Liver-specific agents for contrast-enhanced MRI: Role in oncological imaging

Cancer Imaging

Volumn 13, Issue 4, 2013, Pages 567-579

  Thian, Yee Liang ^a   Riddell, Angela M ^b   Koh, Dow Mu ^b  

^a NATIONAL UNIVERSITY HOSPITAL   (Singapore)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Gadobenate; Gadoxetic acid; Gd BOPTA; Gd EOB DTPA; Liver; Magnetic resonance imaging

Indexed keywords

CONTRAST MEDIUM; GADOBENATE DIMEGLUMINE; GADOXETIC ACID;

BILE DUCT CARCINOMA; CLINICAL PROTOCOL; CONTRAST ENHANCEMENT; DIAGNOSTIC IMAGING; HEMANGIOMA; HEPATOBILIARY SYSTEM; HUMAN; LIVER; LIVER ADENOMA; LIVER CELL CARCINOMA; LIVER FUNCTION; LIVER METASTASIS; LIVER TOXICITY; NODULAR HYPERPLASIA; NUCLEAR MAGNETIC RESONANCE IMAGING; POSTOPERATIVE PERIOD; PREOPERATIVE PERIOD; REVIEW;

BILE DUCT NEOPLASMS; BILE DUCTS, INTRAHEPATIC; CARCINOMA, HEPATOCELLULAR; CHOLANGIOCARCINOMA; CONTRAST MEDIA; GADOLINIUM DTPA; HEMANGIOMA; HUMANS; IMAGE ENHANCEMENT; LIVER NEOPLASMS; MAGNETIC RESONANCE IMAGING; MEGLUMINE; ORGANOMETALLIC COMPOUNDS;

EID: 84891920057     PISSN: None     EISSN: 14707330     Source Type: Journal    
DOI: 10.1102/1470-7330.2013.0050     Document Type: Review

References (91)

