Prevalence of irritable bowel syndrome among university students

Journal of Psychosomatic Research 55 (2003) 501 – 505

Prevalence of irritable bowel syndrome among university students The roles of worry, neuroticism, anxiety sensitivity and visceral anxiety Holly Hazlett-Stevensa,*, Michelle G. Craskeb, Emeran A. Mayerc,d,e,f, Lin Changc,d, Bruce D. Naliboff c,f a

Department of Psychology/298, University of Nevada, Reno, NV 89557, USA Department of Psychology, University of California, Los Angeles, CA, USA c CURE Digestive Diseases Research Center/Neuroenteric Disease Program, University of California School of Medicine, Los Angeles, CA, USA d Department of Medicine, University of California School of Medicine, Greater Los Angeles VA Healthcare System, Los Angeles, CA, USA e Department of Physiology, University of California School of Medicine, Greater Los Angeles VA Healthcare System, Los Angeles, CA, USA f Department of Psychiatry and Biobehavioral Sciences, University of California School of Medicine, Greater Los Angeles VA Healthcare System, Los Angeles, CA, USA b

Received 24 August 2001; accepted 26 November 2002

Abstract Objective: Relationships between presence of irritable bowel syndrome (IBS) and generalized anxiety disorder (GAD), chronic worry, neuroticism, anxiety sensitivity and anxiety about visceral sensations were examined among university students. Methods: College student participants were administered self-report diagnostic measures of IBS and GAD, the Penn State Worry Questionnaire (PSWQ), the Neuroticism subscale of the Eysenck Personality Questionnaire, the Anxiety Sensitivity Index (ASI) and five additional items designed to measure visceral anxiety. Results: The prevalence of IBS and its associated characteristics among students were similar to previous community survey studies, with

the exception of lower symptom severity in the university sample. IBS was associated with a higher frequency of GAD and greater worry, neuroticism, anxiety sensitivity and visceral anxiety. Logistic regression analyses further showed that the measure of anxiety specific to visceral sensations was the strongest predictor of IBS diagnostic status. Conclusion: While various aspects of anxiety appear related to IBS, specific anxiety about visceral sensations appears to be the most significant factor. Implications of the associations between anxiety-related variables, particularly anxiety about visceral sensations, are discussed. D 2003 Elsevier Inc. All rights reserved.

Keywords: Anxiety sensitivity; Generalized anxiety disorder; Irritable bowel syndrome; Neuroticism; Worry

Introduction Irritable bowel syndrome (IBS) is a functional gastrointestinal disorder that affects 10 – 20% of the general population at any one time [1,2]. Both in population and in clinical samples, women are almost twice as likely as men to meet diagnostic criteria for IBS in Western countries [3,4]. Several investigations demonstrate a high prevalence of comorbid psychiatric conditions, especially anxiety and mood disorders, among those suffering from IBS [5,6]. Panic disorder and generalized anxiety disorder (GAD), in particular, have been linked to IBS and gastrointestinal * Corresponding author. Tel.: +1-775-784-6828x2050; fax: +1-775327-5043. E-mail address: [email protected] (H. Hazlett-Stevens). 0022-3999/03/$ – see front matter D 2003 Elsevier Inc. All rights reserved. doi:10.1016/S0022-3999(03)00019-9

distress [7– 12]. Consistent with developmental theories of IBS, we have suggested that anxiety about visceral sensations and fear conditioning to visceral interoceptive cues may play a key role in the development of the full syndrome [5]. Investigations of the developmental course of IBS show that symptoms often appear in early adulthood [13] but that children with recurrent abdominal pain may be at a heightened risk for developing IBS especially in response to stress [14]. Despite this hypothesized developmental course of IBS, little is known about the prevalence and nature of IBS in young adults or its association with psychological symptoms such as anxiety. Gick and Thompson [15] demonstrated that undergraduates with IBS reported higher trait anxiety than asymptomatic control students and a 37% prevalence of IBS. Only a single self-report anxiety symptom measure was included. In another study of a small

502

H. Hazlett-Stevens et al. / Journal of Psychosomatic Research 55 (2003) 501–505

sample (n = 127) of college students [16], less than 16% were identified with any bowel disorder and only 6.3% were identified with IBS using Rome I criteria. This small literature therefore provides an uncertain estimate of the prevalence of IBS in young adults and not enough data to evaluate if there is a similar overlap of IBS with anxiety symptoms as found in adults. The purpose of the current study was to explore the prevalence and nature of IBS in a young adult population and to identify relationships between IBS and specific anxiety measures.

