Active music therapy approach for stroke patients in the post-acute rehabilitation

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1 Neurol Sci (2017) 38: DOI /s BRIEF COMMUNICATION Active music therapy approach for stroke patients in the post-acute rehabilitation Alfredo Raglio 1 Alberto Zaliani 1 Paola Baiardi 1 Daniela Bossi 1 Cinzia Sguazzin 1 Edda Capodaglio 1 Chiara Imbriani 1 Giulia Gontero 1 Marcello Imbriani 1,2 Received: 20 August 2016 / Accepted: 20 January 2017 / Published online: 30 January 2017 Ó Springer-Verlag Italia 2017 Abstract Guidelines in stroke rehabilitation recommend the use of a multidisciplinary approach. Different approaches and techniques with music are used in the stroke rehabilitation to improve motor and cognitive functions but also psychological outcomes. In this randomized controlled pilot trial, relational active music therapy approaches were tested in the post-acute phase of disease. Thirty-eight hospitalized patients with ischemic and hemorrhagic stroke were recruited and allocated in two groups. The experimental group underwent the standard of care (physiotherapy and occupational therapy daily sessions) and relational active music therapy treatments. The control group underwent the standard of care only. Motor functions and psychological aspects were assessed before and after treatments. Music therapy process was also evaluated using a specific rating scale. All groups showed a positive trend in quality of life, functional and disability levels, and gross mobility. The experimental group showed a decrease of anxiety and, in particular, of depression (p = 0.016). In addition, the strength of non-dominant hand (grip) significantly increased in the experimental group (p = 0.041). Music therapy assessment showed a significant improvement over time of non-verbal and sonorous-music relationships. Future studies, including a greater number of patients and follow-up evaluations, are needed to confirm promising results of this study. & Alfredo Raglio alfredo.raglio@icsmaugeri.it 1 2 Istituti Clinici Scientifici Maugeri, Scientific Institute of Pavia, Pavia 27100, Italy Department of Public Health, Experimental ad Forensic Medicine, Section of Occupational Health, University of Pavia, Via Boezio 28, Pavia 27100, Italy Keywords Stroke Music therapy Rehabilitation Psychological outcomes Motor outcomes Communication Introduction Guidelines in stroke rehabilitation recommend the use a multidisciplinary approach. Neurorehabilitation with music is supported by studies showing how music facilitates neural connections and neuronal reorganization of the sensorimotor cortex [1, 2]. Neurological Music Therapy techniques [3] in the stroke rehabilitation are mainly used to improve motor functions (in particular gait functions and upper limbs motor skills) [4, 5] or language functions [6]. Other interventions are referred to the movement sonification (audio-feedback during rehabilitative activities) or to the music-supported motor training [7]. Literature showed also how listening to preferred music can promote cognitive recovery and mood improvement [8]. In this study, a relational active music therapy approach (RAMT) aimed at improving mainly psychological outcomes and communicative/relational aspects. It was also hypothesized that RAMT can improve fine and gross motor skills, in particular in upper extremities. RAMT sessions were based on free interactions between patients and music therapist using rhythmical-melodic instruments (i.e., xylophones, glockenspiels, drums, bongos, ethnic percussions, etc) in a non-verbal setting. During RAMT, the music therapist invites patients to play an active role and to interact using musical instruments. Patients music performances are stimulated mainly by rhythmical patterns involving and improving both motor and emotional functions. Therefore, these interactions

2 894 Neurol Sci (2017) 38: facilitate the expression, modulation, and sharing of patients emotions ( affect attunement moments) [9] and promote communication and motor rehabilitation. Methods Thirty-eight hospitalized right-handed patients with ischemic (n = 35) and hemorrhagic (n = 3) stroke were recruited immediately after the acute phase (during a rehabilitation period of 6 8 weeks) and were randomly allocated in the experimental (n = 19) and control (n = 19) groups. Table 1 summarizes baseline clinical characteristics of the sample. The experimental group underwent the standard of care and RAMT, and the control group underwent standard of care only. In the experimental group, the time of RAMT intervention was subtracted from the standard of care rehabilitation to balance the global time of interventions in the two groups. Inclusion criteria were: Mini Mental State Examination C18, age C40 years, stable clinical conditions, absence of other neurologic and psychiatric diseases, sufficient autonomy in motor functions of upper limbs to use musical instruments, including in the MT setting, and cooperation during music therapy (MT) interaction. Patients with a total aphasia, amusia, previous neurological or psychiatric diseases, or those who underwent previous MT treatments or musical training or practice were excluded from the study. MT sessions were conducted by a trained music therapist and were videotaped with a fixed video camera to perform an MT assessment. MT intervention consisted of 20 RAMT sessions lasting 30 min each, threeweekly. The standard of care treatment consisted of daily sessions of physiotherapy (passive/assisted active mobilization and neurorehabilitative techniques of paretic upper limbs, coordination and balance exercises, and gait training) and occupational therapy (exercises improving fine motor skills and recovering activities of daily living). Any type of psychotropic medications was not administered to the patients during the study. Table 1 Baseline clinical characteristics of experimental and control group patients Experimental group (n = 19) Control group (n = 19) Mean ± SD or N (%) Range Mean ± SD or N (%) Range Sex (M/F) 8 (42%)/11 (58%) 8 (42%)/11 (58%) Education None 6 (31.6%) 7 (36.8%) Primary school 6 (31.6%) 7 (36.8%) Secondary school 6 (31.6%) 5 (13.1%) Degree 1 (5.2%) 0 Age 70.4 ± ± Handedness (right handed) 19 (100%) 19 (100%) Hand motility LP = 8 (42.1%) SLP = 1 (5.3%) LPL = 1 (5.3%) SRP = 6 (31.5%) RP = 3 (15.8%) LP = 2 (10.5%) SLP = 8 (42.1%) SRP = 3 (15.8%) RP = 4 (21.1%) RPL = 2 (10.5%) Lesion type Ischemic 17 (89.5%) 18 (94.7%) Hemorrhagic 2 (10.5%) 1 (5.3%) Lesion site R-BG = 3; B-F, L-P = 1; R-P = 2; L-F = 2; L-MO = 1; B-F = 2; L-C = 1; B-MII = 2; R-T = 1; B-BG = 1; R-FP = 1; R-MO = 1; B-FP = 1 Aphasia 1 (5.3%) 1 (5.3%) Apraxia 2 (10.5%) Dysarthria 9 (47.4%) 8 (42.1%) Thrombolytic treatment 1 (5.3%) 0 L-FTP = 1; B-F,L-CR = 1; B-MII = 5; R-C = 2; B-BG = 1; L-F = 2; L-C = 1; L-BG = 1; B-C, L-P = 1; L-O = 1; R-P = 1; R-F = 1; R-MO = 1 R right, L left, B bilateral, MII multiple ischemic injury, MO medulla oblongata, BG basal ganglia, C cerebellum, T temporal, F frontal, FT fronto-temporal, FTP fronto-temporo-parietal, P parietal, FP fronto-parietal, O occipital, CR corona radiata, LP left paresis, SLP slight left paresis, LPL left plegia, RP right paresis, RP right paresis, RPL right plegia

3 Neurol Sci (2017) 38: A multidimensional assessment was carried out by blinded evaluators before (T0) and after (T1) treatments, using different tools: the Italian version of the National Institutes of Health Stroke Scale (It-NIHSS) to evaluate the stroke-related neurologic deficit; the Functional Independence Measure (FIM) to assess physical and cognitive disability; the Grip-Pinch Dynamometric Test; and the 9Hole Peg Test to quantify strength/dexterity of the hands and the Timed Up and Go Test (TUG) for gross mobility. The Aachener Aphasie Test (Italian version) [10] and a short version of the Montreal Battery of Evaluation of Amusia MBEA (rhythm and melodic contour perception) [11] were used before study to exclude the presence of aphasia or amusia in the patients. Psychological traits (anxiety and depression conditions) and quality of life were assessed using the Hospital Anxiety and Depression Scale (HADS) and the Italian version of McGill Quality-of-Life Questionnaire (MQOL- It). Moreover, trained music therapists not involved in the MT process evaluated the video-recorded sessions (nonverbal and sonorous-music relationship) using the Music Therapy Rating Scale (MTRS) [12]. This tool was created to assess the trend of the relationship between the patient Table 2 Psychological, functional, and motor outcomes in experimental and control groups at baseline (T0) and at the end (T1) of treatment (mean ± standard deviation; Significance = p \ 0.05) Experimental group Control group Global trend (p) MQoL-It (Global Score) T0 6.8 ± ± T ± ± 1.68 HADS-A T ± ± T ± ± 3.97 HADS-D T ± ± T ± ± 3.11 It-NIHSS T ± ± 2.27 < T ± ± 2.04 FIM T ± ± < T ± ± Grip-pinch test T0 Grip (DH) ± ± T1 Grip (DH) ± ± 9.69 T0 Grip (NDH) ± ± T1 Grip (NDH) ± ± 9.54 T0 Pinch (DH) 7.52 ± ± T1 Pinch (DH) 8.09 ± ± 4.35 T0 Pinch (NDH) 6.06? ? T1 Pinch (NDH) 6.08? ? Hole peg test T0 (DH) ± ± T1 (DH) ± ± 8.9 T0 (NDH) ± ± T1 (NDH) 42.8 ± ± 8.49 Timed Up & Go test T ± ± T ± ± 7.52 Group*time interaction (p) Bold indicates p \ 0.05 MQoL-It Italian version of McGill Quality-of-Life Questionnaire, HADS-A Hospital Anxiety and Depression Scale (Anxiety), HADS-D Hospital Anxiety and Depression Scale (Depression), NIHSS Italian version of the National Institutes of Health Stroke Scale, FIM functional independence measure, DH dominant hand, NDH non-dominant hand

4 896 Neurol Sci (2017) 38: and the therapist during the RAMT treatment. In this study, the MTRS was used by independent evaluators that observed the videotapes of RAMT sessions. The level of non-verbal and sonorous-music relationship behaviors was ranked from 0 (no relationship) to 4 (maximum relationship) points of intensity. This score was assigned at each 15 s interval of the selected sessions. RAMT sessions 1, 5, 10, 15, and 20 were analyzed (considering all patients included in the experimental group) in terms of mean of non-verbal and sonorous-music relationships, to evaluate the trend of RAMT process. Descriptive statistics were carried out for all the recorded variables. Repeated measures analysis of variance (ANOVA) models with one factor was run to evaluate differences between groups (experiment vs standard of care) over time (baseline vs end of treatment). A significant group*time interaction term (p \ 0.05) was used to detect these differences. Repeated measure ANOVA was also used to assess differences over time in MTRS assessments (sessions 1 20). This study was approved by the Local Ethical Committee (No. 823 CEC, 2012/05/07), and all patients signed an informed consent before the beginning of the study. Results No clinical differences between groups were found. All groups showed a significant positive trend in quality of life (MQoL-it global score) (p = 0.04). This trend was stronger in the experimental group (?14%) vs control group (?3%). The experimental group showed also a decrease of anxiety and depression (p = 0.016). Functional and disability levels globally improved both in experimental and control groups (p = 0.001) as well as gross mobility (p = 0.032), but the strength of non-dominant hand (left in all patients recruited in the study) significantly increased in the experimental group compared to the control group (p = 0.041). In particular, in the Experimental Group, 50% of left paretic patients (n = 5) improved the Grip scores (Grip-Pinch Test), while in Control Group, only 20% of left paretic patients (n = 2) improved that scores. Main results are summarized in Table 2. MT assessment showed a significant improvement of the relationship (non-verbal and sonorous-music communication) between patients and music therapist (Fig. 1). Discussion Study results confirmed the positive impact of RAMT on psychological outcomes in the post-acute rehabilitation of stroke patients, in particular on depression and quality of NV SM NV+SM p= Session 1 Session 5 Session 10 Session 15 Session 20 life. RAMT has also increased the communication and empathetic relationship moments between patients and the music therapist, facilitating emotional expression and sharing. Motor functions (in particular upper limb and hand movements) were stimulated by use of musical instruments making possible the combination and integration of physical and psychological aspects. In this perspective, a selection of musical instruments during MT sessions could be appropriate to support specific movements