Skip to main content

Cerebral Disorders and Consequences of Delayed Intrauterine Development of a Full-Term Baby: The Role of Oxidative Stress and Melatonin

Abstract

The review presents the results of clinical and experimental studies, indicating a high frequency of structural and functional disorders, brain development, and mechanisms that determine long-term adverse effects in children born with intrauterine growth retardation (IUGR). The key role of maternal melatonin and its circadian rhythm in protection against damage caused by oxidative stress and inflammation during pregnancy complications is considered. The development of specific biomarkers for early diagnosis of brain damage in IUGR of a child and methods of early neuroprotection will make it possible to approach the prevention of neuropsychiatric consequences from a new perspective.

This is a preview of subscription content, access via your institution.

REFERENCES

  1. Malhotra, A., Allison, B.J., Castillo-Melendez, M., et al., Neonatal morbidities of fetal growth restriction: pathophysiology and impact, Front. Endocrinol. (Lausanne), 2019, vol. 10, art. ID 55.

  2. Wang, Y., Fu, W., and Liu, J., Neurodevelopment in children with intrauterine growth restriction: adverse effects and interventions, J. Matern.-Fetal Neonat. Med., 2016, vol. 29, no. 4, p. 660.

    CAS  Article  Google Scholar 

  3. Armengaud, J.B., Yzydorczyk, C., Siddeek, B., et al., Intrauterine growth restriction: clinical consequences on health and disease at adulthood, Reprod. Toxicol., 2021, vol. 99, p. 168.

    CAS  PubMed  Article  Google Scholar 

  4. Leitner, Y., Fattal-Valevski, A., Geva, R., et al., Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study, J. Child Neurol., 2007, vol. 22, no. 5, p. 580.

    PubMed  Article  Google Scholar 

  5. Saenger, P., Czernichow, P., Hughes, I., and Reiter, E.O., Small for gestational age: short stature and beyond, Endocrinol. Rev., 2007, vol. 28, no. 2, p. 219.

    CAS  Article  Google Scholar 

  6. Miller, S.L., Huppi, P.S., and Mallard, C., The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome, J. Physiol., 2016, vol. 594, no. 4, p. 807.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. Figueras, F. and Gardosi, J., Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management, Am. J. Obstet. Gynecol., 2011, vol. 204, no. 4, p. 288.

    PubMed  Article  Google Scholar 

  8. Krishna, R.G. and Bhat, B., Molecular mechanisms of intrauterine growth restriction, J. Matern.-Fetal Neonat. Med., 2018, vol. 31, no. 19, p. 2634.

    Article  CAS  Google Scholar 

  9. Romo, A., Carceller, R., and Tobajas, J., Intrauterine growth retardation (IUGR): epidemiology and etiology, Pediatr. Endocrinol. Rev., 2009, vol. 6, suppl. 3, p. 332.

    PubMed  Google Scholar 

  10. Nasiri, K., Moodie, E.E.M., and Abenhaim, H.A., To what extent is the association between race and fetal growth restriction explained by adequacy of prenatal care? A causal mediation analysis of a retrospectively selected cohort, Am. J. Epidemiol., 2020, vol. 189, no. 11, p. 1360.

    PubMed  PubMed Central  Article  Google Scholar 

  11. Nardozza, L.M., Caetano, A.C., Zamarian, A.C., et al., Fetal growth restriction: current knowledge, Arch. Gynecol. Obstet., 2017, vol. 295, no. 5, p. 1061.

    PubMed  Article  Google Scholar 

  12. Sharma, D., Shastri, S., and Sharma, P., Intrauterine growth restriction: antenatal and postnatal aspects, Clin. Med. Insights Pediatr., 2016, vol. 10, p. 67.

    PubMed  PubMed Central  Google Scholar 

  13. Strizhakov, A.N., Ignatko, I.V., Timokhina, E.V., and Belotserkovtseva, L.D., Sindrom zaderzhki rosta ploda: patogenez, diagnostika, lechenie, akusherskaya taktika (Intrauterine Fetal Growth Restriction: Pathogenesis, Diagnostic, Management, and Obstetric Tactics), Moscow: GEOTAR-Media, 2013.

