 |
|
Cost-effectiveness of Endoscopy in Irritable Bowel Syndrome
Saud Suleiman, MD;
Amnon Sonnenberg, MD, MSc
Arch Intern Med. 2001;161:369-375.
ABSTRACT
| |
Background It is unknown to what extent at what expense flexible sigmoidoscopy
and colonoscopy add to the diagnosis of irritable bowel syndrome (IBS). The
aim of the study was to assess the incremental cost-effectiveness of endoscopic
procedures in the workup for IBS.
Methods Using the Bayes formula, we calculated the increase in diagnostic certainty
for a consecutive number of tests. We also calculated the incremental cost-effectiveness
ratio, which corresponds to the test costs divided by the increment in diagnostic
certainty.
Results The diagnosis of IBS can be established with a relatively high probability
of more than 80% relying on relatively inexpensive and noninvasive tests only.
Flexible sigmoidoscopy or colonoscopy constitute the most costly portion of
any workup for IBS, which amounts to 50% to 75% of the overall costs. Because
of their high incremental cost-effectiveness ratio, endoscopic procedures
should not be used at the beginning of the diagnostic workup. This outcome
of the analysis remains largely unaffected within reasonable ranges of the
sensitivity and specificity of various tests.
Conclusions In the diagnosis of IBS, inexpensive, noninvasive tests should be used
first to rule out other diagnoses. Despite their high incremental cost-effectiveness
ratio, flexible sigmoidoscopy and colonoscopy are indicated when a serious
organic disease is reasonably likely and needs to be ruled out.
INTRODUCTION
IRRITABLE BOWEL syndrome (IBS) affects 15% to 20% of the US population,1 of whom only 30% seek medical attention for this condition.2-4 Its diagnosis is based
primarily on the occurrence of typical symptoms.5
In the absence of any specific biochemical markers, symptoms constitute the
only positive test modality for diagnosis of IBS. Studies6-9
have shown the sensitivity associated with typical symptoms to vary between
42% and 94% and the specificity to vary between 55% and 94%. To improve the
diagnostic probability, physicians must resort to ruling out other potential
organic diseases, such as inflammatory bowel disease, microscopic colitis,
gastrointestinal infections, lactose intolerance, intestinal malabsorption,
endocrine disorders, and colorectal cancer.10-11
This requires multiple laboratory tests, stool studies, radiologic small bowel
follow-through, and flexible sigmoidoscopy or colonoscopy.11-13
The expenditures rise as a result of the multitude of tests necessary to rule
out other medical conditions and to increase the certainty associated with
the specific diagnosis of IBS. It was estimated that the excess medical cost
for diagnosing IBS in the United States in 1992 was $8 billion.14
The present study focuses on the cost-effectiveness of endoscopic procedures
in the workup of IBS. How much do flexible sigmoidoscopy and colonoscopy add
to establishing a diagnosis of IBS and at what expense? The aim of our study
was to assess the incremental cost-effectiveness of endoscopic procedures
in the workup for IBS.
METHODS
GENERAL DECISION MODEL
The diagnosis of IBS is assumed to be based on a sequence of 6 consecutive
tests: (1) history and physical examination, (2) general laboratory panel,
(3) hydrogen breath test, (4) radiologic small bowel follow-through, (5) flexible
sigmoidoscopy, and (6) colonoscopy. The order of tests can be permutated in
many different ways, and the diagnostic workup can be stopped after any given
number of tests. The increase in diagnostic certainty for a consecutive number
of tests is calculated using the Bayes formula.15
The incremental cost-effectiveness ratio (ICER) corresponds to the increment
in test costs divided by the increment in diagnostic certainty. For the purpose
of the present analysis, the ICER is defined as costs per 1% increase in the
probability of having IBS. We also calculate the average cost-effectiveness
ratio (ACER) of establishing 1 diagnosis of IBS, ie, the total costs of all
diagnostic tests in the entire patient population divided by the number of
correct diagnoses.
TEST COSTS
Table 1 lists the physician
and facility costs associated with the 6 diagnostic procedures. The procedures
are assigned code numbers from the Physicians' Current Procedural
Terminology (CPT), using the code numbers to assign costs to each test.
