| | Prevalence and risk factors of irritable bowel syndrome in Korean adolescent girls: A school-based studyReceived 8 March 2008; received in revised form 30 May 2008; accepted 12 July 2008. Abstract BackgroundIrritable bowel syndrome (IBS) is one of the most common functional gastrointestinal disorders, with a strong female predominance. When compared to the vast knowledge pertaining to adults with IBS, very little is known about IBS in the adolescent population. In Korea, the field of adolescent health with IBS is just beginning to develop, so there is still a lack of information concerning the prevalence of IBS in adolescent groups. ObjectivesThe purposes of this study were to explore the prevalence of IBS among Korean adolescent girls, and identify the risk factors affecting IBS occurrence. DesignThis study adopted a cross-sectional descriptive design using the self-reported questionnaire. MethodsA total of 405 adolescent females were recruited from 5 academic high schools in Korea in August and September of 2007. IBS was diagnosed based on the Rome II criteria. For the evaluation of risk factors on the IBS, we investigated dietary habit, life style, stress, anxiety, depression, and premenstrual syndrome (PMS). ResultsThe prevalence of IBS according to Rome II criteria was 25.7% in the subjects. The multivariate logistic regression analyses revealed that higher stress (OR 2.25, 95% CI 1.13–4.48), anxiety (OR 4.27, 95% CI 1.09–16.71), and depression (OR 10.87, 95% CI 1.14–103.81) were independently associated with increased IBS occurrence. ConclusionsThe prevalence of IBS in female adolescent students from this study was higher compared with those reported in the Western countries. This study provides much need information about the relatively unstudied Korean female adolescents in terms of IBS issues and aspects of psychological attributes to IBS. This study has the potential to influence the development of better promotion programs for adolescents and women's health. What is already known about the topic? •Irritable bowel syndrome (IBS) is a common disorder of the general population that can lead to loss of working time and increased health-care costs. •The small number of previous studies carried out in Western countries has investigated psychological attributes, menstrual cycle, dietary habits and lifestyle as risk factors of IBS. •Some Korean studies have focused on the prevalence of IBS in adults, and there are few data on the prevalence and risk factors (including psychological and menstruation-related problems) in adolescents with IBS. What this paper adds •The prevalence of IBS in healthy female adolescents is higher in Korea than in other Asian countries and the West. •Psychological factors may play an important role in the development of IBS and its severity in adolescents. 1. Introduction  Irritable bowel syndrome (IBS) is a common functional gastrointestinal disorder that is characterized by chronic abdominal discomfort or pain, bloating and changes in bowel habits (Agrawal and Whorwell, 2006). The reported prevalence of IBS is 15–24% in the general population, with the reported variation being due to epidemiological studies using different diagnostic criteria, population selection and data sources (Frank et al., 2002, Hungin et al., 2003). Most of the literature comes from Western industrialized societies, but this disorder appears to be equally common in Asia (Dong et al., 2005, Spiller, 2004). The number of new IBS patients increases by 1% annually in South Korea, with 20–50% of such patients being referred from primary health-care centres to specialized gastrointestinal clinics (Han et al., 2006, Yoo, 2002). IBS can affect men and women of all ages and the condition generally appears first in young adulthood, with the prevalence being twofold higher in women than in men (Sloots et al., 2001). IBS does not permanently damage the intestines and does not lead to serious diseases such as cancer, and most people with IBS can control their symptoms with diet, stress management and prescribed medications. However, IBS has a major impact on quality of life. Aspects of social and professional life are affected, resulting in increased absenteeism from work and reduced job opportunities and social interaction (Camilleri and Williams, 2000, De Giorgio et al., 2004). IBS therefore exerts a significant psychological and physical cost on those afflicted with it. Adolescence is a unique time in human development, both physiologically and psychologically. Adolescents in modern society face many health issues, particularly in the areas of mental, emotional and social health. Unfortunately, adolescence is also a period of life when there is little or no contact with health-care professionals, with subsequent adult health depending on risk factors and health-related behaviours performed during adolescence (Hyams et al., 1996, Lim and Kim, 2003). Moreover, Korean adolescents devote large amounts of time to study, and many attend private cramming schools after school on weekends in order to do well in the entrance examinations of high-ranking universities (Lee and Larson, 2000). In the Korean high-school