PARASOMNIAS INCLUDING THE RESTLESS LEGS SYNDROME

SLEEP DISORDERS 0272-5231/98 $8.00 + .OO

PARASOMNIAS INCLUDING THE RESTLESS LEGS SYNDROME

Mark W. Mahowald, MD, and Carlos H. Schenck, MD

Parasomnias are undesirable motor, verbal, or experiential phenomena that occur during the sleep period. They may be conveniently categorized as primary parusomnias (disorders of the sleep states per se), or secondary para- sornnius (disorders of other organ systems that manifest themselves during sleep). The primary sleep parasomnias can be classified ac- cording to the sleep state of origin (rapid eye movement [REMJ), non-rapid eye movement [NREM], or miscellaneous (those not respect- ing sleep state). Secondary sleep parasomnias can be further classified by the organ system involved.l1°

Integral to the understanding of parasomnias is the concept of state-dependent reorganization of the central nervous system (CNS). Until relatively recently, it was believed that sleep was a unitary phenomenon and simply represented the passive absence of wakefulness (W); a time of relative brain inactivity. In the 1930s, it was discovered that the brain is active during sleep. In 1953, it was discovered that sleep is actually a bimodal process-REM and NREM-indicating that, humans, as most mammals, spend their lives in three completely different states of being: W, REM sleep, and NREM sleep. Each of those states has its unique neuroanatomic, neurophysiologic, neurochemical, and neuro- pharmacologic correlates.l0. 78, 193, 206

There is compelling evidence that there is

extensive reorganization of CNS activity during sleep. Almost all portions of the nervous system are active across all three states of being-but active in a different mode. Multi- ple state-determining variables are recruited to occur in concert, resulting in the declara- tion of a given state. Parasomnias are clinical phenomena, which, by-and-large, are related to the changes in brain organization across states, and are particularly apt to occur during the transition periods from one state to another.lg1 Given the large number of neural networks, neurotransmitters, and other state- determining substances that must be recruited synchronously, and given the frequent transitions among the three states of being, it is surprising that parasomnias do not occur more frequently than they do. The concept of state dissociation in animals and humans has been reviewed extensively."*, 113 Figure 1 por- trays a simplified conceptualization of the overlapping nature of the various parasomnias. Table 1 lists the various primary and secondary parasomnias.

PRIMARY SLEEP PHENOMENA

In keeping with the previous discussion, key to understanding the primary sleep parasomnias is the concept that sleep and wakefulness are not invariably mutually exclusive

From the Minnesota Regional Sleep Disorders Center, Hennepin County Medical Center; and the Departments of Neurology (MWM) and Psychiatry (CHS), Hennepin County Medical Center and the University of Minnesota Medical School, Minneapolis, Minnesota

CLINICS IN CHEST MEDICINE

VOLUME 19 * NUMBER 1 MARCH 1998 183

184 MAHOWALD & SCHENCK

Hypnagogic hallucinations Disorders of Arousal Confusional arousals

Overlapping parasomnias

Status dissociatus

Figure 1. The overlapping nature of states and conditions associated with parasomnias. RBD = REM sleep behavior disorder; PTSD = post-traumatic stress disorder. (from Mahowald MW. Schenck CH: NREM sleep parasomnias. Neurology Clinics 14:677, 1996; with permission.)

states, and that the various state-determining variables of W, NREM, and REM sleep may occur simultaneously or oscillate rapidly. The admixture of W and NREM would explain confusional arousals (sleep-drunkenness), automatic behavior or "micro-sleeps."60, I4l, 160,

162,uo The tonic and phasic components of REM sleep may become dissociated, intrud- ing or persisting into W, explaining.cataplexy, wakeful dreaming, and the persistence of motor activity during REM sleep.115

Normal Rapid Eye Movement Phenomena

Conventional dreams are normal events that occur during REM sleep.

Dream anxiety attacks are simply frightening dreams, frequently associated with moderate autonomic activity (tachycardia, tachypnea, diaphoresis) and arousal. There is usually immediate return of complete alertness, with recollection of the dream events that resulted in arousal. The immediate postarousal alertness and the vivid memory of the dream content differentiate nightmares from disorders of a r~usa l .~

Drug-induced dreams: Although the sudden appearance or worsening of dream content or

nightmares may be a harbinger for exacerbation of psychiatric disease,64 it may also represent a medication effect. Impressive dreams and dream anxiety attacks have been reported in association with a myriad of commonly prescribed medications, particularly antihy- pertensive medications and virtually all anti- parkinsonian agents."O

The dissociation of the components of REM sleep may result in bizarre experiences and behaviors such as sleep paralysis and hypnagogic (occurring at sleep onset) or hypnopompic (occurring upon awakening) hallucinations. Such symptoms may occur in normal individuals, particularly in the setting of sleep deprivation, and are occasionally misinterpreted by the afflicted individual or the consulting physicianls2 as manifestations of psychiatric disease. In the absence of other symptoms of narcolepsy, such as hypersomnia or cataplexy, further evaluation is unwarranted.

Abnormal Rapid Eye Movement Phenomena

REM sleep behavior disorder (RBD) is a fascinating experiment of nature. It was predicted by animal experiments in 1965 when cats with bilateral perilocus ceruleus pontine le-

PARASOMNIAS INCLUDING THE RESTLESS LEGS SYNDROME 185

Table 1. CLASSIFICATION OF THE PARASOMNIAS

I. Primary sleep phenomena A. Rapid eye movement sleep phenomena

1. Normal a. Conventional dreams b. Dream anxiety attacks (nightmares) c. Drug-induced dreams

a. Rapid eye movement sleep behavior disorder 2. Abnormal

B. Non-rapid eye movement sleep phenomena 1. Normal

a. Hypnagogic imagery b. Sleep starts (hypnic jerks)

