Hostname: page-component-89b8bd64d-72crv Total loading time: 0 Render date: 2026-05-09T16:39:01.747Z Has data issue: false hasContentIssue false
  • English
  • Français

The epigenetics of maternal cigarette smoking during pregnancy and effects on child development

Published online by Cambridge University Press:  15 October 2012

Valerie S. Knopik ,
Matthew A. Maccani ,
Sarah Francazio  and
John E. McGeary
Valerie S. Knopik*
Affiliation:
Rhode Island Hospital Brown University
Matthew A. Maccani
Affiliation:
Rhode Island Hospital Brown University
Sarah Francazio
Affiliation:
Rhode Island Hospital Providence College
John E. McGeary
Affiliation:
Rhode Island Hospital Brown University Providence VA Medical Center
*
Address correspondence and reprint requests to: Valerie S. Knopik, Bradley Hasbro Children's Research Center, Coro West, Suite 204, Hoppin Street, Providence, RI 02903; E-mail: valerie_knopik@brown.edu.
Get access Rights & Permissions [Opens in a new window]

Abstract

The period of in utero development is one of the most critical windows during which adverse intrauterine conditions and exposures can influence the growth and development of the fetus as well as the child's future postnatal health and behavior. Maternal cigarette smoking during pregnancy remains a relatively common but nonetheless hazardous in utero exposure. Previous studies have associated prenatal smoke exposure with reduced birth weight, poor developmental and psychological outcomes, and increased risk for diseases and behavioral disorders later in life. Researchers are now learning that many of the mechanisms whereby maternal smoke exposure may affect key pathways crucial for proper fetal growth and development are epigenetic in nature. Maternal cigarette smoking during pregnancy has been associated with altered DNA methylation and dysregulated expression of microRNA, but a deeper understanding of the epigenetics of maternal cigarette smoking during pregnancy as well as how these epigenetic changes may affect later health and behavior remain to be elucidated. This article seeks to explore many of the previously described epigenetic alterations associated with maternal cigarette smoking during pregnancy and assess how such changes may have consequences for both fetal growth and development, as well as later child health, behavior, and well-being. We also outline future directions for this new and exciting field of research.

Information

Type
Articles
Information
Development and Psychopathology , Volume 24 , Issue 4: Contributions of the Genetic/Genomic Sciences to Developmental Psychopathology , November 2012 , pp. 1377 - 1390
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Abbott, L. C., & Winzer-Serhan, U. H. (2012). Smoking during pregnancy: Lessons learned from epidemiological studies and experimental studies using animal models. Critical Reviews in Toxicology, 42, 279–303.Google Scholar
Agrawal, A., Knopik, V. S., Pergadia, M. L., Waldron, M., Bucholz, K. K., Martin, N. G., et al. (2008). Correlates of cigarette smoking during pregnancy and its genetic and environmental overlap with nicotine dependence. Nicotine and Tobacco Research, 10, 567–578.Google Scholar
Argente, J., Mehls, O., & Barrios, V. (2010). Growth and body composition in very young SGA children. Pediatric Nephrology, 25, 679–685.CrossRefGoogle ScholarPubMed
Ba, Y., Yu, H., Liu, F., Geng, X., Zhu, C., Zhu, Q., et al. (2011). Relationship of folate, vitamin B12 and methylation of insulin-like growth factor-II in maternal and cord blood. European Journal of Clinical Nutrition, 65, 480–485.CrossRefGoogle ScholarPubMed
Barker, D. J. (2004). Developmental origins of adult health and disease. Journal of Epidemiology and Community Health, 58, 114–115.Google Scholar
Barker, D. J., & Clark, P. M. (1997). Fetal undernutrition and disease in later life. Reviews of Reproduction, 2, 105–112.CrossRefGoogle ScholarPubMed
