Magnetic Resonance Imaging of the Liver: Current Clinical Applications

Subspecialty Clinics: Radiology Magnetic Resonance Imaging of the Liver: Current Clinical Applications

C. DANIEL JOHNSON, M.D., Department ofDiagnostic Radiology

Magnetic resonance imaging provides excellent anatomic depiction of the liver and important information about focal and diffuse diseases that affect this organ. In this report, the current clinical applications of magnetic resonance imaging of the liver in patients with known or suspected hepatic metastatic lesions, hepatocellular carcinoma, cavernous hemangiomas, focal fatty infiltration, focal nodular hyperplasia, hepatic adenoma, regenerative nodules in hepatic cirrhosis, or iron overload are reviewed, and the limitations of the technique are discussed.

The clinical applications of magnetic resonance imaging (MRI) of the liver have slowly expanded during the past decade as technical advances have overcome problems associated with respiratory motion artifact and vascular artifact. Initially, MRI was used only for clinical problems that other conventional techniques, such as computed tomography (CT) and ultrasonography, had failed to resolve. Currently, MRI remains not only an important problem-solving technique but also the initial imaging test for the detection and characterization of various liver diseases. Herein the clinical applications of MRI of the liver at the Mayo Clinic are reviewed and the diseases that affect the liver focally or diffusely are discussed. TECHNIQUES A discussion of the various imaging techniques currently in use is beyond the scope of this article. Considerable resources and research have been devoted to exploring magnetic field strength, pulse sequence design, and magnetic resonance-specific contrast agents. In fact, a review of the radiologic literature published during the past few years shows that more articles have been focused on these fundaAddress reprint requests to Dr. C. D. Johnson, Department of Diagnostic Radiology, Mayo Clinic, Rochester, MN 55905. Mayo Clin Proc 1993; 68:147-156

mental technical issues of imaging than on the findings in a particular disease. Despite substantial effort, answers to many of the technical issues are unclear. Although most major medical centers have scanning systems with high field strength magnets, excellent clinical results can be obtained with low field strength (less than 0.5 T) and medium field strength (0.5 to 1 T) magnets.!" Systems with high field strength (more than 1 T) generate higher signal-to-noise values and hence have the' potential for faster scanning, higher spatial resolution, and thinner body slice sections than systems with low field strength. Unfortunately, motion artifact is also more of a problem at high field strengths, and modem equipment must routinely use several artifact-suppressing software techniques (gradient moment nulling, respiratory compensation, and spatial presaturationj.>" Pulse sequence design, particularly techniques that are fast and that can be used to obtain images during breath holding, is still under vigorous development."!' With these techniques, elimination of respiratory artifact has substantially improved image quality. Additionally, dynamic scanning during intravenous administration of a contrast agent is now possible. Generally, both TI- and T2-weighted images are necessary to evaluate the hepatic parenchyma. At the Mayo Clinic, radiologists use both 'I'l- and T2-weighted spin-echo sequences as well as a breath-holding technique (magnetiza147

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tion-prepared gradient echo) that was developed in the Mayo MRI research laboratory (Fig. 1) (Campeau NG, Johnson CD, Riederer SJ, Holsinger-Bampton AB, Ehman RL. Unpublished data)." On the basis of the clinical situation, additional sequences can be performed. Various contrast agents are being developed. Only gadolinium-based agents are widely available.P:" and my colleagues and I use them only in selected patients. Gadopentetic acid is a nonspecific intravascular agent that closely mimics the behavior of iodinated contrast material. Results of preliminary studies of new tissue-specific contrast agents are promising. These new agents have the potential for superior detection and characterization of lesions.'>"

FOCAL LIVER DISEASES Metastatic Involvement.-Most early investigations of MRI of focal liver lesions compared CT and MRI and discussed the ability of MRI to detect metastatic disease. Some published studies advocated CT, whereas others favored MRp4.18-21 Both techniques have drawbacks, particularly in the detection and characterization of lesions less than I em in diameter. Generally, both CT and MRI are equally sensitive as preoperative screening studies in patients with known or

