Cutaneous nonmycotic T- and natural killer/T-cell lymphomas: Diagnostic challenges and dilemmas

Journal of the American Academy of Dermatology

Volumn 70, Issue 4, 2014, Pages 724-735

  Chuang, Shih Sung ^a,b,c   Ko, Young Hyeh ^d  

^a CHI MEI MEDICAL CENTER   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

cutaneous T cell lymphoma; extranodal natural killer T cell lymphoma, nasal type; hydroa vacciniforme like lymphoma; peripheral T cell lymphoma; subcutaneous panniculitis like T cell lymphoma

Indexed keywords

CD30 ANTIGEN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN;

ARTICLE; CANCER CLASSIFICATION; CANCER DIAGNOSIS; CANCER GROWTH; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLASSIFICATION ALGORITHM; CLINICAL FEATURE; CUTANEOUS T CELL LYMPHOMA; DIFFERENTIAL DIAGNOSIS; EPSTEIN BARR VIRUS; HUMAN; HUMAN T CELL LEUKEMIA VIRUS; HYDROA VACCINIFORME; HYDROA VACCINIFORME LIKE LYMPHOMA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LARGE CELL LYMPHOMA; LYMPHOMA CELL; LYMPHOMATOID PAPULOSIS; LYMPHOPROLIFERATIVE DISEASE; MYCOSIS FUNGOIDES; NK T CELL LYMPHOMA; PERIPHERAL T CELL LYMPHOMA; PRIORITY JOURNAL; RARE DISEASE; SUBCUTANEOUS T CELL LYMPHOMA; T CELL LEUKEMIA; T CELL LYMPHOMA;

CD30(+) LYMPHOPROLIFERATIVE DISORDER; CUTANEOUS T-CELL LYMPHOMA; EXTRANODAL NATURAL KILLER/T-CELL LYMPHOMA, NASAL TYPE; HYDROA VACCINIFORME-LIKE LYMPHOMA; PERIPHERAL T-CELL LYMPHOMA; SUBCUTANEOUS PANNICULITIS-LIKE T-CELL LYMPHOMA;

ASIAN CONTINENTAL ANCESTRY GROUP; BIOPSY, NEEDLE; DIAGNOSIS, DIFFERENTIAL; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KILLER CELLS, NATURAL; LYMPHOMA, T-CELL, CUTANEOUS; MALE; MYCOSIS FUNGOIDES; PANNICULITIS; RARE DISEASES; RISK ASSESSMENT; SKIN NEOPLASMS;

EID: 84896077348     PISSN: 01909622     EISSN: 10976787     Source Type: Journal    
DOI: 10.1016/j.jaad.2013.11.047     Document Type: Review

References (78)

