Abstract
Although maternal smoking during pregnancy has been shown to be associated with an increased risk of offspring attention-deficit/hyperactivity disorder (ADHD) in Western countries, there is no empirical evidence in non-Caucasian. Purpose of the present study is to examine the relationship between maternal smoking during pregnancy and offspring ADHD in Japanese population. A case–control study design was adopted. A total of 90 pairs of children with ADHD and mothers as well as 270 corresponding control pairs were recruited throughout the study period. A psychiatrist interviewed all the mothers of children with ADHD and control children and elicited information regarding their lifestyles during pregnancy, including active and passive smoking or drinking habits, as well as psychosocial and perinatal factors. Diagnosis of ADHD was made by each physician in charge according to DSM-IV diagnostic criteria. Logistic regression analysis was used to calculate odds ratios (OR) and 95% confidence intervals (CI) with adjustments for other possible confounding factors. Maternal active smoking during pregnancy was associated with an approximately twofold increased risk of offspring ADHD, even after adjusting for socioeconomic and perinatal confounding factors (OR 1.8 95% CI 0.9–3.6). However, the association was obviously attenuated when factors regarding parental psychopathological vulnerability were controlled (OR 1.3 95% CI 0.6–2.9). On the other hand, maternal passive smoking during pregnancy failed to show any material association with ADHD. These results suggested that a significant part of the association between maternal smoking during pregnancy, and ADHD might be explained by genetic factors including parental psychopathological vulnerability.
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Altink ME, Slaats-Willemse DI, Rommelse NN, Buschgens CJ, Fliers EA, Arias-Vásquez A, Xu X, Franke B, Sergeant JA, Faraone SV, Buitelaar JK (2009) Effects of maternal and paternal smoking on attentional control in children with and without ADHD. Eur Child Adolesc Psychiatry 18:465–475
Banerjee TD, Middleton F, Faraone SV (2007) Environmental risk factors for attention-deficit hyperactivity disorder. Acta Paediatr 96:1269–1274
Barkley RA (2006) Comorbid disorders, social and family adjustment, and subtype. In: Barkley RA (ed) Attention-deficit hyperactivity disorder, 3rd edn. The Guilford Press, New York, pp 184–218
Becker K, El-Faddagh M, Schmidt MH, Esser G, Laucht M (2008) Interaction of dopamine transporter genotype with prenatal smoke exposure on ADHD symptoms. J Pediatr 152:263–269
Biederman J (2005) Attention-deficit/hyperactivity disorder: a selective overview. Biol Psychiatry 57:1215–1220
Brookes KJ, Mill J, Guindalini C et al (2006) A common haplotype of the dopamine transporter gene associated with attention-deficit/hyperactivity disorder and interacting with maternal use of alcohol during pregnancy. Arch Gen Psychiatry 63:74–81
Brookes KJ, Xu X, Anney R et al (2008) Association of ADHD with genetic variants in the 5′-region of the dopamine transporter gene: evidence for allelic heterogeneity. Am J Med Genet B Neuropsychiatr Genet 147B:1519–1523
Coghill D, Rohde LA, Banaschewski T (2008) Attention-deficit/hyperactivity disorder. In: Banaschewski T, Rohde LA (eds) Biological child psychiatry. Recent trends and developments. Advances in biological psychiatry. Karger Press, Basel, pp 1–20
DiMaio S, Grizenko N, Joober R (2003) Dopamine genes and attention-deficit hyperactivity disorder: a review. J Psychiatry Neurosci 28:27–38
Fukuhara S, Suzukamo Y (2004) Manual of the SF-8 Japanese version. Institute for Health Outcomes & Process Evaluation Research, Kyoto (in Japanese)
