Falls are an important cause of injury, injury-related disability, and death in older adults. Approximately 30% of adults aged ≥ 60 yr fall each year and prevalence increases with age.1 There is strong evidence that patients with chronic obstructive pulmonary disease (COPD) are at an even higher risk of falling.2,3 Possible underlying mechanisms for impaired balance in COPD are lower limb muscle weakness,4 altered trunk mechanics,5 somatosensory deficits,4 altered postural control,6 comorbidities (eg, osteoporosis, osteoarthritis, cognitive impairment), and/or multiple medication use (eg, corticosteroids, psychotropics, cardiac medication).4 Furthermore, impaired balance has been shown to be associated with decreased physical activity in COPD and loss of independence in activities of daily living.7
Treatment and management of COPD are often focused on stabilizing the respiratory function and improving exercise capacity.8 Exercise training is even described as being the cornerstone of pulmonary rehabilitation (PR) in the 2013 American Thoracic Society/European Respiratory Society statement on PR.9 However, since falls are associated with an increased risk of all-cause mortality, improving balance and preventing falls are becoming a novel treatment target in patients with COPD,10 and measures of balance are now recommended to be included in the clinical assessment of patients with COPD.9
Although results of studies using exercise interventions to improve balance in patients with COPD are encouraging, to the best of our knowledge there is no systematic overview of the effects of the different interventions on balance and fall risk.11,12 Therefore, the purpose of this review was to systematically review the effect of exercise-based interventions on fall risk and balance in patients with COPD.
This study was conducted and reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines.13
INFORMATION SOURCES AND SEARCH STRATEGY
A computerized literature search was performed on August 1, 2019, using PubMed, Web of Science, EMBASE, and CINAHL. The following key words and MeSH terms were used combined with “AND” and/or “OR”: COPD, chronic obstructive pulmonary disease, emphysema, chronic bronchitis, chronic airflow obstruction, exercise, training, strength training, resistance training, aerobic training, rehabilitation, postural balance, gait stability, gait instability, fall-risk, and risk of falls. All search terms, including the full search string and inclusion and exclusion criteria, are presented in Supplemental Digital Content 1, available at: http://links.lww.com/JCRP/A173. References from relevant articles were also screened for additional relevant papers.
Original studies that met the following criteria were included: (1) participants: patients with COPD; (2) study design: randomized controlled trials (RCTs) or within-group studies; and (3) outcomes: effect of an exercise-based intervention on balance and fall risk. Articles were excluded when (1) data were not described specified for COPD; (2) the duration of the intervention was <14 d; and (3) balance or fall risk was not reported as an outcome measure. In addition, non–English language articles, review articles, editorials, qualitative studies, methodology studies, and congress abstracts were excluded.
DATA EXTRACTION AND METHODOLOGICAL QUALITY ASSESSMENT
Two independent reviewers (J.M.L.D. and A.W.V.) independently screened titles and abstracts for eligibility and reviewed the full text of articles that met the inclusion criteria. Disagreements could be resolved by consulting a third reviewer (M.A.S.).
Study details and relevant results were obtained in a predesigned data abstraction form. For each study, first authors, participant characteristics (sex, age, and disease severity), exercise intervention, outcome parameters, and main outcomes were recorded. If necessary, authors of included studies were contacted directly to request additional data.
The risk of bias was independently assessed by 2 reviewers (J.M.L.D. and A.W.V.), using the risk of bias tool RoB214 for RCTs and ROBINS-I15 for non-RCTs. Both tools assess the risk of bias in several domains as well as the overall risk of bias. The risk of bias was assessed as low, some concerns, or high for RCTs; and low, moderate, serious, or critical in within-group studies.
