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3D"ContinuingNature Clinical Practice Neurology (2007) = 3,=20 628-639
doi:10.1038/ncpneuro0634=20  3D""=20
Received 14 = June 2007 |=20 Accepted 9 August 2007

Surgery Insight: the role of surgery in the management of = low-grade=20 gliomas

Nader Pouratian, Ashok Asthagiri, Jay Jagannathan, Mark E = Shaffrey and=20 David Schiff*  About=20 the authors

Correspondence *Neuro-Oncology Center, = University of=20 Virginia Health System, PO Box 800432, Charlottesville, VA 22908=960432, = USA=20

Email davidschiff@virginia.edu

=

3D"Medscape

Medscape Continuing Medical Education = online
Medscape,=20 LLC is pleased to provide online continuing medical education (CME) for = this=20 journal article, allowing clinicians the opportunity to earn CME credit. = Medscape, LLC is accredited by the Accreditation Council for Continuing = Medical=20 Education (ACCME) to provide CME for physicians. Medscape, LLC = designates this=20 educational activity for a maximum of 1.0 AMA PRA Category 1 Credits=99. = Physicians should only claim credit commensurate with the extent of = their=20 participation in the activity. All other clinicians completing this = activity=20 will be issued a certificate of participation. To receive credit, please=20 complete the post-test.

Learning objectives

Upon completion of this activity, participants should be able to:

  1. Distinguish types of low-grade gliomas.
  2. Describe the prevalence of low-grade gliomas.
  3. Identify the most common presentations of low-grade gliomas.
  4. Describe characteristics of low-grade gliomas amenable to surgical = resection.
  5. List potential benefits of gross total resection for patients with = low-grade gliomas.

To complete the questions online and earn continuing education = credits, you=20 must be a registered user on Medscape.com. If you are not registered on = Medscape.com please click on the = New Users:=20 Free Registration link on the top left-hand side of the website to = register.=20 Registration is free. For questions regarding the content of this = activity,=20 contact the accredited provider for this CME activity: CME@medscape.net. For technical = assistance,=20 contact CME@webmd.net.

Summary

The benefits of surgery for the management of low-grade = gliomas=20 have been difficult to determine from the literature. This difficulty = might be=20 explained by the inconsistency of the published data, and also by = advances in=20 both neuroimaging and neurosurgical techniques, which have made surgical = intervention a safer and more viable option than it has been in the = past, making=20 the earlier studies less applicable to modern care. In this article, we=20 critically analyze the utility of surgery in the management of low-grade = gliomas, including the value of observation without surgical = intervention, the=20 relative risks and benefits of biopsy versus craniotomy and resection, = and=20 recent advances that have made surgery safer and gross total resection a = more=20 realistic proposition. As we will discuss, the literature provides = modest=20 evidence that surgery leads to improved outcomes through a reduction in = tumor=20 burden. As a result of advances in surgical techniques, the time might = now be=20 right to effectively and accurately assess the influence of aggressive = surgical=20 resection on the prognosis of low-grade gliomas.

Review criteria

For this review, we searched PubMed by using Entrez = without date=20 restrictions and including early release publications. Search terms = included=20 "low-grade glioma" in combination with each of the following terms:=20 "observation", "biopsy" and "surgery". The abstracts of retrieved = citations were=20 reviewed for relevant content. Full articles were obtained and = references were=20 checked for additional material when appropriate.

Keywords:

astrocytoma,=20 low-grade=20 glioma, oligoastrocytoma,=20 oligodendroglioma,=20 surgical=20 resection

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Introduction

Although their name might imply otherwise, low-grade = gliomas=20 result in considerable morbidity and inevitable death. The benefits of = various=20 interventions=97including fractionated radiotherapy, chemotherapy and = surgical=20 resection=97have all been disputed, but the role of surgical = intervention is=20 particularly controversial. This debate stems in part from the = inconsistency of=20 results from published reports regarding the benefits of surgical = intervention,=20 and is complicated further by advances in neuroimaging and neurosurgical = techniques that have made surgical resection a safe and viable option = for an=20 increasing number of patients.

In this Review, we will critically analyze the utility = of surgery=20 in the management of low-grade gliomas, including the role of = observation=20 without surgical intervention, the debate regarding biopsy versus = resection, and=20 the recent surgical advances that have made surgery for low-grade = gliomas=20 increasingly safe and widely available.

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Epidemiology

The phrase 'low-grade gliomas' encompasses the entire = spectrum of=20 WHO grade I and II gliomas, which includes ependymomas, pilocytic = astrocytomas,=20 pleomorphic xanthoastrocytomas, diffuse astrocytomas, = oligodendrogliomas, and=20 mixed gliomas. Although arbitrarily clustered under the umbrella = low-grade=20 glioma nomenclature, this heterogeneous group of tumors is clinically,=20 histologically and molecularly diverse, and is, therefore, not generally = studied=20 or discussed as a single entity. For example, WHO grade I lesions, which = include=20 pilocytic astrocytomas and gangliogliomas, are, unlike WHO grade II = lesions,=20 well circumscribed and noninfiltrative, and complete surgical resection = is=20 universally considered curative.1=20 In this Review, we will limit our discussion to WHO grade II diffuse=20 astrocytomas, oligodendrogliomas and oligoastrocytomas, all of which = have=20 similar invasive and malignant potential.

