Oxidative Stress-Mediated Aging during the Fetal and Perinatal Periods

Oxidative stress is worldwide recognized as a fundamental component of the aging, a process that begins before birth. There is a critical balance between free radical generation and antioxidant defenses. Oxidative stress is caused by an imbalance between the production of free radicals and the ability of antioxidant system to detoxify them. Oxidative stress can occur early in pregnancy and continue in the postnatal period; this damage is implicated in the pathophysiology of pregnancy-related disorders, including recurrent pregnancy loss, preeclampsia and preterm premature rupture of membranes. Moreover, diseases of the neonatal period such as bronchopulmonary dysplasia, retinopathy of prematurity, necrotizing enterocolitis, and periventricular leukomalacia are related to free radical damage. The specific contribution of oxidative stress to the pathogenesis and progression of these neonatal diseases is only partially understood. This review summarizes what is known about the role of oxidative stress in pregnancy and in the pathogenesis of common disorders of the newborn, as a component of the early aging process.

[1]  A. Gilman‐Sachs,et al.  Immunological Modes of Pregnancy Loss: Inflammation, Immune Effectors, and Stress , 2014, American journal of reproductive immunology.

[2]  S. Berger,et al.  Epigenetics of aging and aging-related disease. , 2014, The journals of gerontology. Series A, Biological sciences and medical sciences.

[3]  G. Werstuck,et al.  Oxidative Stress and Aging Diseases , 2014, Oxidative medicine and cellular longevity.

[4]  R. Reiter,et al.  Melatonin and stable circadian rhythms optimize maternal, placental and fetal physiology. , 2014, Human reproduction update.

[5]  R. Uauy,et al.  Endothelial heterogeneity in the umbilico-placental unit: DNA methylation as an innuendo of epigenetic diversity , 2014, Front. Pharmacol..

[6]  K. Karki,et al.  Association of oxidative DNA damage, protein oxidation and antioxidant function with oxidative stress induced cellular injury in pre-eclamptic/eclamptic mothers during fetal circulation. , 2014, Chemico-biological interactions.

[7]  R. Reiter,et al.  Melatonin: The watchdog of villous trophoblast homeostasis against hypoxia/reoxygenation-induced oxidative stress and apoptosis , 2013, Molecular and Cellular Endocrinology.

[8]  R. Reiter,et al.  Protective Role of Melatonin in Neonatal Diseases , 2013, Oxidative medicine and cellular longevity.

[9]  J. Perry,et al.  Development of the Preterm Gut Microbiome in Twins at Risk of Necrotising Enterocolitis and Sepsis , 2013, PloS one.

[10]  Á. Tósaki,et al.  Management of multicellular senescence and oxidative stress , 2013, Journal of cellular and molecular medicine.

[11]  R. Reiter,et al.  On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK , 2013, Journal of pineal research.

[12]  Kazushi Watanabe,et al.  The severity of hypoxic changes and oxidative DNA damage in the placenta of early-onset preeclamptic women and fetal growth restriction , 2013, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[13]  D. Walker,et al.  Mechanisms of Melatonin-Induced Protection in the Brain of Late Gestation Fetal Sheep in Response to Hypoxia , 2013, Developmental Neuroscience.

[14]  C. Vaillancourt,et al.  Placental melatonin production and melatonin receptor expression are altered in preeclampsia: new insights into the role of this hormone in pregnancy , 2012, Journal of pineal research.

[15]  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.

[16]  Y. Hayashi,et al.  Prophylactic administration of melatonin to the mother throughout pregnancy can protect against oxidative cerebral damage in neonatal rats , 2012, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[17]  A. Starkov,et al.  Hypoxic-Ischemic Injury in the Developing Brain: The Role of Reactive Oxygen Species Originating in Mitochondria , 2012, Neurology research international.

[18]  L. Fuentes-Broto,et al.  Alzheimer’s disease: pathological mechanisms and the beneficial role of melatonin , 2012, Journal of pineal research.

