CoChat
Sign Up
Cited by 72

The DOI matches its Crossref record; 20 of the 20 references it cites were found in a registry or an index.

Epigenetic Alterations of Maternal Tobacco Smoking during Pregnancy: A Narrative Review

Nakamura, Aurélie, François, Olivier, Lepeule, Johanna·2021·International Journal of Environmental Research and Public Health
DOI 10.3390/ijerph18105083PMC PMC8151244
Open this paper in CoChat — free account

Abstract

In utero exposure to maternal tobacco smoking is the leading cause of birth complications in addition to being associated with later impairment in child’s development. Epigenetic alterations, such as DNA methylation (DNAm), miRNAs expression, and histone modifications, belong to possible underlying mechanisms linking maternal tobacco smoking during pregnancy and adverse birth outcomes and later child’s development. The aims of this review were to provide an update on (1) the main results of epidemiological studies on the impact of in utero exposure to maternal tobacco smoking on epigenetic mechanisms, and (2) the technical issues and methods used in such studies. In contrast with miRNA and histone modifications, DNAm has been the most extensively studied epigenetic mechanism with regard to in utero exposure to maternal tobacco smoking. Most studies relied on cord blood and children’s blood, but placenta is increasingly recognized as a powerful tool, especially for markers of pregnancy exposures. Some recent studies suggest reversibility in DNAm in certain genomic regions as well as memory of smoking exposure in DNAm in other regions, upon smoking cessation before or during pregnancy. Furthermore, reversibility could be more pronounced in miRNA expression compared to DNAm. Increasing evidence based on longitudinal data shows that maternal smoking-associated DNAm changes persist during childhood. In this review, we also discuss some issues related to cell heterogeneity as well as downstream statistical analyses used to relate maternal tobacco smoking during pregnancy and epigenetics. The epigenetic effects of maternal smoking during pregnancy have been among the most widely investigated in the epigenetic epidemiology field. However, there are still huge gaps to fill in, including on the impact on miRNA expression and histone modifications to get a better view of the whole epigenetic machinery. The consistency of maternal tobacco smoking effects across epigenetic marks and across tissues will also provide crucial information for future studies. Advancement in bioinformatic and biostatistics approaches is key to develop a comprehensive analysis of these biological systems.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/ijerph18105083

Cites

20 of 20 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 20 references

Research works printed but not linked: 151

  1. Drake, 2018, Cigarette Smoking during Pregnancy: United States, 2016, NCHS Data Brief., 305, 1
  2. Krist, 2021, Interventions for Tobacco Smoking Cessation in Adults, Including Pregnant Persons: US Preventive Services Task Force Recommendation Statement, JAMA, 325, 265, 10.1001/jama.2020.25019 · DOI · Paper page
  3. Demiguel, 2018, Évolution de La Consommation de Tabac à l’occasion d’une Grossesse En France En 2016, Bull. Epidemiol. Hebd., 35, 694
  4. Ballon, 2019, Which Modifiable Prenatal Factors Mediate the Relation between Socio-economic Position and a Child’s Weight and Length at Birth?, Matern. Child. Nutr., 15, e12878, 10.1111/mcn.12878 · DOI
  5. Cameron, 2015, A Review of the Relationship between Socioeconomic Position and the Early-Life Predictors of Obesity, Curr. Obes. Rep., 4, 350, 10.1007/s13679-015-0168-5 · DOI
  6. Nakamura, 2020, Maternal Education and Offspring Birth Weight for Gestational Age: The Mediating Effect of Smoking during Pregnancy, Eur. J. Public Health, 30, 1001, 10.1093/eurpub/ckaa076 · DOI
