Approach to Diagnosis of B-cell Lymphoproliferative Disorders. Eric Hsi, MD Department of Laboratory Medicine
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1 Approach to Diagnosis of B-cell Lymphoproliferative Disorders Eric Hsi, MD Department of Laboratory Medicine
2 No relevant financial disclosures
3 Outline The small B-cell lymphoproliferative disorders CLL MCL HCL and HCLv SMZL LPL B-PLL
4 B-CLL 90% of chronic leukemias in the West. 2-6 cases/100,000 people years Median age 65 M>F 2:1 Signs/Symptoms: Most asymptomatic Lymphocytosis (> 5x10 9 /L monoclonal B-cells with CLL phenotype) Fatigue, hemolytic anemia, infection, organomegaly/adenopathy M protein may be present
5 B-CLL Familial predisposition 5-10% have CLL in more than one family member 2-7x risk of CLL in 1 st degree relatives 1 st degree relatives have higher incidence of CLL-type MBL
6 B-CLL Morphology Small round lymphocytes Occasional prolymphocytes (usually <2%) Some cases may have irregular cells with nuclear clefting. Smudge cells
7 CLL Morphologic variation CLL with increased prolymphocytes CLL/PLL - Between 10 and 55% PL associated with worse prognosis. Atypical morphology Less condensed chromatin cleaved lymphocytes
8 CLL
9 CLL
10 CLL/PLL
11 CLL Bone marrow Involved by definition Patterns can be nodular, interstitial, diffuse Proliferation centers uncommon Diffuse pattern has been associated with higher stage and worse prognosis.
12 B-CLL Immunophenotype: CD19+, CD5+, CD20 dim+, CD23+, CD45+, CD200+, FMC7-, CD79b-/+, sig dim Genetics Rearranged Ig genes Del 13q14 (50%), trisomy 12 (20%), del 11q22-23 (20%), del 17p (10%), del 6q (5%) Trisomy 12 linked to atypical morphology Del 13q linked to typical morphology and favorable prognosis (isolated) Del 17p, del 11q22-23, and del 6q: unfavorable prognosis Del 17p in particular shows treatment resistance and short survival
13 B-CLL DDx: B-PLL, T-PLL, MCL, SMZL, FL, L-1 ALL
14 DDx FL L1-ALL MCL
15 B-CLL search for prognostic factors IgH somatic hypermutational status ( 2%) Mutated CLL better prognosis than unmutated CLL. Multiple studies have confirmed this finding. VH3-21 poor prognosis independent of mutational status FISH for recurrent abnormalities CD38 expression status predicts for OS Cutoff of 20% or 30% commonly used Associated with IGH mutational status Unmutated CLL associated with CD38 expression Mutated CLL associated with lack of CD38 expression ZAP-70 Gene expression profiling of mutated vs unmutated CLL identified ZAP-70 as differentially expressed. Hamblin et al 1999 Tobin et al Blood 2002 Damle et al 1999 Weistner et al 2003
16 IGH mutational status and CD38 predict outcome in CLL Survival by Mutational Status Survival by CD38 Status Damle et al 1999
17 Karyotypic abnormalities also predict outcome Several karyotypic abnormalities have been known to occur commonly CLL does not grow well in culture True incidence was not clear Interphase FISH allowed determination of the abnormalities Frequency and clinical significance Dohner H et al 2000
18 Genetic abnormalities in CLL Prognostic information Dohner et al NEJM 2000
19 CLL mutations and CNV Landau Cell 2013
20 Pathways for Driver Mutations Landau Cell 2013
21 CLL Median survival 7 yrs. Transformations PLL High grade (large cell) lymphoma - Richter s transformation HD-like LBL, MM (rare) Treatment: Watch/wait Nucleoside analog (fludarabine), cyclophosphamide +/- rituximab Newer targeted agents (NCCN 2017) BTK inhibitors ibrutinib (relapsed CLL, CLL with 17p/TP53 mutation) PI3K inhibitors idelalisib (relapsed CLL) BCL2 inhibitors venetoclax (relapsed CLL with 17p) Anti-CD20 mabs ofatumumab, obinutuzumab
