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Editorial

Systems Contributing to Balance Disorders in Older Adults

^a Department of Exercise and Movement Science and Institute of Neuroscience, University of Oregon, Eugene

Decision Editor: John E. Morley, MB, BCh

IT has been shown repeatedly that older adults show a high risk for falls and that these falls are a principal contributor to fatalities in this population ^(1)(2)(3)(4). The high risk of fatalities caused by falls in older adults has made this area of research a high priority for health care. An initial aim of this research has been to document age-related deterioration in balance control to subsequently create effective assessment and treatment programs based on these specific deficits.

In this issue of The Journal of Gerontology: Medical Sciences, we have included an article by Medell and Alexander ⁽⁵⁾ that examines the correlation between falls in older adults and performance on a new clinical measure, the Rapid Step Test. They show that this measure of a protective balance response is strongly related to underlying balance impairment in older adults. It is just this type of research, which combines knowledge of research on balance impairments in older adults with the creation and testing of new clinical tools for assessing balance control, that is very important in bridging the gap between research on balance in older adults and its application to clinical practice.

During the early years of research on balance function in the older adult, balance was assessed both in the clinic and in the research lab using global measures of balance abilities, such as total body sway ⁽⁶⁾ and the measurement of reflex function ⁽⁷⁾.

Early research exploring balance changes in older adults by Sheldon ⁽⁶⁾ examined the degree to which subjects in age groups from 6 years through 80 years swayed during quiet stance. Sheldon used a very simple technique for measuring global body sway that he could take into institutional settings. He devised a triangular metal frame with u-shaped pads that fit over the shoulders of the subject. He placed a pencil at the apex of the triangle. The pencil marked a subject's sway on graph paper that was placed right below the pencil. Using this technique of measuring global body sway, he observed that subjects at both ends of the age spectrum (6–14 years and 50–80 years) had greater difficulty in minimizing sway during quiet stance than those in the midrange of the age spectrum.

During the last 15 years, stabilometry or static force plate measures of center of foot pressure (COP) have become much more popular as measures of stability. Toupet and colleagues ⁽⁸⁾ tested 500 adults, ranging in age from 40 to 80 years, and found that postural sway (COP) increased with each decade of life, with the highest levels of spontaneous movement found in 80 year olds.

A separate study has shown that sway velocity of a similar group of older subjects was significantly greater than in young adults ⁽⁹⁾. In addition, Fernie and colleagues ⁽¹⁰⁾ examined both sway amplitude and velocity during quiet stance in a population of institutionalized elderly persons and determined that sway velocity (but not amplitude) was significantly greater for those who fell one or more times in a year than for those who had not fallen. This implies that, in certain populations, velocity of sway may be more sensitive to balance problems than absolute sway.

Patla and colleagues ⁽¹¹⁾ and others make the point that measures of spontaneous sway during normal quiet stance are not necessarily appropriate measures of balance dyscontrol, because older adults are not challenged by normal quiet stance balance and are thus typically well within their balance capacity. Patla and colleagues also make the point that large excursions of COP are often considered a reflection of poor balance control; however, some individuals may use larger and higher frequency excursions of COP to increase information about balance from their sensory systems, while remaining well within their limits of stability ⁽¹¹⁾. Patla thus proposes that static balance be assessed under challenging conditions, for example, tandem stance with eyes open versus eyes closed.

Horak ⁽¹²⁾ has also noted that there are many patients with neurological disorders, such as Parkinson's disease, who have normal sway during quiet stance though they have poor balance control. She suggests that this may be due to increased stiffness or rigidity in their neuromuscular system, limiting sway to a smaller area during quiet stance. Thus, a simple global measure of sway during normal eyes-open quiet stance may not be the best way to evaluate balance dysfunction in the older adult.

A study by Maki and coworkers ⁽¹³⁾ compared a wide range of balance tests to determine their ability to predict the risk of future falling in an ambulatory and independent older adult population. Both static and dynamic posturography tests, as well as simple clinical balance tests, were examined. Results showed that lateral spontaneous sway amplitude in eyes-closed conditions was the single best predictor of future falling risk, even in those individuals who had no recent history of falling. It is important to note that lateral sway was the important sway parameter, rather than anteroposterior (AP) sway, as it is AP sway that has been more typically measured in balance research.

