Secondary Logo

Journal Logo

Execution of Activities of Daily Living in Persons with Parkinson Disease

SKINNER, JARED W.1; LEE, HYO KEUN1; ROEMMICH, RYAN T.2,3; AMANO, SHINICHI4; HASS, CHRIS J.1,5

Medicine & Science in Sports & Exercise: September 2015 - Volume 47 - Issue 9 - p 1906–1912
doi: 10.1249/MSS.0000000000000598
APPLIED SCIENCES
Free

Introduction Muscular weakness and the motor difficulties associated with Parkinson disease (PD) often impair the performance of activities of daily living (ADL). However, little is known about the magnitude and distribution of relative muscular effort of persons with PD during ADL. The purpose of this investigation was to determine the relative magnitude of lower extremity moment production that persons with PD use to perform common ADL.

Methods Fifteen participants with mild-to-moderate PD and 14 age/sex-matched controls volunteered. Participants performed a series of ADL tasks, as follows: gait initiation (GI), gait, and stair ascending tasks. Participants were then asked to perform maximal-effort isokinetic tests of hip and knee extension and ankle plantarflexion at speeds of 90° per second and 120° per second. Relative effort was quantified as a percentage of the maximal isokinetic value produced by a joint during performance of the ADL. Relative effort and peak isokinetic joint moments were analyzed using a mixed-model ANOVA with repeated measures. All other comparisons were evaluated using independent t-tests.

Results Persons with PD produced smaller ankle plantarflexion moment at both 90° per second and 120° per second (P < 0.05). Relative effort during GI (271% vs 189%, P < 0.05) and gait (270% vs 161%, P < 0.05) was significantly greater at the ankle in persons with PD. Contribution of the ankle to the support moment was lower in PD during stair ascending (24% vs 34%) and GI (63% vs 57%) compared with that in controls.

Conclusions The reduced ankle moments during ADL are indicative of deficits in muscular capabilities in those with PD. Moreover, PD caused a redistribution of joint torques, such that PD participants used their hip extensors more and ankle plantarflexors less.

1Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, FL; 2Motion Analysis Laboratory, Kennedy Krieger Institute, Baltimore, MD; 3Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD; 4Ohio Musculoskeletal and Neurological Institute, Ohio University, Athens OH; and 5Center for Movement Disorders and Neurorestoration, Gainesville, FL

Address for correspondence: Chris Hass, Ph.D., Department of Applied Physiology and Kinesiology, University of Florida, 100 Florida Gym, PO Box 118205, Gainesville, FL 32611–8205; E-mail: cjhass@hhp.ufl.edu.

Submitted for publication September 2014.

Accepted for publication December 2014.

Healthy young adults efficiently coordinate activity across many muscles to execute activities of daily living (ADL) safely while minimizing fatigue (15). However, the ability to efficiently execute ADL such as standing, dressing, walking and stair ascending has been shown to decrease with advancing age (15,36). Because these activities are fundamental for maintaining independence and quality of life, the deterioration in the ability of older adults to perform ADL is concerning.

Previous research has shown that healthy older adults (HOA) perform ADL at a higher percentage of their maximal lower extremity moment production capabilities compared with healthy young adults (2,15). The increase in relative effort often requires the development of an altered or compensatory movement strategy to perform ADL (5,14,19,34,36), which has been associated with increased fatigue and risk of falling (15,35). For example, both DeVita et al. (7) and Karamanidis et al. (19) observed a redistribution of joint moments in the sagittal and frontal planes across the knee and hip for older adults while ascending and descending steps and during steady-state walking (6,19,20). DeVita and Hortobágyi (6) reported that the relative contribution of the hip to the total support moment during the stance phase in older adults was significantly higher compared with that in younger adults during gait. In addition, Karamanidis et al. (19) reported that older adults showed higher knee adduction and knee internal rotation joint moments during the stance phase during stair ascension (SA). In these studies, the altered moment control strategy was often related to the reduced capabilities of specific muscle groups to generate force (6,7,19,20). Collectively, these studies suggest that older adults are able to compensate for muscle weakness during performance of a variety of ADL (10,19,25,33,36) by modifying their motor execution strategy.