Batstra, L., Hadders-Algra, M., & Neeleman, J. (2003). Effect of antenatal exposure to maternal smoking on behavioural problems and academic achievement in childhood: Prospective evidence from a Dutch birth cohort. Early Human Development, 75, 21–33.Google Scholar
Benasich, A. A., & Tallal, P. (2002). Infant discrimination of rapid auditory cues predicts later language impairment. Behavioural Brain Research, 136, 31–49.CrossRefGoogle ScholarPubMed
Bird, A. (2007). Perceptions of epigenetics. Nature, 447(7143), 396–398.Google Scholar
Breton, C. V., Byun, H. M., Wenten, M., Pan, F., Yang, A., & Gilliland, F. D. (2009). Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. American Journal of Respiratory and Critical Care Medicine, 180, 462–467.CrossRefGoogle ScholarPubMed
Brown, A. S., Susser, E. S., Lin, S. P., Neugebauer, R., & Gorman, J. M. (1995). Increased risk of affective disorders in males after second trimester prenatal exposure to the Dutch hunger winter of 1944–45. British Journal of Psychiatry, 166, 601–606.CrossRefGoogle Scholar
Calabrese, F., Molteni, R., Racagni, G., & Riva, M. A. (2009). Neuronal plasticity: A link between stress and mood disorders. Psychoneuroendocrinology, 34(Suppl. 1), S208–S216.Google Scholar
Castles, A., Adams, E. K., Melvin, C. L., Kelsch, C., & Boulton, M. L. (1999). Effects of smoking during pregnancy. Five meta-analyses. American Journal of Preventative Medicine, 16, 208–215.CrossRefGoogle ScholarPubMed
Chmurzynska, A. (2010). Fetal programming: Link between early nutrition, DNA methylation, and complex diseases. Nutrition Reviews, 68, 87–98.Google Scholar
Cicchetti, D. (2006). Development and psychopathology. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology: Vol. 1. Theory and method (2nd ed.). New York: Wiley.Google Scholar
Cnattingius, S. (2004). The epidemiology of smoking during pregnancy: Smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine and Tobacco Research, 6(Suppl. 2), S125–S140.Google Scholar
Cook, D. G., & Strachan, D. P. (1999). Health effects of passive smoking—10: Summary of effects of parental smoking on the respiratory health of children and implications for research. Thorax, 54, 357–366.Google Scholar
Cornelius, M. D., & Day, N. L. (2009). Developmental consequences of prenatal tobacco exposure. Current Opinions in Neurology, 22, 121–125.Google Scholar
Cornelius, M. D., Ryan, C. M., Day, N. L., Goldschmidt, L., & Willford, J. A. (2001). Prenatal tobacco effects on neuropsychological outcomes among preadolescents. Journal of Developmental and Behavioral Pediatrics, 22, 217–225.CrossRefGoogle ScholarPubMed
Crane-Godreau, M. A., Maccani, M. A., Eszterhas, S. K., Warner, S. L., Jukosky, J. A., & Fiering, S. (2009). Exposure to cigarette smoke disrupts CCL20-mediated antimicrobial activity in respiratory epithelial cells. Open Immunology Journal, 2, 86–93.Google ScholarPubMed
D'Onofrio, B. M., Singh, A. L., Iliadou, A., Lambe, M., Hultman, C. M., Grann, M., et al. (2010). Familial confounding of the association between maternal smoking during pregnancy and offspring criminality: A population-based study in Sweden. Archives of General Psychiatry, 67, 529–538.Google Scholar
D'Onofrio, B. M., Singh, A. L., Iliadou, A., Lambe, M., Hultman, C. M., Neiderhiser, J. M., et al. (2010). A quasi-experimental study of maternal smoking during pregnancy and offspring academic achievement. Child Development, 81, 80–100.Google Scholar
D'Onofrio, B. M., Turkheimer, E. N., Eaves, L. J., Corey, L. A., Berg, K., Solaas, M. H., et al. (2003). The role of the children of twins design in elucidating causal relations between parent characteristics and child outcomes. Journal of Child Psychology and Psychiatry, 44, 1130–1144.Google Scholar
D'Onofrio, B. M., Van Hulle, C. A., Waldman, I. D., Rodgers, J. L., Harden, K. P., Rathouz, P. J., et al. (2008). Smoking during pregnancy and offspring externalizing problems: An exploration of genetic and environmental confounds. Development and Psychopathology, 20, 139–164.Google Scholar
