A molecularly integrated grade for meningioma.


Journal

Neuro-oncology
ISSN: 1523-5866
Titre abrégé: Neuro Oncol
Pays: England
ID NLM: 100887420

Informations de publication

Date de publication:
04 05 2022
Historique:
pubmed: 12 9 2021
medline: 10 5 2022
entrez: 11 9 2021
Statut: ppublish

Résumé

Meningiomas are the most common primary intracranial tumor in adults. Clinical care is currently guided by the World Health Organization (WHO) grade assigned to meningiomas, a 3-tiered grading system based on histopathology features, as well as extent of surgical resection. Clinical behavior, however, often fails to conform to the WHO grade. Additional prognostic information is needed to optimize patient management. We evaluated whether chromosomal copy-number data improved prediction of time-to-recurrence for patients with meningioma who were treated with surgery, relative to the WHO schema. The models were developed using Cox proportional hazards, random survival forest, and gradient boosting in a discovery cohort of 527 meningioma patients and validated in 2 independent cohorts of 172 meningioma patients characterized by orthogonal genomic platforms. We developed a 3-tiered grading scheme (Integrated Grades 1-3), which incorporated mitotic count and loss of chromosome 1p, 3p, 4, 6, 10, 14q, 18, 19, or CDKN2A. 32% of meningiomas reclassified to either a lower-risk or higher-risk Integrated Grade compared to their assigned WHO grade. The Integrated Grade more accurately identified meningioma patients at risk for recurrence, relative to the WHO grade, as determined by time-dependent area under the curve, average precision, and the Brier score. We propose a molecularly integrated grading scheme for meningiomas that significantly improves upon the current WHO grading system in prediction of progression-free survival. This framework can be broadly adopted by clinicians with relative ease using widely available genomic technologies and presents an advance in the care of meningioma patients.

Sections du résumé

BACKGROUND
Meningiomas are the most common primary intracranial tumor in adults. Clinical care is currently guided by the World Health Organization (WHO) grade assigned to meningiomas, a 3-tiered grading system based on histopathology features, as well as extent of surgical resection. Clinical behavior, however, often fails to conform to the WHO grade. Additional prognostic information is needed to optimize patient management.
METHODS
We evaluated whether chromosomal copy-number data improved prediction of time-to-recurrence for patients with meningioma who were treated with surgery, relative to the WHO schema. The models were developed using Cox proportional hazards, random survival forest, and gradient boosting in a discovery cohort of 527 meningioma patients and validated in 2 independent cohorts of 172 meningioma patients characterized by orthogonal genomic platforms.
RESULTS
We developed a 3-tiered grading scheme (Integrated Grades 1-3), which incorporated mitotic count and loss of chromosome 1p, 3p, 4, 6, 10, 14q, 18, 19, or CDKN2A. 32% of meningiomas reclassified to either a lower-risk or higher-risk Integrated Grade compared to their assigned WHO grade. The Integrated Grade more accurately identified meningioma patients at risk for recurrence, relative to the WHO grade, as determined by time-dependent area under the curve, average precision, and the Brier score.
CONCLUSION
We propose a molecularly integrated grading scheme for meningiomas that significantly improves upon the current WHO grading system in prediction of progression-free survival. This framework can be broadly adopted by clinicians with relative ease using widely available genomic technologies and presents an advance in the care of meningioma patients.

Identifiants

pubmed: 34508644
pii: 6368844
doi: 10.1093/neuonc/noab213
pmc: PMC9071299
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

796-808

Subventions

Organisme : NCI NIH HHS
ID : R01 CA262311
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007618
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007753
Pays : United States

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Neuro-Oncology.

