Features of neurogenesis in fetal growth restriction

Kan N.E., Leonova A.A., Tyutyunnik V.L., Khachatryan Z.V.

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, Moscow, Russia
The paper analyzes the current literature data on the role of neurogenesis and fetal programming in fetal growth restriction. It considers the mechanisms and scientific hypotheses that lead to structural changes in the central nervous system and to neuroregulatory disorders even in the intrauterine period with adverse consequences to the development of the nervous system and social cognitive functions. The paper discusses the role of potential proteins as markers for brain damage in fetal growth restriction. A change in fetal programming, in the direction of immunometabolic processes, and in the level of an inflammatory response is a cause of health impairment, vital cardiovascular and neuroendocrine diseases in the postnatal period of life. Therefore, the identification of cellular and molecular mechanisms that cause placental dysfunction, the optimal development of fetal organs, and the disruption of genetic/epigenetic programming, proteins as markers for fetal brain matter damage, the determination of which is necessary for the early diagnosis of hypoxic ischemic encephalopathy, is a serious problem that needs to be further studied.
Conclusion: With the introduction of modern studies of epigenetic regulation, there is hope for the development of new methods to predict and diagnose fetal growth restriction, taking into account the findings on etiology and pathogenesis. Increasing information on the fetal programming of certain diseases in adults may be an important trigger to stop the progression of pathology.

