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Immunol. 8:774. doi: 10.3389/fphys.2017.00774, Nalli, C., Iodice, A., Andreoli, L., Galli, J., Lojacono, A., Motta, M., et al. (2015). Available online at: http://www.ncbi.nlm.nih.gov/books/NBK544290/ (accessed April 8, 2021). Analg. On the other hand, the hypothalamic-pituitary-adrenals (HPA) axis and vagal activation become more finely tuned (Bystrova, 2009). Gynaecol. 37, 558562. 8:356. doi: 10.3389/fmicb.2017.00356, Lavin, J. P. (1982). The dysregulation of placental functions can induce an insufficient intake of nutrients for the fetus, thus, especially during mid and late gestation, impairing the development of various brain areas, including the hypothalamus that seems to be particularly sensitive to the nutrient deficiency (Nugent and Bale, 2015). Clark SL, Nageotte MP, Garite TJ, Freeman RK, Miller DA, Simpson KR, Belfort MA, Dildy GA, Parer JT, Berkowitz RL, DAlton M, Rouse DJ, Gilstrap LC, Vintzileos AM, van Dorsten JP, Boehm FH, Miller LA, Hankins GD. Perinatal psychoneuroimmunology: protocols for the study of prenatal stress and its effects on fetal and postnatal brain development, in Psychoneuroimmunology Methods in Molecular Biology, ed Q. Yan (New York, NY: Springer New York), 353376. 41, 323. Developmental milestones of the autonomic nervous system revealed via longitudinal monitoring of fetal heart rate variability. J. Obstet. In response to sudden auditory stimulation, the central nervous system activates the cardioacceleratory center. Gender does not affect fetal heart rate variation. Neurology 56, 12781284. 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). Timeline of fetal and postnatal development that shows the main events related to ANS development in order to define the main critical windows clinicians should pay attention to. Res. Rezk, A. Y., Abdulqawi, K., Mustafa, R. M., El-Azm, T. M. A., and Al-Inany, H. (2008). The frequency and size of deceleration are important indicators as well as the nature of the FHR between contractions and trends over time. doi: 10.1016/j.earlhumdev.2018.07.003, Mller, F., and O'Rahilly, R. (1989). New York, NY: W. W. Norton. 10:CD002271. Breastfeed. J. Obstet. 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. Hypothermia for newborns with hypoxic-ischemic encephalopathy. A variety of different ANS and vagus nerve pattern activities are now well-established between different sexes, which can be well-represented by HRV tracking even during fetal life. Since yawning has been related to thermoregulatory behaviors and the ability of switching between arousal and rest states, both of which are strictly dependent on ANS functionality, the detection of yawning at this early age could represent a useful indicator of ANS development or, as suggested, brainstem functionality (Walusinski, 2006, 2010, 2014; Gallup and Eldakar, 2013). Environ. 2009 Aug 12;302(6):660-8. This seems to be associated with an increased risk for antibiotic-resistant neonatal sepsis (Mercer et al., 1999; Hantoushzadeh et al., 2020). 80, vii94. It is worth noting that, from the 2nd trimester, HRV metrics can successfully estimate fetal autonomic brain age (Hoyer et al., 2012, 2013b, 2015, 2017, 2019). Human fetal heart rate variability-characteristics of autonomic regulation in the third trimester of gestation. J. Ind. doi: 10.1016/s0022-2828(05)82386-7, Morrison, J. L., Berry, M. J., Botting, K. J., Darby, J. R. T., Frasch, M. G., Gatford, K. L., et al. The 1st stage begins when significant and regular contractions start and ends when there is a full cervical dilation of 10 cm. Standards of measurement, physiological interpretation, and clinical use. The FHR returned to predeceleration levels after the compressions ended in both groups. Early exposure of buprenorphine induces higher levels of fHRV, whereas at 3236 GWA fetuses display less suppression of motor activity (Jansson et al., 2011; Conradt et al., 2018), indicating the involvement of the vagus nerve system. Maternal heart rate variability and fetal behavior in hypertensive and normotensive pregnancies. Baltimore, MD: Johns Hopkins University Press. doi: 10.1080/02724999208250616, Ledger, W. J., and Blaser, M. J. Citalopram use in pregnancy: prospective comparative evaluation of pregnancy and fetal outcome. Clin. 30, 12691303. 