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BRAIN RESEARCH REVIEWS XX (2007) XXX– XXX

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Review ☆ Sexsomnia: Abnormal sexual behavior during

Monica L. Andersena,⁎, Dalva Poyaresa, Rosana S.C. Alvesb, Robert Skomroc, Sergio Tufika aDepartment of Psychobiology - Universidade Federal de São Paulo, Escola Paulista de Medicina (UNIFESP/EPM), São Paulo, SP, Brazil bDepartment of Neurology - University of São Paulo (USP), São Paulo, SP, Brazil cUniversity of Saskatchewan, Saskatoon, Saskatchewan, Canada

ARTICLE INFO ABSTRACT

Article history: This review attempts to assemble the characteristics of a distinct variant of Accepted 26 June 2007 called sexsomnia/sleepsex from the seemingly scarce literature into a coherent theoretical framework. Common features of sexsomnia include sexual with autonomic activation (e.g. nocturnal , , , Keywords: ). Somnambulistic sexual behavior and its clinical implications, the role of precipitating factors, diagnostic, treatment, and medico-legal issues are also reviewed. The characteristics of several individuals described in literature including their family/personal Sexsomnia history of parasomnia as well as the abnormal behaviors occurring during sleep are reported. Sleepsex © 2007 Elsevier B.V. All rights reserved. Atypical sexual behavior Stress

Contents

1. Introduction ...... 0 2. ...... 0 3. Sexsomnia: atypical sexual behavior during sleep...... 0 4. Background ...... 0 5. Physiological genital events during sleep ...... 0 6. Precipitants of parasomnic behavior ...... 0 6.1. Sleep deprivation...... 0 6.2. Sleep fragmentation ...... 0 6.3. Alcohol or consumption ...... 0 6.4. Stress ...... 0

☆ THEME: Neural Basis of Behavior: Biological rhythms and sleep/Brain Research Reviews. ⁎ Corresponding author: Department of Psychobiology - Universidade Federal de São Paulo, Rua Napoleão de Barros, 925, Vila Clementino - SP 04024- 002, São Paulo, Brazil. Fax: +55 11 5572 5092. E-mail address: [email protected] (M.L. Andersen).

0165-0173/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.brainresrev.2007.06.005

Please cite this article as: Andersen, M.L., et al., Sexsomnia: Abnormal sexual behavior during sleep, Brain Res. Rev. (2007), doi:10.1016/j.brainresrev.2007.06.005 ARTICLE IN PRESS

2 BRAIN RESEARCH REVIEWS XX (2007) XXX– XXX

7. Medico-legal issues ...... 0 8. Diagnostic aspects...... 0 9. Treatment ...... 0 10. Final considerations...... 0 Acknowledgments ...... 0 References ...... 0

1. Introduction sidered medical disorders because they may result in injuries, may induce or are induced by sleep disruption, and have The fact that sleep is promptly reversible is probably the most adverse health effects and psychosocial consequences. REM important characteristic which differentiates it from most sleep behavior disorder (RBD) may herald the onset of a neu- other states of altered . Electrophysiological rodegenerative disorder (Schenk and Mahowald, 1996; Boeve studies in the 1950s demonstrated that there were two main et al., 2001, 2003). RBD is a more recently described parasomnic states of sleep, non-rapid eye movement (NREM) and rapid eye disorder and is characterized by vigorous motor activity which movement (REM) sleep. The NREM sleep is recognized by low- occurs exclusively during REM sleep (Schenk et al., 1986); it frequency and high-amplitude waves, presence of sleep spin- consists of often injurious dream-enactment motor activity dles on an electroencephalogram (EEG) recording, and muscle associated with vivid dreaming. RBD is more frequent in older tone reduction. The electrophysiological features of REM sleep adults and in males, its actual prevalence in general popula- are a combination of desynchronized EEG, loss of electromyo- tion is unknown but is estimated as 0.5% (Ohayon et al., 1997). gram (EMG) activity, and the presence of rapid eye movements. A subgroup of RBD patients with NREM parasomnias (sleep- The EEG reflects the intense cortical activity that distinguishes walking and sleep terrors) have been reported to have the REM from NREM sleep, but its similarity to the EEG of wake- Parasomnia Overlap Syndrome (Schenck et al., 1997). Overall fulness also led it to be called “paradoxical” sleep. severe parasomnias are distressing and, in some cases, can be The homeostatic sleep drive appears to control NREM ra- hazardous to the sleeper and his/her partner. ther than REM sleep. Sleep is normally entered through NREM Motor parasomnias are complex motor behaviors occurring rather than REM sleep in adults with intensification of the during NREM sleep, REM sleep, or transitional states. They are – homeostatic drive increasing the duration and depth of NREM classified as either arousal disorders, sleep wake transition sleep at the expense of REM. NREM sleep provides time for disorders, parasomnias associated with REM sleep, or other restorative processes to take place within the central nervous parasomnias (ICSD, 2005). Sleepwalking is one of the most system (CNS) and other parts of the body. Overall, NREM sleep frequent parasomnias occurring during NREM sleep, with appears to be a state in which energy is conserved enabling variable degrees of complexity and duration. Benign forms of both the CNS and other systems to either recover from the NREM arousal parasomnias occur frequently in childhood and activity of the previous episode of wakefulness or to prepare attenuate in teen years; however, they can persist into or for the next episode. In this sense, NREM, REM sleep, and begin in adulthood (Szelenberger et al., 2005). Sleepwalking is wakefulness are not mutually exclusive states. The occur- the end result of an often complex set of predisposing, prim- rence of states of incomplete awakening from sleep may ge- ing, and precipitating factors (Pressman, 2007). nerate parasomnias (Wills and Garcia, 2002).

