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Journal of Alzheimer’s Disease xx (20xx) x–xx DOI 10.3233/JAD-170990 IOS Press
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Isabelle Roucha,b,c,∗ , Elodie Pongana,b,c , Yohana Levequed , Barbara Tillmannd , B´eatrice Tromberte , Jean Claude Geteneta , Nicolas Augustef , Pierre Krolak-Salmonb,c,g , the LACM´e group1 , Bernard Laurenta,h and Jean-Michel Doreyg,i
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Personality Modulates the Efficacy of Art Intervention on Chronic Pain in a Population of Patients with Alzheimer’s Disease
a Memory Clinical and Research Center of Saint Etienne (CMRR) Neurology Unit, University Hospital of Saint Etienne, Saint Etienne, France b Memory Clinical and Research Center of Lyon (CMRR), Hospital of Charpennes, University Hospital of Lyon, France c Institute of Aging I-Vie, University Hospital of Lyon, France d INSERM, U1028, CNRS, UMR5292, University Lyon 1, Lyon Neuroscience Research Center, Psychoacoustic and Auditory Cognition team, Lyon, France e Public Health and Medical Information Unit, University Hospital of Saint-Etienne, Saint Etienne, France f Memory Clinical and Research Center of Saint Etienne (CMRR) Geriatrics Unit, University Hospital of Saint Etienne, Saint Etienne, France g Brain Dynamics and Cognition, Lyon Neuroscience Research Center, INSERM U1028, CNRS UMR 5292, Lyon, France h INSERM, U1028, CNRS, UMR5292, Neuropain team, Lyon Neuroscience Research Center, Lyon, France i Department of Psychiatry, Hospital Le Vinatier, Bron, France
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Accepted 14 February 2018
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Abstract. Background: Alzheimer’s disease (AD) mainly occurs in elderly individuals. Comorbidities and chronic pain are frequent in this population. Previous studies revealed that personality modulates both chronic pain (CP) and AD occurrence and evolution. Moreover, as pain treatments can induce side-effects, non-drugs treatments, such as art interventions, are interesting alternative therapies for decreasing CP in these patients. Objective: Our aim was to assess the potential role of personality traits on art intervention efficacy for reducing CP in a population of patients with mild AD. Methods: Design: multicenter randomized controlled trial. Fifty mild AD patients underwent a 12-week art intervention including singing and painting groups. Personality was assessed with the Big Five Inventory before the sessions. CP was measured with Numeric Rating Scale (NRS) [Usual pain (NRS-U) and most Intense pain (NRS-I)], Simple Visual Scale [Usual pain (SVS-U) and most Intense pain (SVS-I)] and Brief Pain Inventory (BPI) before and after the sessions. The influence of personality traits on CP evolution before and after art intervention was assessed with multiple linear regression models.
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1 LACM´ e Group: Nicolas Auguste, Romain Bachelet, Laurence Brunon, Jenny Dayot, Jean-Michel Dorey, Hanane El Haouari, Marion Fatisson, Marion Ferrer, Charlotte Gaillat, Claire Gentil, Jean Claude Getenet, Karine Goldet, Pierre Krolak-Salmon, Bernard Laurent, Marie Leroyer, Yohana Leveque, Agn`es Michon, Ang´elique Mortreux, Malou Navez, Anca Neagu, Catherine Perrot, Elodie Pongan, Isabelle Rouch,
Mathilde Solimeo, Barbara Tillmann, Ana¨ıs Touzet du Vigier, Elodie Vulliez. ∗ Correspondence to: Isabelle Rouch, Memory Clinical and Research Center of Saint Etienne (CMRR), Neurology Unit, Hospital of Saint Etienne, Avenue Albert Raimond, 42055 Saint Etienne, France. Tel.: +33 4 77 12 73 98; Fax +33 4 77 12 72 79; E-mail:
[email protected].
