Neurodevelopmental disorders in children born to mothers with thyroid dysfunction: Evidence of fetal programming?

European Journal of Endocrinology

Volumn 177, Issue 1, 2017, Pages R27-R36

  Andersen, Stine Linding ^a,b   Carlé, Allan ^a   Karmisholt, Jesper ^a   Pedersen, Inge Bülow ^a   Andersen, Stig ^c,d  

^a Departments of Endocrinology   (Denmark)

^b Clinical Biochemistry   (Denmark)

^c AALBORG UNIVERSITY HOSPITAL   (Denmark)

^d AALBORG UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

THYROID HORMONE;

BRAIN DEVELOPMENT; BRAIN DISEASE; EXPERIMENTAL STUDY; FETUS BRAIN; HUMAN; MATERNAL DISEASE; MENTAL DISEASE; MOTHER; NONHUMAN; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROGENY; REVIEW; THYROID DISEASE; ADULT; COMPLICATION; FEMALE; FETUS DEVELOPMENT; INFANT; NEURODEVELOPMENTAL DISORDERS; NEWBORN; PATHOPHYSIOLOGY; PREGNANCY; PREGNANCY COMPLICATION;

ADULT; FEMALE; FETAL DEVELOPMENT; HUMANS; INFANT; INFANT, NEWBORN; MOTHERS; NEURODEVELOPMENTAL DISORDERS; PREGNANCY; PREGNANCY COMPLICATIONS; THYROID DISEASES;

EID: 85020425945     PISSN: 08044643     EISSN: 1479683X     Source Type: Journal    
DOI: 10.1530/EJE-16-0947     Document Type: Review

References (75)

