DOI: 10.1148/rg.255045180
RadioGraphics 2005;25:1299-1320
© RSNA, 2005
Focal Hepatic Lesions: Diagnostic Value of Enhancement Pattern Approach with Contrast-enhanced 3D Gradient-Echo MR Imaging1
Khaled M. Elsayes, MD2,
Vamsidhar R. Narra, MD,
Yuming Yin, MD,
Govind Mukundan, MD,
Markus Lammle, MD and
Jeffrey J. Brown, MD
1 From the Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 S Kingshighway Blvd, St Louis, MO 63110. Presented as an education exhibit at the 2003 RSNA Annual Meeting. Received September 8, 2004; revision requested September 30; final revision received February 22, 2005; accepted March 1. J.J.B. is a consultant to GE Healthcare and Tyco/Mallinckrodt; all remaining authors have no financial relationships to disclose.
Address correspondence to K.M.E. (e-mail: elsayesk{at}mir.wustl.edu).
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Abstract
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Focal hepatic lesions constitute a daily challenge in the clinical setting. However, noninvasive methods can be useful in the detection and characterization of these lesions. The noninvasive diagnosis of liver lesions is usually achieved with contrast material–enhanced computed tomography and magnetic resonance (MR) imaging. Dynamic three-dimensional gradient-recalled-echo MR imaging provides dynamic contrast-enhanced thin-section images with fat saturation and a high signal-to-noise ratio and is excellent for the evaluation of various focal hepatic lesions. A comprehensive MR imaging examination in this setting includes T2-weighted and chemical shift T1-weighted imaging and demonstrates characteristic enhancement patterns that can be helpful in the diagnosis of most of these lesions. These enhancement patterns are seen during particular phases of contrast-enhanced imaging and include arterial phase enhancement, delayed phase enhancement, peripheral washout, ring enhancement, nodule-within-a-nodule enhancement, true central scar, pseudocentral scar, and pseudocapsule. Familiarity with these enhancement patterns can help in the identification of specific focal lesions of the liver.
© RSNA, 2005
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LEARNING OBJECTIVES FOR TEST 5
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After reading this article and taking the test, the reader will be able to:
- Describe contrast-enhanced 3D gradient-echo MR imaging technique in the diagnosis of focal hepatic lesions.
- Identify the various enhancement patterns of focal hepatic lesions seen with this modality.
- Discuss the value of contrast-enhanced 3D gradient-echo MR imaging in the diagnosis of these lesions.
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Introduction
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The detection and characterization of focal hepatic lesions continues to be a challenge. Magnetic resonance (MR) imaging plays an important role in the evaluation of a wide range of benign and malignant focal hepatic lesions. The use of three-dimensional (3D) gradient-recalled-echo (GRE) sequences such as volumetric interpolated breath-hold examination (VIBE) has improved MR imaging by providing dynamic contrast material–enhanced thin-section images with fat saturation and a high signal-to-noise ratio (1).
Contrast-enhanced 3D GRE MR imaging demonstrates characteristic enhancement patterns that can be helpful in the diagnosis of various focal hepatic lesions. These enhancement patterns are seen during specific phases of imaging and include arterial phase enhancement, delayed phase enhancement, peripheral washout, ring enhancement, nodule-within-a-nodule enhancement, true central scar, pseudocentral scar, and pseudocapsule. In this article, we discuss and illustrate the use of contrast-enhanced 3D GRE MR imaging in the detection and characterization of focal lesions of the liver.
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Imaging Technique
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The pulse sequences used for MR imaging of the liver are similar to those used for standard abdominal MR imaging. Our standard protocol consists of (a) coronal T2-weighted half-Fourier acquisition of single-shot turbo spin-echo images, (b) axial turbo (fast) spin-echo T2-weighted or long-echo-time inversion recovery (IR) images obtained during a single breath hold, and (c) axial in-phase and out-of-phase chemical shift GRE T1-weighted images obtained during a single breath hold.
Three-dimensional GRE breath-hold sequences such as VIBE are used to obtain unenhanced and dynamic gadolinium-enhanced images. VIBE is usually performed with the following parameters: repetition time, 4–6 msec; echo time, 1–2 msec; flip angle, 12°; section thickness, 3–4 mm with zero interpolation, yielding an effective section thickness of 1.5–2 mm; matrix, 320 x 160; and breath hold, 24–28 seconds.
Three-dimensional GRE imaging has several advantages over two-dimensional dynamic imaging (1,2): (a) 3D images can be reformatted in any plane, (b) high-quality thin-section images with no gaps can be obtained, and (c) the detection and localization of small focal hepatic lesions is superior (Fig 1). In addition, the same data set can be used to generate high-quality images depicting the vasculature (Fig 1b).
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Figure 1a. Hepatocellular carcinoma (HCC) in a 63-year-old man with liver cirrhosis. Axial (a) and coronal (b) arterial phase 3D GRE VIBE MR images show an enhancing focus of HCC (arrow). Note the accurate depiction of the vascular relationship on the coronal image.
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Figure 1b. Hepatocellular carcinoma (HCC) in a 63-year-old man with liver cirrhosis. Axial (a) and coronal (b) arterial phase 3D GRE VIBE MR images show an enhancing focus of HCC (arrow). Note the accurate depiction of the vascular relationship on the coronal image.