  14. Dall’Asta, A., Brunelli, V., and Prefumo, F., Early onset fetal growth restriction, Matern. Health Neonatol. Perinatol., 2017, vol. 3, p. 2.

    PubMed  PubMed Central  Article  Google Scholar 

  15. Figueras, F. and Gratacos, E., Update on the diagnosis and classification on fetal growth restriction and proposal of a stage-based management protocol, Fetal Diagn. Ther., 2014, vol. 36, no. 2, p. 86.

    PubMed  Article  Google Scholar 

  16. Ignatko, I.V., Denisova, Yu.V., Filippova, Yu.A., and Dubinin, A.O., Differential diagnostics of early and late forms of fetal growth retardation syndrome, Ural. Med. Zh., 2020, no. 12 (195), p. 91.

  17. Giussani, D.A., The fetal brain sparing response to hypoxia: physiological mechanisms, J. Physiol., 2016, vol. 594, no. 5, p. 1215.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. Poudel, R., McMillen, I.C., Dunn, S.L., et al., Impact of chronic hypoxemia on blood flow to the brain, heart, and adrenal gland in the late-gestation IUGR sheep fetus, Am. J. Physiol.: Regul. Integr. Comp. Physiol., 2015, vol. 308, no. 3, p. 151.

    Google Scholar 

  19. Cohen, E., Baerts, W., and van Bel, F., Brain-sparing in intrauterine growth restriction: considerations for the neonatologist, Neonatology., 2015, vol. 108, no. 4, p. 269.

    PubMed  Article  Google Scholar 

  20. Murray, E., Fernades, M., Fazel, M., et al., Differential effect of intrauterine growth restriction on childhood neurodevelopment: a systematic review, Br. J. Obstet. Gynaecol., 2015, vol. 122, no. 8, p. 1062.

    CAS  Article  Google Scholar 

  21. Zhu, M.Y., Milligan, N., Keating, S., et al., The hemodynamics of late-onset intrauterine growth restriction by MRI, Am. J. Obstet. Gynecol., 2016, vol. 214, no. 3, p. 367.

    PubMed  Article  Google Scholar 

  22. Samuelsen, G.B., Pakkenberg, B., Bogdanovic, N., et al., Severe cell reduction in the future brain cortex in human growth-restricted fetuses and infants, Am. J. Obstet. Gynecol., 2007, vol. 197, no. 1, p. 56.

    PubMed  Article  Google Scholar 

  23. Dubois, J., Benders, M., Borradori-Tolsa, C., et al., Primary cortical folding in the human newborn: an early marker of later functional development, Brain, 2008, vol. 131, no. 8, p. 2028.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. Dieni, S. and Rees, S., Dendritic morphology is altered in hippocampal neurons following prenatal compromise, J. Neurobiol., 2003, vol. 55, no. 1, p. 41.

    PubMed  Article  Google Scholar 

  25. Damodaram, M.S., Story, L., Eixarch, E., et al., Fetal volumetry using magnetic resonance imaging in intrauterine growth restriction, Early Hum. Dev., 2012, vol. 88, supl. 1, p. 35.

    Article  Google Scholar 

  26. Evsyukova, I.I., Koval’chuk-Kovalevskaya, O.V., Maslyanyuk, N.A., and Dodkhoev, D.S., Features of cyclic sleep organization and melatonin production in full-term newborns with intrauterine growth retardation, Hum. Physiol., 2013, vol. 39, no. 6, p. 617.

    CAS  Article  Google Scholar 

  27. Eixarch, E., Meler, E., Iraola, A., et al., Neurodevelopmental outcome in 2-year-old infants who were small-for-gestational age term fetuses with cerebral blood flow redistribution, Ultrasound Obstet. Gynecol., 2008, vol. 32, no. 7, p. 894.

