Maternal hypothyroxinaemia in early pregnancy and problem behavior in 5-year-old offspring

Psychoneuroendocrinology

Volumn 81, Issue , 2017, Pages 29-35

  Oostenbroek, Maurits H W ^a   Kersten, Remco H J ^a   Tros, Benjamin ^a   Kunst, Anton E ^a   Vrijkotte, Tanja G M ^a   Finken, Martijn J J ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Follow up studies; Maternal hypothyroxinemia; Pregnancy; Problem behavior; Thyroid function

Indexed keywords

THYROTROPIN; THYROXINE;

ADULT; ARTICLE; ATTENTION DEFICIT DISORDER; ATTENTION DISTURBANCE; CHILD; COMMUNITY SAMPLE; CONDUCT PROBLEM; CONTROLLED STUDY; EMOTIONAL PROBLEM; FEMALE; FIRST TRIMESTER PREGNANCY; FREE THYROXINE INDEX; HUMAN; HYPERACTIVITY; HYPOTHYROXINEMIA; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; PARENT; PEER RELATIONSHIP PROBLEM; PRESCHOOL CHILD; PROBLEM BEHAVIOR; PROSOCIAL BEHAVIOR; STRENGTHS AND DIFFICULTIES QUESTIONNAIRE; TEACHER; THYROID DISEASE; BLOOD; GESTATIONAL AGE; MOTHER; PREGNANCY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE; PSYCHOLOGY; THYROID FUNCTION TEST; YOUNG ADULT;

ADULT; CHILD, PRESCHOOL; FEMALE; GESTATIONAL AGE; HUMANS; LONGITUDINAL STUDIES; MALE; MOTHERS; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; PROBLEM BEHAVIOR; THYROID FUNCTION TESTS; THYROTROPIN; THYROXINE; YOUNG ADULT;

EID: 85017286128     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2017.03.021     Document Type: Article

References (48)