68, 9881001. As the 3rd trimester advances, specific nociceptive event-related potentials in the brain increasingly develop until 3537 WGA (Verriotis et al., 2016). J. doi: 10.1016/j.semerg.2015.06.005, Gallup, A. C., Church, A. M., and Pelegrino, A. J. doi: 10.2307/1131844, Doyle, R. M., Harris, K., Kamiza, S., Harjunmaa, U., Ashorn, U., Nkhoma, M., et al. Opioid dependence and pregnancy: minimizing stress on the fetal brain. Several uncontrollable situations such as natural disasters, relational or financial problems, bereavement, and/or stressful daily hassles can threaten a woman's life during her pregnancy. Your doctor will then take action to prevent medical complications for your newborn. Physiotherapy 104, 338346. Sleep disorders in pregnancy. Scand. Front. doi: 10.1111/aogs.12681, Haley, D. W., Handmaker, N. S., and Lowe, J. Moreover, an exploratory study conducted on twins, highlighted that sex-specific differences in fetuses can be noticed both in linear and non-linear fHR metrics. Health Rep. 2, 304314. doi: 10.3399/bjgpopen19X101674, Mackenzie, J., Murray, E., and Lusher, J. After 2 minutes of complete cord compression, the FHR in the deceleration began to recover despite continuing fall in cerebral oxygenation and rising hypertension. Biosci. (2017). Neurosci. doi: 10.1097/OGX.0000000000000007, Verdurmen, K. M. J., Warmerdam, G. J. J., Lempersz, C., Hulsenboom, A. D. J., Renckens, J., Dieleman, J. P., et al. Hence, further research is needed about these drugs' impact on fetal vagus nerve development. Fetal functional brain age assessed from universal developmental indices obtained from neuro-vegetative activity patterns. Even if further research is needed, maternal vitamin D intake deficit correlates with altered metabolic and contractile development of the heart and the control mechanisms of blood pressure in fetuses (Morris et al., 1995; Gale et al., 2008). Res. The impact of maternal obesity on childhood neurodevelopment. Surg. The vagus nerve and the inflammatory reflexlinking immunity and metabolism. (2013). (2016). As pathologies can affect ANS development, altered ANS function can make newborns more vulnerable to those same pathologies, due to failure in activating efficient anti-inflammatory reflexes including the CAP (Yiallourou et al., 2012; Mulkey et al., 2018; Bonaz et al., 2021). A second component of the chemoreflex response to hypoxemia is parasympathetic, mediated via the vagus nerve, resulting in a fall in heart rate. Ther. Acad. Antibiotic use in pregnancy and drug-resistant infant sepsis. The role of immune factors in shaping fetal neurodevelopment. An increase in the heart rate c. An increase in stroke volume d. No change a. Can. Endocrinol. Child Health 23, 285291. The fear of missing fetal injury during labor has led to soaring CS rates and the failure of the EFM has resulted in the misguided dissent over its utility in general throwing the proverbial baby with the bathwater. The homeostatic response that preserves the . doi: 10.1016/S0140-6736(08)60074-4. Cell Tissue Res. which intrinsic homeostatic response is the fetus demonstrating . Frasch, M. G. (2020). Fetal development of complex autonomic control evaluated from multiscale heart rate patterns. Lee CY, Di Loreto PC, OLane JM. Regul. Brain Dev. A., Caulfield, L. E., Costigan, K. A., Merialdi, M., Nguyen, R. H. N., Zavaleta, N., et al. doi: 10.1111/jog.12619. Commentary: Computerised interpretation of fetal heart rate during labour (INFANT): a randomised controlled trial. fHRV undergoes fewer changes with the use of the full lateral position, compared with the use of wedged supine position (Preston et al., 1993). Usually, any process that causes the following conditions is capable of inducing late decelerations: Two of the most common late deceleration causes include an overactive uterus and hypotension due to epidural analgesia. Gomes, E. L. D. F. D., Santos, C. M. D., Santos, A. D. C. S., Silva, A. G. D., Frana, M. A. M., Romanini, D. S., et al. doi: 10.1016/j.ajog.2019.04.029, Flenady, V., Ellwood, D., Bradford, B., Coory, M., Middleton, P., Gardener, G., et al. From maternal diet to neurodevelopmental disorders: a story of neuroinflammation. Oxytocin increases autonomic cardiac control: moderation by loneliness. Autonomic nervous system regulation of baseline heart rate in the fetal lamb. (13) and Bennet et al. Maternal pathologies influence the onset of altered neurodevelopment patterns during fetal life, which could lead to actual neurologic disorders during childhood (Faa et al., 2016; Vohr et al., 2017). These methods are not held to a specific clinical hypothesis. Pediatr. Am J Obstet