- Department of General Surgery, West China Hospital, Sichuan University, Chengdu 610041, China;
【Abstract】Objective To explore the different characteristics of tumor recurrence after liver transplantation (LT) and hepatectomy (HC) in patients with hepatocellular carcinoma (HCC). Methods The literatures about tumor recurrence of HCC after LT and HC were reviewed and their characteristics were compared. Results There are distinctions of recurrence rates, time, common sites between the recurred tumors after LT and HC, and their correlation factors and mechanisms of recurrence are also different. Conclusion Preventive measures should be strengthened and treatments should be more targeted according to the different characteristics of tumor recurrence after LT and HC to improve postoperative life quality and increase the survival rate.
Citation: Lu Bo,WEN Tianfu.. Comparison on Characteristics of Tumor Recurrence of Hepatocellular Carcinoma after Liver Transplantation and Hepatectomy. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2008, 15(3): 166-170. doi: Copy
1. | 68 Poon RT, Fan ST, Lo CM, et al. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation [ J ] . Ann Surg, 2002; 235(3) ∶ 373. |
2. | Jemal A, Murray T, Ward E, et al. Cancer statistics, 2005 [J]. CA Cancer J Clin, 2005; 55(1)∶10. |
3. | Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis [J]. N Engl J Med, 1996; 334(11)∶693. |
4. | Marsh JW, Dvorchik I, Bonham CA, et al. Is the pathologic TNM staging system for patients with hepatoma predictive of outcome? [J]. Cancer, 2000; 88(3)∶538. |
5. | Yao FY, Ferrell L, Bass NM, et al. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival [J]. Hepatology, 2001; 33(6)∶1394. |
6. | 严律南, 王震侠. 肝癌肝移植的适应证及应用前景 [J]. 中国普外基础与临床杂志, 2006; 13(2)∶132. |
7. | 樊嘉, 周俭, 徐泱, 等. 肝癌肝移植适应证的选择: 上海复旦标准 [J]. 中华医学杂志, 2006; 86(18)∶1227. |
8. | 吴阶平, 裘法祖主编. 黄家驷外科学(上、中、下) [M]. 第6版. 北京: 人民卫生出版社, 2000∶1230~1233. |
9. | Sun HC, Tang ZY. Preventive treatment for recurrence after curative resection of hepatocellular carcinoma——a literature review of randomized control trial [J]. World J Gasrtoenterol, 2003; 9(4)∶635. |
10. | 黄洁夫主编. 肝脏胆道肿瘤外科学 [M]. 北京: 人民卫生出版社, 1999∶673~677. |
11. | 汤钊猷, 余业勤主编. 原发性肝癌(2) [M]. 上海: 上海科学技术出版社, 1998∶438~440. |
12. | Regalia E, Fassati LR, Valente U, et al. Pattern and management of recurrent hepatocellular carcinoma after liver transplantation [J]. J Hepatobiliary Pancreat Surg, 1998; 5(1)∶29. |
13. | Roayaie S, Schwartz JD, Sung MW, et al. Recurrence of hepatocellular carcinoma after liver transplant: patterns and prognosis [J]. Liver Transpl, 2004; 10(4)∶534. |
14. | 吴天鸣, 杨翔, 贺强, 等. 肝移植治疗原发性肝癌的探讨 [J]. 临床外科杂志, 2002; 10(6)∶371. |
15. | 郑树森, 吴健, 黄东胜, 等. 肝脏移植在治疗肝脏恶性肿瘤中的作用 [J]. 中华肝胆外科杂志, 2002; 8(5)∶265. |
16. | Kumada T, Nakano S, Takeda I, et al. Patterns of recurrence after initial treatment in patients with small hepatocellular carcinoma [J]. Hepatology, 1997; 25(1)∶87. |
17. | Schlitt HJ, Neipp M, Weimann A, et al. Recurrence patterns of hepatocellular and fibrolamellar carcinoma after liver transplantation [J]. J Clin Oncol, 1999; 17(1)∶324. |
18. | Kakumu S. Trends in liver cancer researched by the Liver Cancer Study Group of Japan [J]. Hepatol Res, 2002; 24(Suppl)∶21. |
19. | Ikai I, Itai Y, Okita K, et al. Report of the 15th follow-up survey of primary liver cancer [J]. Hepatol Res, 2004; 28(1)∶21. |
