Functional impact of vibratory proprioceptive assistance in patients with facioscapulohumeral muscular dystrophy Edith Ribot-Ciscar, PhD,1, Virginie Milhe-De Bovis, MD,2, Jean-Marc Aimonetti, PhD, 1, Bernard Lapeyssonnie, PT2, Emmanuelle Campana-Salort, MD,2, Jean Pouget, MD, PhD2, Shahram Attarian, MD, PhD2 1
Aix Marseille Université, CNRS, NIA UMR 7260, 13331, Marseille, France
2
Centre de référence des maladies neuromusculaires et de la SLA, CHU la Timone,
Marseille, France
ACKNOWLEDGEMENTS: This work was supported by Association Française contre les Myopathies (AFM), CNRS and INSERM grants. Running title : Vibratory assistance in FSHD
Corresponding author: Edith Ribot-Ciscar - Aix Marseille Université, CNRS, NIA UMR 7260. FR 3C FR 3512, Case B, Centre Saint-Charles, 3 Place Victor Hugo, 13331 Marseille CEDEX 03 France. Tel: +33 4 13 55 08 33; fax: +33 4 13 55 08 42 - e-mail: [email protected] No author has a financial relationship with the company who manufactures any product or equipment discussed in this manuscript, or any other apparent conflict of interest.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as an ‘Accepted Article’, doi: 10.1002/mus.24605 This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 2 of 25
Functional impact of vibratory proprioceptive assistance in subjects with facioscapulohumeral muscular dystrophy ABSTRACT Introduction: We analyzed the effects of a rehabilitation method based on the use of vibratory proprioceptive assistance (VPA) in subjects with facioscapulohumeral muscular dystrophy. Methods: Eight subjects were given 1 month of mechanical vibratory treatment that consisted of 8 sessions of 40 min stimulation on the more affected side. During each session, illusory movements were induced as follows: sensations of extension or flexion of the forearm or elevation of the arm via vibration applied to the distal tendon of the biceps (BB), triceps brachialis (TB), or pectoralis major muscles (PM), respectively, and of elevation of the arm with extension or flexion of the forearm via vibration of PM+BB or PM+TB, respectively. Results: Treatment led to a significant increase in the amplitude of voluntary shoulder flexion, constant score, and self-rated health. Conclusion: VPA may serve as a rehabilitation method for reducing the deleterious effects of decline in motor activities.
Abbreviations: FSHD: facioscapulohumeral muscular dystrophy; VPA: vibratory proprioceptive assistance; TB: triceps brachialis; BB: biceps brachialis; PM: pectoralis major muscle.
Key Words: muscle tendon vibration; illusory movement; rehabilitation; muscular dystrophy; facioscapulohumeral muscular dystrophy; FSHD
2 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Page 3 of 25
Muscle & Nerve
INTRODUCTION Motor activities of all types (postural and segmental) generate a continuous inflow of sensory messages arising from the muscles involved and the surrounding tissues
1
. These
proprioceptive messages are involved in organization of reflexes and automatic motor activities
2
. They also contribute greatly to conscious representation of posture and
movements and consequently constitute one of the main factors involved in the organisation of voluntary motor activities 3. As an example, it has recently been shown that simple proprioceptive training that consists of discriminating subtle changes in the vibration frequency applied to muscle tendons of the hand makes it possible to restore normal motor control of the hand in cases of musician’s dystonia 4. Inversely, a progressive loss of proprioceptive inputs, as when motor activities decline, induces cortical changes that alter the capacity to send reliable commands to the effectors, as shown in patients suffering from complex regional pain syndrome 5. Studies conducted on deafferented patients with pure sensory stroke
8
6,7
or patients
also indicate such a relationship between sensory deficits and
motor disabilities. The application of muscle tendon vibrations can preserve the functional integrity of the sensory and motor systems when motor activities decline. This stimulus activates muscle spindle primary afferents
9
and generates a proprioceptive message that is interpreted by
subjects at rest with their eyes closed as a movement that would have stretched the vibrated muscle
10,11
. When appropriate patterns of vibration are applied to given muscle groups,
sensations of illusory movements as complex as writing and drawing can be induced
12,13
.
