Anxiety and depression comorbidities in irritable bowel syndrome (IBS): a systematic review and meta-analysis

  • Guillaume Fond
  • Anderson Loundou
  • Nora Hamdani
  • Wahid Boukouaci
  • Aroldo Dargel
  • José Oliveira
  • Matthieu Roger
  • Ryad Tamouza
  • Marion Leboyer
  • Laurent Boyer
Original Paper

Abstract

Irritable bowel syndrome (IBS) has been associated with high prevalence of psychological disorders. However, it remains unclear whether IBS and each of its subtypes (predominant diarrhea IBS-D, constipation IBS-C, mixed IBS-M) are associated with higher anxiety and depressive symptoms levels. This study aimed to determine the associations of IBS and each of its subtypes with anxiety and/or depression. We conducted a systematic review and meta-analysis using five electronic databases (PubMed, PsychINFO, BIOSIS, Science Direct, and Cochrane CENTRAL). We selected case–control studies comparing anxiety and depression levels of patients with IBS to healthy controls, using standardized rating scales. Outcomes were measured as random pooled standardized mean differences (SMD). Ten studies were included in our analysis (885 patients and 1,384 healthy controls). Patients with IBS had significant higher anxiety and depression levels than controls (respectively, SMD = 0.76, 95 % CI 0.47; 0.69, p < 0.01, I2 = 81.7 % and SMD = 0.80, 95 % CI 0.42; 1.19, p < 0.01, I2 = 90.7 %). This significant difference was confirmed for patients with IBS-C and -D subtypes for anxiety, and only in IBS-D patients for depression. However, other IBS subtypes had a statistical trend to be associated with both anxiety and depressive symptomatology, which suggests a lack of power due to the small number of studies included. Patients with IBS had significantly higher levels of anxiety and depression than healthy controls. Anxiety and depression symptomatology should be systematically checked and treated in IBS patients, as psychological factors are important moderators of symptom severity, symptom persistence, decisions to seek treatment, and response to treatment.

Keywords

Irritable bowel syndrome Anxiety Depression Psychiatric comorbidities 

Supplementary material

406_2014_502_MOESM1_ESM.docx (77 kb)
Supplementary material 1 (DOCX 77 kb)

