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doi:10.1111/jgh.12974
GASTROENTEROLOGY
Irritable bowel syndrome among Japanese adolescents: A nationally representative survey Ryuichiro Yamamoto,* Yoshitaka Kaneita,† Yoneatsu Osaki,‡ Hideyuki Kanda,§ Kenji Suzuki,¶ Susumu Higuchi,** Maki Ikeda,†† Shuji Kondo,†† Takeshi Munezawa‡‡ and Takashi Ohida†† *Division of Clinical Psychology, Health Care and Special Support, Graduate School of Education, Joetsu University of Education, Niigata, † Department of Public Health and Epidemiology, Faculty of Medicine, Oita University, Oita, ‡Division of Environmental and Preventive Medicine, Department of Social Medicine, Faculty of Medicine, Tottori University, Tottori, §Department of Environmental Medicine and Public Health, Faculty of Medicine, Shimane University, Shimane, ¶Suzuki Mental Clinic, **National Hospital Organization Kurihama Medical and Addiction Center, Kanagawa, ††Division of Public Health, Department of Social Medicine, School of Medicine, Nihon University and ‡‡ADVANTAGE Psychology Institute, Tokyo, Japan
Key words cross-sectional survey, irritable bowel syndrome, Japanese adolescent, nationally representative survey. Accepted for publication 23 March 2015. Correspondence Dr Yoshitaka Kaneita, Department of Public Health and Epidemiology, Faculty of Medicine, Oita University, 1-1 Idaigaoka, Hazama-machi, Yufuin City, Oita 879-5593, Japan. Email: [email protected] Declaration of conflict of interest: There is nothing to disclose regarding funding or conflict of interest with respect to this study.
Abstract Background and Aim: No nationally representative survey of irritable bowel syndrome (IBS) among adolescents has ever been performed in Japan. In the present study, we aimed to clarify the prevalence of IBS among Japanese adolescents and the factors associated with it. Methods: The items related to the diagnostic criteria for IBS based on the Rome III Diagnostic Criteria for Functional Gastrointestinal Disorders were included in a crosssectional nationwide survey of “alcohol consumption and smoking habits among junior and senior high school students.” The participating schools were sampled from among all junior and senior high schools in Japan using the cluster-sampling method, and selfadministered questionnaires were sent to the selected schools by mail. Among 99 416 questionnaires that were collected, data from 98 411 valid responses were analyzed. Results: The results showed that the prevalence of IBS was 18.6%. Although no sex difference was observed in the overall prevalence of IBS, the prevalence of diarrheapredominant IBS was higher among boys than among girls, and the prevalence of constipation-predominant IBS was higher among girls than among boys. The prevalence of IBS increased with progression of the school grade, and there were the significant relationships between IBS and sleep-phase delay and insomnia symptoms. IBS was also significantly associated with poor mental health status. Conclusion: These results indicate that IBS is common among junior and senior high school students, and associated with lifestyle and mental health.
Introduction Irritable bowel syndrome (IBS) is a functional disorder characterized mainly by chronic or recurrent abdominal pain or discomfort and disturbances in bowel movements. The reported prevalence rate of IBS is 2–22%, although the figures vary depending on differences in survey subjects, evaluation criteria, and survey procedures.1 Although IBS itself is not a life-threatening condition, it has been reported that its symptoms substantially degrade healthrelated quality of life2 in comparison with other disorders affecting gastrointestinal (GI) function (e.g. gastroesophageal reflux disease) or chronic non-GI diseases (e.g. asthma or migraine). Studies have shown that economic losses caused by IBS, both direct and indirect, are substantial.3 IBS is a pathological condition common among people of all ages,1 but with a high prevalence among adolescents.4 Therefore, to formulate appropriate public 1354
health measures, it is important to clarify the actual prevalence of IBS among adolescents and the factors associated with it. However, few epidemiological studies of IBS have focused on Japanese adolescents. Endo et al. surveyed the prevalence of IBS among junior high school students in Japan and examined the associations between IBS symptoms and health-related quality of life.5 They found that the prevalence rate of IBS among adolescents was 14.6% in 2004 and 19% in 2009, thus showing an increasing trend.5 However, because their study was conducted in a specific region in Japan, and regional differences in the prevalence of IBS have been reported,6 there has been a need for a nationwide survey using a representative sample to accurately determine the prevalence of IBS among Japanese adolescents. In addition, it is important to examine the etiology of IBS and the factors of affected individuals before establishing a public health approach. In the present study, we attempted to clarify the preva-
Journal of Gastroenterology and Hepatology 30 (2015) 1354–1360 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd
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lence of IBS and its associated factors among Japanese adolescents by adding IBS-related items to a questionnaire that had been used previously in cross-sectional nationwide surveys of lifestyle and sleep in adolescents conducted regularly by the Ministry of Health, Labor and Welfare, Japan.
Methods Participants and sampling. We have previously conducted five cross-sectional nationwide surveys (in 1996, 2000, 2004, 2007, and 2008) of “alcohol consumption and smoking habits among junior and senior high school students.”7–13 The present study represents the sixth such survey. For this study, from among the 10 815 junior high schools and 5116 senior high schools registered in Japan as of May 1, 2010,14 131 junior high schools (selection rate: 1.2%) and 113 senior high schools (selection rate: 2.2%) were sampled. Using the stratified single-stage cluster-sampling method, we divided Japan into regional blocks and randomly selected schools from each block. In order to avoid any sampling bias toward specific regional blocks, stratified sampling was performed using the regional blocks as the strata. All of the students enrolled in the sampled schools were the subjects of this study. The sample size was determined by referring to the response rate and confidence intervals (CIs) based on the variance of the results obtained from previous studies.8,9 In the Japanese education system, children enter primary school at the age of 6 years and leave after 6 years of study. They then enter junior high school for 3 years, followed by a further 3 years at senior high school. Primary and junior high school education is compulsory. In this study, the first to third years of junior high school are called the seventh (12 or 13 years old) to ninth grade (14 or15 years old), and the first to third years of senior high school are called the tenth (15 years old or higher) and twelfth grade (17 years old or higher).
Survey procedure. We sent a letter to the principal of each selected school asking for cooperation in our survey, along with the same number of questionnaires and envelopes as the number of students enrolled at the school. At schools that agreed to participate, each class teacher distributed the questionnaires to the students. To protect the privacy of respondents and obtain candid responses, it was clearly stated on the questionnaire that completed questionnaires would not be seen by the teachers. After filling in the anonymous questionnaire, each student was asked to seal it in the envelope provided with an adhesive flap. Collection and delivery of the questionnaires were entrusted to the class teachers, who were instructed to follow the guidelines for conducting the survey. The teachers collected the sealed envelopes and returned them to Nihon University School of Medicine without opening them. The survey period was from October 2010 until the end of December 2010. The survey was approved by the ethics committee of Nihon University School of Medicine.
Measures. The major areas included in the questionnaire were (i) personal data, (ii) lifestyle, (iii) sleep status, (iv) mental health status, (v) frequency of stools, and (vi) symptoms of IBS.
