Surgical management of eloquent supratentorial low-grade gliomas with special emphasis on intraoperative imaging.

OBJECTIVE: Eloquent diffuse low-grade gliomas (LGGs) threaten patients' neurologic function and are also associated with inferior survival. Many neurosurgeons still refrain from early resection due to the fear of iatrogenic neurologic injury. However, the perceived safety of expectant management strategies may soon be overshadowed by the progressive deficits of tumor growth in eloquent regions. It is also known that radical and successful surgery prolongs progression-free survival, overall survival, and may reduce seizure burden and also potentially neurocognitive functions. Thus early successful surgery with preservation of function has a significant impact on patients' health. In modern neurosurgery, safe resection is often possible with detailed knowledge of anatomy and function together with the active use of various intraoperative surgical tools. We present illustrative cases of eloquent LGGs treated with different intraoperative tools. METHODS: An introduction to important intraoperative tools in LGG surgery is provided by experts in the field and described in five cases viewed in the context of the recent LGG literature. RESULTS: We present five cases with presumed eloquently located LGGs where extensive resection was offered using different intraoperative techniques. The clinical and radiologic outcomes are described. CONCLUSIONS: Correct use of intraoperative tools together with the surgeon's knowledge of anatomy and function will provide good functional and oncologic results in eloquently located LGGs. Watchful waiting or deferral of surgery due to tumor location (i.e., claiming inoperability) is very rarely good practice.

Model-based correction of velocity measurements in navigated 3-D ultrasound imaging during neurosurgical interventions.

In neurosurgery, information of blood flow is important to identify and avoid damage to important vessels. Three-dimensional intraoperative ultrasound color-Doppler imaging has proven useful in this respect. However, due to Doppler angle-dependencies and the complexity of the vascular architecture, clinical valuable 3-D information of flow direction and velocity is currently not available. In this work, we aim to correct for angle-dependencies in 3-D flow images based on a geometric model of the neurovascular tree generated on-the-fly from free-hand 2-D imaging and an accurate position sensor system. The 3-D vessel model acts as a priori information of vessel orientation used to angle-correct the Doppler measurements, as well as provide an estimate of the average flow direction. Based on the flow direction we were also able to do aliasing correction to approximately double the measurable velocity range. In vitro experiments revealed a high accuracy and robustness for estimating the mean direction of flow. Accurate angle-correction of axial velocities were possible given a sufficient beam-to-flow angle for at least parts of a vessel segment . In vitro experiments showed an absolute relative bias of 9.5% for a challenging low-flow scenario. The method also showed promising results in vivo, improving the depiction of flow in the distal branches of intracranial aneurysms and the feeding arteries of an arteriovenous malformation. Careful inspection by an experienced surgeon confirmed the correct flow direction for all in vivo examples.

Tissue motion and strain in the human brain assessed by intraoperative ultrasound in glioma patients.

The objective of the study was to investigate tissue motion and strain imposed by cardiovascular pulsation in pathologic and normal brain parenchyma, as quantified from in vivo ultrasound data. Ultrasound acquired during surgery of 16 patients with glial tumors was retrospectively processed and analyzed. The tissue velocity was quantified at depths of 1cm, 2cm and 3cm from brain cortex to investigate spatial dependency with depth. Comparison of strain and velocity in tumor and adjacent normal parenchyma was performed by selecting two regions-of-interest in the hyperechoic tumor and two regions in the low-echogenic areas interpreted as mainly normal tissue with some degree of tumor cell infiltration. The absolute maximum tissue velocity is seen to increase with increasing depths in 14 of 16 cases (87.5%). The maximum tissue velocities in the four regions close to the ultrasound visible tumor border are not statistically different (p=0.163 to p=0.975). The strain magnitudes are significantly higher in the regions with expected normal brain parenchyma than in regions with expected glial tumor tissue, both for the two regions being closest to the tumor border (p=0.0004) and for the two regions further away from the tumor border (p=0.0009). We conclude that the velocity of the brain parenchyma imposed by arterial pulsation during a cardiac cycle is generally increasing with increasing depth from cortex. The maximum velocity appears to be similar in regions with expected normal brain and tumor tissue, thus, does not seem to be affected by pathology. Strain magnitude is, however, a suitable parameter for discrimination of glial tumor and normal brain parenchyma. (E-mail: Tormod.Selbekk@sintef.no).

Blood flow imaging: an angle-independent ultrasound modality for intraoperative assessment of flow dynamics in neurovascular surgery.

