Aplastic Anemia and related bone marrow failures. Ryotaro Nakamura, MD Department of Hematology/HCT City of Hope National Medical Center Duarte, CA
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1 Aplastic Anemia and related bone marrow failures Ryotaro Nakamura, MD Department of Hematology/HCT City of Hope National Medical Center Duarte, CA
2 CONFLICTS OF INTEREST Advisory Board meetings: Merck, Celgene, Jazz Phamaceuticals
3 History In 1888, Paul Ehrlich first described an autopsy case of a young pregnant woman who died after a brief catastrophic illness characterized by symptoms of anemia, bleeding, and infection. He concluded from the absence of nucleated red cells in the circulation and the fatty appearance of the femur "a deficient functioning of the bone marrow." Erlich P. Ueber einem Fall von Anämie mit Bemerkungen über regenerative Veränderungen des Knochenmarks. Charité-Annalen 1888: 13:
4 Aplastic anemia: empty bone marrow with low blood counts In 1904 Vaquez and Aubertin, following Ehrlich in the discussion of a similarly fatal French case, named the disease "la forme aplastique" to emphasize "anhématopoièse."
5 History - Aplastic anemia appeared as a frequent result of industrial benzene exposure: Santesson's report of Swedish bicycle factory workers (1897) Martland's descriptions of rapidly fatal pancytopenia among Newark, NJ, leather workers ( ) - Aplastic anemia also was recognized as a rare complication of pharmaceutical use (i.e. chloramphenicol in the 1960s). Direct toxic effects were assumed to explain the disease. --- but how?
6 Epidemiology The annual incidence of aplastic anemia in Europe: 2 cases per million population. U.S.: Findings from several retrospective studies suggest that the incidence is cases per million population). Aplastic anemia is thought to be more common in Asia than in the West. The incidence was accurately determined to be 4 cases per million in Bangkok ( closer to 6 cases per million in the rural areas of Thailand). Environmental versus genetic factors? This increase is not observed in people of Asian ancestry who are presently living in the United States.
7 Natural History Poor prognosis before the era of BMT/Immunosuppression Androgen for SAA: Blood 1979; 53: 504
8 Classification: Only blood counts matter *Super (very) severe: ANC < 200/ul
9 Prognosis proportional to the degree of cytopenias (ANC)
10 Pathophysiology Empty bone marrow Reduced blood counts and hematopoietic progenitors at all levels: - committed progenitors for WBC/RBC - long term culture initiating cell - CD34+
11 Pathophysiology Deficient stroma in supporting hematopoiesis? Unlikely based on - cytokines: normal or elevated - engraftment with bone marrow transplant
12 The Nobel Prize in Physiology or Medicine 1990 Joseph E. Murray, E. Donnall Thomas Joseph E. Murray discovered how rejection following organ transplantation in man could be mastered, and E. Donnall Thomas managed to diminish the severe reaction that the graft can cause in the recipient, i.e. the so-called "graft-versus-host" reaction (GVH). In addition, Thomas could show that intraveneously infused bone marrow cells were able to repopulate the bone marrow and produce new blood cells.
13 Initial success with syngeneic bone marrow infusion without conditioning -> simply the defect of hematopoietic cells? Appelbaum et al. Blood 1980; 55: 1033 However, RR= only about 50%, which can be rescued by conditioning
14 Autoimmune Pathophysiology? Mathé et al. (BMJ 1970, Exp Hem 1976) -ALG conditioning followed by haplo-bmt led to autologous recovery of hematopoiesis Speck et al (Lancet 1977) - Prospective ALG treatment for AA : 12 of 29 responded.
15 Laboratory data for autoimmune pathophysiology Suppressive effect of patients lymphocytes on hematopoietic colony formation Suppression of erythroid-colony formation by lymphocytes from patients with aplastic anemia Hoffman R., Zanjani E. D., Lutton J. D., Zalusky R., Wasserman L. R. N Engl J Med 1977; 296: Increased Th1 cytokines: gamma IFN, TNF, IL-2 (oligo) clonal expansion of effector T cells Increased expression of IFN-gamma by both flow cytometry and microarray Expansion of specific V beta subfamilies by flow cytometry Skewing by V beta spectratyping indicative of oligoclonal expansion Oligoclonal expansion of cytotoxic T cells correlates with disease activity. Increased T-bet (transcription factor regulator for Th1 cytokines) HLA-A2 (DR1501) is over-represented in patients with AA.
