Role of Air Pollution in Development of Hepatocellular Carcinoma Among Chronic Hepatitis B Patients Treated With Nucleotide/Nucleoside Analogues
This article relates to:
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Blowin' in the Wind: Air Pollution and the Risk of Hepatocellular Carcinoma
- Volume 45Issue 6Liver International
- First Published online: May 27, 2025
Tyng-Yuan Jang
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
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Department of Internal Medicine, Pingtung Hospital, Ministry of Health and Welfare, Ping-Tung, Taiwan
Search for more papers by this authorYu-ting Zeng
Department of Geomatics, National Cheng Kung University, Tainan, Taiwan
Search for more papers by this authorPo-Cheng Liang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorChih-Da Wu
Department of Geomatics, National Cheng Kung University, Tainan, Taiwan
Innovation and Development Center of Sustainable Agriculture, National Chung Hsing University, Tainan, Taiwan
Search for more papers by this authorYu-Ju Wei
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorPei-Chien Tsai
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorPo-Yao Hsu
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorMing-Yen Hsieh
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorYi-Hung Lin
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorMeng-Hsuan Hsieh
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorChih-Wen Wang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorJeng-Fu Yang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorMing-Lun Yeh
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorChung-Feng Huang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorWan-Long Chuang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorJee-Fu Huang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorYa-Yun Cheng
School of Medicine and Doctoral Program of Clinical and Experimental Medicine, College of Medicine, Center of Excellence for Metabolic Associated Fatty Liver Disease, National Sun Yat-Sen University, Kaohsiung, Taiwan
Search for more papers by this authorCorresponding Author
Chia-Yen Dai
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Correspondence:
Chia-Yen Dai ([email protected])
Pau-Chung Chen ([email protected])
Search for more papers by this authorCorresponding Author
Pau-Chung Chen
Department of Geomatics, National Cheng Kung University, Tainan, Taiwan
Department of Public Health, National Taiwan University, Taipei, Taiwan
Department of Environmental and Occupational Medicine, National Taiwan University Hospital, Taipei, Taiwan
National Institute of Environmental Health Sciences, National Health Research Institutes, Miaoli, Taiwan
Correspondence:
Chia-Yen Dai ([email protected])
Pau-Chung Chen ([email protected])
Search for more papers by this authorMing-Lung Yu
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Division of Hepato-Gastroenterology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan
Search for more papers by this authorTyng-Yuan Jang
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
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Department of Internal Medicine, Pingtung Hospital, Ministry of Health and Welfare, Ping-Tung, Taiwan
Search for more papers by this authorYu-ting Zeng
Department of Geomatics, National Cheng Kung University, Tainan, Taiwan
Search for more papers by this authorPo-Cheng Liang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorChih-Da Wu
Department of Geomatics, National Cheng Kung University, Tainan, Taiwan
Innovation and Development Center of Sustainable Agriculture, National Chung Hsing University, Tainan, Taiwan
Search for more papers by this authorYu-Ju Wei
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorPei-Chien Tsai
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorPo-Yao Hsu
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorMing-Yen Hsieh
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorYi-Hung Lin
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorMeng-Hsuan Hsieh
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorChih-Wen Wang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorJeng-Fu Yang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorMing-Lun Yeh
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorChung-Feng Huang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorWan-Long Chuang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorJee-Fu Huang
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Search for more papers by this authorYa-Yun Cheng
School of Medicine and Doctoral Program of Clinical and Experimental Medicine, College of Medicine, Center of Excellence for Metabolic Associated Fatty Liver Disease, National Sun Yat-Sen University, Kaohsiung, Taiwan
Search for more papers by this authorCorresponding Author
Chia-Yen Dai
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Correspondence:
Chia-Yen Dai ([email protected])
Pau-Chung Chen ([email protected])
Search for more papers by this authorCorresponding Author
Pau-Chung Chen
Department of Geomatics, National Cheng Kung University, Tainan, Taiwan
Department of Public Health, National Taiwan University, Taipei, Taiwan
Department of Environmental and Occupational Medicine, National Taiwan University Hospital, Taipei, Taiwan
National Institute of Environmental Health Sciences, National Health Research Institutes, Miaoli, Taiwan
Correspondence:
Chia-Yen Dai ([email protected])
Pau-Chung Chen ([email protected])
Search for more papers by this authorMing-Lung Yu
Hepatobiliary Division, Department of Internal Medicine, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan
College of Medicine, Center for Liquid Biopsy and Cohort Research, Kaohsiung Medical University, Kaohsiung, Taiwan
Division of Hepato-Gastroenterology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan
Search for more papers by this authorHandling Editor: Alessio Aghemo
Funding: This work was supported, in part, by a grant from Kaohsiung Medical University (NSTC 112-2314-B-037-076-MY3, NSTC 112-2314-B-037-009, NSTC 112-2923-B-037-002-MY3) and Kaohsiung Medical University Hospital (KMUHDK(B)111003-2, KMUH111-1R05, KMUH112-2M02).