    CAS  PubMed  Article  Google Scholar 

  28. Rosa, S.J., Steegers, E.A., Verburg, B.O., et al., What is spared by fetal brain-sparing? Fetal circulatory redistribution and behavioral problems in the general population, Am. J. Epidemiol., 2008, vol. 168, no. 10, p. 1145.

    Article  Google Scholar 

  29. Hartkopf, J., Schleger, F., Keune, J., et al., Impact of intrauterine growth restriction on cognitive and motor development at 2 years of age, Front. Physiol., 2018, vol. 9, p. 1278.

    PubMed  PubMed Central  Article  Google Scholar 

  30. Sacchi, C., Marino, C., Nosarti, C., et al., Association of intrauterine growth restriction and small for gestational age status with childhood cognitive outcomes: a systematic review and meta-analysis, J.A.M.A. Pediatr., 2020, vol. 174, no. 8, p. 772.

    Google Scholar 

  31. Bellido-González, M., Díaz-López, M.A., López-Criado, S., and Maldonado-Lozano, J., Cognitive functioning and academic achievement in children aged 6–8 years, born at term after intrauterine growth restriction and fetal cerebral redistribution, J. Pediatr. Psychol., 2017, vol. 42, no. 3, p. 345.

    PubMed  Google Scholar 

  32. Korkalainen, N., Partanen, L., Rasanen, L., et al., Fetal hemodynamics and language skills in primary school-aged children with fetal growth restriction: a longitudinal study, Early Hum. Dev., 2019, vol. 134, p. 34.

    PubMed  Article  Google Scholar 

  33. Partanen, L., Korkalainen, N., Mäkikallio, K., et al., Fetal growth restriction is associated with poor reading and spelling skills at eight years to 10 years of age, Acta Paediatr., 2018, vol. 107, no. 1, p. 79.

    PubMed  Article  Google Scholar 

  34. Ozhegov, A.M., Trubachev, E.A., and Petrova, I.N., Cardio-cerebral hemodynamics in children of the first year of life born with intrauterine growth restriction, Detskaya Bol’nitsa, 2012, vol. 48, no. 2, p. 34.

    Google Scholar 

  35. Geva, R., Eshel, R., Leitner, Y., et al., Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study, Pediatrics, 2006, vol. 118, no. 1, p. 91.

    PubMed  Article  Google Scholar 

  36. Baschat, A.A., Neurodevelopment after fetal growth restriction, Fetal Diagn. Ther., 2014, vol. 36, no. 2, p. 136.

    PubMed  Article  Google Scholar 

  37. Pels, A., Knaven, O.C., Wijnberg-Williams, B.J., et al., Neurodevelopmental outcomes at five years after early-onset fetal growth restriction: analyses in a Dutch subgroup participating in a European management trial, Eur. J. Obstet. Gynecol. Reprod. Biol., 2019, vol. 234, p. 63.

    CAS  PubMed  Article  Google Scholar 

  38. Vollmer, B. and Edmonds, C.J., School age neurological and cognitive outcomes of fetal growth retardation or small for gestational age Birth weight, Front. Endocrinol., 2019, vol. 10, p. 186.

    Article  Google Scholar 

  39. Arcangelli, T., Thilaganathan, B., Hooper, R., et al., Neurodevelopmental delay in small babies at term: a systematic review, Ultrasound Obstet. Gynecol., 2012, vol. 40, no. 3, p. 267.

    Article  Google Scholar 

  40. Castillo-Melendez, M., Yawno, T., Allison, B., et al., Cerebrovascular adaptations to chronic hypoxia in the growth restricted lamb, Int. J. Dev. Neurosci., 2015, vol. 45, p. 55.

    CAS  PubMed  Article  Google Scholar 

  41. Tolcos, M., Petratos, S., Hirst, J.J., et al., Blocked, delayed, or obstructed: What causes poor white matter development in intrauterine growth restricted infants? Prog. Neurobiol., 2017, vol. 154, p. 62.

    PubMed  Article  Google Scholar 

  42. Alves de Alencar Rocha, A.K., Allison, B.J., Yawno, T., et al., Early- versus late-onset fetal growth restriction differentially affects the development of the fetal sheep brain, Dev. Neurosci., 2017, vol. 39, nos. 1–4, p. 141.