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24. | Salizzoni M, Romagnoli R, Lupo F, et al. Microscopic vascular invasion detected by anti-CD34 immunohistochemistry as a predictor of recurrence of hepatocellular carcinoma after liver transplantation [J]. Transplantation, 2003; 76(5)∶844. |
25. | Shah SA, Tan JC, McGilvray ID, et al. Accuracy of staging as a predictor for recurrence after liver transplantation for hepatocellular carcinoma [J]. Transplantation, 2006; 81(12)∶1633. |
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27. | Roayaie S, Frischer JS, Emre SH, et al. Long-term results with multimodal adjuvant therapy and liver transplantation for the treatment of hepatocellular carcinomas larger than 5 centimeters [J]. Ann Surg, 2002; 235(4)∶533. |
28. | Jonas S, Bechstein WO, Steinmüller T, et al. Vascular invasion and histopathologic grading determine outcome after liver transplantation for hepatocellular carcinoma in cirrhosis [J]. Hepatology, 2001; 33(5)∶1080. |
29. | Grasso A, Stigliano R, Morisco F, et al. Liver transplantation and recurrent hepatocellular carcinoma: predictive value of nodule size in a retrospective and explant study [J]. Transplantation, 2006; 81(11)∶1532. |
30. | Pawlik TM, Delman KA, Vauthey JN, et al. Tumor size predicts vascular invasion and histologic grade: Implications for selection of surgical treatment for hepatocellular carcinoma [J]. Liver Transpl, 2005; 11(9)∶1086. |
31. | Plessier A, Codes L, Consigny Y, et al. Underestimation of the influence of satellite nodules as a risk factor for post-transplantation recurrence in patients with small hepatocellular carcinoma [J]. Liver Transpl, 2004; 10(2 Suppl 1)∶S86. |
32. | Esnaola NF,Lauwers GY,Mirza NQ, et al. Predictors of microvascular invasion in patients with hepatocellular carcinoma who are candidates for orthotopic liver transplantation [J]. J Gastrointest Surg, 2002; 6(2)∶224. |
33. | Vivarelli M, Bellusci R, Cucchetti A, et al. Low recurrence rate of hepatocellular carcinoma after liver transplantation: better patient selection or lower immunosuppression? [J]. Transplantation, 2002; 74(12)∶1746. |
34. | Herrero JI, Sangro B, Quiroga J, et al. Influence of tumor characteristics on the outcome of liver transplantation among patients with liver cirrhosis and hepatocellular carcinoma [J]. Liver Transpl, 2001; 7(7)∶631. |
35. | 黄洁夫. 肝移植治疗原发性肝癌的现状及前景 [J]. 肝胆外科杂志, 1999; 7(3)∶163. |
36. | Vivarelli M, Cucchetti A, Piscaglia F, et al. Analysis of risk factors for tumor recurrence after liver transplantation for hepatocellular carcinoma: key role of immunosuppression [J]. Liver Transpl, 2005; 11(5)∶497. |
37. | Majno P, Giostra E, Mentha G; Geneva Liver Cancer Study. Is there a customised immunosuppressive regimen for patients transplanted with hepatocellular carcinoma? [J]. J Hepatol, 2005; 43(4)∶577. |
38. | 杨甲梅, 温增庆. 肝移植术治疗原发性肝癌 [J]. 肝胆外科杂志,1999; 7(3)∶166. |
39. | Guba M,Von Breitenbuch P,Steinbauer M, et al. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor [J]. Nat Med, 2002; 8(2)∶128. |
40. | Luan FL, Hojo M, Maluccio M, et al. Rapamycin blocks tumor progression: unlinking immunosuppression from antitumor efficacy [J]. Transplantation, 2002; 73(10)∶1565. |
41. | 王征, 樊嘉, 周俭, 等. 雷帕霉素抑制肝癌细胞生长及转移的实验研究 [J]. 中华医学杂志, 2006; 86(24)∶1666. |
