Advances in the surgical resection of temporo-parieto-occipital junction gliomas

Advances in the surgical resection of temporo-parieto-occipital junction gliomas

Chapter 8 Advances in the surgical resection of temporo-parietooccipital junction gliomas Isaac Yanga,b and Giyarpuram N. Prashanta,b a Department o...

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Chapter 8

Advances in the surgical resection of temporo-parietooccipital junction gliomas Isaac Yanga,b and Giyarpuram N. Prashanta,b a

Department of Neurosurgery, UCLA, Los Angeles, CA, United States, bUCLA Jonsson Comprehensive Cancer Center, Los Angeles, CA, United States

Introduction The temporo-parieto-occipital (TPO) junction is a critical region of the brain, serving vital functionally significant diverse processes. However, it is not a primary anatomical region that comes to mind when considering the so-called “eloquent” areas of the cerebral cortex, such as the peri-Rolandic gyri, Broca’s area, and Wernicke’s area. Traditionally, the brain was thought to be functionally organized in discrete anatomical regions that subserved specific tasks, with corresponding permanent deficits occurring due to damage in those regions. Recent studies have demonstrated numerous instances of functionally significant cortical regions distributed beyond the canonical “eloquent” areas.1–4 In addition, accounts in the literature of patients who have undergone resection of gliomas or other pathology in “eloquent” regions without manifesting the expected neurological deficits have undermined this model.5–7 This highlights both intrinsic anatomic and functional variability between patients and the plasticity of dynamic functional circuits in the presence of slow-growing intracranial mass lesions.8–10 The idea of an integrated and dynamic brain network is encapsulated in the hodotopical model, in which a structure of cortical “nodes” and subcortical “connections” (short and long white matter tracts) serve as the substrate through which both specific functions exist and higher order cognition occurs.11,12 This burgeoning area has been termed human brain connectomics, evaluating the correlation between structural and functional neuroanatomy with respect to large-scale brain networks.13–15 The TPO junction plays a significant role in this connectomic framework, serving as a location for many of the key nodes and tracts that make up this network. New Techniques for Management of ‘Inoperable’ Gliomas. https://doi.org/10.1016/B978-0-12-813633-1.00008-6 © 2019 Elsevier Inc. All rights reserved.

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Cortical anatomy It is essential to have a firm understanding of cerebral neuroanatomy prior to engaging in the surgical resection of gliomas of the TPO junction. For the purposes of this chapter and its relevance toward transcortical surgical approaches, we will focus primarily on the lateral cortical and subcortical anatomy of the three lobes—parietal, occipital, and temporal (Fig. 1). The TPO junction can be roughly delineated by beginning at the posterior end of the Sylvian fissure, where the parietal, occipital, and temporal lobes meet. The central sulcus serves as an important anatomical and functional landmark, dividing the obliquely oriented precentral and postcentral gyri. The postcentral sulcus is the origin of the intraparietal sulcus, which runs posteriorly dividing the superolateral parietal lobe into the superior parietal lobule (SPL) and inferior parietal lobule (IPL). The posterior extent of the parietal lobe is the imaginary line that runs from emergence of the parieto-occipital sulcus medially to the preoccipital notch,

FIG. 1 Cortical anatomy of the brain. Por, pars orbitalis; Ptr, pars triangularis; Pop, pars opercularis; Mfg, middle frontal gyrus; Pre, precentral gyrus; Post, postcentral gyrus; Spl, superior parietal lobule; Smg, supramarginal gyrus; Ang, angular gyrus; Sog, superior occipital gyrus; Mog, middle occipital gyrus; Iog, inferior occipital gyrus; Stg, superior temporal gyrus; Mtg, middle temporal gyrus; Itg, inferior temporal gyrus.

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which is approximately 5 cm anterior to the occipital pole.16 The SPL is classically quadrangular in shape and extends medially to the interhemispheric fissure to form the precuneus. The IPL is made up of the supramarginal gyrus (SMG), which encircles the posterior terminus of the Sylvian fissure and continuous with the superior temporal gyrus, the angular gyrus (AG), which surrounds the distal superior temporal sulcus, and the middle temporal gyrus. The SMG and AG are separated by the intermediate sulcus, which classically arises from the intraparietal sulcus. The intraparietal sulcus also continues posteriorly as the intraoccipital sulcus, dividing the superior occipital gyrus (SOG) from the middle occipital gyrus (MOG). The middle occipital gyrus and the inferior occipital gyrus (IOG) are separated by the inferior occipital sulcus. The lateral surface of the temporal lobe is composed of three longitudinal gyri, with the posterior extent being the imaginary line from the medial origin of the parieto-occipital sulcus to the preoccipital notch.