1. Oudkerk M, Torres CG, Song B, et al. Characterization of liver lesions with mangafodipir trisodium-enhanced MR imaging: multicenter study comparing MR and dual-phase spiral CT. Radiology 2002; 223: 517-524.
2. Koh KC, Kim HJ, Choe WH, et al. The clinical usefulness of SPIO-MRI in detection and staging of hepatocellular carcinoma. Taehan Kan Hakhoe Chi 2003; 9: 17-24.
3. Reimer P, Schneider G, Schima W. Hepatobiliary contrast agents for contrast-enhanced MRI of the liver: properties, clinical development and applications. Eur Radiol 2004; 14: 559-578.
4. Gandhi SN, Brown MA, Wong JG, Aguirre DA, Sirlin CB. MR contrast agents for liver imaging: what, when, how. Radiographics 2006; 26: 1621-1636.
5. Rohrer M, Bauer H, Mintorovitch J, Requardt M, Weinmann H-J. Comparison of magnetic properties of MRI contrast media solutions at different magnetic field strengths. Invest Radiol 2005; 40: 715-724.
6. Reimer P, Rummeny EJ, Shamsi K, et al. Phase II clinical evaluation of Gd-EOB-DTPA: dose, safety aspects and pulse sequence. Radiology 1996; 199: 177-183.
7. Brismar TB, Dahlstrom N, Edsborg N, Persson A, Smedby O, Albiin N. Liver vessel enhancement by Gd-BOPTA and Gd-EOB-DTPA: a comparison in healthy volunteers. Acta Radiol 2009; 50: 709-715.
8. Tamada T, Ito K, Sone T, et al. Dynamic contrast-enhanced magnetic resonance imaging of abdominal solid organ and major vessel: comparison of enhancement effect between Gd-EOB-DTPA and Gd-DTPA. J Magn Reson Imaging 2009; 29: 636-640.
9. Zech CJ, Vos B, Nordell A, et al. Vascular enhancement in early dynamic liver MR imaging in an animal model: comparison of two injection regimen and two different doses Gd-EOB-DTPA (gadoxetic acid) with standard Gd-DTPA. Invest Radiol 2009; 44: 305-310.
10. Runge VM. A comparison of two MR hepatobiliary gadolinium chelates: Gd-BOPTA and Gd-EOB-DTPA. J Comput Assist Tomogr 1998; 22: 643-650.
11. Frydrychowicz A, Nagle SK, D'Souza SL, Vigen KK, Reeder SB. Optimized high-resolution contrast-enhanced hepatobiliary imaging at 3 tesla: a cross-over comparison of gadobenate dimeglumine and gadoxetic acid. J Magn Reson Imaging 2011; 34: 585-594.
12. Planchamp C, Hadengue A, Stieger B, et al. Function of both sinusoidal and canalicular transporters controls the concentration of organic anions within hepatocytes. Mol Pharmacol 2007; 71: 1089-1097.
13. Leonhardt M, Keiser M, Oswald S, et al. Hepatic uptake of the magnetic resonance imaging contrast agent Gd-EOB-DTPA: role of human organic anion transporters. Drug Metab Dispos 2010; 38: 1024-1108.
14. Tsuboyama T, Onishi H, Kim T, et al. Hepatocellular carcinoma: hepatocyte-selective enhancement at gadoxetic acid-enhanced MR imaging-correlation with expression of sinusoidal and canalicular transporters and bile accumulation. Radiology 2010; 255: 824-833.
15. Millet P, Moulin M, Stieger B, Daali Y, Pastor CM. How organic anions accumulate in hepatocytes lacking Mrp2: evidence in rat liver. J Pharmacol Exp Ther 2011; 336: 624-632.
16. Choi SA, Lee SS, Jung I-H, Kim HA, Byun JH, Lee MG. The effect of gadoxetic acid enhancement on lesion detection and characterisation using T2 weighted imaging and diffusion weighted imaging of the liver. Br J Radiol 2012; 85: 29-36.
17. Ahn SJ, Kim M-J, Hong H-S, Kim KA, Song H-T. Distinguishing hemangiomas from malignant solid hepatic lesions: a comparison of heavily T2-weighted images obtained before and after administration of gadoxetic acid. J Magn Reson Imaging 2011; 34: 310-317.
18. Colagrande S, Mazzoni LN, Mazzoni E, Pradella S. Effects of gadoxetic acid on quantitative diffusion-weighted imaging of the liver. J Magn Reson Imaging 2012; 36: 881-889.
