Journal of Neurogastroenterology and Motility 2019; 25(2): 233-240  https://doi.org/10.5056/jnm18028
Psychosocial Factors Associated With Irritable Bowel Syndrome Development in Chinese College Freshmen
Chen Jiang, Yan Xu, Stuti Sharma, Lei Zhang, Huan Wang, Jun Song, Wei Qian, Tao Bai*, Xiaohua Hou*
Division of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
Correspondence to: *Tao Bai and Xiaohua Hou are equally responsible for this study. Tao Bai, MD, Division of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China Tel: +86-15802734363, Fax: +86-27-85726057, E-mail: drbaitao@126.com. Xiaohua Hou, MD, Division of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China Tel: +86-13035143646, Fax: +86-27-85726057, E-mail: houxh@medmail.com.cn
Received: January 22, 2018; Revised: December 20, 2018; Accepted: February 26, 2019; Published online: April 30, 2019.
© The Korean Society of Neurogastroenterology and Motility. All rights reserved.

cc This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Background/Aims

The role of psychosocial factors on irritable bowel syndrome (IBS) in adolescents is incompletely understood. The aim of this study is to investigate the association between the psychosocial factors and the risk of developing IBS in college freshmen.

Methods

A cross-sectional survey was conducted in a randomly selected freshmen population in Wuhan China (n = 2449). Questionnaire evaluated demographics and psychosocial risks. The population was divided into 3 groups: non-discomfort, chronic abdominal discomfort and IBS. The association between the development of IBS and psychosocial factors was analyzed by ordinal and multiple logistic regression analysis.

Results

A total of 2053 (83.8%) completed this survey (mean age, 18.2 ± 0.9 years; female, 35.6%). Among them, 82 (4.0%) fulfilled the Rome III criteria for IBS. Female (odds ratio [OR], 3.31; 95% confidence interval [CI], 2.47–4.45), experience of abuse (OR, 2.44; 95% CI, 1.10–5.56), and suicidal intention (OR, 2.17; 95% CI, 1.15–4.17) were more likely to have IBS. Compared with chronic abdominal discomfort, however, depression (OR, 5.55; 95% CI, 1.36–22.71) was the only dependent risk factor for IBS.

Conclusion

The prevalence of IBS in college freshmen is 4.0%, and to the freshmen, psychosocial factors such as experience of abuse, depression, and suicidal intention were associated with high risk of developing IBS.

Keywords: Child abuse, Depression, Irritable bowel syndrome, Suicide
Introduction

Irritable bowel syndrome (IBS) is a common functional gastrointestinal disorder (FGID) in the general population, which cause a heavy social burden.16 Morbidity of IBS is diverse according to age, sex, occupation, and so on. Globally, the prevalence of IBS among college and university students was reported to range from 7.4% to 29.5%,710 much higher than those among children and adolescence (range from 1.2% to 5.6%).1116 In addition, previous researches showed that symptoms of IBS often appear in early adulthood.17 Therefore, the threshold of adulthood could be a progressive period for IBS.

The variety of the IBS incidence in early lifetime might be affected by a gradual development process of IBS. Chronic or recurrent abdominal pain is common in school-aged children and adolescents, and the prevalence was reported to range from 7% to 45%.1820 The chronic abdominal discomfort was suggested by previous studies to be an early-stage of IBS.21,22 In a birth cohort, Stuart Howell at el23 found childhood abdominal pain could progress to adult IBS and was not the result from psychiatric comorbidity or emotional distress in adulthood. However, it has still not been clarified which factors mediated the precession from normality via chronic abdominal pain to IBS in early lifetime.

Psychosocial disorders before adulthood might serve as such factors. In adolescents, a previous article reported that psychosocial stress was significantly associated with reports of IBS-like symptoms in cases with recurrent abdominal pain.22 Meanwhile, in a study evaluating the association between pediatric functional abdominal pain and FGIDs in adulthood, pediatric depression was identified as the predictor of FGID (including IBS) later in life.24 These results implied that abdominal discomfort could develop into adult IBS not in all children, but only those with some certain psychosocial disorders.

