PHYS THER
Vol. 88, No. 1, January 2008, pp. 77-87
DOI: 10.2522/ptj.20070022
Cardiorespiratory Capacity After Weight-Supported Treadmill Training in Patients With Traumatic Brain Injury
Kurt A Mossberg,
Evelyne E Orlander and
Julie L Norcross
KA Mossberg, PT, PhD, is Professor, Department of Physical Therapy, School of Allied Health Sciences, University of Texas Medical Branch, 301 University Blvd, Galveston, TX 77555-1144 (USA)
EE Orlander, PT, MPT, is Research Assistant, Department of Physical Therapy, School of Allied Health Sciences, University of Texas Medical Branch
JL Norcross, BS, is Research Assistant, Department of Physical Therapy, School of Allied Health Sciences, University of Texas Medical Branch
Address all correspondence to Dr Mossberg at: kmossber{at}utmb.edu
Submitted January 18, 2007;
Accepted August 7, 2007
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Abstract
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Background and Purpose: The primary goal of body-weight–supported treadmill training (BWSTT) has been to improve the temporal and spatial characteristics of unsupported overground walking; however, little attention has been given to cardiorespiratory adaptations. The purpose of this case report is to describe the effects of BWSTT on cardiorespiratory fitness in 2 patients recovering from severe traumatic brain injury (TBI).
Case Description: Both patients were involved in motor vehicle accidents and were studied after admission to a postacute residential treatment program. Patient 1 was a 25-year-old man (initial Glasgow Coma Scale [GCS] score=3) who began observation and treatment 3 months after the injury. Patient 2 was an 18-year-old woman (initial GCS=6) who began observation and treatment 1 year after the injury.
Outcomes: Each patient received 2 to 3 sessions of BWSTT per week. Aerobic capacity was measured while they ambulated on a treadmill without body-weight support before and after BWSTT. Both patients' submaximal and peak responses improved. For patient 1 and patient 2, total treadmill work performed increased 134% and 53%, respectively. Peak oxygen uptake increased 24% for patient 1 and 16% for patient 2. Estimated cardiac stroke volume (oxygen pulse) increased 32% and 26% for patient 1 and patient 2, respectively.
Discussion: The observations made on these 2 patients suggest that BWSTT has the potential to favorably change cardiorespiratory capacity after TBI.
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Introduction
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Body-weight–supported treadmill training (BWSTT) has been studied extensively in patients with spinal cord injury (SCI)1,2 and stroke.3–5 The patients train on a treadmill while having a harness system partially support their body weight. Very little research has been done on the effectiveness of BWSTT in patients recovering from traumatic brain injury (TBI). Two case reports describing changes in 4 patients were published initially,6,7 and more recently a controlled trial comparing BWSTT to conventional overground walking has been reported.8 The primary goal of BWSTT has been to improve the temporal and spatial characteristics of unsupported overground walking.
The effect of BWSTT on the cardiovascular and respiratory systems has received little attention. The majority of studies have only described the acute responses to varying levels of weight support and treadmill speeds. Danielsson and Sunnerhagen9 and David and colleagues10 compared acute responses of patients with stroke and individuals who were healthy. Physiologic responses to BWSTT were studied in one patient with SCI,11 and this form of treatment has been combined with neuromuscular electrical stimulation in subjects with complete and incomplete tetraplegia.12 Most recently, a study comparing the metabolic costs of robotic- versus therapist-assisted BWSTT was reported.13
In contrast to the study of acute responses, less attention has been paid to the long-term physiologic adaptations that result from several weeks of BWSTT. Positive changes were reported in sympathetic regulation of the cardiovascular system after 6 months of BWSTT in 8 individuals with C4–5 incomplete tetraplegia.14 This same research group found improved vascular elasticity in 6 people with motor complete SCI after 4 months of BWSTT.15 In another study,16 results from 6 patients with SCI and 1 patient with "cranial trauma" suggest an improvement in the energy and cardiac costs of ambulation after 4 to 7 weeks of BWSTT. In the study by Gazzani et al,16 however, graded exercise testing was not performed, and consequently no assessment was made of peak cardiorespiratory fitness before or after training. Furthermore, that study provided little description of the patient with brain injury other than age (61 years) and time since injury (37 years).
