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1 B-cell Chronic Lymphoproliferative Disorders of the Blood and Bone Marrow Disclosures I have nothing to disclose. Jeffrey L. Jorgensen, MD, PhD Department of Hematopathology, UT M.D. Anderson Cancer Center, Houston, TX Outline Chronic lymphocytic leukemia/small lymphocytic lymphoma Newer diagnostic tools Prognostic and predictive factors Refined guidelines for monoclonal B-cell lymphocytosis Hairy cell leukemia Diagnostic tools Outline Disease-defining mutation: BRAF V600E Distinction from HCL-variant Gray-zone cases?
2 CLL/SLL Most common leukemia in the Western Hemisphere ~25% of all leukemias in the U.S. 8,960 estimated new cases in 206 4,660 estimated deaths in 206 Median age ~70 years Incidence increases with advancing age ~30% under 60 y, ~5% under 50 y Morphology Small, mature-appearing appearing lymphocytes Pale-staining proliferation centers in lymph nodes, bone marrow in some cases CLL/SLL Immunophenotype Pan B-cell antigens +, most dim (CD20, CD22, CD79b, surface light chains) CD5 +, CD23 + Proliferation centers - pitfalls and prognostic factors PCs can have cyclin D expression in up to 30% of CLL/SLL Negative for SOX, t(;4) Large/confluent PCs (> one 20x field) and/or PCs with a high proliferative fraction (>40%) are a significant ifi and independent d adverse prognostic indicator 2 CLL/SLL with atypical phenotype May show decreased CD5, and/or brighter than usual pan-b-cell markers (CD20, CD22, FMC-7, and/or CD79b/light chain) Often associated with trisomy 2 Differential diagnosis includes mantle cell lymphoma, marginal zone lymphoma, other low- grade lymphomas Gradowski et al. Am J Clin Pathol 202; 38:32. 2 Gine et al. Haematologica 200; 95:526, Ciccone et al. Leukemia 202; 26:499, Falchi et al. Blood 204; 23:
3 Newer markers: LEF (Lymphoid enhancer binding factor ) Transcription factor, WNT/ β- catenin pathway Normally expressed in some T and pro-b cells but not mature B cells. Largest series: 00% positive in CLL, not in other small B-cell LPD (total of 290 B-LPD) Rare MCL reported as positive 2 Tandon et al. Mod Pathol 20; 24: O'Malley et al. Ann Diagn Pathol 207; 26:57. Ig superfamily member Widely expressed (B cells, activated T cells, thymocytes, endothelial cells and neurons) Positive in nearly all CLL cases, strong in most, including those with an atypical phenotype Most MCL are dim/negative Newer markers: CD200 Challagundla et al. Am J Clin Pathol 204; 42:837. CD200+ in a distinctive subset of MCL Newer markers: CD49d Rare (25/688, 4%) Most negative for SOX (76%) Increased proportion of non-nodal nodal leukemic variant Relatively indolent clinical course, many patients were not treated up- front Typical MCL Integrin family (α subunit), surface molecule Promotes microenvironment- i mediated proliferation of CLL leukemic cells Prognostic value independent of CD38/ ZAP70 Hu et al. Mod Pathol epub 207 CD200+ MCL Bulian et al. J Clin Oncol 204; 32:897. 3
4 CLL/SLL clinical course Most patients (80-90%) present with asymptomatic disease Treatable, but incurable (?) 5 year overall actuarial survival ~80% Death from complications of immune dysfunction and myelosuppression Outcome CLL/SLL clinical course ~/3 patients: indolent disease with normal survival ~/3 patients: initially indolent disease that progresses ~/3 patients: aggressive disease Outcome can be difficult to predict, esp. in early-stage patients Clinical markers ex. clinical stage (Rai or Binet), age, gender Histologic markers Prognostic markers ex. pattern and extent of marrow involvement Serum markers ex. 2-microglobulin, lactate dehydrogenase, thymidine kinase Cellular markers ex. lymphocyte doubling time, surface CD38, intracellular ZAP70, CD49d Molecular markers ex. IGHV somatic mutation status, cytogenetic and genetic abnormalities Reviewed in Cramer et al. Nat Rev Clin Oncol 20; 8:38. Somatic Mutation of Ig Heavy and Light Chain Variable Region Genes Normal mechanism that generates antibody diversity in response to antigen within the germinal center AICDA introduces point mutations into IGHV and IGLV,, which form the antigen binding site Results in higher affinity antigen-binding sites Tobin G and Rosenquist R. Med Oncol 2005;22:
5 IGHV somatic mutation status correlates with prognosis Mutated: 2% deviation from germline IGHV sequence Unmutated: 2% deviation from germline IGHV sequence Median survival Mutated, 25 years Unmutated, 8 years ~/2 cases mutated, ~/2 unmutated Damle et al. Blood 999; 94:840, Hamblin et al. Blood 999; 94:848. Cytogenetic Findings in CLL Conventional cytogenetic analysis Standard culture conditions 20% of cases abnormal Translocations uncommon Fluorescence in situ hybridization (FISH) 80% of cases abnormal deletions at 3q4 (~50%) trisomy 2 (~20%) deletions at q (~20%) deletions at 7p3 (~5%) deletions at 6q2 (~5%) Impact of FISH Analysis on CLL Prognosis Molecular genetic findings in CLL/SLL No disease-defining defining mutations Most common: NOTCH, SF3B, TP53, ATM, BIRC3, POT, and MYD88 Worse prognosis: TP53, ATM, NOTCH, SF3B, and BIRC3 IGVH3-2 gene usage Dohner et al. N Engl J Med 2000; 343:90. Puente et al. Nature 20; 475:0, Landau et al. Nature 205; 526:525. 5
6 Predictive factors for response to therapy in CLL/SLL Prognostic correlate with overall outcome Predictive correlate with response to therapy Abnormalities in TP53 predict lack of response to fludarabine therapy Deletions detected by conventional cytogenetics or FISH Mutations detected by PCR, NGS Non-genotoxic therapies are preferred Rossi et al. Blood 203; 2:403, Rossi et al. Leuk Lymphoma 207; 58:548. Non-genotoxic therapies for CLL/SLL B-cell receptor signaling inhibition Bruton s tyrosine kinase inhibitor: ibrutinib PI-3-kinase inhibitor: idelalisib BCL-2 inhibition: venetoclax Combination therapy with these and immunotherapy Anti-CD20: rituximab, ofatumumab Rossi et al. Leuk Lymphoma 207; 58:548. Monoclonal B-cell Lymphocytosis (MBL) Monoclonal B cells <5 x 0 9 /L in peripheral blood Not CLL/SLL, or other B-cell LPD: No lymphadenopathy, organomegaly, other extramedullary involvement Assess carefully for lymphoma if non-cll phenotype Present in up to 2% of adults with normal CBC, using highly sensitive flow cytometry Rawstron et al. Blood 2002; 00:635, Nieto et al. Blood 2009; 4:33. MBL subtypes by phenotype CLL-like (70%) Typical phenotype, CD5+, CD20 (dim), Ig (dim) Usually mutated IGHV; spectrum of FISH findings similar to CLL Atypical CLL-like (5%) CD5+, CD20 (bright) or CD23-, must rule out MCL (FISH) Karube et al. Semin Cancer Biol 204; 24:3, Xochelli et al. Blood 204; 23:99. 6
7 MBL subtypes by phenotype Non-CLL-like (5%) CD20 (mod to bright+), CD5 -/+ (20% of cases weak) Subset with genotype suggestive of splenic MZL: del(7q), t(7q), i(7q) Indolent non-nodal nodal leukemic MCL may be CD5 -/+, rule out by FISH MBCL subtypes by cell count Low count (<0.5 x 0 9 /L, most <50/μl) Very low risk of progression, no monitoring required High count (0.5 5 x 0 9 /L): Annual progression requiring treatment -2% Subset (5-9%) with high risk cytogenetic alterations Requires clinical monitoring, similar to Rai stage 0 CLL Karube et al. Semin Cancer Biol 204; 24:3, Xochelli et al. Blood 204; 23:99. Rawstron et al. Blood 2002; 00:635, Nieto et al. Blood 2009; 4:33. Hairy cell leukemia (HCL) Older patients, splenomegaly, usu. pancytopenic Monocytopenia is characteristic Infections lead to morbidity/mortality Often dry tap; BM touch prep may be key Cells intermediate in size, cytoplasm with frayed margins Preserved hairy cells usually a minority, bare nuclei common 7
