The polysomnographic characteristics of REM sleep behavior

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1 ORIGINAL ARTICLE Quantification of Tonic and Phasic Muscle Activity in REM Sleep Behavior Disorder Geert Mayer,* Karl Kesper, Thomas Ploch, Sebastian Canisius, Thomas Penzel, Wolfgang Oertel, and Karin Stiasny-Kolster Summary: REM sleep behavior disorder (RBD) is characterized by excessive tone of the chin muscle and limb movement during sleep. In the past, quantification of increased muscle tone in REM sleep has been performed visually, using no stringent criteria. The aim of this study was to develop an automatic analysis, allowing the quantification of muscle activity and its amplitude for all sleep stages, with a focus on REM sleep in patients with RBD. Forty-eight patients (27 male, 21 female) with RBD were included in the analysis. Twentyone had idiopathic RBD; 28 had narcolepsy plus RBD. Twenty-five patients without confirmed sleep disorder served as control subjects. The amplitude of the EMG was generated from the difference of the upper and lower envelope of the mentalis muscle recordings. By smoothing the amplitude curve, a threshold curve was defined. Any muscle activity beyond the threshold curve was defined as motor activity. The means of the motor activity per second were summarized statistically and calculated for each sleep stage. Due to variable distribution of REM sleep, the latter was assigned to respective quartiles of the recorded night. Muscle activity was defined according to a histogram as short-lasting ( 0.5 second) and long-lasting ( 0.5 second) activity. No difference in the distribution of REM sleep/quartile and mean muscle tone throughout the sleep cycle could be found within the RBD groups and control subjects. Muscle activity was in the range of 200 ms. No clusters or regular distribution of muscle activity were found. Long muscle activity in the group with manifest clinical RBD was significantly higher than in control subjects, whereas it was nonsignificantly higher in subclinical RBD. The correlation between the frequency of long muscle activity in REM sleep and age was highly significant only for patients with idiopathic RBD. Automatic analysis of muscle activity in sleep is a reliable, easy method that may easily be used in the evaluation for REM sleep behavior disorder, creating indices of muscle activity similar to the indices for sleep apnea or PLMS. Together with the overt behavior, the analyses provides an important tool to get a deeper insight into the pathophysiology of RBD. Long movements appear to represent the motor disinhibition in REM *Department of Neurology, Hephata Klinik, Schwalmstadt-Treysa, Germany; Sleep Laboratory, Department of Internal Medicine, Philipps- University of Marburg, Germany; Department of Sleep Medicine, Charite, University of Berlin; and Department of Neurology, Center of Nervous Diseases, Philipps-University of Marburg, Germany. Address correspondence and reprint requests to Prof. Dr. Med. Geert Mayer, Hephata Klinik, Department of Neurology, Schwalmstadt-Treysa, Germany; geert.mayer@hephata.com. Copyright 2008 by the American Clinical Neurophysiology Society ISSN: /08/ sleep more distinct than short movements. The positive correlation of age and increased motor activity in REM sleep in idiopathic RBD highlights the idea of age dependant motor disinhibition as a continuum of a neurodegenerative disorder, which in narcolepsy patients with RBD only seems to happen as a single temporal event at onset of the disorder. Key Words: REM sleep behavior disorder, Muscle tone, EMG m. mentalis, Automatic EMG analysis, Age, Narcolepsy. (J Clin Neurophysiol 2008;25: 48 55) The polysomnographic characteristics of REM sleep behavior disorder (RBD) are excessive muscle tone of the chin muscle and limb movement during REM sleep (American Academy of Sleep Medicine, ICSD 2, 2005). As RBD is a predictor for neurodegenerative disorders (Arnulf, 2005; Boeve, 2001; Boeve, 2003; Plazzi, 1997; Schenck, 2003; Mahowald and Schenck, 2004; Iranzo et al., 2005; Lai and Siegel, 2003; Olson et al., 2000; Schenck et al., 1996) and frequently occurs in narcolepsy (Mayer, 2002; Nightingale 2005; Schenck, 1992), it is of importance to quantify the disinhibition of REM muscle atonia, to distinguish it from REM atonia in other sleep disorders and in healthy subjects. Several quantification methods have been proposed that are based on different assumptions, undefined EMG characteristics, and that have studied few patients only (Bliwise, 2006; Eisensehr, 2000; Ferini Strambi, 2004; Lapierre, 1992; Mahowald, 2004). Most methods used visual scoring, which is time consuming. A major problem in scoring muscle activity in REM sleep is the complete lack of definition of what is pathologic. Another problem is the