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Severe psychosocial stress and heavy cigarette smoking during pregnancy: an examination of the pre- and perinatal risk factors associated with ADHD and Tourette syndrome

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Abstract

Attention-deficit/hyperactivity disorder (ADHD) is frequently diagnosed in children with Tourette syndrome (TS). The basis for this co-occurrence is uncertain. This study aimed to determine if specific pre- and perinatal risk factors, including heavy maternal smoking and severe psychosocial stress during pregnancy, were associated with one or both disorders, or neither. We compared maternal report data on pre- and perinatal risk factors on 222 children between the ages of 7 and 18 years including 45 individuals with TS alone, 52 individuals with ADHD alone, 60 individuals with condition of comorbid TS + ADHD, and 65 unaffected control children. Pre- and perinatal histories as well as psychiatric assessments were performed using standardized questionnaires and semi-structured interviews with the mothers and children. Logistic regression was used to determine the odds ratio for each variable of interest. Compared to the mothers of unaffected control children, the mothers of children with ADHD alone reported higher rates of heavy smoking (>10 cigarettes per day) during pregnancy and higher levels of severe psychosocial stress during pregnancy (OR = 13.5, p < 0.01 and OR = 6.8, p < 0.002, respectively). The TS + ADHD and the TS alone patients also had higher rates heavy maternal smoking and high levels of psychosocial stress compared to the control children, but these differences failed to reach statistical significance (heavy smoking: OR = 8.5, p < 0.052, OR = 4.6, p < 0.19, respectively; severe psychosocial stress: OR = 3.1, p < 0.07, OR = 2.6, p < 0.11, respectively). Heavy maternal smoking and severe levels psychosocial stress during pregnancy were independently associated with a diagnosis of ADHD. TS patients also had higher rates of these risk factors, but the ORs failed to reach statistical significance. Efforts are needed to reduce the frequency of these risk factors in high-risk populations. Future studies, using genetically sensitive designs, are also needed to sort out the causal pathways.

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Abbreviations

TS:

Tourette syndrome

ADHD:

Attention-deficit/hyperactivity disorder

OCD:

Obsessive compulsive disorder

LBW:

Low birth weight

YGTSS:

Yale global tic severity scale

CY-BOCS:

Children’s Yale brown obsessive compulsive scale

MSRPFED:

Modified schedule for risk and protective factors in early development

RCMAS:

Revised children’s manifest anxiety scale

LSS:

Level of stress severity scale

CAS:

Coping ability scale

PCS:

Pregnancy complication scale

SMSPC:

Severe maternal stress with poor coping

References

  1. Costello EJ, Mustillo S, Erkanli A et al (2003) Prevalence and development of psychiatric disorders in childhood and adolescence. Arch Gen Psychiatry 60(8):837–844

    Article  PubMed  Google Scholar 

  2. Khalifa N, Von Knorring AL (2006) Psychopathology in a Swedish population of school children with tic disorders. J Am Acad Child Adolesc Psychiatry 45(11):1346–1353

    Article  PubMed  Google Scholar 

  3. Kurlan R, Como PG, Miller B et al (2002) The behavioral spectrum of tic disorders: a community-based study. Neurology 59(3):414–420

    CAS  PubMed  Google Scholar 

  4. Centers for Disease Control, Prevention (CDC) (2009) Prevalence of diagnosed Tourette syndrome in persons aged 6–17 years—United States, 2007. Morb Mortal Wkly Rep 58(21):581–585

    Google Scholar 

  5. Scahill L, Sukhodolsky DG, Williams SK et al (2005) Public health significance of tic disorders in children and adolescents. Adv Neurol 96:240–248

    PubMed  Google Scholar 

  6. Hoekstra PJ, Steenhuis MP, Troost PW et al (2004) Relative contribution of attention-deficit hyperactivity disorder, obsessive-compulsive disorder, and tic severity to social and behavioral problems in tic disorders. J Dev Behav Pediatr 25(4):272–279

    Article  PubMed  Google Scholar 

  7. Spencer T, Biederman J, Coffey B et al (2001) Tourette disorder and ADHD. Adv Neurol 85:57–77

    CAS  PubMed  Google Scholar 

  8. Sukhodolsky DG, Scahill L, Zhang H et al (2003) Disruptive behavior in children with Tourette’s syndrome: association with ADHD comorbidity, tic severity, and functional impairment. J Am Acad Child Adolesc Psychiatry 42(1):98–105

    Article  PubMed  Google Scholar 

  9. Grados MA, Mathews CA, Tourette Syndrome Association International Consortium for Genetics (2008) Latent class analysis of Gilles de la Tourette syndrome using comorbidities: clinical and genetic implications. Biol Psychiatry 64(3):219–225

