Magnetic resonance imaging of hepatocellular carcinoma
2004; Elsevier BV; Volume: 127; Issue: 5 Linguagem: Inglês
10.1053/j.gastro.2004.09.028
ISSN1528-0012
AutoresBachir Taouli, Mariela Losada, A.E. Holland, Glenn A. Krinsky,
Tópico(s)Liver Disease and Transplantation
ResumoHepatocellular carcinoma (HCC), the most common primary hepatic malignancy, usually develops in patients with cirrhosis, growing sequentially from low-grade dysplastic nodules to frank malignant HCC. Its recognition is critical because curative treatment and prognosis require early diagnosis. Survival in patients with HCC relates directly to the number, size, and extent of lesions at diagnosis. Imaging of HCC is complicated because the tumor has a varied imaging appearance and frequently coexists with other cirrhotic nodules. Magnetic resonance imaging (MRI), the best available diagnostic technique, offers good contrast resolution and diagnostic sensitivity ranging from 33% to 77%. The main difficulty is not in diagnosing large tumors, but rather small tumors (<2 cm), because of considerable overlap on imaging between benign (regenerative), borderline (dysplastic), and malignant nodules. Increasing degrees of histological malignancy are associated with increasing arterialization and loss of portal blood supply; therefore, recognition of HCC requires dynamic imaging with gadolinium-enhanced T1-weighted sequence. Typically, HCC is a focal lesion with high signal intensity on T2-weighted images, variable signal intensity on T1-weighted images, intense arterial phase enhancement after gadolinium injection, and isointensity or hypointensity at the portal venous phase. The sensitivity of MRI for detecting small lesions is low, and improvement is still needed. Newer contrast agents, higher field strength (3 Tesla) imaging, and perfusion and diffusion MRI techniques possibly will provide greater sensitivity and specificity for detecting small HCCs in the future. Hepatocellular carcinoma (HCC), the most common primary hepatic malignancy, usually develops in patients with cirrhosis, growing sequentially from low-grade dysplastic nodules to frank malignant HCC. Its recognition is critical because curative treatment and prognosis require early diagnosis. Survival in patients with HCC relates directly to the number, size, and extent of lesions at diagnosis. Imaging of HCC is complicated because the tumor has a varied imaging appearance and frequently coexists with other cirrhotic nodules. Magnetic resonance imaging (MRI), the best available diagnostic technique, offers good contrast resolution and diagnostic sensitivity ranging from 33% to 77%. The main difficulty is not in diagnosing large tumors, but rather small tumors (<2 cm), because of considerable overlap on imaging between benign (regenerative), borderline (dysplastic), and malignant nodules. Increasing degrees of histological malignancy are associated with increasing arterialization and loss of portal blood supply; therefore, recognition of HCC requires dynamic imaging with gadolinium-enhanced T1-weighted sequence. Typically, HCC is a focal lesion with high signal intensity on T2-weighted images, variable signal intensity on T1-weighted images, intense arterial phase enhancement after gadolinium injection, and isointensity or hypointensity at the portal venous phase. The sensitivity of MRI for detecting small lesions is low, and improvement is still needed. Newer contrast agents, higher field strength (3 Tesla) imaging, and perfusion and diffusion MRI techniques possibly will provide greater sensitivity and specificity for detecting small HCCs in the future. Hepatocellular carcinoma (HCC) accounts for 90% of primary liver neoplasms, represents the fifth most common cancer in the world, and is responsible for up to 1 million deaths annually worldwide.1Rustgi V.K. Epidemiology of hepatocellular carcinoma.Gastroenterol Clin North Am. 1987; 16: 545-551PubMed Google Scholar, 2Fung J. Marsh W. The quandary over liver transplantation for hepatocellular carcinoma the greater sin?.Liver Transpl. 