Diagnosis and management of extranodal NK/T cell lymphoma nasal type

Expert Review of Hematology

Volumn 9, Issue 9, 2016, Pages 861-871

  Tse, Eric ^a   Kwong, Yok Lam ^a  

^a QUEEN MARY HOSPITAL   (Hong Kong)

Author keywords

Epstein Barr virus; Extranodal NK T cell lymphoma; hematopoietic stem cell transplantation; L asparaginase; natural killer cell

Indexed keywords

ANTHRACYCLINE DERIVATIVE; ASPARAGINASE; BIOLOGICAL MARKER; CD3 ANTIGEN; CD56 ANTIGEN; GRANZYME B; VIRUS DNA;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; AUTOLOGOUS HEMATOPOIETIC STEM CELL TRANSPLANTATION; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER REGRESSION; CANCER SURVIVAL; CHEMORADIOTHERAPY; CLINICAL FEATURE; DISEASE SEVERITY; EPSTEIN BARR VIRUS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; LONG TERM SURVIVAL; MOLECULAR PATHOLOGY; NK T CELL LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; REVIEW; TREATMENT RESPONSE; CANCER STAGING; COMPLICATION; DISEASE MANAGEMENT; DRUG RESISTANCE; EPSTEIN BARR VIRUS INFECTION; GENETIC PREDISPOSITION; IMMUNOPHENOTYPING; LYMPHOMA, EXTRANODAL NK-T-CELL; METABOLISM; MORTALITY; MULTIMODAL IMAGING; MULTIMODALITY CANCER THERAPY; MUTATION; NATURAL KILLER CELL; PATHOLOGY; PHENOTYPE; PROGNOSIS; RECURRENT DISEASE; TREATMENT OUTCOME; VIROLOGY;

CHEMORADIOTHERAPY; COMBINED MODALITY THERAPY; DISEASE MANAGEMENT; DRUG RESISTANCE, NEOPLASM; EPSTEIN-BARR VIRUS INFECTIONS; GENETIC PREDISPOSITION TO DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOPHENOTYPING; KILLER CELLS, NATURAL; LYMPHOMA, EXTRANODAL NK-T-CELL; MULTIMODAL IMAGING; MUTATION; NEOPLASM STAGING; PHENOTYPE; PROGNOSIS; RECURRENCE; TREATMENT OUTCOME;

EID: 84983770623     PISSN: 17474086     EISSN: 17474094     Source Type: Journal    
DOI: 10.1080/17474086.2016.1206465     Document Type: Review

References (85)