    Article  PubMed  Google Scholar 

  10. Plessen KJ, Royal JM, Peterson BS (2007) Neuroimaging of tic disorders with co-existing attention-deficit/hyperactivity disorder. Eur Child Adolesc Psychiatry 1:60–70

    Article  Google Scholar 

  11. Pasamanick B, Kawi A (1956) A study of the association of prenatal and paranatal factors with the development of tics in children; a preliminary investigation. J Pediatr 48(5):596–601

    Article  CAS  PubMed  Google Scholar 

  12. Shapiro AK, Shapiro E, Wayne H (1972) Birth, developmental and family histories and demographic information in Tourette’s syndrome. J Nerv Ment Dis 155(5):335–344

    CAS  PubMed  Google Scholar 

  13. Leckman JF, Price RA, Walkup JT et al (1987) Nongenetic factors in Gilles de la Tourette’s syndrome. Arch Gen Psychiatry 44(1):100

    CAS  PubMed  Google Scholar 

  14. Leckman JF, Dolnansky ES, Hardin MT et al (1990) Perinatal factors in the expression of Tourette’s syndrome: an exploratory study. J Am Acad Child Adolesc Psychiatry 29(2):220–226

    Article  CAS  PubMed  Google Scholar 

  15. Hyde TM, Aaronson BA, Randolph C et al (1992) Relationship of birth weight to the phenotypic expression of Gilles de la Tourette’s syndrome in monozygotic twins. Neurology 42(3):652–658

    CAS  PubMed  Google Scholar 

  16. Burd L, Severud R, Klug MG et al (1999) Prenatal and perinatal risk factors for Tourette disorder. J Perinat Med 27(4):295–302

    Article  CAS  PubMed  Google Scholar 

  17. Mathews CA, Bimson B, Lowe TL et al (2006) Association between maternal smoking and increased symptom severity in Tourette’s syndrome. Am J Psychiatry 163(6):1066–1073

    Article  PubMed  Google Scholar 

  18. Pringsheim T, Sandor P, Lang A et al (2009) Prenatal and perinatal morbidity in children with Tourette syndrome and attention-deficit hyperactivity disorder. J Dev Behav Pediatr 30(2):115–121

    Article  PubMed  Google Scholar 

  19. Bos-Veneman NG, Kuin A, Minderaa RB, Hoekstra PJ (2010) Role of perinatal adversities on tic severity and symptoms of attention deficit/hyperactivity disorder in children and adolescents with a tic disorder. J Dev Behav Pediatr 31(2):100–106

    Article  PubMed  Google Scholar 

  20. Ward AJ (1991) Prenatal stress and childhood psychopathology. Child Psychiatry Hum Dev 22:97–110

    Article  CAS  PubMed  Google Scholar 

  21. McIntosh DE, Mulkins RS, Dean RS (1995) Utilization of maternal perinatal risk indicators in the differential diagnosis of ADHD and UADD children. Int J Neurosci 81(1–2):35–46

    Article  CAS  PubMed  Google Scholar 

  22. Milberger S, Biederman J, Faraone SV et al (1998) Further evidence of an association between maternal smoking during pregnancy and attention deficit hyperactivity disorder: findings from a high-risk sample of siblings. J Clin Child Psychol 27(3):352–358

    Article  CAS  PubMed  Google Scholar 

  23. Mick E, Biederman J, Faraone SV et al (2002) Case-control study of attention-deficit hyperactivity disorder and maternal smoking, alcohol use, and drug use during pregnancy. J Am Acad Child Adolesc Psychiatry 41(4):378–385

    Article  PubMed  Google Scholar 

  24. Mick E, Biederman J, Prince J et al (2002) Impact of low birth weight on attention-deficit hyperactivity disorder. J Dev Behav Pediatr 23(1):16–22

    PubMed  Google Scholar 

  25. Huizink AC, de Medina PG, Mulder EJ et al (2002) Psychological measures of prenatal stress as predictors of infant temperament. J Am Acad Child Adolesc Psychiatry 41(9):1078–1085

    Article  PubMed  Google Scholar 

  26. Phares TM, Morrow B, Lansky A et al (2004) Surveillance for disparities in maternal health-related behaviors—selected states, Pregnancy Risk Assessment Monitoring System (PRAMS), 2000–2001. MMWR Surveill Summ 53(4):1–13

    PubMed  Google Scholar 

  27. Rodriguez A, Bohlin G (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46(3):246–254

    Article  PubMed  Google Scholar 

  28. Langley K, Rice F, van den Bree MB et al (2005) Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behaviour. Minerva Pediatr 57(6):359–371

