DOI:10.2214/AJR.07.3155
AJR 2008; 191:175-181
© American Roentgen Ray Society
Is Small-Bowel Radiography Necessary Before Double-Balloon Endoscopy?
Takayuki Matsumoto1,
Motohiro Esaki,
Shinichiro Yada,
Yukihiko Jo,
Tomohiko Moriyama and
Mitsuo Iida
1 All authors: Department of Medicine and Clinical Science, Graduate School of
Medical Sciences, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka
812-8582, Japan.
Received September 14, 2007;
accepted after revision January 8, 2008.
Address correspondence to T. Matsumoto
(matane{at}intmed2.med.kyushu-u.ac.jp).
Abstract
OBJECTIVE. Small-bowel radiography may be replaced by enteroscopy in
the diagnosis of small-intestine lesions. We retrospectively elucidated the
diagnostic yield of small-bowel radiography performed before double-balloon
endoscopy.
MATERIALS AND METHODS. One hundred twenty-four patients who
underwent double-balloon endoscopy during the period 2004–2006 were
classified into those with abnormal radiographic findings (n = 45),
normal radiographic findings (n = 31), and no small-bowl radiographs
(n = 48). The classification was based on the use of small-bowel
radiography and the diagnosis before double-balloon endoscopy. The indications
for, approaches to, and diagnostic yields of double-balloon endoscopy were
compared for the three groups. The diagnostic yield of small-bowel radiography
was considered positive when any sign of pathologic change in the small bowel
was identified. The diagnostic yield of double-balloon endoscopy was
considered positive when endoscopic or biopsy findings explained the clinical
manifestations.
RESULTS. The group with abnormal findings on small-bowel radiography
was younger (15–86 years) and less frequently had obscure bleeding
(8.9%) than the group with normal findings on small-bowel radiography (age,
17–84 years; frequency of obscure bleeding, 45.2%) (p = 0.01)
or the group without small-bowel radiographs (age, 15–91 years;
frequency of obscure bleeding, 64.6%) (p < 0.0001). The positive
diagnostic yield of double-balloon endoscopy was highest in the group with
abnormal findings on small-bowel radiography (71.1%), followed by the group
with no small-bowel radiographs (45.8%) and the group with normal findings on
small-bowel radiography (35.5%) (p = 0.0002). Among patients who did
undergo small-bowl radiography, the accuracy of the technique was 68.4%, the
positive predictive value was 71.1%, and the negative predictive value was
64.5%. The positive diagnostic yields of small-bowel radiography and
double-balloon endoscopy were not statistically different (59.2% for
small-bowel radiography, 56.6% for double-balloon endoscopy; p >
0.1).
CONCLUSION. The diagnostic accuracy of double-balloon endoscopy
seems to improve if the procedure is preceded by small-bowel radiography.
Keywords: diagnosis • enteroscopy • small-bowel radiography
Introduction
It has become possible to evalu ate an extensive area of the small
intestine with endoscopy. Video cap sule endoscopy is a noninvasive procedure
performed with a wireless capsule
[1]. Another procedure is an
invasive method performed with a conventional enteroscope and an overtube
[2,
3]. Because it is performed
with two balloons attached to the tips of the scope and the overtube, the
latter procedure is called double-balloon endoscopy. Double-balloon endoscopy
is performed through the mouth and the anus, thus total evaluation is achieved
at metachronous antegrade and retrograde double-balloon endoscopic procedures
[3,
4]. In addition, forceps biopsy
and therapeutic interventions can be performed during double-balloon endoscopy
[2–4].
It thus seems likely that the value of double-balloon endoscopy increases in
cases in which appropriate complementary screening procedures are
performed.
Video capsule endoscopy has been found superior to small-bowel radiography
in the detection of pathologic conditions in the small intestine
[5–7],
especially Crohn's disease
[8–11]
and intestinal polyposis [12].