de Rooij, S. R., Wouters, H., Yonker, J. E., Painter, R. C., & Roseboom, T. J. (2010). Prenatal undernutrition and cognitive function in late adulthood. Proceedings of the National Academy of Sciences, 107, 16881–16886.Google Scholar
Doherty, S. P., Grabowski, J., Hoffman, C., Ng, S. P., & Zelikoff, J. T. (2009). Early life insult from cigarette smoke may be predictive of chronic diseases later in life. Biomarkers, 14(Suppl. 1), 97–101.CrossRefGoogle ScholarPubMed
Du, T., & Zamore, P. D. (2007). Beginning to understand microRNA function. Cell Research, 17, 661–663.Google Scholar
Einarson, A., & Riordan, S. (2009). Smoking in pregnancy and lactation: A review of risks and cessation strategies. European Journal of Clinical Pharmacology, 65, 325–330.CrossRefGoogle ScholarPubMed
Ernst, M., Moolchan, E. T., & Robinson, M. L. (2001). Behavioral and neural consequences of prenatal exposure to nicotine. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 630–641.Google Scholar
Fergusson, D. M., Woodward, L. J., & Horwood, L. J. (1998). Maternal smoking during pregnancy and psychiatric adjustment in late adolescence. Archives of General Psychiatry, 55, 721–727.CrossRefGoogle ScholarPubMed
Filiberto, A. C., Maccani, M. A., Koestler, D., Wilhelm-Benartzi, C., Avissar-Whiting, M., Banister, C. E., et al. (2011). Birthweight is associated with DNA promoter methylation of the glucocorticoid receptor in human placenta. Epigenetics, 6, 566–572.Google Scholar
Fried, P. A., O'Connell, C. M., & Watkinson, B. (1992). 60- and 72-month follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol: Cognitive and language assessment. Journal of Developmental and Behavioral Pediatrics, 13, 383–391.Google Scholar
Fried, P. A., Watkinson, B., & Gray, R. (1992). A follow-up study of attentional behavior in 6-year-old children exposed prenatally to marihuana, cigarettes, and alcohol. Neurotoxicology and Teratology, 14, 299–311.Google Scholar
Fuchikami, M., Morinobu, S., Segawa, M., Okamoto, Y., Yamawaki, S., Ozaki, N., et al. (2011). DNA methylation profiles of the brain-derived neurotrophic factor (BDNF) gene as a potent diagnostic biomarker in major depression. PLoS One, 6, e23881.Google Scholar
Gillman, M. W. (2005). Developmental origins of health and disease. New England Journal of Medicine, 353, 1848–1850.CrossRefGoogle ScholarPubMed
Gilman, S. E., Gardener, H., & Buka, S. L. (2008). Maternal smoking during pregnancy and children's cognitive and physical development: A causal risk factor? American Journal of Epidemiology, 168, 522–531.Google Scholar
Goodwin, R. D., Keyes, K., & Simuro, N. (2007). Mental disorders and nicotine dependence among pregnant women in the United States. Obstetrics and Gynecology, 109, 875–883.Google Scholar
Guerrero-Preston, R., Goldman, L. R., Brebi-Mieville, P., Ili-Gangas, C., Lebron, C., Witter, F. R., et al. (2010). Global DNA hypomethylation is associated with in utero exposure to cotinine and perfluorinated alkyl compounds. Epigenetics, 5, 539–546.Google Scholar
Guo, L., Choufani, S., Ferreira, J., Smith, A., Chitayat, D., Shuman, C., et al. (2008). Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Developmental Biology, 320, 79–91.Google Scholar
Hales, C. N., & Barker, D. J. (1992). Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia, 35, 595–601.Google Scholar
Herbeck, Y. E., Gulevich, R. G., Amelkina, O. A., Plyusnina, I. Z., & Oskina, I. N. (2010). Conserved methylation of the glucocorticoid receptor gene exon 1(7) promoter in rats subjected to a maternal methyl-supplemented diet. International Journal of Developmental Neuroscience, 28, 9–12.CrossRefGoogle ScholarPubMed
Hochberg, Z., Feil, R., Constancia, M., Fraga, M., Junien, C., Carel, J. C., et al. (2010). Child health, developmental plasticity, and epigenetic programming. Endocrine Reviews, 32, 159–224.Google Scholar
Huang, E. J., & Reichardt, L. F. (2001). Neurotrophins: Roles in neuronal development and function. Annual Review of Neuroscience, 24, 677–736.Google Scholar
