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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 39  |  Issue : 3  |  Page : 140-149

A study of psychiatric comorbidities in irritable bowel syndrome


Department of Psychiatry, Faculty of Medicine, Benha University, Benha, Egypt

Date of Submission10-May-2018
Date of Acceptance12-Jun-2018
Date of Web Publication11-Oct-2018

Correspondence Address:
Shewikar T El-Bakry
Department of Psychiatry, Faculty of Medicine, Benha University, Benha
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ejpsy.ejpsy_9_18

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  Abstract 


Background Irretable bowel syndrome (IBS) is a functional syndrome characterized by chronic abdominal pain accompanied by altered bowel habits. Stress often worsens the symptoms of patients with IBS. Psychiatric disorders and IBS appear to have bidirectional comorbidities.
Objectives The aim of this study was to assess the psychiatric comorbidities in patients with IBS.
Patients and methods The study included a total number of 150 patients complaining of IBS symptoms with at least one episode of abdominal pain or flatulence per week in association with a change in bowel habit. All patients in the study were subjected to a detailed history taking and complete general and local abdominal examination. Moreover, International Classification of Diseases-10th revision internal medicine criteria for diagnosis, International Classification of Diseases-10th revision symptom checklist for mental disorders, and social readjustment rating scale were estimated.
Results Patients of all age groups visit the clinics when they complain from IBS, mostly those of ages ranging from 31 to 40 years, who represented 38% of the studied group. Females complained more than males (66 and 34%). The most frequent psychiatric comorbidity with IBS was the neurotic and behavioral syndromes (53.3%) followed by psychotic and affective syndromes (32%), then the organic mental and psychoactive substance use syndrome (8%), and lastly, the personality disorders (4%). There was a significant association between IBS type and depression, generalized anxiety disorder (GAD), panic disorder, obsessive compulsive disorder (OCD), and somatization. Moreover, there was a significant correlation between IBS type and bipolar disorder, depression, GAD, panic disorder, OCD, somatization, and nonorganic sleep disorder.
Conclusion Most patients with IBS have associated psychiatric or somatic comorbidities or overlapping other functional gastrointenstinal disorder (FGIDs). Patients with IBS have significantly higher levels of psychiatric comorbidities than healthy ones and are more susceptible to stress-related disorders.

Keywords: irritable bowel syndrome, psychiatric comorbidities, psychiatric disorders


How to cite this article:
Michael VS, El Hamady MM, El-Bakry ST, Awd MM. A study of psychiatric comorbidities in irritable bowel syndrome. Egypt J Psychiatr 2018;39:140-9

How to cite this URL:
Michael VS, El Hamady MM, El-Bakry ST, Awd MM. A study of psychiatric comorbidities in irritable bowel syndrome. Egypt J Psychiatr [serial online] 2018 [cited 2024 Mar 29];39:140-9. Available from: https://new.ejpsy.eg.net//text.asp?2018/39/3/140/243032




  Introduction Top


Irretable bowel syndrome (IBS) or spastic colon is a symptom-based diagnosis. It is characterized by chronic abdominal pain, discomfort, bloating, and alteration of bowel habits. Onset of IBS is more likely to occur after an infection (IBS-postinfectious), or a stressful life event, but varies little with age. The most common theory is that IBS is a disorder of the interaction between the brain and the gastrointestinal (GI) tract. For at least some individuals, abnormalities in the gut flora occur, and it has been theorized that these abnormalities result in inflammation and altered bowel function (Khanna and Tosh, 2014).

The interaction between psychiatric disorders and IBS should not be ignored when developing strategies for screening and treatment. The simultaneous presence of a mental disorder and IBS worsens the prognosis of both diseases involved to a significantly greater extent (Stanculete, 2017).

van Tilburg et al. (2013) identified the most important psychological factors predicting IBS symptom severity and investigated how these psychological variables are related to each other. Although cause and effect cannot be determined, they suggested that the most fruitful approach to curb negative effects of psychological factors on IBS is to reduce catastrophizing and somatization.

IBS is a chronic functional gut disorder that affects ∼8–10% of the population in western countries, mainly young and middle aged women. Although IBS, as with other functional gut disorders, is a benign disorder with a good long-term prognosis, it has an important effect on a patient’s quality of life. IBS also produces a significant economic burden owing to both direct health care-related costs and indirect costs because of impaired work productivity. In fact, IBS has been proposed as the second leading cause of absenteeism after the common cold (Lovell and Ford, 2012).

