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Lower Extremity Muscle Strength and Force Variability in Persons With Parkinson Disease

Skinner, Jared W., PhD; Christou, Evangelos A., PhD; Hass, Chris J., PhD

Journal of Neurologic Physical Therapy: January 2019 - Volume 43 - Issue 1 - p 56–62
doi: 10.1097/NPT.0000000000000244
Research Articles

Background and Purpose: Adequate lower limb strength and motor control are essential for mobility and quality of life. People with Parkinson disease (PD) experience a significant and progressive decline in motor capabilities as part of this neurodegenerative disease. The primary objective of this study was to examine the effect of PD on (1) muscular strength and (2) force steadiness in muscles that are primarily responsible for locomotion and stability.

Methods: Thirteen persons with PD and 13 healthy age-matched controls participated. Participants performed maximal and submaximal (5%, 10%, and 20% maximum voluntary contractions) isometric force tasks with the limb stabilized in a customized device. Strength of the hip extensors and flexors, hip abductors and adductors, and ankle plantar flexors and dorsiflexors was quantified based on data obtained from force transducers, with the relevant joint stabilized in standardized positions.

Results: Individuals with PD were weaker and exhibited higher amounts of force variability than controls across the lower extremity. Reduced strength was greatest in the hip flexors (2.0 N/kg vs 2.6 N/kg) and ankle plantar flexors (1.74 N/kg vs 2.64 N/kg) and dorsiflexors (1.9 N/kg vs 2.3 N/kg). Force steadiness was impaired in the hip flexors, ankle plantar flexors, and dorsiflexors.

Discussion and Conclusions: Reduced maximal force production was concomitant with impaired force control within the muscles that are critical for effective ambulation (hip flexion, ankle dorsiflexion, and ankle plantar flexion). These features should be evaluated when considering contributors to reduced mobility and quality of life.

Video Abstract available for more insights from the authors (see Video, Supplemental Digital Content 1, available at: http://links.lww.com/JNPT/A241).

Geriatric Research Education and Clinical Centers, Malcom Randall VA Medical Center, Gainesville, Florida (J.W.S.); and Department of Applied Physiology and Kinesiology, University of Florida, Gainesville (E.A.C., C.J.H.).

Correspondence: Jared W. Skinner, PhD, North Florida/South Georgia Veterans Health System, Geriatric Research, Education, and Clinical Centers (GRECC) (182), 1601 SW Archer Rd, Gainesville, FL (jared.skinner@va.gov).

The authors declare no conflict of interest.

Supplemental digital content is available for this article. Direct URL citation appears in the printed text and is provided in the HTML and PDF versions of this article on the journal's Web site (www.jnpt.org).

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INTRODUCTION

Parkinson disease (PD) is a common neurodegenerative disorder that can cause a variety of motor symptoms, including resting tremor, rigidity, akinesia/bradykinesia, and postural instability and gait disturbance.1 Although these symptoms have wide-ranging effects on motor performance and completion of activities of daily living (ADL), the underlying impairment within the neuromuscular system is not fully understood. Individuals with PD often exhibit lower levels of maximal force production (muscle weakness) compared with healthy controls.2–7 Our previous investigation observed reduced torque generation at the ankle and general weakness at the hip and knee in PD compared with controls.2 These strength deficits have been shown to lead to compensatory strategies that altered the ability to perform ADL.2 Thus, reduced muscular strength has the potential to negatively influence performance of ADL.

Maximum force production in the muscles of the hip, knee, and ankle joints has been individually related to performance of ADL, including rising from a chair, navigating stairs, and forward propulsion.2 , 8 , 9 Although maximal strength appears to be important for functional mobility, most daily movements occur at submaximal force levels, ranging from 2% to 15% of maximum strength depending on the difficulty and intensity (ie, level of required muscle force) of the activity.10–13 Thus, control of submaximal force, defined as the variability in muscle force output, across the muscles of the lower extremity is also important for functional mobility. Lower extremity force control has been considered a marker of impairment during functional tasks such as walking endurance, chair rising, and stair climbing in older adults.14 Reduced force control of the ankle plantar flexors during low-intensity contractions is also highly associated with increased postural sway in elderly adults.12 Moreover, correlations between force control and falling in older adults have been reported.13 Although these studies were not performed in persons with PD, they provide a basis for investigating the force control abilities of the lower extremity in this mobility-impaired population. To date, the capacity of people with PD to exert maximal force and precisely control submaximal force within the prominent lower extremity muscles, specifically those critical for propulsion during walking, has not been fully evaluated in the extant literature. The primary aim of this study was to assess both maximal force production and force control across the primary muscles of the lower extremity responsible for propulsion and stability during walking. We hypothesized that persons with PD would exhibit reduced strength and display higher amounts of force variability across the lower extremity muscle groups compared with healthy older adults (HOAs).

