Abstract
Purpose
Hyperperfusion may be related to outcome in neonates with hypoxic-ischemic encephalopathy (HIE). The purpose of this study was to evaluate whether arterial spin labelling (ASL) perfusion is associated with outcome in neonates with HIE and to compare the predictive value of ASL MRI to known MRI predictive markers.
Methods
Twenty-eight neonates diagnosed with HIE and assessed with MR imaging (conventional MRI, diffusion-weighted MRI, MR spectroscopy [MRS], and ASL MRI) were included. Perfusion in the basal ganglia and thalami was measured. Outcome at 9 or 18 months of age was scored as either adverse (death or cerebral palsy) or favourable.
Results
The median (range) perfusion in the basal ganglia and thalami (BGT) was 63 (28-108) ml/100 g/min in the neonates with adverse outcome and 28 (12-51) ml/100 g/min in the infants with favourable outcome (p < 0.01). The area-under-the-curve was 0.92 for ASL MRI, 0.97 for MRI score, 0.96 for Lac/NAA and 0.92 for ADC in the BGT. The combination of Lac/NAA and ASL MRI results was the best predictor of outcome (r 2 = 0.86, p < 0.001).
Conclusion
Higher ASL perfusion values in neonates with HIE are associated with a worse neurodevelopmental outcome. A combination of the MRS and ASL MRI information is the best predictor of outcome.
Key Points
• Arterial spin labelling MRI can predict outcome in neonates with hypoxic-ischemic encephalopathy
• Basal ganglia and thalami perfusion is higher in neonates with adverse outcome
• Arterial spin labelling complements known MRI parameters in the prediction of outcome
• The combined information of ASL and MRS measurements is the best predictor of outcome
Similar content being viewed by others
Abbreviations
- ADC:
-
Apparent diffusion coefficient
- aEEG:
-
Amplitude-integrated electroencephalography
- ASL:
-
Arterial spin labelling
- AUC:
-
Area under the curve
- CBF:
-
Cerebral blood flow
- Cho:
-
Choline
- Cr:
-
Creatine
- DWI:
-
Diffusion-weighted imaging
- EPI:
-
Echo-planar imaging
- HIE:
-
Hypoxic-ischemic encephalopathy
- 1H MRS:
-
Proton spectroscopy
- ICC:
-
Intraclass correlation coefficient
- Lac:
-
Lactate
- MRI:
-
Magnetic Resonance Imaging
- NAA:
-
N-acetylaspartate
- Pulsar:
-
Pulsed star labelling of arterial regions
- ROI:
-
Region of interest
- SNR:
-
Signal-to-noise ratio
- T1b :
-
Longitudinal relaxation rate of blood
References
Himmelmann K, Hagberg G, Beckung E, Hagberg B, Uvebrant P (2005) The changing panorama of cerebral palsy in Sweden. IX. Prevalence and origin in the birth-year period 1995-1998. Acta Paediatr 94(3):287–294
Wyatt JS, Gluckman PD, Liu PY et al (2007) Determinants of outcomes after head cooling for neonatal encephalopathy. Pediatrics 119(5):912–921
Dilenge ME, Majnemer A, Shevell MI (2001) Long-term developmental outcome of asphyxiated term neonates. J Child Neurol 16(11):781–792
Jouvet P, Cowan FM, Cox P et al (1999) Reproducibility and accuracy of MR imaging of the brain after severe birth asphyxia. AJNR Am J Neuroradiol 20(7):1343–1348
Boichot C, Walker PM, Durand C et al (2006) Term neonate prognoses after perinatal asphyxia: contributions of MR imaging, MR spectroscopy, relaxation times, and apparent diffusion coefficients. Radiology 239(3):839–848
Thayyil S, Chandrasekaran M, Taylor A et al (2010) Cerebral magnetic resonance biomarkers in neonatal encephalopathy: a meta-analysis. Pediatrics 125(2):e382–e395
Rutherford M, Counsell S, Allsop J et al (2004) Diffusion-weighted magnetic resonance imaging in term perinatal brain injury: a comparison with site of lesion and time from birth. Pediatrics 114(4):1004–1014
Pryds O, Greisen G, Lou H, Friis-Hansen B (1990) Vasoparalysis associated with brain damage in asphyxiated term infants. J Pediatr 117(1):119–125