3. Sexsomnia: atypical sexual behavior during 2. Parasomnias sleep

Sleep is a vital behavior and occupies approximately one-third One of the most intriguing clinical entities of parasomnia is a of a person's lifetime. The incidence of both sleep fragmenting distinct variant of sleepwalking known as sexsomnia, som- disorders and chronic partial sleep deprivation is very high in nambulistic sexual behavior or “sleepsex” (Buchanan, 1991; our society (Bonnet and Arand, 2003), leading to a dramatic Fenwick, 1996; Shapiro et al., 1996, 2003). Recently, Schenck surge in the occurrence of sleep complaints and . et al. (2007) advocated the use of the terms pertaining to There are several types of sleep disorders, one of the most abnormal sleep and sex as sleep-related abnormal sexual be- fascinating of which is a category of parasomnias: well de- haviors, sexual behavior in sleep, among others. The authors scribed and common nocturnal phenomena defined as went on to formulate the first classification of sleep-related “events that occur intermittently or episodically during the disorders and abnormal sexual behaviors and experiences. night” (Driver and Shapiro, 1993). These undesirable physical The authors proposed this classification based upon the fol- or behavioral phenomena may occur in any phase of sleep. lowing rationale: (1) growing awareness that abnormal sexual Parasomnias are undesirable behavioral or experiential behaviors can emerge during sleep; (2) expanding set of sleep phenomena which occur during sleep, or during transition disorders known to be associated with abnormal sexual be- from sleep to wakefulness (Mahowald, 2000a,b). These events haviors, or misperception of sexual behaviors; (3) the cause of are manifestations of CNS activation transmitted into skeletal sleepsex can often be identified after clinical and polysomno- muscle and autonomic nervous system. Parasomnias are con- graphic (PSG) evaluations, and can be treated; (4) the forensic

Please cite this article as: Andersen, M.L., et al., Sexsomnia: Abnormal sexual behavior during sleep, Brain Res. Rev. (2007), doi:10.1016/j.brainresrev.2007.06.005 laect hsatcea:Adre,ML,e l,Sxona bomlsxa eairdrn le,BanRs e.(2007), Rev. Res. Brain sleep, during behavior sexual Abnormal Sexsomnia: al., et M.L., Andersen, as: doi: article this cite Please Table 1 – Case summaries for individuals with episodes of atypical sexual behavior during sleep 10.1016/j.brainresrev.2007.06.005 S Gender Age Family history Personal history Precipitating PSG Epworth Abnormal behavior Frequency Respiratory Medico- Refs of parasomnia of parasomnia factors during sleep events legal issues

D Man NA NA Sleepwalking NA No No NA NA Yes Motet, 1897(see (urination in public) Thoinot, 1911) Man 18 Sleepwalking No No Homosexual assault NA Langeluddeke (1955) SC Man 34 No Sleeptalking and Stress No No 2–3/week NA No Wong (1986) night terrors GS Man 35 Sleepwalking and Alcohol No No 2 NA Yes Hartman (1983) night terrors of his daughters H.M Man 27 No No Shift work Yes No¥ Sexual assault 2 OSA Yes Hurwitz et al. of a child (1989)

DA Man 35 Sleepwalking, Alcohol and drug No No Sexual assault 1 Yes XXX (2007) XX REVIEWS RESEARCH BRAIN RIL NPRESS IN ARTICLE enuresis and night of his daughter terror JW Man 27 Sleepwalking Sleepwalking Stress, alcohol and SD No No Indecent exposure 1 NA Yes Buchanan (1991) 1 Woman 26 Sleepwalking Sleepwalking Tiredness and alcohol No No Indecent exposure NA NA No Fenwick (1996) 2 Man 36 NA Sleepwalking Tiredness No No Indecent exposure NA NA No 3 Man y NA Sleepwalking Stress, tiredness, No No Sexual assault NA NA Yes alcohol and SD (?) GL Man y NA Sleepwalking Tiredness and alcohol No No Homosexual assault Some NA Yes occasions 5 Man y NA Sleepwalking Alcohol No No Sexual assault 1 NA Yes 6 Woman – NA Evidence of sleep Alcohol No No 1 NA Yes talking 7 Woman – NA NA Alcohol, tiredness. No No Sexual intercourse 1 NA Yes temazepam and SD – Man 43 No Sleepwalking and No No No and Very No Shapiro et al., sleepeating intercourse frequent 1996; Rosenfeld –

and Elhajjar, XXX 1998 Man 45 Frequent No No No Sexual assault 1 NA Yes sleepwalking of a teenager – Man 27 Brother: Violent nocturnal Alcohol Yes 4 Sexual intercourse 1x/month No No Alves et al. sleepwalking behaviors and (1999) sleepwalking JK# Man 27 Sleepwalking Sleepwalking and Alcohol and multiple Yes No Sexual assault Frequent Snoring Criminal Shapiro et al. sleep talking substance abuse (cunnilingus and and OSA charges had (2003) sexual intercourse) been laid CJ Man 39 NA Sleep talking Stress and SD Yes No Sexually touching 2/life Not Yes his daughter mentioned AF## Man 32 Yes Sleep talking Stress, alcohol Yes No Sexual assault 1 NA Yes and one episode and marijuana of a child of sleepwalking LD* Man 35 NA Sleepwalking Alcohol and multiple Yes No Sexual assault Not NA Yes

