Abstract
Attention deficit hyperactivity disorder (ADHD) is a neurodevelopmental disorder which is caused by the interplay of genetic and environmental risk factors such as second-hand smoke (SHS). The association between postnatal exposure to SHS and ADHD risk in children was still inconclusive. We performed a systematic review and meta-analysis to explore the definite association. We searched for relevant studies from PubMed, Embase, Ovid, and Web of Science databases up to January 2020. We used random effect models to calculate pooled odds ratio (OR) with 95% confidence interval (CI). Subgroup analyses and sensitive analyses were also performed to solve the heterogeneity. According to our inclusion criteria, 9 studies including 6 cross-sectional studies, 2 cohort studies, and 1 case-control study were included in the final analysis. Postnatal exposure to SHS increased the risk of ADHD in children (OR: 1.60; 95% CI: 1.37–1.87). Children who exposed to SHS were found a slight risk for conduct problems (OR: 1.33, 95% CI: 1.00–1.77). Among the studies which used cotinine as a biomarker for SHS exposure, a lower pooled OR (OR = 1.16, 95%CI = 1.01, 1.33) was observed between cotinine and ADHD in children. Our meta-analysis results suggested that SHS exposure may be a risk factor for ADHD. We also found that SHS exposure may be associated with some adverse behavioral outcomes. More prospective studies should be conducted to confirm the relationship between SHS exposure and ADHD in children.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Association AP (1994) Diagnostic and statistical manual of mental disorders, fourth edition(DSM-IV) vol 42. Am Psych Ass
Bandiera FC, Richardson AK, Lee DJ, He J-P, Merikangas KR (2011) Secondhand smoke exposure and mental health among children and adolescents. Arch Pediatr Adolesc Med 165:332–338. https://doi.org/10.1001/archpediatrics.2011.30
Bauer NS, Anand V, Carroll AE, Downs SM (2015) Secondhand smoke exposure, parental depressive symptoms and preschool behavioral outcomes. J Pediatr Nurs 30:227–235. https://doi.org/10.1016/j.pedn.2014.06.004
Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101
Braun JM, Kahn RS, Froehlich T, Auinger P, Lanphear BP (2006) Exposures to environmental toxicants and attention deficit hyperactivity disorder in U.S. children. Environ Health Perspect 114:1904–1909. https://doi.org/10.1289/ehp.9478
Cho YJ, Choi R, Park S, J-w K (2018) Parental smoking and depression, and attention-deficit hyperactivity disorder in children and adolescents: Korean national health and nutrition examination survey 2005-2014. Asia Pac Psychiatry 10:e12327. https://doi.org/10.1111/appy.12327
Cole J, Ball HA, Martin NC, Scourfield J, McGuffin P (2009) Genetic overlap between measures of hyperactivity/inattention and mood in children and adolescents. J Am Acad Child Adolesc Psychiatry 48:1094–1101. https://doi.org/10.1097/CHI.0b013e3181b7666e
Counotte DS, Spijker S, van de Burgwal LH, Hogenboom F, Schoffelmeer ANM, de Vries TJ, Smit AB, Pattij T (2009) Long-lasting cognitive deficits resulting from adolescent nicotine exposure in rats. Neuropsychopharmacology 34:299–306. https://doi.org/10.1038/npp.2008.96
De Ridder A, De Graeve D (2006) Healthcare use, social burden and costs of children with and without ADHD in Flanders, Belgium. Clin Drug Investig 26:75–90. https://doi.org/10.2165/00044011-200626020-00003
DiFranza JR, Aligne CA, Weitzman M (2004) Prenatal and postnatal environmental tobacco smoke exposure and children's health. Pediatrics 113:1007–1015. https://doi.org/10.1542/peds.113.4.S1.1007
Dong T et al (2018) Prenatal exposure to maternal smoking during pregnancy and attention-deficit/hyperactivity disorder in offspring: a meta-analysis. Reprod Toxicol 76:63–70. https://doi.org/10.1016/j.reprotox.2017.12.010
Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot–based method of testing and adjusting for publication Bias in Meta-analysis. Biometrics 56:455–463. https://doi.org/10.1111/j.0006-341X.2000.00455.x
Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634. https://doi.org/10.1136/bmj.315.7109.629
Fergusson DM, Horwood LJ, Lynskey MT (1993) Maternal smoking before and after pregnancy: effects on behavioral outcomes in middle childhood. Pediatrics 92:815–840. https://doi.org/10.1203/00006450-199312000-00028
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–e1063. https://doi.org/10.1542/peds.2009-0738
Gehring U, Leaderer BP, Heinrich J, Oldenwening M, Giovannangelo MECA, Nordling E, Merkel G, Hoek G, Bellander T, Brunekreef B (2006) Comparison of parental reports of smoking and residential air nicotine concentrations in children. Occup Environ Med 63:766–772. https://doi.org/10.1136/oem.2006.027151
