Skip to main content
SpringerLink
Log in

Prognosis of Hepatocellular Carcinoma Patients Who Achieved Long-Term Recurrence-Free Survival After Curative Therapy: Impact of the ALBI Grade

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery

Abstract

Background/Aims

Some patients experience very late recurrence of HCC more than 5 years after initial therapy. We aimed to clarify the predictive factors for very late recurrence of HCC in such cases.

Methods

Among 807 HCC patients undergoing surgical resection or ablative therapy with curative intent, the patients who survived for 5 years without any recurrence were reviewed. The prognosis and possible predictive factors for late recurrence were analyzed retrospectively.

Results

A total of 184 patients survived for more than 5 years without recurrence. Among them, 61 patients experienced recurrence, at a median of 6 years after initial therapy. In univariate analysis, the pre-treatment aspartate aminotransferase, alanine aminotransferase, Child-Pugh class, and ALBI grade were not related to recurrence, but those at 5 years after treatment were significantly related to recurrence. By multivariate analysis, an ALBI grade of 2–3 at 5 years was an independent risk factor for recurrence (P < 0.0001). Moreover, variation of the ALBI grade over the 5 years after the initial treatment was significantly related to recurrence-free survival.

Conclusions

The ALBI grade is an effective index of the variation in liver function after curative therapy and may be a useful prognostic factor for the long-term recurrence-free survival of HCC patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Bruix J, Sherman M. Practice Guidelines Committee, American Association for the Study of Liver Diseases: Management of hepatocellular carcinoma: an update. Hepatology 2011;53:1020–1022.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Yu SJ. A concise review of updated guidelines regarding the management of hepatocellular carcinoma around the world: 2010-2016. Clin Mol Hepatol 2016;22:7–17.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Fan ST, Poon RT, Yeung C, Lam CM, Lo CM, Yuen WK, Ng KK, Liu CL, Chan SC. Outcomes after partial hepatectomy for hepatocellular cancer within the Milan criteria. Br J Surg 2011;98:1292–1300.

    Article  PubMed  CAS  Google Scholar 

  4. Peng ZW, Zhang YJ, Chen MS, Lin XJ, Liang HH, Shi M. Radiofrequency ablation as first-line treatment for small solitary hepatocellular carcinoma: long-term results. Eur J Surg Oncol 2010;36:1054–1060.

    Article  PubMed  Google Scholar 

  5. Sung PS, Yang H, Na GH, Hwang S, Kang D, Jang JW, Bae SH, Choi JY, Kim DG, Yoon SK, You YK. Long-term outcomes of liver resection versus transplantation for hepatocellular carcinoma in a region where living donation is a main source. Ann Transplant 2017;22:276–284.

    Article  PubMed  Google Scholar 

  6. Shen JY, Li C, Wen TF, Yan LN, Li B, Wang WT, Yang JY, Xu MQ, Nazar Highness T. Liver transplantation versus surgical resection for HCC meeting the Milan criteria. Medicine 2016; 95:52(e5756).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Zheng J, Kuk D, Gonen M, Balachandran VP, Kingham TP, Allen PJ, D’Angelica MI, Jarnagin WR, DeMatteo RP. Actual 10-years survivors after resection of hepatocellular carcinoma. Ann Surg Oncol 2017; 24:1358–1366.

    Article  PubMed  Google Scholar 

  8. Johnson PJ, Berhane S, Kagebayashi C, Satomura S, Teng M, Reeves HL, O’Beirne J, Fox R, Skowronska A, Palmer D, Yeo W, Mo F, Lai P, Inarrairaegui M, Chan SL, Sangro B, Miksad R, Tada T, Kumada T, Toyoda H. Assessment of liver function in patients with hepatocellular carcinoma: a new evidence-based approach - the ALBI grade. J Clin Oncol 2015; 33:550–558.

    Article  PubMed  Google Scholar 

  9. Kuo YH, Wang JH, Hung CH, Rau KM, Wu IP, Chen CH, Kee KM, Hu TH, Lu SN. Albumin-Bilirubin grade predicts prognosis of HCC patients with sorafenib use. J Gastroenterol Hepatol 2017;32:1975–1981.

    Article  PubMed  CAS  Google Scholar 

  10. Waked I, Berhane S, Toyoda H, Chan SL, Stem N, Palmer D, Tada Y, Yeo W, Mo F, Bettinger D, Kirstein MM, Inarrairaegui M, Gomaa A, Vogel A, Meyer T, Sangro B, Lai P, Kumada T, Johnson PJ. Transarterial chemo-embolisation of hepatocellular carcinoma: impact of liver function and vascular invasion. Br J Cancer 2017;116:448–454.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Liu PH, Hsu CY, Hsia CY, Lee YH, Chiou YY, Huang YH, Lee FY, Lin HC, Hou MC, Huo TI. ALBI and PALBI grade predict survival for HCC across treatment modalities and BCLC stages in the MELD Era. J Gastroenterol Hepatol 2017;32:879–886.

