Comprehensive evaluation of treatment and outcomes of low-grade diffuse gliomas

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Abstract

Background

Low-grade gliomas affect younger adults and carry a favorable prognosis. They include a variety of biological features affecting clinical behavior and treatment. Having no guidelines on treatment established, we aim to describe clinical and treatment patterns of low-grade gliomas across the largest cancer database in the United States.

Methods

We analyzed the National Cancer Database from 2004 to 2015, for adult patients with a diagnosis of World Health Organization grade II diffuse glioma.

Results

We analyzed 13,621 cases with median age of 41 years. Over 56% were male, 88.4% were white, 6.1% were black, and 7.6% Hispanic. The most common primary site location was the cerebrum (79.9%). Overall, 72.2% received surgery, 36.0% radiation, and 27.3% chemotherapy. Treatment combinations included surgery only (41.5%), chemotherapy + surgery (6.6%), chemotherapy only (3.1%), radiation + chemotherapy + surgery (10.7%), radiation + surgery (11.5%), radiation only (6.1%), and radiotherapy + chemotherapy (6.7%). Radiation was more common in treatment of elderly patients, 1p/19q co-deletion (37.3% versus 24.3%, p<0.01), and tumors with midline location. Median survival was 11 years with younger age, 1p/19q co-deletion, and cerebrum location offered survival advantage.

Conclusions

Tumor location, 1p/19q co-deletion, and age were the main determinants of treatment received and survival, likely reflecting tumor biology differences. Any form of treatment was preferred over watchful waiting in the majority of the patients (86.1% versus 8.1%). Survival of low-grade gliomas is higher than previously reported in the majority of clinical trials and population-based analyses. Our analysis provides a real world estimation of treatment decisions, use of molecular data, and outcomes.

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Most cited references 28

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Radiation plus Procarbazine, CCNU, and Vincristine in Low-Grade Glioma.

Jan C. Buckner, Edward G. Shaw, Stephanie L. Pugh … (2016)

Grade 2 gliomas occur most commonly in young adults and cause progressive neurologic deterioration and premature death. Early results of this trial showed that treatment with procarbazine, lomustine (also called CCNU), and vincristine after radiation therapy at the time of initial diagnosis resulted in longer progression-free survival, but not overall survival, than radiation therapy alone. We now report the long-term results.

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Independent association of extent of resection with survival in patients with malignant brain astrocytoma.

Matthew McGirt, Kaisorn Chaichana, Muraya Gathinji … (2009)

With recent advances in the adjuvant treatment of malignant brain astrocytomas, it is increasingly debated whether extent of resection affects survival. In this study, the authors investigate this issue after primary and revision resection of these lesions. The authors retrospectively reviewed the cases of 1215 patients who underwent surgery for malignant brain astrocytomas (World Health Organization [WHO] Grade III or IV) at a single institution from 1996 to 2006. Patients with deep-seated or unresectable lesions were excluded. Based on MR imaging results obtained < 48 hours after surgery, gross-total resection (GTR) was defined as no residual enhancement, near-total resection (NTR) as having thin rim enhancement of the resection cavity only, and subtotal resection (STR) as having residual nodular enhancement. The independent association of extent of resection and subsequent survival was assessed via a multivariate proportional hazards regression analysis. Magnetic resonance imaging studies were available for review in 949 cases. The mean age and mean Karnofsky Performance Scale (KPS) score at time of surgery were 51 +/- 16 years and 80 +/- 10, respectively. Surgery consisted of primary resection in 549 patients (58%) and revision resection for tumor recurrence in 400 patients (42%). The lesion was WHO Grade IV in 700 patients (74%) and Grade III in 249 (26%); there were 167 astrocytomas and 82 mixed oligoastrocytoma. Among patients who underwent resection, GTR, NTR, and STR were achieved in 330 (35%), 388 (41%), and 231 cases (24%), respectively. Adjusting for factors associated with survival (for example, age, KPS score, Gliadel and/or temozolomide use, and subsequent resection), GTR versus NTR (p < 0.05) and NTR versus STR (p < 0.05) were independently associated with improved survival after both primary and revision resection of glioblastoma multiforme (GBM). For primary GBM resection, the median survival after GTR, NTR, and STR was 13, 11, and 8 months, respectively. After revision resection, the median survival after GTR, NTR, and STR was 11, 9, and 5 months, respectively. Adjusting for factors associated with survival for WHO Grade III astrocytoma (age, KPS score, and revision resection), GTR versus STR (p < 0.05) was associated with improved survival. Gross-total resection versus NTR was not associated with an independent survival benefit in patients with WHO Grade III astrocytomas. The median survival after primary resection of WHO Grade III (mixed oligoastrocytomas excluded) for GTR, NTR, and STR was 58, 46, and 34 months, respectively. In the authors' experience with both primary and secondary resection of malignant brain astrocytomas, increasing extent of resection was associated with improved survival independent of age, degree of disability, WHO grade, or subsequent treatment modalities used. The maximum extent of resection should be safely attempted while minimizing the risk of surgically induced neurological injury.

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Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas.

