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Draft:CIMPACT-NOW

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Background

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The Consortium to Inform Molecular and Practical Approaches to CNS Tumor Taxonomy (cIMPACT-NOW) is an organization of physicians and scientists with expertise in brain tumors, including neuropathologists was well as neuro-oncologists (pediatric and adult), that was formed just after publication of the 2016 Updated 4th Edition of the World Health Organization (WHO) Classification of Tumours of the Central Nervous System “blue book”.[1][2] The organization was created because discussions for the 2016 Updated 4th Edition had brought up the question of how tumor classifications could keep up with the rapid pace of molecular discoveries in neuro-oncology ("the field is moving so fast that we need to have more regular updates"[3]). Discussions by a number of tumor neuropathologists, led by David Louis[4] and Andreas von Deimling[5], resulted in the idea of a consortium that worked in the time periods between WHO classifications.[6][7]

cIMPACT-NOW, with sponsorship from the International Society of Neuropathology,[8] issued a series of seven updates between 2018 and 2020, and the 2021 5th Edition World Health Organization (WHO) Classification of Tumours of the Central Nervous System[9] largely adopted the recommendations of the first seven cIMPACT-NOW updates.[10][11] For example, Mortensen et al. stated that "In 2018 the Consortium to Inform Molecular and Practical Approaches to CNS Tumor Taxonomy (cIMPACT-NOW) released their third update, wherein they recommended IDH-wildtype diffuse astrocytic tumors with either TERT promoter mutation, EGFR gene amplification or a combination of gain of entire chromosome 7 and loss of entire chromosome 10 (+7/−10) should be considered WHO grade 4 due to much more aggressive behavior, despite lacking the typical histological features... In cIMPACT-NOW update 6, with sufficient clinical data confirming that survival for DAG-G is similar to glioblastomas IDH-wildtype, the following diagnostic criteria were suggested for glioblastoma: microvascular proliferation, or necrosis, or one (or more); TERT promoter mutation, EGFR amplification or + 7/− 10. These suggestions were incorporated into the fifth edition of WHO-CNS (WHO-CNS5)."[12] cIMPACT updates have also influenced the conduct of clinical trials (e.g., EORTC-2013-BTG[13]) and have been supported by patient advocacy groups.[14]


In 2020, Onizuka et al.[15] reviewed the first five cIMPACT-NOW updates and Gonzalez Castro[16] summarized that the first seven cIMPACT-NOW updates. Gonzalez Castro wrote that the updates

translate to recent advances in our understanding of the molecular underpinnings of CNS tumors. Salient recommendations include those that provide guidance for how even in the absence of histopathological characteristics of the highest malignancy grade, molecular markers can be used to reach a diagnosis of glioblastoma, IDH–wild-type or astrocytoma, IDH-mutant, grade IV. The cIMPACT-NOW guidelines have important implications for clinical practice and for the design and interpretation of clinical trials. Additionally, cIMPACT-NOW has proposed several changes regarding diagnostic principles and nomenclature, as well as made suggestions on which tumor types have now emerged as mature enough to deserve a separate status in a next WHO [5th edition] classification.[16]

A concern was added that "the fact that these updates have been published in neuropathology journals may have limited the propagation of this information to the wider clinical neuro-oncology community."[16]

Following the success of the WHO CNS 5th edition capitalizing on cIMPACT-NOW updates, cIMPACT-NOW began a second phase after publication of the WHO CNS 5th edition, transferring overall leadership from David Louis[4] to Pieter Wesseling[17] and reconstituting its committees in order to formulate new topics and new working groups. To date, this second phase has resulted in four updates (cIMPACT-NOW updates 8, 9, 10, and 11) and two working committees still in progress. The 11 published updates are summarized below.  All cIMPACT-NOW updates have been published as public access.

cIMPACT-NOW Update 1

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cIMPACT-NOW Update 1, published in 2018, clarified the use of the established term NOS (Not Otherwise Specified),[18] stating that this designation should be used when diagnostic information (histological or molecular) necessary to assign a more specific WHO diagnosis is not available. The update also proposed use of the (new to neuro-oncology) term NEC (Not Elsewhere Classified). NEC would be used when necessary diagnostic testing had been successfully performed, but the results did not readily allow for a WHO 2016 diagnosis; reasons for this could include discordance between clinical, histological, immunohistochemical, and/or genetic features, or because the tumor conformed to a new/emerging entity that was not yet part of the WHO classification. This approach became a standard approach for the 2021 WHO classification and for diagnostic neuropathology practices around the world.[19][20][21]

