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Age-associated differences in sensori-motor function and balance in community dwelling women.

Summary

Tests of visual, vestibular, sensori-motor and balance function were administered to 550 women, aged between 20 and 99 years at a Balance and Gait Laboratory. All of the sensory, motor and balance system measures showed significant age-associated differences. Multiple regression analyses revealed that the measures of lower limb sensation were the consistent sensori-motor factors contributing to balance under normal conditions (standing on a firm surface with eyes open or closed). Under more challenging conditions (standing on foam with eyes open) vision, strength and reaction time played significant roles, whilst when standing on foam with eyes closed, vestibular function also made a significant contribution. Analysis of percentage increases in sway under conditions where visual and peripheral sensation systems were removed or diminished, compared with sway under optimal conditions, indicated that up until age 65 there was an increased reliance on vision for balance control. Beyond this age, the contribution made by vision declined, so that in the oldest age-groups reduced vision was less able to supplement peripheral input, resulting in increased sway areas. Peripheral sensation however was the most important sensory system in the maintenance of static postural stability at all ages.

Introduction

In recent years there has been considerable interest in elucidating the contributions made by visual, vestibular and somatosensory systems to balance control in young and elderly persons. Researchers have addressed this problem in two ways: by assessing correlations between specific sensory systems and measures of stability such as body sway and by experimentally manipulating sensory inputs so as to determine the degree to which such interventions affect stability.

Most studies that have assessed associations between sensory systems and increased body sway on firm surfaces have shown that impaired vibration sense shows the strongest correlation [1-4]. Whilst a number of studies have not found a significant association between impaired proprioception and increased body sway, this could be because of the acknowledged imprecision of the clinical tests used [2, 4]. In a previous study of hostel residents, Lord et al. found that both reduced proprioception as measured quantitatively and tactile sensitivity were related to increased sway [5]. Only one study, that by Lichtenstein et al., has reported a significant association between vision (near visual acuity) and sway [6], whilst a number of reports have found negligible associations between vestibular function and sway [2, 5, 7].

Lord et al. have extended this work by examining which sensory and motor factors are associated with sway when peripheral input has been altered, that is by having subjects stand on a compliant (foam rubber) surface. Under this condition with eyes open, reduced vision and strength, in addition to impaired peripheral input, were significantly associated with increased sway, whilst under this condition with eyes closed, strength and reaction time played significant roles [5].

With regard to experimental manipulations of the sensory systems, elimination of vision, simply by having subjects close their eyes, is by far the easiest intervention. In addition, the extent to which induced partial visual loss affects stability has been examined [8-11]. In contrast, sensory input from the lower limbs and vestibular function are harder to manipulate experimentally and in a number of cases unpleasant for subjects. Techniques used for reducing sensory input from the legs have included ischaemia induced by cuffs at the level of the ankle and thigh [I 2, 1 3], cooling the feet in ice water [14] and having subjects stand on foam rubber [5, 8, 15, 16] and platform surfaces that rotate co-axially with the ankle joints [9, 17]. The functioning of the vestibular system has been minimized by head tilt [10, 11] and by having subjects perform an 'equivalent person task' in which subjects must balance a freely moving weight (equivalent to their own body weight) attached to a platform with an axis of rotation identical to that of the ankles, and adjust its position with the feet while movement of the head is precluded [18]. These studies have revealed that sway is increased when any sensory input is removed or altered and more so if two sensory inputs are altered concurrently.

Significant declines in all the major sensory and motor inputs that contribute to balance with age have been reported [19-26], although it has not been shown whether there are variable rates of decline among these systems and in consequence whether there are age-associated changes in the importance of each of these sensory systems to balance control. In a previous paper, sensory and motor contributions to stability were examined in elderly institutionalized subjects [5]. In this paper, we examine these sensori-motor, vestibular and visual systems in a large community population of women to determine whether there are age-associated differences in the contributions made by the sensory inputs to balance control.

