Stroke is the leading cause of adult disability worldwide (29). Jorgensen et al. (17) reported that following a period of rehabilitation, 64% of stroke survivors could walk independently, 14% required assistance, and 22% were unable to walk. Thus, although a large proportion of people who have had strokes return to some form of ambulation, many will walk with some gait impairment.
It is generally accepted that locomotor impairment, which results from many pathological conditions, increases the metabolic cost of walking (4,25,27,30). For example, patients with incomplete spinal cord injury have a 26% greater rate of oxygen uptake when walking compared with healthy subjects (18). Similarly, younger amputee patients who have undergone adequate prosthetic rehabilitation have an increase in energy expenditure of 24% compared with healthy controls even with comparable walking speeds (7).
In those who have experienced a stroke, the energy expenditure of walking is 1.5-2 times greater than healthy controls (9,14,19). On a practical level, the consequences of a relatively high energy cost when walking may limit the individual's daily, functional activity (1,23).
Often quoted previous research examining energy expenditure in those following a stroke has been carried out more than 20 yr ago (9,14). Other studies (6,12) have used a treadmill to examine the differences in oxygen consumption during walking in stroke patients. The advantage of using a treadmill is that the walking speed of the subject can be more easily controlled. However, this is still an ongoing debate regarding whether the kinematics of gait on a treadmill are comparable with those of overground walking in healthy subjects, far less than those with walking impairment (2,3).
Previous work in this field has also focused on older people with stroke (4,10,30). There is a paucity of literature investigating younger people with hemiplegia, who arguably may be significantly more disabled compared with their peer group.
Therefore, the aim of this study was to examine the physiological cost of overground walking in younger stroke patients just prior to discharge from the inpatient phase of their rehabilitation. We aimed to investigate whether this patient group had greater metabolic cost during locomotion than age- and sex-matched controls by comparing the oxygen consumption between the two groups at their own preferred walking speed (PWS) and of the controls at the PWS of the patient.
Additionally, to account for the relatively slow walking speed of stroke patients, we compared metabolic cost per unit of distance of the controls while they walked at the PWS of their matched patient.
METHODS
Thirteen stroke patients and 13 age- and sex-matched control subjects were recruited for the study. The patient group was a convenience sample of young stroke patients (nine males and four females) who had experienced a first episode hemiparesis in the preceding 8 months and were being treated as inpatients in the South Glasgow University Hospital (Table 1). The patients were tested an average of 3.6 months (range of 1-8 months) after their stroke. Hemiparesis was due either to cerebral infarct or hemorrhage and was evident clinically and also radiologically by computerized tomography (CT) scan. To be eligible for the study the patient had to be able to walk for 5 min. The use of a walking aid or orthosis was permitted if this was required by the patient. Patients were excluded if they had significant cardiovascular, respiratory, or musculoskeletal comorbidity. Of the 11 stroke patients whose drug history was available, five patients were taking no medication, six were taking asprin, two were taking betablockers, one subject was taking an angiotensin converting enzyme (ACE) inhibitor, and one a calcium antagonist. These medications were all prescribed following the stroke mainly as secondary preventative measures. Nine of the 13 stroke patients required the use of one cane to walk.
;)
TABLE 1: Description of the stroke patients and their matched control.
The control group was a convenience sample of hospital employees and their families, matched to the patient group in terms of age, weight, and gender (nine males and four females as per patient population). Due to logistical reasons, dietary intake prior to testing could not be regulated for the patient group; hence it was left unregulated for the control group as well.
All subjects were given written information on the study, and written informed consent was obtained. All procedures were approved by the South Glasgow University Trust Hospital's ethics committee and were consistent with the Declaration of Helsinki.
For each of the stroke patients a Motricity index was performed. This test gives a quick overall indication of the patient's upper- and lower-limb impairment. In the lower limb it measures the strength in the hip flexors, knee extensors, and ankle dorsiflexors. It has been shown to be valid and reliable (5,8). The scale ranges from 1, which is representative of no activity, to 100, which represents normal muscle strength.
