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Keywords:

  • abdomen;
  • hepatobiliary imaging;
  • MRI

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

Hypervascular liver lesions are frequently encountered and can be characterised by using hepatobiliary contrast agents at MRI examinations. The imaging characteristics of a variety of hypervascular liver lesions are presented with an emphasis on differentiating features.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

A number of focal pathologies are encountered in the liver, and many will be referred to MRI for further characterisation using hepatobiliary contrast agents (HBCAs). An appreciation of the varied appearance of these lesions is necessary for accurate diagnosis. Frequently encountered lesions are described and illustrated below with an emphasis on the hepatobiliary phase (HPB) appearance and discriminating features. A discussion of HBCAs and the imaging characteristics of focal nodular hyperplasia (FNH) is outlined in Part 1 of this series.[1] The discussion below is limited to gadobenate dimeglumine (Multihance; Bracco Imaging, Milan, Italy) and gadoxetate disodium (Primovist (Eovist in the United States); Bayer Schering Pharma, Berlin, Germany) as these are the dominant agents used in Australia and New Zealand. A summary of findings is provided in Table 1.

Table 1. Table outlining the imaging features of various pathologies and features that may help discriminate between pathologies
 Arterial phaseDWIADCHBPPotential discriminating features
  1. ADC, apparent diffusion coefficient; DWI, diffusion weighted imaging; FNH, focal nodular hyperplasia; HBP, hepatobiliary phase; HCA, hepatocellular adenoma; HCC, hepatocellular carcinoma.

FNHHyperenhancingHyperintenseIso or hypointenseIso or hyperintenseT2 hyperintense scar
HCAHyperenhancingHyperintenseIso or hypointenseHypointenseDiffuse intralesional fat, ‘atoll’ sign, haemorrhage
HCCHyperenhancingHyperintenseIso or hypointenseUsually hypointense. Some are hyperintense

Washout in portal venous or equilibrium phase.

Chronic liver disease

Low-grade dysplastic noduleIsointenseIsointenseIsointensehyperintenseChronic liver disease
High-grade dysplastic noduleIsointenseHyperintenseIso or hypointenseHypointenseChronic liver disease
Fibrolamellar HCCHyperenhancingHyperintenseIso or hypointenseHypointenseLarge scar with low T2 signal, calcification
Hypervascular metastasesHyperenhancingHyperintenseIso or hypointenseHypointenseReview pancreas and kidneys for potential primary tumours, and metastases elsewhere
Flash filling haemangiomaHyperenhancingHyperintensehyperintenseHypointenseTypically small. Follow vessel signal on dynamic phases. High T2 signal
Perfusion anomalyHyperenhancingIsointenseIsointenseIsointenseTypically small and peripheral. Not seen on T2 images
PeliosisHyperenhancingHyperintenseHyperintenseHypointenseCentrifugal enhancement and high T2 signal

Haemangioma

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

Haemangioma are the most common liver tumour and are usually asymptomatic incidental findings. The majority has an incomplete ring of peripheral nodular enhancement that progresses in a centripetal fashion with increasing delay; however, haemangiomas may be arterially hyperenhancing compared with background liver. These so called ‘flash filling haemangiomas’ are typically small being less than 2 cm in diameter and usually follow vascular signal on portal venous and late phases.[2]

Because of the rapid enhancement of liver using gadoxetate acid, the peripheral enhancement of haemangiomas may be obscured and difficult to appreciate. The bright background liver may also cause them to be hypoenhancing at the equilibrium phase with ‘pseudowashout’.[3] Also, because haemangiomas do not contain functioning hepatocytes, they are hypointense in the HBP (Fig. 1). These difficulties in the dynamic phase are not encountered using gadobenate dimeglumine because of slow hepatocyte uptake of this agent. If haemangioma is considered likely, we prefer to avoid using gadoxetate acid as the features are better illustrated with standard gadolinium chelates and with gadobenate dimeglumine. High T2 signal and high apparent diffusion coefficient values are reassuring for the diagnosis of haemangioma.[4] Multiple T2 acquisitions with increasing TE are also useful for the diagnosis of haemangioma as these lesions maintain high signal. Giant haemangiomas are a variant and can measure 10 cm in size. They may be more heterogenous than small haemangiomas and may contain areas of thrombosis. It is not necessary to continue performing delayed phase acquisitions until the entire lesion fills (a thrombotic component will not enhance). An uncommon variant of haemangioma is a sclerosed haemangioma. These are a diagnostic challenge as they have mildly elevated T2 signal (less than a typical haemangioma) and do not have centripetal enhancement. They can be indistinguishable from malignant lesions at imaging.

