Ann. N.Y. Acad. Sci. ISSN 0077-8923
A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S Issue: The Neurosciences and Music V
Efficacy of musical interventions in dementia: methodological requirements of nonpharmacological trials 1 Severine Samson,1,2 Sylvain Clement, Pauline Narme,3 Loris Schiaratura,4 ´ ´ 1,5 and Nathalie Ehrle´ 1
Equipe Neuropsychologie: Audition, Cognition et Action (EA 4072), UFR de psychologie, Universite´ Lille-Nord de France, Hopital Pitie-Salp etri Paris, France. 3 Equipe Neuropsychologie du Villeneuve d’Ascq, France. 2 Unite´ d’epilepsie, ´ ˆ ´ ˆ ere, ` Vieillissement (EA 4468), Institut de Psychologie, Universite´ Paris Descartes, Paris, France. 4 Laboratoire de Psychologie: Interactions Temps Emotions Cognition (EA 4072), UFR de psychologie, Universite´ Lille-Nord de France, Villeneuve d’Ascq, Maison-Blanche, CMRR Champagne-Ardenne, France France. 5 Service de Neurologie, CHU de Reims, Hopital ˆ Address for correspondence: Severine Samson, Department of Psychology, University of Lille, BP 60 149, 59653 Villeneuve ´ d’Ascq Cedex, France. [email protected]
The management of patients with Alzheimer’s disease is a significant public health problem given the limited effectiveness of pharmacological therapies combined with iatrogenic effects of drug treatments in dementia. Consequently, the development of nondrug care, such as musical interventions, has become a necessity. The experimental rigor of studies in this area, however, is often lacking. It is therefore difficult to determine the impact of musical interventions on patients with dementia. As part of a series of studies, we carried out randomized controlled trials to compare the effectiveness of musical activities to other pleasant activities on various functions in patients with severe Alzheimer’s disease. The data obtained in these trials are discussed in light of the methodological constraints and requirements specific to these clinical studies. Although the results demonstrate the power of music on the emotional and behavioral status of patients, they also suggest that other pleasant activities (e.g., cooking) are also effective, leaving open the question about the specific benefits of music in patients with dementia. All these findings highlight the promising potential for nonpharmacological treatments to improve the well-being of patients living in residential care and to reduce caregiver burden. Keywords: Alzheimer’s disease; music; nonpharmacological treatment; randomized controlled trial; emotion
Music-based therapeutic strategies in persons with dementia The management of memory and behavioral disorders in patients with dementia (PWD) is currently unsatisfactory. Behavioral disorders are particularly difficult to control and represent a main cause of institutionalization1 and caregiver distress.2 In recent years, significant advances have been made in terms of understanding the pathophysiological mechanisms of neurodegenerative diseases, but current pharmacological treatments are essentially symptomatic and do not have a satisfactory impact on symptoms related to dementia progression. The limited effectiveness of these treatments and severe iatrogenesis associated with neuroleptics have led several health institutions to recommend the
development of nonpharmacological complementary interventions as first-line treatment.3,4 As a result, music activities are seeing a growing success with PWD as well as with caregivers. PWD are reactive to music until very advanced stages of the disease5–8 and can learn and recognize musical tunes even in the severe stage. In contrast with impaired verbal memory,6,9 music memory seems to be partially preserved in PWD.5 In addition, music easily elicits movements stimulating interactions between perception and action systems, as already underlined by Fraisse, Ol´eron, and Paillard.10 These effects may be underpinned by diminished control of inhibition in patients with severe Alzheimer’s disease (AD). Indeed, it is common to observe patients who spontaneously synchronize their movements with music, and this can
doi: 10.1111/nyas.12621 C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
249
Musical interventions in dementia
Samson et al.
subsequently facilitate social cohesion in a group setting. Finally, by inducing strong emotions,11,12 music can also help patients to relax by modulating psychological and physiological functions, especially those related to stress.13 As a consequence, the power of music and its nonverbal nature offer a privileged communication medium when language is diminished or abolished. Although the mechanisms underlying all these effects remain poorly understood, the intriguing sensitivity of PWD to music justifies its use for therapeutic purposes.
associated with biased estimates of treatment effects and with systematic errors. In this paper, we discuss this issue by reporting two successive studies to illustrate how methodological weaknesses might bias results by amplifying the effect of a music intervention and to warn clinicians and scientists about the hasty conclusions that can result from a lack of experimental rigor.
Assessing the efficacy of music-based interventions in PWD
In two previous studies,17,19 we performed RCTs to examine the short- and long-term effects of a music intervention (group-based musical activities) on emotional state and behavioral functioning of PWD. The main objective was to assess the efficacy of nonpharmacological treatments on the well-being of PWD. We were also interested in testing the possible superiority of music over nonmusic interventions. As a nonmusical activity, we selected cooking as it provides an ideal control intervention for music. Both activities are easily performed in a group setting, are multisensory, pleasurable, and can trigger old memories. The similarities and differences between these two studies are summarized in Table 1.