(continued on next page) 3 4 laect hsatcea:Adre,ML,e l,Sxona bomlsxa eairdrn le,BanRs e.(2007), Rev. Res. Brain sleep, during behavior sexual Abnormal Sexsomnia: al., et M.L., Andersen, as: doi: article this cite Please 10.1016/j.brainresrev.2007.06.005 RI EERHRVESX 20)XXX (2007) XX REVIEWS RESEARCH BRAIN RIL NPRESS IN ARTICLE

Table 1 (continued)

S Gender Age Family history Personal history Precipitating PSG Epworth Abnormal behavior Frequency Respiratory Medico- Refs of parasomnia of parasomnia factors during sleep events legal issues

and sleep talking substance abuse of a child mentioned and sexual intercourse with his wife DW Man 43 Yes Sleepwalking and Alcohol Yes No Sexual behavior Frequent NA No sleep talking JD Man 27 NA NA Alcohol Yes No Sexual intercourse Frequent NA No AK Woman 38 Yes Confusional awake Stress Yes NA Masturbation Frequent NA No JK Woman 40 Yes Apparently no No No NA Masturbation Frequent NA No TC** Man 28 Yes , Night No Yes 12 Sexual intercourse Frequent NA No –

terrors and XXX sleepwalking KB Man 37 NA Sleepwalking Stress and alcohol Yes NA Sexual behavior 1x/month Upper airways No resistance syndrome WW Man 16 NA Sleepwalking No NA NA Sexual assault 1NANo of his uncle 1 Woman 27 NA Sleep talking No No NA Moaning 3×/week NA No Guilleminault et al. (2002) 2 Woman 28 NA Sleep talking No No NA Moaning Not NA No mentioned 3 Woman 26 NA Sleep talking NA No NA Moaning and violent Not NA No masturbation mentioned 4 Man 31 NA Sleep talking NA No NA Moaning, violent Variable NA No masturbation and genital bruising 5 Man 23 NA NA NA No NA Sexual assault Not Snoring, No laect hsatcea:Adre,ML,e l,Sxona bomlsxa eairdrn le,BanRs e.(2007), Rev. Res. Brain sleep, during behavior sexual Abnormal Sexsomnia: al., et M.L., Andersen, as: doi: article this cite Please mentioned respiratory

10.1016/j.brainresrev.2007.06.005 pauses and 6 Man 38 NA NA SD No NA Sexual assault and 2x/month NA No intercourse 7 Man 27 NA NA NA No NA Sexual assault Variable NA No 8 Man 29 NA Excessive legs Former multiple No NA Sexual assault Not NA No movements during substance abuse mentioned 9 Woman 26 NA NA NA No NA Sexual assault Not NA No mentioned 10 Man 33 NA NA NA No NA Sexual assault and Not NA Yes intercourse mentioned 11 Man 18 NA Restless sleeper, SD No NA Sexual assault Not NA Yes mentioned RI EERHRVESX 20)XXX (2007) XX REVIEWS RESEARCH BRAIN , sleep PRESS IN ARTICLE talking, sleep terrors, enuresis and somnambulism JB Man 22 Strong family Sleepwalking Alcohol Yes 12 Anal, vaginal and 2 OSA Yes Ebrahim (2006) sleepwalking oral

S: subject; OSA: ; y: young; NA: not applicable; SD: sleep deprivation; PSG: . ¥Multiple Sleep Latency Testing revealed a mean sleep latency of 3.5 over four , three with REM. *Schizophrenic. **Patient reported some of the features of Klein–Levin syndrome (fluctuating appetite and and a history of heat stress requiring hospital admission). # (group of psychiatric syndromes primarily characterized by a deviant sexual fantasies, cravings, urges, and/or behaviors—Cannas et al., 2006). ##Posttraumatic stress disorder and major depression. – XXX 5 ARTICLE IN PRESS

