Pretreatment gamma-glutamyl transferase predicts mortality in patients with chronic hepatitis B treated with nucleotide/nucleoside analogs.

GGT HBV NA mortality treatment

Journal

The Kaohsiung journal of medical sciences
ISSN: 2410-8650
Titre abrégé: Kaohsiung J Med Sci
Pays: China (Republic : 1949- )
ID NLM: 100960562

Informations de publication

Date de publication:
27 Oct 2023
Historique:
revised: 18 09 2023
received: 23 08 2023
accepted: 02 10 2023
pubmed: 27 10 2023
medline: 27 10 2023
entrez: 27 10 2023
Statut: aheadofprint

Résumé

Elevated serum gamma-glutamyl transferase (GGT) levels are associated with chronic hepatitis B (CHB)-related hepatocellular carcinoma. However, their role in predicting mortality in patients with CHB treated with nucleotide/nucleoside analogs (NAs) remains elusive. Altogether, 2843 patients with CHB treated with NAs were recruited from a multinational cohort. Serum GGT levels before and 6 months (Month-6) after initiating NAs were measured to explore their association with all-cause, liver-related, and non-liver-related mortality. The annual incidence of all-cause mortality was 0.9/100 person-years over a follow-up period of 17,436.3 person-years. Compared with patients who survived, those who died had a significantly higher pretreatment (89.3 vs. 67.4 U/L, p = 0.002) and Month-6-GGT levels (62.1 vs. 38.4 U/L, p < 0.001). The factors associated with all-cause mortality included cirrhosis (hazard ratio [HR]/95% confidence interval [CI]: 2.66/1.92-3.70, p < 0.001), pretreatment GGT levels (HR/CI: 1.004/1.003-1.006, p < 0.001), alanine aminotransferase level (HR/CI: 0.996/0.994-0.998, p = 0.001), and age (HR/CI: 1.06/1.04-1.07, p < 0.001). Regarding liver-related mortality, the independent factors included cirrhosis (HR/CI: 4.36/2.79-6.89, p < 0.001), pretreatment GGT levels (HR/CI: 1.006/1.004-1.008, p < 0.001), alanine aminotransferase level (HR/CI: 0.993/0.990-0.997, p = 0.001), age (HR/CI: 1.03/1.01-1.05, p < 0.001), and fatty liver disease (HR/CI: 0.30/0.15-0.59, p = 0.001). Pretreatment GGT levels were also independently predictive of non-liver-related mortality (HR/CI: 1.003/1.000-1.005, p = 0.03). The results remained consistent after excluding the patients with a history of alcohol use. A dose-dependent manner of <25, 25-75, and >75 percentile of pretreatment GGT levels was observed with respect to the all-cause mortality (trend p < 0.001). Pretreatment serum GGT levels predicted all-cause, liver-related, and non-liver-related mortality in patients with CHB treated with NAs.

Identifiants

pubmed: 37885338
doi: 10.1002/kjm2.12771
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Kaohsiung Medical University
ID : KMUH109-9R05
Organisme : Kaohsiung Medical University
ID : MOST 111-2314-B-037-069-MY2
Organisme : Kaohsiung Medical University Hospital
ID : KMUH110-0M03
Organisme : Kaohsiung Medical University Hospital
ID : KMUH110-0M06
Organisme : Kaohsiung Medical University Hospital
ID : KMHK-DK(C)111004
Organisme : Kaohsiung Medical University Hospital
ID : KMUH-DK()109005~1
Organisme : Kaohsiung Medical University Hospital
ID : KMUH-DK(B)111002-1
Organisme : Kaohsiung Medical University Hospital
ID : KMHK-DK(C)111006
Organisme : Ministry of Health and Welfare, Taiwan
ID : MOHW111-TDU-B-221-014007

Informations de copyright

© 2023 The Authors. The Kaohsiung Journal of Medical Sciences published by John Wiley & Sons Australia, Ltd on behalf of Kaohsiung Medical University.

