Roles of parasympathetic outflow and sympathetic outflow in the cardiovascular response to brief umbilical cord occlusion in fetal sheep

Recher, Morgan; Prevost, Arthur Lauriot Dit; Sharma, Dyuti; Jonckheere, Julien De; Garabédian, Charles; Storme, Laurent

doi:10.1371/journal.pone.0254155

Cited by 5 publications

(4 citation statements)

References 33 publications

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“…During the first and second quarters, FHR during the reperfusion period was considerably higher in the vagotomy group than in the control group, probably reflecting the unopposed effects of high circulating catecholamines in the absence of parasympathetic tone (Galinsky et al., 2014, 2016; Lear, Beacom, Kasai, et al., 2020; Recher et al., 2021). In turn, this indicates that there is high parasympathetic activity between UCOs that markedly restrains FHR in control fetuses (Lear, Beacom, Westgate, et al., 2020; Lear, Westgate, Kasai, et al., 2020; Recher et al., 2021; Tournier et al., 2022). This tachycardia in the vagotomy group progressively reduced in magnitude, with less difference compared with the control group in the third and fourth quarters.…”

Section: Discussionmentioning

confidence: 98%

“…During the first and second quarters, FHR during the reperfusion period was considerably higher in the vagotomy group than in the control group, probably reflecting the unopposed effects of high circulating catecholamines in the absence of parasympathetic tone (Galinsky et al, 2014(Galinsky et al, , 2016Recher et al, 2021). In turn, this indicates that there is high parasympathetic activity between UCOs that markedly restrains FHR in control fetuses Recher et al, 2021;Tournier et al, 2022). This tachycardia in the vagotomy group progressively reduced in magnitude, with less difference compared with the control group in the third and fourth quarters.…”

Section: Control Of Fetal Heart Rate During and Between Decelerationsmentioning

confidence: 99%

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Dissecting the contributions of the peripheral chemoreflex and myocardial hypoxia to fetal heart rate decelerations in near‐term fetal sheep

Lear

Beacom

Dhillon

et al. 2023

The Journal of Physiology

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Brief repeated fetal hypoxaemia during labour can trigger intrapartum decelerations of the fetal heart rate (FHR) via the peripheral chemoreflex or the direct effects of myocardial hypoxia, but the relative contribution of these two mechanisms and how this balance changes with evolving fetal compromise remain unknown. In the present study, chronically instrumented near‐term fetal sheep received surgical vagotomy (n = 8) or sham vagotomy (control, n = 11) to disable the peripheral chemoreflex and unmask myocardial hypoxia. One‐minute complete umbilical cord occlusions (UCOs) were performed every 2.5 min for 4 h or until arterial pressure fell below 20 mmHg. Hypotension and severe acidaemia developed progressively after 65.7 ± 7.2 UCOs in control fetuses and 49.5 ± 7.8 UCOs after vagotomy. Vagotomy was associated with faster development of metabolic acidaemia and faster impairment of arterial pressure during UCOs without impairing centralization of blood flow or neurophysiological adaptation to UCOs. During the first half of the UCO series, before severe hypotension developed, vagotomy was associated with a marked increase in FHR during UCOs. After the onset of evolving severe hypotension, FHR fell faster in control fetuses during the first 20 s of UCOs, but FHR during the final 40 s of UCOs became progressively more similar between groups, with no difference in the nadir of decelerations. In conclusion, FHR decelerations were initiated and sustained by the peripheral chemoreflex at a time when fetuses were able to maintain arterial pressure. After the onset of evolving hypotension and acidaemia, the peripheral chemoreflex continued to initiate decelerations, but myocardial hypoxia became progressively more important in sustaining and deepening decelerations. Key points Brief repeated hypoxaemia during labour can trigger fetal heart rate decelerations by either the peripheral chemoreflex or myocardial hypoxia, but how this balance changes with fetal compromise is unknown. Reflex control of fetal heart rate was disabled by vagotomy to unmask the effects of myocardial hypoxia in chronically instrumented fetal sheep. Fetuses were then subjected to repeated brief hypoxaemia consistent with the rates of uterine contractions during labour. We show that the peripheral chemoreflex controls brief decelerations in their entirety at a time when fetuses were able to maintain normal or increased arterial pressure. The peripheral chemoreflex still initiated decelerations even after the onset of evolving hypotension and acidaemia, but myocardial hypoxia made an increasing contribution to sustain and deepen decelerations.

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Section: Discussionmentioning

confidence: 98%

“…During the first and second quarters, FHR during the reperfusion period was considerably higher in the vagotomy group than in the control group, probably reflecting the unopposed effects of high circulating catecholamines in the absence of parasympathetic tone (Galinsky et al, 2014(Galinsky et al, , 2016Recher et al, 2021). In turn, this indicates that there is high parasympathetic activity between UCOs that markedly restrains FHR in control fetuses Recher et al, 2021;Tournier et al, 2022). This tachycardia in the vagotomy group progressively reduced in magnitude, with less difference compared with the control group in the third and fourth quarters.…”

Section: Control Of Fetal Heart Rate During and Between Decelerationsmentioning

confidence: 99%

Dissecting the contributions of the peripheral chemoreflex and myocardial hypoxia to fetal heart rate decelerations in near‐term fetal sheep

