Sleep Medicine 12 (2011) S59–S63
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Sleep Medicine
journal homepage: www.elsevier.com/locate/sleep
Original Article
Motor events during REM sleep in patients with narcolepsy–cataplexy:
A video-polysomnographic pilot study
Christian Franceschini a,b,⇑, Raffaele Ferri c, Fabio Pizza a, Lara Ricotta a, Stefano Vandi a, Stefania Detto a,
Francesca Poli a, Carlo Pruneti b, Michela Mazzetti d, Carlo Cipolli d, Elio Lugaresi a, Giuseppe Plazzi a
a
Department of Neurological Sciences, University of Bologna, Bologna, Italy
Department of Psychology, University of Parma, Parma, Italy
Department of Neurology, Oasi Institute IRCCS, Troina, Italy
d
Department of Psychology, University of Bologna, Bologna, Italy
b
c
a r t i c l e
i n f o
Article history:
Received 27 September 2011
Received in revised form 11 October 2011
Accepted 12 October 2011
Keywords:
REM sleep behavior disorder
Narcolepsy–cataplexy
Video-PSG recording
Simple and complex motor events
REM sleep
Vocalizations
Dream enactment
a b s t r a c t
Objective: We carried out a systematic video-polysomnographic analysis of the number and type of
motor events during REM sleep in narcolepsy–cataplexy patients with REM sleep behavior disorder
(NC + RBD) but not clinical RBD (NC RBD).
Methods: Twelve NC + RBD and 10 NC RBD male patients underwent video-polysomnography (videoPSG). Motor events of different type and complexity (i.e., elementary and complex movements and vocalizations) occurring during REM sleep were visually assessed, and indices of their frequency per hour of
REM sleep were calculated. Subsequently, the index values were compared in NC + RBD versus NC RBD
patients.
Results: Typical RBD behaviors observed in five NC + RBD patients were not included in any type of motor
events. No objective conventional sleep parameter, including visual analysis of chin electromyographic
(EMG) activity, significantly differed between the two groups of NC patients. NC + RBD patients showed
higher occurrence of elementary movements (p = 0.034) during REM sleep compared with NC RBD
patients, but the occurrence of complex movements did not differ significantly.
Conclusions: Video-analysis of motor events during REM sleep may improve the diagnosis of RBD in NC.
RBD in NC patients is mainly characterized by elementary rather than complex movements, consistent
with the view that RBD with NC patients displays a distinct phenotype with respect to other RBD patients.
Ó 2011 Elsevier B.V. All rights reserved.
1. Introduction
REM sleep behavior disorder (RBD), first described in 1986 by
Schenck et al. [1], is an REM sleep parasomnia characterized by
the lack of physiological muscle atonia during REM sleep (REM
without atonia – RWA) at polysomnography (PSG), and by an intense motor activity leading to potentially harmful dream-enacting
behaviors [1]. These motor manifestations seem to reflect the concomitant dream, by translating some of its contents into motor
behaviors: patients scream, kick and punch, assault their bed partner, fall out of bed, and may cause sleep-related injuries [2]. RBD
episodes may occur in otherwise healthy people (idiopathic RBD),
but also arise or even herald the first signs of disease in a variety
of progressive neurodegenerative conditions (mainly synucleinop-
⇑ Corresponding author. Address: Department of Neurological Sciences, University of Bologna, Via Ugo Foscolo 7, 40123 Bologna, Italy. Tel.: +39 051 2092926; fax:
+39 051 2092963.
E-mail address: [email protected] (C. Franceschini).
1389-9457/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.sleep.2011.10.013
athies, i.e. Parkinson Disease, Multiple System Atrophy, Levy Body
Dementia) [3–6], and in patients with narcolepsy [7–12].
