The effects of nicotine on human fetal development

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 108, Issue 2, 2016, Pages 181-192

  Holbrook, Bradley D ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

e cigarette; fetus; nicotine; smoking; teratogen; tobacco

Indexed keywords

NICOTINE;

ACADEMIC ACHIEVEMENT; ANTISOCIAL BEHAVIOR; ATTENTION DEFICIT DISORDER; CARDIOVASCULAR EFFECT; CONGENITAL DISORDER; CRIMINAL BEHAVIOR; ELECTRONIC CIGARETTE; ENDOCRINE SYSTEM; FETUS; FETUS DEVELOPMENT; HUMAN; INTELLIGENCE; MATERNAL SMOKING; PERINATAL PERIOD; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; REPRODUCTION; RESPIRATORY FUNCTION; REVIEW; SUBSTANCE ABUSE; ADVERSE EFFECTS; CHEMICALLY INDUCED; DRUG EFFECTS; FEMALE; PREGNANCY COMPLICATION; SMOKING; TOBACCO;

ELECTRONIC CIGARETTES; FEMALE; FETAL DEVELOPMENT; FETUS; HUMANS; NICOTINE; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; SMOKING; TOBACCO;

EID: 84976625877     PISSN: 1542975X     EISSN: 15429768     Source Type: Journal    
DOI: 10.1002/bdrc.21128     Document Type: Review

References (142)

1. Abbott LC, Winzer-Serhan UH. 2012. Smoking during pregnancy: lessons learned from epidemiological studies and experimental studies using animal models. Crit Rev Toxicol 42:279–303.
2. Adgent MA. 2006. Environmental tobacco smoke and sudden infant death syndrome: a review. Birth Defects Res B Dev Reprod Toxicol 77:69–85.
3. Anblagan D, Jones NW, Costigan C, et al. 2013. Maternal smoking during pregnancy and fetal organ growth: a magnetic resonance imaging study. PLoS ONE 8:e67223.
4. Ashford J, van Lier PA, Timmermans M, et al. Prenatal smoking and internalizing and externalizing problems in children studied from childhood to late adolescence. J Am Acad Child Adolesc Psychiatry 47:779–787.
5. Ankum WM, Mol BW, Van der Veen F, Bossuyt PM. 1996. Risk factors for ectopic pregnancy: a meta-analysis. Fertil Steril 65:1093–1099.
6. Athanasakis E, Karavasiliadou S, Styliadis I. 2011. The factors contributing to the risk of sudden infant death syndrome. Hippokratia 15:127–131.
7. Baba S, Wikstrom AK, Stephansson O, Cnattingius S. 2012. Influence of smoking and snuff cessation on risk of preterm birth. Eur J Epidemiol 27:297–304.
8. Baba S, Wikstrom AK, Stephansson O, Cnattingius S. 2013. Changes in snuff and smoking habits in Swedish pregnant women and risk for small for gestational age births. Bjog 120:456–462.
9. Baba S, Wikstrom AK, Stephansson O, Cnattingius S. 2014. Influence of snuff and smoking habits in early pregnancy on risks for stillbirth and early neonatal mortality. Nicotine Tob Res 16:78–83.
10. Badr LK, Abdallah B, Mahmoud A. 2005. Precursors of preterm birth: comparison of three ethnic groups in the middle East and the United States. J Obstet Gynecol Neonatal Nurs 34:444–452.
11. Bahl V, Lin S, Xu N, et al. 2012. Comparison of electronic cigarette refill fluid cytotoxicity using embryonic and adult models. Reprod Toxicol 34:529–537.
12. Batty GD, Der G, Deary IJ. 2006. Effect of maternal smoking during pregnancy on offspring's cognitive ability: empirical evidence for complete confounding in the US national longitudinal survey of youth. Pediatrics 118:943–950.
13. Baeza-Loya S, Viswanath H, Carter A, et al. 2014. Perceptions about e-cigarette safety may lead to e-smoking during pregnancy. Bull Menninger Clin 78:243–252.
14. Bergmann KE, Bergmann RL, Von KR, et al. 2003. Early determinants of childhood overweight and adiposity in a birth cohort study: role of breast-feeding. Int J Obes Relat Metab Disord 27:162–172.