1. J.C.Sun, L.L.Lanier NK cell development, homeostasis and function:parallels with CD8⁺ T cells. Nat Rev Immunol. 2011;11(10):645–657.• This article provides a detailed account of the development of NK cells that may be useful in the understanding of NK/T-cell lymphoma.
2. A.Cerwenka, L.L.Lanier. Natural killer cell memory in infection, inflammation and cancer. Nat Rev Immunol. 2016;16(2):112–123.
3. E.Montaldo, P.Vacca, L.Moretta, et al. Development of human natural killer cells and other innate lymphoid cells. Semin Immunol. 2014;26(2):107–113.
4. P.Parham. MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol. 2005;5(3):201–214.
5. C.S.Chim, G.C.Ooi, T.W.Shek, et al. Lethal midline granuloma revisited:nasal T/Natural-killer cell lymphoma. J Clin Oncol. 1999;17(4):1322–1325.
6. Y.L.Kwong. Natural killer-cell malignancies:diagnosis and treatment. Leukemia. 2005;19(12):2186–2194.
7. N.L.Harris, E.S.Jaffe, H.Stein, et al. A revised European-American classification of lymphoid neoplasms:a proposal from the international lymphoma study group. Blood. 1994;84(5):1361–1392.
8. J.K.Chan, W.Y.Tsang, C.S.Ng. Clarification of CD3 immunoreactivity in nasal T/natural killer cell lymphomas:the neoplastic cells are often CD3 epsilon+. Blood. 1996;87(2):839–841.
9. T.Pongpruttipan, S.Sukpanichnant, T.Assanasen, et al. Extranodal NK/T-cell lymphoma, nasal type, includes cases of natural killer cell and αβ, γδ, and αβ/γδ T-cell origin:a comprehensive clinicopathologic and phenotypic study. Am J Surg Pathol. 2012;36(4):481–499.
10. M.Hong, T.Lee, S.Young Kang, et al. Nasal-type NK/T-cell lymphomas are more frequently T rather than NK lineage based on T-cell receptor gene, RNA, and protein studies:lineage does not predict clinical behavior. Mod Pathol. 2016;29(5):430–443.
11. J.K.Chan, L.Quintanilla-Martinez, J.A.Ferry, et al. Extranodal NK/T-cell lymphoma, nasal type. In:S.H.Swerdlow, E.Campo, N.L.Harris, et al. editor. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon:International Agency for Research on Cancer; 2008. p. 285–288.
12. K.F.Wong, J.K.Chan, Y.L.Kwong. Identification of del(6)(q21q25) as a recurring chromosomal abnormality in putative NK cell lymphoma/leukaemia. Br J Haematol. 1997;98(4):922–926.
13. L.L.Siu, K.F.Wong, J.K.Chan, et al. Comparative genomic hybridization analysis of natural killer cell lymphoma/leukemia. Recognition of consistent patterns of genetic alterations. Am J Pathol. 1999;155(5):1419–1425.
14. L.L.Siu, V.Chan, J.K.Chan, et al. Consistent patterns of allelic loss in natural killer cell lymphoma. Am J Pathol. 2000;157(6):1803–1809.
15. C.Küçük, J.Iqbal, X.Hu, et al. PRDM1 is a tumor suppressor gene in natural killer cell malignancies. Proc Natl Acad Sci USA. 2011;108(50):20119–20124.
16. K.Karube, M.Nakagawa, S.Tsuzuki, et al. Identification of FOXO3 and PRDM1 as tumor-suppressor gene candidates in NK-cell neoplasms by genomic and functional analyses. Blood. 2011;118(12):3195–3204.
17. C.Küçük, X.Hu, J.Iqbal, et al. HACE1 is a tumor suppressor gene candidate in natural killer cell neoplasms. Am J Pathol. 2013;182(1):49–55.
18. Y.W.Chen, T.Guo, L.Shen, et al. Receptor-type tyrosine-protein phosphatase κ directly targets STAT3 activation for tumor suppression in nasal NK/T-cell lymphoma. Blood. 2015;125(10):1589–1600.
19. J.Iqbal, D.D.Weisenburger, A.Chowdhury, et al. International peripheral T-cell lymphoma project. Natural killer cell lymphoma shares strikingly similar molecular features with a group of non-hepatosplenic γδ T-cell lymphoma and is highly sensitive to a novel aurora kinase a inhibitor in vitro. Leukemia. 2011;25(2):348–358.
