BRIEF ARTICLES. KEY WORDS: Blastic plasmacytoid dendritic cell neoplasm, BPDCN, Allogeneic stem cell transplantation
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1 BRIEF ARTICLES Blastic Plasmacytoid Dendritic Cell Neoplasia (BPDC) in Elderly Patients: Results of a Treatment Algorithm Employing Allogeneic Stem Cell Transplantation with Moderately Reduced Conditioning Intensity Sascha Dietrich, 1 Mindaugas Andrulis, 2 Ute Hegenbart, 1 Thomas Schmitt, 1 Frauke Bellos, 1 Uwe M. Martens, 3 Julia Meissner, 1 Alwin Kr amer, 1 Anthony D. Ho, 1 Peter Dreger 1 Blastic plasmacytoid dendritic cell neoplasm (BPDC), formerly known as blastic NK cell lymphoma, is a rare hematopoietic malignancy preferentially involving skin, bone marrow, and lymph nodes. The overall prognosis of BPDC is dismal, with a median overall survival (OS) of only 12 to 14 months despite aggressive chemotherapy. Anecdotal reports suggest that younger patients might benefit from myeloablative therapy with autologous or allogeneic stem cell transplantation (allosct). However, with a median age at diagnosis beyond 60 years, BPDC primarily affects elderly patients. Here, we present for the first time evidence that also in elderly patients, allosct for BPDC is feasible and may result in sustained remission if conditioning with moderately reduced intensity is used. Between 2006 and 2009, 6 patients were treated at our institution who fulfilled the diagnostic criteria for BPDC. Median age was 67 (range: 55-80) years. All responded to acute leukemia-type induction therapy. Whereas 2 patients who were ineligible for allosctrapidly died of disease recurrence, 4 patients underwent allosct from unrelated donors as part of first-line (n 5 1) or salvage treatment (n 5 3). Two patients allografted in remission live disease free 57 and 16 months post-allosct, whereas 2 patients transplanted with active disease achieved complete remission but relapsed 6 and 18 months after transplantation, respectively. In conclusion, reduced-intensity conditioning (RIC) allosct from unrelated donors is feasible and seems to be effective in elderly patients with BPDC, suggesting that allosct should be pursued aggressively in patients with this otherwise fatal disease up to 70 years of age. Biol Blood Marrow Transplant 17: (2011) Ó 2011 American Society for Blood and Marrow Transplantation KEY WORDS: Blastic plasmacytoid dendritic cell neoplasm, BPDCN, Allogeneic stem cell transplantation INTRODUCTION From the 1 Department of Medicine V, University of Heidelberg, Heidelberg, Germany; 2 Institute of Pathology, University of Heidelberg, Heidelberg, Germany; and 3 Department of Medicine III, SLK-Kliniken, Heilbronn, Germany. Financial disclosure: See Acknowledgments on page Correspondence and reprint requests: Sascha Dietrich, MD, Medizinische Klinik V, Department of Heamatology, Im Neuenheimer Feld 410, Heidelberg, Germany ( sascha. dietrich@med.uni-heidelberg.de). Received November 13, 2010; accepted December 28, 2010 Ó 2011 American Society for Blood and Marrow Transplantation /$36.00 doi: /j.bbmt Blastic plasmacytoid dendritic cell neoplasm (BPDC) is a rare hematopoietic neoplasia preferentially involving the skin, the bone marrow, and lymph nodes. Although the typical CD4 1 /CD56 1 expression of this tumor resulted in provisional classification as blastic NK-cell lymphoma, immunophenotypic, molecular, and functional properties, such as CD123, TCL1 expression, and production of interferon-alpha (IFN-a), suggested pathogenetic relations to plasmacytoid dendritic cells, paving the way for the term Blastic plasmacytoid dendritic cell neoplasm, which now has been adopted by the 2008 WHO classification [1-3]. The putative normal counterpart of BPDC is the precursor of the plasmacytoid dendritic cells [3]. BPDC has a male/female ratio of 3:1 and primarily affects elderly patients (median age at diagnosis years) but has occurred in patients younger than 40 years in 20% to 30% of the cases [4,5]. Upto 90% of patients have skin lesions. Lymph node involvement is common (40%-50%), and low-level bone marrow and peripheral blood involvement are seen in most cases (60%-90%); however, initial fulminant leukemia is rare (5%-25%). Overt leukemia is a common feature of BPDC progression or relapse, often with a myelomonocytic phenotype, and is nearly always present in the terminal stage. The overall prognosis for patients with BPDC is dismal, with a median 1250
