Abstract
A cross-sectional study was conducted between October 2019 and January 2020 in seven Japanese municipal elementary schools in Higashiyamato City, Tokyo. A questionnaire was distributed to 922 children enrolled in the 1st and 2nd grades. After excluding incomplete questionnaires, 629 (52.3% male) children were included in the analysis. Both sleep disorders and constipation are highly prevalent among elementary school children and could be associated with each other since sometimes they coexist in adults. Therefore, the purpose of the present study was to evaluate the association between sleep and constipation among community-based elementary school children. Among children who reported insufficient sleep, multivariable-adjusted odds ratio (95% confidence interval) for constipation was 2.82 (1.48–5.37; p-value: 0.002) and 2.19 (1.26–3.84; p-value: 0.008) for children reporting unrefreshing sleep. Constipation was significantly associated with insufficient and unrefreshing sleep in elementary school children. Since both functional constipation and sleep have been reported to be strongly linked with altered gut microbiome, future studies assessing the value of symbiotics in addressing these issues seem warranted.
Keywords: Sleep, Constipation, Children, Japan
Introduction
Sleep disorders [1], as well as obstructive sleep apnoea, are highly prevalent in school children [2] and are associated with physical, cognitive and behavioral consequences that can translate into academic failure, depression, hypertension, enuresis and many other problems [1, 3, 4]. We previously reported that shorter sleep duration is associated with an increased risk of obesity and behavioral problems in a large cohort of elementary school children in Japan [2] and also in the USA [5].
Constipation is also a common occurrence in school children, with estimated prevalence ranging from 0.5 to 32.2% in children from birth to eighteen years of age [6]. Functional constipation has been shown to impair health-related quality of life and to increase school absenteeism [7]. In as much as a quarter of the children who suffer from constipation, the problem persists into adulthood [8]. However, medical care is provided to only a small minority of such children. Indeed, only 3% of all the visits to pediatric clinics mentioned constipation as a significant problem [9], thereby accounting for the reduced frequency of therapeutic interventions.
Poor sleep is associated with gastrointestinal symptoms among adult patients with either irritable bowel syndrome or with chronic constipation [10]. Considering the elevated prevalence of both sleep disorders and constipation in elementary school children, it is quite possible that these two conditions may be interrelated. However, there is only limited evidence on their putative association pediatric cohorts. Therefore, the purpose of the present study was to evaluate the association between sleep disorders and constipation in community-dwelling elementary school children.
Methods
Participants
A cross-sectional study was performed between October 2019 and January 2020 at seven Japanese municipal elementary schools in Higashiyamato City, Tokyo, which has a population of approximately 85,000. A parents-reported questionnaire was distributed to 922 children in the first grade (6–7-year-old) and in the second grade (7–8-year-old). Parents and caregivers answered the questionnaires. The participating children and their parents completed informed assent and consent forms before participation. The questionnaire response rate was 70.8%. The study protocol was approved by the Juntendo Hospital Ethics Committee (#18-032).
Criteria for definition of constipation
The prevalence of constipation can vary greatly depending on the definition used. Some community-based studies use a single symptom while others use a combination of symptoms from the Rome criteria to define clinical constipation [11].
According to the Rome IV consensus guidelines, both constipation type I and type II were defined in the present study. Infrequent bowel movements (Constipation type I) were assessed using a Likert-type response scale with the following responses: ‘two to three times a day’, ‘once a day’, ‘two to three times a week’, and ‘less than three times a week’. Responses of ‘two to three times a week’ and ‘less than three times a week’ were defined as constipation. This conforms with the recommendations included in the Rome IV criteria, which is the most widely accepted diagnostic criteria for functional constipation, and defines it as ‘two or fewer defecations in the toilet per week’. Hard stools and painful evacuations (Constipation type II) were assessed using the following responses: ‘comfortable stool’, ‘loose stool to diarrhea’, ‘hard stool’, ‘constipation’, and ‘mix of diarrhea and constipation’. The responses of ‘hard stool’, ‘constipation’, and ‘mix of diarrhea and constipation’ were defined as constipation. These criteria also conform to the Rome IV consensus guidelines, which define it as a ‘history of painful or hard bowel movements”.
Questionnaires and variables
In addition to the items concerning constipation, the survey questionnaire included questions regarding the child’s sleep, as well as demographic variables such as sex, age, height, and weight.
