Development of a composite diffusion tensor imaging score correlating with short-term neurological status in neonatal hypoxic–ischemic encephalopathy
Hypoxic–ischemic encephalopathy (HIE) is the most common cause of neonatal acquired brain injury. Although conventional MRI may predict neurodevelopmental outcomes, accurate prognostication remains difficult. As diffusion tensor imaging (DTI) may provide an additional diagnostic and prognostic value...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2022.931360/full |
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| author | Kengo Onda Eva Catenaccio Jill Chotiyanonta Raul Chavez-Valdez Raul Chavez-Valdez Avner Meoded Bruno P. Soares Aylin Tekes Aylin Tekes Harisa Spahic Sarah C. Miller Sarah-Jane Parker Charlamaine Parkinson Charlamaine Parkinson Dhananjay M. Vaidya Ernest M. Graham Carl E. Stafstrom Carl E. Stafstrom Allen D. Everett Frances J. Northington Frances J. Northington Kenichi Oishi |
| author_facet | Kengo Onda Eva Catenaccio Jill Chotiyanonta Raul Chavez-Valdez Raul Chavez-Valdez Avner Meoded Bruno P. Soares Aylin Tekes Aylin Tekes Harisa Spahic Sarah C. Miller Sarah-Jane Parker Charlamaine Parkinson Charlamaine Parkinson Dhananjay M. Vaidya Ernest M. Graham Carl E. Stafstrom Carl E. Stafstrom Allen D. Everett Frances J. Northington Frances J. Northington Kenichi Oishi |
| author_sort | Kengo Onda |
| collection | DOAJ |
| description | Hypoxic–ischemic encephalopathy (HIE) is the most common cause of neonatal acquired brain injury. Although conventional MRI may predict neurodevelopmental outcomes, accurate prognostication remains difficult. As diffusion tensor imaging (DTI) may provide an additional diagnostic and prognostic value over conventional MRI, we aimed to develop a composite DTI (cDTI) score to relate to short-term neurological function. Sixty prospective neonates treated with therapeutic hypothermia (TH) for HIE were evaluated with DTI, with a voxel size of 1 × 1 × 2 mm. Fractional anisotropy (FA) and mean diffusivity (MD) from 100 neuroanatomical regions (FA/MD *100 = 200 DTI parameters in total) were quantified using an atlas-based image parcellation technique. A least absolute shrinkage and selection operator (LASSO) regression was applied to the DTI parameters to generate the cDTI score. Time to full oral nutrition [short-term oral feeding (STO) score] was used as a measure of short-term neurological function and was correlated with extracted DTI features. Seventeen DTI parameters were selected with LASSO and built into the final unbiased regression model. The selected factors included FA or MD values of the limbic structures, the corticospinal tract, and the frontotemporal cortices. While the cDTI score strongly correlated with the STO score (rho = 0.83, p = 2.8 × 10−16), it only weakly correlated with the Sarnat score (rho = 0.27, p = 0.035) and moderately with the NICHD-NRN neuroimaging score (rho = 0.43, p = 6.6 × 10−04). In contrast to the cDTI score, the NICHD-NRN score only moderately correlated with the STO score (rho = 0.37, p = 0.0037). Using a mixed-model analysis, interleukin-10 at admission to the NICU (p = 1.5 × 10−13) and tau protein at the end of TH/rewarming (p = 0.036) and after rewarming (p = 0.0015) were significantly associated with higher cDTI scores, suggesting that high cDTI scores were related to the intensity of the early inflammatory response and the severity of neuronal impairment after TH. In conclusion, a data-driven unbiased approach was applied to identify anatomical structures associated with some aspects of neurological function of HIE neonates after cooling and to build a cDTI score, which was correlated with the severity of short-term neurological functions. |
| first_indexed | 2024-04-14T03:39:51Z |
| format | Article |
| id | doaj.art-bfc3571b19134a858756427593fb1b46 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-14T03:39:51Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Neuroscience |
| spelling | doaj.art-bfc3571b19134a858756427593fb1b462022-12-22T02:14:34ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2022-08-011610.3389/fnins.2022.931360931360Development of a composite diffusion tensor imaging score correlating with short-term neurological status in neonatal hypoxic–ischemic encephalopathyKengo Onda0Eva Catenaccio1Jill Chotiyanonta2Raul Chavez-Valdez3Raul Chavez-Valdez4Avner Meoded5Bruno P. Soares6Aylin Tekes7Aylin Tekes8Harisa Spahic9Sarah C. Miller10Sarah-Jane Parker11Charlamaine Parkinson12Charlamaine Parkinson13Dhananjay M. Vaidya14Ernest M. Graham15Carl E. Stafstrom16Carl E. Stafstrom17Allen D. Everett18Frances J. Northington19Frances J. Northington20Kenichi Oishi21The Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesDivision of Pediatric Neurology, Department of Pediatrics, Children's Hospital of Philadelphia, Philadelphia, PA, United StatesThe Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesNeuroscience Intensive Care Nursery Program, Division of Neonatology, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesDivision of Neonatology, Department of Pediatrics, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesEdward B. Singleton Department of Radiology, Texas Children's Hospital, Baylor College of Medicine, Houston, TX, United StatesDivision of Neuroradiology, Department of Radiology, Larner College of Medicine at the University of Vermont, Burlington, VT, United StatesNeuroscience Intensive Care Nursery Program, Division of Neonatology, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesDivision of Pediatric Radiology and Pediatric Neuroradiology, Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesDivision of Neonatology, Department of Pediatrics, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesDivision of Neonatology, Department of Pediatrics, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesSt. George's