Mechanisms of injury in the nervous system in fetuses with growth restriction
- Authors: Nikolayenkov I.P.1, Shakalis D.V.2,3, Sudakov D.S.1,4
-
Affiliations:
- The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott
- St. Petersburg State Pediatric Medical University
- Perinatal Center, Leningrad Regional Clinical Hospital
- North-Western State Medical University named after I.I. Mechnikov
- Issue: Vol 73, No 1 (2024)
- Pages: 125-136
- Section: Reviews
- Submitted: 23.06.2023
- Accepted: 08.12.2023
- Published: 26.03.2024
- URL: https://journals.eco-vector.com/jowd/article/view/501748
- DOI: https://doi.org/10.17816/JOWD501748
- ID: 501748
Cite item
Abstract
This review article analyzes current literature on the mechanisms of damage to the nervous system in fetal growth restriction, which is a leading cause of perinatal morbidity and mortality in the economically developed countries. In some cases, this condition is associated with damage to the fetal nervous system, the symptoms of which can persist throughout life. Foundation of the effective pathogenetic therapy for intrauterine growth restriction during pregnancy would significantly reduce child mortality, morbidity and disability, and ease the financial burden on the healthcare system and social institutions.
Full Text
About the authors
Igor P. Nikolayenkov
The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott
Email: nikolaenkov_igor@mail.ru
ORCID iD: 0000-0003-2780-0887
MD, Cand. Sci. (Med.)
Russian Federation, Saint PetersburgDmitry V. Shakalis
St. Petersburg State Pediatric Medical University; Perinatal Center, Leningrad Regional Clinical Hospital
Email: shakalisdoc@gmail.com
ORCID iD: 0009-0002-7876-365X
MD
Russian Federation, Saint Petersburg; Saint PetersburgDmitry S. Sudakov
The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott; North-Western State Medical University named after I.I. Mechnikov
Author for correspondence.
Email: suddakovv@yandex.ru
ORCID iD: 0000-0002-5270-0397
MD, Cand. Sci. (Med.)
Russian Federation, Saint Petersburg; Saint PetersburgReferences
- Miller SL, Huppi PS, Mallard C. The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome. J Physiol. 2016;594(4):807–823. doi: 10.1113/JP271402
- Audette MC, Kingdom JC. Screening for fetal growth restriction and placental insufficiency. Semin Fetal Neonatal Med. 2018;23(2):119–125. doi: 10.1016/j.siny.2017.11.004
- Bruin C, Damhuis S, Gordijn S, et al. Evaluation and management of suspected fetal growth restriction. Obstet Gynecol Clin North Am. 2021;48(2):371–385. doi: 10.1016/j.ogc.2021.02.007
- Ignatko IV, Bogomazova IM, Kardanova MA. Current views on the diagnosis and prognosis of fetal growth restriction (a literature review). Journal of Obstetrics and Women’s Diseases. 2023;72(3):65–76. EDN: JAVPCA doi: 10.17816/JOWD344442
- Russian Society of Obstetricians and Gynecologists. Insufficient fetal growth requiring maternal medical care (fetal growth restriction). Clinical recommendations. 2022. Available from: https://roag-portal.ru/recommendations_obstetrics (In Russ.)