Preservation of muscle functionality is important for maintaining quality of life and preventing disability during healthy aging; it becomes particularly important in persons with neurodegenerative movement disorders such as Parkinson disease (PD) (5,10,25). The combination of aging, disease-specific degeneration, and disuse in PD often results in postural instability (24), abnormal muscle activation (8), increased variability in force production (4,5), deficits in moment generation (16), and increased muscular fatigue (37). In addition, persons with PD exhibit decreased neuromuscular complexity during movements such as gait, suggesting altered neural control (31). Previous research has observed associations between several of these motor deficits and decreased ability to perform ADL and exercise efficiently (5,35). Stanley et al. (35) reported that during submaximal cardiovascular exercise, persons with PD performed at a higher percentage of their peak oxygen consumption with respect to healthy persons, thus indicating reduced metabolic efficiency. Knowledge of the cardiovascular relative effort in individuals with PD is important for safe exercise prescription, but the quantification of relative effort in terms of muscle strength or joint moments during performance of ADL could also provide better understanding of the causes of mobility limitations and fatigue in PD. Although many aspects of motor performance in PD have been evaluated (e.g., the spatiotemporal and center of pressure parameters of gait and gait initiation (GI) (11,12,25), the relative magnitude of the muscular effort required to perform ADL has yet to be examined. This information will be important for enhancing the design of interventions or rehabilitation sessions so that they effectively target specific limitations. Changes in health care coverage, lack of independence, progressing disability, and the presence of nonmotor symptoms such as apathy and depression are all barriers to rehabilitation in this population. Thus, it is critically important that individual therapy sessions can target specific underlying features of ADL impairment.

The aims of this investigation were 1) to determine the relative effort required to perform common ADL in persons with PD compared with that in HOA and 2) to examine the distribution of lower extremity moments at the hip, knee, and ankle that contribute to the support moment with which persons with PD perform ADL. We hypothesize that persons with PD will use a higher percentage of their relative effort because of decreased maximal joint moment generation and thus require a redistribution of the mechanical load at the hip, knee, and ankle joints to perform ADL. Ultimately, knowledge of the specific joint capabilities could lead to facilitation of evidence-based interventions and clinical care for those with PD.

Back to Top | Article Outline

METHODS

Participants

Fifteen participants with mild-to-moderate PD were involved in this study (age (mean ± SD), 65 ± 8 yr; height, 170.56 ± 7.97 cm; body mass, 77.37 ± 10.4 kg; eight male and seven female participants, Unified Parkinson Disease Rating Scale motor score in the on-medication state, 27 ± 7; Hoehn and Yahr score, 2.6 ± 0.3) and 14 age-matched HOA (age, 65 ± 7 yr; height, 170.4 ± 10.4 cm; body mass, 71.5 ± 14.75 kg; seven male and seven female participants) participated in this study. None of the participants had engaged in resistance training for at least 3 months previously nor had they experienced any lower extremity orthopedic injury for at least 1 yr. Participants with PD were evaluated during their self-reported period of maximal therapeutic benefit (approximately 1–1.5 h after their last dose of anti-Parkinsonian medication). The study was approved by the University of Florida institutional review board, and a written consent was obtained from all participants before participation.

Back to Top | Article Outline

Experimental design

Participants performed GI, gait, and SA tasks (10,32,34) in a randomized order. Participants were given adequate rest between trials and tasks to minimize fatigue. Thirty-five passive reflective markers were attached to the whole body in accordance with the Vicon Plug-in-Gait total body marker set. Kinematic data were collected using a 10-camera Optical Capture System (120 Hz Vicon Nexus; Vicon, Oxford, United Kingdom). For the GI trials, participants began by standing quietly at the center of the 8-m walkway on one of the walkway’s three force plates (360 Hz; Bertec Corporation, Columbus, OH) that was mounted flush to the laboratory floor. Kinematic and kinetic data were time synchronized and filtered using fourth-order low-pass Butterworth filters with cutoff frequencies of 10 Hz. Initial foot positioning for the GI trials was selected by the participant and constrained for the remaining trials. A verbal cue of “ready” was given to the participants, and after a brief pause, they then initiated walking at their own discretion and continued to walk the entire distance of the walkway. During the gait trials, the participants walked across the entire length of the walkway at a comfortable self-selected pace. During the SA task, participants ascended a single stair (15 cm high × 36 cm wide) that was secured atop one of the force plates. Participants were instructed to initiate the movement by stepping onto the stair first with their dominant/more affected leg (depending on group) and remain standing in a static position once both feet were atop the stair. Initial foot contact and toe off were identified for each trial from the force plate data. The more affected leg was self-reported by participants with PD and later confirmed with Unified Parkinson Disease Rating Scale motor scores. Leg dominance was determined on the basis of asking “Which leg would the participant use to kick a soccer ball?” (1).

