Magnetic resonance spectroscopy assessment of brain injury after moderate hypothermia in neonatal encephalopathy: a prospective multicentre cohort study

In neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention, complicating early prognostication and rendering trials of promising neuroprotectants slow and expensive. We aimed to determine the accuracy of thalamic proton magneti...

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Published in:	Lancet neurology Vol. 18; no. 1; pp. 35 - 45
Main Authors:	Lally, Peter J, Montaldo, Paolo, Oliveira, Vânia, Soe, Aung, Swamy, Ravi, Bassett, Paul, Mendoza, Josephine, Atreja, Gaurav, Kariholu, Ujwal, Pattnayak, Santosh, Sashikumar, Palaniappan, Harizaj, Helen, Mitchell, Martin, Ganesh, Vijayakumar, Harigopal, Sundeep, Dixon, Jennifer, English, Philip, Clarke, Paul, Muthukumar, Priya, Satodia, Prakash, Wayte, Sarah, Abernethy, Laurence J, Yajamanyam, Kiran, Bainbridge, Alan, Price, David, Huertas, Angela, Sharp, David J, Kalra, Vaneet, Chawla, Sanjay, Shankaran, Seetha, Thayyil, Sudhin, Harigopal, Sundeeep
Format:	Journal Article
Language:	English
Published:	England Elsevier Ltd 01.01.2019 Elsevier Limited Lancet Pub. Group
Subjects:	Accuracy Anisotropy Aspartic Acid - analogs & derivatives Aspartic Acid - metabolism Basal ganglia Biomarkers Brain - diagnostic imaging Brain - metabolism Brain injury Brain research Choline Clinical trials Cohort analysis Congenital defects Cortex Creatine EEG Encephalopathy Female Humans Hypothermia Hypothermia, Induced Hypoxia-Ischemia, Brain - diagnostic imaging Hypoxia-Ischemia, Brain - metabolism Hypoxia-Ischemia, Brain - therapy Infant Infant, Newborn Infants Intensive care units Lactic acid Magnetic resonance imaging Magnetic Resonance Spectroscopy Male N-Acetylaspartate Neonates Neurodevelopmental disorders Neuroprotection Newborn babies NMR Nuclear magnetic resonance Prospective Studies Protons Scanners Software Spectrum analysis Thalamus Traumatic brain injury Treatment Outcome United Kingdom > UK United States > US
ISSN:	1474-4422, 1474-4465, 1474-4465
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Abstract	In neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention, complicating early prognostication and rendering trials of promising neuroprotectants slow and expensive. We aimed to determine the accuracy of thalamic proton magnetic resonance (MR) spectroscopy (MRS) biomarkers as early predictors of the neurodevelopmental abnormalities observed years after neonatal encephalopathy. We did a prospective multicentre cohort study across eight neonatal intensive care units in the UK and USA, recruiting term and near-term neonates who received therapeutic hypothermia for neonatal encephalopathy. We excluded infants with life-threatening congenital malformations, syndromic disorders, neurometabolic diseases, or any alternative diagnoses for encephalopathy that were apparent within 6 h of birth. We obtained T1-weighted, T2-weighted, and diffusion-weighted MRI and thalamic proton MRS 4–14 days after birth. Clinical neurodevelopmental tests were done 18–24 months later. The primary outcome was the association between MR biomarkers and an adverse neurodevelopmental outcome, defined as death or moderate or severe disability, measured using a multivariable prognostic model. We used receiver operating characteristic (ROC) curves to examine the prognostic accuracy of the individual biomarkers. This trial is registered with ClinicalTrials.gov, number NCT01309711. Between Jan 29, 2013, and June 25, 2016, we recruited 223 infants who all underwent MRI and MRS at a median age of 7 days (IQR 5–10), with 190 (85%) followed up for neurological examination at a median age of 23 months (20–25). Of those followed up, 31 (16%) had moderate or severe disability, including one death. Multiple logistic regression analysis could not be done because thalamic N-acetylaspartate (NAA) concentration alone accurately predicted an adverse neurodevelopmental outcome (area under the curve [AUC] of 0·99 [95% CI 0·94–1·00]; sensitivity 100% [74–100]; specificity 97% [90–100]; n=82); the models would not converge when any