Stimulation of Thyroid Function by Human Chorionic Gonadotropin during Pregnancy: A Risk Factor for Thyroid Disease and a Mechanism for Known Risk Factors

Thyroid

Volumn 27, Issue 3, 2017, Pages 440-450

  Korevaar, Tim I M ^a   De Rijke, Yolanda B ^b   Chaker, Layal ^a   Medici, Marco ^a   Jaddoe, Vincent W V ^a,b   Steegers, Eric A P ^b   Visser, Theo J ^a   Peeters, Robin P ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b SOPHIA CHILDREN S HOSPITAL   (Netherlands)

Author keywords

FT4; HCG; pregnancy; TSH

Indexed keywords

CHORIONIC GONADOTROPIN; CREATININE; THYROID PEROXIDASE ANTIBODY; THYROTROPIN; THYROXINE;

ARTICLE; BODY MASS; CHEMOLUMINESCENCE; COHORT ANALYSIS; DISEASE ASSOCIATION; ENZYME ACTIVITY; FEMALE; FREE THYROXINE INDEX; HUMAN; HYPERTHYROIDISM; HYPOTHYROIDISM; MAJOR CLINICAL STUDY; MATERNAL AGE; MATERNAL SERUM; NULLIPARA; OVERT HYPERTHYROIDISM; PARITY; PREGNANCY; PREGNANT WOMAN; PRIMIPARA; PRIORITY JOURNAL; PROSPECTIVE STUDY; RISK FACTOR; SMOKING; SUBCLINICAL HYPERTHYROIDISM; SUBCLINICAL HYPOTHYROIDISM; THYROID DISEASE; THYROID FUNCTION; ADULT; BLOOD; NETHERLANDS; PREGNANCY COMPLICATION; YOUNG ADULT;

ADULT; CHORIONIC GONADOTROPIN; COHORT STUDIES; FEMALE; HUMANS; HYPERTHYROIDISM; HYPOTHYROIDISM; NETHERLANDS; PREGNANCY; PREGNANCY COMPLICATIONS; PROSPECTIVE STUDIES; RISK FACTORS; THYROTROPIN; THYROXINE; YOUNG ADULT;

EID: 85014676416     PISSN: 10507256     EISSN: 15579077     Source Type: Journal    
DOI: 10.1089/thy.2016.0527     Document Type: Article

References (58)

