Original Paper Received: January 15, 2013 Accepted: August 25, 2013 Published online: January 21, 2014

Eur Neurol 2014;71:115–119 DOI: 10.1159/000355277

A Polysomnographic and Clinical Study of Sleep Disorders in Patients with Behçet and Neuro-Behçet Syndrome Uğur Uygunoğlu Gulcin Benbir Sabahattin Saip Hakan Kaynak Aksel Siva  Department of Neurology, Cerrahpasa Faculty of Medicine, Istanbul University, Istanbul, Turkey

Key Words Neuro-Behçet syndrome · Behçet syndrome · Quality of sleep

Abstract Brainstem is the most common site of involvement in neuroBehçet syndrome (NBS). On the other hand, the critical importance of this anatomical region in the regulation of sleep has been disregarded in the literature. We aimed to investigate the microstructure of sleep in patients with Behçet syndrome (BS) and NBS. Patients were allocated to 2 groups: (1) BS without any neurological involvement and (2) NBS with brainstem lesions only. A control group was also enrolled in this study. The comparison of polysomnographic parameters between all patients (BS and NBS) with the control group showed that sleep onset was longer (p = 0.006), the duration of superficial NREM sleep stage (N2) was significantly longer (p = 0.018), and the respiratory disturbance index was significantly higher (p = 0.034) in patients. Sleep apnea and restless legs syndrome are more commonly observed in BS and NBS. Our findings emphasize the importance of questioning the quality of sleep and its disorders in patients with BS in order to better handle the common somatic complaints in these patients, such as fatigue or daytime sleepiness. © 2014 S. Karger AG, Basel

© 2014 S. Karger AG, Basel 0014–3022/14/0714–0115$38.00/0 E-Mail [email protected] www.karger.com/ene

Introduction

Behçet syndrome (BS) is a heterogeneous, relapsing, multisystemic, inflammatory disorder with a chronic course and an unknown cause [1, 2]. It was first defined by a Turkish dermatologist, Hulusi Behçet, in 1937 [3]. It is a relatively rare condition, with the highest prevalence in countries along the ancient Silk Road, but it has a worldwide distribution [4]. Although the underlying etiopathogenesis is not clearly understood, it is characterized by the predominant histopathological feature of vasculitis, involving veins and arteries of distinct sizes [1]. A genetic susceptibility was shown, namely that the presence of human leukocyte antigen B51 allele on chromosome 6p21 was more common in patients with BS [5, 6]. Clinically, the hallmark characteristics of the disease are recurrent oral and genital aphthous ulcers and relapsing uveitis [2]. One of the most devastating presentations of BS is the involvement of the nervous system. The involvement of the central nervous system (CNS) in BS was first reported by Knapp et al. [7] in 1941 and named neuro-Behçet syndrome (NBS) by Cavara and D’ermo [8] in 1954. Neurological involvement in BS was reported to vary between 3 and 25%, and pathological studies performed in autopsied patients showed that 20% of patients with BS had neurological involvement [9–13]. In a study in our center, NBS was found to affect 13% of male and 5.6% of female patients of a total of 387 patients Uğur Uygunoğlu, MD Department of Neurology Cerrahpasa Faculty of Medicine, Istanbul University TR–34098 Istanbul (Turkey) E-Mail uuygun1903 @ yahoo.com

with BS [9]. The male preponderance (2- to 8-fold) was also observed in some other studies [14]. The mortality and morbidity ratios were reported to be higher in male patients with NBS [9]. NBS was divided into two main categories, parenchymal and nonparenchymal involvement [15, 16]. Parenchymal NBS usually has a polyphasic and progressive course, while nonparenchymal NBS, such as cerebral venous thrombosis, rarely relapses [15]. Histopathologically, parenchymal lesions represent inflammatory cellular infiltration of mononuclear cells around small vessels with gliosis and atrophy in chronic lesions [17]. Multiple areas of CNS could be affected in NBS, the most common site of involvement being the brainstem [18, 19]. Coban et al. [20] reported that large confluent brainstem and/or basal ganglia lesions were both sensitive and specific for the diagnosis of acute NBS. Early brainstem atrophy, especially asymmetrical involvement, was also proposed as a valuable diagnostic finding for NBS [21]. The most common imaging findings include large lesions in the brainstem or basal ganglia, extending to the diencephalon, which are observed as hypointense lesions in T1weigthed magnetic resonance imaging (MRI) and as hyperintense signal abnormality in T2-weigthed MRI [22]. These lesions were hypothesized to be secondary to microhemorrhages and edema caused by multiple thromboses in venules and small veins [23]. The most common clinical presentation of NBS is the brainstem syndrome, as it is the most common site for CNS involvement. The symptoms include pyramidal findings, facial palsy, nystagmus, ophthalmoplegia, ataxia, and palatal myoclonus [24, 25]. Sphincter disturbance, cognitive impairment, symptoms of raised intracranial pressure due to dural sinus occlusion, and very rarely, arterial stroke syndromes were also reported [2, 24, 26]. On the other hand, the critical importance of this anatomical region in the regulation of sleep has been disregarded in the literature. In this study, we aimed to investigate the microstructure of sleep and sleep disorders in patients with BS and NBS. Methods We evaluated all patients followed up in our neurology outpatient clinic with the diagnosis of BS for 5 months. The diagnosis of BS and NBS was made according to the International Diagnostic Criteria of Behçet’s Disease [27–29]. All patients had a full systematic and neurological examination in addition to cranial MRI. On the basis of these findings, patients were allocated to 2 groups: (1) BS without any neurological involvement and (2) NBS with brainstem lesions only. Other patients with different types of neurological involvement, such as deep venous thrombosis, were all ex-

