Top

Abdominal Radiology

Published in:

01-08-2019 | Magnetic Resonance Imaging | Hepatobiliary

Assessment of liver fibrosis with gadoxetic acid-enhanced MRI: comparisons with transient elastography, ElastPQ, and serologic fibrosis markers

Authors: Hyeon Ji Jang, Ji Hye Min, Jeong Eun Lee, Kyung Sook Shin, Kyung-Hee Kim, Seo-Youn Choi

Published in: Abdominal Radiology | Issue 8/2019

Abstract

Objectives

To compare the diagnostic performance of gadoxetic acid-enhanced magnetic resonance imaging (MRI), ultrasonography (US)—based elastography, and serologic fibrosis markers in assessing the stage of liver fibrosis.

Materials and methods

This retrospective study included 67 patients (55 male and 12 female; mean age 62.5 years) who underwent gadoxetic acid-enhanced MRI and liver stiffness measurements before liver biopsy or surgery between January 2014 and January 2018. Measurements were performed using transient elastography (TE), ultrasound shear wave elastography point quantification (ElastPQ), and blood tests. The following MRI-based fibrosis markers were assessed: contrast enhancement index (CEI), liver–spleen contrast ratio (LSC), liver–portal vein contrast ratio (LPC), and signal intensity ratio (SIR). The diagnostic performances of fibrosis markers were compared using the area under the receiver operating characteristic curve (AUC), with histopathologic fibrosis stage as the reference standard.

Results

The fibrosis stages were F0–F1 (n = 17), F2 (n = 7), F3 (n = 20), and F4 (n = 23). MRI-based fibrosis markers negatively correlated with histologic stage: CEI (r = –0.786); LSC (r = − 0.718); LPC (r = − 0.448); and SIR (r = − 0.617; all P < 0.001). For diagnosis of either significant liver fibrosis (≥ F2) or cirrhosis (F4), the CEI provided better diagnostic accuracy (AUC = 0.898 and 0.881) than the aspartate aminotransferase-to-platelet ratio index (APRI) (AUC = 0.699 and 0.715; all P < 0.05). The CEI displayed similar diagnostic accuracy for ≥ F2 or F4 when using TE (AUC = 0.866 and 0.884, both P > 0.05) or ElastPQ [AUC = 0.751 (P = 0.021) and AUC = 0.786 (P = 0.234)].

Conclusions

The CEI measured by gadoxetic acid-enhanced MRI allows the staging of liver fibrosis, with a diagnostic accuracy comparable to that of TE and superior to that of ElastPQ or APRI.

Available only for authorised users

Motosugi U, Ichikawa T, Oguri M, Sano K, Sou H, Muhi A, Matsuda M, Fujii H, Enomoto N, Araki T (2011) Staging liver fibrosis by using liver-enhancement ratio of gadoxetic acid-enhanced MR imaging: comparison with aspartate aminotransferase-to-platelet ratio index. Magn Reson Imaging 29:1047-1052. https://doi.org/10.1016/j.mri.2011.05.007 CrossRefPubMed

Yoshida H, Shiratori Y, Moriyama M, Arakawa Y, Ide T, Sata M, Inoue O, Yano M, Tanaka M, Fujiyama S, Nishiguchi S, Kuroki T, Imazeki F, Yokosuka O, Kinoyama S, Yamada G, Omata M (1999) Interferon therapy reduces the risk for hepatocellular carcinoma: national surveillance program of cirrhotic and noncirrhotic patients with chronic hepatitis C in Japan. IHIT Study Group. Inhibition of Hepatocarcinogenesis by Interferon Therapy. Ann Intern Med 131:174-181CrossRefPubMed

Regev A, Berho M, Jeffers LJ, Milikowski C, Molina EG, Pyrsopoulos NT, Feng ZZ, Reddy KR, Schiff ER (2002) Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol 97:2614-2618. https://doi.org/10.1111/j.1572-0241.2002.06038.x CrossRefPubMed

Bedossa P, Carrat F (2009) Liver biopsy: the best, not the gold standard. J Hepatol 50:1-3. https://doi.org/10.1016/j.jhep.2008.10.014 CrossRefPubMed

Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD (2009) Liver biopsy. Hepatology 49:1017-1044. https://doi.org/10.1002/hep.22742 CrossRefPubMed