    CAS  PubMed  Article  Google Scholar 

  43. Uysal, A., Oktem, G., Yilmaz, O., et al., Quantitative immunohistochemical analysis f nitric oxide synthases and apoptosis regulator proteins in the fetal rat brain following maternal uterine artery ligation, Int. J. Neurosci., 2008, vol. 118, no. 6, p. 891.

    CAS  PubMed  Article  Google Scholar 

  44. Lister, J.P., Blatt, G.J., De Bassio, W.A., et al., Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation, Hipocampus, 2005, vol. 15, no. 3, p. 393.

    Article  Google Scholar 

  45. Mallard, C., Loeliger, M., Copolov, D., and Rees, S., Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth restriction, Neuroscience, 2000, vol. 100, no. 2, p. 327.

    CAS  PubMed  Article  Google Scholar 

  46. Sasaki, J., Fukami, E., Mimura, S., et al., Abnormal cerebral neuronal migration in a rat model of intrauterine growth retardation induced by synthetic thromboxane A2, Early Hum. Dev., 2000, vol. 58, no. 2, p. 91.

    CAS  PubMed  Article  Google Scholar 

  47. Basilious, A., Yager, J., and Fehlings, M.G., Neurological outcomes of animal models of uterine artery ligation and relevance to human intrauterine growth restriction: a systematic review, Dev. Med. Child Neurol., 2015, vol. 57, no. 5, p. 420.

    PubMed  Article  Google Scholar 

  48. Batalle, D., Muñoz-Moreno, E., Arbat-Plana, A., et al., Long-term reorganization of structural brain networks in a rabbit model of intrauterine growth restriction, NeuroImage, 2014, vol. 100, p. 24.

    PubMed  Article  Google Scholar 

  49. Tumanova, N.L., Vasiliev, D.S., Dubrovskaya, N.M., and Zhuravin, I.A., Ultrastructural alterations in the sensorimotor cortex upon delayed development of motor behavior in early ontogenesis of rats exposed to prenatal hypoxia, Cell Tissue Biol., 2018, vol. 12, no. 5, p. 419.

    Article  Google Scholar 

  50. Hsiao, E.Y. and Patterson, P.H., Placental regulation of maternal-fetal interactions and brain development, Dev. Neurobiol., 2012, vol. 72, no. 10, p. 1317.

    PubMed  Article  Google Scholar 

  51. Perez, M., Robbins, M.E., Revhaug, C., and Saugstad, O.D., Oxygen radical disease in the newborn, revisited: oxidative stress and disease in the newborn period, Free Radical Biol. Med., 2019, vol. 142, p. 61.

    CAS  Article  Google Scholar 

  52. D’Angelo, G., Chimenz, R., Reiter, R.J., and Gitto, E., Use of melatonin in oxidative stress related neonatal diseases, Antioxidant (Basel), 2020, vol. 9, no. 6, p. 477.

    Article  CAS  Google Scholar 

  53. Lemasters, J.J., Qian, T., He, L., et al., Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy, Antioxid. Redox Signaling, 2002, vol. 4, no. 5, p. 769.

    CAS  Article  Google Scholar 

  54. Solevag, A.L., Schmolzer, G.M., and Cheung, P.Y., Novel interventions to reduce oxidative-stress related brain injury in neonatal asphyxia, Free Radical Biol. Med., 2019, vol. 142, p. 113.

    CAS  Article  Google Scholar 

  55. Vasiljevic, B., Maglajlic-Djukic, S., Gojnic, M., et al., New insights into the pathogenesis of perinatal hypoxic-ischemic brain injury, Pediatr. Int., 2011, vol. 53, no. 4, p. 454.

    CAS  PubMed  Article  Google Scholar 

  56. Back S.A., Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms, Ment. Retard. Dev. Disabil. Res. Rev., 2006, vol. 12, no. 2, p. 129.

