Digestive Diseases and Sciences

, Volume 46, Issue 11, pp 2542–2548

Pain Hypersensitivity in Patients with Functional Gastrointestinal Disorders: A Gastrointestinal-Specific Defect or a General Systemic Condition?

  • M. Bouin
  • P. Meunier
  • M. Riberdy-Poitras
  • P. Poitras
Article

Abstract

Visceral hypersensitivity was shown in patients with functional gastrointestinal disorders (FGID). The mechanisms underlying this sensory dysfunction remain undetermined. The initial hypothesis of a generalized reduction in pain tolerance was rejected by further studies that suggested a normal tolerance to somatic stimuli and led to the generally accepted assumption that pain intolerance is specific and exclusive for visceral stimuli in these patients. We wanted to revisit this theory by examining whether patients with FGID reported perception and tolerance to somatic pain differently from normal subjects and whether the response to somatic pain stimulus was correlated to gastrointestinal symptoms or psychological status or distress. Thirty-three patients with FGID (Rome II criteria)(F/M: 26/7; mean age 48 ± 9.9) and 33 normal controls (F/M: 24/9; mean age 44.1 ± 6.8) were asked to immerse their nondominant hand into 4°C water for as long as possible (maximum 120 sec). Time before appearance of: (1) discomfort, (2) pain, and (3) withdrawing of the hand were noted. The intensity of pain was rated on a visual analog scale from 0 to 100. Self-report questionnaires were used to assess the severity of gastrointestinal symptoms (St-Luc GI index) and the psychological distress (SCL-90) in the patient group. Data are expressed in seconds as mean ± sem. Discomfort sensory thresholds were similar in controls and FGID patients (28 ± 3 and 24 ± 2, respectively; NS) whereas pain and withdrawing were significantly lower in FGID (41 ± 3 and 76 ± 6 sec) than in controls (62 ± 6 and 102 ± 4; P < 0.05). Pain intensity was similar in both groups (64 ± 4 vs 67 ± 3; NS). Female patients showed lower sensory thresholds than male patients and control females (pain thresholds: 39.8 ± 3.4 vs 67.8 ± 16.7 and vs 56.8 ± 8.7; P < 0.05). Sensory thresholds were not different in subgroups of patients with FGID (irritable bowel syndrome and functional dyspepsia). No correlation was shown between sensory thresholds and gastrointestinal index or SCL 90-test. In conclusion, FGID patients showed a threshold to painful somatic stimulus that was lower than in normal subjects. These findings suggest that patients with FGID may have hyperalgesia and low pain tolerance that is not limited to the viscera, but that is part of a systemic general condition.

