Psychosomatics 39:45-54, February 1998
© 1998 The Academy of Psychosomatic Medine
The Relationship Between Irritable Bowel Syndrome and Psychiatric Illness
A Family Study
Catherine L. Woodman, M.D.,
Kevin Breen, M.D.,
Russell Noyes, Jr., M.D.,
Carol Moss, M.A.,
Robert Fagerholm, M.D.,
Stephen J. Yagla, M.S., and
Robert Summers, M.D.
Received September 17, 1996; revised November 5, 1996; accepted January 24, 1997. From the University of Iowa and Veterans Administration, Iowa City, Iowa; the University of Kentucky, Louisville; and the University of Iowa, Iowa City. Address reprint requests to Dr. Woodman, University of Iowa, Department of Psychiatry, 200 Hawkins Drive, Iowa City, IA 52242.
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ABSTRACT
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Although irritable bowel syndrome (IBS) is a common disorder among gastrointestinal clinic outpatients, it continues to be a diagnosis of exclusion. In treatment-seeking populations, IBS has been frequently associated with psychiatric illness, and this co-occurrence has added to controversy about the validity of the IBS diagnosis. This study is a preliminary effort to examine the nature of this relationship by using the family study design. The probands consisted of 20 patients with IBS and 20 patients who had undergone laproscopic cholecystectomy. Their first-degree relatives were interviewed to obtain lifetime diagnoses of functional gastrointestinal and psychiatric syndromes. Significantly more IBS probands had lifetime psychiatric illness than the cholecystectomy probands. The lifetime prevalence of IBS as well as other functional gastrointestinal syndromes was not significantly different between the groups of relatives. However, significantly more relatives of the IBS probands had lifetime psychiatric illness than the relatives of the cholecystectomy probands. Among the relatives with functional gastrointestinal disorders, significantly more had psychiatric illness. This preliminary study provides support for a relationship between IBS and psychiatric illness by the finding of an increased prevalence of psychiatric disorders among the relatives of patients who have IBS.
Key Words: Irritable Bowel Syndrome • Gastrointestinal Disorders
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INTRODUCTION
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Since Da Costa's article in 1871 describing irritable bowel syndrome (IBS), an association between IBS and psychiatric illnesses has been observed in clinical populations, with from 38% to 100% of patients diagnosed as having psychiatric disorders.1–8 As a result of this association, the validity of the diagnosis of IBS has been questioned. There is no one psychiatric disorder that has been linked with IBS, but depression, anxiety, and somatoform disorders have most frequently been diagnosed.9–11 Along these same lines, Chaudhury and Truelove12 observed an association between psychological factors and the onset and/or exacerbation of IBS in over 80% of their cases. These factors included diagnosable psychiatric illness, personality pathology, and environmental stressors. In addition, the patients with IBS in one study have shown heightened symptomatic and physiologic responses to psychosocial stressors.13 Compared with the other medical patients and nonpatients, the individuals with IBS have more often reported stressful life events preceding the onset of illness and hospitalizations.14, 15
The nature of the relationship between irritable bowel and other functional bowel syndromes to psychiatric disorders remains uncertain. Psychiatric disturbance in persons with IBS might represent a reaction to the stress of chronic gastrointestinal illness. This possibility seems to have been excluded by the finding of lesser rates of psychiatric illness among patients with organic gastrointestinal illness (e.g., inflammatory bowel disease).16 Alternatively, IBS might represent an associated feature of various psychiatric syndromes. This has been suggested by a number of investigators and is supported by the finding of high rates of irritable bowel symptoms among persons with anxiety disorders.17–22 It is also possible that the association between IBS and psychiatric disorders observed in clinical populations does not exist in the wider community. Thus, persons with IBS who also have a psychiatric illness may be more likely to seek treatment. Several studies have supported this possibility as well.23–25 The findings from nonpatient populations are not consistent, however, and many studies did not use structured interviews. Clarification of this relationship has important diagnostic and treatment implications and may be sought through community surveys and family studies.