    PubMed  Article  Google Scholar 

  57. Chiarello, D.I., Abada, C., Rojasa, D., et al., Oxidative stress: normal pregnancy versus preeclampsia, Biochim. Biophys. Acta, Mol. Basis Dis., 2020, vol. 1866, no. 2, art. ID 165354.

  58. Rodrigo, J., Fernandez, A.P., and Serrano, J., The role of free radicals in cerebral hypoxia and ischemia, Free Radical Biol. Med., 2005, vol. 39, no. 1, p. 26.

    CAS  Article  Google Scholar 

  59. Korkmaz, A., Rosales-Corral, S., and Reiter, R.J., Gene regulation by melatonin linked to epigenetic phenomena, Gene, 2012, vol. 503, no. 1, p. 1.

    CAS  PubMed  Article  Google Scholar 

  60. Morozova, A.Yu., Arutyunyan, A.V., Morozova, P.Yu., et al., Effect of prenatal hypoxia on activity of the soluble forms of cholinesterases in rat brain structures during early postnatal ontogenesis, J. Evol. Biochem. Physiol., 2020, vol. 56, no. 6, p. 531.

    CAS  Article  Google Scholar 

  61. Zakharova, E.I., Svinov, M.M., Germanova, E.N., et al., Involvement mechanisms of cholinergic systems into the morphofunctional reorganization of the neocortex and hippocampus in brain hypoxia, in Problemy gipoksii: molekulyarnye, fiziologicheskie i meditsinskie aspekty (Hypoxia: Molecular, Physiological, and Medical Aspects), Luk’yanova, L.D. and Ushakova, I.B., Moscow, 2004.

  62. Kaur, C., Rathnasamy, G., and Ling, E.A., Roles of activated microglia in hypoxia induced neuroinflammation in the developing brain and the retina, J. Neuroimmun. Pharmacol., 2013, vol. 8, no. 1, p. 66.

    Article  Google Scholar 

  63. Hossain, M.A., Hypoxic-ischemic injury in neonatal brain: involvement of a novel neuronal molecule in neuronal cell death and potential target for neuroprotection, Int. J. Dev. Neurosci., 2008, vol. 26, no. 1, p. 93.

    CAS  PubMed  Article  Google Scholar 

  64. Sullivan, E.L., Grayson, B., Takahashi, D., et al., Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring, J. Neurosci., 2010, vol. 30, no. 10, p. 3826.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. Maltepe, E., Bakardjiev, A.I., and Fisher, S.J., The placenta: transcriptional, epigenetic, and physiological integration during development, J. Clin. Invest., 2010, vol. 120, no. 4, p. 1016.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. Jawahar, M.C., Murgatroyd, C., Harrison, E.L., and Baune, B.T., Epigenetic alterations following early postnatal stress: a review on novel aetiological mechanisms of common psychiatric disorders, Clin. Epigenet., 2015, vol. 7, p. 122.

    Article  CAS  Google Scholar 

  67. Liu, J. and Casaccia, P., Epigenetic regulation of oligodendrocyte identity, Trends Neurosci., 2010, vol. 33, no. 4, p. 193.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  68. van der Burg, J.W., Sen, S., Chomitz, V.R., et al., The role of systemic inflammation linking maternal BMI to neurodevelopment in children, Pediatr. Res., 2016, vol. 79, no. 1-1, p. 3.

  69. Ogata, J., Yamanishi, H., and Ishibashi-Ueda, H., Review: role of cerebral vessels in ischaemic injury of the brain, Neuropathol. Appl. Neurobiol., 2011, vol. 37, no. 1, p. 40.

    CAS  PubMed  Article  Google Scholar 

  70. Goines, P.E., Croen, L.A., Braunschweig, D., et al., Increased midgestational IFN-γ, IL-4 and IL-5 in women bearing a child with autism: a case-control study, Mol. Autism, 2011, vol. 2, no. 13, p. 1.

    Article  CAS  Google Scholar 

  71. McGowan, P.O. and Szyf, M., The epigenetics of social adversity in early life: implications for mental health outcomes, Neurobiol. Dis., 2010, vol. 39, no. 10, p. 66.

