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Prenatal exposure to very severe maternal obesity is associated with adverse neuropsychiatric outcomes in children

Published online by Cambridge University Press:  25 October 2016

T. H. Mina ,
M. Lahti ,
A. J. Drake ,
K. Räikkönen ,
H. Minnis ,
F. C. Denison ,
J. E. Norman  and
R. M. Reynolds
T. H. Mina
Affiliation:
University BHF Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK Tommy's Centre for Maternal and Fetal Health, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK
M. Lahti
Affiliation:
University BHF Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland
A. J. Drake
Affiliation:
University BHF Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK
K. Räikkönen
Affiliation:
Institute of Behavioural Sciences, University of Helsinki, Helsinki, Finland
H. Minnis
Affiliation:
Institute of Health and Wellbeing, University of Glasgow, Glasgow, Scotland, UK
F. C. Denison
Affiliation:
Tommy's Centre for Maternal and Fetal Health, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK MRC Centre for Reproductive Health, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK
J. E. Norman
Affiliation:
Tommy's Centre for Maternal and Fetal Health, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK MRC Centre for Reproductive Health, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK
R. M. Reynolds*
Affiliation:
University BHF Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK Tommy's Centre for Maternal and Fetal Health, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, Scotland, UK
*
*Address for correspondence: Professor R. M. Reynolds, University BHF Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, 47 Little France, Edinburgh EH16 4TJ, Scotland, UK. (Email: r.reynolds@ed.ac.uk)
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Abstract

Background

Prenatal maternal obesity has been linked to adverse childhood neuropsychiatric outcomes, including increased symptoms of attention deficit hyperactivity disorder (ADHD), internalizing and externalizing problems, affective disorders and neurodevelopmental problems but few studies have studied neuropsychiatric outcomes among offspring born to very severely obese women or assessed potential familial confounding by maternal psychological distress.

Method

We evaluated neuropsychiatric symptoms in 112 children aged 3–5 years whose mothers had participated in a longitudinal study of obesity in pregnancy (50 very severe obesity, BMI ⩾40 kg/m2, obese class III and 62 lean, BMI 18.5–25 kg/m2). The mothers completed the Conners’ Hyperactivity Scale, Early Symptomatic Syndrome Eliciting Neurodevelopmental Clinical Examination Questionnaire (ESSENCE-Q), Child's Sleep Habits Questionnaire (CSHQ), Strengths and Difficulties Questionnaire (SDQ), and Child Behavior Checklist (CBCL) to assess child neuropsychiatric symptoms. Covariates included child's sex, age, birthweight, gestational age, socioeconomic deprivation levels, maternal age, parity, smoking status during pregnancy, gestational diabetes and maternal concurrent symptoms of anxiety and depression assessed using State Anxiety of Spielberger State-Trait Anxiety Index (STAI) and General Health Questionnaire (GHQ), respectively.

Results

Children exposed to prenatal maternal very severe obesity had significantly higher scores in the Conners’ Hyperactivity Scale; ESSENCE-Q; total sleep problems in CSHQ; hyperactivity, conduct problems and total difficulties scales of the SDQ; higher externalizing and total problems, anxious/depressed, aggressive behaviour and other problem syndrome scores and higher DSM-oriented affective, anxiety and ADHD problems in CBCL. Prenatal maternal very severe obesity remained a significant predictor of child neuropsychiatric problems across multiple scales independent of demographic factors, prenatal factors and maternal concurrent symptoms of anxiety and depression.

Conclusions

Prenatal maternal very severe obesity is a strong predictor of increased neuropsychiatric problems in early childhood.

Keywords

Affectiveattention deficitexternalizinghyperactivityneurodevelopmentalobesityprenatalsleep
Type
Original Articles
Information
Psychological Medicine , Volume 47 , Issue 2 , January 2017 , pp. 353 - 362
Copyright
Copyright © Cambridge University Press 2016 