16 Intracellular staining for IFN-gamma in lymphocytes from patients and healthy controls Sloand et al. Blood 2002
17 IFN-gamma-lymphocytes in a patient with AA with hematologic response/relapse Sloand et al. Blood 2002
18 Idiopathic vs. secondary AA Treatment response/prognosis - not differ after drug-induced AA Post-hepatitis AA - not due to liver transplant (high incidence only after liver transplant for acute non-a/b hepatitis not other causes) Pregnancy-associated - challenges in management - ATG can t be given. - cyclosporine with caution - termination - supportive care - pregnant again?
19 Evaluation H&P CBC, differentials, reticulocyte, chemistry, haptoglobin, etc. Bone marrow biopsy (cellularity <30%, no or minimal MgK) Cytogenetics (normal) Flow cytometry for PNH clone/lymphoproliferative disorder HLA typing Fanconi test (<40 years old or clinically suspected) NGS for somatic mutations?
20 Treatment Supportive care Transfusion: leukodepleted, irradiated Growth factors: GCSF Prophylactic antibiotics for selected cases Iron chelation for chronic patients Super severe: not usually supportable as outpatient Definitive therapy (BMT/IST) severe aplastic anemia moderate aplastic anemia with symptomatic cytopenia/transfusion dependence
21 Allogeneic BMT Standard therapy when sibling donor available BM graft preferred Cytoxan alone: 35-60% rejection attributed in part to allosensitization from transfusions Cy 50mg/kg x 4 days + ATG 30mg/kg x 3 days in late 70 s Updated results: Storb, Blume, O Donnell et al: BBMT n=94 - median age 26: 2-59) - median duration of AA: 2 months - prior IST: about 1/3
22 Allogeneic BMT (COH/FHCRC/Stanford) Figure 1. Kaplan-Meier curve of survival among the 94 patients who underwent BMT Graft rejection=4: three were salvaged with second PBSCT. Storb, Blume, O Donnell et al: BBMT 2001
23 Allogeneic BMT (COH/FHCRC/Stanford) Cumulative incidences of (A) graft rejection (B) developing acute grade II-IV GVHD in patients with aplastic anemia given HLA-identical marrow grafts following CY/ATG and GVHD prophylaxis with MTX/CSP, (C) prevalence of chronic GVHD (D) probability of survival among the 29 patients with chronic GVHD and probability of discontinuing immunosuppression Storb, Blume, O Donnell et al: BBMT 2001
24 Non-myeloablative conditioning (NIH study) Flu 125mg/m2, Cy 120mg/kg +ATG SAA with no response to ATG (10)/PNH(4) GVHD prophylaxis: CSA/MMF PBSCT All achieved engraftment GVHD 56% (II-IV) Survival 87%
25 Allogeneic BMT (CIBMTR)
26 Allogeneic BMT (CIBMTR)
27 MUD transplants for AA Reference Year of BMT N Age Conditioning Graft failure Survival NMDP (0.9-47) Cy/TBI (LNI or ATG) 11% 36% IBMTR % (<20yo) 35% (21-40yo) NMDP (1.3-46) Cy/ATG/2-6G TBI 2% 58% JMDP (1-46) Cy/ATG/TBI or LNI 11% 56% NMDP update (1-53) Cy/ATG/2G TBI 5% 55% (5 year) * no significant difference in survival between < 1yr vs. > 1 yr from the diagnosis
28 Minimum Effective Dose of Total Body Irradiation in MUD BMT for SAA Cyclophosphamide plus ATG conditioning is insufficient for sustained hematopoietic reconstitution in patients with severe aplastic anemia transplanted with marrow from HLA-A, B, DRB matched unrelated donors [letter]. Blood. 1994;83: Prospective study to determine the minimal dose of TBI sufficient to achieve sustained engraftment when it is used in combination with ATG 30 mg/kgx3 days, Cy 50 mg/kg x 4 days. to determine the tolerability and toxicity of the regimen. The starting dosage of TBI was cgy following CY/ATG The TBI dose was to be escalated in increments of 200 cgy if graft failure occurred in the absence of prohibitive toxicity, and de-escalated for toxicity in the absence of graft failure. Biology of Blood and Marrow Transplantation 7: (2001)
29 Minimum Effective Dose of Total Body Irradiation in MUD BMT for SAA Biology of Blood and Marrow Transplantation 7: (2001)