Références

GBD 2019 Hepatitis B Collaborators. Global, regional, and national burden of hepatitis B, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet Gastroenterol Hepatol. 2022;7:796-829.
Bixler D, Zhong Y, Ly KN, Moorman AC, Spradling PR, Teshale EH, et al. Mortality among patients with chronic hepatitis B infection: the Chronic Hepatitis Cohort Study (CHeCS). Clin Infect Dis. 2019;68:956-963.
Zhou K, Dodge JL, Grab J, Poltavskiy E, Terrault NA. Mortality in adults with chronic hepatitis B infection in the United States: a population-based study. Aliment Pharmacol Ther. 2020;52:382-389.
Si J, Yu C, Guo Y, Bian Z, Meng R, Yang L, et al. Chronic hepatitis B virus infection and total and cause-specific mortality: a prospective cohort study of 0.5 million people. BMJ Open. 2019;9:e027696.
Alavi M, Grebely J, Hajarizadeh B, Amin J, Larney S, Law MG, et al. Mortality trends among people with hepatitis B and C: a population-based linkage study, 1993-2012. BMC Infect Dis. 2018;18:215.
Chen VL, Yeh ML, Le AK, Jun M, Saeed WK, Yang JD, et al. Anti-viral therapy is associated with improved survival but is underutilised in patients with hepatitis B virus-related hepatocellular carcinoma: real-world east and west experience. Aliment Pharmacol Ther. 2018;48:44-54.
Nguyen MH, Wong G, Gane E, Kao JH, Dusheiko G. Hepatitis B virus: advances in prevention, diagnosis, and therapy. Clin Microbiol Rev. 2020;33:e00046-19.
Whitfield JB. Gamma glutamyl transferase. Crit Rev Clin Lab Sci. 2001;38:263-355.
Kunutsor SK. Gamma-glutamyltransferase-friend or foe within? Liver Int. 2016;36:1723-1734.
Koenig G, Seneff S. Gamma-glutamyltransferase: a predictive biomarker of cellular antioxidant inadequacy and disease risk. Dis Markers. 2015;2015:818570.
Hu G, Tuomilehto J, Pukkala E, Hakulinen T, Antikainen R, Vartiainen E, et al. Joint effects of coffee consumption and serum gamma-glutamyltransferase on the risk of liver cancer. Hepatology. 2008;48:129-136.
Huang CF, Jang TY, Jun DW, Ahn SB, An J, Enomoto M, et al. On-treatment gamma-glutamyl transferase predicts the development of hepatocellular carcinoma in chronic hepatitis B patients. Liver Int. 2022;42:59-68.
Huang CF, Yeh ML, Tsai PC, Hsieh MH, Yang HL, Hsieh MY, et al. Baseline gamma-glutamyl transferase levels strongly correlate with hepatocellular carcinoma development in non-cirrhotic patients with successful hepatitis C virus eradication. J Hepatol. 2014;61:67-74.
Sarin SK, Kumar M, Lau GK, Abbas Z, Chan HL, Chen CJ, et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int. 2016;10:1-98.
Chien RN, Kao JH, Peng CY, Chen CH, Liu CJ, Huang YH, et al. Taiwan consensus statement on the management of chronic hepatitis B. J Formos Med Assoc. 2019;118:7-38.
Drafting Committee for Hepatitis Management Guidelines and the Japan Society of Hepatology. JSH Guidelines for the management of hepatitis B virus infection. Hepatol Res. 2014;44(Suppl S1):1-58.
Korean Association for the Study of the Liver (KASL). KASL clinical practice guidelines for management of chronic hepatitis B. Clin Mol Hepatol. 2019;25:93-159.
Ziol M, Handra-Luca A, Kettaneh A, Christidis C, Mal F, Kazemi F, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with chronic hepatitis C. Hepatology. 2005;41:48-54.
Saadeh S, Younossi ZM, Remer EM, Gramlich T, Ong JP, Hurley M, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology. 2002;123:745-750.
Wong MCS, Huang JLW, George J, Huang J, Leung C, Eslam M, et al. The changing epidemiology of liver diseases in the Asia-Pacific region. Nat Rev Gastroenterol Hepatol. 2019;16:57-73.
Stepanova M, Rafiq N, Younossi ZM. Components of metabolic syndrome are independent predictors of mortality in patients with chronic liver disease: a population-based study. Gut. 2010;59:1410-1415.
Mallet V, Hamed K, Schwarzinger M. Prognosis of patients with chronic hepatitis B in France (2008-2013): a nationwide, observational and hospital-based study. J Hepatol. 2017;66:514-520.
Aberkane H, Stoltz JF, Galteau MM, Wellman M. Erythrocytes as targets for gamma-glutamyltranspeptidase initiated pro-oxidant reaction. Eur J Haematol. 2002;68:262-271.
Aberg F, Luukkonen PK, But A, Salomaa V, Britton A, Petersen KM, et al. Development and validation of a model to predict incident chronic liver disease in the general population: the CLivD score. J Hepatol. 2022;77:302-311.
Strasak AM, Rapp K, Brant LJ, Hilbe W, Gregory M, Oberaigner W, et al. Association of gamma-glutamyltransferase and risk of cancer incidence in men: a prospective study. Cancer Res. 2008;68:3970-3977.
Ho FK, Ferguson LD, Celis-Morales CA, Gray SR, Forrest E, Alazawi W, et al. Association of gamma-glutamyltransferase levels with total mortality, liver-related and cardiovascular outcomes: a prospective cohort study in the UK Biobank. eClinicalMedicine. 2022;48:101435.
Eminler AT, Irak K, Ayyildiz T, Keskin M, Kiyici M, Gurel S, et al. The relation between liver histopathology and GGT levels in viral hepatitis: more important in hepatitis B. Turk J Gastroenterol. 2014;25:411-415.
Huang R, Yang CC, Liu Y, Xia J, Su R, Xiong YL, et al. Association of serum gamma-glutamyl transferase with treatment outcome in chronic hepatitis B patients. World J Gastroenterol. 2015;21:9957-9965.
Zhao Z, Zhu Y, Ni X, Lin J, Li H, Zheng L, et al. Serum GGT/ALT ratio predicts vascular invasion in HBV-related HCC. Cancer Cell Int. 2021;21:517.
Banderas DZ, Escobedo J, Gonzalez E, Liceaga MG, Ramirez JC, Castro MG. Gamma-glutamyl transferase: a marker of nonalcoholic fatty liver disease in patients with the metabolic syndrome. Eur J Gastroenterol Hepatol. 2012;24:805-810.
Fujii H, Doi H, Ko T, Fukuma T, Kadono T, Asaeda K, et al. Frequently abnormal serum gamma-glutamyl transferase activity is associated with future development of fatty liver: a retrospective cohort study. BMC Gastroenterol. 2020;20:217.
Chung GE, Jeong SM, Cho EJ, Yoo JJ, Cho Y, Lee KN, et al. Association of fatty liver index with all-cause and disease-specific mortality: a nationwide cohort study. Metabolism. 2022;133:155222.
Peleg N, Issachar A, Sneh Arbib O, Cohen-Naftaly M, Braun M, Leshno M, et al. Liver steatosis is a strong predictor of mortality and cancer in chronic hepatitis B regardless of viral load. JHEP Rep. 2019;1:9-16.
Li J, Yang HI, Yeh ML, Le MH, Le AK, Yeo YH, et al. Association between fatty liver and cirrhosis, hepatocellular carcinoma, and hepatitis B surface antigen Seroclearance in chronic hepatitis B. J Infect Dis. 2021;224:294-302.
Sung KC, Ryu S, Kim BS, Cheong ES, Park DI, Kim BI, et al. Gamma-glutamyl transferase is associated with mortality outcomes independently of fatty liver. Clin Chem. 2015;61:1173-1181.

