Undernutrition during the first half of gestation increases the predominance of fetal tissue in late-gestation ovine placentomes

Steyn, Clare; Hawkins, Paul; Saito, Tsukuru; Noakes, D.E.; Kingdom, John; Hanson, Mark A.

doi:10.1016/s0301-2115(01)00321-9

Cited by 43 publications

(37 citation statements)

References 18 publications

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“…Periconceptional undernutrition resulted in a greater proportion of C and D type placentomes, the opposite of the findings in twins, but consistent with other studies of early gestation undernutrition (Steyn et al 2001; Fowden et al 2006). Similar changes have also been reported following dexamethasone exposure in early gestation (Laraya et al 2000) and prolonged hypoxia secondary to altitude (Penninga & Longo, 1998).…”

Section: Discussionsupporting

confidence: 90%

Effects of twin pregnancy and periconceptional undernutrition on maternal metabolism, fetal growth and glucose–insulin axis function in ovine pregnancy

Rumball

Harding

Oliver

et al. 2008

The Journal of Physiology

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Although twins have lower birthweights than singletons, they may not experience the increased disease risk in adulthood reportedly associated with low birthweight. In contrast, another periconceptional event, maternal undernutrition, does not reduce birthweight but does affect fetal and postnatal physiology in sheep. We therefore studied maternal and fetal metabolism, growth and glucose-insulin axis function in late gestation in twin and singleton sheep pregnancies, either undernourished from 60 days before until 30 days after conception or fed ad libitum. We found that twin-bearing ewes had decreased maternal food intake in late gestation and lower maternal and fetal plasma glucose and insulin levels. Twin fetuses had fewer everted placentomes, grew slower in late gestation, and had a greater insulin response to a glucose challenge, but lesser response to arginine. In contrast, periconceptional undernutrition led to increased maternal food intake and a more rapid fall in maternal glucose levels in response to fasting. Periconceptional undernutrition increased the number of everted placentomes, and abolished the difference in insulin responses to glucose between twins and singletons. Thus, the physiology of twin pregnancy is quite different from that of singleton pregnancy, and is probably determined by a combination of factors acting in both early and late gestation. The inconsistency of the relationships between low birthweight and postnatal disease risk of twins may lie in their very different fetal development. These data suggest that twin pregnancy may be another paradigm of developmental programming, and indicate that twins and singletons must be examined separately in any study of fetal or postnatal physiology.

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Section: Discussionsupporting

confidence: 90%

Effects of twin pregnancy and periconceptional undernutrition on maternal metabolism, fetal growth and glucose–insulin axis function in ovine pregnancy

Rumball

Harding

Oliver

et al. 2008

The Journal of Physiology

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“…These data are similar to results for control ewes in studies by Vatnick et al [4], Clarke et al [13], Steyn et al [14], Gardner et al [15], and Osgerby et al [16], as well as for ewes in which the fetal or placental weights were compromised [5,[13][14][15][16][17][18][19][20][21].…”

Section: Discussionsupporting

confidence: 89%

“…Similar to singleton pregnancy, most of the placenta consisted of type A placentomes in twin and triplet pregnancies. Other authors have suggested that, in instances where the placenta is stressed by maternal nutrient restriction [5,13,14,16,18,19], hypoxia [17], or fetectomy [4], a shift occurs in placentomes from type A to more advanced types such as C and D. In these studies, it was suggested that the shift to more advanced types of placentomes was an attempt to rescue the fetus, perhaps because of increased placentome vascularity or blood flow. For example, Vatnick et al [4] reported that when fetectomy was performed on twins there was an increase in the number of more advanced types of placentomes, with fetuses being similar in weight to singletons.…”

Section: Discussionmentioning

confidence: 99%

Effect of Morphology on Placentome Size, Vascularity, and Vasoreactivity in Late Pregnant Sheep1

