Original Article

Co-sleeping and Childhood Enuresis in China Jun Ma, MD, PhD,*†‡ Shenghui Li, MD, PhD,† Fan Jiang, MD, PhD,*†‡ Xingming Jin, MD,*†‡ Xiaoming Shen, MD, PhD,*† Fei Li, MD, PhD*†‡ ABSTRACT: Objective: Co-sleeping is associated with disturbance of the natural sleep pattern, including sleep fragmentation and daytime sleepiness. Nocturnal enuresis (NE) or bed-wetting, although benign, is a significant cause of distress to affected children and their caregiver(s). This study investigated the relationship between co-sleeping and NE in primary school children from China. Methods: Data from a previous sleep study of primary school children from 8 cities across China were analyzed. Multivariable regression analysis was performed to assess the relationship between co-sleeping and NE while controlling for a number of confounding factors. The prevalence of NE in co-sleeping and non–co-sleeping children in different age groups was evaluated. Results: The prevalence of co-sleeping and NE in children aged 5 to 12 years was 22.8% and 4.6%, respectively. Co-sleeping was associated with a higher prevalence of NE in primary school age children (odds ratio [OR], 1.50; 95% confidence interval [CI], 1.27–1.77; p < .001) after adjusting for confounding factors. The differences in the prevalence of NE between co-sleepers and non–co-sleepers were significant in the 9-year age group (OR, 1.49; 95% CI, 1.06–2.11; p 5 .025) and 11- to 12-year age group (OR, 3.16; 95% CI, 2.19–4.57; p < .001). Conclusion: Co-sleeping may increase the risk of NE in primary school children, particularly in those aged 11 to 12 years. (J Dev Behav Pediatr 35:44–49, 2014) Index terms: co-sleeping, sleep disturbances, nocturnal enuresis, developmental milestones.

C

o-sleeping, defined as children frequently sleeping in their caregiver’s bed, is common in eastern cultures. Although it is accepted that co-sleeping provides both physical and emotional support to children, its benefits are controversial.1,2 Recent studies have shown that cosleeping is associated with sudden infant death syndrome, sleep-related nighttime crying, and various sleep disorders in older children.3–8 Studies have associated co-sleeping with sleep disturbances, such as fragmented sleep, daytime sleepiness, sleep anxiety, bedtime resistance, parasomnia, and sleep-disordered breathing.3,9–12 However, there is little information about the relationship between co-sleeping and nocturnal enuresis (NE).

From the *Department of Developmental and Behavioral Pediatrics, Shanghai Children’s Medical Centre, Shanghai Jiaotong University School of Medicine, Shanghai, China; †MOE-Shanghai Key Laboratory of Children’s Environmental Health, Shanghai Jiaotong University School of Medicine, Shanghai, China; ‡Shanghai Institute of Pediatric Translational Medicine, Shanghai Children’s Medical Centre, Shanghai Jiaotong University School of Medicine, Shanghai, China. Received May 2013; accepted September 2013. Supported by the Ministry of Education of China (NCET program), National Science Foundation of China (81000592, 91232706, 81222012), Science and Technology Commission of Shanghai Municipality (10DZ2272200, 09DZ2200900, 10PJ1407500, 10PJ1403500, 10231203903 and 10JC1411200), Shanghai Municipal Education Commission (11ZZ103), Shanghai Municipal Health Bureau (2010004), Morning Star Rewarding Fund (Category B, 2011,) and Bairen Rewarding Fund of Shanghai Jiaotong University. Disclosure: The authors declare no conflict of interest. Address for reprints: Fei Li, MD, PhD, Department of Developmental and Behavioral Pediatrics, Shanghai Children’s Medical Center, 1678 Dong fang Road, Shanghai, China 200127; e-mail: [email protected]. Copyright Ó 2013 Lippincott Williams & Wilkins

