Differential diagnostic efficacy of Gd-EOB-DTPA-enhanced magnetic resonance imaging for dysplastic nodules and hepatocellular carcinoma: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

LI Wenjing ^1,2,3,4,5 , XU Yongsheng ^2,3,4 ,  LEI Junqiang ^2,3,4

1. First Clinical Medical College of Lanzhou University, Lanzhou 730000, P. R. China;
2. Department of Radiology, the First Hospital of Lanzhou University, Lanzhou 730013, P. R. China;
3. Gansu Province Clinical Research Center for Radiology Imaging, Lanzhou 730013, P. R. China;
4. Intelligent Imaging Medical Engineering Research Center of Gansu Province, Lanzhou 730013, P. R. China;
5. EMB Center of Lanzhou University, Lanzhou 730000, P. R. China;

Corresponding author：

LEI Junqiang, Email: leijq1990@163.com

Keywords：

Gadolinium ethoxybenzyl DTPA; Gd-EOB-DTPA; Magnetic resonance imaging; Dysplastic nodules; Hepatocellular carcinoma; Diagnostic imaging; Meta-analysis

DOI：

10.7507/1672-2531.202306128

Video：

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Objective To systematically review the overall diagnostic efficacy of Gd-EOB-DTPA-enhanced MRI in differentiating dysplastic nodules (DNs) and hepatocellular carcinoma (HCC), exploring whether the hepatobiliary phase can effectively improve diagnostic accuracy. Methods The PubMed, Embase, Web of Science, Cochrane Library, CNKI, WanFang Data, and CBM databases were searched from January 1998 to March 2023 to identify original studies on Gd-EOB-DTPA-enhanced MRI for the differential diagnosis of DNs and HCC. Two investigators independently performed literature screening, extraction of data features and quality assessment. Meta-analysis was performed using Stata 17.0 and Meta-disc1.4 software. Results A total of 14 papers were included in this meta-analysis, including 375 DNs and 653 HCC. The results of meta-analysis showed that, in the multiparametric diagnostic sequence, the pooled Sen, Spe, PLR, NLR and AUC were 0.95 (95%CI 0.87 to 0.98), 0.95 (95%CI 0.91 to 0.97), 18.57 (95%CI 9.64 to 35.78), 0.06 (95%CI 0.02 to 0.14) and 0.98 (95%CI 0.97 to 0.99), respectively. Conclusion Gd-EOB-DTPA-enhanced MRI has a good differential diagnostic value for DNs and HCC. Hepatobiliary phase imaging also greatly compensates for the diagnostic deficiency of dynamic enhancement with low sensitivity for early HCC.

Citation： LI Wenjing, XU Yongsheng, LEI Junqiang. Differential diagnostic efficacy of Gd-EOB-DTPA-enhanced magnetic resonance imaging for dysplastic nodules and hepatocellular carcinoma: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2023, 23(12): 1400-1406. doi: 10.7507/1672-2531.202306128 Copy