definition of tonic and phasic muscle activity in the literature. The general definition of tonic periods of REM sleep is complete atonia (active postsynaptic inhibition of motoneurons, hyperpolarization of membrane potential); that of phasic periods of REM sleep is myoclonic twitches (repetitive depolarizations of motoneurons). Muscle activity in REM sleep has been defined 15 years ago and is still being used with modifications (Consens et al., 2005; Lapierre et al., 1992). The definition for tonic muscle activity is long-lasting activity accompanied by complex movement: 20 to 30 seconds of REM sleep epochs with abnormally elevated background activity for 50% of the epoch. The definition for phasic activity is: presenting motor activity in the range of twitches: 2 seconds of mini epochs with bursts of EMG 48 Journal of Clinical Neurophysiology Volume 25, Number 1, February 2008

2 Journal of Clinical Neurophysiology Volume 25, Number 1, February 2008 Quantification of Muscle Activity in REM SBD TABLE 1. Demographic Data of the Study Population (Based on Exclusion Criteria of Automatic Analysis) All RBD Patients Mean SD IRBD Mean SD nrbd Mean SD Controls Mean SD Age (years) Duration of RBD (years) Body mass index activity. This definition does not define a clear temporal distinction of both activities. In analogy to the definition of the periodic limb movement disorder, which is quite prevalent in RBD patients, Eisensehr et al. (2003) defined short- and long-lasting muscle activity as below and beyond 0.5 second. The different approaches to study muscle activity in REM sleep make it difficult to compare the results of past and future studies. Therefore, the aim of our study was to develop an automatic analysis that would allow the quantification of muscle activity and its amplitude throughout all sleep phases, of tonic and phasic muscle activity in REM sleep, to analyze the periodicity of long and short muscle activity in REM sleep, to compare subclinical and clinical forms of RBD, and to find cutoff scores that distinguish between RBD and other disorders (Mayer et al., 2006). These findings would then be related to the direct video-based observation of RBD. PATIENTS AND METHODS We studied 62 consecutive patients evaluated for sleep disorders (33 men, 29 women) diagnosed with RBD (confirmed by clinical, videometric, and polysomnographic criteria according ICSD-2). All patients had at least one polysomnography. All patients with RBD had UPDRS III, olfactory testing, MMSE; 13 had FP-CIT SPECT (for details, see Stiasny-Kolster et al., 2005). None of the patients consumed antidepressants or stimulants. Thirty-four patients had clear-cut narcolepsy with cataplexy and RBD (nrbd) (16 men, 18 women), 28 patients had idiopathic RBD (irbd) (17 men, 11 women). Twenty-five control patients (CO) (16 men, 6 women) scored for sleep apnea had simple snoring without any obstructive component in their polysomnographies and served as control subjects. Due to the exclusion criteria of the automatic analysis of muscle activity (see below), the number of patients included was reduced to 48 (27 men, 21 women). For demographics, see Table 1 and Fig. 1. Behavior during REM sleep was scored as no event, minor (small, short movements of one limb), mild (complex, repetitive movements of more than one limb or the head), and severe (kicking, punching, falling out of bed). In the irbd group, 2 patients had severe, 6 mild, 11 minor, and 2 patients no observed behavior. In the nrbd group, 6 patients had mild, 15 minor, and 6 patients no observed behavior. Olfaction was impaired in 96.1% of all RBD patients; none of the patients had cognitive impairment in the MMSE, 7 patients in the irbd group had mild motor impairment in the UPDRS III, and 5 irbd patients had abnormal FP-CIT scans (for details see Stiasny-Kolster et al., 2005). All polysomnographic recordings were performed with the Sagura system (Sagura Polysomnograph 2000, Sagura Medizintechnik GmbH; Mühlheim, Germany) including EMG of the chin muscle (bipolar) and both legs. Sixteen recordings of RBD patients were performed with electrodes of both biceps muscles. All EMG recordings had the same calibration and filters (sampling rate, 200 Hz; amplification, 200 mv; filter, 120 Hz; time constant, 0.03). The patients scored for sleep apnea had a standard cardiorespiratory polysomnography with recordings of both tibialis muscles. The EMG analysis applied for the EMG of m. mentalis exclusively was developed by K. Kesper. Because amplitude 10 8 Age nrbd irbd controls 6 N > 0-10 > > > > > Age / years > > > > FIGURE 1. Age distribution of 48 patients. Copyright 2008 by the American Clinical Neurophysiology Society 49

