Subcutaneous, blastic natural killer (NK), NK/T-cell, and other cytotoxic lymphomas of the skin: A morphologic, immunophenotypic, and molecular study of 50 patients

American Journal of Surgical Pathology

Volumn 28, Issue 6, 2004, Pages 719-735

  Massone, Cesare ^a,b   Chott, Andreas ^c   Metze, Dieter ^d   Kerl, Katrin ^e   Citarella, Luigi ^a,f   Vale, Esmeralda ^g   Kerl, Helmut ^a   Cerroni, Lorenzo ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e UNIVERSITY OF GENEVA   (Switzerland)

^f UNIVERSITY OF ROME TOR VERGATA   (Italy)

^g Dermatologic Center   (Portugal)

Author keywords

Blastic NK cell lymphoma; Cutaneous T cell lymphoma; Epidermotropic CD8+ T cell lymphoma; Nasal type extranodal NK T cell lymphoma; Subcutaneous "panniculitis like" T cell lymphoma

Indexed keywords

CD2 ANTIGEN; CD20 ANTIGEN; CD3 ANTIGEN; CD30 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD7 ANTIGEN; CD8 ANTIGEN; HLA DR ANTIGEN;

ADULT; AGED; ARTICLE; CLASSIFICATION; CLINICAL ARTICLE; CYTOTOXIC LYMPHOCYTE; EPSTEIN BARR VIRUS; EUROPE; FEMALE; GENETIC ANALYSIS; HEMATOLOGIC MALIGNANCY; HISTOPATHOLOGY; HUMAN; IMMUNOPHENOTYPING; LYMPHOMA; MALE; NATURAL KILLER CELL; PANNICULITIS; PLEOMORPHIC T CELL LYMPHOMA; RETROSPECTIVE STUDY; SKIN LYMPHOMA; SURVIVAL; T CELL LYMPHOMA; WORLD HEALTH ORGANIZATION;

ADULT; AGED; ANTIGENS, CD30; ANTIGENS, CD8; FEMALE; HUMANS; IMMUNOPHENOTYPING; KILLER CELLS, NATURAL; LYMPHOMA, LARGE-CELL; LYMPHOMA, T-CELL, CUTANEOUS; MALE; MIDDLE AGED; PANNICULITIS; SKIN NEOPLASMS; SURVIVAL RATE; T-LYMPHOCYTES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 2542451247     PISSN: 01475185     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.pas.0000126719.71954.4f     Document Type: Article

References (95)

