The impact of cigarette smoking on the health of descendants

References

• Centers for Disease Control and Prevention (CDC). Vital signs: current cigarette smoking among adults aged ≥18 years – United States, 2009. MMWR Morb. Mortal. Wkly Rep.59(35), 1135–1140 (2010).
   PubMedGoogle Scholar
• Statistics Canada. Smoking, 2009: Canadian Community Health Survey. Health Fact Sheets. Statistics Canada. Ottawa, ON, Canada (2010).
   Google Scholar
• Centers for Disease Control and Prevention (CDC). Smoking during pregnancy – United States, 1990–2002. MMWR Morb. Mortal. Wkly Rep.53, 911–915 (2004).
   PubMedGoogle Scholar
• Tong V, Jones J, Dietz P, D’Angelo D, Bombard J. Trends in smoking before, during, and after pregnancy – Pregnancy Risk Assessment Monitoring System (PRAMS), United States, 31 Sites, 2000–2005. MMWR Surveill. Summ.58, 1–29 (2009).
   Google Scholar
• Al Sa-hab B, Saqib M, Hauser G, Tamim H. Prevalence of smoking during pregnancy and associated risk factors among Canadian women: a national survey. BMC Pregnancy Childbirth10, 1–9 (2010).
   PubMed Web of Science ®Google Scholar
• Soares SR, Melo MA. Cigarette smoking and IVF. Expert. Rev. Obstet. Gynecol.3, 555–563 (2008).
   Google Scholar
• Soares SR, Melo MA. Cigarette smoking and reproductive function. Curr. Opin. Obstet. Gynecol.20, 281–291 (2008).
   PubMed Web of Science ®Google Scholar
• Kiziler AR, Aydemir B, Onaran I et al. High levels of cadmium and lead in seminal fluid and blood of smoking men are associated with high oxidative stress and damage in infertile subjects. Biol. Trace Elem. Res. Winter120, 82–91 (2007).
   PubMed Web of Science ®Google Scholar
• Hackshaw A, Rodeck C, Boniface S. Maternal smoking in pregnancy and birth defects: a systematic review based on 173,687 malformed cases and 11.7 million controls. Hum. Reprod. Update17, 589–604 (2011).
   PubMed Web of Science ®Google Scholar
• Quinton AE, Cook CM, Peek MJ. The relationship between cigarette smoking, endothelial function and intrauterine growth restriction in human pregnancy. BJOG115, 780–784 (2008).
   PubMed Web of Science ®Google Scholar
• Talbot P. In vitro assessment of reproductive toxicity of tobacco smoke and its constituents. Birth Defects Res. C Embryo Today84, 61–72 (2008).
   PubMedGoogle Scholar
• Rogers JM. Tobacco and pregnancy. Reprod. Toxicol.28, 152–160 (2009).
   PubMed Web of Science ®Google Scholar
• Dietz P, Engand L, Shapiro-Mendonza C, Tong V, Farr S, Callaghan W. Infant morbidity and mortality attributable to prenatal smoking in the US. Am. J. Prev. Med.39, 45–52 (2010).
   PubMed Web of Science ®Google Scholar
• Cornelius MD, De Genna NM, Leech SL, Willford JA, Goldschmidt L, Day NL. Effects of prenatal cigarette smoke exposure on neurobehavioral outcomes in 10-year-old children of adolescent mothers. Neurotoxicol. Teratol.33, 137–144 (2011).
   PubMed Web of Science ®Google Scholar
• Stroud L, Paster R, Goodwin M et al. Maternal smoking during pregnancy and neonatal behavior: a large-scale community study. Pediatrics23, e842–e848 (2009).
   Google Scholar
• Lotfipour S, Leonard G, Perron M et al. Prenatal exposure to maternal cigarette smoking interacts with a polymorphism in the alfa-6 nicotinic acetylcholine receptor gene to influence drug use and striatum volume in adolescence. Mot. Psychiatry15, 6–8 (2010).
   PubMed Web of Science ®Google Scholar
• Lewis B, Kirchner H, Short E et al. Prenatal cocaine and tobacco effects on children’s language trajectories. Pediatrics1151, 102–106 (2007).