ISSN 1387-2877/18/$35.00 © 2018 – IOS Press and the authors. All rights reserved
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Keywords: Alzheimer’s disease, music, pain, personality
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INTRODUCTION
PATIENTS AND METHODS
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Alzheimer’s disease (AD), mainly occurring after 75 years [1, 2], is often associated with multiple comorbidities that can induce chronic pain (CP) [3]. In this frail population, analgesic drugs can induce serious side effects, such as increasing the risk of confusion, cognitive decline or falls, thus limiting their prescriptions. It has been suggested that non-pharmacological therapies could be a useful alternative pain relief care strategy in these patients. Among them, art therapy, including music intervention (MI), is often used for adult patients with CP [4–9] or in the elderly suffering from pain [5, 6]. In patients suffering from AD, MI improves cognitive and behavioral disorders [7–11]. In the LACM´e study, we investigated for the first time the efficacy of music and painting intervention on CP in patients with prodromal or mild AD, using a Randomized Controlled Trial (RCT). Our results revealed a reduction of CP after both 3-month music and painting interventions [12]. While there is strong evidence suggesting that some personality profiles could influence pain experiencing, little is known concerning the potential modulation effects of personality profiles on non-pharmacological interventions. The most widely accepted personality theory is the five factors model that consists of five personality dimensions: neuroticism, extraversion, openness to experience, agreeableness, and conscientiousness [13]. Neuroticism is considered to be the strongest predictor of vulnerability to stress and common mental disorders. It has been shown that high levels of neuroticism are also associated with CP development and maintenance [14–19]. Given these different elements, we wonder if prior personality can influence the effect of a therapeutic intervention on CP. The present analysis aimed at assessing the potential effect of personality, assessed with the Five Factors model, on music or painting intervention efficacy for reducing CP in the LACM´e population.
Study design
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The present analysis was based on data from LACM´e study, a multicenter Randomized Controlled Trial with two parallel arms and a blinded endpoint evaluation. The LACM´e study aimed as assessing the efficacy of music or painting interventions on chronic pain, anxiety, depression, quality of life, self-esteem and cognition on 59 patients with prodromal or mild AD. The study was approved by Saint Etienne University ethics committee. This trial was registered at clinicaltrials.gov (Identifier: NCT02670993). The LACM´e design is presented in more detailed in a previous paper [12].
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Results: A positive association was observed between neuroticism and the evolution of three CP measures including NRS-U (B = 0.34, p = 0.01), SVS-U (B = 0.20, p = 0.04), and BPI-U (B = 0.46, p = 0.02) evolution. No significant relationship was observed between neuroticism and NRS-I, SVS-I and BPI-R evolution. Conclusion: Our findings suggest that neuroticism can decrease the efficacy of group art intervention on pain in patients with mild AD. Individual therapies could be more appropriate for these patients. These results emphasize the interest of taking into account patients’ personality before proposing them to participate to a group therapy.
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Participants Participants were recruited from 3 memory clinics located in University Hospitals from Saint Etienne (neurology and geriatrics units) and Lyon (geriatrics unit), France. Inclusion criteria All participants recruited for the study met the following inclusion criteria: 60 years and older, probable AD, according to Diagnostic and Statistical Manual of Mental Disorders-V [20, 21] and National Institute of Neurological and Communicative Disorders and Stroke/Alzheimer’s Disease and Related Disorders Association (NINCDS/ADRDA) criteria [22]. The severity of cognitive disorders was assessed with Mini-Mental State Examination (MMSE), and only participants with a MMSE superior or equal to 20 were included. The included patients also presented chronic pain, assessed with the Simple Visual Scale (SVS) [23], at moderate or severe stage, and were able to complete the clinical evaluations.
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Measures Baseline evaluations were made after obtaining participants inform consent (T1). The patients underwent an extensive assessment including AD diagnosis and stage, personality, CP assessment, demographic and lifestyle factor assessments. Concerning followup measures, CP was evaluated at 12- week follow-up (T2).
