- Department of Neurosurgery, Huntsman Cancer Institute and Clinical Neurosciences Center, University of Utah, Salt Lake City, UT, USA
Randy L. Jensen
Department of Neurosurgery, Huntsman Cancer Institute and Clinical Neurosciences Center, University of Utah, Salt Lake City, UT, USA
DOI:10.4103/2152-7806.95422Copyright: © 2012 Garber ST. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
How to cite this article: Garber ST, Jensen RL. Image guidance for brain metastases resection. Surg Neurol Int 26-Apr-2012;3:
How to cite this URL: Garber ST, Jensen RL. Image guidance for brain metastases resection. Surg Neurol Int 26-Apr-2012;3:. Available from: http://sni.wpengine.com/surgicalint_articles/image-guidance-for-brain-metastases-resection/
The primary goal in removing a metastatic brain tumor is to maximize surgical resection while minimizing the risk of neurological injury. Intraoperative image guidance is frequently used in the resection of both primary and metastatic brain tumors. Stereotactic volumetric techniques allow for smaller craniotomies, facilitate lesion localization, and help neurosurgeons avoid eloquent structures. In turn, this leads to decreased patient morbidity and shorter hospitalizations. Image guidance is not without shortcomings, however, perhaps the most significant of which is inaccuracy of tumor resection associated with intraoperative brain shifts. The goal of this review is to expound on the uses of image guidance and discuss avoidance of technical pitfalls in the resection of cerebral metastatic lesions.
Keywords: Brain metastases, image guidance, resection
Brain metastases occur in 25–35% of all cancer patients, often leading to debilitating neurologic symptoms and contributing to a worse overall prognosis.[
In the senior author's (RLJ) practice, patients with metastatic disease are treated with various modalities for management of their intracranial disease [
The role of surgical resection in the management of intracranial disease became widely accepted with the publication in 1990 of the seminal paper by Patchell et al.,[
Despite initial resistance by many experienced neurosurgeons, the use of image guidance and neuronavigation has become standard in the resection of metastatic brain lesions.[
Dating back to the days of the eminent neurologist Paul Broca, the quest for cerebral localization has proved difficult. In more modern times, even in the hands of the most experienced neurosurgeons, finding intracranial targets can be challenging. This is especially true in smaller lesions or those near eloquent cortex, as illustrated by a simple case example. A 67-year-old man with a history of renal cell carcinoma diagnosed 4 years earlier presented to his local neurosurgeon with left arm weakness. He had known cervical spondylotic radiculopathy that had been treated with an anterior cervical discectomy and fusion 1 year earlier by the same neurosurgeon. Cervical magnetic resonance imaging (MRI) did not reveal a cause for his weakness, but a brain MRI disclosed a 1-cm right frontal lesion [
The patient described in Figure 1 underwent a frameless stereotactic craniotomy using intraoperative surgical navigation. Preoperative axial T1-weighted gadolinium-enhanced MRIs demonstrating actual lesion (a), with prior surgical bed visible anterior to lesion (b). Coronal T1-weighted gadolinium-enhanced MRIs demonstrating actual lesion (c), with prior surgical bed visible anterior to lesion (d). Sagittal T1-weighted nonenhanced MRIs demonstrating actual lesion with prior surgical bed visible anterior to lesion (e) and actual surgical bed (f). The lesion was identified and was histologically consistent with renal cell carcinoma
Precise intraoperative navigation is dependent on obtaining preoperative stereotactic MRI. The intraoperative imaging system must provide images with enough resolution to distinguish between tumor and normal brain and also between tumor and non-tumor pathologies such as peritumoral edema.[
In a retrospective study of 150 patients with single and multiple brain metastases, Schackert et al.[
Image guidance not only results in less surgical morbidity and greater accuracy of resection, but also in less overall cost to the patient. A British study done in 2000 showed that in patients undergoing craniotomy for meningioma resection, the use of image guidance resulted in a statistically significant decrease in surgical time as well as shorter duration of time in the intensive care unit (1.7 day vs. 1 day) and in overall length of hospital stay (13.5 days vs. 8.5 days).[
There is a learning curve involved in employing intraoperative neuronavigation, especially for neurosurgeons trained before its development; however, contemporarily trained neurosurgical residents are well versed in the use of image-guided neurosurgery. Although improvements can be difficult to quantify in a formal randomized controlled study, neuronavigational techniques have improved over time as increasingly sophisticated neuronavigational platforms are introduced and as practitioners become more versed in the world of high-speed computing. Initially, the time required to set up the navigational systems preoperatively increased operating room time; however, although we have not specifically measured this process, we believe that this set-up time has decreased over the years of using these systems. Of course, with each software upgrade or computer operating system change, or when using a new navigation platform, these issues can return even for the experienced surgeon. Nevertheless, the time saved by precise localization of the lesion before skin incision and the decreased time spent searching for a lesion makes up for the time spent setting up the case before beginning the actual operative procedure.
