|Year : 2009 | Volume
| Issue : 2 | Page : 120-126
The role of surgery in the management of intracranial gliomas: Current concepts
OM Nunez1, HJ Seol2, JT Rutka3
1 Department of Neurosurgery, University Hospital "Abel Santamaria", Pinar del Rio, Cuba
2 Arthur and Sonia Labatt Brain Tumor Research Centre, Hospital for Sick Children, Toronto, Canada; Department of Neurosurgery, Kangwon National University College of Medicine, Chuncheon, Korea
3 Arthur and Sonia Labatt Brain Tumor Research Centre, Hospital for Sick Children, Toronto, Canada
J T Rutka
Arthur and Sonia Labatt Brain Tumor Research Centre, Hospital for Sick Children, Toronto, Canada
Source of Support: None, Conflict of Interest: None
The role of surgery in the management of human gliomas has been controversial. The results from numerous neurosurgical series are inconsistent. The current adjuvant therapies have facilitated treatment of patients, and have rendered neurosurgical removal without morbidity or mortality more commonplace than ever before. Here, we investigated the role of surgery in the management of adults with low- and high-grade gliomas. Even though there is substantial evidence which claims that surgery per se has a role to play in extending patient survival, there is a paucity of randomized clinical trials on this subject, and little in the way of Class II data to support these claims. However, this should not divert patients away from surgery, because there may be additional benefits from a concerted effort to remove a tumor completely. At the present time, it seems best that clinicians continue to individualize patient treatment based on a myriad of factors that relate to the patient, the patient's tumor, and the known biology of the disease.
Keywords: Adjuvant therapies, advance in neurosurgery, extension of resection, glioma, surgery, survival
|How to cite this article:|
Nunez O M, Seol H J, Rutka J T. The role of surgery in the management of intracranial gliomas: Current concepts. Indian J Cancer 2009;46:120-6
| » Introduction|| |
Gliomas are the most common primary tumors of the central nervous system (CNS), representing approximately 50% of the newly diagnosed brain tumors. According to the 2007 World Health Organization (WHO) classification, there are many different types of gliomas: Astrocytic, oligodendroglial, mixed oligoastrocytic tumors, ependymomas, and choroid plexus tumors.  Of these, astrocytomas, have the highest incidence. ,
The classification of human gliomas includes both histological features such as nuclear atypia, mitotic figures, microvascular proliferation and focal pseudopalisading necrosis,  and the separation into four grades (I-IV), with low-grade tumors being grades I and II, and high-grades tumors, grades III (anaplastic tumors) and IV (glioblastoma). This grading system has proved most accurate in predicting the clinical outcome.
The goals of glioma surgery are: To obtain a tissue sample for diagnosis; to decrease tumor mass; to relieve neurological symptoms; and to provide time so that other treatments, such as, cranial irradiation and chemotherapy can be performed.
The biology, clinical , and outcome are different for low- and high-grade gliomas in adults, but the treatments for these neoplasms are somewhat similar. Cranial irradiation after surgical debulking has been a mainstay of therapy in a majority of cases. Despite the advances in the care of patients with gliomas these past 15 years, surgery still plays an important and decisive role in the management of these patients. Here we discuss the current concepts on gliomas in adults, including natural history studies, surgical intervention, biopsy versus resection, impact of the extent of resection, impact of adjuvant therapies, molecular tools, and some recent advanced techniques, with which surgery has become more safe and predictable.
| » Low Grade Gliomas|| |
Low-grade gliomas (LGGs) are typically classified as WHO grade I and II neoplasms and include pilocytic astrocytomas, diffuse astrocytomas, oligodendrogliomas, ependymomas, and mixed gliomas. However, LGGs are understandably a heterogeneous group which is clinically and molecularly diverse. Therefore, we will limit our discussion here to WHO grade II diffuse astrocytomas, oligodendrogliomas, and mixed gliomas, which share similar characteristics of clinical manifestations, with invasive and malignant potential. 