Methods

Subjects: Five hundred and fifty women comprised the study sample. The 414 subjects aged 65 years and over (mean age 73.6 years, SD 6.3) were drawn from the Randwick Falls and Fractures Study [27]. These women, who were living in private households, were recruited from randomly selected Australian Bureau of Statistics districts in the Municipality of Randwick, in Sydney, Australia. All women in the target age group living within these districts (who were identified using extracted information from the electoral roll) were invited to take part in the study. The only exclusion criteria were not living at the dwelling at the time of the study or having no or very little English. Participation was voluntary and informed consent was sought at the commencement of the study.

The number and percentage of women in five-year age groups in the study population and in the Randwick local government area as a whole are shown in Table I. The sample was over-represented in the age group 75-79 years and under-represented in the age groups 80-84 years and 85 years and over. The under-representation in the oldest age groups was most likely due to higher proportions of women in these age groups in the reference population living in hostels and nursing homes [27]. A full description of the sample characteristics and recruitment procedures for the Randwick Falls and Fractures study has been reported elsewhere [27].

Table I. Age distribution of the study sample and women aged 65 years and over in the Randwick Local Government Area
Age group    Study sample    Randwick LGA

65-69         133(32.1)       2835(30.0)
70-74          98(23.7)       2269(24.0)
75-79         114(27.5)       1964(20.8)
80-84          47(11.4)       1328(14.1)
85+             22(5.3)       1043(11.0)

Total        414(100.0)      9439(100.0)


In addition, 136 women aged 20-64 years comprised a younger sample. These women were generally a convenience sample although most of the women aged 55-64 were also randomly recruited from the community. The younger sample was selected so as to include at least 20 subjects per decade. In all, the sample comprised 23 women aged 20-29 years, 20 aged 30-39 years, 20 aged 40-49 years, 30 aged 50-59 years, 43 aged 60-64 years, 133 aged 65-69 years, 98 aged 70-74 years, 114 aged 75-79 years, 47 aged 80-84 years and 22 aged 85 years and over.

Sensori-motor function assessments: The test battery included nine tests of individual sensory and motor systems and five 'composite' tests of reaction time and stability. The sensory and motor tests included three visual tests: high and low contrast visual acuity and contrast sensitivity; three tests of sensation in the leg - touch thresholds at the ankle, vibration sense at the knee and a test of proprioception; two tests of vestibular function - the vertical X writing test and a test of vestibular optical stability; and quadriceps strength. The composite tests included a test of reaction time, and tests of body sway on firm and compliant (foam rubber) surfaces.

Visual acuity was measured using a dual visual acuity contrast chart [28]. This chart consisted of a high-contrast visual acuity letter chart (similar to a Snellen scale) and a low-(10%) contrast letter chart (where contrast = the difference between the maximum and minimum luminances divided by their sum). Acuity was measured binocularly for both high-and low-contrast scales with subjects wearing their best correction spectacles at a test distance of 4 metres. Visual acuity was measured in terms of logarithm of the minimum angle resolvable (MAR) in minutes of arc. Low-contrast acuity was then compared with high-contrast acuity. This difference was also measured in terms of the logarithm of the minimurn.angle resolvable [281.

Contrast sensitivity was assessed using the `Melbourne Edge Test', a non-grating test specifically designed for screening purposes [20]. The test presented 20 circular patches containing edges with reducing contrast. Correct identification of the orientation of the edge allowed a measurement of contrast sensitivity expressed in decibel units, where dB = - 10 [log.sub.10] Contrast.

Touch thresholds were measured with a Semmes-Weinstein Pressure Aesthesiometer [29]. This instrument contained 20 nylon monofilaments of equal length, but varying in diameter. The filaments were applied to the centre of the lateral malleolus and measurements were expressed in logarithms of milligrams pressure.

Vibration sense was measured using an clectronic device capable of generating a 200 Hz vibration of varying intensity. The vibration was applied to the tibial tuberosity and was measured in microns of motion perpendicular to the body surface.

