Periconceptional nutrition and the relationship between maternal body weight changes in the periconceptional period and feto‐placental growth in the sheep

Abstract

Recent studies in the sheep have shown that maternal undernutrition during the periconceptional period, when the nutrient demands of the embryo are minimal, can alter the subsequent development of the metabolic, endocrine and cardiovascular systems and that these effects may, in part, depend on embryo number. We have tested the hypotheses that there are relationships between maternal weight or body condition at the time of conception and feto-placental growth during the first 55 days of pregnancy, and that periconceptional undernutrition has a differential effect on these relationships in singleton and twin pregnancies. We have investigated the effect of periconceptional undernutrition in the ewe (control n = 24, restricted at 70% of control feed allowance, PCUN n = 21) from 45 days prior to mating until 7 days after mating on placental and fetal weight and on placental histology in singleton and twin pregnancies at 53-56 days' gestation, i.e. during the period of maximal placental growth. In control, but not PCUN ewes carrying singleton pregnancies, there were direct relationships between maternal weight gain during the periconceptional period and uteroplacental weights at 53-56 days' gestation. There were direct relationships, however, between placental and fetal weights in both control and PCUN singleton pregnancies. In contrast to the singletons, in control twin pregnancies, there was no effect of maternal weight gain in the periconceptional period on any measure of uteroplacental growth, and there was also no relationship between placental and fetal weight. This lack of a relationship may be related to the increased uteroplacental weight and mean placentome weight in the twin pregnancies (control singletons: 2.45 ± 0.18 g; control twins: 4.10 ± 0.62 g). In the PCUN group, however, a greater weight loss between the start of the feeding regime and post mortem at ∼ day 55, was associated with a larger placenta and fetus, and the direct relationship between placental and fetal mass was restored. In summary, the present study has demonstrated that there are important relationships between maternal weight gain during the periconceptional period and feto-placental growth during the first 56 days of pregnancy, and that periconceptional undernutrition has a differential effect on these relationships in singleton and twin pregnancies. In singleton pregnancies, periconceptional undernutrition disrupts the relationship between maternal weight gain during the periconceptional period and uteroplacental growth, and in twin pregnancies periconceptional undernutrition results in the emergence of an inverse relationship between maternal weight gain during early pregnancy and uteroplacental growth and a dependence of fetal growth on placental growth. These changes highlight the importance of the periconceptional environment in setting the placental and fetal growth trajectories, and have implications for the programmed development of the metabolic, cardiovascular and endocrine systems of the fetus and adult.

Litter-size-dependent intrauterine growth restriction in sheep

“…Therefore, litter-size-dependent IUGR may result from failure of the uteroplacental complex fully to support growth of the multiple foetuses within the same uterus. Indeed, available evidence from studies of both sheep (Edwards and McMillen, 2002;Gardner et al, 2004;MacLaughlin et al, 2005) and humans (De Boo and Harding, 2006) suggests that reduced BWTs of individual lambs born in litters with more than one lamb have features in common with IUGR in lambs resulting from undernutrition, such as reduction in uterine blood flow per foetus and lower metabolite concentration in the maternal and foetal circulations. However, as ewes can clearly maintain a litter to term for which total weight approaches three times that of a normal single lamb (Dickinson et al, 1962), it is unclear why the individual BWTs of lambs born as twins or triplets are lower than those of lambs born as singletons.…”

Programming the brain: Common outcomes and gaps in knowledge from animal studies of IUGR

“…Fetal and neonatal body and brain weights are reduced in the 135 majority of these preclinical models, as is seen in human IUGR (Table 1, 2), although each model 136 affects neurodevelopment, and in turn cognitive outcomes to varying degrees. While there are 137 additional animal models of perturbed prenatal development in which neurodevelopment and/or 138 cognitive outcomes have been investigated, for example those investigating effects of 139 periconceptional and early gestational undernutrition in the sheep [76][77][78], these models do not 140 restrict fetal growth in late gestation or reduce size at birth as occur in human IUGR and are 141 therefore not discussed further in this review. Similarly, this review is limited to those models of 142 IUGR in which neurodevelopmental and/or cognitive outcomes have been reported.…”

The effect of maternal nutrition level during the periconception period on fetal muscle development and plasma hormone concentrations in sheep

“…Similarly, MacLaughlin et al (2005) reported that short-term undernutrition from 45 days before mating until 7 days after mating in singleton gestations did not affect uterine, fetal weights, weight of fetal membranes, placentome number, mean placentome weight and total placental weight at 53 to 56 days of pregnancy in the sheep. Quigley et al (2005) reported that maternal nutrition level in ewes during periconception period from 18 days before until 6 days after ovulation did not affect the primary fiber numbers of singleton fetus, but maternal over nutrition increased total muscle fiber numbers, secondary fiber numbers and secondary to primary fiber ratio in the ST muscles of singleton fetuses on day 75 of gestation compared with fetuses from undernutrition ewes.…”