Non–Rapid Eye Movement Sleep and Overlap Parasomnias

Home , Automatic behavior, Confusional arousals, Night eating syndrome, Pica (disorder), Rapid eye movement sleep, Sleep

Review Article

Address correspondence to Dr Muna Irfan, G8 Minnesota Non–Rapid Eye Regional Sleep Disorders Center, Hennepin County Medical Center, 900 South Movement Sleep and 8th St, Minneapolis, MN 55415, [email protected]. Relationship Disclosure: Overlap Parasomnias Dr Irfan reports no disclosure. Dr Schenck has received personal compensation as a MunaIrfan,MD;CarlosH.Schenck,MD;MichaelJ.Howell,MD,FAAN consultant for Sunovion Pharmaceuticals, Inc. Dr Howell serves as an associate editor for ABSTRACT MedLink.com and Purpose of Review: This article reviews the spectrum of nonYrapid eye movement has received personal (non-REM) sleep parasomnias, including sleepwalking, confusional arousals, and sleep compensation for speaking engagements from the Sleep terrors, which represent the range of phenotypic disorders of arousal from non-REM Performance Institute. sleep that occurs in children and adults. Dr Howell receives royalties Recent Findings: The International Classification of Sleep Disorders, Third Edition from UpToDate, Inc and research/grant support (ICSD-3) classifies parasomnias according to the sleep stage they emerge from: REM, from the National Institutes non-REM, or other. Demographics, clinical features, and diagnosis of non-REM of Health. parasomnias are reviewed in this article, and an up-to-date synopsis of guidelines for Unlabeled Use of management strategies to assist in the treatment of these sleep disorders is provided. Products/Investigationl Use Disclosure: Summary: The non-REM parasomnias are most common in children and adolescents Drs Irfan, Schenck, and but may persist into adulthood. They can be distinguishable from REM parasomnias Howell discuss the and nocturnal epilepsies, and, importantly, may lead to injury. Additionally, other unlabeled/investigational use of benzodiazepines and parasomnias in this spectrum include sleep-related eating disorder and sexsomnia. melatonin for the treatment Overlap parasomnia disorder includes one or more manifestations of a non-REM of parasomnias. parasomnia seen in combination with REM sleep behavior disorder, representing an * 2017 American Academy apparent erosion of the normally distinct stages of non-REM and REM sleep. A similar of Neurology. yet much more extreme dissociation of states underlies agrypnia excitata and status dissociatus, which represent rare, severe dissociations between non-REM, REM, and wake states resulting clinically in oneiric behaviors and severe derangement of normal polysomnographic wake and sleep stage characteristics. Management of non-REM and overlap parasomnias and state dissociation disorders include ensuring bedroom safety and prescription of clonazepam or hypnosis, in select cases, although in children and adolescents with noninjurious behaviors, non-REM parasomnias are often age-limited developmental disorders, which may ultimately remit by adulthood, and, in these cases, counseling and education alone may suffice. Timely and accurate recognition of the non-REM and overlap parasomnias is crucial to limiting potential patient injury.

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INTRODUCTION ‘‘other’’ in the International Classifica- Parasomnias are characterized by abnor- tion of Sleep Disorders, Third Edition mal nocturnal behaviors, experiences, [ICSD-3]) (Table 6-1).1 The key common and autonomic responses emanating clinical characteristics of non-REM para- from sleep.1 Parasomnias are catego- somnias are recurrence of episodes of rized according to the sleep stage they incomplete awakening from sleep and emerge from as rapid eye movement amnesia. These episodes can have vari- (REM) sleep parasomnias, non-REM able clinical presentations of disruptive sleep parasomnias, or state-independent abnormal behavior, such as ambulation, parasomnias (which are classified as eating, and talking during sleep. If

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KEY POINTS h the patient’s family. The general criteria Parasomnias are TABLE 6-1 Classification of categorized according a,b for disorders of arousal from non-REM Parasomnias 1 to the sleep stage they sleep are outlined in Table 6-2. emerge from as rapid b Non-Rapid Eye Movement eye movement sleep Sleep Parasomnias PATHOPHYSIOLOGY OF Y NON–RAPID EYE MOVEMENT parasomnias, non rapid Confusional arousals eye movement sleep SLEEP PARASOMNIAS Sleepwalking (somnambulism) parasomnias, or other The varying clinical phenotypes of Sleep terrors (state-independent) disorders of arousal from non-REM Sleep-related eating disorder parasomnias. sleep include confusional arousals, Sexsomniac h NonYrapid eye sleepwalking, and sleep terrors; all b movement parasomnias Other Parasomnias these share the same presumed un- occur mostly during Exploding head syndrome derlying pathophysiologic mechanism slow-wave sleep Sleep-related hallucinations of an incomplete transition from non- (sleep stage N3) but Sleep enuresis REM sleep to the awake state when can also arise from Parasomnias due to a sleep-wake boundary dyscontrol oc- sleep stage N2. medical disorder curs. Non-REM parasomnias occur h Any factor increasing Parasomnias due to a mostly during slow-wave sleep (sleep the propensity for medication or substance stage N3) but can also arise from sleep fragmentation Parasomnia, unspecified sleep stage N2.2 Several physio- (eg, pain, restless legs b Isolated Symptoms syndrome symptoms logic phenomena can precipitate the Sleeptalking (somniloquy) and periodic limb occurrence of these parasomnias by b movements, obstructive Parasomnia Overlap impairing complete cortical arousal c sleep apnea events, or Disorders out of the sleep state. Any factor in- c extrinsic stimuli such Status dissociatus creasing the propensity for sleep frag- as loud noises) can a Data from the American Academy of mentation (eg, pain, restless legs lead to partial cortical Sleep Medicine.1 syndrome [RLS] symptoms and peri- b arousal with impaired Excludes rapid eye movement (REM)Yrelated parasomnias. odic limb movements, obstructive consciousness. c Not included in the International sleep apnea [OSA] events, or extrinsic Classification of Sleep Disorders, stimuli such as loud noises) can lead Third Edition. to partial cortical arousal with impaired consciousness.3 Disorders of arousal may be exacer- left untreated, the nocturnal episodes bated by conditions that promote the can lead to clinical consequences in the homeostatic sleep drive, such as sleep patient, such as injuries and distress to deprivation and sedating medications,