In the literature, numerous studies have claimed that music-based interventions have positive effects on the well-being of PWD, but there are few controlled studies that provide strong evidence supporting this statement. Even if the development of better-controlled studies in recent years is incontestable, deficiencies in reports of such clinical trials are still frequent, as outlined in several reviews.4,14–16 Limitations of these studies can be due to various biases (i.e., unspecified selection criteria, small sample size, lack of randomization and of a blinded assessor, group dissimilarity at baseline, no test-retest, no control group). The absence of a nonmusic or another intervention group to control for changes due to patients’ stimulation (and to the social impact of group activities) also limits the conclusion about the specific impact of a music intervention. Moreover, there is virtually no experimental research about the potential long-term effects of music-based activities in PWD and their caregivers (except for three recent studies17–19 ). Thus, there is an urgent need to go beyond intuitions and investigate the efficiency of music-based intervention in the treatment of PWD more rigorously with adequate experimental methodology. Well-designed and properly executed randomized controlled trials (RCTs) provide the best evidence for the efficacy of nonpharmacological treatments. As emphasized by a group of scientists and editors who developed the CONSORT (Consolidated Standards of Reporting Trials) statement to improve the quality of RCT reporting,20 “trials with inadequate or poor methodological approaches are associated with exaggerated treatment effects” (p. 663). In other words, findings contaminated by numerous uncontrolled factors are 250
Insight from RCTs in patients with advanced AD
Study 1 In the first study,17 14 PWD were recruited within a single center. All the participants met the diagnostic criteria for dementia of Alzheimer’s type or mixed dementia according to the DSM-IV.21 Only patients with moderate to severe stages of dementia were included. They were all native French speakers to ensure familiarity with the songs selected for music sessions. Patients were randomly assigned to each intervention group, and a person not directly involved in data collection performed the randomization. Patients engaged in either music or cooking activities twice a week (2 h each session) for 1 month, with the total duration of the intervention being 16 hours. Each intervention group included seven patients supervised by a therapist with the help of another person. During each intervention, receptive (listening to music or tasting recipes) and productive (clapping hands or singing with music or preparing a recipe) phases were alternated. Two different therapists were involved in this RCT, each supervising the music or cooking intervention. The one who supervised music intervention had
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
Samson et al.
Musical interventions in dementia
Table 1. List of items to control in RCTs investigating the efficiency of nonpharmacological treatments on PWD
Items to control in RCTs Clinical population Sample size Attrition bias Single- or multiple-center Eligibility criteria (cf. text) Study design (parallel or crossover) Intervention group (music) Control intervention group (cooking) Control group (usual care) Random group assignment Test-retest (no differences in baseline data) Time period of intervention Intensity (number of time per week) Dosage (duration of intervention) Duration of follow-up (from the beginning of intervention) Number of therapists
Therapists’ personal preference
Primary outcome measure Blind assessment (interviewer) Blind assessment (raters of video recording) Secondary outcome measures
Similarities between interventions (music vs. cooking) • Active versus passive activities • Attractiveness • Novelty between sessions
Study 1: Cl´ement et al. (2012)17
Study 2: Narme et al. (2014)19
PWD N = 14 21% Single-center Controlled Parallel group Yes Yes No Yes Yes
PWD N = 48 23% Single-center Controlled Parallel group Yes Yes No Yes Yes
No change Different No change No change No change No change No change No change No change No change No change
4 weeks 2 16 hours 8 weeks
4 weeks 2 8 hours 8 weeks
No change No change Different No change
2
1 (for both music and cooking)
Different
Cooking (for both interventions)
Different
Emotional state Yes Yes
No change Different No change
None
Cognitive status Functional status Behavioral status Caregivers’ distress
Different
No No No
Yes Yes No
Different Different No change
(1 for music and 1 for cooking) Music (for music intervention) No (for cooking intervention) Emotional state No Yes
a clear preference for music activities but no prior education in music therapy. Emotional state was determined by assessing discourse content, emotional facial expressions, and mood. These three outcome measures were performed six times with each patient with two
evaluations before the intervention (BL–1 , BL0 ) to obtain baseline measures and to control test–retest effect, two evaluations to test short-term effects of the intervention after the fourth (IMID ) and the last sessions (IEND ), and two follow-up measures to assess long-term effects after the end of the
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
251
Musical interventions in dementia
Samson et al.
intervention, 2 (POST+2 ) and 4 (POST+4 ) weeks postintervention. Discourse content and emotional facial expressions were assessed using short semistructured filmed interviews. During this interview a psychologist questioned each patient individually about his or her feelings at the present time. However, this person was not blind to the patient’s intervention group. Emotional facial expressions and discourse content were analyzed from the first two min of each filmed interview. Two independent and blinded observers rated audio and video recordings to count the number of positive and negative verbal and facial expressions (according to the Facial Action Coding System22 ). Mood was assessed with an adaptation of the State–Trait Anxiety Inventory for Adults (STAI-A).23 Unlike the standard procedure, a caregiver completed the questionnaire. Instead of using the global score, we separately summed the ratings of the 10 positive and 10 negative statements, consistent with how the facial expressions and discourse content were analyzed. From each measure (facial expression, discourse, mood), an emotional index was derived from the positive and the negative scores. A positive emotional index meant that the patient displayed more positive than negative emotions, and a negative emotional index meant the reverse. The change of emotional state was the primary outcome of interest. This change was measured by the difference in the emotional index for facial expressions, discourse content, and mood between baseline and posttreatment assessments. As depicted in Figure 1 (left panel), the mean emotional index improved for discourse content, facial expressions, and mood after the fourth (IMID ) and eighth (IEND ) music sessions, and this improvement persisted at 2 (POST+2 ) and 4 (POST+4 ) weeks after the end of the intervention for discourse content and mood. Based on this profile of results, we showed that music had short-term positive effects on all three emotional indices and long-term effects on two indices (discourse valence and mood). Conversely, there was no significant benefit of cooking interventions on emotional state, with the exception of a short-term effect on mood. The findings of this study suggest that music was more effective than cooking in improving the emotional state of PWD. As previously discussed,19,24 several methodological weaknesses might have biased the reported 252