Although low-grade gliomas are less common than = malignant gliomas=20 (of which there are 8,000=9610,000=20 cases per year) and far less common than brain metastases (75,000=96150,000=20 cases per year), they are far from rare. Approximately 2,000=963,000 = low-grade=20 gliomas are diagnosed in the US every year, accounting for nearly 15% of = all=20 primary brain tumors.2=20 According to the Central Brain Tumor Registry of the United States = (CBTRUS), the=20 various histological classes of low-grade glioma have incidences varying = between=20 0.10 and 0.46 per 100,000 people, and a cumulative incidence of = approximately=20 0.9 per 100,000 people.2

Despite the preponderance of astrocytomas, there has = been an=20 apparent increase in recent years in the incidence of pure = oligodendrogliomas=20 and of mixed oligoastrocytomas. This increase might be partly = attributable to an=20 increased tendency for neuropathologists to seek out such diagnoses, in = view of=20 the relatively favorable prognosis conveyed by an oligodendroglial=20 component.3=20 Low-grade gliomas are particularly prevalent among white people and = among men,=20 and the highest incidence is in people between 35 and 44 years of age. = Low-grade=20 astrocytomas in adults are most commonly located in the cerebral = hemispheres,=20 with a predilection for 'secondary' functional areas such as the = supplementary=20 motor area and the insular lobe.4=20 Oligodendrogliomas are most commonly seen along the cerebral convexity = in=20 subcortical areas, particularly in the frontal lobe, but sporadic = reports of=20 posterior fossa oligodendrogliomas exist.

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Signs, Symptoms and Prognosis

Low-grade gliomas produce signs and symptoms of disease = through=20 three main mechanisms: direct infiltration and destruction of neurons; = local=20 pressure from edema, hemorrhage and tumor mass; and intracranial = hypertension=20 owing to mass effect or ventricular obstruction. In many cases, the = insidious=20 onset of symptoms related to low-grade gliomas might delay the correct = diagnosis=20 for many years. When patients become symptomatic, seizure is the most = common=20 presenting sign, occurring in up to 80% of cases.5,=20 6=20 Other less common modes of presentation include headache, lethargy and=20 personality changes. The patient's presenting symptoms and imaging=20 characteristics can critically affect management; both neurosurgeons and = neuro-oncologists are likely to recommend surgical intervention for = patients=20 presenting with signs and symptoms attributable to mass effect or = intracranial=20 hypertension.

Although the effect of surgery on low-grade glioma = prognosis is a=20 topic for debate, several factors are recognized to be associated with = poor=20 prognosis, including, but not limited to, advanced age at time of=20 diagnosis,3,=20 5,=20 6,=20 7=20 larger tumor size on presentation (before surgical intervention),6,=20 8,=20 9,=20 10=20 and rapid tumor growth rate.11=20 Favorable prognostic factors include presentation with seizure (as = opposed to=20 with an abnormal neurological examination), and having an = oligodendroglial=20 component, a 1p and 19q chromosomal deletion, or a tumor that does not = cross the=20 midline.

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Is there a role for observation without surgery?

Historically, expectant management has been considered = to be a=20 plausible management paradigm for patients who have lesions with typical = features of low-grade glioma, especially those with minimal symptoms or = seizures=20 that are well controlled with antiepileptic drugs.12=20 Expectant management can potentially provide patients with an overall = improved=20 quality of life (QOL) for the duration of disease by not exposing them = at the=20 time of diagnosis to the morbidity and mortality risks associated with = biopsy or=20 with craniotomy and resection. Imaging characteristics considered to be = typical=20 of low-grade glioma include low attenuation on CT scanning, and T1 = shortening,=20 T2 prolongation, and absence of contrast enhancement on MRI (Figure=20 1).13=20 The diagnostic value of these 'typical' imaging characteristics has, = however,=20 come under scrutiny. Kondziolka and colleagues found that imaging-based=20 diagnosis of low-grade glioma was accurate in only 50% of patients (on = the basis=20 of comparison with stereotactic biopsy results).13=20 Likewise, Scott and colleagues found that, in a series of 314 patients, = grading=20 gliomas on the basis of imaging characteristics alone underestimated the = degree=20 of malignancy in one-third of cases.14=20 Furthermore, although contrast enhancement on MRI has long been = considered a=20 sign of malignancy, recent studies of chemotherapeutics for low-grade = glioma=20 have reported contrast enhancement in up to 60% of low-grade = gliomas.15=20 The use of magnetic resonance spectroscopy and perfusion-weighted = imaging has=20 markedly increased the accuracy and sensitivity of imaging-based = diagnosis and=20 grading of gliomas, but these techniques are still associated with = significant=20 error rates and are not used in routine clinical neuroimaging.16,=20 17,=20 18

Figure=20 1 Typical MRI scan of a low-grade glioma, histopathologically = defined=20 as a WHO grade II oligodendroglioma.