Ortiz Lucas et al. (2010) have suggested an alteration in the immune system cell profile of patients with IBS and a close relationship between the immune and nervous systems. Furthermore, Kajander et al. (2008) have studied the relationship between probiotic intake and blood cytokine levels and changes in fecal microbita.

The aim of this study is to examine the psychiatric comorbidities in patients with IBS, to throw light on correlation between IBS subtypes and psychiatric disorders, and to study stress-related exacerbation of IBS symptoms.


  Patients and methods Top


This cross-sectional study was conducted in the Outpatient Clinics of Internal Medicine at Benha Teaching Hospital in Benha City, Qaliobya Governorate, Egypt. A formal consent was taken from the patients it was explained to them that their privacy is preserved and they can terminate the procedure at any time without any consequences and they have the right to know the right of the research. The study followed the ethical protocol of Benha University.

It included a total number of 150 patients complaining of IBS symptoms with at least one episode of abdominal pain or flatulence per week in association with a change in bowel habit.

Inclusion criteria

This study had the following inclusion criteria:
  1. Both male and female patients more than or equal to 18 years of age.
  2. Patients having recurrent IBS symptoms at least once a week, diagnosed by International Classification of Disease-10th revision (ICD-10) internal medicine.


Exclusion criteria

The following were the exclusion criteria:
  1. Patients less than 18 years.
  2. Patients not fulfilling criteria of ICD-10 internal medicine for IBS.
  3. Patients having any chronic medical or endocrinal condition.
  4. Patients having inflammatory bowel diseases proved by colonoscopy.
  5. Patients having any functional GI disorder (e.g. Gastroesophageal reflux disease, GERD).
  6. Patients with recent GI operation.
  7. Any inflammation, infection, heart diseases, and renal diseases.
  8. Patients with a diagnosed psychiatric disorder or receiving treatment for it.


Tools

All patients in the study were subjected to the following:
  1. A semistructured interview empathizing the demographic data such as age, sex and past history, and medical history. Review of drug history to exclude any drug that may affect GI motility.
  2. Complete general examination.
  3. Local abdominal examination.
    1. ICD-10 internal medicine criteria for diagnoses for IBS.
    2. ICD-10 symptom checklist for mental disorders.
    3. Social readjustment rating scale (Okashaet al., 1981). It is a 43-item scale measuring the susceptibility to develop stress-related disorders.


Statistical analysis

Data were entered, checked, and analyzed using Epi-Info, version 6, and Dean, 2016 SPSS Windows version 21.

Data were summarized using correlation study and χ2-test.

The threshold of significance is fixed at 5% level (P value).

The results were considered:
  1. Significant when the probability of error is less than 5% (P<0.05).
  2. Nonsignificant when the probability of error is more than 5% (P>0.05).
  3. Highly significant when the probability of error is less than 0.1% (P<0.001).


The smaller the P value obtained, the more significant are the results.


  Results Top


[Table 1] reveals that the highest percent of patients were in the range of 31–40 (38%) years of age, to a lesser extent were patients ranging from 18 to 30 (36%) years of age, patients ranging from 41 to 50 years represented 18%, patients ranging from 51 to 60 years of age represented 5.3%, and patients above 60 years represented 2.7%.
  1. Regarding sex, 34% were males and 66% were females.
  2. According to the level of education, 12% were illiterate, 30.7% had only primary certificate, 40% had high school certificate, and 17.3% were university graduate.
  3. Concerning occupation, 33.3% of the patients were working, 53.4% were not working (this percent includes house wives), and 13.3% stopped working owing to the illness.
  4. The married patients represented 77.33%, and the singles, the divorced, and widows represented 9.3, 6, and 7.33%, respectively.
Table 1 Distribution of patients with irritable bowel syndrome according to their sociodemographic characteristics

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[Table 2] shows that the highest percent of patients had mixed type of IBS (58.7%), patients with constipation type were 24%, and patients with diarrhea type were 17.3%. Of all patients with IBS, only 37.3% did not have psychiatric comorbidities and 62.7% had a psychiatric comorbidity. Of patients with IBS having psychiatric comorbidity, 17.3% were type C, 9.4% were type D, and 36% were type M.
Table 2 Irritable bowel syndrome types and psychiatric comorbidity