Method Participants A total of 1021 university students (331 men, 618 women and 72 unspecified) from three undergraduate psychology classes (n = 569, 322 and 130, respectively) completed the questionnaire packet. While these psychology classes are among the most widely attended of all undergraduate classes, regardless of major area of study, the gender distribution (approximately 65% female) includes a somewhat higher proportion of females than the UCLA undergraduate population as a whole (45% male, 55% female). The three classes did not significantly differ from each other in terms of gender distribution ( P > .3). Data regarding participants’ age were available for the two largest classes, yielding a mean age of 18.83 years (S.D. = 2.22). These two classes did not different in age ( P > .3). Procedure All participants completed a questionnaire packet containing measures of IBS, GAD, worry, neuroticism, anxiety sensitivity and visceral anxiety as part of a larger mass testing procedure during the class period. The contents of the packet varied for each of the three classes but all contained the IBS diagnostic questions. Measures IBS symptoms IBS diagnostic status was determined according to Rome II survey criteria [17]. These criteria include self-report of continuous or repeated lower abdominal discomfort or pain associated with at least two symptoms of defecation relief, change in stool frequency or change in stool consistency over the past 3 months. The first undergraduate psychology class, consisting of 569 students, completed a brief IBS screening measure designed to assess Rome II diagnostic criteria and whether a physician had ever been consulted for those symptoms. The second class, consisting of 322 students, completed a more extensive abdominal symptom questionnaire that included assessment of Rome II diagnostic criteria, symptom severity, typical symptoms and

most bothersome GI-related symptom [18]. The remaining 130 students completed a measure of IBS that allowed for assessment of Rome II diagnostic criteria, symptom severity, most bothersome symptom and whether a physician had ever been consulted for those symptoms. Symptom severity was obtained with a five-point Likert scale in which 1 represented no symptoms, 2 referred to mild symptoms, 3 was moderate severity, 4 represented severe symptoms and lifestyle interference and 5 reflected very severe symptoms that markedly affect one’s lifestyle [18,19]. GAD symptoms The Generalized Anxiety Disorder Questionnaire (GADQ-IV) [20] was completed by 825 participants. The GAD-QIV is based on the original GAD-Q [21], a reliable and valid self-report diagnostic measure of GAD that accurately identifies individuals who meet DSM-IV diagnostic criteria [22] following an extensive diagnostic clinical interview. Recent research has shown that the GAD-Q-IV correctly identified up to 92% of individuals who received a clinical diagnosis of GAD according to DSM-IV criteria from the Anxiety Disorders Interview Schedule-IV [23]. Studies of its specificity demonstrate that that the GAD-Q-IV can reliably distinguish GAD from panic disorder and social phobia [20]. Worry A total of 814 participants completed the Penn State Worry Questionnaire (PSWQ) [24], a widely used measure of general trait worry with strong psychometric properties [24,25]. Neuroticism The personality trait of neuroticism was measured in 438 of the participants with the 24-item subscale of the Eysenck Personality Questionnaire [26]. Anxiety sensitivity The Anxiety Sensitivity Index (ASI) [27] was completed by 447 participants. The ASI is a 16-item reliable and valid index of the tendency to believe that the physical sensations associated with anxiety are harmful, bearing negative physical, social or psychological consequences. Visceral anxiety Specific anxiety of visceral sensations was measured by adding five items to the original ASI that specifically address fears of stomach and bowel sensations. These items were generated by selecting initial phrases of original ASI items (e.g., ‘‘It scares me’’) and changing the ending to describe specific IBS-related gastrointestinal sensations (e.g., ‘‘that my bowel habits are not regular’’) and are listed in Appendix A. Principal components factor analysis with varimax rotation including all 21 items yielded a four-factor solution. Three of these four factors included only the original 16 ASI items. With the exception of one item, all items loading on these three factors were consistent with the