Therefore, in this cross-sectional study, we attempt to clarify the prevalence of IBS among Chinese college freshmen and search for potential psychosocial factors associated with high risk of developing IBS in this special period.

Materials and Methods

Participants

All participants in our study were recruited from the freshmen who were about to enroll in the Huazhong University of Science and Technology in Wuhan City. Random cluster sampling method was applied for participant selection. Informed consents were obtained from both the students and university prior to our survey. In August 2017, the included freshmen received the questionnaires in a classroom, and completed the questionnaires voluntarily and anonymously with assistance of special trained doctors. Of the available 2449 recruited freshmen, 2053 students completed the questionnaire (83.8% response rate). Meanwhile, a detailed inquiry into previous medical records was applied for those freshmen suspected of suffering with IBS to exclude organic disease. Suspected or confirmed patients with organic disease were advised to consult physicians. The research protocol was approved by The Ethics Committee of Tongji Medical College, Huazhong University of Science and Technology (IORG No. IORG0003571).

Questionnaires

Demographic information was evaluated such as age, sex (male or female), height, weight, body mass index (BMI), residence (city, town or rural area), education (science & engineering, liberal arts or medicine), and family type (only-child or multi-child, single-parent or two-parent).Then, screening questions was applied to identify IBS patients, such as (1) Did you suffer pain or other discomfort in your abdomen in the last 3 months?; (2) What is the frequency and duration of this pain or discomfort?; (3) Did your stool character abnormally change when you had this pain or discomfort?; and (4) Did your stools frequency abnormally change when you had this pain or discomfort? Freshmen with a positive answer to the first question were further interviewed regarding abdominal symptoms and characters. Information included general characters (ie, age, sex, and BMI), abdominal feelings (pain, bloating or other discomfort) and psychosocial characteristics such as anxiety, depression, suicidal intention and experience of abuse (emotional, physical or sexual) was collected. The questions and options were based on the Rome III diagnostic criteria. Since it has been reported that chronic abdominal discomfort in children is a precursor of IBS in adulthood,2325 this study considered the freshmen with abdominal discomfort of more than 3 months as an unique group with a high risk of developing IBS. Accordingly, the included cases were divided into 3 groups: IBS group (cases met Rome III IBS diagnostic criteria), chronic abdominal discomfort group (cases with abdominal discomforts, more than 3 months but not fit for Rome III IBS diagnosis), and others. Also, the data of psychosocial factors was collected by questionnaires, including depression, anxiety, suicidal intention, and abuse history according to the Rome III Psychosocial Alarm Questionnaire for the FGIDs.

Statistical Methods

Our study expanded previous investigations by stratified analyses of IBS development. Differences in general characteristics according to IBS development among 3 groups were evaluated by ANOVA or the chi-square test. Then, confounders such as sex, age, BMI, major, living area, family, anxiety, depression, experience of abuse, and suicidal intention were adjusted to exclude their intertwined influence on IBS development.

The odds ratios (ORs) of IBS development were calculated by the ordinal logistic regression analysis model with adjusting for sex, age, BMI, major, residual area, and family structure. Multiple logistic regression analysis was also performed, adjusting for mentioned risk factors. SPSS version 17.0 (IBM Corp, Armonk, NY, USA) was applied for statistical analysis. The mean ± SD was evaluated for quantitative variables, while frequencies were applied for qualitative variables. Two-tailed analyses were conducted, and P-value < 0.05 were considered statistically significant in this study.

Results

Subject Characteristics

The overall questionnaire response rate was 83.8%. The mean age of these students was 18.2 ± 0.9 years, and 731 (35.6%) students were female. The mean height, weight, and BMI were 169.5 ± 7.9 cm, 60.7 ± 11.6 kg, and 21.0 ± 3.1 kg/m2, respectively. Nine-hundred fifty-four (46.4%) students came from urban areas, 453 (22.1%) from suburban areas, while others from rural areas. In total, 121 (5.9%) students came from a single-parent family, with the remaining from double-parent households. Also, 1216 (59.3%) freshmen were the only child, while 837 (40.7%) had siblings. The demographic or clinical symptoms of the recruited freshmen are displayed in the Supplementary Table.