OBJECTIVE: The objective of this study was to investigate the clinical applicability of navigated blood flow imaging (BFI) in neurovascular applications. BFI is a new 2-dimensional ultrasound modality that offers angle-independent visualization of flow. When integrated with 3-dimensional (3D) navigation technology, BFI can be considered as a first step toward the ideal tool for surgical needs: a real-time, high-resolution, 3D visualization that properly portrays both vessel geometry and flow direction. METHODS: A 3D model of the vascular tree was extracted from preoperative magnetic resonance angiographic data and used as a reference for intraoperative any-plane guided ultrasound acquisitions. A high-end ultrasound scanner was interconnected, and synchronized recordings of BFI and 3D navigation scenes were acquired. The potential of BFI as an intraoperative tool for flow visualization was evaluated in 3 cerebral aneurysms and 3 arteriovenous malformations. RESULTS: The neurovascular flow direction was properly visualized in all cases using BFI. Navigation technology allowed for identification of the vessels of interest, despite the presence of brain shift. The surgeon found BFI to be very intuitive compared with conventional color Doppler methods. BFI allowed for quality control of sufficient flow in all distal arteries during aneurysm surgery and made it easier to discern between feeding arteries and draining veins during surgery for arteriovenous malformations. CONCLUSION: BFI seems to be a promising modality for neurovascular flow visualization that may provide the neurosurgeon with a valuable tool for safer surgical interventions. However, further work is needed to establish the clinical usefulness of the proposed imaging setup.

Comparison of navigated 3D ultrasound findings with histopathology in subsequent phases of glioblastoma resection.

OBJECTIVE: The purpose of the study was to compare the ability of navigated 3D ultrasound to distinguish tumour and normal brain tissue at the tumour border zone in subsequent phases of resection. MATERIALS AND METHODS: Biopsies were sampled in the tumour border zone as seen in the US images before and during surgery. After resection, biopsies were sampled in the resection cavity wall. Histopathology was compared with the surgeon's image findings. RESULTS: Before resection, the tumour border was delineated by ultrasound with high specificity and sensitivity (both 95%). During resection, ultrasound had acceptable sensitivity (87%), but poor specificity (42%), due to biopsies falsely classified as tumour by the surgeon. After resection, sensitivity was poor (26%), due to tumour or infiltrated tissue in several biopsies deemed normal by ultrasound, but the specificity was acceptable (88%). CONCLUSIONS: Our study shows that although glioblastomas are well delineated prior to resection, there seem to be overestimation of tumour tissue during resection. After resection tumour remnants and infiltrated brain tissue in the resection cavity wall may be undetected. We believe that the benefits of intraoperative ultrasound outweigh the shortcomings, but users of intraoperative ultrasound should keep the limitations shown in our study in mind.

Operation of arteriovenous malformations assisted by stereoscopic navigation-controlled display of preoperative magnetic resonance angiography and intraoperative ultrasound angiography.

OBJECTIVE: To study the application of navigated stereoscopic display of preoperative three-dimensional (3-D) magnetic resonance angiography and intraoperative 3-D ultrasound angiography in a clinical setting. METHODS: Preoperative magnetic resonance angiography and intraoperative ultrasound angiography are presented as stereoscopic images on the monitor during the operation by a simple red/blue technique. Two projections are generated, one for each eye, according to a simple ray casting method. Because of integration with a navigation system, it is possible to identify vessels with a pointer. The system has been applied during operations on nine patients with arteriovenous malformations (AVMs). Seven of the patients had AVMs in an eloquent area. RESULTS: The technology makes it easier to understand the vascular architecture during the operation, and it offers a possibility to identify and clip AVM feeders both on the surface and deep in the tissue at the beginning of the operation. All 28 feeders identified on the preoperative angiograms were identified by intraoperative navigated stereoscopy. Twenty-five were clipped at the beginning of the operation. The other three were clipped at a later phase of the operation. 3-D ultrasound angiography was useful to map the size of the nidus, to detect the degree of brain shift, and to identify residual AVM. CONCLUSION: Stereoscopic visualization enhances the surgeon's perception of the vascular architecture, and integrated with navigation technology, this offers a reliable system for identification and clipping of AVM feeders in the initial phase of the operation.

Intraoperative navigated 3-dimensional ultrasound angiography in tumor surgery.

BACKGROUND: Avoiding damage to blood vessels is often the concern of the neurosurgeon during tumor surgery. Using angiographic image data in neuronavigation may be useful in cases where vascular anatomy is of special interest. Since 2003, we have routinely used 3D ultrasound angiography in tumor surgery, and between January 2003 and May 2005, 62 patients with different tumors have been operated using intraoperative 3D ultrasound angiography in neuronavigation. METHODS: An ultrasound-based neuronavigation system was used. In addition to 3D ultrasound tissue image data, 3D ultrasound angiography (power Doppler) image data were acquired at different stages of the operation. The value and role of navigated 3D ultrasound angiography as judged by the surgeon were recorded. RESULTS: We found that intraoperative ultrasound angiography was easy to acquire and interpret, and that image quality was sufficient for neuronavigation. In 26 of 62 cases, ultrasound angiography was found to be helpful by visualizing hidden vessels adjacent to and inside the tumor, facilitating tailored approaches and safe biopsy sampling. CONCLUSIONS: Intraoperative 3D ultrasound angiography is straightforward to use, image quality is sufficient for image guidance, and it adds valuable information about hidden vessels, increasing safety and facilitating tailored approaches. Furthermore, with updated 3D ultrasound angiography imaging, accuracy of neuronavigation may be maintained in cases of brain shift.

