Functional Magnetic Resonance Imaging of Regional Brain Activity in Patients with Intracerebral Gliomas: Findings and Implications for Clinical Management

Abstract

Functional magnetic resonance imaging (fMRI) was performed in seven patients harboring intracerebral gliomas proven by histological analysis using a noninvasive blood oxygen level-dependent technique based on the documented discrepancy between regional increases in blood flow and oxygen use in response to regional brain activation. We combined fMRI with conventional magnetic resonance imaging (MRI) during motor or language task activation experiments to investigate the potential usefulness of mapping regional brain activity as part of treatment planning in patients with intracerebral gliomas, in whom preservation of areas of functioning brain tissue is critical. Statistical fMRI maps were generated and directly mapped onto conventional MRI scans obtained at the same session. Of the five patients cooperative enough to remain motionless for the study and perform the task, the location of activation in the primary sensorimotor cortex on the side of the tumor was clearly displaced compared with that in the normal contralateral hemisphere in four patients. Four of the five tumors in these patients showed fMRI activation within the periphery of (or immediately adjacent to) areas of presumed tumor based on spin-echo MRI. In some patients with neurological deficit, the extent of activation was reduced on the side of the tumor as compared with the normal hemisphere. The supplemental motor area and the ipsilateral primary motor cortex were also reproducibly activated during motor tasks. We conclude that blood oxygen level-dependent fMRI can localize areas of cortical function in patients undergoing treatment planning for gliomas so that therapy can be directed away from regions of residual function. Our preliminary data suggest that functioning cortex within or adjacent to tumor margins can be demonstrated, which may correspond to partial preservation of clinical function. Our preliminary data also suggest that there may be a quantifiable difference on fMRI between activation in tumor-bearing cortex and activation in corresponding normal cortex in the contralateral hemisphere. We postulate that the magnitude of this difference may relate to the severity of patient deficit.

The Role of Functional MRI in Intracranial Glioma Resection

“…Particular attention should be taken in such cases and further preoperative, possibly invasive studies, need to be performed. In high grade gliomas, the presence of neovascularization, the induction of neuro-chemical changes in the cytosol and the subsequent alteration of the regional cerebral blood flow and the oxygen extraction fraction, the presence of arteriovenous shunting, and the presence of tumor-associated edema and mass effect causing mechanical vasoconstriction, as well as the presence of scar tissue secondary to a previous craniotomy may result into significant BOLD signal changes [Atlas et al, 1996;Giussani et al, 2010;Haberg et al, 2004;Krishnan et al, 2004 ]. It has been demonstrated, that in 10-31% of the performed fMRI studies the obtained data cannot be processed, and this percentage in glioma populations ranges between 0-30% [Haberg et al, 2004].…”

“…Accurate knowledge of the anatomical relationship of a glioma with neighboring eloquent cortical areas is of paramount importance for maximizing tumor resection, minimizing the chance of postoperative neurological deficit, and thus maximizing the patient's safety. Functional MRI has been employed for more than 15 years in the preoperative evaluation of patients harboring intracranial gliomas for identifying, accurately localizing, and intraoperatively avoiding functional cortical centers [Atlas et al, 1996;Berntsen et al, 2010;Bizzi et al, 2008;Fandino et al, 1999;Fitzgerald et al, 1997;Giussani et al, 2010;Haberg et al, 2004;Hirsch et al, 2000;Hoenig et al, 2005;Krasnow et al, 2003;Krishnan et al, 2004;Lehericy et al, 2000;Li et al, 2010;Lurito et al, 2000;Mueller et al, 1996;National Comprehensive Cancer Network, 2007;Petrovich et al, 2005;Pouratian et al, 2002;Puce et al, 1995;Roux et al, Ruge et al, 1999;Rutten et al, 2002;Sanai & Berger, 2008;Schulder et al, 1998;Signorelli et al, 2003;Tieleman et al, 2007;Tomczak et al, 2000;Yetkin et al, 1997;Yousry et al, 1995] (Figures 1 & 2). Several clinical studies have been performed comparing fMRI with intraoperative electrophysiological stimulation studies, with varying results, and frequently contradictory conclusions [Atlas et al, 1996;Berntsen et al, 2010;Bizzi et al, 2008;Fandino et al, 1999;Fitzgerald et al, 1997;…”

“…Therefore, their results are not comparable, in the vast majority of cases. However, a systematic review of the existent clinical studies show that fMRI constitutes a routine clinical practice in many neuro-oncology centers around the world, which provides the opportunity to the performing neurosurgeon for a more realistic and accurate preoperative discussion with the patient, a wiser decision-making process, a safer surgical planning, and a more aggressive tumor resection [Atlas et al, 1996;Berntsen et al, 2010;Bizzi et al, 2008;Fandino et al, 1999;Fitzgerald et al, 1997;Giussani et al, 2010;Haberg et al, 2004;Hirsch et al, 2000;Hoenig et al, 2005;Krasnow et al, 2003;Krishnan et al, 2004;Lehericy et al, 2000;Li et al, 2010;Lurito et al, 2000;Mueller et al, 1996;National Comprehensive Cancer Network, 2007;Petrovich et al, 2005;Pouratian et al, 2002;Puce et al, 1995;Ruge et al, 1999;Roux et al, 2003;Rutten et al, 2002;Sanai & Berger, 2008;Schulder et al, 1998;Signorelli et al, 2003;Tieleman et al, 2007;Tomczak et al, 2000;Yetkin et al, 1997;Yousry et al, 1995]. Several studies also emphasize that fMRI can localize more accurately motor and sensory cortical areas than language areas, and therefore they indicate the necessity for employing complimentary intraoperative electrophysiological stimulation studies, in cases of tumor proximity to language-associated cortical areas [Berntsen et al, 2010;Giussani et al, 2010;Hirsch et al, 2000;Roux et al, 2003;…”

“…They reported that fMRI accuracy in their prospective study was 100%, while they concluded that maximal tumor resection and no new postoperative neurological deficits were observed in their series [Schulder et al, 1998]. Contrariwise, Atlas et al [Atlas et al, 1996] reported a series of seven patients with gliomas, undergoing preoperative fMRI at 1.5T. Their fMRI protocol included single-or multi-stage active finger tapping as motor tasks [Atlas et al, 1996].…”

“…Contrariwise, Atlas et al [Atlas et al, 1996] reported a series of seven patients with gliomas, undergoing preoperative fMRI at 1.5T. Their fMRI protocol included single-or multi-stage active finger tapping as motor tasks [Atlas et al, 1996]. They reported that in 28.5% of their cases fMRI failed to identify the motor cortex, while they postulated that glioblastomas and high-grade gliomas may alter the obtained BOLD signal [Atlas et al, 1996].…”