Family studies contribute strongly to the classification of medical conditions, especially when information about etiology is limited, as it is in psychiatry. They are important for validating disease entities and defining diagnostic boundaries. Studies of this kind have established the familial transmission of depressive, anxiety, and somatoform disorders.26–30 There have been no family studies of IBS, but 1 family history study found that 50% of the mothers of children with recurrent abdominal pain had gastrointestinal symptoms that were regarded as functional by their physicians.31 We report what is, to our knowledge, the first family study of IBS. By using a tertiary-care population, we began to investigate the familial transmission of IBS and to examine the relationship between this factor and psychiatric illness. A finding of increased IBS in the relatives of IBS probands, as compared with relatives of control probands, would support the validity of IBS as currently defined. Further, a finding of increased co-occurrence of bowel and psychiatric illness among relatives would support the existence of a relationship between the two.
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METHODS
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Probands
Our study was conducted in 1994. Probands were recruited from the University of Iowa Center for Digestive Diseases. All new clinic patients between the ages of 30 and 60 years who had been diagnosed with IBS in 1 calendar year were asked to participate, until 20 probands were recruited. Patients who were new to the clinic were recruited to decrease the biases of more severe illness and more unusual illness patterns that can be seen in long-term tertiary-care patients. The potential probands were told that we were interested in them regardless of whether they thought their family members had gastrointestinal disorders. Patients were excluded if they had psychoses, dementia, or mental retardation. Patients who had coexisting medical illnesses that were not considered well-controlled were also excluded. The potential subjects were contacted first by letter and then by telephone at least 1 year after their index visit. Randomly selected subjects were screened by telephone, and those that initially qualified and were agreeable were interviewed.
Prospective IBS proband charts were reviewed by one of the authors (CLW). Exclusion criteria included 1) red or white blood cells in the stool; 2) elevation of body temperature >100°F; 3) a history of seizure disorder or uncontrolled endocrine, hematologic, or neurologic disorder; 4) a history of abuse of laxatives or antidiarrheal agents; and 5) other known gastrointestinal pathology. Patients were excluded who had significant pathology on 1) physical examination, 2) prior sigmoidoscopy, and 3) lactose tolerance test. Any proband whose workup for IBS did not include the above was considered eligible for the study. The probands with IBS were required to meet the criteria proposed by Manning32 (Table 1). The diagnosis was confirmed by using the Functional Bowel Syndrome Questionnaire at the time of the interview.33
Twenty control probands were obtained from the same clinic. They had undergone laproscopic cholecystectomy in the same calendar year and were matched for gender and age within 5 years. Laproscopic cholecystectomy patients were chosen as a control group because they had known gastrointestinal pathology. Inflammatory bowel disease (IBD) patients have served as a control group in prior studies of IBS, but they were not a suitable control group for a family study. The prodrome of IBD is insidious, and the diseases are heritable, so relatives in the early stages of IBD could be mistakenly diagnosed with a functional bowel disorder.16, 34
The control probands had undergone laproscopic cholecystectomy after ultrasound evidence of cholelithiasis had been found. The presence of stones was confirmed at cholecystectomy. The charts of prospective control probands were reviewed by one of the authors (CLW). Exclusion criteria included 1) biliary tract symptoms >3 months postcholecystectomy; 2) a history of IBS or other known gastrointestinal pathology; 3) a history of lactose intolerance; 4) a history of seizures or uncontrolled endocrine, hematologic, or neurologic disease; and 5) a history of abuse of laxatives or antidiarrheals. Significant abnormalities on physical examination were also grounds for exclusion.
