Skip to main content
Top
Published in: World Journal of Surgery 1/2020

01-01-2020 | Liver Cirrhosis | Original Scientific Report

The ALBI Grade is a Good Predictive Model for Very Late Recurrence in Patients with Hepatocellular Carcinoma Undergoing Primary Resection

Authors: Chun-Yu Lin, Chih-Che Lin, Chih-Chi Wang, Chao-Long Chen, Tsung-Hui Hu, Chao-Hung Hung, Pao-Yuan Huang, Ming-Chao Tsai

Published in: World Journal of Surgery | Issue 1/2020

Login to get access

Abstract

Background

Hepatocellular carcinoma (HCC) patients still have risk for very late recurrence after curative resection. This study assesses prognostic factors in HCC patients with recurrence-free survival (RFS) for 5 years after primary resection.

Methods

We enrolled 383 HCC patients who received primary tumor resection and achieved more than 5 years without recurrence after resection between January 2001 and April 2013. Predictive factors, including albumin-bilirubin (ALBI) grade, for RFS and overall survival (OS) were analyzed.

Results

After a median follow-up of 103 months, 57 patients (14.9%) had recurrent HCC, and 14 (3.7%) died. Independent predictors for HCC recurrence were male sex (p = 0.035), pre-operative liver cirrhosis (LC) (p = 0.025), serum creatinine  > 1.5 mg/dL (p = 0.045), post-operative 5th-year alpha-fetoprotein (AFP) > 15 ng/ml (p < 0.001), LC (p = 0.004), and ALBI grades 2 and 3 (p < 0.001). I ndependent risk factors for poor survival were age >70 years (p = 0.002), post-operative 5th-year AFP > 15 ng/ml (p = 0.003), and ALBI grades 2 and 3 (p = 0.002). Patients whose deteriorated ALBI grades 5 years after resection had adverse RFS outcomes compared to those with constant (p = 0.056) and improved ALBI grades (p = 0.008). In subgroup analysis, patients with post-operative 5th-year ALBI grades 2 and 3 had significantly poorer RFS and OS (both p < 0.001) than those with grade 1 among patients with low post-operative 5th-year AFP (<15 ng/mL).