Gillberg C (2006) Autism spectrum disorders. In: Gillberg C, Harrington R, Steinhausen HC (eds) A clinician’s handbook of child and adolescent psychiatry. Cambridge University Press, Cambridge, pp 447–488
Kagawa Y (2003) List of ingredients, digest version, 5th edn. Kagawa education institute of nutrition, Tokyo (in Japanese)
Knopik VS (2009) Maternal smoking during pregnancy and child outcomes: real or spurious effect? Dev Neuropsychol 34:1–36
Knopik VS, Sparrow EP, Madden PAF et al (2005) Contributions of parental alcoholism, prenatal substance exposure, and genetic transmission to child ADHD risk: a female twin study. Psychol Med 35:625–635
Kollins SH, McClernon FJ, Fuemmeler BF (2005) Association between smoking and attention-deficit/hyperactivity disorder symptoms in a population-based sample of adults. Arch Gen Psychiatry 62:1142–1147
Konofal E, Lecendreux M, Arnulf I, Mouren MC (2004) Iron deficiency in children with attention-deficit/hyperactivity disorder. Arch Pediatr Adolesc Med 158:1113–1115
Konofal E, Lecendreux M, Deron J et al (2008) Effects of iron supplementation on attention deficit hyperactivity disorder in children. Pediatr Neurol 38:20–26
Langley K, Rice F, Van Den Bree MBM, Thapar A (2005) Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behavior. Minerva Pediatr 57:359–371
Lehn H, Derks EM, Hudziak JJ, Heutink P, van Beijsterveldt TC, Boomsma DI (2007) Attention problems and attention-deficit/hyperactivity disorder in discordant and concordant monozygotic twins: evidence of environmental mediators. J Am Acad Child Adolesc Psychiatry 46:83–91
Leonard S, Adler LE, Benhammou K et al (2001) Smoking and mental illness. Pharmacol Biochem Behav 70:561–570
Linnet KM, Dalsgaard S, Obel C et al (2003) Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am J Psychiatry 160:1028–1040
Maughan B, Taylor A, Caspi A, Moffitt TE (2004) Prenatal smoking and early childhood conduct problems: testing genetic and environmental explanations of the association. Arch Gen Psychiatry 61:836–843
Mick E, Biederman J, Faraone SV, Sayer J, Kleinman S (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 41:378–385
Milberger S, Biederman J, Faraone SV, Chen L, Jones J (1996) Is Maternal smoking during pregnancy a risk factor for attention deficit hyperactivity disorder in children? Am J Psychiatry 153:1138–1142
Milberger S, Biederman J, Faraone SV, Jones J (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 27:352–358
Moura PJ, Lombroso PJ, Mercadante MT (2008) Autism. In: Banaschewski T, Rohde LA (eds) Biological child psychiatry. Recent trends and developments. Advances in biological psychiatry. Karger Press, Basel, pp 21–38
Neuman RJ, Lobos E, Reich W, Henderson CA, Sun LW, Todd RD (2007) Prenatal smoking exposure and dopaminergic genotypes interact to cause a severe ADHD subtype. Biol Psychiatry 61:1320–1328
Office for Life-Style Related Disease Control General Affairs Division Health Service Bureau, Ministry of Health, Labor and Welfare, Japan (2007) Smoking status. In: The National Health and Nutrition Survey in Japan, 2005. Ministry of Health, Labor and Welfare, Japan, Tokyo, pp 60 (in Japanese)
Paz R, Barsness B, Martenson T, Tanner D, Allan AM (2007) Behavioral teratogenicity induced by nonforced maternal nicotine consumption. Neuropsychopharmacol 32:693–699
Polanczyk G, de Lima MS, Horta BL, Biederman J, Rohde LA (2007) The worldwide prevalence of attention-deficit/hyperactivity disorder: a systematic review and meta-regression analyses. Am J Psychiatry 164:942–948
Rodriguez A, Gunilla B (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiat 46:246–254
