European Radiology

, Volume 28, Issue 5, pp 1884–1890 | Cite as

Imaging putative foetal cerebral blood oxygenation using susceptibility weighted imaging (SWI)

  • Brijesh Kumar Yadav
  • Uday Krishnamurthy
  • Sagar Buch
  • Pavan Jella
  • Edgar Hernandez-Andrade
  • Lami Yeo
  • Steven J. Korzeniewski
  • Anabela Trifan
  • Sonia S. Hassan
  • E. Mark Haacke
  • Roberto Romero
  • Jaladhar Neelavalli
Magnetic Resonance



To evaluate the magnetic susceptibility, ∆χ v , as a surrogate marker of venous blood oxygen saturation, S v O 2, in second- and third-trimester normal human foetuses.


Thirty-six pregnant women, having a mean gestational age (GA) of 31 2/7 weeks, underwent magnetic resonance imaging (MRI). Susceptibility-weighted imaging (SWI) data from the foetal brain were acquired. ∆χ v of the superior sagittal sinus (SSS) was quantified using MR susceptometry from the intra-vascular phase measurements. Assuming the magnetic property of foetal blood, ∆χ do , is the same as that of adult blood, S v O 2 was derived from the measured Δχ v . The variation of ∆χ v and S v O 2, as a function of GA, was statistically evaluated.


The mean ∆χ v in the SSS in the second-trimester (n = 8) and third-trimester foetuses (n = 28) was found to be 0.34± 0.06 ppm and 0.49 ±0.05 ppm, respectively. Correspondingly, the derived S v O 2 values were 69.4% ±3.27% and 62.6% ±3.25%. Although not statistically significant, an increasing trend (p = 0.08) in Δχ v and a decreasing trend (p = 0.22) in S v O 2 with respect to advancing gestation was observed.


We report cerebral venous blood magnetic susceptibility and putative oxygen saturation in healthy human foetuses. Cerebral oxygen saturation in healthy human foetuses, despite a slight decreasing trend, does not change significantly with advancing gestation.

Key points

• Cerebral venous magnetic susceptibility and oxygenation in human foetuses can be quantified.

• Cerebral venous oxygenation was not different between second- and third-trimester foetuses.

• Foetal cerebral venous oxygenation does not change significantly with advancing gestation.


Susceptibility-weighted imaging (SWI) Foetal Brain Oxygen saturation Susceptometry 



Susceptibility-weighted imaging


Magnetic resonance imaging


Superior sagittal sinus


Venous oxygen saturation


Magnetic susceptibility


Magnetic susceptibility difference between fully oxygenated and deoxygenated foetal blood




Foetal haemoglobin


Adult haemoglobin


Foetal heart rate


Gestational age



The authors would like to thank Maria Cabrera and the research staff at the PRB for their help in volunteer recruitment.


This research was supported, in part, by the Perinatology Research Branch (PRB), Program for Perinatal Research and Obstetrics, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, US Department of Health and Human Services (NICHD/NIH/DHHS); in part, with Federal funds from NICHD/NIH/DHHS under contract no. HHSN275201300006C; and an STTR grant from the NHLBI no. 1R42HL112580- 01A1.

Compliance with ethical standards


The scientific guarantor of this publication is Dr. Jaladhar Neelavalli, PhD.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors has significant statistical expertise.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.