Goodman R (1997) The strengths and difficulties questionnaire: a research note. J Child Psychol Psychiatry 38:581–586. https://doi.org/10.1111/j.1469-7610.1997.tb01545.x
Heath CJ, Picciotto MR (2009) Nicotine-induced plasticity during development: modulation of the cholinergic system and long-term consequences for circuits involved in attention and sensory processing. Neuropharmacology 56(Suppl 1):254–262. https://doi.org/10.1016/j.neuropharm.2008.07.020
Herrmann M, King K, Weitzman M (2008) Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment. Curr Opin Pediatr 20:184–190. https://doi.org/10.1097/MOP.0b013e3282f56165
Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560. https://doi.org/10.1136/bmj.327.7414.557
Huang L, Wang Y, Zhang L, Zheng Z, Zhu T, Qu Y, Mu D (2018) Maternal smoking and attention-deficit/hyperactivity disorder in offspring: a meta-analysis. Pediatrics 141:e20172465. https://doi.org/10.1542/peds.2017-2465
Jarvis MJ, Russell MAH, Benowitz NL, Feyerabend C (1988) Elimination of cotinine from body fluids: implications for noninvasive measurement of tobacco smoke exposure. Am J Public Health 78:696–698. https://doi.org/10.2105/ajph.78.6.696
Joo H, Lim M-H, Ha M, Kwon H-J, Yoo SJ, Choi K-H, Paik K-C (2017) Secondhand smoke exposure and low blood lead levels in association with attention-deficit hyperactivity disorder and its symptom domain in children: a community-based case-control study. Nicotine Tob Res 19:19–101. https://doi.org/10.1093/ntr/ntw152
Kabir Z, Connolly GN, Alpert HR (2011) Secondhand smoke exposure and neurobehavioral disorders among children in the United States. Pediatrics 128:263–270. https://doi.org/10.1542/peds.2011-0023
Kim KM, Lim MH, Kwon H-J, Yoo S, Kim JW, Ha M, Paik K (2018) Associations between urinary cotinine and symptoms of attention deficit/hyperactivity disorder and autism spectrum disorder. Environ Res 166:481–486. https://doi.org/10.1016/j.envres.2018.06.018
Klein RG, Mannuzza S, Olazagasti MAR, Roizen E, Hutchison JA, Lashua EC, Castellanos FX (2012) Clinical and functional outcome of childhood attention-deficit/hyperactivity disorder 33 years later. Arch Gen Psychiatry 69:1295–1303. https://doi.org/10.1001/archgenpsychiatry.2012.271
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 behaviour. A review. Minerva Pediatr 57:359–371
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700. https://doi.org/10.1136/bmj.b2700
Lichtenstein P, Carlström E, Råstam M, Gillberg C, Anckarsäter H (2010) The genetics of autism spectrum disorders and related neuropsychiatric disorders in childhood. Am J Psychiatry 167:1357–1363. https://doi.org/10.1176/appi.ajp.2010.10020223
Max W, Sung H-Y, Shi Y (2013) Attention deficit hyperactivity disorder among children exposed to secondhand smoke: a logistic regression analysis of secondary data. Int J Nurs Stud 50:797–806. https://doi.org/10.1016/j.ijnurstu.2012.10.002
Minatoya M, Araki A, Itoh S, Yamazaki K, Kobayashi S, Miyashita C, Sasaki S, Kishi R (2019) Prenatal tobacco exposure and ADHD symptoms at pre-school age: the Hokkaido Study on Environment and Children’s Health. Environ Health Prev Med 24:74. https://doi.org/10.1186/s12199-019-0834-4
Obel C, Zhu JL, Olsen J, Breining S, Li J, Grønborg TK, Gissler M, Rutter M (2016) The risk of attention deficit hyperactivity disorder in children exposed to maternal smoking during pregnancy - a re-examination using a sibling design. J Child Psychol Psychiatry 57:532–537. https://doi.org/10.1111/jcpp.12478
Oberg M, Jaakkola MS, Woodward A, Peruga A, Prüss-Ustün A (2011) Worldwide burden of disease from exposure to second-hand smoke: a retrospective analysis of data from 192 countries. Lancet 377:139–146. https://doi.org/10.1016/S0140-6736(10)61388-8
Padrón A, Galán I, García-Esquinas E, Fernández E, Ballbè M, Rodríguez-Artalejo F (2016) Exposure to secondhand smoke in the home and mental health in children: a population-based study. Tob Control 25:307–312. https://doi.org/10.1136/tobaccocontrol-2014-052077
Pagani LS (2014) Environmental tobacco smoke exposure and brain development: the case of attention deficit/hyperactivity disorder. Neurosci Biobehav Rev 44:195–205. https://doi.org/10.1016/j.neubiorev.2013.03.008
Preedy VR, Watson RR (2010) ICD-9. In: Handbook of disease burdens and quality of life measures. Springer, New York, pp 4232–4232
Rostom A DC, Cranney A (2004) Celiac disease: summary. In: Rockville (MD): Agency for Healthcare Research and Quality (US)