1. Bernal J & Nunez J. Thyroid hormones and brain development. European Journal of Endocrinology 1995 133 390-398. (doi:10.1530/eje.0.1330390).
2. Moog NK, Entringer S, Heim C, Wadhwa PD, Kathmann N & Buss C. Influence of maternal thyroid hormones during gestation on fetal brain development. Neuroscience 2017 342 68-100. (doi:10.1016/j.neuroscience.2015.09.070).
3. Kimura-Kuroda J, Nagata I, Negishi-Kato M & Kuroda Y. Thyroid hormone-dependent development of mouse cerebellar Purkinje cells in vitro. Brain Research: Developmental Brain Research 2002 137 55-65. (doi:10.1016/S0165-3806(02)00408-X).
4. Horn S, Kersseboom S, Mayerl S, Muller J, Groba C, Trajkovic-Arsic M, Ackermann T, Visser TJ & Heuer H. Tetrac can replace thyroid hormone during brain development in mouse mutants deficient in the thyroid hormone transporter mct8. Endocrinology 2013 154 968-979. (doi:10.1210/en.2012-1628).
5. Ahmed OM, Abd El-Tawab SM & Ahmed RG. Effects of experimentally induced maternal hypothyroidism and hyperthyroidism on the development of rat offspring: I. The development of the thyroid hormones-neurotransmitters and adenosinergic system interactions. International Journal of Developmental Neuroscience 2010 28 437-454. (doi:10.1016/j.ijdevneu.2010.06.007).
6. Chen ZP & Hetzel BS. Cretinism revisited. Best Practice and Research: Clinical Endocrinology and Metabolism 2010 24 39-50. (doi:10.1016/j.beem.2009.08.014).
7. Willoughby KA, McAndrews MP & Rovet J. Effects of maternal hypothyroidism on offspring hippocampus and memory. Thyroid 2013 24 576-584. (doi:10.1089/thy.2013.0215).
8. Ghassabian A, El Marroun H, Peeters RP, Jaddoe VW, Hofman A, Verhulst FC, Tiemeier H & White T. Downstream effects of maternal hypothyroxinemia in early pregnancy: nonverbal IQ and brain morphology in school-Age children. Journal of Clinical Endocrinology and Metabolism 2014 99 2383-2390. (doi:10.1210/jc.2013-4281).
9. Samadi A, Skocic J & Rovet JF. Children born to women treated for hypothyroidism during pregnancy show abnormal corpus callosum development. Thyroid 2015 25 494-502. (doi:10.1089/thy.2014.0548).
10. Lischinsky JE, Skocic J, Clairman H & Rovet J. Preliminary findings show maternal hypothyroidism may contribute to abnormal cortical morphology in offspring. Frontiers in Endocrinology 2016 7 16. (doi:10.3389/fendo.2016.00016).
11. Korevaar TI, Muetzel R, Medici M, Chaker L, Jaddoe VW, de Rijke YB, Steegers EA, Visser TJ, White T, Tiemeier H et al. Association of maternal thyroid function during early pregnancy with offspring IQ and brain morphology in childhood: A population-based prospective cohort study. Lancet: Diabetes and Endocrinology 2016 4 35-43. (doi:10.1016/s2213-8587(15)00327-7).
12. Little J. Epidemiology of neurodevelopmental disorders in children. Prostaglandins, Leukotrienes, and Essential Fatty Acids 2000 63 11-20. (doi:10.1054/plef.2000.0185).
13. Thapar A & Cooper M. Attention deficit hyperactivity disorder. Lancet 2016 387 1240-1250. (doi:10.1016/S0140-6736(15)00238-X).
14. Susser E, Hoek HW & Brown A. Neurodevelopmental disorders after prenatal famine: The story of the Dutch Famine Study. American Journal of Epidemiology 1998 147 213-216. (doi:10.1093/oxfordjournals.aje.a009439).
15. Forsdahl A. Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? British Journal of Preventive and Social Medicine 1977 31 91-95.
16. Barker DJ, Winter PD, Osmond C, Margetts B & Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet 1989 2 577-580. (doi:10.1016/S0140-6736(89)90710-1).
17. Hales CN & Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia 1992 35 595-601. (doi:10.1007/BF00400248).
18. Kyle UG & Pichard C. The Dutch Famine of 1944-1945: A pathophysiological model of long-Term consequences of wasting disease. Current Opinion in Clinical Nutrition and Metabolic Care 2006 9 388-394. (doi:10.1097/01.mco.0000232898.74415.42).
19. Li Y, He Y, Qi L, Jaddoe VW, Feskens EJ, Yang X, Ma G & Hu FB. Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood. Diabetes 2010 59 2400-2406. (doi:10.2337/db10-0385).
20. Ekbom A, Trichopoulos D, Adami HO, Hsieh CC & Lan SJ. Evidence of prenatal influences on breast cancer risk. Lancet 1992 340 1015-1018. (doi:10.1016/0140-6736(92)93019-J).
21. Fraser A & Lawlor DA. Long-Term health outcomes in offspring born to women with diabetes in pregnancy. Current Diabetes Reports 2014 14 489. (doi:10.1007/s11892-014-0489-x).