30 Minimum Effective Dose of Total Body Irradiation in MUD BMT for SAA Blood. 2006;108:
31 Minimum Effective Dose of Total Body Irradiation in MUD BMT for SAA Cy-ATG with 200cGy TBI as the standard Blood. 2006;108:
32 Minimum Effective Dose of Cytoxan when Flu was added in MUD BMT for SAA: BMT CTN 0301 ATG: day -4 to -2 (H 30mg/kg or R 3mg/kg) Fludarabine: day -5 to -2 (120mg/m2) TBI 200: day -1 Cy 0mg/kg: 3/3 graft failure Cy 150mg/kg: NRM 50% Cy 100mg/kg and 50mg/kg: continued for phase II Lancet Haematol. 2015; 2(9): e367 e375
33 BMT CTN 0301 Lancet Haematol. 2015; 2(9): e367 e375
34 Immunosuppressive therapy ALG: 12/27 responses (Lancet 1977) ATG: Champlin et al. ATG vs. supportive care (NEJM 1983) ATG/CSA: 40mg/kg x 4days+CSA, lower prednisone NIH study (Blood 1995) - 55 patients - response rate: 67% at 3 months, 78% at 1 year - relapse: 36% a 2 years - survival: 72% at 2 years ATG/CSA vs. ATG: SAA: 65% vs. 39% (p=0.03) (NEJM 1991) ATG vs. CSA: NS but the response rate was only 20% in both with 3 months crossover -> not interpretable (1992). A randomized trial of standard immunosuppression versus cyclosporine and filgrastim in severe aplastic anemia [Abstract] Blood. 1997;90(Suppl 1):439-a. ATG/CSA vs. CSA: non-severe AA: 74% vs. 46% (p=0.02) (Blood 1999)
35 Supportive care during ATG Safe but difficult Severe infusion reactions: fever, rigor, hives, hypotension, anaphylaxis Usually worse on days 1-2 than days 3-4 Anti-histamine, Tylenol, generous use of steroids: 1mg/kg/d + additional 1mg/kg during infusion Secure central line 1:1 nursing, ICU as necessary immediate drop in counts with quick recovery to the baseline (in a few days) Response: 2-3 months after ATG Subacute immunologic effects (serum sickness median onset ~ day 10) Continue prednisone around 1mg/kg/d through day 10, then rapid taper Can be self-limiting Increase in steroids can quickly improve Note: - Corticosteroids are not part of IST. - Don t do skin test.
36 Immunosuppressive therapy Follow up NIH study 122 patients (31<18yo, 91 > 18 yo) Response: 60% at 3 months, 61% at 6 months - survival: 55% at 7 years - relapse: 35% at 5 years but no impact on survival Late clonal evolution (MDS/AML) about 20% at 10 years Plt or ARC > 50k/ul at 3 months predicted a better survival (90% vs. 42%) JAMA Mar 5;289(9):1130-5
37 High-dose Cytoxan (200mg/kg over 4 days) 19 patients with SAA (9=VSAA) median age 47 median time to ANC >0.5: 49 days RR=65% 4 deaths (infection/bleeding) No relapse/clonal evolution!! Brodsky et al. (Annal Int Med 2001)
38 High-dose Cytoxan HD cytoxan as salvage (Exp Hem 2004) 53% RR 1 PNH and 1 MDS in non-responders Cy+CSA versus ATG+CSA (NIH study: Lancet 2000) 31 pt (15=Cy/CSA, 16=ATG/CSA) no difference in RR more early deaths in Cy (3 in the first 3 months) more invasive aspergillosis in Cy (4 vs 0) relapse 25% in Cy, 43% in ATG (p=ns) no difference in PNH clone size in each arm post Tx cytogenetic abnormality: 2/13 in ATG, 1/12 in Cy (ns)
39 Types of ATG: horse vs. rabbit? N Engl J Med. 2011;365(5): Year of Rabbit
40 Types of ATG: horse vs. rabbit? N Engl J Med. 2011;365(5): Year of Rabbit
41 Types of ATG: horse vs. rabbit? N Engl J Med. 2011;365(5): Year of Rabbit
42 Salvage IST Causes of treatment failure and relapse in aplastic anemia Exhaustion of stem cell reserves Insufficient immunosuppression/persistent immune attacks Hereditary bone marrow failure Non-immune pathogenesis Salvage Immunosuppressive therapy GITMO: r-atg (3.5mg/kgx5days) after failing h-atg 30 patients median interval from h-atg: 151 days 77% transfusion independence BJH 1999; 107: 330
43 Salvage therapy - eltrombopag (Promacta) Eleven of 25 patients (44%) had a hematologic response in at least one lineage at 12 weeks, with minimal toxic effects. N Engl J Med 2012;367:11-9.
