THE AMERICAN JOURNAL OF GASTROENTEROLOGY
1, 2000
© 2000 by Am. Coll. of Gastroenterology
Published by Elsevier Science Inc.
Correlation of Symptom Criteria With
Perception Thresholds During Rectosigmoid
Distension in Irritable Bowel Syndrome Patients
Max Schmulson, M.D., Lin Chang, M.D., Bruce Naliboff, Ph.D., Oh Young Lee, M.D., and
Emeran A. Mayer, M.D.
UCLA/CURE Neuroenteric Disease Program, Department of Medicine and Physiology, UCLA School of
Medicine, Los Angeles, California
OBJECTIVE: Due to a lack of reliable biological markers, the
diagnosis of irritable bowel syndrome (IBS) is based on
symptom criteria. The possible physiological correlates of
these criteria are not known. Our aims were to identify
correlations of currently used IBS symptom criteria with
distinct alterations in visceral perception.
METHODS: Forty-two IBS patients (51% women) with a
mean age of 39.5 ⫾ 1.4 yr, were included; 64% of patients
were recruited from advertisement and 36% were clinic
referrals. Patients completed a bowel symptom question-
naire, which included the Rome criteria and symptom
severity ratings. Rectal discomfort thresholds were eval-
uated in all patients and in 19 controls, using a nonbiased
tracking protocol consisting of phasic rectal balloon dis-
tensions before (PreTh) and after (PostTh) repetitive,
high-pressure sigmoid distensions. We assessed the effect
of each Rome criteria and symptom severity on PreTh and
PostTh.
RESULTS: IBS symptom severity was reported as moderate
in 38.1% and as severe in 61.9% of patients. Overall, lower
thresholds were observed in IBS patients than in controls
(PreTh: 28.2 ⫾ 1.7 vs 36.3 ⫾ 2.8 mm Hg, p ⬍ 0.05; PostTh:
25.3 ⫾ 1.5 vs 34.2 ⫾ 2.7 mm Hg, p ⬍ 0.01). When
assessing the effect of Rome criteria on rectal thresholds, we
found that patients with hard/lumpy stools had lower thresh-
olds than those without them, whereas patients with loose
watery stools had higher thresholds than those who lacked
them (both p ⬍ 0.05). The lowering of rectal discomfort
thresholds after sigmoid stimulation was observed regard-
less of the presence or absence of any Rome criteria or
symptom severity.
CONCLUSION: Although a decrease in rectal discomfort
thresholds after sigmoid stimulation is seen in IBS re-
gardless of specific symptoms, baseline and postsigmoid
stimulation thresholds are lower in IBS patients with
constipation-related symptoms. (Am J Gastroenterol
2000;95:152–156. © 2000 by Am. Coll. of Gastroenter-
ology)
Vol. 95, No.
ISSN 0002-9270/00/$20.00
PII S0002-9270(99)00736-4
INTRODUCTION
Irritable bowel syndrome (IBS) is a chronic functional in-
testinal disorder characterized by abdominal pain or discom-
fort and disturbed defecation, including altered stool con-
sistency, altered bowel movement frequency, urgency,
straining, belief of incomplete evacuation, and abdominal
bloating or distension (1). The diagnosis of IBS is based on
symptom criteria known as the Rome criteria, which were
developed from the review of previous studies using a
consensus of experts (1). An important concern is that these
criteria have not been validated, mainly due to the lack of
universal and specific biological markers for IBS.
The lack of biological markers unique to IBS is related to
a poor understanding of IBS pathophysiology. Alterations in
intestinal and colonic motility such as jejunal clustered
contractions and increased gastrocolonic response have
been reported (2, 3), but are not consistently present in IBS.
