Maternal nutrition is a substantial part of the developmental or metabolic programming of newborns (Koletzko et al., 2018, 2019), with short- and long-term consequences on health and a relevant impact on fetoplacental growth patterns (Morrison and Regnault, 2016). Synaptic and intrinsic homeostasis cooperate to optimize single neuron doi: 10.2165/00148581-200305090-00004, McCarthy, J. J., Leamon, M. H., Finnegan, L. P., and Fassbender, C. (2017). A decrease in the heart rate b. (2). doi: 10.1016/0002-9378(82)90616-0, Jonsson, M., Nordn-Lindeberg, S., Ostlund, I., and Hanson, U. Lastly, early pain reactivity measured through HRV in alcohol-exposed newborns seems to be blunted, suggesting different responsiveness to environmental stimuli even after birth (Oberlander et al., 2010). doi: 10.7556/jaoa.2018.108, Snijder, C. A., Roeleveld, N., te Velde, E., Steegers, E. A. P., Raat, H., Hofman, A., et al. Mayo Clin. 9, 17641773. Occup. Placental microbial colonization and its association with pre-eclampsia. 78, 11031107, Goldenberg, R. L., Culhane, J. F., Iams, J. D., and Romero, R. (2008). When they suspect fetal hypoxia, they must determine the delivery timing to prevent serious consequences for your newborn. Epidemiology 19, 851859. Biol. 71, 313321. Reprod. doi: 10.1148/rg.2015150092, Rou, G., Samoilescu, G., Rau, M. C., and Baltag, O. (1991). Fetal Neonatal Med. Immunol. 24, 474481. These processes can be implemented through cell autonomous or intercellular signaling. As the 3rd trimester advances, specific nociceptive event-related potentials in the brain increasingly develop until 3537 WGA (Verriotis et al., 2016). 55, 1721. Lastly, this feto-maternal pro-inflammatory state could interfere with the set point of the fetal vagal regulatory system through CAP dysregulation, thus impairing fetal intestinal permeability and integrity (Garzoni et al., 2013). Am. 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O. 81, 909917. 11 Articles, This article is part of the Research Topic, The Fetal ANS Development: The Search of Critical Windows, The Environmental Factors Affecting the ANS Development, Clinical Implications for the Management of Fetuses and Newborns, https://doi.org/10.3389/fnins.2021.721605, Committee on Fetus and Newborn and Section on Anesthesiology and Pain Medicine, 2016, Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, 1996, http://www.ncbi.nlm.nih.gov/books/NBK470566/, http://www.ncbi.nlm.nih.gov/books/NBK539789/, https://embryology.med.unsw.edu.au/embryology/index.php/Neural_System_Development, http://www.ncbi.nlm.nih.gov/books/NBK513398/, http://www.ncbi.nlm.nih.gov/books/NBK544290/, Creative Commons Attribution License (CC BY). Integr. The deprivation of the REM sleep phase during uterine life can lead to altered cortical and brainstem development and to the supersensitivity to the noradrenaline of the pyramidal cells in the hippocampus, impairing the receptors' sensitivity (Mirmiran et al., 2003). Brief report: can a composite heart rate variability biomarker shed new insights about autism spectrum disorder in school-aged children? ACOG Practice Bulletin No. The production of testosterone in male fetuses begins during the 2nd month of pregnancy and reaches the maximum in the 2nd trimester (Chung and Auger, 2013), just before when vagal tone starts to rise (Mulkey and du Plessis, 2019). 54, 3437. An update on the controversies of tocolytic therapy for the prevention of preterm birth. Clark SL, Hamilton EF, Garite TJ, Timmins A, Warrick PA, Smith S. The limits of electronic fetal heart rate monitoring in the prevention of neonatal metabolic acidemia. Am J Obstet Gynecol. J. Clin. doi: 10.1007/BF00315698, Multon, O., Senat, M.-V., Minoui, S., Hue, M.-V., Frydman, R., and Ville, Y. Intervention minimizing preterm infants' exposure to NICU light and noise. 16, 509517. 