However, video capsule endoscopy is not optimal for localization of pathologic
changes in the small bowel, and when preparation is poor or intestinal
strictures are present, lesions can be missed. For these reasons, small-bowel
radiography, especially with the double-contrast technique, has been suggested
as a complementary procedure to video capsule endoscopy
[13,
14]. It also has been
suggested
[15–18]
that double-balloon endoscopy is equivalent or even superior to video capsule
endoscopy for the diagnosis of small-intestine lesions in patients with
gastrointestinal bleeding of obscure origin. In this investigation, we
retrospectively analyzed the contribution of small-bowel radiography to the
diagnostic yield of double-balloon endoscopy.
Materials and Methods
Patients
We reviewed all the clinical records of patients examined with
double-balloon endoscopy at our institution during the 3-year period January
2004–December 2006. During that period, 177 double-balloon endoscopic
procedures were per formed on 127 patients. Three patients underwent
retrograde double-balloon endoscopy because difficulty had been encountered at
colonoscopy. The other 124 patients (53 women, 71 men; mean age, 53 years;
range, 15–91 years) who underwent double-balloon endoscopy for
exploration of the small intestine were the subjects of this study.
We routinely perform small-bowel radiography before double-balloon
endoscopy. The patients were thus informed of both examinations. Patients who
refused small-bowel radiography were not exam ined with that procedure. In the
cases of patients with poor performance status or whose condition necessitated
an immediate diag nostic procedure, we discussed the decision mak ing for the
diagnos tic evaluation with the refer ring physicians.
Indication for Small-Bowel Examinations
The indications for small-bowel radiography and double-balloon endoscopy
were divided into three categories modified from those described by Davies et
al. [19] in 1995. The first
category was obscure bleeding, defined as a clinical manifestation that
includes all three of the following symptoms: hemoglobin concentration less
than 11 g/dL, apparent hematochezia or positive result of a fecal occult blood
test for 2 days or more, and normal findings at both
esophagogastroduodenoscopy and total colonoscopy. Twelve of our 49 patients
with obscure bleeding were further examined with scinti graphy with normal
results. The second cate gory of indications for small-bowel examination was
polyposis of the gastro intestinal tract detected with esophago gastro duo
denoscopy or total colonoscopy. The third category of indic ations was
symptoms sug gestive of tumorous, in flammatory, or miscellaneous pathologic
con ditions of the small intestine. These symptoms included abdominal pain,
vomiting, diar rhea, weight loss, fever, and malabsorption. The indi cation
was obscure bleeding for 49 patients, poly posis for 18 pa tients, and other
symptoms for 57 patients.
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Fig. 2A — 60-year-old man with obscure gastrointestinal bleeding.
Biopsy specimens contained adenocarcinoma. Double-contrast small-bowel
radiograph depicts thickened folds and diminutive protrusions in middle
portion of small intestine.
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Fig. 2B — 60-year-old man with obscure gastrointestinal bleeding.
Biopsy specimens contained adenocarcinoma. Double-balloon endoscopic image
shows thickened folds in middle of small intestine. Biopsy revealed follicular
lymphoma.
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Small-Bowel Radiography
In the two groups who underwent small-bowel radiography, imaging was
performed with a double-contrast technique described previously
[20]. In brief, patients were
prepared with insertion of a nasojejunal tube under fluoroscopic guidance. The
tube was fixed at the ligament of Treitz by means of pneumodilation of the
balloon at the tip of the tube. Barium sulfate (200–300 mL, 70%
volume/weight) was slowly injected through the tube until the terminal ileum
was filled with the contrast material. The small intestine was then inflated
with 800–1,000 mL of air injected through the tube. When sufficient
inflation was achieved, 40 mg of scopolamine butyl bromide was injected IV to
inhibit peristalsis and for acquisition of double-contrast images (Figs.
1A and
2A).
Double-Balloon Endoscopy
Double-balloon endoscopy was performed with a double-balloon enteroscopy
system (Fig. 3A,
3B). Antegrade double-balloon
endoscopy was perform ed through the mouth and retrograde double-balloon endo
scopy through the anus as described by Yamamoto et al.
