Hepatitis B virus preS2Δ38–55 variants: A newly identified risk factor for hepatocellular carcinoma
Damien Cohen,
Sumantra Ghosh,
Yusuke Shimakawa,
Njie Ramou,
Pierre Simon Garcia,
Anaëlle Dubois,
Clément Guillot,
Nora Kakwata-Nkor Deluce,
Valentin Tilloy,
Geoffroy Durand,
Catherine Voegele,
Gibril Ndow,
Umberto d'Alessandro,
Céline Brochier-Armanet,
Sophie Alain,
Florence Le Calvez-Kelm,
Janet Hall,
Fabien Zoulim,
Maimuna Mendy,
Mark Thursz,
Maud Lemoine,
Isabelle Chemin
Affiliations
Damien Cohen
INSERM U1052, CNRS 5286, Univ Lyon, Université Claude Bernard Lyon 1, Centre Léon Bérard, Centre de Recherche en Cancérologie de Lyon, Lyon, France
Sumantra Ghosh
INSERM U1052, CNRS 5286, Univ Lyon, Université Claude Bernard Lyon 1, Centre Léon Bérard, Centre de Recherche en Cancérologie de Lyon, Lyon, France
Yusuke Shimakawa
Unité d'Épidémiologie des Maladies Émergentes, Institut Pasteur, Paris, France
Njie Ramou
International Agency for Research on Cancer, Lyon, France
Pierre Simon Garcia
Univ Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, Villeurbanne, France; Molecular Microbiology and Structural Biochemistry, Institut de Biologie et de Chimie des Protéines 7 passage du Vercors, Lyon Cedex, France
Anaëlle Dubois
INSERM U1052, CNRS 5286, Univ Lyon, Université Claude Bernard Lyon 1, Centre Léon Bérard, Centre de Recherche en Cancérologie de Lyon, Lyon, France
Clément Guillot
INSERM U1052, CNRS 5286, Univ Lyon, Université Claude Bernard Lyon 1, Centre Léon Bérard, Centre de Recherche en Cancérologie de Lyon, Lyon, France
Nora Kakwata-Nkor Deluce
INSERM U1052, CNRS 5286, Univ Lyon, Université Claude Bernard Lyon 1, Centre Léon Bérard, Centre de Recherche en Cancérologie de Lyon, Lyon, France
Valentin Tilloy
Microbiology Department, CHU Limoges, Genomic Platform GenoLim, UMR Inserm 1092/FR CNRS 145 GEIST, Faculté de Médecine-Université de Limoges, CHU Dupuytren, CBRS, Limoges, France
Geoffroy Durand
International Agency for Research on Cancer, Lyon, France
Catherine Voegele
International Agency for Research on Cancer, Lyon, France
Gibril Ndow
Medical Research Council Unit, The Gambia at the London School of Hygiene and Tropical Medicine, Banjul, The Gambia
Umberto d'Alessandro
Medical Research Council Unit, The Gambia at the London School of Hygiene and Tropical Medicine, Banjul, The Gambia
Céline Brochier-Armanet
Univ Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, Villeurbanne, France
Sophie Alain
Microbiology Department, CHU Limoges, Genomic Platform GenoLim, UMR Inserm 1092/FR CNRS 145 GEIST, Faculté de Médecine-Université de Limoges, CHU Dupuytren, CBRS, Limoges, France
Florence Le Calvez-Kelm
International Agency for Research on Cancer, Lyon, France
Janet Hall
INSERM U1052, CNRS 5286, Univ Lyon, Université Claude Bernard Lyon 1, Centre Léon Bérard, Centre de Recherche en Cancérologie de Lyon, Lyon, France
Fabien Zoulim
INSERM U1052, CNRS 5286, Univ Lyon, Université Claude Bernard Lyon 1, Centre Léon Bérard, Centre de Recherche en Cancérologie de Lyon, Lyon, France; Department of Hepatology, Groupement Hospitalier Nord, Hospices Civils de Lyon, Lyon, France
Maimuna Mendy
International Agency for Research on Cancer, Lyon, France
Mark Thursz
Department of Metabolism, Digestion and Reproduction, Liver Unit, Imperial College London, London, UK
Maud Lemoine
Department of Metabolism, Digestion and Reproduction, Liver Unit, Imperial College London, London, UK
Isabelle Chemin
INSERM U1052, CNRS 5286, Univ Lyon, Université Claude Bernard Lyon 1, Centre Léon Bérard, Centre de Recherche en Cancérologie de Lyon, Lyon, France; Corresponding author. Address: INSERM U1052, CNRS UMR5286, Centre de Recherche en Cancérologie de Lyon Université Claude Bernard, 151 cours Albert Thomas, Lyon, France.
Background & Aims: Although HBV is a major cause of death in Africa, its genetic variability has been poorly documented. This study aimed to address whether HBV genotype and surface gene variants are associated with HBV-related liver disease in The Gambia. Methods: We conducted a case-control study nested in the Prevention of Liver Fibrosis and Cancer in Africa programme. Consecutive treatment-naive patients with chronic HBV infection and detectable viral load were recruited: 211 controls with no significant liver disease and 91 cases (56 cirrhosis and 35 HCC cases). HBV genotypes and surface gene variants were determined by Sanger sequencing or next-generation sequencing (NGS) in serum DNA. Aflatoxin B1 (AFB1)-specific codon 249 TP53 mutation was determined by NGS in circulating cell-free plasma DNA. Results: In phylogenetic analysis, 85% of individuals carried HBV genotype E, 14% genotype A, and 1% A/E recombinant viruses. Surface gene variants were more frequently observed in cases (43% and 57% in cirrhosis and HCC cases, respectively) than controls (25%; p 2,000 IU/ml (OR 22.7 [8.0–64.9]), HBsAg levels <10,000 IU/ml (OR 19.0 [5.5–65.3]), and AFB1 exposure (OR 29.3 [3.7–230.4]) on HCC risk. Conclusions: This study identified a hotspot for HBV preS2 deletions as a strong independent factor for HCC in The Gambia, with HBV genotypes and AFB1 exposure contributing to the high liver cancer risk. Lay summary: Although HBV-related liver disease is highly prevalent in sub-Saharan Africa, the associated virological characteristics are poorly studied. Using clinical data from African patients chronically infected with HBV, an assessment of the virological variability (genotypes and mutations) and exposure to AFB1, a toxin often contaminating food, was carried out. Our results show that HBV genotypes, the presence of a highly prevalent mutant form of HBV, and AFB1 exposure contribute to the high liver cancer risk in this population.