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Systematic review of cardiopulmonary exercise testing post stroke: Are we adhering to practice recommendations?
OBJECTIVE: To systematically review the use of cardiopulmonary exercise testing in people who have survived a stroke. The following questions are addressed: (i) What are the testing procedures used? (ii) What are the patient, safety and outcomes characteristics in the cardiopulmonary exercise testing procedures? (iii) Which criteria are used to determine maximum oxygen uptake (VO2peak/max) in the cardiopulmonary exercise testing procedures?
METHODS: Systematic review of studies of cardiopulmonary exercise testing in stroke survivors. PubMed, EMBASE, and CINAHL were searched from inception until January 2014. MeSH headings and keywords used were: oxygen capacity, oxygen consumption, oxygen uptake, peak VO2, max VO2, aerobic fitness, physical fitness, aerobic capacity, physical endurance and stroke. Search and selection were performed independently by 2 reviewers. Sixty studies were scrutinized, including 2,104 stroke survivors.
RESULTS: Protocols included treadmill (n = 21), bicycle (n = 33), stepper (n = 3) and arm (n = 1) ergometry. Five studies reported 11 adverse events (1%). Secondary outcomes were reported in few studies, which hampered interpretation of the patient’s effort, and hence the value of the VO2peak.
CONCLUSION: Most studies did not adhere, or insufficiently adhered, to the existing cardiopulmonary exercise testing guidelines for exercise testing. Thus, the results of cardiopulmonary exercise testing protocols in stroke patients cannot be compared.
Ingrid G.L. van de Port, Gert Kwakkel, Harriet Wittink
, Center of Excellence for Rehabilitation Medicine Utrecht, Rehabilitation Center De Hoogstraat and Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, NL-3583 TM Utrecht, The Netherlands. E-mail: firstname.lastname@example.org
2. Gordon NF, Gulanick M, Costa F, Fletcher G, Franklin BA, Roth EJ, et al. Physical activity and exercise recommendations for stroke survivors: an American Heart Association scientific statement from the Council on Clinical Cardiology, Subcommittee on Exercise, Cardiac Rehabilitation, and Prevention; the Council on Cardiovascular Nursing; the Council on Nutrition, Physical Activity, and Metabolism; and the Stroke Council. Stroke 2004; 35: 1230–1240.
3. Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, et al. Clinician’s guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation 2010; 122: 191–225.
4. American Thoracic Society, American College of Chest Physicians. ATS/ACCP Statement on cardiopulmonary exercise testing. Am J Respir Crit Care Med 2003; 167: 211–277.
5. Guazzi M, Adams V, Conraads V, Halle M, Mezzani A, Vanhees L, et al. EACPR/AHA Scientific Statement. Clinical recommendations for cardiopulmonary exercise testing data assessment in specific patient populations. Circulation 2012; 126: 2261–2274.
6. Outermans J, van de Port I, Wittink H, de Groot J, Kwakkel G. How strongly is aerobic capacity correlated with walking speed and distance after stroke? Systematic review and meta-analysis of the literature. Phys Ther 2015; 95: 835–853.
7. Stoller O, de Bruin ED, Knols RH, Hunt KJ. Effects of cardiovascular exercise early after stroke: systematic review and meta-analysis. BMC Neurol 2012; 12: 45.
8. Smith AC, Saunders DH, Mead G. Cardiorespiratory fitness after stroke: a systematic review. Int J Stroke 2012; 7: 499–510.
9. Hill A, Lupton H. Muscular exercise, lactic acid, and the supply and utilization of oxygen. Q J Med 1923; 16: 135–171.
10. Duncan GE, Howley ET, Johnson BN. Applicability of VO2max criteria: discontinuous versus continuous protocols. Med Sci Sports Exerc 1997; 29: 273–278.
11. Howley ET, Bassett DR, Jr, Welch HG. Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc 1995; 27: 1292–1301.
12. Kelly JO, Kilbreath SL, Davis GM, Zeman B, Raymond J. Cardiorespiratory fitness and walking ability in subacute stroke patients. Arch Phys Med Rehabil 2003; 84: 1780–1785.
13. 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.
14. Eng JJ, Dawson AS, Chu KS. Submaximal exercise in persons with stroke: test-retest reliability and concurrent validity with maximal oxygen consumption. Arch Phys Med Rehabil 2004; 85: 113–118.