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METHODS

Participants

Thirteen persons with PD (6 males) and 13 (7 males) healthy age controls (±2 years) were recruited for the investigation. The sample size was based on a priori power analyses utilizing force measures from pilot data and prior investigations investigating force control in both PD and older adult populations.15 , 16 Alpha was set at 0.5 and beta was set at 0.2, and the effect size of interest was set at 0.3 for sample size determination. Participants who enrolled in the study had not experienced any lower extremity orthopedic injury for at least 1 year prior to participation. All persons with PD were being treated with stable doses of antiparkinsonian medication (no change in frequency or dosage within the previous 2 months). Participants provided written informed consent before participating in the study as approved by the University of Florida Institutional Review Board. Participants with PD were evaluated and diagnosis of idiopathic PD was confirmed by a movement disorders neurologist using UK Brain bank diagnostic criteria17 and were recruited from the University's movement disorders center. Participants with PD did not exhibit fluctuations within the medication cycle and were tested in their optimally medicated state (“ON” meds). Participants were tested while “ON” because (1) this most accurately represents normal behavior throughout the waking day in most persons with PD, and (2) motor deficits can be observed in PD even after the administration of antiparkinsonian medication.18

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Experimental Protocol

Participants abstained from physical activity within the 24 hours prior to testing. At the beginning of the visit, participants with PD were evaluated using the Unified Parkinson Disease Rating Scale (UPDRS) while being recorded. These videos were scored by a single independent movement disorders-trained neurologist who was blinded to the purpose of the study.

Maximal force production and submaximal force control of the major muscle groups of the lower extremity were assessed via strain gauge (S-Beam Tension and Compression Load Cell, FUTEK Advanced Sensor Technology Inc, Irvine, California), with the relevant joint stabilized in a standardized position. We specifically examined performance within the hip extensors (HEs), hip flexors (HFs), hip abductors (HABs), hip adductors (HADs), and ankle plantar flexors (PFs) and dorsiflexors (DFs) utilizing a custom-built apparatus embedded with force sensors as described later. These muscles were evaluated because they are essential contributors to locomotor ability.19–23 During normal walking, the primary task of the muscles that control the hip and ankle joints are to provide support against gravity and contribute to propulsion.19 , 23 , 24 To begin, each participant was first familiarized with the assessment procedures. This familiarization period included a verbal explanation of the task and 3 practice trials at submaximal isometric efforts for each of the muscle groups to be tested. After the familiarization period, each participant performed maximum voluntary contractions (MVCs) at the hip (HE, HF, HAD, and HAB) and ankle (DF and PF) for both the right and left legs. The order of testing was randomized prior to beginning the experimental protocol.

Following the MVC testing, participants performed the force control task at 3 submaximal force levels (5%, 10%, and 20% MVC) for both the right and left legs. Again, prior to beginning the tasks participants were familiarized with the study procedures. For this task, the participants attempted to match a constant force level for 20 seconds. This approach has been previously utilized to evaluate force control ability in several previous investigations.14 , 25 , 26 The levels of intensity were selected based on prior evidence in older adults that suggested changes in force variability with age are more pronounced at low levels of MVC25 , 27 and to encompass the low end of a “normal” range of MVC that older individuals typically utilize during ADL.8 , 28 During the experiments, ratings of fatigue were assessed using the Borg Category Ratio or Borg CR-10, a numerically based, self-perceived exertion rating scale (0-10, 0 indicating rest and 10 is maximal exertion) at the beginning and end of the testing session.29 The testing order for the force levels and which leg was tested first was randomized prior to beginning the experimental protocol.

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Apparatus

Ankle Muscle Testing

Participants were seated with the hip and knee joints positioned at 90° flexion and hip abducted approximately 10°.30 To stabilize the ankle for testing, the foot was secured in a customized device with an adjustable foot plate positioned parallel with the floor. The foot was secured by straps at the level of the metatarsals. The strap and foot positioning isolate the movement of the ankle to the sagittal plane (dorsiflexion and plantar flexion)30 (see Figure 1A).