1.	Caldwell S, Park SH. The epidemiology of hepatocellular cancer: from the perspectives of public health problem to tumor biology. J Gastroenterol, 2009, 44(Suppl 19): 96-101.
2.	International Consensus Group for Hepatocellular Neoplasia, The International Consensus Group for Hepatocellular Neoplasia. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology, 2009, 492(2): 658-664.
3.	Hwang J, Kim YK, Jeong WK, et al. Nonhypervascular hypointense nodules at gadoxetic acid-enhanced MR imaging in chronic liver disease: diffusion-weighted imaging for characterization. Radiology. 2015, 276(1): 137-146.
4.	Sato T, Kondo F, Ebara M, et al. Natural history of large regenerative nodules and dysplastic nodules in liver cirrhosis: 28-year follow-up study. Hepatol Int, 2015, 9(2): 330-336.
5.	Di Tommaso L, Sangiovanni A, Borzio M, et al. Advanced precancerous lesions in the liver. Best Pract Res Clin Gastroenterol, 2013, 27(2): 269-284.
6.	Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part I. Development, growth, and spread: key pathologic and imaging aspects. Radiology, 2014, 272(3): 635-654.
7.	Garrett R. Solid liver masses: approach to management from the standpoint of a radiologist. Curr Gastroenterol Rep, 2013, 15(12): 359.
8.	Bluemke DA, Sahani D, Amendola M, et al. Efficacy and safety of MR imaging with liver-specific contrast agent: U. S. multicenter phase Ⅲ study. Radiology, 2005, 237(1): 89-98.
9.	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): 785-792.
10.	高芬, 蔡萍, 刘晨, 等. 肝细胞癌癌前结节影像学特征的研究进展. 中华肝脏病杂志, 2020, 28(1): 9-13.
11.	Granito A, Galassi M, Piscaglia F, et al. Impact of gadoxetic acid (Gd-EOB-DTPA)-enhanced magnetic resonance on the non-invasive diagnosis of small hepatocellular carcinoma: a prospective study. Aliment Pharmacol Ther, 2013, 37(3): 355-363.
12.	Renzulli M, Biselli M, Brocchi S, et al. New hallmark of hepatocellular carcinoma, early hepatocellular carcinoma and high-grade dysplastic nodules on Gd-EOB-DTPA MRI in patients with cirrhosis: a new diagnostic algorithm. Gut, 2018, 67(9): 1674-1682.
13.	Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med, 2011, 155(8): 529-536.
14.	Chou CT, Chen YL, Su WW, et al. Characterization of cirrhotic nodules with gadoxetic acid-enhanced magnetic resonance imaging: the efficacy of hepatocyte-phase imaging. J Magn Reson Imaging, 2010, 32(4): 895-902.
15.	Chou CT, Chen YL, Wu HK, et al. Characterization of hyperintense nodules on precontrast T1-weighted MRI: utility of gadoxetic acid-enhanced hepatocyte-phase imaging. J Magn Reson Imaging, 2011, 33(3): 625-632.
16.	Wang YC, Chou CT, Lin CP, et al. The value of Gd-EOB-DTPA-enhanced MR imaging in characterizing cirrhotic nodules with atypical enhancement on Gd-DTPA-enhanced MR images. PLoS One, 2017, 12(3): e0174594.
17.	Zhong X, Tang H, Lu B, et al. Differentiation of small hepatocellular carcinoma from dysplastic nodules in cirrhotic liver: texture analysis based on MRI improved performance in comparison over gadoxetic acid-enhanced MR and diffusion-weighted imaging. Front Oncol, 2020, 9(2): 1382.
18.	Chou CT, Wu WP, Chen CB, et al. The utility of gadoxetic acid-enhanced MR imaging to characterize atypical cirrhotic nodules detected on dynamic CT images. PLoS One, 2014, 9(10): e107869.
19.	杨健, 柏玉涵, 时昭红, 等. Gd-EOB-DTPA多模态MRI对常规MRI不典型强化肝硬化结节的诊断价值. 中国医学影像学杂志, 2019, 27(9): 695-699.
20.	田玉亭, 李代欣, 付志浩, 等. 钆塞酸二钠磁共振成像表观弥散系数值联合最大强化率鉴别肝硬化背景下不典型增生结节与小肝癌. 中国肝脏病杂志(电子版), 2020, 12(4): 17-22.
21.	杨健, 柏玉涵. Gd-EOB-DTPA增强MRI对CT不典型强化肝硬化结节的诊断价值. 现代临床医学, 2020, 46(4): 261-264.
22.	Bartolozzi C, Battaglia V, Bargellini I, et al. Contrast-enhanced magnetic resonance imaging of 102 nodules in cirrhosis: correlation with histological findings on explanted livers. Abdom Imaging, 2013, 38(2): 290-296.
