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Associations among Strength, Steadiness, and Hand Function across the Adult Life Span

MARMON, ADAM R.1; PASCOE, MICHAEL A.2; SCHWARTZ, ROBERT S.3; ENOKA, ROGER M.2

Author Information
Medicine & Science in Sports & Exercise: April 2011 - Volume 43 - Issue 4 - p 560-567
doi: 10.1249/MSS.0b013e3181f3f3ab

Abstract

The neuromuscular mechanisms responsible for the decline in motor function with advancing age have been difficult to identify because of the constraints that are necessary to obtain experimental indices of motor performance. As an index of fine motor function, for example, tests of steadiness typically require an individual to exert a constant submaximal force during an isometric contraction of an isolated muscle or group of muscles, which may have limited functional relevance. Although the fluctuations in force during such steady contractions vary with contraction type (4,11,19), contraction intensity (2,4,10,31), and age (10,11,31), few studies have examined the functional significance of these fluctuations in the force (5,26).

Furthermore, steadiness is often measured during tasks that involve few agonist and antagonist muscles, such as abduction/adduction of the index finger (10,17,19,32,33), so that there is a more direct association between the activation signal sent from the nervous system and the resulting mechanical output. Even the simplest everyday task, however, rarely involves such isolated actions, which begs the question of whether or not differences in the steadiness of experimental tasks are associated with differences in functional capabilities. The aim of this study was to investigate the associations among measures of strength, steadiness, and fine motor function of hand muscles across the adult life span.

METHODS

Seventy-five subjects (18-89 yr; 45 women) participated in the study after informed consent was obtained. The sample was categorized into three groups of 25 subjects each: young (18-36 yr; 11 women), middle-aged (40-60 yr; 17 women), and old (≥65 yr; 17 women) adults. All subjects were free from neurological disease and were not taking any medications that are known to influence neuromuscular function. The Human Research Committee at the University of Colorado in Boulder approved the procedures.

Procedures.

Each subject participated in one session that lasted ∼2.5 h. After providing informed consent, the handedness of each participant was quantified using the Edinburgh Handedness Inventory (25). Subjects then completed tests to assess strength, steadiness, and hand function with the dominant and nondominant hands. The order of testing strength and steadiness, functional tasks, and hand was counterbalanced across subjects.

Strength and steadiness tests.

Strength was measured as the maximal force that each participant could produce during index finger abduction, a precision pinch task involving the index finger and thumb, and a handgrip task. Steadiness was quantified as the fluctuations in force during steady, submaximal contractions as participants exerted an abduction force with the index finger using the first dorsal interosseus muscle (FDI) or pinched a load cell between the padding of the thumb and index finger (pinch). Index finger force was measured with subjects seated comfortably in a chair with the shoulder abducted by about 45°, the elbow extended slightly past 90°, and the forearm resting on a table. The palm of the hand was horizontal and strapped to a board that limited movement to index finger abduction about the metacarpophalangeal joint (Fig. 1A). The index finger was fitted with an orthotic that made contact with the load cell at the radial border of the proximal interphalangeal joint. The abduction forces were recorded with low- and high-sensitivity transducers (0.021 and 0.436 V·N−1, respectively; Model 13; Sensotec, Columbus, OH) to provide a sufficiently high signal-to-noise ratio over the range of forces measured in the protocol.

F1-2
FIGURE 1:
Experimental setups that were used to measure hand steadiness and function. Steadiness: index finger abduction (A) and precision pinch (B). Function: Grooved Pegboard (C), OperationTM (D), star cutout (E), and Archimedes spirals (F).