considering rehabilitative aims. Hand motility (grip) significantly improved in the Experimental Group, also in paretic upper limb, proving the efficacy of music therapy also in impaired arms rehabilitation. This result could be explained considering the training effect of music therapy sessions that involve cortical motor areas but also auditory and integrative auditory sensorimotor circuits, promoting plastic changes in the motor system [1, 5, 13 16]. Two critical points of the study are the small number of recruited patients and the lack of a follow-up assessment. This aspect is related to the patients difficulties to go back to the rehabilitative center (the most part of the patients arrived from places very far from hospital). In conclusion, the study showed that RAMT can have a positive impact on the general well-being and motivation in the post-acute rehabilitation of stroke patients improving their psychological conditions and fine motor functions. Future studies, including a greater number of patients and a follow-up evaluation, are needed to confirm these promising results. Compliance with ethical standards p= p=0.003 p=>0.001 p=0.037 p=0.005 p=0.015 p=0.012 p=0.001 Fig. 1 Trend of non-verbal, Sonorous-music, and non-verbal? sonorous-music relationships during Sessions 1, 5, 10, 15, and 20 (significance = p \ 0.05; assessment of significant improvements between the considered session and the previous session) Conflict of interest The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

5 Neurol Sci (2017) 38: Funding The authors received no financial support for the research, authorship, and/or publication of this article. References 1. Altenmüller E, Marco-Pallares J, Münte TF, Schneider S (2009) Neural organization underlies improvement in stroke induced motor dysfunction by music supported therapy. Ann N Y Acad Sci 1169: Ripollés P, Rojo N, Grau-Sánchez J et al (2015) Music supported therapy promotes motor plasticity in individuals with chronic stroke. Brain Imaging Behav. doi: /s x 3. Thaut MH (2015) The discovery of human auditory-motor entrainment and its role in the development of neurologic music therapy. Prog Brain Res 217: Bradt J, Magee WL, Dileo C, Wheeler BL, McGilloway E (2010) Music therapy for acquired brain injury. Cochrane Database Syst Rev 7:CD Schneider S, Schonle PW, Altenmuller E, Munte TF (2007) Using musical instruments to improve motor skill recovery following a stroke. J Neurol 254(1339):46 6. Zumbansen A, Peretz I, Hébert S (2014) Melodic intonation therapy: back to basics for future research. Front Neurol 28: Scholz DS, Rhode S, Großbach M et al (2015) Moving with music for stroke rehabilitation: a sonification feasibility study. Ann N Y Acad Sci 1337: Särkämö T, Tervaniemi M, Laitinen S et al (2008) Music listening enhances cognitive recovery and mood after middle cerebral artery stroke. Brain 131: Raglio A, Oasi O, Gianotti M et al (2015) Improvement of spontaneous language in stroke patients with chronic aphasia treated with music therapy: a randomized controlled trial. Int J Neurosci 126: Luzzatti C, Wilmes K, De Bleser R (1996) Aachner Aphasie Test (AAT), versione Italiana, seconda edizione. Organizzazioni Speciali, Firenze, Italy 11. Peretz I, Champod AS, Hyde K (2003) Varieties of musical disorders. The Montreal battery of evaluation of Amusia. Ann N Y Acad Sci 999: Raglio A, Traficante D, Oasi O (2011) The evaluation of music therapy process in the intersubjective perspective: the music therapy rating scale. A pilot study. Pragmat Obs Res 2: Bangert M, Altenmuller E (2003) Mapping perception to action in piano practice: a longitudinal DC-EEG-study. BMC Neurosci 4: Bangert M, Peschel T, Schlaug G et al (2006) Shared networks for auditory and motor processing in professional pianists: evidence from fmri conjunction. NeuroImage 30: Meyer M, Elmer S, Baumann S, Jancke L (2007) Shorttermplasticity in the auditory system: differential neural responses to perception and imagery of speech and music. Restor Neurol Neurosci 25: Baumann S, Koeneke S, Schmidt CF et al (2007) A network for audio-motor coordination in skilled pianists and non-musicians. Brain Res 1161:65 78

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