Horowitz JM, Venkatesh SK, Ehman RL, Jhaveri K, Kamath P, Ohliger MA, Samir AE, Silva AC, Taouli B, Torbenson MS, Wells ML, Yeh B, Miller FH (2017) Evaluation of hepatic fibrosis: a review from the society of abdominal radiology disease focus panel. Abdom Radiol (NY) 42:2037-2053. https://doi.org/10.1007/s00261-017-1211-7 CrossRef

Singh S, Venkatesh SK, Wang Z, Miller FH, Motosugi U, Low RN, Hassanein T, Asbach P, Godfrey EM, Yin M, Chen J, Keaveny AP, Bridges M, Bohte A, Murad MH, Lomas DJ, Talwalkar JA, Ehman RL (2015) Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol 13:440-451.e446. https://doi.org/10.1016/j.cgh.2014.09.046 CrossRefPubMed

Venkatesh SK, Yin M, Ehman RL (2013) Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging 37:544-555. https://doi.org/10.1002/jmri.23731 CrossRefPubMedPubMedCentral

Venkatesh SK, Ehman RL (2015) Magnetic resonance elastography of abdomen. Abdom Imaging 40:745–759. https://doi.org/10.1007/s00261-014-0315-6 CrossRefPubMedPubMedCentral

10.

Rockey DC, Bissell DM (2006) Noninvasive measures of liver fibrosis. Hepatology 43:S113–120. https://doi.org/10.1002/hep.21046 CrossRefPubMed

11.

Kennedy P, Wagner M, Castera L, Hong CW, Johnson CL, Sirlin CB, Taouli B (2018) Quantitative Elastography Methods in Liver Disease: Current Evidence and Future Directions. Radiology 286:738-763. https://doi.org/10.1148/radiol.2018170601 CrossRefPubMed

12.

Asayama Y, Tajima T, Nishie A, Ishigami K, Kakihara D, Nakayama T, Okamoto D, Fujita N, Aishima S, Shirabe K, Honda H (2011) Uptake of Gd-EOB-DTPA by hepatocellular carcinoma: radiologic-pathologic correlation with special reference to bile production. Eur J Radiol 80:e243-248. https://doi.org/10.1016/j.ejrad.2010.10.032 CrossRefPubMed

13.

Kobayashi S, Matsui O, Gabata T, Koda W, Minami T, Ryu Y, Kozaka K, Kitao A (2012) Relationship between signal intensity on hepatobiliary phase of gadolinium ethoxybenzyl diethylenetriaminepentaacetic acid (Gd-EOB-DTPA)-enhanced MR imaging and prognosis of borderline lesions of hepatocellular carcinoma. Eur J Radiol 81:3002-3009. https://doi.org/10.1016/j.ejrad.2012.03.029 CrossRefPubMed

14.

Akai H, Matsuda I, Kiryu S, Tajima T, Takao H, Watanabe Y, Imamura H, Kokudo N, Akahane M, Ohtomo K (2012) Fate of hypointense lesions on Gd-EOB-DTPA-enhanced magnetic resonance imaging. Eur J Radiol 81:2973-2977. https://doi.org/10.1016/j.ejrad.2012.01.007 CrossRefPubMed

15.

Verloh N, Haimerl M, Rennert J, Muller-Wille R, Niessen C, Kirchner G, Scherer MN, Schreyer AG, Stroszczynski C, Fellner C, Wiggermann P (2013) Impact of liver cirrhosis on liver enhancement at Gd-EOB-DTPA enhanced MRI at 3 Tesla. Eur J Radiol 82:1710-1715. https://doi.org/10.1016/j.ejrad.2013.05.033 CrossRefPubMed

16.

Ryeom HK, Kim SH, Kim JY, Kim HJ, Lee JM, Chang YM, Kim YS, Kang DS (2004) Quantitative evaluation of liver function with MRI Using Gd-EOB-DTPA. Korean J Radiol 5:231-239. https://doi.org/10.3348/kjr.2004.5.4.231 CrossRefPubMedPubMedCentral

17.

Tamada T, Ito K, Higaki A, Yoshida K, Kanki A, Sato T, Higashi H, Sone T (2011) Gd-EOB-DTPA-enhanced MR imaging: evaluation of hepatic enhancement effects in normal and cirrhotic livers. Eur J Radiol 80:e311-316. https://doi.org/10.1016/j.ejrad.2011.01.020 CrossRefPubMed

18.

