 |
|
Evidence- and Consensus-Based Practice Guidelines for the Diagnosis of Irritable Bowel Syndrome
Ronnie Fass, MD;
George F. Longstreth, MD;
Mark Pimentel, MD;
Steven Fullerton, MPH;
Simcha M. Russak, MA;
Chiun-Fang Chiou, PhD;
Eileen Reyes, BS;
Paul Crane, MD;
Glenn Eisen, MD;
Bill McCarberg, MD;
Joshua Ofman, MD, MSHS
Arch Intern Med. 2001;161:2081-2088.
ABSTRACT
| |
Background Irritable bowel syndrome (IBS) presents a significant diagnostic and
management challenge for primary care practitioners. Improving the accuracy
and timeliness of diagnosis may result in improved quality and efficiency
of care.
Objective To systematically appraise the existing diagnostic criteria and combine
the evidence with expert opinion to derive evidence- and consensus-based guidelines
for a diagnostic approach to patients with suspected IBS.
Methods We performed a systematic literature review (January 1966–April
2000) of computerized bibliographic databases. Articles meeting explicit inclusion
criteria for diagnostic studies in IBS were subjected to critical appraisal,
which formed the basis of guideline statements presented to an expert panel.
To develop a diagnostic algorithm, an expert panel of specialists and primary
care physicians was used to fill in gaps in the literature. Consensus was
developed using a modified Delphi technique.
Results The systematic literature review identified only 13 published studies
regarding the effectiveness of competing diagnostic approaches for IBS, the
accuracy of diagnostic tests, and the internal validity of current diagnostic
symptom criteria. Few studies met accepted methodological criteria. While
symptom criteria have been validated, the utility of endoscopic and other
diagnostic interventions remains unknown. An analysis of the literature, combined
with consensus from experienced clinicians, resulted in the development of
a diagnostic algorithm relevant to primary care that emphasizes a symptom-based
diagnostic approach, refers patients with alarm symptoms to subspecialists,
and reserves radiographic, endoscopic, and other tests for referral cases.
The resulting algorithm highlights the reliance on symptom criteria and comprises
a primary module, 3 submodules based on the predominant symptom pattern (constipation,
diarrhea, and pain) and severity level, and a subspecialist referral module.
Conclusions The dearth of available evidence highlights the need for more rigorous
scientific validation to identify the most accurate methods of diagnosing
IBS. Until such time, the diagnostic algorithm presented herein could inform
decision making for a range of providers caring for primary care patients
with abdominal discomfort or pain and altered bowel function suggestive of
IBS.
INTRODUCTION
IRRITABLE BOWEL syndrome (IBS) is a common disorder characterized by
abdominal pain, bloating, and disturbed defecation. Irritable bowel syndrome
remains the most common disorder encountered by gastroenterologists.1 The incidence of IBS is reported to be 15% to 20%
in the general population,2-3
with prevalence rates dependent upon the symptom criteria4
used to define the condition. Furthermore, functional bowel complaints such
as IBS are responsible for nearly 50% of visits to gastroenterologists.5
Presently there are no known biochemical or structural markers for identifying
patients with IBS. In most cases, a diagnosis of IBS is based on typical symptoms
and negative results of a limited diagnostic evaluation. Consequently, symptom
criteria for diagnosis have been proposed. Currently, the most widely accepted
criteria include the Rome I criteria,6 the
Manning criteria,7 and the recently developed
Rome II consensus criteria.8 These criteria
have been used in research protocols to facilitate study inclusion. However,
they have undergone limited validation, particularly in primary care settings.
In addition to symptom criteria, several diagnostic algorithms, such
as that proposed by Schmulson and Chang,9 have
been developed to facilitate the diagnosis and management of IBS. However,
most guidelines were developed for use in the specialty care setting and targeted
for patients with more severe symptoms. While many algorithms use structured
and validated expert panel methods, most panels consisted of academic center
subspecialists, who may not reflect the understanding and concerns of provider
organizations focused on the provision of care in the primary care setting.
The objective of the present study was to arrive at evidence- and consensus-based
guidelines for a diagnostic approach to patients with suspected IBS with specific
relevance to primary care providers. Our evidence-based approach to guideline
development relied upon a systematic review of the published medical literature
and consensus from an expert panel of experienced clinicians in a variety
of health care settings. A modified Delphi technique was used for instances
in which the published literature could not inform the decision-making process.
