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Published in: European Radiology 11/2019

01-11-2019 | Hepatic Adenoma | Hepatobiliary-Pancreas

MRI for characterization of benign hepatocellular tumors on hepatobiliary phase: the added value of in-phase imaging and lesion-to-liver visual signal intensity ratio

Authors: P. Lebert, M. Adens-Fauquembergue, M. Azahaf, V. Gnemmi, H. Behal, A. Luciani, O. Ernst

Published in: European Radiology | Issue 11/2019

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Abstract

Objectives

To evaluate the lesion-to-liver visual signal intensity ratio (SIR) before and at the hepatobiliary phase MRI (HBP-MRI) after gadobenate dimeglumine (Gd-BOPTA) injection, using several T1-weighted images (T1-WI), for the characterization of benign hepatocellular lesions.

Methods

Patients with histologically proven focal nodular hyperplasia (FNH) and hepatocellular adenoma (HCA), who underwent Gd-BOPTA-enhanced HBP-MRI from 2009 to 2017, were retrospectively identified. The lesion-to-liver SIR was visually assessed by two radiologists on HBP (post-HBP analysis) and compared with that of unenhanced sequences (pre/post-HBP analysis) on T1-WI in-phase (T1-IP), out-of-phase (T1-OP), and fat suppression (T1-FS). Lesions were classified as hyper-, iso-, or hypointense on post-HBP, and as decreasing, stable, or increasing SIR on pre/post-HBP analyses. The performance of the different T1-WI sequences for the diagnostic of FNH was evaluated on post-HBP analysis.

Results

Twenty-nine FNHs and 33 HCAs were analyzed. On post-HBP analysis, FNHs appeared hyper-/isointense in 89.7% of all T1-WI. HCAs appeared hypointense in 93.9%, 63.6%, and 69.7% of T1-IP, T1-OP, and T1-FS, respectively. FNHs exhibited an increasing SIR in 55.2–58.6%, a stable SIR in 44.8–58.6%, and a decreasing SIR in 0%, whereas HCAs exhibited a decreasing SIR in 66.7–93.9%, a stable SIR in 6.1–33.3%, and an increasing SIR in 0% (p < 0.0001). The specificity of T1-IP was significantly higher than that of T1-OP (p = 0.015) and T1-FS (p = 0.042).

Conclusion

T1-IP is the most reliable sequence due to misleading tumor/liver signal ratio in the case of fatty liver when using T1-FS or T1-OP. The pre/post-HBP lesion-to-liver SIR is accurate to classify benign hepatocellular lesions and contributes to avoid biopsy.