[19]  M. Benders,et al.  May oxidative stress biomarkers in cord blood predict the occurrence of necrotizing enterocolitis in preterm infants? , 2012, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[20]  E. Camm,et al.  Developmental Programming of Cardiovascular Dysfunction by Prenatal Hypoxia and Oxidative Stress , 2012, PloS one.

[21]  R. Reiter,et al.  Potential utility of melatonin as an antioxidant during pregnancy and in the perinatal period , 2012, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[22]  M. Hanson,et al.  Review: Placenta, evolution and lifelong health. , 2012, Placenta.

[23]  S. Dey,et al.  Sensing senescence in preterm birth , 2012, Cell cycle.

[24]  R. Reiter,et al.  Melatonin: The smart killer The human trophoblast as a model , 2012, Molecular and Cellular Endocrinology.

[25]  S. Dey,et al.  Heightened uterine mammalian target of rapamycin complex 1 (mTORC1) signaling provokes preterm birth in mice , 2011, Proceedings of the National Academy of Sciences.

[26]  R. Romero,et al.  Supplementation with vitamins C and E during pregnancy for the prevention of preeclampsia and other adverse maternal and perinatal outcomes: a systematic review and metaanalysis. , 2011, American journal of obstetrics and gynecology.

[27]  Kazushi Watanabe,et al.  Placental oxidative DNA damage and its repair in preeclamptic women with fetal growth restriction. , 2011, Placenta.

[28]  J. Davis,et al.  Future applications of antioxidants in premature infants , 2011, Current opinion in pediatrics.

[29]  M. Fraga,et al.  Aging genetics and aging. , 2011, Aging and disease.

[30]  Manisha N. Patel,et al.  Mitochondrial dysfunction and oxidative stress: a contributing link to acquired epilepsy? , 2010, Journal of bioenergetics and biomembranes.

[31]  Vinay M Nadkarni,et al.  Part 14: Pediatric Advanced Life Support , 2010 .

[32]  M. Hazinski,et al.  Part 15: neonatal resuscitation: 2010 American Heart Association Guidelines for Cardiopulmonary Resuscitation and Emergency Cardiovascular Care. , 2010, Circulation.

[33]  R. Neumar,et al.  Part 9: post-cardiac arrest care: 2010 American Heart Association Guidelines for Cardiopulmonary Resuscitation and Emergency Cardiovascular Care. , 2010, Circulation.

[34]  G. Buonocore,et al.  AO-26. Predictive power of oxidative stress markers for the early identification of newborns at high risk for free radicals related diseases , 2010 .

[35]  Z. Ungvari,et al.  Effect of hyperoxic resuscitation on propensity of germinal matrix haemorrhage and cerebral injury , 2010, Neuropathology and applied neurobiology.

[36]  M. Schluchter,et al.  A higher incidence of intermittent hypoxemic episodes is associated with severe retinopathy of prematurity. , 2010, The Journal of pediatrics.

[37]  M. Ristow,et al.  How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis) , 2010, Experimental Gerontology.

[38]  Zhangsheng Yu,et al.  Growth of lung parenchyma in infants and toddlers with chronic lung disease of infancy. , 2010, American journal of respiratory and critical care medicine.

[39]  E. Sokołowska,et al.  Melatonin enhances antioxidant action of α‐tocopherol and ascorbate against NADPH‐ and iron‐dependent lipid peroxidation in human placental mitochondria , 2010, Journal of pineal research.

[40]  G. Buonocore,et al.  Early identification of the risk for free radical-related diseases in preterm newborns. , 2010, Early human development.

[41]  Y. Hayashi,et al.  Therapeutic Effects of Maternal Melatonin Administration on Ischemia/Reperfusion-Induced Oxidative Cerebral Damage in Neonatal Rats , 2009, Neonatology.

[42]  R. Reiter,et al.  Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin , 2009, Critical reviews in biochemistry and molecular biology.

[43]  Lydia W. S. Finley,et al.  The coordination of nuclear and mitochondrial communication during aging and calorie restriction , 2009, Ageing Research Reviews.

[44]  G. Buonocore,et al.  Biomarkers of oxidative stress in babies at high risk for retinopathy of prematurity. , 2009, Frontiers in bioscience.

