Gastroenterology

Gastroenterology

Volume 115, Issue 5, November 1998, Pages 1263-1271
Gastroenterology

Special Reports and Reviews
Is rectal pain sensitivity a biological marker for irritable bowel syndrome: Psychological influences on pain perception,☆☆

https://doi.org/10.1016/S0016-5085(98)70099-XGet rights and content

Abstract

Background & Aims: Rectal pain sensitivity has been called a biological marker for irritable bowel syndrome, but this conclusion may be premature. This article is a critical review of the evidence for psychological influences on perception. Methods: The world literature accessible through Index Medicus from 1973 to 1997 was systematically reviewed. Results: Evidence favoring a biological basis for pain sensitivity is that two thirds of patients report pain at abnormally low thresholds of rectal distention despite normal somatic pain thresholds. Pain thresholds are not correlated with anxiety or depression. Evidence favoring psychological influences on perception is that patients with the irritable bowel syndrome rate even sham distentions as more painful, and when perception tests that minimize psychological influences are used, they have normal sensory thresholds. Also, stress alters sensory thresholds. Sensitization by repeated distention has been cited as evidence of a biological basis for hyperalgesia, but it is not unique to patients with irritable bowel. Brain imaging shows that different regions are activated by painful distention in patients with irritable bowel syndrome, but this is consistent with psychological influences on perception. Conclusions: Psychological factors influence pain thresholds in patients with the irritable bowel syndrome. Two cognitive traits, selective attention to gastrointestinal sensations and disease attribution, may account for increased pain sensitivity.

GASTROENTEROLOGY 1998;115:1263-1271

Section snippets

Methodological considerations

This article is based on a review of the world literature that is indexed in Index Medicus for the years 1973–1997. Only articles relating to pain thresholds in patients with IBS were included; the literature on pain perception in functional dyspepsia and functional esophageal disorders was not surveyed. Search terms were irritable bowel, pain, barostat, and the names of selected authors known to have contributed to this literature. No non-English language articles that reported original data

Perceptual response bias

Nonperceptual factors, such as prior learning and the anticipated consequences of reporting pain, can affect the threshold at which pain is reported. For example, some subjects may report pain at a low intensity of stimulation to insure that they do not experience harm, whereas other subjects may deny pain even at levels of stimulation that cause tissue damage because they want to appear strong or stoical. When measuring perceptual sensitivity, the investigator normally tries to minimize these

Different approaches to measuring pain yield different outcomes

Twenty-seven studies of distention-related pain or discomfort were reviewed, some of which used more than one method of assessing sensory thresholds. When the balloon was inflated in a continuous or cumulative manner until the first report of pain or discomfort (AML method), 11 studies14, 17, 31, 32, 33, 34, 35, 36, 37, 38, 39 found lower thresholds in patients with IBS than in healthy controls and 5 studies10, 18, 40, 41, 42 found no difference. When phasic distentions were presented in an

Thresholds for nonpainful sensations produced by distention

If response bias caused by negative emotions such as anxiety influence perception in patients with IBS, one would expect response bias to be strongest for pain, which is a potentially threatening sensation, weakest for nonthreatening sensations such as the lowest detectable distention, and intermediate for urgency to defecate. Conversely, if visceral hypersensitivity is primarily due to biological differences between IBS patients and controls, one might expect patients with IBS to differ from

Pain from the skin

If increased pain sensitivity in patients with IBS is part of a neurotic tendency to label any aversive stimulus as painful, one would expect IBS patients to have lower thresholds for pain produced by aversive stimuli applied to the skin as well as lower thresholds for gastrointestinal distention. Six studies have tested this hypothesis,28, 34, 35, 46, 51, 55 and all 6 found patients with IBS to be either similar to or less sensitive than healthy controls to painful stimulation of the skin.

Experimental manipulation of psychological state: Effects on pain threshold

If patients with IBS are more sensitive to visceral pain because of psychological bias, interventions that reduce negative emotional states should raise the pain threshold and result in fewer or less severe reports of pain. Consistent with this hypothesis, Prior et al.28 reported that, in patients with diarrhea-predominant IBS, the thresholds for gas, stool, urge, and discomfort were all significantly increased during hypnosis compared with pretreatment. Ford et al.21 reported that stress

Sensitization by repeated distention of the rectum

Munakata et al.25 reported that repeated distentions of the rectum at a painful intensity caused sensitization (i.e., reduced sensory thresholds) in patients with IBS but not in healthy controls. If sensitization is indeed unique to IBS patients, this would suggest that visceral hypersensitivity in IBS has a biological basis. However, others have observed sensitization phenomena in healthy controls43, 56 and in laboratory rats.57

Activation of different regions of the brain by rectal distention

Silverman et al.52 used positron emission tomography (PET scanning) to show that rectal distention caused activation of different regions of the brain in IBS patients compared with controls both during painful distention of the rectum and in response to the anticipation of painful distention (i.e., during blank trials). Distention caused activation of the anterior cingulate gyrus in healthy controls, but caused activation of the left prefrontal cortex in patients with IBS. Thus, there is an

Correlation of psychological traits with sensory thresholds

If lower pain thresholds in patients with IBS are a result of psychological influences on perception, one would expect to see a correlation between pain thresholds and psychological test scores. In 8 of 10 studies addressing this question,10, 25, 28, 34, 43, 44, 45, 47, 48, 55 these correlations were not statistically significant: traditionally defined psychological traits such as anxiety, depression, and neuroticism are not predictive of pain thresholds. However, somatization as measured by

A model to account for perceptual response bias

Figure 1 shows a schematic representation of how psychological factors may interact with physiological events to affect pain perception and related health outcomes.

. Schematic model showing how cognitive/psychological, physiological, and methodological factors may interact to influence the threshold for pain produced by rectal distention. The model suggests that the threshold for pain influences the frequency and severity of clinical pain and the utilization of health care services by patients

Summary and conclusions

Observations that have been cited as evidence for a biological basis for visceral hyperalgesia are as follows: (1) Approximately two thirds of patients with IBS report pain or discomfort at a lower threshold than healthy controls. (2) Patients with IBS have larger areas and/or atypical areas of somatic referral than healthy controls when the rectum is distended. This has been interpreted as evidence for sensitization of spinal afferents. (3) Pain thresholds are not correlated with anxiety or

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    Address requests for reprints to: William E. Whitehead, Ph.D., Division of Digestive Diseases and Nutrition, Campus Box 7080, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7080. e-mail: [email protected]; fax: (919) 966-6842.

    ☆☆

    Supported by National Institutes of Health grants KO5 MH00133 and RO1 DK31369 and by a grant from Solvay Pharmaceuticals.

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