Instruments
The Structured Clinical Interview for DSM-III-R , nonpatient version (SCID-NP), was used to obtain lifetime psychiatric diagnoses.35 The Family Informant Schedule and Criteria (FISC) was used to obtain family history of psychiatric illness, and a family informant gastrointestinal-disease questionnaire developed for this study was used to obtain a family history of IBS.36 The Functional Bowel Syndrome Questionnaire was used to identify gastrointestinal disorders.2 This instrument was developed to diagnose current functional bowel disorders, as defined by the Rome convention.33 The instrument was modified to obtain lifetime diagnoses, but the criteria of 3 months continuous illness was retained. The instrument allows for threshold and subthreshold diagnoses to be made. The reliability and validity of the original instrument were examined,33 but not those of the modified version. A digestive-disease questionnaire, a 17-item list of common gastrointestinal disorders, was used to obtain a history of current and past gastrointestinal disorders. In cases where there was a positive response, a history was gathered about how the diagnosis was reached, and, where possible, medical records were obtained and reviewed by a gastroenterologist (RS). In addition, a brief medical history was obtained by using a structured interview developed for this study. This interview included an assessment of health care utilization, including information about hospitalizations, medications, and physicians seen in the year prior to interview.
The Brief Symptom Inventory, a 53-item self-rated instrument with 9 subscales, was used to assess psychological and somatic symptoms.37 The Whitely Index, a 14-item self-rated instrument with 3 subscales, was used to measure hypochondriasis.38
Procedures
The probands who met the earlier described criteria and provided informed consent were interviewed in person by one of the authors (KB or RF) who used the SCID-NP to obtain lifetime and current psychiatric diagnoses for each proband.35 The interviewers had been trained in the use of this instrument. Through our use of the FISC,36 the probands provided information about psychiatric and gastrointestinal disorders in their first-degree relatives.
All first-degree relatives were contacted about participating in the study, first by mail and then by telephone. Those relatives living within a 150-mile radius were interviewed personally, and those who lived further away were interviewed by phone. The interviews of all relatives were done by a single investigator (CM) who was blind to proband status. This interviewer had a masters' degree, with training and experience in psychiatric interviewing. The instruments administered include the SCID-NP, the Functional Bowel Syndrome Questionnaire, the Brief Symptom Inventory, and the Whitely Index. The interviews were 1–2 hours in length, and the questionnaires were returned by self-addressed and stamped mailer. A clinical narrative was recorded for each interview, which included history of present and past psychiatric and gastrointestinal illnesses, with particular attention paid to the temporal relationship between them. Medical records were obtained when indicated by using standard release-of-information forms.
The data for each first-degree relative, including the clinical narrative, SCID-NP and FISC information, and medical records, were independently reviewed by two investigators (RN and CLW) who were also blind to the proband status to achieve a best-estimate diagnosis. All records of the relatives with bowel symptoms were reviewed by a gastroenterologist (RS). Disagreements about diagnosis were resolved by consensus.
Analyses
Differences between the IBS and the control relatives were examined by using Students' t-test for continuous variables and chi-square or, where applicable, Fisher's exact test for categorical variables. The variables examined included IBS, functional gastrointestinal disorders, psychiatric disorders, and demographic variables. Because of the study's exploratory nature, we have indicated P-values of <0.05 for descriptive and comparative purposes.
A sample size of 20 probands for each group was chosen based on the limited data available to us. One family history study found functional bowel disorders in 50% of the mothers. If IBS were to occur in 1 family member in 50% of families, in 20 families in each group we would be able to detect a 35% difference between the IBS families and control families with 0.80 power by using Fisher's exact test of association at the 0.05 significance level (two-tailed). Family studies of psychiatric disorders done at the University of Iowa that used 20 probands have found statistically significant differences between the first-degree relatives of probands and control subjects.
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RESULTS
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We found that 128 gastroenterology patients who had IBS and 73 more who had undergone laproscopic cholecystectomy remained eligible for study after chart review. Letters were then sent to randomly selected patients inviting them to participate. Sixty-two patients with IBS were contacted, and 27 patients were interviewed to obtain 20 probands. Seven patients who were interviewed did not meet criteria for current IBS; therefore, they were eliminated from further consideration. Forty-four cholecystectomy patients were contacted, and 21 were interviewed to obtain 20 control probands. One of the cholecystectomy patients who was interviewed met criteria for IBS. The rate of refusal was not significantly different between the groups (56% vs. 53%), and no differences were noted in the reasons for refusal.