The questions on sleep-associated behaviors and symptoms included the following: ‘What time does your child go to bed?’, ‘How long does your child sleep?’, ‘Does your child snore during sleep?’, ‘Do you think your child’s sleep is sufficient?’, ‘Does your child have difficulty getting up in the morning?’, ‘Does it take time for your child to wake up properly in the morning?’, and ‘Does your child seem tired?’. The weekly frequencies of unrefreshing sleep were evaluated by the statements of ‘waking up properly in the morning’ and ‘difficulty getting up in the morning’, and were assessed using a Likert-type response scale with the following responses: ‘never,’ ‘once,’ ‘twice,’ ‘three to four times,’ or ‘five or more times’ [3]. The weekly frequency of daytime tiredness was also assessed using a Likert-type response scale with the following responses: ‘never,’ ‘once,’ ‘twice,’ ‘three to four times,’ or ‘five or more times’. Those questions addressing "insufficient sleep" are derived from a well-established questionnaire on pediatric sleep apnea, i.e., Japanese version of the severity hierarchy score (SHS-J) [12].
The questionnaire also covered the participants’ medical history, including diseases such as asthma and adenotonsillar hypertrophy. The Rohrer’s index, which is a widely used anthropometric measure, was used to assess obesity, and was calculated using the following formula: Rohrer’s index = 100 × body weight (g)/length (cm)3. In general, children in Japan with a Rohrer’s index of > 145 are considered overweight.
Data analysis
Univariate and multivariate logistic analyses were employed to evaluate odds ratios (ORs) and the 95% confidence intervals (95% CI) for constipation, with children who reported sufficient sleep, refreshing sleep, or not being tired in the morning serving as reference.
Multivariate analyses were adjusted for potential confounding factors including age, gender, Rohrer’s index, snoring frequency during sleep, and weekday sleep duration. All statistical analyses were performed using SAS version 9.4 software (SAS Institute Inc., Cary, NC, USA).
Results
Participant demographics
We received 653 responses. After excluding incomplete questionnaires, complete datasets for 629 children (first graders: n = 327; second graders: n = 302) were available for analysis. Table 1 shows the demographic characteristics of the participants, including the two types of constipation reports, i.e., infrequent bowel movements and hard stool. The prevalence of constipation I and II was higher in girls (31 and 20.7%, respectively) compared to boys (23.1 and 8.8%; p < 0.05 for both). The average sleep duration was similar in boys and girls. Demographics of excluded participants from the analysis are shown in Supplementary Table 1.
Table 1.
Study participant demographics
| All | Boys | Girls | p-valueb | |
|---|---|---|---|---|
| N | 629 | 329 | 300 | |
| Age, mean (SD) | 7.2 (0.7) | 7.1 (0.6) | 7.2 (0.7) | 0.64 |
| Rohrer’s index, mean (SD) | 129.2 (16.2) | 128.0 (15.3) | 130.6 (17.1) | 0.44 |
| Overweight,a n (%) | 75 (12.3) | 33 (10.3) | 42 (14.5) | 0.11 |
| Hypertrophy of adenoid or tonsilla, n (%) | 48 (7.6) | 32 (9.7) | 16 (5.3) | 0.04 |
| Weekday sleep duration (min), mean (SD) | 553.6 (37.4) | 553.1 (35.6) | 554.2 (39.4) | 0.49 |
| Constipation type I, n (%) | 169 (26.9) | 76 (23.1) | 93 (31.0) | 0.03 |
| Constipation type II, n (%) | 91 (14.5) | 29 (8.8) | 62 (20.7) | < 0.0001 |
aRohrer’s index > 145
bp-value for chi-squared test
Association between sleep sufficiency and constipation
Table 2 shows the sex-specific prevalence of constipation and ORs (95% CI) in children according to their sleep sufficiency. Globally, the prevalence of constipation type II in children with insufficient sleep was higher (p = 0.003). The multivariate-adjusted OR (95% CI) of constipation type I and type II for all children with insufficient sleep was 1.25 (0.72–2.33) and 2.82 (1.48–5.37; p < 0.05), respectively, compared to those with sufficient sleep, (Girls: 3.47 (95% CI 1.43–8.66); Boys: 2.44 (95% CI 0.90–6.63)).
Table 2.
