Skip to main content
SpringerLink
Log in

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

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objective

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.

Methods

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.

Results

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.

Conclusion

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3.

Similar content being viewed by others

Abbreviations

SWI:

Susceptibility-weighted imaging

MRI:

Magnetic resonance imaging

SSS:

Superior sagittal sinus

S v O 2 :

Venous oxygen saturation

∆χ v :

Magnetic susceptibility

∆χ do :

Magnetic susceptibility difference between fully oxygenated and deoxygenated foetal blood

Hct :

Haematocrit

HbF:

Foetal haemoglobin

HbA:

Adult haemoglobin

FHR:

Foetal heart rate

GA:

Gestational age

References

  1. Schneider H (2011) Oxygenation of the placental–fetal unit in humans. Respir Physiol Neurobiol 178:51–58

    Article  PubMed  Google Scholar 

  2. Baschat AA (2004) Pathophysiology of fetal growth restriction: implications for diagnosis and surveillance. Obstet Gynecol Surv 59:617–627

    Article  PubMed  Google Scholar 

  3. Baschat DAA (2004) Fetal responses to placental insufficiency: an update. BJOG Int J Obstet Gynaecol 111:1031–1041

    Article  CAS  Google Scholar 

  4. Valcamonico A et al (1994) Absent end-diastolic velocity in umbilical artery: risk of neonatal morbidity and brain damage. Am J Obstet Gynecol 170:796–801

    Article  CAS  PubMed  Google Scholar 

  5. Gramellini D et al (1992) Cerebral-umbilical Doppler ratio as a predictor of adverse perinatal outcome. Obstet Gynecol 79:416–420

    Article  CAS  PubMed  Google Scholar 

  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 2:266–271

    Article  CAS  PubMed  Google Scholar 

  7. Al-Ghazali W et al (1989) Evidence of redistribution of cardiac output in asymmetrical growth retardation. BJOG Int J Obstet Gynaecol 96:697–704

    Article  CAS  Google Scholar 

  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 19:140–146

    Article  CAS  PubMed  Google Scholar 

  9. Dubiel M, Gunnarsson G, Gudmundsson S (2002) Blood redistribution in the fetal brain during chronic hypoxia. Ultrasound Obstet Gynecol 20:117–121

    Article  CAS  PubMed  Google Scholar 

  10. Wladimiroff J, Tonge H, Stewart P (1986) Doppler ultrasound assessment of cerebral blood flow in the human fetus. BJOG Int J Obstet Gynaecol 93:471–475

    Article  CAS  Google Scholar 

  11. Rosen K, Kjellmer I (1975) Changes in the fetal heart rate and ECG during hypoxia. Acta Physiol 93:59–66

    Article  CAS  Google Scholar 

  12. Parer J et al (1980) Increased fetal heart rate variability with acute hypoxia in chronically instrumented sheep. Eur J Obstet Gynecol Reprod Biol 10:393–399

    Article  CAS  PubMed  Google Scholar 

  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 95:980–989

    Article  CAS  Google Scholar 

  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 175:63–72

    Article  CAS  PubMed  Google Scholar 

  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 98:820–823

    Article  CAS  Google Scholar 

  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 30:502–509

    Article  CAS  PubMed  Google Scholar 

  17. Vintzileos AM et al (2005) Transabdominal fetal pulse oximetry with near-infrared spectroscopy. Am J Obstet Gynecol 192:129–133

    Article  PubMed  Google Scholar 

  18. Rutherford M et al (2008) MR imaging methods for assessing fetal brain development. Develop Neurobiol 68:700–711

    Article  CAS  Google Scholar 

  19. Levine D et al (2003) Fast MR imaging of fetal central nervous system abnormalities 1. Radiology 229:51–61

    Article  PubMed  Google Scholar 

  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 111:784–792

    Article  CAS  Google Scholar 

  21. Wolfberg AJ et al (2007) Identification of fetal cerebral lactate using magnetic resonance spectroscopy. Am J Obstet Gynecol 196:e9–e11

    Article  PubMed  Google Scholar 

  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. e7

    Article  Google Scholar 

  23. Zhu MY et al (2016) The hemodynamics of late-onset intrauterine growth restriction by MRI. Am J Obstet Gynecol 214:367. e1–367. e17

    Article  Google Scholar 

  24. Stuber M et al (2002) Preliminary report on in vivo coronary MRA at 3 Tesla in humans. Magn Reson Med 48:425–429

    Article  PubMed  Google Scholar 

  25. Frayne R et al (2003) Magnetic resonance imaging at 3.0 Tesla: challenges and advantages in clinical neurological imaging. Investig Radiol 38:385–402

    Google Scholar 

  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 5:341–346

    Article  CAS  PubMed  Google Scholar 

  27. Fernández-Seara MA et al (2006) MR susceptometry for measuring global brain oxygen extraction. Magn Reson Med 55:967–973

    Article  PubMed  Google Scholar 

  28. Vegh V et al. (2015) Selective channel combination of MRI signal phase. Magnetic Resonance in Medicine

  29. Neelavalli J et al (2014) Measuring venous blood oxygenation in fetal brain using susceptibility-weighted imaging. J Magn Reson Imaging 39:998–1006

    Article  PubMed  PubMed Central  Google Scholar 

  30. Cheema R et al (2004) Fetal cerebral venous Doppler velocimetry in normal and high-risk pregnancy. Ultrasound Obstet Gynecol 24:147–153