    CAS  PubMed  Google Scholar 

  29. Grizenko N, Shayan YR, Polotskaia A et al (2008) Relation of maternal stress during pregnancy to symptom severity and response to treatment in children with ADHD. J Psychiatry Neurosci 33(1):10–16

    PubMed  Google Scholar 

  30. Boulet SL, Schieve LA, Boyle CA (2009) Birth weight and health and developmental outcomes in US children, 1997-2005. Matern Child Health J. 2009 Nov 10 [Epub ahead of print]

  31. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders: DSM-IV-TR, 4th edn. American Psychiatric Association, Washington, DC

    Google Scholar 

  32. Wechsler D (1991) Wechsler intelligence scale for children, 3rd edn (WISC-III). The Psychological Corporation, San Antonio, TX

    Google Scholar 

  33. Kaufman J, Birmaher B, Brent D et al (1997) Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36(7):980–988

    Article  CAS  PubMed  Google Scholar 

  34. Leckman JF, Sholomskas D, Thompson WD et al (1982) Best estimate of lifetime psychiatric diagnosis: a methodological study. Arch Gen Psychiatry 39(8):879–883

    CAS  PubMed  Google Scholar 

  35. Leckman JF, Riddle MA, Hardin MT et al (1989) The Yale global tic severity scale: initial testing of a clinician-rated scale of tic severity. J Am Acad Child Adolesc Psychiatry 28(4):566–573

    Article  CAS  PubMed  Google Scholar 

  36. DuPaul GJ (1991) Parent and teacher ratings of ADHD symptoms: psychometric properties in a community-based sample. J Clin Child Psychol 20:245–253

    Article  Google Scholar 

  37. Scahill L, Riddle MA, McSwiggin-Hardin M et al (1997) Children’s Yale-brown obsessive compulsive scale: reliability and validity. J Am Acad Child Adolesc Psychiatry 36(6):844–852

    Article  CAS  PubMed  Google Scholar 

  38. Reynolds CR, Richmond BO (1985) Revised children’s manifest anxiety scale (RCMAS), 3rd edn. Western Psychological Services, Washington, DC

    Google Scholar 

  39. Kovacs M (1992) Children’s depression inventory. Multi Health Systems, North Tonawanda, NY

    Google Scholar 

  40. Hollingshead A (1975) Four-factor index of social status. Yale University Press, New Haven

    Google Scholar 

  41. Walkup JT, Leckman JF (1988) Modified schedule for risk and protective factors early in development. Child Study Center, Yale University, New Haven

    Google Scholar 

  42. Vasconcelos MS, Sampaio AS, Hounie AG et al (2007) Prenatal, perinatal, and postnatal risk factors in obsessive-compulsive disorder. Biol Psychiatry 61(3):301–307

    Article  PubMed  Google Scholar 

  43. LeSage MG, Gustaf E, Dufek MB et al (2006) Effects of maternal intravenous nicotine administration on locomotor behaviour in preweanling rats. Pharmacol Biochem Behav 85:575–583

    Article  CAS  PubMed  Google Scholar 

  44. Gatzke-Kopp LM, Beauchaine TP (2007) Direct and passive prenatal nicotine exposure and the development of externalizing psychopathology. Child Psychiatry Hum Dev 38(4):255–269

    Article  PubMed  Google Scholar 

  45. Winzer-Serhan UH (2008) Long-term consequences of maternal smoking and developmental chronic nicotine exposure. Front Biosci 13:636–649

    Article  CAS  PubMed  Google Scholar 

  46. Knopik VS, Heath AC, Jacob T et al (2006) Maternal alcohol use disorder and offspring ADHD: disentangling genetic and environmental effects using a children-of-twins design. Psychol Med 36(10):1461–1471

    Article  PubMed  Google Scholar 

  47. Altink ME, Slaats-Willemse DI, Rommelse NN et al (2009) Effects of maternal and paternal smoking on attentional control in children with and without ADHD. Eur Child Adolesc Psychiatry 18(8):465–475

    Article  PubMed  Google Scholar 

  48. Thapar A, Rice F, Hay D, Boivin J et al (2009) Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry 66(8):722–727

    Article  CAS  PubMed  Google Scholar 

  49. Rice F, Harold GT, Boivin J, van den Bree M, Hay DF, Thapar A (2010) The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences. Psychol Med 40(2):335–345

    Article  CAS  PubMed  Google Scholar 

  50. Talge NM, Neal C, Glover V, Stress Early, Translational Research and Prevention Science Network: Fetal and Neonatal Experience on Child and Adolescent Mental Health (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry 48:245–261