additional variable was examined. The AUC (95% CI) of clinical examination at 6 h (n=190) and at discharge (n=167) were 0·72 (0·65–0·78) and 0·60 (0·53–0·68), respectively, and the AUC of abnormal amplitude integrated EEG at 6 h (n=169) was 0·73 (0·65–0·79). On conventional MRI (n=190), cortical injury had an AUC of 0·67 (0·60–0·73), basal ganglia or thalamic injury had an AUC of 0·81 (0·75–0·87), and abnormal signal in the posterior limb of internal capsule (PLIC) had an AUC of 0·82 (0·76–0·87). Fractional anisotropy of PLIC (n=65) had an AUC of 0·82 (0·76–0·87). MRS metabolite peak-area ratios (n=160) of NAA–creatine (<1·29) had an AUC of 0·79 (0·72–0·85), of NAA–choline had an AUC of 0·74 (0·66–0·80), and of lactate–NAA (>0·22) had an AUC of 0·94 (0·89–0·97). Thalamic proton MRS measures acquired soon after birth in neonatal encephalopathy had the highest accuracy to predict neurdevelopment 2 years later. These methods could be applied to increase the power of neuroprotection trials while reducing their duration. National Institute for Health Research UK.
AbstractList	In neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention, complicating early prognostication and rendering trials of promising neuroprotectants slow and expensive. We aimed to determine the accuracy of thalamic proton magnetic resonance (MR) spectroscopy (MRS) biomarkers as early predictors of the neurodevelopmental abnormalities observed years after neonatal encephalopathy.BACKGROUNDIn neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention, complicating early prognostication and rendering trials of promising neuroprotectants slow and expensive. We aimed to determine the accuracy of thalamic proton magnetic resonance (MR) spectroscopy (MRS) biomarkers as early predictors of the neurodevelopmental abnormalities observed years after neonatal encephalopathy.We did a prospective multicentre cohort study across eight neonatal intensive care units in the UK and USA, recruiting term and near-term neonates who received therapeutic hypothermia for neonatal encephalopathy. We excluded infants with life-threatening congenital malformations, syndromic disorders, neurometabolic diseases, or any alternative diagnoses for encephalopathy that were apparent within 6 h of birth. We obtained T1-weighted, T2-weighted, and diffusion-weighted MRI and thalamic proton MRS 4-14 days after birth. Clinical neurodevelopmental tests were done 18-24 months later. The primary outcome was the association between MR biomarkers and an adverse neurodevelopmental outcome, defined as death or moderate or severe disability, measured using a multivariable prognostic model. We used receiver operating characteristic (ROC) curves to examine the prognostic accuracy of the individual biomarkers. This trial is registered with ClinicalTrials.gov, number NCT01309711.METHODSWe did a prospective multicentre cohort study across eight neonatal intensive care units in the UK and USA, recruiting term and near-term neonates who received therapeutic hypothermia for neonatal encephalopathy. We excluded infants with life-threatening congenital malformations, syndromic disorders, neurometabolic diseases, or any alternative diagnoses for encephalopathy that were apparent within 6 h of birth. We obtained T1-weighted, T2-weighted, and diffusion-weighted MRI and thalamic proton MRS 4-14 days after birth. Clinical neurodevelopmental tests were done 18-24 months later. The primary outcome was the association between MR biomarkers and an adverse neurodevelopmental outcome, defined as death or moderate or severe disability, measured using a multivariable prognostic model. We used receiver operating characteristic (ROC) curves to examine the prognostic accuracy of the individual biomarkers. This trial is registered with ClinicalTrials.gov, number NCT01309711.Between Jan 29, 2013, and June 25, 2016, we recruited 223 infants who all underwent MRI and MRS at a median age of 7 days (IQR 5-10), with 190 (85%) followed up for neurological examination at a median age of 23 months (20-25). Of those followed up, 31 (16%) had moderate or severe disability, including one death. Multiple