Advertisement

European Child & Adolescent Psychiatry

, Volume 24, Issue 8, pp 919–929 | Cite as

Maternal smoking and offspring inattention and hyperactivity: results from a cross-national European survey

  • Viviane Kovess
  • Katherine M. KeyesEmail author
  • Ava Hamilton
  • Ondine Pez
  • Adina Bitfoi
  • Ceren Koç
  • Dietmar Goelitz
  • Rowella Kuijpers
  • Sigita Lesinskiene
  • Zlatka Mihova
  • Roy Otten
  • C. Fermanian
  • Daniel J. Pilowsky
  • Ezra Susser
Original Contribution

Abstract

In utero exposure to tobacco smoke is associated with adverse neonatal outcomes; the association with later childhood mental health outcomes remains controversial. We used a strategy involving comparison of maternal and paternal smoking reports in a sample pooling data from six diverse European countries. Data were drawn from mother (N = 4,517) and teacher (N = 4,611) reported attention deficit and hyperactivity disorder (ADHD) symptoms in school children aged 6–11 in Turkey, Romania, Bulgaria, Lithuania, Germany, and the Netherlands, surveyed in 2010. Mothers report on self and husband’s smoking patterns during the pregnancy period. Logistic regression used with control covariates including demographics, maternal distress, live births, region, and post-pregnancy smoking. In unadjusted models, maternal prenatal smoking was associated with probable ADHD based on mother [Odds Ratio (OR) = 1.82, 95 % Confidence Interval (CI) 1.45–2.29], teacher (OR = 1.69, 95 % CI 1.33–2.14) and mother plus teacher (OR = 1.49, 95 % CI 1.03–2.17) report. Paternal prenatal smoking was similarly associated with probable ADHD in unadjusted models. When controlled for relevant confounders, maternal prenatal smoking remained a risk factor for offspring probable ADHD based on mother report (OR = 1.44, 95 % CI 1.06–1.96), whereas the effect of paternal prenatal smoking diminished (e.g., mother report: OR = 1.17, 95 % CI 0.92–1.49). Drawing on data from a diverse set of countries across Europe, we document that the association between maternal smoking and offspring ADHD is stronger than that of paternal smoking during the pregnancy period and offspring ADHD. To the extent that confounding is shared between parents, these results reflect a potential intrauterine influence of smoking on ADHD in children.

Keywords

ADHD Hyperactivity Smoking Prenatal smoking In utero tobacco 

Abbreviations

ADHD

Attention deficit hyperactivity disorder

SDQ

Strengths and difficulties questionnaire

CI

Confidence interval

Notes

Acknowledgments

This project had been financed by the European Union, grant number 2006336.

Conflict of interest

The authors report no conflicts of interest.

Supplementary material

787_2014_641_MOESM1_ESM.doc (204 kb)
Supplementary material 1 (DOC 203 kb)

