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Association of perfluorinated chemical exposure in utero with maternal and infant thyroid hormone levels in the Sapporo cohort of Hokkaido Study on the Environment and Children’s Health

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Environmental Health and Preventive Medicine Aims and scope

Abstract

Objectives

Perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) have been widely used as industrial products, and are persistent organic pollutants due to their chemical stability. Previous studies suggested that PFOS and PFOA might disrupt thyroid hormone (TH) status. Although TH plays an important role in fetal growth during pregnancy, little attention has been paid to the relationships between maternal exposure to perfluorocarbons and TH statuses of mothers and fetuses. We investigated the effects of low levels of environmental PFOS and PFOA on thyroid function of mothers and infants.

Methods

Of the eligible subjects in a prospective cohort, 392 mother–infant pairs were selected. Concentration of maternal serum PFOS and PFOA was measured in samples taken during the second and third trimesters or within 1 week of delivery. Blood samples for measuring thyroid stimulating hormone (TSH) and free thyroxine (FT4) levels were obtained from mothers at early gestational stage (median 11.1 weeks), and from infants between 4 and 7 days of age, respectively.

Results

Median concentrations of PFOS and PFOA were 5.2 [95 % confidence interval (CI) 1.6–12.3] and 1.2 (95 % CI limitation of detection–3.4) ng/mL, respectively. Maternal PFOS levels were inversely correlated with maternal serum TSH and positively associated with infant serum TSH, whereas maternal PFOA showed no significant relationship with TSH or FT4 among mothers and infants.

Conclusions

These findings suggest that PFOS may independently affect the secretion and balances of maternal and infant TSH even at low levels of environmental exposure.

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References

  1. Fromme H, Tittlemier SA, Volkel W, Wilhelm M, Twardella D. Perfluorinated compounds—exposure assessment for the general population in Western countries. Int J Hyg Environ Health. 2009;212(3):239–70.

    Article  CAS  PubMed  Google Scholar 

  2. Butenhoff JL, Olsen GW, Pfahles-Hutchens A. The applicability of biomonitoring data for perfluorooctanesulfonate to the environmental public health continuum. Environ Health Perspect. 2006;114(11):1776–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Tully JS, Needham LL. Serum concentrations of 11 polyfluoroalkyl compounds in the US population: data from the national health and nutrition examination survey (NHANES). Environ Sci Technol. 2007;41(7):2237–42.

    Article  CAS  PubMed  Google Scholar 

  4. Harada K, Saito N, Inoue K, Yoshinaga T, Watanabe T, Sasaki S, Kamiyama S, Koizumi A. The influence of time, sex and geographic factors on levels of perfluorooctane sulfonate and perfluorooctanoate in human serum over the last 25 years. J Occup Health. 2004;46(2):141–7.

    Article  CAS  PubMed  Google Scholar 

  5. Kannan K, Corsolini S, Falandysz J, Fillmann G, Kumar KS, Loganathan BG, Mohd MA, Olivero J, Van Wouwe N, Yang JH, et al. Perfluorooctanesulfonate and related fluorochemicals in human blood from several countries. Environ Sci Technol. 2004;38(17):4489–95.

    Article  CAS  PubMed  Google Scholar 

  6. Olsen GW, Burris JM, Ehresman DJ, Froehlich JW, Seacat AM, Butenhoff JL, Zobel LR. Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environ Health Perspect. 2007;115(9):1298–305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Inoue K, Okada F, Ito R, Kato S, Sasaki S, Nakajima S, Uno A, Saijo Y, Sata F, Yoshimura Y, et al. Perfluorooctane sulfonate (PFOS) and related perfluorinated compounds in human maternal and cord blood samples: assessment of PFOS exposure in a susceptible population during pregnancy. Environ Health Perspect. 2004;112(11):1204–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Midasch O, Drexler H, Hart N, Beckmann MW, Angerer J. Transplacental exposure of neonates to perfluorooctanesulfonate and perfluorooctanoate: a pilot study. Int Arch Occup Environ Health. 2007;80(7):643–8.