logistic regression analysis could not be done because thalamic N-acetylaspartate (NAA) concentration alone accurately predicted an adverse neurodevelopmental outcome (area under the curve [AUC] of 0·99 [95% CI 0·94-1·00]; sensitivity 100% [74-100]; specificity 97% [90-100]; n=82); the models would not converge when any additional variable was examined. The AUC (95% CI) of clinical examination at 6 h (n=190) and at discharge (n=167) were 0·72 (0·65-0·78) and 0·60 (0·53-0·68), respectively, and the AUC of abnormal amplitude integrated EEG at 6 h (n=169) was 0·73 (0·65-0·79). On conventional MRI (n=190), cortical injury had an AUC of 0·67 (0·60-0·73), basal ganglia or thalamic injury had an AUC of 0·81 (0·75-0·87), and abnormal signal in the posterior limb of internal capsule (PLIC) had an AUC of 0·82 (0·76-0·87). Fractional anisotropy of PLIC (n=65) had an AUC of 0·82 (0·76-0·87). MRS metabolite peak-area ratios (n=160) of NAA-creatine (<1·29) had an AUC of 0·79 (0·72-0·85), of NAA-choline had an AUC of 0·74 (0·66-0·80), and of lactate-NAA (>0·22) had an AUC of 0·94 (0·89-0·97).FINDINGSBetween Jan 29, 2013, and June 25, 2016, we recruited 223 infants who all underwent MRI and MRS at a median age of 7 days (IQR 5-10), with 190 (85%) followed up for neurological examination at a median age of 23 months (20-25). Of those followed up, 31 (16%) had moderate or severe disability, including one death. Multiple logistic regression analysis could not be done because thalamic N-acetylaspartate (NAA) concentration alone accurately predicted an adverse neurodevelopmental outcome (area under the curve [AUC] of 0·99 [95% CI 0·94-1·00]; sensitivity 100% [74-100]; specificity 97% [90-100]; n=82); the models would not converge when any additional variable was examined. The AUC (95% CI) of clinical examination at 6 h (n=190) and at discharge (n=167) were 0·72 (0·65-0·78) and 0·60 (0·53-0·68), respectively, and the AUC of abnormal amplitude integrated EEG at 6 h (n=169) was 0·73 (0·65-0·79). On conventional MRI (n=190), cortical injury had an AUC of 0·67 (0·60-0·73), basal ganglia or thalamic injury had an AUC of 0·81 (0·75-0·87), and abnormal signal in the posterior limb of internal capsule (PLIC) had an AUC of 0·82 (0·76-0·87). Fractional anisotropy of PLIC (n=65) had an AUC of 0·82 (0·76-0·87). MRS metabolite peak-area ratios (n=160) of NAA-creatine (<1·29) had an AUC of 0·79 (0·72-0·85), of NAA-choline had an AUC of 0·74 (0·66-0·80), and of lactate-NAA (>0·22) had an AUC of 0·94 (0·89-0·97).Thalamic proton MRS measures acquired soon after birth in neonatal encephalopathy had the highest accuracy to predict neurdevelopment 2 years later. These methods could be applied to increase the power of neuroprotection trials while reducing their duration.INTERPRETATIONThalamic proton MRS measures acquired soon after birth in neonatal encephalopathy had the highest accuracy to predict neurdevelopment 2 years later. These methods could be applied to increase the power of neuroprotection trials while reducing their duration.National Institute for Health Research UK.FUNDINGNational Institute for Health Research UK. In neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention, complicating early prognostication and rendering trials of promising neuroprotectants slow and expensive. We aimed to determine the accuracy of thalamic proton magnetic resonance (MR) spectroscopy (MRS) biomarkers as early predictors of the neurodevelopmental abnormalities observed years after neonatal encephalopathy. We did a prospective multicentre cohort study across eight neonatal intensive care units in the UK and USA, recruiting term and near-term neonates who received therapeutic hypothermia for neonatal encephalopathy. We excluded infants with life-threatening congenital malformations, syndromic disorders, neurometabolic diseases, or any alternative diagnoses for encephalopathy that were apparent within 6 h of birth. We obtained T -weighted, T -weighted, and diffusion-weighted MRI and thalamic proton MRS 4-14 days after birth. Clinical neurodevelopmental tests were done 18-24 months later. The primary outcome was the association