6 BRAIN RESEARCH REVIEWS XX (2007) XXX– XXX aspects of abnormal sleep-related sexual behavior have com- genitals. When he emerged from his state of half stupor, he manded increasing attention, and finally, (5) new data on claimed to remember nothing of the events surrounding his periodic , e.g. Kleine–Levin syndrome, including arrest but was convicted to three months' imprisonment. The its range and frequency of abnormal sexual behaviors that case is interesting since it exposes the relationship between have recently been published. mental state, , and sexual offences in The etiology of this parasomnia is not yet elucidated and relation to sleep. most afflicted individuals do not seek therapeutic interven- tion, probably due to ignorance of the condition or embar- rassment. Atypical sexual behavior during sleep has rarely 5. Physiological genital events during sleep been documented; however, because of recent case reports within forensic contexts, more attention has been paid to the In 1944, Ohlmeyer and co-workers discovered the occurrence matter (Guilleminault et al., 2002). Although there has been of penile erection cycles during sleep in adult males. Such increased interest in all aspects of sleep-generating mechan- sleep-related (SRE) appeared at 85-min intervals and isms and male , comprehension of sleep had an average duration of 25 min (Ohlmeyer et al., 1944). As a disorders as they relate to sexual behavior is still unclear. result of this initial study, Oswald (1962) noted that erection In 2003, Shapiro and colleagues stated that sexsomnia accompanied some REM periods, but subsequent investiga- should be considered a distinct entity in the family of tions of Fisher et al. (1965) and Karacan et al. (1966) parasomnias, since its unique combination of particular demonstrated a strong temporal association between the activated systems in sleep, namely, specific motor, and occurrence of erection and REM. Erectile episodes were found autonomic activation supports this view. Nevertheless, it to dovetail with over 95% of REM periods while erection was may be quite challenging to distinguish between typical entirely absent during non-rapid eye movement (NREM) sleep, sleepwalking and sexsomnia. The uniqueness of the condition except immediately before and after REM periods (Fisher et al., is the involvement of a partner (usually more than a witness). 1965). Similarly, Karacan et al. (1966) reported that 80% of REM The typical behavior consists of complex autonomic func- periods displayed this phenomenon although, there were also tions, motor activities, and behavioral elements (Shapiro et al., occasional instances of erection during NREM sleep. While 2003). As pointed out by Ebrahim (2006), sexual behavior in men develop erection in REM sleep, women had vaginal sleep is considered a variant of sleepwalking disorder as the lubrication (Fenwick, 1996). overwhelming majority of people with this disorder have a Penile tumescence cycles in sleep occur in all normal previous and familiar history of sleepwalking. Of note, the healthy males from birth through adulthood and into old age repertoire of sexual behavior during sleep can vary from (Hursch et al., 1972; Karacan et al., 1972a,b; 1976) regardless of explicit vocalizations (with sexual content), violent mastur- the dream content (Hirshkowitz and Moore, 1996). For bation, and complex sexual activities including oral sex, and instance, by studying males from 3 to 79 years, Karacan and vaginal or anal intercourse. In some cases sexual behavior co-workers (1978) determined that there is a rapid decrease in during sleep is associated with injury to subject or his/her bed total sleeping time throughout the teen years with no partner, being considered a special form of violence. Guille- significant change from 20 to 50 years of age. Total REM minault et al. (2006) found that NREM sleepwalkers had an time decreases throughout the preteen and teen years and in increased incidence of harmful behavior compared to patients subsequent years remains stable at approximately 100 min with RBD. However, Mahowald and Schenck (1995) found that per night. Total penile tumescence time decreases from age aggressive behavior was commoner in patients with RBD. In 13 through age 79. Tumescence time during these years is 2002, Guilleminault et al., in their series of 12 cases docu- approximately 90 min per night, or 20% of total sleep time. mented with PSG, reported the following diagnosis associated The increase in total penile tumescence time during the with sexual behavior during sleep: NREM sleep somnambu- prepubertal and very early pubertal years is associated with lism, REM sleep behavior disorder, and frontal lobe seizures. an increase in NREM-related tumescence as REM decreases. As demonstrated in Table 1, previous history of sleepwalking In addition, there is a steady albeit slight decline in REM- is the leading feature in most cases. This review presents and related erection from age 20 to the 70s with an associated examines clinical case reports, court cases, and attempts to increase in NREM-related erection. In the 20- to 29-year-old assemble the characteristics of a distinct variant of sleepwalk- population, the average length of an SRE episode is 38 min, ing called sexsomnia from the seemingly scarce literature into whereas the average length of the SRE episode is 27 min in a coherent theoretical framework. the 61- to 67-year-old population. Not all SRE episodes are associated with full erection and, in fact, the incidence of partial erections increases during SRE with advancing age 4. Background (Kessler, 1988). More challenging to explain is erection during NREM sleep. Even though there is scant literature on this subject, there is at Somnambulistic episodes occur out of stages 3 and 4 of NREM least one early report of sexual behavior during sleepwalking. sleep, and the presence of an erection is not considered In the Annales d'Hygiene et de Médecine Légale in 1897, Motet exclusion criteria for sleepwalking (Shapiro et al., 2003). Most described a case of somnambulism and (see parasomnic behavior, with or without sexual content, does Thoinot, 1911). E.D. was arrested outside a public urinal on Rue not occur in slow wave sleep (SWS) but arises out of SWS, Saint-Célie, where he had remained for more than half an suggesting that the presence of erections implies sexual hour attempting to entice a policeman by exposing his intent. The interpretation of NREM sleep erections is unclear.

Please cite this article as: Andersen, M.L., et al., Sexsomnia: Abnormal sexual behavior during sleep, Brain Res. Rev. (2007), doi:10.1016/j.brainresrev.2007.06.005 ARTICLE IN PRESS

