NK-Cell Lymphoblastic Leukemia/Lymphoma (Literature Review and Authors’ Experience)

NK-T-CELL MALIGNANCIES ,

MA Frenkel’, OYu Baranova, AS Antipova, NA Kupryshina, NN Tupitsyn

N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478

For correspondence: Alina Sergeevna Antipova, 24 Kashirskoye sh., Moscow, Russian Federation, 115478; Tel.: +7(499)324-28-54; e-mail: a.s.antipova@gmail.com

For citation: Frenkel’ MA, Baranova OYu, Antipova AS, et al. NK-Cell Lymphoblastic Leukemia/Lymphoma (Literature Review and Authors’ Experience). Clinical oncohematology. 2016;9(2):208–17 (In Russ).

DOI: 10.21320/2500-2139-2016-9-2-208-217

ABSTRACT

Aim. To investigate clinical and laboratory features of NK-cell lymphoblastic leukemia/lymphoma (NK-LL).

Methods. Of 161 patients treated in the Department of Chemotherapy of Hemoblastoses of the N.N. Blokhin Russian Cancer Research Center from 2000 to 2014, NK-LL was diagnosed in 1 patient (0.6 %). In the Laboratory of Hematopoietic Immunology of the N.N. Blokhin Russian Cancer Research Center, NK-LL was diagnosed in 3 more patients referred from other healthcare institutions over the same period of time. The disease was diagnosed in accordance with the 2008 WHO criteria. Therefore, the NK-LL group consisted of 4 patients (3 men and 1 woman) aged 29, 40, 59, and 82.

Results. All patients had total bone marrow blast metaplasia (> 70 %) and extramedullary lesions in the form of generalized lymphadenopathy, hepatosplenomegaly, lesions of skin, tonsils, mediastinum, and CNS in the form of neuroleukemia. Cytochemical response in blast cells to myeloperoxidase, lipids, and nonspecific esterase was negative. In all patients, expression of CD56 antigen (69.8–99.1 %) and T-associated CD7 antigen (66.2–92.0 %) were found on blast cells. There was no expression of myeloid, T- and B-lymphoid antigens. In one patient, the PCR demonstrated no T-cell receptor gene chain rearrangement. The cytogenetic study was not performed in any patient. Induction therapy of NK-LL patients was carried out mainly according to treatment regimens for acute lymphoblastic leukemia. The complete remission (1 and 7 months) was achieved in 2 patients. The longest remission (20 months) was obtained using a combined regime RACOP for the treatment of a relapse. The life span after the diagnosis (beginning from the date on the initiation of therapy) was 1, 5, 17, and 29 months.

Conclusion. The analysis demonstrates low efficacy of current regimens for treatment of NK-LL. The treatment success seems to depend on timely and accurate diagnosis of this complex, aggressive malignant tumor, as well as on development of new therapeutic approaches.

Keywords: NK-cell lymphoblastic leukemia/lymphoma, blastic plasmacytoid dendritic cell neoplasm.

