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Annals of Neurodegenerative Disorders

Cite this article: Unglik J, Bungener C, Delgadillo D, Salachas F, Pradat PF, et al. (2016) Emotional Feeling, Coping Strategies and Apathy in Amyotrophic Lateral Sclerosis. Ann Neurodegener Dis 1(4): 1019.

*Corresponding authorJohanna Unglik, Laboratoire de Psychopathologie et Processus de Santé, Université Paris Descartes, 71 av. Edouard Vaillant, 92774 Boulogne-Billancourt Cedex, France, Email:

Submitted: 26 October 2016

Accepted: 01 December 2016

Published: 03 December 2016

Copyright© 2016 Unglik et al.

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Keywords•ALS patients•Emotion•Coping•Apathy•Anxious symptoms•Depressive symptoms

Research Article

Emotional Feeling, Coping Strategies and Apathy in Amyotrophic Lateral SclerosisJohanna Unglik1,2*, Catherine Bungener1, Daniel Delgadillo2, François Salachas2, Pierre François Pradat2,6, Gaëlle Bruneteau2,8, Timothée Lenglet3, Nadine Le Forestier2, Philippe Couratier4, Yannick Vacher5, and Lucette Lacomblez2,7 1Laboratoire de Psychopathologie et Processus de Santé – EA 4057, Sorbonne Paris Cité, Université Paris Descartes, Paris, France2Département de Neurologie, Centre référent SLA, AP-HP, Hôpital Pitié-Salpêtrière, F-75013, Paris, France3Département de Neurophysiologie Clinique, AP-HP, Hôpital Pitié-Salpêtrière, F-75013, Paris, France4Département de Neurologie, CHU, Hôpital Dupuytren, Limoges, France5Département de la Recherche Clinique et du Développement, AP-HP, Hôpital Saint-Louis, Paris, France 6CNRS, INSERM, Laboratoire d’Imagerie Biomédicale (LIB), Sorbonne universités, UPMC université Paris 06, F-75013, Paris, France7CNRS, INSERM, Laboratoire d’Imagerie Biomédicale (LIB), CIC_1422, Sorbonne universités, UPMC université Paris 06, F-75013, Paris, France8Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Université Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France

Abstract

The main objective of this research was to explore positive and negative emotions, coping strategies, apathy, anxious and depressive symptoms in patients suffering from ALS. Data were collected from 169 patients with an average age of 63 ± 11.6 years. The self-administered questionnaires HADS, EPN-31, CHIP and Marin’s apathy evaluation scale were answered by all patients. Half of the patients had depressive symptoms and 60% had anxious symptoms. The patients experienced on average more negative than positive emotions. They preferentially used emotional regulation followed by seeking of well-being. Emotional regulation and palliative coping were positively correlated with negative emotions, apathy, anxiety and depression, and appeared to be non-adaptive strategies to cope with the disease. Distraction coping and cognitive avoidance were negatively correlated with anxiety, depression and apathy, and positively with positive emotions. These strategies seem to be protective factors against anxious and depressive symptoms.

ABBREVIATIONSALS: Amyotrophic Lateral Sclerosis

INTRODUCTIONAmyotrophic lateral sclerosis (ALS) is a progressive

neurodegenerative disorder involving motor neurons of the cerebral cortex, brain stem and spinal cord. The loss of motor neurons quickly generates a progressive muscle paralysis usually leading to death from respiratory failure in 3-5 years. The cause of the disease is unknown and there is currently no effective treatment. The non-motor manifestations of ALS include cognitive and/or behavioural dysfunctions. Approximately 50% of patients have minor cognitive deficits and 5-13% of them meet criteria for frontotemporal dementia (FTD) [1]. The most predominant behavioural symptom from the beginning of the disease is apathy [2], which can manifest in different ways: behavioural, cognitive and/or emotional. In ALS, the specific

apathetic profile corresponds to a high loss of initiative and weak emotional blunting [3].

Psychopathological signs such as depressive and anxious symptoms are frequently observed, and are higher than in the general population [4,5]. However, the prevalence of major depressive episodes is almost identical to that in the general population [6]. Regarding anxiety, ALS patients experienced anxiety over both how to live and how to die [7] and this was correlated with disease progression [8]. During the diagnostic period, the state-anxiety scores (anxiety felt at the moment) were high and gradually decreased during the follow-up [9]. Kurt [10] summarised that anxious symptoms in patients may vary from 0% to 30% depending on the stage of the disease and the evaluation method. According to a literature review of different psychological fields in ALS, a more specific exploration of depressive features and a greater number of studies on anxiety, which is currently an understudied area, seem needed [11]. These results also raise

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the question of the patients’ adjustment abilities, leading to an interest in coping strategies. These are defined by Lazarus [12] as “the constantly changing cognitive and behavioural efforts to manage the specific external or internal demands that are appraised as taxing or exceeding the resources of the person”. The most used coping strategies in 33 newly-diagnosed patients were support (problem-management coping) and independence (emotion-management coping) [13]. There was a positive correlation between active coping strategies and lifespan [14]. These coping strategies strengthen the sense of control, leading the patients to adopt a “fighting spirit”. Some researchers [15] showed that ALS patients used significantly fewer active coping strategies, such as thinking about the situation or taking adequate measures, compared to cancer patients with a negative prognosis. However, Matuz and colleagues [16] suggested an association between problem-focused and emotion-focused strategies. First, searching for information and support can help patients to initiate actions that are necessary to lead to optimal care. On the other hand, using avoidance prevents focusing attention on negative information and consequences that may occur during the progression of the disease. Overall, emotion-focused strategies are positively correlated with depression and anxiety while avoidance is usually considered a maladaptive strategy because it prevents patients from taking appropriate measures about their own care. However, given the clinical specificity of ALS, cognitive avoidance could be considered an appropriate coping strategy by allowing patients not to think continually about their disease and its threatening consequences. A preliminary study in ALS [17] showed that patients whose diagnosis was less than six months ago used emotion-focused strategies more frequently and presented a greater emotional deficit with a lack of expressiveness.

Currently, there is a lack of studies regarding emotional functioning including both positive and negative emotions felt by ALS patients. Lulé et al. [18], emphasised that patients at an early stage of the disease tended to rate neutral, negative and positive emotional stimuli more positively than control subjects, and were less likely to respond when presented with negative stimuli. This may mean that ALS patients have difficulty in processing negative emotions.

Our main objective was to describe the links between the different psychological dimensions, such as positive and negative emotions, coping strategies, apathy, anxious and depressive symptoms, in ALS patients. Secondary objectives were to explore the possible influences of socio-demographic and clinical variables on the studied dimensions including comparing patients with and without depressive and anxious symptoms.

A better understanding of the coping strategies adopted by patients given their emotional experience while controlling apathy, anxious and depressive symptoms could enable them to be offered more targeted and efficient psychological care.

MATERIALS AND METHODS

Patients

ALS patients hospitalised in the day care unit in the ALS Centre of Salpêtrière (Paris) or Dupuytren (Limoges) Hospitals,

between October 2012 and January 2015, were invited to participate in the study. Patients diagnosed by a neurologist with FTD were excluded. Socio-demographic and medical data were collected from their medical records. This study was approved by the ethics committee of Salpêtrière Hospital and all included patients signed an informed written consent before completing the self-questionnaires.

Assessments

All participants received a booklet containing the following self-questionnaires: Hospital Anxiety and Depression Scale (HADS) [19], validated in French by Razavi et al. [20], which evaluates the severity of anxious and depressive symptoms during the last week but is not a diagnostic tool. This scale of 14 items gives a total score and a score for two subscales (depression and anxiety): the maximum level is 42 for the overall scale and 21 for each of the subscales. The thresholds for the two sub-scores are 0-7: lack of anxious and/or depressive symptoms; 8-10: mild anxious and/or depressive symptoms; 11-21: moderate to severe anxious and/or depressive symptoms. This scale has been widely used in neurological disorders because it contains no somatic symptoms.

Positive and Negative Emotionality scale (EPN-31), validated in French by Pelissolo et al. [21], on a psychiatric population, evaluates the basic emotions. It provides three main scores: positive emotions (10 items), negative emotions (18 items), and emotions of surprise (3 items). The instruction given to the individual was to estimate how often he or she felt each of the 31 emotions over a period of one month, using a scale with seven levels ranging from “never” to “several times a day”, rated from 1 to 7.

Coping with Health Injuries and Problems (CHIP) [22,23], assesses several coping strategies such as emotional regulation, seeking well-being/self-preservation, distraction coping, instrumental coping, palliative coping and cognitive avoidance. This instrument of 24 items uses a Likert scale from 1 (“not at all”) to 5 (“very much”).

Apathy Evaluation scale of Marin et al. [24], consists of 18 items rated from 1 (not at all characteristic) to 4 (very characteristic). The total score varied from 18 to 72 points (higher scores indicate more severe apathy). Raimo et al. [25], defined a cut-off of > 35.5 for this scale in patients with multiple sclerosis.

Statistical analysis

A descriptive analysis was conducted for each variable as well as non-parametric tests such as Spearman’s correlation and the Kolmogorov-Smirnov test. Correlations were made between the psychological variables and dimensions such as age, diagnosis duration, disease severity (ALS-FRS scores) and survival duration. The Kolmogorov-Smirnov test enabled comparisons according to gender, onset of the disease, presence or absence of anxious and depressive symptoms, receiving or not anxiolytic and antidepressant treatments. Statistical analyses were performed with Statistica and the significant level was set at p<.05. Because many correlations were carried out, the significance level was

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adjusted using Bonferroni correction (at p < .015).

RESULTS Socio-demographic and medical variables

Socio-demographic and medical characteristics are presented in Table (1). Regarding the socio-demographic variables, 169 participants (92 men (54.5%)) with an average age of 63 ± 11.6 years were included. The majority of patients were married or cohabiting with their partner (84,2%) and the education levels of patients were relatively heterogeneous.

With regard to the medical characteristics, the spinal form constituted 73,4% of our sample. The mean ALS-FRS score was 30.5 ± 9.35 points (range: 8-46) and the mean diagnosis duration was 26.3 ± 32 months (range: 0.5-210.6). Thirty patients (17.8%) had received their diagnosis within the last six months, forty (23.7%) between 7 and 12 months, forty-one patients (24.3%) between 13 and 24 months, and fifty-eight patients (34.3%) more than 24 months ago. At the time of analysis (March 2016), the mean survival duration was 46.2 ± 36.6 months (range: 6-236) with 99 (58.6%) deceased people. Almost all patients were treated with riluzole (96.4%), 24.2% were taking an antidepressant treatment and 12.4% an anxiolytic treatment of whom 7.7% were treated for depressive symptoms and 14.8% for anxious symptoms. In fact, these treatments had also been prescribed for other symptoms of the disease (pain, spasticity, impaired sleep or pseudo-bulbar symptoms).

Age was negatively correlated with distraction coping (r = -.19; p = .01) and cognitive avoidance (r = -.2, p = .008). Negative correlations were observed between ALS-FRS scores and variables such as negative emotions (r = -.25, p = .001), palliative coping (r = -.3, p = .00008), the HADS depression score (r = -.19, p = .01) and the apathy scores (r = -.18, p = .01). No correlations were found with diagnosis duration and survival time.

Psychopathological variables

Regarding the clinical variables (Table 2), negative emotions received higher scores than positive emotions. The most used coping strategies were emotional regulation followed by the seeking of well-being. The HAD scale indicated mild anxious (8.7 ± 4.1) and very mild depressive (7.8 ± 4.3) symptoms. However, 60% of patients presented a score of anxiety ≥ 8, and 51% of patients a score of depression ≥ 8. The apathy scale showed a mean score (36.3 ± 10.2) above the cut-off (> 35.5) defined by Raimo et al. [25].

The only significant difference concerned gender. Significantly lower scores were found in men for negative emotions (p < .025) and emotional regulation (p < .05) compared to women. No other significant differences were observed according to the onset of the disease, the presence or absence of anxious and depressive symptoms, and receiving or not anxiolytic or antidepressant treatments.

Comparisons between patients with scores < 8 and ≥ 8 for anxiety and/or depression (HADS) are presented in Table (3). Patients with anxiety and depression scores ≥ 8 had higher scores for negative emotions and emotional regulation strategy.

For patients with depression scores ≥ 8, significantly lower scores were found for positive emotions, cognitive avoidance and distraction coping whereas significantly higher scores were observed for palliative coping and for apathy.

The results highlighted a positive correlation between anxious and depressive symptoms scores, and between these dimensions and apathy scores. Significant associations were observed between coping strategies, psychopathological dimensions and emotions (Figure 1-3, Table 4).

Specifically, anxio-depressive symptoms and apathy were positively correlated with emotional regulation and negatively correlated with distraction coping. Depressive symptoms and apathy were also positively correlated with palliative coping and negatively with cognitive avoidance (Figure 1-2).

Figure 3 presents the positive correlations between negative emotions with anxious (r = .65; p < .0001) and depressive symptoms (r = .59; p < .0001), apathy (r = .27; p < .001), emotional regulation (r = .65; p < .0001) and palliative coping (r = .28; p < .001); and negative correlation with distraction coping (r = -.28; p < .001). In contrast, positive emotions were negatively correlated with anxious (r = -.22; p < .015) and depressive symptoms (r = -.38; p < .0001), apathy (r = -.28; p < .0001), emotional regulation (r = -.23; p < .015); and positively correlated with distraction coping (r = .34; p < .0001) and cognitive avoidance (r = .21; p <

Figure 1 Significant correlations (p < .015) between coping strategies and anxious and depressive symptoms.

Figure 2 Significant correlations (p < .015) between apathy, coping strategies and anxious and depressive symptoms.

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Table 2: Mean scores on clinical scales.Scales Dimensions Mean SD Range

EPN-31 (n = 153)Positive emotions 43.7 11.8 11 - 69Negative emotions 53.7 20.9 18 - 100

CHIP (n = 160)

Emotional regulation 24.3 5.6 9 - 35Seeking well-being 19.8 2.9 10 - 25Instrumental coping 8.7 4 3 - 15Distraction coping 8.1 2.9 2 - 15Palliative coping 8 2.6 2 - 14Cognitive avoidance 6.4 2.9 2 - 15

HADS (n = 161)

Anxiety Score < 8Score 8-10Score > 11

8.7 64 (39.7%) 41 (25.5%) 56 (34.8%)

4.1 0 - 20

Depression Score < 8Score 8-10Score > 11

7.879 (49.1%)42 (26.1%)40 (24.8%)

4.30 - 18

Marin scale (n = 162) Apathy 36.3 10.2 18 - 67

.015).

DISCUSSIONThe main objective of this research was to study several

aspects, such as positive and negative emotions, apathy, anxious and depressive symptoms, and coping strategies in ALS patients and possible links between them.

Regarding the propensity for emotional feeling, patients experienced on average more negative than positive emotions. Thus, the tendency of ALS patients to evaluate stimuli more positively [18] does not appear to be related to their emotional feelings. We have also observed that the severity of depressive and anxious symptoms appeared low on average, in accordance with some previous studies [17,26,27]. However, our study revealed that 51% of patients presented mild to severe depressive

symptoms and 60% mild to severe anxious symptoms. These data are significantly higher compared to the preliminary study [17] which highlighted a level of about 11% of patients with mild depressive or anxious symptoms. This disparity could be explained by the variability of the tools used; namely an external evaluation conducted during a clinical interview in the study of Bungener et al. [17], and a self-evaluation in our study.

We observed a negative correlation between positive emotions and dimensions as apathy, anxiety and depression while negative emotions highlighted the opposite pattern of associations. Given the existence of a positive link between negative emotions and apathy, we can hypothesise that emotions were very little blunted in accordance with the study of Radakovic et al. [3]. In fact, the apathetic patients can name and feel negative emotions.

Table 1: Socio-demographic and medical variables.

Socio-demographic and medical variables Patients

Mean age (SD; range) 63.3 (11.6; 30-87)

Gender (n = 169)Male 92 (54.5%)Female 77 (45.5%)

Marital status (n = 165)Single 5.4%Married/Cohabiting 84.2%Divorced/Separated/Widowed 16.4%

Education level (n = 159)< 12 years 38.4%12 years 21.4%> 12 years 40.2%

ALS onset (n = 169)Spinal form 73.4%Bulbar form 26.6%

ALS forms (n = 164)Sporadic 90.8%Familial 9.2%

Mean ALS-FRS score (SD; range) 30.5 (9.35; 8-46)

Mean diagnosis duration (months) 26.3 (32; 0.5-210.6)

Mean survival duration (months) 46.2 (36.6; 6-236)

Treatments (n = 169)Riluzole 96.4%Antidepressant 24.2%Anxiolytic 12.4%

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Table 3: Significant differences between patients with scores < 8 and ≥ 8 for anxiety and depression (HADS).

Scales DimensionsHADS-Anxiety Score ≥ 8(n = 97/60%)

HADS-Anxiety Score < 8(n = 64/40%)

P

EPN-31 Negative emotions 62.2 (18.2) 40.8 (16.3) p< .001

CHIP Emotional regulation 26.7 (4.5) 20.7 (5.1) p< .001

HADS-DepressionScore ≥ 8 (n = 82/51%)

HADS-Depression Score < 8(n = 79/49%)

P

EPN-31Positive emotions 40 (11.6) 47.6 (10.1) p< .005Negative emotions 64.8 (18.5) 42.1 (15) p< .001

CHIP

Cognitive avoidance 5.6 (2.3) 7.2 (3.1) p< .005

Palliative coping 8.7 (2.6) 7.2 (2.3) p< .005

Distraction coping 6.9 (2.6) 9.3 (2.6) p< .001

Emotional regulation 27.3 (4.3) 21.3 (5.1) p< .001Marin Apathy 41.1 (8.6) 31.9 (9.5) p< .001HADS Anxiety 10.8 (3.6) 6.5 (3.4) p< .001

Table 4: Correlations between the scores of all variables.

N = 169Emotionality Depression Anxiety Apathy

P N HADS-D HADS-A Marin

Coping strategies

ER -.23 * .65 *** .61*** .61*** .23*

SB .07 -.01 -.06 .06 -.1

DC .34*** -.28** -.50*** -.25** -.5***

IC -.05 -.03 -.04 .11 -.15

PC .13 .28** .31*** .15 .33***

CA .21* -.07 -.32*** -.01 -.34***

Depression HADS-D -.38*** .59*** / .57*** .6***

Anxiety HADS-A -.22* .65*** .57*** / .2*

Apathy Marin -.28*** .27** .6*** .2* /* p< .015; **p < .001; *** p < .0001Abbreviations: ER: Emotional Regulation; SB: Seeking Well-Being; DC: Distraction Coping; IC: Instrumental Coping; PC: Palliative Coping; CA: Cognitive Avoidance; P: Positive Emotions; N: Negative Emotions; HADS-D: Depression on HADS; HADS-A: Anxiety on HADS.

Various coping strategies were used but two of them, emotional regulation (attempts by the individual to regulate emotions associated with concern about this disease) and seeking well-being (efforts to get better) were the most used. These results may be consistent with previous studies [16,26] reporting the mixed use of emotion-focused and problem-focused strategies. Furthermore, the results revealed that the presence of anxiety or depression affects how the patient copes with illness and their subjective feeling of positive and negative emotions. Obviously, anxious and non-anxious patients differed significantly in their emotional feelings, particularly in their negative emotions and their use of an emotional regulation strategy. It appears important to notice that men tended to experience fewer negative emotions and use emotional regulation less intensely than women. Significant differences were also observed between depressed and non-depressed patients with the former experiencing positive emotions less frequently and negative emotions more often. They expressed more anxiety, more apathy and preferentially used emotional regulation and palliative coping strategies, unlike non-depressed patients who

used cognitive avoidance and distraction coping. The presence of psychopathological symptoms seems to impair the psychological functioning of patients and hence their adjustment process to illness. These symptoms may be related to the disease severity, which was positively correlated with depressive symptoms, apathy, negative emotions and palliative coping.

This research highlighted that some coping strategies were associated with emotional feeling, apathy and psychopathological symptoms such as anxiety and depression. In fact, emotional regulation and palliative coping (staying in bed and falling sleep) were positively correlated with negative emotions, apathy, anxiety and depression. On the contrary, distraction coping and cognitive avoidance in our patients were positively correlated with positive emotions and negatively with anxiety, depression and apathy. Although causality cannot be established, a tentative explanation is provided according to previous studies stating that coping strategies predicted anxiety and depression [28,29]. We can thus hypothesise that coping strategies such as emotional regulation and palliative coping are non-adaptive strategies to

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cope with the disease while distraction coping and cognitive avoidance seem to be protective factors against depressive and anxious symptomatology. Moreover, correlations showed that these latter coping strategies were used more by younger people. Therefore, these results emphasise that cognitive or behavioural avoidance seems to be more appropriate to cope with ALS, compared to problem-focused strategies.

The interpretation of these results must be taken cautiously given some limitations of this study. For example, the population is heterogeneous in its clinical form, length of evolution, stages of the disease and administration of treatments. Moreover, self-questionnaires were used only to reflect the patient’s point of view. Nevertheless, the large sample size provides an interesting description of the psychological aspects of ALS patients during their follow-up day care hospitalisation.

CONCLUSIONThese results highlight the importance of identifying the

presence of depressive and anxious symptoms as well as apathy given the links between these dimensions and the use of coping strategies that seem non-adaptive. These patients may be more likely to develop psychopathological disorders later during the evolution of the disease. It would therefore be interesting to assess these dimensions as soon as possible in order to adjust the patient’s care. Finally, it would be appropriate to explore longitudinally the psychopathological signs, emotional processing and coping strategies controlling cognitive functioning, and to take into consideration the partner in order to observe the reciprocity of these dimensions.

ACKNOWLEDGEMENTSThe authors thank the subjects whose participation made this

study possible. S. Lejeune, M. Veyrat-Masson, M. Nicol Penoty, M. Chouly and P. Bonnet provided technical assistance.

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Figure 3 Significant correlations (p < .015) between emotions and other variables.

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Unglik J, Bungener C, Delgadillo D, Salachas F, Pradat PF, et al. (2016) Emotional Feeling, Coping Strategies and Apathy in Amyotrophic Lateral Sclerosis. Ann Neurodegener Dis 1(4): 1019.

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