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European Child & Adolescent Psychiatry

, Volume 28, Issue 3, pp 377–388 | Cite as

Head circumference and child ADHD symptoms and cognitive functioning: results from a large population-based cohort study

  • Muriel Ferrer
  • Raquel García-Esteban
  • Carmen Iñiguez
  • Olga Costa
  • Ana Fernández-Somoano
  • Cristina Rodríguez-Delhi
  • Jesús Ibarluzea
  • Aitana Lertxundi
  • Cathryn Tonne
  • Jordi Sunyer
  • Jordi JulvezEmail author
Original Contribution
  • 244 Downloads

Abstract

The aim of this study is to understand the association between prenatal, newborn and postnatal head circumference (HC) and preschool neurodevelopment in a large population-based birth cohort. The INMA project followed 1795 children from 12 weeks of pregnancy to preschool years. HC measurements were carried out prospectively, and following a standardized protocol during pregnancy (12, 20 and 34 weeks), birth, and child ages of 1–1.5 and 4 years old; and z-scores were further estimated. Prenatal head growth was assessed using conditional z-scores between weeks 12–20 and 20–34. Several neuropsychological tests [MSCA (cognition), CPT (attention)] and behavioral rating scales [DSM-IV-ADHD, CAST (autism), CPSCS (social competence)] were carried out during the last follow-up (5 years old). Multivariable models adjusted for family and child characteristics were applied to analyze associations between HC and neurodevelopment. In fully adjusted models, prenatal HC and head growth showed little or no associations with the neurodevelopment outcomes. Independent associations were observed between HC z-scores at birth, 1–1.5 years and 4 years and MSCA global cognitive scores and DSM-IV inattention symptoms. Specifically, z-score at birth was positively associated with general cognitive scores [β 1.22, 95% confidence interval (CI) 0.59, 1.85], and we observed a protective association with ADHD-DSM-IV total symptoms, mean ratio (MR) 0.85 (0.75, 0.96). Prenatal HC and head growth measurements gave little information about child cognitive abilities and behavior at preschool years. However, HC at birth and early childhood was positively associated with a range of neuropsychological outcomes, including protective associations with ADHD symptoms.

Keywords

Head circumference, neuropsychological development ADHD symptoms Cohort study 

Abbreviations

ASC

Autism spectrum conditions

ASD

Autism spectrum disorder

BSID

Bayley scales of infant development

CAST

Childhood autism spectrum test

CI

Confidence interval

CPT

Conner’s kiddie continuous performance test

CPSCS

California preschool social competence scale

CBCL

Child behavior check list

DSM-IV-ADHD

Attention-deficit/hyperactivity disorder criteria of the diagnostic and statistical manual of mental disorders, fourth edition form list

ELBW

Extremely low birth weight

FDR

False discovery rate

HC

Head Circumference

INMA

Infancia y medio ambiente [environment and childhood]

SD

Standard deviation

MSCA

McCarthy scales of children’s abilities

MR

Mean ratio

Notes

Acknowledgements

We would like to thank all the participants of the INMA Project for their collaboration as well as the project investigators at each cohort center as well as the coordination centers. A full roster of the INMA Project investigators can be found at http://www.PROYECTOINMA.org/. Wilma Zijlema did English edits in the manuscript.

