Download Pediatric Parasomnias

PEDIATRIC PARASOMNIAS
Pediatric Parasomnias
Thornton B.A. Mason II, MD, PhD1; Allan I. Pack, MBChB, PhD2
Division of Neurology, The Children’s Hospital of Philadelphia; 2Chief, Division of Sleep Medicine; Director, Center for Sleep and Respiratory
Neurobiology, University of Pennsylvania, Philadelphia, PA
1
associated with REM sleep; and 3) other parasomnias. We detail here
issues in the clinical diagosis, evaluation, and management of multiple
pediatric parasomnias. The further study of parasomnias in children may
help elucidate the multi-factorial etiologies of these fascinating conditions,
shedding light on the potential genetic bases as well as environmental
contributions.
Keywords: Parasomnia, arousal, NREM sleep, REM sleep
Citation: Mason TBA; Pack AI. Pediatric parasomnias. SLEEP 2007:
30(2);141-151.
Abstract: Parasomnias in childhood are common, and often more frequent than in adults. The large number of parasomnias underscore that
sleep is not simply a quiescent state, but can involve complex episodes
of movement, ranging from subtle to dramatic and complex. Clinicians
should be aware that many pediatric parasomnias are benign, self-limited, and may not persist into late childhood or adolescence. Importantly,
parasomnias in childhood often differ in type from adults. Nevertheless,
parasomnias across ages can be classified as: 1) disorders of arousal
(from non-rapid eye movement, or NREM, sleep); 2) parasomnias usually
disorders include incomplete transition from slow wave sleep,
automatic behavior, altered perception of the environment, and
variable degrees of amnesia for the event. In particular, because
of the association with slow wave sleep, the arousal parasomnias
tend to occur in the first third of the night, when slow wave sleep
is most prominent.1 The child’s sleep stage transition from SWS
is abnormal, often when shifting into lighter NREM sleep (e.g.,
stage 2) just prior to the first REM sleep episode. The patient in
a sense becomes “stuck” between deep sleep and wakefulness.4
The EEG during these episodes demonstrates an admixture of
theta, delta, and alpha frequencies.
INTRODUCTION
ACCORDING TO THE INTERNATIONAL CLASSIFICATION OF SLEEP DISORDERS (ICSD-2), PARASOMNIAS
ARE “UNDESIRABLE PHYSICAL EVENTS OR experiences
that occur during entry into sleep, within sleep, or during arousals
from sleep.”1 The large number of parasomnias underscore that
sleep is not simply a quiescent state, but can involve complex episodes of movement, ranging from subtle to dramatic and complex.
The obvious, prolonged, dramatic events are most likely to raise
concerns of patients, relatives, and clinicians, prompting medical
evaluation.2 As delineated by the International Classification of
Sleep Disorders, Second Edition, parasomnias are classified as:
1) disorders of arousal (from non-rapid eye movement, or NREM,
sleep); 2) parasomnias usually associated with REM sleep; and 3)
other parasomnias. This convenient categorization scheme will be
used to order the discussion that follows. The goal of this review
is to summarize important clinical features of the different parasomnias, with an emphasis on manifestations seen in the pediatric
population.
Prevalence
The disorders of arousal parasomnias are more frequent in
childhood than in adolescence or adulthood. Prevalence estimates
in childhood for sleep terrors range from 1%-6%, for sleepwalking up to 17% with a peak at 8-12 years, and confusional arousals
up to 17.3%.1 Based on structured telephone interviews, Ohayon
et al. reported that the percentage of adolescents and adults (aged
15-24 years) with sleep terrors was 2.2%, sleepwalking 2%, and
confusional arousals 4.2%; the prevalence significantly decreased
after age 25, and no sex differences were observed.5
Disorders Of Arousal From NREM Sleep
An important subset of pediatric parasomnias includes the disorders of arousal. These parasomnias may be considered part of a
continuum, as they share overlapping features: sleepwalking, confusional arousals, and sleep terrors. While most often occurring in
slow wave sleep (stages 3, 4 of NREM sleep), these parasomnias
can also occur in stage 2 NREM sleep.3 Common aspects of these
Evaluation
The office evaluation of a child with any parasomnia should be
thorough. Because parasomnias occur out of sleep, a child’s recollection of events is fragmented at best. Indeed, in most cases the
child will not remember any details of what transpired. Parents
should be questioned regarding what events typically occur, how
soon after sleep onset these events are noted, and whether episodes
take place during naps as well as at night. Parents should also be
asked to describe in detail the movements and behaviors that are
typically seen. Information regarding whether the movements are
rhythmic or stereotyped and whether the movements occur at different times through the night should be gathered; these features,
if present, may support an epileptic origin to the events. Parents
can also report whether similar events have been noted during
wakefulness. To complement the parents’ descriptions, home videos often prove very useful for identifying and classifying parasomnias.6 A detailed history may also be supported through the
Disclosure Statement
This was not an industry supported study. Dr. Pack has done consulting for
Cypress Biotechnology and performed a speaking engagement for Merck
Pharmaceuticals. Dr. Mason has indicated no financial conflicts of interest.
Submitted for publication January 4, 2006
Accepted for publication October 10, 2006
Address correspondence to: Thornton B.A. Mason II, MD, PhD, Division
of Neurology, Wood Center 6th Floor, The Children’s Hospital of Philadelphia, 34th St. and Civic Center Blvd., Philadelphia, PA 19104. E-mail:
[email protected]
SLEEP, Vol. 30, No. 2, 2007
141
Pediatric Parasomnias—Mason and Pack
unarousability.13 With sleep terrors, children may report indistinct
recollections of threats (monsters, spiders, snakes) from which
they have to defend themselves.10,14 Considerations in the differential diagnosis of sleep terrors include nightmares, nocturnal
panic attacks, epileptic events (see below), and cluster headaches.
Sleep terrors are more prevalent in childhood than later life; peak
prevalence is between 5-7 years, and resolution typically occurs
before adolescence. Sleep terrors affect approximately 3% of
children between the ages of 4-12 years and <1% of adults.15
completion of sleep diaries, in which parents record sleep periods,
arousals/awakenings, and parasomnia events.
The sleep history should be accompanied by a comprehensive
physical and neurological exam, to look for features that would
be associated with an underlying sleep disruptor: for obstructive
sleep apnea, features such as adenotonsillar hypertrophy, retrognathia, and mid-face hypoplasia; for periodic limb movements in
sleep, features such as peripheral neuropathy or myelopathy.
