Cardiovascular responses to high-intensity stair climbing in individuals with coronary artery disease

Sydney E Valentino, Emily C Dunford, Jonathan Dubberley, Eva M Lonn, Martin J Gibala, Stuart M Phillips, Maureen J MacDonald, Sydney E Valentino, Emily C Dunford, Jonathan Dubberley, Eva M Lonn, Martin J Gibala, Stuart M Phillips, Maureen J MacDonald

Abstract

Exercise-based cardiac rehabilitation leads to improvements in cardiovascular function in individuals with coronary artery disease. The cardiac effects of coronary artery disease (CAD) can be quantified using clinical echocardiographic measures, such as ejection fraction (EF). Measures of cardiovascular function typically only used in research settings can provide additional information and maybe more sensitive indices to assess changes after exercise-based cardiac rehabilitation. These additional measures include endothelial function (measured by flow-mediated dilation), left ventricular twist, myocardial performance index, and global longitudinal strain. To investigate the cardiovascular response to 12 week of either traditional moderate-intensity (TRAD) or stair climbing-based high-intensity interval (STAIR) exercise-based cardiac rehabilitation using both clinical and additional measures of cardiovascular function in individuals with CAD. Measurements were made at baseline (BL) and after supervised (4wk) and unsupervised (12 week) of training. This study was registered as a clinical trial at clinicaltrials.gov (NCT03235674). Participants were randomized into either TRAD (n = 9, 8M/1F) and STAIR (n = 9, 8M/1F). There was a training-associated increase in one component of left ventricular twist: Cardiac apical rotation (TRAD: BL: 5.6 ± 3.3º, 4 week: 8.0 ± 3.9º, 12 week: 6.2 ± 5.1º and STAIR: BL: 5.1 ± 3.6º, 4 week: 7.4 ± 3.9º, 12 week: 7.8 ± 2.8º, p (time) = 0.03, η2 = 0.20; main effect) and post-hoc analysis revealed a difference between BL and 4 week (p = 0.02). There were no changes in any other clinical or additional measures of cardiovascular function. The small increase in cardiac apical rotation observed after 4 weeks of training may indicate an early change in cardiac function. A larger overall training stimulus may be needed to elicit other cardiovascular function changes.

Keywords: HIIT; cardiac function; cardiac rehabilitation; flow-mediated dilation; stair climbing.

© 2022 The Authors. Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.

Figures

FIGURE 1
FIGURE 1
Speckle‐tracking echocardiography analysis of PSAX‐AP and PSAX‐MV images and the subsequent calculation required to obtain LV twist
FIGURE 2
FIGURE 2
Representative image of MPI analysis from Doppler tracings of mitral inflow and LV outflow. A = time between filling periods; B = ejection time (ET). The sum of is isovolumic contraction time (ICT) and isovolumic relaxation time (IRT) can be obtained by the subtraction of B from A. Image is not to scale for the purpose of depicting the analysis graphically
FIGURE 3
FIGURE 3
Individual values overlayed on the box and whisker format of baseline (BL), 4, and 12 week for each of the following: (a) relative flow‐mediated dilation (FMD), (b) peak left ventricular twist, (c) peak basal rotation, and (d) peak apical rotation. *Denotes p < 0.05

References

    1. Abate, E. , Hoogslag, G. E. , Antoni, M. L. , Nucifora, G. , Delgado, V. , Holman, E. R. , Schalij, M. J. , Bax, J. J. , & Marsan, N. A. (2012). Value of three‐dimensional speckle‐tracking longitudinal strain for predicting improvement of left ventricular function after acute myocardial infarction. American Journal of Cardiology, 110, 961–967. 10.1016/j.amjcard.2012.05.023
    1. Allison, M. , Baglole, J. , Martin, B. , Macinnis, M. , Gurd, B. , & Gibala, M. (2017). Brief intense stair climbing improves cardiorespiratory fitness. Medicine and Science in Sports and Exercise, 49, 298–307. 10.1249/MSS.0000000000001188
    1. Amsterdam, E. A. , Wenger, N. K. , Brindis, R. G. , Casey, D. E. , Ganiats, T. G. , Holmes, D. R. , Jaffe, A. S. , Jneid, H. , Kelly, R. F. , Kontos, M. C. , Levine, G. N. , Liebson, P. R. , Mukherjee, D. , Peterson, E. D. , Sabatine, M. S. , Smalling, R. W. , & Zieman, S. J. (2014). 2014 AHA/acc guideline for the management of patients with Non‐ST‐Elevation acute coronary syndromes: A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Journal of the American College of Cardiology, 64, e139–e228.