22. Berry DC, Boggess K & Johnson QB. Management of pregnant women with type 2 diabetes mellitus and the consequences of fetal programming in their offspring. Current Diabetes Reports 2016 16 36. (doi:10.1007/s11892-016-0733-7).
23. Reynolds RM. Glucocorticoid excess and the developmental origins of disease: Two decades of testing the hypothesis - 2012 Curt Richter Award Winner. Psychoneuroendocrinology 2013 38 1-11. (doi:10.1016/j.psyneuen.2012.08.012).
24. Entringer S, Buss C & Wadhwa PD. Prenatal stress, development, health and disease risk: A psychobiological perspective-2015 Curt Richter Award Paper. Psychoneuroendocrinology 2015 62 366-375. (doi:10.1016/j.psyneuen.2015.08.019).
25. Phillips DI, Cooper C, Fall C, Prentice L, Osmond C, Barker DJ & Rees Smith B. Fetal growth and autoimmune thyroid disease. Quarterly Journal of Medicine 1993 86 247-253. (doi:10.5001/omj.2015.84).
26. Phillips DI, Barker DJ & Osmond C. Infant feeding, fetal growth and adult thyroid function. Acta Endocrinologica 1993 129 134-138. (doi:10.1530/acta.0.1290134).
27. Brix TH, Kyvik KO & Hegedus L. Low birth weight is not associated with clinically overt thyroid disease: A population based twin casecontrol study. Clinical Endocrinology 2000 53 171-176. (doi:10.1046/j.1365-2265.2000.01025.x).
28. Brix TH, Hansen PS, Rudbeck AB, Hansen JB, Skytthe A, Kyvik KO & Hegedus L. Low birth weight is not associated with thyroid autoimmunity: A population-based twin study. Journal of Clinical Endocrinology and Metabolism 2006 91 3499-3502. (doi:10.1210/jc.2006-1348).
29. Frost M, Petersen I, Hegedus L, Christiansen L, Brix T & Christensen K. Regulation of the pituitary-Thyroid axis in adulthood is not related to birth weight: Evidence from extremely birth weightdiscordant monozygotic Danish twin pairs. Thyroid 2013 23 785-790. (doi:10.1089/thy.2012.0095).
30. Mittag J, Lyons DJ, Sallstrom J, Vujovic M, Dudazy-Gralla S, Warner A, Wallis K, Alkemade A, Nordstrom K, Monyer H et al. Thyroid hormone is required for hypothalamic neurons regulating cardiovascular functions. Journal of Clinical Investigation 2013 123 509-516. (doi:10.1172/JCI65252).
31. Godoy GA, Korevaar TI, Peeters RP, Hofman A, de Rijke YB, Bongers- Schokking JJ, Tiemeier H, Jaddoe VW & Gaillard R. Maternal thyroid hormones during pregnancy, childhood adiposity and cardiovascular risk factors: The Generation R Study. Clinical Endocrinology 2014 81 117-125. (doi:10.1111/cen.12399).
32. Grattan MJ, Thomas DS, Hornberger LK, Hamilton RM, Midodzi WK & Vohra S. Maternal hypothyroidism may be associated with CHD in offspring. Cardiology in the Young 2015 25 1247-1253. (doi:10.1017/S1047951114001887).
33. Rytter D, Andersen SL, Bech BH, Halldorsson TI, Henriksen TB, Laurberg P & Olsen SF. Maternal thyroid function in pregnancy may program offspring blood pressure, but not adiposity at 20 y of age. Pediatric Research 2016 80 7-13. (doi:10.1038/pr.2016.56).
34. Vulsma T, Gons MH & de Vijlder JJ. Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to a total organification defect or thyroid agenesis. New England Journal of Medicine 1989 321 13-16. (doi:10.1056/NEJM198907063210103).
35. Morreale de Escobar G, Obregon MJ & Escobar del Rey F. Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia? Journal of Clinical Endocrinology and Metabolism 2000 85 3975-3987. (doi:10.1210/jc.85.11.3975).
36. Ismail FY, Fatemi A & Johnston MV. Cerebral plasticity: Windows of opportunity in the developing brain. European Journal of Paediatric Neurology 2017 21 23-48. (doi:10.1016/j.ejpn.2016.07.007).
37. Bernal J. Thyroid hormone regulated genes in cerebral cortex development. Journal of Endocrinology 2017 232 R83-R97. (doi:10.1530/JOE-16-0424).
38. Gil-Ibanez P, Bernal J & Morte B. Thyroid hormone regulation of gene expression in primary cerebrocortical cells: Role of thyroid hormone receptor subtypes and interactions with retinoic acid and glucocorticoids. PLoS ONE 2014 9 e91692. (doi:10.1371/journal.pone.0091692).
39. Gil-Ibanez P, Garcia-Garcia F, Dopazo J, Bernal J & Morte B. Global transcriptome analysis of primary cerebrocortical cells: identification of genes regulated by triiodothyronine in specific cell types. Cerebral Cortex 2017 27 706-717. (doi:10.1093/cercor/bhv273).