Huijbregts, S. C., Seguin, J. R., Zoccolillo, M., Boivin, M., & Tremblay, R. E. (2007). Associations of maternal prenatal smoking with early childhood physical aggression, hyperactivity–impulsivity, and their co-occurrence. Journal of Abnormal Child Psychology, 35, 203–215.Google Scholar
Huijbregts, S. C., Seguin, J. R., Zoccolillo, M., Boivin, M., & Tremblay, R. E. (2008). Maternal prenatal smoking, parental antisocial behavior, and early childhood physical aggression. Development and Psychopathology, 20, 437–453.Google Scholar
Huizink, A. C., & Mulder, E. J. (2006). Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neuroscience & Biobehavioral Reviews, 30, 24–41.CrossRefGoogle ScholarPubMed
Jaakkola, N., Jaakkola, M. S., Gissler, M., & Jaakkola, J. J. (2001). Smoking during pregnancy in Finland: Determinants and trends, 1987–1997. American Journal of Public Health, 91, 284–286.Google Scholar
Jaenisch, R. (1997). DNA methylation and imprinting: Why bother? Trends in Genetics, 13, 323–329.Google Scholar
Johansson, A. L., Dickman, P. W., Kramer, M. S., & Cnattingius, S. (2009). Maternal smoking and infant mortality: Does quitting smoking reduce the risk of infant death? Epidemiology, 20, 590–597.Google Scholar
Kable, J. A., Coles, C. D., Lynch, M. E., & Carroll, J. (2009). The impact of maternal smoking on fast auditory brainstem responses. Neurotoxicology and Teratology, 31, 216–224.CrossRefGoogle ScholarPubMed
Kaddar, T., Rouault, J. P., Chien, W. W., Chebel, A., Gadoux, M., Salles, G., et al. (2009). Two new miR-16 targets: Caprin-1 and HMGA1, proteins implicated in cell proliferation. Biology of the Cell, 101, 511–524.Google Scholar
Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Urven, L., McCarrey, J., et al. (1992). Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes and Development, 6, 705–714.CrossRefGoogle ScholarPubMed
Ke, X., Schober, M. E., McKnight, R. A., O'Grady, S., Caprau, D., Yu, X., et al. (2010). Intrauterine growth retardation affects expression and epigenetic characteristics of the rat hippocampal glucocorticoid receptor gene. Physiological Genomics, 42, 177–189.Google Scholar
Kiechl-Kohlendorfer, U., Ralser, E., Pupp Peglow, U., Reiter, G., Griesmaier, E., & Trawoger, R. (2010). Smoking in pregnancy: A risk factor for adverse neurodevelopmental outcome in preterm infants? Acta Paediatrica, 99, 1016–1019.Google Scholar
Knopik, V. S. (2009). Maternal smoking during pregnancy and child outcomes: Real or spurious effect? Developmental Neuropsychology, 34, 1–36.CrossRefGoogle ScholarPubMed
Knopik, V. S., Heath, A. C., Jacob, T., Slutske, W. S., Bucholz, K. K., Madden, P. A., et al. (2006). Maternal alcohol use disorder and offspring ADHD: Disentangling genetic and environmental effects using a children-of-twins design. Psychological Medicine, 36, 1461–1471.Google Scholar
Knopik, V. S., Jacob, T., Haber, J. R., Swenson, L. P., & Howell, D. N. (2009). Paternal alcoholism and offspring ADHD problems: A children of twins design. Twin Research and Human Genetics, 12, 53–62.CrossRefGoogle ScholarPubMed
Knopik, V. S., McGeary, J. E., Nugent, N., Francazio, S., & Heath, A. C. (2010). Smoking during pregnancy, maternal xenobiotic metabolism genes, and child externalizing behavior: A case-crossover design. Behavior Genetics, 40, 799–800.Google Scholar
Knopik, V. S., McGeary, J. E., Nugent, N., Francazio, S., & Heath, A. C. (in press). Child ADHD: Maternal xenobiotic metabolism genes and smoking during pregnancy. Behavior Genetics.Google Scholar
Knopik, V. S., Sparrow, E. P., Madden, P. A., Bucholz, K. K., Hudziak, J. J., Reich, W., et al. (2005). Contributions of parental alcoholism, prenatal substance exposure, and genetic transmission to child ADHD risk: A female twin study. Psychological Medicine, 35, 625–635.Google Scholar
Kuja-Halkola, R., D'Onofrio, B. M., Iliadou, A. N., Langstrom, N., & Lichtenstein, P. (2010). Prenatal smoking exposure and offspring stress coping in late adolescence: No causal link. International Journal of Epidemiology, 39, 1531–1540.Google Scholar