cIMPACT-NOW Update 2

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cIMPACT-NOW Update 2, published in 2018,[22] put forth clarifications regarding two diagnoses: Diffuse Midline Glioma, H3 K27M-mutant and Diffuse Astrocytoma/Anaplastic Astrocytoma, IDH-mutant. The group advised that the diagnosis of Diffuse Midline Glioma, H3 K27M­­–mutant should be made only in the situation that tumors are diffuse (i.e., infiltrating into brain tissue), midline (e.g., thalamus, brain stem, spinal cord), glial in nature, and H3 K27M-mutant. In other words, even in the presence of H3 K27M mutation, the designation should not be used in tumors that do not have all of these features. The cIMPACT-NOw Update 2 clarifications have been cited for guidelines by the Korean Society for Neuro-Oncology for treating such patients and have influenced trial interpretations for this tumor type.[23] The update also streamlined the use of immunohistochemical and molecular testing for the diagnosis of Diffuse Astrocytoma, IDH-mutant or Anaplastic Astrocytoma, IDH-mutant, stating that the diagnosis could be made if the tumor was a diffuse astrocytic-appearing WHO grade II or III glioma that has IDH mutation as well as loss of ATRX nuclear expression and/or strong, diffuse p53 immunopositivity; in this setting, a diagnosis can be rendered in the absence of the more time-consuming and less widely available chromosome 1p/19q testing.

cIMPACT-NOW Update 3

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cIMPACT-NOW Update 3, published in 2018,[24] opined that to diagnose the highest-grade glioma, glioblastoma, one could use some molecular criteria. (To date, diagnoses of glioblastoma were histologically based.) Based on detailed literature review, the update proposed that specific molecular findings in an IDH-wildtype WHO grade II or grade III diffuse astrocytic glioma would predict that the tumor would follow a course more similar to a WHO grade IV glioblastoma-- i.e., even when the lesion lacked the traditional histological features of glioblastoma. These molecular findings were: EGFR amplification; and/or whole chromosome 7 gain and whole chromosome 10 loss (+7/-10); and/or TERT promoter mutation. Therefore, a diffuse astrocytic gliomas of histologic grade II and III with any of these findings would correspond to WHO grade IV behavior.

These criteria have been investigated in series such as those of Molica et al.,[25] who concluded that "Our data set on 313 cases confirmed the favorable prognostic value of IDH1/2 mutations, and validated the cIMPACT-NOW 3 signature as high-risk marker, thus confirming prognostically relevant subgroups." Tesileanu et al. also showed that these criteria supported a diagnosis of glioblastoma in the absence of histological diagnostics feature.[26] Studies have also evaluated the addition of radiological information to the pathology-based criteria of cIMPACT-NOW.[27] The recommendations of cIMPACT-NOW Update 3 and Update 5 (see below) were endorsed by European Association of Neuro-Oncology (EANO) guidelines[28] and subsequently incorporated into the 5th edition of the CNS WHO Classification.[9] Notably, however, other studies have now questioned whether TERT promoter mutation alone should be one of these criteria.[29][30]

cIMPACT-NOW Update 4

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cIMPACT-NOW Update 4, published in 2019,[31] drafted a classification approach for WHO grade II IDH-wildtype / H3-wildtype diffuse gliomas, primarily those occuring in childhood. Using an integrated diagnosis[32] that accounted for histologic and genetic features, the draft classification parceled these largely low-grade pediatric diffuse gliomas into those that were: MYB-altered; MYBL1-altered; FGFR1 TKD-duplicated; FGFR1-mutant; or BRAFV600E-mutant (but without CDKN2A/B deletion); or those with other MAPK pathway alterations. This approach was summarized by Funakoshi et al. in their 2021 review of pediatric glioma diagnosis, biology and treatment[33] and the concepts were adopted by the 5th edition of the CNS WHO Classification.[9]

cIMPACT-NOW Update 5

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cIMPACT-NOW Update 5, published in 2020,[34] reviewed data to propose an approach to grading of IDH-mutant diffuse astrocytomas and suggested clear separation of IDH-wildtype from IDH-mutant astrocytic tumors as well as the use of Arabic rather than Roman numerals for grading. A highly significant feature of this update was the recommendation that molecular information should be used for diagnoses: both the establishment of IDH mutation status and the determination of whether CDKN2A homozygous deletion is present. The recommendations of cIMPACT-NOW Update 3 and Update 5 were endorsed by European Association of Neuro-Oncology (EANO) guidelines[28] and subsequently incorporated into the 5th edition of the CNS WHO Classification.[10] In addition, given the importance of tumor grading for diffuse astrocytomas, the criteria are being revisited in 2025 as part of another cIMPACT-NOW working committee.

