Serotonin and cyclic sleep organization in full-term newborn infants with intrauterine growth retardation

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BACKGROUND: The high frequency of neurological and mental diseases in children who had intrauterine retardatiojn development indicates the need to study specific markers of disorders of fetal brain functional development, in particular, the state of the serotonergic system, which plays a key role in the morpho-functional development of the brain in early ontogenesis.

AIM: To study the content of serotonin in full-term newborns with intrauterine development delay in comparison with quantitative and qualitative characteristics of sleep.

MATERIALS AND MЕTHODS: The main group consisted of 26 newborns, whose intrauterine development took place in conditions of chronic placental insufficiency, which led to the formation of an asymmetric form of intrauterine retardatiojn development. The control group consisted of 72 healthy newborns from healthy mothers without pregnancy complications. Children of each group are divided into three subgroups depending on gestational age: I — 37, II — 38, III — 39–40 weeks. In all children, 7–12 hours after birth, an electropoligram of sleep was recorded (an electroencephalograph of the company “Mizar”, Russia) and its quantitative and qualitative analyses were carried out, highlighting the orthodox, paradoxical phase and undifferentiated state. The serotonin content was determined in platelet-rich plasma of blood from the umbilical cord vein after birth, as well as in a platelet suspension prepared from venous blood taken on the first day of life. The content of serotonin in platelets was judged by the indicator obtained by dividing the amount of serotonin in the platelet suspension by the platelet level. The amount of serotonin was determined by high-performance liquid chromatography with electrochemical detection. Statistical analysis was performed using the Statistica 6 program (Statsoft Inc, USA).

RESULTS: We report here a low content of serotonin in platelet-rich plasma and platelets of newborns with intrauterine growth retardation and the absence of its normal increase in weeks 37–39 of intrauterine development, as well as a violation of the genetic programming for the sleep-wake cycle organization.

CONCLUSIONS: Assessment of the serotonin-producing system of the brain in comparison with the newborn sleep pattern can serve as a diagnostic marker of brain damage and substantiate the need for timely application of neuroprotection.

作者简介

Natalia Zvereva

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: tata-83@bk.ru
ORCID iD: 0000-0002-1220-1147
俄罗斯联邦, Saint Petersburg

Yuliya Milyutina

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: milyutina1010@mail.ru
ORCID iD: 0000-0003-1951-8312
SPIN 代码: 6449-5635
Scopus 作者 ID: 24824836300
Researcher ID: AAE-6182-2019

Cand. Sci. (Biol.)

俄罗斯联邦, Saint Petersburg

Alexander Arutjunyan

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: alexarutiunjan@gmail.com
ORCID iD: 0000-0002-0608-9427
Scopus 作者 ID: 6506430871

Dr. Sci. (Biol.), Professor, Honored Scientist of the Russian Federation

俄罗斯联邦, Saint Petersburg

Inna Evsyukova

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

编辑信件的主要联系方式.
Email: eevs@yandex.ru
ORCID iD: 0000-0003-4456-2198
SPIN 代码: 4444-4567

