REM Behavior Disorder

Stephen H. Sheldon and Darius A. Loughmanee

REM sleep behavior disorder (RBD) is classified as a parasomnia usually associated with REM sleep. It has been defined as abnormal behaviors occurring during REM sleep that may cause injury to self or others or may result in sleep disruption.¹ Alternate names include onirism; stage 1 REM sleep, REM sleep without atonia, paradoxical sleep without atonia, and REM sleep motor parasomnia (RMP). As RBD has been noted only sporadically in the pediatric sleep medicine literature and consists mostly of case reports, the latter terminology (RMP) appears more appropriate when referring to this symptom complex in children and adolescents. It is unclear whether this complex and polysomnographic findings have similar implications in the pediatric population when compared to adults.

In 1975, a disorganized relation of tonic and phasic events during REM sleep was described in a patient with a tumor located in the brainstem.² RBD as a clinical entity was described by Schenck and colleagues in 1986 as a parasomnia that typically occurred in older male patients³ and was associated with synucleinopathic degenerative disorders (for example Parkinson disease, Lewy body dementia, and multiple system atrophy).^4,5 Certain medications have also been associated with RBD in adults including serotonin reuptake inhibitors.⁶ Although symptoms of RBD in childhood and adolescence were thought to be rare, there is increasing information that RBD, or a disorder that may fulfill criteria for this diagnosis, exists in the pediatric population.^7–9

Dream reports and nightmares are common in childhood.¹⁰ NREM sleep partial arousal disorders are also common. Differentiation of REM dream reports and mentation during partial arousals from NREM sleep is at times problematic since children will often report a story line when asked if they were having a ‘nightmare’ regardless of dream content, making diagnosis using adult criteria difficult. Similarly, since there are no systematic studies of RBD/RMP in children and adolescents and literature consists mainly of case reports, it is difficult to conclude RBD in adults and RBD/RMP in children are manifestations of the same disorder. Putative pathophysiological etiologies are speculative and complex.¹¹

Symptoms of RBD/RMP in children and adolescents are based on clinical history of movement and apparent dream enactment. Nonetheless, this may often be difficult to clinically differentiate from confusional arousals where there may be a report of a dream of being chased or attacked, agitation, and unusual and/or aggressive movements during a spell. Time of night and a history of NREM parasomnia may be helpful in differentiation. Symptoms of RBD in adults include talking, laughing, shouting, gesturing, and reaching, grabbing, arm flailing, punching, kicking, sitting up, leaping from bed, crawling, and running. Quiet walking is uncommon. These symptoms can be similar to symptoms classically associated with NREM partial arousal disorders including but not limited to sleep terrors, agitated sleepwalking, and confusional arousals. They may also be seen in patients with paroxysmal hypnogenic dystonia.

An essential feature of RBD/RMP is dream enactment.¹ This appears to be due to absence of normal REM sleep skeletal muscle atonia. Paradoxical muscle activity results in gross complex body movements allowing for ‘acting out’ dreams. Adults can typically report vivid dream recall following a spell. Dream recall may be more difficult to elicit and content may not be as clear in the pediatric patient.

Abnormalities of REM sleep that appear during polysomnographic recording include augmentation of chin muscle tone, increased chin or limb phasic twitching, excessive episodic limb movements, gross body jerking, somewhat purposeful movements and/or vocalizations, and occasional violent behavior.

Assessment of symptoms suggesting RBD/RMP can be problematic in children. This is particularly true of the dream report. Pediatric patients communicate perceptions differently than adults, tend to be more concrete in descriptions, and there may be impairment in the ability to adequately verbalize symptoms and/or dream content. Additionally, there may be considerable ‘programming’ of the child’s report by parents/caretakers. When clinical history is difficult to interpret, the child’s behavior at the time of the dream might be helpful.⁸

Medical and scientific literature regarding RBD/RMP in children consists mainly of case reports. In 1975, Barros-Ferreira et al. described an 8-year-old female with an infiltrating pontine tumor.² The patient presented with symptoms of agitation at night along with mouth movements, somniloquy, and laughing during sleep. These clinical findings were associated with reported disorganized relationships of phasic and tonic REM sleep. Subsequently, Schenck and colleagues¹² described a syndrome of excessive restlessness and complex stereotypic movements during sleep in a 10-year-old following the removal of a midline cerebellar astrocytoma. These were associated with intermittent loss of REM atonia associated with some of these complex movements and frequent episodic limb movements in REM and NREM sleep. Interestingly, the patient’s 8-year-old brother had similar polysomnographic findings, without clinical symptoms.