3 Mayer et at. Journal of Clinical Neurophysiology Volume 25, Number 1, February 2008 FIGURE 2. Analysis of chin EMG with smoothing procedure. criteria in past publications (Consens et al., 2005; Lapierre, 1992) is missing for tonic muscle activity, it was defined as the basic level of EMG that can be measured in a phase without clear cut EMG activation as an amplitude. The amplitude of EMG was generated from the difference of the upper and lower envelope (smoothing over 5 samples, second) (Fig. 2). A threshold curve was defined by smoothing of the amplitude curve over 200 seconds (40,000 samples), which was multiplied by factor 2 for REM sleep according to the definition that EMG during phasic activation in REM sleep should have at least twice the baseline amplitude (Eisensehr, 2003) (Fig. 3). Muscle activity was defined as lying beyond the threshold curve. Clusters of muscle activity at a distance of 1 second were defined as one event taking into account an increase of frequency of long muscle activity. From the amplitude curve a 50 mean was calculated for each second (mean muscle tone, sample rate: 1 Hz). Short activations were smoothed out by the means per second, whereas longer activations resulted in few elevated means per second, which did not interfere with statistics; 50-Hz intrusions from the current voltage were removed before analysis by an effective digital filter. The visually scored sleep profiles were then included into the analysis. REM phases in short distance of 10 epochs apart were scored as one phase to abstain from highly fragmented REM sleep. The means per second for each PSG were summarized statistically (mean, standard deviation, number) and calculated for each sleep stage (unclassified, wake, NREM1-4, REM, movement time). The data were exported into separate files for the calculation of stage-specific tone characteristics (mean values, standard deviation) and sleep stage related histograms of muscle activity from 0 to 200 mv. Copyright 2008 by the American Clinical Neurophysiology Society

4 Journal of Clinical Neurophysiology Volume 25, Number 1, February 2008 Quantification of Muscle Activity in REM SBD FIGURE 3. activity. Threshold for muscle For technical reasons some exclusion criteria had to be defined: If a single sleep section did not contain at least 300 seconds (5 minutes), because muscle tone of these short sleep stages are mainly characterized by stage transitions and would influence the results. Visual scoring of EMG signal curves identified some recordings with very high muscle activity due to false calibration. Recordings with a mean muscle activity 20 mv in one sleep stage or 10 mv in two sleep stages. PSGs Without Sleep Stage Related Modulation of Amplitude Due to Interference of Amplifier Noise REM sleep in each patient occurred with a different distribution throughout the night. To compare REM sleep between the different patients, we decided to divide the PSG into quartiles and to assign REM sleep to the respective quartile. Muscle activity was discriminated for short ( 0.5 second) and long ( 0.5 second) activity according to the scoring rules of periodic limb movement (Coleman et al., 1982). Statistics All statistical analysis was performed with SPSS for windows. Means and standard deviation of muscle tone per sleep stage were evaluated for each patient from the respective single means from the PSG. Differences were compared by the Mann-Whitney U-test (2 sided). Spearman correlation coefficients were used to evaluate the relation between two variables. 15 Mean stage specific muscle tone nrbd irbd controls Muscle tone / 10 6 Volt ,33 8,11 6,44 5,10 5,91 3,34 4,15 4,29 3,61 3,32 2,44 2,52 3,35 2,78 3,11 3,59 2,11 2,20 0 FIGURE 4. WAKE WACH NREM1 NREM2 NREM3 NREM4 REM Sleep stage Stage specific muscle tone. Copyright 2008 by the American Clinical Neurophysiology Society 51

5 Mayer et at. Journal of Clinical Neurophysiology Volume 25, Number 1, February nrbd movement duration / ms irbd FIGURE 5. Histogram of movement durations. movement duration / ms RESULTS The evaluation of the mean muscle tone during wake and all sleep stages assessed for patients did not show significant differences between irbd, nrbd, and CO patients (Fig. 4). The mean duration of REM sleep/quartile was longer for the first REM period in nrbd patients, as expected. In all other quartiles, the duration of REM did not differ between groups. The mean distribution of REM sleep/quartile did not differ between the groups, either. The histograms for the movement durations showed that the majority of movements lasted about 200 ms. No clustering for certain durations could be seen that would allow identifying a periodicity or peaks with defined length (Fig. 5). The analysis of long and short muscle activity in REM sleep showed a significantly higher amount of long and short 52 muscle activity in irbd and nrbd patients compared with CO patients, whereas it did