Nishie A, Asayama Y, Ishigami K, Tajima T, Kakihara D, Nakayama T, Takayama Y, Okamoto D, Taketomi A, Shirabe K, Fujita N, Obara M, Yoshimitsu K, Honda H (2012) MR prediction of liver fibrosis using a liver-specific contrast agent: Superparamagnetic iron oxide versus Gd-EOB-DTPA. J Magn Reson Imaging 36:664-671. https://doi.org/10.1002/jmri.23691 CrossRefPubMed

19.

Tsuda N, Okada M, Murakami T (2010) New proposal for the staging of nonalcoholic steatohepatitis: evaluation of liver fibrosis on Gd-EOB-DTPA-enhanced MRI. Eur J Radiol 73:137-142. https://doi.org/10.1016/j.ejrad.2008.09.036 CrossRefPubMed

20.

Lee S, Choi D, Jeong WK (2016) Hepatic enhancement of Gd-EOB-DTPA-enhanced 3 Tesla MR imaging: Assessing severity of liver cirrhosis. J Magn Reson Imaging 44:1339-1345. https://doi.org/10.1002/jmri.25288 CrossRefPubMed

21.

Goshima S, Kanematsu M, Watanabe H, Kondo H, Kawada H, Moriyama N, Bae KT (2012) Gd-EOB-DTPA-enhanced MR imaging: prediction of hepatic fibrosis stages using liver contrast enhancement index and liver-to-spleen volumetric ratio. J Magn Reson Imaging 36:1148-1153. https://doi.org/10.1002/jmri.23758 CrossRefPubMed

22.

Zhang W, Wang X, Miao Y, Hu C, Zhao W (2018) Liver function correlates with liver-to-portal vein contrast ratio during the hepatobiliary phase with Gd-EOB-DTPA-enhanced MR at 3 Tesla. Abdom Radiol (NY) 43:2262-2269. https://doi.org/10.1007/s00261-018-1462-y CrossRef

23.

Noda Y, Goshima S, Kajita K, Kawada H, Kawai N, Koyasu H, Matsuo M, Bae KT (2016) Biliary tract enhancement in gadoxetic acid-enhanced MRI correlates with liver function biomarkers. Eur J Radiol 85:2001-2007. https://doi.org/10.1016/j.ejrad.2016.09.003 CrossRefPubMed

24.

Lin ZH, Xin YN, Dong QJ, Wang Q, Jiang XJ, Zhan SH, Sun Y, Xuan SY (2011) Performance of the aspartate aminotransferase-to-platelet ratio index for the staging of hepatitis C-related fibrosis: an updated meta-analysis. Hepatology 53:726-736. https://doi.org/10.1002/hep.24105 CrossRefPubMed

25.

Motosugi U, Ichikawa T, Sou H, Sano K, Tominaga L, Kitamura T, Araki T (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. https://doi.org/10.1002/jmri.21956 CrossRefPubMed

26.

Bedossa P, Poynard T (1996) An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology 24:289-293. https://doi.org/10.1002/hep.510240201 CrossRef

27.

Group FMCS (1994) Intraobserver and interobserver variations in liver biopsy interpretation in patients with chronic hepatitis C. The French METAVIR Cooperative Study Group. Hepatology 20:15-20CrossRef

28.

Koo TK, Li MY (2016) A Guideline of Selecting and Reporting Intraclass Correlation Coefficients for Reliability Research. J Chiropr Med 15:155-163. https://doi.org/10.1016/j.jcm.2016.02.012 CrossRefPubMedPubMedCentral

29.

Verloh N, Utpatel K, Haimerl M, Zeman F, Fellner C, Fichtner-Feigl S, Teufel A, Stroszczynski C, Evert M, Wiggermann P (2015) Liver fibrosis and Gd-EOB-DTPA-enhanced MRI: A histopathologic correlation. Sci Rep 5:15408. https://doi.org/10.1038/srep15408 CrossRefPubMedPubMedCentral

30.

Choi YR, Lee JM, Yoon JH, Han JK, Choi BI (2013) Comparison of magnetic resonance elastography and gadoxetate disodium-enhanced magnetic resonance imaging for the evaluation of hepatic fibrosis. Invest Radiol 48:607-613. https://doi.org/10.1097/RLI.0b013e318289ff8f CrossRefPubMed

31.