The probands did not differ significantly on demographic parameters (Table 2). The groups that had been matched for age and gender were comparable with respect to marital status, occupational class, and educational level (Hollingshead Two-Factor Index of Social Position). All probands were Caucasian. By study design, the IBS probands had current IBS with no other known gastrointestinal disorders. The control probands had cholelithiasis with amelioration of symptoms postsurgery and no other known gastrointestinal pathology.
The IBS probands had a greater frequency of lifetime psychiatric disorders than the control probands (Table 3). These probands had significantly more mood disorders (70% vs. 25%, P=0.004); anxiety disorders (50% vs. 20%, P=0.01); and somatoform disorders (35% vs. 0%, P=0.003). The IBS probands had significantly more lifetime substance use disorders than the control probands (35% vs. 0%, P=0.003). No proband had a current diagnosis of substance abuse at the time of interview. The IBS probands had more Axis I diagnoses than did the control probands (mean=2.8 vs. 0.6).
The IBS probands had 99 first-degree relatives. The mean±standard deviation (SD) age of these relatives was 45.2±17.4 years, and 56% were women. Personal interviews were completed on 46.9%, 23.5% refused, 14.3% were deceased, 14.3% were not located, and 1 relative could not be interviewed because of severe dementia. There were 112 relatives of control probands. The mean±SD age of these relatives was 42.9±17.1 years, and 51% were female. Personal interviews were completed on 67.5%, 13.5% refused, 14.4% were deceased, 3.6% were not located, and 1 relative could not be interviewed because of severe dementia. The two groups did not differ significantly in terms of age, gender, marital status, or occupational class. The interviewed control relatives had achieved a higher educational level than the IBS relatives (3.91 vs. 3.32,  2=16.25, df=5, P<0.01, Hollingshead Two-Factor Index of Social Position). Among all relatives, 41% were interviewed in person and 16% by telephone. Among the living relatives, more women than men agreed to be interviewed (64% vs. 52%, NS).
The frequencies of lifetime functional bowel disorders among the interviewed relatives are shown in Table 4. There was no significant difference in the frequency of IBS between the irritable bowel and control relatives (2.1% vs. 1.3%, NS). When subthreshold cases of IBS were included, there was still no significant difference between the groups (14.6% vs. 8%, NS). When frequencies of threshold and subthreshold IBS for all relatives were compared (based on family history data for those relatives not interviewed), the results were again similar.
When the first-degree relatives diagnosed with any functional lower gastrointestinal disorder (including IBS, functional constipation, functional diarrhea, unspecified functional bowel disease, functional abdominal pain, and functional biliary disease) were examined, a trend toward more lower gastrointestinal disorders was found in the IBS relatives (27.0% vs. 16.0%, P=0.10). When functional upper gastrointestinal disorders (globus, rumination syndrome, functional chest pain, functional heartburn, functional dyspepsia, aerophagia) were evaluated, the difference between the IBS relatives and control relatives did not achieve significance (17.0% vs. 9.3%, NS). Finally, when IBS relatives with any functional gastrointestinal disorder (upper and lower gastrointestinal disorders) were combined, there was again no significant difference between the groups (33% vs. 22%, NS). There was also no difference in the number of relatives with 1 or more organic gastrointestinal disorders between groups (59.6% vs. 49.3%, NS).
The frequencies of lifetime psychiatric diagnoses among the interviewed relatives are shown in Table 5. More relatives of the IBS probands had mood disorders (33.3% vs. 17.0%, P=0.04) and anxiety disorders (41.7% vs. 18.7%, P=0.005) than did those of the control probands. When anxiety disorders were examined individually, a significantly greater proportion of the IBS relatives had generalized anxiety disorder than the control relatives (14.9% vs. 4.3%, P=0.05). In addition, there was a trend toward greater frequency of panic disorder (15.0% vs. 5.0%, P=0.07 ) and social phobia (30.0% vs. 10.0%, P=0.07 ) among the IBS relatives. The incidence of obsessive-compulsive disorder was not different between the groups (2.1% vs. 1.8%, NS). There was a trend toward a greater frequency of substance use disorders (18.8% vs. 32.0%, P=0.09) among the control compared with the IBS relatives. When the frequencies of diagnoses for all relatives were compared, using family history data for the relatives not interviewed, the results were similar.
