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pISSN 2093-9175 / eISSN 2233-8853 BRIEF COMMUNICATION https://doi.org/10.17241/smr.2020.00535

Sleep Environment and Non-Rapid Eye Movement-Related Parasomnia Among Children: 42 Case Series

Joohee Lee, MD, Sungook Yeo, MD, Kyumin Kim, MD, Seockhoon Chung, MD, PhD Department of , University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea

The purpose of this study was to identify the clinical features related to environment of non- rapid eye movement (NREM)-related parasomnia. It was a retrospective medical record review of 42 children. We investigated demographic information, sleep pattern, sleep environment, and the mother’s dysfunctional beliefs about the child’s sleep. The mean age of subjects was 6.3± 3.1. The diagnosis was (n = 21), (n = 8), confusional arousal (n = 2), and unspeci- fied (n = 11). The average time of sleep pattern was as follow; 21:39± 0:54 pm, time 22:13 ± 0:54 pm, wake-up time 7:37 ± 0:42 am and NREM-related parasomnia occurrence time 1:09 ± 2:04 am. The average number of co-sleeping members was 2.8. 48.5% (n = 16) mothers experienced coldness while sleeping, and 64.7% (n = 22) parents had dysfunctional beliefs about their children’s sleep. The large number of co-sleeping members, coldness mothers experienced while sleeping, and dysfunctional beliefs about their children’s sleep may influence the NREM-pa- rasomnia in children. Sleep Med Res 2020;11(1):49-52

Key WordsaaParasomnia, Sleep environment, Co-sleep, Children.

INTRODUCTION

Received: April 3, 2020 A significant number of children are impacted by sleep disorders, reported in 25–62% of Revised: April 27, 2020 Accepted: May 4, 2020 such children [1,2]. Among sleep disorders, parasomnia is more common in children than in Correspondence adults. Parasomnia is one of seven major categories of sleep disorders registered in the Inter- Seockhoon Chung, MD, PhD Department of Psychiatry, national Classification of (ICSD) [3]. Parasomnia is a phenomenon in which University of Ulsan College of Medicine, abnormal movements, behavior, emotional experiences occur that are not desired during Asan Medical Center, sleep or arousal. In ICSD-3, depending on the stage of sleep in which symptoms occur, para- 88 Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Korea somnias were classified into three clusters: non-rapid eye movement (NREM)-related para- Tel +82-2-3010-3411 somnias, REM-related parasomnias, and other parasomnias. The sleeping environment con- Fax +82-2-485-8381 E-mail [email protected] ditions often influence the occurrence and severity of parasomnia by sleep disruption. Any conditions that impair sleep maintenance and promote NREM fragmentation could increase ORCID Joohee Lee the risk of parasomnias [4]. https://orcid.org/0000-0002-3114-1944 Co-sleeping, which is a natural part of parenting in Eastern cultures, would be one of the Sungook Yeo https://orcid.org/0000-0003-4127-3040 risk factors for sleep disruption in children. In the past, co-sleeping was an important means Kyumin Kim of survival to protect their children from danger such as predators, poisonous bugs, or even https://orcid.org/0000-0003-1203-1157 Seockhoon Chung other humans during the night. As civilization developed, humans built houses and segregat- https://orcid.org/0000-0002-9798-3642 ed family members into separate rooms. This change was accompanied by changes in the atti- cc This is an Open Access article distributed un- tude towards co-sleeping. It has become a matter of choice for parents. With this change, sev- der the terms of the Creative Commons Attribu- eral intense controversy over the hazards and benefits of -sharing emerged. The most tion Non-Commercial License (https://creative- commons.org/licenses/by-nc/4.0) which permits typical topic is the case of sudden infant death syndrome, and the American Academy of Pe- unrestricted non-commercial use, distribution, diatrics issued guidelines warning against bed-sharing [5]. In Eastern cultures, co-sleeping re- and reproduction in any medium, provided the original work is properly cited. mains highly prevalent. Several interesting factors such as positive maternal attitudes towards

