GUT 1997;41:505-512 ( October )

Evidence for two distinct perceptual alterations in irritable bowel syndrome

B D Naliboff,^a J Munakata,^ab S Fullerton,^ab R H Gracely,^e A Kodner,^a F Harraf,^a E A Mayer^ac

^a CURE Digestive Diseases Research Center/Neuroenteric Disease Program, WLA VA Medical Center, and UCLA, Los Angeles, CA 90073, USA, ^b Department of Medicine, ^c Department of Physiology, ^d Department of Psychology, ^e Neuropathic Pain and Pain Assessment Section, NAB, NIDR, NIH, Bethesda, MD 20892, USA

Correspondence to: Dr B D Naliboff, WLA VA Medical Center, Neuroenteric Biology Group, Bldg 115/CURE, 11301 Wilshire Blvd, Los Angeles, CA 90073, USA.

Accepted for publication 2 May 1997

Background and aimsVisceral hyperalgesia has been implicated as a factor contributing to symptom generation in irritable bowel syndrome (IBS). However, previous studies using intestinal balloon distension have used psychophysical procedures which do not provide adequate and unbiased measures of visceral sensitivity.
MethodsThree psychophysical tasks were examined in 45 patients with IBS (positive Rome criteria) and 14 controls using rectal balloon distension with a computerised distension device. Discomfort threshold and tolerance were assessed during an ascending series of phasic pressure stimuli and during an interactive threshold tracking procedure. In addition, stimulus response functions were generated from intensity and unpleasantness ratings of the rectal distensions.
ResultsDiscomfort threshold and tolerance for the ascending stimuli were significantly lower for the patients with IBS compared with the controls. In contrast, discomfort thresholds during the tracking procedure and stimulus response curves for the ascending series were not different between the groups. A factor analysis of the psychophysical data was consistent with the presence of two distinct and unrelated perceptual alterations related to rectal distension: hypervigilance for visceral stimuli, manifested as lowered response criteria for using the descriptor "discomfort"; and rectal hypersensitivity, manifested as a lower discomfort threshold and left shift of the stimulus response curves.
ConclusionsPatients with IBS as a group have a greater propensity to label visceral sensations negatively and show a lower tolerance for rectal balloon distension. A subgroup of patients also have baseline rectal hypersensitivity, assessed by unbiased measures of discomfort threshold and stimulus intensity judgements.
(GUT 1997;41:505-512)

Keywords: irritable bowel syndrome;  visceral hypersensitivity;  pain threshold

---

© 1997 by Gut
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

Relevant Article

Opening the doors of perception in the irritable bowel syndrome

LESLEY A HOUGHTON and P J WHORWELL
Gut 1997 41: 567-568. [Extract] [Full Text] [PDF]

This article has been cited by other articles:

• Malin, S. A., Christianson, J. A., Bielefeldt, K., Davis, B. M. (2009). TRPV1 Expression Defines Functionally Distinct Pelvic Colon Afferents. J. Neurosci. 29: 743-752 [Abstract] [Full Text]  
• Naliboff, B. D., Waters, A. M., Labus, J. S., Kilpatrick, L., Craske, M. G., Chang, L., Negoro, H., Ibrahimovic, H., Mayer, E. A., Ornitz, E. (2008). Increased Acoustic Startle Responses in IBS Patients During Abdominal and Nonabdominal Threat. Psychosom. Med. 70: 920-927 [Abstract] [Full Text]  
• Naliboff, B. D., Frese, M. P., Rapgay, L. (2008). Mind/Body Psychological Treatments for Irritable Bowel Syndrome. Evid Based Complement Alternat Med 5: 41-50 [Abstract] [Full Text]  
• Mayer, E A, Bradesi, S, Chang, L, Spiegel, B M R, Bueller, J A, Naliboff, B D (2008). Functional GI disorders: from animal models to drug development. Gut 57: 384-404 [Abstract] [Full Text]  
• Berman, S. M., Naliboff, B. D., Suyenobu, B., Labus, J. S., Stains, J., Ohning, G., Kilpatrick, L., Bueller, J. A., Ruby, K., Jarcho, J., Mayer, E. A. (2008). Reduced Brainstem Inhibition during Anticipated Pelvic Visceral Pain Correlates with Enhanced Brain Response to the Visceral Stimulus in Women with Irritable Bowel Syndrome. J. Neurosci. 28: 349-359 [Abstract] [Full Text]  
• Spiller, R, Aziz, Q, Creed, F, Emmanuel, A, Houghton, L, Hungin, P, Jones, R, Kumar, D, Rubin, G, Trudgill, N, Whorwell, P (2007). Guidelines on the irritable bowel syndrome: mechanisms and practical management. Gut 56: 1770-1798 [Abstract] [Full Text]  
• Dorn, S. D, Palsson, O. S, Thiwan, S. I M, Kanazawa, M., Clark, W C., van Tilburg, M. A L, Drossman, D. A, Scarlett, Y., Levy, R. L, Ringel, Y., Crowell, M. D, Olden, K. W, Whitehead, W. E (2007). Increased colonic pain sensitivity in irritable bowel syndrome is the result of an increased tendency to report pain rather than increased neurosensory sensitivity. Gut 56: 1202-1209 [Abstract] [Full Text]  
• Coen, S. J., Gregory, L. J., Yaguez, L., Amaro, E. Jr., Brammer, M., Williams, S. C. R., Aziz, Q. (2007). Reproducibility of human brain activity evoked by esophageal stimulation using functional magnetic resonance imaging. Am. J. Physiol. Gastrointest. Liver Physiol. 293: G188-G197 [Abstract] [Full Text]  
• Lu, C.-L., Liu, C.-C., Fuh, J.-L., Liu, P.-Y., Wu, C.-W., Chang, F.-Y., Lee, S.-D. (2007). Irritable bowel syndrome and negative appendectomy: a prospective multivariable investigation. Gut 56: 655-660 [Abstract] [Full Text]  
• Harris, M. L., Hobson, A. R., Hamdy, S., Thompson, D. G., Akkermans, L. M., Aziz, Q. (2006). Neurophysiological evaluation of healthy human anorectal sensation. Am. J. Physiol. Gastrointest. Liver Physiol. 291: G950-G958 [Abstract] [Full Text]  
• Chang, L., Mayer, E. A., Labus, J. S., Schmulson, M., Lee, O. Y., Olivas, T. I., Stains, J., Naliboff, B. D. (2006). Effect of sex on perception of rectosigmoid stimuli in irritable bowel syndrome. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291: R277-R284 [Abstract] [Full Text]  
• Berman, S. M., Naliboff, B. D., Suyenobu, B., Labus, J. S., Stains, J., Bueller, J. A., Ruby, K., Mayer, E. A. (2006). Sex differences in regional brain response to aversive pelvic visceral stimuli. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291: R268-R276 [Abstract] [Full Text]  
• Moshiree, B, Zhou, Q, Price, D D, Verne, G N (2006). Central sensitisation in visceral pain disorders. Gut 55: 905-908 [Abstract] [Full Text]  
• Lackner, J. M., Gudleski, G. D., Zack, M. M., Katz, L. A., Powell, C., Krasner, S., Holmes, E., Dorscheimer, K. (2006). Measuring health-related quality of life in patients with irritable bowel syndrome: can less be more?. Psychosom. Med. 68: 312-320 [Abstract] [Full Text]  
• Kwan, C. L., Diamant, N. E., Pope, G., Mikula, K., Mikulis, D. J., Davis, K. D. (2005). Abnormal forebrain activity in functional bowel disorder patients with chronic pain. Neurology 65: 1268-1277 [Abstract] [Full Text]  
• Tillisch, K, Mayer, E A, Labus, J S, Stains, J, Chang, L, Naliboff, B D (2005). Sex specific alterations in autonomic function among patients with irritable bowel syndrome. Gut 54: 1396-1401 [Abstract] [Full Text]  
• Chan, C L H, Lunniss, P J, Wang, D, Williams, N S, Scott, S M (2005). Rectal sensorimotor dysfunction in patients with urge faecal incontinence: evidence from prolonged manometric studies. Gut 54: 1263-1272 [Abstract] [Full Text]  
• Brierley, S. M, Carter, R, Jones, W III, Xu, L., Robinson, D. R, Hicks, G. A, Gebhart, G. F, Blackshaw, L. A. (2005). Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J. Physiol. 567: 267-281 [Abstract] [Full Text]  