Key Points

•The T1-weighted images in-phase should be systematically included in the HBP-MRI protocol, as it is the most reliable sequence especially in the case of fatty liver.
•The comparison between lesion-to-liver signal intensity ratios on unenhanced and at the hepatobiliary phase sequences is useful to classify benign hepatocellular lesions in three categories without misclassification: FNH (increasing signal intensity ratio), HCA (decreasing signal intensity ration), and indeterminate lesions (stable signal intensity ratio).
Literature
1.
2.
go back to reference Bioulac-Sage P, Laumonier H, Rullier A et al (2009) Over-expression of glutamine synthetase in focal nodular hyperplasia: a novel easy diagnostic tool in surgical pathology. Liver Int 29:459–465CrossRef Bioulac-Sage P, Laumonier H, Rullier A et al (2009) Over-expression of glutamine synthetase in focal nodular hyperplasia: a novel easy diagnostic tool in surgical pathology. Liver Int 29:459–465CrossRef
3.
go back to reference Laumonier H, Bioulac-Sage P, Laurent C, Zucman-Rossi J, Balabaud C, Trillaud H (2008) Hepatocellular adenomas: magnetic resonance imaging features as a function of molecular pathological classification. Hepatology 48:808–818CrossRef Laumonier H, Bioulac-Sage P, Laurent C, Zucman-Rossi J, Balabaud C, Trillaud H (2008) Hepatocellular adenomas: magnetic resonance imaging features as a function of molecular pathological classification. Hepatology 48:808–818CrossRef
4.
go back to reference van Aalten SM, Thomeer MG, Terkivatan T et al (2011) Hepatocellular adenomas: correlation of MR imaging findings with pathologic subtype classification. Radiology 261:172–181CrossRef van Aalten SM, Thomeer MG, Terkivatan T et al (2011) Hepatocellular adenomas: correlation of MR imaging findings with pathologic subtype classification. Radiology 261:172–181CrossRef
5.
go back to reference Thomeer MG, Willemssen FE, Biermann KK et al (2014) MRI features of inflammatory hepatocellular adenomas on hepatocyte phase imaging with liver-specific contrast agents. J Magn Reson Imaging 39:1259–1264CrossRef Thomeer MG, Willemssen FE, Biermann KK et al (2014) MRI features of inflammatory hepatocellular adenomas on hepatocyte phase imaging with liver-specific contrast agents. J Magn Reson Imaging 39:1259–1264CrossRef
6.
go back to reference Bieze M, van den Esschert JW, Nio CY et al (2012) 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 199:26–34CrossRef Bieze M, van den Esschert JW, Nio CY et al (2012) 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 199:26–34CrossRef
7.
go back to reference van Kessel CS, de Boer E, ten Kate FJ, Brosens LA, Veldhuis WB, van Leeuwen MS (2013) Focal nodular hyperplasia: hepatobiliary enhancement patterns on gadoxetic-acid contrast-enhanced MRI. Abdom Imaging 38:490–501 van Kessel CS, de Boer E, ten Kate FJ, Brosens LA, Veldhuis WB, van Leeuwen MS (2013) Focal nodular hyperplasia: hepatobiliary enhancement patterns on gadoxetic-acid contrast-enhanced MRI. Abdom Imaging 38:490–501
8.
go back to reference European Association for the Study of the Liver (2016) EASL clinical practice guidelines on the management of benign liver tumours. J Hepatol 65:386–398CrossRef European Association for the Study of the Liver (2016) EASL clinical practice guidelines on the management of benign liver tumours. J Hepatol 65:386–398CrossRef
9.
go back to reference Ronot M, Vilgrain V (2014) Imaging of benign hepatocellular lesions: current concepts and recent updates. Clin Res Hepatol Gastroenterol 38:681–688CrossRef Ronot M, Vilgrain V (2014) Imaging of benign hepatocellular lesions: current concepts and recent updates. Clin Res Hepatol Gastroenterol 38:681–688CrossRef
10.
go back to reference Neri E, Bali MA, Ba-Ssalamah A et al (2016) ESGAR consensus statement on liver MR imaging and clinical use of liver-specific contrast agents. Eur Radiol 26:921–931CrossRef Neri E, Bali MA, Ba-Ssalamah A et al (2016) ESGAR consensus statement on liver MR imaging and clinical use of liver-specific contrast agents. Eur Radiol 26:921–931CrossRef
11.
go back to reference Merkle EM, Zech CJ, Bartolozzi C et al (2016) Consensus report from the 7th international forum for liver magnetic resonance imaging. Eur Radiol 26:674–682CrossRef Merkle EM, Zech CJ, Bartolozzi C et al (2016) Consensus report from the 7th international forum for liver magnetic resonance imaging. Eur Radiol 26:674–682CrossRef
12.
