Chronic obstructive pulmonary disease (COPD) is a progressive respiratory disease characterized by limitations in lung airflow.1 It is a leading cause of morbidity and mortality in Canada,2 and it currently ranks as the third leading cause of death worldwide.3 It is now well established that COPD is a complex, multisystem disease that impacts considerably more than an individual's lung function.4-9 In particular, recent evidence has identified prominent balance impairments among those with COPD that may contribute to an increased risk of falls in this population.8,10-21
Balance is a complex skill that is achieved through the integration and coordination of the musculoskeletal and neural systems of the human body.22-24 Muscle strength is one component that has been highlighted as a key contributor to balance problems and falls in older adults.18,24-27 Given that skeletal muscle dysfunction is a commonly identified impairment in people with COPD,9 it is not surprising that lower-limb muscle weakness has also been linked to balance deficits and increased fall risk in this population.10,12,13,18
Given the integral role that muscle strength plays in the successful maintenance of balance, and the strong associations between both muscle weakness and balance impairment with falls, there is a need to address muscle strength deficits as part of balance assessment and training for people with COPD. The purpose of this review is to examine the role of muscle strength in the assessment and management of balance problems among individuals with COPD. Our specific aims are to (1) synthesize the literature on the role of muscle strength in balance control among older adults; (2) provide an overview of what is known about these relationships in people with COPD; and (3) describe clinical applications of assessing and training muscle strength in the context of improving balance among individuals with COPD.
THE ROLE OF MUSCLE STRENGTH IN BALANCE CONTROL IN HEALTHY INDIVIDUALS
Balance Control and the Role of the Musculoskeletal System
Balance, or postural control, can be defined as “the act of maintaining, achieving, or restoring a state of balance during any posture or activity.”28 It consists of 2 major components: postural orientation, or the control of body alignment in relation to the environment, and postural equilibrium, or the body's ability to maintain center of mass (COM) while static or during movement.29 Balance can be controlled either reactively when an individual responds to an external force, or proactively when an individual anticipates a postural challenge.30 The central nervous system is responsible for recognizing destabilizing forces and stimulating musculature to generate the right amount of force to delay the motion of COM. There are a multitude of factors that regulate balance because it is reliant on inputs from musculoskeletal, neural, vestibular, kinesthetic, motor control, and cognitive systems.30
In relation to the musculoskeletal system, the ankle dorsiflexors, ankle plantarflexors, knee flexors, and knee extensors are the major muscle groups needed for postural stability, with primary contributors being the tibialis anterior (ankle dorsiflexion), gastrocnemius (ankle plantarflexion), hamstrings (knee flexion), and quadriceps (knee extension).31 Each has a different role in contributing to balance maintenance. The dorsiflexors are responsible for stability during backward movements to prevent the COM from extending posteriorly beyond the base of support. The plantarflexors are in control of stabilizing the COM when there is anterior movement beyond the base of support. The knee flexors are responsible for forward sway and the knee extensors control backward sway.31 Finally, there is a role for the hip abductors and adductors in the control of lateral stability, which may be of a particular relevance for fall risk.22,24 Dysfunction in any of these muscle groups contributing to postural stability can lead to declines in balance performance26 and an increased fall risk.26
Age-Related Changes in Muscle and Postural Control
Aging is a process that alters the properties of the neural, sensory, and musculoskeletal systems,24,26,32,33 which can further lead to balance deficits and an increased fall risk among older adults.24,34 In terms of muscle function and normal aging, neural system alterations include a reduced activation of muscle from decreased neural drive and impairments in contractile properties, as well as a decline in the ability to develop and produce muscle force.24,34 Age-related musculoskeletal alterations include a loss of muscle mass (sarcopenia) with preferential atrophy of type II muscle fibers, decreases in force generation, reductions in power, decreases in specific tension, and fatigability.34