The purpose of this effort is to provide primary care and nonacademic clinicians
with guidance to improve the evaluation and diagnosis of patients with IBS.
METHODS
A 3-phase approach was used to construct the evidence-based guidelines
for diagnosing IBS. The phases include a systematic literature review of diagnostic
studies in IBS, a comprehensive appraisal of prior studies and estimates of
the accuracy of diagnostic tests, and convening an expert panel to synthesize
this information and develop consensus-based recommendations about the diagnosis
of IBS.
SYSTEMATIC REVIEW OF THE LITERATURE
We searched 4 computerized bibliographic databases (MEDLINE, HEALTHSTAR,
Evidence-Based Medicine, and the Cochrane Database) to identify English-language
articles published between January 1966 and April 2000. The focus of the search
was on articles that evaluated the performance of diagnostic tests and procedures
for IBS. Search terms and strategies were developed in cooperation with an
expert librarian experienced in advanced search strategies of health-related
computerized databases. In addition, the search included the bibliographies
of key reviews and of all articles that met the search criteria.
Articles were accepted for review if they used an objective gold standard
(ie, Manning, Kruis, or Rome I criteria or clinical assessment) and met one
of the following criteria: compared 2 diagnostic modalities, distinguished
IBS from another condition, appraised individual symptoms for their diagnostic
association, or provided sensitivity/specificity data on a diagnostic modality.
EVALUATION OF PUBLISHED STUDIES
The symptom criteria were assessed for their test characteristics and
performance (Table 1) based on
abstraction of the following information from each study: study design1 (ie, gold standard, diagnostic performance, and disease
prevalence) and diagnostic accuracy2 (ie, sensitivity,
specificity, and diagnostic odds ratio).
|
|
|
|
Table 1. Comparison of Diagnostic Criteria*
|
|
|
The quality of each study was assessed by summing the weights of the
study characteristics met. These weights were obtained from a multivariate
regression analysis reported in a recent publication by Lijmer and colleagues12 that evaluated design-related bias in assessments
of diagnostic tests. The potential range of each study's total score was from
0 to 8 unweighted and from 0 to 13.2 weighted. The study characteristics included
spectrum (clinical population vs case-control), verification (complete vs
different reference tests vs partial), interpretation of test results (blinded
vs not blinded), patient selection (consecutive vs nonconsecutive), data collection
(prospective vs retrospective vs unknown), details test (sufficient vs insufficient),
details reference test (sufficient vs insufficient), and details population
(sufficient vs insufficient). Studies were classified as low quality if they
scored in the lowest tertile. Conversely, studies were classified as being
of medium-high quality if their scores were in the middle or high tertile
(Table 2).
|
|
|
|
Table 2. Criteria for Grading the Quality of Diagnostic Studies
|
|
|
EXPERT PANEL
Because many areas were not addressed in the published literature, in
order to complete a diagnostic algorithm, an expert panel was assembled consisting
of physicians from 3 medical settings: an academic medical center, a Veterans
Affairs medical center, and a large group-model health maintenance organization.
Guideline statements were developed from the systematic review, existing guidelines
identified in the supplemental literature review, and expert opinion. The
panel was asked to vote on the relative appropriateness of each guideline
statement by considering both the expected costs and health benefits. Response
options were based on a scale from 1 to 9, ranging from extremely inappropriate1 to extremely appropriate.9
A score of 5 was considered equivocal. The RAND appropriateness methodology
for scoring responses13 was used as the basis
for determining consensus. Results were evaluated with respect to tertile1-9
after discarding the lowest and highest scores. Agreement was reached if the
remaining 4 scores fell within any 3-point range. Disagreement occurred if
at least 1 of the remaining 4 ratings fell within the lowest tertile and at
least 1 score fell within the highest tertile. Unclear opinion was defined
as all of the votes falling within adjoining tertiles. Experts were allowed
to modify their votes after independently reviewing the results of the group's
ratings.
