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Cirrhosis: MR imaging features
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MR IMAGING OF THE LIVER II: DISEASES
CIRRHOSIS: MR IMAGING FEATURES Katsuyoshi Ito, MD, Donald G. Mitchell, MD, and Evan S. Siegelman, MD
A wide range of disease processes cause hepatic injury and may lead to cirrhosis. Although cirrhosis has traditionally been diagnosed by laboratory examination or liver biopsy, MR imaging can facilitate this diagnosis. MR imaging can provide a comprehensive evaluation of cirrhosis, including findings such as changes of regional hepatic morphology, nodular liver surface, iron and fat deposition, ascites, regenerative nodules, splenomegaly, and varices and collaterals. 18 In certain instances, the specificity of MR imaging findings is sufficient to obviate the need for histologic examination. In this article, we review the spectrum of MR findings of cirrhosis and its complications.
MORPHOLOGIC CHANGES OF THE LIVER Advanced Cirrhosis Cirrhosis occurs as a chronic response to repeated episodes of hepatocellular injury. It is characterized by repeated episodes of impaired circulation, injury, and inflammation,
and the key components of regeneration and fibrosis.12 Although there are many causes of cirrhosis, including viral infections, alcohol abuse, hemochromatosis, autoimmune disease, Wilson’s disease, primary sclerosing cholangitis, and primary biliary cirrhosis, the most common pathologic conditions are alcohol-related injury and viral hepatitis.15 During its course, cirrhosis gives rise to progressive lobar or segmental changes of hepatic morphology. Characteristic MR imaging features of advanced cirrhosis include atrophy of the right hepatic lobe and the left medial segment, with compensatory hypertrophy of the caudate lobe and the left lateral segment. A ratio equal to or greater than 0.65 (90% specific for the presence of cirrhosis) between the transverse width of the caudate lobe and that of the right lobe can be used to differentiate normal from cirrhotic livers.17 The patterns of hepatic morphologic changes overlap among different causes of cirrhosis, preventing identification of the specific cause of cirrhosis. There are, however, some etiologic tendencies in their appearances. Enlargement of the lateral segment, accompanied by shrinkage of the right lobe and
From the Department of Radiology, Yamaguchi University School of Medicine, Ube, Yamaguchi, Japan (KI); and the Department of Radiology, Thomas Jefferson University Hospital (KI, DGM); and the Department of Radiology, University of Pennsylvania Medical Center (ESS), Philadelphia, Pennsylvania
MRI CLINICS OF NORTH AMERICA VOLUME 10 • NUMBER 1 • FEBRUARY 2002
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Figure 1. Advanced cirrhosis in a patient with viral hepatitis B infection. Opposed-phase gradient echo (GRE) MR image shows marked enlargement of the left lateral segment of the liver (arrow). Left medial segment is not visible on this image because of its atrophic change.
the left medial segment, occurs frequently in patients with viral-induced cirrhosis (Fig. 1). Conversely, marked caudate lobe enlargement is typically associated with alcoholic cirrhosis (Fig. 2). Occasionally, only the lateral or posterior segments are atrophic. This is seen most often in patients with primary sclerosing cholangitis (Fig. 3).8, 22 The liver in patients with end-stage cirrhosis caused by primary biliary cirrhosis occasionally is diffusely hypertrophic.
Early Cirrhosis Cirrhosis can be categorized clinically as compensated or decompensated. Compensated cirrhosis is often asymptomatic and may be discovered at a routine clinical examination or by biochemical screening. Morphologic changes of the liver are seen less frequently in early compensated cirrhosis, impairing diagnostic imaging. The caudate-to-right-lobe ratio cannot predict the
Figure 2. Advanced cirrhosis in a patient with alcoholic abuse. T2-weighted fast spin-echo (FSE) image shows marked hypertrophy of the caudate lobe (arrow).
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Figure 3. Primary sclerosing cholangitis. T1-weighted SE image shows marked enlargement of the caudate lobe of the liver (arrow). The lateral and medial segment of the left hepatic lobe are not seen in this level because of their severe atrophic changes. (From Ito K, Mitchell DJ, Outwater E et al: Primary sclerosing cholangitis: MR imaging features. AJR 172:1527– 1533, 1999; with permission.)
presence or absence of early cirrhosis.19 Enlargement of the hilar periportal space has been found helpful for the diagnosis of early cirrhosis (Fig. 4). Enlargement of the hilar periportal space was visible in 98% of patients with early cirrhosis who did not have conventional signs (e.g., splenomegaly, portosystemic collateral vessels, ascites, or surface nodularity), whereas this finding was seen in only 11% of patients with normal livers.19 Of-
ten, expansion of the major interlobar fissure is seen in these patients with early cirrhosis, causing extrahepatic fat to fill the space between the left medial and lateral segments (Fig. 5). Enlargement of the hilar periportal space filled with increased fatty tissue is considered to be caused by atrophy of the medial segment of the left hepatic lobe.26 Therefore, atrophy of the left medial segment may be an initial morphologic change of the liver in early cirrhosis.
Figure 4. Early cirrhosis. T1-weighted SE image demonstrates enlargement of the hilar periportal space (arrow) between the left medial segment of the liver and the right portal vein.
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Figure 5. Early cirrhosis. T2-weighted FSE image shows expansion of the major interlobar fissure (arrow). Note increased extrahepatic fat between the left medial and lateral segments.
REGENERATIVE NODULES Microscopically, cirrhosis can be characterized as having micronodular, macronodular, or mixed regenerative changes. Micronodular cirrhosis, common in alcoholic liver disease and hemochromatosis, has regenerative nodules of 3 mm or less, with thin fibrous septa (Fig. 6). Conversely, in patients with viralinduced cirrhosis (especially hepatitis B), the regenerative nodules are 3 mm to 15 mm in size with thick fibrous septa; this is classified as macronodular cirrhosis (Fig. 7). Both types result in progressive fibrosis, hepatic failure,
and portal hypertension. Sometimes, regenerative nodules form large masses, mimicking hepatocellular carcinomas. Regenerative nodules are revealed in only 25% of unenhanced CT scans because of limited contrast resolution. MR images can depict regenerative nodules with greater clarity than other imaging modalities. The typical appearance of regenerative nodules on MR images consists of isointense or relatively hyperintense nodules on T1-weighted images and low-signal-intensity nodules on T2weighted images. These appearances may be caused by the prolonged T1 and T2 values of
Figure 6. Nodular surface of the liver. Gadolinium-enhanced GRE image demonstrates irregularity of the liver surface (arrows) caused by regenerative nodules.
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Figure 7. Macronodular regenerative nodules. Gadolinium-enhanced GRE image demonstrates the hypointense nodules (arrows) less than 3 mm in diameter, representing micronodular regenerative nodules.
fibrous septa, because of infiltration by inflammatory cells and the development of pseudo bile ducts in the fibrous septa surrounding the regenerative nodules.25, 33 Regenerative nodules often accumulate more iron than the surrounding hepatic parenchyma does. MR imaging has the advantage of detecting siderotic regenerative nodules, which are demonstrated as having low signal intensity on T2-weighted and gradientecho (GRE) images (Fig. 8). Because GRE MR imaging is particularly susceptible to mag-
netic field heterogeneity, siderotic regenerative nodules may cause artifactual enlargement of the regenerative nodules.31
NODULAR SURFACE OF THE LIVER Distortion of the hepatic parenchyma has a variable effect on the surface of the liver. The liver contour often appears nodular in patients with cirrhosis. A nodular liver surface on ultrasound was seen in 88% of cirrhotic
Figure 8. Macronodular regenerative nodules in a patient with viral hepatitis B infection. T1-weighted GRE image demonstrates relatively hyperintense nodules (arrows) 3 to 15 mm in diameter with thick hypointense septa, representing macronodular regenerative nodules.