system, students experience high stress levels related to general studying demands and preparations for college admission, which may contribute to high rates of serious physical or psychological problems (Kim and Lim, 2002). The risk factors of IBS are not well understood but are probably multiple, including biological, psychological and social factors (Dapoigny et al., 2003, Drossman, 2006). It is not yet possible to precisely diagnose the individual causes of IBS and the underlying maintenance mechanisms, despite these factors being researched extensively over the past few decades. Nurses should encourage adolescents to seek care promptly if they experience symptoms of IBS. However, there is a paucity of empirical data on the prevalence and risk factors of IBS in Korean adolescents. The aims of the present study were (1) to describe the prevalence of IBS in Korean adolescent females according to the Rome II diagnostic criteria based on bowel symptoms, and (2) to identify the risk factors that influence the presence of IBS. 2. Methods 2.2. Ethical aspects Letters were sent to seven academic high schools to request permission for their students to participate in this study on the health of adolescent girls. Ethical approval was obtained from five schools, from which the study subjects were recruited. Before collecting any data, the researcher met with students during a class period and provided them with an information sheet describing the study, and emphasized the voluntary nature of their participation. Signed informed consent to participate was obtained from all subjects. Each participant was assigned a code known only to the researcher in order to preserve confidentiality. 2.3. Instruments 2.3.1. Diagnosis of IBS The diagnosis of IBS was based on Rome II criteria, which are based strictly on symptoms and exhibit higher specificity than other criteria, making this system useful for diagnosing in clinical practices due to the lower possibility of missing organic conditions (Malagelada and Malagelada, 2006). According to the Rome II system, IBS involves abdominal discomfort or pain lasting at least 12 weeks as the primary symptom, together with at least two out of three other features: (1) the pain is relieved with defecation, (2) the symptom onset is associated with a change in frequency of stool or (3) the symptom onset is associated with a change in the form (appearance) of stools (Dapoigny et al., 2003). Subjects with IBS were categorized as either a constipation-predominant type or a diarrhoea-predominant type; those who could not be categorized as either of these were classified as alternators. 2.3.2. Dietary and lifestyle factors Based on a literature review, data on the following dietary and lifestyle factors associated with IBS were collected from the participants using a short questionnaire. The 11-item questionnaire was used to obtain information on diet and lifestyle during the previous 12 months. Dietary factors included mealtimes (regularly/irregularly), frequency of grain intake, and intakes of milk products, fruit, sweet food, salty food and fatty food (preferred/not preferred). The lifestyle factors included smoking (yes/no), exercise level (almost never/sometimes/almost everyday) and alcohol consumption (yes/no). 2.3.3. Stress The Brief Encounter Psychosocial Instrument (BEPSI) is a well-studied and validated indicator of perceived stress that is useful among primary-care populations (Frank and Zyzanski, 1988). The BEPSI is acceptable as a screening instrument for the rapid assessment of stress in busy practices. This assessment tool was selected since it has been used frequently in both domestic and Western research (Bae et al., 1996), thus allowing comparisons, has sound validity and reliability, and is simple and rapid to apply to subjects. Bae et al. (1996) developed a Korean translation of the BEPSI. The five items are scored on a Likert-type 5-point scale from 1 (not at all) to 5 (almost always). The range of possible scores for this scale is 5–25, where a higher score being indicative of a higher level of perceived stress. To provide comparisons between the group for whom the stress level score was in the lowest 25% of scores and that for whom the stress level score was in the highest 25% of scores, the level of stress was divided into quartiles. Cronbach's alpha for stress was 0.824. 2.3.4. The hospital anxiety and depression scale The hospital anxiety and depression (HAD) scale is a brief, self-reported measure of anxiety (HAD-anxiety) and depression (HAD-depression) that was developed by Zigmond and Snaith (1983). The HAD scale consists of two, seven-item, self-reported subscales designed to assess current anxiety and depressive symptomatology, respectively, in non-psychiatric hospital settings. The items are scored on a 4-point scale from 0 (not present) to 3 (considerable). The item scores are added, giving sub-scale scores on the HAD-anxiety and the HAD-depression scales from 0 to 21. In this study, interpretation of the HAD Scale is based primarily on the use of generally accepted cut-off scores (Herrmann, 1997). For HAD-anxiety and HAD-depression, raw scores of between 8 and 10 identify mild cases, 11–15 moderate cases and 16 or above, severe cases. Cronbach's alpha values for HAD-anxiety and HAD-depression were 0.750 and 0.710, respectively. 