Neuroendocrine markers and psychological features in patients with irritable bowel syndrome

Abstract

Background and aims

The key role of the brain-gut axis in the pathophysiology of irritable bowel syndrome (IBS) has been recognized. The aim of this study was to assess the possible association between IBS, neuroendocrine markers, and psychological features.

Methods

One hundred and twenty-five consecutive IBS patients and 105 healthy subjects were enrolled. Plasma serotonin, plasma and urinary cortisol, and plasma neuropeptide Y levels were evaluated. All patients were given a questionnaire to assess IBS symptom severity. In 66 patients, a psychodiagnostic assessment was carried out.

Results

A high incidence of specific psychological features, including state anxiety (69.69 %), trait anxiety (54.54 %), obsessions and compulsions (28.78 %), was observed in IBS patients. A positive correlation between neuropeptide Y and state anxiety (r = 0.287, p = 0.024) and simulation/social ingenuity (r = 0.269, p = 0.039) was found in these patients. In diarrhea-predominant IBS, plasma cortisol was linearly related to plasma serotonin (r = 0.5663, p < 0.001).

Conclusions

In IBS patients, a significant correlation was found between specific psychological features and neuroendocrine markers, especially plasma cortisol and neuropeptide Y; in diarrhea-predominant IBS, a correlation between plasma cortisol and serotonin was found, although it needs to be confirmed in more extensive cohorts.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Abbreviations

NPY:

Neuropeptide Y

IBS:

Irritable bowel syndrome

HS:

Healthy subjects

References

  1. 1.

    Camilleri M, Choi MG (1997) Irritable bowel syndrome. Aliment Pharmacol Ther 11:3–15

    PubMed  Article  CAS  Google Scholar 

  2. 2.

    Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC (2006) Functional bowel disorders. Gastroenterology 130:1480–1491

    PubMed  Article  Google Scholar 

  3. 3.

    Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Müller-Lissner SA (1999) Functional bowel disorders and functional abdominal pain. Gut 45:II43–II47

    PubMed  Article  Google Scholar 

  4. 4.

    Lydiard RB, Fossey MD, Marsh W, Ballenger JC (1993) Prevalence of psychiatric disorders in patients with irritable bowel syndrome. Psychosomatics 34:229–234

    PubMed  Article  CAS  Google Scholar 

  5. 5.

    Drossman DA, Creed FH, Olden KW, Svedlund J, Toner BB, Whitehead WE (1999) Psychosocial aspects of the functional gastrointestinal disorders. Gut 45:II 25–II 30

    Google Scholar 

  6. 6.

    Gunn MC, Cavin AA, Mansfield JC (2003) Management of irritable bowel syndrome. Postgrad Med J 79:154–158

    PubMed  Article  CAS  Google Scholar 

  7. 7.

    Kim DY, Camilleri M (2000) Serotonin: a mediator of the brain–gut connection. Am J Gastroenterol 95:2698–2709

    PubMed  CAS  Google Scholar 

  8. 8.

    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. doi:10.1007/s00535-012-0627-7

  9. 9.

    Karantanos T, Markoutsaki T, Gazouli M, Anagnou NP, Karamanolis DG (2010) Current insights in to the pathophysiology of irritable bowel syndrome. Gut Pathog 2:3

    PubMed  Article  Google Scholar 

  10. 10.

    Kawahito Y, Sano H, Mukai S, Asai K, Kimura S, Yamamura Y, Kato H, Chrousos GP, Wilder RL, Kondo M (1995) Corticotropin releasing hormone in colonic mucosa in patients with ulcerative colitis. Gut 37:544–551

    PubMed  Article  CAS  Google Scholar 

  11. 11.

    Stasi C, Frisoli A, Bellini M, Taddei S, Costa F, Biagi S, Mumolo MG, Ricchiuti A, Marchi S (2006) Increased levels of neuropeptide Y in patients with irritable bowel syndrome. Dig Liver Dis 38:S131

    Article  Google Scholar 

  12. 12.

