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Table of Contents    
ORIGINAL ARTICLE
Year : 2018  |  Volume : 66  |  Issue : 3  |  Page : 700-708

Sleep disorders in amyotrophic lateral sclerosis: A questionnaire-based study from India


1 Department of Neurophysiology; Department of Sleep Medicine, Sir Ganga Ram Hospital, Delhi, India
2 Department of Neurophysiology, Sir Ganga Ram Hospital, Delhi, India

Date of Web Publication15-May-2018

Correspondence Address:
Dr. Mandaville Gourie-Devi
Department of Neurophysiology, Sir Ganga Ram Hospital, New Delhi - 110 060
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.232327

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 » Abstract 


Background: Amyotrophic lateral sclerosis (ALS) is a relatively rare neurological disorder affecting upper and lower motor neurons in the brain and spinal cord with survival for 3-5 years and rarely beyond 10 years. Sleep disturbances in ALS are underreported and undertreated and there is no related data from India. This study aimed to assess the frequency of sleep disorders in patients of ALS and their determinants.
Methods: Patients with definite and probable ALS as per the El Escorial criteria were recruited from May 2014 to April 2016. Functional impairment, presence of sleep specific abnormalities and anxiety and depression were assessed using standardized questionnaires.
Results: Forty patients with ALS (23 male; 17 female) with their median age at presentation being 58.5 years (range 44-75 years) and the median duration of illness being 18 months (range: 4-120 months) were includedin the study. Half of the patients had poor sleep quality, which was significantly worse across all components of Pittsburgh Sleep Quality Index (PSQI) compared to controls. Sleep disorders were observed in 70%, insomnia in 65%, sleep disordered breathing/hypoventilation in 52.5% and restless legs syndrome in 5% patients. Night time awakenings attributable to symptoms associated with ALS were noted in 85%, and anxiety and depression in 57.5% patients. Excessive daytime somnolence emerged as an independent predictor for the presence of sleep disorders in ALS patients on multivariate logistic regression [P = 0.043, odd's ratio (OR) 1.435; 95% confidence interval[CI] (1.011-2.036)].
Conclusion: This is the first study from India providing insight into the presence of sleep disorders in ALS. About half of the patients of ALS had a poor sleep quality and two-thirds suffered from sleep disturbances.


Keywords: Amyotrophic lateral sclerosis, anxiety, cramps, depression, insomnia, obstructive sleep apnea, restless legs syndrome, sleep disorders
Key Messages:
This questionnaire-based study from India studying the sleep disorders prevalent in patients with amyotrophic lateral sclerosis. (ALS) showed that sleep disorders were frequent in ALS, predominantly insomnia and sleep disordered breathing disorders, and were significantly affected by poor functional scores as well as anxiety and depression. The study highlights the need for routine assessment of sleep and nocturnal complaints in ALS patients. Concerted efforts should be made towards developing devices to overcome the ALS-specific physical disabilities causing sleep fragmentation, as well as administering cognitive behavioural therapy for insomnia, anxiety and depression.


How to cite this article:
Panda S, Gourie-Devi M, Sharma A. Sleep disorders in amyotrophic lateral sclerosis: A questionnaire-based study from India. Neurol India 2018;66:700-8

How to cite this URL:
Panda S, Gourie-Devi M, Sharma A. Sleep disorders in amyotrophic lateral sclerosis: A questionnaire-based study from India. Neurol India [serial online] 2018 [cited 2018 Aug 20];66:700-8. Available from: http://www.neurologyindia.com/text.asp?2018/66/3/700/232327




Amyotrophic lateral sclerosis (ALS) is a progressive neurodegenerative disorder affecting the upper and lower motor neurons in the brain and spinal cord. It is uniformly distributed the world over with an annual incidence of 1/100,000 and a prevalence of 2 to 7/100,000 population.[1],[2] The diagnosis of ALS is based on clinical and electrophysiological criteria and is given different levels of diagnostic certainty as 'definite, probable, possible and suspected' by the El Escorial criteria [3] and the revised El Escorial criteria.[4] The average survival in the Caucasian populations ranges between 2 to 5 years;[5],[6] however, a study from India of 1153 patients of ALS has shown a median duration of survival of 114.8 ± 25.9 months.[7]