Lambe, M., Hultman, C., Torrang, A., Maccabe, J., & Cnattingius, S. (2006). Maternal smoking during pregnancy and school performance at age 15. Epidemiology, 17, 524–530.Google Scholar
Lambers, D. S., & Clark, K. E. (1996). The maternal and fetal physiologic effects of nicotine. Seminars in Perinatology, 20, 115–126.Google Scholar
Lee, B. E., Hong, Y. C., Park, H., Ha, M., Kim, J. H., Chang, N., et al. (2011). Secondhand smoke exposure during pregnancy and infantile neurodevelopment. Environmental Research, 111, 539–544.Google Scholar
Lee, R. C., Feinbaum, R. L., & Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843–854.Google Scholar
Linnet, K. M., Wisborg, K., Obel, C., Secher, N. J., Thomsen, P. H., Agerbo, E., et al. (2005). Smoking during pregnancy and the risk for hyperkinetic disorder in offspring. Pediatrics, 116, 462–467.Google Scholar
Lumley, T., & Levy, D. (2000). Bias in the case-crossover design: Implications for studies of air pollution. Environmetrics, 11, 689–704.Google Scholar
Lundberg, F., Cnattingius, S., D'Onofrio, B., Altman, D., Lambe, M., Hultman, C., et al. (2009). Maternal smoking during pregnancy and intellectual performance in young adult Swedish male offspring. Paediatrics and Perinatal Epidemiology, 24, 79–87.Google Scholar
Maccani, M. A., Avissar-Whiting, M., Banister, C. E., McGonnigal, B., Padbury, J. F., & Marsit, C. J. (2010). Maternal cigarette smoking during pregnancy is associated with downregulation of miR-16, miR-21, and miR-146a in the placenta. Epigenetics, 5, 583–589.Google Scholar
Maccani, M. A., & Knopik, V. S. (2012). Cigarette smoke exposure-associated alterations to non-coding RNA. Frontiers in Genetics, 3, 53.Google Scholar
Maccani, M. A., & Marsit, C. J. (2009). Epigenetics in the placenta. American Journal of Reproductive Immunology, 62, 78–89.Google Scholar
Maccani, M. A., & Marsit, C. J. (2011). Exposure and fetal growth-associated miRNA alterations in the human placenta. Clinical Epigenetics, 2, 401–404.Google Scholar
Makin, J., Fried, P. A., & Watkinson, B. (1991). A comparison of active and passive smoking during pregnancy: Long-term effects. Neurotoxicology and Teratology, 13, 5–12.CrossRefGoogle ScholarPubMed
Maughan, B., Taylor, A., Caspi, A., & Moffitt, T. E. (2004). Prenatal smoking and early childhood conduct problems: Testing genetic and environmental explanations of the association. Archives of General Psychiatry, 61, 836–843.Google Scholar
McCartney, J. S., Fried, P. A., & Watkinson, B. (1994). Central auditory processing in school-age children prenatally exposed to cigarette smoke. Neurotoxicology and Teratology, 16, 269–276.CrossRefGoogle ScholarPubMed
Meyer, K. A., Williams, P., Hernandez-Diaz, S., & Cnattingius, S. (2004). Smoking and the risk of oral clefts: Exploring the impact of study designs. Epidemiology, 15, 671–678.Google Scholar
Meza-Sosa, K. F., Valle-Garcia, D., Pedraza-Alva, G., & Perez-Martinez, L. (2011). Role of microRNAs in central nervous system development and pathology. Journal of Neuroscience Research, 90, 1–12.Google Scholar
Mick, E., Biederman, J., Faraone, S. V., Sayer, J., & Kleinman, S. (2002). Case-control study of attention-deficit hyperactivity disorder and maternal smoking, alcohol use, and drug use during pregnancy. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 378–385.Google Scholar
Milberger, S., Biederman, J., Faraone, S. V., Chen, L., & Jones, J. (1996). Is maternal smoking during pregnancy a risk factor for attention deficit hyperactivity disorder in children? American Journal of Psychiatry, 153, 1138–1142.Google Scholar
Miska, E. A. (2005). How microRNAs control cell division, differentiation and death. Current Opinion in Genetics and Development, 15, 563–568.Google Scholar
Mohsin, M., & Bauman, A. E. (2005). Socio-demographic factors associated with smoking and smoking cessation among 426,344 pregnant women in New South Wales, Australia. BMC Public Health, 5, 138.Google Scholar
