CME/SAM. Mixed Phenotype Acute Leukemia
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1 AJCP / Original Article Mixed Phenotype Acute Leukemia A Study of 61 Cases Using World Health Organization and European Group for the Immunological Classification of Leukaemias Criteria Olga K. Weinberg, MD, 1 Mahesh Seetharam, MD, 2 Li Ren, 3 Ash Alizadeh, MD, PhD, 3 and Daniel A. Arber, MD 3 From the 1 Boston Children s Hospital, Boston, MA; 2 Arizona Oncology, Scottsdale; and 3 Stanford University Medical Center, Stanford, CA. Key Words: Mixed phenotype acute leukemia; Biphenotypic; Bilineal Am J Clin Pathol December 2014;142: ABSTRACT Objectives: The 2008 World Health Organization (WHO) classification system grouped bilineal and biphenotypic acute leukemias together under a new heading of mixed phenotype acute leukemia (MPAL). The lineage-specific marker criteria have also changed for a diagnosis of MPAL. The goal of this study was to characterize clinical significance of this new group. Methods: Sixty-one patients diagnosed with MPAL using either European Group for the Immunological Classification of Leukaemias (EGIL) criteria or 2008 WHO criteria were included in this study. Results: Sixteen patients (26%) diagnosed with acute biphenotypic leukemia using EGIL criteria did not fulfill 2008 WHO criteria for MPAL. Cytogenetic data were available for 32 patients, and the most common abnormality was t(9;22) (five of 32 cases). Clinical outcome data suggested that younger patients with MPAL (<21 years) had better overall survival (OS) in both the EGIL and WHO groups (EGIL, P =.0403; WHO, P =.0601). Compared with 177 patients with acute myeloid leukemia (AML), MPAL patients had better OS (P =.0003) and progression-free survival (P =.0001). However, no difference in OS between MPAL and 387 patients with acute lymphoblastic leukemia was present (P =.599). Conclusions: As defined by the 2008 WHO classification, fewer patients are now classified as having MPAL than with the EGIL criteria. In this study, patients with MPAL have a better clinical outcome compared with patients with AML. Upon completion of this activity you will be able to: summarize criteria of leukemias that should be included in mixed phenotype acute leukemia as defined by the 2008 World Health Organization (WHO) classification. contrast the 2008 WHO definition with the prior definition used by the European Group for the Immunological Classification of Leukaemias. list the markers needed for lineage determination as defined by the 2008 WHO classification. The ASCP is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The ASCP designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 Credit per article. Physicians should claim only the credit commensurate with the extent of their participation in the activity. This activity qualifies as an American Board of Pathology Maintenance of Certification Part II Self-Assessment Module. The authors of this article and the planning committee members and staff have no relevant financial relationships with commercial interests to disclose. Questions appear on p 878. Exam is located at Acute leukemia with a mixed phenotype is a rare disease and comprises 2% to 5% of all acute leukemias. These disorders have been historically labeled by a variety of names, such as mixed lineage leukemia, bilineal leukemia, and biphenotypic leukemia, and the criteria for diagnosis have often been arbitrary. 1 One of the first major attempts to define this disorder was the scoring criteria proposed by the European Group for the Immunological Classification of Leukaemias (EGIL). 2 A score was assigned for specific myeloid or lymphoid markers expressed by the blasts, and biphenotypic acute leukemia was defined when a score more than 2 points was achieved for each lineage Table 1. 2,3 The 2001 World Health Organization (WHO) classification of hematopoietic and lymphoid neoplasms incorporated the EGIL scoring system when defining acute leukemias of ambiguous lineage. 4 CME/SAM Am J Clin Pathol 2014;142:
2 Weinberg et al / Mixed Phenotype Acute Leukemia Table 1 European Group for the Immunological Classification of Leukaemias Scoring System for Biphenotypic Acute Leukemia 3 Points a B Lineage T Lineage Myeloid Lineage 2 CD79a CD3 (m/cyt) Anti-MPO (antilysozyme) cyt IgM Anti-TCR a/b cyt CD22 Anti-TCR g/d 1 CD19 CD2 CD117 (c-kit) CD10 CD5 CD13 CD20 CD8 CD33 CD10 CD65s 0.5 TdT TdT CD14 CD24 CD7 CD15 CD1a CD64 a More than 2 points are required to assign a lineage. Table World Health Organization Classification: Acute Leukemias of Ambiguous Lineage Lineage Myeloid T lineage B lineage Marker Myeloperoxidase OR Monocytic differentiation (at least two of the following: NSE, CD11c, CD14, CD64, or lysozyme) Cytoplasmic CD3 OR Surface CD3 Strong CD19 and at least one of the following with strong expression: CD79a, cytoplasmic CD22, or CD10 OR Weak CD19 and at least two of the following with strong expression: CD79a, cytoplasmic CD22, or CD10 In 2008, the WHO classification proposed a simpler diagnostic algorithm to define mixed phenotype acute leukemia (MPAL), which relies on fewer, more lineage-specific markers Table 2. 5 Briefly, myeloid lineage requires the presence of myeloperoxidase as detected by flow cytometry, immunohistochemistry, or cytochemistry or evidence of monocytic differentiation (with at least two of the following markers being positive: nonspecific esterase cytochemistry, CD11c, CD14, or CD64). T lineage can be shown with cytoplasmic or surface CD3, and multiple antigens are required for B lineage, including CD19, CD79a, CD22, and CD10. MPAL with t(9;22) and MLL rearrangement have been separated as distinct subtypes. The remaining cases are now designated as MPAL, not otherwise specified. 5 A specific reference is now made in the 2008 WHO classification to exclude cases that can be classified in another category, either by genetic or clinical features. For instance, acute myeloid leukemia (AML) with t(8;21), t(15;17), and inv(16) can express lymphoid-associated markers but should be classified as AML with recurrent genetic abnormalities. Cases of chronic myelogenous leukemia (CML) in blast crisis, AML with myelodysplasia-related changes, and therapyrelated AML should be classified as their respective entities even if they happen to have a mixed phenotype. In their study, van den Ancker et al 6 found a significant difference in the number of patients defined by the EGIL and 2008 WHO classification (30 vs 8; 5.8% vs 1.5%), and the difference between the two groups was largely due to reclassification of a subset of cases as AML with the 8;21 translocation, AML with myelodysplasia-related changes, therapy-related acute leukemia, or CML in blast crisis. Information about clinical characteristics and frequency of patients with MPAL is limited. Using the definition proposed by the 2008 WHO classification, a recent study of 100 MPAL cases found that although this disease affects both children and adults, it is more common in adults. 7 Blasts in most cases showed myeloid and B- or T-lymphoid lineage, with only rare cases involving all three lineages. 7 No correlation was found between age, morphology, immunophenotype, or cytogenetics. Most patients in this study had a complex karyotype (24 cases or 32%), and only 28% of their cases were classified as MPAL with t(9;22)/bcr-abl and MPAL with 11q23/MLL rearrangements. Similarly, Yan et al 8 looked at 117 patients with MPAL as defined by the 2008 WHO classification and found that 22 (24%) of 92 cases with available karyotypes showed a complex karyotype. However, in the 2008 WHO classification, patients with a complex karyotype (which is considered a myelodysplastic syndrome related cytogenetic abnormality) should be classified as having AML with myelodysplasia-related changes. 