a TABLE 6-2 General Diagnostic Criteria for Disorders of Arousal

A. Recurrent episodes of incomplete awakening from sleep B. Lack of or inappropriate response to intervention or redirection during episodes C. Limited or no cognition or dream imagery D. Partial or complete amnesia for the event E. Nocturnal disturbance is not explained by other sleep, psychiatric, or medical disorder or medication/substance use a Data from the American Academy of Sleep Medicine.1

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. KEY POINT by increasing the threshold for arousal. walkingatchromosome20hasalso h 8 Conditions that These conditions hinder the normal been identified. Factors and conditions exacerbate disorders of sleep-wake transition by enhancing associated with the arousal parasomnias arousal include those sleep inertia and thus lead to emergence are listed in Table 6-3. that promote the of the abnormal nocturnal behavior. homeostatic sleep Pressman4 has eloquently conceptu- CONFUSIONAL AROUSALS drive, such as sleep alized a model for the non-REM disor- Confusional arousals are partial awak- deprivation and ders of arousal. A patient with an enings from slow-wave sleep, also sedating medications, intrinsic predisposition is primed by known as sleep drunkenness and by increasing the influences such as sedating medications Elpenor syndrome. The individual typi- threshold for arousal. that hinder normal cortical arousal. cally sits up in a disoriented state Consequently, precipitating factors such and has some automatic behavior, such as OSA or environmental disruption (eg, as mumbling, low-intensity vocaliza- noise) trigger a disordered arousal from tions, confused motoric activity without non-REM sleep (this is analogous to, yet distinct from, the 3P model for the etiology of insomnia disorder discussed TABLE 6-3 Factors and in the article ‘‘Chronic Insomnia Disor- Conditions der’’byAlonY.Avidan,MD,MPH, Associated With FAAN,andDavidN.Neubauer,MD,5 in Arousal Parasomnias this issue of Continuum). Non-REM parasomnia behaviors b Predisposing Factors are manifested as arousal associated Genetic factors with disorientation, amnestic behav- Human leukocyte antigen ior, and confusion. The individual (HLA) DQB1*05 and HLA becomes ensnared in a state between DQB1*04 alleles non-REM and wakefulness due to Chromosome 20q12-q13.12 locus disintegration of discrete boundaries Maturational factors between sleep and wake states. The physiologic responses are reminiscent Ambulating disorders of primordial instinctive behavioral Restless legs syndrome manifestations, such as locomotion, (for sleepwalking) b aggression, and feeding, in conjunction Priming/Precipitating Factors with amnestic behavior during these Enhancing slow-wave sleep nocturnal episodes.1 The higher preva- Sleep deprivation lence of non-REM parasomnias in the Circadian misalignment pediatric population also suggests that Impairing cortical arousal developmental immaturity of sleep- Central nervous system wake boundary regulation is an addi- suppressant drugs tional vulnerability factor that occurs at Increasing sleep fragmentation younger ages.1 Extrinsic stimuli In addition to the environmental and Periodic limb movements metabolic factors discussed, genetic ele- Obstructive sleep apnea ments have been suggested. Studies Medical disorders such have demonstrated a high prevalence as gastroesophageal of human leukocyte antigen (HLA) reflux disease DQB1*05:01 and HLA DQB1*04 alleles Psychiatric disorders in various non-REM parasomnias.6,7 An and stress autosomal dominant trait for sleep-

