Reduced combined ventricular output and increased oxygen extraction fraction in a fetus with complete heart block demonstrated by MRI

IntroductionTabled 1KEY TEACHING POINTS•Bradycardia in a complete heart block fetus is associated with a significant reduction in fetal combined ventricular output, resulting in restricted fetal growth and elevated oxygen extraction.•Magnetic resonance imaging (MRI) confirmed the “brain-sparing physiology” that was indicated by the Doppler assessment.•MRI hemodynamic assessment could provide a useful adjunct to conventional ultrasound parameters in the monitoring of fetal well-being in complete heart block. Open table in a new tab Congenital complete heart block (CHB) occurs in approximately 1 in 15,000 live births.1Michaelsson M. Engle M. Congenital complete heart block: an international study of the natural history story.Clin Cardiol. 1972; 4: 101Google Scholar It may result from an immune- or non-immune-mediated process, with immune-mediated cases usually associated with high-titer maternal anti-Ro antibodies, which cross the placenta and may result in injury to the fetal cardiac conduction tissues.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar Autoimmune-mediated congenital CHB is associated with significant morbidity and mortality in the perinatal period.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar One study reported a total mortality rate of CHB to be 19%, of which 27% died in utero and 45% died within the first 3 months of life.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar Risk factors for poor fetal outcome include premature delivery, fetal hydrops, low heart rate, and ventricular endocardial fibroelastosis.3Jaeggi E.T. Hamilton R.M. Silverman E.D. Zamora S.A. Hornberger L.K. Outcome of children with fetal, neonatal or childhood diagnosis of isolated congenital atrioventricular block.J Am Coll Cardiol. 2002; 39: 130-137Abstract Full Text Full Text PDF PubMed Scopus (310) Google Scholar CHB is known to decrease cardiac output in postnatal patients.4Yagel S. Silverman N. Fetal Cardiology: Embryology, Genetics, Physiology, Echocardiographic Evaluation, Diagnosis and Perinatal Management of Cardiac Diseases (Series in Maternal-Fetal Medicine). New York, NY: Informa;. 2008; Crossref Google Scholar However, the hemodynamics of the fetal circulation in the setting of CHB have not been well characterized. Fetal echocardiography can be used to detect and analyze fetal arrhythmias. Mechanical assessment by M mode can be used to characterize fetal bradycardia including CHB, and pulsed Doppler is also widely employed to visualize the temporal relationships of the blood flows in the heart and great vessels that delineate the timing of cardiac electrical events.4Yagel S. Silverman N. Fetal Cardiology: Embryology, Genetics, Physiology, Echocardiographic Evaluation, Diagnosis and Perinatal Management of Cardiac Diseases (Series in Maternal-Fetal Medicine). New York, NY: Informa;. 2008; Crossref Google Scholar New magnetic resonance imaging (MRI) technology now provides an additional noninvasive method for measuring the oxygen saturation (SaO2) and flow in fetal blood vessels. The feasibility of this MRI technique, which incorporates a combination of cine phase-contrast MRI and T2 mapping, has been shown in normal fetal circulation, and in fetuses with congenital heart disease and growth and to an in the setting of M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google N. S. et hemodynamics of growth by Google bradycardia was first in a with lupus a The been for an elevated anti-Ro the first the fetus was to be in heart with an rate of and ventricular rate of of cardiac endocardial or The fetal was the The was a of and the atrioventricular conduction to CHB and the fetal heart rate to The was to fetal heart rates and the fetus was by for and was in The and fetal growth ultrasound in with growth The heart rate was and a was with ventricular The was from the of with ventricular a blood of and of fetal a The fetal from to M new and for for PubMed Scopus Google MRI hemodynamic of a a fetal MRI was a MRI to M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google Scholar an of fetal of which was the for The fetal heart rate was the of the MRI was used for cardiac phase-contrast MRI of fetal blood of flow in the fetal is shown in 1 The phase-contrast with M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google Scholar The low normal flow in the and and flows in and The combined ventricular output of and was an MRI to blood was normal in the low in vessels to in normal fetuses fetal to and the of the T2 of blood with fetal to be the for the and oxygen of blood in fetal vessels was to M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google