SLEEPWALKING
Influencing Factors
Sleepwalking (somnambulism) in childhood shares features
with sleepwalking in adults. Sleepwalking may be either calm or
agitated with varying degrees of complexity and duration.7 The
frequency of sleepwalking may be underestimated because of
episodes that are unobserved or unremembered.8 In his landmark
studies, Klackenberg reported that the presence of sleepwalking
of variable frequency was highest at 11-12 years, with males and
females equally affected.9 Children with somnambulism are usually calm and do not demonstrate fear. The child may be found
walking into a parent’s room, bathroom, or different parts of the
house. With mobility go concerns for safety, because subjects
with sleepwalking are at risk for injury.7 The subject may climb
through windows, wander in bathrooms, attempt to walk downstairs, and sometimes leave the house. Injuries to the child may
include trauma from falls, lacerations from broken window / patio
glass doors, even hypothermia from exposure.2
Disorders of arousal (sleep walking, confusional arousals,
sleep terrors) can be thought of as being due to a faulty “switch”
that prevents normal sleep cycle progression. The transition from
SWS to lighter sleep, just prior to REM sleep onset, is abnormal. The patient is neither fully asleep nor fully awake.4 The EEG
demonstrates an admixture of different EEG frequencies.16
There are multiple factors that may influence arousal parasomnias. Age is an important issue, as many parasomnias are
much more likely to occur in childhood than later in life. Another
contributing factor includes the homeostatic drive to sleep, with
more frequent or more severe parasomnia episodes being associated with prolonged sleep deprivation. Sleep deprivation has
been shown to increase the complexity and frequency of sleep
walking events in a sleep laboratory during subsequent recovery
nights; thus, sleep deprivation may facilitate a polysomnographically-based diagnosis.17 Other factors that may trigger parasomnias include medications (e.g., neuroleptics, sedative hypnotics,
stimulants, and antihistamines), a noisy or stimulating sleep environment, fever, stress, and intrinsic sleep disorders (such as obstructive sleep apnea and periodic limb movements in sleep).18
Features in the child’s history that support obstructive sleep apnea
include the presence of snoring, gasping in sleep, and pauses in
breathing. Overnight polysomnography is indicated when there
is concern for an intrinsic sleep disruptor (e.g., periodic limb
movements, obstructive sleep apnea), rather than to document the
parasomnia per se, as parasomnia events recorded in the sleep
laboratory may be atypical if indeed present at all (see Figure
1). Reviewing questionnaire data, Owens et al. reported that parasomnias such as sleepwalking and sleep terrors appeared significantly more common in children with obstructive sleep apnea
than in normal children.19 Guilleminault et al. reported in children
that sleep disordered breathing or periodic limb movements in
sleep/restless legs syndrome may trigger sleep walking or sleep
terrors, as these parasomnias disappeared after treatment of obstructive sleep apnea or periodic limb movements in sleep/restless
legs syndrome.14 In another study, children with sleep-disordered
breathing experienced more parasomnias than those without.20 In
childhood, psychopathology is thought to be extremely rare as
an influencing factor for arousal parasomnias.3 In adults, there is
controversy, but no close association has been established.21
Several studies support a genetic predisposition for arousal parasomnias. Some evidence draws from studies of sleep terrors,
in which a possible autosomal dominant disorder was seen in a
3-generation family.22 Kales et al. reported that the prevalence of
sleep terrors and sleep walking in first degree relatives of individuals with sleep terrors was 10 times greater than in the general
population. They estimated a 60% chance of a child being affected if both parents were affected.23 A study of monozygotic and
CONFUSIONAL AROUSALS
Confusional arousals have more associated agitation than that
usually expected with sleepwalking. Confusional arousals occur
mainly in infants and toddlers. A typical episode may begin with
movements and moaning, then evolve to confused and agitated
behavior with calling out, crying, or thrashing.10 Attempts to wake
the child fully are unsuccessful. The child appears confused, with
eyes open or closed, and is very agitated or even combative. Physical injury is rarely seen.11 The child resists the parents’ efforts at
consolation, and more forceful attempts to intervene may result in
increased resistance and further agitation. A confusional arousal
episode may last 5-15 minutes (although sometimes longer) before the child calms and returns to a restful sleep. In adults, sleep
drunkenness (schlaftrunkenheit) can occur on rapid awakening
from especially deep sleep. Factors that increase sleep drunkenness include sleep deprivation, medication effects, or other sleep
disorders with excessive sleepiness or abnormal sleep/wake patterns.2 In a large sample of individuals ages 15 –100 years, confusional arousals were self-reported by 4.2% of the sample; the
prevalence was equal in males and females, and was highest in the
15-24 year old age group, decreasing significantly with advancing
age.5
SLEEP TERRORS
Sleep terrors are dramatic partial arousals from slow wave
sleep. The child may sit up suddenly and scream, with an intense,
blood-curdling “battle cry.” The episode is a fight-flight phenomenon. Autonomic activation is present, with mydriasis, diaphoresis, and tachycardia.12 There is increased respiratory tidal volume, and an intense look of fear on the face. Moreover, there is a
“curious paradox” of endogenous arousal coexistent with external
SLEEP, Vol. 30, No. 2, 2007
142
Pediatric Parasomnias—Mason and Pack
Figure 1—An epoch from an overnight polysomnogram in a 7-year-old boy with a history of sleep terrors. The first three quarters of the epoch
include the high-amplitude slow waves of stage 4 NREM sleep. There is a sudden arousal (long arrow) with an admixture of EEG frequencies and
muscle movement. The partial arousal parasomnia occurred in the first third of the study (short arrow) and lasted less than 3 minutes. The patient
was confused and mildly agitated, then transitioned to stage 2 sleep and soon back to slow wave sleep (see sleep staging, marked by the bracket).
dizygotic twins demonstrated that sleep terrors are under moderate to strong genetic control.24 Proposed modes of inheritance for
sleepwalking include multifactorial models, autosomal recessive
inheritance with incomplete penetrance, and autosomal dominant
inheritance with variable penetrance.25 Working from the Finnish
Twin Cohort, Hublin et al. reported that >1/3 of sleepwalking in
adults and >1/2 in children is attributable to genetic factors; both
additive and dominant genetic effects were proposed.8 Lecendreux
et al. in a family-based study found a positive association between
the HLA-DQB1*05 subtype and sleepwalking, suggesting a possible further interaction between the immune system and sleep.25
trolled), and multiple attacks per night. In some cases, seizures
may be brief, with preserved consciousness; typically, seizures
do not necessarily predominate during the first third of the night
(as with arousal parasomnias) and may occur on waking or falling asleep.26 Within sleep, seizures are more likely to occur from
non-REM stages 1-2 sleep, rather than slow wave sleep (when
arousal parasomnias typically arise). If epilepsy is considered, an
expanded EEG montage is needed: sleep-deprived EEG, videoEEG as inpatient, or ambulatory continuous EEG recording can
be required. While ambulatory continuous EEG recording for
seizure detection and classification has the appeal of potentially
greater convenience and lower cost, there are several limitations:
contamination of the EEG signal by artifacts (loose leads, muscle
activity, movement), a decreased number of channels available
for the recording, and a lack of video documentation to review
behavioral manifestations.27 A routine daytime EEG that includes
sleep may be valuable in demonstrating epileptiform discharges
that would add further support for an underlying seizure disorder.
When considering epilepsy in the differential diagnosis of
children with paroxysms of complex movements during sleep, a
particular subtype of interest is nocturnal frontal lobe epilepsy.
Nocturnal frontal lobe epilepsy can manifest in three patterns,
Clinical Studies
In evaluating arousal parasomnias, it is rare to capture a full,
typical event during an overnight in-laboratory sleep study (polysomnography). Nevertheless, polysomnography may play an important role. When there is a clinical suspicion, polysomnography
can be used to assess whether other disorders of sleep are present, including obstructive sleep apnea, as well as whether there
might be seizures. Features supporting epilepsy in the differential
diagnosis of nocturnal paroxysmal events include stereotyped behavior, a history of seizures (even if purported to be well conSLEEP, Vol. 30, No. 2, 2007
143
Pediatric Parasomnias—Mason and Pack
that may lie along a continuum: 1) paroxysmal arousals, which
involve abrupt, frequently recurring arousals from sleep with
stereotyped movements (raising the head, sitting, screaming, or
looking around as if frightened); dystonic posture of the limbs
often occurs, with a typical event duration of less than 20 seconds; 2) nocturnal paroxysmal dystonia, where sudden arousals occur with complex, stereotyped, and sometimes bizarre sequences of movements (asymmetric tonic or dystonic postures,
cycling movements, kicking, twisting, or rocking of the pelvis);
event duration is typically less than 2 minutes; and 3) episodic
nocturnal wanderings, where sudden awakenings with abnormal
motor features are followed by agitated somnambulism (jumping,
twisting around, moving aimlessly), possibly accompanied by
screaming or agitated behavior; the duration is usually less than 3
minutes.28,29 The mean age of onset for nocturnal frontal lobe epilepsy is 10-12 years, and affected patients usually have a history
of normal psychomotor development. Establishing the diagnosis
may be difficult as neuroimaging is usually normal and more than
half the cases may not have ictal or interictal EEG changes. Anticonvulsants are often effective, especially carbamezepine. There
is a genetic form of nocturnal frontal lobe epilepsy that is autosomal dominant, and it has been linked to chromosome 20q13.2,
with three mutations in the nicotinic acetylcholine receptor α4
subunit identified; another linkage to chromosome 15q24 has
been reported.30,31
3 to 6 week course of treatment may be curative, allowing withdrawal of the medication.7
Parasomnias Usually Associated With REM Sleep
The discussion that follows regarding REM-associated parasomnias draws primarily from sleep medicine experiences in
adults. It is unclear at present how prominent and indeed how
clinically important some of these disorders are in children, particularly REM sleep behavior disorder.
REM Sleep Behavior Disorder
REM sleep behavior disorder (also known as REM sleep motor disorder) involves “problematic behavioral release,” with enacting of unpleasant, combative dreams. Instead of the expected
REM sleep atonia, patients with REM sleep behavior disorder
have complex movements that can be vigorous and even violent.