Prevalence of Irritable Bowel Syndrome

Of the 2053 college freshmen included in this study, 82 (4.0%) were diagnosed with IBS based on the Rome III criteria, and 176 (8.6%) suffered with chronic abdominal discomfort. More females (49 [59.8%]) than males (33 [40.2%]) were diagnosed as with IBS. The IBS was more common in freshmen with anxiety (P = 0.007), depression (P < 0.001) and experience of abuse (P = 0.001), major of liberal arts (P = 0.012), and suicidal intention (P = 0.001), than those without (Table 1).

Exploratory Analysis for Correlation Between Psychosocial Factors and Irritable Bowel Syndrome Development

Among students with IBS (n = 82), chronic abdominal discomfort (n = 176) and others (n = 1795), ordinal logistic regression analysis showed that female (OR, 3.31; 95% CI, 2.47–4.45; P < 0.001), experience of abuse (OR, 2.44; 95% CI, 1.10–5.56; P = 0.029), and suicidal intention (OR, 2.17; 95% CI, 1.15–4.17; P = 0.017) were independent risk factors to IBS development (Table 2).

In addition, multivariable logistic regression showed that depression was significantly associated with IBS risk compared with the chronic abdominal discomfort group (OR, 5.55; 95% CI, 1.36–22.71; P = 0.017) after being adjusted for other factors (Table 3).

Discussion

Our results showed that the prevalence of IBS in college freshman was 4.0%. Interestingly, it is different from our previous study which reported the prevalence was 15.7% in the same university.9 Although the newer Rome III diagnostic criteria were applied for the current study, this 4.0% IBS prevalence in this study rate is comparable to the 1.2–5.6%1116 estimated for children and adolescence populations, which utilized the original Rome III criteria, but not to the 8.3–29.5% reported for university students.7,10,26 Besides, the prevalence of IBS in Chinese freshmen was also lower than that reported from the Asian Rome III survey of adults.2729 Our results implied that the prevalence of IBS might increase after entering university, and early adulthood might be an IBS susceptible period at least for the well-educated population.

Factors which might affect the increasing prevalence of IBS in freshmen were assessed, and the psychosocial factors were found to contribute to IBS development in college freshmen. Firstly, abuse experience in freshmen, including physical, sexual, and emotional abuse, was associated with increased vulnerability toward IBS. In a previous population-based survey conducted by Talley et al,25 the high risk of IBS was significantly associated with abuse in childhood (OR, 2.02; 95% CI, 1.29–3.15), but not adulthood (OR, 1.39; 95% CI, 0.88–2.19). In addition, another research also showed IBS sufferers experienced more abuse compared with non-IBS populations, and abuse were associated with reports of greater gastrointestinal symptoms; however, the authors contributed such relationship to the concomitant mood disturbances.30 Consistent with previous studies,31 our results showed experience of abuse before adulthood was associated with the development of IBS. But based on these results, psychological distress might not independently contribute to the development of IBS, at least not to the whole span of the development. So, experience of abuse before adulthood could have an independent association with IBS development.

Psychological factors such as depression are common among the children and adults with functional abdominal discomfort and/or IBS.3234 However, it remains unclear whether depression before adulthood could be a significant marker for IBS into early adulthood. Our results showed that on the threshold of adulthood, more severe depression was observed in freshmen with IBS than those with only chronic abdominal discomfort. Similar to our report, in a prospective study of pediatric functional abdominal pain, after controlling for sex, age, follow up duration, baseline severity of abdominal pain, and so on, depression in childhood still significantly predicts FGID (including IBS) in young adulthood.24 Considering the dramatic increase of prevalence in early adulthood, it could be greatly beneficial for the freshmen with chronic abdominal discomfort to receive psychotherapy or antidepressants if necessary to prevent progression of IBS. Besides, current results demonstrated development of IBS could increase the risk for suicidal intention, and this association existed independently of co-morbid depression. This finding, consistent with the analysis of Miller et al35 in IBS patients, implied freshmen with IBS should be explicitly evaluated for possible suicidal behavior and timely interventions should be offered if any suicidal intention be detected.