DIAGNOSTIC ALGORITHM
Guidelines in the form of a diagnostic algorithm were developed incorporating
the best available evidence and expert opinion regarding the diagnosis of
IBS. Expert opinion was used when evidence in the literature did not exist
to inform the decision. Guideline statements were incorporated into the algorithm
when they met 1 of 2 criteria: if there was strong literature-based evidence
or if the expert panel voted that the guideline statement was appropriate
(ie, a median score >5). The algorithm details whether there was agreement
or disagreement among the expert panel. The methodology of the algorithm flowcharts
is consistent with the format previously adopted by the Agency for Health
Care Policy Research.14
RESULTS
SYSTEMATIC REVIEW
The initial search strategy identified 291 titles. One hundred twenty-eight
abstracts remained after explicit title rejection criteria were applied. Further
evaluation of these 128 abstracts resulted in 88 articles for final review.
Of the 88 articles identified, 28 (32%) met the criteria for inclusion in
the systematic review.
PERFORMANCE AND QUALITY EVALUATION OF DIAGNOSTIC CRITERIA
Manning Criteria
Of the 3 sets of diagnostic criteria identified in this review, the
Manning criteria appeared to be the most extensively studied. Manning and
colleagues7 originally identified only 4 symptoms
that were significantly more prevalent in IBS patients than in organic controls.
Two further symptoms approached statistical significance (mucus per rectum
and sensation of incomplete evacuation). Using the 4 significant symptoms,
subjects having less than 2 symptoms had a positive predictive value for IBS
of 12%. If 2 or more symptoms were present, the positive predictive value
was 74%. Finally, if 2 or more symptoms were present with all 6 symptoms included,
the positive predictive value was 63%. Groups have continued to determine
sensitivity and specificity data for 2 of 4 and 2 or 3 of 6 symptoms (Table 3).
|
|
|
|
Table 3. Summary of Studies Validating Standard Diagnostic Criteria*
|
|
|
When 2 of 4 symptoms were used, the Manning criteria yielded a sensitivity
and specificity of 91% and 70%, respectively.7, 16-17
In addition, when 2 or more of 6 criteria were used, sensitivity ranged from
84% to 94% and specificity ranged from 55% to 76%.7, 16-18,21
In articles in which 3 or more symptoms were assessed (irrespective of whether
it was out of 4 or 6), sensitivity ranged from 63% to 90% and specificity
ranged from 70% to 93%.16-20
The diagnostic ability of the Manning criteria also depended on the
control group used. All but 1 study compared the ability to distinguish IBS
from organic gastrointestinal (GI) disease.15
However, interpretation of the validation studies is problematic since many
of the control group patients experienced or had upper GI symptoms rather
than the organic lower GI disorders from which IBS more generally needs to
be distinguished. The Manning criteria fared better when used to distinguish
patients with IBS from healthy controls (sensitivity, 65%-66%; specificity,
86%-93%)15, 19 than when used to
distinguish IBS from organic GI disease (sensitivity, 58%-94%; specificity,
55%-93%).7, 15-17,19-20
Kruis Score
Kruis and colleagues10 used a point system
whereby functional symptoms received positive values and "red flag" symptoms
received negative values (Table 3).
Based on this point system, using a score of 44 or greater, to identify IBS
(or  3 symptoms from the list in Table
1), the sensitivity was reported as 64% and the specificity as 99%.10
Rome I Criteria
Rome I criteria were developed through expert consensus as the first
of an ongoing series of criteria for the standardization of diagnostic criteria
for IBS.5, 8 The 3 elements of
the Manning criteria that were elucidated in factor analysis constitute the
first part of the Rome I criteria. Despite this, the published validation
of these criteria is minimal. Table 3
summarizes data from 2 studies, only one of which provided an evaluation of
the sensitivity and specificity of the criteria.23
The Rome I criteria demonstrated a sensitivity of 65% and specificity of 100%.
The positive predictive value ranged between 69% and 100% in these 2 patient
groups. However, the study had a relatively small sample size and combined
the absence of red flag features with symptom criteria.
Comparisons of Criteria
Although the Rome I criteria have not been well tested in a controlled
fashion, studies have tried to compare results between the various criteria.
Two articles compared the agreement among various diagnostic criteria for
IBS. There was good agreement between the Manning and Rome I diagnosis of
IBS in 1 study ( = 0.72).24 Additionally,
in a large population-based study, 98% of subjects who tested positive for
the Rome I criteria also met the Manning criteria.25
However, of the subjects who tested positive for 2 or more of the Manning
criteria, only 37% were positive using the Rome I criteria. The lower prevalence
rate could be due to the inclusion of pain as a necessary precondition in
the Rome I criteria.