- Morales-Roselló J, Khalil A, Morlando M, et al. Changes in fetal Doppler indices as a marker of failure to reach growth potential at term. Ultrasound Obstet Gynecol. 2014;43(3):303–310. doi: 10.1002/uog.13319
- Prior T, Paramasivam G, Bennett P, et al. Are fetuses that fail to achieve their growth potential at increased risk of intrapartum compromise? Ultrasound Obstet Gynecol. 2015;46(4):460–464. doi: 10.1002/uog.14758
- Poon LC, Tan MY, Yerlikaya G, et al. Birth weight in live births and stillbirths. Ultrasound Obstet Gynecol. 2016;48(5):602–606. doi: 10.1002/uog.17287
- Bligh LN, Flatley CJ, Kumar S. Reduced growth velocity at term is associated with adverse neonatal outcomes in non-small for gestational age infants. Eur J Obstet Gynecol Reprod Biol. 2019;240:125–129. doi: 10.1016/j.ejogrb.2019.06.026
- Gordijn SJ, Beune IM, Thilaganathan B, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48(3):333–339. doi: 10.1002/uog.15884
- Lees CC, Stampalija T, Baschat A, et al. ISUOG Practice Guidelines: diagnosis and management of small-for-gestational-age fetus and fetal growth restriction. Ultrasound Obstet Gynecol. 2020;56(2):298–312. doi: 10.1002/uog.22134
- Salomon LJ, Alfirevic Z, Da Silva Costa F, et al. ISUOG Practice Guidelines: ultrasound assessment of fetal biometry and growth. Ultrasound Obstet Gynecol. 2019;53(6):715–723. doi: 10.1002/uog.20272
- Molina LCG, Odibo L, Zientara S, et al. Validation of Delphi procedure consensus criteria for defining fetal growth restriction. Ultrasound Obstet Gynecol. 2020;56(1):61–66. doi: 10.1002/uog.20854
- Jarvis S, Glinianaia SV, Torrioli MG, et al; Surveillance of Cerebral Palsy in Europe (SCPE) collaboration of European Cerebral Palsy Registers. Cerebral palsy and intrauterine growth in single births: European collaborative study. Lancet. 2003;362(9390):1106–1111. doi: 10.1016/S0140-6736(03)14466-2
- Blair EM, Nelson KB. Fetal growth restriction and risk of cerebral palsy in singletons born after at least 35 weeks’ gestation. Am J Obstet Gynecol. 2015;212(4):520.e1–520.e7. doi: 10.1016/j.ajog.2014.10.1103
- Jacobsson B, Ahlin K, Francis A, et al. Cerebral palsy and restricted growth status at birth: population-based case-control study. BJOG. 2008;115(10):1250–1255. doi: 10.1111/j.1471-0528.2008.01827.x
- Guellec I, Lapillonne A, Marret S, et al; Étude Épidémiologique sur les Petits Âges Gestationnels (EPIPAGE; [Epidemiological Study on Small Gestational Ages]) Study Group. Effect of intra- and extrauterine growth on long-term neurologic outcomes of very preterm infants. J Pediatr. 2016;175:93.e1–99.e1. doi: 10.1016/j.jpeds.2016.05.027
- Cordero L, Franco A, Joy SD, et al. Monochorionic diamniotic infants without twin-to-twin transfusion syndrome. J Perinatol. 2005;25(12):753–758. doi: 10.1038/sj.jp.7211405
- Edmonds CJ, Isaacs EB, Cole TJ, et al. The effect of intrauterine growth on verbal IQ scores in childhood: a study of monozygotic twins. Pediatrics. 2010;126(5):e1095–e1101. doi: 10.1542/peds.2008-3684
- Baschat AA. Neurodevelopment after fetal growth restriction. Fetal Diagn Ther. 2014;36(2):136–142. doi: 10.1159/000353631
- Olivier P, Baud O, Evrard P, et al. Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol. 2005;64(11):998–1006. doi: 10.1097/01.jnen.0000187052.81889.57
