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Effects of a Single Hand–Exercise Session on Manual Dexterity and Strength in Persons with Parkinson Disease: A Randomized Controlled Trial
PM R XXX (2015) 1-8
www.pmrjournal.org
Original Research
Effects of a Single HandeExercise Session on Manual Dexterity and Strength in Persons with Parkinson Disease: A Randomized Controlled Trial Sara Mateos-Toset, OT, MS, Irene Cabrera-Martos, PT, MS, ´nchez, PT, MS, Araceli Ortiz-Rubio, OT, MS, Irene Torres-Sa ´lez-Jime ´nez, PhD, Marie Carmen Valenza, PT, PhD Emilio Gonza
Abstract Objective: To evaluate the effects on manual dexterity, hand grip, and pinch strength of a single intervention focused on hand exercises. Design: Randomized, controlled, blinded study. Patients: Sixty people with Parkinson disease (PD) were recruited; 30 participants were allocated to a brief exercise session and 30 to a control group. Interventions: Participants randomized to the experimental group received a 15-minute exercise session focused on hand training using therapeutic putty. Participants allocated to the control group performed active upper limb exercises. Main Outcome Measurements: Measures of manual dexterity (assessed by the Purdue Pegboard Test and the Chessington Occupational Therapy Neurologic Assessment Battery dexterity task) and strength (hand grip and pinch strength) were recorded at baseline and after the intervention. Results: Participants had significantly improved manual dexterity values (P < .05) after the intervention. They also had increased hand grip (P < .001) and pinch strength (P < .05). Conclusions: A single handeexercise session showed an improvement in manual dexterity and strength in persons with PD.
Introduction Persons with Parkinson disease (PD) frequently experience manual dexterity impairment [1] and muscle weakness [2], which has an impact on the performance of daily living activities, leading to a reduction in everyday activities and negative repercussion on quality of life. The major cause of disability in people with PD is the decrease of the quality of movement [3] affecting the performance of functional tasks because of bradykinesia, rigidity, and tremor [4]. Some studies have described difficulties in performing and maintaining repetitive and rhythmic voluntary movements [5,6]. These difficulties lead to manual dexterity impairments, with timing and force modulation affecting the quality of hand function progressively throughout the disease [3,7]. Different authors have
shown alterations in the execution of fine manipulative hand activities (eg, buttoning, handwriting, and tying shoelaces) because of reduced finger torque control and decreased interdigit individualization [1,8]. People with PD retain the ability to anticipate and plan movements but have greater difficulty combining the movements of reach and grip during active mobility, especially when the grip is made with all fingers. This impairment affects the performance of functional activities [9-11]. Additionally, some studies have reported upper-limb deficits with bilateral asymmetric motor impairments, including a delayed onset of the opening of the hand, delayed movement initiation of the forearm, lack of coordination, loss of muscle control, and difficulties in the dissociation between the left and right arm [12-14]. Muscle weakness has also been described as an important impairment related to PD, with repercussions
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Single HandeExercise Session in Persons With PD
for functionality [15]. Reduction in muscle strength can compromise the ability of individuals to perform activities that require strength and is related to muscle activation and the speed with which movements are performed [16]. Different therapeutic strategies, including exercises and directed repetitions, have improved functionality and autonomy in patients with PD who achieve relevant motor improvements [1,3]. It has also been reported that imitation learning and motor control relearning have a positive effect in the motor training [17]. Most interventional studies have focused on the lower limbs, specifically on gait and stability [18,19]. We hypothesized that a brief therapeutic intervention focused on hand exercises would have beneficial effects on manual dexterity and strength in persons with PD. The effectiveness of a single session could provide an immediate therapeutic response that is important to improve the performance of daily activities. Therefore, the aim of this study was to evaluate the effects on manual dexterity and strength of a single intervention focused on hand exercises. Methods Subjects After obtaining ethical approval from the University of Granada Ethics Committee, people with PD were recruited from a local Parkinson Association between March and July 2013. These persons received 2 sessions of physical therapy per week from the Association. Prior to participation, individuals gave informed consent in accordance with the Declaration of Helsinki. All the participants were clinically diagnosed with PD by a neurologist. Participants were eligible if they were older than 50 years and had stage II-III of disease progression as defined by the Hoehn and Yahr scale [20]. Persons were excluded if they had severe cognitive impairment (ie, a Mini-Mental State Examination score lower than 24) [21] or comprehension deficits that prevented them from following verbal commands, had visual or acoustic limitations defined as a total or partial loss of sight or hearing, were diagnosed with a neurologic condition other than PD, had musculoskeletal disorders defined as injuries or conditions affecting the musculoskeletal system including nerves, muscles, and tendons of the hand or fingers, and/or if they had previous trauma or fracture of the upper extremity. Participants were randomly assigned 1:1 to an experimental group or a control group. The randomization sequence was drawn up and kept off-site by a statistician who was not aware of the study aims, using a random number generator in blocks of 8 with no stratification. The sequence of subjects included in the experimental or control groups were mailed from the statistician to the recruiter. A research assistant assigned the participants to