  7. Shipton, D., Tappin, D.M., Vadiveloo, T., Crossley, J.A., Aitken, D.A., and Chalmers, J. (2009). Reliability of Self Reported Smoking Status by Pregnant Women for Estimating Smoking Prevalence: A Retrospective, Cross Sectional Study. BMJ, 339. · DOI
  8. Coleman, T., Chamberlain, C., Davey, M., Cooper, S.E., and Leonardi-Bee, J. (2015). Pharmacological Interventions for Promoting Smoking Cessation during Pregnancy. Cochrane Database Syst. Rev., 2015. · DOI · Paper page
  9. Morris, 2011, Molecular Mechanisms of Maternal Cannabis and Cigarette Use on Human Neurodevelopment, Eur. J. Neurosci., 34, 1574, 10.1111/j.1460-9568.2011.07884.x · DOI
  10. Dempsey, 2002, Accelerated Metabolism of Nicotine and Cotinine in Pregnant Smokers, J. Pharmacol. Exp. Ther., 301, 594, 10.1124/jpet.301.2.594 · DOI · Paper page
  11. Porter, 2008, In Utero Tobacco Exposure Is Associated with Modified Effects of Maternal Factors on Fetal Growth, Am. J. Obstet. Gynecol., 198, 66.e1, 10.1016/j.ajog.2007.06.078 · DOI
  12. Gould, G.S., Havard, A., Lim, L.L., and Kumar, R. (2020). Exposure to Tobacco, Environmental Tobacco Smoke and Nicotine in Pregnancy: A Pragmatic Overview of Reviews of Maternal and Child Outcomes, Effectiveness of Interventions and Barriers and Facilitators to Quitting. IJERPH, 17. · DOI
  13. Philips, E.M., Santos, S., Trasande, L., Aurrekoetxea, J.J., Barros, H., von Berg, A., Bergström, A., Bird, P.K., Brescianini, S., and Ní Chaoimh, C. (2020). Changes in Parental Smoking during Pregnancy and Risks of Adverse Birth Outcomes and Childhood Overweight in Europe and North America: An Individual Participant Data Meta-Analysis of 229,000 Singleton Births. PLoS Med., 17. · DOI
  14. Roelands, 2009, Consequences of Smoking during Pregnancy on Maternal Health, J. Womens Health, 18, 867, 10.1089/jwh.2008.1024 · DOI
  15. Suter, 2010, Genetic and Epigenetic Influences Associated with Intrauterine Growth Restriction Due to in Utero Tobacco Exposure, Pediatr. Endocrinol. Rev., 8, 94
  16. Greenhalgh, E., Ford, C., and Winstanley, M. (2020). 3.8 Child health and maternal smoking before and after birth. Tobacco in Australia, Cancer Council Victoria. Available online: https://www.tobaccoinaustralia.org.au/chapter-3-health-effects/3-8-child-health-and-maternal-smoking.
  17. Knopik, 2009, Maternal Smoking during Pregnancy and Child Outcomes: Real or Spurious Effect?, Dev. Neuropsychol., 34, 1, 10.1080/87565640802564366 · DOI
  18. Quelhas, 2018, The Association between Active Tobacco Use during Pregnancy and Growth Outcomes of Children under Five Years of Age: A Systematic Review and Meta-Analysis, BMC Public Health, 18, 1, 10.1186/s12889-018-6137-7 · DOI · Paper page
  19. Juárez, S.P., and Merlo, J. (2013). Revisiting the Effect of Maternal Smoking during Pregnancy on Offspring Birthweight: A Quasi-Experimental Sibling Analysis in Sweden. PLoS ONE, 8. · DOI
  20. Banderali, 2015, Short and Long Term Health Effects of Parental Tobacco Smoking during Pregnancy and Lactation: A Descriptive Review, J. Transl. Med., 13, 1, 10.1186/s12967-015-0690-y · DOI · Paper page
  21. Oken, 2008, Maternal Smoking during Pregnancy and Child Overweight: Systematic Review and Meta-Analysis, IJO, 32, 201
  22. McEvoy, 2017, Pulmonary Effects of Maternal Smoking on the Fetus and Child: Effects on Lung Development, Respiratory Morbidities, and Life Long Lung Health, Paediatr. Resp. Rev., 21, 27
  23. Noakes, 2006, Maternal Smoking Is Associated with Impaired Neonatal Toll-like-Receptor-Mediated Immune Responses, Eur. Resp. J., 28, 721, 10.1183/09031936.06.00050206 · DOI
  24. Dong, 2018, Prenatal Exposure to Maternal Smoking during Pregnancy and Attention-Deficit/Hyperactivity Disorder in Offspring: A Meta-Analysis, Reprod. Toxicol., 76, 63, 10.1016/j.reprotox.2017.12.010 · DOI · Paper page
  25. Froggatt, 2020, Infant Neurobehavioural Consequences of Prenatal Cigarette Exposure: A Systematic Review and Meta-analysis, Acta Paediatr., 109, 1112, 10.1111/apa.15132 · DOI