2. Abnormal-disorders of arousal a. Confusional arousals b. Sleepwalking c. Sleep terrors

C. Miscellaneous 1. Bruxism 2. Enuresis 3. Rhythmic movement disorder 4. Restless legs syndrome and the periodic limb movement disorder 5. Posttraumatic stress disorder 6. Somniloquy

11. Secondary sleep phenomena A. Central nervous system

1. Seizures 2. Headaches

B. Cardiopulmonary 1. Cardiac arrhythmias 2. Nocturnal angina pectoris 3. Nocturnal asthma 4. Respiratory dyskinesias 5. Sleep hiccup 6. Miscellaneous

C. Gastrointestinal 1. Gastroesophageal reflux 2. Diffuse esophageal spasm

1. Panic attacks 2. Psychogenic dissociative states. 3. Malingering 4. Nocturnal leg cramps

D. Miscellaneous

111. Parasomnias of particular interest to pulmonologists A. Obstructive sleep apnea-induced arousals resembling rapid eye movement sleep behavior disorder B. Rapid eye movement sleep behavior disorder protection against obstructive sleep apnea C. Obstructive sleep apnea-induced confusional arousals resembling disorders of arousal D. Nasal continuous positive airway pressure treatment of obstructive sleep apnea, inducing disorders of arousal E. Compromise of nasal continuous positive airway pressure treatment by disorders of arousal F. Obstructive sleep apnea-induced arousals associated with sleep-related eating

G. Sleep-related eating resulting in weight gain, resulting in obstructive sleep apnea H. Obstructive sleep apnea-induced sleep-related seizures I. Obstructive sleep apnea-induced cerebral anoxic attacks

sions demonstrated prominent motor activity during REM sleep. That was termed REM sleep without atoniu. RBD was not formally recognized and named in humans until the mid 1980~.'~*

REM-atoniu represents an active paralysis involving specific neuronal circuitry, and not passive relaxation of somatic muscles (spar- ing the diaphragm, permitting respiration during REM sleep). In normal REM sleep, the

motor system is paralyzed at the level of the spinal motoneurons, but highly activated at higher levels of the neuraxis.'86 It is likely that the REM-atonia may serve as a protective mechanism, preventing motor manifestations and accompaniments of the highly activated brain during REM sleep.

The typical complaint of a patient with RBD is violent dream-enacting behaviors that are potentially injurious to the individual or


El -A1

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EKG

F7 - T3

T3 - T5

T5 - 01 F8 - T4

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T6 - 0 2

Nasal Airflow (Thermocouple)

Figure 2. Polysomnographic correlates of dream-enacting behaviors in REM sleep behavior disorder (RBD). REM sleep contains dense, high-voltage REM activity (1 and 2), and there is a fast-frequency, low-voltage, desynchronized electroencephalogram (EEG) (3-5, 12-1 7) characteristic of REM sleep. The submental EMG muscle tone is increased (6), as is seen often with RBD. The arms (7 and 8) and legs (9 and 10) show bursts of intense twitching that accompany observable behaviors noted by the technician. This sequence culml:nates in a spontaneous awakening when the patient reports a terrifying dream. (From Mahowald MW, Schenck CH: REM sleep behavior disorder. In Kryger MH, Roth T, Dement WC (eds): Principles and Practice of Sleep Medicine, ed 2. Philadelphia, WB Saunders, 1994, p 580; with permission.)

bed partner. Acute and chronic forms of RBD exist. The acute form of RBD can emerge during withdrawal from ethanol or sedative- hypnotic abuse and with anticholinergic and other drug intoxication states. Few studies are available on the acute form, because it is transient and often associated with impressive symptoms of withdrawal, making formal sleep studies technically difficult to perform and interpret.173, 176

The chronic form most often presents to the physician for evaluation. The older (more than age 50 years) and male predominance (80% to 90'/0) in RBD is overwhelming, although females and virtually all age groups are represented. One quarter of the patients have a prodrome, often lengthy, involving subclinical behavioral release during sleep.

It is important to realize that RBD behaviors occur within REM sleep, often without associated tachycardia, and not during arousals from REM sleep (Fig. 2). There is a strong link between altered dreams and dream-enacting behaviors, suggesting a mutual pathophysiology: Patients do not enact their cus- tomary dreams, but rather they enact distinctly altered dreams, usually involving confrontation, aggression, and violence. De- spite the impressive behavioral and electro- myographic (EMG) motor activity, few patients with RBD complain of excessive sleep disruption and daytime fatigue, and multiple sleep latency testing rarely documents daytime somnolence, the exception being those cases in which RBD is associated with (and another manifestation of) narcolepsy.


Some cases have an identifiable underlying neurologic disorder, but many are idiopathic. Extensive neurologic evaluation (evoked po- tentials, CT, MR images, etc.) is warranted only if the history or neurologic examination is suggestive of structural CNS pathology.*76

The minimum diagnostic criteria of RBD are:

1. Polysomnographic (PSG) abnormality during REM sleep: elevated submental EMG tone or excessive phasic submental or limb EMG twitching

2. Documentation of abnormal REM sleep behaviors during PSG studies (prominent limb or truncal jerking; complex, vigorous, or violent behaviors), or a history of injurious or disruptive sleep behaviors

3. Absence of EEG epileptiform activity during REM sleep

The PSG and behavioral features of RBD are indistinguishable-regardless of gender, age, or presence/absence of an underlying neurologic disorder. That suggests the presence of a "final common pathway" in RBD that can be accessed by a wide variety of pathologic states.

Clonazepam is a remarkably effective treatment in human RBD, controlling both the behavioral and dream-disordered components of RBD. Treatment is usually immediately effective at a dose of 0.5 to 1 rng at bedtime (range, 0.25-4 mg). Prompt relapse of RBD occurs whenever the patient fails to take clonazepam on a given night. Despite the dramatic control of the clinical symptoms, clonazepam has little effect on the characteristic PSG REM sleep abnormalities. Nightly clonazepam is effective and safe, without development of tolerance over many years. Adjunctive or alternative treatments, based on anectotal reports, for the few RBD patients who do not respond fully to clonazepam or who develop daytime somnolence from the agent, include desipramine or imipramine; carbamazepine; clonidine, carbidopa/L-dopa and L-tryptophan, melatonin, or gabapentin.