Odds ratios (95% confidence interval) for constipation according to sleep insufficiency
| Sufficient sleep | Insufficient sleep | p-value | |
|---|---|---|---|
| All | 565 | 64 | |
| Constipation type I, n (%) | 150 (26.6) | 19 (29.7) | |
| Univariate model | 1.00 | 1.17 (0.66–2.06) | 0.59 |
| Multivariate model 1a | 1.00 | 1.17 (0.68–2.15) | 0.53 |
| Multivariate model 2b | 1.00 | 1.25 (0.72–2.33) | 0.44 |
| Constipation type II, n (%) | 74 (13.1) | 17 (26.6) | |
| Univariate model | 1.00 | 2.40 (1.31–4.40) | 0.005 |
| Multivariate model 1a | 1.00 | 2.69 (1.43–5.06) | 0.002 |
| Multivariate model 2b | 1.00 | 2.82 (1.48–5.37) | 0.002 |
| Boys | 292 | 37 | |
| Constipation type I, n (%) | 69 (23.6) | 7 (18.9) | |
| Univariate model | 1.00 | 0.75 (0.32–1.79) | 0.52 |
| Multivariate model 3c | 1.00 | 0.75 (0.31–1.79) | 0.51 |
| Multivariate model 4d | 1.00 | 0.78 (0.33–1.87) | 0.58 |
| Constipation type II, n (%) | 23 (7.9) | 6 (16.2) | |
| Univariate model | 1.00 | 2.26 (0.86–5.99) | 0.10 |
| Multivariate model 3c | 1.00 | 2.38 (0.89–6.34) | 0.08 |
| Multivariate model 4d | 1.00 | 2.44 (0.90–6.63) | 0.08 |
| Girls | 273 | 27 | |
| Constipation type I, n (%) | 81 (29.7) | 12 (44.4) | |
| Univariate model | 1.00 | 1.90 (0.85–4.23) | 0.12 |
| Multivariate model 3c | 1.00 | 1.76 (0.79–3.99) | 0.17 |
| Multivariate model 4d | 1.00 | 2.13 (0.91–5.03) | 0.10 |
| Constipation type II, n (%) | 51 (18.7) | 11 (40.7) | |
| Univariate model | 1.00 | 2.99 (1.29–6.95) | 0.01 |
| Multivariate model 3c | 1.00 | 3.00 (1.30–6.92) | 0.01 |
| Multivariate model 4d | 1.00 | 3.47 (1.43–8.66) | 0.006 |
aAdjusted for age, sex, and Rohrer’s index
bAdjusted for age, sex, Rohrer’s index, frequency of snoring, and weekday sleep duration
cAdjusted for age and Rohrer’s index
dAdjusted for age, Rohrer’s index, frequency of snoring, and weekday sleep duration
Association between unrefreshing sleep in the morning and constipation
Table 3 shows the sex-specific prevalence of constipation and ORs (95% CI) in children according to the frequency of unrefreshing sleep. A higher prevalence of unrefreshing sleep in the morning was associated with a higher prevalence of constipation. The multivariate-adjusted OR (95% CI) of constipation type I and type II for children who reported unrefreshing sleep three or more nights per week were 1.48 (95% CI 1.03–2.42; p = 0.05) and 2.19 (95% CI 1.26–3.84; p = 0.018) when compared to those children with refreshing sleep. A similar association was observed in girls (Table 3).
Table 3.
Odds ratios (95% confidence interval) for constipation according to the weekly frequency of unrefreshing sleep
| Weekly frequency of unrefreshing sleep | p for trend | |||
|---|---|---|---|---|
| Never | Once or twice | Three or more times | ||
| All | 251 | 174 | 204 | |
| Constipation type I, n (%) | 59 (23.5) | 45 (25.9) | 65 (31.9) | |
| Univariate model | 1.00 | 1.14 (0.73–1.78) | 1.52 (1.01–2.30) | 0.06 |
| Multivariate model 1a | 1.00 | 1.11 (0.70–1.74) | 1.48 (0.98–2.25) | 0.06 |
| Multivariate model 2b | 1.00 | 1.15 (0.73–1.81) | 1.48 (1.03–2.42) | 0.03 |
| Constipation type II, n (%) | 24 (9.6) | 27 (15.5) | 40 (19.6) | |
| Univariate model | 1.00 | 1.74 (0.97–3.13) | 2.31 (1.34–3.98) | 0.003 |
| Multivariate model 1a | 1.00 | 1.60 (0.89–2.91) | 2.18 (1.26–3.81) | 0.007 |
| Multivariate model 2b | 1.00 | 1.59 (0.87–2.91) | 2.19 (1.26–3.84) | 0.008 |
| Boys | 144 | 86 | 99 | |