Importantly, such muscle tendon vibrations have been demonstrated to preserve normal
3 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 4 of 25
cortical sensorimotor networks in conditions of hypo-afferentation consecutive to experimental hand immobilization 14. In previous studies, we showed that patients with muscular dystrophy experience sensations of illusory movements induced by muscle tendon vibration
15
. These results account for the
fact that despite alteration of the motor component of the muscles, the sensory component (the muscle spindles) is, at least partly, spared in muscular dystrophy. This muscle sensory sparing was also supported by the results of electrophysiological studies which showed that the intrafusal muscle fibers controlling muscle receptor sensitivity are functionally preserved in that they conserve their ability to contract in response to a fusimotor drive 16. In light of these observations, we were interested in analyzing the effects of a rehabilitation method based on the use of vibratory proprioceptive assistance (VPA) that specifically activates these preserved muscle receptors in patients with muscular dystrophy. We chose to study subjects with facioscapulohumeral muscular dystrophy (FSHD). FSHD patients characteristically have difficulties performing overhead activities due to shoulder girdle weakness, which is generally visible as asymmetrical scapular winging and pectoralis muscle atrophy. The strength and magnitude of active shoulder flexion or abduction are reduced markedly. Shoulder girdle weakness is the first complaint in 82% of FSHD patients 17. Such difficulties are very incapacitating, primarily because they limit self-care and ability to reach for objects in the environment. These complaints led us to evoke sensations of illusory movements that resemble the movements that are lost progressively lost, namely the sensation of elevation of the arm with either extension or flexion of the forearm. We assessed whether activating the sensory, perceptual, and motor components by means of VPA could reduce the deleterious effects of the gradual decline in motor abilities in FSHD.
4 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Page 5 of 25
Muscle & Nerve
MATERIALS and METHODS Subjects Nine subjects (6 women, 3 men) with FSHD, as determined by molecular analysis (D4Z4 deletion in 4q35 with less than 10 repetitions), were studied. Among them, 8 (mean age: 58 ±11 years) participated in the entire protocol, and 1 who was younger (25 years old) stopped participating before the end of the protocol, and therefore, the related data were excluded from the analysis. All subjects gave informed consent for the procedure, which was approved by the local ethics committee (CPP Aix-Marseille I).
Mechanical vibration treatment At the beginning of the treatment, subjects underwent a few trials of vibratory stimulation to make them familiar with the equipment and the sensations of illusory movement. Vibrations (frequency: 80 Hz; peak-to-peak amplitude: 0.5 mm) were delivered for 10 seconds via a mechanical vibrator (DC motors with eccentric masses, 1.5 cm in diameter, Technoconcept France). The vibrator length was 4 cm for biceps (BB) and triceps brachialis (TB) stimulation and 8 cm for stimulation of the pectoralis major muscle (PM). The vibrators were applied to the tendon of the targeted muscle groups (the distal tendon for the BB and TB and in the axilla for the PM); they were held in place using elastic bands. Each treatment session consisted of 6 blocks of vibratory stimulation (Figure 1). The first block consisted of 5 trials involving stimulation of the triceps brachialis to induce a sensation of flexion of the forearm. The second block consisted of 5 stimulation trials of the PM to induce a sensation of abduction of the shoulder. The third block consisted of 10 trials in which
5 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 6 of 25
the same muscles (TB and PM) were vibrated simultaneously to induce a sensation of elevation of the arm with flexion of the forearm. The fourth block consisted of 5 trials involving biceps brachialis stimulation to induce a sensation of forearm extension, followed by 5 trials involving stimulation of the PM to induce a sensation of shoulder abduction (fifth block) and 10 trials in which the same muscles (BB and PM) were vibrated simultaneously to induce a sensation of raising the arm with extension of the forearm (sixth block). The vibration trials were each separated by a resting period of 20-30 s. In each trial, the arm was maintained in position by the experimenter so that the vibrated muscles were slightly stretched before the stimuli were applied. This condition is necessary for an illusory movement to be induced
11
. The total duration of each treatment session was generally 40
min, but it could last up to an hour if the subject experienced difficulty in achieving a mentally and physically relaxed state, which is a condition essential for feeling illusory movements. INSERT Figure 1 near here Before the treatment was applied, the subjects were instructed to keep their eyes closed, to remain as relaxed as possible, and to focus their attention on the movement of the limb. After each trial, the participants were asked to describe verbally the sensation of illusory movement they perceived and to rate its quality using a 3-level scale (1: not clear, 2: quite clear and precise, 3: resembling a real movement 18). They were also invited to make any comment they felt necessary about the illusions they had perceived. Sensations of illusory movement are often accompanied by an involuntary contraction of the antagonist to the vibrated muscle, called antagonist vibratory responses (AVRs 11). The presence of such responses was visually controlled and noted in the experimental notebook.