Low-grade gliomas are generally relatively slow-growing primary brain tumors. However, they may exhibit a diverse clinical behavior. Many patients present with only seizures and are neurologically stable for a prolonged period of time. However, others may show functional deficits or signs of increased intracranial pressure. The benefits of various interventions including radiotherapy, chemotherapy, and surgical resection, have been described, but the role of the extent of surgery remains unclear. At this time, there is no consensus on the policy of surgical treatment for LGG. Either biopsy, subtotal or total excision can be undertaken, given the tumor's location, the patient's age, and the safety of performing surgery.
| » High Grade Gliomas|| |
High Grade Gliomas (HGGs) are also called "malignant gliomas." These tumors represent the most common primary brain tumor in the adult population. For HGGs, the incidence is 5 to 10 per 100,000 persons, and the median survival is about two to three years for WHO grade III and ten 10 to twelve 12 months for grades IV. , The term glioblastoma multiforme (GBM), was introduced by Mallory in 1914, and is still used at the present time to depict the most malignant of intracranial glial tumors. 
Some controversies still exist regarding the surgical treatment of HGGs. For the last 30 years, the neurosurgery community has debated the issue of the extent of resection. In actuality, aggressive resections began when Walter Dandy performed the first hemispherectomy in 1928, in order to achieve the "total" removal of an intracranial glioma.  Despite this very aggressive approach, all patients succumbed from the disease retained in the hemisphere. This illustrates the highly invasive and infiltrative potential of GBMs. Total resection is impossible in most cases, especially when tumors are situated in eloquent areas. , Today, even with a near-total resection, the survival time of most patients hovers around 12 months. In some series, gross total resection of over 98% of the tumor, followed by chemotherapy and radiotherapy, may offer some improvement in the overall survival. ,,,,,,
| » Neurosurgical Adjuncts to Overcome Morbidity|| |
Historically, intraoperative electrocortical stimulation has proven to be the gold standard in glioma surgery for the avoidance of postoperative neurological deterioration. Advances in brain mapping techniques have gradually emerged and are part of the clinician's armamentarium to supplement clinical and radiological findings for preoperative planning. Preoperative functional magnetic resonance imaging (fMRI) enables the definition of the cortical functional areas and their proximity to the tumor tissue, and can provide global preoperative information about the resectability of the tumor without causing neurological deterioration.  In addition, magnetic source imaging (MSI) with magnetoencephalography (MEG) provides a presurgical map, which clearly identifies the functional brain areas. As with fMRI, MSI correlates well with intraoperative cortical stimulation.  Diffusion tensor imaging (DTI) is a noninvasive method of studying the structure of human neuronal fibers and tracts. It captures the local water diffusion characteristics of tissues and models the 3D distribution of Brownian motion More Details as the diffusion tensor.  It is beneficial to delineate margins of the glioma because DTI is sensitive to the directional diffusion of water along white matter tracks.  Kamada et al,  suggested that preoperative cortical and subcortical maps generated by a combination of functional MRI, MSI, and DTI are predictive and can be confirmed by intraoperative cortical and subcortical stimulation mapping.
Intraoperatively, cortical or subcortical stimulation can be used to aggressively remove gliomas and avoid injury to long tract fiber pathways such as the corticospinal tract. Several retrospective series have shown that these techniques allow for aggressive neurosurgery for LGGs, within eloquent areas, and are associated with a decrease in the risk of neurological sequelae after surgery, and to an improvement in the extent of resection, with an impact on survival. ,,
Currently, frameless stereotactic neuronavigation is very helpful in approaching deep seated tumors and voiding errors in trajectory during surgery. However, neuronavigation is known to be associated with intraoperative brain shifts, which render the device somewhat problematic.  To solve the problem of brain shifts, intraoperative MRI has been invented to allow for continuous updating of imaging data, with compensation for the brain shift. Several retrospective articles have shown an increase in the extent of resection and survival time when intraoperative MRI is used. , As a result of advances in surgical techniques including pre- and intraoperative adjuncts and devices, more extensive surgery is now possible. In addition, greater resection of a tumor leads to less chance of sampling error, which can be problematic when biopsies are performed.
| » Adjuvant therapies|| |
While surgery alone is often used to treat grade I gliomas, including pilocytic astrocytomas, all the other grades will require some form of combination therapy including radiotherapy (RT), chemotherapy or both.
