypertens 1998, 16:1789-1796.
• [33]Grassi G, Seravalle G, Stella ML, Turri C, Zanchetti A, Mancia G: Sympathoexcitatory responses to the acute blood pressure fall induced by central or peripheral antihypertensive drugs. Am J Hypertens 2000, 13:29-34.
• [34]Grassi G, Seravalle G, Dell’Oro R, Trevano FQ, Bombelli M, Scopelliti F, Facchini A, Mancia G, Study CROSS: Comparative effects of candesartan and hydrochlorothiazide on blood pressure, insulin sensitivity, and sympathetic drive in obese hypertensive individuals: results of the CROSS study. J Hypertens 2003, 21:1761-1769.
• [35]Tsuji H, Larson MG, Venditti FJ Jr, Manders ES, Evans JC, Feldman CL, et al.: Impact of reduced heart rate variability on risk for cardiac events. The Framingham Heart Study. Circulation 1996, 94:2850-5.
• [36]La Rovere MT, Pinna GD, Hohnloser SH, Marcus FI, Mortara A, Nohara R, et al.: Baroreflex sensitivity and heart rate variability in the identification of patients at risk for life-threatening arrhythmias: implications for clinical trials. Circulation 2001, 103:2072-7.
• [37]Perkiomaki J, Ukkola O, Kiviniemi A, Tulppo M, Ylitalo A, Kesaniemi YA, et al.: Heart rate variability findings as a predictor of atrial fibrillation in middle-aged population. J Cardiovasc Electrophysiol 2014, 25:719-24.
• [38]Singh N, Mironov D, Armstrong PW, Ross AM, Langer A: Heart rate variability assessment early after acute myocardial infarction. Pathophysiological and prognostic correlates. GUSTO ECG Substudy Investigators. Global Utilization of Streptokinase and TPA for Occluded Arteries. Circulation 1996, 93:1388-95.
• [39]Coviello I, Pinnacchio G, Laurito M, Stazi A, Battipaglia I, Barone L, et al.: Prognostic role of heart rate variability in patients with ST-segment elevation acute myocardial infarction treated by primary angioplasty. Cardiology 2013, 124:63-70.
• [40]Ponikowski P, Anker SD, Chua TP, Szelemej R, Piepoli M, Adamopoulos S, et al.: Depressed heart rate variability as an independent predictor of death in chronic congestive heart failure secondary to ischemic or idiopathic dilated cardiomyopathy. Am J Cardiol 1997, 79:1645-50.
• [41]Rizzo MR, Sasso FC, Marfella R, Siniscalchi M, Paolisso P, Carbonara O, et al.: Autonomic dysfunction is associated with brief episodes of atrial fibrillation in type 2 diabetes. J Diabetes Complications 2014, 29:88-92.
• [42]Bassi A, Colivicchi F, Santini M, Caltagirone C: Cardiac autonomic dysfunction and functional outcome after ischaemic stroke. Eur J Neurol 2007, 14:917-22.
• [43]Graff B, Gasecki D, Rojek A, Boutouyrie P, Nyka W, Laurent S, et al.: Heart rate variability and functional outcome in ischemic stroke: a multiparameter approach. J Hypertens 2013, 31:1629-36.
• [44]Binici Z, Mouridsen MR, Kober L, Sajadieh A: Decreased nighttime heart rate variability is associated with increased stroke risk. Stroke 2011, 42:3196-201.
• [45]Tang YD, Dewland TA, Wencker D, Katz SD: Post-exercise heart rate recovery independently predicts mortality risk in patients with chronic heart failure. J Card Fail 2009, 15:850-5.
• [46]Cole CR, Foody JM, Blackstone EH, Lauer MS: Heart rate recovery after submaximal exercise testing as a predictor of mortality in a cardiovascularly healthy cohort. Ann Intern Med 2000, 132:552-5.
• [47]Buchheit M, Papelier Y, Laursen PB, Ahmaidi S: Noninvasive assessment of cardiac parasympathetic function: postexercise heart rate recovery or heart rate variability? Am J Physiol Heart Circ Physiol 2007, 293:H8-10.
• [48]Erciyas AH, Topalkara K, Topaktas S, Akyuz A, Dener S: Supression of cardiac parasympathetic functions in patients with right hemispheric stroke. Eur J Neurol 1999, 6:685-90.
• [49]Xiong L, Leung HW, Chen XY, Leung WH, Soo OY, Wong KS: Autonomic dysfunction in different subtypes of post-acute ischemic stroke. J Neurol Sci 2014, 337:141-6.
• [50]Liao D, Cai J, Barnes RW, Tyroler HA, Rautaharju P, Holme I, et al.: Association of cardiac autonomic function and the development of hypertension: the ARIC study. Am J Hypert 1996, 9:1147-56.
• [51]Pierpont GL, Stolpman DR, Gornick CC: Heart rate recovery post-exercise as an index of parasympathetic activity. J Auton Nerv Syst 2000, 80:169-74.
• [52]Evrengul H, Tanriverdi H, Kose S, Amasyali B, Kilic A, Celik T, et al.: The relationship between heart rate recovery and heart rate variability in coronary artery disease. Ann Noninvasive Electrocardiol 2006, 11:154-62.
• [53]Mravec B: The role of the vagus nerve in stroke. Auton Neurosci 2010, 158:8-12.
• [54]Rodrigues B, Jorge L, Mostarda CT, Rosa KT, Medeiros A, Malfitano C, et al.: Aerobic exercise training delays cardiac dysfunction and improves autonomic control of circulation in diabetic rats undergoing myocardial infarction. J Card Fail 2012, 18(9):734-44.
• [55]Souza SB, Flues K, Paulini J, Mostarda C, Rodrigues B, Souza LE, et al.: Role of exercise training in cardiovascular autonomic dysfunction and mortality in diabetic ovariectomized rats. Hypertension 2007, 50:786-91.
• [56]La Rovere MT, Mortara A, Sandrone G, Lombardi F: Autonomic nervous system adaptations to short-term exercise training. Chest 1992, 101(Suppl 5):299S-303S.
• [57]Jorge L, Rodrigues B, Rosa KT, Malfitano C, Loureiro TC, Medeiros A, et al.: Cardiac and peripheral adjustments induced by early exercise training intervention were associated with autonomic improvement in infarcted rats: role in functional capacity and mortality. Eur Heart J 2011, 32:904-12.
• [58]Jin H, Jiang Y, Wei Q, Chen L, Ma G: Effects of aerobic cycling training on cardiovascular fitness and heart rate recovery in patients with chronic stroke. NeuroRehabilitation 2013, 32:327-35.