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Benign Hypoenhancing Lesions
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Hepatic Cysts
Hepatic cysts are among the most common liver lesions. Hepatic cysts appear markedly hypointense on T1-weighted MR images and markedly hyperintense on T2-weighted images (Fig 2). They demonstrate no internal enhancement on contrast-enhanced images (Fig 2–4). The cyst wall is very thin or even imperceptible. Hepatic cysts have well-defined margins and are usually oval or round. The presence of thick walls or enhancing internal components suggests the diagnosis of hepatic abscess or neoplasm rather than a simple cyst.
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Figure 2. Simple hepatic cyst. Axial contrast-enhanced 3D GRE T1-weighted VIBE MR image shows a simple cyst (arrow) with the typical features of nonenhancement and low signal intensity. The diagnosis was confirmed at 18-month follow-up in combination with these typical imaging features.
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Figure 3. Hepatic cysts in a patient with Caroli disease. Axial contrast-enhanced 3D VIBE MR image shows cystic dilatation of the biliary ducts manifesting as multiple small, nonenhancing cysts. Note the presence of the "central dot sign" (arrow).
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Figure 4. Hepatic cysts in a patient with adult polycystic kidney disease. Axial contrast-enhanced 3D GRE T1-weighted VIBE MR image shows multiple cysts involving the liver and both kidneys. Note that some of the cysts are hemorrhagic.
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Simple Hepatic Cyst.—
Simple hepatic cysts are benign developmental lesions that do not communicate with the biliary tree (Fig 2) (3,4). The current theory is that true hepatic cysts originate from hamartomatous tissue (3,4). Simple hepatic cysts are common and are presumed to be present in 2.5% of the population (5). They are more common in women, and their prevalence increases with patient age. Simple hepatic cysts are almost always asymptomatic (3–5).
Caroli Disease.—
Caroli disease is a rare condition characterized by congenital cystic dilatation of the intrahepatic bile ducts (6). Although Caroli disease generally involves the entire liver, it may be segmental or lobar. Its inheritance is autosomal recessive. Two forms of Caroli disease have been described: (a) a less common "pure" form (type 1) and (b) a more complex form (type 2) that is associated with other ductal plate abnormalities such as hepatic fibrosis (5,7). Patients suffer from bouts of recurrent fever and pain. Jaundice occurs when a stone blocks the common bile duct (8). Several imaging modalities have been used to study this disease, including ultrasonography, computed tomography, and hepatobiliary scintigraphy, but only endoscopic retrograde cholangiopancreatography and direct cholangiography have proved to allow accurate diagnosis. However, these latter two modalities are invasive and may produce serious complications. MR cholangiopancreatography is a noninvasive imaging technique that has become the first-choice modality for diagnosing Caroli disease (9–11). MR imaging allows visualization of multiple small, nonenhancing cysts and demonstrates the connection of these cysts to the biliary ducts (Fig 3). The central dot sign is created by tiny contrast-enhanced dots within the dilated intrahepatic bile ducts and is considered to be strongly suggestive of Caroli disease (Fig 3) (4).
Autosomal Dominant Polycystic Kidney Disease.—
A wide spectrum of hepatic and renal involvement may be seen in patients with autosomal dominant polycystic kidney disease. Although hepatic cysts are found in 40% of cases of autosomal dominant polycystic disease involving the kidneys (Fig 4), they may be seen without identifiable renal involvement at imaging (12). Patients with autosomal dominant polycystic liver disease are usually asymptomatic, with liver dysfunction occurring only sporadically (3). However, advanced disease can result in hepatomegaly, liver failure, or Budd-Chiari syndrome. Polycystic liver disease patients with symptoms refractory to other treatments or with symptomatic hepatic cystic disease and end-stage renal cystic disease may be considered for liver or combined liver-kidney transplantation (13).
At MR imaging, hepatic cysts in polycystic liver disease have very high signal intensity on T2-weighted images and low signal intensity on T1-weighted images and do not enhance after the administration of gadolinium-based contrast material. Because of the large number of cysts, signal intensity changes indicating intracystic hemorrhage are more frequently encountered than in cases of simple hepatic cysts (5).
Regenerating and Dysplastic Nodules
Accurate characterization of the various nodular lesions that occur in the liver, particularly the cirrhotic liver, is important for appropriate patient treatment. The majority of HCCs are believed to arise as a regenerating nodule and progress to a low-grade dysplastic nodule, then to a high-grade dysplastic nodule, and eventually to an HCC.
Regenerating Nodules.—
In patients with cirrhosis, regenerating nodules form as a result of distorted liver architecture and heterogeneous regeneration. Regenerating nodules are seen as low-signal-intensity areas on both T1- and T2-weighted MR images (Fig 5), with minimal enhancement after contrast material administration (14).
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Figure 5a. Regenerating nodules. Axial IR T2-weighted (a) and contrast-enhanced 3D GRE T1-weighted VIBE (b) MR images show multiple small (<5-mm) focal lesions representing regenerating nodules. The lesions exhibit low signal intensity on both images and no enhancement after contrast material injection.
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Figure 5b. Regenerating nodules. Axial IR T2-weighted (a) and contrast-enhanced 3D GRE T1-weighted VIBE (b) MR images show multiple small (<5-mm) focal lesions representing regenerating nodules. The lesions exhibit low signal intensity on both images and no enhancement after contrast material injection.
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Dysplastic Nodules.—
A dysplastic nodule is defined as a small cluster of hepatocytes with dysplasia indicating the presence of nuclear and cytoplasmic changes but without definite histologic criteria for malignancy. Thus, dysplastic nodules are considered premalignant. Dysplastic foci are common in cirrhosis and uncommon in the non-cirrhotic liver. The distinction between dysplastic nodules and small HCCs is of major clinical importance. Early detection of HCC and the differentiation of this neoplasm from a dysplastic nodule are critical because the treatment of HCC is most effective when the tumor is small (14–16).