- Olivier P, Baud O, Bouslama M, et al. Moderate growth restriction: deleterious and protective effects on white matter damage. Neurobiol Dis. 200726(1):253–263. doi: 10.1016/j.nbd.2007.01.001
- 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;131(Pt 8):2028–2041. doi: 10.1093/brain/awn137
- Samuelsen GB, Pakkenberg B, Bogdanović N, et al. Severe cell reduction in the future brain cortex in human growth-restricted fetuses and infants. Am J Obstet Gynecol. 2007;197(1):56.e1–56.e.7. doi: 10.1016/j.ajog.2007.02.011
- Fung C, Ke X, Brown AS, et al. Uteroplacental insufficiency alters rat hippocampal cellular phenotype in conjunction with ErbB receptor expression. Pediatr Res. 2012;72(1):2–9. doi: 10.1038/pr.2012.32
- Isaacs EB, Lucas A, Chong WK, et al. Hippocampal volume and everyday memory in children of very low birth weight. Pediatr Res. 2000;47(6):713–720. doi: 10.1203/00006450-200006000-00006
- Weng C, Huang L, Feng H, et al. Gestational chronic intermittent hypoxia induces hypertension, proteinuria, and fetal growth restriction in mice. Sleep Breath. 2022;26(4):1661–1669. doi: 10.1007/s11325-021-02529-3
- Poudel R, McMillen IC, Dunn SL, 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;308(3):R151–R162. doi: 10.1152/ajpregu.00036.2014
- Flood K, Unterscheider J, Daly S, et al. The role of brain sparing in the prediction of adverse outcomes in intrauterine growth restriction: results of the multicenter PORTO Study. Am J Obstet Gynecol. 2014;211(3):288.e1–288.e5. doi: 10.1016/j.ajog.2014.05.008
- Mone F, McConnell B, Thompson A, et al. Fetal umbilical artery Doppler pulsatility index and childhood neurocognitive outcome at 12 years. BMJ Open. 2016;6(6). doi: 10.1136/bmjopen-2015-008916
- Hernandez-Andrade E, Figueroa-Diesel H, Jansson T, et al. Changes in regional fetal cerebral blood flow perfusion in relation to hemodynamic deterioration in severely growth-restricted fetuses. Ultrasound Obstet Gynecol. 2008;32(1):71–76. doi: 10.1002/uog.5377
- Rees S, Harding R, Walker D. The biological basis of injury and neuroprotection in the fetal and neonatal brain. Int J Dev Neurosci. 2011;29(6):551–563. doi: 10.1016/j.ijdevneu.2011.04.004
- Favrais G, van de Looij Y, Fleiss B, et al. Systemic inflammation disrupts the developmental program of white matter. Ann Neurol. 2011;70(4):550–565. doi: 10.1002/ana.22489
- Rideau Batista Novais A, Pham H, Van de Looij Y, et al. Transcriptomic regulations in oligodendroglial and microglial cells related to brain damage following fetal growth restriction. Glia. 2016;64(12):2306–2320. doi: 10.1002/glia.23079
- Campbell LR, Pang Y, Ojeda NB, et al. Intracerebral lipopolysaccharide induces neuroinflammatory change and augmented brain injury in growth-restricted neonatal rats. Pediatr Res. 2012;71(6):645–652. doi: 10.1038/pr.2012.26
- Fleiss B, Gressens P. Tertiary mechanisms of brain damage: a new hope for treatment of cerebral palsy? Lancet Neurol. 2012;11(6):556–566. doi: 10.1016/S1474-4422(12)70058-3
- Muniyappa R, Sowers JR. Role of insulin resistance in endothelial dysfunction. Rev Endocr Metab Disord. 2013;14(1):5–12. doi: 10.1007/s11154-012-9229-1
- Kuzminykh TU, Borisova VYu, Nikolayenkov IP, et al. Role of biologically active molecules in uterine contractile activity. Journal of Obstetrics and Women’s Diseases. 2019;68(1):21–27. EDN: ZABXXV doi: 10.17816/JOWD68121-27