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References

Achenbach, TM, Rescorla, LA (2000). Manual for the ASEBA Preschool Forms & Profiles: An Integrated System of Multi-informant Assessment. Burlington, VT: University of Vermont, Research Center for Children, Youth & Families.Google Scholar
Antoniou, EE, Fowler, T, Reed, K, Southwood, TR, McCleery, JP, Zeegers, MP (2014). Maternal pre-pregnancy weight and externalising behaviour problems in preschool children: a UK-based twin study. BMJ Open 4, e005974.CrossRefGoogle ScholarPubMed
Atladottir, HO, Gyllenberg, D, Langridge, A, Sandin, S, Hansen, SN, Leonard, H, Gissle, M, Reichenberg, A, Schendel, DE, Bourke, J, Hultman, CM, Grice, DE, Buxbaum, JD, Parner, ET (2015). The increasing prevalence of reported diagnoses of childhood psychiatric disorders: a descriptive multinational comparison. European Child & Adolescent Psychiatry 24, 173–183.CrossRefGoogle ScholarPubMed
Bilbo, S, Schwarz, J (2012). The immune system and developmental programming of brain and behavior. Frontiers in Neuroendocrinology 33, 267–286.CrossRefGoogle ScholarPubMed
Boyle, CA, Boulet, S, Schieve, LA, Cohen, RA, Blumberg, SJ, Yeargin-Allsopp, M, Visser, S, Kogan, MD (2011). Trends in the prevalence of developmental disabilities in US children, 1997–2008. Pediatrics 127, 1034–1042.CrossRefGoogle ScholarPubMed
Brion, MJ, Zeegers, M, Jaddoe, V, Verhulst, F, Tiemeier, H, Lawlor, DA, Smith, GD (2011). Intrauterine effects of maternal prepregnancy overweight on child cognition and behavior in 2 cohorts. Pediatrics 127, e202–e211.CrossRefGoogle ScholarPubMed
Brown, AS, Sourander, A, Hinkka-Yli-Salomaki, S, McKeague, IW, Sundvall, J, Surcel, HM (2014). Elevated maternal C-reactive protein and autism in a national birth cohort. Molecular Psychiatry 19, 259–264.CrossRefGoogle Scholar
Buescher, AVS, Cidav, Z, Knapp, M, Mandell, DS (2014). Costs of autism spectrum disorders in the United Kingdom and the United States. JAMA Pediatrics 168, 721–728.CrossRefGoogle ScholarPubMed
Buss, C, Entringer, S, Davis, EP, Hobel, CJ, Swanson, JM, Wadhwa, PD, Sandman, CA (2012). Impaired executive function mediates the association between maternal pre-pregnancy body mass index and child ADHD symptoms. PLoS ONE 7, e37758.CrossRefGoogle ScholarPubMed
Caspi, A, Moffitt, TE, Newman, DL, Silva, PA (1996). Behavioral observations at age 3 years predict adult psychiatric disorders. Longitudinal evidence from a birth cohort. Archives of General Psychiatry 53, 1033–1039.CrossRefGoogle ScholarPubMed
Chen, Q, Sjolander, A, Langstrom, N, Rodriguez, A, Serlachius, E, D'Onofrio, BM, Lichtenstein, P, Larsson, H (2014). Maternal pre-pregnancy body mass index and offspring attention deficit hyperactivity disorder: a population-based cohort study using a sibling-comparison design. International Journal of Epidemiology 43, 83–90.CrossRefGoogle ScholarPubMed
Chu, S, Kim, S, Bish, C (2009). Prepregnancy obesity prevalence in the United States, 2004–2005. Maternal and Child Health Journal 13, 614–620.CrossRefGoogle ScholarPubMed
Croft, S, Stride, C, Maughan, B, Rowe, R (2015). Validity of the strengths and difficulties questionnaire in preschool-aged children. Pediatrics 135, e1210–e1219.CrossRefGoogle ScholarPubMed
Dunn, G, Morgan, C, Bale, T (2011). Sex-specificity in transgenerational epigenetic programming. Hormones and Behavior 59, 290–295.CrossRefGoogle ScholarPubMed
Erhart, M, Döpfner, M, Ravens-Sieberer, U, Bella Study Group (2008). Psychometric properties of two ADHD questionnaires: comparing the Conners’ scale and the FBB-HKS in the general population of German Children and adolescents–results of the BELLA Study. European Child & Adolescent Psychiatry 17, 106–115.CrossRefGoogle ScholarPubMed
Fisher, SC, Kim, SY, Sharma, AJ, Rochat, R, Morrow, B (2013). Is obesity still increasing among pregnant women? Prepregnancy obesity trends in 20 states, 2003–2009. Preventive Medicine 56, 372–378.CrossRefGoogle ScholarPubMed
Gardner, RM, Lee, BK, Magnusson, C, Rai, D, Frisell, T, Karlsson, H, Idring, S, Dalman, C (2015). Maternal body mass index during early pregnancy, gestational weight gain, and risk of autism spectrum disorders: results from a Swedish total population and discordant sibling study. International Journal of Epidemiology 44, 870–883.CrossRefGoogle ScholarPubMed