    1. Anderson, T. J. , Uehata, A. , Gerhard, M. D. , Meredith, I. T. , Knab, S. , Delagrange, D. , Lieberman, E. H. , Ganz, P. , Creager, M. A. , Yeung, A. C. , & Selwyn, A. P. (1995). Close relation of endothelial function in the human coronary and peripheral circulations. Journal of the American College of Cardiology, 26, 1235–1241. 10.1016/0735-1097(95)00327-4
    1. Awadalla, H. , Saleh, M. A. , Abdel Kader, M. , & Mansour, A. (2017). Left ventricular torsion assessed by two‐dimensional echocardiography speckle tracking as a predictor of left ventricular remodeling and short‐term outcome following primary percutaneous coronary intervention for acute myocardial infarction: A single‐cent. Echocardiography, 34, 1159–1169.
    1. Borg, G. A. V. , Hassmén, P. , & Lagerström, M. (1987). Perceived exertion related to heart rate and blood lactate during arm and leg exercise. European Journal of Applied Physiology and Occupational Physiology, 56, 679–685. 10.1007/BF00424810
    1. Chen, Y. C. , Tsai, J. C. , Liou, Y. M. , & Chan, P. (2017). Effectiveness of endurance exercise training in patients with coronary artery disease: A meta‐analysis of randomised controlled trials. European Journal of Cardiovascular Nursing, 16, 397–408.
    1. Cornelissen, V. A. , Onkelinx, S. , Goetschalckx, K. , Thomaes, T. , Janssens, S. , Fagard, R. , Verhamme, P. , & Vanhees, L. (2014). Exercise‐based cardiac rehabilitation improves endothelial function assessed by flow‐mediated dilation but not by pulse amplitude tonometry*. European Journal of Preventive Cardiology, 21, 39–48. 10.1177/2047487312460516
    1. Currie, K. D. , Dubberley, J. B. , McKelvie, R. S. , & Macdonald, M. J. (2013). Low‐volume, high‐intensity interval training in patients with CAD. Medicine and Science in Sports and Exercise, 45, 1436–1442. 10.1249/MSS.0b013e31828bbbd4
    1. Daly, J. , Sindone, A. P. , Hons, B. , Thompson, D. R. , Hancock, K. , Chang, E. , & Davidson, P. (2002). Barriers to participation in and adherence to cardiac rehabilitation programs: A critical literature review. Progress in Cardiovascular Nursing, 17, 8–17.
    1. Dong, S.‐J. , Hees, P. S. , Huang, W. , Buffer, S. A. , Weiss, J. L. , Shapiro, E. P. , James, L. , & Shapiro, E. P. (1999). Independent effects of preload, afterload, and contractility on left ventricular torsion. American Journal of Physiology‐Heart and Circulatory Physiology, 277, 1053–1060. 10.1152/ajpheart.1999.277.3.H1053
    1. Dunford, E. C. , Valentino, S. E. , Dubberley, J. , Oikawa, S. Y. , McGlory, C. , Lonn, E. , Jung, M. E. , Gibala, M. J. , Phillips, S. M. , & MacDonald, M. J. (2021). Brief vigorous stair climbing effectively improves cardiorespiratory fitness in patients with coronary artery disease: A randomized trial. Frontiers in Sports and Active Living, 3, 1–12.