19. Motosugi U, Ichikawa T, Sou H, et al. Effects of gadoxetic acid on liver elasticity measurement by using magnetic resonance elastography. Magn Reson Imaging 2012; 30: 128-132.
20. Muhi A, Ichikawa T, Motosugi U, Sou H, Sano K, Araki T. Diffusion- and T2-weighted MR imaging of the liver: effect of intravenous administration of gadoxetic acid disodium. Magn Reson Med Sci 2012; 11: 185-191.
21. Tamada T, Ito K, Yoshida K, et al. Comparison of three different injection methods for arterial phase of Gd-EOB-DTPA enhanced MR imaging of the liver. Eur J Radiol 2011; 80: e284-e288.
22. Tanimoto AA, Higuchi NN, Ueno AA. Reduction of ringing artifacts in the arterial phase of gadoxetic acid-enhanced dynamic MR imaging. Magn Reson Med Sci 2011; 11: 91-97.
23. Mitsuzaki K, Yamashita Y, Ogata I, Nishiharu T, Urata J, Takahashi M. Multiple-phase helical CT of the liver for detecting small hepatomas in patients with liver cirrhosis: contrast-injection protocol and optimal timing. AJR Am J Roentgenol 1996; 167: 753-757.
24. Chung S-H, Kim M-J, Choi JY, Hong H-S. Comparison of two different injection rates of gadoxetic acid for arterial phase MRI of the liver. J Magn Reson Imaging 2010; 31: 365-372.
25. Tanimoto A, Higuchi N, Ueno A. Reduction of ringing artifacts in the arterial phase of gadoxetic acid-enhanced dynamic MR imaging. Magn Reson Med Sci 2012; 11: 91-97.
26. Davenport MS, Viglianti BL, Al-Hawary MM, et al. Comparison of acute transient dyspnea after intravenous administration of gadoxetate disodium and gadobenate dimeglumine: effect on arterial phase image quality. Radiology 2013; 266: 452-461.
27. van Kessel CS, Veldhuis WB, van den Bosch MAAJ, van Leeuwen MS. MR liver imaging with Gd-EOB-DTPA: a delay time of 10 minutes is sufficient for lesion characterisation. Eur Radiol 2012; 22: 2153-2160.
28. Jeong HT, Kim M-J, Park M-S, et al. Detection of liver metastases using gadoxetic-enhanced dynamic and 10- and 20-minute delayed phase MR imaging. J Magn Reson Imaging 2012; 35: 635-643.
29. Kim S, Mussi TC, Lee LJ, Mausner EV, Cho KC, Rosenkrantz AB. Effect of flip angle for optimization of image quality of gadoxetate disodium-enhanced biliary imaging at 1.5 T. AJR Am J Roentgenol 2013; 200: 90-96. doi: 10.2214/AJR.12.8722.
30. Haradome H, Grazioli L, Al manea K, et al. Gadoxetic acid disodium-enhanced hepatocyte phase MRI: can increasing the flip angle improve focal liver lesion detection? J Magn Reson Imaging 2012; 35: 132-139.
31. Kim SH, Kim SH, Lee J, et al. Gadoxetic acid-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. AJR Am J Roentgenol 2009; 192: 1675-1681.
32. Hwang J, Kim SH, Lee MW, Lee JY. Small (≤ 2 cm) hepatocellular carcinoma in patients with chronic liver disease: comparison of gadoxetic acid-enhanced 3.0 T MRI and multiphasic 64-multi-row detector CT. Br J Radiol 2012; 85: e314-e322.
33. Choi JW, Lee JM, Kim SJ, et al. Hepatocellular carcinoma: imaging patterns on gadoxetic acid-enhanced MR images and their value as an imaging biomarker. Radiology 2013; 267: 776-786.
34. Kitao A, Zen Y, Matsui O, et al. Hepatocellular carcinoma: signal intensity at gadoxetic acid-enhanced MR imaging-correlation with molecular transporters and histopathologic features. Radiology 2010; 256: 817-826.
35. Kitao A, Matsui O, Yoneda N, et al. The uptake transporter OATP8 expression decreases during multistep hepatocarcinogenesis: correlation with gadoxetic acid enhanced MR imaging. Eur Radiol 2011; 21: 2056-2066.
