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The Physiology of Intrapartum Fetal Compromise at Term Jessica M Expert Review ajog.org The physiology of intrapartum fetal compromise at term Jessica M. Turner, MBChB MRCOG; Murray D. Mitchell, FRCOG DPhil(Oxon); Sailesh S. Kumar, FRCOG FRANZCOG DPhil(Oxon) CMFM n the majority of women, placental I function is sufficient to allow Uterine contractions in labor result in a 60% reduction in uteroplacental perfusion, appropriate growth of the fetus causing transient fetal and placental hypoxia. A healthy term fetus with a normally throughout pregnancy and to help shield developed placenta is able to accommodate this transient hypoxia by activation of the it from the hypoxic stresses of labor. In peripheral chemoreflex, resulting in a reduction in oxygen consumption and a central- some women, depending on the degree ization of oxygenated blood to critical organs, namely the heart, brain, and adrenals. of placental dysfunction, fetal growth Providing there is adequate time for placental and fetal reperfusion between contrac- restriction may ensue or intrapartum tions, these fetuses will be able to withstand prolonged periods of intermittent hypoxia fetal compromise may develop if the and avoid severe hypoxic injury. However, there exists a cohort of fetuses in whom placenta is not able to meet the extra fetal abnormal placental development in the first half of pregnancy results in failure of demands required during the last few endovascular invasion of the spiral arteries by the cytotrophoblastic cells and inadequate weeks of pregnancy or during labor and placental angiogenesis. This produces a high-resistance, low-flow circulation predis- thereby predispose these infants to hyp- posing to hypoperfusion, hypoxia, reperfusion injury, and oxidative stress within the oxic insults. If severe enough, these can placenta. Furthermore, this renders the placenta susceptible to fluctuations and result in emergency operative birth, reduction in uteroplacental perfusion in response to external compression and stimuli (as death, short-term morbidity, and sig- occurs in labor), further reducing fetal capillary perfusion, placing the fetus at risk of nificant long-term neurodevelopmental inadequate gas/nutrient exchange. This placental dysfunction predisposes the fetus to issues. intrapartum fetal compromise. In the absence of a rare catastrophic event, intrapartum Globally, perinatal hypoxia remains a fetal compromise occurs as a gradual process when there is an inability of the fetal heart major contributor to stillbirth, hypoxic to respond to the peripheral chemoreflex to maintain cardiac output. This may arise as a ischemic encephalopathy (HIE), and consequence of placental dysfunction reducing pre-labor myocardial glycogen stores cerebral palsy; 10% of the global burden necessary for anaerobic metabolism or due to an inadequate placental perfusion be- of disease is attributable to newborn tween contractions to restore fetal oxygen and nutrient exchange. If the hypoxic insult is conditions. It is estimated that world- severe enough and long enough, profound multiorgan injury and even death may occur. wide, 23% of the 4 million neonatal This review provides a detailed synopsis of the events that can result in placental deaths per year occur because of intra- dysfunction, how this may predispose to intrapartum fetal hypoxia, and what protective partum complications.1,2 Of newborns mechanisms are in place to avoid hypoxic injury. who develop HIE, almost 1 million die in Key words: the first month of life and 25% of sur- fetal hypoxia, hypoxic ischemic encephalopathy, inadequate placentation, vivors have long-term sequelae such as intrapartum fetal compromise, peripheral chemoreflex, physiology, placental development From the Mater Research Institute (Drs Turner and Kumar) and Faculty of Medicine (Drs Turner cerebral palsy with intrapartum hypoxia, uterine contractions.5 Uterine contrac- and Kumar), University of Queensland; and accounting for 1 in 5 cases in term tions reduce uteroplacental perfusion by Institute of Health and Biomedical Innovation - 3 6 Centre for Children’s Health Research, Faculty infants. Indeed, the World Health Or- as much as 60% and although most of Health, Queensland University of Technology ganization estimates that disability- fetuses are able to tolerate this reduction (Dr Mitchell), Brisbane, Queensland, Australia. adjusted life years due to neonatal in placental perfusion, there exists a Received Feb. 22, 2019; revised June 26, 2019; encephalopathy, birth asphyxia, and cohort that are unable to and are at risk accepted July 18, 2019. birth trauma are comparable with of hypoxic injury. Fetuses that are unable J.T. and S.K. acknowledge research support by congenital malformations, type II dia- to withstand these periods of intermit- the Mater