1. Agnarsson BA, Vonderheid EC, Kadin ME. Cutaneous T cell lymphoma with suppressor/cytotoxic (CD8) phenotype: identification of rapidly progressive and chronic subtypes. J Am Acad Dermatol. 1990;22:569-577.
2. Alegre VA, Winkelmann RK. Histiocytic cytophagic panniculitis. J Am Acad Dermatol. 1989;20:177-185.
3. Arnulf B, Copie-Bergman C, Delfau-Larue MH, et al. Nonhepatosplenic gammadelta T-cell lymphoma: a subset of cytotoxic lymphomas with mucosal or skin localization. Blood. 1998;91:1723-1731.
4. Au WY, Ng WM, Choy C, et al. Aggressive subcutaneous panniculitis-like T-cell lymphoma: complete remission with fludarabine, mitoxantrone and dexamethasone. Br J Dermatol. 2000;143:408-410.
5. Avinoach I, Halevy S, Argov S, et al. Gamma/delta T-cell lymphoma involving the subcutaneous tissue and associated with a hemophagocytic syndrome. Am J Dermatopathol. 1994;16:426-433.
6. Bagot M, Bouloc A, Charue D, et al. Do primary cutaneous non-T non-B CD4+CD56+ lymphomas belong to the myelo-monocytic lineage? J Invest Dermatol. 1998;111:1242-1244.
7. Beljaards RC, Meijer CJ, Van der Putte SC, et al. Primary cutaneous T-cell lymphoma: clinicopathological features and prognostic parameters of 35 cases other than mycosis fungoides and CD30-positive large cell lymphoma. J Pathol. 1994;172:53-60.
8. Berti E, Cerri A, Cavicchini S, et al. Primary cutaneous gamma/delta T-cell lymphoma presenting as disseminated pagetoid reticulosis. J Invest Dermatol. 1991;96:718-723.
9. Berti E, Tomasini D, Vermeer MH, et al. Primary cutaneous CD8-positive epidermotropic cytotoxic T cell lymphomas. A distinct clinicopathological entity with an aggressive clinical behavior. Am J Pathol. 1999;155: 483-492.
10. Bower CP, Standen GR, Pawade J, et al. Cutaneous presentation of steroid responsive blastoid natural killer cell lymphoma. Br J Dermatol. 2000; 142:1017-1020.
11. Brody JP, Allen S, Schulman P, et al. Acute agranular CD4-positive natural killer cell leukemia. Comprehensive clinicopathologic studies including virologic and in vitro culture with inducing agents. Cancer. 1995;75: 2474-2483.
12. Burg G, Dummer R, Wilhelm M, et al. A subcutaneous delta-positive T-cell lymphoma that produces interferon gamma. N Engl J Med. 1991; 325:1078-1081.
13. Burg G, Dummer R, Nestle F. Distinct subtypes of subcutaneous T-cell lymphoma. Arch Dermatol. 1994;130:1073.
14. Cerroni L, Smolle J, Soyer HP, et al. Immunophenotyping of cutaneous lymphoid infiltrates in frozen and paraffin-embedded tissue sections: a comparative study. J Am Acad Dermatol. 1990;22:405-413.
15. Chan JK, Sin VC, Wong KF, et al. Non nasal lymphoma expressing the natural killer cell marker CD56: a clinicopathologic study of 49 cases of an uncommon aggressive neoplasm. Blood. 1997;89:4501-4513.
16. Chan JK, Yip TT, Tsang WY, et al. Detection of Epstein-Barr viral RNA in malignant lymphomas of the upper aerodigestive tract. Am J Surg Pathol. 1994;18:938-946.
17. Chan JK. Natural killer cell neoplasms. Anat Pathol. 1998;3:77-145.
18. Chan JK. Peripheral T-cell and NK-cell neoplasms: an integrated approach to diagnosis. Mod Pathol. 1999;12:177-199.
19. Chan JKC, Jaffe ES, Ralfkiaer E. Blastic NK-cell lymphoma. In: Jaffe ES, Harris NL, Stein H, et al, eds. World Health Organization Classitication of Tumours. Tumours of Haemotopoietic and Lymphoid Tissues. Lyon: IARC Press, 2001:214-215.
20. Chan JKC, Jaffe ES, Ralfkiaer E. Extranodal NK/T-cell lymphoma, nasal type. In: Jaffe ES, Harris NL, Stein H, et al, eds. World Health Organization Classification of Tumours. Tumours of haemotopoietic and lymphoid tissues. Lyon: IARC Press, 2001:204-205.
21. Chang SE, Choi HJ, Huh J, et al. A case of primary cutaneous CD56+, TdT+, CD4+, blastic NK-cell lymphoma in a 19-year-old woman. Am J Dermatopathol. 2002;24:72-75.
22. Chang SE, Huh J, Choi JH, et al. Clinicopathological features of CD56+ nasal-type T/natural killer cell lymphomas with lobular panniculitis. Br J Dermatol. 2000;142:924-930.
23. Chaperot L, Bendriss N, Manches O, et al. Identification of a leukemic counterpart of the plasmacytoid dendritic cells. Blood. 2001;97:3210-3217.