Gynecol. Human fetal behavior: 100 years of study. As the parasympathetic system is constituted by the oculomotor, facial, glossopharyngeal, and vagus nerves, and since the trigeminal, facial, glossopharyngeal, spinal accessory, and vagus nerves lay the foundations for social interaction especially in newbornsthese nerves are central to sensing environmental stimuli, including the human voice, and to carrying out behaviors such as head-turning, smiling, sucking, and swallowing(Porges, 2011), the cranial nerves maturation may be paramount for an optimal ANS growth and, thus, for developing regulatory adaptive responses. doi: 10.1038/sj.jp.7200445, Aidy, S. E., Dinan, T. G., and Cryan, J. F. (2015). Am. Gut microbiota: the conductor in the orchestra of immuneneuroendocrine communication. Does osteopathic manipulative treatment induce autonomic changes in healthy participants? Neural crest cells contribute an astrocyte-like glial population to the spleen. A low APGAR (i.e., appearance, pulse, grimace, activity, and respiration) score, Greater chance of admission to the neonatal intensive care unit after delivery. Linear and complex heart rate dynamics vary with sex in relation to fetal behavioural states. B. Nevertheless, prone sleeping is considered a risk factor for SIDS and it shows a lower short-term variability in HRV (Lucchini et al., 2016). Early Hum. Figure 6: Superimposed decelerations from uterine artery compression (in blue) and cord compression (in red). Interestingly, gestational age can also be precisely estimated by measuring the opening and closing time of fetal cardiac valves (Marzbanrad et al., 2017), finding that could highlight the contribution of intrinsic fHRV or, at least, heart activity, to global HRV. At 46 WGA the primitive diaphragm appears (Hill, 2021d) and, by 7 WGA, the four chambers of the heart have formed, thus connecting the heart to the aorta and the pulmonary trunk. Sorokin, Y., Dierker, L. J., Pillay, S. K., Zador, I. E., Schreiner, M. L., and Rosen, M. G. (1982). 42:ac010e. U.S.A. 107, 1675716758. In adult cardiology, ECG changes are very helpful to diagnose myocardial infarction because there is a direct relationship, precisely defined by anatomy and electromagnetic physics, linking the presence of Q waves in the 12-lead ECG to the location of injured myocardium. Board Fam. 201, 10021006. doi: 10.1146/annurev-cellbio-021120-033518, Lutterodt, M. C., Khler, P., Kragstrup, J., Nicolaisdottir, D. R., Siersma, V., and Ertmann, R. K. (2019). Cell. Sci. 43, 395407. There is no clarity on its usefulness in decreasing perinatal mortality or cerebral palsy when measured by a CTG which has been explained by the incorrect focus of EFM on prediction of acidemia, a poor correlate to fetal injury, instead of predicting fetal cardiovascular decompensation per se as well as the limitations of CTG technologies in capturing the short-term time scale fluctuations of HRV reflecting vagal modulations (Alfirevic et al., 2017; Frasch et al., 2017; Frasch, 2018; Gold and Frasch, 2021). doi: 10.1016/j.earlhumdev.2017.09.002, Gong, W., Liang, Q., Zheng, D., Zhong, R., Wen, Y., and Wang, X. PLOS ONE 13:e0200799. As discussed throughout this article the relationship between heart rate and the underlying fetal condition is complex. Lupus 26, 552558. A short review of adipokines, smooth muscle and uterine contractility. At the beginning of the 2nd trimester, the cerebral cortex creates more and more sulci and gyri to increase its surface area and allow brain development. Natl. Paediatr. In this sense, dysregulations in mother circadian rhythm, due to disturbed sleep-awake patterns, could interfere with the development of circadian control systems of the fetus and, consequently, with the circadian profile of the vagus nerve, impacting the physiologic vagal neurodevelopment itself. The neural tube also begins to thin to form the central canal of the spinal cord (Moore et al., 2016). Res. doi: 10.1016/j.earlhumdev.2009.08.001, Buyon, J. P. (1998). J. R. Soc. (2018). The Polyvagal Theory: Neurophysiological Foundations of Emotions, Attachment, Communication, and Self-Regulation, 1st Edn. doi: 10.3109/14767058.2014.964202, Kariniemi, V., and Mml, P. (1981). Comp. Sleep deprivation during pregnancy and maternal and fetal outcomes: is there a relationship? Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Stages of labor, in StatPearls (Treasure Island, FL: StatPearls Publishing). J. 