[45]  Michael Stumvoll,et al.  Antioxidants prevent health-promoting effects of physical exercise in humans , 2009, Proceedings of the National Academy of Sciences.

[46]  Marcus H. Jones,et al.  Growth of the lung parenchyma early in life. , 2009, American journal of respiratory and critical care medicine.

[47]  L. Ment,et al.  The diagnosis, management, and postnatal prevention of intraventricular hemorrhage in the preterm neonate. , 2008, Clinics in perinatology.

[48]  Y. Hayashi,et al.  Melatonin preserves fetal growth in rats by protecting against ischemia/reperfusion‐induced oxidative/nitrosative mitochondrial damage in the placenta , 2008, Journal of pineal research.

[49]  H. Modanlou,et al.  Effects of Brief, Clustered Versus Dispersed Hypoxic Episodes on Systemic and Ocular Growth Factors in a Rat Model of Oxygen-Induced Retinopathy , 2008, Pediatric Research.

[50]  R. Menon Spontaneous preterm birth, a clinical dilemma: Etiologic, pathophysiologic and genetic heterogeneities and racial disparity , 2008, Acta obstetricia et gynecologica Scandinavica.

[51]  P. Raspor,et al.  The antioxidant and pro‐oxidant activity of vitamin C and trolox in vitro: a comparative study , 2008, Journal of applied toxicology : JAT.

[52]  C. Vaillancourt,et al.  Human placental trophoblasts synthesize melatonin and express its receptors , 2008, Journal of pineal research.

[53]  G. Fan,et al.  The many roles of chemokine receptors in neurodegenerative disorders: emerging new therapeutical strategies. , 2007, Current medicinal chemistry.

[54]  Edward J Calabrese,et al.  Biological stress response terminology: Integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework. , 2007, Toxicology and applied pharmacology.

[55]  D. Kiel,et al.  Inflammatory markers and the risk of Alzheimer disease , 2007, Neurology.

[56]  D. Charnock-Jones,et al.  Nuclear factor-kappa B, p38, and stress-activated protein kinase mitogen-activated protein kinase signaling pathways regulate proinflammatory cytokines and apoptosis in human placental explants in response to oxidative stress: effects of antioxidant vitamins. , 2007, The American journal of pathology.

[57]  B. Koletzko,et al.  Oxidative stress and antioxidant protection in the perinatal period , 2007, Current opinion in clinical nutrition and metabolic care.

[58]  Christian Gluud,et al.  Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. , 2007, JAMA.

[59]  J. Pincemail,et al.  [Oxidative stress]. , 2007, Revue medicale de Liege.

[60]  L. Poston,et al.  Placental-related diseases of pregnancy: Involvement of oxidative stress and implications in human evolution. , 2006, Human reproduction update.

[61]  Caroline A Crowther,et al.  Spontaneous preterm delivery in primiparous women at low risk in Denmark: population based study , 2006, BMJ : British Medical Journal.

[62]  L. Poston,et al.  Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomised placebo-controlled trial , 2006, The Lancet.

[63]  A. Ayala,et al.  Correlation between circulating biomarkers of oxidative stress of maternal and umbilical cord blood at birth , 2006, Free radical research.

[64]  Sajal Gupta,et al.  The Role of Placental Oxidative Stress and Lipid Peroxidation in Preeclampsia , 2005, Obstetrical & gynecological survey.

[65]  G. Buonocore,et al.  Correlation among cytokines, bronchopulmonary dysplasia and modality of ventilation in preterm newborns: improvement with melatonin treatment , 2005, Journal of pineal research.

[66]  G. Buonocore,et al.  Isoprostanes in amniotic fluid: a predictive marker for fetal growth restriction in pregnancy. , 2005, Free radical biology & medicine.

[67]  E. Yan,et al.  Melatonin Provides Neuroprotection in the Late-Gestation Fetal Sheep Brain in Response to Umbilical Cord Occlusion , 2005, Developmental Neuroscience.

[68]  V. Clifton,et al.  Increased biological oxidation and reduced anti-oxidant enzyme activity in pre-eclamptic placentae. , 2004, Placenta.