Pinch forces were recorded with a force transducer (0.090 V·N−1; Mini-40; ATI Industrial Automation, Apex, NC) mounted between two cylinders that were 2.5 cm in diameter. The length of the device was 4 cm, and it was held between the padding of the thumb and index finger. The forearm was in a neutral posture with the styloid process of the ulna resting on the edge of the testing table and digits three to five flexed into the palm (Fig. 1B). Handgrip strength was obtained using a handgrip dynamometer (Hydraulic Hand Dynamometer; Baseline Evaluation Instruments, Irvington, TX) and was always the final measurement during the strength and steadiness tests. Subjects were seated upright in a chair for the handgrip measurement with the arm to the side and the elbow flexed to 90°.

The peak force was measured for the three tasks during maximal voluntary contractions (MVC). Subjects were instructed to increase the force from rest to maximum gradually during ∼3 s and to hold that maximum for ∼2 s. Subjects were provided with verbal encouragement during each MVC and rested for 1 min between trials. Feedback for the index finger abduction and pinch MVC was provided in real time on a 17-inch computer monitor placed 1.2 m in front of the subject at eye level. Subjects completed two to five trials of the abduction and pinch tasks, with the greatest force generated from these trials taken as the MVC. To ensure reliable measurement of the maximal force, the peak force had to be within 5% of the value recorded in another trial. Force data were sampled at 1 kHz using an analog-to-digital converter (Power 1401; Cambridge Electronic Design, Cambridge, UK) and stored on a computer for offline analysis. The maximal handgrip strength was taken as the greatest force exerted during three trials.

Force steadiness was measured during both the index finger abduction and pinch tasks. Each task involved maintaining an isometric contraction at a target force of 5% MVC for 60 s. Feedback was provided using custom software (LabVIEW version 8.2; National Instruments, Austin, TX) that displayed the target force and the force exerted by the subject intermittently (5 s with feedback and 5 s without) with a feedback gain of 1.4% MVC per centimeter. The target force was displayed as a white line on a black background, and the force exerted by the subject was shown as a red line. All subjects affirmed that they were able to see both lines.

Functional tests.

Hand function was evaluated with four tasks: Grooved Pegboard, the game OperationTM, star cutout, and Archimedes spirals. Subjects were instructed not to support their elbows on the table or chair during any of the functional tests. The Grooved Pegboard (Lafayette Instruments, Lafayette, IN) test required subjects to place small metal pegs into holes on a board as quickly as possible. The other functional tests were all performed at self-selected speeds. The pegboard had 25 holes arranged in five rows by five columns. The pegs and holes had a key-hole shape, and the orientation of the 25 holes varied across the board (Fig. 1C). Any peg could fit into any hole but only when the orientation of the two key-hole shapes was aligned. Subjects were instructed to fill the entire board one row at a time from top to bottom. The rows were filled starting on the right for the left hand and on the left for the right hand. All subjects completed three trials with each hand.

OperationTM (Hasbro, Pawtucket, RI) is a board game that consists of 13 small plastic pieces of varying shapes and sizes placed inside similarly shaped cavities cut into a game board. The task was to use metal tweezers to remove the pieces of plastic from the game board without touching the sides of the cavity or dropping the piece of plastic (Fig. 1D). When the metal tweezers made contact with the cavity lining, a light on the game board was illuminated; the vibrating mechanism that is a standard feature of the game was disconnected during testing. Subjects were provided with up to three attempts to remove each of the 13 pieces without making an error (touching or dropping). The game was performed once with each hand.

The star-cutout task involved subjects using a pair of ambidextrous scissors (Fiskars Manufacturing, Wausau, WI) to cut around a five-pointed star (83 × 106 mm2) printed on a piece of paper (153 × 109 mm2). The star comprised parallel lines that were 3 mm apart. The task, completed once with each hand, was to cut out the star by staying between the two lines (Fig. 1E).

The Archimedes spirals task involved tracing model spiral printed on a piece of paper that was taped to the tabletop (Fig. 1F). The subject was instructed to match the model spiral as accurately as possible, without allowing the pen to leave the paper once the tracing began. The task began in the center of the spiral and moved toward the periphery. Each subject completed three spiral tracings with each hand (see Supplemental Digital Content 1, https://links.lww.com/MSS/A52, for more detail on the analysis).