1. Willemze R, Jaffe ES, Burg G, Cerroni L, Berti E, Swerdlow SH, et al. WHO-EORTC classification for cutaneous lymphomas. Blood 2005;105:3768-85. (Pubitemid 40656118)
2. Nagasawa T, Miwa H, Nakatsuka S, Itami S, Yoshikawa K, Aozasa K. Characteristics of cutaneous lymphomas in Osaka, Japan (1988-1999) based on the European Organization for Research and Treatment of Cancer classification. Am J Dermatopathol 2000;22:510-4. (Pubitemid 32054844)
3. Su IJ, Wu YC, Chen YC, Hsieh HC, Cheng AL, Wang CH, et al. Cutaneous manifestations of postthymic T cell malignancies: description of five clinicopathologic subtypes. J Am Acad Dermatol 1990;23:653-62. (Pubitemid 20336391)
4. Lee MW. Characteristics of cutaneous lymphomas in Korea. Clin Exp Dermatol 2003;28:639-46.
5. Liao JB, Chuang SS, Chen HC, Tseng HH, Wang JS, Hsieh PP. Clinicopathologic analysis of cutaneous lymphoma in Taiwan: a high frequency of extranodal NK/T-cell lymphoma, nasal type, with an extremely poor prognosis. Arch Pathol Lab Med 2010;134:996-1002.
6. Yasukawa K, Kato N, Kodama K, Hamasaka A, Hata H. The spectrum of cutaneous lymphomas in Japan: a study of 62 cases based on the World Health Organization classification. J Cutan Pathol 2006;33:487-91. (Pubitemid 44049885)
7. Burg G, Kempf W, Cozzio A, Feit J, Willemze R, Jaffe ES, et al. WHO/EORTC classification of cutaneous lymphomas 2005: histological and molecular aspects. J Cutan Pathol 2005;32:647-74. (Pubitemid 41719746)
8. Burg G, Jaffe ES, Kempf W, Berti E, Cerroni L, Chimenti S, et al. Hematolymphoid tumors. In: Leboit PE BG, Weedon D, Sarasin A, editors. World Health Organization classification of tumors pathology and genetics skin tumors. Lyon: IARC Press; 2006. pp. 165-228.
9. Grogg KL, Jung S, Erickson LA, McClure RF, Dogan A. Primary cutaneous CD4-positive small/medium-sized pleomorphic T-cell lymphoma: a clonal T-cell lymphoproliferative disorder with indolent behavior. Mod Pathol 2008;21:708-15. (Pubitemid 351744836)
10. Rodriguez Pinilla SM, Roncador G, Rodriguez-Peralto JL, Mollejo M, Garcia JF, Montes-Moreno S, et al. Primary cutaneous CD41 small/medium-sized pleomorphic T-cell lymphoma expresses follicular T-cell markers. Am J Surg Pathol 2009;33:81-90.
11. Willemze R, Jansen PM, Cerroni L, Berti E, Santucci M, Assaf C, et al. Subcutaneous panniculitis-like T-cell lymphoma: definition, classification, and prognostic factors; an EORTC cutaneous lymphoma group study of 83 cases. Blood 2008;111:838-45.
12. Yang SF, Chang WY, Lan CC, Isaacson PG, Chuang SS. Composite primary cutaneous peripheral T-cell lymphoma and Epstein-Barr virus-positive large B-cell lymphoma. Leuk Lymphoma 2011;52:2027-30.
13. Dy JA, Chen SW, Chang CH, Chang ST, Kuo SY, Ye H, et al. Composite lymphoma after chemotherapy with regressed diffuse large B-cell lymphoma and transformed cytotoxic T-cell lymphoma. Leuk Lymphoma 2013;54:1101-4.
14. Ho JW, Ho FC, Chan AC, Liang RH, Srivastava G. Frequent detection of Epstein-Barr viruseinfected B cells in peripheral T-cell lymphomas. J Pathol 1998;185:79-85. (Pubitemid 28266720)
15. Murphy M, Fullen D, Carlson JA. Low CD7 expression in benign and malignant cutaneous lymphocytic infiltrates: experience with an antibody reactive with paraffin-embedded tissue. Am J Dermatopathol 2002;24:6-16. (Pubitemid 34121780)
16. Duncan LM, Kumar S. Chapter 40; Primary cutaneous T-cell lymphomas: rare subtypes. In: Jaffe ES, Harris NL, Vardiman JW, et al, editors. Hematopathology. St Louis: Saunders; 2011. pp. 617-28.
