B. doi: 10.1002/bdra.23045, Lattimore, K. A., Donn, S. M., Kaciroti, N., Kemper, A. R., Neal, C. R., and Vazquez, D. M. (2005). 17, 354381. At about 1820 WGA, rapid eye movements (REM) can be detected (Borsani et al., 2019) as well as quiet and active sleeping states (Dereymaeker et al., 2017), although fetal behavioral states do not show particular coherence with ANS tone (Brndle et al., 2015). The above-mentioned studies show us what impact labor can have on the ANS and the vagus nerve. Lear CA, Galinsky R, Wassink G, Mitchell CJ, Davidson JO, Westgate JA, Bennet L, Gunn AJ. (2018). Placenta 54, 3037. J. Afr. Physiol. These and other metabolic or immune pathologies that could arise later in life might have their origin in alteration of CAP functioning, that is, in inflammation regulation by the ANS (Pavlov and Tracey, 2012; Burgio, 2015; Bonaz et al., 2021). Fetal yawning, in Frontiers of Neurology and Neuroscience, ed. (2018). Immun. 29, 24572460. During the 3rd trimester of pregnancy, emerging fetal sleep states are detectable, with the onset of the functional organization of the sleep cycle around 2830 WGA, and these patterns gradually consolidate around 36 WGA (Van den Bergh and Mulder, 2012). doi: 10.1016/j.earlhumdev.2007.12.001, Berntson, G. G., and Cacioppo, J. T. (2004). 15:721605. doi: 10.3389/fnins.2021.721605. For instance, stroke can easily alter both sympathetic and parasympathetic tone, thus impairing the ANS regulatory capacities (Reich et al., 2019). (2017). Rev. doi: 10.1038/s41390-021-01420-x. The effect of lumbar epidural anesthesia on fetal heart rate baseline variability. Microbiol. The evidence so far shows that the intrinsic fHRV is influenced by the fetal ANS activity and, conversely, also shapes the ANS activity into the postnatal period, at least in part via the afferent fibers of the vagus nerve (Herry et al., 2021). Sex differences in fetal heart rate and variability assessed by antenatal computerized cardiotocography. Cahill AG, Tuuli MG, Stout MJ, Lpez JD, Macones GA. A prospective cohort study of fetal heart rate monitoring: deceleration area is predictive of fetal acidemia. Am. Fetal monitors are better at separating maternal and fetal heart rate. 101, 11411150. Front. The homeostatic response that preserves the . doi: 10.1148/rg.2015150092, Rou, G., Samoilescu, G., Rau, M. C., and Baltag, O. What is amiss is the understanding and acting upon the fact that each fetus and newborn are not truly new, but, rather, come with weeks and months of experience in utero. 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). 42:ac010e. Birth Defects Res. These situations increase the risk of impairment of fetal brain development resulting in emotional, behavioral, and/or cognitive problems in later life (Glover, 2015; Antonelli et al., 2021). doi: 10.1006/drev.1998.0452, Koletzko, B., Cremer, M., Flothktter, M., Graf, C., Hauner, H., Hellmers, C., et al. Transl. Breastfeed. J. 51, 346356. doi: 10.1016/j.jri.2018.01.004, Pryor, J. R., Maalouf, F. I., Krans, E. E., Schumacher, R. E., Cooper, W. O., and Patrick, S. W. (2017). 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). FC, MC, SV, CV, and AM conceptualized the paper. doi: 10.1126/science.7414330, Glover, V. (2015). Psychopharmacology (Berl.) (2011). J. Expo. Aspects regarding the occupational and non-occupational exposure to low frequency and radiofrequency electromagnetic fields, in 2016 International Conference on Applied and Theoretical Electricity (ICATE) (Craiova), 16. In particular, centers that are paramount to neurotransmitters (e.g. A decrease in the heart rate b. BJOG Int. Using fetal oximetry probes many centers reported images of deep decelerations with little or no change in fetal oxygen saturation. As revealed by HRV analysis, the ANS constantly develops. The nadir of the deceleration was very close to the end of the compression period in both groups. This situation puts newborns at risk of cardiovascular and metabolic dysfunctions, which can then negatively affect the developing brain by inducing inflammation or glucose deficiency (Hillman et al., 2012; Morton and Brodsky, 2016; Mulkey and du Plessis, 2018). (2016). 