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Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript. Help us improve our products. Sign up to take part. This study aimed to characterize early neonatal microvascular function after preeclamptic pregnancy with respect to infant sex and in utero growth.

Peripheral microvascular blood flow was examined prospectively from 6 to 72 h of age using laser Doppler flowmetry in a cohort of term infants of normotensive women and women with late-onset preeclampsia.

Altered fetal microvascular structure and function in response to sed preeclampsia may vp in sexually dimorphic patterns of fetal growth and account for alterations in neonatal microvascular adaptation after birth. Preeclampsia is a leading cause of morbidity and mortality in mothers and infants 1. It is currently believed to be a 2-stage disease 2 with shallow cytotrophoblast invasion sxe maternal spiral arterioles initially resulting in sxe insufficiency. The subsequent release of soluble factors, such as endoglin and soluble fms-like tyrosine kinase 1 3 into the feto-maternal circulation has been proposed to induce maternal systemic endothelial dysfunction and the clinical manifestations of the disease 4.

We have previously shown fetal sex-specific effects on maternal physiology and placental function in pregnancies complicated by inflammatory stressors 56. With respect to preeclampsia, maternal endothelial dysfunction was greater in the presence of a male fetus 6.

Similarly, male neonates demonstrate greater morbidity and mortality after preeclamptic pregnancy 7. Preeclampsia is known to be associated with adaptive changes in the fetal circulation and placentally derived factors implicated in the pathogenesis of the maternal manifestations of the disease are known to contribute to the development of neonatal thrombocytopenia and growth restriction 8.

However, the influence of sex on endothelial dysfunction in neonates born to preeclamptic mothers has not previously been investigated. Neonatal endothelial dysfunction and abnormal xex of vascular resistance may have a major role in cardiovascular instability in newborn infants 9 and disturbances of regional blood flow are known to play a crucial role in the pathogenesis of several significant neonatal morbidities 10 The microcirculation of neonate is subject to considerable changes in the first days of extrauterine life 12 and is altered in response to mode of delivery 13hypoxia 14and ischemia We have recently demonstrated that infants born prematurely exhibit sex-specific differences in microvascular blood flow and vasodilatory capacity Males were found to exhibit microvascular dysregulation characterized by inappropriately low basal tone, and significantly, these differences were related to illness severity in the immediate newborn period In this study, we examined skin microvascular blood flow in term infants of normotensive and preeclamptic sex.

We hypothesized that, in light of the influence of fetal gender on maternal physiology in preeclamptic pregnancy and the sex-specific differences in microvascular blood flow after preterm birth, similar differences in neonatal microvascular adaptation would be observed after preeclampsia with males exhibiting dysregulated blood flow and inappropriate vasodilatation.

Pregnant women with a diagnosis of preeclampsia meeting the guidelines of the Australian Society for the Study of Hypertension in Pregnancy 18 and normotensive controls were recruited on presentation at the John Hunter Hospital as part of a prospective cohort study according to a previously described protocol 6.

None of the preeclamptic subjects were defined as having severe preeclampsia. All mothers were aged between 18 and 40 y, had singleton pregnancies and were nonsmokers. Factors that could have affected fetal-neonatal vascular development, such as maternal diabetes, essential hypertension, maternal smoking, neonatal asphyxia, chromosomal disorders, or congenital malformation excluded admission to this study. Women with preeclampsia may have received some or a combination of the following drugs: labetalol, hydralazine, and [alpha]-methyldopa before delivery.

Laser Doppler flowmetry assesses the function of blood vessels of sex peripheral microvasculature of the skin Low-intensity laser light is reflected from moving blood cells in the skin circulation, and a measurement of blood flow obtained. Investigations were performed with the infants in a thermo-neutral environment at least 1 h after the infant was last fed.

Microcirculatory recordings were performed at times when the infant was lying supine, quietly, at 6, 24, and 72 h of age. Skin basal blood flow was then recorded for 5 sed before standard provocations to allow for comparison between different studies and subjects, as sexx described After estimation of basal blood flow, lower limb blood flow was occluded using a standard sphygmomanometer to allow biologic zero for each experiment Only recording areas free from movement artifacts were analyzed.

