DOI:10.2214/AJR.07.2068
AJR 2007; 189:W84-W89
© American Roentgen Ray Society
Intrabiliary Rupture of Hepatic Hydatid Cysts: Diagnostic Accuracy of MR Cholangiopancreatography
Ay
e Erden1,
Necati Örmeci2,
Suat Fitoz1,
lhan Erden1,
Sumru Tanju1 and
Yasemin Genç3
1 Department of Radiology, Ankara University School of Medicine,
Talatpaa Bulvari, Sihhiye, 06100, Ankara, Turkey.
2 Department of Gastroenterology, Ankara University School of Medicine, Ankara,
Turkey.
3 Department of Biostatistics, Ankara University School of Medicine,
Talatpaa Bulvari, Sihhiye, 06100, Ankara, Turkey.
Received November 23, 2006;
accepted after revision March 26, 2007.
Address correspondence to A. Erden
(ayse.erden{at}medicine.ankara.edu.tr).
WEB This is a Web exclusive article.
Abstract
OBJECTIVE. The purpose of this study was to establish the role of MR
cholangiopancreatography (MRCP) in the diagnosis of biliary rupture in hepatic
hydatid disease. We sought to determine whether the morphologic features of
cysts and bile duct abnormalities detected on MRCP are specific enough for
identification of intrabiliary rupture.
CONCLUSION. If one of the following MRCP findings of apparent
connection between hydatid cyst and biliary system, deformation of cyst, focal
defect in cyst wall, or beaklike projection extending from cyst wall was
present in a patient with hepatic hydatid cyst, the sensitivity of MRCP was
91.7% and the specificity was 82.8% for identification of intrabiliary
rupture.
Keywords: hydatid cyst • liver • MR cholangiopancreatography
Introduction
One of the most frequent complications of hepatic hydatid disease is
rupture of cysts into the bile ducts. The communication between the biliary
tree and the hydatid cyst can be frank or occult. The most common clinical
manifestations of frank intrabiliary rupture are colicky right hypochondrial
pain and obstructive jaundice accompanied by fever and chills
[1,
2]. Occult rupture, on the
other hand, usually has no clinical signs, and the most common symptom, if
present, is abdominal pain. Occult cystobiliary communication can cause
postoperative biliary fistulas unless the opening in the bile duct is detected
and properly sutured during the surgery
[2]. Laboratory investigations
show an elevated WBC count and serum bilirubin level and cholestasis
[2] in patients with positive
results of serologic tests. The diagnosis can be suspected in the presence of
these clinical findings and laboratory data
[1,
2]. Imaging, however, is needed
for detection of the hydatid cyst and prompt localization of the intrabiliary
rupture, which necessitates early surgical intervention
[1,
2].
ERCP is the reference standard in the diagnosis of many biliary tract
abnormalities and probably is the most reliable preoperative imaging method
for visualization of biliary rupture
[3]. Galati et al.
[4] reported that preoperative
ERCP is useful in the care of patients with cystobiliary fistula because it
allows visualization of the fistula and drainage of the biliary tree and is
associated with an 11.1% to 7.6% reduction in the incidence of postoperative
complications.
MR cholangiopancreatography (MRCP) is rapidly replacing diagnostic ERCP in
the management of various biliary diseases. MRCP is a promising tool in the
detection of cystobiliary communication and provides complementary information
about the entire region affected by the hydatid cyst
[5]. However, the diagnostic
accuracy of MRCP in patients with intrabiliary rupture has not been
quantified, to our knowledge. Most of the MR cholangiographic information
about biliary rupture has been provided in the form of isolated case reports
[6,
7] describing frank
communication. There remains a poor understanding of the indirect MRCP
findings. Therefore, we aimed to establish the role of MRCP in the diagnosis
of biliary rupture associated with hepatic hydatid disease. We also sought to
determine whether the morphologic features of the cysts and bile duct
abnormalities detected on MRCP are specific enough for identification of
intrabiliary rupture.
