Special Reports and ReviewsIs rectal pain sensitivity a biological marker for irritable bowel syndrome: Psychological influences on pain perception☆,☆☆
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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.
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.
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Supported by National Institutes of Health grants KO5 MH00133 and RO1 DK31369 and by a grant from Solvay Pharmaceuticals.