Data analysis.

Steadiness was quantified over selected segments of the force record from the 60-s plateau of each trial (Fig. 2). The plateau was subdivided into six 10-s sweeps; each sweep consisted of 5 s with feedback and 5 s without. The first and last sweeps were discarded, and the analysis was performed on the middle four sweeps. The last 2.3 s of the feedback segment and the first 2.3 s of the no-feedback segment were analyzed, excluding a 600-ms transition period between conditions. Force steadiness was quantified as the coefficient of variation for force.

F2-2
FIGURE 2:
Force segments used to measure steadiness. Each steadiness trial consisted of six 10-s sweeps, where feedback was intermittently presented (5 s with and 5 s without). The last 2.3 s of the feedback condition and the first 2.3 s of the no-feedback condition, excluding a 0.6-s transition period, were averaged across the middle four sweeps.

Pegboard performance was expressed as the time needed to fill all 25 holes of the pegboard. The outcome measure was the average across the three trials for each hand. The performance score for OperationTM was the sum of the number of attempts needed to remove all 13 game pieces: 1.00 point on the first attempt, 0.66 on the second attempt, 0.33 on the third attempt, and 0 if not removed. Star-cutout performance was indicated as the number of cuts across either the inner or the outer border of the star. The outcome measure for Archimedes spirals was the SD of the trace radii relative to the model radii. To achieve this measure, each trace was scanned and digitized, and Cartesian coordinates were assigned to each data point so that the length of each radius could be quantified. The SD for the three traces from a given hand was averaged.

To examine the differences in performance among the three age groups (young, middle-aged, and old), one-way ANOVAs were performed on a composite score (average of dominant and nondominant hands) for each dependent variable. The associations between strength, steadiness, and function were examined by calculating Pearson's correlation coefficients that compared measures within and across test series. Stepwise multiple regression models were developed to identify those measures that best predicted performance in each function and steadiness task. In addition, analyses of covariance tests were performed with the significant regression models to determine whether there were differences in predictability across the three age groups. All statistical procedures were performed with SPSS Statistics (version 16.0.1; SPSS, Inc., Chicago, IL). The α level for all statistical analyses was set at 0.05, and all data are presented as the mean ± SD in the text and tables and as mean ± SE in the figures.

RESULTS

Measurements were obtained from 75 subjects as they performed three tests of strength, two tests of steadiness, and four tests of function with both their dominant and nondominant hands. There were significant differences in strength, steadiness, and function across the adult life span (Table 1) and significant associations between some of the measures (Table 2). The maximal force exerted during both pinch and index finger tests was significantly greater for young adults compared with old adults. Similarly, young adults performed better in all four functional tasks and both steadiness tasks when compared with old adults. The young and middle-aged adults only differed in Grooved Pegboard performance, whereas the middle-aged and old adults were significantly different for both steadiness tasks and for three of the four functional tasks (star cutout, OperationTM, and Pegboard). Significant multiple regression models suggested that steadiness was more strongly associated with, and consequently a better predictor of, functional performance than was strength.

T1-2
TABLE 1:
Descriptive statistics.
T2-2
TABLE 2:
Multiple regression analyses.

Age-related differences.

The old adults were significantly weaker than the young adults in all three strength tests: grip, pinch, and index finger (Table 1; differences of 30.3%, 18.0%, and 19.8%, respectively, P < 0.05). However, the old adults were not weaker than the middle-aged adults (differences of 17.8%, 6.7%, and 13.6%, respectively, P ≥ 0.078), and the middle-aged adults were not weaker than the young adults for any of the three tests (differences of 15.1%, 12.1%, and 7.1%, respectively, P ≥ 0.080).