Quality of the Criteria
Each of the studies used to validate standard diagnostic criteria was
scored based on quality criteria. The raw scores ranged from 1 through 8,
and weighted scores ranged from 3 to 13.2. Of the 7 validation studies for
the Manning criteria, all but 1 were of medium to high quality. The 3 validation
studies on the Kruis criteria all received a medium to high quality score.
Only 1 of the 2 validation studies for the Rome I criteria obtained a medium
to high quality score. Two additional studies were identified that compared
diagnostic criteria.24-25 However,
these studies did not compare the criteria with a diagnostic gold standard.
DIAGNOSTIC ALGORITHM
The diagnostic algorithm was developed based on consensus of the guideline
statements that were derived from the systematic review, supplemental review,
and expert opinion. The algorithm consisted of a primary module, a primary
care workup module that comprised 3 predominant symptom patterns (constipation,
diarrhea, and pain), and a subspecialist referral module (Figure 1, Figure 2, and Figure 3).
|
|
|
|
Figure 1. Irritable bowel syndrome diagnostic
algorithm for a new primary care patient. Asterisk indicates that experts
agree that chronic abdominal pain plus 2 or more Manning criteria is an acceptable
alternative to the Rome I criteria. GI indicates gastrointestinal; CBC, complete
blood cell count; TSH, thyrotropin (thyroid-stimulating hormone) level; and
ESR, erythrocyte sedimentation rate.
|
|
|
|
|
|
|
Figure 2. Irritable bowel syndrome diagnostic
algorithm for constipation, diarrhea, and abdominal pain (module 1).
|
|
|
|
|
|
|
Figure 3. Irritable bowel syndrome diagnostic
algorithm for gastrointestinal subspecialty workup (module 2). CBC indicates
complete blood cell count; ESR, erythrocyte sedimentation rate; TSH, thyrotropin
(thyroid-stimulating hormone) level; FOBT, fecal occult blood test; and EMG,
electromyography.
|
|
|
While the evidence suggests that the Manning criteria have the greatest
number of validation studies, the expert panel reached consensus and selected
the Rome II criteria as the primary diagnostic symptom criteria. The Rome
II criteria incorporate the most valid elements of the Manning criteria while
broadening inclusion with the addition of abdominal discomfort or pain and
potentially greater discrimination between IBS and other functional disorders.
In addition, the subcategorization of IBS on the validated Rome I platform
facilitates management in a clinical algorithm. Given the validity of the
Manning criteria, the panel alternatively accepted chronic abdominal pain
plus 2 or more Manning criteria as an acceptable criterion for the algorithm.
Severity of illness was classified into 3 categories: mild (can be ignored
if the patient does not think about it), moderate (cannot be ignored but does
not affect patient's lifestyle), and severe/very severe (affects patient's
lifestyle).26 Predominant symptom patterns
were chosen by the expert panel based on the categorization of the Rome Working
Group.11
After patients are categorized, a thorough history should be taken to
identify previous interventions, therapies, and medications used. In some
cases, a psychosocial assessment is recommended. The expert panel achieved
consensus that an empirical trial of therapy based on the predominant symptom
complex does aid in the treatment of patients with suspected IBS. Failure
to respond to empirical trials may have diagnostic implications as in other
functional GI disorders, although evidence is forthcoming. Conservative empirical
trials may include the use of antidiarrheal agents for predominant diarrhea
symptoms or antispasmodics for predominant pain symptoms. Trials could also
include psychosocial counseling, stress reduction, or biofeedback based on
needs assessment. Further diagnostic consideration may be undertaken depending
upon responses to this trial. Upon referral to a subspecialist, traditional
invasive and noninvasive testing is recommended, if necessary, to establish
the diagnosis and to arrive at a therapeutic approach targeted at the predominant
symptom complex.
In the development of the algorithm, there were areas of agreement and
disagreement that impacted the specific diagnostic approach. For example,
all of the experts agreed that it is "inappropriate" to have all patients
who are " . . . referred to the gastroenterology subspecialty unit with suspected
IBS be given an anorectal manometry exam." Conversely, experts disagreed whether
it would be appropriate that all patients " . . . referred to the gastroenterology
subspecialty unit with suspected IBS be given a large bowel exam."