2 Biol Blood Marrow Transplant 17: , 2011 BPDC in Elderly Patients 1251 overall survival of 12 to 14 months, irrespective of the initial pattern of disease [4,5]. Most cases show an initial response to multiagent chemotherapy (80%- 90%), but relapses with subsequent drug resistance occur in the vast majority of patients after a median of only 9 to 11 months [5-7]. However, superior results have been reported anecdotally in younger patients who received stem cell transplantation (SCT). These very preliminary reports suggest that long-term disease control can be achieved by myeloablative treatment followed by autologous or allogeneic SCT (allosct) in selected young patients transplanted in first remission [5,7]. Here, we present for the first time evidence that also in elderly patients allosct is feasible and may result in sustained remission of BPDC if conditioning with moderately reduced intensity is used. This is also the first report showing that allosct in BPDC can be successful without the use of total-body irradiation (TBI), and that it can be safely performed with well-matched, partially matched, or mismatched unrelated donors. PATIENTS AND METHODS Identification of Patients The electronic patient file system of the institution was screened for all patients with BPDC treated between 2006 and 2009 using the terms blastic plasmacytoid dendritic cell neoplasm and blastic NK lymphoma. For verification of the diagnosis of BPDC, tissue sections or the written histology and immunophenotyping reports were reviewed by an experienced hematopathologist (M.A.), and the diagnostic algorithm suggested by Tsagarakis et al. [8] and Garnache-Ottou et al. [9] was applied. Coexpression of CD4, CD56, and CD123 in the absence of other lineage specific markers such as CD11c, MPO, lysozyme, CD79a, ccd3 was the minimum requirement for diagnosis. Treatment Policy Because of the paucity of published information and in the absence of a formal protocol for this orphan disease, no stringent treatment policy was in place. However, basically, the treatment algorithm employed was as follows: if not precluded by comorbidity or very advanced age, patients received an acute leukemia-like induction regimen consisting of daunorubicin and cytarabine (Ara-C) followed by high-dose Ara-C consolidation or equivalent (AML-like; 3 patients), or containing dexamethasone, methotrexate, vincristine, cyclophosphamide, adriamycin/daunorubicin, cyclophosphamide/ifosfamide (ALL-like; 3 patients). Once relapse occurred, patients received individual salvage therapy followed by reduced-intensity conditioning (RIC) allosct in responding patients younger than 70 years with a comorbidity score (HCT-CI) of equal or less than 2 [10]. From 2009 onward, it was intended to perform consolidating RIC allosct as part of first-line therapy. Patients were treated according to protocols approved by the responsible institutional review board and gave written informed consent to each individual treatment. allosct Conditioning was selected according to the comorbidity of the individual patient. Because the disease was considered as blastic NK cell lymphoma until 2008, however, attempts were made to treat the patients on a protocol that was in place for allosct of poor-risk aggressive lymphoma at our institution (DSHNHL 2003 R3, BfArM Nr ). This protocol used submyeloablative doses of busulfan with fludarabine and cyclophosphamide, followed by transplantation of unmanipulated peripheral blood stem cell grafts obtained from siblings or unrelated donors [11]. If age or comorbidity precluded the use of this regimen, fludarabine-treosulfan was used instead [12]. Patients with an unrelated donor received anti-thymocyte globuline (ATG). Unrelated donors were selected according to the results of high-resolution HLA genotyping for HLA-A, -B, -C, -DRB1, and -DQB1) [13]. Unrelated donor matching was classified as wellmatched, partially matched, or mismatched according to the proposal by Weisdorf et al. [14]. Posttransplant immunosuppression was performed with cyclosporine and methotrexate or mycophenolate mofetil and tacrolimus. Supportive care was applied according to local standard operating procedures. RESULTS Patient Characteristics at Diagnosis Nine patients who matched the search criteria could be identified from our databases. According to the diagnostic algorithm suggested by Garnache- Ottou et al. [9] and Tsagarakis et al. [8], the diagnosis of BPDC