Mother׳s environmental tobacco smoke exposure during pregnancy and externalizing behavior problems in children
Open accessAbstract
Background While the impact of active maternal smoking during pregnancy on child health has been well investigated, the association between maternal passive smoking, or environmental tobacco smoke (ETS), or second-hand smoke, and behavioral development of offspring is less clear. This study examines the association between maternal ETS exposure during pregnancy and child behavior problems.Methods Cross-sectional data of 646 mother-child pairs from the Jintan China Cohort Study were used in the analyses. Mother's exposure to tobacco smoking at home, the workplace, and other places during pregnancy (for the determination of maternal ETS exposure) and children's behaviors (via Child Behavior Checklist) were assessed when the children were 5-6 years old. Logistic regression models were constructed to examine associations between maternal exposure to ETS during pregnancy and internalizing and externalizing behavior problems, adjusting for potential cofounders including child sex and parental characteristics.Results 37% of mothers reported ETS during pregnancy. Children of mothers exposed to ETS during pregnancy had higher scores for externalizing and total behavior problems, with 25% of children whose mothers were exposed to ETS compared to 16% of children of unexposed mothers. After adjusting for potential confounders, ETS exposure was associated with a higher risk of externalizing behavior problems in offspring of exposed mothers (OR=2.08, 95% confidence interval [CI] 1.27-3.43). Analysis after multiple imputations and sensitivity analysis further verified the association, but no dose-response relationship was found. ETS exposure, however, was not associated with internalizing or total behavior problems.Conclusion This study suggests that maternal ETS exposure during pregnancy may impact child behavioral development, particularly externalizing behaviors.
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Secondhand smoke is a different chemical mixture than primary smoke, has evidence of neurodevelopmental toxicity, and is a very common exposure.
“secondhand smoke is a different chemical mixture than primary smoke, (2) there is evidence that secondhand smoke exhibits neurodevelopmental toxicity,61,62 and (3) it is a very common exposure.”
From Environmental Chemical Exposures and Autism Spectrum Disorders: A Review of the Epidemiological Evidence (2014) · cites this paper as [61]
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Raine, A., Ishikawa, S. S., Arce, E., Lencz, T., Knuth, K. H., Bihrle, S., LaCasse, L., & Colletti, P. M. (2004) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00727-3 · Cited by 213 · cited 1× · see citing works
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“…during pregnancy is associated with child behavior problems, such as attention deficit and hyperactivity disorder (ADHD) (Button et al., 2005; Fergusson et al., 1993; Hutchinson et al., 2010; Kotimaa et al., 2003; Linnet et al., 2005; Milberger et al., 1996, 1998; Tiesler et al., 2011),…”
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Kotimaa, A., Moilanen, I. K., Taanila, A. M., Ebeling, H. E., Smalley, S. L., McGough, J. J., Hartikainen, A., & Järvelin, M. (2003) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000046866.56865.a2 · Cited by 161 · cited 3× · see citing works
“direct intake of tobacco through cigarettes) during pregnancy is associated with child behavior problems, such as attention deficit and hyperactivity disorder (ADHD) (Button et al., 2005; Fergusson et al., 1993; Hutchinson et al., 2010; Kotimaa et al., 2003; Linnet et al., 2005; Milberger et al., 1996, 1998; Tiesler e…”
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“Detailed sampling and research procedures of this larger cohort study have been described elsewhere (Liu et al., 2011b, 2010).”
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“Three studies included less than 200 mother–child pairs and found that child prenatal exposure through maternal ETS exposure was related to a higher risk of aggression and externalizing behavior problems (Gatzke-Kopp and Beauchaine, 2007; Hsieh et al., 2010; Makin et al., 1991).”
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Linnet, K. M., Wisborg, K., Obel, C., Secher, N. J., Thomsen, P. H., Agerbo, E., & Henriksen, T. B. (2005) · PEDIATRICS · doi:10.1542/peds.2004-2054 · Cited by 142 · cited 3× · see citing works
“direct intake of tobacco through cigarettes) during pregnancy is associated with child behavior problems, such as attention deficit and hyperactivity disorder (ADHD) (Button et al., 2005; Fergusson et al., 1993; Hutchinson et al., 2010; Kotimaa et al., 2003; Linnet et al., 2005; Milberger et al., 1996, 1998; Tiesler e…”
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“direct intake of tobacco through cigarettes) during pregnancy is associated with child behavior problems, such as attention deficit and hyperactivity disorder (ADHD) (Button et al., 2005; Fergusson et al., 1993; Hutchinson et al., 2010; Kotimaa et al., 2003; Linnet et al., 2005; Milberger et al., 1996, 1998; Tiesler e…”
BackgroundMaternal 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 · cited 4× · see citing works
“…used paternal indoor smoking as an indicator of maternal ETS exposure (i.e. workplace and other exposures were excluded) and found an association between ETS exposure and child externalizing behavior problems (assessed using the CBLC) after adjusting for children’s age and sex (Roza et al., 2009).”