H. Hazlett-Stevens et al. / Journal of Psychosomatic Research 55 (2003) 501–505

structure reported by Zinbarg et al. [28] for the factors labeled Physical Concerns, Mental Incapacitation Concerns and Social Concerns. The fourth factor was only comprised of the additional five visceral anxiety items (all factor loadings >.40), supporting the use of these additional five items as a separate measure.

Results Sample characteristics Approximately 91% of students enrolled in the undergraduate psychology classes involved with mass testing elected to participate. Of the original 1021 participants, 905 (88.6%) fully completed the IBS questionnaire, allowing for determination of IBS diagnostic status. All analyses were therefore limited to this final sample. IBS was detected in 99 of these 905 participants (10.9%). An additional 29 participants (3.2%) endorsed continuous or repeated lower abdominal discomfort or pain for the past 3 months with only one of the associated bowel habit symptoms. These participants reporting partial IBS criteria were eliminated from subsequent analyses. Of the 67 IBS participants who responded to the physician consultation question, 26 (38.8%) reported previously consulting a doctor about their IBS symptoms. Gender information was available for 93 of the IBS participants. While 66 (71%) IBS participants were women, c2 analysis revealed that this gender distribution was not different from the asymptomatic group (64.1% female, P < .19). Bowel habit classification using Rome II criteria was determined for 72 IBS participants: 30 IBS participants (41.7%) were diarrhea predominant, 25 (34.7%) were constipation predominant and 17 (23.6%) did not meet criteria for either classification. The mean reported severity of symptoms for the IBS participants was 2.62 on a 1 – 5 scale (n = 47, S.D. = 0.68), reflecting mild to moderate symptom severity. Finally, IBS participants most often identified their ‘‘most bothersome symptom’’ as irregular bowel habits such as diarrhea or constipation (38.3%), belly pain (23.4%) or sensation of fullness, gas or bloating (14.9%). Relationship to psychological variables GAD diagnostic status was determined by responses to the GAD-Q-IV for 709 participants. Of the 79 IBS participants, 17 (21.5%) also met full diagnostic criteria for GAD compared to only 7% of the participants without IBS. c2 analysis yielded a statistically significant association between IBS and GAD diagnostic status [c2(1) = 18.86, P < .001]. Comparisons between participants with and without IBS were then conducted for PSWQ, Neuroticism, ASI and Visceral Anxiety measures with two-tailed independentsamples t tests. A Bonferroni correction of a < .0125 (.05/4) was used to control for the inflation of Type I error

503

Table 1 Means, standard deviations and sample sizes for self-report measures IBS

No IBS

Measure

M

S.D.

n

M

S.D.

n

PSWQ Neuroticism ASI Visceral Anxiety

53.83 13.40 21.89 5.45

13.58 5.84 10.75 4.27

77 47 47 47

45.84 * 10.22 * 16.36 * 2.40 *

13.84 5.53 9.47 2.74

626 352 355 354

* P < .001.

associated with multiple comparisons. Scores on all four of these measures were higher for the IBS group than for the asymptomatic group [PSWQ: t(701) = 4.79, P < .001; Neuroticism: t(397) = 3.68, P < .001; ASI: t(400) = 3.70, P < .001; Visceral Anxiety: t(51.15) = 4.76, P < .001]. See Table 1 for sample sizes, means and standard deviations. Logistic regression analyses were then conducted to examine the interdependence of these variables in their association with IBS status. Logistic regression analysis, including PSWQ, ASI, Neuroticism and Visceral Anxiety measures, was conducted to predict IBS diagnostic status (n = 267). While this analysis yielded a significant effect [c2(4) = 23.18, P < .001], only the Visceral Anxiety measure significantly predicted IBS status [odds ratio (OR) = 1.32, 95% CI = 1.13 – 1.53, P < .001]. Because all four of these measures were not available for the entire sample, this analysis was repeated including only ASI, Neuroticism and Visceral Anxiety measures to increase sample size (n = 398). This analysis again revealed that only the Visceral Anxiety measure significantly predicted IBS status [odds ratio = 1.26, 95% CI = 1.13– 1.40, P < .001]. Thus, Visceral Anxiety was found to be the most individually related and powerful predictor of IBS among the psychological measures.