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patients.7 This sign can be identified on MR imaging as irregularity of the liver surface, commonly seen on the surface of the left lateral segment (Fig. 9). This finding is an objective sign that directly correlates with the size of the underlying regenerative nodules. A surface that is smooth or deformed by multiple small nodules is typical in micronodular cirrhosis; a coarse nodularity of the surface is the result of micronodular cirrhosis.9
IRON DEPOSITION Cirrhosis can cause hepatic parenchymal iron deposition. Iron deposition within tissues reduces T2 and T2* relaxation times significantly, allowing MR imaging to be sensitive and specific for iron and its regional distribution.1 The presence of excess hepatic iron has traditionally been confirmed by liver biopsy with histology and measurement of hepatic iron content. Recent studies have shown a significant correlation between the hepatic iron concentration revealed at MR imaging with T2-weighted or T2*-weighted sequences and the hepatic iron concentration value measured at biopsy. These studies indicated that MR imaging with these sequences can be used to accurately quantify the amount of hepatic iron.11, 14 Qualitative MR evaluation of the distribution of abnormal low signal
intensity can suggest the correct underlying cause. Images of cirrhotic patients with genetic hemochromatosis (GH) show low pancreatic signal intensity (Fig. 10), whereas those of cirrhotic patients without GH show normal pancreatic signal intensity and tend to have only mildly decreased liver signal intensity.36 FIBROSIS Intrahepatic fibrosis can occur diffusely or focally in the cirrhotic liver and is visualized as high intensity on T2-weighted MR images. Four different patterns of diffuse fibrosis are seen on T2-weighted MR images: (1) patchy, poorly defined regions of high signal intensity, (2) thin perilobular bands of high signal intensity, (3) thick bridging bands of high signal intensity that surround regenerative nodules, and (4) diffuse fibrosis that causes perivascular (bull’s-eye) cuffing. 9 Most fibrosis appears as regions of low signal intensity on T1-weighted MR images and shows mild enhancement on contrast-enhanced MR images. Although most forms of diffuse fibrosis can occur in any type of cirrhosis, thin perilobular bands and perivascular cuffing appear most commonly in primary biliary cirrhosis. Focal confluent fibrosis can mimic hepatocellular carcinoma on imaging. This type of massive fibrosis is commonly located in the
Figure 9. Siderotic regenerative nodules. T1-weighted GRE image shows multiple hepatic nodules with markedly low-signal intensity (arrows), representing siderotic regenerative nodules.
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Figure 10. Hepatic iron deposition in a patient with cirrhosis. In-phase T1-weighted GRE image shows the liver with decreased signal intensity (arrow) compared with the skeletal muscle. Note the pancreas with normal signal intensity.
anterior and medial segments of the liver and has a wedge-shaped appearance, but in some patients the entire segment is involved.32 T2weighted MR images depict the lesions as regions of high signal intensity with characteristic retraction of the overlying liver capsule (Fig. 11). EXPANDED GALLBLADDER FOSSA SIGN The gallbladder normally fits in a fossa between the right hepatic lobe and the medial segment of the left hepatic lobe in the plane of
Figure 11. Confluent fibrosis. T2-weighted FSE image with fat suppression shows a wedge-shaped lesion with high signal intensity (arrow) located in the anterior segment, corresponding to focal confluent fibrosis. Note characteristic retraction of the liver surface.
the major interlobar fissure. In patients with cirrhosis, however, the pericholecystic space (gallbladder fossa) is often enlarged and filled with increased fat tissue, presenting the expanded gallbladder fossa (GBF) sign (Fig. 12).20 The expanded GBF sign has high specificity and positive predictive value (98% for each) for diagnosing cirrhosis. 20 The expanded GBF sign is defined as enlargement of the pericholecystic space (i.e., gallbladder fossa), 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 by the anterior edge of the caudate lobe, with nonvisualization of the medial segment of the left hepatic lobe on the same axial image. The expanded GBF sign in cirrhotic livers may be dependent on a combination of the following four factors: (1) atrophy of the medial segment of the left hepatic lobe, (2) hypertrophy of the caudate lobe, (3) atrophy of the right hepatic lobe (mainly the anterior segment) with counterclockwise rotation of the major interlobar fissure, and (4) enlargement of the lateral segment of the left hepatic lobe, especially in the cephalocaudal direction. The expanded GBF sign is a frequently present, specific indicator of cirrhosis. It can be used as a simple and highly specific sign of cirrhosis. PROGRESSIVE CIRRHOSIS Cirrhosis progresses slowly from compensated to decompensated cirrhosis, and finally
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Figure 12. Expanded gallbladder fossa (GBF) sign. T2weighted FSE image shows enlargement of GBF (arrow) and intrusion of intestines into this space, presenting the expanded GBF sign. Hypertrophy of the left lateral segment and atrophy of the right hepatic lobe as well as irregularity of the liver surface also are noted. The left medial segment is not seen at this level because of its atrophic change.
to end-stage cirrhosis. In patients with progressive cirrhosis in whom the clinical stage deteriorated from Child A (compensated) to Child B or C (decompensated) cirrhosis, the volume of the anterior, posterior, and medial segments decreased significantly (Fig. 13), whereas the volume of the caudate lobe and left lateral segment did not change.21 Conversely, in patients with stable cirrhosis in
whom the clinical stage remained at Child A (compensated) cirrhosis, the volume of the caudate lobe and left lateral segment increased significantly, although there was no significant change in the volume of the anterior, posterior, and medial segments.21 These results indicate that in compensated (stable) cirrhosis, hypertrophy of the lateral segment and the caudate lobe is the predominant
Figure 13. Progressive cirrhosis that has progressed from child A to C during 53 months of followup. A, Initial MR image shows slight enlargement of the caudate lobe of the liver (arrow). Atrophy of the medial segment and the right lobe of the liver, however, is not apparent. B, MR image obtained 53 months later shows marked atrophy of the medial segment of the left hepatic lobe (arrow). The falciform ligament (arrowhead) has rotated counterclockwise relative to the earlier examination caused by the atrophy of the left medial segment. (From Ito K, Mitchell DG, Hann HWL et al: Progressive viral-induced cirrhosis: serial MR imaging findings and clinical correlation. Radiology 207:729–735, 1998; with permission.)
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finding on serial MR imaging, whereas atrophy of the medial segment and the right lobe is the significant finding in progressive cirrhosis. In compensated cirrhosis, the damaged liver preserves hepatic function, in part, by compensatory hypertrophy of the lateral segment and the caudate lobe, even though cirrhosis might slowly and gradually progress throughout the liver. When hepatic fibrosis proceeds and the ability for lateral segment and caudate lobe hypertrophy exceeds its upper limit, the cirrhotic liver cannot compensate anymore, resulting in progression to clinically decompensated cirrhosis. Then, atrophy of the medial segment and the right lobe becomes evident. These findings are helpful for understanding disease progression in patients with cirrhosis.
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Figure 14. Dilatation of right inferior phrenic artery. Threedimensional (3-D) contrast-enhanced arterial-phase dynamic MR image with fat suppression demonstrates the dilated right inferior phrenic artery (arrow) between the inferior vena cava and the right crus of diaphragm in a patient with cirrhosis.
GASTROINTESTINAL WALL THICKENING DILATATION OF RIGHT INFERIOR PHRENIC ARTERY The inferior phrenic arteries are two small vessels that supply the diaphragm. The right inferior phrenic artery is clinically important because it can act as a feeding vessel for hepatocellular carcinoma (HCC) located near the liver surface.6, 10, 41 It is known that the inferior phrenic arterial flow to the liver increases when the hepatic arteries are occluded.40 Additionally, right inferior phrenic artery enlargement is often observed in patients with cirrhosis. This finding is readily depicted on axial thin-section, three-dimensional (3D), contrast-enhanced, arterial-phase, dynamic MR images with fat suppression (Fig. 14). In cirrhotic patients, atrophy of the liver enlarges the space between the inferior vena cava and the crus of diaphragm, resulting in better delineation of the dilated right inferior phrenic artery within this space. One possible cause for the right inferior phrenic artery enlargement in cirrhotic patients is that the right inferior phrenic arterial flow may increase secondarily, along with hepatic arterial flow, to compensate for the decreased portal inflow in cirrhotic livers.
