Significant sleep disturbances in euthymic bipolar patients

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ScienceDirect Comprehensive Psychiatry 54 (2013) 1003 – 1008 www.elsevier.com/locate/comppsych

Significant sleep disturbances in euthymic bipolar patients Paulo Marcos Brasil Rocha a,⁎, Fernando Silva Neves a, b , Humberto Corrêa a, b, c a Programa de Pós-graduação em Neurociências, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte (MG), Brazil Departamento de Saúde Mental, Faculdade de Medicina, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte (MG), Brazil c Instituto Nacional de Ciência e Tecnologia de Medicina Molecular, Belo Horizonte, Minas Gerais, Brazil

b

Abstract Objective: A growing amount of data suggests that sleep dysfunction is frequently observed in bipolar disorder (BD) patients even when they do not fulfill the criteria for major mood episodes. Thus, we performed a case–control study assessing sleep status in a group of euthymic BD patients and a group of health controls. Methods: A total of 209 subjects (104 health controls and 105 BD patients) were enrolled in the study. The Pittsburgh Sleep Quality Index (PSQI) was used for sleep assessment. Inclusion criteria for the BD group were a diagnosis of BD, following DSM-IV-TR criteria, according to the MINI-plus structured clinical interview. Euthymia was established as a score lower than 7 both in the Hamilton Depression Rating Scale (HDRS) and in the Young Mania Rating Scale (YMRS). Health controls were also interviewed using the MINI-plus and included in this study if they were free of any current or past DSM-IV-TR axis I psychiatric disorder as well the actual use of psychopharmacological medications. Results: While 21.2 % of the control group displayed poor sleep quality according to the global PSQI-BR score, 82.9 % of the euthymic BD patients had poor sleep quality (p = 0.000). PSQI sleep duration subcomponent showed comparable results in the two groups (p = 0.535), even though BD patients had significant disruptions in sleep latency (p = 0.000) and sleep efficiency (p = 0.000) subcomponents. Conclusion: We were able to show that BD patients, even in euthymic phase, exhibit a significantly worse sleep quality as compared with health controls as assessed by PSQI total score and five of its seven subcomponents. © 2013 Elsevier Inc. All rights reserved.

1. Introduction Bipolar disorder (BD) is a chronic, disabilitating and recurrent mood disorder characterized by manic/hypomanic and depressive states along with interepisodic phases named euthymia [1,2]. At least theoretically, it is an asymptomatic phase since the current diagnosis criteria for BD do not contemplate any symptoms during euthymia [2]. Nevertheless, in recent years a strong amount of evidence shows that BD patients may present significant impairments even when in euthymic phase of the disorder, contributing to reduce global functioning, a worse quality of life and poor prognosis [3–5]. A growing amount of data shows that sleep dysfunction is

This study was supported by Instituto Nacional de Ciência e Tecnologia de Medicina Molecular (INCT/CNPq/MCT, FAPEMIG), CNPq Grant No. 473674/2009-2, and FAPEMIG Grant PPM-IV. No previous presentation of the data. ⁎ Corresponding author. Rua do Ouro 1138/1601 Serra, Belo Horizonte, Minas Gerais 30220-000, Brazil. Tel.: +55 31 32252393. E-mail address: [email protected] (P.M.B. Rocha). 0010-440X/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.comppsych.2013.04.006

frequently observed even when BD patients do not fulfill the criteria for major mood episodes [6]. Thus, at least partially, sleep dysfunction could explain those observed impairments. Sleep disturbances are quite common features of both manic and depressive phases of the disorder [6] and were pointed as a core disease characteristic since the early descriptions of manic depressive insanity by Kraepelin [7]. Since then, many studies have confirmed Kraepelin's statement both in depression and mania. In depression, retrospective studies consistently showed that insomnia, hypersomnia and early awakening are frequent symptoms during depressive episodes, with rates between 77% and 90% [8–11]. Prospective studies have demonstrated that insomnia is an important predictor of depressive episodes [12,13] and associated with higher taxes of recurrences in unipolar and bipolar depression [12,14,15]. Furthermore, polysomnographic studies showed higher sleep fragmentation and early awakening, resulting in altered sleep latency and sleep efficiency compared to controls [16]. During manic episodes, studies have demonstrated that the vast majority of BD patients suffer from decreased sleep need,

