Non-invasive MRI measurements of venous oxygenation, oxygen extraction fraction and oxygen consumption in neonates

BACKGROUND AND PURPOSE Brain oxygen consumption reflects neuronal activity and can therefore be used to investigate brain development or neuronal injury in neonates. In this paper we present the first results of a non-invasive MRI method to evaluate whole brain oxygen consumption in neonates. MATERIALS AND METHODS For this study 51 neonates were included. The T1 and T2 of blood in the sagittal sinus were fitted using the 'T2 prepared tissue relaxation inversion recovery' pulse sequence (T2-TRIR). From the T1 and the T2 of blood, the venous oxygenation and the oxygen extraction fraction (OEF) were calculated. The cerebral metabolic rate of oxygen (CMRO2) was the resultant of the venous oxygenation and arterial spin labeling whole brain cerebral blood flow (CBF) measurements. RESULTS Venous oxygenation was 59±14% (mean±sd), OEF was 40±14%, CBF was 14±5ml/100g/min and CMRO2 was 30±12μmol/100g/min. The OEF in preterms at term-equivalent age was higher than in the preterms and in the infants with hypoxic-ischemic encephalopathy (p<0.01). The OEF, CBF and CMRO2 increased (p<0.01, <0.05 and <0.01, respectively) with postnatal age. CONCLUSION We presented an MRI technique to evaluate whole-brain oxygen consumption in neonates non-invasively. The measured values are in line with reference values found by invasive measurement techniques. Preterms and infants with HIE demonstrated significant lower oxygen extraction fraction than the preterms at term-equivalent age. This could be due to decreased neuronal activity as a reflection of brain development or as a result of tissue damage, increased cerebral blood flow due to immature or impaired autoregulation, or could be caused by differences in postnatal age.

[1]  Anders M. Dale,et al.  Diffuse optical imaging of brain activation: approaches to optimizing image sensitivity, resolution, and accuracy , 2004, NeuroImage.

[2]  D. Delpy,et al.  Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation. , 1988, Biochimica et biophysica acta.

[3]  J. Palis,et al.  Developmental biology of erythropoiesis. , 1998, Blood reviews.

[4]  K Farahani,et al.  MRI of thermally denatured blood: methemoglobin formation and relaxation effects. , 1999, Magnetic resonance imaging.

[5]  U. Kiechl‐Kohlendorfer,et al.  Adverse neurodevelopmental outcome in preterm infants: risk factor profiles for different gestational ages , 2009, Acta paediatrica.

[6]  Xavier Golay,et al.  A method for rapid in vivo measurement of blood T1 , 2011, NMR in biomedicine.

[7]  Agnese Suppiej,et al.  Can tissue oxygenation index (TOI) and cotside neurophysiological variables predict outcome in depressed/asphyxiated newborn infants? , 2007, Early human development.

[8]  Jeroen van der Grond,et al.  Cerebral Lactate and N-Acetyl-Aspartate/Choline Ratios in Asphyxiated Full-Term Neonates Demonstrated In Vivo Using Proton Magnetic Resonance Spectroscopy , 1994, Pediatric Research.

[9]  Frank van Bel,et al.  Cerebral oxygenation and cerebral oxygen extraction in the preterm infant: the impact of respiratory distress syndrome , 2006, Experimental Brain Research.

[10]  David Hinkley,et al.  Bootstrap Methods: Another Look at the Jackknife , 2008 .

[11]  B Hagberg,et al.  The changing panorama of cerebral palsy in Sweden. IX. Prevalence and origin in the birth‐year period 1995–1998 , 1996, Acta paediatrica.

[12]  Maria A Proytcheva,et al.  Issues in neonatal cellular analysis. , 2009, American journal of clinical pathology.

[13]  S K Warfield,et al.  Brain Perfusion in Asphyxiated Newborns Treated with Therapeutic Hypothermia , 2011, American Journal of Neuroradiology.

[14]  Hanzhang Lu,et al.  Noninvasive quantification of whole‐brain cerebral metabolic rate of oxygen (CMRO2) by MRI , 2009, Magnetic resonance in medicine.

[15]  P. Bandettini,et al.  QUIPSS II with thin‐slice TI1 periodic saturation: A method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling , 1999, Magnetic resonance in medicine.

[16]  W J Powers,et al.  Cerebral oxygen metabolism in newborns. , 1993, Pediatrics.

[17]  Peiying Liu,et al.  Quantitative assessment of global cerebral metabolic rate of oxygen (CMRO2) in neonates using MRI , 2014, NMR in biomedicine.

[18]  Jennifer M. Lynch,et al.  Cerebral Oxygen Metabolism in Neonates with Congenital Heart Disease Quantified by MRI and Optics , 2014, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[19]  P. Grant,et al.  Near-infrared spectroscopy assessment of cerebral oxygen metabolism in the developing premature brain , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[20]  O. Pryds,et al.  Vasoparalysis associated with brain damage in asphyxiated term infants. , 1990, The Journal of pediatrics.

[21]  Xavier Golay,et al.  Pulsed star labeling of arterial regions (PULSAR): A robust regional perfusion technique for high field imaging , 2005, Magnetic resonance in medicine.

[22]  P Ellen Grant,et al.  Acute injury to the immature brain with hypoxia with or without hypoperfusion. , 2006, Magnetic resonance imaging clinics of North America.

