Case Control Study
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Sep 28, 2017; 23(36): 6674-6684
Published online Sep 28, 2017. doi: 10.3748/wjg.v23.i36.6674
Genetic biomarkers for hepatocellular cancer risk in a caucasian population
Elena De Mattia, Erika Cecchin, Jerry Polesel, Alessia Bignucolo, Rossana Roncato, Francesco Lupo, Marina Crovatto, Angela Buonadonna, Claudio Tiribelli, Giuseppe Toffoli
Elena De Mattia, Erika Cecchin, Alessia Bignucolo, Rossana Roncato, Giuseppe Toffoli, Clinical and Experimental Pharmacology, “Centro di Riferimento Oncologico” - National Cancer Institute, 33081 Aviano, Italy
Jerry Polesel, Unit of Cancer Epidemiology, “Centro di Riferimento Oncologico” - National Cancer Institute, 33081 Aviano, Italy
Francesco Lupo, General Surgery 2U and Liver Transplantation Center, A.O.U. Città della Salute e della Scienza di Torino, University of Torino, 10124 Torino, Italy
Marina Crovatto, Cytogenetics and Molecular Biology Unit, Santa Maria degli Angeli Hospital Pordenone, 33170 Pordenone, Italy
Angela Buonadonna, Medical Oncology Unit, “Centro di Riferimento Oncologico” - National Cancer Institute, 33081 Aviano, Italy
Claudio Tiribelli, Fondazione Italiana Fegato, AREA Science Park, 34149 Trieste, Italy
Author contributions: De Mattia E and Cecchin E designed the study and wrote the manuscript; Polesel J was involved in the statistical analysis and interpretation of data; Bignucolo A and Roncato R performed the majority of experiments; Lupo F, Crovatto M, Buonadonna A and Tiribelli C participated in the enrollment of cases and control groups; Toffoli G designed the study and edited the manuscript.
Supported by AIRC (Italian Association for Cancer Research) Regional Grant 2004.
Institutional review board statement: The study was reviewed and approved by the CRO- National Cancer Institute Institutional Review Board.
Informed consent statement: All study participants, before blood sampling, provided written informed consent for the genetic analysis.
Conflict-of-interest statement: The authors declare no conflict of interest.
Data sharing statement: Technical appendix, statistical code, and dataset are available from the corresponding author at gtoffoli@cro.it.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Dr. Giuseppe Toffoli, MD, Director, Clinical and Experimental Pharmacology, “Centro di Riferimento Oncologico” - National Cancer Institute, Via Franco Gallini n. 2, 33081 Aviano, Italy. gtoffoli@cro.it
Telephone: 39-434-659612 Fax: 39-434-659799
Received: February 27, 2017
Peer-review started: February 28, 2017
First decision: April 28, 2017
Revised: May 17, 2017
Accepted: July 4, 2017
Article in press: July 4, 2017
Published online: September 28, 2017
Processing time: 209 Days and 13.2 Hours
Abstract
AIM

To uncover novel genetic markers that could contribute to predicting hepatocellular carcinoma (HCC) susceptibility in Caucasians.

METHODS

The present retrospective case-control study compared genotype frequencies between a cohort of HCC cases and two, independent, HCC-free, age/sex-matched control groups. The HCC cohort comprised 192 homogeneous patients that had undergone orthotopic liver transplantation. The first control group comprised 167 patients that were matched to the HCC cohort for the percentage of hepatitis B (HBV) and/or hepatitis C (HCV) infections. A second control group included 192 virus-free, healthy individuals that were used to evaluate the generalizability of the identified predictive markers. All cases and controls were Caucasian. The three study populations were characterized with a panel of 31 markers derived from 21 genes that encoded key proteins involved in hepatocarcinogenesis-related pathways. The study end-point was to assess the association between genetic variants and HCC onset.

RESULTS

Five genetic markers were identified as risk factors for HCC in high-risk patients infected with HBV/HCV. According to a dominant model, reduced HCC risk was associated with three polymorphisms: ERCC1 rs3212986 (OR = 0.46, 95%CI: 0.30-0.71, P = 0.0005), GST-P1 rs1138272 (OR = 0.41, 95%CI: 0.21-0.81, P = 0.0097), and CYP17A1 rs743572 (OR = 0.50, 95%CI: 0.31-0.79, P = 0.0032). Conversely, according to a recessive model, increased HCC risk was associated with two polymorphisms: XRCC3 rs1799794 (OR = 3.70, 95%CI: 1.02-13.39, P = 0.0461) and ABCB1 rs1128503 (OR = 2.06, 95%CI: 1.18-3.61, P = 0.0111). These associations remained significant in a subgroup analysis, where patients were stratified according to viral status (HBV- or HCV-positive serology). Two variants exhibited a serology-specific effect: ABCB1 rs1128503 (OR = 4.18, 95%CI: 1.55-11.29, P = 0.0048) showed an effect in the HBV-positive subgroup; and ERCC1 rs3212986 (OR = 0.33, 95%CI: 0.18-0.60, P = 0.0003) showed an effect in the HCV-positive subgroup. Among the five markers identified, ERCC1 rs3212986 (OR = 0.43, P < 0.0001) and CYP17A1 rs743572 (OR = 0.73, P = 0.0310) had a different distribution in patients with HCC compared to healthy individuals. With a recursive partitioning approach, we also demonstrated that significant gene-gene interactions between ERCC1 rs3212986, CYP17A1 rs743572, GST-P1 rs1138272, and the previously described UGT1A7*3 predictive marker, played a role in the complex trait of HCC susceptibility.

CONCLUSION

We identified five polymorphisms and interactions that contributed crucially to predicting HCC risk. These findings represented an important step towards improving HCC diagnosis and management.

Keywords: ERCC1; XRCC3; GST-P1; CYP17A1; MDR-1; Polymorphisms; Hepatocellular carcinoma risk; Early diagnosis; Antiviral therapy; Hepatitis B viral/hepatitis C viral

Core tip: It is a great challenge to define new biomarkers of hepatocellular carcinoma (HCC) risk for HCC management. This work identified five genetic markers in key pathways linked to hepatocarcinogenesis (ERCC1 rs3212986, GSTP1 rs1138272, CYP17A1 rs743572, XRCC3 rs1799794, and ABCB1 rs112850), which could predict individual HCC susceptibility, particularly in a high-risk [hepatitis B viral/hepatitis C viral (HCV)-infected] Caucasian population. We also identified potential gene-gene interactions that should be included in the definition of HCC risk. These findings could contribute to improved HCC surveillance, early cancer diagnoses, and potential curative therapies. For patients with HCV, these markers could be considered selection criteria for the personalized use of recently developed, highly expensive anti-viral therapies.