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Intraoperative MRI for High and Low Grade Gliomas
C H A P T E R
20 Intraoperative MRI for High and Low Grade Gliomas Tomas Garzon-Muvdi1, George Samandouras2 1
Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, MD, United States; 2Victor Horsley Department of Neurosurgery, The National Hospital for Neurology and Neurosurgery, Queen Square, London, United Kingdom
INTRODUCTION Extent of Resection of Gliomas and Outcome There are multiple well-established factors that are related to the outcome of patients with both high (HGGs) and low grade gliomas (LGGs). These factors include extent of resection (EOR), age of the patient, functional status, O6-methylguanine-DNA-methyltransferase (MGMT) methylation status, and mutation status of isocitrate dehydrogenase (IDH-1) (Chaichana, Parker, Olivi, & Quinones-Hinojosa, 2010; Juratli et al., 2012; Lacroix et al., 2001; Leibetseder et al., 2013; Stupp et al., 2005). There have been several ways of quantifying EOR ranging from surgeondetermined EOR, volumetric, and nonvolumetric analyses. Surgeon-determined EOR in glioma is unreliable with surgeons overestimating EOR when compared with postoperative imaging. In a prospective series of 111 patients with diagnosis of LGG, neurosurgeon-determined gross total resection (GTR) was inaccurate in approximately
Comprehensive Overview of Modern Surgical Approaches to Intrinsic Brain Tumors https://doi.org/10.1016/B978-0-12-811783-5.00020-3
59% of patients and also had increased risk of tumor progression (Shaw et al., 2008). Studies have been performed using nonvolumetric and volumetric analyses of the EOR in HGG patients. In nonvolumetric analyses, the EOR was divided arbitrarily into GTR, near total resection (NTR), and subtotal resection (STR). The majority of the studies where nonvolumetric analysis was performed showed that there was improvement in overall survival when GTR was achieved independent of other factors (Brown et al., 2008; Lamborn, Chang, & Prados, 2004; McGirt et al., 2009; Oszvald et al., 2012; Stark, Nabavi, Mehdorn, & Blomer, 2005). In the largest systematic review and metaanalysis by T. J. Brown et al. (2016), the authors show that GTR provides significant benefit in terms of survival and progression-free survival (PFS) as compared with STR in glioblastoma multiforme . Multiple groups also performed volumetric analysis of the EOR. Lacroix et al. (2001) measured the EOR volumetrically using pre- and postoperative MRIs retrospectively in 416 patients and demonstrated that there was a significant benefit when
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there was resection of 98% or greater of the tumor volume. Sanai et al. demonstrated that there was a survival benefit even with 78% EOR. Other studies have shown different thresholds of benefit with EOR (Chaichana et al., 2014; Orringer et al., 2012). In a study by K. L. Chaichana et al. (2014) the authors also concluded that in conjunction with EOR percentage, the residual volume was an important factor determining the benefit of survival for HGG patients. In the context of LGGs, EOR is also an important determinant of survival and PFS. In a retrospective analysis of 216 patients, Smith et al. found that improved outcomes are also determined by greater EOR. This study was performed by volumetric analysis of fluid attenuated inversion recovery (FLAIR) MRI imaging pre- and postoperatively (Smith et al., 2008). In another retrospective study where EOR was categorized as GTR, STR, and NTR, McGirt et al. (2008) concluded that GTR was associated with later tumor progression and improved survival. In a study comparing observation versus surgical resection in patients with LGG, early surgical resection was associated with improved survival (Jakola et al., 2012). Other studies and recommendations support the practice of attempting to increase EOR to improve outcomes for patients with LGGs (Aghi et al., 2015; Albert, Forsting, Sartor, Adams, & Kunze, 1994; Jungk et al., 2016). It is in this context where intraoperative MRI (iMRI) becomes extremely useful in the treatment of HGG and LGG, where it can provide updated, relatively real-time information accounting for the brain shift that has occurred during the initial part of the resection and also to assess EOR and presence of residual tumor. The latter is particularly useful for LGG because it is more difficult to determine tumor from nontumor tissue intraoperatively.
iMRI in Neurosurgery: Technical Concepts iMRI was introduced into neurosurgery to allow the surgeon to use neuronavigation with
TABLE 20.1
Advantages and Disadvantages of Intraoperative MRI
Advantages
Disadvantages
Allows update of neuronavigation systems after brain shift following dural opening and/or tumor resection
Cost of intraoperative MRI systems
Intraoperative evaluation to detect residual tumor
Increased operative time secondary to time needed for image acquisition
Increase in extent of resection of high and low grade gliomas
Need for special infrastructure and instruments in the operating room
Prevention of neurological injury
updated images and to assess EOR of brain tumors (Table 20.1). Its addition to the neurosurgical armamentarium to determine EOR and to eliminate the problem of brain shift after opening of the dura and volume loss from tumor resection has proved to be valuable. MRI technology has evolved significantly and image quality has improved with it (Kubben et al., 2011), thus enhancing extent of brain tumor resection and improving the outcomes for patients with HGG and LGG (Schneider et al., 2005). Tesla (T) is the standard unit of the magnetic flux density introduced in 1960 and equals to one weber per square meter. Based on general conventions, the following categories are identified: (1) ultralow field (<0.2 T), (2) low and midfield (0.3e1.0 T), (3) high field (1.0e3.0 T), (4) very high field (3.0e7.0 T), and (5) ultrahigh field (>7 T). For practical reasons, in the current chapter, low and high field iMRI systems are considered as <0.5 T and 1.5e3.0 T, respectively. As a reference, Earth’s magnetic field is 5 10 5 T. Shielding in the operating suite is required to prevent magnetic and radiofrequency interference (RFI) between the magnetic field and other magnetic or electrical devices, which can
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INTRODUCTION
degrade the quality of images, and to protect patients and personnel in the vicinity of the magnet. Low field magnets have a signal-to-noise ratio strongly dependent on the avoidance of RFI, and image quality is much more likely to be affected by external RFI. A typical method of shielding is to apply copper to shield the walls of the operating room. iMRI can be performed with platforms of different categories, depending on the strength of the magnetic field (Table 20.2). With increasing magnetic field strength comes better image quality. However, increasing magnetic field strength also comes with increased cost of TABLE 20.2 MRI Magnetic Field Strength
Advantages and Disadvantages of Different iMRI Field Strengths
Advantages
Disadvantages
• Poor image Ultralow • Mobile equipment quality field (<0.2 T) that can be transported into different operating rooms • No need for additional infrastructure or instruments • Inexpensive equipment compared with higher strength MRI Low field (0.5 T)
• Potential for performance of intraoperative electrophysiological monitoring during the surgery
High field (>1.5 T)
• High cost of the • Faster image acquisition time equipment • Optimal image quality • Need for • Greater variety of additional imaging sequences infrastructure • Improved imaging for • Surgery needs nonenhancing tumors to stop for image acquisition
T, tesla.