[23]  Karam Sidaros,et al.  Noninvasive Measurements of Regional Cerebral Perfusion in Preterm and Term Neonates by Magnetic Resonance Arterial Spin Labeling , 2006, Pediatric Research.

[24]  Hanzhang Lu,et al.  Quantitative evaluation of oxygenation in venous vessels using T2‐Relaxation‐Under‐Spin‐Tagging MRI , 2008, Magnetic resonance in medicine.

[25]  Jeroen Hendrikse,et al.  Regional changes in brain perfusion during brain maturation measured non-invasively with Arterial Spin Labeling MRI in neonates. , 2013, European Journal of Radiology.

[26]  Albert Macovski,et al.  Coronary Angiography with Magnetization‐Prepared T2 Contrast , 1995, Magnetic resonance in medicine.

[27]  Simon K. Warfield,et al.  Near-infrared spectroscopy versus magnetic resonance imaging to study brain perfusion in newborns with hypoxic–ischemic encephalopathy treated with hypothermia , 2014, NeuroImage.

[28]  Esben Thade Petersen,et al.  Model‐free arterial spin labeling quantification approach for perfusion MRI , 2006, Magnetic resonance in medicine.

[29]  Floris Groenendaal,et al.  Patterns of neonatal hypoxic–ischaemic brain injury , 2010, Neuroradiology.

[30]  Xavier Golay,et al.  Determining the longitudinal relaxation time (T1) of blood at 3.0 Tesla , 2004, Magnetic resonance in medicine.

[31]  M. Mintun,et al.  Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. , 1984, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[32]  N. Kissoon,et al.  Cerebral blood flow, cross-brain oxygen extraction, and fontanelle pressure after hypoxic-ischemic injury in newborn infants. , 1991, The Journal of pediatrics.

[33]  Valentina Vanzo,et al.  Influence of ventilation mode on neonatal cerebral blood flow and volume. , 2009, Early human development.

[34]  Xavier Golay,et al.  Sickle cell disease: continuous arterial spin-labeling perfusion MR imaging in children. , 2003, Radiology.

[35]  Jeremy F Magland,et al.  Rapid magnetic resonance measurement of global cerebral metabolic rate of oxygen consumption in humans during rest and hypercapnia , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[36]  W J Powers,et al.  Cerebral blood flow requirement for brain viability in newborn infants is lower than in adults , 1988, Annals of neurology.

[37]  Michael Bock,et al.  Arterial spin labeling in combination with a look‐locker sampling strategy: Inflow turbo‐sampling EPI‐FAIR (ITS‐FAIR) , 2001, Magnetic resonance in medicine.

[38]  B. Rosen,et al.  High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis , 1996, Magnetic resonance in medicine.

[39]  J. Detre,et al.  Why perfusion in neonates with congenital heart defects is negative--technical issues related to pulsed arterial spin labeling. , 2006, Magnetic resonance imaging.

[40]  M. Raichle,et al.  What is the Correct Value for the Brain-Blood Partition Coefficient for Water? , 1985, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[41]  A. Guyton,et al.  Textbook of Medical Physiology , 1961 .

[42]  J. Skatrud,et al.  Cerebrovascular response to arousal from NREM and REM sleep. , 2008, Sleep.

[43]  Yuan Shi,et al.  Changes of positron emission tomography in newborn infants at different gestational ages, and neonatal hypoxic-ischemic encephalopathy. , 2012, Pediatric neurology.

[44]  Peiying Liu,et al.  Calibration and validation of TRUST MRI for the estimation of cerebral blood oxygenation , 2012, Magnetic resonance in medicine.

[45]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  Esben Thade Petersen,et al.  Simultaneous OEF and Haematocrit assessment using T 2 Prepared Blood Relaxation Imaging with Inversion Recovery , 2011 .

[47]  N Catherine,et al.  Developmental hematopoiesis in normal human fetal blood. , 1991, Blood.

[48]  Kjell Erlandsson,et al.  Cerebral Glucose Metabolism Measured by Positron Emission Tomography in Term Newborn Infants with Hypoxic Ischemic Encephalopathy , 1999, Pediatric Research.

[49]  Jeroen Hendrikse,et al.  Arterial Spin Labeling Magnetic Resonance Imaging: Intracranial and Emerging Extracranial Applications. , 2013, PET clinics.

[50]  David A Boas,et al.  Assessment of Infant Brain Development With Frequency-Domain Near-Infrared Spectroscopy , 2007, Pediatric Research.

[51]  R. Zaizov,et al.  POSTNATAL CHANGES IN SOME RED CELL PARAMETERS , 1971, Acta paediatrica Scandinavica.

[52]  R. Christensen,et al.  Hematologic Problems of the Neonate , 2000 .

[53]  L. Skov,et al.  Estimation of Cerebral Venous Saturation in Newborn Infants by Near Infrared Spectroscopy , 1993, Pediatric Research.

[54]  Gunnar Naulaers,et al.  Effect of Treatment of Subclinical Neonatal Seizures Detected With aEEG: Randomized, Controlled Trial , 2010, Pediatrics.

[55]  F Wingert,et al.  Brain growth in man. , 1986, Bibliotheca anatomica.

[56]  T. Borza,et al.  Diffusional water permeability of mammalian red blood cells. , 1995, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[57]  Paolo Tagliabue,et al.  Near Infrared Spectroscopy in healthy preterm and term newborns: correlation with gestational age and standard monitoring parameters. , 2009, Current neurovascular research.