    1. Ehsani, A. A. , Hagberg, J. M. , & Hickson, R. C. (1978). Rapid changes in left ventricular dimensions and mass in response to physical conditioning and deconditioning. American Journal of Cardiology, 42, 52–56. 10.1016/0002-9149(78)90984-0
    1. Eržen, B. , Šabovič, M. , Šebeštjen, M. , & Poredoš, P. (2007). Endothelial dysfunction, intima‐media thickness, ankle‐brachial pressure index, and pulse pressure in young post‐myocardial infarction patients with various expressions of classical risk factors. Heart and Vessels, 22, 215–222. 10.1007/s00380-006-0958-5
    1. Faul, F. , Erdfelder, E. , Lang, A.‐G. , & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39, 175–191.
    1. Fletcher, G. F. , Ades, P. A. , Kligfield, P. , Arena, R. , Balady, G. J. , Bittner, V. A. , Coke, L. A. , Fleg, J. L. , Forman, D. E. , Gerber, T. C. , Gulati, M. , Madan, K. , Rhodes, J. , Thompson, P. D. , & Williams, M. A. (2013). Exercise standards for testing and training: A scientific statement from the American Heart Association. Circulation, 128, 873–934.
    1. Fraker, T. D. , & Fihn, S. D. (2007). Chronic Angina focused update of the ACC/AHA 2002 guidelines for the management of patients with chronic stable Angina. A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines Writing Group to Devel. Journal of the American College of Cardiology, 50, 2264–2274.
    1. Ghisi, G. L. D. M. , Chaves, G. S. D. S. , Bennett, A. , Lavie, C. J. , & Grace, S. L. (2019). The effects of cardiac rehabilitation on mortality and morbidity in women: A meta‐analysis attempt. Journal of Cardiopulmonary Rehabilitation and Prevention, 39, 39–42.
    1. Giannuzzi, P. , Temporelli, P. L. , Corrà, U. , & Tavazzi, L. (2003). Antiremodeling effect of long‐term exercise training in patients with stable chronic heart failure: Results of the exercise in left ventricular dysfunction and chronic heart failure (ELVD‐CHF) trial. Circulation, 108, 554–559.
    1. Giannuzzi, P. , Temporelli, P. L. , Marchioli, R. , Maggioni, P. M. , Balestroni, G. , Ceci, V. , Chieffo, C. , Gattone, M. , Griffo, R. , Schwieger, C. , Tavazzi, L. , Urbinati, S. , Valagusa, F. , & Vanuzzo, D. (2008). Global secondary prevention strategies to limit event recurrence after myocardial infarction (GOSPEL). Archives of Internal Medicine, 168, 2195–2204.
    1. Godkin, F. E. , Jenkins, E. M. , Little, J. P. , Nazarali, Z. , Percival, M. E. , & Gibala, M. J. (2018). The effect of brief intermittent stair climbing on glycemic control in people with type 2 diabetes: A pilot study. Applied Physiology, Nutrition and Metabolism, 43, 969–972.
    1. Green, D. J. , Jones, H. , Thijssen, D. , Cable, N. T. , & Atkinson, G. (2011). Flow‐mediated dilation and cardiovascular event prediction: Does nitric oxide matter? Hypertension, 57, 363–369. 10.1161/HYPERTENSIONAHA.110.167015
    1. Haykowsky, M. J. , Liang, Y. , Pechter, D. , Jones, L. W. , McAlister, F. A. , & Clark, A. M. (2007). A meta‐analysis of the effect of exercise training on left ventricular remodeling in heart failure patients. Journal of the American College of Cardiology, 49, 2329–2336. 10.1016/j.jacc.2007.02.055
    1. Huang, Y. C. , Tsai, H. H. , Fu, T. C. , Hsu, C. C. , & Wang, J. S. (2019). High‐intensity interval training improves left ventricular contractile function. Medicine and Science in Sports and Exercise, 51, 1420–1428. 10.1249/MSS.0000000000001931
    1. Karapolat, H. , Demir, E. , Bozkaya, Y. T. , Eyigor, S. , Nalbantgil, S. , Durmaz, B. , & Zoghi, M. (2009). Comparison of hospital‐based versus home‐based exercise training in patients with heart failure: Effects on functional capacity, quality of life, psychological symptoms, and hemodynamic parameters. Clinical Research in Cardiology, 98, 635–642.
