Mol. Limitations of ST analysis in clinical practice: three cases of intrapartum metabolic acidosis. Effects of intramuscular pethidine on fetal heart rate variability during labour. The occupational and environmental exposure to pollution may be another important disrupting factor for fetal ANS development. Nutrition during pregnancy, lactation and early childhood and its implications for maternal and long-term child health: the early nutrition project recommendations. Pediatr. Whereas, in the previous section we described the fetal development in relation to ANS maturation, showing potential short-term and long-term alteration in case something should negatively affect pregnancy or labor, this section will now detail what factors can alter ANS development and in which ways. It is possible, therefore, to assume that the mother, considering the limited light-dark variation during intrauterine life, entrains the developing circadian rhythm of the fetus to this cycle (Mirmiran et al., 2003). Sci. Clin. Fetal heart rate deceleration, albeit somewhat delayed, still occurred in response to cord compression. Placental microbial colonization and its association with pre-eclampsia. 118, e246e251. Experiments were designed with less drastic interventions to simulate more realistic clinical conditions. Brain Dev. Integr. Frasch, M. G. (2020). Teratol. Maternal occupational exposure to polycyclic aromatic hydrocarbons and risk of neural tube defect-affected pregnancies. 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. Two-year infant neurodevelopmental outcome after single or multiple antenatal courses of corticosteroids to prevent complications of prematurity. Med. Dev. doi: 10.3390/nu7053067, Wang, X., Durosier, L. D., Ross, M. G., Richardson, B. S., and Frasch, M. G. (2014). Am. Eur J Obstet Gynecol Reprod Biol. Fetal myocardial acidosis is occurring B. Fetal hypoxemia may be present C. The fetus has oxygen reserves - CORRECT ANSWERS B. Fetal hypoxemia may be present Which intrinsic homeostatic response is the fetus demonstrating when abrupt variable decelerations are present? Long-term neurodevelopmental outcome of children born to prospectively followed pregnancies of women with systemic lupus erythematosus and/or antiphospholipid syndrome. Cord compression and uterine contractions can induce decelerations. (2013b). Microbiome 6:196. doi: 10.1186/s40168-018-0575-4, Lemyre, B., and Chau, V. (2018). a. Obstet. Fetal mediators of the relationships between increased pregnancy and labour blood pressure and newborn irritability. (2016). World J. Pediatr. Theyve concluded that the chances of fetal hypoxia remain low if repeated decelerations arent present and fetal heart tracing is otherwise normal. doi: 10.1002/pd.4932, Edwards, N., Middleton, P. G., Blyton, D. M., and Sullivan, C. E. (2002). Res. As a consequence, by relying on appropriate animal models, several authors have defined potential critical windows related to human brain development (see, for instance, Figure 1 in Morrison et al., 2018). ANS, autonomic nervous system; CAN, central autonomic network; fHRV, fetal heart rate variability; FM, fetal movement; GM, general movement; PNS, parasympathetic nervous system; WGA, weeks gestational age. Prenatal cardiac function and postnatal cognitive development: an exploratory study. Furthermore, without uterus protection, newborns can be particularly sensitive to sounds, which usually overcome the 45 dB limit recommended by the American Academy of Pediatrics (Almadhoob and Ohlsson, 2020), thus resulting in toxic stress (Weber and Harrison, 2019). doi: 10.1016/j.semnephrol.2010.10.007. 56, 3539. 34, 668675. This detects changes in the normal FHR pattern at the time of labor, reassuring your obstetrician if its safe to proceed. 1993 Feb;461:431-49. Semin. Curr. 2003 Mar; 188(3):820-3. 36, 10551064. doi: 10.1515/jpme.1993.21.2.107, Clarkson, C. E., and Adams, N. (2018). Ther. Impact of chronic fetal hypoxia and inflammation on cardiac pacemaker cell development. 