Rückinger S, Rzehak P, Chen CM, Sausenthaler S, Koletzko S, Bauer CP, Hoffmann U, Kramer U, Berdel D, von Berg A, Bayer O, Wichmann HE, von Kries R, Heinrich J, GINI-plus Study Group (2010) Prenatal and postnatal tobacco exposure and behavioral problems in 10-year-old children: results from the GINI-plus prospective birth cohort study. Environ Health Perspect 118:150–154. https://doi.org/10.1289/ehp.0901209
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 45:1338–1345. https://doi.org/10.1097/S0890-8567(09)61916-X
Seccareccia F, Zuccaro P, Pacifici R, Meli P, Pannozzo F, Freeman KM, Santaquilani A, Giampaoli S (2003) Serum cotinine as a marker of environmental tobacco smoke exposure in epidemiological studies: the experience of the MATISS project. Eur J Epidemiol 18:487–492. https://doi.org/10.1023/A:1024672522802
Slotkin TA, Pinkerton KE, Seidler FJ (2006) Perinatal environmental tobacco smoke exposure in rhesus monkeys: critical periods and regional selectivity for effects on brain cell development and lipid peroxidation. Environ Health Perspect 114:34–39. https://doi.org/10.1289/ehp.8286
Sourander A, Sucksdorff M, Chudal R, Surcel HM, Hinkka-Yli-Salomäki S, Gyllenberg D, Cheslack-Postava K, Brown AS (2019) Prenatal cotinine levels and ADHD among offspring. Pediatrics 143:e20183144. https://doi.org/10.1542/peds.2018-3144
Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605. https://doi.org/10.1007/s10654-010-9491-z
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiologyA proposal for reporting. JAMA 283:2008–2012. https://doi.org/10.1001/jama.283.15.2008
Thapar A, Holmes J, Poulton K, Harrington R (1999) Genetic basis of attention deficit and hyperactivity. Br J Psychiatry 174:105–111. https://doi.org/10.1192/bjp.174.2.105
Thapar A, Harrington R, McGuffin P (2001) Examining the comorbidity of ADHD-related behaviours and conduct problems using a twin study design. Br J Psychiatry 179:224–229. https://doi.org/10.1192/bjp.179.3.224
Thapar A, Langley K, Asherson P, Gill M (2007) Gene-environment interplay in attention-deficit hyperactivity disorder and the importance of a developmental perspective. Br J Psychiatry 190:1–3. https://doi.org/10.1192/bjp.bp.106.027003
Thapar A, Cooper M, Jefferies R, Stergiakouli E (2012) What causes attention deficit hyperactivity disorder? Arch Dis Child 97:260–265. https://doi.org/10.1136/archdischild-2011-300482
Tiesler CMT, Chen CM, Sausenthaler S, Herbarth O, Lehmann I, Schaaf B, Krämer U, von Berg A, von Kries R, Wichmann HE, Heinrich J, LISA Study Group (2011) Passive smoking and behavioural problems in children: results from the LISAplus prospective birth cohort study. Environ Res 111:1173–1179. https://doi.org/10.1016/j.envres.2011.06.011
Tistarelli N, Fagnani C, Troianiello M, Stazi MA, Adriani W (2020) The nature and nurture of ADHD and its comorbidities: a narrative review on twin studies. Neurosci Biobehav Rev 109:63–77. https://doi.org/10.1016/j.neubiorev.2019.12.017
Torres S, Merino C, Paton B, Correig X, Ramírez N (2018) Biomarkers of exposure to secondhand and thirdhand tobacco smoke: recent advances and future perspectives. Int J Environ Res Public Health 15. https://doi.org/10.3390/ijerph15122693
Twardella D, Bolte G, Fromme H, Wildner M, von Kries R (2010) Exposure to secondhand tobacco smoke and child behaviour - results from a cross-sectional study among preschool children in Bavaria. Acta Paediatr 99:106–111. https://doi.org/10.1111/j.1651-2227.2009.01522.x
Wang H, Li F, Zhang Y, Jiang F, Zhang J (2019) The association between exposure to secondhand smoke and psychological symptoms among Chinese children. BMC Public Health 19:923. https://doi.org/10.1186/s12889-019-7006-8
Weitzman M, Gortmaker S, Sobol A (1992) Maternal smoking and behavior problems of children. Pediatrics 90:342–349
Wong ICK, Banaschewski T, Buitelaar J, Cortese S, Döpfner M, Simonoff E, Coghill D (2019) Emerging challenges in pharmacotherapy research on attention-deficit hyperactivity disorder-outcome measures beyond symptom control and clinical trials. Lancet Psychiatry 6:528–537. https://doi.org/10.1016/S2215-0366(19)30096-3
Funding
This study was funded by Shantou Science and Technology Project (No. 190827075265313, 190823105264087, 2019ST005).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 711 kb).
Rights and permissions
About this article
Cite this article
Huang, A., Wu, K., Cai, Z. et al. Association between postnatal second-hand smoke exposure and ADHD in children: a systematic review and meta-analysis. Environ Sci Pollut Res 28, 1370–1380 (2021). https://doi.org/10.1007/s11356-020-11269-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-11269-y