the groups and contacted them by phone to obtain an appointment. The design of the study and participants’ distribution between groups is shown in Figure 1. After the allocation, baseline measures were taken. All of the data were collected by an independent researcher who was blinded to the allocation group of the patients. Anthropometric (height, weight, and body mass index) and sociodemographic (marital status and academic studies) data were obtained by self-report of each participant. The clinical records of participants were also reviewed, and the disease duration and the medication intake were obtained. The severity of PD was assessed across behaviors, activities of daily living, motor abilities, and other complications using the Movement Disorders Society-Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) [22]. Outcome Measures Trained study personnel who were unaware of group assignment performed all the outcome assessments at the university laboratory. Manual dexterity and strength were evaluated on the “on” phase in the participants included in the study at baseline and immediately after the intervention. Manual dexterity was assessed by the Purdue Pegboard Test [23]. Four subtests were included: dominant hand, nondominant hand, bimanual, and assembly task [24]. In the 3 first tasks, in 30 seconds, patients put as many pegs as possible in the holes of the board with one hand and bimanually. In the assembly task, patients have 60 seconds to manipulate pegs, collars, and washers onto the board. The score is the number of pegs and pieces placed on the board. The Purdue Pegboard Test reliably evaluates manual dexterity in patients with PD [25]. Manual coordination and speed movement is an important part of manual dexterity, and it was assessed using one component from the Chessington Occupational Therapy Neurologic Assessment Battery (COTNAB) [26]. This task consists of 3 subtests performed with dominant, nondominant, and both hands. In all the subtests, we registered the time in seconds that it took to move the blocks from one board to another. The COTNAB battery has previously shown good validity in patients with neurologic diseases [26]. Hand grip and pinch strength (lateral, distal, and tripod pinch) were measured using a dynamometer (Jamar dynamometer and pinch meter; Lafayette Instrument Company, Lafayette, IN) [27-29]. Procedures For this double-blind, randomized, controlled clinical trial, 62 participants were initially screened for eligibility. Two patients were excluded because one declined to provide informed consent and one did not meet the inclusion criteria.
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Figure 1. Flow diagram of the phases of the trial.
After the outcome measures were assessed, the exercise session started. Sessions were individualized, and the approximate duration was 15 minutes. Both intervention and control sessions took place with the therapist sitting in front of the participant, in a comfortable position with a horizontal surface between them. Visual and verbal feedback from the therapist was provided during the session for all subjects. The therapist performed the exercises at the same time as the patients, adding verbal cues to ensure the proper execution. The participants allocated to the control group performed active upper limb range of movement exercises for 15 minutes. Participants randomized to the experimental group were included in an exercise session focused on hand training. Therapeutic putty (Patterson Medical Ltd, Sutton, United Kingdom) with a softmedium resistance was used. The therapist monitored and supervised the exercises. The protocol was designed using a variety of hand-strengthening movements intended to improve hand function, including hand and finger active exercises (Figure 2). The exercises progressed from global to specific ones, finishing with finger movements and with both hands. The exercises included were rolling the putty, opening and closing the hands, and exercises involving pinch performance, finger abduction, finger adduction, finger flexion, finger extension, and finger opposition. No harm or unintended effects were reported by any participant. At the end of the intervention the independent, blinded researcher did the postintervention testing.
Statistical Analysis The data obtained were analyzed using SPSS version 20.0 (IBM Corp, Armonk, NY). Descriptive statistics (mean standard deviation) were used to determine participant characteristics. Prior to statistical analysis, the Kolmogorov-Smirnov test was performed to assess the normality of continuous data. Normally distributed variables were compared by one-way analysis of variance (ANOVA). Non-normally distributed variables (symptom duration) were compared using the KruskalWallis test, with an a level of significance of 0.05. The ANOVA was used to assess differences for repeated measures, and the statistical analysis was conducted at 95% confidence level. The sample size in the current study was powered to detect statistical differences with 85% power based on a previous pilot study. Results Thirty participants were randomly allocated to the experimental group and 30 to the control group. The main sociodemographic and clinical characteristics of the patients included in the study are shown in Table 1. The majority of participants in both groups were men, with women making up 40% of the experimental group and 33% of the control group. No statistically significant differences were found between the 2 groups for any variable. Clinical data did not demonstrate differences in the different components of MDS-UPDRS scores.
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Single HandeExercise Session in Persons With PD
Figure 2. Procedure for the hand exercise program. (A) The putty was moved between the wrist proper and the finger tips. (B) The putty was moved with the lateral part of the hand between the wrist proper and the finger tips. (C) The putty was squeezed in one hand. (D) The putty was flattened with the heel of the hand. (E) The putty was rolled between both hands. (F) After rolling the putty into a ball, it was pinched between the thumbs and all the fingers with both hands at once.
