WHO 2016 update lymphoid neoplasms. Dr Sue Morgan Alfred Hospital, Melbourne
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1 WHO 2016 update lymphoid neoplasms Dr Sue Morgan Alfred Hospital, Melbourne
2 WHO 4 th edition 2008 Established guideline worldwide for diagnosis of haematological malignancy for the last 9 years Significant developments, particularly in molecular genetics which have impact on disease categorization, prognosis and therapy Revision required
3 Clinical Advisory Committee meeting clinicians (haematologists, oncologists) 18 haematopathologists & geneticists US, Europe & Asian centres Further development by editorial team of 11 Summary of proposed changes to be included in the revision published in Blood May 2016 Formal publication as a blue book expected in autumn 2017 (publications@iarc.fr)
4 Goals of a gold standard classification system Does not include patient factors, nor treatment response Rappaport 1956 Keil 1974 WHO 1976 National Cancer Institute s Working Formulation (IWF) 1982 Revised European-American Classification of Lymphoid Neoplasms (REAL) 1994
5 A noble aim The 2016 WHO classification and associated monograph aim to provide updated diagnostic categories and criteria, together with biological and clinical correlates, and facilitate state-of-the-art patient care, future therapeutic advances, and basic research in this field. Histopathological classification Clinical behaviour of the tumour Characteristic genetic aberrations
6 Definite entities No new discrete conditions Confirmation of some previous provisional entities as definite Changes to definitions or descriptions Provisional entities Diagnoses for which the evidence suggesting a discrete condition is suggestive but not definitive at this time Small numbers of new conditions
7 Mature B-cell lymphoid neoplasms Concepts Reclassification of some lymphoid proliferations as benign Inclusion of new genetic mutations Major changes in diagnosis of aggressive B-cell lymphomas which impact on therapy
8 Monoclonal B-cell lymphocytosis (MBL) Monoclonal B-cell population in peripheral blood of up to 5 x 10 9 /L Phenotype: CLL, atypical CLL or non-cll (CD5-) No other features of lymphoma Detected in up to 12% of healthy individuals using highly sensitive flow cytometry Nieto et. al. Blood 2009; 114: 33-7 Risk of progression to CLL, analogous to MGUS/myeloma
9 MBL new information WHO Almost all CLL cases preceded by MBL 2. Presence of cytopenias or disease-related symptoms cannot upgrade an MBL case to CLL Landgren et al. N Engl J Med 2009; 360:
10 MBL new information WHO Size of MBL clone matters low count MBL (<0.5 x 10 9 /L) Very low risk of transformation to CLL high count MBL (>0.5 x 10 9 /L) Increased risk of infections & secondary malignancy 1-2% transformation risk per year At least yearly review required Immunogenetic testing confirms similarity of HC-MBL to CLL Frequency of unmutated IgH gene rearrangements in MBL & CLL Frequency of BcR stereotypy in MBL & CLL Vardi et al. Blood 2013: 121:
11 MBL new information WHO Tissue-based MBL Small lymphocytic lymphoma subgroup with low risk of progression All nodes < 1.5cm on CT scan No proliferation centres seen in nodes Gibson et al. Haematologica 2011;96:
12 CLL/SLL a histologic subset confers poor prognosis Proliferation centres within nodal tissue can be identified by: MYC expression cyclin D1 expression in 1/3 Adverse prognosis can be defined histologically Large and confluent proliferation centres (high cytogenetic risk CLL correlated) Increased mitotic rate MYC Gibson et al. Br J Haematol; 2016: 175:
13 Follicular Lymphoma ISFN Follicular lymphoma in-situ In-situ follicular neoplasm BCL2 overexpressing centrocytes/centroblasts in architecturally normal nodes with normal follicles Settings Normal After therapy Synchronous disease Precursor No predictors for progression Number of follicles Proportion of follicles affected Extent of involvement with strong BCL2 positivity WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues, 4 th ed., 2008
14 Follicular lymphoma insights into Normal pathogenesis In-situ follicular neoplasm (ISFN) t(14;18) in blood Follicular lymphoma (FL) t(14;18) in nodal tissue FL immunophenotype by flow in nodal tissue Abnormal DNA methylation Chromosomal copynumber abnormalities X X Roulland et al. J Clin Oncol. 2014:32: Number of abnormalities
15 Follicular lymphoma new entities Pediatric-type FL (definite entity) Almost exclusively males, nodal involvement Blastoid cytological features with high proliferation rate (like FL grade 3) No BCL2 rearrangements, but BCL2 expression Characterised by MEK/ERK pathway mutations Excellent prognosis
16 Follicular lymphoma new entities Large B-cell lymphoma with IRF4 rearrangement (provisional) Subgroup of germinal centre B- cell lymphomas composing FL grade 3 or (centroblastic) DLBCL Low stage, Waldeyer s ring or neck Children, young adults BCL6, IRF4/MUM1 IH positive No BCL2 rearrangements More aggressive than pediatrictype FL but treatment responsive Liu et al. Am J Surg Pathol. 2013; 37:
17 Mantle cell lymphoma WHO describes three subtypes Two distinct pathways of NHL development Classical Indolent, leukaemic, nonnodal In-situ mantle cell neoplasia (ISMCN) Analogous to ISFN Cyclin D1+ cells in mantle zones of follicles Low rate of progression even if disseminated
18 Characteristic molecular abnormalities in mature B-cell neoplasms Since 2008 multiple mutations described Insights into pathogenesis Disease-defining Prognostic Made possible by: Wide availability of cost-effective nextgeneration sequencing technology Screening of large tumour databases Gene expression profiling Measurement of differential gene expression in cell populations: abnormal upregulation or downregulation Classification of cells within like pathways Identification of possible critical pathogenic molecular pathways Klein et al. J Exp Med, 2001; 194:
19 Molecular advances hairy cell leukaemia Disease-defining BRAF V600E mutation 1. Expressed in 100% of HCL cells 2. Expressed in all cells of malignant clone 3. Not expressed in any other cells with similar morphology Hairy-cell variant Splenic red pulp lymphoma Splenic marginal zone lymphoma Tiacci et al. N Engl J Med 2011; 364:
20 Molecular advances hairy cell leukaemia variants IGHV4-34 positive HCLc & HCLv Inferior response to cladribine, higher WCC at diagnosis, worse overall survival 48% have MAP2K1 mutations encodes MEK, downstream of BRAF 40% 10% IGHV4-34 no IGHV4-34 BRAF V600E IGHV4-34 Hairy cell variant Classic hairy cell leukaemia Waterfall et al. Nat Genetics, 2014: 46:8-10 Xi et al. Blood. 2012;119:3330 2
21 Molecular advances lymphoplasmacytic lymphoma (LPL) MYD88 L235P mutation found in ~90% of LPL and Waldenstrom s macroglobulinaemia (LPL with IgM paraprotein) Treon et al. N Engl J Med 2012; 367: Reanalysis of difficult cases in subsequent publications Redefinition of LPL: relatively monomorphic small B-cell lymphoma with plasmacytic differentiation LPL with wild-type MYD88 Rare Poor prognosis Poor response to ibrutinib
22 Molecular advances lymphoplasmacytic lymphoma (LPL) When to test for MYD88 L265P? Not in all cases, only when plasmacytic differentiation present and diagnosis in doubt Note that MYD88 L265P never present in IgG/A MGUS or plasma cell myeloma Suggests IgM MGUS related to LPL and other B-cell LPDs Frequency of MYD88 L265P mutations in B cell neoplasms CXCR4 mutations also NOT in myeloma 30% LPL, 20% IgM MGUS Swerdlow et al. Virchows Arch Mar; 468(3):
23 Molecular advances CLL/SLL No definite disease-defining mutations Large number of mutations with low frequency Some have adverse prognostic impact, often associated with adverse cytogenetic risk Examples: TP53, NOTCH1, SF3B1, BIRC3, ATM
24 CLL/SLL - Mutations occur in multiple pathways Lawrence et al. N Engl J Med 2011: 365:
25 CLL/SLL molecular prognostication Jeromin et al. Leukaemia. 2014; 28: Updated risk stratifications combining molecular markers with FISH proposed (e.g. Rossi et. al. Blood, 2013.) WHO 2016 does not currently recommend utilizing these at current levels of evidence
26 Molecular advances mantle cell lymphoma 1. NOTCH1/2 and TP53 mutations predict for poor risk disease 2. Cyclin D1 -, SOX11 + mantle cell lymphoma Difficult to diagnose with no classic t(11;14) rearrangement Similar genomic profile to CCND1 MCL, confirming SOX11 immunohistochemistry Chromosomal rearrangements in ~50% involving CCND2 on chromosome 12p (IGK, IGL or IGH partners) Salaverria et al. Blood :
27 Aggressive B-cell lymphomas Major changes to classification in order to incorporate the role of MYC, BCL2 and BCL6 double-hit lymphomas Diffuse large B-cell lymphoma double expressor category better defined Cell-of-origin classification
28 MYC and BCL2 in aggressive MYC protein detected: 30-40% DLBCL % Burkitt lymphoma 5% normal germinal centre B-cells lymphomas BCL2 protein detected in: >50% DLBCL 0% Burkitt lymphoma 0% normal germinal centre B-cells MYC function induced by immunoglobin gene Multiple cellular functions Promotes cell proliferation Induces genomic instability Amplifies transcription of other genes BCL2 function Inhibits apoptosis Additional abnormalities required to induce lymphoma BCL6: a transcription factor normally suppresses MYC and BCL2 in germinal centres. BCL6 deregulation induces tumours in mice
29 MYC, BCL2, BCL6 expression Detected by immunohistochemistry MYC, BCL2, BCL6 translocations Detected by: G-banded karyotyping FISH
30 WHO 2008 B-cell lymphoma, unclassifiable (with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma) Criteria vague NOT based on distinct genetic profile Poorly reproducible Significance for therapy unclear
31 New definite entity: High-grade B-cell lymphoma, with MYC and BCL2 and/or BCL6 translocations Dismal prognosis (median survival years) Sequential acquisition of t(14;18) translocation, followed by a translocation involving MYC on 8q24 Reclassification of 5% of DLBCL diagnosed by WHO 2008 triple-hit, 20% MYC and BCL6, 20% MYC and BCL2, 60% ~90% GCB phenotype
32 WHO 2016 new assessment of aggressive lymphomas MYC rearrangement alone MYC and BCL2 and/or BCL6 rearrangement
33 Case 1: how to use the new classification 57 yo man Rapidly enlarging mass left neck Histology: B-cell lymphoma, with features intermediate between diffuse large B-cell lymphoma and Burkitt's lymphoma BCL2 Immunohistochemistry alone is insufficient to diagnose a patient with DLBCL/BL. FISH must be performed. BCL6 MYC FISH identified rearranged MYC signals in 58/162 (35%) cells scored. This is molecular cytogenetic evidence of a translocation involving the MYC gene at 8q24.
34 Diffuse large B cell lymphoma Common disease, but with variable outcome Morphologic subtypes are not prognostic 2016 US lymphoid malignancy statistics (Hodgkin lymphoma not included)
35 Patient samples DLBCL cell of origin classification genes Two groups of DLBCL with distinct gene expression profiles reflecting their normal B-cell counterpart Alizadeh et al. Nature, 2000; 403:
36 Roschewski et al. Nat Rev Clin Oncol. 2014;11: 12-23
37 DLBCL cell of origin highly predictive of outcome WHO 2008 subclassification optional Alizadeh et al. Nature, 2000; 403:
38 Activated B- cell GCB DLBCL immunohistochemical determination of cell-of-origin reasonable correlation with gene-expression profiling Limitations of Hans algorithm: Subgroup of unclassifiable tumours (10-15%) Reproducibility Subjective Hans et al. Blood, 2004; 103:
39 GCB DLBCL DLBCL revised WHO mandates allocation to cell-of-origin subtypes Therapeutic trials of targeted agents selectively affecting differential molecular pathways ABC DLBCL Roschewski et al. Nat Rev Clin Oncol. 2014;11: 12-23
40 DLBCL double expressor lymphomas Increased expression of MYC or BCL proteins by immunohistochemistry can occur in the absence of translocations Definitions of positivity important 40% MYC-expressing cells >50% BCL2-expressing cells Eight independent studies demonstrate poor prognosis Diagnosis and relapse Poor response to induction regimens, salvage chemotherapy, autologous transplantation Prognostic factor, not a separate category
41 Morphology and immunophenotype Germinal-centre BC DLBCL (%) Activated BC High grade B-cell NHL (%) MYC protein by IH Incidence of translocation BCL2 protein by IH Incidence of translocation Double-expressor DLBCL NA Sesques et al. Blood, 2017; 129:
42 The level of MYC protein expression depends on the underlying mechanism High-grade B-cell lymphoma GCB phenotype Burkitt lymphoma ABC phenotype Sesques & Johnson, Blood. 2017; 129: 280-8
43 Sesques & Johnson, Blood. 2017; 129: 280-8
44 Case 2 : DLBCL reporting in WHO 2016 era 79 yo woman Extensive nodal, soft tissue and bony masses. Stage IVBE Activated B- cell phenotype CD10 BCL6 MUM1
45 Case 2 : DLBCL reporting in WHO 2016 era Double-expressor status confirmed on immunohistochemistry MYC BCL2 Is FISH required to determine whether patient is a High-grade B-cell lymphoma, with MYC and BCL2 and/or BCL6 translocations?? Yes, but is it worthwhile/cost effective/necessary?