Copyright © 2020 The Korean Society of 49 Sleep Environment and NREM Parasomnia co-sleeping, number of children, and poor child health were RESULTS associated with an increased incidence of co-sleeping [6,7]. Recent studies have reported that co-sleeping has adverse ef- fects on infants’ sleep and increases arousal [7,8]. The mean age of subjects was 6.3± 3.1, and 27 (64.3%) chil- The influence of the environment is also critical. dren were males (Table 1). In sibling orders, the first child was Sleep disruption can be triggered by poor , in- the most common with 24 children (57.1%) followed by 11 cluding bright light, excessive noise, extreme temperature, second-born (26.2%) and one third-born (2.4%). The diagno- mattress, and so on [9]. Last, the mothers’ dysfunctional belief sis was night terror (n = 21, 50.0%), sleepwalking (n = 8), con- in their children’s sleep can negatively impact the child’s sleep fusional arousal (n = 2), and unspecified (n = 11). The average problems. For example, “If you don’t sleep well, you won’t be time of sleep pattern was as follow; bedtime 21:39 ± 0:54 pm, tall” or “If you talk nonsense while asleep, you have a mental problem” are typical concerns of parents. The parent’s dysfunc- Table 1. Demographic variables of 42 non-REM related parasom- nia cases tional belief could make a child’s sleep problem more severe and may terrorize the mother as well as the child. Of course, Variables Subjects (n = 42) there is a relationship between sleep with growth hormone and Sex (male) 27 (64.3) sleep problems in children with developmental delay, but it Sibling order cannot be reversed. 1st/2nd/3rd 24 (57.1) / We hypothesized that factors related to the sleeping environ- 11 (26.2) / 1 (2.4) ment may affect the occurrence or progression of parasomnia. Diagnosis The purpose of this study was to identify the clinical features re- Confusional arousal 2 (4.8) lated to the sleep environment of childhood-onset NREM-relat- Night terror 21 (50.0) ed parasomnia and to develop a nonpharmacological treatment. Sleep walking 8 (19.0) Unspecified 11 (26.2) METHODS Age (year) 6.3 ± 3.1 Family members (person) 4.1 ± 0.8 This study design was a retrospective review of the medical Persons in a room while sleeping (co-sleeping) 2.8 ± 1.0 records of pediatric patients younger than age 18 diagnosed Data are presented as n (%) or mean ± standard deviation. with parasomnia. Forty-two children with parents, who had visited the Pediatric Sleep Clinic at Asan Medical Center July 1, Table 2. Clinical characteristics of 42 non-REM related parasom- 2018–June 30, 2019, were included in this study. Cases with neu- nia cases rological damage, neurological diseases, or sleep difficulties -at Variables Subjects (n = 42) tributable to other major mental illnesses such as and Bedtime 21:39 ± 0:54 pm , were excluded from this study. The following infor- ± mation was reviewed through retrospective review of medical Sleep onset time 22:13 0:54 pm records: demographic information, the sleep pattern (bedtime, Wake-up time 7:37 ± 0:42 am sleep onset time, wake-up time, ), symptoms of parasomnias, Parasomnia event time 1:09 ± 2:04 am the environmental sleep conditions (noise, brightness, room Night sweats of children 12/33 (36.4) temperature, humidity, activities before bedtime), co-sleep en- Mothers who experienced coldness while sleeping 16/33 (48.5) vironment condition (the number of people sharing a room at Dysfunctional beliefs of mothers about their 22/34 (64.7) bedtime, patient’s night sweats, if the co-sleeping mother expe- children’s sleep riences coldness while sleeping) and mothers’ dysfunctional Children taking a 16/36 (44.4) beliefs about the relationship between sleep and growth. Based Children reporting noise complaints 3/34 (8.8) on the above data, we reviewed the clinical features of parasom- Children reporting that the sleeping space nias. SPSS version 21.0 software (IBM Corp., Armonk, NY, 8/34 (23.5) USA) was used for the statistical analysis. Statistical signifi- brightness problems Children reporting room temperature or cance was defined by a p value < 0.05. This study was approved 12/33 (36.4) by the Institutional Review Board of Asan Medical Center (IRB humidity complaints No. 2019-0954), which waived the requirement for informed Children with acute stressors 10/34 (29.4) consent. Children with poor hygiene activities bedtime 5/27 (18.5) (TV, smart phone) Data are presented as n (%) or mean ± standard deviation.

