Lupus (2014) 23, 1350–1357 http://lup.sagepub.com

PAPER

Poor sleep quality in systemic lupus erythematosus: does it depend on depressive symptoms? L Palagini1, C Tani2, RM Bruno3, A Gemignani4, M Mauri1, S Bombardieri2, D Riemann5 and M Mosca2 1

Psychiatry Unit, Department of Clinical and Experimental Medicine, School of Medicine, University of Pisa, Pisa, Italy; 2Rheumatology Unit, Department of Clinical and Experimental Medicine, School of Medicine, University of Pisa, Pisa, Italy; 3Institute of Clinical Physiology – CNR, Pisa, Italy; 4Psychology Unit, Department of Surgery, Medical, Molecular & Critical Area Pathology, School of Medicine, University of Pisa, Pisa, Italy; and 5Department of Psychiatry & Psychotherapy, University of Freiburg Medical Center, Freiburg, Germany

Objectives: Sleep disturbances are frequently observed in rheumatic diseases including systemic lupus erythematosus (SLE). This study aimed at evaluating the prevalence of insomnia, poor sleep quality and their determinants in a cohort of SLE patients. Methods: Eighty-one consecutive SLE female patients were evaluated in a cross-sectional study. The Pittsburgh Sleep Quality Index (PSQI), the Insomnia Severity Index (ISI), the Beck Depression Inventory (BDI) and the Self-rating Anxiety Scale (SAS) were administered. Patients with previous diagnosis of obstructive sleep apnea or restless legs syndrome were excluded. Fifty-three women with hypertension (without SLE) were enrolled as control group (H). Results: In the SLE cohort poor sleep quality (65.4% vs 39.6%, p < 0.01) and difficulty in maintaining sleep and/or early morning awakening (65.4% vs 22.6%, p < 0.001), but not insomnia (33.3% vs 22.6%, p ¼ ns), were more prevalent than in H. Depressive symptoms were present in 34.6% of SLE vs 13.2% H patients (p < 0.001) while state anxiety was more common in H patients (H 35.8% vs SLE 17.3%, p < 0.005). SLE was associated with a 2.5-times higher probability of presenting poor sleep quality in comparison to H (OR 2.5 [CI 1.21–5.16]). After adjusting for confounders, both depressive symptoms (OR 4.4, [1.4–14.3]) and use of immunosuppressive drugs (OR 4.3 [CI 1.3–14.8]) were significantly associated with poor sleep quality in SLE patients. Furthermore, poor sleep quality was not associated either with disease duration or activity. Conclusions: In a cohort of SLE women, insomnia and poor sleep quality, especially difficulties in maintaining sleep, were common. Depressive symptoms might be responsible for the higher prevalence of poor sleep quality in SLE. Lupus (2014) 23, 1350–1357. Key words: Insomnia; poor sleep quality; systemic lupus erythematosus; depression; anxiety

Introduction Sleep is an active process by which metabolism, tissue restoration and general homeostatic balance are maintained.1,2 Sleep disorders have emerged as important course and severity determinants of many conditions including rheumatologic disorders, and among them, systemic lupus erythematosus (SLE).3–9 In rheumatic diseases nocturnal sleep disruption is a common finding, manifesting in different complaints such as difficulty falling asleep, poor quality and nonrestorative sleep, numerous awakenings Correspondence to: Laura Palagini, Psychiatry Unit, Department of Clinical and Experimental Medicine, School of Medicine, University of Pisa, Via Roma 67, 56100, Pisa, Italy. Email: [email protected], [email protected] Received 7 February 2014; accepted 2 June 2014

during the night, early morning awakening, daytime sleepiness, chronic fatigue and sensations of restlessness, which all may significantly affect the quality of life in these patients. On the other hand, it has also been hypothesized that sleep disorders may exert a negative effect on disease parameters and its course.4 Among the rheumatic disorders, rheumatoid arthritis and fibromyalgia have been investigated more extensively from a sleep medicine perspective.4 Different types of sleep disorders, including insomnia, obstructive sleep apnea syndrome (OSAS) or restless legs syndrome (RLS), have also been reported to occur frequently in patients with SLE;4,9 only few studies have explored this association with controversial results. In particular, the question whether sleep is affected by suffering from a chronic, disabling disease or by the disease process itself, with its immunological

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and inflammatory derangement, is still a matter of debate. As a consequence, the primary aim of this study is to investigate the prevalence and characteristics of sleep quality and insomnia in SLE and to compare sleep features with a clinical control group of hypertensive patients matched for age and gender. The secondary aim is to evaluate the relationships between insomnia/poor sleep quality and disease-related variables, as well as comorbidities and therapies in the SLE sample.