(A) T1 sequence demonstrating T1 shortening in the right = frontal lobe.=20 (B) T2 sequence demonstrating T2 prolongation (hyperintensity) at = the=20 site of the glioma. (C) Contrast-enhanced imaging of the glioma = showing=20 no marked contrast enhancement. Although these images are considered = 'typical',=20 numerous studies have questioned the reliability and accuracy of these = imaging=20 characteristics for the diagnosis of low-grade glioma.

Full=20 figure and legend (26K)Figures=20 & Tables indexDownload=20 Power Point slide (82K)

The preponderance of studies that contradict the notion = of a=20 pathognomonic imaging profile for low-grade glioma that could be = elucidated=20 using standard imaging sequences suggests that tissue acquisition = remains=20 mandatory for the accurate diagnosis, prognostication and management of = these=20 tumors. In an era when management regimens are predicated on the basis = of tumor=20 cytogenetics, tissue-based diagnosis carries increasing prognostic and=20 therapeutic implications and the absence of such evaluation inevitably = limits=20 the scope of therapeutic interventions.

In addition to misdiagnosis, expectant management = carries other=20 risks, including malignant degeneration, interval tumor growth that = makes=20 subsequent resection more difficult or impossible, and development of an = irreversible neurological deficit.19=20 Despite these theoretical risks, a comparison between initial = conservative=20 management and immediate surgical resection by Recht and colleagues = reported=20 that the timing of intervention did not affect rates of malignant=20 transformation, overall survival (OS), or QOL.20=20 Similarly, Reijneveld and co-workers found that, although patients with=20 low-grade gliomas experienced significant cognitive disturbances and = impairments=20 in QOL, a 'wait-and-see' policy did not worsen these afflictions.21=20 Furthermore, van Veelen et al. reported that the 5-year survival = was=20 identical (63%) in patients who underwent surgery immediately on = diagnosis and=20 those who underwent surgery at the time of clinical or radiographic=20 progression.22=20 Despite the consistent finding that the timing of tissue diagnosis is = not=20 critical, it is important to stress that the studies performed on this = topic to=20 date have all been retrospective, which inevitably introduces = considerable=20 selection bias and limits interpretation and applicability.

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Biopsy or resection?

Both stereotactic biopsy and open biopsy provide an = opportunity to=20 characterize the histology and cytogenetics of a suspected low-grade = glioma=20 without the morbidity and mortality risks associated with a large = craniotomy. In=20 general, biopsy has been advocated in the setting of tumors located = adjacent or=20 deep to eloquent cortices, which would not be amenable to gross total = resection=20 (GTR).23=20 Whereas stereotactic biopsies are preferred for patients with deeper = lesions,=20 open biopsies are reserved for those with superficial lesions that are = easily=20 accessible via a small craniotomy and for those with lesions immediately = adjacent to eloquent cortices, which should be mapped before biopsy. = Craniotomy=20 and resection, on the other hand, have traditionally been reserved for = patients=20 with appreciable mass effect from low-grade glioma (which results in = increased=20 intracranial pressure or neurological deficit) and for those with = symptomatic=20 epilepsy that is refractory to antiepileptic therapy.22,=20 24

In general, the diagnostic yield of stereotactic biopsy = is high=20 (90=9695%).25,=20 26,=20 27=20 Several studies have, however, raised concerns regarding the reliability = and=20 accuracy of biopsy-based diagnoses.23,=20 26,=20 28,=20 29=20 Aker and colleagues scrutinized results from 23 patients who initially = underwent=20 stereotactic biopsy and subsequently required craniotomy, and reported = that the=20 accuracy of histological diagnosis made on the basis of a stereotactic = biopsy=20 sample was only 83%.26=20 In three of the four misdiagnosed cases, a biopsy-based diagnosis of = low-grade=20 glioma was changed to anaplastic astrocytoma, granulomatous cerebritis, = or=20 dysembryoblastic neuroepithelial tumor. Similarly, McGirt and co-workers = reported 79% accuracy of diagnosis in 23 patients who underwent biopsy = followed=20 within 60 days by resection.28=20 Even more concerning, Jackson and colleagues at the MD Anderson Cancer = Center,=20 Houston, TX, reported accuracy rates inferior to those reported by = McGirt et=20 al., ranging between 51% and 62%.23=20 Accuracy rates depended on the expertise of the interpreting = neuropathologists,=20 highlighting the need for expert neuropathology consultation when using=20 stereotactic biopsy in order to obtain the best possible = accuracy.23=20 Despite discrepancies between histopathology results from stereotactic = biopsy=20 and craniotomy, some groups have argued that appropriate treatments are = still=20 administered in 93=9696% of cases, owing to similarities in treatment = paradigms=20 for gliomas of different grades.28,=20 30=20 Such viewpoints are, however, becoming less valid as clinical studies = further=20 stratify treatment paradigms according to tumor grade and cytogenetics.=20 Moreover, prognostication and patient counseling is inevitably adversely = affected by misdiagnosis.