In addition, the diagnosis of one or more HCCs in a patient with cirrhosis may affect prioritization for liver transplantation. Although dysplastic nodules have a variable MR imaging appearance, they are generally hypointense or, more commonly, hyperintense on T1-weighted images and iso- or hypointense on T2-weighted images, without prominent arterial phase enhancement after contrast material administration (Fig 6) (14). Dysplastic nodules are almost never hyperintense on T2-weighted images, an important feature that can be helpful in distinguishing a dysplastic nodule from HCC at unenhanced MR imaging (14,17,18).
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Figure 6a. Dysplastic nodules. Axial unenhanced (a) and contrast-enhanced (b) 3D GRE T1-weighted VIBE MR images show multiple small focal lesions representing dysplastic nodules. The lesions exhibit high signal intensity on both images and no enhancement after contrast material administration. On axial T2-weighted images (not shown), the lesions demonstrated low signal intensity.
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Figure 6b. Dysplastic nodules. Axial unenhanced (a) and contrast-enhanced (b) 3D GRE T1-weighted VIBE MR images show multiple small focal lesions representing dysplastic nodules. The lesions exhibit high signal intensity on both images and no enhancement after contrast material administration. On axial T2-weighted images (not shown), the lesions demonstrated low signal intensity.
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Because the main blood supply to dysplastic nodules is from the portal venous system and that to HCC is from the hepatic arterial system (19), HCC can often be distinguished from a dysplastic nodule at dynamic gadolinium-enhanced MR imaging on the basis of identification of hepatic arterial phase enhancement (20). Dysplastic nodules generally do not enhance during the hepatic arterial phase.
Lipoma
Lipoma is not commonly seen in the liver. Hepatic lipomas have high signal intensity on non-fat-suppressed T1-weighted MR images and low signal intensity on fat-suppressed T1-weighted images, with no enhancement after gadolinium chelate administration (Fig 7) (21).
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Figure 7a. Lipoma. Axial in-phase T1-weighted (a) and contrast-enhanced 3D GRE T1-weighted VIBE (b) MR images show lipoma with the typical features of high signal intensity on the non-fat-suppressed image (arrow in a) and low signal intensity with no enhancement on the fat-suppressed (VIBE sequence) image (arrow in b).
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Figure 7b. Lipoma. Axial in-phase T1-weighted (a) and contrast-enhanced 3D GRE T1-weighted VIBE (b) MR images show lipoma with the typical features of high signal intensity on the non-fat-suppressed image (arrow in a) and low signal intensity with no enhancement on the fat-suppressed (VIBE sequence) image (arrow in b).
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Bile Duct Hamartoma
Bile duct hamartomas, also called von Meyenburg complexes, are uncommon benign biliary malformations. These lesions may be solitary or multiple. They are asymptomatic and are typically discovered incidentally at imaging studies, surgery, or autopsy. Bile duct hamartomas are usually less than 1 cm in diameter and are often numerous when identified on radiologic images (22).
At MR imaging, bile duct hamartomas are small (<1-cm), well-defined lesions, have low T1 signal intensity and high T2 signal intensity (23,24), and demonstrate no internal enhancement on contrast-enhanced images (Fig 8). A thin, enhancing rim representing the surrounding liver parenchyma can sometimes be seen on both immediate and delayed phase contrast-enhanced images (22).
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Figure 8a. Biliary hamartoma. Coronal MR cholangiopancreaticogram (a) and axial contrast-enhanced VIBE MR image (b) show multiple lesions (arrows in b) representing biliary hamartomas. The lesions demonstrate low T1 and high T2 signal intensity and a thin rim of enhancement.
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Figure 8b. Biliary hamartoma. Coronal MR cholangiopancreaticogram (a) and axial contrast-enhanced VIBE MR image (b) show multiple lesions (arrows in b) representing biliary hamartomas. The lesions demonstrate low T1 and high T2 signal intensity and a thin rim of enhancement.
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Malignant Hypoenhancing Lesions
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Metastatic disease is the most common cause of malignant liver lesions in the United States (25). After regional lymph nodes, the liver is the most common site for metastasis. In autopsy series of patients who had primary tumors, liver metastases are seen in 50% of cases (26). Detection and characterization of liver metastases in patients with primary tumors is very important because these patients may have benign lesions that must be differentiated from metastases to avoid unnecessary further diagnostic work-up or errors in patient staging (25). Hepatic metastases can be classified according to their enhancement pattern into two categories: hypovascular and hypervascular.
Hypovascular Metastases
Colon, lung, prostate, gastric, and transitional cell carcinomas are the most common primary tumors with hypovascular metastases to the liver. These metastatic lesions usually demonstrate low signal intensity on T1-weighted MR images and are iso-to hyperintense on T2-weighted images, with delayed enhancement on contrast-enhanced images (Fig 9). Occasionally, they show early ring enhancement (26–30).
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Figure 9. Hypovascular metastases in a 59-year-old patient with colon cancer. Early phase contrast-enhanced 3D GRE T1-weighted VIBE MR image shows hypovascular metastases with low signal intensity and no enhancement (arrow). Progressive enhancement was seen on delayed phase images (not shown).
