Sleep Problems and Daytime Sleepiness in Children with Nocturnal Enuresis

Article Information

Child Kidney Dis. 2016;20(2):50-56
Published online October, 30, 2016. doi: http://dx.doi.org/10.3339/jkspn.2016.20.2.50
1Department of Pediatrics, Busan St. Mary’s Hospital, Busan, Korea
2Department of Pediatrics, Kyungpook National University School of Medicine, Daegu, Korea
3Department of Pediatrics, Catholic University of Daegu School of Medicine, Daegu, Korea
Corresponding author:Min Hyun Cho, M.D. Department of Pediatrics, Kyungpook National University Medical Center, 807 Hogukno, Buk-gu, Daegu 41404 Korea Tel: +82-53-200-2741 Fax: +82-53-200-2039 E-mail: chomh@knu.ac.kr
Received : July, 28, 2016. October, 10, 2016. Accepted : October, 11, 2016.
Copyright © 2016 The Korean Society of Pediatric Nephrology 2016 This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Purpose

Nocturnal enuresis (NE) is one of the most common problems in childhood. NE has a multifactorial etiology and is influenced by sleep and arousal mechanisms. The aim of the present study was to prospectively evaluate sleep problems and patterns in children with NE compared with normal healthy controls.

Methods

Twenty-eight children with NE and 16 healthy controls were included in the study. To evaluate sleep habits and disturbances, parents and children filled out a questionnaire that included items about sleep patterns and sleep-related behaviors prior to treatment for NE. Demographic factors and other data were compared for the two groups based on the responses to the sleep questionnaire.

Results

Night awakening, sleepwalking, and periodic limb movements were more prevalent in children with NE, but symptoms of sleep-disordered breathing were not increased in this group. There were statistically significant differences in periodic limb movements and daytime sleepiness between the two groups.

Conclusion

Children with NE seemed to have more sleep problems such as night awakening, sleepwalking, and periodic limb movements. In addition, a higher level of daytime sleepiness and hyperactivity in patients with NE suggested a relationship between NE and sleep disorders.

Keywords: Nocturnal enuresis, Children, Sleep disorder, Periodic limb movement

Introduction

Nocturnal enuresis (NE) is commonly called nighttime bedwetting and refers to discrete episodes (≥1 time/month) of urinary incontinence during sleep in children ≥5 years of age [1]. NE is a common problem in children, occurring in approximately fifteen percent of five-year-old children. Children with NE can suffer from emotional stress or psychological injury, such as low self-esteem, depression, guilt, discouragement, and anxiety [2]. In spite of perceived risk of psychosocial problems associated with NE, the treatment for NE may be prolonged and is often associated with relapses because the etiology is ambiguous and multifactorial [3-5].

Among many potential causes of NE, increased nocturnal urine production, bladder instability, and decreased nocturnal bladder capacity are considered as the main pathophysiological mechanisms. On the other hand, a correlation between sleep disorder and NE could also be considered as a cause, as found by some previous studies [6,7]. The children affected by NE could have a high threshold of cortical arousability, so they are unable to awake when the bladder reaches its maximum capacity. Some authors noted that the prevalence of obstructive sleep apnea and periodic limb movements were increased in enuretic children. Moreover, bedwetting could disturb the children’s sleep, as they would have to change out of wet clothes and in turn evoke problems of daytime sleepiness. Therefore, we should be interested in the sleep habits of children affected by NE.

The aim of this study was to evaluate the association between NE and sleep related problems including daytime sleepiness among Korean children.

Materials and methods

The study was carried out among children who were diagnosed as suffering from NE in Kyungpook National University Hospital during a 7-month period from April 2013 to October 2013. NE was defined as repeated urination into the bed or clothes during sleep, occurring ≥1 time per month for at least three consecutive months in a child ≥5 years of age. All children previously diagnosed with NE or found to be suffering from NE due to secondary etiologies on history taking, routine blood and urine analysis were excluded from the study. Those with urinary incontinence associated with a well-known urological dysfunction or neurological disease and taking some form of medication for enuresis were also excluded. The subjects in the control group were recruited from the healthy children who were involved in the study of normal polysomnographic characteristics [8]. To obtain data about their sleep pattern and problems associated with sleep, the sleep questionnaire was used in both groups.