MD, Dr. Sci. (Med.), Professor

俄罗斯联邦, Saint Petersburg

参考

  1. Öztürk HNO, Türker PF. Fetal programming: could intrauterin life affect health status in adulthood? Obstet Gynecol Sci. 2021;64(6):473–483. doi: 10.5468/ogs.21154
  2. Olfson M, Blanco C, Wang S, et al. National trends in the mental health care of children, adolescents, and adults by office-based physicians. JAMA Psychiatry. 2014;71(1):81–90. doi: 10.1001/jamapsychiatry.2013.3074
  3. Gumusoglu SB, Chilukuri ASS, Santillan DA, et al. Neurodevelopmental outcomes of prenatal preeclampsia exposure. Trends Neurosci. 2020;43(4):253–268. doi: 10.1016/j.tins.2020.02.003
  4. Evsyukova II. Cerebral disorders and consequences of delayed intrauterine development of a full-term baby: the role of oxidative stress and melatonin. Human Physiology. 2022;48(3):340–345. (In Russ.). doi: 10.31857/S0131164622030055
  5. Morris G, Fernandes BS, Puri BK, et al. Leaky brain in neurological and psychiatric disorders: drivers and consequences. Aust N Z J Psychiatry. 2018;52(10):924–948. doi: 10.1177/0004867418796955
  6. Wang Y, Fu W, Liu J. Neurodevelopment in children with intrauterine growth restriction: adverse effects and interventions. J Matern Fetal Neonatal Med. 2016;29(4):660–668. doi: 10.3109/14767058.2015.1015417
  7. Nardozza LM, Caetano AC, Zamarian AC, et al. Fetal growth restriction: current knowledge. Arch Gynecol Obstet. 2017;295(5):1061–1077. doi: 10.1007/s00404-017-4341-9
  8. 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;9. doi: 10.3389/fphys.2018.01278
  9. 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. JAMA Pediatr. 2020;174(8):772–781. doi: 10.1001/jamapediatrics.2020.1097
  10. Korkalainen N, Partanen L, Räsänen J, et al. Fetal hemodynamics and language skills in primary school-aged children with fetal growth restriction: a longitudinal study. Early Hum Dev. 2019;134:34–40. doi: 10.1016/j.earlhumdev.2019.05.019
  11. Baschat AA. Neurodevelopment after fetal growth restriction. Fetal Diagn Ther. 2014;36(2):136–142. doi: 10.1159/000353631
  12. Armengaud JB, Yzydorczyk C, Siddeek B, et al. Intrauterine growth restriction: clinical consequences on health and disease at adulthood. Reprod Toxicol. 2021;99:168–176. doi: 10.1016/j.reprotox.2020.10.005
  13. Kepser LJ, Homberg JR. The neurodevelopmental effects of serotonin: a behavioural perspective. Behav Brain Res. 2015;277:3–13. doi: 10.1016/j.bbr.2014.05.022
  14. Sidorova IS, Nikitina NA, Unanyan AL, et al. Development of the human fetal brain and the influence of prenatal damaging factors on the main stages of neurogenesis. Russian Bulletin of Obstetrician-Gynecologist. 2022;22(1):35-44. (In Russ.). doi: 10.17116/rosakush20222201135
  15. Jenkins TA, Nguyen JC, Polglaze KE, et al. Influence of tryptophan and serotonin on mood and cognition with a possible role of the gut-brain axis. Nutrients. 2016;8(1). doi: 10.3390/nu8010056
  16. Evsyukova II. The cyclic organization of sleep in early ontogenesis in different conditions of intrauterine fetus development. Russian Journal of Physiology. 2013;99(2):166–174.
  17. Oreland L, Hallman J. Blood platelets as a peripheral marker for the central serotonin system. Nord J Psychiatry. 1989;43(20):43–51. doi: 10.3109/08039488909100833
  18. Anderson GM, Czarkowski K, Ravski N, et al. Platelet serotonin in newborns and infants: ontogeny, heritability, and effect of in utero exposure to selective serotonin reuptake inhibitors. Pediatr Res. 2004;56(3):418–422. doi: 10.1203/01.PDR.0000136278.23672.A0
  19. Hazra M, Benson S, Sandler M. Blood 5-hydroxytryptamine levels in the newborn. Arch Dis Child. 1965;40(213):513–515. doi: 10.1136/adc.40.213.513
