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What Is the Advance of Extent of Resection in Glioblastoma Surgical Treatment—A Systematic Review

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What Is the Advance of Extent of Resection in Glioblastoma Surgical Treatment—A Systematic Review Wang et al. Chinese Neurosurgical Journal (2019) 5:2 https://doi.org/10.1186/s41016-018-0150-7 中华医学会神经外科学分会 CHINESE MEDICAL ASSOCIATION CHINESE NEUROSURGICAL SOCIETY REVIEW Open Access What is the advance of extent of resection in glioblastoma surgical treatment—a systematic review Lei Wang1,3†, Buqing Liang2†, Yan Icy Li1,4, Xiang Liu1, Jason Huang2 and Yan Michael Li1* Abstract Glioblastoma multiform (GBM) is the most common malignant brain tumor characterized by poor prognosis, increased invasiveness, and high relapse rates. The relative survival estimates are quite low in spite of the standard treatment for GBM in recent years. Now, it has been gradually accepted that the amount of tumor mass removed correlates with longer survival rates. Although new technique advances allowing intraoperative analysis of tumor and normal brain tissue and functional paradigms based on stimulation techniques to map eloquent areas have been used for GBM resection, visual identification of tumor margins still remains a challenge for neurosurgeons. This article attempts to review and summarize the evolution of surgical resection for glioblastomas. Keywords: Glioblastoma multiform (GBM), Biopsy, Extent of resection (EOR), Gross total resection (GTR) Background surgical treatment for GBM: (1) early biopsy, (2) gross Glioblastoma multiform (GBM) is the most common of total resection (GTR) for contrast-enhanced T1 mag- all malignant central nervous system (CNS) tumors, netic resonance imaging (MRI), and (3) Maximal-resec- which accounts for 47.1% of primary malignant brain tion for T2 magnetic resonance imaging or tumors, or about 12,390 new cases each year in the fluid-attenuated inversion recovery (FLAIR) abnormal- USA [1].SinceGBMisoneofthemostaggressivetypes ities. This article reviews the key historic literature and of cancer, relative survival estimates are quite low, with focuses on the evolution of surgical resection strategies only 5.1% of patients surviving 5 years after diagnosis for glioblastomas. [2]. The optimal treatment for GBM consists of the combination of surgical resection, radiation therapy, Early biopsy stage and chemotherapy [3–5]. The surgical resection for gli- One of the founding fathers of modern neurosurgery, oma aims at relieving mass effect, achieving cytoreduc- Walter Dandy [8], described the five right hemispherec- tion, and providing adequate tissue for histology and tomy procedures that he performed for the treatment molecular tumor characterization [3]. In the absence of of gliomas. Though he briefly mentioned the patholo- new neurological deficit, which are one of the prognos- gies for some of the cases, it is safe to judge from his tic factors in glioblastomas, higher volume of tumor description that a number of tumors possessed the mass resected correlates with longer survival in GBM characteristics of malignancy: spreading to the contra- patients [6, 7]. Furthermore, there is no controversy lateral side via corpus callosum, and recurrence in a about maximal resection which is beneficial for pa- short period of time. In the conclusion part, Dandy tient’s prognosis compared to biopsy or no surgery. In concluded that although this was a very aggressive op- general, there are three stages in the development of eration to be advised, it nevertheless offers much longer extension of life to patients compared to any other pos- * Correspondence: [email protected] sible form of treatment. Moreover, when the tumor † Lei Wang and Buqing Liang contributed equally to this work. cannot be completely resected, the procedure offers a 1Department of Neurosurgery and Radiology, University of Rochester Medical Center, 601 Elmwood Avenue, Rochester, NY 14642, USA treatment possibility otherwise not obtainable in certain Full list of author information is available at the end of the article tumors situated within the confines of the hemisphere. © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Wang et al. Chinese Neurosurgical Journal (2019) 5:2 Page 2 of 6 This can be considered as the first documented surgical reviewed relevant papers published from January 1996 procedure proposed for the treatment of malignant to December 2015. Adult patients (37 studies were re- gliomas. cruited) with newly diagnosed supratentorial GBM undergoing various EORs were analyzed and presented Contrast-enhanced T1 MRI for gross total