Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-19T19:51:14.516Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of maternal prenatal thyroid function on offspring depression: Findings from the ALSPAC cohort

Published online by Cambridge University Press:  28 January 2019

Dagnachew Muluye Fetene Open the ORCID record for Dagnachew Muluye Fetene [Opens in a new window] ,
Kim S. Betts  and
Rosa Alati
Dagnachew Muluye Fetene*
Affiliation:
Institute for Social Science Research, University of Queensland, Brisbane, Australia College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia School of Public Health, University of Queensland, Brisbane, Australia
Kim S. Betts
Affiliation:
Institute for Social Science Research, University of Queensland, Brisbane, Australia
Rosa Alati
Affiliation:
Institute for Social Science Research, University of Queensland, Brisbane, Australia
*
Author for correspondence: Dagnachew Muluye Fetene, Institute for Social Science Research, The University of Queensland, Level 2, Dianella Building (1021), 80 Meiers Rd, Indooroopilly QLD 4068, Australia. E-mail: dagnachew.fetene@uqconnect.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Maternal thyroid dysfunction during pregnancy may contribute to offspring neurobehavioral disorders. In this paper, we investigate the relationship between maternal thyroid function during pregnancy and offspring depression and anxiety. Data were taken from the Avon Longitudinal Study of Parents and Children. A total of 2,920 mother-child pairs were included. Thyroid-stimulating hormone levels, free thyroxine (FT4), and thyroid peroxidase antibodies were assessed during the first trimester of pregnancy because maternal supply is the only source of thyroid hormone for the fetus during the first 12 weeks of gestation. Child symptoms of depression and anxiety were assessed using the Development and Well-Being Assessment at ages 7.5 and 15 years. The odds of presenting with depression and anxiety were estimated using the generalized estimating equation. The level of FT4 during the first trimester of pregnancy was associated with child depression combined at ages 7.5 and 15 (odds ratio = 1.21, 95% confidence interval [1.00, 1.14]. An increase of 1 standard deviation of FT4 during pregnancy increased the odds of child depression by 28% after adjustment made for potential confounders. No association was found among maternal levels of thyroid-stimulating hormone, FT4, and thyroid peroxidase antibodies and childhood anxiety. In conclusion, increased levels of FT4 during the first trimester of pregnancy appear be linked to greater risk of offspring depression.