| Constipation type I, n (%) | 34 (23.6) | 16 (18.6) | 26 (26.3) | |
| Univariate model | 1.00 | 0.74 (0.38–1.44) | 1.15 (0.64–2.08) | 0.55 |
| Multivariate model 3c | 1.00 | 0.73 (0.37–1.42) | 1.16 (0.64–2.11) | 0.54 |
| Multivariate model 4d | 1.00 | 0.78 (0.40–1.54) | 1.29 (0.70–2.11) | 0.31 |
| Constipation type II, n (%) | 10 (6.9) | 7 (8.1) | 12 (12.1) | |
| Univariate model | 1.00 | 1.19 (0.44–3.24) | 1.85 (0.77–4.46) | 0.16 |
| Multivariate model 3c | 1.00 | 1.21 (0.44–3.31) | 1.83 (0.75–4.43) | 0.17 |
| Multivariate model 4d | 1.00 | 1.08 (0.39–3.00) | 1.65 (0.67–4.08) | 0.26 |
| Girls | 107 | 88 | 105 | |
| Constipation type I, n (%) | 25 (23.4) | 29 (33.0) | 39 (37.1) | |
| Univariate model | 1.00 | 1.61 (0.86–3.03) | 1.94 (1.07–3.52) | 0.04 |
| Multivariate model 3c | 1.00 | 1.59 (0.84–3.02) | 2.04 (1.19–3.74) | 0.03 |
| Multivariate model 4d | 1.00 | 1.62 (0.85–3.10) | 2.13 (1.15–3.93) | 0.02 |
| Constipation type II, n (%) | 14 (13.1) | 20 (22.7) | 28 (26.7) | |
| Univariate model | 1.00 | 1.95 (0.92–4.14) | 2.42 (1.19–4.91) | 0.02 |
| Multivariate model 3c | 1.00 | 1.88 (0.88–4.01) | 2.48 (1.21–5.06) | 0.02 |
| Multivariate model 4d | 1.00 | 1.94 (0.91–4.16) | 2.53 (1.23–5.19) | 0.02 |
aAdjusted for age, sex, and Rohrer’s index
bAdjusted for age, sex, Rohrer’s index, frequency of snoring, and weekday sleep duration
cAdjusted for age and Rohrer’s index
dAdjusted for age, Rohrer’s index, frequency of snoring, and weekday sleep duration
Association between tiredness and constipation
Table 4 shows the sex-specific prevalence of constipation and ORs (95% CI) in children according to their reported frequency of tiredness, whereby a higher prevalence of tiredness was associated with a higher prevalence of constipation type II (Fig. 1).
Table 4.
Odds ratios (95% confidence interval) for constipation according to weekly frequency of tiredness
| Weekly frequency of tiredness | p for trend | ||||
|---|---|---|---|---|---|
| Never | Once or twice | Three or more times | |||
| All | 350 | 245 | 34 | ||
| Constipation type I, n (%) | 95 (15.1) | 61 (9.7) | 13 (2.1) | ||
| Univariate model | 1.00 | 0.89 (0.61–1.29) | 1.66 (0.80–3.45) | 0.38 | |
| Multivariate model 1a | 1.00 | 0.90 (0.62–1.31) | 1.51 (0.72–3.17) | 0.48 | |
| Multivariate model 2b | 1.00 | 0.95 (0.64–1.40) | 1.64 (0.77–3.49) | 0.31 | |
| Constipation type II, n (%) | 44 (12.6) | 34 (13.9) | 13 (38.2) | ||
| Univariate model | 1.00 | 1.12 (0.69–1.81) | 4.31 (2.01–9.21) | < 0.0001 | |
| Multivariate model 1a | 1.00 | 1.20 (0.73–1.96) | 3.73 (1.69–8.12) | < 0.0001 | |
| Multivariate model 2b | 1.00 | 1.20 (0.79–1.98) | 3.81 (1.72–8.45) | < 0.0001 | |
| Boys | 179 | 139 | 11 | ||
| Constipation type I, n (%) | 39 (11.9) | 34 (10.3) | 3 (0.9) | ||
| Univariate model | 1.00 | 1.16 (0.69–1.97) | 1.35 (0.34–5.32) | 0.53 | |
| Multivariate model 3c | 1.00 | 1.22 (0.72–2.08) | 1.44 (0.36–5.81) | 0.44 | |
| Multivariate model 4d | 1.00 | 1.35 (0.77–2.36) | 1.61 (0.39–6.68) | 0.31 | |
| Constipation type II, n (%) | 14 (7.8) | 13 (9.4) | 2 (18.2) | ||
| Univariate model | 1.00 | 1.22 (0.55–2.68) | 2.62 (0.52–13.3) | 0.26 | |
| Multivariate model 3c | 1.00 | 1.25 (0.56–2.78) | 2.69 (0.49–13.2) | 0.26 | |
| Multivariate model 4d | 1.00 | 1.04 (0.46–2.37) | 2.06 (0.38–11.2) | 0.45 | |
| Girls | 171 | 106 | 23 | ||
| Constipation type I, n (%) | 56 (18.7) | 27 (9.0) | 10 (3.3) | ||
