CHRONIC OBSTRUCTIVE pulmonary disease increasingly

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1 1460 ORIGINAL ARTICLE Effect of Pulmonary Rehabilitation on Balance in Persons With Chronic Obstructive Pulmonary Disease Marla K. Beauchamp, MSc, PT, Sachi O Hoski, BSc, Roger S. Goldstein, MD, FRCP(C), FCCP, Dina Brooks, PT, PhD ABSTRACT. Beauchamp MK, O Hoski S, Goldstein RS, Brooks D. Effect of pulmonary rehabilitation on balance in persons with chronic obstructive pulmonary disease. Arch Phys Med Rehabil 2010;91: Objectives: To describe within-subject effects of pulmonary rehabilitation (PR) on balance in persons with chronic obstructive pulmonary disease (COPD) and to determine whether any observed changes in balance were associated with change in exercise tolerance or health-related quality of life. Design: Single-arm longitudinal study. Setting: Inpatient PR center. Participants: Subjects with COPD (N 29; mean SD age, y; forced expiratory volume in 1 second, 46.3% 22.3% predicted; 59% men [n 17]). Interventions: A standardized 6-week multidisciplinary PR program (exercise training, breathing exercises, education, and psychologic support). Main Outcome Measures: Balance was assessed using the Berg Balance Scale (BBS), Timed Up and Go (TUG) test, and the Activities-Specific Balance Confidence (ABC) scale. Exercise tolerance was determined from the 6-minute walk test (6MWT), and health-related quality of life from the Chronic Respiratory Questionnaire (CRQ). Results: Subjects showed small improvements in BBS ( points; P.001) and TUG ( s; P.003) scores, but not in ABC scores ( points; P.05). There was a weak relationship between change in BBS and change in CRQ scores (r.40; P.045) and no relationship with change in 6MWT. Conclusions: PR contributed to minor improvements in balance and had no effect on balance confidence in subjects with COPD. Further work is warranted to determine the optimal intervention for improving balance in this population. Key Words: Accidental falls; Postural balance; Pulmonary disease, chronic obstructive; Rehabilitation. From the Graduate Department of Rehabilitation Science (Beauchamp, Brooks), Department of Physical Therapy, University of Toronto (Brooks); and Department of Respiratory Medicine, West Park Healthcare Centre (Beauchamp, O Hoski, Goldstein, Brooks), Toronto, ON, Canada. Presented to the Ontario Thoracic Society/Ontario Respiratory Care Society, January 27 29, 2010, Toronto, Ontario, Canada and the Canadian Respiratory Health Professionals and Canadian Thoracic Society, April 29 May 1, 2010, Halifax, Nova Scotia, Canada. Supported by the Ontario Respiratory Care Society; a Canada Research Chair; Canadian Respiratory Health Professionals; the Canadian Institutes of Health Research; and the University of Toronto National Sanitarium Association Chair in Respiratory Rehabilitation Research. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Correspondence to Dina Brooks, PT, PhD, Associate Professor, Dept of Physical Therapy, University Ave, Toronto, Ontario M5G 1V7, Canada, dina.brooks@utoronto.ca. Reprints are not available from the author /10/ $36.00/0 doi: /j.apmr by the American Congress of Rehabilitation Medicine CHRONIC OBSTRUCTIVE pulmonary disease increasingly is recognized as a systemic disease associated with a broad array of physical functional limitations. 1,2 Impairments in peripheral muscle function, mobility, and exercise capacity are well established in these patients. 3-6 However, emerging evidence also suggests that older adults with COPD show important reductions in balance control that may be associated with an increased fall risk in this population. 7 Although information regarding postural control in persons with lung disease is limited, evidence suggests that balance deficits constitute an important secondary impairment in older adults with COPD. 2,7-9 Two studies have shown reduced balance performance and coordination in subjects with COPD compared with healthy controls. 2,8 One study examining the impact of fatigue on physiologic measures of postural sway found that patients with COPD showed impaired static postural control after a 6MWT in the absence of visual input (eyesclosed condition). 9 In addition, we recently reported that standard clinical balance measures discriminated between fallers and nonfallers with COPD, despite similar pulmonary function and 6MWT distances in the 2 groups. 7 The American Geriatrics Society recommends exercise with balance training as an essential component of a multifactorial falls intervention strategy for community-dwelling older adults who are at risk for falling. 10 Although the exercise component of PR is considered the cornerstone of rehabilitation for patients with COPD, it is directed predominately to training peripheral muscles. Balance training and fall prevention strategies are not included in international guidelines for PR, and very few programs include standardized balance assessment. 11 Although exercise can improve balance and decrease fall risk in older adults, interventions that include exercises to challenge balance have greater effects on fall risk and balance To date, no study has examined whether the exercise component of standard PR 11 might affect balance, even without targeted training. ABC BBS COPD CRQ FEV 1 MDC PR 6MWT TUG VO 2 peak List of Abbreviations Activities-Specific Balance Confidence Berg Balance Scale chronic obstructive pulmonary disease Chronic Respiratory Questionnaire forced expiratory volume in the first second of expiration minimal detectable change pulmonary rehabilitation six-minute walk test Timed Up and Go peak oxygen consumption