Scholar The the fetal circulation in this with shown in oxygen in the and with fetal oxygen and oxygen can be M. J. R. M. hemodynamic for the normal fetus by MRI and T2 Congenital of the Scopus Google Scholar The fetus normal and which was associated with a oxygen et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google resonance imaging flow in fetal vessels. saturation T2 in fetal vessels. oxygen oxygen and oxygen for for normal fetuses also M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google Scholar combined ventricular blood the MRI this study provides new the hemodynamic of a heart rate and atrioventricular that the bradycardia was associated with an in oxygen to fetal within the normal the reduction in fetal that is by with the CHB and low reported by et fetal with which may have been to a combination of fetal and M. and outcome of children with congenital complete heart block in utero or a PubMed Scopus Google and PubMed Scopus Google in the setting of in and of the circulation in to the of fetal is in the setting of CHB, the in M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google of fetal heart rate Google R. M. in and fetal Doppler in PubMed Scopus Google Scholar However, the which this is a of and has been shown to have in the setting of The Doppler postnatal outcome in fetuses with congenital heart block.J 2008; PubMed Scopus Google Scholar The Doppler a that the fetal growth a in this in which the was and was in the normal resulting in a the the is by the MRI flow which that the of the in the was in normal fetuses M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google is by blood flow and the oxygen of Congenital of the Scopus Google Scholar can is from the maternal circulation to the in of oxygen the or blood Congenital of the Scopus Google Scholar the low normal was by with normal T2 in with normal and oxygen fetal was to an in the in the and was also in fetal of oxygen from to that can be by with in J. The of blood flow fetal Scopus Google of T2 to is from blood and not for the T2 of fetal could also the T2 and fetal be R. S. Fetal in the assessment of Scopus Google Scholar which could However, this is in this the neonatal was to the normal T2 has not been for in blood in fetal has been shown T2 and conventional blood in the vessels of children with congenital heart disease and in fetal Hornberger L.K. MRI of blood oxygen saturation in children with congenital heart PubMed Scopus Google J. M. R. MRI of fetal blood oxygen saturation in cardiac of fetal a feasibility PubMed Scopus Google Scholar the of technique, in the that is noninvasive for The of ultrasound of the of fetal have been to flow Doppler and to in of with an of and for the blood flow the of the of blood flow by and of Full Text PDF Scopus Google Scholar phase-contrast MRI is the noninvasive for the of flow in fetal and is used in postnatal for measuring cardiac output, J. M. flow with phase-contrast and 2002; PubMed Scopus Google Scholar However, the of fetal MRI this to and the hemodynamic obtained in a may not be of or in fetal this is the first of fetal hemodynamic by MRI in the setting of congenital MRI confirmed the “brain-sparing physiology” that was indicated by the Doppler provide the of a cardiac hemodynamic for growth which may be by the of in this CHB also provides to that an of approximately in the bradycardia is associated with a significant reduction in fetal resulting in restricted fetal growth and elevated oxygen the in oxygen is to in fetuses with and with of congenital heart disease associated with the of or of congenital heart disease associated with normal oxygen et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google Scholar this the heart rate was and is that fetuses in CHB with ventricular rates to normal that in this of hemodynamic assessment could provide a useful adjunct to conventional ultrasound parameters in the monitoring of fetal well-being in the setting of study with a of CHB be to the and in CHB fetuses and also the of MRI in monitoring CHB IntroductionTabled 1KEY TEACHING POINTS•Bradycardia in a complete heart block fetus is associated with a significant reduction in fetal combined ventricular output, resulting in restricted fetal growth and elevated oxygen extraction.•Magnetic resonance imaging (MRI) confirmed the “brain-sparing physiology” that was indicated by the Doppler assessment.•MRI hemodynamic assessment could provide a useful adjunct to conventional ultrasound parameters in the monitoring of fetal well-being in complete heart block. Open table in a new tab Congenital complete heart block (CHB) occurs in approximately 1 in 15,000 live births.1Michaelsson M. Engle M. Congenital complete heart block: an international study of the natural history story.Clin Cardiol. 