All between-group results and within-group results are presented as mean change ± SD. When the mean change ± SD were not reported, data were requested from the corresponding authors. When no response was received or data were unavailable, results were calculated using methods described in the Cochrane Handbook.16 To be able to compare results from studies that did not use the same outcome measure, effect sizes were calculated using Cohen d. Results of the studies were compared with the minimal clinical important differences (MCID), recently reported by Beauchamp.17
Our search identified 76 unique studies, of which 15 fulfilled eligibility criteria.11,12,18–30 Reasons for exclusion were no balance or fall risk outcome reported (n = 3), not describing original data (n = 1), results from patients with COPD were not specified (n = 2), not meeting the minimum intervention duration of 14 d (n = 1), and no RCT or a within-group study design (n = 1) (see Supplemental Digital Content 2, available at: http://links.lww.com/JCRP/A174).
RISK OF BIAS
In 4 of the 15 studies included in this review, the overall risk of bias was low.12,18–20 One RCT11 was considered at high risk of bias due to the concealment of the allocation sequence being unclear, as well as the blinding of outcome assessors. Two RCTs21,27 raised some concerns due to the lack of blinding of outcome assessors.
Three within-group studies22,24,31 were at serious risk of bias because of high rates and/or unblinded outcome assessors. Two within-group studies28,29 had a moderate risk of bias, while 3 within-group studies were rated as “no information,” because of a lack of information in key domains of the bias assessment.
A summary of the results of the qualitative assessment is presented in Supplemental Digital Content 3, available at: http://links.lww.com/JCRP/A175. The complete results of the qualitative assessment can be found in Supplemental Digital Content 4 (RCTs; available at: http://links.lww.com/JCRP/A176) and Supplemental Digital Content 5 (within-group studies; available at: http://links.lww.com/JCRP/A177).
GENERAL STUDY CHARACTERISTICS AND POPULATIONS
Study characteristics are described in Table 1. Six RCTs11,12,18,20,21,27 and 9 within-group studies were included in this review.19,22–24,26,28–31 Four RCTs11,20,21,27 also reported the within-group results. The corresponding authors were contacted if additional data were required, but unfortunately not all authors responded. When no response was received, the data were presented as not reported or means ± SD were calculated according to the methods described in the Cochrane Handbook. Of the 15 included studies, 8 studies performed the intervention in an outpatient setting11,18,21–23,26,27,30 and 4 in an inpatient setting.12,19,24,29 Three studies included patients from both in- and outpatient settings.28,29,31
A total of 842 participants was evaluated, with reported mean ages ranging from 58 to 73 yr. Seven studies11,12,19,20,24,25,28 included patients with on average severe COPD (mean forced expiratory volume in the first second of expiration [FEV1] 30-50% predicted), 8 studies18,21,23,26,27,29,30 included patients with moderate COPD (mean FEV1 50-80% predicted), and 1 study22 included patients with mild COPD (mean FEV1> 80% predicted). Most studies had a relatively small sample size (<50 patients per group). Only Mesquita et al28 had a sample size of 378 patients. Adverse events were reported only in 4 studies.18,20,30,31 The balance measures used in the included studies are briefly described in Table 2.
Study outcomes are described in Table 3. The interventions reported in the included studies often included PR, with or without an additional training component: Two studies focused on the effects of PR only,19,22 while 5 studies added an extra training modality to PR (neuromuscular electrical stimulation,21 whole-body vibration training,20 or balance training11,12,23). Leung et al18 used t'ai chi as the only intervention. All studies measured the balance outcomes immediately after the end of the intervention. No outcomes measuring fall risk were reported.
Three studies that performed only conventional PR19,28,29 used a within-group study design to investigate the effect of PR on balance. One study19 used a 6-wk inpatient setting and 2 studies28,29 were performed in a mixed in-/outpatient setting where the outpatient PR program took 16 wk and the inpatient PR program took 8 wk. All within-group studies used the Timed Up and Go (TUG) test and 2 studies found significant improvements after PR,19,28 which also exceeded the MCID17 (P = .003, effect size [ES]: 1.0, P < .001, ES: 0.3). Beauchamp et al19 used the Berg Balance Scale (BBS) as an additional measure of balance. Although improvements were significant (P < .001, ES: 0.6), the MCID was not exceeded. Mesquita et al28 also reported stratified results for normal and abnormal TUG at baseline, with significant improvements only in the group with the abnormal TUG at baseline (P < .001, ES: 0.6).
