Maternal cigarette smoking and child psychiatric morbidity: a longitudinal study
Abstract
Objective. Previous studies have linked maternal smoking during pregnancy with behavioral disturbance in children. However, additional evidence is needed to address the causality of the relationship. The present study analyses result from an Australian cohort of 5342 5-year-old children whose mothers were recruited early in pregnancy. Methods. Smoking history was gathered for prepregnancy, first clinic visit (FCV), late pregnancy, and when the child was 6 months and 5 years of age. Behavior problems at the age of 5 were assessed using a modified Child Behavior Check List (CBCL) shown to have high agreement with the complete CBCL. This resulted in the formation of three scales: internalizing; social, attentional and thought; and externalizing behavior problems, which were then dichotimized at the 90th percentile in each case. Logistic regression was used to model these outcomes as a function of maternal smoking at five time points during which it was assessed. A series of models explored the effect of additional adjustment for confounding. The predictors of attrition (29.5%) throughout the cohort were also identified by multivariate modeling. Results. The final analysis was carried out on a cohort of mother-child pairs for whom data and child behavior outcomes were complete. The mean age of children was 5 years, 6 months with a range from 4 to 6 years. The mean age of mothers at the time of birth of the child was 25 years, with a range from 13 to 47 years. Mothers lost to follow-up were more likely to be younger, single, and less well-educated than those who continued participation, although maternal smoking was not an independent determinant. Unadjusted analyses showed strong associations between externalizing child behavior and maternal smoking during pregnancy and at the 5-year follow-up, with relative risks (RRs) up to 2.6 for children of women smoking at least 20 cigarettes per day at the first antenatal clinic visit. A clear dose-response relationship existed in most relationships with higher levels of smoking being associated with higher rates of externalizing behavior problems. Weaker relationships occurred for internalizing behavior and social, attentional and thought behavior problems. Multivariate analysis of the timing in more detail that the association between maternal smoking and child behavior problems persisted, although the evidence for dose-response diminished. Moreover, it was primarily associated with smoking as determined by questions asked at the FCV (RR = 1.52, 2.03, 2.16) for 1 to 9, 10 to 19, and ≥20 cigarettes per day, respectively, compared with nonsmoking and secondarily by smoking determined at the 5-year follow-up (RR = 1.52, 1.87, 1.29) for 1 to 9, 10 to 19, and ≥20 cigarettes per day respectively, compared with nonsmoking. This association appeared to be independent of a wide range of possible confounders such as maternal age, education, social class, marital status and mental health, gestation at FCV, complications during pregnancy, the child's sex, gestational age at birth, and age at last follow-up. Adjustments were also made for the mother's employment since birth, family structure, and maternal mental health at the time of the CBCL assessment. Associations between externalizing behavior problems and maternal smoking at other times, and those between other behavioral problems examined and maternal smoking were not significant. Conclusion. Although previous studies have found evidence for an association between maternal smoking and child behavior problems, the strength of this study lies in its size, its detailed and consistent measurement of maternal smoking, and its ability to control for many social and biological factors linked to maternal smoking and child behavior. The statistical evidence for a causal relationship between maternal smoking as measured at the first antenatal clinic visit and the development of externalizing behavior in children is strongly suggestive, because of the specificity of effect and timing, and the adjustment for a comprehensive range of other risk factors. An alternative explanation that mothers who smoke might be inclined to report behavior problems differently was considered unlikely because the effect was specific to externalizing behavior and the major exposure occurred 5 years before the reported behavior. Additionally, the existence of a factor (beyond those already included in the analysis) that might be related to both behavior problems and any propensity to misreport smoking seems sufficiently implausible to rule out misclassification of smoking status as another alternative explanation for the findings. The timing of the relationship between smoking in pregnancy and externalizing behavior problems, and its independence of small for gestational age status at birth, suggests that placental insufficiency and oxygen deprivation are not important in the pathogenesis. It is possible that nicotine in the fetal brain derived from maternal
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Cites
- STATISTICAL PACKAGE FOR SOCIAL SCIENCES
Reddy, M. V. (2014) · Apple Academic Press eBooks · doi:10.1201/b17560-26 · Cited by 12,121 · see citing works
(1983) · Medical Entomology and Zoology · Cited by 4,251 · see citing works
Achenbach, T. M., & EDELBROCK, C. S. (1981) · Monographs of the Society for Research in Child Development · doi:10.2307/1165983 · Cited by 1,690 · see citing works
An Introduction to Sample Selection Bias in Sociological Data
Berk, R. A. (1983) · American Sociological Review · doi:10.2307/2095230 · Cited by 1,213 · see citing works
Laurie, D., Wisden, W., & Seeburg, P. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04151.1992 · Cited by 1,144 · see citing works
Statistical Methods in Epidemiology
(2012) · Springer eBooks · doi:10.1007/springerreference_205629 · Cited by 1,123 · see citing works
インターグループ (1986) · Medical Entomology and Zoology · Cited by 809 · see citing works
Developmental-Behavioral Pediatrics
(2008) · Elsevier eBooks · doi:10.1016/b978-0-323-04025-9.x5001-6 · Cited by 374 · see citing works
Maternal smoking and behavior problems of children.