• Low image quality
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the MRI machine and the infrastructure needed in the operating room to support this technology. In the first report of the use of iMRI in the neurosurgical operating room in 1997, Black et al. (1997) used iMRI for the treatment of diverse intracranial and spinal lesions ranging from stereotactic biopsies to surgical resection of intrinsic brain tumors. Their system (GE Signa SP) used an open configuration 0.5 T MRI, termed the “double doughnut,” where the operating table was situated in a narrow place between two vertical magnets, which made patient positioning and surgeon’s mobility in the operating room limited. This system weighed 6000 kg and was installed in a room outside of the operating rooms (Hadani, 2011). Another group at the time, developed a 0.12 T low-field scanner called the PoleStar mobile iMRI system (Odin Medical Technologies and Medtronic, Inc.) that weighed 500 kg. This provided acceptable images and was easily merged into the operating room (Hadani, 2011). This system was capable of eliminating changes in navigation due to brain shift, and the image quality was sufficient to aid with tumor resection. Concurrently, a system was developed by Siemens (Magnetom Open) that was a 0.2 T MRI scanner with an open C-shaped configuration where the patient’s head was placed for image acquisition. In addition to the advantage of mobility of the iMRI scanner in low-field systems, it is possible to use regular operating instruments during the procedure with these systems. Because of the better image quality of highfield MRI scanners, the delineation of tumor margins is better. This is especially critical for nonenhancing tumors, namely LGGs. T2 and FLAIR sequences are typically more informative regarding tumor margins for nonenhancing tumors (Fig. 20.1). This increased image quality is associated with limited mobility of the MRI scanner and increased need for infrastructure and cost of installation. High-field iMRI systems are installed in specially built operating rooms, where the magnet moves toward the operating
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FIGURE 20.1
The use of intraoperative MRI (iMRI) for a patient with a low grade glioma. (A) Preoperative MRI demonstrating a left medial frontal mass that is nonenhancing with contrast and more conspicuous on T2 and T2 fluid attenuated inversion recovery (FLAIR) (left: sagittal T1 MRI with contrast, left middle: T2 axial, right middle: T2 FLAIR, right: axial T1 with contrast). (B) iMRI images showing adequate resection of the left medial frontal mass but with residual posteriorly into the supplementary motor cortex that was not identified during surgery (left: sagittal T2, right: axial T2). (C) Additional resection was pursued after the iMRI and postoperative image showing resection cavity with no residual T2 or T2 FLAIR hyperintensity (left: sagittal T1 MRI with contrast, left middle: T2 axial, right middle: T2 FLAIR, right: axial T1 with contrast).
table or the table moves into the magnet. They usually have a closed configuration of the magnetic bore and require special cranial fixation devices that are MRI compatible and that incorporate radiofrequency coils. The use of regular operating instruments is possible as long as they are outside the 5-G field; however, specialized iMRI-compatible instruments and anesthesia equipment have been developed. Some of the limitations of iMRI include its high cost and need for special infrastructure (Foroglou, Zamani, & Black, 2009). Additionally, the time necessary for acquisition of images extends the surgical time. Moreover, the detection
of residual tissue depends heavily on the radiological appearance of the tissue. For instance, in the case of contrast-enhancing HGG tumors, resection of contrast-enhancing tissue results in radiological GTR, but it is well known that residual neoplastic tissue and cells exist beyond the contrast enhancement due to tumor invasion that cannot be identified on current MRI protocols (Kubben et al., 2012). It is conceivable that with the combination of multiple intraoperative imaging modalities, EOR could be enhanced. However, this is only relevant if improved EOR leads to increased survival and better functional outcomes.