    Bearcroft CP, Perret D, Farthing MJG (1998) Postprandial plasma 5-hydroxytryptamine in diarrhoea-predominant irritable bowel syndrome: a pilot study. Gut 42:42–46

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Bellini M, Rappelli L, Blandizzi C, Costa F, Stasi C, Colucci R, Giannaccini G, Marazziti D, Betti L, Baroni S, Mumolo MG, Marchi S, Del Tacca M (2003) Platelet serotonin transporter in patients with diarrhea-predominant irritable bowel syndrome both before and after treatment with alosetron. Am J Gastroenterol 98:2705–2711

    PubMed  Article  CAS  Google Scholar 

  14. 14.

    Engsbro AL, Simren M, Bytzer P (2012) The Rome II and Rome III criteria identify the same subtype-populations in irritable bowel syndrome: agreement depends on the method used for symptom report. Neurogastroenterol Motil. doi:10.1111/j.1365-2982.2012.01908

  15. 15.

    Francis CY, Morris J, Whorwell PJ (1997) The irritable bowel severity scoring system: a simple method of monitoring irritable bowel syndrome and its progress. Aliment Pharmacol Ther 11:395–402

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    Hodgson RJ, Rachman S (1977) Obsessional-compulsive complaints. Behav Res Ther 15:389–395

    PubMed  Article  CAS  Google Scholar 

  17. 17.

    Spielberger CD (1983) State-trait anxiety inventory: a comprehensive bibliography. Consulting Psychologist, Palo Alto

    Google Scholar 

  18. 18.

    Bertolotti G, Michielin P, Sanavio E, Simonetti G, Vidotto G, Zorn AM (1985) CBA—Cognitive behavioral assessment 2.0.—Una batteria a vasto spettro per la pratica clinico-terapeutica—Firenze, Organizzazioni Speciali

  19. 19.

    Drossman DA, McKee DC, Sandler RS, Mitchell CM, Cramer EM, Lowman BC, Burger AL (1988) Psychosocial factors in the irritable bowel syndrome. A multivariate study of patients and nonpatients with irritable bowel syndrome. Gastroenterology 95:701–708

    PubMed  CAS  Google Scholar 

  20. 20.

    Heitkemper M, Jarret M, Cain K, Shaver J, Bond E, Woods NF, Walker E (1996) Increased urine catecholamines and cortisol in women with irritable bowel syndrome. Am J Gastroenterol 91:906–913

    PubMed  CAS  Google Scholar 

  21. 21.

    Plotsky PM, Owens MJ, Nemeroff CB (1998) Psychoneuroendocrinology of depression. Hypothalamic–pituitary–adrenal axis. Psychiatr Clin North Am 21:293–307

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Böhmelt AH, Nater UM, Franke S, Hellhammer DH, Ehlert U (2005) Basal and stimulated hypothalamic–pituitary–adrenal axis activity in patients with functional gastrointestinal disorders and healthy controls. Psychosom Med 67:288–294

    PubMed  Article  Google Scholar 

  23. 23.

    Chang L, Sundaresh S, Elliott J, Anton PA, Baldi P, Licudine A, Mayer M, Vuong T, Hirano M, Naliboff BD, Ameen VZ, Mayer EA (2009) Dysregulation of the hypothalamic–pituitary–adrenal (HPA) axis in irritable bowel syndrome. Neurogastroenterol Motil 21:149–159

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    Elsenbruch S, Orr WC (2001) Diarrhea- and constipation-predominant IBS patients differ in postprandial autonomic and cortisol responses. Am J Gastroenterol 96:460–466

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    Fukudo S, Nomura T, Hongo M (1998) Impact of corticotropin-releasing hormone on gastrointestinal motility and adrenocorticotropic hormone in normal controls and patients with irritable bowel syndrome. Gut 42:845–849

    PubMed  Article  CAS  Google Scholar 

  26. 26.