15. Blacquiere MJ, Timens W, Melgert BN, et al. 2009. Maternal smoking during pregnancy induces airwayremodelling in mice offspring. Eur Respir J 33:1133–1140.
16. Booij L, Benkelfat C, Leyton M, et al. 2012. Perinatal effects on in vivo measures of human brain serotonin synthesis in adulthood: a 27-year longitudinal study. Our Neuropsychopharmacol 22:419–423.
17. Boucher O, Jacobson JL, Burden MJ, et al. 2014. Prenatal tobacco exposure and response inhibition in school-aged children: an event-related potential study. Neurotoxicol Teratol 44:81–88.
18. Brennan PA, Grekin ER, Mednick SA. 1999. Maternal smoking during pregnancy and adult male criminal outcomes. Arch Gen Psychiatry 56:215.
19. Brennan PA, Grekin ER, Mortensen EL, Mednick SA. 2002. Relationship of maternal smoking during pregnancy with criminal arrest and hospitalization for substance abuse in male and female adult offspring. Am J Psychiatry 159:48–54.
20. Breslau N, Paneth N, Lucia VC, Paneth-Pollak R. 2005. Maternal smoking during pregnancy and offspring IQ. Int J Epidemiol 34:1047–1053.
21. Brion MJ, Leary SD, Lawlor DA, et al. 2008. Modifiable maternal exposures and offspring blood pressure: a review of epidemiological studies of maternal age, diet, and smoking. Pediatr Res 63:593–598.
22. Brion MJ, Victora C, Matijasevich A, et al. 2010. Maternal smoking and child psychological problems: disentangling causal and noncausal effects. Pediatrics 126:e57–e65.
23. Brown RW, Hanrahan JP, Castile RG, Tager IB. 1995. Effect of maternal smoking during pregnancy on passive respiratory mechanics in early infancy. Pediatr Pulmonol 19:23–28.
24. Bruin JE, Gerstein HC, Holloway AC. 2010. Long-term consequences of fetal and neonatal nicotine exposure: a critical review. Toxicol Sci 116:364–374.
25. Burke H, Leonardi-Bee J, Hashim A, et al. 2012. Prenatal and passive smoke exposure and incidence of asthma and wheeze: systematic review and meta-analysis. Pediatrics 129:735–744.
26. Button TM, Thapar A, McGuffin P. 2005. Relationship between antisocial behaviour, attention-deficit hyperactivity disorder and maternal prenatal smoking. Br J Psychiatry 187:155–160.
27. Chang L, Cloak CC, Jiang CS, et al. 2012. Lower glial metabolite levels in brains of young children with prenatal nicotine exposure. J Neuroimmune Pharmacol 7:243–252.
28. Cheraghi M, Salvi S. 2009. Environmental tobacco smoke (ETS) and respiratory health in children. Eur J Pediatr 168:897–905.
29. Cho K, Frijters JC, Zhang H, et al. 2013. Prenatal exposure to nicotine and impaired reading performance. J Pediatr 162:713–718.
30. Chung KC, Kowalski CP, Kim HM, Buchman SR. 2000. Maternal cigarette smoking during pregnancy and the risk of having a child with cleft lip/palate. Plast Reconstr Surg 105:485–491.
31. Cohen G, Roux JC, Grailhe R, et al. 2005. Perinatal exposure to nicotine causes deficits associated with a loss of nicotinic receptor function. Proc Natl Acad Sci U S A 102:3817–3821.
32. Cornelius MD, Ryan CM, Day NL, et al. 2001. Prenatal tobacco effects on neuropsychological outcomes among preadolescents. J Dev Behav Pediatr 22:217–225.
33. Cornelius MD, Goldschmidt L, Day NL. 2012. Prenatal cigarette smoking: long-term effects on young adult behavior problems and smoking behavior. Neurotoxicol Teratol 34:554–559.
34. D'Onofrio BM, Van Hulle CA, Goodnight JA, et al. 2012. Is maternal smoking during pregnancy a causal environmental risk factor for adolescent antisocial behavior? Testing etiological theories and assumptions. Psychol Med 42:1535–1545.