2002; 8: 775-777Crossref PubMed Scopus (48) Google Scholar During the last 20 years, the incidence of HCC in the United States has increased from 1.4 to 2.4/100,000, with a concomitant 41% increase in overall mortality rate.3El-Serag H.B. Mason A.C. Rising incidence of hepatocellular carcinoma in the United States.N Engl J Med. 1999; 340: 745-750Crossref PubMed Scopus (2736) Google Scholar The major risk factor for HCC is cirrhosis. All types of cirrhosis predispose to HCC, but the incidence is particularly high in patients with chronic hepatitis B virus infection, chronic hepatitis C virus infection, and alcoholic liver disease. Men are affected 3 times more often than women.3El-Serag H.B. Mason A.C. Rising incidence of hepatocellular carcinoma in the United States.N Engl J Med. 1999; 340: 745-750Crossref PubMed Scopus (2736) Google Scholar The 5-year survival rate for untreated symptomatic HCC is <5%,3El-Serag H.B. Mason A.C. Rising incidence of hepatocellular carcinoma in the United States.N Engl J Med. 1999; 340: 745-750Crossref PubMed Scopus (2736) Google Scholar whereas the 5-year survival rate in patients with cirrhosis who have a small (<2 cm) HCC lesion and undergo liver transplantation is 80%; therefore, detection of small HCCs is highly critical to patient outcome.4Mazzaferro V. Regalia E. Doci R. Andreola S. Pulvirenti A. Bozzetti F. Montalto F. Ammatuna A. Gennari L. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis.N Engl J Med. 1996; 334: 693-699Crossref PubMed Scopus (6024) Google Scholar Survival of patients with HCC is related directly to the number, size, and extent of lesions at diagnosis. There is considerable overlap in imaging appearances of different types of cirrhotic nodules. Because it provides excellent contrast resolution and multiplanar evaluation, magnetic resonance (MR) imaging (MRI) is the examination of choice for detecting and characterizing cirrhotic nodules. Compared with ultrasound and computed tomography (CT), MRI is superior in detecting and characterizing HCC in the cirrhotic liver.5Winter III, T.C. Takayasu K. Muramatsu Y. Furukawa H. Wakao F. Koga H. Sakamoto M. Hirohashi S. Freeny P.C. Early advanced hepatocellular carcinoma evaluation of CT and MR appearance with pathologic correlation.Radiology. 1994; 192: 379-387PubMed Google Scholar, 6Yamashita Y. Mitsuzaki K. Yi T. Ogata I. Nishiharu T. Urata J. Takahashi M. Small hepatocellular carcinoma in patients with chronic liver damage prospective comparison of detection with dynamic MR imaging and helical CT of the whole liver.Radiology. 1996; 200: 79-84Crossref PubMed Scopus (280) Google Scholar, 7Rode A. Bancel B. Douek P. Chrvallier M. Vilgrain V. Picaud G. Henry L. Berger F. Bizollon T. Gaudin J.L. Ducerf C. Small nodule detection in cirrhotic livers evaluation with US, spiral CT, and MRI and correlation with pathologic examination of explanted liver.J Comput Assist Tomogr. 2001; 25: 327-336Crossref PubMed Scopus (264) Google Scholar MRI is highly accurate for the diagnosis of large HCC nodules; however, it is much less accurate for lesions <2 cm in diameter. Use of intravenous contrast material with multiphasic imaging (arterial, portal venous, and equilibrium) is essential to accurately identify focal hepatic lesions. Cirrhosis is a diffuse hepatic parenchymal process characterized by fibrosis and nodular regeneration. Cirrhotic nodules are classified morphologically by their size: micronodular (nodules 3 mm), or their histological pattern: regenerative (benign), dysplastic (borderline), or malignant (HCC).8Terminology of nodular hepatocellular lesions. International Working Party..Hepatology. 