2012 Sep; 207(3):206. e1-8. Selye, H. (1950). Despite this evidence, other authors claim that placental microbiome does not existthe aforementioned results would be just due to methodological errorsor that there is only extremely low biomass, probably leading to minor clinical effects (Lauder et al., 2016; Leiby et al., 2018; Kuperman et al., 2020; Parris et al., 2021). Child. (2006). While intracellular Ca 2+ has long been hypothesized to be a feedback control signal, the molecular machinery enabling a network-wide homeostatic response remains largely unknown. (2020). Newborns can also be subject to EMFs, from the incubator or the care unit environment. The fetuses, moreover, appear to have an increased risk of preterm birth (Morrison et al., 2005; Suri et al., 2007; Oyebode et al., 2012) and poor neonatal adaptation syndrome (Lattimore et al., 2005; Sivojelezova et al., 2005). doi: 10.4103/jdmimsu.jdmimsu_194_20, Sheng, J. Although there are not evident depressive effects on non-stress test reactivity or variability in the case of daily opioid use for chronic pain (Brar et al., 2020), the current guidelines recommend a prescription at the lowest effective dose (Ray-Griffith et al., 2018). In contrast, we are entering a stretch of Perfect Weather with the convergence of conditions collectively conducive to advancing the science of electronic fetal heart rate interpretation in actual clinical practice. (2011). (2017). 1996;8(3):471-82. Fletcher AJ, Gardner DS, Edwards CM, Fowden AL, Giussani DA. Even if the light-dark cycle does not seem to significantly affect the fetal circadian rhythm, there are age-dependent fHRV patterns after transabdominal fetal stimulation with halogen light, similarly to the VAS (Peleg and Goldman, 1980), which seem increasingly definite in the later stages of pregnancy, when the fetal optic pathways and ANS control on the cardiac activity reach maturity (Thanaboonyawat et al., 2006). J. Womens Health 10, 153164. University of Erlangen Nuremberg, Germany. Dev. Hillman, N. H., Kallapur, S. G., and Jobe, A. H. (2012). Ulmer Yaniv, A., Salomon, R., Waidergoren, S., Shimon-Raz, O., Djalovski, A., and Feldman, R. (2021). Rep. 9:11020. doi: 10.1038/s41598-019-47306-1, Mulkey, S. B., Kota, S., Swisher, C. B., Hitchings, L., Metzler, M., Wang, Y., et al. doi: 10.1016/j.ajog.2005.05.012, Sklerov, M., Dayan, E., and Browner, N. (2019). Res. Fetal heart rate variability responsiveness to maternal stress, non-invasively detected from maternal transabdominal ECG. Does reduction of amniotic fluid affect fetal movements? Am. Nevertheless, neonatal intensive care units have improved so much in the years that babies born as early as 2022 weeks can survive if properly treated (Moore et al., 2016). Pregnancy-related pain. Am J Obstet Gynecol. 315, R1123R1153. Behav. J. Clin. 1975 Feb;45(2):142-6. doi: 10.1016/j.biopsycho.2005.08.008, Bekedam, D. J., Mulder, E. J. H., Snijders, R. J. M., and Visser, G. H. A. When a doctor suspects fetal hypoxia, they must determine the delivery timing to prevent serious consequences for your newborn. A clinical perspective of necrotizing enterocolitis: past, present, and future. Senat, M. V., Minoui, S., Multon, O., Fernandez, H., Frydman, R., and Ville, Y. Ther. The hypothalamic-pituitary-adrenal axis: development, programming actions of hormones, and maternal-fetal interactions. Can. Ter. Biol. That is, the machine (computer) learns from the actual data. (2020). Hum. A decrease in the heart rate The vagus nerve begins maturation 26 to 28 weeks. 