BRAIN RESEARCH REVIEWS XX (2007) XXX– XXX 7

Penile erections may also emerge during partial from abuse (4.3%). Moreover, sleep deprivation was another iden- NREM sleep as a manifestation of emerging wakefulness with tified risk factor. . However, it is unlikely that full wakefulness is established, since complete occurred in all reported 6.1. Sleep deprivation cases of sexsomnia (Schenck et al., 2007). Shapiro and co-workers (2003) made the observation that Sleep deprivation per se represents a common type of stress sexual behavior in sleep may arise from either a dreamlike that can lead to physiological consequences (Tufik et al., 1978; experience (NREM dreaming) or, perhaps, dreaming with Rechtschaffen et al., 1983; Andersen et al., 2004, 2005a,b; sexual content (a feature of REM sleep). They argue that this Andersen and Tufik, 2006). Chronic insomnia leads to persist- recall of dreamlike experience has been associated with NREM ing tiredness and due to lack of energy. Respiratory sleep parasomnias, and does not imply the occurrence of REM and other medical conditions may be exacerbated in sleep and parasomnia. There is evidence that the organization associ- may have potentially serious complications resulting in ated with sexual behavior during sleep (as in the cases of DW reduced life expectancy. and KB—Table 1) is different in sleep, but in some cases these Disturbances in the sleep–wake rhythm and/or sleep behaviors can constitute a replication of patterns seen during deprivation are increasingly frequent due to tribulations of wakefulness (e.g. LD). modern life in developed countries (Spiegel et al., 1999). For Nevertheless, according to these authors, sexsomnia and instance, constant exposure to artificial light and interactive sleepwalking present with distinct clinical features. The main activities, such as television or Internet, are combined with features of sexsomnia often include sexual arousal with social and economic pressures to shorten the time spent autonomic activation (e.g. nocturnal erection, vaginal lubri- asleep. Since sleep deprivation is reported to increase the cation, nocturnal emission, dream orgasms (“wet dreams”), frequency of complex behaviors in sleepwalkers (for review sweating, cardiorespiratory response). In particular, ejacula- see Pressman, 2007), it must be considered as potential tion has been reported in some cases (e.g. case 7—Guillemi- precipitating factor. naultetal.,2002). Sexsomnia without sexual arousal, Many subjects can become chronically sleep deprived as a however, was also reported as in the case of AF, and this result of their current life style (Miro et al., 2002; Leibowitz may hinder correct diagnosis (Shapiro et al., 2003). A case of et al., 2006). Of note is a common pattern of irregular sleep– GL, a young male army private with a long history of wake schedules, one that restricts sleep during a working sleepwalking illustrates this point. He was accused of a week, builds a sleep deficit which is then repaid by longer homosexual assault by caressing his colleague's genitals. At sleep at weekends resulting in high sleep efficiency, short martial court, it was stated that at no time during the alleged sleep latency, and an increased duration of stages 3 and 4 assault did the defendant have an erection, and the court NREM sleep. Waking later in the morning, however, causes a accepted that it was highly unlikely that a purposeful phase delay the subsequent day, which is often followed by an homosexual assault would take place without the defendant early wake-up time at the start of the working week. The being sexually aroused. The timing of the event, 1 h after duration of sleep is thereby considerably shortened and sleep going to sleep, was suggestive of an episode occurring in SWS, deprivation resumes (Shneerson, 2000). Despite the fact that and the absence of an erection was taken as supportive sleep deprivation has been cited as one of the major evidence (Fenwick, 1996). The court martial dismissed the precipitating factor triggering sleepwalking episodes, we case and the pilot returned to flying duties, as reported by found 5 cases occurring in male subjects and one woman Fenwick (1996). presenting with sleep deprivation prior to nocturnal abnormal These cases demonstrate that it is possible, in men, to sexual behavior (see Table 1). differentiate between a conscious sexual assault and a somnambulistic . Indeed, sexual assaults are 6.2. Sleep fragmentation likely to involve sexual arousal with an erection. Notwith- standing, if there is predominant behavior oriented towards Most sleep disorders, such as sleep apnea, periodic leg the genital areas, there is a greater likelihood for sexsomnia, movements (PLM), , , or insomnia as opposed to parasomnic activity that is only sporadically can lead to sleep fragmentation. Parasomnias are associated and incidentally oriented towards the genital areas. with high indices of sleep fragmentation such as microarou- sal, sleep stage shifts, and number of awakenings (Haba-Rubio et al., 2004). An abnormal deep sleep associated with a high 6. Precipitants of parasomnic behavior SWS fragmentation might be responsible for the occurrence of sleepwalking and sleep terrors (Espa et al., 2000). Different trigger factors can precipitate a sleep automatism NREM sleep parasomnia patients present with higher and should be identified when sexsomnia event occurs. The degree of sleep fragmentation particularly during SWS (Espa most common precipitants of a recurrence of parasomnic et al., 2000; Besset and Espa, 2001). However, few studies have behavior in adults are stress, sleep deprivation/fragmentation, addressed the issue of sleep fragmentation as a trigger of alcohol or drug consumption, excessive fatigue (tiredness), parasomnia attacks. Espa et al. (2002) reported that a great and physical overactivity in the evening. As pointed out by number of arousal reactions in parasomniacs are involved in Schenck and co-workers (2007) precipitating factors for sex- triggering the parasomnia episodes. The authors emphasized somnia included physical contact with another person in bed the need to rule out potential causes of sleep fragmentation, (64%), stress (52%), fatigue (41%), alcohol use (14.6%), and drug such as sleep-related breathing disorders in adults with

Please cite this article as: Andersen, M.L., et al., Sexsomnia: Abnormal sexual behavior during sleep, Brain Res. Rev. (2007), doi:10.1016/j.brainresrev.2007.06.005 ARTICLE IN PRESS

