Ga strointestina l Imaging • Origina l Research

Barium Enema Evaluation

of Colonic Involvement in
Endometriosis
Niccolò Faccioli1 OBJECTIVE. The purpose of our study was to define the role of double-contrast barium
Riccardo Manfredi1 enema (DCBE) compared with laparoscopy in the diagnosis and local staging of intestinal
Paride Mainardi2 endometriosis.
Emiliano Dalla Chiara2 MATERIALS AND METHODS. A search of our radiology database revealed the cases
Elide Spoto2 of 234 women who underwent surgical resection for pelvic endometriosis with associated
Luca Minelli3 intestinal surgery for intestinal endometriosis. We retrospectively evaluated all preoperative
DCBE images for the presence of bowel endometriosis and the number, site (rectum,
American Journal of Roentgenology 2008.190:1050-1054.

Roberto Pozzi Mucelli1

sigmoid, cecum), and size of the lesions. The radiographic findings at DCBE were
retrospectively cor- related with those at surgical pathologic examination.
RESULTS. DCBE revealed 211 intestinal lesions of bowel endometriosis in 168 (71.8%)
of 234 patients with pelvic endometriosis clinically enrolled. Forty (23.8%) of the 168
women had more than one endometriotic bowel nodule (two nodules in 37 cases, three in
three cases). Laparoscopy revealed 233 intestinal lesions in 174 (74.3%) of the patients.
Fifty-four (31.0%) of 174 women had more than one endometriotic bowel nodule (two
nodules in 49 cases, three in five cases). There was 100% correlation between the DCBE and
histologic findings as far as site and size of the lesions were concerned. DCBE had a
sensitivity of 88.4%, specificity of 93.0%, positive predictive value of 97.5%, negative
predictive of 71.0%, and accuracy of 89.5% in the identification of bowel endometriosis.
CONCLUSION. DCBE is helpful in discerning bowel wall involvement in endometrio-
sis, enabling proper surgical planning. DCBE also appears to have a role in the management
of endometriosis.

elvic endometriosis is a disease asymptomatic and are often diagnosed at

characterized by the presence of surgery [5, 6].
Keywords: bowel endometriosis, double-contrast barium functional endometrial glands Complete laparoscopic excision of bowel
enema, endometriosis, intestinal endometriosis and stroma in locations outside endometriosis offers good long-term symp-

P
the uterine cavity. Five percent to 27% of
DOI:10.2214/AJR.07.3062 women with pelvic endometriosis present
Received August 24, 2007; accepted after revision
with endometriotic implants on the intestinal
October 10, 2007. wall. Bowel endometriosis affects the rectum
and the rectosigmoid junction in 70–85% of
1
Department of Radiology, University of Verona, cases. Less frequent sites are the appendix,
Policlinico G. B. Rossi, Piazzale Scuro 10, 37134 Verona,
cecum, and distal ileum [1–4].
Italy. Address correspondence to N. Faccioli
(nfaccioli@sirm.org). The clinical presentation of bowel endo-
metriosis can mimic irritable bowel syn-
Department of Radiology, Sacro Cuore Hospital, Negrar,
2
drome and, in the most severe cases,
Verona, Italy. obstruc- tive bowel disease. Symptoms are
Department of Gynecology, Sacro Cuore Hospital,
3 related to the site and extent of bowel
Negrar, Verona, Italy. implants. The implants can be single and
discrete or multi- focal and diffuse. The
AJR 2008; 190:1050–1054 lesions also can be superficial, localized to
0361–803X/08/1904–1050
the bowel serosa, or they can invade the
subserosa and the mus- cularis propria,
© American Roentgen Ray Society causing bowel-wall thicken- ing due to
fibrosis. Most lesions, however, are
tomatic relief. To ensure complete removal
of all endometriotic implants, intestinal sur-
gery with or without intestinal resection is
needed. A thorough preoperative evaluation
should be performed to correctly ascertain
the presence, anatomic distribution, and
extent of intestinal endometriosis so that
intestinal surgery can be planned. The
preoperative decision to perform intestinal
surgery greatly influences the type of bowel
preparation, the need for a colorectal
surgeon, the patient’s psychological
acceptance of proctectomy if needed, and
the provision of signed informed consent
[5].
The diagnosis of bowel endometriosis is
challenging because gastrointestinal symp-
toms are not specific. Various imaging tech-
niques have been proposed for the diagnosis