To our knowledge, this is the first study of IBS prevalence and risk factors among Chinese university freshmen population. Results of this study should be interpreted in light of study limitations. Firstly, the items of questionnaire were limited and some detailed exclusion criteria (eg, other FGID) were not fully assessed. Therefore, the prevalence of IBS had a potential to be overestimated. Also, since our data are cross-sectional, we do not intend to suggest that the results showed the direction of the association of psychosocial factors with IBS. In fact, it remains possible that the factors such as suicidal intention, experience of abuse and depression might increase under influence of IBS. So, at best, this data provides a possible causal relationship which could be confirmed through longitudinal analyses.

In summary, the present study found that the prevalence of IBS in university freshmen was low and similar to that reported for children and adolescence populations by our former researches. There was a significant association between the risk of developing IBS and experience of abuse and suicidal intention. In addition, depression might be connect with high risk of developing IBS in freshmen with chronic abdominal discomfort. An important clinical implication is that early adulthood in university could be a critical period for IBS development, and psychosocial factors such as experience of abuse, suicidal intention, and depression was related with risk of developing IBS.

Supplementary Information
Acknowledgements

We would like to appreciate Mr Zhiqiang Qiu, Mr Xi Yuan, and Mr Qihao Zhao from Huazhong University of Science and Technology for their generous endorsement during the investigation. We also thank Ms Zhen Ouyang, Ms Shan Gao, and Ms Can Chen whose help was invaluable in the completion of this study.

Tables

General Characteristics of Participants According to Irritable Bowel Syndrome Development

Characteristics Non-discomfort group Abdominal discomfort group IBS group P-value
Sex < 0.001
 Females 574 (32.0) 108 (61.4) 49 (59.8)
 Males 1221 (68.0) 68 (38.6) 33 (40.2)
Age (yr) 18.2 ± 0.9 18.1 ± 0.8 18.1 ± 0.6 0.913
BMI (kg/m2) 21.0 ± 3.2 20. 7 ± 2. 9 21.0 ± 2.8 0.052
Education 0.012
 Engineering 1175 (65.5) 103 (58.5) 42 (51.2)
 Liberal arts 125 (7.0) 17 (9.7) 12 (14.6)
 Medicine 495 (27.5) 56 (31.8) 28 (34.1)
Residence 0.655
 City 827 (46.1) 84 (47.7) 43 (52.4)
 Rural area 567 (31.6) 58 (33.0) 21 (25.6)
 Town 401 (22.3) 34 (19.3) 18 (22.0)
Only child 0.594
 Yes 1060 (59.1) 103 (58.5) 53 (64.6)
 No 735 (40.9) 73 (41.5) 29 (35.4)
Single parent 0.235
 No 1695 (94.4) 161 (91.5) 76 (92.7)
 Yes 100 (5.6) 15 (8.5) 6 (7.3)
Anxiety 0.007
 No 1752 (97.6) 171 (97.2) 75 (91.5)
 Yes 43 (2.4) 5 (2.8) 7 (8.5)
Depression < 0.001
 No 1727 (96.2) 172 (97.7) 69 (84.1)
 Yes 68 (3.8) 4 (2.3) 13 (15.9)
Experience of abuse 0.001
 No 1767 (98.4) 174 (98.9) 75 (91.5)
 Yes 28 (1.6) 2 (1.1) 7 (8.5)
Suicidal intention 0.001
 No 1747 (97.3) 169 (96.0) 75 (91.5)
 Yes 48 (2.7) 7 (4.0) 7 (8.5)

IBS, irritable bowel syndrome; BMI, body mass index.

Values were expressed as n (%) or mean ± standard deviation.


