Abstract
To elucidate the potential factors modulating exposure to aflatoxin B1 (AFB1) in three Chinese populations, an epidemiologic study was conducted in Fusui County and Nanning City of Guangxi Province and Chengdu City of Sichuan Province. The incidence rates of hepatocelluar carcinoma (HCC) for males in these three regions were 92–97 per 100,000, 32–47 per 100,000, and 21 per 100,000, respectively. Eighty-nine residents from Fusui, 196 residents from Nanning, and 118 residents from Chengdu were screened for AFB1–albumin adduct (AAA) levels and hepatitis virus (HBV, HCV, HDV, HEV, and HGV) infections, as well as liver biochemistry (alanine aminotransferase [ALT], aspartate aminotransferase [AST], alkaline phosphatase [ALP], γ-glutamyl transpeptidase [GGT], 5′-nucleotidase, globulin [GLO], direct bilirubin, indirect bilirubin, and bile acid levels). At least one marker of hepatitis virus (HV) infection was present in 47.2% (42/89) of subjects from Fusui, while in Nanning and Chengdu the values were 15.8% (31/196) and 22.0% (26/118), respectively. In contrast to females, a higher level of AAA was observed in males; the difference was statistically significant in both the Nanning (P = 0.023) and the Chengdu (P = 0.026) subjects. In the Chengdu group, there was a significantly higher level of AAA in cases with HV infection (P = 0.041). There was a close association between AAA level and BMI in the adults without HV infection (r = 0.148, P = 0.044). Also, AAA was closely associated with DBIL and GGT in non-HV-infected minors (P < 0.05), closely associated with ALB, GLO, and GGT in HV-infected minors (P < 0.05), and closely associated with IBIL, GLO, TBA, and AST in non-HV-infected adults (P < 0.01). The co-effect of HV infection and AFB1 exposure may be responsible for the high risk of HCC in the Fusui region, whereas age, gender, BMI, and HV infection may modify individual aflatoxin levels. The relationship between AAA level and liver biochemistry indicates injury induced by aflatoxin to both hepatic parenchyma and biliary tract. But the associations vary with age and HV infection status.
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References
National Cancer Control Office: Atlas of Cancer Mortality in The People’s Republic of China. Shanghai, Nanjing Institute of Geography, China Map Press, 1979
Huang TR, Yu JH, Zhang ZQ, et al.: Analysis on epidemic feature and secular trend of primary liver cancer in Guangxi. Guangxi Med J 22:677–679, 2000
Yeh FS, Mo CC, Luo S, Henderson BE, Tong MJ, Yu M: A serological case-control study of primary hepatocellular carcinoma in Guangxi, China. Cancer Res 45:872–873, 1985
Wang JS, Huang T, Su J, et al.: Hepatocellular carcinoma and aflatoxin exposure in Zhuqing Village, Fusui County, People’s Republic of China. Cancer Epidemiol Biomarkers Prev 10:143–146, 2001
Yeh FS, Yu MC, Mo CC, Luo S, Tong MJ. Henderson BE: Hepatitis B virus, aflatoxins, and hepatocellular carcinoma in southern Guangxi, China. Cancer Res 49:2506–2509, 1989
Gan LS, Skipper PL, Peng XC, et al.: Serum albumin adducts in the molecular epidemiology of aflatoxin carcinogenesis: correlation with aflatoxin B1 intake and urinary excretion of aflatoxin M1. Carcinogenesis 9:1323–1325, 1988
Groopman JD, Zhu JQ, Donahue PR, et al.: Molecular dosimetry of urinary aflatoxin-DNA adducts in people living in Guangxi Autonomous Region, People’s Republic of China. Cancer Res 52:45–52, 1992
Wang Y, Wang DQ, Song Y, Deng Y, Zhang ZG: Continuous monitoring of oncology death in Sichuan Province from 1989 to 1993. Zhong Liu Fang Zhi [Oncol Prev Treat] 34:1–4, 1995 (Chinese)
Chen SY, Chen CJ, Chou SR, et al.: Association of aflatoxin B(1)-albumin adduct levels with hepatitis B surface antigen status among adolescents in Taiwan. Cancer Epidemiol Biomarkers Prev 10:1223–1226, 2001
Chen CJ, Wang LY, Lu SN, et al.: Elevated aflatoxin exposure and increased risk of hepatocellular carcinoma. Hepatology 24:38–42, 1996
Santella RM, Yang XY, Hsieh LL, Young TL: Immunologic methods for the detection of carcinogen adducts in humans. Prog Clin Biol Res 340C:247–257, 1990
Santella RM, Zhang YJ, Chen CJ, et al.: Immunohistochemical detection of aflatoxin B1-DNA adducts and hepatitis B virus antigens in hepatocellular carcinoma and nontumorous liver tissue. Environ Health Perspect 99:199–202, 1993
Wild CP, Fortuin M, Donato F, et al.: Aflatoxin, liver enzymes, and hepatitis B virus infection in Gambian children. Cancer Epidemiol Biomarkers Prev 2:555–561, 1993
Wild CP, Yin F, Turner PC, et al.: Environmental and genetic determinants of aflatoxin-albumin adducts in Gambia. Int J Cancer 86:1–7, 2000
Chen SY, Chen CJ, Tsai WY, et al.: Associations of plasma aflatoxin B1-albumin adduct level with plasma selenium level and genetic polymorphisms of glutathione S-transferase M1 and T1. Nutr Cancer 38:179–185, 2000