between MR biomarkers and an adverse neurodevelopmental outcome, defined as death or moderate or severe disability, measured using a multivariable prognostic model. We used receiver operating characteristic (ROC) curves to examine the prognostic accuracy of the individual biomarkers. This trial is registered with ClinicalTrials.gov, number NCT01309711. Between Jan 29, 2013, and June 25, 2016, we recruited 223 infants who all underwent MRI and MRS at a median age of 7 days (IQR 5-10), with 190 (85%) followed up for neurological examination at a median age of 23 months (20-25). Of those followed up, 31 (16%) had moderate or severe disability, including one death. Multiple logistic regression analysis could not be done because thalamic N-acetylaspartate (NAA) concentration alone accurately predicted an adverse neurodevelopmental outcome (area under the curve [AUC] of 0·99 [95% CI 0·94-1·00]; sensitivity 100% [74-100]; specificity 97% [90-100]; n=82); the models would not converge when any additional variable was examined. The AUC (95% CI) of clinical examination at 6 h (n=190) and at discharge (n=167) were 0·72 (0·65-0·78) and 0·60 (0·53-0·68), respectively, and the AUC of abnormal amplitude integrated EEG at 6 h (n=169) was 0·73 (0·65-0·79). On conventional MRI (n=190), cortical injury had an AUC of 0·67 (0·60-0·73), basal ganglia or thalamic injury had an AUC of 0·81 (0·75-0·87), and abnormal signal in the posterior limb of internal capsule (PLIC) had an AUC of 0·82 (0·76-0·87). Fractional anisotropy of PLIC (n=65) had an AUC of 0·82 (0·76-0·87). MRS metabolite peak-area ratios (n=160) of NAA-creatine (<1·29) had an AUC of 0·79 (0·72-0·85), of NAA-choline had an AUC of 0·74 (0·66-0·80), and of lactate-NAA (>0·22) had an AUC of 0·94 (0·89-0·97). Thalamic proton MRS measures acquired soon after birth in neonatal encephalopathy had the highest accuracy to predict neurdevelopment 2 years later. These methods could be applied to increase the power of neuroprotection trials while reducing their duration. National Institute for Health Research UK. In neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention, complicating early prognostication and rendering trials of promising neuroprotectants slow and expensive. We aimed to determine the accuracy of thalamic proton magnetic resonance (MR) spectroscopy (MRS) biomarkers as early predictors of the neurodevelopmental abnormalities observed years after neonatal encephalopathy. We did a prospective multicentre cohort study across eight neonatal intensive care units in the UK and USA, recruiting term and near-term neonates who received therapeutic hypothermia for neonatal encephalopathy. We excluded infants with life-threatening congenital malformations, syndromic disorders, neurometabolic diseases, or any alternative diagnoses for encephalopathy that were apparent within 6 h of birth. We obtained T1-weighted, T2-weighted, and diffusion-weighted MRI and thalamic proton MRS 4–14 days after birth. Clinical neurodevelopmental tests were done 18–24 months later. The primary outcome was the association between MR biomarkers and an adverse neurodevelopmental outcome, defined as death or moderate or severe disability, measured using a multivariable prognostic model. We used receiver operating characteristic (ROC) curves to examine the prognostic accuracy of the individual biomarkers. This trial is registered with ClinicalTrials.gov, number NCT01309711. Between Jan 29, 2013, and June 25, 2016, we recruited 223 infants who all underwent MRI and MRS at a median age of 7 days (IQR 5–10), with 190 (85%) followed up for neurological examination at a median age of 23 months (20–25). Of those followed up, 31 (16%) had moderate or severe disability, including one death. Multiple logistic regression analysis could not be done because thalamic N-acetylaspartate (NAA) concentration alone accurately predicted an adverse neurodevelopmental outcome (area under the curve [AUC] of 0·99 [95% CI 0·94–1·00]; sensitivity 100% [74–100]; specificity 97% [90–100]; n=82); the models would not converge when any additional variable was examined. The AUC (95% CI) of clinical