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Lymphoma
Lymphomatous involvement of the liver can be primary or secondary. Primary hepatic lymphoma is rare. Secondary involvement of the liver can occur in up to 50% of patients with non-Hodgkin lymphoma and 20% of patients with Hodgkin lymphoma (31–33). Lymphomatous lesions usually have low signal intensity on T1-weighted MR images and variable signal intensity on T2-weighted images. They usually enhance minimally just after gadolinium chelate administration (34,35) and may show faint peripheral rim enhancement on subsequent images (Fig 10) (36). The variable signal intensity on T2-weighted images is associated with a similar pattern of variable contrast enhancement (36).
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Figure 10. Lymphoma. Axial contrast-enhanced 3D GRE T1-weighted VIBE MR image demonstrates two small, well-defined hepatic lymphomatous deposits with faint marginal enhancement (arrows). Marked central biliary dilatation is also noted.
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Inflammatory Lesions
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Sarcoidosis
Sarcoidosis is a granulomatous systemic disease of unknown cause that can involve numerous sites, including the liver. Liver involvement by sarcoidosis can be documented at biopsy in 24%–94% of patients (37–39). At MR imaging, the lesions are hypointense with all pulse sequences and hypoenhancing relative to the background liver. The lesions are most conspicuous on fat-saturated T2-weighted images and early phase gadolinium-enhanced T1-weighted images (Fig 11). Sarcoid lesions usually enhance minimally on delayed phase contrast-enhanced images (37,40,41).
Histoplasmosis
Although histoplasmosis may be seen in patients with competent immune systems, it is more prevalent in immunocompromised patients. During the acute and subacute phases of histoplasmosis, scattered hypointense lesions may be seen on both T1- and T2-weighted MR images, with no significant enhancement after contrast material administration (Fig 12) (42–44). Focal calcification typically occurs during the chronic stage of histoplasmosis but is usually difficult to discern on MR images (45).
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Figure 12. Histoplasmosis. Axial contrast-enhanced 3D GRE T1-weighted VIBE MR image shows non-enhancing hypointense lesions secondary to histoplasmosis. Note the enhancing areas surrounding these nonenhancing foci. Splenic involvement is also seen.
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Miscellaneous Lesions
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Focal Fat
Focal fat deposition or focal sparing can mimic a focal hepatic mass. Areas of abnormal fat deposition within the liver show a characteristic signal loss on opposed phase images (Fig 13) (46). Although gadolinium enhancement is not critical for making the correct diagnosis, the presence of normally enhancing liver parenchyma within areas of altered fat deposition or focal sparing helps confirm the diagnosis (47).
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Figure 13a. Focal fat deposition. Axial in-phase (a), out-of-phase (b), and contrast-enhanced 3D GRE VIBE (c) T1-weighted MR images show multiple lesions, with typical signal dropout on the out-of-phase image compared with the in-phase image. Note also the presence of normally enhancing liver parenchyma within areas of altered fat deposition.
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Figure 13b. Focal fat deposition. Axial in-phase (a), out-of-phase (b), and contrast-enhanced 3D GRE VIBE (c) T1-weighted MR images show multiple lesions, with typical signal dropout on the out-of-phase image compared with the in-phase image. Note also the presence of normally enhancing liver parenchyma within areas of altered fat deposition.
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Figure 13c. Focal fat deposition. Axial in-phase (a), out-of-phase (b), and contrast-enhanced 3D GRE VIBE (c) T1-weighted MR images show multiple lesions, with typical signal dropout on the out-of-phase image compared with the in-phase image. Note also the presence of normally enhancing liver parenchyma within areas of altered fat deposition.
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Confluent Hepatic Fibrosis
Fibrosis can occur diffusely or focally in the setting of cirrhosis. Focal disease is usually located in the anterior and medial segments of the liver and has a wedge-shaped appearance, but in some patients the entire segment is involved (48). Fibrosis can appear as an area of low signal intensity on T1-weighted MR images and high signal intensity on T2-weighted images. It usually demonstrates delayed enhancement on contrast-enhanced images. Retraction of the overlying liver capsule (Fig 14) and a typical geographic pattern of involvement can be helpful in diagnosing this condition and in distinguishing it from HCC (48,49).
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Figure 14a. Confluent hepatic fibrosis. Axial IR T2-weighted (a), non-fat-suppressed T1-weighted (b), and contrast-enhanced 3D GRE T1-weighted VIBE (c) MR images show a large, heterogeneous area of confluent hepatic fibrosis. The lesion exhibits low T1 signal intensity and high T2 signal intensity, with no significant early contrast enhancement. Retraction of the capsular surface is also noted (arrow in b).
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Figure 14b. Confluent hepatic fibrosis. Axial IR T2-weighted (a), non-fat-suppressed T1-weighted (b), and contrast-enhanced 3D GRE T1-weighted VIBE (c) MR images show a large, heterogeneous area of confluent hepatic fibrosis. The lesion exhibits low T1 signal intensity and high T2 signal intensity, with no significant early contrast enhancement. Retraction of the capsular surface is also noted (arrow in b).
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Figure 14c. Confluent hepatic fibrosis. Axial IR T2-weighted (a), non-fat-suppressed T1-weighted (b), and contrast-enhanced 3D GRE T1-weighted VIBE (c) MR images show a large, heterogeneous area of confluent hepatic fibrosis. The lesion exhibits low T1 signal intensity and high T2 signal intensity, with no significant early contrast enhancement. Retraction of the capsular surface is also noted (arrow in b).