5 The overall frequency of MPAL when defined by the 2008 WHO criteria is not yet clear. Al-Seraihy et al 9 retrospectively evaluated 633 children younger than 14 years with acute leukemia and found that 24 (3.8%) of these cases were classified as biphenotypic acute leukemia using the EGIL criteria, while 11 (1.7%) were categorized as MPAL using the new 2008 WHO criteria. The goal of our study was to characterize the new MPAL group as defined by the 2008 WHO classification and to compare this with the previously used EGIL definition in both adults and children. We looked for differences in clinical presentation and outcome in patients with MPAL as defined by the EGIL and 2008 WHO classification. The outcome of newly defined MPAL group was compared with a group of patients with acute lymphoblastic leukemia (ALL) and AML. Materials and Methods Patients Sixty-one patients diagnosed with MPAL or acute biphenotypic/bilineal leukemia at Stanford University from 804 Am J Clin Pathol 2014;142:
3 AJCP / Original Article Table 3 Summary of Clinical Data and Immunophenotype Data in All Patients With Mixed Phenotype Acute Leukemia a Characteristic Total (n = 61) EGIL (n = 59) 2008 WHO (n = 45) T/Myeloid (n = 14) B/Myeloid (n = 30) Sex, No. Female Male Age, Median (range), y 32 (1-84) 32 (1-84) 28 (1-78) 30 (1-76) 25 (1-78) WBC, median (range), 10 9 /L 24.2 ( ) 25.0 ( ) 27.9 ( ) 15.1 ( ) 21.9 ( ) Hemoglobin, median (range), g/l 9.1 ( ) 9.1 ( ) 9 ( ) 8.8 ( ) 9.1 ( ) Platelets, median (range), 10 9 /L 53 (8-220) 53 (8-220) 46 (8-268) 51 (12-180) 57 (8-220) Bone marrow blasts, median (range), % 70 (19-98) 70 (19-98) 70 (20-96) 65 (21-98) 77 (19-98) Immunophenotype, No. CD34 41/61 39/59 31/45 9/14 21/30 cmpo 44/61 44/59 44/45 14/14 29/30 CD13 43/61 43/52 30/40 10/13 20/27 CD14 5/33 5/33 4/26 0/8 4/18 CD64 6/33 6/33 6/27 2/9 4/18 CD33 50/57 50/55 35/42 11/12 23/29 CD117 22/38 22/38 15/29 9/10 6/18 CD19 39/55 39/55 31/45 0/14 30/30 CD20 5/42 5/42 3/32 0/14 3/17 CD10 29/53 29/53 24/41 3/11 21/29 CD22 20/38 20/37 16/37 0/14 16/22 CD79a 32/41 31/40 25/32 2/8 22/23 ccd3 18/42 17/38 15/32 14/14 0/17 CD2 8/38 8/38 4/31 4/14 0/16 CD5 4/40 6/38 4/31 4/14 0/16 CD7 23/41 23/39 15/31 12/14 2/16 EGIL, European Group for the Immunological Classification of Leukaemias; WHO, World Health Organization. a One case had the B, T, and myeloid phenotype to 2009 using either EGIL or 2008 WHO criteria were studied. All cases were diagnosed with bone marrow aspirates, blood smears, trephine biopsies, and/or flow cytometry. Clinical parameters, hemogram data, and flow cytometry results at the time of diagnosis were reviewed. In the flow cytometry study, a marker was considered positive when 10% or more of the blasts reacted with a definite intensity shift greater than a corresponding negative control. Clinical follow-up information was obtained by retrospective review of the electronic charts. Similarly, a group of 387 ALL and 177 AML cases diagnosed during the same period with clinical outcome in the form of overall survival (OS) was used in the clinical outcome comparison. This study was approved by Stanford University s institutional review board. Statistical Analysis OS, progression-free survival (PFS), and complete response were defined as previously described. 10 These parameters were compared using Kaplan-Meier methods and the log-rank test. Univariate and multivariate Cox proportional hazards models were performed. Quantitative factors were treated as continuous variables in these regression models. Categorical variables were compared using the Fisher exact test. Results Clinical Features Sixty-one patients, including 36 males and 25 females with a median age of 32 years (range, 1-84 years), were studied. Twenty-three patients (38%) were younger than 21 years. The median white blood cell count at presentation was /L, hemoglobin was 9.1 g/l, platelets were /L, and blast count in the marrow was 70% Table 3. Follow-up information was available in 31 patients. The mean follow-up time was 450 days, with a range between 60 and 3,440 days. The median PFS was 360 days. Fourteen (45%) patients