When assessing the value and role of biopsy in the = management of=20 low-grade gliomas, it is important to consider not only the yield and = accuracy=20 of biopsy, but also the risks associated with the procedure. Despite its = reputation for safety, stereotactic biopsy is not without risk. To = quantify the=20 morbidity and mortality of the procedure, Hall reviewed 17 series = comprising a=20 total of 7,471 stereotactic brain biopsies.27=20 He reported an overall morbidity rate of 3.5% and a mortality rate of = 0.7%,=20 which were largely related to procedure-induced hemorrhage. Risk factors = for=20 biopsy-associated morbidity include basal ganglia lesions, thalamic = lesions,=20 diabetes, and hyperglycemia on the day of surgery.31

In contrast to biopsy, surgical resection minimizes the = likelihood=20 of sampling error by providing considerably more tissue for = histopathological=20 analysis, but it inherently exposes the patient to greater risk. = Enthusiasm for=20 surgical resection has grown in light of advances in neuroimaging and=20 neurosurgical techniques that have made surgical resection safer and = more=20 accessible, and on the basis of numerous reports on the benefits of GTR = with=20 respect to both symptom control and prolongation of survival and time to = progression. Although not curative, GTR theoretically provides multiple=20 benefits, including reduction in the number of cells at risk of = undergoing=20 genetic events that result in malignant transformation, increased = efficacy of=20 adjuvant therapy, and symptomatic relief owing to reduced mass effect. = Surgical=20 resection has been particularly effective at controlling medically = refractory=20 seizures, resulting in near-seizure-free status, or a substantial = reduction in=20 seizure frequency and intensity, in nearly all patients.32,=20 33

Although large preoperative tumor size (diameter = >5=966 cm) is=20 consistently identified as a poor prognostic factor for survival,3,=20 6=20 the effect on clinical outcome of reduced tumor size remains = controversial, and=20 several studies have produced inconsistent results (Table=20 1). Keles and colleagues critically reviewed the literature with = respect to=20 the effect of extent of resection on outcomes in low-grade glioma and = found that=20 a preponderance of modern studies support extensive resection over = biopsy=20 alone.19=20 Leighton and co-workers, who retrospectively studied 167 consecutive = patients=20 treated at the London Regional Cancer Centre, ON, Canada, for low-grade = glioma=20 over a period of 16 years found, on both univariate and multivariate = analysis,=20 that minimal postoperative residual tumor was associated with = significantly=20 improved 5-year OS (82% vs 64%; P =3D 0.008 on univariate = analysis,=20 P =3D 0.006 on multivariate analysis).7=20 Other groups have likewise reported, in retrospective series, that = aggressive=20 surgical resection can prolong the time to tumor recurrence and reduce = the=20 malignant transformation rate.5,=20 8,=20 34=20 Lo and colleagues specifically queried whether patients who received=20 postoperative radiation therapy had benefited from extensive = resections.35=20 Of the 65 patients who received postoperative radiation therapy, the 12 = patients=20 who had GTR (as assessed by postoperative imaging) had significantly = longer=20 10-year OS than those who had subtotal resection or biopsy only (90% vs = 41.4%;=20 P =3D 0.001).

Table=20 1 Large studies investigating the effect of surgical resection = on=20 outcomes of low-grade glioma.

Full=20 tableFigures=20 & Tables indexDownload=20 Power Point slide (132K)

The results from prospective trials on resection and = postoperative=20 radiation therapy, however, are not so compelling. For example, a = prospective=20 intergroup American trial, designed primarily to compare the effects of = low-dose=20 versus high-dose radiation therapy, reported, on univariate analysis, a=20 significant 5-year OS advantage in patients who had GTR compared with = those who=20 had subtotal resection or biopsy alone (88% vs 56% and 71%, = respectively;=20 P =3D 0.0151).3=20 This trial also reported prolonged progression-free survival (PFS) in = patients=20 who had GTR compared with those who did not (hazard ratio 0.44, P = =3D=20 0.0138 on univariate analysis).3=20 Pignatti and colleagues and Karim and co-workers both retrospectively = studied=20 prospectively collected data from European Organisation for Research and = Treatment of Cancer trials (22844 and 22845, and 22844 only, = respectively) and=20 found, on univariate analysis, that extensive resection (i.e. >90%) = was=20 associated with longer OS.6,=20 10=20 Despite consistent findings on univariate analysis, on multivariate = analysis the=20 benefits of extensive resection were marginal at best in both studies. = The=20 failure of prospective trials to identify a benefit on multivariate = analysis=20 seriously challenges the role of extensive surgery in the management of=20 low-grade gliomas. It is important to point out, however, that these = studies=20 were not primarily intended to assess the effect of extensive resection, = and=20 were, therefore, not designed or powered to reliably evaluate this = factor. For=20 example, in most studies, the extent of resection was gauged on the = basis of the=20 'surgeon's impression', which is an unreliable assessment. Further = complicating=20 the interpretation of the literature are several other studies that = contradict=20 the finding that the difference in OS or PFS among patients relates to = the=20 extent of resection.19,=20 36,=20 37

The effect of surgical resection on QOL, as well as on = survival,=20 must be considered. Teixidor and colleagues recently studied the = consequence of=20 surgical resection on higher cognitive functions, specifically verbal = working=20 memory, as this function can dramatically affect a patient's QOL.38=20 As in previous studies, the authors found that most patients with = low-grade=20 glioma had preoperative cognitive deficits.21,=20 38=20 Although surgery can induce further deficits, these exacerbations are = transient=20 in most patients. Patients generally recover preoperative cognitive = function, or=20 even improve upon it, within 3 months after surgery.