1995; 22 (Anonymous): 983-993PubMed Google Scholar, 9Ferrell L.D. Crawford J.M. Dhillon A.P. Scheuer P.J. Nakanuma Y. Proposal for standardized criteria for the diagnosis of benign, borderline, and malignant hepatocellular lesions arising in chronic advanced liver disease.Am J Surg Pathol. 1993; 17: 1113-1123Crossref PubMed Scopus (156) Google Scholar The pathogenesis of HCC in patients with cirrhosis is a multistep dedifferentiation process that progresses from a regenerative nodule through a dysplastic or borderline nodule to frank HCC.10Sakamoto M. Hirohashi S. Shimosato Y. Early stages of multistep hepatocarcinogenesis adenomatous hyperplasia and early hepatocellular carcinoma.Hum Pathol. 1991; 22: 172-178Abstract Full Text PDF PubMed Scopus (516) Google Scholar This process constitutes a continuous spectrum of abnormality; thus, there is considerable overlap in imaging and histological characteristics of cirrhotic nodules. Nevertheless, it is of utmost importance to distinguish benign from premalignant or malignant lesions because early liver transplantation provides the only opportunity for cure in patients with HCC and cirrhosis.11Hemming A.W. Cattral M.S. Reed A.I. Van Der Werf W.J. Greig P.D. Howard R.J. Liver transplantation for hepatocellular carcinoma.Ann Surg. 2001; 233: 652-659Crossref PubMed Scopus (300) Google Scholar A preoperative diagnosis of HCC also will increase a patient's Model for End-Stage Liver Disease score, with a subsequent decrease in waiting time for a cadaveric liver transplant. Regenerative nodules correspond histologically to local proliferation of hepatocytes surrounded by fibrous septa. Their blood supply is similar to that of normal liver, mainly from the portal vein with a small arterial contribution.12Lim J.H. Kim E.Y. Lee W.J. Lim H.K. Do Y.S. Choo I.W. Park C.K. Regenerative nodules in liver cirrhosis findings at CT during arterial portography and CT hepatic arteriography with histopathologic correlation.Radiology. 1999; 210: 451-458Crossref PubMed Scopus (55) Google Scholar Hemosiderin deposition is common in regenerative nodules (siderotic nodules) and produces specific imaging features on MRI13Ito K. Mitchell D.G. Gabata T. Hann H.W. Kim P.N. Fujita T. Awaya H. Honjo K. Matsunaga N. Hepatocellular carcinoma association with increased iron deposition in the cirrhotic liver at MR imaging.Radiology. 1999; 212: 235-240PubMed Google Scholar, 14Krinsky G.A. Lee V.S. Nguyen M.T. Rofsky N.M. Theise N.D. Morgan G.R. Teperman L.W. Weinreb J.C. Siderotic nodules in the cirrhotic liver at MR imaging with explant correlation no increased frequency of dysplastic nodules and hepatocellular carcinoma.Radiology. 2001; 218: 47-53Crossref PubMed Scopus (48) Google Scholar, 15Kim M.J. Mitchell D.G. Ito K. Kim J.H. Pasqualin D. Rubin R. Hepatic iron deposition on magnetic resonance imaging correlation with inflammatory activity.J Comput Assist Tomogr. 2002; 26: 988-993Crossref PubMed Scopus (17) Google Scholar (Figure 1). It has been suggested that iron deposition within regenerative nodules increases the risk for developing HCC.13Ito K. Mitchell D.G. Gabata T. Hann H.W. Kim P.N. Fujita T. Awaya H. Honjo K. Matsunaga N. Hepatocellular carcinoma association with increased iron deposition in the cirrhotic liver at MR imaging.Radiology. 1999; 212: 235-240PubMed Google Scholar, 14Krinsky G.A. Lee V.S. Nguyen M.T. Rofsky N.M. Theise N.D. Morgan G.R. Teperman L.W. Weinreb J.C. Siderotic nodules in the cirrhotic liver at MR imaging with explant correlation no increased frequency of dysplastic nodules and hepatocellular carcinoma.Radiology. 