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EDUCATION EXHIBIT
135
MR Imaging of
the Gallbladder:
A Pictorial Essay1
CME FEATURE
See accompanying
test at http://
www.rsna.org
/education
/rg_cme.html
LEARNING
OBJECTIVES
FOR TEST 3
After reading this
article and taking
the test, the reader
will be able to:
Discuss
the state䡲
of-the-art MR and
MR cholangiographic imaging techniques for the diagnosis of gallbladder
disease.
䡲 Describe the normal MR imaging features of the gallbladder.
䡲 Identify the MR
imaging appearances
of gallbladder disease.
TEACHING
POINTS
See last page
Onofrio A. Catalano, MD2 ● Dushyant V. Sahani, MD ● Sanjeeva P.
Kalva, MD ● Matthew S. Cushing, MD ● Peter F. Hahn, MD, PhD
Jeffrey J. Brown, MD ● Robert R. Edelman, MD
The gallbladder serves as the repository for bile produced in the liver.
However, bile within the gallbladder may become supersaturated with
cholesterol, leading to crystal precipitation and subsequent gallstone
formation. The most common disorders of the gallbladder are related
to gallstones and include symptomatic cholelithiasis, acute and chronic
cholecystitis, and carcinoma of the gallbladder. Other conditions that
can affect the gallbladder include biliary dyskinesia (functional), adenomyomatosis (hyperplastic), and postoperative changes or complications (iatrogenic). Ultrasonography (US) has been the traditional modality for evaluating gallbladder disease, primarily owing to its high
sensitivity and specificity for both stone disease and gallbladder inflammation. US performed before and after ingestion of a fatty meal may
also be useful for functional evaluation of the gallbladder. However,
US is limited by patient body habitus, with degradation of image quality and anatomic detail in obese individuals. With the advent of faster
and more efficient imaging techniques, magnetic resonance (MR) imaging has assumed an increasing role as an adjunct modality for gallbladder imaging, primarily in patients who are incompletely assessed
with US. MR imaging allows simultaneous anatomic and physiologic
assessment of the gallbladder and biliary tract in both initial evaluation
of disease and examination of the postoperative patient. This assessment is accomplished chiefly through the use of MR imaging contrast
agents excreted preferentially via the biliary system.
©
RSNA, 2008
Abbreviations: BOPTA ⫽ benzyloxypropionictetraacetate, CHD ⫽ common hepatic duct, HIDA ⫽ hydroxyiminodiacetic acid, MnDPDP ⫽ mangafodipir trisodium, SE ⫽ spin-echo, XGC ⫽ xanthogranulomatous cholecystitis, 3D ⫽ three-dimensional
RadioGraphics 2008; 28:135–155 ● Published online 10.1148/rg.281065183 ● Content Codes:
1From
the Department of Radiology, Division of Gastrointestinal Radiology, Massachusetts General Hospital, WHT 270, 55 Fruit St, Boston, MA
02114 (O.A.C., D.V.S., S.P.K., M.S.C., P.F.H.); Mallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, Mo
(J.J.B.); and the Department of Radiology, Northwestern University School of Medicine, Evanston, Ill (R.R.E.). Presented as an education exhibit at
the 2004 RSNA Annual Meeting. Received October 23, 2006; revision requested January 23, 2007; final revision received June 7; accepted June 11.
The authors discuss an investigational or unlabeled use of a commercial product, device, or pharmaceutical that has not been approved for such purpose by the FDA. D.V.S. is a researcher for GE Healthcare and a consultant with Bracco Diagnostics; S.P.K. received research grants from Johnson &
Johnson (Cordis) and Cook and is with the speakers’ bureau of Johnson & Johnson; J.J.B. is a consultant with Tyco Healthcare (Mallinckrodt), Bayer
Healthcare, and GE Healthcare and is with the speakers’ bureau of Bracco Diagnostics; and R.R.E. received research support from GE Healthcare and
Schering (Berlex); all remaining authors have no financial relationships to disclose. Address correspondence to D.V.S. (e-mail: [email protected]).
2Current
©
address: Department of Radiology, AO G Rummo, Benevento, Italy.
RSNA, 2008
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Figure 1. Two-dimensional versus three-dimensional (3D) MR cholangiopancreatography. (a) During
two-dimensional acquisition, a thick slab is imaged in an oblique plane. Two-dimensional heavily T2-weighted
MR cholangiopancreatogram shows fluid-filled structures, which may overlap because the imaging is performed in only one plane. The biliary and pancreatic ducts are well visualized. (b) Three-dimensional thinsection maximum-intensity-projection reformatted heavily T2-weighted MR cholangiopancreatogram shows
how it is possible to rotate and separate the structures with a 3D sequence.
Introduction
The gallbladder is a pear-shaped hollow viscus
located in the right upper quadrant, lodged on the
visceral surface of the liver between segments IV
and V, and connected to the hepatic duct through
the cystic duct to form the common bile duct.
The gallbladder is composed of the fundus, which
usually projects beyond the inferior border of the
liver; the body; and the neck. It is usually 7–10
cm long and 2.5 cm wide, and the wall measures
less than 3 mm in thickness (1). The gallbladder
serves as the repository for bile produced in the
liver, with an average volume of 30 –50 mL (2).
Bile within the gallbladder may become supersaturated with cholesterol, leading to crystal precipitation and subsequent gallstone formation.
Imaging of the gallbladder is typically requested for evaluation of right upper quadrant
pain in patients with or without fever and jaundice. Ultrasonography (US) is typically the initial
imaging modality. However, technologic advances in magnetic resonance (MR) imaging software, hardware, and contrast media (eg, phasedarray surface coils, breath-hold imaging, singleshot imaging techniques, hepatobiliary contrast
agents) allow MR imaging to be used as the initial
imaging modality for the evaluation of pain, jaundice, or masses or as a problem-solving tool for
gallbladder disease. Moreover, MR imaging
Figure 2. Three-dimensional MR cholangiopancreatogram shows the normal gallbladder. The cystic duct
appears as a curvilinear bright line connecting the gallbladder with the common hepatic duct (CHD). Pancreas divisum is incidentally noted.
allows functional assessment of the gallbladder
through the use of contrast agents excreted preferentially via the biliary system.