6 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Page 7 of 25
Muscle & Nerve
Protocol Subjects came in on the first day to undergo a complete clinical check-up that consisted of recording a medical history and performing a clinical examination (see Table 1). We performed muscle strength testing of the main body muscles and established the motor function measure (MFM,
19
); both of these indices show that our population of patients is
homogeneous. We also estimated more specifically functional scores for the upper (Brooke 20) and lower limbs (Gardner-Medwin and Walton score (SF-36
22
21
). Finally, we recorded the quality of life
) and the subject’s self-rated health on a vertical visual analog scale 23(0-100;
0=worst imaginable health state; 100=best imaginable health state). For each shoulder, radiography and ultrasound imaging were conducted, an articular examination was performed, and the constant score was defined. The constant score (maximum score=100) is a commonly used estimate of shoulder function; it includes a pain score, a functional assessment, and measurements of range of motion and strength 24. The higher value of 3 maximum isometric abduction forces, measured successively with a dynamometer, was also recorded. At the end of the examination, the treated side was determined; it corresponded to the more affected side in the case of asymmetrical disease or the dominant side when weakness was symmetrical. To be included in the sample, the subjects had to perform an active shoulder abduction that could not exceed 120° for at least 1 shoulder and to present a Brooke score of between 2 and 4. Subjects with orthopedic disease (as revealed by radiography and/or ultrasound imaging) and subjects with an operated shoulder were excluded. Any physiotherapy initiated more than 3 months prior to inclusion was maintained without change throughout the experimental period. Similarly, subjects on medication maintained that medication during the month of vibratory treatment.
7 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 8 of 25
INSERT Table 1 near here
After the initial visit, subjects underwent the VPA treatment, which consisted of 1 session of treatment (the 6 blocks described above) every 4 days for 1 month (8 sessions in total). At the end of the treatment, subjects came 1 last time for a final check-up. Both prior to and after each VPA session, we recorded the level of pain reported on an analog visual scale (0-15; 0=no pain; 15=the most pain imaginable) and shoulder abduction and flexion maximum amplitudes voluntarily executed by the subject; i.e., maximally moving the straight arm up to the side or to the front away from the body. These measures, obtained with a goniometer by the same physiotherapist, were collected for both the treated and untreated sides.
Data analysis: For each type of shoulder movement, the variation in amplitude across sessions of VPA treatment was tested statistically using a Friedman test, because the data did not follow a normal distribution, as determined with a Shapiro-Wilk test. The Wilcoxon signed rank test was used to compare pre- and post-treatment values, i.e., movement amplitudes, isometric abduction force, constant score, quality of life score, and self-rated health score. The significance level was set at P < 0.05.
8 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Page 9 of 25
Muscle & Nerve
RESULTS Induction of sensations of illusory movement Vibratory stimulation was first applied to each targeted muscle in isolation to familiarize the subject with the sensations of illusory movements. Vibration applied to the tendon of the TB or BB induced a clear sensation of flexion or extension of the forearm, and vibration applied to the PM induced a clear sensation of shoulder abduction. More complex sensations were induced by combining stimulation of 2 muscle groups simultaneously: the triceps and pectoralis major (TB+PM) or the biceps and pectoralis major (BB+PM). Under these conditions, all subjects experienced sensations that were exactly those expected: the illusion of elevation of the arm with flexion of the forearm with TB+PM and the illusion of elevation of the arm with extension of the forearm with BB+PM. The amplitudes of these illusory movements generally exceeded the amplitude of the same movements when performed voluntarily, as reported by the subjects. Furthermore, in both conditions, the sensations resembled a real movement, as revealed by the subjects’ ratings, which reached the maximum on the 3-level scale 18 (2.6 ± 0.3 with TB+PM and 2.9 ± 0.1 with BB+PM). Finally, in most trials, the experimenter noticed visually that these complex sensations of illusory movements were associated with frequent antagonist vibratory responses in the lateral deltoid muscle.
