Journal of Hepato-Biliary-Pancreatic Surgery

, Volume 15, Issue 5, pp 493–500 | Cite as

Efficacy of anatomic resection vs nonanatomic resection for small nodular hepatocellular carcinoma based on gross classification

  • Shinichi Ueno
  • Fumitake Kubo
  • Masahiko Sakoda
  • Kiyokazu Hiwatashi
  • Taro Tateno
  • Yuko Mataki
  • Kosei Maemura
  • Hiroyuki Shinchi
  • Shoji Natsugoe
  • Takashi Aikou
Original article



It has been reported that anatomic resection may be preferable to nonanatomic resection for small hepatocellular carcinomas (HCCs), by reducing socalled “micrometastases” (portal venous tumor extension and intrahepatic metastases). Nonanatomic resection or ablation has also been used as therapy for small HCCs. We studied the effectiveness of anatomic resection for small nodular HCCs, especially from the viewpoints of tumor size and gross classification.


A retrospective cohort study was performed in 116 consecutive patients who underwent curative hepatic resection for HCCs 3 cm or smaller and with three or fewer nodules. The outcome of anatomic resection (including segmentectomy, sectoriectomy, and hemihepatectomy) was compared to that of nonanatomic partial hepatectomy.


The group that underwent anatomic resection (n = 52) had relatively better overall survival and significantly better recurrence-free survival than those with nonanatomic resection (n = 64). On Cox multivariate analysis, however, liver function was more closely associated with survival. The effect of anatomic resection was more prominent in the subgroup with the nonboundary type nodules (single nodular type with extranodular growth, confluent multinodular type, and invasive type) than in the subgroup with the boundary type (vaguely nodular and single nodular type). Micrometastases in the nonboundary type were found further from the main tumor (9.5 ± 6.2 mm) than those in the boundary type (within 3.1 +-1.4 mm).


In patients with HCC nodules equal to or less than 3 cm and with the nonboundary type, anatomic resection should be employed to the extent that liver function allows, because this procedure would be more favorable than nonanatomic resection in eradicating micrometastases that have extended away from the tumor’s margin.

