Effects of Age and Localized Muscle Fatigue on Ankle Plantar Flexor Torque Development

King, Gregory W PhD; Stylianou, Antonis P. PhD; Kluding, Patricia M. PT, PhD; Jernigan, Stephen D. PT; Luchies, Carl W. PhD

Journal of Geriatric Physical Therapy:
doi: 10.1519/JPT.0b013e318221f53b
Research Reports

Background and Purpose: Older adults often experience age-related declines in strength, which contribute to fall risk. Such age-related levels of fall risk may be compounded by further declines in strength caused by acute muscle fatigue. Both age- and fatigue-related strength reductions likely impact the ability to quickly develop joint torques needed to arrest falls. Therefore, the purpose of this study was to investigate the combined effects of age and localized muscle fatigue on lower extremity joint torque development.

Methods: Young (mean age, 26 (2.5) years) and older (mean age, 71 (2.8) years) healthy male adults performed an isometric ankle plantar flexion force control task before and after an ankle plantar flexor fatiguing exercise. Force control performance was quantified using onset time, settling time, and rate of torque development.

Results: Age-related increases and decreases were observed for onset time and rate of torque development, respectively. A fatigue-related decrease in rate of torque development was observed in young, but not older adults.

Discussion: The results suggest performance declines that may relate to older adults' reduced ability to prevent falls. A fatigue-related performance decline was observed among young adults, but not older, suggesting the presence of age-related factors such as motor unit remodeling and alterations in perceived exertion.

Conclusions: Older adults demonstrated an overall reduction in the ability to quickly produce ankle torque, which may have implications for balance recovery and fall risk among older adults.

Author Information

1Department of Civil and Mechanical Engineering, University of Missouri–Kansas City.

2Department of Mechanical Engineering, University of Kansas, Lawrence.

3Department of Physical Therapy and Rehabilitation Sciences, University of Kansas Medical Center, Kansas City.

Address correspondence to: Gregory W. King, PhD, University, of Missouri–Kansas City, 5100 Rockhill Road, 352 RH, Flarsheim Hall, Kansas City, MO 64110 (kinggr@umkc.edu).

The authors declare no conflict of interest.

Article Outline
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A fall resulting in an injury represents a serious health challenge for older adults, particularly among those aged 65 years or older.1,2 It is well known that lower extremity strength is related to fall risk,3,4 and that maximal muscle strength decreases with age5; however, maximal strength levels are rarely used during activities of daily living (ADL). Therefore, the evaluation of submaximal force control (FC) ability may be more functionally relevant for studying age- related strength declines as they provide measures comparable to FC efforts required for ADL and for maintaining balance.6 Previous research has demonstrated that FC ability at submaximal levels of strength declines with age. For example, age increased force variability, safety margin, and error when producing knee extension79 or ankle plantar flexion10 torque to match a target level. Therefore, FC assessments are sensitive to age-related changes and may be relevant to fall risk assessment.

Physical exertion can cause temporary periods of localized muscle fatigue. The combined effects of age- and exertion-related strength declines due to localized fatigue may temporarily increase older adults' level of effort relative to the maximal strength capacity, thus reducing the ability to safely perform balance-related ADL.11,12 Although physical activity can potentially improve balance stability in the long term,13 it has negative short-term effects on postural control.1416 Such fatigue effects, coupled with known age-related declines (eg, reduced FC ability and reduced maximal strength capacity), may translate into an increased fall risk among older adults.

The ability to regain balance following a fall-provoking disturbance is likely related to the capacity for high rates of strength development and quickly initiating the onset of active FC 17,18 in addition to maximal available strength levels and the ability to accurately control submaximal levels of strength. Therefore, we selected an FC testing paradigm because it provides a controlled environment in which to quantify strength development characteristics and onset of active FC at a targeted submaximal force level.

In the following experiment, we used an FC task to investigate the combined effects of age and localized muscle fatigue on characteristics of lower extremity joint torque development. Specifically, we focused on ankle plantar flexion torque development due to the ankle's role in postural stability during standing19,20 and functional relevance for older adults.20 Furthermore, the commonly cited finding that fatigue resistance increases with age2126 is not well- established for the ankle plantar flexors; these muscles, particularly the soleus, are less susceptible to muscle fiberremodeling27 and may not exhibit the age-related fatigue resistance observed in other muscle groups (eg, knee extensors). We therefore tested the hypothesis that older adults, compared with young adults, would exhibit delays in torque response and rate of torque development, and that these effects would be amplified by localized muscle fatigue.