Balance Training Combined With PR
Two studies11,12 investigated the specific effect of adding balance training to PR through an RCT design. Both studies added the balance training program as described by Beauchamp et al,12 which consists of a combination of stance exercises, transition exercises, gait exercises, and functional strengthening with a progressively increased difficulty level. After a 24-wk outpatient program, Mkacher et al11 found significant improvements in TUG in both groups (intervention group [I]: P < .01 and ES: 4.9, control group [C]: P < .05 and ES: 1.6), also exceeding the MCID, while BBS did not change. Significant between-group differences were found for both TUG and BBS (P < .01, ES: 1.7; P < .01, ES: 3.0), also exceeding MCID. Beauchamp et al12 added balance training to a 6-wk inpatient PR program and used the BBS and Balance Evaluation Systems Test (BESTest) as measure for balance. Although for both outcomes a significant difference between the control group and the intervention group was found (P < .01, ES: 0.6), only the differences in BBS exceeded the MCID.
Four studies22–24,31 used a within-group design to assess the effect of PR with balance training. Two studies22,23 used a 12-wk outpatient PR setting with TUG as the outcome measure of balance and found significant (P < .001, ES: 0.8; P = .001, ES: 1.2) and clinically relevant improvements. One study31 was focused on reducing the gap between evidence and practice by training the health care professionals in knowledge translation before implementing the balance training in the 6-wk PR program with a combined in- and outpatient setting. They used the previously mentioned results from Beauchamp et al12 as a comparison and also followed the same balance training program. Significant results were found in all outcome measures (BBS: P < .001, ES: 1.2; BESTest total: P < .001, ES: 2.2; BESTest subscores: P < .001, ES ranged from 1.0-1.5). One study24 used a 6-wk inpatient PR setting with balance training but found no significant improvements on the BBS and BESTest. This was also the only study that assessed the long-term effects of an intervention. Unfortunately, due to a high dropout rate, only 14% of the initial number of recruited subjects completed the 12-mo follow-up. No significant differences were found when comparing pre-PR results with post-PR measurements and follow-up measurements.
Two studies26,27 used a slightly modified version of PR called family-based PR, where family members were more involved during the PR program. This program also included balance training, although balance was not the main outcome of the studies. Both studies used the TUG as a measure of functional balance. One of these studies27 was designed as an RCT, in which the control group consisted of PR with balance training but without the increased involvement of family members. Both groups showed significant improvements in the TUG (I: P < .001, ES: 0.8; C: P < .001, ES: 0.5), and no between-group differences were found. The within-group study26 also showed significant improvements when comparing pre- with post-intervention results (P = .002, ES: 1.0).
Other Training Interventions Combined With PR
Mekki et al21 investigated the effect of adding neuromuscular electrical stimulation of several leg muscles to 24 wk of PR. Berg Balance Scale and TUG test were used, along with measures of center of pressure (CoP) displacement in anterior-posterior and mediolateral directions, as well as CoP area. All CoP measures were tested with eyes open and eyes closed. The intervention group showed significant improvements in all balance measures (BBS: P < .001, ES: 3.0; TUG: P < .001, ES: 3.0; all CoP measures: P < .001, ES ranged from 0.4-6.5). The improvements in TUG and BBS exceeded MCID. The control group that received only PR improved significantly in BBS and TUG (BBS: P < .001, ES: 2.3; TUG: P < .001, ES: 1.7), also exceeding MCID, while only 3 of 6 CoP measures showed significant improvements (CoP displacement mediolateral eyes open: P < 0.05, ES: 0.5; CoP area eyes open and eyes closed: P < .001, ES: 1.4). Berg Balance Scale and TUG differed significantly between the intervention and control groups (BBS: P = .01, ES: 0.6; TUG: P = .02, ES: 0.8), but this difference did not exceed the MCID.