15. Jones LW, Eves ND, Haykowsky M, Joy AA, Douglas PS. Cardiorespiratory exercise testing in clinical oncology research: systematic review and practice recommendations. Lancet Oncol 2008; 9: 757–765.
16. Stoller O, de Bruin ED, Schindelholz M, Schuster C, de Bie RA, Hunt KJ. Evaluation of exercise capacity after severe stroke using robotics-assisted treadmill exercise: a proof-of-concept study. Technol Health Care 2013; 21: 157–166.
17. 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: 327–335.
18. Hill TR, Gjellesvik TI, Moen PM, Torhaug T, Fimland MS, Helgerud J, et al. Maximal strength training enhances strength and functional performance in chronic stroke survivors. Am J Phys Med Rehabil 2012; 91: 393–400.
19. Salbach NM, Brooks D, Romano J, Woon L, Dolmage TE. Cardiorespiratory responses during the 6-minute walk and ramp cycle ergometer tests and their relationship to physical activity in stroke. Neurorehabil Neural Repair 2014; 28: 111–119.
20. Stoller O, Schindelholz M, Bichsel L, Schuster C, de Bie RA, de Bruin ED, et al. Feedback-controlled robotics-assisted treadmill exercise to assess and influence aerobic capacity early after stroke: a proof-of-concept study. Disabil Rehabil Assist Technol 2014; 9: 271–278.
21. Jakovljevic DG, Moore SA, Tan LB, Rochester L, Ford GA, Trenell MI. Discrepancy between cardiac and physical functional reserves in stroke. Stroke 2012; 43: 1422–1425.
22. Teixeira da Cunha Filho I, Lim PA, Qureshy H, Henson H, Monga T, Protas EJ. A comparison of regular rehabilitation and regular rehabilitation with supported treadmill ambulation training for acute stroke patients. J Rehabil Res Dev 2001; 38: 245–255.
23. Chen JK, Chen TW, Chen CH, Huang MH. Preliminary study of exercise capacity in post-acute stroke survivors. Kaohsiung J Med Sci 2010; 26: 175–181.
24. Fujitani J, Ishikawa T, Akai M, Kakurai S. Influence of daily activity on changes in physical fitness for people with post-stroke hemiplegia. Am J Phys Med Rehabil 1999; 78: 540–544.
25. Stibrant Sunnerhagen K. Circuit training in community-living “younger” men after stroke. J Stroke Cerebrovasc Dis 2007; 16: 122–129.
26. Michael K, Goldberg AP, Treuth MS, Beans J, Normandt P, Macko RF. Progressive adaptive physical activity in stroke improves balance, gait, and fitness: preliminary results. Top Stroke Rehabil 2009; 16: 133–139.
27. Tomczak CR, Jelani A, Haennel RG, Haykowsky MJ, Welsh R, Manns PJ. Cardiac reserve and pulmonary gas exchange kinetics in patients with stroke. Stroke 2008; 39: 3102–3106.
28. Billinger SA, Loudon JK, Gajewski BJ. Validity of a total body recumbent stepper exercise test to assess cardiorespiratory fitness. J Strength Cond Res 2008; 22: 1556–1562.
29. Billinger SA, Guo LX, Pohl PS, Kluding PM. Single limb exercise: pilot study of physiological and functional responses to forced use of the hemiparetic lower extremity. Top Stroke Rehabil 2010; 17: 128–139.
30. Billinger SA, Mattlage AE, Ashenden AL, Lentz AA, Harter G, Rippee MA. Aerobic exercise in subacute stroke improves cardiovascular health and physical performance. J Neurol Phys Ther 2012; 36: 159–165.
31. Tseng BY, Billinger SA, Gajewski BJ, Kluding PM. Exertion fatigue and chronic fatigue are two distinct constructs in people post-stroke. Stroke 2010; 41: 2908–2912.
32. Tang A, Marzolini S, Oh P, McIlroy WE, Brooks D. Feasibility and effects of adapted cardiac rehabilitation after stroke: a prospective trial. BMC Neurol 2010; 10: 40.
33. Marzolini S, Oh P, McIlroy W, Brooks D. The feasibility of cardiopulmonary exercise testing for prescribing exercise to people after stroke. Stroke 2012; 43: 1075–1081.