20. S.B.Ng, V.Selvarajan, G.Huang, et al. Activated oncogenic pathways and therapeutic targets in extranodal nasal-type NK/T cell lymphoma revealed by gene expression profiling. J Pathol. 2011;223(4):496–510.
21. G.C.Koo, S.Y.Tan, T.Tang, et al. Janus kinase 3-activating mutations identified in natural killer/T-cell lymphoma. Cancer Discov. 2012;2(7):591–597.
22. C.Küçük, B.Jiang, X.Hu, et al. Activating mutations of STAT5B and STAT3 in lymphomas derived from γδ-T or NK cells. Nat Commun. 2015;6:6025.
23. L.Jiang, Z.H.Gu, Z.X.Yan, et al. Exome sequencing identifies somatic mutations of DDX3X in natural killer/T-cell lymphoma. Nat Genet. 2015;47(9):1061–1066.• This article provides a useful account of the genetic mutations found in NK/T-cell lymphoma.
24. S.Lee, H.Y.Park, S.Y.Kang, et al. Genetic alterations of JAK/STAT cascade and histone modification in extranodal NK/T-cell lymphoma nasal type. Oncotarget. 2015;6(19):17764–17776.
25. L.L.Siu, J.K.Chan, K.F.Wong, et al. Specific patterns of gene methylation in natural killer cell lymphomas:p73 is consistently involved. Am J Pathol. 2002;160(1):59–66.
26. C.Küçük, X.Hu, B.Jiang, et al. Global promoter methylation analysis reveals novel candidate tumor suppressor genes in natural killer cell lymphoma. Clin Cancer Res. 2015;21(7):1699–1711.
27. Y.L.Kwong, P.L.Khong. Central palatal perforation in nasal natural killer cell lymphoma. Br J Haematol. 2011;152(1):2.
28. Y.L.Kwong, A.C.Chan, R.Liang, et al. CD56+ NK lymphomas:clinicopathological features and prognosis. Br J Haematol. 1997;97(4):821–829.
29. K.Takata, M.E.Hong, P.Sitthinamsuwan, et al. Primary cutaneous NK/T-cell lymphoma, nasal type and CD56-positive peripheral T-cell lymphoma:a cellular lineage and clinicopathologic study of 60 patients from Asia. Am J Surg Pathol. 2015;39(1):1–12.
30. C.S.Chim, W.Y.Au, T.W.Shek, et al. Primary CD56 positive lymphomas of the gastrointestinal tract. Cancer. 2001;91(3):525–533.
31. S.J.Kim, H.A.Jung, S.S.Chuang, et al.; Asia Lymphoma Study Group. Extranodal natural killer/T-cell lymphoma involving the gastrointestinal tract:analysis of clinical features and outcomes from the Asia Lymphoma Study Group. J Hematol Oncol. 2013;6:86.
32. W.Y.Au, A.C.Chan, Y.L.Kwong. Scrotal skin ulcer in a patient with a previous tonsillectomy because of natural killer cell lymphoma. Am J Dermatopathol. 1998;20(6):582–585.
33. C.S.Chim, W.Y.Au, C.Poon, et al. Primary natural killer cell lymphoma of skeletal muscle. Histopathology. 2002;41(4):371–374.
34. C.S.Chim, C.Choy, R.Liang, et al. Isolated uterine relapse of nasal T/Nk cell lymphoma. Leuk Lymphoma. 1999;34(5–6):629–632.
35. C.S.Chim, E.S.Ma, F.Loong, et al. Diagnostic cues for natural killer cell lymphoma:primary nodal presentation and the role of in situ hybridisation for Epstein-Barr virus encoded early small RNA in detecting occult bone marrow involvement. J Clin Pathol. 2005;58(4):443–445.
36. W.K.Chan, W.Y.Au, C.Y.Wong, et al. Metabolic activity measured by F-18 FDG PET in natural killer-cell lymphoma compared to aggressive B- and T-cell lymphomas. Clin Nucl Med. 2010;35(8):571–575.
37. E.Tse, R.Leung, P.L.Khong, et al. Non-nasal natural killer cell lymphoma:not non-nasal after all. Ann Hematol. 2009;88(2):185–187.
38. J.K.Chan, E.S.Jaffe, E.Ralfkiaer, et al. Aggresssive NK-cell leukaemia. In:S.H.Swerdlow, E.Campo, N.L.Harris, et al. editor. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon:International Agency for Research on Cancer; 2008. p. 276–277.