| Univariate model | 1.00 | 0.70 (0.41–1.21) | 1.58 (0.65–3.83) | 0.61 | |
| Multivariate model 3c | 1.00 | 0.67 (0.38–1.17) | 1.41 (0.57–3.46) | 0.79 | |
| Multivariate model 4d | 1.00 | 0.69 (0.39–1.21) | 1.54 (0.61–3.85) | 0.65 | |
| Constipation type II, n (%) | 30 | (17.5) | 21 (19.8) | 11 (47.8) | |
| Univariate model | 1.00 | 1.16 (0.63–2.16) | 4.31 (1.74–10.7) | 0.002 | |
| Multivariate model 3c | 1.00 | 1.19 (0.63–2.23) | 4.21 (1.67–10.6) | 0.002 | |
| Multivariate model 4d | 1.00 | 1.24 (0.66–2.33) | 4.61 (1.80–11.8) | 0.002 | |
aAdjusted for age, sex, and Rohrer’s index
bAdjusted for age, sex, Rohrer’s index, frequency of snoring, and weekday sleep duration
cAdjusted for age and Rohrer’s index
dAdjusted for age, Rohrer’s index, frequency of snoring, and weekday sleep duration
Fig. 1.
Participant flow diagram
The multivariate-adjusted odds ratio of constipation type II for children who reported tiredness three or more nights per week was 3.81 (95%CI: 1.72–8.43; p < 0.001), compared to those without tiredness. A similar association was observed in girls (Table 4).
Association between constipation and other sleep-related factors
Table 5 shows that children with constipation type II were more likely to have insufficient sleep and tiredness. Furthermore, those children with constipation were more likely to have later bedtimes (later than 22:00) and later wake-up times (later than 7:00) during schooldays (Supplementary Table 2).
Table 5.
Odds ratios (95% confidence interval) for sleep insufficiency according to constipation
| Total | Constipation type I | p-value | Constipation type II | p-value | ||||
|---|---|---|---|---|---|---|---|---|
| Normal | Constipation | Normal | Constipation | |||||
| 629 | 460 | 169 | 538 | 91 | ||||
| Insufficient sleep, n (%) | 64 (10.1) | 45 (9.7) | 19 (11.2) | 47 (8.7) | 17 (18.7) | |||
| Univariate model | Ref | 1.18 (0.66–2.08) | 0.57 | Ref | 2.42 (1.32–4.43) | 0.003 | ||
| Multivariate model 1a | Ref | 1.18 (0.67–2.10) | 0.57 | Ref | 2.73 (1.45–5.13) | 0.003 | ||
| Multivariate model 2b | Ref | 1.29 (0.71–2.32) | 0.40 | Ref | 2.86 (1.50–5.44) | 0.001 | ||
| Weekly frequency of unrefreshing sleep, n (%) | 77 (12.2) | 56 (12.1) | 21 (12.4) | 63 (11.6) | 14 (18.2) | |||
| Univariate model | Ref | 1.03 (0.60–1.75) | 0.92 | Ref | 1.37 (0.73–2.55) | 0.33 | ||
| Multivariate model 1a | Ref | 1.10 (0.64–1.89) | 0.74 | Ref | 1.53 (0.80–2.93) | 0.20 | ||
| Multivariate model 2b | Ref | 1.66 (0.91–3.03) | 0.10 | Ref | 1.56 (0.76–3.19) | 0.23 | ||
| Weekly frequency of tiredness, n (%) | 34 (5.4) | 21 | (4.5) | 13 (7.6) | 21 (3.9) | 13 (14.1) | ||
| Univariate model | Ref | 1.74 (0.85–3.56) | 0.13 | Ref | 4.10 (1.97–8.51) | < 0.0001 | ||
| Multivariate model 1a | Ref | 1.56 (0.76–3.24) | 0.23 | Ref | 3.45 (1.63–7.31) | 0.001 | ||
| Multivariate model 2b | Ref | 1.71 (0.82–3.61) | 0.15 | Ref | 3.49 (1.63–7.46) | 0.001 | ||
a Adjusted for age, sex, and Rohrer’s index; b Adjusted for age, sex, Rohrer’s index, frequency of snoring, and weekday sleep duration
Table 6 shows the prevalence of constipation and ORs (95% CI) in children according to their sleep sufficiency after stratification for wake-up time. The multivariate-adjusted OR (95% CI) of constipation type II for the children with earlier bed times before 11 pm on schooldays with insufficient sleep were 3.34 (1.51–7.39) and 1.94 (0.68–5.54), and that for early wake-up times before 7:00, respectively.