44 | www.jdbp.org

Nocturnal enuresis or bed-wetting is defined as involuntary urination during the night sleep after 5 years of age.13 Its cause is a complex one and still not fully understood. The 3 systems theory has been widely used to explain the pathogenesis of NE, including an impairment in the dialogue between the brain and bladder during sleep,13,14 dysregulation in the circadian rhythm of vasopressin secretion, and bladder dysfunction (see study by Butler and Holland17 for details).15–19 For example, an impairment in brain-bladder dialogue during sleep could cause children to fail to get up and urinate when the bladder is full. The dysregulation in the circadian rhythm of vasopressin secretion may lead to the nocturnal polyuria and exacerbate existing NE. The bladder dysfunction, for example, a small functional bladder capacity may induce higher frequency of bed-wetting. Co-sleeping is associated with fragmented sleep, which can result in sleep deprivation and delayed awakening. The latter may further compromise the dialogue between the brain and bladder in children with NE.20,21 Moreover, fragmented sleep may interfere with the circadian rhythm of vasopressin secretion, which in turn can cause nocturia and NE.22–24 Previous studies have shown that children’s age, gender, and body mass index are related to co-sleeping3,7,8,25 and NE.13,15,19 In addition, parents’ education, family structure, house size (defined as the average per-capita living area), and household income are associated with co-sleeping.3,7,8 Therefore, we hypothesized that co-sleeping with a caregiver may relate to childhood NE. We predicted that NE prevalence would be more significant in older co-sleeping children. A study by BaHammam et al26 is the Journal of Developmental & Behavioral Pediatrics

only report that shows that enuresis is a predictor of co-sleeping, but the authors failed to make any further interpretations about the relationship between the two. Because remission of NE is highly affected by environmental and training factors,27,28 the identification of risk factors will have significant clinical implications for treating NE.

METHODS Participants This study used data from a large sleep survey in primary school children from 8 cities across China. The sampling method and study design were described previously,3,29,30 and they are based on a clusterstratified selection method, which took into account population density, economic standards, and geographic location. Study subjects were from the Chinese cities of Urumqi, Chengdu, Xi’an, Hohhot, Wuhan, Canton, Shanghai, and Harbin. Three to 10 districts in each city and 1 to 3 primary schools within each district were randomly chosen. Of 23,791 children recruited from Grades 1 to 6 at 55 elementary schools, 22,018 (92.5%) met a minimum quality standard of being able to respond to the questionnaires. After excluding subjects with missing information on co-sleeping or bedwetting, 21,509 (90.4%) children were considered the study sample and included in the final analysis. There were 10,668 boys (49.6%) and 10,841 girls (50.4%), with a mean age of 9.16 years (SD, 1.73 years; range, 5–12 years). There were 4,901 (22.8%) co-sleepers and 16,608 (77.2%) non–co-sleepers.

Procedure The study protocol was approved by the Ministry of Education of the People’s Republic of China and Shanghai Jiao Tong University School of Medicine Human Research Ethics Committee. The questionnaires were distributed between November and December of 2005. The research aims and protocol were explained to the principals and teachers at the participating schools. The questionnaires were taken by the students to their caregiver(s). The accompanying introduction letter explained the project’s purpose and gave detailed instructions on how to complete the questionnaires. The teachers explained the importance of this investigation to the caregiver(s) of every student either by telephone or during home visits. Because of the increased public awareness about the impact of sleep patterns on health in recent decades in China, responses were generally positive. Caregivers who participated in this study completed questionnaires anonymously. Informed consent was obtained from the caregiver(s) and children.

Measures The questionnaires used in this study included the following: (1) a demographic section (37 items including age, gender, height, weight, physical, and psychological Vol. 35, No. 1, January 2014

condition); (2) a family and social environment section (41 items including parents’ education, household income, computer/television use, and homework schedule); (3) the children’s sleep habits questionnaire (36 items including sleep duration, bedtime behaviors, and daytime sleepiness); and (4) a quality-of-life section (25 items including children’s mood, feeling, self-consciousness, friendship, motivation, and interest). These questionnaires have been previously described.3,30,31 Sleep arrangements were identified with a particular question: “How often does your child sleep in the parent(s)/ caregiver(s) bed at night?” The answers were (1) usually, 5 to 7 nights per week; (2) sometimes, 2 to 4 nights per week; (3) rarely, 0 to 1 night per week. In this study, we defined co-sleeping as bed sharing that occurred 5 to 7 nights per week.3 The children that shared beds for less than 5 nights per week were defined as non-co-sleepers. This definition is in accordance with a previously published study.3 Nocturnal enuresis (NE) was defined as wetting the bed 2 or more times per week, according to the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision (DSM-4-TR).32 Although it was impossible to rule out secondary NE (due to some condition such as bladder infection) based on the questionnaire, it has been reported that more than 85% of NE in children is of a primary monosymptomatic type.33