Given the paucity of information regarding the long-term physiologic adaptations to BWSTT in general and in patients with TBI specifically, the purpose of this case report was to describe the effects of BWSTT on cardiorespiratory fitness in 2 patients during postacute recovery from traumatic brain injury (TBI). We expected that BWSTT would change peak oxygen uptake (
O2) and other variables consistent with a positive change in aerobic capacity. We based this expectation on the premise that BWSTT would allow for a greater intensity of training than conventional overground walking with manual and mechanical assistance.
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Patient Histories and Reviews of Systems
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Two patients admitted to a postacute residential treatment center for brain injury gave written informed consent to receive the intervention. Committees for the Protection of Human Subjects at both the residential treatment center and the University of Texas Medical Branch approved the procedures. All Health Information Portability and Accessibility Act guidelines were followed. Both patients were involved in motor vehicle accidents and had no significant medical histories prior to their accidents. Neither patient reported participating in a regular cardiorespiratory fitness program, and both patients, therefore, were considered essentially sedentary prior to and after their accidents. Neither patient reported a smoking history.
Patient 1 was a 25-year-old man who was admitted 3 months after his accident and had an immediate postinjury Glasgow Coma Scale (GCS) score of 3 at the accident scene. Initial imaging studies of the brain revealed a contusion and shear injury of the corpus callosum, increased image intensity in the left temporal region, and a subarachnoid hemorrhage. Patient 2 was an 18-year-old woman who was admitted 1 year after her accident and had an immediate postinjury GCS score of 6 in the emergency department. Initial imaging studies revealed cerebral contusions, intraventricular hemorrhage, and brain-stem contusion.
Besides the initial imaging studies of the brain, further review of the patients’ neurological system revealed residual impairments. Both patients had depression (patient 1 was prescribed trazodone, patient 2 was prescribed fluoxetine and imipramine). In addition, patient 2 was taking propranolol for migraine prophylaxis and divalproex for seizure control. Cognitive screening of patient 1 revealed mild impairment in mathematical calculations and verbal reasoning and moderate to severe impairment in visual constructional skills and verbal/auditory memory. Cognitive screening of patient 2 revealed below-average performance in the naming of simple objects and below-average performance in mathematical calculations. Patient 2 often demonstrated inappropriate social skills, had a low tolerance of other people, and required constant cueing to stay focused on tasks. Both patients could follow 2-step commands.
Review of the musculoskeletal system in both patients revealed mild (3+/5 to 4/5) deficits in muscle force production across multiple joints and limitations in range of motion (most notably in active ankle dorsiflexion). Patient 1 experienced intermittent moderate knee pain when moving from a sitting to a standing position or from a standing to a sitting position and when climbing or descending stairs and was prescribed a combination of indomethacin and tramadol.
Reviews of the cardiovascular and integumentary systems were unremarkable in both patients. Regarding the pulmonary system, the only thing notable was that patient 2 exhibited occasional asthmatic symptoms, which were treated with an albuterol inhaler, as necessary. In addition, both patients were prescribed antihistamines (cetirizine for patient 1 and fexofenadine for patient 2). Lastly, patient 1 had a body mass index (BMI) of 33.6, putting him in the "obese" category. Patient 2 had a BMI of 24.9, putting her in the "healthy" category.
Clinical Impression
Both patients had characteristics typical of the individual recovering from TBI and were considered good candidates to receive the examination and intervention procedures. Each patient had cognitive impairments but was considered above the minimal requirements needed to perform each of the physical examination procedures reliably. Because of the nature of the injury, further specific tests that integrated all of the major systems were necessary (see "Examination" section). These tests included measures of balance, gait speed, and endurance. Both patients were capable of ambulating overground without manual assistance at a self-selected speed that consequently allowed for measurements of their gait speed and endurance.