Table 6.
Odds ratios (95% confidence interval) for constipation according to sleep insufficiency
| Sufficient sleep | Insufficient sleep | p-value | |
|---|---|---|---|
| Weekday bedtime < 22:00 | 476 | 38 | |
| Constipation type I, n (%) | 123 (25.8) | 10 (26.3) | 0.95 |
| Univariate model | Ref | 1.03 (0.48–2.17) | 0.95 |
| Multivariate model 1a | Ref | 1.05 (0.49–2.23) | 0.91 |
| Multivariate model 2b | Ref | 1.09 (0.51–2.35) | 0.82 |
| Constipation type II, n (%) | 57 (12.0) | 11 (29.0) | 0.002 |
| Univariate model | Ref | 3.00 (1.41–6.36) | 0.004 |
| Multivariate model 1a | Ref | 3.37 (1.52–7.44) | 0.003 |
| Multivariate model 2b | Ref | 3.34 (1.51–7.39) | 0.003 |
| Weekday bedtime ≥ 22:00 | 92 | 26 | |
| Constipation type I, n (%) | 27 (29.4) | 9 (34.6) | 0.61 |
| Univariate model | Ref | 1.28 (0.51–3.21) | 0.61 |
| Multivariate model 1a | Ref | 1.25 (0.48–3.22) | 0.65 |
| Multivariate model 2b | Ref | 1.26 (0.48–3.33) | 0.64 |
| Constipation type II, n (%) | 17 (18.5) | 6 (23.1) | 0.61 |
| Univariate model | Ref | 1.32 (0.46–3.80) | 0.60 |
| Multivariate model 1a | Ref | 1.63 (0.53–4.98) | 0.39 |
| Multivariate model 2b | Ref | 1.60 (0.51–5.06) | 0.42 |
| Weekday wake-up time < 7:00 | 388 | 38 | |
| Constipation type I, n (%) | 94 (24.2) | 10 (26.3) | 0.78 |
| Univariate model | Ref | 1.18 (0.50–2.82) | 0.70 |
| Multivariate model 1a | Ref | 1.27 (0.50–3.19) | 0.62 |
| Multivariate model 2b | Ref | 1.13 (0.52–2.45) | 0.76 |
| Constipation type II, n (%) | 42 (10.8) | 10 (26.3) | 0.005 |
| Univariate model | Ref | 2.94 (1.34–6.48) | 0.007 |
| Multivariate model 1a | Ref | 2.92 (1.28–6.65) | 0.01 |
| Multivariate model 2b | Ref | 2.84 (1.24–6.50) | 0.01 |
| Weekday wake-up time ≥ 7:00 | 178 | 26 | |
| Constipation type I, n (%) | 55 (30.9) | 9 (34.6) | 0.70 |
| Univariate model | Ref | 1.12 (0.52–2.39) | 0.77 |
| Multivariate model 1a | Ref | 1.10 (0.51–2.35) | 0.82 |
| Multivariate model 2b | Ref | 1.20 (0.47–3.09) | 0.70 |
| Constipation type II, n (%) | 32 (18.0) | 7 (26.9) | 0.28 |
| Univariate model | Ref | 1.68 (0.65–4.34) | 0.28 |
| Multivariate model 1a | Ref | 2.13 (0.77–5.90) | 0.15 |
| Multivariate model 2b | Ref | 1.94 (0.68–5.54) | 0.21 |
aAdjusted for age, sex, and Rohrer’s index
bAdjusted for age, sex, Rohrer’s index, frequency of snoring, and weekday sleep duration
Discussion
Summary of the data
In the present study, insufficient sleep, unrefreshing sleep, and tiredness were associated with constipation. The stratified analysis by sex showed that this association was preferentially observed in girls who also manifested a significantly higher prevalence of both types of constipation, while the association by wake-up time was exclusively observed in those who woke up before 7 am, and not among those who woke up at 7 am or later. In addition, those children who woke up at 7 am or later were more likely to denote constipation than those waking up before 7 am (p = 0.005), thereby supporting previous observations that those rushing to leave in the morning are more likely to suffer from constipation [11]. The results of the present study in children corroborate previous findings in adults [10, 11]. This was further confirmed by our findings on those well-sleeping "early-bird" children who went to bed early (i.e., before 22:00 pm) and woke up before 7:00 am. Indeed, these children are less likely to suffer from constipation type II (Fig. 2).