1. Aarnoudse-Moens, C.S., Weisglas-Kuperus, N., van Goudoever, J.B., Oosterlaan, J., Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight infants. Pediatrics 124 (2009), 717–728.
2. Auso, E., Lavado-Autric, R., Cuevas, E., Escobar del Rey, F., 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 145 (2004), 4037–4047.
3. Bath, S.C., Steer, C.D., Golding, J., Emmett, P., Rayman, M.P., Effect of inadequate iodine status in UK pregnant women on cognitive outcomes in their children: results from the Avon Longitudinal Study of Parents and Children (ALSPAC). Lancet 382 (2013), 331–337.
4. Berbel, P., Mestre, J.L., Santamaría, A., Palazón, I., Franco, A., Graells, M., González-Torga, A., Morreale de Escobar, G., 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 (2009), 511–519.
5. Bernal, J., Thyroid hormone regulated genes in cerebral cortex development. J. Endocrinol. 232 (2017), R83–R97.
6. Bonvincini, C., Faraone, S.V., Scassellati, C., Common and specific genes and peripheral biomarkers in children and adults with attention-deficit/hyperactivity disorder. World J. Biol. Psychiatry 18:January (2017), 1–52 (Epub ahead of print).
7. Craig, W.Y., Allan, W.C., Kloza, E.M., Pulkkinen, A.J., Waisbren, S., Spratt, D.I., Palomaki, G.E., Neveux, L.M., Haddow, J.E., Mid-gestational maternal free thyroxine concentration and offsprin neurocognitive development at age two years. J. Clin. Endocrinol. Metab. 97 (2012), E22–E28.
8. De Moura, L.M., Cogo-Moreira, H., de Ávila, C.R., Pan, P.M., Gadelha, A., Moriyama, T., del Aquilla, M.A., Hoexter, M., Salum, G.A., Picon, F.A., Anés, M., Mercadante, M.T., Lacerda, A., Amaro, E. Jr., Miguel, E.C., Rohde, L.A., Bressan, R.A., McGuire, P., Sato, J.R., de Jesus Mari, J., Jackowski, A.P., Children with poor reading skills at the word level show reduced fractional anisotropy in white matter tracts of both hemispheres. Brain Connect. 6 (2016), 519–523.
9. Delange, F., Benker, G., Caron, P., Eber, O., Ott, W., Peter, F., Podoba, J., Simescu, M., Szybinsky, Z., Vertongen, F., Vitti, P., Wiersinga, W., Zamrazil, V., Thyroid volume and urinary iodine in European schoolchildren: standardization of values for assessment of iodine deficiency. Eur. J. Endocrinol. 136 (1997), 180–187.
10. Finken, M.J., van Eijsden, M., Loomans, E.M., Vrijkotte, T.G., Rotteveel, J., Maternal hypothyroxinemia in early pregnancy predicts reduced performance in reaction time tests in 5- to 6-year-old offspring. J. Clin. Endocrinol. Metab. 98 (2013), 1417–1426.
11. Frank, J.E., Faix, J.E., Hermos, R.J., Mullaney, D.M., Rojan, D.A., Mitchell, M.L., Klein, R.Z., Thyroid function in very low birth weight infants: effects on neonatal hypothyroidism screening. J. Pediatr. 128 (1996), 548–554.
12. Ghassabian, A., Bongers-Schokking, J.J., Henrichs, J., Jaddoe, V.W., Visser, T.J., Visser, W., de Muinck Keizer-Schrama, S.M., Hooijkaas, H., Steegers, E.A., Hofman, A., Verhulst, F.C., van der Ende, J., de Rijke, Y.B., Tiemeier, H., Maternal thyroid function during pregnancy and behavioral problems in the offspring: the Generation R study. Pediatr. Res. 69 (2011), 454–459.
13. Ghassabian, A., Bongers-Schokking, J.J., de Rijke, Y.B., van Mil, N., Jaddoe, V.W., de Muinck Keizer-Schrama, S.M., Hooijkaas, H., Hofman, A., Visser, W., Roman, G.C., Visser, T.J., Verhulst, F.C., Tiemeier, H., Maternal thyroid autoimmunity during pregnancy and the risk of attention deficit/hyperactivity problems in children: the Generation R Study. Thyroid 22 (2012), 178–186.
14. Ghassabian, A., el Marroun, H., Peeters, R.P., Jaddoe, V.W., Hofman, A., Verhulst, F.C., Tiemeier, H., White, T., Downstream effects of maternal hypothyroxinemia in early pregnancy: nonverbal IQ and brain morphology in school-age children. J. Clin. Endocrinol. Metab. 99 (2014), 2383–2390.