REM sleep behavior disorder in adults tends to have a male predominance, with onset usually in the sixth to seventh decade of
life; in a major case series, 25% of patients experienced a prodrome with a mean duration of 22 years (range 2-48 years), where
vocalizations and partial limb movements without complex behavior occurred during REM sleep.28 REM sleep behavior disorder is uncommon in children but can occur.
Affected patients with REM behavior disorder, while in a dream
state, may injure themselves or their bed partners by punching,
grabbing, or kicking.11,35 As a result, trauma can occur (e.g., lacerations, ecchymoses, and fractures) that may be at times severe
and perhaps life-threatening. Patients with REM sleep behavior
disorder report that their dreams have more action, intensity, and
violence than typical dreams.36 While there is variable loss of the
general muscle paralysis typically associated with REM sleep, all
other major features of REM sleep remain intact in REM sleep
behavior disorder. Other aspects of generalized anomalous motor control in REM sleep behavior disorder include periodic limb
movements and nonperiodic limb twitching in NREM sleep.
Years before REM sleep behavior disorder was first described
in humans, REM sleep without atonia was demonstrated in pioneering experiments using animal models in the laboratories of
Jouvet and Morrison.37,38 After placement of symmetric pontine
tegmental lesions in cats, episodes of REM sleep without atonia were observed, in which the cats raised their heads, stood,
and even walked, while all other cardinal features of REM sleep
were recorded concurrently.37 It is believed that the pontine lesions affect the descending reticular formation and result in a loss
of the inhibition of the alpha motor neurons that occurs during
REM sleep.39 Further animal experiments supported a complexity to the control of the behaviors during REM sleep, as different
behaviors in REM sleep were dependent on the specific pontine
lesion sites.40 Potentially, multiple brainstem regions and pathways could be involved in human REM sleep behavior disorder,
including the ventral mesopontine junction, the locus coeruleus
and the laterodorsal and pedunculopontine tegmental nuclei in the
pons, and the gigantocellularis, magnocellularis and paramedianis nuclei in the medial medulla.41
The brain regions involved in dreaming during human REM
sleep have been explored in multiple studies. Functional PET
scans have demonstrated increased regional blood flow in REM
sleep in the pontine tegmentum, both amygdaloid complexes, left
thalamus, anterior cingulate cortex, and right parietal operculum.42
Management
Treatment of disorders of arousal includes reassuring parents
that parasomnias are common in childhood and can be managed
effectively. The parents should be counseled where appropriate
on instituting important safety measures, i.e., placing mattress on
the floor, securing windows and outside doors, covering windows
with heavy curtains, and using alarm systems and bells to alert
parents should the child leave the room. Another important intervention is to ask parents and patients to maintain a sleep diary,
which will foster routine notation of sleep times and may help to
reinforce the principle of minimizing sleep deprivation to lessen
the frequency and duration of parasomnias. Attention should be
focused on ensuring that caffeine-containing beverages are eliminated completely, as caffeine may contribute to decreased sleep
efficiency and thereby increase sleep debt. Parents should be advised not to try to restrain or waken the child during an episode.
Not only is waking such a child difficult, it is unnecessary and
counterproductive. The result may be prolonging/worsening of
the episode. If the child has no recollection of the episode, then
there is no value in recounting them the following day, as this
may promote anxiety.2 When arousal disorders occur consistently
at a particular time, scheduled or anticipatory awakenings several
minutes beforehand may help ameliorate the events;32-34 scheduled awakenings may be ineffective in children who do not have
arousal parasomnias frequently and at a predictable time.6
Medications should be reserved for those rare, protracted cases
with no associated sleep disorder, with frequent parasomnias, and
with a threat of injury to patients/others. Medications that have
been used successfully in the past include benzodiazepines and
tricyclic antidepressants.15 Low-dose clonazepam is often effective in controlling arousal disorders in children. Starting with 0.25
mg an hour before bedtime, the dose may be increased slowly
with attention to symptoms of daytime sedation. In some cases, a
SLEEP, Vol. 30, No. 2, 2007
144
Pediatric Parasomnias—Mason and Pack
accounts for up to 60% of observed cases in adults.41 REM sleep
behavior disorder can also be seen in degenerative central nervous system disorders, including Parkinson disease, Lewy-body
dementia, and multi-system atrophy, Machado-Joseph disease,
and parkinsonism with parkin gene mutations (Park2).49 Indeed,
in adults, the majority of patients with “idiopathic” REM sleep
behavior disorder will eventually develop neurodegenerative disorders;4 longitudinal data support the emergence of other signs
and symptoms of neurologic dysfunction, often with a latency
of more than a decade from the onset of REM sleep behavior
disorder.50,51
Among the neurodegenerative disorders, REM sleep behavior
disorder is significantly more frequent in patients with Parkinson
disease, multiple system atrophy, and dementia with Lewy bodies;52 these disorders have similar inclusions containing the protein α-synuclein, and hence they may be referred to collectively
as “synucleinopathies.”52,53 Emerging data suggest that idiopathic
REM sleep behavior disorder is not simply a parasomnia, but
may indeed involve multiple neurologic abnormalities including
impaired cortical activity, decreased dopaminergic innervation,
autonomic abnormalities, and neuropsychological deficits while
patients are asleep and awake.41 Olfactory dysfunction in patients
with idiopathic REM sleep behavior disorder may offer a further
clue to the diagnosis of an underlying α-synucleinopathy (particularly Parkinson disease).54 REM sleep behavior disorder is more
common after age 50, and 80%-90% of those affected are men.55
Functional relationships between dream features and brain structure include the following: emotional aspects of dreams are likely
related to activation of the amygdalar complexes bilaterally, orbito-frontal cortex, and the anterior cingulate gyrus; perceptual features likely relate to activation of occipital and temporal cortices;
the memory content in dreams likely results from mesio-temporal
regions; and the bizarre, irrational content of dreams may be the
consequence of hypoactivation of the prefrontal cortex.43,44 Motor
initiation and control centers play a key role in the experience of
movement in dreaming, and these regions include the basal ganglia, brainstem motor pattern generators, and the primary motor
cortex.44 These motor centers are activated in normal REM sleep,
but, pathologically, associated movements are only physically executed in REM sleep behavior disorder.
The differential diagnosis of REM sleep behavior disorder is
long, and includes the following: nocturnal seizures; sleepwalking/sleep terrors; hypnogenic paroxysmal dystonia (attacks from
sleep of extremity torsion, which when brief are likely partial
motor seizures from the cerebral frontal lobe); episodic nocturnal wanderings (potentially another manifestation of nocturnal
frontal lobe epilepsy); rhythmic disorders of NREM and REM
sleep; obstructive sleep apnea with agitated arousals; nocturnal
psychogenic dissociative disorders (complex and often injurious
activity during apparent sleep, but with a concurrent waking EEG
pattern; reported in patients with a prior history of physical or sexual abuse during childhood) and malingering.36,45 Dream enacting
behaviors have been seen in adults with severe obstructive sleep
apnea; polysomnography has demonstrated that the apparent acting out of dreams (with kicking, gesturing, talking, and raising the
arms) occurred during arousals at the end of the obstructive sleep
apnea episodes. Effective treatment of the sleep apnea with continuous positive airway pressure eliminates the unusual behavior,
which has been termed “pseudo-REM sleep behavior disorder.”
While rare, children and adolescents have been documented to
have REM sleep behavior disorder (subclinical, idiopathic, and
symptomatic), with onset as early as 11 months of age.46 REM
sleep behavior disorder in children may occur in the clinical setting of narcolepsy. REM sleep behavior disorder has also been
documented in children with neurological disorders such as brainstem tumors, juvenile Parkinson disease, and olivopontocerebellar degeneration.36,47 Other pediatric disorders associated with
REM sleep behavior disorder or subclinical REM sleep behavior
disorder based on case reports include Tourette syndrome, xeroderma pigmentosum, and infantile spasms.36,46 Clues to REM
sleep behavior disorder in children include nightmares associated
with body movements, trauma from movements during sleep,
and limb/body movements associated with vivid dream recall.