The identification of molecular markers, such as, the enzyme methylguanine methyltransferase (MGMT), epigenetically silenced in some tumors by methylation of the CpG island in the promoter region, has now been shown to be a predictive marker for treatment response to the chemotherapeutic agent, temozolomide (TMZ). Other molecular markers in clinical use today include the loss of heterozygosity on chromosomes 1p and 19q. If a patient with an anaplastic oligodendroglioma has this molecular phenotype, the overall survival is significantly better following treatment with chemotherapy. As more than 30% of GBM patients exhibit epidermal growth factor receptor (EGFR) amplification on their tumors, treatment with EGFR inhibitors, such as, gefitinib and erlotinib has been introduced. Currently, there is a phase II study which uses Cilentigide, an integrin inhibitor, for GBM. Other molecular treatments which are being examined are the use of an oral anti-vascular endothelial receptor (VEGF) tyrosine kinase inhibitor, and the use of wafers impregnated with chemotherapy, such as carmustine, to treat some patients after neurosurgical resection (GLIADEL).
| » Is Surgical Intervention Beneficial?|| |
A 'wait-and-see' policy has been considered for patients harboring typical LGG, especially with minimal symptoms or controllable seizures. This strategy may give some patients an overall improved quality of life (QOL) for some duration, because they are not exposed to the possible morbidity and mortality related to surgery. However, Scott et al, has shown that grading gliomas on the basis of imaging characteristics alone underestimated the degree of malignancy in one-third of the cases.  They advocated procuring of tissue for diagnosis whenever it was deemed safe and possible.
Moreover, even though contrast enhancement on MRI has long been believed to be a sign of malignancy, recent studies have suggested that contrast enhancement may occur in up to 40-60% of LGGs. , In the future, additional information may be gleaned through magnetic resonance spectroscopy and perfusion-weighted imaging, but at the moment, these techniques are still associated with significant error rates. ,
As well as a possible error in diagnosis, the expectant management of patients with LGGs can bring on other risks, such as, malignant degeneration, subsequent tumor growth, and irreversible neurological deficit. However, despite these theoretical risks, several retrospective series revealed that the timing of surgical intervention did not affect the rates of malignant transformation, overall survival, or QOL.  While there is still some debate on this matter, procuring a tissue diagnosis by surgical intervention may be a reasonable first stem in the management of LGG patients, irrespective of their site of origin. Standard therapy for patients with progressive, symptomatic LGG remains fractionated radiotherapy (RT) after surgical intervention, although several clinical trials using chemotherapy, such as, TMZ before or after RT in LGG, have recently shown some effect. 
For HGGs the policy of 'wait-and-see' has never been considered, even for tumors located in deep or eloquent areas. For GBM patients with multifocal disease, the use of biopsy-only has been reported with poor survival time in the pre-temozolomide era,  with a series reporting around 30% one-year survival, with biopsy alone. ,,,,
A small prospective series by Schneider et al ,  [Table 1] showed a correlation between resection and survival time. Nevertheless, physicians still considering aggressive surgical options for patients with HGGs need to take into account the importance of relief of the symptoms and the need to get patients to their adjuvant therapies to improve survival and not be hindered by neurological morbidity. We summarize only three of the series reported after 2000, showing some significant improvement in survival with aggressive resection of HGGs [Table 1].
| » The Extent of Surgical Resection|| |
Historically, biopsy has been used for tumors located adjacent to or deep within eloquent cortices. While stereotactic biopsy is chosen for patients with deep-seated lesions, resection is reserved for those with superficial lesions. Sometimes, brain mapping before surgery is useful, especially in the eloquent cortex. On the other hand, craniotomy and resection have an advantage for patients with significant mass effect, which results in increased intracranial pressure or neurological deficit and for those with symptomatic refractory epilepsy.  However, several studies show the possibility of misdiagnosis or bias of sampling. They even suggest that stereotactic biopsy may be an additional, even unnecessary procedure in the management of glioma, because it added an additional 0.9% and 4% risk of mortality and major morbidity, in each, and led to an inaccurate diagnosis in one-third to one-half of the cases. , Despite discrepancies between histopathology and clinical phenotype, some studies have shown that appropriate treatment was administered in more than 90% of the LGG cases.  From a pure risk taking vantage point, stereotactic biopsy may be more beneficial than craniotomy. In contrast to biopsy, surgical resection can minimize the likelihood of sampling error, but it exposes the patients to a higher risk.  Although not curative, total resection provides multiple benefits, including reduction in cell number, increased efficacy of adjuvant therapies, and symptomatic relief. Interestingly, studies have shown that a large preoperative tumor size is a poor prognosis factor. 