    1. Kim, H. K. , Sohn, D. W. , Lee, S. E. , Choi, S. Y. , Park, J. S. , Kim, Y. J. , Oh, B. H. , Park, Y. B. , & Choi, Y. S. (2007). Assessment of left ventricular rotation and torsion with two‐dimensional speckle tracking echocardiography. Journal of the American Society of Echocardiography, 20, 45–53. 10.1016/j.echo.2006.07.007
    1. Kocabay, G. , Muraru, D. , Peluso, D. , Cucchini, U. , Mihaila, S. , Padayattil‐Jose, S. , Gentian, D. , Iliceto, S. , Vinereanu, D. , & Badano, L. P. (2014). Normal left ventricular mechanics by two‐dimensional speckle‐tracking echocardiography. Reference values in healthy adults. Revista Española De Cardiología (English Edition), 67, 651–658. 10.1016/j.rec.2013.12.009
    1. Kou, S. , Suzuki, K. , Akashi, Y. J. , Mizukoshi, K. , Takai, M. , Izumo, M. , Shimozato, T. , Hayashi, A. , Ohtaki, E. , Osada, N. , Omiya, K. , Nobuoka, S. , & Miyake, F. (2011). Global longitudinal strain by two‐dimensional speckle tracking imaging predicts exercise capacity in patients with chronic heart failure. J Echocardiogr, 9, 64–72. 10.1007/s12574-010-0076-3
    1. Lakens, D. (2013). Calculating and reporting effect sizes to facilitate cumulative science: A practical primer for t‐tests and ANOVAs. Frontiers in Psychology, 4, 1–12.
    1. Lang, R. M. , Badano, L. P. , Mor‐Avi, V. , Afilalo, J. , Armstrong, A. , Ernande, L. , Flachskampf, F. A. , Foster, E. , Goldstein, S. A. , Kuznetsova, T. , Lancellotti, P. , Muraru, D. , Picard, M. H. , Rietzschel, E. R. , Rudski, L. , Spencer, K. T. , Tsang, W. , & Voigt, J. U. (2015). Recommendations for cardiac chamber quantification by echocardiography in adults: An update from the American society of echocardiography and the European association of cardiovascular imaging. European Heart Journal of Cardiovascular Imaging, 16, 233–271.
    1. Lavie, C. J. , & Bennett, A. (2017). Enhancing cardiac rehabilitation in women. Journal of Women's Health, 26, 817–819. 10.1089/jwh.2017.6476
    1. Little, R. J. A. (1988). A test of missing completely at random for multivariate data with missing values. Journal of American Statistical Association, 83, 1198–1202. 10.1080/01621459.1988.10478722
    1. Martin, B. J. , Arena, R. , Haykowsky, M. , Hauer, T. , Austford, L. D. , Knudtson, M. , Aggarwal, S. , & Stone, J. A. (2013). Cardiovascular fitness and mortality after contemporary cardiac rehabilitation. Mayo Clinic Proceedings, 88, 455–463. 10.1016/j.mayocp.2013.02.013
    1. Marzolini, S. , Oh, P. I. , & Brooks, D. (2012). Effect of combined aerobic and resistance training versus aerobic training alone in individuals with coronary artery disease: A meta‐analysis. European Journal of Preventive Cardiology, 19, 81–94.
