Intraoperative acquisition of DTI in cranial neurosurgery: readout-segmented DTI versus standard single-shot DTI

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OBJECTIVE

Diffusion tensor imaging (DTI) tractography is commonly used in neurosurgical practice but is largely limited to the preoperative setting. This is due primarily to image degradation caused by susceptibility artifact when conventional single-shot (SS) echo-planar imaging (EPI) DTI (SS-DTI) is acquired for open cranial, surgical position intraoperative DTI (iDTI). Readout-segmented (RS) EPI DTI (RS-DTI) has been reported to reduce such artifact but has not yet been evaluated in the intraoperative MRI (iMRI) environment. The authors evaluated the performance of RS versus SS EPI for DTI of the human brain in the iMRI setting.

METHODS

Pre- and intraoperative 3-T 3D T1-weighted and 2D multislice RS-iDTI (called RESOLVE [readout segmentation of long variable echo-trains] on the Siemens platform) and SS-iDTI images were acquired in 22 adult patients undergoing intraaxial iMRI resections for suspected low-grade glioma (14; 64%), high-grade glioma (7; 32%), or focal cortical dysplasia. Regional susceptibility artifact, anatomical deviation relative to T1-weighted imaging, and tractographic output for surgically relevant tracts were compared between iDTI sequences as well as the intraoperative tract shifts from preoperative DTI.

RESULTS

RS-iDTI resulted in qualitatively less regional susceptibility artifact (resection cavity, orbitofrontal and anterior temporal cortices) and mean anatomical deviation in regions most prone to susceptibility artifact (RS-iDTI 2.7 ± 0.2 vs SS-iDTI 7.5 ± 0.4 mm) compared to SS-iDTI. Although tract reconstruction success did not significantly differ by DTI method, susceptibility artifact–related tractography failure (of at least 1 surgically relevant tract) occurred for SS-iDTI in 8/22 (36%) patients, and in 5 of these 8 patients RS-iDTI permitted successful reconstruction. Among cases with successful tractography for both sequences, maximal intersequence differences were substantial (mean 9.5 ± 5.7 mm, range −27.1 to 18.7 mm).

CONCLUSIONS

RS EPI enables higher quality and more accurate DTI for surgically relevant tractography of major white matter tracts in intraoperative, open cranium neurosurgical applications at 3 T.

ABBREVIATIONS CSpT = corticospinal tract; DEC = directionally encoded color; DTI = diffusion-tensor imaging; EPI = echo-planar imaging; HGG = high-grade glioma; iDTI = intraoperative DTI; iMRI = intraoperative MRI; LGG = low-grade glioma; ROI = region of interest; RS = readout segmented; SNR = signal-to-noise ratio; SS = single-shot; SS-DTI = SS echo-planar imaging DTI; TTD = target-to-tract distance; ΔTTD = intraoperative change in TTD.

Article Information

Correspondence Cameron A. Elliott: University of Alberta, Edmonton, AB, Canada. celliott@ualberta.ca.

INCLUDE WHEN CITING Published online August 16, 2019; DOI: 10.3171/2019.5.JNS19890.

T.S. and C.B. contributed equally to this work and share senior authorship.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Susceptibility artifact comparison of RS-DTI versus SS-DTI in 3 iMRI cases. The preoperative T1, intraoperative T1-weighted (iT1), and the intraoperative average b1000 diffusion-weighted images for RS-iDTI and SS-iDTI are shown for 2 slices in each of 3 representative cases. RS-iDTI enhanced image quality with reduced susceptibility artifact image degradation and sharper structural delineation compared to SS-iDTI, as highlighted by ellipses. Please note that in patient 22 the surgeon elected to replace the bone flap and fold the skin over (without closing dura) to protect the brain from the draping.

  • View in gallery

    Average absolute anatomical deviation of RS-iDTI compared to SS-iDTI. Average anatomical deviation was reduced significantly on RS-iDTI relative to SS-iDTI as measured from the absolute value of the distance (in mm) between the corresponding anatomical points in the resection cavity (A), orbitofrontal cortex (B), and anterior temporal tip (C) on iDTI versus susceptibility artifact–resistant T1-weighted images. ****p < 0.0001, ***p < 0.001. Bars indicate group mean and error bars denote SD.

  • View in gallery

    Bland-Altman plot of TTD when tract reconstruction was possible with RS-iDTI and SS-iDTI. The difference in TTD (RS-iDTI minus SS-iDTI TTD) is plotted against the mean of the 2 measurements (in mm). The solid line represents the overall mean of the differences (−0.3 mm) while the dashed lines represent the mean of the differences ± 1.96 (limits of agreement).

  • View in gallery

    Differences in intraoperative tractographic output and intraoperative shift in TTD. Representative example in patient 7 (63-year-old male with HGG) comparing multiplanar preoperative (A, D, G) and intraoperative tract reconstructions acquired in the surgical position, with dura and cranium open for RS-iDTI data (B, E, H) and SS-iDTI data (C, F, I) of the corticospinal tract (blue) and inferior fronto-occipital fasciculus (IFOF) (green). The tracts are overlaid on T1 images in each case. RS-iDTI routinely demonstrated more robust tract reconstructions with fewer tractographic failures (e.g., IFOF failure in panel I) than SS-iDTI.

  • View in gallery

    Differences in intraoperative tractographic output and intraoperative tract shift in TTD. Representative example in patient 6 (36-year-old male with HGG) comparing multiplanar preoperative (A, D, G, J, M, P) and intraoperative tract reconstructions at 2 identical locations acquired in surgical position, with dura and cranium open for RS-iDTI data (B, E, H, K, N, Q) and SS-iDTI data (C, F, I, L, O, R) of the corticospinal tract (blue), superior longitudinal fasciculus (green), and anterior corpus callosum (red). RS-iDTI routinely demonstrated more robust tract reconstructions with fewer tractographic failures than SS-iDTI. Large intersequence differences were demonstrated between RS-iDTI– and SS-iDTI–modeled tracts.

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