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Benign Arterial Phase–enhancing Lesions
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Hepatic adenoma is a focal benign proliferation of hepatocytes within an otherwise normal liver. These lesions most often occur in young women who have used oral contraceptives. In some cases, the lesions regress after oral contraceptives are discontinued. The unenhanced MR imaging appearance of hepatic adenomas ranges from mildly hypointense to hyperintense on T1-weighted images. The high signal intensity is due to the presence of fat or blood products. On T2-weighted images, hepatic adenomas have a nonspecific, heterogeneous, slightly hyperintense appearance. Immediate enhancement is seen on arterial phase images after intravenous gadolinium chelate administration but rapidly fades to near isointensity on subsequent images (Fig 15) (14,50).
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Figure 15. Hepatic adenoma. Axial arterial phase contrast-enhanced VIBE MR image demonstrates an adenoma (white arrow) with typical immediate enhancement. Note also the focal area of hemorrhage (black arrow). Fading of the enhancement was seen on subsequent images (not shown).
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Malignant Arterial Phase–enhancing Lesions
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Hepatocellular Carcinoma
HCC is the most common primary malignant hepatic neoplasm. Underlying cirrhosis from alcoholism, hepatitis (B and C), and toxin exposure are the predominant causal factors. Standard liver function tests are not helpful in the diagnosis of HCC, particularly in cirrhotic patients. The serum 
-fetoprotein level is usually elevated in patients with HCC (51). On T1-weighted MR images, HCC is most often hypointense relative to the liver, although hyperintense lesions or areas of hyperintensity within hypointense lesions may be seen. These hyperintense regions within the HCC reflect the presence of fat, copper, protein, or blood secondary to intralesional hemorrhage. On T2-weighted images, HCC is generally hyperintense, although well-differentiated lesions that are isointense relative to the liver parenchyma may be seen. Most HCCs show intense enhancement on arterial phase contrast-enhanced images (Fig 1) (14,52). It is important to recognize HCC while it is still small because the tumor is aggressive and has a fast doubling time (53). Small HCCs may also appear as small foci that are slightly hyperintense relative to the surrounding liver on T2-weighted MR images. On T1-weighted images, such areas may be isointense, hypointense, or hyperintense relative to the liver. On arterial phase dynamic gadolinium-enhanced images, most small HCCs show intense enhancement (14).
A large HCC may have a number of characteristic features, such as a mosaic pattern, a tumor capsule, extracapsular extension with formation of satellite nodules, vascular invasion, and extrahepatic dissemination, including lymph node and distant metastases (53). The mosaic pattern is created by confluent small nodules separated by thin septa and necrotic areas within the tumor. This pattern is more often depicted on T2-weighted MR images than on T1-weighted images. On both T1- and T2-weighted images, the mosaic pattern appears as areas of variable signal intensity, whereas on gadolinium-enhanced images, the lesions enhance in a heterogeneous pattern during the arterial phase and subsequent phases (14,54).
Hypervascular Metastases
Islet cell tumors, breast cancer, melanoma, thyroid cancer, and carcinoid tumor are among the most common primary tumors that lead to hypervascular hepatic metastases. Hypervascular metastases are best seen during the arterial phase of enhancement (Fig 16). Most of these lesions have high signal intensity on T2-weighted MR images (29,55).
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Figure 16. Hypervascular metastases in a 55-year-old man with a carcinoid tumor. Axial early phase contrast-enhanced 3D GRE T1-weighted VIBE MR image shows multiple hypervascular metastases with marked enhancement (arrows). Delayed washout was seen on subsequent images (not shown).
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Transient Hepatic Intensity Difference
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Transient hepatic intensity difference (THID) is a phenomenon characterized by a patchy wedge-shaped area of enhancement involving a hepatic subsegment (Fig 17). This finding is seen transiently immediately after contrast material administration, with fading on subsequent images. The cause of THID is still unknown, but the phenomenon is thought to represent an imbalance between the hepatic arterial and portal venous supply to affected subsegments caused by increased hepatic arterial blood flow in the presence of portal vein obstruction (Fig 18) (56,57). Typically, transiently increased segmental perfusion enhancement indicates that the portal venous supply is compromised due to compression or thrombosis. Schlund et al (57) reported its occurrence with isolated right or left portal vein occlusion.
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Figure 17. THID. Axial contrast-enhanced 3D GRE T1-weighted VIBE MR image shows a hypoenhancing focal liver lesion involving the porta hepatis (arrow), with THID involving the left hepatic lobe as a result of invasion of the left portal vein branch. Biliary dilatation is also noted.
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Figure 18. Drawings illustrate the change from a normal vascular supply (left) to THID (right). Normal flow in the portal vein (PV) becomes markedly lighter in THID, whereas normal flow in the hepatic artery (HA) becomes markedly heavier.
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Hypervascular Lesions with Central Scar
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Focal Nodular Hyperplasia
Focal nodular hyperplasia (FNH) is the second most common benign liver lesion. FNH occurs most frequently in adult women, with a 2:1 female predilection. The lesion varies from mildly hypointense to isointense on T1-weighted MR images and from mildly hyperintense to isointense on T2-weighted images. Unlike in fibrolamellar HCC, the central scar in FNH is not a true scar, but represents a congeries of blood vessels, bile ducts, and sometimes a focal area of cirrhosis. This "central scar" is characteristically hyperintense on T2-weighted images. The mild hyperintensity of the lesion on T2-weighted images may be related to the presence of vascular channels or edema throughout the lesion. FNH is perfused by the hepatic arterial system and shows marked, nearly uniform arterial phase enhancement. The degree of lesion enhancement lessens on subsequent contrast-enhanced images, with lesion signal intensity approaching that of the surrounding liver parenchyma. The central scar has low signal intensity on early phase contrast-enhanced images but gradually enhances to become hyperintense relative to the rest of the lesion on delayed phase images (Fig 19) (58).
