The prognostic value of liver stiffness in patients with hepatocellular carcinoma: a meta-analysis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

HE Chao ¹ , BAI Jian ¹ ,  LUO Shuntian ²

1. Department of General Surgery, Changsha Central Hospital, University of South China, Changsha 410018, P. R. China;
2. Department of General Surgery, Zhongshan Chenxinghai Hospital, Zhongshan, Guangdong 528415, P. R. China;

Corresponding author：

LUO Shuntian, Email: 2236303745@qq.com

Keywords：

liver stiffness; hepatocellular carcinoma; prognosis; meta-analysis

DOI：

10.7507/1007-9424.202107021

Video：

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Objective To systematically evaluate the association between liver stiffness and the prognosis of patients with hepatocellular carcinoma (HCC). Methods We searched PubMed, Web of Science, Wanfang, and CNKI databases for relevant literatures about the association between liver stiffness and the prognosis of HCC patients. Then we selected eligible literatures according to the including and excluding criteria, and we used Revman 5.3 software to perform statistical analysis. Results A total of 18 articles with 3 152 HCC patients were included. Meta results showed that HCC patients with higher liver stiffness had shorter recurrence free survival time [HR=1.09, 95%CI (1.04, 1.14), P<0.000 1], lower 5-year recurrence free survival rate [OR=2.67, 95%CI (2.08, 3.44), P<0.000 01], higher 5-year recurrence rate [OR=0.19, 95%CI (0.09, 0.38), P<0.000 01], shorter overall survival time [HR=2.42, 95%CI (1.45, 4.03), P=0.000 7], and lower 5-year overall survival rate [OR=2.89, 95%CI (2.18, 3.83), P<0.000 01]. Conclusion Liver stiffness measurement can predict the prognosis of HCC patients.

Citation： HE Chao, BAI Jian, LUO Shuntian. The prognostic value of liver stiffness in patients with hepatocellular carcinoma: a meta-analysis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(5): 658-665. doi: 10.7507/1007-9424.202107021 Copy