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suspected metastatic disease. CT is probably superior to MRI for evaluating extrahepatic organs and spaces and for identifying calcifications; however, for achieving optimal results in the liver, CT is dependent on dynamic incremental techniques after intravenous bolus infusion of iodinated contrast material. In comparison, MRI has superior contrast resolution, may be advantageous in characterizing small hepatic lesions, and is not dependent on the administration of contrast agents. In patients being considered for metastasectomy, additional studies, including CT-arterial portography or intraoperative ultrasonography (or both), are usually necessary after screening CT or MRU2-25 Hypervascular lesions (islet cell carcinoma, carcinoid tumors, thyroid tumors, and melanoma) metastatic to the liver are sometimes difficult to image with CT. After administration of iodinated contrast material, these lesions can rapidly become isodense with the normal hepatic parenchyma; their borders often become indistinct, and the entire lesion may become "invisible.?" Nonenhanced and delayed (4 to 6 hours after administration of contrast material) CT scans may be helpful in imaging these tumors, but this approach can increase scanning time and cause scheduling problems. We have found that MRI is most satisfactory for imaging

Fig. I. Improved detection of small hepatic lesions with breath-holding technique during magnetic resonance imaging. A, Tl-weighted spin-echo (repetition time, 250 ms; echo time, 15 ms) image of liver necessitating almost 3 th minutes for acquisition of six image sections. Liver is mildly inhomogeneous with no definite lesions. B, Note multiple tiny low-intensity lesions (arrows) throughout liver on magnetization-prepared gradient-recalled acquisition single slice breath-holding (7-second) image.

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hypervascular metastatic lesions (Carlson BA, Johnson CD, Stephens DR, Ward EM, Kvols LK. Unpublished data). Hypervascular metastatic involvement in patients with neuroendocrine tumors is well demarcated on MRI and can be measured accurately to assess response to treatment (Fig. 2). Many patients prefer MRl because neither orally nor intravenously administered contrast agents are necessary. Hepatocellular Carcinoma.-Using ultrasonography or CT to examine patients with cirrhosis for hepatocellular carcinoma can occasionally be difficult because regenerative nodules, fatty infiltration, and morphologic alterations from cirrhosis can mask or mimic a hepatic mass. In addition, in many patients with portal venous hypertension, diminished portal venous perfusion of the liver can decrease contrast enhancement of that organ and diminish the conspicuousness of the lesion. In such patients, MRI can be helpful in determining whether hepatocellular carcinoma is present. Malignant degeneration within a cirrhotic liver should be suspected when a nodule or mass is hyperintense (or heterogeneous with zones of hyperintense signal) on T2-weighted images (Fig. 3). Almost half of these malignant tumors have a homogeneously increased signal intensity on Tl-weighted images.":" The cause of this increased signal is thought to be steatosis, hemorrhage, or, possibly, deposition of copper in the tumor. The lesions without steatosis are hypointense on Tl-weighted images. Many solitary and some multifocal hepatocellular carcinomas have a well-defined low signal intensity capsule. Diffuse tumor manifests as multiple tiny infiltrating nodules throughout most of the hepatic parenchyma. Vascular invasion is often identified, particularly in

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large hepatic tumors (Fig. 3). Malignant degeneration within macroregenerative nodules has been reported. It appears as tiny foci of increased signal intensity in low signal intensity hemosiderin-containing nodules ("nodule within a nodule")." Cavernous Hemangioma.-Cavernous hemangiomas, common benign hepatic lesions, are clinically significant because they must be distinguished from more serious liver tumors. Frequently, a hepatic mass is discovered in a patient with a known primary malignant lesion. Characterization of the mass is critical in determining appropriate treatment options for the patient. Many imaging tests, including MRl, CT, ultrasonography, and radionuclide scans that use Tc99m-Iabeled erythrocytes, are reliable for diagnosing cavernous hemangioma. MRl is the most sensitive modality for detecting hemangiomas; it accurately distinguishes these benign lesions from metastatic tumors.F:" Because other less expensive modalities are often accurate, we recommend MRl in selected patients only. MRI should be used for patients with small lesions (less than 2 cm) or those with multiple lesions at various levels in the liver. Small lesions may be difficult to locate with CT because of differences in respiratory effort from one slice to another. Additionally, in small lesions, the characteristic enhancement pattern on CT scans may be difficult to identify if the lesion is studied late in the course of intravenous administration of contrast material. MRI should also be used in patients with renal insufficiency or allergies to iodinated contrast material. Because radionuclide scans have limited spatial resolution, lesions less than 2 em in diameter are not well visualized.