    Article  CAS  PubMed  Google Scholar 

  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 151:333–337

    Article  CAS  PubMed  Google Scholar 

  32. Wang Y et al (2000) Artery and vein separation using susceptibility-dependent phase in contrast-enhanced MRA. J Magn Reson Imaging 12:661–670

    Article  CAS  PubMed  Google Scholar 

  33. Boulot P et al (1993) Hematologic values of fetal blood obtained by means of cordocentesis. Fetal Diagn Ther 8:309–316

    Article  CAS  PubMed  Google Scholar 

  34. Jain V, Langham MC, Wehrli FW (2010) MRI estimation of global brain oxygen consumption rate. J Cereb Blood Flow Metab 30:1598–1607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 45:533–542

    Article  CAS  PubMed  Google Scholar 

  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 German

    Article  CAS  PubMed  Google Scholar 

  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 34:380–388

    Article  CAS  PubMed  Google Scholar 

  38. Burton G, Jaunaiux E (2001) Maternal vascularisation of the human placenta: does the embryo develop in a hypoxic environment? Gynécologie Obstétrique Fertilité 29:503–508

    Article  CAS  Google Scholar 

  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 169:1393–1398

    Article  CAS  PubMed  Google Scholar 

  40. Nield LE et al (2002) MRI-based blood oxygen saturation measurements in infants and children with congenital heart disease. Pediatr Radiol 32:518–522

    Article  PubMed  Google Scholar 

  41. Liu P et al (2014) Quantitative assessment of global cerebral metabolic rate of oxygen (CMRO2) in neonates using MRI. NMR Biomed 27:332–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Chua S et al (1997) Fetal oxygen saturation during labour. BJOG Int J Obstet Gynaecol 104:1080–1083

    Article  CAS  Google Scholar 

  43. Dildy GA, Loucks CA, Clark SL (1993) Intrapartum fetal pulse oximetry in the presence of fetal cardiac arrhythmia. Am J Obstet Gynecol 169:1609–1611

    Article  CAS  PubMed  Google Scholar 

  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 175:682–687

    Article  CAS  PubMed  Google Scholar 

  45. Avni R et al (2016) MR Imaging-derived oxygen-hemoglobin dissociation curves and fetal-placental oxygen-hemoglobin affinities. Radiology 280:68–77

    Article  PubMed  PubMed Central  Google Scholar 

  46. Bard H et al (1970) The relative rates of synthesis of hemoglobins A and F in immature red cells of newborn infants. Pediatrics 45:766–772

    CAS  PubMed  Google Scholar 

  47. Weisskoff RM, Kiihne S (1992) MRI susceptometry: Image-based measurement of absolute susceptibility of MR contrast agents and human blood. Magn Reson Med 24:375–383

    Article  CAS  PubMed  Google Scholar 

  48. Liu C et al (2015) Susceptibility-weighted imaging and quantitative susceptibility mapping in the brain. J Magn Reson Imaging 42:23–41

    Article  PubMed  Google Scholar 

  49. Johnson G, Wadghiri YZ, Turnbull DH (1999) 2 D multislice and 3 D MRI sequences are often equally sensitive. Magn Reson Med 41:824–828

    Article  CAS  PubMed  Google Scholar 

  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 43:209–220

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

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

Funding

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.

Author information

Authors and Affiliations

  1. Department of Radiology, Wayne State University School of Medicine, 4201 St. Antoine, Detroit, MI, 48201, USA

    Brijesh Kumar Yadav, Uday Krishnamurthy, Pavan Jella, Anabela Trifan, E. Mark Haacke & Jaladhar Neelavalli

  2. Department of Biomedical Engineering, Wayne State University College of Engineering, Detroit, MI, USA

    Brijesh Kumar Yadav, Uday Krishnamurthy & E. Mark Haacke

  3. The MRI Institute for Biomedical Research, Waterloo, ON, Canada

    Sagar Buch & E. Mark Haacke

  4. Perinatology Research Branch, NICHD/NIH/DHHS, Hutzel Women’s Hospital, 3990 John R, 4 Brush, Detroit, MI, 48201, USA

    Edgar Hernandez-Andrade, Lami Yeo, Steven J. Korzeniewski, Sonia S. Hassan & Roberto Romero

  5. Department of Obstetrics and Gynecology, Wayne State University School of Medicine, Detroit, MI, USA

    Edgar Hernandez-Andrade, Lami Yeo, Steven J. Korzeniewski & Sonia S. Hassan

  6. Department of Obstetrics and Gynecology, University of Michigan, Ann Arbor, MI, USA

    Roberto Romero

  7. Department of Epidemiology and Biostatistics, Michigan State University, East Lansing, MI, USA

    Steven J. Korzeniewski & Roberto Romero

  8. Center for Molecular Medicine and Genetics, Wayne State University, Detroit, MI, USA

    Roberto Romero

Authors
  1. Brijesh Kumar Yadav
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Uday Krishnamurthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sagar Buch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pavan Jella
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Edgar Hernandez-Andrade
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lami Yeo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Steven J. Korzeniewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anabela Trifan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sonia S. Hassan
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. E. Mark Haacke
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Roberto Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jaladhar Neelavalli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Roberto Romero or Jaladhar Neelavalli.

Ethics declarations

Guarantor

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.

Methodology

• prospective

• experimental

• performed at one institution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yadav, B.K., Krishnamurthy, U., Buch, S. et al. Imaging putative foetal cerebral blood oxygenation using susceptibility weighted imaging (SWI). Eur Radiol 28, 1884–1890 (2018). https://doi.org/10.1007/s00330-017-5160-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-017-5160-x

Keywords

Search

Navigation