Feier D, Balassy C, Bastati N, Stift J, Badea R, Ba-Ssalamah A (2013) Liver fibrosis: histopathologic and biochemical influences on diagnostic efficacy of hepatobiliary contrast-enhanced MR imaging in staging. Radiology 269:460-468. https://doi.org/10.1148/radiol.13122482 CrossRefPubMed

32.

Noren B, Forsgren MF, Dahlqvist Leinhard O, Dahlstrom N, Kihlberg J, Romu T, Kechagias S, Almer S, Smedby O, Lundberg P (2013) Separation of advanced from mild hepatic fibrosis by quantification of the hepatobiliary uptake of Gd-EOB-DTPA. Eur Radiol 23:174-181. https://doi.org/10.1007/s00330-012-2583-2 CrossRefPubMed

33.

Pascolo L, Cupelli F, Anelli PL, Lorusso V, Visigalli M, Uggeri F, Tiribelli C (1999) Molecular mechanisms for the hepatic uptake of magnetic resonance imaging contrast agents. Biochem Biophys Res Commun 257:746-752. https://doi.org/10.1006/bbrc.1999.0454 CrossRefPubMed

34.

Tsuboyama T, Onishi H, Kim T, Akita H, Hori M, Tatsumi M, Nakamoto A, Nagano H, Matsuura N, Wakasa K, Tomoda K (2010) Hepatocellular carcinoma: hepatocyte-selective enhancement at gadoxetic acid-enhanced MR imaging--correlation with expression of sinusoidal and canalicular transporters and bile accumulation. Radiology 255:824-833. https://doi.org/10.1148/radiol.10091557 CrossRefPubMed

35.

Tsuda N, Matsui O (2010) Cirrhotic rat liver: reference to transporter activity and morphologic changes in bile canaliculi--gadoxetic acid-enhanced MR imaging. Radiology 256:767-773. https://doi.org/10.1148/radiol.10092065 CrossRefPubMed

36.

van Montfoort JE, Stieger B, Meijer DK, Weinmann HJ, Meier PJ, Fattinger KE (1999) Hepatic uptake of the magnetic resonance imaging contrast agent gadoxetate by the organic anion transporting polypeptide Oatp1. J Pharmacol Exp Ther 290:153-157PubMed

37.

Weinmann HJ, Bauer H, Frenzel T, Muhler A, Ebert W (1996) Mechanism of hepatic uptake of gadoxetate disodium. Acad Radiol 3 Suppl 2:S232-234CrossRefPubMed

38.

Lee NK, Kim S, Kim GH, Heo J, Seo HI, Kim TU, Kang DH (2012) Significance of the "delayed hyperintense portal vein sign" in the hepatobiliary phase MRI obtained with Gd-EOB-DTPA. J Magn Reson Imaging 36:678-685. https://doi.org/10.1002/jmri.23700 CrossRefPubMed

39.

Ni Y, Marchal G, Lukito G, Yu J, Muhler A, Baert AL (1994) MR imaging evaluation of liver enhancement by Gd-EOB-DTPA in selective and total bile duct obstruction in rats: correlation with serologic, microcholangiographic, and histologic findings. Radiology 190:753-758. https://doi.org/10.1148/radiology.190.3.8115623 CrossRefPubMed

40.

Kim T, Murakami T, Hasuike Y, Gotoh M, Kato N, Takahashi M, Miyazawa T, Narumi Y, Monden M, Nakamura H (1997) Experimental hepatic dysfunction: evaluation by MRI with Gd-EOB-DTPA. J Magn Reson Imaging 7:683-688CrossRefPubMed

41.

Watanabe H, Kanematsu M, Goshima S, Kondo H, Onozuka M, Moriyama N, Bae KT (2011) Staging hepatic fibrosis: comparison of gadoxetate disodium-enhanced and diffusion-weighted MR imaging--preliminary observations. Radiology 259:142-150. https://doi.org/10.1148/radiol.10100621 CrossRefPubMed

42.

Takatsu Y, Kobayashi S, Miyati T, Shiozaki T (2016) A novel method for evaluating enhancement using gadolinium-ethoxybenzyl-diethylenetriamine penta-acetic acid in the hepatobiliary phase of magnetic resonance imaging. Clin Imaging 40:1112-1117. https://doi.org/10.1016/j.clinimag.2016.07.001 CrossRefPubMed

43.