Keywords

fetal growth retardation
neurogenesis
fetal programming
epigenetics

References

  1. Савельева Г.М., Сухих Г.Т., Серов В.Н., Радзинский В.Е., ред. Акушерство. Национальное руководство. 2-е изд. М.: ГЭОТАР-Медиа; 2022. 1080с. [Savelieva G.M., Sukhikh G.T., Serov V.N., Radzinsky V.E., ed. Obstetrics: National guideline. 2nd ed., revised and additional. Moscow: «GEOTAR-Media»; 2022. 1080 p. (in Russian)]
  2. Министерство здравоохраненеия Российской Федерации. Недостаточный рост плода, требующий предоставления медицинской помощи (задержка роста плода). Клинические рекомендации. М.; 2021. 71с. [Ministry of Health of the Russian Federation. Insufficient fetal growth requiring medical attention (fetal growth retardation). Clinical guidelines. Moscow; 2021. 71 p.(in Russian)].
  3. RCOG. Small-for-gestational-age fetus, investigation and management.Green-top Guideline No. 31. 2014.
  4. Sharma D., Farahbakhsh N., Shastri S., Sharma P. Intrauterine growth restriction – part 2. J. Matern. Fetal Neonatal Med. 2016; 29(24): 4037-48. https://dx.doi.org/10.3109/14767058.2016.1154525.
  5. Джобава Э.М. Фетальное программирование. Акушерство и гинекология. 2018; 3: 10-5. https://dx.doi.org/10.18565/aig.2018.3.10-15. [Jobava E.M. Fetal programming. Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2018; 7: 10-5. (in Russian)]. https://dx.doi.org/10.18565/aig.2018.3.10-15.
  6. Armengaud J.B., Yzydorczyk C., Siddeek B., Peyter A.C., Simeoni U. Intrauterine growth restriction: clinical consequences on health and disease at adulthood. Reprod. Toxicol. 2021; 99: 168-76. https://dx.doi.org/10.1016/j.reprotox.2020.10.005.
  7. Kwon E.J., Kim Y.J. What is fetal programming?: a lifetime health is under the control of in utero health. Obstet. Gynecol. Sci. 2017; 60(6): 506-19.https://dx.doi.org/10.5468/ogs.2017.60.6.506.
  8. Schwartz J., Morrison J.L. Impact and mechanisms of fetal physiological programming. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005; 288(1):R11-5. https://dx.doi.org/10.1152/ajpregu.00698.2004.
  9. Петров Ю.А., Купина А.Д. Фетальное программирование – способ предупреждения заболеваний во взрослом возрасте. Медицинский cовет. 2020; 13: 50-6. https://dx.doi.org/10.21518/2079-701X-2020-13-50-56. [Petrov Yu.A., Kupina A.D. Fetal programming is a way to prevent diseases in adulthood (literature review). Meditsinskiy sovet/Medical Council. 2020; 13: 50-6. (in Russian) https://dx.doi.org/10.21518/2079-701X-2020-13-50-56.
  10. Fall C.H.D., Kumaran K. Metabolic programming in early life in humans. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2019; 374(1770): 20180123.https://dx.doi.org/10.1098/rstb.2018.0123.
  11. Fernandez-Twinn D.S., Hjort L., Novakovic B., Ozanne S.E., Saffery R. Intrauterine programming of obesity and type 2 diabetes. Diabetologia. 2019; 62(10): 1789-801. https://dx.doi.org/10.1007/s00125-019-4951-9.
  12. Marciniak A., Patro-Małysza J., Kimber-Trojnar Ż., Marciniak B., Oleszczuk J., Leszczyńska-Gorzelak B. Fetal programming of the metabolic syndrome. Taiwan. J. Obstet. Gynecol. 2017; 56(2): 133-8. https://dx.doi.org/10.1016/j.tjog.2017.01.001.
  13. Макаров И.О., Юдина Е.В., Боровкова Е.И. Задержка роста плода. Врачебная тактика. Учебное пособие. 3-е изд. М.: МЕДпресс-информ; 2016. 56с. [Makarov I.O., Yudina E.V., Borovkova E.I. Fetal growth retardation. medical tactics. Tutorial. 3rd ed. Moscow: MEDpress-inform; 2012. 56 p. (in Russian)].
  14. Perrone S., Santacroce A., Picardi A., Buonocore G. Fetal programming and early identification of newborns at high risk of free radical-mediated diseases. World J. Clin. Pediatr. 2016; 5(2): 172-81. https://dx.doi.org/10.5409/wjcp.v5.i2.172.
  15. Железова М.Е., Зефирова Т.П., Канюков С.С. Задержка роста плода: современные подходы к диагностике и ведению беременности. Практическая медицина. 2019; 17(4): 8-14. https://dx.doi.org/10.32000/2072-1757-2019-4-8-14. [Zhelezova M.E., Zefirova T.P., Kanyukov S.S. Fetal growth retardation: modern approaches to the diagnosis and management of pregnancy. Practical medicine. 2019; 17(4): 8-14. (in Russian)]. https://dx.doi.org/10.32000/2072-1757-2019-4-8-14.
  16. Bendix I., Miller S.L., Winterhager E. Editorial: causes and consequences of intrauterine growth restriction. Front. Endocrinol. (Lausanne). 2020; 11: 205. https://dx.doi.org/10.3389/fendo.2020.00205.
  17. von Beckerath A.K., Kollmann M., Rotky-Fast C., Karpf E., Lang U., Klaritsch P. Perinatal complications and long-term neurodevelopmental outcome of infants with intrauterine growth restriction. Am. J. Obstet. Gynecol. 2013; 208(2): 130.e1-6. https://dx.doi.org/10.1016/j.ajog.2012.11.014.
  18. Липатов И.С., Тезиков Ю.В., Амосов М.С., Зуморина Э.М. Клинико-патогенетические варианты задержки роста плода различных сроков манифестации. Медицинский совет. 2021; 3: 54-65. https://dx.doi.org/10.21518/2079-701X-2021-3-54-65. [Lipatov I.S., Tezikov Yu.V., Amosov M.S., Zumorina E.M. Clinical and pathogenetic variants of fetal growth retardation of different periods of manifestation. Meditsinskiy sovet/Medical Council. 2021; (3): 54-65. (in Russian)]. https://dx.doi.org/10.21518/2079-701X-2021-3-54-65.
  19. Стрижаков А.Н., Мирющенко М.И., Игнатко И.В., Попова Н.Г., Флорова В.С., Кузнецов А.С. Прогнозирование синдрома задержки роста плода у беременных высокого риска. Акушерство и гинекология. 2017; 7: 34-44. https://dx.doi.org/10.18565/aig.2017.7.34-44. [Strizhakov A.N., Miryushchenko M.M., Ignatko I.V., Popova N.G., Florova V.S., Kuznetsov A.S.Prediction of fetal growth restriction in high-risk pregnant women. Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2017; 7: 34-44.(in Russian)]. https://dx.doi.org/10.18565/aig.2017.7.34-44.
  20. Wan L., Luo K., Chen P. Mechanisms underlying neurologic Injury in intrauterine growth restriction. J. Child Neurol. 2021; 36(9): 776-84.https://dx.doi.org/10.1177/0883073821999896.