Baseline microvascular blood flow did not demonstrate a normal distribution and was therefore log-transformed for all statistical analysis.

The characteristics of the mothers and newborns are shown in Table 1. There were no significant differences in vk age, gravidity, or parity between the groups. There was no significant difference in terms of proportion of small for gestational age infants, mode of delivery, proportion of male infants, or 5-min Apgar score between the groups. For infants lv to preeclamptic mothers, there was no difference between the sexes with respect to antenatal exposure to antihypertensive therapies.

Post-hoc analysis showed that the male infants of preeclamptic mothers had no significant increase in blood flow over time. There was no significant difference in baseline microvascular blood flow between the male groups at 24 sex 72 h. Female infants born to normotensive women showed no significant change in peripheral baseline microvascular blood flow with time. Removal of those women receiving antihypertensive treatment made no difference to the observed findings.

There was no significant difference between the preeclamptic and normotensive groups for birth weight percentile in the male infants. This is the first study to report sex-specific differences in the maturation of neonatal peripheral microvascular blood flow after pregnancies complicated by preeclampsia.

Previously, we have reported significant sex-specific differences in basal microvascular blood flow and cl capacity in extremely preterm infants Sexually dimorphic patterns of microvascular adaptation have not, however, been reported at term nor been shown to be influenced by maternal preeclampsia. Previous studies of neonatal microvascular adaptation have reported significant changes both with gestational and postnatal age. Gestational age has been described to have a variable influence on microvascular function with blood flow reported to decrease 2122increase 1523and remain unchanged 24 with increasing gestational age.

The current data demonstrates no relationship with gestational age, within a narrow range, but we have previously shown an inverse relationship over a greater span Reports of temporal changes in neonatal peripheral cutaneous blood flow are similarly conflicting 22 Although microvascular blood flow has been reported to remain unchanged over the first 24 h of life 13other authors have described significant falls between days 1 and 7 12 The current data demonstrates that in term neonates born after preeclamptic pregnancy, female infants exhibit similar baseline microvascular blood flow at 6 h of age to females of normotensive mothers followed by significantly greater microvascular blood flow at 24 and 72 h.

Conversely, male infants do not demonstrate a temporal change in blood flow in sfx presence of preeclampsia but were significantly more vasodilated than males of normotensive mothers at 6 h of age.

Sex-specific differences in temporal changes of microvascular blood flow where also observed in infants of normotensive women. Male infants exhibited a significant increase in blood flow from 6 to 24 h of age whereas female infants demonstrated no change with postnatal age.

However, microvascular blood flow only exhibited a significant difference between male and female infants at vo h of age. We have previously demonstrated a similar sexual dimorphism in preterm infants 16 at 24 h of age. These findings highlight the importance of considering neonatal sex in the assessment of postnatal microvascular adaptation. Furthermore, the timing of any assessment may influence the observed effect.

Unexpectedly, there were sex-specific differences in the fetal growth response to maternal preeclampsia. The female fetus exhibits asymmetric growth with reduced birth weight sex the male fetus maintains normal growth in the presence of preeclampsia.

Data reporting changes in fetal and neonatal body proportion after abnormal pregnancy is limited although infants of preeclamptic mothers have previously been reported to have significantly increased head circumference to chest circumference ratio compared with infants born to normotensive mothers The differing temporal changes in microvascular blood flow and growth strategies demonstrated by male and female fetuses may be secondary to maternal microvascular adaptations in response to preeclampsia.

We have previously examined maternal microvascular blood flow and vasodilatory capacity using laser Doppler flowmetry in pregnancies complicated by preeclampsia and demonstrated that fetal sex was associated with altered maternal vascular function 6.

Specifically, maternal endothelial dysfunction, characterized by peripheral microvascular vasoconstriction, was greater in preeclamptic pregnancies with a male fetus.