results. The person who interviewed the patients was the therapist in charge of the music intervention. Because she was not blind to the patient’s group, the change in emotional state observed in the music group might have been due to bias, not only by the familiarity of the assessors but also by the implicit memory of enjoyable social interactions during music interventions. In addition, the small number of participants might have compromised the generalization of the data. Therefore, it is difficult to conclude if the benefit of music in this study is domain specific or if it is related to other confounding factors such as familiarity, arousal, attractiveness, and/or pleasantness. To overcome these pitfalls, we carried out a second study. Study 2 The general design of this second study19 was very similar to that of the previous one, except for a few differences that are outlined below and summarized in Table 1. In this study we increased the sample size and recruited 48 PWD in a single center (different from study 1), with a similar attrition rate to our previous study. We used the same three emotional indices to examine patients’ emotional state, but we also measured cognitive, functional, and behavioral functioning as well as caregiver distress. Owing to clinical constraints from the nursing home, we had to reduce the duration of each intervention session to 1 h, decreasing the total duration of interventions from 16 to 8 hours. To control the potential bias effect of specific therapist, a single person supervised both music and cooking interventions. We also improved the attractiveness of cooking sessions by adapting the activities to patients and balanced the proportion of active and passive activities in both interventions. Finally, an important difference concerned the psychologist in charge of the interview. External to the residential care home, this person was completely blind to the patient’s intervention group, which had not been the case in the previous study. Moreover, the psychologist who assessed cognitive abilities and functional behaviors and the caregivers who completed questionnaires were all blinded as well. Therefore, all the assessors (interviewer, psychologist, caregivers, and raters) were blinded from the patient’s group affiliation. The results of this “better-controlled” study, displayed in Figure 1 (right panel), showed that both music and cooking interventions resulted in
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
Samson et al.
A
Musical interventions in dementia
B
Figure 1. Mean emotional indices (%) of the two intervention groups (music and cooking) for discourse content, facial expressions, and mood across the six evaluations (bars represent the standard error of the mean, and lines with asterisks correspond to significant differences (P < 0.05) between a value and the baseline (BL0 )). (A) Left panel, study 1;17 (B) right panel, study 2.19
improved emotional state as indicated by facial expressions and mood indices. It is noteworthy that the magnitude of the short- and long-term positive effects of music on emotional indices reported in study 1 was reduced. Moreover, the music intervention in study 1 was significantly better than cooking in producing positive emotions in PWD, illustrating the so-called exaggerated treatment effect. As depicted in Figure 1, the beneficial effect of music in study 2 was no different from that of cooking. Taken together, these findings suggest that implicit associations between the pleasant activities and the therapist (without any episodic memory of music sessions) might have influenced the findings of study 1. This effect seems to result, at least in part, from interactions with a therapist rather than from the musical intervention per se, emphasizing the
importance of using blind assessors (interviewers and raters) in such studies. Although we found that the effect of the music intervention on patients’ emotional state was less marked after strict control of different factors, there were significant changes in several other measures during and after both types of interventions relative to baseline. Specifically, we found that music and cooking interventions also reduced the severity of behavioral disorders and consequently diminished professional caregiver distress. These additional results seem even more reliable because many methodological constraints have been taken into account in this second RCT. Overall, the novelty of study 2 was in its finding that enjoyable or pleasant activities other than music can also improve the well-being of PWD and their caregivers. To further
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
253
Musical interventions in dementia
Samson et al.
explore the impact of nonpharmacological approaches in dementia, it will be necessary to include another control group of participants who receive the usual care without any intervention. This additional constraint will help to ensure that positive changes did not result from familiarity with the assessor (interviewer) and cannot be attributed to group activities in general, a placebo effect, or natural variations of disease. Such a study is presently in progress in our laboratory. Conclusions and future prospects On the basis of the previously reported data, we can conclude that nonpharmacological interventions, such as music and cooking offered twice weekly over 1 month to PWD with severe cognitive decline, can improve emotional and behavioral functioning in patients and reduce caregiver distress. We found that music activities did not have greater therapeutic effects than other pleasant activities. This absence of difference between the benefits of music and cooking argues against music specificity in improving well-being in PWD. As highlighted in this report, trials assessing behavioral manipulations require additional constraints that are not always so crucial or relevant in pharmacological therapy studies. The major difficulty in such nonpharmacological trials is to preserve blinding at every stage of behavioral evaluation. Even if the therapist cannot be blinded, the healthcare professionals in charge of the participants and the people assessing the patients (outcome assessors) should be blinded. Contact among caregivers, assessors, and therapists should be avoided, thus limiting the risk for performance bias. In multicenter studies, other constraints requiring specific analysis are necessary to control care provider and center. To help clinicians and scientists to improve the quality of such studies, we proposed a list of items to take into account in designing nonphamacological RCTs (see Table 1). Such methodological rigor is in agreement with the CONSORT statement20 and is necessary to document the possible impact of nonpharmacological therapy on behavioral responses in RCTs. This will be essential to propose guidelines for the formulation of public heath policies. Well-designed prospective trials are therefore needed to establish the efficacy of music interventions under clinical circumstances and to generalize the recently published results.18,19 254
They will also be useful to clarify the precise mechanism by which nonpharmacological approaches, and music intervention in particular, induce positive emotional and behavioral changes in patients with severe dementia and their family or medical caregivers. In view of the increasing number of PWD and the limited resources of public health care, enjoyable group activities provide a viable and promising alternative to pharmacological treatments to improve the emotional status of PWD and to reduce caregiver distress. Nonpharmacological interventions such as music or cooking involving one or two caregivers with a group of six to eight patients are feasible activities, especially for patients in residential care, with a reasonable cost/benefit ratio.25 Acknowledgments The authors are grateful to Amee Baird for her helpful comments on previous versions of the manuscript, to the psychologists (A. Tonini, L. Sintes, A. Saenz, and S. Desdouits) who carried out the evaluations and the interventions with the assistance of L. Foulon and R. Goret. The authors are also grateful to the caregivers of the Valenciennes Hospital and Wilson Nursing Home who gave their time ensuring the study feasibility. These studies have received funding from the French Ministry (ANR-09-BLAN-0310-02), the private Fondation Plan Alzheimer, and the Institut Universitaire de France to S.S. Conflicts of interest The authors declare no conflicts of interest.