The sleep questionnaire was designed for children and parents to collect information about baseline sleep patterns and problems. Baseline clinical characteristics of sleep patterns include sleep duration, time to sleep and sleeping place. The sleep questionnaire about sleep patterns includes 4 domains: (1) bedtime behaviors and insomnia symptoms (4 items), (2) symptoms of sleep disturbance during the night (5 items), (3) symptoms of sleep disordered breathing (3 items), (4) symptoms of excessive somnolence and behaviors of daytime (10 items) (Table 1, Appendix). A 5-point response scale is used on each question (0=never a problem; 1=almost never a problem (0-1 day per week); 2=sometimes a problem (2-4 days per week); 3=often a problem (more than 5 days per week); 4=unknowingness). The items were selected from Sleep Disturbances Scale for Children (SDSC), Pediatric Sleep Questionnaire (PSQ), and Pediatric Daytime Sleepiness Scale (PDSS) by the authors, and these were translated into the local language. The questionnaire was completed jointly by the parents and children during their first hospital visit. In addition, their demographic data and medical history were also collected. The questionnaire of control group was filled out by their parents. This study was approved by the institutional review board of Kyungpook National University Hospital (KNU MC 13-1020). The aim of the study was described in the top of the sleep questionnaire and all parents and children gave their written informed consent.

Table 1.
Table 1.

Sleep Questionnaire Items used for the Subjects

Statistical analysis was performed using PASW statistical software version 18.0 (IBM, Somers, NY, USA). Analysis of results was performed using Kolmogorov-Smirnov test of normality. A chi square test was also used to compare the statistical difference between NE group and control group. P-value ≤0.05 was considered significant.

Results

1. Demographic Characteristics and Baseline Sleep Patterns of the Subjects

Forty-four subjects were included in this study, which included twenty-eight children affected by NE (NE group) and sixteen healthy children (control group). The mean age of the children in NE group was 8.4±3.2 years, (range: 5-17 years) and gender ratio 13:15 (male: female). In control group, the mean age was 6.7±2.0 years, (range: 5-10 years) and gender ratio 11:5 (male: female) (Table 2). Table 2 shows the mean sleep latency, sleep duration and co-sleeping and similar results of two groups. In addition, there were no definite difference of sleep duration between weekday and weekend.

Table 2.
Table 2.

Demographic Characteristics and Baseline Sleep Patterns of the Subjects

2. Bedtime behaviors and insomnia symptoms

Compared to control group, children in NE group showed higher prevalence of irregular bedtime (7 children, 25% vs. 2 children, 12.5%) and night awakening (6 children, 21.4% vs. 1 child, 6.2%), while they had a similar prevalence in the symptoms of reluctance to go to sleep and sleep latency (10.7% vs. 12.5%, 21.4% vs. 25%, respectively) (Table 3). However, this was not statistically significant.

Table 3.
Table 3.

Symptoms of Bedtime Behavior and Sleep Disordered Breathing in Subjects

3. Symptoms of sleep disturbance during sleep

The prevalence of periodic limb movement was significantly higher in NE group than in control group (10 children, 35.7% vs. 1 child, 6.2%, P=0.036). Other symptoms like sleep talking (21.4% vs. 12.5%), sleepwalking (7.1% vs. 0%), teeth grinding (7.1% vs. 6.2%), and kicking legs (7.1% vs. 0%), also showed higher prevalence in NE group than controls but did not differ significantly (Fig. 1).

Fig. 1.
Fig. 1.

During sleep, sleep talking, sleep walking, bruxism, and periodic limb movement were more prevalent in children with nocturnal enuresis. There was statistically significant difference in periodic limb movements (P=0.036) between the two groups. NE, nocturnal enuresis.

4. Symptoms of sleep disordered breathing

Half of the children (50%) in both NE group and control group had the symptom of mouth breathing and they had a similar prevalence of snoring (14.3% vs. 18.8%). No NE individual had sleep apnea (Table 3).