24. Cho KH, Oh JK, Kim CW, et al. Peripheral T-cell lymphoma involving subcutaneous tissue. Br J Dermatol. 1995;132:290-295.
25. Chott A, Augustin I, Wrba F, et al. Peripheral T-cell lymphomas: a clinicopathologic study of 75 cases. Hum Pathol. 1990;21:1117-1125.
26. Craig AJ, Cualing H, Thomas G, et al. Cytophagic histiocytic panniculitis: a syndrome associated with benign and malignant panniculitis: case comparison and review of the literature. J Am Acad Dermatol. 1998;39:721-736.
27. Crotty CP, Winkelmann RK. Cytophagic histiocytic panniculitis with fever, cytopenia, liver failure, and terminal hemorrhagic diathesis. J Am Acad Dermatol. 1981;4:181-194.
28. Dargent JL, Roufosse C, Delville JP, et al. Subcutaneous panniculitis-like T-cell lymphoma: further evidence for a distinct neoplasm originating from large granular lymphocytes of T/NK phenotype. J Cutan Pathol. 1998;25:394-400.
29. de Wolf-Peeters C, Achten R. Gammadelta T-cell lymphomas: a homogeneous entity? Histopathology. 2000;36:294-305.
30. DiGiuseppe JA, Louie DC, Williams JE, et al. Blastic natural killer cell leukemia/lymphoma: a clinicopathologic study. Am J Surg Pathol. 1997; 21:1223-1230.
31. Dummer R, Potoczna N, Haffner AC, et al. A primary cutaneous non-T, non-B CD4+, CD56+ lymphoma. Arch Dermatol. 1996;132:550-553.
32. El Shabrawi-Caelen L, Cerroni L, Kerl H. The clinicopathologic spectrum of cytotoxic lymphomas of the skin. Semin Cutan Med Surg. 2000;19: 118-123.
33. Feuillard J, Jacob MC, Valensi F, et al. Clinical and biologic features of CD4(+)CD56(+) malignancies. Blood. 2002;99:1556-1563.
34. Fink-Puches R, Zenahlik P, Bäck B, et al. Primary cutaneous lymphomas: applicability of current classification schemes (European Organization for Research and Treatment of Cancer, World Health Organization) based on clinicopathologic features observed in a large group of patients. Blood. 2002;99:800-805.
35. Gonzalez CL, Medeiros LJ, Braziel RM, et al. T-cell lymphoma involving subcutaneous tissue. A clinicopathologic entity commonly associated with hemophagocytic syndrome. Am J Surg Pathol. 1991;15:17-27.
36. Harris NL, Jaffe ES, Stein H, et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood. 1994;84:1361-1392.
37. Haycox CL, Back AL, Raugi GJ, et al. Subcutaneous T-cell lymphoma treated with systemic chemotherapy, autologous stem cell support, and limb amputation. J Am Acad Dermatol. 1997;37:832-835.
38. Hoque SR, Child FJ, Whittaker SJ, et al. Subcutaneous panniculitis-like T-cell lymphoma: clinicopathological, immunophenotypic and molecular analysis of six patients. Br J Dermatol. 2003;148:516-525.
39. Huilgol SC, Fenton D, Pambakian H, et al. Fatal cytophagic panniculitis and haemophagocytic syndrome. Clin Exp Dermatol. 1998;23:51-55.
40. Husak R, Blume-Peytaki U, Orfanos CE. Aleukemic leukemia cutis in an adolescent boy. N Engl J Med. 1999;340:893-894.
41. Hytiroglou P, Phelps RG, Wattenberg DJ, et al. Histiocytic cytophagic panniculitis: molecular evidence for a clonal T-cell disorder. J Am Acad Dermatol. 1992;27:333-336.
42. Jaffe ES, Harris NL, Stein H, et al. World Health Organization Classification of Tumours. Tumours of haemotopoietic and lymphoid tissues. Lyon: IARC Press, 2001.
43. Jaffe ES, Ralfkiaer E. Subcutaneous panniculitis-like T-cell lymphoma. In: Jaffe ES, Harris NL, Stein H, et al, eds. World Health Organization Classification of Tumours. Tumours of haemotopoietic and lymphoid tissues. Lyon: IARC Press, 2001:212-213.
44. Jaffe ES. Nasal and nasal-type T/NK cell lymphoma: a unique form of lymphoma associated with the Epstein-Barr virus. Histopathology. 1995; 27:581-583.
45. Jing X, Nakamura Y, Nakamura M, et al. Detection of Epstein-Barr virus DNA in gastric carcinoma with lymphoid stroma. Viral Immunol. 1997; 10:49-58.
46. Joly P, Vasseur E, Esteve E, et al. Primary cutaneous medium and large cell lymphomas other than mycosis fungoides. An immunohistological and follow-up study on 54 cases. French Study Group for Cutaneous Lymphomas. Br J Dermatol. 1995;132:506-512.
47. Jones D, Vega F, Sarris AH, et al. CD4-CD8-"double-negative" cutaneous T-cell lymphomas share common histologic features and an aggressive clinical course. Am J Surg Pathol. 2002;26:225-231.