References

  1. 1.
    Alander T, Heimer G, Svardsudd K, Agreus L (2008) Abuse in women and men with and without functional gastrointestinal disorders. Dig Dis Sci 53(7):1856–1864. doi:10.1007/s10620-007-0101-1 PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Ballou SK, Keefer L (2013) Multicultural considerations in the diagnosis and management of irritable bowel syndrome: a selective summary. Eur J Gastroenterol Hepatol. doi:10.1097/MEG.0b013e3283632bf2 PubMedGoogle Scholar
  3. 3.
    Beck AT, Epstein N, Brown G, Steer RA (1988) An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol 56(6):893–897PubMedCrossRefGoogle Scholar
  4. 4.
    Bercik P, Collins SM, Verdu EF (2012) Microbes and the gut-brain axis. Neurogastroenterol Motil 24(5):405–413. doi:10.1111/j.1365-2982.2012.01906.x PubMedCrossRefGoogle Scholar
  5. 5.
    Berman S, Suyenobu B, Naliboff BD, Bueller J, Stains J, Wong H, Mayer EA (2012) Evidence for alterations in central noradrenergic signalling in irritable bowel syndrome. Neuroimage 63(4):1854–1863. doi:10.1016/j.neuroimage.2012.08.028 PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to meta-analysis. Wiley, ChichesterCrossRefGoogle Scholar
  7. 7.
    Brandt LJ, Bjorkman D, Fennerty MB, Locke GR, Olden K, Peterson W, Talley N (2002) Systematic review on the management of irritable bowel syndrome in North America. Am J Gastroenterol 97(11 Suppl):S7–26PubMedGoogle Scholar
  8. 8.
    Camilleri M, McKinzie S, Busciglio I, Low PA, Sweetser S, Burton D, Zinsmeister AR (2008) Prospective study of motor, sensory, psychologic, and autonomic functions in patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 6(7):772–781. doi:10.1016/j.cgh.2008.02.060 PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Cheng J, Zhang J, Lu C, Wang L (2012) Using optogenetics to translate the “inflammatory dialogue” between heart and brain in the context of stress. Neurosci Bull 28(4):435–448. doi:10.1007/s12264-012-1246-2 PubMedCrossRefGoogle Scholar
  10. 10.
    Chitkara DK, van Tilburg MA, Blois-Martin N, Whitehead WE (2008) Early life risk factors that contribute to irritable bowel syndrome in adults: a systematic review. Am J Gastroenterol 103(3): 765–774; quiz 775. doi:10.1111/j.1572-0241.2007.01722.x Google Scholar
  11. 11.
    Cho HS, Park JM, Lim CH, Cho YK, Lee IS, Kim SW, Chung YK (2011) Anxiety, depression and quality of life in patients with irritable bowel syndrome. Gut Liver 5(1):29–36. doi:10.5009/gnl.2011.5.1.29 PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Cosco TD, Doyle F, Ward M, McGee H (2012) Latent structure of the Hospital Anxiety And Depression Scale: a 10-year systematic review. J Psychosom Res 72(3):180–184. doi:10.1016/j.jpsychores.2011.06.008 PubMedCrossRefGoogle Scholar
  13. 13.
    Coyne JC, van Sonderen E (2012) No further research needed: abandoning the Hospital and Anxiety Depression Scale (HADS). J Psychosom Res 72(3):173–174. doi:10.1016/j.jpsychores.2011.12.003 PubMedCrossRefGoogle Scholar
  14. 14.
    Derogatis LR, Rickels K, Rock AF (1976) The SCL-90 and the MMPI: a step in the validation of a new self-report scale. Br J Psychiatry 128:280–289PubMedCrossRefGoogle Scholar
  15. 15.
    DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188PubMedCrossRefGoogle Scholar
  16. 16.
    Doyle F, Cosco T, Conroy R (2012) Why the HADS is still important: reply to Coyne & van Sonderen. J Psychosom Res 73(1): 74; author reply 77–78. doi:10.1016/j.jpsychores.2012.04.003
  17. 17.
    Drossman DA, Chang L, Bellamy N, Gallo-Torres HE, Lembo A, Mearin F, Whorwell P (2011) Severity in irritable bowel syndrome: a rome foundation working team report. Am J Gastroenterol 106(10): 1749–1759; quiz 1760. doi:10.1038/ajg.2011.201 Google Scholar
  18. 18.
    Farzaneh N, Ghobakhlou M, Moghimi-Dehkordi B, Naderi N, Fadai F (2012) Evaluation of psychological aspects among subtypes of irritable bowel syndrome. Indian J Psychol Med 34(2):144–148. doi:10.4103/0253-7176.101780 PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Felger JC, Lotrich FE (2013) Inflammatory cytokines in depression: neurobiological mechanisms and therapeutic implications. Neuroscience 246:199–229. doi:10.1016/j.neuroscience.2013.04.060 PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Fond G, Boukouaci W, Leboyer M, Tamouza R (2013) Targeting microbiota in major psychiatric disorders: mechanisms, preclinical data, gastro-intestinal comorbidities and therapeutic options (Submitted)Google Scholar
