Perilesional resection technique of glioblastoma: intraoperative ultrasound and histological findings of the resection borders in a single center experience

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Abstract

Introduction

The surgical goal in glioblastoma treatment is the maximal safe resection of the tumor. Currently the lack of consensus on surgical technique opens different approaches. This study describes the “perilesional technique” and its outcomes in terms of the extent of resection, progression free survival and overall survival.

Methods

Patients included (n = 40) received a diagnosis of glioblastoma and underwent surgery using the perilesional dissection technique at “San Gerardo Hospital”between 2018 and 2021. The tumor core was progressively isolated using a circumferential movement, healthy brain margins were protected with Cottonoid patties in a “shingles on the roof” fashion, then the tumorwas removed en bloc. Intraoperative ultrasound (iOUS) was used and at least 1 bioptic sample of “healthy” margin of the resection was collected and analyzed. The extent of resection was quantified. Extent of surgical resection (EOR) and progression free survival (PFS)were safety endpoints of the procedure.

Results

Thirty-four patients (85%) received a gross total resection(GTR) while 3 (7.5%) patients received a sub-total resection (STR), and 3 (7.5%) a partial resection (PR). The mean post-operative residual volume was 1.44 cm ³ (range 0–15.9 cm ³).During surgery, a total of 76 margins were collected: 51 (67.1%) were tumor free, 25 (32.9%) were infiltrated. The median PFS was 13.4 months, 15.3 in the GTR group and 9.6 months in the STR-PR group.

Conclusions

Perilesional resection is an efficient technique which aims to bring the surgeon to a safe environment, carefully reaching the “healthy” brain before removing the tumoren bloc. This technique can achieve excellent tumor margins, extent of resection, and preservation of apatient’s functions.

Supplementary Information

The online version contains supplementary material available at 10.1007/s11060-022-04232-z.

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Most cited references 30

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Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma

Roger Stupp, Warren P Mason, Martin van den Bent … (2005)

Glioblastoma, the most common primary brain tumor in adults, is usually rapidly fatal. The current standard of care for newly diagnosed glioblastoma is surgical resection to the extent feasible, followed by adjuvant radiotherapy. In this trial we compared radiotherapy alone with radiotherapy plus temozolomide, given concomitantly with and after radiotherapy, in terms of efficacy and safety. Patients with newly diagnosed, histologically confirmed glioblastoma were randomly assigned to receive radiotherapy alone (fractionated focal irradiation in daily fractions of 2 Gy given 5 days per week for 6 weeks, for a total of 60 Gy) or radiotherapy plus continuous daily temozolomide (75 mg per square meter of body-surface area per day, 7 days per week from the first to the last day of radiotherapy), followed by six cycles of adjuvant temozolomide (150 to 200 mg per square meter for 5 days during each 28-day cycle). The primary end point was overall survival. A total of 573 patients from 85 centers underwent randomization. The median age was 56 years, and 84 percent of patients had undergone debulking surgery. At a median follow-up of 28 months, the median survival was 14.6 months with radiotherapy plus temozolomide and 12.1 months with radiotherapy alone. The unadjusted hazard ratio for death in the radiotherapy-plus-temozolomide group was 0.63 (95 percent confidence interval, 0.52 to 0.75; P<0.001 by the log-rank test). The two-year survival rate was 26.5 percent with radiotherapy plus temozolomide and 10.4 percent with radiotherapy alone. Concomitant treatment with radiotherapy plus temozolomide resulted in grade 3 or 4 hematologic toxic effects in 7 percent of patients. The addition of temozolomide to radiotherapy for newly diagnosed glioblastoma resulted in a clinically meaningful and statistically significant survival benefit with minimal additional toxicity. Copyright 2005 Massachusetts Medical Society.