Discussion Approximately 11% of this college student sample currently met diagnostic criteria for IBS, falling between the 6.3% reported by Norton et al. [16] and the 37% reported by Gick and Thompson [15] in previous university student investigations. Although the newer Rome II diagnostic criteria were used for the current study, this 11% IBS prevalence rate is comparable to the 13.5% reported for 15 – 34-year-old participants in the U.S. household survey [4], which utilized the original Rome I criteria, and to the 10 – 20% estimated for adult populations [1,2]. Almost 40% of the students suffering from IBS in the current investigation reported consulting a physician for these symptoms. Contrary to our prediction, this rate is quite comparable to the 45.8% found in the general adult population [4] and discrepant from the fewer than 19% previously reported among college students [15]. Our results suggest that factors other than age per se, such as access to health care, sociocultural variables and severity of IBS symptoms, have the most significant impact on health care behaviors. As with

504

H. Hazlett-Stevens et al. / Journal of Psychosomatic Research 55 (2003) 501–505

older samples [29], illness severity may also play a significant role in the consulting behavior of younger populations. However, due to sample size restrictions, we were not able to directly test this hypothesis. The current investigation yielded a greater proportion of women to men in the IBS group compared to the asymptomatic group, but this difference was not statistically significant. A previous study of IBS in college students [15] also failed to find expected gender differences. However, overall samples for both studies included a majority of women. Thus, these studies cannot eliminate sampling bias as a possible cause for lack of a gender effect and therefore do not provide conclusive evidence for a lack of female predominance in younger IBS sufferers. It should be noted that the results are consistent with the U.S. household survey [4], which showed an increase in female but not male frequency of IBS in the 45 or older age group compared to the 15– 34-year-old group. Therefore, several lines of evidence suggest the possibility of increasing female predominance in IBS later in its developmental course. Future young adult survey studies in which both genders are represented equally might address this question. The general profile of most bothersome symptoms and the predominant bowel habits reported by the university sample were similar to the rates reported in population studies of older community and patient samples [13,18]. These results suggest that IBS is not qualitatively dissimilar in older and younger groups. Of perhaps most significance, the results from the psychological measures suggest that the relationships between anxiety disturbance and IBS symptoms seen in clinical populations are also observed in university students. Participants with IBS were more likely to have GAD and reported higher levels of trait worry, anxiety sensitivity and neuroticism than their asymptomatic counterparts. In addition, they reported greater anxiety specific to stomach and bowel visceral sensations, and this measure was the strongest predictor of IBS diagnostic status. Thus, while more general measures of anxiety-related constructs were elevated among IBS individuals, the most direct manifestation of anxiety among this group appears to be anxiety specific to visceral sensations. This observed relationship between visceral anxiety and IBS is similar to that of anxiety sensitivity and panic disorder in which an acquired fear of anxiety-related physiological arousal results in additional anxiety about the recurrence of panic and, in some cases, significant behavioral change [30]. IBS may therefore reflect a vicious cycle of anxious responding in which fears and negative beliefs about gastrointestinal sensations lead to increased anxiety and vigilance toward these bodily sensations. The visceral sensations themselves may then increase as a result of this anxiety, leading to even greater fear and avoidance of gastrointestinal sensations and situations associated with such sensations. Taken together, these results suggest that while predisposing vulnerability factors such as neuroticism and enhanced stress responsiveness contribute to the devel-

