Associations between Perfluoroalkyl acids (PFASs) and maternal thyroid hormones in early pregnancy: A population-based cohort study

Environmental Research

Volumn 133, Issue , 2014, Pages 338-347

  Webster, Glenys M ^a,b   Venners, Scott A ^b   Mattman, Andre ^c   Martin, Jonathan W ^d  

^a SIMON FRASER UNIVERSITY   (Canada)

^b CHILDREN S AND WOMEN S HEALTH CENTRE OF BRITISH COLUMBIA   (Canada)

^c ST PAUL S HOSPITAL   (Canada)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Chemicals health and pregnancy (CHirP) study; Perfluoroalkyl acids (PFASs); PFCs; Pregnancy; Thyroid hormones; Thyroid peroxidase antibody (TPOAb)

Indexed keywords

IODINE; PERFLUORO COMPOUND; PERFLUOROHEXANESULFONATE; PERFLUORONONANOIC ACID; PERFLUOROOCTANESULFONIC ACID; PERFLUOROOCTANOIC ACID; THYROID PEROXIDASE ANTIBODY; THYROTROPIN; THYROXINE; UNCLASSIFIED DRUG;

ACID; ANTIBODY; BRAIN; CHILD HEALTH; HORMONE; MATERNAL HEALTH; PREGNANCY; SERUM;

ADULT; ALCOHOL CONSUMPTION; ARTICLE; BODY MASS; BRAIN DEVELOPMENT; COHORT ANALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATIONAL STUDY; DRUG USE; FEMALE; FETUS DEVELOPMENT; FREE THYROXINE INDEX; GESTATIONAL AGE; HUMAN; MAJOR CLINICAL STUDY; MATERNAL AGE; MATERNAL HYPERTENSION; MATERNAL SERUM; MATERNAL SMOKING; MATERNAL STRESS; POPULATION RESEARCH; PREGNANT WOMAN; PRIORITY JOURNAL; SECOND TRIMESTER PREGNANCY; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL;

BRITISH COLUMBIA; CANADA; VANCOUVER [BRITISH COLUMBIA];

CHEMICALS HEALTH AND PREGNANCY (CHIRP) STUDY; PERFLUOROALKYL ACIDS (PFASS); PFCS; PREGNANCY; THYROID HORMONES; THYROID PEROXIDASE ANTIBODY (TPOAB);

ADOLESCENT; ADULT; ALKANESULFONIC ACIDS; CAPRYLATES; COHORT STUDIES; ENVIRONMENTAL POLLUTANTS; FEMALE; FLUOROCARBONS; HUMANS; PREGNANCY; PREGNANCY TRIMESTER, SECOND; SULFONIC ACIDS; THYROTROPIN; THYROXINE; YOUNG ADULT;

EID: 84904263809     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2014.06.012     Document Type: Article

References (80)