- Misharina EV, Borodina VL, Glavnova OB, et al. Insulin resistance and hyperinsulinemia. Journal of Obstetrics and Women’s Diseases. 2016;65(1):75–86. EDN: VVRVNL doi: 10.17816/JOWD65175-86
- Nestler JE. Regulation of the aromatase activity of human placental cytotrophoblasts by insulin, insulin-like growth factor-I, and -II. J Steroid Biochem Mol Biol. 1993;44(4–6):449–457. doi: 10.1016/0960-0760(93)90249-v
- Jobe SO, Tyler CT, Magness RR. Aberrant synthesis, metabolism, and plasma accumulation of circulating estrogens and estrogen metabolites in preeclampsia implications for vascular dysfunction. Hypertension. 2013;61(2):480–487. doi: 10.1161/HYPERTENSIONAHA.111.201624
- Berkane N, Liere P, Oudinet JP, et al. From pregnancy to preeclampsia: a key role for estrogens. Endocr Rev. 2017;38(2):123–144. doi: 10.1210/er.2016-1065
- Berkane N, Liere P, Lefevre G, et al. Abnormal steroidogenesis and aromatase activity in preeclampsia. Placenta. 2018;69:40–49. doi: 10.1016/j.placenta.2018.07.004
- Boucher J, Charalambous M, Zarse K, et al. Insulin and insulin-like growth factor 1 receptors are required for normal expression of imprinted genes. Proc Natl Acad Sci USA. 2014;111(40):14512–14517. doi: 10.1073/pnas.1415475111
- Leger J, Noel M, Limal JM, et al. Growth factors and intrauterine growth retardation. II. Serum growth hormone, insulin-like growth factor (IGF) I, and IGF-binding protein 3 levels in children with intrauterine growth retardation compared with normal control subjects: prospective study from birth to two years of age. Study Group of IUGR. Pediatr Res. 1996;40(1):101–107. doi: 10.1203/00006450-199607000-00018
- Godfrey KM, Hales CN, Osmond C, et al. Relation of cord plasma concentrations of proinsulin, 32-33 split proinsulin, insulin and C-peptide to placental weight and the baby’s size and proportions at birth. Early Hum Dev. 1996;46(1–2):129–140. doi: 10.1016/0378-3782(96)01752-5
- Gicquel C, Le Bouc Y. Hormonal regulation of fetal growth. Horm Res. 2006;65(Suppl 3):28–33. doi: 10.1159/000091503
- Dyer AH, Vahdatpour C, Sanfeliu A, et al. The role of Insulin-like growth factor 1 (IGF-1) in brain development, maturation and neuroplasticity. Neuroscience. 2016;325:89–99. doi: 10.1016/j.neuroscience.2016.03.056
- Park SE, Lawson M, Dantzer R, et al. Insulin-like growth factor-I peptides act centrally to decrease depression-like behavior of mice treated intraperitoneally with lipopolysaccharide. J Neuroinflammation. 2011;8:179. doi: 10.1186/1742-2094-8-179
- Pang Y, Zheng B, Campbell LR, et al. IGF-1 can either protect against or increase LPS-induced damage in the developing rat brain. Pediatr Res. 2010;67(6):579–584. doi: 10.1203/PDR.0b013e3181dc240f
- Cai Z, Fan LW, Lin S, et al. Intranasal administration of insulin-like growth factor-1 protects against lipopolysaccharide-induced injury in the developing rat brain. Neuroscience. 2011;194:195–207. doi: 10.1016/j.neuroscience.2011.08.003
- Lin S, Fan LW, Rhodes PG, et al. Intranasal administration of IGF-1 attenuates hypoxic-ischemic brain injury in neonatal rats. Exp Neurol. 2009;217(2):361–370. doi: 10.1016/j.expneurol.2009.03.021
- Wood TL, Loladze V, Altieri S, et al. Delayed IGF-1 administration rescues oligodendrocyte progenitors from glutamate-induced cell death and hypoxic-ischemic brain damage. Dev Neurosci. 2007;29(4–5):302–310. doi: 10.1159/000105471
