Fluorescence-Guided Surgery, Intraoperative Imaging, and Brain Mapping (iMRI, DTI, and Cortical Mapping)

16 Fluorescence-Guided Surgery, Intraoperative Imaging, and Brain Mapping (iMRI, DTI, and Cortical Mapping)


Jan Coburger and Philippe Schucht


Abstract
Intraoperative MRI (iMRI) and intraoperative mapping/monitoring (IOM) have synergistic effects on fluorescence-guided surgery (FGS). iMRI has been shown to increase the extent of resection (EOR) of brain tumors, particularly high-grade gliomas. In combination with FGS, iMRI may identify tumor tissue undetected by FGS, with tumor tissue hidden in a surgical operculum or behind a nonfluorescent tissue layer. Diffusion tenser imaging helps estimate the location of essential tracts, such as the arcuate fascicle or the corticospinal tract, which is of particular interest in FGS as 5-aminolevulinic acid (5-ALA) induced fluorescence does not differentiate between eloquent and noneloquent areas. Ultimately, IOM have become an indispensable part of surgery, especially in FGS. Due to the higher sensitivity of 5-ALA-induced fluorescence compared to MRI gadolinium contrast enhancement, FGS can lead to tumor resections beyond the preoperative gadolinium-enhanced T1 imaging, bringing presumed-eloquent structures into harm’s way. By clarifying whether these presumed eloquent, fluorescent tissue remnants actually harbor eloquent function, IOM, in the hands of the experienced neurosurgeon, can be used to safely increase the EOR in addition to protecting neurological function. Combining safety- and resection-enhancing intraoperative technologies (IOM and FGS) has been shown to result in more extensive resections, leading to a higher success rate of gross total resections, while simultaneously improving neurological outcome. Continuous dynamic mapping has evolved as a safe, ergonomic, and time-efficient strategy of IOM and hence has become the new benchmark of intraoperative function protection.


Keywords: intraoperative imaging, iMRI, DTI, IOM, motor mapping, continuous dynamic mapping


16.1 Fluorescence-Guided Surgery and Intraoperative MRI


Many authors refer to intraoperative magnetic resonance imaging (iMRI) as the “gold standard” of intraoperative imaging techniques in brain tumor surgery since it allows for a classical tomographical image of the whole brain during surgery. iMRI shows a detailed depiction of soft tissue. Further, additionally available sequences similar to standard diagnostic MRI host a broad range of indications from intra- and extra-axial lesions up to vascular malformations and functional imaging.


16.1.1 Principles of Intraoperative MRI


The basic idea for development of iMRI was the issue of intraoperative brain shift due to cerebrospinal fluid loss, tumor resection, and tissue edema leading to an increasing error of neuronavigation during surgery.1,2 The first iMRI systems were so-called open scanners or double donut scanners (image Fig. 16.1).3 Surgeons were operating in between the magnetic coils. Based on this configuration, it was only feasible to perform surgery using low magnetic field strength significantly below 1 T. Pre- and postoperative imaging, however, is routinely performed on a 1.5 or even 3-T magnet usually referred to as high-field MRIs. Thus, based on the low field strength, image quality was not comparable to standard diagnostic imaging. Scanning time is long and the number of available sequences is limited on a low-field iMRI. Nevertheless, early data from low-field iMRI-assisted surgeries showed a safe application and a significant benefit of extent of resection (EOR) based on the chance of an intraoperative scan especially for glioma patients.4,5,6,7 Using a low-field iMRI as well, Senft et al performed a randomized controlled trial (RCT) assessing iMRI assisted versus conventional microsurgical resection in patients with glioblastoma (GBM) tumors eligible for a gross total resection (GTR). The authors showed a significantly increased rate of GTR in the iMRI group leading to an increased progression-free survival (PFS) for those patients.8 The data are monocentric and show a considerably lower case number as in the 5-aminolevulinic acid (5-ALA) trial by Stummer et al.9 However, Senft et al provide the first study with level-one evidence supporting the benefit of iMRI. Additionally, the importance of GTR as a crucial prognostic factor was emphasized. High-field iMRI systems require dedicated operating rooms (OR) with magnetic shielding and a 5-Gauss safety zone around the scanner (image Fig. 16.2). For an intraoperative scan, the patient is positioned in a dedicated head coil that allows for a sharp fixation of the patient’s head using three or more pins (image Fig. 16.3). Most available head holders are flexible. However, patient positioning is limited when using high-field iMRI. Certain standard positions like park bench or sitting/semi-sitting positions are not possible. For high-field intraoperative MRI, most standard radiological diagnostic MRI scanners are used inside the OR. Thus, in contrast to low-field iMRI due to the significantly higher magnetic field, the surgery has to be performed distant from the magnet and a scan during surgery requires a transfer of the patient into the scanner as shown in image Fig. 16.4. Due to the increased image acquisition speed in the high-field MRI, the overall workflow is improved compared to low-field iMRI.10 Some centers even use the intraoperative MRI in a two-room solution for routine diagnostic imaging and intraoperative imaging for brain tumors (image Fig. 16.5).11