Methods

involvement as well as actual disease manifestations and ongoing therapies were recorded. Previous or ongoing neurological manifestations were defined according to the American College of Rheumatology nomenclature and case definitions.13 Cumulative glucocorticoid (GC) dosages until the assessment time was also computed. Disease activity was evaluated using the European Consensus Lupus Activity Measurement Index (ECLAM); a score >2 was considered as indicative of active disease.14 Cumulative damage was measured using the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index (SLICC/ACR DI).15

Patients

Questionnaires

From January to December 2012, 81 consecutive outpatients attending the Lupus Clinic of the Rheumatology Unit of the University of Pisa, Italy, were evaluated. All subjects enrolled fulfilled at least four of the American College of Rheumatology revised criteria for SLE.10 An age-matched control group of women suffering from another chronic disease, i.e. hypertension (H), was also recruited at their first visit to the Hypertension Outpatient Unit of the University of Pisa. Essential arterial H was diagnosed according to current guidelines.11 SLE and H subjects underwent a complete medical evaluation, including a clinical interview to determine the patients’ medical, neurologic and psychiatric disorders and pre-existing sleep disorders. Inclusion criteria were age >18 years and written informed consent; exclusion criteria were major cognitive deficits that would preclude the completion of the questionnaires, or severe medical diseases including endstage renal disease and active neoplastic disease. Furthermore, patients with a score of 1 or more on item 10 of the Pittsburgh Sleep Quality Index (PSQI),12 regarding self-reported symptoms or symptoms reported by the patient’s roommate that were compatible with OSAS or RLS, were excluded from the analysis after enrollment, as they may affect both insomnia symptoms and sleep quality.

The following questionnaires were administered to the patients:

Clinical evaluations After enrollment, patients underwent a standard medical examination. Anthropometric data (weight and height) and sociodemographic data, including age, education and employment status were also collected. For SLE patients, medical and pharmacological history, previous organ

. Pittsburgh Sleep Quality Index (PSQI):12 The PSQI is a widely used, self-rated, standardized questionnaire, assessing sleep quality in the previous month. The 19 questions are grouped into seven component scores, each exploring a different sleep feature, whose sum yields a global PSQI score ranging from 0 to 21. Poor sleep quality was defined, according with the PSQI authors’ recommendations,12 when the PSQI sum score was >5. The following PSQI-derived data were also analyzed: increased sleep latency (>30 minutes) (component 2), difficulty in maintaining sleep and early morning awakening (component 5). . Insomnia Severity Index (ISI):16 The ISI is a seven-question questionnaire for self-assessment of insomnia in the previous two weeks. It is a reliable and valid instrument to detect cases of insomnia. For the purposes of this study, according to the ISI authors’ recommendations,16 insomnia was defined by an ISI score of 8 or higher. . Beck Depression Inventory (BDI):17 The BDI is a 21-question inventory for self-assessment, one of the most widely used instruments for measuring the severity of depression. According with the BDI authors’ recommendations,17 a BDI score greater than 10 is indicative of clinically significant depressive symptoms. . Self-rating Anxiety Scale (SAS):18 The SAS is a 20-item self-report assessment scale built to measure anxiety levels, based on scoring in four groups of manifestations: cognitive, autonomic, motor and central nervous system symptoms. Each question is scored on a Likert-type scale of 1–4. Overall assessment is calculated by Lupus

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total score. According with the SAS authors’ recommendations,18 the presence of anxiety symptoms was defined with an SAS score >44. Statistical analysis Statistical analysis was performed using NCSS 2008.19 Results were expressed as mean  standard deviation (SD). Differences in means between groups were analyzed using analysis of variance for normally distributed variables, or KruskalWallis Z-Test for not normally distributed variables; categorical variables were analyzed by 2 test. Multiple logistic regression models were built in order to elucidate independent determinants of sleep quality and insomnia. Variables associated with p < 0.10 to poor sleep quality or insomnia in the univariate analysis were inserted in the multiple regression model.