figure

Figure 1. Arterial phase (a) showing a flash filling haemangioma (arrow) that is hyperenhancing in the portal venous phase (b) and hypointense in the hepatobiliary phase (c). Diagnosis is confirmed on the T2 (d) showing high signal.

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Hypervascular metastases

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

Hypervascular metastases may arise from neuroendocrine tumours, renal cell carcinoma, melanoma, thyroid carcinoma or choriocarcinoma and appear as arterially hyperenhancing discrete lesions that typically become iso to hypoenhancing in the portal venous phase. Given the potential primary sites, it is important to review the renal and pancreatic parenchyma, which is usually also included on liver MRI field of view. Because of the absence of hepatocytes within metastases, they are hypointense in the HBP (Fig. 2).

figure

Figure 2. Arterial phase image (a) showing multiple arterial enhancing metastases (arrows) in a patient with metastatic breast cancer. The lesions are hypointense (arrows) in the hepatobiliary phase (HBP) (b).

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Hepatocellular adenoma

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

Hepatocellular adenoma (HCA) is uncommon compared with FNH but occurs in a similar patient population (female of reproductive age). There are three subtypes of HCA being (i) hepatocyte nuclear factor 1 (HNFα1)-mutated; (ii) inflammatory; and (iii) β-catenin-mutated HCA.[5] A small proportion of HCA falls into a fourth category of ‘unclassified’. The importance of these subtypes is the different phenotypic expressions with inflammatory HCA having the highest risk of haemorrhagic complications, the β-catenin-mutated HCA having the highest risk of developing hepatocellular carcinoma (HCC) and the HNFα1-mutated HCA having a relatively benign course.[6] With standard hepatic MRI, characterisation of HCA and FNH is inconclusive in 40%.[7] The HBP enhancement of HCA is hypoenhancement compared with normal liver in over 90% of cases allowing accurate differentiation from FNH[8, 9] (Fig. 3). The HBP hypoenhancement is because of absent bile ducts in HCA and reduced expression of OATP8.[8] Once HCA has been diagnosed, it is important to interrogate the lesions for features that may suggest a specific subtype. Frequently, this will require histologic confirmation; however, a number of MRI features may be useful. HNFα1-mutated HCA generally have diffuse steatosis throughout the lesion with signal loss on the opposed phase T1; β-catenin-mutated HCA may have a pseudocapsule and an ill-defined scar, whereas inflammatory HCA may demonstrate an ‘atoll sign’ comprising a T2 hyperintense lesion rim with the central lesion being isointense to normal liver.[10] High T1 signal may be present because of intralesional haemorrhage, fat or glycogen with these features predictive of HCA[7] (Fig. 4), and this may also produce lesion heterogeneity. The arterial phase enhancement is typically less pronounced than FNH enhancement, but it is usually greater than background liver.

figure

Figure 3. T2 weighted MRI (a) shows an isointense segment 7 focal nodular hyperplasia (FNH) (long arrow) and a hyperintense segment 2 hepatocellular adenoma (short arrow). Both lesions are near isointense on the T1 precontrast (b). Both enhance in the arterial phase (c), the FNH more than the adenoma, with mild homogenous hyperenhancement of the FNH in the portal venous (d) with slight heterogenous isointense enhancement of the adenoma. The FNH (long arrow) is homogenously hyperintense in the hepatobiliary phase (HBP) (e), whereas the adenoma (short arrow) is hypointense similar to spleen (S).

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figure

Figure 4. Segment 8 hepatocellular adenoma (arrow) demonstrating marked hyperintensity on precontrast T1. This image is fat suppressed so it may be because of either haemorrhage or glycogen.