  26. Polanska, 2015, Smoking and Alcohol Drinking during Pregnancy as the Risk Factors for Poor Child Neurodevelopment-A Review of Epidemiological Studies, Int. J. Occup. Med. Environ. Health, 28, 419, 10.13075/ijomeh.1896.00424 · DOI
  27. Clifford, 2012, Effects of Maternal Cigarette Smoking during Pregnancy on Cognitive Parameters of Children and Young Adults: A Literature Review, Neurotoxicol. Teratol., 34, 560, 10.1016/j.ntt.2012.09.004 · DOI
  28. Kristjansson, 2018, Maternal Smoking during Pregnancy and Academic Achievement of Offspring over Time: A Registry Data-Based Cohort Study, Int. J. Prev. Med., 113, 74, 10.1016/j.ypmed.2018.05.017 · DOI
  29. Rauschert, 2019, Maternal Smoking during Pregnancy Induces Persistent Epigenetic Changes into Adolescence, Independent of Postnatal Smoke Exposure and Is Associated with Cardiometabolic Risk, Front. Genet., 10, 770, 10.3389/fgene.2019.00770 · DOI
  30. Berlin, 2018, Maternal Smoking during Pregnancy and Negative Health Outcomes in the Offspring, Nicotine Tob Res., 6, 663, 10.1093/ntr/nty035 · DOI
  31. Knopik, 2012, The Epigenetics of Maternal Cigarette Smoking during Pregnancy and Effects on Child Development, Dev. Psychopathol., 24, 1377, 10.1017/S0954579412000776 · DOI · Paper page
  32. Thapar, 2003, Maternal Smoking during Pregnancy and Attention Deficit Hyperactivity Disorder Symptoms in Offspring, Am. J. Psychiatry, 160, 1985, 10.1176/appi.ajp.160.11.1985 · DOI
  33. Thapar, 2009, Prenatal Smoking Might Not Cause Attention-Deficit/Hyperactivity Disorder: Evidence from a Novel Design, Biol. Psychiatry, 66, 722, 10.1016/j.biopsych.2009.05.032 · DOI · Paper page
  34. Lodge, 2018, Grandmaternal Smoking Increases Asthma Risk in Grandchildren: A Nationwide Swedish Cohort, Clin. Exp. Allergy, 48, 167, 10.1111/cea.13031 · DOI
  35. Accordini, 2018, A Three-Generation Study on the Association of Tobacco Smoking with Asthma, Int. J. Epidemiol., 47, 1106, 10.1093/ije/dyy031 · DOI · Paper page
  36. Barker, 1993, Fetal Origins of Coronary Heart Disease, Br. Heart J., 69, 195, 10.1136/hrt.69.3.195 · DOI
  37. Braeken, 2020, Perinatal Resilience for the First 1,000 Days of Life. Concept Analysis and Delphi Survey, Front. Psychol., 11, 2993
  38. Selevan, 2000, Identifying Critical Windows of Exposure for Children’s Health, Environ. Health Perspect., 108, 451
  39. Victora, 2010, Worldwide Timing of Growth Faltering: Revisiting Implications for Interventions, Pediatrics, 125, e473, 10.1542/peds.2009-1519 · DOI
  40. Mandy, 2018, Developmental Origins of Health and Disease: The Relevance to Developing Nations, Int. Health, 10, 66, 10.1093/inthealth/ihy006 · DOI
  41. Barouki, 2018, Epigenetics as a Mechanism Linking Developmental Exposures to Long-Term Toxicity, Environ. Int., 114, 77, 10.1016/j.envint.2018.02.014 · DOI
  42. Grandjean, 2015, Life-Long Implications of Developmental Exposure to Environmental Stressors: New Perspectives, Endocrinology, 156, 3408, 10.1210/en.2015-1350 · DOI
  43. Prendergast, 2014, The Stunting Syndrome in Developing Countries, Paediatr. Int. Child Health, 34, 250, 10.1179/2046905514Y.0000000158 · DOI
  44. Hanson, 2014, Early Developmental Conditioning of Later Health and Disease: Physiology or Pathophysiology?, Physiol. Rev., 94, 1027, 10.1152/physrev.00029.2013 · DOI · Paper page
  45. Wyrwoll, 2012, Prenatal Excess Glucocorticoid Exposure and Adult Affective Disorders: A Role for Serotonergic and Catecholamine Pathways, Neuroendocrinology, 95, 47, 10.1159/000331345 · DOI
  46. Margueron, 2010, Chromatin Structure and the Inheritance of Epigenetic Information, Nat. Rev. Genet., 11, 285, 10.1038/nrg2752 · DOI
  47. Schaefer, 2015, The Genetics of Epigenetic Inheritance: Modes, Molecules, and Mechanisms, Q. Rev. Biol., 90, 381, 10.1086/683699 · DOI
  48. Rogers, 2019, Smoking and Pregnancy: Epigenetics and Developmental Origins of the Metabolic Syndrome, Birth Defects Res., 111, 1259, 10.1002/bdr2.1550 · DOI