go back to reference Grazioli L, Morana G, Kirchin MA, Schneider G (2005) Accurate differentiation of focal nodular hyperplasia from hepatic adenoma at gadobenate dimeglumine-enhanced MR imaging: prospective study. Radiology 236:166–177CrossRef Grazioli L, Morana G, Kirchin MA, Schneider G (2005) Accurate differentiation of focal nodular hyperplasia from hepatic adenoma at gadobenate dimeglumine-enhanced MR imaging: prospective study. Radiology 236:166–177CrossRef
13.
go back to reference Ferlicot S, Kobeiter H, van Nhieu JT et al (2004) MRI of atypical focal nodular hyperplasia of the liver: radiology-pathology correlation. AJR Am J Roentgenol 182:1227–1231CrossRef Ferlicot S, Kobeiter H, van Nhieu JT et al (2004) MRI of atypical focal nodular hyperplasia of the liver: radiology-pathology correlation. AJR Am J Roentgenol 182:1227–1231CrossRef
14.
go back to reference Khanna M, Ramanathan S, Fasih N, Schieda N, Virmani V, McInnes MDF (2015) Current updates on the molecular genetics and magnetic resonance imaging of focal nodular hyperplasia and hepatocellular adenoma. Insights Imaging 6:347–362CrossRef Khanna M, Ramanathan S, Fasih N, Schieda N, Virmani V, McInnes MDF (2015) Current updates on the molecular genetics and magnetic resonance imaging of focal nodular hyperplasia and hepatocellular adenoma. Insights Imaging 6:347–362CrossRef
15.
go back to reference Suh CH, Kim KW, Park SH et al (2018) A cost-effectiveness analysis of the diagnostic strategies for differentiating focal nodular hyperplasia from hepatocellular adenoma. Eur Radiol 28:214–225CrossRef Suh CH, Kim KW, Park SH et al (2018) A cost-effectiveness analysis of the diagnostic strategies for differentiating focal nodular hyperplasia from hepatocellular adenoma. Eur Radiol 28:214–225CrossRef
16.
go back to reference Grieser C, Steffen IG, Kramme IB et al (2014) Gadoxetic acid enhanced MRI for differentiation of FNH and HCA: a single centre experience. Eur Radiol 24:1339–1348CrossRef Grieser C, Steffen IG, Kramme IB et al (2014) Gadoxetic acid enhanced MRI for differentiation of FNH and HCA: a single centre experience. Eur Radiol 24:1339–1348CrossRef
17.
go back to reference Tselikas L, Pigneur F, Roux M et al (2017) Impact of hepatobiliary phase liver MRI versus contrast-enhanced ultrasound after an inconclusive extracellular gadolinium-based contrast-enhanced MRI for the diagnosis of benign hepatocellular tumors. Abdom Radiol (NY) 42:825–832CrossRef Tselikas L, Pigneur F, Roux M et al (2017) Impact of hepatobiliary phase liver MRI versus contrast-enhanced ultrasound after an inconclusive extracellular gadolinium-based contrast-enhanced MRI for the diagnosis of benign hepatocellular tumors. Abdom Radiol (NY) 42:825–832CrossRef
18.
go back to reference Pirovano G, Vanzulli A, Marti-Bonmati L et al (2000) Evaluation of the accuracy of gadobenate dimeglumine-enhanced MR imaging in the detection and characterization of focal liver lesions. AJR Am J Roentgenol 175:1111–1120CrossRef Pirovano G, Vanzulli A, Marti-Bonmati L et al (2000) Evaluation of the accuracy of gadobenate dimeglumine-enhanced MR imaging in the detection and characterization of focal liver lesions. AJR Am J Roentgenol 175:1111–1120CrossRef
19.
go back to reference Zech CJ, Grazioli L, Breuer J, Reiser MF, Schoenberg SO (2008) Diagnostic performance and description of morphological features of focal nodular hyperplasia in Gd-EOB-DTPA-enhanced liver magnetic resonance imaging: results of a multicenter trial. Invest Radiol 43:504–511CrossRef Zech CJ, Grazioli L, Breuer J, Reiser MF, Schoenberg SO (2008) Diagnostic performance and description of morphological features of focal nodular hyperplasia in Gd-EOB-DTPA-enhanced liver magnetic resonance imaging: results of a multicenter trial. Invest Radiol 43:504–511CrossRef
20.
go back to reference McInnes MD, Hibbert RM, Inacio JR, Schieda N (2015) Focal nodular hyperplasia and hepatocellular adenoma: accuracy of gadoxetic acid-enhanced MR imaging--a systematic review. Radiology 277:413–423CrossRef McInnes MD, Hibbert RM, Inacio JR, Schieda N (2015) Focal nodular hyperplasia and hepatocellular adenoma: accuracy of gadoxetic acid-enhanced MR imaging--a systematic review. Radiology 277:413–423CrossRef
21.
go back to reference Suh CH, Kim KW, Kim GY, Shin YM, Kim PN, Park SH (2015) The diagnostic value of Gd-EOB-DTPA-MRI for the diagnosis of focal nodular hyperplasia: a systematic review and meta-analysis. Eur Radiol 25:950–960CrossRef Suh CH, Kim KW, Kim GY, Shin YM, Kim PN, Park SH (2015) The diagnostic value of Gd-EOB-DTPA-MRI for the diagnosis of focal nodular hyperplasia: a systematic review and meta-analysis. Eur Radiol 25:950–960CrossRef