The impact of these age-related neural and musculoskeletal changes on balance and fall risk can be observed when considering responses to external perturbations. Compensatory stepping (eg, taking a step to avoid a fall in the event of a postural perturbation) and reaching reactions (eg, reaching to grasp a railing during a loss of balance) are the 2 major mechanisms that counterbalance perturbations and play key functional roles in fall prevention.22,24 Both types of reactions undergo significant age-related changes that may arise from muscle dysfunction, whereby older adults demonstrate an impaired ability to control lateral stability during stepping reactions35 and also exhibit deficits in producing reaching reactions rapidly.22,24,35 For stepping reactions to counter loss of balance, it has been suggested that decreases in strength in specific muscle groups among older adults may result in stability challenges during the swing phase and landing.22 In particular, substantial weakness of the hip abductors and adductors may contribute to problems maintaining lateral stability while stepping, which could increase the risk of falling laterally.24,35 Falls due to a loss of balance laterally have been shown to be common among older adults.36,37 In addition to this, the rate of muscle-force production may also impact stepping reactions in older adults because they may have a limited capacity to generate the fast movements required to address extreme postural challenges.24,38 An age-related loss of fast-twitch muscle fibers and the slowing of information processing, in combination with reductions in nerve conduction velocity and neural activation may contribute to this limited capacity to generate rapid movements.24,34
Association Between Measures of Muscle Strength and Balance
With the recognition of the role of muscle strength in the maintenance of balance, several studies and reviews have explored the relationship between muscle strength and balance among older adults. A systematic review by Orr26 (2010) examined cross-sectional associations between clinical measures of muscle strength or power and balance among healthy older adults, while also looking at the impact of strength training interventions on balance. Most of the included studies assessed at least one of the key muscle groups for postural control (ankle dorsiflexors, ankle plantarflexors, knee extensors, and knee flexors), with knee extensors and flexors assessed most frequently. Muscle strength was most commonly measured using 1 repetition maximum on resistance machines, but other measures included isometric or isokinetic dynamometers, and functional tests (eg, Sit-to-Stand). Muscle power was assessed using resistance machines, the Nottingham Power Rig, and functional tests (eg, Sit-to-Stand and Stair Climb). There was evidence for a consistent relationship between muscle strength and balance performance, where muscle strength was identified as a key contributor to postural stability. However, Orr (2010) noted that muscle weakness should not be considered the only factor contributing to balance dysfunction among older adults because only approximately half of the intervention studies reported a significant improvement in balance after strength training alone. In a more recent systematic review conducted by Muehlbauer et al33 (2015), associations between measures of static, dynamic, anticipatory and reactive balance, and measures of lower-extremity muscle strength were examined in 36 studies of healthy people across the lifespan (ages 6 to 65+). Within this study, lower-extremity muscle strength was categorized into measures of maximal strength (eg, maximal voluntary force/torque of the force–/torque–time curve), explosive force (eg, rate of force/torque development based on slope of the force–/torque–time curve) and power (eg, jump distance, force, height, and power). The study findings indicated that there were primarily small- to medium-sized correlations (r = 0.09–0.57) for all ages between measures of balance and lower-extremity muscle strength/power, although larger correlations (r ≥ 0.35) were shown between measures of dynamic balance and maximal strength in older adults compared with young adults.33
Although there is often a focus on the role of lower-extremity muscle strength in relation to balance performance, trunk muscle strength has also been associated with aspects of static and dynamic balance and falls. A systematic review by Granacher et al.39 (2013) examined the associations between trunk muscle strength and composition, and balance, functional performance and falls among older adults. Within this review, trunk muscle strength entailed measures of both trunk extensors (back muscles) and trunk flexors (abdominal muscles), and muscle composition was defined as trunk muscle area/attenuation (eg, fat infiltration) of the abdominal, paraspinal, quadriceps, and hamstring muscles. The authors were able to identify a low (r2 ranging from <1% to ≤18%) but significant relationship between trunk muscle strength and trunk muscle attenuation and balance, function, and falls across the 4 included studies. It was concluded that trunk strength and stability are important for achieving activities of daily living for older adults, but in particular, a stable and strong trunk may lead to more efficient use of the lower and upper extremities and, in turn, better balance and function among older adults.39 In addition to this, another systematic review conducted by Helbostad et al.40 (2010) assessed the impacts of lower-extremity muscle (ankle plantarflexors and dorsiflexors, knee extensors and flexors, hip abductors and adductors) and trunk muscle (lumbar extensors) fatigue and recovery on balance and functional tasks among older adults. The authors found that fatigue of the lower-extremity and trunk muscles leads to balance dysfunction and impairs performance of functional tasks.40