1.	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.
2.	Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primers, 2021, 7(1): 6. doi: 10.1038/s41572-020-00240-3.
3.	Koike Y, Shiratori Y, Sato S, et al. Risk factors for recurring hepatocellular carcinoma differ according to infected hepatitis virus-an analysis of 236 consecutive patients with a single lesion. Hepatology, 2000, 32(6): 1216-1223.
4.	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): 2614-2618.
5.	刘书林, 王智, 王逸敏, 等. CT动脉增强分数直方图参数评价肝硬变严重程度的价值. 中国普外基础与临床杂志, 2020, 27(1): 97-102.
6.	Sterling RK, Lissen E, Clumeck N, et al. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology, 2006, 43(6): 1317-1325.
7.	Xu G, Xiao Y, Jin B, et al. Liver stiffness: A novel predictor of postoperative complications in patients with hepatocellular carcinoma. J Hepatol, 2020, 73(4): 987. doi: 10.1016/j.jhep.2020.05.024.
8.	Marasco G, Colecchia A, Silva G, et al. Non-invasive tests for the prediction of primary hepatocellular carcinoma. World J Gastroenterol, 2020, 26(24): 3326-3343.
9.	Tamaki N, Higuchi M, Kurosaki M, et al. Risk assessment of hepatocellular carcinoma development by magnetic resonance elastography in chronic hepatitis C patients who achieved sustained virological responses by direct-acting antivirals. J Viral Hepat, 2019, 26(7): 893-899.
10.	Marasco G, Colecchia A, Colli A, et al. Role of liver and spleen stiffness in predicting the recurrence of hepatocellular carcinoma after resection. J Hepatol, 2019, 70(3): 440-448.
11.	Cho HJ, Kim B, Kim HJ, et al. Liver stiffness measured by MR elastography is a predictor of early HCC recurrence after treatment. Eur Radiol, 2020, 30(8): 4182-4192.
12.	周支瑞, 张天嵩, 李博, 等. 生存曲线中Meta分析适宜数据的提取与转换. 中国循证心血管医学杂志, 2014, 6(3): 243-247.
13.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
14.	Tan W, Gao M, Liu N, et al. Body mass index and risk of gallbladder cancer: systematic review and meta-analysis of observational studies. Nutrients, 2015, 7(10): 8321-8334.
15.	Liu Y, Wang X, Xiao J, et al. Prognostic value of postoperative change in liver stiffness in patients with HBV-related hepatocellular carcinoma. J Int Med Res, 2020, 48(4): 300060520908763. doi: 10.1177/0300060520908763.
16.	Rekik S, Allaire M, Mumana A, et al. Transient elastography predicts survival after radiofrequency ablation of hepatocellular carcinoma developing on cirrhosis. J Gastroenterol Hepatol, 2020, 35(1): 142-150.
17.	Abe H, Midorikawa Y, Higaki T, et al. Magnetic resonance elastography-based prediction of hepatocellular carcinoma recurrence after curative resection. Surgery, 2021, 170(1): 167-172.
18.	Kim B, Kim SS, Cho SW, et al. Liver stiffness in magnetic resonance elastography is prognostic for sorafenib-treated advanced hepatocellular carcinoma. Eur Radiol, 2021, 31(4): 2507-2517.
19.	Kim R, Jeong WK, Kang TW, et al. Intrahepatic distant recurrence after radiofrequency ablation of hepatocellular carcinoma: relationship with portal hypertension. Acta Radiol, 2019, 60(12): 1609-1618.
20.	Lee DH, Lee JM, Yi NJ, et al. Hepatic stiffness measurement by using MR elastography: prognostic values after hepatic resection for hepatocellular carcinoma. Eur Radiol, 2017, 27(4): 1713-1721.
21.	Lee DH, Lee JM, Yoon JH, et al. Liver stiffness measured by two-dimensional shear-wave elastography: Prognostic value after radiofrequency ablation for hepatocellular carcinoma. Liver Cancer, 2018, 7(1): 65-75.
22.	Lee JI, Lee HW, Kim SU, et al. Follow-up liver stiffness measurements after liver resection influence oncologic outcomes of hepatitis-b-associated hepatocellular carcinoma with liver cirrhosis. Cancers (Basel), 2019, 11(3): 425. doi: 10.3390/cancers11030425.
23.	Lee PC, Chiou YY, Chiu NC, et al. Liver stiffness measured by acoustic radiation force impulse elastography predicted prognoses of hepatocellular carcinoma after radiofrequency ablation. Sci Rep, 2020, 10(1): 2006. doi: 10.1038/s41598-020-58988-3.
24.	Lee SH, Kim SU, Jang JW, et al. Use of transient elastography to predict de novo recurrence after radiofrequency ablation for hepatocellular carcinoma. Onco Targets Ther, 2015, 8: 347-356.
25.	Lee YR, Park SY, Kim SU, et al. Using transient elastography to predict hepatocellular carcinoma recurrence after radiofrequency ablation. J Gastroenterol Hepatol, 2017, 32(5): 1079-1086.
26.	Qi M, Chen Y, Zhang GQ, et al. Clinical significance of preoperative liver stiffness measurements in primary HBV-positive hepatocellular carcinoma. Future Oncol, 2017, 13(30): 2799-2810.