Materials and Methods
Study Group
Fifty-four patients (39 females and 15 males; mean age, 46.7 years) with
liver hydatid disease diagnosed on the basis of results of serologic tests and
abdominal sonography were referred for MRCP to exclude biliary tract
involvement. Eighteen of the patients had undergone surgery. No data regarding
postoperative complications, such as the possibility of communication with the
biliary system, were present in their records.
Twenty-nine of the 54 patients with symptoms and laboratory results
suggesting biliary involvement underwent ERCP as part of the pretreatment
evaluation. Five other patients, who had symptoms of acute abdomen, underwent
emergency surgical intervention without undergoing ERCP. The surgical records
and postoperative T-tube cholangiograms of these five patients were used for
comparison with MRCP findings. These 34 patients whose ERCP findings or
surgical data and T-tube cholangiograms were available as reference standards
for the analysis of MRCP signs made up the study group (27 females and seven
males; mean age, 45.9 years; age range, 16-75 years). The interval between
MRCP and ERCP or surgery was 5-43 days (mean, 18 days). In 20 of the original
54 cases, standard reference information was not available, and the patients
were excluded from the study.
MRI Technique
MRI was performed with a torso phased-array coil in a 1-T unit (Signa LX
Horizon, GE Healthcare). MRCP was heavily T2-weighted by use of a single-shot
fast spin-echo sequence and both thin (multiple sections) and thick
collimation (single section). Thin-collimation images were obtained in the
axial and coronal planes with respiratory triggering at a section thickness of
3 mm. For 14 patients whose initial images suggested intrabiliary rupture,
3-mm sections obtained in the sagittal plane also were included. The imaging
parameters were as follows: TR/TE, 3,000-30,000/850-970 adapted automatically
with software according to the patient's respiration pattern and the number of
slices; echo-train length, 25; bandwidth, 31.2 kHz; matrix size, 256 x
224-256; number of excitations, 0.5; field of view, 36-46 cm. From the
thin-collimation source images, reconstructions of the biliary system were
generated with a maximum-intensity-projection (MIP) algorithm.
Thick-collimation images were obtained in the coronal or coronal oblique plane
with breath-hold technique. During the single-section acquisition, 13-15
coronal sections 20-70 mm thick were obtained. The breath-hold duration for
each thick slice was 2 seconds. Parameters for the thick-collimation images
were as follows: 1,700-15,000/900-1,100; bandwidth, 25-31.2 kHz; matrix size,
256 x 224-256; number of excitations, 0.5-1.0; field of view, 35-40 cm.
In addition, axial T2-weighted fast spin-echo images (TR varied according to
the patient's breathing pattern; TE, 102 milliseconds; echo-train length,
4-18; section thickness, 8 mm; intersection gap, 1.5; bandwidth, 41.7 kHz;
matrix size, 320 x 192-224; number of excitations, 4; field of view, 36
x 27 cm; acquisition time, 2.05-3.44 minutes) of the upper abdomen were
obtained for better characterization of soft-tissue details.
Review of Data
All of the source, MIP, thick-slab, and T2-weighted fast spin-echo axial
images were evaluated in a retrospective manner by two observers unaware of
the clinical and laboratory data and blinded to the results of other imaging
studies, ERCP, and surgery. The focus of image analysis was to identify
apparent cystobiliary communication, which was assumed to be the direct sign
of intrabiliary rupture
[8].
The observers were asked to record the following three findings that
suggest the presence of communication between a cyst and the biliary system:
deformity of the cyst, defect in the wall of the hydatid cyst, and presence of
a beaklike projection extending from the cyst wall. These findings were
considered indirect signs of intrabiliary rupture. Deformed cyst was defined
as a cyst that had lost its natural smooth round or oval shape. Because it can
be a sequela of intervention or surgical treatment, focal interruption in the
cyst wall also was considered a sign of ruptured hydatid cyst
[8]. Beaklike projection was
assigned to a conical extension of a bile duct with the base faced toward the
cyst [5,
9].
