CASE REPORT. Abstract. Introduction. Case Reports

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1 CASE REPORT Two Elderly Patients with Philadelphia Chromosome Positive Mixed Phenotype Acute Leukemia Who Were Successfully Treated with Dasatinib and Prednisolone Hiroyuki Takata 1, Taichi Ikebe 1, Hitohiro Sasaki 1, Yasuhiko Miyazaki 1, Eiichi Ohtsuka 1, Yoshio Saburi 1, Masao Ogata 2 and Kuniaki Shirao 2 Abstract Philadelphia chromosome positive (Ph+) mixed phenotype acute leukemia (MPAL) is a rare type of acute leukemia having both myeloid and lymphoid features for which no optimal treatment has yet been established. We herein describe two elderly Ph+MPAL patients who achieved molecular remission without any serious adverse events by treatment with dasatinib and prednisolone. Although dasatinib induction therapy combined with prednisolone is known to be a highly effective treatment for Ph+ acute lymphoblastic leukemia, its efficacy for Ph+MPAL has not been shown. The clinical courses of the present cases suggest that combination therapy with dasatinib and prednisolone is a safe and effective therapeutic modality in elderly Ph+ MPAL patients. Key words: mixed phenotype acute leukemia, Philadelphia chromosome, dasatinib, prednisolone () () Introduction Mixed phenotype acute leukemia (MPAL) is a clinical entity defined in the 2008 World Health Organization (WHO) Classification of Tumours of Haematopoietic and Lymphoid Tissues (1). Leukemic cells of MPAL have features of both myeloid and lymphoid lineage, and MPAL comprises 0.5-3% of all acute leukemias (2-5). In the 2008 WHO criteria, MPAL was classified into five subtypes, and Philadelphia chromosome positive (Ph+) MPAL accounts for 20-40% of MPAL (2, 3, 6). Although the prognosis of Ph+MPAL is poor, there is no consensus on the optimal treatment for Ph+ MPAL (7-9). We herein report two elderly patients with Ph+MPAL who were successfully treated with dasatinib and prednisolone. Case 1 Case Reports A 69-year-old woman was admitted to our hospital for glycemic control and pneumonia. Although she had been treated for type 2 diabetes for the past 15 years, no hematological abnormalities were observed during that period. Physical examination revealed severe anemia without splenomegaly or lymphadenopathy. Laboratory findings included the following values: white blood cell (WBC) count of 3,300/μL (blasts 44%), hemoglobin (Hb) level of 5.9 g/ dl, and platelet (PLT) count of /μl. The lactate dehydrogenase (LDH) level was normal (213 U/L). Bone marrow aspiration resulted in a dry tap, and the touch preparation showed a dimorphic cellular population containing 87.6% blasts. Myeloperoxidase (MPO) staining was negative by cytochemistry (Fig. 1). Flow cytometry (FCM) revealed a positive expression for CD10, CD19, CD34 and human leu- Department of Hematology, Oita Prefectural Hospital, Japan and Department of Medical Oncology and Hematology, Oita University Faculty of Medicine, Japan Received for publication February 24, 2015; Accepted for publication August 6, 2015 Correspondence to Dr. Hiroyuki Takata, takata@oita-u.ac.jp 1177

2 Figure 1. Blast cells in bone marrow. Blasts within a dimorphic population are shown. Myeloperoxidase stain is negative. (A, C) May Giemsa stain, 1,000. (B, D) Myeloperoxidase stain, 1,000. Figure 2. Flow cytometry reveals a positive expression of CD10, CD19, CD34, HLA-DR, cy CD79a, cy CD22, and MPO. cy: cytoplasmic, MPO: myeloperoxidase kocyte antigen (HLA)-DR. Additionally, an examination of cytoplasmic markers showed positivity for cytoplasmic CD79a, cytoplasmic CD22, and MPO (Fig. 2). The major bcr-abl mrna level in the peripheral blood was 41,000 copies/μgrna. A G-banding analysis of the peripheral blood revealed a 46, XX karyotype. She did not have splenomegaly, peripheral leukocytosis, absolute basophilia, or history of chronic myeloid leukemia. Consequently, Ph+ MPAL was diagnosed, according to the 2008 WHO classification. Because the patient was elderly with diabetes and also had pneumonia at admission, cytotoxic chemotherapy administration was judged to present too great a risk of precipitating serious infectious disease. She was therefore treated with dasatinib 140 mg/day and prednisolone 60 mg/ day (1 mg/kg/day), and received no cytotoxic agents. Hematological complete remission (CR) was achieved 22 days after the start of therapy. She was discharged on day 27. Major bcr-abl fusion transcripts in the peripheral blood had disappeared based on the findings of real-time quantitative polymerase chain reaction (RQ-PCR) 32 days after the start of therapy. The patient was maintained on dasatinib (140 mg/ day) and prednisolone was tapered to 5 mg/day (Fig. 3). During the 16 months of follow-up, molecular CR has been maintained without any serious adverse events. Case 2 A 69-year-old woman presented with a chief complaint of 1178