  49. Rauschert, 2020, Machine Learning-Based DNA Methylation Score for Fetal Exposure to Maternal Smoking: Development and Validation in Samples Collected from Adolescents and Adults, Environ. Health Perspect., 128, 097003, 10.1289/EHP6076 · DOI
  50. Tolhoek, 2015, Prenatal Parental Tobacco Smoking, Gene Specific DNA Methylation, and Newborns Size: The Generation R Study, Clin. Epigenet., 7, 1
  51. Breton, 2009, Prenatal Tobacco Smoke Exposure Affects Global and Gene-Specific DNA Methylation, Am. J. Respir. Crit. Care Med., 180, 462, 10.1164/rccm.200901-0135OC · DOI
  52. Cardenas, 2019, Mediation by Placental DNA Methylation of the Association of Prenatal Maternal Smoking and Birth Weight, Am. J. Epidemiol., 188, 1878, 10.1093/aje/kwz184 · DOI
  53. Everson, 2019, Placental Methylation Signatures from Maternal Smoking during Pregnancy and Potential Impacts on Fetal Growth: Meta-Analyses from 7 Cohorts, Environ. Epidemiol., 3, 115, 10.1097/01.EE9.0000606984.20424.8e · DOI
  54. Fa, 2016, Assessment of Global DNA Methylation in the First Trimester Fetal Tissues Exposed to Maternal Cigarette Smoking, Clin. Epigenet., 8, 1, 10.1186/s13148-016-0296-0 · DOI
  55. Flom, 2011, Prenatal Smoke Exposure and Genomic DNA Methylation in a Multiethnic Birth Cohort, Cancer Epidemiol. Biomark. Prev., 20, 2518, 10.1158/1055-9965.EPI-11-0553 · DOI
  56. Hannon, 2019, Variable DNA Methylation in Neonates Mediates the Association between Prenatal Smoking and Birth Weight, Philos. Trans. R. Soc. B, 374, 20180120, 10.1098/rstb.2018.0120 · DOI
  57. Herberth, 2014, Maternal and Cord Blood MiR-223 Expression Associates with Prenatal Tobacco Smoke Exposure and Low Regulatory T-Cell Numbers, J. Allergy Clin. Immunol., 133, 543, 10.1016/j.jaci.2013.06.036 · DOI
  58. Ivorra, 2015, DNA Methylation Patterns in Newborns Exposed to Tobacco in Utero, J. Transl. Med., 13, 1, 10.1186/s12967-015-0384-5 · DOI
  59. Jamieson, 2020, Smoking, DNA Methylation, and Lung Function: A Mendelian Randomization Analysis to Investigate Causal Pathways, Am. J. Hum. Genet., 106, 315, 10.1016/j.ajhg.2020.01.015 · DOI
  60. Janssen, 2017, Placental Mitochondrial DNA and CYP1A1 Gene Methylation as Molecular Signatures for Tobacco Smoke Exposure in Pregnant Women and the Relevance for Birth Weight, J. Transl. Med., 15, 1, 10.1186/s12967-016-1113-4 · DOI
  61. Joubert, 2012, 450K Epigenome-Wide Scan Identifies Differential DNA Methylation in Newborns Related to Maternal Smoking during Pregnancy, Environ. Health Perspect., 120, 1425, 10.1289/ehp.1205412 · DOI · Paper page
  62. Joubert, 2014, Maternal Smoking and DNA Methylation in Newborns: In Utero Effect or Epigenetic Inheritance?, Cancer Epidemiol. Biomark. Prev., 23, 1007, 10.1158/1055-9965.EPI-13-1256 · DOI
  63. Joubert, 2016, DNA Methylation in Newborns and Maternal Smoking in Pregnancy: Genome-Wide Consortium Meta-Analysis, AJHG, 98, 680, 10.1016/j.ajhg.2016.02.019 · DOI · Paper page
  64. Kheirkhah Rahimabad, P., Anthony, T.M., Jones, A.D., Eslamimehr, S., Mukherjee, N., Ewart, S., Holloway, J.W., Arshad, H., Commodore, S., and Karmaus, W. (2020). Nicotine and Its Downstream Metabolites in Maternal and Cord Sera: Biomarkers of Prenatal Smoking Exposure Associated with Offspring DNA Methylation. IJERPH, 17. · DOI
  65. Xu, 2015, DNA Methylation Mediates the Effect of Maternal Smoking during Pregnancy on Birthweight of the Offspring, Int. J. Epidemiol., 44, 1224, 10.1093/ije/dyv048 · DOI
  66. Shu, 2016, Presence of an Epigenetic Signature of Prenatal Cigarette Smoke Exposure in Childhood, Environ. Res., 144, 139, 10.1016/j.envres.2015.11.014 · DOI
  67. Lkhagvadorj, 2020, Prenatal Smoke Exposure Induces Persistent Cyp2a5 Methylation and Increases Nicotine Metabolism in the Liver of Neonatal and Adult Male Offspring, Epigenetics, 15, 1370, 10.1080/15592294.2020.1782655 · DOI
  68. Maccani, 2010, Maternal Cigarette Smoking during Pregnancy Is Associated with Downregulation of MiR-16, MiR-21, and MiR-146a in the Placenta, Epigenetics, 5, 583, 10.4161/epi.5.7.12762 · DOI · Paper page