There is an association between RBD and extrapyramidal disease. Apparently idiopathic RBD may be the initial manifestation of a later-appearing extrapyramidal disorder such as multiple-system atrophy or Parkinson's d i s e a ~ e . ' ~ ~ , ~ ~ , 227 In one series, 38% of patients initially diagnosed as having idiopathic RBD subsequently developed parkinsonism a mean of 3.7 years after the diagnosis

of RBD, and a mean of 12.7 years after the initial onset of RBD symptoms. REM sleep without atonia and fully developed RBD may also be seen in patients with parkinsonism.17* Ongoing neurologic evaluation of patients with RBD, therefore, is warranted, looking for signs of extrapyramidal disease.

In addition, an association between RBD and narcolepsy has been well documented. The demographics of combined narcolepsy/ RBD are those of narcolepsy (not older males), indicating that RBD in narcolepsy is yet another manifestation of the "state bound- ary dyscontrol" of that condition. Treatment of cataplexy (with tricyclic antidepressants) may induce or aggravate RBD.167

A condition termed status dissociatus is the most extreme form of RBD, and appears to represent the complete breakdown of state- determining boundaries. The patients, by behavioral observation, appear to be either awake or asleep; clinically, their behavioral "sleep" is atypical, however, characterized by frequent muscle twitching, vocalization, and reports of dream-like mentation upon spontaneous or forced awakening. Polygraphically, there are few, if any, features of either conventional REM or NREM sleep; rather, there is the simultaneous admixture of elements of W, REM sleep, and NREM sleep. Conditions associated with status dissociatus include protracted withdrawal from alcohol abuse, narcolepsy, olivopontocerebellar degenera- tion, and prior open heart surgery. Clona- zepam may be effective in treating the sleep- related motor and verbal behaviors.'12, *I3

Normal Non-Rapid Eye Movement Sleep Phenomena

A number of normal NREM phenomena may result in clinical symptoms or complaints; these include hypagogic imagery and sleep starts.

Contrary to popular opinion, dreaming is not confined to REM sleep, instead occurring during all stages of sleep-both REM and NREM-and even during relaxed wakefulness while alpha rhythm is present on the electroencephalogram (EEG).%, 50, 52* 207 Conse- quently, the report of dream-like experiences occurring at sleep onset does not necessarily imply REM-onset sleep and therefore should not be used as a marker for narcolepsy.

Sleep starts (hypnic jerks) are experienced by many normal individuals during the tran-


sition between wake and sleep. The most common is the motor sleep start, a sudden jerk of all or part of the body, occasionally awakening the victim or bed partner.'& Varia- tions on that theme include visual (flashes of light, fragmentary visual hallucinations), auditory (loud bangs, snapping noises), or somesthetic (pain, floating, something flow- ing through the body) sleep starts. The sen- sory phenomena may occur without the body jerk.33, 52, lo7, Sleep starts represent a normal (although not understood) physiologic event, and should not be confused with seizures or other neurologic conditions.

Abnormal Non-Rapid Eye Movement Phenomena

Disorders of arousal are the most impressive and most frequent of the NREM sleep phenomena. They share common features- pa- tients have a positive family history, suggesting a genetic component; they tend to arise from slow-wave sleep (stages 3 and 4 of NREM sleep), therefore usually occurring in the first third of the sleep cycle (and rarely during naps); and they are common in childhood, usually decreasing in frequency with increasing age?, 13, 47, 63, Although the disorders of arousal occur most frequently during the deepest stages of NREM sleep (stages 3 or 4, or slow-wave sleep), they may occur during any stage of NREM sleep, and may occur late in the sleep period.139 Disorders of arousal occur on a broad spectrum, ranging from confusional arousals, through somnambulism (sleep walking), to sleep terrors (also termed pavor nocturnus). Some take the form of "specialized" behaviors such as sleep- related eating and sleep-related sexual activity-without conscious awareness.

Confusional arousals (also termed sleep drunkenness) are often seen in children, and are characterized by movements in bed, occasionally, thrashing about, or inconsolable

Sleepwalking is prevalent in childhood (1?'0- 17%), peaking at 11 to 12 years of age, and is far more common in adults (4%-10%) than generally acknowledged.20, 5 4 ~ 70, 90 Sleep- walking may be either calm or agitated, with varying degrees of complexity and duration.

The sleep terror is the most dramatic disorder of arousal (Fig. 3). It is frequently initiated by a loud, blood-curdling scream associated with extreme panic, followed by prominent

160

motor activity such as hitting the wall, run- ning around or out of the bedroom- sometimes resulting in bodily injury or property damage. A universal feature is inconsolability. Complete amnesia for the activity is typical, but may be in~omplete.4~. 48, 79 Although usually benign, the behaviors may be violent, resulting in considerable injury to the victim or others or damage to the environment, occasionally with forensic implications."*

Disorders of arousal may be triggered by febrile illness, alcohol, prior sleep deprivation, and emotional stress.142, 205 Medication- induced cases have been reported with sedatives or hypnotics, neuroleptics, minor tranquilizers, stimulants, and antihistamines, often taken in combination?*, lZ5, 14*, 220 Disor- ders of arousal may be exacerbated by pregnancy or menstruation, suggesting hormonal

It is important to remember that other, underlying sleep disorders that result in frequent arousals such as obstructive sleep apnea (OSA),S* nocturnal seizures, or periodic limb movement disorder may serve to trigger disorders of arousal. Although the observed clinical phenomenon may be sleepwalking or sleep terrors, therefore, the true underlying sleep disorder may be very different. It is a common clinical experience to see an improvement in disorders of arousal following effective treatment of OSA. Conversely, effective treatment of OSA with nasal continuous positive airway pressure (CPAP) may result in disorders of arousal, presumably associated with deep NREM sleep rebound.45, 127

It is commonly believed that persistence of such behaviors beyond childhood or their development in adulthood is an indication of significant psych~pathology.~~~ I9O Numerous studiess9* Io6, 130, 174 have dispelled that myth, indicating that significant psychopathology is usually not present in adults with disorders of arousal.