  20. Evsyukova II, Koval’chuk-Kovalevskaya OV, Maslyanyuk NA, et al. Osobennosti tsiklicheskoi organizatsii sna i produktsii melatonina u donoshennykh novorozhdennykh detei s zaderzhkoi vnutriutrobnogo razvitiya. Fiziologiya cheloveka. 2013;39(6):617–624. doi: 10.7868/S0131164613060040
  21. Ryukert EN. Osobennosti funktsionirovaniya serotoninergicheskoy i opiodnoy sistem u detey pervykh mesyatsev zhizni s gipoksicheski ishemicheskim porazheniem TsNS, vzaimosvyaz’ s temperamentom. [dissertation abstract]. Moscow; 2007. [cited 2022 Nov 12]. Available from: https://www.dissercat.com/content/osobennosti-funktsionirovaniya-serotoninergicheskoi-i-opiodnoi-sistem-u-detei-pervykh-mesyat
  22. Berezhanskaya SB, Luk’yanova EA. Level of serum biogenous amines in children with perinatal hypoxic-ishemic and traumatic central nervous system lesion. Pediatriya. 2002;81(1):23–26.
  23. Miheeva IG, Ryukert EN, Brusov OS, et al. Serum serotonin level in neonates with hypoxic ischemic CNS. Pediatriya. Zhurnal im. G.N. Speranskogo. 2008;87(1):40–44.
  24. Gall V, Kosec V, Vranes HS, et al. Platelet serotonin concentration at term pregnancy and after birth: physiologic values for Croatian population. Coll Antropol. 2011;35(3):715–718.
  25. Furs VV, Doroshenko EM. Nekotorye pokazateli obmena triptofana pri fiziologicheski protekayushchei beremennosti. Zhurnal Grodnenskogo gosudarstvennogo meditsinskogo universiteta. 2011;(4):36–38. (In Russ.)
  26. Field T, Diego M, Hernandez-Reif M, et al. Prenatal serotonin and neonatal outcome: brief report. Infant Behav Dev. 2008;31(2):316–320. doi: 10.1016/j.infbeh.2007.12.009
  27. Rosenfeld CS. Placental serotonin signaling, pregnancy outcomes, and regulation of fetal brain development. Biol Reprod. 2020;102(3):532–538. doi: 10.1093/biolre/ioz204
  28. Kliman HJ, Quaratella SB, Setaro AC, et al. Pathway of maternal serotonin to the human embryo and fetus. Endocrinology. 2018;159(4):1609–1629. doi: 10.1210/en.2017-03025
  29. Balija M, Bordukalo-Niksic T, Mokrovic G, et al. Serotonin level and serotonin uptake in human platelets: a variable interrelation under marked physiological influences. Clin Chim Acta. 2011;412(3–4):299–304. doi: 10.1016/j.cca.2010.10.024
  30. Brenner B, Harney JT, Ahmed BA, et al. Plasma serotonin levels and the platelet serotonin transporter. J Neurochem. 2007;102(1):206–215. doi: 10.1111/j.1471-4159.2007.04542.x
  31. Baković P, Kesić M, Perić M, et al. Differential serotonin uptake mechanisms at the human maternal-fetal interface. Int J Mol Sci. 2021;22(15). doi: 10.3390/ijms22157807
  32. Forstner D, Guettler J, Gauster M. Changes in maternal platelet physiology during gestation and their interaction with trophoblasts. Int J Mol Sci. 2021;22(19). doi: 10.3390/ijms221910732
  33. Mercado CP, Kilic F. Molecular mechanisms of SERT in platelets: regulation of plasma serotonin levels. Mol Interv. 2010;10(4):231–241. doi: 10.1124/mi.10.4.6
  34. Ye W, Xie L, Li C, et al. Impaired development of fetal serotonergic neurons in intrauterine growth restricted baboons. J Med Primatol. 2014;43(4):284–287. doi: 10.1111/jmp.12116
  35. Laurent L, Deroy K, St-Pierre J, et al C. Human placenta expresses both peripheral and neuronal isoform of tryptophan hydroxylase. Biochimie. 2017;140:159–165. doi: 10.1016/j.biochi.2017.07.008
  36. Bonnin A, Goeden N, Chen K, et al. A transient placental source of serotonin for the fetal forebrain. Nature. 2011;472(7343):347–350. doi: 10.1038/nature09972
  37. Sundström E, Kölare S, Souverbie F, et al. Neurochemical differentiation of human bulbospinal monoaminergic neurons during the first trimester. Brain Res Dev Brain Res. 1993;75(1):1–12. doi: 10.1016/0165-3806(93)90059-j
  38. Verney C, Lebrand C, Gaspar P. Changing distribution of monoaminergic markers in the developing human cerebral cortex with special emphasis on the serotonin transporter. Anat Rec. 2002;267(2):87–93. doi: 10.1002/ar.10089