Although there are many retrospective data [Table 2] showing the benefit of extensive surgery for overall survival or QOL in LGG, ,,,,, these are limited by the retrospective nature of these studies. There have been two prospective trials [Table 2], which showed the benefit of extensive surgery on overall survival or progression-free survival by univariate analysis. , Despite consistent findings on univariate analysis, on multivariate analysis, the benefits of extensive surgery were minimal in these studies.
To date there is no class I evidence supporting radical tumor removal in LGGs. In addition, several articles recently revealed that brain MRI has a serious limitation to delineating the true tumor extent when methionine positron emission tomography (PET) or fluorodeoxyglucose (FDG) PET were used. , Nonetheless, many neurosurgeons opt for extensive surgery in LGGs. The definition of the extent of resection has been evaluated on the basis of the surgeon's impressions alone (which frequently overestimate the extent of resection), while in others it has been assessed by CT or postoperative T2-weighted or fluid-attenuated inversion-recovery (FLAIR) MRI images.  Obviously future trials should use MRI for evaluating the extent of resection rather than relying on the neurosurgeon's opinion.
Interestingly, recent studies suggested neoadjuvant temozolomide chemotherapy before surgery could result in shrinkage of the unresectable tumor. , Even though a couple of nonrandomized studies showed even temozolomide chemotherapy alone shrank a tumor volume enough to consider further surgery, , the real effects, benefits, and risks are still being investigated by the European Organization for Research and Treatment of Cancer (EORTC) / National Cancer Institute of Canada (NCIC).
The impact of the extension of surgical resection on HGGs had been studied extensively. In 11 series reported after 2000, seven of them showed statistics in favor of more extensive resections, whereas, in four this was not the case [Table 3].
The key point here is related to the type of analyses used to determine the extent of resection. Six studies used nonvolumetric analyses, relying on the surgeon's estimation of the extent of resection. In the five that used volumetric analyses, they did show survival advantages with extensive resections. However, once again, these were mostly retrospective studies, influenced by biological factors, including age and Karnofsky performance scores, among other biases that were introduced.
In 2006 Stummer et al . performed a randomized controlled multicenter phase III trial with the use of 5-aminolevulinic acid (ALA) for Fluorescence-guided glioma surgery,  showing 65% "complete resection" compared to 36% in the control group, showing an accurate estimation of the value of the extent of resection for HGG. How this technique ultimately relates to overall patient survival remains to be determined.
| » Conclusions|| |
Our review investigated numerous reports in the literature supporting the importance of surgery for the treatment of low- and high-grade gliomas. Many articles showed the impact of more extensive and aggressive resections. However, most of the studies are retrospective or multivariate and nonrandomized in nature. Today, the management of these patients relies on combined therapies, which have been evolving over the last two decades. Concerning the role of surgery in patients with LGGs and HGGs, it is hoped that definitive trials lie just ahead. For the moment, clinicians should continue to individualize the management of their patients, taking into account the patient's age, tumor location, imaging studies, pathology of the tumor, and prognostic molecular markers. 
| » Acknowledgments|| |
This study was partly supported by the Kangwon National University (Ho Jun Seol), the Wiley Fund, and Brainchild, at the Hospital for Sick Children.