   Google Scholar
• Key A, Ferguson M, Mofese D, Peach K, Lehman C, Molfese V. Smoking during pregnancy affects speech-processing ability in newborn infants. Environ. Health Perspect.115, 623–629 (2007).
   PubMed Web of Science ®Google Scholar
• Silberg JL, Parr T, Neale MC, Rutter M, Angold A, Eaves LJ. Maternal smoking during pregnancy and risk to boys conduct disturbance: an examination of the causal hypothesis. Biol. Psychiatry53, 130–135 (2003).
   PubMed Web of Science ®Google Scholar
• Slotkin TA, Lappi SE, Seidler FJ. Impact of fetal nicotine exposure on development of rat brain regions: critical sensitive periods or effects of withdrawal? Brain Res. Bull.31, 319–328 (1993).
   PubMed Web of Science ®Google Scholar
• Slotkin TA. Fetal nicotine or cocaine exposure: which one is worse? J. Pharmacol. Exp. Ther.285, 931–945 (1998).
   PubMed Web of Science ®Google Scholar
• Carter S, Paterson J, Gao W, Iustini L. Maternal smoking during pregnancy and behavior problems in a birth cohort of 2-year-old Pacific children in New Zealand. Early Hum. Dev.84, 59–66 (2008).
   PubMed Web of Science ®Google Scholar
• Huijbregts S, Seguin J, Zoccolillo M, Boivin M, Tremblay R. Role of maternal prenatal smoking, prenatal antisocial behavior and early childhood physical aggression. Dev. Psychopathol.20, 437–453 (2008).
   PubMed Web of Science ®Google Scholar
• Asford J, van Lier P, Timmermans M, Cuijpers P, Koot H. Prenatal smoking and internalizing and externalizing problems in children studied from childhood to late adolescence. J. Am. Acad. Child. Adolesc. Psychiatry47, 779–787 (2008).
   PubMed Web of Science ®Google Scholar
• Brion MJ, Victora C, Matijasevich A et al. Maternal smoking and child psychological problems: disentangling causal and noncausal effects. Pediatrics126, e57–e65 (2010).
   Google Scholar
• Gatzke-Kopp LM, Beauchaine TP. Direct and passive prenatal nicotine exposure and the development of externalizing psychopathology. Child Psychiatry Hum. Dev.38, 255–269 (2007).
   PubMed Web of Science ®Google Scholar
• Murray J, Irving B, Farrington D, Colman I, Bloxsom C. Very early predictors of conduct problems and crime: results from a national cohort study. J. Child Psychol. Psychiatry51, 1198–1207 (2010).
   PubMed Web of Science ®Google Scholar
• Wakschlag LS, Pickett KE, Cook E, Benowitz NL, Leventhal BL. Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review. Am. J. Public Health92, 966–974 (2002).
   PubMed Web of Science ®Google Scholar
• Wakschlag LS, Pickett KE, Kasza KE, Loeber R. Is prenatal smoking associated with a developmental pattern of conduct problems in young boys? J. Am. Acad. Child Adolesc. Psychiatry45, 461–467 (2006).
   PubMed Web of Science ®Google Scholar
• Julvez J, Ribas-Fitó N, Torrent M, Forns M, Garcia-Esteban R, Sunyer J. Maternal smoking habits and cognitive development of children at age 4 years in a population-based birth cohort. Int. J. Epidemiol.36, 825–832 (2007).
   PubMed Web of Science ®Google Scholar
• Weitzman M, Byrd RS, Aligne CA, Moss M. 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 (2002).
   PubMed Web of Science ®Google Scholar
• Huizink AC, Mulder EJ. Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neurosci. Biobehav. Rev.30, 24–41 (2006).
   PubMed Web of Science ®Google Scholar
• Maughan B, Taylor A, Caspi A, Moffit TE. Prenatal smoking and early childhood conduct problems: testing genetic and environmental explanations of the association. Arch. Gen. Psychiatry61, 836–843 (2004).
   PubMed Web of Science ®Google Scholar
• Maughan B, Taylor C, Taylor A, Butler N, Bynner J. Prenatal smoking and childhood conduct problems: a causal association. J. Child Psychol. Psychiatry42, 1021–1028 (2001).