22.
go back to reference Roux M, Pigneur F, Calderaro J et al (2015) Differentiation of focal nodular hyperplasia from hepatocellular adenoma: role of the quantitative analysis of gadobenate dimeglumine-enhanced hepatobiliary phase MRI. J Magn Reson Imaging 42:1249–1258CrossRef Roux M, Pigneur F, Calderaro J et al (2015) Differentiation of focal nodular hyperplasia from hepatocellular adenoma: role of the quantitative analysis of gadobenate dimeglumine-enhanced hepatobiliary phase MRI. J Magn Reson Imaging 42:1249–1258CrossRef
23.
go back to reference Goodwin MD, Dobson JE, Sirlin CB, Lim BG, Stella DL (2011) Diagnostic challenges and pitfalls in MR imaging with hepatocyte-specific contrast agents. Radiographics 31:1547–1568CrossRef Goodwin MD, Dobson JE, Sirlin CB, Lim BG, Stella DL (2011) Diagnostic challenges and pitfalls in MR imaging with hepatocyte-specific contrast agents. Radiographics 31:1547–1568CrossRef
24.
go back to reference Gupta RT, Iseman CM, Leyendecker JR, Shyknevsky I, Merkle EM, Taouli B (2012) Diagnosis of focal nodular hyperplasia with MRI: multicenter retrospective study comparing gadobenate dimeglumine to gadoxetate disodium. AJR Am J Roentgenol 199:35–43CrossRef Gupta RT, Iseman CM, Leyendecker JR, Shyknevsky I, Merkle EM, Taouli B (2012) Diagnosis of focal nodular hyperplasia with MRI: multicenter retrospective study comparing gadobenate dimeglumine to gadoxetate disodium. AJR Am J Roentgenol 199:35–43CrossRef
25.
go back to reference Agarwal S, Fuentes-Orrego JM, Arnason T et al (2014) Inflammatory hepatocellular adenomas can mimic focal nodular hyperplasia on gadoxetic acid-enhanced MRI. AJR Am J Roentgenol 203:W408–W414CrossRef Agarwal S, Fuentes-Orrego JM, Arnason T et al (2014) Inflammatory hepatocellular adenomas can mimic focal nodular hyperplasia on gadoxetic acid-enhanced MRI. AJR Am J Roentgenol 203:W408–W414CrossRef
26.
go back to reference Donato H, França M, Candelária I, Caseiro-Alves F (2017) Liver MRI: from basic protocol to advanced techniques. Eur J Radiol 93:30–39CrossRef Donato H, França M, Candelária I, Caseiro-Alves F (2017) Liver MRI: from basic protocol to advanced techniques. Eur J Radiol 93:30–39CrossRef
27.
go back to reference European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO) (2016) EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol 64(6):1388–1402CrossRef European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO) (2016) EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J Hepatol 64(6):1388–1402CrossRef
28.
go back to reference Bioulac-Sage P, Balabaud C, Wanless I (2010) Focal nodular hyperplasia and hepatocellular adenoma. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds) WHO Classification of Tumours of the Digestive System. IARC, Lyon, pp 198–204 Bioulac-Sage P, Balabaud C, Wanless I (2010) Focal nodular hyperplasia and hepatocellular adenoma. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds) WHO Classification of Tumours of the Digestive System. IARC, Lyon, pp 198–204
29.
go back to reference Grazioli L, Bondioni MP, Haradome H et al (2012) Hepatocellular adenoma and focal nodular hyperplasia: value of gadoxetic acid-enhanced MR imaging in differential diagnosis. Radiology 262:520–529CrossRef Grazioli L, Bondioni MP, Haradome H et al (2012) Hepatocellular adenoma and focal nodular hyperplasia: value of gadoxetic acid-enhanced MR imaging in differential diagnosis. Radiology 262:520–529CrossRef
30.
go back to reference Yoneda N, Matsui O, Kitao A et al (2012) Beta-catenin-activated hepatocellular adenoma showing hyperintensity on hepatobiliary-phase gadoxetic-enhanced magnetic resonance imaging and overexpression of OATP8. Jpn J Radiol 30:777–782CrossRef Yoneda N, Matsui O, Kitao A et al (2012) Beta-catenin-activated hepatocellular adenoma showing hyperintensity on hepatobiliary-phase gadoxetic-enhanced magnetic resonance imaging and overexpression of OATP8. Jpn J Radiol 30:777–782CrossRef
31.
go back to reference Nault JC, Couchy G, Balabaud C et al (2017) Molecular classification of hepatocellular adenoma associates with risk factors, bleeding, and malignant transformation. Gastroenterology 152:880–894.e886CrossRef Nault JC, Couchy G, Balabaud C et al (2017) Molecular classification of hepatocellular adenoma associates with risk factors, bleeding, and malignant transformation. Gastroenterology 152:880–894.e886CrossRef