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KEY POINTS h Confusional arousals are ambulation, and sympathetic hyperac- having a history of sleepwalking, sup- partial awakenings from tivity. Confusional arousals are more portive of a significant hereditary influ- 13 slow-wave sleep. The common in pediatric populations, the ence. The prevalence of sleepwalking 9 individual typically sits prevalence being up to 17%, while in is decreased in adults, seen in only 1% 1,13 up in a disoriented state adults, the prevalence is reported to be to 4%, although a 2014 study pro- and has some only 3% to 4%.10 The episode is posed that noninjurious sleepwalking automatic behavior, typically brief in duration, lasting for is actually 12%, much higher than such as mumbling, a few minutes, and associated with previously recognized.14 low-intensity diminished or altered responsiveness The nocturnal episodes can range vocalizations, confused to external stimuli. Occasionally, the from aimless wandering to complex, motoric activity without event might be prolonged, particu- protracted, inappropriate behaviors, ambulation, and larly with sedative hypnotic use.11,12 such as urinating in the closet, driving sympathetic hyperactivity. Partial or complete amnesia is noted, an automobile, or leaving the house h Sleepwalking is the with an absence or only vague re- unclothed in extreme weather condi- disorder of arousal collection of the episode afterward. tions.1 During an episode, sleepwalkers manifesting with According to ICSD-3, several criteria typically do not respond to attempts at prominent ambulatory behavior. should be met for the diagnosis, as redirection. Forceful restraining is not outlined in Table 6-4.1 advised unless a high risk for injury exists. Occasionally, unintentional self- injurious actions, such as walking off a TABLE 6-4 Diagnostic Criteria balcony or operating a motor vehicle, for Confusional 15 Arousala can result in grave consequences. Sleepwalking tends to occur in the first A. The disorder fulfills general half of the night, akin to the other non- criteria for nonYrapid REM disorders of arousal, and is related eye movement sleep to the greater predominance of slow- disorders of arousal wave sleep (sleep stage N3) in the first B. The episodes consist of few hours of sleep. The ICSD-3 diag- patient demonstrating nostic criteria for sleepwalking are listed confused behavior after in Table 6-5. arousal while in bed In adults, sleepwalking is frequently C. Absence of terror or associated with other sleep disorders, ambulation out of bed such as RLS and OSA, as well as with a Data from the American Academy of Sleep Medicine.1 use of sedative hypnotic medications,

TABLE 6-5 Diagnostic Criteria SLEEPWALKING for Sleepwalkinga Sleepwalking (somnambulism) is the disorder of arousal manifesting with A. The disorder fulfills general Y prominent ambulatory behavior.1 A criteria for non rapid eye movement sleep large 2015 prospective study revealed disorders of arousal the overall pediatric prevalence (ages B. Arousals are associated 2.5 to 13 years) of sleepwalking to be with ambulation and 29.1%, with the peak observed at age other complex behaviors 10.13 The prevalence increased to out of bed 47.4% for children with one parent with a Data from the American Academy 1 a history of sleepwalking and up to of Sleep Medicine. 61.5% for children with both parents

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. KEY POINTS in particular, the commonly prescribed piercing scream at the onset of an abrupt h Sleep terrors consist of benzodiazepine receptor agonists. arousal with autonomic hyperactivity episodes of intense Other than the priming and precipitat- and behavioral manifestation of intense fright accompanied by ing conditions previously mentioned, fear. The prevalence of sleep terrors in loud crying or screaming other medical conditions such as viti- children varies widely, from 14.7% to in which the patient ligo, hyperthyroidism, migraines, fe- 56%.1,13 In adults, the prevalence is appears terrified and brile illness, head injury, encephalitis, reported as much lower at 2.2%,1,11 inconsolable. Increased stroke, and chronic pain syndrome with a relatively constant rate of 2.3% to autonomic activity have also been implicated.1,16 In addi- 2.6% in those 15 to 64 years of age, results in tachypnea, tion to the benzodiazepine receptor decreasing to 1% in those older than tachycardia, mydriasis, agonists,11 a wide variety of other 65 years of age.1 diaphoresis, and increased muscle tone. medication types have been implicated Sleep terrors consist of episodes of as provoking influences for sleep- intense fright accompanied by loud h Comprehensive historical walking, including antidepressants crying or screaming in which the pa- accounts of witnessed (amitriptyline, bupropion, paroxetine, tient appears terrified and inconsolable. events obtained from the patient and a collateral mirtazapine), antipsychotics (quetia- Increased autonomic activity results in historian, especially the pine, olanzapine), antihypertensives tachypnea, tachycardia, mydriasis, dia- 1 parents in children or a (propranolol, metoprolol), antiepi- phoresis, and increased muscle tone. bed partner in adults, is leptic drugs (topiramate), antiasthma Patients are generally amnestic for crucial for diagnosis of agents (montelukast), and antibiotics episodes of sleep terror, although parasomnia disorders. (fluoroquinolones).1,12 occasionally in adults, partial amnesia A common and clinically relevant might be noted with vague recollec- scenario is zolpidem-induced sleep- tion of a fragment of apparent dream walking, among other amnestic behav- mentation associated with the ex- iors during sleep, such as sleep-related perience, such as a description of the eating disorder, often associated with ceiling collapsing or a fire in the the predisposing factor of underlying bedroom.12 Typically, the behaviors RLS. Since RLS frequently mimics in- are noninjurious but can cause signifi- somnia,1 the use of hypnotic drugs in cant parental distress and sleep disrup- patients with RLS is unfortunately com- tion (Case 6-1). Attempts to console monandmayleadtosleepwalkingand the patient can lead to paradoxical other related amnestic behaviors during increase in aggression.12 The diagnostic sleep.12 Thus, caution may be indicated criteria for diagnosis of sleep terrors are when a sedative hypnotic is given to listed in Table 6-6.1 patients predisposed to ambulation due to RLS and motor restlessness or with CLINICAL EVALUATION OF underlying cognitive impairments, es- NON–RAPID EYE MOVEMENT pecially those with memory and execu- DISORDERS OF AROUSAL tive dysfunction that may disinhibit Comprehensive historical accounts of amnestic behaviors and the primitive witnessed events obtained from the instinct of locomotion; in these settings, patient and a collateral historian, es- sleepwalking and other amnestic behav- pecially the parents in children or a iors may emerge as complications of bed partner in adults, is crucial for the hypnotic therapy.11,12 diagnosis of parasomnia disorders. The patient’s signs during an event SLEEP TERRORS further aid in supporting the suspected Sleep terrors (also known as night terrors diagnosis (eg, in a patient with night or pavor nocturnus) are a dramatic terrors, the patient may exhibit tachy- disorder of arousal that start with a cardia, palpitations, and diaphoresis,