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Study Design and Participants

A quasi-experimental design was used to investigate age effects on FC in fatigued and nonfatigued conditions. Thirteen young (mean age, 26 (2.5); age range, 21–30 years) and 12 older (mean age, 71 (2.8); age range, 66–77 years) male adults participated in this study. Both groups of participants were healthy, independent, and nonsedentary. All participants were formally screened for major musculoskeletal, cardiovascular, and neurological disorders using a 23-item questionnaire administered verbally by a research coordinator during initial participant contact. Further evaluation was performed by a physical therapist during testing sessions to ensure that participants were able to comply with study requirements. All participants provided informed consent as approved by the institution's human subjects committee.

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Each participant was seated on a bench in a recumbent position with the knee in 90° of flexion, and the foot secured to a footplate attached to a dynamometer (Cybex 6000, CSMI, Norwood, Massachusetts). The participant's thigh and pelvis were immobilized using Velcro straps (Figure 1). Participants performed isometric and isokinetic maximum voluntary contraction (MVC), FC, and exercise tasks in the order shown in Figure 2.

Isometric MVC was defined as the maximum plantar flexion torque (Tisometric) produced during three 3-second isometric trials. Isokinetic MVC was defined as the maximum torque (Tisokinetic) during a 5-second isokinetic ankle plantar flexion task performed at 30° per second.

Force control tests were done with the ankle positioned in 10° of plantar flexion. The participant was instructed to respond to an auditory stimulus by producing ankle plantar flexion torque equal to 40% of the isometric MVC as quickly as possible and then holding the target level as steady as possible. The 40% target level was selected to be consistent with those used in previous studies6,8,9,28 and to ensure a level of

effort well less than the near-maximal rate often used by older adults during ADL.11 Continuous feedback was provided on a computer monitor located directly in front of the participant that displayed a graph with target and actual torque levels (Figure 3). Each FC test lasted 15 seconds. Force control trials were done before warm-up, after warm-up, and at 0, 1, 2, 3, 4, and 5 minutes after the fatigue exercise. Fatigue recovery was verified using the outcome variables, which all returned to baseline values within 5 minutes of postfatigue testing and were not considered further; only FC trials immediately before and after the fatigue task were included in further processing (Figure 2).

Warm-up exercise consisted of 4 sets of 2 isokinetic plantar flexion contractions at 30° per second. Participants were asked to use intensity levels of 25%, 50%, 75%, and 100% of perceived MVC for each of the 4 sets.7

Fatigue exercise consisted of maximal isokinetic contractions with the ankle plantar flexors at 30° per second. Fatigue was defined to occur when peak plantar flexor torque dropped to less than 50% of the isokinetic MVC for 3 consecutive contractions (Figure 4). No resistance was provided during return contractions (ankle dorsiflexion).

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Data Processing

Torque data were collected during all FC tests with the Cybex 6000 dynamometer. Data were sampled at 2000 Hz using a 16-bit A/D data acquisition board controlled by LabVIEW Express 7.0 (National Instruments, Austin, Texas).

All data were analyzed using MATLAB (The Mathworks, Inc, Natick, Massachusetts). Torque data were low-pass filtered using a cutoff frequency of 10 Hz. Each FC data set was divided into transient and steady state regions. The transient region (TR) was defined as the time period beginning with torque onset and ending with torque settling time (defined later). The steady state region was defined as the 5-second period following torque settling time, during which the participant maintained the target torque level. Since only torque development was of interest in the current study, only variables characterizing the TR were included in the analysis.

Variables calculated during the TR included onset time, settling time, and rate of torque development (Figure 3). Onset time (tonset) was defined as the time at which the torque increased to 3 standard deviations more than the baseline (prestimulus) level. Settling time (tsettle) was defined as the first point in a 1-second window of data in which the torque remained within ±5% of the target value (40% isometric strength capacity). Rate of torque development (S) was defined as the slope of a least squares line fit to the linear portion of the TR, defined as the duration between onset and the time at which the torque had reached its root- mean-square value (or 70.7% of the target level).

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Statistical Analysis

All statistical analyses were performed with SPSS 16.0 (SPSS, Inc, Chicago, Illinois). To explore age differences in baseline strength levels, an independent samples t test was performed on isometric and isokinetic MVC measures, with age as the between-subjects factor. A repeated-measures multivariate analysis of variance (MANOVA) was performed on the outcome variables using age and fatigue as between-subjects and within-subjects factors, respectively. Follow-up univariate tests were performed on individual variables demonstrating a significant multivariate main effect or interaction. To account for multiple testing during follow-up analyses, significance levels were adjusted using the Bonferroni method. Comparisons with P < .05 were considered statistically significant.