    PubMed  Article  Google Scholar 

  72. Lesch, K.-P., When the serotonin transporter gene meets adversity: the contribution of animal models to understanding epigenetic mechanisms in affective disorders and resilience, Curr. Top. Behav. Neurosci., 2011, vol. 7, p. 251.

    PubMed  Article  Google Scholar 

  73. Bale, T.L., Baram, T.Z., Brown, A.S., et al., Early life programming and neurodevelopmental disorders, Biol. Psychiatry, 2010, vol. 68, no. 4, p. 314.

    PubMed  PubMed Central  Article  Google Scholar 

  74. Evsyukova, I.I., The role of melatonin in prenatal ontogenesis, J. Evol. Biochem. Phys., 2021, vol. 57, no. 1, p. 33.

    CAS  Article  Google Scholar 

  75. Korkmaz, A. and Reiter, R.J., Epigenetic regulation: a new research area for melatonin, J. Pineal Res., 2008, vol. 44, no. 1, p. 41.

    CAS  PubMed  Google Scholar 

  76. Sharma, R., Ottenhof, T., Rzeczkowska, P.A., and Niles, L.P., Epigenetic targets for melatonin: induction of histone H3 hyperacetylation and gene expression in C17.2 neural stem cells, J. Pineal Res., 2008, vol. 45, no. 3, p. 277.

    CAS  PubMed  Article  Google Scholar 

  77. Galano, A., Tan, D.X., Reiter, R.J., et al., Melatonin: a versatile protector against oxidative DNA damage, Molecules, 2018, vol. 23, no. 3, p. 530.

    PubMed Central  Article  CAS  Google Scholar 

  78. Ireland, K.E., Maloyan, A., and Myatt, L., Melatonin improves mitochondrial respiration in syncytiotrophoblasts from placentas of obese women, Reprod. Sci., 2018, vol. 25, no. 1, p. 120.

    CAS  PubMed  Article  Google Scholar 

  79. Chitimus, D.M., Popescu, M.R., Voiculescu, S.E., et al., Melatonin’s impact on antioxidative and anti-inflammatory reprogramming in homeostasis and disease, Biomolecules, 2020, vol. 10, no. 9, p. 1211.

    CAS  PubMed Central  Article  Google Scholar 

  80. Carloni, C., Favrais, G., Saliba, E., et al., Melatonin modulates neonatal brain inflammation through endoplasmic reticulum stress, autophagy, and miR-34a/silent information regulator 1 pathway, J. Pineal Res., 2016, vol. 61, no. 3, p. 370.

    CAS  PubMed  Article  Google Scholar 

  81. Olivier, P., Fontaine, R.H., Loron, G., et al., Melatonin promotes oligodendroglial maturation of injured white matter in neonatal rats, PLoS One, 2009, vol. 4, no. 9, p. 7128.

    Article  CAS  Google Scholar 

  82. Tarocco, A., Caroccia, N., Morciano, G., et al., Melatonin as a master regulator of cell death and inflammation: molecular mechanisms and clinical implications for newborn care, Cell Death Dis., 2019, vol. 10, no. 4, p. 317.

    PubMed  PubMed Central  Article  Google Scholar 

  83. Arutjunyan, A.V., Evsyukova, I.I., and Polyako-va, V.O., The role of melatonin in morphofunctional development of the brain in early ontogeny, Neurochem. J., 2019, vol. 13, no. 3, p. 240.

    CAS  Article  Google Scholar 

  84. Sivakumar, J., Lu, J., Ling, E.A., and Kaur, C., Vascular endothelial growth factor and nitric oxide production in response to hypoxia in the choroid plexus in neonatal brain, Brain Pathol., 2008, vol. 18, no. 1, p. 71.

    CAS  PubMed  Article  Google Scholar 

  85. Kaur, C., Sivakumar, Y., Lu, J., et al., Melatonin attenuates hypoxia-induced ultrastructural changes and increased vascular permeability in the developing hippocampus, Brain Pathol., 2008, vol. 18, no. 4, p. 533.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Shimada, M., Seki, H., Samejima, M., et al., Salivary melatonin levels and sleep-wake rhythms in pregnant women with hypertensive and glucose metabolic disorders: a prospective analysis, Biosci. Trends, 2016, vol. 10, no. 1, p. 34.