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INTRODUCTION
Role of iMRI in Surgery for Glial Neoplasms Gliomas are central nervous system (CNS) neoplasms that infiltrate the surrounding normal brain parenchyma. The invasive nature of gliomas muddles treatment of these tumors, and this characteristic is shared by LGGs (WHO grade II) and HGGs (WHO grades III and IV). Amassed evidence, mainly through retrospective studies, suggests that EOR is an important determinant of the outcome for patients with LGGs and HGGs (Chaichana et al., 2014; Lacroix et al., 2001; Lote et al., 1997; McGirt et al., 2008; McGirt et al., 2009; Nakamura et al., 2000). The methodology used to determine the tumor border with imaging techniques or intraoperative procedures is challenging because of the heterogeneity of gliomas and of their infiltrative nature even beyond contrast-enhancing regions. These infiltrative tumors are often indistinguishable from normal brain tissue during microsurgical resection. With the development and use of iMRI, improvement of neuronavigation and surgical technology can be enhanced (Table 20.3). iMRI enables the neurosurgeon to better define the tumor borders through updated neuronavigation after brain shift and intraoperative feedback after initial resection to assess EOR. This is possible due to the quality of images obtained during surgery; however, it is more time consuming and expensive than other intraoperative imaging modalities such as intraoperative ultrasound and fluorescence-guided surgery (Mahboob & Eljamel, 2017). According to a review by Mahboob and Eljamel (2017), iMRI provides similar rates of GTR when compared with intraoperative ultrasound and fluorescenceguided surgery. The estimated frequency of GTR with HGG achieved with iMRI was 70%, and the cost of resection of HGG with iMRI was of approximately $3625. In studies comparing iMRI versus neuronavigation alone in the resection of HGG, it was found that iMRI is associated with significantly greater
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frequency of EOR than with neuronavigation alone (Li, Qian, Niu, & Fu, 2017). Additionally, some studies have found that this increase in EOR is associated with increased survival (Eljamel & Mahboob, 2016). Randomized controlled trials assessing the role of iMRI in glioma surgery resulted in level I evidence that supports the use of iMRI in glioma surgery. Senft et al. (2011) enrolled 58 patients who were randomized to iMRI resection or neuronavigation alone, and they concluded that the use of iMRI resulted in a higher percentage of the patients with GTR in the iMRI cohort. They found that the use of iMRI improved PFS, but there was no difference in overall survival (Senft et al., 2011). In another study with 170 patients treated with high-field iMRI, Coburger, Wirtz, and Konig (2015) observed that rate of GTR and overall survival were better, whereas complication rates were lower than previously reported. However, in an additional randomized controlled trial that only included 14 patients designed to compare the role of iMRI versus neuronavigation, the authors concluded that there was no benefit in EOR or in survival for patients who had iMRI-guided surgery (Kubben et al., 2014). A major limitation of this study was that the authors utilized ultralow field MRI, suggesting that the use of high-field MRI is important for achieving greater EOR. In a literature review of iMRI studies for the resection of HGG, the authors conclude that the use of iMRI enhances EOR and leads to better PFS (Kubben et al., 2012). Other retrospective studies conclude that the use of iMRI is useful for achieving greater EOR in HGG (Bohinski et al., 2001; Kuhnt et al., 2011; Mahboob & Eljamel, 2017; Mohammadi et al., 2014). Studies evaluating the role of iMRI for treatment of LGG are not as prevalent as those for HGG. Nevertheless, the majority of the data support that iMRI also enhances EOR for LGGs. iMRI has an accuracy to detect residual tumor of 83% in LGG and proved to be more accurate than intraoperative ultrasound
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Studies Evaluating Role of iMRI in the Resection of Gliomas
Author
Year
Number of Patients
Pathology
Randomized Conclusion
Black et al.
1997
140
Various pathologies
No
iMRI is helpful in resection of tumors and optimizing surgical approach
Kubben et al.
2012
10
HGG
No
Absence of contrast enhancement is a bad predictor of absence of tumor
Li et al.
2017
Metaanalysis: 264-iMRI 249-conventional neuronavigation
HGG
No
iMRI results in greater EOR and improved PFS
Senft et al.
2011
58
HGG
Yes
iMRI enhances EOR
Coburger and Wirtz
2015
170
HGG
No
EOR and overall survival were improved, and complication rate was lower with iMRI
Kubben et al.
2014
14
HGG
Yes
No advantage when compared with neuronavigation alone
Bohinski et al.
2001
40
Glioma (WHO grade IIeIV)
No
Improvement in glioma volumetric resection
Kuhnt et al.
2011
135
HGG
No
iMRI enhances EOR and improves survival
Mohammadi et al.
2014
102
Enhancing and nonenhancing gliomas
No
iMRI improves EOR in all gliomas but particularly in nonenhancing gliomas
Schneider et al.
2001
Pala et al.
2016
33
LGG
No
iMRI is better at estimating residual tumor volume better than postoperative MRI
Roder et al.
2016
65
Pediatric LGG
No
Better EOR and PFS were achieved with iMRI
Roeder et al.
2014
117
HGG
No
iMRI is superior than 5-ALA and conventional microsurgery in enhancing EOR and PFS
Muragaki
2006
96
Glioma (WHO grade IeIV)
No
iMRI enhances EOR
EOR, extent of resection; HGG, high grade glioma; iMRI, intraoperative MRI; LGG, low grade glioma; PFS, progression-free survival; WHO, World Health Organization.
at detecting residual tumor. These findings were histologically corroborated (Coburger, Scheuerle, et al., 2015). In a retrospective study by Mohammadi et al. analyzing the role of
iMRI in the resection of nonenhancing gliomas, the authors found that this technology was especially useful for this radiological subset of tumors. In this study, patients who were found
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INTRODUCTION
to have residual tumor and whose tumor was not in eloquent regions of the brain, repeat resection was performed after iMRI, leading to a final tumor volume of 0.21 mL (Mohammadi et al., 2014). In a similar study, Schneider et al. (2001) studied 12 patients with nearly realtime imaging with 0.5 T iMRI. They were able to identify residual tumor after initial resection in some of their patients and were able to improve resection after iMRI imaging. The utility of iMRI has also been evaluated in pediatric patients with LGG (Giordano, Arraez, Samii, Samii, & Di Rocco, 2016). Some groups have even explored the utility of iMRI for
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assessment of EOR without subsequent resection, showing that iMRI provides a better volumetric estimate of the residual tumor, potentially changing the management strategy of patients with LGG depending on residual tumor volume and patient age (Pala et al., 2016). In a study by Roder et al. (2016) that evaluated the EOR and PFS in patients with LGG and iMRI, the authors found that use of iMRI resulted in better EOR and in improved PFS. Taken together, this evidence strongly suggests the use of iMRI for the resection of HGG and LGG as a means to improve EOR and subsequently PFS (Fig. 20.2).