34. Sutbeyaz ST, Koseoglu F, Inan L, Coskun O. Respiratory muscle training improves cardiopulmonary function and exercise tolerance in subjects with subacute stroke: a randomized controlled trial. Clin Rehabil 2010; 24: 240–250.
35. Macko RF, DeSouza CA, Tretter LD, Silver KH, Smith GV, Anderson PA, et al. Treadmill aerobic exercise training reduces the energy expenditure and cardiovascular demands of hemiparetic gait in chronic stroke patients. A preliminary report. Stroke 1997; 28: 326–330.
36. Mackay-Lyons MJ, Makrides L. Longitudinal changes in exercise capacity after stroke. Arch Phys Med Rehabil 2004; 85: 1608–1612.
37. Mackay-Lyons M, McDonald A, Matheson J, Eskes G, Klus MA. Dual effects of body-weight supported treadmill training on cardiovascular fitness and walking ability early after stroke: a randomized controlled trial. Neurorehabil Neural Repair 2013; 27: 644–653.
38. Mackay-Lyons M, Makrides L. Exercise capacity early after stroke. Arch Phys Med Rehabil 2002; 83: 1697–1702.
39. 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.
40. Letombe A, Cornille C, Delahaye H, Khaled A, Morice O, Tomaszewski A, et al. Early post-stroke physical conditioning in hemiplegic patients: a preliminary study. Ann Phys Rehabil Med 2010; 53: 632–642.
41. Carvalho C, Willen C, Sunnerhagen KS. Relationship between walking function and one-legged bicycling test in subjects in the later stage post-stroke. J Rehabil Med 2008; 40: 721–726.
42. Rimmer JH, Rauworth AE, Wang EC, Nicola TL, Hill B. A preliminary study to examine the effects of aerobic and therapeutic (nonaerobic) exercise on cardiorespiratory fitness and coronary risk reduction in stroke survivors. Arch Phys Med Rehabil 2009; 90: 407–412.
43. Rimmer JH, Riley B, Creviston T, Nicola T. Exercise training in a predominantly African-American group of stroke survivors. Med Sci Sports Exerc 2000; 32: 1990–1996.
44. Yates JS, Studenski S, Gollub S, Whitman R, Perera S, Lai SM, et al. Bicycle ergometry in subacute-stroke survivors: feasibility, safety, and exercise performance. J Aging Phys Activity 2004; 12: 64–74.
45. Askim T, Dahl AE, Aamot IL, Hokstad A, Helbostad J, Indredavik B. High-intensity aerobic interval training for patients 3–9 months after stroke: a feasibility study. Physiother Res Int 2013; 29: 343–350.
46. Kim BR, Han EY, Joo SJ, Kim SY, Yoon HM. Cardiovascular fitness as a predictor of functional recovery in subacute stroke patients. Disabil Rehabil 2014; 36: 227–231.
47. Pang MY, Eng JJ, Dawson AS. Relationship between ambulatory capacity and cardiorespiratory fitness in chronic stroke: influence of stroke-specific impairments. Chest 2005; 127: 495–501.
48. Dobrovolny CL, Ivey FM, Rogers MA, Sorkin JD, Macko RF. Reliability of treadmill exercise testing in older patients with chronic hemiparetic stroke. Arch Phys Med Rehabil 2003; 84: 1308–1312.
49. Shephard R. Maximal oxygen intake and independence in old age. Br J Sports Med 2009; 43: 342–346.
50. Fairbarn M, Blackie S, McElvaney N, Wiggs B, Paré P, Pardy R. Prediction of heart rate and oxygen uptake during incremental and maximal exercise in healthy adults. Chest 1994; 105: 1365–1369.
51. Janssen TW, Beltman JM, Elich P, Koppe PA, Konijnenbelt H, de Haan A, et al. Effects of electric stimulation-assisted cycling training in people with chronic stroke. Arch Phys Med Rehabil 2008; 89: 463–469.
52. Danielsson A, Sunnerhagen KS. Oxygen consumption during treadmill walking with and without body weight support in patients with hemiparesis after stroke and in healthy subjects. Arch Phys Med Rehabil 2000; 81: 953–957.
53. Gordon NF, Duncan JJ. Effect of beta-blockers on exercise physiology: implications for exercise training. Med Sci Sports Exerc 1991; 23: 668–676.