23.	Shin SK, Kim YS, Choi SJ, et al. Characterization of small (≤3 cm) hepatic lesions with atypical enhancement feature and hypointensity in hepatobiliary phase of gadoxetic acid-enhanced MRI in cirrhosis: a STARD-compliant article. Medicine (Baltimore), 2017, 96(29): e7278.
24.	Sano K, Ichikawa T, Motosugi U, et al. Imaging study of early hepatocellular carcinoma: usefulness of gadoxetic acid-enhanced MR imaging. Radiology, 2011, 261(3): 834-844.
25.	Inoue T, Kudo M, Komuta M, et al. Assessment of Gd-EOB-DTPA-enhanced MRI for HCC and dysplastic nodules and comparison of detection sensitivity versus MDCT. J Gastroenterol, 2012, 47(9): 1036-1047.
26.	苏家威, 俞顺. 钆塞酸二钠增强扫描对钆喷酸葡胺增强磁共振成像中表现不典型肝硬化结节的诊断价值. 实用医学影像杂志, 2022, 23(3): 293-296.
27.	Xiong J, Luo J, Bian J, et al. Overall diagnostic accuracy of different MR imaging sequences for detection of dysplastic nodules: a systematic review and meta-analysis. Eur Radiol, 2022, 32(2): 1285-1296.
28.	Park MJ, Kim YK, Lee MH, et al. Validation of diagnostic criteria using gadoxetic acid-enhanced and diffusion-weighted MR imaging for small hepatocellular carcinoma (≤2.0 cm) in patients with hepatitis-induced liver cirrhosis. Acta Radiol, 2013, 54(2): 127-136.
29.	Di Martino M, Anzidei M, Zaccagna F, et al. Qualitative analysis of small (≤2 cm) regenerative nodules, dysplastic nodules and well-differentiated HCCs with gadoxetic acid MRI. BMC Med Imaging, 2016, 16(1): 62.
30.	国家卫生健康委办公厅. 原发性肝癌诊疗指南(2022年版). 浙江实用医学, 2022, 27(6): 528-536.
31.	Liu X, Jiang H, Chen J, et al. Gadoxetic acid disodium-enhanced magnetic resonance imaging outperformed multidetector computed tomography in diagnosing small hepatocellular carcinoma: a meta-analysis. Liver Transpl, 2017, 23(12): 1505-1518.
32.	Lee YJ, Lee JM, Lee JS, et al. Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis. Radiology, 2015, 275(1): 97-109.
33.	Practice Guidelines Committee, American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma. Hepatology, 2005, 42(5): 1208-1236.
34.	Sangiovanni A, Manini MA, Iavarone M, et al. The diagnostic and economic impact of contrast imaging techniques in the diagnosis of small hepatocellular carcinoma in cirrhosis. Gut, 2010, 59(5): 638-644.
35.	Golfieri R, Renzulli M, Lucidi V, et al. Contribution of the hepatobiliary phase of Gd-EOB-DTPA-enhanced MRI to dynamic MRI in the detection of hypovascular small (≤ 2 cm) HCC in cirrhosis. Eur Radiol, 2011, 21(6): 1233-1242.
36.	Willatt JM, Hussain HK, Adusumilli S, et al. MR imaging of hepatocellular carcinoma in the cirrhotic liver: challenges and controversies. Radiology, 2008, 247(2): 311-330.
37.	Kogita S, Imai Y, Okada M, et al. Gd-EOB-DTPA-enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow. Eur Radiol, 2010, 20(10): 2405-2413.
38.	Schneider G, Altmeyer K, Kirchin MA, et al. Evaluation of a novel time-efficient protocol for gadobenate dimeglumine (Gd-BOPTA)-enhanced liver magnetic resonance imaging. Invest Radiol, 2007, 42(2): 105-115.
39.	Reis MA, Baroni RH. Liver-specific magnetic resonance contrast medium in the evaluation of chronic liver disease. Einstein (Sao Paulo), 2015, 13(2): 326-329.
40.	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(6): 1675-1681.
41.	Zech CJ, Ba-Ssalamah A, Berg T, et al. Consensus report from the 8th International Forum for Liver Magnetic Resonance Imaging. Eur Radiol, 2020, 30(1): 370-382.
42.	Shenoy-Bhangle A, Baliyan V, Kordbacheh H, et al. Diffusion weighted magnetic resonance imaging of liver: principles, clinical applications and recent updates. World J Hepatol, 2017, 9(26): 1081-1091.
43.	Jang MA, Kim B, Lee YK. Reporting quality of diagnostic accuracy studies in laboratory medicine: adherence to standards for reporting of diagnostic accuracy studies (STARD) 2015. Ann Lab Med, 2020, 40(3): 245-252.