Ordinal Logistic Regression Analysis With Risk Factors for Irritable Bowel Syndrome Development

Characteristics Estimate SE WALS P-value OR (95% CI)
Sex
 Females 1.2 0.2 63.8 < 0.001 3.31 (2.47–4.45)
 Males 1
Age (yr) −0.0 0.1 0.1 0.750 0.98 (0.87–1.14)
 BMI (kg/m2) 0.0 0.0 0.0 0.945 1.01 (0.96–1.05)
Education
 Engineering −0.0 0.1 0.0 0.948 0.99 (0.73–1.34)
 Liberal arts 0.1 0.2 0.4 0.540 1.15 (0.72–1.86)
 Medicine 1
Residence
 City 0.1 0.2 0.3 0.569 1.11 (0.78–1.58)
 Rural area 0.2 0.2 1.0 0.301 1.24 (0.83–1.86)
 Town 1
Only child
 Yes 1
 No −0.1 0.2 0.3 0.606 0.92 (0.67–1.26)
Single parent
 No 1
 Yes 0.3 0.2 1.7 0.197 1.39 (0.84–2.32)
Anxiety
 No 1
 Yes 0.2 0.4 0.3 0.599 0.81(0.59–1.23)
Depression
 No 1
 Yes 0.2 0.3 0.5 0.482 1.26 (0.64–2.56)
Experience of abuse
 No 1
 Yes 0.9 0.4 4.7 0.029 2.44 (1.10–5.56)
Suicidal intention
 No 1
 Yes 0.8 0.3 5.7 0.017 2.17 (1.15–4.17)

SE, standard error; WALS, weighted-average least squares; OR, odds ratio; CI, confidence interval; BMI, body mass index.


Multivariate Logistic Regression Analyses for Risk Factors of Irritable Bowel Syndrome

Characteristics β SE WALS P-value OR (95% CI)
Sex
 Females 1
 Males 0.1 0.3 0.1 0.748 1.11 (0.57–2.15)
Age (yr) −0.0 0.2 0.1 0.774 0.94 (0.64–1.39)
BMI (kg/m2) 0.0 0.0 0.6 0.454 1.04 (0.94–1.15)
Education
 Engineering 1
 Liberal arts 0.6 0.5 1.5 0.216 1.79 (0.71–4.52)
 Medicine 0.2 0.3 0.4 0.522 1.23 (0.65–2.35)
Residence
 City 1
 Rural area −0.5 0.4 1.4 0.244 0.62 (0.28–1.38)
 Town −0.0 0.4 0.0 0.896 0.95 (0.44–2.03)
Only child
 Yes 1
 No −0.0 0.4 0.0 0.940 0.97 (0.48–1.97)
Single parent
 No 1
 Yes −0.3 0.6 0.4 0.531 0.70 (0.23–2.11)
Anxiety
 No 1
 Yes 0.0 0.8 0.0 0.989 1.01 (0.21–4.78)
Depression
 No 1
 Yes 1.7 0.8 5.7 0.017 5.55 (1.36–22.71)
Experience of abuse
 No 1
 Yes 1.4 0.9 2.6 0.109 4.22 (0.72–24.50)
Suicidal intention
 No 1
 Yes 0.7 0.6 1.5 0.226 2.05 (0.64–6.52)

SE, standard error; WALS, weighted-average least squares; OR, odds ratio; CI, confidence interval; BMI, body mass index.


Footnotes

Supplementary Material

Note: To access the supplementary table mentioned in this article, visit the online version of Journal of Neurogastroenterology and Motility at http://www.jnmjournal.org/, and at https://doi.org/10.5056/jnm18028.

Financial support: This study was supported in full by the foundation of Key Clinical Construction Projects of Gastroenterology from the National Health and Family Planning Commission of China.

Conflicts of interest: None.

Author contributions: Tao Bai, Xiaohua Hou, and Chen Jiang conceived and designed the study; Tao Bai, Chen Jiang, and Yan Xu performed the data analysis; Chen Jiang and Tao Bai wrote the paper; and Stuti Sharma, Lei Zhang, Huan Wang, Jun Song, Wei Qian, and Xiaohua Hou reviewed and edited the manuscript. All authors read and approved the manuscript.