The abnormal preservation of muscle tone during REM, with increased REM phasic muscle activity, can be identified in children
on overnight polysomnography.46,48 In a series of 5 pediatric cases
of REM sleep behavior disorder, clonazepam given in bedtime
doses of 0.25 mg has been reported to be completely effective in
eliminating the parasomnia.48
Pharmacotherapy can aggravate preexisting REM sleep behavior disorder and in some cases lead to REM sleep behavior disorder. Commonly implicated medications are antidepressants (such
as tricyclic antidepressants, venlafaxine, and fluoxetine).36 Chronic REM sleep behavior disorder can arise without apparent cause;
REM sleep behavior disorder is currently termed “idiopathic”
when no neurologic signs or CNS lesions are found. This form
SLEEP, Vol. 30, No. 2, 2007
Clinical Studies and Treatment
Polysomnography reveals persistent elevated muscle tone and
movement throughout REM sleep, including distinctly increased
phasic EMG activity.36 The placement of additional EMG leads
during the recording may be helpful in demonstrating increased
movements of the arms, legs, and truck. Periodic limb movements in sleep may be seen in addition to increased phasic muscle activity. No epileptiform activity or frank seizures are seen.11
Most adults with REM behavior disorder improve with low-dose
clonazepam (0.5-2 mg taken at bedtime), which suppresses phasic REM EMG activity; in this setting, clonazepam is reported to
be safe and efficacious. Rather than restoring REM atonia, clonazepam suppresses phasic EMG activity (with behavioral control).36 Typically, relapse of REM behavior disorder occurs immediately with discontinuation of clonazepam.39 Melatonin given
in a range of 3-9 mg in adults is reported to restore REM atonia,
and may be effective as monotherapy for REM behavior disorder,
or in combination with clonazepam.36 Melatonin apparently has
its therapeutic activity in restoring REM atonia (as distinct from
the phasic motor activity mechanism of clonazepam).56,57 Melatonin may be considered for treatment of REM behavior disorder
when there is an incomplete response to clonazepam, or concerns
that clonazepam might potentially aggravate existing dementia
or exacerbate daytime sleepiness.57 No prospective, randomized,
controlled trials of melatonin or clonazepam for REM behavior
disorder have been performed to date.
REM sleep behavior disorder can coexist with other sleep disorders, resulting in combined narcolepsy-REM sleep behavior
disorder and parasomnia overlap disorder.36 Parasomnia overlap
disorder refers to patients having combined (injurious) sleepwalking and/or sleep terrors with REM sleep behavior disorder; those
cases that are idiopathic in origin have been reported to have an
145
Pediatric Parasomnias—Mason and Pack
earlier onset (childhood) than a symptomatic subgroup (early
adulthood), where cases develop secondary to some other underlying pathological process.58 Moreover, Schenck and Mahowald describe status dissociatus, a most extreme manifestation of
REM sleep behavior disorder, with apparent complete disruption
of state-determining boundaries.36 On polysomnography, behavioral and self-perceived sleep actually consists of a simultaneous
admixture of elements of NREM sleep, REM sleep, and wakefulness.59 These findings are similar to the clinical impression,
where sleep is atypical with vocalizations, twitching, and reports
of dream-like mentation on forced or spontaneous awakenings.
Conditions potentially associated with status dissociatus include
narcolepsy, protracted withdrawal from alcohol abuse, olivopontocerebellar degeneration, prior open-heart surgery, and fatal familial insomnia. Status dissociatus may respond to clonazepam.36
type) are perceptions not based in reality that can occur at sleep
onset (hypnagogic hallucinations) or on awakening (hypnopompic hallucinations). While these hallucinations are primarily visual, they can also include tactile, auditory, or kinetic phenomena.
Sleep related hallucinations may be associated with episodes of
sleep paralysis, concomitantly or on different nights. It is unclear
currently whether sleep related hallucinations are always associated with REM intrusion into wakefulness, as is this case with
isolated recurrent sleep paralysis.1
Nightmare Disorder
Nightmares are generally well known as vivid dreams with intense feelings of terror or dread64 that typically awaken a patient
from sleep. While children may appear anxious after awakening,
they can relay a developmentally appropriate description of sometimes very detailed dream imagery (unlike the vague descriptions,
if any, that children offer after a sleep terror).11 Although dreaming
may occur in other sleep stages, nightmares with their characteristically complex storylines and increasingly frightening content
usually occur during REM sleep (and are therefore more common
during the second half of a major sleep period). Prominent motor
activity during nightmares rarely occurs, in contrast to REM behavior disorder and sleep terrors;65 phasic muscle twitches, however, may be increased.11 Bad dreams may have similar dream
content, but do not trigger awakenings from sleep. Bad dreams
are felt to be 3 to 4 times more prevalent than nightmares.66
Between the ages of 3 and 6 years, nightmares are especially
common, noted at least occasionally in 30%-90% and often in
5%-30% of children in this age group. During childhood, boys
and girls are equally affected, but in adults, women appear to be
significantly more affected.65 Nielsen et al. reported that the recall of disturbing dreams was more prevalent in girls than boys
at ages 13 and 16 years.66 There is a carryover effect with maturation; those with nightmares in childhood (often or sometimes)
have nightmares as adults weekly or monthly in 28.5% of males
and 32.5% of females.65 As reviewed by Levin and Fireman, occasional nightmares in adults are quite common with 85% of respondents having at least one episode in the past year, and 2%-6%
having weekly nightmares.64
Recurrent Isolated Sleep Paralysis
Sleep paralysis is a generalized, fleeting inability to speak or to
move the trunk, head, and limbs that occurs during the transitional
period between sleep and wakefulness. The episodes are transient,
lasting variably from one minute or less to several minutes.60 There
is preservation of consciousness. Despite their relative brevity,
episodes of sleep paralysis can be quite distressing, particularly if
associated with hallucinations.60 The sleep paralysis phenomenon
is known in many cultures, and has been named “Old Hag” in
Newfoundland, “Kokma” in the West Indies, “Kanashibari” in Japan, and “being ridden by the witch” by some southern U.S. African Americans.61 Sleep paralysis may occur as part of the classical
tetrad of narcolepsy, as an isolated form in otherwise healthy individuals, or in a familial form apparently under genetic control.62
Few reports exist that explore possible genetic factors in sleep
paralysis;1 one study of 22 patients with sleep paralysis found a
positive family history of sleep paralysis in 19 (86%).63 Factors
such as fatigue, stress, irregular schedules, shift work, sleeping
in a supine position, alcohol/caffeine use, and sleep deprivation
may predispose individuals to sleep paralysis.60,62 Mental disorders associated with sleep paralysis include panic disorder, other
anxiety disorders, bipolar disorder, posttraumatic stress disorder,
and depression.61
Conditions that could mimic isolated sleep paralysis include
atonic seizures, cataplexy, hypokalemic periodic paralysis, drug
withdrawal/abuse (particularly anxiolytic medications, which
can result in physical immobility on awakening because of their
muscle relaxant properties), hysterical or psychotic states with
immobility, and REM rebound.60,62 For the diagnosis of recurrent
isolated sleep paralysis, one needs to exclude the possibility that
the parasomnia is not better explained by another sleep disorder,
mental disorder, neurological disorder, medical disorder, or medication/substance use.1
While some reports suggest that isolated sleep paralysis begins
in childhood or adolescence in most cases,62 others support onset
across the lifespan.60 In a sample of European subjects age 15
years or older studied by Ohayon et al.,5,60 6.2% of the sample
experienced at least one sleep paralysis episode during their lifetime; other surveys found higher lifetime prevalences of 15%40%.1 Ohayon et al. found that 12.4% of adult subjects with sleep
paralysis had episodes that started during childhood, while 10.8%
had onset during adolescence (prior to age 18).60
Sleep related hallucinations (another ICSD-2 parasomnia
SLEEP, Vol. 30, No. 2, 2007
Associated Disorders
While infrequent nightmares likely do not merit further evaluation or treatment, it is important to note that there is an increased
prevalence of psychiatric disorders in patients with nightmares
compared to controls. In particular, schizophrenic spectrum pathology has been described: borderline or schizoid personality
disorder, schizotypal personality, and schizophrenia.64,65 In children, psychiatric disorders have been seen more than 3 times as
often in those with nightmares than those without; in adults, the
proportion of patients with psychiatric disorders is about 5 times
greater than among those without nightmares.65 Frequent disturbing dreams have been found to be associated with anxiety at age
13 and generalized anxiety disorder, separation anxiety, and overanxious disorder symptoms in later adolescence (age 16).66 Nightmares may also be a specific marker for a history of sexual abuse
in children and adolescents.67 Children with posttraumatic stress
disorder (from direct violence, witnessed violence, accidents, or
natural disasters, for example) may re-experience the trauma with
trauma-specific reenactments, repetitive play involving trauma
146
Pediatric Parasomnias—Mason and Pack
Table 1—Comparison of Pediatric Parasomnias and Nocturnal Seizures
Timing during sleep
Sleep stage at start
First Third
SWS
Confusional
Arousals
First Third
SWS
Duration
Agitation
Autonomic arousal
EEG abnormalities
Amnesia
Post-event confusion
Family history / genetic
Episodes in wakefulness
Structural CNS lesion
2-30 min.