An early description of the PSG features of RBD in narcoleptic
patients was reported in the 1970s as a ‘‘dissociated’’ sleep state,
characterized by the coexistence of electroencephalographic
(EEG) features of REM sleep and the persistence of elevated tonic
chin EMG activity intermingled with bursts of phasic activations
[13]. After the first documented association of RBD and narcolepsy
by Schenck and Mahowald in 1992 [12], several studies confirmed
a fairly high prevalence of RBD in narcoleptic patients [7–12]. The
variations in prevalence rates in these studies seem to depend on
the tools used to assess RBD; in fact, studies based on history taking or questionnaires detected an association widely ranging from
36% to 61%, whereas studies based on video-PSG disclosed that
43.2% of patients with narcolepsy–cataplexy (NC) displayed RBD
[7]. Video-PSG studies have also shown that RBD is not an everynight phenomenon in NC patients [7,14].
An increased chin EMG activity during REM sleep has been previously reported as a common trait in NC since the 1970s [13].
Studies on NC patients using visual scoring techniques
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[11,10,15,16] or computerized analysis tools [17,18] have confirmed an elevated EMG activation during REM sleep, which is also,
albeit slightly, higher in NC patients with RBD [19].
Some other items of evidence suggest that NC patients present
specific clinical and pathophysiological features in control. Indeed,
narcolepsy patients and RBD patients share common polysomnographic abnormalities indicative of impaired motor control during
REM sleep: in particular, they share an increased number of periodic limb movements during sleep (PLMS), especially in REM sleep
[20,8]), and an absence or reduction of physiologic REM sleep muscle atonia [17,11]. Moreover, narcolepsy patients show rhythmic
movements intermingled over a plateau of muscle atonia during
sleep paralysis, and inappropriate occurrence of muscle atonia
and jerking activities accompanying cataplexy attacks during
wakefulness [7]. To account for these features, it has been suggested that they may be due to the underlying hypocretin-1
(hcrt-1) defect, resulting not only in sleep state instability, but also
in unwanted postural atonia during wakefulness and in increased
muscular activity during REM sleep [21,22].
To substantiate this view, a careful and complete classification
and quantification of motor events during REM sleep in narcoleptic
patients is needed. This classification could also lead to the identification of behavioral and PSG indices of motor events capable of
distinguishing NC patients with RBD from those without, even in
the absence of clear RBD episodes. Indeed, RBD occurrence is not
an every-night phenomenon and, therefore, the usual one-night video-PSG recording made to confirm the clinical diagnosis [7,14]
may not capture it.
In this pilot study we therefore examined the PSG and behavioral characteristics of motor events during REM sleep in NC patients with (NC + RBD) and without clinically-documented RBD
(NC RBD). To characterize the behavioral patterns of all the visually detectable motor events, a detailed and comprehensive videoPSG analysis was carried out using a slightly modified version of
the Frauscher and coworkers’ scoring system [23].
2. Materials and methods
2.1. Patients
In the series of NC patients first diagnosed from January to August 2011 at the Sleep Disorders Center, Department of Neurological Sciences, University of Bologna, it was planned that only men
would be selected for the present study. This decision, which was
due to the exploratory aims of the study (and, thus, the need to exclude possible gender-related confounding factors), was based on
the prevalence of men in the population (and also presumable in
our series) of NC patients.
The diagnosis of NC was made in 22 men according to the clinical (i.e., daytime sleepiness, cataplexy) and polysomnographic
(i.e., a 48 h continuous PSG followed by a five nap opportunity
multiple sleep latency test, MSLT) international criteria [2]. Moreover, human leukocyte antigen (HLA) DQB1⁄0602 typing, and,
whenever possible, cerebrospinal fluid (CSF) hcrt-1 measurement
were performed. Subjective sleepiness at the time of the study
was assessed by means of the Italian version of the Epworth Sleepiness Scale (ESS) [24,25].
Among the 22 first-diagnosed patients, a clinical diagnosis of
RBD was posed in 12 patients (NC + RBD) on the basis of the responses to a specific semi-structured questionnaire [26], which
was framed according to the International Classification of Sleep
Disorders 2nd Edition (ICSD-2) [2], and aimed at establishing the
diagnosis of RBD by examining its clinical features over the past
12 months. The questionnaire was focused on the following RBD
characteristics: (i) clinical features: vocalizations, movements of
limbs and body, spontaneous report of dream experience, and re-
port of any specific content of mental experience during sleep;
(ii) duration and overnight distribution of RBD; (iii) frequency of
episodes, and (iv) occurrence of sleep-related injuries.
