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Environmental exposure and clinical correlates of hepatocellular carcinoma in New York City: a case only study


In the U.S., Hepatocellular carcinoma (HCC) incidence rates have increased. We aimed to determine whether environmental exposure plays a role in the high incidence of HCC observed in New York City. We conducted a hospital-based case only study to examine the prevalence of aflatoxin B1 (AFB1)- and polycyclic aromatic hydrocarbon (PAH)-albumin adducts and the distribution of adducts by different characteristics of HCC patients. Blood samples were collected from 155 HCC patients for biomarker analyses. We observed that about 46% and 49% of cases had detectable AFB1- and PAH-albumin adducts, respectively. There were significant differences between AFB1-albumin adducts and selected factors such as HCV infection status (p = 0.04), diabetes (p = 0.03) and Barcelona Clinic Liver Cancer stage (p = 0.02). Cases with detectable PAH-albumin adducts had a smoking history compared with those with nondetectable levels (p = 0.04). The level of AFB1-albumin adducts was positively correlated with plasma bilirubin (rs = 0.32, p < 0.0001) and adiponectin concentrations (rs = 0.28, p = 0.0005). The level of aflatoxin B1-albumin adducts was negatively associated with blood albumin concentration (rs = − 0.28, p = 0.0009) and plasma DNA LINE-1 methylation (rs = − 0.16, p = 0.04). Our study provides additional evidence that environmental exposures including to aflatoxin might drive the high incidence of HCC observed in the New York City.

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Fig. 1


  1. 1.

    White DL, Thrift AP, Kanwal F, Davila J, El-Serag HB (2017) Incidence of Hepatocellular carcinoma in All 50 United States, from 2000 through 2012. Gastroenterology 152(4):812-820.e815

    Article  Google Scholar 

  2. 2.

    Kamath GR, Taioli E, Egorova N et al (2018) Liver cancer disparities in New York City: a neighborhood view of risk and harm reduction factors. Front Oncol 8:220–220

    Article  Google Scholar 

  3. 3.

    Phillips DH (1999) Polycyclic aromatic hydrocarbons in the diet. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 443(1):139–147

    CAS  Article  Google Scholar 

  4. 4.

    Wu H-C, Wang Q, Wang L-W et al (2007) Polycyclic aromatic hydrocarbon- and aflatoxin-albumin adducts, and Hepatitis B virus infection and Hepatocellular carcinoma in Taiwan. Cancer Lett 252(1):104–114

    CAS  Article  Google Scholar 

  5. 5.

    Johnson NM, Qian G, Xu L et al (2010) Aflatoxin and PAH exposure biomarkers in a U.S. population with a high incidence of hepatocellular carcinoma. Sci Total Environ 408(23):6027–6031

    CAS  Article  Google Scholar 

  6. 6.

    Huang MN, Yu W, Teoh WW et al (2017) Genome-scale mutational signatures of aflatoxin in cells, mice, and human tumors. Genom Res 27(9):1475–1486

    CAS  Article  Google Scholar 

  7. 7.

    Eskola M, Kos G, Elliott CT, Hajšlová J, Mayar S, Krska R (2020) Worldwide contamination of food-crops with mycotoxins: validity of the widely cited ‘FAO estimate’ of 25. Crit Rev Food Sci Nutr 60(16):2773–2789

    CAS  Article  Google Scholar 

  8. 8.

    Peromingo B, Rodríguez A, Bernáldez V, Delgado J, Rodríguez M (2016) Effect of temperature and water activity on growth and aflatoxin production by Aspergillus flavus and Aspergillus parasiticus on cured meat model systems. Meat Sci 122:76–83

    CAS  Article  Google Scholar 

  9. 9.

    Turner PC, Snyder JA (2021) Development and limitations of exposure biomarkers to dietary contaminants mycotoxins. Toxins (Basel) 13(5):314

    CAS  Article  Google Scholar 

  10. 10.

    Scholl PF, Turner PC, Sutcliffe AE et al (2006) Quantitative comparison of aflatoxin B1 serum albumin adducts in humans by isotope dilution mass spectrometry and ELISA. Cancer Epidemiol Biomark Prev 15(4):823–826

    CAS  Article  Google Scholar 

  11. 11.

    Scholl PF, McCoy L, Kensler TW, Groopman JD (2006) Quantitative analysis and chronic dosimetry of the aflatoxin B1 plasma albumin adduct Lys-AFB1 in rats by isotope dilution mass spectrometry. Chem Res Toxicol 19(1):44–49

    CAS  Article  Google Scholar 

  12. 12.