2001; 218: 47-53Crossref PubMed Scopus (48) Google Scholar, 15Kim M.J. Mitchell D.G. Ito K. Kim J.H. Pasqualin D. Rubin R. Hepatic iron deposition on magnetic resonance imaging correlation with inflammatory activity.J Comput Assist Tomogr. 2002; 26: 988-993Crossref PubMed Scopus (17) Google Scholar Dysplastic nodules are regenerative nodules containing atypical cells without definite histological features of malignancy.8Terminology of nodular hepatocellular lesions. International Working Party..Hepatology. 1995; 22 (Anonymous): 983-993PubMed Google Scholar They are present in 15%–25% of cirrhotic livers at the time of transplantation.16Ferrell L. Wright T. Lake J. Roberts J. Ascher N. Incidence and diagnostic features of macroregenerative nodules vs small hepatocellular carcinoma in cirrhotic livers.Hepatology. 1992; 16: 1372-1381Crossref PubMed Scopus (132) Google Scholar, 17Krinsky G.A. Lee V.S. Theise N.D. Weinreb J.C. Rofsky N.M. Diflo T. Reperman L.W. Hepatocellular carcinoma and dysplastic nodules in patients with cirrhosis prospective diagnosis with MR imaging and explantation correlation.Radiology. 2001; 219: 445-454Crossref PubMed Scopus (286) Google Scholar Dysplastic nodules can be classified as low or high grade depending on the severity of cellular atypia, and they represent an intermediate step in the pathogenesis of HCC. Malignant transformation within a dysplastic nodule has been identified as early as 4 months after the first detection of the dysplastic nodule.18Takayama T. Makuuchi M. Hirohashi S. Sakamoto S. Okazaki N. Takayasu K. Kosuge T. Motoo Y. Yamazaki S. Hasegawa H. Malignant transformation of adenomatous hyperplasia to hepatocellular carcinoma.Lancet. 1990; 336: 1150-1153Abstract PubMed Scopus (405) Google Scholar High-grade dysplastic nodules may contain a focus of HCC, leading to the "nodule within a nodule" appearance on MRI19 (Figure 2). Dysplastic nodules usually are larger than regenerative nodules, but the 2 may be impossible to distinguish, both pathologically8Terminology of nodular hepatocellular lesions. International Working Party..Hepatology. 1995; 22 (Anonymous): 983-993PubMed Google Scholar and on MRI.20Krinsky G.A. Israel G. Nondysplastic nodules that are hyperintense on T1-weighted gradient-echo MR imaging frequency in cirrhotic patients undergoing transplantation.AJR Am J Roentgenol. 2003; 180: 1023-1027Crossref PubMed Scopus (40) Google Scholar Dysplastic nodules typically are hypovascular lesions with predominantly portal blood supply, although increased arterial flow is seen in a small minority.21Matsui O. Kadoya M. Kameyama T. Yoshikawa J. Takashima T. Nakanuma Y. Unoura M. Kobayashi K. Izumi R. Ida M. et al.Benign and malignant nodules in cirrhotic livers distinction based on blood supply.Radiology. 1991; 178: 493-497PubMed Google Scholar HCC is a malignant neoplasm composed of cells with hepatocellular differentiation. HCC that develops in a cirrhotic liver may be solitary and well defined, multifocal, or diffusely infiltrative. Small HCC nodules (<2 cm) usually are well differentiated (Figure 3), whereas less well-differentiated tumors are typically larger at presentation and often associated with stromal invasion and metastases. Diffusely infiltrating tumors tend to be poorly differentiated and carry a dismal prognosis because they grow rapidly, frequently invade the main portal and hepatic veins, and also may, although less often, invade bile ducts. A mosaic appearance is seen with HCC when multiple tumor nodules are separated by fibrous septa or necrotic areas. Recent advances in MRI software and hardware, including the use of parallel imaging