In this article, we review MR imaging techniques for the evaluation of the gallbladder and
the normal MR imaging appearance of this structure. In addition, we discuss and illustrate congenital abnormalities of the gallbladder and a variety of pathologic conditions affecting the gallbladder (cholelithiasis, acute and chronic
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Table 1
MR Imaging Protocol
Step
Description
Evaluation of gallbladder anatomy
MR cholecystography
Contrast-enhanced MR
cholecystography
Dynamic contrastenhanced study
Axial in-phase and opposed-phase breath-hold gradient-echo T1-weighted imaging
(TR msec/first TE msec/second TE msec ⫽ 150–200/4.2/1.8, flip angle ⫽ 80°, section thickness ⫽ 6–9 mm); axial and coronal breath-hold steady state fast SE T2weighted imaging (TR/TE ⫽ minimum/180, section thickness ⫽ 5 mm); axial respiratory-triggered fat-saturated T2-weighted imaging (TR/TE ⫽ 5000/80, echo train
length ⫽ 12, section thickness ⫽ 3 mm)
Oblique radial steady state fast SE T2-weighted imaging (14 sections) (TR/TE ⫽ minimum/500, section thickness ⫽ 40 mm); oblique right anterior steady state fast SE
T2-weighted imaging (TR/TE ⫽ minimum/160, section thickness ⫽ 5 mm); oblique
left anterior steady state fast SE T2-weighted imaging (TR/TE ⫽ minimum/160, section thickness ⫽ 5 mm); 3D fat-saturated MR cholangiopancreatography (TR/TE ⫽
4000/500–600, section thickness ⫽ 1.4 mm)
0.05–0.1 mL/kg (up to 20 mL) of gadolinium benzyloxyproprionictetraacetate
(BOPTA) (Multihance; Bracco, Milano, Italy) at 2 mL/sec or 0.5 ␮mol/kg of mangafodipir trisodium (MnDPDP) (Teslascan; Amersham Health, Princeton, NJ)
slowly administered over 1–2 min; axial and coronal 3D breath-hold interpolated
fat-suppressed spoiled gradient-echo T1-weighted imaging (TR/TE ⫽ 6.5/2.1, flip
angle ⫽ 15°, section thickness ⫽ 2.4 mm) 30–90 minutes after contrast material injection
0.1 mmol/kg (up to 40 mL) of gadolinium-based contrast material injected at 2 mL/sec
or 0.05–0.1 mL/kg (up to 20 mL) of gadolinium BOPTA injected at 2 mL/sec; axial
3D fat-suppressed spoiled gradient-echo imaging (TR/TE ⫽ 4.5/1.9, flip angle ⫽
12°, section thickness ⫽ 4–5 mm) to cover the entire liver (run prior to and 25 sec,
60–70 sec, and 120 sec after bolus administration)
TE ⫽ echo time, TR ⫽ repetition time.
cholecystitis, Mirizzi syndrome, xanthogranulomatous cholecystitis [XGC], adenomyomatosis,
carcinoma, lymphoma, endometrial implants).
We also discuss functional evaluation of the gallbladder in the acute setting, postoperative functional evaluation of the gallbladder and biliary
tree, and the assessment of angiogenesis as a possible future application.
Imaging Techniques
MR imaging sequences should be tailored to the
clinical question. T2-weighted sequences (usually
fast spin-echo [SE] sequences with respiratory
gating) are optimal for evaluating soft-tissue abnormalities involving the wall of the gallbladder,
the biliary system, and adjacent soft-tissue structures. The section thickness should be less than 5
mm, with a 1–2-mm gap between sections. Useful
additional T2-weighted sequences are similar to
those used to evaluate the biliary tree (MR
cholangiopancreatography) (Figs 1, 2): acquisition techniques such as half-Fourier rapid acquisition with relaxation enhancement and singleshot fast SE imaging. Although T1-weighted MR
imaging of the gallbladder can be performed with
either SE or breath-hold spoiled gradient-echo
techniques, the latter are superior because they
decrease respiratory artifacts.
Dynamic contrast material– enhanced fat-suppressed T1-weighted MR imaging sequences improve the delineation of the gallbladder wall, bile
ducts, and associated entities such as inflammation and neoplasms and allow assessment of the
liver parenchyma for tumor invasion and metastatic disease (Table 1).
Two agents, MnDPDP and gadolinium
BOPTA—the latter not yet having been approved
in the United States for evaluation of the gallbladder and biliary tree—are excreted into the bile.
After being injected intravenously, these agents
are specifically taken up by the hepatocytes and
subsequently excreted into the bile, resulting in
significant T1 shortening of the bile, which appears hyperintense on T1-weighted MR images.
This phenomenon permits evaluation of the
physiologic characteristics of the gallbladder and
biliary tree. This branch of MR cholangiography
is known as functional MR cholangiography
(2– 4).
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Figure 3. Gallbladder sludge in a 63-year-old man who underwent MR imaging for a left adrenal
mass. Coronal T2-weighted (a) and axial in-phase T1-weighted (b) MR images show an incidental finding of dependent material within the gallbladder lumen (arrow). The material is hypointense on the T2weighted image and hyperintense on the T1-weighted image.
Normal Appearance of the Gallbladder
The gallbladder should be imaged after the patient has fasted for 8 –12 hours, which promotes
physiologic distention of the gallbladder. On T2weighted images, the gallbladder wall has low
signal intensity and stands out against the bright
visceral fat. The wall adjacent to the liver cannot
be identified as a separate structure. On T1weighted images, the gallbladder wall has intermediate signal intensity and enhances uniformly
after the administration of gadolinium-based contrast material. The portion of the gallbladder wall
adjacent to the liver may not be well appreciated
owing to similar enhancement of the wall and the
liver parenchyma.
The insertion of the cystic duct into the hepatic duct can be demonstrated with routine T2weighted imaging and MR cholangiography.
Normal bile appears uniformly bright with T2weighted sequences. On T1-weighted images,
bile varies greatly in signal intensity depending on
its concentration.
During fasting, bile undergoes a process of
concentration. Water is reabsorbed and the concentration of cholesterol and bile salts increases,
leading to a shortened T1 relaxation time and,
consequently, to bright bile on T1-weighted images. A layering effect is sometimes observed,
with concentrated and denser bile in the dependent position.
Gallbladder sludge may have similar signal intensity characteristics, namely, iso- to mild hyperintensity on T2-weighted images and hyperintensity on T1-weighted images (Fig 3) (2– 4).