39. L.L.Siu, J.K.Chan, Y.L.Kwong. Natural killer cell malignancies:clinicopathologic and molecular features. Histol Histopathol. 2002;17(2):539–554.
40. E.Tse, Y.L.Kwong. Practical management of natural killer/T-cell lymphoma. Curr Opin Oncol. 2012;24(5):480–486.
41. G.C.Ooi, C.S.Chim, R.Liang, et al. Nasal T-cell/natural killer cell lymphoma:CT and MR imaging features of a new clinicopathologic entity. AJR Am J Roentgenol. 2000;174(4):1141–1145.
42. P.L.Khong, C.B.Pang, R.Liang, et al. Fluorine-18 fluorodeoxyglucose positron emission tomography in mature T-cell and natural killer cell malignancies. Ann Hematol. 2008;87(8):613–621.
43. W.Y.Au, A.Pang, C.Choy, et al. Quantification of circulating Epstein-Barr virus (EBV) DNA in the diagnosis and monitoring of natural killer cell and EBV-positive lymphomas in immunocompetent patients. Blood. 2004;104(1):243–249.•• The first article to demonstrate the role of EBV DNA quantification in the diagnosis, follow-up and prognostication of NK/T-cell lymphoma.
44. J.A.Kanakry, A.M.Hegde, C.M.Durand, et al. The clinical significance of EBV DNA in the plasma and peripheral blood mononuclear cells of patients with or without EBV diseases. Blood. 2016;127(16):2007–2017.• This article demonstrates that plasma is superior to whole blood for EBV DNA quantifications in pathological conditions.
45. F.Ishida, Y.L.Kwong. Diagnosis and management of natural killer-cell malignancies. Expert Rev Hematol. 2010;3(5):593–602.
46. E.Tse, Y.L.Kwong. How I treat NK/T-cell lymphomas. Blood. 2013;121(25):4997–5005.•• A very comprehensive review of the diagnosis, treatment and prognostication of NK/T-cell lymphoma.
47. Y.Yang, Y.Zhu, J.Z.Cao, et al. Risk-adapted therapy for early-stage extranodal nasal-type NK/T-cell lymphoma:analysis from a multicenter study. Blood. 2015;126(12):1424–1432.
48. E.Tse, Y.L.Kwong. Nasal NK/T-cell lymphoma:RT, CT, or both. Blood. 2015;126(12):1400–1401.
49. A.Jaccard, N.Gachard, B.Marin, et al.; GELA and GOELAMS intergroup. Efficacy of L-asparaginase with methotrexate and dexamethasone (AspaMetDex regimen) in patients with refractory or relapsing extranodal NK/T-cell lymphoma, a phase 2 study. Blood. 2011;117(6):1834–1839.
50. L.H.Dong, L.J.Zhang, W.J.Wang, et al. Sequential DICE combined with l-asparaginase chemotherapy followed by involved field radiation in newly diagnosed, stage IE to IIE, nasal and extranodal NK/T-cell lymphoma. Leuk Lymphoma. 2016;57(7):1600–1606.
51. L.Wang, Z.H.Wang, X.Q.Chen, et al. First-line combination of gemcitabine, oxaliplatin, and L-asparaginase (GELOX) followed by involved-field radiation therapy for patients with stage IE/IIE extranodal natural killer/T-cell lymphoma. Cancer. 2013;119(2):348–355.
52. L.Wang, Z.H.Wang, X.Q.Chen, et al. First-line combination of GELOX followed by radiation therapy for patients with stage IE/IIE ENKTL:an updated analysis with long-term follow-up. Oncol Lett. 2015;10(2):1036–1040.
53. M.Kim, T.M.Kim, K.H.Kim, et al. Ifosfamide, methotrexate, etoposide, and prednisolone (IMEP) plus L-asparaginase as a first-line therapy improves outcomes in stage III/IV NK/T cell-lymphoma, nasal type (NTCL). Ann Hematol. 2015;94(3):437–444.
54. M.Jiang, H.Zhang, Y.Jiang, et al. Phase 2 trial of “sandwich” L-asparaginase, vincristine, and prednisone chemotherapy with radiotherapy in newly diagnosed, stage IE to IIE, nasal type, extranodal natural killer/T-cell lymphoma. Cancer. 2012;118(13):3294–3301.