1. Glinoer D, de Nayer P, Bourdoux P, Lemone M, Robyn C, van Steirteghem A, Kinthaert J, Lejeune B 1990 Regulation of maternal thyroid during pregnancy. J Clin Endocrinol Metab 71:276-287.
2. Haddow JE, McClain MR, Lambert-Messerlian G, Palomaki GE, Canick JA, Cleary-Goldman J, Malone FD, Porter TF, Nyberg DA, Bernstein P, D'Alton ME, First and Second Trimester Evaluation of Risk for Fetal Aneuploidy Research Consortium 2008 Variability in thyroid-stimulating hormone suppression by human chorionic [corrected] gonadotropin during early pregnancy. J Clin Endocrinol Metab 93:3341-3347.
3. Korevaar TI, Steegers EA, de Rijke YB, Schalekamp-Timmermans S,VisserWE, Hofman A, Jaddoe VW, Tiemeier H, Visser TJ, Medici M, Peeters RP 2015 Reference ranges and determinants of total hCG levels during pregnancy: the Generation R Study. Eur J Epidemiol 30:1057-1066.
4. Thorpe-Beeston JG, Nicolaides KH, Felton CV, Butler J, McGregor AM 1991 Maturation of the secretion of thyroid hormone and thyroid-stimulating hormone in the fetus. N Engl J Med 324:532-536.
5. Burrow GN, Fisher DA, Larsen PR 1994 Maternal and fetal thyroid function. N Engl J Med 331:1072-1078.
6. Stagnaro-Green A, Abalovich M, Alexander E, Azizi F, Mestman J, Negro R, Nixon A, Pearce EN, Soldin OP, Sullivan S, Wiersinga W, American Thyroid Association Taskforce on Thyroid Disease During Pregnancy and Postpartum 2011 Guidelines of the American Thyroid Association for the diagnosis and management of thyroid disease during pregnancy and postpartum. Thyroid 21:1081-1125.
7. De Groot L, Abalovich M, Alexander EK, Amino N, Barbour L, Cobin RH, Eastman CJ, Lazarus JH, Luton D, Mandel SJ, Mestman J, Rovet J, Sullivan S 2012 Management of thyroid dysfunction during pregnancy and postpartum: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97:2543-2565.
8. Lazarus J, Brown RS, Daumerie C, Hubalewska-Dydejczyk A, Negro R, Vaidya B 2014 2014 European thyroid association guidelines for the management of subclinical hypothyroidism in pregnancy and in children. Eur Thyroid J 3:76-94.
9. Chan S, Boelaert K 2015 Optimal management of hypothyroidism, hypothyroxinaemia and euthyroid TPO antibody positivity preconception and in pregnancy. Clin Endocrinol (Oxf) 82:313-326.
10. Korevaar TI, Muetzel R, Medici M, Chaker L, Jaddoe VW, de Rijke YB, Steegers EA, Visser TJ, White T, Tiemeier H, Peeters RP 2016 Association of maternal thyroid function during early pregnancy with offspring IQ and brain morphology in childhood: a population-based prospective cohort study. Lancet Diabetes Endocrinol 4:35-43.
11. Modesto T, Tiemeier H, Peeters RP, Jaddoe VW, Hofman A, Verhulst FC, Ghassabian A 2015 Maternal mild thyroid hormone insufficiency in early pregnancy and attentiondeficit/ hyperactivity disorder symptoms in children. JAMA Pediatr 169:838-845.
12. Medici M, Korevaar TI, Visser WE, Visser TJ, Peeters RP 2015 Thyroid function in pregnancy: what is normal? Clin Chem 61:704-713.
13. Krassas GE, Poppe K, Glinoer D 2010 Thyroid function and human reproductive health. Endocr Rev 31:702-755.
14. Dieguez M, Herrero A, Avello N, Suarez P, Delgado E, Menendez E 2016 Prevalence of thyroid dysfunction in women in early pregnancy: does it increase with maternal age? Clin Endocrinol (Oxf) 84:121-126.
15. Mannisto T, Surcel HM, Ruokonen A, Vaarasmaki M, Pouta A, Bloigu A, Jarvelin MR, Hartikainen AL, Suvanto E 2011 Early pregnancy reference intervals of thyroid hormone concentrations in a thyroid antibody-negative pregnant population. Thyroid 21:291-298.
16. Mannisto T, Hartikainen AL, Vaarasmaki M, Bloigu A, Surcel HM, Pouta A, Jarvelin MR, Ruokonen A, Suvanto E 2012 Smoking and early pregnancy thyroid hormone and anti-thyroid antibody levels in euthyroid mothers of the Northern Finland Birth Cohort 1986. Thyroid 22:944-950.
17. Mosso L, Martinez A, Rojas MP, Latorre G, Margozzini P, Lyng T, Carvajal J, Campusano C, Arteaga E, Boucai L 2016 Early pregnancy thyroid hormone reference ranges in Chilean women: the influence of body mass index. Clin Endocrinol (Oxf) 85:942-948.
18. Korevaar TI, Medici M, de Rijke YB, Visser W, de Muinck Keizer-Schrama SM, Jaddoe VW, Hofman A, Ross HA, Visser WE, Hooijkaas H, Steegers EA, Tiemeier H, Bongers-Schokking JJ, Visser TJ, Peeters RP 2013 Ethnic differences in maternal thyroid parameters during pregnancy: the Generation R study. J Clin Endocrinol Metab 98:3678-3686.
