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Herbal Medicine Containing Aristolochic Acid and the Risk of Primary Liver Cancer in Patients with Hepatitis C Virus Infection

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Herbal Medicine Containing Aristolochic Acid and the Risk of Primary Liver Cancer in Patients with Hepatitis C Virus Infection Published OnlineFirst August 13, 2019; DOI: 10.1158/1055-9965.EPI-19-0023 Research Article Cancer Epidemiology, Biomarkers Herbal Medicine Containing Aristolochic Acid and & Prevention the Risk of Primary Liver Cancer in Patients with Hepatitis C Virus Infection Chi-Jen Chen1, Yao-Hsu Yang2,3,4,5, Meng-Hung Lin4, Chuan-Pin Lee4, Yu-Tse Tsan6,7, Ming-Nan Lai8, Hsiao-Yu Yang2,9,10, Pat Doyle11, Wen-Chao Ho12, and Pau-Chung Chen2,9,10,13,14 Abstract Background: We investigated the association between tak- Results: During the follow-up period of 3,052,132 person- ing herbal medicine (HM) containing aristolochic acid (AA) years, we identified 25,502 PLC cases; this corresponded to an and the risk of primary liver cancer (PLC) among patients with overall incidence rate of 835.5 PLCs per 100,000 person- hepatitis C virus (HCV) infection. years. The adjusted HRs were 1.21 [95% confidence interval Methods: This is a prospective study for the long-term follow- (CI), 1.18–1.24], 1.48 (95% CI, 1.37–1.59), 1.50 (95% CI, up of a nationwide population-based cohort of patients ages 1.34–1.68), and 1.88 (95% CI, 1.61–2.19) for estimated AA 18 years or older diagnosed with HCV infection during 1997 to usage groups: 1 to 250, 251 to 500, 501 to 1,000, and 2010. A total of 223,467 HCV-infected patients were identified more than 1,000 mg, respectively, relative to no AA exposure using the National Health Insurance Research Database in (reference group). Taiwan. The use of HM containing AA was evaluated among Conclusions: The current findings suggest that among patients who had visited traditional Chinese medicine clinics HCV-positive patients, increasing exposure to AA poses an beginning from 1997 to 1 year prior to the diagnosis of PLC or increased risk of acquiring PLC. dates censored (2003). We tracked each individual patient from Impact: AA may increase the risk of PLC in HCV-positive 1997 to 2013 to identify incident cases of PLC since 1999. populations. Introduction 1Graduate Institute of Data Science, Taipei Medical University, Taipei, Taiwan. Aristolochic acid (AA) is found in some Chinese herbs and 2Institute of Environmental and Occupational Health Sciences, National Taiwan occurs naturally in plants in the genera Aristolochia and Asarum, University College of Public Health, Taipei, Taiwan. 3Department of Traditional which grow worldwide (1). Prior to stricter regulation in 2003, Chinese Medicine, Chang Gung Memorial Hospital, Chiayi County, Taiwan. 4 more than 100 million people used Chinese herbs containing AA Health Informatics and Epidemiology Laboratory, Chang Gung Memorial Hos- fi fi pital, Chiayi County, Taiwan. 5School of Traditional Chinese Medicine, College of in China (2). AA was rst identi ed as a factor in urothelial Medicine, Chang Gung University, Taoyuan, Taiwan. 6Division of Occupational carcinoma (3, 4). Plants containing AA and AA itself are listed as Medicine, Department of Emergency Medicine, Taichung Veterans General human carcinogens by the International Agency for Research on Hospital, Taichung, Taiwan. 7School of Medicine, Chung Shan Medical University, Cancer (5, 6). AA increases DNA adduct formation and mutant Taichung, Taiwan. 8Department of Statistics, Feng Chia University, Taichung, frequency in experimental animals in both liver and kidney (7). A 9 Taiwan. Department of Public Health, National Taiwan University College of new study also demonstrated that AA induced liver cancer in Public Health, Taipei, Taiwan. 10Department of Environmental and Occupational Medicine, National Taiwan University Hospital and National Taiwan University mice (8). In Taiwan, hepatocellular carcinomas (HCC) are nearly College of Medicine, Taipei, Taiwan. 11Department of Non-communicable Dis- always associated with AA-mediated mutations, and this AA ease Epidemiology, London School of Hygiene and Tropical Medicine, London, signature was also identified throughout the Asian world and United Kingdom. 12Department of Public Health, China Medical University, again among Asian patients treated elsewhere (9). Furthermore, Taichung, Taiwan. 13Innovation and Policy Centre for Population Health and there was a significant dose–response relationship between the Sustainable Environment, National Taiwan University College of Public Health, consumption of AA and HCC in patients with HBV infection in Taipei, Taiwan. 14Office of Occupational Safety and Health, National Taiwan Taiwan (10). University Hospital, Taipei, Taiwan. Persons infected with hepatitis C virus (HCV) had more than Note: C.-J. Chen and Y.-H. Yang contributed equally to this article. 