8 BRAIN RESEARCH REVIEWS XX (2007) XXX– XXX arousal-related parasomnia, and suggested the use of esoph- 6.4. Stress ageal pressure monitoring to better detect respiratory effort events. Similar findings were reported by Guilleminault et al. Stress seems to be an important trigger in some cases. Indeed, (2003) in a population of children with sleepwalking. They for one patient, fatigue and interpersonal tension appeared to reported a high frequency of sleep-related breathing disorder precede each somnambulistic episode. Stress should be among these children, and in their family members. In their carefully distinguished from psychological disorders, such as series treatment of sleep disordered breathing improved depression and . In 2003, Lecendreux et al. identified sleepwalking episodes. Another study showed that sleepwalk- stressful life events in 55.5% of their subject group that ers presented with a high Cyclic Alternating Pattern (CAP) rate preceded the occurrence of sleepwalking. As pointed out by suggesting sleep instability. The authors concluded that subtle Pressman (2007), the stressful life events included family sleep disorders associated with chronic sleepwalking consti- conflicts, work-related problems, and changes in sleep envi- tute the unstable NREM sleep background on which sleep- ronment. For instance, AF (32 years old) was referred to the walking events occur, and that this subtle sleep disorder sleep clinic after having been accused of sexually assaulting a should be systematically searched for and treated when young girl. His sleep history was significant for sleep talking sleepwalking is associated to abnormal CAP (Guilleminault and, one occasion, sleepwalking, in addition to a family et al., 2006). history of parasomnia. After a traumatic personal loss (AF had to identify his father's crushed body) and initiation of 6.3. Alcohol or drug consumption excessive use of alcohol, his behavior changed (Shapiro et al., 2003). Mr. F was acquitted on the charge of sexual assault. Drug ingestion, sometimes combined with alcohol, has been suggested as a precipitating factor for sexsomnia (Luchins et al., 1978; Huapaya, 1979; Nadel, 1981). For instance, among a 7. Medico-legal issues group of seven subjects with sexual behavior in sleep (Shapiro et al., 1996), five had alcohol and/or substance abuse as It is not unusual that after an all-night party single people common precipitants of their sexual parasomnias. The role of sleep over at a friend's house, but, it has now become socially alcohol alone has not been firmly established although it was acceptable, in some cultures, for men and women to sleep implicated in one third of cases of murder during sleep- together in the same room and even in the same bed, even if walking (Bonkalo, 1974) and it is known that at the time of high they have not known each other well (Fenwick, 1996). Thus, it alcohol blood levels (or alcohol intoxication), some sleep is not surprising that an increasing number of criminal cases confusional behavior on awakening might be expected are coming before the courts where the interaction of sexual (Ebrahim, 2006). behavior and sleep is reported to have led to an offence, In the JW case (Buchanan, 1991), further analyzed by usually rape of or with a child. In our Schenck and Mahowald (1998), the forensic psychiatrist review, sleepsex was far more injurious to the bed partner testifying for the prosecution claimed that the consumption than to the person affected with parasomnia, although ad- of alcohol reduced the defendant's sexual inhibitions and he verse psychosocial consequences were quite common in both then engaged in an “opportunistic offence” when a sexual patients and bed partners. Sequelae may also be accompanied object (inadvertently) presents itself to him. The judge by reactive emotional distancing that may lead to some concluded that: “Fleeting disturbances of consciousness marital estrangement with counseling sometimes which are external to the person's individual, emotional and being sought (Schenck et al., 2007). psychological make-up do not fall within the concept of a A crime committed during sleep is regarded in law as an disease of the mind. The evidence is that this episode was automatism, the accepted legal definition of which was given triggered by external causes”. by Viscount Kilmuir in the House of Lords appeal in the case of The “external causes” were alcohol, stress, and sleep Bratty vs. Attorney General of Northern Ireland (Bratty, 1961). deprivation. In fact, JW had engaged in at least two sleepwalking Viscount Kilmuir described an automatism as “the state of a episodes in the context of excessive alcohol consumption (one person who, though capable of action, is not conscious of what during the night before his wedding in which he urinated next to he is doing.…” In other words it means unconscious, his sister bed, and the night he was charged with child sexual involuntary action (see Buchanan, 1991). misconduct). Schenck and Mahowald (1998) argued that the In the analysis of JW case of sexual misconduct with a child court could have called more attention to the issue of excessive by Schenck and Mahowald (1998), the authors raised the issue alcohol consumption, since it played a central role in the of whether a sleepwalker with episodes provoked by alcohol sequence of events that resulted in criminal misconduct, and excess should be held legally responsible for his behavior since it should have played a more relevant role in determining during alcohol-provoked sleepwalking events. whether the defendant's sleepwalking posed a “continuing A different category of sleep-related offences are alleged danger”. Recommendation for clinical consultation either in or sexual assaults in which the assailant is awake and regard to possible alcohol abuse or to his childhood-onset the victim is asleep (cases 6 and 7—Fenwick, 1996, as depicted history of sleepwalking should have been provided (Fenwick, in Table 1). A conviction of rape will be likely if the defendant 1996). Furthermore, it is advisable that adults or teenagers with admits that the victim was unquestionably asleep and did not NREM sleep parasomnias be informed of the risks of co-sleeping, wake up during intercourse (alcohol consumption or use of including with minors, especially after drinking alcohol or after drugs should also be considered). If the intercourse took place sleep deprivation (Schenck et al., 2007). in stages 3 or 4 of NREM sleep then there is a possibility that

Please cite this article as: Andersen, M.L., et al., Sexsomnia: Abnormal sexual behavior during sleep, Brain Res. Rev. (2007), doi:10.1016/j.brainresrev.2007.06.005 ARTICLE IN PRESS