27.	Shousha HI, Fouad R, Elbaz TM, et al. Predictors of recurrence and survival of hepatocellular carcinoma: A prospective study including transient elastography and cancer stem cell markers. Arab J Gastroenterol, 2020, 21(2): 95-101.
28.	Siu-Ting Lau R, Ip P, Lai-Hung Wong G, et al. Liver stiffness measurement predicts short-term and long-term outcomes in patients with hepatocellular carcinoma after curative liver resection. Surgeon, 2021 Feb 24. Online ahead of print. doi: 10.1016/j.surge.2021.01.004.
29.	Wang JH, Li WF, Yong CC, et al. Liver stiffness and insulin resistance in predicting recurrence for early stage hepatoma patients after curative resection. Sci Rep, 2021, 11(1): 6041. doi: 10.1038/s41598-021-85431-y.
30.	Xie XX, Yu YQ. Prognosis value of liver stiffness measurements by 2D-SWE in primary HBV-positive hepatocellular carcinoma following radiofrequency ablation. Translational Cancer Research, 2020, 9(4): 2518-2526.
31.	Huang Z, Huang J, Zhou T, et al. Prognostic value of liver stiffness measurement for the liver-related surgical outcomes of patients under hepatic resection: A meta-analysis. PLoS One, 2018, 13(1): e0190512. doi: 10.1371/journal.pone.0190512.
32.	Singh S, Fujii LL, Murad MH, et al. Liver stiffness is associated with risk of decompensation, liver cancer, and death in patients with chronic liver diseases: a systematic review and meta-analysis. Clin Gastroenterol Hepatol, 2013, 11(12): 1573-1584. e1-2; quiz e88-89.
33.	Oh JH, Goh MJ, Park Y, et al. Different performance of liver stiffness measurement according to etiology and outcome for the prediction of liver-related events. Dig Dis Sci, 2021, 66(8): 2816-2825.
34.	Shen Y, Wu SD, Wu L, et al. The prognostic role of liver stiffness in patients with chronic liver disease: a systematic review and dose-response meta-analysis. Hepatol Int, 2019, 13(5): 560-572.
35.	Colecchia A, Schiumerini R, Cucchetti A, et al. Prognostic factors for hepatocellular carcinoma recurrence. World J Gastroenterol, 2014, 20(20): 5935-5950.
36.	Kim BS, Seo YS, Kim YS, et al. Reduced risk of hepatocellular carcinoma by achieving a subcirrhotic liver stiffness through antiviral agents in hepatitis B virus-related advanced fibrosis or cirrhosis. J Gastroenterol Hepatol, 2018, 33(2): 503-510.
37.	Liang LY, Wong VW, Tse YK, et al. Improvement in enhanced liver fibrosis score and liver stiffness measurement reflects lower risk of hepatocellular carcinoma. Aliment Pharmacol Ther, 2019, 49(12): 1509-1517.
38.	Kumada T, Toyoda H, Yasuda S, et al. Prediction of hepatocellular carcinoma by liver stiffness measurements using magnetic resonance elastography after eradicating hepatitis C virus. Clin Transl Gastroenterol, 2021, 12(4): e00337. doi: 10.14309/ctg.0000000000000337.
39.	Ichikawa S, Motosugi U, Morisaka H, et al. Comparison of the diagnostic accuracies of magnetic resonance elastography and transient elastography for hepatic fibrosis. Magn Reson Imaging, 2015, 33(1): 26-30.
40.	Bonekamp S, Kamel I, Solga S, et al. Can imaging modalities diagnose and stage hepatic fibrosis and cirrhosis accurately? J Hepatol, 2009, 50(1): 17-35.
41.	Gu J, Zhang E, Liang B, et al. Use of direct liver stiffness measurement in evaluating the severity of liver cirrhosis in patients with hepatocellular carcinoma. World J Surg, 2020, 44(8): 2777-2783.
42.	Janssens F, Spahr L, Rubbia-Brandt L, et al. Hepatic amyloidosis increases liver stiffness measured by transient elastography. Acta Gastroenterol Belg, 2010, 73(1): 52-54.
43.	Liu K, Wong VWS, Liang LY, et al. Clinical outcomes and management of patients with chronic hepatitis B and liver stiffness measurement in the grey zone. Liver Int, 2019, 39(3): 494-502.
44.	Kim SU, Kim BK, Han KH. Clinical application of liver stiffness measurement using transient elastography: a surgical perspective. Digestion, 2013, 88(4): 258-265.
45.	Xie LT, Gu JH, Chai WL, et al. Pre-operative detection of liver fibrosis in hepatocellular carcinoma patients using 2D shear wave elastography: Where to measure? Ultrasound Med Biol, 2020, 46(6): 1412-1423.
46.	Chong CC, Wong GL, Chan AW, et al. Liver stiffness measurement predicts high-grade post-hepatectomy liver failure: A prospective cohort study. J Gastroenterol Hepatol, 2017, 32(2): 506-514.
47.	Yoon JS, Lee YR, Kweon YO, et al. Comparison of acoustic radiation force impulse elastography and transient elastography for prediction of hepatocellular carcinoma recurrence after radiofrequency ablation. Eur J Gastroenterol Hepatol, 2018, 30(10): 1230-1236.