THE ROLE OF MUSCLE STRENGTH IN BALANCE CONTROL IN CHRONIC OBSTRUCTIVE PULMONARY DISEASE
Skeletal Muscle Dysfunction and Chronic Obstructive Pulmonary Disease
Skeletal muscle dysfunction is not only an age-related concern but also an identified secondary impairment in COPD.4-7,9,41,42 Skeletal muscle dysfunction in COPD results in abnormalities pertaining to structural alterations of skeletal muscle and skeletal muscle function.6,7,9,41,42 Muscle atrophy of primarily type II fibers, decreased capillary numbers and contacts (capillary:fiber ratio), mitochondrial dysfunction, and disturbances in metabolic enzyme activity have all been identified as possible abnormalities in terms of structural alterations in skeletal muscle.6,7,9,41,42 Reduced muscle strength and endurance have been identified as possible abnormalities in regard to skeletal muscle function.6,7,9,41,42 These muscle abnormalities may be attributed to hypoxia, oxidative stress, low levels of anabolic hormones and growth factors, hypercapnia, inflammation, impairments in energy balance in regard to regulation of protein and nutrition, vitamin D deficiency, corticosteroid use, impairments in the renin–angiotensin system, and smoking.6,7,9,41,42
Association Between Skeletal Muscle Dysfunction and Balance in Chronic Obstructive Pulmonary Disease
Despite the extensive literature on skeletal muscle dysfunction in people with COPD, relatively few studies have examined these abnormalities with respect to their potential impact on the extensive balance problems that have been documented in this population. In a comprehensive study of the subsystems underlying the observed balance deficits in people with COPD, it was previously noted that individuals with COPD had a unique profile of balance deficits, which included marked impairments in the biomechanics balance subsystem.10 Balance performance in this subsystem included tasks related to strength, range of motion, and posture and was reduced by more than 30% in people with COPD compared with age-matched controls. In this study, maximal voluntary isometric contractions of the knee extensors/flexors and ankle plantar/dorsiflexors were also measured. Small to modest associations (r = 0.2–0.4) were reported between knee muscle strength and clinical measures of balance such as the Berg Balance Scale (BBS), with smaller associations noted between ankle strength and balance. Although the patients with COPD had reduced strength values compared with the age-matched controls, the magnitude of these associations were not unlike the ones reported in healthy populations,26,33 suggesting that muscle weakness may be a contributor, but not solely responsible for balance problems in people with COPD.10 Finally, people with COPD also showed a delayed stepping reaction for balance recovery in response to unexpected perturbations, despite a lack of slower muscle onset latencies (measured through electromyography [EMG]) compared with controls.10 Therefore, skeletal muscle dysfunction may well have explained this impaired ability to generate adequate muscle power in response to perturbations; however, further studies are required to evaluate this.
Altered trunk muscle mechanics may also help explain decreased postural control in patients with COPD.7 In quiet standing, mediolateral (ML) balance control is reliant on hip and trunk moments and movements43 and may be more impaired than anterioposterior control in individuals with COPD.21 It has been suggested that ML static balance is reduced in COPD as a result of a decreased contribution of trunk muscles and moments to balance.19 This has been attributed to increased respiration demands in COPD requiring more abdominal muscle activation,21 which could affect trunk muscle support toward postural control.44 Using EMG to measure trunk muscle activity and the time needed to regain baseline center of pressure velocity after rapid arm movements in static standing, Smith et al19 (2016) demonstrated that compromised balance recovery in COPD was associated with greater trunk muscle activity than was needed for breathing. Therefore, in people with COPD, balance may be compromised in part because of the double demand placed on trunk muscles in regard to postural and respiratory functions.
An additional relevant consideration in people with COPD is the impact of acute exacerbations of the disease (AECOPD) on muscle strength and balance. A recent study conducted by Oliveira et al20 (2017) investigated balance impairments, muscle strength, and falls in the context of AECOPD. The authors measured quadriceps strength with a handheld dynamometer and balance using both computerized posturography and the BBS in hospitalized patients with AECOPD, stable patients with COPD and healthy controls. Balance impairment in both individuals with AECOPD and stable COPD were associated with reduced quadricep strength (AECOPD—28% and stable COPD—14%). In addition, although balance performance was not different in those with AECOPD compared with stable patients, it was reported that patients with AECOPD experienced more falls in the 1 year after discharge compared to those with stable COPD. Therefore, it is possible that reduced muscle strength in people with AECOPD may further contribute to balance deficits and an increased fall risk in these patients after discharge.