Keywords

ALSPACdepressionoffspringpregnancythyroid function
Type
Regular Articles
Information
Development and Psychopathology , Volume 32 , Issue 1 , February 2020 , pp. 189 - 196
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, E. K., Pearce, E. N., Brent, G. A., Brown, R. S., Chen, H., Dosiou, C., … Sullivan, S. (2017). 2017 Guidelines of the American Thyroid Association for the Diagnosis and Management of Thyroid Disease During Pregnancy and the Postpartum. Thyroid, 27, 315–389. doi:10.1089/thy.2016.0457CrossRefGoogle ScholarPubMed
Alwan, N. A., Cade, J. E., Greenwood, D. C., Deanfield, J., & Lawlor, D. A. (2014). Associations of maternal iron intake and hemoglobin in pregnancy with offspring vascular phenotypes and adiposity at age 10: Findings from the Avon Longitudinal Study of Parents and Children. PLOS ONE, 9, e84684. doi:10.1371/journal.pone.0084684CrossRefGoogle ScholarPubMed
Andersen, S. L., Olsen, J., Wu, C. S., & Laurberg, P. (2014). Psychiatric disease in late adolescence and young adulthood. Foetal programming by maternal hypothyroidism? Clinical Endocrinology (Oxford), 81, 126–133. doi:10.1111/cen.12415CrossRefGoogle Scholar
Anderson, J. J., Hoath, S., Zammit, S., Meyer, T. D., Pell, J. P., Mackay, D., & Smith, D. J. (2016). Gestational influenza and risk of hypomania in young adulthood: Prospective birth cohort study. Journal of Affective Disorders, 200, 182–188. doi:10.1016/j.jad.2016.04.048CrossRefGoogle ScholarPubMed
Bale, T. L., Baram, T. Z., Brown, A. S., Goldstein, J. M., Insel, T. R., McCarthy, M. M., … Nestler, E. J. (2010). Early life programming and neurodevelopmental disorders. Biological Psychiatry, 68, 314–319. doi:10.1016/j.biopsych.2010.05.028CrossRefGoogle ScholarPubMed
Balucan, F. S., Morshed, S. A., & Davies, T. F. (2013). Thyroid autoantibodies in pregnancy: Their role, regulation and clinical relevance. Journal of Thyroid Research, 2013, 182472. doi:10.1155/2013/182472CrossRefGoogle ScholarPubMed
Bauer, M., Heinz, A., & Whybrow, P. C. (2002). Thyroid hormones, serotonin and mood: Of synergy and significance in the adult brain. Molecular Psychiatry, 7, 140. doi:10.1038/sj.mp.4000963CrossRefGoogle ScholarPubMed
Bernal, J. (2000). Thyroid hormones in brain development and function. In De Groot, L. J., Chrousos, G., Dungan, K., et al. (Eds.), Endotext. South Dartmouth, MA: MDText.com, Inc. Retrieved December 19, 2018, from https://www.ncbi.nlm.nih.gov/books/NBK285549/?report=classicGoogle Scholar
Boyd, A., Golding, J., Macleod, J., Lawlor, D. A., Fraser, A., Henderson, J., … Davey Smith, G. (2013). Cohort profile: The ‘children of the 90s’–the index offspring of the Avon Longitudinal Study of Parents and Children. International Journal of Epidemiology, 42, 111–127. doi:10.1093/ije/dys064CrossRefGoogle ScholarPubMed
Brent, G. A. (2012). The debate over thyroid-function screening in pregnancy. New England Journal of Medicine, 366, 562–563. doi:doi:10.1056/NEJMe1112591CrossRefGoogle ScholarPubMed
Brown, A. S., Surcel, H. M., Hinkka-Yli-Salomäki, S., Cheslack-Postava, K., Bao, Y., & Sourander, A. (2015). Maternal thyroid autoantibody and elevated risk of autism in a national birth cohort. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 57, 86–92.CrossRefGoogle Scholar
Brunoni, A. R., Lopes, M., & Fregni, F. (2008). A systematic review and meta-analysis of clinical studies on major depression and BDNF levels: Implications for the role of neuroplasticity in depression. International Journal of Neuropsychopharmacology, 11, 1169–1180. doi:10.1017/s1461145708009309CrossRefGoogle ScholarPubMed
Chevrier, J., Harley, K. G., Kogut, K., Holland, N., Johnson, C., & Eskenazi, B. (2011). Maternal thyroid function during the second half of pregnancy and child neurodevelopment at 6, 12, 24, and 60 months of age. Journal of Thyroid Research, 2011, 426427. doi:10.4061/2011/426427CrossRefGoogle ScholarPubMed
de Escobar, G. M., Obregon, M. J., & del Rey, F. E. (2004). Maternal thyroid hormones early in pregnancy and fetal brain development. Best Practice & Research Clinical Endocrinology & Metabolism, 18, 225–248. doi:10.1016/j.beem.2004.03.012CrossRefGoogle ScholarPubMed
Dowling, A. L., Martz, G. U., Leonard, J. L., & Zoeller, R. T. (2000). Acute changes in maternal thyroid hormone induce rapid and transient changes in gene expression in fetal rat brain. Journal of Neuroscience, 20, 2255–2265.CrossRefGoogle ScholarPubMed
Foland-Ross, L. C., Sacchet, M. D., Prasad, G., Gilbert, B., Thompson, P. M., & Gotlib, I. H. (2015). Cortical thickness predicts the first onset of major depression in adolescence. International Journal of Developmental Neuroscience, 46, 125–131. doi:10.1016/j.ijdevneu.2015.07.007CrossRefGoogle ScholarPubMed