No statistically significant differences were found between the 2 groups for any measure of manual dexterity and hand grip and the different pinch strength measurements at baseline. Pre- to postintervention values regarding the manual dexterity measurements in both the intervention and control groups are shown in Table 2. Between-groups significant differences have been found in all the manual dexterity variables measured. Table 3 shows pre- to postintervention values regarding the hand grip and pinch strength
measurements in both the intervention and control groups. After performing the exercises, between-groups significant differences were found in hand grip and pinch strength variables except for tripod pinch in the nondominant hand. Discussion This study examined the effectiveness of a single therapeutic session focused on hand exercises to
Table 1 Sociodemographic and clinical variables of the participants (N ¼ 60) Variable
Intervention Group (n ¼ 30)
Control Group (n ¼ 30)
P Value
Gender, n (% women) Age, y, mean SD BMI, kg/m2, mean SD Marital status, n (%) Single Married Separated/divorced Widow/widower Academic studies, n (%) No studies Elementary school High school University degree Clinical data MMSE, mean SD Disease duration, y, mean SD MDS-UPDRS score, mean SD Part I Part II Part III Part IV Medication intake, mg/d, mean SD
12 (40) 72.60 8.86 26.56 3.21
10 (33.3) 69.97 9.59 25.68 2.33
.238 .274 .229
3 (10) 17 (56.7) 3 (10) 7 (23.3)
1 (3.3) 23 (76.7) 1 (3.3) 5 (16.7)
2 (6.70) 5 (16.70) 10 (33.3) 13 (43.3)
1 (3.35) 6 (20.00) 11 (36.70) 11 (36.70)
27.83 1.74 6.60 4.15 11.57 13.27 21.53 2.10 812.68
5.78 5.91 12.16 2.94 367.67
.654
.959
28.00 1.72 7.10 3.44
.711 .596
.770 .947 .874 .860 .994
12.00 13.37 21.03 2.23 796.43
5.63 5.78 12.08 2.89 346.04
SD ¼ standard deviation; BMI ¼ body mass index; MMSE ¼ Mini-Mental State Examination; MDS-UPDRS ¼ Movement Disorders Society-Unified Parkinson’s Disease Rating Scale; Part I ¼ Nonmotor experiences of daily living; Part II ¼ motor experiences of daily living; Part III ¼ motor examination; Part IV ¼ motor complications.
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Table 2 Pre- to postintervention values in manual dexterity measures
Purdue Pegboard Test (no. of pieces) Dominant hand Preintervention Postintervention Nondominant hand Preintervention Postintervention Bimanual task Preintervention Postintervention Assembly task Preintervention Postintervention COTNAB dexterity task(s) Dominant hand Preintervention Postintervention Nondominant hand Preintervention Postintervention Bimanual Preintervention Postintervention
Experimental Group (n ¼ 30)
Control Group (n ¼ 30)
Between-Groups Mean Change SD (95% CI)
Between-Groups P Value
8.43 2.70 9.97 2.36
9.23 1.79 9.47 1.89
0.50 1.25 (0.03, 0.97)
.037
8.17 2.79 9.03 2.31
8.87 2.03 8.57 2.09
0.47 1.17 (0.03, 0.90)
.037
5.83 2.10 6.70 2.17
6.17 1.84 6.20 1.73
0.50 1.13 (0.07, 0.93)
.023
14.50 4.93 16.60 5.05
15.20 3.45 15.83 3.77
0.77 2.05 (0.01, 1.53)
.049
43.37 10.57 39.43 8.82
41.93 7.66 41.00 8.24
1.57 3.97 (0.025, 3.05)
.039
43.13 8.36 39.03 6.58
40.77 6.08 41.03 6.14
2.00 4.99 (0.13, 2.19)
.037
27.60 7.39 24.93 5.85
26.63 4.59 27.00 5.64
2.06 4.53 (0.37, 3.76)
.018
SD ¼ standard deviation; CI ¼ confidence interval; COTNAB ¼ Chessington Occupational Therapy Neurological Assessment Battery.
improve strength and manual dexterity in persons with PD. Our main findings were the following: (1) a programmed 15-minute exercise session was able to induce a significant improvement in different manual dexterity
tasks when compared with a control intervention, and (2) a single exercise session was able to induce an increase of hand grip and pinch strength in patients with PD.
Table 3 Pre- to postintervention values in hand grip and pinch strength
Hand grip strength (kilogram force) Dominant hand Preintervention Postintervention Nondominant hand Preintervention Postintervention Pinch strength (kilogram force) Lateral pinch dominant hand Preintervention Postintervention Lateral pinch nondominant hand Preintervention Postintervention Distal pinch dominant hand Preintervention Postintervention Distal pinch nondominant hand Preintervention Postintervention Tripod pinch dominant hand Preintervention Postintervention Tripod pinch nondominant hand Preintervention Postintervention
Experimental Group (n ¼ 30)
Control Group (n ¼ 30)
Between-Groups Mean Change SD (95% CI)
Between-Groups P Value
19.67 8.41 21.53 9.10
20.43 7.25 19.93 7.75
1.60 3.94 (0.13, 3.07)
.034
17.48 7.09 19.18 7.97
18.60 6.12 18.25 7.41
0.93 2.32 (0.07, 1.80)
.036
6.71 1.64 7.03 1.76
6.92 1.69 6.58 1.77
0.45 1.18 (0.01, 0.89)
.046
6.03 1.71 6.15 1.53
5.92 1.57 5.82 1.53
0.33 0.83 (0.02, 0.64)
.037
5.10 1.68 5.73 1.76
5.45 1.56 5.35 1.82
0.38 0.81 (0.08, 0.68)
.014
4.50 1.47 5.13 1.68
4.87 1.68 4.83 1.78
0.30 0.69 (0.04, 0.55)
.024
5.71 1.93 6.26 1.93
5.50 1.67 5.68 2.05
0.63 1.27 (0.15, 1.11)
.011
5.15 1.64 5.53 1.72
5.13 1.81 5.33 1.77
0.20 0.77 (e0.08, 0.49)
.167
SD ¼ standard deviation; CI ¼ confidence interval.