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Case 6-1 A 5-year-old girl presented with her parents, who described distressing nightly behaviors that had been occurring over the past year. After going to sleep at about 8:00 PM, she would awaken with a scream at about 11:00 PM seemingly confused and very difficult to console. Attempts to calm her only resulted in increased agitation. During an episode, the child would sweat profusely and breathe rapidly, and her heart raced. Her mother felt that during these episodes the girl was ‘‘possessed by a demon.’’ She recently contacted emergency services as she was convinced the child was having a seizure. These events lasted approximately 15 minutes, and then the girl fell back asleep. In the morning, she had no recollection of events. The child’s napping schedule had recently changed as she had started kindergarten, resulting in much shorter naps. She had a normal medical history. Her examination was normal. The patient was diagnosed with sleep terrors, and her parents were reassured that this condition did not represent a neurologic emergency. Efforts were made with the child’s school to allow for a longer nap, which led to resolution of the episodes. At 1-year follow-up, the sleep terrors had not recurred. Comment. This case demonstrates several clinical aspects typical of sleep terrors, including age-related onset during childhood, high parental concern, nighttime sleep disturbance, and association with a stressor such as change in school setting and daytime napping behaviors. In this case, liberalizing the patient’s daytime napping led to decreased sleep homeostatic drive at night and led to resolution of the child’s sleep terror events.

which help to distinguish the diag- somnography can be performed to nosis from other disorders of arousal assist in the diagnosis. such as sleepwalking). In cases in which details are not clear, video-EEG poly- DIFFERENTIAL DIAGNOSIS OF NON–RAPID EYE MOVEMENT PARASOMNIAS The non-REM disorders of arousal should TABLE 6-6 Diagnostic Criteria for Sleep Terrorsa be distinguished from other sleep-related disorders with potential similar clinical A. The disorder fulfills general presentation, which include REM sleep criteria for nonYrapid behavior disorder (RBD), sleep-related eye movement sleep epilepsy, sleep-related dissociative disor- disorders of arousal der, alcohol- and drug-related behavioral B. The arousal is characterized manifestations during sleep, OSA, and by sudden fright manifested psychogenic spells or malingering. by terrifying scream/ RBD may be differentiated from non- vocalization at the onset REM disorders of arousal by several C. Events comprising intense distinctive features, including complex fear and signs of autonomic arousal, mydriasis, dream enactment behaviors, which par- tachycardia, tachypnea, allel described dream mentation and and diaphoresis often involve defense against attack or a Data from the American Academy of aggression, and its more frequent oc- Sleep Medicine.1 currence in the second half of the night. Video-polysomnography can help

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. & KEY POINT differentiate these disorders, sometimes Potentially injurious h For pediatric directly by capturing actual events but & Potentially originating from parasomnias, the also by assessing for the loss of skeletal epileptogenic activity, if prior American Academy muscle atonia (as measured by EMG) evaluation has been inconclusive of Sleep Medicine during REM sleep, which is supportive These practice parameters further suggests performing of the alternative diagnosis of RBD. For recommend use of expanded EEG comprehensive more information on RBD, refer to the and EMG channels with good-quality video-polysomnography, article ‘‘Rapid Eye Movement Sleep video.18 with extended EEG and EMG montages if Behavior Disorder and Other Rapid For pediatric cases, the AASM sug- obstructive sleep apnea Eye Movement Sleep Parasomnias’’ by gests performing comprehensive video- Birgit HPgl, MD, and Alex Iranzo, MD,17 is suspected or polysomnography, with extended EEG parasomnia-related in this issue of Continuum. Sleep- and EMG montages if OSA is suspected arousals are violent. related epilepsy is exhibited by stereo- or parasomnia-related arousals are vio- typical repetitive behavior with bicycling, lent.19 The purpose of such an evalu- rocking, or running leg movements or, ation is to identify a reversible sleep less often, by episodic nocturnal wan- disorder for which treatment could dering episodes. In such cases, a full lead to resolution of the parasomnia EEG montage should be conducted and prevention of injury. Because of simultaneously with polysomnography their intermittent nature, nocturnal to delineate the nature of these events. episodes might not be recorded dur- A history of significant psychosocial ing a single-night study, but features pathology, including sexual abuse, such as non-REM sleep instability, should raise concern for a possible epileptiform abnormalities, and changes diagnosis of a dissociative disorder. in REM sleep atonia can help support Aggravating factors, such as RLS and a clinical diagnosis. The yield can be OSA, should also be carefully screened increased significantly by the com- for and addressed, since effective treat- bination of prior sleep deprivation ment of these sleep comorbidities may with forced awakening from auditory reduce the propensity that provoke stimuli, but this approach is only rarely arousals from non-REM sleep, thereby applied in clinical practice and should decreasing the occurrence of non-REM be pursued only with appropriate disorders of arousal. Clinical character- oversight, such as driving restric- istics of various parasomnias are listed tion before and after the study and in Table 6-7, and their polysomno- seizure/injury precautions in the sleep graphic findings are listed in Table 6-8. laboratory.19 In confusional arousals, sleep ter- POLYSOMNOGRAPHIC rors, and sleepwalking, a buildup of EVALUATION OF PARASOMNIAS hypersynchronous delta frequency EEG The American Academy of Sleep Medicine activity is variably associated with the (AASM) has published practice guidelines arousal from sleep or may occur pre- 18 for the evaluation of parasomnias. ceding the event. Following arousal, According to the AASM, comprehensive persistent slow cortical activity is var- in-laboratory video-polysomnography is iable, evolving into either normal wak- indicated if the parasomnias are: ing background alpha activity or a & Atypical or unusual in terms of age, return to the non-REM sleep state.12 A onset, duration, or specific behavior segment of a typical polysomnogra- & Frequent in occurrence, (more phic tracing of confusional arousal is than 2 or 3 times a week) illustrated in Figure 6-1.