Received: December 27, 2015

Accepted: January 2, 2016

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REFERENCES

  1. Lanier LL, Le AM, Civin CI, et al. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol. 1986;136:4480–6.
  2. Nagler A, Lanier L, Cwirla S, et al. Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol. 1989;143:3183–91.
  3. 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. 4th edition. Lyon: IARC Press; 2008. pp. 150–5.
  4. Chan JKC, Jaffe ES, Ralfkiaer E. Blastic NK-cell lymphoma. In: Jaffe ES, Harris NL, Stein H, Vardiman JW. World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. Lyon: IARC Press; 2001. pp. 106–7.
  5. Sanchez MJ, Muench MO, Roncarolo MG, et al. Identification of a common T/natural killer cell progenitor in human fetal thymus. J Exp Med. 1994;180(2):569–76. doi: 10.1084/jem.180.2.569.
  6. Oshimi K. Progress in understanding and managing natural killer-cell malignancies. Br J Haematol. 2007;139(4):532–44. doi: 10.1111/j.1365-2141.2007.06835.x.
  7. Grzywacz B, Kataria Nan, Kataria Nik, et al. Natural killer-cell differentiation by myeloid progenitors. Blood. 2011;117(13):3548–58. doi: 10.1182/blood-2010-04-281394.
  8. Suzuki R, Nakamura S, Suzumiya J, et al. Blastic natural killer cell lymphoma/leukemia (CD56-positive blastic tumor). 2005;104(5):1022–31. doi: 10.1002/cncr.21268.
  9. Bekkenk MW, Jansen PM, Meijer CJ, et al. CD56+ hematological neoplasms presenting in the skin: a retrospective analysis of 23 new cases and 130 cases from the literature. Ann Oncol. 2004;15(7):1097–108. doi: 10.1093/annonc/mdh268.
  10. Massone C, Chott A, Metze D, et al. Subcutaneous, blastic natural killer (NK), NK/T-cell, and other cytotoxic lymphomas of the skin: a morphologic, immunophenotypic, and molecular study of 50 patients. Am J Surg Pathol. 2004;28(6):719–35. doi: 10.1097/01.pas.0000126719.71954.4f.
  11. Santucci M, Pimpinelli N, Massi D, et al. Cytotoxic/natural killer cell cutaneous lymphomas. Report of EORTC Cutaneous Lymphoma Task Force Workshop. Cancer. 2003;97(3):610–27. doi: 10.1002/cncr.11107.
  12. Facchetti F, Jones DM, Petrella T. Blastic plasmacytoid dendritic cell neoplasm. In: Swerdlow SH, Campo E, Harris NL, et al, eds. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. 4th edition. Lyon: IARC Press; 2008. pp. 145–7.
  13. Dubois SG, Etzell JE, Matthay KK, et al. Pediatric acute blastic natural killer cell leukemia. Leuk Lymphoma. 2002;43(4):901–6. doi: 10.1080/10428190290017088.
  14. Hyakuna N, Toguchi S, Higa T, et al. Childhood blastic NK cell leukemia successfully treated with L-asparaginase and allogeneic bone marrow transplantation. Pediatr Blood Cancer. 2004;42(7):631–4. doi: 10.1002/pbc.20034.
  15. Liang X, Greffe B, Garrington T, Graham DK. Precursor natural killer cell leukemia. Pediatr. Blood Cancer. 2008;50(4):876–8. doi: 10.1002/pbc.21189.
  16. Matano S, Nakamura S, Nakamura S, et al. Monomorphic agranular natural killer cell lymphoma/leukemia with no Epstein-Barr virus association. Acta Haematol. 1999;101(4):206–8. doi: 10.1159/000040955.
  17. Tamura H, Ogata K, Mori S, et al. Lymphoblastic lymphoma of natural killer cell origin, presenting as pancreatic tumour. 1998;32(6):508–11. doi: 10.1046/j.1365-2559.1998.00417.x.
  18. Guan XQ, Xu L, Ke ZY, et al. Five Chinese pediatric patients with leukemias possibly arising from immature natural killer cells: clinical features and courses. Pediatr Hematol Oncol. 2011;28(3):187–93. doi: 10.3109/08880018.2010.535117.
  19. Zheng YY, Chen G, Zhou XG, et al. Retrospective analysis of 4 cases of the so-called blastic NK-cell lymphoma, with reference to the 2008 WHO classification of tumors of haematopoietic and lymphoid tissues. Zhonghua Bing Li Xue Za Zhi. 2010;39(9):600–5.