Three-dimensional ultrasonography navigation in spinal cord tumor surgery. Technical note.

The authors describe the technical application of three-dimensional (3D) ultrasonography navigation in spinal cord tumor surgery. The spinal cord is a complex neurological structure in which there is the potential for causing neurological morbidity during tumor resection. Standard neuronavigation systems based on computed tomography or C-arm images are not adapted to tumor surgery in the spinal cord. Since 2004 the authors have been using a 3D ultrasonography-based neuronavigation system. During surgery, two-dimensional ultrasound images were acquired and reconstructed into 3D image data to assist in tumor resection. The navigation cameras read the position of a patient reference frame attached to a spinous process, the ultrasonography probe, and surgical instruments. Five- and 10-MHz phased-array ultrasonography probes equipped with optical tracking frames were used for image data acquisition. Spinal cord tumors were visualized using ultrasonography, and 3D ultrasonography-guided tumor biopsy sampling and resection were performed. The practice of attaching the reference frame to a spinous process adjacent to the spinal cord tumor, as well as performing image acquisition just before starting the resection, reduced the possible sources of inaccuracy. The technical application of a navigation system based on intraoperative 3D ultrasound image reconstruction seems feasible and may have the potential of improving functional outcome in association with spinal cord tumor surgery.

Computer-assisted 3D ultrasound-guided neurosurgery: technological contributions, including multimodal registration and advanced display, demonstrating future perspectives.

BACKGROUND: Navigation systems are now frequently being used for guiding surgical procedures. Existing neuronavigation systems suffer from the lack of updated images when tissue changes during surgery as well as from user-friendly displays of all essential images for accurate and safe surgery guidance. METHODS: We have developed various new technologies for improved neuronavigation. Using intraoperative 3D ultrasound (US) imaging, we have developed various registration algorithms for using and updating a complete multimodal and multivolume 3D map for navigation. RESULTS: We experienced that advanced multimodal visualization makes it easy to interpret information from several image volumes and modalities simultaneously. Using high quality intraoperative 3D ultrasound, essential preoperative information could be corrected due to brain shift. fMRI and other important preoperative data could then be used together with intraoperative ultrasound imaging for more accurate, safer and improved guidance of therapy. CONCLUSIONS: We claim that new features, as demonstrated in the present paper, using intraoperative 3D ultrasound in combination with advanced registration and display algorithms will represent important contributions towards more accurate, safer and more optimized future patient treatment.

Operation of arteriovenous malformations assisted by stereoscopic navigation-controlled display of preoperative magnetic resonance angiography and intraoperative ultrasound angiography.

OBJECTIVE: To study the application of navigated stereoscopic display of preoperative three-dimensional (3-D) magnetic resonance angiography and intraoperative 3-D ultrasound angiography in a clinical setting. METHODS: Preoperative magnetic resonance angiography and intraoperative ultrasound angiography are presented as stereoscopic images on the monitor during the operation by a simple red/blue technique. Two projections are generated, one for each eye, according to a simple ray casting method. Because of integration with a navigation system, it is possible to identify vessels with a pointer. The system has been applied during operations on nine patients with arteriovenous malformations (AVMs). Seven of the patients had AVMs in an eloquent area. RESULTS: The technology makes it easier to understand the vascular architecture during the operation, and it offers a possibility to identify and clip AVM feeders both on the surface and deep in the tissue at the beginning of the operation. All 28 feeders identified on the preoperative angiograms were identified by intraoperative navigated stereoscopy. Twenty-five were clipped at the beginning of the operation. The other three were clipped at a later phase of the operation. 3-D ultrasound angiography was useful to map the size of the nidus, to detect the degree of brain shift, and to identify residual AVM. CONCLUSION: Stereoscopic visualization enhances the surgeon's perception of the vascular architecture, and integrated with navigation technology, this offers a reliable system for identification and clipping of AVM feeders in the initial phase of the operation.

Strain processing of intraoperative ultrasound images of brain tumours: initial results.

The purpose of the study was to investigate a method for strain calculation and its ability to discriminate between brain tumour and normal brain. During surgery of a low-grade astrocytoma and a metastasis, we acquired ultrasound (US) radiofrequency (RF) data with a hand-held probe at the dura mater. Using cross-correlation and phase-sensitive processing, we quantified the tissue displacements between consecutive US images and, subsequently, the local strain. In the elastograms, the tumour lesions were associated with lower strain levels than those found in the surrounding normal tissue. For both investigated cases, the strain images showed good agreement with the B-mode images. However, the results also indicated that the tumour interpretation might be different in the two modalities. An important finding was that the tissue motion caused by arterial pulsation is sufficient for generating elastograms. Requiring no specialised equipment or changes to acquisition procedures, strain data can be obtained as easily as conventional US imaging.

