The Usefulness of Stereotactic Neuronavigation Along with Intraoperative Imaging in Malignant Brain Tumor Surgery



Fig. 4.1
Intraoperative use of ultrasound revealing a hyperechoic lesion representing tumor prior to resection. A hypoechoic area in the center is the carotid artery. The apparatus remains on the field allowing for relatively quick, real-time feedback about extent of resection



The most important advantage of iUS is that it provides the neurosurgeon with realtime information, including accurate localization and characterization of a lesion, compensation for brain shift that can be problematic for stereotactic neuronavigation systems, and detection of unforeseen surgical sequelae, such as intraoperative hemorrhage or hydrocephalus, therefore decreasing surgical time and potential morbidity [25]. iUS can better define critical tumor margins and decrease the likelihood of leaving residual tumor [14, 27]. It can easily locate and help evacuate cystic components, as well as define tumor tissue planes. iUS can be readily available with a relatively low cost when used routinely in an established tumor practice [25, 28]. The time it takes to perform an intraoperative ultrasound is very short (i.e., seconds to minutes) and can be performed numerous times, and no additional personnel is needed if the surgeon has sufficient experience with its use and interpretation.

Evidence indeed suggests that the imaging provided by iUS is seemingly advantageous to the success of brain tumor surgery. Saether et al. studied the use of 3D iUS in GBM surgery, and their findings suggest improvement in survival with this technology even after adjusting for known prognostic factors [14, 29]. In this retrospective study, Seather et al., reviewed 193 GBM patients and analyzed the effect of the use of 3D ultrasound and neuronavigation on overall survival [29]. They observed an increase in survival (9.6 vs. 11.9 months; HR = 0.7; p = 0.034) after adjusting for age, WHO performance status, and type of radiotherapy and chemotherapy [29]. Moiyadi et al. in a retrospective series studied the effects of the use of 3D iUS and revealed that combining 3D iUS data with MR guided neuronavigation resulted in further resection attempts and gross total resection (GTR) levels comparable to the use of iMRI [14, 30]. In the senior author’s practice, the use of iUS, along with stereotactic neuronavigation, is standard on all tumor cases. The use of iMRI is reserved as an adjunct to iUS in more infiltrative tumors, such as malignant gliomas, where it can be more difficult to interpret residual tumor versus edematous brain on the border of the resection cavity.

Though undeniably useful, versatile, and readily available, it should be noted, however, the sensitivity and specificity of iUS is far less as compared with iMRI (see below) and interpretation of findings requires training and experience [31]. For example, a hyperechoic rim can be observed around the resection cavity which may be interpreted as tumor, although this is a nonspecific finding [32]. One of the other common artifactual problems of iUS is acoustic enhancement artifact (AEA). These artifacts appear at the bottom of the resection cavity after some tumor debulking when ultrasound penetrates through a higher column of saline. The appearance of AEAs is due to a large difference between a very low attenuation of acoustic waves in saline and high attenuation of acoustic waves in brain tissue, and they may block detection of tumor remnants at the depth of resection cavity [33, 34]. Using a mini US probe within the cavity may decrease the column of saline between the probe area of interest and then reduce the AEAs at the depth of the resection cavity [34, 35].

Novel technological advancements in ultrasonography can help overcome some of the shortcomings of more traditional, two-dimensional (2D) iUS. Over the last two decades, for instance, 3D iUS systems have become available and such multiplanar imaging capabilities can help overcome some of the limitations with regard to orientation of 2D US, leading to improved quality of imaging [30]. As mentioned, navigated iUS can use tracked ultrasound images (both 2D and 3D) for guidance and improvement in orientation [36]. The ultrasound can be used along with the preoperative MRI for the purpose of navigation and can help eliminate any inherent potential registration inaccuracies [37]. Co-registering with functional imaging [i.e., functional MRI (fMRI) and diffusion tensor imaging (DTI)] can further enhance the safety of the resection. Finally, contrast-enhanced iUS techniques can help improve tumor visualization with the intraoperative administration of contrast [38].