15-fold higher HCC risk than uninfected persons (11). HCV Corresponding Authors: Pau-Chung Chen, National Taiwan University, 17 Xuz- infection is still a major public health burden in Taiwan, the hou Road, Taipei 10055, Taiwan. Phone: 88-6-2-3366-8088; Fax: 88-6-2-3366- United States, and worldwide, especially in relation to HCC and 8734; E-mail: [email protected]; and Wen-Chao Ho, Department of Public cancer-related mortality (12). Plants containing AA were prohib- Health, China Medical University, 91 Hsueh-Shih Road, Taichung 40402, Taiwan. Phone: 88-6-04-2205-3366, ext. 6117; E-mail: [email protected] ited in some countries and in Taiwan since November 2003 (13); however, more than 30% of the population in Taiwan was Cancer Epidemiol Biomarkers Prev 2019;XX:XX–XX reportedly prescribed Chinese herbs containing AA between doi: 10.1158/1055-9965.EPI-19-0023 1997 and 2003 (14). Given the lack of a large population- Ó2019 American Association for Cancer Research. based study assessing the effect of AA exposure on risk of primary www.aacrjournals.org OF1 Downloaded from cebp.aacrjournals.org on September 24, 2021. © 2019 American Association for Cancer Research. Published OnlineFirst August 13, 2019; DOI: 10.1158/1055-9965.EPI-19-0023 Chen et al. liver cancer (PLC) in HCV-infected individuals, the objective of this research was to investigate whether the use of herbal medicine Total number of beneficiaries, 1997–2010, (HM) containing AA was associated with increased risk of PLC from NHI database in Taiwan N among HCV-infected patients. ( = 22,717,053) Materials and Methods HCV infection cohort ages 18 years or Data source older (ICD-9: 070.7, 070.41, 070.44, National Health Insurance (NHI) Research Database was used n for the current analysis, and the study design has been described in 070.51, 070.54, V02.62) ( = 406,460) detail previously (15). In brief, the NHI program has provided compulsory universal health insurance since 1995 including both traditional Chinese and western medicine for most of the coun- try's population (99%). Data were collected from both hospital Excluded n admissions and outpatient visits and included following patient 1. Incomplete data ( = 3,613) characteristics: sex, birth dates, dates of visits, date of admission, 2. Co-HBV (ICD-9: 070.2, 070.3, n date of discharge, and up to three outpatient visit diagnoses or five V02.61) patients ( = 133,559) discharge diagnoses defined by International Classification of Diseases, Ninth Revision classification (ICD-9). Patient prescrip- tion information, duration, and drug dosage were also collected. According to the study criteria mentioned above, a population- Excluded based cohort of patients ages 18 years or older who had a 1. PLC (ICD-9: 155.0) before diagnosis of HCV infection (ICD-9 codes 070.41, 070.44, January 1, 1999 (n = 2,485) 070.51, 070.54, 070.7, and V02.62) without HBV infection 2. Without visiting Chinese (ICD-9 codes 070.2, 070.3, and V02.61) between January 1, medicine clinics (n = 43,336) 1997, and December 31, 2010, was identified and included in the final analysis (Fig. 1; refs. 16, 17). For ensuring comparability, only patients who had visited traditional Chinese medicine clinics between January 1, 1997, and 1 year prior to the diagnosis of PLC Patients with HCV infection (n = 223,467) or the censor dates were included. In accordance with personal electronic data protection regulations, strict confidentiality guide- line was closely followed. The National Health Research Institutes Figure 1. (NHRI) of Taiwan maintains and anonymizes the NHI reim- Study design flowchart. bursement data as files suitable for study. This research was also approved by the Institutional Review Board of the National Taiwan University Hospital. Diagnosis of PLC Patients with PLC were identified by diagnostic code, ICD-9 Exposure of HM containing AA code 155.0, and the initial diagnosis used as the index date. The Following standard prescriptions recommended by the Com- diagnosis of PLC was made following the recommendation of the mittee on Chinese Medicine and Pharmacy in Taiwan, HM American Association for the Study of Liver Diseases Practice produced prior to promulgation of new regulations in November Guidelines, NHI (24). To improve the validity of the diagnosis, 2003 could include the following herbs containing AA: Guang only PLC patients who met the diagnosis criteria aforementioned Fang Ji (Aristolochia fangji), Guan Mu Tong (Aristolochia manshur- were included in the analysis. Additional analyses of newly iensis), Ma Dou Ling (fruits of Aristolochia contorta or Aristolochia diagnosed patients from January 1, 1999, to December 31, debilis), Qing Mu Xiang (roots of Aristolochia debilis), Tian Xian 2013, were performed to ensure that all subjects had a minimum Teng (stems and leaves of Aristolochia contorta or Aristolochia 2-year exposure to HM prior to diagnosis with PLC. debilis), and Xi Xin (Asarum sieboldii or Asarum heterotropoides; ref. 18). Upon the recommendation of ancient Chinese medicine Potential confounders books, these herbs were taken as either single products or com- Comorbid diagnoses were identified as potential confounders ponents of mixed herbal formulas. The original amount of herbs recorded beginning January 1, 1997, to 1 year before the diagnosis was determined in the unit of grams for each mixture of HM and of PLC or the censor dates.
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