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Hepatocellular Carcinoma

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

A variety of focal lesions occur in the setting of chronic liver disease in a spectrum from regenerating nodules to HCC, and liver specific contrast agents can be used to differentiate many of these pathologies. Arterial hyperenhancement followed by washout is a major diagnostic feature of HCC, and the presence of these two signs should prompt the diagnosis of HCC regardless of the HBP appearance. Unfortunately, for small HCC, arterial hyperenhancement is specific but is insensitive with a sensitivity of 60–80% at MRI and approximately 60% at CT.[11, 12] The introduction of diffusion weighted imaging (DWI) and HBCAs has substantially aided the differentiation of nodules in the cirrhotic liver.

HCC are typically hypointense in the HBP (Fig. 5), although contrast retention has been described in both well-differentiated and moderately differentiated tumours. The mechanism is thought, in part, to relate to expression of OATP1B3,[13] and it is also more common in ‘green’ bile producing HCC.[14] The largest series of HBP retention by HCC was described by Lee et al.,[14] and all of these cases demonstrated arterial enhancement followed by washout in the portal venous and equilibrium phases allowing the correct diagnosis of HCC as based on established criteria as prescribed by the American Association for the Study of Liver Disease (AASLD)[15] (Fig. 6). In an excellent study using explanted liver pathology as gold standard, Bartolozzi et al.[16] found HBP hypointensity in 39 of 40 HCCs, 21 of 30 high-grade dysplastic nodules (HGDN) and no hypointense low-grade dysplastic nodules (LGDN). Indeed, 31 of 32 LGDN were hyperintense in the HBP, and the only other hyperintense HBP lesion was a single HGDN.

figure

Figure 5. Arterial phase (a) shows a hyperenhancing hepatocellular carcinoma (HCC), with washout in the portal venous (b) and hypointensity in the hepatobiliary phase (HBP) (c).

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figure

Figure 6. Non-contrast T1 (a) shows a segment 7 hepatocellular carcinoma (HCC) with focal fat at the three o'clock position (arrow). The HCC has arterial enhancement (b), portal venous washout with subtle capsule (c), but retention of contrast (arrow) in the hepatobiliary phase (HBP) (d).

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The role of DWI in the diagnosis of HCC has been examined. In a study comprising 109 HCC in 91 patients,[12] standard MRI using the AASLD guidelines had a sensitivity of 60%, but by combining arterial hyperenhancement with elevated DWI signal, the sensitivity increased to approximately 76%. Sensitivity increased to nearly 85% if HCC was diagnosed if a lesion fulfilled AALSD guidelines or had hypervascularity and elevated DWI signal. The majority of HCCs have elevated signal on DWI which is seen more frequently than elevated T2 signal.[17] In contrast, LGDNs do not have arterial hyperenhancement and are typically isointense on DWI which enables them to be differentiated from HGDNs that are frequently hyperintense on DWI. Arterially hypovascular lesions in chronic liver disease that are hyperintense on DWI and hypointense in the HBP will progress to a classic hypervascular HCC in over 50% of cases.[18]

Fibrolamellar HCC

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

A variant of HCC is fibrolamellar HCC, which is uncommon but occurs typically in young patients with no history of chronic liver disease. The imaging features of fibrolamellar HCC have been well described by Ichikawa et al.[19] Lesions are generally large with an average diameter over 10 cm (range 3–27 cm), and the margins are often lobulated and well defined. A central scar is seen in 71% at CT and 82% at MRI. The scar may enhance in the delayed phase and is hypointense on T1 and T2 unlike the T2 hyperintense scar in FNH. The scar is also typically larger than an FNH scar and frequently has associated small foci of calcification best appreciated on CT. This compares with FNH that only exceedingly rarely has calcific foci. Lesions are hypointense on T1 and hyperintense on T2. Heterogenous arterial hyperenhancement occurs with 36% washing out in the portal venous phase, 48% being isoenhancing and 16% hyperenhancing compared with normal liver (Fig. 7). Lymphadenopathy is present in 65% typically around the hepatic hilum and hepatoduodenal ligament. In our experience, they are hypointense in the HPB reflecting their poorly differentiated histology.

figure

Figure 7. T2 image of a fibrolamellar hepatocellular carcinoma (HCC) (a) with a hypointense scar (arrow), heterogenous arterial phase enhancement (b), mild heterogeneity in the portal venous phase with non-enhancing scar (c) and marked hypointensity in the hepatobiliary phase (HBP) (d).