BackgroundMethodResultInfluentialEarly health risk factors for violence: Conceptualization, evidence, and implications
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“Tobacco smoke contains thousands of chemical compounds, and many of these compounds are known neurotoxicants (Liu and Wuerker, 2005; Liu, 2011).”
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“The CBCL includes measures of seven syndromes: anxiety/depression, emotional reaction, withdrawn, somatic complaints, sleep problems, attention problems, and aggression.”
BackgroundResultInfluentialChild Behavior Problems Increased by Maternal Smoking During Pregnancy
Orlebeke, J. F., Knol, D. L., & Verhulst, F. C. (1999) · Archives of Environmental Health An International Journal · doi:10.1080/00039899909602231 · Cited by 100 · cited 2× · see citing works
“…problems (Fergusson et al., 1993; Wakschlag et al., 1997, 2006), aggression, and other externalizing behaviors (Boutwell et al., 2011; Brook et al., 2006; Fergusson et al., 1998; Huijbregts et al., 2008; Orlebeke et al., 1997, 1999), as well as adult criminal behavior (Brennan et al., 1999).”
BackgroundResultIs Prenatal Smoking Associated With a Developmental Pattern of Conduct Problems in Young Boys?
Wakschlag, L. S., Pickett, K. E., Kasza, K., & Loeber, R. (2006) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000198597.53572.3e · Cited by 97 · cited 1× · see citing works
“…al., 2010; Kotimaa et al., 2003; Linnet et al., 2005; Milberger et al., 1996, 1998; Tiesler et al., 2011), conduct problems (Fergusson et al., 1993; Wakschlag et al., 1997, 2006), aggression, and other externalizing behaviors (Boutwell et al., 2011; Brook et al., 2006; Fergusson et al., 1998;…”
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Increase in Child Behavior Problems Resulting from Maternal Smoking during Pregnancy
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“…problems (Fergusson et al., 1993; Wakschlag et al., 1997, 2006), aggression, and other externalizing behaviors (Boutwell et al., 2011; Brook et al., 2006; Fergusson et al., 1998; Huijbregts et al., 2008; Orlebeke et al., 1997, 1999), as well as adult criminal behavior (Brennan et al., 1999).”
BackgroundResultMaternal prenatal smoking, parental antisocial behavior, and early childhood physical aggression
Huijbregts, S. C. J., Séguin, J. R., Zoccolillo, M., Boivin, M., & Tremblay, R. E. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000217 · Cited by 89 · cited 4× · see citing works
“, 1997, 2006), aggression, and other externalizing behaviors (Boutwell et al., 2011; Brook et al., 2006; Fergusson et al., 1998; Huijbregts et al., 2008; Orlebeke et al., 1997, 1999), as well as adult criminal behavior (Brennan et al.”
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Liu, J., McCauley, L., Zhao, Y., Zhang, H., Pinto‐Martin, J. A., & Jintan Cohort Study Group (2009) · International Journal of Epidemiology · doi:10.1093/ije/dyp205 · Cited by 84 · cited 2× · see citing works
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“Tobacco smoke contains thousands of chemical compounds, and many of these compounds are known neurotoxicants (Liu and Wuerker, 2005; Liu, 2011).”
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O'Connor, R. J., Li, Q., Stephens, W. E., Hammond, D., Elton‐Marshall, T., Cummings, K. M., Giovino, G. A., & Fong, G. T. (2010) · Tobacco Control · doi:10.1136/tc.2009.030163 · Cited by 65 · cited 1× · see citing works
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BackgroundA questionnaire for assessing environmental tobacco smoke exposure
Nondahl, D. M., Cruickshanks, K. J., & Schubert, C. R. (2004) · Environmental Research · doi:10.1016/j.envres.2004.02.005 · Cited by 61 · cited 1× · see citing works
“The validity of self-reported ETS exposure is still a concern, although some studies, particularly recent studies in Asia, have found this methodology acceptable and useful (Chiu et al., 2008; Kaufman et al., 2002; Nondahl et al., 2005).”