Fig. 2.
Venn diagram between constipation and insufficient sleep
The presence of constipation was significantly associated with insufficient sleep, the frequency of unrefreshing sleep, and the frequency of daytime tiredness in girls but not in boys. The higher prevalence of constipation has been previously noted in both girls and women of all ages [13]. Although insufficient sleep, frequent unrefreshing sleep, and tiredness tended to increase the prevalence of constipation in boys, the association failed to achieve statistical significance. We posit that the differences in the prevalence of constipation between boys and girls may be accounted for by some possible underlying factors that exhibit sex dimorphism. Indeed, colonic transit is faster in males than in females [14], and perhaps this physiological difference may partly contribute to the higher prevalence of defecatory disorders and constipation in females [15]. The female sex hormonal effects elevate the prevalence of constipation in girls [16], which will make their association more remarkable than in boys.
Insufficient sleep is associated with hard stool (type II constipation), rather than with infrequent bowel movements (Type I, Tables 2, 3, 5). There may be several reasons for the disparity between type I and type II constipation. First, a harder stool may be associated with a lack of water in fecal material and therefore impairment in the anorectal nervous system, such as reduced "sensation" and "urge", both of which are associated with sleep disorders [17]. Second, infrequent bowel movements are more likely associated with withholding behaviours [18]. There are 6 domains of paediatric sleep health, so-called RU-SATED, which include Regularity, Satisfaction, Alertness, Timing, Efficiency, and Duration. Therefore, not only sleep apnea (alertness) and sleep duration, but also other factors of RU-SATED may affect the association, such as social jet lag, lifestyle issues, and increased screen time.
Although the potential mechanisms underlying idiopathic constipation are not well established, decreased propulsive activity may be an important contributory factor [19]. Since such propulsive activity exhibits a prominent circadian pattern in all people irrespective of sex or age, it is possible that differences in constipation prevalence between sexes may reflect, among other factors, differences in the effect of sleep on propulsive and defecatory activity as a function of circadian clock alignment and as a result of optimal or sub-optimal sleep structure. Indeed, it is well established that sleep exerts a profound effect on gastrointestinal motility [20]. In light of the intrinsically reduced motility among females [21], it is possible that these two elements, namely a propensity for constipation and susceptibility to sleep perturbations will coincide to generate a more profound effect in a priori vulnerable children, particularly girls.
Several studies have indicated a bidirectional association between obstructive sleep apnoea syndrome and alterations in the gut microbiome in animal models and humans [11]. It is possible that the aforementioned differences in gastrointestinal transit times between girls and boys and the superimposition of the effect of sleep on the gut microbiota will result in relative gut dysbiosis in vulnerable children, particularly girls. It is well documented that dysbiosis of the gut does not only contribute to functional constipation but also psychological and behavioral changes. Conversely, gut dysbiosis has also been implicated in the emergence of disrupted sleep architecture and altered overall sleep patterning [22]. Indeed, nascent literature over the last decade has indicated that the diversity and abundance of specific microorganisms in the intestinal microbiome modified is by the presence of sleep disorders such as in mouse models of sleep apnoea [23] and in humans with sleep disorders [24]. This is probably reflective of the fact that sleep disorders affect the microbiota-gut-brain axis and may disrupt the homeostatic characteristics of the various bowel functions [11]. In recent years, the link between sleep disorders such as sleep apnea and changes in gut microbiome has also emerged in children [25], suggesting that alterations in the microorganisms in the gut elicited by disrupted sleep may also manifest as functional perturbations in the bowel, e.g., constipation. Thus, the link between sleep and constipation may be alternatively explained by the microbiota-gut-brain axis, in which tryptophan and its metabolite, 5-HT, play key roles in both sleep and gut motility [26].
Constipation in children impairs their quality of life as well as that of their parents. This observation is also clearly documented when sleep problems are present [27] and the additive or synergistic effects of these two issues cannot be overlooked. Taken together, the present study indicates that poor sleep and constipation are likely to co-exist and potentially affect each other. Thus, improving sleep quality and quantity may be worth pursuing to prevent the worsening of constipation in susceptible children, particularly in girls.