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Perfusion anomalies

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

Although perfusion anomalies may occur in normal livers, they are most frequently seen in the setting of chronic liver disease and in these cases require differentiation from HCC. Because of the liver having a dual blood supply comprising hepatic arterial blood (25%) and portal venous blood (75%), any reduction in hepatic arterial resistance, or increase in portal venous resistance, will result in an arterially hyperenhancing focus. These lesions are usually located in the periphery of the liver, are typically small (under 10 mm),[20] frequently ill defined and are only seen in the hepatic arterial phase with no evidence of signal abnormality on DWI, precontrast T1 or T2 weighted images. The absence of a focal lesion in the HBP implies normal functioning hepatocytes are present and confirms the diagnosis as a perfusion anomaly pseudolesion[21] (Fig. 8).

figure

Figure 8. Arterial phase image in a patient with alcohol-related chronic liver disease showing two arterial enhancing foci (a) arrows. Neither lesion can be seen in the portal venous phase (b). The posterior lesion (long arrow) is hypointense in the hepatobiliary phase (HBP) (c) and is a hepatocellular carcinoma, whereas the more anterior lesion is not seen and is a perfusion anomaly.

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Peliosis

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

Peliosis is a rare condition characterised by dilated hepatic sinusoids forming vascular lakes.[20] They are highly variable in size, and although many cases are idiopathic, multiple conditions such as infections, tumours, medications, toxins and diabetes may be causative with resolution of peliosis following treatment of the underlying condition. The MRI signal characteristics are variable because of the presence of blood products. However in general most lesions are T2 hyperintense, T1 hypointense and following contrast administration are hypervascular. The enhancement frequently has centrifugal progression and with lesions remaining hyperintense in the equlibrium phase.[22] Because of the bulk of the lesion comprising vascular lakes, peliosis is hypoenhancing in the HBP (Fig. 9).

figure

Figure 9. Precontrast T1 (a) shows a well-defined segment 7 lesion of peliosis. Central enhancement in the arterial phase (b) increases in size in the portal venous phase (c). The lesion is hypointense similar to vessel in the hepatobiliary phase (d).