AJR:190, April 2008 1

 Barium Enema of Endometriosis

of bowel endometriosis, but all have limita- (88.5%), rectal pain coincident with menses; and the rectum was obtained. Once barium reached
tions. CT [7–9] and MRI [10–12] have been 99 (42.3%), symptoms of acute, chronic, or the hepatic flexure, the colon was drained by
described, but the importance of double- intermittent bowel obstruction. All women had gravity of as much barium as possible to empty
contrast barium enema (DCBE) in the negative results of serum tests for the rectal ampulla while not completely clearing
preop- erative evaluation of patients with
carcinoembryonic antigen, CA-125, and CA-19.9. the entire rectosigmoid colon. The anticholinergic
suspected intestinal endometriosis has been
agent hyoscine N-butylbromide (Buscopan,
underplayed [13–17]. DCBE has advantages
Surgery Boehringer Ingelheim) was then used to induce
such as ease of performance, low cost, and
All patients underwent surgery with a mean colonic hypotonia. Room air was then gently and
ready availabil- ity. The only disadvantage is
interval between DCBE and surgery of 33 days intermittently insufflated into the colon with an
limited luminal perspective for the
(range, 27–45 days). Independently from the insufflator (Blue Air Bulb Insufflator, Bracco).
examination. The purpose of this study was
findings at DCBE, all women underwent Each colonic segment was viewed in detail on
to define the role of DCBE, particularly in
operative laparoscopy because of the presence of spot radiographs and mid- to high-magnification
the diagnosis and local staging of intestinal
pelvic endometriosis. During laparoscopic digital images. The whole procedure lasted an
endometriosis, by comparing the results with
surgery, laparoscopic segmental resection of the average of 10 minutes with a maximum of 3
those at laparoscopy.
involved part of the intestine was scheduled for minutes of fluo- roscopy. The procedure was well
endo- metriotic nodules larger than 2.5 cm tolerated by 210 (89.7%) of the patients, and 24
Materials and Methods
detected at DCBE and for multiple bowel nodules. (10.2%) of the pa- tients reported mild discomfort.
Patient Population
In all the other patients, superficial excision, In no case was the procedure terminated owing to
This retrospective study was performed in the
serosal shaving, or full-thickness disk excision patient intolerance.
period January 2002–December 2006 (overall
was first attempted, and laparoscopic segmental
duration, 60 months). The study was approved by
resection was considered a second choice. All of Image Analysis
American Journal of Roentgenology 2008.190:1050-1054.