Fig. 2. Hypervascular metastatic involvement of liver. A, Computed tomographic scan, showing multiple ill-defined metastatic lesions. B, Diffuse high-intensity metastatic involvement is evident throughout liver on T2-weighted (repetition time, 2,500 ms; echo time, 110

ms) magnetic resonance image of patient with metastatic carcinoid tumor. Of note, lesions are better defined and more conspicuous and extent of tumor is better appreciated on magnetic resonance image than on computed tomographic scan.

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Fig. 3. Hepatocellular carcinoma on T2-weighted (repetition time, 2,000 ms; echo time, 70 ms) magnetic resonance images. A, Note hyperintense mass in right hepatic lobe. Tumor extends into right hepatic vein and inferior vena cava (arrows). B, Same mass at lower level extends into right portal vein (arrow). Ascites with high signal intensity is also present.

Hemangiomas adjacent to the heart or to major intrahepatic vessels can also be difficult to identify with scintigraphy. Characteristically, hemangiomas are well-circumscribed, homogeneous lesions that have low signal intensity on Tlweighted images and high signal intensity on T2-weighted images (Fig. 4).38 The signal intensity of hemangiomas mimics that of cerebrospinal fluid. Large lesions often have central areas of heterogeneity caused by fibrosis or

thrombosis. Echo times of at least 100 ms have been recommended to distinguish hemangiomas from other malignant masses. In patients with equivocal lesions, MRI may be enhanced by intravenous administration of gadoliniumdiethylenetriamine pentaacetic acid." Focal Fatty Infiltration.-Fatty infiltration of the liver is a common finding in patients with metabolic and hepatotoxic conditions. Usually, this condition is readily

Fig. 4. Magnetic resonance images of cavernous hemangioma ofliver. A, Multiple small low-intensity lesions (arrows) are evident on TIweighted (repetition time, 250 ms; echo time, 15 ms) image. B, Lesions are well defined, homogeneous, and hyperintense (similar to intensity of cerebrospinal fluid) on T2-weighted (repetition time, 2,000 ms; echo time, 110 ms) image. Findings are characteristic of cavernous hemangioma. Patient was referred for assessment of metastatic colorectal cancer. Biopsy of two of the lesions was performed with ultrasonographic guidance, and pathologic findings confirmed diagnosis of cavernous hemangioma.

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recognized with ultrasonography or CT. Focal accumulation of fat in the liver is encountered less frequently, and in patients with an underlying malignant tumor, distinguishing this benign condition from metastatic involvement is clinically important. MRI reliably discriminates between focal fatty infiltration and other hepatic masses (Fig. 5). With use of a specific imaging sequence, fat can be distinguished from other types of hepatic tissues. This pulse sequence is based on the difference in precessional frequency between fat and water protons.w" With MR!, the amount of fat in the liver or lesion can be quantified."

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Focal Nodular Hyperplasia.-Focal nodular hyperplasia, a benign condition of the liver, occurs in about 3% of the general population. Usually, it is discovered incidentally, and its importance lies in distinguishing it from other hepatic lesions that necessitate a particular treatment, such as hepatic adenoma, hepatocellular carcinoma, or metastatic tumor. The characteristic MRI appearance of focal nodular hyperplasia is a well-circumscribed mass that is isointense on both Tl- and T2-weighted images (Fig. 6).43 Unfortunately, only a few lesions have this appearance. Many lesions are isointense on either Tl- or T2-weighted images