    CAS  PubMed  Article  Google Scholar 

  87. Evsyukova, I.I., Molecular functional mechanisms of the mother-placenta-fetus system in obesity and gestational diabetes mellitus, Mol. Med., 2020, vol. 18, no. 1, p. 56.

    Google Scholar 

  88. Bouchlariotou, S., Liakopoulos, V., Giannopou-lou, M., et al., Melatonin secretion is impaired in women with preeclampsia and abnormal circadian blood pressure rhythm, Ren. Failure, 2014, vol. 36, no. 7, p. 1001.

    CAS  Article  Google Scholar 

  89. Shalal, M.M., Kadhim, I.M., Abbas, N.S., and Abdulsattar, G., Measuring of plasma melatonin level in patients with preeclampsia, J. Fac. Med. Baghdad, 2017, vol. 59, no. 3, p. 234.

    Article  Google Scholar 

  90. Zeng K., Gao Y., Wan J., et al., The reduction in circulating levels of melatonin may be associated with the development of preeclampsia, J. Hum. Hypertens., 2016, vol. 30, no. 11, p. 666.

    CAS  PubMed  Article  Google Scholar 

  91. Lanoix, D., Guerin, P., and Vaillancourt, C., Placental melatonin production and melatonin receptor expression are altered in preeclampsia: new insights into the role of this hormone in pregnancy, J. Pineal Res., 2012, vol. 53, no. 4, p. 417.

    CAS  PubMed  Article  Google Scholar 

  92. Gupta, S., Aziz, N., Sekhon, L., et al., Lipid peroxidation and antioxidant status in preeclampsia. A systematic review, Obstet. Gynecol. Surv., 2009, vol. 64, no. 11, p. 750.

    PubMed  Article  Google Scholar 

  93. Berbets, A., Koval, H., Barbe, A., et al., Melatonin decreases and cytokines increase in women with placental insufficiency, J. Matern.-Fetal Neonat. Med., 2021, vol. 34, no. 3, p. 373.

    CAS  Article  Google Scholar 

  94. Ivanov, D.O., Evsyukova, I.I., Mazzoccoli, G., et al., The role of prenatal melatonin in the regulation of childhood obesity, Biology, 2020, vol. 9, no. 4, p. 72.

    CAS  PubMed Central  Article  Google Scholar 

  95. Tain, Y.-L., Huang, L.-T., and Hsu, C.-N., Developntal programming of adult disease: reprogramming by melatonin? Int. J. Mol. Sci., 2017, vol. 18, no. 2, p. 426.

    PubMed Central  Article  CAS  Google Scholar 

  96. Wilkinson, D., Shepherd, E., and Wallace, E.M., Melatonin for women in pregnancy for neuroprotection of the fetus, Cochrane Database Syst. Rev., 2016, vol. 3, no. 3, art. ID CDO10527.

    Google Scholar 

  97. Sagrillo-Fagundes, L., Assunção Salustiano, E.M., Ruano, R., et al., Melatonin modulates autophagy and inflammation protecting human placental trophoblast from hypoxia/reoxygenation, J. Pineal Res., 2018, vol. 65, no. 4, p. 12520.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. I. Evsyukova.

Ethics declarations

CONFLICT OF INTERESTS

The authors declare that they do not have a conflict of interest.

COMPLIANCE WITH ETHICAL STANDARDS

This work does not contain any studies involving animals or human subjects performed by any of the authors.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Evsyukova, I.I. Cerebral Disorders and Consequences of Delayed Intrauterine Development of a Full-Term Baby: The Role of Oxidative Stress and Melatonin. Hum Physiol 48, 340–345 (2022). https://doi.org/10.1134/S0362119722030057

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0362119722030057

Keywords:

  • newborns
  • IUGR
  • brain
  • neuropsychiatric consequences
  • mechanism
  • melatonin