2 EFFECT OF PULMONARY REHABILITATION ON BALANCE, Beauchamp 1461 Table 1: Baseline Demographic and Functional Data for Study Subjects Variable The objectives of this study are to (1) describe within-subject effects of conventional PR on balance in people with COPD and (2) determine whether observed changes in balance are associated with change in exercise tolerance or health-related quality of life. METHODS Result Men/women 17/12 Supplemental oxygen 13 (45) Age (y) Body mass index (kg/m 2 ) FEV 1 (L) FEV 1 (% predicted) MRC dyspnea scale Median, 3; IQR, 3 6MWT distance (m) Gait aid use: rollator 8 (28) BBS score TUG score (s) ABC scale Fall history 12 (41) NOTE. (N 29). Values shown as n, mean SD, or n (%) unless otherwise indicated. Abbreviations: IQR, interquartile range; MRC, Medical Research Council. Participants Consecutive patients (N 38) enrolled in PR were approached for inclusion in the study; 5 did not meet eligibility criteria and 4 patients did not complete the 6-week PR program and were excluded. Therefore, 29 older adults with moderate to severe COPD (FEV 1, 46.3% 22.3% predicted; age, y; 59% men [n 17]) completed the study. Subject characteristics are listed in table 1. Patients were eligible to participate in this study if they met the following inclusion criteria: (1) physician diagnosis of COPD (FEV 1 80% predicted and FEV 1 /forced vital capacity 70% predicted) according to international guidelines, 15 (2) smoking history greater than 20 pack-years, and (3) ability to provide written informed consent. Patients with comorbid conditions likely to influence safety or balance were excluded. Specific exclusion criteria were (1) known cognitive impairment, (2) mechanical ventilation for all or part of the day, (3) neurologic or musculoskeletal condition that limited mobility, and (4) symptomatic cardiovascular disease. Data Collection Procedures After study approval by the local research ethics board, consecutive patients enrolled in a 6-week inpatient PR program at West Park Healthcare Centre (Toronto, Canada) between September and December 2009 were approached to attend a pre- and postrehabilitation assessment session. After obtaining informed consent, measurements of lung function at rest, height, weight, and use of supplementary oxygen were retrieved from the patient s medical chart. Results from assessments of exercise tolerance (6MWT) and health-related quality of life (CRQ) were obtained from the patient s treating physical therapist. All 5 treating physical therapists had received prior training for administration of the tests according to standardized guidelines. A questionnaire was used to establish the number of times each patient had fallen during the preceding 12 months, using the following standard definition: A fall would be when you find yourself suddenly on the ground, without intending to get there, after you were either in a lying, sitting, or standing position. 16 The Medical Research Council dyspnea scale was used to characterize patients with COPD in terms of functional limitation resulting from dyspnea. 17 The questionnaire includes 5 grades (statements), with higher grades indicating greater perceived respiratory disability. Patients are asked to select the statement that best describes their limitation. Balance testing and questionnaires were administered by the same registered physical therapist (M.K.B.) or kinesiologist (S.O.), in a quiet laboratory setting. At the time of the postrehabilitation assessment, raters were unaware of baseline test scores; all data were analyzed only upon study completion. The order of the tests was standardized for all subjects; balance tests were completed first, followed by questionnaires. If a patient required the use of a gait aid, the same gait aid was used in both assessments. Participants were encouraged to rest as needed throughout the assessment sessions. Intervention: PR The PR program consisted of a 6-week inpatient multidisciplinary program 18 consistent with clinical practice guidelines put forth by the American College of Chest Physicians. 11 The rehabilitation program had 4 main components: 1. Supervised endurance exercise training 4 to 5 times a week. After a baseline 6MWT, each patient received an individualized program based on 60% to 80% of the average speed achieved during the 6MWT (for treadmill exercise or walking) or 60% to 80% of the estimation of VO 2 peak from the 6MWT for bicycle training. Training emphasized intervaltype exercise; periods of high-intensity exercise were alternated with rest periods (ie, 3min at 80% VO 2 peak alternated with 2min of relative rest). Exercise duration was progressed until patients were able to tolerate 20 to 30 minutes of endurance exercise at the highest tolerated symptom level, after which the speed or intensity was increased by 10% to 20%. 2. Lower- and upper-extremity strength training 3 times a week. Muscles trained in the lower extremity included quadriceps, hamstrings, hip flexors, hip abductors, and hip extensors. Exercises were completed in sitting and standing positions with the use of ankle weights for resistance. Upper-extremity strength training included biceps, triceps, and deltoids using free weights, and pectoral muscles, using a resistance band. The amount of resistance provided was based on the patient s ability to complete 15 to 20 repetitions. Progression included increasing the resistance and number of sets from 1 set to 2 to 3 sets as tolerated. During both endurance and resistance training, patients were asked to rate their dyspnea and leg fatigue using a visual analog scale (Borg, 0 10) to monitor their exercise intensity Breathing exercises daily. Patients received a daily 30- minute class that included stretching of major muscle groups and instruction on diaphragmatic and pursed lip breathing. 4. Self-management education and psychological and social support were provided through lectures, relaxation classes, and recreational activities at least twice a week for 30 minutes. Measures The following measures were completed pre- and post-pr.