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with taxes as high 69%–99% [17–19]. Several studies have also showed that sleep reduction is the most frequent prodrome of new manic episodes [20–22]. In fact, prospective studies have showed that sleep reduction is an important predictor of new manic episodes in BD patients [23,24]. Likewise, some studies have showed that artificial sleep deprivation can trigger BD patients into new episodes of mania [25,26]. Far less studies are available concerning sleep disturbances in the interepisodic/euthymic phase of the disorder [27]. Harvey et al. [28] conducted a study comparing the sleep function of 20 euthymic BD with 20 controls and 20 primary insomnia patients using the Pittsburgh Sleep Quality Index (PSQI) and actigraphy. The authors' findings show that sleep status of the BD group was similar to the primary insomnia group and differed from the control group. Still, the authors found that 70% of the euthymic BD patients had poor sleep quality according to the PSQI assessment. Actigraphic studies showed that, compared to controls, euthymic BD showed longer sleep onset latency, lower average daily activity, and more fragmentation of the sleep– wake cycle and more night-to-night variability [29–31]. Thus, in order to better address this question, we conducted a case–control study comparing sleep performance in a larger sample of euthymic BD patients with a group of controls matched for several potential interfering bias factors, such as age, gender and clinical comorbidities. We hypothesized that BD patients will differ significantly from controls in sleep quality and in general sleep performance.

2. Methods Our study was performed at the IPSEMG (Instituto de Previdência do Servidor Público do Estado de Minas Gerais) and HC-UFMG (Hospital das Clínicas da Universidade Federal de Minas Gerais) Bipolar Unities. Local human ethics committee approved all the procedures of our research and individuals had given a voluntary written informed consent after a full explanation of the study. 2.1. Study design This is a case–control study where a total of 209 subjects (104 health controls and 105 BD patients) were enrolled. All subjects answered a personal and demographic questionnaire for better characterization of the sample. Inclusion criteria for the BD group were a diagnosis of BD, following DSM-IV-TR criteria, according to the MINI-plus structured clinical interview [32]. Euthymia was established as a score lower than 7 both in the Hamilton Depression Rating Scale (HDRS) [33] and in the Young Mania Rating Scale (YMRS) [34]. Health controls were also interviewed using the MINI-plus and included in this study if they were free of any current or past DSM-IV-TR Axis I psychiatric disorder as well the actual use of psychopharmacological medica-

tions. Alcohol dependence was an exclusion criterion for both groups. 2.2. Sleep assessment We used the Pittsburgh Sleep Quality Index validated to the Portuguese language for (PSQI-BR) sleep assessment of the subjects [35]. The PSQI is a self-rating questionnaire created with the main goal of providing a standardized measure of sleep quality that would be easily answered and interpreted, which would also reliably discriminate subjects with good sleep quality from those with poor sleep quality [35,36]. The questionnaire assesses sleep quality and disturbances over a 30-day period. It consists of 19 selfrated questions grouped into seven subcomponents equally rated in a scale from 0 to 3, generating a final score from 0 to 21. The seven subcomponents correspond to specific dimensions related to sleep quality that are generally assessed in clinical practice. Global PSQI scores N 5 point to poor sleep quality identifying clinically significant sleep disturbance with 89.6% sensitivity and 86.5% specificity. We further compared groups transforming each of the seven PSQI subcomponents into categorical variables. 2.3. Chronic medical conditions Lifetime chronic medical conditions were accessed by clinical interview and review of medical records. They were measured by counting the number of medical conditions reported. It was taken into account conditions as stroke, heart attack, heart disease, hypertension, asthma, lung disease, diabetes, ulcer, seizure disorders, and cancer. Like previous studies, we used this variable (the count for lifetime chronic medical conditions) as a continuous variable [37]. 2.4. Statistical analysis Initially, we performed a comparison of clinical and demographic variables between the euthymic BD and the control group. Thus we compared the results of the application of the PSQI-BR between the two groups. We used the chi-square asymptotic or exact Pearson's test for categorical variables and the Mann–Whitney test when treating age as a continuous variable. All variables were assessed considering a significance level of 5%. 3. Results In total, 105 BD patients were enrolled in the study. Ninety-four patients (89.50%) fulfilled the diagnostic criteria for BDI, according to DSM-IV-TR, while 11 patients (10.50%) satisfied the criteria for BDII. The control group comprised 104 subjects. Comparisons of clinical and demographic variables between the two groups are presented in Table 1. Groups were comparable for all demographic variables we studied except for employment status (p = 0.000), with only 26.7% of the BD patients attending a