1972; 4: 101Google Scholar It may result from an immune- or non-immune-mediated process, with immune-mediated cases usually associated with high-titer maternal anti-Ro antibodies, which cross the placenta and may result in injury to the fetal cardiac conduction tissues.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar Autoimmune-mediated congenital CHB is associated with significant morbidity and mortality in the perinatal period.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar One study reported a total mortality rate of CHB to be 19%, of which 27% died in utero and 45% died within the first 3 months of life.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar Risk factors for poor fetal outcome include premature delivery, fetal hydrops, low heart rate, and ventricular endocardial fibroelastosis.3Jaeggi E.T. Hamilton R.M. Silverman E.D. Zamora S.A. Hornberger L.K. Outcome of children with fetal, neonatal or childhood diagnosis of isolated congenital atrioventricular block.J Am Coll Cardiol. 2002; 39: 130-137Abstract Full Text Full Text PDF PubMed Scopus (310) Google Scholar CHB is known to decrease cardiac output in postnatal patients.4Yagel S. Silverman N. Fetal Cardiology: Embryology, Genetics, Physiology, Echocardiographic Evaluation, Diagnosis and Perinatal Management of Cardiac Diseases (Series in Maternal-Fetal Medicine). New York, NY: Informa;. 2008; Crossref Google Scholar However, the hemodynamics of the fetal circulation in the setting of CHB have not been well characterized. Fetal echocardiography can be used to detect and analyze fetal arrhythmias. Mechanical assessment by M mode can be used to characterize fetal bradycardia including CHB, and pulsed Doppler is also widely employed to visualize the temporal relationships of the blood flows in the heart and great vessels that delineate the timing of cardiac electrical events.4Yagel S. Silverman N. Fetal Cardiology: Embryology, Genetics, Physiology, Echocardiographic Evaluation, Diagnosis and Perinatal Management of Cardiac Diseases (Series in Maternal-Fetal Medicine). New York, NY: Informa;. 2008; Crossref Google Scholar New magnetic resonance imaging (MRI) technology now provides an additional noninvasive method for measuring the oxygen saturation (SaO2) and flow in fetal blood vessels. The feasibility of this MRI technique, which incorporates a combination of cine phase-contrast MRI and T2 mapping, has been shown in normal fetal circulation, and in fetuses with congenital heart disease and growth and to an in the setting of M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google N. S. et hemodynamics of growth by Google Scholar Congenital complete heart block (CHB) occurs in approximately 1 in 15,000 live births.1Michaelsson M. Engle M. Congenital complete heart block: an international study of the natural history story.Clin Cardiol. 1972; 4: 101Google Scholar It may result from an immune- or non-immune-mediated process, with immune-mediated cases usually associated with high-titer maternal anti-Ro antibodies, which cross the placenta and may result in injury to the fetal cardiac conduction tissues.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar Autoimmune-mediated congenital CHB is associated with significant morbidity and mortality in the perinatal period.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar One study reported a total mortality rate of CHB to be 19%, of which 27% died in utero and 45% died within the first 3 months of life.2Buyon J.P. Hiebert R. Copel J. et al.Autoimmune-associated congenital heart block: demographics, mortality, morbidity and recurrence rates obtained from a national neonatal lupus registry.J Am Coll Cardiol. 1998; 31: 1658-1666Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar Risk factors for poor fetal outcome include premature delivery, fetal hydrops, low heart rate, and ventricular endocardial fibroelastosis.3Jaeggi E.T. Hamilton R.M. Silverman E.D. Zamora S.A. Hornberger L.K. Outcome of children with fetal, neonatal or childhood diagnosis of isolated congenital atrioventricular block.J Am Coll Cardiol. 2002; 39: 130-137Abstract Full Text Full Text PDF PubMed Scopus (310) Google Scholar CHB is known to decrease cardiac output in postnatal patients.4Yagel S. Silverman N. Fetal Cardiology: Embryology, Genetics, Physiology, Echocardiographic Evaluation, Diagnosis and Perinatal Management of Cardiac Diseases (Series in Maternal-Fetal Medicine). New York, NY: Informa;. 