Smoking-Induced Changes in the Maternal Immune, Endocrine, and Metabolic Pathways and Their Impact on Fetal Growth: A Topical Review

Perinatal maternal smoking exposure (PMSE) is one of the major environmental risk factors encountered by the fetus. PMSE is usually associated with adverse pregnancy outcomes that may manifest at different stages of life. Nevertheless, fetal growth restriction is the most common smoking-induced side effect. PMSE induces changes in the maternal multiple organ systems. These alterations may affect placentation, which subsequently affects fetal growth. It is worthy to note, however, that the extent of maternal smoking-induced changes depends mainly on the maternal level of susceptibility. Hence, the perinatal pregnancy outcomes vary depending on the interaction between the triad: the maternal, fetal, and placental modifications, making it more complex. In this review, we try to unveil the effect of smoking-induced maternal changes on the maternal immune, endocrine, and metabolic pathways and their impact on fetal growth.

[1]  Jun Zhang,et al.  Maternal Smoking and Metabolic Health Biomarkers in Newborns , 2015, PloS one.

[2]  Qijun Wu,et al.  Cigarette smoking during pregnancy and preeclampsia risk: a systematic review and meta-analysis of prospective studies , 2015, Oncotarget.

[3]  J. Pollheimer,et al.  Function and control of human invasive trophoblast subtypes: Intrinsic vs. maternal control , 2015, Cell adhesion & migration.

[4]  Li-Tzy Wu,et al.  E-cigarette prevalence and correlates of use among adolescents versus adults: a review and comparison. , 2014, Journal of psychiatric research.

[5]  F. Barré-Sinoussi,et al.  Human decidual macrophages and NK cells differentially express Toll-like receptors and display distinct cytokine profiles upon TLR stimulation , 2014, Front. Microbiol..

[6]  E. Fernández,et al.  Impact of the Spanish Smoke-Free Legislation on Adult, Non-Smoker Exposure to Secondhand Smoke: Cross-Sectional Surveys before (2004) and after (2012) Legislation , 2014, PloS one.

[7]  K. Cummings,et al.  The 2014 Surgeon General's report: commemorating the 50th Anniversary of the 1964 Report of the Advisory Committee to the US Surgeon General and updating the evidence on the health consequences of cigarette smoking. , 2014, American journal of epidemiology.

[8]  F. Malone,et al.  Fetal growth restriction and the risk of perinatal mortality–case studies from the multicentre PORTO study , 2014, BMC Pregnancy and Childbirth.

[9]  E. Jassem,et al.  The many faces of tobacco use among women , 2014, Medical science monitor : international medical journal of experimental and clinical research.

[10]  YunQing Li,et al.  Potential Use of Hyperoxygenated Solution as a Treatment Strategy for Carbon Monoxide Poisoning , 2013, PloS one.

[11]  F. Louwen,et al.  Smoking and Pregnancy — A Review on the First Major Environmental Risk Factor of the Unborn , 2013, International journal of environmental research and public health.

[12]  A. Fayed,et al.  The effectiveness of breath carbon monoxide analyzer in screening for environmental tobacco smoke exposure in Saudi pregnant women , 2013, Annals of thoracic medicine.

[13]  T. Paus,et al.  Maternal Smoking during Pregnancy and Fetal Organ Growth: A Magnetic Resonance Imaging Study , 2013, PloS one.

[14]  A. Golan,et al.  The placental factor in early- and late-onset normotensive fetal growth restriction. , 2013, Placenta.

[15]  B. Perry,et al.  The Moderating Effects of Skin Color and Ethnic Identity Affirmation on Suicide Risk among Low-SES African American Women , 2013, Race and social problems.

[16]  C. Domínguez,et al.  Smoking during Pregnancy: Changes in Mid-Gestation Angiogenic Factors in Women at Risk of Developing Preeclampsia According to Uterine Artery Doppler Findings , 2013, Hypertension in pregnancy.