Effect of VPA on maximum amplitudes of shoulder movements Figure 2 shows the results obtained for the entire study population. It gives the values (means ± SEM) of the maximum shoulder flexion (A) and abduction (B) on the treated (black) and
9 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 10 of 25
untreated (grey) sides. On the treated side, there was a significant effect of treatment session on shoulder flexion amplitude (Friedman test, χ2(8,8)=20.53, P=0.009). In contrast, the mean flexion amplitude remained unchanged across sessions on the untreated side (χ2(8,8)=12.95, P=0.1) (Fig. 2A). Shoulder abduction amplitude also increased across sessions but without reaching significance on the treated side (χ2(8,8)=13.08, P = 0.1). Shoulder abduction also did not change on the untreated side (χ2(8,8)=9.22, P=0.3) (Fig. 2B). The effect of the entire treatment can be expressed by the difference between the before(session 1) and after-treatment (session 9) amplitudes for the entire study population (Fig. 2 C and D). This difference was significantly greater on the treated side compared with the untreated side, when considering the flexion amplitude (Wilcoxon test: Z=2.02, P=0.05). The increase in shoulder abduction was also greater on the treated side compared with the untreated side; however, this difference was not significant statistically (Z=1.54, P=0.1). Additionally, the amplitudes of movements measured before and after each session were very similar (not illustrated), i.e., the mean difference calculated for all sessions was 0.5°±2 (mean ± SEM) for shoulder flexion and 0.3°±2 for shoulder abduction. INSERT Fig. 2 near here
Effect of VPA on secondary outcomes The constant score increased significantly on the treated side from 44.8±3.8 to 54.4 ± 3.9 (Z=2.2, P
Aix Marseille Université, CNRS, NIA UMR 7260, 13331, Marseille, France
2
Centre de référence des maladies neuromusculaires et de la SLA, CHU la Timone,
Marseille, France
ACKNOWLEDGEMENTS: This work was supported by Association Française contre les Myopathies (AFM), CNRS and INSERM grants. Running title : Vibratory assistance in FSHD
Corresponding author: Edith Ribot-Ciscar - Aix Marseille Université, CNRS, NIA UMR 7260. FR 3C FR 3512, Case B, Centre Saint-Charles, 3 Place Victor Hugo, 13331 Marseille CEDEX 03 France. Tel: +33 4 13 55 08 33; fax: +33 4 13 55 08 42 - e-mail: [email protected] No author has a financial relationship with the company who manufactures any product or equipment discussed in this manuscript, or any other apparent conflict of interest.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as an ‘Accepted Article’, doi: 10.1002/mus.24605 This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 2 of 25
Functional impact of vibratory proprioceptive assistance in subjects with facioscapulohumeral muscular dystrophy ABSTRACT Introduction: We analyzed the effects of a rehabilitation method based on the use of vibratory proprioceptive assistance (VPA) in subjects with facioscapulohumeral muscular dystrophy. Methods: Eight subjects were given 1 month of mechanical vibratory treatment that consisted of 8 sessions of 40 min stimulation on the more affected side. During each session, illusory movements were induced as follows: sensations of extension or flexion of the forearm or elevation of the arm via vibration applied to the distal tendon of the biceps (BB), triceps brachialis (TB), or pectoralis major muscles (PM), respectively, and of elevation of the arm with extension or flexion of the forearm via vibration of PM+BB or PM+TB, respectively. Results: Treatment led to a significant increase in the amplitude of voluntary shoulder flexion, constant score, and self-rated health. Conclusion: VPA may serve as a rehabilitation method for reducing the deleterious effects of decline in motor activities.