Auteurs

Tyng-Yuan Jang (TY)

Ph.D. Program in Environmental and Occupational Medicine, College of Medicine, Kaohsiung Medical University and National Health Research Institutes, Kaohsiung, Taiwan.
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.

Po-Cheng Liang (PC)

Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.

Dae Won Jun (DW)

Department of Internal Medicine, Hanyang University Hospital, Hanyang University College of Medicine, Seoul, South Korea.

Jang Han Jung (JH)

Division of Gastroenterology, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea.

Hidenori Toyoda (H)

Department of Gastroenterology and Hepatology, Ogaki Municipal Hospital, Gifu, Japan.

Chih-Wen Wang (CW)

Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.

Man-Fung Yuen (MF)

Department of Medicine, School of Clinical Medicine, Queen Mary Hospital, The University of Hong Kong, Hong Kong, Hong Kong.
State Key Laboratory of Liver Research, The University of Hong Kong, Hong Kong, Hong Kong.

Ka Shing Cheung (KS)

Department of Medicine, School of Clinical Medicine, Queen Mary Hospital, The University of Hong Kong, Hong Kong, Hong Kong.

Satoshi Yasuda (S)

Department of Gastroenterology and Hepatology, Ogaki Municipal Hospital, Gifu, Japan.

Sung Eun Kim (SE)

Department of Internal Medicine, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, South Korea.

Eileen L Yoon (EL)

Department of Internal Medicine, Hanyang University Hospital, Hanyang University College of Medicine, Seoul, South Korea.

Jihyun An (J)

Department of Internal Medicine, Hanyang University College of Medicine, Hanyang University Guri Hospital, Guri, South Korea.

Masaru Enomoto (M)

Department of Hepatology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Ritsuzo Kozuka (R)

Department of Hepatology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Makoto Chuma (M)

Gastroenterological Center, Yokohama City University Medical Center, Yokohama, Japan.

Akito Nozaki (A)

Gastroenterological Center, Yokohama City University Medical Center, Yokohama, Japan.