One of the most reproducible findings in IBS patients is an
enhanced sensitivity to rectosigmoid balloon distension (4 –
7). Together with the clinical observations of a tender sig-
moid colon and enhanced discomfort during sigmoidoscopic
examinations, these findings suggest an important role of
visceral hypersensitivity in the symptom generation of IBS
(8, 9). Reports of visceral hypersensitivity probably include
both a hypervigilance toward rectosigmoid discomfort and
pain, and visceral hyperalgesia (10). In addition, Munakata
et al. have recently shown that high-pressure, repetitive
stimulation of the sigmoid colon consistently results in the
development of rectal hyperalgesia in IBS patients and not
in controls (11), possibly reflecting an inadequate activation
of antinociceptive systems in response to a noxious visceral
stimulus in IBS (12).
In the current study, we sought to examine the relation-
ship between rectal discomfort thresholds before and after
sigmoid stimulation and subjective symptoms. Specifically,
we wanted to examine whether there was any relationship
between Rome symptom criteria and self-reported symptom
severity with rectal discomfort thresholds before and after
sigmoid stimulation. Part of these results have previously
been reported in abstract form (13).
AJG – January, 2000
PATIENTS AND METHODS
Patients
Forty-two consecutive IBS patients encountered at the
UCLA/CURE Neuroenteric Disease Program between 1996
and 1997 were included. Twenty-seven patients (64.0%)
were recruited from advertisement and 15 (36.0%) were
clinic referrals. The diagnosis of IBS was made using Rome
criteria (1) after organic disease was excluded.
Before their initial assessment, patients completed a
bowel symptom questionnaire (BSQ), which included Rome
symptom criteria for IBS and general symptom severity
ratings. Patients were asked if in the past 3 months they had
noticed continuous or repeated discomfort or pain in the
lower abdomen; if the pain or discomfort was typically
relieved by a bowel movement; if it was typically associated
with change in frequency of bowel movements; and if it was
typically associated with change in stool consistency. In
addition, patients were asked if at least one-quarter of the
time in the last 3 months they had experienced any of the
following: fewer than three bowel movements in a week;
more than three bowel movements a day; hard and/or lumpy
stools; loose and/or watery stools; straining during a bowel
movement; urgency (having to rush to the bathroom for a
bowel movement); belief of incomplete bowel movement;
passing mucus (white material during a bowel movement);
or abdominal fullness, bloating, or swelling.
Regarding symptom severity, patients were asked to rate
their usual symptoms as mild (can be ignored if you don’t
think about it); moderate (cannot be ignored, but does not
affect your lifestyle); severe (affects your lifestyle); or very
severe (markedly affects your lifestyle).
Visceral Distension Protocol
All IBS patients and 19 healthy controls without gastroin-
testinal (GI) or other pain conditions, recruited by adver-
tisement, underwent a visceral distension protocol. As pre-
viously described (11), distension of the sigmoid colon and
rectum was effected by air inflation of a double-balloon
catheter. The use of a computer-driven displacement device
that controls volume and pressure (barostat) allowed for the
inflation of the balloons. The device was programmed to
deliver distensions at a rapid volume rate (870 ml/min) to
constant pressure plateaus, and to log the sensations (i.e., no
sensation, moderate sensation, discomfort, and pain) from a
pushbutton marker device. The double-balloon catheter con-
sisted of two identical latex balloons (external diameter, 5
cm; length of each balloon, 9 cm) attached to a silastic
elastomer tube (external diameter, 18F) at both proximal
and distal ends (MAK-LA, Los Angeles, CA). The distance
between the balloons was 9 cm. Before and after completion
of every procedure, each balloon was inflated to exclude a
leak. Using sigmoidoscopic guidance and the assistance of
a Teflon guidewire (Wilson Cook Medical, Winston-Salem,
NC), the balloons were placed in the sigmoid colon and
rectum with the proximal tip at 40 cm from the anal verge.
Symptom Criteria and Perception in IBS 153
All medications known to affect the GI tract were discon-
tinued 48 h before the procedure. A 12-h fast and applica-
tion of two Fleet enemas (C.B. Fleet Inc., Lynchburg, VA)
preceded the endoscopy for balloon placement. All experi-
mental rectosigmoid colon stimulation studies were per-
formed 20 min after balloon placement. Patients were
placed in the left lateral decubitus position on a padded
table. Although the examiner was always present, interac-
tion with the examiner ceased after initial explanation of the
respective task. Subjects had no visual or auditory cues to
anticipate the location or time course of the distensions.