None/mild
None/mild
No
Yes
Usual
Yes
No
No
5-40 min
Moderate
Moderate
No
Yes
Usual
Yes
No
No
Characteristic
Sleepwalking
Sleep Terrors
Nightmares
Seizures
First Third
SWS
Second half
REM
1-10 min
Marked
Severe
No
Yes
Usual
Yes
No
No
3-20 min.
Mild
Mild
No
No
Very rare
No
No
No
Any
Any, esp
St2
2-15 min.
Variable
Variable
Yes
Yes
Usual
Rare
Possibly
Possibly
Adapted from Rosen et al.10 and Broughton.3 SWS, slow wave sleep (stage 3 and 4 NREM sleep); St2, stage 2 NREM sleep.
themes, and generalized nightmares; dreams of the event may
be nonspecific.68 Analyses in twins support persistent genetic effects that impact on the frequency of nightmares in both childhood and adulthood; a study estimated that approximately 44%
of phenotypic variance in nightmares among children and 37%
in adults was due to genetic effects.65 Environmental influences
(e.g., television) appear to influence dream content in a majority
of children.69 For a comparison of nightmares and other pediatric
parasomnias versus nocturnal seizures, see Table 1.
first is polyuria, which at least in some cases is related to a decreased vasopressin peak during sleep (Group 1, volume- or diuresis-dependent patients). The second mechanism can be sudden,
involuntary detrusor contractions with a small nocturnal functional bladder capacity and daytime enuresis (Group 2, detrusor
dependent group). The third cause is felt to be a decreased arousability (Group 3). Patients in Group 1 may respond to DDAVP (1Deamino-8-D-Arginine Vasopressin; also known as desmopressin).75 Patients in Group 2 may respond to alarms.
In the low arousability patients (Group 3) one should consider
whether patients have sleep disordered breathing. A significant
percentage of children with obstructive sleep apnea also have nocturnal enuresis, with estimates ranging from 8%-47%.74 In such
subjects, enuresis can respond to adenotonsillectomy.76 Following adenotonsillectomy, resolution of enuresis has been reported
in 55%-77% of children; most cases resolve in the first month after surgery, with an additional minor resolution thereafter.74 There
are several mechanisms whereby obstructive sleep apnea may be
involved in enuresis. Obstructive respiratory events can be associated with swings of negative intrathoracic pressure and positive
abdominal pressure. Pressure changes may affect bladder function
directly due to abdominal compression, contributing to enuresis.
Cardiac distension in sleep apnea due to increased intrathoracic
pressure results in enhanced secretion of atrial natriuretic peptide,
which in turn inhibits renin secretion and decreases aldosterone
levels; consequently, there is a decrease in intravascular volume
and increased urine and sodium output during sleep, also contributing to enuresis.72,77,78 Treatment of obstructive sleep apnea
reduces levels of atrial natriuretic peptide and increases the mean
levels of renin and aldosterone, thereby reversing this effect.78
Other factors that may play a role in enuresis include genetic
and familial factors, infection, and anatomical variants. From a
family history perspective, enuresis is increased in the offspring
of parents who themselves had enuresis in childhood. It has been
reported, for example, if both parents have a history of childhood
enuresis, there is a 77% risk of their children also developing enuresis. If one parent was enuretic, the risk decreases to 43%. In
cases where neither parent had enuresis during childhood, a much
lower risk of enuresis has been reported (15%).79
Causes of complicated enuresis include urinary tract infection,
spinal cord abnormalities with associated neurogenic bladder, ectopic ureter in females, and posterior urethral valves in males;
Other Parasomnias
Enuresis
Nocturnal enuresis (bedwetting) refers to the passing of urine
while asleep. In children less than 5 years of age, nocturnal enuresis is normal. It has been estimated that at 5 years, approximately
15%-25% of children have nocturnal enuresis.70 Nocturnal enuresis occurs approximately 1.5-2 times more frequently in boys
than girls.71 With each advancing year, the percentage of children
with nocturnal enuresis decreases by about 15%70,72,73; this steady
decrease may indicate interim maturation of bladder or central
nervous system voiding mechanisms.74 In adolescence, only 1%3% are still wetting the bed.
Enuresis can be classified according to time of day (nocturnal enuresis, diurnal enuresis), periods of dryness, and the presence of other symptoms. Primary enuresis refers to enuresis in a
child who has never been dry (continent) consistently since birth,
whereas secondary enuresis is applicable to a child who has had at
least 6 months of dryness prior to recurrence of enuresis.
Another set of terms applies to the relationship of enuresis with
other symptoms. Monosymptomatic or uncomplicated nocturnal
enuresis involves normal voiding at night in bed without other
symptoms referable to the urogenital or gastrointestinal tracts. On
the other hand, polysymptomatic or complicated nocturnal enuresis refers to bedwetting that is associated with daytime symptoms,
such as severe urgency, urge incontinence (inability to inhibit a
bladder contraction and/or inadequate bladder capacity), staccato
voiding (inappropriate voluntary control of the external urinary
sphincter), chronic constipation, or encopresis (involuntary fecal
soiling).70,72
There are many possible etiologies for sleep enuresis. Three
major (nonexclusive) pathologic factors are often involved. The
SLEEP, Vol. 30, No. 2, 2007
147
Pediatric Parasomnias—Mason and Pack
for evaluation of these anatomic concerns, a renal ultrasound and
voiding cystourethrogram may be appropriate.70 A gastrointestinal
evaluation may be indicated for work-up of chronic constipation
or encopresis. Other contributing factors to enuresis have been
reported to include diabetes, psychological stress, sexual abuse,
and excessive evening fluid intake, particularly caffeinated beverages.77
Bader at al. studied children with enuresis and compared athome sleep studies to controls. The sleep of enuretic children was
“polysomnographically normal” although respiratory effort and
flow data were not recorded. Compared to controls, enuretic children had longer time in bed and increased number of sleep cycles.
Enuresis occurred in sleep stages 2, 3, and 4 as well as REM;
most episodes of enuresis occurred in the first half of the night.
About 50% of children with enuresis episodes in a small study
had tachycardia (and thus autonomic arousal) preceding micturition.75
appropriate, experienced psychotherapist is recommended. Coping skills are taught that can be used by the patient to replace
maladaptive responses. Because patients across the spectrum of
dissociative disorders have difficulty with traumatic reenactment
in the forms of self-injurious behavior, suicidality, and revictimization, safety planning is essential in management.82 Therapeutic
modalities may include journal entries to complement therapy
sessions as well as expressive artwork;82 the latter approach may
be expecially suited to younger children.
Exploding Head Syndrome
Exploding head syndrome (EHS) is a harmless but potentially
terrifying situation which usually occurs while a patient is falling
asleep, but less often may occur on awakening. Patients report
a terrifying loud noise, sometimes accompanied by myoclonic
jerks or the perception of a flash of light. The episode lasts only
an instant; afterwards, the patient may experience palpitations
and acute anxiety.84 Typically, exploding head syndrome is not
associated with sudden pain or headache.85,86 Polysomnography
has verified that attacks of exploding head syndrome occur during wakefulness rather than bona fide sleep; no pathological EEG
changes have been found, specifically none indicating an epileptic etiology to this condition.86 Onset of exploding head syndrome
episodes may be during childhood, but most commonly begin in
middle age or later.84 Attacks are variable, and may be sporadic;
periods when exploding head syndrome episodes recur may be
related to stressful situations at school, work, or home.86 Patients
should be reassured about the harmless nature of the symptoms.