Covariates Socio-demographic and lifestyle variable comprising age, gender, educational level, anxiety and depressive symptoms were collected at baseline and used in the present analysis as covariates. Anxiety was measured with STAI and depressive symptoms with GDS scale [12].
Intervention conditions
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The patients participated in 12 weekly two-hour SI or PI sessions during 3 months. The SI was delivered by a professional choir conductor accompanied by a psychologist. A concert gathering the patient choir and a choir of young singers was organized after the SI sessions. The PI was done by a painting teacher accompanied by a psychologist. An exhibition was organized after the PI sessions in the presence of patients’ families and care teams.
Statistical analyses
In the results of our previous LACM´e article [12], both MI and PI provided significant CP decrease after intervention, however, no efficacy difference was observed between the two groups. The SI and PI groups data were therefore analyzed together in the present analyses. For all participants, a descriptive analysis was performed on all study variables using tendency and dispersion measures for quantitative variables and relative and absolute frequencies for qualitative variables. The evolutions of each CP scale before (T1) and after (T2) the art interventions were calculated as follows: (T2 CP scale – T1 CP scale)/T1 CP scale. Pearson’s correlations were computed between each of the personality domains and the evolution of each CP measures. For personality domains significantly correlated to CP evolution, multiple linear regressions were then performed to assess the influence of personality on CP evolution by taking into account age, sex, educational level and art intervention group. As personality, i.e. neurotic trait has been shown to be linked to anxiety and depressive symptoms, the analyses were then performed taking into account anxiety and depression. All statistical tests were two-tailed, and p-values inferior to 0.05 considered as significant. Statistical analyses were performed with SPSS version 17 (SPSS Software, Chicago, USA).
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Primary outcome measures Personality was assessed with the Big Five Inventory (BFI) [24], validated in French and comprising 45 items. Each item contains a sentence describing an aspect of personality related to one of the five major dimensions: extraversion, openness, agreeability, consciousness and neuroticism. The item can reflect either the positive pole or the negative pole of the dimension. The patient is asked to answer on a 5point Likert scale if he/she disagrees (1) or approves (5) the proposal. An inverse score is obtained for the negative items. The BFI provides a score for each of the 5 personality dimensions. Chronic pain was assessed with three different measures, including the Numeric Rating Scale (NRS) [25], the Simple Visual Scale (SVS) [23] and the Brief Pain Inventory (BPI) [26]. In the NRS, the participant selects a number from 0 to 10 that best indicates usual pain level for the past week (with 0 indicating no pain, and 10 the most severe pain one can imagine) (NRS-U). The most intense pain perceived during the 8 last days is then evaluated according to a “worst pain” score on a 0to-10 scale, varying from 0 (no pain) to 10 (the most severe pain one can imagine) (NRS-I). For the SVS, patients are asked to use a categorical scale varying from 0 to 4, with 0 indicating no pain, and 4 indicating very intense pain. As for the NRS, patients are asked to assess successively usual pain from the 8 last days (SVS-U) and the most intense pain from the 8 last days (SVS-I). These scales were validated in populations of patients with mild cognitive disorders [27]. The BPI measures the intensity of pain (sensory dimension, 3 items) (BPI-I) and interference of pain in the patient’s life (reactive dimension, 10 items) (BPI-R), each measure corresponded to a numerical rating scale from 0–10. The sensory dimension assessed usual and worst pain in the 8 last days, and the reactive dimension explored pain repercussions in daily life [26].