The association between gastrointestinal wall thickening and cirrhosis is well recognized. The cause of this is probably edema due to hypoproteinemia, portal hypertension, or a combination of both. One study reported that isolated or predominantly right-sided colonic wall thickening is seen in as many as 25% of patients with end-stage cirrhosis (Fig. 15). This is probably related to changes in blood flow and hydrostatic pressures caused by portal hypertension.16 Many of these patients do not have specific or focal bowel symptoms. Another study demonstrated specific patterns of gastrointestinal wall thickening in patients with cirrhosis: if the jejunum is normal, no wall thickening is seen in the duodenum or in the ileum; if the ascending colon is normal, no wall thickening is seen in the transverse or descending colon.24 Observation of atypical patterns of wall thickening in patients with cirrhosis should prompt a search for additional potential causes, including inflammatory, ischemic, and neoplastic diseases. Haustral thickening of the colon is also seen commonly in patients with cirrhosis, although nodular haustral thickening has been described as a specific feature of pseudomembranous colitis.
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Figure 15. Colonic wall thickening. T2-weighted FSE image shows wall thickening of the ascending colon.
Mesenteric, omental, and retroperitoneal edema occur often in patients with cirrhosis. The appearance of mesenteric edema varies from a mild infiltrative haze to a severe masslike sheath that engulfs the mesenteric vessels. Increasing severity, diffuse distribution, masslike appearance, and recruitment of omental and retroperitoneal sites are parameters of mesenteric edema severity and generally correlate with severe ascites, subcutaneous edema, and low serum albumin levels.5
PORTAL HYPERTENSION Although portal hypertension can result from obstruction at postsinusoidal, sinusoidal, or presinusoidal levels, the major cause of portal hypertension in cirrhosis is the intrahepatic sinusoidal type. During the early stages of portal hypertension, the portal system dilates but flow is maintained. Later, numerous portosystemic collateral pathways from the high-pressure portal system to the low-pressure systemic circulation may develop, reducing the volume of flow to the liver and decreasing the size of the portal vein. Major sites of portosystemic collateralization include the gastroesophageal junction (from the coronary and short gastric veins to the systemic esophageal vein), paraumbilical veins (from the left portal vein to the paraumbilical veins to the systemic epigastric veins),
retroperitoneal regions (from veins of the duodenum, ascending and descending colon, and liver to the systemic lumbar, phrenic, gonadal, and renal veins), gastro- or splenorenal regions (from the coronary, short gastric, and splenic veins to the systemic left renal vein), and hemorrhoidal veins (from the superior hemorrhoidal vein to the systemic middle and inferior hemorrhoidal veins).35 The most prevalent and clinically important portosystemic collaterals are the gastroesophageal varices because they are the most common source of upper gastrointestinal bleeding. Esophageal varices can be seen as enlarged, tortuous veins within the wall of the lower esophagus (Figs. 16 and 17). Three-
Figure 16. Esophageal varices. Gadolinium-enhanced GRE image demonstrates markedly enhanced varices within the esophageal wall (arrow).
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Figure 17. Paraesophageal varices. Gadolinium-enhanced GRE image demonstrates dilated paraesophageal varices around the aorta and the esophagus (arrow).
dimensional contrast-enhanced MR imaging provides excellent depiction of the portal venous system as high-intensity structures and enables continuous tracing of vascular structures (Fig. 18). Therefore, anatomic characteristics of these portosystemic collaterals can be depicted clearly. Esophageal varices are usually supplied by the anterior branch of the left gastric vein, which normally drains inferiorly toward the confluence of the splenic and superior mesenteric veins.39 In patients with esophageal varices, the flow in this vein reverses. The posterior branch of the left gastric vein supplies
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Figure 18. Massive paraesophageal varices. Reconstructed image with MPR technique from 3-D axial images clearly demonstrates the dilated coronary gastric vein and massive paraesophageal varices (arrow). (From Ito K, and Mitchell DG: MR imaging of cirrhosis and its complications. Contemporary Diagnostic Radiology 23:1–6, 2000; with permission.)
paraesophageal varices situated outside the wall of the esophagus in the mediastinum. The normal falciform ligament contains one to three tiny, collapsed paraumbilical veins. In patients with portal hypertension, the caliber of these vessels increases. The dilated paraumbilical veins arise from the left portal vein, traverse the falciform ligament, and drain into the veins of the anterior abdominal wall, sometimes producing a ‘‘Medusa’s head’’ appearance (Fig. 19). Paraumbilical ve-
Figure 19. Paraumbilical vein. A and B, Gadolinium-enhanced GRE images show the paraumbilical vein (arrows) originating from the left portal vein and passing anteriorly through the falciform ligament.
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Figure 20. Splenorenal shunt. A and B, These 3-D contrast-enhanced dynamic (portal phase) axial MR images with fat suppression show the enlarged splenic vein and the dilated tortuous collateral vessels (arrowhead) around the left kidney, running toward the left renal vein (arrow).
nous collaterals have been reported to develop in 10% to 43% of patients with portal hypertension. 4, 28, 30 The paraumbilical vein can become quite large and can function as a desirable route of natural decompression without gastrointestinal bleeding in portal hypertension. A splenorenal or gastrorenal shunt often occurs through an enlarged, left-sided retroperitoneal channel. These shunts may arise
from preexisting, small, normal portosystemic communications (Figs. 20 through 22). Splenorenal shunts typically originate from the splenic hilum, course medial to the enlarged spleen toward the left renal hilum, and anastomose with the left renal vein. The dilated, tortuous vessels between the hila of the spleen and left kidney on MR angiography represent a splenorenal shunt. Fusiform dilatation of the left renal vein is seen frequently.
Figure 21. Right-sided splenorenal shunt. A and B, These 3-D contrast-enhanced dynamic (portalphase) axial MR images with fat suppression show the dilated tortuous collateral vessels around the right kidney originating from the confluence of the superior mesenteric vein and the splenic vein, coursing toward the right side, and finally running into the right renal vein.
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Figure 22. Mesenteric varices. A–C, These 3-D contrast-enhanced dynamic (portal-phase) axial MR images with fat suppression show dilated vascular structures (arrow), running toward the inferior vena cava (IVC), representing mesenteric varices.
COMPLICATIONS AFTER LIVER TRANSPLANTATION Liver transplantation has become the treatment of choice for end-stage liver disease in appropriate candidates. Even with improvements in surgical technique and immunosuppression, however, there are still several significant complications. MR imaging is an outstanding method for comprehensive evaluation of complications after liver transplantation. With one examination, abnormalities of vascular structures, bile ducts, and liver parenchyma can be detected readily.23
or the intersegmental fissure of the transplanted liver are commonly seen within the first few days of transplantation. Lymph nodes are often identified in the porta hepatis and portacaval space and are usually reactive (Fig. 23). Periportal high intensity on T2weighted images is seen with greater frequency in patients with a shorter interval after transplantation (Fig. 24); this persists for several weeks. This may be caused by dilated lymphatics resulting from impaired drainage after surgery. Periportal high intensity does not correlate with acute allograft rejection.27
Common Expected Findings After Transplantation
Vascular Complications
A small amount of ascites, fluid, small seromas, or hematomas in the perihepatic region
Hepatic artery thrombosis is the most common vascular complication, occurring in up
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Figure 23. Lymph nodes enlargement after liver transplantation. T2-weighted FSE image shows reactive lymph nodes enlargement in the porta hepatis (arrows).
to 12% of adult transplant patients. Reported risk factors include increased cold ischemia time of the donor liver, severe acute rejection, ABO blood type incompatibility, and incongruence of the joined vessels.29 After transplantation, the bile duct is entirely dependent on hepatic arterial blood supply, and occlusion of the hepatic artery leads to bile duct ischemia and necrosis. Contrast-enhanced 3D MR angiography is a useful and noninvasive method for evaluating hepatic artery patency, with accuracy similar to that of ultrasound (Fig. 25).37 Portal vein stenosis or thrombosis is an un-
Figure 24. Periportal abnormal intensity. T2-weighted FSE image shows diffuse periportal abnormal high intensity seen as periportal tramline (arrow).
common complication after transplantation. Portal vein stenosis usually occurs at the anastomosis. Symptoms may include portal hypertension, hepatic failure, massive ascites,
Figure 25. Hepatic artery thrombosis. Maximum intensity projection (MIP) image from 3-D contrast-enhanced MR angiography shows proximal thrombosis of hepatic artery (arrow). Note lack of opacification of distal branches. Gastroduodenal artery and the superior mesenteric artery are normal. (From Ito K, Siegelman ES, Stolpen AH et al: MR imaging of complications after liver transplantation. AJR 175:1145–1149, 2000; with permission.)