the local institutional review board, and written

the surgical procedures were performed by the The DCBE images were reviewed by a gastro-
informed consent was obtained from all patients.
same surgeon. All visible endometriotic lesions intestinal radiologist with more than 15 years of
Inclusion criteria for the study were clinical symp-
were excised in all patients; when intestinal experience. The radiologist was not aware of the
toms indicative of serious pelvic endometriosis
resection was needed, it was performed by an clinical findings or the patient’s history. Image
(i.e., dyspareunia, dysmenorrhea, or chronic pelvic
intestinal surgeon. analysis included presence of bowel endometriosis
pain), transvaginal sonographic findings of endo-
on the basis of extrinsic mass effect on the bowel
metriosis, gastrointestinal symptoms suggestive of
Histopathology wall, shortening or flattening of the bowel wall,
bowel endometriosis (cramping abdominal pain
Histopathologic criteria for the diagnosis of crenulation of the mucosa, or a combination of
before or during passage of stools; rectal pain
colorectal endometriosis were the presence of these factors [5, 14, 17]; number of lesions; site of
coincident with menses; symptoms of acute,
ectopic endometrial and stromal tissues pene- the lesions (rectum, sigmoid, cecum); and size of
chronic, or intermittent bowel occlusion), and neg-
trating through at least the serosa of the bowel lesions. The radiographic findings on DCBE were
ative results of serum tests for carcinoembryonic
wall. Intestinal endometriosis was confirmed with retrospectively correlated with those at surgical
antigen, CA-125, and CA-19.9. All of the women
pathologic examination of all resected specimens pathologic examination.
who underwent DCBE were believed to have
that were histologically evaluated (serosa, muscu-
intestinal endometriosis. DCBE was performed
laris propria, mucosa). Statistical Analysis
before surgical intervention for pelvic
Sensitivity, specificity, positive predictive
endometriosis and for preoperative localization
Imaging value, negative predictive value, and accuracy
before intestinal resection. Exclusion criteria were
Because of the chronic character of endo- were calculated. The Pearson correlation
previous radiologic examination of the bowel,
metriosis, no attempt was made to schedule coefficient was used to evaluate the correlation
surgery for endometriosis, and bowel surgery
DCBE at a particular phase of the menstrual between the diameter of the endometriotic nodules
other than appendectomy (39 of 234 patients).
cycle. All patients suspended medical therapy estimated at DCBE and the diameter measured at
Before surgery, all patients were informed that
with pro- gestins or gonadotropin-releasing pathologic evaluation. Data were analyzed with
DCBE was being evaluated for the diagnosis of
hormone at least 3 months before the procedure. the SPSS software package (release 10.0.5, SPSS).
bowel endometriosis. Independently of the
All DCBE procedures were performed with a A value of p < 0.05 was considered statistically
findings at DCBE, the patients signed written
fluoroscopic system (Sireskop SX 40, Siemens significant.
informed consent forms that included consent for
Medical Solutions) with motorized table tilt
serosal shave excision or segmental bowel
equipped with an imaging system (Fluorospot Results
resection if endometriotic intestinal lesions were
TOP, Siemens Medical Solutions). Patient prep- Bowel endometriosis was diagnosed with
found.
aration included a low-residue diet for 3 days DCBE in the cases of 168 of 234 clinically en-
The study population consisted of 234 women
before the examination. On the day before rolled patients with pelvic endometriosis. At
(mean age, 31.6 years; range, 22–44 years). All
surgery, the patients ingested 13 tablets of laparoscopy, abnormal findings suggestive of
patients had clinical symptoms of pelvic endo-
glycosides of senna (Pursennid, Novartis Farma) bowel endometriotic nodules were detected in
metriosis: 197 (84.1%) had dyspareunia; 226
and 15 g of magnesium sulfate and followed them 174 patients, and the endometriotic nature of
(96.5%), dysmenorrhea; and 232 (99.1%), chronic
with 2 L of liquids to minimize the dehydration all removed bowel lesions was confirmed at
pelvic pain. All patients had transvaginal sono-
caused by the preparation. Barium in a 100% histologic examination. Bowel lesions were
graphic findings of pelvic endometriosis. All not recognized in 66 patients with DCBE,
weight-to-volume ratio (Prontobario Colon,
patients also had symptoms indicative of bowel and 60 patients did not have bowel lesions at
Bracco) was instilled into the rectum while the
endometriosis: 211 (90.2%) had cramping abdom- surgery.
patient lay in the left- side-down lateral position.
inal pain before or during passage of stools; 207 DCBE depicted 211 intestinal lesions in
A first lateral view of
 Faccioli et al.
168 (71.8%) of the patients. Forty (23.8%) of
 the 168 women had more than one endo-
metriotic bowel nodule (two nodules in 37
cases, three nodules in three cases) (Fig. 1).
At laparoscopy, however, 233 intestinal le-
sions were identified in 174 (74.3%) of the
patients. Fifty-four (31.0%) of the 174 wom-
en had more than one endometriotic bowel
nodule (two nodules in 49 cases, three nod-
ules in five cases).
At DCBE, 113 lesions were found at the
rectum (Fig. 2), 85 at the sigmoid, and 13 at
the cecum. No nodules were found at the ter-
minal ileum. At laparoscopy, 117 nodules
were found at the rectum, 92 at the sigmoid,
and 24 at the cecum. No nodules were found
at the terminal ileum. Two hundred six
(97.6%) of the 211 lesions found at DCBE
were confirmed at surgery and histologic ex-
amination; 194 of 198 (98.0%) of these le-
sions were at the rectum and sigmoid. Four
lesions were not identified: two adnexal in-
American Journal of Roentgenology 2008.190:1050-1054.

