| | Aerobic Capacity After Traumatic Brain Injury: Comparison With a Nondisabled CohortPresented in part to the American Physical Therapy Association, February 2006, San Diego, CA. Abstract Mossberg KA, Ayala D, Baker T, Heard J, Masel B. Aerobic capacity after traumatic brain injury: comparison with a nondisabled cohort. ObjectiveTo compare aerobic capacity of people recovering from traumatic brain injury (TBI) with an age- and sex-matched group of nondisabled sedentary people. DesignDescriptive comparative study of peak and submaximal physiologic responses. SettingResidential postacute treatment center. ParticipantsConvenience sample of 13 people with TBI and 13 age- and sex-matched nondisabled subjects. All subjects could walk 5.3kph (3.3mph), follow 2-step commands, and comply with testing using the gas collection apparatus. InterventionsNot applicable. Main Outcome MeasuresSubjects performed a graded maximal treadmill test during which heart rate, minute ventilation (V̇e), oxygen consumption (V̇o2), carbon dioxide production, and respiratory exchange ratio (RER) were measured every minute until exhaustion. Ventilatory equivalents for oxygen (V̇e/V̇o2) and oxygen pulse were calculated. ResultsSubjects recovering from TBI had significantly lower peak responses for heart rate, Vo2, Ve, and oxygen pulse TBI (P<.01). Peak RER and Ve/Vo2 were similar. There were significant differences in submaximal responses for V̇e/V̇o2 and oxygen pulse. ConclusionsPatients with TBI were significantly more deconditioned than a comparable group of sedentary people without disability. Participation in cardiorespiratory fitness programs after TBI should be encouraged to prevent secondary disability. AN ESTIMATED 1.4 MILLION people sustain a traumatic brain injury (TBI) in the United States every year.1 A large percentage of these people are relatively young, with mild brain injuries that result in few or no physical impairments. Because they are young, they can expect to live for many years with the potential of developing age-related chronic disabilities. Many such disabilities are associated with physical inactivity and a sedentary lifestyle.2 Some negative results of inactivity are poor stamina, reduced muscle strength, and limited flexibility.3 It is well established that generally, people who live sedentary lifestyles are at greater risk for coronary heart disease, hypertension, thromboses, osteoporosis, obesity, certain cancers, and non-insulin-dependent diabetes mellitus.4 Presumably the same risks faced by the general population exist for people recovering from TBI. The combination of living with a disability and being sedentary increases the risk of developing secondary conditions.5 Unfortunately, longitudinal studies that describe chronic disease development and its relation to physical activity levels in TBI patients have not been reported. The effects of these health problems are confounded in people with disabilities. Jankowski and Sullivan6 provided data that strongly suggest that peak aerobic capacity is related to employment productivity in people recovering from TBI; they have a diminished tolerance for continuous physical activity and chronic fatigue is a common complaint, even years after injury.7, 8 For these reasons, it is crucial that they become as active as is feasible. The degree of aerobic or endurance capacity limitation in recovering TBI patients is not well documented. It has been estimated that their peak aerobic capacities are from 65% to 74% of normative values.6, 9, 10 The certainty of these estimates is questionable for several reasons. First, many patients with TBI have physical impairments. Becker et al11 did a direct comparison of nondisabled sedentary subjects and patients with TBI but 58% (11/19) of the patients had residual motor impairments. In addition, that study assessed submaximal responses but not peak responses. Other factors that lead to questions about these estimates relate to the testing protocols. It is not known whether testing protocols used with the subjects with TBI and the normative values from which the estimates were derived were identical. The above estimates are from studies performed with the treadmill as the testing modality,6 while others utilized the cycle ergometer.10 Bhambhani et al10 tested TBI patients on the cycle ergometer and compared their results with those of people without health problems who performed a treadmill protocol.12 Investigators have compared