    Article  PubMed  Google Scholar 

  51. Szyf M, McGowan P, Meaney MJ (2008) The social environment and the epigenome. Environ Mol Mutagen 49(1):46–60

    Article  CAS  PubMed  Google Scholar 

  52. O’Donnell K, O’Connor TG, Glover V (2009) Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Dev Neurosci 31(4):285–292

    Article  PubMed  Google Scholar 

  53. Corbett BA, Mendoza SP, Baym CL et al (2008) Examining cortisol rhythmicity and responsivity to stress in children with Tourette syndrome. Psychoneuroendocrinology 33(6):810–820

    Article  CAS  PubMed  Google Scholar 

  54. Freitag CM, Hänig S, Palmason H et al (2009) Cortisol awakening response in healthy children and children with ADHD: impact of comorbid disorders and psychosocial risk factors. Psychoneuroendocrinology 34(7):1019–1028

    Article  CAS  PubMed  Google Scholar 

  55. Bloch MH, Leckman JF, Zhu H, Peterson BS (2005) Caudate volumes in childhood predict symptom severity in adults with Tourette syndrome. Neurology 65:1253–1258

    Article  PubMed  Google Scholar 

  56. Martino D, Dale RC, Gilbert DL et al (2009) Immunopathogenic mechanisms in Tourette syndrome: a critical review. Mov Disord 24(9):1267–1279

    Article  PubMed  Google Scholar 

  57. Bombaci M, Grifantini R, Mora M et al (2009) Protein array profiling of tic patient sera reveals a broad range and enhanced immune response against Group A Streptococcus antigens. PLoS One 4(7):e6332

    Article  PubMed  Google Scholar 

  58. Tomeo CA, Rich-Edwards JW, Michels KB et al (1999) Reproducibility and validity of maternal recall of pregnancy related events. Epidemiology 10:774–777

    Article  CAS  PubMed  Google Scholar 

  59. Buka SL, Goldstein JM, Spartos E et al (2004) The retrospective measurement of prenatal and perinatal events: accuracy of maternal recall. Schizophr Res 71(2–3):417–426

    Article  PubMed  Google Scholar 

  60. Centers for Disease Control and Prevention (2004) Smoking during pregnancy—United States, 1990–2002. MMWR 53(39):911–915

    Google Scholar 

  61. Honein MA, Paulozzi LJ, Watkins ML (2001) Maternal smoking and birth defects: validity of birth certificate data for effect estimation. Public Health Rep 116(4):327–335

    Article  CAS  PubMed  Google Scholar 

  62. Meyer S, Raisig A, Gortner L et al (2009) In utero tobacco exposure: the effects of heavy and very heavy smoking on the rate of SGA infants in the Federal State of Saarland, Germany. Eur J Obstet Gynecol Reprod Biol 146(1):37–40

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was funded in part by the Tourette Syndrome Association, Children and Adults with Attention Deficit Disorder, Betsy Henley-Cohn, Sam Gejdenson, the Rembrandt Foundation, Echlin Foundation, and the Kaiser Family. This research was also supported by NIH Grants MH066187, P01MH049351 (JFL), K05 MH076273 (JFL), K02 MH01527 (PJL), K02 MH074677-01 (BSP), 1R01 MH066187-01A2 (HL), K01 MH079317 (YSK), R01 MH59139 (BSP) and RR00125. The authors also wish to thank Virginia Eicher for her invaluable assistance in completing this study.

Conflict of interest statement

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Child Study Center, Yale University School of Medicine, I-383-SHM, 230 South Frontage Road, New Haven, CT, 06520-7920, USA

    Maria G. Motlagh, Liliya Katsovich, Nancy Thompson, Haiqun Lin, Young-Shin Kim, Lawrence Scahill, Paul J. Lombroso, Robert A. King & James F. Leckman

  2. Columbia College of Physicians and Surgeons, The New York State Psychiatric Institute, New York, NY, USA

    Bradley S. Peterson

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  1. Maria G. Motlagh
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  2. Liliya Katsovich
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  3. Nancy Thompson
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  4. Haiqun Lin
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  5. Young-Shin Kim
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  6. Lawrence Scahill
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  8. Robert A. King
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  9. Bradley S. Peterson
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  10. James F. Leckman
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Correspondence to Maria G. Motlagh or James F. Leckman.

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Motlagh, M.G., Katsovich, L., Thompson, N. et al. Severe psychosocial stress and heavy cigarette smoking during pregnancy: an examination of the pre- and perinatal risk factors associated with ADHD and Tourette syndrome. Eur Child Adolesc Psychiatry 19, 755–764 (2010). https://doi.org/10.1007/s00787-010-0115-7

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