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(Radiology. 1999;211:723-726.)
© RSNA, 1999

Gastrointestinal Imaging

Expanded Gallbladder Fossa: Simple MR Imaging Sign of Cirrhosis1

Katsuyoshi Ito, MD, Donald G. Mitchell, MD, Toshifumi Gabata, MD and Shahid M. Hussain, MD

1 From the Department of Radiology, Thomas Jefferson University Hospital, 132 S 10th St, 1096 Main Bldg, Philadelphia, PA 19107 (K.I., D.G.M., T.G., S.M.H.); the Department of Radiology, Yamaguchi University School of Medicine, Yamaguchi, Japan (K.I.); the Department of Radiology, Kanazawa University School of Medicine, Kanazawa, Japan (T.G.). Received July 31, 1998; revision requested August 28; revision received October 13; accepted November 19. Address reprint requests to D.G.M.


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To determine the frequency on magnetic resonance (MR) images of a widened pericholecystic space, which the authors call the expanded gallbladder fossa sign, and to assess the sensitivity and specificity of this sign for cirrhosis.

MATERIALS AND METHODS: Three-hundred thirteen patients who underwent MR imaging were included in this study, including 190 with pathologically proved cirrhosis (cirrhosis patients) and 123 without history of chronic liver diseases (control subjects). MR images were qualitatively evaluated by three independent observers for the presence of the expanded gallbladder fossa sign. This sign was considered present if there was enlargement of the pericholecystic space (ie, gallbladder fossa) and the space was bounded laterally by the edge of the right hepatic lobe and medially by the edge of the left lateral segment, in conjunction with nonvisualization of the left medial segment.

RESULTS: The expanded gallbladder fossa sign was seen in 129 cirrhosis patients and in three control subjects (P < .001). The sensitivity, specificity, accuracy, and positive predictive value of this sign for the MR diagnosis of cirrhosis were 68%, 98%, 80%, and 98%, respectively.

CONCLUSION: The expanded gallbladder fossa sign on MR images is a frequently present, specific indicator of cirrhosis. This sign can be used as a simple and highly specific sign of cirrhosis, if present, despite the overall sensitivity of 68%.

Index terms: Liver, cirrhosis, 761.794 • Liver, MR, 761.121411, 761.121412, 761.121415, 761.12143


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Ultrasonography (US), computed tomography (CT), and magnetic resonance (MR) imaging have become important tools for evaluating the cirrhotic liver. In previous studies, several imaging findings suggestive of cirrhosis have been described (1–6). Morphologic changes of the liver in cirrhosis include enlargement of the caudate lobe and the lateral segment of the left hepatic lobe and atrophy of the right hepatic lobe (mainly, the anterior segment). The diagnostic value of measurements of the hepatic diameter have been indicated in some reports, including the ratio of transverse caudate lobe width to right lobe width (7,8), multidimensional caudate lobe indexes (9) at US and CT, and volume analysis of each liver segment on the basis of the cross-sectional area at CT or MR imaging (10,11). Recently, Lafortune et al (12) reported that a decreased diameter of the medial segment of the left hepatic lobe is a helpful adjunct finding of cirrhosis in the US investigation. However, these measurements and calculations require additional time for data analysis and are rarely used in daily reading sessions.