    Article  CAS  PubMed  Google Scholar 

  9. Apelberg BJ, Witter FR, Herbstman JB, Calafat AM, Halden RU, Needham LL, Goldman LR. Cord serum concentrations of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) in relation to weight and size at birth. Environ Health Perspect. 2007;115(11):1670–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chen MH, Ha EH, Liao HF, Jeng SF, Su YN, Wen TW, Lien GW, Chen CY, Hsieh WS, Chen PC. Perfluorinated compound levels in cord blood and neurodevelopment at 2 years of age. Epidemiology (Cambridge, Mass). 2013;24(6):800–8.

    Article  Google Scholar 

  11. Washino N, Saijo Y, Sasaki S, Kato S, Ban S, Konishi K, Ito R, Nakata A, Iwasaki Y, Saito K, et al. Correlations between prenatal exposure to perfluorinated chemicals and reduced fetal growth. Environ Health Perspect. 2009;117(4):660–7.

    Article  CAS  PubMed  Google Scholar 

  12. Kishi R, Nakajima T, Goudarzi H, Kobayashi S, Sasaki S, Okada E, Miyashita C, Itoh S, Araki A, Ikeno T, et al. The association of prenatal exposure to perfluorinated chemicals with maternal essential and long-chain polyunsaturated fatty acids during pregnancy and the birth weight of their offspring: the Hokkaido Study. Environ Health Perspect. 2015;123:1038–45.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Luebker DJ, York RG, Hansen KJ, Moore JA, Butenhoff JL. Neonatal mortality from in utero exposure to perfluorooctanesulfonate (PFOS) in Sprague-Dawley rats: dose–response, and biochemical and pharmacokinetic parameters. Toxicology. 2005;215(1–2):149–69.

    Article  CAS  PubMed  Google Scholar 

  14. Lau C, Thibodeaux JR, Hanson RG, Rogers JM, Grey BE, Stanton ME, Butenhoff JL, Stevenson LA. Exposure to perfluorooctane sulfonate during pregnancy in rat and mouse. II: postnatal evaluation. Toxicol Sci. 2003;74(2):382–92.

    Article  CAS  PubMed  Google Scholar 

  15. Webster GM, Venners SA, Mattman A, Martin JW. Associations between perfluoroalkyl acids (PFASs) and maternal thyroid hormones in early pregnancy: a population-based cohort study. Environ Res. 2014;133:338–47.

    Article  CAS  PubMed  Google Scholar 

  16. Berg V, Nost TH, Hansen S, Elverland A, Veyhe AS, Jorde R, Odland JO, Sandanger TM. Assessing the relationship between perfluoroalkyl substances, thyroid hormones and binding proteins in pregnant women; a longitudinal mixed effects approach. Environ Int. 2015;77:63–9.

    Article  CAS  PubMed  Google Scholar 

  17. Wang Y, Rogan WJ, Chen PC, Lien GW, Chen HY, Tseng YC, Longnecker MP, Wang SL. Association between maternal serum perfluoroalkyl substances during pregnancy and maternal and cord thyroid hormones: Taiwan maternal and infant cohort study. Environ Health Perspect. 2014;122(5):529–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Kim S, Choi K, Ji K, Seo J, Kho Y, Park J, Kim S, Park S, Hwang I, Jeon J, et al. Trans-placental transfer of thirteen perfluorinated compounds and relations with fetal thyroid hormones. Environ Sci Technol. 2011;45(17):7465–72.

    Article  CAS  PubMed  Google Scholar 

  19. de Cock M, de Boer MR, Lamoree M, Legler J, van de Bor M. Prenatal exposure to endocrine disrupting chemicals in relation to thyroid hormone levels in infants—a Dutch prospective cohort study. Environ Health. 2014;13:106.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kishi R, Kobayashi S, Ikeno T, Araki A, Miyashita C, Itoh S, Sasaki S, Okada E, Kobayashi S, Kashino I, et al. Ten years of progress in the Hokkaido birth cohort study on environment and children’s health: cohort profile—updated 2013. Environ Health Prev Med. 2013;18(6):429–50.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Okada E, Sasaki S, Saijo Y, Washino N, Miyashita C, Kobayashi S, Konishi K, Ito YM, Ito R, Nakata A, et al. Prenatal exposure to perfluorinated chemicals and relationship with allergies and infectious diseases in infants. Environ Res. 2012;112:118–25.

