Elevated Arsenic Exposure Is Associated with an Increased Risk of Chronic Hepatitis B Virus Infection: NHANES (2003–2014) in U.S. Adults

Abstract

Studies concerning the association between arsenic exposure and hepatitis B virus (HB V) infection have been lacking. The present study aimed to examine the association between total urinary arsenic (TUA) and infection of HBV. A total of 5186 participants from National Health and Nutrition Examination Survey (NHANES) 2003–2014 were included in the analysis. We used logistic regression to evaluate the association. We defined two measures of TUA. TUAI was the sum of arsenous acid, arsenicacid, monomethylarsonic acid and dimethylarsenic acid. TUA2 was defined as TUA minus arsenobetaine and arsenocholine. The results showed that the weighted overall prevalence of HBV infection was 6.08%. For NHANES 2003–2014, the medians (interquartile range) of TUAI and TUA2 were 5.60 μg/L (3.97–8.09 μg/L) and 4.91 μg/L (2.36–9.11 μg/L), respectively. Comparing the highest quartile to the lowest quartile after multivariable adjustment showed that the odds ratios (ORs) and 95% confidence intervals (CIs) for TUAI and TUA2 were 2.44 (1.40–4.27) and 2.84 (1.60–5.05), respectively. In conclusion, elevated urinary arsenic was associated with the risk of HBV infection. Further studies, especially prospective studies, are needed to confirm the causal relationship between arsenic exposure and HBV infection.

Keywords

arsenic / exposure / hepatitis B / infection / National Health and Nutrition Examination Survey

References

[1] ShakoorMB, NawazR, HussainF, et al.. Human health implications, risk assessment and remediation of As-contaminated water: A critical review. Sei Total Environ, 2017, 601–602: 756

[2] NachmanKE, BaronPA, RäberG, et al.. Roxarsone, inorganic arsenic, and other arsenic species in chicken: a U.S.-based market basket sample. Environ Health Perspect, 2013, 121(7): 818-824

[3] NigraAE, NachmanKE, LoveDC, et al.. Poultry consumption and arsenic exposure in the U.S. population. Environ Health Perspect, 2017, 125(3): 370-377

[4] RahmanA, VahterM, EkstromEC, et al.. Arsenic exposure in pregnancy increases the risk of lower respiratory tract infection and diarrhea during infancy in Bangladesh. Environ Health Perspect, 2011, 119(5): 719-724

[5] RaqibR, AhmedS, SultanaR, et al.. Effects of in utero arsenic exposure on child immunity and morbidity in rural Bangladesh. Toxicol Lett, 2009, 185(3): 197-202

[6] HeaneyCD, KmushB, Navas-AcienA, et al.. Arsenic exposure and hepatitis E virus infection during pregnancy. Environ Res, 2015, 142: 273-280

[7] CardenasA, SmitE, BethelJW, et al.. Arsenic exposure and the seroprevalence of total hepatitis A antibodies in the US population: NHANES, 2003–2012. Epidemiol Infect, 2016, 144(8): 1641-1651

[8] CardenasA, SmitE, HousemanEA, et al.. Arsenic exposure and prevalence of the varicella zoster virus in the United States: NHANES (2003–2004 and 2009–2010). Environ Health Perspect, 2015, 123(6): 590-596

[9] SchweitzerA, HornJ, MikolajczykRT, et al.. Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet, 2015, 386(10003): 1546-1555

[10] de MartelC, Maucort-BoulchD, PlummerM, et al.. World-wide relative contribution of hepatitis B and C viruses in hepatocellular carcinoma. Hepatology, 2015, 62(4): 1190-1200

[11] FattovichG, BortolottiF, DonatoF. Natural history of chronic hepatitis B: special emphasis on disease progression and prognostic factors. J Hepatol, 2008, 48(2): 335-352

[12] WasleyA, GrytdalS, GallagherK. Surveillance for acute viral hepatitis-United States, 2006. MMWR Surveill Summ, 2008

[13] CDC. About the National Health and Nutrition Examination Survey: Introduction. Available: https://doi.org/www.cdc.gov/nchs/nhanes/about_nhanes.htm [accessed 11 October 2017]. 2014.

[14] CDC.. National Center for Health Statistics: National Health and Nutrition Examination Survey: Analytic Guidelines, 1999–2010. Centers for Disease Control and Prevention, 2013

[15] KruegerWS, WadeTJ. Elevated blood lead and cadmium levels associated with chronic infections among non-smokers in a cross-sectional analysis of NHANES data. Environ Health, 2016, 15: 16

[16] NCHS: Laboratory Procedure Manual, Hepatitis B Core Antibody. Available: https://doi.org/wwwn.cdc.gov/nchs/data/nhanes/2013-2014/labmethods/HEPBD_H_Hepatitis%20B%20core%20antibody_met.pdf [accessed 24 October 2017] 2014.

[17] CaldwellKL, JonesRL, VerdonCP, et al.. Levels of urinary total and speciated arsenic in the US population: National Health and Nutrition Examination Survey 2003–2004. J Expo Sei Environ Epidemiol, 2009

[18] NCHS: Laboratory Procedure Manual, Total Arsenic. Available: https://doi.org/wwwn.cdc.gov/nchs/data/nhanes/2013-2014/labmethods/UM_UMS_UTAS_UTASS_H_MET.pdf [accessed 24 October 2017]. 2014.