3 1462 EFFECT OF PULMONARY REHABILITATION ON BALANCE, Beauchamp Berg Balance Scale. The 14-item BBS 20 was chosen as the primary outcome in this study because it is the most widely accepted and psychometrically robust clinical measure of balance for older adults. 21 Activities such as transfers, reaching, turning around, and single-legged stance were graded on a scale ranging from 0 (unable/unsafe) to 4 (independent/efficient/safe), with higher scores indicating greater balance control. The measurement derived using the BBS has shown internal consistency, intra- and interrater reliability, content validity, construct validity, and predictive validity for determining fall risk in older adults. 22 A cutoff score of 46 and lower has been identified as a useful score to successfully identify those at risk for falling. 23,24 A change of 3.3 (or 4 points) has been suggested to represent an MDC in elderly patients with baseline BBS scores of 45 to 56 points. 25 MDC scores for subjects with lower baseline BBS scores range from 5 to 6 points for community-dwelling older adults. 25 TUG test. The TUG was used to provide a timed measure of balance and functional mobility in our patients. 26 The test requires the patient to rise from a standard armchair, walk 3m at a comfortable pace, walk back to the chair, and sit down. A practice trial was performed (not recorded) and individuals were permitted to use a gait aid if required. The TUG has high intra- and intertester reliability and predictive validity for falls in community-living adults. 22,26 A cutoff score of 16 seconds or more has predicted falls in community-dwelling elderly. 27 Reported MDC scores range from 4 seconds in patients with Alzheimer disease 28 to as high as 15 seconds in frail elderly patients. 29 ABC scale. The ABC scale requires patients to indicate their confidence in performing 16 activities without losing their balance or becoming unsteady on an 11-point scale (0% 100%). 30 Each item describes a specific activity that requires progressively increased balance control. Higher scores indicate higher balance confidence or less fear of falling. The ABC scale has good test-retest reliability, internal consistency, and predictive capacity for falls in older adults who reside in the community. 22,30 A change of 13% has been shown to reflect an MDC for this measure minute walk test. The 6MWT is a valid, responsive, interpretable, self-paced test that quantifies functional exercise capacity in terms of the distance walked in 6 minutes in patients with COPD. 32 The test was supervised by a physical therapist over a 30-m level straight course within an enclosed corridor according to the protocol described by the American Thoracic Society. 33 During each 6MWT, patients received standardized instructions and encouragement. Two tests were performed to account for possible improvements resulting from familiarization, with the greatest distance recorded. Each 6MWT was separated by a minimum of 30 minutes. The measurement properties of this test are well established in the COPD population. 33,34 The minimal clinically important difference for the 6MWT is 54m. 35 Chronic Respiratory Questionnaire. Health-related quality of life was measured using the individualized version of the CRQ. 36 The CRQ is a disease-specific instrument evaluating 4 domains that are considered important to people with chronic airflow limitation. Subjects are required to quantify events and experiences that have taken place during the 2-week period preceding administration of the questionnaire. It includes 20 questions in 4 domains: dyspnea, fatigue, emotional function, and mastery. The dyspnea domain is individualized by allowing patients to choose 5 activities that cause the greatest shortness of breath. The subject rates dyspnea on these selfselected activities during subsequent administrations of the CRQ. Answers are scored on a 7-point scale ranging from 1 (maximum impairment) to 7 (no impairment). The minimal clinically important difference for the CRQ is a change (improvement or deterioration) of.50 points. 37 The CRQ is valid, responsive, and interpretable when used for patients with COPD Statistical Analysis Statistical analyses were performed using SPSS (Statistical Package for Social Sciences). a It was determined that 28 patients were required to yield 80% power (.05) to detect a difference of 3 points or more in the BBS using a paired t test and SD of The assumption of normality was assessed by using frequency histograms and box plots, as well as statistical methods (Shapiro-Wilks test). The occurrence of heteroscedasticity (ie, when measurement error is dependent on the size of the measurement) was investigated graphically by plotting each subject s absolute difference in balance scores against their mean value and calculating the correlation coefficient. 