3 Figure 3. Clinical course of the current patients. CR: complete remission general fatigue. She had undergone mastectomy, systemic chemotherapy and hormonal therapy due to breast cancer 17 years prior to admission. Physical examination revealed mild anemia without splenomegaly or lymphadenopathy. Laboratory findings included the following values: WBC count of 16,000/μL (blasts 68%), Hb level of 11.3 g/dl, and PLT count of /μl. The level of LDH was elevated to 503 IU/L. A bone marrow examination revealed a dimorphic cellular population containing 99% blasts. MPO was negative by cytochemistry (Fig. 1). FCM revealed a positive expression of CD10, CD19, CD34 and HLA-DR. Additionally, positive cytoplasmic markers included cytoplasmic CD79a, cytoplasmic CD22, and MPO (Fig. 2). She was treated with prednisolone 90 mg/day (1.5 mg/kg/day); blasts in the peripheral blood promptly disappeared and LDH fell to within normal limits 7 days after the start of prednisolone. The presence of minor bcr-abl (420,000 copies/μgrna) of the bone marrow was confirmed, and Ph+MPAL was diagnosed according to the 2008 WHO classification. A G-banding analysis of the bone marrow cells revealed 46, XX, t(9;22) (q34;q11.2)[14]/46,idem,-17,+mal[3]/46, XX[3]. She was treated with dasatinib 140 mg/day in addition to prednisolone, which was tapered to 5 mg/day. She was discharged 22 days after the start of dasatinib. Minor bcr-abl fusion transcripts in the bone marrow were found to have disappeared according to RQ-PCR 28 days after the start of dasatinib. She has been maintained on dasatinib (140 mg/ day) and prednisolone (5 mg/day) (Fig. 3). During the 7 months of follow-up, molecular CR has been maintained without any hematologic adverse events, pleural effusion, or hemorrhage. Discussion The prognosis of MPAL is reportedly poorer than that for acute myeloid leukemia or acute lymphoblastic leukemia (ALL) (7-10). Philadelphia chromosome positivity is also related to a poor prognosis (2, 3). Killick et al. (7) reported the 2-year overall survival (OS) rate in patients with Ph+ MPAL to only be 14%. However, the addition of tyrosine kinase inhibitor (TKI) to the induction chemotherapy regimen dramatically improved the outcome of Ph+MPAL. Wang et al. (11) reported that Ph+MPAL patients treated with intensive chemotherapy combined with the first generation TKI imatinib had a superior OS compared to those treated with chemotherapy alone (1-year OS: 43% vs. 0%, respectively). Shimizu et al. (12) reported that Ph+MPAL patients treated with imatinib-containing chemotherapy achieved a 5-year OS rate of 54%, and that there was no significant difference compared to the OS rate of treated Ph+ALL patients. Their findings suggest that combination therapy with imatinib and cytotoxic chemotherapy is effec- 1179