Isolated, often bizarre, sleep-related events may be experienced by perfectly normal people, and most do not warrant further extensive or expensive evaluation. The initial approach to the complaint of unusual sleep- related behavior is to determine whether further evaluation is necessary. The patient should be queried regarding the exact nature of the events. Because many episodes may be associated with partial or complete amnesia, additional descriptive information from a bed partner or other observer may prove invalu-

factors.l*,169.189


W I . I - 1 *la

Figure 3. Polysomnogram (PSG) correlate of sleepwalking. For the initial half of the tracing, there is well-established slow-wave (stages 3/4 NREM) sleep; then, a precipitous arousal occurs, characterized by agitated behavior and striking tachycardia (channel 18). L = left; R = right; Ext. Dig. = extensor digitorum; Ant. Tib. = anterior tibialis. (From Schenck CH, Mahowald MW: Cleve Clin J Med 57(suppl):S9-S23, 1990; with permission.)

able. Guidelines for the need for further evaluation have been developed and include behaviors that:

are potentially violent or injurious are extremely disruptive to other house- hold members result in the complaint of excessive daytime sleepiness are associated with medical, psychiatric, or neurologic symptoms or findings

Serious attention should be paid to parasomnia complaints under these circum- stances. Formal PSG studies, appropriately performed, provide direct or indirect diagnostic information in the majority of cases!, *l, 174

That is of more than academic interest because most of the conditions are readily treat-

able. Care must be taken to obtain the re- quired studies; routine PSGs performed for conventional sleep disorders are inadequate. In addition to the physiologic parameters monitored in the standard PSG, an expanded EEG montage must be obtained; the paper speed must be at least 15 mm/second, and continuous audiovisual monitoring must be used. Experienced technologist observation is invaluable. Multiple night studies may be re- quired to capture an event. Unattended studies have no role in the evaluation of parasomnias."'

Treatment often is not necessary. Reassur- ance of the events' generally benign nature, lack of psychological significance, and their usual tendency to diminish over time, often is sufficient. Benzodiazepines (clonazepam) or


tricyclic antidepressants (imipramine) may be effective, and should be administered if the behaviors are dangerous to person or property or extremely disruptive to family mem- b e r ~ . ~ ~ ~ Paroxetine and trazodone have been reported effective in single cases of disorders of arousal.’*, Io5 Nonpharmacologic treatment such as psychotherapy,sz progressive relax- ati0n,8~ 71, 157 or anticipatory awak- eningzol is recommended for long-term management. Avoidance of potential triggering factors such as drugs, alcohol, and sleep deprivation also is important.

The sleep-related eating disorder is a condition characterized by frequent episodes of nocturnal eating, generally without full conscious awareness, and usually not associated with waking eating disorders. The most common cause appears to be a ”specialized” form of disorder of arousal. The condition often responds to treatment with a combination of dopaminergic and opiate agents. Formal sleep studies are indicated because it may be the manifestation of other sleep disorders such as sleepwalking, restless legs syndrome, periodic limb movement disorder, or OSA.168, 175, 177

Miscellaneous Primary Sleep Parasomnias

A number of primary sleep phenomena re- main poorly understood. They appear not to respect sleep stages.

Bruxism (teeth grinding), intermittent grinding, or clenching of the teeth during sleep may occur during any stage of sleep.53, 164 Recent studies indicate that bruxism may actually represent a symptom of a number of different disorders, including simple bruxism, oro- facial dyskinesia, mandibular dystonia, and tremor.30, Io1 There is little support for previously proposed causes that are local (malocclusion), systemic, psychological, occu- pational, and developmental. Proposed treatments are legion and unvalidated. Formal sleep studies to rule out nocturnal seizures are indicated in individuals who experience significant oral damage.

Enuresis is no longer considered a parasomnia.Ios It may be the sole manifestation of nocturnal seizures.6, 44, 58 Formal PSG study with a full seizure montage and enuresis de- tector is indicated in cases with atypical his- tories or failure to respond to conventional

therapy. It should be remembered that enuresis may be a manifestation of OSA.z31

Rhythmic movement disorder (Rh4D) refers to a group of behaviors characterized by stereotyped movements (rhythmic oscillation of the head or limbs, head banging, or body rocking during sleep) seen most frequently in childhood and, rarely, in adults. It has been seen to arise from all stages of and may occur in the transition from wake to sleep. The cause is unknown, and no predictably effective pharmacologic or behavioral treatment has been reported. Benzodiazepines and tricyclic antidepressants may be tried.199 Rarely, RMD may be the sole manifestation of a seizure.58

The terms restless legs syndrome (RLS) and the periodic limb movement disorder (PLMD) are often confused and, erroneously, used inter- changeably. RLS is a clinical symptom that often results in severe insomnia, whereas PLMD is a PSGfinding that may or may not have clinical significance.10z* lZ6 The reason for the confusion is the fact that the majority of patients with RLS (80%) have the PSG finding of PLMD; however, the converse is not true.132

RLS is a poorly understood, occasionally incapacitating, disorder characterized primarily by a vague and difficult-to-describe unpleasant sensation involving the lower extremities. The discomfort appears primarily during periods of inactivity, particularly during the transition from wake to sleep. Patients often have difficulty in describing the unpleasant sensations; they rarely use conventional terms of discomfort such as “numb- ness, tingling, or pain,” but rather bizarre terms such as “pulling, searing, drawing, crawling, or boring,” suggesting that the sensations are unlike any experienced by unaf- fected people. The distressing sensations are typically relieved only by movement or stim- ulation of the legs. Many different techniques have been found by patients-walking about, stomping the feet; rubbing, squeezing, or stroking the legs; taking hot showers or baths; or applying ointment, hot packs, or wraps to the legs. Although the maneuvers are effective while they are being performed, the discomfort usually returns as soon as the individual becomes inactive or returns to bed. The symptoms rarely also involve the trunk or upper extremities, but usually to a lesser degree than the legs. Infrequently, the symptoms may be confined to the knees or thighs.91 Those more severely affected may find it extremely difficult to sit for prolonged periods


of time such as during long car trips or plane rides.187, 204, 212, 215 The motor restlessness often appears to follow a circadian