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Eur Neurol 2014;71:115–119 DOI: 10.1159/000355277

cluded. A control group including age- and gender-matched healthy subjects was also enrolled in this study. All participants had a whole-night polysomnographic (PSG) recording performed in our sleep laboratory on the Embla a10 system (Flaga, Reykjavik, Iceland). Sleep was recorded and scored according to the American Academy of Sleep Medicine (AASM) Manual for the Scoring of Sleep and Associated Events [30]. 16-channel EEG recordings were used in PSG montage, and electrode placement was performed according the 10–20 system. Other PSG montages included a left and right electrooculogram, chin electromyogram, left and right tibialis anterior electromyogram, electrocardiogram, nasal pressure, oronasal thermistor, thoracal and abdominal strain gauges, pulse oxymetry, and synchronized video recording. All recordings started at the subjects’ usual bedtime and continued until spontaneous awakening. The following conventional sleep parameters were evaluated: time in bed, total sleep time (TST), total NREM/REM time, sleep onset latency, sleep efficiency, wakefulness after sleep onset, duration and percentage of wakefulness, and sleep stages N1, N2, N3 and REM, mean oxygen saturation in wakefulness and sleep, minimum oxygen saturation in sleep, mean heart rate in sleep, respiratory disturbance index (RDI, the sum of apneas, hypopneas and respiratory effortrelated arousals/TST), and periodic leg movement (PLM) index (number of PLM/TST). Clinically, in addition to full systemic and neurological examination, subjective sleep quality was evaluated by Pittsburgh Sleep Quality Test (PSQT), and daytime excessive sleepiness was tested by Epworth Sleepiness Scale (ESS). The presence of restless legs syndrome (RLS) was clinically assessed, and the diagnosis was made on the basis of criteria defined by the International Restless Legs Syndrome Study Group [31]. In comparison with nominal parameters, the Pearson χ2 test was used, and the Mann-Whitney U test was used in comparison with nonparametric parameters. The Kruskal-Wallis test, one-way ANOVA with post hoc Tukey analysis, and Bonferroni correction test were performed in comparison and correlation analysis of parametric values. The threshold level for statistical significance was established at p ≤ 0.05.

Results

A total of 16 patients with BS and 14 patients with NBS and brainstem lesions were included in this study. Patients with NBS were younger than those with BS, though not significantly so (table 1). The gender of the 2 groups of patients, however, was significantly different: males were more commonly affected in the NBS group, while females were more common among patients with BD (p = 0.015; table 1). Body mass index was also similar between the 2 groups. All patients with NBS were under azathioprine treatment. Of all patients, 6 patients were under treatment with azathioprine, 9 patients received colchicine, 2 patients received prednisolone, and 9 patients had a combined treatment with azathioprine together with colchicine and/or prednisolone. Only 4 paUygunoğlu/Benbir/Saip/Kaynak/Siva

Table 1. Comparison of clinical and PSG parameters between patients with BS, patients with NBS, and control subjects

Variables

Clinical variables Age, years Males/females, % BMI Smoking, n (%) ESS PSQT RLS, n (%) History of depression, n (%) PSG variables TIB, min TST, min WASO, min SO, min SE, % N1, % N2, % N3, % REM, % RDI Central apnea index Mean SO2, % Minimum SO2, % PLM index

Patients with BS without neurological complications (n = 16)