Congenital Abnormalities of the Gallbladder
There are many uncommon anomalies of the gallbladder and biliary tree that are delineated with
MR cholangiography. MR cholangiography is
useful in defining (a) the biliary anatomy for preoperative planning, and (b) anatomic variants
that may predispose to conditions such as Mirizzi
syndrome (discussed later).
Bilobed or duplicated gallbladder is a congenital abnormality that is well defined at MR imaging and MR cholangiography. This entity is rare,
having been seen in one of every 4000 adults in
an autopsy series (5), and may be associated with
right upper quadrant pain (Fig 4). Classifications
vary, with distinctions sometimes being made between bilobed gallbladder and true gallbladder
duplication. Bilobed or duplicated gallbladder has
been found to predispose to complications such
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Figure 4. Duplicated gallbladder in a 24-year-old woman with right upper quadrant discomfort and dyspepsia.
(a) Axial single-shot fast SE T2-weighted MR image shows two pear-shaped high-signal-intensity structures in the
gallbladder fossa (arrows). (b) On an axial in-phase gradient-echo T1-weighted MR image, the anterior structure
(arrow) has higher signal intensity than the posterior structure (arrowheads), probably due to increased bile concentration. (c) Coronal 3D maximum-intensity-projection reformatted T1-weighted MR cholecystogram acquired 60
minutes after MnDPDP administration demonstrates enhancement of the pear-shaped structures (arrows) and two
separate cystic ducts (arrowheads), findings that allowed the diagnosis of a double gallbladder.
as cholelithiasis and cholecystitis. Delineation of
the anatomy is important for preoperative planning and avoidance of biliary injury. Techniques
have recently been described for defining the
anatomy of the intra- and extrahepatic biliary tree
more precisely using MnDPDP-enhanced MR
cholangiography (6).
Pathologic Conditions
Affecting the Gallbladder
Cholelithiasis
Cholecystectomy is the most common elective
abdominal surgery in the United States and is
usually prompted by gallstones. Gallstones are
found in about 10% of the general population, are
twice as common in women as in men, and become more prevalent with increasing age.
Obesity, rapid weight loss, pregnancy, and estrogens are known risk factors. Gallbladder stones
are usually classified as cholesterol stones when
they are composed of at least 50% cholesterol
and as pigment stones when they contain lesser
amounts of cholesterol and higher percentages of
other constituents such as calcium bilirubinate
and glycoproteins. Cholesterol stones are by far
the more common, accounting for more than
80% of all gallstones in the United States.
Although most gallstones remain asymptomatic throughout life, some are responsible for
clinical symptoms, the most common being biliary colic. The risk of complications is 1% per
year. US is the most commonly used modality in
the evaluation of gallstone disease, with a high
specificity (⬎95%) and sensitivity (95%) for
stones larger than 2 mm (7,8).
It is important to be familiar with the MR imaging appearance of gallstones, since they are often detected incidentally. Gallstones are best appreciated at T2-weighted MR imaging and MR
cholangiopancreatography and appear as signal
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Figure 5. Cholelithiasis in a 45-year-old man with right upper quadrant pain. (a) Coronal T2weighted MR image reveals stones (arrows) appearing as hypointense material within the hyperintense
bile. (b) On a two-dimensional MR cholangiopancreatogram, the stones are not visible.
Table 2
Gallstone Composition and Signal Intensity
Type of Gallstone
Cholesterol
Pigment
T1 Signal Intensity
Percentage of Stones
Detected
Signal-Intensity Ratio
(Stone to Bile)
Hypointense
Hyperintense
100 (4/4)
90 (18/20)
0.24 ⫾ 0.10
3.36 ⫾ 1.88
voids on both T1- and T2-weighted images (Fig
5) (9). The presence of protein macromolecules
(which have shorter T1 relaxation times) within
gallstones may sometimes be responsible for the
central hyperintensity with a peripheral rim of
hypointensity seen on T1- or T2-weighted images, or for the predominant hyperintensity seen
on T1-weighted images (10,11). MR imaging can
also help distinguish between different types of
gallstones. Like cholesterol stones, pigment
stones typically appear hypointense with T2weighted sequences; unlike cholesterol stones,
they usually have increased signal intensity on
T1-weighted images. Pigment stones also show a
greater range of signal intensity, which in vitro
studies have shown to be related to the degree of
hydration. The composition of the stones may
affect management: Pigment stones may easily be
removed with endoscopic lithotripsy, whereas
cholesterol stones are much harder in consistency
and more difficult to treat endoscopically (Table
2) (12).
Acute Cholecystitis
Acute cholecystitis is by far the most common
acute complication of gallstone disease. The clinical presentation is characterized by right upper
quadrant tenderness, abdominal pain, fever, and
leukocytosis. In 90% of cases, the eliciting factor
is an impacted gallstone obstructing the cystic
duct. In the remaining cases, the condition occurs
in the absence of gallstones and is known as acute
acalculous cholecystitis, which is usually seen in
critically ill patients and carries higher morbidity
and mortality rates.
In the first few days after clinical onset, the
gallbladder appears distended at pathologic analysis, with the lumen filled with exudate and sometimes with pus. Bacteria may be cultured from
gallbladder bile. Bile salts are subsequently ab-
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Figures 6 – 8. (6) Gallbladder wall thickening in an 81-year-old man with hepatitis C virus–related cirrhosis and
hypoproteinemia but no intrinsic gallbladder disease. Axial single-shot fast SE T2-weighted MR image shows thickening and hyperintensity of the gallbladder wall (arrow) due to the patient’s hypoproteinemic state. Note the enlargement of the spleen. (7) Acute cholecystitis in a 77-year-old woman with a history of gallstones who presented with
fever, leukocytosis, and right upper quadrant pain. Fat-saturated respiratory-triggered fast SE T2-weighted MR image shows thickening, sloughing, irregularity, and edema of the gallbladder wall and surrounding liver tissue (arrow).
(8) Acute cholecystitis in a 58-year-old woman who presented with right upper quadrant pain radiating to the right
shoulder, along with fever, vomiting, and leukocytosis. Axial single-shot fast SE T2-weighted MR image shows gallstones (black arrow). The gallbladder wall is thickened and has increased signal intensity. Minimal pericholecystic
fluid is also present (white arrow).
sorbed, and clear mucoid fluid accumulates.
The gallbladder wall is edematous and thickened
(⬎3 mm). Necrosis and perforations may ensue
(8,13).