40. Boyages SC & Halpern JP. Endemic cretinism: Toward a unifying hypothesis. Thyroid 1993 3 59-69. (doi:10.1089/thy.1993.3.59).
41. Bozzi Y, Casarosa S & Caleo M. Epilepsy as a neurodevelopmental disorder. Frontiers in Psychiatry 2012 3 19. (doi:10.3389/fpsyt.2012.00019).
42. Sisodiya S. Feverish prospects for seizure genetics. Nature Genetics 2014 46 1255-1256. (doi:10.1038/ng.3150).
43. Auso E, Lavado-Autric R, Cuevas E, Del Rey FE, Morreale De Escobar G & Berbel P. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 2004 145 4037-4047. (doi:10.1210/en.2004-0274).
44. Gilbert ME, Ramos RL, McCloskey DP & Goodman JH. Subcortical band heterotopia in rat offspring following maternal hypothyroxinaemia: structural and functional characteristics. Journal of Neuroendocrinology 2014 26 528-541. (doi:10.1111/jne.12169).
45. Gallo EF & Posner J. Moving towards causality in attentiondeficit hyperactivity disorder: overview of neural and genetic mechanisms. Lancet Psychiatry 2016 3 555-567. (doi:10.1016/S2215-0366(16)00096-1).
46. Stohn JP, Martinez ME & Hernandez A. Decreased anxiety-And depression-like behaviors and hyperactivity in a type 3 deiodinasedeficient mouse showing brain thyrotoxicosis and peripheral hypothyroidism. Psychoneuroendocrinology 2016 74 46-56. (doi:10.1016/j.psyneuen.2016.08.021).
47. Hauser P, Zametkin AJ, Martinez P, Vitiello B, Matochik JA, Mixson AJ & Weintraub BD. Attention deficit-hyperactivity disorder in people with generalized resistance to thyroid hormone. New England Journal of Medicine 1993 328 997-1001. (doi:10.1056/NEJM199304083281403).
48. Bernal J. Thyroid hormone receptors in brain development and function. Nature Clinical Practice Endocrinology and Metabolism 2007 3 249-259. (doi:10.1038/ncpendmet0424).
49. Andersen SL, Laurberg P, Wu CS & Olsen J. Maternal thyroid dysfunction and risk of seizure in the child: A Danish nationwide cohort study. Journal of Pregnancy 2013 2013 636705. (doi:10.1155/2013/636705).
50. Andersen SL, Laurberg P, Wu CS & Olsen J. Attention deficit hyperactivity disorder and autism spectrum disorder in children born to mothers with thyroid dysfuntion: A Danish nationwide cohort study. BJOG 2014 121 1365-1374. (doi:10.1111/1471-0528.12681).
51. Haddow JE, Palomaki GE, Allan WC, Williams JR, Knight GJ, Gagnon J, O'Heir CE, Mitchell ML, Hermos RJ, Waisbren SE et al. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. New England Journal of Medicine 1999 341 549-555. (doi:10.1056/NEJM199908193410801).
52. Pakkila F, Mannisto T, Pouta A, Hartikainen AL, Ruokonen A, Surcel HM, Bloigu A, Vaarasmaki M, Jarvelin MR, Moilanen I et al. The impact of gestational thyroid hormone concentrations on ADHD symptoms of the child. Journal of Clinical Endocrinology and Metabolism 2014 99 E1-E8. (doi:10.1210/jc.2013-2943).
53. Modesto T, Tiemeier H, Peeters RP, Jaddoe VW, Hofman A, Verhulst FC & Ghassabian A. Maternal mild thyroid hormone insufficiency in early pregnancy and attention-deficit/hyperactivity disorder symptoms in children. JAMA Pediatrics 2015 169 838-845. (doi:10.1001/jamapediatrics.2015.0498).
54. Vermiglio F, Lo Presti VP, Moleti M, Sidoti M, Tortorella G, Scaffidi G, Castagna MG, Mattina F, Violi MA, Crisa A 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. Journal of Clinical Endocrinology and Metabolism 2004 89 6054-6060. (doi:10.1210/jc.2004-0571).
55. Ghassabian A, Bongers-Schokking JJ, de Rijke YB, van Mil N, Jaddoe VW, de Muinck Keizer-Schrama SM, Hooijkaas H, Hofman A, Visser W, Roman GC et al. Maternal thyroid autoimmunity during pregnancy and the risk of attention deficit/hyperactivity problems in children: The Generation R Study. Thyroid 2012 22 178-186. (doi:10.1089/thy.2011.0318).
56. Lazarus JH, Bestwick JP, Channon S, Paradice R, Maina A, Rees R, Chiusano E, John R, Guaraldo V, George LM et al. Antenatal thyroid screening and childhood cognitive function. New England Journal of Medicine 2012 366 493-501. (doi:10.1056/NEJMoa1106104).
57. Casey BM. Effect of treatment of maternal subclinical hypothyroidism or hypothyroxinemia on IQ in offspring. American Journal of Obstetrics and Gynecology 2016 214 S2. (doi:10.1016/j.ajog.2015.10.023).
58. Negro R, Schwartz A, Gismondi R, Tinelli A, Mangieri T & Stagnaro- Green A. Universal screening versus case finding for detection and treatment of thyroid hormonal dysfunction during pregnancy. Journal of Clinical Endocrinology and Metabolism 2010 95 1699-1707. (doi:10.1210/jc.2009-2009).