BRAIN RESEARCH REVIEWS XX (2007) XXX– XXX 9 the victim may not arouse. A more complex condition exists out presence of: epileptic disorder; sleep-disordered breathing, when the defendant claims that the victim was not asleep and narcolepsy, PLM; REM behavior disorder; or NREM sleep the victim had indicated consent or consent was implied (e.g. parasomnia. In fact, as reported by a recent review and other the victim was sleep talking accompanied or not by eye- case series, sleepsex was rarely the only parasomnia behavior opening and closing, body movements, spontaneous tongue in the longitudinal histories of these patients (Schenck et al., movements). All these phenomena are compatible with 2007). automatic sexual movements during sleep, and therefore the Sleep structure is usually normal, but an increase in case may focus on the victim's response to the assailant's arousals during SWS, and sudden arousals from SWS are approaches. If consent could reasonably have been assumed frequently seen in sleepwalkers PSG (Espa et al., 2000). During to be given by the victim, then the sexual act would not the attack, the EEG is typically covered by movement artifacts, constitute a rape (Fenwick, 1996). but in some cases it is possible to identify mixed high ampli- As pointed out by Fenwick (1996),itwouldfirstbe tude slow waves, slow alpha, and theta waves without evi- necessary to establish that the victim would not have wanted dence of wakefulness, between these artifacts (Zadra et al., the sexual contact when awake. If it is clear that she/he would 2004). The subject is usually in stages 3 or 4, more rarely in not have done so, then the deliberation of rape will turn to stage 2 NREM sleep, preceding the onset of the abnormal whether the victim was actually asleep, and secondly to the behavior (Zadra et al., 2004). A burst of hypersynchronous high details of the assailant's behavior and the behavioral amplitude delta waves may be seen in the seconds preceding responses of the victim. In addition it will depend on whether the abnormal movement, persisting during the initial part of the victim's behavioral responses are part of a sleep repertoire the activity (Ebrahim et al., 2005; Pilon et al., 2006), although, it and could have been carried out during sleep. To assist in has recently been considered as a non-specific finding the determination of sleepwalking, the following criteria are (Szelenberger et al., 2005). generally regarded as essential for a diagnosis in the forensic When diagnosis is difficult to obtain, some maneuvers can context (for review Fenwick, 1996; Ebrahim, 2006 and refer- be applied to precipitate the sleepwalking episodes', such as: ences therein): General factors (family history, childhood prior sleep deprivation, arousing subject during SWS, or using sleepwalking, adolescent sleepwalking, and late onset sleep- alcohol prior to . Finally, other tests that may be useful walking) and specific factors (sleep stage, disorientation on in diagnostic screening include: actigraphy, multiple sleep awakening, confusional/automatic behavior, amnesia, trigger latency test, and repeated nocturnal EEG recording at home factors, and out of character behavior). Thus, this kind of (Guilleminault, AASM online). parasomnia may lead to a variety of medico-legal conse- quences, all of which bringing moral and psychological damage. Cases of sleep-related of children 9. Treatment typically have even more drastic long-lasting consequences. Safety precautions and good general measures are recommended for individuals with a parasomnia (Wills 8. Diagnostic aspects and Garcia, 2002). When associated syndromes are recognized, their specific treatment is also a priority. Of note, patients with The history must include detailed description of the event and parasomnias, sleep apnea, and restless legs syndrome should the degree of amnesia, current, past medical, as well as family be questioned (with their bed partners) about any associated history. Moreover, it should elicit presence of previously sleepsex, as pointed by Schenck and co-workers (2007). Most mentioned potential risk factors such as alcohol, drug or primary motor parasomnia cases reported in the literature medication intake, sleep deprivation, stressful life event, show a positive therapeutical response to . anxiety, etc. prior to parasomnic episode. It is also recom- Most disorders of arousal, such as sleepwalking, respond mended that social habits, employment records, and deter- especially well to (Remulla and Guilleminault, mination of the frequency of violence and its stereotypic 2004), making it a good first line of therapy for these cases of nature are investigated. A collateral history from the spouse, “sexsomnia”. The usual recommended dosage ranges from 0.5 bed partner, or family member is also helpful and should to 2.0 mg at bedtime. include: report of the event and prior events; timing of the Antidepressant medication such as sertraline or GABAergic event during sleep; frequency of events over time; age of agents such as valproic acid and lamotrigine may also be used. onset; associated life events or traumas; degree of amnesia However, many reported cases of sexsomnia do not have a observed; and attitude of the subject when fully awake after description of treatment or its effectiveness. In cases associ- the event. Finally, signs of febrile illness must be obtained ated with other sleep disorders, such as sleep-related breath- (Guilleminault, AASM – Medsleep www.aasmnet.org). ing disorders, the treatment should be aimed at the main A careful psychiatric evaluation is needed, because disso- disorder. A case of a patient who had severe obstructive sleep ciative states and early dementia can be associated with apnea syndrome and a history of inappropriate sexual abnormal behavior during the night (Guilleminault et al., behavior during sleep which was abolished after tracheosto- 1998). In some cases repeated PSG recordings are necessary, my has been described (Hurwitz et al., 1989). Sleep hygiene sometimes even home recordings, in order to monitor the measures should also be applied by patients, since disorgani- event. PSG is usually performed with additional EEG channels zation of sleep/wake schedule was pointed out by Moldofsky (minimum of 4 channels) and video monitoring (Plazzi et al., et al. (1995), as precipitating factor for increasing parasomnia 2005; Derry et al., 2006). The evaluation of the test should rule attacks.