The costs represent the average payments allowed for each coded procedure
by the Health Care Financing Administration during fiscal year 2000. Except
for laboratory tests, the dollar amount reflects physician plus facility cost.
In the case of colonoscopy, CPT codes reflect the endoscopy plus one set of
biopsy specimens taken during the procedure. The costs for the biopsy include
the professional fees of a surgical pathologist. No polypectomy or costs of
potential complications resulting from endoscopy are considered. Biopsy costs
were not added to the cost of flexible sigmoidoscopy because rectal biopsies
were found to be unnecessary in the investigation of IBS by MacIntosh and
coworkers,16 and in general they are less likely
to be done routinely.
|
|
|
|
Test Characteristics and Costs*
|
|
|
TEST CHARACTERISTICS
The sensitivity and specificity for each of the tests were obtained
from the literature. The characteristics of taking a history are estimated
based on the sensitivity and specificity reported for the Manning and Rome
criteria.6, 12, 17
The combined sensitivity of multiple blood and stool tests is calculated as
the weighted average of each individual test for a positive gastrointestinal
diagnosis, using various disease prevalence rates as weights (see formula
1). In general, the normal range of each laboratory test is set to include
95% of all true-negative results, ie, a 95% specificity. Bessette and coworkers18 report a sensitivity of 61% for the small bowel follow-through
in detecting small bowel tumors; they also cite other studies that report
sensitivity ranging from 53% to 83%. Others have reported overall sensitivities
of more than 90% for the small bowel follow-through.19
The median value of 70% is taken to estimate the general sensitivity associated
with any small bowel disease. For the hydrogen breath test, we use the median
sensitivity and specificity values reported to test for bacterial overgrowth
and lactase deficiency.20-21 The
sensitivity (sens) and specificity of colonoscopy and flexible sigmoidoscopy
are calculated as the weighted average of these tests for inflammatory colitis,
diverticular disease, and colon cancer,22-25
again using disease prevalence (prev) as weight:
The literature values for sensitivity and specificity show a large
spread, which can be partly explained by the trade-offs between sensitivity
and specificity. As indicated by the receiver operating characteristic of
each test, a sensitivity value can be increased at the expense of lowering
the corresponding specificity value.26
INCREMENTS IN DIAGNOSTIC CERTAINTY
Since IBS affects 15% of the adult population, of whom one third seek
medical attention, the point prevalence of this condition in a general patient
population is estimated as 5%.2-4
This is used as a starting value for the pretest probability (P0) of IBS in
a given patient. The prevalence of IBS in combination with the sensitivity
(sens) and specificity (spec) values taken from Table 1 are then keyed into the Bayes formula to calculate the positive
predictive value (P1) associated with a positive first test result, ie, a
positive history of symptoms:
The positive predictive value (P1) serves as an updated pretest probability
value for the second round of tests, for instance, the laboratory test panel.
The increase in disease probability after each test is calculated by repetitive
use of the Bayes formula. Except for the history and physical examination,
the sensitivity and specificity values of all subsequent tests relate to a
positive diagnosis other than IBS, whereas IBS itself is included in the group
of negative diagnoses. In other words, all subsequent tests are designed to
rule out diagnoses in the differential other than IBS. Therefore, the Bayes
formula for a negative predictivevalue is used to calculate the upgrade in
diagnostic probability (P2) after the second test, for instance,
P2 is subsequently entered as pretest probability into a third Bayes
formula to calculate the negative predictive value of IBS (P3) associated
with a third round of diagnostic testing. This procedure is repeated according
to the number of tests used in trying to establish the diagnosis. The values
P1 - P0, P2 - P1, P3 - P2, and so on correspond to the increments
in diagnostic certainty with respect to IBS.