opment of anxiety problems, they may also leave an individual prone to anxiety about visceral sensations in particular, thereby increasing IBS risk. In the current study, it is not possible to test the causal nature of the relationship between anxiety and IBS. Additional research utilizing longitudinal designs is needed to establish whether anxiety of visceral sensations plays an etiological role in the development of IBS and is not merely a consequence of IBS symptoms. Several limitations of the study should be discussed. The study population was drawn from a major university in an urban setting and therefore not wholly representative of the general young adult population. Also, the study used a survey form of the Rome criteria that may overdiagnose the disorder due to the shortened time frame. Furthermore, the assessment of visceral-related anxiety, while based on the well-established ASI format, is preliminary. Low reliability or inadequate breadth may partially account for the modest size of the odds ratios for this measure in the logistic regression analyses. Other psychological measures such as depression and PTSD, which were not assessed but are associated with worry, GAD symptoms and anxiety sensitivity, may also influence IBS expression and could be moderators of the relationships seen. Finally, the use of somewhat different measures in the three class samples limited the ability to examine some important relationships among the psychological and symptom variables. In summary, the present study found a significant prevalence of IBS in the university undergraduate population similar to that reported for adult population surveys. There was a significant association of IBS diagnosis with anxietyrelated measures, especially anxiety about visceral sensations. The younger IBS subjects had similar symptom patterns to those reported for adults in terms of most bothersome symptoms and bowel habit predominance. Further study of gender differences, quality of life and consulting behavior in younger IBS samples is needed to follow up on the results reported here.

Appendix A. Visceral anxiety items 1. If I feel a stomach cramp, I worry about finding a bathroom. 2. It scares me that my bowel habits are not regular. 3. I am scared certain foods will upset my stomach. 4. When I am nervous, I am afraid to eat. 5. I worry that I do not completely empty my bowels when I go to the bathroom.

References [1] Talley NJ. Irritable bowel syndrome: definition, diagnosis and epidemiology. Bailliere’s Best Pract Res Clin Gastroenterol 1999;13: 371 – 84.

H. Hazlett-Stevens et al. / Journal of Psychosomatic Research 55 (2003) 501–505 [2] Camilleri M, Choi MG. Review article: irritable bowel syndrome. Aliment Pharmacol Ther 1997;11:3 – 15. [3] Thompson WG, Dotevall G, Drossman DA. Irritable bowel syndrome: guidelines for the diagnosis. Gastroenterol Int 1989;2:92 – 5. [4] Drossman DA, Li Z, Anduzzi E, Temple RD, Talley NJ, Thompson WG, Whitehead WE, Janssens J, Funch-Jensen P, Corazziari E, Richter JE, Koch GG. U.S. householder survey of functional gastrointestinal disorders. Dig Dis Sci 1993;38:1569 – 80. [5] Mayer EA, Craske MG, Naliboff BD. Depression, anxiety, and the gastrointestinal system. J Clin Psychiatry 2001;62:28 – 36. [6] Lydiard RB. Irritable bowel syndrome, anxiety, and depression: what are the links? J Clin Psychiatry 2001;62:38 – 45. [7] Lydiard RB, Greenwald S, Weissman MM, Johnson J, Drossman DA, Ballenger JC. Panic disorder and gastrointestinal symptoms: findings from the NIMH Epidemiologic Catchment Area Project. Am J Psychiatry 1994;151:64 – 70. [8] Tollefson GD, Tollefson SL, Pederson M, Luxenberg M, Dunsmore G. Comorbid irritable bowel syndrome in patients with generalized anxiety and major depression. Ann Clin Psychiatry 1991;3:215 – 22. [9] Lydiard RB. Anxiety and the irritable bowel syndrome. Psychiatr Ann 1992;22:612 – 8. [10] Tollefson GD, Luxenberg M, Valentine R, Dunsmore G, Tollefson SL. An open label trial and alprazolam in comorbid irritable bowel syndrome and generalized anxiety disorder. J Clin Psychiatry 1991;52: 502 – 8. [11] Lydiard RB, Laraia MT, Howell EF, Ballenger JC. Can panic disorder present as irritable bowel syndrome? J Clin Psychiatry 1986;47:470 – 3. [12] Lydiard RB, Falsetti SA. Experience with anxiety and depression treatment studies: implications for designing irritable bowel syndrome clinical trials. Am J Med 1999;107:65S – 73S. [13] Talley NJ, Zinsmeister AR, Melton LJ. Irritable bowel syndrome in a community: symptom subgroups, risk factors, and health care utilization. Am J Epidemiol 1995;142:76 – 83. [14] 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 – 5. [15] Gick ML, Thompson WG. Negative affect and the seeking of medical care in university students with irritable bowel syndrome: a preliminary study. J Psychosom Res 1997;43:535 – 40. [16] Norton GR, Norton PJ, Asmundson GJ, Thompson LA, Larsen DK. Neurotic butterflies in my stomach: the role of anxiety, anxiety sensitivity and depression in functional gastrointestinal disorders. J Psychosom Res 1999;47:233 – 40. [17] Drossman DA, Corazziari E, Talley NJ, Heaton KW, Irvine EJ, Muller-Lissner SA. Functional bowel disorders and functional abdominal pain. In: Drossman DA, Corazziari E, editors. Rome II:

[18]

[19]

[20]

[21]

[22]

[23]

[24]

[25]

[26] [27]

[28]

[29]

[30]

505

the functional gastrointestinal disorders. 2nd ed. London (UK): BMJ Publishing Group, 2000. pp. 351 – 432. Schmulson M, Lee OY, Chang L, Naliboff B, Mayer EA. Symptom differences in moderate to severe IBS patients based on predominant bowel habit. Am J Gastroenterol 1999;94:2929 – 35. Talley NJ, Boyce P, Owen BK, Newman P, Paterson K. Initial validation of a bowel symptom questionnaire and measurement of chronic gastrointestinal symptoms in Australians. Aust N Z J Med 1995;25: 302 – 8. Newman MG, Zuellig AR, Kachin KE, Constantino MJ, Przeworski A, Erickson T, Cashman-McGrath L. Preliminary reliability and validity of the GAD-Q-IV: a revised self-report diagnostic measure of generalized anxiety disorder. Behav Ther 2002;33:215 – 33. Roemer L, Borkovec M, Posa S, Borkovec TD. A self-report diagnostic measure of generalized anxiety disorder. J Behav Ther Exp Psychiatry 1995;26:345 – 50. American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 4th ed. Washington (DC): American Psychiatric Association, 1994. Newman MG, Zuellig AR, Kachin KE, Constantino MJ. The reliability and validity of the GAD-Q-IV: a revised self-report measure of generalized anxiety disorder. Poster presented at the 31st Annual Meeting of the Association for the Advancement of Behavior Therapy, Miami Beach, FL, November 1997. Meyer TJ, Miller ML, Metzger RL, Borkovec TD. Development and validation of the Penn State Worry Questionnaire. Behav Res Ther 1990;28:487 – 95. Molina S, Borkovec TD. The Penn State Worry Questionnaire: psychometric properties and associated characteristics. In: Davey GCL, Tallis F, editors. Worrying: perspectives on theory, assessment, and treatment. New York: Wiley, 1994. pp. 265 – 83. Eysenck H, Eysenck SBG. Eysenck Personality Questionnaire. San Diego (CA): Educational and Industrial Testing Service, 1975. Reiss S, Peterson RA, Gursky DM, McNally RJ. Anxiety sensitivity, anxiety frequency, and the prediction of fearfulness. Behav Res Ther 1986;24:1 – 8. Zinbarg RE, Barlow DH, Brown TA. Hierarchical structure and general factor saturation of the Anxiety Sensitivity Index: evidence and implications. Psychol Assess 1997;9:277 – 84. Talley NJ, Boyce PM, Jones M. Predictors of health care seeking for irritable bowel syndrome: a population based study. Gut 1997;41: 394 – 8. Craske MG, Barlow DH. Panic disorder and agoraphobia. In: Barlow DH, editor. Clinical handbook of psychological disorders: a stepby-step treatment manual. 3rd ed. New York: Guilford Press, 2001. pp. 1 – 59.