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Environmental Science and Pollution Research

, Volume 26, Issue 30, pp 31384–31391 | Cite as

Associations between mercury exposure and the risk of nonalcoholic fatty liver disease (NAFLD) in US adolescents

  • Runsen Chen
  • Yang Xu
  • Cheng Xu
  • Yaqin Shu
  • Siyu Ma
  • Changgui Lu
  • Xuming MoEmail author
Research Article
  • 106 Downloads

Abstract

Little is known regarding the effects of environmental mercury (Hg) exposure on liver dysfunction in adolescents. We aimed to explore the association between Hg exposure and the risk of nonalcoholic fatty liver disease (NAFLD) in the adolescent population. The cross-sectional associations between blood Hg concentrations and serum alanine aminotransferase (ALT) levels, a surrogate for suspected NAFLD, were evaluated using data from adolescents (aged 12–17 years old) who participated in the National Health and Nutrition Examination Survey (NHANES), 1999–2014. A final sample of 6389 adolescents was analysed. Elevated ALT was defined as > 25 IU/L and > 22 IU/L for boys and girls ≤ 17 years old, respectively. Odds ratios (ORs) of Hg levels in association with serum ALT levels were estimated using a logistic regression after adjusting for gender, age, ethnicity, serum cotinine, body mass index, the poverty income ratio, and NHANES cycles. The median blood Hg level was 0.73 ± 0.91 μg/L amongst US adolescents. In the adjusted model, the ORs of elevated ALT levels of those in the 4th quartile were higher amongst non-Hispanic white adolescents (OR = 1.76, 95% CI 1.20, 2.59; P = 0.035) and those who were normal or underweight (OR = 1.41, 95% CI 1.08, 1.85; P = 0.020). No association was observed for the other variables. Our results indicate that the positive association between blood Hg exposure and the risk of NAFLD in US adolescents is the highest amongst non-Hispanic white and those who are normal or underweight, regardless of ethnicity. More research is necessary to confirm this association and to clarify the potential mechanisms.

Keywords

NHANES Mercury Adolescent Nonalcoholic fatty liver disease (NAFLD) Alanine aminotransferase 

Notes

Author contribution

Runsen Chen and Yang Xu wrote the main manuscript text, Yaqin Shu and Siyu Ma prepared Tables 1, 2, and 3, and Changgui Lu prepared Fig. 1. Cheng Xu and Xuming Mo were responsible for the accuracy of all content in the proof. All authors reviewed the manuscript.

Funding information

This work was supported by funding from the National Key Research and Development Program of China (2017YFC1308105; 2016YFC1101001); Key Project supported by Medical Science and Technology Development Foundation, Nanjing Department of Health (201723006).

Compliance with ethical standards

Ethics approval and consent to participate

The consent form was signed by participants in the survey, and participants consented to storing specimens of their blood for future research. The CDC/NCHS Ethics Review Board (ERB) approved the NHANES study and gave approval for public dissemination.

Consent for publication

Non applicable. There is no individual level data in our publication.

