The value of abbreviated magnetic resonance imaging sequence in hepatocellular carcinoma screening: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

WANG Cong ^1,2 , SHI Dandan ² , LIANG Jinghong ³ ,  ZHU Shaocheng ²

1. Xinxiang Medical College, Henan Provincial People's Hospital, Xinxiang 453003, P. R. China;
2. Department of Medical Imaging, Henan Provincial People's Hospital, Zhengzhou 450003, P. R. China;
3. School of Public Health, Sun Yat-sen University, Guangzhou 510030, P. R. China;

Corresponding author：

ZHU Shaocheng, Email: zsc2686@163.com

Keywords：

Magnetic resonance imaging; Hepatocellular carcinoma; Screening; Abbreviated sequence; Meta-analysis; Systematic review

DOI：

10.7507/1672-2531.202201035

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To systematically review the diagnostic efficacy of abbreviated magnetic resonance imaging sequence (AMRI) screening for hepatocellular carcinoma (HCC). Methods PubMed, EMbase, The Cochrane Library, Web of Science, CNKI, WanFang Data and VIP databases were electronically searched to collect studies on the diagnostic efficacy of AMRI screening for HCC from inception to March 2022. Two reviewers independently screened the literature, extracted data and assessed the risk of bias of the included studies; then, meta-analysis was performed by using Stata 16.0 software. Results A total of 15 studies involving 2 823 participants were included. The results of meta-analysis showed that combined sensitivity and specificity of AMRI for HCC were 0.85 (95%CI 0.83 to 0.87) and 0.93 (95%CI 0.90 to 0.94). Subgroup analysis showed that, the combined sensitivity and specificity of NC AMRI and HBP AMRI were 0.84 (95%CI 0.81 to 0.87), 0.92 (95%CI 0.88 to 0.95) and 0.88 (95%CI 0.84 to 0.91), 0.93 (95%CI 0.91 to 0.94), respectively. The combined sensitivity and specificity of T2+DWI+HBP in HBP AMRI had the highest diagnostic efficacy. Conclusion Current evidence shows that all AMRI protocols have acceptable sensitivity and specificity for HCC screening. Among them, T2+DWI+HBP protocol shows the highest diagnostic efficiency. Due to the limited quality and quantity of the included studies, more high-quality studies are needed to verify the above conclusion.

Citation： WANG Cong, SHI Dandan, LIANG Jinghong, ZHU Shaocheng. The value of abbreviated magnetic resonance imaging sequence in hepatocellular carcinoma screening: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2022, 22(6): 641-648. doi: 10.7507/1672-2531.202201035 Copy