The number of patients with a positive test result (N1) is determined
by the fraction of true-positive test results (sens) in patients with IBS
(P0) and the fraction of false-positive test results (1 - spec) in subjects
without IBS (1 - P0):
Equation 4 corresponds to the denominator of the Bayes formula of equation
2 multiplied by the initial patient population (N0). Applying equation 4 to
an initial population of N0 = 1000 patients yields a positive history of symptoms
in the following:
Similarly, the number of patients with possible IBS after a negative
laboratory panel corresponds to the denominator of equation 3 multiplied by
the remaining patient population after applying the first test (N1):
SENSITIVITY ANALYSIS
The primary focus of the present analysis relates to the incremental
cost-effectiveness of flexible sigmoidoscopy and colonoscopy. Besides the
sensitivity and specificity of both procedures, this value depends largely
on the pretest probability achieved through other means before embarking on
endoscopic procedures. In a sensitivity analysis, the pretest probability
varied between 80% and 98%.
RESULTS
Figure 1 shows a decision
tree of various possible test sequences. Each box symbolizes a different test
of the sequence. The dollar amount inside the box represents the cumulative
costs spent on tests. The number in the right upper corner represents the
remaining population (of the initial 1000 patients) with a test sequence that
is still suggestive of IBS and to whom the next test will be applied. The
rest of the initial population has dropped out because one of the tests has
suggested another diagnosis than IBS. The percentage value inside the box
represents the cumulative probability for IBS. The cumulative probability
is calculated by repetitive application of the Bayes formula. After a history
plus physical examination, a laboratory test panel, and a hydrogen breath
test, the patient could undergo a flexible sigmoidoscopy, followed by a small
bowel follow-through and a colonoscopy. The order of the last 2 tests could
be reversed. In yet another sequence of tests, the hydrogen breath test may
be followed by a small bowel follow-through, flexible sigmoidoscopy, and colonoscopy. Figure 1 contains only a small sample of
the overall number of possibilities. Theoretically, a sequence of 6 tests
can be permutated in 6! = 720 different ways. In most instances, however,
the workup will start with a physical examination and a laboratory panel,
thus reducing the number of permutations to 4! = 24. Since a physician may
decide to discontinue the diagnostic pursuit after 5, 4, or fewer tests, the
actual number of possible test sequences is somewhat higher than 24. As shown
by the 3 complete sequences at the top of Figure 1, a permutation of identical tests yields the same cumulative
cost and probability values, irrespective of actual test order.
|
|
|
|
Figure 1. Decision tree of diagnostic workup
for irritable bowel syndrome (IBS). In each box, the dollar amount represents
the cumulative costs spent on tests, the percentage value represents the probability
for IBS, and the number in the right upper corner represents the remaining
patients after the test with possible IBS. H&P indicates history and physical
examination; lab, laboratory tests as indicated in Table 1; H2BT, hydrogen breath test; SBFT, small bowel
follow-through; FS, flexible sigmoidoscopy; and colon, colonoscopy.
|
|
|
In Figure 2,
the cumulative costs are plotted against the cumulative probability of diagnosing
IBS. The numbers next to each test represent the remaining population undergoing
each particular test. Four possible sequences are shown. History plus physical
examination, laboratory test panel, hydrogen breath test, and small bowel
follow-through yield a diagnostic probability of 83% at the expense of $398.
Panel A depicts a flat curve that starts to rise steeply only after the inclusion
of flexible sigmoidoscopy and colonoscopy into the diagnostic workup. Flexible
sigmoidoscopy increases the overall probability by 6% at the expense of almost
doubling the cumulative costs. The inclusion of colonoscopy raises the probability
by an additional 7% at the expense of yet again doubling the cumulative costs.
Leaving out flexible sigmoidoscopy, as suggested by panel B, and going directly
from small bowel follow-through to colonoscopy provides only moderate relief
with respect to the overall expenses.
|
|
|
|
Figure 2. The cumulative cost and probability
of irritable bowel syndrome (IBS) associated with various diagnostic paths.
The numbers represents the number of patients subjected to each consecutive
test. H&P indicates history and physical examination; lab, laboratory
tests as indicated in Table 1;
H2BT, hydrogen breath test; SBFT, small bowel follow-through; FS,
flexible sigmoidoscopy; and colon, colonoscopy.
|
|
|
The 2 sequences outlined in the 2 bottom panels (C and D) indicate that
performing endoscopy early during the workup does not represent a valid option,
because it adds large costs to the early workup without pushing the diagnostic
probability beyond 70%. Inexpensive tests at the onset of the diagnostic workup
function as a sieve to exclude patients without IBS and increase its a priori
probability before using the more expensive tests. The test sequences of panels
A and C, as well as panels B and D, contain identical tests, resulting in
the same medical outcome. In the 2 lower panels (C and D), flexible sigmoidoscopy
and colonoscopy, respectively, are used as early as the third diagnostic test.