35. Daseking M, Petermann F, Tischler T, Waldmann HC. 2015. Smoking during pregnancy is a risk factor for executive function deficits in preschool-aged children. Geburtshilfe Frauenheilkd 75:64–71.
36. De Zeeuw P, Zwart F, Schrama R, et al. 2012. Prenatal exposure to cigarette smoke or alcohol and cerebellum volume in attention deficit/hyperactivity disorder and typical development. Transl Psychiatry 2:e84.
37. Dezateaux C, Stocks J, Dundas I, Fletcher ME. 1999. Impaired airway function and wheezing in infancy. The influence of maternal smoking and a genetic predisposition to asthma. Am J Respir Crit Care Med 159:403–410.
38. Downard CD, Grant SN, Maki AC, et al. 2012. Maternal cigarette smoking and the development of necrotizing enterocolitis. Pediatrics 130:78–82.
39. Dutra LM, Glantz SA. 2014. High international electronic cigarette use among never smoker adolescents. J Adolesc Health 55:595–597.
40. Ekblad M, Korkeila J, Lehtonen L. 2015. Smoking during pregnancy affects foetal brain development. Acts Paediatr 104:12–18.
41. El Marroun H, Schmidt MN, Franken IH, et al. 2013. Prenatal tobacco exposure and brain morphology: a prospective study in young children. Neuropsychopharmacology 39:792–800.
42. Elliot J, Vullermin P, Robinson P. 1998. Maternal cigarette smoking is associated with increased inner airway wall thickness in children who die from sudden infant death syndrome. Am J Respir Crit Care Med 158:802–806.
43. England L, Zhang J. 2007. Smoking and risk of preeclampsia: a systematic review. Front Biosci 12:2471–2483.
44. Ernst M, Moolchan ET, Robinson ML. 2001. Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psychiatry 40:630–641.
45. Ernst A, Kristensen SL, Toft G, et al. 2012. Maternal smoking during pregnancy and reproductive health of daughters: a follow-up study spanning two decades. Hum Reprod 27:3593–3600.
46. Fahy JV. 2001. Remodeling of the Airway epithelium in asthma. Am J Respir Crit Care Med 164:S46–S51.
47. Farquhar CM. 2005. Ectopic pregnancy. Lancet 366:583–591.
48. Fergusson DM, Lloyd M. 1991. Smoking during pregnancy and its effects on child cognitive ability from the ages of 8 to 12 years. Paediatr Perinat Epidemiol 5:189–200.
49. Fergusson DM, Horwood LJ. 2001. The Christchurch Health and Development Study: review of findings on child and adolescent mental health. Aust N Z J Psychiatry 35:287–296.
50. Fergusson DM, Horwood LJ, Lynskey MT. 1993. Maternal smoking before and after pregnancy: effects on behavioral outcomes in middle childhood. Pediatrics 92:815–822.
51. Fitzpatrick C, Barnett TA, Pagani LS. 2014. Parental bad habits breed bad behaviors in youth: Exposure to gestational smoke and child impulsivity. Int J Psychophysiol 93:17–21.
52. Fried PA, O'Connell CM. 1987. A comparison of the effects of prenatal exposure to tobacco, alcohol, cannabis and caffeine on birth size and subsequent growth. Neurotoxicol Teratol 9:79–85.
53. Fried PA, James DS, Watkinson B. 2001. Growth and pubertal milestones during adolescence in offspring prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 23:431–436.
54. Fried PA, Watkinson B, Gray R. 2003. Differential effects on cognitive functioning in 13- to 16-year-olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 25:427–436.
55. Gaysina D, Fergusson DM, Leve LD, et al. 2013. Maternal smoking during pregnancy and offspring conduct problems: evidence from 3 independent genetically sensitive researchdesigns. JAMA Psychiatry 70:956–963.
56. Geerts CC, Grobbee DE, van der Ent CK, et al. 2007. Tobacco smoke exposure of pregnant mothers and blood pressure in their newborns: results from the wheezing illnesses study Leidsche Rijn birth cohort. Hypertension 50:572–578.
57. Goldschmidt L, Cornelius MD, Day NL. 2012. Prenatal cigarette smoke exposure and early initiation of multiple substance use. Nicotine Tob Res 14:694–702.