1. 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.
2. Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primers, 2021, 7(1): 6. doi: 10.1038/s41572-020-00240-3.
3. Koike Y, Shiratori Y, Sato S, et al. Risk factors for recurring hepatocellular carcinoma differ according to infected hepatitis virus-an analysis of 236 consecutive patients with a single lesion. Hepatology, 2000, 32(6): 1216-1223.
4. 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): 2614-2618.
5. 刘书林, 王智, 王逸敏, 等. CT动脉增强分数直方图参数评价肝硬变严重程度的价值. 中国普外基础与临床杂志, 2020, 27(1): 97-102.
6. Sterling RK, Lissen E, Clumeck N, et al. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology, 2006, 43(6): 1317-1325.
7. Xu G, Xiao Y, Jin B, et al. Liver stiffness: A novel predictor of postoperative complications in patients with hepatocellular carcinoma. J Hepatol, 2020, 73(4): 987. doi: 10.1016/j.jhep.2020.05.024.
8. Marasco G, Colecchia A, Silva G, et al. Non-invasive tests for the prediction of primary hepatocellular carcinoma. World J Gastroenterol, 2020, 26(24): 3326-3343.
9. Tamaki N, Higuchi M, Kurosaki M, et al. Risk assessment of hepatocellular carcinoma development by magnetic resonance elastography in chronic hepatitis C patients who achieved sustained virological responses by direct-acting antivirals. J Viral Hepat, 2019, 26(7): 893-899.
10. Marasco G, Colecchia A, Colli A, et al. Role of liver and spleen stiffness in predicting the recurrence of hepatocellular carcinoma after resection. J Hepatol, 2019, 70(3): 440-448.
11. Cho HJ, Kim B, Kim HJ, et al. Liver stiffness measured by MR elastography is a predictor of early HCC recurrence after treatment. Eur Radiol, 2020, 30(8): 4182-4192.
12. 周支瑞, 张天嵩, 李博, 等. 生存曲线中Meta分析适宜数据的提取与转换. 中国循证心血管医学杂志, 2014, 6(3): 243-247.
13. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
14. Tan W, Gao M, Liu N, et al. Body mass index and risk of gallbladder cancer: systematic review and meta-analysis of observational studies. Nutrients, 2015, 7(10): 8321-8334.
15. Liu Y, Wang X, Xiao J, et al. Prognostic value of postoperative change in liver stiffness in patients with HBV-related hepatocellular carcinoma. J Int Med Res, 2020, 48(4): 300060520908763. doi: 10.1177/0300060520908763.
16. Rekik S, Allaire M, Mumana A, et al. Transient elastography predicts survival after radiofrequency ablation of hepatocellular carcinoma developing on cirrhosis. J Gastroenterol Hepatol, 2020, 35(1): 142-150.
17. Abe H, Midorikawa Y, Higaki T, et al. Magnetic resonance elastography-based prediction of hepatocellular carcinoma recurrence after curative resection. Surgery, 2021, 170(1): 167-172.
18. Kim B, Kim SS, Cho SW, et al. Liver stiffness in magnetic resonance elastography is prognostic for sorafenib-treated advanced hepatocellular carcinoma. Eur Radiol, 2021, 31(4): 2507-2517.
19. Kim R, Jeong WK, Kang TW, et al. Intrahepatic distant recurrence after radiofrequency ablation of hepatocellular carcinoma: relationship with portal hypertension. Acta Radiol, 2019, 60(12): 1609-1618.
20. Lee DH, Lee JM, Yi NJ, et al. Hepatic stiffness measurement by using MR elastography: prognostic values after hepatic resection for hepatocellular carcinoma. Eur Radiol, 2017, 27(4): 1713-1721.
21. Lee DH, Lee JM, Yoon JH, et al. Liver stiffness measured by two-dimensional shear-wave elastography: Prognostic value after radiofrequency ablation for hepatocellular carcinoma. Liver Cancer, 2018, 7(1): 65-75.
22. Lee JI, Lee HW, Kim SU, et al. Follow-up liver stiffness measurements after liver resection influence oncologic outcomes of hepatitis-b-associated hepatocellular carcinoma with liver cirrhosis. Cancers (Basel), 2019, 11(3): 425. doi: 10.3390/cancers11030425.
23. Lee PC, Chiou YY, Chiu NC, et al. Liver stiffness measured by acoustic radiation force impulse elastography predicted prognoses of hepatocellular carcinoma after radiofrequency ablation. Sci Rep, 2020, 10(1): 2006. doi: 10.1038/s41598-020-58988-3.
24. Lee SH, Kim SU, Jang JW, et al. Use of transient elastography to predict de novo recurrence after radiofrequency ablation for hepatocellular carcinoma. Onco Targets Ther, 2015, 8: 347-356.
25. Lee YR, Park SY, Kim SU, et al. Using transient elastography to predict hepatocellular carcinoma recurrence after radiofrequency ablation. J Gastroenterol Hepatol, 2017, 32(5): 1079-1086.
26. Qi M, Chen Y, Zhang GQ, et al. Clinical significance of preoperative liver stiffness measurements in primary HBV-positive hepatocellular carcinoma. Future Oncol, 2017, 13(30): 2799-2810.