After successful completion of the ADL tasks and adequate rest, participants completed a series of unilateral maximum-effort isokinetic tests for hip extension, knee extension, and ankle plantarflexion at velocities of 90° per second and 120° per second using a Kin-com dynamometer (Chattecx Corporation, Chattanooga, TN) and standardized testing procedures (9,18). The angular velocities were chosen on the basis of previous investigations, and because of close proximity, they share to velocities observed during those achieved during performance of ADL (9,17,24). The order of isokinetic testing was randomized, and the procedure and desired movement pattern were explained to the participants before testing each joint. The rotational axis of the dynamometer was aligned with the transversal joint axis. Participants performed a warm-up at self-perceived 50% of their maximal capabilities to become acclimated to the task. At each velocity, participants performed one set of five maximal effort repetitions for each joint movement. A repetition was defined as moving through the joint’s full range of motion without obstruction. A rest period of 3–5 min was allotted between each exercise to minimize muscular fatigue. The repetition with the highest peak moment for each joint was recorded and normalized to the individual’s body mass and was documented as the peak isokinetic joint moment (N·m·kg−1) at each angular velocity. Maximal isokinetic testing was more fatiguing than the ADL testing and was thus performed first. This was done to eliminate the influence of muscular fatigue during the ADL task.

Sagittal joint moments for hip and knee extension and ankle plantarflexion during the ADL tasks were calculated using a link-segment model and an inverse dynamics approach. The distribution of lower extremity joint moments was also examined as a percentage of the total support moment. The total lower extremity moment (TLEM) was calculated for each of the ADL tasks by summing the peak hip extension, knee extension, and ankle plantarflexion moments from the stance limb during the stepping phase of GI (23), from the dominant limb during the stance phase of gait, and from the lead/stepping leg during the SA task over a period spanning the initial contact of the stepping limb onto the stair until the instant before initial contact of trailing limb. TLEM provides a quantitative assessment of the support and propulsive effort of the musculature for each leg during each specific ADL task (15). By comparing the maximal joint moment of each individual joint to the TLEM, we can assess the relative contribution of each joint to the ADL task. Percentage of hip, knee, and ankle contribution was found by dividing the individual peak joint moment by the peak TLEM. The kinetic data were subsequently normalized for subject’s mass. Relative effort was expressed as the percentage of their maximal joint moment at the hip, knee, and ankle produced during ADL in relation to their maximal joint moment produced during the isokinetic testing.

Back to Top | Article Outline

Statistical analysis

Descriptive statistics for age and body mass were calculated for both groups. The PD group’s more affected limb and HOA’s dominant limb were used for analysis. Maximum isokinetic moment production was compared in joint specific comparisons using a group × speed repeated-measures ANOVA. The peak moments observed during the ADL tasks and the contribution of individual joints to the support moment were compared between groups using independent t-tests. Furthermore, relative effort of each joint was evaluated using a group × speed repeated-measures ANOVA. An a priori significance level of P ≤ 0.05 was adopted for the investigation.

Back to Top | Article Outline

RESULTS

Comparison of isokinetic joint moments

Statistical analysis revealed maximal ankle plantarflexion moment to be significantly lower in the PD group compared with that in the HOA group for the more affected leg at both 90°·s−1 and 120°·s−1. Furthermore, the less affected leg was statistically weaker at 120°·s−1 (P < 0.05) (Table 1). No other significant differences in peak joint moments were noted between the two groups in the isokinetic task.