  69. Markunas, 2014, Identification of DNA Methylation Changes in Newborns Related to Maternal Smoking during Pregnancy, Environ. Health Perspect., 122, 1147, 10.1289/ehp.1307892 · DOI
  70. Miyake, 2018, Association between DNA Methylation in Cord Blood and Maternal Smoking: The Hokkaido Study on Environment and Children’s Health, Sci. Rep., 8, 1, 10.1038/s41598-018-23772-x · DOI
  71. Monasso, 2020, Timing-and Dose-Specific Associations of Prenatal Smoke Exposure with Newborn DNA Methylation, Nicotine Tob. Res., 22, 1917, 10.1093/ntr/ntaa069 · DOI
  72. Morales, 2016, Genome-Wide DNA Methylation Study in Human Placenta Identifies Novel Loci Associated with Maternal Smoking during Pregnancy, Int. J. Epidemiol., 45, 1644, 10.1093/ije/dyw196 · DOI
  73. Murphy, 2012, Gender-Specific Methylation Differences in Relation to Prenatal Exposure to Cigarette Smoke, Gene, 494, 36, 10.1016/j.gene.2011.11.062 · DOI
  74. Nielsen, 2016, DNA Methylation Alterations in Response to Prenatal Exposure of Maternal Cigarette Smoking: A Persistent Epigenetic Impact on Health from Maternal Lifestyle?, Arch. Toxicol., 90, 231, 10.1007/s00204-014-1426-0 · DOI
  75. Cirera, 2018, The Impact of Prenatal Insults on the Human Placental Epigenome: A Systematic Review, Neurotoxicol. Teratol., 66, 80, 10.1016/j.ntt.2018.01.001 · DOI
  76. Patil, 2013, Interaction of Prenatal Maternal Smoking, Interleukin 13 Genetic Variants and DNA Methylation Influencing Airflow and Airway Reactivity, Clin. Epigenet., 5, 1, 10.1186/1868-7083-5-22 · DOI
  77. Reese, 2017, DNA Methylation Score as a Biomarker in Newborns for Sustained Maternal Smoking during Pregnancy, Environ. Health Perspect., 125, 760, 10.1289/EHP333 · DOI
  78. Richmond, 2015, Exploring Possible Epigenetic Mediation of Early-Life Environmental Exposures on Adiposity and Obesity Development, Int. J. Epidemiol., 44, 1191, 10.1093/ije/dyv066 · DOI
  79. Richmond, 2018, DNA Methylation as a Marker for Prenatal Smoke Exposure in Adults, Int. J. Epidemiol., 47, 1120, 10.1093/ije/dyy091 · DOI
  80. Richmond, 2017, Contrasting the Effects of Intra-Uterine Smoking and One-Carbon Micronutrient Exposures on Offspring DNA Methylation, Epigenomics, 9, 351, 10.2217/epi-2016-0135 · DOI
  81. Rousseaux, 2020, Immediate and Durable Effects of Maternal Tobacco Consumption Alter Placental DNA Methylation in Enhancer and Imprinted Gene-Containing Regions, BMC Med., 18, 1, 10.1186/s12916-020-01736-1 · DOI
  82. Rzehak, P., Saffery, R., Reischl, E., Covic, M., Wahl, S., Grote, V., Xhonneux, A., Langhendries, J.-P., Ferre, N., and Closa-Monasterolo, R. (2016). Maternal Smoking during Pregnancy and DNA-Methylation in Children at Age 5.5 Years: Epigenome-Wide-Analysis in the European Childhood Obesity Project (CHOP)-Study. PLoS ONE, 11. · DOI
  83. Shorey-Kendrick, L., McEvoy, C., Tepper, R., Park, B., Gao, L., Milner, K., Morris, C., and Spindel, E. (2020). Epigenome-Wide Analysis of Placental DNA Methylation Associated with Objective Measures of Maternal Smoking. A29. Destroying the Lung with a Puff, American Thoracic Society. · DOI
  84. McEvoy, 2017, Vitamin C Prevents Offspring DNA Methylation Changes Associated with Maternal Smoking in Pregnancy, Am. J. Respir. Crit. Care Med., 196, 745, 10.1164/rccm.201610-2141OC · DOI
  85. Lotfipour, 2010, Maternal Smoking during Pregnancy Is Associated with Epigenetic Modifications of the Brain-derived Neurotrophic Factor-6 Exon in Adolescent Offspring, Am. J. Med. Genet., 153, 1350
  86. Binder, 2017, Locus-Specific DNA Methylation in the Placenta Is Associated with Levels of pro-Inflammatory Proteins in Cord Blood and They Are Both Independently Affected by Maternal Smoking during Pregnancy, Epigenetics, 12, 875, 10.1080/15592294.2017.1361592 · DOI
  87. Maitre, 2020, In Utero and Childhood Exposure to Tobacco Smoke and Multi-Layer Molecular Signatures in Children, BMC Med., 18, 1
  88. Knopik, 2019, Prenatal Substance Exposure and Offspring Development: Does DNA Methylation Play a Role?, Neurotoxicol. Teratol., 71, 50, 10.1016/j.ntt.2018.01.009 · DOI