39, 769771. Aging 78, 117. doi: 10.1042/BSR20171234, Zizzo, A. R., Kirkegaard, I., Hansen, J., Uldbjerg, N., and Mlgaard, H. (2020). The placenta harbors a unique microbiome. This detects changes in the normal FHR pattern at the time of labor, reassuring your obstetrician if it's safe to proceed. (2020). (2020). J. Physiol. Two-year infant neurodevelopmental outcome after single or multiple antenatal courses of corticosteroids to prevent complications of prematurity. Health Dis. These modifications seem to last at worst 4 days after the first dose (Mulder et al., 2004; Verdurmen et al., 2013) and the influence on ANS modulation seems minor (Verdurmen et al., 2018; Noben et al., 2019). Changing heart rate is an important component of this mission but not the only one. Med. doi: 10.1152/jn.90680.2008, Kamitomo, M., Sameshima, H., Ikenoue, T., and Nishibatake, M. (2000). Neurotoxicol. Vasoconstriction is mediated through the -adrenergic receptors in liver, kidney, skin and gut, and vasodilation is mediated through adrenergic receptors in skeletal muscle. Machine learning model on heart rate variability metrics identifies asymptomatic toddlers exposed to Zika virus during pregnancy. Most of the medication administered to the mother during pregnancy can cross the placental barrier and reach the fetus. The discomforts of pregnancy. Microbiol. Summary of the finding of the present review regarding ANS development and HRV. Perinatal fluoxetine has enduring sexually differentiated effects on neurobehavioral outcomes related to social behaviors. (2018). Although the ANS and vagus nerve activity appear to have an endogenous circadian rhythm (Hilton et al., 2000; Kentish et al., 2013), with a pacemaker system that regulates its behavior regardless of sleep-awake states (Malpas and Purdie, 1990; Hilton et al., 2000), a circadian variation pattern of vagal activity can be recorded via HR variations. 1994 Jan;73(1):39-44. Gynaecol. As a result, several motor and neuroendocrine responses are induced: for instance, gastrointestinal and anabolic hormones such as cholecystokinin, insulin, and insulin-like growth factor-1 are released. Arch. Exposure to opioids prenatally could result in programming effects on stress response systems, leading also to long-term consequences (Conradt et al., 2018, 2019). (2016). Sampling rate of heart rate variability impacts the ability to detect acidemia in ovine fetuses near-term. Study Resources. This seems to be significantly influenced also by the combination between twins of different sexes, both in intrapair average and absolute differences (Tendais et al., 2015). Comp. For example, neurons and glial cells in the pancreas do not appear and the thymus loses both its vasculature and its capacity of developing T-cells (Hutchins et al., 2018). In some cases, insular injuries do not significantly change ANS tone; or, despite the effects on ANS tone, systemic hemodynamic meters (e.g., diastolic and systolic blood pressure) do not seem affected by brain injuries (Schneebaum Sender et al., 2017; Reich et al., 2019). J. Alterations in maternally perceived fetal movement and their association with late stillbirth: findings from the Midland and North of England stillbirth casecontrol study. Gynecol. doi: 10.1177/1054773812469223, Al Alam, D., Danopoulos, S., Grubbs, B., Ali, N. A. Brain. Eur. 47, 373386. 36, 23692378. Neural crest cells contribute an astrocyte-like glial population to the spleen. Studies on developmental neurology in the human fetus. Stimulating the vagus nerve typically produces: a. doi: 10.1111/aogs.12681, Haley, D. W., Handmaker, N. S., and Lowe, J. A dysregulation in CRH production, secondary to various maternal conditions, such as hypoxia, increased inflammatory cytokines and glucocorticoids, stress, preeclampsia, and eclampsia, may lead to altered neurodevelopmental patterns of these fetal structures (Allen, 2001; Bale, 2016; Sheng et al., 2020). The myths and physiology surrounding intrapartum decelerations: the critical role of the peripheral chemoreflex. The high immunoreactivity of the premature infants' gut could also lead to neurodevelopmental disorders (Cao et al., 2014). Res. Pediatrics 137:e20154271. Neurosci. Miljkovi, Z., Sabo, A., Stanulovi, M., Jakovljevi, V., and