Muscle Endurance, Muscle Power, and Balance Control in Chronic Obstructive Pulmonary Disease
Although there is a centralized focus on the role of muscle strength in maintaining balance control in individuals with COPD,10,18,45 it is worth noting that both muscle endurance and muscle power may have similar associations with balance.18 To our knowledge, there are no studies that have specifically examined the contribution of deficits in muscle endurance and muscle power to balance problems and fall risk in people with COPD. However, muscle endurance is known to be reduced in individuals with COPD compared with healthy controls.46,47 This reduction is important because it suggests increased muscle fatigability,48 which has been linked to impaired balance control in young adults.49,50 In regard to muscle power, Roig et al.51 demonstrated a 28% decrease in lower-extremity muscle power among individuals with COPD compared with a control group using the Stair Climb Power Test, which they showed was also moderately correlated with the Timed Up and Go (TUG) Test (r = −0.46). Although the TUG test was administered to measure functional performance, the test has been used to measure balance in this population and is frequently used as a measure of balance and fall risk in the elderly.12 Further study of the link between reductions in muscle power in people with COPD and their association with balance and fall risk is warranted. Moreover, in older adults, it has been suggested that muscle power may in fact play a larger role than muscle strength in postural control and fall prevention.52,53 Muscle power not only declines earlier and at a faster rate than muscle strength with increasing age (3.5% decrease per year vs 1.5% per year, respectively),54 but it has been shown to elicit a greater influence on postural control with measures of single-leg stand and postural sway55 and to represent a more important predictor of functional health.52,53 This may be attributed to the need for lower limbs to rapidly generate force to maintain balance during a perturbation22,55 or to complete functional tasks.56 In addition, muscle power may discriminate between elderly fallers and nonfallers,53,57 as well as indicate early signs of balance deficits and fall risk among healthy older adults.58
ASSESSING AND MANAGING MUSCLE WEAKNESS AS PART OF BALANCE ASSESSMENT AND TRAINING
Balance Assessment Considerations
Balance is often referred to and believed of as a singular construct, but it has several underlying mechanisms that are important to keep in mind when assessing and treating balance impairment (Fig. 1). The Systems Framework of Postural Control is a widely recognized model of balance, which organizes postural control into 6 underlying systems: (1) biomechanical constraints (eg, strength and coordination), (2) movement strategies (eg, stepping reactions), (3) sensory strategies (eg, vision, vestibular, and somatosensory), (4) orientation in space, (5) control of dynamics (eg, gait), and (6) cognitive processing (eg, attention).29 In particular, strength is included under “biomechanical constraints.”29 In a scoping review of 66 different balance measures, Sibley et al59 (2015) found that all 66 measures included tasks that evaluated muscle strength and coordination to some degree, whereas other systems such as movement strategies and cognitive processing were less frequently evaluated. It is not surprising; therefore, that in a study of balance assessment practices among physiotherapists, more than 80% of respondents reported regularly assessing underlying motor systems such as strength when evaluating balance.60 Although muscle strength is an important component of balance, measures that assess multiple components are necessary to identify the underlying impairments that can be targeted by interventions. The Balance Evaluation Systems Test (BESTest) is the one standardized clinical measure that has been shown to evaluate all aspects of balance.59 Other measures such as the Clinical Gait and Balance Scale, Fullerton Advanced Balance Scale, Mini-BESTest, and Unified Balance Scale are fairly comprehensive, but most measures identified (52%) evaluated a third or fewer components of balance.59 The Clinical Gait and Balance Scale and The Unified Balance Scale do not cover cognitive influences and verticality components of balance, respectively,59 and both of these measures have only been used in neurological populations to our knowledge. The Fullerton Advanced Balance Scale and the Mini-BESTest are missing the verticality, and functional stability limits components of balance, respectively,59 and both have been used in general populations of older adults.61,62 Despite these findings, the measures most often used in clinical practice are the single-leg stance (SLS) test, the BBS, and the TUG,60 which, with the exception of the BBS, measure less than half of the underlying balance systems.
