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Co-exposure to environmental endocrine disruptors in the US population

  • Lin Chen
  • Kai Luo
  • Ruth Etzel
  • Xiaoyu Zhang
  • Ying Tian
  • Jun ZhangEmail author
Research Article
  • 56 Downloads

Abstract

Exposure to environmental endocrine disruptors (EEDs) has been linked to adverse health outcomes. The vast majority of studies examined one class of EEDs at a time but humans often are exposed to multiple EEDs at the same time. It is, therefore, important to know the co-exposure status of multiple EEDs in an individual, to preclude and control for potential confounding effects posed by co-exposed EEDs. This study examined the concentrations of seven classes of EEDs in the US population utilizing the data from the National Health and Nutrition Examination Survey (NHANES), 2009–2014 survey cycles. We applied linear correlation and cluster analysis to characterize the correlation profile and cluster patterns of these EEDs. We found that EEDs with a similar structure are often highly correlated. Among between-class correlations, mercury and perfluoroalkyl substances (PFAS) and cadmium and polycyclic aromatic hydrocarbons (PAHs) were two significantly correlated EEDs. In epidemiologic studies, measurement and control for co-exposure to pollutants, especially those with similar biological effects, are critical when attempting to make causal inferences. Appropriate statistical methods to handle within- and between-class correlations are needed.

Keywords

Environmental endocrine disruptors NHANES Cluster analysis Correlation Co-exposure PFAS Mercury PAHs Cadmium 

Notes

Funding

This study was partly funded by the National Basic Science Research Program Ministry of Science and Technology of China (Grant No. 2014CB943300), the National Natural Science Foundation of China (81530086) and the clinical research capacity improvement programs of postgraduate from Shanghai Jiao Tong University School of Medicine.

Compliance with ethical standards

Competing interests

The authors declare that they have no conflicts of interest.

Supplementary material

11356_2018_4105_MOESM1_ESM.docx (48 kb)
ESM 1 (DOCX 48 kb)