2008; Crossref Google Scholar However, the hemodynamics of the fetal circulation in the setting of CHB have not been well characterized. Fetal echocardiography can be used to detect and analyze fetal arrhythmias. Mechanical assessment by M mode can be used to characterize fetal bradycardia including CHB, and pulsed Doppler is also widely employed to visualize the temporal relationships of the blood flows in the heart and great vessels that delineate the timing of cardiac electrical events.4Yagel S. Silverman N. Fetal Cardiology: Embryology, Genetics, Physiology, Echocardiographic Evaluation, Diagnosis and Perinatal Management of Cardiac Diseases (Series in Maternal-Fetal Medicine). New York, NY: Informa;. 2008; Crossref Google Scholar New magnetic resonance imaging (MRI) technology now provides an additional noninvasive method for measuring the oxygen saturation (SaO2) and flow in fetal blood vessels. The feasibility of this MRI technique, which incorporates a combination of cine phase-contrast MRI and T2 mapping, has been shown in normal fetal circulation, and in fetuses with congenital heart disease and growth and to an in the setting of M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google N. S. et hemodynamics of growth by Google Scholar bradycardia was first in a with lupus a The been for an elevated anti-Ro the first the fetus was to be in heart with an rate of and ventricular rate of of cardiac endocardial or The fetal was the The was a of and the atrioventricular conduction to CHB and the fetal heart rate to The was to fetal heart rates and the fetus was by for and was in The and fetal growth ultrasound in with growth The heart rate was and a was with ventricular The was from the of with ventricular a blood of and of MRI hemodynamic of a a fetal MRI was a MRI to M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google Scholar an of fetal of which was the for The fetal heart rate was the of the MRI was used for cardiac phase-contrast MRI of fetal blood of flow in the fetal is shown in 1 The phase-contrast with M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google Scholar The low normal flow in the and and flows in and The combined ventricular output of and was an MRI to blood was normal in the low in vessels to in normal fetuses fetal to and the of the T2 of blood with fetal to be the for the and oxygen of blood in fetal vessels was to M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google Scholar The the fetal circulation in this with shown in oxygen in the and with fetal oxygen and oxygen can be M. J. R. M. hemodynamic for the normal fetus by MRI and T2 Congenital of the Scopus Google Scholar The fetus normal and which was associated with a oxygen et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google resonance imaging flow in fetal vessels. saturation T2 in fetal vessels. oxygen oxygen and oxygen for for normal fetuses also M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google Scholar combined ventricular blood Fetal bradycardia was first in a with lupus a The been for an elevated anti-Ro the first the fetus was to be in heart with an rate of and ventricular rate of of cardiac endocardial or The fetal was the The was a of and the atrioventricular conduction to CHB and the fetal heart rate to The was to fetal heart rates and the fetus was by for and was in The and fetal growth ultrasound in with growth The heart rate was and a was with ventricular The was from the of with ventricular a blood of and of Fetal MRI hemodynamic of a a fetal MRI was a MRI to M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google Scholar an of fetal of which was the for The fetal heart rate was the of the MRI was used for cardiac phase-contrast MRI of fetal blood of flow in the fetal is shown in 1 The phase-contrast with M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google Scholar The low normal flow in the and and flows in and The combined ventricular output of and was an MRI to blood was normal in the low in vessels to in normal fetuses fetal to and the of the T2 of blood with fetal to be the for the and oxygen of blood in fetal vessels was to M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google Scholar The the fetal circulation in this with shown in oxygen in the and with fetal oxygen and oxygen can be M. J. R. M. hemodynamic for the normal fetus by MRI and T2 Congenital of the Scopus Google Scholar The fetus normal and which was associated with a oxygen et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google Scholar of a a fetal MRI was a MRI to M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google Scholar an of fetal of which was the for The fetal heart rate was the of the MRI was used for cardiac phase-contrast MRI of fetal blood of flow in the fetal is shown in 1 The phase-contrast with M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google Scholar The low normal flow in the and and flows in and The combined ventricular output of and was an