   PubMed Web of Science ®Google Scholar
• Oken E, Levitan EB, Gillman MW. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int. J. Obes.32, 201–210 (2008).
   PubMed Web of Science ®Google Scholar
• Ino T. Maternal smoking during pregnancy and offspring obesity: meta-analysis. Pediatr. Int.52, 94–99 (2010).
   PubMed Web of Science ®Google Scholar
• Durmus B, Kruithof CJ, Gillman MH et al. Parental smoking during pregnancy, early growth, and risk of obesity in preschool children: the Generation R Study. Am. J. Clin. Nutr.94, 164–171 (2011).
   PubMed Web of Science ®Google Scholar
• Bateson P. Developmental plasticity and evolutionary biology. J. Nutr.137, 1060–1062 (2007).
   PubMed Web of Science ®Google Scholar
• Koshy G, Delpisheh A, Brabin BJ. Dose response association of pregnancy cigarette smoke exposure, childhood stature, overweight and obesity. Eur. J. Public Health21, 286–291 (2011).
   PubMed Web of Science ®Google Scholar
• Storgaard L, Bonde JP, Ernst E et al. Does smoking during pregnancy affect sons’ sperm counts? Epidemiology14, 278–286 (2003).
   PubMed Web of Science ®Google Scholar
• Jensen TK, Jørgensen N, Punab M et al. Association of in utero exposure to maternal smoking with reduced semen quality and testis size in adulthood: a cross-sectional study of 1770 young men from the general population in five European countries. Am. J. Epidemiol.159, 49–58 (2004).
   PubMed Web of Science ®Google Scholar
• Mamsen LS, Lutterodt MC, Andersen EW et al. Cigarette smoking during early pregnancy reduces the number of embryonic germ and somatic cells. Human Reprod.11, 2755–2761 (2010).
   Google Scholar
• Jensen TK, Joffe M, Scheike T et al. Early exposure to smoking and future fecundity among Danish twins. Int. J. Androl.29, 603–613 (2006).
   PubMedGoogle Scholar
• Skakkebaek NE, Rajpert-De Meyts E, Main KM. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum. Reprod.16, 972–978 (2001).
   PubMed Web of Science ®Google Scholar
• Sharpe RM. Pathways of endocrine disruption during male sexual differentiation and masculinization. Best Pract. Res. Clin. Endocrinol. Metab.20, 91–110 (2006).
   PubMed Web of Science ®Google Scholar
• Bendsen E, Byskov AG, Laursen SB, Larsen HP, Andersen CY, Westergaard LG. Number of germ cells and somatic cells in human fetal testes during the first weeks after sex differentiation. Hum. Reprod.18, 13–18 (2003).
   PubMed Web of Science ®Google Scholar
• Künzle R, Mueller MD, Hänggi W, Birkhäuser MH, Drescher H, Bersinger NA. Semen quality of male smokers and nonsmokers in infertile couples. Fertil. Steril.79, 287–291 (2003).
   PubMed Web of Science ®Google Scholar
• Ramlau-Hansen CH, Thulstrup AM, Storgaard L, Toft G, Olsen J, Bonde JP. Is prenatal exposure to tobacco smoking a cause of poor semen quality? A follow-up study. Am. J. Epidemiol.165, 1372–1379 (2007).
   PubMed Web of Science ®Google Scholar
• Pocar P, Fischer B, Klonisch T, Hombach-Klonisch S. Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Curr. Med. Chem.12, 599–616 (2005).
   PubMed Web of Science ®Google Scholar
• Coutts SM, Fulton N, Anderson RA. Environmental toxicant-induced germ cell apoptosis in the human fetal testis. Hum. Reprod.22, 2912–2918 (2007).
   PubMed Web of Science ®Google Scholar
• Bendsen E, Byskov AG, Andersen CY, Westergaard LG. Number of germ cells and somatic cells in human fetal ovaries during the first weeks after sex differentiation. Hum. Reprod.21, 30–35 (2006).
   PubMed Web of Science ®Google Scholar
• Zenzes MT. Smoking and reproduction: gene damage to human gametes and embryos. Hum. Reprod. Update6, 122–131 (2000).