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Figure 26. Portal vein thrombosis. MIP image from 3-D contrast-enhanced MR angiography demonstrates narrowing of the portal vein (arrow) caused by intraluminal thrombosis.
or edema. Contrast-enhanced MR angiography can show obvious narrowing or intraluminal thrombosis (Fig. 26).37 Inferior vena cava (IVC) thrombosis is rare, occurring in less than 3% of transplants and resulting from technical problems or compression of the vessels by a fluid collection.2 Flow-sensitive GRE MR imaging (i.e., timeof-flight or phase-contrast) can also be used to evaluate vascular complications. IVC
thrombus is depicted as an intraluminal defect (Fig. 27).
Biliary Tract Complications Most biliary strictures occur at the anastomotic site and may be caused by scar formation that results in retraction and narrowing. MR cholangiography can be used to screen
Figure 27. IVC thrombosis. A, T1-weighted SE image shows intermediate signal intensity within the IVC (arrow). B, Flow-sensitive GRE image shows signal defects within IVC (arrow), indicating the presence of thrombus. IVC is not completely obstructed.
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Figure 28. Mucocele of cystic duct remnant. T2-weighted coronal single-shot FSE image shows dilated cystic duct remnant (arrow) adjacent to common bile duct. (From Ito K, Siegelman ES, Stolpen AH et al: MR imaging of complications after liver transplantation. AJR 175:1145–1149, 2000; with permission.)
for biliary strictures.13 Bile leakage may occur, sometimes associated with biliary strictures. Leaks at the biliary anastomosis are the most common types, but bile leak may be caused by bile duct necrosis in patients with hepatic artery occlusion, producing bilomas or bile peritonitis. Mucocele of the cystic duct remnant is an uncommon complication that occurs when the donor cystic duct remnant becomes distended with mucus. It manifests a focal fluid collection adjacent to the hepatic duct. MR imaging can help distinguish between hematomas and other fluid collections in hepatic allograft recipients (Fig. 28).
Extrahepatic Complications Right adrenal gland hemorrhage is a complication after liver transplantation.3 Hemorrhage may be caused by (1) venous engorgement due to right adrenal vein ligation during removal of a portion of the IVC at transplantation or (2) coagulopathy secondary to the patient’s preexisting liver dysfunction. Adrenal hematoma is seen as a suprarenal mass on MR images. MR imaging is highly sensitive to hemorrhage because of its specific
Hepatic Parenchymal Complications Hepatic arterial insufficiency caused by thrombosis may induce bile duct necrosis, which may lead to bilomas, abscesses, or hepatic infarctions. Although the differentiation between biloma and abscess is often difficult, abscesses tend to have irregular, thick walls (Fig. 29). Hepatic infarctions are seen commonly as peripheral or central lesions with wedge-shaped or round appearances, without enhancement on contrast-enhanced MR images (Fig. 30).
Figure 29. Hepatic abscess. Gadolinium-enhanced GRE image shows a massive lesion with enhanced thick wall and septa (arrow) in the right hepatic lobe. The diagnosis of abscess was confirmed by percutaneous drainage.
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Figure 30. Hepatic infarctions. Gadolinium-enhanced GRE image shows multiple unenhanced areas with nontumorous configuration (arrows) in the liver, indicating hepatic infarctions secondary to hepatic artery thrombosis. Liver infarction was pathologically confirmed by second transplantation.
high signal with heterogeneity on both T1and T2-weighted images (Fig. 31). Post-transplant lymphoproliferative disorder (PTLD) is a lymphocyte proliferative process that occurs in transplant recipients whose immune systems are compromised. PTLD is strongly associated with infection with Epstein-Barr virus, inducing B-lymphocyte proliferation.38 PTLD may involve any organ in the body, but the lymph nodes, lungs, and gastrointestinal tract are involved most often.34 PTLD is varied in presentation, ranging
Figure 31. Adrenal hemorrhage. Opposed-phase T1weighted GRE image depicts right adrenal hematoma that shows peripheral high signal intensity with central low signal (arrow).
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Figure 32. Post-transplant lymphoproliferative disorder. Gadolinium-enhanced GRE image shows a mass with rim enhancement (arrow) near the liver. Pathologic diagnosis of lymphoma was confirmed by biopsy. (From Ito K, Siegelman ES, Stolpen AH et al: MR imaging of complications after liver transplantation. AJR 175:1145–1149, 2000; with permission.)
from a benign illness resembling mononucleosis to a fulminant lymphoma similar to an aggressive non-Hodgkin’s lymphoma (Fig. 32).
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9. Dodd GDI, Baron RL, Oliver JHI, Federle MP: Spectrum of imaging findings of the liver in end-stage cirrhosis: Part I. Gross morphology and diffuse abnormalities. AJR Am J Roentgenol 173:1031–1036, 1999 10. Duprat G, Charnsangavej C, Wallace S, Carrasco CH: Inferior phrenic artery embolization in the treatment of hepatic neoplasms. Acta Radiol 29:427–429, 1988 11. Ernst O, Sergent G, Bonvarlet P, et al: Hepatic iron overload: Diagnosis and quantification with MR imaging. AJR Am J Roentgenol 168:1205–1208, 1997 12. Fisher MR, Gore RM: Computed tomography in the evaluation of cirrhosis and portal hypertension. J Clin Gastroenterol 7:173–181, 1985 13. Fulcher AS, Turner MA: Orthotopic liver transplantation: Evaluation with MR cholangiography. Radiology 211:715–722, 1999 14. Gomori JM, Horev G, Tamary H, et al: Hepatic iron overload: Quantitative MR imaging. Radiology 179: 367–369, 1991 15. Gore RM: Diffuse liver disease: In Gore RM, Levine NS, Laufer I (eds): Textbook of Gastrointestinal Radiology. Philadelphia, WB Saunders, 1994, pp 1968– 2017 16. Guingrich J, Kuhlman JE: Colonic wall thickening in patients with cirrhosis: CT findings and clinical implications. AJR Am J Roentgenol 172:919–924, 1999 17. Harbin WP, Robert NJ, Ferrucci JT Jr: Diagnosis of cirrhosis based on regional changes in hepatic morphology: A radiological and pathological analysis. Radiology 135:273–283, 1980 18. Ito K, Mitchell DG: MR imaging of cirrhosis and its complications. Contemporary Diagnostic Radiology 23:1–6, 2000 19. Ito K, Mitchell DG, Gabata T: Enlargement of hilar periportal space: A sign of early cirrhosis at MR imaging. J Magn Reson Imaging 11:136–140, 2000 20. Ito K, Mitchell DG, Gabata T, Hussain SM: Expanded gallbladder fossa: Simple MR imaging sign of cirrhosis. Radiology 211:723–726, 1999 21. Ito K, Mitchell DG, Hann HWL, et al: Progressive viral-induced cirrhosis: Serial MR imaging findings and clinical correlation. Radiology 207:729–735, 1998 22. Ito K, Mitchell DG, Outwater EK, Blasbalg R: Primary sclerosing cholangitis: MR imaging features. AJR Am J Roentgenol 172:1527–1533, 1999 23. Ito K, Siegelman ES, Stolpen AH, Mitchell DG: MR imaging of complications after liver transplantation. AJR Am J Roentgenol 175:1145–1149, 2000 24. Karahan OI, Dodd GDI, Chintapalli KN, et al: Gastrointestinal wall thickening in patients with cirrhosis: Frequency and patterns at contrast-enhanced CT. Radiology 215:103–107, 2000 25. Kita K, Kita M, Sato M, et al: MR imaging of liver cirrhosis: Role of fibrous septa in visualization of regenerating nodules. Acta Radiol 37:198–203, 1996