22 Mantle Cell Lymphoma 3-10% of NHL Median age 60 yrs, M:F = 2:1 Poor prognosis - median survival 3-4 yrs. Lymphadenopathy common with presentation at high clinical stage (III or IV) extranodal sites can be involved: spleen, BM, GI tract (MLP), Waldeyer s ring
23 Mantle cell lymphoma Immunophenotype CD5+, CD10-, CD19+, CD20+, CD23-, sig+, FMC7+, CD79b+, Cyclin D1+, SOX11+ Molecular genetics t(11;14)(q13;q32) - CCND1/IGH present in vast majority of cases Blastoid variants associated with secondary changes such as tetraploid TP53 p16 deletion
24 Mantle Cell Lymphoma Diffuse, nodular, mantle zone pattern Monotonous proliferation of small cells with slight nuclear irregularity (centrocytes) Epithelioid histiocytes may be present Mitotic figures frequent (uncommon in low grade lymphomas) Aggressive cytology variants Blastoid Pleomorphic
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26
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28 CD3 CD20 CD5 Cyclin D1
29 BMCL
30 Cyclin D1
31 Mantle cell lymphoma Aggressive disease worst of low grade and high grade lymphomas Median survival 3-4 yrs but improving with newer therapies No plateau in survival curve Indolent variants Non-nodal presentation Spleen, PB involvement Often SOX11 negative High expression of SOX11, HDGFRP3 and DBN1 compared to classical MCL (suggesting a distinct biology) Orchard JA Blood 2003 Royo Leukemia 2012
32 Overall Survival: Nodal vs non-nodal Orchard JA Blood 2003
33 Indolent Leukemic MCL (without splenomegaly) Cases exist that are MBL or CLL-like Lymphocytosis without adenopathy or splenomegaly Ondrejka S Haematologica 2011
34 Indolent Leukemic MCL CD20 CyclinD1 CD20 CyclinD1 CyclinD1 Ondrejka et al Haematologica 2011 CyclinD1/SOX11
35 MCL Prognostic factors Proliferation signature has been shown by GEP studies to be of major importance in MCL Ki67 >30% associated with poor prognosis MIPI IGH mutational status Hypermutated (<97% homology) associated with favorable prognosis in MCL (59% vs 40% 5 year OS) 17p deletion (poor) NGS studies 25 significantly recurrently mutated genes Known drivers: ATM, CCND1 Tumor supressor genes: TP53 Antiapototic proteins (BIRC3) TLR2 Chromatin modifiers (MEF2B, MLL2, WHSC1) NOTCH1 and 2 Navarro et al Cancer Res 2012 Bea PNAS, 2013
36 Cyclin D1 negative MCL Approximately 5% of cases Similar GEP as typical MCL Overexpression of other D cyclin genes Morphology identical to typical MCL SOX11+ by IHC (marker for CCND1- MCL) CCND2 rearrangements in 55% of cases Usually immunoglobulin light gene partners Most often light chains (15 of 18 cases) Salaverria I et al Blood 2013 Fu K et al. Blood 2005 Nakashima M AIMM 2014
37 Enlarged Tonsil 82 yo man
38
39 CD20 CD5 Cyclin D1 LEF1 SOX11
40 Mantle Cell Lymphoma Differential Dx: SLL Mantle zone hyperplasia FCL LBL DLBCL B-PLL (blood)
41 B-PLL
42 In situ mantle cell neoplasia Uncommon (<<1% of reactive LNs) 100 reactive LNs screened by IHC none 1293 consecutive LNs from 132 patients screened by IHC none Can find in look back of patients with MCL 17 cases in largest series Adults (median age 66, M=F), incidental finding May have PB involvement by FC (CD5- or +) Can be found with other small B-cell lymphomas One case had treated MCL 4 years prior to ISMN, was followed for 1 year and developed classic MCL Typically indolent behavior with no treatment 1 of 12 patients with isolated ISMN developed MCL 4 years later (SOX11+) Carvajal-Cuenca Haematologica 2012 Adam et al Mod Pathol 2012
43 In situ mantle cell neoplasia Morphology Undistorted architecture, non-expanded mantle zones Cyclin D1+ cells in mantles, often inner portion, may find cells in GCs
44 Hairy Cell Leukemia Uncommon BCLPD - 2% of lymphoid leukemias Median age 55, M>F 5:1 Presents with splenomegaly, cytopenias, and characteristic monocytopenia.