FIGURE 20.2
Pre- and postoperative images of a low grade glioma resected with the assistance of intraoperative MRI. (A) Preoperative MRI demonstrating a right medial occipitoparietal mass that is hyperintense on T2 and T2 FLAIR imaging and nonenhancing (left: sagittal T1 with contrast, left middle: axial T2, right middle: T2 FLAIR, and right: axial T1 with contrast. (B) Intraoperative MRI images during resection of the right medial occipitoparietal mass that prompted further resection to remove residual T2 hyperintense tissue. There is residual medial and deep to the resection cavity (left: sagittal T2, middle: axial T2, right: axial FLAIR). (C) Postoperative MRI demonstrating gross total resection of right medial occipitoparietal mass (left: sagittal T1 MRI with contrast, left middle: T2 axial, right middle: T2 FLAIR, right: axial T1 with contrast).
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CONCLUSION Maximizing EOR in the treatment of gliomas has been shown to lead to enhanced prognosis through improving overall PFS. With the use of iMRI, the neurosurgeon has the ability to improve the accuracy of neuronavigation and to assess the EOR with an open craniotomy, thus allowing for resection of residual tumor tissue in the same surgical episode. Although this technology has proven to be valuable in the neurosurgical armamentarium, it comes with limitations such as increased cost and need for additional institutional infrastructure. As this technology is used with increasing frequency, we will learn how to better use it for the benefit of patients diagnosed with gliomas.
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Nakamura, M., Konishi, N., Tsunoda, S., Nakase, H., Tsuzuki, T., Aoki, H., … Sakaki, T. (2000). Analysis of prognostic and survival factors related to treatment of low-grade astrocytomas in adults. Oncology, 58(2), 108e116. https://doi.org/10.1159/000012087. Orringer, D., Lau, D., Khatri, S., Zamora-Berridi, G. J., Zhang, K., Wu, C., … Sagher, O. (2012). Extent of resection in patients with glioblastoma: Limiting factors, perception of resectability, and effect on survival. Journal of Neurosurgery, 117(5), 851e859. https://doi.org/10.3171/2012.8.JNS12234. Oszvald, A., Guresir, E., Setzer, M., Vatter, H., Senft, C., Seifert, V., & Franz, K. (2012). Glioblastoma therapy in the elderly and the importance of the extent of resection regardless of age. Journal of Neurosurgery, 116(2), 357e364. https://doi.org/10.3171/2011.8.JNS102114. Pala, A., Brand, C., Kapapa, T., Hlavac, M., Konig, R., Schmitz, B., … Coburger, J. (2016). The value of intraoperative and early postoperative magnetic resonance imaging in low-grade glioma surgery: A retrospective study. World Neurosurgery, 93, 191e197. https://doi.org/ 10.1016/j.wneu.2016.04.120. Roder, C., Bisdas, S., Ebner, F. H., Honegger, J., Naegele, T., Ernemann, U., & Tatagiba, M. (2014). Maximizing the extent of resection and survival benefit of patients in glioblastoma surgery: high-field iMRI versus conventional and 5-ALA-assisted surgery. Eur J Surg Oncol, 40, 297e304. https://doi.org/10.1016/j.ejso.2013.11.022. Roder, C., Breitkopf, M., Bisdas, S., Freitas Rda, S., Dimostheni, A., … Schuhmann, M. U. (2016). Beneficial impact of high-field intraoperative magnetic resonance imaging on the efficacy of pediatric low-grade glioma surgery. Neurosurgical Focus, 40(3), E13. https:// doi.org/10.3171/2015.11.FOCUS15530. Schneider, J. P., Schulz, T., Schmidt, F., Dietrich, J., Lieberenz, S., Trantakis, C., … Kahn, T. (2001). Gross-total surgery of supratentorial low-grade gliomas under intraoperative MR guidance. American Journal of Neuroradiology, 22(1), 89e98.
Schneider, J. P., Trantakis, C., Rubach, M., Schulz, T., Dietrich, J., Winkler, D., … Kahn, T. (2005). Intraoperative MRI to guide the resection of primary supratentorial glioblastoma multiformeea quantitative radiological analysis. Neuroradiology, 47(7), 489e500. https://doi.org/10.1007/ s00234-005-1397-1. Senft, C., Bink, A., Franz, K., Vatter, H., Gasser, T., & Seifert, V. (2011). Intraoperative MRI guidance and extent of resection in glioma surgery: A randomised, controlled trial. The Lancet Oncology, 12(11), 997e1003. https://doi.org/10.1016/ S1470-2045(11)70196-6. Shaw, E. G., Berkey, B., Coons, S. W., Bullard, D., Brachman, D., Buckner, J. C., … Mehta, M. (2008). Recurrence following neurosurgeon-determined gross-total resection of adult supratentorial low-grade glioma: Results of a prospective clinical trial. Journal of Neurosurgery, 109(5), 835e841. https://doi.org/10.3171/JNS/ 2008/109/11/0835. Smith, J. S., Chang, E. F., Lamborn, K. R., Chang, S. M., Prados, M. D., Cha, S., … Berger, M. S. (2008). Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. Journal of Clinical Oncology, 26(8), 1338e1345. https://doi.org/10.1200/ JCO.2007.13.9337. Stark, A. M., Nabavi, A., Mehdorn, H. M., & Blomer, U. (2005). Glioblastoma multiforme-report of 267 cases treated at a single institution. Surgical Neurology, 63(2), 162e169. https://doi.org/10.1016/j.surneu.2004.01.028. Discussion 169. Stupp, R., Mason, W. P., van den Bent, M. J., Weller, M., Fisher, B., Taphoorn, M. J., … National Cancer Institute of Canada Clinical Trials Group. (2005). Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. The New England Journal of Medicine, 352(10), 987e996. https://doi.org/10.1056/NEJMoa043330.