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Single HandeExercise Session in Persons With PD
A hand exercise session of 15 minutes’ duration was conducted by a therapist. Different studies have reported that action observation combined with the repetition of the observed actions has a positive effect in terms of retention of information, increasing the effects on motor function [30-32]. Additionally, it has been shown that a comparison between visual and somatosensory representations of the movement is needed to consolidate a motor learning task [33]. The study of Brown et al [34] found that the visually guided tasks were less affected in the bimanual (two different actions) condition. However, the nonvisually guided tasks were adequately performed in the unimanual condition. According to the results of Gandevia and Burke [35], dexterous finger movements need continuous modification of the ongoing motor program through sensory feedback. In persons with PD, altered sensory process may interfere with motor performance. Sensory input, especially visual input, is supposed to guide and correct the movement [36]. In our study, visual feedback of the motor task was given to the patient, with the addition of verbal cues to ensure the proper performance. Manual dexterity has been described as being affected in persons with PD [37,38]. Persons diagnosed with PD have reported difficulty with fine manipulative activities and everyday hand activities [1], along with an impaired ability to perform bimanual tasks simultaneously [39,40]. After the single therapeutic session, manual dexterity significantly improved. Our intervention showed significant changes in speed and finger movements regarding the Purdue Pegboard Test and COTNAB test scores. This one-time treatment seems to be influenced by an increased attention and visual feedback to movement. It has been previously shown that compensatory visual information may improve the impaired position sense, trajectories of movements, and timing of muscle contraction in persons with PD [41]. During movement, visual information can be used as a feedback signal to monitor the moving limb and to adjust the trajectory as the hand approaches the target. Persons with PD are also more dependent on visual information than are normal subjects to compensate for deficits in motor planning [41]. Therefore, motor patterns, planning, and execution would improve when mediated by less automatic and more conscious attentional processes [42]. Reduction in muscle strength in people with PD has frequently been reported [43-45]. The dopaminergic deficit in persons with PD causes reduction in the excitatory drive of the motor cortex [46], which can affect motor unit recruitment and results in muscle weakness [47]. Muscle function of the arm includes manipulating objects, which requires the recruitment and complex integration of muscle activity from shoulder to fingers. A growing body of evidence indicates that persons with PD report weakness in some muscle groups,
specifically in the wrist and elbow muscles, even when allowance is made for the slow development of maximal force [15,48]. After the intervention, significant improvement in hand grip and pinch strength was achieved. The generation of muscle force involves the ability of the nervous system to activate the muscles effectively through motor unit recruitment [49]. It has also been suggested that early gains may be modulated by motor unit synchronization [50]. Kinesthetic input for sensory feedback and the resistance of the putty may have contributed to change the recruitment threshold of motor units with immediate effects improving the muscle contractility in the experimental group. No previous studies have reported significant differences after a brief intervention in muscle strength. Of interest, Wierzbicka et al [51] compared isometric contraction times in persons with PD and healthy control subjects and found that persons with PD who had normal levels of strength were not slower compared with the control subjects [15]. Other studies proposing hand exercises as a treatment program showed an improvement in hand function in patients with other diseases such as rheumatic or musculoskeletal diseases [52-54]. These studies included exercises focused on increasing the range of motion and the strength. Freund developed a rehabilitation program performed by persons with PD that reduced the severity of bradykinesia, with similar results to ones obtained in our study [7]. Pelosin et al [33] also found an improvement in bradykinesia in a single session of action observation. To date, a single intervention focused on the hand has not resulted in significant changes in a population with dexterity impairment and weakness. A limitation of this study is that we only looked at immediate effects in measurements, and thus it is not possible to determine how long the observed increase in manual dexterity, hand grip, and pinch strength might have lasted. Additionally, a single intervention likely does not induce significant changes in neuronal circuits that would be adequate to provide long-term benefits. Our preliminary results suggest evidence of an immediate beneficial effect on manual dexterity and strength after hand exercises are performed with therapeutic putty. These encouraging results will serve as an impetus to conduct a further randomized controlled trial with training of the patients over a set period of time, with inclusion of a monitorization of skill retention through a follow-up assessment. Results from such an investigation would provide clarity to this area of science and a greater insight into both changes in functionality and the corresponding changes in neuronal circuitry. Conclusions Our results show that a single hand exercise session with therapeutic putty is effective in terms of
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49. Garnett R, Stephens JA. Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man. J Physiol 1981;311:463-473. 50. Sale DG. Neural adaptation to resistance training. Med Sci Sports Exerc 1988;20(suppl 5):S135-S145. 51. Wierzbicka MM, Wiegner AW, Logigian EL, Young RR. Abnormal most-rapid isometric contractions in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 1991;54:210-216. 52. Dziedzic K, Hammond A, eds. Rheumatology: Evidence-Based Practice for Physiotherapists and Occupational Therapists. New York, NY: Churchill Livingstone; 2010. 53. Wessel J. The effectiveness of hand exercises for persons with rheumatoid arthritis: A systematic review. J Hand Ther 2004;17: 174-180. 54. Aldehag A, Jonsson H, Lindblad J, Kottorp A, Ansved T, Kierkegaard M. Effects of hand-training in persons with myotonic dystrophy type 1dA randomised controlled cross-over pilot study. Disabil Rehabil 2013;35:1798-1807.