References 1. Luppa, M., T. Luck, E. Br¨ahler, et al. 2008. Prediction of institutionalisation in dementia. A systematic review. Dement. Geriatr. Cogn. Disord. 26: 65–78. 2. Black, W. & O.P. Almeida. 2004. A systematic review of the association between the behavioral and psychological symptoms of dementia and burden of care. Int. Psychogeriatr. 16: 295–315. 3. National Institute for Health and Care Excellence. 2006. NICE clinical guideline 42: dementia, supporting people with dementia and their carers in health and social care. Available at guidance.nice.org.uk/cg42. 4. Vink, A.C., M.S. Bruinsma & R.J.P.M. Scolten. 2011. Music therapy for people with dementia. Cochrane Database Syst. Rev. 3: CD003477.
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
Samson et al.
5. Baird, A. & S. Samson. 2009. Memory for music in Alzheimer’s disease: unforgettable? Neuropsychol. Rev. 19: 85–101. 6. Samson, S., D. Dellacherie & H. Platel. 2009. Emotional power of music in patients with memory disorders: clinical implications of cognitive neuroscience. Ann. N.Y. Acad. Sci. 1169: 245–255. 7. Takahashi, T. & H. Matsushita. 2006. Long-term effects of music therapy on elderly with moderate/severe dementia. J. Music Ther. 43: 317–333. 8. El Haj, M., L. Fasotti & P. Allain. 2012. The involuntary nature of music-evoked autobiographical memories in Alzheimer’s disease. Conscious Cogn. 21: 238–246. 9. Cuddy, L.L. & J. Duffin. 2005. Music, memory, and Alzheimer’s disease: is music recognition spared in dementia, and how can it be assessed? Med. Hypotheses 64: 229–235. 10. Fraisse, P., G. Ol´eron & J. Paillard. 1953. Dynamogenic effects of music; experimental study. Annee Psychol. 53: 1–34. 11. Blood, A.J. & R.J. Zatorre. 2001. Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc. Natl. Acad. Sci. USA 98: 11818–11823. 12. Salimpoor, V.N., M. Benovoy, K. Larcher, et al. 2011. Anatomically distinct dopamine release during anticipation and experience of peak emotion to music. Nat. Neurosci. 14: 257–262. 13. Khalfa, S., S.D. Bella, M. Roy, et al. 2003. Effects of relaxing music on salivary cortisol level after psychological stress. Ann. N.Y. Acad. Sci. 999: 374–376. 14. Raglio, A., G. Bellelli, P. Mazzola, et al. 2012. Music, music therapy and dementia: a review of literature and the recommandations of the Italian Psychogeriatric Association. Maturitas 72: 305–310. 15. Ueda, T., Y. Suzukamo, M. Sato, et al. 2013. Effects of music therapy on behavioral and psychological symptoms of
Musical interventions in dementia
16.
17.
18.
19.
20.
21.
22. 23.
24.
25.
dementia: a systematic review and meta-analysis. Ageing Res. Rev. 12: 628–641. McDermott, O., N. Crellin, H.M. Ridder, et al. 2012. Music therapy in dementia: a narrative synthesis systematic review. Int. J. Geriatr. Psychiatry 28: 781–794. Cl´ement, S., A. Tonini, F. Khatir, et al. 2012. Short and longer term effects of musical intervention in severe Alzheimer disease. Music Percept. 29: 533–541. S¨ark¨am¨o, T., M. Tervaniemi, S. Laitinen, et al. 2014. Cognitive, emotional and social benefits of regular musical activities in early dementia: randomized controlled study. Gerontologist 54: 634–650. Narme, P., S. Cl´ement, N. Ehrl´e, et al. 2014. Efficacy of musical interventions in dementia: evidence from a randomized controlled trial. J. Alzheimer’s Dis. 38: 359–369. Altman, D.G., K.F. Schulz, D. Moher, et al. 2001. The revised CONSORT statement for reporting randomized trials: explanation and elaboration. Ann. Intern. Med. 134: 663–694. American Psychiatric Association. 1994. Diagnostic and Statistical Manual of Mental Disorders, 4th Ed. (DSM-IV). Washington, DC: American Psychiatric Association. Ekman, P. & W.V. Friesen. 1978. Facial Action Coding System. Palo Alto, CA: Consulting Psychologist Press. Spielberger, C.D. 1983. Manual for the State–Trait Anxiety Inventory (STAI). Palo Alto, CA: Consulting Psychologist Press. Narme, P., A. Tonini, F. Khatir, et al. 2013. Nonpharmacological treatment for Alzheimer’s disease: comparison between musical and non-musical interventions. Geriatr. Psychol. Neuropsychiatr. Vieil. 10: 215–224. Bellelli, G., A. Raglio & M. Trabucchi. 2012. Music interventions against agitated behaviour in elderly persons with dementia: a cost-effective perspective. Int. J. Geriatr. Psychiatry 27: 327.