Dahlqvist Leinhard O, Dahlstrom N, Kihlberg J, Sandstrom P, Brismar TB, Smedby O, Lundberg P (2012) Quantifying differences in hepatic uptake of the liver specific contrast agents Gd-EOB-DTPA and Gd-BOPTA: a pilot study. Eur Radiol 22:642-653. https://doi.org/10.1007/s00330-011-2302-4 CrossRefPubMed

44.

Esterson YB, Flusberg M, Oh S, Mazzariol F, Rozenblit AM, Chernyak V (2015) Improved parenchymal liver enhancement with extended delay on Gd-EOB-DTPA-enhanced MRI in patients with parenchymal liver disease: associated clinical and imaging factors. Clin Radiol 70:723-729. https://doi.org/10.1016/j.crad.2015.03.005 CrossRefPubMed

45.

Lu Q, Lu C, Li J, Ling W, Qi X, He D, Liu J, Wen T, Wu H, Zhu H, Luo Y (2016) Stiffness Value and Serum Biomarkers in Liver Fibrosis Staging: Study in Large Surgical Specimens in Patients with Chronic Hepatitis B. Radiology 280:290-299. https://doi.org/10.1148/radiol.2016151229 CrossRefPubMed

46.

Shaheen AA, Myers RP (2007) Diagnostic accuracy of the aspartate aminotransferase-to-platelet ratio index for the prediction of hepatitis C-related fibrosis: a systematic review. Hepatology 46:912-921. https://doi.org/10.1002/hep.21835 CrossRefPubMed

47.

Yilmaz Y, Yonal O, Kurt R, Bayrak M, Aktas B, Ozdogan O (2011) Noninvasive assessment of liver fibrosis with the aspartate transaminase to platelet ratio index (APRI): Usefulness in patients with chronic liver disease: APRI in chronic liver disease. Hepat Mon 11:103-106PubMedPubMedCentral

48.

Barr RG, Ferraioli G, Palmeri ML, Goodman ZD, Garcia-Tsao G, Rubin J, Garra B, Myers RP, Wilson SR, Rubens D, Levine D (2015) Elastography Assessment of Liver Fibrosis: Society of Radiologists in Ultrasound Consensus Conference Statement. Radiology 276:845-861. https://doi.org/10.1148/radiol.2015150619 CrossRefPubMed

49.

Friedrich-Rust M, Ong MF, Martens S, Sarrazin C, Bojunga J, Zeuzem S, Herrmann E (2008) Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology 134:960-974. https://doi.org/10.1053/j.gastro.2008.01.034 CrossRefPubMed

Title: Assessment of liver fibrosis with gadoxetic acid-enhanced MRI: comparisons with transient elastography, ElastPQ, and serologic fibrosis markers
Authors: Hyeon Ji Jang
Ji Hye Min
Jeong Eun Lee
Kyung Sook Shin
Kyung-Hee Kim
Seo-Youn Choi
Publication date: 01-08-2019
Publisher: Springer US
Keywords: Magnetic Resonance Imaging
Ultrasound
Magnetic Resonance Imaging
Liver Cirrhosis
Ultrasound
Published in: Abdominal Radiology / Issue 8/2019
Print ISSN: 2366-004X
Electronic ISSN: 2366-0058
DOI: https://doi.org/10.1007/s00261-019-02041-z

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Assessment of liver fibrosis with gadoxetic acid-enhanced MRI: comparisons with transient elastography, ElastPQ, and serologic fibrosis markers

Abstract

Objectives

Materials and methods

Results

Conclusions

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Objectives

Materials and methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 8/2019

Evaluating the inflammatory activity in Crohn’s disease using magnetic resonance diffusion kurtosis imaging

Consistency of hepatocellular gadoxetic acid uptake in serial MRI examinations for evaluation of liver function

The occlusion balloon reduction technique for de novo placement and salvage of malpositioned enteric tubes

Phantom (invisible) organ sign

Predicting the pathological response to chemoradiotherapy of non-mucinous rectal cancer using pretreatment texture features based on intravoxel incoherent motion diffusion-weighted imaging

Demystifying the mesenteric root lesions

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page