Conclusion

In HCC patients without recurrence for 5 years after curative resection, post-operative 5th-year ALBI grade is useful for predicting outcomes, even with low AFP during follow-up.
Literature
1.
go back to reference Llovet JM, Zucman-Rossi J, Pikarsky E, Sangro B, Schwartz M, Sherman M, Gores G (2016) Hepatocellular carcinoma Nat Rev Dis Primers 2:16018CrossRef Llovet JM, Zucman-Rossi J, Pikarsky E, Sangro B, Schwartz M, Sherman M, Gores G (2016) Hepatocellular carcinoma Nat Rev Dis Primers 2:16018CrossRef
2.
go back to reference Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108CrossRef Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108CrossRef
3.
go back to reference Ding XX, Zhu QG, Zhang SM, Guan L, Li T, Zhang L, Wang SY et al (2017) Precision medicine for hepatocellular carcinoma: driver mutations and targeted therapy. Oncotarget 8:55715–55730PubMedPubMedCentral Ding XX, Zhu QG, Zhang SM, Guan L, Li T, Zhang L, Wang SY et al (2017) Precision medicine for hepatocellular carcinoma: driver mutations and targeted therapy. Oncotarget 8:55715–55730PubMedPubMedCentral
4.
go back to reference Tang LSY, Covert E, Wilson E, Kottilil S (2018) Chronic Hepatitis B Infection: A Review. JAMA 319:1802–1813CrossRef Tang LSY, Covert E, Wilson E, Kottilil S (2018) Chronic Hepatitis B Infection: A Review. JAMA 319:1802–1813CrossRef
5.
go back to reference Bruix J, Sherman M, American Association for the Study of Liver D. Management of hepatocellular carcinoma: an update. Hepatology 2011;53:1020–1022.CrossRef Bruix J, Sherman M, American Association for the Study of Liver D. Management of hepatocellular carcinoma: an update. Hepatology 2011;53:1020–1022.CrossRef
6.
go back to reference Poon RT (2007) Optimal initial treatment for early hepatocellular carcinoma in patients with preserved liver function: transplantation or resection? Ann Surg Oncol 14:541–547CrossRef Poon RT (2007) Optimal initial treatment for early hepatocellular carcinoma in patients with preserved liver function: transplantation or resection? Ann Surg Oncol 14:541–547CrossRef
7.
go back to reference Poon RT, Fan ST (2004) Hepatectomy for hepatocellular carcinoma: patient selection and postoperative outcome. Liver Transpl 10:S39–45CrossRef Poon RT, Fan ST (2004) Hepatectomy for hepatocellular carcinoma: patient selection and postoperative outcome. Liver Transpl 10:S39–45CrossRef
8.
go back to reference Zheng J, Kuk D, Gonen M, Balachandran VP, Kingham TP, Allen PJ, D'Angelica MI et al (2017) Actual 10-year survivors after resection of hepatocellular carcinoma. Ann Surg Oncol 24:1358–1366CrossRef Zheng J, Kuk D, Gonen M, Balachandran VP, Kingham TP, Allen PJ, D'Angelica MI et al (2017) Actual 10-year survivors after resection of hepatocellular carcinoma. Ann Surg Oncol 24:1358–1366CrossRef
9.
go back to reference Johnson PJ, Berhane S, Kagebayashi C, Satomura S, Teng M, Reeves HL, O'Beirne J et al (2015) Assessment of liver function in patients with hepatocellular carcinoma: a new evidence-based approach-the ALBI grade. J Clin Oncol 33:550–558CrossRef Johnson PJ, Berhane S, Kagebayashi C, Satomura S, Teng M, Reeves HL, O'Beirne J et al (2015) Assessment of liver function in patients with hepatocellular carcinoma: a new evidence-based approach-the ALBI grade. J Clin Oncol 33:550–558CrossRef
10.
go back to reference Harimoto N, Yoshizumi T, Sakata K, Nagatsu A, Motomura T, Itoh S, Harada N et al (2017) Prognostic significance of combined albumin-bilirubin and tumor-node-metastasis staging system in patients who underwent hepatic resection for hepatocellular carcinoma. Hepatol Res 47:1289–1298CrossRef Harimoto N, Yoshizumi T, Sakata K, Nagatsu A, Motomura T, Itoh S, Harada N et al (2017) Prognostic significance of combined albumin-bilirubin and tumor-node-metastasis staging system in patients who underwent hepatic resection for hepatocellular carcinoma. Hepatol Res 47:1289–1298CrossRef
11.
go back to reference Bruix J, Sherman M (2005) Management of hepatocellular carcinoma. Hepatology 42:1208–1236CrossRef Bruix J, Sherman M (2005) Management of hepatocellular carcinoma. Hepatology 42:1208–1236CrossRef
12.
go back to reference Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, Christensen E, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001;35:421–430.CrossRef Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, Christensen E, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001;35:421–430.CrossRef
13.