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TABLE 6-7 Distinguishing Clinical Characteristics of Various Parasomnias

Autonomic Provoking Parasomnia Behavior Symptoms Amnesia Factors Sex Timing Duration Confusional Disoriented, Absent Present Sleep No First Several arousal simple to deprivation predominance, part of minutes, complex with forced but injurious night rarely movements awakening in males prolonged in the bed Sleepwalking Ambulation, Absent Present Sleep No First Several leaving the deprivation predominance, part of minutes to bed, with forced but injurious night prolonged wandering awakening, in males restless legs syndrome Sleep terrors Distraught, Present Present Sleep No First Several agitated, deprivation predominance, part of minutes screaming, with forced but injurious night inconsolable awakening in males Sleep-related High-calorie, Absent Present/ Sleep Females Usually Several eating bizarre variable deprivation, more than first minutes disorder eating after recall restless legs males part of arousal from syndrome, night sleep hypnotic use Sleep Loss of Absent Present Sleep Males Anytime Seconds to enuresis bladder deprivation, more than minutes control increased females while asleep fluid intake Sexsomnia Abnormal Absent Present Sleep Males Anytime Minutes sexual deprivation more than behavior females during sleep/partial arousal Rapid eye Dream- Absent Variable None Males About Seconds to movement enacting recall more than 2 hours minutes (REM) sleep movements/ females after behavior vocalizations sleep disorder onset

KEY POINT MANAGEMENT OF NON–RAPID modifications (eg, removing sharp or h The primary goal of EYE MOVEMENT PARASOMNIAS otherwise potentially harmful objects, managing parasomnias Various strategies to control non-REM furniture, and weapons from the bed- is to ensure the safety parasomnias are discussed below. room; securing windows and other out- of the patient lets; using door alarms) may prevent and cosleeper. Environmental Safety problematic consequences. Careful con- The primary goal of managing paraso- sideration should be given to addressing mniasistoensurethesafetyofthe any reversible predisposing, priming, or patient and cosleeper. Environmental precipitating factors, as discussed in the

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Non–Rapid Eye Sleep Movement (REM) REM Sleep Parasomnia Stage Instability Atonia Other Features Confusional Non-REM Present Present Hypersynchronous EEG arousal delta activity Sleepwalking Non-REM Present Present Restless legs syndrome Sleep terrors Non-REM Present Present Increased heart rate Sleep-related Non-REM Present Present Restless legs syndrome, eating disorder periodic limb movements, rhythmic masticatory muscle activity Sleep enuresis Non-REM/REM Present Present Sexsomnia Non-REM Present Present REM sleep REM Absent Absent Periodic limb movements, behavior irregular heart and disorder respiratory rate

EEG = electroencephalogram. section on pathophysiology. In particu- epines, 86% of patients showed signif- lar, treatment of any comorbid sleep icant improvement after an average KEY POINTS h disorders, such as OSA and RLS, and follow-up of 3.5 years with sustained Treatment of any removal of offending sedative agents benefit.21 Various serotonergic antide- comorbid sleep disorders, such as significantly reduce the occurrence of pressants have also been used for the 20 obstructive sleep apnea disorders of arousal. treatment of non-REM parasomnias, and restless legs especially for sleep terrors. One report syndrome, and removal Pharmacotherapy showed a substantial response to imip- of offending sedative If the parasomnia behavior persists ramine in two patients with sleep- agents significantly 22 after treatment of comorbid sleep con- walking and sleep terrors, while other reduce the occurrence ditions and removal of offending drugs case reports suggested convincing re- of disorders of arousal. 23 24 and precipitating factors, then pharma- sponses to trazodone or paroxetine. h Clonazepam is cologic intervention can be considered. Antidepressants may improve sleep frequently used as a The evidence basis for pharmacothera- terrors by virtue of serotonergic effects first-line agent to treat py of the parasomnias is extremely on the mesencephalic periaqueductal nonYrapid eye sparse and, at times, contradictory. gray matter.24 movement parasomnias Benzodiazepines and antidepressants Behavioral strategies, such as psycho- of disordered arousal, are the mainstay of pharmacotherapy, therapy, have also been employed for although other depending on the type of disorder of treatment of non-REM parasomnias with intermediate and arousal. Clonazepam is frequently used some success.25 For benign parasomnias long-acting benzodiazepines may as a first-line agent to treat non-REM such as confusional arousals and sleep also be used. parasomnias of disordered arousal, al- terrors in children, parents can be re- though other intermediate and long- assured about the generally noninjurious acting benzodiazepines may also be nature of the episodes and informed used. In a series of 69 patients with that events are frequently outgrown. sleepwalking and sleep terrors treated For persistent episodes of sleep ter- with clonazepam and other benzodiaz- ror in children, anticipatory awakenings

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FIGURE 6-1 A 30-second polysomnographic tracing showing an arousal arising from sleep stage N3 (slow-wave sleep) (red arrow), showing hypersynchronous slow-wave activity and increase in muscle tone followed by normal wakefulness.