Lear

Beacom

Dhillon

et al. 2023

The Journal of Physiology

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“…Comparatively, during the strongest contraction, the preterm group seems to behave similarly to parasympathetic blocked subjects in preclinical studies. For example, parasympathetic blocked sheep fetuses (through vagotomy or atropine administration) present higher FHR during and after umbilical cord occlusions in comparison with a control group (non-blocked fetuses) (35,38).…”

Section: Discussionmentioning

confidence: 99%

Uterine activity modifies the response of the fetal autonomic nervous system at preterm active labor

et al. 2023

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BackgroundThe autonomic nervous system of preterm fetuses has a different level of maturity than term fetuses. Thus, their autonomic response to transient hypoxemia caused by uterine contractions in labor may differ. This study aims to compare the behavior of the fetal autonomic response to uterine contractions between preterm and term active labor using a novel time-frequency analysis of fetal heart rate variability (FHRV).MethodsWe performed a case-control study using fetal R-R and uterine activity time series obtained by abdominal electrical recordings from 18 women in active preterm labor (32−36 weeks of gestation) and 19 in active term labor (39−40 weeks of gestation). We analyzed 20 minutes of the fetal R-R time series by applying a Continuous Wavelet Transform (CWT) to obtain frequency (HF, 0.2−1 Hz; LF, 0.05−0.2 Hz) and time-frequency (Flux0, Flux90, and Flux45) domain features. Time domain FHRV features (SDNN, RMSSD, meanNN) were also calculated. In addition, ultra-short FHRV analysis was performed by segmenting the fetal R-R time series according to episodes of the uterine contraction and quiescent periods.ResultsNo significant differences between preterm and term labor were found for FHRV features when calculated over 20 minutes. However, we found significant differences when segmenting between uterine contraction and quiescent periods. In the preterm group, the LF, Flux0, and Flux45 were higher during the average contraction episode compared with the average quiescent period (p<0.01), while in term fetuses, vagally mediated FHRV features (HF and RMSSD) were higher during the average contraction episode (p<0.05). The meanNN was lower during the strongest contraction in preterm fetuses compared to their consecutive quiescent period (p=0.008).ConclusionThe average autonomic response to contractions in preterm fetuses shows sympathetic predominance, while term fetuses respond through parasympathetic activity. Comparison between groups during the strongest contraction showed a diminished fetal autonomic response in the preterm group. Thus, separating contraction and quiescent periods during labor allows for identifying differences in the autonomic nervous system cardiac regulation between preterm and term fetuses.

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“…Individual periods of acute hypoxaemia are sensed by the chemoreceptors of the aortic arch and carotid body, activating the peripheral chemoreflex and increasing parasympathetic and sympathetic neural outflow. The parasympathetic arm triggers a rapid fall in FHR (Lear et al 2021;Recher et al 2021), observed clinically as intrapartum decelerations (Lear et al 2016b). The sympathetic arm triggers profound peripheral vasoconstriction across multiple vascular beds (Giussani et al 1993), which increases arterial blood pressure to All studies were undertaken at approximately 0.85 of gestation, broadly equivalent to the neural maturation of the full-term human fetus.…”

Section: The Physiology Of Labour and Fetal Adaptationmentioning

confidence: 99%

Physiological control of fetal heart rate variability during labour: implications and controversies

Tournier

Beacom

Westgate

et al. 2022

The Journal of Physiology

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The interpretation of fetal heart rate (FHR) patterns is the only available method to continuously monitor fetal well‐being during labour. One of the most important yet contentious aspects of the FHR pattern is changes in FHR variability (FHRV). Some clinical studies suggest that loss of FHRV during labour is a sign of fetal compromise so this is reflected in practice guidelines. Surprisingly, there is little systematic evidence to support this observation. In this review we methodically dissect the potential pathways controlling FHRV during labour‐like hypoxaemia. Before labour, FHRV is controlled by the combined activity of the parasympathetic and sympathetic nervous systems, in part regulated by a complex interplay between fetal sleep state and behaviour. By contrast, preclinical studies using multiple autonomic blockades have now shown that sympathetic neural control of FHRV was potently suppressed between periods of labour‐like hypoxaemia, and thus, that the parasympathetic system is the sole neural regulator of FHRV once FHR decelerations are present during labour. We further discuss the pattern of changes in FHRV during progressive fetal compromise and highlight potential biochemical, behavioural and clinical factors that may regulate parasympathetic‐mediated FHRV during labour. Further studies are needed to investigate the regulators of parasympathetic activity to better understand the dynamic changes in FHRV and their true utility during labour.

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Roles of parasympathetic outflow and sympathetic outflow in the cardiovascular response to brief umbilical cord occlusion in fetal sheep

Cited by 5 publications

References 33 publications

Dissecting the contributions of the peripheral chemoreflex and myocardial hypoxia to fetal heart rate decelerations in near‐term fetal sheep

Dissecting the contributions of the peripheral chemoreflex and myocardial hypoxia to fetal heart rate decelerations in near‐term fetal sheep

Uterine activity modifies the response of the fetal autonomic nervous system at preterm active labor

Physiological control of fetal heart rate variability during labour: implications and controversies

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