Assessment of longitudinal brain development using super-resolution magnetic resonance imaging following fetal surgery for open spina bifida

Prenatal surgery is offered for selected fetuses with open spina bifida (OSB) to improve long-term outcome. We studied the effect of fetal OSB surgery on brain development using advanced magnetic resonance imaging (MRI) techniques to quantify the volume, surface area and shape of cerebral structures...

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Veröffentlicht in:Ultrasound in obstetrics & gynecology 2023-11, Vol.62 (5), p.707-720
Hauptverfasser: Mufti, N, Chappell, J, Aertsen, M, Ebner, M, Fidon, L, Deprest, J, David, A L, Melbourne, A
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container_title Ultrasound in obstetrics & gynecology
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creator Mufti, N
Chappell, J
Aertsen, M
Ebner, M
Fidon, L
Deprest, J
David, A L
Melbourne, A
description Prenatal surgery is offered for selected fetuses with open spina bifida (OSB) to improve long-term outcome. We studied the effect of fetal OSB surgery on brain development using advanced magnetic resonance imaging (MRI) techniques to quantify the volume, surface area and shape of cerebral structures and to analyze surface curvature by means of parameters that correspond to gyrification. We compared MRI data from 29 fetuses with OSB before fetal surgery (mean gestational age (GA), 23 + 3 weeks) and at 1 and 6 weeks after surgery, with that of 36 GA-matched control fetuses (GA range, 21 + 2 to 36 + 2 weeks). Automated super-resolution reconstruction provided three-dimensional isotropic volumetric brain images. Unmyelinated white matter, cerebellum and ventricles were segmented automatically and refined manually, after which volume, surface area and shape parameter (volume/surface area) were quantified. Mathematical markers (shape index (SI) and curvedness) were used to measure gyrification. Parameters were assessed according to lesion type (myelomeningocele vs myeloschisis (MS)), postoperative persistence of hindbrain herniation (HH) and the presence of supratentorial anomalies, namely partial agenesis of the corpus callosum (pACC) and heterotopia (HT). Growth in ventricular volume per week and change in shape parameter per week were higher at 6 weeks after surgery in fetuses with OSB compared with controls (median, 2500.94 (interquartile range (IQR), 1689.70-3580.80) mm /week vs 708.21 (IQR, 474.50-925.00) mm /week; P 
doi_str_mv 10.1002/uog.26244
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We studied the effect of fetal OSB surgery on brain development using advanced magnetic resonance imaging (MRI) techniques to quantify the volume, surface area and shape of cerebral structures and to analyze surface curvature by means of parameters that correspond to gyrification. We compared MRI data from 29 fetuses with OSB before fetal surgery (mean gestational age (GA), 23 + 3 weeks) and at 1 and 6 weeks after surgery, with that of 36 GA-matched control fetuses (GA range, 21 + 2 to 36 + 2 weeks). Automated super-resolution reconstruction provided three-dimensional isotropic volumetric brain images. Unmyelinated white matter, cerebellum and ventricles were segmented automatically and refined manually, after which volume, surface area and shape parameter (volume/surface area) were quantified. Mathematical markers (shape index (SI) and curvedness) were used to measure gyrification. Parameters were assessed according to lesion type (myelomeningocele vs myeloschisis (MS)), postoperative persistence of hindbrain herniation (HH) and the presence of supratentorial anomalies, namely partial agenesis of the corpus callosum (pACC) and heterotopia (HT). Growth in ventricular volume per week and change in shape parameter per week were higher at 6 weeks after surgery in fetuses with OSB compared with controls (median, 2500.94 (interquartile range (IQR), 1689.70-3580.80) mm /week vs 708.21 (IQR, 474.50-925.00) mm /week; P < 0.001 and 0.075 (IQR, 0.047-0.112) mm/week vs 0.022 (IQR, 0.009-0.042) mm/week; P = 0.046, respectively). Ventricular volume growth increased 6 weeks after surgery in