The presence of dilated pericytic ducts distal to a cyst
[8,
10] and intraductal focal loss
of signal intensity (bile ducts containing hydatid cyst material), which have
been reported as indirect signs
[8], also was examined on all
images and tabulated. Dilatation of the pericystic bile ducts was thought to
be related to leakage of cystic fluid into the bile ducts. The reviewers were
asked to record the presence of detached cyst membrane and to document bile
duct changes consisting of displacement of pericystic ducts; stenosis or
complete blockage of the bile ducts due to mass effect of the cyst; and
findings of cholangitis, such as irregularities and focal dilatation
associated with strictures in the course of the bile ducts. Discordant
interpretations were resolved by consensus.
Pericyst is the result of a reaction around a cyst as the cyst grows in
compressed liver tissue [10].
Low signal intensity of this rim on T2-weighted images represents dense
fibrous tissue. The presence of hypointense pericyst on T2-weighted images was
sought in each lesion, and the thickness was measured. A thickness of 5 mm or
less was considered thin pericyst, and a thickness greater than 5 mm was
considered thick pericyst.
Statistical Analysis
To predict the presence of cystobiliary communication, a scoring system was
instituted according to the presence of the following MRCP findings: 1,
apparent connection between the hydatid cyst and the biliary system; 2,
deformation of the cyst; 3, focal defect in cyst wall; 4, beaklike projection
extending from the cyst wall. Each of these findings was scored 1 if present
on MR images and 0 if absent. A patient had a maximum score of 4 when all of
these findings were present. A receiver operating characteristic (ROC) curve
was used to describe the performance of the diagnostic value of the MRCP
score. Youden's index was calculated to detect the best reflected optimal
sensitivity and specificity. The kappa statistic was used for assessment of
interobserver agreement. A kappa value of 0.01-0.20 was considered slight
agreement; 0.21-0.40, fair; 0.41-0.60, moderate; 0.61-0.80, substantial; and
0.81-1.00, almost perfect.
Results
Communication between the cyst and the biliary tree was found at ERCP and
surgery in 12 (35%) of the 34 patients. In these patients, a total of 16 cysts
were found to be ruptured into the biliary ducts. Ten of the ruptured cysts
were in the right lobe of the liver, and six were in the left lobe. The
diameters of the cysts ranged from 2 to 10 cm (mean ± SD, 5.6 ±
2.3 cm). In all patients with intrabiliary rupture, the pericysts were less
than 5 mm thick. The frequency of MRCP findings in patients with intrabiliary
rupture is shown in Table 1.
Apparent cystobiliary communication (Figs.
1A,
1B,
1C and
2A,
2B) was detected in four
patients. The sensitivity, specificity, positive predictive value, negative
predictive value, and accuracy of MRCP for apparent cystobiliary communication
were 33.3%, 100%, 100%, 73.3%, and 76.5%, respectively.
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TABLE 1: Frequency of MR Cholangiopancreatographic Findings in Patients with
Confirmed Intrabiliary Rupture (n = 12)
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Fig. 1A —58-year-old man with five hepatic hydatid cysts 5.5-10 cm in
diameter and true-positive imaging findings. CBD = common bile duct. Coronal
thick-slab MR cholangiopancreatogram shows multiple hydatid cysts and marked
cholangitic changes (open arrow) in proximal bile ducts.
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Fig. 1B —58-year-old man with five hepatic hydatid cysts 5.5-10 cm in
diameter and true-positive imaging findings. CBD = common bile duct. T-tube
cholangiogram obtained 9 days after surgery shows irregular pooling of
contrast material reflecting three residual cavities (thick arrows).
Also evident are fragment of retained hydatid material (thin arrow)
in cavity and diffuse cholangitic changes (open arrow) involving left
lobe.