42. | Mazzaferro V, Battiston C, Perrone S, et al. Radiofrequency ablation of small hepatocellular carcinoma in cirrhotic patients awaiting liver transplantation: a prospective study [J]. Ann Surg, 2004; 240(5)∶900. |
43. | Fontana RJ, Hamidullah H, Nghiem H, et al. Percutaneous radiofrequency thermal ablation of hepatocellular carcinoma: a safe and effective bridge to liver transplantation [J]. Liver Transpl, 2002; 8(12)∶1165. |
44. | Ghobrial RM, Shimoda M, Farmer DG, et al. Factors determining outcome of liver transplantation for hepatocellular carcinoma associated with hepatitis C cirrhosis [J]. Transplant Proc, 2001; 33(1-2)∶1358. |
45. | Sderdahl G, Bckman L, Isoniemi H, et al. A prospective,randomized, multi-centre trial of systemic adjuvant chemotherapy versus no additional treatment in liver transplantation for hepatocellular carcinoma [J]. Transpl Int, 2006; 19(4)∶288. |
46. | Adam R, Azoulay D, Castaing D, et al. Liver resection as a bridge to transplantation for hepatocellular carcinoma on cirrhosis: a reasonable strategy? [J]. Ann Surg, 2003; 238(4)∶508. |
47. | Belghiti J, Cortes A, Abdalla EK, et al. Resection prior to liver transplantation for hepatocellular carcinoma [J]. Ann Surg, 2003; 238(6)∶885. |
48. | Knechtle SJ. Challenging choices: liver transplantation for hepatocellular carcinoma [J]. Ann Surg, 2004; 239(2)∶160. |
49. | Regimbeau JM, Abdalla EK, Vauthey JN, et al. Risk factors for early death due to recurrence after liver resection for hepatocellular carcinoma: results of a multicenter study [J]. J Surg Oncol, 2004; 85(1)∶36. |
50. | Poon RT, Fan ST, Ng IO, et al. Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma [J]. Cancer, 2000; 89(3)∶500. |
51. | 季锡清, 李朝龙, 杨进城, 等. 影响原发性肝细胞肝癌切除术预后的多因素分析 [J]. 中国普通外科杂志, 2004; 19(2)∶91. |
52. | Jwo SC, Chiu JH, Chau GY, et al. Risk factors linked to tumor recurrence of human hepatocellular carcinoma after hepatic resection [J]. Hepatology, 1992; 16(6)∶1367. |
53. | Huang YH, Wu JC, Chen CH, et al. Comparison of recurrence after hepatic resection in patients with hepatitis B vs. hepatitis C-related small hepatocellular carcinoma in hepatitis B virus endemic area [J]. Liver Int, 2005; 25(2)∶236. |
54. | Yamamoto J, Kosuge T, Takayama T, et al. Perioperative blood transfusion promotes recurrence of hepatocellular carcinoma after hepatectomy [J]. Surgery, 1994; 115(3)∶303. |
55. | Chau GY, Lui WY, Tsay SH, et al. Prognostic significance of surgical margin in hepatocellular carcinoma resection: an analysis of 165 Childs’ A patients [J]. J Surg Oncol, 1997; 66(2)∶122. |
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58. | Shi M, Zhang CQ, Zhang YQ, et al. Micrometastases of solitary hepatocellular carcinoma and appropriate resection margin [J]. World J Surg, 2004; 28(4)∶376. |
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- 1. 68 Poon RT, Fan ST, Lo CM, et al. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation [ J ] . Ann Surg, 2002; 235(3) ∶ 373.
- 2. Jemal A, Murray T, Ward E, et al. Cancer statistics, 2005 [J]. CA Cancer J Clin, 2005; 55(1)∶10.
- 3. Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis [J]. N Engl J Med, 1996; 334(11)∶693.
- 4. Marsh JW, Dvorchik I, Bonham CA, et al. Is the pathologic TNM staging system for patients with hepatoma predictive of outcome? [J]. Cancer, 2000; 88(3)∶538.