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Results are summarized in Table 1. The t tests performed on strength measures revealed a significant age-related decrease in isokinetic MVC torque (t23 = 2.938, P < .01, Cohen's d = 1.23), but not isometric MVC torque (t23 = 0.451, P = .656, Cohen's d = 0.19). During the exercise task, the average time to fatigue was 3.19 minutes and 3.09 minutes for young and older participants, respectively; time to fatigue was not significantly different between age groups (t23 = 0.134, P = .895, Cohen's d = 0.06). The MANOVA revealed significant effects for age [Wilks' A (3,11) = 0.391, P = .01] and age X fatigue interaction [Wilks' A (3,11) = 0.491, P = .04]. Follow-up univariate tests revealed significant age effects for onset time (age-related increase: F1,13 = 7.422, P = .02, Cohen's d = 1.44) and rate of torque development (age-related decrease: F113 = 4.899, P = .05, Cohen's d = 1.17); and a significant age X fatigue interaction for rate of torque development (F113 = 10.015, P < .01). Follow-up paired-samples t tests performed on rate of torque development within each age group revealed a significant fatigue-related decrease in rate of torque development among young adults (t = 3.957, P = .02, Cohen's d = 1.58), but no significant fatigue effects among older adults (t = 0.718, P = .56, Cohen's d = 0.23).

Although the MANOVA revealed marginal fatigue effects, follow-up univariate tests revealed a significant fatigue effect on rate of torque development (fatigue-related decrease: F1j13 = 4.790, P = .05, Cohen's d = 0.58).

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This study tested the hypothesis that older adults, compared with young adults, would exhibit delays in torque response and rate of torque development, and that these effects would be amplified by localized muscle fatigue. The age groups tested took similar amounts of time to become fatigued. Isometric strength was also similar between age groups; however, we observed an age-related decline in isokinetic strength. The latter finding is well established and consistent with the literature.29,30 While unexpected, the nonsignificant age group differences in isometric strength was similar to the negligible age effect on maximal isometric knee flexion torque reported by Runnels and colleagues,30 a result that may relate to greater motor unit (MU) synchronization and recruitment during isometric contractions.

Our first main finding is that healthy older adults have reduced ability to quickly generate a submaximal plantar flexion torque about the ankle joint, compared with youngeradults. Both a delayed onset time and a reduced rate of torque development were noted. These results are in agreement with previous studies demonstrating age-related declines in ankle torque development.31,32 This effect suggests an age-related decline in strength development and, since the ankle plantar flexors control anterior-posterior body sway during standing posture,33 may be linked to age-related declines in postural stability and falls. Ankle torque development is also important in stepping responses to restore balance from large perturbations such as a sudden pull at the torso, as well as small postural adjustments following translational perturbations at the base of support. Therefore, our observed age-related decline in ankle torque development may be a contributing factor in balance recovery deficits observed in older adults.34 For example, Mackey and Robinovitch17 demonstrated an age-related decline in the ability to recover balance by contracting the ankle muscles, which was attributed to impaired reaction time, and reduced peak ankle torque and rate of ankle torque development. This result, taken together with results from the current study, has implications for balance recovery ability since older adults may take longer to generate ankle joint torque during balance recovery. If this effect progresses to the degree that joint torque is not being produced quickly enough to effectively restore balance, a fall may occur.

One study limitation is whether or not our FC task is similar to FC used during a balance recovery maneuver in a fall situation. It may be inappropriate to directly compare results from this study (involving a voluntary response) to balance recovery studies (involving a more automatic response). Voluntary responses involve a level of decision making, whereas automatic responses (such as startle responses) are associated with shorter reaction times, suggesting the absence of cerebral cortex processing.35,36 This concept is illustrated by Hall and colleagues,37 who observed no age-related declines in rate of ankle torque development during balance recovery and point out that caution should be exercised when extrapolating findings from studies involving voluntary maneuvers to those with reactive ones. In addition, participants were asked to produce torque “as quickly as possible” in our study, while there is evidence that torque development is scaled relative to perturbation magnitude during balance recovery maneuvers.37,38 This scaling effect precludes direct extrapolation of our results to balance recovery maneuvers; however, assuming our testing protocol invokes maximal torque development, it may be implied that our observed age effects would translate into a decreased balance perturbation magnitude from which a successful balance recovery maneuver is possible. This has been confirmed in studies investigating feet-in-place17 and stepping39,40 responses used for balance recovery.