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[Table 3] illustrates the psychiatric comorbidity with IBS according to ICD-10 symptom checklist, where 8% of patients are in group I (organic mental and psychoactive substance use syndromes), 32% are in group II (psychotic and affective syndromes), 53.3% are in group III (neurotic and behavioral syndromes), and 4% are in group IV (personality disorders).
Table 3 Psychiatric comorbidity in irritable bowel syndrome according to International Classification of Diseases-10th revision symptom checklist

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From [Table 4], it can be deduced that there were no patients with organic mental, whereas psychoactive substance use patients were divided into alcohol use patients (6.38%) and cannabinoids use patients (6.38%).
Table 4 Organic mental and psychoactive substance use syndromes in irritable bowel syndrome according to International Classification of Diseases-10th revision symptom checklist

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[Table 5] shows that 17% of patients with psychiatric comorbidity had schizophrenia, 2.1% had bipolar affective disorder, and 31.9% had depression.
Table 5 Psychotic and affective syndromes in irritable bowel syndrome according to International Classification of Diseases-10th revision symptom checklist

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[Table 6] shows that according to ICD-10 symptom checklist, this group is divided into neurotic and behavioral syndromes. Neurotic syndromes include generalized anxiety disorder (GAD) (35.4%), panic disorder (27.7%), obsessive compulsive disorder (OCD) (6.35%), somatization (39.5%), conversion (0%), and post traumatic stress disorder (PTSD) (4.25%). Behavioral syndromes include anorexia nervosa (4.25%), bulimia nervosa (0%), nonorganic sleep disorder (8.5%), and nonorganic sexual dysfunction (4.25%).
Table 6 Neurotic and behavioral syndromes in irritable bowel syndrome according to International Classification of Diseases-10th revision symptom checklist

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According to ICD-10 symptom checklist, [Table 7] proves that 4.25% had obsessive personality, and the ones with an anxious personality accounted for 2.13%.
Table 7 Personality disorders in irritable bowel syndrome according to International Classification of Diseases-10th revision symptom checklist

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Using the social readjustment rating scale, the severity of being prone to stressful situations was assessed. It is divided into three main categories (mild, moderate, and severe), and each of these categories is then divided according to IBS type into C, D, and M. The risk for developing stress-related disorders was severe among the patients with schizophrenia with mixed type of IBS (six), patients with depression and mixed type IBS (15), patients with both GAD and mixed type IBS (14), and those with somatization and mixed IBS (16), and also a moderate risk was found in patients with both somatization and mixed IBS (seven) ([Table 8]).
Table 8 Distribution of psychiatric comorbidity according to irritable bowel syndrome type and the risk for developing stress-related disorders

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There is a statistically significant association between IBS type and the following psychiatric comorbidities: depression, GAD, panic disorder, OCD, and somatization. A significant correlation was also determined between the types of IBS and bipolar disorder, depression, GAD, panic, disorder, OCD, somatization, and nonorganic sleep disorder ([Table 9]).
Table 9 Test statistics of irritable bowel syndrome type and psychiatric comorbidity

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[Table 10] shows that there is no statistically significant association nor correlation between IBS type and nonpsychiatric patients.
Table 10 Test statistics of irritable bowel syndrome type without psychiatric comorbidity

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There is a statistically significant association and correlation between the severity of susceptibility to develop a stress-related disorder and the following psychiatric comorbidities: depression, GAD, panic disorder, somatization, PTSD, and nonorganic sleep disorder ([Table 11]).
Table 11 Test statistics of susceptibility for developing stress-related disorder in patients with irritable bowel syndrome with psychiatric comorbidity

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[Table 12] shows that there is no statistical significant association between severity to stress-related conditions and nonpsychiatric patients with IBS.
Table 12 Test statistics of susceptibility for developing stress-related disorder in patients with irritable bowel syndrome without psychiatric comorbidity

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From [Table 13], it was noted that sex has a statistically significant correlation with alcohol abuse, cannabinoids, schizophrenia, depression, and nonorganic sexual dysfunction. Regarding age, it has a statistically significant correlation with depression, nonorganic sleep disorder, and nonorganic sexual dysfunction.
Table 13 Correlation matrix

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We also noted that in marital status, there was a statistically significant correlation with schizophrenia, depression, GAD, panic disorder, somatization, anorexia nervosa, nonorganic sleep disorder, and nonorganic sexual dysfunction. Occupation has a statistically significant correlation with alcohol abuse, schizophrenia, depression, and GAD.