45 HCL PB Morphology: Small lymphocyte Spongy chromatin Abundant lacy cytoplasm with peripheral cytoplasmic projections Absent or inconspicuous nucleoli Cytochemistry Strong TRAP positivity
46 HCL - PB TRAP
47 HCL Bone marrow morphology Variable infiltration Interstitial pattern is common Widely spaced cells with bean-shaped nuclei May have fried egg appearance Some cases may spindle, mimicking mast cell disease Reticulin fibrosis is common, often causing a dry tap Some cases can be hypocellular mimicking aplastic anemia Rare cases can present as a bone tumor.
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49 Spleen and Liver in HCL Red pulp infiltration with white pulp atrophy. Red cell lakes can be seen collections of RBCs in spaces lined by hairy cells. Liver shows sinusoidal infiltrates.
50 HCL Immunophenotype CD11c+, CD19+, CD20+, CD22+, CD25+, CD103+ No marker is absolute diagnostic but constellation of bright coexpression of CD22 and CD11c is characteristic. Cyclin D1 is weakly expressed in >50% of cases Genetics Rearranged IgH No specific translocations BRAF V600E
51 Discovery of BRAF V600E in HCL Whole exome sequencing in 1 patient with HCL using CD19+ purified B-cells obtained at diagnosis and CD19- purified lymphocytes obtained after therapy. Sequence variants had to be >25% of reads to allow for heterozygous mutants that were present as a major proportion of the clonal population Mutations in BRAF, CSMD3, SLC5A1, CNTN6, and OR8J1 BRAF known to be mutated in many cancers and encodes for a protein kinase involved in MAPK signaling and was targeted for additional testing Sanger sequencing of additional 47 patients and BRAF V600E was found in 100% of cases Tiacci et al. NEJM 2011
52 Hairy cell leukemia and BRAF V600E HCL HCLv BLPD* SMZL Splen L/L, u 48/48 (100) 0/22 (0) 0/16 (0) 0/21 (0) CLL B-PLL LPL FL DLBL MCL BL Method Ref 0/35 (0) 0/71 (0) 0/18 (0) 0/12 (0) Sanger Tiacci /62 (100) 16/16 (100) 0/1 (0) 2/57 (3.5) 0/91 (0) ASPCR Arcaini /1 (0) Pyro Lennerz /136 (0.7) 1/4 (25) ASPCR Langabeer /23 (100) 0/1 (0) 0/11 (0) ASPCR Tiacci /11 0/1 0/8 0/5 1/6 0/2 0/3 0/6 ASPCR Warden 2013 *non CLL, MCL, FL,
53 Mutation Specific Ab Clone VE1 32/32 cases HCL positive All 20 non-hcl mimics cases negative Further screening >200 cases of mature B-cell neoplasms identified 1 CLL case (confirmed by sequencing) Andrulis M et al AJSP 2012
54 HCL Clinical Indolent course with good response to purine nucleoside analogs deoxycorformycin and 2-deoxyadenosine (2-CDA) DDx HCLv, SMZL, PLL
55 HCL Variant Prolymphocytic variant Cells have visible nucleoli, resembling prlymphocytes Chromatin is more condensed than typical HCL Patients present with higher WBC and often have a serum paraprotein. Immunophenotype: CD25-, CD103+ TRAP - Survival is shorter than HCL and it does not respond to HCL therapy (2CDA).