References

  1. Alkhouri N, Feldstein AE (2016) Noninvasive diagnosis of nonalcoholic fatty liver disease: Are we there yet? Metabolism 65:1087–1095CrossRefGoogle Scholar
  2. Andreoli V, Sprovieri F (2017) Genetic Aspects of Susceptibility to Mercury Toxicity: An Overview. Int J Environ Res Public Health 14Google Scholar
  3. Basu N, Goodrich JM, Head J (2014) Ecogenetics of mercury: from genetic polymorphisms and epigenetics to risk assessment and decision-making. Environ Toxicol Chem 33:1248–1258CrossRefGoogle Scholar
  4. Cave M, Appana S, Patel M, Falkner KC, McClain CJ, Brock G (2010) Polychlorinated biphenyls, lead, and mercury are associated with liver disease in American adults: NHANES 2003-2004. Environ Health Perspect 118:1735–1742CrossRefGoogle Scholar
  5. Centers for Disease Control and Prevention (2006) National Center for Health Statistics. National Health and Nutrition Examination Survey. Available at: https://wwwn.cdc.gov/Nchs/Nhanes/2005-2006/PBCD_D.htm
  6. Choi J, Bae S, Lim H, Lim JA, Lee YH, Ha M, Kwon HJ (2017) Mercury exposure in association with decrease of liver function in adults: a longitudinal study. J Prev Med Public Health 50:377–385CrossRefGoogle Scholar
  7. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320:1240–1243CrossRefGoogle Scholar
  8. Fernandes Azevedo B, Barros Furieri L, Pecanha FM, Wiggers GA, Frizera Vassallo P, Ronacher Simoes M, Fiorim J, Rossi de Batista P, Fioresi M, Rossoni L, Stefanon I, Alonso MJ, Salaices M, Valentim Vassallo D (2012) Toxic effects of mercury on the cardiovascular and central nervous systems. J Biomed Biotechnol 2012:949048CrossRefGoogle Scholar
  9. Fourth National Report on Human Exposure to Environmental Chemicals UT (2015) Centers for Disease Control and Prevention, Department of Health and Human Services: Atlanta, GA, USA, 2015. Available online: (2015): https://www.cdc.gov/biomonitoring/pdf/fourthreport_updatedtables_feb2015.pdf. Accessed 16 Apr 2018
  10. Futatsuka M, Kitano T, Nagano M, Inaoka T, Arimatsu Y, Ueno T, Wakamiya J, Miyamoto K (1992) An epidemiological study with risk analysis of liver diseases in the general population living in a methyl mercury polluted area. J Epidemiol Community Health 46:237–240CrossRefGoogle Scholar
  11. Gardner RM, Nyland JF, Silbergeld EK (2010) Differential immunotoxic effects of inorganic and organic mercury species in vitro. Toxicol Lett 198:182–190CrossRefGoogle Scholar
  12. Le MH, Devaki P, Ha NB, Jun DW, Te HS, Cheung RC, Nguyen MH (2017) Prevalence of non-alcoholic fatty liver disease and risk factors for advanced fibrosis and mortality in the United States. PLoS One 12:e0173499CrossRefGoogle Scholar
  13. Lee H, Kim Y, Sim CS, Ham JO, Kim NS, Lee BK (2014a) Associations between blood mercury levels and subclinical changes in liver enzymes among South Korean general adults: analysis of 2008-2012 Korean national health and nutrition examination survey data. Environ Res 130:14–19CrossRefGoogle Scholar
  14. Lee J, Lee SJ, Lim KT (2014b) Preventive effects of ZPDC glycoprotein (24 kDa) on hepatotoxicity induced by mercury chloride in vitro and in vivo. Cell Biochem Funct 32:520–529CrossRefGoogle Scholar
  15. Lee MR, Lim YH, Lee BE, Hong YC (2017) Blood mercury concentrations are associated with decline in liver function in an elderly population: a panel study. Environ Health 16:17CrossRefGoogle Scholar
  16. Levine KE, Fernando RA, Lang M, Essader A, Handy RW, Collins BJ (2000) Development of a method for the determination of ultra-trace level mercury in adipose tissue by cold vapour atomic fluorescence spectrometry. J Autom Methods Manag Chem 22:103–108CrossRefGoogle Scholar
  17. Llop S, Ballester F, Broberg K (2015) Effect of gene-mercury interactions on mercury toxicokinetics and neurotoxicity. Curr Environ Health Rep 2:179–194CrossRefGoogle Scholar