58. Grewal J, Carmichael SL, Ma C, et al. 2008. Maternal periconceptional smoking and alcohol consumption and risk for select congenital anomalies. Birth Defects Res Part a Clin Mol Teratol 82:519–526.
59. Gunnerbeck A, Edstedt Bonamy AK, Wikstrom AK, et al. 2014. Maternal snuff use and smoking and the risk of oral cleft malformations–a population-based cohort study. PLoS One 9:e84715.
60. Hackshaw A, Rodeck C, Boniface S. 2011. Maternal smoking in pregnancy and birth defects: a systematic review based on 173 687 malformed cases and 11.7 million controls. Hum Reprod Update 17:589–604.
61. Haghighi A, Schwartz DH, Abrahamowicz M, et al. 2013. Prenatal exposure to maternal cigarette smoking, amygdala volume, and fat intake in adolescence. JAMA Psychiatry 70:98–105.
62. Hakonsen LB, Ernst A, Ramlau-Hansen CH. 2014. Maternal cigarette smoking during pregnancy and reproductive health in children: a review of epidemiological studies. Asian J Androl 16:39–49.
63. Harrod CS, Reynolds RM, Chasan-Taber L, et al. 2014. Quantity and timing of maternal prenatal smoking on neonatal body composition: the healthy start study. J Pediatr 165:707–712.
64. Hollams EM, de Klerk NH, Holt PG, Sly PD. 2014. Persistent effects of maternal smoking during pregnancy on lung function and asthma in adolescents. Am J Respir Crit Care Med 189:401–407.
65. Holz NE, Boecker R, Baumeister S, et al. 2014. Effect of prenatal exposure to tobacco smoke on inhibitory control: neuroimaging results from at 25-year prospective study. JAMA Psychiatry 71:786–796.
66. Horne AW, Brown JK, Nio-Kobayashi J, et al. 2014. The association between smoking and ectopic pregnancy: why nicotine is BAD for your fallopian tube. PLoS One 9:e89400.
67. Jacobsen LK, Slotkin TA, Westerveld M, et al. 2006. Visuospatial memory deficits emerging during nicotine withdrawal in adolescents with prenatal exposure to active maternal smoking. Neuropsychopharmacology 31:1550–1561.
68. Jacobsen LK, Picciotto MR, Heath CJ, et al. 2007. Prenatal and adolescent exposure to tobacco smoke modulates the development of white matter microstructure. J Neurosci 27:13491–13498.
69. Jaddoe VW, Verburg BO, de Ridder MA, et al. 2007. Maternal smoking and fetal growth characteristics in different periods of pregnancy: the generation R study. Am J Epidemiol 165:1207–1215.
70. Jugessur A, Wilcox AJ, Murray JC, et al. 2012. Assessing the impact of nicotine dependence genes on the risk of facial clefts: An example of the use of national registry and biobank data. Nor Epidemiol 21:241–250.
71. Kahr MK, Padgett S, Shope CD, et al. 2015. A qualitative assessment of the perceived risks of electronic cigarette and hookah use in pregnancy. BMC Public Health 15:1273.
72. Kallen K. 2000. Maternal smoking during pregnancy and infant head circumference at birth. Early Hum Dev 58:197–204.
73. Kayemba-Kay's S, Ribrault A, Burguet A, et al. 2010. Maternal smoking during pregnancy and fetal growth. Effects in preterm infants of gestational age less than 33 weeks. Swiss Med Wkly 140:w13139.
74. Kho E, North R, Chan E, Stone P, et al. 2009. Changes in Doppler flow velocity waveforms and fetal size at 20 weeks gestation among cigarette smokers. Bjog 16:1300–1306.
75. Khoury MJ, Gomez-Farias M, Mulinare J. 1989. Does maternal cigarette smoking during pregnancy cause cleft lip and palate in offspring? Am J Dis Child 143:333–337.
76. Klings ES, Safaya S, Adewoye AH, et al. 2005. Differential gene expression in pulmonary artery endothelial cells exposed to sickle cell plasma. Physiol Genom 21:293–298.