A COSMED K4b2 (Cosmed, Rome, Italy) gas analysis system was used to measure the percentage of expired oxygen during free walking (16,20). The COSMED system was calibrated prior to each session according to the manufacturer's instructions. Heart rate was measured using a Polar heart rate monitor (Polar, Finland), and gait speed and distance were recorded with a standard stopwatch and a lap counter. The gas analysis system was fitted to the participants, ensuring that the face mask (Hans Rudolph Inc., Kansas City, MO) was attached to avoid any leakage, but remaining comfortable for the participant. The test was initiated on the COSMED, and the subject was asked to sit at rest for a period of 30 s. At the end of this period the test commenced. A discrete period of measuring resting metabolism was not undertaken because prior to testing, dietary intake had not been controlled, and therefore may have led to misleading resting values. Also, previous research similar to our own had not done so (4,10,11,30).
Subjects walked around an elliptical course outlined by two cones 9.5 m apart. This gave a shuttle length of 10 m and eliminated the need for the subjects to stop at each end of the course and turn at 180°, thus encouraging them to walk at a more consistent pace. The course was on the level wooden floor of Glasgow Caledonian University's clinical research center based at South Glasgow University Hospital. For each test the participants walked for 5 min, and the total distance walked and the time taken was recorded. On completion of the 5-min walking period, the subject was requested to sit for 30 s before the test was terminated.
Subjects were first asked to walk around the cones at their PWS. Stroke patients used their normal walking aid if applicable. The control group was then given a minimum recovery period of 5 min, during which the COSMED system remained in place, and they were then instructed to walk at the PWS of the stroke patient to which they were matched. The matched pace was achieved by providing a bleep at the start of each repetition (generated using PowerPoint slide transition advance slide facility, Microsoft Corporation) of the walking circuit and expecting the control to have completed the circuit by the successive bleep. The time between the bleeps was determined to ensure that the control walked at the pace of their matched patient.
Data analysis. Descriptive statistics are presented as means and standard deviations. Age and weight of the two groups, patient and control, were compared. Oxygen uptake per kilogram of body weight (V̇O2 kg−1 (mL·min−1·kg−1)) was used to analyze metabolic cost of gait. The average of this parameter was calculated between minutes 3 and 4 using Excel (Microsoft Corporation). Minutes 3-4 were selected, as the literature suggests that steady state is achieved at this time (12,28). Distance walked and duration of walk were also recorded. Test data were analyzed using a one-way ANOVA, using Mintab version 14 (Minitab Inc.) with the confidence level set at 95%.
RESULTS
The mean age of the patient and control group was 40.7 yr (± 10.0 yr) and 40.8 yr (± 9.6 yr), respectively. The mean weight of the patient group was 69.2 kg (± 15.4 kg), and the mean weight of the control group was 75.2 kg (± 15.9 kg). There were no statistical differences between the two groups in terms of age or weight. For the patient group the mean value for the Motricity index was 52.7 (range 17-80.5), which is close to the midpoint in the scale. Six of the 13 patients had a Motricity index of less than 50%.
At PWS the patient group walked, on average, for 120 m (± 57.8 m) in 310.4 s (± 12.6 s), resulting in an average velocity of 0.39 m·s−1 (± 0.2 m·s−1). In comparison, the control group walked for 373.6 m (± 32.3 m) in 304.5 s (± 1.12 s), resulting in an average velocity of 1.22 m·s−1 (± 0.11 m·s−1). Statistical analysis showed that at PWS there were significant differences between the two groups in walking speed (P < 0.001).
When the control group was asked to walk at a pace equivalent to their matched patient's speed, the control population walked for 122.9 m (± 59.4 m) in 303.4 s (± 12.1 s), resulting in an average velocity of 0.40 m·s−1 (± 0.20 m·s−1). There was no statistical difference in speed between the patient group PWS and the control group at the matched speed.
