New Concepts and Clinical Implications of the 2008 WHO Classification of Lymphomas Elaine S. Jaffe, M.D.
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1 New Concepts and Clinical Implications of the 2008 WHO Classification of Lymphomas Elaine S. Jaffe, M.D.
2 The first step in wisdom is to know the things themselves; this notion consists in having a true idea of the objects; objects are distinguished and known by classifying them methodically and giving them appropriate names. Therefore, classification and name-giving will be the foundation of our science. Carolus Linnaeus ( ) The Father of Taxonomy
3 Why do we classify tumors? We classify to delineate disease entities Correct disease definition is essential for Ongoing studies of pathogenesis Comparison of clinical trials Epidemiological studies Diagnosis of the correct disease is required as a guide to therapy in the individual patient
4 Clinical Relevance of Precise Disease Definitions Treatment of 3 small B-cell malignancies Hairy cell leukemia MALT lymphoma 2-CDA Antibiotics Mantle cell lymphoma Aggressive Rx Response to therapy is disease-specific Anaplastic large cell lymphoma Peripheral T-cell lymphoma, NOS Good Prognosis Poor Prognosis
5 Rudolf Virchow
6 Time Line of Changes in Lymphoma Classification Impact of Clinical and Technical Advances Classifications pre Discoveries Entities HD FL Burkitt MM Sternberg Sarcoma Lymphosarcoma Reticulum Cell Sarcoma Waldenström s Macroglobulinemia Immunology Genetics Staging & Therapy Lymphocyte Transformation B - T cells Chromosomal Abnormalities Southern blot ATLL MALT
7 Multiparameter approach to disease definition based on Morphology Immunophenotype Clinical Features Genomic Alterations
8 WHO Monograph 4 th Edition IARC Press September 2008 Editors: Steven H. Swerdlow, Elias Campo Nancy Lee Harris, Elaine S. Jaffe Stefano A Pileri, Harald Stein Jurgen Thiele, James W. Vardiman 138 pathologists/ hematologists as authors 69 clinicians on a Clinical Advisory Committee Contributors from 40 countries
9 New Aspects of WHO 2008 Greater recognition of early lesions Earliest steps in neoplastic transformation Age as a defining aspect of some neoplasms Both pediatric and elderly Incorporation of borderline categories At least a temporary measure
10 Early Lesions in Lymphoid Neoplasia WHO Lesions of uncertain malignant potential Lymphomatoid papulosis Lymphomatoid granulomatosis WHO 2008 greater recognition of early steps in lymphomagenesis In situ follicular lymphoma Duodenal follicular lymphoma In situ / indolent mantle cell lymphoma Monoclonal B lymphocytosis (MBL)
11 Monoclonal B Lymphocytosis (MBL) Clonal expansions of usually CD5+ B-cells in otherwise healthy persons (Marti 1992) Identified first in familial CLL Progression to CLL occurs at a rate of 1.1% per year (Rawstron et al. NEJM 2008) 13q14 deletion found in ~ 50% of MBL & CLL Usually mutated but IG gene repertoire differs from that of typical CLL (Dagklis Blood 2009)
12 Revised Criteria for CLL (WHO 2008) Diagnosis of CLL requires B-cell count greater than 5 x 10 9 or Evidence of extramedullary disease Revised to permit distinction from MBL Based on B-cell count rather than absolute lymphocyte count Bone marrow involvement may be present A Lymph node counterpart of MBL has been described
13 SLL vs. Tissue Involvement by MBL Gibson et al. Haematologica patients with CD5+ B-cell proliferations in LNs or extranodal sites (2) and monoclonal B-cell proliferations in PB c/w MBL LN architecture maintained Often discovered incidentally, on LN bx for another reason Flow cytometry monoclonal in cases studied Proliferation centers, or LN >1.5 cm are risk factors for progression
14 Follicular and Perifollicular Involvement by CD5+ B-cells Gibson et al Haematologica 2011 CD5 CD20 CD5 PC CD3 LN CD3 Expanded cuff CD20
15 Conclusions of Authors Recommend terminology of CLL/SLL-like cells of uncertain significance If PB findings are those of MBL, not CLL Minimal LN enlargement, < 1.5 cm No proliferation centers Overall architectural preservation
16 Follicular Lymphoma One of the most common lymphomas in adults, 30-40% of adult NHL BCL2/IG translocation with overexpression of BCL2 in 85% Germinal center phenotype with somatic mutation of IGH genes Most patients present with advanced stage, III/IV Generalized lymphadenopathy, BM+ Indolent course but generally incurable Median survival yrs
17 Follicular Lymphomagenesis Pre-B cell with t(14;18) arising from bone marrow Homes to germinal centers in lymph nodes Spread to other lymph nodes, spleen, bone marrow
18 Follicular Lymphoma In Situ (FLIS) Cong et al Blood 2002 Bcl-2
19 BCL2/IGH in Healthy Individuals (Limpens et al. 1991; Roulland et al. 2006) BCL2/IGH is found in peripheral blood of up to 70% of normal adults over age 50 Numbers increase with age Numbers increase with pesticide use in farmers BCL2/IGH + B-cells are not naïve B-cells Memory B-cells, Class switched Have encountered the germinal center reaction Prone to intense trafficking among germinal centers
20 Why do FLIS lymph nodes get biopsied? Usually an incidental finding LN may show reactive hyperplasia or sometimes other lymphoma Unrelated immune stimulus may lead to increased trafficking of FL-like B-cells to germinal centers
21 FL-like B-cells home to the germinal center environment Lack of progression in most patients suggests BCL2/IGH is necessary but not sufficient for neoplastic transformation Second hit is required FL-like PB B-cells & FL in situ are different phases of the same incipient neoplasia Treatment recommendations: If there no other evidence of disease, no therapeutic intervention is indicated
22 Primary FL of the Duodenum (Schmatz JCO 2011) Phenotypically and genetically similar to nodal FL (BCL2/IGH), but usually IgA+ Commonly present in duodenum other sites in distal small bowel Superficial polypoid lesions in mucosa Express homing receptor found on intestinal lymphocytes (α4β7 integrin) Local recurrences without dissemination - another type of in situ FL
23 BCL-2 CD10 CD3
24 Mantle Cell Lymphoma Usually diffuse, may show a mantle zone pattern, surrounding reactive germinal centers t(11;14) CCND1/IGH in > 90% Cyclin D1 + CD5+, Sox11+ Adults, M>F Progressive course with median survival 3-4 yrs Lack of a plateau in most series
25 In situ Mantle Cell Lymphoma Cyclin D1
26 In Situ Mantle Cell Lymphoma Clinical correlations (Carvajal-Cuenca et al. Haematologica, 2011) 5/17 (29%) composite with another B-cell lymphoma CLL, FL, MZL SOX11 expressed in 7/16 (44%) cases, in contrast to typical MCL (SOX11 pos > 90%) (Absence of SOX11 is associated with an indolent form of MCL) 12 pts with minimum 1 yr follow up (median 3 yrs) 1/12 (8%) developed MCL at four years (SOX11+)
27 In Situ Mantle Cell Lymphoma Clinical correlations in 17 cases, continued In 2 cases (both SOX11+) the in situ lesions were discovered after a dx of MCL had been made One in LN obtained 4 yrs prior to MCL diagnosis One 3 yrs after rx for MCL patient was in clinical CR In patients with MCL, FL, CLL or myeloma Retrospective studies may show evidence of the neoplastic clone years prior to diagnosis Rare cases have been transmitted via bone marrow transplant (FL, MCL)
28 Common Themes of In situ FL and MCL Low risk of progression to lymphoma Cells home to their normal compartments Germinal center or mantle cuff Often occur in association with other small B-cell lymphomas Suggests genomic instability in affected patients Breaks at BCL2 & CCND1 preferentially occur at CpG sites and involve AID and RAG (Lieber MR, Annu Rev Biochem. 2010;79: )
29 Malignant Lymphoma Why are there no benign lymphomas? Lymphocytes are cells that traffic or spread as part of their normal function Benign clonal expansions of lymphocytes do not remain localized, but disseminate based on normal lymphocyte homing Benign clonal expansions of plasma cells (sessile cells) do exist, e.g. extraosseous plasmacytoma In situ lesions are the lymphoid equivalent of benign epithelial neoplasms
30 What is the minimal definition of malignant lymphoma in 2011? Clonality is not sufficient There are many benign clonal proliferations e.g. autoimmune disease, HCV, H. pylori gastritis Cytogenetic abnormalities are not sufficient MBL has molecular alterations of CLL MGUS has molecular alterations of myeloma FL in situ has the minimal molecular alteration of FL (IGH/BCL2) Lymphoma is characterized by autonomous growth, escape from immunoregulation
31 Age as a Significant Features in Lymphoid Malignancies Newly recognized mainly pediatric lymphomas Pediatric follicular lymphoma Pediatric nodal marginal zone lymphoma EBV+ T-cell and NK-cell LPD s of childhood (CAEBV) Systemic EBV+ T-cell LPD of childhood Hydroa vacciniforme-like lymphoma
32 Pediatric Follicular Lymphoma Rare subtype in children (1-2%) Tonsils, nasopharynx, GI tract, testis Less often Nodal than adult FL Typically high grade Male >> Female 85% localized, Stage I or II 75% complete remission rate with low relapse rate Some patients cured with excision alone differential with RFH difficult
33 Histologic Features of Nodal PFL CD20 IgD
34 Nodal Pediatric FL Prominent starry sky Follicles composed of medium sized blastoid cells LN
35 CD10 BCL2 BCL6
36 Nodal Pediatric FL Histologic and Immunophenotypic Features Irregular, serpiginous, follicles, with thin or absent mantle zones Follicle centers composed of medium sized blastoid cells, not typical of CC or CB High proliferative rate, but not typical Grade 3 Starry sky Strong CD10, but negative BCL2 Negative for MUM-1
37 Comparison of Pediatric FL and Usual FL Review of Nodal FL in 62 patients under age 30 Pediatric Follicular Lymphoma Histologic Grade Site No Median Age M:F Cases (range) 15 (5-25) Grade 3 LN cases < 18 All M 7 cases > 18 Usual Follicular Lymphoma Grade 1-2 LN (18-29) 9:16 Grade 3 LN (21-28) All F Liu et al, USCAP 2011
38 Differential Diagnosis of PFL Follicular Hyperplasia with CD10+ Monoclonal B-cells (Kussick et al 2004) BCL2 Histological features show overlap with those of pediatric follicular lymphoma enlarged serpiginous follicles Distinction may be subjective
39 Pediatric Testicular Follicular Lymphoma
40 CD20 BCL-2 MIB-1
41 Heterogeneity of Follicular Lymphoma Not all follicular lymphomas are part of the same disease entity Follicular Lymphoma, Grades 1 to 2, 3A In situ follicular lymphoma Intestinal follicular lymphoma Follicular Lymphoma, Grade 3B often BCL2 neg, BCL6 R, CD10 neg, MUM-1/IRF4 + Cutaneous follicle center lymphoma Pediatric follicular lymphoma
42 Pediatric Nodal Marginal Zone Lymphomas Clinical Similarities with Ped FL Taddesse-Heath et al. AJSP 2003 Median age 16; marked M >> F Most often cervical LNs, Stage I Low risk of recurrence following surgical excision Genetic aberrations are uncommon, despite clonality by PCR or immunostains Conservative approach warranted if localized Distinguish from lymphoid hyperplasia with monotypic Lambda expression (Waldeyer s ring)
43 CD20
44 CD20
45 BCL6
46 K λ
47 IgD PTGC-like changes
48 IG PCR for immunoglobulin gene rearrangement
49 Systemic EBV+ T-cell LPD of Childhood Asian or Hispanic children Acute systemic illness with hemophagocytic syndrome Follows acute EBV infection high viral loads EBV+ T-cells are clonal May follow chronic active EBV infection (CAEBV) Overlaps with what has been termed severe CAEBV Liver Bx
50 Hydroa-vacciniforme-like lymphoma Asian or Hispanic children Lesions in sun exposed areas Chronic course but may progress to acute phase with systemic disease Cells of T-cell or less often NK cell origin EBER
51 Most EBV- associated T-cell and NK-cell neoplasms share a similar epidemiology Aggressive NK-cell leukemia Extranodal NK/T-cell lymphoma, nasal type Hydroa vacciniforme-like lymphoma (T>NK) Mosquito-bite allergy (NK >T) Systemic EBV+ T-cell lymphoproliferative disease of childhood Chronic Active EBV-infection
52 Borderline Categories B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and classical Hodgkin lymphoma B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma
53 Differential Diagnosis of Burkitt Lymphoma and DLBCL is still challenging in a subset of cases
54 Evolving Terminology for Borderline Lesions (WF 1982) Small non-cleaved, non-burkitt (REAL 1994) High grade B-cell lymphoma, Burkitt-like Provisional entity, poorly reproducible, no strict criteria (WHO 2001) Burkitt lymphoma, DLBCL Atypical BL for cases of BL with varied cytology (WHO 2008) B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma
55 MYC translocation is necessary but not specific for Burkitt Lymphoma Diagnosis % MYC R Burkitt lymphoma 100% DLBCL 5-8% Transformed follicular ~ 5 % DLBCL, high grade Lymphoblastic, TDT + De Novo Double-hit ~ 5 % Burkitt-like, DLBCL t(14;18) & t (8;14) Plasmablastic lymphoma ~ 40%
56 Gene Expression Profiling of 220 aggressive B-cell lymphomas Hummel M et al. N Engl J Med 2006;354: Identification of 3 groups mbl (molecular Burkitt) Intermediate group Non-mBL (DLBCL) Intermediate group characterized by greater genetic complexity 33% IG-MYC 21% MYC-other partner 21% IG-BCL2 7% BCL6 breaks.
57 Survival: molecular BL vs. intermediate group Hummel M et al. N Engl J Med 2006;354: Kaplan Meier Estimates of Survival According to the mbl Signature. Hummel M et al. N Engl J Med 2006;354:
58 B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma Created to deal with high grade tumors not readily classified as Burkitt lymphoma or DLBCL, probably requiring different management Poor prognosis with R-CHOP, often CNS relapse May have an intermediate gene expression profile Morphology usually not typical DLBCL or BL Most cases carry a MYC translocation MYC Complex, rather than MYC simple MYC translocation occurs as a late, secondary event in tumor evolution
59 High Grade B-cell Lymphoma with Double Hit: MYC & BCL2 BCL-2 Ki-67 BCL-6
60 Aggressive B-cell lymphomas with Double Hit involving C-MYC and BCL2 All studies have shown a poor prognosis with R-CHOP or comparable regimens Savage et al, Johnson et al, BCCA, 2009 Tomita et al, Japan, 2009 Snuderl et al, MGH, 2010 Barrans et al, UK, 2010
61 Barrans S et al. MYC rearrangement in R-CHOP treated DLBCL, JCO patients with DLBCL 245 with FISH data 35 (14%) with c-myc R 19 (54%) also with BCL2 R 3 (8%) also with BCL6 R 7 (20%) had MYC, BCL2 & BCL6 6 (17%) MYC as the sole abnormality Difficult to determine the prognostic significance of MYC alone Most were double or triple hit with MYC
62 Does C-MYC rearrangement necessarily have adverse prognostic significance? MYC+ MYC- DLBCL Rx with DA-EPOCH R impact of C-MYC on Event Free Survival; Dunleavy, Wilson et al. NCI (all negative for BCL2R)
63 Need for Improved Methodology to Detect c-myc translocations to better understand the prevalence and significance of MYC R Complete karyotyping requires fresh tissue FISH is technically demanding and results in diagnostic delay Gene expression profiling is not yet validated or available for clinical use
64 Detection of MYC R in Diagnostic Biopsies MYC+ BL MYC + Break-apart MYC rabbit monoclonal Y69 clone, Epitomics MYC+ DLBCL
65 Tonsil, 5 y.o. Fe: Focal involvement by Burkitt lymphoma
66 Immunohistochemistry for MYC
67 DLBCL negative for MYC despite high proliferative rate with KI-67 BCL2 MYC
68 Follicular Lymphoma with transformation to DLBCL BCL2 MIB-1
69 MYC immunohistochemistry Positive in DLBCL MYC immunohistochemistry Negative in follicular lymphoma
70 MYC Break In DLBCL Component MYC Both FL and DLBCL had Break in BCL2 DLBCL arising in Follicular Lymphoma FISH 73
71 Some DLBCL show elevated MYC protein in the absence of MYC-R by FISH Diagnosis MYC FISH MYC IHC Burkitt 14/14 (100%) 14/14 (100%) DLBCL, HIV+ 4/19 (21%) 16/19 (84%) DLBCL, HIV- 4/30 (14%) 19/30 (63%) Elevated MYC protein is sensitive for MYC-R by FISH but not specific for MYC-R Negative MYC by IHC is strong evidence against MYC-R Bajor-Dattilo et al., USCAP 2012
72 Significance of MYC & BCL2 TR in DLBCL Johnson et al JCO in press MYC TR+ /BCL2 neg, n = 10 Cumulative survival MYC TRneg /BCL2 neg, n = 81 MYC TRneg /BCL2 +, n = 66 MYC TR+ /BCL2 +, n = 8 P < Time (years)
73 Significance of MYC & BCL2 Protein Expression in DLBCL Johnson et al JCO in press MYC PROT+ /BCL2 neg, n = 19 Cumulative survival MYC PROT-neg /BCL2 neg, n = 72 MYC PROT-neg /BCL2 +, n = 45 MYC PROT+ /BCL2 +, n = 28 P < Time (years)
74 B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma is Aggressive B-cell neoplasm with morphological features not typical of either BL or DLBCL Proliferation rate usually lower than BL MYC translocation as a late, secondary event in tumor evolution, MYC complex, not MYC simple Frequent association with BCL2 R Adults, not reported in children Clinically aggressive Frequent involvement of bone marrow, CNS Resistant to R-CHOP and other current therapies
75 B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma is not Diffuse large B-cell lymphoma with only a high growth fraction (MIB-1/KI-67 >90%) Probably not DLBCL with isolated MYCR if double hit or triple hit not identified Burkitt lymphoma with atypical cytology Still BL, if typical genetics and phenotype, especially in pediatric age group
76 AGGRESSIVE B-CELL LYMPHOMAS WITH A MYC R BURKITT MYC/IG MYC simple EBV+/- Good prognosis Plasmablastic MYC complex EBV+ Poor prognosis B-cell, Unclassified MYC complex Poor prognosis DLBCL MYC + rare Questions Remain
77 Taxonomy of Lymphomas in the New Millennium Genomic studies will play an increasing role in defining and refining disease entities, but cannot be the sole basis for the classification of lymphomas at present A multiparameter approach to define disease entities, as exemplified by REAL/ WHO, provides a basis for diagnosis and treatment, and will continue to point the way towards further studies
78 Laboratory of Pathology Stefania Pittaluga Mark Raffeld Theresa Davies-Hill Liqiang Xi Svetlana Pack Michael Emmert-Buck Armin Jegalian Franziska Eberle Joo Song Stefan Dojcinov Qingyan Liu Peijie Cong Eva Bajor-Dattilo Metabolism Branch Wyndham H. Wilson Kieron Dunleavy Louis Staudt Acknowledgements Genetics Branch J. Keith Killian Paul Meltzer Inserm CIML Bertrand Nadel Sandrine Roulland LLMPP/ILSG John Chan, Univ of Neb Elias Campo, Barcelona Lisa Rimsza, Arizona Reiner Siebert, Kiel Randy Gascoyne, BCCA
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