The fluctuations in force (steadiness) for both the index finger and pinch tasks were significantly greater during the visual feedback condition compared with the no-feedback conditions (P ≤ 0.001). As subjects received visual feedback during the strength and function tests, the steadiness data reported here are for the feedback condition only. However, similar differences across age groups were observed in steadiness performance during the no-feedback condition (Supplement Digital Content 2, https://links.lww.com/MSS/A53). The old adults were significantly less steady than both young and middle-aged adults for both the pinch (P ≤ 0.003) and index finger (P < 0.001) steadiness tests (Table 1). For example, the coefficient of variation for force during the index finger test was 4.8% ± 2.9% for the old adults compared with 2.2% ± 0.9% for young and 2.7% ± 1.1% for middle-aged adults. The steadiness performance for the young and middle-aged adults was similar for both tests (P ≥ 0.09).

The time needed to complete the Grooved Pegboard test differed across all three age groups (Table 1): old adults (88.9 ± 15.7 s) required more time than both the young (59.3 ± 6.0 s, P < 0.01) and middle-aged adults (65.7 ± 8.6 s, P < 0.001), and the middle-aged adults needed significantly more time than the young adults (6.4 s, P = 0.021). The old adults had lower scores for OperationTM and more errors in the star cutout when compared with both the young and middle-aged adults (P < 0.001 and P < 0.05, respectively). The young and middle-aged adults had a similar performance in both tests (P = 0.300 and P = 0.963, respectively). The SD of the trace radii relative to the model radii during the Archimedes spirals test were only significantly different between the young and old adults (0.40 ± 0.09 and 0.71 ± 0.84 mm, respectively, P = 0.008). The middle-aged adults (0.49 ± 0.21 mm) were not significantly different from either the young (P = 0.657) or old adults (P = 0.074).

Associations among tests.

There were significant associations among similar tests and between the different tests. For example, the three strength measures were correlated with each other (r ≥ 0.71, P < 0.001), as were the two steadiness measures (r = 0.532, P < 0.001) and the four function measures (absolute r ≥ 0.258, P < 0.05) except for star cutout and Archimedes spirals (r = 0.113, P = 0.168). Comparisons of the strength tests with the steadiness tests revealed significant negative correlations between the three strength measures and pinch steadiness (r ≤ −0.50, P < 0.001), but index finger steadiness was only significantly correlated with grip and index finger strength (r < −0.27, P < 0.01) and not pinch strength (r = −0.132, P = 0.130). Comparisons of the strength tests with the functional tests produced significant positive correlations between the three strength tests and the Grooved Pegboard test (r ≤ −0.20, P < 0.05) and significant negative correlations with OperationTM task (r ≥ 0.38, P < 0.001). However, none of the strength tests were significantly correlated with star-cutout performance (absolute r < 0.117, P ≥ 0.158), and Archimedes spirals was only significantly correlated with grip strength (r = −0.204, P = 0.040) and not with pinch or index finger strength (P > 0.104).

Associations between function and steadiness were significant for performance in the Grooved Pegboard test and OperationTM task with both pinch and index finger steadiness (P < 0.001). Pinch steadiness was also correlated with performance in the star cutout (r = 0.225, P = 0.026) and Archimedes spirals (r = 0.294, P = 0.005), but index finger steadiness was not correlated with either test (P ≥ 0.069).

Predictability of performance.

Multiple regression models were developed to identify the tests that best predicted performance on each of the four functional tests (Table 2). Two of the models were significant: the Grooved Pegboard and OperationTM (Fig. 3, A and B). Time to complete the Grooved Pegboard test was significantly predicted (R2 = 0.36, P = 0.044) by index finger steadiness and grip strength. The scores achieved when performing OperationTM were significantly predicted (R2 = 0.40, P = 0.049) by pinch steadiness, index finger steadiness, and grip strength.