ResultLiu, J., Raine, A., Wuerker, A. K., Venables, P. H., & Mednick, S. A. (2009) · Journal of Research on Adolescence · doi:10.1111/j.1532-7795.2009.00583.x · Cited by 60 · cited 1× · see citing works
“Birth complications have also been linked to externalizing behavior (Liu et al., 2009).”
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“direct intake of tobacco through cigarettes) during pregnancy is associated with child behavior problems, such as attention deficit and hyperactivity disorder (ADHD) (Button et al., 2005; Fergusson et al., 1993; Hutchinson et al., 2010; Kotimaa et al., 2003; Linnet et al., 2005; Milberger et al., 1996, 1998; Tiesler e…”
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“Detailed sampling and research procedures of this larger cohort study have been described elsewhere (Liu et al., 2011b, 2010).”
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“The validity of self-reported ETS exposure is still a concern, although some studies, particularly recent studies in Asia, have found this methodology acceptable and useful (Chiu et al., 2008; Kaufman et al., 2002; Nondahl et al., 2005).”
BackgroundResultHutchinson, J., Pickett, K. E., Green, J., & Wakschlag, L. S. (2009) · Journal of Epidemiology & Community Health · doi:10.1136/jech.2009.089334 · Cited by 45 · cited 3× · see citing works
“direct intake of tobacco through cigarettes) during pregnancy is associated with child behavior problems, such as attention deficit and hyperactivity disorder (ADHD) (Button et al., 2005; Fergusson et al., 1993; Hutchinson et al., 2010; Kotimaa et al., 2003; Linnet et al., 2005; Milberger et al., 1996, 1998; Tiesler e…”
BackgroundGender and tobacco control : a policy brief
Initiative, W. T. F. (2007) · Medical Entomology and Zoology · Cited by 41 · see citing works
Chiu, H.-T., Wu, H. I., & Kuo, H. (2008) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2008.07.005 · Cited by 39 · cited 1× · see citing works
“The validity of self-reported ETS exposure is still a concern, although some studies, particularly recent studies in Asia, have found this methodology acceptable and useful (Chiu et al., 2008; Kaufman et al., 2002; Nondahl et al., 2005).”
ResultHernández‐Martínez, C., Arija, V., Escribano, J., & Canals, J. (2011) · Early Human Development · doi:10.1016/j.earlhumdev.2011.10.004 · Cited by 39 · cited 2× · see citing works
“…changes in offspring (Huijbregts et al., 2011), and adverse neurodevelopment outcomes in infants, including lower motor system cluster scores (Hernandez-Martinez et al., 2011), decreased mental developmental index scores (Lee et al., 2011), lower birth weight, greater congenital anomalies,…”
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Brook, D. W., Zhang, C., Rosenberg, G., & Brook, J. S. (2006) · American Journal on Addictions · doi:10.1080/10550490600998559 · Cited by 27 · cited 4× · see citing works
“, 1997, 2006), aggression, and other externalizing behaviors (Boutwell et al., 2011; Brook et al., 2006; Fergusson et al., 1998; Huijbregts et al., 2008; Orlebeke et al., 1997, 1999), as well as adult criminal behavior (Brennan et al.”
BackgroundInfluentialExposure to environmental tobacco smoke in Chinese new mothers decreased during pregnancy
Fu, C., Chen, Y., Wang, T., Edwards, N. C., & Xu, B. (2008) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2007.12.006 · Cited by 23 · cited 2× · see citing works
“In fact, a recent survey found that 42% of women in China were exposed to ETS during pregnancy (Fu et al., 2008).”
BackgroundResultCYP1A1 Modifies the Effect of Maternal Exposure to Environmental Tobacco Smoke on Child Behavior
Hsieh, C., Jeng, S., Su, Y.-N., Liao, H.-F., Hsieh, W., Wu, K., & Chen, P. (2010) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntq157 · Cited by 23 · see citing works
Maternal smoking during pregnancy and criminal offending among adult offspring
Paradis, A. D., Fitzmaurice, G. M., Koenen, K. C., & Buka, S. L. (2010) · Journal of Epidemiology & Community Health · doi:10.1136/jech.2009.095802 · Cited by 21 · cited 3× · see citing works
“, 1997, 1999) and criminal behavior in adults (Brennan et al., 1999; Paradis et al., 2011), our study extends these findings by being among the first to show that ETS specifically, rather than direct exposure, is associated with negative behavioral outcomes in children.”