Sleep disorders in ALS are largely under-diagnosed and under-reported. Although sleep disturbances have been reported by patients with ALS, the frequency, severity and possible reasons have not been adequately addressed. Only recently, interest has emerged in sleep disorders as they affect the quality of life, which is already compromised in ALS.[8],[9] Till date, there is no data on sleep disorders in ALS from India. The objective of this study was to determine the spectrum of sleep disorders and the factors which may be associated with impaired sleep in patients with ALS. The data emerging from the study will be useful in improving the quality of life by appropriate interventional strategies.


 » Subjects and Methods Top


Design and setting

This was a prospective, questionnaire-based, observational study conducted at Sir Ganga Ram hospital, New Delhi from May 2014 to April 2016. The institutional ethics committee of Sir Ganga Ram hospital had approved the study (EC/09/14/728). A detailed history, clinical examination, nerve conduction study and electromyography were performed on suspected patients attending the neurology services, and those diagnosed to be suffering from ALS were included in the study. The patients and their care-givers were explained about the nature of the study. The inclusion criteria were: i) patients with definite and probable ALS as per the El Escorial criteria;[3],[4] ii) patients of either gender; and, iii) patients who gave informed consent to participate in the study. The exclusion criteria were: i) patients with possible ALS; ii) patients with severe bulbar weakness who were unable to communicate; iii) patients who had respiratory distress or were tracheostomized; and, iv) patients with significant co-existent chronic respiratory or cardiac disorders.

The functional impairment, sleep specific abnormalities (insomnia, excessive daytime sleepiness, restless legs syndrome and parasomnias) and presence of anxiety and depression were assessed using standardized questionnaires including the Amyotrophic Lateral Sclerosis Functional Rating Scale, Epworth Sleepiness Scale, Pittsburgh Sleep Quality Index, Disease Specific Questionnaire, Restless Legs Syndrome Rating Scale and Hospital Anxiety and Depression Scale. All the above scales have been extensively used in studies on Indian patients in whom they have been validated. After a detailed explanation, the respondents completed the questionnaires under supervision. Approximately 60-90 minutes were taken to complete the questionnaires. Polysomnography was not included as a part of the study but those found to have sleep disorders were advised to undergo further evaluation.

Measures used

  1. Amyotrophic Lateral Sclerosis-Functional Rating Scale


  2. The Amyotrophic Lateral Sclerosis Functional Rating Scale (ALSFRS) is an instrument for evaluating the functional status of patients with ALS.[10] ALSFRS includes ten parameters to assess bulbar and motor functions. The minimum score is '0' and maximum score is '40' (bulbar score = 16; motor score = 24) with lower scores indicating severe disability.

  3. Epworth Sleepiness Scale


  4. Epworth Sleepiness Scale (ESS) is a common questionnaire for assessment of excessive daytime sleepiness.[11] It comprises of 8 questions to which response is obtained on a scale from 0 (not at all likely to fall asleep) to 3 (very likely to fall asleep). The maximum total score is 24. An ESS score of 10 and more is suggestive of significant daytime sleepiness and those patients with a score over 15 have severe daytime sleepiness.

  5. Pittsburgh Sleep Quality Index


  6. The Pittsburgh Sleep Quality Index (PSQI) is a self-rating questionnaire evaluating sleep quality over the previous one month.[12] Nineteen items generate seven component scores: a) subjective sleep quality, b) sleep latency, c) sleep duration, d) habitual sleep efficiency, e) sleep disturbances, f) use of sleeping medication, and g) daytime dysfunction. The sum of these seven component scores yields one global score. Each component score has a value of '0' (no difficulty) to '3' (severe difficulty) and the global score ranges from '0' to '21'. A PSQI score >5 is considered as abnormal and is used for categorizing subjects as 'poor sleepers'.