Assessing Balance in People With Chronic Obstructive Pulmonary Disease
In the assessment of balance in people with COPD, the most commonly used measures in the literature are the BBS, the short physical performance battery (SPPB), SLS, and functional reach test (FRT).63 The FRT and SPPB have criterion validity for predicting increased risk of disability in people with COPD, and the BBS is responsive to pulmonary rehabilitation.63 The measures with the most comprehensive evidence for their psychometric properties are the BBS and BESTest, but, consistent with general clinical practice, the BESTest is less frequently used with people with COPD,63 likely owing in part to its more recent development and also its longer administration time (45 minutes vs 30 minutes for BBS). Of note, the minimal clinically important difference has been established for the BBS (5 points) and BESTest (13 points) in patients with COPD undergoing pulmonary rehabilitation.64 Although all these measures provide clinicians with an observation of tasks that provide insight into any muscle strength deficits that may be contributing to balance impairment, only the BESTest has a section explicitly devoted to biomechanical tasks and an associated score solely for this subsystem. Thus, in considering selection of the optimal balance measure, if a comprehensive test to guide exercise prescription is preferred, the BESTest would be the ideal choice if time allows. In terms of shorter balance screening tests to determine the need for further evaluation and risk of falls, there is currently little evidence to guide test selection in COPD. In older adults, tests such as the SLS and TUG are often endorsed for this purpose.65 The SLS has been shown to have excellent reliability,66 to be predictive of injurious falls among older women,67-69 and to discriminate among those with stable COPD, those with AECOPD, and age-matched controls, as well as among those with varying falls history.70 The TUG has been shown to discriminate between fallers and nonfallers in COPD12 and has demonstrated reliability and predictive validity for falls in a few different studies with older adults, but with limited diagnostic accuracy in some populations.71,72 The Centers for Disease Control recommends using tests of standing balance and the TUG as tools for fall risk screening and prevention for older adults.73
Balance Treatment Considerations
Given the impairments in skeletal muscle seen in people with COPD and the contribution of muscle weakness to balance impairment, it is clear that muscle strength should be assessed as part of a comprehensive balance assessment and any weakness treated as a part of an exercise program. Training for muscle strength traditionally includes resistance training with free weights, pulleys, exercise bands, or machines that focuses on specific muscles or muscle groups. On the other hand, strength training for balance typically focuses on lower-extremity muscles and involves more functional exercises such as leg press, hamstring curls, knee extensions, lunges, squats, and calf raises. There is heterogeneity in the programs that have been evaluated in the literature for their effect on balance in the elderly with program durations ranging from 10 weeks to 1 year, session durations ranging from 45 to 90 minutes, and intensities ranging from 40% to 85% of 1 repetition maximum.74-80 Despite showing improvements in TUG,75,77 FRT,77,79 tandem walk test,79 chair rise,77 and SLS77 after resistance training, as highlighted previously in this article, these trials found inconsistent results for the effect of strength training on balance.74,76,78-80 There are benefits of strength training, but in isolation, exercise focused only on strength is not likely to impact balance or falls; only 22% of studies in a systematic review provided support for resistance training to improve balance.81 The most effective programs for older adults are multicomponent programs that include an aspect of training that challenges balance.82 In particular, balance training program durations of 11 to 12 weeks with training frequencies of 3 sessions per week and session durations of 31 to 45 minutes have been found to be effective for improving fall risk.29
Training Balance and Muscle Strength in People With Chronic Obstructive Pulmonary Disease
Several studies have explored changes in balance in people with COPD, which occur as a result of participation in standard pulmonary rehabilitation programs as well as changes that occur as a result of targeted balance training with or without pulmonary rehabilitation. Although conventional pulmonary rehabilitation has been shown to improve balance to a small degree, these improvements have not been shown to be clinically significant.83,84 With targeted and comprehensive balance training, large and clinically meaningful improvements in BBS, BESTest, chair rise, and TUG have been achieved in people with COPD.84-86 These effective balance training programs did include functional strength training as part of the balance training protocols to impact the biomechanical constraints system84,86 that has been shown to be one of the areas of particular impairment in people with COPD.10 Examples of functional strength training that can be incorporated into a balance training program for people with COPD can be found in Table 1. These exercises can be progressed to allow for sufficient overload by increasing the number of repetitions and resistance, and progression of balance difficulty can be achieved by decreasing upper-extremity support, increasing speed of movement, changing sensory information, adding internal balance perturbations or adding a secondary cognitive task. These exercises should be tailored to each individual's abilities and progressed as needed to ensure sufficient and ongoing challenge to both balance and strength.
In summary, we have described how muscle strength is a key contributor to balance in both healthy populations and in people with COPD. Although impairments in skeletal muscle have been well studied in people with COPD, the contributions of this dysfunction to the observed balance deficits in COPD has not been as well studied to date. Furthermore, current research only supports associations between muscle strength and balance performance, and we are unable to determine cause and effect. In addition, the implications of potential deficits in muscle power and endurance for postural control and fall risk in people with COPD requires further study. Comprehensive assessment of balance in people with COPD should include an assessment of muscle strength but also cannot ignore the many other subsystems underlying balance. When targeting muscle strength as part of a balance training program, specific considerations should be given to functional lower-body and trunk exercises that include a challenge to different balance systems.
Marla Beauchamp is supported by an Emerging Research Leader Initiative from the Canadian Respiratory Research Network.
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