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20 Intraoperative MRI for High and Low Grade Gliomas Tomas Garzon-Muvdi1, George Samandouras2 1
Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, MD, United States; 2Victor Horsley Department of Neurosurgery, The National Hospital for Neurology and Neurosurgery, Queen Square, London, United Kingdom
INTRODUCTION Extent of Resection of Gliomas and Outcome There are multiple well-established factors that are related to the outcome of patients with both high (HGGs) and low grade gliomas (LGGs). These factors include extent of resection (EOR), age of the patient, functional status, O6-methylguanine-DNA-methyltransferase (MGMT) methylation status, and mutation status of isocitrate dehydrogenase (IDH-1) (Chaichana, Parker, Olivi, & Quinones-Hinojosa, 2010; Juratli et al., 2012; Lacroix et al., 2001; Leibetseder et al., 2013; Stupp et al., 2005). There have been several ways of quantifying EOR ranging from surgeondetermined EOR, volumetric, and nonvolumetric analyses. Surgeon-determined EOR in glioma is unreliable with surgeons overestimating EOR when compared with postoperative imaging. In a prospective series of 111 patients with diagnosis of LGG, neurosurgeon-determined gross total resection (GTR) was inaccurate in approximately
Comprehensive Overview of Modern Surgical Approaches to Intrinsic Brain Tumors https://doi.org/10.1016/B978-0-12-811783-5.00020-3
59% of patients and also had increased risk of tumor progression (Shaw et al., 2008). Studies have been performed using nonvolumetric and volumetric analyses of the EOR in HGG patients. In nonvolumetric analyses, the EOR was divided arbitrarily into GTR, near total resection (NTR), and subtotal resection (STR). The majority of the studies where nonvolumetric analysis was performed showed that there was improvement in overall survival when GTR was achieved independent of other factors (Brown et al., 2008; Lamborn, Chang, & Prados, 2004; McGirt et al., 2009; Oszvald et al., 2012; Stark, Nabavi, Mehdorn, & Blomer, 2005). In the largest systematic review and metaanalysis by T. J. Brown et al. (2016), the authors show that GTR provides significant benefit in terms of survival and progression-free survival (PFS) as compared with STR in glioblastoma multiforme . Multiple groups also performed volumetric analysis of the EOR. Lacroix et al. (2001) measured the EOR volumetrically using pre- and postoperative MRIs retrospectively in 416 patients and demonstrated that there was a significant benefit when
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Copyright © 2019 Elsevier Inc. All rights reserved.
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there was resection of 98% or greater of the tumor volume. Sanai et al. demonstrated that there was a survival benefit even with 78% EOR. Other studies have shown different thresholds of benefit with EOR (Chaichana et al., 2014; Orringer et al., 2012). In a study by K. L. Chaichana et al. (2014) the authors also concluded that in conjunction with EOR percentage, the residual volume was an important factor determining the benefit of survival for HGG patients. In the context of LGGs, EOR is also an important determinant of survival and PFS. In a retrospective analysis of 216 patients, Smith et al. found that improved outcomes are also determined by greater EOR. This study was performed by volumetric analysis of fluid attenuated inversion recovery (FLAIR) MRI imaging pre- and postoperatively (Smith et al., 2008). In another retrospective study where EOR was categorized as GTR, STR, and NTR, McGirt et al. (2008) concluded that GTR was associated with later tumor progression and improved survival. In a study comparing observation versus surgical resection in patients with LGG, early surgical resection was associated with improved survival (Jakola et al., 2012). Other studies and recommendations support the practice of attempting to increase EOR to improve outcomes for patients with LGGs (Aghi et al., 2015; Albert, Forsting, Sartor, Adams, & Kunze, 1994; Jungk et al., 2016). It is in this context where intraoperative MRI (iMRI) becomes extremely useful in the treatment of HGG and LGG, where it can provide updated, relatively real-time information accounting for the brain shift that has occurred during the initial part of the resection and also to assess EOR and presence of residual tumor. The latter is particularly useful for LGG because it is more difficult to determine tumor from nontumor tissue intraoperatively.