36. Efremidis SC, Hytiroglou P, Matsui O. Enhancement patterns and signal-intensity characteristics of small hepatocellular carcinoma in cirrhosis: pathologic basis and diagnostic challenges. Eur Radiol 2007; 17: 2969-2982.
37. Shimizu A, Ito K, Koike S, Fujita T, Shimizu K, Matsunaga N. Cirrhosis or chronic hepatitis: evaluation of small (< or =2-cm) early-enhancing hepatic lesions with serial contrast-enhanced dynamic MR imaging. Radiology 2003; 226: 550-555.
38. 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: 96-103.
39. Haradome H, Grazioli L, Tinti R, et al. Additional value of gadoxetic acid-DTPA-enhanced hepatobiliary phase MR imaging in the diagnosis of early-stage hepatocellular carcinoma: comparison with dynamic triple-phase multidetector CT imaging. J Magn Reson Imaging 2011; 34: 69-78.
40. Rhee H, Kim MJ, Park MS, Kim KA. Differentiation of early hepatocellular carcinoma from benign hepatocellular nodules on gadoxetic acid-enhanced MRI. Br J Radiol 2012; 85: e837-e844.
41. Sano K, Ichikawa T, Motosugi U, et al. Imaging study of early hepatocellular carcinoma: usefulness of gadoxetic acid-enhanced MR imaging. Radiology 2011; 261: 834-844.
42. Motosugi U, Ichikawa T, Sano K, et al. Outcome of hypovascular hepatic nodules revealing no gadoxetic acid uptake in patients with chronic liver disease. J Magn Reson Imaging 2011; 34: 88-94.
43. Akai H, Matsuda I, Kiryu S, et al. Fate of hypointense lesions on Gd-EOB-DTPA-enhanced magnetic resonance imaging. Eur J Radiol 2012; 81: 2973-2977.
44. Park MJ, Kim YK, Lee MW, et al. Small hepatocellular carcinomas: improved sensitivity by combining gadoxetic acid-enhanced and diffusion-weighted MR imaging patterns. Radiology 2012; 264: 761-770.
45. Park G, Kim YK, Kim CS. Yu HC, Hwang SB. Diagnostic efficacy of gadoxetic acid-enhanced MRI in the detection of hepatocellular carcinomas: comparison with gadopentetate dimeglumine. Br J Radiol 2010; 83: 1010-1016.
46. Khan SA, Thomas HC, Davidson BR, Taylor-Robinson SD. Cholangiocarcinoma. Lancet 2005; 366: 1303-1314.
47. Maetani Y, Itoh K, Watanabe C, et al. MR imaging of intrahepatic cholangiocarcinoma with pathologic correlation. AJR Am J Roentgenol 2001; 176: 1499-1507.
48. Lacomis JM, Baron RL, Oliver JH, Nalesnik MA, Federle MP. Cholangiocarcinoma: delayed CT contrast enhancement patterns. Radiology 1997; 203: 98-104.
49. Péporté ARJ, Sommer WH, Nikolaou K, Reiser MF, Zech CJ. Imaging features of intrahepatic cholangiocarcinoma in Gd-EOB-DTPA-enhanced MRI. Eur J Radiol 2013; 82: e101-e106.
50. Kang Y, Lee JM, Kim SH, Han JK, Choi BI. Intrahepatic mass-forming cholangiocarcinoma: enhancement patterns on gadoxetic acid-enhanced MR images. Radiology 2012; 264: 751-760.
51. Kim SH, Lee CH, Kim BH, et al. Typical and atypical imaging findings of intrahepatic cholangiocarcinoma using gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid-enhanced magnetic resonance imaging. J Comput Assist Tomogr 2012; 36: 704-709.
52. Bosch FX, Ribes J, Díaz M, Cléries R. Primary liver cancer: worldwide incidence and trends. Gastroenterology 2004; 127(Suppl 1): S5-S16.
53. Chan VO, Das JP, Gerstenmaier JF, et al. Diagnostic performance of MDCT, PET/CT and gadoxetic acid (Primovist(®))-enhanced MRI in patients with colorectal liver metastases being considered for hepatic resection: initial experience in a single centre. Ir J Med Sci 2012; 181: 499-509.
54. Berger-Kulemann V, Schima W, Baroud S, et al. Gadoxetic acid-enhanced 3.0 T MR imaging versus multidetector-row CT in the detection of colorectal metastases in fatty liver using intraoperative ultrasound and histopathology as a standard of reference. Eur J Surg Oncol 2012; 38: 670-676.