Disclosure S.M.-T. Department of Physical Therapy, University of Granada, Granada, Spain Disclosure: nothing to disclose I.C.-M. Department of Physical Therapy, University of Granada, Granada, Spain Disclosure: nothing to disclose I.T.-S. Department of Physical Therapy, University of Granada, Granada, Spain Disclosure: nothing to disclose A.O.-R. Department of Physical Therapy, University of Granada, Granada, Spain Disclosure: nothing to disclose
E.G.-J. Department of Nursing, Faculty of Health Sciences, University of Granada, Granada, Spain Disclosure: nothing to disclose M.C.V. Department of Physical Therapy, University of Granada, Av de Madrid SN CP18071, Granada, Spain. Address correspondence to: M.C.V.; e-mail: [email protected] Disclosure: nothing to disclose Submitted for publication December 8, 2014; accepted June 6, 2015.
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Original Research
Effects of a Single HandeExercise Session on Manual Dexterity and Strength in Persons with Parkinson Disease: A Randomized Controlled Trial Sara Mateos-Toset, OT, MS, Irene Cabrera-Martos, PT, MS, ´nchez, PT, MS, Araceli Ortiz-Rubio, OT, MS, Irene Torres-Sa ´lez-Jime ´nez, PhD, Marie Carmen Valenza, PT, PhD Emilio Gonza
Abstract Objective: To evaluate the effects on manual dexterity, hand grip, and pinch strength of a single intervention focused on hand exercises. Design: Randomized, controlled, blinded study. Patients: Sixty people with Parkinson disease (PD) were recruited; 30 participants were allocated to a brief exercise session and 30 to a control group. Interventions: Participants randomized to the experimental group received a 15-minute exercise session focused on hand training using therapeutic putty. Participants allocated to the control group performed active upper limb exercises. Main Outcome Measurements: Measures of manual dexterity (assessed by the Purdue Pegboard Test and the Chessington Occupational Therapy Neurologic Assessment Battery dexterity task) and strength (hand grip and pinch strength) were recorded at baseline and after the intervention. Results: Participants had significantly improved manual dexterity values (P < .05) after the intervention. They also had increased hand grip (P < .001) and pinch strength (P < .05). Conclusions: A single handeexercise session showed an improvement in manual dexterity and strength in persons with PD.
Introduction Persons with Parkinson disease (PD) frequently experience manual dexterity impairment [1] and muscle weakness [2], which has an impact on the performance of daily living activities, leading to a reduction in everyday activities and negative repercussion on quality of life. The major cause of disability in people with PD is the decrease of the quality of movement [3] affecting the performance of functional tasks because of bradykinesia, rigidity, and tremor [4]. Some studies have described difficulties in performing and maintaining repetitive and rhythmic voluntary movements [5,6]. These difficulties lead to manual dexterity impairments, with timing and force modulation affecting the quality of hand function progressively throughout the disease [3,7]. Different authors have
shown alterations in the execution of fine manipulative hand activities (eg, buttoning, handwriting, and tying shoelaces) because of reduced finger torque control and decreased interdigit individualization [1,8]. People with PD retain the ability to anticipate and plan movements but have greater difficulty combining the movements of reach and grip during active mobility, especially when the grip is made with all fingers. This impairment affects the performance of functional activities [9-11]. Additionally, some studies have reported upper-limb deficits with bilateral asymmetric motor impairments, including a delayed onset of the opening of the hand, delayed movement initiation of the forearm, lack of coordination, loss of muscle control, and difficulties in the dissociation between the left and right arm [12-14]. Muscle weakness has also been described as an important impairment related to PD, with repercussions
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Single HandeExercise Session in Persons With PD
for functionality [15]. Reduction in muscle strength can compromise the ability of individuals to perform activities that require strength and is related to muscle activation and the speed with which movements are performed [16]. Different therapeutic strategies, including exercises and directed repetitions, have improved functionality and autonomy in patients with PD who achieve relevant motor improvements [1,3]. It has also been reported that imitation learning and motor control relearning have a positive effect in the motor training [17]. Most interventional studies have focused on the lower limbs, specifically on gait and stability [18,19]. We hypothesized that a brief therapeutic intervention focused on hand exercises would have beneficial effects on manual dexterity and strength in persons with PD. The effectiveness of a single session could provide an immediate therapeutic response that is important to improve the performance of daily activities. Therefore, the aim of this study was to evaluate the effects on manual dexterity and strength of a single intervention focused on hand exercises. Methods Subjects After obtaining ethical approval from the University of Granada Ethics Committee, people with PD were recruited from a local Parkinson Association between March and July 2013. These persons received 2 sessions of physical therapy per week from the Association. Prior to participation, individuals gave informed consent in accordance with the Declaration of Helsinki. All the participants were clinically diagnosed with PD by a neurologist. Participants were eligible if they were older than 50 years and had stage II-III of disease progression as defined by the Hoehn and Yahr scale [20]. Persons were excluded if they had severe cognitive impairment (ie, a Mini-Mental State Examination score lower than 24) [21] or comprehension deficits that prevented them from following verbal commands, had visual or acoustic limitations defined as a total or partial loss of sight or hearing, were diagnosed with a neurologic condition other than PD, had musculoskeletal disorders defined as injuries or conditions affecting the musculoskeletal system including nerves, muscles, and tendons of the hand or fingers, and/or if they had previous trauma or fracture of the upper extremity. Participants were randomly assigned 1:1 to an experimental group or a control group. The randomization sequence was drawn up and kept off-site by a statistician who was not aware of the study aims, using a random number generator in blocks of 8 with no stratification. The sequence of subjects included in the experimental or control groups were mailed from the statistician to the recruiter. A research assistant assigned the participants to