White matter tracts Subcortically, the TPO junction contains multiple white matter tracts that serve as significant components of both local processes and global networks. The first major white matter tract encountered beneath the cortical gray matter and subcortical U fibers is the superior longitudinal fasciculus (SLF), which is divided into direct (arcuate fasciculus) and indirect (SLF II and III) components and provides key connections between classical cortical regions associated with language functions.17,18 The SLF III runs from the posterior third of the STG and MTG and travels to the ventral IPL. A separate bundle from the dorsal IPL, termed the SLF II, travels more horizontally and anteriorly to the ventral frontal lobe. The direct component of the SLF, the arcuate fasciculus, lies deep to these indirect fibers, traveling from the STG and MTG to the frontal lobe in a C shape and terminating in the pars opercularis and pars triangularis of the inferior frontal gyrus, as well as parts of the middle frontal gyrus.18,19 Both the direct and indirect component of the SLF play a critical role in language, with disruptions resulting in phonemic paraphasias, errors in repetition, and dysarthria/ anarthria.4,18–21 The inferior fronto-occipital fasciculus (IFOF) is contained within the external capsule of the frontal operculum, and travels inferiorly through the temporal stem, running above the temporal horn of the lateral ventricle. It continues parallel and lateral to the optic radiations (OR) past the atrium of the lateral ventricle, and fans out at a 45 degree angle with wide cortical connections in the temporal, parietal, and occipital lobes.18 Intraoperative studies using direct electrical stimulation of this tract has resulted in impairments in semantic cognition, including semantic paraphasias.22–27 The inferior longitudinal fasciculus (ILF) is made up of short fibers that travel between temporo-basal regions and the occipital pole. It also contains a deeper component, a horizontal long fiber tract that connects the temporal pole

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the dorsolateral occipital lobe, running lateral to the wall of the temporal horn and crossing the IFOF in a deeper plane prior to the occipital terminations.18,28 It has been suggested that there is a hemispheric functional specialization of this tract, with the dominant left hemisphere involved in semantic and syntactic processing, and the nondominant right hemisphere taking part in visual recognition.29–32 The middle longitudinal fasciculus (MLF) has recently been described in humans, and is thought to connect the superior temporal gyrus to the superior and inferior parietal lobule. While definitive functional significance has not yet been identified, it has been hypothesized that it may play a role in language processing.33–37 The OR can be divided into anterior, middle, and posterior groups. The anterior group arise from the lateral geniculate nucleus (LGN) of the thalamus, curve anteriorly over the roof of the temporal horn, then turn posteriorly ventral and basal to the IFOF, running over the lateral inferior aspect of the atrium of the lateral ventricle and occipital horn to reach the lower bank of the calcarine fissure. The middle group similarly course anteriorly over the temporal horn and run lateral to the atrium and occipital horn. The posterior fibers run directly from the LGN just lateral to the atrium and occipital horn, and beneath the fibers of the IFOF, to the upper bank of the calcarine fissure.38,39 Damage to these tracts can lead to disorders of visual perception and visual field defects.19,21,40 In addition to the specific deficits mentioned previously, the TPO region has been implicated in several higher level functions. These include visuospatial processing and mental arithmetic,41–44 working memory,45–47 handwriting,48–50 reading,51,52 symbol processing,53,54 face and object recognition,55,56 and musical memory.57

Surgical considerations Several recent studies have highlighted the significant impact of extent of resection on patient outcomes in both low- and high-grade gliomas.58–62 Increasing extent of resection can improve the overall survival, progression-free survival, seizure control, and time to malignant transformation.63 While a gross total (or “supratotal”) resection may provide a beneficial effect on patient survival, it must be balanced with surgical morbidity, as significant neurological deficits and decreased functional status can be devastating to the quality of life.59,64,65 This is especially an important consideration in patients with high-grade gliomas who often have a limited life expectancy. Therefore, the neurosurgeon must strike a balance between preserving the functional cortical and subcortical pathways of the TPO junction while maximizing extent of resection of gliomas in this region. It is also key to have a deep understanding of the natural history and biology of the disease; gliomas tend to be infiltrative in nature and often extend through white matter pathways, making gross total resections difficult. A thorough discussion with individual patients and family members to review these

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clinical expectations and risks of surgery ensures that all parties are at the same level of understanding prior to surgery. The concept of dominant vs nondominant hemisphere is important to consider when planning surgery in the TPO junction. While the left hemisphere was traditionally thought to be dominant in most patients, particularly in those who were right handed, early research and more recent studies have revealed numerous instances of neurological deficits after resection of lesions in the right hemisphere, as well as a weaker correlation between handedness and language lateralization than previously believed.7,66–69 In addition, neuropsychological testing of postoperative patients with right hemispheric lesions has revealed impacts on emotions and cognitive functioning.70,71 Therefore, even in patients with gliomas involving the right TPO region a complete assessment of functional activity, including intraoperative mapping, should be considered.