BackgroundResultNeurobiological and behavioral stress reactivity in children prenatally exposed to tobacco
Huijbregts, S. C. J., van Berkel, S. R., Swaab, H., & van Goozen, S. H. M. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.12.008 · Cited by 17 · cited 1× · see citing works
“Maternal exposure to ETS during pregnancy has been previously associated with neurobiological and behavioral changes in offspring (Huijbregts et al., 2011), and adverse neurodevelopment outcomes in infants, including lower motor system cluster scores (Hernandez-Martinez et al., 2011), decreased…”
BackgroundBoutwell, B. B., Beaver, K. M., Gibson, C. L., & Ward, J. T. (2011) · International Journal of Environmental Health Research · doi:10.1080/09603123.2010.544032 · Cited by 14 · cited 2× · see citing works
“, 1997, 2006), aggression, and other externalizing behaviors (Boutwell et al., 2011; Brook et al., 2006; Fergusson et al., 1998; Huijbregts et al., 2008; Orlebeke et al., 1997, 1999), as well as adult criminal behavior (Brennan et al.”
BackgroundInfant Exposure to Environmental Tobacco Smoke:A Prevalence Study in Shanghai
Wang, T. (2007) · Zhongguo chuji weisheng baojian · Cited by 2 · see citing works
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- Centers for Disease Control and PreventionSurgeon General’s report—how tobacco smoke causes disease: the biology and behavioral basis for smoking-attributable disease 2010 Centers for Disease Control and Prevention Atlanta, GA, USA 21452462
- Liu J Wuerker A Biosocial bases of violence: implications for nursing research Int J Nurs Stud 2005 42 229 41 15680620
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Cited by
Sorted by citations
Kalkbrenner, A. E., Schmidt, R. J., & Penlesky, A. C. (2014) · Current Problems in Pediatric and Adolescent Health Care · doi:10.1016/j.cppeds.2014.06.001 · Cited by 268 · see citing works
Early life programming as a target for prevention of child and adolescent mental disorders
Lewis, A. J., Galbally, M., Gannon, T., & Symeonides, C. (2014) · BMC Medicine · doi:10.1186/1741-7015-12-33 · Cited by 133 · see citing works
“with adverse behavioral outcomes [94-96], although a”
Carneiro, A., Dias, P., & Soares, I. (2016) · Journal of Child and Family Studies · doi:10.1007/s10826-016-0456-z · Cited by 112 · see citing works
“…risk drinking (Knudsen et al. 2014) increased IEP, methamphetamine use during pregnancy increases IEP (LaGasse et al. 2013) and EP (Twomey et al. 2013), tobacco exposure during pregnancy (Liu et al. 2013) and maternal smoking during child preschool years increases IEP (Paterson et al. 2013).”
BackgroundMethodInfluentialThe next 1000 days: building on early investments for the health and development of young children
Draper, C. E., Yousafzai, A. K., McCoy, D. C., Cuartas, J. A., Obradović, J., Bhopal, S., Fisher, J., Jeong, J., Klingberg, S., Milner, K. M., et al. (2024) · The Lancet · doi:10.1016/s0140-6736(24)01389-8 · Cited by 129 · see citing works
Environmental Tobacco Smoke Exposure during Pregnancy and Child Neurodevelopment
Polańska, K., Król, A. I., Merecz‐Kot, D., Ligocka, D., Mikołajewska, K., Mirabella, F., Chiarotti, F., Calamandrei, G., & Hanke, W. (2017) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph14070796 · Cited by 66 · see citing works
“The existing studies in this field have selected a variety of indicators of ETS exposure including: the number of cigarettes smoked daily in the presence of a mother over the period of pregnancy [13], at least one person that smoked in a woman’s environment for at least 30 minutes [14], paternal smoking outdoors and i…”
BackgroundHall, B. J., Cauley, M., Burke, D. A., Kiany, A., Slotkin, T. A., & Levin, E. D. (2016) · Toxicological Sciences · doi:10.1093/toxsci/kfw042 · Cited by 57 · see citing works
“, 2005), with increased externalizing behavior (Liu et al., 2013), with emotional disorders (Bandiera et al.”