Because both patients were essentially sedentary and had a TBI with residual neuromusculoskeletal impairments, we were interested in a more detailed assessment of their endurance levels. Neither patient exhibited overt cardiovascular, neuromuscular, or musculoskeletal pathology that would have prevented them from performing a peak aerobic capacity test or from participating in a vigorous exercise program. The only concern was possible exercise-induced asthma in patient 2. We always ensured that the patient had her inhaler in her possession when participating in the examination and intervention procedures.
The primary outcome measures were submaximal and peak cardiorespiratory capacity. According to the American College of Sports Medicine's risk stratification guidelines,17 patient 1's age, BMI, and sedentary lifestyle put him in the "moderate risk" category for maximal aerobic capacity testing; patient 2 was considered "low risk." Regardless of the risk category, the medical director of the facility was always in close proximity during the maximal exercise tests.
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Examination
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Aerobic capacity was measured while the patients ambulated on a treadmill without body-weight support before and after BWSTT. Maximal safe speeds for testing peak aerobic capacity prior to the intervention were 40.2 m/min (1.5 mph) and 21.5 m/min (0.8 mph) for patient 1 and patient 2, respectively. Indicators of maximal aerobic capacity included (1) reaching 85% to 90% of the patient's age-predicted maximum heart rate (HR), (2) a plateau in O2 with an increase in workload, and (3) a respiratory exchange ratio (RER) equal to or greater than 1.15.17 More importantly, the test was stopped if the patient's safety became compromised. The speed used during post-BWSTT testing was identical to the pre-BWSTT speed. Because the treadmill incline was limited to 25%, if the patient was capable of ambulating at 25% for 2 minutes and had not reached the indicators, speed was increased 2.68 m/min (0.1 mph) each minute until peak workload was attained or safety was compromised.
During graded exercise testing, the 2 patients had their resting and exercise HR monitored by electrocardiography.* At no time during the pre-BWSTT or post-BWSTT testing were arrhythmias noted on the electrocardiogram. Minute ventilation (E), O2, carbon dioxide production (CO2) during rest and exercise were determined by a metabolic cart.
Details of the procedure are presented elsewhere,18 and the reliability of submaximal and peak responses in patients recovering from TBI have been reported.19 Work rate (kg·m/min) was calculated by taking into account body weight, speed, and incline of the treadmill during each minute of ambulation. Total work (kg·m) was the sum of all minutes of ambulation.
In addition, balance was assessed using the Berg Balance Scale score.20 Gait impairments required both patients to use assistive devices for ambulation. Gait speed and estimated energy cost of overground ambulation were determined by the 6-minute walk (6MW). Details of the procedure, typical values for patients with TBI, and reliability in patients with TBI have been reported previously.21 Each patient used his or her respective assistive devices to perform the 6MW.
Clinical Impression
Results of aerobic testing indicated that both patients were well below the 10th percentile for peak O2 in age- and sex-matched individuals without impairments.22,23 This finding was not surprising given their respective histories and gait impairments. Moderate to severe balance deficiencies were apparent from the Berg Balance Scale scores. Slow gait speeds and decreased endurance were evident from the results of the 6MW. Both patients complained of fatigue toward the end of the test, and patient 2's safety became compromised. This was accompanied by verbal expressions of frustration and intolerance for the activity.
These findings led to the conclusion that BWSTT would be an appropriate intervention to improve endurance, cardiorespiratory capacity, and the ability to walk unsupported overground. The body-weight support accommodated the weakness and balance impairments. In addition, it allowed staff to concentrate on gait quality rather than body-weight support. The treadmill provided the higher frequency of stepping and consequently could improve endurance and cardiorespiratory capacity, provided the stimulus was the proper intensity.
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Intervention
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For training purposes, the unloading system consisted of a harness system suspended over a treadmill (LiteGait).
The unloading system also had a pair of handles that the patients could use as necessary to facilitate balance and control of the center of gravity. Heart rate during training was monitored via telemetry (Polar Vantage XL heart rate monitor).