Toru Ishikawa (T)

Department of Gastroenterology, Saiseikai Niigata Hospital, Niigata, Japan.

Tsunamasa Watanabe (T)

Division of Gastroenterology and Hepatology, St. Marianna University School of Medicine, Kawasaki, Japan.

Masanori Atsukawa (M)

Division of Gastroenterology and Hepatology, Nippon Medical School, Tokyo, Japan.

Taeang Arai (T)

Division of Gastroenterology and Hepatology, Nippon Medical School, Tokyo, Japan.

Korenobu Hayama (K)

Division of Gastroenterology and Hepatology, Nippon Medical School, Tokyo, Japan.

Masatoshi Ishigami (M)

Department of Gastroenterology & Hepatology, Nagoya University Graduate School of Medicine, Nagoya, Japan.

Yong Kyun Cho (YK)

Department of Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, South Korea.

Eiichi Ogawa (E)

Department of General Internal Medicine, Kyushu University, Kyushu, Japan.

Hyoung Su Kim (HS)

Department of Internal Medicine, Hallym University Kangdong Sacred Heart Hospital, Hallym University College of Medicine, Seoul, South Korea.

Jae-Jun Shim (JJ)

Department of Internal Medicine, Kyung Hee University Hospital, Kyung Hee University School of Medicine, Seoul, South Korea.

Haruki Uojima (H)

Department of Gastroenterology, Internal Medicine, Kitasato University School of Medicine, Sagamihara, Japan.

Soung Won Jeong (SW)

Department of Internal Medicine, Soonchunhyang University Hospital, Soonchunhyang University College of Medicine, Seoul, South Korea.

Sang Bong Ahn (SB)

Department of Internal Medicine, Nowon Eulji Medical Center, Eulji University College of Medicine, Seoul, South Korea.

Koichi Takaguchi (K)

Department of Hepatology, Kagawa Prefectural Central Hospital, Kagawa, Japan.

Tomonori Senoh (T)

Department of Hepatology, Kagawa Prefectural Central Hospital, Kagawa, Japan.

Maria Buti (M)

Liver Unit, Hospital Universitari Vall d'Hebron and CIBEREHD del Instituto Carlos III, Barcelona, Spain.

Elena Vargas-Accarino (E)

Liver Unit, Hospital Universitari Vall d'Hebron and CIBEREHD del Instituto Carlos III, Barcelona, Spain.

Hiroshi Abe (H)

Division of Gastroenterology and Hepatology, Shinmatsudo Central General Hospital, Chiba, Japan.

Hirokazu Takahashi (H)

Liver Center, Saga University Hospital, Saga, Japan.
Division of Metabolism and Endocrinology, Faculty of Medicine, Saga University, Saga, Japan.

Kaori Inoue (K)

Liver Center, Saga University Hospital, Saga, Japan.
Division of Metabolism and Endocrinology, Faculty of Medicine, Saga University, Saga, Japan.

Jee-Fu Huang (JF)

Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.
Faculty of Internal Medicine and Hepatitis Research Center, School of Medicine, College of Medicine, and Center for Cancer Research and Liquid Biopsy, Kaohsiung Medical University, Kaohsiung, Taiwan.

Wan-Long Chuang (WL)

Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.
Faculty of Internal Medicine and Hepatitis Research Center, School of Medicine, College of Medicine, and Center for Cancer Research and Liquid Biopsy, Kaohsiung Medical University, Kaohsiung, Taiwan.

Ming-Lun Yeh (ML)

Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.

Chia-Yen Dai (CY)

Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.
Faculty of Internal Medicine and Hepatitis Research Center, School of Medicine, College of Medicine, and Center for Cancer Research and Liquid Biopsy, Kaohsiung Medical University, Kaohsiung, Taiwan.

Chung-Feng Huang (CF)

Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.
Faculty of Internal Medicine and Hepatitis Research Center, School of Medicine, College of Medicine, and Center for Cancer Research and Liquid Biopsy, Kaohsiung Medical University, Kaohsiung, Taiwan.
Translational Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, and Academia Sinica, Kaohsiung, Taiwan.

Mindie H Nguyen (MH)

Division of Gastroenterology and Hepatology, Department of Medicine, Stanford University Medical Center, Palo Alto, California, USA.

Ming-Lung Yu (ML)

Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan.
Faculty of Internal Medicine and Hepatitis Research Center, School of Medicine, College of Medicine, and Center for Cancer Research and Liquid Biopsy, Kaohsiung Medical University, Kaohsiung, Taiwan.
School of Medicine, College of Medicine, National Sun Yat-Sen University, Kaohsiung, Taiwan.
Division of Hepato-Gastroenterology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan.

Classifications MeSH