US is the usual modality of choice for the diagnosis of acute cholecystitis but may be significantly limited by large body habitus, with obesity
representing an increasingly serious issue in both
Europe and the United States. When US findings
are equivocal, MR imaging may be helpful in detecting stones in the gallbladder neck and cystic
duct and associated gallbladder wall abnormalities. On T2-weighted images, the gallbladder wall
may show increased signal intensity and thickening (⬎3 mm). This finding must be differentiated
from gallbladder wall thickening related to other
causes (eg, hypoproteinemic states) (Fig 6) (2– 4).
Pericholecystic fluid collections and edema of the
surrounding liver tissue may be found (Figs 7, 8).
Viral cholecystitis can have a similar appearance.
Periportal hyperintensity, although a nonspecific
finding, may be observed on T2-weighted images.
Although an inflammation-related increase in
bile protein content may result in variable signal
intensity of the bile on T1-weighted images, the
bile usually appears markedly hypointense with
T1-weighted sequences due to the impairment of
gallbladder concentrating capability, which is
typical of the acute inflammatory state.
Teaching
Point
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Figure 9. Acute cholecystitis with cholangitis in a 61-year-old woman who presented with right upper quadrant
pain, vomiting, nausea, fever, and leukocytosis. (a) Axial T1-weighted MR image shows diffuse gallbladder wall
thickening (arrows). (b) Coronal gadolinium-enhanced fat-suppressed T1-weighted MR image shows marked enhancement of the gallbladder walls, intra- and extrahepatic bile ducts, and surrounding liver tissue (arrows).
Contrast-enhanced fat-suppressed images
demonstrate increased enhancement of the gallbladder wall, adjacent fat, and surrounding liver
parenchyma (Fig 9). The “interrupted rim sign,”
which is characterized by patchy enhancement of
the gallbladder mucosa, represents areas of necrosis and is useful in identifying the gangrenous
form of acute cholecystitis at MR imaging (14 –
16). Gangrenous cholecystitis may be suggested
by asymmetric gallbladder wall thickening due to
intramural microabscesses, intramural hemorrhage, and complex pericholecystic fluid collections containing debris.
Emphysematous cholecystitis is caused by gasforming bacteria that infect the gallbladder wall
and produce intramural and intraluminal gas. It is
easily diagnosed with computed tomography
(CT), is usually acalculous, and can occur in diabetic patients or in cases of atherosclerosis of the
cystic artery with resulting ischemia.
Pericholecystic abscesses result from perforation of the gallbladder and appear on contrastenhanced images as localized fluid collections
with rim enhancement.
Transient enhancement of pericholecystic hepatic parenchyma on dynamic images obtained
immediately after the administration of gadolinium-based contrast material is a highly specific
sign found in 70% of patients with acute cholecystitis (7,8,17). This finding is due to a hyperemic response in the liver adjacent to the inflamed
gallbladder.
Functional evaluation of the gallbladder in
cases of suspected cystic duct obstruction has
long been the province of nuclear medicine and is
used in problem solving in patients with acute
cholecystitis. Functional MR cholangiography
serves as a combination of anatomic and physiologic assessment. Kim et al (18) compared conventional T2-weighted MR cholangiography with
MnDPDP-enhanced functional MR cholangiography in the evaluation of 12 patients with suspected acute cholecystitis. Hydroxyiminodiacetic
acid (HIDA) scans were also obtained to assess
for common bile duct obstruction. The authors
found excellent correlation between findings on
HIDA scans, findings on functional MR cholangiograms, and surgical findings. Furthermore, in
a study by Fayad et al (19), positive predictive
values of up to 100% for the diagnosis of acute
cholecystitis were described in patients examined
with functional MR cholangiography.
Chronic Cholecystitis
Chronic cholecystitis is the most common form of
clinically symptomatic gallbladder disease and is
almost invariably associated with gallstones (7).
The gallbladder appears small and contracted,
with irregular and thickened walls. Signs and
symptoms are vague and include abdominal distention, epigastric discomfort, and nausea (7).
After the administration of gadolinium-based
contrast material, the gallbladder wall enhances
less intensely than in acute cholecystitis. The enTeaching
hancement is usually smooth, slow, and proPoint
longed (Fig 10), unlike in gallbladder carcinoma,
in which it is usually irregular, early, and prolonged (3,4). However, the utility of conventional
MR cholangiography, functional MR cholangiography, and a combination of the two in the evalu-
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Figure 10. Chronic cholecystitis in a 47-year-old woman with right upper quadrant pain. On axial T1-weighted (a),
fat-saturated T2-weighted (b), and gadolinium-enhanced fat-saturated arterial phase (c) and portal venous phase (d)
MR images, the gallbladder wall is thickened and stratified without interruption or irregularity. The tunica muscularis appears hypointense on the T1-weighted image (arrow in a) and hyperintense on the T2-weighted image (arrow
in b) due to edema. The gallbladder wall enhances homogeneously and progressively from the arterial phase to the
portal venous phase. The tunica muscularis remains relatively poorly enhanced on the contrast-enhanced images (arrow in c and d).
ation of chronic cholecystitis has not been clearly
established; in the study mentioned earlier, Fayad
et al (19) found a 50% positive predictive value
for the detection of chronic cholecystitis for both
conventional and functional MR cholangiography.
Mirizzi Syndrome
Mirizzi syndrome is a rare complication of gallstone disease that is caused by an impacted stone
in the neck of the gallbladder or the cystic duct,
leading to extrinsic compression and subsequent
obstruction of the CHD (20). On rare occasions,
it occurs after cholecystectomy due to an impacted stone in the cystic duct remnant.
Mirizzi syndrome is usually classified as either
type 1 (simple obstruction of the CHD) or type 2
(erosion of the wall of the CHD resulting in cholecystocholedochal fistula).
The syndrome is associated with an increased
prevalence of bile duct injury when standard cholecystectomy is performed; therefore, preoperative recognition is of paramount importance (21).
Visualization of a gallstone at the junction of the
CHD and cystic duct with associated biliary ductal dilatation or gallbladder inflammation is diagnostic (22). MR cholangiopancreatography typically reveals an impacted gallstone in the cystic
duct or gallbladder neck associated with dilatation of the biliary tree, with the level of obstruction at the junction of the cystic duct and CHD.