  21. Морозова А.Ю., Милютина Ю.П., Ковальчук-Ковалевская О.В., Арутюнян А.В., Евсюкова И.И. Содержание нейронспецифической енолазы и мозгового нейротрофического фактора в пуповинной крови доношенных новорожденных с задержкой внутриутробного развития. Журнал акушерства и женских болезней. 2019; 68(1): 29-36. https://dx.doi. org/10.17816/JOWD68129-36. [Morozova A.Yu., Milyutina Yu.P., Kovalchuk-Kovalevskaya O.V., Arutyunyan A.V., Evsyukova I.I. Content of neuron-specific enolase and brain-derived neurotrophic factor in cord blood of full-term newborns with intrauterine growth retardation. J. Obstet. Women’s Dis. 2019; 68(1): 29-36. (in Russian)]. https://dx.doi.org/10.17816/JOWD68129-36.
  22. Visentin S., Grumolato F., Nardelli G.B., Di Camillo B., Grisan E., Cosmi E. Early origins of adult disease: low birth weight and vascular remodeling. Atherosclerosis. 2014; 237(2): 391-9. https://dx.doi.org/10.1016/j.atherosclerosis.2014.09.027.
  23. Murray D.M. Biomarkers in neonatal hypoxic-ischemic encephalopathy-Review of the literature to date and future directions for research. Handb. Clin. Neurol. 2019; 162: 281-93. https://dx.doi.org/10.1016/B978-0-444-64029-1.00013-8.
  24. Colson A., Sonveaux P., Debiève F., Sferruzzi-Perri A.N. Adaptations of the human placenta to hypoxia: opportunities for interventions in fetal growth restriction. Hum. Reprod. Update. 2021; 27(3): 531-69. https://dx.doi.org/10.1093/humupd/dmaa053.
  25. Dudink I., Hüppi P.S., Sizonenko S.V., Castillo-Melendez M., Sutherland A.E., Allison B.J., Miller S.L. Altered trajectory of neurodevelopment associated with fetal growth restriction. Exp. Neurol. 2022; 347: 113885. https://dx.doi.org/10.1016/j.expneurol.2021.113885.
  26. Jia Y., Jia X., Xu H., Gao L., Wei C., Li Y. et al. Blood plasma metabolic profile of newborns with hypoxic-ischaemic encephalopathy by GC-MS. Biomed. Res. Int. 2021; 2021: 6677271. https://dx.doi.org/10.1155/2021/6677271.
  27. Zhang Y.J. Recent research on the influence of intrauterine growth restriction on the structure and function of the nervous system. Zhongguo Dang Dai Er Ke Za Zhi. 2021; 23(11): 1184-9. https://dx.doi.org/10.7499/j.issn.1008-8830.2108044.
  28. Briana D.D., Malamitsi-Puchner A. Developmental origins of adult health and disease: The metabolic role of BDNF from early life to adulthood. Metabolism. 2018; 81: 45-51. https://dx.doi.org/10.1016/j.metabol.2017.11.019.
  29. Marosi K., Mattson M.P. BDNF mediates adaptive brain and body responses to energetic challenges. Trends Endocrinol. Metab. 2014; 25(2): 89-98.https://dx.doi.org/10.1016/j.tem.2013.10.006.
  30. Massaro A.N., Wu Y.W., Bammler T.K., Comstock B., Mathur A., McKinstry R.C. et al. Plasma biomarkers of brain injury in neonatal hypoxic-ischemic encephalopathy. J. Pediatr. 2018; 194: 67-75. https://dx.doi.org/10.1016/j.jpeds.2017.10.060.
  31. Pathare-Ingawale P., Chavan-Gautam P. The balance between cell survival and death in the placenta: Do neurotrophins have a role? Syst. Biol. Reprod. Med. 2022; 68(1): 3-12. https://dx.doi.org/10.1080/19396368.2021.1980132.
  32. Chaparro-Huerta V., Flores-Soto M.E., Merin Sigala M.E., Barrera de León J.C., Lemus-Varela M.L., Torres-Mendoza B.M., Beas-Zárate C. Proinflammatory cytokines, enolase and S-100 as early biochemical indicators of hypoxic-ischemic encephalopathy following perinatal asphyxia in newborns. Pediatr. Neonatol. 2017; 58(1): 70-6. https://dx.doi.org/10.1016/j.pedneo.2016.05.001.
  33. Ding Y.X., Cui H. The brain development of infants with intrauterine growth restriction: role of glucocorticoids. Horm. Mol. Biol. Clin. Investig. 2019; 39(1). https://dx.doi.org/10.1515/hmbci-2019-0016.
  34. Gilchrist C., Cumberland A., Walker D., Tolcos M. Intrauterine growth restriction and development of the hippocampus: implications for learning and memory in children and adolescents. Lancet Child Adolesc. Health. 2018; 2(10): 755-64. https://dx.doi.org/10.1016/S2352-4642(18)30245-1.
  35. Sacchi C., O’Muircheartaigh J., Batalle D., Counsell S.J., Simonelli A., Cesano M. et al. Neurodevelopmental outcomes following intrauterine growth restriction and very preterm birth. J. Pediatr. 2021; 238: 135-144.e10. https://dx.doi.org/10.1016/j.jpeds.2021.07.002.
  36. Alkholy U.M., Abdalmonem N., Zaki A., Ali Y.F., Mohamed S.A., Abdelsalam N.I. et al. Early predictors of brain damage in full-term newborns with hypoxic ischemic encephalopathy. Neuropsychiatr. Dis. Treat. 2017; 13: 2133-9.https://dx.doi.org/10.2147/NDT.S144225.
  37. Sacchi C., De Carli P., Mento G., Farroni T., Visentin S., Simonelli A. Socio-emotional and cognitive development in intrauterine growth restricted (IUGR) and typical development infants: early interactive patterns and underlying neural correlates. Rationale and methods of the study. Front. Behav. Neurosci. 2018; 12: 315. https://dx.doi.org/10.3389/fnbeh.2018.00315.
  38. Fernandez-Twinn D.S., Constancia M., Ozanne S.E. Intergenerational epigenetic inheritance in models of developmental programming of adult disease. Semin. Cell Dev. Biol. 2015; 43: 85-95. https://dx.doi.org/10.1016/j.semcdb.2015.06.006.
  39. Shah D.K., Ponnusamy V., Evanson J., Kapellou O., Ekitzidou G., Gupta N. et al. Raised plasma neurofilament light protein levels are associated with abnormal MRI outcomes in newborns undergoing therapeutic hypothermia. Front. Neurol. 2018; 9: 86. https://dx.doi.org/10.3389/fneur.2018.00086.
  40. Кан Н.Е., Тютюнник В.Л., Хачатрян З.В., Садекова А.А., Красный А.М. Прогностическая значимость определения внеклеточной фетальной ДНК в плазме крови при задержке роста плода. Акушерство и гинекология. 2021; 6: 60-5. https://dx.doi.org/10.18565/aig.2021.6.60-65. [Kan N.E., Tyutyunnik V.L., Khachatryan Z.V., Sadekova A.A., Krasnyi A.M. Prognostic value of definition cell-free fetal DNA in blood plasma with intrauterine growth retardation. Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2021; 6: 60-5. (in Russian)]. https://dx.doi.org/10.18565/aig.2021.6.60-65.
  41. Kesavan K., Devaskar S.U. Intrauterine growth restriction: postnatal monitoring and outcomes. Pediatr. Clin. North Am. 2019; 66(2): 403-23. https://dx.doi.org/10.1016/j.pcl.2018.12.009.
  42. Oke S.L., Hardy D.B. The role of cellular stress in intrauterine growth restriction and postnatal dysmetabolism. Int. J. Mol. Sci. 2021; 22(13): 6986.https://dx.doi.org/10.3390/ijms22136986.