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Figure 19a. FNH. Axial IR T2-weighted MR image (a) and contrast-enhanced 3D T1-weighted VIBE MR images obtained during the arterial (b) and equilibrium (c) phases show the typical features of FNH: high T2 signal intensity with immediate lesion enhancement (arrow in a), poor enhancement of the central scar on the early phase image (arrow in b), and increased enhancement of the scar on the delayed phase image (arrow in c).
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Figure 19b. FNH. Axial IR T2-weighted MR image (a) and contrast-enhanced 3D T1-weighted VIBE MR images obtained during the arterial (b) and equilibrium (c) phases show the typical features of FNH: high T2 signal intensity with immediate lesion enhancement (arrow in a), poor enhancement of the central scar on the early phase image (arrow in b), and increased enhancement of the scar on the delayed phase image (arrow in c).
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Figure 19c. FNH. Axial IR T2-weighted MR image (a) and contrast-enhanced 3D T1-weighted VIBE MR images obtained during the arterial (b) and equilibrium (c) phases show the typical features of FNH: high T2 signal intensity with immediate lesion enhancement (arrow in a), poor enhancement of the central scar on the early phase image (arrow in b), and increased enhancement of the scar on the delayed phase image (arrow in c).
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Fibrolamellar HCC
Fibrolamellar HCC is an uncommon type of HCC. Fibrolamellar HCC is usually seen as a large, well-circumscribed focal lesion with low signal intensity on T1-weighted MR images and high signal intensity on T2-weighted images. There is usually early heterogeneous contrast enhancement, which fades on subsequent images. A central radiating scar is seen in 80% of cases and has low signal intensity on T2-weighted images (Fig 20), with minimal or no enhancement on contrast-enhanced images (59). As a result, the scar is usually hypointense relative to the remainder of the tumor.
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Figure 20a. Fibrolamellar HCC. (a) Axial IR T2-weighted MR image demonstrates a lesion containing a low-signal-intensity central scar (arrow). (b, c) On contrast-enhanced 3D GRE T1-weighted VIBE MR images, the lesion demonstrates immediate contrast enhancement during the arterial phase (b) that fades during the portal venous phase (c), with a nonenhancing central scar. The findings on all three images are typical of fibrolamellar HCC.
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Figure 20b. Fibrolamellar HCC. (a) Axial IR T2-weighted MR image demonstrates a lesion containing a low-signal-intensity central scar (arrow). (b, c) On contrast-enhanced 3D GRE T1-weighted VIBE MR images, the lesion demonstrates immediate contrast enhancement during the arterial phase (b) that fades during the portal venous phase (c), with a nonenhancing central scar. The findings on all three images are typical of fibrolamellar HCC.
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Figure 20c. Fibrolamellar HCC. (a) Axial IR T2-weighted MR image demonstrates a lesion containing a low-signal-intensity central scar (arrow). (b, c) On contrast-enhanced 3D GRE T1-weighted VIBE MR images, the lesion demonstrates immediate contrast enhancement during the arterial phase (b) that fades during the portal venous phase (c), with a nonenhancing central scar. The findings on all three images are typical of fibrolamellar HCC.
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FNH and hepatocellular adenoma should be differentiated from fibrolamellar HCC, since they may have imaging characteristics similar to those of fibrolamellar HCC. FNH and hepatocellular adenoma can be differentiated from fibrolamellar HCC on the basis of their enhancement pattern, which is usually homogeneous. Also, the central scar seen in FNH is characteristically hyperintense on T2-weighted MR images (unlike that seen in fibrolamellar HCC).
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Lesions with Other Enhancement Patterns
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Ring Enhancement
Liver Abscesses.—
About 20% of pyogenic liver abscesses are cryptogenic. The remaining 80% are secondary to diseases of the biliary tract (cholangitic), intraabdominal sepsis with spread of infection via the portal venous system (pylophlebitic), extraabdominal foci of suppuration with bacteria reaching the liver via its arterial supply, spread from contiguous infections in adjacent viscera or organs, or spread from penetrating or blunt abdominal trauma.
Abscesses usually have very low signal intensity on T1-weighted MR images and very high signal intensity on T2-weighted images. The presence of an enhancing capsule of variable thickness on contrast-enhanced images (Figs 21, 22) helps differentiate abscesses from simple hepatic cysts (42–44).
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Figure 21a. Pyogenic abscess. Axial IR T2-weighted (a) and contrast-enhanced 3D GRE T1-weighted VIBE (b) MR images show a pyogenic abscess with characteristic ring enhancement (arrow). Note the high T2 signal intensity of the lesion in a; this hyperintensity is exaggerated by iron deposition resulting from hemosiderosis.
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Figure 21b. Pyogenic abscess. Axial IR T2-weighted (a) and contrast-enhanced 3D GRE T1-weighted VIBE (b) MR images show a pyogenic abscess with characteristic ring enhancement (arrow). Note the high T2 signal intensity of the lesion in a; this hyperintensity is exaggerated by iron deposition resulting from hemosiderosis.
