Abstract
Objectives
To determine the imaging and clinicopathological features of MRI doughnut-like nodules (HBP-doughnut nodules), hyperintense at the hepatobiliary phase (HBP) after injection of gadoxetic acid (EOB) and without arterial-phase hyperenhancement (APHE) in cirrhotic liver.
Methods
The Institutional Review Board approved this retrospective study and informed consent was waived. We enrolled 309 consecutive patients with liver cirrhosis who were examined by EOB-MRI, dynamic CT, and angiography-assisted CT between 2008 and 2012 and searched for HBP-doughnut nodules. We evaluated imaging characteristics including haemodynamics and signal intensity of MRI, pathological findings, and frequency of malignant transformation.
Results
One hundred and one HBP-doughnut nodules without APHE were identified in 18 patients (6%), including seven of 59 (12%) patients with hepatitis-B-virus-related, nine of 230 (3.9%) with hepatitis-C-virus-related, and two of 33 (6.1%) with alcoholic cirrhosis. All nodules showed enhancement peaks in the portal phase, the same or increased intranodular portal supply on CT during arterial portography, and the same or decreased intranodular arterial supply on CT during hepatic arteriography. On T2-weighted and diffusion-weighted images, 37 (36%) and 24 (24%) nodules, respectively, showed hyperintensity predominantly in the central area. Three nodules were diagnosed by fine needle biopsy as non-neoplastic hepatic nodules. Ninety-three of 101 (92%) nodules in 16 patients were followed up during an observation period of 1163 ± 902 days (range 57–2920 days), and none showed malignant transformation.
Conclusion
HBP-doughnut nodules without APHE in cirrhotic liver were not infrequent. None became malignant. We propose calling them ‘multiacinar cirrhotic nodules’ based on the classification by an International Working Party.
Key Points
• HBP-doughnut nodules without APHE were seen in 6% of patients with liver cirrhosis.
• The enhancement peak of HBP-doughnut nodules without APHE was in the portal phase, which reflected the fact that they were supplied predominantly by the portal vein, based on angiography-assisted CT findings.
• None of the HBP-doughnut nodules without APHE in cirrhotic liver became malignant, and in conjunction with limited pathological features, they may be corresponding to multiacinar cirrhotic nodules in the International Working Party classification.
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Abbreviations
- APHE:
-
Arterial-phase hyperenhancement
- CTAP:
-
CT during arterial portography
- CTHA:
-
CT during hepatic arteriography
- DWI:
-
Diffusion-weighted images
- EOB:
-
Gadoxetic acid
- FNH:
-
Focal nodular hyperplasia
- HBP:
-
Hepatobiliary phase
- HBV:
-
Hepatitis B virus
- HCC:
-
Hepatocellular carcinoma
- HCV:
-
Hepatitis C virus
- IPH:
-
Idiopathic portal hypertension
- LRN:
-
Large regenerative nodule
- NRH:
-
Nodular regenerative hyperplasia
- OATP:
-
Organic anion transporter polypeptide
- RN:
-
Regenerative nodule
- T1WI:
-
T1-weighted images
- T2WI:
-
T2-weighted images
References
Tanimoto A, Kuwatsuru R, Kadoya M et al (1999) Evaluation of gadobenate dimeglumine in hepatocellular carcinoma: results from phase II and phase III clinical trials in Japan. J Magn Reson Imaging 10:450–460
Motosugi U, Ichikawa T, Sou H et al (2009) Liver parenchymal enhancement of hepatocyte-phase images in Gd-EOB-DTPA-enhanced MR imaging: which biological markers of the liver function affect the enhancement? J Magn Reson Imaging 30:1042–1046
Goodwin MD, Dobson JE, Sirlin CB, Lim BG, Stella DL (2011) Diagnostic challenges and pitfalls in MR imaging with hepatocyte-specific contrast agents. Radiographics 31:1547–1568
Suh YJ, Kim MJ, Choi JY, Park YN, Park MS, Kim KW (2011) Differentiation of hepatic hyperintense lesions seen on gadoxetic acid-enhanced hepatobiliary phase MRI. AJR Am J Roentgenol 197:W44–W52
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 29:739–743
Kobayashi S, Matsui O, Gabata T et al (2012) Intranodular signal intensity analysis of hypovascular high-risk borderline lesions of HCC that illustrate multi-step hepatocarcinogenesis within the nodule on Gd-EOB-DTPA-enhanced MRI. Eur J Radiol 81:3839–3845
Kitao A, Matsui O, Yoneda N et al (2011) The uptake transporter OATP8 expression decreases during multistep hepatocarcinogenesis: correlation with gadoxetic acid enhanced MR imaging. Eur Radiol 21:2056–2066
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 30:777–782
Fukusato T, Soejima Y, Kondo F et al (2015) Preserved or enhanced OATP1B3 expression in hepatocellular adenoma subtypes with nuclear accumulation of β-catenin. Hepatol Res 45:E32–E42
Gentilucci UV, Gallo P, Perrone G et al (2011) Non-cirrhotic portal hypertension with large regenerative nodules: a diagnostic challenge. World J Gastroenterol 17:2580–2584
Hayano S, Naganuma A, Okano Y et al (2016) A case of idiopathic portal hypertension associated with nodular regenerative hyperplasia-like nodule of the liver and mixed connective tissue disease. Nihon Shokakibyo Gakkai Zasshi 113:828–836