• prospective

• experimental

• performed at one institution


  1. 1.
    Schneider H (2011) Oxygenation of the placental–fetal unit in humans. Respir Physiol Neurobiol 178:51–58CrossRefPubMedGoogle Scholar
  2. 2.
    Baschat AA (2004) Pathophysiology of fetal growth restriction: implications for diagnosis and surveillance. Obstet Gynecol Surv 59:617–627CrossRefPubMedGoogle Scholar
  3. 3.
    Baschat DAA (2004) Fetal responses to placental insufficiency: an update. BJOG Int J Obstet Gynaecol 111:1031–1041CrossRefGoogle Scholar
  4. 4.
    Valcamonico A et al (1994) Absent end-diastolic velocity in umbilical artery: risk of neonatal morbidity and brain damage. Am J Obstet Gynecol 170:796–801CrossRefPubMedGoogle Scholar
  5. 5.
    Gramellini D et al (1992) Cerebral-umbilical Doppler ratio as a predictor of adverse perinatal outcome. Obstet Gynecol 79:416–420CrossRefPubMedGoogle Scholar
  6. 6.
    Hecher K et al (1992) Potential for diagnosing imminent risk to appropriate-and small-for-gestational-age fetuses by Doppler sonographic examination of umbilical and cerebral arterial blood flow. Ultrasound Obstet Gynecol 2:266–271CrossRefPubMedGoogle Scholar
  7. 7.
    Al-Ghazali W et al (1989) Evidence of redistribution of cardiac output in asymmetrical growth retardation. BJOG Int J Obstet Gynaecol 96:697–704CrossRefGoogle Scholar
  8. 8.
    Ferrazzi E et al (2002) Temporal sequence of abnormal Doppler changes in the peripheral and central circulatory systems of the severely growth-restricted fetus. Ultrasound Obstet Gynecol 19:140–146CrossRefPubMedGoogle Scholar
  9. 9.
    Dubiel M, Gunnarsson G, Gudmundsson S (2002) Blood redistribution in the fetal brain during chronic hypoxia. Ultrasound Obstet Gynecol 20:117–121CrossRefPubMedGoogle Scholar
  10. 10.
    Wladimiroff J, Tonge H, Stewart P (1986) Doppler ultrasound assessment of cerebral blood flow in the human fetus. BJOG Int J Obstet Gynaecol 93:471–475CrossRefGoogle Scholar
  11. 11.
    Rosen K, Kjellmer I (1975) Changes in the fetal heart rate and ECG during hypoxia. Acta Physiol 93:59–66CrossRefGoogle Scholar
  12. 12.
    Parer J et al (1980) Increased fetal heart rate variability with acute hypoxia in chronically instrumented sheep. Eur J Obstet Gynecol Reprod Biol 10:393–399CrossRefPubMedGoogle Scholar
  13. 13.
    Smith J et al (1988) Antenatal fetal heart rate variation in relation to the respiratory and metabolic status of the compromised human fetus. BJOG Int J Obstet Gynaecol 95:980–989CrossRefGoogle Scholar
  14. 14.
    Gagnon R, Johnston L, Murotsuki J (1996) Fetal placental embolization in the late-gestation ovine fetus: alterations in umbilical blood flow and fetal heart rate patterns. Am J Obstet Gynecol 175:63–72CrossRefPubMedGoogle Scholar
  15. 15.
    Ribbert LS et al (1991) Relation of fetal blood gases and data from computer-assisted analysis of fetal heart rate patterns in small for gestation fetuses. BJOG Int J Obstet Gynaecol 98:820–823CrossRefGoogle Scholar
  16. 16.
    Chipchase J et al (2002) Cerebral hemoglobin concentration and oxygen saturation measured by intensity modulated optical spectroscopy in the human fetus during labor. J Perinat Med 30:502–509CrossRefPubMedGoogle Scholar
  17. 17.
    Vintzileos AM et al (2005) Transabdominal fetal pulse oximetry with near-infrared spectroscopy. Am J Obstet Gynecol 192:129–133CrossRefPubMedGoogle Scholar
  18. 18.
    Rutherford M et al (2008) MR imaging methods for assessing fetal brain development. Develop Neurobiol 68:700–711CrossRefGoogle Scholar
  19. 19.
    Levine D et al (2003) Fast MR imaging of fetal central nervous system abnormalities 1. Radiology 229:51–61CrossRefPubMedGoogle Scholar
  20. 20.
    Whitby E et al (2004) Comparison of ultrasound and magnetic resonance imaging in 100 singleton pregnancies with suspected brain abnormalities. BJOG Int J Obstet Gynaecol 111:784–792CrossRefGoogle Scholar
  21. 21.
    Wolfberg AJ et al (2007) Identification of fetal cerebral lactate using magnetic resonance spectroscopy. Am J Obstet Gynecol 196:e9–e11CrossRefPubMedGoogle Scholar
  22. 22.
    Cetin I et al (2011) Lactate detection in the brain of growth-restricted fetuses with magnetic resonance spectroscopy. Am J Obstet Gynecol 205:350. e1–350. e7CrossRefGoogle Scholar
  23. 23.
    Zhu MY et al (2016) The hemodynamics of late-onset intrauterine growth restriction by MRI. Am J Obstet Gynecol 214:367. e1–367. e17CrossRefGoogle Scholar
  24. 24.
    Stuber M et al (2002) Preliminary report on in vivo coronary MRA at 3 Tesla in humans. Magn Reson Med 48:425–429CrossRefPubMedGoogle Scholar
  25. 25.
    Frayne R et al (2003) Magnetic resonance imaging at 3.0 Tesla: challenges and advantages in clinical neurological imaging. Investig Radiol 38:385–402Google Scholar
  26. 26.