had to be rejected in 2 patients because of a moderate lysozyme expression in their blasts, despite a strong coexpression of CD4, CD56, CD123, and a typical clinical presentation with multiple skin lesions during the first diagnosis. For another patient, CD123, BDCA-2, or BDCA-4 staining has not been available and was therefore not considered to have proven BPDC. Characteristics of the remaining 6 patients in whom the diagnosis of BPDC could be confirmed are shown in Table 1. Median age at diagnosis was 67 (range: 55-80) years. At initial presentation, all patients had multiple skin lesions, 4 patients had bone marrow involvement, and only 1 patient had BPDC-specific blasts detectable in the peripheral
3 1252 S. Dietrich et al. Biol Blood Marrow Transplant 17: , 2011 Table 1. Patient Characteristics and First-Line Treatment Initial Staging F/u since First-Line CT (Months) COD Time to Relapse from Initial Treatment (Months) Relapse Therapy First-Line Treatment Response Skin PB BM LN Diagnostic Tissue Sex/Age at Dx Patient Number 1 Male/63 Skin ALL-like CT CR 18 HD-MTX (8 g/qm) allosct 82+ alive and well 2 Male/66 Skin, BM ALL-like CT CR 11 HD-MTX (8 g/qm), dexa-gemcitabine, 23 dead Disease progression bendamustine (120 mg/qm) allosct 3 Female/72 Skin AML-like CT CR 7 Radiation mitoxantrone (8 mg/qm) 13 dead Disease progression etoposide 50 mg p.o. 4 Male/80 BM CHOP14 CR 5 Best supportive care 6 dead Disease progression 5 Male/69 BM AML-like CT PR 3 AlloSCT 25+ alive after relapse post- allosct CR No relapse 19+ alive and well 6 Female/55 BM ALL-like CT + allosct PB indicates peripheral blood; BM, bone marrow; LN, lymph nodes; Dx, diagnosis; CT, chemotherapy; CHOP, cyclophosphamide, vincristine, doxorubicin, prednisone; NOVE, mithoxantrone, etoposide; ALL, acute lymphoblastic leukemia; AML, acute myeloid leukemia; allosct, allogeneic stem cell transplantation; agvhd, acute graft-versus-host disease; CR, complete response; PR, partial response. blood. Four patients had lymph node enlargement, which was biopsied in 2 patients, confirming the diagnosis of BPDC. First-Line Treatment All patients responded very well to the induction chemotherapy (complete remission [CR]: n 5 5/6, partial remission [PR]: n 5 1/6). However, 5 out of 6 patients relapsed after a median of 7 months (range: 3-11 months) after start of induction treatment. The only patient (#6) who did not experience disease recurrence underwent allosct in first CR and maintained the CR ever since (19 months) (Table 1). Relapse Treatment and allosct Because of advanced age and comorbidity, 2 patients (#3 and #4) were ineligible for further treatment intensification and therefore did not undergo allosct. Both of them died very rapidly because of disease progression. The 3 remaining patients who experienced relapse after frontline treatment proceeded to allosct (Table 2): patient #1 responded to high-dose methotrexate (8 g/m 2 ) given as salvage treatment and was subsequently allografted from a mismatched unrelated donor. He is enjoying ongoing CR for more than 57 months after allosct. Patient #2 did not respond to a variety of salvage attempts and underwent allosct with refractory disease. He achieved a CR directly after allosct but relapsed 6 months thereafter and subsequently died of progressive disease. Patient #5 showed skin relapse 3 months after induction treatment and proceeded without any salvage attempt to the planned allosct, which resulted in a prompt CR. After a very uneventful course, he experienced rapid proliferation of blood and marrow BPDC blasts 18 months posttransplant. DISCUSSION BPDC is an aggressive hematopoietic neoplasm with a very poor prognosis. So far, only little is known on how to achieve durable responses in BPDC. Reimer et al. [5] reviewed the literature on treatment of BPDC in 2003 and found 91 cases, virtually all published as individual case reports. Whereas in 66 patients, initial treatment consisted of local therapy or CHOP-like therapy only (CR rate 55%-70%), 17 received acute-leukemia like induction treatment (CR rate 94%). The remaining 10 patients had been treated in first or subsequent CR with myeloablative therapy followed by allosct in 6 patients and by autologous stem cell transplantation (autosct) in 4 patients. Whereas only 1 of the 4 autosct patients enjoyed long-term remission, 3 out of 4 patients who received allografts in first CR remained alive and disease free 98 (76-115) months