  7. Disease Specific Questionnaire


  8. A questionnaire [13] incorporating Case Western Health Reserve and the Sleep Disorders Questionnaires [14],[15] and translated to Hindi language had been developed to evaluate Indian patients. In the present study, this questionnaire was modified for evaluating patients with ALS (Appendix). There are 53 questions divided into 3 sections: Section 1 ( 36 questions)- sleep disorders including obstructive sleep apnea, narcolepsy, insomnia, restless legs syndrome and parasomnia; Section 2 ( 7 questions)- ALS specific symptoms that disrupt sleep in patients, namely muscle cramps, difficulty in turning sides, pain in limbs/head/neck/back, breathlessness while lying in bed, sudden coughing/choking leading to awakening, nocturia and heartburn during sleep; and, Section 3 ( 10 questions)- associated medical illnesses and past history.

  9. Restless Legs Syndrome Rating Scale


  10. The Restless Legs Syndrome Rating Scale was developed as a tool for assessing the severity of restless legs syndrome (RLS).[16] It is a 10-item questionnaire using Likert-like ratings to indicate how acutely the disorder affected these patients in the previous one week. The questions are divided in two categories- symptoms (nature, intensity and frequency) and their impact (sleep, mood and disturbances in daily functioning). The questions are rated on a scale from 0 to 4, with 4 representing the most severe and 0 the least manifestations. The total score ranges from 0 to 40.

  11. Hospital Anxiety and Depression Scale


  12. The Hospital Anxiety and Depression Scale (HADS) is a brief (14-item), self-reported measure of anxiety and depression.[17] Scores of 8-10 are classified as mild, 11-15 moderate, and 16 and above as severe anxiety and depression.


Data entry was verified at periodic intervals by cross checking all the completed questionnaires to ensure accuracy. Data of age- and gender-matched historical controls from the previous study of one of the authors (SP) were included for comparison.[18]

Statistical analysis

Statistical analysis was done using statistical package for the social sciences (SPSS) version 17.0. Median (± SD) was calculated for continuous variables. The determinants of sleep disorders in ALS were assessed. The data was also compared with age- and gender-matched controls. Chi square test was applied for calculating statistical significance between the groups. Mann-Whitney t-test was used for comparison with controls. The predictors of poor sleep quality and sleep disorders in patients with ALS were assessed by dividing the study subjects into two groups, with and without these attributes. The groups were then compared by univariate and multivariate logistic regression analysis. A P value of ≤0.05 was considered statistically significant.


 » Results Top


A total of 40 patients with ALS were interviewed prospectively. The median age of the subjects at presentation was 58.5 years (range: 44-75) with majority (75%) being more than 50 years. The median age at onset of ALS was 56.25 years (range: 42-74.5). There were 23 (57.5%) male and 17 (42.5%) female patients. The median duration of illness was 18 months (range: 4 -120). In the control group, there were 190 age and gender matched subjects.

Bulbar onset of illness was noted in 12 patients, with onset in upper limbs in 21 and in lower limbs in 7 patients. However, at the time of recruitment for the study, 28 out of 40 patients (70%) had diffuse involvement, 11 had limb involvement alone (27.5%), and only one patient had isolated bulbar involvement. Bulbar onset of ALS was noted to be significantly higher in female patients (P = 0.001) and with the age of onset >50 years (P = 0.038). The functional impairment was mild (ALS-FRS >30) in 20, moderate (ALS-FRS 21 to 30) in 14, and severe (ALS-FRS ≤20) in 6 patients. The median score of bulbar function was 14 (range: 9-16) while that for the motor function was 15 (range: 2-24).