  21. 21.
    Goodwin L, White PD, Hotopf M, Stansfeld SA, Clark C (2013) Life course study of the etiology of self-reported irritable bowel syndrome in the 1958 British birth cohort. Psychosom Med 75(2):202–210. doi:10.1097/PSY.0b013e31827c351b PubMedCrossRefGoogle Scholar
  22. 22.
    Graff LA, Clara I, Walker JR, Lix L, Carr R, Miller N, Bernstein CN (2013) Fatigue, over time, is associated with disease activity and psychological factors in longitudinal study of inflammatory bowel disease. Clin Gastroenterol Hepatol. doi:10.1016/j.cgh.2013.03.031
  23. 23.
    Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560. doi:10.1136/bmj.327.7414.557 PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Huerta I, Bonder A, Lopez L, Ocampo MA, Schmulson M (2002) Differences in the stress symptoms rating scale in Spanish between patients with irritable bowel syndrome (IBS) and healthy controls. Rev Gastroenterol Mexico 67(3):161–165Google Scholar
  25. 25.
    Kennedy PJ, Clarke G, Quigley EM, Groeger JA, Dinan TG, Cryan JF (2012) Gut memories: towards a cognitive neurobiology of irritable bowel syndrome. Neurosci Biobehav Rev 36(1):310–340. doi:10.1016/j.neubiorev.2011.07.001 PubMedCrossRefGoogle Scholar
  26. 26.
    Klooker TK, Braak B, Painter RC, de Rooij SR, van Elburg RM, van den Wijngaard RM, Boeckxstaens GE (2009) Exposure to severe wartime conditions in early life is associated with an increased risk of irritable bowel syndrome: a population-based cohort study. Am J Gastroenterol 104(9):2250–2256. doi:10.1038/ajg.2009.282 PubMedCrossRefGoogle Scholar
  27. 27.
    Lee KJ, Kim YB, Kim JH, Kwon HC, Kim DK, Cho SW (2008) The alteration of enterochromaffin cell, mast cell, and lamina propria T lymphocyte numbers in irritable bowel syndrome and its relationship with psychological factors. J Gastroenterol Hepatol 23(11):1689–1694. doi:10.1111/j.1440-1746.2008.05574.x PubMedCrossRefGoogle Scholar
  28. 28.
    Lee W, Bindman J, Ford T, Glozier N, Moran P, Stewart R, Hotopf M (2007) Bias in psychiatric case–control studies: literature survey. Br J Psychiatry 190:204–209. doi:10.1192/bjp.bp.106.027250 PubMedCrossRefGoogle Scholar
  29. 29.
    Lee YY, Waid A, Tan HJ, Chua SB, Whitehead WE (2012) Validity and reliability of the Malay-language translation of the Rome III Diagnostic Questionnaire for irritable bowel syndrome. J Gastroenterol Hepatol 27(4):746–750. doi:10.1111/j.1440-1746.2011.06943.x PubMedCrossRefGoogle Scholar
  30. 30.
    Levy RL, Olden KW, Naliboff BD, Bradley LA, Francisconi C, Drossman DA, Creed F (2006) Psychosocial aspects of the functional gastrointestinal disorders. Gastroenterology 130(5):1447–1458. doi:10.1053/j.gastro.2005.11.057 PubMedCrossRefGoogle Scholar
  31. 31.
    Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC (2006) Functional bowel disorders. Gastroenterology 130(5):1480–1491. doi:10.1053/j.gastro.2005.11.061 PubMedCrossRefGoogle Scholar
  32. 32.
    Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Group, P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535. doi:10.1136/bmj.b2535 CrossRefGoogle Scholar
  33. 33.
    Muscatello MR, Bruno A, Pandolfo G, Mico U, Stilo S, Scaffidi M, Zoccali R (2010) Depression, anxiety and anger in subtypes of irritable bowel syndrome patients. J Clin Psychol Med Settings 17(1):64–70. doi:10.1007/s10880-009-9182-7 PubMedCrossRefGoogle Scholar
  34. 34.
    Norton S, Cosco T, Doyle F, Done J, Sacker A (2013) The Hospital Anxiety and Depression Scale: a meta confirmatory factor analysis. J Psychosom Res 74(1):74–81. doi:10.1016/j.jpsychores.2012.10.010 PubMedCrossRefGoogle Scholar
  35. 35.