Adolescents irritable bowel syndrome
Personal data. The personal data included, sex, school grade, and type of school (junior high school/senior high school). Lifestyle. The questions related to lifestyle were whether the student ate breakfast and whether he or she participated in extracurricular activities. In addition, to examine smoking and drinking habits, question on how many days the student had smoked (consumed alcoholic beverages) during the previous month was included in the questionnaire. If the response to this question was “1 day or more,” the student was considered a “smoker (alcohol drinker).” Sleep status. The sleep status items included sleep duration, bedtime, subjective sleep assessment, and insomnia symptoms. And each sleep status was defined by reference to the previous studies.11,15 Mental health status. To evaluate the mental health statuses of the respondents, two independent factors (“depression/anxiety” and “loss of positive emotion”) included in the 12-item General Health Questionnaire16–18 were used, and two items that were the highest factor loadings of each factor were selected. Frequency of stools. To evaluate the frequency of stools, a question on the number of times a day the student had defecated on average was included in the questionnaire. A 7-point scale about frequency was used for evaluation. Symptoms of IBS. We prepared questions to evaluate IBS based on the Rome III Diagnostic Criteria for Functional Gastrointestinal Disorders (FGID),19 the definitions that had been used in previous large-scale community-based surveys,20,21 and a previous survey22 of adults conducted in Japan. And we used adult FGID criteria in order to compare the prevalence of this with that of previous Japanese surveys.5,22,23 To examine the presence of abdominal pain or discomfort (prerequisites for IBS), a question on the number of days a month the student had suffered abdominal pain or discomfort in the previous 3 months was included in the questionnaire (possible replies were “never,” “1 day a month,” “2 days a month,” or “3 or more days a month”). If the response was “1 day or more,” the student was instructed to answer the following four questions: (i) “Does your abdominal pain or discomfort ameliorate after defecation? (‘yes’ or ‘no’)”; (ii) “Is the onset of abdominal pain or discomfort associated with a change in stool frequency? (‘increase,’ ‘decrease,’ or ‘no change’)”; (iii) “Is the onset of abdominal pain or discomfort associated with a change in stool form? (‘lumpy or hard stools,’ ‘loose or watery stools,’ ‘repeatedly alternating hard stools and loose stools,’ ‘other form of stools different from usual,’ or ‘no change’)”; and (iv) “Were you diagnosed by a physician as having a common cold or food poisoning that would only temporarily cause abdominal pain or discomfort? (‘yes’ or ‘no’).” A student with IBS was considered to have had abdominal pain or discomfort for at least 3 days a month over the previous 3 months, without a diagnosis of common cold or food poisoning to account for the symptoms (hereafter referred to as “abdominal symptoms due to unknown cause”), and who met at least two of the following three subcategory criteria: abdominal pain or dis-
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Table 1
R Yamamoto et al.
Frequency of stools among Japanese adolescents
Male Junior high school Seventh grade Eighth grade Ninth grade High school Tenth grade Eleventh grade Twelfth grade Total Female Junior high school Seventh grade Eighth grade Ninth grade High school Tenth grade Eleventh grade Twelfth grade Total
< 1T/W (%)
1T/W (%)
1T/4 or 5D (%)
1T/2 or 3D (%)
1T/D (%)
2T/D (%)
> 3T/D (%)
Uncertain (%)
0.8 0.6 1.0
1.5 1.3 0.9
1.7 1.2 1.3
12.1 12.4 11.8
37.1 40.1 41.0
34.3 32.2 32.1
11.3 11.2 10.9
1.4 1.1 1.1
6 435 6 401 6 207
0.5 0.3 0.5 0.6
0.9 0.7 0.9 1.0
1.6 1.2 1.4 1.4
12.3 11.6 11.4 11.9
41.2 40.7 40.7 40.3
32.2 32.5 30.9 32.3
10.3 11.7 13.2 11.4
0.9 1.2 1.1 1.1
10 498 9 965 6 207 48 562
1.8 1.6 1.6
3.0 3.3 3.9
3.5 4.0 3.9
23.3 24.5 26.4
41.4 42.5 43.6
20.6 17.9 15.7
4.6 4.0 3.1
1.9 2.1 1.8
6 606 6 415 6 269
1.7 1.4 1.7 1.6
4.2 4.0 4.1 3.8
5.0 4.4 4.8 4.4
28.8 29.4 28.9 27.4
42.8 42.9 42.1 42.6
13.6 13.7 13.6 15.4
2.8 2.9 3.5 3.4
1.1 1.2 1.2 1.5
10 946 10 203 9 410 49 849
n
Seventh grade = 12 or 13 years old; eighth grade = 13 or 14 years old; ninth grade = 14 or 15 years old; tenth grade = 15 years old or more; eleventh grade = 16 years old or more; twelfth grade = 17 years old or more. D, day; T, time(s); W, week.
comfort (i) improving with defecation, (ii) associated with a change in stool frequency, and (iii) associated with any change in stool form. We classified students with IBS into four subtypes, depending on the change in stool form, by reference to a previous survey.22 Students with IBS who had “lumpy or hard stools” were classified as having IBS with constipation (IBS-C), those with “loose or watery stools” as having IBS with diarrhea (IBS-D), those with “repeatedly alternating hard stools and loose stools” as having IBS mixed type (IBS-M), and those with “other forms of stool different from usual” or “no change” as having untyped IBS (IBS-U). Statistical analysis. First, the responses related to stool frequency were assessed. Next, the prevalence of IBS and that of each IBS subtype was calculated, along with the 95% CI. Then, the sex-based prevalence of IBS was calculated and tabulated into a cross-tabulation table. Finally, multiple logistic regression analyses (step-down method) were performed using binary data from students, with IBS and controls as the explained variables, and personal data, lifestyle factors, sleep status, and mental health status as covariates, in order to describe how many times more likely these covariates among students with IBS are discernible compared with controls. Chi-squared test was also performed to examine differences in each factor of participants by considering the various subtypes of IBS. All analyses were performed using the IBM SPSS Statistics 19 package (Armonk, NY, USA) for Windows.
Results Response rates. Replies were obtained from 89 of the 131 junior high schools (school response rate: 67.9%) and 81 of the 1356
113 senior high schools (school response rate: 71.7%; combined junior and senior high school response rate: 69.7%); 99 416 envelopes were collected. The student response rate as a proportion of enrolled students in the sampled schools was 91.3% for the junior high schools, 92.8% for the senior high schools, and 92.2% as a whole. Accordingly, the overall response rate was 62.1% for the junior high schools, 65.3% for the senior high schools, and 64.0% as a whole. Of the collected questionnaires, 1005 were excluded because the student’s sex or grade was not specified or there were conflicting responses. The data from the remaining 98 411 questionnaires were analyzed.
Frequency of stools. The frequency of stools based on the grade in school and sex is shown in Table 1.
Prevalence of IBS. A total of 17 882 students were considered to have IBS, giving a prevalence of 18.6% (95% CI: 19.2– 17.9%). With regard to IBS subtypes, 2064 students had IBS-C (2.1%; 95% CI: 2.8–1.5%), 9529 had IBS-D (9.9%; 95% CI: 10.5–9.3%), and 2120 had IBS-U (2.2%; 95% CI: 2.8–1.6%). The cross-tabulation based on the grade in school and sex is shown in Table 2.