Funding

Sabadell: This work was supported by grants from the Spanish Ministry of Health [FIS-PI041436]; Instituto de Salud Carlos III [Red INMA G03/176 and CB06/02/0041 and predoctoral grant PFIS 2010, Register FI10/00399]; the Generalitat de Catalunya-CIRIT [1999SGR 00241]; the EU sixth framework project NEWGENERIS [FP6-2003-Food-3-A-016320]; Fundació Roger Torné, and Fundació La Mataró de TV3 (Project No. 090430 & No. 20162210). This study has been funded by Instituto de Salud Carlos III through the projects “CP14/00108 & PI16/00261” (co-funded by European Regional Development Fund “A way to make Europe”). Asturias: This study was funded by grants from Instituto de Salud Carlos III (Red INMA G03/176 and CB06/02/0041), FISS-PI042018, FISS-PI09/02311, FISS-PI1302429, Obra Social Cajastur/Fundación Liberbank and Universidad de Oviedo. Guipuzkoa: This study was funded by grants from Instituto de Salud Carlos III (FIS-PI06/0867 and FIS-PS09/00090), Department of Health of the Basque Government (2005111093 and 2009111069), and the Provincial Government of Gipuzkoa (DFG06/004 and DFG08/001). Valencia: This study was funded by grants from UE (FP7-ENV-2011 cod 282957 and HEALTH.2010.2.4.5-1, Instituto de Salud Carlos III (Red INMA G03/176, CB06/02/0041, FIS-FEDER 03/1615, 04/1509, 04/1112, 04/1931, 05/1079, 05/1052, 06/1213, 07/0314, 09/02647, 11/01007, 11/02591, and CP11/00178), and the Conselleria de Sanitat Generalitat Valenciana; all in Spain. FIS-DENAMIC: PI/11/02038. Jordi Julvez holds a Miguel Servet contract (MS14/00108) awarded by the Spanish Institute of Health Carlos III (Ministry of Economy and Competitiveness). This study was also funded by grants from UE (FP7-ENV-2011 cod 282957 and HEALTH.2010.2.4.5-1), Instituto de Salud Carlos III (Red INMA G03/176, CB06/02/0041, FIS-FEDER 03/1615, 04/1509, 04/1112, 04/1931, 05/1079, 05/1052, 06/1213, 07/0314, 09/02647, 11/01007, 11/02591, 17/00663, and CP11/00178), Alicia Koplowitz Foundation 2017, and the Conselleria de Sanitat Generalitat Valenciana; all in Spain.

Compliance with ethical standards

Conflict of interest

None of the authors have conflicts of interest to disclose. None of the authors have financial relationships relevant to this article to disclose.

Supplementary material

787_2018_1202_MOESM1_ESM.docx (108 kb)
Supplementary material 1 (DOCX 108 kb)