32.
go back to reference Reizine E, Amaddeo G, Pigneur F et al (2018) Quantitative correlation between uptake of Gd-BOPTA on hepatobiliary phase and tumor molecular features in patients with benign hepatocellular lesions. Eur Radiol 28:4243–4253CrossRef Reizine E, Amaddeo G, Pigneur F et al (2018) Quantitative correlation between uptake of Gd-BOPTA on hepatobiliary phase and tumor molecular features in patients with benign hepatocellular lesions. Eur Radiol 28:4243–4253CrossRef
33.
go back to reference Laumonier H, Frulio N, Laurent C, Balabaud C, Zucman-Rossi J, Bioulac-Sage P (2010) Focal nodular hyperplasia with major sinusoidal dilatation: a misleading entity. BMJ Case Rep 2010:bcr0920103311PubMedPubMedCentral Laumonier H, Frulio N, Laurent C, Balabaud C, Zucman-Rossi J, Bioulac-Sage P (2010) Focal nodular hyperplasia with major sinusoidal dilatation: a misleading entity. BMJ Case Rep 2010:bcr0920103311PubMedPubMedCentral
34.
go back to reference Tse JR, Naini BV, Lu DS, Raman SS (2016) Qualitative and quantitative gadoxetic acid-enhanced MR imaging helps subtype hepatocellular adenomas. Radiology 279:118–127CrossRef Tse JR, Naini BV, Lu DS, Raman SS (2016) Qualitative and quantitative gadoxetic acid-enhanced MR imaging helps subtype hepatocellular adenomas. Radiology 279:118–127CrossRef
35.
go back to reference Fujiwara H, Sekine S, Onaya H, Shimada K, Mikata R, Arai Y (2011) Ring-like enhancement of focal nodular hyperplasia with hepatobiliary-phase Gd-EOB-DTPA-enhanced magnetic resonance imaging: radiological-pathological correlation. Jpn J Radiol 29:739–743CrossRef Fujiwara H, Sekine S, Onaya H, Shimada K, Mikata R, Arai Y (2011) Ring-like enhancement of focal nodular hyperplasia with hepatobiliary-phase Gd-EOB-DTPA-enhanced magnetic resonance imaging: radiological-pathological correlation. Jpn J Radiol 29:739–743CrossRef
36.
go back to reference Narita M, Hatano E, Arizono S et al (2009) Expression of OATP1B3 determines uptake of Gd-EOB-DTPA in hepatocellular carcinoma. J Gastroenterol 44:793–798CrossRef Narita M, Hatano E, Arizono S et al (2009) Expression of OATP1B3 determines uptake of Gd-EOB-DTPA in hepatocellular carcinoma. J Gastroenterol 44:793–798CrossRef
37.
go back to reference Dekkers IA, Roos R, van der Molen AJ (2018) Gadolinium retention after administration of contrast agents based on linear chelators and the recommendations of the European Medicines Agency. Eur Radiol 28:1579–1584CrossRef Dekkers IA, Roos R, van der Molen AJ (2018) Gadolinium retention after administration of contrast agents based on linear chelators and the recommendations of the European Medicines Agency. Eur Radiol 28:1579–1584CrossRef
38.
go back to reference Runge VM (2017) Critical questions regarding gadolinium deposition in the brain and body after injections of the gadolinium-based contrast agents, safety, and clinical recommendations in consideration of the EMA’s pharmacovigilance and risk assessment committee recommendation for suspension of the marketing authorizations for 4 linear agents. Invest Radiol 52:317–323CrossRef Runge VM (2017) Critical questions regarding gadolinium deposition in the brain and body after injections of the gadolinium-based contrast agents, safety, and clinical recommendations in consideration of the EMA’s pharmacovigilance and risk assessment committee recommendation for suspension of the marketing authorizations for 4 linear agents. Invest Radiol 52:317–323CrossRef
39.
go back to reference Roux M, Pigneur F, Baranes L et al (2018) Differentiating focal nodular hyperplasia from hepatocellular adenoma: is hepatobiliary phase MRI (HBP-MRI) using linear gadolinium chelates always useful? Abdom Radiol (NY) 43:1670–1681CrossRef Roux M, Pigneur F, Baranes L et al (2018) Differentiating focal nodular hyperplasia from hepatocellular adenoma: is hepatobiliary phase MRI (HBP-MRI) using linear gadolinium chelates always useful? Abdom Radiol (NY) 43:1670–1681CrossRef
Metadata
Title
MRI for characterization of benign hepatocellular tumors on hepatobiliary phase: the added value of in-phase imaging and lesion-to-liver visual signal intensity ratio
Authors
P. Lebert
M. Adens-Fauquembergue
M. Azahaf
V. Gnemmi
H. Behal
A. Luciani
O. Ernst
Publication date
01-11-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 11/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-019-06210-y

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