Importance of sleep quality in functional abdominal pain disorder in pediatric patients

Abstract

The incidence of sleep problems is increasing in children, and they are thought to contribute to pain in functional abdominal pain disorder (FAPD). In this study, we aimed to evaluate the pattern of sleep disturbance in children with FAPD and identify the associated factors. We retrospectively analyzed patients aged 12–18 years who were diagnosed with FAPD based on the Rome IV criteria. To assess sleep problems, we used the Korean version of the Pittsburgh Sleep Quality Index (PSQI-K). To evaluate factors associated with sleep disturbances, we used the odds ratios (OR) estimated in logistic regression models. Among the 66 patients evaluated, 57.6% (38/66) had a total PSQI-K score > 5, indicating a significant disturbance in sleep, 52.6% (20/38) had irritable bowel syndrome (IBS), and 47.4% (18/38) had functional abdominal pain-not otherwise specified. The mean PSQI-K score was 7.2 ± 6.0, and longer sleep onset latency was noted (26.33 ± 19.44 min) in all patients than healthy controls. Almost all PSQI-K subscales scores were elevated in patients with IBS. In univariate analysis, abdominal pain score > 7 and IBS were associated with poor sleep quality. In multivariate analysis, only IBS was associated with sleep disturbance. A relatively large proportion of patients with FAPD had sleep problems and these were more common in patients with IBS. Thus, interventions for improving sleep quality should also be considered in patients with FAPD with severe abdominal pain and IBS.

Introduction

Childhood functional abdominal pain disorder (FAPD) is a common disorder characterized by intermittent abdominal pain with combined bowel movement change and bloating. It is diagnosed after the exclusion of other medical conditions, following appropriate evaluation. Based on the revised Rome IV criteria, FAPD cases can be divided into functional dyspepsia, irritable bowel syndrome (IBS), abdominal migraine, and functional abdominal pain-not otherwise specified (FAP-NOS) [1, 2].

The etiology of FAPD is multifactorial; changes in visceral sensation, altered gastrointestinal motility, microbial dysbiosis, and altered brain–gut axis are factors related to symptoms onset [3]. Psychological distress, such as stress, anxiety, and depression, may have an effect on pain by altering gut motility and increasing gut nerve sensitivity and permeability [4]. Children with FAPD experience higher rates of psychological stress than the healthy population [5]. Thus, understanding the interactions between psychological factors and gut physiology are important in assessing and treating FAPD [6].

Sleep problems are becoming increasingly common and are a major contributing factor for persistent pain in children with FAPD; sleep problems are also more prevalent in children with FAPD than in healthy children [7]. Inadequate sleep or sleep disturbances, such as difficulty initiating and maintaining sleep, poor sleep quality, and daytime somnolence, can negatively affect daily function in a variety of ways [8–10]. Poor sleep quality with disrupted sleep can cause low school achievement and higher levels of emotional problems, such as anxiety and depression [11].

Among patients with FAPD, those with IBS are more commonly affected by sleep disturbances and severe abdominal and somatic pain [12]. However, studies on sleep problems in children with FAPD are limited.

Thus, in this study, we aimed to evaluate the pattern of sleep disturbance and identify the factors related to sleep disturbances in children with FAPD, which might present new treatment options for FAPD.

Materials and methods

Study population

We retrospectively analyzed patients aged 12–18 years and diagnosed with FAPD between January 2019 and March 2020. All included patients had at least 2 months of abdominal pain, at least four times per month, before diagnosis. Among them, patients with organic gastrointestinal disease, significant chronic illness, or a history of abdominal surgery were excluded. FAPD was defined according to the symptom-based revised Rome IV criteria and was divided into subtypes for IBS and, FAP-NOS [13]. In the outpatient clinic, we used a questionnaire for abdominal pain that obtained information such as abdominal pain duration, location, and intensity. The intensity of abdominal pain was rated on an 11-point scale ranging from no pain (0) to the most pain (10) [14]. A pain score of > 7 was interpreted as severe pain [15].

Sleep quality assessment (Pittsburgh Sleep Quality Index)

All patients underwent a self or parent-reported questionnaire that included seven components about sleep and daytime function to assess sleep problems. The Pittsburgh Sleep Quality Index (PSQI) consists of sleep habits (usual sleep duration, sleep onset latency, and time awake after sleep onset), and general questions regarding the frequency of symptoms of sleep disorders (e.g., sleep resistance, waking); we used the Korean version of the PSQI (PSQI-K), which is a validated method for evaluating sleep quality [16]. Each item is scored from 0 to 3, and the total score of the seven components is referred to as the global PSQI score, which ranges from 0 to 21. Patients who scored > 5 points were categorized as having sleep disturbance” [17].

Statistical analysis

Continuous data were expressed as medians or means (± standard deviation) and interquartile ranges. These data were compared using Mann–Whitney U test or Student’s t test. Discrete data were expressed as numbers and percentages and were compared using Fisher’s exact or chi-square tests. To evaluate the factors associated with sleep disturbances, we used the odds ratio (OR) calculated in logistic regression models. Variables, such as sex, age, subtypes of FAPD, and intensity and duration of abdominal pain, were used in the analysis. A p < 0.05 was considered significant. Statistical analyses were performed using SPSS ver. 24.0 (IBM, Chicago, IL, USA).

This retrospective analysis was approved by the Institutional Review Board of Chungnam National University Hospital and conducted in accordance with the Declaration of Helsinki. Informed consents were waived due to the retrospective nature of the study.

Results

Table 1 shows the baseline characteristics of all patients. A total of 66 patients were included in this study. The median age of the patients was 15.5 ± 3.9 years and the male-to-female ratio was 0.8:1. Their mean PSQI-K score was 7.2 ± 6.0, and 57.6% (38/66) of the patients had a total PSQI-K score > 5, indicating a significant disturbance in sleep; 71.4% (20/28) in IBS and 47.4% (18/38) in FAP-NOS. Patients with IBS had higher PSQI-K scores than those with FAP-NOS, but the difference was not statistically significant.

Table 1.

Baseline characteristics of patients with FAPD

Variable	Total N = 66	IBS N = 28	FAP-NOS N = 38	p value	Cohen’s d
Male	30 (45.5)	12 (42.9)	18 (47.4)	0.539	0.10
Age (years)	13.39 ± 1.34	14.14 ± 1.56	12.84 ± 0.83	0.153	0.05
Severity of symptom	4.79 ± 1.21	5.29 ± 1.26	4.42 ± 1.07	0.042	0.65
Duration of symptom (months)	36.64 ± 47.7	52.43 ± 56.04	25 ± 37.94	0.103	0.13
Presence of sleep disturbances (PSQI-K score > 5)	38 (57.6)	20 (71.4)	18 (47.4)	0.034	0.52
PSQI-K scoring	7.2 ± 6.0	9.0 ± 6.2	6.0 ± 5.6	0.159	0.23

Values are presented as either frequency (percentage) or the mean ± standard deviation

FAPD functional abdominal pain disorder, IBS irritable bowel syndrome, FAP-NOS functional abdominal pain-not otherwise specified, PSQI-K Pittsburgh Sleep Quality Index-Korea

Table 2 shows the distributions of subscales scores of the PSQI-K. The average sleep duration was 8.5 ± 1.60 h in all patients. Patients with IBS had significantly shorter sleep duration (6.85 ± 1.77 h) than those with FAP-NOS (9.05 ± 1.11 h). The median sleep onset latency was 26.33 ± 19.44 min in all patients. The scores of almost all components were elevated in IBS patients than FAP-NOS, indicating poor sleep quality in these group. Statistically significant differences were observed in two components; self-reported sleep quality rate and trouble staying awake.

Table 2.

Detailed subscale results of the PSQI-K in patients with FAPD

Variable	Total N = 66	IBS N = 28	FAP-NOS N = 38	p value	Cohen’s d
Average hours slept	8.50 ± 1.60	6.85 ± 1.77	9.05 ± 1.11	0.005	0.70
Sleep onset latency (min)	26.33 ± 19.44	22.14 ± 20.38	26.58 ± 20.88	0.768	0.23
Cannot get to sleep within 30 min	0.85 ± 1.25	1.07 ± 1.38	0.88 ± 1.15	0.389	0.15
Wake up in the middle of the night or early morning	1.0 ± 1.11	1.07 ± 1.14	0.94 ± 1.13	0.758	0.11
Have to get up to use the bathroom	0.64 ± 0.82	0.79 ± 0.80	0.52 ± 0.84	0.376	0.03
Cannot breathe comfortably	0.36 ± 0.78	0.36 ± 0.74	0.37 ± 0.83	0.968	0.11
Cough or snore loudly	0.58 ± 0.96	0.36 ± 0.84	0.74 ± 1.04	0.273	0.05
Feel too cold	0.33 ± 0.77	0.36 ± 0.74	0.32 ± 0.82	0.881	0.20
Feel too hot	0.24 ± 0.75	0.07 ± 0.26	0.37 ± 0.96	0.211	0.03
Have bad dreams	0.18 ± 0.52	0.29 ± 0.72	0.11 ± 0.32	0.340	0.30
Have pain	1.42 ± 1.5	1.85 ± 1.46	1.10 ± 1.48	0.158	0.10
Overall sleep quality rate (self)	0.30 ± 0.46	0.51 ± 0.51	0.16 ± 0.37	0.035	0.06
Take medicine to sleep	0.09 ± 0.52	0.00 ± 0.00	0.15 ± 0.68	0.399	0.16
Trouble staying awake while in social activity	0.66 ± 1.02	1.14 ± 1.23	0.31 ± 0.67	0.019	0.45

Values are presented as mean ± standard deviation

FAPD functional abdominal pain disorder, IBS irritable bowel syndrome, FAP-NOS functional abdominal pain-not otherwise specified, PSQI-K Pittsburgh Sleep Quality Index-Korea

Table 3 shows the baseline characteristics according to sleep disturbances. Neither age nor sex was associated with sleep disturbances. Patients with sleep disturbances had more severe abdominal pain scores than those without sleep disturbances (6.05 ± 1.02 vs. 4.43 ± 1.39, p = 0.049, Cohen’s d = 0.80). Among the 38 patients with sleep disturbances, 20 were diagnosed with IBS.