and surface phased-array coils, provide faster sequences that can be acquired within a breath-hold, decreasing motion and respiratory artifacts. In our institution, we use breath-hold sequences for routine liver MRI examination (whole acquisition time < 30 min). The protocol includes T1-weighted in- and out-of-phase gradient-recalled echo (GRE) to evaluate for microscopic fat content, Turbo Spin Echo (Siemens Medical Systems, Erlangen, Germany) T2-weighted with spectral fat saturation or T2-fast short tau inversion recovery, T2-weighted single-shot rapid acquisition with relaxation enhancement, and 3-dimensional T1-weighted fat suppressed GRE volume interpolated breath-hold examination before and after dynamic injection of 15–20 mL of gadolinium chelates using an automatic injector, with acquisitions at the arterial, portal venous, and equilibrium phases. We use 3-dimensional volume interpolated breath-hold examination because a greater signal to noise ratio and thinner slices are obtained compared with 2-dimensional methods. We use the shortest possible repetition time to minimize acquisition time and allow sequential acquisitions through the entire liver during breath-holding. Fat suppression improves the conspicuity of contrast enhancement and eliminates chemical-shift artifacts at fat-water interfaces. Our group was the first to show the use of a test bolus of contrast to ensure accurate timing of the hepatic arterial phase examination in patients with varying circulation times.22Earls J.P. Rofsky N.M. DeCorato D.R. Krinsky G.A. Weinreb J.C. Hepatic arterial-phase dynamic gadolinium-enhanced MR imaging optimization with a test examination and a power injector.Radiology. 1997; 202: 268-273PubMed Google Scholar The macronodular architecture of the cirrhotic liver and morphological characteristics of HCC usually are well shown on T1- and T2-weighted images. HCC can be hypointense, isointense, or hyperintense compared with the surrounding liver.7Rode A. Bancel B. Douek P. Chrvallier M. Vilgrain V. Picaud G. Henry L. Berger F. Bizollon T. Gaudin J.L. Ducerf C. Small nodule detection in cirrhotic livers evaluation with US, spiral CT, and MRI and correlation with pathologic examination of explanted liver.J Comput Assist Tomogr. 2001; 25: 327-336Crossref PubMed Scopus (264) Google Scholar, 23Kadoya M. Matsui O. Takashima T. Nonomura A. Hepatocellular carcinoma correlation of MR imaging and histopathologic findings.Radiology. 1992; 183: 819-825PubMed Google Scholar, 24Honda H. Kaneko K. Kanazawa Y. Haqyashi T. Fukuya T. Matsumata T. Maeda T. Masuda K. MR imaging of hepatocellular carcinomas effect of Cu and Fe contents on signal intensity.Abdom Imaging. 1997; 22: 60-66Crossref PubMed Scopus (22) Google Scholar Most well-differentiated HCCs and high-grade dysplastic nodules have high signal intensity on T1-weighted images25Matsui O. Kadoya M. Kameyama T. Yoshikawa J. Arai K. Gabata T. Takashima T. Nakanuma Y. Terada T. Ida M. Adenomatous hyperplastic nodules in the cirrhotic liver differentiation from hepatocellular carcinoma with MR imaging.Radiology. 1989; 173: 123-126PubMed Google Scholar, 26Earls J.P. Theise N.D. Weinreb J.C. DeCorata D.R. Krinsky G.A. Rofsky N.M. Mizrachi H. Tepereman L.W. Dysplastic nodules and hepatocellular carcinoma thin-section MR imaging of explanted cirrhotic livers with pathologic correlation.Radiology. 1996; 201: 207-214PubMed Google Scholar (Figures 2 and 3), and T1 hyperintensity can be related to copper, Fe3+, or glycogen deposition; high protein or lipid content; or possibly the degree of differentiation.27Amano S. Ebara M. Yajima T. Fukuda H. Yoshikawa M. Sugiura N. Kato K. Kondo F. Matsumoto T. Saisho H. Assessment of cancer cell differentiation in small hepatocellular carcinoma by computed tomography and magnetic resonance imaging.J Gastroenterol Hepatol. 