| » References|| |
|1.||Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al . The 2007 WHO classification of tumors of the central nervous system. Acta Neuropathol 2007;114:97-109. |
|2.||Legler JM, Ries LA, Smith MA, Warren JL, Heineman EF, Kaplan RS, et al . Brain and other central nervous system cancers: Recent trends in incidence and mortality. J Natl Cancer Inst 1999;91:2050-1. |
|3.||Wrensch M, Minn Y, Chew T, Bondy M, Berger MS. Epidemiology of primary brain tumors: current concepts and review of the literature. Neuro Oncol 2002;4:278-99. |
|4.||Sehati N, Liau LM. Adjuvant treatment for gliomas. Contemp Neurosurg 2003;25:1-9. |
|5.||Pouratian N, Asthagiri A, Jagannathan J, Shaffrey ME, Schiff D. Medscape: Surgery Insight: The role of surgery in the management of low-grade gliomas. Nat Clin Pract Neurol 2007;3:628-39. |
|6.||Scott CB, Scarantino C, Urtasun R, Movsas B, Jones CU, Simpson JR, et al . Validation and predictive power of Radiation Therapy Oncology Group (RTOG) recursive partitioning analysis classes for malignant glioma patients: A report using RTOG 90-06. Int J Radiat Oncol Biol Phys 1998;40:51-5. |
|7.||Davis FG, McCarthy BJ, Freels S, Kupelian V, Bondy ML. The conditional probability of survival of patients with primary malignant brain tumors: Surveillance, epidemiology, and end results (SEER) data. Cancer 1999;85:485-91. |
|8.||Mallory FB. Principles of Pathologic Histology. Philadelphia: WB Saunders, 1925, the first reported case of glioma resection was performed by Rickman Godlee in 1884 Bennett H, Godlee RJ. Excision of a tumor from the brain. Lancet 1884;2:1090-1. |
|9.||Dandy WE. Removal of right cerebral hemisphere for certain tumors with hemiplegia. JAMA 1928;90:823-5. |
|10.||Ammirati M, Vick N, Liao YL, Ciric I, Mikhael M. Effect of the extent of surgical resection on survival and quality of life in patients with supratentorial glioblastomas and anaplastic astrocytomas. Neurosurgery 1987;21:201-6. |
|11.||Sawaya R, Hammoud M, Schoppa D, Hess KR, Wu SZ, Shi WM, et al . Neurosurgical outcomes in a modern series of 400 craniotomies for treatment of parenchymal tumors. Neurosurgery 1998;42:1044-55. |
|12.||Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, et al . A multivariate analysis of 416 patients with glioblastoma multiforme: Prognosis, extent of resection, and survival. J Neurosurg 2001;95:190-8. |
|13.||Laws ER, Shaffrey ME, Morris A, Anderson FA Jr. Surgical management of intracranial gliomas-does radical resection improve outcome? Acta Neurochir Suppl 2003;85:47-53. |
|14.||Stark AM, Hedderich J, Held-Feindt J, Mehdorn HM. Glioblastoma-the consequences of advanced patient age on treatment and survival. Neurosurg Rev 2007;30:56-61. |
|15.||Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: A randomised controlled multicentre phase III trial. Lancet Oncol 2006;7:392-401. |
|16.||Mineo JF, Bordron A, Baroncini M, Ramirez C, Maurage CA, Blond S, et al . Prognosis factors of survival time in patients with glioblastoma multiforme: A multivariate analysis of 340 patients. Acta Neurochir (Wien) 2007;149:245-52. |
|17.||Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery 2008;62:753-64. |
|18.||Brem SS, Bierman PJ, Black P, Blumenthal DT, Brem H, Chamberlain MC, et al . Central nervous system cancers: Clinical practice guidelines in oncology. J Natl Compr Canc Netw 2005;3:644-90. |
|19.||Roessler K, Donat M, Lanzenberger R, Novak K, Geissler A, Gartus A, et al . Evaluation of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome. J Neurol Neurosurg Psychiatry 2005;76:1152-7. |
|20.||Gallen CC, Schwartz BJ, Bucholz RD, Malik G, Barkley GL, Smith J, et al . Presurgical localization of functional cortex using magnetic source imaging. J Neurosurg 1995;82:988-94. |
|21.||Berman JI, Berger MS, Mukherjee P, Henry RG. Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas. J Neurosurg 2004;101:66-72. |