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
255
A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S Issue: The Neurosciences and Music V
Efficacy of musical interventions in dementia: methodological requirements of nonpharmacological trials 1 Severine Samson,1,2 Sylvain Clement, Pauline Narme,3 Loris Schiaratura,4 ´ ´ 1,5 and Nathalie Ehrle´ 1
Equipe Neuropsychologie: Audition, Cognition et Action (EA 4072), UFR de psychologie, Universite´ Lille-Nord de France, Hopital Pitie-Salp etri Paris, France. 3 Equipe Neuropsychologie du Villeneuve d’Ascq, France. 2 Unite´ d’epilepsie, ´ ˆ ´ ˆ ere, ` Vieillissement (EA 4468), Institut de Psychologie, Universite´ Paris Descartes, Paris, France. 4 Laboratoire de Psychologie: Interactions Temps Emotions Cognition (EA 4072), UFR de psychologie, Universite´ Lille-Nord de France, Villeneuve d’Ascq, Maison-Blanche, CMRR Champagne-Ardenne, France France. 5 Service de Neurologie, CHU de Reims, Hopital ˆ Address for correspondence: Severine Samson, Department of Psychology, University of Lille, BP 60 149, 59653 Villeneuve ´ d’Ascq Cedex, France. [email protected]
The management of patients with Alzheimer’s disease is a significant public health problem given the limited effectiveness of pharmacological therapies combined with iatrogenic effects of drug treatments in dementia. Consequently, the development of nondrug care, such as musical interventions, has become a necessity. The experimental rigor of studies in this area, however, is often lacking. It is therefore difficult to determine the impact of musical interventions on patients with dementia. As part of a series of studies, we carried out randomized controlled trials to compare the effectiveness of musical activities to other pleasant activities on various functions in patients with severe Alzheimer’s disease. The data obtained in these trials are discussed in light of the methodological constraints and requirements specific to these clinical studies. Although the results demonstrate the power of music on the emotional and behavioral status of patients, they also suggest that other pleasant activities (e.g., cooking) are also effective, leaving open the question about the specific benefits of music in patients with dementia. All these findings highlight the promising potential for nonpharmacological treatments to improve the well-being of patients living in residential care and to reduce caregiver burden. Keywords: Alzheimer’s disease; music; nonpharmacological treatment; randomized controlled trial; emotion
Music-based therapeutic strategies in persons with dementia The management of memory and behavioral disorders in patients with dementia (PWD) is currently unsatisfactory. Behavioral disorders are particularly difficult to control and represent a main cause of institutionalization1 and caregiver distress.2 In recent years, significant advances have been made in terms of understanding the pathophysiological mechanisms of neurodegenerative diseases, but current pharmacological treatments are essentially symptomatic and do not have a satisfactory impact on symptoms related to dementia progression. The limited effectiveness of these treatments and severe iatrogenesis associated with neuroleptics have led several health institutions to recommend the
development of nonpharmacological complementary interventions as first-line treatment.3,4 As a result, music activities are seeing a growing success with PWD as well as with caregivers. PWD are reactive to music until very advanced stages of the disease5–8 and can learn and recognize musical tunes even in the severe stage. In contrast with impaired verbal memory,6,9 music memory seems to be partially preserved in PWD.5 In addition, music easily elicits movements stimulating interactions between perception and action systems, as already underlined by Fraisse, Ol´eron, and Paillard.10 These effects may be underpinned by diminished control of inhibition in patients with severe Alzheimer’s disease (AD). Indeed, it is common to observe patients who spontaneously synchronize their movements with music, and this can
doi: 10.1111/nyas.12621 C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
249
Musical interventions in dementia
Samson et al.
subsequently facilitate social cohesion in a group setting. Finally, by inducing strong emotions,11,12 music can also help patients to relax by modulating psychological and physiological functions, especially those related to stress.13 As a consequence, the power of music and its nonverbal nature offer a privileged communication medium when language is diminished or abolished. Although the mechanisms underlying all these effects remain poorly understood, the intriguing sensitivity of PWD to music justifies its use for therapeutic purposes.
associated with biased estimates of treatment effects and with systematic errors. In this paper, we discuss this issue by reporting two successive studies to illustrate how methodological weaknesses might bias results by amplifying the effect of a music intervention and to warn clinicians and scientists about the hasty conclusions that can result from a lack of experimental rigor.
Assessing the efficacy of music-based interventions in PWD
In two previous studies,17,19 we performed RCTs to examine the short- and long-term effects of a music intervention (group-based musical activities) on emotional state and behavioral functioning of PWD. The main objective was to assess the efficacy of nonpharmacological treatments on the well-being of PWD. We were also interested in testing the possible superiority of music over nonmusic interventions. As a nonmusical activity, we selected cooking as it provides an ideal control intervention for music. Both activities are easily performed in a group setting, are multisensory, pleasurable, and can trigger old memories. The similarities and differences between these two studies are summarized in Table 1.