At MR imaging for the evaluation of the liver, we noted that the pericholecystic space (gallbladder fossa) was frequently enlarged in patients with cirrhosis. We call this appearance the expanded gallbladder fossa sign. A simple visual MR finding to diagnose cirrhosis would be helpful in clinical MR practice. The purpose of this study was to determine the frequency of the finding of the expanded gallbladder fossa sign on MR images and to assess its sensitivity and specificity as a simple diagnostic MR imaging sign of cirrhosis.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Patient Population
From June 1994 through December 1997 at our institutions, liver MR records and clinical MR requests were searched to identify patients with cirrhosis and patients without chronic liver diseases. Then these cases were cross-referenced to the pathologic records to select patients with pathologically proved cirrhosis. Because these two factors can affect the morphologic changes of the liver, patients were excluded from this study (a) if they had a history of cholecystectomy or hepatic resection or (b) if malignant tumors larger than 2 cm in diameter were present. Consequently, this study population included a total of 313 patients (181 men and 132 women; age range, 22–87 years; mean age, 52.7 years), 190 with pathologically proved cirrhosis (cirrhosis patients [116 men and 74 women; age range, 22–87 years; mean age, 52.4 years]) and 123 with no clinical evidence of chronic liver diseases (control group [65 men and 58 women; age range, 22–81 years; mean age, 53.3 years]). Control subjects had undergone MR imaging for reasons other than chronic liver diseases (eg, suspected liver cyst or hemangioma, benign disease of other organs). Cirrhosis patients had been referred for MR imaging to evaluate the severity of cirrhosis and portal hypertension, to acquire preoperative studies before liver transplantation, or to screen or further examine liver lesions that were suspected with other imaging modalities. Cirrhosis was caused by viral infection (hepatitis B [n = 30], C [n = 76], or B and C [n = 10]), alcohol abuse (n = 19), primary biliary cirrhosis (n = 8), or {alpha}1-antitripsin deficiency (n = 3), or the origin was cryptogenic (n = 12) or undetermined due to insufficient clinical data (n = 32). Pathologic confirmation of cirrhosis was made by means of percutaneous liver biopsy in 149 patients, liver transplantation in 18, transjugular liver biopsy in 19, and autopsy in four.

MR Imaging Technique
All patients underwent MR imaging at 1.5 T (Signa, GE Medical Systems, Milwaukee, Wis; Magnetom H-15 or Vision, Siemens, Erlangen, Germany). All patients underwent axial T1- and T2-weighted MR imaging. T1-weighted imaging included one or more of the following sequences: conventional spin echo (repetition time msec/echo time msec = 400–600/11–22), in-phase gradient echo (80–210/4.0–4.8 or 9.0 with 70°–90° flip angle), and opposed-phase gradient echo (80–210/1.6–2.7 or 6.0–7.0 with 60°–90° flip angle). T2-weighted imaging included the following sequences: conventional spin echo (1,500–3,000/50–100), breathing-averaged fast spin echo (3,000–7,500/91–104 [effective]) with or without fat suppression, and breath-hold fast spin echo (2,500–4,200/70–138 [effective]). Most patients also underwent T1-weighted opposed-phase gradient-echo imaging with multiphasic dynamic techniques after intravenous injection of 0.1 mmol per kilogram of body weight gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ, or Japan-Schering, Osaka, Japan). Other imaging parameters included 256 x 128–256 imaging matrix, usually with use of a rectangular field of view to reduce the number of phase-encoding views, and 7–12-mm-thick sections with 2-mm or less section gap.

Imaging Interpretation
MR images were reviewed retrospectively and independently by three of four radiologists (K.I., D.G.M., T.G., S.M.H.) experienced in abdominal MR imaging. The reviewers were blinded to the final diagnosis with regard to the presence of cirrhosis, and they evaluated the images qualitatively for the presence of the expanded gallbladder fossa sign. Cases of the cirrhosis patients and control subjects were randomly mixed. When the reviewers disagreed about the presence of the expanded gallbladder fossa sign, a majority opinion was used as the final decision for data analysis. The expanded gallbladder fossa sign was considered present if there was enlargement of the pericholecystic space (ie, gallbladder fossa) and the space was bounded laterally by the edge of the right hepatic lobe, medially by the edge of the lateral segment of the left hepatic lobe, and, occasionally, posteriorly by the anterior edge of the caudate lobe. These findings were seen in conjunction with nonvisualization of the medial segment of the left hepatic lobe on the same axial image (Figs 1–3). With the expanded gallbladder fossa sign, the gallbladder fossa was filled with increased fat tissue, bowel, and sometimes collateral vessels. The expanded gallbladder fossa sign was not considered to be present in cases in which the gallbladder (or gallbladder fossa) was covered by the medial segment of the left hepatic lobe even though the amount of fat tissue increased between the gallbladder and the left lateral segment (Fig 4).