26. Lafortune M, Matricardi L, Denys A, et al: Segment 4 (the quadrate lobe): A barometer of cirrhotic liver disease at US. Radiology 206:157–160, 1998 27. Lang P, Schnarkowski P, Grampp S, et al: Liver transplantation: Significance of the periportal collar on MRI. J Comput Assist Tomogr 19:580–585, 1995 28. Lebrec D, Fleury PD, Rueff B, et al: Portal hypertension, size of esophageal varices, and risk of gastrointestinal bleeding in alcoholic cirrhosis. Gastroenterology 79:1139–1144, 1980 29. Legmann P, Costes V, Tudoret L, et al: Hepatic artery thrombosis after liver transplantation: Diagnosis with spiral CT. AJR Am J Roentgenol 164:97–101, 1995 30. McCain AH, Bernardino ME, Sones PJ, et al: Varices from portal hypertension: Correlation of CT and angiography. Radiology 154:63–69, 1985 31. Murakami T, Kuroda C, Marukawa T, et al: Regenerating nodules in hepatic cirrhosis. MR findings with pathologic correlation. AJR Am J Roentgenol 155: 1227–1231, 1990 32. Ohtomo K, Baron RL, Dodd GD, et al: Confluent hepatic fibrosis in advanced cirrhosis: Evaluation with MR imaging. Radiology 189:871–874, 1993 33. Ohtomo K, Itai Y, Ohtomo Y, et al: Regenerating nodules of liver cirrhosis: MR imaging with pathologic correlation. AJR Am J Roentgenol 154:505–507, 1990 34. Pickhardt PJ, Siegel MJ: Posttransplantation lymphoproliferative disorder of the abdomen: CT evaluation in 51 patients. Radiology 213:73–78, 1999 35. Pieters PC, Miller WJ, DeMeo JH: Evaluation of the portal venous system: Complementary roles of invasive and noninvasive imaging strategies. Radiographics 17:879–895, 1997 36. Siegelman ES, Mitchell DG, Semelka RC: Abdominal iron deposition: Metabolism, MR findings, and clinical importance. Radiology 199:13–22, 1996 37. Stafford-Johnson DB, Hamilton BH, Dong Q, et al: Vascular complications of liver transplantation: Evaluation with gadolinium-enhanced MR angiography. Radiology 207:153–160, 1998 38. Strouse PJ, Platt JF, Francis IR, Bree RL: Tumorous intrahepatic lymphoproliferative disorder in transplanted livers. AJR Am J Roentgenol 167:1159–1162, 1996 39. Takashi M, Igarashi M, Hino S, et al: Esophageal varices: Correlation of left gastric venography and endoscopy in patients with portal hypertension. Radiology 155:327–331, 1985 40. Takeuchi Y, Arai Y, Inaba Y, et al: Extrahepatic arterial supply to the liver: Observation with a unified CT and angiography system during temporary balloon occlusion of the proper hepatic artery. Radiology 209: 121–128, 1998 41. Tanabe N, Iwasaki T, Chida N, et al: Hepatocellular carcinomas supplied by inferior phrenic arteries. Acta Radiol 39:443–447, 1998 Address reprint requests to Katsuyoshi Ito, MD Department of Radiology Yamaguchi University School of Medicine 1-1-1 Minami Kogushi Ube, Yamaguchi 755–8505 Japan e-mail: [email protected]
MR IMAGING OF THE LIVER II: DISEASES
CIRRHOSIS: MR IMAGING FEATURES Katsuyoshi Ito, MD, Donald G. Mitchell, MD, and Evan S. Siegelman, MD
A wide range of disease processes cause hepatic injury and may lead to cirrhosis. Although cirrhosis has traditionally been diagnosed by laboratory examination or liver biopsy, MR imaging can facilitate this diagnosis. MR imaging can provide a comprehensive evaluation of cirrhosis, including findings such as changes of regional hepatic morphology, nodular liver surface, iron and fat deposition, ascites, regenerative nodules, splenomegaly, and varices and collaterals. 18 In certain instances, the specificity of MR imaging findings is sufficient to obviate the need for histologic examination. In this article, we review the spectrum of MR findings of cirrhosis and its complications.
MORPHOLOGIC CHANGES OF THE LIVER Advanced Cirrhosis Cirrhosis occurs as a chronic response to repeated episodes of hepatocellular injury. It is characterized by repeated episodes of impaired circulation, injury, and inflammation,
and the key components of regeneration and fibrosis.12 Although there are many causes of cirrhosis, including viral infections, alcohol abuse, hemochromatosis, autoimmune disease, Wilson’s disease, primary sclerosing cholangitis, and primary biliary cirrhosis, the most common pathologic conditions are alcohol-related injury and viral hepatitis.15 During its course, cirrhosis gives rise to progressive lobar or segmental changes of hepatic morphology. Characteristic MR imaging features of advanced cirrhosis include atrophy of the right hepatic lobe and the left medial segment, with compensatory hypertrophy of the caudate lobe and the left lateral segment. A ratio equal to or greater than 0.65 (90% specific for the presence of cirrhosis) between the transverse width of the caudate lobe and that of the right lobe can be used to differentiate normal from cirrhotic livers.17 The patterns of hepatic morphologic changes overlap among different causes of cirrhosis, preventing identification of the specific cause of cirrhosis. There are, however, some etiologic tendencies in their appearances. Enlargement of the lateral segment, accompanied by shrinkage of the right lobe and
From the Department of Radiology, Yamaguchi University School of Medicine, Ube, Yamaguchi, Japan (KI); and the Department of Radiology, Thomas Jefferson University Hospital (KI, DGM); and the Department of Radiology, University of Pennsylvania Medical Center (ESS), Philadelphia, Pennsylvania
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Figure 1. Advanced cirrhosis in a patient with viral hepatitis B infection. Opposed-phase gradient echo (GRE) MR image shows marked enlargement of the left lateral segment of the liver (arrow). Left medial segment is not visible on this image because of its atrophic change.
the left medial segment, occurs frequently in patients with viral-induced cirrhosis (Fig. 1). Conversely, marked caudate lobe enlargement is typically associated with alcoholic cirrhosis (Fig. 2). Occasionally, only the lateral or posterior segments are atrophic. This is seen most often in patients with primary sclerosing cholangitis (Fig. 3).8, 22 The liver in patients with end-stage cirrhosis caused by primary biliary cirrhosis occasionally is diffusely hypertrophic.
Early Cirrhosis Cirrhosis can be categorized clinically as compensated or decompensated. Compensated cirrhosis is often asymptomatic and may be discovered at a routine clinical examination or by biochemical screening. Morphologic changes of the liver are seen less frequently in early compensated cirrhosis, impairing diagnostic imaging. The caudate-to-right-lobe ratio cannot predict the
Figure 2. Advanced cirrhosis in a patient with alcoholic abuse. T2-weighted fast spin-echo (FSE) image shows marked hypertrophy of the caudate lobe (arrow).
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Figure 3. Primary sclerosing cholangitis. T1-weighted SE image shows marked enlargement of the caudate lobe of the liver (arrow). The lateral and medial segment of the left hepatic lobe are not seen in this level because of their severe atrophic changes. (From Ito K, Mitchell DJ, Outwater E et al: Primary sclerosing cholangitis: MR imaging features. AJR 172:1527– 1533, 1999; with permission.)
presence or absence of early cirrhosis.19 Enlargement of the hilar periportal space has been found helpful for the diagnosis of early cirrhosis (Fig. 4). Enlargement of the hilar periportal space was visible in 98% of patients with early cirrhosis who did not have conventional signs (e.g., splenomegaly, portosystemic collateral vessels, ascites, or surface nodularity), whereas this finding was seen in only 11% of patients with normal livers.19 Of-
ten, expansion of the major interlobar fissure is seen in these patients with early cirrhosis, causing extrahepatic fat to fill the space between the left medial and lateral segments (Fig. 5). Enlargement of the hilar periportal space filled with increased fatty tissue is considered to be caused by atrophy of the medial segment of the left hepatic lobe.26 Therefore, atrophy of the left medial segment may be an initial morphologic change of the liver in early cirrhosis.