cycling with treadmill ambulation in the nondisabled13 and after TBI9 and found peak oxygen consumption (Vo2peak) was significantly higher on a treadmill than on a bicycle ergometer. Furthermore, it is well known that Vo2peak can vary depending on the treadmill protocol.14, 15 Consequently, these estimates are based on comparisons that may not be valid. We know of no data that directly compares the aerobic capacity of recovering TBI subjects with few, if any, physical impairments with the aerobic capacity of nondisabled subjects of similar age and sex when performing identical graded exercise tests. Such a comparison is necessary in order to draw accurate conclusions about the cardiorespiratory fitness of patients recovering from TBI. Our purpose in this study was to make just such a comparison. Methods  Participants The 13 participants with TBI were residents in a residential postacute treatment center and had been admitted primarily for neuropsychologic and vocational rehabilitation. To be included in the study, they had to be free of overt cardiovascular disease, could not be taking cardiovascular medications, could follow 2-step commands, could comply with the gas collection apparatus, and could walk independently at a treadmill speed of 5.3kph (3.3mph). Patients were screened and clinical examinations found no obvious balance and musculoskeletal impairments. Cognitive screening showed that 9 subjects scored average on attention, language comprehension, sentence repetition, and naming of simple objects. The greatest cognition impairments in the TBI group were in the areas of verbal and auditory memory, visual memory, and visual constructional skills. Table 1 shows the age characteristics of all 26 subjects. Patients with TBI were tested an average of 10.4±9.5 months (range, 6wk to 32mo) after injury. Initial examination postinjury showed 11 subjects had severe injuries (Glasgow Coma Scale [GCS] score range, 3−8), 1 subject had a moderate injury (GCS score, 9), and 1 subject had a mild injury (GCS score, 13). The injuries resulted from motor vehicle collisions (n=10), falls (n=2), and an assault (n=1). An equal number of age- and sex-matched nondisabled subjects were studied after a general screening for cardiovascular health. The apparently healthy people were recruited through personal contact with one of the investigators. They were faculty members, students, and staff members of a local university and the residential treatment center. Twelve men and 1 woman in each group gave their written informed consent to participate. Institutional review boards at both the residential treatment center and the university approved all procedures. All subjects were familiar and comfortable with treadmill ambulation and none were participants in regular formal aerobic exercise programs prior to testing. Five patients with TBI and 1 nondisabled subject were smokers. | | |  | Characteristics | Mean ± SD | Range | |
|---|
| TBI (n=13) | | | | |  Age at injury (y) | 30.4±8.1 | 19–47 | | | Age at test (y) | 31.2±7.9 | 22–48 | | | Nondisabled (n=13) | | | | | Age at test (y) | 31.7±6.8 | 23–49 | | | | |
Instrumentation Cardiorespiratory measures were evaluated using an automated metabolic carta and resting and exercise heart rates were monitored through electrocardiography.b The metabolic cart was calibrated before and immediately after each test, using gases of known concentrations. The pneumotach was calibrated with a 3-L syringe. We used a standard treadmill that was equipped with side railings and handles at the front. Subjects were told to use the hand supports for balance only and were constantly reminded during the test to use them for that purpose only. We used a waist belt that was free of attachments to the treadmill to secure electrocardiography lead wires and to facilitate manual assistance if a subject’s balance was compromised. At no time during the testing, however, were the subjects given manual assistance. Procedure All subjects performed a graded maximal treadmill test that was a modification of the Balke-Ware protocol.16 There was a 2–minute warm-up at 1% incline during which the treadmill speed was gradually increased to a velocity of 5.3kph (3.3mph). During the test, the velocity was kept constant while the incline was increased 2% each minute. This modified protocol has been used previously in people recovering from TBI9, 17 and has been shown to be reliable in this population.18 Heart rate, electrocardiogram, oxygen