Feasibility of multimodal magnetic resonance imaging to assess maternal hyperoxygenation in sheep pregnancy

An adequate supply of oxygen is crucial for optimal fetal growth and development. Estimation of quantitative indices that reflect tissue diffusivity and oxygenation have been enabled by advances in magnetic resonance imaging (MRI) technology. However, the current diagnostic tools in clinical obstetrics, such as Doppler ultrasound measurements of umbilical blood flow and cardiotocography, do not offer direct information about the oxygen supply to the fetus, nor placental function in vivo. Although MRI provides an opportunity to identify critical changes in fetal oxygenation, exact tissue oxygen content cannot be established in humans. Preclinical models such as pregnant sheep allow the use of invasive methods to validate MRI measurements. The present study investigates the relationship between changes in MRI signal and conventional blood gas analyser measurements during normoxic and hyperoxic conditions in pregnant sheep. Several studies have reported an increase in human fetal oxygenation during 100% maternal oxygen inhalation. We investigated the physiological impact of maternal hyperoxygenation on the placenta in normal pregnant sheep using multimodal functional MRI. Using a multicompartment MRI signal model, we observed the expected increase in feto-placental oxygen saturation with maternal hyperoxygenation. In addition, maternal hyperoxygenation resulted in a significant increase in blood-oxygenation-level-dependent (BOLD) signal intensities, suggesting that BOLD MRI allows non-invasive assessment of the feto-placental response to maternal hyperoxygenation in sheep. Our data suggest that diffusion and relaxation-based MRI is sensitive to acute changes in maternal and feto-placental oxygenation and demonstrate a link between MRI-parameter estimated and reference oxygen saturation. KEY POINTS: Quantification of feto-placental oxygenation and function are important for correct differential diagnosis of placental insufficiency. The only current method for obtaining information about fetal oxygen delivery is cordocentesis. However, there is a risk of inducing preterm birth and/or fetal loss associated with the procedure. Magnetic resonance imaging (MRI) can estimate changes in oxygenation in specific areas of placental and fetal tissue. Using the DECIDE (i.e. diffusion-relaxation combined imaging for detailed placental evaluation) multicompartment model that is sensitive to changes in maternal and feto-placental oxygenation and the blood-oxygenation-level-dependent (BOLD) MRI technique in the sheep fetus, we have demonstrated that maternal hyperoxygenation increases oxygenation of fetal tissue in the placenta. There was a differential effect according to placentome morphological type. This study shows a link between MRI estimated parameters and reference maternal and fetal <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics><mml:msub><mml:mi>S</mml:mi> <mml:msub><mml:mi>O</mml:mi> <mml:mn>2</mml:mn></mml:msub> </mml:msub> <mml:annotation>${{S}_{{{{\mathrm{O}}}_2}}}$</mml:annotation></mml:semantics> </mml:math> and <mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:semantics><mml:msub><mml:mi>P</mml:mi> <mml:msub><mml:mi>O</mml:mi> <mml:mn>2</mml:mn></mml:msub> </mml:msub> <mml:annotation>${{P}_{{{{\mathrm{O}}}_2}}}$</mml:annotation></mml:semantics> </mml:math> by blood gas analyser, supporting the possibility of using multimodal MRI for measuring regional changes in tissue oxygenation in vivo.