55. Kim YK, Park G, Kim CS, Yu HC, Han YM. Diagnostic efficacy of gadoxetic acid-enhanced MRI for the detection and characterisation of liver metastases: comparison with multidetector-row CT. Br J Radiol 2012; 85: 539-547.
56. Runge VM, Lee C, Williams NM. Detectability of small liver metastases with gadolinium BOPTA. Invest Radiol 1997; 32: 557-565.
57. Danet I-M, Semelka RC, Leonardou P, et al. Spectrum of MRI appearances of untreated metastases of the liver. AJR Am J Roentgenol 2003; 181: 809-817.
58. Mahfouz AE, Hamm B, Wolf KJ. Peripheral washout: a sign of malignancy on dynamic gadolinium-enhanced MR images of focal liver lesions. Radiology 1994; 190: 49-52.
59. Ha S, Lee CH, Kim BH, et al. Paradoxical uptake of Gd-EOB-DTPA on the hepatobiliary phase in the evaluation of hepatic metastasis from breast cancer: is the "target sign" a common finding? Magn Reson Imaging 2012; 30: 1083-1090.
60. Kim YK, Lee JM, Kim CS. Gadobenate dimeglumine-enhanced liver MR imaging: value of dynamic and delayed imaging for the characterization and detection of focal liver lesions. Eur Radiol 2004; 14: 5-13.
61. Song WS, Schwope RB, Taylor KA, Lisanti CJ. Unexpected uptake of gadoxetic acid in a hepatic metastasis from T-cell lymphoma. Cancer Imaging 2012; 12: 122-125.
62. Koh DM, Collins DJ, Wallace T, Chau I, Riddell AM. Combining diffusion-weighted MRI with Gd-EOB-DTPA-enhanced MRI improves the detection of colorectal liver metastases. Br J Radiol 2012; 85: 980-989.
63. Buell JF, Tranchart H, Cannon R, Dagher I. Management of benign hepatic tumors. Surg Clin North Am 2010; 90: 719-735.
64. Bioulac-Sage P, Balabaud C, Wanless IR. Diagnosis of focal nodular hyperplasia: not so easy. Am J Surg Pathol 2001; 25: 1322-1325.
65. Nguyen BN, Fléjou JF, Terris B, Belghiti J, Degott C. Focal nodular hyperplasia of the liver: a comprehensive pathologic study of 305 lesions and recognition of new histologic forms. Am J Surg Pathol 1999; 23: 1441-1454.
66. van Kessel CS, de Boer E, Kate FJWT, Brosens LAA, Veldhuis WB, van Leeuwen MS. Focal nodular hyperplasia: hepatobiliary enhancement patterns on gadoxetic-acid contrast-enhanced MRI. Abdom Imaging 2012; 38: 490-501.
67. Zech CJ, Grazioli L, Breuer J, Reiser MF, Schoenberg SO. 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 2008; 43: 504-511.
68. Grazioli L, Morana G, Kirchin MA, Schneider G. Accurate differentiation of focal nodular hyperplasia from hepatic adenoma at gadobenate dimeglumine-enhanced MR imaging: prospective study. Radiology 2005; 236: 166-177.
69. Stoot JHMB, Coelen RJS, De Jong MC, Dejong CHC. Malignant transformation of hepatocellular adenomas into hepatocellular carcinomas: a systematic review including more than 1600 adenoma cases. HPB (Oxford) 2010; 12: 509-522.
70. Bioulac-Sage P, Balabaud C, Zucman-Rossi J. Subtype classification of hepatocellular adenoma. Dig Surg 2010; 27: 39-45.
71. van Aalten SM, Thomeer MGJ, Terkivatan T, et al. Hepatocellular adenomas: correlation of MR imaging findings with pathologic subtype classification. Radiology 2011; 261: 172-181.
72. Grazioli L, Bondioni MP, Haradome H, et al. Hepatocellular adenoma and focal nodular hyperplasia: value of gadoxetic acid-enhanced MR imaging in differential diagnosis. Radiology 2012; 262: 520-529.
73. Denecke T, Steffen IG, Agarwal S, et al. Appearance of hepatocellular adenomas on gadoxetic acid-enhanced MRI. Eur Radiol 2012; 22: 1769-1775.