K Myrmel, Roar Kloster, Ole Solheim … (2012)

There are no controlled studies on surgical treatment of diffuse low-grade gliomas (LGGs), and management is controversial. To examine survival in population-based parallel cohorts of LGGs from 2 Norwegian university hospitals with different surgical treatment strategies. Both neurosurgical departments are exclusive providers in adjacent geographical regions with regional referral practices. In hospital A diagnostic biopsies followed by a "wait and scan" approach has been favored (biopsy and watchful waiting), while early resections have been advocated in hospital B (early resection). Thus, the treatment strategy in individual patients has been highly dependent on the patient's residential address. Histopathology specimens from all adult patients diagnosed with LGG from 1998 through 2009 underwent a blinded histopathological review to ensure uniform classification and inclusion. Follow-up ended April 11, 2011. There were 153 patients (66 from the center favoring biopsy and watchful waiting and 87 from the center favoring early resection) with diffuse LGGs included. The prespecified primary end point was overall survival based on regional comparisons without adjusting for administered treatment. Results Initial biopsy alone was carried out in 47 (71%) patients served by the center favoring biopsy and watchful waiting and in 12 (14%) patients served by the center favoring early resection (P < .001). Median follow-up was 7.0 years (interquartile range, 4.5-10.9) at the center favoring biopsy and watchful waiting and 7.1 years (interquartile range, 4.2-9.9) at the center favoring early resection (P=.95). The 2 groups were comparable with respect to baseline parameters. Overall survival was significantly better with early surgical resection (P=.01). Median survival was 5.9 years (95% CI, 4.5-7.3) with the approach favoring biopsy only while median survival was not reached with the approach favoring early resection. Estimated 5-year survival was 60% (95% CI, 48%-72%) and 74% (95% CI, 64%-84%) for biopsy and watchful waiting and early resection, respectively. In an adjusted multivariable analysis the relative hazard ratio was 1.8 (95% CI, 1.1-2.9, P=.03) when treated at the center favoring biopsy and watchful waiting. For patients in Norway with LGG, treatment at a center that favored early surgical resection was associated with better overall survival than treatment at a center that favored biopsy and watchful waiting. This survival benefit remained after adjusting for validated prognostic factors.

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Author and article information

Contributors

Catherine R. Garcia: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing

Stacey A. Slone: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing

Thomas Pittman: Role: ConceptualizationRole: MethodologyRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing

William H. St. Clair: Role: ConceptualizationRole: MethodologyRole: ResourcesRole: ValidationRole: Writing – review & editing

Donita D. Lightner: Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing

John L. Villano:

ORCID: http://orcid.org/0000-0001-5583-0093

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing

Johan Pallud: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 20 September 2018

Publication date Collection: 2018

Volume: 13

Issue: 9

Electronic Location Identifier: e0203639

Affiliations

[1 ] Markey Cancer Center, University of Kentucky, Lexington, Kentucky, United States of America

[2 ] Division on Cancer Biostatistics, University of Kentucky, Lexington, Kentucky, United States of America

[3 ] Department of Neurosurgery, University of Kentucky, Lexington, Kentucky, United States of America

[4 ] Department of Radiation Oncology, University of Kentucky, Lexington, Kentucky, United States of America

[5 ] Department of Neurology, University of Kentucky, Lexington, Kentucky, United States of America

[6 ] Department of Medicine, University of Kentucky, Lexington, Kentucky, United States of America

Centre Hospitalier Sainte Anne, FRANCE

Author notes

Competing Interests: The authors have no conflicts of interest.

* E-mail: jlvillano@ 123456uky.edu

Author information

John L. Villano http://orcid.org/0000-0001-5583-0093

Article

Publisher ID: PONE-D-18-12520

DOI: 10.1371/journal.pone.0203639

PMC ID: 6147430

PubMed ID: 30235224

SO-VID: 91e5e379-ae96-467f-ada3-9c5841bf5e42

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 25 April 2018

Date accepted : 26 August 2018

Page count

Figures: 3, Tables: 3, Pages: 16

Funding

Funded by: Biostatistics and Bioinformatics Shared Resource of the University of Kentucky Markey Cancer Center

Award ID: P30CA177558

Award Recipient : Stacey A. Slone

Ms. Slone was supported by the Biostatistics and Bioinformatics Shared Resource of the University of Kentucky Markey Cancer Center (P30CA177558).

Custom metadata

Data Availability The data is provided by the National Cancer Database and is available upon request by the National Cancer Database for investigators associated with Commission on Cancer accredited institutions. The National Cancer Database retains the decision of accessing the data based on an application process. Association to a Commission on Cancer accredited cancer program is required for applying. The application process opens throughout the year and requires a protocol submission. We applied for and were granted access to the data in the fall of 2017. Details on obtaining participant user files for data analysis is available in the following URL: https://na01.safelinks.protection.outlook.com/?url=https%3A%2F%2Fwww.facs.org%2Fquality-programs%2Fcancer%2Fncdb%2Fpuf&data=02%7C01%7Cjlvillano%40uky.edu%7C3e1f308e33a24f5e821608d60f427ddf%7C2b30530b69b64457b818481cb53d42ae%7C0%7C0%7C636713175589924852&sdata=siZFFXbVtzNa5qO4xWijysSJw3y%2FlA8uORwVyCub0C8%3D&reserved=0. Finally, collaborative interactions is an option for researchers outside of the Commission on Cancer accredited institutions, but data management and analysis (no data transfer) must be performed by the PI of the protocol approved from a Commission on Cancer accredited institution.

Comprehensive evaluation of treatment and outcomes of low-grade diffuse gliomas

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Abstract

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Results

Conclusions

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Most cited references 28

Radiation plus Procarbazine, CCNU, and Vincristine in Low-Grade Glioma.

Independent association of extent of resection with survival in patients with malignant brain astrocytoma.

Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas.

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