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Figure 11. Mirizzi syndrome in a 42-year-old man who presented with right upper quadrant pain, fever, vomiting,
leukocytosis, and hyperbilirubinemia. US revealed gallstones and dilated intrahepatic biliary ducts. (a) Thick-slab
MR cholangiopancreatogram shows the dilated intrahepatic biliary ducts and the level of obstruction at the CHD
due to extrinsic compression (top arrow). Bottom arrow indicates the point at which the cystic duct joins the CHD.
(b) Axial single-shot fast SE T2-weighted MR image reveals stones within the gallbladder lumen and an impacted
stone in the cystic duct (arrow). (c) Axial contrast-enhanced fat-suppressed T1-weighted MR image shows diffuse
enhancement of the gallbladder and cystic duct due to associated inflammation (arrow).
The gallbladder wall is usually thickened. It
has a smooth contour and enhances after contrast
material administration (Fig 11).
Whereas US and CT can usually demonstrate
only the presence and level of biliary obstruction,
MR cholangiopancreatography can further characterize the nature of the obstruction, define the
burden of gallstones in the biliary tree, and help
evaluate the cystic duct obstruction. Moreover,
MR cholangiopancreatography can help detect
some anatomic variants that predispose to the
development of the syndrome, such as a low insertion of the cystic duct or a long parallel cystic
duct.
Contrast-enhanced MR imaging can demonstrate the inflammation of the gallbladder associated with Mirizzi syndrome (23,24).
Xanthogranulomatous Cholecystitis
XGC is an uncommon inflammatory disease of
the gallbladder that is characterized histologically
by a focal or diffuse destructive inflammatory process with xanthomalike foam cells, scarring, and
ceroid nodules.
At macroscopic analysis, the gallbladder appears nodular, with thickened and poorly defined
walls; gallstones are present in most cases. The
surrounding fat and liver may be infiltrated. The
process may extend to involve other nearby organs such as the colon and duodenum and may
be complicated by fistulous or abscess formation.
Lymphadenopathy and biliary obstruction may be
associated findings, and gallbladder cancer may
coexist.
XGC is thought to be induced by intramural
extravasation of bile from the Rokitansky-Aschoff
sinuses or from superficial mucosal ulcerations,
leading to an inflammatory response in which histiocytes predominate as they ingest the chemically
irritating cholesterol crystals (7,25,26).
The disease usually manifests as an acute episode of cholecystitis in women 60 –70 years of age
and tends to persist even for years (7).
At CT, XGC closely resembles gallbladder
carcinoma, with diffuse or focal gallbladder wall
thickening, heterogeneous wall enhancement, and
hypoattenuating intramural nodules.
Statistically significant CT findings that help
discriminate between gallbladder malignancy and
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Figure 12. XGC in a 63-year-old woman with right upper quadrant pain and abnormal liver function test results.
(a) US image shows echogenic stones and debris (arrowhead), diffuse gallbladder wall thickening, and masslike hypoechogenicity in the liver (arrow). (b) Contrast-enhanced abdominal CT scan demonstrates gallbladder wall thickening with heterogeneous enhancement. Note the continuous enhancement of the gallbladder mucosa (arrows) and
the diffuse character of the wall thickening. (c) Axial fat-saturated respiratory-triggered fast SE T2-weighted MR image shows diffuse thickening with a fundal mass and unbroken mucosal hyperintensity. There is focal high T2 signal
intensity within the wall of the gallbladder (arrow), a finding that is consistent with an intramural collection. (d) Gadolinium-enhanced T1-weighted MR image shows diffuse wall thickening with a mass at the fundus (arrow) and continuous enhancement of the gallbladder mucosa. (e) Photograph of the gross pathologic specimen of the gallbladder
obtained at cholecystectomy shows diffuse thickening of the wall, intramural xanthogranulomas, and intraluminal
stones.
XGC include (a) low-attenuation intramural
nodules occupying more than 60% of the thickened wall area and corresponding to the xanthogranulomas, and (b) continuous linear en-
hancement of the mucosa. In one series, although
diffuse gallbladder wall thickening was observed
in 91% of cases of XGC, it was also seen in 41%
of cases of gallbladder carcinoma (27); thus, wall
thickening alone is a sign with only limited utility
(27,28).
MR imaging demonstrates intramural lesions
with markedly elevated T2 signal intensity that
correspond to the low-attenuation intramural
nodules seen at CT. Preservation of linear mucosal enhancement at MR imaging is suggestive of
XGC rather than carcinoma (Fig 12) (29).
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Figures 13, 14. (13) Adenomyomatosis in a 51-year-old man. (a) Contrast-enhanced CT scan demonstrates focal
fundal gallbladder wall thickening (arrow) with only minimal enhancement. (b) T2-weighted MR image shows wall
thickening (arrow) and increased mural signal intensity. (c) Contrast-enhanced T1-weighted MR image also shows
only minimal enhancement (arrow). (14) Adenomyomatosis in a 53-year-old man. MR imaging of the liver was
performed to evaluate thickening of the gallbladder fundus that was seen at US performed at another institution.
(a, b) Axial (a) and coronal (b) T2-weighted MR images show focal thickening of the gallbladder wall in the fundus
(arrow in a), with small hyperintense foci (string of beads sign) representing dilated Rokitansky-Aschoff sinuses (arrow in b). (c) Axial gadolinium-enhanced portal venous phase T1-weighted MR image shows enhancement of the
gallbladder wall (arrow).
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Adenomyomatosis of the Gallbladder
Adenomyomatosis of the gallbladder is a common, distinct, noninflammatory benign condition
that has been reported in up to 8.7% of cholecystectomy specimens. It is more frequently seen in
women than in men, usually manifests with persistent right upper quadrant pain, and is usually
associated with gallstones (90% of cases). Adenomyomatosis is characterized by excessive proliferation of surface epithelium with deep and
branching invaginations (Rokitansky-Aschoff sinuses) into the thickened tunica muscularis or
beyond (26,30,31). The Rokitansky-Aschoff sinuses can be found in about 90% of gallbladder
specimens; if they are deep, branching, and accompanied by hyperplasia of the muscular layer,
adenomyomatosis can be diagnosed (30). At
gross examination, adenomyomatosis of the gallbladder may manifest as diffuse, segmental, or
focal disease. Diffuse adenomyomatosis manifests
as diffuse mural thickening and luminal narrowing. In the segmental form, there is focal circumferential thickening in the midportion (“waist”) of
the gallbladder, producing an “hourglass” appearance (32).