72, 587593. Med. Clin. 27, 12451250. doi: 10.1016/j.midw.2017.10.011, Macklem, P. T., and Seely, A. J. Nutr. While this summary provides the basics for understanding heart rate regulation, it is important to remember that our understanding of this physiology continues to evolve. Animal models for the study of neonatal disease, in Animal Models for the Study of Human Disease, ed P. Michael Conn (London: Academic Press) 805837. Fetal growth restriction: from polyvagal theory to developmental impairments? Early Hum. 2007 Nov;114(11):1442-4. doi: 10.5546/aap.2020.eng.e246, Casagrande, D., Gugala, Z., Clark, S. M., and Lindsey, R. W. (2015). Currently, ANS development is usually assessed during the 3rd trimester, when vagus nerve myelination begins (Mulkey and du Plessis, 2018). J. Obstet. J. Obstet. Reducing low back and posterior pelvic pain during and after pregnancy using OMT. Consequently, the fetal and infant capacity to homeostatically adapt to the environment could be impaired (Van den Bergh and Mulder, 2012). New York, NY: W. W. Norton. Effect of halogen light in fetal stimulation for fetal well-being assessment. A. Exp. Although CS delivery is far faster than a vaginal birth modality, the fetus is still subjected to significant stress that can create changes in the development of some systems, including the ANS (Tribe et al., 2018). doi: 10.1016/j.braindev.2018.10.009, Brndle, J., Preissl, H., Draganova, R., Ortiz, E., Kagan, K. O., Abele, H., et al. doi: 10.1007/978-1-4939-7828-1_19, Frasch, M. G., Boylan, G. B., Wu, H.-T., and Devane, D. (2017). Sustained neurobehavioral effects of exposure to SSRI antidepressants during development: molecular to clinical evidence. A decrease in the heart rate The vagus nerve begins maturation 26 to 28 weeks. 10:413. doi: 10.3389/fcimb.2020.00413, Oliveira, V., von Rosenberg, W., Montaldo, P., Adjei, T., Mendoza, J., Shivamurthappa, V., et al. Early oxygen levels contribute to brain injury in extremely preterm infants. Since the development of ANS and the vagus influence have been shown to be reflected in cardiac variability, this paper will rely in particular on studies using fetal heart rate variability (fHRV) to monitor the continued growth and health of both animal and human fetuses. Med. doi: 10.1017/S095457942000142X, Hoyer, D., Kowalski, E.-M., Schmidt, A., Tetschke, F., Nowack, S., Rudolph, A., et al. 17. N. Y. Acad. Women Birth 32, 12. Furthermore, ANS alterations in newborns can lead to neurological dysfunctions including cerebral palsy at 2 years of age (Dimitrijevi et al., 2016). (1999). Neurodevelopment: the impact of nutrition and inflammation during preconception and pregnancy in low-resource settings. Briefly, through the vagus nerve, the brain receives information about the body's inflammatory milieu and, thus, activates neuroimmune responses to dampen the detected inflammation (Garzoni et al., 2013; Frasch, 2020; Bonaz et al., 2021). Health Perspect. (2003). doi: 10.1071/RD05030, Morsi, A., DeFranco, D., and Witchel, S. F. (2018). Experiments were designed with less drastic interventions to simulate more realistic clinical conditions. doi: 10.1038/tp.2015.32, Nensi, A., De Silva, D. A., von Dadelszen, P., Sawchuck, D., Synnes, A. R., Crane, J., et al. Sympathetic neural activation does not mediate heart rate variability during repeated brief umbilical cord occlusions in near-term fetal sheep. (2020). Sci. 662, 118134. The influence of corticosteroids on fetal heart rate variability: a systematic review of the literature. Fetal development assessed by heart rate patternstime scales of complex autonomic control. J. Physiol. (12), Over that last decade mounting evidence based on recent animal experimentation with very sensitive sensors and finer time resolution, has produced more information about hand chemoreceptors and their role in the production of decelerations. 