COMMENT
The objective of the present study was to use the best available evidence,
supplemented by expert opinion, to arrive at evidence- and consensus-based
guidelines for a diagnostic approach to patients with suspected IBS. Scant
data were identified in the published literature regarding the effectiveness
of competing diagnostic approaches, the accuracy of diagnostic tests, and
the internal validity of current diagnostic symptom criteria. As a result,
it was necessary to rely upon previously published validation studies, previously
developed practice guidelines, and the consensus opinion of our expert panel
when developing guidelines. To achieve the study's objective, a panel was
assembled that reflects the needs and concerns of primary care providers.
Preliminary efforts toward the development of diagnostic guidelines
entailed the systematic review of previous investigations. Of the studies
identified in the review, 8 assessed the Manning criteria,7, 15-21
3 evaluated the Kruis criteria,10, 20, 22
and 2 evaluated the Rome I criteria21, 23
(Table 3). The latest Rome II
criteria are based on needed improvements to the Rome I criteria and use the
most valid elements of the Manning criteria. However, it is evident that more
research is needed to better validate both the Rome I and Rome II criteria.
Still, the potential advantages of the Rome II criteria include simplicity
and improved sensitivity as a result of the inclusion of discomfort and pain
as symptoms. Furthermore, the Rome II criteria have potentially greater specificity
given that they do not include the second part of the Rome I criteria (non–pain-related
symptoms), which had poor clustering in factor analysis.
Over the past decade, research has begun to reveal differences in physiological
findings in IBS subjects with different predominant symptom patterns, including
dysmotility, gut hypersensitivity, and altered brain activation, among others.11 To subclassify by predominant symptom, diarrhea vs
constipation, new criteria were needed to better identify these subgroups.
Thus, the Rome II criteria may offer improved discriminative ability for diagnosing
patients with IBS.8 While abstracts assessing
the validity of the Rome II criteria have been presented,27-31
no full-length reports on the validity of the Rome II criteria had been published
at the time of this report.
The Manning and Rome criteria have gained much attention. However, the
Kruis score10 has not been as widely adopted,
possibly because of the inclusion of red flag symptoms as part of the scoring
algorithm. Red flag symptoms are quite common in subjects with IBS, and, based
on the present review, blood in the stool may be seen in up to 31% of IBS
subjects, with no objective cause identified on subsequent evaluation.15 Blood in the stool alone could represent hemorrhoidal
bleeding in IBS patients, yet, in the Kruis score, this would incur a penalty
of 98 points—enough to fail to meet the criteria for IBS. This may explain
the relatively low sensitivity and high specificity of the Kruis score. Frigerio
and colleagues22 adjusted the score to exclude
a diagnosis of organic digestive disease in patients with 44 or more points.
Still, their modification was unable to significantly improve the sensitivity
of the criteria.
Based on the present evaluation, studies that assessed standard diagnostic
criteria were generally of medium to high quality. However, only 1 study of
medium to high quality evaluating the Rome I criteria was identified in the
review. Although surveys and symptom criteria have been used as an aid to
identify IBS and to distinguish IBS from other functional disorders,26, 32-35
procedures have most often been relied upon to rule out organic disease. While
the expert panel reached agreement regarding the use of sigmoidoscopy and
colonoscopy in the guidelines, no validated evidence was found to support
the diagnostic value of these and other commonly used invasive and noninvasive
procedures (eg, blood tests or colonic transit studies). Moreover, recent
evidence suggests that testing for and treating small intestine bacterial
overgrowth in IBS may result in improved outcomes,36
but diagnostic utility in the primary care practice setting requires further
validation.
The diagnostic algorithm presented represents an accumulation of the
best available evidence- and consensus-based expert opinion from a variety
of practice settings. We recognize that there is a lack of expert consensus
in many areas—both among experts and between experts and the published
literature. Guideline statements were incorporated that were deemed appropriate
even if there was disagreement among experts. This enhances the flexibility
of the algorithm, allowing providers greater opportunity to employ their own
judgment. Accepted components of the algorithm include the differential treatment
of patients based on predominant symptom type (constipation vs diarrhea vs
abdominal pain) and the fact that younger patients without alarm symptoms
should be seen initially in the primary care setting. There is agreement that
symptom severity should play a role in the intensity of treatment. However,
it is well known that IBS patients often present with extraintestinal symptoms,
especially psychological comorbidity, that may dramatically influence the
classification of severity. While we advocate empirical trials in our algorithm
as an aid to management, the diagnostic validity of this approach remains
unclear. Furthermore, the utility of newly available medications targeting
the pathophysiological mechanisms of IBS remains unclear. Still, these medications
hold promise for more targeted empirical trials based on the pathophysiological
mechanism of the predominant symptom complex. The potential utility of targeted
empirical trials is that a treatment response may become a diagnostic indicator
in itself. Therefore, the predictive value of empirical therapy must be assessed
in prospective trials.