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The 2021 WHO Classification of Tumors of the Central Nervous System: a summary

David N Louis, Arie Perry, Pieter Wesseling … (2021)

The fifth edition of the WHO Classification of Tumors of the Central Nervous System (CNS), published in 2021, is the sixth version of the international standard for the classification of brain and spinal cord tumors. Building on the 2016 updated fourth edition and the work of the Consortium to Inform Molecular and Practical Approaches to CNS Tumor Taxonomy, the 2021 fifth edition introduces major changes that advance the role of molecular diagnostics in CNS tumor classification. At the same time, it remains wedded to other established approaches to tumor diagnosis such as histology and immunohistochemistry. In doing so, the fifth edition establishes some different approaches to both CNS tumor nomenclature and grading and it emphasizes the importance of integrated diagnoses and layered reports. New tumor types and subtypes are introduced, some based on novel diagnostic technologies such as DNA methylome profiling. The present review summarizes the major general changes in the 2021 fifth edition classification and the specific changes in each taxonomic category. It is hoped that this summary provides an overview to facilitate more in-depth exploration of the entire fifth edition of the WHO Classification of Tumors of the Central Nervous System.

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Association of Maximal Extent of Resection of Contrast-Enhanced and Non–Contrast-Enhanced Tumor With Survival Within Molecular Subgroups of Patients With Newly Diagnosed Glioblastoma

Annette M. Molinaro, Shawn L Hervey-Jumper, Ramin A Morshed … (2020)

This multicenter cohort study assesses the association of maximal extent of resection of contrast-enhanced and non–contrast-enhanced tumor with survival among patients with newly diagnosed glioblastoma in different molecular subgroups to develop a new road map for cytoreductive surgery. Is maximal extent of resection of non–contrast-enhanced and contrast-enhanced tumor associated with improved survival within molecularly defined subgroups of newly diagnosed glioblastoma? In this cohort study of 761 patients with newly diagnosed glioblastoma, maximal resection of contrast-enhanced plus non–contrast-enhanced tumor was found to be associated with increased overall survival in younger patients, whereas maximal resection of contrast-enhanced tumor was associated with increased overall survival in older patients, regardless of molecular subgroup. These findings indicate that maximal extent of resection of the contrast-enhanced tumor in all patients and the contrast-enhanced plus non–contrast-enhanced tumor in younger patients is associated with increased overall survival regardless of molecular subgroup and suggest a need to reconsider surgical strategies for these patients in the molecular era. Per the World Health Organization 2016 integrative classification, newly diagnosed glioblastomas are separated into isocitrate dehydrogenase gene 1 or 2 ( IDH )–wild-type and IDH -mutant subtypes, with median patient survival of 1.2 and 3.6 years, respectively. Although maximal resection of contrast-enhanced (CE) tumor is associated with longer survival, the prognostic importance of maximal resection within molecular subgroups and the potential importance of resection of non–contrast-enhanced (NCE) disease is poorly understood. To assess the association of resection of CE and NCE tumors in conjunction with molecular and clinical information to develop a new road map for cytoreductive surgery. This retrospective, multicenter cohort study included a development cohort from the University of California, San Francisco (761 patients diagnosed from January 1, 1997, through December 31, 2017, with 9.6 years of follow-up) and validation cohorts from the Mayo Clinic (107 patients diagnosed from January 1, 2004, through December 31, 2014, with 5.7 years of follow-up) and the Ohio Brain Tumor Study (99 patients with data collected from January 1, 2008, through December 31, 2011, with a median follow-up of 10.9 months). Image accessors were blinded to patient groupings. Eligible patients underwent surgical resection for newly diagnosed glioblastoma and had available survival, molecular, and clinical data and preoperative and postoperative magnetic resonance images. Data were analyzed from November 15, 2018, to March 15, 2019. Overall survival. Among the 761 patients included in the development cohort (468 [61.5%] men; median age, 60 [interquartile range, 51.6-67.7] years), younger patients with IDH –wild-type tumors and aggressive resection of CE and NCE tumors had survival similar to that of patients with IDH -mutant tumors (median overall survival [OS], 37.3 [95% CI, 31.6-70.7] months). Younger patients with IDH– wild-type tumors and reduction of CE tumor but residual NCE tumors fared worse (median OS, 16.5 [95% CI, 14.7-18.3] months). Older patients with IDH –wild-type tumors benefited from reduction of CE tumor (median OS, 12.4 [95% CI, 11.4-14.0] months). The results were validated in the 2 external cohorts. The association between aggressive CE and NCE in patients with IDH –wild-type tumors was not attenuated by the methylation status of the promoter region of the DNA repair enzyme O6-methylguanine-DNA methyltransferase. This study confirms an association between maximal resection of CE tumor and OS in patients with glioblastoma across all subgroups. In addition, maximal resection of NCE tumor was associated with longer OS in younger patients, regardless of IDH status, and among patients with IDH –wild-type glioblastoma regardless of the methylation status of the promoter region of the DNA repair enzyme O6-methylguanine-DNA methyltransferase. These conclusions may help reassess surgical strategies for individual patients with newly diagnosed glioblastoma.