In the literature, numerous studies have claimed that music-based interventions have positive effects on the well-being of PWD, but there are few controlled studies that provide strong evidence supporting this statement. Even if the development of better-controlled studies in recent years is incontestable, deficiencies in reports of such clinical trials are still frequent, as outlined in several reviews.4,14–16 Limitations of these studies can be due to various biases (i.e., unspecified selection criteria, small sample size, lack of randomization and of a blinded assessor, group dissimilarity at baseline, no test-retest, no control group). The absence of a nonmusic or another intervention group to control for changes due to patients’ stimulation (and to the social impact of group activities) also limits the conclusion about the specific impact of a music intervention. Moreover, there is virtually no experimental research about the potential long-term effects of music-based activities in PWD and their caregivers (except for three recent studies17–19 ). Thus, there is an urgent need to go beyond intuitions and investigate the efficiency of music-based intervention in the treatment of PWD more rigorously with adequate experimental methodology. Well-designed and properly executed randomized controlled trials (RCTs) provide the best evidence for the efficacy of nonpharmacological treatments. As emphasized by a group of scientists and editors who developed the CONSORT (Consolidated Standards of Reporting Trials) statement to improve the quality of RCT reporting,20 “trials with inadequate or poor methodological approaches are associated with exaggerated treatment effects” (p. 663). In other words, findings contaminated by numerous uncontrolled factors are 250
Insight from RCTs in patients with advanced AD
Study 1 In the first study,17 14 PWD were recruited within a single center. All the participants met the diagnostic criteria for dementia of Alzheimer’s type or mixed dementia according to the DSM-IV.21 Only patients with moderate to severe stages of dementia were included. They were all native French speakers to ensure familiarity with the songs selected for music sessions. Patients were randomly assigned to each intervention group, and a person not directly involved in data collection performed the randomization. Patients engaged in either music or cooking activities twice a week (2 h each session) for 1 month, with the total duration of the intervention being 16 hours. Each intervention group included seven patients supervised by a therapist with the help of another person. During each intervention, receptive (listening to music or tasting recipes) and productive (clapping hands or singing with music or preparing a recipe) phases were alternated. Two different therapists were involved in this RCT, each supervising the music or cooking intervention. The one who supervised music intervention had
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
Samson et al.
Musical interventions in dementia
Table 1. List of items to control in RCTs investigating the efficiency of nonpharmacological treatments on PWD
Items to control in RCTs Clinical population Sample size Attrition bias Single- or multiple-center Eligibility criteria (cf. text) Study design (parallel or crossover) Intervention group (music) Control intervention group (cooking) Control group (usual care) Random group assignment Test-retest (no differences in baseline data) Time period of intervention Intensity (number of time per week) Dosage (duration of intervention) Duration of follow-up (from the beginning of intervention) Number of therapists
Therapists’ personal preference
Primary outcome measure Blind assessment (interviewer) Blind assessment (raters of video recording) Secondary outcome measures
Similarities between interventions (music vs. cooking) • Active versus passive activities • Attractiveness • Novelty between sessions
Study 1: Cl´ement et al. (2012)17
Study 2: Narme et al. (2014)19
PWD N = 14 21% Single-center Controlled Parallel group Yes Yes No Yes Yes
PWD N = 48 23% Single-center Controlled Parallel group Yes Yes No Yes Yes
No change Different No change No change No change No change No change No change No change No change No change
4 weeks 2 16 hours 8 weeks
4 weeks 2 8 hours 8 weeks
No change No change Different No change
2
1 (for both music and cooking)
Different
Cooking (for both interventions)
Different
Emotional state Yes Yes
No change Different No change
None
Cognitive status Functional status Behavioral status Caregivers’ distress
Different
No No No
Yes Yes No
Different Different No change
(1 for music and 1 for cooking) Music (for music intervention) No (for cooking intervention) Emotional state No Yes
a clear preference for music activities but no prior education in music therapy. Emotional state was determined by assessing discourse content, emotional facial expressions, and mood. These three outcome measures were performed six times with each patient with two
evaluations before the intervention (BL–1 , BL0 ) to obtain baseline measures and to control test–retest effect, two evaluations to test short-term effects of the intervention after the fourth (IMID ) and the last sessions (IEND ), and two follow-up measures to assess long-term effects after the end of the
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
251
Musical interventions in dementia
Samson et al.
intervention, 2 (POST+2 ) and 4 (POST+4 ) weeks postintervention. Discourse content and emotional facial expressions were assessed using short semistructured filmed interviews. During this interview a psychologist questioned each patient individually about his or her feelings at the present time. However, this person was not blind to the patient’s intervention group. Emotional facial expressions and discourse content were analyzed from the first two min of each filmed interview. Two independent and blinded observers rated audio and video recordings to count the number of positive and negative verbal and facial expressions (according to the Facial Action Coding System22 ). Mood was assessed with an adaptation of the State–Trait Anxiety Inventory for Adults (STAI-A).23 Unlike the standard procedure, a caregiver completed the questionnaire. Instead of using the global score, we separately summed the ratings of the 10 positive and 10 negative statements, consistent with how the facial expressions and discourse content were analyzed. From each measure (facial expression, discourse, mood), an emotional index was derived from the positive and the negative scores. A positive emotional index meant that the patient displayed more positive than negative emotions, and a negative emotional index meant the reverse. The change of emotional state was the primary outcome of interest. This change was measured by the difference in the emotional index for facial expressions, discourse content, and mood between baseline and posttreatment assessments. As depicted in Figure 1 (left panel), the mean emotional index improved for discourse content, facial expressions, and mood after the fourth (IMID ) and eighth (IEND ) music sessions, and this improvement persisted at 2 (POST+2 ) and 4 (POST+4 ) weeks after the end of the intervention for discourse content and mood. Based on this profile of results, we showed that music had short-term positive effects on all three emotional indices and long-term effects on two indices (discourse valence and mood). Conversely, there was no significant benefit of cooking interventions on emotional state, with the exception of a short-term effect on mood. The findings of this study suggest that music was more effective than cooking in improving the emotional state of PWD. As previously discussed,19,24 several methodological weaknesses might have biased the reported 252