flammatory masses originating from the

ovary and involving the bowel wall (Fig. 3)
and two suspected double lesions. Fourteen
of 194 lesions involved the mucosa, 94 the
submucosa, and 86 the serosa.
Twelve (92%) of 13 lesions at the cecum
were confirmed at surgery and histologic ex-
amination (Fig. 4). One lesion was a false-
A B
positive finding. Six lesions involved the
Fig. 1—34-year-old woman with suspected intestinal implants of endometriosis.
mus- cle wall, five the submucosa, and one A and B, Lateral (A) and oblique (B) spot images show three endometriotic lesions exhibiting
lesion only the serosa. Twenty-seven lesions extrinsic mass effect with crenulation of contour and spiculation that are direct signs of infiltration
not pre- operatively recognized were of bowel wall (arrows). Small polypoid lesion (arrowhead) is benign tubular adenoma confirmed
at surgery.
identified at sur- gery. Six of these lesions
were in patients who
had normal findings at DCBE. Fifteen of the
27 lesions were at the sigmoid and 12 at the
cecum. Eleven of the 27 lesions were strictly
adjacent to other lesions correctly identified
at DCBE. Seven of the 27 lesions were
superfi- cial, not infiltrating the muscle wall.
Five le- sions were not recognized because
of diffi- culty depicting them in tricky
locations, such as the appendix and near the
ileocecal valve. In one case residual feces
covered a lesion at the cecum. In another
case nonocclusive stenosis caused poor
passage of contrast me- dium at the cecum,
limiting the evaluation. Two lesions, at the
rectum and the rectosig- moid junction, were Fig. 2—28-year-old woman with suspected sured by the pathologist (Pearson’s correla- tion
intestinal
not identified at DCBE owing to diagnostic implants of endometriosis and finding of coefficient, r = 0.966; p < 0.001).
errors. rectal localization of intestinal endometriosis. Ninety-six nodules were removed with partial-
At DCBE the mean largest diameter of Double- contrast barium enema image shows thickness nodulectomy (superficial excision or
extrinsic mass effect and spiculation (arrow)
the endometriotic nodule was estimated to serosal shaving), 120 with full- thickness
of rectal wall that appears infiltrated. Surgical
be 2.5 ± 1.2 [SD] cm (range, 0.7–7.2 cm). At and histologic findings confirmed intestinal nodulectomy, and 15 with bowel resection.
pathologic evaluation the mean largest diam- implants of endometriosis. Fourteen women underwent bowel resection. One
eter of the endometriotic nodule was 2.5 ± patient underwent two bowel resections because
1.1 cm (range, 0.8–7.1 cm). A statistically she had two endometri- otic nodules, one on the
significant positive correlation was observed rectum and one on the cecum. A small polypoid
for the diameter of the endometriotic lesion at the sigmoid recognized with DCBE was
nodules estimated at DCBE and the diameter mea-
resected and at histologic examination proved to
105 AJR:190, April 2008
be benign tubular adenoma (Fig. 1B). Fig. 3—23-year-old woman with suspected
intestinal
implants of endometriosis. Double-contrast barium
enema examination showed pathologic pelvic process
involving bowel serosa at rectosigmoid
junction.
Finding of extrinsic mass effect and
spiculation (arrows) owing to poor wall
distention after air
insufflation suggested endometriotic wall
infiltration. Histologic examination of these
alterations showed adnexal inflammation
originating from ovary.

