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Key Words Heart rate, brain, injury, oxygen consumption. by Helen Dawes Andrew Bateman Jane Culpan Oona M Scott Neil K Roach Derick T Wade

Heart Rate as a Measure of Exercise Testing Early after Acquired Brain Injury
Summary Background The relationship between heart rate and oxygen consumption ( V O2) in individuals with acquired brain injury has been described as being curvilinear; which could lead to under-estimation of exercise intensity when prescribed by heart rate. Purpose This study examines the linearity of the heart rate/oxygen consumption relationship during incremental cycle ergometer exercise in individuals early after brain injury and provides an estimate of the intra-individual reliability of the heart rate response. Method A convenience sample of 38 individuals attending an inpatient neurological rehabilitation centre after acquired brain injury who met the inclusion criteria (trauma 18, stroke 9, tumour and hypoxia 11) underwent testing. Oxygen consumption and heart rate were measured during a graded cycle ergometer test. A further six individuals underwent re-testing within one week Results The heart rate/ oxygen consumption response was linear and can be described by the equation: HR = 86 + 0.029 V O2 ( SE; 0.003). Heart rate during the second test was on average 8 beats per minute lower than in the first test. The random error during the final stage of testing was 8 and 17 beats per minute respectively. Conclusions The linear relationship between heart rate and oxygen consumption suggests that exercise intensity can be validly prescribed from heart rate in this group and within the scale range used in this study. The reduced heart rate in individuals re-tested within ten days suggests some bias and that clinicians may need to consider more familiarisation periods before exercise testing. Reliability of exercise testing in this clinical group needs further investigation.
Dawes, H, Bateman, A, Culpan, J, Scott, O M, Roach, N K and Wade, T (2003). Heart rate as a measure of exercise testing early after acquired brain injury, Physiotherapy, 89, 10, 570-574.
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Introduction Aerobic exercise as part of the rehabilitation process for people with acquired brain injury has been shown to increase physiological fitness reserve and improve movement economy (Hunter et al, 1990; Potempa et al, 1995; Bateman et al, 1998, 1999; Macko et al , 2001). For accurate prescription of aerobic exercise in this clinical group, valid and reliable measures of exercise intensity are needed. In healthy individuals it has been established that the rate of oxygen consumption (V O 2 ) increases linearly with work rate during cycling and is the criterion measure of exercise intensity during sub-maximal aerobic exercise. The linear relationship of heart rate to V O2 during sub-maximal exercise and high level of intra-individual reliability enable heart rate to be used as a valid and stable measure of exercise intensity (Jones and Kane, 1979; ACSM, 1998). Measures of oxygen use are cumbersome and not appropriate for measuring exercise intensity in the clinical environment; measures of heart rate are more commonly used. The relationship of work-rate to V O2 has been described as linear in individuals recovering from stroke, traumatic brain injury and acquired brain injury (Hunter et al , 1990; Macko et al , 1997a; Dawes et al , 2003). However there is limited description of the heart rate response in individuals with acquired brain injury (Hoskins, 1975; Becker et al, 1978; King et al, 1989; Macko et al, 1997b; Bateman et al, 1999; Dawes et al , 1999). It has been suggested that the relationship between heart rate and oxygen consumption during sub-maximal exercise in people with acquired brain injury is linear, but this result was found from a two-stage incremental test (Becker et al , 1978) whereas the results of a multi-stage

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incremental exercise test described the relationship as curvilinear (Jankowski and Sullivan, 1990). A non-linear response has also been reported during arm exercise in some patients with multiple sclerosis (Senaratne et al, 1984). Why would the relationship between heart rate and V O 2 be non-linear in individuals with acquired brain injury? Previous studies have proposed autonomic dysfunction as a possible factor altering cardiovascular control in individuals early after acquired brain injury (Hines et al, 1981; Senaratne et al, 1984; Koorpelainen, 1999). An alternative suggestion is an altered central neural drive (Innes and Evans, 1992) or altered central response to afferent impulses arriving from skeletal muscle during exercise (Senaratne et al, 1984). Certainly the heart rate/V O2 relationship requires further investigation, as a curvilinear relationship between heart rate and V O2 may lead to underestimation of exercise intensity if prescribed from heart rate, as this prescription is based on a linear heart rate/V O 2 relationship. An altered relationship would have implications in the accurate and effective prescription of exercise in this group. This study examined heart rate in relation to V O 2 during incremental cycle ergometer exercise. The test-retest reliability of this response was investigated in a small sub-group. Methods This study was conducted on a convenience sample of 38 inpatients of whom 29 were male, a mean of 18.8 (SD 6.8) weeks after brain injury (see table). Consecutively referred patients were recruited to the study if they were medically stable, certified by the senior medical officer following American College of Sports Medicine guidelines (1998), were able to exercise on a bicycle, follow simple commands and were not currently taking medication with known exercise effects. This sample reflected a typical group of individuals selected for aerobic training following brain injury. Individuals participated after reading the invitation letter and giving informed consent in accordance with the declaration of Helsinki and local Research Ethics Committee guidelines (WHO, 1996). Assessment of the response to incremental cycle ergometer exercise was