77. Kyrklund-Blomberg NB, Granath F, Cnattingius S. 2005. Maternal smoking and causes of very preterm birth. Acta Obstet Gynecol Scand 84:572–577.
78. Lambe M, Hultman C, Torrang A, et al. 2006. Maternal smoking during pregnancy and school performance at age 15. Epidemiology 17:524–530.
79. Langley K, Rice F, van den Bree MB, Thapar A. 2005. Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behaviour. A review. Minerv Pediatr 57:359–371.
80. Lavezzi AM, Corna MF, Repetti ML, Matturri L. 2013a. Cerebellar Purkinje cell vulnerability to prenatal nicotine exposure in sudden unexplained perinatal death. Folia Neuropathol 51:290–301.
81. Lavezzi AM, Matturri L, Del Corno G, Johanson CE. 2013b. Vulnerability of fourth ventricle choroid plexus in sudden unexplained fetal and infant death syndromes related to smoking mothers. Int J Dev Neurosci 31:319–327.
82. Law KL, Stroud LR, LaGasse LL, et al. 2003. Smoking during pregnancy and newborn neurobehavior. Pediatrics 111:1318–1323.
83. Leve LD, Neiderhiser JM, Shaw DS, et al. 2013. The Early Growth and DevelopmentStudy: A prospective adoption study of child behavior from birth through middle childhood. Twin Res Hum Genet 16:412–423.
84. 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.
85. Liu J, Cohen RA, Gongvatana A, et al. 2011. Impact of prenatal exposure to cocaine and tobacco on diffusion tensor imaging and sensation seeking in adolescents. J Pediatr 159:771–775.
86. Longo CA, Fried PA, Cameron I, Smith AM. 2013. The long-term effects of prenatal nicotine exposure on response inhibition: an fMRI study of young adults. Neurotoxicol Teratol 39:9–18.
87. Longo CA, Fried P, Cameron IM, Smith A. 2014. The long-term effects of prenatal nicotine exposure on verbal working memory: an fMRI study of young adults. Drug Alcohol Depend 144:61–69.
88. Luck W, Nau H, Hansen R, Steldinger R. 1985. Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev Pharmacol Ther 8:384–395.
89. Machado J, Filho PVM, Petersen GO, Chatkin JM. 2011. Quantitative effects of tobacco smoking exposure on the maternal fetal circulation. BMC Preg Childbirth 11:24–30.
90. Maritz GS. 2013. Perinatal exposure to nicotine and implications for subsequent obstructive lung disease. Paediatr Respir Rev 14:3–8.
91. Maritz GS, Harding R. 2011. Life-long programming implications of exposure to tobacco smoking and nicotine before and soon after birth: evidence for altered lung development. Int J Environ Res Public Health 8:875–898.
92. Mark KS, Farquhar B, Chisolm MS, et al. 2015. Knowledge, attitudes, and practice of electronic cigarette use among pregnant women. J Addict Med 9:266–272.
93. Matta SG, Balfour DJ, Benowitz NL, et al. 2007. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190:269–319.
94. Mazurek JM, England LJ. 2016. Cigarette smoking among working women of reproductive age—United States, 2009–2013. Nicotine Tob Res 18:894–899.
95. Mitchell EA, Thompson JM, Robinson E, et al. 2002. Smoking. nicotine and tar and risk of small for gestational age babies. Acta Paediatr 91:323–328.
96. Montgomery SM, Ekbom A. 2002. Smoking during pregnancy and diabetes mellitus in a British longitudinal birth cohort. Bmj 324:26–27.
97. Morales-Suárez-Varela MM, Bille C, Christensen K, Olsen J. 2006. Smoking habits, nicotine use, and congenital malformations. Obstet Gynecol 107:51–57.
98. Morrow RJ, Ritchie JW, Bull SB. 1988. Maternal cigarette smoking: the effects on umbilical and uterine blood flow velocity. Am J Obstet Gynecol 159:1069–1071.
99. Mortensen EL, Michaelsen KF, Sanders SA, Reinisch JM. 2005. A dose-response relationship between maternal smoking during late pregnancy and adult intelligence in male offspring. Paediatr Perinat Epidemiol 19:4–11.