Finally, the probability of developing a stress-related disorder has a statistically significant correlation with IBS type, depression, GAD, panic disorder, somatization, PTSD, and nonorganic sleep disorder.


  Discussion Top


Ford et al. (2010) reported an overlap between IBS and functional dyspepsia in 15–42% of patients. Gwee et al. (2010) have also highlighted an overlap between functional dyspepsia and IBS. Not only somatic or other functional gastrointenstinal disorder (FGIDs), but also 54–94% of patients with IBS do have associated psychiatric comorbidities.

Mnnikes (2011) reported that patients with IBS have a poor quality of life (QOL) as compared with the general population. The QOL in patients with IBS depends not only on the symptoms specific to IBS but also on the associated comorbid psychiatric and somatic diseases. Unless somatic and psychiatric manifestations are recognized and treated, the treatment of IBS will remain incomplete. In fact, there are evidences that even low-dose tricyclic antidepressants lead to overall improvement in the symptoms of IBS.

There is a lack of data with very few studies associating IBS and risk of psychiatric disorders, hence the idea for the current study ascended. The current study included a total number of 150 patients. All complained of IBS symptoms with at least one episode of abdominal pain or flatulence per week in association with a change in bowel habit.

All patients in the study were subjected to a detailed history taking and complete general and local abdominal examination.

The results showed that the highest percent of patients ranged from 31 to 40 (38%) years, to a lesser extent were patients ranging from 18 to 30 (36%) years, patients ranging from 41 to 50 (18%) years, patients ranging from 51 to 60 (5.3%) years, and patients above 60 (2.7%) years. Regarding sex, 34% were males and 66% were females.

In a study by Singh et al. (2012), the mean age of patients with IBS and controls was 32.9±9.4 (72.8% male) years and 31.6±10 (67.7% male) years, respectively. Regarding age, their results were almost similar, yet the sex did not come in accordance with the current results.

van Tilburg et al. (2013) on the contrary agreed with both the age and predomination of females in their study, where the mean age in their study was 34.6 years (SD=11.7; age range, 18–73) and participants were predominantly female (81.5%).

Lee et al. (2015) explored the relationship between IBS and the subsequent development of psychiatric disorders including schizophrenia, bipolar disorder, depressive disorder, anxiety disorder, and sleep disorder. Their research demonstrated that 56.45% were male and 43.55% were female. The median age of the patients was 47.47 years.

According to the level of education, 12% were illiterate, 30.7% had only primary certificate, 40% had high school certificate, and 17.3% were university graduates. Concerning occupation, 33.3% of the patients were working, 53.4% were not working (this percent includes housewives), and 13.3% stopped working after getting ill. Regarding marital status, 9.3% were single, 77.33% were married, 6% were divorced, and 7.33% were widow.

The results showed that the highest percent of patients had mixed type of IBS (58.7%), patients with constipation type were 24%, and patients with diarrhea type were 17.3%.

Singh et al. (2012) is not consistent with the current findings as they illustrated that 57 (31%) had IBS-C, 69 (37.5%) had IBS-D, 58 (31.5%) had IBS-M, and none had IBS-U, that is, all types were reported almost similarly. In the present research, the mixed type was the predominant type. Probably the ones experiencing diarrhea alone or constipation alone assume that their disturbed bowl habits could be related to a type of food or drinking tap water.

Of all patients with IBS, only 37.3% did not have psychiatric comorbidity and 62.7% had psychiatric comorbidity. Of patients with IBS with psychiatric comorbidity, 17.3% were type C, 9.4% were type D, and 36% were type M.

The results of Singh et al. (2012) concur with the current results, as they found that at least one or more psychiatric comorbidity was identified in 147 patient with IBS which was significantly higher in comparison with controls (79.9 vs. 34.3%). The presence of at least one psychiatric illness was significantly higher among patients with severe disease in comparison with those having mild IBS (94.4 vs. 35.7%) and moderately severe IBS (94.4 vs. 76.1%).

The present results demonstrated that psychiatric comorbidity in IBS to be as follows: 8% of the patients were in group I (organic mental and psychoactive substance use syndromes), 32% in group II (psychotic and affective syndromes), 53.3% in group III (neurotic and behavioral syndromes), and 4% in group IV (personality disorders).

There were no patients with organic mental, whereas psychoactive substance use patients were divided into alcohol use patients (6.38%) and cannabinoids use patients (6.38%). Moreover, 17% of psychiatric comorbidity patients had schizophrenia, 2.1% had bipolar affective disorder, and 31.9% had depression. Moreover, 4.25% had obsessive personality and 2.13% had anxious personality.

Certain personality traits or temperament characteristics may make one vulnerable to the effects of stressors. A widely studied personality factor is neuroticism, which describes people who readily experience negative effect. Participants high in neuroticism are more reactive to stress and have stronger reactions to recurring problems. Neuroticism is one of the few personality traits that have been consistently found to be increased in patients with IBS compared with controls (Tosic-Golubovic et al., 2010).

Likelihood for developing stress-related disorders and definitely IBS is divided into three main categories (mild, moderate, and severe). The highest numbers were found in schizophrenia where six patients had severe IBS with type M. In depression, 15 patients had severe IBS with type M. In GAD, 14 patients had severe IBS with type M, whereas in somatization, seven patients had moderate IBS with type M and 16 patients had severe IBS with type M.

Zhou and Verne (2011) suggested that organization of somatic complaints into discrete diagnosis is an artifact of medical subspecialization. On the basis of clinical history, the patient can be diagnosed having somatization disorder by a psychiatrist, fibromyalgia by a rheumatologist, IBS by a gastroenterologist, chronic pelvic pain by a gynecologist, and so on. However, this coexistence of various somatic comorbidities with IBS also highlights that these disorders share a common underlying pathophysiology. van Tilburg et al. (2013) found that IBS severity was predominantly moderate (43%) to high (39.5%).

Widespread somatic hypersensitivity has also been shown in patients with IBS. This somatic and visceral hypersensitivity can thus be a common underlying pathophysiological factor for IBS and associated somatic comorbidities (Sperber and Dekel, 2010).

Ford et al. (2010) have shown that excess healthcare costs in IBS are mainly owing to associated comorbidities which is of immense importance considering the high prevalence of the IBS in the general population.

The current work revealed a statistically significant association and a significant correlation between IBS type and the following psychiatric comorbidities: depression, GAD, panic disorder, OCD, and somatization. It was noted from the value of R that depression, GAD, and somatization increase more in IBS type M than D and C, whereas panic and OCD increase more in IBS type C than D and M. Moreover, from the value of R, the correlation between IBS type and depression is stronger than GAD, then somatization, panic disorder, and finally OCD. There is no statistically significant association between IBS type and other psychiatric comorbidities.

Moreover, there was a statistically significant association between the liability to have a stress-related disorder severity and the following psychiatric comorbidities: depression, GAD, panic disorder, somatization, PTSD, and nonorganic sleep disorder. Moreover, a significant correlation between the severity to be liable to stress-related disorder and the following psychiatric comorbidities: depression, GAD, panic disorder, somatization, PTSD, and nonorganic sleep disorder. It was noticed from the value of R that the severity of depression, GAD, panic disorder, somatization, PTSD, and nonorganic sleep disorder increases with the increase of severity of having a stress-related disorder. Moreover, from the value of R, the correlation between this severity and somatization is stronger than depression, then GAD, then nonorganic sleep, then PTSD, and finally panic disorder.

Furthermore, sex had a statistically significant correlation with alcohol abuse, cannabinoids, schizophrenia, depression, and nonorganic sexual dysfunction. The negative sign means that it is more in males, whereas postive sign means that it is more in females, so alcohol abuse, cannabinoids, schizophrenia, and nonorganic sexual are more in males whereas depression is more in females. This agrees with the prevalence rates of mental disorders that alcohol consumption, cannabis use, and schizophrenia are more in males, whereas anxiety and depression are more in females.