[17]  S. Hawes,et al.  Association of Maternal Smoking During Pregnancy With Infant Hospitalization and Mortality Due to Infectious Diseases , 2013, The Pediatric infectious disease journal.

[18]  E. Levin,et al.  Evaluation of the Association between Maternal Smoking, Childhood Obesity, and Metabolic Disorders: A National Toxicology Program Workshop Review , 2012, Environmental health perspectives.

[19]  Lubo Zhang,et al.  Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: Mechanisms and possible interventions , 2012, Progress in Neurobiology.

[20]  A. Tripathi,et al.  Physiological Changes in Hematological Parameters During Pregnancy , 2012, Indian Journal of Hematology and Blood Transfusion.

[21]  M. Faas,et al.  Smoking during pregnancy influences the maternal immune response in mice and humans. , 2012, American journal of obstetrics and gynecology.

[22]  D. Prabhakaran,et al.  Pathophysiological Mechanisms of Tobacco-Related CVD. , 2012, Global heart.

[23]  E. Saltó,et al.  Assessment of prenatal exposure to tobacco smoke by cotinine in cord blood for the evaluation of smoking control policies in Spain , 2012, BMC Pregnancy and Childbirth.

[24]  K. Khunti,et al.  Birthweight Centile Charts for South Asian Infants Born in the UK , 2011, Neonatology.

[25]  A. Hackshaw,et al.  Maternal smoking in pregnancy and birth defects: a systematic review based on 173 687 malformed cases and 11.7 million controls , 2011, Human reproduction update.

[26]  Guisera Lee,et al.  Perinatal outcomes and maternal clinical characteristics in IUGR with absent or reversed end-diastolic flow velocity in the umbilical artery , 2011, Archives of Gynecology and Obstetrics.

[27]  A. Baschat,et al.  Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction , 2011, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[28]  A. Hofman,et al.  Maternal smoking during pregnancy, fetal arterial resistance adaptations and cardiovascular function in childhood , 2011, BJOG : an international journal of obstetrics and gynaecology.

[29]  Francesc Figueras,et al.  Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. , 2011, American Journal of Obstetrics and Gynecology.

[30]  V. Zanardo,et al.  Consequences in Infants That Were Intrauterine Growth Restricted , 2011, Journal of pregnancy.

[31]  S. Dube,et al.  Estimates of nondisclosure of cigarette smoking among pregnant and nonpregnant women of reproductive age in the United States. , 2011, American journal of epidemiology.

[32]  S. Wen,et al.  The risk of adverse pregnancy outcomes is increased in preeclamptic women who smoke compared with nonpreeclamptic women who do not smoke. , 2010, American Journal of Obstetrics and Gynecology.

[33]  C. Power,et al.  Maternal smoking in pregnancy, adult adiposity and other risk factors for cardiovascular disease. , 2010, Atherosclerosis.

[34]  T. Shima,et al.  REVIEW ARTICLE: Th1/Th2/Th17 and Regulatory T‐Cell Paradigm in Pregnancy , 2010, American journal of reproductive immunology.

[35]  I. Berlin,et al.  Newborns' cord blood plasma cotinine concentrations are similar to that of their delivering smoking mothers. , 2010, Drug and alcohol dependence.

[36]  M. Vahter,et al.  Accumulation of cadmium in human placenta interacts with the transport of micronutrients to the fetus. , 2010, Toxicology letters.

[37]  V. Knopik.  Maternal Smoking During Pregnancy and Child Outcomes: Real or Spurious Effect? , 2009, Developmental neuropsychology.

[38]  D. Grobbee,et al.  Parental Smoking and Vascular Damage in Young Adult Offspring: Is Early Life Exposure Critical?: The Atherosclerosis Risk in Young Adults Study , 2008, Arteriosclerosis, thrombosis, and vascular biology.

[39]  R. Ness,et al.  Cigarette smoke exposure and angiogenic factors in pregnancy and preeclampsia. , 2008, American journal of hypertension.