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Fungal hepatic abscesses are opportunistic infections that occur in immunocompromised patients, typically by means of hematogenous dissemination. Microabscesses often involve the liver and spleen and, occasionally, the kidneys. Candidal abscesses are usually seen as multiple small (<5-mm), ring-enhancing lesions (Fig 23 ) (42–44). At pretreatment MR imaging, the nodules appear as rounded lesions less than 1 cm in diameter, with minimal hypointensity on T1-weighted and gadolinium-enhanced images and marked hyperintensity on T2-weighted images. In the subacute stage following treatment, the lesions are mildly to moderately hyperintense on T1- and T2-weighted images and demonstrate enhancement on gadolinium-enhanced images. A dark ring is usually seen around these lesions with all sequences. Completely treated lesions are minimally hypointense on T1-weighted images, isointense to mildly hyperintense on T2-weighted images, moderately hypointense on early phase gadolinium-enhanced images, and minimally hypointense on delayed phase gadolinium-enhanced images (60).
Pseudocapsule.—
HCC lesions may have a pseudocapsule composed of compressed liver parenchyma. The pseudocapsule is typically hypointense on T1-weighted MR images and hyperintense on T2-weighted images, with delayed enhancement on contrast-enhanced images (Fig 24) (61).
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Figure 24. Pseudocapsule. Axial delayed phase contrast-enhanced 3D GRE T1-weighted MR image shows a tumor pseudocapsule (arrows) with the characteristic features of low signal intensity and conspicuous enhancement.
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Radiofrequency-ablated Areas.—
The coagulation necrosis resulting from radiofrequency ablation typically has intermediate to high signal intensity relative to the liver parenchyma on T1-weighted MR images and low signal intensity on T2-weighted images. A hyperintense rim around the ablation area may be seen at T2-weighted imaging, likely related to edema from thermal injury. Any discrete areas of hypointensity on T1-weighted images or hyperintensity on T2-weighted images should raise suspicion for residual or recurrent tumor. However, a recently ablated area may have heterogeneous signal intensity on both T1- and T2-weighted MR images owing to the nonuniform evolution of inflammation, hemorrhage, and necrosis (62), making the interpretation of unenhanced images difficult. Contrast-enhanced images are routinely used for follow-up after treatment with radiofrequency ablation, the ablated area being unenhanced except for a smooth, thin, enhanced rim representing peripheral hyperemia (Fig 25). Residual or recurrent tumor manifests as a noncircumferential nodular area of enhancement (62). This rim typically persists for approximately 3 months, after which the lesion enhancement and ring enhancement progressively decrease (62,63).
Nodule-within-a-Nodule Enhancement
Early HCC may have a nodule-within-a-nodule appearance on MR images. This appearance results when a focus of HCC originates within a dysplastic nodule but has not yet completely replaced the nodule. On T2-weighted MR images, this enhancement pattern appears as a focus of moderately high signal intensity within a low-signal-intensity nodule. The inner nodule appears hypointense on T1-weighted images and shows marked arterial phase enhancement on contrast-enhanced images (Fig 26) (64).
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Figure 26a. Nodule-within-a-nodule enhancement pattern. Axial unenhanced (a) and arterial phase contrast-enhanced (b) 3D GRE T1-weighted VIBE MR images show an area of HCC (arrowhead) arising within a dysplastic nodule (arrow).
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Figure 26b. Nodule-within-a-nodule enhancement pattern. Axial unenhanced (a) and arterial phase contrast-enhanced (b) 3D GRE T1-weighted VIBE MR images show an area of HCC (arrowhead) arising within a dysplastic nodule (arrow).
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Peripheral Washout Sign
The "peripheral washout sign" specifically indicates malignancy and has been described in some cases of hepatic metastases from carcinoid, breast, colon, and gastric cancers. This sign manifests as a peripheral rim that is hypointense relative to the center of the lesion (Fig 27) (65) and is best seen 10 minutes after the administration of contrast material.
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Figure 27a. Peripheral washout sign. Axial arterial phase (a) and delayed phase (b) contrast-enhanced 3D GRE T1-weighted VIBE MR images show a metastatic deposit from colon cancer. The lesion is hypoenhancing on the arterial phase image. On the delayed phase image, it has a peripheral rim (arrows) that is hypointense relative to the center of the lesion.
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Figure 27b. Peripheral washout sign. Axial arterial phase (a) and delayed phase (b) contrast-enhanced 3D GRE T1-weighted VIBE MR images show a metastatic deposit from colon cancer. The lesion is hypoenhancing on the arterial phase image. On the delayed phase image, it has a peripheral rim (arrows) that is hypointense relative to the center of the lesion.
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Rim Enhancement
Biliary Cystadenoma or Cystadenocarci-noma.—
Biliary cystadenoma or cystadenocarcinoma is a rare cystic biliary epithelial neoplasm. Cystadenomas are considered by many pathologists to be premalignant lesions. They have a propensity for local recurrence and are viewed on a continuum with cystadenocarcinomas. Cystadenomas are typically large and multilocular. Mucin content occasionally renders these tumors hyperintense on T1-weighted MR images. Cystadenomas typically demonstrate rim enhancement (Fig 28), with occasional enhancement of internal solid components (4).
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Figure 28. Cystadenoma. Axial contrast-enhanced 3D GRE T1-weighted MR image shows a multilocular cystic lesion (arrow) with an enhancing rim and septa, findings that represent a biliary cystadenoma.
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Hematoma.—
Liver hematoma demonstrates the MR imaging characteristics of blood and of the breakdown products of hemoglobin. Subacute hematomas are typically bright on T1-weighted MR images due to the T1 shortening effects of methemoglobin. Chronic hematomas are usually dark on T2-weighted images due to the presence of hemosiderin. Some hematomas show rim enhancement following contrast material administration (Fig 29) (31,66).