BackgroundPrenatal risk factors for internalizing and externalizing problems in childhood
Tien, J., Lewis, G. D., & Liu, J. (2019) · World Journal of Pediatrics · doi:10.1007/s12519-019-00319-2 · Cited by 59 · see citing works
“Epidemiological studies in China [48, 49], Japan [50], and the United States [36] have all reported a link between prenatal SHS exposure and hyperactivity.”
BackgroundSelf-citationCohort Profile Update: The China Jintan Child Cohort Study
Liu, J., Cao, S., Chen, Z., Raine, A., Hanlon, A. L., Ai, Y., Zhou, G., Yan, C., Leung, P. W. L., McCauley, L., et al. (2015) · International Journal of Epidemiology · doi:10.1093/ije/dyv119 · Cited by 48 · see citing works
“Children of mothers exposed to second-hand smoking during pregnancy had higher scores for externalizing and total behaviour problems.(61) A positive association between a marker for prenatal testosterone exposure [i.”
BackgroundSelf-citationMedical Record Validation of Maternal Recall of Pregnancy and Birth Events From a Twin Cohort
Liu, J., Tuvblad, C., Li, L., Raine, A., & Baker, L. A. (2013) · Twin Research and Human Genetics · doi:10.1017/thg.2013.31 · Cited by 45 · see citing works
“…researchers due to its association with many long-term outcomes in offspring (Batty et al., 2006; Brook et al., 2006, 2008; Button et al., 2005; Lambe et al., 2006; Liu et al., 2013), it may be more suitable to present mothers with categorical answers, or ask within a more immediate recall period.”
Self-citationPrenatal Tobacco Exposure Shortens Telomere Length in Children
Ip, P., Chung, B. H., Ho, F. K. W., Chan, G., Deng, W., Wong, W. H. S., Lee, S. L., Chan, P. Y. T., Ying, D., Wong, W. L., et al. (2016) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntw139 · Cited by 40 · see citing works
Lamy, S., Laqueille, X., & Thibaut, F. (2014) · L Encéphale · doi:10.1016/j.encep.2014.08.012 · Cited by 33 · see citing works
Lin, Q., Hou, X., Yin, X., Wen, G., Sun, D., Xian, D., Fan, L., Jiang, H., Jin, J., Yu, J. Z., et al. (2017) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph14101132 · Cited by 33 · see citing works
“One study [17] in China reported that maternal ETS exposure was associated with a higher risk of externalizing behavior problems in offspring aged 5–6 years old (OR = 2.”
BackgroundResultFang, X., Strodl, E. S., Liu, B., Liu, L., Yin, X., Wen, G., Sun, D., Xian, D., Jiang, H., Jin, J., et al. (2019) · Environmental Research · doi:10.1016/j.envres.2019.108612 · Cited by 32 · see citing works
Margolis, A. E., Pagliaccio, D., Ramphal, B., Banker, S. M., Thomas, L. V., Robinson, M., Honda, M., Sussman, T. J., Posner, J. E., Kannan, K., et al. (2021) · Environment International · doi:10.1016/j.envint.2021.106516 · Cited by 24 · see citing works
Trends in exposure to second hand smoke at home among children and nonsmoker adolescents
Jain, R. B. (2015) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2015.10.076 · Cited by 23 · see citing works
Antenatal and Early Postnatal Antecedents of Parent-Reported Attention Problems at 2 Years of Age
Downey, L. C., O’Shea, T. M., Allred, E. N., Kuban, K., McElrath, T. F., Warner, D. D., Ware, J., Hecht, J. L., Onderdonk, A. B., & Leviton, A. (2014) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2014.08.004 · Cited by 22 · see citing works
“Antenatal exposure to the tobacco smoke of others has been associated with externalizing behaviors, which include hyperactivity.(30) Numerous studies in animals indicate that exposure of the fetus to nicotine has persisting effects on brain structure and function, resulting in a heightened risk of neurobehavioral abno…”
Environmental exposure and child health in China
Ding, G., Gao, Y. X., Kan, H., Zeng, Q., Yan, C., Li, F., Jiang, F., Landrigan, P. J., Tian, Y., & Zhang, J. (2024) · Environment International · doi:10.1016/j.envint.2024.108722 · Cited by 21 · see citing works
Bull, L., Oliver, C., Callaghan, E., & Woodcock, K. A. (2014) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-014-2308-2 · Cited by 19 · see citing works
“ships (Donkin et al. 2013; Fraser et al. 2001; Liu et al. 2013; Sinha et al. 2013).”