Molfese, D. L. (2000). Predicting dyslexia at 8 years of age using neonatal brain responses. Brain and Language, 72, 238–245.Google Scholar
Monk, M., Boubelik, M., & Lehnert, S. (1987). Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development, 99, 371–382.CrossRefGoogle ScholarPubMed
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 3, 97–106.Google Scholar
Olds, D. L., Henderson, C. R. Jr., & Tatelbaum, R. (1994). Intellectual impairment in children of women who smoke cigarettes during pregnancy. Pediatrics, 93, 221–227.CrossRefGoogle ScholarPubMed
Pajer, K., Andrus, B. M., Gardner, W., Lourie, A., Strange, B., Campo, J., et al. (2012). Discovery of blood transcriptomic markers for depression in animal models and pilot validation in subjects with early-onset major depression. Translational Psychiatry, 2, e101.CrossRefGoogle ScholarPubMed
Paz, R., Barsness, B., Martenson, T., Tanner, D., & Allan, A. M. (2007). Behavioral teratogenicity induced by nonforced maternal nicotine consumption. Neuropsychopharmacology, 32, 693–699.Google Scholar
Price, T. S., Grosser, T., Plomin, R., & Jaffee, S. R. (2010). Fetal genotype for the xenobiotic metabolizing enzyme NQO1 influences intrauterine growth among infants whose mothers smoked during pregnancy. Child Development, 81, 101–114.Google Scholar
Razin, A., & Shemer, R. (1995). DNA methylation in early development. Human Molecular Genetics, 4, 1751–1755.Google Scholar
Reamon-Buettner, S. M., Mutschler, V., & Borlak, J. (2008). The next innovation cycle in toxicogenomics: Environmental epigenetics. Mutation Research, 659, 158–165.Google Scholar
Rice, F., Harold, G. T., Boivin, J., Hay, D. F., van den Bree, M., & Thapar, A. (2009). Disentangling prenatal and inherited influences in humans with an experimental design. Proceedings of the National Academy of Sciences, 106, 2464–2467.Google Scholar
Rice, F., Harold, G. T., Boivin, J., van den Bree, M., Hay, D. F., & Thapar, A. (2010). The links between prenatal stress and offspring development and psychopathology: Disentangling environmental and inherited influences. Psychological Medicine, 40, 335–345.CrossRefGoogle ScholarPubMed
Schulz, L. C. (2010). The Dutch Hunger Winter and the developmental origins of health and disease. Proceedings of the National Academy of Sciences, 107, 16757–16758.Google Scholar
Sexton, M., Fox, N. L., & Hebel, J. R. (1990). Prenatal exposure to tobacco: II. Effects on cognitive functioning at age three. International Journal of Epidemiology, 19, 72–77.Google Scholar
Sexton, M., & Hebel, J. R. (1984). A clinical trial of change in maternal smoking and its effect on birth weight. Journal of the American Medical Association, 251, 911–915.Google Scholar
Shadish, W. R., Cook, T. D., & Campbell, D. T. (2002). Experimental and quasi-experimental designs for generalized causal inference. Belmont, CA: Wadsworth/Cengage Learning.Google Scholar
Shah, N. R., & Bracken, M. B. (2000). A systematic review and meta-analysis of prospective studies on the association between maternal cigarette smoking and preterm delivery. American Journal of Obstetrics and Gynecology, 182, 465–472.Google Scholar
Shea, A. K., & Steiner, M. (2008). Cigarette smoking during pregnancy. Nicotine and Tobacco Research, 10, 267–278.CrossRefGoogle ScholarPubMed
Sood, R., Zehnder, J. L., Druzin, M. L., & Brown, P. O. (2006). Gene expression patterns in human placenta. Proceedings of the National Academy of Sciences, 103, 5478–5483.CrossRefGoogle ScholarPubMed
Stein, A. D., Ravelli, A. C., & Lumey, L. H. (1995). Famine, third-trimester pregnancy weight gain, and intrauterine growth: The Dutch Famine Birth Cohort Study. Human Biology, 67, 135–150.Google Scholar
Stein, Z., Susser, M., Saenger, G., & Marolla, F. (1972). Nutrition and mental performance. Science, 178, 708–713.Google Scholar
Suter, M., Abramovici, A., Showalter, L., Hu, M., Shope, C. D., Varner, M., et al. (2010). In utero tobacco exposure epigenetically modifies placental CYP1A1 expression. Metabolism, 59, 1481–1490.Google Scholar