5. Symptoms of daytime sleepiness

Children with NE had a higher prevalence of all symptoms concerned with daytime behaviors except inattentiveness, as compared to controls. Especially, the prevalence of some daytime behaviors like difficulty in waking up in the morning (42.9% vs. 12.5%, P=0.03) and hyperactivity (53.6 % vs. 12.5%, P=0.01) was significantly higher in NE group than in control group (Fig. 2).

Fig. 2.
Fig. 2.

Children with nocturnal enuresis have a higher level of daytime sleepiness and hyperactivity. NE, nocturnal enuresis.

Discussion

This study showed the interesting finding that NE group had a higher prevalence for most sleep-related problems and bad bedtime habits as compared to the control group. Especially, the prevalence of periodic limb movements, difficulty to wake up in the morning, and hyperactivity, was significantly different between both groups. However, both groups had no difference in the prevalence of symptoms suggestive of sleep apnea.

NE could alter sleep architecture or be the consequence of an abnormal sleep structure. Previous reports show that NE could be associated with sleep-disordered breathing, especially obstructive sleep apnea [9]. Sleep-disordered breathing is a common problem during childhood and is a term that describes a spectrum of upper airway obstruction during sleep from primary snoring to obstructive sleep apnea. One of the potential mechanisms accounting for the increased prevalence of enuresis in sleep apnea may be related to the release of both atrial and brain natriuretic peptides from cardiac myocytes after cardiac wall distension, as induced by the increased negative intrathoracic pressure following inspiratory efforts [10]. On the basis of these findings, it is suggested that NE could be used as a predictor of sleep-disordered breathing [11] and obstructive sleep apnea may be a new therapeutic target for NE.

In publishing literature, several researchers reported that therapy-resistant children with NE displayed higher periodic limb movements in sleep and sleep fragmentation than the controls [12-14]. They found that the periodic limb movement index and total arousal index were increased in children with NE, without a significant association with the other enuretic parameters, and suggested a hypothesis that it could refer to an autonomic imbalance as an independent pacemaker, with a possible key role for dopaminergic neurotransmission [13,14]. However, other studies using polysomnography revealed that the sleep architecture did not significantly differ between NE children and normal controls and between wet and dry nights in a NE individual and nocturnal enuresis occurred with almost the same frequency in all sleep stages [15,16]. It seems that further studies are needed to determine the potential factors influencing not only awakening threshold but also sleep architecture.

According to a nationwide epidemiological study of NE in Korean adolescents and adults, the incidence of NE was especially high in the adolescent and adult population with chronic insomnia and it could be a result of NE [17]. Existing evidence suggests that sleep disturbances at night are associated with both emotional and behavioral difficulties in daytime and evoke cognitive impairment and learning disabilities [18-20].

This study showed that children with NE have a higher prevalence of daytime sleepiness. The daytime sleepiness could be induced by NE disturbing the sleep or result from a combination of abnormal sleep structure and nocturnal enuresis [21]. The majority of children with NE tend to have poor sleep quality and quantity because they awake to urinate at night by themselves or are awoken by their parents [4]. While adults with sleep disturbance complain of sleepiness, children with sleep disturbances could show attention deficit or hyperactivity during the day. In our study, children with NE had a higher prevalence of hyperactivity, such as fidgetiness or difficulty to stay seated, than controls. Although it is hard to conclude this phenomenon is due to sleep disturbance resulting from NE, the clinicians have to consider this possibility and, in severe cases, consider further evaluation including psychological assessment.

Children with NE could be assailed by emotional instability or discouragement and tend to have a sad mood or low self-esteem. Bedwetting may harm the child’s relationships with family or friends and could negatively affect social development. Moreover, psychosocial problems could be intensified if daytime sleepiness or declining activity is combined with NE due to sleep disturbance [9,22]. In general, physicians and parents of NE children tend to focus on the symptom of NE and insufficiently consider sleep disturbances or problems associated with it [23].

NE is a multifactorial condition with different contributing factors; so careful evaluation and management are required to determine specific urological issues such as nocturnal polyuria or overactive bladder, psychosocial, and sleep-related problems. Therefore, it is important to be fully aware of NE-related sleep disturbance or daytime problems as well as NE itself.