- Lopes C, Ribeiro M, Duarte AI, et al. IGF-1 intranasal administration rescues Huntington’s disease phenotypes in YAC128 mice. Mol Neurobiol. 2014;49(3):1126–1142. doi: 10.1007/s12035-013-8585-5
- Murphy VE, Smith R, Giles WB, et al. Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocr Rev. 2006;27(2):141–169. doi: 10.1210/er.2005-0011
- Gurpide E, Marks C, de Ziegler D, et al. Asymmetric release of estrone and estradiol derived from labeled precursors in perfused human placentas. Am J Obstet Gynecol. 1982;144(5):551–555. doi: 10.1016/0002-9378(82)90226-5
- Wu L, Einstein M, Geissler WM, et al. Expression cloning and characterization of human 17 beta-hydroxysteroid dehydrogenase type 2, a microsomal enzyme possessing 20 alpha-hydroxysteroid dehydrogenase activity. J Biol Chem. 1993;268(17):12964–12969. doi: 10.1016/s0021-9258(18)31480-7
- Miranda A, Sousa N. Maternal hormonal milieu influence on fetal brain development. Brain Behav. 2018;8(2). doi: 10.1002/brb3.920
- Xiao Q, Luo Y, Lv F, et al. Protective effects of 17β-estradiol on hippocampal myelinated fibers in ovariectomized middle-aged rats. Neuroscience. 2018;385:143–153. doi: 10.1016/j.neuroscience.2018.06.006
- Cambiasso MJ, Colombo JA, Carrer HF. Differential effect of oestradiol and astroglia-conditioned media on the growth of hypothalamic neurons from male and female rat brains. Eur J Neurosci. 2000;12(7):2291–2298. doi: 10.1046/j.1460-9568.2000.00120.x
- Pansiot J, Mairesse J, Baud O. Protecting the developing brain by 17β-estradiol. Oncotarget. 2017;8(6):9011–9012. doi: 10.18632/oncotarget.14819
- McCarthy MM. The two faces of estradiol: effects on the developing brain. Neuroscientist. 2009;15(6):599–610. doi: 10.1177/1073858409340924
- Schumacher M, Hussain R, Gago N, et al. Progesterone synthesis in the nervous system: implications for myelination and myelin repair. Front Neurosci. 2012;6:10. doi: 10.3389/fnins.2012.00010
- Tsutsui K, Ukena K. Neurosteroids in the cerebellar Purkinje neuron and their actions (review). Int J Mol Med. 1999;4(1):49–56. doi: 10.3892/ijmm.4.1.49
- Luoma JI, Kelley BG, Mermelstein PG. Progesterone inhibition of voltage-gated calcium channels is a potential neuroprotective mechanism against excitotoxicity. Steroids. 2011;76(9):845–855. doi: 10.1016/j.steroids.2011.02.013
- Pluchino N, Russo M, Genazzani AR. The fetal brain: role of progesterone and allopregnanolone. Horm Mol Biol Clin Investig. 2016;27(1):29–34. doi: 10.1515/hmbci-2016-0020
- Nguyen PN, Billiards SS, Walker DW, et al. Changes in 5alpha-pregnane steroids and neurosteroidogenic enzyme expression in the perinatal sheep. Pediatr Res. 2003;53(6):956–964. doi: 10.1203/01.PDR.0000064905.64688.10
- Brunton PJ, Russell JA, Hirst JJ. Allopregnanolone in the brain: protecting pregnancy and birth outcomes. Prog Neurobiol. 2014;113:106–136. doi: 10.1016/j.pneurobio.2013.08.005
- Palliser HK, Kelleher MA, Tolcos M, et al. Effect of postnatal progesterone therapy following preterm birth on neurosteroid concentrations and cerebellar myelination in guinea pigs. J Dev Orig Health Dis. 2015;6(4):350–361. doi: 10.1017/S2040174415001075
- Xiao G, Wei J, Yan W, et al. Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: a randomized controlled trial. Crit Care. 2008;12(2):R61. doi: 10.1186/cc6887