Shifting endoscopy toward the beginning of the diagnostic workup leads to
a larger number of patients undergoing endoscopy. In the sequence of panel
A, for instance, only 31 subjects undergo flexible sigmoidoscopy compared
with 75 patients in panel C. Similarly, only 31 subjects undergo colonoscopy
in the sequence of panel B compared with 75 in panel D. The total cost of
testing in the entire patient population corresponds to the sum of patients
associated with each test in Figure 2
multiplied by the respective test costs. The ACER corresponds to the total
cost divided by the number of correct diagnoses of IBS. Although sequences
A and C lead to identical medical outcomes, their ACERs are $18 382 and
$24 686 per diagnosis, respectively. Similarly, the identical outcomes
of the 2 sequences B and D are associated with ACERs of $12 724 and $14 355
per diagnosis, respectively.
The sequences depicted in Figure 1
and Figure 2 are restricted to the
analyses of true test results. The cumulative costs of diagnosing IBS may
become further inflated by the contribution of false tests. For instance,
the atypical description of bowel symptoms may convince the physician to pursue
diagnoses other than IBS and invest in many unnecessary tests. Similarly,
a false-positive sign of ileal obstruction or inflammation may mislead the
physician to rule out a diagnosis of inflammatory bowel disease, intestinal
lymphoma, or tumor before returning to the workup for IBS. No systematic analysis
can predict the variety and types of erroneous and occasionally convoluted
workups that may ensue from false test results. A false-positive diagnosis
of IBS would not contribute to the cost of IBS itself but add to the costs
of other differential diagnoses.
Under baseline conditions, history and physical examination, laboratory
tests, hydrogen breath test, and small bowel follow-through reach a probability
value of 83%, with a total of $398 spent on diagnostic workup. The ICER of
all 4 tests, compared with the baseline prevalence rate of 5%, is $398/(83% -
5%) = $510 per 1% increase in diagnostic probability. The ICER of flexible
sigmoidoscopy is $5846 for this step alone. Colonoscopy alone is associated
with an ICER of $8246, whereas the combination of both endoscopic procedures
is associated with an ICER of $9338. A higher pretest probability leads to
lower increments in diagnostic certainty achieved through endoscopy and, hence,
a higher ICER. Figure 3 shows the
relation between pretest probability and the ICER of endoscopic procedures.
When varying the pretest probability, one notices a change in the incline
for each of the series at 94%, when the ICER becomes steeper. This indicates
that the expenditures become much greater for smaller gains in probability
beyond this probability.
|
|
|
|
Figure 3. Incremental cost-effectiveness
ratio (ICER) of endoscopic procedures plotted against the pretest probability
achieved by nonendoscopic means. The ICER is given in US dollars per 1% increase
in the diagnostic probability of irritable bowel syndrome (IBS).
|
|
|
COMMENT
The objective of performing medical tests is to increase the diagnostic
probability associated with a given diagnosis. Most diagnoses can be ascertained
by a sequence of one or few positive test results. Irritable bowel syndrome
constitutes a diagnostic conundrum, because its workup is mainly composed
of negative test results. Except for a set of specific symptoms that may be
ascertained through careful history taking, IBS can only be approached in
an indirect fashion by ruling out other differential diagnoses. The large
variety of diagnoses associated with abdominal pain harbors the potential
risk of turning the workup for IBS into a rather expensive medical exercise.
Our analysis suggests that the diagnosis of IBS can be established with a
relatively high probability by relying on relatively inexpensive and noninvasive
tests only. Endoscopic procedures should not be used at the beginning of the
diagnostic workup, and they should be reserved for patients in whom high diagnostic
certainty is deemed necessary. Flexible sigmoidoscopy or colonoscopy constitute
the most costly portion of any workup for IBS, which amounts to 50% to 75%
of the overall costs. This outcome of the analysis remains largely unaffected
by the sensitivity and specificity of various tests. In general, a better
diagnosis of IBS by means other than endoscopy increases the ICER of subsequent
endoscopy.