Perhaps the greatest limitation of neurosurgical image-guided stereotactic lesion removal is intraoperative brain shift.[
Several techniques can be used during removal of malignant cerebral metastases to help prevent or minimize intraoperative brain shifts. These include avoiding brain contraction techniques, such as hyperventilation and mannitol administration, until the tumor is exposed and ready to be debulked. Eschewing CSF diversion whenever possible and tracing the tumor margins using neuronavigation prior to tumor resection may also help reduce the amount of brain shift, as will avoiding penetrating a tumoral cyst.[
One potential method for correcting for intraoperative brain shift once it occurs is the use of intraoperative MRI (IMRI), an emerging technique that allows for intraoperative imaging and reregistration of the navigational system. The newly acquired image is done in the same position as the surgical position and any brain shifting from CSF loss or tumor removal is visualized in situ. This technology is not widely available, and its usefulness for neurosurgical procedures has not been fully quantified. Several studies have demonstrated its usefulness in primary brain tumors, especially low- and high-grade gliomas;[
A 67-year-old man with 1-month history of confusion was found to have a heterogeneously enhancing mass thought to represent a primary high-grade glioma or metastatic lesion. (a) T1-weighted SPGR MRI with gadolinium enhancement. (b) Intraoperative T1-weighted SPGR MRI with gadolinium enhancement showing a noticeable amount of brain shift that would have rendered the original navigational MRI inaccurate
When image guidance is used, both mean hospital stay and overall survival are similar in patients with single and multiple metastatic lesions, with no increase in perioperative complications.[
The use of neuronavigation with metastatic tumors in the posterior fossa is more controversial. Although we have used image-guided surgical techniques for many cerebellar lesions, it is somewhat less helpful in certain situations. First, given the small size of the posterior fossa and the well-defined borders of the tentorium and convexity dura, neuronavigation is not always necessary. Second, the prone position used in these surgeries can make access to external landmarks and fiducial markers more difficult than in supratentorial cases. Nevertheless, for deep-seated lesions of the posterior fossa, especially those near cerebellar nuclei, brainstem, or brachium pontis, neuronavigation may prove helpful and possibly even indispensable.
While gross total resection is desirable, many metastatic lesions have poorly defined borders and infiltrate into surrounding normal brain, so judgment must be exercised to avoid damaging the surrounding eloquent structures. Metastatic lesions, especially those treated with SRS, often show a mixture of radiation changes in the surrounding brain, necrotic tumor areas, and nests of live tumor cells. This is a situation where neuronavigation can help guide the surgeon to differentiate tumor from normal brain. This is also a situation in which IMRI may prove useful.
Neuronavigation is perhaps most useful for tumors located in eloquent cortex because critical structures can be avoided with precise lesion localization. The navigation system is indispensable in the operating room but may be even more important before the operative procedure begins. We routinely plan surgical approaches to avoid eloquent cortex using the anatomical data supplied by the preoperative MRI in the treatment planning station. Additionally, by using diffusion-weighted imaging with cortical tractography, fMRI, and positron emission tomography (PET) images loaded into the navigation system and fused to the anatomical data set, surgical plans can be made to minimize risk and maximize tumor resection. In addition, if the primary tumor is known, the surgeon should be aware of those lesions that have a high tendency to hemorrhage, including melanoma and renal cell tumors.[
Along these same lines, there are reports that piecemeal resection of a supratentorial brain metastasis carries a higher risk of leptomeningeal disease (LMD) than en bloc resection or SRS.[
All patients scheduled to undergo craniotomy for resection of cerebral metastases undergo stereotactic brain imaging with fiducial markers. Since almost all metastatic tumors enhance after administration of contrast agent, a T1-weighted, three-dimensional spoiled gradient recalled (SPGR) acquisition in a steady state with gadolinium contrast is our image of choice. Stereotactic computed tomography with contrast can be used for cases in which an MRI is not possible. For patients with severe renal failure, MRI without contrast is used, but this may require acquiring both a T1-weighted SPGR without contrast and a stereotactic T2-weighted MRI. In this situation, we fuse the two images and use them to best define the tumor borders. The fiducial markers are a luxury that can reduce registration time in the operating room and theoretically improve accuracy; however, when there is a delay between acquiring the preoperative imaging and the surgical procedure, external anatomical landmarks such as the medial and lateral canthi, pinna or tragus of the ear, tip of the nose, nasion, and any prior surgical scars can all act as registration fiducials.
This imaging is then loaded onto the image guidance system either remotely through the hospital network or from a compact disc prepared by the radiology department. We routinely load the images and plan the surgical approach the evening before surgery or while the operating room is being prepared on the morning of surgery. Once in the operating room, the patient is placed in the Mayfield head holder and secured in place using three-point fixation. When we are using IMRI, a special head holder and a navigation localizer are used. The techniques for IMRI are described elsewhere and are outside the scope of this report.[
Our experience with over 750 craniotomies using image-guided navigation, including roughly 200 for metastatic disease, has been one of improved extent of resection and less damage to surrounding eloquent structures. Others have reported similar results. In a review of 54 patients who underwent image-guided resection of malignant brain tumors (9 metastatic, 45 high-grade gliomas), 47 patients successfully underwent tumor resection.[
Advances in the early diagnosis and treatment of various types of malignancies, while leading to greater life expectancy in those affected, have also resulted in a higher number of cerebral metastases. The use of intraoperative image guidance techniques enables the location and definition of cerebral metastases, leading to smaller craniotomies, less patient morbidity, and more accurate surgical resection. However, intraoperative imaging is not without pitfalls, the most significant being intraoperative brain shifts during resection, which can lead to inaccuracy in defining tumor boundaries. Future studies are needed with larger patient numbers to prospectively determine success of resection among patients with cerebral metastases using image guidance versus those in which imaging is not used. Additionally, studies that quantify the amount of brain shift intraoperatively and then correlate this shift with the extent of surgical resection would be useful to determine the exact effects of these changes on surgical outcome. Regardless, the use of image guidance is vital in the successful resection of cerebral metastases, and we recommend its use in all cases of metastatic lesion removal to maximize resection and minimize patient morbidity.
Publication of this manuscript has been made possible by an educational grant from
The authors would like to thank Kristin Kraus, MSc, for her help in preparing this paper.
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