Figure 1 shows (a) the oxygen uptake and (b) oxygen uptake per unit of distance walked for both patients and controls at their PWS. For oxygen uptake at PWS, patients recorded values of 11.12 mL·kg−1 (± 3.1 mL·kg−1), and controls recorded values of 11.97 mL·kg−1 (± 1.8 mL·kg−1); the values for controls at the PWS of the patients was 7.14 mL·kg−1 (± 1.4 mL·kg−1). There were no statistical differences in oxygen uptake between the controls and patients at their respective PWS (P = 0.403), but a statistical difference was noted between the patients at their PWS and the controls walking at the PWS of the patients (P < 0.01).
FIGURE 1: Mean and standard deviations of (A) oxygen uptake and (B) oxygen uptake per unit of distance for stroke patients at their PWS (white bar), controls at PWS (solid bar), and controls walking at the PWS of the patient to whom they were matched (hatched bar). NS, nonsignificant; * significant at P < 0.05.
When the distance subjects walked was considered in relation to the oxygen uptake, at PWS the oxygen uptake for patients was 0.63 mL·kg−1·m−1 (± 0.41 mL·kg−1·m−1), and for controls 0.16 mL·kg−1·m−1 (± 0.02 mL·kg−1·m−1). The values for controls walking at the PWS of the patients was 0.36 mL·kg−1·m−1 (± 0.18 mL·kg−1·m−1). In this situation there were statistically significant differences between patients and controls at their PWS (P < 0.01) and between patients PWS and controls at PWS of the patients (P = 0.043).
Thus, it appears that at PWS both groups have a similar metabolic oxygen requirement. However, the stroke patients require a significantly greater oxygen uptake to walk a much shorter distance, and thus walk with a much less efficient gait pattern. This is shown in Figure 2 where, at PWS, the oxygen uptake of the control group is very much less than that of the patients, even though the speed of walking is much higher. Even when the controls were asked to walk at the speed matched to that of the patients, the oxygen uptake of the controls generally remained lower than that of the patients. This pattern is consistent with earlier work in this area (3,26).
FIGURE 2: Oxygen uptake per unit of distance as a function of the walking speed of stroke patients at their PWS (open circles), controls at PWS (open squares), and controls walking at the PWS of the patient to whom they were matched (closed squares).
DISCUSSION
The mean age of our patient group was 40.7 yr. This represents a younger population of stroke patients than previously studied, where the mean age was in the sixth or seventh decade (4,6,10,30). The patients in the study had experienced their stoke on average 3.6 months prior to testing, whereas other studies have examined stroke patients much later after the initial event (5,30).
The patient population demonstrated a wide range of motor impairment, as confirmed by the variation in the Motricity index scores. These observations would suggest that overall the stroke patients displayed a relatively high level of disability. However, because the Motricity index has not been recorded in other relevant studies, direct comparisons are not possible. Only 4 of the 13 patients were able to walk independently without the use of a walking aid, and this is comparable to the study by Cunha-Filho et al. (10) where 13 of the 20 subjects with stroke required assistance to walk.
The PWS of the patient group was, on average, 0.39 m·s−1 and was significantly different from that of the controls' PWS of 1.22 m·s−1. The self-selected gait speed of the stroke patients was lower than that observed in other studies, which ranged from 0.48 to 0.67 m·s−1 (10,30) and is much lower than the optimum walking speed in healthy subjects of 1.2-1.4 m·s−1 (21). The relatively low walking speed observed in this study may reflect the fact that these patients had experienced fairly recent strokes and were at a very early (i.e., inpatient) stage in their rehabilitation program. However, the stroke subjects studied by Cunha-Filho et al. (10) had also experienced recent stroke (i.e., less than 6 months), and they were able to walk at a faster pace of 0.67 m·s−1.
At PWS the oxygen uptake of our stroke patients was 11.12 mL·kg−1. This compares with 10.18 mL·kg−1 reported by Cunha-Filho et al. (10). The oxygen uptake of our control group at their PWS was not significantly different from that of the patient group (11.97 mL·kg−1), although it was higher. Cunha-Filho et al. (10) also reported no statistical difference between patients and controls, although the controls did present a lower oxygen uptake than the patients (9.61 vs 10.18 mL·kg−1). This finding is consistent with previous reports that gait is at its most efficient when the person walks at their own PWS. Previous investigations have suggested that the K4b2 may overestimate (13) or underestimate (21) the oxygen uptake of the patients. Whatever the small error of measurement involved, it is systematically the same for both patients and controls within the present study.