The present analysis uses the Bayes formula to calculate the increment
in diagnostic certainty achieved through a sequence of consecutive tests.
In strictly mathematical terms, the repeated application of Bayes formula
requires that the tests are statistically independent. In reality, such conditions
are rarely met. For instance, inflammatory bowel disease may lead to intestinal
obstruction, visible on the small bowel follow-through, and crampy abdominal
pain. Obviously, some of the pain may stem from the intestinal obstruction,
and the 2 signs are not independent of each other. Similarly, rectal cancer
could result in 4 related signs—constipation, anemia plus positive fecal
occult blood test result, and a positive finding during sigmoidoscopy. The
erroneous assumption of test independence tends to overestimate the cumulative
probability of multiple tests and the diagnostic increment associated with
individual tests. These types of errors concern mostly the diagnostic contribution
exerted by the 2 endoscopic procedures. Obviously, flexible sigmoidoscopy
and colonoscopy constitute similar tests, and the actual contribution of a
colonoscopy after a flexible sigmoidoscopy may be much smaller than calculated
here based on its sensitivity and specificity alone.
In modeling the path toward a diagnosis of IBS, we considered only true-positive
and true-negative test results that helped to improve the probability of this
particular diagnosis. False tests would prolong the diagnostic chain and inflate
the costs of the diagnosis. More tests would also add to the overall risk
of adverse effects and complications associated with any lengthy medical workup
involving multiple procedures. Since errors occur randomly and their financial
consequences are difficult to predict, we decided to restrict the cost analysis
to Medicare reimbursement for various medical costs. In ignoring these additional
costs, our analysis of diagnosing IBS underestimates the true cost of consecutive
testing. The analysis focuses on the implications of advancing the workup
toward a correct diagnosis of IBS, but it cannot measure the cost-effectiveness
of excluding other diagnoses, such as colorectal cancer, diverticulitis, or
inflammatory bowel disease. Foremost, there would be no reason to restrict
the benefit of exclusion to gastrointestinal disease, and the diagnostician
could well claim the benefit of having excluded in essence an entire textbook
of medicine in each individual patient. One would need to know the myriad
costs associated with the entirety of other diagnoses and quantify all gains
in terms of quality-adjusted life-years achieved through each individual test.
Besides the difficulties in accumulating such information, the results would
be compromised by the arbitrariness of what diagnoses or parameters to consider.
The analysis of IBS would become overwhelmed by other issues, and its outcome
would be extremely sensitive to minor changes in the underlying assumptions.
The general benefit of endoscopy in the workup of gastrointestinal disease
or the cost-effectiveness of colonoscopy in colorectal cancer reside outside
the realm of the present analysis.
The model shows that 4 relatively simple, noninvasive tests can achieve
a diagnostic probability of more than 80%. Such a value may provide sufficient
diagnostic certainty in a young patient with a history of similar symptoms
during a prolonged period. Patients with IBS fall into the age range of 30
to 55 years.6-7,14, 27-28
The prevalence and incidence of IBS decline with increasing age, and during
a 5-year follow-up patients tend to recover from their symptoms of IBS.29 Most patients have their symptoms for more than 2
years.7 This pattern is in striking contrast
to colorectal cancer, where most cases occur after the age of 50 years. These
patients also present with a shorter history that tends to worsen over time.
Besides colorectal cancer, the need to rule out inflammatory bowel disease
or microscopic colitis represents another reason to schedule an endoscopic
procedure in patients with abdominal symptoms. Hamm and coworkers30 analyzed the results of endoscopy in 306 patients
who met the Rome criteria for IBS. Only 7 patients presented with colonic
abnormalities, of whom 3 had inflammatory bowel disease, 1 had intestinal
obstruction, and 3 had colonic polyps. Vanner and coworkers31
reported that in the absence of alarm signs, such as weight loss, nocturnal
symptoms, blood mixed with stool, recent antibiotic use, family history of
colon cancer, or relevant abnormalities on physical examination, the Rome
criteria had a sensitivity of 65% and a specificity of 100%.