BackgroundBrief Counseling on Secondhand Smoke Exposure in Pregnant Women in Argentina and Uruguay
Alemán, A., Morello, P., Colomar, M., Llambí, L., Berrueta, M. B., Gibbons, L., Buekens, P. M., & Althabe, F. (2016) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph14010028 · Cited by 18 · see citing works
Su, Z., McDonnell, D., Abbas, J., Shi, L., Cai, Y., & Yang, L. (2021) · JMIR Cancer · doi:10.2196/24984 · Cited by 17 · see citing works
“This insight is particularly promising for expectant mothers, as the adverse impacts of secondhand smoke are more pronounced for this population, and can harm both the mother’s and the infant’s health and well-being [13-18].”
BackgroundCauley, M. C., Hall, B. J., Abreu‐Villaça, Y., Junaid, S., White, H., Kiany, A., Slotkin, T. A., & Levin, E. D. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.07.012 · Cited by 15 · see citing works
“These include increased externalizing behavior (Liu et al., 2013), emotional dysfunction (Bandiera et al.”
Hoehn, J., Riekert, K. A., Borrelli, B., Rand, C. S., & Eakin, M. N. (2016) · Health Education Research · doi:10.1093/her/cyw028 · Cited by 11 · see citing works
“Pediatric SHSe has been shown to exacerbate asthma symptoms [1, 2], and is associated with increased risk of bronchitis, pneumonia and other respiratory infections [3], sudden infant death syndrome [4, 5], middle ear disease [6], atopic dermatitis [7], attention deficit hyperactivity disorder [8], externalizing behavi…”
BackgroundGreenwood, P. B., DeSerisy, M. L., Koe, E., Rodriguez, E. R., Salas, L., Perera, F. P., Herbstman, J. B., Pagliaccio, D., & Margolis, A. E. (2024) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2024.107338 · Cited by 10 · see citing works
Prenatal Exposure to Secondhand Smoke and the Development of Self-Control
Meldrum, R. C., & Barnes, J. C. (2016) · Journal of Developmental and Life-Course Criminology · doi:10.1007/s40865-016-0038-1 · Cited by 9 · see citing works
Yang, H.-S., Lim, H., Choi, J., Bae, S., Kim, Y., Kwon, H., & Ha, M. (2018) · Journal of Korean Medical Science · doi:10.3346/jkms.2018.33.e229 · Cited by 9 · see citing works
Yusuf, K. K., Salihu, H. M., Wilson, R. E., Mbah, A. K., Sappenfield, W. M., Bruder, K., Wudil, U. J., & Aliyu, M. H. (2019) · Current Developments in Nutrition · doi:10.1093/cdn/nzz025 · Cited by 8 · see citing works
“Maternal tobacco exposure is associated with reduced head circumference (1, 2), altered indicators of infant body proportionality, such as brain-body weight ratio (BBR) (3), and infant neurocognitive developmental problems (6, 7).”
BackgroundYe, H., Yang, X., & Hanna, F. S. (2023) · Children · doi:10.3390/children10081354 · Cited by 9 · see citing works
“, (2013) [23] ETS exposure was associated with a higher risk of externalizing behaviour problems in the offspring of exposed mothers.”
BackgroundInfluentialYang, X. C., Yin, Z., Cheng, Y., Yang, W., Zhu, Z., Zhang, M., Li, D., Liu, D., Yan, H., & Zeng, L. (2018) · Scientific Reports · doi:10.1038/s41598-018-32171-1 · Cited by 6 · see citing works
Margolis, A. E., Lee, S. H., Liu, R., Goolsby, L., Champagne, F. A., Herbstman, J. B., & Beebe, B. A. (2023) · Environmental Research · doi:10.1016/j.envres.2023.115652 · Cited by 5 · see citing works
“with externalizing behaviors and increased hyperactivity in 5–6 year olds and preschool-age children (Lin, 2017; Liu et al., 2013).”