Ford, T., Goodman, R., & Meltzer, H. (2003). The British Child and Adolescent Mental Health Survey 1999: The prevalence of DSM-IV disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 42, 1203–1211. doi:10.1097/00004583-200310000-00011CrossRefGoogle ScholarPubMed
Fraser, A., Macdonald-Wallis, C., Tilling, K., Boyd, A., Golding, J., Davey Smith, G., … Lawlor, D. A. (2013). Cohort profile: The Avon Longitudinal Study of Parents and Children: ALSPAC mothers cohort. International Journal of Epidemiology, 42, 97–110. doi:10.1093/ije/dys066CrossRefGoogle ScholarPubMed
Fuglestad, A. J., Kroupina, M. G., Johnson, D. E., & Georgieff, M. K. (2016). Micronutrient status and neurodevelopment in internationally adopted children. Acta Paediatrica, 105, e67–e76. doi:10.1111/apa.13234CrossRefGoogle ScholarPubMed
Göbel, A., Heldmann, M., Göttlich, M., Dirk, A.-L., Brabant, G., & Münte, T. F. (2015). Effect of experimental thyrotoxicosis on brain gray matter: A voxel-based morphometry study. European Thyroid Journal, 4(Suppl 1), 113–118. doi:10.1159/000398793CrossRefGoogle ScholarPubMed
Goodman, R., Ford, T., Richards, H., Gatward, R., & Meltzer, H. (2000). The development and well-being assessment: Description and initial validation of an integrated assessment of child and adolescent psychopathology. Journal of Child Psychology and Psychiatry, 41, 645–655.CrossRefGoogle ScholarPubMed
Goodman, A., Heiervang, E., Collishaw, S., & Goodman, R. (2011). The ‘DAWBA bands’ as an ordered-categorical measure of child mental health: Description and validation in British and Norwegian samples. Social Psychiatry and Psychiatric Epidemiology, 46, 521–532. doi:10.1007/s00127-010-0219-xCrossRefGoogle ScholarPubMed
Gyllenberg, D., Sourander, A., Surcel, H. M., Hinkka-Yli-Salomaki, S., McKeague, I. W., & Brown, A. S. (2015). Hypothyroxinemia during gestation and offspring schizophrenia in a national birth cohort. Biological Psychiatry, 79, 962–970. doi:10.1016/j.biopsych.2015.06.014CrossRefGoogle Scholar
James, S. R., Franklyn, J. A., & Kilby, M. D. (2007). Placental transport of thyroid hormone. Best Practice & Research Clinical Endocrinology & Metabolism, 21, 253–264. doi:10.1016/j.beem.2007.03.001CrossRefGoogle ScholarPubMed
Mann, J. J. (2013). The serotonergic system in mood disorders and suicidal behaviour. Philosophical Transactions of the Royal Society B: Biological Sciences, 368, 20120537. doi:10.1098/rstb.2012.0537CrossRefGoogle ScholarPubMed
Männistö, T., Mendola, P., Grewal, J., Xie, Y., Chen, Z., & Laughon, S. K. (2013). Thyroid diseases and adverse pregnancy outcomes in a contemporary US cohort. Journal of Clinical Endocrinology and Metabolism, 98, 2725–2733. doi:10.1210/jc.2012-4233CrossRefGoogle Scholar
McLeod, B. D., Weisz, J. R., & Wood, J. J. (2007). Examining the association between parenting and childhood depression: A meta-analysis. Clinical Psychology Review, 27, 986–1003. doi:https://doi.org/10.1016/j.cpr.2007.03.001CrossRefGoogle ScholarPubMed
Medici, M., Timmermans, S., Visser, W., de Muinck Keizer-Schrama, S. M., Jaddoe, V. W., Hofman, A., … Steegers, E. A. (2013). Maternal thyroid hormone parameters during early pregnancy and birth weight: The Generation R Study. Journal of Clinical Endocrinology and Metabolism, 98, 59–66. doi:10.1210/jc.2012-2420CrossRefGoogle ScholarPubMed
Miao, Q., Zhang, S., Guan, Y. H., Ye, H. Y., Zhang, Z. Y., Zhang, Q. Y., … Li, Y. M. (2011). Reversible changes in brain glucose metabolism following thyroid function normalization in hyperthyroidism. American Journal of Neuroradiology, 32, 1034–1042. doi:10.3174/ajnr.A2449CrossRefGoogle ScholarPubMed
Modesto, T., Tiemeier, H., Peeters, R. P., Jaddoe, V. W., Hofman, A., Verhulst, F. C., & Ghassabian, A. (2015). Maternal mild thyroid hormone insufficiency in early pregnancy and attention-deficit/hyperactivity disorder symptoms in children. JAMA Pediatrics, 169, 838–845. doi:10.1001/jamapediatrics.2015.0498CrossRefGoogle ScholarPubMed
Mohan, V., Sinha, R. A., Pathak, A., Rastogi, L., Kumar, P., Pal, A., & Godbole, M. M. (2012). Maternal thyroid hormone deficiency affects the fetal neocorticogenesis by reducing the proliferating pool, rate of neurogenesis and indirect neurogenesis. Experimental Neurology, 237, 477–488. doi:10.1016/j.expneurol.2012.07.019CrossRefGoogle ScholarPubMed
National Collaborating Centre for Mental Health (UK). (2005). Depression. Depression in children and young people: Identification and management in primary, community and secondary care. NICE Clinical Guidelines, No. 28. Leicester, UK.Google Scholar