17. Gill HS, Lau WH, Chan AC, Leung RY, Khong PL, Leung AY, et al. CD20 expression in natural killer T cell lymphoma. Histopathology 2010;57:157-9.
18. + T-cell lymphoma: clinicopathologic analysis of 9 cases and a review of the literature. Am J Surg Pathol 2008;32:1593-607.
19. Hsieh YC, Chang ST, Huang WT, Ichinohasama R, Chuang SS. Adult T-cell leukemia/lymphoma comprising non-floral leukemic cells in Taiwan, a country non-endemic for human T-cell leukemia virus type I. Leuk Lymphoma 2009;50:1540-2.
20. Lin TH,WuHC, Hsieh YC, Tseng CE, Ichinohasama R, Chuang SS. CD4 and CD8 double-negative adult T-cell leukemia/ lymphoma with monomorphic cells expressing CD99: a diagnostic challenge in a country non-endemic for human T-cell leukemia virus. Pathol Int 2013;63:132-7.
21. Garcia-Herrera A, Song JY, Chuang SS, Villamor N, Colomo L, Pittaluga S, et al. Nonhepatosplenic gammadelta T-cell lymphomas represent a spectrum of aggressive cytotoxic T-cell lymphomas with a mainly extranodal presentation. Am J Surg Pathol 2011;35:1214-25.
22. Rodriguez-Pinilla SM, Ortiz-Romero PL, Monsalvez V, Tomas IE, Almagro M, Sevilla A, et al. TCR-gamma expression in primary cutaneous T-cell lymphomas. Am J Surg Pathol 2013;37:375-84.
23. Chuang SS. Cutaneous non-MF T-cell and NK-cell lymphoproliferative disorders. In: Murphy MJ, editor. Molecular diagnostics in dermatology and dermatopathology. New York: Humana Press; 2011. pp. 233-45.
24. Bekkenk MW, Geelen FA, van Voorst Vader PC, Heule F, Geerts ML, van Vloten WA, et al. Primary and secondary cutaneous CD30(1) lymphoproliferative disorders: a report from the Dutch cutaneous lymphoma group on the long-term follow-up data of 219 patients and guidelines for diagnosis and treatment. Blood 2000;95:3653-61. (Pubitemid 30412833)
25. Ralfkiaer E, Willemze R, Pauli M, Kadin ME. Primary cutaneous CD30-positive lymphoproliferative disorders. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al, editors. WHO classification of tumors of hematopoietic and lymphoid tissues. Lyon: IARC; 2008. pp. 300-1.
26. Kadin ME. Chapter 39; Primary cutaneous CD30-positive T-cell lymphoproliferative disorders. In: Jaffe ES, Harris NL, Vardiman JW, Campo E, Arber DA, editors. Hematopathology. St Louis: Saunders; 2011. pp. 604-16.
27. Willemze R, Beljaards RC. Spectrum of primary cutaneous CD30 (Ki-1)-positive lymphoproliferative disorders: a proposal for classification and guidelines for management and treatment. J Am Acad Dermatol 1993;28:973-80. (Pubitemid 23160651)
28. + cutaneous lymphoproliferative disorders: the Stanford experience in lymphomatoid papulosis and primary cutaneous anaplastic large cell lymphoma. J Am Acad Dermatol 2003;49:1049-58.
29. Flann S, Orchard GE, Wain EM, Russell-Jones R. Three cases of lymphomatoid papulosis with a CD561 immunophenotype. J Am Acad Dermatol 2006;55:903-6. (Pubitemid 44556843)
30. Kim DS, Choi YJ, Oh SH, Lee MG. A case of indolent CD56- positive lymphomatoid papulosis. J Am Acad Dermatol 2010; 63:e114-6.
31. Saggini A, Gulia A, Argenyi Z, Fink-Puches R, Lissia A, Magana M, et al. A variant of lymphomatoid papulosis simulating primary cutaneous aggressive epidermotropic CD81 cytotoxic T-cell lymphoma: description of 9 cases. Am J Surg Pathol 2010;34:1168-75.