|22.||Price SJ, Jena R, Burnet NG, Hutchinson PJ, Dean AF, Peρa A, et al . Improved delineation of glioma margins and regions of infiltration with the use of diffusion tensor imaging: an image-guided biopsy study. AJNR Am J Neuroradiol 2006;27:1969-74. |
|23.||Kamada K, Todo T, Masutani Y, Aoki S, Ino K, Morita A, et al . Visualization of the frontotemporal language fibers by tractography combined with functional magnetic resonance imaging and magnetoencephalography. J Neurosurg 2007;106:90-8. |
|24.||Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, et al . Intraoperative mapping of the subcortical language pathways using direct stimulations: An anatomo-functional study. Brain 2002;125:199-214. |
|25.||Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Van Effenterre R, et al . Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: A comparative study between two series without (1985-96) and with (1996-2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 2005;76:845-51. |
|26.||Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS. Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: Evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 2004;100:369-75. |
|27.||Nimsky C, Ganslandt O, Hastreiter P, Fahlbusch R. Intraoperative compensation for brain shift. Surg Neurol 2001;56:357-64. |
|28.||Wirtz CR, Knauth M, Staubert A, Bonsanto MM, Sartor K, Kunze S, et al . Clinical evaluation and follow-up results for intraoperative magnetic resonance imaging in neurosurgery. Neurosurgery 2000;46:1112-20. |
|29.||Claus EB, Horlacher A, Hsu L, Schwartz RB, Dello-Iacono D, Talos F, et al . Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer 2005;103:1227-33. |
|30.||Scott JN, Brasher PM, Sevick RJ, Rewcastle NB, Forsyth PA. How often are nonenhancing supratentorial gliomas malignant? A population study. Neurology 2002;59:947-9. |
|31.||Pace A, Vidiri A, Galiθ E, Carosi M, Telera S, Cianciulli AM, et al . Temozolomide chemotherapy for progressive low-grade glioma: Clinical benefits and radiological response. Ann Oncol 2003;14:1722-6. |
|32.||Law M, Yang S, Wang H, Babb JS, Johnson G, Cha S, et al . Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. AJNR Am J Neuroradiol 2003;24:1989-98. |
|33.||Spampinato MV, Smith JK, Kwock L, Ewend M, Grimme JD, Camacho DL, et al . Cerebral blood volume measurements and proton MR spectroscopy in grading of oligodendroglial tumors. AJR Am J Roentgenol 2007;188:204-12. |
|34.||Reijneveld JC, Sitskoorn MM, Klein M, Nuyen J, Taphoorn MJ. Cognitive status and quality of life in patients with suspected versus proven low-grade gliomas. Neurology 2001;56:618-23. |
|35.||Stupp R, Hegi ME, van den Bent MJ, Mason WP, Weller M, Mirimanoff RO, et al . European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group: Changing paradigms: An update on the multidisciplinary management of malignant glioma. Oncologist 2006;11:165-80. |
|36.||Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al . European Organization for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96. |
|37.||Balaρa C, Capellades J, Teixidor P, Roussos I, Ballester R, Cuello M, et al . Clinical course of high-grade glioma patients with a "biopsy-only" surgical approach: A need for individualised treatment. Clin Transl Oncol 2007;9:797-803. |
|38.||Laws ER, Parney IF, Huang W, Anderson F, Morris AM, Asher A, et al . Glioma Outcomes Investigators. Survival following surgery and prognostic factors for recently diagnosed malignant glioma: Data from the Glioma Outcomes Project. J Neurosurg 2003;99:467-73. |
|39.||Jeremic B, Grujicic D, Antunovic V, Djuric L, Stojanovic M, Shibamoto Y. Influence of extent of surgery and tumor location on treatment outcome of patients with glioblastoma multiforme treated with combined modality approach. J Neurooncol 1994;21:177-85. |