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  		Figure 1a. Normal liver without the expanded gallbladder fossa sign in a 57-year-old man. (a) Axial contrast material–enhanced T1-weighted gradient-echo image (130/1.6 with 90° flip angle) with fat suppression demonstrates normal liver without morphologic changes of cirrhosis. Gallbladder (arrow) is located in a fossa between the right hepatic lobe and the medial segment of the left hepatic lobe. (b) On the axial contrast-enhanced T1-weighted gradient-echo image (130/1.6 with 90° flip angle) with fat suppression obtained 3 cm below a, the gallbladder (arrowhead) is still covered by the medial segment (arrow) of the left hepatic lobe. At this level, the left lateral segment is no longer seen.

 


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  		Figure 1b. Normal liver without the expanded gallbladder fossa sign in a 57-year-old man. (a) Axial contrast material–enhanced T1-weighted gradient-echo image (130/1.6 with 90° flip angle) with fat suppression demonstrates normal liver without morphologic changes of cirrhosis. Gallbladder (arrow) is located in a fossa between the right hepatic lobe and the medial segment of the left hepatic lobe. (b) On the axial contrast-enhanced T1-weighted gradient-echo image (130/1.6 with 90° flip angle) with fat suppression obtained 3 cm below a, the gallbladder (arrowhead) is still covered by the medial segment (arrow) of the left hepatic lobe. At this level, the left lateral segment is no longer seen.

 


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  		Figure 2. Cirrhosis with the expanded gallbladder fossa sign in a 71-year-old man. Axial T1-weighted conventional spin-echo image (600/15) shows the enlarged pericholecystic space (gallbladder fossa) filled with increased fat tissue, demonstrating the expanded gallbladder fossa sign (black arrow). Note slight enlargement of the caudate lobe (white arrowhead) and of the left lateral segment (black arrowhead) and atrophy of the right hepatic lobe (nearly complete atrophy of the anterior segment) (white arrow). The left medial segment is not seen at this level because of its atrophic change.

 


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  		Figure 3. Cirrhosis with the expanded gallbladder fossa sign in a 62-year-old man. Axial contrast-enhanced T1-weighted gradient-echo image (120/2.2 with 90° flip angle) with fat suppression demonstrates enlargement of the gallbladder fossa (white arrow) and intrusion of collateral vessels (black arrow) into this space, demonstrating the expanded gallbladder fossa sign. Note enlargement of the left lateral segment (black arrowhead) and of the caudate lobe (white arrowhead). The gallbladder is not seen at this level.

 


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  		Figure 4. Normal liver mimicking the expanded gallbladder fossa sign in a 49-year-old woman. Axial contrast-enhanced T1-weighted gradient-echo image (120/2.3 with 90° flip angle) with fat suppression shows the enlarged pericholecystic space (long arrow) between the gallbladder and the left lateral segment (short arrow), resembling the expanded gallbladder fossa sign. In this case, however, the expanded gallbladder fossa sign was not considered to be present because the gallbladder (*) was covered by the left medial segment (arrowhead).

 
Statistical Analysis
The {kappa} statistic was used to assess interobserver variability in the MR readings (13). The level of agreement was defined as follows: {kappa} < 0, no agreement; {kappa} = 0.00–0.40, poor agreement; {kappa} = 0.41–0.75, good agreement; and {kappa} = 0.76–1.00, excellent agreement. The frequency of the expanded gallbladder fossa sign in the cirrhosis patients was compared with that in the control subjects by means of the {chi}2 test. A P value of less than .05 was considered to indicate a statistically significant difference. The sensitivity, specificity, and accuracy of this sign for the MR imaging diagnosis of cirrhosis were also calculated.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
In the analysis of interobserver variability for the readers, the {kappa} values for the expanded gallbladder fossa sign indicated good or excellent agreement (range, 0.70–0.79).