consumption (V̇o2), carbon dioxide production (V̇co2), minute ventilation (V̇e), and respiratory exchange ratio (RER) were monitored continuously throughout the test. Subjects were encouraged to give their best effort. The test was stopped if the subject asked to stop, if continued ambulation became unsafe, or when 2 of the following 3 peak criteria were achieved: (1) the subject’s V̇o2 reached a plateau with an increase in workload, (2) the heart rate reached 90% of age-predicted maximum (220 − age), and (3) the subject achieved an RER equal to or greater than 1.15.19 Peak effort was defined as the highest values recorded during the last 30 seconds of exercise. Data Analyses Oxygen pulse, a noninvasive estimate of cardiac stroke volume, was calculated as the ratio of oxygen consumed (in L/min) to heart rate (in bpm).20 Ventilatory equivalent for oxygen (V̇e/V̇o2) is a measure of the ventilatory muscle effort required to exchange a given amount of oxygen. It was calculated as the ratio of minute ventilation (in L/min) to oxygen consumed (in L/min). We analyzed peak data for heart rate, Vo2, oxygen pulse, Ve, Ve/Vo2, and RER with paired samples t tests. Because we studied multiple variables, a Bonferroni adjustment was made in order to maintain an α level of .05. We used a multivariate repeated-measures 2-way analysis of variance to test for the main effects of time and group as well as time-by-group interaction for the submaximal responses up to and including minute 6. Data beyond minute 6 were excluded from this submaximal analysis because the first subjects in the TBI group started to reach their peaks after minute 7. Pearson product moment correlations on Vo2peak and heart rate versus subject demographics were performed. All analyses were carried out at the α level of .05. Statistical analyses were performed using a personal computer–based statistical software program.c Results Table 2 shows a comparison of average peak values for heart rate, Vo2, Ve, oxygen pulse, Ve/Vo2, and RER between the 2 subject groups. After the Bonferroni adjustment all variables except Ve/Vo2 and RER differed statistically (P<.01). The fact that RER was similar in the groups suggests that the level of effort (level of anaerobic metabolism) was similar. Patients with TBI were more likely to reach an oxygen plateau and an RER equal to or greater than 1.15 and less likely to reach 90% of their age-predicted maximal heart rate. | | | | Measures | Nondisabled | TBI | |
|---|
| Heart rate (bpm) | 193±9⁎ | 166±18 | | | Vo2 (mL·kg−1·min−1) | 35.4±4.3⁎ | 27.0±4.6 | | | Oxygen pulse (mL/beat) | 15.8±2.2⁎ | 12.0±2.0 | | | Ve (L/min) | 105.7±17.9⁎ | 71.7±14.7 | | | Ve/Vo2 | 34.9±4.7 | 36.4±3.9 | | | RER (Vco2/Vo2) | 1.22±0.10 | 1.22±0.10 | | | | |
Figure 1 illustrates the differences in the distribution of Vo2peak values (in mL·kg−1·min−1) and oxygen pulse (in mL/beat) between participants with no disability and those recovering from TBI. The greater oxygen pulse for the subjects without disability suggests that cardiac stroke volume was lower in patients with TBI. Correlations between the initial severity of injury (GCS) and Vo2peak or heart rate (table 3) were not significant. There was a modest positive correlation (r=.45) between the time since injury and the peak aerobic capacity but this was not significant (P=.12), and recovery time only predicted 20% of the variance in Vo2peak for the subjects with TBI. There was a significant inverse relation (P<.05) between the age of a patient and his/her peak aerobic capacity. There was a much more modest and insignificant relationship (r=−0.36) between age and Vo2peak for the nondisabled subjects. | | | | Subject Demographics | Vo2peak | Peak Heart Rate | |
|---|
| TBI (n=13) | | | | | GCS score | .20 | .02 | | | Time since injury | .45 | .20 | | | Age at test (y) | −.63⁎ | −.27 | | | Nondisabled (n=13) | | | | | Age at test (y) | −.36 | −.44 | | | | |