1.	Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primers, 2021, 7(1): 6.
2.	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
3.	Serper M, Taddei TH, Mehta R, et al. Association of provider specialty and multidisciplinary care with hepatocellular carcinoma treatment and mortality. Gastroenterology, 2017, 152(8): 1954-1964.
4.	Roayaie S, Obeidat K, Sposito C, et al. Resection of hepatocellular cancer ≤2 cm: results from two Western centers. Hepatology, 2013, 57(4): 1426-1435.
5.	Hasegawa K, Kokudo N, Makuuchi M, et al. Comparison of resection and ablation for hepatocellular carcinoma: a cohort study based on a Japanese nationwide survey. J Hepatol, 2013, 58(4): 724-729.
6.	Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American association for the study of liver diseases. Hepatology, 2018, 68(2): 723-750.
7.	European Association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol, 2018, 69(1): 182-236.
8.	Tzartzeva K, Obi J, Rich NE, et al. Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: a meta-analysis. Gastroenterology, 2018, 154(6): 1706-1718.
9.	Singal A, Volk ML, Waljee A, et al. Meta-analysis: surveillance with ultrasound for early-stage hepatocellular carcinoma in patients with cirrhosis. Aliment Pharmacol Ther, 2009, 30(1): 37-47.
10.	Kim SY, An J, Lim YS, et al. MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma. JAMA Oncol, 2017, 3(4): 456-463.
11.	国家卫生健康委办公厅. 原发性肝癌诊疗指南(2022年版). 中华外科杂志, 2022, 60(4): 273-309.
12.	Radiology ACO. CT/MRI liver imaging reporting and data system version 2018. Available at: https://www.acr.org/-/media/ACR/Files/RADS/LI-RADS/LI-RADS-2018-Core.pdf.
13.	International Consensus Group for Hepatocellular Neoplasiathe. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology, 2009, 49(2): 658-664.
14.	中国抗癌协会肝癌专业委员会, 中华医学会肝病学分会肝癌学组, 中国抗癌协会病理专业委员会, 等. 原发性肝癌规范化病理诊断指南(2015年版). 临床肝胆病杂志, 2015, 31(6): 833-839.
15.	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.
16.	Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ, 2003, 327(7414): 557-560.
17.	Van Houwelingen HC, Arends LR, Stijnen T. Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med, 2002, 21(4): 589-624.
18.	Chu H, Cole SR. Bivariate meta-analysis of sensitivity and specificity with sparse data: a generalized linear mixed model approach. J Clin Epidemiol, 2006, 59(12): 1331-1332.
19.	Reitsma JB, Glas AS, Rutjes AW, et al. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol, 2005, 58(10): 982-990.
20.	Riley RD, Abrams KR, Sutton AJ, et al. Bivariate random-effects meta-analysis and the estimation of between-study correlation. BMC Med Res Methodol, 2007, 7: 3.
21.	Deeks JJ, Macaskill P, Irwig L. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol, 2005, 58(9): 882-893.
22.	Whang S, Choi MH, Choi JI, et al. Comparison of diagnostic performance of non-contrast MRI and abbreviated MRI using gadoxetic acid in initially diagnosed hepatocellular carcinoma patients: a simulation study of surveillance for hepatocellular carcinomas. Eur Radiol, 2020, 30(8): 4150-4163.
23.	Vietti Violi N, Lewis S, Liao J, et al. Gadoxetate-enhanced abbreviated MRI is highly accurate for hepatocellular carcinoma screening. Eur Radiol, 2020, 30(11): 6003-6013.
24.	Park HJ, Jang HY, Kim SY, et al. Non-enhanced magnetic resonance imaging as a surveillance tool for hepatocellular carcinoma: Comparison with ultrasound. J Hepatol, 2020, 72(4): 718-724.
25.	Kim JS, Lee JK, Baek SY, et al. Diagnostic performance of a minimized protocol of non-contrast MRI for hepatocellular carcinoma surveillance. Abdom Radiol (NY), 2020, 45(1): 211-219.
26.	Chan MV, McDonald SJ, Ong YY, et al. HCC screening: assessment of an abbreviated non-contrast MRI protocol. Eur Radiol Exp, 2019, 3(1): 49.
27.	Brunsing RL, Chen DH, Schlein A, et al. Gadoxetate-enhanced abbreviated MRI for hepatocellular carcinoma surveillance: preliminary experience. Radiol Imaging Cancer, 2019, 1(2): e190010.
