Skip to main content

Advertisement

Log in

Maternal prenatal thyroid function and trajectories of offspring emotional and behavioural problems: findings from the ALSPAC cohort

  • Original Contribution
  • Published:
European Child & Adolescent Psychiatry Aims and scope Submit manuscript

Abstract

Maternal thyroid hormone may have impact on fetal brain development and consequently lead to offspring mental health problems. This study examined the role of maternal prenatal thyroid function on trajectories of offspring emotional and behavioural problems. Data were taken from the Avon Longitudinal Study of Parents and Children. A total of 4839 mother–child pairs were included. Thyroid-stimulating hormone (TSH) levels, free thyroxine (FT4), and thyroid peroxidase antibodies (TPO-Ab) were assessed during the first trimester of pregnancy. Childhood emotional and behavioural problems were assessed using the Strengths and difficulties questionnaire. A group-based modelling approach was used to identify the different trajectories of offspring emotional and behavioural problems reported by parents over four waves of measurement at age 3.5 (42 months), 6.75 (81 months), 9 and 11 years. Multinomial logistic regression was then used to test for an association between hormone levels and class membership. We identified four trajectories of offspring emotional and behavioural problems; normative-decreasing (49.7%), moderate-decreasing (35.7%), moderate-static (8.4%), and high-decreasing (6.2%) trajectory. There were no significant differences in the mean values of mother’s FT4, TSH, and the proportion of mothers with positive TPO-Ab between trajectories. Univariable and multivariable multinomial logistic models showed no association between maternal thyroid function (FT4, TSH, and TPO-Ab) and the trajectories of offspring emotional and behavioural problems. The results of our study show that maternal thyroid parameters in a community population are not associated with trajectories of offspring emotional and behavioural problems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1

Similar content being viewed by others

References

  1. Erskine HE, Moffitt TE, Copeland WE, Costello EJ, Ferrari AJ, Patton G, Degenhardt L, Vos T, Whiteford HA, Scott JG (2015) A heavy burden on young minds: the global burden of mental and substance use disorders in children and youth. Psychol Med 45(7):1551–1563. https://doi.org/10.1017/s0033291714002888

    Article  CAS  PubMed  Google Scholar 

  2. Scott JG, Tunbridge M, Stathis S (2018) The Aggressive Child. J Paediatr Child Health 54(10):1165–1169. https://doi.org/10.1111/jpc.14182

    Article  PubMed  Google Scholar 

  3. McGovern CW, Sigman M (2005) Continuity and change from early childhood to adolescence in autism. J Child Psychol Psychiatry 46(4):401–408. https://doi.org/10.1111/j.1469-7610.2004.00361.x

    Article  PubMed  Google Scholar 

  4. Daelmans B, Darmstadt GL, Lombardi J, Black MM, Britto PR, Lye S, Dua T, Bhutta ZA, Richter LM (2016) Early childhood development: the foundation of sustainable development. The Lancet 389(10064):9–11. https://doi.org/10.1016/S0140-6736(16)31659-2

    Article  Google Scholar 

  5. Fetene DM, Betts KS, Alati R (2017) Mechanisms in endocrinology: maternal thyroid dysfunction during pregnancy and behavioural and psychiatric disorders of children: a systematic review. Eur J Endocrinol 177(5):R261–R273

    Article  CAS  Google Scholar 

  6. Ghassabian A, Bongers-Schokking JJ, De Rijke YB, Van Mil N, Jaddoe VWV, De Muinck Keizer-Schrama SMPF, Hooijkaas H, Hofman A, Visser W, Roman GC, Visser TJ, Verhulst FC, Tiemeier H (2012) Maternal thyroid autoimmunity during pregnancy and the risk of attention deficit/hyperactivity problems in children: the generation r study. Thyroid 22(2):178–186

    Article  CAS  Google Scholar 

  7. Haddow JE, Palomaki GE, Allan WC, Williams JR, Knight GJ, Gagnon J, O'Heir CE, Mitchell ML, Hermos RJ, Waisbren SE, Faix JD, Klein RZ (1999) Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N Engl J Med 341(8):549–555. https://doi.org/10.1056/NEJM199908193410801

    Article  CAS  PubMed  Google Scholar 

  8. Stenzel D, Huttner WB (2013) Role of maternal thyroid hormones in the developing neocortex and during human evolution. Front Neuroanatomy 7:19. https://doi.org/10.3389/fnana.2013.00019

    Article  Google Scholar 

  9. Bernal J (2000) Thyroid Hormones in Brain Development and Function. Endotext [Internet]. MDText.com, Inc., South Dartmouth (MA)

  10. Auso E, Lavado-Autric R, Cuevas E, Del Rey FE, Morreale De Escobar G, Berbel P (2004) A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 145(9):4037–4047. https://doi.org/10.1210/en.2004-0274