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Table 1 Patients’ characteristics (n = 50) Gender Women Men Education (y) 11 Group SI PI Age MMSE Personality domains Neuroticism Conscientiousness Openness Agreeability Extraversion Chronic pain measures NRS-U NRS-I SVS-U SVS-I BPI –I BPI-R
Baseline N
%
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64 36
7 13 12 7 11
14 26 24 14 22
24 26
48 52
Mean
SE
Mean
SE
79.82 24.62
6.65 2.61
– –
– –
2.83 3.68 3.07 4.38 3.15
0.93 5.86 0.60 0.47 0.74
– – – – –
– – – – –
3.30 5.04 1.68 2.10 8.76 16.3
2.42 3.19 0.93 1.14 7.09 15.3
2.98 4.18 1.34 1.86 8.22 12.63
The correlations between personality domains and the evolution of CP scales were presented in Table 2. Neuroticism was positively correlated to the evolution of CP measures across art interventions, including NRS-U (r = 0.39, p = 0.01), SVS-U (r = 0.31, p = 0.04) and BPI-U (r = 0.36, p = 0.02) evolutions. A trend to a negative correlation was observed between conscientiousness and NRS-U (r = –0.31, p = 0.05), BPI-U (r = –0.29, p = 0.07) evolutions. There were no significant correlations between agreeability, extraversion or openness and the different CP evolution measures. The association between neuroticism and CP evolution was then assessed with multivariate linear regression analysis adjusted on age, sex, educational level and art intervention group. The results were provided on Table 3. An association was observed between higher neuroticism and lower decrease of NRS-U (B = 0.34, p = 0.01), SVS-U (B = 0.20, p = 0.04) and BPI-U (B = 0.46, p = 0.02) evolution. No significant relationship was observed between neuroticism and NRS-I, SVS-I and BPI-R evolution. To take into account the potential role of anxiety and depression on pain measures evolution, the significant analyses were then adjusted on GDS and STAI. The associations between higher neuroticism and lower decrease remained significant for NRS-U (B = 0.39, p = 0.01), SVS-U (B = 0.31, p = 0.04) and BPI-I (B = 0.35, p = 0.02) evolution.
T2 follow-up
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DISCUSSION
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A total of 50 patients completed the baseline and the T2 evaluations and provided the data for the present analyses. Table 1 shows the baseline demographic and personality, characteristics of the population, and baseline and T2 CP measures. A decrease in each CP measure was observed between baseline and T2. A decrease rate of 9.7% was observed for NRS-U, 17% for NRS-I, 20.2% for SVS-U, 11.4% for SVS-I, 6.1% for BPI-I and 22.5% for BPI-R.
2.65 3.01 0.96 1.23 7.93 15.91
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RESULTS
[-8pt] CP scales evolution
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Neuroticism r(1) p
NRS-U NRS-I SVS-U SVS-I BPI-R BPI-I
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0.39 0.15 0.31 0.06 0.16 0.36
(1) Pearson’s
correlation.
0.01 0.34 0.04 0.71 0.31 0.02
r
Conscientiousness p
In a previous study, we have demonstrated that art interventions represented by music therapy and painting could lead to CP reduction in patients with AD [12]. The present study aimed to assess whether personality traits may influence the efficiency of these art interventions in this patient population. The results revealed that a high neuroticism level was significantly linked to a weaker improvement of CP,
–0.31 –0.18 –0.17 –0.19 –0.12 –0.28
0.05 0.24 0.25 0.22 0.45 0.07
r
Openness p
–0.27 –0.08 –0.01 –0.06 0.03 –0.11
0.09 –0.11 0.93 0.69 0.84 0.47
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Table 2 Correlations between personality dimensions and CP evolution
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Agreeability p
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Extraversion r p –0.11 –0.03 0.02 0.04 0.11 –0.07
0.50 0.85 0.89 0.81 0.49 0.64
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NRS-U NRS-I SVS-U SVS-I BPI-R BPI-I
B(1)
SE(2)
Neuroticism 95% CI(3) p
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0.14 0.12 0.08 0.04 0.18 0.19
0.06; 0.62 –0.05; 0.42 0.04; 0.37 –0.06; 0.01 –0.10; 0.63 0.07; 0.83
Adjusted R2
0.02 0.12 0.02 0.52 0.16 0.02
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(1) Regression
coefficient; (2) standard error; (3) Confidence interval for regression coefficient. Multiple linear regressions adjusted on age, sex, educational level, and SI or PI group. 3b B(1)
SE(2)
NRS-U 0.39 NRS-I –0.35 SVS-U 0.31 SVS-I –0.38 BPI-R 0.26 BPI-I 0.46
0.13 0.21 0.08 0.04 0.18 0.19
Neuroticism 95% CI(3) p 0.08; 0.61 –0.92; –0.08 0.01; 0.32 –0.06; 0.01 –0.10; 0.63 0.07; 0.83
Adjusted R2
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0.13 0.10 0.07 0.14 0.03 0.20
(1) Regression
coefficient; (2) standard error; (3) Confidence interval for regression coefficient. Multiple linear regressions adjusted on age, sex, educational level, GDS and STAI scores and SI or PI group.