Examination of submaximal responses revealed that subjects with TBI consumed slightly greater amounts of oxygen during the initial exercise stages (fig 2). During the first 6 minutes of submaximal exercise, however, there was no significant group effect (P=.61). After this time the subjects without disability began consuming greater amounts of oxygen consistent with the greater workload and their greater peak aerobic capacity. Similarly, the TBI subjects had slightly greater submaximal minute ventilation than the nondisabled cohort but there was no significant group effect (P=.09, data not shown). Figure 3 illustrates the submaximal ventilatory equivalents for oxygen for both groups through minute 6. There were significant differences between the nondisabled and TBI groups (group effect, P=.002). Subsequent pairwise comparisons revealed significant differences after the second minute of exercise. In addition, there was a significant interaction between group and time of exercise (P=.014). Subjects with TBI tended to have higher submaximal heart rates than nondisabled subjects in the first 6 minutes of walking but there was no significant group effect (P=.16, data not shown). Only until late in the test did the nondisabled subjects start to attain higher heart rates consistent with their higher peak heart rate (see table 2). Figure 4 illustrates the submaximal oxygen pulse for the 2 groups. Again, there were significant differences between the 2 groups after minute 2 (group effect, P=.006). Discussion Before this study, there had been no direct comparisons of cardiopulmonary fitness of a healthy population with that of people recovering from TBI who had few, if any, physical impairments. We found significant differences in several variables related to cardiorespiratory fitness. Our results indicate that patients recovering from TBI have cardiovascular and pulmonary limitations in endurance activities. One of the more surprising differences between the groups was the peak heart rate response. We found that all nondisabled subjects attained greater than 90% of age-predicted maximum heart rate but only 8 of 13 patients recovering from TBI achieved this level. This fact, combined with the lower oxygen pulses (see Fig 1, Fig 4), suggests a limitation in exercise cardiac output. We also found pulmonary limitations to peak endurance activity. A study by Becker et al11 found the submaximal V̇e/V̇o2 to be 30% higher in people with TBI than in nondisabled subjects. We found differences on the same order for most minutes of submaximal exercise. Peak values for the 2 groups in our study, however, did not differ due to the relative differences in Vo2peak and Ve (76% of TBI and 68% of normative values, respectively). The higher submaximal V̇e/V̇o2 (see fig 3) indicates that breathing is less efficient and people with TBI must breathe harder during physical activity to exchange a given volume of oxygen. Becker’s group also found oxygen pulse to be approximately 35% lower in patients with TBI at peak exercise, a finding similar to ours. Balke and Ware16 studied the work capacity of male Air Force personnel and rated it as a function of Vo2peak and test duration. According to their study, subjects were rated “very poor” if their oxygen uptake was 25 to 30mL·kg−1·min−1. A Vo2peak of less than 25mL·kg−1·min−1 was considered an “inferior” level of fitness. In our sample, 9 of 12 men with TBI fell into 1 or the other of these 2 “most unfit” classifications. The average for the nondisabled men (35.3mL·kg−1·min−1) would be rated as borderline “fair,” a rating given to people whose oxygen uptake is 35 to 40mL·kg−1·min−1.16 Because our protocol is a modification of the Balke-Ware protocol, we assume that comparisons are reasonably valid. We have, however, modified the protocol; speed is gradually increased to 3.3mph in the first 2 minutes and the incline increases 2% every minute instead of the 1% used by Balke and Ware. In another study of healthy subjects,21 untrained men had Vo2peak that approximated 44mL·kg−1·min−1 and untrained women had Vo2peak of approximately 39mL·kg−1·min−1. For our subjects without disability, on average the 12 men and 1 woman consumed 20% and 7% less oxygen at peak work, respectively. The 12 men and 1 woman with TBI consumed 39% and 28% less oxygen at peak work, respectively. Because the details of the testing protocol used in the untrained subjects were not provided by Saltin and Åstrand,21 comparisons should be made with caution. Using a different data set for normative values, peak aerobic capacity for all patients with TBI was less than or equal to the 5th percentile when compared with the age- and sex-matched healthy subjects.22 In those subjects, peak aerobic capacity ranged from the 5th to the 75th percentile; the median was the 10th percentile. Even greater caution should be taken if these normative values are used for comparison because peak aerobic capacity is estimated based on heart rate responses to submaximal “stepping” activity. From