F3-2
FIGURE 3:
Predictions of performance for young, middle-aged, and old adults based on stepwise multiple regression analysis. The times taken to complete the Grooved Pegboard test (A) were predicted with the data for grip strength and index finger abduction steadiness. The OperationTM scores (B) were predicted with the data for grip strength, pinch steadiness, and index finger abduction steadiness. Precision pinch steadiness (C) was predicted with the data for index finger abduction strength and the performance scores for OperationTM. Steadiness during index finger abduction (D)was predicted with the data for pinch and index finger abduction strength and performance times for the Grooved Pegboard test.

Conversely, pinch steadiness was significantly predicted (R2 = 0.46, P < 0.001) by the scores for OperationTM and index finger strength (Fig. 3C). Index finger steadiness was significantly predicted (R2 = 0.43, P = 0.022) by the time to complete the Grooved Pegboard test, pinch strength, and index finger strength (Fig. 3D).

Differences in the significant multiple regression models across the three age groups were evaluated using analysis of covariance. There were no significant interactions in the models predicting Grooved Pegboard performance, OperationTM performance, pinch steadiness, or index finger steadiness, indicating that the predictability of performance in these tests did not differ across the adult life span.

DISCUSSION

The goal of the study was to examine the associations between experimental measures of hand function across the adult life span. The main findings were that the fluctuations in force during steady contractions with hand muscles were moderately associated with performance on functional tests and these associations were maintained across the adult life span. Furthermore, steadiness performance was more strongly associated with measures of fine motor function than with those of strength.

Strength.

Progressive declines in strength were observed across the adult life span for all three strength measures (grip, pinch, and index finger abduction), which agrees with previous studies (16,21). However, statistical differences in strength were only observed between the young and old adults. The middle-aged adults were not statistically different from either the young or the old adults, but their strength was between that for these two groups for all three measures, which indicates that the progressive loss of strength for hand muscles did not reach statistical significance until old age in this cohort. The reduced index finger abduction strength exhibited by old adults relative to young adults in the current study (19.8%) was similar to the difference observed by Kamen et al. (17) (19.2%). The reductions in index finger abduction strength were more similar to the changes in pinch strength than grip strength (18.0% and 30.3%, respectively); however, it is not apparent what factors may have accounted for the differences in strength decline among these three tasks.

When analyzing data from the Cardiovascular Health Study (9), Hirsch et al. (13) found significant correlations between anthropometric variables and strength, suggesting that strength loss is primarily due to reductions in muscle mass. Other studies, however, have found that changes in the contractile properties of muscle (e.g., normalized force, contraction time, half relaxation time) (21,27,34) cannot explain the entire age-related decline in strength (15,23). Rather, some features of muscle activation also seem to contribute to the decrease in strength. Older adults, for example, exhibit greater levels of antagonist coactivation compared with young adults (22), which, while helping to stabilize the joint, also reduces the net torque exerted about a joint. The greater-than-necessary amount of coactivation used by older adults is underscored by the decline in antagonist coactivation after participation in a training protocol (12). Furthermore, improvements in strength after training have been associated with increases in agonist muscle activation (12,23), which can be attributed to increased motor unit activity (24,28). Therefore, age-related differences in strength are due not only to changes in the size and quantity of muscle but also to changes in muscle activation.

Steadiness.

Consistent with previous studies (10,11), the magnitude of the normalized force fluctuations was greater for old adults than for young adults during the constant-force contractions for both the pinch and index finger tasks. Furthermore, the present study also showed that old adults were significantly less steady compared with middle-aged adults in both tasks, whereas the middle-aged adults were not statistically different than the young adults. The features of the motor output from the spinal cord that are responsible for differences in steadiness have not been fully elucidated but are likely to include changes in the average motor unit force (10), antagonist coactivation (14), and motor unit discharge variability (1). Although visuomotor processes can contribute to age-related differences in steadiness, the associations with hand function in the current study were similar for the feedback and no-feedback conditions (Supplemental Digital Content 3, https://links.lww.com/MSS/A54). As previous studies have shown (18,20,30), however, strength training can reduce the fluctuations in force during steady contractions well before muscle hypertrophy can occur (8,24,28), which suggests that differences in steadiness are likely due to alterations in muscle activation.