Gloeckl et al20 used whole-body vibration training as an added intervention to 3 wk of PR. Only balance measures in stance were used, where the absolute path length of the center of force was measured using a force plate. All balance measures improved significantly in the intervention group (P values ranged from <.001-.029, effect sizes ranged from 0.4-0.7), while no significant differences were found in the control group. When comparing the intervention group with the control group, all balance measures differed significantly, with the exception of the Romberg stance eyes closed absolute path length.
Two studies used exercise-based interventions without PR. Leung et al18 used 12 wk of t'ai chi training 2 times/wk as a training modality for the intervention group, while the control group received usual medical care without exercise training. The outcome measures were body sway in anterior-posterior and mediolateral directions, with feet in semitandem or side-by-side position, and functional reach distance. All balance outcomes, except body sway in semitandem in anterior-posterior direction, significantly improved after the intervention (P < .01, ES ranged from 0.2-1.1).
Rinaldo et al30 performed a study in which patients were randomly assigned to one of the intervention groups. One group (CT) received 28 wk of supervised combined exercise training 3 d/wk. The other group (EDU) received a 28-wk physical activity education program that consisted of a combination of both supervised and self-directed training sessions. The total of supervised and self-directed sessions added up to 3 times/wk. Balance was assessed using the timed 1-leg stance. Both groups showed significant improvements that remained significant after a follow-up period of 14 wk (CT: P < .05, ES ranged from 0.8-1.7; EDU: P < .05, ES ranged from 0.4-0.8). No between-group differences were found.
This is the first review systematically evaluating the effects of exercise-based interventions on balance and fall risk in patients with COPD. As balance impairment is a common problem in patients with COPD, which contributes to an increased risk of falling, identification of exercise-based interventions that are effective in improving balance in COPD is important.2,3,12 Moreover, good balance control is believed to be fundamental in the ability to maintain functional independence in activities of daily living.7 Findings of this review indicate that exercise-based interventions are effective in improving balance in patients with COPD. All included articles reported positive effects on balance outcomes after intervention, often exceeding the MCID.
In this review, a wide variety of exercise-based interventions with duration ranging from 3-28 wk was included. Of the 15 studies included in this review, 6 studies used a randomized controlled design11,12,18,20,21,27 while 9 studies performed pre-/post-intervention comparisons19,22–24,26,28,29,31 or compared 2 interventions.30
A large number of outcome measures was used to assess balance. Recently, Beauchamp17 provided a critical evidence-based overview of balance measurement in patients with COPD, including TUG, BBS, BESTest, and Mini-BESTest. The TUG, BBS, BESTest, and Mini-BESTest were described to be useful in assessing balance in patients with COPD, with documented construct validity and intra- and interrater reliability. The TUG, BBS, BESTest, and Mini-BESTest are considered reliable and validated measures of balance and have an adequate accuracy in assessing fall status and/or fall risk.28,32–35 Looking at studies that reported TUG, BBS, and BESTest (Mini-BESTest was not used in any of the included studies), PR with added balance training has the highest effect size. Fall risk was not reported in any of the included studies.
Three studies18,20,30 did not use any of the recommended tools for balance assessment in patients with COPD. Instead, they used single task instruments, such as the functional reach test or 1-leg stance, or instruments that assess only body sway in a specific standing position. Although these tests are less physically demanding, the comprehensiveness of these instruments in assessing functional balance is very limited. Balance can be influenced by many factors, including muscle strength.36 Therefore, the results of the studies using single-task instruments might not be as relevant as the results of the studies that used the recommended comprehensive balance assessment tools.
Looking at the quality of the studies, 9 studies11,21–24,27–29,31 had an increased risk of bias. This was due to the lack of blinding of outcome assessors. While blinding of participants and persons performing the intervention is sometimes not possible, due to the nature of the intervention, the blinding of outcome assessors was not hindered by this. Also, a high number of dropouts23,24,31 and uncertainty about the concealment of the allocation sequence11 negatively impacted the risk of bias. Two studies26,30 did not provide sufficient information to assess the risk of bias.