In addition, NC duration was systematically investigated together with clinical history of the following sleep disorders: nonREM parasomnias (i.e., confusional arousals, sleepwalking, sleep
terrors), sleep-talking, sleep-related bruxism, sleep-enuresis, and
sleep-related eating syndrome [2].
At the time of the study, all NC patients were drug-naïve. The
clinical features of the two subgroups of NC + RBD (n = 12) and
NC RBD patients (n = 10) are reported in Table 1.
The institutional review board of the Department of Neurological Sciences, University of Bologna approved the study project. All
patients signed a written informed consent before the study entry.
2.2. Video-polysomnography
After an adaptation night without video-recording, NC patients
underwent a full night of sleep in – laboratory with video-PSG
recording.
Patients were allowed to be asleep and awake spontaneously,
without any time restriction. The parameters considered for the
PSG recording were: EEG (C3-A2, C4-A1, O2-A1), bilateral electrooculogram (EOG), chin EMG, and electrocardiogram (ECG). The
breathing pattern was monitored through an oro-nasal thermistor,
thoraco-abdominal bands, and a finger pulse oximeter [27]. Patients with an apnea/hypopnea index (AHI) P15 were excluded
[27,2]. PLMS were scored according to the current international
criteria [28], and the PLMS index (PLMI) was computed [28].
The video recording, time-synchronized with the PSG track, was
obtained from an infrared camera (video resolution of 1280 960
pixels). PSG tracks were scored by a sleep expert according to the
criteria of Rechtshaffen and Kales [29]. All the percentages of the
time spent in each sleep stage referred to the total sleep time
(TST), whereas the sleep efficiency referred to the time in bed (TIB).
Moreover, the activation of the chin EMG signal in REM sleep
was evaluated according to the criteria proposed by Lapierre and
Montplaisir in 1992 [30], and Consens et al. [15], in order to obtain
the percentage of the total REM epochs scored as tonic (Tonic REM
30-s epochs%) and to obtain the phasic EMG density (Phasic REM
3-s miniepochs%).
2.3. Definition of motor events
The video classification of motor events in REM sleep was performed according to the classification proposed by Frauscher and
colleagues in 2007 [23]. Accordingly, motor events were classified
considering their complexity (and also considering the parts of the
body involved) as follows:
(a) Elementary:
(i) myoclonic events: events defined as sudden, brief, and
involuntary, and involving the limbs, face or trunk,
(ii) simple events: the single twitch of the fingers, or more
important, a ‘‘body jerk’’.
(b) Complex:
(i) complex events: events that involve multiple muscle
groups at the same time,
(ii) acting out events (i.e., clear-cut RBD episodes),
(iii) aggressive and/or violent movements: motor behaviors in which the patient can potentially hurt or injure
himself and/or the bed partner (e.g., kicking or
punching).
(c) Vocalization:
(i) not associated with visible motor events,
(ii) associated with visible motor events.
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Table 1
Clinical data of patients included in the study.
NC
Age at PSG (yy)
ESS (score)
Age at EDS onset (yy)
Age at cataplexy onset (yy)
Narcolepsy duration (yy)
CSF Hcrt-1 (pg/ml)
Estimate RBD duration (yy)
Hypnagogic hallucinations
Sleep paralysis
HLA DQB1⁄0602 positivity
Confusional arousal, sleepwalking, sleep-terrors
Sleep talking
Sleep-related bruxism
Sleep-enuresis
SRED
RBD
Table 2
PSG data of the two groups of NC patients.