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Since alcohol, drugs, stress, and sleep deprivation may a sexual behavior during sleep is rarely confirmed in the trigger the episodes, the patient should be informed and laboratory. In Shapiro's study (2003), a PSG and video carefully guided to avoid these factors. Stress management surveillance demonstrated that LD initiated sexual programs or psychotherapy may be helpful particularly if with his wife, which then led to intercourse. The PSG revealed there is anxiety, depression, or other psychiatric conditions that LD was “drifting” between stage 1 and wakefulness. which may be associated with the sleep disturbance. It is In summary, this sleep disorder should receive more known that sleep fragmentation, partial cumulative sleep attention. This condition appears to be underrecognized and deprivation, and total sleep deprivation in normal controls it is suggested that questions about sleep and sex be included result in a significant increase in SWS when sleep is permitted in the clinical evaluation of suspected parasomnias. Physi- to return to normal (see Pressman, 2007), supporting the cians assessing these cases should have a complete under- assumption that parasomnias may increase in frequency after standing of sleep physiology, behavior, and disorders. This an abnormal sleep condition. unfortunate condition brings about not only personal, marital, and familiar turmoil, but frequently results in medico-legal consequences. 10. Final considerations

In the last few decades, we have experienced a remarkable Acknowledgments increase in knowledge about human behavior during sleep, and about how sleep disorders (e.g. parasomnias) can emerge The authors would like to express their cordial thanks to or be induced. We have also improved our diagnostic skills Tathiana A.F. Alvarenga for kind assistance. This work was and treatment options of these disorders. Reports describing supported by grants from Associação Fundo de Incentivo à sexual activity of sleeping humans are still rather infrequent Psicofarmacologia (AFIP) and Fundação de Amparo à Pesquisa and the etiology of this peculiar sleep disorder is still obscure. do Estado de São Paulo (CEPID #98/14303-3 to ST). It is not clear if this constitutes a new clinical entity of parasomnias, and indeed a new disorder (for review Schenck et al., 2007). Moreover, sexsomnia is often a longstanding REFERENCES disorder that carries major adverse physical, psychosocial, and legal consequences. We anticipate that this condition is currently underreported. Alves, R., Aloe, F., Tavares, S., 1999. Sexual behavior in sleep, sleepwalking and possible REM behavior disorder: a case It has been shown in the case series presented here that report. Sleep Res. Online 2, 71–72. somnambulism associated with is predominantly a Andersen, M.L., Tufik, S., 2006. Does male sexual behavior require male disorder. The basis for the male predominance in the progesterone. Brains Res. Rev. 51, 136–143. reported cases of sexsomnia is not known (Schenck et al., Andersen, M.L., Martins, P.J.F., D'Almeida, V., Santos, R.F., 2007). If sexsomnia is similar in etiology to other NREM Bignotto, M., Tufik, S., 2004. Effects of paradoxical sleep parasomnias such as somnambulism then perhaps the deprivation on blood parameters associated with – infrequency of female somnambulistic behavior is related to cardiovascular risk in aged rats. Exp. Gerontol. 39, 817 824. Andersen, M.L., Martins, P.J.F., D'Almeida, V., Bignotto, M., Tufik, the fact that female genital exhibitionism and are S., 2005a. Endocrinological alterations during sleep deprivation also unusual occurrences. Females almost exclusively en- and recovery in male rats. J. Sleep Res. 14, 83–90. gaged in masturbation and sexual vocalizations, whereas Andersen, M.L., Perry, J.C., Tufik, S., 2005b. Acute cocaine effects in males commonly engaged in sexual fondling and sexual paradoxical sleep deprived male rats. Prog. Neuro- intercourse with females (Schenck et al., 2007). This may be Psychopharmacol. Biol. 29, 245–251. due, not only to cultural and social factors, but also to relative Besset, A., Espa, F., 2001. Disorders of arousal. Rev. Neurol. 157, S107–S111. sex differences. Boeve, B.F., Silber, M.H., Ferman, T.J., Lucas, J.A., Parisi, J.E., 2001. All cases of suspected sexsomnia should be thoroughly Association of REM sleep behavior disorder and evaluated with particular attention to the high-risk behaviors neurodegenerative disease may reflect an underlying known to precipitate sleepwalking, such as sleep deprivation, synucleinopathy. Mov. Disord. 16, 622–630. drug abuse, alcohol, and stress. This report is in agreement with Boeve, B.F., Silber, M.H., Parisi, J.E., Dickson, D.W., Ferman, T.J., previous literature showing that violent behavior during sleep is Benarroch, E.E., Schmeichel, A.M., Smith, G.E., Petersen, R.C., more frequent in males (Moldofsky et al., 1995; Mahowald and Ahlskog, J.E., Matsumoto, J.Y., Knopman, D.S., Schenck, C.H., Mahowald, M.W., 2003. Synucleinopathy pathology and REM Schenck, 1995; Ohayon et al., 1997; Schenck et al., 2007). sleep behavior disorder plus dementia or parkinsonism. As there is an increasing proportion of sleep deprived Neurology 61, 40–45. adults as well as teenagers, special attention should be paid to Bonkalo, A., 1974. Impulsive acts and confusional states during the consequences of sleep loss. In the older population, sleep incomplete arousal from sleep: crinimological and forensic fragmentation and sleep respiratory disorders (e.g. sleep implications. Psychiatr. Q. 48, 400–409. apnea) are very prevalent and have been described to Bonnet, M.H., Arand, D.L., 2003. Clinical effects of sleep precipitate sexsomnia in subjects with previous history of fragmentation versus sleep deprivation. Sleep Med. Rev. 7, 297–310. somnambulism. Shapiro and colleagues (2003) recommended Bratty, V., 1961. Attorney general for Northern Ireland. North. Irel. that the bed-partner be present during the full PSG assess- Law Rep. 78–110. ment. Since the incidence of parasomnic events is generally Buchanan, A., 1991. Sleepwalking and indecent exposure. Med. Sci. lower in the clinical setting (Mahowald, 2000a,b), the finding of Law 31, 38–40.

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