There are several limitations to the present study. First, the findings
of our systematic review were likely confounded by publication bias; that
is, small studies with positive findings are selectively published. Thus,
it is possible that studies with negative findings regarding the discriminative
capability of symptom criteria or poor test characteristics of standard diagnostic
tests may not have been discovered in our review. There were also many gaps
in the literature, which meant that expert opinion was required to develop
the algorithm. Additionally, several areas of disagreement remained even after
a modified Delphi method was used. The algorithm was based primarily on expert
consensus, yet, in some cases, consensus-based recommendations were not possible,
as clearly elucidated in the algorithm. As with all guidelines, providers
must use their best judgment in determining which patients are eligible for
the guidelines and in which cases the guidelines should be strictly adhered
to. Finally, because of the scope of the present study, there are no recommendations
in the algorithm regarding the possible impact that sex has on IBS symptom
reporting and on symptom-based diagnostic criteria. Indeed, differences between
the sexes in health-seeking behavior have been reported by Hochstrasser and
Angst,37 who found that women sought care for
GI problems significantly more often than did men.
Further research is necessary to define the most accurate methods of
patient identification and diagnosis. Studies should be performed using established
methodological standards for diagnostic test evaluation and should compare
the most commonly used criteria and diagnostic tests. Finally, a prospective
evaluation of the impact of systematic approaches to care for patients with
IBS should be performed to document the impact of guidelines on the cost-effectiveness
and outcomes of care. We hope that, until results from comparative prospective
studies are available, the algorithm will inform the decision-making process
for a wide range of providers caring for primary care patients with abdominal
discomfort or pain and altered bowel function suggestive of IBS.
AUTHOR INFORMATION
Accepted for publication March 29, 2001.
This study was sponsored by an educational grant from the Novartis Pharmaceuticals
Corp, East Hanover, NJ.
Corresponding author and reprints: Joshua Ofman, MD, MSHS, Zynx Health
Inc, 9100 Wilshire Blvd, East Tower, Suite 655, Beverly Hills, CA 90212 (e-mail: ofmanj{at}zynx.com).
From the Department of Medicine, Southern Arizona Veterans Affairs
Medical Center, Tucson (Dr Fass); Department of Medicine, Kaiser Permanente
Medical Care Program, San Diego, Calif (Drs Longstreth, Crane, and McCarberg);
Departments of Medicine (Drs Pimentel and Ofman) and Health Services Reseach
(Dr Ofman), Cedars-Sinai Health System, Los Angeles, Calif; Zynx Health Inc,
Los Angeles (Messrs Fullerton and Russak, Drs Chiou and Ofman, and Ms Reyes);
and Department of Medicine, Vanderbilt University Medical Center, Nashville,
Tenn (Dr Eisen).
REFERENCES
| |
1. Camilleri M, Choi MG. Review article: irritable bowel syndrome [review]. Aliment Pharmacol Ther. 1997;11:3-15.
WEB OF SCIENCE
| PUBMED
2. Drossman DA, Whitehead WE, Camilleri M. Irritable bowel syndrome: a technical review for practice guideline
development [review]. Gastroenterology. 1997;112:2120-2137.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
3. Thompson WG, Heaton KW. Functional bowel disorders in apparently healthy people. Gastroenterology. 1980;79:283-288.
WEB OF SCIENCE
| PUBMED
4. Saito YA, Locke GR, Talley NJ, Zinsmeister AR, Fett SL, Melton III LJ. A comparison of the Rome and Manning criteria for case identification
in epidemiological investigations of irritable bowel syndrome. Am J Gastroenterol. 2000;95:2816-2824.
FULL TEXT
| PUBMED
5. Thompson WG. The functional gastrointestinal bowel disorders. In: Drossman D, ed. The Functional Gastrointestinal
Disorders. McLean, Va: Degnon Associates; 1994:117-134.