8, 3841, Pelzer, E., Gomez-Arango, L. F., Barrett, H. L., and Nitert, M. D. (2017). Gynecol. J. Exp. The first stage of dilatation begins with the initiation of true labor contractions and ends when the cervix is fully dilated. As aids for the readers, Table 1 contains the meaning of the several HRV metrics cited in the following sections, whereas Figure 1 and Table 2 summarize the main findings of the current review. Brain. In neonatal life activation of these centers induces strong stimulation for breathing. 2: Maintaining homeostasis through feedback requires a stimulus, sensor, control center, and effector. 21, 107116. (2021). Available online at: (accessed May 13, 2021)>, Russell, N. E., Higgins, M. F., Kinsley, B. F., Foley, M. E., and McAuliffe, F. M. (2016). Medications youve taken, as well as gestational age could impact FHR patterns. Indeed, several animal studies and even some human studies have shown that many factors (e.g., malnutrition, high level of stress, toxic exposure) during early, mid, and late gestation can impair brain and ANS development/regulation, thus inducing biological and behavioral alterations. A., and Visser, G. H. A. (2010). Hill, M. A. 1975 Feb;45(2):142-6. Cell Tissue Res. From 25 WGA until birth, the vagus nerve myelination, the vagal control by the nucleus ambiguus, and, thus, the PNS rapidly develop, as testified by the appearance of short-term variability in frequency-domain HRV metrics (e.g., HF) and the proportional reduction of long-term variability metrics (e.g., LF), more related to SNS and baroreflex functions (Mulkey and du Plessis, 2018, 2019; Schlatterer et al., 2021). Neonatal Nurs. Circadian variation in gastric vagal afferent mechanosensitivity. The effects of sleep quality and duration in late pregnancy on labor and fetal outcome. Front. Treatments for pregnancy-related lumbopelvic pain: a systematic review of physiotherapy modalities. Early development of sleep and brain functional connectivity in term-born and preterm infants. J. Obstet. 524, 12591269. A., Caulfield, L. E., Costigan, K. A., Merialdi, M., Nguyen, R. H. N., Zavaleta, N., et al. An increase in the heart rate c. An increase in stroke volume d. No change a. 18, 459464. Sci. 57:101. doi: 10.3345/kjp.2014.57.3.101. The brainintestinal mucosaappendix microbiomebrain loop. doi: 10.1177/15353702-0323006-05, Zheng, J., Xiao, X., Zhang, Q., Mao, L., Yu, M., and Xu, J. The definition of stress has evolved through time, but it is now accepted that a stressor is an uncontrollable environmental demand that exceeds the physiological imbalance of the organism (Selye, 1950; Koolhaas et al., 2011). Dev. Believed to be an abnormal FHR pattern, late decelerations indicate a reduction in heart rate, usually after a uterine contraction. Supine position with manual restraint for flexion seems to have positive effects on ANS as measured through HRV (Gomes et al., 2019). 20, S31S36. A., Porges, S. W., Scanlon, J. W., Alemi, B., and Scanlon, K. B. Dev. Reprod Fertil Dev. 27, 197200. Immediate and delayed effects of antenatal corticosteroids on fetal heart rate: a randomized trial that compares betamethasone acetate and phosphate, betamethasone phosphate, and dexamethasone. Gynecol. doi: 10.1016/j.heliyon.2019.e01300, Pavlov, V. A., and Tracey, K. J. Effects of antihypertensive drugs on the unborn child. doi: 10.1097/EDE.0b013e31822546fd. doi: 10.1038/jes.2013.19, Dogra, Y., Suri, V., Aggarwal, N., and Dogra, R. K. (2019). Gynecol. Interestingly, the analysis of specific HRV metrics, for instance, SDNN (more related to global neuroautonomic regulation), RMSSD (more related to vagal modulation), and PE, can help identify the actual behavioral state and, therefore, detect potential problems in neurodevelopment whether incoherence between HRV and body movements is detected (Schneider et al., 2008; Brndle et al., 2015). Front. The effects of maternal hyperoxia on fetal breathing movements, body movements and heart rate variation in growth retarded fetuses. In order to prevent severe brain injury from a lack of oxygen, your doctor must revive the fetus and quickly address the source of late decels. Fetal Neonatal Med. Dev. Autonomic development in preterm infants is associated with morbidity of prematurity. 