References
  1. Ballou S, Keefer L. The impact of irritable bowel syndrome on daily functioning: characterizing and understanding daily consequences of IBS. Neurogastroenterol Motil 2017;29:e12982.
    Pubmed KoreaMed CrossRef
  2. Corsetti M, Whorwell P. The global impact of IBS: time to think about IBS-specific models of care?. Therap Adv Gastroenterol 2017;10:727-736.
    Pubmed KoreaMed CrossRef
  3. Mearin F, Cortes X, Mackinnon J, Bertsch J, Fortea J, Tack J. Economic and quality-of-life burden of moderate-to-severe irritable bowel syndrome with constipation (IBS-C) in Spain: the IBIS-C study. Value Health 2014;17:A365.
    Pubmed CrossRef
  4. Böhn L, Störsrud S, Törnblom H, Bengtsson U, Simrén M. Self-reported food-related gastrointestinal symptoms in IBS are common and associated with more severe symptoms and reduced quality of life. Am J Gastroenterol 2013;108:634-641.
    Pubmed CrossRef
  5. Dibonaventura MD, Prior M, Prieto P, Fortea J. Burden of constipation-predominant irritable bowel syndrome (IBS-C) in France, Italy, and the United Kingdom. Clin Exp Gastroenterol 2012;5:203-212.
    Pubmed KoreaMed CrossRef
  6. Jung HK, Kim YH, Park JY, et al. Estimating the burden of irritable bowel syndrome: analysis of a nationwide korean database. J Neurogastroenterol Motil 2014;20:242-252.
    Pubmed KoreaMed CrossRef
  7. Dong YY, Chen FX, Yu YB, et al. A school-based study with Rome III criteria on the prevalence of functional gastrointestinal disorders in Chinese college and university students. PLoS One 2013;8:e54183.
    Pubmed KoreaMed CrossRef
  8. Dong YY, Zuo XL, Li CQ, Yu YB, Zhao QJ, Li YQ. Prevalence of irritable bowel syndrome in Chinese college and university students assessed using Rome III criteria. World J Gastroenterol 2010;16:4221-4226.
    Pubmed KoreaMed CrossRef
  9. Shen L, Kong H, Hou X. Prevalence of irritable bowel syndrome and its relationship with psychological stress status in Chinese university students. J Gastroenterol Hepatol 2009;24:1885-1890.
    Pubmed CrossRef
  10. Wang Y, Jin F, Chi B, et al. Gender differences in irritable bowel syndrome among medical students at inner mongolia medical university, China: a cross-sectional study. Psychol Health Med 2016;21:964-974.
    Pubmed CrossRef
  11. Lu PL, Saps M, Chanis RA, Velasco-Benitez CA. The prevalence of functional gastrointestinal disorders in children in Panama: a school-based study. Acta Paediatr 2016;105:e232-e236.
    Pubmed CrossRef
  12. Lewis ML, Palsson OS, Whitehead WE, van Tilburg MAL. Prevalence of functional gastrointestinal disorders in children and adolescents. J Pediatr 2016;177:39-43, e3.
    Pubmed CrossRef
  13. Xing Z, Hou X, Zhou K, Qin D, Pan W. Impact of parental-rearing styles on irritable bowel syndrome in adolescents: a school-based study. J Gastroenterol Hepatol 2014;29:463-468.
    Pubmed CrossRef
  14. Saps M, Nichols-Vinueza DX, Rosen JM, Velasco-Benitez CA. Prevalence of functional gastrointestinal disorders in Colombian school children. J Pediatr 2014;164:542-545, e1.
    Pubmed CrossRef
  15. Saps M, Adams P, Bonilla S, Chogle A, Nichols-Vinueza D. Parental report of abdominal pain and abdominal pain-related functional gastrointestinal disorders from a community survey. J Pediatr Gastroenterol Nutr 2012;55:707-710.
    Pubmed CrossRef
  16. Devanarayana NM, Mettananda S, Liyanarachchi C, et al. Abdominal pain-predominant functional gastrointestinal diseases in children and adolescents: prevalence, symptomatology, and association with emotional stress. J Pediatr Gastroenterol Nutr 2011;53:659-665.
    Pubmed CrossRef
  17. 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.
    Pubmed CrossRef