1. Abbassi-Ghanavati M., Casey B.M., Spong C.Y., McIntire D.D., Halvorson L.M., Cunningham F.G. Pregnancy outcomes in women with thyroid peroxidase antibodies. Obstet. Gynecol. 2010, 116:381-386.
2. Asvold B.O., Bjøro T., Vatten L.J. Association of thyroid function with estimated glomerular filtration rate in a population-based study: the HUNT study. Eur. J. Endocrinol. 2011, 164:101-105. 10.1530/EJE-10-0705.
3. Barbesino G. Drugs affecting thyroid function. Thyroid 2010, 20:763-770.
4. BCPHP, 2009. British Columbia Perinatal Database.
5. Bellinger D.C. A strategy for comparing the contributions of environmental chemicals and other risk factors to neurodevelopment of children. Environ. Health Perspect. 2011, 120:501-507. 10.1289/ehp.1104170.
6. Bernal J., Guadaño-Ferraz A., Morte B. Perspectives in the study of thyroid hormone action on brain development and function. Thyroid 2003, 13:1005-1012. 10.1089/105072503770867174.
7. Bloom M.S., Kannan K., Spliethoff H.M., Tao L., Aldous K.M., Vena J.E. Exploratory assessment of perfluorinated compounds and human thyroid function. Physiol. Behav. 2010, 99:240-245.
8. Buckshee K., Kriplani A., Kapil A., Bhargava V.L., Takkar D. Hypothyroidism complicating pregnancy. Aust. N. Z. J. Obstet. Gynaecol. 1992, 32:240-242.
9. Butenhoff J., Costa G., Elcombe C., Farrar D., Hansen K., Iwai H., et al. Toxicity of ammonium perfluorooctanoate in male cynomolgus monkeys after oral dosing for 6 months. Toxicol. Sci. 2002, 69:244-257.
10. Calafat A.M., Wong L.Y., Kuklenyik Z., Reidy J.A., Needham L.L. 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. 2007, 115:1596-1602.
11. Chan E., Burstyn I., Cherry N., Bamforth F., Martin J.W. Perfluorinated acids and hypothyroxinemia in pregnant women. Environ. Res. 2011.
12. Chang S.-C., Thibodeaux J.R., Eastvold M.L., Ehresman D.J., Bjork J.A., Froehlich J.W., et al. Thyroid hormone status and pituitary function in adult rats given oral doses of perfluorooctanesulfonate (PFOS). Toxicology 2008, 243:330-339.
13. Chang S.C., Thibodeaux J.R., Eastvold M.L., Ehresman D.J., Bjork J.A., Froehlich J.W., et al. Negative bias from analog methods used in the analysis of free thyroxine in rat serum containing perfluorooctanesulfonate (PFOS). Toxicology 2007, 234:21-33.
14. Dallaire R., Dewailly E., Pereg D., Dery S., Ayotte P. Thyroid function and plasma concentrations of polyhalogenated compounds in Inuit adults. Environ. Health Perspect. 2009, 117:1380-1386.
15. Davis L.E., Leveno K.J., Cunningham F.G. Hypothyroidism complicating pregnancy. Obstet. Gynecol. 1988, 72:108-112.
16. Debieve F., Duliere S., Bernard P., Hubinont C., De Nayer P., Daumerie C. To treat or not to treat euthyroid autoimmune disorder during pregnancy?. Gynecol. Obstet. Investig. 2009, 67:178-182.
17. Emmett E.A., Shofer F.S., Zhang H., Freeman D., Desai C., Shaw L.M. Community exposure to perfluorooctanoate: relationships between serum concentrations and exposure sources. J. Occup. Environ. Med. 2006, 48:759-770.
18. Gilliand F. Fluorocarbons and Human Health: Studies in Occupational Cohort (Doctoral dissertation) 1992, University of Minnesota, Minneapolis, MN.
19. Glinoer D. What happens to the normal thyroid during pregnancy?. Thyroid 1999, 9:631-635.
20. Guillaume J., Schussler G.C., Goldman J. Components of the total serum thyroid hormone concentrations during pregnancy: high free thyroxine and blunted thyrotropin (TSH) response to TSH-releasing hormone in the first trimester. J. Clin. Endocrinol. Metab. 1985, 60:678-684.
21. Haddow J.E., Palomaki G.E., Allan W.C., Williams J.R., Knight G.J., Gagnon J., et al. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N. Engl. J. Med. 1999, 341:549-555.