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. (2018). 8:721. doi: 10.3389/fphys.2017.00721, Frasch, M. G., Burns, P., Benito, J., Cortes, M., Cao, M., Fecteau, G., et al. Dev. Cochrane Database Syst. General movements quality, as well as their variability and modulation in intensity and velocity, could be valid indicators of fetal neurodevelopment, in particular concerning supra-spinal control on motor activity (Moreira Neto and Porovic, 2018). Maternal and paternal occupational exposure to agricultural work and the risk of anencephaly. Little has changed in the physical devices that record fetal heart rate and contractions. doi: 10.1038/s41398-021-01198-w, Hanamsagar, R., and Bilbo, S. D. (2016). 2005 Oct;99(4):1477-82, Lear CA, Galinsky R, Wassink G, Yamaguchi K, Davidson JO, Westgate JA, Bennet L, Gunn AJ. Publ. Eur J Obstet Gynecol Reprod Biol. Effects of obstetric analgesics and anesthetics on the neonate. 230, 376388. 598, 249263. 1993;19:105-11. Invest. Effect of epidural analgesia on the fetal heart rate. Psychiatry 11, 112. J. Med. Int. Ann. Drugs to Support Fetal Growth Synthetic glucocorticoids (sGCs) are the therapy of choice to support fetal maturation for the risk of preterm delivery. BJOG Int. A study with autonomic blocking agents in fetal lambs. IX: prolonged pregnancy. J. Obstet. doi: 10.1016/j.mehy.2008.09.033, Cahill, A. G., Mathur, A. M., Smyser, C. D., Mckinstry, R. C., Roehl, K. A., Lpez, J. D., et al. Labor in humans is certainly associated with physiological changes, most of which are regulated by ANS (Sanghavi and Rutherford, 2014; Soma-Pillay et al., 2016). In particular, we will study what events can interfere with the correct development of these two systems by analyzing the evidence from preclinical and clinical studies in this regard, with the aim of preventing potential complications with long-term consequences. Catecholamine mediated effects are relatively slow reflecting their half-life of 2 to 3 minutes. Off. Decelerations were present when there was mild hypertension during the compression but they were also present when marked hypotension accompanied the compression. Assessed occupational exposure to chlorinated, aromatic and Stoddard solvents during pregnancy and risk of fetal growth restriction. Ann. PLoS ONE 12:e0180167. 12:20160545. doi: 10.1098/rsbl.2016.0545, Gallup, A. C., and Eldakar, O. T. (2013). An examination of changes in maternal neuroimmune function during pregnancy and the postpartum period. 39, 2837. Bone Jt. Biological mechanisms that might underlie iron's effects on fetal growth and preterm birth. A. While late decelerations sometimes point to an abnormally low concentration of fetal blood oxygen, various other factors could be at play. (2020). Is less noise, light and parental/caregiver stress in the neonatal intensive care unit better for neonates? BJOG Int. Am. Physiol. In particular, a steep rise in PNS tone can be detected around 3738 WGA and basal fetal cardiovascular function becomes more influenced by the PNS. 161, 771774. 2007 Sep;197(3):236.e1-11. Care Med. . Non-invasive biomarkers of fetal brain development reflecting prenatal stress: an integrative multi-scale multi-species perspective on data collection and analysis. Am J Obstet Gynecol. Regul. [Low back pain during pregnancy. Am. Correlation between human nervous system development and acquisition of fetal skills: an overview. Baltimore, MD: Johns Hopkins University Press. Reproduction 60, 193199. Gender-specific evolution of fetal heart rate variability throughout gestation: a study of 8823 cases. Subst. 8, 173179. From maternal diet to neurodevelopmental disorders: a story of neuroinflammation. The following text describes the principal physiological pathways that control heart rate and influence heart rate variability. Fetal heart rate variability responsiveness to maternal stress, non-invasively detected from maternal transabdominal ECG. doi: 10.1080/02724999208250616, Ledger, W. J., and Blaser, M. J. Early Hum. 