Implications for public health
Constipation is a common occurrence in school children and adversely affects health-related quality of life while also increasing school absenteeism [7]. Importantly, constipation may persist into adulthood [8], and may not only involve the intestinal tract but can also be associated with other diseases, such as cardiovascular and cerebrovascular diseases, asthma, and mental disorders [28]. Constipation also imposes a financial burden related to the high costs of healthcare; the number of children hospitalized due to constipation in the USA increased by 112% from 1997 to 2009, and the costs associated with hospitalization increased by 221.5% [28].
A previously published study showed that insufficient sleep was associated with nocturnal enuresis, whilst insufficient sleep in the present study was not associated with actual sleep duration, nor with nocturnal enuresis, restless behaviors, fidgety behaviors, and poor concentration in school. Furthermore, since sleep disorders similarly impose a heightened economic burden and reduction in quality of life [27], the association and overlap between these two conditions suggest the possibility that improving sleep issues in children may reduce the severity or present altogether the occurrence of constipation in a significant subset of children, particularly girls.
Strengths
The strength of our study is its large sample size, and, therefore, stratification with sex was possible.
Limitations
The present study has several limitations. First, the information was extracted based on parent-reported questionnaires, and, therefore, the responses may reflect personal bias. Defecation frequency and stool characteristics were not assessed by medical professionals and therefore such reports may not be accurate. Furthermore, the definition of constipation might be affected by the sociocultural elements and therefore include a larger proportion of the community than in other cohorts in which Rome IV criteria were used. However, we should point out that the prevalence of constipation in the present study was similar to those found in other surveys using a parent-reported questionnaire [13, 29, 30].
Second, cross-sectional approach of the present study precludes in causality inferences. Third, the information about dietary habits, physical activity and obesity are known as traditional risk factors for constipation [31], although the data in the present study were adjusted exclusively for Rohrer's index, and despite such adjustment, we found that the association between insufficient sleep and constipation remained statistically significant. Finally, as mentioned above there could be a reporter bias, because parents whose children suffer from sleep-related problems or constipation will tend to be concerned about their somatic manifestations. However, the questionnaire response rate was elevated (70.8%) and the anthropometric characteristics and sleep duration of participants were similar to those who were excluded from analysis due to incomplete data, and, furthermore, no significant statistical differences emerged between the current study and other previous nationwide surveys [30].
Conclusions
Sleep disorders and constipation are highly prevalent among Japanese elementary school children. Furthermore, those children with insufficient sleep are more likely to suffer from constipation with girls being particularly vulnerable to this association. We propose that interventions aiming to improve sleep quality and quantity may reduce the prevalence of constipation in childhood and improve the overall outcomes of this frequent and often chronic condition.
Acknowledgements
We gratefully acknowledge the children who participated in the survey, their parents, and the members of the educational committee in Higashiyamato City who took part in this study. We also gratefully acknowledge the work of past and present members of our research department.
Author contributions
Ritsuko Furuya conceptualized and designed the study, drafted the manuscript, reviewed and critically revised the manuscript for important intellectual content, collected data, and contributed to data analysis and interpretation. Hiroo Wada supervised data collection of the study, contributed to data interpretation, and critically revised the manuscript for important intellectual content. Keisuke Onuki, Takayuki Kitazawa, Mariko Miyakawa, Qinye Zhua, Yuito Ueda, and Setsuko Sato made a substantial contribution to the explanation and informed consent of participants, data collection, and analysis and interpretation. Hiroshi Nakano contributed to data interpretation and critically revised the manuscript for important intellectual content. David Gozal contributed to the interpretation of the data and made critical revisions to the manuscript for important intellectual content. Takeshi Tanigawa acquired funding, conceptualized and designed the study, critically revised the manuscript for important intellectual content, and gave final approval of the version to be published. All authors read and approved the final manuscript as submitted and agree to be accountable for all aspects of the work.
Funding
This study was supported by a Ministry of Education, Culture, Sports, Science, and Technology/Japan Society for the Promotion of Science (MEXT/JSPS) Grant-in-Aid for Scientific Research (KAKENHI; Grant Number 17K19928), JSPS Grant-in-Aid for Scientific Research (KAKENHI; Grant Number JP22H00496), Research Grant on Policy Planning and Evaluation (No.20IA2004) from the Ministry of Health, Labour and Welfare, Japan, and a research grant from Juntendo University (Tokyo, Japan).
Declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The participating children and their parents completed informed assent and consent forms before participation. This study was approved by the Ethical Review Board of the Hospital Ethics Committee Juntendo University Hospital (authorization number: 18-032). All procedures performed in studies involving human participants were conducted in accordance with ethical standards and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Ethical standards
The manuscript does not contain clinical studies or patient data.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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