1. Caldwell S, Park SH. The epidemiology of hepatocellular cancer: from the perspectives of public health problem to tumor biology. J Gastroenterol, 2009, 44(Suppl 19): 96-101.
2. International Consensus Group for Hepatocellular Neoplasia, The International Consensus Group for Hepatocellular Neoplasia. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology, 2009, 492(2): 658-664.
3. Hwang J, Kim YK, Jeong WK, et al. Nonhypervascular hypointense nodules at gadoxetic acid-enhanced MR imaging in chronic liver disease: diffusion-weighted imaging for characterization. Radiology. 2015, 276(1): 137-146.
4. Sato T, Kondo F, Ebara M, et al. Natural history of large regenerative nodules and dysplastic nodules in liver cirrhosis: 28-year follow-up study. Hepatol Int, 2015, 9(2): 330-336.
5. Di Tommaso L, Sangiovanni A, Borzio M, et al. Advanced precancerous lesions in the liver. Best Pract Res Clin Gastroenterol, 2013, 27(2): 269-284.
6. Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part I. Development, growth, and spread: key pathologic and imaging aspects. Radiology, 2014, 272(3): 635-654.
7. Garrett R. Solid liver masses: approach to management from the standpoint of a radiologist. Curr Gastroenterol Rep, 2013, 15(12): 359.
8. Bluemke DA, Sahani D, Amendola M, et al. Efficacy and safety of MR imaging with liver-specific contrast agent: U. S. multicenter phase Ⅲ study. Radiology, 2005, 237(1): 89-98.
9. 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): 785-792.
10. 高芬, 蔡萍, 刘晨, 等. 肝细胞癌癌前结节影像学特征的研究进展. 中华肝脏病杂志, 2020, 28(1): 9-13.
11. Granito A, Galassi M, Piscaglia F, et al. Impact of gadoxetic acid (Gd-EOB-DTPA)-enhanced magnetic resonance on the non-invasive diagnosis of small hepatocellular carcinoma: a prospective study. Aliment Pharmacol Ther, 2013, 37(3): 355-363.
12. Renzulli M, Biselli M, Brocchi S, et al. New hallmark of hepatocellular carcinoma, early hepatocellular carcinoma and high-grade dysplastic nodules on Gd-EOB-DTPA MRI in patients with cirrhosis: a new diagnostic algorithm. Gut, 2018, 67(9): 1674-1682.
13. Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med, 2011, 155(8): 529-536.
14. Chou CT, Chen YL, Su WW, et al. Characterization of cirrhotic nodules with gadoxetic acid-enhanced magnetic resonance imaging: the efficacy of hepatocyte-phase imaging. J Magn Reson Imaging, 2010, 32(4): 895-902.
15. Chou CT, Chen YL, Wu HK, et al. Characterization of hyperintense nodules on precontrast T1-weighted MRI: utility of gadoxetic acid-enhanced hepatocyte-phase imaging. J Magn Reson Imaging, 2011, 33(3): 625-632.
16. Wang YC, Chou CT, Lin CP, et al. The value of Gd-EOB-DTPA-enhanced MR imaging in characterizing cirrhotic nodules with atypical enhancement on Gd-DTPA-enhanced MR images. PLoS One, 2017, 12(3): e0174594.
17. Zhong X, Tang H, Lu B, et al. Differentiation of small hepatocellular carcinoma from dysplastic nodules in cirrhotic liver: texture analysis based on MRI improved performance in comparison over gadoxetic acid-enhanced MR and diffusion-weighted imaging. Front Oncol, 2020, 9(2): 1382.
18. Chou CT, Wu WP, Chen CB, et al. The utility of gadoxetic acid-enhanced MR imaging to characterize atypical cirrhotic nodules detected on dynamic CT images. PLoS One, 2014, 9(10): e107869.
19. 杨健, 柏玉涵, 时昭红, 等. Gd-EOB-DTPA多模态MRI对常规MRI不典型强化肝硬化结节的诊断价值. 中国医学影像学杂志, 2019, 27(9): 695-699.
20. 田玉亭, 李代欣, 付志浩, 等. 钆塞酸二钠磁共振成像表观弥散系数值联合最大强化率鉴别肝硬化背景下不典型增生结节与小肝癌. 中国肝脏病杂志(电子版), 2020, 12(4): 17-22.
21. 杨健, 柏玉涵. Gd-EOB-DTPA增强MRI对CT不典型强化肝硬化结节的诊断价值. 现代临床医学, 2020, 46(4): 261-264.
22. Bartolozzi C, Battaglia V, Bargellini I, et al. Contrast-enhanced magnetic resonance imaging of 102 nodules in cirrhosis: correlation with histological findings on explanted livers. Abdom Imaging, 2013, 38(2): 290-296.
23. Shin SK, Kim YS, Choi SJ, et al. Characterization of small (≤3 cm) hepatic lesions with atypical enhancement feature and hypointensity in hepatobiliary phase of gadoxetic acid-enhanced MRI in cirrhosis: a STARD-compliant article. Medicine (Baltimore), 2017, 96(29): e7278.