  39. Ranzil S, Walker DW, Borg AJ, et al. The relationship between the placental serotonin pathway and fetal growth restriction. Biochimie. 2019;161:80–87. doi: 10.1016/j.biochi.2018.12.016
  40. Yang CJ, Tan HP, Du YJ. The developmental disruptions of serotonin signaling may involved in autism during early brain development. Neuroscience. 2014;267:1–10. doi: 10.1016/j.neuroscience.2014.02.021
  41. Brummelte S, Mc Glanaghy E, Bonnin A, et al. Developmental changes in serotonin signaling: Implications for early brain function, behavior and adaptation. Neuroscience. 2017;342:212–231. doi: 10.1016/j.neuroscience.2016.02.037
  42. Nasyrova DI, Sapronova AYa, Balbashev AV, et al. Razvitie tsentral’noi i perifericheskoi serotonin-produtsiruyushchikh sistem u krys v ontogeneze. Zhurnal evolyutsionnoi biokhimii i fiziologii. 2009;45(1):68–74. (In Russ.)
  43. Roland CS, Hu J, Ren CE, et al. Morphological changes of placental syncytium and their implications for the pathogenesis of preeclampsia. Cell Mol Life Sci. 2016;73(2):365–376. doi: 10.1007/s00018-015-2069-x
  44. Gumusoglu S, Scroggins S, Vignato J, et al. The serotonin-immune axis in preeclampsia. Curr Hypertens Rep. 2021;23(7):37. doi: 10.1007/s11906-021-01155-4
  45. Liu D, Gao Q, Wang Y, et al. Placental dysfunction: the core mechanism for poor neurodevelopmental outcomes in the offspring of preeclampsia pregnancies. Placenta. 2022;126:224–232. doi: 10.1016/j.placenta.2022.07.014
  46. Rosenfeld CS. The placenta-brain-axis. J Neurosci Res. 2021;99(1):271–283. doi: 10.1002/jnr.24603
  47. Shallie PD, Naicker T. The placenta as a window to the brain: a review on the role of placental markers in prenatal programming of neurodevelopment. Int J Dev Neurosci. 2019;73:41–49. doi: 10.1016/j.ijdevneu.2019.01.003
  48. Chrzanowska B, Wańkowicz B, Prokopczyk J. Serotonin concentration in the rat fetal brain in experimental intrauterine dystrophy. Probl Med Wieku Rozwoj. 1984;13:193–197.
  49. Ye X, Shin BC, Baldauf C, et al. Developing brain glucose transporters, serotonin, serotonin transporter, and oxytocin receptor expression in response to early-life hypocaloric and hypercaloric dietary, and air pollutant exposures. Dev Neurosci. 2021;43(1):27–42. doi: 10.1159/000514709
  50. Homberg J, Mudde J, Braam B, et al. Blood pressure in mutant rats lacking the 5-hydroxytryptamine transporter. Hypertension. 2006;48(6):e115–e117. doi: 10.1161/01.HYP.0000246306.61289.d8
  51. Alenina N, Kikic D, Todiras M, et al. Growth retardation and altered autonomic control in mice lacking brain serotonin. Proc Natl Acad Sci USA. 2009;106(25):10332–10337. doi: 10.1073/pnas.0810793106
  52. Hanswijk SI, Spoelder M, Shan L, et al. Gestational factors throughout fetal neurodevelopment: the serotonin link. Int J Mol Sci. 2020;21(16). doi: 10.3390/ijms21165850
  53. Sato K. Placenta-derived hypo-serotonin situations in the developing forebrain cause autism. Med Hypotheses. 2013;80(4):368–372. doi: 10.1016/j.mehy.2013.01.002
  54. Sodhi MS, Sanders-Bush E. Serotonin and brain development. Int Rev Neurobiol. 2004;59:111–174. doi: 10.1016/S0074-7742(04)59006-2
  55. Peirano P, Algarín C, Uauy R. Sleep-wake states and their regulatory mechanisms throughout early human development. J Pediatr. 2003;143(4):S70–S79. doi: 10.1067/s0022-3476(03)00404-9
  56. Uchitel J, Vanhatalo S, Austin T. Early development of sleep and brain functional connectivity in term-born and preterm infants. Pediatr Res. 2022;91(4):771–786. doi: 10.1038/s41390-021-01497-4

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2. Fig. 1. Serotonin content in platelets of healthy newborns and newborns with intrauterine growth retardation. * p < 0.05; ** p < 0.01

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