- 5. Yao FY, Ferrell L, Bass NM, et al. Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival [J]. Hepatology, 2001; 33(6)∶1394.
- 6. 严律南, 王震侠. 肝癌肝移植的适应证及应用前景 [J]. 中国普外基础与临床杂志, 2006; 13(2)∶132.
- 7. 樊嘉, 周俭, 徐泱, 等. 肝癌肝移植适应证的选择: 上海复旦标准 [J]. 中华医学杂志, 2006; 86(18)∶1227.
- 8. 吴阶平, 裘法祖主编. 黄家驷外科学(上、中、下) [M]. 第6版. 北京: 人民卫生出版社, 2000∶1230~1233.
- 9. Sun HC, Tang ZY. Preventive treatment for recurrence after curative resection of hepatocellular carcinoma——a literature review of randomized control trial [J]. World J Gasrtoenterol, 2003; 9(4)∶635.
- 10. 黄洁夫主编. 肝脏胆道肿瘤外科学 [M]. 北京: 人民卫生出版社, 1999∶673~677.
- 11. 汤钊猷, 余业勤主编. 原发性肝癌(2) [M]. 上海: 上海科学技术出版社, 1998∶438~440.
- 12. Regalia E, Fassati LR, Valente U, et al. Pattern and management of recurrent hepatocellular carcinoma after liver transplantation [J]. J Hepatobiliary Pancreat Surg, 1998; 5(1)∶29.
- 13. Roayaie S, Schwartz JD, Sung MW, et al. Recurrence of hepatocellular carcinoma after liver transplant: patterns and prognosis [J]. Liver Transpl, 2004; 10(4)∶534.
- 14. 吴天鸣, 杨翔, 贺强, 等. 肝移植治疗原发性肝癌的探讨 [J]. 临床外科杂志, 2002; 10(6)∶371.
- 15. 郑树森, 吴健, 黄东胜, 等. 肝脏移植在治疗肝脏恶性肿瘤中的作用 [J]. 中华肝胆外科杂志, 2002; 8(5)∶265.
- 16. Kumada T, Nakano S, Takeda I, et al. Patterns of recurrence after initial treatment in patients with small hepatocellular carcinoma [J]. Hepatology, 1997; 25(1)∶87.
- 17. Schlitt HJ, Neipp M, Weimann A, et al. Recurrence patterns of hepatocellular and fibrolamellar carcinoma after liver transplantation [J]. J Clin Oncol, 1999; 17(1)∶324.
- 18. Kakumu S. Trends in liver cancer researched by the Liver Cancer Study Group of Japan [J]. Hepatol Res, 2002; 24(Suppl)∶21.
- 19. Ikai I, Itai Y, Okita K, et al. Report of the 15th follow-up survey of primary liver cancer [J]. Hepatol Res, 2004; 28(1)∶21.
- 20. 林芷英, 汤钊猷, 余业勤, 等. 原发性肝癌根治切除后的复发和治疗 [J]. 中华外科杂志, 1991; 29(2)∶93.
- 21. 杨世忠, 董家鸿. 肝癌肝外转移复发的临床研究进展 [J]. 中华普通外科杂志, 2004; 19(1)∶56.
- 22. Katyal S, Oliver JH 3rd, Peterson MS, et al. Extrahepatic metastases of hepatocellular carcinoma [J]. Radiology, 2000; 216(3)∶698.
- 23. Hemming AW, Cattral MS, Reed AI, et al. Liver transplantation for hepatocellular carcinoma [J]. Ann Surg, 2001; 233(5)∶652.
- 24. Salizzoni M, Romagnoli R, Lupo F, et al. Microscopic vascular invasion detected by anti-CD34 immunohistochemistry as a predictor of recurrence of hepatocellular carcinoma after liver transplantation [J]. Transplantation, 2003; 76(5)∶844.
- 25. Shah SA, Tan JC, McGilvray ID, et al. Accuracy of staging as a predictor for recurrence after liver transplantation for hepatocellular carcinoma [J]. Transplantation, 2006; 81(12)∶1633.