When examining neural contributions to falls, clinicians also have traditionally assessed function using a reflex model of motor control. For example, clinical assessment has traditionally included the evaluation of such reflexes as tendon reflexes, righting reflexes, and vestibulo-ocular reflexes. This traditional type of evaluation has been based on a theoretical framework that predicts that reflexes are the basis of motor function and of postural control ^(14)(15). Conclusions concerning age-related changes in motor function that have come from this theoretical framework have considered many motor control changes in the older adult as resulting from a release of primitive reflexes. Paulson and Gottlieb ⁽⁷⁾ have noted, for example, that there is a reappearance of primitive reflexes in aging patients with pathology, which they viewed as a "release" of lower levels of nervous system function.

In recent years, both clinicians and researchers have taken a broader approach to determining the extent of balance problems in older adults and their contributions to falls. Researchers have become aware that there are three primary categories of factors that contribute to balance control, and all of these must be considered when evaluating falls in a given individual. These include the constraints within the individual (intrinsic factors) and both the constraints of the environment and of the task (extrinsic factors). Studies have found that there are complex interactions between intrinsic factors related to the individual and extrinsic factors related to the task and the environment ^(16)(17)(18).

One of these studies ⁽¹⁷⁾ initially examined adults over 70 years of age who lived independently, then followed up subjects for 1 year, recording all falls. Using rather broad categories for classification of intrinsic factors associated with falls, the researchers noted that low levels of physical activity, reduced proximal muscle strength, and reduced stability while standing were highly correlated with an increased risk of falling. Other factors, including impairment of gait, arthritis of the knees, stroke, use of psychotropic drugs, and hypotension were also correlated with an increased risk of falls. Their primary conclusion was that most falls in older adults are associated with multiple risk factors, and many of these may be remediated. In addition, they concluded that it is important for the clinician to identify the intrinsic and extrinsic factors that contributed to a particular fall and correct as many as possible.

Concomitant with the development of the previously described research focus, studies have attempted to identify more clearly the constraints on balance control within the different neural and musculoskeletal systems of the individual. This approach, often called a systems approach, aids the clinician in determining the extent to which constraints in the function of specific subsystems contribute to deterioration in balance in the older adult. In this research, balance has been defined as the ability to maintain the center of body mass within the limits of stability, defined by the boundaries of the base of support. Using a systems perspective, the clinician perceives balance as emerging from complex interactions among the musculoskeletal and neural systems of the individual, and the task and environmental conditions in which they find themselves ^(19)(20)(21).

The systems approach has a number of advantages for the assessment and treatment of balance dysfunction, including the fact that it allows the clinician to more easily assess the contributions of individual neural and musculoskeletal subsystems to balance dysfunction. In addition, it notes that three different types of tasks are important to consider when evaluating balance control in an older adult. These include not only quiet stance balance, but also reactive (responding to a balance threat) and proactive (stabilizing the body before making a voluntary movement) balance control.

Because measures of balance during quiet stance may be insensitive to many balance problems in the older adult, scientists have begun to use an additional paradigm to measure reactive balance function. This is a moveable platform that can simulate balance threats, such as the sudden start or stop of a bus or subway car in which one is standing. Thus, this measure is able to test the performance capacity of older adults by continually increasing the difficulty of the task until the person has difficulty in responding efficiently. Some of the studies that have examined changes in sensory, motor, and cognitive variables that are correlated with aging and with falls will be summarized later.

	Age-Related Changes in Motor Systems

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Woollacott and colleagues ⁽²²⁾ performed one of the first studies to examine age-related changes in postural muscle response characteristics elicited when balance was threatened. When the stability of young adults is threatened by support surface movements, they typically regain stability by using an ankle movement strategy in which sway is focused at the ankle joint. Muscle responses are activated first in the ankle muscles (stretched by the ankle joint movement) and then radiate upward to the muscles of the thigh and hip. Woollacott and colleagues ⁽²²⁾ compared the muscle response characteristics of healthy older adults (n = 12, aged 61–78 years) and younger adults (aged 19–38 years), and found that there were similarities in response organization between the older and younger groups. For example, most older adults used a distal to proximal muscle response organization.

There were also clear differences between the two groups. For example, older adults showed significantly slower muscle response onset latencies, and five older adults showed occasional disruptions in muscle response organization, with proximal muscles being activated before distal muscles. In other studies on patients with central nervous system dysfunction, researchers have also found this proximal to distal response organization ⁽²³⁾. Older adults also used coactivation of the antagonist muscles along with the agonist muscles at a given joint more frequently than young adults. This is a strategy that stiffens the joints, thus reducing the degrees of freedom of body motion that need to be controlled. It has also been shown that many older adults used a balance strategy involving hip movements significantly more often than young adults ^(24)(25). Hip movements are typically used by young adults when given very large balance threats.