References

  1. 1.
    Walker SP, Thame MM, Chang SM, Bennett F, Forrester TE (2007) Association of growth in utero with cognitive function at age 6–8 years. Early Hum Dev 83(6):355–360PubMedGoogle Scholar
  2. 2.
    Heinonen K, Räikkönen K, Pesonen A-K et al (2008) Prenatal and postnatal growth and cognitive abilities at 56 months of age: a longitudinal study of infants born at term. Pediatrics 121(5):e1325–e1333PubMedGoogle Scholar
  3. 3.
    Harris SR (2015) Measuring head circumference: update on infant microcephaly. Canadian Family Physician Medecin de Famille Canadien 61(8):680–684PubMedPubMedCentralGoogle Scholar
  4. 4.
    Veena SR, Krishnaveni GV, Wills AK et al (2010) Association of birthweight and head circumference at birth to cognitive performance in 9- to 10-year-old children in South India: prospective birth cohort study. Pediatr Res 67(4):424–429PubMedPubMedCentralGoogle Scholar
  5. 5.
    Ivanovic DM, Leiva BP, Pérez HT et al (2004) Head size and intelligence, learning, nutritional status and brain development. Head, IQ, learning, nutrition and brain. Neuropsychologia 42(8):1118–1131PubMedGoogle Scholar
  6. 6.
    Räikkönen K, Forsen T, Henriksson M et al (2009) Growth trajectories and intellectual abilities in young adulthood: the Helsinki birth cohort study. Am J Epidemiol 170(4):447–455PubMedGoogle Scholar
  7. 7.
    Rãikkonen K, Pesonen A (2009) Early life origins of psychological development and mental health. Scand J Psychol 50(6):583–591PubMedGoogle Scholar
  8. 8.
    Raikkonen K, Kajantie E, Pesonen AK, Heinonen K, Alastalo H, Leskinen JT, Nyman K, Henriksson M, Lahti J, Lahti M, Pyhälä R, Tuovinen S, Osmond C, Barker DJ, Eriksson JG (2013) Early life origins cognitive decline: findings in elderly men in the Helsinki birth cohort study. PLoS One 8(1):e54707PubMedPubMedCentralGoogle Scholar
  9. 9.
    Scharf RJ, Rogawski ET, Murray-Kolb LE, Maphula A, Svensen E, Tofail F, Rasheed M, Abreu C, Vasquez AO, Shrestha R, Pendergast L, Mduma E, Koshy B, Conaway MR, Platts-Mills JA, Guerrant RL, DeBoer MD (2018) Early childhood growth and cognitive outcomes: findings from the MAL-ED study. Matern Child Nutr.  https://doi.org/10.1111/mcn.12584 PubMedGoogle Scholar
  10. 10.
    Fujimura M, Seryu JI (1977) Velocity of head growth during the perinatal period. Arch Dis Child 52(2):105–112PubMedPubMedCentralGoogle Scholar
  11. 11.
    Coronado R, Macaya A, Giraldo J, Roig-Quilis M (2014) Concordance between a head circumference growth function and intellectual disability in relation with the cause of microcephaly. Anales de Pediatría 83:109–116 (English edition) PubMedGoogle Scholar
  12. 12.
    Leppänen M, Lapinleimu H, Lind A, Matomäki J, Lehtonen L, Haataja L, Rautava P (2014) Antenatal and postnatal growth and 5-year cognitive outcome in very preterm infants. Pediatrics 133(1):63–70PubMedGoogle Scholar
  13. 13.
    Raz S, Newman JB, De Bastos AK, Peters BN, Batton DG (2014) Postnatal growth and neuropsychological performance in preterm-birth preschoolers. Neuropsychology 28(2):188–201PubMedGoogle Scholar
  14. 14.
    Álamo-Junquera D, Sunyer J, Iñiguez C et al (2015) Prenatal head growth and child neuropsychological development at age 14 months. American Journal of Obstetrics and Gynecology 212(5):661.e1–661.e11Google Scholar
  15. 15.
    Lawlor DA, Batty GD, Morton SM, Deary IJ, Macintyre S, Ronalds G, Leon DA (2005) Early life predictors of childhood intelligence: evidence from the Aberdeen children of the 1950s study. J Epidemiol Community Health 59(8):656–663PubMedPubMedCentralGoogle Scholar
  16. 16.
    Boucher O, Julvez J, Guxens M et al (2017) Association between breastfeeding duration and cognitive development, autistic traits and ADHD symptoms: a multicenter study in Spain. Pediatr Res 81(3):434–442PubMedGoogle Scholar