74. Vander Borght S, Libbrecht L, Blokzijl H, et al. Diagnostic and pathogenetic implications of the expression of hepatic transporters in focal lesions occurring in normal liver. J Pathol 2005; 207: 471-482.
75. 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: 26-34.
76. Purysko AS, Remer EM, Coppa CP, Obuchowski NA, Schneider E, Veniero JC. Characteristics and distinguishing features of hepatocellular adenoma and focal nodular hyperplasia on gadoxetate disodium-enhanced MRI. AJR Am J Roentgenol 2011; 198: 115-123.
77. Gupta RT, Marin D, Boll DT, et al. Hepatic hemangiomas: difference in enhancement pattern on 3T MR imaging with gadobenate dimeglumine versus gadoxetate disodium. Eur J Radiol 2012; 81: 2457-2462.
78. 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: W490-W496.
79. Yoshimura N, Saito K, Saguchi T, et al. Distinguishing hepatic hemangiomas from metastatic tumors using T1 mapping on gadoxetic-acid-enhanced MRI. Magn Reson Imaging 2013; 31: 23-27.
80. Grazioli L, Kirchin M, Pirovano G, Spinazzi A. MultiHance in the dynamic phase of contrast enhancement: a pictorial assessment. J Comput Assist Tomogr 1999; 23(Suppl 1): S61-S64.
81. Motosugi U, Ichikawa T, Onohara K, Sou H, Sano K, Muhi A, Araki T. Distinguishing hepatic metastasis from hemangioma using gadoxetic acid-enhanced magnetic resonance imaging. Invest Radiol 2011; 46: 359-365.
82. Sun HY, Lee JM, Park HS, et al. Gadoxetic acid-enhanced MRI with MR cholangiography for the preoperative evaluation of bile duct cancer. J Magn Reson Imaging 2012; 38: 138-147. doi: 10.1002/jmri.23957.
83. Alegre Castellanos A, Molina Granados JF, Escribano Fernandez J, Gallardo Muñoz I, Triviño Tarradas F de A. Early phase detection of bile leak after hepatobiliary surgery: value of Gd-EOB-DTPA-enhanced MR cholangiography. Abdom Imaging 2012; 37: 795-802.
84. Kumazawa K, Edamoto Y, Yanase M, Nakayama T. Liver analysis using gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid-enhanced magnetic resonance imaging: correlation with histological grading and quantitative liver evaluation prior to hepatectomy. Hepatol Res 2012; 42: 1081-1088.
85. Nojiri S, Kusakabe A, Fujiwara K, et al. Noninvasive evaluation of hepatic fibrosis in HCV-infected patients using EOB-MR imaging. J Gastroenterol Hepatol 2013; 28: 1032-1039. doi: 10.1111/jgh.12181.
86. Chen B-B, Hsu C-Y, Yu C-W, et al. Clinical and histologic implications of delayed hepatobiliary enhancement on magnetic resonance imaging with gadolinium ethoxybenzyl diethylenetriaminepentaacetic acid. Invest Radiol 2012; 47: 649-655.
87. Lau H, Man K, Fan ST, Yu WC, Lo CM, Wong J. Evaluation of preoperative hepatic function in patients with hepatocellular carcinoma undergoing hepatectomy. Br J Surg 1997; 84: 1255-1259.
88. Wibmer A, Prusa AM, Nolz R, Gruenberger T, Schindl M, Ba-Ssalamah A. Liver failure after major liver resection: risk assessment by using preoperative gadoxetic acid-enhanced 3-T MR imaging. Radiology 2013; doi:10.1148/radiol. 13130210.
89. Rubbia-Brandt L, Audard V, Sartoretti P, et al. Severe hepatic sinusoidal obstruction associated with oxaliplatin-based chemotherapy in patients with metastatic colorectal cancer. Ann Oncol 2004; 15: 460-466.
90. Zdenkowski N, Chen S, van der Westhuizen A, Ackland S. Curative strategies for liver metastases from colorectal cancer: a review. Oncologist 2012; 17: 201-211.
91. Shin N-Y, Kim M-J, Lim JS, et al. Accuracy of gadoxetic acid-enhanced magnetic resonance imaging for the diagnosis of sinusoidal obstruction syndrome in patients with chemotherapy-treated colorectal liver metastases. Eur Radiol 2012; 22: 864-871.