[2,
3]. With the patient under
light sedation with 5 mg of midazolam, the scope and the overtube were
advanced to the small intestine with reciprocal inflation and deflation of the
balloons attached to the tips. During insertion of the scope, the balloon of
the overtube was inflated and attached to the small-intestine wall. As an
alter native, the balloon of the scope was inflated and attached to the
intestinal wall during insertion of the overtube. When necessary, the overtube
was advanced under fluoroscopy. At the most distal site during antegrade
double-balloon endoscopy and at the most proximal site during retrograde
double-balloon endoscopy, the small-intestine mucosa was marked with a tattoo
by means of submucosal injection of sterilized ink through an injection
catheter. The small intestine within the reach of the scope was then examined
carefully (Figs. 1B and
2B). Forceps biopsy was
performed if the enteroscopist deemed it necessary.
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Fig. 3B —Double-balloon endoscopy system. Photograph shows two
balloons at tips of enteroscope and overtube. During procedure, balloons are
reciprocally inflated with air and attached to small-intestine wall.
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Assessment of Radiography and Double-Balloon Endoscopy
Three observers reviewed the small-bowel radiographs. Patients with
radiographic signs considered significant by two or more observers were placed
in the abnormal findings group. The others were in the normal findings group.
Double-balloon endoscopy findings were assessed by the enteroscopist. In
patients with obscure bleeding, the enteroscopic diagnosis was made on the
basis of the endoscopic finding. In patients who underwent double-balloon
endoscopy because of polyposis and other symptoms, the double-balloon
endoscopic diagnosis was established in consideration of both endoscopic and
histologic findings. The diagnostic yield of double-balloon endoscopy for
these patients was considered positive when either endoscopic or histologic
examination revealed significant findings explain ing the symptoms.
The patients were divided into three groups according to the small-bowel
radiographic findings: those with the diagnosis of a pathologic condition of
the small intestine on the basis of small-bowel radiographic findings, those
who had normal small-bowel radiographic findings, and those who did not
undergo small-bowel radiography. We compared the positive diagnostic yield of
double-balloon endoscopy for the three patient groups. We also assessed the
diagnostic values (sensitivity, specifi city, accuracy, and positive and
negative predictive values) of small-bowel radiography and compared them with
the findings for patients examined with both procedures.
Statistical Analysis
Continuous variables were expressed as median and range and were compared
among the groups with use of the Kruskal-Wallis test and the Mann-Whitney
test. Categoric variables were expressed as percentages and compared among the
groups with the chi-square test or Fisher's exact probability test. The
diagnostic yields of small-bowel radiography and double-balloon endoscopy were
compared with use of the McNemar test. Stepwise logistic regression analysis
was performed to evaluate significant variables, which affected the diagnostic
yield of double-balloon endoscopy. All statistical values were calculated with
a two-tailed method with statistical software (SPSS version 10.0 for Microsoft
Windows, SPSS Japan). A value of p < 0.05 was considered
significant.
Results
A total of 174 double-balloon endoscopy procedures were performed on 124
patients. There were no serious complications related to the double-balloon
endoscopy procedures. Seventy-six of the 124 patients underwent small-bowel
radiography, and the examinations were completed without complications.
Small-bowel radiography depicted radiographic signs of small-intestine lesions
in 45 patients; the results were negative in the other 31 patients.
Forty-eight patients did not undergo small-bowel radiography.
Comparison of Clinical and Procedure-Related Features Among Groups
The three groups were heterogeneous in clinical features and in the
double-balloon endoscopy procedure used. As shown in
Table 1, the group with
abnormal findings on small-bowel radiography was significantly younger (median
age, 48 years; range, 15–86 years) than the group with normal
small-bowel radiographic findings (median age, 58; range, 17–84 years)
and the group who did not undergo small-bowel radiography (median age, 62;
range, 15–91 years) (p < 0.01). In addition, the indications
for double-balloon endoscopy were different for the groups (p <
0.0001). Obscure bleeding was the most frequent indication in the group who
did not undergo small-bowel radiography (65%) but was the indication for 45.2%
of the group with normal small-bowel radiographic findings and only 8.5% of
the group with abnormal findings on small-bowel radiography. Indications other
than obscure bleeding and polyposis were most frequent in the group with
abnormal findings on small-bowel radiography (71.1%).