The localized form of adenomyomatosis manifests as a focal, frequently semilunar or crescentic
solid mass, usually in the fundus of the gallbladder (Figs 13, 14) (26).
Dysplastic changes and even carcinoma may
arise from adenomyomatous epithelium, especially in patients with segmental type adenomyomatosis, but this phenomenon seems to be related
to the presence of gallstones and chronic inflammation (26,33).
MR imaging demonstrates the mural thickening and multiple intramural cystic components
(Rokitansky-Aschoff sinuses) (34).
Adenomyomatosis can appear almost identical
to a mass and may be difficult to distinguish from
gallbladder malignancy. On contrast-enhanced
images, the diffuse type shows early mucosal and
subsequent serosal enhancement.
The “string of beads sign,” the hallmark of adenomyomatosis at MR imaging, refers to highTeaching
signal-intensity foci in the gallbladder wall on T2Point
weighted images, findings that correspond to bilefilled Rokitansky-Aschoff sinuses. This sign is
highly specific (92%) in diagnosing gallbladder
adenomyomatosis versus gallbladder cancer.
Catalano et al 147
The sign may be absent in cases of small (⬍3-mm)
sinuses or sinuses filled with inspissated proteinaceous bile or small calculi; therefore, its sensitivity is only 62%. In approximately 70% of
patients, the contrast enhancement pattern of
adenomyomatosis is indistinguishable from that
of gallbladder cancer (31,33).
Gallbladder Carcinoma
Gallbladder cancer is the fifth most common gastrointestinal carcinoma and the most common
carcinoma of the biliary tree, with an incidence of
2.5 new cases per 100,000 population per year. It
is usually advanced at presentation, having spread
to the lymph nodes and invaded the surrounding
structures, mainly the liver; furthermore, it has a
poor outcome, with a median patient survival
time of 3 months and a 5-year survival rate of 5%
(35). Gallbladder cancer most often occurs in the
elderly and in women and is usually associated
with gallstones (90% of cases). Other risk factors
include a chronic typhoid carrier state, a long
common pancreatic-biliary channel, and porcelain gallbladder. About 20% of patients with porcelain gallbladder develop gallbladder cancer
(36). It has been postulated that the most important risk factor is the presence of chronic gallbladder inflammation, usually related to stones (35).
The initial presenting signs and symptoms are
vague and nonspecific; they include abdominal
pain (mainly in the right upper quadrant), weight
loss, and fever. Jaundice develops when the carcinoma involves and obstructs the common bile
duct, right hepatic duct, or CHD (36,37). Carcinoembryogenic antigen values higher than 4
ng/mL in the appropriate clinical setting are 93%
specific but only 50% sensitive for the diagnosis
of gallbladder cancer (35). At histologic analysis,
about 90% of gallbladder carcinomas are adenocarcinomas; other causes, such as small cell carcinomas and squamous cell carcinomas, are rare
(36,37).
Gallbladder cancer usually arises in the fundus
or neck, but its rapid spread may obscure the site
of origin (38). It progresses from epithelial dysplasia to carcinoma in situ to invasive carcinoma
(35). Because of the thinness of the muscular
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Figure 15. Gallbladder cancer in a 73-year-old
woman who presented with abdominal pain, hyperbilirubinemia, and weight loss. On an axial fat-saturated
T2-weighted MR image (a) and axial (b) and coronal (c) gadolinium-enhanced T1-weighted MR images,
the gallbladder wall is heterogeneously thickened (thick
arrow in a, arrow in b and c). The mucosa and submucosa cannot be clearly distinguished along the entire
gallbladder wall. Stones are present within the gallbladder lumen (thin arrows in a). In contrast, chronic cholecystitis manifests as smooth, well-defined enhancement
of the gallbladder wall with preservation of the submucosa (cf Fig 10).
layer and the continuity of the connective tissue
of the gallbladder wall with the interlobular connective tissue of the liver, gallbladder carcinoma
can easily invade the liver and gain access to the
lymphatic and vascular channels. Once it has penetrated the serosa, it can also spread to the peritoneal cavity. According to the American Joint
Committee on Cancer (AJCC)–Union Internationale Contre le Cancer (UICC) TNM classification system, gall bladder carcinoma is considered
to be T1 when confined within the muscular
layer, T2 when it extends beyond the muscular
layer into the perimuscular connective tissue, T3
when liver invasion of less than 2 cm has occurred, and T4 when the extent of liver involvement exceeds 2 cm. Although lymphatic drainage
may not follow a predictable pattern, it usually
involves the cystic and pericholedochal nodes initially (N1) but subsequently extends into the posterior pancreaticoduodenal, retroportal, and celiac nodes (N2). Involvement of intercaval nodes
occurs later and is classified as M1 (35).
At macroscopic examination, gallbladder cancer typically manifests as either (a) focal or diffuse mural thickening; (b) an intraluminal polypoid mass; or (c) a soft-tissue mass replacing the
gallbladder, with invasion of the liver. Gallbladder carcinomas most often manifest as diffusely
infiltrating lesions extending into the liver (⬃68%
of cases) and less often manifest as intraluminal
polypoid masses or mural thickening (37).
New and potentially curative surgical therapies
have been introduced that allow a 5-year survival
rate of more than 50%. These therapies include
resection of the gallbladder, resection of segments
IVb and V of the liver, and even extended right
hepatectomy and regional lymphadenectomy.
They necessitate an accurate preoperative radiologic assessment of tumor extension and a preoperative vascular “road map” (35,39,40).
Focal or diffuse mural thickening of more than
1 cm as well as asymmetric thickening are highly
suggestive of the diagnosis (41,42). On T2-
Teaching
Point
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Catalano et al 149
Figure 16. Sludge mimicking neoplasm. (a, b) On axial fat-saturated T2-weighted (a) and gadolinium-enhanced
T1-weighted baseline (b) MR images, the gallbladder lumen appears to be filled by a mass that is hypointense on the
T2-weighted image (arrow in a) and hyperintense on the T1-weighted image (arrow in b). The gallbladder wall is of
normal thickness on the baseline image. (c, d) On axial fat-saturated T2-weighted (c) and gadolinium-enhanced T1weighted (d) MR images obtained 2 months later, the “mass” has disappeared, indicating that the finding in a and b
represented sludge. Irregular thickening of the gallbladder wall due to inflammation is also seen (arrow).
weighted images, the tumor is usually heterogeneously hyperintense relative to the liver, whereas
on T1-weighted images it is relatively iso- or hypointense. All gallbladder cancers show enhancement after the administration of gadoliniumbased contrast material. In the early phase of
dynamic contrast-enhanced imaging, the outer
margin of enhancement is irregular, whereas it
appears smooth in chronic cholecystitis. The late
phases of enhancement are less useful because of
the spread of enhancement toward the outer wall
in both chronic cholecystitis and gallbladder car-
cinoma (39,43). However, these characteristics
may overlap, and it may be difficult to differentiate benign mural thickening from gallbladder carcinoma (Figs 15, 16).