Weitzman, M., Gortmaker, S., & Sobol, A. (1992) · Pediatrics · doi:10.1542/peds.90.3.342 · Cited by 311 · see citing works
Keeping, J. D., Najman, J. M., MORRISON, J., Western, J., Andersen, M. J., & Williams, G. M. (1989) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1989.tb02388.x · Cited by 255 · see citing works
Self-citationMental development of children whose mothers smoked during pregnancy.
Naeye, R. L., & Peters, E. C. (1984) · PubMed · Cited by 227 · see citing works
Maternal Smoking Before and After Pregnancy: Effects on Behavioral Outcomes in Middle Childhood
Fergusson, D. M., Horwood, L. J., & Lynskey, M. T. (1993) · PEDIATRICS · doi:10.1542/peds.92.6.815 · Cited by 205 · see citing works
The reliability of self-reported cigarette consumption in the United States.
Hatziandreu, E. J., Pierce, J. P., Fiore, M. C., Grise, V. N., Novotny, T. E., & Davis, R. M. (1989) · American Journal of Public Health · doi:10.2105/ajph.79.8.1020 · Cited by 155 · see citing works
SMOKING DURING PREGNANCY AND ITS EFFECTS ON THE FETUS
Cole, P. V., Hawkins, L., & Roberts, D. J. (1972) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1972.tb12920.x · Cited by 144 · see citing works
Hyperkinesis and Maternal Smoking
Denson, R., Nanson, J., & Mcwatters, M. A. (1975) · Canadian Psychiatric Association Journal · doi:10.1177/070674377502000302 · Cited by 111 · see citing works
Rantakallio, P. T., Läärä, E., Isohanni, M. K., & Moilanen, I. K. (1992) · International Journal of Epidemiology · doi:10.1093/ije/21.6.1106 · Cited by 101 · see citing works
Maternal smoking during pregnancy affects children's vigilance performance
Kristjansson, E., Fried, P. A., & Watkinson, B. (1989) · Drug and Alcohol Dependence · doi:10.1016/0376-8716(89)90003-3 · Cited by 100 · see citing works
Strecher, V. J., Becker, M. H., Clark, N. M., & Prasada-Rao, P. (1989) · Journal of General Internal Medicine · doi:10.1007/bf02602359 · Cited by 72 · see citing works
Validity of cigarette smoking habits in three epidemiologic studies in Utah
Slattery, M. L., Hunt, S. C., French, T. K., Ford, M. H., & Williams, R. R. (1989) · Preventive Medicine · doi:10.1016/0091-7435(89)90050-9 · Cited by 47 · see citing works
Class Change in the Personal Illness Hierarchy
Foulds, G. A., Bedford, A., & Csapo, K. G. (1975) · The British Journal of Psychiatry · doi:10.1192/bjp.127.4.316 · Cited by 27 · see citing works
A Replication Study of Foulds' and Bedford's Hierarchical Model of Depression
Bagshaw, V. E., & Bagshaw, V. E. (1977) · The British Journal of Psychiatry · doi:10.1192/bjp.131.1.53 · Cited by 27 · see citing works
A Test of the Hierarchical Model of Personal Illness
McPherson, F. M., Antram, M., Bagshaw, V. E., et al. (1977) · The British Journal of Psychiatry · doi:10.1192/bjp.131.1.56 · Cited by 25 · see citing works
Static encephalopathies of infancy and childhood
Miller, G., & Ramer, J. C. (1992) · Raven Press eBooks · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Linnet, K. M., Dalsgaard, S., Obel, C., Wisborg, K., Henriksen, T. B., Rodriguez, A., Kotimaa, A., Moilanen, I., Thomsen, P. H., Olsen, J., et al. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.6.1028 · Cited by 778 · see citing works
Exposures to environmental toxicants and attention deficit hyperactivity disorder in U.S. children
Braun, J. M., Kahn, R. S., Froehlich, T., Auinger, P., & Lanphear, B. P. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.9478 · Cited by 573 · see citing works
Huizink, A. C., & Mulder, E. J. H. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.005 · Cited by 468 · see citing works
Maternal lifestyle and environmental risk factors for autism spectrum disorders
Lyall, K., Schmidt, R. J., & Hertz-Picciotto, I. (2014) · International Journal of Epidemiology · doi:10.1093/ije/dyt282 · Cited by 427 · see citing works
Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review
Wakschlag, L. S., Pickett, K. E., Cook, E., Benowitz, N. L., & Leventhal, B. L. (2002) · American Journal of Public Health · doi:10.2105/ajph.92.6.966 · Cited by 371 · see citing works
Exposure to environmental tobacco smoke and cognitive abilities among u.S. Children and adolescents
Yolton, K., Dietrich, K., Auinger, P., Lanphear, B. P., & Hornung, R. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7210 · Cited by 331 · see citing works
Nicotine and the adolescent brain: insights from an animal model