27. Shousha HI, Fouad R, Elbaz TM, et al. Predictors of recurrence and survival of hepatocellular carcinoma: A prospective study including transient elastography and cancer stem cell markers. Arab J Gastroenterol, 2020, 21(2): 95-101.
28. Siu-Ting Lau R, Ip P, Lai-Hung Wong G, et al. Liver stiffness measurement predicts short-term and long-term outcomes in patients with hepatocellular carcinoma after curative liver resection. Surgeon, 2021 Feb 24. Online ahead of print. doi: 10.1016/j.surge.2021.01.004.
29. Wang JH, Li WF, Yong CC, et al. Liver stiffness and insulin resistance in predicting recurrence for early stage hepatoma patients after curative resection. Sci Rep, 2021, 11(1): 6041. doi: 10.1038/s41598-021-85431-y.
30. Xie XX, Yu YQ. Prognosis value of liver stiffness measurements by 2D-SWE in primary HBV-positive hepatocellular carcinoma following radiofrequency ablation. Translational Cancer Research, 2020, 9(4): 2518-2526.
31. Huang Z, Huang J, Zhou T, et al. Prognostic value of liver stiffness measurement for the liver-related surgical outcomes of patients under hepatic resection: A meta-analysis. PLoS One, 2018, 13(1): e0190512. doi: 10.1371/journal.pone.0190512.
32. Singh S, Fujii LL, Murad MH, et al. Liver stiffness is associated with risk of decompensation, liver cancer, and death in patients with chronic liver diseases: a systematic review and meta-analysis. Clin Gastroenterol Hepatol, 2013, 11(12): 1573-1584. e1-2; quiz e88-89.
33. Oh JH, Goh MJ, Park Y, et al. Different performance of liver stiffness measurement according to etiology and outcome for the prediction of liver-related events. Dig Dis Sci, 2021, 66(8): 2816-2825.
34. Shen Y, Wu SD, Wu L, et al. The prognostic role of liver stiffness in patients with chronic liver disease: a systematic review and dose-response meta-analysis. Hepatol Int, 2019, 13(5): 560-572.
35. Colecchia A, Schiumerini R, Cucchetti A, et al. Prognostic factors for hepatocellular carcinoma recurrence. World J Gastroenterol, 2014, 20(20): 5935-5950.
36. Kim BS, Seo YS, Kim YS, et al. Reduced risk of hepatocellular carcinoma by achieving a subcirrhotic liver stiffness through antiviral agents in hepatitis B virus-related advanced fibrosis or cirrhosis. J Gastroenterol Hepatol, 2018, 33(2): 503-510.
37. Liang LY, Wong VW, Tse YK, et al. Improvement in enhanced liver fibrosis score and liver stiffness measurement reflects lower risk of hepatocellular carcinoma. Aliment Pharmacol Ther, 2019, 49(12): 1509-1517.
38. Kumada T, Toyoda H, Yasuda S, et al. Prediction of hepatocellular carcinoma by liver stiffness measurements using magnetic resonance elastography after eradicating hepatitis C virus. Clin Transl Gastroenterol, 2021, 12(4): e00337. doi: 10.14309/ctg.0000000000000337.
39. Ichikawa S, Motosugi U, Morisaka H, et al. Comparison of the diagnostic accuracies of magnetic resonance elastography and transient elastography for hepatic fibrosis. Magn Reson Imaging, 2015, 33(1): 26-30.
40. Bonekamp S, Kamel I, Solga S, et al. Can imaging modalities diagnose and stage hepatic fibrosis and cirrhosis accurately? J Hepatol, 2009, 50(1): 17-35.
41. Gu J, Zhang E, Liang B, et al. Use of direct liver stiffness measurement in evaluating the severity of liver cirrhosis in patients with hepatocellular carcinoma. World J Surg, 2020, 44(8): 2777-2783.
42. Janssens F, Spahr L, Rubbia-Brandt L, et al. Hepatic amyloidosis increases liver stiffness measured by transient elastography. Acta Gastroenterol Belg, 2010, 73(1): 52-54.
43. Liu K, Wong VWS, Liang LY, et al. Clinical outcomes and management of patients with chronic hepatitis B and liver stiffness measurement in the grey zone. Liver Int, 2019, 39(3): 494-502.
44. Kim SU, Kim BK, Han KH. Clinical application of liver stiffness measurement using transient elastography: a surgical perspective. Digestion, 2013, 88(4): 258-265.
45. Xie LT, Gu JH, Chai WL, et al. Pre-operative detection of liver fibrosis in hepatocellular carcinoma patients using 2D shear wave elastography: Where to measure? Ultrasound Med Biol, 2020, 46(6): 1412-1423.
46. Chong CC, Wong GL, Chan AW, et al. Liver stiffness measurement predicts high-grade post-hepatectomy liver failure: A prospective cohort study. J Gastroenterol Hepatol, 2017, 32(2): 506-514.
47. Yoon JS, Lee YR, Kweon YO, et al. Comparison of acoustic radiation force impulse elastography and transient elastography for prediction of hepatocellular carcinoma recurrence after radiofrequency ablation. Eur J Gastroenterol Hepatol, 2018, 30(10): 1230-1236.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

The prognostic value of liver stiffness in patients with hepatocellular carcinoma: a meta-analysis

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