- 26. Bismuth H, Majno PE, Adam R. Liver transplantation for hepatocellular carcinoma [J]. Semin Liver Dis, 1999; 19(3)∶311.
- 27. Roayaie S, Frischer JS, Emre SH, et al. Long-term results with multimodal adjuvant therapy and liver transplantation for the treatment of hepatocellular carcinomas larger than 5 centimeters [J]. Ann Surg, 2002; 235(4)∶533.
- 28. Jonas S, Bechstein WO, Steinmüller T, et al. Vascular invasion and histopathologic grading determine outcome after liver transplantation for hepatocellular carcinoma in cirrhosis [J]. Hepatology, 2001; 33(5)∶1080.
- 29. Grasso A, Stigliano R, Morisco F, et al. Liver transplantation and recurrent hepatocellular carcinoma: predictive value of nodule size in a retrospective and explant study [J]. Transplantation, 2006; 81(11)∶1532.
- 30. Pawlik TM, Delman KA, Vauthey JN, et al. Tumor size predicts vascular invasion and histologic grade: Implications for selection of surgical treatment for hepatocellular carcinoma [J]. Liver Transpl, 2005; 11(9)∶1086.
- 31. Plessier A, Codes L, Consigny Y, et al. Underestimation of the influence of satellite nodules as a risk factor for post-transplantation recurrence in patients with small hepatocellular carcinoma [J]. Liver Transpl, 2004; 10(2 Suppl 1)∶S86.
- 32. Esnaola NF,Lauwers GY,Mirza NQ, et al. Predictors of microvascular invasion in patients with hepatocellular carcinoma who are candidates for orthotopic liver transplantation [J]. J Gastrointest Surg, 2002; 6(2)∶224.
- 33. Vivarelli M, Bellusci R, Cucchetti A, et al. Low recurrence rate of hepatocellular carcinoma after liver transplantation: better patient selection or lower immunosuppression? [J]. Transplantation, 2002; 74(12)∶1746.
- 34. Herrero JI, Sangro B, Quiroga J, et al. Influence of tumor characteristics on the outcome of liver transplantation among patients with liver cirrhosis and hepatocellular carcinoma [J]. Liver Transpl, 2001; 7(7)∶631.
- 35. 黄洁夫. 肝移植治疗原发性肝癌的现状及前景 [J]. 肝胆外科杂志, 1999; 7(3)∶163.
- 36. Vivarelli M, Cucchetti A, Piscaglia F, et al. Analysis of risk factors for tumor recurrence after liver transplantation for hepatocellular carcinoma: key role of immunosuppression [J]. Liver Transpl, 2005; 11(5)∶497.
- 37. Majno P, Giostra E, Mentha G; Geneva Liver Cancer Study. Is there a customised immunosuppressive regimen for patients transplanted with hepatocellular carcinoma? [J]. J Hepatol, 2005; 43(4)∶577.
- 38. 杨甲梅, 温增庆. 肝移植术治疗原发性肝癌 [J]. 肝胆外科杂志,1999; 7(3)∶166.
- 39. Guba M,Von Breitenbuch P,Steinbauer M, et al. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor [J]. Nat Med, 2002; 8(2)∶128.
- 40. Luan FL, Hojo M, Maluccio M, et al. Rapamycin blocks tumor progression: unlinking immunosuppression from antitumor efficacy [J]. Transplantation, 2002; 73(10)∶1565.
- 41. 王征, 樊嘉, 周俭, 等. 雷帕霉素抑制肝癌细胞生长及转移的实验研究 [J]. 中华医学杂志, 2006; 86(24)∶1666.
- 42. Mazzaferro V, Battiston C, Perrone S, et al. Radiofrequency ablation of small hepatocellular carcinoma in cirrhotic patients awaiting liver transplantation: a prospective study [J]. Ann Surg, 2004; 240(5)∶900.