These citations from the last 2 paragraphs should not be misinterpreted,
however, to indicate that flexible sigmoidoscopy or colonoscopy can be generally
dispensed within the workup for irritable bowel. Similarly, the high ICER
of endoscopy must not be mistaken as an argument against its use in the diagnosis
of IBS. Toward the end of all diagnostic workups, increasing amounts of money
are spent on confirming a suspected diagnosis and raising its probability
by a few points only. This law of diminishing return permeates a large variety
of medical and nonmedical endeavors. In a previous decision analysis, it was
shown that a diagnostic test remains indicated as long as the pretest probability
(P) of a given disease exceeds the ratio of test cost (T) to disease cost
(C), that is, P > T/C.32 In the case of colorectal
cancer or inflammatory bowel disease, for instance, the overall costs of the
disease outweigh the costs of a single endoscopy by a factor of 50 or more,
for which the ratio is 2% or less. In other words, a gap in the diagnostic
probability between 80% and 100% may be large in some patients and represent
an intolerable risk. An endoscopic procedure that would help in bridging this
gap and eliminating the risk of serious organic disease may well justify its
high ICER.
In conclusion, endoscopic procedures represent the most costly portion
in the workup for IBS, contributing to 50% to 75% of the total cost. They
should be scheduled at the end of a diagnostic chain, using less expensive
tests first to rule out other differential diagnoses. Despite their high ICER,
however, the utilization of endoscopic procedures is indicated in all patients
in whom, besides diagnosing IBS, ruling out a serious organic disease is necessary.
AUTHOR INFORMATION
Accepted for publication August 22, 2000.
Corresponding author and reprints: Amnon Sonnenberg, MD, MSc, Department
of Veterans Affairs Medical Center 111F, 1501 San Pedro Dr SE, Albuquerque,
NM 87108 (e-mail: sonnbrg{at}unm.edu).
From the Department of Veterans Affairs Medical Center and University
of New Mexico, Albuquerque, NM.
REFERENCES
| |
1. Drossman DA, Thompson WG. The irritable bowel syndrome: review and a graduated multicomponent
treatment approach. Ann Intern Med. 1992;116:1009-1016.
2. Jones R, Lydeard S. Irritable bowel syndrome in the general population. BMJ. 1992;304:87-90.
3. Thompson WG, Heaton KW. Functional bowel disorders in apparently healthy people. Gastroenterology. 1980;79:283-288.
ISI
| PUBMED
4. Bommelaer G, Rouch M, Dapoigny M, et al. Epidemiology of functional bowel disorders in apparently healthy people. Gastroenterol Clin Biol. 1986;10:7-12.
ISI
| PUBMED
5. Hammer J, Talley NJ. Diagnostic criteria for the irritable bowel syndrome. Am J Med. 1999;107(suppl 5A):5S-11S.
6. 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
7. Talley NJ, Zinsmeister AR, Van Dyke C, Melton LJ. Epidemiology of colonic symptoms and the irritable bowel syndrome. Gastroenterology. 1991;101:927-934.
ISI
| PUBMED
8. 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
9. 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
|
ISI
| PUBMED
10. Schmulson MW, Chang L. Diagnostic approach to the patient with irritable bowel syndrome. Am J Med. 1999;107(suppl 5A):20S-26S.
11. Lynn RB, Friedman LS. Irritable bowel syndrome. N Engl J Med. 1993;329:1940-1945.
FREE FULL TEXT
12. Coremans G, Dapoigny M, Müller-Lissner S, et al. Diagnostic procedures in irritable bowel syndrome. Digestion. 1995;56:76-84.
ISI
| PUBMED
13. Tolliver BA, Herrera JL, DiPalma JA. Evaluation of patients who meet clinical criteria for irritable bowel
syndrome. Am J Gastroenterol. 1994;89:176-178.
ISI
| PUBMED
14. Talley NJ, Gabriel SE, Harmsen WS, Zinsmeister AR, Evans RW. Medical costs in community subjects with irritable bowel syndrome. Gastroenterology. 1995;109:1736-1741.