28.	Tillman BG, Gorman JD, Hru JM, et al. Diagnostic per-lesion performance of a simulated gadoxetate disodium-enhanced abbreviated MRI protocol for hepatocellular carcinoma screening. Clin Radiol, 2018, 73(5): 485-493.
29.	McNamara MM, Thomas JV, Alexander LF, et al. Diffusion-weighted MRI as a screening tool for hepatocellular carcinoma in cirrhotic livers: correlation with explant data-a pilot study. Abdom Radiol (NY), 2018, 43(10): 2686-2692.
30.	Han S, Choi JI, Park MY, et al. The diagnostic performance of liver MRI without intravenous contrast for detecting hepatocellular carcinoma: a case-controlled feasibility study. Korean J Radiol, 2018, 19(4): 568-577.
31.	Sutherland T, Watts J, Ryan M, et al. Diffusion-weighted MRI for hepatocellular carcinoma screening in chronic liver disease: Direct comparison with ultrasound screening. J Med Imaging Radiat Oncol, 2017, 61(1): 34-39.
32.	Besa C, Lewis S, Pandharipande PV, et al. Hepatocellular carcinoma detection: diagnostic performance of a simulated abbreviated MRI protocol combining diffusion-weighted and T1-weighted imaging at the delayed phase post gadoxetic acid. Abdom Radiol (NY), 2017, 42(1): 179-190.
33.	Marks RM, Ryan A, Heba ER, et al. Diagnostic per-patient accuracy of an abbreviated hepatobiliary phase gadoxetic acid-enhanced MRI for hepatocellular carcinoma surveillance. AJR Am J Roentgenol, 2015, 204(3): 527-535.
34.	Jalli R, Jafari SH, Sefidbakht S, et al. Comparison of the accuracy of DWI and ultrasonography in screening hepatocellular carcinoma in patients with chronic liver disease. Iran J Radiol, 2015, 12(1): e12708.
35.	Kim YK, Kim YK, Park HJ, et al. Noncontrast MRI with diffusion-weighted imaging as the sole imaging modality for detecting liver malignancy in patients with high risk for hepatocellular carcinoma. Magn Reson Imaging, 2014, 32(6): 610-618.
36.	王聪, 郭然, 师丹丹, 等. 肝脏特异性对比剂MRI优化序列在高风险人群中筛查小肝癌的价值研究. 磁共振成像, 2021, 12(9): 20-24.
37.	Enomoto S, Tamai H, Shingaki N, et al. Assessment of hepatocellular carcinomas using conventional magnetic resonance imaging correlated with histological differentiation and a serum marker of poor prognosis. Hepatol Int, 2011, 5(2): 730-737.
38.	Kelekis NL, Semelka RC, Worawattanakul S, et al. Hepatocellular carcinoma in North America: a multiinstitutional study of appearance on T1-weighted, T2-weighted, and serial gadolinium-enhanced gradient-echo images. AJR Am J Roentgenol, 1998, 170(4): 1005-1013.
39.	Kwee TC, Takahara T, Ochiai R, et al. Diffusion-weighted whole-body imaging with background body signal suppression (DWIBS): features and potential applications in oncology. Eur Radiol, 2008, 18(9): 1937-1952.
40.	Liu X, Zou L, Liu F, et al. Gadoxetic acid disodium-enhanced magnetic resonance imaging for the detection of hepatocellular carcinoma: a meta-analysis. PLoS One, 2013, 8(8): e70896.
41.	Andersson KL, Salomon JA, Goldie SJ, et al. Cost effectiveness of alternative surveillance strategies for hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol, 2008, 6(12): 1418-1424.
42.	Goossens N, Singal AG, King LY, et al. Cost-effectiveness of risk score-stratified hepatocellular carcinoma screening in patients with cirrhosis. Clin Transl Gastroenterol, 2017, 8(6): e101.
43.	Lima PH, Fan B, Bérubé J, et al. Cost-utility analysis of imaging for surveillance and diagnosis of hepatocellular carcinoma. AJR Am J Roentgenol, 2019, 213(1): 17-25.
44.	Rao SX, Wang J, Wang J, et al. Chinese consensus on the clinical application of hepatobiliary magnetic resonance imaging contrast agent: Gadoxetic acid disodium. J Dig Dis, 2019, 20(2): 54-61.
45.	Brunsing RL, Fowler KJ, Yokoo T, et al. Alternative approach of hepatocellular carcinoma surveillance: abbreviated MRI. Hepatoma Res, 2020, 6: 59.
46.	Ramalho J, Ramalho M. Gadolinium deposition and chronic toxicity. Magn Reson Imaging Clin N Am, 2017, 25(4): 765-778.
47.	Cerny M, Bergeron C, Billiard JS, et al. LI-RADS for MR imaging diagnosis of hepatocellular carcinoma: performance of major and ancillary features. Radiology, 2018, 288(1): 118-128.
48.	姚刚, 曹峻, 谷昊, 等. 腹腔镜与开腹肝切除术比较治疗肝癌的Meta分析. 中国循证医学杂志, 2013, 13(5): 588-595.

1. Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primers, 2021, 7(1): 6.
2. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
3. Serper M, Taddei TH, Mehta R, et al. Association of provider specialty and multidisciplinary care with hepatocellular carcinoma treatment and mortality. Gastroenterology, 2017, 152(8): 1954-1964.
4. Roayaie S, Obeidat K, Sposito C, et al. Resection of hepatocellular cancer ≤2 cm: results from two Western centers. Hepatology, 2013, 57(4): 1426-1435.
5. Hasegawa K, Kokudo N, Makuuchi M, et al. Comparison of resection and ablation for hepatocellular carcinoma: a cohort study based on a Japanese nationwide survey. J Hepatol, 2013, 58(4): 724-729.
6. Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American association for the study of liver diseases. Hepatology, 2018, 68(2): 723-750.
7. European Association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol, 2018, 69(1): 182-236.
8. Tzartzeva K, Obi J, Rich NE, et al. Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: a meta-analysis. Gastroenterology, 2018, 154(6): 1706-1718.
9. Singal A, Volk ML, Waljee A, et al. Meta-analysis: surveillance with ultrasound for early-stage hepatocellular carcinoma in patients with cirrhosis. Aliment Pharmacol Ther, 2009, 30(1): 37-47.
10. Kim SY, An J, Lim YS, et al. MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma. JAMA Oncol, 2017, 3(4): 456-463.
11. 国家卫生健康委办公厅. 原发性肝癌诊疗指南(2022年版). 中华外科杂志, 2022, 60(4): 273-309.
12. Radiology ACO. CT/MRI liver imaging reporting and data system version 2018. Available at: https://www.acr.org/-/media/ACR/Files/RADS/LI-RADS/LI-RADS-2018-Core.pdf.
13. International Consensus Group for Hepatocellular Neoplasiathe. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology, 2009, 49(2): 658-664.
14. 中国抗癌协会肝癌专业委员会, 中华医学会肝病学分会肝癌学组, 中国抗癌协会病理专业委员会, 等. 原发性肝癌规范化病理诊断指南(2015年版). 临床肝胆病杂志, 2015, 31(6): 833-839.
15. 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.
16. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ, 2003, 327(7414): 557-560.
17. Van Houwelingen HC, Arends LR, Stijnen T. Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med, 2002, 21(4): 589-624.
18. Chu H, Cole SR. Bivariate meta-analysis of sensitivity and specificity with sparse data: a generalized linear mixed model approach. J Clin Epidemiol, 2006, 59(12): 1331-1332.
19. Reitsma JB, Glas AS, Rutjes AW, et al. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol, 2005, 58(10): 982-990.
20. Riley RD, Abrams KR, Sutton AJ, et al. Bivariate random-effects meta-analysis and the estimation of between-study correlation. BMC Med Res Methodol, 2007, 7: 3.
21. Deeks JJ, Macaskill P, Irwig L. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol, 2005, 58(9): 882-893.
22. Whang S, Choi MH, Choi JI, et al. Comparison of diagnostic performance of non-contrast MRI and abbreviated MRI using gadoxetic acid in initially diagnosed hepatocellular carcinoma patients: a simulation study of surveillance for hepatocellular carcinomas. Eur Radiol, 2020, 30(8): 4150-4163.
23. Vietti Violi N, Lewis S, Liao J, et al. Gadoxetate-enhanced abbreviated MRI is highly accurate for hepatocellular carcinoma screening. Eur Radiol, 2020, 30(11): 6003-6013.
24. Park HJ, Jang HY, Kim SY, et al. Non-enhanced magnetic resonance imaging as a surveillance tool for hepatocellular carcinoma: Comparison with ultrasound. J Hepatol, 2020, 72(4): 718-724.
25. Kim JS, Lee JK, Baek SY, et al. Diagnostic performance of a minimized protocol of non-contrast MRI for hepatocellular carcinoma surveillance. Abdom Radiol (NY), 2020, 45(1): 211-219.
26. Chan MV, McDonald SJ, Ong YY, et al. HCC screening: assessment of an abbreviated non-contrast MRI protocol. Eur Radiol Exp, 2019, 3(1): 49.
27. Brunsing RL, Chen DH, Schlein A, et al. Gadoxetate-enhanced abbreviated MRI for hepatocellular carcinoma surveillance: preliminary experience. Radiol Imaging Cancer, 2019, 1(2): e190010.
28. Tillman BG, Gorman JD, Hru JM, et al. Diagnostic per-lesion performance of a simulated gadoxetate disodium-enhanced abbreviated MRI protocol for hepatocellular carcinoma screening. Clin Radiol, 2018, 73(5): 485-493.