Key words

Hepatocellular carcinoma Anatomic resection Micrometastasis 


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  1. 1.
    Arii S, Tanaka J, Yamazoe Y, et al. Predictive factors for intrahepatic recurrence of hepatocellular carcinoma after partial hepatectomy. Cancer 1992;69:913–919.PubMedCrossRefGoogle Scholar
  2. 2.
    Vauthey JN, Klimstra D, Franceschi D, et al. Factors affecting long-term outcome after hepatic resection for hepatocellular carcinoma. Ann Surg 1995;169:28–35.CrossRefGoogle Scholar
  3. 3.
    Takayama T, Makuuchi M, Hirohashi S, et al. Early hepatocellular carcinoma as an entity with a high cure rate of surgical cure. Hepatology 1998;28:1141–1146.Google Scholar
  4. 4.
    Shimada M, Takenaka K, Taguchi K, et al. Prognostic factors after repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 1998;227:80–85.PubMedCrossRefGoogle Scholar
  5. 5.
    Ueno S, Tanabe G, Yoshida A, et al. Postoperative prediction of and strategy for metastatic recurrent hepatocellular carcinoma according to histologic activity of hepatitis. Cancer 1999;86:248–254.PubMedCrossRefGoogle Scholar
  6. 6.
    Poon RT, Fan ST, Ng IO, et al. Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer 2000;89:500–507.PubMedCrossRefGoogle Scholar
  7. 7.
    Tsai TJ, Chau GY, Lui WY, et al. Clinical significance of microscopic tumor venous invasion in patients with resectable hepatocellular carcinoma. Surgery 2000;127:603–608.PubMedCrossRefGoogle Scholar
  8. 8.
    Kondo K, Chijiiwa K, Makino I, et al. Risk factors for early death after liver resection in patients with solitary hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 2005;12:399–404.PubMedCrossRefGoogle Scholar
  9. 9.
    Minagawa M, Ikai I, Matsuyama Y, et al. Staging of hepatocellular carcinoma: assessment of the Japanese TNM and AJCC/UICC TNM systems in a cohort of 13 772 patients in Japan. Ann Surg 2007;245:909–922.PubMedCrossRefGoogle Scholar
  10. 10.
    Kosuge T, Makuuchi M, Takayama T, et al. Long-term results after resection of hepatocellular carcinoma: experience of 480 cases. Hepatogastroenterology 1993;40:328–332.PubMedGoogle Scholar
  11. 11.
    Imamura H, Matsuyama Y, Miyagawa Y, et al. Prognostic significance of anatomical resection and des-gamma-carboxy prothrombin in patients with hepatocellular carcinoma. Br J Surg 1999;86:1032–1038.PubMedCrossRefGoogle Scholar
  12. 12.
    Hasegawa K, Kokudo N, Imamura H, et al. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg 2005;242:252–259.PubMedCrossRefGoogle Scholar
  13. 13.
    Fuster J, Garcia-Valdecasas JC, Grande L, et al. Hepatocellular carcinoma and cirrhosis. Results of surgical treatment in a European series. Ann Surg 1996;223:297–302.PubMedCrossRefGoogle Scholar
  14. 14.
    Regimbeau JM, Kianmanesh R, Farges O, et al. Extent of liver resection influences the outcome in patients with cirrhosis and small hepatocellular carcinoma. Surgery 2002;131:311–317.PubMedCrossRefGoogle Scholar
  15. 15.
    Kaibori M, Matsui Y, Hijikawa T, et al. Comparison of limited and anatomic hepatic resection for hepatocellular carcinoma with hepatitis C. Surgery 2006;139:385–394.PubMedCrossRefGoogle Scholar
  16. 16.
    Yamamoto M, Takasaki K, Ohtsubo T, et al. Effectiveness of Systematized hepatectomy with Glisson’s pedicle transection at the hepatic hilus for small nodular hepatocellular carcinoma: retrospective analysis. Surgery 2001;130:443–448.PubMedCrossRefGoogle Scholar
  17. 17.
    Livraghi T, Bolondi L, Lazzaroni S, et al. Percutaneous ethanol injection in the treatment of hepatocellular carcinoma in cirrhosis. A study on 207 patients. Cancer 1992;69:925–929.PubMedCrossRefGoogle Scholar
  18. 18.
    Livraghi T, Giorgio A, Marin G, et al. Hepatocellular carcinoma and cirrhosis in 746 patients: long-term results of percutaneous ethanol injection. Radiology 1995;197:101–108.PubMedGoogle Scholar
  19. 19.
    Lin SM, Lin CJ, Lin CC, et al. Radiofrequency ablation improves prognosis compared with ethanol injection for hepatocellular carcinoma ≤ 4 cm. Gastroenterology 2004;127:1714–1723.PubMedCrossRefGoogle Scholar
