A change in brain white matter after shunt surgery in idiopathic normal pressure hydrocephalus: a tract-based spatial statistics study

Abstract

Background: The aim of this study was to elucidate changes in cerebral white matter after shunt surgery in idiopathic normal pressure hydrocephalus (INPH) using diffusion tensor imaging (DTI).

Methods: Twenty-eight consecutive INPH patients whose symptoms were followed for 1 year after shunt placement and 10 healthy control (HC) subjects were enrolled. Twenty of the initial 28 INPH patients were shunt-responsive (SR) and the other 8 patients were non-responsive (SNR). The cerebral white matter integrity was detected by assessing fractional anisotropy (FA) and mean diffusivity (MD). The mean hemispheric DTI indices and the ventricular sizes were calculated, and a map of these DTI indices was created for each subject. The DTI maps were analysed to compare preshunt INPH with HC and preshunt INPH with 1 year after shunt placement in each INPH group, using tract-based spatial statistics. We restricted analyses to the left hemisphere because of shunt valve artefacts.

Results: The ventricles became significantly smaller after shunt placement both in the SR and SNR groups. In addition, there was a significant interaction between clinical improvement after shunt and decrease in ventricular size. Although the hemispheric DTI indices were not significantly changed after shunt placement, there was a significant interaction between clinical improvement and increase in hemispheric MD. Compared with the HC group, FA in the corpus callosum and in the subcortical white matter of the convexity and the occipital cortex was significantly lower in SR at baseline, whereas MD in the periventricular and peri-Sylvian white matter was significantly higher in the SR group. Compared with the pre-operative images, the post-operative FA was only decreased in the corona radiata and only in the SR group. There were no significant regions in which DTI indices were altered after shunt placement in the SNR group.

Conclusions: Brain white matter regions in which FA was decreased after shunt placement were in the corona radiata between the lateral ventricles and the Sylvian fissures. This finding was observed only in shunt-responsive INPH patients and might reflect the plasticity of the brain for mechanical pressure changes from the cerebrospinal fluid system.

Keywords: Diffusion tensor imaging; Idiopathic normal pressure hydrocephalus; Lumboperitoneal shunt; Ventriculoperitoneal shunt; White matter.

Fig. 1

Comparison of skeletons and mis-registrations observed in TBSS analysis. a Demonstrates the mean FA skeleton (green) derived from the study (the comparison between the patients with INPH and the healthy control subjects) and the FMRIB58 FA standard space skeleton (grey). The periventricular tracks in the mean FA skeleton (the internal capsules and the corpus callosum in particular) are out of position. b Shows a sample of mis-registration that occurred in the comparison of MD maps between the patients with INPH and the healthy control subjects. The back-projected voxels (red) in the columns, bodies, and crura of the bilateral fornixes were positioned on each side of the lateral ventricle, and those in a peri-Sylvian portion of the SWM of bilateral frontal operculums were on each side of the Sylvian fissure. A anterior, I inferior, L left, P posterior, S superior

Fig. 2

Changes in left VV/ICV ratio, hemispheric FA, and hemispheric MD after shunt placement. Significance of interaction between shunt effectiveness for clinical improvement and for each index is denoted as follows: *p < 0.05; **p < 0.001

Fig. 3

White matter regions in which FA values were significantly lower in shunt-responsive INPH. The areas with significantly lower FA values are demonstrated by colours ranging from blue to light-blue in the shunt-responsive INPH patients compared to control subjects (p < 0.05, corrected for multiple comparisons by using TFCE). The mis-registered regions are shown in white. A anterior, L left, P posterior

Fig. 4

White matter regions in which MD values were significantly higher in shunt-responsive INPH. The areas with significantly higher MD values are demonstrated by colours ranging from red to yellow in the shunt-responsive INPH patients compared to control subjects (p < 0.05, corrected for multiple comparisons by using TFCE). The mis-registered regions are shown in white. A anterior, L left, P posterior

Fig. 5

White matter regions in which FA values significantly changed after shunt placement. a Demonstrates the areas with significantly decreased FA values after shunt placement in the shunt-responsive INPH patients using colours ranging from light-blue to pink (p < 0.05, corrected for multiple comparisons by using TFCE). b Shows the position of the anatomical ROI. On colour-coded FA map, red, green, and blue represent the direction of fibres (red, right-left; green, anterior-posterior; blue, superior-inferior). The ROI was placed on the blue regions in the left radiata on the axial slice that included the genu of the corpus callosum. A anterior, L left, P posterior