Intraoperative Magnetic Resonance Imaging (iMRI)


While MRI imaging has long been a fundamental component in the diagnosis and treatment of malignant brain tumors for its ability to provide surgeons with high-resolution multiplanar anatomic detail of the brain, it has more recently become an important intraoperative tool [39]. The ability to image the brain during surgery facilitates superior neuronavigation and can help overcome the limitations of stereotactic neuronavigation systems, rendering them more effective throughout the entirety of the surgery. More specifically, the use of iMRI can correct for these inherent neuronavigation inaccuracies that accrue over the course of an operation by allowing re-registration of the stereotactic neuronavigation with the intraoperative scan that is obtained after many of these steps of the operation that contribute to neuronavigation inaccuracy are completed. iMRI also has substantial benefit in verifying the extent of tumor resection and location of residual tumor after resection has begun, although it should be noted that this pertains primarily to intra-axial tumors that can be difficult to distinguish from normal brain tissue and holds less benefit from easily delineated extra-axial masses (Fig. 4.2). Intraoperative imaging has the additional capabilities that it can be used to confirm the correct positioning of a biopsy needle in the case of stereotactic biopsies or demonstrate the presence of early complications such as hemorrhage or ischemia that can be addressed intraoperatively [40].

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Fig. 4.2
A 47-year-old man with recurrent GBM after treatment with radiation and chemotherapy. Preoperative T1-weighted post gadolinium MRI (a) reveals a right frontoparietal mass. Intraoperative T1-weighted post gadolinium MRI (b) shows some residual treatment effects with tumor along the anterior resection cavity that appeared like gliotic brain grossly under the microscope

Intraoperative MRI first became available in the 1990s with the advent of open bore magnets [39]. The first intraoperative magnets had low field strength (0.2–0.5T), which required longer scan times, limited anatomic resolution, and had lower signal-to-noise ratios compared to modern conventional high field strength MRIs [41, 42]. Furthermore, low field strength MRIs did not provide the ability to perform more advanced imaging techniques such as diffusion-weighted imaging (DWI), DTI, magnetic resonance angiography (MRA), magnetic resonance spectroscopy (MRS), and functional (fMRI) imaging [43]. More recent advancements with higher field strength (1.5–3.0T) MRI systems address these shortcomings and have subsequently become an emerging tool in malignant brain tumor resection. The benefits of such an iMRI system not only provide for high-resolution multiplanar anatomic detail of intracranial tissues (and the same caliber as preoperative imaging), but also allow for these advanced imaging techniques.

iMRI has been shown to be an effective tool in improving neurosurgical outcomes while minimizing complications [44]. In one recent randomized controlled trial of adults with enhancing gliomas, 49 patients were analyzed after randomization to undergo conventional surgical resection or resection with the aid of intraoperative MRI [44]. Patients in the iMRI group had a significantly higher rate of complete tumor resection than the control group, while the rates of postoperative neurological deficits did not significantly differ [44]. Notably, in patients who underwent additional tumor resection based on the iMRI findings, none suffered neurological complications. Various case series have shown that iMRI results in improved rates of tumor resection [10, 31, 4557]. For example, Senft and colleagues demonstrated that in patients undergoing surgery for intended GTR of GBM, the use of iMRI leads to a significantly increased rate of complete tumor resection (100%), compared to patients who underwent resection without iMRI (61%) [54]. One study investigating the role of iMRI in GBM resection found that achieving a >98% resection was significantly associated with improved overall survival compared to resection of <98% of the tumor (median survival 14 months vs. 9 months) [10]. Hatiboglu et al. found that in a subset of their patients undergoing glioma resection, the use of iMRI followed by additional tumor resection improved the average extent of resection from 76 to 96% [45]. Likewise, in a series of nearly 300 patients, Kuhnt and colleagues found that the use of iMRI with subsequent additional tumor resection guided by the intraoperative images significantly improved the rate of GTR of gliomas. Additionally, they found using volumetric analysis that additional resection following iMRI leads to a significantly lower volume of residual tumor [46]. Others, however, have not shown similar benefits of iMRI. A recent but small randomized controlled trial comparing resection with standard neuronavigation to resection aided by low field iMRI found no significant differences with respect to extent of resection, clinical performance, and survival. However, the benefits of iMRI in this study may have been limited by the low-strength (0.15T) magnet used [58].

Despite these advantages, an iMRI system presents a number of logistical and safety challenges that must be addressed prior to clinical implementation. The first among these is the design and construction of a suitable operating room. iMRI systems require rooms with adequate radiofrequency shielding in order to prevent image artifact and magnetic shielding to protect equipment and patients outside the iMRI suite. Additionally, the rooms must be equipped with dedicated MR-compatible surgical and anesthesia equipment and must be large enough so that non-MRI-compatible equipment can be stored at a safe distance from the magnet while it is in use. Non-MRI-compatible equipment must be kept at a distance beyond the 5-gauss field line of the magnet while it is in use [59]. While the magnets themselves may be too deep to allow easy surgical access while the patient is positioned in the scanner, mobile systems, in which the MRI bore can be brought in and out of the operating room, circumvent this drawback [41]. Many modern iMRI suites house the MRI magnet in a separate room connected to the main operating area, and the magnet can be brought into the main operating room via tracks on the ceiling to center over the patient’s head (Fig. 4.3).