Abbreviations: FSHD: facioscapulohumeral muscular dystrophy; VPA: vibratory proprioceptive assistance; TB: triceps brachialis; BB: biceps brachialis; PM: pectoralis major muscle.
Key Words: muscle tendon vibration; illusory movement; rehabilitation; muscular dystrophy; facioscapulohumeral muscular dystrophy; FSHD
2 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Page 3 of 25
Muscle & Nerve
INTRODUCTION Motor activities of all types (postural and segmental) generate a continuous inflow of sensory messages arising from the muscles involved and the surrounding tissues
1
. These
proprioceptive messages are involved in organization of reflexes and automatic motor activities
2
. They also contribute greatly to conscious representation of posture and
movements and consequently constitute one of the main factors involved in the organisation of voluntary motor activities 3. As an example, it has recently been shown that simple proprioceptive training that consists of discriminating subtle changes in the vibration frequency applied to muscle tendons of the hand makes it possible to restore normal motor control of the hand in cases of musician’s dystonia 4. Inversely, a progressive loss of proprioceptive inputs, as when motor activities decline, induces cortical changes that alter the capacity to send reliable commands to the effectors, as shown in patients suffering from complex regional pain syndrome 5. Studies conducted on deafferented patients with pure sensory stroke
8
6,7
or patients
also indicate such a relationship between sensory deficits and
motor disabilities. The application of muscle tendon vibrations can preserve the functional integrity of the sensory and motor systems when motor activities decline. This stimulus activates muscle spindle primary afferents
9
and generates a proprioceptive message that is interpreted by
subjects at rest with their eyes closed as a movement that would have stretched the vibrated muscle
10,11
. When appropriate patterns of vibration are applied to given muscle groups,
sensations of illusory movements as complex as writing and drawing can be induced
12,13
.
Importantly, such muscle tendon vibrations have been demonstrated to preserve normal
3 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 4 of 25
cortical sensorimotor networks in conditions of hypo-afferentation consecutive to experimental hand immobilization 14. In previous studies, we showed that patients with muscular dystrophy experience sensations of illusory movements induced by muscle tendon vibration
15
. These results account for the
fact that despite alteration of the motor component of the muscles, the sensory component (the muscle spindles) is, at least partly, spared in muscular dystrophy. This muscle sensory sparing was also supported by the results of electrophysiological studies which showed that the intrafusal muscle fibers controlling muscle receptor sensitivity are functionally preserved in that they conserve their ability to contract in response to a fusimotor drive 16. In light of these observations, we were interested in analyzing the effects of a rehabilitation method based on the use of vibratory proprioceptive assistance (VPA) that specifically activates these preserved muscle receptors in patients with muscular dystrophy. We chose to study subjects with facioscapulohumeral muscular dystrophy (FSHD). FSHD patients characteristically have difficulties performing overhead activities due to shoulder girdle weakness, which is generally visible as asymmetrical scapular winging and pectoralis muscle atrophy. The strength and magnitude of active shoulder flexion or abduction are reduced markedly. Shoulder girdle weakness is the first complaint in 82% of FSHD patients 17. Such difficulties are very incapacitating, primarily because they limit self-care and ability to reach for objects in the environment. These complaints led us to evoke sensations of illusory movements that resemble the movements that are lost progressively lost, namely the sensation of elevation of the arm with either extension or flexion of the forearm. We assessed whether activating the sensory, perceptual, and motor components by means of VPA could reduce the deleterious effects of the gradual decline in motor abilities in FSHD.
4 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Page 5 of 25
Muscle & Nerve
MATERIALS and METHODS Subjects Nine subjects (6 women, 3 men) with FSHD, as determined by molecular analysis (D4Z4 deletion in 4q35 with less than 10 repetitions), were studied. Among them, 8 (mean age: 58 ±11 years) participated in the entire protocol, and 1 who was younger (25 years old) stopped participating before the end of the protocol, and therefore, the related data were excluded from the analysis. All subjects gave informed consent for the procedure, which was approved by the local ethics committee (CPP Aix-Marseille I).