6. Drossman DA, Richter JE, Talley NJ. The Functional Gastrointestinal Disorders, Pathophysiology,
and Treatment: A Multinational Consensus. Boston, Mass: Little Brown; 1994.
7. Manning AP, Thompson WG, Heaton KW, Morris AF. Towards positive diagnosis of the irritable bowel. BMJ. 1978;2:653-654.
8. Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Muller-Lissner SA. Functional bowel disorders and functional abdominal pain. Gut. 1999;45(suppl II):II43-II47.
9. Schmulson MW, Chang L. Diagnostic approach to the patient with irritable bowel syndrome [review]. Am J Med. 1999;107(5A):20S-26S.
10. Kruis W, Thieme C, Weinzierl M, Schussler P, Holl J, Paulus W. A diagnostic score for the irritable bowel syndrome: its value in the
exclusion of organic disease. Gastroenterology. 1984;87:1-7.
WEB OF SCIENCE
| PUBMED
11. Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Muller-Lissner SA. C. Functional bowel disorders and fuctional abdominal pain. In: Drossman AD, Talley NJ, Corazziari ETNJ, Thompson WG, Whitehead
WE, eds. Rome II: The Functional Gastrointestinal Disorders. McLean, Va: Degnon Associates; 2000:351-432.
12. Lijmer JG, Mol BW, Heisterkamp S, et al. Empirical evidence of design-related bias in studies of diagnostic
tests JAMA. 1999;282:1061-1066. [published erratum appears in JAMA. 2000;283:1963].
FREE FULL TEXT
13. Kahn KL, Roth CP, Kosecoff J, et al. Indications for Selected Medical and Surgical Procedures—A
Literature Review and Ratings of Appropriateness. Santa Monica, Calif: RAND Corp; 1986.
14. Using Clinical Practice Guidelines to Evaluate Quality of Care. Vol 1. Bethesda, Md: US Dept of Health and Human Services; 1995.
Publication AHCPR 95-0045.
15. Talley NJ, Phillips SF, Melton LJ, Mulvihill C, Wiltgen C, Zinsmeister AR. Diagnostic value of the Manning criteria in irritable bowel syndrome. Gut. 1990;31:77-81.
FREE FULL TEXT
16. Talley NJ, Zinsmeister AR, Van Dyke C, Melton III LJ. Epidemiology of colonic symptoms and the irritable bowel syndrome. Gastroenterology. 1991;101:927-934. [published erratum appears in Gastroenterology. 1992;102:746].
17. Talley NJ. Sensitivity and specificity of the Manning criteria [letter]. Gastroenterology. 1992;102:1828-1829.
PUBMED
18. Jeong H, Lee HR, Yoo BC, Park SM. Manning criteria in irritable bowel syndrome: its diagnostic significance. Korean J Intern Med. 1993;8:34-39.
PUBMED
19. Rao KP, Gupta S, Jain AK, Agrawal AK, Gupta JP. Evaluation of Manning's criteria in the diagnosis of irritable bowel
syndrome. J Assoc Physicians India. 1993;41:357-363.
PUBMED
20. Dogan UB, Unal S. Kruis scoring system and Manning's criteria in diagnosis of irritable
bowel syndrome: is it better to use combined? Acta Gastroenterol Belg. 1996;59:225-228.
PUBMED
21. Thompson WG. Gender differences in irritable bowel symptoms. Eur J Gastroenterol Hepatol. 1997;9:299-302.
PUBMED
22. Frigerio G, Beretta A, Orsenigo G, Tadeo G, Imperiali G, Minoli G. Irritable bowel syndrome: still far from a positive diagnosis. Dig Dis Sci. 1992;37:164-167.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
23. Vanner SJ, Depew WT, Paterson WG, et al. Predictive value of the Rome criteria for diagnosing the irritable
bowel syndrome. Am J Gastroenterol. 1999;94:2912-2917.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
24. Kay L, Jorgensen T, Lanng C. Irritable bowel syndrome: which definitions are consistent? J Intern Med. 1998;244:489-494.
PUBMED
25. Hahn BA, Saunders WB, Maier WC. Differences between individuals with self-reported irritable bowel
syndrome (IBS) and IBS-like symptoms. Dig Dis Sci. 1997;42:2585-2590.