32. Kempf W, Kazakov DV, Scharer L, Rutten A, Mentzel T, Paredes BE, et al. Angioinvasive lymphomatoid papulosis: a new variant simulating aggressive lymphomas. Am J Surg Pathol 2013;37:1-13.
33. Bertolotti A, Pham-Ledard AL, Vergier B, Parrens M, Bedane C, Beylot-Barry M. Lymphomatoid papulosis type D: an aggressive histology for an indolent disease. Br J Dermatol 2013;169:1157-9.
34. Karai LJ, Kadin ME, Hsi ED, Sluzevich JC, Ketterling RP, Knudson RA, et al. Chromosomal rearrangements of 6p25.3 define a new subtype of lymphomatoid papulosis. Am J Surg Pathol 2013;37:1173-81.
35. Kempf W. CD301 lymphoproliferative disorders: histopathology, differential diagnosis, new variants, and simulators. J Cutan Pathol 2006;33(Suppl):58-70.
36. Tokura Y, Sugita K, Yagi H, Shimauchi T, Kabashima K, Takigawa M. Primary cutaneous anaplastic large cell lymphoma with fatal leukemic outcome in association with CLA and CCR4-negative conversion. J Am Acad Dermatol 2007;57(Suppl):S92-6. (Pubitemid 47552643)
37. Oschlies I, Lisfeld J, Lamant L, Nakazawa A, d'Amore ES, Hansson U, et al. ALK-positive anaplastic large cell lymphoma limited to the skin: clinical, histopathological and molecular analysis of 6 pediatric cases; a report from the ALCL99 study. Haematologica 2013;98:50-6.
38. Sciallis AP, Law ME, Inwards DJ, McClure RF, Macon WR, Kurtin PJ, et al. Mucosal CD30-positive T-cell lymphoproliferations of the head and neck show a clinicopathologic spectrum similar to cutaneous CD30-positive T-cell lymphoproliferative disorders. Mod Pathol 2012;25:983-92.
39. Jaffe ES, Gaulard P, Ralfkiaer E, Cerroni L, Meijer CJLM. Subcutaneous panniculitis-like T-cell lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al, editors. WHO classification of tumors of hematopoietic and lymphoid tissues. Lyon: IARC; 2008. pp. 294-5.
40. Kong YY, Dai B, Kong JC, Zhou XY, Lu HF, Shen L, et al. Subcutaneous panniculitis-like T-cell lymphoma: a clinicopathologic, immunophenotypic, and molecular study of 22 Asian cases according to WHO-EORTC classification. Am J Surg Pathol 2008;32:1495-502.
41. Ng PP, Tan SH, Tan T. Lupus erythematosus panniculitis: a clinicopathologic study. Int J Dermatol 2002;41:488-90. (Pubitemid 35021487)
42. Massone C, Kodama K, Salmhofer W, Abe R, Shimizu H, Parodi A, et al. Lupus erythematosus panniculitis (lupus profundus): clinical, histopathological, and molecular analysis of nine cases. J Cutan Pathol 2005;32:396-404. (Pubitemid 40853001)
43. Massone C, Lozzi GP, Egberts F, Fink-Puches R, Cota C, Kerl H, et al. The protean spectrum of non-Hodgkin lymphomas with prominent involvement of subcutaneous fat. J Cutan Pathol 2006;33:418-25. (Pubitemid 43865300)
44. Farkas L, Beiske K, Lund-Johansen F, Brandtzaeg P, Jahnsen FL. Plasmacytoid dendritic cells (natural interferon-alpha/betaproducing cells) accumulate in cutaneous lupus erythematosus lesions. Am J Pathol 2001;159:237-43. (Pubitemid 33704208)
45. Liau JY, Chuang SS, Chu CY, Ku WH, Tsai JH, Shih TF. The presence of clusters of plasmacytoid dendritic cells is a helpful feature for differentiating lupus panniculitis from subcutaneous panniculitis-like T-cell lymphoma. Histopathology 2013;62:1057-66.
46. Pincus LB, LeBoit PE,McCalmont TH, Ricci R, BuzioC, Fox LP, et al. Subcutaneous panniculitis-like T-cell lymphoma with overlapping clinicopathologic features of lupus erythematosus: coexistence of 2 entities? Am J Dermatopathol 2009;31:520-6.