19. Korevaar TI, Nieboer D, Bisschop PH, Goddijn M, Medici M, Chaker L, de Rijke YB, Jaddoe VW, Visser TJ, Steyerberg EW, Tiemeier H, Vrijkotte TG, Peeters RP 2016 Risk factors and a clinical prediction model for low maternal thyroid function during early pregnancy: two populationbased prospective cohort studies. Clin Endocrinol (Oxf) 85:902-909.
20. Shi X, Han C, Li C, Mao J, Wang W, Xie X, Li C, Xu B, Meng T, Du J, Zhang S, Gao Z, Zhang X, Fan C, Shan Z, Teng W 2015 Optimal and safe upper limits of iodine intake for early pregnancy in iodine-sufficient regions: a cross-sectional study of 7190 pregnant women in China. J Clin Endocrinol Metab 100:1630-1638.
21. Ashoor G, Maiz N, Cuckle H, Jawdat F, Nicolaides KH 2011 Maternal thyroid function at 11-13 weeks of gestation in fetal trisomies 21 and 18. Prenat Diagn 31:33-37.
22. Goetzl L, Krantz D, Simpson JL, Silver RK, Zachary JM, Pergament E, Platt LD, Mahoney MJ, Wapner RJ 2004 Pregnancy-associated plasma protein A, free beta-hCG, nuchal translucency, and risk of pregnancy loss. Obstet Gynecol 104:30-36.
23. Keikkala E, Vuorela P, Laivuori H, Romppanen J, Heinonen S, Stenman UH 2013 First trimester hyperglycosylated human chorionic gonadotrophin in serum: a marker of earlyonset preeclampsia. Placenta 34:1059-1065.
24. Rabie NZ, Magann EF 2014 Human chronic gonadotropin concentrations in very early pregnancy and subsequent preeclampsia. Womens Health (Lond Engl) 10:483-485.
25. Androutsopoulos G, Gkogkos P, Decavalas G 2013 Midtrimester maternal serum HCG and alpha fetal protein levels: clinical significance and prediction of adverse pregnancy outcome. Int J Endocrinol Metab 11:102-106.
26. Gonen R, Perez R, David M, Dar H, Merksamer R, Sharf M 1992 The association between unexplained second-trimester maternal serum hCG elevation and pregnancy complications. Obstet Gynecol 80:83-86.
27. Korevaar TI, Steegers EA, Pop VJ, Broeren MA, Chaker L, de Rijke YB, Jaddoe VW, Medici M, Visser TJ, Tiemeier H, Peeters RP 2016 Thyroid autoimmunity impairs the thyroidal response to hCG: two population-based prospective cohort studies. J Clin Endocrinol Metab Oct 18:jc20162942 [Epub ahead of print].
28. Jaddoe VW, van Duijn CM, Franco OH, van der Heijden AJ, van Iizendoorn MH, de Jongste JC, van der Lugt A, Mackenbach JP, Moll HA, Raat H, Rivadeneira F, Steegers EA, Tiemeier H, Uitterlinden AG, Verhulst FC, Hofman A 2012 The Generation R Study: design and cohort update 2012. Eur J Epidemiol 27:739-756.
29. Medici M, de Rijke YB, Peeters RP, Visser W, de Muinck Keizer-Schrama SM, Jaddoe VV, Hofman A, Hooijkaas H, Steegers EA, Tiemeier H, Bongers-Schokking JJ, Visser TJ 2012 Maternal early pregnancy and newborn thyroid hormone parameters: the Generation R study. J Clin Endocrinol Metab 97:646-652.
30. Cole LA 2012 The hCG assay or pregnancy test. Clin Chem Lab Med 50:617-630.
31. Medici M, Korevaar TI, Schalekamp-Timmermans S, Gaillard R, de Rijke YB, Visser WE, Visser W, de Muinck Keizer-Schrama SM, Hofman A, Hooijkaas H, Bongers-Schokking JJ, Tiemeier H, Jaddoe VW, Visser TJ, Peeters RP, Steegers EA 2014 Maternal early-pregnancy thyroid function is associated with subsequent hypertensive disorders of pregnancy: the generation R study. J Clin Endocrinol Metab 99:E2591-2598.
32. Korevaar TI, Steegers EA, de Rijke YB, Visser WE, Jaddoe VW, Visser TJ, Medici M, Peeters RP 2015 Placental angiogenic factors are associated with maternal thyroid function and modify hCG-mediated FT4 stimulation. J Clin Endocrinol Metab 100:E1328-1334.
33. Cooper DS, Laurberg P 2013 Hyperthyroidism in pregnancy. Lancet Diabetes Endocrinol 1:238-249.
34. Koren G, Madjunkova S, Maltepe C 2014 The protective effects of nausea and vomiting of pregnancy against adverse fetal outcome-A systematic review. Reprod Toxicol 47:77-80.
35. Korevaar TI, Steegers EA, Chaker L, Medici M, Jaddoe VW, Visser TJ, de Rijke YB, Peeters RP 2016 The risk of pre-eclampsia according to high thyroid function in pregnancy differs by hCG concentration. J Clin Endocrinol Metab:jc20162397.
36. Henrichs J, Ghassabian A, Peeters RP, Tiemeier H 2013 Maternal hypothyroxinemia and effects on cognitive functioning in childhood: how and why? Clin Endocrinol (Oxf) 79:152-162.
37. Korevaar TI, Schalekamp-Timmermans S, de Rijke YB, Visser WE, Visser W, de Muinck Keizer-Schrama SM, Hofman A, Ross HA, Hooijkaas H, Tiemeier H, Bongers-Schokking JJ, Jaddoe VW, Visser TJ, Steegers EA, Medici M, Peeters RP 2013 Hypothyroxinemia and TPO-antibody positivity are risk factors for premature delivery: the generation R study. J Clin Endocrinol Metab 98:4382-4390.