54. Buchfuhrer MJ, Hansen JE, Robinson TE, Sue DY, Wasserman K, Whipp BJ. Optimizing the exercise protocol for cardiopulmonary assessment. J Appl Physiol Respir Environ Exerc Physiol 1983; 55: 1558–1564.
55. Olivier C, Dore J, Blanchet S, Brooks D, Richards CL, Martel G, et al. Maximal cardiorespiratory fitness testing in individuals with chronic stroke with cognitive impairment: practice test effects and test-retest reliability. Arch Phys Med Rehabil 2013; 94: 2277–2282.
56. Myers J, Arena R, Franklin B, Pina I, Kraus WE, McInnis K, et al. Recommendations for clinical exercise laboratories: a scientific statement from the American Heart Association. Circulation 2009; 119: 3144–3161.
57. Swain DP, Abernathy KS, Smith CS, Lee SJ, Bunn SA. Target heart rates for the development of cardiorespiratory fitness. Med Sci Sports Exerc 1994; 26: 112–116.
58. Huggett DL, Connelly DM, Overend TJ. Maximal aerobic capacity testing of older adults: a critical review. J Gerontol A Biol Sci Med Sci 2005; 60: 57–66.
59. Poole DC, Wilkerson DP, Jones AM. Validity of criteria for establishing maximal O2 uptake during ramp exercise tests. Eur J Appl Physiol 2008; 102: 403–410.
60. Midgley AW, Carroll S, Marchant D, McNaughton LR, Siegler J. Evaluation of true maximal oxygen uptake based on a novel set of standardized criteria. Appl Physiol Nutr Metab 2009; 34: 115–123.
61. Edvardsen E, Hem E, Anderssen SA. End criteria for reaching maximal oxygen uptake must be strict and adjusted to sex and age: a cross-sectional study. PLoS One 2014; 9: e85276.
62. Cumming GR, Borysyk LM. Criteria for maximum oxygen uptake in men over 40 in a population survey. Med Sci Sports 1972; 4: 18–22.
63. Brooks D, Tang A, Sibley KM, McIlroy WE. Profile of patients at admission into an inpatient stroke rehabilitation programme: cardiorespiratory fitness and functional characteristics. Physiother Can 2008; 60: 171–179.
64. Gjellesvik TI, Brurok B, Hoff J, Torhaug T, Helgerud J. Effect of high aerobic intensity interval treadmill walking in people with chronic stroke: a pilot study with one year follow-up. Top Stroke Rehabil 2012; 19: 353–360.
65. Globas C, Becker C, Cerny J, Lam JM, Lindemann U, Forrester LW, et al. Chronic stroke survivors benefit from high-intensity aerobic treadmill exercise: a randomized control trial. Neurorehabil Neural Repair 2012; 26: 85–95.
66. Ivey FM, Hafer-Macko CE, Ryan AS, Macko RF. Impaired leg vasodilatory function after stroke: adaptations with treadmill exercise training. Stroke 2010; 41: 2913–2917.
67. Lee SY, Kang SY, Im SH, Kim BR, Kim SM, Yoon HM, et al. The effects of assisted ergometer training with a functional electrical stimulation on exercise capacity and functional ability in subacute stroke patients. Ann Rehabil Med 2013; 37: 619–627.
68. Luft AR, Macko RF, Forrester LW, Villagra F, Ivey F, Sorkin JD, et al. Treadmill exercise activates subcortical neural networks and improves walking after stroke: a randomized controlled trial. Stroke 2008; 39: 3341–3350.
69. Macko RF, Smith GV, Dobrovolny CL, Sorkin JD, Goldberg AP, Silver KH. Treadmill training improves fitness reserve in chronic stroke patients. Arch Phys Med Rehabil 2001; 82: 879–884.
70. Macko RF, Ivey FM, Forrester LW, Hanley D, Sorkin JD, Katzel LI, et al. Treadmill exercise rehabilitation improves ambulatory function and cardiovascular fitness in patients with chronic stroke: a randomized, controlled trial. Stroke 2005; 36: 2206–2211.
71. Michael KM, Allen JK, Macko RF. Reduced ambulatory activity after stroke: the role of balance, gait, and cardiovascular fitness. Arch Phys Med Rehabil 2005; 86: 1552–1556.