The oxygen uptake per unit of distance in the present study was 0.63 mL·kg−1·m−1. This is markedly higher than previous studies, by 125, 91, and 56% (4,10,30). The relatively high value from the present study is probably a direct result of the slower walking speed of our stroke patients compared with those of other studies in this area, even although our patient group are younger than those previously studied.
Danielsson (12) reported oxygen uptake per unit of distance ranging between 0.51 and 0.58 mL·kg−1·m−1, which is comparable with that reported in our study. The study by Danielsson study employed a treadmill to assess gait function with and without carbon composite foot orthosis and reported walking speed ranging from 0.27 to 0.34 m·s−1. However, work on speed adaptations during treadmill and overground walking following stroke (3) identifies that treadmill walking at PWS is on average 0.55 m·s−1 slower than overground walking. It is therefore questionable whether direct comparison between our work and that of Danielsson (12) is valid.
When we matched the speed of the control group to the PWS of the patient group we found that the oxygen uptake and the oxygen uptake per unit of distance walked for the control group were both statistically significantly different from that of the patient group. Patients required a 75% increase in oxygen uptake per unit of distance walking at their PWS compared with controls walking at the PWS of the patients. In comparison, it cost the patient almost three times more oxygen uptake per unit of distance than controls to walk at the patient PWS. This would suggest that the increased metabolic cost of walking for people who have experienced a stroke is not solely due to a slower, and hence less efficient, self-selected pace, as has been suggested previously (25,30).
Tesio et al. (25) suggested that the increased cost of gait in stroke patients may be due to either the reduced speed or mechanical inefficiency. Using a meta-analysis they reported that the cost of walking in stroke was not due to mechanical inefficiency because using the inverted pendulum model (where walking is a system of kinetic energy that is converted to potential energy and then back to kinetic energy again), stroke patients present a lower efficiency on the affected side, which is compensated for by a greater efficiency on the unaffected limb. Olney et al. (23), however, suggest that stroke patients are unable to generate sufficient walking speed to allow energy conservation using the inverted pendulum model, and further suggest that compensatory strategies, especially hip hitching, explain the higher energy cost of walking in stroke patients.
Other explanations for the higher oxygen uptake in stroke relate to the consequential motor impairments that occur following a stroke (e.g., the presence of spasticity (10)). In patients with multiple sclerosis, where the economy of walking is also compromised, Oligiatti et al. (22) hypothesize that agonist/antagonist cocontraction during walking, together with longer contraction times for spastic muscles, lead to increased energy expenditure. This may also be the case for stroke patients who display spasticity.
Other factors, such as pain, fear of falling, and impaired balance may also increase the ener1gy requirement for walking. Thus, the increased cost of walking that is seen following stroke may be due to the direct effect of the stroke and/or the compensatory mechanisms that are employed to allow some functional activity, including walking. The three main contributory factors to the high metabolic cost of stroke gait could be considered as the speed of the gait, the spasticity present, and compensatory mechanisms.
From a rehabilitation perspective, the results of the current study are very important because they demonstrate for the first time that the efficiency of walking of younger stroke patients is significantly compromised. As all of the individuals who took part in the study were inpatients, they were at a very early stage in their rehabilitation process. It is generally accepted that early rehabilitation focuses on mobility, thus improving independence, and it is only in the later stages of rehabilitation that aerobic activity is considered. Initially, the increased effort required to walk may limit activities of daily living. However, in the long term the reduction in activity of the younger stroke victim may lead to a further decline in cardiopulmonary fitness and other problems such as disuse atrophy and weakness, which can further impair function (19).
The observed high metabolic cost and slow speed have an impact on the patient with hemiplegia's functional ambulation in the community. Prior to discharge, our patient group was demonstrating a metabolic cost of overground walking (an everyday activity) that was almost three times greater than comparable nonstroke sufferers. To access facilities such as supermarkets, banks, etc., it has been calculated that individuals have to walk around 300 m from the nearest parking space for a disabled person. (24). Considering these results, it would take the stroke patient over 12 min to walk this distance, and thus would make the effort involved too great for regular functional activity. It has also been calculated that the average walking speed for crossing a road safely is 1.06 m·s−1, which is more than double the average speed of our patients. This study would suggest that, even for younger stroke patients, aerobic training could be a vital component of the rehabilitation process to optimize functional recovery (15).
LIMITATIONS
Only a relatively small number of patients met the inclusion criteria, although the number is comparable with that of previous research. These patients were all free from significant cardiovascular, respiratory, or musculoskeletal comorbidity before suffering their stroke. The same could not be said for the average stroke patient, who is usually older and often has significant comorbidity, and either of these factors would increase oxygen demand when walking. Because of the small numbers in this study, generalizability of these findings should be viewed with caution.
All of our patients were tested relatively soon after their stroke (average 3.6 months), and it is therefore difficult to demarcate the relative impact of age and/or time since stroke onset had on our results. In the absence of an older control group and the size of the sample rendering covariate analysis undesirable, statistical methods to achieve this have not been attempted. Previous work in this area with comparable times since stroke onset in an older patient group (10,11) reported considerably lower oxygen uptake per unit of distance than reported in the present study.
Because recovery can continue for at least 6 months (26), it would be interesting to repeat our study and test the patients again after 6 months or 1 yr to investigate the long-term effect of the stroke on their oxygen consumption.
CONCLUSION
As has been shown previously, this study confirms that there is increased energy expenditure when walking with a hemiplegic gait. Understandably, the inpatient stage of neurorehabilitation programs tends to focus on improving the patient's mobility and function and reducing hospital stay. This study would suggest that, even for younger stroke patients, early rehabilitation should also consider aerobic evaluation and training, with the ultimate aim of optimizing functional independence in the community.
We would like to thank the patients and controls who volunteered for this study, and the staff at South Glasgow University Hospital for their help and support. This study was carried out with no external funding.
REFERENCES
1. Ada, L., C. M. Dean, J. M. Hall, J. Bampton, and S. Crompton. A treadmill and overground walking program improves walking in persons residing in the community after stroke: a placebo-controlled, randomized trial.
Arch. Phys. Med. Rehabil. 84:1486-1491, 2003.
2. Alton, F., L. Baldey, S. Caplan, and M. C. Morrissey. A kinematic comparison of overground and treadmill walking.
Clin. Biomech. 13:434-440, 1998.
3. Bayat, R., H. Barbeau, and A. Lamontagne. Speed and temporal-distance adaptations during treadmill and overground walking following stroke.
Neurorehabil. Neural. Repair 19:115-124, 2005.
4. Bernardi, M., A. Macaluso, E. Sproviero, et al. Cost of walking and locomotor impairment.
J. Electromyogr. Kinesiol. 9:149-157, 1999.
5. Cameron, D., and R. W. Bonhannon. Criterion validity of lower extremity Motricity Index scores.
Clin. Rehabil. 14:208-211, 2000.
6. Chen, G., C. Patten, D. H. Kothari, and F. E. Zajac. Gait differences between individuals with post-stroke hemiparesis and non-disabled controls at matched speeds.
Gait Posture 22:51-56, 2005.
7. Chin, T., S. Sawamura, R. Shiba, et al. Effect of intelligent prosthesis (IP) on the walking ability of young transfemoral amputees: comparison of IP users with able bodied people.
Am. J. Phys. Med. Rehabil. 82:447-451, 2003.
8. Collin, C., and D. Wade. Assessing motor impairment after stroke: a pilot reliability study.
J. Neurol. Neurosurg. Psychiatry 53:576-579, 1990.
9. Corcoran, P. J., R. H. Jebson, G. L. Brengelman, and B. C. Simons. Effects of plastic and metal leg braces on speed and energy cost of hemiparetic ambulation.
Arch. Phys. Med. Rehabil. 51:69-77, 1970.
10. Cunha-Filho, I. T., H. Henson, H. Qureshy, A. L. Williams, S. A. Holmes, and E. J. Protas. Differential responses to measures of gait performance among healthy and nNeurologically impaired individuals.