38. Medici M, Timmermans S, Visser W, de Muinck Keizer-Schrama SM, Jaddoe VW, Hofman A, Hooijkaas H, de Rijke YB, Tiemeier H, Bongers-Schokking JJ, Visser TJ, Peeters RP, Steegers EA 2013 Maternal thyroid hormone parameters during early pregnancy and birth weight: the Generation R Study. J Clin Endocrinol Metab 98:59-66.
39. Julvez J, Alvarez-Pedrerol M, Rebagliato M, Murcia M, Forns J, Garcia-Esteban R, Lertxundi N, Espada M, Tardon A, Riano Galan I, Sunyer J 2013 Thyroxine levels during pregnancy in healthy women and early child neurodevelopment. Epidemiology 24:150-157.
40. Berbel P, Mestre JL, Santamaria A, Palazon I, Franco A, Graells M, Gonzalez-Torga A, de Escobar GM 2009 Delayed neurobehavioral development in children born to pregnant women with mild hypothyroxinemia during the first month of gestation: the importance of early iodine supplementation. Thyroid 19:511-519.
41. Pop VJ, Vulsma T 2005 Maternal hypothyroxinaemia during (early) gestation. Lancet 365:1604-1606.
42. Zimmermann MB 2007 The adverse effects of mild-tomoderate iodine deficiency during pregnancy and childhood: a review. Thyroid 17:829-835.
43. Zimmermann MB, Boelaert K 2015 Iodine deficiency and thyroid disorders. Lancet Diabetes Endocrinol 3:286-295.
44. Pedersen KM, Laurberg P, Iversen E, Knudsen PR, Gregersen HE, Rasmussen OS, Larsen KR, Eriksen GM, Johannesen PL 1993 Amelioration of some pregnancyassociated variations in thyroid function by iodine supplementation. J Clin Endocrinol Metab 77:1078-1083.
45. Negro R, Soldin OP, Obregon MJ, Stagnaro-Green A 2011 Hypothyroxinemia and pregnancy. Endocr Pract 17:422-429.
46. Abbassi-Ghanavati M, Casey BM, Spong CY, McIntire DD, Halvorson LM, Cunningham FG 2010 Pregnancy outcomes in women with thyroid peroxidase antibodies. Obstet Gynecol 116:381-386.
47. Laurberg P, Knudsen N, Andersen S, Carle A, Pedersen IB, Karmisholt J 2012 Thyroid function and obesity. European Thyroid Journal 1:159-167.
48. Sanchez VC, Goldstein J, Stuart RC, Hovanesian V, Huo L, Munzberg H, Friedman TC, Bjorbaek C, Nillni EA 2004 Regulation of hypothalamic prohormone convertases 1 and 2 and effects on processing of prothyrotropin-releasing hormone. J Clin Invest 114:357-369.
49. Legradi G, Emerson CH, Ahima RS, Flier JS, Lechan RM 1997 Leptin prevents fasting-induced suppression of prothyrotropin-releasing hormone messenger ribonucleic acid in neurons of the hypothalamic paraventricular nucleus. Endocrinology 138:2569-2576.
50. Roef G, Lapauw B, Goemaere S, Zmierczak HG, Toye K, Kaufman JM, Taes Y 2012 Body composition and metabolic parameters are associated with variation in thyroid hormone levels among euthyroid young men. Eur J Endocrinol 167:719-726.
51. Clifton VL, Stark MJ, Osei-Kumah A, Hodyl NA 2012 Review: The feto-placental unit, pregnancy pathology and impact on long term maternal health. Placenta 33: S37-41.
52. Scott NM, Hodyl NA, Murphy VE, Osei-Kumah A, Wyper H, Hodgson DM, Smith R, Clifton VL 2009 Placental cytokine expression covaries with maternal asthma severity and fetal sex. J Immunol 182:1411-1420.
53. Brown ZA, Schalekamp-Timmermans S, Tiemeier HW, Hofman A, Jaddoe VW, Steegers EA 2014 Fetal sex specific differences in human placentation: a prospective cohort study. Placenta 35:359-364.
54. Yoshimura M, Hershman JM, Pang XP, Berg L, Pekary AE 1993 Activation of the thyrotropin (TSH) receptor by human chorionic gonadotropin and luteinizing hormone in Chinese hamster ovary cells expressing functional human TSH receptors. J Clin Endocrinol Metab 77:1009-1013.
55. Yoshimura M, Pekary AE, Pang XP, Berg L, Goodwin TM, Hershman JM 1994 Thyrotropic activity of basic isoelectric forms of human chorionic gonadotropin extracted from hydatidiform mole tissues. J Clin Endocrinol Metab 78: 862-866.
56. Hoermann R, Kubota K, Amir SM 1993 Role of subunit sialic acid in hepatic binding, plasma survival rate, and in vivo thyrotropic activity of human chorionic gonadotropin. Thyroid 3:41-47.
57. Boas M, Forman JL, Juul A, Feldt-Rasmussen U, Skakkebaek NE, Hilsted L, Chellakooty M, Larsen T, Larsen JF, Petersen JH, Main KM 2009 Narrow intra-individual variation of maternal thyroid function in pregnancy based on a longitudinal study on 132 women. Eur J Endocrinol 161: 903-910.
58. Kovalevskaya G, Birken S, Kakuma T, O'Connor JF 1999 Early pregnancy human chorionic gonadotropin (hCG) isoforms measured by an immunometric assay for choriocarcinoma-like hCG. J Endocrinol 161:99-106.