   PubMed Web of Science ®Google Scholar
• Hockley SL, Arlt VM, Brewer D et al. AHR- and DNA-damage-mediated age expression responses induced by benzo[a]pyrene in human cell lines. Chem. Res. Toxicol.20, 1797–1810 (2007).
   PubMed Web of Science ®Google Scholar
• Matikainen TM, Moriyama T, Morita Y et al. Ligand activation of the aromatic hydrocarbon receptor transcription factor drives Bax-dependent apoptosis in developing fetal ovarian germ cells. Endocrinology143, 615–620 (2002).
   PubMed Web of Science ®Google Scholar
• Lutterodt MC, Sørensen KP, Larsen KB, Skouby SO, Andersen CY, Byskov AG. The number of oogonia and somatic cells in the human female embryo and fetus in relation to whether or not exposed to maternal cigarette smoking. Hum. Reprod.24, 2558–2566 (2009).
   PubMed Web of Science ®Google Scholar
• Ye X, Skjaerven R, Basso O et al.In utero exposure to tobacco smoke and subsequent reduced fertility in females. Human Reprod.11, 2901–2906 (2010).
   Google Scholar
• Shrestha A, Nohr EA, Bech BH, Ramlau-Hansen CH, Olsen J. Smoking and alcohol use during pregnancy and age of menarche in daughters. Hum. Reprod.26, 259–265 (2011).
   PubMed Web of Science ®Google Scholar
• Smith LM, Cloak CC, Poland RE, Torday J, Ross MG. Prenatal nicotine increases testosterone levels in the fetus and female offspring. Nicotine Tob. Res.5, 369–374 (2003).
   PubMed Web of Science ®Google Scholar
• US Environmental Protection Agency (EPA). Supplemental guidance for assessing susceptibility from early-life exposure to arcinogens. Risk Assessment Forum. EPA/630/R-03/003F. US Environmental Protection Agency (EPA), Washington DC, WA, USA (2005).
   Google Scholar
• Sorahan T, McKinney PA, Mann JR et al. Childhood cancer and parental use of tobacco: findings from the inter-regional epidemiological study of childhood cancer (IRESCC). Br. J. Cancer84, 141–146 (2001).
   PubMed Web of Science ®Google Scholar
• Yauk CL, Berndt ML, Williams A, Rowan-Carroll A, Douglas GR, Stämpfli MR. Mainstream tobacco smoke causes paternal germ-line DNA mutation. Cancer Res.67, 5103–5106 (2007).
   PubMed Web of Science ®Google Scholar
• Cooper AR, Moley KH. Maternal tobacco use and its preimplantation effects on fertility: more reasons to stop smoking. Semin. Reprod. Med.26, 204–212 (2008).
   PubMed Web of Science ®Google Scholar
• Altshuler K, Berg M, Frazier LM et al. Critical Periods in Development. Paper 2003-2. OCHP Paper Series on Children’s Health and the Environment. US Environmental Protection Agency (EPA), Washington DC, WA, USA (2003).
   Google Scholar
• Ortega-García JA, Martin M, López-Fernández MT et al. Transgenerational tobacco smoke exposure and childhood cancer: an observational study. J. Paediatr. Child Health46, 291–295 (2010).
   PubMed Web of Science ®Google Scholar
• Sorahan T, Lancashire RJ. Parental cigarette smoking and childhood risks of hepatoblastoma: OSCC data. Br. J. Cancer90, 1016–1018 (2004).
   PubMed Web of Science ®Google Scholar
• Rudant J, Menegaux F, Leverger G et al. Childhood hematopoietic malignancies and parental use of tobacco and alcohol: the ESCALE study (SFCE). Cancer Causes Control19, 1277–1290 (2008).
   PubMed Web of Science ®Google Scholar
• Liu R, Zhang L, McHale CM, Hammond SK. Paternal smoking and risk of childhood acute lymphoblastic leukemia: systematic review and meta-analysis. J. Oncol.2011, 854584 (2011).
   PubMedGoogle Scholar
• Chang JS. Parental smoking and childhood leukemia. Methods Mol. Biol.472, 103–137 (2009).
   PubMedGoogle Scholar