iMRI in Neurosurgery: Technical Concepts iMRI was introduced into neurosurgery to allow the surgeon to use neuronavigation with
TABLE 20.1
Advantages and Disadvantages of Intraoperative MRI
Advantages
Disadvantages
Allows update of neuronavigation systems after brain shift following dural opening and/or tumor resection
Cost of intraoperative MRI systems
Intraoperative evaluation to detect residual tumor
Increased operative time secondary to time needed for image acquisition
Increase in extent of resection of high and low grade gliomas
Need for special infrastructure and instruments in the operating room
Prevention of neurological injury
updated images and to assess EOR of brain tumors (Table 20.1). Its addition to the neurosurgical armamentarium to determine EOR and to eliminate the problem of brain shift after opening of the dura and volume loss from tumor resection has proved to be valuable. MRI technology has evolved significantly and image quality has improved with it (Kubben et al., 2011), thus enhancing extent of brain tumor resection and improving the outcomes for patients with HGG and LGG (Schneider et al., 2005). Tesla (T) is the standard unit of the magnetic flux density introduced in 1960 and equals to one weber per square meter. Based on general conventions, the following categories are identified: (1) ultralow field (<0.2 T), (2) low and midfield (0.3e1.0 T), (3) high field (1.0e3.0 T), (4) very high field (3.0e7.0 T), and (5) ultrahigh field (>7 T). For practical reasons, in the current chapter, low and high field iMRI systems are considered as <0.5 T and 1.5e3.0 T, respectively. As a reference, Earth’s magnetic field is 5 10 5 T. Shielding in the operating suite is required to prevent magnetic and radiofrequency interference (RFI) between the magnetic field and other magnetic or electrical devices, which can
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INTRODUCTION
degrade the quality of images, and to protect patients and personnel in the vicinity of the magnet. Low field magnets have a signal-to-noise ratio strongly dependent on the avoidance of RFI, and image quality is much more likely to be affected by external RFI. A typical method of shielding is to apply copper to shield the walls of the operating room. iMRI can be performed with platforms of different categories, depending on the strength of the magnetic field (Table 20.2). With increasing magnetic field strength comes better image quality. However, increasing magnetic field strength also comes with increased cost of TABLE 20.2 MRI Magnetic Field Strength
Advantages and Disadvantages of Different iMRI Field Strengths
Advantages
Disadvantages
• Poor image Ultralow • Mobile equipment quality field (<0.2 T) that can be transported into different operating rooms • No need for additional infrastructure or instruments • Inexpensive equipment compared with higher strength MRI Low field (0.5 T)
• Potential for performance of intraoperative electrophysiological monitoring during the surgery
High field (>1.5 T)
• High cost of the • Faster image acquisition time equipment • Optimal image quality • Need for • Greater variety of additional imaging sequences infrastructure • Improved imaging for • Surgery needs nonenhancing tumors to stop for image acquisition
T, tesla.
• Low image quality
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the MRI machine and the infrastructure needed in the operating room to support this technology. In the first report of the use of iMRI in the neurosurgical operating room in 1997, Black et al. (1997) used iMRI for the treatment of diverse intracranial and spinal lesions ranging from stereotactic biopsies to surgical resection of intrinsic brain tumors. Their system (GE Signa SP) used an open configuration 0.5 T MRI, termed the “double doughnut,” where the operating table was situated in a narrow place between two vertical magnets, which made patient positioning and surgeon’s mobility in the operating room limited. This system weighed 6000 kg and was installed in a room outside of the operating rooms (Hadani, 2011). Another group at the time, developed a 0.12 T low-field scanner called the PoleStar mobile iMRI system (Odin Medical Technologies and Medtronic, Inc.) that weighed 500 kg. This provided acceptable images and was easily merged into the operating room (Hadani, 2011). This system was capable of eliminating changes in navigation due to brain shift, and the image quality was sufficient to aid with tumor resection. Concurrently, a system was developed by Siemens (Magnetom Open) that was a 0.2 T MRI scanner with an open C-shaped configuration where the patient’s head was placed for image acquisition. In addition to the advantage of mobility of the iMRI scanner in low-field systems, it is possible to use regular operating instruments during the procedure with these systems. Because of the better image quality of highfield MRI scanners, the delineation of tumor margins is better. This is especially critical for nonenhancing tumors, namely LGGs. T2 and FLAIR sequences are typically more informative regarding tumor margins for nonenhancing tumors (Fig. 20.1). This increased image quality is associated with limited mobility of the MRI scanner and increased need for infrastructure and cost of installation. High-field iMRI systems are installed in specially built operating rooms, where the magnet moves toward the operating
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FIGURE 20.1
The use of intraoperative MRI (iMRI) for a patient with a low grade glioma. (A) Preoperative MRI demonstrating a left medial frontal mass that is nonenhancing with contrast and more conspicuous on T2 and T2 fluid attenuated inversion recovery (FLAIR) (left: sagittal T1 MRI with contrast, left middle: T2 axial, right middle: T2 FLAIR, right: axial T1 with contrast). (B) iMRI images showing adequate resection of the left medial frontal mass but with residual posteriorly into the supplementary motor cortex that was not identified during surgery (left: sagittal T2, right: axial T2). (C) Additional resection was pursued after the iMRI and postoperative image showing resection cavity with no residual T2 or T2 FLAIR hyperintensity (left: sagittal T1 MRI with contrast, left middle: T2 axial, right middle: T2 FLAIR, right: axial T1 with contrast).
table or the table moves into the magnet. They usually have a closed configuration of the magnetic bore and require special cranial fixation devices that are MRI compatible and that incorporate radiofrequency coils. The use of regular operating instruments is possible as long as they are outside the 5-G field; however, specialized iMRI-compatible instruments and anesthesia equipment have been developed. Some of the limitations of iMRI include its high cost and need for special infrastructure (Foroglou, Zamani, & Black, 2009). Additionally, the time necessary for acquisition of images extends the surgical time. Moreover, the detection
of residual tissue depends heavily on the radiological appearance of the tissue. For instance, in the case of contrast-enhancing HGG tumors, resection of contrast-enhancing tissue results in radiological GTR, but it is well known that residual neoplastic tissue and cells exist beyond the contrast enhancement due to tumor invasion that cannot be identified on current MRI protocols (Kubben et al., 2012). It is conceivable that with the combination of multiple intraoperative imaging modalities, EOR could be enhanced. However, this is only relevant if improved EOR leads to increased survival and better functional outcomes.