University of London, London, United KingdomNeuroscience Intensive Care Nursery Program, Division of Neonatology, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesDivision of Neonatology, Department of Pediatrics, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesDepartment of General Internal Medicine, The Johns Hopkins University School of Medicine, Baltimore, MD, United States0Division of Maternal-Fetal Medicine, Department of Gynecology and Obstetrics, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesNeuroscience Intensive Care Nursery Program, Division of Neonatology, The Johns Hopkins University School of Medicine, Baltimore, MD, United States1Division of Pediatric Neurology, Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD, United States2Division of Pediatric Cardiology, Department of Pediatrics, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesNeuroscience Intensive Care Nursery Program, Division of Neonatology, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesDivision of Neonatology, Department of Pediatrics, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesThe Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, Baltimore, MD, United StatesHypoxic–ischemic encephalopathy (HIE) is the most common cause of neonatal acquired brain injury. Although conventional MRI may predict neurodevelopmental outcomes, accurate prognostication remains difficult. As diffusion tensor imaging (DTI) may provide an additional diagnostic and prognostic value over conventional MRI, we aimed to develop a composite DTI (cDTI) score to relate to short-term neurological function. Sixty prospective neonates treated with therapeutic hypothermia (TH) for HIE were evaluated with DTI, with a voxel size of 1 × 1 × 2 mm. Fractional anisotropy (FA) and mean diffusivity (MD) from 100 neuroanatomical regions (FA/MD *100 = 200 DTI parameters in total) were quantified using an atlas-based image parcellation technique. A least absolute shrinkage and selection operator (LASSO) regression was applied to the DTI parameters to generate the cDTI score. Time to full oral nutrition [short-term oral feeding (STO) score] was used as a measure of short-term neurological function and was correlated with extracted DTI features. Seventeen DTI parameters were selected with LASSO and built into the final unbiased regression model. The selected factors included FA or MD values of the limbic structures, the corticospinal tract, and the frontotemporal cortices. While the cDTI score strongly correlated with the STO score (rho = 0.83, p = 2.8 × 10−16), it only weakly correlated with the Sarnat score (rho = 0.27, p = 0.035) and moderately with the NICHD-NRN neuroimaging score (rho = 0.43, p = 6.6 × 10−04). In contrast to the cDTI score, the NICHD-NRN score only moderately correlated with the STO score (rho = 0.37, p = 0.0037). Using a mixed-model analysis, interleukin-10 at admission to the NICU (p = 1.5 × 10−13) and tau protein at the end of TH/rewarming (p = 0.036) and after rewarming (p = 0.0015) were significantly associated with higher cDTI scores, suggesting that high cDTI scores were related to the intensity of the early inflammatory response and the severity of neuronal impairment after TH. In conclusion, a data-driven unbiased approach was applied to identify anatomical structures associated with some aspects of neurological function of HIE neonates after cooling and to build a cDTI score, which was correlated with the severity of short-term neurological functions.https://www.frontiersin.org/articles/10.3389/fnins.2022.931360/fullhypoxic-ischemic encephalopathyoutcome predictiondiffusion tensor imagingneonatal brain atlasleast absolute shrinkage and selection operatorshort-term neurologic outcome |
| spellingShingle | Kengo Onda Eva Catenaccio Jill Chotiyanonta Raul Chavez-Valdez Raul Chavez-Valdez Avner Meoded Bruno P. Soares Aylin Tekes Aylin Tekes Harisa Spahic Sarah C. Miller Sarah-Jane Parker Charlamaine Parkinson Charlamaine Parkinson Dhananjay M. Vaidya Ernest M. Graham Carl E. Stafstrom Carl E. Stafstrom Allen D. Everett Frances J. Northington Frances J. Northington Kenichi Oishi Development of a composite diffusion tensor imaging score correlating with short-term neurological status in neonatal hypoxic–ischemic encephalopathy Frontiers in Neuroscience hypoxic-ischemic encephalopathy outcome prediction diffusion tensor imaging neonatal brain atlas least absolute shrinkage and selection operator short-term neurologic outcome |
| title | Development of a composite diffusion tensor imaging score correlating with short-term neurological status in neonatal hypoxic–ischemic encephalopathy |
| title_full | Development of a composite diffusion tensor imaging score correlating with short-term neurological status in neonatal hypoxic–ischemic encephalopathy |
| title_fullStr | Development of a composite diffusion tensor imaging score correlating with short-term neurological status in neonatal hypoxic–ischemic encephalopathy |
| title_full_unstemmed | Development of a composite diffusion tensor imaging score correlating with short-term neurological status in neonatal hypoxic–ischemic encephalopathy |
| title_short | Development of a composite diffusion tensor imaging score correlating with short-term neurological status in neonatal hypoxic–ischemic encephalopathy |
| title_sort | development of a composite diffusion tensor imaging score correlating with short term neurological status in neonatal hypoxic ischemic encephalopathy |
| topic | hypoxic-ischemic encephalopathy outcome prediction diffusion tensor imaging neonatal brain atlas least absolute shrinkage and selection operator short-term neurologic outcome |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2022.931360/full |
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