RLS is very common, affecting 5% to 10% of the general population. It may begin in childhood, but tends to be more prevalent with increasing age. It affects men and women. Its association with menstruation, pregnancy, and menopause may explain the possible female predominance. In retrospect, the symptoms of many patients suffering from RLS began in early to mid-childhood, and there is growing evidence that RLS may masquerade as "attention deficit disorder with hyperactivity" and "growing pains" in

The majority of cases are idiopathic or familial. A positive family history may be obtained in up to 50% of cases. Hormonal in- fluences are suggested by the history of exacerbation during menstruation, pregnancy, or menopause. Up to 27% of pregnant women may experience RLS. Although RLS has been associated with a wide variety of other medical and neurologic conditions such as iron- deficiency anemia and various peripheral neuropathies, such cases appear to be rare. RLS affects 20% to 40% of patients with chronic renal failure on dialysis, and may be extraordinarily bothersome in such cases (Fig. 4).I'j5 The RLS symptoms disappear following successful renal transplantation. Extensive and expensive medical and neurologic evalu- ations are not warranted unless there are historical or physical examination suggestions of other medical disorders. Environmental factors such as caffeine, fatigue, or stress may worsen the symptoms. Although once believed to be psychiatric in nature, there is no evidence whatsoever that RLS is related to any psychological or psychiatric problems. Recent elegant functional neuroimaging studies have identified thalamic, red nucleus, and brainstem involvement in the generation of periodic limb movements in patients with RLS.25

There is growing evidence that RLS may be seen following neurologic insults such as Lyme-disease myelitis,66 post-polio syn- dr0me,2~ lumbosacral radic~lopathy,'~~, 214 spinal cord pathology (syringomyelia, radiation- induced myelopathy),226 foramen magnum meningi~rna,'~~ and peripheral n e u r ~ p a t h y . ~ ~ ~

PLMD was formerly known as periodic movement of sleep or nocturnal myoclonus. PLMD is characterized by periodic (every 2 0 4 0 seconds) movements of the legs during

children.150,151,216

sleep, usually most prominent during the lighter stages of NREM sleep.153 The movements may be associated with arousals that often are too brief to be perceived by the individual. It should be emphasized that the arousals are often associated with the extrem- ity movements but are not necessarily caused by the movements.131 If the frequent arousals result in interruption of sleep, they may result in excessive daytime sleepiness.

Almost all people with RLS have PLMD (SOY0), but the converse is not true. RLS is an unpleasant sensation perceived by the individual during wakefulness, whereas, in PLMD, the movements occur during sleep and most often are not appreciated by the person-only the daytime consequence is felt.

The entire issue of what constitutes an arousal has become more complicated with the suggestion that arousals manifest by autonomic changes without EEG evidence of arousal may be of clinical relevance.12o, lz4

There is evidence that the periodic limb movements may be generated by motor pattern generators in the spinal cord because the movements may persist following complete spinal cord transection or spinal cord lesion~.~*, lgo, 228, 229 Brainstem mechanisms have also been implicated in animal experi- m e n t ~ . ~ ~ , 97

RLS can usually be diagnosed by the history alone; formal sleep studies are not indicated in most cases. In the absence of RLS, PLMD is best diagnosed by formal sleep studies.

RLS is one of the most important causes of insomnia, both because of its prevalence and because of its response to treatment. Most cases of RLS respond gratifyingly to medical treatment. Three main classes of medications are effective:

1. Anti-Parkinson medication such as L- dopa/carbidopa, bromocriptine, pergolide, or selegiline (Patients should be in- formed that the response to such agents does not imply any relationship between RLS and Parkinson disease)41,

2. Benzodiazepines such as diazepam, clonazepam, temazepam, or triaz01am'~~

3. Opiates such as codeine, oxycodone, methadone, tramadol, or propoxy- phene217

Many patients respond to one, but not another agent, even within the same class of medications. Combinations of drugs may be effective and often are necessary. Other agents are available for unusually difficult cases, in-


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Figure 4. Severe sleep fragmentation due to total body periodic movements in a patient with chronic end-stage renal disease. The symptoms of the restless-legs syndrome and the sleep fragmentation, induced by periodic body movements, contribute to the misery of many patients undergoing chronic dialysis. These symptoms generally respond well to medical management (see text).

cluding baclofen, carbamazepine, clonidine, gabapentin, and phenoxybenzamine.2ns Be- cause of the nature of some of the aforemen- tioned medications (especially the benzodiazepines and opiates), some physicians are hesitant to prescribe them on a long-term ba- sis. In fact, the incidence of abuse, tolerance, or addiction to opiates or benzodiazepines in this patient population appears to be insig- nificant, and such concerns should not pre- vent aggressive treatment of this disabling condition.

Occasionally, carbidopa/L-dopa is very effective in the evening, but results in the reap- pearance of symptoms the following day. In those cases, the controlled release form of carbidopa/L-dopa may be given in the evening and again in the Some commonly prescribed medications such as the tri-

cyclic antidepressants, fluoxetine or lithium, may actually worsen the Cer- tainly, specific treatment for iron-deficiency anemia is indicated if that condition is found. The treatment for uremia/dialysis-related RLS is the same as for idiopathic RLS.165,203,2w Adjunctive behavioral treatments such as relaxation therapy, biofeedback, and stress re- duction also may be of value.93

The "painful legs and moving toes" syndrome, which may follow spinal cord or cauda equina injury, may be confused with

Propriospinal myoclonus is a spinal cord-mediated movement disorder that is in the differential diagnosis of RLS, and that may shed light on the pathophysiology of RLS and

Posttraumatic stress disorder (PTSD) is often

RLS.40, 138, 179, 180, 191,213

PLMD.23, 24, 28,49, 77, 85, 143, 152, 202. 228


associated with subjective sleep complaints including "nightmares" and sleep terror-like experiences.I2 Despite prominent subjective sleep complaints, no significant objective sleep abnormalities have been identified in PTSD."