Sugimori K, Numata K, Okada M et al (2017) Central vascular structures as a characteristic finding of regenerative nodules using hepatobiliary phase gadolinium ethoxybenzyl diethylenetriaminepentaacetic acid-enhanced MRI and arterial dominant phase contrast-enhanced US. J Med Ultrason (2001) 44:89–100
Di Martino M, Anzidei M, Zaccagna F et al (2016) Qualitative analysis of small (</=2 cm) regenerative nodules, dysplastic nodules and well-differentiated HCCs with gadoxetic acid MRI. BMC Med Imaging 16:62
International Working Party (1995) Terminology of nodular hepatocellular lesions. Hepatology 22:983–993
Kitao A, Zen Y, Matsui O, Gabata T, Nakanuma Y (2009) Hepatocarcinogenesis: multistep changes of drainage vessels at CT during arterial portography and hepatic arteriography-radiologic-pathologic correlation. Radiology 252:605–614
Mohajer K, Frydrychowicz A, Robbins JB, Loeffler AG, Reed TD, Reeder SB (2012) characterisation of hepatic adenoma and focal nodular hyperplasia with gadoxetic acid. J Magn Reson Imaging 36:686–696
International Consensus Group for Hepatocellular Neoplasia (2009) Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology 49:658–664
Ferrell LD, Kakar S, Terracciano LM, Wee A (2017) Chap 13. Tumours and tumour-like lesions of the liver, 7 edn. Elsevier
Watanabe A, Ramalho M, AlObaidy M, Kim HJ, Velloni FG, Semelka RC (2015) Magnetic resonance imaging of the cirrhotic liver: an update. World J Hepatol 7:468–487
Krinsky GA, Lee VS (2000) MR imaging of cirrhotic nodules. Abdom Imaging 25:471–482
Hanna RF, Aguirre DA, Kased N, Emery SC, Peterson MR, Sirlin CB (2008) Cirrhosis-associated hepatocellular nodules: correlation of histopathologic and MR imaging features. Radiographics 28:747–769
Shimamatsu K, Kage M, Nakashima O, Kojiro M (1994) Pathomorphological study of HCV antibody-positive liver cirrhosis. J Gastroenterol Hepatol 9:624–630
Husainy MA, Sayyed F, Peddu P (2017) Typical and atypical benign liver lesions: a review. Clin Imaging 44:79–91
Yamamoto T, Sugimoto H, Takahashi N, Isobe Y (2006) Hepatic hyperplastic nodules showing stains by portal blood flow: hemodynamics revealed by CTAP and CTHA. Abdom Imaging 31:65–68
Yoneda N, Matsui O, Kitao A et al (2016) Benign hepatocellular nodules: hepatobiliary phase of gadoxetic acid-enhanced MR imaging based on molecular background. Radiographics 36:2010–2027
Wanless IR, Solt LC, Kortan P, Deck JH, Gardiner GW, Prokipchuk EJ (1981) Nodular regenerative hyperplasia of the liver associated with macroglobulinemia. A clue to the pathogenesis. Am J Med 70:1203–1209
Yoneda N, Matsui O, Kitao A et al (2012) Hepatocyte transporter expression in FNH and FNH-like nodule: correlation with signal intensity on gadoxetic acid enhanced magnetic resonance images. Jpn J Radiol 30:499–508
Kitao A, Matsui O, Yoneda N et al (2015) Hepatocellular carcinoma with β-catenin mutation: imaging and pathologic characteristics. Radiology:141315
Kitao A, Matsui O, Yoneda N et al (2012) Hypervascular hepatocellular carcinoma: correlation between biologic features and signal intensity on gadoxetic acid-enhanced MR images. Radiology 265:780–789
Kitao A, Zen Y, Matsui O et al (2010) Hepatocellular carcinoma: signal intensity at gadoxetic acid-enhanced MR imaging--correlation with molecular transporters and histopathologic features. Radiology 256:817–826
Kitao A, Matsui O, Yoneda N et al (2018) Differentiation between hepatocellular carcinoma showing hyperintensity on the hepatobiliary phase of gadoxetic acid–enhanced MRI and focal nodular hyperplasia by CT and MRI. AJR Am J Roentgenol 211:1–11
Galia M, Taibbi A, Marin D et al (2014) Focal lesions in cirrhotic liver: what else beyond hepatocellular carcinoma? Diagn Interv Radiol 20:222–228
Newerla C, Schaeffer F, Terracciano L, Hohmann J (2012) Multiple FNH-like lesions in a patient with chronic Budd-Chiari syndrome: Gd-EOB-enhanced MRI and BR1 CEUS findings. Case Rep Radiol 2012:685486
Acknowledgements
We thank Cathel Kerr, Ph.D., and Libby Cone, M.D., M.A., from Edanz Group (www.edanzediting.com/ac) for editing drafts of this manuscript.
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The scientific guarantor of this publication is Toshifumi Gabata, M.D., Ph.D.
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No complex statistical methods were necessary for this paper.
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Written informed consent was waived by the Institutional Review Board.
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Approval was obtained from the Institutional Review Board of Kanazawa University Graduate School of Medical Sciences, Japan.
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• retrospective
• observational
• performed at one institution
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Kozaka, K., Kobayashi, S., Yoneda, N. et al. Doughnut-like hyperintense nodules on hepatobiliary phase without arterial-phase hyperenhancement in cirrhotic liver: imaging and clinicopathological features. Eur Radiol 29, 6489–6498 (2019). https://doi.org/10.1007/s00330-019-06329-y
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DOI: https://doi.org/10.1007/s00330-019-06329-y