Références

J Neurosurg. 2019 Feb 15;132(2):491-502
pubmed: 30771780
J Clin Oncol. 2011 Apr 10;29(11):1408-14
pubmed: 20823417
J Neurooncol. 2009 May;93(1):25-39
pubmed: 19430880
Science. 2013 Mar 1;339(6123):1077-80
pubmed: 23348505
Nat Commun. 2020 Jan 3;11(1):89
pubmed: 31900397
Cancer Cell. 2015 May 11;27(5):728-43
pubmed: 25965575
Neuro Oncol. 2019 Nov 1;21(Suppl 5):v1-v100
pubmed: 31675094
NPJ Genom Med. 2017;2:
pubmed: 28713588
Neuro Oncol. 2016 Apr;18(4):565-74
pubmed: 26493095
Sci Rep. 2018 Sep 10;8(1):13537
pubmed: 30202034
J Natl Cancer Inst. 2015 Dec 13;108(5):
pubmed: 26668184
J Neuropathol Exp Neurol. 2016 Jan;75(1):44-52
pubmed: 26705409
Arch Pathol Lab Med. 2017 Jun;141(6):751-758
pubmed: 28557599
J Neurosurg. 2018 Jul;129(1):35-47
pubmed: 28984517
Neuro Oncol. 2017 Apr 1;19(4):535-545
pubmed: 28170043
Am J Pathol. 2001 Aug;159(2):661-9
pubmed: 11485924
J Neurosurg. 2015 Jan;122(1):4-23
pubmed: 25343186
J Neurosurg. 2004 Aug;101(2):210-8
pubmed: 15309910
J Neuropathol Exp Neurol. 2020 Jul 1;79(7):754-762
pubmed: 32447376
Med Decis Making. 2006 Nov-Dec;26(6):565-74
pubmed: 17099194
Am J Surg Pathol. 1997 Dec;21(12):1455-65
pubmed: 9414189
Cancer Genet. 2015 Jun;208(6):345-50
pubmed: 25963524
Nat Genet. 2013 Mar;45(3):285-9
pubmed: 23334667
N Engl J Med. 2015 Jun 25;372(26):2499-508
pubmed: 26061753
Neuro Oncol. 2019 Jul 11;21(7):901-910
pubmed: 31158293
Acta Neuropathol. 2020 Jul;140(1):89-93
pubmed: 32405805
Radiother Oncol. 2018 Aug;128(2):260-265
pubmed: 29960684
Neuro Oncol. 2016 Feb;18(2):269-74
pubmed: 26323607
Cell Rep. 2018 Mar 27;22(13):3672-3683
pubmed: 29590631
Lancet Oncol. 2017 May;18(5):682-694
pubmed: 28314689
Proc Natl Acad Sci U S A. 2019 Oct 22;116(43):21715-21726
pubmed: 31591222
Cancer Discov. 2012 Jan;2(1):82-93
pubmed: 22585170
J Mol Diagn. 2004 Nov;6(4):316-25
pubmed: 15507670
Oncotarget. 2017 Nov 24;8(65):109228-109237
pubmed: 29312603
Neuro Oncol. 2017 Mar 1;19(3):453-454
pubmed: 28391316
Neuro Oncol. 2014 May;16(5):735-47
pubmed: 24536048
Neuro Oncol. 2017 Oct 19;19(11):1553-1564
pubmed: 28482030
N Engl J Med. 2007 Nov 1;357(18):1821-8
pubmed: 17978290
J Neurosurg. 2020 Oct 9;:1-8
pubmed: 33035995
Neuro Oncol. 2021 Aug 2;23(8):1231-1251
pubmed: 34185076
Stat Probab Lett. 2010 Jul 1;80(13-14):1056-1064
pubmed: 20582150
Neuro Oncol. 2019 Jan 1;21(1):26-36
pubmed: 30137421
Acta Neuropathol. 2016 Jun;131(6):803-20
pubmed: 27157931
J Stat Softw. 2011 Mar;39(5):1-13
pubmed: 27065756
Nat Genet. 2016 Oct;48(10):1253-9
pubmed: 27548314
Endocrinology. 2017 Jul 1;158(7):2284-2291
pubmed: 28486603

Auteurs

Joseph Driver (J)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Samantha E Hoffman (SE)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
Harvard-MIT Program in Health Science Technology, MD-PhD Program, Harvard Medical School, Boston, Massachusetts, USA.

Sherwin Tavakol (S)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Eleanor Woodward (E)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Eduardo A Maury (EA)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
Harvard-MIT Program in Health Science Technology, MD-PhD Program, Harvard Medical School, Boston, Massachusetts, USA.
Bioinformatics and Integrative Genomics Program, Harvard Medical School, Boston, Massachusetts, USA.

Varun Bhave (V)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Noah F Greenwald (NF)

Cancer Biology Program, Stanford University School of Medicine, Stanford, California, USA.

Farshad Nassiri (F)

Department of Neurosurgery, University of Toronto, Toronto, Ontario, Canada.

Kenneth Aldape (K)

National Cancer Institute, Bethesda, Maryland, USA.

Gelareh Zadeh (G)

Department of Neurosurgery, University of Toronto, Toronto, Ontario, Canada.

Abrar Choudhury (A)

Departments of Radiation Oncology and Neurological Surgery, University of California San Francisco, San Francisco, California, USA.

Harish N Vasudevan (HN)

Departments of Radiation Oncology and Neurological Surgery, University of California San Francisco, San Francisco, California, USA.

Stephen T Magill (ST)

Departments of Radiation Oncology and Neurological Surgery, University of California San Francisco, San Francisco, California, USA.

David R Raleigh (DR)

Departments of Radiation Oncology and Neurological Surgery, University of California San Francisco, San Francisco, California, USA.

Malak Abedalthagafi (M)

King Fahad Medical City and King Abdulaziz City for Science and Technology, Riyadh, Saudi Arabia.

Ayal A Aizer (AA)

Department of Radiation Oncology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Brian M Alexander (BM)

Department of Radiation Oncology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Keith L Ligon (KL)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

David A Reardon (DA)

Center for Neuro-Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.

Patrick Y Wen (PY)

Center for Neuro-Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.

Ossama Al-Mefty (O)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Azra H Ligon (AH)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Adrian M Dubuc (AM)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Rameen Beroukhim (R)

Center for Neuro-Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.
Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.
Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.

Elizabeth B Claus (EB)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
Yale School of Public Health, New Haven, Connecticut, USA.

Ian F Dunn (IF)

Department of Neurosurgery, Oklahoma University Medical Center, Oklahoma City, Oklahoma, USA.

Sandro Santagata (S)

Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.

Wenya Linda Bi (WL)

Department of Neurosurgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH