Clinical Analysis of Anatomical Resection for the Treatment of Hepatocellular Carcinoma Based on the Stratification of Liver Function
Yusuke Yamamoto
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorCorresponding Author
Hisashi Ikoma
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
[email protected]Search for more papers by this authorRyo Morimura
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorHirotaka Konishi
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorYasutoshi Murayama
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorShuhei Komatsu
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorAtsushi Shiozaki
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorYoshiaki Kuriu
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorTakeshi Kubota
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorMasayoshi Nakanishi
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorDaisuke Ichikawa
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorHitoshi Fujiwara
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorKazuma Okamoto
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorChouhei Sakakura
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorToshiya Ochiai
Department of Surgery, North Medical Center Kyoto Prefectural University of Medicine, 481 Yosanocho, Yosagun, 6292261 Kyoto, Japan
Search for more papers by this authorEigo Otsuji
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorYusuke Yamamoto
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorCorresponding Author
Hisashi Ikoma
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
[email protected]Search for more papers by this authorRyo Morimura
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorHirotaka Konishi
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorYasutoshi Murayama
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorShuhei Komatsu
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorAtsushi Shiozaki
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorYoshiaki Kuriu
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorTakeshi Kubota
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorMasayoshi Nakanishi
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorDaisuke Ichikawa
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorHitoshi Fujiwara
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorKazuma Okamoto
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorChouhei Sakakura
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorToshiya Ochiai
Department of Surgery, North Medical Center Kyoto Prefectural University of Medicine, 481 Yosanocho, Yosagun, 6292261 Kyoto, Japan
Search for more papers by this authorEigo Otsuji
Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, 6028566 Kyoto, Japan
Search for more papers by this authorAbstract
Background
This study aimed to clarify the efficacy of anatomical resection (AR) for the treatment of hepatocellular carcinoma (HCC) compared with that of nonanatomical resection (NAR) based on the stratification of liver function (LF).
Methods
The clinical records of 174 patients with a single HCC, 2–5 cm in diameter and without macroscopic vascular invasion, were analyzed. AR was performed in 132 patients and NAR was performed in 42 patients. The indocyanine green retention rate at 15 min (ICGR15) of the 78 patients classified as the good-LF group was 10–20 % and the ICGR15 of the 54 patients classified as the poor-LF group was 20–40 %.
Results
The 5-year overall survival (OS) and disease-free survival rates of the 174 patients were 67.6 and 33.4 %, respectively. Cox proportional hazard analysis identified ICGR15 ≥20 %, liver cirrhosis, α-fetoprotein ≥100 mg/dL, and infiltrating growth as independent prognostic factors. Liver cirrhosis was significantly less frequent in patients who underwent AR than in patients who underwent NAR (52 vs. 79 %, p = 0.002). In the subgroup analysis of the good-LF group, there were no significant differences in 5-year OS after AR and NAR (73.3 vs. 65.2 %, p = 0.857). By contrast, in the subgroup analysis of the poor-LF group, the 5-year OS after AR was significantly worse than after NAR (45.3 vs. 77.4 %, p = 0.044).
Conclusion
In patients with an ICGR15 ≥20 %, we recommend NAR rather than AR for the treatment of a solitary 2–5-cm-diameter HCC and without macroscopic vascular invasion.
References
- 1BoschFX, RibesJ, DiazM et al. Primary liver cancer: worldwide incidence and trends. Gastroenterology (2004) 127: S5–S161550810210.1053/j.gastro.2004.09.011
- 2LlovetJM, BustamanteJ, CastellsA et al. Natural history of untreated nonsurgical hepatocellular carcinoma: rationale for the design and evaluation of therapeutic trials. Hepatology (1999) 29: 62–67986285110.1002/hep.510290145
- 3PoonRT, NgIO, FanST et al. Clinicopathologic features of long-term survivors and disease-free survivors after resection of hepatocellular carcinoma: a study of a prospective cohort. J Clin Oncol (2001) 19: 3037–304411408499
- 4Tung-Ping PoonR, FanST, WongJ Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg (2000) 232: 10–241086219010.1097/00000658-200007000-00003
- 5YukiK, HirohashiS, SakamotoM et al. Growth and spread of hepatocellular carcinoma: a review of 240 consecutive autopsy cases. Cancer (1990) 66: 2174–2179217174810.1002/1097-0142(19901115)66:10<2174::AID-CNCR2820661022>3.0.CO;2-A
10.1002/1097-0142(19901115)66:10<2174::AID-CNCR2820661022>3.0.CO;2-A CAS PubMed Web of Science® Google Scholar
- 6MakuuchiM, HasegawaH, YamazakiS Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet (1985) 161: 346–3502996162
- 7MakuuchiM, ImamuraH, SugawaraY et al. Progress in surgical treatment of hepatocellular carcinoma. Oncology (2002) 62(Suppl 1): 74–811186879010.1159/000048280
- 8RegimbeauJM, KianmaneshR, FargesO et al. Extent of liver resection influences the outcome in patients with cirrhosis and small hepatocellular carcinoma. Surgery (2002) 131: 311–3171189403610.1067/msy.2002.121892
- 9HasegawaK, KokudoN, ImamuraH et al. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg (2005) 242: 252–2591604121610.1097/01.sla.0000171307.37401.db
- 10EguchiS, KanematsuT, AriiS et al. Comparison of the outcomes between an anatomical subsegmentectomy and a non-anatomical minor hepatectomy for single hepatocellular carcinomas based on a Japanese nationwide survey. Surgery (2008) 143: 469–4751837404310.1016/j.surg.2007.12.003
- 11YamazakiO, MatsuyamaM, HoriiK et al. Comparison of the outcomes between anatomical resection and limited resection for single hepatocellular carcinomas no larger than 5 cm in diameter: a single-center study. J Hepatobiliary Pancreat Sci (2010) 17: 349–3582046456610.1007/s00534-009-0253-9
- 12KaiboriM, MatsuiY, HijikawaT et al. Comparison of limited and anatomic hepatic resection for hepatocellular carcinoma with hepatitis C. Surgery (2006) 139: 385–3941654650410.1016/j.surg.2005.08.035
- 13ChoYB, LeeKU, LeeHW et al. Anatomic versus non-anatomic resection for small single hepatocellular carcinomas. Hepatogastroenterology (2007) 54: 1766–176918019714
- 14UenoS, KuboF, SakodaM et al. Efficacy of anatomic resection vs nonanatomic resection for small nodular hepatocellular carcinoma based on gross classification. J Hepatobiliary Pancreat Surg (2008) 15: 493–5001883680310.1007/s00534-007-1312-8
- 15WakaiT, ShiraiY, SakataJ et al. Anatomic resection independently improves long-term survival in patients with T1–T2 hepatocellular carcinoma. Ann Surg Oncol (2007) 14: 1356–13651725228910.1245/s10434-006-9318-z
- 16ImamuraH, MatsuyamaY, MiyagawaY et al. Prognostic significance of anatomical resection and des-gamma-carboxy prothrombin in patients with hepatocellular carcinoma. Br J Surg (1999) 86: 1032–10381046063910.1046/j.1365-2168.1999.01185.x
- 17KobayashiA, MiyagawaS, MiwaS et al. Prognostic impact of anatomical resection on early and late intrahepatic recurrence in patients with hepatocellular carcinoma. J Hepatobiliary Pancreat Surg (2008) 15: 515–5211883680610.1007/s00534-007-1293-7
- 18TanakaK, ShimadaH, MatsumotoC et al. Anatomic versus limited nonanatomic resection for solitary hepatocellular carcinoma. Surgery (2008) 143: 607–6151843600810.1016/j.surg.2008.01.006