Despite the preponderance of modern studies favoring = GTR, there is=20 a paucity of class I evidence supporting or refuting radical tumor = removal.=20 Moreover, the available statistical evidence in both retrospective and=20 prospective reports published to date is adulterated by numerous = inherent=20 limitations, including patient-selection bias, treatment-selection bias, = and=20 inconsistent and inaccurate means of assessing the extent of resection. = The=20 effect of selection bias in particular should not be underestimated.=20 Unfortunately, surgical selection criteria are rarely, if ever, reported = (Table=20 1). Patients with polar or lobar tumors with sharp borders are more = likely=20 to undergo and benefit from aggressive resection than those with less = well=20 defined lesions. By contrast, patients with probable low-grade glioma = who are=20 fully functional and never undergo treatment are not enrolled in = surgical=20 series. Tumor histopathology might also introduce selection bias;=20 oligodendrogliomas=97which often have sharp radiographic borders and = are,=20 therefore, more amenable to extensive resection than are fibrillary=20 astrocytomas=97have a better natural history than astrocytomas, and = might thereby=20 introduce a considerable potential selection bias into a surgical = series. For=20 each study, therefore, it is important to consider the patient and tumor = characteristics of both patients who were included in the analysis and = those who=20 were excluded. Notwithstanding the effect of selection bias, the lack of = a=20 consistent means of measuring the extent of resection probably adversely = affects=20 the interpretation of the literature (Table=20 1). In some studies, the extent of resection has been assessed on = the basis=20 of the surgeon's impression alone, whereas in others it has been = assessed by use=20 of inferior imaging modalities such as CT or by objective evaluation of=20 postoperative T2-weighted or fluid-attenuated inversion recovery (FLAIR) = MRI.=20 The definition of 'extensive' resection has also been variable, with = some=20 studies reporting and evaluating the absolute volume of residual = tumor8=20 and others considering the percentage of the preoperative tumor volume = that=20 remained after surgery.6,=20 22

Notably, a couple of recent studies suggest a possible = role for=20 neoadjuvant chemotherapy before surgical resection.39,=20 40=20 In both reported cases, although contralateral involvement via the = corpus=20 callosum originally prohibited GTR, chemotherapy was able to shrink the = tumors=20 to such an extent as to make GTR possible. Studies of temozolomide for = the=20 treatment of low-grade glioma suggest that significant tumor shrinkage = is=20 possible with chemotherapy alone.15,=20 41=20 It is unclear, however, how often chemotherapy can shrink a tumor enough = to make=20 GTR possible. The effect of the timing of surgery can and will be = appreciated=20 only when a prospective trial is performed, as was performed by van den = Bent=20 et al. to assess the timing of radiation therapy for the = management of=20 low-grade glioma.42

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Advances in neurosurgery

Advances in neurosurgical technology, including the = introduction=20 of preoperative and intraoperative brain mapping techniques and = intraoperative=20 image guidance, have made surgery for low-grade glioma increasingly safe = and=20 accessible. Perhaps more importantly, preoperative functional brain = mapping has=20 empowered surgeons to operate on patients who previously might not have = been=20 considered suitable candidates for surgery.

Historically, eloquent cortices have been identified on = the basis=20 of anatomical landmarks. In the context of brain tumors, however, these=20 landmarks can be difficult to delineate, and this approach to = identification=20 cannot account for individual variability or plasticity-related changes. = Preoperative brain mapping techniques, including functional MRI (fMRI) = and=20 magnetic source imaging (MSI), have, therefore, revolutionized the = assessment of=20 patients with brain tumors. Preoperative maps help determine the need = for=20 intraoperative mapping, the best approach (or 'corridor') to tumor = resection in=20 order to spare eloquent cortices, and the limits of resection. Moreover, = the use=20 of preoperative maps can make intraoperative mapping safer and more=20 efficient.

Blood-oxygen-level-dependent (BOLD) fMRI,43=20 a functional neuroimaging technique that maps the brain by detecting=20 perfusion-related changes that are coupled to cognitive tasks (and, = therefore,=20 to neuronal activity), has become the predominant functional = neuroimaging=20 technique (Figure=20 2). Recent technological advances, including increasing the magnetic = resonance field strength, improved sequence and task design and = selection, and=20 superior analytical techniques, have made fMRI increasingly sensitive = and=20 reliable.44,=20 45,=20 46,=20 47,=20 48,=20 49=20 Increasing the field strength provides improved signal-to-noise ratio = and=20 spatial resolution, and more-rapid imaging=97a particularly important=20 consideration in patients with low-grade glioma who might not tolerate = prolonged=20 imaging sessions. FitzGerald and colleagues found that fMRI was highly = sensitive=20 (81=9692%), but not very specific (0=9653%), for intraoperative = identification of=20 essential language areas.50=20 The low specificity (i.e. fMRI showed activation of areas that were not=20 essential for linguistic tasks) suggests that fMRI could direct the = surgeon to=20 areas of interest so that it might be determined whether activated = cortices are=20 'essential' or 'nonessential'=97thereby obviating the need to map the = entirety of=20 the exposed cortex, but still necessitating intraoperative cortical = mapping to=20 guide resection. Nevertheless, the relationship between the use of fMRI = maps and=20 clinical outcomes remains uncharacterized. Moreover, the question of = whether=20 perfusion-related responses are adversely affected by an adjacent tumor = has not=20 yet been answered.