Received 13.07.2022

Accepted 13.09.2022

About the Authors

Natalia E. Kan, Professor, Dr. Med. Sci., Deputy Director for Science, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of the Russia, +7(926)220-86-55, kan-med@mail.ru, Researcher ID: B-2370-2015, SPIN-cod: 5378-8437, Authors ID: 624900, Scopus Author ID: 57008835600, https://orcid.org/0000-0001-5087-5946. 117997, Russia, Moscow, Ac. Oparina str., 4.
Anastasia A. Leonova, postgraduate student, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of the Russia, +7(937)453-54-27, nastena27-03@mail.ru, https://orcid.org/0000-0001-6707-3464, 117997, Russia, Moscow, Ac. Oparina str. 4.
Victor L. Tyutyunnik, Professor, Dr. Med. Sci., Leading Researcher at the Research and Development Service, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of the Russia, +7(903)969-50-41, tioutiounnik@mail.ru, Researcher ID: B-2364-2015, SPIN-cod: 1963-1359, Authors ID: 213217, Scopus Author ID: 56190621500, https://orcid.org/0000-0002-5830-5099, 117997, Russia, Moscow, Ac. Oparina str., 4.
Zarine V. Khachatryan, postgraduate student, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of the Russia, +7(909)656-24-56, z.v.khachatryan@gmail.com, 117997, Russia, Moscow, Ac. Oparina str. 4.

Authors’ contributions: Kan N.E., Leonova A.A., Tyutyunnik V.L., Khachatryan Z.V. – concept and development of the design of the investigation, obtaining the data to be analyzed, collection of publications, processing and analysis of material on the topic of the article, writing the text of the manuscript, editing the article.
Conflicts of interest: The authors declare that there are no conflicts of interest.
Funding: The investigation has not been sponsored.
For citation: Kan N.E., Leonova A.A., Tyutyunnik V.L., Khachatryan Z.V.
Features of neurogenesis in fetal growth restriction
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2022; 11: 24-30 (in Russian)
https://dx.doi.org/10.18565/aig.2022.11.24-30

Similar Articles

By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.