    1. Maufrais, C. , Schuster, I. , Doucende, G. , Vitiello, D. , Rupp, T. , Dauzat, M. , Obert, P. , & Nottin, S. (2014). Endurance training minimizes age‐related changes of left ventricular twist‐untwist mechanics. Journal of the American Society of Echocardiography, 27, 1208–1215. 10.1016/j.echo.2014.07.007
    1. McGregor, G. , Stöhr, E. J. , Oxborough, D. , Kimani, P. , & Shave, R. (2018). Effect of exercise training on left ventricular mechanics after acute myocardial infarction‐an exploratory study. Annals of Physical and Rehabilitation Medicine, 61, 119–124. 10.1016/j.rehab.2018.01.003
    1. McKay, R. , Pfeffer, M. , Pasternak, R. , Markis, J. , Come, P. , Nakao, S. , Alderman, J. , Ferguson, J. , Safian, R. , & Grossman, W. (1986). Left ventricular remodeling after myocardial infarction: A corollary to infarct expansion. Circulation, 74, 693–702.
    1. Moholdt, T. T. , Amundsen, B. H. , Rustad, L. A. , Wahba, A. , Løvø, K. T. , Gullikstad, L. R. , Bye, A. , Skogvoll, E. , Wisløff, U. , & Slørdahl, S. A. (2009). Aerobic interval training versus continuous moderate exercise after coronary artery bypass surgery: A randomized study of cardiovascular effects and quality of life. American Heart Journal, 158, 1031–1037.
    1. O’Driscoll, J. , Wright, S. , Taylor, K. , Coleman, D. , Sharma, R. , & Wiles, J. (2018). Cardiac autonomic and left ventricular mechanics following high intensity interval training: A randomised cross‐over controlled study. Journal of Applied Physiology, 125, 1030–1040.
    1. Omar, M. S. , Vallabhajosyula, S. , & Sengupta, P. P. (2015). Left ventricular twist and torsion: Research observation and clincial applications. Circulation: Cardiovascular Imaging, 8, 74–82.
    1. Pastore, M. C. , Mandoli, G. E. , Contorni, F. , Cavigli, L. , Focardi, M. , D'Ascenzi, F. , Patti, G. , Mondillo, S. , & Cameli, M. (2021). Speckle tracking echocardiography: Early predictor of diagnosis and prognosis in coronary artery disease. BioMed Research International, 2021, 1–11. 10.1155/2021/6685378
    1. Peller, M. , Balsam, P. , Główczynska, R. , Ossolinski, K. , Gilarowska, A. , Kołtowski, Ł. , Grabowski, M. , Filipiak, K. J. , & Opolski, G. (2016). The impact of physical training on endothelial function in myocardial infarction survivors: Pilot study. Kardiologia Polska, 74, 439–446.
    1. Pfeffer, M. A. , & Braunwald, E. (1990). Ventricular remodeling after myocardial infarction additional: Observations and clinical implications. Circulation, 81, 1161–1172.
    1. Pyke, K. E. , Hartnett, J. A. , & Tschakovsky, M. E. (2008). Are the dynamic response characteristics of brachial artery flow‐mediated dilation sensitive to the magnitude of increase in shear stimulus? Journal of Applied Physiology, 105, 282–292. 10.1152/japplphysiol.01190.2007
    1. Qin, Y. , Bundham, P. K. , Yuan, Z. L. , & Chen, M. H. (2021). The effect of high‐intensity interval training on exercise capacity in post‐myocardial infarction patients: A systematic review and meta‐analysis. European Journal of Preventive Cardiology, 00, 1–10.
    1. Ramos, J. S. , Dalleck, L. C. , Tjonna, A. E. , Beetham, K. S. , & Coombes, J. S. (2015). The impact of high‐intensity interval training versus moderate‐intensity continuous training on vascular function: A systematic review and meta‐analysis. Sports Medicine, 45, 679–692.