  18. Chiou FK, How CH, Ong C. Recurrent abdominal pain in childhood. Singapore Med J 2013;54:195-199.
    Pubmed CrossRef
  19. Singh UK, Prasad R, Verma N. Chronic abdominal pain in children. Indian J Pediatr 2013;80:132-137.
    Pubmed CrossRef
  20. Eminson M, Benjamin S, Shortall A, Woods T, Faragher B. Physical symptoms and illness attitudes in adolescents: an epidemiological study. J Child Psychol Psychiatry 1996;37:519-528.
    Pubmed CrossRef
  21. Walker LS, Guite JW, Duke M, Barnard JA, Greene JW. Recurrent abdominal pain: a potential precursor of irritable bowel syndrome in adolescents and young adults. J Pediatr 1998;132:1010-1015.
    Pubmed CrossRef
  22. Walker LS, Garber J, Van Slyke DA, Greene JW. Long-term health outcomes in patients with recurrent abdominal pain. J Pediatr Psychol 1995;20:233-245.
    Pubmed CrossRef
  23. Howell S, Poulton R, Talley NJ. The natural history of childhood abdominal pain and its association with adult irritable bowel syndrome: birth-cohort study. Am J Gastroenterol 2005;100:2071-2078.
    Pubmed CrossRef
  24. Horst S, Shelby G, Anderson J, et al. Predicting persistence of functional abdominal pain from childhood into young adulthood. Clin Gastroenterol Hepatol 2014;12:2026-2032.
    Pubmed KoreaMed CrossRef
  25. Talley NJ, Boyce PM, Jones M. Is the association between irritable bowel syndrome and abuse explained by neuroticism? A population based study. Gut 1998;42:47-53.
    Pubmed KoreaMed CrossRef
  26. Alaqeel MK, Alowaimer NA, Alonezan AF, Almegbel NY, Alaujan FY. Prevalence of irritable bowel syndrome and its association with anxiety among medical students at king saud bin abdulaziz university for health sciences in Riyadh. Pak J Med Sci 2017;33:33-36.
    Pubmed KoreaMed CrossRef
  27. Chatila R, Merhi M, Hariri E, Sabbah N, Deeb ME. Irritable bowel syndrome: prevalence, risk factors in an adult Lebanese population. BMC Gastroenterol 2017;17:137.
    Pubmed KoreaMed CrossRef
  28. Siah KT, Wong RK, Chan YH, Ho KY, Gwee KA. Prevalence of irritable bowel syndrome in Singapore and its association with dietary, lifestyle, and environmental factors. J Neurogastroenterol Motil 2016;22:670-676.
    Pubmed KoreaMed CrossRef
  29. Xiong LS, Shi Q, Gong XR, Cui Y, Chen MH. The spectra, symptom profiles and overlap of Rome III functional gastrointestinal disorders in a tertiary center in South China. J Dig Dis 2014;15:538-544.
    Pubmed CrossRef
  30. Kanuri N, Cassell B, Bruce SE, et al. The impact of abuse and mood on bowel symptoms and health-related quality of life in irritable bowel syndrome (IBS). Neurogastroenterol Motil 2016;28:1508-1517.
    Pubmed KoreaMed CrossRef
  31. Bradford K, Shih W, Videlock EJ, et al. Association between early adverse life events and irritable bowel syndrome. Clin Gastroenterol Hepatol 2012;10:385390, e1-e3.
    Pubmed KoreaMed CrossRef
  32. Lee C, Doo E, Choi JM, et al. The increased level of depression and anxiety in irritable bowel syndrome patients compared with healthy controls: systematic review and meta-analysis. J Neurogastroenterol Motil 2017;23:349-362.
    Pubmed KoreaMed CrossRef
  33. Lee SK, Yoon DW, Lee S, Kim J, Choi KM, Shin C. The association between irritable bowel syndrome and the coexistence of depression and insomnia. J Psychosom Res 2017;93:1-5.
    Pubmed CrossRef
  34. Farzaneh N, Ghobakhlou M, Moghimi-Dehkordi B, Naderi N, Fadai F. Anxiety and depression in a sample of Iranian patients with irritable bowel syndrome. Iran J Psychiatry Behav Sci 2013;7:30-36.
    Pubmed KoreaMed
  35. Miller V, Hopkins L, Whorwell PJ. Suicidal ideation in patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 2004;2:1064-1068.
    Pubmed CrossRef


This Article

e-submission

Archives

Aims and Scope