cases with pACC (P < 0.001) and those with persistent HH (P = 0.002). During that time period, the change in unmyelinated white-matter shape parameter per week was decreased in OSB fetuses compared with controls (0.056 (IQR, 0.044-0.092) mm/week vs 0.159 (IQR, 0.100-0.247) mm/week; P = 0.002), particularly in cases with persistent HH (P = 0.011), MS (P = 0.015), HT (P = 0.022), HT with corpus callosum anomaly (P = 0.017) and persistent HH with corpus callosum anomaly (P = 0.007). At 6 weeks postoperatively, despite OSB fetuses having a lower rate of change in curvedness compared with controls (0.061 (IQR, 0.040-0.093) mm /week vs 0.094 (IQR, 0.070-0.146) mm /week; P < 0.001), reversing the trend seen at 1 week after surgery (0.144 (IQR, 0.099-0.236) mm /week vs 0.072 (IQR, 0.059-0.081) mm /week; P < 0.001), gyrification, as determined using SI, appeared to be increased in OSB fetuses overall compared with controls. This observation was more prominent in fetuses with pACC and those with severe ventriculomegaly (P-value range, < 0.001 to 0.006). Following fetal OSB repair, volume, shape and curvedness of ventricles and unmyelinated white matter differed significantly compared with those of normal fetuses. Morphological brain changes after fetal surgery were not limited to effects on the circulation of cerebrospinal fluid. These observations may have implications for postnatal neurocognitive outcome. © 2023 The Authors. Ultrasound in Obstetrics & Gynecology published by John Wiley & Sons Ltd on behalf of International Society of Ultrasound in Obstetrics and Gynecology.]]></description><identifier>ISSN: 0960-7692</identifier><identifier>EISSN: 1469-0705</identifier><identifier>DOI: 10.1002/uog.26244</identifier><identifier>PMID: 37161647</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Anomalies ; Brain ; Brain - diagnostic imaging ; Cerebellum ; Cerebrospinal fluid ; Cognition ; Corpus callosum ; Female ; Fetus ; Fetuses ; Gestational Age ; Gynecology ; Hindbrain ; Humans ; Image reconstruction ; Magnetic resonance imaging ; Magnetic Resonance Imaging - methods ; Medical imaging ; Meningomyelocele - surgery ; Neuroimaging ; Obstetrics ; Original Paper ; Original Papers ; Parameters ; Pregnancy ; Retrospective Studies ; Spina bifida ; Spina Bifida Cystica - diagnostic imaging ; Spina Bifida Cystica - surgery ; Substantia alba ; Surface area ; Surgery ; Ultrasonic imaging ; Ultrasonography, Prenatal ; Ultrasound ; Ventricle</subject><ispartof>Ultrasound in obstetrics &amp; gynecology, 2023-11, Vol.62 (5), p.707-720</ispartof><rights>2023 The Authors. 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We studied the effect of fetal OSB surgery on brain development using advanced magnetic resonance imaging (MRI) techniques to quantify the volume, surface area and shape of cerebral structures and to analyze surface curvature by means of parameters that correspond to gyrification. We compared MRI data from 29 fetuses with OSB before fetal surgery (mean gestational age (GA), 23 + 3 weeks) and at 1 and 6 weeks after surgery, with that of 36 GA-matched control fetuses (GA range, 21 + 2 to 36 + 2 weeks). Automated super-resolution reconstruction provided three-dimensional isotropic volumetric brain images. Unmyelinated white matter, cerebellum and ventricles were segmented automatically and refined manually, after which volume, surface area and shape parameter (volume/surface area) were quantified. Mathematical markers (shape index (SI) and curvedness) were used to measure gyrification. Parameters were assessed according to lesion type (myelomeningocele vs myeloschisis (MS)), postoperative persistence of hindbrain herniation (HH) and the presence of supratentorial anomalies, namely partial agenesis of the corpus callosum (pACC) and heterotopia (HT). Growth in ventricular volume per week and change in shape parameter per week were higher at 6 weeks after surgery in fetuses with OSB compared with controls (median, 2500.94 (interquartile range (IQR), 1689.70-3580.80) mm /week vs 708.21 (IQR, 474.50-925.00) mm /week; P < 0.001 and 0.075 (IQR, 0.047-0.112) mm/week vs 0.022 (IQR, 0.009-0.042) mm/week; P = 0.046, respectively). Ventricular