[40]  J. Bannigan,et al.  Cadmium: toxic effects on the reproductive system and the embryo. , 2008, Reproductive toxicology.

[41]  M. Stämpfli,et al.  Impairment of human NK cell cytotoxic activity and cytokine release by cigarette smoke , 2008, Journal of leukocyte biology.

[42]  A. Hofman,et al.  Active and passive maternal smoking during pregnancy and the risks of low birthweight and preterm birth: the Generation R Study. , 2008, Paediatric and perinatal epidemiology.

[43]  G. Shaw,et al.  Craniosynostosis and maternal smoking. , 2008, Birth defects research. Part A, Clinical and molecular teratology.

[44]  Andrew J Thorley,et al.  Pulmonary epithelium, cigarette smoke, and chronic obstructive pulmonary disease , 2007, International journal of chronic obstructive pulmonary disease.

[45]  H. Salihu,et al.  Epidemiology of prenatal smoking and perinatal outcomes. , 2007, Early human development.

[46]  R. Wickström.  Effects of Nicotine During Pregnancy: Human and Experimental Evidence , 2007, Current neuropharmacology.

[47]  G. Smith,et al.  Similar Associations of Parental Prenatal Smoking Suggest Child Blood Pressure Is Not Influenced by Intrauterine Effects , 2007, Hypertension.

[48]  J. Deloia,et al.  The effects of cigarette smoking on circulating maternal leukocytes during pregnancy. , 2007, Clinical immunology.

[49]  Kelley R. Peach,et al.  Smoking during Pregnancy Affects Speech-Processing Ability in Newborn Infants , 2006, Environmental health perspectives.

[50]  S. Cnattingius,et al.  Environmental Tobacco Smoke and Risk of Spontaneous Abortion , 2006, Epidemiology.

[51]  Gail M. Williams,et al.  Does maternal smoking during pregnancy have a direct effect on future offspring obesity? Evidence from a prospective birth cohort study. , 2006, American journal of epidemiology.

[52]  G. Badger,et al.  Maternal Smoking and Its Association With Birth Weight , 2005, Obstetrics and gynecology.

[53]  R. Kirby,et al.  Smoking‐associated fetal morbidity among older gravidas: a population study , 2005, Acta obstetricia et gynecologica Scandinavica.

[54]  James Pirkle,et al.  Environmental Tobacco Smoke and Pregnancy Outcome , 2004, Epidemiology.

[55]  Gail M. Williams,et al.  Associations of Parental, Birth, and Early Life Characteristics With Systolic Blood Pressure at 5 Years of Age: Findings From the Mater-University Study of Pregnancy and Its Outcomes , 2004, Circulation.

[56]  R. Hornung,et al.  Exposure to Environmental Tobacco Smoke and Cognitive Abilities among U.S. Children and Adolescents , 2004, Environmental health perspectives.

[57]  Sven Cnattingius,et al.  The epidemiology of smoking during pregnancy: smoking prevalence, maternal characteristics, and pregnancy outcomes. , 2004, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[58]  C. Loffredo,et al.  Population-based study of l-transposition of the great arteries: possible associations with environmental factors. , 2003, Birth defects research. Part A, Clinical and molecular teratology.

[59]  I. Athanassakis,et al.  Interplay between T helper type 1 and type 2 cytokines and soluble major histocompatibility complex molecules: a paradigm in pregnancy , 2002, Immunology.

[60]  A. Hatagima.  Genetic polymorphisms and metabolism of endocrine disruptors in cancer susceptibility. , 2002, Cadernos de saude publica.

[61]  P. Zielinsky,et al.  Acute effects of maternal smoking on fetal-placental-maternal system hemodynamics. , 2002, Arquivos brasileiros de cardiologia.

[62]  K. Kostial,et al.  Placental cadmium and progesterone concentrations in cigarette smokers. , 2001, Reproductive toxicology.

[63]  J. Kendrick,et al.  Effects of smoking reduction during pregnancy on the birth weight of term infants. , 2001, American journal of epidemiology.