the groups and contacted them by phone to obtain an appointment. The design of the study and participants’ distribution between groups is shown in Figure 1. After the allocation, baseline measures were taken. All of the data were collected by an independent researcher who was blinded to the allocation group of the patients. Anthropometric (height, weight, and body mass index) and sociodemographic (marital status and academic studies) data were obtained by self-report of each participant. The clinical records of participants were also reviewed, and the disease duration and the medication intake were obtained. The severity of PD was assessed across behaviors, activities of daily living, motor abilities, and other complications using the Movement Disorders Society-Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) [22]. Outcome Measures Trained study personnel who were unaware of group assignment performed all the outcome assessments at the university laboratory. Manual dexterity and strength were evaluated on the “on” phase in the participants included in the study at baseline and immediately after the intervention. Manual dexterity was assessed by the Purdue Pegboard Test [23]. Four subtests were included: dominant hand, nondominant hand, bimanual, and assembly task [24]. In the 3 first tasks, in 30 seconds, patients put as many pegs as possible in the holes of the board with one hand and bimanually. In the assembly task, patients have 60 seconds to manipulate pegs, collars, and washers onto the board. The score is the number of pegs and pieces placed on the board. The Purdue Pegboard Test reliably evaluates manual dexterity in patients with PD [25]. Manual coordination and speed movement is an important part of manual dexterity, and it was assessed using one component from the Chessington Occupational Therapy Neurologic Assessment Battery (COTNAB) [26]. This task consists of 3 subtests performed with dominant, nondominant, and both hands. In all the subtests, we registered the time in seconds that it took to move the blocks from one board to another. The COTNAB battery has previously shown good validity in patients with neurologic diseases [26]. Hand grip and pinch strength (lateral, distal, and tripod pinch) were measured using a dynamometer (Jamar dynamometer and pinch meter; Lafayette Instrument Company, Lafayette, IN) [27-29]. Procedures For this double-blind, randomized, controlled clinical trial, 62 participants were initially screened for eligibility. Two patients were excluded because one declined to provide informed consent and one did not meet the inclusion criteria.
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Figure 1. Flow diagram of the phases of the trial.
After the outcome measures were assessed, the exercise session started. Sessions were individualized, and the approximate duration was 15 minutes. Both intervention and control sessions took place with the therapist sitting in front of the participant, in a comfortable position with a horizontal surface between them. Visual and verbal feedback from the therapist was provided during the session for all subjects. The therapist performed the exercises at the same time as the patients, adding verbal cues to ensure the proper execution. The participants allocated to the control group performed active upper limb range of movement exercises for 15 minutes. Participants randomized to the experimental group were included in an exercise session focused on hand training. Therapeutic putty (Patterson Medical Ltd, Sutton, United Kingdom) with a softmedium resistance was used. The therapist monitored and supervised the exercises. The protocol was designed using a variety of hand-strengthening movements intended to improve hand function, including hand and finger active exercises (Figure 2). The exercises progressed from global to specific ones, finishing with finger movements and with both hands. The exercises included were rolling the putty, opening and closing the hands, and exercises involving pinch performance, finger abduction, finger adduction, finger flexion, finger extension, and finger opposition. No harm or unintended effects were reported by any participant. At the end of the intervention the independent, blinded researcher did the postintervention testing.
Statistical Analysis The data obtained were analyzed using SPSS version 20.0 (IBM Corp, Armonk, NY). Descriptive statistics (mean standard deviation) were used to determine participant characteristics. Prior to statistical analysis, the Kolmogorov-Smirnov test was performed to assess the normality of continuous data. Normally distributed variables were compared by one-way analysis of variance (ANOVA). Non-normally distributed variables (symptom duration) were compared using the KruskalWallis test, with an a level of significance of 0.05. The ANOVA was used to assess differences for repeated measures, and the statistical analysis was conducted at 95% confidence level. The sample size in the current study was powered to detect statistical differences with 85% power based on a previous pilot study. Results Thirty participants were randomly allocated to the experimental group and 30 to the control group. The main sociodemographic and clinical characteristics of the patients included in the study are shown in Table 1. The majority of participants in both groups were men, with women making up 40% of the experimental group and 33% of the control group. No statistically significant differences were found between the 2 groups for any variable. Clinical data did not demonstrate differences in the different components of MDS-UPDRS scores.
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Single HandeExercise Session in Persons With PD
Figure 2. Procedure for the hand exercise program. (A) The putty was moved between the wrist proper and the finger tips. (B) The putty was moved with the lateral part of the hand between the wrist proper and the finger tips. (C) The putty was squeezed in one hand. (D) The putty was flattened with the heel of the hand. (E) The putty was rolled between both hands. (F) After rolling the putty into a ball, it was pinched between the thumbs and all the fingers with both hands at once.
