Rheumatol Int (2013) 33:285–290 DOI 10.1007/s00296-012-2376-6
ORIGINAL ARTICLE
Sleep disturbance in Moroccan patients with ankylosing spondylitis: Prevalence and relationships with disease-specific variables, psychological status and quality of life Jinane Hakkou • Samira Rostom • Mariam Mengat • Nawal Aissaoui • Rachid Bahiri • Najia Hajjaj-Hassouni
Received: 18 September 2011 / Accepted: 11 March 2012 / Published online: 24 March 2012 Ó Springer-Verlag 2012
Abstract Sleep disturbance is often reported by the patients with ankylosing spondylitis (AS), with awakenings produced by inflammatory pain. There are limited studies about sleep disturbance on these patients, and especially its association with psychological state and quality of life to examine the prevalence of sleep disturbance and to assess its association with disease-specific variables, psychological status and quality of life. One hundred and ten patients were included in this cross-sectional study according to the modified New York criteria for AS. Clinical and biological parameters were evaluated. Sleep disturbance was assessed by the fourth item of Hamilton Anxiety Scale. Psychological status was assessed by The Hospital Anxiety and Depression Scale including depression subscale and anxiety subscale. The quality of life was evaluated by the short form-36 (SF-36). Sleep disturbance was found in 64.5 %, depression in 55.5 % and anxiety in 60.9 % amongst our patients. Significantly, worse pain, higher disease activity and functional disability were present in patients with sleep disturbance. Likewise, sleep problems were significantly higher in patients with depression, anxiety and in patients with low scores of the SF36. Multivariate logistic regression analysis revealed that the pain (OR = 1.019) and depression (OR = 1.304) were independent risk factors that influenced sleep disturbance. Sleep problems are prevalent amongst Moroccan patients with AS. Our findings J. Hakkou (&) S. Rostom M. Mengat N. Aissaoui R. Bahiri N. Hajjaj-Hassouni Department of Rheumatology, El Ayachi University Hospital, Sale, Morocco e-mail:
[email protected] J. Hakkou S. Rostom M. Mengat N. Aissaoui R. Bahiri N. Hajjaj-Hassouni University Mohammed V-Souissi, Rabat, Morocco
suggest that pain and depression were the independent risk factors that influenced the sleep disturbance and hence, the need for evaluation and optimal management of pain and depression to improve sleep quality in AS patients. Keywords Sleep disturbance Ankylosing spondylitis Quality of life Depression Anxiety
Introduction Ankylosing spondylitis (AS) is a chronic inflammatory disease that causes significant pain. It characteristically affects the sacroiliac joints and spine. Key features include enthesitis, fibrosis and bony ankylosis [1]. Genetic susceptibility determined predominantly by the HLA B27 allele, however, new insights have been provided by the recent identification of susceptibility genes other than HLA-B27 [2]. Sleep problems are common in rheumatological disorders such as rheumatoid arthritis, systemic sclerosis and fibromyalgia [3–5]. Sleep disturbance is often reported by the patients with AS (86–91 %), with awakenings produced by inflammatory pain [6, 7]. Furthermore, recent evidence has pointed out a possible role for the cytokines in the regulation of sleep [8–10], which provides further reason for exploring sleep patterns in patients with inflammatory systemic disorders. There are limited studies about sleep disturbance on patients with AS and especially its association with psychological state and quality of life. Indeed, several studies have shown that psychological disorders frequently coexist with AS [11] and a study states that health-related quality of life in Moroccan patients with AS is damaged in a significant way. Mental as well as physical aspects were affected [12].
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This study was designed to assess the following in Moroccan patients with AS: (a) the prevalence of sleep disturbance (b) and its association with disease-specific variables (disease activity and functional status), psychological status (depression and anxiety) and quality of life.