TABLE 1

TABLE 1

Back to Top | Article Outline

Peak sagittal joint moments during ADL

Figure 1 illustrates representative joint moment profiles from one HOA and one PD subject during GI (top row), gait (middle row), and SA (bottom row). Results of the ADL task indicated that the PD group produced significantly greater hip extension moments during GI (P < 0.05). The TLEM produced during GI was not statistically significant between groups (P > 0.05). The analyses did not indicate significant differences in peak sagittal joint moments between groups during gait. In addition, there was no statistical difference in TLEM between groups during gait (P > 0.05). During SA, however, those with PD produced significantly greater hip extension moments than HOA (P < 0.05) (Table 2). Furthermore, although the finding was not statistically significant, the PD group showed diminished ankle plantarflexor moments during SA when compared with HOA (P = 0.07). There was no statistical difference in TLEM between groups during SA (P > 0.05).

TABLE 2

TABLE 2

FIGURE 1

FIGURE 1

Back to Top | Article Outline

Comparison of relative effort

The PD group required a higher percentage of their maximal ankle plantarflexor capabilities (90° per second) to provide locomotor propulsion during GI (271% vs 189%, P = 0.04) (Fig. 2A) and gait (270% vs 161%, P = 0.02) (Fig. 2B) compared with healthy controls. There was a statistical trend supporting similar GI findings when considering the ankle plantarflexor moments produced at 120° per second (277% vs 186%, P = 0.05) and during gait (290% vs 190%, P = 0.06). There was no significant difference in the relative effort between PD and HOA (P > 0.05) at any joints during the SA task.

FIGURE 2

FIGURE 2

Back to Top | Article Outline

Contribution of individual joint moments during AD to support moment

During the GI task, the statistical analysis revealed that the PD group displayed diminished ankle plantarflexor contribution (58% vs 62% HOA, P = 0.03) (Fig. 3A) when compared with HOA. Analysis of the gait task revealed no differences in the percent contribution of any of the lower body joint moments in PD and HOA (Fig. 3B). The contribution from the ankle was significantly lower in PD (24% vs 34% HOA, P = 0.02) during SA (Fig. 3C). Persons with PD also performed SA with significantly greater contribution from the hip as a percentage of TLEM (41% vs 27% HOA, P = 0.01). There were no significant differences in the contribution of the knee to the TLEM between PD and HOA (P > 0.05) during any of the ADL tasks.

FIGURE 3

FIGURE 3

Back to Top | Article Outline

DISCUSSION

This study investigated the relative magnitude of lower extremity moment production and joint moment distribution with which persons with PD perform ADL compared with HOA. In support of our hypothesis, and previous literature, our work suggested that PD has diminished isokinetic peak ankle plantarflexor moments (9). Individuals with PD used a higher magnitude of their relative effort at the ankle during GI and gait. Furthermore, our findings suggest that individuals with PD alter their task execution strategy when performing SA and GI by redistributing the contribution between the joints, specifically increased hip and decreased ankle contribution to the support moment.

Although numerous studies have evaluated muscular capabilities (5,25), peak joint moments (9,24,29) and peak torque across isokinetic velocities (18,24,26,29) produced by individuals with PD across several joints, there is still a lack of continuity in the extant literature as to which muscle groups are consistently impaired (5,26,27,37). Our findings suggested that the reduced joint moment production was localized to the ankle, rather than globally apparent across the entire lower extremity chain. Moreover, other studies have documented additional reductions in the hip, knee, and trunk moment production (5,24,26,29). Our study found that the two investigated angular velocities have no effect on the joint moment. Several studies provide evidence that individual joint moment production may be reliant on velocity (24,26,28). Although this position is widely accepted in the literature, our results show that muscle weakness was not associated with the tested velocities. Other studies have also demonstrated evidence that is similar to our findings (9,21,22). Durmus et al. (9) reported that isokinetic movement velocity had no statistical effect on the joint moments. The conflicting evidence may partly be due to the relatively close proximity of the two tested velocities. In addition, the results could reflect potential differences because of the wide range of muscular strength that can be measured across testing modalities, individual joint geometry, and degree of habitual physical activity.