Figure 1

Figure 1

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Hip Muscle Testing

Participants stood upright in a custom frame that isolated the movement of the hip to uniplanar actions: hip flexion, hip extension, hip abduction, and adduction. The strap was positioned superior to the knee joint. Participants exerted force in the horizontal direction against a strap that was attached in series to a fixed 1-dimensional force transducer (see Figure 1B). The muscle force signals acquired with the 1-dimensional force transducer were sampled at 1 kHz with a Power 1401 A/D board (Cambridge Electronic Design, UK) and a NI-DAQ card (Model USB6251, National Instruments, Austin, Texas) and data were stored on a computer.

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Maximum Voluntary Contraction

Initiation of the MVC trial began with an on-screen start command that was displayed on the monitor, and the MVC trial terminated with an on-screen stop command. Participants were instructed to increase force from baseline to maximum as quickly as possible and maintain their maximum force for approximately 3 seconds.16 , 31 Participants performed maximal trials until the maximum force of 2 trials was within 5% of each other.32 All participants could produce 2 MVC trials with 5% of each other within 3 attempts. Two trials were chosen based on pilot data that indicated no statistical difference when averaging 2 independent trials compared with the average of 3 independent trials. In addition, performing consecutive maximal effort trials increases an individual's level of fatigue. A minimum of 1 minute of rest was given between trials. An additional MVC test was performed approximately 5 minutes after completing both experimental protocols to determine whether fatigue may have influenced the results.

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Submaximal Force Control

During the submaximal force control task, the target position was provided as a red line in the middle of a 32-inch monitor (SyncMaster 320MP-2, resolution: 1360 × 768 pixels, Samsung Electronics America, New Jersey), and the force produced was shown as a blue line progressing with time from left to right.30 Participants were seated during ankle muscle testing and standing during hip muscle testing, and faced a monitor located 1.25 m away at eye level.30 , 33 The position of the apparatus and the strain gauge (S-Beam Tension and Compression Load Cell, FUTEK Advanced Sensor Technology Inc, Irvine, California) was rotated 90° during hip abduction and adduction testing. Participants affirmed that they could see the screen and its display clearly, without any obstruction or limitations. The visual gain for the task was 0.05°. We selected this visual feedback to eliminate the effects of visuomotor corrections on force control.33 The protocol for the force control task was similar to previous investigations.30 , 34 The participants were instructed to gradually push/pull against the force transducer and increase their force to match the target force. When the target was reached, participants were instructed to maintain their force on the target as accurately and as consistently as possible. For each task, participants performed 3 trials and each trial lasted 20 seconds. Participants had a minimum of 30-second rest between trials and 3 minutes of rest between the tasks. A custom-written program (MATLAB, MathWorks, Inc) controlled the targeted force level and gain of visual feedback.

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Data Processing

The maximal value of each MVC trial was quantified as the average of the 10 force values surrounding the peak force produced during a single continuous isometric contraction.32 We quantified the MVC from the average of the 2 MVC trials. This value was used for analysis and formulation of relative intensities for the submaximal force trials. This procedure produced a more conservative MVC that reflects the capacity to maintain a maximal contraction, which better reflects ADL.33

For the submaximal force trials, the first 5 seconds and final 1 second of force data were eliminated from all analyses to account for early and late force adjustments, resulting in a 14-second submaximal force signal. The 14-second submaximal force signal was filtered using a fourth-order Butterworth filter at a cutoff frequency of 20 Hz.35 For this investigation, force steadiness was defined as the coefficient of variation (CV). CV of force was computed as the standard deviation (SD) of force/mean force output × 100. Force steadiness was quantified using a detrended force signal. Detrending was performed using the detrend function in Matlab, which removes the best straight-line fit linear trend from the data.36 In addition, detrending the force signal removed any drifting of force, which could influence the quantification of force variability.

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Statistical Analysis

All statistical analyses were performed by using commercial software 0 (JMP Pro version 11, SAS Institute Inc, Cary, North Carolina) and the level of significance for all analyses was set at P < 0.05. Descriptive statistics are reported as mean ± SD. The normality for continuous variables in groups was confirmed by the Shapiro-Wilk test. We used the t test or the Mann-Whitney U test for comparisons for MVC. We first compared performance values between legs (most affected and least affected side and dominant and nondominant). The most affected side was determined through participant self-report and then verified from clinician scoring of the UPDRS. Since no significant differences (P > 0.05) were detected between legs, we collapsed MVC values across legs for statistical analysis. Two-way analyses of variance with repeated measures on force levels (5%, 10%, and 20% of MVC) were used to test for between- and within-group differences in force steadiness at each muscle group.