The expanded gallbladder fossa sign was seen in 129 of the 190 cirrhosis patients (Figs 2, 3) and in three of the 123 control subjects (P < .001). The sensitivity, specificity, accuracy, and positive predictive value of the expanded gallbladder fossa sign for the MR diagnosis of cirrhosis were 68%, 98%, 80%, and 98%, respectively. Among the three control subjects with the expanded gallbladder fossa sign, one had a small medial segment of the left hepatic lobe, which might be congenital (Fig 5), and two had a large lateral segment of the left hepatic lobe in the cephalocaudal direction, which is probably a normal variant.



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  		Figure 5. Noncirrhotic liver with the expanded gallbladder fossa sign in a 44-year-old woman. Axial contrast-enhanced T1-weighted gradient-echo image (140/2.2 with 90° flip angle) with fat suppression shows the expanded gallbladder fossa sign (arrow) due to the small medial segment of the left hepatic lobe, which is not seen at this level.

 

   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
For the diagnosis of cirrhosis at cross-sectional imaging, several reports have described the potential importance of the quantitative analysis of regional changes in hepatic morphology (7–12). The disadvantage of these methods, however, was the necessity for additional efforts to perform several measurements of the liver segments and the resultant calculations. In the current study, we evaluated the diagnostic potential of the expanded gallbladder fossa sign as a simple qualitative visual finding for cirrhosis. Our results showed that the sign had high specificity and positive predictive value (each, 98%) for cirrhosis.

Normally, the gallbladder is located on the visceral surface of the liver in a fossa between the right hepatic lobe and the medial segment of the left hepatic lobe in the plane of the major interlobar fissure. The gallbladder fits in this fossa, which contains little fatty tissue. At the caudal level, the gallbladder is covered by a part of the medial segment of the left hepatic lobe. Conversely, the pericholecystic space (gallbladder fossa) is often enlarged in patients with cirrhosis and is filled with increased fatty tissue, demonstrating the expanded gallbladder fossa sign.

The expanded gallbladder fossa sign in cirrhotic livers may depend on four factors: (a) atrophy of the medial segment of the left hepatic lobe, (b) hypertrophy of the caudate lobe, (c) atrophy of the right hepatic lobe (mainly the anterior segment) with counterclockwise rotation of the major interlobar fissure, and (d) actual enlargement of the lateral segment of the left hepatic lobe especially in the cephalocaudal direction. In previous studies, these factors have often been evaluated separately for the diagnosis of cirrhosis. Hess et al (9) focused on enlargement of the caudate lobe and indicated the utility of multidimensional caudate lobe measurements. Kubota et al (14) concentrated on shrinkage of the right hepatic lobe and rotation of the interlobar fissure determined by measuring an "interlobar fissure angle." Lafortune et al (12) emphasized atrophy of the left medial segment based on measurements of its transverse diameter. Each of these individual findings are characteristics of cirrhosis, so systematic analysis of combined hepatic morphologic changes may be more effective for the diagnosis of cirrhosis. The expanded gallbladder fossa sign is a consequence of each of these morphologic changes in the liver. Additionally, this sign is simpler to evaluate in clinical practice than are quantitative measurements. Although the expanded gallbladder fossa sign is determined by means of visual inspection, good interobserver agreement proves this sign is reproducible.

Segmental liver volume is related to portal venous blood flow because of various trophic factors within portal venous blood (15,16). Therefore, altered portal blood flow in liver segments is likely to be attributed to regional changes in hepatic morphology, producing the expanded gallbladder fossa sign, although the exact mechanism remains unclear (6,7,12).

In our series, the sensitivity of the expanded gallbladder fossa sign for diagnosis of cirrhosis was relatively low (68%), indicating that one of three patients with cirrhosis will not exhibit it. However, its high specificity renders this sign as important as other findings of cirrhosis that may be more sensitive. This sign is not meant to be used alone but in conjunction with other intra- and extrahepatic findings for cirrhosis described in prior reports (2,4,5); therefore, the low sensitivity of this sign is not a great disadvantage.