Subjects and methods Subjects Hundred and ten patients consecutive with a higher age to 18 and who fulfilled the modified New York classification criteria for AS [13] had differing levels of symptomatic activities and were willing to participate in the study were included in this study conducted at El Ayachi Hospital. The patients who had other diseases that may cause sleep disturbance, such as fibromyalgia, malignancy and other chronic diseases, were excluded from the study. We have the ethics committee consent on this matter. Data collection and measurements Demographic characteristics were documented for each patient. The disease activity was evaluated by the Bath Ankylosing Spondylitis Disease Activity Index (BASDAI) [14]; it is a patient reported measure of AS disease activity. This index uses six 10-cm horizontal visual analogue scale (VAS) to assess the severity of fatigue, spinal and peripheral joint pain, localized tenderness and morning stiffness in patients with AS. The final BASDAI score has a range of 0–10; a lesser number represents less severe disease activity. Moroccan version of this scale has been assessed for its validity and reliability [15]. The Bath Ankylosing Spondylitis Functional Index (BASFI) [16] was used to assess function. This scale is based on 10 questions about daily functioning, each scored on a 10-cm visual analogue scale (VAS), reflecting status over the past month. The mean of the 10 scales generates the score with ‘10’ denoting worst possible functional status. Moroccan version of this scale has been assessed for its validity and reliability [15]. Sleep disturbance Sleep disturbance was assessed by the fourth item of Hamilton Anxiety Scale [17], and scored according to: 0: not present, 1: mild, 2: moderate, 3: severe, 4: very severe and by the number of nocturnal awakenings. The Hamilton Anxiety Scale is a rating scale developed to quantify the severity of anxiety symptomatology [17]. It consists of 14 items, each defined by a series of symptoms. Each item is rated on a 5-point scale, ranging from 0 (not present) to 4 (severe).
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Patients were dichotomized into a group with insomnia if the fourth item of Hamilton Anxiety Scale was equal to at least 1, and into a group without insomnia in other cases. Depression measurements The Hospital Anxiety and Depression Scale (HADS) was used in patients with AS to assess depression and anxiety. This scale was developed by Zigmond and Snaith [18], and Arabic version of this scale has been assessed for its validity and reliability [19]. The HADS is a 14-item scale designed to detect anxiety and depression, independent of somatic symptoms. It consists of two 7 item subscales measuring depression and anxiety. A 4-point response scale (from 0 representing absence of symptoms, to 3 representing maximum symptomatology) is used, with possible scores for each subscale ranging from 0 to 21. Higher scores indicate higher levels of disorder. A number of clinical classification schemes have been used to categorize scores on the HADS. In the original article, the following cut-offs were suggested: 0–7 = ‘non-cases’; 8–10 = ‘possible case’; 11–21 = ‘probable case’. This scale is used to scan anxiety and depression in a short time to diagnose the level of risk in physically ill patients. We used HADS-D C 8 to define the depressed subgroup and HADS-A C 8 to define the anxious subgroup [20, 21]. Measure of the quality of life Generic health status was measured using the short form (SF)-36 questionnaire [22], which measures eight multiitem dimensions: physical functioning (10 items), role limitations due to physical problems (four items), role limitations due to emotional problems (three items), social functioning (two items), mental health (five items), energy/ vitality (four items), pain (two items) and general health perception (five items). For each dimension item, scores are coded, summed and transformed on a scale from 0 (worst possible health state measured by the questionnaire) to 100 (best possible health state). On the basis of these separate subscales, component summary scores can be calculated to provide a global measure of physical (PCS) and mental functioning (MCS) [23]. The PCS and MCS scores range from 0 to 100, with higher scores indicating better health [23] Arabic version of this scale has been assessed for its validity and reliability [24]. Statistical analysis Data were analysed using SPSS for Windows, version 13 and level of significance was set as p \ 0.05. Descriptive data were used for assessing the parameters related to disease. Student’s t-test or the Mann–Whitney
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test was used in independent groups for parametric variables depending on whether data were normally distributed or not. The Chi-square test was used to compare the categorical variables. Multivariate logistic regression using stepwise-automated methods was used to determine the independent determinant of sleep disturbance. The odds ratios (ORs) were calculated for each explanatory variable. The level of significance was set at p \ 0.05.
Results
287 Table 1 Demographic and disease-related characteristics of patients with ankylosing spondylitis Parameters Agea (years) Male
Relation between sleep disturbance, disease-specific variables, domains of SF 36 and psychological scores Significantly worse pain, higher disease activity, important degradation of functional status and high number of nocturnal awakenings were present in patients with sleep disturbance. However, there was no significant relationship between insomnia and demographic variables including age and sex. The correlation coefficients were shown in Table 2. All domains of SF-36 were deteriorated with low scores in patients with insomnia than in non-insomniac patients. The correlation coefficients were shown in Table 2. Using HADS scores of 8 or higher to identify clinically depressed subgroups or anxious subgroups, sleep disturbance was significantly higher in patients with depression and/or anxiety. The correlation coefficients were shown in Table 2. Depressive disorders are present in 71.8 % of insomniacs versus 25.6 % of non-insomniacs and anxiety disorders in 76.1 % of insomniacs versus 33.3 % of non-insomniacs. Multivariate logistic regression analysis revealed that the pain (OR = 1.019; CI 95 % = 1.003–1.035; p = 0.023) and depression (OR = 1.304; CI 95 % = 1.163–1.463; p \ 0.001) were independent risk factors that influenced sleep disturbance (Table 3).
38.5 ± 12.6 75 (68.2 %)
Painc (VAS) (0–100 mm)
10 (0–60)
BASDAIa (0–10)
4.4 ± 2.6
BASFIa (0–10)
5.5 ± 3
HADS-Aa
9.5 ± 5
a
HADS-D Domains of SF36a
Clinical characteristics One hundred and ten patients were recruited, with male predominance n = 75 (68.2 %). The mean age of patients was 38.5 ± 12.6 years. Demographic and disease-related data, the level of depression, anxiety, quality of life and sleep disturbance of the patients are given in Table 1. The mean of HAD depression and HAD anxiety were 9.1 ± 5.3 and 9.5 ± 5, respectively. It was observed that 64.5 % of patients had sleep disorders, 55.5 % had depression and 60 % had anxiety. Insomnia was mild in 18.2 % of the total sample, was moderate in 21.8 %, severe in 15.5 % and very severe in 9 % of patients. The mean number of nocturnal awakenings was 1.46 ± 1.43.
b
9.1 ± 5.3
Physical functioning
44.50 ± 30.42
Role limitations due to physical problems
21.72 ± 36.43
Role limitations due to emotional problems
37.87 ± 47.28
Social functioning
57.93 ± 34.44
Mental health
52.99 ± 23.87
Energy/vitality
41.36 ± 22.51
Bodily pain
40.20 ± 25.89
General health perception
37.17 ± 20.34
SF36 PCS
33.11 ± 10.24
SF36 MCS
41.01 ± 13.20
The number of nocturnal awakeningsa
1.46 ± 1.43
Insomnia item of Hamilton Not presentb
35.5 (39 %)
Mildb Moderateb
18.2 (20 %) 21.8 (24 %)
Severeb
15.5 (17 %)
Very severeb
9 (10 %)
Depressionb
61 (55.5 %)
Anxietyb
67 (60.9 %)
a
29.2 ± 23.2
ESR (mm/1st H)
VAS visual analogue scale, BASDAI Bath Ankylosing Spondylitis Disease Activity Index, BASFI Bath Ankylosing Spondylitis Functional Index, HAD Hospital Anxiety and Depression Scale, HADSA Anxiety Subscale, HADS-D Depression Subscale, SF36 short Form 36, PCS component summary scores of physical functioning, MCS component summary scores of mental functioning, ESR erythrocyte sedimentation rate, CRP C reactive protein a
Mean ± SD
b
Number and percentage
c
Median (Quartiles)
Discussion In the present study, 64.5 % of all patients had sleep disturbance, defined as difficulties of initiating and maintaining sleep. It was found that the pain and depression were significantly associated with insomnia in our data. Sleep disturbance is a frequent complaint reported by patients with AS and is still largely ignored in terms of clinical care, education and research. In our data, we found insomnia in 64.5 % of patients. Similar results have also
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288 Table 2 Relation between sleep disturbance, diseasespecific variables, domains of SF 36 and psychological state
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Characteristics
Sleep disturbance Yes (n = 71)
No (n = 39)
p
Agea (years)
39.09 ± 11.73
37.48 ± 14.19
0.52
Sex maleb
48 (67.6 %)
27 (69.2 %)
0.86
Painc (VAS) (0–100 mm)
20 (0–70)
0 (0–40)
0.04
Disease-specific variables
a
\0.001
BASDAI (0–10)
5.09 ± 2.54
3.16 ± 2.32
BASFIa (0–10)
5.98 ± 2.95
4.65 ± 3.13
0.03
Number of nocturnal awakeningsa
1.85 ± 1.44
0.74 ± 1.09
\0.001
Quality of life by SF 36a VAS visual analogue scale, BASDAI Bath Ankylosing Spondylitis Disease Activity Index, BASFI Bath Ankylosing Spondylitis Functional Index, SF36 Short Form 36, PCS component summary scores of physical functioning, MCS component summary scores of mental functioning, HADSD Depression Subscale, HADSA Anxiety Subscale a
Test t student
b
Test Chi-square
c
Mann–Whitney U
Physical functioning
37.39 ± 29.66
57.43 ± 27.71
0.001
Role limitations due to physical problems
10.07 ± 25.36
42.94 ± 43.66
\0.001
Role limitations due to emotional problems Social functioning
23.70 ± 41.44 51.37 ± 34.43
63.67 ± 46.80 69.87 ± 31.50
\0.001 0.006
Mental health
46.92 ± 23.06
64.02 ± 21.47
\0.001
Energy/vitality
35.70 ± 22.83
51.66 ± 18
\0.001
Bodily pain
32.71 ± 23.97
53.84 ± 23.84
\0.001
General health perception
33.71 ± 19.42
43.46 ± 20.71
0.016
SF 36 PCS
30.85 ± 9.69
37.21 ± 10.05
0.002
SF 36 MCS
37.57 ± 12.46
47.29 ± 12.32
\0.001
Depression (HADS-D C 8)
51 (71.8 %)
10 (25.6 %)
\0.001
Anxiety (HADS-A C 8)
54 (76.1 %)
13 (33.3 %)
\0.001
Psychological stateb
Table 3 Risk factors for sleep disturbance in univariate and multivariate analysis Characteristics
Univariate analysis
Multivariate analysis
Sleep disturbance
Sleep disturbance
OR
CI (95 %)
p
BASDAI (0–10)
1.384
1.152–1.661
0.001
BASFI (0–10)
1.156
1.011–1.321
0.034
Pain (VAS) (0–10 mm) SF36 PCS
1.015 0.939
1.001–1.028 0.902–0.978
0.030 0.002 \0.001
SF36 MCS
0.942
0.911–0.974
HADS-D
1.287
1.154–1.434
\0.001
HADS-A
1.194
1.085–1.313
\0.001
OR
CI (95 %)
p
1.019
1.003–1.035
0.023
1.304
1.163–1.463
\0.001
OR odds ratio, CI confidence interval BASDAI Bath Ankylosing Spondylitis Disease Activity Index, BASFI Bath Ankylosing Spondylitis Functional Index, SF36 Short Form 36, PCS component summary scores of physical functioning, MCS component summary scores of mental functioning, HADS-D Depression Subscale, HADS-A Anxiety Subscale
been reported by Ward et al. [25] and Gu¨naydin et al. [26], who observed that 54 and 54.8 %, respectively, of AS patients had disturbance of sleep quality. Da Costa et al. [27] found that 69 % of patients with spondylarthropathy classified as poor sleepers. Heiberg et al. [28] reported that sleep is considered a prioritized dimension for improvement, more frequently by patients with AS than by patients with other inflammatory arthropathies (rheumatoid arthritis and psoriatic arthritis).