The development of high-field iMRI (1.5 and 3.0 T) allows for comparable image quality and similar available sequences as in routine diagnostic MRI. Tumor depiction is similar to preoperative imaging. image Fig. 16.6 shows a T1 MPRAGE sequence with contrast from an intraoperative scan with the skull open. Assessment of images is simplified, and better depiction of residual tumor is possible due to increased image resolution during glioma and pituitary surgery when compared to low-field imaging.10 The rate of GTR in low-grade gliomas was found to be increased in a retrospective multicenter series when a high-field iMRI was used instead of a low-field iMRI.12 Further, advances in diagnostic imaging can usually be translated to intraoperative use.


16.1.2 Intraoperative Diffusion Tenser Imaging and Its Clinical Implications


During glioma surgery, high-field iMRI allows for intraoperative functional imaging sequences that can be of high surgical value. Especially relevant in this regard is the acquisition of diffusion tenser imaging (DTI) data.13 Based on this MRI sequence, a probabilistic or deterministic fiber tracking of functional relevant cerebral tracts like the corticospinal tract (CST), arcuate fascicle, or optic radiation can be performed preoperatively and integrated in the neuronavigation system.14,15 Using high-field iMRI, these data can be updated intraoperatively. It has been shown that due to intraoperative brain shift, a significant change of the position of crucial tracts like the CST can occur.16 image Fig. 16.7 shows an intraoperative example of shift of the CST that was verified by intraoperative subcortical mapping. iMRI-based intraoperative tractography shows a high sensitivity localizing the CST.17 However, intraoperative DTI imaging data can be disturbed by artifacts surgeons should be aware of. Especially in superficial locations or in resection cavities that cannot be filled with saline properly during the iMRI scan, the air to brain interface can distort DTI images significantly.18 Thus, a combined use of subcortical mapping of the CST and an intraoperative update of DTI images using iMRI is the method of choice to maximize safety for patients.






16.1.3 Intraoperative Functional Imaging


Additional MRI sequences beyond gadolinium-diethylenetriamine pentaacetic acid (Gd-DTPA) enhanced T1, T2, FLAIR, and diffusion-weighted imaging (DWI) are perfusion-weighted imaging (PWI) and MRI spectroscopy. Both methods are of significant value in diagnostic imaging but can also be used to detect residual tumor intraoperatively.19,20 image Fig. 16.8 shows an example of intraoperative PWI compared to preoperative diagnostic imaging and amino acid PET (AA-PET) imaging. Even resting state connectivity networks were assessed intraoperatively in a first pilot study during general anesthesia, proving very interesting future perspective for functional imaging in patients with eloquent gliomas.21



16.1.4 Limitations of Intraoperative MRI


Concerning surgical workflow, an intraoperative MRI scan is time consuming, especially if additional diagnostic sequences beyond the routine are performed. Further, repetitive administration of Gd-DTPA leads to a nonspecific parenchymal enhancement. Surgical induced changes in T2 might further lead to a decrease of specificity after repetitive scans.22 Thus, while theoretically a GTR should be possible using iMRI as the gold standard of intraoperative imaging in all eligible cases, several practical constraints might hamper a GTR also when using iMRI. In the literature, EOR with iMRI in a patient in whom a GTR was feasible is reported to be around 97%.8,23,24 Additionally to the interruption of surgical workflow, constructional requirements and high primary costs hamper the distribution of the technique. A central issue in the assessment of a method for accuracy of tumor detection is the definition of a lesion in the typical imaging techniques. In GBM, typically contrast-enhanced T1 imaging is used to define the borders of the solid tumor. Based on AA-PET and histopathological studies, it is well known that the tumor extends well beyond the borders of the contrast enhancement.25,26,27,28 Thus, high-field iMRI-based resection is limited by the general interpretation of MRI data by surgeons and the respective conclusions and strategies derived from it.


16.1.5 Combined Use of 5-ALA and Intraoperative MRI


Other intraoperative imaging or visualization techniques like 5-ALA provide a different depiction of tumor tissue based on the technique itself. Due to the direct metabolism of 5-ALA to fluorescent protoporphyrin IX (PpIX), 5-ALA provides better detection of solid and invasive tumor compared to intraoperative Gd-DTPA enhancement alone during iMRI.29 However, a single center retrospective analysis shows a potential advantage concerning rate of GTR of iMRI-assisted resection compared to 5-ALA-based surgery alone.24 This might be due to the intraoperative update of navigation data and the excellent overview of the resection cavity using an intraoperative MRI. Further, potential satellite lesions can be detected with iMRI that might be missed using 5-ALA.


Feb 12, 2020 | Posted by in NEUROSURGERY | Comments Off on Fluorescence-Guided Surgery, Intraoperative Imaging, and Brain Mapping (iMRI, DTI, and Cortical Mapping)
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