References

  1. 1.
    Aaronson NK, Acquadro C, Alonso J, Apolone G, Bucquet D, Bullinger M, Bungay K, Fukuhara S, Gandek B, Keller S et al (1992) International quality of life assessment (IQOLA) project. Qual Life Res 1:349–351PubMedCrossRefGoogle Scholar
  2. 2.
    Agrawal A, Scherrer JF, Grant JD, Sartor CE, Pergadia ML, Duncan AE, Madden PA, Haber JR, Jacob T, Bucholz KK, Xian H (2010) The effects of maternal smoking during pregnancy on offspring outcomes. Prev Med 50:13–18PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Ball SW, Gilman SE, Mick E, Fitzmaurice G, Ganz ML, Seidman LJ, Buka SL (2010) Revisiting the association between maternal smoking during pregnancy and ADHD. J Psychiatr Res 44:1058–1062PubMedCrossRefGoogle Scholar
  4. 4.
    Biederman J, Faraone SV, Monuteaux MC, Grossbard JR (2004) How informative are parent reports of attention-deficit/hyperactivity disorder symptoms for assessing outcome in clinical trials of long-acting treatments? A pooled analysis of parents’ and teachers’ reports. Pediatrics 113:1667–1671PubMedCrossRefGoogle Scholar
  5. 5.
    Biederman J, Petty CR, Bhide PG, Woodworth KY, Faraone S (2012) Does exposure to maternal smoking during pregnancy affect the clinical features of ADHD? Results from a controlled study. World J Biol Psychiatry 13:60–64PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Brion MJ, Victora C, Matijasevich A, Horta B, Anselmi L, Steer C, Menezes AM, Lawlor DA, Davey Smith G (2010) Maternal smoking and child psychological problems: disentangling causal and noncausal effects. Pediatrics 126:e57–65PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Button TM, Thapar A, McGuffin P (2005) Relationship between antisocial behaviour, attention-deficit hyperactivity disorder and maternal prenatal smoking. Br J Psychiatry 187:155–160PubMedCrossRefGoogle Scholar
  8. 8.
    CCHS (2007) Canadian community health survey, cycle 4.1. Statistics Canada, CanadaGoogle Scholar
  9. 9.
    D’Onofrio BM, Van Hulle CA, Waldman ID, Rodgers JL, Harden KP, Rathouz PJ, Lahey BB (2008) Smoking during pregnancy and offspring externalizing problems: an exploration of genetic and environmental confounds. Dev Psychopathol 20:139–164PubMedCentralPubMedGoogle Scholar
  10. 10.
    Davey Smith G (2008) Assessing intrauterine influences on offspring health outcomes: can epidemiological studies yield robust findings? Basic Clin Pharmacol Toxicol 102:245–256CrossRefGoogle Scholar
  11. 11.
    Smith GD (2012) Negative control exposures in epidemiologic studies. Epidemiology 23:350–351Google Scholar
  12. 12.
    DiFranza JR, Aligne CA, Weitzman M (2004) Prenatal and postnatal environmental tobacco smoke exposure and children’s health. Pediatrics 113:1007–1015PubMedGoogle Scholar
  13. 13.
    DiPietro JA, Hodgson DM, Costigan KA, Hilton SC, Johnson TR (1996) Fetal neurobehavioral development. Child Dev 67:2553–2567PubMedCrossRefGoogle Scholar
  14. 14.
    Ellis LC, Berg-Nielsen TS, Lydersen S, Wichstrom L (2012) Smoking during pregnancy and psychiatric disorders in preschoolers. Eur Child Adolesc Psychiatry 21:635–644PubMedCrossRefGoogle Scholar
  15. 15.
    Eriksson P, Ankarberg E, Fredriksson A (2000) Exposure to nicotine during a defined period in neonatal life induces permanent changes in brain nicotinic receptors and in behaviour of adult mice. Brain Res 853:41–48PubMedCrossRefGoogle Scholar
  16. 16.