NE has a high rate of spontaneous resolution. However, active intervention for NE is recommended to patients at emotional or psychosocial risk, especially adolescents. If sleep-related problems or therapy resistance are indicated, a multidisciplinary setting should be considered for diagnosis and treatment. For example, the patients with periodic limb movement disorder need further evaluations for restless legs syndrome and medical treatment, such as dopamine agonist or iron supplementation. And surgical treatment is helpful for the children with moderate to severe obstructive sleep apnea syndrome.

One limitation of this study is the relatively small sample size. The other limitation, which should be considered, is that this is a questionnaire-based study, wherein the questionnaire is a subjective tool, without polysomnography or physical activity monitoring system. In addition, we used the questionnaire where the items were selected and organized from international sleep associated questionnaires by the authors and then translated into the local language. An internationally authorized sleep questionnaire for Korean children needs to be developed.

Conclusively, the present study is the first study on the prevalence of NE combined with sleep-related problems in Korean children. Further studies are needed to clarify whether sleep related problems are improved following treatment of NE.

Footnotes

Conflict of interest

No potential conflict of interest relevant to this article was reported.

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Appendix

Fig. 1.

During sleep, sleep talking, sleep walking, bruxism, and periodic limb movement were more prevalent in children with nocturnal enuresis. There was statistically significant difference in periodic limb movements (P=0.036) between the two groups. NE, nocturnal enuresis.

Fig. 2.

Children with nocturnal enuresis have a higher level of daytime sleepiness and hyperactivity. NE, nocturnal enuresis.

Table 1.

Sleep Questionnaire Items used for the Subjects

Bedtime behaviors and insomnia symptoms
 The child has irregular bedtime routine.
 The child goes to bed reluctantly.
 How long after going to bed does your child usually fall asleep? (more than 30 min)
 The child wakes up more than twice per night.
Symptoms of sleep disturbance during the night
 You have observed the child talking in his/her sleep.
 You have observed the child sleepwalking.
 The child grinds his/her teeth during sleep.
 The child has jerking of legs while asleep.
 You have observed periodic limb movements of child during sleep.
Symptoms of sleep disordered breathing
 The child snores.
 The child gasps for breath or in unable to breath during sleep.
 You have observed the child mouth-breathing.
Symptoms of excessive somnolence and behaviors of daytime
 The child awakes in the morning feeling tired.
 The child is difficult to wake up in the morning.
 The child falls asleep or gets drowsy during class.
 The child is tired and grumpy during the day.
 The child does not seem to listen when spoken to directly.
 The child has difficulty organizing tasks and activities.
 The child is easily distracted by extraneous stimuli.
 The child fidgets with hands or feet or squirms in seat.
 The child in “on the go” or often acts as if “driven by motor”.
 The child interrupts others (conversation or games).

Table 2.

Demographic Characteristics and Baseline Sleep Patterns of the Subjects

NE Group Control Group
No n=28 n=16
M: F 13:15 11:5
SL (min) 16.8±13.19 (range: 2-60) 16.2±14.23 (range: 5-40)
SD-WD (min) 538.6±69.06 (range: 360-630) 564.4±41.31 (range: 480-660)
SD-WE (min) 567.1±50.17 (range: 480-660) 561.9±62.11 (range: 420-680)
Co-sleeping n=18 (64.3%) n=12 (75.0%)
Age (yr.) 8.4±3.19 (range: 5-17) 6.7±1.98 (range: 5-10)

Data are presented as mean±SD.

Abbreviations: NE, nocturnal enuresis; No, number; M, male; F, female; SL, sleep latency; SD, sleep duration; WD, weekday; WE, weekend.

Table 3.

Symptoms of Bedtime Behavior and Sleep Disordered Breathing in Subjects

NE Group (n, %) Control Group (n, %) P value
Bedtime behavior and insomnia symptoms of the subjects
 Irregular bed time routine 7, 25 2, 12.5 0.45
 Going to bed reluctantly 3, 10.7 2, 12.5 0.608
 Prolonged sleep latency 6, 21.4 4, 25 0.692
 Night awakening 6, 21.4 1, 6.2 0.533
Symptoms of sleep disordered breathing in subjects
 Snoring 4, 14.3 3, 18.8 0.504
 Sleep apnea 0, 0 1, 6.2 0.364
 Mouth breathing 14, 50 8, 50 1

Abbreviation: NE, nocturnal enuresis.