Int J Thyroidol.  2020 May;13(1):19-29. 10.11106/ijt.2020.13.1.19.

Effect of Multiple Exposure to Perfluorinated Chemicals on Thyroid Function among Adults in the US: The National Health and Nutrition Examination Survey 2007-2008 and 2011-2012

Affiliations
  • 1Division of Endocrinology and Metabolism, Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea
  • 2Division of Endocrinology and Metabolism, Department of Internal Medicine, Hallym University College of Medicine, Chuncheon, Korea
  • 3Department of Internal Medicine, Seoul National University College of Medicine, Seoul, Korea

Abstract

Background and Objectives
Perfluoroalkyl substances (PFASs) are known to disrupt the thyroid hormone system. However, no study has assessed the association between multiple exposure to PFASs and the thyroid hormone system. This study aimed to identify the singular effects of each PFAS and the effects of multiple exposure to PFASs on the thyroid hormone profile in a representative sample of the US population.
Materials and Methods
We used data from the US National Health and Nutrition Examination Survey (NHANES) 2007-2008 and 2011-2012. To assess the effect of simultaneous exposure to multiple PFASs on thyroid function, principal component (PC) analysis with varimax rotation was performed. Multivariate linear regression analysis was conducted to identify the effect of each PFAS and PC on thyroid function.
Results
In this study, perfluorooctanoate (PFOA) was associated with a decrease in total T4 and Free T4 levels. Perfluorooctane sulfonate (PFOS) was associated with a decrease in total T4 level and perfluorononanoate (PFNA) and perfluorodecanoate (PFDeA) were associated with decreases in TSH levels. In PC analysis, two PCs were identified. PC1 included PFOA, PFOS, perfluorohexane sulfonate (PFHxS), PFNA and 2-(N-methyl-perfluorooctane sulfonamido) acetic acid with high loading. PC2 included PFNA, PFDeA, and perfluoroundecanoate (PFUA). In the multivariate linear regression analysis, PC1 showed negative correlations with total T4 and Free T4 levels, whereas PC2 showed a negative correlation with TSH level.
Conclusion
We found that singular and multiple exposure to PFASs was associated with a disruption in thyroid hormone system.

Keyword

Endocrine disruptors; Perfluorinated chemicals; Thyroid hormones

Figure

  • Fig. 1 Flowchart of participant selection.