  20. Lin CW, Liu TY, Chen SU, et al. CD94 1A transcripts characterize lymphoblastic lymphoma/leukemia of immature natural killer cell origin with distinct clinical features. 2005;106(10):3567–74. doi: 10.1182/blood-2005-02-0519.
  21. Kawano S, Tatsumi E, Yoneda N, et al. Novel leukemic lymphoma with probable derivation from immature stage of natural killer (NK) lineage in an aged patient. Hematol Oncol. 1995;13(1):1–11. doi: 10.1002/hon.2900130102.
  22. Koita H, Suzumiya J, Ohshima K, et al. Lymphoblastic lymphoma expressing natural killer cell phenotype with involvement of the mediastinum and nasal cavity. J Surg Pathol. 1997;21(2):242–8. doi: 10.1097/00000478-199702000-00016.
  23. Wong N, Wong KF, Chan JK, et al. Chromosomal translocations are common in natural killer-cell lymphoma/leukemia as shown by spectral karyotyping. Hum Pathol. 2000;31(6):771–4. doi: 10.1053/hupa.2000.7625.
  24. Liang X, Graham DK. Natural Killer Cell Neoplasms. Cancer. 2008;112(7):1425–36. doi: 10.1002/cncr.23316.
  25. Marquez C, Trigueros C, Franco JM, et al. Identification of a common developmental pathway for thymic natural killer cells and dendritic cells. Blood. 1998;91(8):2760–71.
  26. Blasius AL, Barchet W, Cella M, Colonna M. Development and function of murine B220+CD11c+NK1.1+ cells identify them as a subset of NK cells. J Exp Med. 2007;204(11):2561–8. doi: 10.1084/jem.20070991.
  27. Vosshenrich CA, Lesjean-Pottier S, Hasan M, et al. CD11cloB220+ interferon-producing killer dendritic cells are activated natural killer cells. J Exp Med. 2007;204(11):2569–78. doi: 10.1084/jem.20071451.
  28. Hanna J, Gonen-Gross T, Fitchett J, et al. Novel APC-like properties of human NK cells directly regulate T cell activation. J Clin Invest. 2004;114(11):1612–23. doi: 10.1172/jci22787.
  29. Spits H, Lanier LL. Natural killer or dendritic: what’s in a name? 2007;26(1):11–6. doi: 10.1016/j.immuni.2007.01.004.
  30. Lim D, Goodman H, Rademaker M, et al. Blastic plasmacytoid dendritic cell neoplasm. Australas J Dermatol. 2013;54(2):43–5. doi: 10.1111/j.1440-0960.2011.00848.x.
  31. Prochaska L, Dakhil C, Mathur S. Blastic Plasmacytoid Dendritic Cell Neoplasm: A Rapidly Progressive and Fatal Disease without Aggressive Intervention. Clin Med Insights Case Rep. 2013;18(6):201–4. doi: 10.4137/CCRep.S12608.
  32. Nguyen CM, Stuart L, Skupsky H, et al. Blastic plasmacytoid dendritic cell neoplasm in the pediatric population: a case series and review of the literature. Am J Dermatopathol. 2015;37(12):924–8. doi: 10.1097/DAD.0000000000000348.
  33. Dharmani PA, Mittal NM, Subramanian PG, et al. Blastic plasmacytoid dendritic cell neoplasm: report of two pediatric cases. Indian J Pathol Microbiol. 2015;58(1):72–6. doi: 10.4103/0377-4929.151193.
  34. Sugimoto KJ, Shimada A, Wakabayashi M, et al. CD56-positive adult T-cell leukemia/lymphoma: a case report and a review of the literature. Med Mol Morphol. 2015;48(1):54–9. doi: 10.1007/s00795-014-0072-1.
  35. Voelkl A, Flaig M, Roehnisch T, et al. Blastic plasmacytoid dendritic cell neoplasm with acute myeloid leukemia successfully treated to a remission currently of 26 months duration. Leuk Res. 2011;35(6):61–3. doi: 10.1016/j.leukres.2010.11.019.
  36. Shi Y, Wang E. Blastic Plasmacytoid Dendritic Cell Neoplasm: A Clinicopathologic Arch Pathol Lab Med. 2014;138(4):564–9. doi: 10.5858/arpa.2013-0101-rs.
  37. Takiuchi Y, Maruoka H, Aoki K, et al. Leukemic manifestation of blastic plasmacytoid dendritic cell neoplasm lacking skin lesion: a borderline case between acute monocytic leukemia. J Clin Exp Hematopathol. 2012;52(2):107–11. doi: 10.3960/jslrt.52.107.
  38. Chang HJ, Lee MD, Yi HG, et al. A case of blastic plasmacytoid dendritic cell neoplasm initially mimicking cutaneous lupus erythematosus. Cancer Res Treat. 2010;42(4):239–43. doi: 10.4143/crt.2010.42.4.239.