Figure=20 2 Functional MRI scan for preoperative planning.

Rather than relying on anatomical landmarks for functional = localization,=20 functional MRI has enabled surgeons to precisely localize brain function = and to=20 use this information to plan for safer resection of low-grade glioma. = (A)=20 Axial, (B) sagittal and (C) coronal T1 MRI scans with = overlying=20 red areas of activation demonstrate the regions of the brain activated = during=20 right-hand motor activity. These images can be fused to create a=20 three-dimensional rendering of functional anatomy to guide the surgeon = and make=20 surgery safer.

Full=20 figure and legend (47K)Figures=20 & Tables indexDownload=20 Power Point slide (103K)

MSI fuses magnetoencephalography and MRI, projecting the = extrapolated source localization of the magnetoencephalographic signals = onto a=20 co-registered anatomical MRI scan. As in other mapping techniques, MSI = maps are=20 generated by comparing 'activity' during a resting state with that = detected=20 during the performance of a specific task. Like fMRI, MSI correlates = well with=20 intraoperative maps.51,=20 52=20 Moreover, MSI can be used to identify the 25=9646% of patients with = gliomas who=20 are at risk of neurological deficit from surgical intervention.53,=20 54,=20 55=20 Patients with MSI signals within 5 mm of a tumor are considered to be at = high=20 risk of surgery-induced neurological deficit, those with activations = between 6=20 mm and 10 mm from the tumor are slated for subtotal resection, and those = with=20 localizations greater than 10 mm from the tumor are deemed candidates = for=20 GTR.54

Diffusion tensor imaging (DTI) is an MRI technique that = creates=20 probabilistic maps of white matter pathways on the basis of voxel = anisotropy, a=20 measure of the preferential direction of diffusion of water. DTI can = identify=20 white matter pathways that have been either infiltrated or displaced by = tumors.=20 Preclinical studies suggest that DTI will have an increasingly important = role in=20 the planning of glioma surgery; the technique can identify white matter = pathways=20 that should be spared during surgery in order to ensure that functional = cortices=20 (as identified by other techniques) are not 'disconnected' from their = respective=20 projection areas.56=20 Kamada and colleagues verified that preoperative cortical and = subcortical maps=20 generated by a combination of fMRI, MSI and DTI are predictive and can = be=20 confirmed by intraoperative cortical and subcortical stimulation = mapping.57

In the operating room, technological advances have made = cortical=20 and subcortical stimulation mapping easier to implement, making these = techniques=20 a more routine part of neurosurgery. In view of its reliability in = predicting=20 postoperative outcomes, stimulation mapping is considered to be the gold = standard for neurosurgical brain mapping. In this approach, the brain is = mapped=20 by either activating the tissue of interest, as in motor mapping, or by=20 temporarily inducing deficits, as in language mapping. To evaluate the = effect of=20 stimulation mapping on the efficacy and safety of surgery for low-grade = glioma,=20 Duffau and colleagues compared a retrospective series of 100 patients = who were=20 operated on without guidance from intraoperative mapping (between 1985 = and 1996)=20 and a prospective series of 122 patients who were operated on with = concurrent=20 use of electrocortical stimulation mapping (between 1996 and = 2003).58=20 The latter group had a significantly lower rate of severe permanent = deficits=20 (6.5% vs 17%), a higher rate of GTR and subtotal resections (25% and 51% = vs 6%=20 and 37%, respectively), and a survival advantage, compared with the = former=20 group.58=20 Moreover, the authors found that the definition of 'operability' changed = considerably between the two series: the percentage of tumors operated = on within=20 eloquent cortices increased from 35% to 62%. Stimulation of subcortical = white=20 matter tracts has also become an increasingly important adjunct to=20 intraoperative mapping, permitting the surgeon to spare descending = pathways and=20 predict postoperative morbidity.59=20 Patients in whom subcortical motor tracts are identified in the resected = areas=20 are significantly more likely to experience temporary or permanent motor = deficits than those in whom subcortical motor pathways cannot be = identified in=20 these areas.60

In addition to stimulation mapping, advanced = intraoperative image=20 guidance techniques can now provide a highly accurate real-time=20 three-dimensional 'road map' to an individual patient's brain, which = enables=20 surgeons to operate more safely in the face of distorted anatomy. These = road=20 maps are created by registering anatomical or artificial landmarks = (fiducials)=20 on a high-resolution preoperative MRI scan of the patient's head and = pairing=20 them with corresponding positions on the patient's head after it is = positioned=20 for surgery. Current frameless stereotactic neuronavigation devices use = optical=20 triangulation or low-frequency electromagnetic fields to determine the = location=20 of an instrument within the operative field. Intraoperative image = guidance=20 provides ongoing feedback with respect to regional anatomical = relationships,=20 location of normal tissues that must be preserved, and extent of = resection. This=20 feedback during surgery can be particularly useful for low-grade glioma, = in=20 which the delineation between tumor and surrounding white matter is = indistinct.=20 Lumenta et al. described a series of 40 patients (21 of whom had = glial=20 neoplasms) who underwent resection of deep-seated intracerebral lesions = guided=20 by neuronavigation and cortical mapping. Complete resection was possible = in all=20 but three of the patients, and permanent neurological deficits were only = noted=20 in two.61=20 Although excellent for initial planning, the reliability of maps from=20 preoperative MRI for intraoperative guidance decreases during surgery = owing to=20 'brain shift', a phenomenon attributable to tumor removal, ongoing = cerebrospinal=20 fluid loss, and brain edema.62,=20 63