RECTAL SENSORY TRACKING. The electronic disten-
sion device was programmed to deliver intermittent phasic
stimuli (15-s duration/5-mm Hg increments) separated by an
interpulse interval (30-s duration/5 mm Hg) within a stim-
ulus tracking paradigm (600-s duration; 14 distension trials),
as previously reported (11). During each stimulus and rest
period, subjects were prompted by the distension device to
report the intensity of their sensations by triggering the
pushbutton marker device. If the subject indicated a sensa-
tion below the discomfort level (i.e., no sensation or mod-
erate sensation), the next stimulus increased by 5 mm Hg. If
the subject indicated discomfort, the next stimulus was
randomized to remain at the same or to decrease by 5 mm
Hg. If the subject reported the onset of pain, the next
stimulus decreased by 5 mm Hg. This paradigm was per-
formed before and after the sigmoid conditioning stimulus.
SIGMOID COLON CONDITIONING STIMULUS. Dis-
tension of the sigmoid colon consisted of 600 s of intermit-
tent rapid phasic distensions (30-s duration; 60 mm Hg) with
an interpulse rest (30-s duration; 5-mm Hg increment).
OUTCOME PARAMETERS. Perception thresholds for
rectal discomfort were expressed as intrarectal pressure be-
fore (PreTh) and after (PostTh) sigmoid stimulation, and
were quantified by averaging the last six stimulus pressures
after discomfort was reported. Patients were considered
hypersensitive if their discomfort threshold was below 30
mm Hg, as defined by the 95% confidence limit of the
healthy controls.
Statistical Analysis
The prevalence of the various viscerosensory symptoms was
expressed in percentages. Discomfort thresholds were ex-
pressed in mean values. The primary analysis of the rela-
tionship between each of the symptom variables and the
rectal perception thresholds consisted of a set of repeated-
measures analysis of variance (ANOVA). Each ANOVA
compared two groups (presence and absence of symptoms)
across two conditions (PreTh, PostTh). A significant main
effect of groups would indicate a difference in discomfort
thresholds depending on symptom presence. A significant
condition effect indicated a decrease in rectal thresholds
after sigmoid stimulation regardless of symptom presence or
154 Schmulson et al. AJG – Vol. 95, No. 1, 2000

Table 1. Prevalence of Rome Criteria Correlation of Rome Criteria

Prevalence, and Rectal Perception Thresholds
Symptom Criteria % (n) As shown in Table 2, only three Rome symptom criteria
Pain-discomfort relieved by a BM 45.2 (19) were associated with lower rectal discomfort thresholds in
Pain-discomfort associated with change 45.2 (19) IBS patients: the presence of pain associated with change in
in frequency of BM stool consistency; the presence of hard and/or lumpy stools;
Pain-discomfort associated with change 9.5 (4) and the absence of loose and/or watery stools (group effect,
in consistency of stools all: p ⬍ 0.05). No group effect was observed in relation to
⬍3 BM/wk 11.9 (5)
⬎3 BM/day 52.4 (22) any other Rome criteria. A sigmoid conditioning effect was
Hard/lumpy stools 42.9 (18) observed regardless of the presence or absence of any of the
Loose/watery stools 66.7 (28) criteria (all: p ⬍ 0.05). Baseline thresholds for patients with
Straining 59.5 (25) absence of hard and/or lumpy stools and those with loose
Urgency 64.3 (27) and/or watery stools were not different from controls (p ⬎
Incomplete evacuation 78.6 (33)
Mucus 42.9 (18) 0.05).
Bloating 80.9 (34)
BM ⫽ bowel movement.
Self-Reported Severity and Rectal Perception Thresholds
There was no difference in rectal discomfort thresholds
between patients with moderate (PreTh: 33.1 ⫾ 3.0 mm Hg,
absence, and a significant interaction indicated a differential PostTh: 31.6 ⫾ 3.3 mm Hg) and severe (PreTh: 29.2 ⫾ 2.3
effect of symptom presence on the two thresholds. mm Hg, PostTh: 28.3 ⫾ 2.8 mm Hg) symptom ratings.