Regarding age, it showed a statistically significant correlation with depression, nonorganic sleep disorder, and nonorganic sexual dysfunction. The positive sign means that the incidane of the disease increases with increase in age. In education, there is no statistically significant correlation with any of the psychiatric comorbidities.

Moreover, marital status had a statistically significant correlation with schizophrenia, depression, GAD, panic disorder, somatization, anorexia nervosa, nonorganic sleep disorder, and nonorganic sexual dysfunction. The positive sign means that the incidence of the disease is more in single, than married, then divorced, and finally widow, whereas the negative sign means that the incidence of the disease is more in widow than divorced, and then married, and then single. GAD, panic disorder, somatization, anorexia nervosa, nonorganic sleep disorder, and nonorganic sexual dysfunction have positive sign, whereas schizophrenia and depression have negative sign.

Occupation has a statistically significant correlation with alcohol abuse, schizophrenia, depression, and GAD. The positive sign means that the incidence of the disease is more in working than not working, then stopped working, whereas the negative sign means that the incidence of the disease is more in stopped working than not working, and then working only. GAD has a positive sign, whereas alcohol abuse, schizophrenia, and depression has a negative sign.

Finally, IBS severity has a statistically significant correlation with IBS type, depression, GAD, panic disorder, somatization, PTSD, and nonorganic sleep disorder. We noted from the value of R (positive sign) that the severity of these psychiatric comorbidities increases with increase of IBS severity.

Mykletun et al. (2010) found no association between bipolar disorder and IBS. Singh et al. (2012) observed that total QOL score decreased by 0.4 U with each 1 U increase in IBS severity score. They concluded that most patients with IBS had associated psychiatric, somatic comorbidities, and reduced QOL. Very few of them received specific psychiatric treatment.

van Tilburg et al. (2013) indicated that catastrophizing and somatization were the only two psychological variables directly associated with IBS severity. Increases in catastrophizing and somatization were associated with increases in IBS symptom severity. Additionally, anxiety had an indirect effect on IBS symptoms through catastrophizing as well as somatization − whereas anxiety was in turn predicted by neuroticism and life events. Thus, neuroticism and stressful life events increase anxiety. The effect of anxiety on IBS severity is mediated by catastrophizing and somatization. They suggested that the most fruitful approach to curb negative effects of psychological factors on IBS is to reduce catastrohizing and somatization.

Lee et al. (2015) found that the most common subsequent psychiatric disorders were depressive disorder, anxiety disorder, and sleep disorder. The incidence rates for depressive disorder, anxiety disorder, sleep disorder, and bipolar disorder were all significantly higher for the IBS cohort than for the comparison cohort. They concluded that IBS may increase the risk of subsequent depressive disorder, anxiety disorder, sleep disorder, and bipolar disorder.


  Conclusion Top


Most patients with IBS have associated psychiatric or somatic comorbidities. We indicated an increased risk of depressive disorder, anxiety disorder, sleep disorder, and bipolar disorder among patients with IBS. Physiological and social factors are of importance in predicting IBS severity and interact with psychological factors to predict IBS outcomes.

We can conclude that patients with IBS have significantly higher levels of psychiatric comorbidites than healthy ones. There is a strong correlation between severity of psychiatric sympatomatology and duration of IBS. Stress worsens symptoms of IBS.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Gwee KA, Bak YT, Ghoshal UC, Gonlachanvit S, Lee OY, Fock KM et al. (2010). Asian consensus on orritable bowel syndrome. J Gastroenterol Hepatol 25:1189–1205.  Back to cited text no. 3
    
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Kajander K, Myllyluoma E, Rajilić-Stojanović M, Kyrönpalo S, Rasmussen M, Järvenpää S et al. (2008). Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota. Aliment Pharmacol Ther 27:48–57.  Back to cited text no. 4
    
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Khanna S, Tosh PK (2014). A clinician’s primer on the role of the microbiome in human health and disease. Mayo Clin Proc 89:107–114.  Back to cited text no. 5
    
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Mykletun A, Jacka F, Williams L, Pasco J, Henry M, Nicholson GC et al. (2010). Prevalence of mood and anxiety disorder in self reported irritable bowel syndrome (IBS). An epidemiological population based study of women. BMC Gastroenterol 10:88.  Back to cited text no. 9
    
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9], [Table 10], [Table 11], [Table 12], [Table 13]


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