55. H.Ding, J.Chang, L.G.Liu, et al. High-dose methotrexate, etoposide, dexamethasone and pegaspargase (MEDA) combination chemotherapy is effective for advanced and relapsed/refractory extranodal natural killer/T cell lymphoma:a retrospective study. Int J Hematol. 2015;102(2):181–187.
56. Y.L.Kwong, W.S.Kim, S.T.Lim, et al. SMILE for natural killer/T-cell lymphoma:analysis of safety and efficacy from the Asia Lymphoma Study Group. Blood. 2012;120(15):2973–2980.•• The article that established the role of SMILE in the treatment of relapsed/refractory and high-risk NK/T-cell lymphoma.
57. M.Yamaguchi, Y.L.Kwong, W.S.Kim, et al. Phase II study of SMILE chemotherapy for newly diagnosed stage IV, relapsed, or refractory extranodal natural killer (NK)/T-cell lymphoma, nasal type:the NK-Cell Tumor Study Group study. J Clin Oncol. 2011;29(33):4410–4416.•• The original article that established the role of SMILE in relapsed/refractory NK/T-cell lymphoma.
58. S.J.Kim, D.H.Yang, J.S.Kim, et al. Concurrent chemoradiotherapy followed by L-asparaginase-containing chemotherapy, VIDL, for localized nasal extranodal NK/T cell lymphoma:CISL08-01 phase II study. Ann Hematol. 2014;93(11):1895–1901.
59. M.Yamaguchi, K.Tobinai, M.Oguchi, et al. Phase I/II study of concurrent chemoradiotherapy for localized nasal natural killer/T-cell lymphoma:Japan Clinical Oncology Group Study JCOG0211. J Clin Oncol. 2009;27(33):5594–5600.• One of the articles showing benefit of concomitant chemoradiotherapy.
60. M.Yamaguchi, K.Tobinai, M.Oguchi, et al. Concurrent chemoradiotherapy for localized nasal natural killer/T-cell lymphoma:an updated analysis of the Japan clinical oncology group study JCOG0211. J Clin Oncol. 2012;30(32):4044–4046.
61. S.J.Kim, K.Kim, B.S.Kim, et al. Phase II trial of concurrent radiation and weekly cisplatin followed by VIPD chemotherapy in newly diagnosed, stage IE to IIE, nasal, extranodal NK/T-cell lymphoma:consortium for improving survival of lymphoma study. J Clin Oncol. 2009;27(35):6027–6032.• One of the articles that established the use of concomitant chemoradiotherapy in NK/T-cell lymphoma.
62. W.S.Kim, S.Y.Song, Y.C.Ahn, et al. CHOP followed by involved field radiation:is it optimal for localized nasal natural killer/T-cell lymphoma? Ann Oncol. 2001;12(3):349–352.
63. W.Yong, W.Zheng, Y.Zhang, et al. L-asparaginase-based regimen in the treatment of refractory midline nasal/nasal-type T/NK-cell lymphoma. Int J Hematol. 2003;78(2):163–167.
64. M.Ando, K.Sugimoto, T.Kitoh, et al. Selective apoptosis of natural killer-cell tumours by l-asparaginase. Br J Haematol. 2005;130(6):860–868.
65. L.Zhang, M.Jiang, L.Xie, et al. Five-year analysis from phase 2 trial of “sandwich” chemoradiotherapy in newly diagnosed, stage IE to IIE, nasal type, extranodal natural killer/T-cell lymphoma. Cancer Med. 2016;5(1):33–40.
66. H.K.Ahn, S.J.Kim, D.W.Hwang, et al. Gemcitabine alone and/or containing chemotherapy is efficient in refractory or relapsed NK/T-cell lymphoma. Invest New Drugs. 2013;31(2):469–472.
67. C.S.Chim, S.Y.Ma, W.Y.Au, et al. Primary nasal natural killer cell lymphoma:long-term treatment outcome and relationship with the International Prognostic Index. Blood. 2004;103(1):216–221.
68. J.Lee, C.Suh, Y.H.Park, et al. Extranodal natural killer T-cell lymphoma, nasal-type:a prognostic model from a retrospective multicenter study. J Clin Oncol. 2006 Feb 1;24(4):612–618.
69. S.J.Kim, D.H.Yoon, A.Jaccard, et al. A prognostic index for natural killer cell lymphoma after non-anthracycline-based treatment:a multicentre, retrospective analysis. Lancet Oncol. 2016;17(3):389–400.•• A prognostic index devised for patients receiving non-anthracycline containing regimens.