KEY POINTS 15 to 20 minutes before the typical time eating disorders and incongruent with h For persistent episodes of occurrence has been shown to be other disorders of arousal.1,30 of sleep terrors in highly effective in aborting the epi- The episodes of sleep-related eating children, anticipatory sodes.25 Hypnotherapy has also been in sleep-related eating disorder are not awakenings 15 to employed, with variable benefit from driven by hunger but seem to comprise 20 minutes before the 27% to 87% reported in different case involuntary compulsive eating after par- typical time of 26 occurrence has been series for non-REM parasomnias. tial arousal from sleep. Episodes consist shown to be highly of ingestion of peculiar combinations of effective in aborting SLEEP-RELATED EATING items; carbohydrate-rich foods; or ined- the episodes. DISORDER ible or toxic materials such as raw or h Sleep-related eating Sleep-related eating disorder is a con- frozen meat, pet food, or buttered disorder is a condition dition characterized by recurrent epi- cigarettes. Sleep-related eating disorder characterized by sodes of typically amnestic binge canleadtomultipleadverseconse- recurrent episodes of eating of high-calorie food and some- quences, such as weight gain, injuries typically amnestic binge times bizarre pica-type ingestions after sustained from careless handling of eating of high-calorie partial arousal from non-REM sleep. food items during an episode, precipi- food and sometimes The community prevalence of sleep- tation or exacerbation of diabetes bizarre pica-type related eating disorder is currently mellitus, hypercholesterolemia, or den- ingestions after partial not well characterized. Schenck and tal caries. The frequency of episodes Y arousal from non rapid colleagues27 found the prevalence of ranges from a few times a week to eye movement sleep. sleep-related eating disorder was 0.5% multiple times per night.1 The criteria in a sleep clinic referral population. In for diagnosis of sleep-related eating college students, the occurrence was disorder are listed in Table 6-9.1 4.6%,28 and sleep-related eating disor- The pathophysiologic mechanism of der was found to affect 3.4% of patients sleep-related eating disorder is not in a depression clinic.29,30 Sleep-related established, although it has been pro- eating disorder has a 60% to 83% posed that several heterogeneous female preponderance, consistent with factors may play a causative role. Most

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. KEY POINTS researchers agree that sleep-related eat- linergic drugs, have also been re- h 1 Most researchers agree ing disorder is a variant of sleepwalking ported. Several other factors have been that sleep-related eating since it is characterized by partial or associated with sleep-related eating disorder is a variant of incomplete arousals from sleep, in- disorder, including alcohol and other sleepwalking since it is volves ambulation culminating in feed- substance use, cessation of smoking, characterized by partial ing behavior, and is affected by the acute stress, onset of narcolepsy, auto- or incomplete arousals usual predisposing influences for non- immune hepatitis, and encephalitis.1 from sleep, involves REM disorders of arousal, especially Sleep-related eating disorders should ambulation culminating RLS, as well as other precipitating con- be distinguished from other conditions in feeding behavior, ditions as previously discussed.28 Pa- such as night eating syndrome and the and is affected by the tients with sleep-related eating disorder nocturnal occurrence of other eating dis- usual predisposing influences for nonYrapid share many similarities with somnam- orders, such as bulimia nervosa, binge eye movement disorders bulists, including that both conditions eating disorder, binge/purge type an- of arousal. originate from non-REM sleep and that orexia nervosa, and Kleine-Levin syn- h 60% of patients with sleep-related eating drome. Night eating syndrome is Night eating syndrome is characterized by disorder have a history of past or con- characterized by excessive eating at 1,27,30 excessive eating at night current sleepwalking (Case 6-2). night before bedtime or after awakening before bedtime or after Wakeful nocturnal eating is a common from sleep but, unlike sleep-related awakening from sleep nonmotor manifestation of RLS; thus, eating disorder, is associated with fully but, unlike sleep-related misclassification of RLS as insomnia preserved awareness and intentional eating disorder, is and resulting treatment with sedative eating. In contrast to daytime eating associated with fully hypnotic medication, especially zolpidem, disorders, compensatory behavior such preserved awareness can lead to the emergence of amnestic as induced vomiting or laxative use is and intentional eating. sleep-related eating disorder.11,12,31 not noticed in sleep-related eating Zolpidem is the most common disorder, although other eating disor- agentthatinducessleep-relatedeating ders can occur concurrently. Kleine- disorder, but a wide range of other Levin syndrome is a complex disorder psychotropic medications, including of recurrent periodic hypersomnia, benzodiazepines, mirtazapine, que- cognitive impairment, hypersexuality, tiapine, lithium carbonate, and anticho- and hyperphagia during wakefulness

a TABLE 6-9 Diagnostic Criteria for Sleep-Related Eating Disorder

A. Recurrent episodes of dysfunctional eating occurring after arousal from main sleep period B. Presence of at least one of the following with recurrent involuntary eating 1. Consumption of peculiar form or combination of food or inedible/toxic substances 2. Sleep-related injurious/potentially injurious behavior noted during food preparation/pursuit 3. Adverse consequences from recurrent nocturnal eating C. Partial or complete loss of awareness during the episode with subsequent impaired recall D. Disturbance is not explained by another sleep, mental, or medical disorder or medication/substance use a Data from the American Academy of Sleep Medicine.1