Gruji, I. doi: 10.1016/j.jcrc.2010.11.008, Mulder, E. J. H., Derks, J. Res. doi: 10.1016/j.ajog.2014.12.041, Aplin, J. D., Myers, J. E., Timms, K., and Westwood, M. (2020). Antenatal interventions based upon fetal surveillance of the daily opioid-exposed fetus: a descriptive analysis. doi: 10.1093/humrep/der437, Soma-Pillay, P., Nelson-Piercy, C., Tolppanen, H., and Mebazaa, A. Biol. A low APGAR (i.e., appearance, pulse, grimace, activity, and respiration) score, Greater chance of admission to the neonatal intensive care unit after delivery. The immune system and microbiome in pregnancy. Bacterial communities found in placental tissues are associated with severe chorioamnionitis and adverse birth outcomes. J. Perinat. When recurrent late decelerations are occurring the - Course Hero Front. Indeed, in preterm infants, both too high or too low oxygenation can be dangerous for the nervous system. doi: 10.1053/smrv.2002.0243, Montagna, A., and Nosarti, C. (2016). doi: 10.2307/1131844, Doyle, R. M., Harris, K., Kamiza, S., Harjunmaa, U., Ashorn, U., Nkhoma, M., et al. 8:948. doi: 10.3389/fnhum.2014.00948, Hoyer, D., Nowack, S., Bauer, S., Tetschke, F., Ludwig, S., Moraru, L., et al. An antenatal marker of neurodevelopmental outcomes in infants with congenital heart disease. According to a recent systematic analysis, FMs can affect the ANS as revealed through modifications in the time-domain and frequency-domain fHRV metrics. which intrinsic homeostatic response is the fetus demonstrating Maternal inflammation disrupts fetal neurodevelopment via increased placental output of serotonin to the fetal brain. doi: 10.1111/aji.12355, Simkin, J. E., Zhang, D., Stamp, L. A., and Newgreen, D. F. (2019). Normal and abnormal US findings in early first-trimester pregnancy: review of the society of radiologists in ultrasound 2012 consensus panel recommendations. Dev. This paper will also focus on which factorsi.e., fetal characteristics and behaviors, maternal lifestyle and pathologies, placental health and dysfunction, labor, incubator conditions, and drug exposuremay affect the development of the vagus. Caton Alissa, R., Bell Erin, M., Druschel Charlotte, M., Werler Martha, M., Lin Angela, E., Browne Marilyn, L., et al. (2020). doi: 10.2139/ssrn.3441806, Bernardes, J., Gonalves, H., Ayres-de-Campos, D., and Rocha, A. P. (2008). BJGP Open 3:bjgpopen19X101674. Gynecol. The International Federation of Gynecology and Obstetrics (FIGO) released specific guidelines on the subject. Birth Defects Res. (2017). Consequently, a cerebral alteration, caused by a brain injury, affects the ANS including the vagus. World J. Pediatr. Ped Research 2013;74: 50-72. (2014). 7:57. doi: 10.3389/fnint.2013.00057, Gemmel, M., De Lacalle, S., Mort, S. C., Hill, L. A., Charlier, T. D., and Pawluski, J. L. (2019). Hypertension 54, 6370. doi: 10.1136/bmjopen-2017-020031, Herry, C. L., Burns, P., Desrochers, A., Fecteau, G., Durosier, L. D., Cao, M., et al. Am J Obstet Gynecol. doi: 10.2174/1570159X19666210125150955. 16, 479494. Women Birth 32, 12. Fetal motor activity, therefore, results closely tied to breathing and cardiovascular patterns, which are modulated by the ANS (Zizzo et al., 2020). Teratol. In this sense, monitoring the quality and the evolutionary pattern of FMs could reveal useful insight regarding ANS, in particular, vagal maturation. For instance, although we know that folate deficiency can impede the neural tube closure or that alcohol can induce dramatic brain modifications (Moore et al., 2016), we still lack knowledge about more subtle influences, that is, the precise effects of just some alcohol during the first weeks of pregnancy or the early effects of maternal stress (Avalos et al., 2014; Caspers Conway et al., 2014; Antonelli et al., 2021). Front. Physiol. Neurosci. Sarkar, P., Lobmaier, S., Fabre, B., Gonzlez, D., Mueller, A., Frasch, M. G., et