50 Sleep Med Res 2020;11(1):49-52 Lee J, et al. sleep onset time 22:13 ± 0:54 pm, wake-up time 7:37 ± 0:42 co-sleepers showed more frequent awakening than solitary- am and NREM-related parasomnia event time 1:09 ± 2:04 am sleepers [11]. Other studies using the of (Table 2). The average number of family members and persons mother-infants have reported that bed-sharing promoted infant in a room while sleeping (co-sleep) was 4.1 and 2.8, respectively. arousal as well as an arousal of the mother [11-13]. Twelve of 33 (36.4%) children reported night sweats, while 16 In this study, we observed that children diagnosed with pa- of 33 (48.5%) mothers experienced coldness while sleeping to- rasomnia perspired at night, but the mothers experienced gether. Among the parents of the subjects, 22 (64.7%) parents coldness. This difference in subjective thermal perceptions be- believed that sleep disorders would adversely impact their child’s tween children and mothers may have made the mother act to physical or psychological development. There was no significant warm the thermal environment. The exposure of heat or cold difference in clinical characteristics between night terror and is one of the critical factors that can affect sleep stages [14]. Too sleepwalking group except age (night terror 4.6 ± 2.8, sleep- much heat exposure by thermoregulatory behavior such as walking 8.5 ± 2.1). or clothing can increase wakefulness and decrease slow wave sleep and REM sleep, but cold exposure did not im- pact the sleep stage [15]. We can assume that the mother who DISCUSSION experienced coldness was not significantly impacted, but the child’s sleep with heat could be disturbed. Although the moth- In the investigation of the relationship between NREM para- er’s behavior was not investigated in this study, it is a topic somnia and sleep environment, the number of co-sleeping worth examining in subsequent studies. members was relatively large, approximately three people in Sleep problems of children are related to their parents’ the same space. Interestingly, many mothers experienced cold- levels [16]. In this study, mothers who came to the hospital be- ness next to their sleeping children who were perspiring. More cause of the child’s sleep problems were under much stress. They than half of the mothers had dysfunctional beliefs about sleep expressed concerns that ‘My child would have trouble growing if regarding their children. he or she couldn’t sleep well’ or ‘If my child talks nonsense while The significance of the sleep environment in sleep problems in asleep, it means that he or she may have a mental problem.’ is well known. Sleeping in a place that is noisy or too bright Dysfunctional beliefs in sleep refer to maladaptive ideas and leads to sleep problems in the child [2,10]. The physical envi- worry about sleep that are detrimental and increase sleep prob- ronment as well as the environment created by the co-sleeping lems. It is one of the critical factors that impact actual sleep mother can impact the child’s sleep. According to a previous problems [17]. Chronic patients have more dysfunc- path analysis study conducted by our team, sleeping problems tional beliefs about sleep and complain more negativity about occur more often in preschool children co-sleeping with par- the consequences of insomnia compared to healthy sleepers ents than in children sleeping alone [10]. Co-sleeping with [18]. These findings have been replicated in specific pediatric parents resulted in the mother perceiving her child as difficult populations whose parents have dysfunctional beliefs about to care for, and this mother’s stress was likely to be related to children’s sleep. The parent’s ideas about a child’s sleep problem the child’s sleeping problems and sleep environment. Through may impact the child’s dysfunctional belief and their child’s ac- the research results, we became interested in the relationship tual sleep [19,20]. between co-sleeping and NREM-parasomnias. The term ‘co- This study had limitations. First, it was a retrospective study. sleeping’ is a more comprehensive concept that includes ‘bed- The data used in the analysis were insufficient to understand sharing’ and ‘room-sharing.’ In this study, we did not distin- the clinical features regarding parasomnias fully. Second, the guish bed-sharing from room-sharing. sample size was small, and there were no controls. Last, clinical We hypothesize one of the important reasons for the high characteristics were collected without sleep polysomnography. prevalence of co-sleeping is that Korean have a floor- However, we observed the difference in subjective thermal per- heating system. The traditional floor-heating system heats the ception between parasomnia children and mothers. The con- floor and promotes the circulation of warm air to warm the en- nection between the thermal environment and NREM sleep tire room. Sleep space-sharing is comparatively much easier be- stage may have an implication of parasomnia. It remains un- cause much more extensive space, the whole floor instead of known if co-sleep conditions may be related to the predisposi- just the bed, could be used for sleeping. From the perspective tion of parasomnia. Further understanding of the relationship of space use and positive parental attitudes toward co-sleeping, between sleep environment and parasomnia could contribute a large number of parents opt to sleep with their children until to a better evaluation of the sleep environment and establish they attend elementary school. Apart from the discussion on proper sleep hygiene education and treatment. the safety of bed-sharing, a few studies have reported that bed- Acknowledgments sharing may have other adverse impacts on the quality of in- None. fants’ sleep [7,8]. One of the most replicated findings was that