Gillberg, C (2010). The ESSENCE in child psychiatry: early symptomatic syndromes eliciting neurodevelopmental clinical examinations. Research in Developmental Disabilities 31, 1543–1551.CrossRefGoogle ScholarPubMed
Goodlin-jones, BL, Sitnick, SL, Tang, K, Liu, Jy, Anders, TF (2008). The children's sleep habits questionnaire in toddlers and preschool children. Journal of Developmental and Behavioural Pediatrics 29, 82–88.CrossRefGoogle ScholarPubMed
Goodman, R (1997). The strengths and difficulties questionnaire: a research note. Journal of Child Psychology and Psychiatry, and Allied Disciplines 38, 581–586.CrossRefGoogle ScholarPubMed
Goodman, SH, Rouse, MH, Connell, AM, Broth, MR, Hall, CM, Heyward, D (2011). Maternal depression and child psychopathology: a meta-analytic review. Clinical Child and Family Psychology Review 14, 1–27.CrossRefGoogle ScholarPubMed
Heinrich, A, Buchmann, AF, Zohsel, K, Dukal, H, Frank, J, Treutlein, J, Nieratschker, V, Witt, SH, Brandeis, D, Schmidt, MH, Esser, G, Banaschewski, T, Laucht, M, Rietschel, M (2015). Alterations of glucocorticoid receptor gene methylation in externalizing disorders during childhood and adolescence. Behavioural Genetics 45, 529–536.CrossRefGoogle ScholarPubMed
Heslehurst, N, Rankin, J, Wilkinson, JR, Summerbell, CD (2010). A nationally representative study of maternal obesity in England, UK: trends in incidence and demographic inequalities in 619 323 Births, 1989–2007. International Journal of Obesity, 34, 420–428.CrossRefGoogle ScholarPubMed
Jo, Hj, Schieve, LA, Sharma, AJ, Hinkle, SN, Li, Rw, Lind, JN (2015). Maternal prepregnancy body mass index and child psychosocial development at 6 years of age. Pediatrics 135, e1198–e1209.CrossRefGoogle ScholarPubMed
Krakowiak, P, Walker, CK, Bremer, AA, Baker, AS, Ozonoff, S, Hansen, RL, Hertz-Picciotto, I (2012). Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders. Pediatrics 129, e1121–e1128.CrossRefGoogle ScholarPubMed
Le, HH, Hodgkins, P, Postma, MJ, Kahle, J, Sikirica, V, Setyawan, J, Erder, MH (2014). Economic impact of childhood/adolescent ADHD in a European setting: the Netherlands as a reference case. European Child & Adolescent Psychiatry 23, 587–598.CrossRefGoogle Scholar
Li, YM, Ou, JJ, Liu, L, Zhang, D, Zhao, JP, Tang, SY (2015). Association between maternal obesity and autism spectrum disorder in offspring: a meta-analysis. Journal of Autism and Developmental Disorders 46, 95–102.CrossRefGoogle Scholar
Lovejoy, MC, Graczyk, PA, O'Hare, E, Neuman, G (2000). Maternal depression and parenting behavior: a meta-analytic review. Clinical Psychology Reviews 20, 561–592.CrossRefGoogle ScholarPubMed
Madigan, S, Brumario, LE, Villani, V, Atkinson, L, Lyons-Ruth, K (2016). Representational and questionnaire measures of attachment: a meta-analysis of relations to child internalizing and externalizing problems. Psychological Bulletin 142, 367–299.CrossRefGoogle ScholarPubMed
McLoone, P (2004). Carstairs Scores for Scottish Postcode Sectors from the 2001 Census. MRC Social and Public Health Sciences Unit: Glasgow.Google Scholar
Mina, TH, Denison, FC, Forbes, S, Stirrat, LI, Norman, JE, Reynolds, RM (2015). Associations of mood symptoms with ante- and postnatal weight change in obese pregnancy are not mediated by cortisol. Psychological Medicine 45, 133–146.CrossRefGoogle Scholar
Molyneaux, E, Poston, L, Ashurst-Williams, S, Howard, LM (2014). Obesity and mental disorders during pregnancy and postpartum. Obstetrics & Gynecology 123, 857–867.CrossRefGoogle ScholarPubMed
Norman, JE, Reynolds, RM (2011). The consequences of obesity and excess weight gain in pregnancy. The Proceedings of the Nutrition Society 70, 450–456.CrossRefGoogle ScholarPubMed
Parade, SH, Ridout, KK, Seifer, R, Armstrong, DA, Marsit, CJ, McWilliams, MA, Tyrka, AR (2016). Methylation of the glucocorticoid receptor gene promoter in preschoolers: links with internalizing behaviour problems. Child Development 87, 86–97.CrossRefGoogle Scholar
Pihlakoski, L, Sourander, A, Aromaa, M, Rautava, P, Helenius, H, Sillanpää, M (2006). The continuity of psychophatology from early childhood to preadolescence: a prospective cohort study of 3–12-year-old children. European Child & Adolescent Psychiatry 15, 409–417.CrossRefGoogle Scholar