    Haacke EM et al (1997) In vivo measurement of blood oxygen saturation using magnetic resonance imaging: A direct validation of the blood oxygen level-dependent concept in functional brain imaging. Hum Brain Mapp 5:341–346CrossRefPubMedGoogle Scholar
  27. 27.
    Fernández-Seara MA et al (2006) MR susceptometry for measuring global brain oxygen extraction. Magn Reson Med 55:967–973CrossRefPubMedGoogle Scholar
  28. 28.
    Vegh V et al. (2015) Selective channel combination of MRI signal phase. Magnetic Resonance in MedicineGoogle Scholar
  29. 29.
    Neelavalli J et al (2014) Measuring venous blood oxygenation in fetal brain using susceptibility-weighted imaging. J Magn Reson Imaging 39:998–1006CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Cheema R et al (2004) Fetal cerebral venous Doppler velocimetry in normal and high-risk pregnancy. Ultrasound Obstet Gynecol 24:147–153CrossRefPubMedGoogle Scholar
  31. 31.
    Hadlock FP et al (1985) Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study. Am J Obstet Gynecol 151:333–337CrossRefPubMedGoogle Scholar
  32. 32.
    Wang Y et al (2000) Artery and vein separation using susceptibility-dependent phase in contrast-enhanced MRA. J Magn Reson Imaging 12:661–670CrossRefPubMedGoogle Scholar
  33. 33.
    Boulot P et al (1993) Hematologic values of fetal blood obtained by means of cordocentesis. Fetal Diagn Ther 8:309–316CrossRefPubMedGoogle Scholar
  34. 34.
    Jain V, Langham MC, Wehrli FW (2010) MRI estimation of global brain oxygen consumption rate. J Cereb Blood Flow Metab 30:1598–1607CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Spees WM et al (2001) Water proton MR properties of human blood at 1.5 Tesla: Magnetic susceptibility, T1, T2, T* 2, and non-Lorentzian signal behavior. Magn Reson Med 45:533–542CrossRefPubMedGoogle Scholar
  36. 36.
    Schroter B et al (1997) Normal value curves for intrauterine fetal blood gas and acid-base parameters in the 2nd and 3rd trimester. Gynakol Geburtshilfliche Rundsch 37:130–135 Article in GermanCrossRefPubMedGoogle Scholar
  37. 37.
    Jain V et al (2014) Cerebral oxygen metabolism in neonates with congenital heart disease quantified by MRI and optics. J Cereb Blood Flow Metab 34:380–388CrossRefPubMedGoogle Scholar
  38. 38.
    Burton G, Jaunaiux E (2001) Maternal vascularisation of the human placenta: does the embryo develop in a hypoxic environment? Gynécologie Obstétrique Fertilité 29:503–508CrossRefGoogle Scholar
  39. 39.
    Veille J-C, Hanson R, Tatum K (1993) Longitudinal quantitation of middle cerebral artery blood flow in normal human fetuses. Am J Obstet Gynecol 169:1393–1398CrossRefPubMedGoogle Scholar
  40. 40.
    Nield LE et al (2002) MRI-based blood oxygen saturation measurements in infants and children with congenital heart disease. Pediatr Radiol 32:518–522CrossRefPubMedGoogle Scholar
  41. 41.
    Liu P et al (2014) Quantitative assessment of global cerebral metabolic rate of oxygen (CMRO2) in neonates using MRI. NMR Biomed 27:332–340CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Chua S et al (1997) Fetal oxygen saturation during labour. BJOG Int J Obstet Gynaecol 104:1080–1083CrossRefGoogle Scholar
  43. 43.
    Dildy GA, Loucks CA, Clark SL (1993) Intrapartum fetal pulse oximetry in the presence of fetal cardiac arrhythmia. Am J Obstet Gynecol 169:1609–1611CrossRefPubMedGoogle Scholar
  44. 44.
    Dildy GA et al (1996) The relationship between oxygen saturation and pH in umbilical blood: implications for intrapartum fetal oxygen saturation monitoring. Am J Obstet Gynecol 175:682–687CrossRefPubMedGoogle Scholar
  45. 45.
    Avni R et al (2016) MR Imaging-derived oxygen-hemoglobin dissociation curves and fetal-placental oxygen-hemoglobin affinities. Radiology 280:68–77CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Bard H et al (1970) The relative rates of synthesis of hemoglobins A and F in immature red cells of newborn infants. Pediatrics 45:766–772PubMedGoogle Scholar
  47. 47.
    Weisskoff RM, Kiihne S (1992) MRI susceptometry: Image-based measurement of absolute susceptibility of MR contrast agents and human blood. Magn Reson Med 24:375–383CrossRefPubMedGoogle Scholar
  48. 48.
    Liu C et al (2015) Susceptibility-weighted imaging and quantitative susceptibility mapping in the brain. J Magn Reson Imaging 42:23–41CrossRefPubMedGoogle Scholar
  49. 49.
    Johnson G, Wadghiri YZ, Turnbull DH (1999) 2 D multislice and 3 D MRI sequences are often equally sensitive. Magn Reson Med 41:824–828CrossRefPubMedGoogle Scholar
  50. 50.
    Krishnamurthy U et al (2015) MR imaging of the fetal brain at 1.5 T and 3.0 T field strengths: comparing specific absorption rate (SAR) and image quality. J Perinat Med 43:209–220CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2017