Arch. Phys. Med. Rehabil. 84:1774-1779, 2003.
11. Cunha-Filho, I. T., H. Henson, S. Wankadia, and E. J. Protas. Reliability of measures of gait performance and oxygen consumption with stroke survivors.
J. Rehab. Res. Dev. 40:19-26, 2002.
12. Danielsson, A., and K. S. Sunnerhagen. Energy expenditure in stroke subjects walking with a carbon composite ankle foot orthosis.
J. Rehabil. Med. 36:165-169, 2003.
13. Duffield, R., B. Dawson, H. C. Pinnington, and P. Wong. Accuracy and reliability of a Cosmed K4b2 portable gas analysis system.
J. Sci. Med. Sport 7:11-22, 2004.
14. Gerston, J., and W. Orr. External work of walking in hemiparetic patients.
Scand. J. Rehabil. Med. 3:85-88, 1971.
15. Gordon, N. F., M. Gulanick, F. Costa, 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.
Circulation 109:2031-2041, 2004.
16. Hausswirth, C., A. X. Bigard, and J. M. Le Chevalier. The Cosmed K4 telemetry system as an accurate device for oxygen uptake measurements during exercise.
Int. J. Sports Med. 18:449-53, 1997.
17. Jorgensen, H. S., H. Nakayama, H. O. Raaschou, and T. S. Olsen. Recovery of walking function in stroke patients: the Copenhagen Stroke Study.
Arch. Phys. Med. Rehabil. 76:27-32, 1995.
18. Lapointe, R., Y. Lajoie, O. Serresse, and H. Barbeau. Functional community ambulation requirements in incomplete spinal cord injured subjects.
Spinal Cord 39:327-335, 2001.
19. Macko, R. F., L. I. Katzel, A. Yataco, et al. Low-velocity graded treadmill stress testing in hemiparetic stroke patients.
Stroke 28:988-992, 1997.
20. Maiolo, C., G. Melchiorri, L. Iacopino, S. Masala, and A. De Lorenzo. Physical activity energy expenditure measured using a portable telemetric device in comparison with a mass spectrometer.
Br. J. Sports Med. 37:445-447, 2003.
21. McLaughlin, J. E., G. A. King, E. T. Howley, D. R. Basset Jr., and B. E. Ainsworth. Validation of the Cosmed K4 b2 Portable Metabolic System.
J. Sports Med. 22:280-284, 2001.
22. Oligiati, R., J. Burgunder, and M. Mumenthaler. Increased energy cost of walking in multiple sclerosis: effect of spasticity, ataxia and weakness.
Arch. Phys. Med. Rehabil. 69:846-849, 1989.
23. Olney, S. J., T. N. Monga, and P. A. Costigan. Mechanical energy of walking of stoke patients.
Arch. Phys. Med. Rehabil. 67:92-98, 1986.
24. Robinett, C. S., and M. A. Vondran. Functional ambulation velocity and distance requirements in rural and urban communities.
Phys. Ther. 68:1371-1373, 1998.
25. Tesio, L., G. S. Roi, and F. Moller. Pathological gaits: inefficiency is not a rule.
Clin. Biomech. 6:47-50, 1991.
26. Wade, D. T., and R. L. Hewer. Functional abilities after stroke: measurement, natural history and prognosis.
J. Neurol. Neurosurg. Psychiatry 50:177-182, 1987.
27. Waters, R. L., and S. Mulroy. The energy expenditure of normal and pathologic gait.
Gait Posture 9:207-231, 1999.
28. Whipp, B. J., and K. Wasserman. O
2 uptake kinetics for various intensities of constant load work.
J. Appl. Physiol. 33:351-356, 1972.
29. World Health Organization.
The World Health Report 2003 - shaping the future. World Health Organization. Page 20, 2003.
30. Zamparo, P., M. P. Francescato, G. De Luca, L. Lovati, and P. E. Di Prampero. The energy cost of level walking in patients with hemiplegia.
Scand. J. Med. Sci. Sports 5:348-52, 1995.