The limitations of intraoperative image guidance have = been=20 partially overcome with the advent of intraoperative magnetic resonance = systems=20 that provide real-time imaging of the brain in its intraoperative = position.=20 Black and colleagues highlighted the important contribution of = intraoperative=20 MRI to successful tumor resection with the observation that, in over = one-third=20 of cases, the surgeon's judgment of the extent of GTR was deemed = incorrect by=20 intraoperative MRI, thus prompting further surgical resection.64=20 Similarly, Wirtz et al. found that implementation of = intraoperative MRI=20 resulted in a significantly higher rate of GTR (67% compared with 38% = without=20 the use of intraoperative MRI), which was associated with a significant = increase=20 in survival times.65=20 Claus and co-workers found that patients who underwent surgical = resection of=20 low-grade gliomas with concurrent intraoperative MRI guidance had better = 1-year,=20 2-year and 5-year survival rates than those reported in the = CBTRUS.66=20 The authors also suggested a possible association between GTR using=20 intraoperative MRI guidance and prolonged PFS and OS (although this = correlation=20 did not achieve significance). Further studies of this topic are = warranted,=20 especially in light of the ongoing interest in defining the effect of = GTR on=20 outcomes in low-grade glioma.

Notwithstanding the technological advances that have = made surgical=20 resection a viable option in a greater number of patients with low-grade = glioma,=20 it is still recognized that GTR might not be possible in all cases. The=20 radiographic appearance of a low-grade glioma necessarily dictates its=20 amenability to resection. Low-grade gliomas might involve critical = structures,=20 including the corpus callosum, thalamus or basal ganglia, might be well=20 circumscribed or infiltrative, and might be unilateral or bilateral. = Predictors=20 of incomplete tumor resection include diffuse tumor margin on = T2-weighted MRI,=20 oligodendroglioma or oligoastrocytoma histopathological tumor type, = large tumor=20 volume, and tumor involving the corpus callosum, corticospinal tract, = insular=20 lobe, middle cerebral artery, motor cortex, optic radiation, visual = cortex, or=20 basal ganglia.67=20 In general, unilateral, well-circumscribed, cortex-based lesions are = ideal=20 candidates for resection. Nonetheless, recent reports suggest that = tumors that=20 were once considered unresectable, owing to involvement of the corpus = callosum,=20 insula or eloquent language cortices, can now undergo resective = procedures=20 without the risk of sequelae being increased.68,=20 69

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Future trials

Given the advances in modern neurosurgical and = neuroimaging=20 techniques, which permit safer surgical resections and more-accurate = assessment=20 of the extent of resection than was previously possible, neurosurgeons = and=20 neuro-oncologists might finally be in a position to accurately explore = the=20 extent to which aggressive resection improves the prognosis of low-grade = glioma.

Planning a trial to compare conservative and aggressive = surgical=20 management is complex and poses several challenges. The trial should = ideally be=20 randomized, but ethical concerns have limited this approach. A = randomized trial=20 was proposed to the American College of Surgeons Oncology Group = (ACOSOG), in=20 which patients with incidental low-grade glioma (or those well = controlled with a=20 single antiepileptic agent after a single seizure) would be randomly = allocated=20 to either biopsy or surgical resection. This trial was, however, = rejected over=20 concerns that the literature might already contain sufficient evidence = to=20 support resection. Instead of a randomized design, a trial must, = therefore, be=20 designed with a prospective cohort construction. To obtain adequate = accrual and=20 follow-up, such a trial would require the enrollment of at least 1,100 = patients,=20 who would have to be observed for approximately 10 years (or until=20 death).70=20 In light of the low incidence of low-grade glioma (2,000=963,000 cases = per year in=20 the US), enrollment of a sufficient number of patients would necessitate = multi-institutional=97if not multinational=97cooperation. To reduce = institutional=20 bias, data must be collected and analyzed at a central location. To = ensure the=20 validity of the trial, the extent of resection would have to be = evaluated=20 objectively by unbiased investigators (i.e. investigators not involved = with=20 patient care and blinded to patient outcomes) who would use volumetric=20 measurements from T2-weighted or FLAIR MRI sequences. Primary end points = should=20 include OS, PFS, and QOL (including assessments of neurocognitive = function).=20 Pre-planned statistical analyses should account for known prognostic = factors,=20 including age, preoperative tumor size, and histopathological subtype = (including=20 1p and 19q deletion status). Moreover, analyses should take into account = factors=20 that limit the success of GTR, including diffuse tumor margin on = T2-weighted MRI=20 and involvement of eloquent areas (e.g. visual cortex and motor cortex). = Finally, analyses must account for adjunctive therapies, including = fractionated=20 radiotherapy and chemotherapy. Interim analyses should be planned in = case either=20 biopsy or surgical resection proves to be superior on early analysis. = Clearly,=20 the coordination, data collection and statistical analysis that would be = involved in such a trial would be technically difficult, but this method = might=20 be the only means of definitively answering the question regarding the = role of=20 surgical resection in the management of low-grade glioma.