Exploratory analysis for correlates of IBS. The results of multiple logistic regression analyses are shown in Table 3. All covariates except for sex and early morning awakenings were significantly related to IBS. The results of chi-squared tests are shown in Table 4. There were significant differences among IBS subtypes in sex, drinking
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Table 2
Adolescents irritable bowel syndrome
Prevalence of IBS among Japanese adolescents n
Male Junior high school Seventh grade Eighth grade Ninth grade High school Tenth grade Eleventh grade Twelfth grade Total Female Junior high school Seventh grade Eighth grade Ninth grade High school Tenth grade Eleventh grade Twelfth grade Total
IBS-C (%)
IBS-D (%)
IBS-M (%)
IBS-U (%)
IBS total (%)
6 297 6 285 6 084
0.8 1.1 1.0
6.6 7.9 9.7
1.7 2.1 2.5
1.4 1.7 2.2
10.5 12.9 15.4
10 298 9 767 8 882 47 613
1.3 1.2 1.6 1.2
11.7 13.1 13.9 11.0
3.1 3.6 3.7 2.9
2.6 2.7 3.1 2.4
18.7 20.7 22.3 17.5
6 426 6 281 6 113
1.7 2.3 2.2
5.2 6.9 7.5
2.9 4.1 4.3
1.3 1.2 1.6
11.1 14.5 15.6
10 688 9 945 9 208 48 641
3.1 3.8 4.3 3.1
9.1 10.6 11.5 8.9
6.1 7.1 7.7 5.7
2.3 2.3 2.7 2.0
20.5 23.8 26.2 19.6
Seventh grade = 12 or 13 years old; eighth grade = 13 or 14 years old; ninth grade = 14 or 15 years old; tenth grade = 15 years old or more; eleventh grade = 16 years old or more; twelfth grade = 17 years old or more. For calculation of the prevalence rates, subjects were excluded if a diagnosis could not be determined because of missing responses. IBS, irritable bowel syndrome; IBS total, all types of irritable bowel syndrome; IBS-C, irritable bowel syndrome with constipation; IBS-D, irritable bowel syndrome with diarrhea; IBS-M, irritable bowel syndrome mixed type; IBS-U, untyped irritable bowel syndrome.
alcohol, sleep duration, subjective sleep assessment, difficulty initiating sleep, difficulty maintaining sleep, depression and anxiety, and loss of positive emotion.
Discussion Prevalence of IBS and its subtypes. In this study, the prevalence of IBS among Japanese adolescents was 18.6%. The prevalence identified in this study was similar to that reported in a survey5 of junior high school students in Miyagi Prefecture, which used the Rome II diagnostic criteria (14.6% in 2004 and 19% in 2009). Compared with the Rome II criteria, the use of the Rome III criteria has been reported to produce higher prevalence rate estimations.21,23,24 The prevalence of IBS in this study was also higher than that (13.1%) reported from a nationwide Internet Rome III survey of adults.23 Examination of the prevalence rates of IBS subtypes in the present study indicated that IBS-D had the highest prevalence. This finding was in accord with the results of a crosssectional survey22 that used the Rome III diagnostic criteria and included Japanese workers. Because the prevalence of IBS (particularly IBS-D) among adolescents in Japan thus appears to be very high, appropriate public health measures are urgently needed. Correlates of IBS Relationship between personal data and IBS. There was no difference in the prevalence rate of IBS between the sexes. However, in terms of IBS subtype, the prevalence rates of IBS-C
and IBS-M were higher among girls than among boys, whereas those of IBS-D and IBS-U were higher among boys than among girls. Such differences were also observed in a previous survey22 of Japanese adults, which suggested that constipation tended to be more frequent among women than among men.25 We also observed a linear relationship between grade in school and IBS. In Japan, adolescence might be a period of IBS susceptibility. Relationship between lifestyle and IBS. The present study indicated that the prevalence of IBS among students who never ate breakfast or who ate occasionally was lower than that among those who ate every day. However, the previous study26 suggested that people with IBS had a significantly higher frequency of not eating breakfast than a control group without abdominal symptoms. The gastrocolic reflex associated with intake of breakfast contributes to regularity of metabolic rhythm.27 More details regarding breakfast intake, such as its timing and content, should be investigated in future studies. The prevalence of IBS among smokers was lower than nonsmokers. The results of previous studies on this topic have varied; one study22 reported that the prevalence of IBS among smokers was higher than that among nonsmokers, but others28,29 reported no associations. It was reported that the effects of smoking on colonic transit time differed in individual attributes.30 The effects of smoking in adolescents may differ from those in adults. The effects of smoking on the GI function of adolescents will need to be examined. An association between alcohol consumption and IBS, particularly IBS-M, was suggested. Previous epidemiological studies tar-
Journal of Gastroenterology and Hepatology 30 (2015) 1354–1360 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd
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Table 3
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Exploratory analysis for correlates of irritable bowel syndrome Covariates
Sex Grade in school
Eating breakfast
Extracurricular activity Smoking Drinking alcohol Sleep duration
Bedtime Subjective sleep assessment Difficulty initiating sleep Difficulty maintaining sleep Early morning awakening Depression and anxiety Loss of positive emotion
Adjusted odds ratio Male Female Seventh grade Eighth grade Ninth grade Tenth grade Eleventh grade Twelfth grade Daily Occasionally Never Participating Not participating No Yes No Yes 8h Before 0:00 After 0:00 Good Bad No Yes No Yes No Yes No Yes No Yes
Reference 1.03 Reference 1.20 1.25 1.64 1.87 2.01 Reference 0.86 0.86 Reference 1.11 Reference 0.83 Reference 1.21 0.84 0.98 Reference 0.99 0.95 Reference 1.23 Reference 1.35 Reference 1.16 Reference 1.13 Reference 0.93 Reference 1.62 Reference 1.10
95% confidence interval
P-value
Low
High
1.00
1.07
0.08
1.11 1.16 1.53 1.74 1.87
1.30 1.36 1.76 2.01 2.16
0.00 0.00 0.00 0.00 0.00
0.80 0.80
0.90 0.92
0.00 0.00
1.07
1.15
0.00
0.76
0.91
0.00
1.17 0.80 0.93
1.26 0.89 1.03
0.00 0.00 0.33
0.94 0.89
1.05 1.02
0.83 0.17
1.19
1.29
0.00
1.29
1.40
0.00
1.11
1.22
0.00
1.07
1.19
0.00
0.86
1.00
0.06
1.56
1.68
0.00
1.05
1.16
0.00
The results of the final steps are shown. All variables were entered.
geting adults have produced varying results; one study28 reported no association between alcohol consumption and IBS (subtypes were not examined), whereas another study22 reported an association only with IBS-D. In addition to the direct effects of alcohol on tissues, the process of alcohol metabolism affects the bloodstream, motility, and digestive/absorptive functions of the GI tract.31 Such effects might be observed in the adolescents in this study. It has been suggested that the prevalence of IBS is lower in individuals who sleep less than 5 h per night. However, a previous study found that patients with IBS had significantly shorter sleep duration than those who did not.27 In this study, late bedtime and insomnia symptoms (subjective sleep quality difficulty initiating or maintaining sleep) were related to IBS. It has been reported that GI motility has a circadian rhythm similar to the sleep–wake cycle,32,33 and that there are interactive relations between GI motility and the sleep–wake cycle. Based on these findings, it may be concluded that worsened sleep efficiency because of insomnia 1358
symptoms and the disrupted sleep–wake rhythm, rather than sleep duration, may be associated with IBS. And students with IBS-M experience more insomnia symptoms and go to bed later than those with other phenotypes. The relationships between sleep disturbance and GI motility will need to be investigated. Relationship between mental health status and IBS. The results suggested that depression/anxiety was strongly associated with IBS, along with previous studies. Many studies have reported associations between IBS and mental disorders, particularly mood disorders and anxiety disorders.34,35 In addition, because it has been reported that adolescents with IBS have higher subjective stress levels than those without IBS, management of depression/ anxiety seems to be important.36 And in this study, the constipation symptom was especially related to mental health status. The reason of these result and brain–gut correlation in adolescents will need to be explained.
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Table 4
Adolescents irritable bowel syndrome
Characteristics of the correlates based on the subtypes of IBS
Variables Sex Grade in school
Eating breakfast
Extracurricular activity Smoking Drinking alcohol Sleep duration
Bedtime Subjective sleep assessment Difficulty initiating sleep Difficulty maintaining sleep Early morning awakening Depression and anxiety Loss of positive emotion
Male Female Seventh grade Eighth grade Ninth grade Tenth grade Eleventh grade Twelfth grade Daily Occasional Never No Yes No Yes No Yes 8h Before 0:00 After 0:00 Good Bad No Yes No Yes No Yes No Yes No Yes
IBS-C
IBS-D
‡
†
576 1488† 155 212 195 467 500 535 1739 188 117 739 1297 1977 84 1372 687 395 357 922 226 240 877 1158 1075 962 1681 358 1755 285 1920 123 752‡ 1291† 1696‡ 344†
5218 4311‡ 749 928 1048 2172 2340 2292 7968 856 587 3238 6128 9112 410 6369† 3141‡ 1731 1621 4299 1046 697 4048 5341 4939† 4436‡ 7836† 1550‡ 8265† 1126‡ 8898 507 4134† 5276‡ 8020 1388
IBS-M ‡
1404 2765† 294 391 412 9 74 1057 1041 3475 391 262 1400 2701 4003 163 2626‡ 1533† 805 783† 1845 437 258‡ 1696‡ 2421† 1984‡ 2118† 3287‡ 823† 3499‡ 617† 3854 268 1538‡ 2589† 3466 659
IBS-U †
1131 989‡ 174 186 234 509 494 523 1783 193 128 745 1343 2002 114 1433 682 380 346 949 257 174† 943 1160 1116 978 1738 361 1850 253 1979 123 991† 1115‡ 1811 294
Total
χ2
8 329 9 553 1 372 1 717 1 889 4 122 4 391 4 391 14 965 1 628 1 094 6 122 11 469 17 094 774 11 800 6 043 3 311 3 107 8 015 1 966 1 269 7 564 10 080 9 114 8 494 14 542 3 092 15 369 2 281 16 651 1 021 7 415 10 271 14 993 2 685
863.4
3
0.00
19.5
15
0.19
1.5
6
0.96
3.7
3
0.29
7.5
3
0.06
22.3
3
0.00
22.9
12
0.03
8.3
3
0.04
24.9
3
0.00
24.5
3
0.00
26.4
3
0.00
6.8
3
0.08
97.8
3
0.00
10.2
3
0.02
df
P-value
Seventh grade = 12 or 13 years old; eighth grade = 13 or 14 years old; ninth grade = 14 or 15 years old; tenth grade = 15 years old or more; eleventh grade = 16 years old or more; twelfth grade = 17 years old or more. Haberman residual analyses were performed for variables that were found to be significant with a significance level of 5% in the chi-squared test. † The observed frequency was significantly greater than the expected frequency at the 5% level. ‡ The observed frequency was significantly smaller than the expected frequency at the 5% level. IBS, irritable bowel syndrome; IBS-C, irritable bowel syndrome with constipation; IBS-D, irritable bowel syndrome with diarrhea; IBS-M, irritable bowel syndrome mixed type; IBS-U, untyped irritable bowel syndrome.
Limitation and future direction. To our knowledge, this was the first nationally representative study of IBS among Japanese adolescents. But the items of questionnaire were limited because this survey was performed at a single point in time. Detailed exclusion criteria (e.g. red flags of Rome III, other functional GI disease, or organic GI disease) were not checked. Therefore, the prevalence had potential to be overestimated. And school-related valuables (absenteeism or presenteeism from school, or school examination performance) and consultation behavior also were not assessed. So it is hard to say how much IBS and its related condition leads school maladaptation. And we conducted crosssectional survey and multivariable analysis in this study; these
kinds of methods tend to make the result significant because of large sample size. Based on this study, analytic epidemiological studies or intervention study, which clarifies the detail as pointed above, will be needed. Especially, the significant relationships between delayed sleep-phase, insomnia symptoms, and poor mental health status and IBS were confirmed in this study. In our previous study, students with insomnia symptoms were one in four or five,10,11 and mental health and sleep statuses were related among adolescents.37 From the viewpoint of school health, the effects of health education (e.g. bedtime and insomnia management and stress management) on IBS prevention will need to be examined.
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Acknowledgment This study was supported by a health science research grant from the Ministry of Health, Labor and Welfare of the Japanese Government.
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22
23
24
25
26
27 28
29
30
31 32
33
34
35
36
37
Japanese adolescents and associated sleep statue. Psychiatry Res. 2011; 188: 138–46. Longstreth GF, Thompson G, Chey WD et al. Functional bowel disorders. Gastroenterology 2006; 130: 1480–91. Khoshkrood-Mansoori B, Pourhoseingholi MA, Safaee A et al. Irritable bowel syndrome: a population based study. J. Gastrointestin. Liver Dis. 2009; 18: 413–18. Park DW, Lee OY, Shim SG et al. The differences in prevalence and sociodemographic characteristics of irritable bowel syndrome according to Rome II and Rome III. J. Neurogastroenterol. Motil. 2010; 16: 186–93. Kubo M, Fujiwara Y, Shiba M et al. Differences between risk factors among irritable bowel syndrome subtypes in Japanese adults. J. Neurogastroenterol. Motil. 2011; 23: 249–54. Miwa H. Prevalence of irritable bowel syndrome in Japan: internet survey using Rome III criteria. Patient Prefer. Adherence 2008; 2: 143–7. Sperber AD, Shvartzman P, Friger M et al. A comparative reappraisal of the Rome II and Rome III diagnostic criteria: are we getting closer to the “true” prevalence of irritable bowel syndrome? Eur. J. Gastroenterol. Hepatol. 2007; 19: 441–7. Stewart WF, Liberman JN, Sandler RS et al. Epidemiology of constipation (EPOC) study in the United States: relation of clinical subtypes to sociodemographic features. Am. J. Gastroenterol. 1999; 94: 3530–40. Ono S, Komada Y, Ariga H et al. An epidemiological study of the relationship between bowel habits and sleep health of adult women living in the Tokyo metropolitan area. J. JP Soc. Psychosom. Obstet. Gynecol. 2005; 10: 67–75. (In Japanese with English abstract.) Stokkan KA, Yamazaki S, Tei H et al. Entrainment of circadian clock in the liver by feeding. Science 2001; 291: 490–3. Talley NJ, Zinsmeister AR, Melton LJ 3rd. Irritable bowel syndrome in a community: symptom subgroups, risk factors, and health care utilization. Am. J. Epidemiol. 1995; 142: 76–83. Locke GR 3rd, Zinsmeister AR, Talley NJ et al. Risk factors for irritable bowel syndrome: role of analgesics and food sensitivities. Am. J. Gastroenterol. 2000; 95: 157–65. Meier R, Beglinger C, Dederding JP et al. Influence of age, gender, hormonal status and smoking habits on colonic transit time. Neurogastroenterol. Motil. 1995; 7: 235–8. Bujanda L. The effects of alcohol consumption upon the gastrointestinal tract. Am. J. Gastroenterol. 2000; 95: 3374–82. Goo RJ, Moore JG, Greenberg E et al. Circadian variation in gastric emptying of meals in humans. Gastroenterology 1987; 93: 515–18. Furukawa Y, Cook IJ, Panagopoulos V et al. Relationship between sleep patterns and human colonic patterns. Gastroenterology 1994; 107: 1372–81. Gros DF, Antony MM, McCabe RE et al. Frequency and severity of the symptoms of irritable bowel syndrome across the anxiety disorders and depression. J. Anxiety Disord. 2009; 23: 290–6. Garakani A, Win T, Virk A et al. Comorbidity of irritable bowel syndrome in psychiatric patients: a review. Am. J. Ther. 2003; 10: 61–7. Endo Y. Stress and irritable bowel syndrome in adolescence. Jpn. J. Psychosom. Med. 2010; 50: 733–40. (In Japanese with English abstract.) Kaneita Y, Ohida T, Osaki Y et al. Association between mental health statues and sleep status among adolescents in Japan: a nationwide cross-sectional survey. J. Clin. Psychiatry 2007; 68: 1426–35.
Journal of Gastroenterology and Hepatology 30 (2015) 1354–1360 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd
doi:10.1111/jgh.12974
GASTROENTEROLOGY
Irritable bowel syndrome among Japanese adolescents: A nationally representative survey Ryuichiro Yamamoto,* Yoshitaka Kaneita,† Yoneatsu Osaki,‡ Hideyuki Kanda,§ Kenji Suzuki,¶ Susumu Higuchi,** Maki Ikeda,†† Shuji Kondo,†† Takeshi Munezawa‡‡ and Takashi Ohida†† *Division of Clinical Psychology, Health Care and Special Support, Graduate School of Education, Joetsu University of Education, Niigata, † Department of Public Health and Epidemiology, Faculty of Medicine, Oita University, Oita, ‡Division of Environmental and Preventive Medicine, Department of Social Medicine, Faculty of Medicine, Tottori University, Tottori, §Department of Environmental Medicine and Public Health, Faculty of Medicine, Shimane University, Shimane, ¶Suzuki Mental Clinic, **National Hospital Organization Kurihama Medical and Addiction Center, Kanagawa, ††Division of Public Health, Department of Social Medicine, School of Medicine, Nihon University and ‡‡ADVANTAGE Psychology Institute, Tokyo, Japan
Key words cross-sectional survey, irritable bowel syndrome, Japanese adolescent, nationally representative survey. Accepted for publication 23 March 2015. Correspondence Dr Yoshitaka Kaneita, Department of Public Health and Epidemiology, Faculty of Medicine, Oita University, 1-1 Idaigaoka, Hazama-machi, Yufuin City, Oita 879-5593, Japan. Email: [email protected] Declaration of conflict of interest: There is nothing to disclose regarding funding or conflict of interest with respect to this study.
Abstract Background and Aim: No nationally representative survey of irritable bowel syndrome (IBS) among adolescents has ever been performed in Japan. In the present study, we aimed to clarify the prevalence of IBS among Japanese adolescents and the factors associated with it. Methods: The items related to the diagnostic criteria for IBS based on the Rome III Diagnostic Criteria for Functional Gastrointestinal Disorders were included in a crosssectional nationwide survey of “alcohol consumption and smoking habits among junior and senior high school students.” The participating schools were sampled from among all junior and senior high schools in Japan using the cluster-sampling method, and selfadministered questionnaires were sent to the selected schools by mail. Among 99 416 questionnaires that were collected, data from 98 411 valid responses were analyzed. Results: The results showed that the prevalence of IBS was 18.6%. Although no sex difference was observed in the overall prevalence of IBS, the prevalence of diarrheapredominant IBS was higher among boys than among girls, and the prevalence of constipation-predominant IBS was higher among girls than among boys. The prevalence of IBS increased with progression of the school grade, and there were the significant relationships between IBS and sleep-phase delay and insomnia symptoms. IBS was also significantly associated with poor mental health status. Conclusion: These results indicate that IBS is common among junior and senior high school students, and associated with lifestyle and mental health.
Introduction Irritable bowel syndrome (IBS) is a functional disorder characterized mainly by chronic or recurrent abdominal pain or discomfort and disturbances in bowel movements. The reported prevalence rate of IBS is 2–22%, although the figures vary depending on differences in survey subjects, evaluation criteria, and survey procedures.1 Although IBS itself is not a life-threatening condition, it has been reported that its symptoms substantially degrade healthrelated quality of life2 in comparison with other disorders affecting gastrointestinal (GI) function (e.g. gastroesophageal reflux disease) or chronic non-GI diseases (e.g. asthma or migraine). Studies have shown that economic losses caused by IBS, both direct and indirect, are substantial.3 IBS is a pathological condition common among people of all ages,1 but with a high prevalence among adolescents.4 Therefore, to formulate appropriate public 1354
health measures, it is important to clarify the actual prevalence of IBS among adolescents and the factors associated with it. However, few epidemiological studies of IBS have focused on Japanese adolescents. Endo et al. surveyed the prevalence of IBS among junior high school students in Japan and examined the associations between IBS symptoms and health-related quality of life.5 They found that the prevalence rate of IBS among adolescents was 14.6% in 2004 and 19% in 2009, thus showing an increasing trend.5 However, because their study was conducted in a specific region in Japan, and regional differences in the prevalence of IBS have been reported,6 there has been a need for a nationwide survey using a representative sample to accurately determine the prevalence of IBS among Japanese adolescents. In addition, it is important to examine the etiology of IBS and the factors of affected individuals before establishing a public health approach. In the present study, we attempted to clarify the preva-
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lence of IBS and its associated factors among Japanese adolescents by adding IBS-related items to a questionnaire that had been used previously in cross-sectional nationwide surveys of lifestyle and sleep in adolescents conducted regularly by the Ministry of Health, Labor and Welfare, Japan.
Methods Participants and sampling. We have previously conducted five cross-sectional nationwide surveys (in 1996, 2000, 2004, 2007, and 2008) of “alcohol consumption and smoking habits among junior and senior high school students.”7–13 The present study represents the sixth such survey. For this study, from among the 10 815 junior high schools and 5116 senior high schools registered in Japan as of May 1, 2010,14 131 junior high schools (selection rate: 1.2%) and 113 senior high schools (selection rate: 2.2%) were sampled. Using the stratified single-stage cluster-sampling method, we divided Japan into regional blocks and randomly selected schools from each block. In order to avoid any sampling bias toward specific regional blocks, stratified sampling was performed using the regional blocks as the strata. All of the students enrolled in the sampled schools were the subjects of this study. The sample size was determined by referring to the response rate and confidence intervals (CIs) based on the variance of the results obtained from previous studies.8,9 In the Japanese education system, children enter primary school at the age of 6 years and leave after 6 years of study. They then enter junior high school for 3 years, followed by a further 3 years at senior high school. Primary and junior high school education is compulsory. In this study, the first to third years of junior high school are called the seventh (12 or 13 years old) to ninth grade (14 or15 years old), and the first to third years of senior high school are called the tenth (15 years old or higher) and twelfth grade (17 years old or higher).
Survey procedure. We sent a letter to the principal of each selected school asking for cooperation in our survey, along with the same number of questionnaires and envelopes as the number of students enrolled at the school. At schools that agreed to participate, each class teacher distributed the questionnaires to the students. To protect the privacy of respondents and obtain candid responses, it was clearly stated on the questionnaire that completed questionnaires would not be seen by the teachers. After filling in the anonymous questionnaire, each student was asked to seal it in the envelope provided with an adhesive flap. Collection and delivery of the questionnaires were entrusted to the class teachers, who were instructed to follow the guidelines for conducting the survey. The teachers collected the sealed envelopes and returned them to Nihon University School of Medicine without opening them. The survey period was from October 2010 until the end of December 2010. The survey was approved by the ethics committee of Nihon University School of Medicine.
Measures. The major areas included in the questionnaire were (i) personal data, (ii) lifestyle, (iii) sleep status, (iv) mental health status, (v) frequency of stools, and (vi) symptoms of IBS.
Adolescents irritable bowel syndrome
Personal data. The personal data included, sex, school grade, and type of school (junior high school/senior high school). Lifestyle. The questions related to lifestyle were whether the student ate breakfast and whether he or she participated in extracurricular activities. In addition, to examine smoking and drinking habits, question on how many days the student had smoked (consumed alcoholic beverages) during the previous month was included in the questionnaire. If the response to this question was “1 day or more,” the student was considered a “smoker (alcohol drinker).” Sleep status. The sleep status items included sleep duration, bedtime, subjective sleep assessment, and insomnia symptoms. And each sleep status was defined by reference to the previous studies.11,15 Mental health status. To evaluate the mental health statuses of the respondents, two independent factors (“depression/anxiety” and “loss of positive emotion”) included in the 12-item General Health Questionnaire16–18 were used, and two items that were the highest factor loadings of each factor were selected. Frequency of stools. To evaluate the frequency of stools, a question on the number of times a day the student had defecated on average was included in the questionnaire. A 7-point scale about frequency was used for evaluation. Symptoms of IBS. We prepared questions to evaluate IBS based on the Rome III Diagnostic Criteria for Functional Gastrointestinal Disorders (FGID),19 the definitions that had been used in previous large-scale community-based surveys,20,21 and a previous survey22 of adults conducted in Japan. And we used adult FGID criteria in order to compare the prevalence of this with that of previous Japanese surveys.5,22,23 To examine the presence of abdominal pain or discomfort (prerequisites for IBS), a question on the number of days a month the student had suffered abdominal pain or discomfort in the previous 3 months was included in the questionnaire (possible replies were “never,” “1 day a month,” “2 days a month,” or “3 or more days a month”). If the response was “1 day or more,” the student was instructed to answer the following four questions: (i) “Does your abdominal pain or discomfort ameliorate after defecation? (‘yes’ or ‘no’)”; (ii) “Is the onset of abdominal pain or discomfort associated with a change in stool frequency? (‘increase,’ ‘decrease,’ or ‘no change’)”; (iii) “Is the onset of abdominal pain or discomfort associated with a change in stool form? (‘lumpy or hard stools,’ ‘loose or watery stools,’ ‘repeatedly alternating hard stools and loose stools,’ ‘other form of stools different from usual,’ or ‘no change’)”; and (iv) “Were you diagnosed by a physician as having a common cold or food poisoning that would only temporarily cause abdominal pain or discomfort? (‘yes’ or ‘no’).” A student with IBS was considered to have had abdominal pain or discomfort for at least 3 days a month over the previous 3 months, without a diagnosis of common cold or food poisoning to account for the symptoms (hereafter referred to as “abdominal symptoms due to unknown cause”), and who met at least two of the following three subcategory criteria: abdominal pain or dis-
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Table 1
R Yamamoto et al.
Frequency of stools among Japanese adolescents
Male Junior high school Seventh grade Eighth grade Ninth grade High school Tenth grade Eleventh grade Twelfth grade Total Female Junior high school Seventh grade Eighth grade Ninth grade High school Tenth grade Eleventh grade Twelfth grade Total
< 1T/W (%)
1T/W (%)
1T/4 or 5D (%)
1T/2 or 3D (%)
1T/D (%)
2T/D (%)
> 3T/D (%)
Uncertain (%)
0.8 0.6 1.0
1.5 1.3 0.9
1.7 1.2 1.3
12.1 12.4 11.8
37.1 40.1 41.0
34.3 32.2 32.1
11.3 11.2 10.9
1.4 1.1 1.1
6 435 6 401 6 207
0.5 0.3 0.5 0.6
0.9 0.7 0.9 1.0
1.6 1.2 1.4 1.4
12.3 11.6 11.4 11.9
41.2 40.7 40.7 40.3
32.2 32.5 30.9 32.3
10.3 11.7 13.2 11.4
0.9 1.2 1.1 1.1
10 498 9 965 6 207 48 562
1.8 1.6 1.6
3.0 3.3 3.9
3.5 4.0 3.9
23.3 24.5 26.4
41.4 42.5 43.6
20.6 17.9 15.7
4.6 4.0 3.1
1.9 2.1 1.8
6 606 6 415 6 269
1.7 1.4 1.7 1.6
4.2 4.0 4.1 3.8
5.0 4.4 4.8 4.4
28.8 29.4 28.9 27.4
42.8 42.9 42.1 42.6
13.6 13.7 13.6 15.4
2.8 2.9 3.5 3.4
1.1 1.2 1.2 1.5
10 946 10 203 9 410 49 849
n
Seventh grade = 12 or 13 years old; eighth grade = 13 or 14 years old; ninth grade = 14 or 15 years old; tenth grade = 15 years old or more; eleventh grade = 16 years old or more; twelfth grade = 17 years old or more. D, day; T, time(s); W, week.
comfort (i) improving with defecation, (ii) associated with a change in stool frequency, and (iii) associated with any change in stool form. We classified students with IBS into four subtypes, depending on the change in stool form, by reference to a previous survey.22 Students with IBS who had “lumpy or hard stools” were classified as having IBS with constipation (IBS-C), those with “loose or watery stools” as having IBS with diarrhea (IBS-D), those with “repeatedly alternating hard stools and loose stools” as having IBS mixed type (IBS-M), and those with “other forms of stool different from usual” or “no change” as having untyped IBS (IBS-U). Statistical analysis. First, the responses related to stool frequency were assessed. Next, the prevalence of IBS and that of each IBS subtype was calculated, along with the 95% CI. Then, the sex-based prevalence of IBS was calculated and tabulated into a cross-tabulation table. Finally, multiple logistic regression analyses (step-down method) were performed using binary data from students, with IBS and controls as the explained variables, and personal data, lifestyle factors, sleep status, and mental health status as covariates, in order to describe how many times more likely these covariates among students with IBS are discernible compared with controls. Chi-squared test was also performed to examine differences in each factor of participants by considering the various subtypes of IBS. All analyses were performed using the IBM SPSS Statistics 19 package (Armonk, NY, USA) for Windows.
Results Response rates. Replies were obtained from 89 of the 131 junior high schools (school response rate: 67.9%) and 81 of the 1356
113 senior high schools (school response rate: 71.7%; combined junior and senior high school response rate: 69.7%); 99 416 envelopes were collected. The student response rate as a proportion of enrolled students in the sampled schools was 91.3% for the junior high schools, 92.8% for the senior high schools, and 92.2% as a whole. Accordingly, the overall response rate was 62.1% for the junior high schools, 65.3% for the senior high schools, and 64.0% as a whole. Of the collected questionnaires, 1005 were excluded because the student’s sex or grade was not specified or there were conflicting responses. The data from the remaining 98 411 questionnaires were analyzed.
Frequency of stools. The frequency of stools based on the grade in school and sex is shown in Table 1.
Prevalence of IBS. A total of 17 882 students were considered to have IBS, giving a prevalence of 18.6% (95% CI: 19.2– 17.9%). With regard to IBS subtypes, 2064 students had IBS-C (2.1%; 95% CI: 2.8–1.5%), 9529 had IBS-D (9.9%; 95% CI: 10.5–9.3%), and 2120 had IBS-U (2.2%; 95% CI: 2.8–1.6%). The cross-tabulation based on the grade in school and sex is shown in Table 2.
Exploratory analysis for correlates of IBS. The results of multiple logistic regression analyses are shown in Table 3. All covariates except for sex and early morning awakenings were significantly related to IBS. The results of chi-squared tests are shown in Table 4. There were significant differences among IBS subtypes in sex, drinking
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Table 2
Adolescents irritable bowel syndrome
Prevalence of IBS among Japanese adolescents n
Male Junior high school Seventh grade Eighth grade Ninth grade High school Tenth grade Eleventh grade Twelfth grade Total Female Junior high school Seventh grade Eighth grade Ninth grade High school Tenth grade Eleventh grade Twelfth grade Total
IBS-C (%)
IBS-D (%)
IBS-M (%)
IBS-U (%)
IBS total (%)
6 297 6 285 6 084
0.8 1.1 1.0
6.6 7.9 9.7
1.7 2.1 2.5
1.4 1.7 2.2
10.5 12.9 15.4
10 298 9 767 8 882 47 613
1.3 1.2 1.6 1.2
11.7 13.1 13.9 11.0
3.1 3.6 3.7 2.9
2.6 2.7 3.1 2.4
18.7 20.7 22.3 17.5
6 426 6 281 6 113
1.7 2.3 2.2
5.2 6.9 7.5
2.9 4.1 4.3
1.3 1.2 1.6
11.1 14.5 15.6
10 688 9 945 9 208 48 641
3.1 3.8 4.3 3.1
9.1 10.6 11.5 8.9
6.1 7.1 7.7 5.7
2.3 2.3 2.7 2.0
20.5 23.8 26.2 19.6
Seventh grade = 12 or 13 years old; eighth grade = 13 or 14 years old; ninth grade = 14 or 15 years old; tenth grade = 15 years old or more; eleventh grade = 16 years old or more; twelfth grade = 17 years old or more. For calculation of the prevalence rates, subjects were excluded if a diagnosis could not be determined because of missing responses. IBS, irritable bowel syndrome; IBS total, all types of irritable bowel syndrome; IBS-C, irritable bowel syndrome with constipation; IBS-D, irritable bowel syndrome with diarrhea; IBS-M, irritable bowel syndrome mixed type; IBS-U, untyped irritable bowel syndrome.
alcohol, sleep duration, subjective sleep assessment, difficulty initiating sleep, difficulty maintaining sleep, depression and anxiety, and loss of positive emotion.
Discussion Prevalence of IBS and its subtypes. In this study, the prevalence of IBS among Japanese adolescents was 18.6%. The prevalence identified in this study was similar to that reported in a survey5 of junior high school students in Miyagi Prefecture, which used the Rome II diagnostic criteria (14.6% in 2004 and 19% in 2009). Compared with the Rome II criteria, the use of the Rome III criteria has been reported to produce higher prevalence rate estimations.21,23,24 The prevalence of IBS in this study was also higher than that (13.1%) reported from a nationwide Internet Rome III survey of adults.23 Examination of the prevalence rates of IBS subtypes in the present study indicated that IBS-D had the highest prevalence. This finding was in accord with the results of a crosssectional survey22 that used the Rome III diagnostic criteria and included Japanese workers. Because the prevalence of IBS (particularly IBS-D) among adolescents in Japan thus appears to be very high, appropriate public health measures are urgently needed. Correlates of IBS Relationship between personal data and IBS. There was no difference in the prevalence rate of IBS between the sexes. However, in terms of IBS subtype, the prevalence rates of IBS-C
and IBS-M were higher among girls than among boys, whereas those of IBS-D and IBS-U were higher among boys than among girls. Such differences were also observed in a previous survey22 of Japanese adults, which suggested that constipation tended to be more frequent among women than among men.25 We also observed a linear relationship between grade in school and IBS. In Japan, adolescence might be a period of IBS susceptibility. Relationship between lifestyle and IBS. The present study indicated that the prevalence of IBS among students who never ate breakfast or who ate occasionally was lower than that among those who ate every day. However, the previous study26 suggested that people with IBS had a significantly higher frequency of not eating breakfast than a control group without abdominal symptoms. The gastrocolic reflex associated with intake of breakfast contributes to regularity of metabolic rhythm.27 More details regarding breakfast intake, such as its timing and content, should be investigated in future studies. The prevalence of IBS among smokers was lower than nonsmokers. The results of previous studies on this topic have varied; one study22 reported that the prevalence of IBS among smokers was higher than that among nonsmokers, but others28,29 reported no associations. It was reported that the effects of smoking on colonic transit time differed in individual attributes.30 The effects of smoking in adolescents may differ from those in adults. The effects of smoking on the GI function of adolescents will need to be examined. An association between alcohol consumption and IBS, particularly IBS-M, was suggested. Previous epidemiological studies tar-
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Table 3
R Yamamoto et al.
Exploratory analysis for correlates of irritable bowel syndrome Covariates
Sex Grade in school
Eating breakfast
Extracurricular activity Smoking Drinking alcohol Sleep duration
Bedtime Subjective sleep assessment Difficulty initiating sleep Difficulty maintaining sleep Early morning awakening Depression and anxiety Loss of positive emotion
Adjusted odds ratio Male Female Seventh grade Eighth grade Ninth grade Tenth grade Eleventh grade Twelfth grade Daily Occasionally Never Participating Not participating No Yes No Yes 8h Before 0:00 After 0:00 Good Bad No Yes No Yes No Yes No Yes No Yes
Reference 1.03 Reference 1.20 1.25 1.64 1.87 2.01 Reference 0.86 0.86 Reference 1.11 Reference 0.83 Reference 1.21 0.84 0.98 Reference 0.99 0.95 Reference 1.23 Reference 1.35 Reference 1.16 Reference 1.13 Reference 0.93 Reference 1.62 Reference 1.10
95% confidence interval
P-value
Low
High
1.00
1.07
0.08
1.11 1.16 1.53 1.74 1.87
1.30 1.36 1.76 2.01 2.16
0.00 0.00 0.00 0.00 0.00
0.80 0.80
0.90 0.92
0.00 0.00
1.07
1.15
0.00
0.76
0.91
0.00
1.17 0.80 0.93
1.26 0.89 1.03
0.00 0.00 0.33
0.94 0.89
1.05 1.02
0.83 0.17
1.19
1.29
0.00
1.29
1.40
0.00
1.11
1.22
0.00
1.07
1.19
0.00
0.86
1.00
0.06
1.56
1.68
0.00
1.05
1.16
0.00
The results of the final steps are shown. All variables were entered.
geting adults have produced varying results; one study28 reported no association between alcohol consumption and IBS (subtypes were not examined), whereas another study22 reported an association only with IBS-D. In addition to the direct effects of alcohol on tissues, the process of alcohol metabolism affects the bloodstream, motility, and digestive/absorptive functions of the GI tract.31 Such effects might be observed in the adolescents in this study. It has been suggested that the prevalence of IBS is lower in individuals who sleep less than 5 h per night. However, a previous study found that patients with IBS had significantly shorter sleep duration than those who did not.27 In this study, late bedtime and insomnia symptoms (subjective sleep quality difficulty initiating or maintaining sleep) were related to IBS. It has been reported that GI motility has a circadian rhythm similar to the sleep–wake cycle,32,33 and that there are interactive relations between GI motility and the sleep–wake cycle. Based on these findings, it may be concluded that worsened sleep efficiency because of insomnia 1358
symptoms and the disrupted sleep–wake rhythm, rather than sleep duration, may be associated with IBS. And students with IBS-M experience more insomnia symptoms and go to bed later than those with other phenotypes. The relationships between sleep disturbance and GI motility will need to be investigated. Relationship between mental health status and IBS. The results suggested that depression/anxiety was strongly associated with IBS, along with previous studies. Many studies have reported associations between IBS and mental disorders, particularly mood disorders and anxiety disorders.34,35 In addition, because it has been reported that adolescents with IBS have higher subjective stress levels than those without IBS, management of depression/ anxiety seems to be important.36 And in this study, the constipation symptom was especially related to mental health status. The reason of these result and brain–gut correlation in adolescents will need to be explained.
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Table 4
Adolescents irritable bowel syndrome
Characteristics of the correlates based on the subtypes of IBS
Variables Sex Grade in school
Eating breakfast
Extracurricular activity Smoking Drinking alcohol Sleep duration
Bedtime Subjective sleep assessment Difficulty initiating sleep Difficulty maintaining sleep Early morning awakening Depression and anxiety Loss of positive emotion
Male Female Seventh grade Eighth grade Ninth grade Tenth grade Eleventh grade Twelfth grade Daily Occasional Never No Yes No Yes No Yes 8h Before 0:00 After 0:00 Good Bad No Yes No Yes No Yes No Yes No Yes
IBS-C
IBS-D
‡
†
576 1488† 155 212 195 467 500 535 1739 188 117 739 1297 1977 84 1372 687 395 357 922 226 240 877 1158 1075 962 1681 358 1755 285 1920 123 752‡ 1291† 1696‡ 344†
5218 4311‡ 749 928 1048 2172 2340 2292 7968 856 587 3238 6128 9112 410 6369† 3141‡ 1731 1621 4299 1046 697 4048 5341 4939† 4436‡ 7836† 1550‡ 8265† 1126‡ 8898 507 4134† 5276‡ 8020 1388
IBS-M ‡
1404 2765† 294 391 412 9 74 1057 1041 3475 391 262 1400 2701 4003 163 2626‡ 1533† 805 783† 1845 437 258‡ 1696‡ 2421† 1984‡ 2118† 3287‡ 823† 3499‡ 617† 3854 268 1538‡ 2589† 3466 659
IBS-U †
1131 989‡ 174 186 234 509 494 523 1783 193 128 745 1343 2002 114 1433 682 380 346 949 257 174† 943 1160 1116 978 1738 361 1850 253 1979 123 991† 1115‡ 1811 294
Total
χ2
8 329 9 553 1 372 1 717 1 889 4 122 4 391 4 391 14 965 1 628 1 094 6 122 11 469 17 094 774 11 800 6 043 3 311 3 107 8 015 1 966 1 269 7 564 10 080 9 114 8 494 14 542 3 092 15 369 2 281 16 651 1 021 7 415 10 271 14 993 2 685
863.4
3
0.00
19.5
15
0.19
1.5
6
0.96
3.7
3
0.29
7.5
3
0.06
22.3
3
0.00
22.9
12
0.03
8.3
3
0.04
24.9
3
0.00
24.5
3
0.00
26.4
3
0.00
6.8
3
0.08
97.8
3
0.00
10.2
3
0.02
df
P-value
Seventh grade = 12 or 13 years old; eighth grade = 13 or 14 years old; ninth grade = 14 or 15 years old; tenth grade = 15 years old or more; eleventh grade = 16 years old or more; twelfth grade = 17 years old or more. Haberman residual analyses were performed for variables that were found to be significant with a significance level of 5% in the chi-squared test. † The observed frequency was significantly greater than the expected frequency at the 5% level. ‡ The observed frequency was significantly smaller than the expected frequency at the 5% level. IBS, irritable bowel syndrome; IBS-C, irritable bowel syndrome with constipation; IBS-D, irritable bowel syndrome with diarrhea; IBS-M, irritable bowel syndrome mixed type; IBS-U, untyped irritable bowel syndrome.
Limitation and future direction. To our knowledge, this was the first nationally representative study of IBS among Japanese adolescents. But the items of questionnaire were limited because this survey was performed at a single point in time. Detailed exclusion criteria (e.g. red flags of Rome III, other functional GI disease, or organic GI disease) were not checked. Therefore, the prevalence had potential to be overestimated. And school-related valuables (absenteeism or presenteeism from school, or school examination performance) and consultation behavior also were not assessed. So it is hard to say how much IBS and its related condition leads school maladaptation. And we conducted crosssectional survey and multivariable analysis in this study; these
kinds of methods tend to make the result significant because of large sample size. Based on this study, analytic epidemiological studies or intervention study, which clarifies the detail as pointed above, will be needed. Especially, the significant relationships between delayed sleep-phase, insomnia symptoms, and poor mental health status and IBS were confirmed in this study. In our previous study, students with insomnia symptoms were one in four or five,10,11 and mental health and sleep statuses were related among adolescents.37 From the viewpoint of school health, the effects of health education (e.g. bedtime and insomnia management and stress management) on IBS prevention will need to be examined.
Journal of Gastroenterology and Hepatology 30 (2015) 1354–1360 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd
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Acknowledgment This study was supported by a health science research grant from the Ministry of Health, Labor and Welfare of the Japanese Government.
References
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