24. Sano K, Ichikawa T, Motosugi U, et al. Imaging study of early hepatocellular carcinoma: usefulness of gadoxetic acid-enhanced MR imaging. Radiology, 2011, 261(3): 834-844.
25. Inoue T, Kudo M, Komuta M, et al. Assessment of Gd-EOB-DTPA-enhanced MRI for HCC and dysplastic nodules and comparison of detection sensitivity versus MDCT. J Gastroenterol, 2012, 47(9): 1036-1047.
26. 苏家威, 俞顺. 钆塞酸二钠增强扫描对钆喷酸葡胺增强磁共振成像中表现不典型肝硬化结节的诊断价值. 实用医学影像杂志, 2022, 23(3): 293-296.
27. Xiong J, Luo J, Bian J, et al. Overall diagnostic accuracy of different MR imaging sequences for detection of dysplastic nodules: a systematic review and meta-analysis. Eur Radiol, 2022, 32(2): 1285-1296.
28. Park MJ, Kim YK, Lee MH, et al. Validation of diagnostic criteria using gadoxetic acid-enhanced and diffusion-weighted MR imaging for small hepatocellular carcinoma (≤2.0 cm) in patients with hepatitis-induced liver cirrhosis. Acta Radiol, 2013, 54(2): 127-136.
29. Di Martino M, Anzidei M, Zaccagna F, et al. Qualitative analysis of small (≤2 cm) regenerative nodules, dysplastic nodules and well-differentiated HCCs with gadoxetic acid MRI. BMC Med Imaging, 2016, 16(1): 62.
30. 国家卫生健康委办公厅. 原发性肝癌诊疗指南(2022年版). 浙江实用医学, 2022, 27(6): 528-536.
31. Liu X, Jiang H, Chen J, et al. Gadoxetic acid disodium-enhanced magnetic resonance imaging outperformed multidetector computed tomography in diagnosing small hepatocellular carcinoma: a meta-analysis. Liver Transpl, 2017, 23(12): 1505-1518.
32. Lee YJ, Lee JM, Lee JS, et al. Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis. Radiology, 2015, 275(1): 97-109.
33. Practice Guidelines Committee, American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma. Hepatology, 2005, 42(5): 1208-1236.
34. Sangiovanni A, Manini MA, Iavarone M, et al. The diagnostic and economic impact of contrast imaging techniques in the diagnosis of small hepatocellular carcinoma in cirrhosis. Gut, 2010, 59(5): 638-644.
35. Golfieri R, Renzulli M, Lucidi V, et al. Contribution of the hepatobiliary phase of Gd-EOB-DTPA-enhanced MRI to dynamic MRI in the detection of hypovascular small (≤ 2 cm) HCC in cirrhosis. Eur Radiol, 2011, 21(6): 1233-1242.
36. Willatt JM, Hussain HK, Adusumilli S, et al. MR imaging of hepatocellular carcinoma in the cirrhotic liver: challenges and controversies. Radiology, 2008, 247(2): 311-330.
37. Kogita S, Imai Y, Okada M, et al. Gd-EOB-DTPA-enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow. Eur Radiol, 2010, 20(10): 2405-2413.
38. Schneider G, Altmeyer K, Kirchin MA, et al. Evaluation of a novel time-efficient protocol for gadobenate dimeglumine (Gd-BOPTA)-enhanced liver magnetic resonance imaging. Invest Radiol, 2007, 42(2): 105-115.
39. Reis MA, Baroni RH. Liver-specific magnetic resonance contrast medium in the evaluation of chronic liver disease. Einstein (Sao Paulo), 2015, 13(2): 326-329.
40. 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(6): 1675-1681.
41. Zech CJ, Ba-Ssalamah A, Berg T, et al. Consensus report from the 8th International Forum for Liver Magnetic Resonance Imaging. Eur Radiol, 2020, 30(1): 370-382.
42. Shenoy-Bhangle A, Baliyan V, Kordbacheh H, et al. Diffusion weighted magnetic resonance imaging of liver: principles, clinical applications and recent updates. World J Hepatol, 2017, 9(26): 1081-1091.
43. Jang MA, Kim B, Lee YK. Reporting quality of diagnostic accuracy studies in laboratory medicine: adherence to standards for reporting of diagnostic accuracy studies (STARD) 2015. Ann Lab Med, 2020, 40(3): 245-252.

Chinese Journal of Evidence-Based Medicine

Differential diagnostic efficacy of Gd-EOB-DTPA-enhanced magnetic resonance imaging for dysplastic nodules and hepatocellular carcinoma: a meta-analysis

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