ABSTRACT
Background and Aims
To investigate the association between air pollution and hepatocellular carcinoma (HCC) in chronic hepatitis B (CHB) patients treated with nucleotide/nucleoside analogues.
Methods
We enrolled 1298 CHB patients treated with nucleotide/nucleoside analogues and analysed the incidence and risk factors for HCC. Daily estimates of air pollutants were estimated since the previous year from the enrolment date.
Results
The annual incidence of HCC was 2.1/100 person-years after a follow-up period of over 4840.5 person-years. Factors with the strongest association with HCC development were liver cirrhosis (hazard ratio [HR]/95% confidence interval [CI]: 3.00/1.55–5.81; p = 0.001), male sex (2.98/1.51–5.90; p = 0.02), body mass index (1.11/1.04–1.18; p = 0.002) and age (1.06/1.04–1.09; p < 0.001). Among patients with cirrhosis, the factors associated with HCC development were male sex (HR/95% CI: 2.10/1.00–4.25; p = 0.04) and NO2 (per one-unit increment, parts per billion; 1.07/1.01–1.13; p = 0.01). Moreover, patients with the highest quartile of annual NO2 exposure had more than a three-fold risk of HCC than those with the lowest quartile of annual exposure (HR/95% CI: 3.26/1.34–7.93; p = 0.01). Among patients without cirrhosis, the strongest factors associated with HCC development were male sex (HR/95% CI: 5.86/1.79–19.23; p = 0.004), age (1.12/1.07–1.17; p < 0.001) and platelet count (0.99/0.98–1.00; p = 0.04).
Conclusions
Air pollution influences HCC development in CHB patients who receive nucleotide/nucleoside analogue therapy. Long-term NO2 exposure might accelerate HCC development in CHB patients with cirrhosis receiving nucleotide/nucleoside analogue treatment.
Conflicts of Interest
The authors declare no conflicts of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.
Supporting Information
| Filename | Description |
|---|---|
| liv16149-sup-0001-FigureS1.tifTIFF image, 90.3 KB |
Figure S1. The basic summary statistics of air pollutants. |
| liv16149-sup-0002-FigureS2.tifTIFF image, 103.7 KB |
Figure S2. The Kaplan–Meier curves for HCC development. |
| liv16149-sup-0003-FigureS3.tifTIFF image, 114.8 KB |
Figure S3. The Kaplan–Meier curves for HCC development of high NO2 level (≥ 19.26 ppb) and low NO2 level (< 19.26 ppb). |
| liv16149-sup-0004-Tables.docxWord 2007 document , 18.3 KB |
Table S1. Pearson’s correlation coefficients of air pollutants. Table S2. Study population exposure to air in Kaohsiung. Table S3. Factors associated with high NO2* in cirrhotic patients. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
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