In 1998, five patients who were evaluated for unusual behaviors during sleep associated with unusual nightmares, displacement from the bed, and sleep-related motor activity were reported.⁷ Dissociated state of REM sleep was suspected because limb movements and/or body movements were associated with vivid dream recall, nightmares associated with dream enactment, or injurious motor activity during sleep. Five matched comparison subjects who had been referred for evaluation of pediatric obstructive sleep apnea were chosen since movement and electrocortical arousals were common following occlusive and/or partially occlusive respiratory events, particularly during REM sleep. There were more reports of nightmares, excessive muscle tone during REM sleep, more frequent gross body movements, and increased phasic chin muscle activity (without increased eye movement activity) during REM sleep in subjects with RMP.

REM sleep motor abnormalities have also been reported in patients with autistic spectrum disorder,¹³ seizures,¹⁴ post-traumatic stress disorder,¹⁵ hereditary quivering chin with tongue biting,¹⁶ and Tourette’s syndrome.¹⁷

Nevsimalova and colleagues have reported RMP as the presenting symptom of narcolepsy–cataplexy in two children.¹⁸ Presenting symptoms included excessive daytime sleepiness and sporadic cataplectic attacks. Diagnosis of narcolepsy–cataplexy was established based on short sleep latency on standard MSLT testing, multiple sleep onset REM periods, low cerebrospinal fluid hypocretin levels, and the presence of human leukocyte antigen (HLA)-DQB1*0602. Along with the onset of EDS and cataplexy, the patients exhibited restless sleep, nightmares, and movements during sleep, somniloquy, and harmful behaviors. RBD has been reported in about one-third of adults with narcolepsy-cataplexy.¹⁹

Lloyd and colleagues ⁹ retrospectively evaluated 15 patients with symptoms of RMP and REM sleep without atonia. Mean age at diagnosis was 9.5 years with a range of 3–17 years. Nightmares were reported in 13 of the patients. Excessive daytime sleepiness was noted in about half. Other comorbid states included anxiety, attention deficit disorder, developmental delay, Smith–Magenis syndrome, pervasive developmental disorder, narcolepsy, idiopathic hypersomnia, and Moebius syndrome. Reviewing both presentations and response to therapy (including benzodiazepine, melatonin) and response to discontinuing a tricyclic medication, it was concluded that RMP may be associated with neurological abnormalities, narcolepsy, or medication. It seems to be distinct from NREM partial-arousal disorders and adult RBD. Although Rye and colleagues²³ reported REM sleep without atonia, dream enactment, and excessive daytime sleepiness in a patient with juvenile Parkinson’s disease, neurodevelopmental disorders, narcolepsy, and medication effect occur in some patients, but specific neurodegenerative disorder appears to be quite uncommon.

Limited evidence exists regarding appropriate treatment for RMP in children. Treatments have typically been guided by those that have been successful in adults. About 90% of adult patients with RBD clinically respond well to clonazepam at doses from 0.5 to 2.0 mg.²⁰ Use of clonazepam may be limited in children due to its long half-life and duration of action. A shorter-acting benzodiazepine (for example, lorazepam) may be better tolerated by children and anecdotally has been as effective as clonazepam without a residual daytime ‘hangover’ effect noted to be associated with long-acting benzodiazepines. In adults, there has been little, if any, tendency for the development of tolerance, dependency, abuse, or sleep disruption with clonazepam for long-term treatment of RBD.

In summary, RMP appears to represent state dissociation during REM sleep associated with paradoxical motor activity and vivid dream recall that can result in injury in children and adolescents. This motor dyscontrol may be a final common pathway for a variety of disorders ranging from narcolepsy–cataplexy, to post-traumatic stress disorder,7,16,17 and autistic spectrum disorder.^8,21 Interestingly, early in development, motor activity during REM sleep is common and normal, resulting in the term ‘active sleep.’ Therefore, RMP may also occur in otherwise normal children and represent dysfunction of maturation, particularly in the pontine tegmental region.^21,22 By clinical history alone, other more commonly recognized childhood parasomnias, such as confusional arousals, sleepwalking, and sleep terrors, might be considered. However, these NREM partial-arousal disorders are characteristically associated with amnesia for the event, absence of vivid dream recall, and occur during the first third to first half of the sleep period. Nonetheless, diagnosis can be difficult and requires a high index of suspicion. When symptoms suggestive of RMP occur in children or adolescents, underlying etiologies and/or comorbidities require comprehensive evaluation. RMP requires further research and longitudinal studies aimed at epidemiology, pathophysiology, and predictive significance of REM sleep motor dyscontrol during childhood.