40.2+9.5 29.4/70.6 25.4+5.0 3 (17.6) 3.1+2.0 7.9+4.4 7 (41.2) 3 (17.6) 417.1+28.4 350.4+30.4 41.6+25.6 19.3+17.9 84.2+6.2 5.8+2.1 53.9+10.1 23.7+8.8 16.6+6.4 8.6+13.3 0.6+0.4 96.9+1.1 90.5+4.6 7.1+9.5

Patients with NBS (n = 14)

36.1+7.9 76.5/23.5 24.4+4.6 7 (41.2) 2.9+1.8 6.1+4.0 4 (23.5) 1 (5.9) 416.6+44.2 320.8+66.4 65.5+52.4 26.9+20.3 77.1+13.1 6.5+4.2 53.9+12.8 25.0+10.6 12.8+6.5 5.2+7.9 1.2+0.8 96.4+1.2 89.5+6.6 9.3+22.1

p value (between patients with BS and NBS)

0.359 0.015 0.819 0.138 0.381 0.339 0.394 0.224 0.999 0.285 0.282 0.343 0.178 0.916 1.000 0.921 0.322 0.631 0.680 0.885 0.841 0.913

Control group (n = 44)

35.4+8.7 41.7/58.3 26.5+5.6 14 (31.8) 2.1+1.3 6.9+1.7 5 (11.4) 3/6.8 410.5+47.8 331.2+59.8 56.4+48.6 13.4+12.5 80.8+12.3 5.8+6.6 46.4+11.7 24.5+10.0 14.9+8.5 3.1+4.5 2.0+1.1 96.6+4.3 92.1+3.5 12.3+14.0

p value (between control group and all patients) 0.230 0.401 0.233 0.241 0.275 0.454 0.040 0.688 0.618 0.880 0.786 0.006 0.668 0.066 0.018 0.625 0.821 0.034 0.268 0.227 0.156 0.067

Unless otherwise indicated values represent mean + SD. Values in bold represent statistical significance. RDI is the sum of obstructive hypopnea, obstructive apnea, and respiratory effort-related arousals. BMI = Body mass index; TIB = time in bed; WASO = wakefulness after sleep onset; SO = sleep onset; SE = sleep efficiency; N1–N3 = sleep stages.

tients with BS without neurological involvement had no treatment. The PSG parameters of these 2 groups are given in table 1. None of the PSG parameters displayed significant differences between patients with BS and NBS. In addition, the comparison of the PSG parameters of each group with those of healthy controls did not reveal any significant differences either. On the other hand, the comparison of the PSG parameters in all patients (BS and NBS) with the control group did show that sleep onset was significantly longer (p = 0.006), the duration of superficial NREM sleep stage (N2) was significantly longer (p  = 0.018), and RDI was significantly higher (p = 0.034) in patients (table 1). The RDI was lower than 5/h in 20 patients; RDI was between 5 and 14/h in 8 patients, and only 2 patients had an RDI higher than 15/h. These 2 patients with severe obstructive sleep apnea syndrome were later sent to the sleep center of our university for appropriate

treatment. The Pittsburgh Sleep Quality Test and the Epworth Sleepiness Scale were not different between the 2 groups of patients, or between patients and controls. On the other hand, the presence of RLS was significantly more common in patients with BS and NBS compared to healthy subjects (p = 0.040; table 1). In particular, the parameters regarding the REM sleep stage were analyzed in this study population, since only NBS patients with brainstem involvement were enrolled in the study. However, the latency for REM sleep onset, duration and the percentage of REM sleep stage did not show any significant differences between patients with BS, patients with NBS, and healthy subjects (p  > 0.05). Moreover, we also analyzed the RDI in REM sleep and the PLM in sleep index in REM sleep, which were similar in the 2 patient groups and controls as well (p > 0.05). None of the participants – patients with BS, NBS, or controls – had REM without atonia.