To our knowledge, this is the first investigation to determine the relative effort of each joint (hip, knee, and ankle) during performance of three common ADL in persons with PD. The results of our study indicated that these differences in relative effort were localized to the distal joint during GI and gait. Previous research has indicated that older adults perform closer to their maximal muscular capabilities when performing ADL as compared with younger adults. Hortobágyi et al. (15) demonstrated that older adults perform at 24% higher magnitude of relative effort at the knee joint (78% vs 54%) when ascending a stair, 46% higher relative effort during stair descent (88% vs 42%), and 38% greater relative effort during chair rise performance (80% vs 42%) compared with younger adults. Herein, the amount of relative effort at the ankle in those with PD was 1.43-fold greater during GI (Fig. 2A) and 1.7-fold greater in PD during gait (Fig. 2B) compared with HOA. These findings may help explain the increased cardiovascular demands persons with PD exhibit during their movements. Indeed, Protas et al. (30) and Stanley et al. (35) reported that individuals with PD expend about 20% more energy than healthy people during movements. On the basis of these findings, interventions should be aimed at enhancing maximal strength and neuromuscular coordination so that performance of ADL become relatively less effortful. Persons with PD seem to adopt an alternative control strategy to perform SA and GI. We observed that persons with PD redistribute the TLEM between the joints and produce proportionally less ankle moment and more hip moment to perform GI (Fig. 3A) and SA (Fig. 3C). These individuals with PD seem to adopt a strategy to execute GI and SA with less torque at the most impaired joint and subsequently alter torque at adjacent joints. Such a strategy has also been observed by older adults during level walking. DeVita and Hortobágyi (6) reported that whereas the total support moments are similar in young and old adults, the distribution of moments between the joints differed. Hip angular moment impulse and work were significantly greater, whereas ankle angular moment impulse and work were significantly less compared with those in young adults. Furthermore, these authors also observed a switch to a more prominent role of the hip (less knee torque and more hip torque) during stairway ascension. In PD, the ankle plantarflexors were more adversely affected than the hip extensors, thus resulting in the alteration of the relative contribution of the individual muscle groups to the support moment. The combination of these observations of redistribution of moments to a greater reliance on proximal muscles is demonstrative of the adaptability of the human neuromuscular system to shift function from weak or impaired muscle groups to those with better neuromuscular function.

The limitations in this study include a relative homogeneous sample of patients with PD with mild disease severity, with the ADL tasks performed during optimally medicated state. Future studies need to examine differences in relative effort during ADL performance along the spectrum of patients with PD (i.e., disease duration and greater disease severity) and whether PD medication alters the ability of patients to redistribute joint moments during ADL. Future investigations should also consider examining lower extremity joint moments across a larger range of velocities because previous studies have shown greater differences between persons with PD and controls at higher velocities (9). The use of torque dynamometers should also be considered a limitation to this study. Although it is often assumed that the moments recorded by the dynamometer and the joint moments produced by muscles are equivalent, previous literature has shown that resultant moments at the knee joint and the moments measured by the dynamometer are different (3,13). Gravitational effects, inertial effects, and nonrigidity of the dynamometer–leg system can influence the equivalence of these two moments and thus introduce variability in the results (3,13).

In conclusion, the present study demonstrates that persons with PD have diminished capacities for joint moment production at the ankle, which ultimately influences the contribution and relative effort of the ankle to aid in locomotion during gait, GI, and SA. As aforementioned, these results may have important implications for rehabilitative therapy and could be used as a diagnostic aid for both clinicians and researchers. Future research should evaluate whether improving muscle strength would lead to improved functional performance in persons with PD. If the results are confirmed in larger studies, they will affirm the need for training or interventions to target the diminished capabilities in the plantarflexors designed to improve performance in moment generation and contributions to ADL.

This work was supported partly by the University of Florida National Parkinson’s Disease Foundation Center of Excellence.

All authors report that they have no financial and personal relationships with other people or organizations that could inappropriately influence (bias) the work of this article.