Mechanical vibration treatment At the beginning of the treatment, subjects underwent a few trials of vibratory stimulation to make them familiar with the equipment and the sensations of illusory movement. Vibrations (frequency: 80 Hz; peak-to-peak amplitude: 0.5 mm) were delivered for 10 seconds via a mechanical vibrator (DC motors with eccentric masses, 1.5 cm in diameter, Technoconcept France). The vibrator length was 4 cm for biceps (BB) and triceps brachialis (TB) stimulation and 8 cm for stimulation of the pectoralis major muscle (PM). The vibrators were applied to the tendon of the targeted muscle groups (the distal tendon for the BB and TB and in the axilla for the PM); they were held in place using elastic bands. Each treatment session consisted of 6 blocks of vibratory stimulation (Figure 1). The first block consisted of 5 trials involving stimulation of the triceps brachialis to induce a sensation of flexion of the forearm. The second block consisted of 5 stimulation trials of the PM to induce a sensation of abduction of the shoulder. The third block consisted of 10 trials in which
5 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 6 of 25
the same muscles (TB and PM) were vibrated simultaneously to induce a sensation of elevation of the arm with flexion of the forearm. The fourth block consisted of 5 trials involving biceps brachialis stimulation to induce a sensation of forearm extension, followed by 5 trials involving stimulation of the PM to induce a sensation of shoulder abduction (fifth block) and 10 trials in which the same muscles (BB and PM) were vibrated simultaneously to induce a sensation of raising the arm with extension of the forearm (sixth block). The vibration trials were each separated by a resting period of 20-30 s. In each trial, the arm was maintained in position by the experimenter so that the vibrated muscles were slightly stretched before the stimuli were applied. This condition is necessary for an illusory movement to be induced
11
. The total duration of each treatment session was generally 40
min, but it could last up to an hour if the subject experienced difficulty in achieving a mentally and physically relaxed state, which is a condition essential for feeling illusory movements. INSERT Figure 1 near here Before the treatment was applied, the subjects were instructed to keep their eyes closed, to remain as relaxed as possible, and to focus their attention on the movement of the limb. After each trial, the participants were asked to describe verbally the sensation of illusory movement they perceived and to rate its quality using a 3-level scale (1: not clear, 2: quite clear and precise, 3: resembling a real movement 18). They were also invited to make any comment they felt necessary about the illusions they had perceived. Sensations of illusory movement are often accompanied by an involuntary contraction of the antagonist to the vibrated muscle, called antagonist vibratory responses (AVRs 11). The presence of such responses was visually controlled and noted in the experimental notebook.
6 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Page 7 of 25
Muscle & Nerve
Protocol Subjects came in on the first day to undergo a complete clinical check-up that consisted of recording a medical history and performing a clinical examination (see Table 1). We performed muscle strength testing of the main body muscles and established the motor function measure (MFM,
19
); both of these indices show that our population of patients is
homogeneous. We also estimated more specifically functional scores for the upper (Brooke 20) and lower limbs (Gardner-Medwin and Walton score (SF-36
22
21
). Finally, we recorded the quality of life
) and the subject’s self-rated health on a vertical visual analog scale 23(0-100;
0=worst imaginable health state; 100=best imaginable health state). For each shoulder, radiography and ultrasound imaging were conducted, an articular examination was performed, and the constant score was defined. The constant score (maximum score=100) is a commonly used estimate of shoulder function; it includes a pain score, a functional assessment, and measurements of range of motion and strength 24. The higher value of 3 maximum isometric abduction forces, measured successively with a dynamometer, was also recorded. At the end of the examination, the treated side was determined; it corresponded to the more affected side in the case of asymmetrical disease or the dominant side when weakness was symmetrical. To be included in the sample, the subjects had to perform an active shoulder abduction that could not exceed 120° for at least 1 shoulder and to present a Brooke score of between 2 and 4. Subjects with orthopedic disease (as revealed by radiography and/or ultrasound imaging) and subjects with an operated shoulder were excluded. Any physiotherapy initiated more than 3 months prior to inclusion was maintained without change throughout the experimental period. Similarly, subjects on medication maintained that medication during the month of vibratory treatment.