Scores on measures of psychological and somatic symptoms obtained from interviewed relatives are shown in Table 6. The relatives of the IBS probands scored significantly higher on the depression and anxiety subscales of the Brief Symptom Inventory than did the relatives of the control probands. There were no differences between the groups with respect to extroversion (8.4±5.3 vs. 7.5±5.4, NS) and neuroticism (3.9±2.6 vs. 3.6±1.7, NS). Likewise, there was no difference between groups on the Whitely Index (20.6±5.9 vs. 20.6±6.2, NS).
The two groups of relatives were similar with respect to the observed relationship between bowel and psychiatric syndromes, so interviewed relatives were combined for further examination of this phenomenon. Seventy-three percent of the relatives who had functional gastrointestinal disorders also had a psychiatric illness, compared with 32% of the relatives without functional gastrointestinal disorders. As shown in Table 7, the relatives with functional bowel disorders were more likely to have depressive and anxiety disorders than the relatives with no bowel disorders. There was no statistically significant difference in the proportion who had lifetime psychiatric disorders between the relatives with functional lower gastrointestinal disorders and the relatives with functional upper gastrointestinal disorders. With respect to temporal relationship, 37% developed a psychiatric disorder first, 33% developed a gastrointestinal disorder first, and 30% developed the disorders concurrently.
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DISCUSSION
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This preliminary study found no increase in IBS, as it is currently defined, among the relatives of patients with this disturbance. There was no increase in the lifetime prevalence of IBS, whether broadly or narrowly defined, in the relatives of IBS probands, compared with the relatives of the control probands. In fact, the rates of IBS among the IBS relatives are comparable with those observed in the community.17 These findings are contrary to previous evidence, although, to our knowledge, no family study, using strict criteria for IBS and personal, structured interviews of first-degree relatives, had previously been done. The findings need to be interpreted cautiously because of our small sample. Indeed, the frequency of all functional lower gastrointestinal disorders combined was higher in the IBS relatives than in the control relatives. However, for this factor to reach statistical significance with 80% power, 236 relatives in each group would have been required.
The probands with IBS had an increased lifetime prevalence of psychiatric disorders compared with the control probands. Ninety percent of the IBS probands had 1 or more psychiatric disorders—mostly depressive and anxiety disorders—compared with 40% of the cholecystectomy probands obtained from the same gastroenterology clinic. This finding confirms what other studies of clinical IBS populations have found and is at the upper end of the reported range (38%–100%).3 The lifetime prevalence of depressive disorders, anxiety disorders, and somatoform disorders is also consistent with older and more recent studies that have used diagnostic criteria and structured interviews.16, 34, 39 The IBS probands were recruited from a tertiary-care center, which may account for the high rate of comorbid psychiatric disorders. Such centers attract more severe, treatment-resistant patients, and if there were a genetic component to IBS, one would expect it to be manifested in the families of such probands.
The relatives of probands with IBS had an increased frequency of lifetime psychiatric illness compared with the relatives of control probands. This increase is similar to that observed in families of patients with anxiety and depressive disorders.27–29, 40 The psychiatric disorders associated with IBS appear to be familial. They are, therefore, unlikely to be reactions to bowel disorders in these relatives. What is not ruled out is the possibility that the psychiatric disorders in our irritable bowel probands contributed to their decision to seek treatment for their bowel disorder. Consistent with the latter possibility, a number of studies have found increased utilization of health care by persons with psychiatric illness, especially patients with panic disorder and major depression.41 We have not, in this preliminary study, excluded the possibility that in the probands, the link between bowel disorders and psychiatric disorders reflects treatment-seeking bias. A study based on probands identified in the community would eliminate such a potential bias.