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

Back to Top | Article Outline

REFERENCES

1. Alexander MS, Flodin BW, Marigold DS. Prism adaptation and generalization during visually guided locomotor tasks. J Neurophysiol. 2011; 106 (2): 860–71.
2. Amano S, Roemmich RT, Skinner JW, Hass CJ. Ambulation and Parkinson disease. Phys Med Rehabil Clin N Am. 2013; 24 (2): 371–92.
3. Arampatzis A, Karamanidis K, De Monte G, Stafilidis S, Morey-Klapsing G, Brüggemann G-P. Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin Biomechanics. 2004; 19 (3): 277–83.
4. Corcos DM, Chen CM, Quinn NP, McAuley J, Rothwell JC. Strength in Parkinson’s disease: relationship to rate of force generation and clinical status. Ann Neurol. 1996; 39 (1): 79–88.
5. David FJ, Rafferty MR, Robichaud JA, et al. Progressive resistance exercise and Parkinson’s disease: a review of potential mechanisms. Parkinsons Dis. 2012; 2012: 124527.
6. DeVita P, Hortobágyi T. Age causes a redistribution of joint torques and powers during gait. J Appl Physiol (1985). 2000; 88 (5): 1804–11.
7. DeVita P, Mizelle C, Vestal A, et al. Neuromuscular reorganization during stairway locomotion in old adults. Med Sci Sports Exerc. 2001; 33 (5 Suppl): S344.
8. Dietz V, Zijlstra W, Prokop T, Berger W. Leg muscle activation during gait in Parkinson’s disease: adaptation and interlimb coordination. Electroencephalogr Clin Neurophysiol. 1995; 97 (6): 408–15.
9. Durmus B, Baysal O, Altinayar S, Altay Z, Ersoy Y, Ozcan C. Lower extremity isokinetic muscle strength in patients with Parkinson’s disease. J Clin Neurosci. 2010; 17 (7): 893–6.
10. Hass CJ, Buckley TA, Pitsikoulis C, Barthelemy EJ. Progressive resistance training improves gait initiation in individuals with Parkinson’s disease. Gait Posture. 2012; 35 (4): 669–73.
11. Hass CJ, Malczak P, Nocera J, et al. Quantitative normative gait data in a large cohort of ambulatory persons with Parkinson’s disease. PLoS One. 2012; 7 (8): e42337.
12. Hass CJ, Waddell DE, Fleming RP, Juncos JL, Gregor RJ. Gait initiation and dynamic balance control in Parkinson’s disease. Arch Phys Med Rehabil. 2005; 86 (11): 2172–6.
13. Herzog W. The relation between the resultant moments at a joint and the moments measured by an isokinetic dynamometer. J Biomech. 1988; 21 (1): 5–12.
14. Hortobágyi T, DeVita P. Altered movement strategy increases lower extremity stiffness during stepping down in the aged. J Gerontol A Biol Sci Med Sci. 1999; 54 (2): B63–70.
15. Hortobágyi T, Mizelle C, Beam S, DeVita P. Old adults perform activities of daily living near their maximal capabilities. J Gerontol A Biol Sci Med Sci. 2003; 58 (5): M453–60.
16. Inkster LM, Eng JJ, MacIntyre DL, Stoessl AJ. Leg muscle strength is reduced in Parkinson’s disease and relates to the ability to rise from a chair. Mov Disord. 2003; 18 (2): 157–62.
17. Jevsevar DS, Riley PO, Hodge WA, Krebs DE. Knee kinematics and kinetics during locomotor activities of daily living in subjects with knee arthroplasty and in healthy control subjects. Phys Ther. 1993; 73 (4): 229–39; discussion 40–2.
18. Kakinuma S, Nogaki H, Pramanik B, Morimatsu M. Muscle weakness in Parkinson’s disease: isokinetic study of the lower limbs. Eur Neurol. 1998; 39 (4): 218–22.
19. Karamanidis K, Arampatzis A. Evidence of mechanical load redistribution at the knee joint in the elderly when ascending stairs and ramps. Ann Biomed Eng. 2009; 37 (3): 467–76.