Results Clinical characteristics Among the 88 SLE patients enrolled, those with self-reported (or reported by roommate) sleep apneas, snoring, and leg restlessness (n ¼ 5) or with incomplete data (n ¼ 2) were excluded. The final analysis was performed on 81 SLE patients. Clinical characteristics of the study population are listed in Table 1. Renal involvement was recorded in 38 patients (43.2%), being active in three patients, while neurological manifestations were reported in 12 (13.6%) patients: cerebrovascular disease in eight cases, Table 1 Clinical and socio-demographic characteristics of the study population

Age (years) Education (%) -undergraduate -graduated Employment status (%) -unemployed/household -employed Disease duration (years) Smoking (%) Hypertension (%) Obesity (%) Diabetes mellitus (%) Hypercholesterolemia (%)

SLE (n ¼ 81)

H (n ¼ 53)

p value

43.6  11.2

44.0  7.8

0.42

90.2 9.9

93.2 15.1

0.61

51.3 48.7 15  8 13.8 22.5 3.9 2.5 23.1

39.6 60.4 82 21.7 100 20.5 2.0 19.2

0.11

SLE: lupus erythematosus; H: hypertension.

< 0.0001 0.25 0.05), while the prevalence of insomnia was not significant (ns) (p ¼ 0.18). Considering sleep Table 2 Sleep and psychiatric characteristics of the study population

ISI (mean  SD) PSQI (mean  SD) BDI (mean  SD) SAS (mean  SD) Insomnia (%) Poor sleep quality (%) Increased sleep latency (%) Difficulty maintaining sleep/early awakening (%) State anxiety (%) Depressive symptoms (%) Hypnotics use (%)

SLE (n ¼ 81)

H (n ¼ 53)

p value

6.2  7.7 7.2  3.6 5.9  7.9 24.8  14.7 33.3 65.4 27.2 65.4

5.4  6.6 5.4  6.7 2.4  4.7 25.0  7.8 22.6 39.6 26.4 22.6

0.43 0.0004 0.0003 0.02 0.18 0.003 0.92 10 years, anxiety, depressive symptoms), only depressive symptoms were significantly associated with poor sleep quality (OR 5.6 [CI 1.8– 17.4]), while the association between SLE and poor sleep quality lost significance (OR 1.1 [CI 0.4–3.3]). Comparison between SLE subgroups with or without sleep disorders Sleep and psychiatric features of the study population are listed in Table 2. Poor sleep quality, defined as a global PSQI score >5, was present in 65.4% of the SLE population, while insomnia, defined by an ISI score >8, was present in 33.3%. Difficulty in maintaining sleep and early morning awakening was largely prevalent among SLE patients, reaching 65.4%. Depressive symptoms were more common (34.6%) than anxiety symptoms (17.3%) in the SLE sample. As shown in Table 3, prevalence of poor sleep quality, insomnia, depressive symptoms and anxiety level were not significantly affected by comorbidities such as fibromyalgia (p ¼ ns for all) and hypertension (p ¼ ns for all) in the SLE group (Table 3). Depressive symptoms were more common in SLE patients with poor sleep quality and insomnia with respect to SLE patients without sleep disorders (41.5% vs 21.4 %

and 44.5% vs 29.6%, respectively; p < 0.05 for both), while this was not observed for anxiety (13% vs 25% and 14% vs 18%, respectively; p ¼ ns for both) (Table 4). Concerning the disease characteristics, renal involvement was significantly (p < 0.05) more common in the SLE poor sleepers as compared to normal sleepers (50.9% vs 28.6%). It was also more common in SLE patients suffering from insomnia as compared to normal sleepers (55.6% vs 37%). In addition neurologic involvement and antiphospholipid syndrome tended to be more frequent in SLE patients suffering from insomnia with respect to their counterparts, even if the difference did not reach statistical significance

Table 3 Sleep and psychiatric characteristics of SLE patients: effect of fibromyalgia and hypertension Without H With H Without F With F (n ¼ 62) (n ¼ 19) (n ¼ 68) (n ¼ 13) State anxiety (%) Depressive symptoms (%) Insomnia (%) Poor sleep quality (%) Increased sleep latency (%) Difficulty maintaining sleep/early awakening (%) Hypnotics use (%)

19.4 32.3 32.3 61.3 22.6 61.3

5.6 44.4 38.9 77.8 38.9 77.8

16.2 30.9 30.9 64.7 25.0 64.7

23.1 53.8 46.2 69.2 38.5 69.2

8.1

11.1

8.8

7.7

SLE: systemic lupus erythematosus; H: hypertension; F: fibromyalgia. All p ¼ not significant.