72. Michael KM, Allen JK, Macko RF. Fatigue after stroke: relationship to mobility, fitness, ambulatory activity, social support, and falls efficacy. Rehabil Nurs 2006; 31: 210–217.
73. Ovando AC, Michaelsen SM, Carvalho T, Herber V. Evaluation of cardiopulmonary fitness in individuals with hemiparesis after cerebrovascular accident. Arq Bras Cardiol 2011; 96: 140–147.
74. Patterson SL, Forrester LW, Rodgers MM, Ryan AS, Ivey FM, Sorkin JD, et al. Determinants of walking function after stroke: differences by deficit severity. Arch Phys Med Rehabil 2007; 88: 115–119.
75. Stookey AD, Katzel LI, Steinbrenner G, Shaughnessy M, Ivey FM. The Short Physical Performance Battery as a Predictor of Functional Capacity after Stroke. J Stroke Cerebrovasc Dis 2014; 23: 130–135.
76. Yang AL, Lee SD, Su CT, Wang JL, Lin KL. Effects of exercise intervention on patients with stroke with prior coronary artery disease: aerobic capacity, functional ability, and lipid profile: a pilot study. J Rehabil Med 2007; 39: 88–90.
77. Chang WH, Kim MS, Huh JP, Lee PK, Kim YH. Effects of robot-assisted gait training on cardiopulmonary fitness in subacute stroke patients: a randomized controlled study. Neurorehabil Neural Repair 2012; 26: 318–324.
78. Koopman AD, Eken MM, van Bezeij T, Valent LJ, Houdijk H. Does clinical rehabilitation impose sufficient cardiorespiratory strain to improve aerobic fitness? J Rehabil Med 2013; 45: 92–98.
79. Baert I, Vanlandewijck Y, Feys H, Vanhees L, Beyens H, Daly D. Determinants of cardiorespiratory fitness at 3, 6 and 12 months poststroke. Disabil Rehabil 2012; 34: 1835–1842.
80. Chen CK, Weng MC, Chen TW, Huang MH. Oxygen uptake response to cycle ergometry in post-acute stroke patients with different severity of hemiparesis. Kaohsiung J Med Sci 2013; 29: 617–623.
81. Courbon A, Calmels P, Roche F, Ramas J, Rimaud D, Fayolle-Minon I. Relationship between maximal exercise capacity and walking capacity in adult hemiplegic stroke patients. Am J Phys Med Rehabil 2006; 85: 436–442.
82. Katoh J, Murakami M, Hirayama M, Nagata Y, Hayakawa M, Tanizaki T. Correlation of pedometric measurement of daily physical activity with exercise endurance by oxygen uptake kinetics in ambulatory stroke patients. J Phys Ther Sci 2002; 14: 77–80.
83. Lee M, Kilbreath SL, Singh MF, Zeman B, Lord SR, Raymond J, et al. Comparison of effect of aerobic cycle training and progressive resistance training on walking ability after stroke: a randomized sham exercise-controlled study. J Am Geriatr Soc 2008; 56: 976–985.
84. Murakami M, Katoh J, Hirayama M, Hayakawa M, Tanizaki T, Furukawa H. Physical fitness and exercise endurance measured by oxygen uptake kinetics in stroke patients. J Phys Ther Sci 2002; 14: 73–76.
85. Potempa K, Lopez M, Braun LT, Szidon JP, Fogg L, Tincknell T. Physiological outcomes of aerobic exercise training in hemiparetic stroke patients. Stroke 1995; 26: 101–105.
86. Severinsen K, Jakobsen JK, Overgaard K, Andersen H. Normalized muscle strength, aerobic capacity, and walking performance in chronic stroke: a population-based study on the potential for endurance and resistance training. Arch Phys Med Rehabil 2011; 92: 1663–1668.
87. Tang A, Eng JJ, Brasher PM, Madden KM, Mohammadi A, Krassioukov AV, et al. Physical Activity Correlates with Arterial Stiffness in Community-dwelling Individuals with Stroke. J Stroke Cerebrovasc Dis 2014; 23: 259–266.
88. Tseng BY, Kluding P. The relationship between fatigue, aerobic fitness, and motor control in people with chronic stroke: a pilot study. J Geriatr Phys Ther 2009; 32: 97–102.
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