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Fig. 1C —58-year-old man with five hepatic hydatid cysts 5.5-10 cm in
diameter and true-positive imaging findings. CBD = common bile duct. Sagittal
heavily T2-weighted source image shows interruption of cyst wall and
cystobiliary communication (arrows).
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Fig. 2A —49-year-old woman with surgically confirmed biliary rupture and
true-positive imaging findings. Axial heavily T2-weighted MR image shows
hydatid cyst in right lobe of liver. Cystobiliary communication and defect in
posterolateral aspect of pericyst are apparent. Tiny area of low signal
intensity (arrow) represents intraductal hydatid material.
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Fig. 2B —49-year-old woman with surgically confirmed biliary rupture and
true-positive imaging findings. Maximum-intensity-projection MR image in
coronal plane shows crowding and dilatation of proximal bile ducts associated
with cystobiliary communication (arrow). Splaying of left
intrahepatic bile ducts is secondary to hypertrophy of left lobe. CBD = common
bile duct.
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During analysis, rupture was identified with MRCP in eight cases, which
were ultimately coded as true-positive diagnoses (Figs.
1A,
1B,
1C,
2A,
2B,
3). Eighteen examinations had
true-negative findings for intrabiliary rupture (Fig.
4A,
4B,
4C), four had false-positive
findings (Fig. 5), and another
four had false-negative findings (Fig.
6A,
6B,
6C). Review of four
false-positive diagnoses showed that dilatation of the distal pericystic bile
ducts in all cases was misinterpreted as an indicator of leaked cystic content
(Fig. 5). In two patients,
rupture seemed highly probable on MRCP, but no communication was found on
ERCP. Both deformation in the cyst and detachment of the cyst membrane were
present in two of the patients with false-positive diagnoses.
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Fig. 4A —23-year-old woman without intrabiliary rupture of hepatic hydatid
cyst and true-negative imaging findings. Axial T2-weighted fast spin-echo MR
image shows noncommunicating hydatid cyst. Integrity of pericyst is preserved.
Bile ducts around cyst are massively dilated and appear somewhat
distorted.
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Fig. 4B —23-year-old woman without intrabiliary rupture of hepatic hydatid
cyst and true-negative imaging findings. Coronal thick-slab MR
cholangiopancreatogram shows pericystic bile duct changes characteristic of
cholangitis—ectasia, irregularity, and tortuosity. Intraductal cyst
content and discontinuity of cyst wall are not present.
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Fig. 4C —23-year-old woman without intrabiliary rupture of hepatic hydatid
cyst and true-negative imaging findings. T-tube cholangiogram shows ductal
changes similar to those in B. Lack of opacification of residual cavity
excludes possible cystobiliary communication.
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Fig. 5 —39-year-old woman with hydatid cyst in lateral segment of
left lobe of liver and false-positive imaging findings. Coronal
maximum-intensity-projection MR image shows moderate dilatation
(arrow) of bile duct draining this segment and its close relation to
cyst, which falsely suggest possible cystobiliary communication. CBD = common
bile duct.
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Fig. 6A —34-year-old woman with multiple hydatid cysts of various sizes and
false-negative imaging findings. Coronal thick-slab MR cholangiopancreatogram
shows moderately dilated and distorted bile ducts superimposed on cysts;
however, intrabiliary rupture was not suspected, even on source images. Thick
arrow indicates ruptured cyst. Thin arrow indicates distribution of biliary
radicles similar to that in B. CBD = common bile duct.
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Fig. 6B —34-year-old woman with multiple hydatid cysts of various sizes and
false-negative imaging findings. ERCP image shows straightening and separation
of left intrahepatic bile ducts suggesting mass effect caused by multiple
space-occupying lesions. Collection of contrast material in diaphragmatic
surface of liver is in ruptured hydatid cyst (black arrow). Smooth
cyst (arrowhead) in right lobe is outlined by contrast material.