Comparisons among groups were performed with the ␹2 There was a significant lowering of thresholds after sigmoid
test for categorical data and the t test for continuous data. stimulation in both the moderate and severe symptom
Statistical significance was assessed at the p ⬍ 0.05 level. groups (p ⬍ 0.01).

RESULTS
Clinical Characteristics
The IBS patient group comprised 22 women and 20 men,
and the healthy control group comprised 10 women and nine
men (NS). There was no difference in mean age between the
IBS patients and healthy controls (39.5 ⫾ 1.4 vs 38.7 ⫾ 3.2
yr, NS). Prevalence of IBS-Rome criteria is shown in Table
1. Self-reported symptom severity was rated as moderate by
38.1% (n ⫽ 16) and severe by 61.9% (n ⫽ 26) of the
patients. None of the patients rated their symptoms as mild.
Rectal Discomfort Thresholds
Rectal perception thresholds were significantly lower in IBS
patients than in healthy controls both before (PreTh: IBS ⫽
28.2 ⫾ 1.7 mm Hg vs controls ⫽ 36.3 ⫾ 2.8 mm Hg, p ⬍
0.05) and after sigmoid stimulation (PostTh: IBS ⫽ 25.3 ⫾
1.5 mm Hg, controls ⫽ 34.2 ⫾ 2.7 mm Hg, p ⬍ 0.01).
DISCUSSION
In the current study we have shown that IBS patients who
report pain associated with change in stool consistency,
patients with hard and/or lumpy stools, and patients without
loose and/or watery stools have lower rectal thresholds to
discomfort both before and after repetitive high-pressure
stimulation of the sigmoid colon. Noxious sigmoid stimu-
lation induced lowering of perception thresholds to rectal
distension regardless of the presence or absence of any
Rome symptom criteria or self-reported symptom severity.
The first finding suggests that rectal hypersensitivity is
associated with symptom criteria related to constipation
predominance, and the second finding suggests that a de-
crease in rectal perception thresholds after noxious sigmoid
stimulation is an inherent characteristic of IBS independent
of symptom pattern.

Table 2. Rome Symptom Criteria With a Significant Difference in Rectal Discomfort Thresholds
PreTh, PostTh,
Rome Criteria mm Hg (mean ⫾ SE) mm Hg (mean ⫾ SE) p Value
Pain-discomfort associated with change in
consistency of stools
Yes 2.64 ⫾ 2.1 25.0 ⫾ 1.9
No 40.0 ⫾ 2.5 31.9 ⫾ 3.5 ⬍0.05
Hard and/or lumpy stools
Yes 24.6 ⫾ 2.4 22.3 ⫾ 2.3
No 30.9 ⫾ 2.3 27.6 ⫾ 1.9 ⬍0.05
Loose and/or water stools
Yes 30.7 ⫾ 2.1 23.4 ⫾ 2.6
No 23.4 ⫾ 2.6 21.6 ⫾ 2.3 ⬍0.05
PreTh - before, and PostTh, after repetitive, high-pressure sigmoid distentions.
AJG – January, 2000
The diagnosis of IBS is based on symptom criteria (1) but
as of yet, no biological validation has been made of these
criteria, and their physiological significance is not known
(14). Lower pain thresholds to colonic distension has been
reported by Ritchie et al. (4) and many other studies have
reported hypersensitivity to balloon distensions in IBS pa-
tients (5–7). More recently, our group has reported lower
rectal discomfort thresholds after high-pressure, noxious
sigmoid stimulation in IBS patients (11) and this was con-
firmed in the current study, which included triple the num-
ber of patients. Although the mean change in discomfort
thresholds for the IBS group is somewhat smaller in the
present study than in our previous report (11), all IBS
subgroups showed decreased thresholds after sigmoid con-
ditioning. Sample variables such as gender prevalence, pre-
dominance of painful symptoms, and subject recruitment
procedure (advertisement vs clinic referral) may account for
differences in magnitude of change across studies as all of
these factors may affect visceral sensitivity. The finding of
inducible rectal hyperalgesia in IBS patients may be due to
inadequate activation of antinociceptive systems in response
to a noxious visceral stimulus (11). Such a hypothesis has
recently been supported by brain imaging studies using the
same repetitive sigmoid distension paradigm. Although
healthy control subjects showed activation of the periaque-
ductal gray (PAG) and thalamus in response to the noxious
sigmoid stimulus, IBS patients failed to show the activation
of these brain regions concerned with activation of antino-
ciceptive responses (12).