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INTRODUCTION
Role of iMRI in Surgery for Glial Neoplasms Gliomas are central nervous system (CNS) neoplasms that infiltrate the surrounding normal brain parenchyma. The invasive nature of gliomas muddles treatment of these tumors, and this characteristic is shared by LGGs (WHO grade II) and HGGs (WHO grades III and IV). Amassed evidence, mainly through retrospective studies, suggests that EOR is an important determinant of the outcome for patients with LGGs and HGGs (Chaichana et al., 2014; Lacroix et al., 2001; Lote et al., 1997; McGirt et al., 2008; McGirt et al., 2009; Nakamura et al., 2000). The methodology used to determine the tumor border with imaging techniques or intraoperative procedures is challenging because of the heterogeneity of gliomas and of their infiltrative nature even beyond contrast-enhancing regions. These infiltrative tumors are often indistinguishable from normal brain tissue during microsurgical resection. With the development and use of iMRI, improvement of neuronavigation and surgical technology can be enhanced (Table 20.3). iMRI enables the neurosurgeon to better define the tumor borders through updated neuronavigation after brain shift and intraoperative feedback after initial resection to assess EOR. This is possible due to the quality of images obtained during surgery; however, it is more time consuming and expensive than other intraoperative imaging modalities such as intraoperative ultrasound and fluorescence-guided surgery (Mahboob & Eljamel, 2017). According to a review by Mahboob and Eljamel (2017), iMRI provides similar rates of GTR when compared with intraoperative ultrasound and fluorescenceguided surgery. The estimated frequency of GTR with HGG achieved with iMRI was 70%, and the cost of resection of HGG with iMRI was of approximately $3625. In studies comparing iMRI versus neuronavigation alone in the resection of HGG, it was found that iMRI is associated with significantly greater
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frequency of EOR than with neuronavigation alone (Li, Qian, Niu, & Fu, 2017). Additionally, some studies have found that this increase in EOR is associated with increased survival (Eljamel & Mahboob, 2016). Randomized controlled trials assessing the role of iMRI in glioma surgery resulted in level I evidence that supports the use of iMRI in glioma surgery. Senft et al. (2011) enrolled 58 patients who were randomized to iMRI resection or neuronavigation alone, and they concluded that the use of iMRI resulted in a higher percentage of the patients with GTR in the iMRI cohort. They found that the use of iMRI improved PFS, but there was no difference in overall survival (Senft et al., 2011). In another study with 170 patients treated with high-field iMRI, Coburger, Wirtz, and Konig (2015) observed that rate of GTR and overall survival were better, whereas complication rates were lower than previously reported. However, in an additional randomized controlled trial that only included 14 patients designed to compare the role of iMRI versus neuronavigation, the authors concluded that there was no benefit in EOR or in survival for patients who had iMRI-guided surgery (Kubben et al., 2014). A major limitation of this study was that the authors utilized ultralow field MRI, suggesting that the use of high-field MRI is important for achieving greater EOR. In a literature review of iMRI studies for the resection of HGG, the authors conclude that the use of iMRI enhances EOR and leads to better PFS (Kubben et al., 2012). Other retrospective studies conclude that the use of iMRI is useful for achieving greater EOR in HGG (Bohinski et al., 2001; Kuhnt et al., 2011; Mahboob & Eljamel, 2017; Mohammadi et al., 2014). Studies evaluating the role of iMRI for treatment of LGG are not as prevalent as those for HGG. Nevertheless, the majority of the data support that iMRI also enhances EOR for LGGs. iMRI has an accuracy to detect residual tumor of 83% in LGG and proved to be more accurate than intraoperative ultrasound
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352 TABLE 20.3
20. INTRAOPERATIVE MRI FOR HIGH AND LOW GRADE GLIOMAS
Studies Evaluating Role of iMRI in the Resection of Gliomas
Author
Year
Number of Patients
Pathology
Randomized Conclusion
Black et al.
1997
140
Various pathologies
No
iMRI is helpful in resection of tumors and optimizing surgical approach
Kubben et al.
2012
10
HGG
No
Absence of contrast enhancement is a bad predictor of absence of tumor
Li et al.
2017
Metaanalysis: 264-iMRI 249-conventional neuronavigation
HGG
No
iMRI results in greater EOR and improved PFS
Senft et al.
2011
58
HGG
Yes
iMRI enhances EOR
Coburger and Wirtz
2015
170
HGG
No
EOR and overall survival were improved, and complication rate was lower with iMRI
Kubben et al.
2014
14
HGG
Yes
No advantage when compared with neuronavigation alone
Bohinski et al.
2001
40
Glioma (WHO grade IIeIV)
No
Improvement in glioma volumetric resection
Kuhnt et al.
2011
135
HGG
No
iMRI enhances EOR and improves survival
Mohammadi et al.
2014
102
Enhancing and nonenhancing gliomas
No
iMRI improves EOR in all gliomas but particularly in nonenhancing gliomas
Schneider et al.
2001
Pala et al.
2016
33
LGG
No
iMRI is better at estimating residual tumor volume better than postoperative MRI
Roder et al.
2016
65
Pediatric LGG
No
Better EOR and PFS were achieved with iMRI
Roeder et al.