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. Diagn. Int. During this period, yawning develops (Borsani et al., 2019). Child. The most frequently observed symptoms are: low back pain, headache, pelvic girdle pain (PGP), leg cramps, breast tenderness, abdominal pain, and ligament pain (Davis, 1996; Jarrell, 2017; Lutterodt et al., 2019). It is instead well known that methylmercury from seafood impairs the higher centers of cardiac autonomic function (Karita et al., 2018), leading to severe ANS abnormalities (Srensen et al., 1999; Grandjean et al., 2004; Murata et al., 2006; Gribble et al., 2015). Epidemiol. doi: 10.1038/s41390-021-01497-4. Maturation of the human fetal startle response: evidence for sex-specific maturation of the human fetus. 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). Transl. Pediatrics 144::e20190128. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). Invest. BJOG Int. Med. J. Autism Dev. Changing patterns of birth asphyxia and trauma over 20 years. The fetal heart rate pattern we observe is the combined results of many physiological actions. Maternal perfusion in the intervillous space is generally maintained during the early part of a uterine contraction. Persistent low variability is concerning, especially when present on admission or associated with decelerations and tachycardia.16 Low variability must not be ignored, but it appears that moderate variability does not guarantee the absence of acidemia. Effect of epidural labor analgesia on fetal heart rate and neonatal outcome. Biol. Biol. doi: 10.1017/S095457942000142X, Hoyer, D., Kowalski, E.-M., Schmidt, A., Tetschke, F., Nowack, S., Rudolph, A., et al. The endotoxemia, through lipopolysaccharide molecules, seems to interfere with the cardiac pacemaker synchronization system, altering the fHRV pattern (Frasch and Giussani, 2020). However, it is important to highlight that so far fHR monitoring has not been enough to prevent fetal injury during labor and, consequently, long-term complications. Review of sleep-EEG in preterm and term neonates. Development of fetal and neonatal sleep and circadian rhythms. Neuroscience 338, 207219. 36. doi: 10.1515/JPM.2008.059, Schulz, L. C. (2010). Early Hum. Fertil. Antenatal interventions based upon fetal surveillance of the daily opioid-exposed fetus: a descriptive analysis. 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). Neural System Development - Embryology. A key role in the control of inflammation is played by the CAP and a functional neuroimmunological link in the fetus has been shown to improve postnatal health and brain injury (Frasch et al., 2016; Liu et al., 2016). In this model hypertension followed by baroreceptor response were proposed as the key steps stimulating the cardioinhibitory center and causing slowing of the heart rate mediated via the vagus. Autonomic responses to sighs in healthy infants and in victims of sudden infant death. Electronic storage of vast amounts of clinical data and tracings makes it feasible to study rare outcomes like severe metabolic acidemia or hypoxic ischemic encephalopathy. Fetal programming of neuropsychiatric disorders. Hypothermia Temp. Hull J, Dodd KL. Moreover, some studies have highlighted that the same factors can differently affect development based on the exposure period (i.e., early vs. late gestation) (Schulz, 2010; Gartstein and Skinner, 2018; Kasahara et al., 2020, 2021). 37, 954967. doi: 10.1111/j.1742-7924.2010.00142.x, Parris, K. M., Amabebe, E., Cohen, M. C., and Anumba, D. O. Indeed, dysfunctional CAP can fail in regulating inflammation, thus letting the immune system go unchecked and free to induce tissue damage, shock, and even death, whereas, on the other hand, a functional CAP can prevent microglia activation, thus showing a neuroprotective effect (Garzoni et al., 2013; Frasch et al., 2016). J. Nurs. (1997). 