Among all relatives (the IBS and control relatives combined), we observed an association between gastrointestinal and psychiatric disturbances. More relatives with functional bowel disorders had lifetime psychiatric disorders than the relatives without bowel disorders (73% vs. 31%, P<0.001). Conversely, more relatives with lifetime psychiatric illnesses had functional bowel disorders than did relatives without psychiatric illness (73% vs. 32%, P<0.001). The two disorders appeared to be linked whichever way the association was examined. This association between disorders suggests that they may be transmitted together and may represent features of a single disturbance. This study does not address what it is that may be transmitted or the contribution of heredity and/or environment to disease expression.
Among the relatives with coexisting disturbances, the psychiatric disorders occurred prior to or concurrent with the onset of IBS in two-thirds of cases, lending some support to the hypothesis that functional gastrointestinal disturbances may be secondary manifestations of psychiatric illness. This temporal relationship is similar to that found in clinical populations, where psychiatric disorders tend to develop before or coincide with the onset of gastrointestinal disorders.16 Of course, the lifetime history of both bowel and psychiatric disorders was obtained retrospectively, and this method may be less reliable than prospectively gathered data. Consequently, this finding should be interpreted cautiously. Nevertheless, it is certainly conceivable that the physiological abnormalities that accompany psychiatric disorders might contribute to the altered gastrointestinal function.
There are a number of study limitations. The first is small sample size. As noted earlier, we run the risk of failing to find differences that exist if our sample is not large enough. However, the probands in this study had relatively severe illnesses, and, for this reason, we were more likely to find a familial transmission if it were present. Second was a high refusal rate among potentially eligible probands. We attempted to minimize bias in the recruitment of subjects, but those who refused may have differed from those who took part. A third possible limitation has to do with the reliability of the diagnosis of IBS. We made lifetime diagnoses without physical or laboratory examination. Even the Manning criteria have not been examined with respect to reliability, despite their wide acceptance.32, 33 To lessen the possible impact of these criteria, we also defined IBS broadly. While doing so did not change the results, there was a trend toward increased familial aggregation as a result.
This study supports a relationship between psychiatric disorders and functional bowel disorders based on an increased prevalence of psychiatric illness among the relatives of the IBS probands. The broader the definition of bowel disorders, the stronger the association becomes. Continued exploration of the relationship between IBS and psychiatric illness is needed. An epidemiologic study, using a large community-acquired sample, may be the next logical step. A study of this design would address two limitations of this study. An epidemiologic study would eliminate selection bias that may operate in a tertiary-care population. It would also determine whether an association between psychiatric disorders and IBS exists in the community. If an association between IBS and psychiatric disorders is found in the community, future studies need to address the contribution that environment may make to the expression of both functional bowel disorders and psychiatric disorders (e.g., early childhood environment, physical and sexual abuse, separation from a parent). Further efforts are needed to validate the current diagnostic criteria for IBS, including follow-up studies and diagnostic boundary studies. Follow-up studies can demonstrate the stability of a disorder over time, studies of subthreshold vs. threshold patients can establish the boundary for the diagnosis of an illness, and both can contribute to establishing the independent status of a disorder.
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A. J. Gelenberg, R. B. Lydiard, R. L. Rudolph, L. Aguiar, J. T. Haskins, and E. Salinas
Efficacy of Venlafaxine Extended-Release Capsules in Nondepressed Outpatients With Generalized Anxiety Disorder: A 6-Month Randomized Controlled Trial
JAMA,
June 21, 2000;
283(23):
3082 - 3088.
[Abstract]
[Full Text]
[PDF]
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P. Burke, M. Elliott, and R. Fleissner
Irritable Bowel Syndrome and Recurrent Abdominal Pain: A Comparative Review
Psychosomatics,
August 1, 1999;
40(4):
277 - 285.
[Abstract]
[Full Text]
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ABSTRACT
INTRODUCTION