Function.

The four measures of hand function chosen for this study were intended to examine different aspects of hand function, including a clinically validated task (Grooved Pegboard) (29), a novel task similar to the experimental pinching task but more complex (OperationTM), and two more common tasks: writing (Archimedes spirals) and scissor use (star cutout). The selected tasks had a diverse set of requirements, but speed was not the primary component of each measure.

A consistent finding in all four tasks was that the old adults exhibited statistically poorer performance than young adults (P < 0.05). Statistical differences between young and middle-aged adults, however, were only observed for the Grooved Pegboard test (P = 0.021), whereas the middle-aged adults performed statistically better than the old adults did during the Grooved Pegboard (P < 0.001), OperationTM (P < 0.001), and star cutout (P = 0.034) tasks but not the Archimedes spirals (P = 0.074). These findings suggest that hand function is impaired in old adults, even for tasks that do not depend on speed. However, the only task that showed statistical differences across all three age groups was the Grooved Pegboard. The Grooved Pegboard test, therefore, should be considered the most appropriate test of the four examined for quantifying changes in hand function across the adult life span. Moreover, the National Institutes for Health is currently developing a "toolbox" intended to encompass a group of assessment tools that can be used in a variety of setting and across the life span, and the Grooved Pegboard test is being considered as the measure of manual dexterity.

Associations among strength, steadiness, and function.

There were significant associations among all three measures of strength (P < 0.001) and the two measures of steadiness (P < 0.001). Together, these findings suggest that measures of strength and steadiness within a given individual are similar for different hand postures. The four measures of hand function were also correlated with one another (P < 0.05), with the exception of the association between Archimedes spirals and star-cutout tasks (P = 0.168), suggesting parallel changes the various characteristics of hand function that change with age. Included in these characteristics are speed of movement (3), tactile sensitivity (6), and coordination of muscle activity (7).

This study is not the first to show an association between strength and function (3); however, a novel finding from the current study is the association between measures of steadiness and function. Namely, experimental measures of pinch steadiness were significantly correlated with functional performance in the Grooved Pegboard test (P < 0.001), Operation task (P < 0.001), and Archimedes spirals (P = 0.011). Similarly, steadiness during index finger abduction was also significantly correlated with performance in the Grooved Pegboard test and OperationTM task (P < 0.001). Furthermore, the associations of measures for the Grooved Pegboard test and OperationTM task were stronger with measures of steadiness than measures of strength. For example, the Pearson correlation coefficient for Grooved Pegboard time and pinch steadiness was larger (r = 0.464, P < 0.001) than the correlation coefficients for Grooved Pegboard test and grip strength (r = −0.342, P = 0.003), pinch strength (r = −0.197, P = 0.091), and index abduction strength (r = −0.252, P = 0.029). These data suggest that steadiness measures may be more strongly associated with functional hand measures than measures of hand muscle strength. Moreover, the results of the multiple regression analyses identified steadiness as the better predictor of performance for the Grooved Pegboard test and Operation task than strength measures.

In conclusion, the observed associations between strength, steadiness, and function of hand muscles were not statistically different across the three age groups examined. Therefore, measures of steadiness comprise an adequate index of hand function and, when complemented by other neurophysiological recordings, can provide insight into the mechanisms responsible for age-related differences in motor performance.

Funding received for this work was from the National Institutes of Health. This work was supported by AG09000 to R. M. Enoka and T32 AG00279 awarded to R. Schwartz that supported A. R. Marmon and M. A. Pascoe.

The authors have nothing to disclose.

The authors thank Greg Carey for statistical support.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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Keywords:

FORCE CONTROL; AGING; MUSCLE; GROOVED PEGBOARD

Supplemental Digital Content

©2011The American College of Sports Medicine