Fig. 5. Magnetic resonanceimages,depictingfocal fatty infiltrationof liver. A, Region of high signal intensity is present in both right and left hepatic lobes on Tl-weighted (repetition time, 250 ms; echo time, 15 ms) image. Hepatic veins course normally through region of interest. B, Normal hepatic signal is present in region of concern on T2-weighted (repetition time, 2,000 ms; echo time, 70 ms) image. Findings are typical of focal fatty infiltration. C, Note poorly defined low-intensity region involving right and left hepatic lobes in this gradient echo (repetitiontime, 30 ms; echo time, 16ms; flip angle, 70°) image. Fat protons are out of phase with water protons and appear as region of diminished signal. D (samelevel as C), By using same gradient echo pulse sequence, region of interest is now isointensewith rest of liver except that echo delay has been increasedby 3 ms (repetition time, 30 ms; echo time, 19 ms: flip angle, 70°). Fat protons are in phase with water protons and have signal intensity similar to that of other nonfatty hepatic tissue.

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Fig. 6. Magnetic resonance images, showing hepatic focal nodular hyperplasia. A, Mass isointense with liver is present in right hepatic lobe on Tl-weighted (repetition time, 250 ms; echo time, 15 ms) image (arrows). B, Mass is also isointense with liver on T2-weighted image (repetition time, 2,000 ms; echo time, 70 ms) except for hyperintense central scar. Findings are characteristic of focal nodular hyperplasia.

but not on both. A central scar is seen in approximately half of all these lesions and is often hyperintense on the T2weighted image." Dynamic MRI scanning after the injection of a bolus of gadolinium demonstrates hyperintense enhancement during the arterial phase.P-" Usually, the enhancement appears uniform throughout the lesion, except for the central scar. Peripheral rim enhancement is notably absent. The use of contrast agents is not necessary in all patients but may be helpful in those with indeterminate or equivocal lesions. If a definitive diagnosis cannot be made, a sulfur-colloid liver-spleen scan is often helpful in demonstrating the presence of Kupffer cells in focal nodular hyperplasia. Hepatic Adenoma.-Hepatic adenomas are rare, benign neoplasms generally found in women of childbearing age and are often associated with the use of oral contraceptives. Usually, patients have acute abdominal pain because of intratumoral hemorrhage. Occasionally, the bleeding may develop into life-threatening hemoperitoneum. The MRI findings of hepatic adenoma are nonspecific." Most often, the lesions are solitary, well circumscribed, of low signal intensity on Tl-weighted images, and of heterogeneously high signal intensity on T2-weighted images (Fig. 7). On T1-weighted images, some tumors have increased signal intensity caused by recent hemorrhage or abundant glycogen in the lesion. The most important differential consideration is hepatocellular carcinoma, which can have identical imaging features. Surgical resection is recommended for both conditions.

DIFFUSE LIVER DISEASE Cirrhosis.-MRI can be useful in documenting the morphologic changes of cirrhosis, including atrophy of the right hepatic lobe and hypertrophy of the lateral segment of the left hepatic lobe. Frequently, macronodular regenerative changes can be identified and often appear as small rounded masses throughout the liver that are hyperintense or isointense with normal liver on Tl-weighted images and that are isointense or hypointense on T2-weighted images (Fig. 8).48 The hypointense nodules on T2-weighted images are believed to be caused by deposition of hemosiderin in the regenerating nodules; they are most apparent on gradient echo images (because of the paramagnetic effects of iron).49,5o Distinguishing hepatocellular carcinoma from regenerative nodules is usually dependent on the signal intensity of the mass on T2-weighted images. Regenerative nodules usually remain low in signal intensity on T2-weighted images and mimic the signal intensity of normal hepatic parenchyma. In most patients, hepatocellular carcinomas have higher signal intensity than does the hepatic parenchyma. The secondary changes of portal venous hypertension, including splenomegaly, upper abdominal varices, and alterations and abnormalities of the portal vein, can be demonstrated clearly with MRI. A new technique, phase-contrast cineangiography, can be used to demonstrate the direction of blood flow and to determine the velocity and volume of portal blood flow (Burkart DJ, Johnson CD, Morton MJ, Wolf RL, Ehman RL. Unpublished data).