    Eskenazi B, Prehn AW, Christianson RE (1995) Passive and active maternal smoking as measured by serum cotinine: the effect on birthweight. Am J Public Health 85:395–398PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Fergusson DM, Horwood LJ, Lynskey MT (1993) Maternal smoking before and after pregnancy: effects on behavioral outcomes in middle childhood. Pediatrics 92:815–822PubMedGoogle Scholar
  18. 18.
    European Communities (2008) Flash Eurobarometer, Survey on Tobacco. European Union, The Office for publications of the European CommunitiesGoogle Scholar
  19. 19.
    Fogelman KR, Manor O (1988) Smoking in pregnancy and development into early adulthood. BMJ 297:1233–1236PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Frisell T, Oberg S, Kuja-Halkola R, Sjolander A (2012) Sibling comparison designs: bias from non-shared confounders and measurement error. Epidemiology 23:713–720PubMedCrossRefGoogle Scholar
  21. 21.
    Froehlich TE, Lanphear BP, Auinger P, Hornung R, Epstein JN, Braun J, Kahn RS (2009) Association of tobacco and lead exposures with attention-deficit/hyperactivity disorder. Pediatrics 124:e1054–1063PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Gilman SE, Gardener H, Buka SL (2008) Maternal smoking during pregnancy and children’s cognitive and physical development: a causal risk factor? Am J Epidemiol 168:522–531PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Goodman R (1997) The strengths and difficulties questionnaire: a research note. J Child Psychol Psychiatry 38:581–586PubMedCrossRefGoogle Scholar
  24. 24.
    Gualtieri CT, Johnson LG (2005) ADHD: is objective diagnosis possible? Psychiatry (Edgmont) 2:44–53Google Scholar
  25. 25.
    Ino T (2010) Maternal smoking during pregnancy and offspring obesity: meta-analysis. Pediatr Int 52:94–99PubMedCrossRefGoogle Scholar
  26. 26.
    Johns JM, Louis TM, Becker RF, Means LW (1982) Behavioral effects of prenatal exposure to nicotine in guinea pigs. Neurobehav Toxicol Teratol 4:365–369PubMedGoogle Scholar
  27. 27.
    Keyes KM, Davey Smith G, Susser E (2014) Associations of prenatal maternal smoking with offspring hyperactivity: causal or confunded? Psychol Med 44:857–867Google Scholar
  28. 28.
    Keyes KM, Davey Smith G, Susser E (2014) Commentary: smoking in pregnancy and offspring health: early insights into family-based and ‘negative control’ studies? Int J Epidemiol 43:1381–1388Google Scholar
  29. 29.
    Knopik VS (2009) Maternal smoking during pregnancy and child outcomes: real or spurious effect? Dev Neuropsychol 34:1–36PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Kovess V, Pilowsky DJ, Boyd A, Pez O, Bitfoi A, Carta M, Eke C, Golitz D, Kuijpers R, Lesinskiene S, Mihova Z, Otten R, Susser E (2013) Parental smoking in the vicinity of children and tobacco control policies in the European region. PLoS One 8:e56783Google Scholar
  31. 31.
    Langley K, Heron J, Smith GD, Thapar A (2012) Maternal and paternal smoking during pregnancy and risk of ADHD symptoms in offspring: testing for intrauterine effects. Am J Epidemiol 176:261–268PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Langley K, Rice F, van den Bree MB, Thapar A (2005) Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behaviour. A review. Minerva Pediatr 57:359–371PubMedGoogle Scholar
  33. 33.
    Lavigne JV, Dulcan MK, LeBailly SA, Binns HJ (2012) Can parent reports serve as a proxy for teacher ratings in medication management of attention-deficit hyperactivity disorder? J Dev Behav Pediatr 33:336–342PubMedCrossRefGoogle Scholar
  34. 34.
    Li J, Olsen J, Vestergaard M, Obel C (2010) Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: a nationwide follow-up study in Denmark. Eur Child Adolesc Psychiatry 19:747–753PubMedCrossRefGoogle Scholar