56 HCL v CD19+, CD20+, CD25-, CD22+, CD11c+, CD103+, TRAP- Spleen - red pulp predominant infiltrate
57 MAP2K1 (MEK1) mutation Recently, activating mutations in MAPK21 (exons 2-3) in HCLv and IGH V-34 expression classic HCL have been discovered. 6/15 IGHV4-34 negative HCLv 4/9 IGHV4-34 positive HCLv 5/7 IGHV4-34 negatiev chcl Waterfall et al. Nat Genetics 2014
58 Lymphoplasmacytic Lymphoma Uncommon type of lymphoma (1.5% of NHL) Disease of older adults (median age 63 yrs.), slight male predominance. Commonly involves LN, spleen, BM Often associated with Waldenstrom s macroglobulinemia (IgM paraprotein, >3 gm/dl) Paraprotein can cause cryoglobulinemia, autoimmune HA, neuropathy (myelin-associated glycoprotein)
59 LPL Morphology - LN Diffuse architecture Lymphoplasmacytic cells, Dutcher bodies Plasma cells may be present as admixed cells or in clusters Interfollicular pattern recognized Parcortical or perisinusoidal involvement with sparing of overall architecture and patent sinuses epithelioid histiocytes can mimic Lennert s lymphoma Small follicles or hyperplastic follicles Marginal zone/monocytoid B-cells absent
60 LPL - BM Interstitial or diffuse involvement Small lymphocytes, plasmacytoid lymphocytes, plasma cells Occasional centroblastic or immunoblastic cells Dutcher bodies often present Lymphoplasmacytoid, lymphoplasmacytic, and polymorphous types have been described
61 Lymphoplasmacytic Lymphoma Immunophenotype CD19+, CD20+, CD79a+, sig+, cig+ CD5-, CD10- Molecular genetics MYD88 L265P in >95% of cases 50% of IgM MGUS CXCR4 mutations in 27% (NS/FS mutations) Nonsense mutation assoc higher BM involvement and symptomatic disease requiring therapy Association with Hepatitis C infection and Type II mixed cyroglobulinemia Treon SP et al Blood 2014
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65 CD20 CD5 Kappa Lambda
66 Peripheral Blood -55 yo man with anemia and high total protein -IgM kappa paraprotein
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69 CD3 CD20 CD138 Cyclin D1
70 Kappa Lambda
71 Lymphoplasmacytic Lymphoma Differential Dx: SLL Plasmacytoma Marginal zone lymphoma Multiple myeloma Lymphoplasmacytic morphology, often with t(11;14)(q13;q32)
72 66 yo woman presented with anemia and leukopenia BM Aspirate 50x
73 BM Aspirate 100x
74
75 CD138 CD20 Cyclin D1 PAX5 Kappa Lambda
76 Additional Studies FISH positive for IGH/CCND1 MYD88 L265P negative Diagnosis: Plasma cell myeloma with IGH-CCND1 and CD20 expression
77 Splenic Marginal Zone Lymphoma Older adults (median age 66) presenting with splenomegaly +/- villous lymphocytes White pulp involvement with expanded marginal zones (perifollicular areas). Mantle zones infiltrated but GC can be intact sometimes. Red pulp also involved. Nodules have darker appearance in center with lighter outer rim (monocytoid B-cells) Hilar lymph nodes have nodular and diffuse infilrate Cytology varies from center of nodule to outer rim with larger cells collecting at outer edge.
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79 SMZL Immunophenotype CD19+, CD20+, sig+ CD5-, CD10-, CD22-/+, CD11c-/+, CD25-/+ (30%+), CD103- IgD+ (may distinguish nodal and SMZL from MALT type MZL) Campo et al Am J Surg Pathol, Molecular genetic Loss of 7q22-36 in 30-40% (mirna 29a1 and mirna29b) NOTCH pathway gene mutations (40%) NOTCH2 activating mutation in 10-25% of cases. Others (SPEN, DTX1, NOTCH1) NFkB activation (50%) KLF2 inactivating mutations in 20-40% Loss of NFkB inhibitory activity Non-canonical, canonical pathways PTPRD 0% (contrast with NMZL) Chromatin modification genes (40%) KMT2D(MLL2), SIN3A, ARIDA1, EP300, CREBBP, TBL1XR1 Kiel MJ et al. J Exp Med 2012 Rossi D et al J Exp Med 2012 Clipson et al Leukemia 2015 Spina V et al Best Pract Res Clin Haaemtol 2017
80 Mutations and Pathways in MZL Spina V Best Pract Res Clinc Haematol 2017