MRI to blood was normal in the low in vessels to in normal fetuses fetal to and the of the T2 of blood with fetal to be the for the and oxygen of blood in fetal vessels was to M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google M. of of the of blood flow in the normal fetal circulation a PubMed Scopus Google Scholar The the fetal circulation in this with shown in oxygen in the and with fetal oxygen and oxygen can be M. J. R. M. hemodynamic for the normal fetus by MRI and T2 Congenital of the Scopus Google Scholar The fetus normal and which was associated with a oxygen et fetal oxygen is associated with in fetuses with congenital heart PubMed Scopus Google Scholar the MRI this study provides new the hemodynamic of a heart rate and atrioventricular that the bradycardia was associated with an in oxygen to fetal within the normal the reduction in fetal that is by with the CHB and low reported by et fetal with which may have been to a combination of fetal and M. and outcome of children with congenital complete heart block in utero or a PubMed Scopus Google and PubMed Scopus Google in the setting of in and of the circulation in to the of fetal is in the setting of CHB, the in M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google of fetal heart rate Google R. M. in and fetal Doppler in PubMed Scopus Google Scholar However, the which this is a of and has been shown to have in the setting of The Doppler postnatal outcome in fetuses with congenital heart block.J 2008; PubMed Scopus Google Scholar The Doppler a that the fetal growth a in this in which the was and was in the normal resulting in a the the is by the MRI flow which that the of the in the was in normal fetuses M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google is by blood flow and the oxygen of Congenital of the Scopus Google Scholar can is from the maternal circulation to the in of oxygen the or blood Congenital of the Scopus Google Scholar the low normal was by with normal T2 in with normal and oxygen fetal was to an in the in the and was also in fetal of oxygen from to that can be by with in J. The of blood flow fetal Scopus Google of T2 to is from blood and not for the T2 of fetal could also the T2 and fetal be R. S. Fetal in the assessment of Scopus Google Scholar which could However, this is in this the neonatal was to the normal T2 has not been for in blood in fetal has been shown T2 and conventional blood in the vessels of children with congenital heart disease and in fetal Hornberger L.K. MRI of blood oxygen saturation in children with congenital heart PubMed Scopus Google J. M. R. MRI of fetal blood oxygen saturation in cardiac of fetal a feasibility PubMed Scopus Google Scholar the of technique, in the that is noninvasive for The of ultrasound of the of fetal have been to flow Doppler and to in of with an of and for the blood flow the of the of blood flow by and of Full Text PDF Scopus Google Scholar phase-contrast MRI is the noninvasive for the of flow in fetal and is used in postnatal for measuring cardiac output, J. M. flow with phase-contrast and 2002; PubMed Scopus Google Scholar However, the of fetal MRI this to and the hemodynamic obtained in a may not be of or in fetal the MRI this study provides new the hemodynamic of a heart rate and atrioventricular that the bradycardia was associated with an in oxygen to fetal within the normal the reduction in fetal that is by with the CHB and low reported by et fetal with which may have been to a combination of fetal and M. and outcome of children with congenital complete heart block in utero or a PubMed Scopus Google and PubMed Scopus Google Scholar Doppler in the setting of in and of the circulation in to the of fetal is in the setting of CHB, the in M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google of fetal heart rate Google R. M. in and fetal Doppler in PubMed Scopus Google Scholar However, the which this is a of and has been shown to have in the setting of The Doppler postnatal outcome in fetuses with congenital heart block.J 2008; PubMed Scopus Google Scholar The Doppler a that the fetal growth a in this in which the was and was in the normal resulting in a the the is by the MRI flow which that the of the in the was in normal fetuses M. J. M. of blood flow in the vessels of the normal fetal circulation by magnetic resonance Google Scholar Fetal is by blood flow and the oxygen of Congenital of the Scopus Google Scholar can is from the maternal circulation to the in of oxygen the or blood Congenital of the Scopus Google Scholar the low normal was by with normal T2 in with normal and oxygen fetal was to an in the in the and was also in fetal of oxygen from to that can be by with in J. 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