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Table 1 Clinical and demographic variables assessed in the BD and control groups.

Table 2 Clinical variables assessed in the BD sample.

Clinical and demographic variables

p-Value

Clinical variables of the BD sample

Medium or N

Standard deviation or %

0.877

Duration of illness Number of hospitalizations Age at onset of illness Age at 1st manic episode Age at 1st depressive episode No. of manic/mixed episodes No. of depressive episodes No. of rapid cycling patients Suicide attempt No. of attempts Age at 1st attempt

19.79 6.20 26.30 28.73 26.92 6.133 7.114 26/105 52/105 2.53 29.36

12.999 7.123 9.970 10.154 9.304 6.833 5.456 24.761 49.52 2.275 9.82

No. of clinical medical comorbidities None 1 ≥2 Use of clinical medications Yes No Current alcohol consumption Sim Não Alcohol consumption style Social Abusive Past alcohol consumption Yes No Tobacco use Yes No Coffee use Yes No Coffee consumption style Only morning Several times a day Age (y; continuous) Age (categorical) ≤ 50 y N 50 y Sex Female Male Number of years in school 5-8 ≥9 Marital status Single Married Others (widowed + divorced) Employment status Active Inactive Children Yes No

Bipolar (n = 105)

Controls (n = 104)

55 (52.4%) 58 (55.8%) 29 (27.6%) 26 (25.0%) 21 (20.0%) 20 (19.2%) 0.620 48 (45.7%) 44 (42.3%) 57 (54.3%) 60 (57.7%) 0.298 40 (38.1%) 47 (45.2%) 65 (61.9%) 57 (54.8%) 0.000 24 (60.0%) 47 (100.0%) 16 (40.0%) 0 (0.0%) 0.398 54 (51.4%) 46 (45.5%) 51 (48.6%) 55 (54.5%) 0.000 49 (46.7%) 11 (10.6%) 56 (53.3%) 93 (89.4%) 0.744 85 (81.0%) 86 (82.7%) 20 (19.0%) 18 (17.3%) 0.104 32 (37.6%) 43 (50.0%) 53 (62.4%) 43 (50.0%) 47 ± 18.5 46 ± 36

0.883 0.956

64 (61.0%) 63 (60.6%) 41 (39.0%) 41 (39.4%) 0.497 81 (77.1%) 76 (73.1%) 24 (22.9%) 28 (26.9%) 0.070

hospitalizations, number of major mood episode and the high-frequency polypharmacy of psychiatric drugs may show the severity of this BD sample. Benzodizepines, nonbenzodiazepines hypnotics and fenothiazines were the specific sleep medications prescribed in our BD sample. Most common medical conditions in the BD group were, respectively, systemic arterial hypertension, hypothyeoidism and diabetes, as shown in Table 3. Comparisons of PSQI scores between the groups are shown in Table 4. While 21.2 % of the control group displayed poor sleep quality according to the global PSQI-BR score, as much as 82.9 % of the euthymic BD patients had poor sleep quality (p = 0.000). Concerning the seven PSQI subcomponents, we found that the two groups were significantly different in five. These results show specific domains in which impairment is critical and supplies

28 (26.7%) 17 (16.3%) 77 (73.3%) 87 (83.7%) 0.090 Table 3 Psychiatric and clinical medication and comorbidities in the BD sample.