[69]  L. Monte,et al.  [Bronchopulmonary dysplasia]. , 2005, Jornal de pediatria.

[70]  L. Myatt,et al.  Oxidative stress in the placenta , 2004, Histochemistry and Cell Biology.

[71]  L. Ment,et al.  Injury and repair in developing brain , 2004, Archives of Disease in Childhood - Fetal and Neonatal Edition.

[72]  L. Poston,et al.  Trophoblast oxidative stress, antioxidants and pregnancy outcome--a review. , 2004, Placenta.

[73]  R. Kohen,et al.  Oxidative stress in childhood--in health and disease states. , 2004, Clinical nutrition.

[74]  Vanesa Martín,et al.  Regulation of antioxidant enzymes: a significant role for melatonin , 2004, Journal of pineal research.

[75]  L. V. Van’ko,et al.  Changes in Regulation of Oxidase Activity of Peripheral Blood Granulocytes in Women with Habitual Abortions , 2003, Bulletin of Experimental Biology and Medicine.

[76]  R. Menon,et al.  Fetal membrane inflammatory cytokines: a switching mechanism between the preterm premature rupture of the membranes and preterm labor pathways , 2004, Journal of perinatal medicine.

[77]  R. Gagnon Placental insufficiency and its consequences. , 2003, European journal of obstetrics, gynecology, and reproductive biology.

[78]  H. Kinney,et al.  Nitrosative and Oxidative Injury to Premyelinating Oligodendrocytes in Periventricular Leukomalacia , 2003, Journal of neuropathology and experimental neurology.

[79]  I. Sargent,et al.  Pre-eclampsia, the placenta and the maternal systemic inflammatory response--a review. , 2003, Placenta.

[80]  O. Saugstad Bronchopulmonary dysplasia-oxidative stress and antioxidants. , 2003, Seminars in neonatology : SN.

[81]  B. Koletzko,et al.  Analysis of FA contents in individual lipid fractions from human placental tissue , 2003, Lipids.

[82]  M. Fuente Effects of antioxidants on immune system ageing , 2002, European Journal of Clinical Nutrition.

[83]  L. Kovács,et al.  Antioxidant enzyme activities are decreased in preterm infants and in neonates born via caesarean section. , 2002, European journal of obstetrics, gynecology, and reproductive biology.

[84]  R. Reiter,et al.  Causes of Oxidative Stress in the Pre- and Perinatal Period , 2002, Neonatology.

[85]  W. Lefkowitz Oxygen and resuscitation: beyond the myth. , 2002, Pediatrics.

[86]  R. Reiter,et al.  Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. , 2002, Current topics in medicinal chemistry.

[87]  S. Cuzzocrea,et al.  Increased levels of malondialdehyde and nitrite/nitrate in the blood of asphyxiated newborns: reduction by melatonin , 2001, Journal of pineal research.

[88]  T. Sano,et al.  [Diabetic retinopathy]. , 2001, Nihon rinsho. Japanese journal of clinical medicine.

[89]  E. Jauniaux,et al.  Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. , 2000, The American journal of pathology.

[90]  J Kattwinkel,et al.  International Guidelines for Neonatal Resuscitation: An excerpt from the Guidelines 2000 for Cardiopulmonary Resuscitation and Emergency Cardiovascular Care: International Consensus on Science. Contributors and Reviewers for the Neonatal Resuscitation Guidelines. , 2000, Pediatrics.

[91]  K. Hensley,et al.  Reactive oxygen species, cell signaling, and cell injury. , 2000, Free radical biology & medicine.

[92]  A. Jobe,et al.  Lung Injury and Surfactant Metabolism after Hyperventilation of Premature Lambs , 2000, Pediatric Research.

[93]  A. Wakatsuki,et al.  Melatonin increases activities of glutathione peroxidase and superoxide dismutase in fetal rat brain , 2000, Journal of pineal research.

[94]  C. V. Smith,et al.  Pulmonary Hypertension in Chronic Lung Disease of Infancy: Pathogenesis, Pathophysiology, and Treatment , 1999 .