8 HCL on touch prep HCL: BM biopsy morphology Pattern: interstitial infiltrate, often subtle Widely spaced cells with distinct cytoplasmic borders, fried egg appearance May mimic erythroid precursors May be misdiagnosed d as MDS, aplastic anemia HCL in bone marrow core biopsy HCL phenotype: TRAP Tartrate-resistant resistant acid phophatase (TRAP) by cytochemistry on smears: HCL strongly (+), but may be only in a few cells Not specific: some marginal zone lymphomas (MZL) are weakly (+) 8
9 HCL phenotype: TRAP HCL: Classic IHC markers DBA.44: B-cell marker, sensitive but not specific [LPL, MZL, mantle cell lymphoma may be (+)] Cyclin D is (+) in most cases Usually weak, not associated with t(;4) Useful for distinction from marginal zone lymphoma (MZL) Miranda, et al. (2000), Mod Pathol 3:308 Sherman, et al. (20), Am J Clin Pathol 36:390 HCL Classic IHC markers: Annexin A HCL: Annexin A by IHC Involved in phagocytosis, cell signaling Gene expression profiling: overexpressed in HCL Highly specific for HCL among B-cell LPD Granulocytes (+), some T cells also (+) Must correlate with a B-cell marker Background too high h for minimal i residual disease detection Falini, et al. (2004), Lancet 363:869 Sherman, et al. (20), Am J Clin Pathol 36:390 Grans+ 9
10 HCL - Newer IHC marker: TBX2 T-box transcription factor, expressed in Th cells Regulates IgG class switching, induced by CpG in B cells HCL: Most reported cases (+), often strong/uniform Other small B-cell LPDs: Many cases (+), often weaker Normal BM: rare scattered interstitial T cells (+) Low background, OK for MRD (2-5% level) HCL - Flow cytometry Characteristic immunophenotype: CDc bright+, CD22 bright+, CD25+, CD03+, CD23+, CD200 bright+ Also CD9 bright+, CD20 bright+ Subset of cases may be CD0+ Dorfman, et al. (2004), Am J Clin Pathol 22:292 Sherman, et al. (20), Am J Clin Pathol 36:390 HCL: Insights from whole exome sequencing Index case: BRAF V600E mutation identified Mutational hotspot in melanoma, papillary thyroid ca., Langerhans -cell histiocytosis Kinase upstream of MEK and ERK 47/47 HCL cases also positive 95/95 other peripheral B-cell LPDs negative HCL: Detection of BRAF V600E PCR with allele-specific oligonucleotide primers,2 0.% sensitivity in treated patients IHC for mutant BRAF 3 Suitable for diagnosis, potentially MRD Tiacci, et al. (20), N Engl J Med 364:2305 Arcaini, et al. (202),Blood 9:88, 2 Tiacci, et al. (202),Blood 9:92 3 Turakhia et al. Am J Clin Pathol 205; 44:87. 0
11 HCL: Therapy Highly sensitive to purine nucleoside analogs Pentostatin, cladribine These are immunosuppressive Relapse often responds to re-treatment Investigational: BRAF inhibitors (vemurafenib vemurafenib, dabrafenib) BTK inhibitor (ibrutinib) Immunotoxins (anti-cd22+toxin) HCL variant CBC: often higher white count, no monocytopenia Morphology: may have irregular nuclei, prominent nucleoli Immunophenotype: Often CD03+, CDc bright+, DBA.44+ Absent CD25, CD23, annexin A Genotype: No BRAF V600E mutation Not responsive to HCL front-line therapy Grever et al. Blood 207; 29:553. HCL gray zone? Small subset of cases with IGH4-34 gene usage HCL-classic phenotype (CD25+, CD23+, annexin A+) Absent BRAF V600E mutations Worse response to cladribine By WHO 2008 criteria, these are HCL-classic, but WHO 206 suggests that t they may be more closely related to HCL-variant HCL-variant cases frequently use IGH4-34 Acknowledgements Lynne Abruzzo, MD PhD, Ohio State University Jian He, MD PhD (fellow), MD Anderson Cancer Center Both kindly provided selected slides Arons et al. Leuk Lymphoma 20; 52 Suppl 2:99, Xi et al. Blood 202; 9:3330, Waterfall et al. Nat Genet 204; 46:8.
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