32 (30.5%) 34 (32.7%) 49 (46.7%) 58 (55.8%) 24 (22.9%) 12 (11.5%) 0.000 28 (26.7%) 83 (79.8%) 77 (73.3%) 21 (20.2%) 0.812 67 (63.8%) 68 (65.4%) 38 (36.2%) 36 (34.6%)

regular occupation, while 79.8% of the control group had an active regular labor status. Groups also did not differ significantly in the majority of the clinical variables evaluated but they differed in current alcohol consumption style (0.000) and use of tobacco (p = 0.000). Of those who have existing beverage habits, the BD group had a 40.0% rate for abusive consumption compared with 0% for the control group. Interestingly, the rates for current alcohol consumption were higher in the control group than in the BD group (47% versus 40%), although they did not reach statistical significance. Tables 2 and 3 show relevant data regarding clinical variables of the BD sample. Variables such as number of

Medications and comorbidities Psychiatric medication Lithium Anticonvulsants Atypical Typical Benzodiazepines Antidepressant Stimulants Most frequent clinical medication Antihypertensives Thyroid hormone Hypoglycemiants Axis I psychiatric comorbidities Generalized anxiety disorder Panic disorder Eating disorders Posttraumatic stress disorder Obsessive compulsive disorder Most frequent medical conditions Systemic hypertension Hypothiroidism Diabetes

N (105)

%

50/105 78/105 36/105 35/105 64/105 34/105 0/105

47.619 74.285 34.285 33.333 60.952 32.380 0

34/105 16/105 10/105

32.380 15.238 9.523

28/105 16/105 5/105 2/105 1/105

26.666 17.977 4.761 1.941 0.952

34/105 16/105 10/105

32.380 15.238 9.523

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Table 4 Global score and the seven subcomponents of the PSQI in the two groups. Sleep assessment Global PSQI-BR score Good sleep quality (PSQI-BR ≤ 5) Poor sleep quality (PSQI-BR N 5) Subjective sleep quality Good/Very good Poor/Very poor Sleep latency Normal Disrupted Sleep duration ≤7h N7h Sleep efficiency Normal Disrupted Sleep disturbances Normal Disrupted Use of sleep medication Yes No Daytime dysfunction Normal Disrupted

Bipolar (n = 105)

Controls (n = 104)

p-Value 0.000

18 (17.1%) 87 (82.9%)

82 (78.8%) 22 (21.2%)

50 (47.6%) 55 (52.4%)

88 (84.6%) 16 (15.4%)

12 (11.4%) 93 (88.6%)

61 (58.7%) 43 (41.3%)

57 (54.3%) 48 (45.7%)

52 (50.0%) 52 (50.0%)

41 (39.0%) 64 (61.0%)

79 (76.0%) 25 (24.0%)

6 (5.7%) 99 (94.3%)

13 (12.5%) 91 (87.5%)

0.000

0.000

0.535

0.000

0.088

0.000 82 (78.1%) 0 (0.0%) 23 (21.9%) 104 (100%) 17 (16.2%) 88 (83.8%)

44 (42.3%) 0.000 60 (57.7%)

clinicians and researchers with more insightful understanding of sleep profiles during the euthymic phase of the disorder. Sleep duration subcomponent showed comparable results in the two groups (p = 0.535), even though BD patients had significant disruptions in sleep latency (p = 0.000) and sleep efficiency (p = 0.000). The subcomponent sleep disturbance was not able to distinguish the two groups in the extent that both displayed important impairments (BD group: 94.3 % versus control group: 87.5 %) (p = 0.088). Nevertheless, BD patients had higher rates of sleep disturbances compared to controls.