- Noorlander CW, De Graan PN, Middeldorp J, et al. Ontogeny of hippocampal corticosteroid receptors: effects of antenatal glucocorticoids in human and mouse. J Comp Neurol. 2006;499(6):924–932. doi: 10.1002/cne.21162
- Anacker C, Cattaneo A, Luoni A, et al. Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacology. 2013;38(5):872–883. doi: 10.1038/npp.2012.253
- Economides DL, Nicolaides KH, Linton EA, et al. Plasma cortisol and adrenocorticotropin in appropriate and small for gestational age fetuses. Fetal Ther. 1988;3(3):158–164. doi: 10.1159/000263348
- Filiberto AC, Maccani MA, Koestler D, et al. Birthweight is associated with DNA promoter methylation of the glucocorticoid receptor in human placenta. Epigenetics. 2011;6(5):566–572. doi: 10.4161/epi.6.5.15236
- Ke X, Schober ME, McKnight RA, et al. Intrauterine growth retardation affects expression and epigenetic characteristics of the rat hippocampal glucocorticoid receptor gene. Physiol Genomics. 2010;42(2):177–189. doi: 10.1152/physiolgenomics.00201.2009
- Gómez-González B, Escobar A. Prenatal stress alters microglial development and distribution in postnatal rat brain. Acta Neuropathol. 2010;119(3):303–315. doi: 10.1007/s00401-009-0590-4
- Roque A, Ochoa-Zarzosa A, Torner L. Maternal separation activates microglial cells and induces an inflammatory response in the hippocampus of male rat pups, independently of hypothalamic and peripheral cytokine levels. Brain Behav Immun. 2016;55:39–48. doi: 10.1016/j.bbi.2015.09.017
- Matthews SG. Antenatal glucocorticoids and programming of the developing CNS. Pediatr Res. 2000;47(3):291–300. doi: 10.1203/00006450-200003000-00003
- Aylamazyan EK, Mozgovaya EV. Preeclampsia: theory and practice. Moscow: MEDpress-inform; 2008. EDN: QLRQIV
- Nikolaenkov IP. Anti-Mullerian hormone in the pathogenesis of polycystic ovary syndrome [dissertation]. Saint Petersburg; 2014. Available from: https://www.dissercat.com/content/antimyullerovgormon-v-patogeneze-sindroma-olikistoznykh-yaichnikov EDN: ZPMABL
- Acromite MT, Mantzoros CS, Leach RE, et al. Androgens in preeclampsia. Am J Obstet Gynecol. 1999;180(1 Pt 1):60–63. doi: 10.1016/s0002-9378(99)70150-x
- Pepene CE. Evidence for visfatin as an independent predictor of endothelial dysfunction in polycystic ovary syndrome. Clin Endocrinol. 2012;76(1):119–125. doi: 10.1111/j.1365-2265.2011.04171.x
- Kanasaki M, Srivastava SP, Yang F, et al. Deficiency in catechol-o-methyltransferase is linked to a disruption of glucose homeostasis in mice. Sci Rep. 2017;7(1):7927. doi: 10.1038/s41598-017-08513-w
- Nikolayenkov IP, Kuzminykh TU, Tarasova MA, et al. Features of the course of pregnancy in women with polycystic ovary syndrome. Journal of Obstetrics and Women’s Diseases. 2020;69(5):105–112. EDN: HNEEAT doi: 10.17816/JOWD695105-112
- Sun M, Maliqueo M, Benrick A, et al. Maternal androgen excess reduces placental and fetal weights, increases placental steroidogenesis, and leads to long-term health effects in their female offspring. Am J Physiol Endocrinol Metab. 2012;303(11):E1373–E1385. doi: 10.1152/ajpendo.00421.2012
- Wixey JA, Chand KK, Pham L, et al. Therapeutic potential to reduce brain injury in growth restricted newborns. J Physiol. 2018;596(23):5675–5686. doi: 10.1113/JP275428