There are two possible reasons that not all cases of cirrhosis will exhibit the expanded gallbladder fossa sign. In some patients with early and mild cirrhosis, morphologic changes in the liver may not be apparent, resulting in absence of the expanded gallbladder fossa sign. In patients with compensated cirrhosis, characteristic changes in hepatic morphology (hypertrophy of the left lateral segment and the caudate lobe and atrophy of the left medial segment and the right lobe) will occur, producing the expanded gallbladder fossa sign. However, in patients with more advanced cirrhosis, the lateral segment of the left hepatic lobe shows atrophic change rather than enlargement (6). Therefore, absence of the expanded gallbladder fossa sign may be attributed to atrophy of the left lateral segment and a preserved gallbladder position (17) despite shrinkage of the left medial and right hepatic lobes. In these patients, however, other diagnostic findings for cirrhosis should be readily seen. It would be interesting to compare the clinical stage of cirrhosis in the false-negative cases.

It should be noted that the expanded gallbladder fossa sign was found in 2% (three of 123) of the control subjects. This may relate to normal hepatic morphologic variations or to rare congenital anomalies of the liver. In one of these three patients, the expanded gallbladder fossa sign was seen due to a small left medial segment. Morioka et al (18) reported a case of agenesis of the medial segment of the left hepatic lobe, and Burton et al (19) reported a case of bipartite liver. In these two previous cases, morphologic changes in the liver were similar to our expanded gallbladder fossa sign. In the remaining two patients, the expanded gallbladder fossa sign was due to a large left lateral segment. Chezmar et al (20) revealed that the lateral segment of the left hepatic lobe demonstrated marked variability in size based on volumetric calculation at spiral CT.

This study has limitations that deserve special mention. We did not evaluate the frequency of the expanded gallbladder fossa sign in our patient population in relation to other classic findings of cirrhosis, such as nodularity of the liver surface, coarse liver architecture, ascites, and signs of portal hypertension. Consideration of additional findings suggestive of cirrhosis would improve sensitivity for the MR imaging diagnosis of cirrhosis. Additionally, performance of a further prospective study would be necessary to determine if the expanded gallbladder fossa sign has prognostic importance for cirrhosis or can be used to monitor clinical progression. Another limitation of this study is that our patient selection based on MR records and pathologic proof of cirrhosis might be biased because patients with early cirrhosis who did not undergo liver biopsy might have been overlooked. Finally, the expanded gallbladder fossa sign can also be assessed by means of CT, although MR imaging may offer a more extensive, comprehensive evaluation of cirrhosis than can other imaging methods, including findings such as minimal ascites, fat and iron deposition, and detection of dysplastic nodules.

In conclusion, the expanded gallbladder fossa sign on MR images of the liver is a simple, frequently present, specific indicator of cirrhosis, with a positive predictive value of 98%.


   Footnotes
 
Author contributions: Guarantors of integrity of entire study, K.I., D.G.M.; study concepts, K.I., D.G.M.; study design, K.I.; definition of intellectual content, K.I., D.G.M.; literature research, K.I.; clinical studies, K.I., D.G.M.; data acquisition, all authors; data analysis, K.I.; statistical analysis, K.I.; manuscript preparation, K.I.; manuscript editing and review, D.G.M.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Goyal AK, Pokharna DS, Sharma SK. Ultrasonic diagnosis of cirrhosis: reference to quantitative measurements of hepatic dimensions. Gastrointest Radiol 1990; 15:32-34.[Medline]
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  3. Ferral H, Male R, Cardiel M, Munoz L, Ferrari FQ. Cirrhosis: diagnosis by liver surface analysis with high-frequency ultrasound. Gastrointest Radiol 1992; 17:74-78.[Medline]
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  6. Ito K, Mitchell DG, Hann HWL, et al. Progressive viral-induced cirrhosis: serial MR imaging findings and clinical correlation. Radiology 1998; 207:729-735.[Abstract/Free Full Text]
  7. Harbin WP, Robert NJ, Ferrucci JT, Jr. Diagnosis of cirrhosis based on regional changes in hepatic morphology: a radiological and pathological analysis. Radiology 1980; 135:273-283.[Abstract/Free Full Text]
  8. Giorgio A, Amoroso P, Lettieri G, et al. Cirrhosis: value of caudate to right lobe ratio in diagnosis with ultrasound. Radiology 1986; 161:443-445.[Abstract/Free Full Text]
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