4 Biol Blood Marrow Transplant 17: , 2011 BPDC in Elderly Patients 1253 Table 2. Details of AlloSCT Sex/Age at allosct Status at allosct Conditioning Donor GVHD Prophylaxis agvhd cgvhd Survival after allosct (Months) Patient Number MMUD (8/10 - HLA-A and -B allele mm) MMF, tacrolimus None Extensive 57+ alive & in CR 1 Male/64 CR2 Fludarabine (125 mg/qm) Busulfan (12 mg/kg orally) None +8 dead b/o disease progression (relapse 6 months after allosct, no response to Gem-Dex) PMUD (9/10 - A allele mm) MMF, tacrolimus Steroid-sensitive gut GVHD grade II 2 Male/67 PR4 Fludarabine (100 mg/qm) Busulfan (4.8 mg/kg i.v.) WMUD (9/10 - DQB1 allele mm) CSA, MTX None None 20+ alive with refractory relapse 18 months after allosct Treosulfan (3 g/qm) Fludarabin (150 mg/qm) ATG 30 mg/kg 5 Male/70 Untreated relapse (cutaneous lesions) WMUD (9/10 - DQB1 allele mm) MMF, tacrolimus None Limited 16+ alive & in CR 6 Female/56 CR1 Fludarabine (125 mg/qm) Busulfan (9.6 mg/kg i.v.) CR indicates complete remission; PR, partial remission; MUD, matched unrelated donor; MMUD, mismatched unrelated donor; PMUD, partially matched unrelated donor; MMUD, mismatched unrelated donor; ATG, anti-thymocyte globulin; CSA, cyclosporine; MTX, methotrexate; MMF, mycopheolate; NOVE, mithoxantrone, etoposide; Gem-Dex, gemcitabine, dexamethasone; cgvhd, chronic graft-versus-host disease; agvhd, acute graft-versus-host disease. posttransplant. It has to be stressed that the median age of these 4 patients was only 26 (6-29) years. In contrast, median overall survival (OS) was only 9 to 13 months in the other 3 groups without allosct consolidation. Age emerged as significant prognostic factor (OS 18 months for patients \60 years versus 9 months for patients.60 years; P \.0001). Taking into account the limitations inferred by the heterogeneity and the retrospective nature of this compilation, these results suggested that a proportion of younger patients might be cured with high-dose therapy followed by allosct or autosct performed in first complete remission. A registry analysis from the French Cutaneous Lymphoma database described 47 patients with BPDC [7]. Thirty-seven were treated with radiation, monochemotherapy, or polychemotherapy only, whereas 10 received an additional autosct (n 5 1) or allosct (n 5 9). The median age of the allografted patients was 38 years. In the absence of any further information on donor source, conditioning, and other essential transplant-related variables, OS of the transplanted patients was 40 months and thus significantly better than that of the 37 nontransplanted patients who had a median survival of 1 year [7]. Similarly, a case collection by Bekkenk et al. [4] found superior outcome of 8 patients who underwent autologous or allogeneic SCT compared to 53 other patients who were treated without transplantation. Here, we report our experience in 6 patients with BPDC treated since 2006 at our department. In line with published data [5], we show that initial response to acute leukemia-type chemotherapy treatment is good, but relapse occurred very rapidly after a median of only 7 months if allosct was not performed in first remission. The high relapse rate despite good responses underlines the need for more effective consolidation strategies. Given the success anecdotally seen with myeloablative allosct in young patients, we decided to offer our patients, who were all elderly, allosct with dose-reduced conditioning. We show here for the first time that RIC allosct may offer curative potential also in elderly patients. This is of particular importance because the majority of patients affected by BPDC is beyond 60 years of age [4,5]. Although the conditioning regimens used for patients with BPDC in our institution were not myeloablative by the traditional criteria, they were still rather intense, which on the one hand may favor the conditioning regimen to be responsible for disease control after allosct. The fact that the 2 patients with active or refractory disease achieved CR immediately after transplantation is in keeping with this hypothesis. On the other hand, the only long-term remission of BPDC observed to date with RIC is our patient #1, who received a transplant from a mismatched
