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Current Medical Imaging

Author(s): Lu-Yao Lai, Meng-Ping Huang, Song Su and Jian Shu*

DOI: 10.2174/1573405616666201130101229

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Liver Fibrosis Staging with Gadolinium Ethoxybenzyl Diethylenetriamine Penta-Acetic Acid-enhanced: A Systematic Review and Meta-analysis

Page: [854 - 863] Pages: 10

  • * (Excluding Mailing and Handling)

Abstract

Objective: While liver biopsy is the golden standard for liver-fibrosis diagnosis, it is also invasive and has many limitations. Non-invasive techniques such as Magnetic Resonance Imaging (MRI) need to be further developed for liver fibrosis staging. This study aimed to evaluate the diagnostic accuracy of Gadolinium Ethoxybenzyl Diethylenetriamine Penta-acetic Acid (Gd-EOBDTPA)- enhanced MRI for liver fibrosis through systematic review and meta-analysis.

Methods: This study comprehensively searched relevant article in PubMed, Embase, and the Cochrane Library published from 2004 to 2018 to find studies analyzing the diagnostic accuracy of Gd-EOB-DTPA-enhanced MRI for liver fibrosis. Two reviewers independently screened the retrieved articles, extracted the required data from the included studies, and evaluated the methodological quality of the studies. The pooled sensitivity, specificity, positive likelihood ratio, negative likelihood ratio, diagnostic odds ratio, and Summary Receiver Operating Characteristics (SROC) curve were assessed.

Results: This study finally included 16 studies (n = 1,599) and selected a random-effects model based on the results of the I2 statistic to combine them. The areas under the SROC curve for the detection of F1 or greater, F2 or greater, F3 or greater, or F4 liver fibrosis were 0.8669, 0.8399, 0.8481, and 0.8858, respectively.

Conclusion: Gd-EOB-DTPA-enhanced MRI showed a good diagnostic performance for staging liver fibrosis, especially for F4 liver fibrosis.

Keywords: Radiology, magnetic resonance imaging, liver diseases, liver cirrhosis, contrast media, gadolinium ethoxybenzyl DTPA.