	Age-Related Changes in Sensory Systems

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Research from a number of labs has explored age-related changes in sensory contributions to balance control ^{(8)(22)(24)(26)(27)(28)(29)(30)}. Three different sensory systems contribute to balance control, and these sensory systems show age-related functional declines that may affect balance function. In addition, the way that the central nervous system organizes these sensory inputs for balance control may also show age-related modification, as a result of either deterioration in the sensory systems themselves or in compensation for losses in a specific sensory system.

One way of determining the effect of vision on quiet stance balance is to create the illusion of postural sway through visual flow created by an experimental moving room. In these experiments, the walls and ceiling of the room move, while the floor remains still. Young adults typically show small amounts of sway in response to visual flow simulating sway. Research by Wade and coworkers ⁽³¹⁾ compared the effects of visual flow on postural responses (COP measurements) in healthy older and young adults and found that the older adults sway more than young adults. They stated that this may be due to peripheral neuropathy in older adults, causing increased reliance on vision.

A second study by Sundermeier and colleagues ⁽³²⁾ compared the effects of visual flow on postural responses of young, and stable and unstable older adults. They found that the unstable older adults showed significantly more reliance on visual flow than the young or stable adults as measured by COP. The unstable older adults used higher levels of sheer forces when compensating for the simulated postural sway, thus suggesting higher use of hip strategies, even in response to visual perturbations to posture.

In a similar study, Ring and colleagues ⁽³³⁾ used a visual image on a screen in front of subjects to create the illusion of movement toward the subject. In these "visual push" experiments, they found that recent fallers (within 2 weeks) and remote fallers (within the last year) swayed significantly more than nonfaller older adults (ages 65–86). They proposed that the visual push test could be used in the clinic to determine if older adults are at increased risk of falling.

Studies have also examined the effects of somatosensory deficits on reactive balance control in older adults. Patients with somatosensory deficits caused by peripheral neuropathy have significant delays in muscle response onset latencies in response to platform perturbations and difficulty modulating response amplitudes in relation to stimulus size ⁽³⁴⁾.

Studies examining the contributions of the vestibular system to balance control in young adults conclude that one of the roles of the vestibular system is that of an absolute reference system to which the other sensory systems (visual/somatosensory) may be compared and calibrated ^(35)(36). A loss of vestibular function with age would cause this absolute reference to be less reliable. Thus, there would be problems dealing with conflicting information coming from the visual and somatosensory systems. This could be one factor causing older adults with vestibular deficits to have difficulty with dizziness and unsteadiness when they are in situations with conflicting visual and somatosensory information.

It may be difficult to isolate deficits in sensory organization abilities in older adults, as redundant sensory information from the three sensory systems can mask problems in one of the senses under normal sensory conditions ⁽³⁶⁾. Thus, a number of research laboratories have used the sensory organization test to examine the ability of healthy older adults to balance efficiently under changing sensory conditions during quiet stance ^{(22)(24)(26)(29)}. These studies examined postural sway under six conditions: 1, vision normal; 2, eyes closed; 3, visual surround sway-referenced (movement correlated with body sway); 4, platform sway-referenced/eyes open; 5, platform sway-referenced/eyes closed; and 6, platform and visual surround sway-referenced.

Results from this research showed that healthy active older adults did not have significant differences from young adults in body sway, except when both ankle joint inputs and visual inputs were distorted or absent (conditions 5 and 6). Under these conditions 30% to 50% of the older adults lost balance or took a step on the first trial ^(22)(27). On the second and/or third trials, the balance of the older adults improved significantly. This suggests that healthy active older adults are able to adapt senses for postural control, but only with practice in conditions with reduced or conflicting sensory inputs.

	Age-Related Changes in Cognitive Systems

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As may be implied from the results of the previously described research on balance in the older adult, historically, age-related instability has been thought to be caused by decreases in the function of the sensory or motor systems. However, recent studies indicate that there may be other sources of instability including cognitive and, specifically, attentional allocation deficits. Postural control has often been thought of as an automatic or reflexly controlled task and thus was expected to use minimal attentional resources. However, more recently, scientists have discovered evidence against this assumption. In the following section, we will review current research on attentional requirements of postural control and changes in these requirements in older adults.