Multimodal image fusion in ultrasound-based neuronavigation: improving overview and interpretation by integrating preoperative MRI with intraoperative 3D ultrasound.

OBJECTIVE: We have investigated alternative ways to integrate intraoperative 3D ultrasound images and preoperative MR images in the same 3D scene for visualizing brain shift and improving overview and interpretation in ultrasound-based neuronavigation. MATERIALS AND METHODS: A Multi-Modal Volume Visualizer (MMVV) was developed that can read data exported from the SonoWand neuronavigation system and reconstruct the spatial relationship between the volumes available at any given time during an operation, thus enabling the exploration of new ways to fuse pre- and intraoperative data for planning, guidance and therapy control. In addition, the mismatch between MRI volumes registered to the patient and intraoperative ultrasound acquired from the dura was qualified. RESULTS: The results show that image fusion of intraoperative ultrasound images in combination with preoperative MRI will make perception of available information easier by providing updated (real-time) image information and an extended overview of the operating field during surgery. This approach will assess the degree of anatomical changes during surgery and give the surgeon an understanding of how identical structures are imaged using the different imaging modalities. The present study showed that in 50% of the cases there were indications of brain shift even before the surgical procedure had started. CONCLUSIONS: We believe that image fusion between intraoperative 3D ultrasound and preoperative MRI might improve the quality of the surgical procedure and hence also improve the patient outcome.

Brain operations guided by real-time two-dimensional ultrasound: new possibilities as a result of improved image quality.

OBJECTIVE: In 1995, a project was initiated in Trondheim, Norway, to investigate various possibilities for more frequent use of ultrasound in brain surgery. Since that time, the quality of ultrasonic images has improved considerably through technological adjustment of parameters. The objective of the present study was to explore essential clinical parameters required for the successful use of ultrasonic guidance in brain surgery. METHODS: During the study period, several surgical setups designed to optimize the use of intraoperative real-time two-dimensional ultrasonic imaging were explored. These included various positions of the ultrasound probe in relation to both the operation cavity and the lesion, as well as the position of the operation channel in relation to the gravity line. RESULTS: All lesions from the latest period (1997-2001; n = 114) were depicted well by ultrasound imaging, with the exception of two cases. High image quality and direct image guidance of the tool were maintained best throughout the operation by imaging through an intact dura and at an angle relative to a vertical operation channel. All tumor operations were performed without complications, and ultrasound imaging was found to be an important factor in the detection of remaining tumor tissue at the conclusion of surgery. For 14 low vascular tumors, the operation was guided only by ultrasound imaging. No bleeding complications occurred. A method of minimally invasive ultrasound-guided evacuation of hematomas was developed. In 19 patients, the method was found to be efficient (i.e., >90% of the hematoma was evacuated) and without complications, except for one patient who experienced rebleeding. CONCLUSION: With proper planning and surgical setup, ultrasound imaging may provide acceptable image quality for use in image-guided brain operations.

Neuronavigation by intraoperative three-dimensional ultrasound: initial experience during brain tumor resection.

OBJECTIVE: Three-dimensional (3-D) ultrasound is an intraoperative imaging modality used in neuronavigation as an alternative to magnetic resonance imaging (MRI). This article summarizes 4 years of clinical experience in the use of intraoperative 3-D ultrasound integrated into neuronavigation for guidance in brain tumor resection. METHODS: Patients were selected for inclusion in the study on the basis of the size and location of their lesion. Preoperative 3-D MRI data were registered and used for planning as in other conventional neuronavigation systems. Intraoperative 3-D ultrasound images were acquired three to six times, and tumor resection was guided on the basis of these updated 3-D images. RESULTS: Intraoperative 3-D ultrasound represents a good solution to the problem of brain shift in neuronavigation because it easily provides an updated, and hence more accurate, map of the patient's true anatomy in all phases of the operation. Ultrasound makes it possible to follow the progression of the operation, and it improves the radicality of tumor resection by detecting tumor tissue that would remain if the imaging technology had not been used (in 53% of the cases). Integration of 3-D ultrasound with navigation technology solves the orientation problem experienced previously with two-dimensional ultrasound in neurosurgery. The technology makes it possible to directly compare intraoperative ultrasound and MRI data regarding visualization of the lesion. Ultrasound image quality is useful for guiding surgical procedures. CONCLUSION: Intraoperative 3-D ultrasound seems to provide a time- and cost-effective way to update high-quality 3-D maps used in neuronavigation.