[95]  P. Van Reempts,et al.  International guidelines for neonatal resuscitation: an excerpt from the guidelines 2000 for cardiopulmonary resuscitation and emergency cardiovascular care: international consensus on science , 2000 .

[96]  V. Bhandari,et al.  Hyperoxia Causes an Increase in Antioxidant Enzyme Activity in Adult and Fetal Rat Type II Pneumocytes , 2000, Lung.

[97]  C. Hubel,et al.  Oxidative Stress in the Pathogenesis of Preeclampsia (44447) , 1999, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[98]  B. Gladen,et al.  Levels of lipid peroxides in uncomplicated pregnancy: a review of the literature. , 1999, Reproductive toxicology.

[99]  R. Dellinger Inhaled nitric oxide in acute lung injury and acute respiratory distress syndrome , 1999, Intensive Care Medicine.

[100]  C. Price,et al.  Maternal and developmental toxicity evaluation of melatonin administered orally to pregnant Sprague-Dawley rats. , 1999, Toxicological sciences : an official journal of the Society of Toxicology.

[101]  V. Nadkarni,et al.  Resuscitation of the newly born infant: an advisory statement from the Pediatric Working Group of the International Liaison Committee on Resuscitation. , 1999, Resuscitation.

[102]  M. Nazıroğlu,et al.  Blood plasma levels of lipoperoxides, glutathione peroxidase, beta carotene, vitamin A and E in women with habitual abortion , 1998, Cell biochemistry and function.

[103]  C. Redman,et al.  Circulating markers of oxidative stress are raised in normal pregnancy and pre‐eclampsia , 1998, British journal of obstetrics and gynaecology.

[104]  S. Walsh,et al.  Placental mitochondria as a source of oxidative stress in pre-eclampsia. , 1998, Placenta.

[105]  A. Wakatsuki,et al.  Maternal‐fetal transfer of melatonin in pregnant women near term , 1998, Journal of pineal research.

[106]  G. Aykaç-toker,et al.  Imbalance between Lipid Peroxidation and Antioxidant Status in Preeclampsia , 1998, Gynecologic and Obstetric Investigation.

[107]  H. Ischiropoulos,et al.  Plasma 3-nitrotyrosine is elevated in premature infants who develop bronchopulmonary dysplasia. , 1998, Pediatrics.

[108]  R. Romero,et al.  Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. , 1996, American journal of obstetrics and gynecology.

[109]  O. Saugstad Mechanisms of tissue injury by oxygen radicals: implications for neonatal disease , 1996, Acta paediatrica.

[110]  L. Parker,et al.  Necrotizing Enterocolitis: Have We Made Any Progress in Reducing the Risk? , 2013, Advances in neonatal care : official journal of the National Association of Neonatal Nurses.

[111]  T. Akiyama,et al.  Oxygen radical-induced single-strand DNA breaks and repair of the damage in a cell-free system. , 1995, Mutation research.

[112]  S. Walsh,et al.  Secretion of lipid peroxides by the human placenta. , 1993, American journal of obstetrics and gynecology.

[113]  T. Slater,et al.  An introduction to free radical biochemistry. , 1993, British medical bulletin.

[114]  B. Speidel Effective Care of the Newborn Infant , 1992 .

[115]  Z. Medvedev AN ATTEMPT AT A RATIONAL CLASSIFICATION OF THEORIES OF AGEING , 1990, Biological reviews of the Cambridge Philosophical Society.

[116]  J. Eaton,et al.  Oxygen radicals and antioxidant enzymes alter pulmonary vascular reactivity in the rat lung. , 1989, Journal of applied physiology.

[117]  O. Saugstad,et al.  Reactive oxygen metabolites relax the lamb ductus arteriosus by stimulating prostaglandin production. , 1989, Circulation research.

[118]  O. Saugstad Hypoxanthine as an Indicator of Hypoxia: Its Role in Health and Disease through Free Radical Production , 1988, Pediatric Research.

[119]  W. Silverman Retinopathy of prematurity: oxygen dogma challenged. , 1982, Archives of disease in childhood.