In the present study we have found lower rectal discom-
fort thresholds both before and after sigmoid stimulation in
patients who report hard and/or lumpy stools, compared
with those who do not, and in those who lack loose and/or
watery stools, compared with those who have them. Re-
cently we have reported lower rectal discomfort thresholds
after sigmoid stimulation in constipation-predominant com-
pared with diarrhea-predominant IBS patients (15). Al-
though this finding is in agreement with our current study,
the former study differs from the current one because it
excluded patients who have alternating bowel habits, to
study the differences in visceral perception between the IBS
patients with constipation and diarrhea. In the present study,
we included all patients regardless of their bowel habit
predominance, to assess the relationship of each Rome cri-
teria with rectal discomfort thresholds.
In addition to the differences in visceral perception, re-
cent reports have shown differences in viscerosensory
symptoms (15), brain activation (16), and autonomic (17,
18) and neuroendocrine (19, 20) control among IBS patients
with different bowel habit predominance. We have demon-
strated that compared with diarrhea-predominant IBS pa-
tients, constipation-predominant patients more commonly
report viscerosensory symptoms of the upper and lower GI
tract, musculoskeletal symptoms, and impaired vital func-
tions, such as quality of sleep, appetite, and sexual function
(15). Furthermore, a preliminary positron emission tomog-
Symptom Criteria and Perception in IBS 155
raphy study has shown that the left prefrontal cortex (LPC)
can be differentially activated depending on bowel habit
predominance (16). Patients with constipation-predominant
IBS activate the lateral area of the LPC, which is a sensory
association area, whereas diarrhea-predominant patients ac-
tivate a more medial area of the LPC, which is associated
with autonomic control (16).
Different autonomic responses in IBS constipation-pre-
dominant versus diarrhea-predominant patients have been
supported by Aggarwal et al. (17), who reported that con-
stipated patients manifested cholinergic abnormalities
whereas diarrhea patients had adrenergic abnormalities. Others
have confirmed abnormal cholinergic function in constipation-
predominant IBS patients (18), and enhanced sympathetic re-
sponses in diarrhea-predominant patients (21, 22).
Overall, IBS patients demonstrated rectal sensitization
after noxious sigmoid stimulation regardless of bowel habit
symptoms. IBS patients with constipation-related symptoms
show a greater degree of perceptual abnormalities than
patients with diarrhea-associated symptoms. One may spec-
ulate that different central alterations in visceromotor and
viscerosensory processing underlie these observed differ-
ences, and that these differences may have important im-
plications for response to therapies. Further analysis of the
relationship between autonomic and sensory findings may
enhance our ability to better diagnose and subclassify IBS
patients for targeted treatments.
There are no accepted criteria available to classify bowel
habit predominance in IBS and the physiological signifi-
cance of IBS Rome symptom criteria for bowel habit is still
unknown. It seems reasonable to believe from the current
findings that the presence of pain associated with change in
stool consistency, hard and/or lumpy stools, and the absence
of loose and/or watery stools—which point towards consti-
pation Rome symptom criteria—are related to visceral hy-
persensitivity and may be important discriminants in clas-
sifying bowel habit predominance in IBS.
Reprint requests and correspondence: Emeran A. Mayer, M.D.,
UCLA/CURE Neuroenteric Disease Program, WLA VA Medical
Center, Building 115, Room 223, 11301 Wilshire Boulevard, Los
Angeles, CA 90073.
Received Jan. 18, 1999; accepted July 7, 1999.
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