    Occhipinti K, Smith JW (2012) Irritable bowel syndrome: a review and update. Clin Colon Rectal Surg 25(1):46–52. doi:10.1055/s-0032-1301759 PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Savas LS, White DL, Wieman M, Daci K, Fitzgerald S, Laday Smith S, El-Serag HB (2009) Irritable bowel syndrome and dyspepsia among women veterans: prevalence and association with psychological distress. Aliment Pharmacol Ther 29(1):115–125. doi:10.1111/j.1365-2036.2008.03847.x PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Solmaz M, Kavuk I, Sayar K (2003) Psychological factors in the irritable bowel syndrome. Eur J Med Res 8(12):549–556PubMedGoogle Scholar
  38. 38.
    Spanier JA, Howden CW, Jones MP (2003) A systematic review of alternative therapies in the irritable bowel syndrome. Arch Intern Med 163(3):265–274PubMedCrossRefGoogle Scholar
  39. 39.
    Stasi C, Rosselli M, Bellini M, Laffi G, Milani S (2012) Altered neuro-endocrine-immune pathways in the irritable bowel syndrome: the top-down and the bottom-up model. J Gastroenterol 47(11):1177–1185. doi:10.1007/s00535-012-0627-7 PubMedCrossRefGoogle Scholar
  40. 40.
    Sugaya N, Nomura S, Shimada H (2012) Relationship between cognitive factors and anxiety in individuals with irritable bowel syndrome. Int J Behav Med 19(3):308–315. doi:10.1007/s12529-011-9195-0 PubMedCrossRefGoogle Scholar
  41. 41.
    Talley NJ, Howell S, Poulton R (2001) The irritable bowel syndrome and psychiatric disorders in the community: is there a link? Am J Gastroenterol 96(4):1072–1079. doi:10.1111/j.1572-0241.2001.03741.x PubMedCrossRefGoogle Scholar
  42. 42.
    Talley NJ, Phillips SF, Melton J 3rd, Wiltgen C, Zinsmeister AR (1989) A patient questionnaire to identify bowel disease. Ann Intern Med 111(8):671–674PubMedCrossRefGoogle Scholar
  43. 43.
    Talley NJ, Phillips SF, Wiltgen CM, Zinsmeister AR, Melton LJ 3rd (1990) Assessment of functional gastrointestinal disease: the bowel disease questionnaire. Mayo Clin Proc 65(11):1456–1479PubMedCrossRefGoogle Scholar
  44. 44.
    Tosic-Golubovic S, Miljkovic S, Nagorni A, Lazarevic D, Nikolic G (2010) Irritable bowel syndrome, anxiety, depression and personality characteristics. Psychiatr Danub 22(3):418–424PubMedGoogle Scholar
  45. 45.
    van der Veek PP, Van Rood YR, Masclee AA (2008) Symptom severity but not psychopathology predicts visceral hypersensitivity in irritable bowel syndrome. Clin Gastroenterol Hepatol 6(3):321–328. doi:10.1016/j.cgh.2007.12.005 PubMedCrossRefGoogle Scholar
  46. 46.
    van Tilburg MA, Palsson OS, Whitehead WE (2013) Which psychological factors exacerbate irritable bowel syndrome? Development of a comprehensive model. J Psychosom Res 74(6):486–492. doi:10.1016/j.jpsychores.2013.03.004 PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    van Tilburg MA, Runyan DK, Zolotor AJ, Graham JC, Dubowitz H, Litrownik AJ, Whitehead WE (2010) Unexplained gastrointestinal symptoms after abuse in a prospective study of children at risk for abuse and neglect. Ann Fam Med 8(2):134–140. doi:10.1370/afm.1053 PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Vassos E, Collier DA, Fazel S (2013) Systematic meta-analyses and field synopsis of genetic association studies of violence and aggression. Mol Psychiatry. doi:10.1038/mp.2013.31 PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Guillaume Fond
    • 1
    • 5
  • Anderson Loundou
    • 2
  • Nora Hamdani
    • 1
  • Wahid Boukouaci
    • 4
  • Aroldo Dargel
    • 3
    • 4
  • José Oliveira
    • 4
  • Matthieu Roger
    • 1
  • Ryad Tamouza
    • 4
  • Marion Leboyer
    • 1
  • Laurent Boyer
    • 2
  1. 1.Pôle de psychiatrie des hôpitaux universitaires H Mondor, DHU Pe-Psy, INSERM U955, Eq Psychiatrie Génétique, Fondation FondaMental Fondation de coopération scientifique en santé mentaleUniversité Paris EstCréteilFrance
  2. 2.EA 3279-Self-perceived Health Assessment Research Unit, School of MedicineLa Timone UniversityMarseilleFrance
  3. 3.Laboratory of Molecular Psychiatry, Centro de Pesquisas Experimentais, Hospital de Clínicas de Porto AlegreINCT for Translational MedicinePorto AlegreBrazil
  4. 4.Jean Dausset Laboratory and INSERM, UMRS 940Hôpital Saint LouisParisFrance
  5. 5.Pole de PsychiatrieHôpital A. ChenevierCréteilFrance

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