  89. Suter, 2020, The Impact of Tobacco Chemicals and Nicotine on Placental Development, Prent. Diagn., 40, 1193, 10.1002/pd.5660 · DOI · Paper page
  90. Fragou, 2019, Smoking and DNA Methylation: Correlation of Methylation with Smoking Behavior and Association with Diseases and Fetus Development Following Prenatal Exposure, Food Chem. Toxicol., 129, 312, 10.1016/j.fct.2019.04.059 · DOI
  91. Kaur, 2019, A Systematic Review of Smoking-Related Epigenetic Alterations, Arch. Toxicol., 93, 2715, 10.1007/s00204-019-02562-y · DOI
  92. Silva, 2021, Cigarette Smoke-Induced Alterations in Blood: A Review of Research on DNA Methylation and Gene Expression, Exp. Clin. Psychopharmacol., 29, 116, 10.1037/pha0000382 · DOI
  93. Moore, 2013, DNA Methylation and Its Basic Function, Neuropsychopharmacology, 38, 23, 10.1038/npp.2012.112 · DOI · Paper page
  94. Dolinoy, 2007, Epigenetic Gene Regulation: Linking Early Developmental Environment to Adult Disease, Reprod. Toxicol., 23, 297, 10.1016/j.reprotox.2006.08.012 · DOI
  95. Jones, 1980, Cellular Differentiation, Cytidine Analogs and DNA Methylation, Cell, 20, 85, 10.1016/0092-8674(80)90237-8 · DOI · Paper page
  96. Phillips, 2008, The Role of Methylation in Gene Expression, Nat. Edu., 1, 116
  97. Collas, 2007, Programming the Genome in Embryonic and Somatic Stem Cells, JCMM, 11, 602
  98. Weber, 2007, Genomic Patterns of DNA Methylation: Targets and Function of an Epigenetic Mark, COCEBI, 19, 273
  99. 2018, Environmental Epigenetic Changes, as Risk Factors for the Development of Diseases in Children: A Systematic Review, Ann. Glob. Health, 84, 212, 10.29024/aogh.909 · DOI
  100. Vlahos, A., Mansell, T., Saffery, R., and Novakovic, B. (2019). Human Placental Methylome in the Interplay of Adverse Placental Health, Environmental Exposure, and Pregnancy Outcome. PLoS Genet., 15. · DOI
  101. Abraham, 2018, Pregnancy Exposure to Atmospheric Pollution and Meteorological Conditions and Placental DNA Methylation, Environ. Int., 118, 334, 10.1016/j.envint.2018.05.007 · DOI
  102. Reik, 2001, Epigenetic Reprogramming in Mammalian Development, Science, 293, 1089, 10.1126/science.1063443 · DOI · Paper page
  103. Suter, 2012, Maternal Smoking as a Model for Environmental Epigenetic Changes Affecting Birthweight and Fetal Programming, MHR, 19, 1
  104. Goldman, 2010, Global DNA Hypomethylation Is Associated with in Utero Exposure to Cotinine and Perfluorinated Alkyl Compounds, Epigenetics, 5, 539, 10.4161/epi.5.6.12378 · DOI
  105. Witt, 2018, Impact on Birth Weight of Maternal Smoking throughout Pregnancy Mediated by DNA Methylation, BMC Genom., 19, 1, 10.1186/s12864-018-4652-7 · DOI
  106. Appleton, A.A., Armstrong, D.A., Lesseur, C., Lee, J., Padbury, J.F., Lester, B.M., and Marsit, C.J. (2013). Patterning in Placental 11-B Hydroxysteroid Dehydrogenase Methylation According to Prenatal Socioeconomic Adversity. PLoS ONE, 8. · DOI
  107. Suter, 2010, In Utero Tobacco Exposure Epigenetically Modifies Placental CYP1A1 Expression, Metabolism, 59, 1481, 10.1016/j.metabol.2010.01.013 · DOI · Paper page
  108. Suter, 2011, Maternal Tobacco Use Modestly Alters Correlated Epigenome-Wide Placental DNA Methylation and Gene Expression, Epigenetics, 6, 1284, 10.4161/epi.6.11.17819 · DOI · Paper page
  109. Chatterton, 2017, In Utero Exposure to Maternal Smoking Is Associated with DNA Methylation Alterations and Reduced Neuronal Content in the Developing Fetal Brain, Epigenet. Chromatin, 10, 1, 10.1186/s13072-017-0111-y · DOI
  110. Bauer, 2016, Environment-induced Epigenetic Reprogramming in Genomic Regulatory Elements in Smoking Mothers and Their Children, Mol. Syst. Biol., 12, 861, 10.15252/msb.20156520 · DOI
  111. Maccani, 2009, Epigenetics in the Placenta, Am. J. Reprod. Immunol., 62, 78, 10.1111/j.1600-0897.2009.00716.x · DOI
  112. Maccani, 2012, Cigarette Smoke Exposure-Associated Alterations to Non-Coding RNA, Front. Genet., 3, 53, 10.3389/fgene.2012.00053 · DOI