conducted between 10.00 and 15.00 hours. All participants were familiarised with the procedure and equipment in a session in the week preceding testing and asked to refrain from consumption of food, alcohol, caffeine, cigarettes and taking part in any physical exercise in the two hours prior to testing. Cycle ergometer testing was used as this enabled the early recruitment of individuals after brain injury. Testing was conducted within a room temperature range of 23 to 26 C. Blood pressure was monitored throughout the procedure according to the American College of Sports Medicine guidelines (1998). After resting on the cycle ergometer (Ergoline ER800s, Bitz, Germany) for three minutes, a modified Sjostrand protocol was per formed (Sjostrand, 1947). Patients cycled at a cadence of 40 rpm. After an initial unloaded three minutes, work rate was initially increased by 25 watts and then by 10 watts every two minutes, until volitional exhaustion. Heart rate was recorded using a three-lead electrocardiogram (Siemens, Germany). Breath-by-breath V O 2 was monitored continuously (Oxycon Alpha metabolic cart, Bunnik, Netherlands). Breath-by-breath measures of gas concentrations and volumes were averaged over eight breaths and recorded to computer disk at ten-second intervals. Values were calculated from mean values over the final 30 seconds of each incremental stage. Six patients from the sample repeated the same exercise protocol within one week under the same conditions.

Authors Dr Helen Dawes PhD is a senior lecturer in exercise physiology in the School of Biological and Molecular Sciences, Oxford Brookes University and Oxford Centre of Enablement. This study was carried out while she was a research assistant at the University of East London. Dr Andrew Bateman PhD and Jane Culpan BSc are senior lecturers and Professor Oona M Scott PhD is in the Department of Health Sciences, University of East London. Neil K Roach MSc is a subject leader in the Department of Exercise and Sport Science, Manchester Metropolitan University. Professor Derick T Wade MD is a consultant and professor in neurological rehabilitation at Oxford Centre of Enablement.

Characteristics of subjects in study group Injury Male Female Age Barthel score* Mean (SD) Median (range) 38 49 39 (11.6) (10.3) (11.9) 14 (919)

Traumatic brain injury Stroke Tumour and hypoxia

16 5 8

5 4 3

13 (1018) 14 (1019)

* Barthel index of functioning in activities of daily living (maximum score 20 = independence)

Statistical Analysis Employing cur ve estimation, linear regression was found to offer the line of best fit for heart rate to oxygen consumption. This was established by visual inspection of the regression
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200

180

Heart rate (beats per minute)

160

140 120 100

80

60

40 0 500 1000 1500 Oxygen consumption (ml/minute) 2000 2500 3000

Fig 1: Heart rate to rate of oxygen consumption relationship during a continuous incremental cycle ergometer test, cadence 40 rpm in 38 individuals following acquired brain injury y = 86 + 0.029x , r = 0.65, r2 = 0.42 Increment 1: Mean difference of test 1 test 2 (bias) 1.96 SD (random error expressed as limits of agreement) Bias: 10 beats per minute 95% Limits of agreement 28 beats per minute
Difference test 1 - test 2 40 20 0 -20 -40 100 150 200

Mean value test 1 and test 2

Increment 2: Bias: 5 beats per minute 95% Limits of agreement 8 beats per minute
Difference test 1 - test 2 40 20 0 -20 -40

100

150

200

residuals against the independent variable for each curve, the r and r 2 values and from examination of the statistical significance of the parameter estimate of heart rate by analysis of variance. The residuals from regression analysis of the brain injury group met the assumptions of independence, linearity, normality and constant variance. Differences between tests 1 and 2 and the mean of both tests for heart rate were plotted as Bland and Altman plots at exercise increments 1, 2 and the final exercise increment. Plots were observed for heteroscedascity. Random error (1.96 SD) of the two tests at each exercise increment and bias (mean difference) are reported (Atkinson and Nevill, 1999). Results The relationship between heart rate and rate of oxygen consumption during the continuous incremental cycle ergometer test is represented in figure 1. Linear regression was found to give the line of best fit for oxygen consumption against heart rate data. The regression coefficient: heart rate = 86 + 0.029 V O2 was found to best describe the data. Given the regression equation we can be 95% confident that for a given V O2, heart rate will be y 1.96 0.003 . The overall goodness of fit determined by r and r2 was 0.65 and 0.42 respectively. The test-retest reliability for heart rate data obtained from the two tests within 10