2014
117
HGG
No
iMRI is superior than 5-ALA and conventional microsurgery in enhancing EOR and PFS
Muragaki
2006
96
Glioma (WHO grade IeIV)
No
iMRI enhances EOR
EOR, extent of resection; HGG, high grade glioma; iMRI, intraoperative MRI; LGG, low grade glioma; PFS, progression-free survival; WHO, World Health Organization.
at detecting residual tumor. These findings were histologically corroborated (Coburger, Scheuerle, et al., 2015). In a retrospective study by Mohammadi et al. analyzing the role of
iMRI in the resection of nonenhancing gliomas, the authors found that this technology was especially useful for this radiological subset of tumors. In this study, patients who were found
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INTRODUCTION
to have residual tumor and whose tumor was not in eloquent regions of the brain, repeat resection was performed after iMRI, leading to a final tumor volume of 0.21 mL (Mohammadi et al., 2014). In a similar study, Schneider et al. (2001) studied 12 patients with nearly realtime imaging with 0.5 T iMRI. They were able to identify residual tumor after initial resection in some of their patients and were able to improve resection after iMRI imaging. The utility of iMRI has also been evaluated in pediatric patients with LGG (Giordano, Arraez, Samii, Samii, & Di Rocco, 2016). Some groups have even explored the utility of iMRI for
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assessment of EOR without subsequent resection, showing that iMRI provides a better volumetric estimate of the residual tumor, potentially changing the management strategy of patients with LGG depending on residual tumor volume and patient age (Pala et al., 2016). In a study by Roder et al. (2016) that evaluated the EOR and PFS in patients with LGG and iMRI, the authors found that use of iMRI resulted in better EOR and in improved PFS. Taken together, this evidence strongly suggests the use of iMRI for the resection of HGG and LGG as a means to improve EOR and subsequently PFS (Fig. 20.2).
FIGURE 20.2
Pre- and postoperative images of a low grade glioma resected with the assistance of intraoperative MRI. (A) Preoperative MRI demonstrating a right medial occipitoparietal mass that is hyperintense on T2 and T2 FLAIR imaging and nonenhancing (left: sagittal T1 with contrast, left middle: axial T2, right middle: T2 FLAIR, and right: axial T1 with contrast. (B) Intraoperative MRI images during resection of the right medial occipitoparietal mass that prompted further resection to remove residual T2 hyperintense tissue. There is residual medial and deep to the resection cavity (left: sagittal T2, middle: axial T2, right: axial FLAIR). (C) Postoperative MRI demonstrating gross total resection of right medial occipitoparietal mass (left: sagittal T1 MRI with contrast, left middle: T2 axial, right middle: T2 FLAIR, right: axial T1 with contrast).
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20. INTRAOPERATIVE MRI FOR HIGH AND LOW GRADE GLIOMAS
CONCLUSION Maximizing EOR in the treatment of gliomas has been shown to lead to enhanced prognosis through improving overall PFS. With the use of iMRI, the neurosurgeon has the ability to improve the accuracy of neuronavigation and to assess the EOR with an open craniotomy, thus allowing for resection of residual tumor tissue in the same surgical episode. Although this technology has proven to be valuable in the neurosurgical armamentarium, it comes with limitations such as increased cost and need for additional institutional infrastructure. As this technology is used with increasing frequency, we will learn how to better use it for the benefit of patients diagnosed with gliomas.
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Brown, P. D., Decker, P. A., Rummans, T. A., Clark, M. M., Frost, M. H., Ballman, K. V., … Buckner, J. C. (2008). A prospective study of quality of life in adults with newly diagnosed high-grade gliomas: Comparison of patient and caregiver ratings of quality of life. American Journal of Clinical Oncology, 31(2), 163e168. https://doi.org/ 10.1097/COC.0b013e318149f1d3. Brown, T. J., Brennan, M. C., Li, M., Church, E. W., Brandmeir, N. J., Rakszawski, K. L., … Glantz, M. (2016). Association of the extent of resection with survival in glioblastoma: A systematic review and meta-analysis. JAMA Oncology, 2(11), 1460e1469. https://doi.org/ 10.1001/jamaoncol.2016.1373. Chaichana, K., Parker, S., Olivi, A., & Quinones-Hinojosa, A. (2010). A proposed classification system that projects outcomes based on preoperative variables for adult patients with glioblastoma multiforme. Journal of Neurosurgery, 112(5), 997e1004. https://doi.org/10.3171/2009.9.JNS09805. Chaichana, K. L., Jusue-Torres, I., Navarro-Ramirez, R., Raza, S. M., Pascual-Gallego, M., Ibrahim, A., … Quinones-Hinojosa, A. (2014). Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro-Oncology, 16(1), 113e122. https://doi.org/10.1093/neuonc/not137. Coburger, J., Scheuerle, A., Thal, D. R., Engelke, J., Hlavac, M., Wirtz, C. R., & Konig, R. (2015). Linear array ultrasound in low-grade glioma surgery: Histology-based assessment of accuracy in comparison to conventional intraoperative ultrasound and intraoperative MRI. Acta Neurochirurgica (Wien), 157(2), 195e206. https:// doi.org/10.1007/s00701-014-2314-3. Coburger, J., Wirtz, C. R., & Konig, R. W. (2015b). Impact of extent of resection and recurrent surgery on clinical outcome and overall survival in a consecutive series of 170 patients for glioblastoma in intraoperative high field iMRI. Journal of Neurosurgical Sciences, 61(3), 233e244. https://doi.org/10.23736/S0390-5616.16.03284-7. Eljamel, M. S., & Mahboob, S. O. (2016). The effectiveness and cost-effectiveness of intraoperative imaging in high-grade glioma resection; a comparative review of intraoperative ALA, fluorescein, ultrasound and MRI. Photodiagnosis and Photodynamic Therapy, 16, 35e43. https://doi.org/ 10.1016/j.pdpdt.2016.07.012. Foroglou, N., Zamani, A., & Black, P. (2009). Intra-operative MRI (iop-MR) for brain tumour surgery. British Journal of Neurosurgery, 23(1), 14e22. https://doi.org/10.1080/ 02688690802610587. Giordano, M., Arraez, C., Samii, A., Samii, M., & Di Rocco, C. (2016). Neurosurgical tools to extend tumor resection in pediatric hemispheric low-grade gliomas: iMRI. Child’s Nervous System, 32(10), 1915e1922. https://doi.org/ 10.1007/s00381-016-3177-0.
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