    Schleicher RL, McCoy LF, Powers CD, Sternberg MR, Pfeiffer CM (2013) Serum concentrations of an aflatoxin-albumin adduct in the National Health and Nutrition Examination Survey (NHANES) 1999–2000. Clin Chim Acta 423:46–50

    CAS  Article  Google Scholar 

  13. 13.

    Xue KS, Tang L, Shen CL et al (2021) Increase in aflatoxin exposure in two populations residing in East and West Texas, United States. Int J Hyg Environ Health 231:113662

    CAS  Article  Google Scholar 

  14. 14.

    Lunn RM, Zhang Y-J, Wang L-Y et al (1997) p53 mutations, chronic Hepatitis B virus infection, and alfatoxin exposure in Hepatocellular carcinoma in Taiwan. Can Res 57(16):3471–3477

    CAS  Google Scholar 

  15. 15.

    Jiao J, Niu W, Wang Y et al (2018) Prevalence of aflatoxin-associated tp53r249s mutation in Hepatocellular carcinoma in Hispanics in South Texas. Cancer Prev Res 11(2):103–112

    CAS  Article  Google Scholar 

  16. 16.

    Wu H-C, Wang Q, Yang H-I et al (2009) Aflatoxin B(1) exposure, Hepatitis B virus infection and Hepatocellular carcinoma in Taiwan. Cancer Epidemiol Biomark Prev 18(3):846–853

    CAS  Article  Google Scholar 

  17. 17.

    Qian GS, Ross RK, Yu MC et al (1994) A follow-up study of urinary markers of aflatoxin exposure and liver cancer risk in Shanghai, People’s Republic of China. Cancer Epidemiol Biomark Prev 3(1):3–10

    CAS  Google Scholar 

  18. 18.

    Chu Y-J, Yang H-I, Wu H-C et al (2018) Aflatoxin B(1) exposure increases the risk of hepatocellular carcinoma associated with hepatitis C virus infection or alcohol consumption. Eur J Cancer (Oxford, England: 1990) 94:37–46

    CAS  Article  Google Scholar 

  19. 19.

    Deng T, Lyon CJ, Bergin S, Caligiuri MA, Hsueh WA (2016) Obesity, inflammation, and cancer. Annu Rev Pathol 11:421–449

    CAS  Article  Google Scholar 

  20. 20.

    Chen MJ, Yeh YT, Lee KT, Tsai CJ, Lee HH, Wang SN (2012) The promoting effect of adiponectin in hepatocellular carcinoma. J Surg Oncol 106(2):181–187

    CAS  Article  Google Scholar 

  21. 21.

    Yeh C-C, Goyal A, Shen J et al (2017) Global level of plasma DNA methylation is associated with overall survival in patients with Hepatocellular carcinoma. Ann Surg Oncol 24(12):3788–3795

    Article  Google Scholar 

  22. 22.

    Mohsenzadeh MS, Hedayati N, Riahi-Zanjani B, Karimi G (2016) Immunosuppression following dietary aflatoxin B1 exposure: a review of the existing evidence. Toxin Rev 35(3–4):121–127

    CAS  Article  Google Scholar 

  23. 23.

    Petrick JL, Campbell PT, Koshiol J et al (2018) Tobacco, alcohol use and risk of hepatocellular carcinoma and intrahepatic cholangiocarcinoma: the liver cancer pooling project. Br J Cancer 118(7):1005–1012

    Article  Google Scholar 

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This work was supported by awards from the National Cancer Institute [R01ES005116 and P30 CA013696] and the National Institute of Environmental Health Sciences [P30 ES009089]. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

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Conceptualization (H-CW, JS, AS, and RMS), Data curation (H-CW, JS, AS, and RMS), Formal analysis (H-CW), Funding acquisition (AS, and RMS), Investigation (H-CW, JS, AS, and RMS), Methodology (H-CW, and RMS), Project administration (H-CW and RMS), Resource (RMS), Software (H-CW), Supervision (RMS), Writing-original draft (H-CW), writing-review/editing (H-CW, JS, AS, and RMS),

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Correspondence to Hui-Chen Wu.

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Wu, HC., Shen, J., Siegel, A. et al. Environmental exposure and clinical correlates of hepatocellular carcinoma in New York City: a case only study. Cancer Causes Control (2021).

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  • Aflatoxin
  • Aflatoxin B1-albumin adduct
  • Hepatocellular carcinoma
  • LINE-1 methylation
  • Adiponectin
  • Polycyclic aromatic hydrocarbon