2.3.5. Premenstrual syndrome The Korean premenstrual syndrome (PMS) questionnaire was used to assess the level of measure PMS. This questionnaire was developed by Kwon (1996) and was based on the Menstrual Distress Questionnaire (Moos, 1968), an open-questioned interview with Korean 20 female high-school students and peer review, and tested through several empirical studies in South Korea. It has well-demonstrated reliability and validity in Korea (Kim et al., 2004). This 48-item, Likert-type scale has a 5-point response format ranging from 1 (not at all) to 5 (very much). These scales included behavioural change (nine items), negative affect (eight items), labelled pain (seven items), impaired concentration (eight items), water retention (six items), skin change (two items), autonomic reactions (six items) and dietary change (two items). The range of possible scores for this scale is 48–240, with a higher score indicating a higher level of PMS symptoms. To provide comparisons between the group for whom the PMS score was in the lowest 25% of scores and that for whom the PMS score was in the highest 25% of scores, the level of PMS was divided into quartiles. Cronbach's alpha for PMS was 0.963 in this study. 2.4. Statistical analysis Data were analysed using the Statistical Package for Social Sciences software (version 12.0). Univariate analyses were performed using the chi-square test, and the forward logistic regression model was used for the multivariate analysis. The categorized probable risk factors were entered into the logistic regression analysis as categorical covariates using a different reference category for each risk factor. Sum variables (stress and PMS) were formed for analytical purposes from the items that measure the dependent variables. The scores that each subject gave to the questions that belonged to each category were summed. The sum variables were then divided into four categories according to a quartile. The first quartile (designated Q1) is the lower quartile, cutting off the lowest 25% of data. The second quartile (designated Q2) is the median, cutting the data set in half. The third quartile (designated Q3) is the upper quartile, cutting off the highest 25% of data. In descriptive statistics, a quartile is any of the three values that divide the sorted data set into four equal parts, so that each part represents one-quarter of the sample or population. Stress levels were divided into quartiles as follows: scores of less than 10, 11 or 12, 13–15 and greater than 15 were classified as Q1, Q2, Q3 and Q4, respectively. PMS was divided into quartiles as follows: scores of less than 93, 94–122, 123–144 and greater than 144 were classified as Q1, Q2, Q3 and Q4, respectively. The dependent variable (IBS) was coded as either 1 (IBS) or 0 (non-IBS). 3. Results 3.2. Risk factors of IBS Dietary and lifestyle factors in the two groups are presented in Table 2. Univariate analysis showed that IBS patients ate significantly more salty (χ2 =4.183, p=0.041) and higher-cholesterol (χ2=4.248, p=0.039) food than non-IBS subjects. No group differences were noted for smoking, exercise or alcohol consumption. | | |  | Variables | Categories | Total (n=405) | With IBS (n=104) | Without IBS (n=301) | χ2 | p-Value | |
|---|
| | | n (%) | n (%) | n (%) | | | |
|---|
| Food habit | | | Mealtime | Regularly | 186 (45.9) | 53 (28.5) | 133 (71.5) | 1.429 | 0.232 | | | Irregularly | 219 (54.1) | 51 (23.3) | 168 (76.7) | | | | | | | | Grains | Almost every times | 273 (67.4) | 80 (29.3) | 193 (70.7) | 5.774 | 0.056 | | | Sometimes | 98 (24.2) | 18 (18.4) | 80 (81.6) | | | | | Once | 34 (8.4) | 6 (17.6) | 28 (82.4) | | | | | | | | Dairy produce | Almost everyday | 98 (24.3) | 30 (30.6) | 68 (69.4) | 3.873 | 0.144 | | | Sometimes | 192 (47.5) | 52 (27.1) | 140 (72.9) | | | | | Almost never | 114 (28.2) | 22 (19.3) | 92 (80.7) | | | | | | | | Fruit | Almost everyday | 126 (31.1) | 26 (20.6) | 100 (79.4) | 4.411 | 0.110 | | | Sometimes | 199 (49.1) | 51 (25.6) | 148 (74.4) | | | | | Almost never | 80 (19.8) | 27 (33.8) | 53 (66.3) | | | | | | | | Sweet food | Not preferred | 115 (28.4) | 22 (19.1) | 93 (80.9) | 3.609 | 0.057 | | | Preferred | 290 (71.6) | 82 (28.3) | 208 (71.7) | | | | | | | | Salty food | Not preferred | 237 (58.5) | 52 (21.9) | 185 (78.1) | 4.183 | 0.041 | | | Preferred | 168 (41.5) | 52 (31.0) | 116 (69.0) | | | | | | | | Fatty food | Not preferred | 184 (45.4) | 44 (23.9) | 140 (76.1) | 0.551 | 0.458 | | | Preferred | 221 (54.6) | 60 (27.1) | 161 (72.9) | | | | | | | | High-cholesterol food | Not preferred | 256 (63.2) | 57 (22.3) | 199 (77.7) | 4.248 | 0.039 | | | Preferred | 149 (36.8) | 47 (31.5) | 102 (68.5) | | | | | | | | Smoking | No | 389 (96.0) | 100 (25.7) | 289 (74.3) | 0.004 | 0.949 | | | Yes | 16 (4.0) | 4 (25.0) | 12 (75.0) | | | | | | | | Exercise levels | Almost never | 253 (62.5) | 66 (26.1) | 187 (73.9) | 0.093 | 0.954 | | | Sometimes | 78 (19.2) | 19 (24.4) | 59 (75.6) | | | | | Almost everyday | 74 (18.3) | 19 (25.7) | 55 (74.3) | | | | | | | | Alcohol consumption | No | 366 (90.4) | 92 (25.1) | 274 (74.9) | 0.586 | 0.444 | | | Yes | 39 (9.6) | 12 (30.8) | 27 (69.2) | | | | | | |