  17. 17.
    Monroy-Torres R, Naves-Sánchez J, Ortega-García JA (2012) Breastfeeding and metabolic indicators in Mexican premature newborns. Rev Invest Clin 64(6 Pt 1):521–528PubMedGoogle Scholar
  18. 18.
    Castellanos FX, Lee PP, Sharp W et al (2002) Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA 288(14):1740–1748PubMedGoogle Scholar
  19. 19.
    Linnet K, Wisborg K, Agerbo E, Secher N, Thomsen P, Henriksen T (2006) Gestational age, birth weight, and the risk of hyperkinetic disorder. Arch Dis Child 91(8):655–660PubMedPubMedCentralGoogle Scholar
  20. 20.
    Hultman C, Torrång A, Tuvblad C, Cnattingius S, Larsson J, Lichtenstein P (2007) Birth weight and attention-deficit/hyperactivity symptoms in childhood and early adolescence: a prospective Swedish twin study. J Am Acad Child Adolesc Psychiatry 46(3):370–377PubMedGoogle Scholar
  21. 21.
    Vander Ploeg Booth K (2016) Attention-deficit/hyperactivity disorder (ADHD) in children born preterm and with poor fetal growth. NeoReviews 17(4):e213–e219Google Scholar
  22. 22.
    Julvez J, Forns M, Ribas-Fitó N, Torrent M, Sunyer J (2011) Attention behavior and hyperactivity and concurrent neurocognitive and social competence functioning in 4-year-olds from two population-based birth cohorts. Eur Psychiatry J Assoc Eur Psychiatry 26(6):381–389Google Scholar
  23. 23.
    Stathis S, O’Callaghan M, Harvey J, Rogers Y (1999) Head circumference in ELBW babies is associated with learning difficulties and cognition but not ADHD in the school-aged child. Dev Med Child Neurol 41(6):375–380PubMedGoogle Scholar
  24. 24.
    Heinonen K, Räikkönen K, Pesonen A-K et al (2011) Trajectories of growth and symptoms of attention-deficit/hyperactivity disorder in children: a longitudinal study. BMC Pediatrics 11:84PubMedPubMedCentralGoogle Scholar
  25. 25.
    Lahti J, Räikkönen K, Kajantie E, Heinonen K, Pesonen A-K, Järvenpää A-L, Strandberg T (2006) Small body size at birth and behavioural symptoms of ADHD in children aged five to six years. J Child Psychol Psychiatry 47(11):1167–1174PubMedGoogle Scholar
  26. 26.
    Murray E, Matijasevich A, Santos IS, Barros AJ, Anselmi L, Barros FC, Stein A (2015) Sex differences in the association between foetal growth and child attention at age four: specific vulnerability of girls. J Child Psychol Psychiatry 56(12):1380–1388PubMedGoogle Scholar
  27. 27.
    Courchesne E, Carper R, Akshoomoff N (2003) Evidence of brain overgrowth in the first year of life in Autism. J Am Med Assoc 290(3):337–344Google Scholar
  28. 28.
    Sacco R, Gabriele S, Persico A (2015) Head circumference and brain size in autism spectrum disorder: a systematic review and meta-analysis. Psychiatry Res Neuroimaging 234(2):239–251Google Scholar
  29. 29.
    Pyhälä R, Hovi P, Lahti M, Sammallahti S, Lahti J, Heinonen K, Pesonen AK, Strang-Karlsson S, Eriksson JG, Andersson S, Järvenpää AL, Kajantie E, Räikkönen K (2014) Very low birth weight, infant growth, and autism-spectrum traits in adulthood. Pediatrics 134(6):1075–1083PubMedGoogle Scholar
  30. 30.
    Zwaigenbaum L, Young GS, Stone WL et al (2014) Early head growth in infants at risk of autism: a baby siblings research consortium study. J Am Acad Child Adolesc Psychiatry 53:1053–1062PubMedPubMedCentralGoogle Scholar
  31. 31.
    Zhang L, Thomas KM, Davidson MC, Casey BJ, Heier LA, Uluğ AM (2005) MR quantitation of volume and diffusion changes in the developing brain. AJNR Am J Neuroradiol 26(1):45–49PubMedGoogle Scholar
  32. 32.
    James HE, Perszyk AA, MacGregor TL, Aldana PR (2015) The value of head circumference measurements after 36 months of age: a clinical report and review of practice patterns. J Neurosurg Pediatr 16(2):186–194PubMedGoogle Scholar