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Links between neuroticism and treatment outcome in psychiatric conditions and CP sufferers
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Individuals with a high level of neuroticism are more likely to exhibit psychological distress, emotional dysregulation, hostility, and impulsivity [28]. It is now well established that there is a strong correlation between neuroticism and psychiatric illness, such as depression, anxiety or personality disorder [29, 30]. In psychiatric populations, it has been suggested that higher levels of neuroticism could interfere with the efficacy and compliance of treatments [31]. For instance, in a population of patients with major depression, high neuroticism scores have been shown to be associated with poor pharmacotherapy and psychotherapy outcome [32]. The negative effects of neuroticism on the therapeutics’ efficiency, whether pharmacological or not, has been explained by the lack of adequate coping strategies [33].
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independently from current anxiety and depressive symptoms. Higher conscientiousness seemed to be associated with better CP’s improvement; however, the correlation just failed to reach significance, possibly due to a lack of statistical power.
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High level of neuroticism is also known to favor the occurrence of numerous physical diseases and to impede their evolution [34]. CP is a typical example of the interaction between personality and expression of a physical disease. In a recent review, Naylor et al. questioned the individualization of a pain personality characterized by high neuroticism, harm avoidance and lower self-directedness, contributing to enclose the sufferers into a vicious circle of fear, avoidance and physical suffering [14]. Other authors reported that individuals with higher neuroticism complain of more widespread pain and tend to elicit more catastrophic thoughts about CP [35, 36]. Personality traits including neuroticism, anxiety sensitivity and experiential avoidance were identified as risk factors for increased probability of disability in patients with CP [37]. Only a few previous studies measured the influence of personality on CP treatment efficacy, reporting controversial results. A study conducted by Kempke et al. on 53 patients who followed a pain education program found that self-critical perfectionism was significantly associated with negative CP treatment outcome [38]. Conversely, Torres et al. showed in a population of patients with fibromyalgia that individuals with higher neuroticism and lower extraversion have reached a wider pain improvement after a 6-month multidisciplinary treatment. However, patients with higher neuroticism remained in a worse affective state than patient with lower neuroticism, suggested that depression have to be taken into account when examining the effect of personality pain experiencing [39].
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Table 3 Relationships between neuroticism and each CP evolution – multivariate linear regressions
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Clinical implications for painful AD patients The number of publications investigating the link between personality and dementia has been growing recently. Neuroticism is now considered as a plausible risk factor for dementia onset, which may alter the natural course of the disease [40, 41]. A high level of neuroticism has also been correlated with accelerated cognitive decline, and challenging behaviors [42, 43]. Up to now, the impact of the personality in the response to treatments in neurocognitive disorders has been rarely taken into account, in particular for non-pharmacological interventions. To avoid iatrogenic side-effects of psychotropic drugs, nonpharmacological interventions are recommended as the first line treatment of behavioral disturbances, but their efficiency is still debated [44]. In the light of these discrepancy results, the impact of personality profile should be considered when evaluating non
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Limitations
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interventions to the individual’s expectations, their needs and personality profile [45, 48, 50]. It could be useful to adapt specific strategic care in patients scoring high in neuroticism. Kolanowski et al. [48] suggested to shorten duration of group activities. Sometimes individual care should be preferred to group care, notably in patients with high levels of anxiety. These individual managements could be better tailored after personality assessment.
