Advertisement

Similar Fecal Microbiota Signatures in Patients With Diarrhea-Predominant Irritable Bowel Syndrome and Patients With Depression

      Background & Aims

      Patients with irritable bowel syndrome (IBS) often have psychiatric comorbidities. Alterations in the intestinal microbiota have been associated with IBS and depression, but it is not clear if there is a microbial relationship between these disorders. We studied the profiles of fecal microbiota samples from patients with IBS, depression, or comorbidities of IBS and depression; we determined the relationships among these profiles and clinical and pathophysiological features of these disorders.

      Methods

      We used 454 pyrosequencing to analyze fecal microbiota samples from 100 subjects (40 with diarrhea-predominant IBS [IBS-D], 15 with depression, 25 with comorbidities of IBS and depression, and 20 healthy individuals [controls]), recruited at Peking University. Abdominal and psychological symptoms were evaluated with validated questionnaires. Visceral sensitivity was evaluated using a barostat. Colonic mucosal inflammation was assayed by immunohistochemical analyses of sigmoid tissue biopsy specimens.

      Results

      Fecal microbiota signatures were similar between patients with IBS-D and depression in that they were less diverse than samples from controls and had similar abundances of alterations. They were characterized by high proportions of Bacteroides (type I), Prevotella (type II), or nondominant microbiota (type III). Most patients with IBS-D or depression had type I or type II profiles (IBS-D had 85% type I and type II profiles, depression had 80% type I and type II profiles). Colon tissues from patients with type I or type II profiles had higher levels of inflammatory markers than colon tissues from patients with type III profiles. The level of colon inflammation correlated with the severity of IBS symptoms.

      Conclusions

      Patients with IBS-D and depression have similar alterations in fecal microbiota; these might be related to the pathogenesis of these disorders. We identified 3 microbial profiles in patients that could indicate different subtypes of IBS and depression or be used as diagnostic biomarkers.

      Keywords

      Abbreviations used in this paper:

      COMO (comorbidities of irritable bowel syndrome and depression), DSM-IV (Diagnostic and Statistical Manual of Mental Disorders, 4th edition), IBS (irritable bowel syndrome), MCP-1 (monocyte chemotactic protein-1), MINI (Mini-International Neuropsychiatric Interview), MIP-1α (macrophage inflammatory protein-1α), PCA (principal component analysis), SDS (Self-Rating Depression Scale), SSS (Symptom Severity Scores)
      To read this article in full you will need to make a payment
      AGA Member Login
      Login with your AGA username and password.
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Spiller R.
        • Aziz Q.
        • Creed F.
        • et al.
        Guideline on the irritable bower syndrome: mechanisms and practical management.
        Gut. 2007; 56: 1770-1798
        • Bengtson M.B.
        • Aamodt G.
        • Vatn M.H.
        • et al.
        Co-occurrence of IBS and symptoms of anxiety or depression, among Norwegian twins, is influenced by both heredity and intrauterine growth.
        BMC Gastroenterol. 2015; 15: 9
        • Modabbernia M.J.
        • Mansour-Ghanaei F.
        • Imani A.
        • et al.
        Anxiety-depressive disorders among irritable bowel syndrome patients in Guilan, Iran.
        BMC Res Notes. 2012; 5: 112
        • Mayer E.A.
        • Tillisch K.
        The brain-gut axis in abdominal pain syndromes.
        Annu Rev Med. 2011; 62: 381-396
        • Barreau F.
        • Salvador-Cartier C.
        • Houdeau E.
        • et al.
        Long-term alterations of colonic nerve-mast cell interactions induced by neonatal maternal deprivation in rats.
        Gut. 2008; 57: 582-590
        • Xu D.
        • Gao J.
        • Gillilland M.
        • et al.
        Rifaximin alters intestinal bacteria and prevents stress-induced gut inflammation and visceral hyperalgesia in rats.
        Gastroenterology. 2014; 146: 484-496
        • Jeffery I.B.
        • O’Toole P.W.
        • Öhman L.
        • et al.
        An irritable bowel syndrome subtype defined by species-specific alterations in fecal microbiota.
        Gut. 2012; 61: 997-1006
        • Ng S.C.
        • Lam E.F.
        • Lam T.T.
        • et al.
        Effect of probiotic bacteria on the intestinal microbiota in irritable bowel syndrome.
        J Gastroenterol Hepatol. 2013; 28: 1624-1631
        • Rajilić-Stojanović M.
        • Biagi E.
        • Heilig H.G.
        • et al.
        Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome.
        Gastroenterology. 2011; 141: 1792-1801
        • Codling C.
        • O'Mahony L.
        • Shanahan F.
        • et al.
        A molecular analysis of fecal and mucosal bacterial communities in irritable bowel syndrome.
        Dig Dis Sci. 2010; 55: 392-397
        • Parkes G.C.
        • Rayment N.B.
        • Hudspith B.N.
        • et al.
        Distinct microbial populations exist in the mucosa-associated microbiota of sub-groups of irritable bowel syndrome.
        Neurogastroenterol Motil. 2012; 24: 31-39
        • Ouwehand A.C.
        • Salminen S.
        • Arvola T.
        • et al.
        Microbiota composition of the intestinal mucosa: association with fecal microbiota?.
        Microbiol Immunol. 2004; 48: 497-500
        • Durban A.
        • Abellan J.J.
        • Jimenez-Hernandez N.
        • et al.
        Assessing gut microbial diversity from feces and rectal mucosa.
        Microb Ecol. 2011; 61: 123-133
        • Naseribafrouei A.
        • Hestad K.
        • Avershina E.
        • et al.
        Correlation between the human fecal microbiota and depression.
        Neurogastroenterol Motil. 2014; 26: 1155-1162
        • Diaz Heijtz R.
        • Wang S.
        • Anuar F.
        • et al.
        Normal gut microbiota modulates brain development and behavior.
        Proc Natl Acad Sci U S A. 2011; 108: 3047-3052
        • Ogbonnaya E.S.
        • Clarke G.
        • Shanahan F.
        • et al.
        Adult hippocampal neurogenesis is regulated by the microbiome.
        Biol Psychiatry. 2015; 78: e7-e9
        • Mayer E.A.
        • Savidge T.
        • Shulman R.J.
        • et al.
        Brain gut microbiome interactions and functional bowel disorders.
        Gastroenterology. 2014; 146: 1500-1512
        • Cryan J.F.
        • Dinan T.G.
        More than a gut feeling: the microbiota regulates neurodevelopment and behavior.
        Neuropsychopharmacology. 2015; 40: 241-242
        • Murphy P.M.
        • Baggiolini M.
        • Charo I.F.
        • et al.
        International Union of Pharmacology. XXII. Nomenclature for chemokine receptors.
        Pharmacol Rev. 2000; 52: 145-176
        • Alemán J.O.
        • Eusebi L.H.
        • Ricciardiello L.
        • et al.
        Mechanisms of obesity-induced gastrointestinal neoplasia.
        Gastroenterology. 2014; 146: 357-373
        • Olefsky J.M.
        • Glass C.K.
        Macrophages, inflammation, and insulin resistance.
        Annu Rev Physiol. 2010; 72: 219-246
        • Souza D.G.
        • Vieira A.T.
        • Soares A.C.
        • et al.
        The essential role of the intestinal microbiota in facilitating acute inflammatory responses.
        J Immunol. 2004; 173: 4137-4146
        • Ritter U.
        • Moll H.
        Monocyte chemotactic protein-1 stimulates the killing of leishmania major by human monocytes, acts synergistically with IFN-gamma and is antagonized by IL-4.
        Eur J Immunol. 2000; 30: 3111-3120
        • van Zuiden M.
        • Heijnen C.J.
        • van de Schoot R.
        • et al.
        Cytokine production by leukocytes of military personnel with depressive symptoms after deployment to a combat-zone: a prospective, longitudinal study.
        PLoS One. 2011; 6: e29142
        • Margulies M.
        • Egholm M.
        • Altman W.E.
        • et al.
        Genome sequencing in microfabricated high-density picolitre reactors.
        Nature. 2005; 437: 376-380
        • Arumugam M.
        • Raes J.
        • Pelletier E.
        • et al.
        Enterotypes of the human gut microbiome.
        Nature. 2011; 473: 174-180
        • Rhee S.H.
        • Pothoulakis C.
        • Mayer E.A.
        Principles and clinical implications of the brain-gut-enteric microbiota axis.
        Nat Rev Gastroenterol Hepatol. 2009; 6: 306-314
        • Mayer E.A.
        Gut feelings: the emerging biology of gut-brain communication.
        Nat Rev Neurosci. 2011; 12: 453-466
        • Zitomersky N.L.
        • Atkinson B.J.
        • Franklin S.W.
        • et al.
        Characterization of adherent bacteroidales from intestinal biopsies of children and young adults with inflammatory bowel disease.
        PLoS One. 2013; 8: e63686
        • Chen L.
        • Wang W.
        • Zhou R.
        • et al.
        Characteristics of fecal and mucosa-associated microbiota in Chinese patients with inflammatory bowel disease.
        Medicine (Baltimore). 2014; 93: e51
        • Tagami S.
        • Susuki K.
        • Takeda M.
        • et al.
        Fulminant case of Guillain-Barré syndrome with poor recovery and depression following Haemophilus influenzae infection.
        Psychiatry Clin Neurosci. 2008; 62: 486
        • Lackner J.M.
        • Gudleski G.D.
        • Thakur E.R.
        • et al.
        The impact of physical complaints, social environment, and psychological functioning on IBS patients' health perceptions: looking beyond GI symptom severity.
        Am J Gastroenterol. 2014; 109: 224-233

      References

        • Sheehan D.V.
        • Lecrubier Y.
        • Sheehan K.H.
        • et al.
        The Mini International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10.
        J Clin Psychiatry. 1998; 59: 22-33
        • Si T.M.
        • Shu L.
        • Dang W.M.
        • et al.
        Evaluation of the reliability and validity of Chinese version of the Mini-International Neuropsychiatric Interview in patients with mental disorders [Chinese].
        Chin Ment Health J. 2009; 23: 493-497
        • McInnes P.
        • Cutting M.
        Manual of procedures for human microbiome project: core microbiome sampling protocol A HMP protocol # 07-001, Version 12.0. 2010; (Available at: http://hmpdacc.org/resources/tools_protocols.php)
        • Remmele W.
        • Stegner H.E.
        Recommendation for uniform definition of an immunoreactive score (irs) for immunohistochemical estrogen receptor detection (er-ica) in breast cancer tissue.
        Der Pathologe. 1987; 8: 138-140
        • Lindner J.L.
        • Loibl S.
        • Denkert C.
        • et al.
        Expression of secreted protein acidic and rich in cysteine (SPARC) in breast cancer and response to neoadjuvant chemotherapy.
        Ann Oncol. 2015; 26: 95-100
        • Schloss P.D.
        • Westcott S.L.
        • Ryabin T.
        • et al.
        Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.
        Appl Environ Microbiol. 2009; 75: 7537-7541