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KEY POINT h Dopamine agonists Case 6-2 and topiramate have A 44-year-old woman presented with amnestic nocturnal eating, which been used as had resulted in a 20 kg (44 lb) weight gain over the previous 6 months. pharmacotherapy She experienced events involving sleepwalking to the kitchen and eating for sleep-related large portions of chocolate, peanut butter, and crackers. She would eating disorder. often wake up with a distended abdomen and chocolate spread on her fingers. She was found once by her husband, who said that she was ‘‘in a trance.’’ These events occurred approximately 4 to 5 times per week. Her diabetes mellitus was poorly controlled, and her dentist found three new dental caries. These behaviors began after she started receiving zolpidem for ‘‘insomnia.’’ She had been reluctant to stop the drug since it was helping her fall asleep at night. However, further careful history revealed that she did not have hypervigilant insomnia, but instead her difficulty falling asleep was related to overwhelming discomfort in her legs compelling her to move her legs and walk at night. Before zolpidem therapy, she would often spend hours awake at night ambulating through the house and sometimes having a small snack. The patient was diagnosed with sleep-related eating disorder and restless legs syndrome (RLS). Zolpidem was discontinued and pramipexole started, which resolved the difficulty with sleep initiation, and she had no further episodes of sleep-related eating disorder. Comment. This case is a classic example of insomnia caused by RLS mistreated with zolpidem. She had no recollection of the nocturnal eating episodes with preference for carbohydrate-rich food items, which led to consequences such as poor oral hygiene and hyperglycemia. Thus, it is important to recognize this condition and address it in a timely manner. The treatment of underlying RLS not only improved her insomnia but also controlled the sleep-related eating disorder episodes.

with eventual return to baseline and pharmacotherapy for sleep-related thus can be easily separated from the eating disorder. In an original case symptomatology of sleep-related eating series, Schenck and colleagues33 disorder. For more information on showed improvement in 52% of pa- Kleine-Levin syndrome, refer to the tients (14 of 27) who received do- article ‘‘Narcolepsy and Other Central pamine agonist agents. A randomized Hypersomnias’’ by Yves Dauvilliers, controlled trial of pramipexole up to MD, PhD, and Lucie Barateau, MD,32 0.36 mg/d showed decrease in noc- in this issue of Continuum. turnal activity by actigraphy and sub- The goal of treatment in sleep- jective improvement in sleep.34 Topi- related eating disorder is to eliminate ramate has been proposed to exert any precipitating factors, such as hyp- anorexigenic actions.29 According to notic medications, and to recognize and Winkelman,35 68% of patients re- treat any contributing comorbid sleep sponded to topiramate, with a mean disorders, especially RLS. Removal of dose of 135 mg/d, but the discontinu- any offending drug, along with treat- ation rate was high because of side ment of RLS and OSA, has been shown effects. Schenck and Mahowald36 also to resolve many cases of sleep-related showed good response with topiramate eating disorder.29Y31 Dopamine agonists treatment, which was well tolerated and topiramate have been used as over 1.8 years.

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Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited. SEXSOMNIA KEY POINTS associated with Parkinson disease, on- h Sexsomnia is classified Neurologists should be aware of set was noted with the initiation or dose as a subtype of sexsomnia for several reasons. Neurolo- increase of pramipexole therapy. None nonYrapid eye gists are often consulted for evaluation of the patients had a prior history of movement parasomnia of unusual behaviors, including sleep- parasomnia, sexual disorder, or impulse disorders of arousal related abnormal sexual behaviors control disorder. A detailed medication in the International (sexsomnia). Rarely, sexual behavior history with the bed partner’s assis- Classification of Sleep may arise from nocturnal seizures, tance is critical in the evaluation of a Disorders, Third Edition. which can often be successfully treated, patient with sexsomnia, along with a h Parasomnia overlap andsexsomniamaybecomorbidwith detailed history of any parasomnia, disorder is a condition neurologic disorders such as Parkinson sleep-disordered breathing, medical- with clinical features of disease and narcolepsy. neurologic-psychiatric problems, or both nonYrapid eye The first classification of sleep- family history. movement sleep related disorders associated with Treatment data are limited; however, parasomnias and rapid abnormal sexual behaviors and expe- in one series, 86% of patients had eye movement sleep behavior disorder. riences was published in 2007,37 with control of sexsomnia with bedtime clo- an update in 2015.38 Sexsomnia and nazepam, and 100% (4 of 4) of patients sleep-related eating disorder are con- with comorbid OSA had resolution with sidered ‘‘appetitive’’ parasomnias, and control of OSA on nasal continuous they can be comorbid in the same positive airway pressure. patient. Sexsomnia is classified as a Ten cases of ictal/presumed ictal subtype of non-REM parasomnia dis- sexsomnia have been described, dem- orders of arousal in ICSD-3,1 with onstrating a striking contrast between sexual behaviors that emerge during thehighrateofrecallforictal partial arousals from slow-wave (delta sexsomnia episodes and the virtually or stage N3) sleep, as is typical of the complete amnesia for sexsomnia other non-REM parasomnias. (parasomnia) episodes in all but two In a large series of 49 patients, cases. In the 5 of 7 patients with sexsomnia was male predominant reported treatment data, antiepileptic (75%), with a mean age of onset of drug therapy completely suppressed 28 years and mean age at presentation the ictal sleep-related sexual seizures.38 of 35 years. A broad range of sexual behaviors was reported, including sex- PARASOMNIA OVERLAP ual intercourse/attempted intercourse DISORDER (49%), fondling the bed partner (40%), Parasomnia overlap disorder is a con- agitated/assaultive sexual behaviors dition with clinical features of both (37%), masturbation (23%), sexsomnia non-REM parasomnias and RBD. While with minors (20%), sexual vocaliza- overlap parasomnia disorder is cur- tions (19%), and spontaneous sleep rently classified as a subtype of REM orgasm (4%). Not surprisingly, sex- parasomnias,1 some believe it may be somnia can lead to adverse legal a distinct entity because of several consequences. The forensic implica- differentiating features, such as occur- tions of sexsomnia have recently been rence at a younger age and more reviewed.38 Shift work was a trigger for frequent presentation with non-REM sexsomnia in one predisposed patient, parasomnias compared to REM-related and selective serotonin reuptake in- behaviors.39,40 Overlap parasomnia hibitor (SSRI) therapy for depression disorder can also be seen secondary was a trigger for sexsomnia in another to various disorders such as narco- patient. In four cases of sexsomnia lepsy, multiple sclerosis, brain tumors,