  35. 35.
    Lindblad F, Hjern A (2010) ADHD after fetal exposure to maternal smoking. Nicotine Tob Res 12:408–415PubMedCrossRefGoogle Scholar
  36. 36.
    Linnet KM, Dalsgaard S, Obel C, Wisborg K, Henriksen TB, Rodriguez A, Kotimaa A, Moilanen I, Thomsen PH, Olsen J, Jarvelin MR (2003) Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am J Psychiatry 160:1028–1040PubMedCrossRefGoogle Scholar
  37. 37.
    Linnet KM, Wisborg K, Obel C, Secher NJ, Thomsen PH, Agerbo E, Henriksen TB (2005) Smoking during pregnancy and the risk for hyperkinetic disorder in offspring. Pediatrics 116:462–467PubMedCrossRefGoogle Scholar
  38. 38.
    Nigg JT, Breslau N (2007) Prenatal smoking exposure, low birth weight, and disruptive behavior disorders. J Am Acad Child Adolesc Psychiatry 46:362–369PubMedCrossRefGoogle Scholar
  39. 39.
    Nomura Y, Marks DJ, Halperin JM (2010) Prenatal exposure to maternal and paternal smoking on attention deficit hyperactivity disorders symptoms and diagnosis in offspring. J Nerv Ment Dis 198:672–678PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Obel C, Olsen J, Henriksen TB, Rodriguez A, Jarvelin MR, Moilanen I, Parner E, Linnet KM, Taanila A, Ebeling H, Heiervang E, Gissler M (2011) Is maternal smoking during pregnancy a risk factor for hyperkinetic disorder? Findings from a sibling design. Int J Epidemiol 40:338–345PubMedCrossRefGoogle Scholar
  41. 41.
    Pez O, Boyd A, Fermanian C, Kovess V (2013) The school children mental health project. School Children Mental Health Europe. Available at: http://www.scmheproject.com/admin/includes/archivos//EUROPEAN_REPORT-_School_survey_FINAL.pdf
  42. 42.
    Pez O, Boyd A, Fermanian C, Kovess-Masfety V (2011) European report: the school children mental health evaluation phase 1: validation of the SCMHE instruments. http://www.scmheproject.com/resources.php
  43. 43.
    Rodriguez A, Bohlin G (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46:246–254PubMedCrossRefGoogle Scholar
  44. 44.
    Roza SJ, Verhulst FC, Jaddoe VW, Steegers EA, Mackenbach JP, Hofman A, Tiemeier H (2009) Maternal smoking during pregnancy and child behaviour problems: the Generation R Study. Int J Epidemiol 38:680–689PubMedCrossRefGoogle Scholar
  45. 45.
    Schmitz M, Denardin D, Laufer Silva T, Pianca T, Hutz MH, Faraone S, Rohde LA (2006) Smoking during pregnancy and attention-deficit/hyperactivity disorder, predominantly inattentive type: a case-control study. J Am Acad Child Adolesc Psychiatry 45:1338–1345PubMedCrossRefGoogle Scholar
  46. 46.
    Sexton M, Hebel JR (1984) A clinical trial of change in maternal smoking and its effect on birth weight. JAMA 251:911–915PubMedCrossRefGoogle Scholar
  47. 47.
    Sherman DK, McGue MK, Iacono WG (1997) Twin concordance for attention deficit hyperactivity disorder: a comparison of teachers’ and mothers reports. Am J Psychiatry 154:532–535PubMedCrossRefGoogle Scholar
  48. 48.
    Susser E, Eide MG, Begg M (2010) Invited commentary: the use of sibship studies to detect familial confounding. Am J Epidemiol 172:537–539PubMedCrossRefGoogle Scholar
  49. 49.
    Thakur GA, Sengupta SM, Grizenko N, Schmitz N, Page V, Joober R (2013) Maternal smoking during pregnancy and ADHD: a comprehensive clinical and neurocognitive characterization. Nicotine Tob Res 15:149–157PubMedCrossRefGoogle Scholar
  50. 50.