  113. Wahid, 2010, MicroRNAs: Synthesis, Mechanism, Function, and Recent Clinical Trials, Biochim. Biophys. Acta Mol. Cell Res., 1803, 1231, 10.1016/j.bbamcr.2010.06.013 · DOI
  114. Sood, 2006, Gene Expression Patterns in Human Placenta, PNAS, 103, 5478, 10.1073/pnas.0508035103 · DOI · Paper page
  115. Vrijens, 2015, MicroRNAs as Potential Signatures of Environmental Exposure or Effect: A Systematic Review, Environ. Health Perspect., 123, 399, 10.1289/ehp.1408459 · DOI
  116. Buck, 2020, Developmental Nicotine Exposure Engenders Intergenerational Downregulation and Aberrant Posttranslational Modification of Cardinal Epigenetic Factors in the Frontal Cortices, Striata, and Hippocampi of Adolescent Mice, Epigenet. Chromatin, 13, 1, 10.1186/s13072-020-00332-0 · DOI
  117. Xie, 2018, Prenatal Nicotine Exposure Intergenerationally Programs Imperfect Articular Cartilage via Histone Deacetylation through Maternal Lineage, Toxicol. Appl. Pharmacol., 352, 107, 10.1016/j.taap.2018.03.018 · DOI
  118. Lim, A.S., Srivastava, G.P., Yu, L., Chibnik, L.B., Xu, J., Buchman, A.S., Schneider, J.A., Myers, A.J., Bennett, D.A., and De Jager, P.L. (2014). 24-Hour Rhythms of DNA Methylation and Their Relation with Rhythms of RNA Expression in the Human Dorsolateral Prefrontal Cortex. PLoS Genet., 10. · DOI
  119. Sikdar, 2019, Comparison of Smoking-Related DNA Methylation between Newborns from Prenatal Exposure and Adults from Personal Smoking, Epigenomics, 11, 1487, 10.2217/epi-2019-0066 · DOI
  120. Armstrong, 2014, Global and Gene-specific DNA Methylation across Multiple Tissues in Early Infancy: Implications for Children’s Health Research, FASEB J., 28, 2088, 10.1096/fj.13-238402 · DOI · Paper page
  121. Baccarelli, 2017, Epigenome-Wide Cross-Tissue Predictive Modeling and Comparison of Cord Blood and Placental Methylation in a Birth Cohort, Epigenomics, 9, 231, 10.2217/epi-2016-0109 · DOI
  122. Groleau, 2021, Comparative Epigenome-Wide Analysis Highlights Placenta-Specific Differentially Methylated Regions, Epigenomics, 13, 357, 10.2217/epi-2020-0271 · DOI
  123. Karttunen, 2010, Placental Transfer and DNA Binding of Benzo (a) Pyrene in Human Placental Perfusion, Toxicol. Lett., 197, 75, 10.1016/j.toxlet.2010.04.028 · DOI
  124. Heijmans, 2009, The Epigenome: Archive of the Prenatal Environment, Epigenetics, 4, 526, 10.4161/epi.4.8.10265 · DOI
  125. Champagne, 2012, Epigenetic and Neurodevelopmental Perspectives on Variation in Parenting Behavior, Parenting, 12, 202, 10.1080/15295192.2012.683358 · DOI
  126. Bonnin, 2011, Fetal, Maternal, and Placental Sources of Serotonin and New Implications for Developmental Programming of the Brain, Neuroscience, 197, 1, 10.1016/j.neuroscience.2011.10.005 · DOI · Paper page
  127. Yen, 1994, The Placenta as the Third Brain, J. Reprod. Med., 39, 277
  128. Houseman, 2016, Reference-Free Deconvolution of DNA Methylation Data and Mediation by Cell Composition Effects, BMC Bioinform., 17, 1, 10.1186/s12859-016-1140-4 · DOI
  129. Titus, 2017, Cell-Type Deconvolution from DNA Methylation: A Review of Recent Applications, Hum. Mol. Genet., 26, R216, 10.1093/hmg/ddx275 · DOI
  130. Bakulski, 2016, DNA Methylation of Cord Blood Cell Types: Applications for Mixed Cell Birth Studies, Epigenetics, 11, 354, 10.1080/15592294.2016.1161875 · DOI
  131. Yuan, 2019, Accurate Ethnicity Prediction from Placental DNA Methylation Data, Epigenet. Chromatin, 12, 1, 10.1186/s13072-019-0296-3 · DOI
  132. Scherer, M., Schmidt, F., Lazareva, O., Walter, J., Baumbach, J., Schulz, M.H., and List, M. (2021). Machine Learning for Deciphering Cell Heterogeneity and Gene Regulation. Nat. Comput. Sci. · DOI
  133. Holbrook, 2017, Is Cellular Heterogeneity Merely a Confounder to Be Removed from Epigenome-Wide Association Studies?, Epigenomics, 9, 1143, 10.2217/epi-2017-0032 · DOI
  134. Konwar, 2019, Association of a Placental Interleukin-6 Genetic Variant (Rs1800796) with DNA Methylation, Gene Expression and Risk of Acute Chorioamnionitis, BMC Med. Genet., 20, 1, 10.1186/s12881-019-0768-0 · DOI