dyspepsia functional gastrointestinal disorder irritable bowel syndrome pain sensitivity 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. 1.
    Jones R, Lydeard S: Irritable bowel syndrome in the general population. Br Med J 304:87–90, 1992Google Scholar
  2. 2.
    Longstreth GF, Wolde-Tsadik G: Irritable bowel-type symptoms in HMO examinees. Dig Dis Sci 389:1581–1589, 1993Google Scholar
  3. 3.
    Ritchie J: Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14:125–132, 1973Google Scholar
  4. 4.
    Mertz H, Naliboff B, Munakata J, Niazi N, Mayer E: Altered rectal perception is a biological marker of patients with irritable bowel syndrome. Gastroenterology 109:40–52, 1995Google Scholar
  5. 5.
    Prior A, Sorial E, 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, 1993Google Scholar
  6. 6.
    Naliboff BD, Munakata J, Fullerton S, Gracely RH, Kodner A, Harraf F, Mayer EA: Evidence for two distinct perceptual alterations in irritable bowel syndrome. Gut 41:505–512, 1997Google Scholar
  7. 7.
    Lembo T, Munakata J, Mertz H, Niazi N, Kodner A, Nikas V, Mayer EA: Evidence for the hypersensitivity of lumbar splanchnic afferents in irritable bowel syndrome. Gastroenterology 107:1686–1696, 1994Google Scholar
  8. 8.
    Mayer EA, Gebhart GF: Basic and clinical aspects of visceral hypergesia. Gastroenterology 107:271–293, 1994Google Scholar
  9. 9.
    Whitehead WE, Palsson OS: Is rectal pain sensitivity a biological marker for irritable bowel syndrom: Psychological influences on pain perception. Gastroenterology 115:1263–1271, 1998Google Scholar
  10. 10.
    Accarino AM, Aspiroz F, Malagelada JR: Selective dysfunction of mechanosensitive intestinal afferents in irritable bowel syndrome. Gastroenterology 108:636–643, 1995Google Scholar
  11. 11.
    Latimer P, Campbell D, Latimer M, Sarna S, Daniel E, Waterfall W: Irritable bowel syndrome: A test of the colonic hyperalgesia hypothesis. J Behav Med 23:285–295, 1979Google Scholar
  12. 12.
    Whitehead WE, Bosmajian L, Zonderman AD, Costa PT Jr, Schuster MM: Symptoms of psychologic distress associated with irritable bowel syndrome: Comparison of community and medical clinic samples. Gastroenterology 95:709–714, 1988Google Scholar
  13. 13.
    Drossman DA, McKee DC, Sandler RS, Mitchell CM, Cramer EM, Lowman BC, Burger AL: Psychological factors in the irritable bowel syndrome. A multi-variate study of patients and nonpatients with irritable bowel syndrome. Gastroenterology 95:701–708, 1988Google Scholar
  14. 14.
    Cook IJ, Van Eeden A, Collins SM: Patients with irritable bowel syndrome have greater pain tolerance than normal subjects. Gastroenterology 93:727–733, 1987Google Scholar
  15. 15.
    Whitehead WE, Holtkotter B, Enck P, Hoelzl R, Holmes KD, Anthony J, Shabsin HS, Schuster MM: Tolerance for rectosigmoid distension in irritable bowel syndrome. Gastroenterology 98:1187–1192, 1990Google Scholar
  16. 16.
    Thumshirn M, Coulie B, Camilleri M, Zinsmeister AR, Burton DD, van Dyke C: Effects of alosetron on gastrointestinal transit time and rectal sensation in patients with irritable bowel syndrome. Aliment Pharmacol Ther 14(7):869–878, 2000Google Scholar
  17. 17.
    Poitras P, Riberdy Poitras M, Plourde V, Boivin M, Verrier P: Evolution of visceral sensitivity in IBS patients treated by group psychotherapy or amitriptyline. (submitted)Google Scholar
  18. 18.
    Bouin M, Poitras P, Boivin M, Laganière M, Devroede G, Plourde V: Visceral pain processing in patients with painfull or painless functional bowel disorders. Gastroenterology 120:A3228, 2001Google Scholar
  19. 19.
    Thompson WG, Creed F, Drossman DA, Heaton KW, Mazzacca G: Functional bowel disease and functional abdominal pain. Gastroenterology International 5:75–91, 1992Google Scholar
  20. 20.
    Drossman DA, Corazziari E, Talley NJ, Thompson WG, Whitehead WE: Rome II: Multinational Consensus Document on Functional Gastrointestinal Disorders. Gut 45(suppl II):II1–II81, 1999Google Scholar
  21. 21.