Drug treatment is not needed.
Sleep Related Dissociative Disorders
Dissociation is a separation of discrete mental processes from
the mainstream of brain activity with a loss of integrated function
and autonomous operation of the isolated elements. Dissociation
plays a role in dissociative disorders, somatoform disorders, and
posttraumatic stress disorder. Sleep related dissociative disorder
is a variant of dissociative disorders. They occur from wakefulness out of a sleep bout, or wakefulness in the transition to sleep,
and involve a disruption of the usually integrated functions of
memory, consciousness, identity, or perception of the environment. The 3 categories of dissociative disorders that have been
documented with sleep related dissociative disorder include dissociative fugue (a disturbed state of consciousness where a patient
appears fully aware in performing activities but subsequently has
no recollection), dissociative identity disorder (formerly called
multiple personality disorder), and dissociative disorder not otherwise specified.
Most patients with sleep related dissociative disorder have corresponding daytime episodes of disturbed behavior, confusion,
and associated amnesia, as well as a current or past history of
physical or sexual abuse.1 Childhood traumatic events may result
in the development of dissociative symptoms, possibly serving as
a defense mechanism. There appears to be an association between
nightmares and dissociative states or experiences. Agargun et al.,
for example, found a strong association in college students between nightmares and childhood traumatic experiences.80 Patients
with dissociative disorders also often experience nightmare disorder; those patients with both disorders have been reported to have
suicide attempts, a higher rate of self-mutilating behavior, and
comorbidity with borderline personality disorder more than those
without nightmare disorder.81 During the sleep related behaviors,
patients can scream, run, or display sexualized behavior. These
activities may represent reenactment of previous abuse situations;
there is amnesia for the behavior on the following day. The age of
onset can range from childhood to middle adulthood. Other parasomnias, particularly disorders of arousal described earlier, must
be differentiated from the dissociative episodes.1
Patients with dissociative disorders are challenging to treat,
requiring a flexible approach that may include cognitive-behavioral therapy, sensorimotor psychotherapy, posttraumatic disorder
treatment, and clinical hypnosis.82,83 Accordingly, referral to an
SLEEP, Vol. 30, No. 2, 2007
Sleep Related Eating Disorder
Sleep related eating disorder has combined characteristics of
sleepwalking and daytime eating disorders (such as the compulsive eating of bulimia nervosa or binge eating disorder). Patients
with sleep related eating disorder experience a partial arousal
from sleep, often 2-3 hours after sleep onset. Their subsequent
eating is ‘out-of-control’ (rapid and sloppy, often with high carbohydrate foods and sometimes taken in odd food combinations
that may include nonnutritive substances). Patients may become
angry or agitated if they are disturbed during an episode and have
limited to no recall of the episode the following day.87 Common
responses to nocturnal eating include morning anorexia or restriction of daytime eating. In a case series of 23 patients with sleep
related eating disorder, Winkelman reported that 3 had onset before age 10 years, with the majority having onset in adolescence
or early adulthood.87
Associated Disorders
Most patients with sleep related eating disorders have histories of other parasomnias (isolated sleepwalking, enuresis, sleep
terrors, or some combination of these), and more than one-third
had a daytime eating disorder (bulimia nervosa, anorexia nervosa,
or binge eating disorder).87 Sleep related eating disorder has also
been reported in the setting of other primary sleep disorders such
as periodic limb movement disorder or obstructive sleep apnea;
it may be that an associated partial arousal from sleep triggers
a nocturnal eating episode in a susceptible individual.87 Medications that increase the risk of sleep related eating disorder include
148
Pediatric Parasomnias—Mason and Pack
triazolam abuse, olanzapine, respiridone, and zolpidem.88-90
In addition to sleep related eating disorder, the differential diagnosis of nocturnal eating includes nocturnal eating syndrome
(eating at night with full alertness), binge-eating disorder or
bulimia nervosa with nocturnal eating (eating at night with full
alertness, combined with a daytime eating disorder), dissociative
disorder with nocturnal eating (eating at night and altered level of
awareness in the setting of disorders such as multiple personality
disorder, posttraumatic stress disorder), and Kleine-Levin Syndrome.87
Kleine-Levin syndrome is a rare disorder characterized by recurrent episodes of hypersomnia (each often lasting as long as a
week or more), and frequently associated cognitive disturbances
(attention and memory defects, prominent confusion, decreased
concentration), altered perceptions of reality, changes in eating behavior (such as eating larger amounts of food), depressed
mood, irritability, and hypersexuality (as well as other compulsive
behaviors). Onset is often during adolescence, more commonly
in males; Kleine-Levin syndrome usually abates by early adulthood.91
expiration only, and last 2-20 seconds; the sounds tend to be repeated in clusters of 2 minutes to an hour, and occur several times
per night. Polysomnography has shown that catathrenia is associated with a slightly decreased heart rate and moderately positive
intra-esophageal pressure. The groaning ends in a snort, followed
by rebound in heart rate. The onset of catathrenia may begin during childhood or adolescence.92 The etiology of this groaning is
unclear, as no underlying psychiatric or respiratory disease has
been found. While catathrenia may have an adverse impact on
social and familial function, no specific therapy has been found
to be effective.
CONCLUSION
In summary, parasomnias in childhood are common, and often more frequent than in adults. Clinicians should be aware that
many pediatric parasomnias are benign, self-limited, and may
not persist into late childhood or adolescence. Parasomnias in
childhood often differ in type from adults (e.g., sleep terrors in
childhood are much more likely than REM behavior disorder).
Parasomnias in adults may portend significant psychiatric disturbances or neurodegenerative disorders, while these concerns are
rarely supported in childhood.
When evaluating pediatric parasomnias, a detailed history
from parents (perhaps supported by home videotapes) is most
helpful. Persistent, prominent, and complex cases require physi-
Catathrenia
Catathrenia, or nocturnal groaning, can occur in NREM sleep
Evaluating
Pediatric Parasomnias
TheTreating
moaning/groaning
sounds are in
(stage Figure
2) and 2:
REM
sleep.92and
When do events occur?
1st half of the night
2nd half of the night
Anytime during sleep
Child active but not fully
awake or fully asleep
Bed is wet
Vivid dreaming?
Dx: arousal parasomnias
- Sleepwalking
- Sleep terrors
- Confusional arousals
Evaluation:
- Home videotape
- Medical history
- Exam
- Consider triggers
- Sleep diary
- Consider PSG
Treatment:
-Re-assurance
-Increase total sleep
-Management of OSA,
RLS/PLMS if present
-Safety measures
-Scheduled awakenings
-Rarely medication
Dx: Nocturnal enuresis
Yes
No
Combative or
violent?
Yes
Inability to move
with preserved
alertness?
No
Dx: RBD
(rare)
Dx: Nightmare
Disorder
Evaluation:
-Detailed
neuro. exam
- PSG with
added EMG
- MRI
Evaluation:
If frequent,
severe, consider
psychiatric
issues (e.g.
anxiety, abuse,
PTSD)
Treatment:
- Clonazepam
- Melatonin
Treatment:
If marked,
-Psychotherapy
-Psychotropic
medication
Dx: Recurrent
sleep paralysis
Evaluation:
- Consider
narcolepsy
-Predisposing
factors, incl.
medications
- Psychiatric
issues
Treatment:
- Modify
predisposing
factors
- Reassurance
Evaluation:
- Presence of other
urogenital or g.i. symptoms
- Anatomical factors
- Presence of polyuria
- Possible functional bladder
abnormality
- Urinalysis for infection, diabetes
- PSG for OSA
Treatment:
- Specific treatement of
underlying disorder(s)
- DDAVP for polyuria
- Alarms for small
functional bladder
capacity
Abbreviations: Dx, diagnosis; PSG,
polysomnography; OSA, obstructive
sleep apnea; RLS/PLMS, restless legs
syndrome /periodic limb movements in
sleep; RBD, REM sleep behavior
disorder; PTSD, post-traumatic stress
disorder; DDAVP, 1-Deamino-8-DArginine Vasopressin
Figure 2—Evaluating and Treating Pediatric Parasomnias
SLEEP, Vol. 30, No. 2, 2007
149
Pediatric Parasomnias—Mason and Pack
cian management, aided by the appropriate use of diagnostic studies (polysomnography, expanded EEG recordings) and possible
pharmacotherapy (see Figure 2). The further study of parasomnias in children may help elucidate the multifactorial etiologies
of these fascinating conditions, shedding light on their potential
genetic bases as well as environmental contributions.