The types of experimental paradigms used to study attentional allocation process are dual task paradigms. In these paradigms, two tasks (postural plus secondary task) are performed together, and the extent to which the performance on either task declines indicates the extent to which the two tasks share attentional resources ⁽³⁷⁾.

As has been summarized in earlier sections of this editorial, it is clear that there are age-related reductions in stability in many older adults. But are these age differences in stability increased with added cognitive demands? Recently, Maylor and Wing ⁽³⁸⁾ performed a study to determine the types of cognitive demands that increase postural sway in older adults. Healthy older and young adults stood quietly (primary task) while performing the following types of secondary cognitive tasks intended to test different aspects of working memory: (i) a random digit generation task, testing central executive function; (ii) Brook's spatial memory task, testing what could be called a visual-spatial sketch-pad (VSSP) function; (iii) backward digit recall, testing the phonological loop and VSSP; (iv) silent counting, test the phonological loop; and (v) counting backwards by threes, testing the phonological store of the phonological loop.

Younger adults performed significantly better than older adults on all the cognitive tasks except silent counting; in addition, they were more stable than the older adults throughout the tasks. Age-related decreases in stability were greatest for the Brook's spatial memory task and backward digit recall during the dual task situation. Maylor and Wing concluded that age-related differences in balance were increased by cognitive tasks involving the visual-spatial sketch pad part of working memory. They proposed that this could be due to an increased reliance on vision for postural control by older adults as a result of proprioceptive and/or vestibular loss ⁽³⁸⁾.

If postural control requires attentional processing, it is possible that decreasing sensory information would demand more attention. Thus, older adults could show more difficulty than young adults under these circumstances. Teasdale and coworkers ⁽³⁹⁾ studied the balance (COP measurements) of young (mean age, 24 years) and older (mean age, 71 years) adults while sitting (control condition) and standing with eyes open versus eyes closed on a normal surface versus a foam surface. The foam surface decreased sway-related somatosensory information available for balance control. The researchers measured reaction time (RT) on a secondary task (a button press at the sound of an auditory cue). As sensory information decreased, RT became significantly longer for older adults compared with young adults, suggesting that the amount of attention is dependent on the degree of instability associated with the task.

To determine how performing an attentionally demanding task affects postural sway in young, and healthy older and balance-impaired older adults, Shumway-Cook and coworkers ⁽⁴⁰⁾ examined the ability of these subjects to perform postural tasks of varying difficulty (standing on a normal surface vs foam) while performing cognitively demanding secondary tasks. They found that there were decrements in performance in the postural stability measures, rather than the cognitive measures, for young adults, and healthy older and balance impaired older adults. Differences between the young and healthy older adults only became apparent when task complexity was increased—either by adding the secondary task or by adding the more challenging postural condition. However, balance-impaired older adults showed problems even in less complex task conditions.

The previously described experiments examined attentional constraints on the balance performance of older adults in quiet stance situations, but it would also be important to know if recovery from balance threats requires more attention for the older adult than for the young adult. To answer this question, Brown and colleagues ⁽⁴¹⁾ asked older and younger subjects to respond to unexpected platform displacements, either with no secondary task or while performing a math task (count backward by threes). Attentional requirements for the recovery of balance were higher for the older adults compared with the young adults.

In summary, early research on balance control in older adults used mainly a global measure of sway to determine if age-related changes occurred in balance. This approach has limitations, because amount of sway during normal quiet stance is not necessarily correlated with level of balance control. More recent research has used a systems approach to study changes in the various systems contributing to reduced balance control in the older adult. Research examining changes in the motor systems contributing to reductions in the ability of older adults to recover from balance threats have shown: (i) delays in muscle onset latencies; (ii) increased coactivation of agonist and antagonist muscles at the joints, possibly to increase joint stiffness and to decrease the numbers of degrees of freedom of movement to be controlled; and (iii) problems with organization of muscle responses in some subjects. Research examining changes in the sensory systems has shown an increased reliance on visual cues for balance control (possibly due to loss of sensation in the feet and ankles) due to peripheral neuropathy. Research examining age-related changes in attentional demands associated with balance control has shown that this varies depending on the complexity of the postural task, with age-related increases in attentional demands becoming more apparent as the inherent stability demands increase.

Received March 17, 2000

Accepted April 11, 2000

	References

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