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. 2021 Oct;63(10):1721-1734.
doi: 10.1007/s00234-021-02725-8. Epub 2021 May 1.

Cortical spectral matching and shape and volume analysis of the fetal brain pre- and post-fetal surgery for spina bifida: a retrospective study

Nada Mufti  1   2 , Michael Aertsen  3 , Michael Ebner  4   5 , Lucas Fidon  4 , Premal Patel  6 , Muhamad Bin Abdul Rahman  4 , Yannick Brackenier  4 , Gregor Ekart  4 , Virginia Fernandez  4 , Tom Vercauteren  4   5 , Sebastien Ourselin  4   5 , Dominic Thomson  7 , Luc De Catte  8   9 , Philippe Demaerel  3 , Jan Deprest  10   8   9 , Anna L David  10   8   9 , Andrew Melbourne  4   5
Affiliations

Cortical spectral matching and shape and volume analysis of the fetal brain pre- and post-fetal surgery for spina bifida: a retrospective study

Nada Mufti et al. Neuroradiology. 2021 Oct.

Abstract

Purpose: A retrospective study was performed to study the effect of fetal surgery on brain development measured by MRI in fetuses with myelomeningocele (MMC).

Methods: MRI scans of 12 MMC fetuses before and after surgery were compared to 24 age-matched controls without central nervous system abnormalities. An automated super-resolution reconstruction technique generated isotropic brain volumes to mitigate 2D MRI fetal motion artefact. Unmyelinated white matter, cerebellum and ventricles were automatically segmented, and cerebral volume, shape and cortical folding were thereafter quantified. Biometric measures were calculated for cerebellar herniation level (CHL), clivus-supraocciput angle (CSO), transverse cerebellar diameter (TCD) and ventricular width (VW). Shape index (SI), a mathematical marker of gyrification, was derived. We compared cerebral volume, surface area and SI before and after MMC fetal surgery versus controls. We additionally identified any relationship between these outcomes and biometric measurements.

Results: MMC ventricular volume/week (mm3/week) increased after fetal surgery (median: 3699, interquartile range (IQR): 1651-5395) compared to controls (median: 648, IQR: 371-896); P = 0.015. The MMC SI is higher pre-operatively in all cerebral lobes in comparison to that in controls. Change in SI/week in MMC fetuses was higher in the left temporal lobe (median: 0.039, IQR: 0.021-0.054), left parietal lobe (median: 0.032, IQR: 0.023-0.039) and right occipital lobe (median: 0.027, IQR: 0.019-0.040) versus controls (P = 0.002 to 0.005). Ventricular volume (mm3) and VW (mm) (r = 0.64), cerebellar volume and TCD (r = 0.56) were moderately correlated.

Conclusions: Following fetal myelomeningocele repair, brain volume, shape and SI were significantly different from normal in most cerebral layers. Morphological brain changes after fetal surgery are not limited to hindbrain herniation reversal. These findings may have neurocognitive outcome implications and require further evaluation.

Keywords: Cortical spectral matching; Fetal surgery; MRI; Myelomeningocele; Shape; Volume.

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Conflict of interest statement

The authors have no relevant financial or non-financial interests to disclose.

Figures

Fig. 1
Fig. 1
An example of the original super-resolution reconstruction (SRR) data displayed pre-operatively (top row) and post-operatively (bottom row) in the axial, coronal and sagittal planes (right to left)
Fig. 2
Fig. 2
The first five spectral modes of the unmyelinated white matter of a fetus for two different time points: before surgery (top row) and after surgery (bottom row)
Fig. 3
Fig. 3
Map display (with accompanying colour scale (right)) of curvedness and shape index for the unmyelinated white matter of a fetus pre-surgery and post-surgery. a This map shows the apparent locations of development of several primary (black arrow) and secondary sulci (black box). b Post-surgery shape index mapped to the pre-surgery mesh. c Post-surgery mesh. d Difference in shape index and curvedness (B-A)
Fig. 4
Fig. 4
a Volume (mm3) of MMC ventricles pre-surgery and post-surgery, and age-matched controls against gestational age in weeks. b Volume (mm3) of MMC ventricles pre-surgery and post-surgery compared to early and late controls. The p values compare differences in measurements between pre-MMC surgery and post-MMC surgery, and early and late controls to controls. c Absolute difference in change in volume (mm3) of ventricles after surgery for MMC compared to controls. d Rate of change in volume/time (mm3/week) of ventricles after surgery for MMC against age-matched controls
Fig. 5
Fig. 5
a Shape parameter (mm−1) of MMC ventricles pre-surgery and post-surgery, and age-matched controls against gestational age in weeks. b Shape parameter (mm−1) of MMC ventricles pre-surgery and post-surgery compared to early and late controls. The p values compare differences in measurements between pre-MMC surgery and post-MMC surgery, and early and late controls to controls. c Absolute difference in change in shape parameter (mm−1) of ventricles after surgery for MMC compared to controls. d Rate of change in shape parameter/time (mm−1/week) of ventricles after surgery for MMC against age-matched controls
Fig. 6
Fig. 6
a Shape index of MMC left temporal lobe pre-surgery and post-surgery compared to early and late controls. The p values compare differences in measurements between pre-MMC surgery and post-MMC surgery, and early and late controls to controls. b Rate of change in shape index/time (week−1) of the left temporal lobe after surgery for MMC against age-matched controls. c Shape index of MMC right temporal lobe pre-surgery and post-surgery compared to early and late controls. The p values compare differences in measurements between pre-MMC surgery and post-MMC surgery, and early and late controls to controls. d Rate of change in shape index/time (week−1) of right temporal lobe after surgery for MMC against age-matched controls
Fig. 7
Fig. 7
a Shape index of MMC left parietal lobe pre-surgery and post-surgery compared to early and late controls. The p values compare differences in measurements between pre-MMC surgery and post-MMC surgery, and early and late controls to controls. b Rate of change in shape index/time (week−1) of left parietal lobe after surgery for MMC against age-matched controls. c Shape index of MMC right parietal lobe pre-surgery and post-surgery compared to early and late controls. The p values compare differences in measurements between pre-MMC surgery and post-MMC surgery, and early and late controls to controls. d Rate of change in shape index/time (week−1) of right parietal lobe after surgery for MMC against age-matched controls
Fig. 8
Fig. 8
a Shape index of MMC left occipital lobe pre-surgery and post-surgery compared to early and late controls. The p values compare differences in measurements between pre-MMC surgery and post-MMC surgery, and early and late controls to controls. b Rate of change in shape index/time (week−1) of left occipital lobe after surgery for MMC against age-matched controls. c Shape index of MMC right occipital lobe pre-surgery and post-surgery compared to early and late controls. The p values compare differences in measurements between pre-MMC surgery and post-MMC surgery, and early and late controls to controls. d Rate of change in shape index/time (week−1) of the right occipital lobe after surgery for MMC against age-matched controls
Fig. 9
Fig. 9
Map display of shape index for the left frontal lobe (top row), left occipital lobe (middle row) and right occipital lobe (bottom row) of a fetal mesh. (a) Pre-surgery, (b) post-surgery shape index mapped to the pre-surgery mesh, (c) post-surgery mesh and (d) difference in shape index and curvedness (B-A). For orientation purposes, a 3D brain mesh (right) is provided for the left frontal lobe (red), left occipital lobe (white) and right occipital lobe (dark blue). Asterisks (*) are provided on 3D brain meshes for lobe identification
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