No study reported the effects of dual-task training, virtual reality training, or perturbation-based training. A review by de Amorim et al37 concluded that findings of studies using virtual reality training in elderly populations showed promising results. In a review by Ghai et al,38 beneficial effects of dual-task training in fall-prone elderly populations were demonstrated. Furthermore, in a review by McCrum et al,39 the majority of the included studies showed beneficial effects of perturbation-based training on the reactive recovery response in elderly populations. Moreover, it has been shown that elderly populations are able to adapt locomotion, although the rate of adaptation was decreased compared with younger adults.40 In addition, retainment of favorable effects up to a year after exposure to perturbation-based training has been reported in older adults.41,42 It would be interesting to demonstrate whether these training modalities provide beneficial effects in patients with COPD. Furthermore, novel outcomes such as margins of stability43,44 could provide us with new information on the causes of balance impairment in COPD, enabling us to target balance problems more specifically in patients with COPD.
This review has several limitations. First, only 15 studies were eligible for inclusion. Including studies in languages other than English might have resulted in more eligible articles, although it has been suggested that the exclusion of non–English studies does not affect the results.16 Furthermore, since balance assessment and training in COPD are emerging topics for research, it is understandable that a limited amount of records was available at the time of the search. Second, almost all studies included in this review had a relatively small sample size. It would be recommended to perform more studies with a larger sample size, so that results can be generalized to the whole COPD population. Third, most studies performed an intervention in which PR was included. Patients in an earlier stage of COPD or patients who are less limited by their symptoms are less likely to participate in a PR program. Therefore, these patients might not be sufficiently represented in this review. Fourth, due to the diversity of the studies, no meta-analysis was performed, which is in accordance with Cochrane guidelines.16 Finally, little is known on long-term effects of the interventions in patients with COPD. All outcomes were measured immediately after the end of the intervention. Only 1 study24 followed patients for 12 mo after the intervention but found no significant effect of the intervention and suffered from a high dropout rate during follow-up. It is still unclear whether positive effects measured after interventions will sustain in the long-term. Although immediate beneficial effects of an intervention are a good starting point, the ultimate goal should be to find an intervention that has the ability to maintain a positive effect for a longer period of time. A sustained effect of an intervention that improves balance and decreases fall risk would provide a good rationale for implementing such an intervention in usual care. Although exercise interventions such as perturbation training have shown beneficial long-term effects in the elderly,40,42 a combination of behavioral and exercise interventions will probably be necessary to optimize preservation of beneficial effects in patients with COPD.
Considering the increased risk of falls associated with COPD as well as increased mortality, interventions focusing on balance improvement in patients with COPD are important. The American Thoracic Society/European Respiratory Society statement on PR has also reported that balance should be one of the outcome assessments of PR.9 This review confirms previous findings that a standardized measure of balance in COPD is currently lacking.17,45 Indeed, a large variety in outcome measures was used, and instructions for the tests were not standardized. For example, some studies instructed the patients for the TUG to stand up from a chair, walk as quickly and safely as possible back and forth on a 3-m course, and sit down,22,23,27 while others instructed patients to walk at a comfortable pace.11,19,28,29 It seems necessary to determine a standardized balance assessment to be able to adequately assess effects of different interventions.
Exercise-based interventions have the potential to improve balance in patients with COPD. Pulmonary rehabilitation combined with balance training showed the most beneficial effect on balance, when considering the recommended balance assessment instruments. Whether and to what extent these interventions also have a positive effect on fall risk remains currently unknown.
The authors thank Dr Regina Leung (Concord Repatriation General Hospital, Sydney, Australia), Dr Samantha Harrison (Teesside University, Middleborough, United Kingdom), Dr Dina Brooks (West Park Healthcare Centre, Ontario, Canada), Dr Marla Beauchamp (McMaster University, Ontario, Canada), Dr Rainer Gloeckl (Schoen Klinik Berchtesgadener Land, Schoenau am Koenigssee, Germany), Dr Rafael Mesquita (Horn, the Netherlands), and Dr Wai-Yan Liu (Horn, the Netherlands) for sending additional data to complete this review.
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