In 25% of patients, gallbladder carcinoma
manifests as an intraluminal polypoid mass, usually well differentiated and confined to the muscular layer with a better prognosis (9,44). On T1weighted images, the polypoid form is seen as an
intermediate-signal-intensity mass protruding
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Figure 17. Gallbladder carcinoma in a 73-year-old
woman who presented with right upper quadrant pain,
weight loss, and hyperbilirubinemia. (a) Axial fat-suppressed T1-weighted MR image shows irregular gallbladder wall thickening with a focal mass at the fundus
(arrows). The mass exhibits the intermediate signal intensity typically seen on T1-weighted images. (b) On an
axial fat-suppressed T2-weighted MR image, the mass
is heterogeneously hyperintense (arrows). (c) Contrastenhanced T1-weighted MR image shows the mass with
variable enhancement. The tumor-liver interface is ill
defined (arrow), a finding that suggests tumor infiltration of the liver.
into the lumen and arising from the wall of the
gallbladder, which may be thickened. On T2weighted images, the mass exhibits increased signal intensity. Necrosis and calcification are rare in
this type of tumor (9,45,46). Polypoid lesions
enhance moderately and homogeneously on gadolinium-enhanced images. Malignant polypoid
lesions are usually larger than 1 cm and demonTeaching strate early and prolonged enhancement; in conPoint
trast, benign lesions demonstrate early enhancement with subsequent washout (9,47).
Gallbladder carcinoma most commonly manifests as a large solid mass in the gallbladder fossa
obscuring the gallbladder, with extension into the
liver or adjacent organs (Figs 17, 18). Nonvisualization of the gallbladder and the presence of gallstones within the mass are helpful in making the
diagnosis. The mass demonstrates intermediate
signal intensity on T1-weighted images and heterogeneously hyperintense signal intensity on T2weighted images. Enhancement is early and prolonged after gadolinium-based contrast material
administration (Fig 17) (47). Gadolinium-en-
hanced fat-suppressed T1-weighted images are
useful in diagnosing tumor extent, direct invasion
of surrounding organs, liver metastases, and involvement of critical vascular structures such as
the portal vein and hepatic artery (9,39,48). MR
imaging has a high sensitivity for the detection of
direct hepatic invasion (100%), although it may
lead to underestimation of the depth of invasion
in 11% of patients. Its sensitivity for the detection
of lymphadenopathy is also high (nearly 92%).
MR cholangiopancreatography facilitates identification of the site of biliary obstruction, which may
be caused by duct compression by the tumor or
by lymphadenopathy or induced by duct invasion.
MR imaging has a sensitivity of 92% in detecting
biliary dilatation but is less efficient (sensitivity of
69%) in detecting bile duct invasion. Microscopic
invasion should be suspected in cases of tumor
contiguity with a duct, even if a biliary obstruction cannot be visualized. Small peritoneal implants may be better appreciated on delayed gadolinium-enhanced fat-suppressed T1-weighted
images (9,39).
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Figure 18. Lymphoma of the gallbladder in a 37-year-old man who presented with weight loss and vague abdominal pain. (a, b) Contrast-enhanced fat-suppressed arterial phase (a) and portal venous phase (b) T1-weighted MR
images demonstrate irregular thickening of the gallbladder wall in the fundus, with an associated soft-tissue mass (arrows in a, black arrows in b) infiltrating the liver. A focal lesion in the liver, one of several deposits of lymphoma, is
also seen (white arrow in b). A single retroperitoneal lymph node is evident (arrowhead in b). (c) MR image obtained
at a higher level demonstrates biliary ductal dilatation (black arrows) and additional parenchymal lesions (white arrows). (d) MR cholangiopancreatogram demonstrates an irregularly contoured gallbladder with biliary ductal dilatation. Arrow indicates an obstruction; arrowheads indicate a biliary stent.
Lymphoma of the Gallbladder
Lymphoma of the gallbladder is rare and may
represent primary non-Hodgkin lymphoma from
mucosa-associated lymphoid tissue or may be
secondary to systemic disease (49,50). Primary
lymphoma is extremely rare, having been reported in only about 20 cases. At MR imaging, it
is difficult to differentiate between primary gallbladder cancer and gallbladder lymphoma. MR
imaging findings include thickening of the gallbladder wall; a mass in the gallbladder fossa with
extension into the liver, with the mass being hypointense on T1-weighted images and hyperintense on T2-weighted images relative to the liver;
biliary obstruction; and lymph nodes in the porta
hepatis (Fig 18). Tumor extension into the liver
may mimic adenomyomatosis at US, but MR
cholangiopancreatograms will not show the string
of beads sign, a sign that is typical of adenomyomatosis and allows its identification (51).
Endometrial Implants on the Gallbladder
Rarely, endometrial implants may occur on the
surface of the gallbladder. Contrast-enhanced
T1- and T2-weighted MR images will demonstrate the presence of blood products with variable enhancement (Fig 19).
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Figure 19. Endometrial implant on the surface of the gallbladder in a 35-year-old woman with right upper quadrant pain. Liver function tests showed no abnormalities. US disclosed a mass in hepatic segment IV. (a) Axial fatsuppressed T1-weighted MR image shows a hyperintense mass (arrow) on the medial surface of the gallbladder.
(b) On an axial T2-weighted MR image, the mass is hypointense (arrow), a finding that suggests the presence of subacute blood.
Functional Evaluation
of the Gallbladder in Patients with Acute Symptoms
MR cholangiography can be used to evaluate gallbladder function in terms of volume and ejection
fraction following ingestion of a fatty meal or the
infusion of cholecystokinin. The gallbladder ejection fraction following the infusion of cholecystokinin has been found to correlate with that measured at hepatobiliary scintigraphy performed
with HIDA. It is possible to assess the patency
and range of contractions of that portion of the
bile duct covered by the sphincter of Oddi with
pharmacodynamic MR cholangiopancreatography after the ingestion of a fatty meal or the infusion of secretin (52).