White arrow indicates distribution of biliary radicles similar to that in
A. GB = gallbladder.
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Fig. 6C —34-year-old woman with multiple hydatid cysts of various sizes and
false-negative imaging findings. Coronal source MR image shows ruptured cyst
(thick arrow) with triangular deformity (thin arrow) found
at retrospective evaluation.
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In one of the four false-negative diagnoses, the reviewers interpreted two
cysts measuring 2.5 and 4.5 cm in diameter connected with each other as
unruptured, although deformation and focal interruption of the walls of the
cysts were present. In another false-negative diagnosis, proximity of seven
large hepatic cysts 6-10 cm in diameter made evaluation difficult. No sign
suggesting rupture was identified even during retrospective analysis. In the
third case, two cysts exhibited membrane detachment. Vague focal interruption
of the cyst wall was seen in one of the cysts, but alone it might not have
been accepted as suggesting the presence of rupture. In the last case, 17
cysts were present in the liver parenchyma, and two of them proved ruptured.
The only sign suggesting the rupture was a deformed appearance of the cysts
(Fig. 6A,
6B,
6C).
The ROC plot showed the relation between the true-positive rate
(sensitivity) and the false-positive rate (1 - specificity) over all possible
decision values. The area under the ROC curve was 0.928 ± 0.055 and was
considered statistically significant (p < 0.001) at separating
patients without rupture of hepatic hydatid disease from patients with
intrabiliary rupture. We defined cutoff values for different levels of
sensitivity and specificity using the ROC curve and Youden's index. A score of
0.5 appeared to be an optimum threshold for determining whether a patient had
rupture at a sensitivity of 91.7% and a specificity of 82.8%. In another
words, if any of the four signs was present in a patient, the sensitivity of
the method was 91.7%, and the specificity was 82.8%.
The kappa values ± SE of interobserver agreement for apparent
cystobiliary communication, deformity of the cyst, defect in the hydatid cyst
wall, and beaklike projection extending from the cyst wall were 
= 1
(p = 0.000), = 0.462 ± 0.162 (p = 0.007),
= 0.454 ± 0.152 (p = 0.004), and = 0.608
± 0.158 (p = 0.000), respectively. The kappa statistics for
the two reviewers had a statistically significant level of agreement regarding
the presence of MRCP findings.
Discussion
The radiologic findings of intrabiliary rupture include direct and indirect
signs [8]. The only direct sign
of rupture is visible communication between the cyst and the biliary tree.
Although the probability of rupture is very high in the presence of this
finding, it was present in only 33% of cases of ruptured cyst in our study.
Deformation of a cyst suggests decreased intracystic pressure and may be the
only indirect sign of intrabiliary rupture. This finding was seen in 75% of
our cases of biliary rupture. However, deformation can be a result of medical
or surgical treatment and does not necessarily indicate rupture. For this
reason, collapse of or decrease in the size of a cyst in the follow-up of
untreated patients may be a more significant sign of rupture.
Pericyst is the outer layer of a cyst and consists of thick and avascular
fibrous tissue-containing bile ducts
[10]. A focal defect in the
pericyst on T2-weighted images was seen in 66.7% of our patients with rupture.
Cyst wall discontinuity is considered a direct sign of rupture and is found in
75% of cases [9]. The diagnosis
of rupture is likely if a bile duct extending from the interrupted wall points
toward the porta hepatis [5,
9]. Beaklike projection from
the cyst wall was seen in 50% of our patients with intrabiliary rupture. A
surgical defect should be considered in the differential diagnosis of cyst
wall defect.
The inner layer of a hydatid cyst, known as endocyst, grows faster than
pericyst, becomes redundant, and folds on itself
[10]. Although it can be the
consequence of aging and ischemia, detachment of endocyst manifesting as
undulating membrane also can be the result of percutaneous treatment and
contained or communicating rupture
[11]. In our study, detachment
of the membrane was seen in 50% of cases of rupture
(Table 1). If a cyst ruptures
to the biliary system, hydatid fragments and particles entering the biliary
tree can cause clinical symptoms simulating cholelithiasis. MRCP showed linear
or leaflike intraductal areas of low signal intensity representing cyst
material in our three patients with frank cystobiliary communication.