  33. 33.
    Guxens M, Ballester F, Espada M, INMA Project et al (2012) Cohort Profile: the INMA–INfancia y Medio Ambiente–(Environment and Childhood) Project. Int J Epidemiol 41(4):930–940PubMedGoogle Scholar
  34. 34.
    (1982) Intraclass correlation coefficient. In: Kotz S, Johnson NL (eds) Encyclopaedia of statistical sciences, vol 4. Wiley, New York, pp 213–217Google Scholar
  35. 35.
    Pinheiro J, Bates D (2000) Mixed-effects models in S and S PLUS: statistics and computing. Springer, New YorkGoogle Scholar
  36. 36.
    Iñiguez C, Ballester F, Amorós R, Murcia M, Plana A, Rebagliato M (2012) Active and passive smoking during pregnancy and ultrasound measures of fetal growth in a cohort of pregnant women. J Epidemiol Community Health 66(6):563–570PubMedGoogle Scholar
  37. 37.
    Gurrin LC, Blake KV, Evans SF, Newnham JP (2001) Statistical measures of foetal growth using linear mixed models applied to the foetal origins hypothesis. Stat Med 20(22):3391–3409PubMedGoogle Scholar
  38. 38.
    Royston P (1995) Calculation of unconditional and conditional reference intervals for foetal size and growth from longitudinal measurements. Stat Med 14(13):1417–1436PubMedGoogle Scholar
  39. 39.
    Villar J, Cheikh Ismail L, Victora CG et al (2014) International fetal and newborn growth consortium for the 21st century (INTERGROWTH-21st). International standards for newborn weight, length, and head circumference by gestational age and sex: the newborn cross-sectional study of the INTERGROWTH-21st Project. Lancet 384(9946):857–868PubMedGoogle Scholar
  40. 40.
    de Onis M, Garza C, Onyango AW, Rolland-Cachera MF (2009) Le, Comité de nutrition de la Société française de pédiatrie. [WHO growth standards for infants and young children]. Arch Pediatr 16(1):47–53PubMedGoogle Scholar
  41. 41.
    McCarthy DMSCA (2009) Escalas McCarthy de Aptitudes y Psicomotricidad para Niños. TEA Ediciones, MadridGoogle Scholar
  42. 42.
    Julvez J, Forns M, Ribas-Fito N, Mazon C, Torrent M, Garcia-Esteban R (2008) Psychometric characteristics of the California preschool social competence scale in a Spanish population sample. Early Educ Dev 19:795–815Google Scholar
  43. 43.
    Scott F, Baron-Cohen S, Bolton P, Brayne C (2002) The CAST (childhood Asperger syndrome test): preliminary development of UK screen for mainstream primary-school children. Autism 6(1):9–31PubMedGoogle Scholar
  44. 44.
    Williams J, Scott F, Stott C et al (2005) The CAST (childhood Asperger syndrome test): test accuracy. Autism 9:45–68PubMedGoogle Scholar
  45. 45.
    American Psychiatric Association (2002) Manual diagnóstico y estadístico de los trastornos mentales. Masson, IV. BarcelonaGoogle Scholar
  46. 46.
    Sterba S, Egger HL, Angold A (2007) Diagnostic specificity and nonspecificity in the dimensions of preschool psychopathology. J Child Psychol Psychiatry [Internet] 48(10):1005–1013Google Scholar
  47. 47.
    Conners C, Staff M (2001) Conners’ kiddie continuous performance test (K-CPT): computer program for windows technical guide and software manual. Multi-Health Systems, Inc, TorontoGoogle Scholar
  48. 48.
    Conners C, Epstein J, Angold A, Klaric J (2003) Continuous performance test performance in a normative epidemiological sample. J Abnorm Child Psychol 31:555–562PubMedGoogle Scholar
  49. 49.
    Vilor-Tejedor N, Alemany S, Forns J, Cáceres A, Murcia M, Macià D, Pujol J, Sunyer J, González JR (2016) Assessment of susceptibility risk factors for ADHD in imaging genetic studies. J Atten Disord.  https://doi.org/10.1177/1087054716664408
  50. 50.