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Conclusions

Although a 'wait-and-see' policy might not adversely = affect=20 patients with low-grade glioma, the emergence of novel therapeutic = strategies=20 has increased the importance of obtaining tissue for both histological = and=20 cytogenetic characterization, so as to optimize patient management. = Although the=20 benefit of tissue acquisition by either biopsy or cytoreductive surgery = seems=20 indisputable, the precise role of surgical resection=97especially in = patients=20 without mass effect or symptoms of intracranial hypertension=97remains = unclear.=20 The literature provides modest evidence that surgery improves patient = outcomes=20 by reducing tumor burden. Nonetheless, it is not possible to devise a = prescribed=20 treatment algorithm on the basis of the current level of evidence. Until = prospective trials have been conducted and analyzed, neuro-oncologists = and=20 neurosurgeons must continue to individualize the evaluation and = treatment of=20 low-grade glioma on the basis of symptomatology, patient and tumor=20 characteristics, and patient preference.

Key points

  • Approximately 2,000=963,000 low-grade gliomas are diagnosed in the = US every=20 year, resulting in considerable morbidity and inevitable death
  • Management options for low-grade glioma include observation, = radiotherapy,=20 chemotherapy and surgical resection; the role of surgical resection is = particularly controversial
  • The literature provides modest evidence that surgery improves = outcomes by=20 reducing tumor burden, but there is a paucity of class I evidence
  • Advances in neurosurgical and neuroimaging techniques have made = surgical=20 resection of low-grade gliomas a safe option for an increasing number = of=20 patients
  • In light of recent advances, the time might be right to = effectively and=20 accurately assess the effect of aggressive surgical resection on the = prognosis=20 of low-grade glioma

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Acknowledgments

D=E9sir=E9e Lie, University of California, Irvine, CA, = is the author=20 of and is solely responsible for the content of the learning objectives, = questions and answers of the Medscape-accredited continuing medical = education=20 activity associated with this article.

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The authors declared no competing interests.

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Nature Clinical Practice Neurology

ISSN: 1745-834X

EISSN: 1745-8358

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url(/common/includes/header/images/logon.gif) no-repeat right center; = PADDING-BOTTOM: 0px; TEXT-TRANSFORM: uppercase; COLOR: #b1062e; = PADDING-TOP: 0px; LETTER-SPACING: -0.1em; TEXT-DECORATION: none } #head-er .logon A.login:hover { BACKGROUND: url(/common/includes/header/images/logon_over.gif) = no-repeat right center; TEXT-DECORATION: underline } #head-er .logon A.login:active { BACKGROUND: url(/common/includes/header/images/logon.gif) no-repeat = right center } #head-er .logon A.logoff { PADDING-RIGHT: 15px; PADDING-LEFT: 15px; FONT-WEIGHT: bold; BACKGROUND: = url(/common/includes/header/images/logoff.gif) no-repeat right center; = PADDING-BOTTOM: 0px; TEXT-TRANSFORM: uppercase; COLOR: #b1062e; = PADDING-TOP: 0px; LETTER-SPACING: -0.1em; TEXT-DECORATION: none } #head-er .logon P { MARGIN: 0px } #head-er .logon .user { FONT-WEIGHT: bold } #head-er .logon .inst { FONT-WEIGHT: bold } #head-er .image-user-services-wrap { FLOAT: left; WIDTH: 100%; BACKGROUND-COLOR: #d6335c } #head-er 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TEXT-DECORATION: none } MAP.journal-nav UL LI A.on { COLOR: #fff; BACKGROUND-COLOR: #c00 } MAP.journal-nav UL LI A.on:visited { COLOR: #fff; BACKGROUND-COLOR: #c00 } MAP.journal-nav UL LI A.submission { PADDING-LEFT: 20px! important; BACKGROUND: = url(/common/images/online_submissions.gif) no-repeat left center } MAP.journal-nav UL LI UL.subnav { BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; = PADDING-BOTTOM: 0px; MARGIN: 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: = none; TEXT-ALIGN: left } MAP.journal-nav UL LI UL.subnav LI { BACKGROUND: url(/common/images/nav_dots2.gif) #fafafa no-repeat 11px = 5px; BORDER-BOTTOM-WIDTH: 0px; MARGIN: 0px } MAP.journal-nav UL LI UL.subnav LI.on { BACKGROUND: url(/common/images/nav_dots1.gif) #c00 no-repeat 11px 5px; = BORDER-BOTTOM: #fafafa 1px solid } * HTML MAP.journal-nav UL LI UL.subnav A { PADDING-RIGHT: 10px! important; PADDING-LEFT: 20px! important; = PADDING-BOTTOM: 2px! important; PADDING-TOP: 2px! important } MAP.journal-nav UL 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