2003; 18: 273-279Crossref PubMed Scopus (37) Google Scholar, 28Ebara M. Fukuda H. Kojima Y. Morimoto N. Yoshikawa M. Sugiura N. Satoh T. Kondo F. Yukawa M. Matsumoto M. Saisho H. Small hepatocellular carcinoma relationship of signal intensity to histopathologic findings and metal content of the tumor and surrounding hepatic parenchyma.Radiology. 1999; 210: 81-88Crossref PubMed Scopus (115) Google Scholar In-phase and opposed-phase images can show microscopic fat components within HCCs, areas of fat accumulation showing a signal drop on opposed-phase images29Mitchell D.G. Palazzo J. Hann H.W. Rifkin M.D. Burk Jr, D.L. Rubin R. Hepatocellular tumors with high signal on T1-weighted MR images chemical shift MR imaging and histologic correlation.J Comput Assist Tomogr. 1991; 15: 762-769Crossref PubMed Scopus (73) Google Scholar (Figure 3). On T2-weighted images, HCCs classically are hyperintense, whereas most dysplastic nodules are hypointense, rarely hyperintense17Krinsky G.A. Lee V.S. Theise N.D. Weinreb J.C. Rofsky N.M. Diflo T. Reperman L.W. Hepatocellular carcinoma and dysplastic nodules in patients with cirrhosis prospective diagnosis with MR imaging and explantation correlation.Radiology. 2001; 219: 445-454Crossref PubMed Scopus (286) Google Scholar, 25Matsui O. Kadoya M. Kameyama T. Yoshikawa J. Arai K. Gabata T. Takashima T. Nakanuma Y. Terada T. Ida M. Adenomatous hyperplastic nodules in the cirrhotic liver differentiation from hepatocellular carcinoma with MR imaging.Radiology. 1989; 173: 123-126PubMed Google Scholar, 26Earls J.P. Theise N.D. Weinreb J.C. DeCorata D.R. Krinsky G.A. Rofsky N.M. Mizrachi H. Tepereman L.W. Dysplastic nodules and hepatocellular carcinoma thin-section MR imaging of explanted cirrhotic livers with pathologic correlation.Radiology. 1996; 201: 207-214PubMed Google Scholar (Figures 2 and 4). However, well-differentiated HCC lesions can be isointense or, rarely, hypointense on T2-weighted images.21Matsui O. Kadoya M. Kameyama T. Yoshikawa J. Takashima T. Nakanuma Y. Unoura M. Kobayashi K. Izumi R. Ida M. et al.Benign and malignant nodules in cirrhotic livers distinction based on blood supply.Radiology. 1991; 178: 493-497PubMed Google Scholar, 26Earls J.P. Theise N.D. Weinreb J.C. DeCorata D.R. Krinsky G.A. Rofsky N.M. Mizrachi H. Tepereman L.W. Dysplastic nodules and hepatocellular carcinoma thin-section MR imaging of explanted cirrhotic livers with pathologic correlation.Radiology. 1996; 201: 207-214PubMed Google Scholar A focus of high signal intensity on T2 within a hypointense or isointense nodule (nodule within a nodule sign) is highly suggestive of HCC developing within a dysplastic nodule19Mitchell D.G. Rubin R. Siegelman E.S. Burk Jr, D.L. Rifkin M.D. Hepatocellular carcinoma within siderotic regenerative nodules appearance as a nodule within a nodule on MR images.Radiology. 1991; 178: 101-103PubMed Google Scholar (Figure 2). By correlating the signal intensity of HCC and tumor metal content, Ebara et al28Ebara M. Fukuda H. Kojima Y. Morimoto N. Yoshikawa M. Sugiura N. Satoh T. Kondo F. Yukawa M. Matsumoto M. Saisho H. Small hepatocellular carcinoma relationship of signal intensity to histopathologic findings and metal content of the tumor and surrounding hepatic parenchyma.Radiology. 1999; 210: 81-88Crossref PubMed Scopus (115) Google Scholar showed that the signal intensity of HCC on T1- and T2-weighted images is related to the degree of histological differentiation and intratumoral copper content, whereas signal intensity on T2-weighted images is related to the degree of histological differentiation. However, a relationship between copper content and signal intensity of HCC was not confirmed by other studies.30Nakakoshi T. Kajiyama M. Fujita N. Jong-Hon K. Takeichi N. Miyasaka K. Quantitative analyses of correlations of signal intensity on T1-weighted images and T1 relaxation time with copper concentration in the rat liver.Acad Radiol. 