Graphical Abstract

[1]
Haimerl M, Utpatel K, Verloh N, et al. Gd-EOB-DTPA-enhanced MR relaxometry for the detection and staging of liver fibrosis. Sci Rep 2017; 7(1): 41429.
[http://dx.doi.org/10.1038/srep41429] [PMID: 28128291]
[2]
Singh S, Venkatesh SK, Wang Z, et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: A systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol 2015; 13(3): 440-451.e6.
[http://dx.doi.org/10.1016/j.cgh.2014.09.046] [PMID: 25305349]
[3]
Tsochatzis EA, Bosch J, Burroughs AK. Liver cirrhosis. Lancet 2014; 383(9930): 1749-61.
[http://dx.doi.org/10.1016/S0140-6736(14)60121-5] [PMID: 24480518]
[4]
Trautwein C, Friedman SL, Schuppan D, Pinzani M. Hepatic fibrosis: Concept to treatment. J Hepatol 2015; 62(1)(Suppl.): S15-24.
[http://dx.doi.org/10.1016/j.jhep.2015.02.039] [PMID: 25920084]
[5]
Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med 2001; 344(7): 495-500.
[http://dx.doi.org/10.1056/NEJM200102153440706] [PMID: 11172192]
[6]
Christensen C, Bruden D, Livingston S, et al. Diagnostic accuracy of a fibrosis serum panel (FIBROSpect II) compared with Knodell and Ishak liver biopsy scores in chronic hepatitis C patients. J Viral Hepat 2006; 13(10): 652-8.
[http://dx.doi.org/10.1111/j.1365-2893.2006.00743.x] [PMID: 16970596]
[7]
Regev A, Berho M, Jeffers LJ, et al. Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol 2002; 97(10): 2614-8.
[http://dx.doi.org/10.1111/j.1572-0241.2002.06038.x] [PMID: 12385448]
[8]
Bedossa P, Carrat F. Liver biopsy: the best, not the gold standard. J Hepatol 2009; 50(1): 1-3.
[http://dx.doi.org/10.1016/j.jhep.2008.10.014] [PMID: 19017551]
[9]
Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD. American Association for the Study of Liver Diseases. Liver biopsy. Hepatology 2009; 49(3): 1017-44.
[http://dx.doi.org/10.1002/hep.22742] [PMID: 19243014]
[10]
Verloh N, Utpatel K, Haimerl M, et al. Detecting liver fibrosis with Gd-EOB-DTPA-enhanced MRI: A confirmatory study. Sci Rep 2018; 8(1): 6207.
[http://dx.doi.org/10.1038/s41598-018-24316-z] [PMID: 29670136]
[11]
Caviglia GP, Ciancio A, Rosso C, et al. Non-invasive methods for the assessment of hepatic fibrosis: transient elastography, hyaluronic acid, 13C-aminopyrine breath test and cytokeratin 18 fragment. Ann Hepatol 2013; 13(1): 91-7.
[http://dx.doi.org/10.1016/S1665-2681(19)30909-3] [PMID: 24378271]
[12]
Caviglia GP, Rosso C, Fagoonee S, Saracco GM, Pellicano R. Liver fibrosis: the 2017 state of art. Panminerva Med 2017; 59(4): 320-31.
[PMID: 28880053]
[13]
Bruce M, Kolokythas O, Ferraioli G, Filice C, O’Donnell M. Limitations and artifacts in shear-wave elastography of the liver. Biomed Eng Lett 2017; 7(2): 81-9.
[http://dx.doi.org/10.1007/s13534-017-0028-1] [PMID: 30603154]
[14]
Srinivasa Babu A, Wells ML, Teytelboym OM, et al. Elastography in chronic liver disease: Modalities, techniques, limitations, and future directions. Radiographics 2016; 36(7): 1987-2006.
[http://dx.doi.org/10.1148/rg.2016160042] [PMID: 27689833]
[15]
Castéra L, Foucher J, Bernard P-H, et al. Pitfalls of liver stiffness measurement: A 5-year prospective study of 13,369 examinations. Hepatology 2010; 51(3): 828-35.
[http://dx.doi.org/10.1002/hep.23425] [PMID: 20063276]
[16]
Hamm B, Staks T, Mühler A, et al. Phase I clinical evaluation of Gd-EOB-DTPA as a hepatobiliary MR contrast agent: Safety, pharmacokinetics, and MR imaging. Radiology 1995; 195(3): 785-92.
[http://dx.doi.org/10.1148/radiology.195.3.7754011] [PMID: 7754011]
[17]
Pan S, Wang XQ, Guo QY. Quantitative assessment of hepatic fibrosis in chronic hepatitis B and C: T1 mapping on Gd-EOB-DTPA-enhanced liver magnetic resonance imaging. World J Gastroenterol 2018; 24(18): 2024-35.
[http://dx.doi.org/10.3748/wjg.v24.i18.2024] [PMID: 29760545]
[18]
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(7): 1024-8.
[http://dx.doi.org/10.1124/dmd.110.032862] [PMID: 20406852]
[19]
