Placental Compartmentalization of Lipid Metabolism: Implications for Singleton and Twin Pregnancies

The study of placental lipid metabolism in uncomplicated pregnancies has not been developed in the literature to date. Its importance lies in expanding the knowledge of placental function to enable comparison with pathological pregnancies in future research. The aim of the present study was to compare the lipid metabolic activity and storage of the maternal and fetal sides of the placenta in healthy pregnancies. Moreover, we compare singleton vs. twin pregnancies to determine if placental metabolic needs differ. We analyzed placental explants from uncomplicated pregnancies, 20 from singleton and 8 from bichorial-biamniotic twin pregnancies (n = 28). Six cotyledon fragments were collected from each placenta at different distances from the umbilical cord, three close to the chorionic plate (hereinafter, we will refer to them as "fetal side") and another three close to the anchoring villi into the decidua basalis (referred to as "maternal side"). The samples were analyzed for quantitative assay placental fatty acid oxidation (FAO) and esterification (FAE) activities and triglyceride levels. The location of lipid storage in the chorionic villi was assessed by Oil red-O staining. Placental fatty acid oxidation did not show differences when comparing the maternal and fetal sides of the placenta or between single and twin pregnancies. When comparing placental sides, FAE was increased twofold in the maternal side compared to the fetal side of the placenta (P = 0.013). The tendency for lipogenesis in the placenta was exemplified by the FAE/FAO ratio, which was a 37.1% higher on the maternal side (P = 0.019). Despite this, triglyceride levels were five times higher in the fetal side than in the maternal one (P = 0.024). When analyzing singleton vs. twins, FAE was superior in the fetal side in multiple pregnancies (× 2.6, P = 0.007) and the FAE/FAO ratio was significantly higher in twins than in singleton pregnancies, on both sides of the placenta. Despite this finding, triglyceride levels were similar in twin and singleton pregnancies. Comparing the placentas of twins in the same pregnancy, there were no differences in lipid metabolism (FAO or FAE) or placental triglyceride levels between the two co-twins. Using Oil red-O staining, lipid storage in chorionic villi was found to be located on the syncytiotrophoblast cells and not in the connecting axis. The maternal side of the placenta is more active in the esterification of fatty acids, while the storage of neutral lipids concentrates on the fetal side. Moreover, multiple gestations have increased esterification without changes in the concentration of placental triglycerides, probably due to a higher transfer to the fetal circulation in response to the greater energy demand from twin fetuses.