FULL TEXT
|
ISI
| PUBMED
15. Ingelfinger JA, Mosteller F, Thibodeau LA, Ware JH. Biostatistics in Clinical Medicine. New York, NY: McMillan Publishing Co; 1983:1-24.
16. MacIntosh DG, Thompson G, Patel DG, Barr R, Guindi M. Is rectal biopsy necessary in irritable bowel syndrome? Am J Gastroenterol. 1992;87:1407-1409.
ISI
| PUBMED
17. 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
18. Bessette JR, Maglinte DDT, Kelvin FM, Chernish SM. Primary malignant tumors in the small bowel: a comparison of the small-bowel
enema and conventional follow-through examination. AJR Am J Roentgenol. 1989;153:741-744.
FREE FULL TEXT
19. Ott DJ, Chen YM, Gelfand DW, Van Swearingen F, Munitz HA. Detailed per-oral small bowel examination vs. entereoclysis, part II:
radiographic accuracy. Radiology. 1985;155:31-34.
ABSTRACT
20. Corazza GR, Menozzi MG, Strocchi A, et al. The diagnosis of small bowel bacterial overgrowth reliability of jejunal
culture and inadequacy of breath hydrogen testing. Gastroenterology. 1990;98:302-309.
ISI
| PUBMED
21. Koetse HA, Stellaard F, Bijleveld CM, et al. Non-invasive detection of low-intestinal lactase activity in children
by use of a combined 13CO2/H2 breath test. Scand J Gastroenterol. 1999;34:35-40.
ISI
| PUBMED
22. Eddy DM, Nugent FW, Eddy JF, et al. Screening for colorectal cancer in a high risk population results of
a mathematical model. Gastroenterology. 1987;92:682-692.
ISI
| PUBMED
23. Thoeni RF, Menuck L. Comparison of barium enema and colonoscopy in the detection of small
colonic polyps. Radiology. 1977;124:631-635.
ABSTRACT
24. Thoeni RF, Petras A. Detection of rectal and rectosigmoid lesions by double-contrast barium
enema examination and sigmoidoscopy. Radiology. 1982;142:59-62.
FREE FULL TEXT
25. Aggarwal V, Mittal SK, Kumar N, Chowdhury V. A comparative study of double contrast barium enema and colonoscopy
for evaluation of rectal bleeding in children. Trop Gastroenterol. 1995;16:132-137.
PUBMED
26. Weinstein MC, ed, Feinstein HV, ed. Clinical Decision Analysis. Philadelphia, Pa: WB Saunders Co; 1980:114-121.
27. Drossman DA, Camilleri M. Irritable bowel syndrome: a technical review for practice guideline
development. Gastroenterology. 1997;112:2120-2137.
FULL TEXT
|
ISI
| PUBMED
28. Longstreth GF, Wolde-Tsadik G. Irritable bowel-type symptoms in HMO examinees: prevalence, demographics,
and clinical correlates. Dig Dis Sci. 1993;38:1581-1589.
FULL TEXT
|
ISI
| PUBMED
29. Kay L, Jorgensen T, Jensen KH. The epidemiology of irritable bowel syndrome in a random population:
prevalence, incidence, natural history and risk factors. J Intern Med. 1994;236:23-30.
ISI
| PUBMED
30. Hamm LR, Sorrells SC, Harding JP, et al. Additional investigations fail to alter the diagnosis of irritable
bowel syndrome in subjects fulfilling the Rome criteria. Am J Gastroenterol. 1999;94:1279-1282.
FULL TEXT
|
ISI
| PUBMED
31. 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
|
ISI
| PUBMED
32. Sonnenberg A, Townsend WF, Müller AD. Evaluation of dyspepsia: cost-benefit analysis of different approaches. Eur J Gastroenterol Hepatol. 1995;7:655-659.
ISI
| PUBMED
 CiteULike  Connotea  Del.icio.us  Digg  Reddit  Technorati
What's this?
RELATED ARTICLE
Archives of Internal Medicine Reader's Choice: Continuing Medical Education
Arch Intern Med. 2001;161(3):487-488.
FULL TEXT
|