114, 11941201. Regarding vagal activity in fetuses, not all the authors agree in observing significative sex-related differences (Oguch and Steer, 1998; DiPietro et al., 2004; Lange et al., 2005; Bhide and Acharya, 2018), even when the same methodologies were used. At birth, the higher cortical networks controlling the ANS increase their connectivity (Schlatterer et al., 2021) and, in low-risk newborns at around 1 day of age, coherence between electrocortical activity and brainstem-mediated autonomic tone, especially parasympathetic, can be easily detected (Mulkey et al., 2021). The onset of fetal breathing movements, in particular, induces a variation in the main vagal nerve activity parameters: RMSSD and HF power increase, while LH/HF power decreases. Frasch, M. G., Szynkaruk, M., Prout, A. P., Nygard, K., Cao, M., Veldhuizen, R., et al. The intrapartum deceleration in center stage: a physiologic approach to the interpretation of fetal heart rate changes in labor. Garabedian C, De Jonckheere J, Butruille L, Deruelle P, Storme L, Houfflin-Debarge V. Understanding fetal physiology and second line monitoring during labor. Nutrients 7, 20012014. 128:1443. doi: 10.1111/1471-0528.16674, Gold, N., Herry, C. L., Wang, X., and Frasch, M. G. (2021). 135, 7177. 130, 403407. doi: 10.3109/14767058.2011.600370. (2021). which intrinsic homeostatic response is the fetus demonstrating . Immunol. Nurs. 140, 702706. Psychosomatics and psychopathology: looking up and down from the brain. doi: 10.2147/JIR.S248382, Haraldsdottir, K., Watson, A. M., Goss, K. N., Beshish, A. G., Pegelow, D. F., Palta, M., et al. Sleep-disordered breathing during pregnancy. The association between fetal heart rate patterns and fetal movements in pregnancies between 20 and 30 weeks' gestation. Expert Help. 31, 7085. J. doi: 10.1007/s40572-015-0053-0, Gutke, A., Betten, C., Degerskr, K., Pousette, S., and Olsn, M. F. (2015). A., Tsai, A. S., Ghaemi, M. S., Han, X., Ando, K., et al. Feedback may be negative or positive. University of Erlangen Nuremberg, Germany. Thorax 57, 555558. doi: 10.1111/mono.v80.3, DiPietro, J. 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). 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). Early Hum. Microbiomemicroglia connections via the gutbrain axis. J Appl Physiol (1985). doi: 10.1006/drev.1998.0452, Koletzko, B., Cremer, M., Flothktter, M., Graf, C., Hauner, H., Hellmers, C., et al. doi: 10.1111/jog.12619. Physiol. Rev. MF has patents on aECG (WO2018160890A1) and EEG technologies for fetal monitoring (US9215999). (2014). The clinical goal of electronic fetal monitoring is to identify fetuses with increased risk of hypoxic injury so that intervention can avoid adverse outcome without also causing excessive numbers of unnecessary interventions. Dev. doi: 10.1111/aogs.13437, Boehm, F. H., Woodruff, L. F., and Growdon, J. H. (1975). (2019). Med. Once deceleration starts, it takes about 20 to 30 seconds to reach its lowest point. (2015). These processes can be implemented through cell autonomous or intercellular signaling. Behav. Front. Smoke and alcohol exposure can induce in premature newborns higher sympathetic function, lower parasympathetic function, and had less cardiac autonomic adaptability (Mulkey and du Plessis, 2019). A. Baroreceptor B. Catecholamine C. Sympathetic correct answerA. Hum. doi: 10.4274/tjod.galenos.2019.59932. Heart rate variability. 181, 816821. Available online at: (accessed April 23, 2021). Immunol. doi: 10.1016/0002-9378(82)90812-2, Spinillo, A., Viazzo, F., Colleoni, R., Chiara, A., Maria Cerbo, R., and Fazzi, E. (2004). Rev. Indeed, in preterm infants, both too high or too low oxygenation can be dangerous for the nervous system. 82, 417436. Pelvic girdle pain and low back pain in pregnancy: a review. Pathogen-induced heart rate changes associated with cholinergic nervous system activation. 