    Article  PubMed  Google Scholar 

  12. Pinato DJ, Sharma R, Allara E, Yen C, Arizumi T, Kubota K, Bettinger D, Jang JW, Smirne C, Kim YW, Kudo M, Howell J, Ramaswami R, Burlone ME, Guerra V, Thimme R, Ishizuka M, Stebbing J, Pirisi M, Carr BI. The ALBI grade provides objective hepatic reserve estimation across each BCLC stage of hepatocellular carcinoma. J Hepatol 2017; 66:338–346.

    Article  PubMed  Google Scholar 

  13. Seyama Y, Kokudo N. Assessment of liver function for safe hepatic resection. Hepatol Res 2009; 39:107–116.

    Article  PubMed  Google Scholar 

  14. Toyoda H, Lai PB, O’Beirne J, Chong CC, Berhane S, Reeves H, Manas D, Fox RP, Yeo W, Mo F, Chan AW, Tada T, Inarrairaegui M, Vogel A, Schweitzer N, Chan SL, Sangro B, Kumada T, Johnson PJ. Long-term impact of liver function of on curative therapy for hepatocellular carcinoma: application of the ALBI grade. Br J Cancer 2016; 114:744–750.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Takami Y, Ryu T, Wada Y, Saitsu H. Evaluation of intraoperative microwave coagulo-necrotic therapy (MCN) for hepatocellular carcinoma: a single center experience of 719 consecutive cases. J Hepatobiliary Pancreat Sci 2013; 20:332–341.

    Article  PubMed  Google Scholar 

  16. Ryu T, Takami Y, Tsutsumi N, Tateishi M, Mikagi K, Wada Y, Saitsu H. Simultaneous microwave coagulo-necrotic therapy (MCN) and laparoscopic splenectomy for the treatment of hepatocellular carcinoma with cirrhotic hypersplenism. Surg Today 2017;47:548–554.

    Article  PubMed  CAS  Google Scholar 

  17. Matsumoto K, Yoshimoto J, Sugo H, Kojima K, Futagawa S, Matsumoto T. Relationship between the histological degrees of hepatitis and the postoperative recurrence of hepatocellular carcinoma in patients with hepatitis C. Hepatol Res 2002;23:196–201.

    Article  PubMed  Google Scholar 

  18. Ryu T, Takami Y, Wada Y, Tateishi M, Matsushima H, Mikagi K, Saitsu H. Double- and triple-positive tumor markers predict early recurrence and poor survival in patients with hepatocellular carcinoma within the Milan criteria and Child-Pugh class A. J Gastrointest Surg 2017; 21:957–1966.

    Article  PubMed  Google Scholar 

  19. Yamamoto J, Kosuge T, Takayama T, Shimada K, Yamasaki S, Ozaki H, Yamaguchi N, Makuuchi M. Recurrence of hepatocellular carcinoma after surgery. Br J Surg 1996; 83:1219–1222.

    Article  PubMed  CAS  Google Scholar 

  20. Jwo SC, Chiu JH, Chau GY, Loong CC, Liu WY. Risk factors linked to tumor recurrence of human hepatocellular carcinoma after hepatic resection. Hepatology 1992; 16:1367–1371.

    Article  PubMed  CAS  Google Scholar 

  21. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, Sugawara Y, Minagawa M, Takayama T, Kawasaki S, Makuuchi M. Risk factors contributing early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 2003; 38:200–207.

    Article  PubMed  Google Scholar 

  22. Poon RT, Fan ST, Ng IO, Lo CM, Liu CL, Wong J. Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer 2000; 89:500–507.

    Article  PubMed  CAS  Google Scholar 

  23. Portolani N, Coniglio A, Ghidoni S, Giovanelli M, Benetti A, Tiberio GA, Giulini SM. Early and late recurrence after liver resection for hepatocellular carcinoma: prognostic and therapeutic implications. Ann Surg 2006; 243:229–235.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Yamamoto Y, Ikoma H, Morimura R, Konishi H, Murayama Y, Komatsu S, Shiozaki A, Kuriu Y, Kubota T, Nakanishi M, Ichikawa D, Fujiwara H, Okamoto K, Sakakura C, Ochiai T, Otsuji E. Optimal duration of the early and late recurrence of hepatocellular carcinoma after hepatectomy. World J Gastroenterol 2015; 21:1207–1215.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Honda K, Seike M, Oribe J, Endo M, Arakawa M, Syo H, Iwao M, Tokoro M, Nishimura J, Mori T, Yamashita T, Fukuchi S, Muro T, Murakami K. Risk factors for deterioration of long-term liver function after radiofrequency ablation therapy. World J Hepatol 2016; 8:597–604.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Ho CM, Lee PH, Shau WY, Ho MC, Wu YM, Hu RH. Survival in patients with recurrent hepatocellular carcinoma after primary hepatectomy: comparative effectiveness of treatment modalities. Surgery 2012; 151:700–709.