    Article  CAS  PubMed  Google Scholar 

  22. Williams FL, Mires GJ, Barnett C, Ogston SA, van Toor H, Visser TJ, Hume R. Transient hypothyroxinemia in preterm infants: the role of cord sera thyroid hormone levels adjusted for prenatal and intrapartum factors. J Clin Endocrinol Metab. 2005;90(8):4599–606.

    Article  CAS  PubMed  Google Scholar 

  23. Mortimer RH. Thyroid function tests. Aust Prescr. 2011;34(1):12–5.

    Article  Google Scholar 

  24. Harada KH, Yang HR, Moon CS, Hung NN, Hitomi T, Inoue K, Niisoe T, Watanabe T, Kamiyama S, Takenaka K, et al. Levels of perfluorooctane sulfonate and perfluorooctanoic acid in female serum samples from Japan in 2008, Korea in 1994–2008 and Vietnam in 2007–2008. Chemosphere. 2010;79(3):314–9.

    Article  CAS  PubMed  Google Scholar 

  25. Papadopoulou E, Haug LS, Sabaredzovic A, Eggesbo M, Longnecker MP. Reliability of perfluoroalkyl substances in plasma of 100 women in two consecutive pregnancies. Environ Res. 2015;140:421–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Jain RB. Effect of pregnancy on the levels of selected perfluoroalkyl compounds for females aged 17–39 years: data from National Health and Nutrition Examination Survey 2003–2008. J Toxicol Environ Health Part A. 2013;76(7):409–21.

    Article  CAS  PubMed  Google Scholar 

  27. Javins B, Hobbs G, Ducatman AM, Pilkerton C, Tacker D, Knox SS. Circulating maternal perfluoroalkyl substances during pregnancy in the C8 Health Study. Environ Sci Technol. 2013;47(3):1606–13.

    CAS  PubMed  Google Scholar 

  28. de Escobar GM, Obregon MJ, del Rey FE. Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract Res Clin Endocrinol Metab. 2004;18(2):225–48.

    Article  PubMed  Google Scholar 

  29. Obregon MJ, Calvo RM, Del Rey FE, de Escobar GM. Ontogenesis of thyroid function and interactions with maternal function. Endocr Dev. 2007;10:86–98.

    CAS  PubMed  Google Scholar 

  30. Ben-Rafael Z, Struass JF 3rd, Arendash-Durand B, Mastroianni L Jr, Flickinger GL. Changes in thyroid function tests and sex hormone binding globulin associated with treatment by gonadotropin. Fertil Steril. 1987;48(2):318–20.

    Article  CAS  PubMed  Google Scholar 

  31. Kuppens SM, Kooistra L, Wijnen HA, Vader HL, Hasaart TH, Oei SG, Vulsma T, Pop VJ. Neonatal thyroid screening results are related to gestational maternal thyroid function. Clin Endocrinol. 2011;75(3):382–7.

    Article  CAS  Google Scholar 

  32. Lau C, Anitole K, Hodes C, Lai D, Pfahles-Hutchens A, Seed J. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol Sci. 2007;99(2):366–94.

    Article  CAS  PubMed  Google Scholar 

  33. Zhang T, Sun H, Qin X, Gan Z, Kannan K. PFOS and PFOA in paired urine and blood from general adults and pregnant women: assessment of urinary elimination. Environ Sci Pollut Res Int. 2015;22(7):5572–9.

    Article  CAS  PubMed  Google Scholar 

  34. Olsen GW, Zobel LR. Assessment of lipid, hepatic, and thyroid parameters with serum perfluorooctanoate (PFOA) concentrations in fluorochemical production workers. Int Arch Occup Environ Health. 2007;81(2):231–46.

    Article  CAS  PubMed  Google Scholar 

  35. Fei C, McLaughlin JK, Tarone RE, Olsen J. Perfluorinated chemicals and fetal growth: a study within the Danish National Birth Cohort. Environ Health Perspect. 2007;115(11):1677–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Johnson JD, Gibson SJ, Ober RF. Absorption of FC-95-14C in rats after a single oral dose. St Paul: Riker Laboratories, Inc; 1979 (US EPA Docket No 8(e)HQ-1180–00374).