Contrast-enhanced MR cholangiography with
MnDPDP or gadolinium BOPTA can be used to
assess gallbladder function as well as biliary obstruction (Fig 20) (53).
For MnDPDP-enhanced MR cholangiography, 0.5 mL/kg of MnDPDP up to a maximum of
35–50 mL is slowly injected intravenously for 1–2
minutes, followed by a 10-mL saline flush. The
patient is scanned 15–30 minutes after injection
to obtain MnDPDP-enhanced T1-weighted MR
cholangiopancreatograms.
For MR cholangiography with gadolinium
BOPTA, 0.05 mmol (0.1 mL)/kg of gadolinium
BOPTA up to a maximum of 15 mL is administered intravenously with a power injector at a rate
of 2 mL/sec, followed by a 20-mL saline flush.
During intravenous administration, dynamic vascular images are acquired with the same scanning
delay and parameters that are used with any nonhepatospecific extracellular gadolinium chelate.
At 30 – 60 minutes after injection, the patient is
rescanned to take advantage of the biliary excretion and to obtain gadolinium-enhanced T1weighted MR cholangiopancreatograms.
Normally, contrast-enhanced bile will appear
bright in both the gallbladder lumen and the bile
ducts on delayed T1-weighted images. In our experience, contrast-enhanced bile will not accumulate in the gallbladder lumen in cases of compromised gallbladder function or cystic duct obstruction.
Postoperative Functional Evaluation of the
Gallbladder and Biliary Tree
The presence of air in the biliary system is common following endoscopic retrograde cholangiopancreatography, endoscopic papillotomy, and
the creation of biliary-enteric anastomoses. Because the air is nondependent within both the
gallbladder and the biliary tree, it is seen as a nondependent signal void–fluid level on T2-weighted
images.
MR imaging may be useful in identifying noncalcified dropped gallstones, since CT may fail to
depict them. With T2-weighted sequences, these
stones appear as focal well-defined signal voids,
whereas with T1-weighted sequences their signal
intensity is variable. The surrounding inflammatory tissue is hyperintense on T2-weighted images
and shows variable enhancement after the administration of gadolinium-based contrast material. If
an abscess has developed, it appears as a relatively
well-defined fluid collection with rim enhancement.
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Catalano et al 153
Figure 20. Preoperative MnDPDP-enhanced MR cholangiographic evaluation for living donor liver transplantation. (a) Axial fat-suppressed T1-weighted MR image shows the gallbladder and cystic duct containing bright bile
(arrow), a finding caused by the excretion of contrast material into the bile. The heterogeneous signal intensity within
the gallbladder is due to incomplete mixing of the contrast material and bile. (b) Maximum-intensity-projection image of the gallbladder and liver demonstrates the normal intra- and extrahepatic bile ducts and gallbladder.
MR cholangiopancreatography, especially with
MnDPDP, is useful in identifying postoperative
biliary leaks, biliary strictures, and cystic duct
leaks (54).
Contrast-enhanced T1-weighted MR cholangiography with intravenous hepatobiliary contrast
agents, either in combination with conventional
MR cholangiography or as a single delayed contrast-enhanced study, can help differentiate biliary-enteric anastomotic strictures from functional
obstruction and help identify postoperative leaks
(55–57).
In a series of 13 patients with hepaticojejunostomies, Hottat et al (58) compared the accuracy
of MnDPDP-enhanced functional MR cholangiography with that of conventional T2-weighted
MR cholangiography in assessing anastomotic
stricture. Although seven patients had dilated intrahepatic bile ducts at T2-weighted MR cholangiography, only two were found to have delayed
excretion of MnDPDP at T1-weighted imaging.
These two patients were also the only ones in
whom percutaneous transhepatic cholangiography showed strictures requiring dilation (58). The
tendency of conventional T2-weighted MR
cholangiography to lead to overestimation of
strictures in cases of biliary ductal dilatation has
been documented previously (59). Although
these findings are preliminary, they dovetail with
current imaging concepts, and functional MR
cholangiography would appear to afford an opportunity to streamline imaging protocols.
Future Applications:
Assessment of Angiogenesis
Unresectable gallbladder cancer has traditionally
had an extremely poor prognosis due to the lack
of success with traditional chemotherapeutic
treatment. Novel treatment methods with the socalled angiogenesis inhibitors are being devised
that target the vascular supply of the tumor.
These agents may be used alone or in combination with conventional therapies. The initial
changes resulting from such treatment methods
may not be visualized at routine imaging. Dynamic contrast-enhanced MR imaging can play a
role in assessing tumor angiogenesis, thereby allowing the monitoring of antiangiogenic effects
(60,61).
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This article meets the criteria for 1.0 credit hour in category 1 of the AMA Physician’s Recognition Award. To obtain
credit, see accompanying test at http://www.rsna.org/education/rg_cme.html.
RG
Volume 28 • Volume 1 • January-February 2008
Catalano et al
MR Imaging of the Gallbladder: A Pictorial Essay
Onofrio A. Catalano, MD, et al
RadioGraphics 2008; 28:135–155 ● Published online 10.1148/rg.281065183 ● Content Codes:
Page 141
On T2-weighted images, the gallbladder wall may show increased signal intensity and thickening
(more than 3 mm). This finding must be differentiated from gallbladder wall thickening related to
other causes (eg, hypoproteinemic states) (Fig 6) (2–4).
Page 142
The enhancement is usually smooth, slow, and prolonged (Fig 10), unlike in gallbladder carcinoma,
in which it is usually irregular, early, and prolonged (3,4).
Page 147
The "string of beads sign," the hallmark of adenomyomatosis at MR imaging, refers to high-signalintensity foci in the gallbladder wall on T2-weighted images, findings that correspond to bile-filled
Rokitansky-Aschoff sinuses. This sign is highly specific (92%) in diagnosing gallbladder
adenomyomatosis versus gallbladder cancer.
Page 148
Gallbladder carcinomas most often manifest as diffusely infiltrating lesions extending into the liver
(~68% of cases) and less often manifest as intraluminal polypoid masses or mural thickening (37).
Page 150
Malignant polypoid lesions are usually larger than 1 cm and demonstrate early and prolonged
enhancement; in contrast, benign lesions demonstrate early enhancement with subsequent washout
(9,47).