15. Ghassabian, A., Steenweg-de Graaff, J., Peeters, R.P., Ross, H.A., Jaddoe, V.W., Hofman, A., Verhulst, F.C., White, T., Tiemeier, H., Maternal urinary iodine concentration in pregnancy and children's cognition: results from a population-based birth cohort in an iodine-sufficient area. BMJ Open, 4, 2014, e005520.
16. Goodman, R., The strengths and difficulties questionnaire: a research note. J. Child Psychol. Psychiatry 38 (1997), 581–586.
17. Haddow, J.E., Palomaki, G.E., Allan, W.C., Williams, J.R., Knight, G.J., Gagnon, J., O'Heir, C.E., Mitchell, M.L., Hermos, R.J., Waisbren, S.E., Faix, J.D., Klein, R.Z., Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N. Engl. J. Med. 341 (1999), 549–555.
18. Henrichs, J., Bongers-Schokking, J.J., Schenk, J.J., Ghassabian, A., Schmidt, H.G., Visser, T.J., Hooijkaas, H., de Muinck Keizer-Schrama, S.M., Hofman, A., Jaddoe, V.W., Visser, W., Steegers, E.A., Verhulst, F.C., de Rijke, Y.B., Tiemeier, H., Maternal thyroid function during early pregnancy and cognitive functioning in early childhood: the Generation R study. J. Clin. Endocrinol. Metab. 95 (2009), 4227–4234.
19. Kalff, A.C., de Sonneville, L.M., Hurks, P.P., Hendriksen, J.G., Kroes, M., Feron, F.J., Steyaert, J., van Zeben, T.M., Vles, J.S., Jolles, J., Speed, speed variability, and accuracy of information processing in 5–6-year-old children at risk of ADHD. J. Int. Neuropsychol. Soc. 11 (2005), 173–183.
20. Korevaar, T.I., Muetzel, R., Medici, M., Chaker, L., Jaddoe, V.W., de Rijke, Y.B., Steegers, E.A., Visser, T.J., White, T., Tiemeier, H., Peeters, R.P., 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 (2016), 35–43.
21. Langevin, L.M., Macmaster, F.P., Crawford, S., Lebel, C., Dewey, D., Common white matter microstructure alterations in pediatric motor and attention disorders. J. Pediatr. 164 (2014), 1157–1164.
22. Lazarus, J.H., Bestwick, J.P., Channon, S., Paradice, R., Maina, A., Rees, R., Chiusano, E., John, R., Guaraldo, V., George, L.M., Perona, M., Dall'Amico, D., Parkes, A.B., Joomun, M., Wald, N.J., Antenatal thyroid screening and childhood cognitive function. N. Engl. J. Med. 366 (2012), 493–501.
23. Li, Y., Shan, Z., Teng, W., Yu, X., Li, Y., Fan, C., Teng, X., Guo, R., Wang, H., Li, J., Chen, Y., Wang, W., Chawinga, M., Zhang, L., Yang, L., Zhao, Y., Hua, T., Abnormalities of maternal thyroid function during pregnancy affect neuropsychological development of their children at 25–30 months. Clin. Endocrinol. (Oxf.) 72 (2010), 825–829.
24. Matejko, A.A., Ansari, D., Drawing connections between white matter and numerical and mathematical cognition: a literature review. Neurosci. Biobehav. Rev. 48 (2015), 35–52.
25. Mieloo, C., Raat, H., van Oort, F., Bevaart, F., Vogel, I., Donker, M., Jansen, W., Validity and reliability of the strengths and difficulties questionnaire in 5–6 year olds: differences by gender or by parental education?. PLoS One, 7, 2012, e36805.
26. Mieloo, C.L., Bevaart, F., Donker, M.C., van Oort, F.V., Raat, H., Jansen, W., Validation of the SDQ in a multi-ethnic population of young children. Eur. J. Public Health 24 (2014), 26–32.
27. Modesto, T., Tiemeier, H., Peeters, R.P., Jaddoe, V.W., Hofman, A., Verhulst, F.C., Ghassabian, A., Maternal mild thyroid hormone insufficiency in early pregnancy and attention-Deficit/Hyperactivity disorder symptoms in children. JAMA Pediatr. 169 (2015), 838–845.
28. Morreale de Escobar, G., Obregon, M.J., Escobar del Rey, F., Maternal thyroid hormones early in pregnancy and brain development. Best. Pract. Res. Clin. Endocrinol. Metab. 18 (2004), 225–248.
29. Morte, B., Díez, D., Ausó, E., Belinchón, M.M., Gil-Ibáñez, P., Grijota-Martínez, C., Navarro, D., de Escobar, G.M., Berbel, P., Bernal, J., Thyroid hormone regulation of gene expression in the developing rat fetal cerebral cortex: prominent role of the Ca2+/calmodulin-dependent protein kinase IV pathway. Endocrinology 15 (2010), 810–820.