go back to reference Heimbach JK, Kulik LM, Finn RS, Sirlin CB, Abecassis MM, Roberts LR, Zhu AX et al (2018) AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 67:358–380CrossRef Heimbach JK, Kulik LM, Finn RS, Sirlin CB, Abecassis MM, Roberts LR, Zhu AX et al (2018) AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 67:358–380CrossRef
14.
go back to reference Yamamoto Y, Ikoma H, Morimura R, Konishi H, Murayama Y, Komatsu S, Shiozaki A et al (2015) Optimal duration of the early and late recurrence of hepatocellular carcinoma after hepatectomy. World J Gastroenterol 21:1207–1215CrossRef Yamamoto Y, Ikoma H, Morimura R, Konishi H, Murayama Y, Komatsu S, Shiozaki A et al (2015) Optimal duration of the early and late recurrence of hepatocellular carcinoma after hepatectomy. World J Gastroenterol 21:1207–1215CrossRef
15.
go back to reference Toyoda H, Kumada T, Tada T, Yama T, Mizuno K, Sone Y, Maeda A et al (2017) Differences in the impact of prognostic factors for hepatocellular carcinoma over time. Cancer Sci 108:2438–2444CrossRef Toyoda H, Kumada T, Tada T, Yama T, Mizuno K, Sone Y, Maeda A et al (2017) Differences in the impact of prognostic factors for hepatocellular carcinoma over time. Cancer Sci 108:2438–2444CrossRef
16.
go back to reference Matsushima H, Takami Y, Ryu T, Yoshitomi M, Tateishi M, Wada Y, Saitsu H (2018) Prognosis of hepatocellular carcinoma patients who achieved long-term recurrence-free survival after curative therapy: impact of the ALBI grade. J Gastrointest Surg 22:1230–1238CrossRef Matsushima H, Takami Y, Ryu T, Yoshitomi M, Tateishi M, Wada Y, Saitsu H (2018) Prognosis of hepatocellular carcinoma patients who achieved long-term recurrence-free survival after curative therapy: impact of the ALBI grade. J Gastrointest Surg 22:1230–1238CrossRef
17.
go back to reference Wang Q, Fiel MI, Blank S, Luan W, Kadri H, Kim KW, Manizate F et al (2013) Impact of liver fibrosis on prognosis following liver resection for hepatitis B-associated hepatocellular carcinoma. Br J Cancer 109:573–581CrossRef Wang Q, Fiel MI, Blank S, Luan W, Kadri H, Kim KW, Manizate F et al (2013) Impact of liver fibrosis on prognosis following liver resection for hepatitis B-associated hepatocellular carcinoma. Br J Cancer 109:573–581CrossRef
18.
go back to reference Vallet-Pichard A, Mallet V, Pol S (2006) FIB-4: a simple, inexpensive and accurate marker of fibrosis in HCV-infected patients. Hepatology 44:769CrossRef Vallet-Pichard A, Mallet V, Pol S (2006) FIB-4: a simple, inexpensive and accurate marker of fibrosis in HCV-infected patients. Hepatology 44:769CrossRef
19.
go back to reference Kim WR, Berg T, Asselah T, Flisiak R, Fung S, Gordon SC, Janssen HL et al (2016) Evaluation of APRI and FIB-4 scoring systems for non-invasive assessment of hepatic fibrosis in chronic hepatitis B patients. J Hepatol 64:773–780CrossRef Kim WR, Berg T, Asselah T, Flisiak R, Fung S, Gordon SC, Janssen HL et al (2016) Evaluation of APRI and FIB-4 scoring systems for non-invasive assessment of hepatic fibrosis in chronic hepatitis B patients. J Hepatol 64:773–780CrossRef
20.
go back to reference Houot M, Ngo Y, Munteanu M, Marque S, Poynard T (2016) Systematic review with meta-analysis: direct comparisons of biomarkers for the diagnosis of fibrosis in chronic hepatitis C and B. Aliment Pharmacol Ther 43:16–29CrossRef Houot M, Ngo Y, Munteanu M, Marque S, Poynard T (2016) Systematic review with meta-analysis: direct comparisons of biomarkers for the diagnosis of fibrosis in chronic hepatitis C and B. Aliment Pharmacol Ther 43:16–29CrossRef
21.
go back to reference Li J, Gordon SC, Rupp LB, Zhang T, Boscarino JA, Vijayadeva V, Schmidt MA et al (2014) The validity of serum markers for fibrosis staging in chronic hepatitis B and C. J Viral Hepat 21:930–937CrossRef Li J, Gordon SC, Rupp LB, Zhang T, Boscarino JA, Vijayadeva V, Schmidt MA et al (2014) The validity of serum markers for fibrosis staging in chronic hepatitis B and C. J Viral Hepat 21:930–937CrossRef
22.
go back to reference Ucar F, Sezer S, Ginis Z, Ozturk G, Albayrak A, Basar O, Ekiz F et al (2013) APRI, the FIB-4 score, and Forn's index have noninvasive diagnostic value for liver fibrosis in patients with chronic hepatitis B. Eur J Gastroenterol Hepatol 25:1076–1081CrossRef Ucar F, Sezer S, Ginis Z, Ozturk G, Albayrak A, Basar O, Ekiz F et al (2013) APRI, the FIB-4 score, and Forn's index have noninvasive diagnostic value for liver fibrosis in patients with chronic hepatitis B. Eur J Gastroenterol Hepatol 25:1076–1081CrossRef
23.