No statistically significant differences were found between the 2 groups for any measure of manual dexterity and hand grip and the different pinch strength measurements at baseline. Pre- to postintervention values regarding the manual dexterity measurements in both the intervention and control groups are shown in Table 2. Between-groups significant differences have been found in all the manual dexterity variables measured. Table 3 shows pre- to postintervention values regarding the hand grip and pinch strength
measurements in both the intervention and control groups. After performing the exercises, between-groups significant differences were found in hand grip and pinch strength variables except for tripod pinch in the nondominant hand. Discussion This study examined the effectiveness of a single therapeutic session focused on hand exercises to
Table 1 Sociodemographic and clinical variables of the participants (N ¼ 60) Variable
Intervention Group (n ¼ 30)
Control Group (n ¼ 30)
P Value
Gender, n (% women) Age, y, mean SD BMI, kg/m2, mean SD Marital status, n (%) Single Married Separated/divorced Widow/widower Academic studies, n (%) No studies Elementary school High school University degree Clinical data MMSE, mean SD Disease duration, y, mean SD MDS-UPDRS score, mean SD Part I Part II Part III Part IV Medication intake, mg/d, mean SD
12 (40) 72.60 8.86 26.56 3.21
10 (33.3) 69.97 9.59 25.68 2.33
.238 .274 .229
3 (10) 17 (56.7) 3 (10) 7 (23.3)
1 (3.3) 23 (76.7) 1 (3.3) 5 (16.7)
2 (6.70) 5 (16.70) 10 (33.3) 13 (43.3)
1 (3.35) 6 (20.00) 11 (36.70) 11 (36.70)
27.83 1.74 6.60 4.15 11.57 13.27 21.53 2.10 812.68
5.78 5.91 12.16 2.94 367.67
.654
.959
28.00 1.72 7.10 3.44
.711 .596
.770 .947 .874 .860 .994
12.00 13.37 21.03 2.23 796.43
5.63 5.78 12.08 2.89 346.04
SD ¼ standard deviation; BMI ¼ body mass index; MMSE ¼ Mini-Mental State Examination; MDS-UPDRS ¼ Movement Disorders Society-Unified Parkinson’s Disease Rating Scale; Part I ¼ Nonmotor experiences of daily living; Part II ¼ motor experiences of daily living; Part III ¼ motor examination; Part IV ¼ motor complications.
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Table 2 Pre- to postintervention values in manual dexterity measures
Purdue Pegboard Test (no. of pieces) Dominant hand Preintervention Postintervention Nondominant hand Preintervention Postintervention Bimanual task Preintervention Postintervention Assembly task Preintervention Postintervention COTNAB dexterity task(s) Dominant hand Preintervention Postintervention Nondominant hand Preintervention Postintervention Bimanual Preintervention Postintervention
Experimental Group (n ¼ 30)
Control Group (n ¼ 30)
Between-Groups Mean Change SD (95% CI)
Between-Groups P Value
8.43 2.70 9.97 2.36
9.23 1.79 9.47 1.89
0.50 1.25 (0.03, 0.97)
.037
8.17 2.79 9.03 2.31
8.87 2.03 8.57 2.09
0.47 1.17 (0.03, 0.90)
.037
5.83 2.10 6.70 2.17
6.17 1.84 6.20 1.73
0.50 1.13 (0.07, 0.93)
.023
14.50 4.93 16.60 5.05
15.20 3.45 15.83 3.77
0.77 2.05 (0.01, 1.53)
.049
43.37 10.57 39.43 8.82
41.93 7.66 41.00 8.24
1.57 3.97 (0.025, 3.05)
.039
43.13 8.36 39.03 6.58
40.77 6.08 41.03 6.14
2.00 4.99 (0.13, 2.19)
.037
27.60 7.39 24.93 5.85
26.63 4.59 27.00 5.64
2.06 4.53 (0.37, 3.76)
.018
SD ¼ standard deviation; CI ¼ confidence interval; COTNAB ¼ Chessington Occupational Therapy Neurological Assessment Battery.
improve strength and manual dexterity in persons with PD. Our main findings were the following: (1) a programmed 15-minute exercise session was able to induce a significant improvement in different manual dexterity
tasks when compared with a control intervention, and (2) a single exercise session was able to induce an increase of hand grip and pinch strength in patients with PD.
Table 3 Pre- to postintervention values in hand grip and pinch strength
Hand grip strength (kilogram force) Dominant hand Preintervention Postintervention Nondominant hand Preintervention Postintervention Pinch strength (kilogram force) Lateral pinch dominant hand Preintervention Postintervention Lateral pinch nondominant hand Preintervention Postintervention Distal pinch dominant hand Preintervention Postintervention Distal pinch nondominant hand Preintervention Postintervention Tripod pinch dominant hand Preintervention Postintervention Tripod pinch nondominant hand Preintervention Postintervention
Experimental Group (n ¼ 30)
Control Group (n ¼ 30)
Between-Groups Mean Change SD (95% CI)
Between-Groups P Value
19.67 8.41 21.53 9.10
20.43 7.25 19.93 7.75
1.60 3.94 (0.13, 3.07)
.034
17.48 7.09 19.18 7.97
18.60 6.12 18.25 7.41
0.93 2.32 (0.07, 1.80)
.036
6.71 1.64 7.03 1.76
6.92 1.69 6.58 1.77
0.45 1.18 (0.01, 0.89)
.046
6.03 1.71 6.15 1.53
5.92 1.57 5.82 1.53
0.33 0.83 (0.02, 0.64)
.037
5.10 1.68 5.73 1.76
5.45 1.56 5.35 1.82
0.38 0.81 (0.08, 0.68)
.014
4.50 1.47 5.13 1.68
4.87 1.68 4.83 1.78
0.30 0.69 (0.04, 0.55)
.024
5.71 1.93 6.26 1.93
5.50 1.67 5.68 2.05
0.63 1.27 (0.15, 1.11)
.011
5.15 1.64 5.53 1.72
5.13 1.81 5.33 1.77
0.20 0.77 (e0.08, 0.49)
.167
SD ¼ standard deviation; CI ¼ confidence interval.
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Single HandeExercise Session in Persons With PD
A hand exercise session of 15 minutes’ duration was conducted by a therapist. Different studies have reported that action observation combined with the repetition of the observed actions has a positive effect in terms of retention of information, increasing the effects on motor function [30-32]. Additionally, it has been shown that a comparison between visual and somatosensory representations of the movement is needed to consolidate a motor learning task [33]. The study of Brown et al [34] found that the visually guided tasks were less affected in the bimanual (two different actions) condition. However, the nonvisually guided tasks were adequately performed in the unimanual condition. According to the results of Gandevia and Burke [35], dexterous finger movements need continuous modification of the ongoing motor program through sensory feedback. In persons with PD, altered sensory process may interfere with motor performance. Sensory input, especially visual input, is supposed to guide and correct the movement [36]. In our study, visual feedback of the motor task was given to the patient, with the addition of verbal cues to ensure the proper performance. Manual dexterity has been described as being affected in persons with PD [37,38]. Persons diagnosed with PD have reported difficulty with fine manipulative activities and everyday hand activities [1], along with an impaired ability to perform bimanual tasks simultaneously [39,40]. After the single therapeutic session, manual dexterity significantly improved. Our intervention showed significant changes in speed and finger movements regarding the Purdue Pegboard Test and COTNAB test scores. This one-time treatment seems to be influenced by an increased attention and visual feedback to movement. It has been previously shown that compensatory visual information may improve the impaired position sense, trajectories of movements, and timing of muscle contraction in persons with PD [41]. During movement, visual information can be used as a feedback signal to monitor the moving limb and to adjust the trajectory as the hand approaches the target. Persons with PD are also more dependent on visual information than are normal subjects to compensate for deficits in motor planning [41]. Therefore, motor patterns, planning, and execution would improve when mediated by less automatic and more conscious attentional processes [42]. Reduction in muscle strength in people with PD has frequently been reported [43-45]. The dopaminergic deficit in persons with PD causes reduction in the excitatory drive of the motor cortex [46], which can affect motor unit recruitment and results in muscle weakness [47]. Muscle function of the arm includes manipulating objects, which requires the recruitment and complex integration of muscle activity from shoulder to fingers. A growing body of evidence indicates that persons with PD report weakness in some muscle groups,
specifically in the wrist and elbow muscles, even when allowance is made for the slow development of maximal force [15,48]. After the intervention, significant improvement in hand grip and pinch strength was achieved. The generation of muscle force involves the ability of the nervous system to activate the muscles effectively through motor unit recruitment [49]. It has also been suggested that early gains may be modulated by motor unit synchronization [50]. Kinesthetic input for sensory feedback and the resistance of the putty may have contributed to change the recruitment threshold of motor units with immediate effects improving the muscle contractility in the experimental group. No previous studies have reported significant differences after a brief intervention in muscle strength. Of interest, Wierzbicka et al [51] compared isometric contraction times in persons with PD and healthy control subjects and found that persons with PD who had normal levels of strength were not slower compared with the control subjects [15]. Other studies proposing hand exercises as a treatment program showed an improvement in hand function in patients with other diseases such as rheumatic or musculoskeletal diseases [52-54]. These studies included exercises focused on increasing the range of motion and the strength. Freund developed a rehabilitation program performed by persons with PD that reduced the severity of bradykinesia, with similar results to ones obtained in our study [7]. Pelosin et al [33] also found an improvement in bradykinesia in a single session of action observation. To date, a single intervention focused on the hand has not resulted in significant changes in a population with dexterity impairment and weakness. A limitation of this study is that we only looked at immediate effects in measurements, and thus it is not possible to determine how long the observed increase in manual dexterity, hand grip, and pinch strength might have lasted. Additionally, a single intervention likely does not induce significant changes in neuronal circuits that would be adequate to provide long-term benefits. Our preliminary results suggest evidence of an immediate beneficial effect on manual dexterity and strength after hand exercises are performed with therapeutic putty. These encouraging results will serve as an impetus to conduct a further randomized controlled trial with training of the patients over a set period of time, with inclusion of a monitorization of skill retention through a follow-up assessment. Results from such an investigation would provide clarity to this area of science and a greater insight into both changes in functionality and the corresponding changes in neuronal circuitry. Conclusions Our results show that a single hand exercise session with therapeutic putty is effective in terms of
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Disclosure S.M.-T. Department of Physical Therapy, University of Granada, Granada, Spain Disclosure: nothing to disclose I.C.-M. Department of Physical Therapy, University of Granada, Granada, Spain Disclosure: nothing to disclose I.T.-S. Department of Physical Therapy, University of Granada, Granada, Spain Disclosure: nothing to disclose A.O.-R. Department of Physical Therapy, University of Granada, Granada, Spain Disclosure: nothing to disclose
E.G.-J. Department of Nursing, Faculty of Health Sciences, University of Granada, Granada, Spain Disclosure: nothing to disclose M.C.V. Department of Physical Therapy, University of Granada, Av de Madrid SN CP18071, Granada, Spain. Address correspondence to: M.C.V.; e-mail: [email protected] Disclosure: nothing to disclose Submitted for publication December 8, 2014; accepted June 6, 2015.