Somniloquy (sleep talking) is very common in the general population, may have a genetic component,' and is of no apparent clinical or psychological significance. It occurs in both REM and NREM sleep.7,

SECONDARY SLEEP PHENOMENA

The secondary phenomena are parasomnias representing either abnormal or excessive autonomic or physiologic events arising from specific organ systems, and occurring preferentially during sleep. They can be ap- proached by organ system.

Central Nervous System Parasomnias

Sleep-Related Seizures

Sleep and epilepsy are common bedfellows. In some individuals, sleep or sleep deprivation potentiates seizures.39, 156, 198 Conversely, seizure disorders can affect the wake/sleep

In most cases, epilepsy is highly state- dependent-NREM sleep promotes seizures, whereas REM sleep is a relatively anti-epileptic state.'%, That state-dependent vulnera- bility to seizures reflects the dramatic reorganization of the entire CNS as it moves across the three states of being-W, NREM sleep, and REM sleep.

Virtually all sleep disorders may be coun- terfeited by seizures, and vice versa. Hyper- somnia, insomnia, and parasomnias all may be the result of seizures. The behaviors associated with nocturnal seizures are often very bizarre, and masquerade as primary sleep parasomnias, secondary sleep parasomnias, or psychiatric condition^.'^^ Furthermore, sleep disorders may worsen a coexisting seizure disorder. OSA, for example, may make seizures more difficult to control because of the apnea-related sleep fragmentation and sleep deprivation. The overlapping nature of seizures and sleep disorders has been reviewed extensively e1~ewhere.l'~

Clinical differentiation between sleep and epileptic phenomena may be difficult, and

misdiagnosis in both directions is common. The diagnosis of nocturnal seizures may be enigmatic, particularly if there is no history of diurnal spells. Both waking and sleep-deprived EEGs may fail to reveal the diagnosi~,'~, 148 necessitating all-night PSG study using a full seizure montage, appro- priate paper speed, and continuous video recording. Reasons for misdiagnosis include: (1) obscuration of the scalp EEG by movement artifact, (2) absence of scalp EEG manifestations of seizure activity, (3) EEG seizure manifestation appearing to be an "arousal" pattern, and (4) absence of EEG or clinical post-ictal period.'14 "Ambulatory" EEG monitoring has led to the misdiagnosis of functional psychiatric disease in a number of our patients subsequently demonstrated to have bona fide nocturnal seizures.

The difficulties in evaluating unusual sleep- related events emphasize the necessity of extensive, in-person laboratory monitoring with interpretation of all data (clinical, EEG, sleep, video, and technologist-provided information) by personnel experienced in both sleep medicine and epileptology. Although exclusively nocturnal seizures may be uncommon, they are routinely misdiagnosed, and should never be overlooked as possible causes in any sleep-related behavior that is recurrent, stereotyped, or inappropriate, regardless of the specific nature of the behavior.

Effective treatment is available for most sleep disorders and for seizures, and is predi- cated on an accurate diagnosis. If seizures are responsible for the sleep /wake complaint, treatment is similar to that for other seizure disorders.

The headache symptoms of cluster headache, chronic paroxysmal hemicrania, and, possi- bly, migraines, in some cases, are REM sleep- related, explaining the common report of sleep-related headaches in those condition^.^^, 37, 86, Sleep-related headaches are greatly overrated as a marker for OSA.3

Cardiopulmonary Parasomnias

Cardiac arrhythmias during sleep have been studied extensively. Any relationship between sleep in general, and sleep stage spe- cifically, to arrhythmias is variable and unpre- d i~ tab1e . l~~ Dramatic anecdotal exceptions include REM sleep-related asystole61 and sound-induced ventricular fibrillationzz4 in young, otherwise healthy individuals.


Nocturnal angina pectoris, as with sleep- related arrhythmias, may have a correlation with sleep and sleep stage in certain individuals, but no generalizations are 109,

associated with obstructive sleep a ~ n e a . ~ ~ Sleep-related exacerbation of nocturnal

asthma is a common complaint in asthmatic patients. No predictable sleep stage relationship has been identifiedz6, 74, 133, and many factors likely are operant, including circadian endocrine and body temperature changes.16

Numerous respiratory dyskinesias may occur or persist during the sleep period. They include (1) segmental myoclonus such as palatal myocl~nus~~, loo or diaphragmatic 73, 149 and (2) paroxysmal dystonia.lsl Respira- tory dyskinesias may also be the manifestation of neuroleptic-induced dyskinesias, and may or may not persist during ~leep.9~1 158,

223, 225 Respiratory dyskinesias should be dif- ferentiated from unusual nocturnal seizures that present with primarily or exclusively respiratory symptoms.197, 211, 218

Persistent hiccup may continue during all stages of sleep, but its persistence during sleep in individuals with chronic hiccup is variable.% The frequency diminishes during sleep, more so in REM than NREM periods. Interestingly, sleep hiccups are rarely associated with arousals.9, 11

Miscellaneous isolated cases of sleep-related dyspnea, choking, and expiratory groaning have been reported. The causes and treatment are ~nclear.3~ The sole manifestation of nocturnal seizures may be paroxysmal chokingz2

135. 136, 144. 155, 183. 196, 221 Nocturnal angina may be

Gastrointestinal Parasomnias

Numerous gastrointestinal disorders such as gastroesophageal reflux and diffuse esophageal spasm may result in paroxysmal arousals during sleep, often mimicking disorders of other organ systems.l16