    Sritwtanakul K, Kelvie W, Iasagna L, Calimlin JF, Weis OF, Metha G: Studies with different types of visual analog scales for measurement of pain. Clin Pharmacol Ther 34:234–239, 1983Google Scholar
  22. 22.
    Derogatis LR, Rickels K, Rock AF: The SCL-90 and the MMPI: A step in the validation of a new self-report scale. Br J Psychiatry 128:280–289, 1976Google Scholar
  23. 23.
    Riberdy Poitras M, Verrier P, So C, Poitras P: Group counseling psychotherapy for patients with functional gastrointestinal disorders. (submitted)Google Scholar
  24. 24.
    Huet PM, Deslauriers J, Tran A, Faucher C, Charbonneau J: Impact of fatigue on the quality of life of patients with primary biliary cirrhosis. Am J Gastroenterol 95:760–767, 2000Google Scholar
  25. 25.
    Verne GE, Price DD, Robinson ME: Hypersensibility to cutaneous (heat induced) pain in the irritable bowel syndrome. Gastroenterology 118(4, suppl 2):A4433, 2000Google Scholar
  26. 26.
    Ploghaus A, Tracey I, Gati J, Clare S, Menon R, Matthews P, Rawlins J: Dissociating pain from its anticipation in the human brain. Science 284:1979–1981, 1999Google Scholar
  27. 27.
    Accarino AM, Azpiroz F, Malagelada JR: Focusing attention at the gut: effects on viscero-visceral reflexes and perception. Gastroenterology 104:A468, 1993Google Scholar
  28. 28.
    Drossman DA, Creed FH, Olden KW, Svedlund J, Toner BB, Whitehead WE: Psychological aspect of the functional gastrointestinal disorder. Gut 45(suppl II):II25–II30, 1999Google Scholar
  29. 29.
    Blanchard EB: Irritable bowel syndrome. In Psychophysiological Disorders. RJ Gatchel EB Blanchard (eds). Washington, DC, American Psychological Association, 1993, pp 23–62Google Scholar
  30. 30.
    Verrier P, Boivin M, Charbonneau J, Reeves N, Renaud S, Poitras P, Devroede G, Laganiere M, Plounde V: Patients presenting with functional abdominal pain: Evidence that visceral hyperalgesia is not associated with some degree of global amplification of symptoms. Gastroenterology 112(4):A846, 1997Google Scholar
  31. 31.
    Gear RW, Miaskowski C, Gordon N, Paul S, Heller P, Levine J: Kappa opioids produce significantly greater analgesia in women than in men. Nature Med 2:1248–1250, 1996Google Scholar
  32. 32.
    Giamberadino MA, Berkley KJ, Iezzi S, deBigonlina P, Vecchiet L: Changes in skin and muscle sensitivity in dysmenorrheic vs. normal women as a function of body site and monthly cycle. Soc Neurosci Abstr 21:1638, 1995Google Scholar
  33. 33.
    Berkley KJ: Sex differences in pain. Behav Brain Sci 20: 371–380, 1997Google Scholar
  34. 34.
    Unruh AM: Gender variations in clinical pain experience. Pain 65:123–167, 1996Google Scholar
  35. 35.
    Jackson NA, Houghton LA, Whorwell PJ: The menstrual cycle affects rectal visceral sensitivity in patients with irritable bowel syndrome (IBS) but not healthy volunteers. Gastroenterol 112:A1132, 1997 (abstract)Google Scholar
  36. 36.
    Munakata J, Naliboff B, Harraf F, Kodnek A, Lembo T, Chang L, Silverman DH, Meyer EA: Repetitive sigmoid stimulation induces rectal hyperalgesia in patients with irritable bowel syndrome. Gastroenterol 112:55–63, 1997Google Scholar
  37. 37.
    Fillingim R, Maixner W: Gender differences in the responses to noxious stimuli. Pain Forum 4:209–221, 1995Google Scholar
  38. 38.
    Mayer EA, Naliboff B, Lee O, Munakata J, Chang L: Genderrelated differences in functional gastrointestinal disorders. Aliment Pharmacol Ther 13(suppl 2):65–69, 1999Google Scholar
  39. 39.
    Ali A, Richardson D, Toner B: Feminine gender role and illness behaviour in irritable bowel syndrome. J Gender Culture Health 3(1):59–65, 1998Google Scholar
  40. 40.
    Toner BB, Akman D: Gender role and irritable bowel syndrome: Literature review and hypothesis. Am J Gastroenterol 95(1):11–15, 2000Google Scholar

Copyright information

© Plenum Publishing Corporation 2001

Authors and Affiliations

  • M. Bouin
    • 1
  • P. Meunier
    • 1
  • M. Riberdy-Poitras
    • 1
  • P. Poitras
    • 1
  1. 1.Hôpital Saint-LucUniversité de MontréalMontréalCanada

Personalised recommendations