Vonnahme

Arndt

Johnson

et al. 2008

Biology of Reproduction

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Ovine placentomes vary in shape, with type A placentomes being concave, type D convex, and types B and C intermediate in morphology. It has been speculated that as placentomes advance in type they differ in vascularity and nutrient transport capacity. Our objective was to determine cellularity and vascularity measurements, angiogenic factor expression, and arterial vasoactivity within different morphologic types of placentomes. On Day 130 of gestation, placentomes were collected from multiparous ewes (n = 38) and were evaluated for size, cellularity estimates, angiogenic factor mRNA expression, capillary vascularity (capillary size, capillary surface density [CSD], capillary number density [CND], and capillary area density [CAD]), and vasoreactivity to potassium chloride and angiotensin II. The average weight and size of type A and B placentomes were less (P < 0.01) than those of type C and D placentomes. Placentome morphology did not affect (P > or = 0.24) cotyledonary or caruncular cellularity estimates or percentage of cellular proliferation. Placentome morphology affected (P > or = 0.41) neither caruncular CAD, CND, CSD, or capillary size nor cotyledonary CND, CSD, or capillary size. Cotyledonary CAD was increased (P < 0.01) in type B and D placentomes compared with type A placentomes. Furthermore, placentome type did not affect (P > or = 0.06) angiogenic factor gene expression in the cotyledon or the caruncle. Size, but not morphologic type of placentome, was associated with greater caruncular artery contractility to potassium chloride and angiotensin II (P < 0.01 for both). Placentome size, but not morphologic type, may be important for vascularity and nutrient transfer in the placenta of the pregnant ewe.

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“…Nevertheless one feature of mid-pregnancy undernutrition common to three different research groups is a marked change in placental morphology, namely eversion and increased development of the fetal cotyledon Steyn et al, 2001;Osgerby et al, 2004). This change in morphology is thought to reflect an adaptive compensatory response by the placenta in order to maximize transplacental exchange capacity and maintain fetal growth.…”

Section: Early and Mid-pregnancy Nutritionmentioning

confidence: 99%

Nutritional paradigms of ovine fetal growth restriction: Implications for human pregnancy

et al. 2005

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Low birth weight and prematurity are associated with short inter-pregnancy intervals, low pre-pregnancy weights, insufficient maternal weight gains during pregnancy, multifetal pregnancies and a young maternal age. Improvements in maternal nutritional status are arguably imperative for ensuring an appropriate pregnancy outcome in these vulnerable groups, but ethical boundaries limit these investigations. Experimental paradigms using the pregnant sheep have been widely used to identify the nutritionally sensitive periods of conceptus development. In adult sheep, severe undernutrition during the periconceptual period accelerates maturation of the fetal hypothalamic-pituitary adrenal axis and results in pre-term delivery. Low pre-pregnancy weight, followed by undernutrition during mid-pregnancy, results in reduced placental growth and lower birth weights at term. Studies that have restricted nutrients during mid-gestation only reveal variable effects on the placental and fetal growth trajectory, however if undernutrition is prolonged during late-pregnancy, fetal growth is compromised, particularly in twin pregnancies. In contrast, overnourishing the adolescent sheep to promote rapid maternal growth, results in the premature delivery of low birth weight lambs. These effects are mediated by impaired placental growth, uteroplacental blood flows and fetal nutrient uptakes. At the other end of the nutritional spectrum, undernourishing the adolescent sheep to gradually deplete nutrient reserves, results in fetal growth restriction which is independent of alterations in placental mass.

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Undernutrition during the first half of gestation increases the predominance of fetal tissue in late-gestation ovine placentomes

Cited by 43 publications

References 18 publications

Effects of twin pregnancy and periconceptional undernutrition on maternal metabolism, fetal growth and glucose–insulin axis function in ovine pregnancy

Effects of twin pregnancy and periconceptional undernutrition on maternal metabolism, fetal growth and glucose–insulin axis function in ovine pregnancy

Effect of Morphology on Placentome Size, Vascularity, and Vasoreactivity in Late Pregnant Sheep1

Nutritional paradigms of ovine fetal growth restriction: Implications for human pregnancy

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