BackgroundEstandarización del Child Behavior Checklist para preescolares de población urbana de Argentina
Vázquez, N., & Samaniego, V. C. (2017) · Revista Evaluar · doi:10.35670/1667-4545.v17.n1.17075 · Cited by 6 · see citing works
Developmental Neurotoxicity of Nicotine and Tobacco
Levin, E. D., & Abreu‐Villaça, Y. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809405-1.00039-0 · Cited by 5 · see citing works
Sehgal, N., Brennan, P. A., Dunlop, A. L., Liang, D., Corwin, E. J., Tan, Y., Everson, T. M., Caudle, W. M., Panuwet, P., D'Souza, P. E., et al. (2025) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2025.107536 · Cited by 4 · see citing works
Sharkawy, M. E., Heinze, S., Hendrowarsito, L., Weinberger, A., Huß, J., Nennstiel, U., Herr, C. E. W., Kutzora, S., for the GME Study Group, Doerk, W., et al. (2021) · BMC Public Health · doi:10.1186/s12889-021-12130-8 · Cited by 3 · see citing works
Glenn, A. L., Ragno, L., & Liu, J. (2023) · NeuroToxicology · doi:10.1016/j.neuro.2023.05.012 · Cited by 3 · see citing works
Self-citationFetal exposures and maternal mental disorders in pregnancy: a network analysis
Lewis, A. J., Zanden, B. E. V., & Galbally, M. (2025) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174425100093 · Cited by 2 · see citing works
“28,29,30 Equally, we also do not include exposures to heavy metals, or endocrine altering plastics.”
Benavides, J., Cohen, J. W., Chillrud, L., Cohen, G., DeSerisy, M. L., Ramphal, B., Goldsmith, J., Kioumourtzoglou, M., & Margolis, A. E. (2025) · Environmental Epidemiology · doi:10.1097/ee9.0000000000000417 · Cited by 1 · see citing works
Liu, J., Yeung, C. Y. N. A., & Leung, P. W. L. (2018) · Child Indicators Research · doi:10.1007/s12187-018-9580-1 · Cited by 1 · see citing works
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Maldonado, A., Caetano, S. C., Davidson, L. L., Muszkat, D., Silva, L. M., Gutiérrez, J. L. A. W., Surkan, P. J., & Martins, S. S. (2024) · Research Square · doi:10.21203/rs.3.rs-5006281/v1
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“Maternal smoking during pregnancy is also linked to increased risk of sudden infant death syndrome [15], as well as long-term consequences on the offspring from infancy [16, 17] to adulthood [18].”
Sharkawy, M. E., Heinze, S., Hendrowarsito, L., Weinberger, A., Huß, J., Nennstiel, U., Herr, C., & Kutzora, S. (2021) · Figshare · doi:10.6084/m9.figshare.17056880
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Consequences of Fetal Substance Exposure
Castro, R., Shaw, G. M., & Cohen, R. S. (2026) · Cambridge University Press eBooks · doi:10.1017/9781009418034.013
- Authors
- Liu, J., Leung, P. W. L., McCauley, L., Ai, Y., & Pinto-Martin, J.
- Affiliations
- University of Pennsylvania (US)
- Chinese University of Hong Kong (HK)
- Emory University (US)
- Corresponding author
- Liu, Jianghong
- Venue
- NeuroToxicology
- Publisher
- Elsevier BV
- Published
- 2013-01
- Volume
- 34
- Pages
- 167-174
- ISSN
- 0161-813X (ISSN-L)
- PMC
- PMC3587028
- OpenAlex
- W2060695792
- Cited by
- 46
- References
- 55
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 4 · 2023: 3 · 2021: 5 · 2019: 3 · 2018: 5 · 2017: 4 · 2016: 6 · 2015: 2 · 2014: 5 · 2013: 1
- FWCI
- 1.71
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- NeuroToxicology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Environmental Health Sciences (K02-ES019878-01, K01ES015877, K02ES019878, R01ES018858)
- Topics
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
- Keywords
- environmental tobacco smoke, passive smoking, smoking during pregnancy, externalizing problems, internalizing problems, child behavioral development, prenatal exposure
- MeSH terms
- Adult, Age Factors, Child Behavior, Child Behavior Disorders, Child Development, Child, Preschool, China, Cross-Sectional Studies, Female, Humans, Internal-External Control, Male, Pregnancy, Prenatal Exposure Delayed Effects, Psychiatric Status Rating Scales, Surveys and Questionnaires, Risk Factors, Tobacco Smoke Pollution, Chi-Square Distribution, Logistic Models, Odds Ratio, Risk Assessment, Maternal Exposure, Young Adult, Checklist
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