    1. Seals, D. R. , Nagy, E. E. , & Moreau, K. L. (2019). Aerobic exercise training and vascular function with ageing in healthy men and women. Journal of Physiology, 597, 4901–4914. 10.1113/JP277764
    1. Sengupta, P. P. , Tajik, A. J. , Chandrasekaran, K. , & Khandheria, B. K. (2008). Twist mechanics of the left ventricle: Principles and application. JACC: Cardiovascular Imaging, 1, 366–376.
    1. Shenouda, N. , Priest, S. E. , Rizzuto, V. I. , & MacDonald, M. J. (2018). Brachial artery endothelial function is stable across a menstrual and oral contraceptive pill cycle but lower in premenopausal women than in age‐matched men. American Journal of Physiology‐Heart and Circulatory Physiology, 315, H366–H374. 10.1152/ajpheart.00102.2018
    1. Smith, S. C. , Benjamin, E. J. , Bonow, R. O. , Braun, L. T. , Creager, M. A. , Franklin, B. A. , Gibbons, R. J. , Grundy, S. M. , Hiratzka, L. F. , Jones, D. W. , Lloyd‐Jones, D. M. , Minissian, M. , Mosca, L. , Peterson, E. D. , Sacco, R. L. , Spertus, J. , Stein, J. H. , & Taubert, K. A. (2011). AHA/ACCF secondary prevention and risk reduction therapy for patients with coronary and other atherosclerotic vascular disease: 2011 update. Journal of the American College of Cardiology, 58, 2432–2446.
    1. Stöhr, E. J. , Shave, R. E. , Baggish, A. L. , & Weiner, R. (2016). Left ventricular twist mechanics in the context of normal physiology and cardiovascular disease: a review of studies using speckle tracking echocardiography. American Journal of Physiology‐Heart and Circulatory Physiology, 311, 633–644.
    1. Suwaidi, J. A. , Hamasaki, S. , Higano, S. T. , Nishimura, R. A. , Holmes, D. R. , & Lerman, A. (2000). Long‐term follow‐up of patients with mild coronary artery disease and endothelial dysfunction. Circulation, 101, 948–954. 10.1161/01.CIR.101.9.948
    1. Takase, B. , Uehata, A. , Akima, T. , Nagai, T. , Nishioka, T. , Hamabe, A. , Satomura, K. , Ohsuzu, F. , & Kurita, A. (1998). Endothelium‐dependent flow‐mediated vasodilation in coronary and brachial arteries in suspected coronary artery disease. American Journal of Cardiology, 82, 1535–1539. 10.1016/S0002-9149(98)00702-4
    1. Tanaka, S. , Sanuki, Y. , Ozumi, K. , Harada, T. , & Tasaki, H. (2018). Heart failure with preserved vs reduced ejection fraction following cardiac rehabilitation: Impact of endothelial function. Heart and Vessels, 33, 886–892.
    1. Thijssen, D. H. J. , Black, M. A. , Pyke, K. E. , Padilla, J. , Atkinson, G. , Harris, R. A. , Parker, B. , Widlansky, M. E. , Tschakovsky, M. E. , & Green, D. J. (2011). Assessment of flow‐mediated dilation in humans: A methodological and physiological guideline. The American Journal of Physiology‐Heart and Circulatory Physiology, 300, 2–12.