Air-fluid [12] and fat-fluid
[8] levels inside the cyst,
rare signs of cystobiliary communication, were not found in our patients.
Ductal displacement by extrinsic compression was the most common (90.9%)
finding in our patients with intrabiliary rupture. Obstructive cholangitis
induced by insufficient biliary drainage was found on MRCP in two thirds of
the cases of rupture. Dilatation of proximal ducts was the most prominent
finding in such cases. However, dilatation of any duct not attributed to mass
effect, particularly of ducts distal to the hydatid cyst, can be
misinterpreted as an indirect sign of rupture. Leakage of cyst fluid into the
bile ducts through an occult wall defect can be considered responsible for the
ductal dilatation. Such dilated pericystic ducts were the main causes of the
four false-positive results in our study. We believe dilated pericystic ducts
should be considered significant only when their entrance into the defective
wall is seen. Visible dilated ducts in the vicinity of a hydatid cyst not
complicated by rupture is seen in 25% of patients
[10].
Inherent limitations of surgery and ERCP might have affected the results of
our study. We chose to use ERCP and surgical findings as the reference
standards for confirming our imaging findings, but the possibility of
false-negative results existed, even at surgery. If the cyst content is not
stained with bile during surgery, simple openings can be missed
[13]. These occult
communications are responsible for the high recurrence rate of complex hydatid
cysts in the postoperative period. Several investigations have shown that in
the presence of suggestive symptoms, cystobiliary communication should
continue to be suspected even in the absence of ERCP findings. Magistrelli et
al. [3] found the
false-negative ratio of ERCP was 17%
[3]. In a study by Shemesh and
Friedman [14], communications
detected during surgical exploration were not found on ERCP in three of six
cases. The investigators speculated that the cause of the false-negative
results was intermittent or temporary occlusion of the rupture site by cyst
content. In these instances, visualization of the cyst with contrast material
usually is difficult despite correct injection pressure
[14]. In addition, small
ruptures are often kept closed by high intracystic pressure and may be
identified only after evacuation of the cyst content
[3]. According to our
observations, an advantage of MRCP over ERCP is capability for assessing ducts
proximal to an obstruction in cases in which ERCP may be unsuccessful. A
possible cystobiliary communication facing the surface of the liver also may
remain unopacified during ERCP.
The combination of ERCP and cross-sectional techniques is preferred for
investigation of biliary rupture of hydatid cysts. Although they are not
considered effective in the detection of intrabiliary rupture, imaging methods
can accurately show the location and morphologic properties of the cysts. Many
reports [5,
8,
11,
12] have shown the usefulness
of sonography, CT, and conventional MRI in the preoperative detection of
ruptured hepatic hydatid cysts. The imaging signs of rupture are documented in
these reports. Except for a study
[5] of a series of nine cases
of ruptured hydatid cyst, in only a few case reports
[6,
7] to our knowledge have MRCP
observations of biliary rupture been described. These reports emphasize signs
of frank rupture. Thus comparison of our observations with similar data was
not possible.
MRCP depicts the entire biliary tree despite obstruction. It enables
topographic evaluation of hydatid cysts and the level of obstruction. Apparent
cystobiliary communication had high specificity as a direct sign of rupture,
the presence of this sign suggesting the diagnosis. Because the sensitivity
was low, the absence of visible communication did not exclude the diagnosis of
rupture. If any of the four signs (apparent cystobiliary communication,
deformation of the hydatid cyst, focal defect in the cyst wall, and beaklike
projection extending from the cyst wall) was present in a patient, the
sensitivity of MRCP was 91.7%, and the specificity was 82.8%. In conclusion,
MRCP findings are sensitive in the identification of intrabiliary rupture due
to hepatic hydatid disease.
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Abstract
Introduction