Figure 4. Early cirrhosis. T1-weighted SE image demonstrates enlargement of the hilar periportal space (arrow) between the left medial segment of the liver and the right portal vein.
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Figure 5. Early cirrhosis. T2-weighted FSE image shows expansion of the major interlobar fissure (arrow). Note increased extrahepatic fat between the left medial and lateral segments.
REGENERATIVE NODULES Microscopically, cirrhosis can be characterized as having micronodular, macronodular, or mixed regenerative changes. Micronodular cirrhosis, common in alcoholic liver disease and hemochromatosis, has regenerative nodules of 3 mm or less, with thin fibrous septa (Fig. 6). Conversely, in patients with viralinduced cirrhosis (especially hepatitis B), the regenerative nodules are 3 mm to 15 mm in size with thick fibrous septa; this is classified as macronodular cirrhosis (Fig. 7). Both types result in progressive fibrosis, hepatic failure,
and portal hypertension. Sometimes, regenerative nodules form large masses, mimicking hepatocellular carcinomas. Regenerative nodules are revealed in only 25% of unenhanced CT scans because of limited contrast resolution. MR images can depict regenerative nodules with greater clarity than other imaging modalities. The typical appearance of regenerative nodules on MR images consists of isointense or relatively hyperintense nodules on T1-weighted images and low-signal-intensity nodules on T2weighted images. These appearances may be caused by the prolonged T1 and T2 values of
Figure 6. Nodular surface of the liver. Gadolinium-enhanced GRE image demonstrates irregularity of the liver surface (arrows) caused by regenerative nodules.
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Figure 7. Macronodular regenerative nodules. Gadolinium-enhanced GRE image demonstrates the hypointense nodules (arrows) less than 3 mm in diameter, representing micronodular regenerative nodules.
fibrous septa, because of infiltration by inflammatory cells and the development of pseudo bile ducts in the fibrous septa surrounding the regenerative nodules.25, 33 Regenerative nodules often accumulate more iron than the surrounding hepatic parenchyma does. MR imaging has the advantage of detecting siderotic regenerative nodules, which are demonstrated as having low signal intensity on T2-weighted and gradientecho (GRE) images (Fig. 8). Because GRE MR imaging is particularly susceptible to mag-
netic field heterogeneity, siderotic regenerative nodules may cause artifactual enlargement of the regenerative nodules.31
NODULAR SURFACE OF THE LIVER Distortion of the hepatic parenchyma has a variable effect on the surface of the liver. The liver contour often appears nodular in patients with cirrhosis. A nodular liver surface on ultrasound was seen in 88% of cirrhotic
Figure 8. Macronodular regenerative nodules in a patient with viral hepatitis B infection. T1-weighted GRE image demonstrates relatively hyperintense nodules (arrows) 3 to 15 mm in diameter with thick hypointense septa, representing macronodular regenerative nodules.
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patients.7 This sign can be identified on MR imaging as irregularity of the liver surface, commonly seen on the surface of the left lateral segment (Fig. 9). This finding is an objective sign that directly correlates with the size of the underlying regenerative nodules. A surface that is smooth or deformed by multiple small nodules is typical in micronodular cirrhosis; a coarse nodularity of the surface is the result of micronodular cirrhosis.9
IRON DEPOSITION Cirrhosis can cause hepatic parenchymal iron deposition. Iron deposition within tissues reduces T2 and T2* relaxation times significantly, allowing MR imaging to be sensitive and specific for iron and its regional distribution.1 The presence of excess hepatic iron has traditionally been confirmed by liver biopsy with histology and measurement of hepatic iron content. Recent studies have shown a significant correlation between the hepatic iron concentration revealed at MR imaging with T2-weighted or T2*-weighted sequences and the hepatic iron concentration value measured at biopsy. These studies indicated that MR imaging with these sequences can be used to accurately quantify the amount of hepatic iron.11, 14 Qualitative MR evaluation of the distribution of abnormal low signal
intensity can suggest the correct underlying cause. Images of cirrhotic patients with genetic hemochromatosis (GH) show low pancreatic signal intensity (Fig. 10), whereas those of cirrhotic patients without GH show normal pancreatic signal intensity and tend to have only mildly decreased liver signal intensity.36 FIBROSIS Intrahepatic fibrosis can occur diffusely or focally in the cirrhotic liver and is visualized as high intensity on T2-weighted MR images. Four different patterns of diffuse fibrosis are seen on T2-weighted MR images: (1) patchy, poorly defined regions of high signal intensity, (2) thin perilobular bands of high signal intensity, (3) thick bridging bands of high signal intensity that surround regenerative nodules, and (4) diffuse fibrosis that causes perivascular (bull’s-eye) cuffing. 9 Most fibrosis appears as regions of low signal intensity on T1-weighted MR images and shows mild enhancement on contrast-enhanced MR images. Although most forms of diffuse fibrosis can occur in any type of cirrhosis, thin perilobular bands and perivascular cuffing appear most commonly in primary biliary cirrhosis. Focal confluent fibrosis can mimic hepatocellular carcinoma on imaging. This type of massive fibrosis is commonly located in the
Figure 9. Siderotic regenerative nodules. T1-weighted GRE image shows multiple hepatic nodules with markedly low-signal intensity (arrows), representing siderotic regenerative nodules.
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Figure 10. Hepatic iron deposition in a patient with cirrhosis. In-phase T1-weighted GRE image shows the liver with decreased signal intensity (arrow) compared with the skeletal muscle. Note the pancreas with normal signal intensity.
anterior and medial segments of the liver and has a wedge-shaped appearance, but in some patients the entire segment is involved.32 T2weighted MR images depict the lesions as regions of high signal intensity with characteristic retraction of the overlying liver capsule (Fig. 11). EXPANDED GALLBLADDER FOSSA SIGN The gallbladder normally fits in a fossa between the right hepatic lobe and the medial segment of the left hepatic lobe in the plane of
Figure 11. Confluent fibrosis. T2-weighted FSE image with fat suppression shows a wedge-shaped lesion with high signal intensity (arrow) located in the anterior segment, corresponding to focal confluent fibrosis. Note characteristic retraction of the liver surface.
the major interlobar fissure. In patients with cirrhosis, however, the pericholecystic space (gallbladder fossa) is often enlarged and filled with increased fat tissue, presenting the expanded gallbladder fossa (GBF) sign (Fig. 12).20 The expanded GBF sign has high specificity and positive predictive value (98% for each) for diagnosing cirrhosis. 20 The expanded GBF sign is defined as enlargement of the pericholecystic space (i.e., gallbladder fossa), 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 by the anterior edge of the caudate lobe, with nonvisualization of the medial segment of the left hepatic lobe on the same axial image. The expanded GBF sign in cirrhotic livers may be dependent on a combination of the following four factors: (1) atrophy of the medial segment of the left hepatic lobe, (2) hypertrophy of the caudate lobe, (3) atrophy of the right hepatic lobe (mainly the anterior segment) with counterclockwise rotation of the major interlobar fissure, and (4) enlargement of the lateral segment of the left hepatic lobe, especially in the cephalocaudal direction. The expanded GBF sign is a frequently present, specific indicator of cirrhosis. It can be used as a simple and highly specific sign of cirrhosis. PROGRESSIVE CIRRHOSIS Cirrhosis progresses slowly from compensated to decompensated cirrhosis, and finally
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Figure 12. Expanded gallbladder fossa (GBF) sign. T2weighted FSE image shows enlargement of GBF (arrow) and intrusion of intestines into this space, presenting the expanded GBF sign. Hypertrophy of the left lateral segment and atrophy of the right hepatic lobe as well as irregularity of the liver surface also are noted. The left medial segment is not seen at this level because of its atrophic change.
to end-stage cirrhosis. In patients with progressive cirrhosis in whom the clinical stage deteriorated from Child A (compensated) to Child B or C (decompensated) cirrhosis, the volume of the anterior, posterior, and medial segments decreased significantly (Fig. 13), whereas the volume of the caudate lobe and left lateral segment did not change.21 Conversely, in patients with stable cirrhosis in
whom the clinical stage remained at Child A (compensated) cirrhosis, the volume of the caudate lobe and left lateral segment increased significantly, although there was no significant change in the volume of the anterior, posterior, and medial segments.21 These results indicate that in compensated (stable) cirrhosis, hypertrophy of the lateral segment and the caudate lobe is the predominant
Figure 13. Progressive cirrhosis that has progressed from child A to C during 53 months of followup. A, Initial MR image shows slight enlargement of the caudate lobe of the liver (arrow). Atrophy of the medial segment and the right lobe of the liver, however, is not apparent. B, MR image obtained 53 months later shows marked atrophy of the medial segment of the left hepatic lobe (arrow). The falciform ligament (arrowhead) has rotated counterclockwise relative to the earlier examination caused by the atrophy of the left medial segment. (From Ito K, Mitchell DG, Hann HWL et al: Progressive viral-induced cirrhosis: serial MR imaging findings and clinical correlation. Radiology 207:729–735, 1998; with permission.)