1996; 3: 36-39Abstract Full Text PDF PubMed Scopus (4) Google Scholar Hemosiderin deposition is common in regenerative nodules (called siderotic nodules), producing such specific imaging features on MRI as hypointensity on T1-weighted GRE images and T2-weighted GRE images13Ito K. Mitchell D.G. Gabata T. Hann H.W. Kim P.N. Fujita T. Awaya H. Honjo K. Matsunaga N. Hepatocellular carcinoma association with increased iron deposition in the cirrhotic liver at MR imaging.Radiology. 1999; 212: 235-240PubMed Google Scholar, 14Krinsky G.A. Lee V.S. Nguyen M.T. Rofsky N.M. Theise N.D. Morgan G.R. Teperman L.W. Weinreb J.C. Siderotic nodules in the cirrhotic liver at MR imaging with explant correlation no increased frequency of dysplastic nodules and hepatocellular carcinoma.Radiology. 2001; 218: 47-53Crossref PubMed Scopus (48) Google Scholar (Figure 1). Dysplastic nodules usually are homogeneously hyperintense on T1-weighted images, but small HCC nodules may show similar findings (Figures 2 and 3). The overlapping signal intensities of regenerative nodules, dysplastic nodules, and HCC on T1- and T2-weighted images necessitate the use of contrast media, including nonspecific extracellular gadolinium chelates or tissue-specific contrast media. Gadolinium-diethylenetriaminepentaacetic acid is an extracellular contrast medium that produces T1 shortening and enhancement of HCC on T1-weighted images. HCC obtains its blood supply almost exclusively from the hepatic artery, and most HCCs are seen best on arterial phase images (Figure 4, Figure 5, Figure 6),31Kim T. Murakami T. Oi H. Matsushita M. Kishimoto H. Igarashi H. Nakamura H. Okamurs J. Detection of hypervascular hepatocellular carcinoma by dynamic MRI and dynamic spiral CT.J Comput Assist Tomogr. 1995; 19: 948-954Crossref PubMed Scopus (69) Google Scholar, 32Murakami T. Kim T. Oi H. Nakamura H. Igarashi H. Matsushita M. Okamura J. Kozuka T. Detectability of hypervascular hepatocellular carcinoma by arterial phase images of MR and spiral CT.Acta Radiol. 1995; 36: 372-376PubMed Google Scholar, 33Oi H. Murakami T. Kim T. Matsushita M. Kishimoto H. Nakamura H. Dynamic MR imaging and early-phase helical CT for detecting small intrahepatic metastases of hepatocellular carcinoma.AJR Am J Roentgenol. 1996; 166: 369-374Crossref PubMed Scopus (151) Google Scholar allowing differentiation from regenerative and dysplastic nodules, as well as from focal fibrosis, which enhances during the portal and equilibrium phases, with typical capsular retraction (Figure 7). In the portal venous phase, HCCs appear hyperintense, isointense, or hypointense relative to the background liver (Figures 5 and 6). A minority of well-differentiated HCC lesions are hypovascular (Figure 3)21Matsui O. Kadoya M. Kameyama T. Yoshikawa J. Takashima T. Nakanuma Y. Unoura M. Kobayashi K. Izumi R. Ida M. et al.Benign and malignant nodules in cirrhotic livers distinction based on blood supply.Radiology. 