47. Kempf W, Kazakov DV, Kutzner H. Lobular panniculitis due to Borrelia burgdorferi infection mimicking subcutaneous panniculitis-like T-cell lymphoma. Am J Dermatopathol 2013;35:e30-3.
48. Chan JKC, Quintanilla-Martinez L, Ferry JA, Peh S-C. Extranodal NK/T-cell lymphoma, nasal type. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al, editors. WHO classification of tumors of hematopoietic and lymphoid tissues. Lyon: IARC; 2008. pp. 285-8.
49. Pongpruttipan T, Sukpanichnant S, Assanasen T, Wannakrairot P, Boonsakan P, Kanoksil W, et al. Extranodal NK/T-cell lymphoma, nasal type, includes cases of natural killer cell and alphabeta, gammadelta, and alphabeta/gammadelta T-cell origin: a comprehensive clinicopathologic and phenotypic study. Am J Surg Pathol 2012;36:481-99.
50. Choi YL, Park JH, Namkung JH, Lee JH, Yang JM, Lee ES, et al. Extranodal NK/T-cell lymphoma with cutaneous involvement: "nasal" vs "nasal-type" subgroupsea retrospective study of 18 patients. Br J Dermatol 2009;160:333-7.
51. Ahn HK, Suh C, Chuang SS, Suzumiya J, Ko YH, Kim SJ, et al. Extranodal natural killer/T-cell lymphoma from skin or soft tissue: suggestion of treatment from multinational retrospective analysis. Ann Oncol 2012;23:2703-7.
52. Barrionuevo C, Anderson VM, Zevallos-Giampietri E, Zaharia M, Misad O, Bravo F, et al. Hydroa-like cutaneous T-cell lymphoma: a clinicopathologic and molecular genetic study of 16 pediatric cases from Peru. Appl Immunohistochem Mol Morphol 2002;10:7-14. (Pubitemid 34178270)
53. Quintanilla-Marinez L, Kimura H, Jaffe ES. EBV-positive T-cell lymphoproliferative disorders of childhood. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al, editors. WHO classification of tumors of hematopoietic and lymphoid tissues. Lyon: IARC; 2008. pp. 278-80.
54. Kimura H, Ito Y, Kawabe S, Gotoh K, Takahashi Y, Kojima S, et al. EBV-associated T/NK-cell lymphoproliferative diseases in nonimmunocompromised hosts: prospective analysis of 108 cases. Blood 2012;119:673-86.
55. Sangueza M, Plaza JA. Hydroa vacciniforme-like cutaneous T-cell lymphoma: clinicopathologic and immunohistochemical study of 12 cases. J Am Acad Dermatol 2013;69:112-9.
56. Nicot C. Current views in HTLV-I-associated adult T-cell leukemia/lymphoma. Am J Hematol 2005;78:232-9. (Pubitemid 40316504)
57. Ohshima K, Jaffe ES, Kikuchi M. Adult T-cell leukemia/lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al, editors. WHO classification of tumors of hematopoietic and lymphoid tissues. Lyon: IARC; 2008. pp. 281-4.
58. Shimoyama M. Diagnostic criteria and classification of clinical subtypes of adult T-cell leukemia-lymphoma: a report from the lymphoma study group (1984-87). Br J Haematol 1991;79:428-37.
59. Toro JR, Beaty M, Sorbara L, Turner ML, White J, Kingma DW, et al. Gamma delta T-cell lymphoma of the skin: a clinical, microscopic, and molecular study. Arch Dermatol 2000;136:1024-32. (Pubitemid 30629130)
60. Gaulard P, Berti E, Willemze R, Jaffe ES. Primary cutaneous peripheral T-cell lymphoma, rare subtypes. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al, editors. WHO classification of tumors of hematopoietic and lymphoid tissues. Lyon: IARC; 2008. pp. 302-5.
61. Jaffe ES, Nicolae A, Pittaluga S. Peripheral T-cell and NK-cell lymphomas in the WHO classification: pearls and pitfalls. Mod Pathol 2013;26(Suppl):S71- 87.