179, 551569. N. Y. Acad. Brain. In the same way, stress relief during pregnancy, skin-to-skin contact, and social interactions between newborns and parents/caregivers can help newborns tune their ANS, reduce stress, increase resilience, and improve their neural plasticity (Horne, 2018; Mulkey and du Plessis, 2018; Manzotti et al., 2019; Antonelli et al., 2021). The critical role of the central autonomic nervous system in fetal-neonatal transition. Similar hints can also be gained by monitoring organ development due to the research regarding the CAP and the systemic interactions of the vagus nerve (Bonaz et al., 2021). PeriGen User Community. Sustained neurobehavioral effects of exposure to SSRI antidepressants during development: molecular to clinical evidence. doi: 10.1038/pr.2016.155, Bautista, L., and George, R. B. Neurosci. Sleep 35, 177186. 23, 233246. 37, 95110. This is the injection of an anesthetic into your spinal epidural space to eliminate pelvic pain during labor and delivery. Neurosci. Novel heart rate parameters for the assessment of autonomic nervous system function in premature infants. 41, 769775. Decelerations more closely followed cerebral oxygenation. Comp. Glucocorticoid programming. Fetal yawning, in Frontiers of Neurology and Neuroscience, ed. Umbilical cord blood gases were: pH 6.88, PCO2 114, PO2 10, bicarbonate 15, base excess (-) 20. BMC Pregnancy Childbirth 13:111. doi: 10.1186/1471-2393-13-111, Peterson, L. S., Stelzer, I. doi: 10.2174/157488606775252593, De Rogalski Landrot, I., Roche, F., Pichot, V., Teyssier, G., Gaspoz, J.-M., Barthelemy, J.-C., et al. For this reason, before birth neuroendocrine signaling (e.g., catecholamines, cortisol, thyroid hormones, and renin-angiotensin) surges, and SNS outflow from CAN (e.g., hypothalamus, cortical, and brainstem centers) greatly increases. Can. Geburtsh. 201, 10021006. 27, 201209. (2015). Environ. Fetal heart rate is a vital indicator of your babys health. The catecholamines, epinephrine and norepinephrine, secreted from the adrenal, are both hormones and neurotransmitters. FC, MC, SV, CV, and AM conceptualized the paper. Detection of maternal and fetal stress from the electrocardiogram with self-supervised representation learning. (2018). Influence of maternal, obstetric and fetal risk factors on the prevalence of birth asphyxia at term in a Swedish urban population. (2008). Microbiota and neurodevelopmental windows: implications for brain disorders. Fetal Diagn. In the presence of very severe acidemia (pH=6.96) they could not be eliminated by vagal blockade. Standards of measurement, physiological interpretation, and clinical use. Fish intake during pregnancy and foetal neurodevelopmenta systematic review of the evidence. (2007). Since, according to the Polyvagal theory (Beauchaine et al., 2007), the social/emotional development is related to the vagal system, any insult such as maternal distress suffered during the autonomic trajectory development will interfere with the maturation of the cerebral cortices structures and of the ANS disrupting the development of the Social Engagement System of the child (Porges and Furman, 2011). The cervix undergoes biochemical changes that increase its elasticity. Gynaecol. Scand. Hormones, pregnancy, and autoimmune diseases. Rep. 7:45645. doi: 10.1038/srep45645, Bassols, J., Serino, M., Carreras-Badosa, G., Burcelin, R., Blasco-Baque, V., Lopez-Bermejo, A., et al. Cochrane Database Syst. Lett. Dev. 14:601939. doi: 10.3389/fnbeh.2020.601939, Sherer, M. L., Posillico, C. K., and Schwarz, J. M. (2017). doi: 10.1016/j.ajog.2019.04.029, Flenady, V., Ellwood, D., Bradford, B., Coory, M., Middleton, P., Gardener, G., et al. Hum. Theyre a sign of hampered blood flow to your placenta, which might trigger imminent fetal hypoxia (or a lack of oxygen for fetal tissues). Moreover, it seems that monitoring FMs could contribute to creating a primitive maternalchild bonding, even before birth (Flenady et al., 2019). Autonomic responses of premature newborns to body position and environmental noise in the neonatal intensive care unit. Child Health 23, 285291. New York, NY: W. W. Norton. 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