1991; 178: 493-497PubMed Google Scholar and seen best at the portal venous phase because liver parenchymal enhancement peaks at this phase. Delayed images can show late enhancement of the fibrous capsule, which typically is a feature of HCC with a size >2 cm, but not of regenerative or dysplastic nodules. Both necrosis and hemorrhage are common in large tumors.Figure 6(A–C) Multifocal hepatocellular carcinoma. (A) Multiple T2 hyperintense hepatic nodules are present, (B) with strong arterial phase enhancement on postcontrast T1-weighted image (arrows). (C) Most of the nodules are not seen on postcontrast T1-weighted image at the portal venous phase, although some appear hypointense (arrows).View Large Image Figure ViewerDownload (PPT)Figure 7(A, B) Confluent hepatic fibrosis in a cirrhotic patient. (A) T2-weighted image shows ill-defined hyperintense lesion with capsular retraction. (B) Delayed enhancement is seen on T1-weighted image at equilibrium phase (arrow).View Large Image Figure ViewerDownload (PPT) Regenerative and dysplastic nodules may be difficult to identify on postgadolinium images because these are typically hypovascular lesions with predominantly portal blood supply, with enhancement similar to that of the adjacent parenchyma, although increased arterial flow has been described in a small minority of dysplastic nodules.21Matsui O. Kadoya M. Kameyama T. Yoshikawa J. Takashima T. Nakanuma Y. Unoura M. Kobayashi K. Izumi R. Ida M. et al.Benign and malignant nodules in cirrhotic livers distinction based on blood supply.Radiology. 1991; 178: 493-497PubMed Google Scholar The possibility of improving the diagnosis of HCC by the use of contrast agents specifically targeted to liver cells has been evaluated in multiple studies. Tissue-specific MR contrast media that produce T1 enhancement in hepatocytes include mangafodipir, gadobenate, and gadoxetic acid. All these agents show uptake in well-differentiated HCCs, as well as in benign hepatocellular nodules; therefore, their value in discriminating between benign and malignant lesions is limited.34Rofsky N.M. Weinreb J.C. Bernardino M.E. Young S.W. Lee J.K. Noz M.E. Hepatocellular tumors characterization with Mn-DPDP-enhanced MR imaging.Radiology. 1993; 188: 53-59PubMed Google Scholar, 35Murakami T. Baron R.L. Peterson M.S. Oliver III, J.H. Davis P.L. Confer S.R. Federle M.P. Hepatocellular carcinoma MR imaging with mangafodipir trisodium (Mn-DPDP).Radiology. 1996; 200: 69-77PubMed Google Scholar Results with these agents have not been shown to be superior to those with gadolinium for the detection of HCC. Superparamagnetic iron oxide (SPIO) particles are taken up by Kupffer cells of the reticuloendothelial system.36Imai Y. Murakami T. Yoshida S. Nishikawa M. Ohsawa M. Tokunaga K. Murata M. Shibata K. Zushi S. Kurokawa M. Yonezawa T. Kawata S. Takamura M. Nagano H. Sakon M. Monden M. Wakasa K. Nakamura H. Superparamagnetic iron oxide-enhanced magnetic resonance images of hepatocellular carcinoma correlation with histological grading.Hepatology. 2000; 32: 205-212Crossref PubMed Scopus (202) Google Scholar They enhance T2 and T2* relaxation by increasing local field inhomogeneities, causing a marked decrease in the signal intensity of liver tissue, particularly on T2-weighted images. A breath-hold T2-weighted gradient-echo sequence generally is used after SPIO injection because the susceptibility effects are maximized and respiratory artifacts are eliminated. Because of the decrease in signal intensity of the background liver, SPIO particles increase the detection and characterization of focal liver lesions (benign lesions show uptake of SPIO). Kupffer cells are rarely present in patients with HCC; therefore, the tumor will show little or no uptake of SPIO (Figure 8) and will appear more conspicuous after SPIO injection. Using both gadolinium and ferumoxide (an SPIO agent) MR agents, Bhartia et al37Bhartia B. Ward J. Guthrie J.A. Robinson P.J. Hepatocellular carcinoma in cirrhotic livers double-contrast thin-section MR imaging with pathologic correlation of explanted tissue.AJR Am J Roentgenol. 2003; 180: 577-584Crossref PubMed Scopus (120) Google Scholar showed a 78% sensitivity fo
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