van Bel F, Dorrepaal CA, Benders MJ, Zeeuwe PE, van de Bor M, Berger HM (1993) Changes in cerebral hemodynamics and oxygenation in the first 24 hours after birth asphyxia. Pediatrics 92(3):365–372
Rutherford M, Ward P, Allsop J, Malamatentiou C, Counsell S (2005) Magnetic resonance imaging in neonatal encephalopathy. Early Hum Dev 81(1):13–25
Grant PE, Yu D (2006) Acute injury to the immature brain with hypoxia with or without hypoperfusion. Magn Reson Imaging Clin N Am 14(2):271–285
Meek JH, Elwell CE, McCormick DC et al (1999) Abnormal cerebral haemodynamics in perinatally asphyxiated neonates related to outcome. Arch Dis Child Fetal Neonatal 81(2):110–115
Rosenbaum JL, Almli CR, Yundt KD, Altman DI, Powers WJ (1997) Higher neonatal cerebral blood flow correlates with worse childhood neurologic outcome. Neurology 49(4):1035–1041
Wintermark P, Moessinger AC, Gudinchet F, Meuli R (2008) Temporal evolution of MR perfusion in neonatal hypoxic-ischemic encephalopathy. J Magn Reson Imaging 27(6):1229–1234
Blennow M, Ingvar M, Lagercrantz H et al (1995) Early [18 F]FDG positron emission tomography in infants with hypoxic-ischaemic encephalopathy shows hypermetabolism during the postasphyctic period. Acta Paediatr 84(11):1289–1295
Miranda MJ, Olofsson K, Sidaros K (2006) Noninvasive measurements of regional cerebral perfusion in preterm and term neonates by magnetic resonance arterial spin labeling. Pediatr Res 60(3):359–363
Pienaar R, Paldino MJ, Madan N et al (2012) A quantitative method for correlating observations of decreased apparent diffusion coefficient with elevated cerebral blood perfusion in newborns presenting cerebral ischemic insults. Neuroimage 63(3):1510–1518
Wintermark P, Warfield S. New Insights in Perinatal Arterial Ischemic Stroke by Assessing Brain Perfusion. Transl Stroke Res 2011; Available at: http://www.springerlink.com (Accessed 10 November 2011)
De Vis JB, Petersen ET, de Vries LS et al (2013) Regional changes in brain perfusion during brain maturation measured non-invasively with Arterial Spin Labeling MRI in neonates. Eur J Radiol 82(3):538–543
Petersen ET, Zimine I, Ho Y-CL, Golay X (2006) Non-invasive measurement of perfusion: a critical review of arterial spin labelling techniques. Br J Radiol 79(944):688–701
De Vis JB, Petersen ET, Kersbergen KJ et al (2013) Evaluation of perinatal arterial ischemic stroke using noninvasive arterial spin labeling perfusion MRI. Pediatr Res 74(3):307–313
Shi H, Song D, Zhang YX et al (2012) Analysis of arterial spin labeling in 33 patients with hypoxic ischemic encephalopathy. Zhonghua Er Ke Za Zhi 50(2):131–135
Wintermark P, Hansen A, Gregas MC et al (2011) Brain perfusion in asphyxiated newborns treated with therapeutic hypothermia. AJNR Am J Neuroradiol 32(11):2023–2029
Massaro AN, Bouyssi-Kobar M, Chang T, Vezina LG, du Plessis AJ, Limperopoulos C (2013) Brain perfusion in encephalopathic newborns after therapeutic hypothermia. AJNR Am J Neuroradiol 34(8):1649–1655
van Rooij LG, Toet MC, van Huffelen AC et al (2010) Effect of treatment of subclinical neonatal seizures detected with aEEG: randomized, controlled trial. Pediatrics 125(2):e358–e366
Lemmers PM, Zwanenburg RJ, Benders MJ et al (2013) Cerebral oxygenation and brain activity after perinatal asphyxia: does hypothermia change their prognostic value? Pediatr Res 74(2):180–185
Shankaran S, Laptook AR, Ehrenkranz RA et al (2005) Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med 353(15):1574–1584
Thompson CM, Puterman AS, Linley LL et al (1997) The value of a scoring system for hypoxic ischaemic encephalopathy in predicting neurodevelopmental outcome. Acta Paediatr 86(7):757–761
al Naqeeb N, Edwards AD, Cowan FM, Azzopardi D (1999) Assessment of neonatal encephalopathy by amplitude-integrated electroencephalography. Pediatrics 103(6):1263–1271
Golay X, Petersen ET, Hui F (2005) Pulsed star labeling of arterial regions (PULSAR): a robust regional perfusion technique for high field imaging. Magn Reson Med 53(1):15–21