Pollock and Wilmore22 and the other previously cited studies cited confirm that our nondisabled cohort was comprised of sedentary people not undergoing endurance training. Moreover, it further supports our finding that our subjects with TBI had an aerobic capacity that was 76% of the healthy age- and sex-matched comparison group when an identical testing protocol was used. Our results are supported by other indirect comparisons in which patients with TBI approximated only 67%6 and 74%9 of age-predicted maximal V̇o2 during treadmill testing and 65% during cycle ergometry.10 There are probably many factors that contribute to the lower physical work capacity in patients recovering from TBI that have few, if any, physical impairments. The lack of activity is most likely the major contributor. This can result from a lack of motivation and other cognitive deficits, and from a lack of effective education and attention given by rehabilitation professionals to the issue of cardiorespiratory fitness as a key component of both physical health and mental health. Other factors that probably play a role are the indirect effects of certain medications and subtle balance impairments that make unsupervised high intensity training unsafe. More formal investigative work is necessary to know with certainty the reasons for decreased cardiorespiratory fitness. We found a significant inverse relation between age and peak aerobic capacity in the patients recovering from TBI (see table 3). In the nondisabled subjects, however, the age relationship is much weaker, probably because of the lower variability in Vo2peak (see fig 1). The data for patients recovering from TBI only weakly suggest that the longer the time since injury, the greater the peak aerobic capacity. This was somewhat surprising, but still encouraging, in that it supports the notion that endurance levels can increase over time with a resumption of physical activity. Because of the significant differences related to both submaximal and peak cardiorespiratory fitness, however, patients should be encouraged to engage in more formal, properly prescribed endurance training programs. Decreased cardiorespiratory fitness leads to increased fatigability, thus hindering one’s ability to perform a work task. Fatigue is a common complaint among people who have a TBI7, 8 and endurance training has the potential to delay the onset of fatigue. Therefore, aerobic training should be a component of all rehabilitation programs so that TBI patients can increase their work levels during various endurance tasks and hasten their rehabilitation. Data have been published that suggest that aerobic training reduces fatigability and may be essential in the vocational rehabilitation and placement of people with TBI.6 Endurance training programs may play an important role in preparing TBI patients to better handle the sustained work demands occasioned by being employed. Physical conditioning programs have been advocated for many years for patients recovering from TBI.23 Studies that examined changes in physical work capacity have shown that cardiorespiratory variables improved significantly in TBI with regular aerobic training.6, 17, 24, 25, 26 In addition, there is some indication that TBI patients who exercise have fewer emotional challenges.27, 28, 29 One can speculate that increased endurance capacity could result in greater motivation to participate in recreational activities and could facilitate increased levels of community integration. Study Limitations A limitation of our study is that we used samples of convenience for both TBI patients and the nondisabled. The nondisabled cohort consisted of faculty, staff, and students from a local university and staff and students from the residential treatment center and may not have been representative of the healthy population in the community. The majority of our 13 patients had severe injuries but no significant residual physical impairments. Other patients with TBI with only moderate to mild injuries and with minimal or no physical impairments should be studied. Any future comparisons of nondisabled and TBI subjects require direct measurements using identical testing protocols. Testing and training protocols should be designed around the abilities of the individual, with the disability as the key focus. When measurements of peak physical work capacity cannot be made, submaximal responses should be compared. Habitual exercise has an important role