Feier D, Balassy C, Bastati N, Stift J, Badea R, Ba-Ssalamah A. Liver fibrosis: Histopathologic and biochemical influences on diagnostic efficacy of hepatobiliary contrast-enhanced MR imaging in staging. Radiology 2013; 269(2): 460-8.
[http://dx.doi.org/10.1148/radiol.13122482] [PMID: 23878281]
[20]
Giacomini KM, Huang SM, Tweedie DJ, et al. International transporter consortium. membrane transporters in drug development. Nat Rev Drug Discov 2010; 9(3): 215-36.
[http://dx.doi.org/10.1038/nrd3028] [PMID: 20190787]
[21]
Caraiani CN, Dan M, Fenesan DI, Badea R. Description of focal liver lesions with Gd-EOB-DTPA enhanced MRI. Clujul Med 2015; 88(4): 438-48.
[PMID: 26733231]
[22]
McInnes MDF, Moher D, Thombs BD, et al. Preferred reporting items for a systematic review and meta-analysis of diagnostic test accuracy Sstudies: The PRISMA-DTA statement. JAMA 2018; 319(4): 388-96.
[http://dx.doi.org/10.1001/jama.2017.19163] [PMID: 29362800]
[23]
Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2 Group. QUADAS-2: A revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 2011; 155(8): 529-36.
[http://dx.doi.org/10.7326/0003-4819-155-8-201110180-00009] [PMID: 22007046]
[24]
Choi YR, Lee JM, Yoon JH, Han JK, Choi BI. Comparison of magnetic resonance elastography and gadoxetate disodium-enhanced magnetic resonance imaging for the evaluation of hepatic fibrosis. Invest Radiol 2013; 48(8): 607-13.
[http://dx.doi.org/10.1097/RLI.0b013e318289ff8f] [PMID: 23538889]
[25]
Ding Y, Rao S-X, Zhu T, Chen C-Z, Li R-C, Zeng M-S. Liver fibrosis staging using T1 mapping on gadoxetic acid-enhanced MRI compared with DW imaging. Clin Radiol 2015; 70(10): 1096-103.
[http://dx.doi.org/10.1016/j.crad.2015.04.014] [PMID: 26164421]
[26]
Goshima S, Kanematsu M, Watanabe H, et al. 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 2012; 36(5): 1148-53.
[http://dx.doi.org/10.1002/jmri.23758] [PMID: 22848019]
[27]
Harada TL, Saito K, Araki Y, et al. Prediction of high-stage liver fibrosis using ADC value on diffusion-weighted imaging and quantitative enhancement ratio at the hepatobiliary phase of Gd-EOB-DTPA-enhanced MRI at 1.5 T. Acta Radiol 2018; 59(5): 509-16.
[http://dx.doi.org/10.1177/0284185117725778] [PMID: 28853292]
[28]
Jang Y-J, Cho SH, Bae JH, et al. Noninvasive assessment of hepatic fibrosis using gadoxetate-disodium-enhanced 3T MRI. Ann Hepatol 2013; 12(6): 926-34.
[http://dx.doi.org/10.1016/S1665-2681(19)31298-0] [PMID: 24114823]
[29]
Juluru K, Talal AH, Yantiss RK, et al. Diagnostic accuracy of intracellular uptake rates calculated using dynamic Gd-EOB-DTPA-enhanced MRI for hepatic fibrosis stage. J Magn Reson Imaging 2017; 45(4): 1177-85.
[http://dx.doi.org/10.1002/jmri.25431] [PMID: 27527820]
[30]
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(11): 1081-8.
[http://dx.doi.org/10.1111/j.1872-034X.2012.01027.x] [PMID: 22647151]
[31]
Motosugi U, Ichikawa T, Oguri M, et al. 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 2011; 29(8): 1047-52.
[http://dx.doi.org/10.1016/j.mri.2011.05.007] [PMID: 21775085]
[32]
Nishie A, Asayama Y, Ishigami K, et al. MR prediction of liver fibrosis using a liver-specific contrast agent: Superparamagnetic iron oxide versus Gd-EOB-DTPA. J Magn Reson Imaging 2012; 36(3): 664-71.
[http://dx.doi.org/10.1002/jmri.23691] [PMID: 22532503]
[33]
Nojiri S, Kusakabe A, Fujiwara K, et al. Noninvasive evaluation of hepatic fibrosis in hepatitis C virus-infected patients using ethoxybenzyl-magnetic resonance imaging. J Gastroenterol Hepatol 2013; 28(6): 1032-9.
[http://dx.doi.org/10.1111/jgh.12181] [PMID: 23432660]
[34]
Okada M, Murakami T, Yada N, et al. Comparison between T1 relaxation time of Gd-EOB-DTPA-enhanced MRI and liver stiffness measurement of ultrasound elastography in the evaluation of cirrhotic liver. J Magn Reson Imaging 2015; 41(2): 329-38.
[http://dx.doi.org/10.1002/jmri.24529] [PMID: 24343840]
[35]
Wu W-P, Hoi C-I, Chen R-C, Lin C-P, Chou C-T. Comparison of the efficacy of Gd-EOB-DTPA-enhanced magnetic resonance imaging and magnetic resonance elastography in the detection and staging of hepatic fibrosis. Medicine (Baltimore) 2017; 96(42): e8339.
[http://dx.doi.org/10.1097/MD.0000000000008339] [PMID: 29049250]
[36]
Yang L, Ding Y, Rao S, et al. Staging liver fibrosis in chronic hepatitis B with T1 relaxation time index on gadoxetic acid-enhanced MRI: Comparison with aspartate aminotransferase-to-platelet ratio index and FIB-4. J Magn Reson Imaging 2017; 45(4): 1186-94.
[http://dx.doi.org/10.1002/jmri.25440] [PMID: 27563840]
[37]
Swets JA. Measuring the accuracy of diagnostic systems. Science 1988; 240(4857): 1285-93.
[http://dx.doi.org/10.1126/science.3287615] [PMID: 3287615]
[38]
Kim YS, Jang YN, Song JS. Comparison of gradient-recalled echo and spin-echo echo-planar imaging MR elastography in staging liver fibrosis: A meta-analysis. Eur Radiol 2018; 28(4): 1709-18.
[http://dx.doi.org/10.1007/s00330-017-5149-5] [PMID: 29164384]
[39]
Serai SD, Trout AT. Can MR elastography be used to measure liver stiffness in patients with iron overload? Abdom Radiol (NY) 2019; 44(1): 104-9.
[http://dx.doi.org/10.1007/s00261-018-1723-9] [PMID: 30066167]
[40]
Jiang H, Chen J, Gao R, Huang Z, Wu M, Song B. Liver fibrosis staging with diffusion-weighted imaging: A systematic review and meta-analysis. Abdom Radiol (NY) 2017; 42(2): 490-501.
[http://dx.doi.org/10.1007/s00261-016-0913-6] [PMID: 27678393]
[41]
Yang L, Rao S, Wang W, et al. Staging liver fibrosis with DWI: is there an added value for diffusion kurtosis imaging? Eur Radiol 2018; 28(7): 3041-9.
[http://dx.doi.org/10.1007/s00330-017-5245-6] [PMID: 29383522]
[42]
Taouli B, Koh D-M. Diffusion-weighted MR imaging of the liver. Radiology 2010; 254(1): 47-66.
[http://dx.doi.org/10.1148/radiol.09090021] [PMID: 20032142]
[43]
Zhu L, Pan Z, Ma Q, et al. Diffusion kurtosis imaging study of rectal adenocarcinoma associated with histopathologic prognostic factors: Preliminary findings. Radiology 2017; 284(1): 66-76.
[http://dx.doi.org/10.1148/radiol.2016160094] [PMID: 27929929]
[44]
Goshima S, Kanematsu M, Noda Y, Kondo H, Watanabe H, Bae KT. Diffusion kurtosis imaging to assess response to treatment in hypervascular hepatocellular carcinoma. AJR Am J Roentgenol 2015; 204(5): W543-9.
[http://dx.doi.org/10.2214/AJR.14.13235] [PMID: 25905960]
[45]
Anderson SW, Barry B, Soto J, Ozonoff A, O’Brien M, Jara H. Characterizing non-gaussian, high b-value diffusion in liver fibrosis: Stretched exponential and diffusional kurtosis modeling. J Magn Reson Imaging 2014; 39(4): 827-34.
[http://dx.doi.org/10.1002/jmri.24234] [PMID: 24259401]
[46]
Taouli B, Chouli M, Martin AJ, Qayyum A, Coakley FV, Vilgrain V. Chronic hepatitis: role of diffusion-weighted imaging and diffusion tensor imaging for the diagnosis of liver fibrosis and inflammation. J Magn Reson Imaging 2008; 28(1): 89-95.
[http://dx.doi.org/10.1002/jmri.21227] [PMID: 18581382]
[47]
Kaur M, Singh D. Fusion of medical images using deep belief networks. Cluster Comput 2020; 23(2): 1439-53.
[http://dx.doi.org/10.1007/s10586-019-02999-x]
[48]
Razmjooy N, Ashourian M, Karimifard M, et al. Computer-aided diagnosis of skin cancer: A review. Curr. Med. Imaging 2020; p. 16.
[49]
Xie Q, Zhou X, Huang P, Wei J, Wang W, Zheng S. The performance of enhanced liver fibrosis (ELF) test for the staging of liver fibrosis: A meta-analysis. PLoS One 2014; 9(4): e92772.
[http://dx.doi.org/10.1371/journal.pone.0092772] [PMID: 24736610]
[50]
Afdhal NH, Nunes D. Evaluation of liver fibrosis: A concise review. Am J Gastroenterol 2004; 99(6): 1160-74.
[http://dx.doi.org/10.1111/j.1572-0241.2004.30110.x] [PMID: 15180741]
[51]
Nassif A, Jia J, Keiser M, et al. Visualization of hepatic uptake transporter function in healthy subjects by using gadoxetic acid-enhanced MR imaging. Radiology 2012; 264(3): 741-50.
[http://dx.doi.org/10.1148/radiol.12112061] [PMID: 22771883]