  39. Cui XB, Jin J, Pang XL, et al. A case of blastic plasmacytoid dendritic cell neoplasm with ecchymotic lesions on the whole body. Int J Clin Exp Pathol. 2014;7(7):4391–9.
  40. Feng Z, Zhou J, Bentley G. Blastic plasmacytoid dendritic cell neoplasm: report of a case presenting with lung and central nervous system involvement and review of the literature. J La State Med Soc. 2014;166(1):2–9.
  41. Dunlap QA, Day KE, Borak SG. Pathology quiz case: plasmacytoid dendritic cell neoplasm. Allergy Rhinol. (Providence) 2014;5(1):50–2. doi: 10.2500/ar.2014.5.0085.
  42. Rauh MJ, Rahman F, Good D, et al. Blastic plasmacytoid dendritic cell neoplasm with leukemic presentation, lacking cutaneous involvement: case series and literature review. Leuk Res. 2012;36(1):81–6. doi: 10.1016/j.leukres.2011.07.033.
  43. Shinae Yu., Min-Jung K, Kyungeun K, et al. A rare case of acute leukemic presentation of blastic plasmacytoid dendritic cell neoplasm without cutaneous lesions. Ann Lab Med. 2014;34(2):148–51. doi: 10.3343/alm.2014.34.2.148.
  44. Hwang K, Park CJ, Jang S, et al. Immunohistochemical analysis of CD123, CD56 and CD4 for the diagnosis of minimal bone marrow involvement by blastic plasmacytoid dendritic cell neoplasm. 2013;62(5):764–70. doi: 10.1111/his.12079.
  45. Dijkman R, van Doorn R, Szuhai K, et al. Gene expression profiling and array-based CGH classify CD4+CD56+ hematodermic neoplasm and cutaneous myelomonocytic leukemia as distinct disease entities. Blood. 2007;109(4):1720–7. doi: 10.1182/blood-2006-04-018143.
  46. Toya T, Nishimoto N, Koya J, et al. The first case of blastic plasmacytoid dendritic cell neoplasm with MLL-ENL rearrangement. Leuk Res. 2012;36(1):117–8. doi: 10.1016/j.leukres.2011.07.029.
  47. Riaz W, Zhang L, Horna P, et al. Blastic plasmacytoid dendritic cell neoplasm: update on molecular biology, diagnosis, and therapy. Cancer Control. 2014;21(4):279–89.
  48. Kharfan-Dabaja MA, Lazarus HM, Nishihori T, et al. Diagnostic and therapeutic advances in blastic plasmacytoid dendritic cell neoplasm: a focus on hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2013;19(7):1006–12. doi: 10.1016/j.bbmt.2013.01.027.
  49. Paluri R, Nabell L, Borak S, et al. Unique presentation of blastic plasmacytoid dendritic cell neoplasm: a single-center experience and literature review. Hematol Oncol. 2014;33(4):206– doi: 10.1002/hon.2147.
  50. Atalay F, Demirci GT, Bayramgurler D, et al. Blastic plasmacytoid dendritic cell neoplasm: skin and bone marrow infiltration of three cases and the review of the literature. Indian J Hematol Blood Transfus. 2015;31(2):302–6. doi: 10.1007/s12288-014-0464-3.
  51. Pagano L, Valentini CG, Pulsoni A et al. Blastic plasmacytoid dendritic cell neoplasm with leukemic presentation: an Italian multicenter study. 2013;98(2):239–46. doi: 10.3324/haematol.2012.072645.
  52. Lokare A, Nikolousis E, Phillips N, et al. Reduced intensity allogeneic stem cell transplant for treatment of blastic plasmacytoid dendritic cell neoplasm. Hematol Rep. 2014;6(1):5119. doi: 10.4081/hr.2014.5119.
  53. Dietrich S, Andrulis M, Hegenbart U, et al. Blastic plasmacytoid dendritic cell neoplasia (BPDC) in elderly patients: results of a treatment algorithm employing allogeneic stem cell transplantation with moderately reduced conditioning intensity. Biol Blood Marrow Transplant. 2011;17(8):1250–4. doi: 10.1016/j.bbmt.2010.12.706.
  54. Petrella T, Comeau MR, Maynadie M, et al. ‘Agranular CD4+ CD56+ hematodermic neoplasm’ (blastic NK-cell lymphoma) originates from a population of CD56+ precursor cells related to plasmacytoid monocytes. Am J Surg Pathol. 2002;26(7):852–62. doi: 10.1097/00000478-200207000-00003.
  55. Petrella T, Bagot M, Willemze R, et al. Blastic NK-cell lymphomas (agranular CD4+CD56+ hematodermic neoplasms). Am J Clin Pathol. 2005;123(5):662–75. doi: 10.1309/gjwnpd8hu5maj837.