Reference

1. Fromme H, Tittlemier SA, Volkel W, Wilhelm M, Twardella D. 2009; Perfluorinated compounds--exposure assessment for the general population in Western countries. Int J Hyg Environ Health. 212(3):239–70. DOI: 10.1016/j.ijheh.2008.04.007. PMID: 18565792.
2. Calafat AM, Wong LY, Kuklenyik Z, Reidy JA, Needham LL. 2007; Polyfluoroalkyl chemicals in the U.S. population: data from the National Health and Nutrition Examination Survey (NHANES) 2003-2004 and comparisons with NHANES 1999-2000. Environ Health Perspect. 115(11):1596–602. DOI: 10.1289/ehp.10598. PMID: 18007991. PMCID: PMC2072821.
Article
3. U.S. Environmental Protection Agency. 2005. Draft risk assessment of the potential human health effects associated with exposure to perflouroctanoic acids and its salts. Environmental Protection Agency;Washington, DC: U.S.:
4. Grandjean P, Clapp R. 2015; Perfluorinated alkyl substances: emerging insights into health risks. New Solut. 25(2):147–63. DOI: 10.1177/1048291115590506. PMID: 26084549. PMCID: PMC6172956.
5. Bach CC, Bech BH, Brix N, Nohr EA, Bonde JP, Henriksen TB. 2015; Perfluoroalkyl and polyfluoroalkyl substances and human fetal growth: a systematic review. Crit Rev Toxicol. 45(1):53–67. DOI: 10.3109/10408444.2014.952400. PMID: 25372700.
Article
6. Bach CC, Vested A, Jorgensen KT, Bonde JP, Henriksen TB, Toft G. 2016; Perfluoroalkyl and polyfluoroalkyl substances and measures of human fertility: a systematic review. Crit Rev Toxicol. 46(9):735–55. DOI: 10.1080/10408444.2016.1182117. PMID: 27268162.
Article
7. Agency for Toxic Substances and Disease Registry (ATSDR). 2009. Draft toxicological profile for perfluoroalkyls. Available from: URL: https://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=1117&tid=237. May 18, 2010.
8. Olsen GW, Burris JM, Ehresman DJ, Froehlich JW, Seacat AM, Butenhoff JL, et al. 2007; Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environ Health Perspect. 115(9):1298–305. DOI: 10.1289/ehp.10009. PMID: 17805419. PMCID: PMC1964923.
9. Bartell SM, Calafat AM, Lyu C, Kato K, Ryan PB, Steenland K. 2010; Rate of decline in serum PFOA concentrations after granular activated carbon filtration at two public water systems in Ohio and West Virginia. Environ Health Perspect. 118(2):222–8. DOI: 10.1289/ehp.0901252. PMID: 20123620. PMCID: PMC2831921.
Article
10. Li L, Zhai Z, Liu J, Hu J. 2015; Estimating industrial and domestic environmental releases of perfluorooctanoic acid and its salts in China from 2004 to 2012. Chemosphere. 129:100–9. DOI: 10.1016/j.chemosphere.2014.11.049. PMID: 25541533.
Article
11. Glynn A, Berger U, Bignert A, Ullah S, Aune M, Lignell S, et al. 2012; Perfluorinated alkyl acids in blood serum from primiparous women in Sweden: serial sampling during pregnancy and nursing, and temporal trends 1996-2010. Environ Sci Technol. 46(16):9071–9. DOI: 10.1021/es301168c. PMID: 22770559.
Article
12. Stubleski J, Salihovic S, Lind L, Lind PM, van Bavel B, Karrman A. 2016; Changes in serum levels of perfluoroalkyl substances during a 10-year follow-up period in a large population-based cohort. Environ Int. 95:86–92. DOI: 10.1016/j.envint.2016.08.002. PMID: 27542758.
Article
13. Okada E, Kashino I, Matsuura H, Sasaki S, Miyashita C, Yamamoto J, et al. 2013; Temporal trends of perfluoroalkyl acids in plasma samples of pregnant women in Hokkaido, Japan, 2003-2011. Environ Int. 60:89–96. DOI: 10.1016/j.envint.2013.07.013. PMID: 24013022.
Article
14. Gore AC, Chappell VA, Fenton SE, Flaws JA, Nadal A, Prins GS, et al. 2015; EDC-2: The Endocrine Society's second Scientific Statement on endocrine-disrupting chemicals. Endocr Rev. 36(6):E1–150. DOI: 10.1210/er.2015-1010. PMID: 26544531. PMCID: PMC4702494.
Article
15. Butenhoff JL, Chang SC, Ehresman DJ, York RG. 2009; Evaluation of potential reproductive and developmental toxicity of potassium perfluorohexanesulfonate in Sprague Dawley rats. Reprod Toxicol. 27(3-4):331–41. DOI: 10.1016/j.reprotox.2009.01.004. PMID: 19429404.
Article
16. Martin MT, Brennan RJ, Hu W, Ayanoglu E, Lau C, Ren H, et al. 2007; Toxicogenomic study of triazole fungicides and perfluoroalkyl acids in rat livers predicts toxicity and categorizes chemicals based on mechanisms of toxicity. Toxicol Sci. 97(2):595–613. DOI: 10.1093/toxsci/kfm065. PMID: 17383973.
Article
17. Yu WG, Liu W, Jin YH. 2009; Effects of perfluorooctane sulfonate on rat thyroid hormone biosynthesis and metabolism. Environ Toxicol Chem. 28(5):990–6. DOI: 10.1897/08-345.1. PMID: 19045937.
Article