21.
22.
23.
ACKNOWLEDGMENT
24.
This work was supported by an NIH award to Dr. Mason, K23
RR16566-01.
REFERENCES
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
25.
AASM. International classification of sleep disorders, 2nd ed.: Diagnostic and coding manual. Westchester, Illinois: American Academy of Sleep Medicine, 2005
Stores G. Dramatic parasomnias. J R Soc Med. 2001;94:173-176
Broughton R. NREM arousal parasomnias. In: Kryger MH RT, Dement WC, ed. Principles and Practice of Sleep Medicine. Third ed.
Philadelphia: W.B. Saunders Co., 2000:693-706
Fisher C, Kahn E, Edwards A, Davis DM. A psychophysiological
study of nightmares and night terrors. I. Physiological aspects of the
stage 4 night terror. J Nerv Ment Dis. 1973;157:75-98
Ohayon MM, Guilleminault C, Priest RG. Night terrors, sleepwalking, and confusional arousals in the general population: their frequency and relationship to other sleep and mental disorders. J Clin
Psychiatry. 1999;60:268-276; quiz 277
Mindell JA, Owens J. Sleepwalking and Sleep Terrors. A Clinical Guide to Pediatric Sleep. Philadelphia: Lipincott Williams
&Wilkins, 2003
Mahowald MW, Bornemann MC, Schenck CH. Parasomnias. Semin
Neurol. 2004;24:283-292
Hublin C, Kaprio J, Partinen M et al. Prevalence and genetics of sleepwalking: a population-based twin study. Neurology.
1997;48:177-181
Klackenberg G. Somnambulism in childhood--prevalence, course
and behavioral correlations. A prospective longitudinal study (6-16
years). Acta Paediatr Scand. 1982;71:495-499
Rosen GM, Ferber R, Mahowald MW. Evaluation of parasomnias in children. Child and Adolecent Clinics of North America.
1996;5:601-616
Sheldon SH. Parasomnias in childhood. Pediatr Clin North Am.
2004;51:69-88, vi
Mason TB, 2nd, Pack AI. Sleep terrors in childhood. J Pediatr.
2005;147:388-392
Mahowald M. Arousal and sleep-wake transition parasomnias. In:
Lee-Chiong TL SM, Carskadon MA, ed. Sleep Medicine. Philadelphia, PA: Hanley and Belfus, inc., 2002:207-213
Guilleminault C, Palombini L, Pelayo R, Chervin RD. Sleepwalking and sleep terrors in prepubertal children: what triggers them?
Pediatrics. 2003;111:e17-25
Robinson A, Guilleminault C. Disorders of arousal. In: Chokroverty
S HW, Walters AS, ed. Sleep and Movement Disorders. Philadelphia, PA: Butterworth Heinemann, 2003:265-272
Mahowald MW, Ettinger MG. Things that go bump in the night: the
parasomnias revisited. J Clin Neurophysiol. 1990;7:119-143
Joncas S, Zadra A, Paquet J, Montplaisir J. The value of sleep deprivation as a diagnostic tool in adult sleepwalkers. Neurology.
2002;58:936-940
Mahowald MW, Schenck CH, Rosen GM, Hurwitz TD. The role of
a sleep disorder center in evaluating sleep violence. Arch Neurol.
1992;49:604-607
Owens J, Spirito A, Nobile C, Arrigan M. Incidence of parasomnias
in children with obstructive sleep apnea. Sleep. 1997;20:1193-1196
Goodwin JL, Kaemingk KL, Fregosi RF et al. Parasomnias and
SLEEP, Vol. 30, No. 2, 2007
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
150
sleep disordered breathing in Caucasian and Hispanic children the Tucson children’s assessment of sleep apnea study. BMC Med.
2004;2:14
Schenck CH, Mahowald MW. On the reported association of psychopathology with sleep terrors in adults. Sleep. 2000;23:448-449
Hallstrom T. Night terror in adults through three generations. Acta
Psychiatr Scand. 1972;48:350-352
Kales A, Soldatos CR, Bixler EO et al. Hereditary factors in sleepwalking and night terrors. Br J Psychiatry. 1980;137:111-118
Ooki S. [Statistical genetic analysis of some problem behaviors
during sleep in childhood--estimation of genetic and environmental factors influencing multiple health phenomena simultaneously].
Nippon Eiseigaku Zasshi. 2000;55:489-499
Lecendreux M, Bassetti C, Dauvilliers Y et al. HLA and genetic
susceptibility to sleepwalking. Mol Psychiatry. 2003;8:114-117
Malow BA. Paroxysmal events in sleep. J Clin Neurophysiol.
2002;19:522-534
Kotagal P, Costa M, Wyllie E, Wolgamuth B. Paroxysmal nonepileptic events in children and adolescents. Pediatrics. 2002;110:e46
Provini F, Plazzi G, Tinuper P et al. Nocturnal frontal lobe epilepsy. A clinical and polygraphic overview of 100 consecutive cases.
Brain. 1999;122 ( Pt 6):1017-1031
Provini F, Plazzi G, Lugaresi E. From nocturnal paroxysmal dystonia to nocturnal frontal lobe epilepsy. Clin Neurophysiol. 2000;111
Suppl 2:S2-8
Saenz A, Galan J, Caloustian C et al. Autosomal dominant nocturnal
frontal lobe epilepsy in a Spanish family with a Ser252Phe mutation
in the CHRNA4 gene. Arch Neurol. 1999;56:1004-1009
Zucconi M, Ferini-Strambi L. NREM parasomnias: arousal disorders and differentiation from nocturnal frontal lobe epilepsy. Clin
Neurophysiol. 2000;111 Suppl 2:S129-135
Lask B. Sleep disorders. “Working treatment” best for night terrors.
Bmj. 1993;306:1477
Lask B. Novel and non-toxic treatment for night terrors. Bmj.
1988;297:592
Frank NC, Spirito A, Stark L, Owens-Stively J. The use of scheduled awakenings to eliminate childhood sleepwalking. J Pediatr
Psychol. 1997;22:345-353
Schenck CH, Bundlie SR, Ettinger MG, Mahowald MW. Chronic
behavioral disorders of human REM sleep: a new category of parasomnia. Sleep. 1986;9:293-308
Schenck CH, Mahowald MW. REM sleep behavior disorder: clinical, developmental, and neuroscience perspectives 16 years after its
formal identification in SLEEP. Sleep. 2002;25:120-138
Morrison AR, Mann GL, Hendricks JC. The relationship of excessive exploratory behavior in wakefulness to paradoxical sleep without atonia. Sleep. 1981;4:247-257
Jouvet M, Delorme F. Locus coeruleus et sommeil paradoxical. CR
Soc Biol. 1965;159:895-899
Ferini-Strambi L, Zucconi M. REM sleep behavior disorder. Clin
Neurophysiol. 2000;111 Suppl 2:S136-140
Hendricks JC, Morrison AR, Mann GL. Different behaviors during paradoxical sleep without atonia depend on pontine lesion site.
Brain Res. 1982;239:81-105
Fantini ML, Ferini-Strambi L, Montplaisir J. Idiopathic REM sleep
behavior disorder: toward a better nosologic definition. Neurology.
2005;64:780-786
Maquet P, Peters J, Aerts J et al. Functional neuroanatomy of human
rapid-eye-movement sleep and dreaming. Nature. 1996;383:163166
Maquet P, Ruby P, Maudoux A et al. Human cognition during REM
sleep and the activity profile within frontal and parietal cortices:
a reappraisal of functional neuroimaging data. Prog Brain Res.