al. Perinatal hypoxia contributes significantly to the possibility of perinatal brain injury (Gotsch et al., 2007). [Low back pain during pregnancy. At 4 WGA, neurulation occurs: the neural folds arise from the neural plate and begin to fuse in both cranial and caudal direction, thus forming the neural tube, that is, the future central nervous system (CNS). (2020). doi: 10.1016/0002-9378(81)90015-6, Lucchini, M., Fifer, W. P., Sahni, R., and Signorini, M. G. (2016). (2003). The opioid epidemic and neonatal abstinence syndrome in the USA: a review of the continuum of care. The late timing reflects the lag between insult onset (the contraction) and actual reduction in fetal oxygenation. Int. This hypothesis is highly clinically relevant because, in the case of repetitive umbilical cord occlusions with worsening acidemia, fetuses may easily develop cardiovascular decompensation, a phenomenon that occurs through ABP responses to HR decelerations. Fetal scalp electrodes can also be used to directly measure pH during childbirth, but this technique, being even more invasive, is not yet fully accepted and also has some complications (Sabir et al., 2010). The endotoxemia, through lipopolysaccharide molecules, seems to interfere with the cardiac pacemaker synchronization system, altering the fHRV pattern (Frasch and Giussani, 2020). Effect of epidural labor analgesia on fetal heart rate and neonatal outcome. 1983 Jan; 90(1):11-5. Babies' position is another factor that could impact ANS. An increase in arterial blood pressure produces vessel distension and causes arterial baroreceptors to send neuronal messages to the cardioinhibitory center, which in turn causes rapid slowing of the fetal heart rate via the parasympathetic vagus nerve. Assoc. Turk. B., Attridge, J., McGahren, E. D., et al. 193, 20042009. Heart Assoc. Reducing cardioinhibitory activity increases heart rate. (1997). From 34th WGA, female fetuses show indeed a higher mean fHR and entropy, as well as a lower short-term variability and sympathovagal balance, compared to the males (Gonalves et al., 2017). (2006). The fetal heart rate pattern we observe is the combined results of many physiological actions. doi: 10.1016/j.earlhumdev.2019.01.011, Nordenstam, F., Norman, M., and Wickstrm, R. (2019). Indeed, it is known to increase with worsening acidemia (Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, 1996; Frasch et al., 2007, 2009a,b; Durosier et al., 2014). Maternal sleep during pregnancy and poor fetal outcomes: a scoping review of the literature with meta-analysis. In particular, by 6 WGA, the first parasympathetic ganglia can be detected (Mller and O'Rahilly, 1989) and, by 10 WGA, the sympathetic trunks have appeared throughout the vertebral column (Kruepunga et al., 2021) and, apart from the colonic loop, the extrinsic innervation of the enteric nervous system (ENS) is complete (Kruepunga et al., 2020). Gynecol. Proc. 188, 524531. Environmental radiofrequency electromagnetic field levels in a department of pediatrics. Pediatr. Lupus 26, 552558. Fetal heart rate variability and cerebral oxygen consumption in fetal sheep during asphyxia. 2016 Mar 1;594(5):1265-77. The exciting take-home message is that much of this development can be gauged non-invasively during pregnancy using readily available bioelectric sensors such as ECG or, less qualitatively well, but still useful, using ultrasound-derived HR estimation, the mainstay of today's CTG and EFM technologies that is in sore need of technological disruption. J. Perinat. During pregnancy, the maturation pattern of fetal gonads must be taken into account. The placental membrane microbiome is altered among subjects with spontaneous preterm birth with and without chorioamnionitis. MgSO4, which is often administered between 23 and 27 WGA or intrapartum for its tocolytic effect to delay labor onset in pregnancy at risk for preterm birth (Ramsey and Rouse, 2001; Ingemarsson and Lamont, 2003), does not seem to show a significant change in fHRV (Stallworth et al., 1981; Nensi et al., 2014). doi: 10.1530/jrf.0.0600193, Bale, T. L. (2016). Curr. 40:064002. doi: 10.1088/1361-6579/ab205f, Hoyer, D., Schneider, U., Kowalski, E.