18. Kim MJ, Moon S, Oh BC, Jung D, Ji K, Choi K, et al. 2018; Association between perfluoroalkyl substances exposure and thyroid function in adults: A meta-analysis. PLoS One. 13(5):e0197244. DOI: 10.1371/journal.pone.0197244. PMID: 29746532. PMCID: PMC5945046.
Article
19. Kim S, Kim S, Won S, Choi K. 2017; Considering common sources of exposure in association studies - Urinary benzophenone-3 and DEHP metabolites are associated with altered thyroid hormone balance in the NHANES 2007-2008. Environ Int. 107:25–32. DOI: 10.1016/j.envint.2017.06.013. PMID: 28651165.
Article
20. 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):6085–91. DOI: 10.1021/ac050671l. PMID: 16159145.
Article
21. Centers for Disease Control and Prevention. National Health and Nutrition Examination Survey 2007-2008, Data Documentation: Polyfluoroalkyl Chemicals. Available from: URL:https://wwwn.cdc.gov/Nchs/Nhanes/2007-2008/PFC_E.htm#Analytic_Notes. May 18, 2010.
22. Jain RB. 2018; Time trends over 2003-2014 in the concentrations of selected perfluoroalkyl substances among US adults aged >/=20years: Interpretational issues. Sci Total Environ. 645:946–57. DOI: 10.1016/j.scitotenv.2018.07.198. PMID: 30248883.
23. Houde M, Martin JW, Letcher RJ, Solomon KR, Muir DC. 2006; Biological monitoring of polyfluoroalkyl substances: A review. Environ Sci Technol. 40(11):3463–73. DOI: 10.1021/es052580b. PMID: 16786681.
Article
24. Seacat AM, Thomford PJ, Hansen KJ, Olsen GW, Case MT, Butenhoff JL. 2002; Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in cynomolgus monkeys. Toxicol Sci. 68(1):249–64. DOI: 10.1093/toxsci/68.1.249. PMID: 12075127.
Article
25. Butenhoff J, Costa G, Elcombe C, Farrar D, Hansen K, Iwai H, et al. 2002; Toxicity of ammonium perfluorooctanoate in male cynomolgus monkeys after oral dosing for 6 months. Toxicol Sci. 69(1):244–57. DOI: 10.1093/toxsci/69.1.244. PMID: 12215680.
Article
26. 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(2):206–16. DOI: 10.1093/toxsci/kfp055. PMID: 19293372.
Article
27. Chang SC, Thibodeaux JR, Eastvold ML, Ehresman DJ, Bjork JA, Froehlich JW, et al. 2008; Thyroid hormone status and pituitary function in adult rats given oral doses of perfluorooctanesulfonate (PFOS). Toxicology. 243(3):330–9. DOI: 10.1016/j.tox.2007.10.014. PMID: 18063289.
Article
28. Lewis DF, Ioannides C, Parke DV. 1998; Cytochromes P450 and species differences in xenobiotic metabolism and activation of carcinogen. Environ Health Perspect. 106(10):633–41. DOI: 10.1289/ehp.98106633. PMID: 9755138. PMCID: PMC1533178.
Article
29. Steenland K, Fletcher T, Savitz DA. 2010; Epidemiologic evidence on the health effects of perfluorooctanoic acid (PFOA). Environ Health Perspect. 118(8):1100–8. DOI: 10.1289/ehp.0901827. PMID: 20423814. PMCID: PMC2920088.
Article
30. Bloom MS, Kannan K, Spliethoff HM, Tao L, Aldous KM, Vena JE. 2010; Exploratory assessment of perfluorinated compounds and human thyroid function. Physiol Behav. 99(2):240–5. DOI: 10.1016/j.physbeh.2009.02.005. PMID: 19419669.
Article
31. Ji K, Kim S, Kho Y, Paek D, Sakong J, Ha J, et al. 2012; Serum concentrations of major perfluorinated compounds among the general population in Korea: dietary sources and potential impact on thyroid hormones. Environ Int. 45:78–85. DOI: 10.1016/j.envint.2012.03.007. PMID: 22580293.
Article
32. Wang Y, Rogan WJ, Chen PC, Lien GW, Chen HY, Tseng YC, et al. 2014; Association between maternal serum perfluoroalkyl substances during pregnancy and maternal and cord thyroid hormones: Taiwan maternal and infant cohort study. Environ Health Perspect. 122(5):529–34. DOI: 10.1289/ehp.1306925. PMID: 24577800. PMCID: PMC4014761.
Article
33. Gutshall DM, Pilcher GD, Langley AE. 1989; Mechanism of the serum thyroid hormone lowering effect of perfluoro-n-decanoic acid (PFDA) in rats. J Toxicol Environ Health. 28(1):53–65. DOI: 10.1080/15287398909531328. PMID: 2506363.
Article
34. Van Rafelghem MJ, Inhorn SL, Peterson RE. 1987; Effects of perfluorodecanoic acid on thyroid status in rats. Toxicol Appl Pharmacol. 87(3):430–9. DOI: 10.1016/0041-008X(87)90248-1. PMID: 3564018.
Article
35. Liu Y, Wang J, Fang X, Zhang H, Dai J. 2011; The thyroid-disrupting effects of long-term perfluorononanoate exposure on zebrafish (Danio rerio). Ecotoxicology. 20(1):47–55. DOI: 10.1007/s10646-010-0555-3. PMID: 20941541.
Article
36. Czarnota J, Gennings C, Colt JS, De Roos AJ, Cerhan JR, Severson RK, et al. 2015; Analysis of environmental chemical mixtures and non-hodgkin lymphoma risk in the NCI-SEER NHL study. Environ Health Perspect. 123(10):965–70. DOI: 10.1289/ehp.1408630. PMID: 25748701. PMCID: PMC4590749.
Article
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