Polanczyk, GV, Salum, GA, Sugaya, LS, Caye, A, Rohde, LA (2015). Annual research review: a meta-analysis of the worldwife prevalence of mental disorders in children and adolescents. Journal of Child Psychology and Psychiatry 56, 345–365.CrossRefGoogle Scholar
Pugh, SJ, Hutcheon, JA, Richardson, GA, Brooks, MM, Himes, KP, Day, NL, Bodnar, LM (2016). Gestational weight gain, prepregnancy body mass index and offspring attention-deficit hyperactivity disorder symptoms and behaviour at age 10. British Journal of Obstetrics and Gynaecology. Published online: 21 March 2016. doi:10.1111/1471-0528.13909.CrossRefGoogle ScholarPubMed
Räikkönen, K, Pesonen, AK, O'Reilly, JR, Tuovinen, S, Lahti, M, Kajantie, E, Villa, P, Laivuori, H, Hämäläinen, E, Seckl, JR, Reynolds, RM (2015). Maternal depressive symptoms during pregnancy, placental expression of genes regulating glucocorticoid and serotonin function and infant regulatory behaviors. Psychological Medicine 45, 3217–3226.CrossRefGoogle ScholarPubMed
Reising, MM, Watson, KH, Hardcastle, EJ, Merchant, MJ, Roberts, L, Forehand, R, Compas, BE (2013). Parental depression and economic disadvantage: the role of parenting in associations with internalising and externalising symptoms in children and adolescents. Journal of Child and Family Studies 22, 335–343.CrossRefGoogle Scholar
Rescorla, LA, Achenbach, TM, Ivanova, MY, Harder, VS, Otten, L, Bilenberg, N, Bjarnadottir, G, Capron, C, De Pauw, SS, Dias, P, Dobrean, A (2011). International comparisons of behavioral and emotional problems in preschool children: parents’ reports from 24 societies. Journal of Clinical Child & Adolescent Psychology 40, 456–467.CrossRefGoogle ScholarPubMed
Reynolds, RM, Allan, KM, Raja, EA, Bhattacharya, S, McNeill, G, Hannaford, PC, Sarwar, N, Lee, AJ, Norman, JE (2013). Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 Person Years. BMJ (Clinical research ed.) 347, (August). f4539.Google ScholarPubMed
Robinson, M, Zubrick, SR, Pennell, CE, Van Lieshout, RJ, Jacoby, P, Beilin, LJ, Mori, TA, Stanley, FJ, Newnham, JP, Oddy, WH (2013). Pre-pregnancy maternal overweight and obesity increase the risk for affective disorders in offspring. Journal of Developmental Origins of Health and Disease 4, 1–7.CrossRefGoogle ScholarPubMed
Rodriguez, A (2010). Maternal pre-pregnancy obesity and risk for inattention and negative emotionality in children. Journal of Child Psychology and Psychiatry and Allied Disciplines 51, 134–143.CrossRefGoogle ScholarPubMed
Rodriguez, A, Miettunen, J, Henriksen, TB, Olsen, J, Obel, C, Taanila, A, Ebeling, H, Linnet, KM, Moilanen, I, Järvelin, MR (2008). Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts. International Journal of Obesity 32, 550–557.CrossRefGoogle ScholarPubMed
Simpkin, CT, Jenni, OG, Carskadon, MA, Wright, KP Jr., Akacem, LD, Garlo, KG, Lebourgeois, MK (2014). Chronotype is associated with the timing of the circadian clock and sleep in toddlers. Journal of Sleep Research 23, 397–405.CrossRefGoogle ScholarPubMed
Van Batenburg-Eddes, T, Brion, MJ, Henrichs, J, Jaddoe, VWV, Hofman, A, Verhulst, FC, Lawlor, DA, Davey Smith, G, Tiemeier, H (2013). Parental depressive and anxiety symptoms during pregnancy and attention problems in children: a cross-cohort consistency study. Journal of Child Psychology and Psychiatry 54, 591–600.CrossRefGoogle ScholarPubMed
Van den Bergh, BRH, Mennes, M, Oosterlaan, J, Stevens, V, Stiers, P, Marcoen, A, Lagae, L (2005). High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neuroscience and Biobehavioral Reviews 29, 259–269.CrossRefGoogle ScholarPubMed
van der Heijden, K, de Sonneville, L, Swaab, H (2013). Association of eveningness with problem behavior in children: a mediating role of impaired sleep. Chronobiology International 30, 919–929.CrossRefGoogle ScholarPubMed
van Lieshout, RJ, Schmidt, LA, Robinson, M, Niccols, A, Boyle, MH (2013). Maternal pre-pregnancy body mass index and offspring temperament and behavior at 1 and 2 years of age. Child Psychiatry and Human Development 44, 382–390.CrossRefGoogle Scholar
Yap, M, Jorm, A. (2015). Parental factors associated with childhood anxiety, depression, and internalizing problems: a systematic review and meta-analysis. Journal of Affective Disorders 1, 424–440.CrossRefGoogle Scholar
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