Preoperative planning For gliomas involving the TPO junction, it is important to evaluate thoroughly for any preoperative neurological abnormalities or cognitive deficits. With imaging or clinical evidence of involvement of language pathways, we recommend formal neuropsychological testing. At our institution, awake craniotomy with speech mapping is routinely performed for patients in whom the tumor intimately involves cortical or subcortical language pathways. As intraoperative brain mapping is the gold standard for identifying key functional cortical and subcortical regions, it can be utilized for the resection of any intrinsic brain tumor identified as being located adjacent to regions that may contain sensorimotor or language function. In terms of candidacy for awake craniotomy, the ideal patient should be cooperative and able to name objects reliably. Relative contraindications to this procedure include tumors causing significant mass effect and midline shift (>2 cm), obese patients with respiratory compromise, psychiatric history and/or emotional instability, frequent preoperative seizures, and chronic cough. Absolute contraindications (as described by the UCSF group) include severe dysphasia, uncontrolled cough despite medication, and hemiplegia with less than antigravity function.63,72,73 All patients should undergo preoperative high-resolution magnetic resonance imaging (MRI), including thin-cut contrast enhanced images and T2/ FLAIR sequences. Diffusion tensor imaging (DTI) is a useful MRI-based technique, taking advantage of the fractional anisotropy of white matter tracts to determine both orientation of fibers and location with respect to tumors (Fig. 2). In the TPO region particular attention should be paid to the SLF/arcuate fasciculus, IFOF, ILF, and optic radiations. While DTI can be very helpful to localize these tracts preoperatively, it does have significant limitations—(1) DTI only displays anatomic localization and provides no information on functional significance, (2) tumor invasion or edema can alter results and occasionally give an incorrect picture, and (3) if incorporating DTI into a

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FIG. 2 Preoperative planning using DTI scans and region of interest highlighted in neuronavigation software (Brainlab AG, Munich, Germany).

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neuronavigation system, once craniotomy has been performed brain shifts distort the relationships. However, preoperative DTI does appear to correlate well with anatomical fiber tract location, as evaluated by subcortical electrical stimulation.74–76 In addition, in a prospective study in patient with gliomas involving the pyramidal tract, DTI has been shown to decrease morbidity and improve patient quality of life.77 Task-based functional MRI (fMRI) detects blood oxygen level-dependent (BOLD) signal as a measure of alterations in local cerebral blood flow due to neuronal activity. This map of functional activity can then be overlaid on structural MRI sequences to map out the location of “eloquent” regions. While this technique has good spatial resolution and is widely available, it is limited by consistency in the administration and application of tasks, as well as technical considerations such as motion artifacts.78,79 As fMRI broadly displays regions that are active during a specific task, it does not provide information on the specific areas that are essential and will result in a deficit if disrupted. This information can only be obtained with intraoperative brain mapping.

Intraoperative techniques While preoperative imaging can provide benefits in localizing putatively “eloquent” cortical and subcortical areas, intraoperative brain mapping with direct electrical stimulation is the gold standard to determine functionally significant regions of the brain. Using a staged approach, the first step after tumor identification is sensorimotor mapping, followed by cortical stimulation of language sites. Next, the tumor is removed, alternating between subcortical stimulation and resection. In this way, the functional pathways are followed from cortical eloquent regions to the depth of the resection, at which time the entire surgical cavity is surrounded by functional pathways. This functional approach to resection allows for maximal tumor removal with preservation of clinically significant cortex and subcortical fiber tracts.10,72,73,80 To initially identify the location of the motor strip and Rolandic fissure, an electrode grid placed perpendicular to the gyri is used to evaluate SSEP phase reversal (Fig. 3). For lesions involving both the TPO junction and the precentral gyrus/pyramidal tract, cortical and subcortical motor mapping can be performed using a handheld probe or cortical grid under general anesthesia. The electrode is typically used with an initial current frequency of 60 Hz and amplitude of 1 mA, with an increase in stimulating amplitude until movement is identified. A general guideline is to avoid currents above 6 mA in order to reduce risk of intraoperative seizures. Intraoperative language mapping requires awake craniotomy, and in general we prefer an asleep-awake-asleep technique, in which the patient receives intravenous anesthesia and analgesics initially, is woken for the mapping and surgical resection, and then returned to sleep for closure. The patient must be informed prior to the surgery on the details of the procedure and what to