20. Karamanidis K, Arampatzis A. Altered control strategy between leading and trailing leg increases knee adduction moment in the elderly while descending stairs. J Biomech. 2011; 44 (4): 706–11.
21. Kaufman KR, An KN, Litchy WJ, Morrey BF, Chao EY. Dynamic joint forces during knee isokinetic exercise. Am J Sports Med. 1991; 19 (3): 305–16.
22. Kelly NA, Ford MP, Standaert DG, et al. Novel, high-intensity exercise prescription improves muscle mass, mitochondrial function, and physical capacity in individuals with Parkinson’s disease. J Appl Physiol (1985). 2014; 116 (5): 582–92.
23. Mickelborough J, van der Linden ML, Tallis RC, Ennos AR. Muscle activity during gait initiation in normal elderly people. Gait Posture. 2004; 19 (1): 50–7.
24. Nallegowda M, Singh U, Handa G, et al. Role of sensory input and muscle strength in maintenance of balance, gait, and posture in Parkinson’s disease: a pilot study. Am J Phys Med Rehabil. 2004; 83 (12): 898–908.
25. Nocera JR, Buckley T, Waddell D, Okun MS, Hass CJ. Knee extensor strength, dynamic stability, and functional ambulation: are they related in Parkinson’s disease? Arch Phys Med Rehabil. 2010; 91 (4): 589–95.
26. Nogaki H, Kakinuma S, Morimatsu M. Movement velocity dependent muscle strength in Parkinson’s disease. Acta Neurol Scand. 1999; 99 (3): 152–7.
27. Nogaki H, Kakinuma S, Morimatsu M. Muscle weakness in Parkinson’s disease: a follow-up study. Parkinsonism Relat Disord. 2001; 8 (1): 57–62.
28. Pang MY, Mak MK. Influence of contraction type, speed, and joint angle on ankle muscle weakness in Parkinson’s disease: implications for rehabilitation. Arch Phys Med Rehabil. 2012; 93 (12): 2352–9.
29. Pedersen SW, Oberg B, Larsson LE, Lindval B. Gait analysis, isokinetic muscle strength measurement in patients with Parkinson’s disease. Scand J Rehabil Med. 1997; 29 (2): 67–74.
30. Protas EJ, Stanley RK, Jankovic J, MacNeill B. Cardiovascular and metabolic responses to upper- and lower-extremity exercise in men with idiopathic Parkinson’s disease. Phys Ther. 1996; 76 (1): 34–40.
31. Rodriguez KL, Roemmich RT, Cam B, Fregly BJ, Hass CJ. Persons with Parkinson’s disease exhibit decreased neuromuscular complexity during gait. Clin Neurophysiol. 2013; 124 (7): 1390–7.
32. Roemmich RT, Nocera JR, Vallabhajosula S, et al. Spatiotemporal variability during gait initiation in Parkinson’s disease. Gait Posture. 2012; 36 (3): 340–3.
33. Shelburne KB, Torry MR, Pandy MG. Contributions of muscles, ligaments, and the ground-reaction force to tibiofemoral joint loading during normal gait. J Orthop Res. 2006; 24 (10): 1983–90.
34. Song J, Fisher BE, Petzinger G, Wu A, Gordon J, Salem GJ. The relationships between the unified Parkinson’s disease rating scale and lower extremity functional performance in persons with early-stage Parkinson’s disease. Neurorehabil Neural Repair. 2009; 23 (7): 657–61.
35. Stanley RK, Protas EJ, Jankovic J. Exercise performance in those having Parkinson’s disease and healthy normals. Med Sci Sports Exerc. 1999; 31 (6): 761–6.
36. Startzell JK, Owens DA, Mulfinger LM, Cavanagh PR. Stair negotiation in older people: a review. J Am Geriatr Soc. 2000; 48 (5): 567–80.
37. Stevens-Lapsley J, Kluger BM, Schenkman M. Quadriceps muscle weakness, activation deficits, and fatigue with Parkinson disease. Neurorehabil Neural Repair. 2012; 26 (5): 533–41.
Keywords:

RELATIVE EFFORT; ISOKINETIC; MUSCULAR STRENGTH; JOINT TORQUE; MOMENT; NEUROLOGICAL DISORDER

© 2015 American College of Sports Medicine