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Author and article information

Contributors

Carlo Giussani: carlo.giussani@unimib.it

Journal

Journal ID (nlm-ta): J Neurooncol

Journal ID (iso-abbrev): J Neurooncol

Title: Journal of Neuro-Oncology

Publisher: Springer US (New York )

ISSN (Print): 0167-594X

ISSN (Electronic): 1573-7373

Publication date (Electronic): 23 January 2023

Publication date PMC-release: 23 January 2023

Publication date (Print): 2023

Volume: 161

Issue: 3

Pages: 625-632

Affiliations

[1 ]GRID grid.7563.7, ISNI 0000 0001 2174 1754, Department of Medicine and Surgery, School of Medicine and Surgery, , University of Milano-Bicocca, ; Milan, Italy

[2 ]GRID grid.415025.7, ISNI 0000 0004 1756 8604, Neurosurgery, , Fondazione IRCCS San Gerardo dei Tintori, ; Via Pergolesi 33, 20900 Monza, MB Italy

[3 ]GRID grid.415025.7, ISNI 0000 0004 1756 8604, Neuropathology, , Fondazione IRCCS San Gerardo dei Tintori, ; Via Pergolesi 33, MB 20900 Monza, Italy

[4 ]GRID grid.415025.7, ISNI 0000 0004 1756 8604, Neurology, , Fondazione IRCCS San Gerardo dei Tintori, ; Via Pergolesi 33, 20900 Monza, MB Italy

[5 ]GRID grid.415025.7, ISNI 0000 0004 1756 8604, Radiotherapy, , Fondazione IRCCS San Gerardo dei Tintori, ; Via Pergolesi 33, 20900 Monza, MB Italy

[6 ]GRID grid.415025.7, ISNI 0000 0004 1756 8604, Neuroradiology, , Fondazione IRCCS San Gerardo dei Tintori, ; Via Pergolesi 33, 20900 Monza, MB Italy

[7 ]GRID grid.415025.7, ISNI 0000 0004 1756 8604, Neurointensive Care Unit, , Fondazione IRCCS San Gerardo dei Tintori, ; Monza, Italy

Article

Publisher ID: 4232

DOI: 10.1007/s11060-022-04232-z

PMC ID: 9992251

PubMed ID: 36690859

SO-VID: 2806bfdb-3c9e-4fce-82ba-ae72aed5b0c5

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 7 July 2022

Date accepted : 29 December 2022

Funding

Funded by: Università degli Studi di Milano - Bicocca

Open Access :

Open access funding provided by Università degli Studi di Milano - Bicocca within the CRUI-CARE Agreement.

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: brain tumors,neurosurgery,glioblastoma,extent of resection,progression free survival,en bloc resection,perilesional resection,intraoperative ultrasound

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: brain tumors, neurosurgery, glioblastoma, extent of resection, progression free survival, en bloc resection, perilesional resection, intraoperative ultrasound

Perilesional resection technique of glioblastoma: intraoperative ultrasound and histological findings of the resection borders in a single center experience

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Abstract

Introduction

Methods

Results

Conclusions

Supplementary Information

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Karger: Oncology

Most cited references 30

Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma

The 2021 WHO Classification of Tumors of the Central Nervous System: a summary

Association of Maximal Extent of Resection of Contrast-Enhanced and Non–Contrast-Enhanced Tumor With Survival Within Molecular Subgroups of Patients With Newly Diagnosed Glioblastoma

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