59. Hill AB. The environment and disease: Association or causation? Proceedings of the Royal Society of Medicine 1965 58 295-300.
60. Jepsen P, Johnsen SP, Gillman MW & Sorensen HT. Interpretation of observational studies. Heart 2004 90 956-960. (doi:10.1136/hrt.2003.017269).
61. Carle A, Laurberg P, Pedersen IB, Knudsen N, Perrild H, Ovesen L, Rasmussen LB & Jorgensen T. Mainly the younger hypothyroid patients are referred to hospital - evidence for referral bias. Journal of Clinical Epidemiology 2009 62 446-451. (doi:10.1016/j.jclinepi.2008.06.016).
62. Carle A, Pedersen IB, Perrild H, Ovesen L, Jorgensen T & Laurberg P. High age predicts low referral of hyperthyroid patients to specialized hospital departments: Evidence for referral bias. Thyroid 2013 23 1518-1524. (doi:10.1089/thy.2013.0074).
63. Laurberg P, Andersen SL, Hindersson P, Nohr EA & Olsen J. Dynamics and predictors of serum TSH and fT4 reference limits in early pregnancy: A study within the Danish National Birth Cohort. Journal of Clinical Endocrinology and Metabolism 2016 101 2484-2492. (doi:10.1210/jc.2016-1387).
64. Dashe JS, Casey BM, Wells CE, McIntire DD, Byrd EW, Leveno KJ & Cunningham FG. Thyroid-stimulating hormone in singleton and twin pregnancy: importance of gestational age-specific reference ranges. Obstetrics and Gynecology 2005 106 753-757. (doi:10.1097/01.AOG.0000175836.41390.73).
65. Mannisto T, Surcel HM, Ruokonen A, Vaarasmaki M, Pouta A, Bloigu A, Jarvelin MR, Hartikainen AL & Suvanto E. Early pregnancy reference intervals of thyroid hormone concentrations in a thyroid antibody-negative pregnant population. Thyroid 2011 21 291-298. (doi:10.1089/thy.2010.0337).
66. Li C, Shan Z, Mao J, Wang W, Xie X, Zhou W, Li C, Xu B, Bi L, Meng T et al. Assessment of thyroid function during first-Trimester pregnancy: What is the rational upper limit of serum TSH during the first trimester in Chinese pregnant women? Journal of Clinical Endocrinology and Metabolism 2014 99 73-79. (doi:10.1210/jc.2013-1674).
67. Andersen SL, Olsen J & Laurberg P. Foetal programming by maternal thyroid disease. Clinical Endocrinology 2015 81 126-133. (doi:10.1111/cen.12415).
68. Andersen SL, Olsen J, Wu CS & Laurberg P. Smoking reduces the risk of hypothyroidism and increases the risk of hyperthyroidism: Evidence from 450, 842 mothers giving birth in Denmark. Clinical Endocrinology 2014 80 307-314. (doi:10.1111/cen.12279).
69. Hartoft-Nielsen ML, Boas M, Bliddal S, Rasmussen AK, Main K & Feldt-Rasmussen U. Do thyroid disrupting chemicals influence foetal development during pregnancy? Journal of Thyroid Research 2011 2011 342189. (doi:10.4061/2011/342189).
70. Liew Z, Ritz B, von Ehrenstein OS, Bech BH, Nohr EA, Fei C, Bossi R, Henriksen TB, Bonefeld-Jorgensen EC & Olsen J. Attention deficit/hyperactivity disorder and childhood autism in association with prenatal exposure to perfluoroalkyl substances: A nested case-control study in the Danish National Birth Cohort. Environmental Health Perspectives 2015 123 367-373. (doi:10.1289/ehp.1408412).
71. Andersen SL, Olsen J, Wu CS & Laurberg P. Psychiatric disease in late adolescence and young adulthood. Foetal programming by maternal hypothyroidism? Clinical Endocrinology 2014 81 126-133. (doi:10.1111/cen.12415).
72. McLaughlin KA, Gadermann AM, Hwang I, Sampson NA, Al-Hamzawi A, Andrade LH, Angermeyer MC, Benjet C, Bromet EJ, Bruffaerts R et al. Parent psychopathology and offspring mental disorders: Results from the WHO World Mental Health Surveys. British Journal of Psychiatry 2012 200 290-299. (doi:10.1192/bjp.bp.111.101253).
73. Andersen SL, Olsen J, Wu CS & Laurberg P. Low birth weight in children born to mothers with hyperthyroidism and high birth weight in hypothyroidism, whereas preterm birth is common in both conditions: A Danish National Hospital Register study. European Thyroid Journal 2013 2 135-144. (doi:10.1159/000350513).
74. Prummel MF & Wiersinga WM. Thyroid autoimmunity and miscarriage. European Journal of Endocrinology 2004 150 751-755. (doi:10.1530/eje.0.1500751).
75. Reynolds RM, Jacobsen GH & Drake AJ. What is the evidence in humans that DNA methylation changes link events in utero and later life disease? Clinical Endocrinology 2013 78 814-822. (doi:10.1111/cen.12164).