39 For all analyses, P.05 is considered significant. Variables pre- and post-pr were compared using paired t tests for normally distributed data and the Wilcoxon signed-rank test for ordinal data. However, because statistical findings were similar for nonparametric and parametric tests and data were normally distributed, we report results of paired t tests and associated mean difference and 95% confidence intervals for each measure. Change in balance on the BBS was compared with previously reported MDC scores for this measure by using a simple scatter plot. Pearson correlations were conducted to examine the relationship between (1) change in balance and baseline BBS scores and (2) change in balance (BBS and TUG) and response to PR (change in 6MWT and CRQ scores). Data are expressed as mean SD unless otherwise stated. RESULTS Subjects Of 29 patients who completed the study, 12 (41%) reported at least 1 fall in the preceding year (table 1). Eight (67%) of the 12 fallers had a score at the 46-point cutoff or lower for risk for falls on the BBS; 6 fallers (50%) had a score at the 16-second cutoff or higher for the TUG. Overall, 11 patients (38%) achieved a score at the 6-point cutoff or lower for risk for falls on the BBS and a score at the 16-second cutoff or higher for the TUG. PR Outcomes Statistically significant improvements were found for the 6MWD (mean change, 52.5m; P.001), the CRQ dyspnea domain (mean change, 1.5 units; P.001), and total CRQ scores (mean change, 1.4 units; P.001) (table 2). Effect of PR on Balance A comparison of measures of clinical balance and balance confidence pre- and post-pr is provided in table 2. Although there was no significant improvement in balance confidence, performance on the BBS and TUG showed small but significant improvements after rehabilitation (mean change, 2.8 points; P.001; mean change, 1.5s; P.003, respectively). To facilitate understanding of the clinical importance of these changes, a plot of each subject s absolute difference in BBS scores against their mean score with MDC thresholds is shown in fig 1. No heteroscedasticity was found either graphically (see fig 1) or statistically (P.09). There was moderate correlation between baseline BBS score and change in balance (r.60; P.001).

4 EFFECT OF PULMONARY REHABILITATION ON BALANCE, Beauchamp 1463 Table 2: Effect of PR on Balance, Exercise Tolerance, and Health-Related Quality of Life Variable Pre-PR Post-PR Mean Change 95% Confidence Interval BBS score to 3.8 TUG score (s) to 0.5 ABC scale to MWT distance* (m) to 73.9 CRQ dyspnea* to 2.1 CRQ total* to 1.8 NOTE. Values shown as mean SD. Mean change and 95% confidence intervals associated with paired t tests are given for each measure. *6MWT and CRQ data reported for patients (n 27) for whom complete data pre- and post-pr were available. Relationship Between Change in Balance and Response to PR There were no relationships between change in balance and change in 6MWD or CRQ dyspnea scores. However, there was a weak relationship between change in BBS scores and change in overall CRQ scores (r.40; P.05). Fig 1. The differences between pre- and post-pr BBS scores plotted against their mean values with MDC thresholds with 95% confidence (MDC 95 ) for subjects with baseline scores of (A) 45 to 56 points (n 18) and (B) 35 to 44 points (n 9). MDC 95 values from Donoghue and Stokes. 25 Note that no heteroscedasticity was found either graphically or statistically (P>.09). DISCUSSION Although reductions in balance constitute an important secondary impairment in patients with COPD, 2,7-9 to our knowledge, this is the first study to report the effects of PR on measures of balance and fall risk in this population. Although measures of balance showed modest improvements after rehabilitation, the clinical relevance of these improvements is uncertain. In addition, balance confidence, an increasingly measured and targeted construct in fall prevention programs, did not improve after PR. These observations highlight the need for assessing both balance and fall risk in patients with COPD and evaluating the addition of balance training as part of PR. The small changes on the BBS and TUG (2.8 points and 1.5s, respectively) achieved by our patients are difficult to interpret in the absence of published minimal clinically important difference values. However, MDC scores have been reported for these measures in community-dwelling older adults and other populations with balance impairment. 25,28,31 The MDC is an estimate of the smallest change in score that is not caused by chance variation in measurement. It differs from the minimal clinically important difference, which is the smallest change considered important by a client or clinician, and thus introduces an element of subjectivity. 40 A recent investigation of elderly patients undergoing general physical rehabilitation found that the MDC for BBS scores depended on the patient s starting score. 25 For example, for individuals with starting scores of 45 to 56 points on the BBS, an improvement of 4 points is required to be 95% confident that the change was greater than measurement error; for individuals with a baseline BBS score of 35 to 44 points, the MDC is 5 points. In our sample, only 11 (38%) patients achieved an MDC based on their starting BBS score (see fig 1), and the change in TUG scores also did not approach the reported MDC values for this measure. 