Pasquini, M., Berardelli, I., & Biondi, M. (2014). Ethiopathogenesis of depressive disorders. Clinical Practice and Epidemiology in Mental Health: CP & EMH, 10, 166–171. doi:10.2174/1745017901410010166CrossRefGoogle ScholarPubMed
Phillips, J. R., Hewedi, D. H., Eissa, A. M., & Moustafa, A. A. (2015). The cerebellum and psychiatric disorders. Frontiers in Public Health, 3, 66. doi:10.3389/fpubh.2015.00066CrossRefGoogle ScholarPubMed
Roman, G. C., Ghassabian, A., Bongers-Schokking, J. J., Jaddoe, V. W., Hofman, A., de Rijke, Y. B., … Tiemeier, H. (2013). Association of gestational maternal hypothyroxinemia and increased autism risk. Annals of Neurology, 74, 733–742. doi:10.1002/ana.23976CrossRefGoogle ScholarPubMed
Stagnaro-Green, A., Abalovich, M., Alexander, E., Azizi, F., Mestman, J., Negro, R., … Wiersinga, W. (2011). Guidelines of the American Thyroid Association for the Diagnosis and Management of Thyroid Disease During Pregnancy and Postpartum. Thyroid, 21(10), 1081–1125. doi:10.1089/thy.2011.0087CrossRefGoogle ScholarPubMed
Stenzel, D., & Huttner, W. B. (2013). Role of maternal thyroid hormones in the developing neocortex and during human evolution. Frontiers in Neuroanatomy, 7, 19. doi:10.3389/fnana.2013.00019CrossRefGoogle ScholarPubMed
Stenzel, D., Wilsch-Brauninger, M., Wong, F. K., Heuer, H., & Huttner, W. B. (2014). Integrin alphavbeta3 and thyroid hormones promote expansion of progenitors in embryonic neocortex. Development, 141, 795–806. doi:10.1242/dev.101907CrossRefGoogle ScholarPubMed
Stiles, J., & Jernigan, T. L. (2010). The basics of brain development. Neuropsychology Review, 20, 327–348. doi:10.1007/s11065-010-9148-4CrossRefGoogle ScholarPubMed
Taylor, A. E., Howe, L. D., Heron, J. E., Ware, J. J., Hickman, M., & Munafo, M. R. (2014). Maternal smoking during pregnancy and offspring smoking initiation: Assessing the role of intrauterine exposure. Addiction, 109, 1013–1021. doi:10.1111/add.12514CrossRefGoogle ScholarPubMed
van Tol, M. J., van der Wee, N. J., van den Heuvel, O. A., Nielen, M. M., Demenescu, L. R., Aleman, A., … Veltman, D. J. (2010). Regional brain volume in depression and anxiety disorders. Archives of General Psychiatry, 67, 1002–1011. doi:10.1001/archgenpsychiatry.2010.121CrossRefGoogle ScholarPubMed
Wehry, A. M., McNamara, R. K., Adler, C. M., Eliassen, J. C., Croarkin, P., Cerullo, M. A., … Strawn, J. R. (2015). Neurostructural impact of co-occurring anxiety in pediatric patients with major depressive disorder: A voxel-based morphometry study. Journal of Affective Disorders, 171, 54–59. doi:https://doi.org/10.1016/j.jad.2014.09.004CrossRefGoogle ScholarPubMed
Whitehouse, A. J., Holt, B. J., Serralha, M., Holt, P. G., Hart, P. H., & Kusel, M. M. (2013). Maternal vitamin D levels and the autism phenotype among offspring. Journal of Autism and Developmental Disorders, 43, 1495–1504. doi:10.1007/s10803-012-1676-8CrossRefGoogle ScholarPubMed
Whittle, S., Lichter, R., Dennison, M., Vijayakumar, N., Schwartz, O., Byrne, M. L., … Allen, N. B. (2014). Structural brain development and depression onset during adolescence: a prospective longitudinal study. American Journal of Psychiatry, 171, 564–571. doi:10.1176/appi.ajp.2013.13070920CrossRefGoogle ScholarPubMed
Williams, M. D., Harris, R., Dayan, C. M., Evans, J., Gallacher, J., & Ben-Shlomo, Y. (2009). Thyroid function and the natural history of depression: Findings from the Caerphilly Prospective Study (CaPS) and a meta-analysis. Clinical Endocrinology (Oxf), 70, 484–492. doi:10.1111/j.1365-2265.2008.03352.xCrossRefGoogle ScholarPubMed
Yu, D., Zhou, H., Yang, Y., Jiang, Y., Wang, T., Lv, L., … Mao, R. (2015). The bidirectional effects of hypothyroidism and hyperthyroidism on anxiety- and depression-like behaviors in rats. Hormones and Behavior, 69, 106–115. doi:10.1016/j.yhbeh.2015.01.003CrossRefGoogle ScholarPubMed
Zhang, W., Liu, X., Zhang, Y., Song, L., Hou, J., Chen, B., … Lii, H. (2014). Disrupted functional connectivity of the hippocampus in patients with hyperthyroidism: Evidence from resting-state fMRI. European Journal of Radiology, 83, 1907–1913. doi:https://doi.org/10.1016/j.ejrad.2014.07.003CrossRefGoogle ScholarPubMed
Zhang, W., Song, L., Yin, X., Zhang, J., Liu, C., Wang, J., …Lii, H. (2014). Grey matter abnormalities in untreated hyperthyroidism: A voxel-based morphometry study using the DARTEL approach. European Journal of Radiology, 83, e43–e48. doi:10.1016/j.ejrad.2013.09.019CrossRefGoogle ScholarPubMed
Supplementary material: File

Fetene et al. supplementary material

Tables S1 and S2

Download Fetene et al. supplementary material(File)
File 86 KB