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J Physiol Volume 565, Number 1, 111-124, May 15, 2005 DOI: 10.1113/jphysiol.2005.084996
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Periconceptional nutrition and the relationship between maternal body weight changes in the periconceptional period and feto-placental growth in the sheep

S. M. MacLaughlin1, S. K. Walker2, C. T. Roberts3, D. O. Kleemann2 and I. C. McMillen1

1 Discipline of Physiology, School of Molecular and Biomedical Science, University of Adelaide, Adelaide 5005, South Australia
2 South Australian Research and Development Institute, Turretfield Research Centre, Rosedale 5350, South Australia
3 Research Centre for Reproductive Health, Department of Obstetrics and Gynaecology, University of Adelaide, Adelaide 5005, South Australia

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.

(Received 10 February 2005; accepted after revision 14 March 2005; first published online 17 March 2005)
Corresponding author I. C. McMillen: Physiology, School of Molecular and Biomedical Science, University of Adelaide, Adelaide, SA 5005, Australia. Email: caroline.mcmillen{at}adelaide.edu.au




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