[64]  D. Sahota,et al.  Computerized analysis of acute and chronic changes in fetal heart rate variation and fetal activity in association with maternal smoking. , 2001, American journal of obstetrics and gynecology.

[65]  I. Blumenthal.  Carbon Monoxide Poisoning , 2001, Journal of the Royal Society of Medicine.

[66]  S. Fisher,et al.  Concordant in situ and in vitro data show that maternal cigarette smoking negatively regulates placental cytotrophoblast passage through the cell cycle. , 2000, Reproductive toxicology.

[67]  S. Kirkland,et al.  The natural history of smoking during pregnancy among women in Nova Scotia. , 2000, CMAJ : Canadian Medical Association journal = journal de l'Association medicale canadienne.

[68]  R L Andres,et al.  Perinatal complications associated with maternal tobacco use. , 2000, Seminars in neonatology : SN.

[69]  V. Baste,et al.  Maternal smoking and birthweight: effect modification of period, maternal age and paternal smoking , 2000, Acta obstetricia et gynecologica Scandinavica.

[70]  G Koren,et al.  Maternal cocaine use and cigarette smoking in pregnancy in relation to amino acid transport and fetal growth. , 1999, Placenta.

[71]  N. Fisk,et al.  Association between maternal anxiety in pregnancy and increased uterine artery resistance index: cohort based study. , 1999, BMJ.

[72]  G. Koren,et al.  Transplacental transfer and biotransformation studies of nicotine in the human placental cotyledon perfused in vitro. , 1998, Life sciences.

[73]  S. Cnattingius,et al.  Decreasing smoking prevalence during pregnancy in Sweden: the effect on small-for-gestational-age births. , 1997, American journal of public health.

[74]  G. Monica,et al.  Placenta previa, maternal smoking and recurrence risk , 1995, Acta obstetricia et gynecologica Scandinavica.

[75]  K. Stoschitzky,et al.  Diminished Vascular Response to Inhibition of Endothelium‐Derived Nitric Oxide and Enhanced Vasoconstriction to Exogenously Administered Endothelin‐1 in Clinically Healthy Smokers , 1994, Circulation.

[76]  K. Schoendorf,et al.  Relationship of sudden infant death syndrome to maternal smoking during and after pregnancy. , 1992, Pediatrics.

[77]  K J Dalton,et al.  Morphometric differences between the placental vasculature of non‐smokers, smokers and ex‐smokers , 1989, British journal of obstetrics and gynaecology.

[78]  M. Pike,et al.  Cigarette smoking in pregnancy results in marked decrease in maternal hCG and oestradiol levels , 1989, British journal of obstetrics and gynaecology.

[79]  B. R. Kuhnert,et al.  The effect of smoking on placental and fetal zinc status. , 1987, American journal of obstetrics and gynecology.

[80]  J. Wladimiroff,et al.  Acute effect of maternal smoking on the maternal and fetal cardiovascular system. , 1984, Early human development.

[81]  S KAYE,et al.  Carbon monoxide poisoning. , 1957, Virginia medical monthly.

[82]  M. Broce,et al.  Smoking in Pregnancy in West Virginia: Does Cessation/Reduction Improve Perinatal Outcomes? , 2010, Maternal and Child Health Journal.

[83]  G. Decavalas,et al.  Effect of maternal smoking on cord blood estriol, placental lactogen, chorionic gonadotropin, FSH, LH, and cortisol , 2009, Journal of perinatal medicine.

[84]  A. Hofman,et al.  Maternal smoking in pregnancy is associated with cholesterol development in the offspring: A 27-years follow-up study. , 2008, Atherosclerosis.

[85]  N. Benowitz,et al.  Cotinine as a biomarker of environmental tobacco smoke exposure. , 1996, Epidemiologic reviews.

[86]  H Nau,et al.  Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. , 1985, Developmental pharmacology and therapeutics.

[87]  F. Battaglia.  Intrauterine growth. , 1969, The Journal of pediatrics.