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Fig. 7. Magnetic resonance images of hepatic adenoma. A, Large heterogeneous mass is present in right hepatic lobe on Tl-weighted (repetition time, 250 ms; echo time, 15 ms) image. Small zone (arrow) of increased signal is present in tumor and probably represents i ntratumoral hemorrhage. Capsule with low-intensity signal is also evident around periphery of lesion. B, Tumor has heterogeneous signal intensity with central scar on T2-weighted (repetition time, 2,000 ms; echo time, 110 ms) image. At operation, hepatic adenoma was removed.

Iron Overload.-The distribution of deposition of iron in the abdomen is usually categorized as either parenchymal (found in patients with primary hemochromatosis) or reticuloendothelial (found in patients who have had multiple transfusions). Because patients with primary hemochromatosis have iron deposited in the liver, pancreas, heart, and other organs, these organs may malfunction, a situation that leads to cirrhosis and cardiac failure. Iron in transfused blood is

deposited primarily in reticuloendothelial cells (in the bone marrow, spleen, and liver) and does not produce clinically significant organ dysfunction. With use of MRI, patients with iron overload. can often be identified, and primary hemochromatosis can be distinguished from reticuloendothelial deposition. 51 Organs affected by iron overload have low signal intensity on T2-weighted images and on gradient-recalled echoes.

Fig. 8. Magnetic resonance images, demonstrating hepatic cirrhosis with macroregenerative nodules. A, Liver is shrunken; note atrophy of right lobe and hypertrophy of left lobe. Throughout liver, multiple nodules are evident on T I-weighted (repetition time, 250 ms; echo time, 15 ms) image. Signal intensity of these nodules varies from isointense to hyperintense. B, Signal intensity of nodules is isointense with normal liver on T2-weighted (repetition time, 2,000 ms; echo time, 70 ms) image. Findings are consistent with regenerative nodules in cirrhotic liver without malignant degeneration.

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Comparison of the signal intensity of the liver with that of skeletal muscle is a reliable way to detect decreased liver signal. Normally, the liver is more intense than is skeletal muscle. Patients with primary hemochromatosis have decreased signal in the liver and pancreas (Fig. 9), whereas those with reticuloendothelial deposition have decreased signal in the liver, spleen, and marrow. The pancreas is spared in reticuloendothelial overload because it is not a reticuloendothelial organ. The spleen is seldom affected in primary hemochromatosis. Although imaging findings of these patient groups can overlap, MRI is often a useful technique.v-" Quantitative assessment of the amount of iron in specific organs has been reported.":" LIMITATIONS Certain problems associated with MRI of the liver still need to be solved. Most clinical techniques have lower spatial resolution than that available with CT. Currently, detecting and characterizing lesions that are less than I em in diameter are difficult. Improved resolution with satisfactory signalto-noise values may result in detection of small hepatic lesions and in better definition of normal anatomic structures. Despite advances in fast scanning, acquisition of data needs to be more rapid to evaluate physiologic events accurately, to prevent respiratory and pulsatile artifacts, and to expedite examination time. Some hepatic conditions and lesions have specific signal characteristics, but many do not. For these conditions, improved specificity may be achieved with the use of tissue-specific contrast agents.

Fig. 9. Primary hemochromatosis on mildly T2-weighted (repetition time, 2,000 ms; echo time, 40 ms) magnetic resonance image. Both liver and pancreas have very low signal intensity. Spleen has normal high signal intensity. Findings are characteristic of primary hemochromatosis.

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CONCLUSION MRI of the liver has developed into a technique that can provide excellent anatomic depiction of this organ and important information about focal and diffuse diseases that affect it. Detecting lesions with MRI is comparable to that with CT. In selected patients, MRI is the preferred modality for the evaluation of hepatocellular carcinoma, metastatic tumor, cavernous hemangioma, and focal fatty infiltration. Patients with cirrhosis can be identified and screened for complications, including hepatocellular carcinoma and portal venous hypertension. Patients with iron overload can also be identified, and often, primary hemochromatosis can be distinguished from reticuloendothelial overload. The future of MRI of hepatic lesions is encouraging. Technical and pharmaceutical advances promise to enhance diagnostic capabilities and to improve patient care.

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