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Fig. 4.3
iMRI suite at Yale New Haven Hospital. Photograph taken from the operating room looking toward the garage that houses the iMRI (a). The patient has been sterilely draped, and the metal objects have been moved to safety. The magnet moves into the operating room, along a track system, allowing its use in two separate rooms. The magnet is centered over the patient’s head and ready for use (b)

Drawbacks to an iMRI system include the significant upfront expense of the MRI systems and constructing an MRI-compatible operating suite, not to mention availability of space to be specifically allocated to the suite which may not be possible at certain centers. Apart from the initial costs, and unlike iUS, these systems also require additional personnel, including MRI technicians, as well as additional traditional surgical staff to operate the MRI during an operation. Special anesthesia monitors are required. Older models of MRI-compatible head holders can be quite cumbersome and can prohibit positioning in the lateral or prone position, but newer iMRI systems and head holders have improved considerably to where this is amenable (Fig. 4.4). It is also important to note that the use of an iMRI system may be limited by metallic implants in the patient, such as old aneurysm clips or implanted defibrillators. An additional safety consideration is that obtaining an iMRI requires suspension of the surgical procedure in order to place the patient within the MRI scanner. The sterility of the surgical field must also be maintained throughout the imaging process. Relatively slow image acquisition time, coupled with the time it takes to prepare the patient and the room, results in relatively longer operating times than without imaging and, therefore, longer time under anesthesia. In the senior author’s experience, this time is typically approximately forty minutes. In patients with medical comorbidities, the benefits of obtaining intraoperative imaging must be weighed against the risks of additional operating and anesthesia time. In some patients, depending on the type and extent of their tumor in addition to their overall health and prognosis, it may be best to complete tumor resection without obtaining iMRI.

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Fig. 4.4
A more current version of the nonmetal, 3.0T iMRI-compatible head holder


Intraoperative Angiography (iA)


The use of cerebral angiography for brain tumors may be indicated when more detailed vascular information is needed to evaluate arteriovenous shunting, the relationship with major arterial and venous structures, coexisting vascular pathology within or in close vicinity of malignant tumors [60, 61]. Moreover, embolization of tumors can prove invaluable in tumor cases with a robust vascular supply that may be difficult to otherwise control during surgery. The one caveat with preoperative embolization of tumors, however, is that the sudden cutoff of the tumor’s blood supply can lead to an acute worsening of cerebral edema, rendering an immediate life-threatening situation for the patient. Tumor embolization may also cause hemorrhage in large tumors, also leading to acute herniation syndromes [62]. Thus, the removal of the skull flap and resection of the tumor immediately after embolization can be critical to relieve pressure, but these procedures are often performed at two separate locations in the most hospitals.

State-of-the-art operating rooms, however, allow for multiple modalities of diagnostic and intervention capabilities, namely iA and iMRI to coexist in the same room (i.e., hybrid rooms), thus allowing for the opportunity to maximize the success of surgery and patient safety. The accessibility of a biplanar imaging technology within a neurosurgical operating suite allows the neurosurgeon to have the ability to perform a diagnostic or therapeutic cerebral angiogram during or immediately before or after tumor resection. Patients may be anesthetized in the same operation suite, in the same setting, where life-threatening cerebral edema and risks of herniation can be controlled and prevented. Hybrid rooms provide the infrastructure to begin the craniotomy and tumor resection immediately after an embolization procedure, therefore reaping the benefits of eradicating the tumor blood supply, without the consequences. These adjuncts increase the safety, accuracy, and success of each procedure. One example of the success of such a hybrid room is exemplified in Fig. 4.5 in which a feeding artery aneurysm was found deep within a malignant brain tumor. Such an aneurysm would have been difficult to gain access to and control with conventional open surgery, and thus, the use of iA with embolization in a hybrid suite allowed for treatment of the aneurysm and removal of the tumor in the same operative setting.
Oct 17, 2017 | Posted by in NEUROLOGY | Comments Off on The Usefulness of Stereotactic Neuronavigation Along with Intraoperative Imaging in Malignant Brain Tumor Surgery

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