  135. Caye, 2019, LFMM 2: Fast and Accurate Inference of Gene-Environment Associations in Genome-Wide Studies, Mol. Biol. Evol., 36, 852, 10.1093/molbev/msz008 · DOI
  136. Zhang, 2019, OSCA: A Tool for Omic-Data-Based Complex Trait Analysis, Genome Biol., 20, 1, 10.1186/s13059-019-1718-z · DOI
  137. Kanehisa, 2000, KEGG: Kyoto Encyclopedia of Genes and Genomes, Nucleic Acids Res., 28, 27, 10.1093/nar/28.1.27 · DOI · Paper page
  138. Dedeurwaerder, 2011, Evaluation of the Infinium Methylation 450K Technology, Epigenomics, 3, 771, 10.2217/epi.11.105 · DOI · Paper page
  139. Benjamini, 2001, Controlling the False Discovery Rate in Behavior Genetics Research, Behav. Brain Behav., 125, 279, 10.1016/S0166-4328(01)00297-2 · DOI · Paper page
  140. Benjamini, 1995, Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing, J. R. Stat. Soc. Ser. B Stat. Methodol., 57, 289, 10.1111/j.2517-6161.1995.tb02031.x · DOI · Paper page
  141. Storey, 2002, A Direct Approach to False Discovery Rates, J. R. Stat. Soc. Ser. B Stat. Methodol., 64, 479, 10.1111/1467-9868.00346 · DOI · Paper page
  142. Storey, 2003, Statistical Significance for Genomewide Studies, PNAS, 100, 9440, 10.1073/pnas.1530509100 · DOI · Paper page
  143. Paquette, 2015, Placental Epigenetic Patterning of Glucocorticoid Response Genes Is Associated with Infant Neurodevelopment, Epigenomics, 7, 767, 10.2217/epi.15.28 · DOI
  144. Teschendorff, 2018, Statistical and Integrative System-Level Analysis of DNA Methylation Data, Nat. Rev. Genet., 19, 129, 10.1038/nrg.2017.86 · DOI
  145. Robinson, 2014, Statistical Methods for Detecting Differentially Methylated Loci and Regions, Front. Genet., 5, 324, 10.3389/fgene.2014.00324 · DOI
  146. Pedersen, 2012, Comb-p: Software for Combining, Analyzing, Grouping and Correcting Spatially Correlated P-Values, Bioinformatics, 28, 2986, 10.1093/bioinformatics/bts545 · DOI · Paper page
  147. Mallik, 2019, An Evaluation of Supervised Methods for Identifying Differentially Methylated Regions in Illumina Methylation Arrays, Brief. Bioinform., 20, 2224, 10.1093/bib/bby085 · DOI
  148. Xu, 2020, IpDMR: Identification of Differentially Methylated Regions with Interval P-Values, Bioinformatics, 37, 711, 10.1093/bioinformatics/btaa732 · DOI
  149. Stroud, 2016, Epigenetic Regulation of Placental NR3C1: Mechanism Underlying Prenatal Programming of Infant Neurobehavior by Maternal Smoking?, Child Dev., 87, 49, 10.1111/cdev.12482 · DOI
  150. Blum, 2020, Challenges Raised by Mediation Analysis in a High-Dimension Setting, Environ. Health Perspect., 128, 055001, 10.1289/EHP6240 · DOI
  151. Jerolon, A., Baglietto, L., Birmeli, E., Alarcon, F., and Perduca, V. (2020). Causal Mediation Analysis in Presence of Multiple Mediators Uncausally Related. Int. J. Biostat., ahead-of-print. · DOI

Cited by

Sorted by citations

See all 72

Metadata

Authors
Nakamura, A., François, O., & Lepeule, J.
Affiliations
  • Université Grenoble Alpes, Inserm, CNRS, IAB, 38000 Grenoble, France
  • Université Grenoble Alpes, Laboratoire TIMC, CNRS UMR 5525, 38000 Grenoble, France
ORCID
Venue
International Journal of Environmental Research and Public Health
Publisher
MDPI AG
Published
2021-05-11
Volume
18
Issue
10
Pages
5083
ISSN
1660-4601
DOI
10.3390/ijerph18105083
PMC
PMC8151244
Cited by
72
References
20
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • INCa (INCa_13641)
  • French Agency for National Research (ANR-18-CE36-0005)
  • IRESP & INCa (IRESP-19-TABAC-V1-01)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Epigenetic Alterations of Maternal Tobacco Smoking during Pregnancy: A Narrative Review. https://app.cochat.ai/papers/10.3390/ijerph18105083
The paper
Nakamura, A., François, O., & Lepeule, J. (2021). Epigenetic Alterations of Maternal Tobacco Smoking during Pregnancy: A Narrative Review. International Journal of Environmental Research and Public Health. https://doi.org/10.3390/ijerph18105083