objective overall or progression-free survival (PFS) data. resection The meta-analysis revealed that GTR probably in- With the advent of computed tomography (CT) and creases the likelihood of 1-year survival compared with magnetic resonance imaging (MRI), neurosurgeons subtotal resection (STR) by about 61%, 2-year survival were able to localize the tumor preoperatively, dramat- by about 19%, and progression-free survival at 12 ically improving surgical accuracy and lowering mor- months by 51%. In conclusion, GTR is favored in all pa- bidity and mortality. Moreover, the amount of tumor tients with newly diagnosed GBM. mass removed was no longer an approximate estimate of the neurosurgeons. Lacroix et al. [9] introduced the T2 MRI or FLAIR for maximal resection novel concept of a maximum extent of resection (EOR). Sherriff et al. [19] published a retrospective study to The study reported the result of a retrospective study discuss the optimal irradiation pattern for postopera- based on a cohort of 416 patients with histological tive patients with glioblastoma and suggested that proven GBM who underwent tumor resection and most of relapsing tumors occur within 2 cm of the ori- identified five prognostic predictors including age, Kar- ginal contrast-enhanced mass. Due to the invasive na- nofsky Performance Scale (KPS) score, extent of resec- ture of glioblastoma, it is not surprising that the tumor tion, and the degree of necrosis and enhancement on cells have already infiltrated beyond the contrast-en- preoperative MRI. Furthermore, they reached the con- hanced T1 MRI. Here comes a question: can we do clusion that resection of 89% or more of the tumor vol- better than gross total resection? When most of neuro- ume was necessary to obtain significant survival surgeons focused on gross total resection of contrast- improvement after surgery, while resection of 98% or enhanced T1 MRI, Li et al. [20] pushed the boundary more of the tumor volume is a significant independent of surgical resection procedures even further by per- predictor of survival in the multivariate analysis for the forming additional resection of the T2 MRI or FLAIR whole group. This paper established the concept that abnormality beyond the contrast-enhanced T1 MRI. the highest tumor volume resected leads to better prog- Their conclusion consists of two parts: (1) The median nosis in GBM. Specifically, resection of 89% or more of survival time for complete resection patients was sig- the tumor volume significantly increases patient’ssur- nificantly longer than that for incomplete resection pa- vival. Ten years later, Sanai et al. [10]lookedatacohort tients (15.2 months versus 9.8 months, p < 0.001). (2) of 500 newly diagnosed supratentorial GBM patients Resection of a significant portion (≥ 53.21%) of the T2 between 1997 and 2005 who underwent surgical resec- MRI or FLAIR abnormality region, if feasible and tion of the tumors followed by standard chemotherapy safely attempted, could have a beneficial impact on the and radiation therapy. Patients that had previous resec- survival of patients with GBM (median survival time tion or neoadjuvant therapy were excluded. Interest- 20.7 months versus 15.5 months, p < 0.001). At the ingly, it was demonstrated that as little as 78% EOR same time, Brian et al. [21]demonstratedthatthe resulted in a significant survival advantage. At almost molecular and cellular composition of nonenhanced the same time, Orringer et al. [11]showedthatEORis (NE) region differ significantly from those of the significantly affected by tumor location, size, and contrast-enhanced (CE) regions of GBM as determined neurosurgeon’s experience. This retrospective study by radiographically localized biopsies. CE samples had also revealed a relationship between EOR and survival significantly higher cellularity than NE samples. The indicating that EOR greater than 90% was associated NE region showed the histological features of diffusely with greater 1-year survival than EOR less than 90%. infiltrating glioma with neoplastic glial cells inter- However, it was objected that the mixed patient sam- mingled with nonneoplastic and reactive cells. This pling of both newly diagnosed and recurrent GBM dis- novel abnormal T2 MRI or FLAIR resection can be ruptedtheuniformityofthestudy. used to identify and access new therapeutic targets that The concept of maximum EOR stimulated active re- may be expressed by infiltrating glioma cells or by search and leads to several other publications on the re- nonneoplastic/reactive cells that play a key role in dis- lationship among gross total resection (GTR),
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