volume growth increased 6 weeks after surgery in cases with pACC (P < 0.001) and those with persistent HH (P = 0.002). During that time period, the change in unmyelinated white-matter shape parameter per week was decreased in OSB fetuses compared with controls (0.056 (IQR, 0.044-0.092) mm/week vs 0.159 (IQR, 0.100-0.247) mm/week; P = 0.002), particularly in cases with persistent HH (P = 0.011), MS (P = 0.015), HT (P = 0.022), HT with corpus callosum anomaly (P = 0.017) and persistent HH with corpus callosum anomaly (P = 0.007). At 6 weeks postoperatively, despite OSB fetuses having a lower rate of change in curvedness compared with controls (0.061 (IQR, 0.040-0.093) mm /week vs 0.094 (IQR, 0.070-0.146) mm /week; P < 0.001), reversing the trend seen at 1 week after surgery (0.144 (IQR, 0.099-0.236) mm /week vs 0.072 (IQR, 0.059-0.081) mm /week; P < 0.001), gyrification, as determined using SI, appeared to be increased in OSB fetuses overall compared with controls. This observation was more prominent in fetuses with pACC and those with severe ventriculomegaly (P-value range, < 0.001 to 0.006). Following fetal OSB repair, volume, shape and curvedness of ventricles and unmyelinated white matter differed significantly compared with those of normal fetuses. Morphological brain changes after fetal surgery were not limited to effects on the circulation of cerebrospinal fluid. These observations may have implications for postnatal neurocognitive outcome. © 2023 The Authors. Ultrasound in Obstetrics & Gynecology published by John Wiley & Sons Ltd on behalf of International Society of Ultrasound in Obstetrics and Gynecology.]]></description><subject>Anomalies</subject><subject>Brain</subject><subject>Brain - diagnostic imaging</subject><subject>Cerebellum</subject><subject>Cerebrospinal fluid</subject><subject>Cognition</subject><subject>Corpus callosum</subject><subject>Female</subject><subject>Fetus</subject><subject>Fetuses</subject><subject>Gestational Age</subject><subject>Gynecology</subject><subject>Hindbrain</subject><subject>Humans</subject><subject>Image reconstruction</subject><subject>Magnetic resonance imaging</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Medical imaging</subject><subject>Meningomyelocele - surgery</subject><subject>Neuroimaging</subject><subject>Obstetrics</subject><subject>Original Paper</subject><subject>Original Papers</subject><subject>Parameters</subject><subject>Pregnancy</subject><subject>Retrospective Studies</subject><subject>Spina bifida</subject><subject>Spina Bifida Cystica - diagnostic imaging</subject><subject>Spina Bifida Cystica - surgery</subject><subject>Substantia alba</subject><subject>Surface area</subject><subject>Surgery</subject><subject>Ultrasonic imaging</subject><subject>Ultrasonography, Prenatal</subject><subject>Ultrasound</subject><subject>Ventricle</subject><issn>0960-7692</issn><issn>1469-0705</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU1vFSEYhYnR2Gt14R8wJG50MZWvgZmVaRq_kiZudE1gYEYaLoy8Q5v-B3-03NvaqCvI4cnhvO9B6CUlZ5QQ9q7m5YxJJsQjtKNCjh1RpH-MdmSUpFNyZCfoGcAVIUQKLp-iE66opFKoHfp1DuAB9j5tOM845rSErbqQTMS2mJCw89c-5vVIVAhpwVBXX7riIce6hZzw3izJb2HCBy2ZNHkcmnZg5xxjvjne_NY8oZbFl9umF5xXnzCs7S9swxyceY6ezCaCf3F_nqLvHz98u_jcXX799OXi_LKbBBFbJ904ToNxtCd26JVlara2Z9z0zBpnZ24GK5USs3OcS-fERLjhlFpHG0YpP0Xv73zXavfeTW20YqJeS0tdbnU2Qf_7ksIPveRrTckoVNt4c3hz71Dyz-ph0_sAk4_RJJ8raDZQOvJhIGNDX_-HXuVa2n4P1CCUYHSQjXp7R00lAxQ_P6ShRB9K1q1kfSy5sa_-jv9A_mmV_wZh0qc-</recordid><startdate>202311</startdate><enddate>202311</enddate><creator>Mufti, N</creator><creator>Chappell, J</creator><creator>Aertsen, M</creator><creator>Ebner, M</creator><creator>Fidon, L</creator><creator>Deprest, J</creator><creator>David, A L</creator><creator>Melbourne, A</creator><general>Wiley Subscription Services, Inc</general><general>John Wiley &amp; 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We studied the effect of fetal OSB surgery on brain development using advanced magnetic resonance imaging (MRI) techniques to quantify the volume, surface area and shape of cerebral structures and to analyze surface curvature by means of parameters that correspond to gyrification. We