The subjects’ psychological factors and frequencies of PMS and IBS are listed in Table 3. Univariate analysis showed that 14.6% and 40.8% of subjects with stress levels in Q1 and Q4, respectively, had IBS (χ2=19.738, p<0.001). IBS patients had significantly higher levels of anxiety (χ2=20.608, p<0.001) and depression (χ2=19.446, p<0.001), and higher PMS scores (χ2=8.543, p=0.036) compared to non-IBS subjects. Table 4 presents the results of the multivariate logistic regression analysis. The 2-log likelihood value was ‘318.525’, which indicates that the logistic regression model matched the data well. The multivariate logistic regression analyses revealed that higher stress, anxiety and depression were independently associated with increased IBS occurrence. Compared to Q1, the relative risk for stress levels was 3.15 (95% CI=1.40–7.08) in Q2, 1.56 (95% CI=0.73–3.35) in Q3 and 2.25 (95% CI=1.13–4.48) in Q4. The likelihood of IBS was 4.27-fold higher in subjects with severe anxiety than in those with normal anxiety levels (95% CI=1.09–16.71). The prevalence of IBS was 13.21-fold (95% CI=1.40–124.91), 17.08-fold (95% CI=1.83–159.11) and 10.87-fold (95% CI=1.14–103.81) higher in subjects with mild, moderate and severe depression, respectively, than in non-depressed subjects. 4. Discussion We found that the prevalence of IBS in our 405 subjects was 25.7%. The reported prevalence of IBS (Rome II criteria) in adults varies from 8% to 24%: 14–24% in women and 8–19% in men (Drossman, 1999, Hungin et al., 2003). The reported prevalence of IBS varies greatly between epidemiological studies, which may be due to the inclusion of different diagnostic criteria and to different gender and race distributions of the subjects. There are a few points that should be noted. Firstly, some epidemiological studies have found the prevalence of IBS to be higher in children and adolescents than in adults (Dong et al., 2005, Reshetnikov et al., 2001). Secondly, Korean high-school students are under a great deal of pressure due to the long hours of studying required for admission to prestigious universities (Kim and Lim, 2002), and stress levels and IBS are strongly correlated (Drossman, 1999, Hungin et al., 2003). Thirdly, this study was limited by the prevalence being measured only once using the Rome II criteria. IBS is not a disease, and so there is no dependable biological marker for its diagnosis (Dai et al., 2008). A positive diagnosis of IBS is based on clinical criteria of the presentation of a complex of symptoms. However, the use in this study of a survey based on the Rome II criteria may have resulted in overdiagnosis of the disorder due to the short time frame; we should thus consider a differential diagnosis. Several disorders may present with similar symptoms. Examples include colonic neoplasia, inflammatory bowel disease, hyper- or hypo-thyroidism and endometriosis. Psychiatric disorders such as depression and anxiety must also be considered (Tierney et al., 2006). Future should examine the prevalence and risk factors for adolescents using a robust prospective design with repeated measures. We also suggest that prospective comparative studies should be conducted to confirm these results using accurate measurements such as simple blood tests and possibly a rigid sigmoidoscope. The Rome III criteria have recently been published by Drossman (2006); the main amendment is a less restrictive time frame—symptom onset should be at least 6 months prior to diagnosis and the symptom criteria should be fulfilled for the last 3 months. Sperber et al. (2007) reported that the prevalence of IBS in Israeli adults was significantly higher for Rome III criteria than for Rome II criteria, and revisions of the diagnostic criteria for IBS are also responsible for varying prevalence estimates. As the Rome II system has been more widely accepted than Rome III in clinical practice in South Korea, and the validity and reliability of the Rome III criteria in discriminating between IBS and organic disease has not yet been firmly established (Dai et al., 2008), we suggest that follow-up studies should compare the prevalence determined using the Rome II criteria with that determined using the new Rome III criteria for a Korean population. The present findings suggest that the risk factors of IBS are stress, anxiety and depression. Psychological factors play an important role in the development of IBS and may be the most important factors in terms of who manifests IBS and how severe it becomes in adolescents. Nicholl et al. (2007) demonstrated that psychosocial factors indicative of somatization are independent risk factors for the development of IBS in a group of subjects previously free of IBS. A population-based study of 507 middle-school and high-school students by Hyams et al. (1996) indicated that 6–14% of the adolescent population note symptoms consistent with IBS. In that study, anxiety and depression scores were significantly higher in students with