The findings were true-positive in

206 cas- es, true-negative in 66, false-
negative in 27, and false-positive in five
of the cases. DCBE had a sensitivity of
88.4%, specificity of 93.0%, positive
predictive value of 97.5%, negative
predictive value of 71.0%, and accu-
racy of 89.5% in the identification of
bowel endometriosis. In all women who
underwent bowel surgery, there was
100% correlation between DCBE and
histologic findings as far as site and
size of the lesions were concerned.

Discussion
Implants of intestinal endometriosis
are typically located on the
antimesenteric edge of

AJR:190, April 2008 105

 ence of endometriotic lesions involving the
bowel, as previously reported and observed
in all patients of our study. Appreciation of
the en face appearance of the crenulated sur-
face pattern is extremely important, because
this abnormality may be the sole finding. At
times, crenulation is quite striking; it can
also be extremely subtle and easily over-
looked by an untrained radiologist. The dif-
ferential diagnoses have been reported to be
many, including inflammatory lesions such
as diverticulitis, pelvic inflammatory dis-
ease, and benign and malignant colonic neo-
plasm. In our experience, only metastatic
A B carcinoma and pelvic abscesses mimicked
Fig. 4—31-year-old woman with suspected intestinal implants of endometriosis and finding of cecal the appearance of endometriosis [5].
localization of intestinal endometriosis.
A, Double-contrast barium enema image of cecum shows endometriotic localization as endoluminal filling Many surgeons [12, 19] are concerned
defect (arrow) due to wide extrinsic mass effect confirmed at surgery. about performing both radiologic and
B, Photograph of surgical specimen shows endometrial glands and stroma infiltrating fibromuscular endoscopic in- vestigations because these
tissue, smooth-muscle proliferation, and fibrous reaction, resulting in thickening of wall with
endometriosis. Multiple cysts (arrow) are present in perivisceral fat tissue. Mucosal sparing is
studies cannot clearly show the depth of
typical of this disease. parietal involvement, as does CT enteroclysis.
American Journal of Roentgenology 2008.190:1050-1054.