go back to reference Park LS, Tate JP, Justice AC, Lo Re V, Lim JK, Brau N, Brown ST et al (2011) FIB-4 index is associated with hepatocellular carcinoma risk in HIV-infected patients. Cancer Epidemiol Biomarkers Prev 20:2512–2517CrossRef Park LS, Tate JP, Justice AC, Lo Re V, Lim JK, Brau N, Brown ST et al (2011) FIB-4 index is associated with hepatocellular carcinoma risk in HIV-infected patients. Cancer Epidemiol Biomarkers Prev 20:2512–2517CrossRef
24.
go back to reference Cheng J, Zhao P, Liu J, Liu X, Wu X (2016) Preoperative aspartate aminotransferase-to-platelet ratio index (APRI) is a predictor on postoperative outcomes of hepatocellular carcinoma. Medicine (Baltimore) 95:e5486CrossRef Cheng J, Zhao P, Liu J, Liu X, Wu X (2016) Preoperative aspartate aminotransferase-to-platelet ratio index (APRI) is a predictor on postoperative outcomes of hepatocellular carcinoma. Medicine (Baltimore) 95:e5486CrossRef
25.
go back to reference Lurie Y, Webb M, Cytter-Kuint R, Shteingart S, Lederkremer GZ (2015) Non-invasive diagnosis of liver fibrosis and cirrhosis. World J Gastroenterol 21:11567–11583CrossRef Lurie Y, Webb M, Cytter-Kuint R, Shteingart S, Lederkremer GZ (2015) Non-invasive diagnosis of liver fibrosis and cirrhosis. World J Gastroenterol 21:11567–11583CrossRef
26.
go back to reference Tatsumi C, Kudo M, Ueshima K, Kitai S, Takahashi S, Inoue T, Minami Y et al (2008) Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography. Intervirology 51(Suppl 1):27–33CrossRef Tatsumi C, Kudo M, Ueshima K, Kitai S, Takahashi S, Inoue T, Minami Y et al (2008) Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography. Intervirology 51(Suppl 1):27–33CrossRef
27.
go back to reference Denzer UW, Luth S (2009) Non-invasive diagnosis and monitoring of liver fibrosis and cirrhosis. Best Pract Res Clin Gastroenterol 23:453–460CrossRef Denzer UW, Luth S (2009) Non-invasive diagnosis and monitoring of liver fibrosis and cirrhosis. Best Pract Res Clin Gastroenterol 23:453–460CrossRef
28.
go back to reference Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM, Roberts LR et al (2018) Diagnosis, Staging, and Management of Hepatocellular Carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology 68:723–750CrossRef Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM, Roberts LR et al (2018) Diagnosis, Staging, and Management of Hepatocellular Carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology 68:723–750CrossRef
29.
go back to reference Trevisani F, D'Intino PE, Morselli-Labate AM, Mazzella G, Accogli E, Caraceni P, Domenicali M et al (2001) Serum alpha-fetoprotein for diagnosis of hepatocellular carcinoma in patients with chronic liver disease: influence of HBsAg and anti-HCV status. J Hepatol 34:570–575CrossRef Trevisani F, D'Intino PE, Morselli-Labate AM, Mazzella G, Accogli E, Caraceni P, Domenicali M et al (2001) Serum alpha-fetoprotein for diagnosis of hepatocellular carcinoma in patients with chronic liver disease: influence of HBsAg and anti-HCV status. J Hepatol 34:570–575CrossRef
30.
go back to reference Daniele B, Bencivenga A, Megna AS, Tinessa V (2004) Alpha-fetoprotein and ultrasonography screening for hepatocellular carcinoma. Gastroenterology 127:S108–112CrossRef Daniele B, Bencivenga A, Megna AS, Tinessa V (2004) Alpha-fetoprotein and ultrasonography screening for hepatocellular carcinoma. Gastroenterology 127:S108–112CrossRef
31.
go back to reference Tsai MC, Wang JH, Hung CH, Kee KM, Yen YH, Lee CM, Hu TH et al (2010) Favorable alpha-fetoprotein decrease as a prognostic surrogate in patients with hepatocellular carcinoma after radiofrequency ablation. J Gastroenterol Hepatol 25:605–612CrossRef Tsai MC, Wang JH, Hung CH, Kee KM, Yen YH, Lee CM, Hu TH et al (2010) Favorable alpha-fetoprotein decrease as a prognostic surrogate in patients with hepatocellular carcinoma after radiofrequency ablation. J Gastroenterol Hepatol 25:605–612CrossRef
Metadata
Title
The ALBI Grade is a Good Predictive Model for Very Late Recurrence in Patients with Hepatocellular Carcinoma Undergoing Primary Resection
Authors
Chun-Yu Lin
Chih-Che Lin
Chih-Chi Wang
Chao-Long Chen
Tsung-Hui Hu
Chao-Hung Hung
Pao-Yuan Huang
Ming-Chao Tsai
Publication date
01-01-2020
Publisher
Springer International Publishing
Published in
World Journal of Surgery / Issue 1/2020
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI
https://doi.org/10.1007/s00268-019-05197-3

Other articles of this Issue 1/2020

World Journal of Surgery 1/2020 Go to the issue