compared MRI data from 29 fetuses with OSB before fetal surgery (mean gestational age (GA), 23 + 3 weeks) and at 1 and 6 weeks after surgery, with that of 36 GA-matched control fetuses (GA range, 21 + 2 to 36 + 2 weeks). Automated super-resolution reconstruction provided three-dimensional isotropic volumetric brain images. Unmyelinated white matter, cerebellum and ventricles were segmented automatically and refined manually, after which volume, surface area and shape parameter (volume/surface area) were quantified. Mathematical markers (shape index (SI) and curvedness) were used to measure gyrification. Parameters were assessed according to lesion type (myelomeningocele vs myeloschisis (MS)), postoperative persistence of hindbrain herniation (HH) and the presence of supratentorial anomalies, namely partial agenesis of the corpus callosum (pACC) and heterotopia (HT). Growth in ventricular volume per week and change in shape parameter per week were higher at 6 weeks after surgery in fetuses with OSB compared with controls (median, 2500.94 (interquartile range (IQR), 1689.70-3580.80) mm /week vs 708.21 (IQR, 474.50-925.00) mm /week; P < 0.001 and 0.075 (IQR, 0.047-0.112) mm/week vs 0.022 (IQR, 0.009-0.042) mm/week; P = 0.046, respectively). Ventricular volume growth increased 6 weeks after surgery in cases with pACC (P < 0.001) and those with persistent HH (P = 0.002). During that time period, the change in unmyelinated white-matter shape parameter per week was decreased in OSB fetuses compared with controls (0.056 (IQR, 0.044-0.092) mm/week vs 0.159 (IQR, 0.100-0.247) mm/week; P = 0.002), particularly in cases with persistent HH (P = 0.011), MS (P = 0.015), HT (P = 0.022), HT with corpus callosum anomaly (P = 0.017) and persistent HH with corpus callosum anomaly (P = 0.007). At 6 weeks postoperatively, despite OSB fetuses having a lower rate of change in curvedness compared with controls (0.061 (IQR, 0.040-0.093) mm /week vs 0.094 (IQR, 0.070-0.146) mm /week; P < 0.001), reversing the trend seen at 1 week after surgery (0.144 (IQR, 0.099-0.236) mm /week vs 0.072 (IQR, 0.059-0.081) mm /week; P < 0.001), gyrification, as determined using SI, appeared to be increased in OSB fetuses overall compared with controls. This observation was more prominent in fetuses with pACC and those with severe ventriculomegaly (P-value range, < 0.001 to 0.006). Following fetal OSB repair, volume, shape and curvedness of ventricles and unmyelinated white matter differed significantly compared with those of normal fetuses. Morphological brain changes after fetal surgery were not limited to effects on the circulation of cerebrospinal fluid. These observations may have implications for postnatal neurocognitive outcome. © 2023 The Authors. Ultrasound in Obstetrics & Gynecology published by John Wiley & Sons Ltd on behalf of International Society of Ultrasound in Obstetrics and Gynecology.]]></abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>37161647</pmid><doi>10.1002/uog.26244</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-9839-8085</orcidid><orcidid>https://orcid.org/0000-0003-1994-5365</orcidid><orcidid>https://orcid.org/0000-0002-4920-945X</orcidid><oa>free_for_read</oa></addata></record>
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source Wiley Online Library - AutoHoldings Journals; MEDLINE; Wiley Free Archive; EZB Electronic Journals Library
subjects Anomalies
Brain
Brain - diagnostic imaging
Cerebellum
Cerebrospinal fluid
Cognition
Corpus callosum
Female
Fetus
Fetuses
Gestational Age
Gynecology
Hindbrain
Humans
Image reconstruction
Magnetic resonance imaging
Magnetic Resonance Imaging - methods
Medical imaging
Meningomyelocele - surgery
Neuroimaging
Obstetrics
Original Paper
Original Papers
Parameters
Pregnancy
Retrospective Studies
Spina bifida
Spina Bifida Cystica - diagnostic imaging
Spina Bifida Cystica - surgery
Substantia alba
Surface area
Surgery
Ultrasonic imaging
Ultrasonography, Prenatal
Ultrasound
Ventricle
title Assessment of longitudinal brain development using super-resolution magnetic resonance imaging following fetal surgery for open spina bifida
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