Statistical Analysis Mean, standard deviation, frequency, and percentage were used to describe the demographic and social environment characteristics of co-sleeping and non–co-sleeping children, and the prevalence of co-sleeping and NE in different age groups. Student’s t test and x2 test were used to assess the difference between sleeping arrangements. Logistic regression analysis was performed to evaluate the association between co-sleeping and NE. A multivariable regression model was developed to adjust for confounding factors. Odds ratios and 95% confidence intervals were calculated for each age group. The prevalence rate of NE between co-sleeping and non–co-sleeping children in each age group was calculated and compared using x2 test. The Statistical Program for Social Science for Windows (Version 17; IBM, Chicago, IL) was used for the analyses. The statistical significance was set at p , .05 (2 tailed).

RESULTS The study included 4901 (22.8%) primary school children who co-slept with their caregiver(s) for 5 to 7 nights per week. There were no significant differences in gender and parents’ education between co-sleeping and non–cosleeping children. However, significantly more co-sleepers had nocturnal enuresis (NE) and were likely to live in a family with a single-parent or a large family structure, low household income, and small-sized house (Table 1). Overall, the prevalence of NE was 4.6% and that of cosleeping was 22.8%. In order to observe the age effects © 2013 Lippincott Williams & Wilkins

45

on co-sleeping and NE, the study sample was divided into 6 age groups: (1) 5 to 6 years of age (2536 subjects, 11.8%), (2) 7 years of age (3783 subjects, 17.6%), (3) 8 years of age (3812 subjects, 17.7%), (4) 9 years of age (3763 subjects, 17.5%), (5) 10 years of age (3686 subjects, 17.1%), and (6) 11 to 12 years of age (3929 subjects, 18.3%). Co-sleeping was more prevalent than NE in primary school children in all age groups (Fig. 1). Table 2 shows that co-sleeping was associated with a significantly higher occurrence of childhood NE in the bivariate analysis (odds ratio [OR], 1.56; 95% confidence interval [CI], 1.36–1.79; p , .001). The association of cosleeping with NE was significant after applying the multivariable logistic regression model and controlling for confounding factors (adjusted OR, 1.50; 95% CI, 1.27–1.77; p , .001). In each age group, there was a greater association between co-sleeping and NE prevalence than between non–co-sleeping and NE. The association between co-sleeping and NE prevalence was significantly higher in the age groups of 9 and 11 to 12 years

(9 years of age: x2 5 5.21; p 5 .025; 11–12 years of age: x2 5 43.76; p , .001). The OR for NE was 1.17 (95% CI, 0.86–1.60) for the age group of 5 to 6 years; 1.34 (95% CI, 0.89–1.79) for the age group of 7 years; 1.07 (95% CI, 0.75– 1.53) for the age group of 8 years; 1.49 (95% CI, 1.06–2.11) for the age group of 9 years; 1.20 (95% CI, 0.74–1.96) for the age group of 10 years; and 3.16 (95% CI, 2.19–4.57) for the age group of 11 to 12 years, after controlling for confounding factors (Fig. 2).

DISCUSSION In this study, we found that the difference in the prevalence rates of nocturnal enuresis (NE) between cosleepers and non–co-sleepers was 2.2%, representing a large number of cases (approximately 50%). The odds ratio (OR) for NE among co-sleepers was 1.5 times greater than that for non–co-sleepers after controlling for confounding factors. This suggests that children who co-sleep with their caregiver(s) are 1.5 times more likely

Table 1. The General Demographic and Social Environment Factors of Subjects by Sleep Arrangement Factors Male, n (%)

Co-sleeping (n 5 4901)

Non–co-sleeping (n 5 16,608)

t/x2

p

2392 (48.8)

8287 (49.9)

1.81

0.18

8.4 (1.6)

9.4 (1.7)

34.15

,0.001

Children’s body mass index, mean (SD)

17.1 (4.1)