not differ in between irbd and nrbd patients (Fig. 6). We were further interested to look at the muscle activity patients with clinical and subclinical irbd (no patient with nrbd had subclinical RBD). In these patients, we found a nonsignificantly higher number of long and short muscle activity in clinical and subclinical RBD compared with CO patients. Because our age distribution showed a wide range, we correlated age and frequency of long and short muscle activity per hour REM sleep. There was a highly significant correlation between frequency of long muscle activity in REM sleep and age for irbd, but not for the other patient groups (Table 2). Short muscle activity in the scatterplots shows an increase with age but does not reach significance. Copyright 2008 by the American Clinical Neurophysiology Society

6 Journal of Clinical Neurophysiology Volume 25, Number 1, February 2008 Quantification of Muscle Activity in REM SBD FIGURE 6. Frequency of muscle activity. DISCUSSION To our knowledge, this is the first publication using automatic analysis in the muscle tone/activity of patients with RBD during wake and all sleep stages. Analysis of muscle tone using amplitude criteria throughout wake and all sleep stages did not differ among the 3 groups. Muscle activity decreases from stage NREM 1 to 4 and is lowest in REM sleep. It follows the decay of muscle activity from the beginning to the end of one sleep cycle and from sleep onset to sleep offset (Brunner et al., 1990). Within each sleep cycle, the number of short and long muscle activity during REM sleep increases from the first to the last cycle in all 3 groups. The only significant difference between the RBD groups and control patients is the number of long and short muscle activity during REM sleep. This finding is clearly in favor for a quantitative disinhibition of muscle activity during REM sleep in RBD patients. Looking at the muscle activity/amplitude in REM sleep, the difference between RBD and control patients indicates that a threshold for tonic muscle activity could be in the range of 2.1 to 3 mv. This has to be confirmed and validated in larger samples. Discrimination of RBD from control subjects in REM sleep was much easier to perform than in NREM sleep because short and long muscle activity differed significantly. The results of the automatic analysis cannot be compared with those of Lapierre (1992) and Consens (2005) as their amplitude criteria for tonic muscle activity was not defined. Their choice for tonic muscle activity as any change in muscle activity beyond zero accompanied by complex movement remains vague for several reasons: (1) the semiology of complex movement accompanying muscle activity has not been defined. Since control patients also have increase of muscle activity in REM and thus move- TABLE 2. Correlation of Muscle Activity and Age Short Muscle Activity Index (No./h REM) Long Muscle Activity Index (No./h REM) Percentage of Long Muscle Activity in REM N r P r P r P nrbd irbd Control subjects r correlation coefficient; P significant (2-sided). Copyright 2008 by the American Clinical Neurophysiology Society 53

7 Mayer et at. Journal of Clinical Neurophysiology Volume 25, Number 1, February 2008 ment, what is the specific RBD related movement? (2) Many RBD patients have elevated muscle activity without any related movement. This type of activity would be lost to evaluation. (3) The temporal distribution is not quantitative, but all or nothing. With respect to the latter, the finding of more than 98% of 20-second epochs accompanied by tonic muscle activity (Lapierre, 1992) seems to be unrealistic considering minimal motor activity in most RBD patients (Frauscher, 2005). Our data show that the mean length of short-lasting activity is 0.1 second (the length of twitches), that of long-lasting activity about 2 seconds. Only few major behavioral events lie in the 10-second range (see Fig. 5). Considering the amount of short and long muscle activity in REM sleep, the percentage of muscle activity in REM sleep seems to be below 2%. If the amount of more than 2% of muscle activity in REM sleep could define a new threshold for RBD has to be validated by future studies. Because our population has a broad age range (19 to 81 years), age-related change in muscle activity can clearly be demonstrated. The significant increase of long muscle activity and insignificant increase of short muscle activity in REM in irbd patients with age indicates a progressing disinhibition of muscle activity. For nrbd patients who also show a significantly higher amount of short and long muscle activity in REM there is no correlation with age, indicating that the disinhibition may be a process occurring only at narcolepsy onset. This could imply that the neurodegenerative process in narcolepsy is a