  20. 20.
    Shiina S, Teratani T, Obi S, et al. A randomized controlled trial of radiofrequency ablation with ethanol injection for small hepatocellular carcinoma. Gastroenterology 2005;129:122–130.PubMedCrossRefGoogle Scholar
  21. 21.
    Aramaki M, Kawano K, Ohno T, et al. Microwave coagulation therapy for unresectable hepatocellular carcinoma. Hepatogastroenterology 2004;51:1784–1787.PubMedGoogle Scholar
  22. 22.
    Makuuchi M, Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy. Surg Gynecol Obset 1985;161:346–350.Google Scholar
  23. 23.
    Takayama T, Makuuchi M, Kubota K, et al. Randomized comparison of ultrasonic vs clamp transaction of the liver. Arch Surg 2001;136:922–928.PubMedCrossRefGoogle Scholar
  24. 24.
    Ueno S, Tanabe G, Nuruki K, et al. Prognosis of hepatocellular carcinoma associated with Child class B and C cirrhosis in relation to treatment: a multivariate analysis of 411 patients at a single center. J Hepatobiliary Pancreat Surg 2002;9:469–477.PubMedCrossRefGoogle Scholar
  25. 25.
    Yoshidome Y, Tanabe G, Ueno S, et al. Risk prediction using histology of noncancerous liver before hepatic resection for hepatocellular carcinoma. Hepatogastroenterology 2001;48:518–522.PubMedGoogle Scholar
  26. 26.
    Liver Cancer Study Group of Japan. The general rules for the clinical and pathological study of primary liver cancer. 4th ed. Tokyo: Kanehara; 2001.Google Scholar
  27. 27.
    Ueno S, Tanabe G, Nuruki K, et al. Quality of life after hepatectomy in patients with hepatocellular carcinoma: implication of change in hepatic protein synthesis. Hepatogastroenterology 2002;49:492–496.PubMedGoogle Scholar
  28. 28.
    Wakai T, Shirai Y, Sudo T, et al. Long-term outcomes of hepatectomy vs percutaneous ablation for treatment of hepatocellular carcinoma < or =4 cm. World J Gastroenterol 2006;28:546–552.Google Scholar
  29. 29.
    Takada Y, Kurata M, Ohkohchi N. Rapid and aggressive recurrence accompanied by portal tumor thrombus after radiofrequency ablation for hepatocellular carcinoma. Int J Clin Oncol 2003;8:332–335.PubMedCrossRefGoogle Scholar
  30. 30.
    Hori T, Nagata K, Hasuike S, et al. Risk factors for the local recurrence of hepatocellular carcinoma after a single session of percutaneous radiofrequency ablation. J Gastroenterol 2003;38:977–981.PubMedCrossRefGoogle Scholar
  31. 31.
    Wakai T, Shirai Y, Sakata J, et al. Anatomic resection independently improves long-term survival in patients with T1–T2 hepatocellular carcinoma. Ann Surg Oncol 2007;14:1356–1365.PubMedCrossRefGoogle Scholar
  32. 32.
    Suh KS. Systemic hepatectomy for small hepatocellular carcinoma in Korea. J Hepatobiliary Pancreat Surg 2005;12:365–370.PubMedCrossRefGoogle Scholar
  33. 33.
    Ozawa K, Takayasu T, Kumada K, et al. Experience with 225 hepatic resections for hepatocellular carcinoma over 4-year period. Am J Surg 1991;161:677–682.PubMedCrossRefGoogle Scholar
  34. 34.
    Shi M, Zhang CQ, Zhang YQ, et al. Micrometastases of solitary hepatocellular carcinoma and appropriate resection margin. World J Surg 2004;28:376–381.PubMedCrossRefGoogle Scholar
  35. 35.
    Yamanaka J, Saito S, Fujimoto J. Impact of preoperative planning using virtual segmental volumetry on liver resection for hepatocellular carcinoma. World J Surg 2007;31:1251–1257.CrossRefGoogle Scholar
  36. 36.
    Hirooka M, Iuchi H, Kurose K, et al. Abdominal virtual ultrasonographic images reconstructed by multi-detector row helical computed tomography. Eur J Radiol 2005;53:312–317.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2008

Authors and Affiliations

  • Shinichi Ueno
    • 1
  • Fumitake Kubo
    • 1
  • Masahiko Sakoda
    • 1
  • Kiyokazu Hiwatashi
    • 1
  • Taro Tateno
    • 1
  • Yuko Mataki
    • 1
  • Kosei Maemura
    • 1
  • Hiroyuki Shinchi
    • 1
  • Shoji Natsugoe
    • 1
  • Takashi Aikou
    • 1
  1. 1.Department of Surgical Oncology and Digestive Surgery, Field of Oncology, Course of Advanced TherapeuticsKagoshima University Graduate School of Medicine and Dental SciencesKagoshimaJapan

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