NC + RBD
Mann–
Whitney U
test
Mean
SD
Mean
SD
P-Value
35.9
15.2
22.7
24.5
13.2
20.1
19.0
3.0
9.5
9.4
17.3
19.7
14.5
4.7
8.7
11.1
11.2
8.4
9.9
%
34.1
15.3
23.1
22.8
11.1
7.7
8.3
%
NS
NS
NS
NS
NS
NS
/
P-value
60
50
100
0
58
75
92
8
NS
NS
NS
NS
20
10
0
30
17
8
0
33
NS
NS
/
NS
ESS = Epworth Sleepiness Scale; SRED = sleep-related eating syndrome.
Finally, for each patient, we summed the total number of motor
events and calculated an index of each motor event per hour of
REM sleep (i.e., total number of event/hours spent in REM sleep).
In these calculations the movements involved in RBD episodes
(i.e. dream dramatization) were not taken into account.
2.4. Statistical evaluation
All the data collected are reported as mean and standard deviation, or as frequencies for continuous or categorical variables
respectively. Comparisons between NC + RBD and NC RBD patients were carried out using the nonparametric Mann–Whitney
test or the Chi-square test as appropriate for continuous or categorical data. The level of statistical significance was set at 0.05.
3. Results
3.1. Clinical data
Demographic and clinical data of all NC + RBD and NC RBD
patients are shown in Table 1. Age at onset of excessive daytime
sleepiness (EDS) and/or cataplexy, and disease duration did not differ between NC + RBD and NC RBD patients. Subjective sleepiness, assessed by ESS score, and CSF hcrt-1 did not significantly
differ in the two groups. Also there was no difference in other sleep
co-morbidities (including clinical history of other parasomnias) in
the two groups.
3.2. Polysomnographic data
The PSG data (mean ± SD) of the two groups of NC patients are
reported in Table 2. NC + RBD patients did not differ from
NC RBD group for any conventional sleep parameter (time in
bed, total sleep time, sleep efficiency, percentage of time spent in
each sleep stage, AHI, and PLMI). Nevertheless, NC + RBD patients
showed a non-significant trend towards higher REM sleep latency
(57.6 ± 43.6 vs 17.9 ± 28.0 min, p = 0.08), and a lower percentage of
time spent in non-REM sleep stage 2 (40.2 ± 6.1 vs 45.8 ± 5.2%,
p = 0.07) as compared with NC RBD patients. Moreover, while
phasic REM miniepochs percentages did not differentiate NC + RBD
NC
TIB (min)
TST (min)
WASO (min)
SE (%)
SOL (min)
FRL (min)
S1 (%)
S2 (%)
SWS (%)
REM (%)
AHI (index)
PLMS (index)
Phasic REM
miniepochs
(3 s) (%)
Tonic REM epochs
(30 s) (%)
RBD
NC + RBD
Mann–Whitney
U test
Mean
SD
Mean
SD
P-value
526.67
373.40
140.75
71.47
7.52
17.92
14.70
45.78
15.46
24.05
1.80
0.80
6.18
91.95
50.35
41.01
6.26
15.09
28.04
5.79
5.15
5.37
5.67
3.36
2.53
2.81
517.24
378.60
132.85
73.55
5.94
57.65
14.37
40.25
20.23
24.88
6.32
9.06
8.16
103.47
84.30
64.63
9.71
6.01
43.60
8.12
6.05
8.94
8.11
8.73
19.71
3.78
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
5.04
2.86
7.81
4.28
NS
TIB = time in bed; TST = total sleep time; SOL = sleep onset latency; FRL = 1st REM
latency; SE% = sleep efficiency; WASO = wakefulness after sleep onset; S1 = NREM
sleep stage 1; S2 = NREM sleep stage 2; SWS = slow-wave sleep; REM = rapid-eyemovement sleep.
from NC RBD cases, a trend towards an increase of tonic REM
epochs percentages was observed in NC + RBD compared with
NC RBD patients (7.8 ± 4.3 vs 5.0 ± 2.9%, p = 0.080).
3.3. Behavioral data of motor events
No RBD episode was detected in the video-PSG recordings of 10
NC RBD patients, while an RBD episode was detected in the video-PSG recordings of 5 out of 12 NC + RBD patients. An example
of RBD episode is reported in Fig. 1. The mean duration of these five
RBD episodes, two of which occurred in REM sleep of the first half
of the night, was 47 ± 23 s. The movements involved in these RBD
episodes were not scored nor considered for statistical analysis
(see Methods section).
A total of 2109 min of video-PSG recording of NC patients in
REM sleep was visually analyzed, and 1336 motor events were detected. The total number and index of each type of motor event in
NC + RBD and NC RBD patients is reported in Table 3, together
with a statistical comparison using the Mann–Whitney test.
In NC + RBD patients, a mean of 76.4 ± 70.9 motor events was
recorded (index of 45.5/h). The motor events were classified as elementary (61.9 ± 62.6, index of 35.6/h), as complex (10.4 ± 8.1, index of 7.6/h), and as vocalizations (4.1 ± 5.7, index of 2.3/h). The
elementary events, classified as myoclonic (21.9 ± 42.6; index of
10.7/h) and simple (40 ± 30.5; index of 24.9/h), were considerably
more numerous than those classified as complex (complex:
10.2 ± 8.1, index of 7.5/h; acting out: 0.0 ± 0.0, index of 0.0/h;
aggressive: 0.2 ± 0.4, index of 0.1/h).
In NC RBD patients, a mean of 42 ± 21.8 motor events was recorded (index of 27.4/h). The motor events were classified as elementary (34.9 ± 22.0 events; index of 22.7/h), as complex (6 ± 3.8
events; index of 3.9/h), and as vocalizations (1.7 ± 2.7 events; index
of 1.3/h). The elementary events, classified as myoclonic
(14.6 ± 19.8; index of 9.0/h) and simple (20.3 ± 15.2, index of
13.6/h), were grossly more frequent than complex ones. None of
the NC RBD patients presented complex events classified as
acting out and aggressive (Table 3).
Simple movements were significantly more frequent in
NC + RBD versus NC RBD patients when both the total number
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C. Franceschini et al. / Sleep Medicine 12 (2011) S59–S63
Fig. 1. Example of acting out movement of a NC + RDB patient. The patient is sleeping on his back and the PSG tracing is typical for REM sleep. The episode starts with the
patient mumbling, it is accompanied by a slow movement of his right arm to the top immediately followed by a fall on the bed. The patient returns to the starting position,
subsequently he raises the trunk and head and speaks the name of a person (‘‘Rino’’), moving his left arm as if he is asking him something. The episode ends with the patient
positioned on the left side position.
of events (p = 0.050) and its index (p = 0.034) were considered. Furthermore, NC + RBD patients showed a trend towards a higher total
events index (p = 0.070). The other parameters did not show statistically significant differences between groups.
4. Discussion
This video-PSG analysis of the frequencies and behavioral characteristics of motor events in NC patients with and without RBD
strengthens the view that an hcrt-1 defect in NC patients results
in increased muscular activity during REM sleep [21,22] in all NC
patients. Moreover, in keeping with some previous data [19],
NC + RBD patients displayed a significantly increased amount of
simple movements at video-analysis. Additionally, some PSG indicators (namely, the proportions of stage 2 and tonic REM epochs)
showed trends coherent with the main finding.
The main finding undoubtedly expands the role of video-PSG for
the diagnosis of RBD in NC patients, given that the greater amount
of simple movements during REM sleep in NC + RBD may be considered a hallmark for the confirmation of the clinical diagnosis
of RBD in NC patients. It seems worth emphasizing that this is
the first indication of the pathognomonic value of non violent/
complex movements for the video-PSG confirmation of RBD diagnosis in NC patients [23]. The importance of this indication appears
even greater because RBD is not an every-night phenomenon in NC
patients [14], and thus differs from other types of RBD. In these
RBD types the dream dramatization is typical, occurs regularly,
and therefore is easily verifiable by PSG-documented increase of
muscle activities [3,7–12,14,19,31], as well as by subjective reports
of RBD episodes collected on the patients or by questionnaires
compiled by bed partners.
It seems also worth considering the present findings as preliminary, given the methodological limitations of the study, in particular the small size of the sample examined and the exclusion of
the factor ‘‘gender’’ (although its relevance is uncertain). More-
Table 3
Characteristics of motor events in the two groups of NC.
NC RBD
(n = 10)
NC + RBD
(n = 12)
Mann–
Whitney U test
Mean
SD
Mean
SD
P-value
Total events (n)
Total events (index)
42.00
27.43
21.83
11.17
76.40
45.47
70.91
27.45
NS
NS
Elementary
Myoclonic (n)
Myoclonic (index)
Simple (n)
Simple (index)
Total elementary (n)
Total elementary (index)
14.60
9.01
20.30
13.65
34.90
22.67
19.83
11.89
15.25
9.08
22.05
12.08
21.90
10.68
40.00
24.89
61.90
35.56
42.60
13.58
30.46
16.01
62.59
21.37
NS
NS
0.050
0.034
NS
NS
Complex
Complex (n)
Complex (index)
Acting out (n)
Acting out (index)
Aggressive/violent (n)
Aggressive/violent (index)
Total complex (n)
Total complex (index)
6.00
3.90
0.00
0.00
0.00
0.00
6.00
3.90
3.80
1.95
0.00
0.00
0.00
0.00
3.80
1.95
10.20
7.46
0.00
0.00
0.20
0.13
10.40
7.58
8.09
6.16
0.00
0.00
0.42
0.31
8.14
6.23
NS
NS
NS
NS
NS
NS
NS
NS
0.70
1.06
3.50
5.70
NS
0.52
0.77
1.84
2.68
NS
1.00
1.70
0.60
1.07
NS
0.77
1.34
0.49
0.85
NS
1.70
1.29
2.71
2.08
4.10
2.33
5.68
2.80
NS
NS
Vocalization
Not associated to motor
events (n)
Not associated to motor
events (index)
Associated to motor
events (n)
Associated to motor
events (index)
Total vocalization (n)
Total vocalization (index)
over, subjective reports of the mental experience during sleep
were not collected either online or each morning. Finally, patients
were evaluated only for one night, so that the night-to-night
C. Franceschini et al. / Sleep Medicine 12 (2011) S59–S63
variability of RBD phenomena and of motor events could not be
estimated.
Taken as a whole, however, the present findings suggest that video-PSG, when not confirmatory for full blown RBD episodes, may
be useful for the understanding of the characteristics of the sleep
movements in NC patients. In general terms, our report emphasizes the utility of a careful video-analysis, in NC patients, of pathological motor behaviors that have been formerly applied to
patients with other sleep disorders, such as nocturnal frontal lobe
epilepsy [32–34] and RBD, in order to characterize the relation
with sleep and differentiate subtypes of this disorder [35,36].
In summary, this study shows that RBD in NC patients is characterized by a distinct and mild form, often without the full-blown
typical manifestation. Therefore, a careful video-PSG analysis, even
in the absence of a subjectively documented and/or PSG clear-cut
RBD episode, may provide a reliable support for the RBD diagnosis.
Disclosure of financial support and conflicts of interest
Doctor Plazzi has consulted for UCB Pharma and Cephalon.
Doctor. Ferri has consulted for Merck and Co., Sanofi-Aventis,
Sapio-Life, and ATES Medica Device. Professor Cipolli was
supported by a grant from the Fondazione Cassa di Risparmio di
Bologna (Project No. 2008.2443). Professors Pruneti and Lugaresi
and Doctors Franceschini, Pizza, Ricotta, Vandi, Detto, Poli, and
Mazzetti have reported no financial support. No author declared
any conflict of interest.
The ICMJE Uniform Disclosure Form for Potential Conflicts of
Interest associated with this article can be viewed by clicking on
the following link: doi:10.1016/j.sleep.2011.10.013.
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