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RESULTS

All participants successfully completed the testing protocols. MVC at the start of testing was not statistically different from MVC at the end of testing, suggesting fatigue did not influence the findings (1.8% ± 1.1%, P > 0.05). Group means for age, height, and mass did not differ between controls and persons with PD (see the Table).

Table

Table

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Maximal Voluntary Contraction

Examination of MVC trials indicated that persons with PD generated lower isometric force across all muscle groups compared with HOAs. Although there was a distinct pattern for those with PD being weaker than HOAs, statistically significant differences were only detected for the hip flexors (P = 0.01), ankle dorsiflexors (P = 0.03), and ankle plantar flexors (P = 0.001) (see Figure 2). On average, those with PD generated 20% less hip abductor force, 14% less hip adductor force, 10% less hip extensor force, 22% less hip flexor, 35% less plantar flexor force, and 18% less dorsiflexor force.

Figure 2

Figure 2

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Submaximal Force Control

For the hip flexors, there was a significant group (PD vs HOA) × force (force level) interaction [F (2, 48) = 4.612, P < 0.01], indicating that the PD group produced higher variability across all levels of intensity compared with the control group and higher CV at 5% MVC compared with 10% and 20% MVC (see Figure 3). There was a significant group × force interaction for the ankle plantar flexors [F (2, 48) = 4.3217, P < 0.01] and the ankle dorsiflexors [F (2, 48) = 5.9858, P < 0.005]. Similarly, the PD group displayed higher variability at the ankle plantar flexor and dorsiflexors across all levels of intensity compared with the control group and higher CV at 5% MVC compared with 10% and 20% MVC. In addition, participants in the PD group exhibited greater variability at the 10% MVC compared with 20% during plantar flexion. The statistical analyses failed to detect a group × time interaction for the CV of force in the hip abductors and adductors or the hip extensors. However, the statistical analyses detected a main effect of intensity for the CV of force in the hip abductors [F (2, 48) = 35.448, P < 0.001; hip adductors, F (2, 48) = 37.1, P < 0.001; and hip extensors, F (2, 48) = 22.6, P < 0.001]. Across both groups, CV at 5% MVC was higher compared with 10% and 20% MVC. Although not statistically significant, there was a trend that suggested that, across groups, the CV at 10% MVC was higher than the CV at 20% MVC.

Figure 3

Figure 3

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DISCUSSION

This is the first investigation to concurrently evaluate, in persons with PD, both maximal strength and force control in the lower extremity muscles used in locomotion. The results demonstrated that participants with PD produced significantly less force and displayed higher amounts of force variability compared with HOAs. Unexpectedly, these deficits in maximal force and submaximal force control were confined to a few select muscle groups (ie, hip flexors and ankle plantar flexor and dorsiflexors). The potential mechanisms for the reduced force output and force steadiness may be related to impaired cortical activation originating from abnormal drive from the basal ganglia to the thalamus,5 , 37 which can lead to inability to sufficiently activate motoneuron pools, thereby affecting recruitment and discharge rate and thereby impede the facilitation of desired movement.38 , 39 In addition to these central origins, sarcopenia and inactivity likely co-contribute to the observed force deficits and increased difficulty performing ADL.40 , 41

Our results indicated that persons with PD produced significantly less force compared with controls, which is supported by previous literature.3 , 42–44 Likewise, the lack of statistically detectable muscle weakness across all of the joint actions observed in the current study is also supported by the literature.2 For example, individuals with PD produce smaller peak ankle plantar flexion moments, but research has failed to detect differences in moments of hip or the knee joints.2 Together, these results suggest that the muscles of the ankle joint appear to be consistently weaker in persons with PD. However, the impact of this weakness on gait deficits is unclear. While ankle plantar flexion strength has been shown to be associated with both gait velocity and stride length in persons with PD, changes in strength have not been found to be associated with changes in gait.45 Prior investigations observed that muscular deficit in PD is an independent risk factor for falls,46–48 that strength of the knee extensor and plantar flexor muscles is significantly associated with stability and recovery performance from forward falls,49 that the muscle groups around the ankle are pivotal in performance of ADL,2 and that muscle strengthening improves performance of ADL.50 While other factors such as fall history, postural control, and cognitive abilities51–53 significantly contribute to increased fall risk in PD, these findings support that persons with PD who are at risk for falling may benefit from training to increase ankle strength.