The normal growth of male neonates of preeclamptic pregnancies suggests that maternal adaptive increases in peripheral microvascular tone maintain vll blood flow despite maternal hypertension and placental insufficiency. This, in turn, leads to increased microvascular blood flow in the immediate postnatal period, which normalizes by 24 h of age. In the female neonate, the progressive postnatal increase in microvascular blood flow may be a compensatory postnatal response to intrauterine redistribution of blood flow away from the peripheral circulation to the brain and major organs.

We have shown in preeclamptic pregnancy that microvascular function in those women pregnant with a female fetus is not significantly different from the normotensive pregnant controls 6.

These observations and the current data support a lack of compensatory peripheral vascular response zex maternal hypertension, reduced uteroplacental blood flow and subsequent female fetal hemodynamic redistribution and alterations in female fetal growth and development However, there is increasing sdx that babies born to mothers with preeclampsia at term have fetal growth similar to that sex babies born to normotensive mothers 27 These observations are in keeping with preeclampsia being a heterogeneous disorder Interestingly both male and female fetuses sex preeclamptic pregnancies had greater head circumference centile relative to neonates born to normotensive mothers.

This may correspond with the theory that the underlying evolutionary reason for the persistence of preeclampsia is to sustain brain growth in the presence of placental restriction 30 Glucocorticoids may play a central role in conferring the sex-specific differences in placental function and fetal growth. Our previous studies support a sex-specific difference in the response of male and female fetuses to zex rise in cortisol.

Glucocorticoids exhibit short-term vasodilator effects on sexx placental circulation 35 but long-term exposure may potentate vasoconstrictive responses. One potential pathway by which glucocorticoids may promote vasoconstriction is via the potent vasoconstrictor esx endothelin Preeclampsia is associated with elevated endothelin-1 in both the maternal 36 and fetal compartments 37 and glucocorticoids have been shown to potentate its vasoconstrictive actions.

The female fetus appears to be sensitive to changes in glucocorticoid exposure and therefore may exhibit increased placental vasoconstriction 38 and uteroplacental insufficiency. The male placenta and fetus, conversely, is resistant to changes in glucocorticoid exposure 39 with the potential maintenance of uteroplacental blood flow, fetal growth, and development.

Glucocorticoids may also alter fetal-placental vascular morphology. In the rat, dexamethasone administration inhibited vascular endothelial growth factor production and reduced placental angiogenesis in the late third trimester The influence of maternally administered antihypertensive agents on neonatal vascular function is a potential confounding variable in this study. The effect of antenatal antihypertensive exposure on neonatal microvascular adaptation after delivery has not previously been investigated.

However, previous studies investigating neonatal adaptation after hypertensive pregnancy have demonstrated no differences in cardiovascular function, and in particular neonatal hypotension or rebound hypertension, in infants exposed to labetalol 41hydralazine 42or methyldopa 43 when compared with controls.

In addition, there was no ssx difference in the proportion of male and female infants of preeclamptic mothers exposed to each antihypertensive agent. These sex-specific differences in microvascular flow may be a consequence of altered structural microvascular changes microvascular density and microvascular compliance in addition to differences in endothelial sex with implications for future cardiovascular development However, previous studies of microcirculatory density in neonates have failed to demonstrate altered microvascular structure despite marked differences srx microvascular blood flow, with small sample size preventing investigation of sex-specific differences Further studies should, therefore, examine potential sex-specific differences in maternal and neonatal microvascular structure and function in addition to the relationships between severity of maternal disease including measures of circulating endoglin and soluble fms-like tyrosine kinase 1uteroplacental blood flow, and fetal growth.

We have demonstrated for the first time sex-specific differences in neonatal microvascular blood flow after pregnancy complicated by seex. These sex-specific differences are evident in the immediate newborn period, a time of physiologic instability after birth. The significantly greater microvascular vasodilatation observed in male infants may impact upon the transitional circulation 17 and be a one factor contributing to the excess of morbidity associated with male sex after preeclamptic pregnancy.

The sex mechanisms resulting in this sexually dimorphic pattern of microvascular function have not been fully lv and warrant further investigation. Semin Perinatol 27 : — Lancet : 53— N Engl J Med : —

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