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). Auton. These patterns are altered by pain and could hence not only be pre-emptive for negative outcomes for labor and birth (Goldenberg et al., 2008), but also suggest their influence on the neurodevelopment of the fetal vagal system itself (Borovikova et al., 2000; Tracey, 2009; Frasch et al., 2016). Pediatr. An important difference should be moreover emphasized between the CS delivery following a period of labor and CS delivery prior to the onset of labor. Usually, it is administered between 24 and 34 WGA, mainly to ensure optimal fetal pulmonary development (Mulder et al., 2004; Committee on Fetus and Newborn and Section on Anesthesiology and Pain Medicine, 2016). J. Neurosci. American College of Obstetricians and Gynecologists. 17, 641650. doi: 10.1016/j.neurobiolaging.2019.01.021, Faa, G., Manchia, M., Pintus, R., Gerosa, C., Marcialis, M. A., and Fanos, V. (2016). Obstet. fHRV undergoes fewer changes with the use of the full lateral position, compared with the use of wedged supine position (Preston et al., 1993). J. Obstet. 88, 718720. Nutrients 11:1823. doi: 10.3390/nu11081823, Kozar, M., Tonhajzerova, I., Mestanik, M., Matasova, K., Zibolen, M., Calkovska, A., et al. Should one of them be damaged, the other one alone could not regulate the body's homeostasis efficiently anymore. 7:80. doi: 10.3389/fpsyg.2016.00080. Is it also related to comfort? It has been reported in these cases a correlation with deficit in fetal growth, adverse outcomes for labor and birth, and even preterm birth (Lee and Gay, 2004; Micheli et al., 2011; Zafarghandi et al., 2012; Warland et al., 2018). As a result, oligodendrocytes and their progenitors are damaged during a critical period of brain development, thus altering brain myelination and leading even to periventricular leukomalacia (Kadhim et al., 2001). 1981 Dec 1; 141(7):797-806. Environmental radiofrequency electromagnetic field levels in a department of pediatrics. J. Gastrointest. Psychoneuroendocrinology 87, 2734. Infants born with CS delivery following a period of labor have a higher and more developed ANS tone compared to those born with CS without labor (Mulkey et al., 2019). Psychol. With complete vagal and and adrenergic blockade, the decelerations persisted. Similarly, even autoimmune diseases can involve a dysregulation in maternal inflammatory response (Gordon, 2004; Lu-Culligan and Iwasaki, 2020; Han et al., 2021). Heart rate variability in healthy term newborns is related to delivery mode: a prospective observational study. (2013). Sci. Cardiac orienting to auditory stimulation in the fetus. Horne, R. S. (2018). 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). At 2629 WGA, fetuses become able to efficiently control body temperature (Moore et al., 2016). Although incubator EMF seems to be under the normative value, EMFs could become dangerous when the incubator, and thus the newborn, is surrounded by other instruments or staff's devices that, through their own EMF, can give rise to electromagnetic interference (Besset et al., 2020). Consequently, a cerebral alteration, caused by a brain injury, affects the ANS including the vagus. doi: 10.1038/s41390-021-01460-3, Ray-Griffith, S. L., Wendel, M. P., Stowe, Z. N., and Magann, E. F. (2018). N. Y. Acad. J. Perinatol. Obstet. Acta Obstet Gynecol Scand. doi: 10.18632/oncotarget.20110, Gordon, C. (2004). doi: 10.1073/pnas.2012900118, Urfer-Maurer, N., Ludyga, S., Stalder, T., Brand, S., Holsboer-Trachsler, E., Gerber, M., et al. (2007). 304, R383R392. Intrapartum management of category II fetal heart rate tracings: towards standardization of care. doi: 10.1038/35013070, Borre, Y. E., O'Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., and Cryan, J. F. (2014). doi: 10.1016/j.smrv.2018.03.004, Weber, A., and Harrison, T. M. (2019). Res. Classic teaching on the mechanisms of variable decelerations is outlined in Figure 2. Reconsidering fetal pain. (2012). These processes can be implemented through cell autonomous or intercellular signaling. doi: 10.1016/j.jsbmb.2015.09.039, Handal, A. J., Harlow, S. D., Breilh, J., and Lozoff, B. As previously mentioned, oxytocin plays an important role in activating the PNS and it has been shown to dampen SNS (Gamer and Bchel, 2012).
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