examination at 6 h (n=190) and at discharge (n=167) were 0·72 (0·65–0·78) and 0·60 (0·53–0·68), respectively, and the AUC of abnormal amplitude integrated EEG at 6 h (n=169) was 0·73 (0·65–0·79). On conventional MRI (n=190), cortical injury had an AUC of 0·67 (0·60–0·73), basal ganglia or thalamic injury had an AUC of 0·81 (0·75–0·87), and abnormal signal in the posterior limb of internal capsule (PLIC) had an AUC of 0·82 (0·76–0·87). Fractional anisotropy of PLIC (n=65) had an AUC of 0·82 (0·76–0·87). MRS metabolite peak-area ratios (n=160) of NAA–creatine (<1·29) had an AUC of 0·79 (0·72–0·85), of NAA–choline had an AUC of 0·74 (0·66–0·80), and of lactate–NAA (>0·22) had an AUC of 0·94 (0·89–0·97). Thalamic proton MRS measures acquired soon after birth in neonatal encephalopathy had the highest accuracy to predict neurdevelopment 2 years later. These methods could be applied to increase the power of neuroprotection trials while reducing their duration. National Institute for Health Research UK. Summary Background In neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention, complicating early prognostication and rendering trials of promising neuroprotectants slow and expensive. We aimed to determine the accuracy of thalamic proton magnetic resonance (MR) spectroscopy (MRS) biomarkers as early predictors of the neurodevelopmental abnormalities observed years after neonatal encephalopathy. Methods We did a prospective multicentre cohort study across eight neonatal intensive care units in the UK and USA, recruiting term and near-term neonates who received therapeutic hypothermia for neonatal encephalopathy. We excluded infants with life-threatening congenital malformations, syndromic disorders, neurometabolic diseases, or any alternative diagnoses for encephalopathy that were apparent within 6 h of birth. We obtained T1-weighted, T2-weighted, and diffusion-weighted MRI and thalamic proton MRS 4–14 days after birth. Clinical neurodevelopmental tests were done 18–24 months later. The primary outcome was the association between MR biomarkers and an adverse neurodevelopmental outcome, defined as death or moderate or severe disability, measured using a multivariable prognostic model. We used receiver operating characteristic (ROC) curves to examine the prognostic accuracy of the individual biomarkers. This trial is registered with ClinicalTrials.gov, number NCT01309711. Findings Between Jan 29, 2013, and June 25, 2016, we recruited 223 infants who all underwent MRI and MRS at a median age of 7 days (IQR 5–10), with 190 (85%) followed up for neurological examination at a median age of 23 months (20–25). Of those followed up, 31 (16%) had moderate or severe disability, including one death. Multiple logistic regression analysis could not be done because thalamic N-acetylaspartate (NAA) concentration alone accurately predicted an adverse neurodevelopmental outcome (area under the curve [AUC] of 0·99 [95% CI 0·94–1·00]; sensitivity 100% [74–100]; specificity 97% [90–100]; n=82); the models would not converge when any additional variable was examined. The AUC (95% CI) of clinical examination at 6 h (n=190) and at discharge (n=167) were 0·72 (0·65–0·78) and 0·60 (0·53–0·68), respectively, and the AUC of abnormal amplitude integrated EEG at 6 h (n=169) was 0·73 (0·65–0·79). On conventional MRI (n=190), cortical injury had an AUC of 0·67 (0·60–0·73), basal ganglia or thalamic injury had an AUC of 0·81 (0·75–0·87), and abnormal signal in the posterior limb of internal capsule (PLIC) had an AUC of 0·82 (0·76–0·87). Fractional anisotropy of PLIC (n=65) had an AUC of 0·82 (0·76–0·87). MRS metabolite peak-area ratios (n=160) of NAA–creatine (<1·29) had an AUC of 0·79 (0·72–0·85), of NAA–choline had an AUC of 0·74 (0·66–0·80), and of lactate–NAA (>0·22) had an AUC of 0·94 (0·89–0·97). Interpretation Thalamic proton MRS measures acquired soon after birth in neonatal encephalopathy had the highest accuracy to predict neurdevelopment 2 years later. These methods could be applied to increase the power of neuroprotection trials while reducing their duration. Funding National Institute for Health Research UK.