Slotkin, T. (2002) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(02)00199-x · Cited by 284 · see citing works
King, S., Dancause, K., Turcotte‐Tremblay, A., Veru, F., & Laplante, D. P. (2012) · Birth Defects Research Part C: Embryo Today: Reviews · doi:10.1002/bdrc.21026 · Cited by 232 · see citing works
Association of tobacco and lead exposures with attention-deficit/hyperactivity disorder
Froehlich, T. E., Lanphear, B. P., Auinger, P., Hornung, R., Epstein, J. N., Braun, J., & Kahn, R. S. (2009) · Pediatrics · doi:10.1542/peds.2009-0738 · Cited by 234 · see citing works
Trauth, J. A., Seidler, F. J., McCook, E. C., & Slotkin, T. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01994-0 · Cited by 230 · see citing works
Larsson, M., Weiss, B., Janson, S., Sundell, J., & Bornehag, C.-G. (2009) · NeuroToxicology · doi:10.1016/j.neuro.2009.01.011 · Cited by 184 · see citing works
England, L. J., Aagaard, K., Bloch, M., Conway, K., Cosgrove, K., Grana, R., Gould, T. J., Hatsukami, D., Jensen, F., Kandel, D., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.11.013 · Cited by 181 · see citing works
Whitaker, R. C., Orzol, S. M., & Kahn, R. S. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.5.551 · Cited by 175 · see citing works
Jacobsen, L. K., Slotkin, T. A., Mencl, W. E., Frost, S. J., & Pugh, K. R. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301398 · Cited by 144 · see citing works
Maternal smoking during pregnancy and child behaviour problems: The Generation R Study
Roza, S. J., Verhulst, F. C., Jaddoe, V. W., Steegers, E. A., Mackenbach, J. P., Hofman, A., & Tiemeier, H. (2009) · International Journal of Epidemiology · doi:10.1093/ije/dyn163 · Cited by 118 · see citing works
Maternal smoking during pregnancy and bipolar disorder in offspring
Talati, A., Bao, Y., Kaufman, J., Shen, L., Schaefer, C. A., & Brown, A. S. (2013) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.12121500 · Cited by 104 · see citing works
Prenatal smoking exposure and psychiatric symptoms in adolescence
Indredavik, M. S., Brubakk, A., Romundstad, P., & Vik, T. (2007) · Acta Paediatrica · doi:10.1111/j.1651-2227.2006.00148.x · Cited by 101 · see citing works
Moylan, S., Gustavson, K., Øverland, S., Karevold, E. B., Jacka, F. N., Pasco, J. A., & Berk, M. (2015) · BMC Medicine · doi:10.1186/s12916-014-0257-4 · Cited by 87 · see citing works
Carter, S., Paterson, J., Gao, W., & Iusitini, L. (2008) · Early Human Development · doi:10.1016/j.earlhumdev.2007.03.009 · Cited by 41 · see citing works
Varvarigou, A. A., Liatsis, S. G., Vassilakos, P., Decavalas, G., & Beratis, N. G. (2009) · Journal of Perinatal Medicine · doi:10.1515/jpm.2009.028 · Cited by 41 · see citing works
Effects of pre-and neonatal nicotine exposure in rodents: inconsistent evidence
Sobrian, S. K., & Holson, R. R. (2011) · ILAR Journal · doi:10.1093/ilar.52.3.251 · Cited by 8 · see citing works
- Authors
- Williams, G. M., O'Callaghan, M., Najman, J. M., Bor, W., Andersen, F. M. J., Richards, A. D., & BSc, C. U.
- Affiliations
- From the Australian Centre for International and Tropical Health and Nutrition and Departments of
- Mater Misericordiae Hospital (AU)
- Anthropology and Sociology and
- University of Nottingham (GB)
- Academic Division of Child Health, School of Human Development, University of Nottingham, United Kingdom.
- Venue
- PEDIATRICS
- Publisher
- American Academy of Pediatrics (AAP)
- Published
- 1998-07-01
- Volume
- 102
- Issue
- 1
- Pages
- e11-e11
- ISSN
- 0031-4005 (ISSN-L)
- 1098-4275
- OpenAlex
- W2157982108
- Cited by
- 203
- References
- 23
- Citations by year
- 2025: 1 · 2023: 1 · 2022: 1 · 2021: 19 · 2020: 1 · 2019: 2 · 2018: 4 · 2017: 6 · 2016: 8 · 2015: 9 · 2014: 12 · 2013: 7 · 2012: 7
- FWCI
- 3.86
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- PEDIATRICS (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- smoking during pregnancy, child behavior problems, externalizing problems, internalizing problems, prenatal tobacco exposure, dose-response relationship, Child Behavior Checklist, mother-child cohort, smoking cessation during pregnancy, confounding adjustment
- MeSH terms
- Adolescent, Adult, Australia, Mental Disorders, Child, Preschool, Educational Status, Female, Follow-Up Studies, Humans, Longitudinal Studies, Maternal Age, Middle Aged, Pregnancy, Prenatal Exposure Delayed Effects, Risk Factors, Smoking, Cohort Studies, Multivariate Analysis, Logistic Models
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review