81 De novo B-PLL An uncommon disease <1% of lymphocytic leukemias Clinical presentation Median age years at presentation Equal M:F Marked lymphocytosis, splenomegaly without lymphadenopathy, variable anemia/thrombocytopenia Morphology: >55% prolymphocytes Phenotype Mature B-cell markers: CD19, CD20, CD22, FMC7, CD79b, sig CD5 in 20-30% Cyclin D1 negative, SOX11 negative Exclude cases with t(11;14)(q13;q32)/igh-ccnd1 Dearden CE Hematology 2015 Swerdlow SH et al (Eds). WHO Classification of tumours of haematopoietic and lymphoid tissues, IARC 2008
82 B-PLL Generally poor prognosis but a minority (10-15%) may present with indolent/asymptomatic disease May persist for months years Treatment variable (no studies): Stable/indolent watchful waiting First line chemoimmunotherapy (FCR, BR) Relapse/refractory repeat chemoimmunotherapy, BCR inhibitor, trials, SCT. Dearden CE Hematology 2015
83 B-PLL Genetics MYC abnormalities (copy# and translocation) have been reported and appear relative frequently in B- PLL (>50%). Large series of well studied de novo B-PLL cases do not exist No association with Ki-67 index (translocated cases had <30% Ki67 staining) Most cases have a reported aggressive behavior Del(17p) or TP53 loss are also frequent (50%) May occur with MYC translocation Flately E et al. AJCP 2014 Lens D et al. Blood 1997 MYC/IGH Dual Fusion
84 History A 77 yo man with a history of prostate carcinoma (2000) s/p prostatectomy was noticed, at a routine check-up, to have mild thrombocytopenia CBC (Dec. 2003): WBC 6.42, Hgb 14.4, PLT 145K PMN 57%, Lymph 21%, Mono 3%, 9% abnormal lymphocytes. Flow cytometry was performed and showed 39% of lymphocytes were B-cells expressing CD5, CD19, CD20 (bright), CD23, CD79b (bright), FMC7, CD38, lambda (intermediate-bright). FISH studies for IGH-CCND1 were negative.
85 Bone Marrow
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88 CD20 PAX5 CD3 CD5
89 LEF1 SOX11 CD138 k l
90 BCL2 MYC
91 Karyotype 47-53, XY, +der(1;3)(q10;q10)x2, +4, +7, t(8;14)(q24.1;q32), +9, +der(14)t(8;14), +15, add(17)(q21), i(18)(q10)[cp20]
92 History (2) The patient was asymptomatic. Physical exam showed no adenopathy or organomegaly. CT scans of the chest/abdomen showed no adenopathy or mass. Decision was made to watch and wait. He did well with no therapy for 51 months Age 82 Pathologic fracture of the left humerus while playing golf (April 2008)
93 Humerus Biopsy
94 Humerus Biopsy Areas of necrosis were present 2 distinct infiltrates of mononuclear cells Lymphoid cells with features similar to the B-cell lymphoproliferative process originally present in the initial bone marrow biopsy (B-PLL) Immunoblastic component with features of plasmablastic lymphoma (PBL) Lambda restricted CD20 CD5 PAX5 CD138 BCL2 MYC PLL PBL Following images: PLL on left/pbl on right
95 400x original magnification B-PLL PBL
96 CD20 CD20 CD5 CD5
97 CD138 CD138 PAX5 PAX5
98 BCL2 BCL2 MYC MYC
99 PBL: Kappa PBL: Lambda
100 Additional Studies Additional IHC PBL component Cyclin D1-, HHV8-, BCL6-, MYC+, BCL2- VS38c+, Ki67 20% EBER negative Flow cytometry showed: Small B-cell component similar to prior study (CD5+/Lambda+ B-cells) IGH FR3 PCR Single peak Serum/urine protein electrophoresis negative for paraprotein The patient was treated with RCHOP x 5
101 Additional History The patient did well for 1 year and relapsed with multiple bone, soft tissue, lung mases and lymphadenopathy. He began bortezomib therapy but progressed within one month. He suffered a right hip fracture and internal fixation and biopsy was performed (next slide) demonstrating a similar plasmablastic lymphoma IHC/ISH studies showed expression of CD138, MUM1 and cytoplasmic lambda. The cells were negative for EBER, PAX5, cytoplasmic kappa. FISH for MYC rearrangement (break apart probes) was positive The patient elected hospice and died 3 months later (approx. 6 years and 2 mo. after initial diagnosis).