46 Test numbers Case 2 : FISH testing for HGBL-DH? Options: 1. Test all 2. Test those clinically appropriate Escalation of therapy is possible Specific prognostication is useful (e.g. treatment withdrawal if prognosis dismal) 3. Test only GCB phenotype ~50% reduction in testing But only 6% of GCB have DH 4. Test only dual expressors with GCB phenotype ~90% reduction in testing 1/3 of tested patients would have HGBL-DH
47 New provisional entity: Burkitt-like lymphoma with 11q aberrations Disease which looks like Burkitt lymphoma No MYC translocations.. Similar Morphology Gene expression profile Immunophenotype H&E Ki67 CD20 BCL6 Different 11q gains/losses More complex karyotype MYC expression by IH lower than BL Nodal presentation Post transplant LPD Ferreiro et. al. Haematologica 2015;100(7):e275-e279.
48 Mature T- and NK-cell neoplasms Nodal T-cell lymphoma with T follicular helper (TFH) phenotype ALK negative large cell lymphoma Breast implant associated anaplastic large cell lymphoma (alterations to classification of some rare cutaneous & intestinal T-cell disorders)
49 New category: nodal T-cell lymphoma with T follicular helper (TFH) phenotype Gene fusions ITK-SYK CTLA4-CD28. Similar gene expression profile Different presentation TFH phenotype At least 2 of: CD279/PD1, CD10, BCL6, CXCL13, ICOS, SAP, and CCR5 Mutations TET2 IDH2 DNMT3A RHOA CD28 Follicular T-cell lymphoma Nodal PTCL with TFH phenotype Angioimmunoblastic T-cell lymphoma
50 Anaplastic large cell lymphoma confirmed new entities All CD30+ ALK POSITIVE ALK NEGATIVE DEFINITE PROVISIONAL SYSTEMIC Young OS ~70% 5 yr t(2;5) NPM-ALK SYSTEMIC Older OS 15-45% 5 yr JAK-STAT pathway CUTANEOUS Excellent prognosis BREAST- IMPLANT
51 ALCL - Genetic subtypes provide new prognostic information ALK status Genetic aberration 5 year overall survival ALK positive t(2;5) 85% ALK negative DUSP22 rearranged (30%) 90% ALK negative TP63 rearranged (8%) 17% ALK negative WT DUSP22/TP63 (62%) 42% Parilla Castellar et al. Blood : Distinct morphological features in DUSP22 rearranged ALCL: monomorphism sheet-like growth doughnut cells King et al. Am J Surg Pathol Jan; 40(1): 36 43
52 New provisional entity: Breast-implant associated anaplastic large cell lymphoma Accumulation of seroma fluid between the implant and surrounding fibrous capsule Excellent prognosis if confined, worse if capsule infiltration occurs CD30
53 Enteropathy-associated T-cell lymphomas two new distinct aggressive entities Enteropathy-associated TCL Formerly EATL type I Associated with coeliac disease, Caucasian Polymorphic CD56- Monomorphic epitheliotropic intestinal TCL Formally EATL type II No coeliac association, Asian, Hispanic Monomorphic CD56+ Many of γδ T-cell origin (STAT5b, JAK3 mutations) 93% loss of function mutations in tumour suppressor gene SETD2 Roberti et al. Nat Commun. 2016; 7: 12602
54 Other T/NK cell lymphomas STAT3 and STAT5b mutations seen in ~40% of T-cell large granular lymphocyte lymphoma Systemic EBV+ T-cell lymphoma of childhood Confirmed new entity Distinct from chronic active EBV infection Asians, South Americans Fulminant clinical course -haemophagocytic syndrome
55 Hodgkin lymphomas Subtle changes to nodular lymphocyte predominant HL
56 Histiocytic and dendritic cell neoplasms Erdheim Chester disease as new distinct entity (BRAF V600E mutation)
57 The existence of deeply held divergent views concerning the histological identification of tumor cell types is.particularly serious., since the international adoption of a soundly based histopathological classification is a prerequisite to substantial progress at the clinical level. Kaplan, Henry. Br J Cancer. 1975;31(Suppl 2):7-8
58 Morphologic assessment is the foundation of the WHO 2016 classification of lymphoid neoplasms The current revision retains the same structure, with few significant changes Advances in molecular genetics are certain to continue to play a pivotal role in understanding lymphoid malignancies in 2017 and beyond Diagnostic laboratories will need to provide cost-effective, evidence-based genetic testing to guide lymphoma therapy
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