Proprioception was tested using apparatus based on a design by De Domenico and McCloskey [30). Subjects, with their eyes closed, attempted to place the big toe of each foot simultaneously at the same position but opposite side of a vertical perspex sheet. Any difference in matching was measured in degrees.

Vestibular sense was assessed using two tests: the Vertical X Writing Test and a test of vestibulo-ocular stability. The Vertical X Writing Test measured subjects' ability to write columns of `X' characters for up to 20 cm down a vertically mounted piece of paper [5, 31]. For this test subjects sat at a desk with a blank piece of paper mounted vertically in front of them. The arms and body were kept free of contact with the desk or paper and only the pencil tip was allowed to touch the paper. The subjects performed the task with eyes open once, and then five times with the eyes closed. Any vertical deviation was determined by drawing a line from the centre of the X character to the centre of the bottom X character and measuring the angle between this line and the vertical plane. The average angle of deviation from the vertical for the five trials undertaken with the eyes closed was used as the test measure. Stoll found that performance in this test discriminated between healthy persons and those with vestibular lesions, with the vestibularly impaired subjects showing marked deviations from the vertical [32]. He suggested that this simple test can be used for objective identification of vestibulo-spinal deviation.

The Vestibular-optical Stability Test measured any difference between visual acuity at rest and while walking on a treadmill, recorded in logarithms of visual angle.

Quadriceps strength was measured in the sitting position. A strap (which was connected to a spring gauge) was placed around the subject's dominant (stronger) leg. A measure of maximal quadriceps strength was obtained when the subject attempted to extend her leg against the pull of the gauge. Strength was measured in kg and adjusted for body size by dividing the measure by the height of the subject.

Reaction time was assessed with a simple reaction time paradigm, using a light as the stimulus and depression of a switch (by the hand) as the response. A reaction time paradigm using hand movement as the response (rather than a movement by the foot) was used in an attempt to obtain a measure of reaction time that emphasized the decision time component, rather than the movement time component. This was done to gain an indirect measure of central nervous system processing speed. Reaction time was measured in milliseconds.

Sway was measured using a swaymeter that measured displacements of the body at the level of the waist. The device consisted of a rod attached to the subject at waist level by a firm belt. The rod was 40 cm in length and extended behind the subject. A sheet of graph paper (with a millimetre square grid) was fastened to the top of an adjustable-height table which was positioned behind the subject. The height of the table was adjusted so that the rod was in a horizontal plane and the tip of a pen4attached to the end of the rod) could record the movements of the subject on the graph paper. Testing was performed on a firm surface:e (a linoleum covered floor) and on a piece of foam rubber (70 cm x 62 cm x 15 cm thick) with the subject standing in the centre. The same test was repeated on both surfaces with the subject's eyes closed. The foam rubber was used to reduce proprioceptive input from the ankles and cutaneous inputs from the soles of the feet so that subjects would be required to rely on visual and vestibular cues to maintain a steady stance. Four testing conditions were employed: condition A - firm surface, eyes open; condition B - firm surface, eyes closed; condition C - compliant surface, eyes open; and condition D - compliant surface, eyes closed. (The mechanical characteristics of the foam were such that it was compressed to 9 cm when a 50 kg weight was applied equally across its surface.) Total sway (number of square millimetre squares traversed by the pen) in the 30-s periods was recorded for the four test conditions. Subjects who could not perform the sway tests on the foam because of poor balance were given scores equal to three standard deviations above the mean score for these measures.

Full descriptions of the apparatus and procedures along with test-retest reliability scores (and confidence intervals) for the test measures have been reported elsewhere [5].

Statistical analysis: The sensory, motor and body-sway test measures were coded as continuous variables. For variables with right skewed distributions (such as the vibration, proprioception, quadriceps strength, reaction time and sway measures and the vertical X writing test scores) logarithms of variables were analysed. The data were analysed using the SPSS computer package [33].

The ten specific measures of sensori-motor systems were correlated with the measures of body sway (under the four test conditions), using partial correlation analysis to control for age. Multiple regression was used to assess multivariate associations between the sensori-motor variables and the measures of sway. In these analyses, the measures of sway were the dependent variables, and the sensory and motor measures were independent (or `predictor') variables. Age was forced into the regression equations, before other variables were included using forward selection. Only one visual measure was included in the models, as all of the visual measures were strongly inter-correlated. Beta weights for each independent variable included in the regression equations and the multiple correlation co-efficients are presented. Beta weights are the coefficients of the independent variables included in the regression equation expressed in a standardized (z score) form. As the units of each measure have been standardized, the beta weights give an indication of the relative importance of each variable in explaining the variance in the dependent variable (although they do not in an absolute sense reflect the importance of the various independent variables).

Results

Mean scores for the test measures and correlations between. each measure and age are shown in Table I 1. All of the sensori-motor measures were significantly associated with age. Examination of plots revealed that linear or log-linear relationships were appropriate for describing the data for most measures. In two cases, however, i.e. vestibular optical stability to high-and low-contrast stimuli, Spearman rank correlations are reported as the distributions were j shaped (where the most frequent scores were the lowest values-indicating no error). Body weight and body mass index had curvilinear relationships with age, reaching their highest values in the sixth decade. These measures were in fact significantly positively related to age up to age 65 (weight, r = 0.31, p < 0.001; body mass index, r = 0.47, p < 0.001) and significantly inversely related beyond (weight, r = -0.30, p < 0.001; body mass index, r = -0.17, p < 0.001).

[TABULAR DATA OMITTED]

Sensori-motor correlates of sway: Most of the sensorimotor system measures were significantly associated with all four sway measures which may in part indicate concomitant ageing processes (Table III). Table IV shows the associations expressed as partial correlation coefficients, controlling for age, between the individual sensori-motor system measures and the four body sway measures. After controlling for age, poor tactile sensitivity, vibration sense and proprioception, quadriceps strength and reaction time were associated with sway on the floor conditions A and B). These measures plus vestibular sense as measured by the vestibular writing test and the four visual measures: visual acuity to high- and low-contrast stimuli, acuity difference and edge contrast sensitivity were associated with increased body sway with eyes open on the foam (condition C). Poor proprioception, vibration sense, vestibular function (as measured by the vestibular writing test), quadriceps strength and reaction time were associated with body sway, eyes closed, on the foam (condition D).

[TABULAR DATA OMITTED]

Multivariate analyses: Table V shows the sensory and motor system variables that were included in the multiple regression equations for the four sway measures (used as dependent variables). Sensory factors were found to explain most of the variance in body sway in conditions A and B (that is when subjects were standing on a firm surface with eyes open and eyes closed). Touch was included in the multiple regression equation when predicting sway with eyes open, whilst proprioception was included when predicting sway with eyes closed, with vibration sense included in both equations. Quadriceps strength was also a significant predictor for sway with eyes open.

In condition C (eyes open, on the foam), other postural control systems including contrast sensitivity, quadriceps strength and reaction time were found to be associated with sway in addition to peripheral sensation (vibration sense). In condition D (eyes closed, on the foam), lower limb strength was the most important factor in predicting sway. Other variables included were proprioception, vestibular function and age.

Visual, vestibular and peripheral contributions to stability: Table VI shows the mean amount of sway for all four conditions in eight age groups. In addition to increases in sway with age in all conditions, there were notable age-associated changes in the degree that sway increased in conditions when vision and/or peripheral input were removed or reduced compared to the baseline condition, i.e. when subjects were tested with eyes open on a firm surface. Figure 1 shows the changes in the ratios with age between conditions B, C and D and condition A.

[TABULAR DATA OMITTED]

The ratio of sway in condition B to sway in condition A showed a curvilinear association with age, in that the ratio increased from 154% in the age-group 20-39 years to a peak of 167% in the age group 65-69 years before falling to a level of only 131% in the age group 85 years and over. The ratio of sway in condition C to sway in condition A showed an exponential increase with age, in that the ratio increased gradually from 170% in the age group 20-39 years to 180% in the age group 70-74 years before increasing markedly to a level of 282% in the age group 85 years and over. The ratio of sway in condition D to sway in condition A showed a linear increase with age, increasing from 281% in the age group 20-39 years to 423% in the age group 85 years and over.

Estimates of the relative contributions of vision, peripheral sensation and vestibular sense to postural stability were made for each age group using the calculations [5]: (B-A)/B = contribution by vision, (C-A)/C = contribution by peripheral sensation, A/D = contribution by vestibular sense, where A = sway, eyes open, on floor; B = sway, eyes closed, on floor; C = sway, eyes open, on foam; and D = sway, eyes closed, on foam. Contributions are rounded so as to add to 100%. Figure 2 shows percentage contributions of each input in the eight age groups. The contribution made by vision increased up until the age group 65-69 years before declining sharply. The contribution by vestibular sense declined linearly, whilst the contribution by peripheral input increased with age. The percentage, contributions for the oldest age group (85 years and older), vision 21.2%, peripheral sensation 57.7%, and vestibular souse 21.1% are almost identical to the contributions reported previously for a hostel population (mean age = 83 years): vision 21.3%, peripheral sensation 56.3%, and vestibular sense 22.4% [5].

In the group as a whole, all four visual measures: visual acuity, low-contrast visual acuity, acuity difference and contrast sensitivity were associated with the ratio of sway in condition C to sway in condition A (r = 0.12, p < 0.01; r = 0.12, p < 0.01; r = 0.14, p < 0.01; r = -0.27, p < 0.01, respectively), indicating that those with impaired vision showed increased sway in this condition when peripheral sensation was reduced. Large vertical X writing test scores were associated with the ratio of sway in condition D to sway in condition A (r = 0.09, p < 0.05), indicating that those with impaired vestibular function showed increased sway in this condition when vision was absent and peripheral sensation reduced. In those aged 65 years and over, visual acuity was inversely associated with the ratio of sway in condition B to sway in condition A (r = -0.11, p < 0.05) and visual acuity and contrast sensitivity were inversely associated with the ratio of sway in condition D to sway in condition A (r = 0.11 p < 0.05 and r = 0.18, p < 0.01, respectively), indicating that those with visual impairment showed little difference in sway between the eyes open and eyes closed conditions.

Discussion

One of the greatest difficulties in studying the effects of ageing on postural control and mobility lies in separating the effects of ageing itself from those of the inextricably entwined disease processes and life-style processes that accompany ageing. There is a great deal of controversy concerning the actual extent of change in postural control systems and locomoter patterns with age, owing to fundamental differences among researchers in their definition of the term `the normal elderly' [34]. On one hand, one may define the normal elderly as persons free from pathology or on the other hand, one can define the normal aged subject as anyone, for example, over 60 years of age. Clearly, both perspectives on selection criteria are valid, but lead to differing results, depending whether or not pathological conditions are considered as a concomitant of the ageing process.

A major aim of the present study was to gain measures of postural control from a representative sample of subjects aged 65 years and over. Our approach to this problem has been based on the assessment of functional performance, rather than the identification of diseases or disorders, and has placed major emphasis on the quantitative measurement of visual processes, vestibular function, peripheral sensation, muscle strength, reaction time and body sway - factors outlined in our conceptual model [5] as the major body systems that contribute to balance control. Within this conceptual framework, we suggest that any debilitating medical condition (whether diagnosed or not) would be manifest by reduced functioning in one or more sensori-motor system.

Within our study population, age was significantly associated with functioning in most of the visual, vestibular and sensori-motor systems assessed. The strength of these associations is probably underestimated to some extent, however, as women aged 85 years and over were under-represented in the study sample, owing to higher proportions of women in this age group living in institutions.

Several significant associations were also found between these specific `postural control systems' and extent of body sway under various conditions. After controlling for age, increased sway when standing on a firm surface was associated with poor tactile sensitivity, vibration sense, proprioception, strength and reaction time, but not with the visual or vestibular function measures. The finding that increased sway on a firm surface is associated with a loss of sensory input from the lower limbs [1-4], but not with reduced vision or vestibular sense [2, 5, 7] is in accord with most previous research.

When the subjects were standing on the compliant (foam rubber) surface with eyes open, diminished vision as measured by all four visual measures, reduced quadriceps strength, slow reaction times and poor vestibular function as measured by the vertical X writing test in addition to the measures of peripheral sensation were significantly associated with increased sway. Thus it appears that the subjects were compelled to rely on a number of sensory and motor factors in this condition. A similar pattern was evident when vision was removed and peripheral sensation and ankle support were reduced (eyes closed, on the foam), except that, as would be expected, vision played no significant role. When standing on the foam, balance was compromised to such an extent that subjects could clearly detect their body movement. The moderate association between reaction time and sway on the compliant surface suggests that to some extent subjects made voluntary corrections to their stance.

The use of foam rubber clearly diminishes peripheral input, and as a result greatly increases body sway. Compared with alternative approaches, such as cooling or anaesthetizing the feet, or using rotating force platforms, the test is non-invasive and simple to perform. There are limitations to the method, however, in that the compliant surface does not eliminate peripheral input as shown by the positive significant correlations between proprioception, touch and vibration sense and sway on foam. Secondly, the foam also affects effector input as indicated by the significant associations between quadriceps strength and sway on foam.

The multiple regression analyses revealed that the measures of lower limb sensation were the consistent sensori-motor factors contributing to balance under normal conditions (standing on a firm surface with eyes open or closed). Under more challenging conditions (standing on foam with eves open) vision, strength and reaction time play significant roles, whilst when standing on foam with eyes closed, vestibular function also makes a significant contribution.

In many respects, the findings are in agreement with those of our previous study which was conducted in hostel residents [5]. The greater number of significant associations found in the present study most probably results from a greater range in subject functional performance in the test measures due to the much larger age range and because of increased power as a result of the large sample size. In this study an additional measure of vestibular function - the vertical X writing test - was administered to subjects. This test, while also providing only an indirect measure of vestibular function, has advantages over the vestibular stepping test (used in the previous study) and the vestibular optical stability test, in that all subjects regardless of age and balance can perform the test. Of particular interest, poor performance in this test was related to sway in condition D (eyes closed on foam), that is under the condition where vestibular function was the only sensory input left unaltered.

As in previous studies [1-6], it is evident that in spite of the significant associations described, much of the variance in the sway measures remained unaccounted for. It may be that other important factors have not been assessed, that the measures used are too insensitive to detect subtle yet significant impairments in some of the sensory and motor systems or that there is an inherent high degree of variability in the test measures. With regard to peripheral input, it has been suggested that caution should be used when assessing joint position sense in the seated position [351, because proprioceptive sensitivity at the ankle may be increased as much as ten-fold in the standing, weight-bearing position [36].

The finding that sway increases with alterations to sensory inputs is in agreement with previous research. Analysis of percentage increases in sway under conditions where visual and peripheral sensation systems were removed or diminished, compared with sway under optimal conditions indicated that up until age 65 there was an increased reliance on vision for balance control. However, beyond this age, the contribution made by vision declined. In consequence, vision was less able to supplement peripheral input, resulting in increased sway. Peripheral sensation, however, was identified as the most important sensory system in the maintenance of static postural stability across all age-groups.

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Author:Lord, Stephen R.; Ward, John A.
Publication:Age and Ageing
Date:Nov 1, 1994
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