2005;150:219-227
Hobson JA, Pace-Schott EF, Stickgold R. Dreaming and the brain:
toward a cognitive neuroscience of conscious states. Behav Brain
Sci. 2000;23:793-842; discussion 904-1121
Pediatric Parasomnias—Mason and Pack
45. Chokroverty S HW, Walters AS. An approach to the patient with
movement disorders during sleep and classification. In: Chokroverty S HW, Walters AS, ed. Sleep and movement disorders. Philadelphia: Butterworth-Heinemann, 2003:201-218
46. Kohyama J, Shimohira M, Kondo S et al. Motor disturbance during REM sleep in group A xeroderma pigmentosum. Acta Neurol
Scand. 1995;92:91-95
47. Rye DB, Johnston LH, Watts RL, Bliwise DL. Juvenile Parkinson’s
disease with REM sleep behavior disorder, sleepiness, and daytime
REM onset. Neurology. 1999;53:1868-1870
48. Sheldon SH, Jacobsen J. REM-sleep motor disorder in children. J
Child Neurol. 1998;13:257-260
49. Iranzo A, Santamaria J. Severe obstructive sleep apnea/hypopnea
mimicking REM sleep behavior disorder. Sleep. 2005;28:203-206
50. Schenck CH, Bundlie S, Mahowald MW. REM Behavior Disorder (RBD): delayed emergence of parkinsonism and/or dementia in 65% of older men initially diagnosed with idiopathic RBD,
and an analysis of the minimum and maximum tonic and/or phasic
electtomyographic abnormalities found during REM sleep. Sleep.
2003;26:A316
51. Schenck CH, Bundlie SR, Mahowald MW. Delayed emergence of
a parkinsonian disorder in 38% of 29 older men initially diagnosed
with idiopathic rapid eye movement sleep behaviour disorder. Neurology. 1996;46:388-393
52. Boeve BF, Silber MH, Ferman TJ et al. Association of REM sleep
behavior disorder and neurodegenerative disease may reflect an underlying synucleinopathy. Mov Disord. 2001;16:622-630
53. Boeve BF, Silber MH, Parisi JE et al. Synucleinopathy pathology
and REM sleep behavior disorder plus dementia or parkinsonism.
Neurology. 2003;61:40-45
54. Stiasny-Kolster K, Doerr Y, Moller JC et al. Combination of ‘idiopathic’ REM sleep behaviour disorder and olfactory dysfunction as
possible indicator for alpha-synucleinopathy demonstrated by dopamine transporter FP-CIT-SPECT. Brain. 2005;128:126-137
55. Montagna P. Sleep-related non epileptic motor disorders. J Neurol.
2004;251:781-794
56. Schenck CH, Bundlie SR, Ettinger MG, Mahowald MW. Chronic
behavioral disorders of human REM sleep: a new category of parasomnia. 1986 [classical article]. Sleep. 2002;25:293-308
57. Boeve BF, Silber MH, Ferman TJ. Melatonin for treatment of REM
sleep behavior disorder in neurologic disorders: results in 14 patients. Sleep Med. 2003;4:281-284
58. Schenck CH, Boyd JL, Mahowald MW. A parasomnia overlap disorder involving sleepwalking, sleep terrors, and REM sleep behavior disorder in 33 polysomnographically confirmed cases. Sleep.
1997;20:972-981
59. Mahowald MW, Schenck CH. Status dissociatus--a perspective on
states of being. Sleep. 1991;14:69-79
60. Ohayon MM, Zulley J, Guilleminault C, Smirne S. Prevalence and
pathologic associations of sleep paralysis in the general population.
Neurology. 1999;52:1194-1200
61. Paradis CM, Friedman S. Sleep paralysis in African Americans with
panic disorder. Transcult Psychiatry. 2005;42:123-134
62. Buzzi G, Cirignotta F. Isolated sleep paralysis: a web survey. Sleep
Res Online. 2000;3:61-66
63. Dahlitz M, Parkes JD. Sleep paralysis. Lancet. 1993;341:406-407
64. Levin R, Fireman G. Nightmare prevalence, nightmare distress, and
self-reported psychological disturbance. Sleep. 2002;25:205-212
65. Hublin C, Kaprio J, Partinen M, Koskenvuo M. Nightmares: familial aggregation and association with psychiatric disorders in a nationwide twin cohort. Am J Med Genet. 1999;88:329-336
66. Nielsen TA, Laberge L, Paquet J et al. Development of disturbing
dreams during adolescence and their relation to anxiety symptoms.
Sleep. 2000;23:727-736
67. Krakow B, Sandoval D, Schrader R et al. Treatment of chronic
nightmares in adjudicated adolescent girls in a residential facility. J
Adolesc Health. 2001;29:94-100
SLEEP, Vol. 30, No. 2, 2007
68. Stein MT, Heyneman EK, Stern EJ. Recurrent nightmares, aggressive doll play, separation anxiety and witnessing domestic violence
in a 9 year old girl. J Dev Behav Pediatr. 2004;25:419-422
69. Muris P, Merckelbach H, Gadet B, Moulaert V. Fears, worries, and
scary dreams in 4- to 12-year-old children: their content, developmental pattern, and origins. J Clin Child Psychol. 2000;29:43-52
70. Thiedke CC. Nocturnal enuresis. Am Fam Physician. 2003;67:14991506
71. Kajiwara M, Inoue K, Kato M et al. Nocturnal enuresis and overactive bladder in children: an epidemiological study. Int J Urol.
2006;13:36-41
72. Tietjen DN, Husmann DA. Nocturnal enuresis: a guide to evaluation and treatment. Mayo Clin Proc. 1996;71:857-862
73. Laberge L, Tremblay RE, Vitaro F, Montplaisir J. Development
of parasomnias from childhood to early adolescence. Pediatrics.
2000;106:67-74
74. Weissbach A, Leiberman A, Tarasiuk A et al. Adenotonsilectomy
improves enuresis in children with obstructive sleep apnea syndrome. Int J Pediatr Otorhinolaryngol. 2006
75. Bader G, Neveus T, Kruse S, Sillen U. Sleep of primary enuretic
children and controls. Sleep. 2002;25:579-583
76. Neveus T. The role of sleep and arousal in nocturnal enuresis. Acta
Paediatr. 2003;92:1118-1123
77. Umlauf MG, Chasens ER. Sleep disordered breathing and nocturnal
polyuria: nocturia and enuresis. Sleep Med Rev. 2003;7:403-411
78. Follenius M, Krieger J, Krauth MO et al. Obstructive sleep apnea
treatment: peripheral and central effects on plasma renin activity
and aldosterone. Sleep. 1991;14:211-217
79. Norgaard JP, Djurhuus JC, Watanabe H et al. Experience and current status of research into the pathophysiology of nocturnal enuresis. Br J Urol. 1997;79:825-835
80. Agargun MY, Kara H, Ozer OA et al. Nightmares and dissociative
experiences: the key role of childhood traumatic events. Psychiatry
Clin Neurosci. 2003;57:139-145
81. Agargun MY, Kara H, Ozer OA et al. Clinical importance of nightmare disorder in patients with dissociative disorders. Psychiatry
Clin Neurosci. 2003;57:575-579
82. Turkus JA, Kahler JA. Therapeutic interventions in the treatment of
dissociative disorders. Psychiatr Clin N Am. 2006;29:245-262
83. Ogden P, Pain C, Fisher J. A sensorimotor approach to the treatment
of trauma and dissociation. Psychiatr Clin N Am. 2006;29:263-279
84. Evans RW, Pearce JM. Exploding head syndrome. Headache.
2001;41:602-603
85. Jacome DE. Exploding head syndrome and idiopathic stabbing
headache relieved by nifedipine. Cephalalgia. 2001;21:617-618
86. Sachs C, Svanborg E. The exploding head syndrome: polysomnographic recordings and therapeutic suggestions. Sleep. 1991;14:263266
87. Winkelman JW. Clinical and polysomnographic features of sleeprelated eating disorder. J Clin Psychiatry. 1998;59:14-19
88. Lu ML, Shen WW. Sleep-related eating disorder induced by risperidone. J Clin Psychiatry. 2004;65:273-274
89. Paquet V, Strul J, Servais L et al. Sleep-related eating disorder induced by olanzapine. J Clin Psychiatry. 2002;63:597
90. Morgenthaler TI, Silber MH. Amnestic sleep-related eating disorder
associated with zolpidem. Sleep Med. 2002;3:323-327
91. Arnulf I, Zeitzer JM, File J et al. Kleine-Levin syndrome: a systematic review of 186 cases in the literature. Brain. 2005
92. Vetrugno R, Provini F, Plazzi G et al. Catathrenia (nocturnal groaning): a new type of parasomnia. Neurology. 2001;56:681-683
151
Pediatric Parasomnias—Mason and Pack