Author	Mitchell, Martin Abernethy, Laurence J Bassett, Paul Clarke, Paul Mendoza, Josephine Pattnayak, Santosh Satodia, Prakash Harigopal, Sundeep Harigopal, Sundeeep Muthukumar, Priya Swamy, Ravi Huertas, Angela Sashikumar, Palaniappan Yajamanyam, Kiran Harizaj, Helen Kalra, Vaneet Kariholu, Ujwal Bainbridge, Alan Thayyil, Sudhin Ganesh, Vijayakumar Dixon, Jennifer Atreja, Gaurav Chawla, Sanjay Sharp, David J Shankaran, Seetha Oliveira, Vânia Wayte, Sarah Soe, Aung Price, David Montaldo, Paolo Lally, Peter J English, Philip
AuthorAffiliation	e Neonatal Unit, Royal Victoria Infirmary, Newcastle, UK a Centre for Perinatal Neuroscience, Imperial College London, London, UK f Neonatal Unit, Norfolk and Norwich University Hospitals NHS Foundation Trust, Norwich, UK k Neonatal-Perinatal Medicine, Wayne State University, Detroit, MI, USA b Oliver Fisher Neonatal Unit, Medway NHS Foundation Trust, Kent, UK d Neonatal Unit, Imperial College Healthcare NHS Trust, London, UK g Neonatal Unit, University Hospitals Coventry and Warwickshire NHS Trust, Coventry, UK j Computational, Cognitive and Clinical Neuroimaging Laboratory, Imperial College London, London, UK h Neonatal Unit, Liverpool Women's NHS Foundation Trust, Liverpool, UK i Neonatal Unit, University College London Hospitals NHS Foundation Trust, London, UK c Statsconsultancy, Amersham, UK
AuthorAffiliation_xml	– name: j Computational, Cognitive and Clinical Neuroimaging Laboratory, Imperial College London, London, UK – name: a Centre for Perinatal Neuroscience, Imperial College London, London, UK – name: g Neonatal Unit, University Hospitals Coventry and Warwickshire NHS Trust, Coventry, UK – name: b Oliver Fisher Neonatal Unit, Medway NHS Foundation Trust, Kent, UK – name: h Neonatal Unit, Liverpool Women's NHS Foundation Trust, Liverpool, UK – name: c Statsconsultancy, Amersham, UK – name: d Neonatal Unit, Imperial College Healthcare NHS Trust, London, UK – name: i Neonatal Unit, University College London Hospitals NHS Foundation Trust, London, UK – name: k Neonatal-Perinatal Medicine, Wayne State University, Detroit, MI, USA – name: f Neonatal Unit, Norfolk and Norwich University Hospitals NHS Foundation Trust, Norwich, UK – name: e Neonatal Unit, Royal Victoria Infirmary, Newcastle, UK
Author_xml	– sequence: 1 givenname: Peter J surname: Lally fullname: Lally, Peter J organization: Centre for Perinatal Neuroscience, Imperial College London, London, UK – sequence: 2 givenname: Paolo surname: Montaldo fullname: Montaldo, Paolo organization: Centre for Perinatal Neuroscience, Imperial College London, London, UK – sequence: 3 givenname: Vânia surname: Oliveira fullname: Oliveira, Vânia organization: Centre for Perinatal Neuroscience, Imperial College London, London, UK – sequence: 4 givenname: Aung surname: Soe fullname: Soe, Aung organization: Oliver Fisher Neonatal Unit, Medway NHS Foundation Trust, Kent, UK – sequence: 5 givenname: Ravi surname: Swamy fullname: Swamy, Ravi organization: Centre for Perinatal Neuroscience, Imperial College London, London, UK – sequence: 6 givenname: Paul surname: Bassett fullname: Bassett, Paul organization: Statsconsultancy, Amersham, UK – sequence: 7 givenname: Josephine surname: Mendoza fullname: Mendoza, Josephine organization: Centre for Perinatal Neuroscience, Imperial College London, London, UK – sequence: 8 givenname: Gaurav surname: Atreja fullname: Atreja, Gaurav organization: Neonatal Unit, Imperial College Healthcare NHS Trust, London, UK – sequence: 9 givenname: Ujwal surname: Kariholu