Nishida S, Endo N, Yamagiwa H, Tanizawa T, Takahashi HE: Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. J Bone Miner Metab 17:171–177, 1999
Wang JS, Qian GS, Zarba A, et al.: Temporal patterns of aflatoxin-albumin adducts in hepatitis B surface antigen-positive and antigen-negative residents of Daxin, Qidong County, People’s Republic of China. Cancer Epidemiol Biomarkers Prev 5:253–261, 1996
Zhu JQ, Zhang LS, Hu X, et al.: Correlation of dietary aflatoxin B1 levels with excretion of aflatoxin M1 in human urine. Cancer Res 47:1848–1852, 1987
Hou W, Li J, Yang Y, et al.: A study on chemical pollutant in Chengdu inhabitants’ total diets. [Modern Preventive Medicine] 26:183–185, 1999 (Chinese)
De Flora S, Hietanen E, Bartsch H, et al.: Enhanced metabolic activation of chemical hepatocarcinogens in woodchucks infected with hepatitis B virus. Carcinogenesis 10:1099–1106, 1989
Reddy RV, Sharma RP: Effects of aflatoxin B1 on murine lymphocytic functions. Toxicology 54:31–44, 1989
Cusumano V, Rossano F, Merendino RA, et al.: Immunobiological activities of mould products: functional impairment of human monocytes exposed to aflatoxin B1. Res Microbiol 147:385–391, 1996
Barraud L, Guerret S, Chevallier M, et al.: Enhanced duck hepatitis B virus gene expression following aflatoxin B1 exposure. Hepatology 29:1317–1323, 1999
Allen SJ, Wild CP, Wheeler JG, et al.: Aflatoxin exposure, malaria and hepatitis B infection in rural Gambian children. Trans R Soc Trop Med Hyg 86:426–430, 1992
Turner PC, Mendy M, Whittle H, Fortuin M, Hall AJ, Wild CP: Hepatitis B infection and aflatoxin biomarker levels in Gambian children. Trop Med Int Health 5:837–841, 2000
Sun CA, Wu DM, Wang LY, Chen CJ, You SL, Santella RM: Determinants of formation of aflatoxin-albumin adducts: a seven-township study in Taiwan. Br J Cancer 87: 966–970, 2002
Tanaka E: Gender-related differences in pharmacokinetics and their clinical significance. J Clin Pharm Ther 24:339–346, 1999
Ahsan H, Wang LY, Chen CJ, Tsai WY, Santella RM: Variability in aflatoxin-albumin adduct levels and effects of hepatitis B and C virus infection and glutathione S-transferase M1 and T1 genotype. Environ Health Perspect 109:833–837, 2001
Moundipa PF, Domngang FM: Effect of the leafy vegetable Solanum nigrum on the activities of some liver drug-metabolizing enzymes after aflatoxin B1 treatment in female rats. Br J Nutr 65:81–91, 1991
Yousef MI, Salem MH, Kamel KI, Hassan GA, El Nouty FD: Influence of ascorbic acid supplementation on the haematological and clinical biochemistry parameters of male rabbits exposed to aflatoxin B1. J Environ Sci Health B 38:193–209, 2003
Barton CC, Hill DA, Yee SB, Barton EX, Ganey PE, Roth RA: Bacterial lipopolysaccharide exposure augments aflatoxin B(1)-induced liver injury. Toxicol Sci 55:444–452, 2000
Singh J, Tiwari RP, Singh G, Singh S, Vadehra DV: Biochemical and immunological effects of aflatoxins in rabbits. Toxicol Lett 35:225–230, 1987
Clark JD, Hatch RC, Miller DM, Jain AV: Caprine aflatoxicosis: experimental disease and clinical pathologic changes. Am J Vet Res 45:1132–1135, 1984
Cheng YH, Shen TF, Pang VF, Chen BJ: Effects of aflatoxin and carotenoids on growth performance and immune response in mule ducklings. Comp Biochem.Physiol C Toxicol Pharmacol 128:19–26, 2001
Sabbioni G, Skipper PL, Buchi G, Tannenbaum SR: Isolation and characterization of the major serum albumin adduct formed by aflatoxin B1 in vivo in rats. Carcinogenesis 8:819–824, 1987
Sodeinde O, Chan MC, Maxwell SM, Familusi JB, Hendrickse RG: Neonatal jaundice, aflatoxins and naphthols: report of a study in Ibadan, Nigeria. Ann Trop Paediatr 15:107–113, 1995
Quist CF, Howerth EW, Fischer JR, Wyatt RD, Miller DM, Nettles VF: Evaluation of low-level aflatoxin in the diet of white-tailed deer. J Wildl Dis 33:112–121, 1997
Baetz AL, McLoughlin ME: Serum concentration of bile acids in guinea pigs as an indicator of liver damage caused by aflatoxins. Am J Vet Res 44:1971–1972, 1983
Harvey RB, Huff WE, Kubena LF, Corrier DE, Phillips TD: Progression of aflatoxicosis in growing barrows. Am J Vet Res 49:482–487, 1988
Carrillo MC, Rodriguez JV, Monti JA, Pellegrino JM, Rodriguez Garay EA: Impairment of bile secretion induced by aflatoxin B1 in the rat. Res Commun Chem Pathol Pharmacol 38:521–524, 1982
Muller N, Petzinger E: Hepatocellular uptake of aflatoxin B1 by non-ionic diffusion. Inhibition of bile acid transport by interference with membrane lipids. Biochim Biophys Acta 938:334–344, 1988
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Tao, P., Zhi-Ming, L., Tang-Wei, L. et al. Associated Factors in Modulating Aflatoxin B1–Albumin Adduct Level in Three Chinese Populations. Dig Dis Sci 50, 525–532 (2005). https://doi.org/10.1007/s10620-005-2468-1
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DOI: https://doi.org/10.1007/s10620-005-2468-1