29. McNamara MM, Thomas JV, Alexander LF, et al. Diffusion-weighted MRI as a screening tool for hepatocellular carcinoma in cirrhotic livers: correlation with explant data-a pilot study. Abdom Radiol (NY), 2018, 43(10): 2686-2692.
30. Han S, Choi JI, Park MY, et al. The diagnostic performance of liver MRI without intravenous contrast for detecting hepatocellular carcinoma: a case-controlled feasibility study. Korean J Radiol, 2018, 19(4): 568-577.
31. Sutherland T, Watts J, Ryan M, et al. Diffusion-weighted MRI for hepatocellular carcinoma screening in chronic liver disease: Direct comparison with ultrasound screening. J Med Imaging Radiat Oncol, 2017, 61(1): 34-39.
32. Besa C, Lewis S, Pandharipande PV, et al. Hepatocellular carcinoma detection: diagnostic performance of a simulated abbreviated MRI protocol combining diffusion-weighted and T1-weighted imaging at the delayed phase post gadoxetic acid. Abdom Radiol (NY), 2017, 42(1): 179-190.
33. Marks RM, Ryan A, Heba ER, et al. Diagnostic per-patient accuracy of an abbreviated hepatobiliary phase gadoxetic acid-enhanced MRI for hepatocellular carcinoma surveillance. AJR Am J Roentgenol, 2015, 204(3): 527-535.
34. Jalli R, Jafari SH, Sefidbakht S, et al. Comparison of the accuracy of DWI and ultrasonography in screening hepatocellular carcinoma in patients with chronic liver disease. Iran J Radiol, 2015, 12(1): e12708.
35. Kim YK, Kim YK, Park HJ, et al. Noncontrast MRI with diffusion-weighted imaging as the sole imaging modality for detecting liver malignancy in patients with high risk for hepatocellular carcinoma. Magn Reson Imaging, 2014, 32(6): 610-618.
36. 王聪, 郭然, 师丹丹, 等. 肝脏特异性对比剂MRI优化序列在高风险人群中筛查小肝癌的价值研究. 磁共振成像, 2021, 12(9): 20-24.
37. Enomoto S, Tamai H, Shingaki N, et al. Assessment of hepatocellular carcinomas using conventional magnetic resonance imaging correlated with histological differentiation and a serum marker of poor prognosis. Hepatol Int, 2011, 5(2): 730-737.
38. Kelekis NL, Semelka RC, Worawattanakul S, et al. Hepatocellular carcinoma in North America: a multiinstitutional study of appearance on T1-weighted, T2-weighted, and serial gadolinium-enhanced gradient-echo images. AJR Am J Roentgenol, 1998, 170(4): 1005-1013.
39. Kwee TC, Takahara T, Ochiai R, et al. Diffusion-weighted whole-body imaging with background body signal suppression (DWIBS): features and potential applications in oncology. Eur Radiol, 2008, 18(9): 1937-1952.
40. Liu X, Zou L, Liu F, et al. Gadoxetic acid disodium-enhanced magnetic resonance imaging for the detection of hepatocellular carcinoma: a meta-analysis. PLoS One, 2013, 8(8): e70896.
41. Andersson KL, Salomon JA, Goldie SJ, et al. Cost effectiveness of alternative surveillance strategies for hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol, 2008, 6(12): 1418-1424.
42. Goossens N, Singal AG, King LY, et al. Cost-effectiveness of risk score-stratified hepatocellular carcinoma screening in patients with cirrhosis. Clin Transl Gastroenterol, 2017, 8(6): e101.
43. Lima PH, Fan B, Bérubé J, et al. Cost-utility analysis of imaging for surveillance and diagnosis of hepatocellular carcinoma. AJR Am J Roentgenol, 2019, 213(1): 17-25.
44. Rao SX, Wang J, Wang J, et al. Chinese consensus on the clinical application of hepatobiliary magnetic resonance imaging contrast agent: Gadoxetic acid disodium. J Dig Dis, 2019, 20(2): 54-61.
45. Brunsing RL, Fowler KJ, Yokoo T, et al. Alternative approach of hepatocellular carcinoma surveillance: abbreviated MRI. Hepatoma Res, 2020, 6: 59.
46. Ramalho J, Ramalho M. Gadolinium deposition and chronic toxicity. Magn Reson Imaging Clin N Am, 2017, 25(4): 765-778.
47. Cerny M, Bergeron C, Billiard JS, et al. LI-RADS for MR imaging diagnosis of hepatocellular carcinoma: performance of major and ancillary features. Radiology, 2018, 288(1): 118-128.
48. 姚刚, 曹峻, 谷昊, 等. 腹腔镜与开腹肝切除术比较治疗肝癌的Meta分析. 中国循证医学杂志, 2013, 13(5): 588-595.

Chinese Journal of Evidence-Based Medicine

The value of abbreviated magnetic resonance imaging sequence in hepatocellular carcinoma screening: a meta-analysis

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content