[19] NCHS: Laboratory Procedure Manual, Urinary speciated arsenics. Available: https://doi.org/wwwn.cdc.gov/nchs/data/nhanes/2013-2014/labmethods/UAS_UASS_H_MET.pdf [accessed 24 October 2017] 2014.

[20] Frediani, NaiotiEA, VosMB, et al.. Arsenic exposure and risk of nonalcoholic fatty liver disease (NAFLD) among U.S. adolescents and adults: an association modified by race/ethnicity, NHANES 2005–2014. Environ Health, 2018, 17(1): 6

[21] MurerAJ, AbildtrupA, PoulsenOM, et al.. Effect of seafood consumption on the urinary level of total hydride-generating arsenic compounds. Instability of arsenobetaine and arsenocholine. Analyst, 1992, 117(3): 677-680

[22] NCHS: Laboratory Procedure Manual, Urinary Creatinine. Available: https://doi.org/wwwn.cdc.gov/nchs/data/nhanes/2013-2014/labmethods/BIOPRO_H_MET_CREATININE.pdf [accessed 24 October 2017] 2014.

[23] SheehanMC, BurkeTA, BreyssePN, et al.. Association of markers of chronic viral hepatitis and blood mercury levels in US reproductive-age women from NHANES 2001–2008: a cross-sectional study. Environ Health, 2012, 11(1): 62

[24] AlanA. Categorical Data Analysis, 3rd edition. Statistical Methods & Applicaticms, 2002, 14(1): 109-109

[25] KuoCC, WeaverV, FadrowskiJJ, et al.. Arsenic exposure, hyperuricemia, and gout in US adults. Environ Int, 2015, 76: 32-40

[26] BanerjeeN, BaneijeeS, SenR, et al.. Chronic arsenic exposure impairs macrophage functions in the exposed individuals. J Clin Immunol, 2009, 29(5): 582-594

[27] BurnsLA, McCayJA, BrownR, et al.. Arsenic in the sera of gallium arsenide-exposed mice inhibits bacterial growth and increases host resistance. J Pharmacol Exp Ther, 1993, 265(2): 795-800

[28] Hernandez-CastroB, Doniz-PadillaLM, Salgado-BustamanteM, et al.. Effect of arsenic on regulatory T cells. J Clin Immunol, 2009, 29(4): 461-469

[29] BiswasR, GhoshP, BanerjeeN, et al.. Analysis of T-cell proliferation and cytokine secretion in the individuals exposed to arsenic. Hum Exp Toxicol, 2008, 27(5): 381-386

[30] Soto-PenaGA, LunaAL, Acosta-SaavedraL, et al.. Assessment of lymphocyte subpopulations and cytokine secretion in children exposed to arsenic. FASEB J, 2006, 20(6): 779-781

[31] AhmedS, MooreSE, KipplerM, et al.. Arsenic exposure and cell-mediated immunity in preschool children in rural Bangladesh. Toxicol Sei, 2014, 141(1): 166-175

[32] LinX, XuX, ZengX, et al.. Decreased vaccine antibody liters following exposure to multiple metals and metalloids in e-waste-exposed preschool children. Environ Pollut, 2017

[33] DanglebenNL, SkibolaCF, SmithMT. Arsenic immunotoxicity: a review, 2013

[34] MitchellAM, LiC, SamulskiRJ. Arsenic trioxide stabilizes accumulations of adeno-associated virus virions at the perinuclear region, increasing transduction in vitro and in vivo. J Virol, 2013, 87(8): 4571-4583

[35] DrobnaZ, WaltonFS, PaulDS, et al.. Metabolism of arsenic in human liver: the role of membrane transporters. Arch Toxicol, 2010, 84(1): 3-16

[36] BenramdaneL, AccominottiM, FantonL, et al.. Arsenic speciation in human organs following fatal arsenic trioxide poisoning~a case report. Clin Chem, 1999, 45(2): 301-306

[37] BustaffaE, StoccoroA, BianchiF, et al.. Genotoxic and epigenetic mechanisms in arsenic carcinogenicity. Arch Toxicol, 2014, 88(5): 1043-1067

[38] TokarEJ, KojimaC, WaalkesMP. Methylarsonous acid causes oxidative DNA damage in cells independent of the ability to biomethylate inorganic arsenic. Arch Toxicol, 2014

[39] ZhangZ, GaoL, ChengY, et al.. Resveratrol, a natural antioxidant, has a protective effect on liver injury induced by inorganic arsenic exposure. Biomed Res Int5, 2014, 2014: 617202

[40] MazumderDN. Effect of chronic intake of arsenic-contaminated water on liver. Toxicol Appl Pharmacol, 2005, 206(2): 169-175

[41] ShiX, WeiX, KooI, et al.. Metabolomic analysis of the effects of chronic arsenic exposure in a mouse model of diet-induced fatty liver disease. J Proteome Res, 2014, 13(2): 547-554

[42] HuangYK, TsengCH, HuangYL, et al.. Arsenic methylation capability and hypertension risk in subjects living in arseniasis-hyperendemic areas in southwestern Taiwan. Toxicol Appl Pharmacol, 2007, 218(2): 135-142

[43] ShouvalD, ShiboletO. Immunosuppression and HBV reactivation. Semin Liver Dis, 2013, 33(2): 167-177