single temporal event. Concerning short muscle activity in REM, our data can be compared with the phasic electromyographic metric (PEM) in the range of 100 ms, found by Bliwise et al. (2006) for four different age and patient groups. In his young and elderly group, the amount of PEM did not differ. This finding can be confirmed by our results, nevertheless we can state that in irbd, and thus probably in most of the neurodegenerative disorders with RBD there is an age effect on muscle activity. Our automatic analysis differs completely from the methods used before (Bliwise et al., 2006; Consens, 2005; Lapierre, 1992). Except for the study of Bliwise et al., the other authors did not define the parameters for EMG recordings nor how they excluded artifacts or insufficient recordings. A major problem seems to be that the amplitude criteria differs in most studies. Most authors used amplitudes that exceeded at least 4 times the presleep baseline for phasic muscle activity but did not define if this was in REM or NREM sleep or their transitions. We chose to score amplitudes at twice the baseline of previous REM sleep not to rule out muscle activity that might be relevant for the analysis. However, the threshold still has to be established and evaluated by larger studies. Since our histograms showed that most of the muscle activity was in the range of 200 ms, we decided to adapt the proposal of Eisensehr et al. (2003) for short and long muscle activity with a split at 0.5 second, according to the scoring rules for periodic limb movements (Coleman et al.). This type of scoring allows discriminating short muscle activity such as twitches from continuous long-lasting muscle activity, which goes beyond the criteria of counting activity 54 of mini epochs of 2, 2.5, and 3 ms and of counting 50% of 20- or 30-second epochs containing at least 10 seconds of undefined increased muscle tone as performed in most of the recent analyses (Bliwise et al., 2006; Consens, 2005; Lapierre, 1992). Furthermore, this type of scoring results in indices of short and long muscle activity as internationally used for sleep apnea and RLS. Phasic muscle activity was defined as EMG bursts of 0.1 to 5 seconds, tonic activity as 10 seconds of increased muscle tone with behavioral correlates. This definition was not based on the evaluation of means of amplitude of muscle activity and therefore seems to be voluntary. In comparison, our histograms of muscle activity allow to allocate the frequency of duration of muscle activity and to score activity that is beyond or below the given thresholds. Compared with our results the occurrence of tonic/ phasic chin EMG by Lapierre et al. (1992) seems to be extremely high. If this outcome is dependent on the severity of the symptoms or based on the selection of nights with extremely high muscle tone remains unclear. However, severity of symptoms should be assessed for the recorded nights in the future. Furthermore, scoring of muscle activity in REM sleep without and with motor behavior should be performed. As our population had recordings mainly during a single night for diagnostic purposes, and often revealed RBD for the first time, the results may not be comparable to those of Lapierre et al. However, our study represents a more naturalistic setting, since PSG is a major diagnostic tool in the differential diagnoses of many sleep disorders. To express and underline the quantitative aspect of motor activity in REM, we propose to refer to the duration of motor activity as percent of REM sleep in terms of indices, as it is the rule for sleep apnea and the restless legs syndrome. Referring to epochs and mini epochs is confusing when information about technical parameters of the recordings and the proportions of sleep stages and sleep cycles is not presented in the respective publications. CONCLUSION In our study population we could find amplitude criteria of muscle activity throughout all sleep stages and awake, which may serve for future studies with automatic analysis to define age-related thresholds for each sleep stage in healthy persons. Our automatic analysis allows us to define criteria for short and long muscle activity in terms of amplitude and duration, which seem to be better criteria than phasic and tonic muscle activity. The automatic analysis has to be validated by larger patient and control groups and must be correlated with observed behavior. Automatic analysis is a sensitive tool that helps shortening the difficult, long-lasting manual scoring. It is not problematic in scoring tone of the chin muscle activity but may be problematic in scoring arm and leg muscles as the evaluation of PLM and arousal for the scoring rules must be clarified. REFERENCES American Academy of Sleep Medicine. 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