48. Kaddu S, Zenahlik P, Beham-Schmid C, et al. Specific cutaneous infiltrates in patients with myelogenous leukemia: a clinicopathologic study of 26 patients with assessment of diagnostic criteria. J Am Acad Dermatol. 1999;40:966-978.
49. Kadin ME. Cutaneous gamma delta T-cell lymphomas: how and why should they be recognized? Arch Dermatol. 2000;136:1052-1054.
50. Kanavaros P, Lescs MC, Briere J, et al. Nasal T-cell lymphoma: a clinicopathologic entity associated with peculiar phenotype and with Epstein-Barr virus. Blood. 1993;81:2688-2695.
51. Kato N, Yasukawa K, Kimura K, et al. CD2- CD4+ CD56+ hematodermic/hematolymphoid malignancy. J Am Acad Dermatol. 2001;44: 231-238.
52. Khoury JD, Medeiros LJ, Manning JT, et al. CD56(+) TdT(+) blastic natural killer cell tumor of the skin: a primitive systemic malignancy related to myelomonocytic leukemia. Cancer. 2002;94:2401-2408.
53. Ko YH, Kim SH, Ree HJ. Blastic NK-cell lymphoma expressing terminal deoxynucleotidyl transferase with Homer-Wright type pseudorosettes formation. Histopathology. 1998;33:547-553.
54. Kumar S, Krenacs L, Medeiros J, et al. Subcutaneous parmiculitic T-cell lymphoma is a tumor of cytotoxic T lymphocytes. Hum Pathol. 1998;29: 397-403.
55. Leroux D, Mugneret F, Callanan M, et al. CD4(+), CD56(+) DC2 acute leukemia is characterized by recurrent clonal chromosomal changes affecting 6 major targets: a study of 21 cases by the Groupe Francais de Cytogenetique Hematologique. Blood. 2002;99:4154-4159.
56. Lu D, Patel KA, Duvic M, et al. Clinical and pathological spectrum of CD8-positive cutaneous T-cell lymphomas. J Cutan Pathol. 2002;29: 465-472.
57. Magro CM, Crowson AN, Kovatich AJ, et al. Lupus profundus, indeterminate lymphocytic lobular panniculitis and subcutaneous T-cell lymphoma: a spectrum of subcuticular T-cell lymphoid dyscrasia. J Cutan Pathol. 2001;28:235-247.
58. Marzano AV, Alessi E, Berti E. CD30-positive multilobated peripheral T-cell lymphoma primarily involving the subcutaneous tissue. Am J Dermatopathol. 1997;19:284-288.
59. Marzano AV, Berti E, Paulli M, et al. Cytophagic histiocytic panniculitis and subcutaneous panniculitis-like T-cell lymphoma: report of 7 cases. Arch Dermatol. 2000;136:889-896.
60. McCarthy KP, Sloane JP, Kabarowski JHS, et al. A simplified method of detection of clonal rearrangements of the T-cell receptor-gamma chain gene. Diagn Mol Pathol. 1992;1:173-179.
61. Mehregan DA, Su WP, Kurtin PJ. Subcutaneous T-cell lymphoma: a clinical, histopathologic, and immunohistochemical study of six cases. J Cutan Pathol. 1994;21:110-117.
62. Miyamoto T, Yoshino T, Takehisa T, et al. Cutaneous presentation of nasal/nasal type T/NK cell lymphoma: clinicopathological findings of four cases. Br J Dermatol. 1998;139:481-487.
63. Monterroso V, Bujan W, Jaramillo O, et al. Subcutaneous tissue involvement by T-cell lymphoma. A report of 2 cases. Arch Dermatol. 1996;132: 1345-1350.
64. Munn SE, McGregor JM, Jones A, et al. Clinical and pathological heterogeneity in cutaneous gamma-delta T-cell lymphoma: a report of three cases and a review of the literature. Br J Dermatol. 1996;135:976-981.
65. Nagatani T, Okazawa H, Kambara T, et al. Cutaneous monomorphous CD4- and CD56-positive large-cell lymphoma. Dermatology. 2000;200: 202-208.
66. Nakamura S, Koshikawa T, Yatabe Y. et al. Lymphoblastic lymphoma expressing CD56 and TdT. Am J Surg Pathol. 1998;22:135-137.
67. Nakamura S, Suchi T, Koshikawa T, et al. Clinicopathologic study of CD56 (NCAM)-positive angiocentric lymphoma occurring in sites other than the upper and lower respiratory tract. Am J Surg Pathol. 1995;19: 284-296.
68. Ohtake N, Shimada S, Mizoguchi S, et al. Membranocystic lesions in a patient with cytophagic histiocytic panniculitis associated with subcutaneous T-cell lymphoma. Am J Dermatopathol. 1998;20:276-280.
69. O'Quinn RP, Zic JA, Boyd AS. Mycosis fungoides d'emblee: CD30-negative cutaneous large T-cell lymphoma. J Am Acad Dermatol. 2000; 43:861-863.
70. Perniciaro C, Zalla MJ, White JW Jr, et al. Subcutaneous T-cell lymphoma. Report of two additional cases and further observations. Arch Dermatol. 1993;129:1171-1176.