Treatment consisted of 2 to 3 sessions of BWSTT per week. Patient 1 trained for 11 weeks (30 sessions), and patient 2 trained for 15 weeks (38 sessions). Treatment progression consisted of increasing the duration of walking, increasing the speed of the treadmill, and decreasing the partial body-weight support. For patient 1, the percentage of body weight supported ranged between 10% and 15% in the initial phase of treatment, down to 0% in the last phase of treatment. For patient 2, the percentage of body weight supported ranged between 30% and 50% in the initial phase of treatment and decreased to 10% to 15% in the later phase of treatment. The emphasis was on maintaining as normal a gait pattern as possible while training at speeds greater than self-selected overground speeds. Patient 1 did not require manual assistance to move his lower extremities or weight shift. Patient 2 required the assistance of one clinician to manually facilitate swing phase and heel-strike of the right lower extremity during training. All training occurred at the 0% incline.
During BWSTT, HRs ranged between 60% and 85% of age-predicted maximums (220–age) for patient 1. Figure 1 contrasts the heart rate responses during an early and late treatment session in patient 1, who trained for 11 weeks. During each training session, HR during most minutes of ambulation was above the 60% of age-predicted maximum threshold recommended to bring about a cardiorespiratory training effect.17 On average, training intensity occurred at the low end of the target HR zone. Speed and duration of ambulation increased over time.
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Figure 1. Comparison of heart rate responses for patient 1 (P1) during an early session (session 5) and late session (session 30) of body-weight–supported treadmill training (BWSTT). Target heart rate, which was 60%–85% of patient 1's age-predicted maximum, was equal to 117–166 bpm. During session 5, unloading was approximately 10% of body weight, and, during session 30, unloading was 0%. Treadmill speed (m/min) is indicated by arrow sets parallel to the x-axis (session 5=upper arrow set, broken lines; session 30=lower arrow set, solid lines). R=rest or recovery.
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During the early training session (session 5), treadmill speed started at 45.6 m/min (1.7 mph) for 4 minutes and was increased to 50.9 m/min (1.9 mph) for the next 6 minutes. Patient 1 rested for 2 minutes and resumed walking at 50.9 m/min (1.9 mph) for the last 5 minutes of the session before resting. During the last training session (session 30), treadmill speed started at 48.3 m/min (1.8 mph) for 4 minutes, was increased to 53.6 m/min (2.0 mph) for the next 3 minutes, and increased again to 59.0 m/min (2.2 mph) for the remaining 13 minutes of the bout. He rested for 2 minutes and began a second bout at 59.0 m/min (2.2 mph) for an additional 9 minutes, followed by 1 minute of "cool-down" at 42.9 m/min (1.6 mph) before resting.
A similar training pattern was observed for patient 2, who trained for a total of 38 sessions over 15 weeks. However, HR response was not a valid indicator of exercise intensity due to the administration of propranolol; training HR never exceeded 100 bpm (50% of age-predicted maximum). Although speed and duration for patient 2 increased over time, it changed in a very irregular pattern due to inconsistencies in patient tolerance and difficulty with attention to the task and anger and frustration over her inability to "walk normal again." In addition, our experience using ratings of perceived exertion has proven to be an unreliable measure of intensity when exercising patients with TBI. This was a limiting factor in monitoring her treatment response. These issues are not unusual when treating patients recovering from TBI. As a result, more emphasis was placed on decreasing body-weight support during the 15-week intervention. At no time did patient 2 require albuterol for exercise-induced asthma.
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Outcome
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Table 1 details the peak cardiorespiratory capacity values for patient 1 and patient 2 before and after BWSTT. Total work performed during the entire test is shown as the sum of all minutes the patients walked. Patient 1's total work increased 134%, and patient 2's total work increased 53% after training compared with total work before training. As expected, peak HR did not change in either patient. Patient 1 reached approximately 88% and 87% of age-predicted maximum HR on his pre-BWSTT test and postBWSTT test, respectively. Patient 2 achieved peak HRs of 56% and 52% of her age-predicted maximum on her pre-BWSTT and post-BWSTT tests, respectively. Peak O2 increased 24% and 16% in patient 1 and patient 2, respectively. Upon examination of breath-by-breath data, there was an indication that O2 leveled off with an increase in workload during the pre-BWSTT tests for both patients. This same leveling off was not observed during either of the post-BWSTT tests. Peak oxygen pulse increased 32% and 26% in patient 1 and patient 2, respectively. The peak E increased 37% for patient 1; however, E for patient 2 decreased 12%. This also coincided with safety concerns and her desire to stop the test. Neither patient attained an RER greater than 1.15 on either the pre-BWSTT or post-BWSTT tests, suggesting insufficient anaerobic metabolism to ensure that peak aerobic capacity was attained.