|40.||Shinoda J, Sakai N, Murase S, Yano H, Matsuhisa T, Funakoshi T. Selection of eligible patients with supratentorial glioblastoma multiforme for gross total resection. J Neurooncol 2001;52:161-71. |
|41.||Schneider JP, Trantakis C, Rubach M, Schulz T, Dietrich J, Winkler D, et al . Intraoperative MRI to guide the resection of primary supratentorial glioblastoma multiforme: A quantitative radiological analysis. Neuroradiology 2005;47:489-500. |
|42.||Van Veelen ML, Avezaat CJ, Kros JM, van Putten W, Vecht C. Supratentorial low grade astrocytoma: Prognostic factors, dedifferentiation, and the issue of early versus late surgery. J Neurol Neurosurg Psychiatry 1998;64:581-7. |
|43.||Jackson RJ, Fuller GN, Abi-Said D, Lang FF, Gokaslan ZL, Shi WM, et al . Limitations of stereotactic biopsy in the initial management of gliomas. Neuro Oncol 2001;3:193-200. |
|44.||Aker FV, Hakan T, Karadereler S, Erkan M. Accuracy and diagnostic yield of stereotactic biopsy in the diagnosis of brain masses: Comparison of results of biopsy and resected surgical specimens. Neuropathology 2005;25:207-13. |
|45.||McGirt MJ, Villavicencio AT, Bulsara KR, Friedman AH. MRI-guided stereotactic biopsy in the diagnosis of glioma: Comparison of biopsy and surgical resection specimen. Surg Neurol 2003;59:277-81. |
|46.||Shaw E, Arusell R, Scheithauer B, O'Fallon J, O'Neill B, Dinapoli R, et al . Prospective randomized trial of low- versus high-dose radiation therapy in adults with supratentorial low-grade glioma: Initial report of a North Central Cancer Treatment Group/Radiation Therapy Oncology Group/Eastern Cooperative Oncology Group study. J Clin Oncol 2002;20:2267-76. |
|47.||Laws ER Jr, Taylor WF, Clifton MB, Okazaki H. Neurosurgical management of low-grade astrocytoma of the cerebral hemispheres. J Neurosurg 1984;61:665-73. |
|48.||Shaw EG, Daumas-Duport C, Scheithauer BW, Gilbertson DT, O'Fallon JR, Earle JD, et al . Radiation therapy in the management of low-grade supratentorial astrocytomas. J Neurosurg 1989;70:853-61. |
|49.||Philippon JH, Clemenceau SH, Fauchon FH, Foncin JF. Supratentorial low-grade astrocytomas in adults. Neurosurgery 1993;32:554-9. |
|50.||Karim AB, Maat B, Hatlevoll R, Menten J, Rutten EH, Thomas DG, et al . A randomized trial on dose-response in radiation therapy of low-grade cerebral glioma: European Organization for Research and Treatment of Cancer (EORTC) Study 22844. Int J Radiat Oncol Biol Phys 1996;36:549-56. |
|51.||Scerrati M, Roselli R, Iacoangeli M, Pompucci A, Rossi GF. Prognostic factors in low grade (WHO grade II) gliomas of the cerebral hemispheres: The role of surgery. J Neurol Neurosurg Psychiatry 1996;61:291-6. |
|52.||Bauman G, Lote K, Larson D, Stalpers L, Leighton C, Fisher B, et al . Pretreatment factors predict overall survival for patients with low-grade glioma: A recursive partitioning analysis. Int J Radiat Oncol Biol Phys 1999;45:923-9. |
|53.||Pignatti F, van den Bent M, Curran D, Debruyne C, Sylvester R, Therasse P, et al . European Organization for Research and Treatment of Cancer Brain Tumor Cooperative Group; European Organization for Research and Treatment of Cancer Radiotherapy Cooperative Group: Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 2002;20:2076-84. |
|54.||Miwa K, Shinoda J, Yano H, Okumura A, Iwama T, Nakashima T, et al . Discrepancy between lesion distributions on methionine PET and MR images in patients with glioblastoma multiforme: Insight from a PET and MR fusion image study. J Neurol Neurosurg Psychiatry 2004;75:1457-62. |
|55.||Pirotte B, Goldman S, Massager N, David P, Wikler D, Vandesteene A, et al . Comparison of 18F-FDG and 11C-methionine for PET-guided stereotactic brain biopsy of gliomas. J Nucl Med 2004;45:1293-8. |
|56.||Duffau H, Taillandier L, Capelle L. Radical surgery after chemotherapy: A new therapeutic strategy to envision in grade II glioma. J Neurooncol 2006;80:171-6. |
