Challenges and Opportunities of Intraoperative 3D Ultrasound With Neuronavigation in Relation to Intraoperative MRI

Abstract

Introduction: Neuronavigation greatly improves the surgeons ability to approach, assess and operate on brain tumors, but tends to lose its accuracy as the surgery progresses and substantial brain shift and deformation occurs. Intraoperative MRI (iMRI) can partially address this problem but is resource intensive and workflow disruptive. Intraoperative ultrasound (iUS) provides real-time information that can be used to update neuronavigation and provide real-time information regarding the resection progress. We describe the intraoperative use of 3D iUS in relation to iMRI, and discuss the challenges and opportunities in its use in neurosurgical practice.

Methods: We performed a retrospective evaluation of patients who underwent image-guided brain tumor resection in which both 3D iUS and iMRI were used. The study was conducted between June 2020 and December 2020 when an extension of a commercially available navigation software was introduced in our practice enabling 3D iUS volumes to be reconstructed from tracked 2D iUS images. For each patient, three or more 3D iUS images were acquired during the procedure, and one iMRI was acquired towards the end. The iUS images included an extradural ultrasound sweep acquired before dural incision (iUS-1), a post-dural opening iUS (iUS-2), and a third iUS acquired immediately before the iMRI acquisition (iUS-3). iUS-1 and preoperative MRI were compared to evaluate the ability of iUS to visualize tumor boundaries and critical anatomic landmarks; iUS-3 and iMRI were compared to evaluate the ability of iUS for predicting residual tumor.

Results: Twenty-three patients were included in this study. Fifteen patients had tumors located in eloquent or near eloquent brain regions, the majority of patients had low grade gliomas (11), gross total resection was achieved in 12 patients, postoperative temporary deficits were observed in five patients. In twenty-two iUS was able to define tumor location, tumor margins, and was able to indicate relevant landmarks for orientation and guidance. In sixteen cases, white matter fiber tracts computed from preoperative dMRI were overlaid on the iUS images. In nineteen patients, the EOR (GTR or STR) was predicted by iUS and confirmed by iMRI. The remaining four patients where iUS was not able to evaluate the presence or absence of residual tumor were recurrent cases with a previous surgical cavity that hindered good contact between the US probe and the brainsurface.

Conclusion: This recent experience at our institution illustrates the practical benefits, challenges, and opportunities of 3D iUS in relation to iMRI.

Keywords: 3D; iMRI = intraoperative MRI; neurosurgery; tumor; ultrasound.

Figure 1

Case 1 Surgical Plan. (A) Axial T2-weighted imaging showing an hypointensity in the right middle frontal gyrus, anterior to the precentral gyrus; (B) Coronal T2-weighted imaging showing an hypointensity in the right middle frontal gyrus; (C) Sagittal T2*-weighted imaging showing BOLD activation for lip purse test (yellow) on the lateral aspect of the right precentral gyrus; (D) Axial T2*-weighted imaging showing the right Corticospinal Tract (CST) on the deep and posterior margins of the tumor; (E) Coronal T2-weighted imaging showing the right CST descending from the precentral gyrus in the posterior aspect of the tumor; (F) 3D brain reconstruction showing the BOLD activation for lip purse segmented (in blue), the segmented tumor (green) and the CST deep (in purple).

Figure 2

Case 1 intraoperative screen capture with the 3D surgical plan reconstruction with fMRI BOLD activation segmented in orange, tumor in green and Corticospinal Tract in yellow (the upper left panel), and the three orthogonal planes with 3D iUS-1 overlaid on preoperative MP2Rage. Notice the mismatch between the segmented tumor on MRI (green segmentation) and observed tumor on iUS (red arrowhead), placing the tumor site over the sulcus between the gyri making it difficult to know which gyrus was the tumor actually located.

Figure 3

Case 1 Post hoc manually aligned preoperative axial T2-weighted imaging with (A) iUS-1, (B) iUS-2, (C) iUS-3 with right Corticospinal Tract (yellow) and Frontal Aslant Tract (red), and (D) iMRI axial T2-weighted imaging manually aligned with iUS-3. On D it is possible to observe a gross total resection on iUS and confirmed by iMRI.

Figure 4

Case 2 Post hoc manually aligned preoperative axial T2-weighted imaging with (A) iUS-1, (B) iUS-2, (C) iUS-3 with multiple tracts around and inside the tumor, and (D) iMRI axial T2-FLAIR imaging manually aligned with iUS-3 without the overlaid tracts. Notice on C the presence of tracts running through the tumor. On D, it is possible to notice the presence of residual tumor in the posterolateral margin as well as posteriorly along the medial margin in the vicinity of the coursing tracts through the tumor.

Figure 5

Case 2 intraoperative screen capture with the 3D surgical plan reconstruction with fMRI BOLD activation segmented in dark and light blue and tumor in green (upper left panel), and the three orthogonal planes with 3D iUS-3 overlaid on preoperative MP2Rage. Notice the navigation probe in close proximity to the tracts running through the tumor. In order to preserve these tracts, no further resection medially was performed.

Figure 6

iUS1 in Case 3. Central panel shows a sagittal T2*-weighted imaging with fMRI BOLD activations for lower extremity (red) and upper extremity (blue). (A) Coronal iUS-1 showing the most anterior part of the tumor; (B) coronal iUS-1 showing the only possible surgical corridor that avoids the fMRI BOLD activations areas and Corticospinal Tract (CST); (C) Coronal iUS-1 overlaid with fMRI BOLD activation for lower extremity and CST superior to the tumor; (D) coronal iUS-1 with overlay of CST superior to the tumor.

Figure 7

Case3. iUS3 (A) showing unexpected residual tumor (red arrowhead) under the arachnoid fold which was confirmed by iMRI (B).