The investigation of submaximal force control found increased force variability in those with PD compared with HOAs. Consistent with the observations in muscle strength, reduced force control was evident in the hip flexors and ankle plantar flexors and dorsiflexors. Milner-Brown et al54 theorized that when individuals with PD voluntarily attempt to maintain a force, motor units inappropriately stop firing for prolonged periods or fire at abnormally low frequencies (2-3 Hz). Diminished force control interferes with and disrupts the ability to perform smooth and accurate movements and interferes with the ability to perform many ADL.25 , 27 Kouzaki and Shinohara12 reported that the increased force variability at the ankle in older adults during low-intensity lower extremity isometric contractions could accurately predict variability of center of pressure during quiet standing. Therefore, interventions that are centered around reducing force variability may have relevant clinical implications as persons with PD often exhibit impairments in gait and balance function.1

Specific to the pathology of PD, striatal dysfunction may interfere with efficient and coordinated movement. Impaired force steadiness has been linked to abnormal activation of the involved muscles, which is likely due to the structural and neural changes that occur with PD.40 , 55 , 56 Impairments in the variability, intensity, and frequency of corticospinal activation lead to irregular and intermittent discharge patterns of motor units and the recruitment of a greater number of motor units at low force thresholds in persons with PD than in controls. Yoon et al26 recently identified the putamen as one of the brain areas associated with the CV of force. The authors interpreted this as evidence that the basal ganglia play a dominant role in the control of steady contractions across a range of forces. The results from Yoon et al26 may suggest that the observed deficits in force control in the PD group from the current study are associated with the known impairments within the impaired cortico-basal ganglia-thalamic loop.26 Much of our understanding of the deficits in force steadiness or control relies on the information obtained from investigations in the upper extremity of older adults.25 , 33 , 57 However, motor control abilities are known to be different between the upper and lower extremities.58 , 59 There is clinical relevance for understanding submaximal force control across the lower extremity joints, as a more robust knowledge of the motor limitations in PD can potentially lead to a greater number of effective treatment options.

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Limitations

The present study is not without limitations. Our results for maximal force and submaximal force control are limited to the muscles related to actions of the hip and ankle joints. The muscles of the knee were not evaluated. The rationale for not including the knee is due to prior investigations that have suggested that the knee produces only small net mechanical work during walking, playing a primary role in absorbing energy during the stance phase and providing stable locomotion rather than being an important source of either control or propulsion.20 , 22–24 However, in future studies, evaluation of the muscles controlling the knee joint could provide additional understanding of the magnitude of deficits in force production and force control in PD. It seems likely that a comprehensive evaluation of lower extremity performance is needed to fully appreciate the role that force production, and control deficits, may have on performance of mobility-related ADL. In the current study, participants were screened using the UPDRS; the use of the MDS (Movement Disorder Society)-UPDRS, a more sensitive alternative of the UPDRS, could provide more accurate reflection of disease severity. Participants were evaluated during their self-reported optimally medicated state. There is conflicting evidence regarding the impact of antiparkinsonian medications on force steadiness and maximal force.9 , 18 , 39 Future investigations should expand on the current findings and objectively measure the effects of parkinsonian medications on submaximal and maximal force generation in the lower extremity. The relative force levels that were used for the experimental design were chosen based on prior evidence in older adults.11–13 We attempted to evaluate force steadiness at levels of MVC that older individuals typically utilize during normal ADL; however, a wider spectrum of relative intensities could provide more information on how individuals with PD perform near maximal capabilities.

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CONCLUSIONS

The objective of this investigation was to identify reduced muscular capabilities (ie, strength and force steadiness in muscles that are primarily responsible for locomotor function in individuals with PD). These results provide evidence that reduced maximal force production was concomitant with higher force variability within joint actions critical for effective ambulation (hip flexion, ankle dorsiflexion, and plantar flexion). Together, the present data and other prior investigations suggest force production and control capabilities may contribute to impaired mobility, and perhaps fall risk, in persons with PD. We hope future investigations will expand on the results to examine the underlying relationship between deficits in strength and force control, as it has clinical importance for improving mobility and quality of life in individuals with PD.

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Keywords:

activities of daily living; ankle; force variability; Parkinson disease; rehabilitation; strength

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