Table 4 Clinical characteristics of SLE patients according to the presence or absence of poor sleep quality or insomnia Without PSQ (n ¼ 28) State anxiety (%) 25.0 Depression (%) 21.4 Neurologic involvement (%) 7.1 Renal involvement (%) 28.6 APS (%) 7.1 Glucocorticosteroids (%) 85.7 Immunosuppressive 25.0 drugs (%) Cyclophosphamide (%) 7.1 Mycophenolate mofetil (%) 10.7 Azathioprine (%) 0 Cyclosporine (%) 3.6 Methotrexate (%) 3.6 Current smoking (%) 7.1 Obesity (%) 3.7 Age (years) 42.8  11.0 Disease duration (years) 17  9

With PSQ (n ¼ 53)

Without I With I (n ¼ 54) (n ¼ 27)

13.2 41.5 17.0 50.9a 9.4 88.7 52.8a

18.5 29.6 9.3 37.0 5.6 88.9 40.7

14.8 44.4 22.2 55.6 14.8 85.2 48.1

1.7 30.2a 13.2a 5.7 3.8 17.3 4.0 44.0  11.6 15  8

5.6 24.1 3.7 5.6 3.7 13.2 4.0 43.1  11.0 16  9

0 22.2 18.5a 3.7 3.7 14.8 3.7 44.6  12.0 16  7

SLE: systemic lupus erythematosus; PSQ: poor sleep quality; I: insomnia; APS: antiphospholipid syndrome. ap < 0.05. Lupus

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(Table 4). Immunosuppressive therapy was more commonly used in SLE patients with poor sleep quality (p ¼ 0.02), in particular mycophenolate mofetil and azathioprine use was significantly more common in SLE women with than without poor sleep quality. Conversely, the use of GCs and their cumulative dose did not differ among SLE subjects with or without sleep disorders. Similarly, ECLAM and SLICC score did not differ according to the presence or absence of poor sleep quality or insomnia. In order to identify the determinants of poor sleep quality in the SLE group, a multiple logistic regression analysis was performed, considering poor sleep quality as the dependent variable and characteristics whose prevalence was significantly different between SLE women with or without poor sleep quality as independent variables. In a model including depressive symptoms, use of immunosuppressive drugs and renal involvement, both depressive symptoms (OR 4.4, CI 95% 1.4– 14.3) and use of immunosuppressive drugs (OR 4.3, CI 95% 1.3–14.8) remained independent determinants of poor sleep quality (Figure 1).

Discussion The main result of this study is the demonstration of a high prevalence of poor sleep quality and insomnia in a cohort of women with SLE. The prevalence of sleep disorders was higher in SLE patients than in the control group, which consisted of a matched cohort of women affected by another chronic disease, i.e. arterial H. The main determinant of poor sleep quality in the SLE cohort was the presence of depressive symptoms, suggesting that depressed mood might play an important role in the pathogenesis of sleep disorders in SLE.

Our data demonstrated the presence of poor sleep quality in almost two-thirds of the SLE cohort, while insomnia was diagnosed in about one-third. In particular, prevalence of sleep disorders found in SLE patients was higher than in women without SLE.20,21 Our results are in line with what was previously reported in other SLE cohorts.22 When we considered sleep features, difficulty in maintaining sleep and early morning awakening were the most common findings in SLE, confirming previous studies.22–25 As far as the comorbidity with other psychiatric conditions is concerned, SLE patients show high levels of depressive symptoms. In our SLE sample the prevalence of depressive symptoms was about 35%, which is significantly higher than in the general population.26,27 Depression is in fact a very common complaint in SLE and it is included in the SLE neuropsychiatric manifestations.28,29 The prevalence of anxiety was also higher in SLE patients than in the general population.30 Interestingly, SLE patients showed a higher prevalence for poor sleep quality, insomnia and depressive symptoms even when compared with patients suffering from another chronic non-rheumatologic disorder, such as arterial H. Indeed H is a clinical condition in which sleep disorders are particularly well represented and might also play a causative role.8,31 Conversely, the prevalence of anxiety is higher in H than in SLE women, who however presented increased anxiety levels as compared to the general population. This finding may suggest that living with a chronic disease has a profound impact on mood,32,33 anxiety33 and sleep characteristics.34 Indeed we may hypothesize that each chronic condition may be related to a different specific pattern of mood, anxiety and sleep characteristics and it should be addressed using specific assessment and treatment approaches in further studies. Interestingly, hypertensive SLE women

Figure 1 Multiple logistic regression analysis in the systemic lupus erythematosus (SLE) group, using poor sleep quality as dependent variable. Lupus Downloaded from lup.sagepub.com at Northeastern University on January 4, 2015