Table 3.

Baseline characteristics of patients with FAPD according to the presence of sleep disturbances ((PSQI-K score > 5)

Variable	Sleep disturbance (+) N = 38	Sleep disturbance (−) N = 28	p value	Cohen’s d
Male	18 (47.4	12 (42.9)	0.539	0.10
Age (years)	13,63 ± 1.53	13.07 ± 0.997	0.243	0.15
Severity of symptom	6.05 ± 1.02	4.43 ± 1.39	0.049	0.80
Duration of symptom (months)	28.68 ± 46.51	47.43 ± 48.86	0.271	0.25

Values are presented as either frequency (percentage) or mean ± standard deviation

FAPD functional abdominal pain disorder, PSQI-K Pittsburgh Sleep Quality Index-Korea

Table 4 shows the overall associations between sleep disturbances and variables. In the univariate analysis, pain score > 7 and IBS were associated with poor sleep quality. After adjusting for age and sex, multiple logistic regression was used to assess the association between sleep disturbances and subtype of FAPD, intensity of abdominal pain and only IBS was associated with sleep disturbances.

Table 4.

Univariate and multivariate logistic regression analysis of factors associated with sleep disturbances (PSQI-K score > 5)

Variable	Univariate analysis	p value (R2)	Multivariate analysis	p value (R2)
	OR (95% CI)		OR 95% CI
Severe abdominal pain (pain score > 7)	4.07 (0.854–19.432)	0.047 (0.65)	4.28 (0.79–23.187)	0.078 (0.50)
Duration of symptom (> 8 months)	0.20 (0.043–0.902)	0.173 (0.23
Male	1.20 (0.299–4.917)	0.797 (0.15)
IBS	2.77 (0.640–12.059)	0.039 (0.80)	2.53 (0.790–15.059)	0.048 (0.70)

IBS irritable bowel syndrome, PSQI-K Pittsburgh Sleep Quality Index-Korea, CI confidence interval, OR odds ratio

Discussion

In this study, the median PSQI-K score was 7.2 ± 6.0 in patients with FAPD and this score was higher in patients with IBS. More than half of the patients with FAPD had sleep disturbance.

Sleep is important in conserving energy and restoring the body’s physiological processes, promoting physical growth, and supporting mental development. Sleep problem can cause negative consequences, such as daytime sleepiness, learning difficulties and poor academic performance [18]. Moreover, disturbed or insufficient sleep exacerbates pain, which can be reduced through interventions that improve the sleep environment [19].

According to Owens, approximately 25% of children experience some type of sleep problem during healthy childhood; the prevalence of sleep disorders in children with IBS children is higher, affecting 42.4% of children [20]. A separate study in adults reported that sleep disturbances are more common in patients with IBS and that they correlate with IBS-related pain [21]. Dysregulation of the brain–gut axis plays an important role in both FAPD and sleep disorders. The autonomic nervous system and endocrine factors may mediate abnormal brain-gut interactions in IBS [22]. Thus, IBS was thought to be an associated factor in sleep disturbances. In our study, the percentage of patients with sleep disorder was quite high at 57.6%, and patients with IBS more commonly had sleep disturbances than those with FAP-NOS.

A previous study reported that sleep fragmentation, difficulty falling asleep, and short sleep duration were the common complaint in patients with IBS [23]. Sustained Hypothalamus–pituitary–adrenal axis activation and visceral hyperalgesia might cause frequent arousal and awakening [24, 25]. The average sleep duration was 8.5 ± 1.60 h and sleep onset latency was 26.33 ± 19.44 (min), in our study. Additionally, the sleep duration was shorter, and almost all scores of PSQI-k were higher in patens with IBS than FAP-NOS. There was no difference in sleep disturbances between the sexes. A relatively longer sleep onset latency was seen in the patients than that in the general population of Korean children [26].

Sleep disturbances were correlate with abdominal pain severity. Sleep–pain link has not been fully understood, however, neurobiological and inflammatory mechanisms might be involved in this association [27]. Circadian disturbances also had a causative role in severe GI symptoms in nurses with IBS [28] and sleep deprivation caused enhancing susceptibility to depression or anxiety which results in more severe GI symptoms [29]. These finding show the importance of sleep quality and suggest that as a good predictor of GI symptoms in patients with IBS and FAPD.

Our study had some limitations. First, the sample size was small to allow definitive conclusions to be drawn, and the FAPD subgroups were limited. Second, the retrospective study design may have affected the analysis variables.

In conclusion, a relatively large portion of patients with FAPD had sleep problem, and this was more common in patients with IBS. Thus, interventions for improving sleep quality are additional targets for patients with FAPD with severe abdominal pain, and especially in those with IBS.

Declarations

Conflicts of interest

The funding organization(s) played no role in the study design, collection, analysis, and interpretation of data, writing of the report, or decision to submit the report for publication.

Ethical committee permission

This retrospective analysis was approved by the Institutional Review Board of Chungnam National University Hospital and conducted in accordance with principles of the Declaration of Helsinki.

Research involving human participants and/or animals

None.