Luh WM, Wong EC, Pa B, Hyde JS (1999) QUIPSS II with thin-slice TI1 periodic saturation: a method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling. Magn Reson Med 41(6):1246–1254
Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR (1998) A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med 40(3):383–396
Varela M, Hajnal JV, Petersen ET, Golay X, Merchant N, Larkman DJ (2011) A method for rapid in vivo measurement of blood T1. NMR Biomed 24(1):80–88
de Vries LS, Groenendaal F (2010) Patterns of neonatal hypoxic-ischaemic brain injury. Neuroradiology 52(6):555–566
Roelants-Van Rijn AM, van der Grond J, de Vries LS, Groenendaal F (2001) Value of (1)H-MRS using different echo times in neonates with cerebral hypoxia-ischemia. Pediatr Res 49(3):356–362
Alderliesten T, de Vries LS, Benders MJ, Koopman C, Groenendaal F (2011) MR imaging and outcome of term neonates with perinatal asphyxia: value of diffusion-weighted MR imaging and (1)H MR spectroscopy. Radiology 261(1):235–242
Rutherford MA, Pennock JM, Murdoch-Eaton DM, Cowan FM, Dubowitz LM (1992) Athetoid cerebral palsy with cysts in the putamen after hypoxic-ischaemic encephalopathy. Arch Dis Child 67(7):846–850
Roberts I, Sydenham E (2012) Barbiturates for acute traumatic brain injury. Cochrane Database Syst Rev. doi:10.1002/14651858
Kinoshita H, Nakahata K, Dojo M et al (2004) Lidocaine impairs vasodilation mediated by adenosine triphosphate-sensitive K + channels but not by inward rectifier K + channels in rat cerebral microvessels. Anesth Analg 99(3):904–909
de Nadal M, Munar F, Poca MA et al (2000) Cerebral hemodynamic effects of morphine and fentanyl in patients with severe head injury: absence of correlation to cerebral autoregulation. Anesthesiology 92(1):11–19
Bingham RM, Hinds CJ (1987) Influence of bolus doses of phenoperidine on intracranial pressure and systemic arterial pressure in traumatic coma. Br J Anaesth 59(5):592–595
Bandres J, Yao L, Nemoto EM et al (1992) Effects of dobutamine and dopamine on whole brain blood flow and metabolism in unanesthetized monkeys. J Neurosurg Anesthesiol 4(4):250–256
Youden WJ (1950) Index for rating diagnostic tests. Cancer 3(1):32–35
Okereafor A, Allsop J, Counsell SJ et al (2008) Patterns of brain injury in neonates exposed to perinatal sentinel events. Pediatrics 121(5):906–914
Wang J, Licht DJ, Jahng G-H et al (2006) Pediatric perfusion imaging using pulsed arterial spin labeling. J Magn Reson Imaging 24(3):249–254
De Vis JB, Hendrikse J, Groenendaal F et al (2014) Impact of neonate haematocrit variability on the longitudinal relaxation time of blood: Implications for arterial spin labelling MRI. Neuroimage Clin 4:517–525
Roche-Labarbe N, Fenoglio A, Aggarwal A et al (2012) Near-infrared spectroscopy assessment of cerebral oxygen metabolism in the developing premature brain. J Cereb Blood Flow Metab 32(3):481–488
Acknowledgments
The scientific guarantor of this publication is Jill Britt De Vis. 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. This study received funding from the Dutch Technology Foundation STW, Applied Science Division of NWO, the technology program of the Ministry of Economic Affairs, and the ZonMw electromagnetic fields and health program. No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained. Written informed consent was waived by the Institutional Review Board. Methodology: prospective diagnostic or prognostic study, performed at one institution.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
De Vis, J.B., Hendrikse, J., Petersen, E.T. et al. Arterial spin-labelling perfusion MRI and outcome in neonates with hypoxic-ischemic encephalopathy. Eur Radiol 25, 113–121 (2015). https://doi.org/10.1007/s00330-014-3352-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-014-3352-1