cIMPACT-NOW Update 6

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cIMPACT-NOW Update 6, published in 2020,[35] was different from the prior five updates in that it was the produce of an in-person meeting in Utrecht and included WHO representatives, the latter being included because it was anticipated that WHO CNS meetings would begin in early 2020. The meeting was fortunate because the Covid-19 pandemic prevented in-person WHO meetings in the spring of 2020. cIMPACT-NOW Update 6 reviewed possible new entities that might be considered for inclusion in the next WHO classification. The group recommended a substantial number of newly recognized types and subtypes for inclusion in future CNS tumor classifications and also endorsed a number of principles relating to classification categories, approaches to classification, nomenclature, and grading. One of the major recommendations related to a molecular definition of glioblastoma, i.e., if a tumor was IDH- and H3-wildtype and had either TERT promoter mutation, EGFR amplification or +7/−10 copy number changes-- a definition that was incorporated into the 2021 5th edition CNS WHO classification[9] and used by subsequent papers as criteria for further study.[36] New proposed entities that were subsequently incorporated into the 2021 5th edition CNS WHO classification were Diffuse hemispheric glioma, H3 G34-mutant and Astroblastoma, MN1-altered. The proposal of new tumor types also prompted further studies by other groups, such as Chen et al., of some of these entities, leading to further definitional refinements.[37]

cIMPACT-NOW Update 7

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cIMPACT-NOW Update 7, published in 2020,[38] reviewed data on ependymal tumors and made recommendations about the molecular classification of these lesions, including the distinction of PFA and PFB posterior fossa ependymomas and the incorporation of specific molecular markers (e.g., C11orf95 [at the time], YAP1 and MYCN. Importantly, the recommended classification and significance of molecular alterations were dependent on anatomic site, prompting incorporation of anatomic site into the classification proposal. This combined anatomical-molecular approach formed the basis of the 2021 5th edition CNS WHO classification[9][39] and the reclassification by cIMPACT-NOW Update 7 was cited by a large ependymoma consortium as reinforcing the importance of reclassification of ependymal tumors as new molecular data emerges.[40]

cIMPACT-NOW Update 8

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cIMPACT-NOW Update 8 was the first update following the 2021 5th edition CNS WHO classification and was published on line in 2024[41]. The group addressed the influence of recently identified molecular markers on the grading of meningiomas, proposing to assign CNS WHO grade 2 for cases with CNS WHO grade 1 morphology but chromosomal arm 1p deletion in combination with 22q deletion and/or NF2 oncogenic variants.[42][43] Guidance was also provided for more standardized morphological evaluation and interpretation, e.g., pertaining to brain invasion. Using recommendations of the cIMPACT-NOW Update 8, an independent study from Landry et al. confirmed the value of assessing copy number changes (in particular, 1p and 22q loss as well as 1q gain) in grading meningiomas, including that "additional investigation into the role of 1p loss without 22q loss is needed, given the rarity of this event, aligning our conclusions with the recent cIMPACT-NOW statement."[44]

cIMPACT-NOW Update 9

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cIMPACT-NOW Update 9 was published on line in 2024[45] and addressed the rapidly burgeoning area of DNA methylation profiling for CNS tumor diagnosis[46][47]. Use of DNA methylation signatures had been endorsed in the 2021 CNS WHO classification in specific situations,[9] but the use of the technology had broadened considerably since then. Recommendations emphasized the attributes and limitations of the modality and that the methylation classifier is one diagnostic tool to be used alongside previously established diagnostic tools in a fully integrated fashion. The group also stressed the need for backward compatibility of future platforms to enable accumulated data to be compatible with new versions of the array. The publication "paved the road towards how DNA methylation will be even more integrated into the next iteration of the WHO classification.”[3]

cIMPACT-NOW Update 10

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cIMPACT-NOW Update 10, published on line in 2025,[48] addressed the difficult problem of how to define a tumor type in light of the wide array of data types now available (e.g., clinical, histopathological, genetic, genomic and other -omics, DNA methylation).[3] The eventual recommendations proposed that different combinations of such features could fulfill criteria to define a type and potentially a subtype, and suggested the types of publications necessary to support definition of a new tumor type or subtype.

cIMPACT-NOW Update 11

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A working group has submitted a manuscript addressing clarifications to the 5th Edition CNS WHO classification[9], with the manuscript now in press.

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  45. ^ Aldape, K.; Capper, D.; von Deimling, A.; Giannini, C.; Gilbert, M. R.; Hawkins, C.; Hench, J.; Jacques, T. S.; Jones, D.; Louis, D. N.; Mueller, S.; Orr, B. A.; Nasrallah, M.; Pfister, S. M.; Sahm, F.; Snuderl, M.; Solomon, D.; Varlet, P.; Wesseling, P. (2025). "cIMPACT-NOW update 9: Recommendations on utilization of genome-wide DNA methylation profiling for central nervous system tumor diagnostics". Neuro-Oncology Advances. 7 (1): vdae228. doi:10.1093/noajnl/vdae228. PMC 11788596. PMID 39902391.
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