The average sleep latency of patients with ALS was 29.5 ± 26.3 minutes (range: 5-120), which was more than that of control subjects [23.3 ± 15.8 minutes (range: 5-90)].[18] The average duration of actual sleep was 6.5 ± 1.5 hours (range: 2-9) compared to 7.1 ± 0.8 hours (range: 5-8.9) in controls. Excessive daytime sleepiness was noted only in 5 (12.5%) patients. The overall sleep quality was poor (global PSQI score >5) in 50% of patients. All seven components of PSQI and global PSQI were significantly worse in patients with ALS compared to controls [Table 1].
Table 1: Markers of sleep quality on PSQI in amyotrophic lateral sclerosis patients

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Sleep disorders were observed in 28 out of 40 (70%) of ALS patients [Figure 1]; insomnia in 26 (65%), sleep disordered breathing in 21 (52.5%) and RLS in 2 (5%) patients. However, narcolepsy and parasomnia were not observed. In the majority of patients, insomnia was secondary (20/26; 76.9%) and only 6 patients had primary insomnia. Amongst the 26 patients reporting insomnia, 16 (61.5%) had difficulty in initiating sleep, 23 (88.5%) in maintaining sleep, and 10 (38.5%) had early morning awakening. Snoring accounted for sleep fragmentation in 18 (45%) patients. Interestingly, sleep disruption attributable to symptoms associated with ALS was noted in 34 (85%) patients, which included muscle cramps in 17 (42.5%), difficulty in turning sides in bed in 16 (40%), pain at different sites of the body in 9 (22.5%), breathlessness on lying down in bed in 11 (27.5%), choking/coughing in sleep in 2 (5%), nocturia in 25 (62.5%) and heartburn in 13 (32.5%) patients, alone or in combination [Figure 2].
Figure 1: Frequency of sleep disorders in amyotrophic lateral sclerosis patients

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Figure 2: Symptoms other than known sleep causing sleep fragmentation disorders in patients with amyotrophic lateral sclerosis

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The functional impairment, as assessed by ALS-FRS, had a significant correlation with sleep quality and disorders. The ALS-FRS score ≤30 (P = 0.007), particularly the motor score ≤16 (P = 0.046), was associated with greater frequency of insomnia compared to those with higher total and motor scores [Table 2]. On the contrary, the bulbar score did not significantly affect sleep. Symptoms attributable to ALS, including “muscle cramps, difficulty in turning sides, pain in limbs/head/neck/back, breathlessness while lying in bed, sudden coughing/choking leading to awakening, nocturia and heartburn during sleep,” were significantly more common in patients with a low ALS-FRS score (P = 0.006).
Table 2: Associations of insomnia in patients with amyotrophic lateral sclerosis

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Twenty-three of 40 (57.5%) patients had anxiety and depression on HADS; 8 had moderate (HADS 16-42) and 12 had severe anxiety and depression (HADS >42). These symptoms were commonly observed with younger age at onset (<50 years) [P = 0.025] and a longer duration of ALS (>24 months) [P = 0.041] ([Table 3]). Amongst the 26 patients with insomnia, anxiety and depression were noted in 18 (69.2%; P= 0.041) [Severe- 10; moderate-6; mild-2] patients [Table 3]. There was a significant association of anxiety and depression with a lower ALS-FRS ≤30 (85%, P= 0.002) and motor score ≤16 (70.8%, P= 0.037).
Table 3: Correlation of anxiety-depression with other variables

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On univariate analysis, poor sleepers were significantly associated with daytime somnolence (P < 0.001), presence of sleep disorders (<0.001), insomnia (P = 0.002), obstructive sleep apnea (P = 0.02), difficulty in sleep initiation (0.027), difficulty in sleep maintenance (P = 0.014), night-time awakenings (P = 0.02), nocturnal heartburn (P = 0.041) and, anxiety and depression (P = 0.01) [Table 4]. There was no significant correlation between the age of onset, gender, bulbar onset of symptoms or duration of illness with sleep quality. After multivariate analysis, only excessive daytime somnolence emerged as an independent predictor of poor sleep quality [P = 0.004, OR 1.507; 95% CI (1.138-1.997)].
Table 4: Comparison of amyotrophic lateral sclerosis patients with good and poor sleep quality

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In summary, the significant features of ALS patients having sleep disorders were the ALS-FRS score ≤30 (P = 0.014), daytime somnolence (P = 0.024), night time awakening (P = 0.006), poor sleep quality reflected by global PSQI (P < 0.001), and anxiety and depression (P = 0.013) [Table 5]. The ALS-FRS ≤30, daytime somnolence as well as anxiety and depression qualified for multivariate logistic regression; however the only significant predictor for presence of sleep disorders in ALS patients was daytime somnolence [P = 0.043, OR 1.435; 95% CI (1.011-2.036)].
Table 5: Characteristics of amyotrophic lateral sclerosis patients with and without sleep disorders

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 » Discussion Top


Sleep disorders in patients with ALS have received scant attention. A few studies suggest that sleep related complaints such as insomnia, frequent nocturnal awakenings, nightmares and daytime sleepiness do occur.[8] Most of these complaints have been chiefly attributed to nocturnal hypoventilation.[8],[19] In a recent study by Lo Coco et al.,[20] 59% of patients with ALS reported sleep disturbances and a third rated them as moderate or severe. A high frequency of RLS in patients with ALS has also been noted in a few studies.[21],[22] There are no published reports from India regarding the prevalence of sleep disorders in ALS and this is the first study describing the abnormalities during sleep in patients with ALS assessed through interview based questionnaires. The important observations are the presence of a high frequency of sleep disorders (70%) with poor sleep quality in half of the patients. Insomnia was the commonest sleep disorder (65%), followed by sleep disordered breathing (52.5%). Similar to the observations of Lo Coco et al.,[20] the presence of disease related symptoms contributing to sleep fragmentation and night time awakening was a significant finding (seen in 85% patients with sleep disorders).

Majority of patients with insomnia had difficulty in sleep initiation (61.5%) and maintenance (88.5%). The average sleep latency was prolonged with a shorter sleep duration and poor sleep efficiency compared to historical Indian controls,[10] similar to the observations reported by Hetta et al., in 24 patients with ALS.[8] Lo Coco et al.,[20] also found poor quality of sleep with the mean global PSQI score of 7.0 ± 3.74 in a study of 91 patients. Likewise, we also found that the sleep quality in our ALS patients significantly deteriorated across all components of PSQI compared to age- and gender-matched controls. The sleep quality was significantly associated with the presence of sleep disorders, insomnia, OSA, daytime somnolence, night time awakenings, difficulty in sleep initiation and maintenance, heartburn, and anxiety and depression in our study. Only excessive daytime somnolence was a significant predictor of sleep quality, similar to the findings in the study by Lo Coco et al.[20]

Secondary insomnia (76.9%) was the predominant subtype in our study. Insomnia may be linked to the emotional trauma of being aware of the diagnosis of ALS and the presence of anxiety and depression. Apart from anxiety, depression, snoring and nocturia, a novel finding was the contribution of certain symptoms in ALS such as cramps (42.5%), difficulty in turning sides (40%) and pain in parts of the body (22.5%) to sleep fragmentation. This is similar to a report by Lo Coco et al., wherein frequent night time complaints such as nocturia (62.5%), nocturnal cramps (45%), difficulty in turning in bed (38.5%) and snoring (36.3%) were observed.[9] Pain, a neglected symptom of ALS, resulting from musculoskeletal pain syndromes, muscular contractures, spasticity and immobility,[23] also contributed to night time awakening in our study. Nocturnal heartburn, seen in 32.5% in our patients, affected sleep quality adversely and has not been previously reported. These factors responsible for sleep fragmentation were also observed to be more frequent than oberved in healthy controls from North India [snoring (29%), pain (1.8%), difficulty in changing position (0%), nocturia (36.5%)].[24]

Sleep disordered breathing does contribute to sleep disturbances in ALS, as observed in 8 out of 18 patients with bulbar ALS assessed by polysomnography by Ferguson KA et al.[25] This may occur early in patients with bulbar onset ALS, or in the latter stages of limb onset ALS.[26],[27] However, in our study, the frequency of sleep disordered breathing (52.5%) was found to be lower than insomnia (65%). Most (45%) of the patients had snoring and 22.5% had orthopnea or features suggesting obstructive sleep apnea. It is well known that the exact frequency of nocturnal hypoventilation and sleep disordered breathing may not be accurately gauged by a questionnaire alone and polysomnography may demonstrate the true dimensions of the problem. This is important as assisted non-invasive ventilation can reverse the deleterious consequences of sleep-disordered breathing on sleep architecture and help in reducing sleep-related complaints in a proportion of patients with ALS.[28],[29],[30],[31]

Limousin et al., observed RLS in the 18.8% of ALS patients, a figure which is much higher than 2-3% reported in the general population.[22] RLS was surprisingly less frequent in our study (5%), though marginally higher than that observed in North Indian (1%)[24] and South Indian controls (2.9%).[18] The wide variation between the frequency of RLS in these studies may perhaps be due to the ALS patients misinterpreting their sensory symptoms such as cramps and pain in body parts as the positive sensory phenomena of RLS.

Nearly half of our study subjects had moderate-to-severe anxiety and depression. The frequency was higher compared with 27.5% in the study by Lo Coco et al.[9] The psychological distress caused by the physical symptoms and prognosis of ALS may contribute to the high frequency of anxiety and depression, as demonstrated by their significant association with ALS-FRS (P = 0.002) and its motor subscore (P = 0.037). Anxiety and depression also led to sleep fragmentation causing insomnia (P = 0.041) and poor sleep quality (P = 0.01).

The study brings to fore the importance of assessing for daytime sleepiness, which emerged as the only independent predictor of sleep quality as well as the presence of sleep disorders. This was similar to the findings of Lo Coco et al.,[20] who found patients' disability and daytime somnolence as significant predictors of poor sleep quality. Daytime sleepiness is generally considered a reflection of the night-time sleep disturbances, including delayed sleep onset, sleep fragmentation due to whatever cause, or early morning awakening. OSA was not the sole reason of daytime sleepiness. No patient had daytime sleepiness amounting to a reversal of circadian rhythm. The same fact was brought out by the results of the study. In addition, physical disability was found to be significant only on univariate but not on multivariate analysis. On the other hand, though the presence of anxiety and depression did not emerge as a significant predictor due to the small sample size, there was a trend [P = 0.068, OR 6.06; 95% CI (0.878-41.831)] that indicated the importance of these factors.

The present study highlights the need for routine assessment of sleep and nocturnal complaints in ALS patients. Concerted efforts should be made towards developing devices to overcome the ALS-specific physical disabilities causing sleep fragmentation as well as introducing cognitive behavioural therapy for insomnia, anxiety and depression.

The limitation of our study is that it is an observational, questionnaire-based study involving a small sample of patients with ALS without polysomnography. Polysomnographic evaluation would be the gold standard to provide more details about the sleep architectural characteristics as well as the true prevalence of sleep disorders. However, this is a preliminary study assessing the frequency of sleep disorders in ALS patients. Polysomnography was not a part of the protocol and would be done as a separate study keeping in mind the information gathered from the present study.


 » Conclusion Top


Increased awareness is warranted regarding the high prevalence of sleep disorders in ALS patients. Apart from sleep disordered breathing, insomnia more commonly contributes to poor sleep quality in ALS. ALS-specific physical symptoms, such as cramps and difficulty in turning in bed as well as nocturnal heartburn, severity of ALS (especially motor disability) and presence of anxiety-depression, significantly cause sleep fragmentation and consequently insomnia. Overall, the presence of daytime somnolence is the only predictor of poor sleep quality and presence of sleep disorders in ALS patients.

[Additional file 1]

Acknowledgement

The authors are grateful for the help of Ms. Parul Chugh, biostatistician, Sir Ganga Ram hospital.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.





 
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    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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