28,31 Therefore, less than half the sample achieved improvements in balance scores that could not be attributable to measurement error. Given that balance confidence also was unchanged after PR, it is very likely that for most patients, PR did not have a meaningful impact on balance or fall risk. In older adults, fear of falling is associated with an increased risk for falling, restriction of physical activities, and progressive loss of health-related quality of life A recent study of individuals with COPD showed that fear of falling is a pervasive problem associated with increased levels of anxiety and activity avoidance. 44 This is of particular concern given the importance of promoting physical activity in patients with COPD. 45 In the present study, PR did not have an effect on fear of falling, measured using the ABC scale. In light of the detrimental effects of fear of falling on physical function, interventions to target balance confidence are warranted in patients with COPD. Our observed baseline scores for measures of balance performance indicated that more than 1 in 3 subjects met the cutoff for an increased risk for falls, with 41% of our sample reporting at least 1 fall in the preceding year. Risk factors for falls in patients with COPD include lower-limb muscle weakness, impaired activities of daily living, and balance deficits. 46 Al-

5 1464 EFFECT OF PULMONARY REHABILITATION ON BALANCE, Beauchamp though current guidelines for PR recommend progressive resistance exercise for improving peripheral muscle strength in patients with COPD, 11 recent evidence suggests that strength training also may improve daily task performance, such as stair climbing and sit-to-stand in these patients. 47 This highlights the potential role of resistance exercise for improving balance and decreasing fall risk in this population. The relationship between muscle weakness and postural instability is well established in older adults; 48 it is probable that the small improvements in balance observed in this study were caused by the strength training component of PR, albeit of low intensity. However, higher intensity strength training (8 10 repetitions, 2 3 sets) combined with targeted balance training likely are required for exercise programs to have optimal effects on fall risk reduction and balance control. 13,14 Given the range of potential subcomponents that contribute to poor balance, the specific impairments that contribute to altered postural control need to be addressed. In this study, improvements in 6MWT and CRQ scores after PR were similar to results reported in a meta-analysis of PR. 49 This suggests that the small changes in balance scores were not attributable to an ineffective PR program, but more likely to the lack of specific exercises targeted to improve balance control. Changes in BBS scores correlated only weakly with improvements in the CRQ and were not associated with improvements in 6MWT distance. These results also emphasize the importance of using standardized clinical measures for assessing and monitoring changes in balance in persons with COPD. This was a single-arm longitudinal study, and although the within-subject comparisons are an obvious limitation, withholding rehabilitation for control purposes is no longer an option for patients referred for this intervention. Moreover, given that the measured changes were small and unlikely to be of clinical relevance, the absence of a control group does not detract from the validity of these observations. We did not target subjects with a high fall risk or impaired baseline balance scores; therefore, a possible ceiling effect on the BBS may have contributed to the lack of improvement after PR. However, because only 4 patients achieved a perfect starting score, this is unlikely to be the case. In addition, the negative correlation between baseline score and change in BBS score explained only 36% of the variance in this result. In future work, longer follow-up and inclusion of other measures, such as lower-extremity strength, will be necessary to understand changes in balance resulting from rehabilitation interventions. CONCLUSIONS PR was associated with minor changes in results of standard clinical tests of balance and had no effect on balance confidence in patients with COPD. Measures of exercise tolerance and health-related quality of life cannot be used as surrogate measures to derive balance information. These observations emphasize the value of including a balance assessment of patients with moderate and severe COPD, particularly if they have a history of falling. The role of incorporating specific balance training and fall prevention strategies within the framework of PR to minimize disability in this population needs to be explored. Acknowledgements: PR staff and patients. We thank the West Park Healthcare Centre References 1. Wouters EF, Creutzberg EC, Schols AM. Systemic effects in COPD. 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