    Article  PubMed  Google Scholar 

  27. Huang ZY, Liang BY, Xiong M, Zhan DQ, Wei S, Wang GP, Chen YF, Chen XP. Long-term outcomes of repeat hepatic resection in patients with recurrent hepatocellular carcinoma and analysis of recurrent types and their prognosis: a single-center experience in China. Ann Surg Oncol 2012;19:2515–2525.

    Article  PubMed  Google Scholar 

  28. Yamashita Y, Yoshida Y, Kurihara T, Itoh S, Harimoto N, Ikegami T, Yoshizumi T, Uchiyama H, Shirabe K, Maehara Y. Surgical results for recurrent hepatocellular carcinoma after curative hepatectomy: repeat hepatectomy versus salvage living donor liver transplantation. Liver Transplant 2015; 21:961–968.

    Article  Google Scholar 

  29. Benson AB 3rd, Abrams TA, Ben-Josef E, Bloomston PM, Botha JF, Clary BM, Covey A, Curley SA, D’Angelica MI, Davila R, Ensminger WD, Gibbs JF, Laheru D, Malafa MP, Marrero J, Meranze SG, Mulvihill SJ, Park JO, Posey JA, Sachdev J, Salem R, Sigurdson ER, Sofocleous C, Vauthey JN, Venook AP, Goff LW, Yen Y, Zhu AX. NCCN clinical practice guidelines in oncology: hepatobiliary cancers. J Natl Compr Canc Netw 2009; 7:350–391.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Baker EH, Thompson K, McKillop IH, Cochran A, Kirks R, Vrochides D, Martinie JB, Swan RZ, Iannitti DA. Operative microwave ablation for hepatocellular carcinoma: a single center retrospective review of 219 patients. J Gastrointest Oncol 2017; 8:337–346.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Ueno S, Sakoda M, Kubo F, Hiwatashi K, Tateno T, Baba Y, Hasegawa S, Tsubouchi H, Kagoshima Liver Cancer Study Group. Surgical resection versus radiofrequency ablation for small hepatocellular carcinoma within the Milan criteria. J Hepatobiliary Pancreat Surg 2009; 16:359–366.

    Article  PubMed  Google Scholar 

Download references

Sources of Support in any Forms

None to disclose.

Author information

Authors and Affiliations

  1. Department of Hepato-Biliary-Pancreatic Surgery, Clinical Research Institute, National Hospital Organization Kyushu Medical Center, 1-8-1, Jigyohama, Chuoku, Fukuoka City, 810-8563, Japan

    Hajime Matsushima, Yuko Takami, Tomoki Ryu, Munehiro Yoshitomi, Masaki Tateishi, Yoshiyuki Wada & Hideki Saitsu

  2. Department of Surgery, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki City, 852-8501, Japan

    Hajime Matsushima

Authors
  1. Hajime Matsushima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuko Takami
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomoki Ryu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Munehiro Yoshitomi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masaki Tateishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoshiyuki Wada
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hideki Saitsu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Study conception and design: Matsushima H, Takami Y, and Saitsu H.

Acquisition of data: Matsushima H, Ryu T, Yoshitomi M, Tateishi M, and Wada Y.

Analysis and interpretation of data: Matsushima H, Takami Y, and Saitsu H.

Drafting of manuscript: Matsushima H.

Critical revision: Takami Y and Saitsu H.

Corresponding author

Correspondence to Hajime Matsushima.

Ethics declarations

This study was approved by the Ethics Committee on Clinical Investigations of Kyushu Medical Center and performed in accordance with the Declaration of Helsinki. The requirement for written informed consent was waived because of the retrospective design.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matsushima, H., Takami, Y., Ryu, T. et al. Prognosis of Hepatocellular Carcinoma Patients Who Achieved Long-Term Recurrence-Free Survival After Curative Therapy: Impact of the ALBI Grade. J Gastrointest Surg 22, 1230–1238 (2018). https://doi.org/10.1007/s11605-018-3745-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-018-3745-6

Keywords

Search

Navigation