References

  1. Annamalai J, Namasivayam V (2015) Endocrine disrupting chemicals in the atmosphere: their effects on humans and wildlife. Environ Int 76:78–97CrossRefGoogle Scholar
  2. Bobb FJ, Valeri L, Claus BH, Christiani CD, Wright OR, Mazumdar M, Godleski JJ, Coull AB (2015) Bayesian kernel machine regression for estimating the health effects of multi-pollutant mixtures. Biostatistics 16:493–508CrossRefGoogle Scholar
  3. Brendel S, Fetter E, Staude C, Vierke L, Biegel-Engler A (2018) Short-chain perfluoroalkyl acids: environmental concerns and a regulatory strategy under REACH. Environ Sci Eur 30:9CrossRefGoogle Scholar
  4. Buha A, Matovic V, Antonijevic B et al (2018) Overview of cadmium thyroid disrupting effects and mechanisms. Int J Mol Sci 19(5):1501Google Scholar
  5. Casals-Casas C, Desvergne B (2011) Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol 73:135–162CrossRefGoogle Scholar
  6. Cha E, Jeong ES, Han SB, Cha S, Son J, Kim S, Oh HB, Lee J (2018) Ionization of gas-phase polycyclic aromatic hydrocarbons in electrospray ionization coupled with gas chromatography. Anal Chem 90:4203–4211CrossRefGoogle Scholar
  7. Chadeau-Hyam M, Campanella G, Jombart T, Bottolo L, Portengen L, Vineis P, Liquet B, Vermeulen RC (2013) Deciphering the complex: methodological overview of statistical models to derive OMICS-based biomarkers. Environ Mol Mutagen 54:542–557CrossRefGoogle Scholar
  8. Chen A, Kim SS, Chung E, Dietrich KN (2013) Thyroid hormones in relation to lead, mercury, and cadmium exposure in the National Health and nutrition examination survey, 2007-2008. Environ Health Perspect 121:181–186CrossRefGoogle Scholar
  9. Clark JD 3rd, Serdar B, Lee DJ, Arheart K, Wilkinson JD, Fleming LE (2012) Exposure to polycyclic aromatic hydrocarbons and serum inflammatory markers of cardiovascular disease. Environ Res 117:132–137CrossRefGoogle Scholar
  10. Darrow LA, Stein CR, Steenland K (2013) Serum perfluorooctanoic acid and perfluorooctane sulfonate concentrations in relation to birth outcomes in the mid-Ohio Valley, 2005-2010. Environ Health Perspect 121:1207–1213CrossRefGoogle Scholar
  11. Dassuncao C, Hu XC, Nielsen F, Weihe P, Grandjean P, Sunderland EM (2018) Shifting global exposures to poly- and Perfluoroalkyl substances (PFASs) evident in longitudinal birth cohorts from a seafood-consuming population. Environ Sci Technol 52:3738–3747CrossRefGoogle Scholar
  12. Davalos AD, Luben TJ, Herring AH, Sacks JD (2017) Current approaches used in epidemiologic studies to examine short-term multipollutant air pollution exposures. Annals of epidemiology. 27 e141:145–153Google Scholar
  13. Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967–4983CrossRefGoogle Scholar
  14. Grandjean P, Andersen EW, Budtz-Jørgensen E, Nielsen F, Mølbak K, Weihe P, Heilmann C (2012) Serum vaccine antibody concentrations in children exposed to perfluorinated compounds. JAMA 307(4):391–397.  https://doi.org/10.1001/jama.2011.2034. Erratum in: JAMA. 2012;307(11):1142.CrossRefGoogle Scholar
  15. Grandjean P, Heilmann C, Weihe P, Nielsen F, Mogensen UB, Budtz-Jørgensen E (2017a) Serum vaccine antibody concentrations in adolescents exposed to perfluorinated compounds. Environ Health Perspect 125(7):077018.  https://doi.org/10.1289/EHP275 CrossRefGoogle Scholar
  16. Grandjean P, Heilmann C, Weihe P, Nielsen F, Mogensen UB, Timmermann A, Budtz-Jørgensen E (2017b) Estimated exposures to perfluorinated compounds in infancy predict attenuated vaccine antibody concentrations at age 5-years. J Immunotoxicol 14(1):188–195CrossRefGoogle Scholar
  17. Hamra GB, Buckley JP (2018) Environmental exposure mixtures: questions and methods to address them. Curr Epidemiol Rep 5:1–6CrossRefGoogle Scholar
  18. Hastings J, Magka D, Batchelor C et al (2012) Structure-based classification and ontology in chemistry. J Cheminform 4:8CrossRefGoogle Scholar
  19. He P, Lu Y, Liang Y, Chen B, Wu M, Li S, He G, Jin T (2013) Exposure assessment of dietary cadmium: findings from Shanghainese over 40 years, China. BMC Public Health 13:590CrossRefGoogle Scholar
  20. Jin L, Liu M, Zhang L, Li Z, Yu J, Liu J, Ye R, Chen L, Ren A (2016) Exposure of methyl mercury in utero and the risk of neural tube defects in a Chinese population. Reprod Toxicol 61:131–135CrossRefGoogle Scholar
  21. Kabir ER, Rahman MS, Rahman I (2015) A review on endocrine disruptors and their possible impacts on human health. Environ Toxicol Pharmacol 40:241–258CrossRefGoogle Scholar
  22. Kataria A, Trasande L, Trachtman H (2015) The effects of environmental chemicals on renal function. Nat Rev Nephrol 11:610–625CrossRefGoogle Scholar
  23. Kennedy GL Jr, Butenhoff JL, Olsen GW, O'Connor JC, Seacat AM, Perkins RG, Biegel LB, Murphy SR, Farrar DG (2004) The toxicology of perfluorooctanoate. Crit Rev Toxicol 34:351–384CrossRefGoogle Scholar
  24. Korashy HM, El-Kadi AO (2006) The role of aryl hydrocarbon receptor in the pathogenesis of cardiovascular diseases. Drug Metab Rev 38:411–450CrossRefGoogle Scholar
  25. Kuklenyik Z, Needham LL, Calafat AM (2005) Measurement of 18 perfluorinated organic acids and amides in human serum using on-line solid-phase extraction. Anal Chem 77(18):6085–6091CrossRefGoogle Scholar
