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

GIFT-Surg Imaging Working Group, N. Mufti*, J. Chappell, M. Aertsen, M. Ebner, L. Fidon, J. Deprest, A. L. David, A. Melbourne, David Atkinson, Foteini Emmanouella Bredaki, Luc De Catte, Phillippe De Vloo, Philippe Demaerel, Roland Devlieger, Trevor Gaunt, Giles S. Kendall, Sebastien Ourselin, Kelly Pegoretti Baruteau, Adalina SaccoMagdalena Sokolska, Dominic Thompson, Tom Vercauteren

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

1 Citation (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)707-720
Number of pages14
JournalUltrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology
Volume62
Issue number5
Early online date9 May 2023
DOIs
Publication statusPublished - Nov 2023

Keywords

  • curvedness
  • fetal surgery
  • gyrification
  • magnetic resonance imaging
  • MRI
  • open spina bifida
  • super-resolution reconstruction
  • surface area
  • volume

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