5 1254 S. Dietrich et al. Biol Blood Marrow Transplant 17: , 2011 unrelated donor and was the only 1 in our series who suffered from clinically significant chronic graftversus-host disease (cgvhd). This points to the existence of a graft versus leukemia effect (GVL) being potentially effective in BPDC. However, the 2 patients who were transplanted in remission and did not experience disease recurrence also received the most intensive conditioning (Table 2). Further studies with larger patient numbers are necessary for valid conclusions on this issue. Taken together, our data suggests that allosct from matched or mismatched unrelated donors using fludarabine-busulfan-cyclophosphamide or fludarabine-treosulfan conditioning is feasible in elderly patients with BPDC, can induce responses in relapsed and refractory disease, and can provide long-term disease control at least in patients who undergo allosct in remission. It remains to be settled if the activity of the allosct regimens used here relies predominantly on the cytotoxicity of conditioning, or if there is a substantial contribution of GVL effects. Although the numbers are small and the follow-up is short, the quality of responses and the remission duration achieved by the allosct approach used here appear to be markedly superior to that of nontransplantation strategies, suggesting that allosct should be pursued aggressively in patients with BPDC up to 70 years of age, preferentially within prospective clinical studies. In conclusion, it seems that broad implementation of allosct into the treatment algorithm could help to improve the otherwise fatal prognosis of BPDC even in elderly patients representing the typical target population of the disease. Given the fact that relapse after first-line therapy is inevitable and taking into account the difficulties of achieving a second response, allosct might be considered in eligible patients already in first remission. ACKNOWLEDGMENTS Financial disclosures: The authors have nothing to disclose. REFERENCES 1. Herling M, Jones D. CD41/CD561 hematodermic tumor: the features of an evolving entity and its relationship to dendritic cells. Am J Clin Pathol. 2007;127: Herling M, Teitell MA, Shen RR, Medeiros LJ, Jones D. TCL1 expression in plasmacytoid dendritic cells (DC2s) and the related CD41 CD561 blastic tumors of skin. Blood. 2003;101: Swerdlow SH, Campo E, Harris NL, et al. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues, 4th ed. Lyon, France: IARC; Bekkenk MW, Jansen PM, Meijer CJ, Willemze R. CD561 hematological neoplasms presenting in the skin: a retrospective analysis of 23 new cases and 130 cases from the literature. Ann Oncol. 2004;15: Reimer P, Rudiger T, Kraemer D, et al. What is CD41CD561 malignancy and how should it be treated? Bone Marrow Transplant. 2003;32: Assaf C, Gellrich S, Whittaker S, et al. CD56-positive haematological neoplasms of the skin: a multicentre study of the Cutaneous Lymphoma Project Group of the European Organisation for Research and Treatment of Cancer. J Clin Pathol. 2007;60: Dalle S, Beylot-Barry M, Bagot M, et al. Blastic plasmacytoid dendritic cell neoplasm: is transplantation the treatment of choice? Br J Dermatol. 162: Tsagarakis NJ, Kentrou NA, Papadimitriou KA, et al. Acute lymphoplasmacytoid dendritic cell (DC2) leukemia: results from the Hellenic Dendritic Cell Leukemia Study Group. Leuk Res. 34: Garnache-Ottou F, Feuillard J, Ferrand C, et al. Extended diagnostic criteria for plasmacytoid dendritic cell leukaemia. Br J Haematol. 2009;145: Sorror ML, Maris MB, Storb R, et al. Hematopoietic cell transplantation (HCT)-specific comorbidity index: a new tool for risk assessment before allogeneic HCT. Blood. 2005;106: Glass B, Nickelsen M, Dreger P, et al. Reduced-intensity conditioning prior to allogeneic transplantation of hematopoietic stem cells: the need for T cells early after transplantation to induce a graft-versus-lymphoma effect. Bone Marrow Transplant. 2004;34: Casper J, Wolff D, Knauf W, et al. Allogeneic hematopoietic stem-cell transplantation in patients with hematologic malignancies after dose-escalated treosulfan/fludarabine conditioning. J Clin Oncol. 28: Schmitt T, Luft T, Hegenbart U, Tran TH, Ho AD, Dreger P. Pentostatin for treatment of steroid-refractory acute GVHD: a retrospective single-center analysis. Bone Marrow Transplant Jun 21. [Epub ahead of print.] 14. Weisdorf D, Spellman S, Haagenson M, et al. Classification of HLA-matching for retrospective analysis of unrelated donor transplantation: revised definitions to predict survival. Biol Blood Marrow Transplant. 2008;14:
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