  26. Lin Y, Qiu X, Yu N, Yang Q, Araujo JA, Zhu Y (2016) Urinary metabolites of polycyclic aromatic hydrocarbons and the association with lipid peroxidation: a biomarker-based study between Los Angeles and Beijing. Environ Sci Technol 50:3738–3745CrossRefGoogle Scholar
  27. Liu Y, Buchanan S, Anderson HA, Xiao Z, Persky V, Turyk ME (2018) Association of methylmercury intake from seafood consumption and blood mercury level among the Asian and non-Asian populations in the United States. Environ Res 160:212–222CrossRefGoogle Scholar
  28. Long M, Knudsen AK, Pedersen HS, Bonefeld-Jorgensen EC (2015) Food intake and serum persistent organic pollutants in the Greenlandic pregnant women: the ACCEPT sub-study. Sci Total Environ 529:198–212CrossRefGoogle Scholar
  29. Murtagh F, Contreras P (2012) Algorithms for hierarchical clustering: an overview. Wiley Interdisciplinary Reviews Data Mining & Knowledge Discovery 2:86–97CrossRefGoogle Scholar
  30. National Center for Health Statistics (2014) National Health and nutrition examination survey:sample design, 2011-2014. DHHS publication no 2014–1362. National Center for Health Statistics, Hyattsville MDGoogle Scholar
  31. Nishida M, Yamamoto T, Yoshimura Y, Kawada J (1986) Subacute toxicity of methylmercuric chloride and mercuric chloride on mouse thyroid. J Pharmacobio-dyn 9:331–338CrossRefGoogle Scholar
  32. Patrick L (2003) Toxic metals and antioxidants: part II. The role of antioxidants in arsenic and cadmium toxicity. Altern Med Rev 8:106–128Google Scholar
  33. Peng S, Liu L, Zhang X, Heinrich J, Zhang J, Schramm KW, Huang Q, Tian M, Eqani SA, Shen H (2015) A nested case-control study indicating heavy metal residues in meconium associate with maternal gestational diabetes mellitus risk. Environ Health 14(19):19CrossRefGoogle Scholar
  34. Petrakis D, Vassilopoulou L, Mamoulakis C, Psycharakis C, Anifantaki A, Sifakis S, Docea AO, Tsiaoussis J, Makrigiannakis A, Tsatsakis AM (2017) Endocrine disruptors leading to obesity and related diseases. Int J Environ Res Public Health 14(10).  https://doi.org/10.3390/ijerph14101282
  35. Prevedouros K, Cousins Ian T, Buck Robert C et al (2006) Sources, fate and transport of perfluorocarboxylates.[J]. Environ Sci Technol 40:32–44CrossRefGoogle Scholar
  36. Savitz DA, Stein CR, Bartell SM, Elston B, Gong J, Shin HM, Wellenius GA (2012) Perfluorooctanoic acid exposure and pregnancy outcome in a highly exposed community. Epidemiology 23:386–392CrossRefGoogle Scholar
  37. Soldin OP, O'Mara DM, Aschner M (2008) Thyroid hormones and methylmercury toxicity. Biol Trace Elem Res 126:1–12CrossRefGoogle Scholar
  38. Stafoggia M, Breitner S, Hampel R, Basagaña X (2017) Statistical approaches to address multi-pollutant mixtures and multiple exposures: the state of the science. Curr Environ Health Rep 4:481–490CrossRefGoogle Scholar
  39. Stein CR, Savitz DA, Dougan M (2009) Serum levels of perfluorooctanoic acid and perfluorooctane sulfonate and pregnancy outcome. Am J Epidemiol 170:837–846CrossRefGoogle Scholar
  40. Sun Z, Tao Y, Li S, Ferguson KK, Meeker JD, Park SK, Batterman SA, Mukherjee B (2013) Statistical strategies for constructing health risk models with multiple pollutants and their interactions: possible choices and comparisons. Environ Health 12:85CrossRefGoogle Scholar
  41. Tellez-Plaza M, Jones MR, Dominguez-Lucas A, Guallar E, Navas-Acien A (2013) Cadmium exposure and clinical cardiovascular disease: a systematic review. Curr Atheroscler Rep 15:356CrossRefGoogle Scholar
  42. Tibshirani R (2011) Regression shrinkage and selection via the lasso: a retrospective. J R Stat Soc 73:273–282CrossRefGoogle Scholar
  43. Tsochatzis ED, Tzimou-Tsitouridou R, Gika HG (2017) Analytical methodologies for the assessment of phthalate exposure in humans. Crit Rev Anal Chem 47:279–297CrossRefGoogle Scholar
  44. Vigeh M, Nishioka E, Ohtani K, Omori Y, Matsukawa T, Koda S, Yokoyama K (2018) Prenatal mercury exposure and birth weight. Reprod Toxicol 76:78–83CrossRefGoogle Scholar
  45. Weiss JM, Andersson PL, Lamoree MH, Leonards PE, van Leeuwen SP, Hamers T (2009) Competitive binding of poly- and perfluorinated compounds to the thyroid hormone transport protein transthyretin. Toxicol Sci 109:206–216CrossRefGoogle Scholar
  46. Weisskopf MG, Seals RM, Webster TF (2018) Bias amplification in epidemiologic analysis of exposure to mixtures. Environ Health Perspect 126:047003CrossRefGoogle Scholar
  47. Wells EM, Herbstman JB, Lin YH, Hibbeln JR, Halden RU, Witter FR, Goldman LR (2017) Methyl mercury, but not inorganic mercury, associated with higher blood pressure during pregnancy. Environ Res 154:247–252CrossRefGoogle Scholar
  48. Yu WG, Liu W, Jin YH (2009) Effects of perfluorooctane sulfonate on rat thyroid hormone biosynthesis and metabolism. Environ Toxicol Chem 28:990–996CrossRefGoogle Scholar
  49. Zou H, Hastie T (2010) Regularization and variable selection via the elastic net. J R Stat Soc 67:768–768CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Ministry of Education-Shanghai Key Laboratory of Children’s Environmental Health, Xinhua HospitalShanghai Jiao Tong University School of MedicineShanghaiChina
  2. 2.School of Public HealthShanghai Jiao Tong UniversityShanghaiChina
  3. 3.Milkin Institute School of Public HealthThe George Washington UniversityWashingtonUSA

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