Suter, M., Ma, J., Harris, A. S., Patterson, L., Brown, K. A., Shope, C., et al. (2011). Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics, 6, 1284–1294.Google Scholar
Swanson, J. M., Entringer, S., Buss, C., & Wadhwa, P. D. (2009). Developmental origins of health and disease: Environmental exposures. Seminars in Reproductive Medicine, 27, 391–402.Google Scholar
Terry, M. B., Ferris, J. S., Pilsner, R., Flom, J. D., Tehranifar, P., Santella, R. M., et al. (2008). Genomic DNA methylation among women in a multiethnic New York City birth cohort. Cancer Epidemiology, Biomarkers, and Prevention, 17, 2306–2310.Google Scholar
Thapar, A., Fowler, T., Rice, F., Scourfield, J., van den Bree, M., Thomas, H., et al. (2003). Maternal smoking during pregnancy and attention deficit hyperactivity disorder symptoms in offspring. American Journal of Psychiatry, 160, 1985–1989.Google Scholar
Thapar, A., Harold, G., Rice, F., Ge, X., Boivin, J., Hay, D., et al. (2007). Do intrauterine or genetic influences explain the foetal origins of chronic disease? A novel experimental method for disentangling effects. BMC Medical Research Methodology, 7, 25.Google Scholar
Thapar, A., Rice, F., Hay, D., Boivin, J., Langley, K., van den Bree, M., et al. (2009). Prenatal smoking might not cause attention-deficit/hyperactivity disorder: Evidence from a novel design. Biological Psychiatry, 66, 722–727.Google Scholar
Thielen, A., Klus, H., & Muller, L. (2008). Tobacco smoke: unraveling a controversial subject. Experimental and Toxicologic Pathology, 60, 141–156.Google Scholar
Toledo-Rodriguez, M., Lotfipour, S., Leonard, G., Perron, M., Richer, L., Veillette, S., et al. (2010). Maternal smoking during pregnancy is associated with epigenetic modifications of the brain-derived neurotrophic factor-6 exon in adolescent offspring. American Journal of Medical Genetics. Part B: Neuropsychiatric Genetics, 153B, 1350–1354.Google Scholar
US Department of Health and Human Services. (2004). Smoking during pregnancy—United States, 1990–2002. MMWR Morbidity and Mortality Weekly Report, 53, 911–915.Google Scholar
US Department of Health and Human Services. (2006). The health consequences of involuntary exposure to tobacco smoke: A report of the surgeon general. Atlanta, GA: Centers for Disease Control and Prevention.Google Scholar
US Department of Health and Human Services. (2010). A report of the surgeon general: How tobacco smoke causes disease: What it means to you. Atlanta, GA: Centers for Disease Control and Prevention.Google Scholar
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854.Google Scholar
Weaver, I. C., La Plante, P., Weaver, S., Parent, A., Sharma, S., Diorio, J., et al. (2001). Early environmental regulation of hippocampal glucocorticoid receptor gene expression: Characterization of intracellular mediators and potential genomic target sites. Molecular and Cellular Endocrinology, 185, 205–218.Google Scholar
Weissman, M. M., Warner, V., Wickramaratne, P. J., & Kandel, D. B. (1999). Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. Journal of the American Academy of Child and Adolescent Psychiatry, 38, 892–899.Google Scholar
Wilhelm-Benartzi, C. S., Houseman, E. A., Maccani, M. A., Poage, G. M., Koestler, D. C., Langevin, S. M., et al. (2011). In utero exposures, infant growth, and DNA methylation of repetitive element and developmentally related genes in human placenta. Environmental Health Perspectives, 120, 296–302.Google Scholar
Wossidlo, M., Nakamura, T., Lepikhov, K., Marques, C. J., Zakhartchenko, V., Boiani, M., et al. (2011). 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nature Communications, 2, 241.Google Scholar
Xiong, Z., Leme, A. S., Ray, P., Shapiro, S. D., & Lee, J. S. (2011). CX3CR1+ lung mononuclear phagocytes spatially confined to the interstitium produce TNF-α and IL-6 and promote cigarette smoke-induced emphysema. Journal of Immunology, 86, 3206–3214.Google Scholar