    Dinan TG, Quigley EM, Ahmed SM, Scully P, O’Brien S, O’Mahony L, O’Mahony S, Shanahan F, Keeling PW (2006) Hypothalamic–pituitary–gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology 130:304–311

    PubMed  Article  CAS  Google Scholar 

  27. 27.

    Kaplan HI, Sadock BJ, Grebb JA (1994) Kaplan and Sadock's synopsis of psychiatry: behavioral sciences clinical psychiatry, 7th edn. Williams & Wilkins, Baltimore

    Google Scholar 

  28. 28.

    Iovino P, Azpiroz F, Domingo E, Malagelada JR (1995) The sympathetic nervous system modulates perception and reflex responses to gut distention in humans. Gastroenterology 108:680–686

    PubMed  Article  CAS  Google Scholar 

  29. 29.

    Waring WS, Chui M, Japp A, Nicol EF, Ford MJ (2004) Autonomic cardiovascular responses are impaired in women with irritable bowel syndrome. J Clin Gastroenterol 38:658–663

    PubMed  Article  Google Scholar 

  30. 30.

    Heitkemper M, Jarret M, Bond E, Walzer E, Rockwell M (1994) Increased sympathetic nervous system activity in women with IBS. Gastroenterology 106:A509

    Google Scholar 

  31. 31.

    Jorgensen LS, Christiansen P, Raundahl U, Ostgaard S, Christensen NJ, Fenger M, Flachs H (1993) Autonomic nervous system function in patients with functional abdominal pain. An experimental study. Scand J Gastroenterol 28:63–68

    PubMed  Article  CAS  Google Scholar 

  32. 32.

    Levi L (1972) Stress and distress in response to psychosocial stimuli. Laboratory and real life studies on sympathoadrenomedullary and related reactions. Acta Med Scand 528:1–166

    CAS  Google Scholar 

  33. 33.

    Silverman DH, Munakata JA, Ennes H, Mandelkern MA, Hoh CK, Mayer EA (1997) Regional cerebral activity in normal and pathological perception of visceral pain. Gastroenterology 112:64–72

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Drossman DA, Ringel Y, Vogt BA, Leserman J, Lin W, Smith JK, Whitehead W (2003) Alterations of brain activity associated with resolution of emotional distress and pain in a case of severe irritable bowel syndrome. Gastroenterology 124:754–761

    PubMed  Article  Google Scholar 

  35. 35.

    Prior A, Colgan SM, Whorwell PJ (1990) Changes in rectal sensitivity after hypnotherapy with irritable bowel syndrome. Gut 31:896–898

    PubMed  Article  CAS  Google Scholar 

  36. 36.

    Simrén M, Abrahamsson H, Bjornsson ES (2001) An exaggerated sensory component of the gastrocolonic response in patients with irritable bowel syndrome. Gut 48:20–27

    PubMed  Article  Google Scholar 

  37. 37.

    Park JH, Rhee PL, Kim HS, Lee JH, Kim YH, Kim JJ, Rhee JC (2006) Mucosal mast cell counts correlate with visceral hypersensitivity in patients with diarrhea predominant irritable bowel syndrome. J Gastroenterol Hepatol 21(1 Pt 1):71–78

    PubMed  Article  Google Scholar 

  38. 38.

    Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM, Corinaldesi R (2004) Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126:693–702

    PubMed  Article  Google Scholar 

  39. 39.

    Rodríguez-Fandiño O, Hernández-Ruiz J, Schmulson M (2010) From cytokines to toll-like receptors and beyond—current knowledge and future research needs in irritable bowel syndrome. J Neurogastroenterol Motil 16:363–373

    PubMed  Article  Google Scholar 

Download references

Conflict of interest

The authors have no conflicts of interest to disclose.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Cristina Stasi.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stasi, C., Bellini, M., Costa, F. et al. Neuroendocrine markers and psychological features in patients with irritable bowel syndrome. Int J Colorectal Dis 28, 1203–1208 (2013). https://doi.org/10.1007/s00384-013-1646-4

Download citation

Keywords

  • Neuroendocrine markers
  • Psychological features
  • Irritable bowel syndrome