    Article  CAS  PubMed  Google Scholar 

  11. Lavado-Autric R, Ausó E, García-Velasco JV, del Carmen Arufe M, Escobar del Rey F, Berbel P, Morreale de Escobar G (2003) Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 111(7):1073–1082. https://doi.org/10.1172/JCI200316262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ghassabian A, Bongers-Schokking JJ, Henrichs J, Jaddoe VW, Visser TJ, Visser W, de Muinck Keizer-Schrama SM, Hooijkaas H, Steegers EA, Hofman A, Verhulst FC, van der Ende J, de Rijke YB, Tiemeier H (2011) Maternal thyroid function during pregnancy and behavioral problems in the offspring: the generation R study. Pediatr Res 69(5 Pt 1):454–459. https://doi.org/10.1203/PDR.0b013e3182125b0c

    Article  CAS  PubMed  Google Scholar 

  13. Päkkilä F, Männistö T, Pouta A, Hartikainen AL, Ruokonen A, Surcel HM, Bloigu A, Vääräsmäki M, Järvelin MR, Moilanen I, Suvanto E (2014) The impact of gestational thyroid hormone concentrations on ADHD symptoms of the child. J Clin Endocrinol Metab 99(1):E1–E8

    Article  Google Scholar 

  14. Nelson SM, Haig C, McConnachie A, Sattar N, Ring SM, Smith GD, Lawlor DA, Lindsay RS (2018) Maternal thyroid function and child educational attainment: prospective cohort study. The BMJ 360:k452. https://doi.org/10.1136/bmj.k452

    Article  PubMed  PubMed Central  Google Scholar 

  15. Chevrier J, Harley KG, 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. J Thyroid Res 2011:426427. https://doi.org/10.4061/2011/426427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Boyd A, Golding J, Macleod J, Lawlor DA, Fraser A, Henderson J, Molloy L, Ness A, Ring S, Davey Smith G (2013) Cohort profile: the 'children of the 90s'–the index offspring of the avon longitudinal study of parents and children. Int J Epidemiol 42(1):111–127. https://doi.org/10.1093/ije/dys064

    Article  PubMed  Google Scholar 

  17. Fraser A, Macdonald-Wallis C, Tilling K, Boyd A, Golding J, Davey Smith G, Henderson J, Macleod J, Molloy L, Ness A, Ring S, Nelson SM, Lawlor DA (2013) Cohort profile: the avon longitudinal study of parents and children: alspac mothers cohort. Int J Epidemiol 42(1):97–110. https://doi.org/10.1093/ije/dys066

    Article  PubMed  Google Scholar 

  18. Whyte S, Campbell A (2008) The strengths and difficulties questionnaire: a useful screening tool to identify mental health strengths and needs in looked after children and inform care plans at looked after children reviews? Child Care Practice 14(2):193–206. https://doi.org/10.1080/13575270701868868

    Article  Google Scholar 

  19. Posserud MB, Ullebo AK, Plessen KJ, Stormark KM, Gillberg C, Lundervold AJ (2014) Influence of assessment instrument on ADHD diagnosis. Eur Child Adolesc Psychiatry 23(4):197–205. https://doi.org/10.1007/s00787-013-0442-6

    Article  PubMed  Google Scholar 

  20. Rogers I, Emmett P (1998) Diet during pregnancy in a population of pregnant women in South West England. ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. Eur J Clin Nutr 52 (4):246–250

  21. Taylor CM, Hays NP, Emmett PM (2019) Diet at age 10 and 13 years in children identified as picky eaters at age 3 years and in children who are persistent picky eaters in a longitudinal birth cohort study. Nutrients. 10.3390/nu11040807

  22. Rogers I, Emmett P (2003) The effect of maternal smoking status, educational level and age on food and nutrient intakes in preschool children: results from the avon longitudinal study of parents and children. Eur J Clin Nutr 57:854. https://doi.org/10.1038/sj.ejcn.1601619

    Article  CAS  PubMed  Google Scholar 

  23. Jones BL, Nagin DS (2012) A Stata Plugin for Estimating Group-Based Trajectory Models. https://pdfs.semanticscholar.org/fc51/d4ff61909fa893edbf6ee5da32ac48fdc430.pdf.