102 Diagnosis B-prolymphocytic leukemia with prolonged indolent phase (51 months) and subsequent transformation to plasmablastic lymphoma. Educational features: The B-PLL, despite the complex karyotype and t(8;14)(q24;q32) followed an asymptomatic indolent course Termination in a plasmablastic lymphoma that was aggressive but associated with loss of BCL2 protein.
103 Reference Age/Sex WBC Current case 77 M 6.42 Y 51 Iioka J Clin Exp Hematopat M 17.1 Y 9 Merchant Arch Pathol Lab Med F 91.8 N 0 Indolent? TFT Karyotype FISH del17p TP , XY, +der(1;3)(q10;q10)x2, +4, +7, t(8;14)(q24.1;q32), +9, +der(14)t(8;14), +15, add(17)(q21), i(18)(q10)[cp20] N NA 47, XY, +der(3)t(3;8)(p13;q13),-8,t(8;14)(q24;q32)+18[cp5]/48, XY,+add(3)(p13),t(8;14)(q24;q32)+18[2]/46,XY[4] N NA 40 45,XX,add(5)(p15),-6,+7,der(8)add(8)(p23), t(8;14)(q24;q32),add(14)(q32),der(14)t(8;14),-17[cp19]/ 46,XX[1] Y NA Put N Ann Hematol M NA N ,XY,t(8;14)(q24;q32)[13]/45,sl, 9,add(10)(q24)[6]/46,XY[4] N NL 65 M NA N ,XY,t(8;14)(q24;q32),+12,del(15)(q?15q?22),+3mar[16]/46,XY[4] N NL 68 F NA NA NA 73 M NA N ,XX,t(8;14)(q24;q32),+12,del(13)(q13q22),+18[9]/47,sl, X[8]/47,sdl1,t(1;6)(q43;q11), t(11;14)(q13;q32)[3] N NL 48,XY,t(8;14)(q24;q32),del(11)(p1?2p14),+12,del(13)(q14q22),add(16)(p13), 17,+2mar [9]/46,XY[1] Y NL 68 M NA N F NA N ,add(X)(p21)[12], Y[12],add(1)(q42)[6],add(3)(p21)[2],45 46,add(X)(p21)[12], Y[12],add(1)(q42)[6],add(3)(p21)[2],add(12)(q24)[3],der(14)t(?,8,14)(?;q24;q32)[12], 17[8],+mar[5][cp12] Y Y 45,XX,t(2;8)(p12;q24),del(3)(p12),+add(3)(q11),der(8)t(8;9)(p12;q?21), 9, 17,der(19)t( 9;19)(?p;q13)[20] Y Y 33 M NA N 5 46,XY,t(8;22)(q24;q11)[20] N N 63 M NA N ,X, Y,t(8;22)(q24;q11), 17, 20[20] Y Y 68 M NA Y 12 46,XY,t(8;22)(q24;q11),der(8)add(8)(p2?3)t(8;22)(q24;q11)[12]/92,slx2[4] N Y Crisotomo RH Leuk Res F 156 N 0 45,X,-X,add(8)(p11.2),t(8;14)(q24;q32),add(20)ql3[8]/46,XX[12] N NA Kuriakose P Cancer Genet Cytogenet F 31.2 Y > 6 46,XX,t(8;14)(q24.1;q32)[10]/46,XX[1] N NA Lens D Leukemia F 60 N 1 44,XX,der(1)t(1;17)(q42;q11),t(2;8)(p12;q24)?dic(14;17)(p11;?q11),-17, - 18,+mar[19]/46,XX[5] Y Y Flately E Am J Clin Pathol F 37.2 N 0 46,XX,t(8;14)(q24.1;q32)[2]/46,XX[19] N NA 78 M 27.8 N 0 45,XY,add(6)(q27),add(7)(q32),del(7)(q32),t(8;14)(q24.1;q32), 10,add(11)(q25),der(12),add(12)(p13),(q11.2), +1-3mar[4]/46,XY[16] hsr(12)(p13), 13,add(14)(p10), 17, 18,del(20) Y NA
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