- 43. Fontana RJ, Hamidullah H, Nghiem H, et al. Percutaneous radiofrequency thermal ablation of hepatocellular carcinoma: a safe and effective bridge to liver transplantation [J]. Liver Transpl, 2002; 8(12)∶1165.
- 44. Ghobrial RM, Shimoda M, Farmer DG, et al. Factors determining outcome of liver transplantation for hepatocellular carcinoma associated with hepatitis C cirrhosis [J]. Transplant Proc, 2001; 33(1-2)∶1358.
- 45. Sderdahl G, Bckman L, Isoniemi H, et al. A prospective,randomized, multi-centre trial of systemic adjuvant chemotherapy versus no additional treatment in liver transplantation for hepatocellular carcinoma [J]. Transpl Int, 2006; 19(4)∶288.
- 46. Adam R, Azoulay D, Castaing D, et al. Liver resection as a bridge to transplantation for hepatocellular carcinoma on cirrhosis: a reasonable strategy? [J]. Ann Surg, 2003; 238(4)∶508.
- 47. Belghiti J, Cortes A, Abdalla EK, et al. Resection prior to liver transplantation for hepatocellular carcinoma [J]. Ann Surg, 2003; 238(6)∶885.
- 48. Knechtle SJ. Challenging choices: liver transplantation for hepatocellular carcinoma [J]. Ann Surg, 2004; 239(2)∶160.
- 49. Regimbeau JM, Abdalla EK, Vauthey JN, et al. Risk factors for early death due to recurrence after liver resection for hepatocellular carcinoma: results of a multicenter study [J]. J Surg Oncol, 2004; 85(1)∶36.
- 50. Poon RT, Fan ST, Ng IO, et al. Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma [J]. Cancer, 2000; 89(3)∶500.
- 51. 季锡清, 李朝龙, 杨进城, 等. 影响原发性肝细胞肝癌切除术预后的多因素分析 [J]. 中国普通外科杂志, 2004; 19(2)∶91.
- 52. Jwo SC, Chiu JH, Chau GY, et al. Risk factors linked to tumor recurrence of human hepatocellular carcinoma after hepatic resection [J]. Hepatology, 1992; 16(6)∶1367.
- 53. Huang YH, Wu JC, Chen CH, et al. Comparison of recurrence after hepatic resection in patients with hepatitis B vs. hepatitis C-related small hepatocellular carcinoma in hepatitis B virus endemic area [J]. Liver Int, 2005; 25(2)∶236.
- 54. Yamamoto J, Kosuge T, Takayama T, et al. Perioperative blood transfusion promotes recurrence of hepatocellular carcinoma after hepatectomy [J]. Surgery, 1994; 115(3)∶303.
- 55. Chau GY, Lui WY, Tsay SH, et al. Prognostic significance of surgical margin in hepatocellular carcinoma resection: an analysis of 165 Childs’ A patients [J]. J Surg Oncol, 1997; 66(2)∶122.
- 56. Poon RT, Fan ST, Ng IO, et al. Significance of resection margin in hepatectomy for hepatocellular carcinoma: A critical reappraisal [J]. Ann Surg, 2000; 231(4)∶544.
- 57. 徐立, 石明, 张亚奇, 等. 肝细胞癌手术切缘对患者术后复发与生存的影响 [J]. 中华肿瘤杂志, 2006; 28(1)∶47.
- 58. Shi M, Zhang CQ, Zhang YQ, et al. Micrometastases of solitary hepatocellular carcinoma and appropriate resection margin [J]. World J Surg, 2004; 28(4)∶376.
- 59. Wu CC, Ho YZ, Ho WL, et al. Preoperative transcatheter arterial chemoembolization for resectable large hepatocellular carcinoma: a reappraisal [J]. Br J Surg, 1995; 82(1)∶122.
- 60. 王槐志, 董家鸿, 王曙光, 等. 肝移植治疗原发性肝癌 [J]. 实用临床医药杂志, 2003; 7(1)∶27.
- 61. 张树民, 曾昭冲, 孙菁, 等. 肝细胞肝癌肺转移的预后因素分析 [J]. 实用肿瘤杂志, 2005; 20(5)∶395.
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