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FIG. 3 Identification of primary motor and somatosensory cortex with cortical grid electrodes.

expect, and a clear line of communication between the neurosurgical and anesthesia teams is crucial. In preparation for possible intraoperative seizures, a dedicated IV line should be filled with 1-mg-kg propofol bolus, and iced Ringer’s lactate solution available on the surgical field. Short- and long-acting local anesthetics are infused into the scalp and temporalis muscle, and once a focused craniotomy is performed medications are ceased. Infiltration of the dura, particularly in the region of the middle meningeal artery, should also be performed to minimize any pain during patient testing. Stimulation is generally performed beginning at 1–2 mA and increased until relevant language function is established. Common testing for language function includes assessments for speech arrest (during a number counting task), dysarthria, anomia, and alexia. Cortical language sites are mapped every 1 cm, with each site checked 3 times to ensure consistency. A 1-cm margin generally provides adequate protection from functionally significant areas. Compared to intraoperative mapping for motor or language function, assessments of visual pathways are less often performed. However, a postoperative hemianopsia can significantly impact quality of life of patients and also affect ability to obtain a driver’s license in many countries. In limited series published to date, subcortical stimulation of the visual fiber tracts has resulted in reliable identification and preservation of visual function.40,81 This group used a modified picture-naming task with pictures placed in diagonal quadrants, in order to tests both language and visual fields simultaneously. Adjunct technologies can also aid the neurosurgeon in optimal resection of gliomas. Neuronavigation using both structural and functional imaging (such as

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DTI and fMRI) allows the surgeon to integrate localization of the tumor and boundaries with relevant fiber tracts and task-based active areas. While this is not a replacement for intraoperative mapping, it aids in preoperative planning, determining the surgical approach, and discussing with the patient risks of postoperative neurological deficits. A prospective study evaluating fMRI of language and motor functions vs direct electrocortical stimulation resulted in high correlations, with a sensitivity and specificity of approximately 80%.82 One of the main limitations of neuronavigation arises from its inaccuracy during resection, due to CSF loss and brain edema. Intraoperative MRI has attempted to address this issue with the availability to image during the case itself. While this technology is relatively recent, there is evidence that the use of intraoperative MRI for low- and high-grade glioma increases tumor resection rates and improves patient survival, with no additional surgical morbidity.83–87 The primary difficulty with the resection of low- and high-grade gliomas is the tendency to infiltrate through the white matter, and despite maximizing extent of resection the majority of tumors recur within close distance of the resection cavity. Resection of gliomas is further challenging by difficulty in identifying the margin between the normal and diseased brain. 5-Aminolevulic acid (5-ALA) is a natural biochemical amino acid precursor of hemoglobin which is taken up by malignant glioma cells and converted into fluorescing porphyrins.88,89 If given exogenously prior to tumor resection, it can be used to aid in visualization of glioma using a filter mounted to an intraoperative microscope, and has few adverse effects. Recent phase II and phase III trials have established that 5-ALA guided resections result in significant increases in gross total resection (65% vs 36% using conventional microsurgery), greater 6-month progression-free survival, and greater overall survival.90,91 Of note, while a promising treatment option in the resection of high-grade gliomas, 5-ALA has low sensitivity for low-grade tumors.

Conclusion The goal of this chapter is to introduce the reader to the complexity of the TPO region, including the functional cortical and subcortical neuroanatomy. In addition to the canonical eloquent cortical regions, such as the peri-Rolandic gyri, Broca’s area, and Wernicke’s area, the TPO junction contains numerous white matter fibers tracts involved in diverse processes. As recent studies have highlighted the importance of extent of resection on patient survival and quality of life in low- and high-grade gliomas, combining this knowledge of the regional anatomy with modern neurosurgical techniques can result in excellent patient outcomes. The use of novel technologies, including brain mapping, neuronavigation, intraoperative MRI, and fluorescence-guided resections, can also aid in this goal and are essential tools to achieve the best possible results in the care of these patients.

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