Mean value test 1 and test 2

Final increment: Bias: 8 beats per minute 95% Limits of agreement 17 beats per minute
Difference test 1 - test 2 40 20 0 -20 -40

100

150

200

Mean value test 1 and test 2

Fig 2: Bland and Altman plot showing the difference in heart rate (beats per minute) values recorded on two occasions during continuous incremental cycle ergometer exercise plotted against mean heart rate from the two tests. Reported are values recorded at the end of the first, second and final increments. n = 6

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days at increments 1 and 2 and the final increment for six individuals are shown in figure 2. Data are expressed as Bland and Altman plots of the differences between tests 1 and 2 against the mean value obtained for the two tests. There is an observable decrease in heart rate on test 2 in most subjects, but no obser vable heteroscedascity. The bias for each increment (mean difference of tests 1 and 2) and random error (+ 1.96 SD) are expressed in figure 2. Discussion A linear relationship between heart rate and V O 2 was obser ved during submaximal cycling exercise in individuals with acquired brain injury, providing support for the findings of Becker and colleagues (1978). The non-linear relationship described by Jankowski and Sullivan (1990) may have been as a result of their testing protocol having smaller and more frequent time increments. The findings of this current study suggest a linear heart rate response, during incremental cycling in a sub-maximal exercise range, early after brain injury. Exercise intensity expressed as a percentage of maximal heart rate therefore should correspond to a percentage of V O2 max. Heart rate can be validly used to monitor exercise intensity for these clients. It should be noted that people with brain injury often have a reduced exercise capacity and peak heart rate (Hoskins, 1975; King et al , 1989; Potempa et al , 1995; Bateman et al, 1998, 1999). Thus, exercises prescribed at standard recommended intensities as a percentage of estimated maximum heart rate (ACSM, 1998) may work individuals at intensities close to peak heart rate. Exercise intensity
References Atkinson, G and Nevill, A M (1999). Statistical methods for assessing measurement error (reliability) in variables relevant to sports medicine, Sports Medicine, 26, 4, 217-238. American College of Sports Medicine (1998). Guidelines for Graded Exercise Testing and Training, Lea and Febiger, Philadelphia, 5th edn, pages 300-305. Bateman, A, Greenwood, R J and Scott, O M (1998). Quadriceps femoris strength and fatigability in patients after recent brain injury, Journal of Physiology, 509, 44.

is a factor affecting exercise adherence (King et al, 1990) and so when prescribing exercise clinicians should take into account the likely reduced peak heart rate in order to optimise both aerobic training and compliance. Test-retest Intra-individual Reliability The variation in heart rate between tests 1 and 2 was, for the 95% of data points, within 28 beats per minute which is slightly higher than that expected in healthy individuals during cycling (Jones and Kane, 1979). The sample size is small which will have contributed to the magnitude of the variation and further investigation with larger sample sizes is warranted. The lower heart rate values observed in test 2 may reflect some habituation to the test either due to improved movement skill or reduced stress during the testing procedure. This suggests that following brain injury more than one familiarisation period may be required before exercise testing for either research or prescription, as one-off testing may lead to spurious results. Conclusions The linear relationship between heart rate and V O 2 suggests that exercise intensity can be validly prescribed from heart rate in individuals with brain injury. The reduction in heart rate demonstrated on re-testing suggests that more than one familiarisation period may be required before exercise testing in this clinical group. Further investigation of the intraindividual reliability of exercise testing in a larger group of individuals with acquired brain injury is warranted.
Bateman, A, Culpan, J, Dawes, H, TunstallPedoe, D, Scott, O M and Greenwood, R (1999). Exercise tolerance in patients who have suffered recent brain injury, Journal of Sports Sciences, 17, 27-28. Becker, E, Bar-Or, O, Mendelson, L and Najenson, T (1978). Pulmonary functions and responses to exercise of patients following cranio-cerebral injury, Scandinavian Journal of Rehabilitation Medicine, 10, 47-50. Dawes, H, Roach, N, Wade, D and Scott, O M (1999). Variability of rating of exercise intensity perception after brain injury, Proceedings of The British Psychological Society, 7, 2, 122.