Salin-Pascual RJ, Alcocer-Castillejos NV, Alejo-Galarza G (2003) Nicotine dependence and psychiatric disorders. Revista de investigación clínica 55:677–693 (in Spanish)
Satake H, Yamashita H, Yoshida K (2004) The family psychosocial characteristics of children with attention-deficit hyperactivity disorder with or without oppositional or conduct problems in Japan. Child Psychiatry Human Dev 34:219–235
Schmitz M, Denardin D, Silva TL, 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 45:1338–1345
Thapar A, Fowler T, Rice F, Scourfield J, van den Bree M, Thomas H, Harold G, Hay D (2003) Maternal smoking during pregnancy and attention deficit hyperactivity disorder symptoms in offspring. Am J Psychiatry 160:1985–1989
Tsuge M (2007) Special support education for students with Asperger’s syndrome. Nippon Rinsho 65:551–555 (in Japanese)
Williams JM, Ziedonis D (2004) Addressing tobacco among individuals with a mental illness or an addiction. Addict Behav 29:1067–1083
Yamasaki K (2003) ADHD-RS-IV Japanese versions. In: Kanbayashi Y, Saito K, Kita M (eds) Japanese guideline for the diagnosis and treatment of attention deficit hyperactivity disorder (ADHD). Jiho Press, Tokyo, pp 48–53 (in Japanese)
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This work was financially supported by a research grant from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (Grant No. 18590609) and from the Smoking Research Foundation.
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Members of the Wakayama ADHD Study Group are listed in the Appendix.
Appendix: Members of the Wakayama ADHD Study Group (in each affiliation)
Appendix: Members of the Wakayama ADHD Study Group (in each affiliation)
Nobuyuki Miyai, Kazuhisa Miyashita, Kouichi Yoshimasu † (Department of Hygiene, School of Medicine, Wakayama Medical University), Chikako Kiyohara (Department of Preventive Medicine, Graduate School of Medical Sciences, Kyushu University), Mina Booka, Asumi Higa, Genkichi Izumi, Takaomi Minami, Masakazu Miyawaki, Yuko Tsuda, Yoshinobu Tsuno, Tetsu Yoshimasu (Department of Pediatrics, Social Insrance Kinan Hospital), Shoichi Shibuta, Yuko Shima, Hiroyuki Suzuki, Takashi Takeuchi, Hiroko Togawa, Norishige Yoshikawa (Department of Pediatrics, School of Medicine, Wakayama Medical University), Shogo Kihira (Department of Pediatrics, Arita City Hospital), Eiko Honaga, Hiroshi Sato, Koji Toyonaga, Hinako Yamaguchi (Department of Neuropsychiatry, Osaka City General Hospital), Aki Kohno, Daisuke Nakanishi, Hiromichi Nakashima, Hisami Nishida, Kazuyuki Ohtsuki, Akira Yamamoto, Tomoko Yoshioka (Mie Prefectural Asunaro Hospital for Child and Adolescent Psychiatry), Harumi Kose, Kazuhiro Shinosaki (Department of Neuropsychiatry, School of Medicine, Wakayama Medical University), Hiroshi Yamashita (Department of Neuropsychiatry, Graduate School of Medical Sciences, Kyushu University), Junzo Iida (School of Nursing, Nara Medical University), Yoshiro Ono (Wakayama Prefecture Children and Disabled Persons’ Guidance Center), Toshihiko Yanagawa (School of Health and Nursing Sciences, Wakayama Medical University), Toshiko Juri (Department of Pediatrics, Kainan City Hospital), and Akira Miyamoto (Wakayama Prefectural Nanki Welfare Center).
† Principal investigator.
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Yoshimasu, K., Kiyohara, C., Minami, T. et al. Maternal smoking during pregnancy and offspring attention-deficit/hyperactivity disorder: a case–control study in Japan. ADHD Atten Def Hyp Disord 1, 223–231 (2009). https://doi.org/10.1007/s12402-009-0015-1
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DOI: https://doi.org/10.1007/s12402-009-0015-1