• Vandenberghe, J, Vos, R, Persoons, P, Demyttenaere, K, Janssens, J, Tack, J (2005). Dyspeptic patients with visceral hypersensitivity: sensitisation of pain specific or multimodal pathways?. Gut 54: 914-919 [Abstract] [Full Text]  
• Spiller, R. C. (2005). Irritable bowel syndrome. Br Med Bull 72: 15-29 [Abstract] [Full Text]  
• Wilder-Smith, C H, Schindler, D, Lovblad, K, Redmond, S M, Nirkko, A (2004). Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls. Gut 53: 1595-1601 [Abstract] [Full Text]  
• Posserud, I, Agerforz, P, Ekman, R, Bjornsson, E S, Abrahamsson, H, Simren, M (2004). Altered visceral perceptual and neuroendocrine response in patients with irritable bowel syndrome during mental stress. Gut 53: 1102-1108 [Abstract] [Full Text]  
• Guthrie, E., Barlow, J., Fernandes, L., Ratcliffe, J., Read, N., Thompson, D. G., Tomenson, B., Creed, F. (2004). Changes in Tolerance to Rectal Distension Correlate With Changes in Psychological State in Patients With Severe Irritable Bowel Syndrome. Psychosom. Med. 66: 578-582 [Abstract] [Full Text]  
• Kang, Y.-M., Bielefeldt, K., Gebhart, G. F. (2004). Sensitization of Mechanosensitive Gastric Vagal Afferent Fibers in the Rat by Thermal and Chemical Stimuli and Gastric Ulcers. J. Neurophysiol. 91: 1981-1989 [Abstract] [Full Text]  
• Guthrie, E, Creed, F, Fernandes, L, Ratcliffe, J, Van der Jagt, J, Martin, J, Howlett, S, Read, N, Barlow, J, Thompson, D, Tomenson, B (2003). Cluster analysis of symptoms and health seeking behaviour differentiates subgroups of patients with severe irritable bowel syndrome. Gut 52: 1616-1622 [Abstract] [Full Text]  
• Qin, C., Greenwood-Van Meerveld, B., Myers, D. A., Foreman, R. D. (2003). Corticosterone Acts Directly at the Amygdala to Alter Spinal Neuronal Activity in Response to Colorectal Distension. J. Neurophysiol. 89: 1343-1352 [Abstract] [Full Text]  
• Birder, L. A., Kiss, S., de Groat, W. C., Lecci, A., Maggi, C. A. (2003). Effect of Nepadutant, a Neurokinin 2 Tachykinin Receptor Antagonist, on Immediate-Early Gene Expression after Trinitrobenzenesulfonic Acid-Induced Colitis in the Rat. J. Pharmacol. Exp. Ther. 304: 272-276 [Abstract] [Full Text]  
• Houghton, L A, Calvert, E L, Jackson, N A, Cooper, P, Whorwell, P J (2002). Visceral sensation and emotion: a study using hypnosis. Gut 51: 701-704 [Abstract] [Full Text]  
• Mertz, H (2002). Role of the brain and sensory pathways in gastrointestinal sensory disorders in humans. Gut 51: i29-33 [Abstract] [Full Text]  
• Delvaux, M (2002). Role of visceral sensitivity in the pathophysiology of irritable bowel syndrome. Gut 51: i67-71 [Abstract] [Full Text]  
• Okano, S., Ikeura, Y., Inatomi, N. (2002). Effects of Tachykinin NK1 Receptor Antagonists on the Viscerosensory Response Caused by Colorectal Distention in Rabbits. J. Pharmacol. Exp. Ther. 300: 925-931 [Abstract] [Full Text]  
• Okano, S., Nagaya, H., Ikeura, Y., Natsugari, H., Inatomi, N. (2001). Effects of TAK-637, a Novel Neurokinin-1 Receptor Antagonist, on Colonic Function in Vivo. J. Pharmacol. Exp. Ther. 298: 559-564 [Abstract] [Full Text]  
• Naliboff, B. D., Derbyshire, S. W. G., Munakata, J., Berman, S., Mandelkern, M., Chang, L., Mayer, E. A. (2001). Cerebral Activation in Patients With Irritable Bowel Syndrome and Control Subjects During Rectosigmoid Stimulation. Psychosom. Med. 63: 365-375 [Abstract] [Full Text]  
• Feinle, C, Meier, O, Otto, B, D'Amato, M, Fried, M (2001). Role of duodenal lipid and cholecystokinin A receptors in the pathophysiology of functional dyspepsia. Gut 48: 347-355 [Abstract] [Full Text]  
• Jones, J, Boorman, J, Cann, P, Forbes, A, Gomborone, J, Heaton, K, Hungin, P, Kumar, D, Libby, G, Spiller, R, Read, N, Silk, D, Whorwell, P (2000). British Society of Gastroenterology guidelines for the management of the irritable bowel syndrome. Gut 47: ii1-19 [Full Text]  
• Chang, L, Munakata, J, Mayer, E A, Schmulson, M J, Johnson, T D, Bernstein, C N, Saba, L, Naliboff, B, Anton, P A, Matin, K (2000). Perceptual responses in patients with inflammatory and functional bowel disease. Gut 47: 497-505 [Abstract] [Full Text]  
• Burke, P., Elliott, M., Fleissner, R. (1999). Irritable Bowel Syndrome and Recurrent Abdominal Pain: A Comparative Review. Psychosomatics 40: 277-285 [Abstract] [Full Text]  
• Siproudhis, L, Bellissant, E, Juguet, F, Allain, H, Bretagne, J-F, Gosselin, M (1999). Perception of and adaptation to rectal isobaric distension in patients with faecal incontinence. Gut 44: 687-692 [Abstract] [Full Text]  
• Coutinho, S. V., Plotsky, P. M., Sablad, M., Miller, J. C., Zhou, H., Bayati, A. I, McRoberts, J. A., Mayer, E. A. (2002). Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am. J. Physiol. Gastrointest. Liver Physiol. 282: G307-G316 [Abstract] [Full Text]