The antegrade approach was used most frequently in the group with positive
findings on small-bowel radiography (42.2%), and the retrograde approach was
used most in the groups with negative findings on small-bowel radiography
(54.8%) and who did not undergo small-bowel radiography (41.7%). Both
antegrade and retrograde approaches were used in the cases of 20.0% of the
patients in the group with abnormal findings on small-bowel radiography, 29.0%
of the group with normal small-bowel radiographic findings, and 29.7% of the
group who did not undergo small-bowel radiography. The route of double-balloon
endoscopy was not different among the three groups.
Final Diagnosis
The final diagnoses established with a combination of small-bowel
radiographic, double-balloon endoscopic, surgical, and histologic findings are
summarized in Table 2.
Seventy-four (59.7%) of the patients were found to have pathologic conditions
of the small intestine. The diagnoses included localized tumors in 10
patients, gastrointestinal polyposis in 13 patients, vascular lesions in 16
patients, inflammatory disease in 30 patients, and other diseases in five
patients. The small-intestine lesion was more frequently verified in the group
with abnormal findings on small-bowel radiography (38 [84.4%] of 45 patients)
than in the group with normal small-bowel radiographic findings (13 [41.9%] of
31 patients) and the group who did not undergo small-bowel radiography (22
[45.8%] of 48 patients) (p < 0.0001). The prevalence of
small-intestine lesions, however, was not different between the group with
normal small-bowel radiographic findings and the group who did not undergo
small-bowel radiography.
Comparison of Diagnostic Yield of Double-Balloon Endoscopy Among Groups
Sixty-five patients had abnormal findings at double-balloon endoscopy. When
the indications were taken into consideration, the positive diagnostic yield
of double-balloon endoscopy among patients with polyposis was not different
between the two small-bowel radiography groups (77.7% vs 66.7%)
(Table 3). However, the
positive yield of double-balloon endoscopy among patients with obscure
bleeding and those with other symptoms was higher in the group with abnormal
findings on small-bowel radiography than in the group with normal small-bowel
radiographic findings. The overall positive diagnostic yield was significantly
different among the three groups (p = 0.0002), the highest value
(71.1%) occurring in the group with abnormal findings on small-bowel
radiography followed by the group who did not undergo small-bowel radiography
(45.8%) and the group with normal small-bowel radiographic findings
(35.5%).
Stepwise logistic regression analysis revealed that age, sex, indication,
and approach to double-balloon endoscopy did not affect the diagnostic yield
of double-balloon endoscopy. Small-bowel radiographic findings, how ever, were
a significant variable affecting the diagnostic yield of double-balloon
endoscopy. Normal findings on small-bowel radiography (odds ratio, 0.18; 95%
CI, 0.06–0.54) and no small-bowel radiography (odds ratio, 0.24; 95% CI,
0.09–0.69) contributed significantly to the diagnostic yield of
double-balloon endoscopy compared with abnormal small-bowel radiographic
findings.
Diagnostic Results of Small-Bowel Radiography
Table 4 indicates the
sensitivity, specificity, accuracy, positive predictive value, and negative
predictive value of small-bowel radiography among 76 patients. Small-bowel
radiography had a sensitivity of 74.4% and specificity of 60.6% for positive
double-balloon endoscopic diagnosis with a prevalence of 56.6%. Both the
accuracy (68.4%) and the positive predictive value (71.1%) of a double-balloon
endoscopic diagnosis increased when small-bowel radiography was performed
first.
Table 5 shows the results of
a comparison of the diagnostic yield of small-bowel radiography with that of
double-balloon endoscopy. Small-bowel radiography depicted abnormalities in 45
(59.2%) of 76 patients, and double-balloon endoscopy did so in 43 (56.6%) of
the patients. Small-bowel radiography and double-balloon endoscopy had
concordant findings in 52 (68.4%) of the patients, 32 of whom had abnormal
findings. The diagnosis was discordant in the other 24 patients. Among the 24
patients, the small-bowel radiographic findings were normal in 11 patients,
and the double-balloon endoscopic findings were normal in 13 patients. The
diagnostic yield was not statistically different between small-bowel
radiography and double-balloon endoscopy. All 13 patients with abnormal
small-bowel radiographic and normal double-balloon endoscopic findings had
indications other than occult bleeding. In addition, five patients had
undergone abdominal surgery, and eight patients had radiographic signs of
diffuse inflammation. In contrast, five of 11 patients with normal findings on
small-bowel radiography and abnormal double-balloon endoscopic findings were
examined because of occult bleeding.
