TY - JOUR
T1 - Assessment of longitudinal brain development using super-resolution magnetic resonance imaging following fetal surgery for open spina bifida
AU - GIFT-Surg Imaging Working Group
AU - Mufti, N.
AU - Chappell, J.
AU - Aertsen, M.
AU - Ebner, M.
AU - Fidon, L.
AU - Deprest, J.
AU - David, A. L.
AU - Melbourne, A.
AU - Atkinson, David
AU - Bredaki, Foteini Emmanouella
AU - De Catte, Luc
AU - De Vloo, Phillippe
AU - Demaerel, Philippe
AU - Devlieger, Roland
AU - Gaunt, Trevor
AU - Kendall, Giles S.
AU - Ourselin, Sebastien
AU - Baruteau, Kelly Pegoretti
AU - Sacco, Adalina
AU - Sokolska, Magdalena
AU - Thompson, Dominic
AU - Vercauteren, Tom
N1 - Funding Information:
This work was supported by the Guided Instrumentation of Fetal Therapy and Surgery (GIFT‐Surg) project, funded by the Wellcome Trust (203148/Z/16/Z; 203145Z/16/Z; WT101957) and Engineering and Physical Sciences Research Council (EPSRC) (NS/A000049/1; NS/A000050/1; NS/A000027/1; EP/L016478/1). This grant included external peer review for scientific quality with a patient and public involvement panel. S.O. is the principal investigator on this grant and A.L.D., J.D., T.V. and A.M. are coinvestigators. L.F. is funded by the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska‐Curie grant agreement (TRABIT, No. 765148). N.M. is funded with support of the Wellcome/EPSRC centre for Interventional and Surgical Sciences (WEISS) (203145Z/16/Z). A.L.D. is supported by the National Institute for Health Research University College London Hospitals Biomedical Research Centre. The funders had no direction in the study design, data collection, data analysis, manuscript preparation or decision to submit for publication.
Funding Information:
This work was supported by the Guided Instrumentation of Fetal Therapy and Surgery (GIFT-Surg) project, funded by the Wellcome Trust (203148/Z/16/Z; 203145Z/16/Z; WT101957) and Engineering and Physical Sciences Research Council (EPSRC) (NS/A000049/1; NS/A000050/1; NS/A000027/1; EP/L016478/1). This grant included external peer review for scientific quality with a patient and public involvement panel. S.O. is the principal investigator on this grant and A.L.D., J.D., T.V. and A.M. are coinvestigators. L.F. is funded by the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement (TRABIT, No. 765148). N.M. is funded with support of the Wellcome/EPSRC centre for Interventional and Surgical Sciences (WEISS) (203145Z/16/Z). A.L.D. is supported by the National Institute for Health Research University College London Hospitals Biomedical Research Centre. The funders had no direction in the study design, data collection, data analysis, manuscript preparation or decision to submit for publication.
Publisher Copyright:
© 2023 The Authors. Ultrasound in Obstetrics & Gynecology published by John Wiley & Sons Ltd on behalf of International Society of Ultrasound in Obstetrics and Gynecology.
PY - 2023/11
Y1 - 2023/11
N2 - Objectives: 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. Methods: 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). Results: 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
3/week vs 708.21 (IQR, 474.50–925.00) mm
3/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
–1/week vs 0.094 (IQR, 0.070–0.146) mm
–1/week; P < 0.001), reversing the trend seen at 1 week after surgery (0.144 (IQR, 0.099–0.236) mm
–1/week vs 0.072 (IQR, 0.059–0.081) mm
–1/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). Conclusions: 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.
AB - Objectives: 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. Methods: 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). Results: 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
3/week vs 708.21 (IQR, 474.50–925.00) mm
3/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
–1/week vs 0.094 (IQR, 0.070–0.146) mm
–1/week; P < 0.001), reversing the trend seen at 1 week after surgery (0.144 (IQR, 0.099–0.236) mm
–1/week vs 0.072 (IQR, 0.059–0.081) mm
–1/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). Conclusions: 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.
KW - curvedness
KW - fetal surgery
KW - gyrification
KW - magnetic resonance imaging
KW - MRI
KW - open spina bifida
KW - super-resolution reconstruction
KW - surface area
KW - volume
UR - http://www.scopus.com/inward/record.url?scp=85175842709&partnerID=8YFLogxK
U2 - 10.1002/uog.26244
DO - 10.1002/uog.26244
M3 - Article
C2 - 37161647
SN - 0960-7692
VL - 62
SP - 707
EP - 720
JO - Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology
JF - Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology
IS - 5
ER -