Skip to main content
Log in

Visceral perception in irritable bowel syndrome

Rectal and gastric responses to distension and serotonin type 3 antagonism

  • Intestinal Disorders, Inflammatory Bowel Disease, Immunology And Microbiology
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

We wished to determine if visceral perception in the rectum and stomach is altered in patients with irritable bowel syndrome and to evaluate the effects on visceral sensation of 5-HT3 receptor blockade. Twelve community patients with diarrhea-predominant irritable bowel syndrome and 10 healthy controls were studied in a double-blind, randomized, placebo-controlled study. Using two barostats, the stomach and rectum were distended, with pressure increments of 4 mm Hg, from 10 to 26 mm Hg; visceral perception was measured on an ordinal scale of 0–10. Personality traits were measured using standard psychological methods, and somatic pain was evaluated by immersion of the nondominant hand in cold water. The effect of 5-HT3 antagonism was tested with a single intravenous dose of ondansetron at 0.15 mg/kg. Gastric perception was higher in irritable bowel syndrome, but rectal distension was perceived similarly in irritable bowel syndrome and controls. Pain tolerance to cold water was also similar in irritable bowel syndrome and controls. Ondansetron induced rectal relaxation and increased rectal compliance but did not significantly alter gastric compliance or visceral perception. Psychological test scores were similar in patients and controls. We conclude that in this group of psychologically normal patients with irritable bowel syndrome, who were not chronic health-care seekers, visceral perception was normal. Ondansetron did not alter gut perception in health or in irritable bowel syndrome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Zighelboim J, Talley NJ: What are functional bowel disorders? Gastroenterology 104:1196–201, 1993

    PubMed  Google Scholar 

  2. Drossman DA, Thompson GW, Talley NJ, Funch-Jensen P, Janssens J, Whitehead WE: Identification of subgroups of functional gastrointestinal disorders. Gastroenterol Int 3:159–172, 1990

    Google Scholar 

  3. Talley NJ, Kramlinger KG, Burton MC, Colwell LJ, Zinsmeister AR: Psychiatric disorders and childhood abuse in the irritable bowel syndrome. Eur J Gastroenterol Hepatol 5:647–654, 1993

    Google Scholar 

  4. Ritchie J: Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14:125–132, 1973

    PubMed  Google Scholar 

  5. Whitehead WE, Holtkotter B, Enck P, Hoelzl R, Holmes KD, Anthony J: Tolerance for rectosigmoid distension in irritable bowel syndrome. Gastroenterology 98:1187–1192, 1990

    PubMed  Google Scholar 

  6. Prior A, Maxton DG, Whorwell PJ: Anorectal manometry in irritable bowel syndrome: Differences between diarrhoea and constipation predominant subjects. Gut 31:458–462, 1990

    PubMed  Google Scholar 

  7. Whitehead WE, Engel BT, Schuster MM: Irritable bowel syndrome: Physiological and psychological differences between diarrhea-predominant and constipation-predominant patients. Dig Dis Sci 25:404–413, 1980

    PubMed  Google Scholar 

  8. Prior A, Read NW: Reduction of rectal sensitivity and post-prandial motility by granisetron, a 5-HT3-receptor antagonist, in patients with irritable bowel syndrome. Aliment Pharmacol Ther 7:175–180, 1993

    PubMed  Google Scholar 

  9. Hammer J, Phillips SF, Talley NJ, Camilleri M: Effect of a 5-HT3 antagonist (ondansetron) on rectal sensitivity and compliance in health and the irritable bowel syndrome. Aliment Pharmacol Ther 7:543–552, 1993

    PubMed  Google Scholar 

  10. Prior A, Sun W-M, Read NW: Irritable bowel syndrome: Differences between patients who show rectal sensitivity and those who do not. Eur J Gastroenterol Hepatol 5:343–349, 1993

    Google Scholar 

  11. Talley NJ: 5-Hydroxytryptamine agonists and antagonists in the modulation of gastrointestinal motility and sensation: Clinical implications. Aliment Pharmacol Ther 6:273–289, 1992

    PubMed  Google Scholar 

  12. Costall B, Naylor RJ: 5-Hydroxytryptamine: New receptors and novel drugs for gastrointestinal motor disorders. Scand J Gastroenterol 25:769–787, 1990

    PubMed  Google Scholar 

  13. Richardson BP, Engel G, Donatsch P, Stadler PA: Identification of serotonin M-receptor subtypes and their specific blockade by a new class of drugs. Nature 316:126–131, 1985