Discussion
The results of our retrospective study indicate that abnormal findings were
made more frequently in patients who had abnormal findings on small-bowel
radiography than in those with normal small-bowel radiographic findings or
those who were not examined with small-bowel radiography. Furthermore, the
positive diagnostic yield was not different between double-balloon endoscopy
and small-bowel radiography in patients who underwent both procedures. Because
we did not find any other clinical factors predictive of abnormal findings at
double-balloon endoscopy, performing small-bowel radiography first seems to be
the hallmark for decision making for double-balloon endoscopy among patients
with suspected small-intestine lesions.
Since the introduction and establishment of the procedure, double-balloon
endoscopy has become widely accepted, especially in Europe, for the diagnosis
and management of pathologic conditions of the small intestine
[21–24].
Results of single- and multiple-center analyses indicate that double-balloon
endoscopy has contributed greatly to the identification of small-intestine
lesions. Although the investigations have proved the safety and feasibility of
double-balloon endoscopy, to our knowledge, the diagnostic yield of
double-balloon endoscopy has not been compared with that of small-bowel
radiography. In four prospective investigations
[15–18]
with small sample sizes, the diagnostic yield of video capsule endoscopy was
compared with that of double-balloon endoscopy. In those investigations,
abnormal findings were identified more frequently with video capsule endoscopy
than with double-balloon endoscopy in patients with obscure bleeding
[15–17],
although the diagnostic yield of the latter procedure was greater in patients
with suspected small-intestine protrusions or ulcers
[15,
18]. It thus seems possible
that the yield of each diagnostic procedure varies with indication in patients
with suspected small-intestine lesions.
In our retrospective analysis, the prevalence of abnormal findings at
double-balloon endoscopy was not affected by indications. It was determined by
the result of preceding small-bowel radiography. This observation was further
supported by the results of logistic regression analysis, which indicated
abnormal findings on small-bowel radiography were the single independent
factor associated with abnormal findings at double-balloon endoscopy. From our
results and in consideration of the prolonged examination time, the risk of
complications, and the invasiveness of double-balloon endoscopy, small-bowel
radiography seems an inevitable procedure for the diagnosis of small-intestine
lesions. The two procedures also seem complementary; one third of our patients
with normal findings on small-bowel radiography had significant findings on
double-balloon endoscopy.
During the initial period of use of video capsule endoscopy, the diagnostic
value of the procedure was tested in comparison with radiography in patients
with obscure bleeding. This issue was initially examined by Costamagna et al.
[5], who found a higher
diagnostic value of video capsule endoscopy (45%) than of barium
follow-through examination (20%). An extremely lower yield of barium
follow-through examination was found in an investigation by Hara et al.
[7] in which the positive rate
was only 3% for barium follow-through examination and 55% for video capsule
endoscopy. Results of a meta-analysis indicated that barium follow-through
examination was less sensitive in the identification of small-bowel lesions
causing obscure bleeding [25].
Although the number of subjects was small, we detected abnormal findings in
only four of 18 patients with obscure bleeding, even with small-bowel
radiography with the double-contrast technique. These observations suggest
that enteroscopy, rather than small-bowel radiography, is the first choice of
procedure in the care of patients with obscure bleeding.
Comparisons have been attempted for specific categories of small-intestine
lesions—Crohn's disease
[9,
10,
26–28]
and other forms of gastrointestinal polyposis
[12,
29]. In the former category, a
meta-analysis showed video capsule endoscopy superior to barium follow-through
examination for initial diagnosis and for diagnosis of recurrence
[28]. Three prospective
studies have shown video capsule endoscopy superior to detailed enteroclysis
in the detection of diminutive small-intestine lesions of Crohn's disease
[10,
26,
27]. In patients with
gastrointestinal polyposis, the diagnostic yield of each procedure was
assessed more optimally with the incidence and number of protrusions in the
small intestine. Brown et al.