www.sleepmedres.org 51 Sleep Environment and NREM Parasomnia

Conflicts of Interest ders: a brief review for clinicians. Dialogues Clin Neurosci 2003;5:371-88. The authors have no financial conflicts of interest. 10. Lee S, Ha J-H, Moon D-S, Youn S, Kim C, Park B, et al. Effect of sleep environment of preschool children on children’s sleep problems and Authors’ Contribution mothers’ . Sleep Biol Rhythms 2019;17:277-85. Conceptualization: Lee J. Data curation: Yeo S, Kim K. Formal analysis: 11. Mao A, Burnham MM, Goodlin-Jones BL, Gaylor EE, Anders TF. A Lee J, Yeo S. Investigation: Lee J, Yeo S. Methodology: Lee J, Kim K. Proj- comparison of the sleep-wake patterns of cosleeping and solitary-sleep- ect administration: Chung S. Resources: Yeo S, Kim K. Software: Lee J. ing infants. Child Psychiatry Hum Dev 2004;35:95-105. Supervision: Chung S. Validation: Lee J. Visualization: Lee J. Writing— 12. Mosko S, Richard C, McKenna J. Maternal sleep and arousals during bedsharing with infants. Sleep 1997;20:142-50. original draft: Lee J. Writing—review & editing: Chung S. 13. Mosko S, Richard C, McKenna J. Infant arousals during mother-infant bed sharing: implications for infant sleep and sudden infant death syn- REFERENCES drome research. Pediatrics 1997;100:841-9. 1. Owens J. Classification and epidemiology of childhood sleep disor- 14. Harding EC, Franks NP, Wisden W. The temperature dependence of ders. Prim Care 2008;35:533-46. sleep. Front Neurosci 2019;13:336. 2. Spruyt K, O’Brien LM, Cluydts R, Verleye GB, Ferri R. Odds, preva- 15. Okamoto-Mizuno K, Mizuno K. Effects of thermal environment on lence and predictors of sleep problems in school-age normal children. sleep and circadian rhythm. J Physiol Anthropol 2012;31:14. J Sleep Res 2005;14:163-76. 16. Shang CY, Gau SS, Soong WT. Association between childhood sleep 3. Sateia MJ. International classification of sleep disorders-third edition: problems and perinatal factors, parental mental distress and behavioral highlights and modifications. Chest 2014;146:1387-94. problems. J Sleep Res 2006;15:63-73. 4. Bollu PC, Goyal MK, Thakkar MM, Sahota P. Sleep Medicine: para- 17. Harvey AG. A cognitive model of insomnia. Behav Res Ther 2002;40: somnias. Mo Med 2018;115:169-75. 869-93. 5. Task Force on Sudden Infant Death Syndrome, Moon RY. SIDS and 18. Morin CM, Stone J, Trinkle D, Mercer J, Remsberg S. Dysfunctional other sleep-related infant deaths: expansion of recommendations for a beliefs and attitudes about sleep among older adults with and without safe infant sleeping environment. Pediatrics 2011;128:1030-9. insomnia complaints. Psychol Aging 1993;8:463-7. 6. Yang CK, Hahn HM. Cosleeping in young Korean children. J Dev Be- 19. Ng AS, Dodd HF, Gamble AL, Hudson JL. The relationship between hav Pediatr 2002;23:151-7. parent and child dysfunctional beliefs about sleep and child sleep. 7. Liu X, Liu L, Wang R. Bed sharing, sleep habits, and sleep problems Journal of Child and Family Studies 2013;22:827-35. among Chinese school-aged children. Sleep 2003;26:839-44. 20. Peltz JS, Rogge RD. The moderating role of parents’ dysfunctional 8. Madansky D, Edelbrock C. Cosleeping in a community sample of 2- sleep-related beliefs among associations between adolescents’ pre-bed- and 3-year-old children. Pediatrics 1990;86:197-203. time conflict, sleep quality, and their mental health. J Clin Sleep Med 9. Abad VC, Guilleminault C. Diagnosis and treatment of sleep disor- 2019;15:265-74.

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