results. The person who interviewed the patients was the therapist in charge of the music intervention. Because she was not blind to the patient’s group, the change in emotional state observed in the music group might have been due to bias, not only by the familiarity of the assessors but also by the implicit memory of enjoyable social interactions during music interventions. In addition, the small number of participants might have compromised the generalization of the data. Therefore, it is difficult to conclude if the benefit of music in this study is domain specific or if it is related to other confounding factors such as familiarity, arousal, attractiveness, and/or pleasantness. To overcome these pitfalls, we carried out a second study. Study 2 The general design of this second study19 was very similar to that of the previous one, except for a few differences that are outlined below and summarized in Table 1. In this study we increased the sample size and recruited 48 PWD in a single center (different from study 1), with a similar attrition rate to our previous study. We used the same three emotional indices to examine patients’ emotional state, but we also measured cognitive, functional, and behavioral functioning as well as caregiver distress. Owing to clinical constraints from the nursing home, we had to reduce the duration of each intervention session to 1 h, decreasing the total duration of interventions from 16 to 8 hours. To control the potential bias effect of specific therapist, a single person supervised both music and cooking interventions. We also improved the attractiveness of cooking sessions by adapting the activities to patients and balanced the proportion of active and passive activities in both interventions. Finally, an important difference concerned the psychologist in charge of the interview. External to the residential care home, this person was completely blind to the patient’s intervention group, which had not been the case in the previous study. Moreover, the psychologist who assessed cognitive abilities and functional behaviors and the caregivers who completed questionnaires were all blinded as well. Therefore, all the assessors (interviewer, psychologist, caregivers, and raters) were blinded from the patient’s group affiliation. The results of this “better-controlled” study, displayed in Figure 1 (right panel), showed that both music and cooking interventions resulted in
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
Samson et al.
A
Musical interventions in dementia
B
Figure 1. Mean emotional indices (%) of the two intervention groups (music and cooking) for discourse content, facial expressions, and mood across the six evaluations (bars represent the standard error of the mean, and lines with asterisks correspond to significant differences (P < 0.05) between a value and the baseline (BL0 )). (A) Left panel, study 1;17 (B) right panel, study 2.19
improved emotional state as indicated by facial expressions and mood indices. It is noteworthy that the magnitude of the short- and long-term positive effects of music on emotional indices reported in study 1 was reduced. Moreover, the music intervention in study 1 was significantly better than cooking in producing positive emotions in PWD, illustrating the so-called exaggerated treatment effect. As depicted in Figure 1, the beneficial effect of music in study 2 was no different from that of cooking. Taken together, these findings suggest that implicit associations between the pleasant activities and the therapist (without any episodic memory of music sessions) might have influenced the findings of study 1. This effect seems to result, at least in part, from interactions with a therapist rather than from the musical intervention per se, emphasizing the
importance of using blind assessors (interviewers and raters) in such studies. Although we found that the effect of the music intervention on patients’ emotional state was less marked after strict control of different factors, there were significant changes in several other measures during and after both types of interventions relative to baseline. Specifically, we found that music and cooking interventions also reduced the severity of behavioral disorders and consequently diminished professional caregiver distress. These additional results seem even more reliable because many methodological constraints have been taken into account in this second RCT. Overall, the novelty of study 2 was in its finding that enjoyable or pleasant activities other than music can also improve the well-being of PWD and their caregivers. To further
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
253
Musical interventions in dementia
Samson et al.
explore the impact of nonpharmacological approaches in dementia, it will be necessary to include another control group of participants who receive the usual care without any intervention. This additional constraint will help to ensure that positive changes did not result from familiarity with the assessor (interviewer) and cannot be attributed to group activities in general, a placebo effect, or natural variations of disease. Such a study is presently in progress in our laboratory. Conclusions and future prospects On the basis of the previously reported data, we can conclude that nonpharmacological interventions, such as music and cooking offered twice weekly over 1 month to PWD with severe cognitive decline, can improve emotional and behavioral functioning in patients and reduce caregiver distress. We found that music activities did not have greater therapeutic effects than other pleasant activities. This absence of difference between the benefits of music and cooking argues against music specificity in improving well-being in PWD. As highlighted in this report, trials assessing behavioral manipulations require additional constraints that are not always so crucial or relevant in pharmacological therapy studies. The major difficulty in such nonpharmacological trials is to preserve blinding at every stage of behavioral evaluation. Even if the therapist cannot be blinded, the healthcare professionals in charge of the participants and the people assessing the patients (outcome assessors) should be blinded. Contact among caregivers, assessors, and therapists should be avoided, thus limiting the risk for performance bias. In multicenter studies, other constraints requiring specific analysis are necessary to control care provider and center. To help clinicians and scientists to improve the quality of such studies, we proposed a list of items to take into account in designing nonphamacological RCTs (see Table 1). Such methodological rigor is in agreement with the CONSORT statement20 and is necessary to document the possible impact of nonpharmacological therapy on behavioral responses in RCTs. This will be essential to propose guidelines for the formulation of public heath policies. Well-designed prospective trials are therefore needed to establish the efficacy of music interventions under clinical circumstances and to generalize the recently published results.18,19 254
They will also be useful to clarify the precise mechanism by which nonpharmacological approaches, and music intervention in particular, induce positive emotional and behavioral changes in patients with severe dementia and their family or medical caregivers. In view of the increasing number of PWD and the limited resources of public health care, enjoyable group activities provide a viable and promising alternative to pharmacological treatments to improve the emotional status of PWD and to reduce caregiver distress. Nonpharmacological interventions such as music or cooking involving one or two caregivers with a group of six to eight patients are feasible activities, especially for patients in residential care, with a reasonable cost/benefit ratio.25 Acknowledgments The authors are grateful to Amee Baird for her helpful comments on previous versions of the manuscript, to the psychologists (A. Tonini, L. Sintes, A. Saenz, and S. Desdouits) who carried out the evaluations and the interventions with the assistance of L. Foulon and R. Goret. The authors are also grateful to the caregivers of the Valenciennes Hospital and Wilson Nursing Home who gave their time ensuring the study feasibility. These studies have received funding from the French Ministry (ANR-09-BLAN-0310-02), the private Fondation Plan Alzheimer, and the Institut Universitaire de France to S.S. Conflicts of interest The authors declare no conflicts of interest.