-M., Schmidt, A., Witte, O. W., Schleuner, E., et al. BJOG Int. The following text describes the principal physiological pathways that control heart rate and influence heart rate variability. Evidence for adverse effect of perinatal glucocorticoid use on the developing brain. Stress 9, 4854. (2008). (2014). 1, 1724. Recently, placenta calcifications samples collected at delivery have been speculated to act as a memory of prenatal maternal stress and diseases exposure, hence highlighting the potential role of placenta in regulating the offspring's future cardiovascular and metabolic health, even through the in utero modulation of the developing ANS (Wallingford et al., 2018). 80, 8291. doi: 10.2174/157488606775252593, De Rogalski Landrot, I., Roche, F., Pichot, V., Teyssier, G., Gaspoz, J.-M., Barthelemy, J.-C., et al. N. Y. Acad. Identified Q&As 100+ Solutions available. J. Anaesth. Hill, M. A. doi: 10.1177/0961203317694960, Nemoda, Z., Massart, R., Suderman, M., Hallett, M., Li, T., Coote, M., et al. Dalton KJ, Dawes GS, Patrick JE. Biobehav. Eur J Obstet Gynecol Reprod Biol. doi: 10.1016/j.earlhumdev.2007.12.001, Berntson, G. G., and Cacioppo, J. T. (2004). (2021). The Dublin randomized controlled trial of intrapartum fetal heart rate monitoring. Placental vascular calcification and cardiovascular health: it is time to determine how much of maternal and offspring health is written in stone. (2020). doi: 10.1097/EDE.0b013e31822546fd. Pediatr. Moreover, except the third trimester (Mulkey and du Plessis, 2018, 2019), literature usually lacks an analysis of potential critical windows in the perinatal period that may give information about ANS development. J. Gynaecol. Nutrients 11:1823. doi: 10.3390/nu11081823, Kozar, M., Tonhajzerova, I., Mestanik, M., Matasova, K., Zibolen, M., Calkovska, A., et al. doi: 10.1016/0002-9378(82)90812-2, Spinillo, A., Viazzo, F., Colleoni, R., Chiara, A., Maria Cerbo, R., and Fazzi, E. (2004). Desynchronization of autonomic response and central autonomic network connectivity in posttraumatic stress disorder. Umbilical cord compression has been created in research environments by actually compressing the fetal cord with implanted mechanical devices that could be manipulated to compress the cord to different degrees and durations. Exp. Therefore, knowing that the ANS-organ connections are established so early in the embryo could offer useful insight for comprehending the complex role of the vagus nerve and autonomic ganglia in the developing embryo/fetus. The size, shape and timing of decelerations induced by cord compression or uterine artery compression tend to converge in the presence of marked fetal acidemia. Res. 31, 514. Psychol. ArXiv210207768 Phys. 20, 5668. Care 26, 534.e9534.e17. Front. periodic accelerations can indicate all of the following except: A. Stimulation of fetal chemoreceptors B. Tracing is maternal C. Umbilical vein compression A. Stimulation of fetal chemoreceptors All of the following are likely causes of prolonged decelerations except: A. doi: 10.1159/000488106, Morton, S. U., and Brodsky, D. (2016). Prenatal influences on temperament development: the role of environmental epigenetics. J Physiol. (2001). 2002 Mar;24(3):250-76. (2006). doi: 10.1196/annals.1314.006, Sehmbi, H., D'Souza, R., and Bhatia, A. Ontogeny of reticular framework of white pulp and marginal zone in human spleen: immunohistochemical studies of fetal spleens from the 17th to 40th week of gestation.
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