71. Petrella T, Dalac S, Maynadie M, et al. CD4+ CD56+ cutaneous neoplasms: a distinct hematological entity? Groupe Français d'Etude des Lymphomes Cutanés (GFELC). Am J Surg Pathol. 1999;23:137-146.
72. 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;26:852-862.
73. Popper HH, Winter E, Höfler G. DNA sequences of mycobacterium tuberculosis in formalin fixed and paraffin embedded tissue in tuberculosis and sarcoidosis detected by PCR. Am J Clin Pathol. 1994;101:738-741.
74. Przybylski GK, Wu H, Macon WR, et al. Hepatosplenic and subcutaneous panniculitis-like gamma/delta T cell lymphomas are derived from different Vdelta subsets of gamma/delta T lymphocytes. J Mol Diagn. 2000;2: 11-19.
75. Radonich MA, Lazova R, Bolognia J. Cutaneous natural killer/T-cell lymphoma. J Am Acad Dermatol. 2002;46:451-456.
76. Requena L, Sanchez Yus E. Panniculitis. Part II. Mostly lobular panniculitis. J Am Acad Dermatol. 2001;45:325-361.
77. Romero LS, Goltz RW, Nagi C, et al. Subcutaneous T-cell lymphoma with associated hemophagocytic syndrome and terminal leukemic transformation. J Am Acad Dermatol. 1996;34:904-910.
78. Salhany KE, Macon WR, Choi JK, et al. Subcutaneous panniculitis-like T-cell lymphoma: clinicopathologic, immunophenotypic, and genotypic analysis of alpha/beta and gamma/delta subtypes. Am J Surg Pathol. 1998;22:881-893.
79. Santucci M, Pimpinelli N, Massi D, et al. Cytotoxic/natural killer cell cutaneous lymphomas. Cancer. 2003;97:610-627.
80. Scarabello A, Leinweber B, Ardigò M, et al. Cutaneous lymphomas with prominent granulomatous reaction: a potential pitfall in the histopathologic diagnosis of cutaneous T- and B-cell lymphomas. Am J Surg Pathol. 2002;26:1259-1268.
81. Scott AA, Head DR, Kopecky KJ, et al. HLA-DR-, CD33+, CD56+, CD 16- myeloid/natural killer cell acute leukemia: a previously unrecognized form of acute leukemia potentially misdiagnosed as French-American-British acute myeloid leukemia-M3. Blood. 1994;84:244-255.
82. Sterry W, Siebel A, Mielke V. HTLV-1-negative pleomorphic T-cell lymphoma of the skin: the clinicopathological correlations and natural history of 15 patients. Br J Dermatol. 1992;126:456-462.
83. Suzuki R, Yamamoto K, Seto M, et al. CD7+ and CD56+ myeloid/natural killer cell precursor acute leukemia: a distinct hematolymphoid disease entity. Blood. 1997;90:2417-2428.
84. Taniguchi S, Kono T. Subcutaneous T-cell lymphoma in a child with eosinophilia. Br J Dermatol. 2000;142:183-184.
85. Toro JR, Beaty M, Sorbara L, et al. Gamma delta T-cell lymphoma of the skin: a clinical, microscopic, and molecular study. Arch Dermatol. 2000; 136:1024-1032.
86. Toro JR, Liewehr DJ, Pabby N, et al. Gamma delta T-cell phenotype is associated with significantly decreased survival in cutaneous T-cell lymphoma. Blood. 2003;101:3407-3412.
87. Torok L, Gurbity TP, Kirschner A, et al. Panniculitis-like T-cell lymphoma clinically manifested as alopecia. Br J Dermatol. 2002;147:785-788.
88. Vidal E, Brocq L. Etude sur le mycosis fongoïde. La France Médical. 1885;2:946-1019.
89. von den Driesch P, Staib G, Simon M, et al. Subcutaneous T-cell lymphoma. J Am Acad Dermatol. 1997;36:285-289.
90. Wang CE, Su WPD, Kurtin PJ. Subcutaneous panniculitic T-cell lymphoma. Int J Dermatol. 1996;35:1-8.
91. Wan JH, Trainor KJ, Brisco MJ, et al. Monoclonality in B cell lymphoma detected in paraffin wax embedded sections using the polymerase chain reaction. J Clin Pathol. 1990;43:888-890.
92. Wasik F, Kolodziej T, Jelen M, et al. Subcutaneous T-cell lymphoma: report of two cases. J Eur Acad Dermatol Venereol. 1998;10:62-66.
93. Weenig RH, Ng CS, Perniciaro C. Subcutaneous panniculitis-like T-cell lymphoma: an elusive case presenting as lipomembranous panniculitis and a review of 72 cases in the literature. Am J Dermatopathol. 2001;23: 206-215.
94. Wick MR, Patterson JW. Cytophagic histiocytic panniculitis: a critical reappraisal. Arch Dermatol. 2000;136:922-924.
95. Willemze R, Kerl H, Sterry W, et al. EORTC classification for primary cutaneous lymphomas: a proposal from the Cutaneous Lymphoma Study Group of the European Organization for Research and Treatment of Cancer. Blood. 1997;90:354-371.