Authors and Affiliations

  • Brijesh Kumar Yadav
    • 1
    • 2
  • Uday Krishnamurthy
    • 1
    • 2
  • Sagar Buch
    • 3
  • Pavan Jella
    • 1
  • Edgar Hernandez-Andrade
    • 4
    • 5
  • Lami Yeo
    • 4
    • 5
  • Steven J. Korzeniewski
    • 4
    • 5
    • 7
  • Anabela Trifan
    • 1
  • Sonia S. Hassan
    • 4
    • 5
  • E. Mark Haacke
    • 1
    • 2
    • 3
  • Roberto Romero
    • 4
    • 6
    • 7
    • 8
  • Jaladhar Neelavalli
    • 1
  1. 1.Department of RadiologyWayne State University School of MedicineDetroitUSA
  2. 2.Department of Biomedical EngineeringWayne State University College of EngineeringDetroitUSA
  3. 3.The MRI Institute for Biomedical ResearchWaterlooCanada
  4. 4.Perinatology Research BranchNICHD/NIH/DHHS, Hutzel Women’s HospitalDetroitUSA
  5. 5.Department of Obstetrics and GynecologyWayne State University School of MedicineDetroitUSA
  6. 6.Department of Obstetrics and GynecologyUniversity of MichiganAnn ArborUSA
  7. 7.Department of Epidemiology and BiostatisticsMichigan State UniversityEast LansingUSA
  8. 8.Center for Molecular Medicine and GeneticsWayne State UniversityDetroitUSA

Personalised recommendations