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Conclusion

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References

HBCAs enable accurate differentiation between hypervascular liver lesions in both the normal liver and in the setting of chronic liver disease, frequently allowing a confident non-invasive diagnosis to be made.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Haemangioma
  5. Hypervascular metastases
  6. Hepatocellular adenoma
  7. Hepatocellular Carcinoma
  8. Fibrolamellar HCC
  9. Perfusion anomalies
  10. Peliosis
  11. Conclusion
  12. References
  • 1
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  • 2
    Vilgrain V, Boulos L, Vullierme MP, Denys A, Terris B, Menu Y. Imaging of atypical hemangiomas of the liver with pathologic correlation. Radiographics 2000; 20: 379397.
  • 3
    Doo KW, Lee CH, Choi JW, Lee J, Kim KA, Park CM. ‘Pseudo washout’ sign in high-flow hepatic hemangioma on gadoxetic acid contrast-enhanced MRI mimicking hypervascular tumor. AJR Am J Roentgenol 2009; 193: W490496.
  • 4
    Kilickesmez O, Bayramoglu S, Inci E, Cimilli T. Value of apparent diffusion coefficient measurement for discrimination of focal benign and malignant hepatic masses. J Med Imaging Radiat Oncol 2009; 53: 5055.
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    Laumonier H, Bioulac-Sage P, Laurent C, Zucman-Rossi J, Balabaud C, Trillaud H. Hepatocellular adenomas: magnetic resonance imaging features as a function of molecular pathological classification. Hepatology 2008; 48: 808818.
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    Katabathina VS, Menias CO, Shanbhogue AK, Jagirdar J, Paspulati RM, Prasad SR. Genetics and imaging of hepatocellular adenomas: 2011 update. Radiographics 2011; 31: 15291543.
  • 7
    Bieze M, van den Esschert JW, Nio CY et al. Diagnostic accuracy of MRI in differentiating hepatocellular adenoma from focal nodular hyperplasia: prospective study of the additional value of gadoxetate disodium. AJR Am J Roentgenol 2012; 199: 2634.
  • 8
    Mohajer K, Frydrychowicz A, Robbins JB, Loeffler AG, Reed TD, Reeder SB. Characterization of hepatic adenoma and focal nodular hyperplasia with gadoxetic acid. J Magn Reson Imaging 2012; 36: 686696.
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    Denecke T, Steffen IG, Agarwal S et al. Appearance of hepatocellular adenomas on gadoxetic acid-enhanced MRI. Eur Radiol 2012; 22: 17691775.
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    Granito A, Galassi M, Piscaglia F et al. Impact of gadoxetic acid (Gd-EOB-DTPA)-enhanced magnetic resonance on the non-invasive diagnosis of small hepatocellular carcinoma: a prospective study. Aliment Pharmacol Ther 2013; 37: 355363.
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    Piana G, Trinquart L, Meskine N, Barrau V, Beers BV, Vilgrain V. New MR imaging criteria with a diffusion-weighted sequence for the diagnosis of hepatocellular carcinoma in chronic liver diseases. J Hepatol 2011; 55: 126132.
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    Narita M, Hatano E, Arizono S et al. Expression of OATP1B3 determines uptake of Gd-EOB-DTPA in hepatocellular carcinoma. J Gastroenterol 2009; 44: 793798.
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    Lee SA, Lee CH, Jung WY et al. Paradoxical high signal intensity of hepatocellular carcinoma in the hepatobiliary phase of Gd-EOB-DTPA enhanced MRI: initial experience. Magn Reson Imaging 2011; 29: 8390.
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    Bruix J, Sherman M. Management of hepatocellular carcinoma: an update. Hepatology 2011; 53: 10201022.
  • 16
    Bartolozzi C, Battaglia V, Bargellini I et al. Contrast-enhanced magnetic resonance imaging of 102 nodules in cirrhosis: correlation with histological findings on explanted livers. Abdom Imaging 2013; 38: 290296.
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    Nasu K, Kuroki Y, Tsukamoto T, Nakajima H, Mori K, Minami M. Diffusion-weighted imaging of surgically resected hepatocellular carcinoma: imaging characteristics and relationship among signal intensity, apparent diffusion coefficient, and histopathologic grade. AJR Am J Roentgenol 2009; 193: 438444.
  • 18
    Kim YK, Lee WJ, Park MJ, Kim SH, Rhim H, Choi D. Hypovascular hypointense nodules on hepatobiliary phase gadoxetic acid-enhanced MR images in patients with cirrhosis: potential of DW imaging in predicting progression to hypervascular HCC. Radiology 2012; 265: 104114.
  • 19
    Ichikawa T, Federle MP, Grazioli L, Madariaga J, Nalesnik M, Marsh W. Fibrolamellar hepatocellular carcinoma: imaging and pathologic findings in 31 recent cases. Radiology 1999; 213: 352361.
  • 20
    Torabi M, Hosseinzadeh K, Federle MP. CT of nonneoplastic hepatic vascular and perfusion disorders. Radiographics 2008; 28: 19671982.
  • 21
    Sun HY, Lee JM, Shin CI et al. Gadoxetic acid-enhanced magnetic resonance imaging for differentiating small hepatocellular carcinomas (< or =2 cm in diameter) from arterial enhancing pseudolesions: special emphasis on hepatobiliary phase imaging. Invest Radiol 2010; 45: 96103.
  • 22
    Iannaccone R, Federle MP, Brancatelli G et al. Peliosis hepatis: spectrum of imaging findings. AJR Am J Roentgenol 2006; 187: W4352.