Sleep and Behçet Syndrome

Eur Neurol 2014;71:115–119 DOI: 10.1159/000355277

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Discussion

Here we analyzed the microstructure of sleep and sleep disorders in patients with BS and found that PSG parameters did not reveal any significant differences between patients with BS with or without brainstem involvement. On the other hand, the mean sleep onset was delayed in all patients with BS compared to the control group, and the mean duration of the superficial NREM sleep stage was increased, which indicated a worse objective sleep quality in the patient group. RDI was also significantly higher in patients with BS (with or without brainstem involvement). Moreover, RLS was also more commonly present in patients with BS. In particular, the parameters regarding the REM sleep stage were analyzed in this study population, as NBS patients only with brainstem involvement were enrolled in the study. However, we failed to demonstrate any differences in PSG parameters of the REM sleep stage, including latency for REM sleep onset, duration and percentage of REM sleep stage, RDI, and PLM in sleep indices in REM sleep. None of the patients with BS or NBS had REM without atonia. Parenchymal lesions observed in NBS were reported to represent inflammatory cellular infiltration of mononuclear cells around small vessels with gliosis and atrophy in chronic lesions [17]. In addition, these lesions were also found to be consistent with vasculitis in autopsy specimens [32]. Radiologic studies supported this finding, showing significant perilesional edema with a tendency to disappear or to leave disproportionally small residue on follow-up studies consistent with venous infarction [33]. This probable inflammatory-venous pathogenesis for the CNS lesions seen in BS might prevent neuronal damage at the molecular level and lead to preservation of REM-related pathologies in spite of brainstem involvement. Nevertheless, these findings should further be investigated in larger study populations, with detailed neuroimaging analysis with more specific localizations within the brainstem. The effects of BS on sleep have not attracted much interest in the literature. The anatomical importance of brainstem involvement in neurological disorders such as cerebrovascular events or multiple system atrophy, however, has been pointed out previously [34]. It was proposed that the direct involvement of the medullary respiratory neurons that affect the pattern and generation mechanism may induce sleep apnea in these patients [34]. The involvement of respiratory and nonrespiratory motor neurons in the brainstem such as ambiguous nucleus and hypoglossal nucleus was also thought to be responsible for the increased prevalence of sleep apnea in patients with brain118

Eur Neurol 2014;71:115–119 DOI: 10.1159/000355277

stem disorders. Recently, it has been shown that obstructive sleep apnea and accompanying central apneas were more common among patients with MS, particularly those with brainstem involvement, compared to healthy controls [35]. In addition, 1 patient with NBS was reported to present with palatal myoclonus and sleep apnea [25]. In our study, we demonstrated an increase in the presence of sleep apnea in patients with BS, whether there was brainstem involvement or not. Moreover, RLS was also more common in patients with BD. The mesocorticolimbic dopaminergic system plays a crucial part in the regulation of sleep, and pathologies regarding this system were suggested to be responsible for disturbed sleep or sleep disorders such as RLS [36]. Although brainstem involvement did not reveal significant differences in terms of the RDI or PLM index in our study population with BS, a larger population may better reflect the effects of brainstem involvement in this group of patients. Very recently, Tascilar et al. [37] have reported 51 patients with BS without any neurological involvement and found that sleep-related breathing or movement disorders were more prevalent in these patients compared to healthy controls. The authors have similarly pointed out the importance of sleep disorders as regards the quality of life of patients with Behçet disease. We conclude that the quality of sleep is reduced in patients with BS, and sleep disorders, such as sleep apnea and RLS, are more commonly observed in this group of patients. Our findings emphasize the importance of enquiring about the quality of sleep and its disorders in patients with Behçet disease in order to be able to better handle the common somatic complaints in these patients, such as fatigue or daytime sleepiness. On the other hand, an etiopathogenetic explanation regarding a causal relationship could not be made in this cross-sectional study; for this we suggest prospective longitudinal studies in larger populations of patients with BS and NBS.

Disclosure Statement Dr. Ugur Uygunoglu reports receiving travel and registration coverage for attending several national or international congresses or symposia, from Merck Serono, Biogen Idec, Novartis and Allergan. Dr. Gulcin Benbir has no disclosures. Dr. Sabahattin Saip reports receiving research grants from The Scientific and Technological Research Council Of Turkey – Health Sciences Research Grants numbers: 109S070 and 112S052; and also unrestricted research grants from Bayer-Schering AG and from Merck-Serono. Dr Saip also reports receiving travel and registration coverage for attending several national or international congresses or symposia, from Merck Serono, Novartis and Teva. Dr. Hakan Kaynak has no disclosures.

Uygunoğlu/Benbir/Saip/Kaynak/Siva

Dr. Aksel Siva reports receiving research grants to his department and clinical neuroimmunology unit from The Scientific and Technological Research Council Of Turkey – Health Sciences Research Grants numbers: 109S070 and 112S052; and also unrestricted research grants from Bayer-Schering AG and from Merck-

Serono. Dr Siva also reports receiving honoraria or consultation fees Biogen Idec, Allergan, Novartis. He had received travel and registration coverage for attending several national or international congresses or symposia, from Merck Serono, Biogen Idec, Novartis, Teva, Bayer-Schering and Allergan.

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A polysomnographic and clinical study of sleep disorders in patients with Behçet and neuro-Behçet syndrome.

Brainstem is the most common site of involvement in neuro-Behçet syndrome (NBS). On the other hand, the critical importance of this anatomical region ...
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