    1. Thijssen, D. , Bruno, R. , van Mil, A. , Holder, S. , Faita, F. , Greyling, A. , Zock, P. , Taddei, S. , Deanfield, J. , Luscher, T. , Green, D. , & Ghiadoni, L. (2019). Expert consensus and evidence‐based recommendations for the assessment of flow‐mediated dilation in humans. European Heart Journal, 40, 2534–2547. 10.1093/eurheartj/ehz350
    1. Thomas, R. J. , King, M. , Lui, K. , Oldridge, N. , Piña, I. L. , Spertus, J. , Bonow, R. O. , Estes, N. A. M. , Goff, D. C. , Grady, K. L. , Hiniker, A. R. , Masoudi, F. A. , Piña, I. L. , Radford, M. J. , Rumsfeld, J. S. , & Whitman, G. R. (2007). AACVPR/ACC/AHA 2007 performance measures on cardiac rehabilitation for referral to and delivery of cardiac rehabilitation/secondary prevention services. Journal of the American College of Cardiology, 50, 1400–1433. 10.1016/j.jacc.2007.04.033
    1. Toumanidis, S. T. , Kaladaridou, A. , Bramos, D. , Skaltsiotes, E. , Agrios, J. N. , Vasiladiotis, N. , Pamboucas, C. , Kottis, G. , & Moulopoulos, S. D. (2013). Apical rotation as an early indicator of left ventricular systolic dysfunction in acute anterior myocardial infarction: additional study [Online]. Hellenic Journal of Cardiology, 54, 264–272.
    1. Ueshima, K. , Suzuki, T. , Nasu, M. , Saitoh, M. , Kobayashi, N. , Yamazaki, T. , & Hiramori, K. (2005). Effects of exercise training on left ventricular function evaluated by the Tei index in patients with myocardial infarction. Circulation Journal, 69, 564–566. 10.1253/circj.69.564
    1. Van De Heyning, C. M. , De Maeyer, C. , Pattyn, N. , Beckers, P. J. , Cornelissen, V. A. , Goetschalckx, K. , Possemiers, N. , Van Craenenbroeck, E. M. , Voigt, J. U. , Vanhees, L. , & Shivalkar, B. (2018). Impact of aerobic interval training and continuous training on left ventricular geometry and function: A SAINTEX‐CAD substudy. International Journal of Cardiology, 257, 193–198.
    1. Weiner, R. B. , Deluca, J. R. , Wang, F. , Lin, J. , Wasfy, M. M. , Berkstresser, B. , Stöhr, E. , Shave, R. , Lewis, G. D. , Hutter, A. M. , Picard, M. H. , & Baggish, A. L. (2015). Exercise‐induced left ventricular remodeling among competitive athletes: A phasic phenomenon. Circulation: Cardiovascular Imaging, 8, 1–9.
    1. Wendelhag, I. , Liang, Q. , Gustavsson, T. , & Wikstrand, J. (1997). A new automated computerized analyzing system simplifies readings and reduces the variability in ultrasound measurement of intima‐media thickness. Stroke, 28, 2195–2200. 10.1161/01.STR.28.11.2195
    1. White, H. , Norris, R. , Brown, M. , Brandt, P. , Whitlock, R. , & Wild, C. (1987). Left ventricular end‐systolic volume as the major determinant of survival after recovery from myocardial infarction. Circulation, 76, 44–51. 10.1161/01.CIR.76.1.44
    1. Wisloff, U. , Stoylen, A. , Loennechen, J. P. , Bruvold, M. , Rognmo, O. , Haram, P. M. , Tjonna, A. E. , Helgerud, J. , Slørdahl, S. A. , Lee, S. J. , Videm, V. , Bye, A. , Smith, G. L. , Najjar, S. M. , Ellingsen, Ø. , & Skjærpe, T. (2007). Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: A randomized study. Circulation, 115, 3086–3094.
    1. Witvrouwen, I. , Van Craenenbroeck, E. M. , Abreu, A. , Moholdt, T. , & Kränkel, N. (2021). Exercise training in women with cardiovascular disease: Differential response and barriers ‐ Review and perspective. European Journal of Preventive Cardiology, 28, 779–790.
    1. Wong, A. , Figueroa, A. , Son, W. M. , Chernykh, O. , & Park, S. Y. (2018). The effects of stair climbing on arterial stiffness, blood pressure, and leg strength in postmenopausal women with stage 2 hypertension. Menopause, 25, 731–737. 10.1097/GME.0000000000001072

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