One might argue that our study has several limitations. First, our study included patients with a relatively high level of positive personality traits and relatively low pain scores as well as patients with different etiologies of CP. In the future, it would be interesting to include patients with AD, more homogeneous pain etiology and with a higher level of pain. Secondly, because of a relatively weak number of subjects, our study might underestimate the link between personality traits and CP evolution and we thus cannot exclude the contribution of other traits. Third, the present study did not include a control group, i.e. a third group without specific intervention. Given a significant placebo effect, particularly in patients with a neurotic trait, the presence of a control group would have made it possible to differentiate the natural course of chronic pain according to neuroticism level from the effect of the level of neuroticism on the efficacy of treatment by itself. Finally, it could have been interesting to measure personality before and after art intervention, to evaluate the potential modification of personality traits with intervention. However, personality is supposed to be stable over a 4-month period. In conclusion, the present findings showed that neuroticism can decrease the efficacy of group art intervention on pain in patients with mild AD. These results emphasize the interest of taking into account the patients’ personality before proposing them to participate to a group therapy. Further research is needed to confirm these results and to identify the interest of individual versus group therapies according to personality traits.
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pharmacological intervention in dementia [45]. Similar to psychotropic medications, analgesics drugs should be used carefully in the presence of cognitive decline, and there is thus a need to develop alternative care. In a previous paper [12], we previously demonstrated that art therapy is effective in the management of painful symptoms in AD. While the influence of neuroticism on CP treatment has been assessed in a few studies with non-demented painful population, no study has investigated this question in AD patients with CP. This is even more surprising as self-efficacy, pain coping strategies, readiness to change and pain acceptance which favor pain decrease [46] are obviously impaired in this population. Our results are in line with our expectations, showing that neuroticism should be considered as a treatment resistance factor, as it has been described in psychiatric or physical illness conditions. Several explanations can be discussed. High neuroticism is characterized by dysfunctional coping strategies; these may alter the patients’ implication in the art activities and decrease the relational abilities of the individuals within the group of patients. Cognitive decline combined with high neuroticism may worsen to a greater extent inappropriate coping preexisting before the dementia onset. In addition, emotional distress and stress sensibility that often lead to a lack of motivation, concomitant depression, or ruminations, may disrupt the engagement of individuals with higher neuroticism. Moreover, AD can aggravate anxiety in patients with high neuroticism that have a significant risk of self-devaluation in the contact with others. Deficits in attention processes have also been suggested in healthy population scoring high in neuroticism [47]. In a study evaluating the engagement of patients with dementia in recreational activities, Kolanowski et al. [48] suggested that attention deficits associated with neuroticism may contribute to enhanced disengagement conducts. Although univariate analysis showed a negative association between neuroticism and engagement, there was no more significant association in multivariate analyses [48]. Overall, the differential efficiency of art therapy according to the personality shown in our study highlighted the necessity to adapt non pharmacological therapy to individuals’ profile. A systematic evaluation of personality could help the clinician to choose the most appropriate intervention for the patients. According to Yamagushi et al. [49], the efficiency of non-pharmacological intervention is dependent of the patients, families, and therapists involved. Kolanoski stresses the need to tailor non-pharmacological
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ACKNOWLEDGMENTS This study was supported by APICIL Foundation, France Alzheimer Association and Brou De Lauri`ere Foundation.
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The authors kindly thank Anna Maria Dascalita, Florence Fabre, Marie Claire Riocreux, for their help for the study patients’ recruitment and management. Authors’ disclosures available online (https:// www.j-alz.com/manuscript-disclosures/17-0990r2).
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