[29] detected greater numbers
of small-bowel polyps with video capsule endoscopy than with barium
follow-through in 19 patients with Peutz-Jeghers syndrome. In an investigation
in which the subjects were 24 patients with Peutz-Jeghers syndrome or familial
adenomatous polyposis, Mata et al.
[12] identified
small-intestine polyps more frequently (29%) with video capsule endoscopy than
with barium follow-through examination (13%). Because of these observations,
video capsule endoscopy has been suggested as an alternative to barium
follow-through in the diagnosis of small-intestine lesions.
In contrast to data reported previously, our data showed small-bowel
radiography equal to double-balloon endoscopy in the identification of
small-intestine lesions in patients with heterogeneous indications for
enteroscopy. The favorable diagnostic yield of small-bowel radiography in our
patients seems partly explained by the characteristics of our procedure,
namely state-of-the-art double-contrast technique with barium and a large
amount of air. Because even conventional enteroclysis with barium diluted in
methylcellulose solution has been shown superior to CT enteroclysis and MR
enteroclysis in the depiction of diminutive mucosal alterations
[30–33],
our double-contrast technique may be more appropriate for mucosal lesions of
the small bowel. It thus seems possible that a certain proportion of patients
with abnormal findings on double-contrast small-bowel radiography who have
inflammatory or miscellaneous diseases can avoid diagnostic double-balloon
endoscopy.
There were several limitations in the interpretation of our results. First,
we may have underestimated the diagnostic value of double-balloon endoscopy
because we included patients in whom total enteroscopy could not be performed.
However, because the prevalence of abnormal findings at double-balloon
endoscopy among our subjects (52.4%) was similar to those of other
investigations [3,
21–24,
34], false-negative findings
at double-balloon endoscopy seem to have contributed little to our results.
Second, we may have overestimated small-bowel radiography because the number
of patients with obscure bleeding was small and the prevalence of vascular
lesions was low. Whereas small-bowel radiography is theoretically
inappropriate for flat, diminutive vascular lesions such as angiodysplasia and
portal hypertensive enteropathy, those lesions were identified in only 22% of
our patients with abnormal finding at enteroscopy. In other investigations
from Western countries
[21–24,
34], the incidence of vascular
lesions was much higher among patients with abnormal findings at
double-balloon endoscopy. Third, the retrospective nature of the study
resulted in biases in the background of the study populations. There were
trends toward use of double-balloon endoscopy without small-bowel radiography
in the care of aged patients with bleeding and toward use of both examinations
in the care of adolescent patients with presumably inflammatory or
miscellaneous diseases. We thus might have underestimated the diagnostic value
of double-balloon endoscopy to patients who did not undergo small-bowel
radiography. A prospective randomized study with standardized inclusion
criteria is warranted to determine the practical role of small-bowel
radiography before double-balloon endoscopy.
The results of our retrospective analysis indicated that small-intestine
lesions were found more frequently at double-balloon endoscopy of patients
with abnormal small-bowel radiographic findings than in those with normal
small-bowel radiographic findings or those not examined with small-bowel
radiography. In addition, the positive diagnostic yield was not significantly
different between double-balloon endoscopy and small-bowel radiography. These
results suggest that invasive double-balloon endoscopy should not necessarily
be the first choice of procedure for the evaluation of suspected
small-intestine lesions. The roles of small-bowel radiography and, preferably,
video capsule endoscopy in combination with double-balloon endoscopy need to
be evaluated prospectively to establish a diagnostic and therapeutic algorithm
for pathologic conditions of the small intestine. In addition, CT and MR
enteroclyses seem likely complementary tools because the image quality of
these procedures has improved dramatically
[35–37].
The issue needs to be elucidated further because enteroscopy has become more
routinely used than it was previously.
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Abstract
Introduction