fullname: Kariholu, Ujwal organization: Neonatal Unit, Imperial College Healthcare NHS Trust, London, UK – sequence: 10 givenname: Santosh surname: Pattnayak fullname: Pattnayak, Santosh organization: Oliver Fisher Neonatal Unit, Medway NHS Foundation Trust, Kent, UK – sequence: 11 givenname: Palaniappan surname: Sashikumar fullname: Sashikumar, Palaniappan organization: Oliver Fisher Neonatal Unit, Medway NHS Foundation Trust, Kent, UK – sequence: 12 givenname: Helen surname: Harizaj fullname: Harizaj, Helen organization: Oliver Fisher Neonatal Unit, Medway NHS Foundation Trust, Kent, UK – sequence: 13 givenname: Martin surname: Mitchell fullname: Mitchell, Martin organization: Oliver Fisher Neonatal Unit, Medway NHS Foundation Trust, Kent, UK – sequence: 14 givenname: Vijayakumar surname: Ganesh fullname: Ganesh, Vijayakumar organization: Oliver Fisher Neonatal Unit, Medway NHS Foundation Trust, Kent, UK – sequence: 15 givenname: Sundeep surname: Harigopal fullname: Harigopal, Sundeep organization: Neonatal Unit, Royal Victoria Infirmary, Newcastle, UK – sequence: 16 givenname: Jennifer surname: Dixon fullname: Dixon, Jennifer organization: Neonatal Unit, Royal Victoria Infirmary, Newcastle, UK – sequence: 17 givenname: Philip surname: English fullname: English, Philip organization: Neonatal Unit, Royal Victoria Infirmary, Newcastle, UK – sequence: 18 givenname: Paul surname: Clarke fullname: Clarke, Paul organization: Neonatal Unit, Norfolk and Norwich University Hospitals NHS Foundation Trust, Norwich, UK – sequence: 19 givenname: Priya surname: Muthukumar fullname: Muthukumar, Priya organization: Neonatal Unit, Norfolk and Norwich University Hospitals NHS Foundation Trust, Norwich, UK – sequence: 20 givenname: Prakash surname: Satodia fullname: Satodia, Prakash organization: Neonatal Unit, University Hospitals Coventry and Warwickshire NHS Trust, Coventry, UK – sequence: 21 givenname: Sarah surname: Wayte fullname: Wayte, Sarah organization: Neonatal Unit, University Hospitals Coventry and Warwickshire NHS Trust, Coventry, UK – sequence: 22 givenname: Laurence J surname: Abernethy fullname: Abernethy, Laurence J organization: Neonatal Unit, Liverpool Women's NHS Foundation Trust, Liverpool, UK – sequence: 23 givenname: Kiran surname: Yajamanyam fullname: Yajamanyam, Kiran organization: Neonatal Unit, Liverpool Women's NHS Foundation Trust, Liverpool, UK – sequence: 24 givenname: Alan surname: Bainbridge fullname: Bainbridge, Alan organization: Neonatal Unit, University College London Hospitals NHS Foundation Trust, London, UK – sequence: 25 givenname: David surname: Price fullname: Price, David organization: Neonatal Unit, University College London Hospitals NHS Foundation Trust, London, UK – sequence: 26 givenname: Angela surname: Huertas fullname: Huertas, Angela organization: Neonatal Unit, University College London Hospitals NHS Foundation Trust, London, UK – sequence: 27 givenname: David J surname: Sharp fullname: Sharp, David J organization: Computational, Cognitive and Clinical Neuroimaging Laboratory, Imperial College London, London, UK – sequence: 28 givenname: Vaneet surname: Kalra fullname: Kalra, Vaneet organization: Neonatal-Perinatal Medicine, Wayne State University, Detroit, MI, USA – sequence: 29 givenname: Sanjay surname: Chawla fullname: Chawla, Sanjay organization: Neonatal-Perinatal Medicine, Wayne State University, Detroit, MI, USA – sequence: 30 givenname: Seetha surname: Shankaran fullname: Shankaran, Seetha organization: Neonatal-Perinatal Medicine, Wayne