Analyses of submaximal responses were based on comparisons at 70% of each patient's pre-BWSTT peak O2. Seventy percent of baseline peak O2 equated to 12.0 mL/kg/min for patient 1 and 10.2 mL/kg/min for patient 2. Details are presented in Table 2. At a given level of O2 (70% of baseline peak O2), patient 1 increased his work performed 6%, whereas patient 2 was able to perform 36% more work after training (pre-BWSTT=113 kg·m/min versus post-BWSTT=154 kg·m/min). Figure 2 illustrates changes between pre-BWSTT and post-BWSTT O2.
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Table 2. Submaximal Responses at 70% Peak Oxygen Uptake for Each Patient Before and After Body-Weight–Supported Treadmill Training (BWSTT)a
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Figure 2. Oxygen uptake (O2) response versus work performed for each minute of graded exercise testing for patient 1 (P1) and patient 2 (P2) before and after body-weight–supported treadmill training (BWSTT).
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Submaximal HR after training was observed to be lower in both patients compared with submaximal HR before training (Fig. 3). Oxygen pulse responses also were compared before and after BWSTT (Fig. 4). Patient 1 demonstrated an increase after training compared with before training, whereas patient 2 showed virtually no change in her submaximal response. Submaximal E also decreased in both patients after training (Fig. 5). Lastly, changes in Berg Balance Scale scores, gait speed, endurance, and mobility aids are detailed in Table 3.
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Figure 3. Heart rate response versus oxygen uptake (O2) for each minute of graded exercise testing for patient 1 (P1) and patient 2 (P2) before and after body-weight–supported treadmill training (BWSTT).
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Figure 4. Oxygen pulse (O2 pulse) response versus oxygen uptake (O2) for each minute of graded exercise testing for patient 1 (P1) and patient 2 (P2) before and after body-weight–supported treadmill training (BWSTT).
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Discussion
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This is the first detailed report of peak and submaximal cardiorespiratory adaptations to BWSTT in patients recovering from TBI. The improvements in submaximal and peak responses demonstrated by both patients support our initial hypothesis. Although there were differences in how each individual changed after the training period, particularly during submaximal work, the differences observed were consistent with positive changes in cardiorespiratory capacity and efficiency of gait. These training effects took place even though training intensity occurred at the low end of the target HR zone for patient 1 and well below the target HR zone for patient 2 as a result of the negative chronotropic effects of propranolol.
Over the course of the BWSTT sessions, HR responses for patient 1 showed improvements indicative of a cardiovascular training effect. As shown in Figure 1, the training HRs were similar, but speed increased and the level of body-weight support decreased. In addition, the duration of each bout of walking increased, indicative of increased endurance. For patient 2, training HR did not reach levels typically prescribed for endurance training due to the administration of propranolol. The beta-blocker's negative effect on HR and contractility also may explain the lack of a training-induced increase in submaximal oxygen pulse (stroke volume) observed in patient 2 compared with patient 1 (Fig. 4). Her results are consistent with findings reported previously showing that a training effect, albeit blunted, can occur during nonselective beta-blocker administration.24,25 However, there was an increase in peak oxygen pulse of 26% for patient 2 that was likely due to the combination of an increase in peak O2 and the lower HR response during the post-BWSTT graded exercise test. For patient 2, the lower submaximal HR and O2 responses during the post-BWSTT test accounts for the lack of change in submaximal oxygen pulse. The lower HR and O2 are indicative of lower cardiac and energy costs and suggest improved gait efficiency. These submaximal changes were more apparent in patient 2 than in patient 1, probably due to the more pronounced initial gait impairment demonstrated by patient 2.