4. Discussion We were able to show that BD patients even in euthymic phase exhibit a significantly worse sleep quality as compared with health controls as assessed by PSQI-BR total score and five of its seven subcomponents. These results are in agreement with previous studies [38,39], but here we studied a larger sample and we also assessed a health control group matched by many sociodemographic variables. Furthermore, we investigated whether some known risk factors for sleep disturbances, such as clinical medical conditions, could potentially explain the results since it has been previously reported that BD is associated with significant chronic medical burden [40], which could potentially impact sleep function. With regard to the control of confounding factors, the two groups were similar for most of the demographic and clinical data

assessed in the study, with the exception of the variables current alcohol consumption style and use of tobacco. While it is well established that sleep disturbances are common features during manic and depressive episodes of the disorder, it is now starting to become clear that sleep dysfunction are also common features in the interepisodic phase of BD. This fact itself has enormous implications for discussions regarding diagnosis, physiopathology and the treatment of BD. It also confirms the poor prognosis associated with BD and the extent to which these patients display significant subsyndromal symptomatology even in the absence of a current major mood episode. Moreover, it directly provides strength to the understanding of some researchers that sleep behaves both as a trait and as a state feature in BD. Although sleep quality is considered a valid and widespread clinical construct, it is a subjective phenomenon of difficult precise measurement [41]. However, subjective perception of sleep quality correlates with objective findings from sleep laboratory exams such as actigraphy and polysomnography, the gold standard measure of sleep function [42], and this result has been replicated in some posterior studies [43,44]. The instrument we used, PSQI, has been largely used both in clinical and research settings for different groups of patients, including those with psychiatric disorders, primary sleep disorders and even clinical problems such as asthma, oncologic and chronic renal patients [45–47] and has been translated and validated to a variety of languages [35]. The assessment of the subcomponents of the PSQI-BR, even though not standardized by the original validation of the questionnaire, made possible the appreciation of striking new insights concerning sleep parameters of euthymic BD. Despite the fact that sleep duration did not differ between the two groups (p = 0.535), the subcomponents sleep latency (p = 0.000) and sleep efficiency (p = 0.000) were significantly different between the BD and the control groups. These results should be replicated in other samples, but still, they open new possibilities for researchers to understand and study the reasons for the finding of altered sleep latency and efficiency in the presence of usual sleep duration. One possible and promptly logical inference would be to suppose that BD patients spend more time in bed. In other words, BD patients would spend more hours from the minute they go to bed until the moment they rise definitely to life, but with less actually sleeping time. In fact, an actigraphic study involving a sample of euthymic BD which had also a control group point toward this same direction [31]. Other possible factor that would influence these results was the large number of BD patients who were unemployed, which could made needless for the patients an inflexible sleep schedule routine, and would in turn possibly affect the differences observed in sleep patterns between the two groups. In future studies, it would be interesting to build a sample of BD patients who are working in a regular basis. However, other bias could emerge since this group would

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probably be a less severe BD sample in view of the fact that working performance is intact. Our study has some limitations that need to be considered. First, sleep is a complex and multidetermined variable. Thus, we managed to control, as much as possible, for confounding factors, even though it is impracticable to guarantee perfect outcome in such a complicated task. Besides, sleep was evaluated by a questionnaire that assesses a 30-day period. Thus, it is not possible to throw aside a memory bias. Second, another important confounding factor that was assessed is the number of medical clinical conditions. This procedure showed adequacy since the groups did not differ significantly as regards to the number of medical conditions. However, this procedure does not assess the severity of the medical conditions. Additionally, it is impossible to control for all the medical conditions that would affect sleep. Third, we cannot exclude the influence of psychiatric medication on sleep patterns of the BD group. Nonetheless, it would be unfeasible and even unethical to create a BD group free of psychiatric medications. Moreover, the results of such an artificial group would not provide any significant insights of relevant utility in clinical BD samples. Still more, since these patients were not followed sequentially, it is not possible to reject the influence of potential future mood episodes in sleep patterns assessed by the time of the evaluation. This study should be replicated in larger samples to gain more reliability and thus, possibly influence psychiatrist's decision making while treating BD during the interepisodic phase. Also, it opens new and interesting fields for investigations, such as the similarities and differences of sleep patterns while BD patients run into mania and depression and go back into the interepisodic phases. In addition, it would be of interest to understand if there are significant differences in sleep patterns when comparing a group of BDI and BDII. Although the considered limitations that need to be taken into account, the results of the study add supplementary information to the preliminary evidences of the scientific literature of impaired sleep quality in euthymic BD.

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