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finding on serial MR imaging, whereas atrophy of the medial segment and the right lobe is the significant finding in progressive cirrhosis. In compensated cirrhosis, the damaged liver preserves hepatic function, in part, by compensatory hypertrophy of the lateral segment and the caudate lobe, even though cirrhosis might slowly and gradually progress throughout the liver. When hepatic fibrosis proceeds and the ability for lateral segment and caudate lobe hypertrophy exceeds its upper limit, the cirrhotic liver cannot compensate anymore, resulting in progression to clinically decompensated cirrhosis. Then, atrophy of the medial segment and the right lobe becomes evident. These findings are helpful for understanding disease progression in patients with cirrhosis.
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Figure 14. Dilatation of right inferior phrenic artery. Threedimensional (3-D) contrast-enhanced arterial-phase dynamic MR image with fat suppression demonstrates the dilated right inferior phrenic artery (arrow) between the inferior vena cava and the right crus of diaphragm in a patient with cirrhosis.
GASTROINTESTINAL WALL THICKENING DILATATION OF RIGHT INFERIOR PHRENIC ARTERY The inferior phrenic arteries are two small vessels that supply the diaphragm. The right inferior phrenic artery is clinically important because it can act as a feeding vessel for hepatocellular carcinoma (HCC) located near the liver surface.6, 10, 41 It is known that the inferior phrenic arterial flow to the liver increases when the hepatic arteries are occluded.40 Additionally, right inferior phrenic artery enlargement is often observed in patients with cirrhosis. This finding is readily depicted on axial thin-section, three-dimensional (3D), contrast-enhanced, arterial-phase, dynamic MR images with fat suppression (Fig. 14). In cirrhotic patients, atrophy of the liver enlarges the space between the inferior vena cava and the crus of diaphragm, resulting in better delineation of the dilated right inferior phrenic artery within this space. One possible cause for the right inferior phrenic artery enlargement in cirrhotic patients is that the right inferior phrenic arterial flow may increase secondarily, along with hepatic arterial flow, to compensate for the decreased portal inflow in cirrhotic livers.
The association between gastrointestinal wall thickening and cirrhosis is well recognized. The cause of this is probably edema due to hypoproteinemia, portal hypertension, or a combination of both. One study reported that isolated or predominantly right-sided colonic wall thickening is seen in as many as 25% of patients with end-stage cirrhosis (Fig. 15). This is probably related to changes in blood flow and hydrostatic pressures caused by portal hypertension.16 Many of these patients do not have specific or focal bowel symptoms. Another study demonstrated specific patterns of gastrointestinal wall thickening in patients with cirrhosis: if the jejunum is normal, no wall thickening is seen in the duodenum or in the ileum; if the ascending colon is normal, no wall thickening is seen in the transverse or descending colon.24 Observation of atypical patterns of wall thickening in patients with cirrhosis should prompt a search for additional potential causes, including inflammatory, ischemic, and neoplastic diseases. Haustral thickening of the colon is also seen commonly in patients with cirrhosis, although nodular haustral thickening has been described as a specific feature of pseudomembranous colitis.
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Figure 15. Colonic wall thickening. T2-weighted FSE image shows wall thickening of the ascending colon.
Mesenteric, omental, and retroperitoneal edema occur often in patients with cirrhosis. The appearance of mesenteric edema varies from a mild infiltrative haze to a severe masslike sheath that engulfs the mesenteric vessels. Increasing severity, diffuse distribution, masslike appearance, and recruitment of omental and retroperitoneal sites are parameters of mesenteric edema severity and generally correlate with severe ascites, subcutaneous edema, and low serum albumin levels.5
PORTAL HYPERTENSION Although portal hypertension can result from obstruction at postsinusoidal, sinusoidal, or presinusoidal levels, the major cause of portal hypertension in cirrhosis is the intrahepatic sinusoidal type. During the early stages of portal hypertension, the portal system dilates but flow is maintained. Later, numerous portosystemic collateral pathways from the high-pressure portal system to the low-pressure systemic circulation may develop, reducing the volume of flow to the liver and decreasing the size of the portal vein. Major sites of portosystemic collateralization include the gastroesophageal junction (from the coronary and short gastric veins to the systemic esophageal vein), paraumbilical veins (from the left portal vein to the paraumbilical veins to the systemic epigastric veins),
retroperitoneal regions (from veins of the duodenum, ascending and descending colon, and liver to the systemic lumbar, phrenic, gonadal, and renal veins), gastro- or splenorenal regions (from the coronary, short gastric, and splenic veins to the systemic left renal vein), and hemorrhoidal veins (from the superior hemorrhoidal vein to the systemic middle and inferior hemorrhoidal veins).35 The most prevalent and clinically important portosystemic collaterals are the gastroesophageal varices because they are the most common source of upper gastrointestinal bleeding. Esophageal varices can be seen as enlarged, tortuous veins within the wall of the lower esophagus (Figs. 16 and 17). Three-
Figure 16. Esophageal varices. Gadolinium-enhanced GRE image demonstrates markedly enhanced varices within the esophageal wall (arrow).
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Figure 17. Paraesophageal varices. Gadolinium-enhanced GRE image demonstrates dilated paraesophageal varices around the aorta and the esophagus (arrow).
dimensional contrast-enhanced MR imaging provides excellent depiction of the portal venous system as high-intensity structures and enables continuous tracing of vascular structures (Fig. 18). Therefore, anatomic characteristics of these portosystemic collaterals can be depicted clearly. Esophageal varices are usually supplied by the anterior branch of the left gastric vein, which normally drains inferiorly toward the confluence of the splenic and superior mesenteric veins.39 In patients with esophageal varices, the flow in this vein reverses. The posterior branch of the left gastric vein supplies
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Figure 18. Massive paraesophageal varices. Reconstructed image with MPR technique from 3-D axial images clearly demonstrates the dilated coronary gastric vein and massive paraesophageal varices (arrow). (From Ito K, and Mitchell DG: MR imaging of cirrhosis and its complications. Contemporary Diagnostic Radiology 23:1–6, 2000; with permission.)
paraesophageal varices situated outside the wall of the esophagus in the mediastinum. The normal falciform ligament contains one to three tiny, collapsed paraumbilical veins. In patients with portal hypertension, the caliber of these vessels increases. The dilated paraumbilical veins arise from the left portal vein, traverse the falciform ligament, and drain into the veins of the anterior abdominal wall, sometimes producing a ‘‘Medusa’s head’’ appearance (Fig. 19). Paraumbilical ve-
Figure 19. Paraumbilical vein. A and B, Gadolinium-enhanced GRE images show the paraumbilical vein (arrows) originating from the left portal vein and passing anteriorly through the falciform ligament.
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Figure 20. Splenorenal shunt. A and B, These 3-D contrast-enhanced dynamic (portal phase) axial MR images with fat suppression show the enlarged splenic vein and the dilated tortuous collateral vessels (arrowhead) around the left kidney, running toward the left renal vein (arrow).
nous collaterals have been reported to develop in 10% to 43% of patients with portal hypertension. 4, 28, 30 The paraumbilical vein can become quite large and can function as a desirable route of natural decompression without gastrointestinal bleeding in portal hypertension. A splenorenal or gastrorenal shunt often occurs through an enlarged, left-sided retroperitoneal channel. These shunts may arise
from preexisting, small, normal portosystemic communications (Figs. 20 through 22). Splenorenal shunts typically originate from the splenic hilum, course medial to the enlarged spleen toward the left renal hilum, and anastomose with the left renal vein. The dilated, tortuous vessels between the hila of the spleen and left kidney on MR angiography represent a splenorenal shunt. Fusiform dilatation of the left renal vein is seen frequently.