Our results are consistent with the only other study to examine the long-term training effects of BWSTT on the cardiorespiratory system.16 In all subjects studied by Gazzani et al,16 there were improvements noted in energy and cardiac costs of treadmill ambulation. Figure 1 illustrates this same decrease in cardiac cost in the first several minutes of ambulation. The cardiac costs are lower throughout session 30 in which the speed of ambulation is faster and the percentage of body-weight support is lower compared with session 5. It also can be seen in the decreased submaximal HR responses for both patients in Figure 3.
Previous studies26,27 have used the bicycle ergometer as the training modality to accommodate for the gait and balance impairments so often seen in patients with TBI. The concern for safety is a major issue, and, although each study showed improvements, the exercise interventions were not necessarily functional. Our results suggest that BWSTT provides the safety necessary for patients with greater impairments, is more functional, and can bring about improvements in cardiorespiratory capacity.
Although the results suggest that cardiorespiratory adaptations can occur as a result of BWSTT, there are some limitations to our treatment program. First, patient 1 began this intervention only 3 months after his injury, and some of the changes could have been due to spontaneous recovery. Another potential confounding factor is the unknown effects that antidepressants and the combinations of the other prescribed medications had on the patients’ exercise responses and adaptations. Reasons for stopping the maximal tests were more for patient safety than the patients reaching the endpoints for HR, O2, and RER levels, especially during the postBWSTT tests. Consequently, the magnitude of the differences in peak responses may be underestimated because there is greater uncertainty regarding each patient's attainment of their true peak aerobic capacity on the post-BWSTT test. However, perhaps what is most impressive is that both patients were able to attain greater workloads before safety concerns became an issue. It has been suggested that peak workload is a more valid indicator of change than peak physiologic response in patients with significant neurological impairments.28 Moreover, the issue of safety when testing individuals with neuromusculoskeletal impairments reinforces the importance of utilizing submaximal exercise responses as outcome measures.29
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Conclusions
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Neuromusculoskeletal and cognitive impairments after TBI create tremendous barriers to participation in regular physical activity, leading to a sedentary lifestyle and reduced cardiorespiratory fitness. Balance deficits and the inability to ambulate at intensities that bring about the physiologic adaptations necessary to prevent the diseases related to a sedentary lifestyle is a major rehabilitation challenge. Designing and implementing accessible options for patients with TBI who are unable to perform these activities is mandatory and a necessary part of a holistic treatment plan. Our results suggest that optimal intensity, frequency, and duration of BWSTT have the potential to increase cardiorespiratory capacity in patients recovering from TBI. In addition, gait speed increased, energy cost of walking decreased, and the use of assistive devices was reduced in the clinical facility and in the community. These 2 cases suggest that more in-depth examination of the findings be undertaken. As with patients with SCI and stroke, larger controlled studies should be performed to examine the effectiveness of BWSTT in patients recovering from TBI.
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Footnotes
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All authors provided writing. Dr Mossberg provided concept/idea/project design, fund procurement, and facilities/equipment. Ms Orlander and Ms Norcross provided data collection. Dr Mossberg and Ms Orlander provided data analysis. Dr Mossberg and Ms Norcross provided project management. The authors acknowledge Charlie Milton, PT, Brent Masel, MD, and all of the staff at the Transitional Learning Center in Galveston for their support.
An abstract describing a portion of this work was presented at the annual conference of the American Physical Therapy Association; June 21–24, 2006; Orlando, Fla.
This work was partially funded by the generous support of the Moody Foundation and National Institutes of Health grant R01 HD046570.
The procedures were approved by Committees for the Protection of Human Subjects at both the residential treatment center and University of Texas Medical Branch.
* Cardio Perfect Inc, 1870 The Exchange, Suite 150, Atlanta, GA 30339. 
Medical Graphics Corp, 350 Oak Grove Pkwy, St Paul, MN 55127-8599.
Mobility Research, PO Box 3141, Tempe, AZ 85280.
Polar CIC Inc, 99 Seaview Blvd, Port Washington, NY 11050.
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Introduction
Patient Histories and Reviews...