|57.||Voloschin AD, Louis DN, Cosgrove GR, Batchelor TT. Neoadjuvant temozolomide followed by complete resection of a 1p- and 19q-deleted anaplastic oligoastrocytoma: Case study. Neuro Oncol 2005;7:97-100. |
|58.||Van den Bent MJ, Taphoorn MJ, Brandes AA, Menten J, Stupp R, Frenay M, et al . Phase II study of first-line chemotherapy with temozolomide in recurrent oligodendroglial tumors: The European Organization for Research and Treatment of Cancer Brain Tumor Group Study 26971. J Clin Oncol 2003;21:2525-8. |
|59.||Buckner JC, Schomberg PJ, McGinnis WL, Cascino TL, Scheithauer BW, O'Fallon JR, et al . Aphase III study of radiation therapy plus carmustine with or without recombinant interferon-alpha in the treatment of patients with newly diagnosed high-grade glioma. Cancer 2001;92:420-33. |
|60.||Lamborn KR, Chang SM, Prados MD. Prognostic factors for survival of patients with glioblastoma: Recursive partitioning analysis. Neuro Oncol 2004;6:227-35. |
|61.||Brown PD, Maurer MJ, Rummans TA, Pollock BE, Ballman KV, Sloan JA, et al . A prospective study of quality of life in adults with newly diagnosed high-grade gliomas: The impact of the extent of resection on quality of life and survival. Neurosurgery 2005;57:495-504. |
|62.||Ushio Y, Kochi M, Hamada J, Kai Y, Nakamura H. Effect of surgical removal on survival and quality of life in patients with supratentorial glioblastoma. Neurol Med Chir (Tokyo) 2005;45:454-61. |
|63.||Stark AM, Nabavi A, Mehdorn HM, Blφmer U. Glioblastoma multiforme: Report of 267 cases treated at a single institution. Surg Neurol 2005;63:162-9. |
|64.||Nomiya T, Nemoto K, Kumabe T, Takai Y, Yamada S. Prognostic significance of surgery and radiation therapy in cases of anaplastic astrocytoma: Retrospective analysis of 170 cases. J Neurosurg 2007;106:575-81. |
|65.||Levin VA, Yung WK, Bruner J, Kyritsis A, Leeds N, Gleason MJ, et al . Phase II study of accelerated fractionation radiation therapy with carboplatin followed by PCV chemotherapy for the treatment of anaplastic gliomas. Int J Radiat Oncol Biol Phys 2002;53:58-66. |
|66.||Tortosa A, Viρolas N, Villà S, Verger E, Gil JM, Brell M, et al . Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer 2003;97:1063-71. |
|67.||Pope WB, Sayre J, Perlina A, Villablanca JP, Mischel PS, Cloughesy TF. MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol 2005;26:2466-74. |
|68.||Keles GE, Chang EF, Lamborn KR, Tihan T, Chang CJ, Chang SM, et al . Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg 2006;105:34-40. |
[Table 1], [Table 2], [Table 3]
|This article has been cited by|
||Principles of Surgery for Malignant Astrocytomas
| ||Eli T. Sayegh,Taemin Oh,Shayan Fakurnejad,Daniel E. Oyon,Orin Bloch,Andrew T. Parsa |
| ||Seminars in Oncology. 2014; 41(4): 523 |
|[Pubmed] | [DOI]|
||Gliomas of the pineal region
| ||Salima Magrini,Alberto Feletti,Elisabetta Marton,Pierluigi Longatti |
| ||Journal of Neuro-Oncology. 2013; 115(1): 103 |
|[Pubmed] | [DOI]|
||Neuro-oncology - A difficult problem in modern cancer management
| ||Ganguly, S. and Ray, A. |
| ||Journal of the Indian Medical Association. 2012; 110(8): 604-605 |
||Multiple craniotomies in the management of multifocal and multicentric glioblastoma
| ||Hassaneen, W. and Levine, N.B. and Suki, D. and Salaskar, A.L. and De Moura Lima, A. and McCutcheon, I.E. and Prabh, S.S. and Lang, F.F. and DeMonte, F. and Rao, G. and Weinberg, J.S. and Wildrick, D.M. and Aldape, K.D. and Sawaya, R. |
| ||Journal of Neurosurgery. 2011; 114(3): 576-584 |
||Survival analysis of low-grade glioma treated by postoperative radiotherapy
| ||Li, R. and Lan, S.-M. and Wang, H.-W. and Cao, J.-Z. and Ren, S.-H. and Luo, N. and Zhang, L. |
| ||Chinese Journal of Cancer Prevention and Treatment. 2010; 17(13): 1021-1024 |
||Multiple craniotomies in the management of multifocal and multicentric glioblastoma : Clinical article
| || |
| ||Journal of Neurosurgery. 2010; : 1 |
|[VIEW] | [DOI]|