    PubMed  Google Scholar 

  14. Steadman C, Talley NJ, Phillips SF, Van Dyke C: Selective 5-hydroxytryptamine type 3 receptor antagonism with ondansetron as treatment for diarrhea-predominant irritable bowel syndrome: A pilot study. Mayo Clin Proc 67:732–738, 1992

    PubMed  Google Scholar 

  15. Maxton DG, Haigh CG, Whorwell PJ: 5HT3 antagonists: A role in irritable bowel syndrome and non-ulcer dyspepsia? Gut 32:A1228, 1991

  16. Cubeddu LX, Hoffman IS, Fuenmayor NT, Finn AL: Efficacy of ondansetron (GR 38032F) and the role of serotonin in cisplatin-induced nausea and vomiting. N Engl J Med 322:810–816, 1990

    PubMed  Google Scholar 

  17. Marty M, Pouillart P, Scholl S, Droz JP, Azab M, Brion N, Pujade-Lauraine E, Paule B, Paes D, Bons J: Comparison of the 5-hydroxytryptamine3 (serotonin) antagonist ondansetron (GR 38032F) with high-dose metoclopramide in the control of cisplatin-induced emesis. N Engl J Med 322:816–821, 1990

    PubMed  Google Scholar 

  18. Talley NJ, Phillips SF, Melton LJ, Wiltgen C, Zinsmeister AR: A patient questionnaire to identify bowel disease. Ann Intern Med 111:671–674, 1989

    PubMed  Google Scholar 

  19. Thompson WG, Creed F, Drossman DA, Heaton KW, Mazzacca G: Functional bowel disease and functional abdominal pain. Gastroenterol Int 5:75–91, 1992

    Google Scholar 

  20. Pritchard JF: Ondansetron metabolism and pharmacokinetics. Semin Oncol 19(4 suppl 10):9–15, 1992

    Google Scholar 

  21. Azpiroz F, Malagelada J-R: Gastric tone measured by an electronic barostat in health and postsurgical gastroparesis. Gastroenterology 92:934–943, 1987

    PubMed  Google Scholar 

  22. Steadman CJ, Phillips SF, Camilleri M, Haddad AC, Hanson RB: Variation of muscle tone in the human colon. Gastroenterology 101:373–381, 1991

    PubMed  Google Scholar 

  23. Steadman CJ, Phillips SF, Camilleri M, Talley NJ, Haddad A, Hanson R: Control of muscle tone in the human colon. Gut 33:541–546, 1992

    PubMed  Google Scholar 

  24. Bell AM, Pemberton JH, Hanson RB, Zinsmeister AR: Variations in muscle tone of the human rectum: recordings with an electromechanical barostat. Am J Physiol 260:G17-G25, 1991

    PubMed  Google Scholar 

  25. Zighelboim J, Talley NJ, Phillips SF: Response of gastric fundus to rectal distension in healthy persons. Dig Dis Sci 39:1441–45, 1994

    PubMed  Google Scholar 

  26. Sritwtanakul K, Kelvie W, Lasagna L, Calimlim JF, Weis OF, Mehta G: Studies with different types of visual analog scales for measurement of pain. Clin Pharmacol Ther 34:234–239, 1983

    PubMed  Google Scholar 

  27. Sun WM, Read NW, Prior A, Daly J, Cheah SK, Grundy D: Sensory and motor responses to rectal distension vary according to rate and pattern of balloon inflation. Gastroenterology 99:1008–1015, 1990

    PubMed  Google Scholar 

  28. Spielberger DC: Manual for the State Trait Anxiety Inventory. Palo Alto, California, Consulting Psychologists Press, 1983

    Google Scholar 

  29. Feldman M, Walker P, Goldschmiedt M, Cannon D: Role of affect and personality in gastric acid secretion and serum gastrin concentration. Comparative studies in normal men and in male duodenal ulcer patients. Gastroenterology 102:175–180, 1992

    PubMed  Google Scholar 

  30. Derogatis LR: SCL-90-R Administration, Scoring and Procedures Manual II, 2nd ed. Clinical Psychometric Research, 1983

  31. McNair DM, Larr M, Droppleman LF: Manual: Profile of Mood States. San Diego, California, Educational and Industrial Testing Service, 1971

    Google Scholar 

  32. Eysenck HJ, Eysenck SB: Manual of the Eysenck Personality Inventory. London, University of London Press, 1964

    Google Scholar 

  33. Drossman DA, Leserman J, Nachman G, Li ZM, Gluch H, Toomey TC, Mitchell CM: Sexual and physical abuse in women with functional or organic gastrointestinal disorders. Ann Intern Med 113:828–833, 1990