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). Pharmacol. doi: 10.1038/s41390-019-0309-8, Noben, L., Verdurmen, K. M. J., Warmerdam, G. J. J., Vullings, R., Oei, S. G., and van Laar, J. O. E. H. (2019). doi: 10.1159/000307075, Walusinski, O. 90, 131139. 2017 Feb;216(2):163.e1-163.e6. The medulla oblongata also contains the vasomotor center that regulates peripheral blood vessel dilation and constriction to help maintain normal blood pressure and distribute blood to vital organs. Physiol. Physiol. Rochester, NY: Social Science Research Network. Semin. Pregnancy Hypertens. Eng. Lee ACC, Kozulki N, Blencowe H et al. (2019). Central stimuli like a sudden loud sound or a quick increase in blood pressure cause rapid heart rate changes mediated by direct neuronal pathways to the sinoatrial node. J. Obstet. 71, 313321. Epidemiology and causes of preterm birth. Cochrane Database Syst. Hull J, Dodd KL. Stress 9, 4854. (2014). Res. 127:067005. doi: 10.1289/EHP4648, Suri, R., Altshuler, L., Hellemann, G., Burt, V. K., Aquino, A., and Mintz, J. However, theres no clinical evidence suggesting its effectiveness when used alone in women with adequate oxygen levels. Diet and lifestyle before and during pregnancy practical recommendations of the germany-wide healthy start young family network. Q. J. Exp. These pathologies are associated with fetal inflammatory response syndrome, which manifests as increased pro-inflammatory markers, including IL-6, IL-1, and TNF- (Gotsch et al., 2007). J. Clin. Orthop. Maternal vitamin D status during pregnancy and child outcomes. Premature infant responses to noise reduction by earmuffs: effects on behavioral and physiologic measures. FHR decelerations can be associated with little or no change in peripheral hemoglobin oxygen saturation. Multiomic immune clockworks of pregnancy. Autonomic maturation from birth to 2 years: normative values. (2000). Central autonomic network mediates cardiovascular responses to acute inflammation: relevance to increased cardiovascular risk in depression? Magnesium sulfate as a tocolytic agent. Obstet. The persistent exposure to photic stimuli or high noise during pregnancy, for instance, due to the mother's occupation, seems to correlate with reduced fetal growth (Selander et al., 2019), increased incidence of congenital heart diseases (Gong et al., 2017), impaired development of cortical areas (Zhang et al., 1992; Wilson et al., 2008), and potential disruption of the vagus nerve maturation. The case of premature births is probably the most challenging. Pediatr. A Clin. Fetal growth and maternal exposure to particulate matter during pregnancy. The pathologies that induce chronic hypoxemia in the mother, including SBD (Pien and Schwab, 2004) and anemia, may induce dysregulations in the vagal control systems. In fact, fHRV is a non-invasive marker whose changes have been associated with ANS development, vagal modulation, systemic and neurological inflammatory reactions, and even fetal distress during labor. Indeed, respiratory sinus arrhythmia appears to be strictly related and modulated by efferent vagal activity. Neuroscientist 13, 241256. J. Obstet. Which intrinsic homeostatic response is the fetus demonstrating when abrupt variable decelerations are present? Fetal audition. Freeman RK, Garite TJ, Nageotte MP. (2017). You are here: Home. The influence of betamethasone on fetal heart rate variability, obtained by non-invasive fetal electrocardiogram recordings. Maternal occupational exposure to polycyclic aromatic hydrocarbons and risk of neural tube defect-affected pregnancies. PLoS ONE 8:e68211. 114, 11941201. The 3rd stage commences when the fetus is delivered and ends with the delivery of the placenta (afterbirth) (Hutchison et al., 2021). Development of the gonad in normal and anencephalic human fetuses. The effects of pregnancy on autoimmune diseases. Perinatol. Fetal Diagn. Solutions Fetal Neonatal Ed. Labor is divided into three stages. 1993; Giussani, 2016). doi: 10.1097/PCC.0000000000000643, Lobmaier, S. M., Mller, A., Zelgert, C., Shen, C., Su, P. C., Schmidt, G., et al. Integr. (2007). But maybe, more than anything, medical procedures tend to impair babies' sleep the most, in particular since in preterm newborns many interventions are perceived as noxious and painful, thus heightening the stress response (Holsti et al., 2006; Weber and Harrison, 2019). The patterns of cytokine response and the neuroimmune physiology of the fetus and the placenta mirror the maternal ones throughout pregnancy (Sherer et al., 2017, 2018; Prins et al., 2018; Peterson et al., 2020). The cervix undergoes biochemical changes that increase its elasticity. Indeed, extreme variations of environmental or core temperature can impair the ANS, with all due complications (Fox and Matthews, 1989; Mowery et al., 2011). Engl. J. Neurosci. Vasoconstriction is mediated through the -adrenergic receptors in liver, kidney, skin and gut, and vasodilation is mediated through adrenergic receptors in skeletal muscle. 