Our second main finding is the observed age X fatigue interaction on rate of torque development. This suggests that young adults' ability to quickly generate torque is reduced while older adults' performance is unaffected by localized muscle fatigue. This result does not support our hypothesis that a larger fatigue effect would be observed in older adults in comparison with young adults. However, this result is consistent with previous studies demonstrating an age-related decrease in muscle fatigability.2126 Although dependent on fatigue task and muscle type,41 our observed fatigability effect may be partially explained by age-related changes in muscle morphology.42,43 Muscle mass decreases during normal aging, with type II (fast-twitch) fibers showing a preferential atrophy.43,44 In addition, MU remodeling occurs with aging, in which type II fibers are reinnervated by axons already innervating slow MUs such that type II fibers approximate type I (slow-twitch) fibers, which are more fatigue resistant.44 Therefore, a fatiguing exercise could cause a larger proportion of fast-twitch fibers to drop out in young adults, which would result in a more pronounced reduction in rate of torque development during the FC task. Interestingly, the muscle group used in our FC task consists of muscles with different fiber compositions. The soleus, a tonic muscle associated with postural control, is primarily composed of slow-twitch fibers in young and older adults, while the gastrocnemius, a phasic muscle associated with locomotion, has a larger proportion of fast-twitch fibers in young adults.27,45,46 Therefore, MU remodeling, if present, was likely a result of age-related changes in the gastrocnemius muscles only. While our apparent age-related decrease in fatigability suggests the presence of MU remodeling, we did not directly quantify this phenomenon. Future studies should use muscle biopsies to confirm smaller proportions of fast-twitch muscle fibers in older adults. Biopsies may also provide insight into our observed age effects on torque development by confirming age-related changes known to influence muscle performance such as reduced cross-sectional area and increased intramuscular fat.30,47

An alternative explanation for this unexpected age X fatigue effect may be related to differences in fatigue task performance between young and older adults. For example, perceived exertion has been shown to increase with age during fatigue tasks,48 an effect that may have caused older adults' torque output to drop below the defined fatigue threshold before fatigue had actually occurred in our study. Although we did not measure perceived exertion, this effect may have resulted in the lack of fatigue-related torque development degradation among older adults.

The MANOVA used in our study failed to reveal a statistically significant overall fatigue effect on the outcome variables. This was likely caused by the relatively small sample size tested, as follow-up univariate tests did reveal a fatigue-related decrease in rate of torque development. This is in agreement with previous work4951 and may have implications for balance as researchers have observed shortlived, fatigue-related impairments in postural sway.5254

A further limitation of the current study arises from the inclusion criteria used when selecting participants. First, we tested only older men with no recent falling history. While age effects were observed, age or age-related fatigue effects may be amplified in older adults with a history of falling. The observed effects may be further amplified in older women, who have been shown to have reduced levels of strength and strength development in comparison to older men.32,55 The need to extend our work to fall-prone olderadults and to women is illustrated in the compensatory stepping literature, where researchers have demonstrated that fall-prone older adults, particularly older women, use less effective balance recovery maneuvers in comparison to healthy young and older adults.5659 Second, although all participants were functionally very healthy and active, we neither explicitly quantified participants' usual daily activity levels, nor did we exclude persons who may have had an advantage in the tests used (eg, elite athletes or persons who regularly exercised the plantar flexor muscles). Future studies should document participants' daily activity levels to explore their effect on age and fatigue findings.

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This study demonstrated that age and localized muscle fatigue have an impact on the ability to quickly produce a submaximal, isometric, ankle joint torque. Age significantly reduced the ability to produce torque quickly, and fatigue decreased the rate of torque development among young adults. The fatigue-related decline in rate of torque development among young adults was not observed in older adults, suggesting possible age-related changes such as MU remodeling or altered perceived exertion. Even so, older adults had an overall reduction in ankle torque production, which may have implications for balance recovery and fall risk among older adults.

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We thank Molly McVey, Laura Hughes Zahner, Jeffrey Schiffman, Shelley Bhattacharya, and Jacob Marszalek for their assistance with this study. We gratefully thank Joan McDowd, Alica MacKay, and the KUMC Grayhawk Laboratory for assistance with participant recruitment. We also thank for the support of Department of Defense DEPSCoR grant DAAD 19–02-1–0222.

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force control; aging; muscle fatigue; strength; human

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