    Axelrod BN (2002) Validity of the Wechsler abbreviated scale of intelligence and other very short forms of estimating intellectual functioning. Assessment 9(1):17–23PubMedGoogle Scholar
  51. 51.
    González de Rivera JL, Derogatis L, de las Cuevas C (1989) The Spanish Version of the SCL-90-R: normative data in general population. Towson, BaltimoreGoogle Scholar
  52. 52.
    Whitehouse AJ, Zubrick SR, Blair E, Newnham JP, Hickey M (2012) Fetal head circumference growth in children with specific language impairment. Arch Dis Child 97(1):49–51PubMedGoogle Scholar
  53. 53.
    van der Vossen S, Pistorius LR, Mulder EJ, Platenkamp M, Stoutenbeek P, Visser GH, Gooskens RH (2009) Role of prenatal ultrasound in predicting survival and mental and motor functioning in children with spina bifida. Ultrasound Obstet Gynecol 34(3):253–258Google Scholar
  54. 54.
    Jung RE, Haier RJ (2007) The parieto-frontal integration theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 30(2):135PubMedGoogle Scholar
  55. 55.
    Bhutta AT, Cleves MA, Casey PH, Cradock MM, Anand KJS (2002) Cognitive and behavioral outcomes of school-aged children who were born preterm. JAMA 288(6):728–737PubMedGoogle Scholar
  56. 56.
    Ptacek R, Kuzelova H, Paclt I, Zukov I, Fischer S (2009) ADHD and growth: anthropometric changes in medicated and non-medicated ADHD boys. Med Sci Monitor Int Med J Exp Clin Res 15(12):CR595–CR599Google Scholar
  57. 57.
    Portellano JA (2007) Trastorno por déficit de atención (TDAH). In: Portellano JA (ed) Neuropsicologia infantil. Sintesi, Madrid, pp 145–159Google Scholar
  58. 58.
    Wadhwa P, Buss C, Entringer S, Swanson M (2009) Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 27(5):358–368PubMedPubMedCentralGoogle Scholar
  59. 59.
    Julvez J, Ribas-Fito N, Torrent M, Forns M, Garcia-Esteban R, Sunyer J (2007) Maternal smoking habits and cognitive development of children at age 4 years in a population-based birth cohort. Int J Epidemiol 36(4):825–832PubMedGoogle Scholar
  60. 60.
    Schlotz W, Phillips DIW (2009) Fetal origins of mental health: evidence and mechanisms. Brain Behav Immun 23(7):905–916PubMedGoogle Scholar
  61. 61.
    Young JM, Powell TL, Morgan BR et al (2015) Deep grey matter growth predicts neurodevelopmental outcomes in very preterm children. NeuroImage 111:360–368PubMedGoogle Scholar
  62. 62.
    Bartholomeusz HH, Courchesne E, Karns CM (2002) Relationship between head circumference and brain volume in healthy normal toddlers, children, and adults. Neuropediatrics 33(5):239–241PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Muriel Ferrer
    • 1
  • Raquel García-Esteban
    • 1
    • 2
    • 3
  • Carmen Iñiguez
    • 3
    • 4
  • Olga Costa
    • 4
  • Ana Fernández-Somoano
    • 3
    • 5
  • Cristina Rodríguez-Delhi
    • 6
  • Jesús Ibarluzea
    • 3
    • 7
    • 8
  • Aitana Lertxundi
    • 3
    • 8
  • Cathryn Tonne
    • 1
  • Jordi Sunyer
    • 1
    • 2
    • 3
    • 9
  • Jordi Julvez
    • 1
    • 2
    • 3
    • 9
    Email author
  1. 1.ISGlobal, Instituto de Salud Global de Barcelona-Campus MARPRBBBarcelonaSpain
  2. 2.IMIM (Hospital del Mar Medical Research Institute)BarcelonaSpain
  3. 3.CIBER Epidemiologia y Salud Pública (CIBERESP)MadridSpain
  4. 4.Epidemiology and Environmental Health Joint Research UnitValenciaSpain
  5. 5.Departamento de MedicinaUniversidad de OviedoOviedoSpain
  6. 6.Servicio de PediatríaHospital San AgustínAvilésSpain
  7. 7.Public Health Division of GipuzkoaBioDonostia Research InstituteGipuzkoa, San SebastianSpain
  8. 8.Faculty of PsychologyUniversity of the Basque Country (UPV/EHU)San SebastianSpain
  9. 9.Universitat Pompeu Fabra (UPF)BarcelonaSpain

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