    PubMed  Google Scholar 

  34. Costall B, Naylor RJ: Anxiolytic potential of 5-HT3 receptor antagonists. Pharmacol Toxicol 70:157–162, 1992

    PubMed  Google Scholar 

  35. Talley NJ, Kost L, Haddad A, Zinsmeister AR: Comparison of commercial serological tests for detection ofHelicobacter pylori antibodies. J Clin Microbiol 30:3146–3150, 1992

    PubMed  Google Scholar 

  36. Mearin F, Cucala M, Azpiroz F, Malagelada J-R: The origin of symptoms on the brain-gut axis in functional dyspepsia. Gastroenterology 101:999–1006, 1991

    PubMed  Google Scholar 

  37. Lémann M, Dederding JP, Flourié B, Franchisseur C, Rambaud JC, Jian R: Abnormal perception of visceral pain in response to gastric distension in chronic idiopathic dyspepsia: The irritable stomach syndrome. Dig Dis Sci 36:1249–1254, 1991

    PubMed  Google Scholar 

  38. Bradette M, Pare P, Douville P, Morin A: Visceral perception in health and functional dyspepsia: Crossover study of gastric distension with placebo and domperidone. Dig Dis Sci 36:52–58, 1991

    PubMed  Google Scholar 

  39. Kellow JE, Phillips SF: Altered small bowel motility in irritable bowel syndrome is correlated with symptoms. Gastroenterology 92:1885–1893, 1987

    PubMed  Google Scholar 

  40. Costantini M, Sturniolo GC, Zaninotto G, D'Inca R, Polo R, Naccarato R, Ancona E: Altered esophageal pain threshold in irritable bowel syndrome. Dig Dis Sci 38:206–212, 1993

    PubMed  Google Scholar 

  41. Scolapio JS, von der Ohe M, Hanson RB, Camilleri M: Post-prandial function of human ascending colon: A biphasic response involving a 5HT3 mechanism. Gastroenterology 104:A579, 1993

    Google Scholar 

  42. Walker EA, Roy-Byrne PP, Katon WJ: Irritable bowel syndrome and psychiatric illness. Am J Psychiatry 147:565–572, 1990

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  44. Stenger EM: Chronic back pain: View from a psychiatrist's office. Clin J Pain 8:242–246, 1992

    PubMed  Google Scholar 

  45. Talley NJ, Phillips SF, Bruce B, Twomey CK, Zinsmeister AR, Melton LJ III: Relation among personality and symptoms in nonucler dyspepsia and the irritable bowel syndrome. Gastroenterology 99:327–333, 1990

    PubMed  Google Scholar 

  46. Akervall S, Fasth S, Nordgren S, Oresland T, Hulten L: Rectal reservoir and sensory function studied by graded isobaric distension in normal man. Gut 30:496–502, 1989

    PubMed  Google Scholar 

  47. Talley NJ, Phillips SF: Non-ulcer dyspepsia: Potential causes and pathophysiology. Ann Intern Med 108:865–879, 1988

    PubMed  Google Scholar 

  48. Fozard JR: Neuronal 5-HT receptors in the periphery. Neuropharmacology 23:1473–1486, 1984

    PubMed  Google Scholar 

  49. Kilpatrick GJ, Jones BJ, Tyers MB: Identification and distribution of 5-HT3 receptors in rat brain using radioligand binding. Nature 330:746–748, 1987

    PubMed  Google Scholar 

  50. Kilpatrick GJ, Jones BJ, Tyers MB: Binding of the 5-HT3 ligand, (3H)GR65630, to rat area postrema, vagus nerve and the brains of several species. Eur J Pharmacol 159:157–164, 1989

    PubMed  Google Scholar 

  51. Goldberg PA, Kamm MA, Setti-Carraro P, Van Der Sijp JRM, Roth C: 5 HT3 antagonism does not modify visceral sensation or compliance in healthy subjects. Gastroenterology 104:A512, 1993

    Google Scholar 

  52. Wilmer A, Tack J, Coremans G, Janssens J, Vantrappen G: Effect of ondansetron, a 5-HT3-receptor antagonist, on perception of gastric distension and gastric compliance in healthy man. Gastroenterology 104:A603, 1993

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported in part by grants AG09440, DK32121, and RR585 from the National Institutes of Health.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zighelboim, J., Talley, N.J., Phillips, S.F. et al. Visceral perception in irritable bowel syndrome. Digest Dis Sci 40, 819–827 (1995). https://doi.org/10.1007/BF02064986

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02064986

Key words

Navigation