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Sleep disturbances in patients with rheumatic disease have for many years been neglected; recently, an increasing number of articles have dealt with the complicated interactions between pain, fatigue and sleep in rheumatic disorders [26, 29, 30]. Taylor-Gjevre et al. [31] found abnormal sleep quality in 67.3 % of patients with rheumatic diseases. Estimates of the percentage of fibromyalgia patients experiencing some sleep problem range from 74 % in the population on which the American College of
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Rheumatology (ACR) criteria were established [32] to as high as 95 and 99 % in two recent studies [33, 34] and at least 60 % of rheumatoid arthritis patients report sleep problems according to some data [35]. Similar results were found in patients with systemic lupus erythematosus, in whom prevalence of sleep disturbance was 62 % [36]. In our study, 55.5 % of the patients had depression and 60 % had anxiety, which is higher than the literature data. The estimates of the prevalence of emotional problems were from 20 to 31 % [37, 38]. This can be explained by low socioeconomical status of patients and absence of health insurance in addition to the parameters of the disease itself. We found that patients with AS have significantly impaired quality of life on all scales of SF-36, and this concords with the data reported in the literature [39]. The relationship amongst sleep disturbances, diseasespecific variables, mental health status and quality of life in patients with AS has not been investigated as much. In our study, significantly worse pain, higher disease activity, decreasing global function and short form-36 summary scores, depression, and anxiety scores were present in patients with insomnia. We also found that the pain and depression were the independent risk factors that influenced the sleep disturbance. These results partly consist with those of Da Costa et al. [27], who observed that worse functional status was associated with poorer sleep quality, longer sleep latency, shorter sleep duration and poorer sleep efficiency in patients with spondylarthropathy. Higher depressed mood scores emerged in the multivariate analyses as a significant determinant of poorer sleep quality, shorter sleep duration and poorer sleep efficiency [27]. Similar results were reported in patients with different rheumatic disorders. Indeed, Frech et al. [4] found that sleep disturbances are common in systemic sclerosis and are associated with worsening dyspnoea, depressed mood and severity of reflux symptoms [4]. In connection with this, high pain levels and high sleep disruption levels were associated with high depression scores in a 2-year study of over 200 rheumatoid arthritis patients, suggesting associations between pain, sleep and mood problems [35]. Chandrasekhara et al. [36] reported that functional disability, disease activity and depressed mood correlated positively with sleep disturbances in systemic lupus erythematosus and in multiple regression analyses disease activity was found to be an independent determinant of sleep quality. With regard to depression, it was found that insomnia is more frequently noted amongst patients with psychiatric diagnoses, especially major depressive disorders [40]. About pain, Studies by Atkinson et al. [41] and Pilowsky et al. [42] suggest that 50 % of patients with low back
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pain and 70 % of chronic pain patients suffer from sleep disturbance, respectively. A large population studied by Moffitt et al. [43] indicated that pain was the most common cause of a comorbid or secondary sleep disturbance. Several studies suggest that a positive relation is established between sleep problems and fatigue in AS patients. Indeed, patients complaining of important fatigue were more likely to have more than three awakenings in one night and to feel tired in the morning. Jones and al [6] found that the patients with fatigue reported more sleep disturbance, with 41 % (compared to 26 % in patients without fatigue). In our study, the relationship between sleep disturbance and fatigue has not been investigated. Our study has some limitations. Firstly, we did not have healthy control group in order to compare the frequency of sleep disturbance and the others factors related insomnia. Secondary, we did not use a detailed questionnaire for insomnia, although there is no universal questionnaire to assess sleep for comparing this parameter between the different studies. Thirdly, this is a cross-sectional design, consequently, observed associations need confirmation in a longitudinal observational design.
Conclusion Sleep problems are prevalent amongst Moroccan patients with AS. Our findings suggest that pain and depression were the independent risk factors that influenced the sleep disturbance and hence, the need for evaluation and optimal management of pain and depression to improve sleep quality in AS patients. Conflict of interest
None.
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