That may be true, but we believe that what

the bowel, and their appearance is variable.
Sometimes they appear as small pigmented
nodules on the peritoneum, and at other times
as larger lesions with puckering of the serosa.
The infiltration of the muscularis propria can
determine the presence of mural thickening
and associated luminal stenosis. At histologic
examination, endometrial glands and stroma
are found invading the bowel wall from the
se- rosa inward. The submucosa may be
involved, but an important feature is mucosa
free of dis- ease [1, 13]. Small endometriotic
nodules do not directly cause symptoms but
can become symptomatic with growth.
Widespread nodules infiltrating the muscular
layer cause pain and a range of
gastrointestinal symptoms. Bowel in-
volvement may be suspected on the basis of
the clinical history and the findings at
physical ex- amination but often is a late
diagnosis, some- times found only in the
course of surgery.
A precise diagnosis regarding the
presence, location, and extent of bowel
endometriosis is useful for preoperative
evaluation and sur- gical planning [5]. The
preoperative decision to perform intestinal
surgery greatly influences the type of bowel
preparation, the need for a colorectal
surgeon, the patient’s psychological
acceptance of proctectomy if needed, and
provision of informed signed consent [5]. In
our study, we included only patients who
consented to intestinal surgery, but the rejec-
tion rate at our institution is 16%. The
guide- lines for preoperative assessment of
patients with suspected intestinal
really matters is the pre- operative choice to
perform intestinal surgery
endometriosis are not well established. Most scientific reports have considered
only rectal endometriosis, not endometriosis
of the entire large bowel. The evaluation is
usually performed with several radiologic
techniques, but the ideal technique for the
diagnosis of endometriosis should include not
only the rectum but also the whole colon, the
cecum, and the terminal ileum, even though
this location is extremely rare [18]. Only
DCBE, MRI, and CT enteroclysis can depict
the entire large bowel, but MRI data are
inconclusive. One of the most cited arti- cles
[12] reported a sensitivity of 76.5% and
specificity of 97.9% in the diagnosis of rectal
involvement in women with deep infiltrating
endometriosis, but the authors did not inves-
tigate the whole colon.
MRI is limited in the diagnosis of bowel
endometriosis because the lesions often have
histologic components (e.g., fibrosis) that can
alter the signal intensity pattern. Other limi-
tations are the time required to complete each
imaging study and the presence of mo- tion
artifacts. CT enteroclysis, which can de- pict
nonspecific wall thickening, is a new and
promising technique despite its limitations of
radiation exposure and administration of
iodinated contrast medium to women of re-
productive age [7–9]. DCBE has been used in
the diagnosis of endometriotic lesions of the
bowel, but some authors deny its utility or do
not mention it [13, 16].
At DCBE the presence of an extrinsic mass
effect in association with mucosal fine
crenulation is highly suggestive of the pres-
in accordance with lesion size (less or more
than 2.5 cm). In our study population, we rec-
ognized lesions from 0.7 to 7.2 cm. Unlike
Bis- caldi et al. [8, 9], we did not find it
important to evaluate the infiltration of the
lesion, because the surgeon had to resect all
the foci in evaluat- ing the extent of disease
and intraoperatively determining the correct
surgical approach based on the findings.
Nevertheless, DCBE clearly depicts
preoperatively whether stenosis of the lumen is
present, a finding that can change the surgical
approach.
In our clinical practice DCBE has a role in
the diagnosis of intestinal involvement because
it depicts the classic signs of extrinsic involve-
ment of the visceral wall with satisfactory ac-
curacy. These morphologic features, together
with clinical and anamnestic data, aid in for-
mulation of a differential diagnosis from other
abdominal diseases with parietal involvement.
Of the 27 lesions not identified at DCBE, 12
were at the cecum, a site particularly difficult
to evaluate, but a report [5] in the literature in-
dicates that DCBE has the highest accuracy for
lesions at this site. The false-negative findings
at this site were due to incomplete distention,
residual feces, and stenosis by muscular con-
traction that did not allow passage of contrast
medium. Eleven endometriotic foci at the rec-
tum and sigmoid were not correctly
recognized owing to proximity to other
correctly identified lesions with common
fibrotic involvement of the bowel wall. In nine
cases not identified at DCBE, seven lesions had
superficial implants that were inapparent. Two
cases were not
 effectively recognized at DCBE despite in-
volvement of the muscle wall.
Our results might have been biased be-
cause the population was selected. The find-
ings may not apply to other patients, particu-
larly to young otherwise healthy women
with only dysmenorrhea who would be at
extreme- ly low risk of having bowel
involvement.
Although DCBE is not expensive and is
easy to perform, there are limitations to its
use. The experience of the radiologist in the
diagnosis of bowel endometriosis is most
important. Another limitation is that the
whole abdomen cannot be examined with
DCBE, because only pathologic changes in
the mucosal surface are depicted. Further-
more, the origin of an extrinsic mass altering
the profile of a bowel loop can be difficult to
determine. We believe, however, that young
women selected because of clinical suspicion
American Journal of Roentgenology 2008.190:1050-1054.
of intestinal endometriosis usually do not
have other pathologic conditions. This
supposition was confirmed in our series
because only two (0.8%) of 234 clinically
selected women had other pathologic
conditions that necessitated additional CT or
MRI. Nevertheless, DCBE has to be
preferred to CT because of its lower
radiation dose and over MRI because of its
lower cost. In our practice, the mean time for
fluoroscopy is 3 minutes, and the effective
dose is approximately 6 mSv, one-third the
dose of CT of the abdomen [20].
We evaluated the contribution of DCBE
to the detection and staging of bowel
endometri- osis, assessing presence, site, and
size of le- sions and comparing the results
with those of laparoscopy. To this aim, we
selected only pa- tients with endometriosis,
which limits the statistical value of the data.
The data confirm, however, that DCBE is
highly accurate in the
detection of intestinal endometriosis necessi-
tating subsequent intestinal surgery.
Our data show that in expert hands, find-
ings at DCBE are predictive of bowel wall
involvement in endometriosis and allow
proper surgical planning. The reliability of
DCBE is related to rigorous technique and
operator skill. The technique is inexpensive
and simple to perform and appears to have a
role in the management of endometriosis.
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