Advanced Ultrasound Imaging in Glioma Surgery: Beyond Gray-Scale B-mode

Abstract

Introduction: Glioma surgery is aimed at obtaining maximal safe tumor resection while preserving or improving patient's neurological status. For this reason, there is growing interest for intra-operative imaging in neuro-oncological surgery. Intra-operative ultrasound (ioUS) provides the surgeon with real-time, anatomical and functional information. Despite this, in neurosurgery ioUS mainly relies only on gray-scale brightness mode (B-mode). Many other ultrasound imaging modalities, such as Fusion Imaging with pre-operative acquired magnetic resonance imaging (MRI), Doppler modes, Contrast Enhanced Ultrasound (CEUS), and elastosonography have been developed and have been extensively used in other organs. Although these modalities offer valuable real-time intra-operative information, so far their usage during neurosurgical procedures is still limited. Purpose: To present an US-based multimodal approach for image-guidance in glioma surgery, highlighting the different features of advanced US modalities: fusion imaging with pre-operative acquired MRI for Virtual Navigation, B-mode, Doppler (power-, color-, spectral-), CEUS, and elastosonography. Methods: We describe, in a step-by-step fashion, the applications of the most relevant advanced US modalities during different stages of surgery and their implications for surgical decision-making. Each US modality is illustrated from a technical standpoint and its application during glioma surgery is discussed. Results: B-mode offers dynamic morphological information, which can be further implemented with fusion imaging to improve image understanding and orientation. Doppler imaging permits to evaluate anatomy and function of the vascular tree. CEUS allows to perform a real-time angiosonography, providing valuable information in regards of parenchyma and tumor vascularization and perfusion. This facilitates tumor detection and surgical strategy, also allowing to characterize tumor grade and to identify residual tumor. Elastosonography is a promising tool able to better define tumor margins, parenchymal infiltration, tumor consistency and permitting differentiation of high grade and low grade lesions. Conclusions: Multimodal ioUS represents a valuable tool for glioma surgery being highly informative, rapid, repeatable, and real-time. It is able to differentiate low grade from high grade tumors and to provide the surgeon with relevant information for surgical decision-making. ioUS could be integrated with other intra-operative imaging and functional approaches in a synergistic manner to offer the best image guidance for each patient.

Keywords: B-mode; Doppler; Glioma; contrast enhanced ultrasound; elastography; fusion imaging; intra-operative ultrasound; navigated ultrasound.

Figure 1

B-mode representation of different glioma grades. (A) Left temporal pilocytic astrocytoma. (B) Left temporal diffuse astrocytoma. (C) Right parietal anaplastic astrocytoma. (D) Right temporo-parietal glioblastoma. (1) pre-operative volumetric MRI. (2) Intra-operative trans-dural US scan. Note the different lesion appearances and in particular the different degree of margins definition.

Figure 2

Navigated intra-operative B-mode US in a case of left temporo-insular low-grade glioma. Two different configurations of navigated ioUS are displayed: (A) side-by-side or (B) superimposition. The continuous comparison between the two modalities aid in orientation and understanding of ioUS images.

Figure 3

Navigated intra-operative B-mode US in the final stages of surgery. (A) Left temporal anaplastic astrocytoma. (B) Right fronto-temporal glioblastoma. The comparison between ioUS and corresponding pre-operative MRI aid in identifying residual tumor and understanding ioUS semiotics: (A) side-by-side view, (B) superimposition.

Figure 4

Navigated ioUS (advanced modalities). (A) Color and spectral Doppler in a case of left temporo-insular anaplastic oligodendroglioma. (B) Contrast enhanced ultrasound in a case of left insular anaplastic astrocytoma. (C) Strain elastography in a case of left temporal glioblastoma; note the differences between the necrotic and the cystic areas and the interface with surrounding brain. Exploiting the continuous comparison between ioUS an pre-operative MRI is possible to understand US images and to infer about US and MRI correspondences. Legends are as follow: arrow heads: interface between tumor and brain; N: necrotic part of the tumor; C: cystic part of the tumor.

Figure 5

Doppler modalities. (A,B) Color Doppler and spectral doppler in a case of left temporal glioblastoma. (C,D) Power Doppler in a case of right temporal glioblastoma. Color Doppler informs on presence of flow, its direction and velocity through the setting of a region of interest. Spectral Doppler allows for a systematic analysis of flow-velocity over time thus permitting to characterize vessels nature. Power Doppler provides information on amplitude of flow depicting the number of scattering molecules (mainly erythrocytes).

Figure 6

CEUS representation of different glioma grades. (A,B) Right frontal low-grade glioma, (C,D) right frontal anaplastic astrocytoma, (E,F) left frontal glioblastoma. These images demonstrate the different degree and pattern of contrast enhancement among different glioma grades.

Figure 7

Time-frame of contrast enhancement in a case of right temporal glioblastoma. GBM have a rapid arterial and venous phase. MBs transit is chaotic and the peak is extremely intense. The major arterial supplies and draining veins are clearly visible. Contrast enhancement pattern is irregular and heterogeneous CE with both nodular high-enhanced and hypoperfused areas. Tumor borders are better defined than in B-mode.

Figure 8

Comparison between pre- (A) and post-resection (B) CEUS scans in a case of right temporo-parietal glioblastoma. After tumor removal, B-mode became difficult to understand because of surgical-induced artifacts whereas CEUS clearly demonstrates the presence of potential residual tumor.

Figure 9

Strain elastography (SE) scans in different glioma grades. (A,B) SE in a case of right parietal low grade glioma. (C,D) SE in a case of right fronto-parietal glioblastoma. SE is able to differentiate between LGG and HGG relying on their stiffness. LGG appear stiffer than brain whereas HGG softer. Furthermore, SE aid in identifying tumor borders and in distinguishing tumor and edema. (T: tumor, B: brain, arrow heads: interface between tumor and surrounding brain).