Miscellaneous Secondary Parasomnias

Sleep-related panic attacks may occur in patients with diurnal panic, or, rarely, may pre- cede the appearance of diurnal panic, or may be exclusively nocturnal in nature.l’, The striking similarity among the symptoms of dream anxiety attack, sleep terror, nocturnal seizures, and nighttime panic urges caution

in diagnosis.56. 65, 103. 121, 122. 210 OSA can also cause symptoms that mimic nocturnal panic attacks.42

Psychogenic dissociative states are characterized by complex, potentially injurious behavior, occasionally confined to the sleep period. A history of childhood physical or sexual abuse is virtually always present, but may be difficult to elicit. In this condition, unlike other parasomnias, the complex behavior is seen during EEG monitoring to arise from clear EEG-determined wakef~lness.’~~ The potential for confusion of psychogenic dissociative spells with nocturnal seizures or disorders of arousal is great.

Malingering, either personal or as “Mun- chausen by proxy” involving children, may present as violent sleep-related behav-

The compIaint of nocturnal muscle cramping ( N M C ) , frequently nocturnal, is extremely common, but poorly understood. NMC can be familial.” The true incidence and cause are unknown and there has been no systematic study of NMC. A subjective response to quinine sulfate or verapamil has been reported, as has an isolated case responding to transcutaneous nerve ~timulation.’~, 31, 128* 222

iors.55,104,119

MOTOR PARASOMNIAS OF PARTICULAR INTEREST TO PULMONOLOGISTS

To date, nine types of associations between OSA (and its treatment with nasal CPAP) and motor parasomnias have been identified:

1. OSA-induced arousals from REM sleep with dream-related complex or violent behaviors that resemble RBD. In one abstract,’37 five cases were presented: A 68-year-old man with a history of loud snoring and excessive daytime sleepiness (EDS) had several episodes of hitting his wife in bed during attempted dream enactment while dreaming that he was fight- ing. A 67-year-old man had a history of EDS and abnormal nocturnal behaviors in which he would shout and grab and injure his wife while dreaming of prior military experiences and of sporting events. A 69-year-old man presented with a history of EDS and dream- related behaviors, such as turning the pages of a newspaper or screwing in a light bulb. A 52-year-old man suffered from carbon mon- oxide poisoning 1 year previously, which triggered the onset of a progressive disorder of EDS and nocturnal dream enactment, as ob-


served by his wife: He would throw punches as if in a fight; he would kick repeatedly while dreaming that dogs were biting his leg. A 51-year-old man, with OSA and intolerance to nasal CPAP treatment, reported episodes of falling out of bed and of nocturnal wandering, including walking to the refrigerator and putting his fist through a window. He had sustained multiple ecchymoses and lacera- tions during the episodes.

Overnight PSG studies were diagnostic for severe OSA in each of the five patients, but were not diagnostic for RBD or subclinical RBD in any patient. The apnea-hypopnea index ranged from 51 to 196/hour, oxygen saturation nadirs ranged from 68% to 82%, and sleep efficiency ranged from 30% to 79%. REM sleep always demonstrated intact muscle atonia, and no behaviors emerged during that sleep stage.

Three patients had PSG studies during nasal CPAP treatment trials, which revealed normalization of respiratory parameters and (once again) absence of any feature of RBD. Those three patients reported cessation of parasomnia behaviors coincident with initia- tion of nasal CPAP treatment of OSA. One patient was intolerant of nasal CPAP treatment, and reported the ongoing recurrence of parasomnia episodes.

The conclusion of this report was that severe OSA may be associated with behaviors that simulate RBD. That serves as a compelling example of the need to perform PSG studies in the evaluation of the complaint of dream enacting nocturnal behaviors. Treat- ment of presumed RBD with clonazepam (the established treatment of documented RBD) in a case of OSA ”pseudo RBD could result in a worsening of the OSA, which, in turn, could result in a worsening of the “pseudo RBD” that may lead to an increase of the dose of clonazepam, with possible worsening of the OSA, and a vicious cycle could be perpetu- ated.

2. RBD may protect against OSA. There is clinical and experimental evidence suggesting that RBD may protect against OSA. Our center has reported on a series of 96 elderly RBD patients, of whom 84 were men.166 Fourteen (1%’0) had OSA, with mean OSA index of 31/ hour (range, 5-95), mean oxygen saturation of 91% (range, 85”/0-96%), mean oxygen saturation nadir of 84% (range, 72%-92%), and mean apnea duration of 24 k 11 seconds. We concluded that OSA, when present in RBD, is usually mild, and that finding was consistent

with data from an experimental animal model of RBD, in which cats receiving dorsolateral pontine lesions (thus eliminating the custom- ary atonia of REM sleep) exhibited enhanced diaphragmatic ventilation during REM sleep.67 The increased motor drive seen during REM sleep in RBD therefore may also manifest as increased diaphragmatic ventilation during REM sleep, with lessening of any risk for OSA (or lessening of the severity of any pre-existing OSA).

3. OSA-induced confusional arousals from non- REM sleep with complex or violent behaviors that resemble sleepwalking (SW) or sleep terrors (ST). With regard to OSA-induced confusional arousals from non-REM sleep resembling SW/ST, Guilleminault and S i l ~ e s t r i ~ ~ have the following observations: “It is well known that adult patients with OSA syndrome present nocturnal wandering during sleep. These patients frequently demonstrate yelling and screaming during sleep, as well as confusion, disorientation, and sleepwalking. . . . The nocturnal hypoxia and the repetitive sleep dis- ruptions secondary to the OSA syndrome readily explain these symptoms.” This is another example of why overnight PSG studies with extensive physiologic monitoring are mandatory in the evaluation of problematic motor parasomnias.