    Thapar A, Rice F, Hay D, Boivin J, Langley K, van den Bree M, Rutter M, Harold G (2009) Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry 66:722–727PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Thapar A, Rutter M (2009) Do prenatal risk factors cause psychiatric disorder? Be wary of causal claims. Br J Psychiatry 195:100–101PubMedCrossRefGoogle Scholar
  52. 52.
    Tyrrell J, Huikari V, Christie JT, Cavadino A, Bakker R, Brion MJ, Geller F, Paternoster L, Myhre R, Potter C, Johnson PC, Ebrahim S, Feenstra B, Hartikainen AL, Hattersley AT, Hofman A, Kaakinen M, Lowe LP, Magnus P, McConnachie A, Melbye M, Ng JW, Nohr EA, Power C, Ring SM, Sebert SP, Sengpiel V, Taal HR, Watt GC, Sattar N, Relton CL, Jacobsson B, Frayling TM, Sorensen TI, Murray JC, Lawlor DA, Pennell CE, Jaddoe VW, Hypponen E, Lowe WL Jr, Jarvelin MR, Davey Smith G, Freathy RM (2012) Genetic variation in the 15q25 nicotinic acetylcholine receptor gene cluster (CHRNA5-CHRNA3-CHRNB4) interacts with maternal self-reported smoking status during pregnancy to influence birth weight. Hum Mol Genet 21:5344–5358PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    van de Kamp JL, Collins AC (1994) Prenatal nicotine alters nicotinic receptor development in the mouse brain. Pharmacol Biochem Behav 47:889–900PubMedCrossRefGoogle Scholar
  54. 54.
    Vik T, Jacobsen G, Vatten L, Bakketeig LS (1996) Pre- and post-natal growth in children of women who smoked in pregnancy. Early Hum Dev 45:245–255PubMedCrossRefGoogle Scholar
  55. 55.
    Villalbi JR, Salvador J, Cano-Serral G, Rodriguez-Sanz MC, Borrell C (2007) Maternal smoking, social class and outcomes of pregnancy. Paediatr Perinat Epidemiol 21:441–447PubMedCrossRefGoogle Scholar
  56. 56.
    Ware JE, Kosinski M, Keller SD (1994) SF-36 Physical and mental component summary measures: a user’s manual. The Health Institute, New England Medical Center, BostonGoogle Scholar
  57. 57.
    Ware JE, Snow KK, Kosinski M, Gandek B (1993) SF-36 Health Survey: Manual and Interpretation Guide. The Health Institute, New England Medical Center, BostonGoogle Scholar
  58. 58.
    Wolraich ML, Lambert EW, Bickman L, Simmons T, Doffing MA, Worley KA (2004) Assessing the impact of parent and teacher agreement on diagnosing attention-deficit hyperactivity disorder. J Dev Behav Pediatr 25:41–47PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Viviane Kovess
    • 1
  • Katherine M. Keyes
    • 2
    • 11
    Email author
  • Ava Hamilton
    • 2
  • Ondine Pez
    • 1
  • Adina Bitfoi
    • 3
  • Ceren Koç
    • 4
  • Dietmar Goelitz
    • 5
  • Rowella Kuijpers
    • 6
  • Sigita Lesinskiene
    • 7
  • Zlatka Mihova
    • 8
  • Roy Otten
    • 6
  • C. Fermanian
    • 1
  • Daniel J. Pilowsky
    • 2
  • Ezra Susser
    • 2
    • 9
    • 10
  1. 1.EHESP Rennes, Sorbonne Paris Cite, EA 4069Paris Descartes UniversityParisFrance
  2. 2.Departments of Epidemiology and PsychiatryColumbia University, and New York State Psychiatric InstituteNew YorkUSA
  3. 3.The Romanian League for Mental HealthBucharestRomania
  4. 4.Yeniden Health and Education SocietyIstanbulTurkey
  5. 5.Center for Applied Sciences of HealthLeuphana University of LuneburgLuneburgGermany
  6. 6.Behavioral Science InstituteRadboud University NijmegenNijmegenThe Netherlands
  7. 7.Clinic of Psychiatry, Faculty of MedicineUniversity of VilniusVilniusLithuania
  8. 8.New Bulgarian UniversitySofiaBulgaria
  9. 9.New York State Psychiatric Institute, New YorkNew YorkUSA
  10. 10.Department of PsychiatryUniversity of GöttingenGöttingenGermany
  11. 11.Department of Epidemiology, Mailman School of Public HealthColumbia UniversityNew YorkUSA

Personalised recommendations