Address for Correspondence Dr Helen Dawes, School of Biological and Molecular Sciences, Oxford Brookes University, Gipsy Lane Campus, Headington, Oxford OX3 0BP. E-mail hdawes@brookes .ac.uk Acknowledgements This study was funded by North Thames Regional Health Authority and the University of East London. The authors would like to thank the staff of the Royal National Rehabilitation Unit, Homerton Hospital, where testing was carried out.

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Dawes, H, Bateman, A, Culpan, J, Scott, O, Roach, N, Wade, D and Greenwood, R (2003). The effect of increasing effort on movement economy during incremental cycling exercise in individuals early after acquired brain injury, Clinical Rehabilitation, 17, 5, 528-534. Hines, S, Houston, M and Robertson, D (1981). The clinical spectrum of autonomic dysfunction, American Journal of Medicine, 70, 1091-96. Hoskins, T A (1975). Physiologic responses to known exercise loads in hemiparetic patients, Archives of Physical Medicine and Rehabilitation, 56, 544-450. Hunter, M, Tomberlin, J, Kirkikis, C and Kuna, S T (1990). Progressive exercise testing in closed head-injured subjects: Comparison of exercise apparatus in assessment of a physical conditioning program, Physical Therapy, 70, 363-371. Innes, J A C and Evans, P J (1992). Central command influences in cardiorespiratory response to dynamic exercise in humans with unilateral weakness, Journal of Physiology, 448, 551-563. Jankowski, L W and Sullivan, S J (1990). Aerobic neuromuscular training: Effect on the capacity, efficiency and fatigability of patients with traumatic brain injuries, Archives of Physical Medicine and Rehabilitation, 71, 500-504. Jones, N L and Kane, J W (1979). Quality control of exercise test measurements, Medicine and Science in Sports and Exercise, 11, 368-372. King, J L, Guarracini, M, Lenihan, I, Freeman, D, Gagas, B, Boston, A, Bates, E and Noris, S (1989). Adaptive exercise testing for patients with hemiparesis, Journal of Cardiopulmonary Rehabilitation, 9, 237-242. King, A C, Taylor, C B, Haskell, W L and CeBusk, R F (1990). Identifying strategies for increasing employee physical activity levels: Findings from the Stanford/ Lockheed exercise survey, Health Education Quarterly, 17, 269-285.

Koorpelainen, J T, Sotaniemi, K A, Makikallio, A, Huikuri, H V and Myllyla, V V (1999). Dynamic behaviour of heart rate in ischaemic stroke, Stroke, 30, 5, 1008-13. Macko, R F, Katzel, L I, Yataco, A, Tretter, L D, DeSouza, C A, Dengel, D R, Smith, G V and Silver, K H (1997a). Low-velocity graded treadmill stress testing in hemiparetic stroke patients, Stroke, 28, 5, 989-992. Macko, R F, DeSouza, C A, Tretter, L D, Silver, K H, Smith, G V, Anderson, P A, Tomoyasu, N, Gorman, P and Dengel, D R (1997b). Treadmill aerobic exercise training reduces the energy expenditure and cardiovascular demands of hemiparetic gait in chronic stroke patients, Stroke, 28, 326-330. Macko, R F, Smith, G V, Dobrovolny, C L, Sorkin, J D, Goldberg, A P and Silver, K H (2001). Treadmill training improves fitness reserve in chronic stroke patients, Archives of Physical Medicine and Rehabilitation, 82, 879-894. Potempa, K, Lopez, M, Braun, L T, Szidon, P J, Fogg, L and Tincknell, T (1995). Physiological outcomes of aerobic exercise training in hemiparetic stroke patients, Stroke, 26, 101-105. Senaratne, M P J, Carroll, D, Warren, K G and Kppagoda, T (1984). Evidence for cardiovascular autonomic dysfunction in multiple sclerosis, Journal of Neurology, Neurosurgery and Psychiatry, 44, 47, 947-952. Sjostrand, T (1947). Changes in the respiratory organs of workmen at an ore smelting works, Acta Medica Scandinavica, 196 (suppl) 687-699. World Health Organisation (1996). Declaration of Helsinki, British Medical Journal, 313, 7070, 1448-49.

Key Messages The linear relationship between heart rate and V O2 suggests that exercise intensity can be validly prescribed from heart rate in individuals with acquired brain injury. The reduced heart rate in the six individuals retested within one week suggests that clinicians may need to consider a period of familiarisation before exercise testing in this clinical group.

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