4. Nasal CPAP treatment of OSA may result in slow-wave sleep rebound and emergent SW (non-XEM sleep parasomnia). In one report,lZ7 a 33-year-old man without prior history of parasomnia was evaluated on account of a 3-year history of EDS and observed apneas during sleep. During a PSG study, his apnea index during the first 2.5 hours of the study was 106/hour, and he was apneic 57% of the time, with an oxygen saturation nadir of 61%. Nasal CPAP treatment was initiated during the second half of the PSG study, which triggered the emergence of slow-wave sleep rebound with two episodes of frank SW. Ongo- ing nasal CPAP treatment as an outpatient resulted in resolution of EDS and observed apneas. No recurrence of SW was reported.

In a similar case,154 a sleep terror was triggered by residual obstructive apneic episodes that occurred during slow-wave sleep rebound during CPAP administration. Slow- wave sleep rebound alone (without a prior parasomnia history), therefore, in the context of nasal CPAP treatment of OSA, can trigger the emergence of SW.

5. Nasal CPAP treatment of OSA may be compromised by (undiagnosed and untreated) ST


(non-REM sleep parasomnia). Nasal CPAP treatment of documented OSA syndrome in a 58- year-old man was compromised by parasomnia episodes observed by his wife, in which the CPAP mask would be dislodged by short attacks characterized by his sitting up in bed while ~rying.4~ Repeat PSG monitoring documented that nasal CPAP treatment was effective in controlling the OSA while the mask was properly in place; however, the patient had 17 episodes of abrupt arousals from slow- wave (stages 3 and 4) sleep with behaviors consistent with a diagnosis of ST (pavor nocturnus). Treatment of the ST with imipramine was initiated. The authors concluded that "other sleep disorders may be masked by untreated OSAS and. . .only a PSG may be helpful in the differential diagnosis of a poor compliance to CPAP."

6. OSA-induced arousals from non-REM or REM sleep can be associated with involuntary eating (nocturnal sleep-related eating disorder). There can be eventual weight gain that may then aggravate the OSA, causing a vicious cycle. OSA- induced arousals can be associated with involuntary nocturnal eating, which comprises one of the subcategories of nocturnal sleep- related eating di~0rders. l~~ We have reported two cases in which nasal CPAP treatment controlled both the OSA and the nocturnal eating.In The first case involved a 39-year-old woman whose PSG study revealed an apnea index of 72/hour, a total respiratory disturbance index of 145/hour, average oxygen saturation of 76%, and oxygen desaturation nadir of 70%. Treatment with nasal CPAP at 12.0 cm water pressure, with 28% supplemental oxygen, controlled the various signs and symptoms of OSA and also immediately controlled the nocturnal eating disorder, with benefit maintained at 5-month follow-up. The second case involved a 33-year-old man with nightly sleep-related eating and with a history of OSA that was confirmed by PSG study, which documented an apnea index of 65/hour and oxygen desaturation nadir of 83%. Nasal CPAP treatment at 6.0 cm water pressure fully controlled both the OSA and the nocturnal eating disorder.

7. Nocturnal sleep-related eating disorder associated with weight gain that may eventually result in clinical OSA. In a case of "sleep-related eating disorder as a cause of obstructive sleep a ~ n e a , " ~ ~ a 34-year-old man was reported with obesity resulting from nocturnal sleep- related eating disorder and a history of OSA. Incarceration for 1.5 years restricted his access

to food at night, leading to 36-kg weight loss and clinical improvement of the symptoms of OSA. Release from prison allowed the recurrence of unrestricted nocturnal eating, obesity, and OSA symptoms. OSA was documented by PSG study, with an apnea-hypopnea index of 25/hour and oxygen saturation nadir of 81%. The patient refused nasal CPAP treatment and any follow-up. Successful control of nocturnal sleep-related eating disorder with weight loss (e.g., by incarceration!) can result in improvement of coexisting OSA.

8. OSA may induce epileptic seizures with complex or violent behaviors. OSA-induced epileptic seizures have been described in three re- p o r t ~ . ~ ~ , 697 94 Although repeated oxygen desaturations during sleep may have been the immediate trigger for the seizures, chronic sleep deprivation associated with OSA may have also lowered the seizure threshold (in addition to any other factor[s]).

9. OSA has been reported to induce cerebral anoxic attacks. In a case a 52-year-old man was documented to have OSA syndrome. PSG study also revealed cerebral anoxic behavioral attacks during REM sleep. The attacks were caused by severe hypoxia provoked by apneas lasting up to 220 seconds. At the onset of each REM sleep period, the apneas immediately became more prolonged, with a mean duration of 166 seconds. Seven of the 10 apneas in REM sleep led to an attack, with violent leg and arm spasms that lasted 5 to 10 seconds. The EEG during the cerebral anoxic attacks revealed slowing of the frequency and flattening of the ampli- tude; however, no epileptiform activity was recorded before, during, or after the attacks. After the attacks, the patient did not wake up. EEG showed generalized theta activity for 1 to 2 minutes, then stage 2 non-REM sleep or REM sleep reappeared. The patient was amnestic for the attacks on terminal awakening in the morning.

SUMMARY

The three states of mammalian being, W, REM sleep, and NREM sleep, are not mutually exclusive, and may occur simultaneously, oscillate rapidly, or appear in dissociated or incomplete form to produce primary sleep parasomnias. In addition, dysfunctions of a wide variety of organ systems may take ad- vantage of the sleeping state to declare themselves, resulting in secondary sleep parasom-


nias. Contrary to popular opinion, the majority of the often bizarre and frightening experiences are not the manifestation of underlying psychological or psychiatric conditions. There is an interesting interaction between sleep-disordered breathing and parasomnias. Formal study in an experienced sleep disorders center will usually reveal a diagnosable and treatable condition that ex- plains the spells. Continued study of unusual sleep-related events undoubtedly will reveal more fascinating conditions, expanding our knowledge of sleep physiology, and strength- ening the bonds between clinicians and basic- science sleep researchers.

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PARASOMNIAS INCLUDING THE RESTLESS LEGS SYNDROME