in the overall health and well being of people with and without disabilities. The effects of exercise and physical activity in the prevention of cardiovascular disease,30 certain cancers,31 hypertension,32 and osteoporosis33 are well established and support a holistic approach to treatment after TBI. Given the cognitive impairments that often accompany TBI, evidence suggesting that increased physical activity can have beneficial effects on cognitive function in healthy people as well as in clinical populations (eg, depression, elderly with dementia, cardiopulmonary obstructive disorders)34, 35 argue for a rigorous examination of the effects of exercise and physical activity across the continuum of TBI rehabilitation. Conclusions Aerobic fitness is severely limited in patients recovering from TBI who have few, if any, other physical impairments. Our results point to limitations at both cardiac and pulmonary organ system levels. More than likely there is also a limitation in oxygen extraction by the active skeletal muscle, but this needs further study. Patients recovering from the sequelae of TBI who have no musculoskeletal impairments that preclude participation in cardiorespiratory training programs should be encouraged to do so. Longitudinal studies are necessary to determine if these training activities will mitigate the chronic fatigue experienced by a majority of these patients and prevent secondary disability resulting from a sedentary lifestyle. Suppliers Acknowledgments We thank Charlie Milton, MS, PT, for his support in recruiting subjects and Julie Norcross for her expert technical assistance. References 1. 1CDC, National Center for Injury Prevention and Control. Traumatic brain injury. Available at: http://www.cdc.gov/ncipc/factsheets/tbi.htm. Accessed November 29, 2006. 2. 2Booth F, Gordon S, Carlson C, Hamilton M. Waging war on modern chronic diseases: primary prevention through exercise biology. J Appl Physiol. 2000;88:774–787. 3. 3Chakravarthy M, Booth F. Exercise. Philadelphia: Hanley & Belfus; 2003;. 4. 4Pate R, Pratt M, Blair S, et al. Physical activity and public health: a recommendation from the Centers for Disease Control and Prevention and the American College of Sports Medicine. JAMA. 1995;273:402–407. MEDLINE 5. 5Kinne S, Patrick D, Doyle D. Prevalence of secondary conditions among people with disabilities. Am J Public Health. 2004;94:443–445. MEDLINE |
CrossRef
6. 6Jankowski L, Sullivan S. Aerobic and neuromuscular training: effect on the capacity, efficiency, and fatigability of patients with traumatic brain injuries. Arch Phys Med Rehabil. 1990;71:500–504. MEDLINE 7. 7Hillier S, Sharpe M, Metzer J. Outcomes 5 years post-traumatic brain injury (with further reference to neurophysical impairment and disability). Brain Inj. 1997;11:661–675. MEDLINE |
CrossRef
8. 8Borgaro S, Baker J, Wethe J, Prigatano G, Kwasnica C. Subjective reports of fatigue during early recovery from traumatic brain injury. J Head Trauma Rehabil. 2005;20:416–425. MEDLINE |
CrossRef
9. 9Hunter M, Tomberlin J, Kirkikis C, Kuna S. Progressive exercise testing in closed head-injured subjects: comparison of exercise apparatus in assessment of a physical conditioning program. Phys Ther. 1990;70:363–371. MEDLINE 10. 10Bhambhani Y, Rowland G, Farag M. Reliability of peak cardiorespiratory responses in patients with moderate to severe traumatic brain injury. Arch Phys Med Rehabil. 2003;84:1629–1636. Abstract | Full Text |
Full-Text PDF (194 KB)
|
CrossRef
11. 11Becker E, Bar-Or O, Mendelson L, Najenson T. Pulmonary functions and responses to exercise of patients following cranio cerebral injury. Scand J Rehabil Med. 1978;10:47–50. MEDLINE 12. 12Taylor H, Buskirk E, Henschel A. Maximal oxygen intake as an objective measure of cardio-respiratory performance. J Appl Physiol. 1955;8:73–80. 13. 13Hermansen L, Saltin B. Oxygen uptake during maximal treadmill and bicycle exercise. J Appl Physiol. 1969;26:31–37. 14. 14Pollock ML, Bohannon RL, Cooper KH, et al. A comparative analysis of four protocols for maximal treadmill stress testing. Am Heart J. 1976;92:39–46. MEDLINE |
CrossRef
15. 15Lukaski H, Bolonchuk W, Klevay L. Comparison of metabolic responses and oxygen cost during maximal exercise using three treadmill protocols. J Sports Med. 1989;29:223–229. 16. 16Balke B, Ware R. An experimental study of “physical fitness” of Air Force personnel. US Armed Forces Med J. 1959;10:675–688. 17. 17Mossberg K, Kuna S, Masel B. Ambulatory efficiency in persons with acquired brain injury after a rehabilitation intervention. Brain Inj. 2002;16:789–797. MEDLINE |