62. Toro JR, Liewehr DJ, Pabby N, Sorbara L, Raffeld M, Steinberg SM, et al. Gamma-delta T-cell phenotype is associated with significantly decreased survival in cutaneous T-cell lymphoma. Blood 2003;101:3407-12. (Pubitemid 36857921)
63. Endly DC, Weenig RH, Peters MS, Viswanatha DS, Comfere NI. Indolent course of cutaneous gamma-delta T-cell lymphoma. J Cutan Pathol 2013;40:896-902.
64. Schieke SM, Sharaf MA, Lerner A, Runger TM, Mahalingam M. Primary cutaneous CD56 positive lymphoma: a diagnostic conundrum in an unusual case of lymphoma. J Cutan Pathol 2012;39:540-4.
65. Lan MX, Zhen ZX, Ming WH. CD56-negative extranodal nasal type of natural killer/T-cell lymphoma with extranasal skin involvement. Leuk Lymphoma 2009;50:1715-7.
66. Quintanilla-Martinez L, Jansen PM, Kinney MC, Swerdlow SH, Willemze R. Non-mycosis fungoides cutaneous T-cell lymphomas: report of the 2011 Society for Hematopathology/European Association for Hematopathology workshop. Am J Clin Pathol 2013;139:491-514.
67. Szu Lyn Ding C, Ping Chau Y, Yee Lee H, MingYap W, Leong Chuah K. Test and teach. An unusual cause of nodular skin lesions with ulcer. Diagnosis: cutaneous extranodal NK/T-cell lymphoma, nasal type. Pathology 2008;40:714-8.
68. Pan ST, Chang WS, Murphy M, Martinez A, Chuang SS. Cutaneous peripheral T-cell lymphoma of cytotoxic phenotype mimicking extranodal NK/T-cell lymphoma. Am J Dermatopathol 2011;33:e17-20.
69. Friedmann D, Wechsler J, Delfau MH, Esteve E, Farcet JP, de Muret A, et al. Primary cutaneous pleomorphic small T-cell lymphoma: a review of 11 cases; the French study group on cutaneous lymphomas. Arch Dermatol 1995;131:1009-15.
70. + T-cell lymphomas: a heterogeneous group of tumors with different clinicopathologic features and outcome. J Clin Oncol 2008;26:3364-71.
71. Baum CL, Link BK, Neppalli VT, Swick BL, Liu V. Reappraisal of the provisional entity primary cutaneous CD41 small/medium pleomorphic T-cell lymphoma: a series of 10 adult and pediatric patients and review of the literature. J Am Acad Dermatol 2011;65:739-48.
72. Cerroni L. Lymphoproliferative lesions of the skin. J Clin Pathol 2006;59:813-26. (Pubitemid 44211742)
73. Lin MT, Chang HM, Huang CJ, Chen WL, Lin CY, Lin CY, et al. Massive expansion of EBV1 monoclonal T cells with CD5 down-regulation in EBV-associated hemophagocytic lymphohistiocytosis. J Clin Pathol 2007;60:101-3.
74. + small-/medium-sized pleomorphic T-cell lymphoma: a cutaneous nodular proliferation of pleomorphic T lymphocytes of undetermined significance? A study of 136 cases. Am J Dermatopathol 2009;31:317-22.
75. Hagiwara M, Takata K, Shimoyama Y, Yamamoto K, Takahashi E, Asano N, et al. Primary cutaneous T-cell lymphoma of unspecified type with cytotoxic phenotype: clinicopathological analysis of 27 patients. Cancer Sci 2009; 100:33-41.
76. Petrella T, Maubec E, Cornillet-Lefebvre P, Willemze R, Pluot M, Durlach A, et al. Indolent CD8-positive lymphoid proliferation of the ear: a distinct primary cutaneous T-cell lymphoma? Am J Surg Pathol 2007;31:1887-92. (Pubitemid 350175817)
77. Zeng W, Nava VE, Cohen P, Ozdemirli M. Indolent CD8-positive T-cell lymphoid proliferation of the ear: a report of two cases. J Cutan Pathol 2012;39:696-700.
78. Kempf W, Kazakov DV, Cozzio A, Kamarashev J, Kerl K, Plaza T, et al. Primary cutaneous CD8+ small- to medium-sized lymphoproliferative disorder in extrafacial sites: clinicopathologic features and concept on their classification. Am J Dermatopathol 2013;35:159-66.