17.5 (4.1)

6.05

,0.001

Nocturnal enuresis, n (%)

309 (6.3)

681 (4.1)

40.16

,0.001

199.67

,0.001

323 (6.6)

864 (5.2)

Age, mean (SD), yr

Family structure, n (%) Single-parent family Nuclear family

2676 (54.6)

10,911 (65.7)

Large family

1902 (38.8)

4833 (29.1)

Illiterate/elementary/middle school

2852 (58.2)

9716 (58.5)

High school

1549 (31.6)

5215 (31.4)

500 (10.2)

1677 (10.1)

Illiterate/elementary/middle school

2965 (60.5)

10,297 (62.0)

High school

1642 (33.5)

5331 (32.1)

294 (6.0)

980 (5.9)

,800

1113 (22.7)

3122 (18.8)

800–1500

1617 (33.0)

5481 (33.0)

1500–2500

1093 (22.3)

3953 (23.8)

.2500

1078 (22.0)

4052 (24.4)

902 (18.4)

2209 (13.3)

15–25

1593 (32.5)

5149 (31.0)

25–35

1171 (23.9)

4351 (26.2)

.35

Father’s educational levels, n (%)

College or above Mother’s educational levels, mean (SD)

College or above Household income (RMB [Yuan] per person per month), n (%)

House size (m2/person), n (%) ,15

1.69

0.79

8.10

0.09

40.21

,0.001

98.79

,0.001

1235 (25.2)

4899 (29.5)

Psychiatric disorder history, n (%)

260 (5.3)

681 (4.1)

11.78

0.001

Long-term medication use, n (%)

201 (4.1)

448 (2.7)

24.36

,0.001

46 Co-sleeping Correlates With Enuresis

Journal of Developmental & Behavioral Pediatrics

Figure 1. The prevalence rates of co-sleeping and nocturnal enuresis (NE) in different age groups. The x-axis represents the different age groups. The y-axis represents the percent prevalence rate of NE. Cosleeping was more prevalent than NE in all age groups.

to wet their beds than those who do not co-sleep. Given that NE is common in children, the OR is substantial. Furthermore, we found that the oldest age group (11–12 years of age) showed the highest OR for NE (3.16; 95% CI, 2.19–4.57; p , .001), suggesting that a long-term pattern of co-sleeping may slow down the remission of childhood NE and increase the odds of relapse or emergence of new cases. It is possible that co-sleeping is a coping strategy for parents whose children have sleeprelated problems, such as bedtime resistance.34 However, this is an unlikely explanation for children with NE because these children often wet their caregiver’s beds; these caregivers would likely prefer that their child sleep in a separate bed. A number of studies report that NE and other sleep problems are common in co-sleepers.35–37 Only one study examined the relationship between co-sleeping

and NE25; although the authors identified enuresis as a predictor of co-sleeping, they failed to interpret the relationship further. By analyzing the data from our study sample, we confirm that the association between co-sleeping and NE is significant, particularly in older co-sleepers. In addition, we carefully accounted for a number of confounding factors, making our data robust and highly reliable. Our results can be applied toward developing behavioral and interventional therapies to prevent and manage childhood NE. These findings warrant a future prospective cohort study and a mechanisms study to identify if there is a causal link between co-sleeping and NE. If proven, the causal link could be used to recommend that children with NE avoid co-sleeping with their caregiver(s). We postulate at least 3 possible mechanisms to explain the association between co-sleeping and NE: (1) co-sleeping increases the possibility of sleep disturbance, leading to sleep deprivation.3,6–8 Sleep deprivation causes delay or failure to get up to urinate and thus NE onsets; (2) co-sleeping–related sleep disturbance disrupts the secretion of vasopressin during the night, leading to nocturia, an important cause of NE15–19; and (3) caregiver(s) sharing beds are more likely to wake their children to urinate before the bladder is full. Evidence shows that this practice interferes with the development of both nighttime urination control and bladder capacity.38 All these practices cause children with NE to have a reduced sensation of bladder fullness during the night, a learning experience instrumental in developing mature urination habits. Furthermore, co-sleeping may slow down independency in children with NE, which is an important factor for a child to acquire when reaching the developmental milestone of nighttime urination control.39 We found that the prevalence rate of co-sleeping in Chinese children aged 5 to 12 years was 22.8%, much