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were indistinguishable from normotensive SLE women as far as sleep pattern and prevalence of mood disorders are concerned, indicating that SLE disease per se, for its profound impact on quality of life and possibly for disease-specific mechanisms, is the main factor influencing sleep and mood.5,6,35,36 These results could also be of relevance for the education of health care professionals in different specialties in order to achieve better communication and adherence to lifelong treatments. The second part of the study was aimed at identifying the predictors of poor sleep quality in the SLE cohort. We found that in our cohort depressive symptoms were significantly more prevalent in SLE patients suffering from poor sleep quality and insomnia. Furthermore, we performed a multiple logistic regression analysis, including those variables that were significantly associated with poor sleep quality in the univariate analysis. After controlling for all confounding factors, depressive symptoms were determinant of poor sleep quality in SLE. Correlations between poor sleep quality/ insomnia and depressive symptoms have been shown very clearly in the general population 5,6,37 and have also been previously hypothesized in SLE.22–25 Another finding supporting the role of depression in the pathogenesis of sleep disorders in SLE concerns sleep pattern: Our results showed that SLE patients suffer mainly from difficulty in maintaining sleep and/or early morning awakening, which are characteristic features of sleep disorders in depressed patients.38,39 Since our data are derived from a cross-sectional survey, they cannot provide information about causal relationships. However, our study may support previous hypotheses suggesting chronic inflammation as a common pathogenic mechanism among immunologic disorders such as SLE, poor sleep quality/insomnia, and depressive disorders.40–46 We also explored the hypothesis that disease-specific characteristics of SLE might directly influence sleep quality. Surprisingly, we did not find any independent relationship between disease-related variables, such as disease activity and damage and organ involvement, and sleep disturbances in SLE patients. Our results are in agreement with a recent report by Valencia-Flores et al.47 but in conflict with other studies showing a significant correlation with disease activity parameters.25,47–49 One possible explanation of this discrepancy can be represented by the characteristics of our study population; indeed, our patients were all recruited during the routine outpatient visits and, as expected, disease activity was generally low, with

only mild active organ involvement. Among the possible clinical manifestations of the disease, only renal involvement (present or past) and the use of immunosuppressant drugs were more frequent in the subgroup of poor sleepers as compared to normal sleepers. It is well established that chronic kidney disease is associated per se with a variety of sleep disorders.50,51 Worthy of note, the association between immunosuppressive drug use and poor sleep quality remained significant in the multiple logistic regression analysis. This novel finding, though unable to prove a causality link because it originated with cross-sectional data, needs to be confirmed in further studies. However, it should also be considered that both renal damage and the use of immunosuppressive therapy could simply reflect a greater degree of disease severity; indeed, we can hypothesize that patients with renal involvement, usually treated with more intensive therapy, including immunosuppressive drugs, could be at higher risk of sleep problems because of having more severe disease. Surprisingly, poor sleep quality was not related to GC therapy, in contrast to some previous findings.24,45 Since the vast majority of SLE patients included in the study were in chronic, stable treatment with corticosteroids, this might have hampered the results about the role of steroid therapy in the development of sleep disorders. On the basis of these data we may conclude that sleep disorders, especially poor sleep quality, are very common in the SLE population. When compared with another chronic disease such as H, SLE patients seem to have more sleep problems, especially considering sleep quality and difficulty in maintaining sleep. Difficulties in maintaining sleep and/or early morning awakening seem to be the more common sleep feature in SLE, while anxiety does not seem to influence sleep pattern. In the SLE cohort, depressive symptoms and immunosuppressive drug use were independent determinants of poor sleep quality. These results suggest a complex interrelationship between the inflammation system and both sleep and mood regulation. However, studies on this argument are lacking and mechanisms that may relate insomnia or depression to SLE are still unknown. Moreover, since this is a cross-sectional analysis, this relationship needs to be clarified in further prospective and mechanistic studies. Nevertheless, these data highlight the importance of investigating sleep disorders even during routine outpatient visits and during disease remission; indeed, some degree of sleep complaints could represent an important red flag for underlying and Lupus

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unrecognized depressive symptoms, which may be more difficult for the patient to communicate.

Funding This research received no specific grant from any funding agency in the public, commercial, or not or- profit sectors.

Conflict of interest statement The authors have no conflicts of interest to declare.

Acknowledgments We would like to acknowledge Elena Signorini and Elena Cecconi for their contribution and Wendy Doherty for the English revision.

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Poor sleep quality in systemic lupus erythematosus: does it depend on depressive symptoms?

Sleep disturbances are frequently observed in rheumatic diseases including systemic lupus erythematosus (SLE). This study aimed at evaluating the prev...
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