achieved complete remission, and 13 (42%) relapsed after remission. Of the 31 patients, 12 (39%) died of treatment complications. Six (19%) patients received a bone marrow transplant. The treatments were variable and included the following protocols: CALGB 8811 (two patients), CALGB 9511 (two patients), POG 9404 (two patients), AML 2002 (two patients), and hyper-cvad (two patients). The rest of patients received variable treatments, including vincristine, daunorubicin, AraC, and others. Pathologic Features Of the 61 patients included in the study, two (3.3%) were classified as having MPAL using the 2008 WHO classification Am J Clin Pathol 2014;142:
4 Weinberg et al / Mixed Phenotype Acute Leukemia Table 4 Cytogenetic Data in All Patients With Mixed Phenotype Acute Leukemia Divided by EGIL and 2008 WHO Status a Characteristic Total (n = 61) EGIL (n = 59) 2008 WHO (n = 45) T/Myeloid (n = 14) B/Myeloid (n = 30) Cytogenetics Normal t(9;22) t(v;11q23)/mll Abnormalities in chromosome Abnormalities in chromosome EGIL, European Group for the Immunological Classification of Leukaemias; WHO, World Health Organization. a Values are presented as numbers. but did not reach EGIL criteria for mixed phenotype leukemia (Table 3) Table 4. One of these cases had a B/myeloid phenotype with coexpression of CD19, CD10, ccd79a, TdT, CD34, HLA-DR, and MPO. This immunophenotype gives a score of 3 for B lineage but only 2 points for myeloid phenotype in the EGIL criteria. The other case showed blasts with coexpression of ccd3, CD34, CD13, CD33, and MPO, which would be assigned 4 points for myeloid lineage but only 2 points for T lineage in the EGIL criteria. Both of these cases would be classified as MPAL in the 2008 WHO classification but not in the EGIL classification. Sixteen (26%) patients diagnosed with biphenotypic leukemia using the EGIL classification did not meet criteria for MPAL using the 2008 WHO classification. Of these 16 patients, eight had T-lymphoblastic leukemia and eight had B-lymphoblastic leukemia using the 2008 WHO classification. All expressed myeloid markers but did not include MPO or evidence of a monocytic lineage, which is required by the 2008 WHO classification for establishing myeloid lineage. 5 Comparison of clinical presentation data showed no significant differences in age, presenting CBC parameters, or bone marrow blast percentage among patients with MPAL as defined using EGIL vs 2008 WHO criteria (Table 3). Of the 45 cases diagnosed with MPAL using the 2008 WHO criteria, 14 (31%) had the T/myeloid phenotype, 30 (67%) had the B/myeloid phenotype, and one (2%) showed immunophenotypic evidence of a B, T, and myeloid lineage in one blast population. Forty-four (98%) expressed MPO by flow cytometry, immunohistochemistry, or cytochemistry and two showed evidence of monocytic differentiation with expression of CD14 and CD64. Ten (16%) cases had two separate blast populations and would be considered acute bilineal leukemia. Six of these 10 bilineal cases had B/myeloid leukemia and four had T/myeloid leukemia. Comparison of hemogram data between B/myeloid and T/myeloid showed no difference in age, presenting CBC parameters, or bone marrow blast percentage (Table 3). Cytogenetic Abnormalities Among the 32 cases with successful cytogenetic studies, 18 had abnormal karyotypes (Table 4). Five (16%) patients had translocation between chromosomes 9 and 22. Two of these five patients were children. Two (6%) patients had MLL translocations. Other abnormalities included chromosomes 5, 7, and 9. Fourteen (44%) patients had a normal karyotype. Two patients who had blasts with a mixed phenotype but had a complex karyotype on cytogenetic analysis were excluded from this study (since they would be classified as having AML with myelodysplasia-related changes in the 2008 WHO classification). Clinical Outcome Clinical outcome data showed no significant differences in OS or PFS among patients with MPAL using the 2008 WHO criteria compared