  24. Tearne JE, Allen KL, Herbison CE, Lawrence D, Whitehouse AJ, Sawyer MG, Robinson M (2015) The association between prenatal environment and children's mental health trajectories from 2 to 14 years. Eur Child Adolesc Psychiatry 24(9):1015–1024. https://doi.org/10.1007/s00787-014-0651-7

    Article  PubMed  Google Scholar 

  25. Nagin DS, Odgers CL (2010) Group-based trajectory modeling in clinical research. Ann Rev Clin Psychol 6:109–138

    Article  Google Scholar 

  26. Andersen SL, Laurberg P, Wu CS, Olsen J (2014) Attention deficit hyperactivity disorder and autism spectrum disorder in children born to mothers with thyroid dysfunction: a Danish nationwide cohort study. BJOG 121(11):1365–1374. https://doi.org/10.1111/1471-0528.12681

    Article  CAS  PubMed  Google Scholar 

  27. Brown AS, Surcel HM, 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. Prog Neuropsychopharmacol Biol Psychiatry 57:86–92

    Article  CAS  Google Scholar 

  28. Modesto T, Tiemeier H, Peeters RP, Jaddoe VW, Hofman A, Verhulst FC, Ghassabian A (2015) Maternal mild thyroid hormone insufficiency in early pregnancy and attention-deficit/hyperactivity disorder symptoms in children. JAMA Pediatrics 169(9):838–845. https://doi.org/10.1001/jamapediatrics.2015.0498

    Article  PubMed  Google Scholar 

  29. Endendijk JJ, Wijnen HAA, Pop VJM, van Baar AL (2017) Maternal thyroid hormone trajectories during pregnancy and child behavioral problems. Horm Behav 94:84–92. https://doi.org/10.1016/j.yhbeh.2017.06.007

    Article  CAS  PubMed  Google Scholar 

  30. Minatoya M, Itoh S, Araki A, Tamura N, Yamazaki K, Nishihara S, Miyashita C, Kishi R (2017) Associated factors of behavioural problems in children at preschool age: the Hokkaido study on environment and children's health. Child: care, health and development 43 (3):385–392. doi:10.1111/cch.12424

  31. Rees S, Channon S, Waters CS (2018) The impact of maternal prenatal and postnatal anxiety on children’s emotional problems: a systematic review. Eur Child Adolesc Psychiatry. https://doi.org/10.1007/s00787-018-1173-5

    Article  PubMed  PubMed Central  Google Scholar 

  32. Taskforce The American Thyroid Association, on Thyroid Disease During P, Postpartum, Stagnaro-Green A, Abalovich M, Alexander E, Azizi F, Mestman J, Negro R, Nixon A, Pearce EN, Soldin OP, Sullivan S, 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. https://doi.org/10.1089/thy.2011.0087

  33. Männistö T, Mendola P, Grewal J, Xie Y, Chen Z, Laughon SK (2013) Thyroid diseases and adverse pregnancy outcomes in a contemporary US Cohort. J Clin Endocrinol Metab 98(7):2725–2733. https://doi.org/10.1210/jc.2012-4233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Canning EH (1994) Mental disorders in chronically ill children: case identification and parent-child discrepancy. Psychosom Med 56(2):104–108

    Article  CAS  Google Scholar 

  35. Anderson JJ, Hoath S, Zammit S, Meyer TD, Pell JP, Mackay D, Smith DJ (2016) Gestational influenza and risk of hypomania in young adulthood: prospective birth cohort study. J Affect Disord 200:182–188. https://doi.org/10.1016/j.jad.2016.04.048

    Article  PubMed  PubMed Central  Google Scholar 

  36. Alwan NA, Cade JE, Greenwood DC, Deanfield J, Lawlor DA (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(1):e84684. https://doi.org/10.1371/journal.pone.0084684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Taylor AE, Howe LD, Heron JE, Ware JJ, Hickman M, Munafo MR (2014) Maternal smoking during pregnancy and offspring smoking initiation: assessing the role of intrauterine exposure. Addiction (Abingdon, England) 109(6):1013–1021. https://doi.org/10.1111/add.12514

    Article  Google Scholar 

Download references

Acknowledgements

We are extremely grateful to all the families who took part in this study, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists and nurses.

Funding

ALSPAC is supported by the UK Medical Research Council and Wellcome (Grant Ref: 102215/2/13/2) and the University of Bristol. Thyroxine, thyroid-stimulating hormone and thyroid antibody measurements on ALSPAC maternal pregnancy samples were analysed at the University of Glasgow with funding obtained by Professor Scott Nelson from the Chief Scientific Officer of Scotland (ETM/97). Dagnachew Fetene is supported by the University of Queensland Centennial Scholarship and Research Training program. Kim Betts and Rosa Alati are funded by UQ senior Strategic Development fellowship. James Scott is supported by a National Health and Medical Research Council Practitioner Fellowship Grant APP1105807.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dagnachew Muluye Fetene.

Ethics declarations

Conflict of interest

All authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 221 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fetene, D.M., Betts, K.S., Scott, J.G. et al. Maternal prenatal thyroid function and trajectories of offspring emotional and behavioural problems: findings from the ALSPAC cohort. Eur Child Adolesc Psychiatry 29, 871–879 (2020). https://doi.org/10.1007/s00787-019-01404-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00787-019-01404-7

Keywords

Navigation