IBS-type symptoms than in those without such symptoms. Psychological assessments of IBS patients show a higher prevalence of stress, abnormal personality features, psychiatric diagnosis and illness behaviour than in either normal subjects or other medical patients, suggesting that IBS is a biological vulnerability that worsens with psychological distress (Dong et al., 2005, Hazlett-Stevens et al., 2003, Reshetnikov et al., 2001). Negative affects, such as anxiety, can amplify symptoms and lead to their interpretation as an illness. Moreover, Asian IBS subjects often exhibit various psychological disturbances, including anxiety, emotional upset, depression, hysteria and poor psychological scores (Chang and Lu, 2007). Thus, it is clinically important to determine the psychological factors contributing to illness in individual patients. Future work is needed to explain the mechanisms and routes by which psychological factors affect IBS, by studying the relationships between various psychological factors including stress, anxiety and depression with the aid of biochemical markers. In addition, our results require replication to determine their generality because although the gut is physiologically responsive to emotional and stressful stimuli, there is no consistent relationship between psychological factors and IBS. This study found no relationship between PMS and IBS in the multivariate analysis, unlike in the univariate analyses. Women with IBS often report experiencing PMS and dysmenorrhoea (Altman et al., 2006, Heitkemper et al., 2003). PMS has been associated with higher depression, anger and cognitive problems at both the luteal and menses phases (Heitkemper et al., 2003, Kim et al., 2004). However, the menstrual cycle and PMS have been found to be inconsistent contributing factors to the development of IBS (Altman et al., 2006). One limitation of the present study is that the prevalence of IBS and PMS were measured only once and without considering the phase of the menstrual cycle, and hence a future study should examine the changes in the relationship between IBS and PMS in adolescents according to menstrual-cycle phase. The physiological and clinical effects of the menstrual cycle should also be taken into consideration when assessing for disease activity. The multivariate analysis carried out in the present study revealed no independent association between diet and lifestyle factors with the prevalence of IBS. Many patients with IBS believe that their symptoms are caused by food, and so they expect a dietary solution. Some exclude many foods with little evidence of improvement. In clinic-based studies, diet has been implicated as playing a role in functional gastrointestinal disorders including IBS (Saito et al., 2005). There is evidence that symptoms of IBS precede a change in dietary intake such as fibre, lactose, drinks containing excessive amounts of caffeine, fruit and nuts (Drossman, 1999, Herting et al., 2007, Spiller, 2004). The use of a systemic approach revealed that half of all IBS patients respond to a diet that excludes certain foods (Nanda et al., 1989). However, there is scant scientifically valid information on the relationship between diet and IBS symptoms. IBS is a complex disorder with a wide range of symptoms, some of which may indeed be related to diet (Paterson et al., 1999). Therefore the role of foods in gut symptoms needs to be studied further to develop a step-by-step approach for the management of this condition. In conclusion, we suggest that managing aggressive psychological distress in high-school students is very important for reducing the symptoms and morbidity associated with IBS. Thus, it is clinically important to assess the psychological risk factors contributing to illness in individual patients. Future research may lead to interventions that are effective at modifying the degree of psychological distress or negative affectivity. 5. Limitations of the study This study has yielded useful data on IBS in Korean adolescent females, but there are several important limitations that must be taken into consideration when drawing conclusions from the results. Firstly, the study findings are based wholly on self-reported symptoms and data without external verification, and thus we should consider whether the diagnosis of IBS is durable. Secondly, the retrospective and cross-sectional design of this study prevented the assessment of trends and comparisons of the prevalence and risk factors of IBS between this and other studies. We must therefore allow for the possibility that other factors contribute to any observed differences, such as how IBS was defined, when the studies were conducted and the instruments that were used. Another limitation of this study is that we did not include all risk factors of IBS, although we attempted to elucidate the important risk factors of IBS among Korean adolescents.Conflict of interest None.Funding: No competing actual or potential financial interests exist in this manuscript.Ethical approval: Ethical approval was obtained from five schools, from which the study subjects were recruited. 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