- 19TomimaruY, EguchiH, MarubashiS et al. Equivalent outcomes after anatomical and non-anatomical resection of small hepatocellular carcinoma in patients with preserved liver function. Dig Dis Sci (2012) 57: 1942–19482240737710.1007/s10620-012-2114-7
- 20YamashitaY, TaketomiA, ItohS et al. Long-term favorable results of limited hepatic resections for patients with hepatocellular carcinoma: 20 years of experience. J Am Coll Surg (2007) 205: 19–261761732810.1016/j.jamcollsurg.2007.01.069
- 21KanematsuT, TakenakaK, MatsumataT et al. Limited hepatic resection effective for selected cirrhotic patients with primary liver cancer. Ann Surg (1984) 199: 51–56631867710.1097/00000658-198401000-00009
- 22HsiaCY, LuiWY, ChauGY et al. Perioperative safety and prognosis in hepatocellular carcinoma patients with impaired liver function. J Am Coll Surg (2000) 190: 574–5791080102410.1016/S1072-7515(00)00259-3
- 23FanST, LaiEC, LoCM et al. Hospital mortality of major hepatectomy for hepatocellular carcinoma associated with cirrhosis. Arch Surg (1995) 130: 198–203784809210.1001/archsurg.1995.01430020088017
- 24HemmingAW, ScudamoreCH, ShackletonCR et al. Indocyanine green clearance as a predictor of successful hepatic resection in cirrhotic patients. Am J Surg (1992) 163: 515–518157531010.1016/0002-9610(92)90400-L
- 25CouinaudC Lobe et segments hepatiques. Presse Med (1954) 62: 709–71213177441
- 26 Liver Cancer Study Group of Japan General rules for the clinical and pathological study of primary liver cancer, 2nd English edn (2003) TokyoKanehara 13–28
- 27PughRN, Murray-LyonIM, DawsonJL et al. Transection of the oesophagus for bleeding oesophageal varices. Br J Surg (1973) 60: 646–649454191310.1002/bjs.1800600817
- 28ShirabeK, ShimadaM, KajiyamaK et al. Clinicopathologic features of patients with hepatocellular carcinoma surviving >10 years after hepatic resection. Cancer (1998) 83: 2312–2316984053010.1002/(SICI)1097-0142(19981201)83:11<2312::AID-CNCR10>3.0.CO;2-6
10.1002/(SICI)1097-0142(19981201)83:11<2312::AID-CNCR10>3.0.CO;2-6 CAS PubMed Web of Science® Google Scholar
- 29MiyagawaS, MakuuchiM, KawasakiS et al. Criteria for safe hepatic resection. Am J Surg (1995) 169: 589–594777162210.1016/S0002-9610(99)80227-X
- 30PoonRT, FanST Assessment of hepatic reserve for indication of hepatic resection: how I do it. J Hepatobiliary Pancreat Surg (2005) 12: 31–371575409710.1007/s00534-004-0945-0
- 31NagasueN, UchidaM, MakinoY et al. Incidence and factors associated with intrahepatic recurrence following resection of hepatocellular carcinoma. Gastroenterology (1993) 105: 488–494839295510.1016/0016-5085(93)90150-B
- 32YamanakaN, OkamotoE, ToyosakaA et al. Prognostic factors after hepatectomy for hepatocellular carcinomas. A univariate and multivariate analysis. Cancer (1990) 65: 1104–1110
- 33YamamotoJ, KosugeT, TakayamaT et al. Perioperative blood transfusion promotes recurrence of hepatocellular carcinoma after hepatectomy. Surgery (1994) 115: 303–3098128355
- 34WickMR, MooreS, TaswellHF Non-A, non-B hepatitis associated with blood transfusion. Transfusion (1985) 25: 93–101392079210.1046/j.1537-2995.1985.25285169225.x
- 35KatzSC, ShiaJ, LiauKH et al. Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg (2009) 249: 617–6231930022710.1097/SLA.0b013e31819ed22f
- 36ColeP, MorrisonAS Basic issues in population screening for cancer. J Natl Cancer Inst (1980) 64: 1263–12726767876
- 37OchiaiT, SonoyamaT, KikuchiS et al. Anatomic wide hepatectomy for treatment of hepatocellular carcinoma. J Cancer Res Clin Oncol (2007) 133: 563–5691745761010.1007/s00432-007-0205-1
- 38CastellsA, BruixJ, BruC et al. Treatment of small hepatocellular carcinoma in cirrhotic patients: a cohort study comparing surgical resection and percutaneous ethanol injection. Hepatology (1993) 18: 1121–11268225217