  18. Lye E, Legrand M, Clarke J, Probert A (2013) Blood total mercury concentrations in the Canadian population: Canadian Health Measures Survey cycle 1, 2007-2009. Can J Public Health 104:e246–e251CrossRefGoogle Scholar
  19. Minoia C, Ronchi A, Pigatto P, Guzzi G (2009) Effects of mercury on the endocrine system. Crit Rev Toxicol 39:538 author reply 539CrossRefGoogle Scholar
  20. Poursafa P, Ataee E, Motlagh ME, Ardalan G, Tajadini MH, Yazdi M, Kelishadi R (2014) Association of serum lead and mercury level with cardiometabolic risk factors and liver enzymes in a nationally representative sample of adolescents: the CASPIAN-III study. Environ Sci Pollut Res Int 21:13496–13502CrossRefGoogle Scholar
  21. Qin YY, Leung CKM, Leung AOW, Wu SC, Zheng JS, Wong MH (2010) Persistent organic pollutants and heavy metals in adipose tissues of patients with uterine leiomyomas and the association of these pollutants with seafood diet, BMI, and age. Environ Sci Pollut Res 17:229–240CrossRefGoogle Scholar
  22. Rothenberg SE, Korrick SA, Fayad R (2015) The influence of obesity on blood mercury levels for U.S. non-pregnant adults and children: NHANES 2007-2010. Environ Res 138:173–180CrossRefGoogle Scholar
  23. Ruggieri F, Majorani C, Domanico F, Alimonti A (2017) Mercury in Children: Current State on Exposure through Human Biomonitoring Studies. Int J Environ Res Public Health 14Google Scholar
  24. Ruhl CE, Everhart JE (2015) Fatty liver indices in the multiethnic United States National Health and Nutrition Examination Survey. Aliment Pharmacol Ther 41:65–76CrossRefGoogle Scholar
  25. Sattar N, Forrest E, Preiss D (2014) Non-alcoholic fatty liver disease. BMJ 349:g4596CrossRefGoogle Scholar
  26. Schuster PF, Krabbenhoft DP, Naftz DL, Cecil LD, Olson ML, Dewild JF, Susong DD, Green JR, Abbott ML (2002) Atmospheric mercury deposition during the last 270 years: a glacial ice core record of natural and anthropogenic sources. Environ Sci Technol 36:2303–2310CrossRefGoogle Scholar
  27. Schwimmer JB, Dunn W, Norman GJ, Pardee PE, Middleton MS, Kerkar N, Sirlin CB (2010) SAFETY study: alanine aminotransferase cutoff values are set too high for reliable detection of pediatric chronic liver disease. Gastroenterology 138:1357–1364 1364 e1-2CrossRefGoogle Scholar
  28. Temple JL, Cordero P, Li J, Nguyen V, Oben JA (2016) A guide to non-alcoholic fatty liver disease in childhood and adolescence. Int J Mol Sci 17Google Scholar
  29. Verma S, Jensen D, Hart J, Mohanty SR (2013) Predictive value of ALT levels for non-alcoholic steatohepatitis (NASH) and advanced fibrosis in non-alcoholic fatty liver disease (NAFLD). Liver Int 33:1398–1405CrossRefGoogle Scholar
  30. Wadaan MAM (2009) Effects of mercury exposure on blood chemistry and liver histopathology of male rats. J Pharmacol Toxicol 4:126–131CrossRefGoogle Scholar
  31. Wong EW, Cheng CY (2011) Impacts of environmental toxicants on male reproductive dysfunction. Trends Pharmacol Sci 32:290–299CrossRefGoogle Scholar
  32. Zhai H, Chen C, Wang N, Chen Y, Nie X, Han B, Li Q, Xia F, Lu Y (2017) Blood lead level is associated with non-alcoholic fatty liver disease in the Yangtze River Delta region of China in the context of rapid urbanization. Environ Health 16:93CrossRefGoogle Scholar
  33. Zhang Y, Xu C, Fu Z, Shu Y, Zhang J, Lu C, Mo X (2018) Associations between total mercury and methyl mercury exposure and cardiovascular risk factors in US adolescents. Environ Sci Pollut Res Int 25:6265–6272CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Runsen Chen
    • 1
  • Yang Xu
    • 1
  • Cheng Xu
    • 1
  • Yaqin Shu
    • 1
  • Siyu Ma
    • 1
  • Changgui Lu
    • 2
  • Xuming Mo
    • 1
    Email author
  1. 1.Department of Cardiothoracic SurgeryChildren’s Hospital of Nanjing Medical UniversityNanjingChina
  2. 2.Department of Pediatric SurgeryChildren’s Hospital of Nanjing Medical UniversityNanjingChina

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