PUBMED
26. Talley NJ, Phillips SF, Wiltgen CM, Zinsmeister AR, Melton III LJ. Assessment of functional gastrointestinal disease: the bowel disease
questionnaire. Mayo Clin Proc. 1990;65:1456-1479.
WEB OF SCIENCE
| PUBMED
27. Levy RL, Whitehead WE, Feld AD, et al. Agreement between clinician recorded diagnoses and Rome I and Rome
II diagnostic criteria for irritable bowel syndrome [abstract]. Gastroenterology. 2000;118:A2068.
28. Yuri A, Locke G, Prather C, et al. Evaluation of the Rome II criteria for irritable bowel syndrome in
a tertiary care outpatient population [abstract]. Gastroenterology. 2000;118:A2071.
29. Thompson GW, Irvine JE, Pare P. Comparing Rome I and Rome II criteria for irritable bowel syndrome
(IBS) in a prospective survey of the Canadian population [abstract]. Am J Gastroenterol. 2000;96:A2553.
30. Saito YA, Locke GR, Talley NJ, Zinsmeister AR, Fett SL, Melton J. The effect of new diagnostic criteria for irritable bowel syndrome
on community prevalence estimates [abstract]. Gastroenterology. 2000;118:A396.
31. Sperber A, Safieh Y, Jaffer A, et al. A comparison of the prevalence of IBS using Rome I and Rome II criteria
in an epidemiology study [abstract]. Gastroenterology. 2000;118:A397.
32. Kapoor KK, Nigam P, Rastogi CK, Kumar A, Gupta AK. Clinical profile of irritable bowel syndrome. Indian J Gastroenterol. 1985;4:15-16.
PUBMED
33. Talley NJ, Phillips SF, Bruce B, Twomey CK, Zinsmeister AR, Melton III LJ. Relation among personality and symptoms in nonulcer dyspepsia and the
irritable bowel syndrome. Gastroenterology. 1990;99:327-333.
WEB OF SCIENCE
| PUBMED
34. O'Keefe EA, Talley NJ, Tangalos EG, Zinsmeister AR. A bowel symptom questionnaire for the elderly. J Gerontol. 1992;47:M116-M121.
35. Agreus L, Talley NJ, Svardsudd K, Tibblin G, Jones MP. Identifying dyspepsia and irritable bowel syndrome: the value of pain
or discomfort, and bowel habit descriptors. Scand J Gastroenterol. 2000;35:142-151.
FULL TEXT
| PUBMED
36. Pimentel M, Chow EJ, Lin HC. Eradication of small intestinal bacterial overgrowth reduces symptoms
of irritable bowel syndrome. Am J Gastroenterol. 2000;95:3503-3506.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
37. Hochstrasser B, Angst J. The Zurich Study: XXII, epidemiology of gastrointestinal complaints
and comorbidity with anxiety and depression. Eur Arch Psychiatry Clin Neurosci. 1996;246:261-272.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
 CiteULike  Connotea  Del.icio.us  Digg  Reddit  Technorati  Twitter
What's this?
RELATED LETTER
Irritable Bowel Syndrome: New Recommendations for Diagnosis and Treatment
Brian E. Lacy
Arch Intern Med. 2003;163(11):1374-1375.
EXTRACT
| FULL TEXT
RELATED ARTICLE
Archives of Internal Medicine Reader's Choice: Continuing Medical Education
Arch Intern Med. 2001;161(17):2155-2156.
FULL TEXT
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
GPs' explanatory models for irritable bowel syndrome: a mismatch with patient models?
Casiday et al.
Fam Pract 2009;26:34-39.
ABSTRACT
| FULL TEXT
The Central Role of Gastrointestinal-Specific Anxiety in Irritable Bowel Syndrome: Further Validation of the Visceral Sensitivity Index
Labus et al.
Psychosom. Med. 2007;69:89-98.
ABSTRACT
| FULL TEXT
Diagnostic yield of alarm features in irritable bowel syndrome and functional dyspepsia
Hammer et al.
Gut 2004;53:666-672.
ABSTRACT
| FULL TEXT
Irritable Bowel Syndrome: New Recommendations for Diagnosis and Treatment
Lacy
Arch Intern Med 2003;163:1374-1375.
FULL TEXT
|