15:721605. doi: 10.3389/fnins.2021.721605. Intervention minimizing preterm infants' exposure to NICU light and noise. North Am. 107, 475480. Development of fetal and neonatal sleep and circadian rhythms. Other work by Bennet et al has also challenged common teaching about the relationship between hypertension and decelerations. Regul. Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. The effect of labor on maternal and fetal circulating catecholamines. J. Dev. Uchitel, J., Vanhatalo, S., and Austin, T. (2021). Here, we show that hyperactivity-induced REST/NRSF activation, triggers a homeostatic rearrangement of GABAergic inhibition, with increased frequency of miniature inhibitory postsynaptic currents (IPSCs) and amplitude of evoked IPSCs in mouse cultured hippocampal neurons. doi: 10.1113/JP275776. Despite the evidence of positive effects of non-surgical and non-pharmacological treatments, such as physiotherapeutic interventions, acupuncture, or osteopathic manipulations (Gutke et al., 2015; Gallo-Padilla et al., 2016; Ray-Griffith et al., 2018; Smith et al., 2018; Cerritelli et al., 2020), the use of drugs for pain relief (e.g., low-dose aspirin, acetaminophen, non-steroidal anti-inflammatory drugs, and opioids) during pregnancy is still very common (Ray-Griffith et al., 2018). Improving pregnancy outcomes in humans through studies in sheep. Summary of the HRV metrics cited in the main text (Brndle et al., 2015; Massaro et al., 2017; Oliveira et al., 2019; Patural et al., 2019; Frasch et al., 2020a). doi: 10.1038/s41372-019-0342-9, Siddiqui, S., Fifer, W. P., Ordonez-Retamar, M., Nugent, J. D., and Williams, I. Saving the brain one heartbeat at a time: perspectives. PLoS ONE 12:e0180167. doi: 10.1002/14651858.CD006066.pub3, Allen, L. H. (2001). 128:1443. doi: 10.1111/1471-0528.16674, Gold, N., Herry, C. L., Wang, X., and Frasch, M. G. (2021). Here, environmental factors such as temperature, light, noise, procedures could induce a high amount of stress, which could become toxic, that is, induce severe alterations in the brain and organic development, with long-lasting complications (De Jonckheere and Storme, 2019; Weber and Harrison, 2019). Reducing cardioinhibitory activity increases heart rate. (2013). Eur. J. Matern. 15 minutes no matter what stage of labor C. 60 minutes in the active phase of the first stage and every 30 minutes in second stage Correct Ans-A. C Embryo Today Rev. Effect of epidural analgesia on the fetal heart rate. (2015). It is noteworthy that earmuffs show ambiguous results, that is, they can both help oxygenation and sleep and provoke stress (Zahr and de Traversay, 1995; Aita et al., 2013; Almadhoob and Ohlsson, 2020). (2020). Nevertheless, the presence of many confounding factors and the small sample sizes make unclear the mechanism of action of glucocorticoids on fHRV and consequently the impact on ANS development (Verdurmen et al., 2013). SAGE Open Nurs. Some authors have challenged the role of the baroreceptor response as the sole or major cause of fetal heart rate decelerations.6, 13-15 Clinicians who use fetal heart rate recording are strongly encouraged to read in detail excellent summaries of their studies on the mechanisms of fetal heart rate decelerations.6, 13-15, In one set of sheep experiments, blood pressure and fetal cerebral oxygenated hemoglobin were measured during complete cord compression. Perinatol. 56, 3539. The opioid prenatal overexposure has instead neurotoxic consequences on several fetal systems: cardiovascular, respiratory, neurobehavioral, metabolic, and neuroendocrine (Conradt et al., 2018). This hypothesis could be reinforced by the evidence that yawning seems to rely on interoception, the inner sense that constantly monitors the internal milieu and for which the vagus nerve plays a central role, and to be processed by the CAN (in particular, insula, hypothalamus, locus coeruleus, and reticular activating system) (Walusinski, 2006).

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