References 1. Luppa, M., T. Luck, E. Br¨ahler, et al. 2008. Prediction of institutionalisation in dementia. A systematic review. Dement. Geriatr. Cogn. Disord. 26: 65–78. 2. Black, W. & O.P. Almeida. 2004. A systematic review of the association between the behavioral and psychological symptoms of dementia and burden of care. Int. Psychogeriatr. 16: 295–315. 3. National Institute for Health and Care Excellence. 2006. NICE clinical guideline 42: dementia, supporting people with dementia and their carers in health and social care. Available at guidance.nice.org.uk/cg42. 4. Vink, A.C., M.S. Bruinsma & R.J.P.M. Scolten. 2011. Music therapy for people with dementia. Cochrane Database Syst. Rev. 3: CD003477.
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
Samson et al.
5. Baird, A. & S. Samson. 2009. Memory for music in Alzheimer’s disease: unforgettable? Neuropsychol. Rev. 19: 85–101. 6. Samson, S., D. Dellacherie & H. Platel. 2009. Emotional power of music in patients with memory disorders: clinical implications of cognitive neuroscience. Ann. N.Y. Acad. Sci. 1169: 245–255. 7. Takahashi, T. & H. Matsushita. 2006. Long-term effects of music therapy on elderly with moderate/severe dementia. J. Music Ther. 43: 317–333. 8. El Haj, M., L. Fasotti & P. Allain. 2012. The involuntary nature of music-evoked autobiographical memories in Alzheimer’s disease. Conscious Cogn. 21: 238–246. 9. Cuddy, L.L. & J. Duffin. 2005. Music, memory, and Alzheimer’s disease: is music recognition spared in dementia, and how can it be assessed? Med. Hypotheses 64: 229–235. 10. Fraisse, P., G. Ol´eron & J. Paillard. 1953. Dynamogenic effects of music; experimental study. Annee Psychol. 53: 1–34. 11. Blood, A.J. & R.J. Zatorre. 2001. Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc. Natl. Acad. Sci. USA 98: 11818–11823. 12. Salimpoor, V.N., M. Benovoy, K. Larcher, et al. 2011. Anatomically distinct dopamine release during anticipation and experience of peak emotion to music. Nat. Neurosci. 14: 257–262. 13. Khalfa, S., S.D. Bella, M. Roy, et al. 2003. Effects of relaxing music on salivary cortisol level after psychological stress. Ann. N.Y. Acad. Sci. 999: 374–376. 14. Raglio, A., G. Bellelli, P. Mazzola, et al. 2012. Music, music therapy and dementia: a review of literature and the recommandations of the Italian Psychogeriatric Association. Maturitas 72: 305–310. 15. Ueda, T., Y. Suzukamo, M. Sato, et al. 2013. Effects of music therapy on behavioral and psychological symptoms of
Musical interventions in dementia
16.
17.
18.
19.
20.
21.
22. 23.
24.
25.
dementia: a systematic review and meta-analysis. Ageing Res. Rev. 12: 628–641. McDermott, O., N. Crellin, H.M. Ridder, et al. 2012. Music therapy in dementia: a narrative synthesis systematic review. Int. J. Geriatr. Psychiatry 28: 781–794. Cl´ement, S., A. Tonini, F. Khatir, et al. 2012. Short and longer term effects of musical intervention in severe Alzheimer disease. Music Percept. 29: 533–541. S¨ark¨am¨o, T., M. Tervaniemi, S. Laitinen, et al. 2014. Cognitive, emotional and social benefits of regular musical activities in early dementia: randomized controlled study. Gerontologist 54: 634–650. Narme, P., S. Cl´ement, N. Ehrl´e, et al. 2014. Efficacy of musical interventions in dementia: evidence from a randomized controlled trial. J. Alzheimer’s Dis. 38: 359–369. Altman, D.G., K.F. Schulz, D. Moher, et al. 2001. The revised CONSORT statement for reporting randomized trials: explanation and elaboration. Ann. Intern. Med. 134: 663–694. American Psychiatric Association. 1994. Diagnostic and Statistical Manual of Mental Disorders, 4th Ed. (DSM-IV). Washington, DC: American Psychiatric Association. Ekman, P. & W.V. Friesen. 1978. Facial Action Coding System. Palo Alto, CA: Consulting Psychologist Press. Spielberger, C.D. 1983. Manual for the State–Trait Anxiety Inventory (STAI). Palo Alto, CA: Consulting Psychologist Press. Narme, P., A. Tonini, F. Khatir, et al. 2013. Nonpharmacological treatment for Alzheimer’s disease: comparison between musical and non-musical interventions. Geriatr. Psychol. Neuropsychiatr. Vieil. 10: 215–224. Bellelli, G., A. Raglio & M. Trabucchi. 2012. Music interventions against agitated behaviour in elderly persons with dementia: a cost-effective perspective. Int. J. Geriatr. Psychiatry 27: 327.
C 2014 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1337 (2015) 249–255
255