100. Muller KU, Mennigen E, Ripke S, IMAGEN Consortium, et al. 2013. Altered reward processing in adolescents with prenatal exposure to maternal cigarette smoking. JAMA Psychiatry 70:847–856.
101. Naeye RL, Peters EC. 1984. Mental development of children whose mothers smoked during pregnancy. Obstet Gynecol 64:601–607.
102. Nitzkin JL. 2014. The case in favor of E-cigarettes for tobacco harm reduction. Int J Environ Res Public Health 11:6459–6471.
103. Oken E, Huh SY, Taveras EM, Rich-Edwards JW, Gillman MW. 2005. Associations of maternal prenatal smoking with child adiposity and blood pressure. Obes Res 13:2021–2028.
104. Oken E, Levitan EB, Gillman MW. 2008. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond) 32:201–210.
105. Orlebeke JF, Knol DL, Verhulst FC. 1999. Child behavior problems increased by maternal smoking during pregnancy. Arch Environ Health 54:15–19.
106. Pagani LS. 2014. Environmental tobacco smoke exposure and brain development. The case of attention deficit/hyperactivity disorder. Neurosci Biobehav Rev 44:195–205.
107. Park A, O'Malley SS, King SL, Picciotto MR. 2014. Mediating role of stress reactivity in the effects of prenatal tobacco exposure on childhood mental health outcomes. Nicotine Tob Res 16:174–185.
108. Paslakis G, Buchmann AF, Westphal S, et al. 2014. Intrauterine exposure to cigarette smoke is associated with increased ghrelin concentrations in adulthood. Neuroendocrinology 99:123–129.
109. Pattenden S, Antova T, Neuberger M, et al. 2006. Parental smoking and children's respiratory health: Independent effects of prenatal and postnatal exposure. Tobacco Control 15:294–301.
110. Piper BJ, Corbett SM. 2012. Executive function profile in the offspring of women that smoked during pregnancy. Nicotine Tob Res 14:191–199.
111. Pringle PJ, Geary MP, Rodeck CH, et al. 2005. The influence of cigarette smoking on antenatal growth, birth size, and the insulin-like growth factor axis. J Clin Endocrinol Metab 90:2556–2562.
112. Power C, Jefferis BJ. 2002. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol 31:413–419.
113. Power C, Atherton K, Thomas C. 2010. Maternal smoking in pregnancy, adult adiposity and other risk factors for cardiovascular disease. Atherosclerosis 211:643–648.
114. Pretorius E. 2004. Corticosteroids, depression and the role of serotonin. Rev Neurosci 15:109–116.
115. Rasanen P, Hakko H, Isohanni M, et al. 1999. Maternal smoking during pregnancy and risk of criminal behavior among adult male offspring in the Northern Finland 1966 Birth Cohort. Am J Psychiatry 156:857–862.
116. Ravnborg TL, Jensen TK, Andersson AM, et al. 2011. Prenatal and adult exposures to smoking are associated with adverse effects on reproductive hormones, semen quality, final height and body mass index. Hum Reprod 26:1000–1011.
117. Roberts KH, Munafo MR, Rodriguez D, et al. 2005. Longitudinal analysis of the effect of prenatal nicotine exposure on subsequent smoking behavior of offspring. Nicotine Tob Res 7:801–808.
118. Roza SJ, Verburg BO, Jaddoe VW, et al. 2007. Effects of maternal smoking in pregnancy on prenatal brain development. The Generation R Study. Eur J Neurosci 25:611–617.
119. Rydell M, Cnattingius S, Granath F, et al. 2012. Prenatal exposure to tobacco and future nicotine dependence: population-based cohort study. Br J Psychiatry 200:202–209.
120. Sastry BV. 1991. Placental toxicology: tobacco smoke, abused drugs, multiple chemical interactions, and placental function. Reprod Fertil Dev 3:355–372.
121. Sekhon HS, Keller JA, Benowitz NL, Spindel ER. 2001. Prenatal nicotine exposure alters pulmonary function in newborn rhesus monkeys. Am J Respir Crit Care Med 164:989–994.
122. Sekhon HS, Keller JA, Proskocil BJ, et al. 2002. Maternal nicotine exposure upregulates collagen gene expression in fetal monkey lung. Association with alpha7 nicotinic acetylcholine receptors. Am J Respir Cell Mol Biol 26:31–41.