30. Naaijen, J., Bralten, J., Poelmans, G., IMAGE consortium, Glennon, J.C., Franke, B., Buitelaar, J.K., Glutamatergic and GABAergic gene sets in attention-deficit/hyperactivity disorder: association to overlapping traits in ADHD and autism. Transl. Psychiatry, 7, 2017, e999.
31. Navarro, D., Alvarado, M., Navarrete, F., Giner, M., Obregon, M.J., Manzanares, J., Berbel, P., Gestational and early postnatal hypothyroidism alters VGluT1 and VGAT bouton distribution in the neocortex and hippocampus, and behavior in rats. Front. Neuroanat., 9, 2015, 9.
32. Noten, A.M., Loomans, E.M., Vrijkotte, T.G., van Trotsenburg, A.S., Rotteveel, J., van Eijsden, M., Finken, M.J., Maternal hypothyroxinaemia in early pregnancy and school performance in 5-year-old offspring. Eur. J. Endocrinol. 173 (2015), 563–571.
33. Oken, E., Braverman, L.E., Platek, D., Mitchell, M.L., Lee, S.L., Pearce, E.N., Neonatal thyroxine, maternal thyroid function, and child cognition. J. Clin. Endocrinol. Metab. 94 (2009), 497–503.
34. Päkkilä, F., Männistö, T., Pouta, A., Hartikainen, A.L., Ruokonen, A., Surcel, H.M., Bloigu, A., Vääräsmäki, M., Järvelin, M.R., Moilanen, I., Suvanto, E., The impact of gestational thyroid hormone concentrations on ADHD symptoms of the child. J. Clin. Endocrinol. Metab. 99 (2014), E1–E8.
35. Pearce, E.N., Andersson, M., Zimmermann, M.B., Global iodine nutrition: where do we stand in 2013?. Thyroid 23 (2013), 523–528.
36. Pharoah, P.O., Buttfield, I.H., Hetzel, B.S., Neurological damage to the fetus resulting from severe iodine deficiency during pregnancy. Lancet 1 (1971), 308–310.
37. Pop, V.J., Kuijpens, J.L., van Baar, A.L., Verkerk, G., van Son, M.M., de Vijlder, J.J., Vulsma, T., Wiersinga, W.M., Drexhage, H.A., Vader, H.L., Low maternal free thyroxine concentrations during early pregnancy are associated with impaired psychomotor development in infancy. Clin. Endocrinol. (Oxf.) 50 (1999), 149–155.
38. 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. (Oxf.) 59 (2003), 282–288.
39. Qiu, D., Tan, L.H., Zhou, K., Khong, P.L., Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development. Neuroimage 41 (2008), 223–232.
40. Silk, T.J., Vance, A., Rinehart, N., Bradshaw, J.L., Cunnington, R., White-matter abnormalities in attention deficit hyperactivity disorder: a diffusion tensor imaging study. Hum. Brain Mapp. 30 (2009), 2757–2765.
41. Smit, B.J., Kok, J.H., Vulsma, T., Briët, J.M., Boer, K., Wiersinga, W.M., Neurologic development of the newborn and young child in relation to maternal thyroid function. Acta Paediatr. 89 (2000), 291–295.
42. Spielberger, C.D., Gorsuch, R.L., Lushene, R.E., Vagg, P.R., Jacobs, G.A., Manual for the State-Trait Anxiety Inventory. 1983, Consulting Psychologists Press, California.
43. Tromp, M.J., van Eijsden, M., Ravelli, A.C., Bonsel, G.J., Anonymous non-response analysis in the ABCD cohort study enabled by probabilistic record linkage. Pediatr. Perinat. Epidemiol. 23 (2009), 264–272.
44. Vermiglio, F., Lo Presti, V.P., Moleti, M., Sidoti, M., Tortorella, G., Scaffidi, G., Castagna, M.G., Mattina, F., Violi, M.A., Crisà, A., Artemisia, A., Trimarchi, F., 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. 89 (2004), 6054–6060.
45. Wahlhovd, K.B., Fjell, A.M., White matter volume predicts reaction time instability. Neuropsychologia 45 (2007), 2277–2284.
46. d'Andrea, I., Fardella, V., Fardella, S., Pallante, F., Ghigo, A., Iacobucci, R., Maffei, A., Hirsch, E., Lembo, G., Carnevale, D., Lack of kinase-independent activity of PI3K(in locus coeruleus induces ADHD symptoms through increased CREB signaling. EMBO Mol. Med. 16 (2015), 904–917.
47. van Eijsden, M., Vrijkotte, T.G., Gemke, R.J., van der Wal, M.F., Cohort profile: the Amsterdam born children and their development (ABCD) study. Int. J. Epidemiol. 40 (2011), 1176–1186.
48. van Wassenaer, A.G., Kok, J.H., Dekker, F.W., de Vijlder, J.J., Thyroid function in very preterm infants: influences of gestational age and disease. Pediatr. Res. 42 (1997), 604–609.