    Google Scholar 

  37. Seacat AM, Thomford PJ, Hansen KJ, Olsen GW, Case MT, Butenhoff JL. Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in cynomolgus monkeys. Toxicol Sci. 2002;68(1):249–64.

    Article  CAS  PubMed  Google Scholar 

  38. Weiss JM, Andersson PL, Lamoree MH, Leonards PE, van Leeuwen SP, Hamers T. Competitive binding of poly- and perfluorinated compounds to the thyroid hormone transport protein transthyretin. Toxicol Sci. 2009;109(2):206–16.

    Article  CAS  PubMed  Google Scholar 

  39. Haddow JE, McClain MR, Lambert-Messerlian G, Palomaki GE, Canick JA, Cleary-Goldman J, Malone FD, Porter TF, Nyberg DA, Bernstein P, et al. Variability in thyroid-stimulating hormone suppression by human chorionic [corrected] gonadotropin during early pregnancy. J Clin Endocrinol Metab. 2008;93(9):3341–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Glinoer D, de Nayer P, Bourdoux P, Lemone M, Robyn C, van Steirteghem A, Kinthaert J, Lejeune B. Regulation of maternal thyroid during pregnancy. J Clin Endocrinol Metab. 1990;71(2):276–87.

    Article  CAS  PubMed  Google Scholar 

  41. Okada E, Kashino I, Matsuura H, Sasaki S, Miyashita C, Yamamoto J, Ikeno T, Ito YM, Matsumura T, Tamakoshi A, et al. Temporal trends of perfluoroalkyl acids in plasma samples of pregnant women in Hokkaido, Japan, 2003–2011. Environ Int. 2013;60:89–96.

    Article  CAS  PubMed  Google Scholar 

  42. Miyashita C, Sasaki S, Saijo Y, Okada E, Kobayashi S, Baba T, Kajiwara J, Todaka T, Iwasaki Y, Nakazawa H, et al. Demographic, behavioral, dietary, and socioeconomic characteristics related to persistent organic pollutants and mercury levels in pregnant women in Japan. Chemosphere. 2015;133:13–21.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the staff at Sapporo Toho Hospital and the participating mothers and infants for their collaboration. We also thank N. Koibuchi for instruction on thyroid homeostasis function, and R. Ito for the measurement of PFOS and PFOA. This study was supported by Grants-in-Aid for Health Scientific Research from the Japanese Ministry of Health, Labour and Welfare (20805801); and by Grants-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (13307015).

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Authors and Affiliations

  1. Department of Public Health, Hokkaido University Graduate School of Medicine, Sapporo, Japan

    Shizue Kato, Toshiaki Baba, Seiko Sasaki, Akiko Uno & Emiko Okada

  2. Center for Environmental and Health Sciences, Hokkaido University, Sapporo, Japan

    Sachiko Itoh, Chihiro Miyashita & Reiko Kishi

  3. Department of Public Health, School of Medicine, Juntendo University, Tokyo, Japan

    Motoyuki Yuasa

  4. Department of Occupational Therapy, School of Health Sciences, Sapporo Medical University, Sapporo, Japan

    Sonomi Nakajima

  5. Department of Analytical Chemistry, School of Pharmacy and Pharmaceutical Sciences, Hoshi University, Tokyo, Japan

    Hiroyuki Nakazawa & Yusuke Iwasaki

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  1. Shizue Kato
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  2. Sachiko Itoh
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  3. Motoyuki Yuasa
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Correspondence to Reiko Kishi.

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The authors declare that they have no conflicts of interest.

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This study was conducted with written informed consent from all subjects and was approved by the ethics committees of Hokkaido University Graduate School of Medicine.

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Kato, S., Itoh, S., Yuasa, M. et al. Association of perfluorinated chemical exposure in utero with maternal and infant thyroid hormone levels in the Sapporo cohort of Hokkaido Study on the Environment and Children’s Health. Environ Health Prev Med 21, 334–344 (2016). https://doi.org/10.1007/s12199-016-0534-2

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  • DOI: https://doi.org/10.1007/s12199-016-0534-2

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