State University, Detroit, MI, USA – sequence: 31 givenname: Sudhin surname: Thayyil fullname: Thayyil, Sudhin email: s.thayyil@imperial.ac.uk organization: Centre for Perinatal Neuroscience, Imperial College London, London, UK – sequence: 32 givenname: Peter J surname: Lally fullname: Lally, Peter J – sequence: 33 givenname: Paolo surname: Montaldo fullname: Montaldo, Paolo – sequence: 34 givenname: Vânia surname: Oliveira fullname: Oliveira, Vânia – sequence: 35 givenname: Aung surname: Soe fullname: Soe, Aung – sequence: 36 givenname: Ravi surname: Swamy fullname: Swamy, Ravi – sequence: 37 givenname: Paul surname: Bassett fullname: Bassett, Paul – sequence: 38 givenname: Josephine surname: Mendoza fullname: Mendoza, Josephine – sequence: 39 givenname: Gaurav surname: Atreja fullname: Atreja, Gaurav – sequence: 40 givenname: Ujwal surname: Kariholu fullname: Kariholu, Ujwal – sequence: 41 givenname: Santosh surname: Pattnayak fullname: Pattnayak, Santosh – sequence: 42 givenname: Palaniappan surname: Sashikumar fullname: Sashikumar, Palaniappan – sequence: 43 givenname: Helen surname: Harizaj fullname: Harizaj, Helen – sequence: 44 givenname: Martin surname: Mitchell fullname: Mitchell, Martin – sequence: 45 givenname: Vijayakumar surname: Ganesh fullname: Ganesh, Vijayakumar – sequence: 46 givenname: Sundeeep surname: Harigopal fullname: Harigopal, Sundeeep – sequence: 47 givenname: Jennifer surname: Dixon fullname: Dixon, Jennifer – sequence: 48 givenname: Philip surname: English fullname: English, Philip – sequence: 49 givenname: Paul surname: Clarke fullname: Clarke, Paul – sequence: 50 givenname: Priya surname: Muthukumar fullname: Muthukumar, Priya – sequence: 51 givenname: Prakash surname: Satodia fullname: Satodia, Prakash – sequence: 52 givenname: Sarah surname: Wayte fullname: Wayte, Sarah – sequence: 53 givenname: Laurence J surname: Abernethy fullname: Abernethy, Laurence J – sequence: 54 givenname: Kiran surname: Yajamanyam fullname: Yajamanyam, Kiran – sequence: 55 givenname: Alan surname: Bainbridge fullname: Bainbridge, Alan – sequence: 56 givenname: David surname: Price fullname: Price, David – sequence: 57 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Snippet	In neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention, complicating early... Summary Background In neonatal encephalopathy, the clinical manifestations of injury can only be reliably assessed several years after an intervention,...
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SubjectTerms	Accuracy Anisotropy Aspartic Acid - analogs & derivatives Aspartic Acid - metabolism Basal ganglia Biomarkers Brain - diagnostic imaging Brain - metabolism Brain injury Brain research Choline Clinical trials Cohort analysis Congenital defects Cortex Creatine EEG Encephalopathy Female Humans Hypothermia Hypothermia, Induced Hypoxia-Ischemia, Brain - diagnostic imaging Hypoxia-Ischemia, Brain - metabolism Hypoxia-Ischemia, Brain - therapy Infant Infant, Newborn Infants Intensive care units Lactic acid Magnetic resonance imaging Magnetic Resonance Spectroscopy Male N-Acetylaspartate Neonates Neurodevelopmental disorders Neuroprotection Newborn babies NMR Nuclear magnetic resonance Prospective Studies Protons Scanners Software Spectrum analysis Thalamus Traumatic brain injury Treatment Outcome
Title	Magnetic resonance spectroscopy assessment of brain injury after moderate hypothermia in neonatal encephalopathy: a prospective multicentre cohort study
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