22. Health Canada. 2010. Report on Human Biomonitoring of Environmental Chemicals in Canada - Results of the Canadian Health Measures Survey Cycle 1 (2007-2009).
23. Henrichs J., Bongers-Schokking J.J., Schenk J.J., Ghassabian A., Schmidt H.G., Visser T.J., et al. Maternal thyroid function during early pregnancy and cognitive functioning in early childhood: the generation R study. J. Clin. Endocrinol. Metab. 2010, 95:4227-4234.
24. Henrichs J., Ghassabian A., Peeters R.P., Tiemeier H. Maternal hypothyroxinemia and effects on cognitive functioning in childhood: how and why?. Clin. Endocrinol. 2013, 79:152-162. 10.1111/cen.12227.
25. Hornung H., Reed L. Estimation of average concentration in the presence of nondetectable values. Appl. Occup. Environ. Hyg. 1990, 5:46-51.
26. Inoue K., Okada F., Ito R., Kato S., Sasaki S., Nakajima S., 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, 112:1204-1207.
27. Jain R.B. 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, 76:409-421. 10.1080/15287394.2013.771547.
28. Jarrige J., Meurisse H., D'Herbomez M. Reference intervals of maternal free thyroxine (FT4) at the second and third trimesters of pregnancy using Beckman Colter[U+05F3]s access free T4 assay. Endocr. Abstr. 2006, 11:818.
29. Ji K., Kim S., Kho Y., Paek D., Sakong J., Ha J., et al. Serum concentrations of major perfluorinated compounds among the general population in Korea: dietary sources and potential impact on thyroid hormones. Environ. Int. 2012, 45:78-85. 10.1016/j.envint.2012.03.007.
30. Julvez J., Alvarez-Pedrerol M., Rebagliato M., Murcia M., Forns J., Garcia-Esteban R., et al. Thyroxine levels during pregnancy in healthy women and early child neurodevelopment. Epidemiology 2013, 24:150-157. 10.1097/EDE.0b013e318276ccd3.
31. Kannan K., Corsolini S., Falandysz J., Fillmann G., Kumar K.S., Loganathan B.G., et al. Perfluorooctanesulfonate and related fluorochemicals in human blood from several countries. Environ. Sci. Technol. 2004, 38:4489-4495.
32. Karrman A., van Bavel B., Jarnberg U., Hardell L., Lindstrom G. Perfluorinated chemicals in relation to other persistent organic pollutants in human blood. Chemosphere 2006, 64:1582-1591.
33. Kim S., Choi K., Ji K., Seo J., Kho Y., Park J., et al. Trans-placental transfer of thirteen perfluorinated compounds and relations with fetal thyroid hormones. Environ. Sci. Technol. 2011, 45:7465-7472. 10.1021/es202408a.
34. Kissa E. Fluorinated Surfactants and Repellents 2001, Marcel Dekker, Inc., New York, New York.
35. Knox S.S., Jackson T., Frisbee S.J., Javins B., Ducatman A.M. Perfluorocarbon exposure, gender and thyroid function in the C8 Health Project. J. Toxicol. Sci. 2011, 36:403-410.
36. Kooistra L., Crawford S., van Baar A.L., Brouwers E.P., Pop V.J. Neonatal effects of maternal hypothyroxinemia during early pregnancy. Pediatrics 2006, 117:161-167.
37. Krassas G.E., Poppe K., Glinoer D. Thyroid function and human reproductive health. Endocr. Rev. 2010, 31:702-755.
38. Kuklenyik Z., Reich J.A., Tully J.S., Needham L.L., Calafat A.M. Automated solid-phase extraction and measurement of perfluorinated organic acids and amides in human serum and milk. Environ. Sci. Technol. 2004, 38:3698-3704.
39. Landers K.A., McKinnon B.D., Li H., Subramaniam V.N., Mortimer R.H., Richard K. Carrier-mediated thyroid hormone transport into placenta by placental transthyretin. J. Clin. Endocrinol. Metab. 2009, 94:2610-2616. 10.1210/jc.2009-0048.
40. Lau C., Thibodeaux J.R., Hanson R.G., Rogers J.M., Grey B.E., Stanton M.E., et al. Exposure to perfluorooctane sulfonate during pregnancy in rat and mouse. II: Postnatal evaluation. Toxicol. Sci. 2003, 74:382-392.
41. Lepage N., Chitayat D., Kingdom J., Huang T. Association between second-trimester isolated high maternal serum maternal serum human chorionic gonadotropin levels and obstetric complications in singleton and twin pregnancies. Am. J. Obstet. Gynecol. 2003, 188:1354-1359.
42. Leung A.S., Millar L.K., Koonings P.P., Montoro M., Mestman J.H. Perinatal outcome in hypothyroid pregnancies. Obstet. Gynecol. 1993, 81:349-353.
43. Li Y., Shan Z., Teng W., Yu X., Li Y., Fan C., et al. Abnormalities of maternal thyroid function during pregnancy affect neuropsychological development of their children at 25-30 months. Clin. Endocrinol. 2010, 72:825-829.
44. Lockitch G. Handbook of Diagnostic Biochemistry and Hematology in Normal Pregnancy 1993, CRC Press, Boca Raton.
45. Lockwood C.M., Grenache D.G., Gronowski A.M. Serum human chorionic gonadotropin concentrations greater than 400,000IU/L are invariably associated with suppressed serum thyrotropin concentrations. Thyroid 2009, 19:863-868.
46. Lopez-Espinosa M.-J., Mondal D., Armstrong B., Bloom M.S., Fletcher T. 2012. Thyroid function and perfluoroalkyl acids in children living near a chemical plant. Environ. Health Perspect.; 10.1289/ehp.1104370.
47. Luebker D.J., York R.G., Hansen K.J., Moore J.A., Butenhoff J.L. Neonatal mortality from in utero exposure to perfluorooctanesulfonate (PFOS) in Sprague-Dawley rats: dose-response, and biochemical and pharamacokinetic parameters. Toxicology 2005, 215:149-169.
48. Melze.r D., Rice N., Depledge M.H., Henley W.E., Galloway T.S. Association between serum perfluorooctanoic acid (PFOA) and thyroid disease in the U.S. national health and nutrition examination survey. Environ. Health Perspect. 2010, 118:686-692.
49. Morreale de Escobar G., Obregon M.J., Escobar del Rey F. Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia?. J. Clin. Endocrinol. Metab. 2000, 85:3975-3987.
50. Morreale de Escobar G., Obregon M.J., Escobar del Rey F. Role of thyroid hormone during early brain development. Eur. J. Endocrinol. 2004, 151(Suppl. 3):U25-U37.
51. Negro R., Soldin O.P., Obregon M.J., Stagnaro-Green A. Hypothyroxinemia and pregnancy. Endocr. Pract. 2011, 1-24.
52. NHANES. 2007a. Laboratory Procedure Manual: Free Thyroxine (Free T4) in Serum. Available at: http://www.cdc.gov/nchs/data/nhanes/nhanes_07_08/THYROD_e_met_Free_Thyroxine_Free_T4.pdf.
53. NHANES. 2007b. Laboratory Procedure Manual: Thyroid Peroxidase Antibodies in Serum. Available at: http://www.cdc.gov/nchs/data/nhanes/nhanes_07_08/THYROD_e_met_Thyroid_Peroxidase_Antibodies.pdf.
54. NHANES. 2007c. Laboratory Procedure Manual: Thyroid Stimulating Hormone (TSH) in Serum. Available at: http://www.cdc.gov/nchs/data/nhanes/nhanes_07_08/THYROD_e_met_Thyroid_Stimulating_Hormone.pdf.
55. NHANES. 2007d. Laboratory Procedure Manual: Total Thyroxine (Total T4) in Serum. Available at: http://www.cdc.gov/nchs/data/nhanes/nhanes_07_08/THYROD_e_met_Total_Thyroxine_Total_T4.pdf.
56. Olsen G.W., Burris J.M., Burlew M.M., Mandel J.H. Epidemiologic assessment of worker serum perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) concentrations and medical surveillance examinations. J. Occup. Environ. Med./Am. Coll. Occup. Environ. Med. 2003, 45:260-270.
57. Olsen G.W., Church T.R., Miller J.P., Burris J.M., Hansen K.J., Lundberg J.K., et al. Perfluorooctanesulfonate and other fluorochemicals in the serum of American red cross adult blood donors. Environ. Health Perspect. 2003, 111:1892-1901.
58. Olsen G.W., Zobel L.R. Assessment of lipid, hepatic, and thyroid parameters with serum perfluorooctanoate (PFOA) concentrations in fluorochemical production workers. Int. Arch. Occup. Environ. Health 2007, 81:231-246.
59. PASW Statistics. 2009. Release 18.0.1 (13 November 2009).
60. Pop V.J., Brouwers E.P., Vader H.L., Vulsma T., van Baar A.L., de Vijlder J.J. Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3-year follow-up study. Clin. Endocrinol. 2003, 59:282-288.
61. Pop V.J., Kuijpens J.L., van Baar A.L., Verkerk G., van Son M.M., de Vijlder J.J., et al. Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin. Endocrinol. 1999, 50:149-155.
62. Rayman M.P. The importance of selenium to human health. Lancet 2000, 356:233-241. 10.1016/S0140-6736(00)02490-9.
63. SAS Institute Inc., 2008. SAS Version 9.2. Copyright 2008, SAS Institute Inc. Cary, NC, USA.
64. Seacat A.M., Thomford P.J., Hansen K.J., Olsen G.W., Case M.T., Butenhoff J.L. Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in cynomolgus monkeys. Toxicol. Sci. 2002, 68:249-264.
65. Soldin O.P., Soldin S.J. Thyroid hormone testing by tandem mass spectrometry. Clin. Biochem. 2011, 44:89-94.
66. Song M., Kim Y.-J., Park Y.-K., Ryu J.-C. Changes in thyroid peroxidase activity in response to various chemicals. J. Environ. Monit. 2012, 14:2121. 10.1039/c2em30106g.
67. Steenland, K., Fletcher, T., Savitz, D., 2011. C8 Science Panel Status Report: PFOA and Adult Thyroid Disease in the Mid-Ohio Valley.
68. Surks M.I., Sievert R. Drugs and thyroid function. N. Engl. J. Med. 1995, 333:1688-1694.
69. Vermiglio F., Lo Presti V.P., Moleti M., Sidoti M., Tortorella G., Scaffidi G., et al. Attention deficit and hyperactivity disorders in the offspring of mothers exposed to mild-moderate iodine deficiency: a possible novel iodine deficiency disorder in developed countries. J. Clin. Endocrinol. Metab. 2004, 89:6054-6060.
70. Wang Y., Rogan W.J., Chen P.-C., Lien G.-W., Chen H.-Y., Tseng Y.-C., et al. Association between maternal serum perfluoroalkyl substances during pregnancy and maternal and cord thyroid hormones: taiwan maternal and infant cohort study. Environ. Health Perspect. 2014, 10.1289/ehp.1306925.
71. Wang Y., Starling A.P., Haug L.S., Eggesbo M., Becher G., Thomsen C., et al. Association between Perfluoroalkyl substances and thyroid stimulating hormone among pregnant women: a cross-sectional study. Environ. Health 2013, 12:76. 10.1186/1476-069X-12-76.
72. Webster G.M., Teschke K., Janssen P.A. Recruitment of healthy first-trimester pregnant women: lessons from the chemicals, health & pregnancy study (CHirP). Matern. Child Health J. 2011.
73. Weiss J.M., Andersson P.L., Lamoree M.H., Leonards P.E., van Leeuwen S.P., Hamers T. Competitive binding of poly- and perfluorinated compounds to the thyroid hormone transport protein transthyretin. Toxicol. Sci. 2009, 109:206-216.
74. Yu W.G., Liu W., Jin Y.H. Effects of perfluorooctane sulfonate on rat thyroid hormone biosynthesis and metabolism. Environ. Toxicol. Chem./SETAC 2009, 28:990-996.
75. Yu W.G., Liu W., Jin Y.H., Liu X.H., Wang F.Q., Liu L., et al. Prenatal and postnatal impact of perfluorooctane sulfonate (PFOS) on rat development: a cross-foster study on chemical burden and thyroid hormone system. Environ. Sci. Technol. 2009, 43:8416-8422.
76. Yu W.G., Liu W., Liu L., Jin Y.H. Perfluorooctane sulfonate increased hepatic expression of OAPT2 and MRP2 in rats. Arch. Toxicol. 2010.
77. Zhang X., Chen L., Fei X.C., Ma Y.S., Gao H.W. Binding of PFOS to serum albumin and DNA: insight into the molecular toxicity of perfluorochemicals. BMC Mol. Biol. 2009, 10:16.
78. Zhang Y., Beesoon S., Zhu L., Martin J.W. Biomonitoring of perfluoroalkyl acids in human urine and estimates of biological half-life. Environ. Sci. Technol. 2013, (130827075114004). 10.1021/es401905e.
79. Zoeller R.T., Rovet J. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J. Neuroendocrinol. 2004, 16:809-818.
80. Zoeller R.T., Tan S.W., Tyl R.W. General background on the hypothalamic-pituitary-thyroid (HPT) axis. Crit. Rev. Toxicol. 2007, 37:11-53.