CrossRef
18. 18Mossberg K, Greene B. Reliability of graded exercise testing after traumatic train injury: submaximal and peak responses. Am J Phys Med Rehabil. 2005;84:492–500. MEDLINE |
CrossRef
19. 19In: Whaley M editors. ACSM’s guidelines for exercise testing and prescription. 7th ed.. Philadelphia: Lippincott Williams & Wilkins; 2006;. 20. 20Åstrand P, Rodahl K, Dahl H, Stromme S. Textbook of work physiology: physiological basis of exercise. 4th ed.. Champaign: Human Kinetics; 2003;. 21. 21Saltin B, Åstrand P. Maximal oxygen uptake in athletes. J Appl Physiol. 1967;23:353–358. 22. 22Pollock M, Wilmore J. Exercise in health and disease. 2nd ed.. Philadelphia: WB Saunders; 1990;. 23. 23Sullivan S, Richer E, Laurent F. The role and possibilities for physical conditioning programmes in the rehabilitation of traumatically brain-injured persons. Brain Inj. 1990;4:407–414. MEDLINE |
CrossRef
24. 24Kinney-LaPier T, Sirotnak N, Alexander K. Aerobic exercise for a patient with chronic multisystem impairments. Phys Ther. 1998;78:417–424. MEDLINE 25. 25Bateman A, Culpan F, Pickering A, Powell J, Scott O, Greenwood R. The effect of aerobic training on rehabilitation outcomes after recent severe brain injury: a randomized controlled evaluation. Arch Phys Med Rehabil. 2001;82:174–182. Abstract | Full Text |
Full-Text PDF (84 KB)
|
CrossRef
26. 26Bhambhani Y, Rowland G, Farag M. Effects of circuit training on body composition and peak cardiorespiratory responses in patients with moderate to severe traumatic brain injury. Arch Phys Med Rehabil. 2005;86:268–276. Abstract | Full Text |
Full-Text PDF (208 KB)
|
CrossRef
27. 27Moran A. Six cases of severe head injury treated by exercise in addition to other therapies. Med J Aust. 1976;1:396–397. 28. 28Moran A. Problems of a head-injured patient. Med J Aust. 1972;2:782–783. 29. 29Gordon W, Sliwinski M, Echo J, McLoughlin M, Sheerer M, Meili T. The benefits of exercise in individuals with traumatic brain injury: a retrospective study. J Head Trauma Rehabil. 1998;13:58–67. MEDLINE |
CrossRef
30. 30Thompson P, Buchner D, Pina I, et al. Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease: a statement from the Council on Clinical Cardiology (Subcommittee on Exercise, Rehabilitation, and Prevention) and the Council on Nutrition, Physical Activity, and Metabolism (Subcommittee on Physical Activity). Circulation. 2003;107:3109–3116.
CrossRef
31. 31McTiernan A. Physical activity after cancer: physiologic outcomes. Cancer Invest. 2004;22:68–81. MEDLINE |
CrossRef
32. 32The Sixth Report of the Joint National Committee on the Prevention, Detection and Treatment of High Blood Pressure. Washington (DC): Government Printing Office; 1997;. 33. 33Taaffe D, Marcus R. Musculoskeletal health and the older adult. J Rehabil Res Dev. 2000;37:245–254. MEDLINE 34. 34Etnier J, Salazar W, Landers D, Petruzzello S, Ham M, Nowell P. The influence of physical fitness and exercise upon cognitive functioning: a meta-analysis. J Sports Exerc Psychol. 1997;19:249–277. 35. 35Colcombe S, Kramer A. Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci. 2003;14:125–130. MEDLINE |
CrossRef
a Department of Physical Therapy, University of Texas Medical Branch, Galveston, TX b Transitional Learning Center, Galveston, TX.  Correspondence to Kurt A. Mossberg, PhD, PT, Dept of Physical Therapy, University of Texas Medical Branch, 301 University Blvd, Galveston, TX 77555-1144
Supported in part by the Moody Foundation and the National Institutes of Health (grant no. R01 HD046570). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Reprints are not available from the author. PII: S0003-9993(06)01556-5 doi:10.1016/j.apmr.2006.12.006 © 2007 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
|
FULL TEXT01556-5/journalimage?img=PIIS0003999306015565.gr1.lrg.gif&fig=fig1&kwhquery=&issn=0003-9993&ishighres=false&allhighres=false&free=yes','journalimage');)
01556-5/journalimage?img=PIIS0003999306015565.gr2.lrg.gif&fig=fig2&kwhquery=&issn=0003-9993&ishighres=false&allhighres=false&free=yes','journalimage');)
01556-5/journalimage?img=PIIS0003999306015565.gr3.lrg.gif&fig=fig3&kwhquery=&issn=0003-9993&ishighres=false&allhighres=false&free=yes','journalimage');)
01556-5/journalimage?img=PIIS0003999306015565.gr4.lrg.gif&fig=fig4&kwhquery=&issn=0003-9993&ishighres=false&allhighres=false&free=yes','journalimage');)