Figure 21. Right-sided splenorenal shunt. A and B, These 3-D contrast-enhanced dynamic (portalphase) axial MR images with fat suppression show the dilated tortuous collateral vessels around the right kidney originating from the confluence of the superior mesenteric vein and the splenic vein, coursing toward the right side, and finally running into the right renal vein.
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Figure 22. Mesenteric varices. A–C, These 3-D contrast-enhanced dynamic (portal-phase) axial MR images with fat suppression show dilated vascular structures (arrow), running toward the inferior vena cava (IVC), representing mesenteric varices.
COMPLICATIONS AFTER LIVER TRANSPLANTATION Liver transplantation has become the treatment of choice for end-stage liver disease in appropriate candidates. Even with improvements in surgical technique and immunosuppression, however, there are still several significant complications. MR imaging is an outstanding method for comprehensive evaluation of complications after liver transplantation. With one examination, abnormalities of vascular structures, bile ducts, and liver parenchyma can be detected readily.23
or the intersegmental fissure of the transplanted liver are commonly seen within the first few days of transplantation. Lymph nodes are often identified in the porta hepatis and portacaval space and are usually reactive (Fig. 23). Periportal high intensity on T2weighted images is seen with greater frequency in patients with a shorter interval after transplantation (Fig. 24); this persists for several weeks. This may be caused by dilated lymphatics resulting from impaired drainage after surgery. Periportal high intensity does not correlate with acute allograft rejection.27
Common Expected Findings After Transplantation
Vascular Complications
A small amount of ascites, fluid, small seromas, or hematomas in the perihepatic region
Hepatic artery thrombosis is the most common vascular complication, occurring in up
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Figure 23. Lymph nodes enlargement after liver transplantation. T2-weighted FSE image shows reactive lymph nodes enlargement in the porta hepatis (arrows).
to 12% of adult transplant patients. Reported risk factors include increased cold ischemia time of the donor liver, severe acute rejection, ABO blood type incompatibility, and incongruence of the joined vessels.29 After transplantation, the bile duct is entirely dependent on hepatic arterial blood supply, and occlusion of the hepatic artery leads to bile duct ischemia and necrosis. Contrast-enhanced 3D MR angiography is a useful and noninvasive method for evaluating hepatic artery patency, with accuracy similar to that of ultrasound (Fig. 25).37 Portal vein stenosis or thrombosis is an un-
Figure 24. Periportal abnormal intensity. T2-weighted FSE image shows diffuse periportal abnormal high intensity seen as periportal tramline (arrow).
common complication after transplantation. Portal vein stenosis usually occurs at the anastomosis. Symptoms may include portal hypertension, hepatic failure, massive ascites,
Figure 25. Hepatic artery thrombosis. Maximum intensity projection (MIP) image from 3-D contrast-enhanced MR angiography shows proximal thrombosis of hepatic artery (arrow). Note lack of opacification of distal branches. Gastroduodenal artery and the superior mesenteric artery are normal. (From Ito K, Siegelman ES, Stolpen AH et al: MR imaging of complications after liver transplantation. AJR 175:1145–1149, 2000; with permission.)
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Figure 26. Portal vein thrombosis. MIP image from 3-D contrast-enhanced MR angiography demonstrates narrowing of the portal vein (arrow) caused by intraluminal thrombosis.
or edema. Contrast-enhanced MR angiography can show obvious narrowing or intraluminal thrombosis (Fig. 26).37 Inferior vena cava (IVC) thrombosis is rare, occurring in less than 3% of transplants and resulting from technical problems or compression of the vessels by a fluid collection.2 Flow-sensitive GRE MR imaging (i.e., timeof-flight or phase-contrast) can also be used to evaluate vascular complications. IVC
thrombus is depicted as an intraluminal defect (Fig. 27).
Biliary Tract Complications Most biliary strictures occur at the anastomotic site and may be caused by scar formation that results in retraction and narrowing. MR cholangiography can be used to screen
Figure 27. IVC thrombosis. A, T1-weighted SE image shows intermediate signal intensity within the IVC (arrow). B, Flow-sensitive GRE image shows signal defects within IVC (arrow), indicating the presence of thrombus. IVC is not completely obstructed.
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Figure 28. Mucocele of cystic duct remnant. T2-weighted coronal single-shot FSE image shows dilated cystic duct remnant (arrow) adjacent to common bile duct. (From Ito K, Siegelman ES, Stolpen AH et al: MR imaging of complications after liver transplantation. AJR 175:1145–1149, 2000; with permission.)
for biliary strictures.13 Bile leakage may occur, sometimes associated with biliary strictures. Leaks at the biliary anastomosis are the most common types, but bile leak may be caused by bile duct necrosis in patients with hepatic artery occlusion, producing bilomas or bile peritonitis. Mucocele of the cystic duct remnant is an uncommon complication that occurs when the donor cystic duct remnant becomes distended with mucus. It manifests a focal fluid collection adjacent to the hepatic duct. MR imaging can help distinguish between hematomas and other fluid collections in hepatic allograft recipients (Fig. 28).
Extrahepatic Complications Right adrenal gland hemorrhage is a complication after liver transplantation.3 Hemorrhage may be caused by (1) venous engorgement due to right adrenal vein ligation during removal of a portion of the IVC at transplantation or (2) coagulopathy secondary to the patient’s preexisting liver dysfunction. Adrenal hematoma is seen as a suprarenal mass on MR images. MR imaging is highly sensitive to hemorrhage because of its specific
Hepatic Parenchymal Complications Hepatic arterial insufficiency caused by thrombosis may induce bile duct necrosis, which may lead to bilomas, abscesses, or hepatic infarctions. Although the differentiation between biloma and abscess is often difficult, abscesses tend to have irregular, thick walls (Fig. 29). Hepatic infarctions are seen commonly as peripheral or central lesions with wedge-shaped or round appearances, without enhancement on contrast-enhanced MR images (Fig. 30).
Figure 29. Hepatic abscess. Gadolinium-enhanced GRE image shows a massive lesion with enhanced thick wall and septa (arrow) in the right hepatic lobe. The diagnosis of abscess was confirmed by percutaneous drainage.
CIRRHOSIS: MR IMAGING FEATURES
Figure 30. Hepatic infarctions. Gadolinium-enhanced GRE image shows multiple unenhanced areas with nontumorous configuration (arrows) in the liver, indicating hepatic infarctions secondary to hepatic artery thrombosis. Liver infarction was pathologically confirmed by second transplantation.
high signal with heterogeneity on both T1and T2-weighted images (Fig. 31). Post-transplant lymphoproliferative disorder (PTLD) is a lymphocyte proliferative process that occurs in transplant recipients whose immune systems are compromised. PTLD is strongly associated with infection with Epstein-Barr virus, inducing B-lymphocyte proliferation.38 PTLD may involve any organ in the body, but the lymph nodes, lungs, and gastrointestinal tract are involved most often.34 PTLD is varied in presentation, ranging
Figure 31. Adrenal hemorrhage. Opposed-phase T1weighted GRE image depicts right adrenal hematoma that shows peripheral high signal intensity with central low signal (arrow).
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Figure 32. Post-transplant lymphoproliferative disorder. Gadolinium-enhanced GRE image shows a mass with rim enhancement (arrow) near the liver. Pathologic diagnosis of lymphoma was confirmed by biopsy. (From Ito K, Siegelman ES, Stolpen AH et al: MR imaging of complications after liver transplantation. AJR 175:1145–1149, 2000; with permission.)
from a benign illness resembling mononucleosis to a fulminant lymphoma similar to an aggressive non-Hodgkin’s lymphoma (Fig. 32).
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