Table 2. Factors Associated with Nocturnal Enuresis Evaluated by Logistic Regression Models Variables Co-sleeping

Unadjusted OR (95% CI)

p

Adjusted OR (95% CI)

p

1.56 (1.36–1.79)

,0.001

1.50 (1.27–1.77)

,0.001

Younger age

1.14 (1.10–1.19)

,0.001

1.13 (1.08–1.18)

,0.001

Gender (male)

1.55 (1.36–1.76)

,0.001

1.52 (1.30–1.76)

,0.001

Lower children’s body mass index

0.99 (0.97–1.00)

0.06

0.98 (0.97–0.99)

0.036

Family structure Single-parent family

1.52 (1.20–1.93)

0.001

Large family

1.75 (1.36–2.27)

,0.001

1.58 (1.16–2.14)

,0.001

1.15 (1.03–1.29)

Nuclear family Lower father’s educational levels

1.00 1.39 (1.30–1.49)

NS 0.004

1.00 0.015

Lower mother’s educational levels

1.40 (1.30–1.51)

,0.001

1.23 (1.09–1.38)

0.001

Lower household income

1.25 (1.17–1.33)

,0.001

1.10 (1.01–1.19)

0.028

Bigger house size (m2/person)

1.09 (1.02–1.16)

0.009

Psychiatric disorder history

2.55 (2.05–3.18)

,0.001

1.85 (1.42–2.42)

,0.001

Long-term medication use

2.05 (1.56–2.71)

,0.001

1.59 (1.15–2.22)

0.006

NS

A multivariable regression model controlled for various variables. NS, not significant.

Vol. 35, No. 1, January 2014

© 2013 Lippincott Williams & Wilkins

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enuresis (NE). A future prospective cohort study with a larger sample size is required to identify the causal relationship between co-sleeping and NE. ACKNOWLEDGMENTS The authors thank Drs. Shilu Tong, Jun Zhang, and Mark D. Simms for their comments. They also thank all participating principals, teachers, children, and their caregivers for their support for this study.

REFERENCES

Figure 2. The prevalence rates of nocturnal enuresis (NE) in cosleeping and non–co-sleeping children at different age groups. The x-axis represents the different age groups. The y-axis represents the percent prevalence rate of NE. *Co-sleeping was significantly associated with NE in older age groups (9 and 11–12 years of age) (p , .05).

higher than that in western cultures, where co-sleeping prevalence rates were reported to be 5.1% in Switzerland8 and 5.0% in Italy11 among children of a similar age. The prevalence rate of NE in Chinese children aged 5 to 12 years was 4.6%, similar to American primary school children.29 The prevalence rates of both co-sleeping and NE decreased as children grew, which is consistent with other reports.3,7,8,15,18,19 Furthermore, male gender, lower body mass index, less educated parents, lower household income, children’s history of psychiatric disorders, and long-term medication were associated with a greater risk of NE, which is also in accordance with the results of previous large scale surveys.28,29,40,41 There are several limitations to our study. First, using a questionnaire to define NE and co-sleeping made it difficult to identify the potential causes of NE and co-sleeping, which is usually possible through structured interviews, clinical examinations, and laboratory tests. However, similar questionnaires have been applied in previous studies to categorize NE and co-sleeping,3,41 an observation that provides validity to our results. Second, this study is cross-sectional in nature, providing an association between co-sleeping and NE, rather than revealing a causational relationship between the two. Third, although in every age group, the prevalence rate of NE in co-sleepers was higher than that in non– co-sleepers, significant differences were only observed in the age group of 9 and 11 to 12 years. The small sample size of each age group was the most likely reason for this outcome, which suggests the need for a future study with a larger sample size.

CONCLUSION Co-sleeping between caregiver(s) and children, especially older children (9 and 11–12 years of age), was associated with a significantly higher risk of nocturnal 48 Co-sleeping Correlates With Enuresis

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Co-sleeping and childhood enuresis in China.

Co-sleeping is associated with disturbance of the natural sleep pattern, including sleep fragmentation and daytime sleepiness. Nocturnal enuresis (NE)...
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