70. Y.L.Kwong, A.W.Pang, A.Y.Leung, et al. Quantification of circulating Epstein-Barr virus DNA in NK/T-cell lymphoma treated with the SMILE protocol:diagnostic and prognostic significance. Leukemia. 2014;28(4):865–870.• An important article showing the relevance of interim PET/CT scan in NK/T-cell lymphoma patients.
71. 1⁸F-FDG PET/CT scan for early response assessment of SMILE therapy in natural Killer/T-cell lymphoma:a prospective study from a single center. J Nucl Med. 2014;55(6):911–916.• An important article on the role of interim PET/CT scan in NK/T-cell lymphomas.
72. S.J.Kim, J.Y.Choi, S.H.Hyun, et al.; Asia Lymphoma Study Group. Risk stratification on the basis of Deauville score on PET-CT and the presence of Epstein-Barr virus DNA after completion of primary treatment for extranodal natural killer/T-cell lymphoma, nasal type:a multicentre, retrospective analysis. Lancet Haematol. 2015;2(2):e66–74.
73. W.Y.Au, A.K.Lie, R.Liang, et al. Autologous stem cell transplantation for nasal NK/T-cell lymphoma:a progress report on its value. Ann Oncol. 2003;14(11):1673–1676.
74. J.Lee, W.Y.Au, M.J.Park, et al. Autologous hematopoietic stem cell transplantation in extranodal natural killer/T cell lymphoma:a multinational, multicenter, matched controlled study. Biol Blood Marrow Transplant. 2008;14(12):1356–1364.
75. H.Y.Yhim, J.S.Kim, Y.C.Mun, et al. Consortium for Improving Survival of Lymphoma Study. Clinical outcomes and prognostic factors of up-front autologous stem cell transplantation in patients with extranodal natural Killer/T Cell lymphoma. Biol Blood Marrow Transplant. 2015;21(9):1597–1604.
76. Y.L.Kwong. High-dose chemotherapy and hematopoietic SCT in the management of natural killer-cell malignancies. Bone Marrow Transplant. 2009;44(11):709–714.
77. Y.L.Kwong, B.O.Anderson, R.Advani, et al. Asian Oncology Summit. Management of T-cell and natural-killer-cell neoplasms in Asia:consensus statement from the Asian Oncology Summit 2009. Lancet Oncol. 2009;10(11):1093–1101.
78. N.Murashige, M.Kami, Y.Kishi, et al. Allogeneic haematopoietic stem cell transplantation as a promising treatment for natural killer-cell neoplasms. Br J Haematol. 2005;130(4):561–567.
79. D.Ennishi, Y.Maeda, N.Fujii, et al. Allogeneic hematopoietic stem cell transplantation for advanced extranodal natural killer/T-cell lymphoma, nasal type. Leuk Lymphoma. 2011;52(7):1255–1261.
80. E.Tse, T.S.Chan, L.P.Koh, et al. Allogeneic haematopoietic SCT for natural killer/T-cell lymphoma:a multicentre analysis from the Asia Lymphoma Study Group. Bone Marrow Transplant. 2014;49(7):902–906.
81. W.Y.Kim, S.J.Nam, S.Kim, et al. Prognostic implications of CD30 expression in extranodal natural killer/T-cell lymphoma according to treatment modalities. Leuk Lymphoma. 2015;56(6):1778–1786.
82. H.K.Kim, S.M.Moon, J.H.Moon, et al. Complete remission in CD30-positive refractory extranodal NK/T-cell lymphoma with brentuximab vedotin. Blood Res. 2015;50(40):254–256.
83. L.M.Poon, Y.L.Kwong. Complete remission of refractory disseminated NK/T cell lymphoma with brentuximab vedotin and bendamustine. Ann Hematol. 2016;95(5):847–849.
84. Y.Huang, A.de Reyniès, L.de Leval, et al. Gene expression profiling identifies emerging oncogenic pathways operating in extranodal NK/T-cell lymphoma, nasal type. Blood. 2010;115(6):1226–1237.
85. B.J.Chen, C.BC, J.Ouyang, et al. PD-L1 expression is characteristic of a subset of aggressive B-cell lymphomas and virus-associated malignancies. Clin Cancer Res. 2013;19(13):3462–3473.