123. Shaw GM, Carmichael SL, Vollset SE, et al. 2009. Mid-pregnancy cotinine and risks of orofacial clefts and neural tube defects. J Pediatr 154:17–19.
124. Shelton KH, Boivin J, Hay D, et al. 2009. Examining differences in psychological adjustment problems among children conceived by assisted reproductive technologies. Int J Behav Dev 33:385–392.
125. Silva D, Colvin L, Hagemann E, et al. 2014. Environmental riskfactors by gender associated with attention-deficit/hyperactivitydisorder. Pediatrics 133:e14–e22.
126. Smith LM, Cloak CC, Poland RE, et al. 2003. Prenatal nicotine increases testosterone levels in the fetus and female offspring. Nicotine Tob Res 5:369–374.
127. Slotkin TA. 1998. Fetal nicotine or cocaine exposure: which one is worse? J Pharmacol Exp Ther 285:931–945.
128. Slotkin TA, Lappi SE, McCook EC, et al. 1995. Loss of neonatal hypoxia tolerance after prenatal nicotine exposure: implications for sudden infant death syndrome. Brain Res Bull 38:69–75.
129. Stene-Larsen K, Borge AI, Vollrath ME. 2009. Maternal smoking in pregnancy and externalizing behavior in 18-month-old children: results from a population-based prospective study. J Am Acad Child Adolesc Psychiatry 48:283–289.
130. Storgaard L, Bonde JP, Ernst E, et al. 2003. Does smoking during pregnancy affect sons' sperm counts? Epidemiology 14:278–286.
131. Stroud LR, Papandonatos GD, Shenassa E, et al. 2014. Prenatal glucocorticoids and maternal smoking during pregnancy independently program adult nicotine dependence in daughters: a 40-year prospective study. Biol Psychiatry 75:47–55.
132. Suter MA, Mastrobattista J, Sachs M, Aagaard K. 2015. Is there evidence for potential harm of electronic cigarette use in pregnancy? Birth Defects Res a Clin Mol Teratol 103:186–195.
133. Syme C, Abrahamowicz M, Mahboubi A, et al. 2010. Prenatal exposure to maternal cigarette smoking and accumulation of intra-abdominal fat during adolescence. Obesity (Silver Spring) 18:1021–1025.
134. Tager IB, Hanrahan JP, Tosteson TD, et al. 1992. Lung function, pre-and post-natal smoke exposure, and wheezing in the first yaer of life. Am Rev Respir Dis 147:811–817.
135. Tiesler CM, Heinrich J. 2014. Prenatal nicotine exposure and child behavioural problems. Eur Child Adolesc Psychiatry 23:913–929.
136. Thakur GA, Sengupta SM, Grizenko N, et al. 2013. Maternal smoking during pregnancy and ADHD: a comprehensive clinical and neurocognitive characterization. Nicotine Tob Res 15:149–157.
137. Tong VT, Dietz PM Morrow B, et al. 2013. Trends in Smoking Before, During, and After Pregnancy — Pregnancy Risk Assessment Monitoring System, United States, 40 Sites, 2000–2010. MMWR Surveill Summ 62:1–19.
138. Toschke AM, Koletzko B, Slikker W, Jr, et al. 2002. Childhood obesity is associated with maternal smoking in pregnancy. Eur J Pediatr 161:445–448.
139. Weitzman M, Byrd RS, Aligne CA, Moss M. 2002. The effects of tobacco exposure on children's behavioral and cognitive functioning: implications for clinical and public health policy and future research. Neurotoxicol Teratol 24:397–406.
140. Wikstrom AK, Stephansson O, Cnattingius S. 2010. Tobacco use during pregnancy and preeclampsia risk: effects of cigarette smoking and snuff. Hypertension 55:1254–1259.
141. Winzer-Serhan UH. 2008. Long-term consequences of maternal smoking and developmental chronic nicotine exposure. Front Biosci 13:636–649.
142. Zhu JL, Olsen J, Llew Z, et al. 2014. Parental smoking during pregnancy and ADHD in children: the Danish national birth cohort. Pediatrics 134:e382–e388.