44 Eltrombopag Added to Standard Immunosuppression for Aplastic Anemia N Engl J Med Apr 20; 376(16):
45 Faster recovery, better response rate with eltrombopag added to standard immunosuppression for aplastic anemia
46 1 st line therapy: IST or BMT? IBMTR survival data ( ) Age 1-20: 75+3% 21-40: 68+4% > 40: 35+18% Age and ANC: BMT for - Younger Pts - Severely neutropenic
47 Therapeutic Algorithm Age cutoff? HD Cytoxan? + Promacta
48 Cumulative Incidence of Observed Cancers in 860 Patients with Aplastic Anemia Who Received Immunosuppressive Therapy and 748 Patients Who Underwent BMT Socie, G. et al. N Engl J Med 1993;329:
49 Late Events After Immunosuppressive Therapy Rosenfeld, S. et al. JAMA 2003;289:
50 Distinct outcomes for cytogenetic abnormalities Maciejewski, J. P. et al. Blood 2002;99:
51 Case 1 44 yo female presented with pancytopenia in 1996 WBC 2,300/uL, Hb 7g/dL, plts 15,000/uL. Bone Marrow (next slide): variable cellularity, mild dysplasia No clonal T or B cell population Sucrose test negative Cytogenetics: trisomy 8 in 1/30 metaphases. Treated with ATG and CSA, achieved transfusion independence, but remains dependent on GCSF and Epo for anemia. 2002: WBC 10,000/uL, Hb 9.1g/dL, plts 115,000/uL Trisomy 8: 10/20 metaphases
52 Case 1 HLA typing: HLA DR1501
53 Cytogenetic abnormalities in PNH: occurring in GPI-AP positive population Flow-sorting for GPI-AP, followed by FISH patient 2: 57% GPI-AP neg patient 3: 10% GPI-AP neg 12% t-8 0% t-8 45% t-8 0% t-8 BJH 2003
54 Dr. Dameshek s riddle (Blood 1967) What do AA, PNH, and hypoplastic leukemia have in common? 1) frequency of development of PNH in his AA patients 2) overlap between the syndrome of AA and PNH 3) similar high prevalence of both AA and PNH in the Orient That a single insult to the marrow may be responsible for bringing about different kinds of abnormalities, sometimes occurring together,sometimes sequentially, deserves consideration, not only from the conceptual standpoint but from the experimental approach as well.
55 Bone Marrow Failure Syndrome
56 Somatic mutations and clonal hematopoiesis in aplastic anemia NEJM 2015; 373: 35-47
57 NEJM 2015; 373: 35-47
58 Somatic mutations and clonal hematopoiesis in aplastic anemia NEJM 2015; 373: 35-47
59 Somatic mutations and clonal hematopoiesis in aplastic anemia NEJM 2015; 373: 35-47
60 Components of MDS Diagnosis Clonal hematopoiesis Dysplastic morphology Cytopenia
61 Diagnostic Challenges Overlap bone marrow failure syndrome Aplastic anemia red cell aplasia amegakaryocytic thrombocytopenia agranulocytosis Hypoplastic MDS Large granular lymphocyte disease (CD3/CD8/CD57, TCR gene rearrangement) Co-existing PNH clone Idiopathic thrombocytopenic purpura Metabolic (B12, copper deficiency) Other systemic medical illnesses associated with cytopenia (infectious disease, autoimmune disease, liver disease etc.)
62 Indolent Myeloid Hematopoietic Disorders Idiopathic Cytopenias of Unknown Significance (ICUS) Idiopathic Dysplasia of Unknown Significance (IDUS) Clonal Hematopoiesis of Indeterminate Potential (CHIP) Clonal Cytopenias of Unknown Significance (CCUS) Feature ICUS IDUS CHIP CCUS MDS Somatic mutation - - +/- +/- +/- Clonal karyotipic abnormality - - +/- +/- +/- Marrow dysplasia Cytopenia
63 Components of MDS diagnosis and spectrum CHIP Clonal hematopoiesis IDUS Dysplastic morphology MDS CCUS ICUS Cytopenia
64 Summary Diagnostics - Stay open-minded for overlap conditions (naming it doesn t mean understanding it) Pathophysiology of cytopenia in BMF Production failure? - Autoimmune suppression (T cell-mediated SAA, LGL) - Ineffective hematopoiesis (clonal disorders MDS) Peripheral destruction? - Intravascular hemolysis and associated thrombocytopenia (PNH)
65 Summary Management - Importance of supportive care - Transfusion - Antibiotics - Iron chelation - Toxicities and response kinetics of IST - Dynamic decision making process for IST vs. BMT - Consideration for late clonal disorders if IST - BMT: well established using MRD/MUD, - Clinical trials for alternative donor BMT
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