4 tive for Ph+MPAL. Dasatinib is a second generation TKI and a multi-targeted kinase inhibitor of bcr-abl with a two-log increased potency relative to imatinib (13). Dasatinib has demonstrated notable clinical efficacy in patients with Ph+ALL who were resistant or intolerant to imatinib (14, 15). A Grupo Italiano Malattie Ematologiche maligne dell adulto (GIMEMA) study revealed that all 53 evaluable Ph+ALL patients who received dasatinib induction therapy combined with prednisolone achieved hematologic CR without any deaths or relapses. The number of patients who achieved molecular CR was 10 of 44 (22.7%) at 22 days after the start of dasatinib, and a significant difference in the disease-free survival was observed between the patients who achieved molecular CR at day 22 compared with the patients who never reached these levels during induction (16). Little is known, however, about the effect of second generation TKI for patients with Ph+ MPAL. To our knowledge, there is only one previously described patient with Ph+MPAL where the patient achieved a third CR with combination therapy consisting of dasatinib, vincristine, and prednisolone (17). In our cases, patients with Ph+MPAL achieved molecular CR at day 32 (Case 1) and day 28 (Case 2) with dasatinib and prednisolone. The clinical courses of the present cases suggest that induction therapy with dasatinib combined with prednisolone without chemotherapy is safe and highly effective for Ph+MPAL patients. The optimal postinduction treatment protocol remains to be elucidated. The GIMEMA study (16) showed that postinduction treatment in relapsing patients frequently comprised only dasatinib (14 of 23 patients), whereas 5 of 23 patients had received dasatinib plus chemotherapy and/or autografting, and in 2 of 18 allografted patients. Therefore, postinduction dasatinib plus chemotherapy and/or stem cell transplantation is likely to reduce relapse for Ph+ALL. However, dasatinib with cytotoxic chemotherapy has been associated with notable toxicities and treatment discontinuation (18). Although allogeneic stem cell transplantation for Ph+MPAL has been recommended in some reports (2, 11), the optimal treatment strategy for elderly patients has not yet been established. Both of the current patients were elderly and had a very good response to dasatinib and prednisolone therapy, so we did not choose postinduction chemotherapy and/or allogeneic stem cell transplantation. Both patients were discharged after short hospitalization periods and maintained a good quality of life in molecular CR without serious adverse events. However, the profile and incidence of adverse events of dasatinib at a dose of 140 mg/day for elderly patients is not generally understood and therefore requires further systematic study in clinical trials. The clinical courses of the present cases suggest that dasatinib combined with prednisolone therapy is safe and effective for the treatment of Ph+MPAL in elderly patients. Further clinical studies will be needed in the future to establish the optimal treatment regimen for Ph+MPAL. The authors state that they have no Conflict of Interest (COI). References 1. Borowitz MJ, Bene MC, Harris NL, et al. WHO classification of tumours of haematopoietic and lymphoid tissues. IARC Press, Lyon, France, 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 117: , Weinberg OK, Arber DA. Mixed-phenotype acute leukemia: historical overview and a new definition. Leukemia 24: , 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 97: , van den Ancker W, Terwijn M, Westers TM, et al. Acute leukemias of ambiguous lineage: diagnostic consequences of the WHO 2008 classification. Leukemia 24: , Bhatia P, Binota J, Varma N, et al. A study on the expression of BCR-ABL transcript in mixed phenotype acute leukemia (MPAL) cases using the reverse transcriptase polymerase reaction assay (RT-PCR) and its correlation with hematological remission status post initial induction therapy. Mediterr J Hematol Infect Dis 4: e , Killick S, Matutes E, Powles RL, et al. Outcome of biphenotypic acute leukemia. Haematologica 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 over-expression. Br J Haematol 100: , Weir EG, Ali Ansari-Lari M, Batista DA, et al. Acute bilineal leukemia: a rare disease with poor outcome. Leukemia 21: , Heesch S, Neumann M, Schwartz S, et al. Acute leukemias of ambiguous lineage in adults: molecular and clinical characterization. Ann Hematol 92: , Wang Y, Gu M, Mi Y, Qiu L, Bian S, Wang J. Clinical characteristics and outcomes of mixed phenotype acute leukemia with Philadelphia chromosome positive and/or bcr-abl positive in adult. Int J Hematol 94: , Shimizu H, Yokohama A, Hatsumi N, et al. Philadelphia chromosome-positive mixed phenotype acute leukemia in the imatinib era. Eur J Haematol 93: , ShahNP,TranC,LeeFY,ChenP,NorrisD,SawyersCL.Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 305: , Talpaz M, Shah NP, Kantarjian H, et al. Dasatinib in imatinibresistant Philadelphia chromosome-positive leukemias. N Engl J Med 354: , Ottmann O, Dombret H, Martinelli G, et al. Dasatinib induces rapid hematologic and cytogenetic responses in adult patients with Philadelphia chromosome positive acute lymphoblastic leukemia with resistance or intolerance to imatinib: interim results of a phase 2 study. Blood 110: , Foà R, Vitale A, Vignetti M, et al; GIMEMA Acute Leukemia Working Party. Dasatinib as first-line treatment for adult patients with Philadelphia chromosome-positive acute lymphoblastic leukemia. Blood 118: , Kawajiri C, Tanaka H, Hashimoto S, et al. Successful treatment of Philadelphia chromosome-positive mixed phenotype acute leukemia by appropriate alternation of second-generation tyrosine kinase inhibitors according to BCR-ABL1 mutation status. Int J 1180

5 Hematol 99: , Ravandi F, O Brien S, Thomas D, et al. First report of phase 2 study of dasatinib with hyper-cvad for the frontline treatment of patients with Philadelphia chromosome-positive (Ph+) acute lymphoblastic leukemia. Blood 116: , The Japanese Society of Internal Medicine

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