7 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 8 of 25
INSERT Table 1 near here
After the initial visit, subjects underwent the VPA treatment, which consisted of 1 session of treatment (the 6 blocks described above) every 4 days for 1 month (8 sessions in total). At the end of the treatment, subjects came 1 last time for a final check-up. Both prior to and after each VPA session, we recorded the level of pain reported on an analog visual scale (0-15; 0=no pain; 15=the most pain imaginable) and shoulder abduction and flexion maximum amplitudes voluntarily executed by the subject; i.e., maximally moving the straight arm up to the side or to the front away from the body. These measures, obtained with a goniometer by the same physiotherapist, were collected for both the treated and untreated sides.
Data analysis: For each type of shoulder movement, the variation in amplitude across sessions of VPA treatment was tested statistically using a Friedman test, because the data did not follow a normal distribution, as determined with a Shapiro-Wilk test. The Wilcoxon signed rank test was used to compare pre- and post-treatment values, i.e., movement amplitudes, isometric abduction force, constant score, quality of life score, and self-rated health score. The significance level was set at P < 0.05.
8 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Page 9 of 25
Muscle & Nerve
RESULTS Induction of sensations of illusory movement Vibratory stimulation was first applied to each targeted muscle in isolation to familiarize the subject with the sensations of illusory movements. Vibration applied to the tendon of the TB or BB induced a clear sensation of flexion or extension of the forearm, and vibration applied to the PM induced a clear sensation of shoulder abduction. More complex sensations were induced by combining stimulation of 2 muscle groups simultaneously: the triceps and pectoralis major (TB+PM) or the biceps and pectoralis major (BB+PM). Under these conditions, all subjects experienced sensations that were exactly those expected: the illusion of elevation of the arm with flexion of the forearm with TB+PM and the illusion of elevation of the arm with extension of the forearm with BB+PM. The amplitudes of these illusory movements generally exceeded the amplitude of the same movements when performed voluntarily, as reported by the subjects. Furthermore, in both conditions, the sensations resembled a real movement, as revealed by the subjects’ ratings, which reached the maximum on the 3-level scale 18 (2.6 ± 0.3 with TB+PM and 2.9 ± 0.1 with BB+PM). Finally, in most trials, the experimenter noticed visually that these complex sensations of illusory movements were associated with frequent antagonist vibratory responses in the lateral deltoid muscle.
Effect of VPA on maximum amplitudes of shoulder movements Figure 2 shows the results obtained for the entire study population. It gives the values (means ± SEM) of the maximum shoulder flexion (A) and abduction (B) on the treated (black) and
9 John Wiley & Sons, Inc. This article is protected by copyright. All rights reserved.
Muscle & Nerve
Page 10 of 25
untreated (grey) sides. On the treated side, there was a significant effect of treatment session on shoulder flexion amplitude (Friedman test, χ2(8,8)=20.53, P=0.009). In contrast, the mean flexion amplitude remained unchanged across sessions on the untreated side (χ2(8,8)=12.95, P=0.1) (Fig. 2A). Shoulder abduction amplitude also increased across sessions but without reaching significance on the treated side (χ2(8,8)=13.08, P = 0.1). Shoulder abduction also did not change on the untreated side (χ2(8,8)=9.22, P=0.3) (Fig. 2B). The effect of the entire treatment can be expressed by the difference between the before(session 1) and after-treatment (session 9) amplitudes for the entire study population (Fig. 2 C and D). This difference was significantly greater on the treated side compared with the untreated side, when considering the flexion amplitude (Wilcoxon test: Z=2.02, P=0.05). The increase in shoulder abduction was also greater on the treated side compared with the untreated side; however, this difference was not significant statistically (Z=1.54, P=0.1). Additionally, the amplitudes of movements measured before and after each session were very similar (not illustrated), i.e., the mean difference calculated for all sessions was 0.5°±2 (mean ± SEM) for shoulder flexion and 0.3°±2 for shoulder abduction. INSERT Fig. 2 near here
Effect of VPA on secondary outcomes The constant score increased significantly on the treated side from 44.8±3.8 to 54.4 ± 3.9 (Z=2.2, P