with patients defined by the EGIL criteria (OS, P =.639; PFS, P =.474) Figure 1. Even after dividing patients by age (<21 or >21 years) into childhood and adult groups, no difference in outcome between patients with MPAL using the 2008 WHO criteria and those using the EGIL criteria was identified. However, overall younger patients (<21 years) had or trended toward better OS compared with older patients (>21 years) in both the EGIL and WHO groups (EGIL, P =.0403; WHO, P =.0601; Figure 1). Comparing the outcome of B/myeloid vs T/myeloid groups showed no differences in OS or PFS (OS, P =.96; PFS, P =.533). Comparison of outcome by expression of MPO, cytoplasmic CD3, CD19, cytoplasmic CD79a, or CD10 on blasts showed no significant difference in OS or PFS. Compared with all 177 patients with AML, all patients with MPAL had better OS (P =.0003) and PFS (P =.0001) Figure 2. However, no difference in OS between patients with MPAL and ALL was present (P =.599; Figure 2). Discussion The 2008 WHO classification system grouped bilineal and biphenotypic acute leukemias together under a new heading of MPAL. The diagnosis of MPAL is assigned to a case of acute leukemia that shows expression of a combination of antigens of different lineages, so it is not possible to assign a single lineage. A specific reference is now made to exclude 806 Am J Clin Pathol 2014;142:
5 AJCP / Original Article A B WHO 21 years old EGIL >21 years old ,000 1,500 2,000 2,500 3,000 3,500 4, ,000 1,500 2,000 2,500 3,000 3,500 4,000 Figure 1 Comparison of clinical outcome (overall survival) by grouping patients with mixed phenotype acute leukemia by 2008 World Health Organization (WHO) vs European Group for the Immunological Classification of Leukaemias (EGIL) criteria. Clinical outcome was obtained by dividing patients by age (<21 vs >21 years) in both WHO and EGIL groups. A, P =.639. B, WHO, P =.06; EGIL, P =.04. A AML (n = 177) MPAL (n =31) ,000 1,500 2,000 2,500 3,000 3,500 4,000 B ALL (n = 387) MPAL (n = 31) 0 1,000 2,000 3,000 4,000 5,000 6,000 7,000 8,000 9,000 Figure 2 Comparison of outcome in overall survival of all patients with mixed phenotype acute leukemia (MPAL) with a group of patients with acute myeloid leukemia (AML) and acute lymphoblastic leukemia (ALL). A, P = B, P =.599 cases that can be classified in another category, either by genetic or clinical features. In our study, of 61 patients, only 45 (74%) reached criteria for MPAL using the 2008 WHO classification. This is in accordance with another study, 6 which suggests that fewer patients will be classified as having MPAL in the 2008 WHO classification. In this study, we evaluated 61 patients who were classified as having MPAL using either the EGIL or 2008 WHO criteria. Twenty-three (38%) of 61 patients were younger than 21 years. Most cases showed a B/myeloid phenotype (67%) and had normal cytogenetics (44% of patients with cytogenetic information). Seven (22%) patients had t(9;22) or MLL translocations. This distribution is similar to what Matutes et al 7 found in their study. However, both Matutes et al 7 and Yan et al 8 included patients with MPAL who had a complex karyotype (~24%-32% of all their patients) in their series. In the current 2008 WHO classification, the presence of a complex karyotype would be considered AML with myelodysplasia-related changes if defined by cytogenetics alone, and such cases were excluded from our study. Am J Clin Pathol 2014;142:
6 Weinberg et al / Mixed Phenotype Acute Leukemia There are no set treatment protocols for patients with MPAL, which makes evaluation of outcome difficult in studies of this entity. In our study, patients received variable treatments, including both ALL and AML protocols such as CALGB 8811 or 9511, POG 9404, or AML A few studies have compared the outcome of patients with MPAL with matched AML or ALL controls They found that survival of patients with biphenotypic leukemia was worse compared with that of matched controls with AML or ALL. In our study, patients with MPAL had better OS and PFS compared with a group of patients with AML, while no difference was found between patients with MPAL and ALL. This finding might be related to the different criteria used in diagnosis of MPAL (most used EGIL in the prior studies) but could also be related to different therapies used and a small number of patients in studies. Few studies have compared B/myeloid with T/myeloid MPAL groups under the 2008 WHO classification. We found no difference in clinical presentation or in clinical outcome between these two groups. Similarly, no significant difference was found in clinical presentation or outcome between patients who met the EGIL criteria compared with those using the 2008 WHO criteria for MPAL. Presentation at a younger age (<21 years) was associated with a more favorable prognosis in both OS and PFS in the EGIL and 2008 WHO groups. In summary, we have shown in this study that fewer patients are now classified as having MPAL using the 2008 WHO classification. Most of the patients have a B/myeloid phenotype, with fewer having a T/myeloid phenotype or a mixed B, T, and myeloid phenotype. Most patients have a normal karyotype, and only few have t(9;22) or MLL translocations. Clinical treatments are not well defined in this group, and further studies are needed to study the genetic abnormalities to determine pathogenesis and treatment. Address reprint requests to Dr Weinberg: Dept of Pathology, Children s Hospital Boston, 300 Longwood Ave, Boston, MA 02115; Olga.weinberg@childrens.harvard.edu. References 1. Weinberg OK, Arber DA Mixed-phenotype acute leukemia: historical overview and a new definition. Leukemia. 2010;24: Bene MC, Castoldi G, Knapp W, et al. Proposals for the immunological classification of acute leukemias. European Group for the Immunological Characterization of Leukemias (EGIL). Leukemia. 1995;9: European Group for the Immunological Classification of Leukaemias. The value of c-kit in the diagnosis of biphenotypic acute leukemia. Leukemia. 1998;12: Jaffe E, Harris N, Stein HVJ, et al, eds. Pathology and Genetics of Tumors of Hematopoietic and Lymphoid Tissues. 2nd ed. Lyon, France: IARC; Borowitz MJ, Bene MC, Harris NL, et al. Acute leukemias of ambiguous lineage. In: Swerdlow SH, Campo E, Harris NL, et al, eds. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Lyon, France: IARC; 2008: van den Ancker W, Terwijn M, Westers TM, et al. Acute leukemias of ambiguous lineage: diagnostic consequences of the WHO2008 classification. Leukemia. 2010;24: Matutes E, Pickl WF, Van t Veer M, et al. Mixed-phenotype acute leukemia: clinical and laboratory features and outcome in 100 patients defined according to the WHO 2008 classification. Blood. 2011;117: Yan L, Ping N, Zhu M, et al. Clinical, immunophenotypic, cytogenetic, and molecular genetic features in 117 adult patients with mixed-phenotype acute leukemia defined by WHO-2008 classification. Haematologica. 2012;97: Al-Seraihy AS, Owaidah TM, Ayas M, et al. Clinical characteristics and outcome of children with biphenotypic acute leukemia. Haematologica. 2009;94: Weinberg OK, Seetharam M, Ren L, et al. Clinical characterization of acute myeloid leukemia with myelodysplasia-related changes as defined by the 2008 WHO classification system. Blood. 2009;113: Killick S, Matutes E, Powles RL, et al. Outcome of biphenotypic acute leukemia. Haematologica. 1999;84: Legrand O, Perrot JY, Simonin G, et al. Adult biphenotypic acute leukaemia: an entity with poor prognosis which is related to unfavourable cytogenetics and P-glycoprotein overexpression. Br J Haematol. 1998;100: Xu XQ, Wang JM, Lü SQ, et al. Clinical and biological characteristics of adult biphenotypic acute leukemia in comparison with that of acute myeloid leukemia and acute lymphoblastic leukemia: a case series of a Chinese population. Haematologica. 2009;94: Am J Clin Pathol 2014;142:
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