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KEY POINTS h Status dissociatus is a rhombencephalitis, brain trauma, ciation with alcohol withdrawal, Morvan state of complete spinocerebellar ataxia type 3, psychi- syndrome, or fatal familial insomnia 1 disintegration of wake/ atric disorders, substance abuse, and andotherpriondiseases. These pa- 1,41 nonYrapid eye alcohol withdrawal. Polysomno- tients exhibit gestures mimicking semi- movement/rapid eye graphic evaluation demonstrates the purposeful tasks in a confused halluci- movement sleep presence of non-REM parasomnias natory state, termed as oneiric stupor, boundaries that is and non-REM sleep architecture insta- which is the behavioral marker of without identifiable bility as well as dream enactment be- agrypnia excitata.40,41 sleep stages and with havior in REM sleep with loss of normal Careful clinical history with poly- behavioral and REM sleep atonia (showing increased somnographic evaluation and diagnos- motor manifestations muscle tone during REM sleep). tic workup for a possible underlying of oneirism etiology are warranted. Management (dream-enactment Status Dissociatus behaviors). includes treating comorbid sleep dis- Status dissociatus is a state of com- orders such as OSA or RLS and h Agrypnia excitata is an plete disintegration of wake/non-REM/ optimization of sleep and environ- extreme form of status REM sleep boundaries that is without mental safety. Clonazepam is the most dissociatus, with identifiable sleep stages and with be- frequently used agent for this rare near-continuous motor 39,40 and sympathetic havioral and motor manifestations of parasomnia disorder. Alprazolam, hyperactivity, loss of N3 oneirism (dream-enactment behaviors). temazepam, carbamazepine, and mel- 40 sleep stage (slow-wave) An admixture of various polysomnogra- atonin use have also been reported. architecture, and phic markers of different states with For autoimmune etiologies, immuno- dissociation of unidentifiable sleep staging is noted, with therapeutic agents such as steroids, IV conventional nonYrapid the patient appearing asleep behaviorally immunoglobulin (IVIg), and plasma eye movement but having complex motor behavior exchange have been used in some sleep markers. typical of dream enactment. The patho- cases of status dissociatus associated physiologic basis is considered to be with autoimmune encephalopathy.39 related to ,-aminobutyric acidYmediated (GABA-ergic) thalamolimbic dysfunc- CONCLUSION tion.37 Status dissociatus can be seen Non-REM parasomnias include sleep acutely in alcohol withdrawal, subacutely terrors, confusional arousals, and in autoimmune encephalitis (associated sleepwalking and are most frequent in with antiYN-methyl-D-aspartate [NMDA] children and young adults. Non-REM receptor antibodies and antiYvoltage- parasomnias are typically benign in most gated potassium channel complex children; therefore, in most cases, pa- [VGKC] antibodies),40,42 and on a rental counseling, education, and watch- chronic basis in "-synuclein neurode- ful waiting can be undertaken. However, generative disorders such as Parkinson in adults, non-REM parasomnias can be disease, multiple system atrophy, and potentially injurious, so counseling and dementia with Lewy bodies. education to ensure a safe bedroom environment should be undertaken in Agrypnia Excitata all adult patients, and treatment with Agrypnia excitata is an extreme form of behavioral therapies (eg, hypnosis) or status dissociatus, with near-continuous pharmacotherapy with clonazepam motor and sympathetic hyperactivity, should be considered in cases with loss of sleep stage N3 (slow-wave) significant injury potential. Sexsomnia architecture, and dissociation of con- is less frequently reported but shares a ventional non-REM sleep markers such similar pathophysiology. Rare variants as K complexes and sleep spindles. of the non-REM parasomnias include Agrypnia excitata may be seen in asso- overlap parasomnia disorder, status

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