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Figure 29a. Hematoma in a 49-year-old woman who had sustained trauma. (a) Axial IR T2-weighted MR image shows a septated hematoma with high signal intensity. (b) On an axial contrast-enhanced 3D GRE T1-weighted MR image, the hematoma demonstrates rim enhancement (arrow).
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Figure 29b. Hematoma in a 49-year-old woman who had sustained trauma. (a) Axial IR T2-weighted MR image shows a septated hematoma with high signal intensity. (b) On an axial contrast-enhanced 3D GRE T1-weighted MR image, the hematoma demonstrates rim enhancement (arrow).
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Delayed Phase–enhancing Lesions
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Hemangioma
Hemangioma occurs in approximately 20% of the general adult population. Hemangiomas are usually hypointense on T1-weighted MR images and markedly hyperintense on T2-weighted images. On contrast-enhanced images, they demonstrate early peripheral nodular enhancement with progressive centripetal enhancement on subsequent images (Fig 30) (67).
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Figure 30a. Hemangioma. Axial portal venous phase (a) and delayed phase (b) contrast-enhanced 3D GRE T1-weighted MR images show a hepatic hemangioma with the typical findings of early peripheral nodular enhancement (arrow in a) and progressive centripetal filling (arrow in b). These findings helped confirm the diagnosis.
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Figure 30b. Hemangioma. Axial portal venous phase (a) and delayed phase (b) contrast-enhanced 3D GRE T1-weighted MR images show a hepatic hemangioma with the typical findings of early peripheral nodular enhancement (arrow in a) and progressive centripetal filling (arrow in b). These findings helped confirm the diagnosis.
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Intrahepatic Cholangiocarcinoma
Cholangiocarcinoma is the most common biliary tumor and the second most common primary malignant hepatic tumor in adults. The tumor can be classified as peripheral intrahepatic, hilar intrahepatic, or extrahepatic depending on its location. Intrahepatic cholangiocarcinoma is usually hypointense on T1-weighted MR images and hyperintense on T2-weighted images. On contrast-enhanced images, it demonstrates initial peripheral enhancement with concentric internal filling on delayed phase images (Fig 31) (68,69).
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Figure 31a. Intrahepatic cholangiocarcinoma in a 69-year-old man. (a) Axial arterial phase contrast-enhanced 3D GRE T1-weighted VIBE MR image shows a low-signal-intensity tumor area with faint peripheral enhancement. (b) On an axial delayed phase contrast-enhanced 3D GRE T1-weighted VIBE MR image, the tumor area demonstrates progressive filling (arrow).
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Figure 31b. Intrahepatic cholangiocarcinoma in a 69-year-old man. (a) Axial arterial phase contrast-enhanced 3D GRE T1-weighted VIBE MR image shows a low-signal-intensity tumor area with faint peripheral enhancement. (b) On an axial delayed phase contrast-enhanced 3D GRE T1-weighted VIBE MR image, the tumor area demonstrates progressive filling (arrow).
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Peliosis Hepatis
Peliosis hepatis is a rare disorder characterized by cystic hepatic sinusoidal dilatation and the presence of multiple small (1–3-mm), blood-filled lacunar spaces. This condition can be seen in patients with chronic wasting due to tuberculosis or cancer and is associated with the administration of a variety of drugs, including anabolic steroids and oral contraceptives (70,71). The appearance of these lesions on T1-weighted MR images is variable, ranging from hypointense to hyperintense due to hemorrhage. On T2-weighted images, the lesions typically demonstrate high signal intensity. These lesions usually have low signal intensity on arterial phase images, with accumulation of contrast material on portal venous and delayed phase images (Fig 32) (72,73).
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Figure 32a. Peliosis hepatis. Axial IR T2-weighted (a) and portal venous phase contrast-enhanced 3D GRE T1-weighted VIBE (b) MR images show multiple small, confluent cystic lesions. The lesions demonstrate enhancement on the portal venous phase image, a finding that represents peliosis hepatis.
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Figure 32b. Peliosis hepatis. Axial IR T2-weighted (a) and portal venous phase contrast-enhanced 3D GRE T1-weighted VIBE (b) MR images show multiple small, confluent cystic lesions. The lesions demonstrate enhancement on the portal venous phase image, a finding that represents peliosis hepatis.
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Conclusions
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Dynamic contrast-enhanced 3D GRE MR imaging is excellent for the evaluation of various focal hepatic lesions. A comprehensive MR imaging examination in this setting includes T2-weighted and chemical shift T1-weighted imaging and yields characteristic enhancement patterns that can be used to diagnose or at least narrow the differential diagnosis for most of these lesions.
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Footnotes
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Abbreviations: FNH = focal nodular hyperplasia, GRE = gradient-recalled-echo, HCC = hepatocellular carcinoma, IR = inversion recovery, THID = transient hepatic intensity difference, VIBE = volumetric interpolated breath-hold examination, 3D = three-dimensional
2 Current address: Department of Radiology, Theodore Bilharz Institute, Giza, Egypt. 
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K. J. Burkholz and A. C. Silva
AJR Teaching File: Hypervascular Metastasis or Hepatic Hemangioma?
Am. J. Roentgenol.,
June 1, 2008;
190(6_Supplement):
S53 - S56.
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S. D. Beaty, A. C. Silva, and G. DePetris
AJR Teaching File: Incidental Hepatic Mass
Am. J. Roentgenol.,
June 1, 2008;
190(6_Supplement):
S62 - S64.
[Full Text]
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Abstract
LEARNING OBJECTIVES FOR TEST...