Foundation. betes, and HIV/AIDS (54,400 million).4 tent hypoxia manifest their compromise Corresponding author: Sailesh Kumar, FRCOG Although rare, unpredictable and in a variety of ways, including heart rate FRANZCOG DPhil(Oxon) CMFM. sailesh. acute catastrophic events such as abnormalities (decelerations, decrease in [email protected] placental abruption, uterine rupture, or beat-to-beat variability etc) and passage 0002-9378/$36.00 cord prolapse are associated with a high of meconium in utero. In extreme cases, ª 2019 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.ajog.2019.07.032 risk of severe fetal hypoxia; 75% of cases if the hypoxic insult is severe enough, in labor occur gradually as a result of brain injury or death can ensue. This MONTH 2019 American Journal of Obstetrics & Gynecology 1 Expert Review ajog.org review will cover the physiology of the placenta. This occurs through the placental perfusion51 and oxygenation.52 placental development, fetal response to processes of vasculogenesis (differentia- Because of a reduction in uteroplacental intrapartum hypoxia at term, and some tion of mesenchymal-derived heman- perfusion, intermittent placental hyp- recent advances in the screening and gioblasts into endothelial cells)27 and oxia, reperfusion injury, and oxidative identification of vulnerable fetuses. angiogenesis (remodeling and expansion stress occurs, with accelerated tropho- of existing vessels either by branching or blast apoptosis and enhanced endo- Placental Development non-branching processes), which are plasmic reticulum stress.53,54 In vitro Development of the placenta involves 2 modulated by vascular endothelial and in vivo studies have demonstrated complex but concurrent processes: growth factor in first half of preg- that repeated ischemiaereperfusion endothelial invasion of the maternal spi- nancy28,29 and placental growth factor events, as seen in labor, result in a sub- ral arteries by cytotrophoblast (CT) cells (PlGF) after 23 weeks gestation.30,31 stantial decline in placental mRNA and development of the fetal vascular Failure of endovascular invasion of and PlGF levels, which in turn further tree. Endothelial invasion initially results the spiral arteries produces a high- activates inflammatory cytokine e in the formation of a trophoblast “plug,” resistance, low-flow circulation that pathways.55 57 Placentae that are at which results in a relatively hypoxic predisposes to hypoperfusion, hypoxia, greatest risk of ischemiaereperfusion milieu (oxygen partial pressure [PaO2] reperfusion injury, and oxidative stress injury are those with aberrant conver- <20 mm Hg) within the intervillous in the placenta.32 This affects placental sion of spiral arteries, resulting in nar- space.7,8 This hypoxic environment is function through several mechanisms— rower vessels with luminal atherosclerotic crucial for early regulation of CT prolif- the persistent high-pressure flow deposits and retention of vascular inner- eration and differentiation.9 The CT plug through the intervillous space (2-3 m/s vation and vasoreactivity.36,58,59 dissipates after 10 weeks of gestation, compared with 10 cm/s in normally resulting in increased placental blood dilated vessels) results in increased sheer Impact of Labor on the Fetus 10 flow and PaO2. Endovascular invasion stress and damage to the syncytio- Although uterine contractions result in by the CTs into the wall of the spiral ar- trophoblasts lining the chorionic villi, a decline in fetal PaO2 by approximately teries involves de-differentiation of thereby compromising the functional 25%,60 the majority of appropriately adhesion molecules and conversion from capacity of the villi for gas and nutrient grown, healthy, term fetuses are able to an epithelial to endothelial phenotype.11 exchange.33,34 Failure of spiral artery withstand the effects of this over a By the late second trimester, the inner conversion renders these vessels suscep- prolonged period of time. Indeed, third of the myometrial spiral arteries are tible to adrenergic stimulation and normal fetuses can cope with a reduc- 12 35,36 exclusively lined by CTendothelial cells, vasoconstriction, resulting in fluc- tion in PaO2 of up to 50% (from a PaO2 replacing the normal vascular smooth tuations in intervillous PaO2 and above 20 mm Hg to as low as 10e12 muscle with a noncontractile matrix that placental hypoxiaereperfusion injury. mm Hg)61,62 because of their high is nonresponsive to neuronal and hor- Failure of CTendovascular invasion also myocardial glycogen stores,63,64 the monal stimuli.13,14 These remodeled results in retention of a “functional presence of vascular shunts, the vessels dilate 4-fold at their terminal sphincter,” an innervated stricture point increased oxygen affinity of HbF, and portion,15 into low-resistance,
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