Resident Short Reviews. Subcutaneous Panniculitis-like T-Cell Lymphoma
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1 Resident Short Reviews Subcutaneous Panniculitis-like T-Cell Lymphoma Redefinition of Diagnostic Criteria in the Recent World Health Organization European Organization for Research and Treatment of Cancer Classification for Cutaneous Lymphomas Subcutaneous panniculitis-like T-cell lymphoma is a primary T-cell lymphoma that preferentially involves the subcutaneous tissue. Although subcutaneous panniculitis-like T-cell lymphoma has been recognized as a distinctive entity in the category of peripheral T-cell lymphoma in the World Health Organization classification, its diagnostic criteria has been redefined by the recent World Health Organization European Organization for Research and Treatment of Cancer classification for primary cutaneous lymphomas. Subcutaneous panniculitis-like T-cell lymphoma is now restricted to primary cutaneous T-cell lymphoma expressing T-cell receptor phenotype. These lymphomas are usually CD3, CD4, CD8, and CD56, and usually have an indolent clinical course. The clinicopathologic features, differential diagnosis, immunophenotypic characteristics, and molecular features of subcutaneous panniculitis-like T-cell lymphoma are presented in light of the recent World Health Organization European Organization for Research and Treatment of Cancer classification. (Arch Pathol Lab Med. 2009;133: ) Subcutaneous panniculitis-like T-cell lymphoma (SPTCL) is a distinctive skin lymphoma that is characterized by infiltration of the subcutaneous tissue by neoplastic cytotoxic T cells mimicking panniculitis. It was first described by Gonzalez et al 1 in 1991, when they presented 8 cases of T-cell lymphoma localized primarily to the subcutaneous adipose tissue without evident lymph node involvement. It was recognized as a provisional entity and was included in the Revised European-American classification of lymphoid neoplasms in 1994 and later by the European Organization for Research and Treatment of Cancer (EORTC) in ,3 Subcutaneous panniculitis-like T-cell lymphoma was then defined as a distinct entity by the World Health Organization (WHO) classification in Accepted for publication July 7, From the Maui Memorial Medical Center, Clinical Laboratories of Hawaii, Wailuku (Dr Parveen); and the Department of Pathology, Kapiolani Medical Center for Women and Children, Honolulu, Hawaii (Dr Thompson). The authors have no relevant financial interest in the products or companies described in this article. Reprints: Zahida Parveen, MD, Maui Memorial Medical Center, The Clinical Laboratories of Hawaii, 221 Mahalani St, Wailuku, HI ( zahipar@yahoo.com). Zahida Parveen, MD; Karen Thompson, MD It was observed that SPTCL s clinical course was very different depending on the T-cell receptor (TCR) phenotype and immunophenotypic characteristics of the tumor cells. Lymphomas that were TCR phenotype were usually CD4, CD8, CD56 and had an indolent course. On the contrary, lymphomas that were TCR phenotype were usually CD4, CD8, CD56, had a worse prognosis, and were often fatal due to an accompanying hemophagocytic syndrome. 5 Clinical, histologic, and immunophenotypical features of TCR SPTCL and TCR SPTCL are summarized in Table 1. Based on these observations, in the recent World Health Organization European Organization for Research and Treatment of Cancer (WHO- EORTC) classification of primary cutaneous lymphomas, the category of SPTCL is now restricted to cases that express TCR phenotype, whereas cases with TCR phenotype are now placed in a new provisional category of cutaneous T-cell lymphoma 6 (Table 2). The incidence of SPTCL is less than 1% of the non- Hodgkin lymphomas. 4 Since these data were collected prior to the new WHO-EORTC classification and include SPTCL with both TCR and TCR phenotypes, the true incidence of SPTCL is less than previously thought. Subcutaneous panniculitis-like T-cell lymphoma is most common in young adults with a median age of 36 years (range, 9 79 years), with 19% of patients being 20 years or younger. 7 There is a female predominance of this lymphoma, with a male to female ratio of CLINICAL PRESENTATION Patients present with multiple subcutaneous nodules or deeply seated plaques, most commonly on the extremities and trunk. Other sites of involvement include face, neck, and back. 8 The nodules are usually painless, but in rare cases can be painful. Ulceration of nodules in SPTCL is rare, and only 6% of the cases may show ulceration at some stage of the clinical course. 7 In the initial phases of illness, the subcutaneous nodules may regress spontaneously without treatment. New nodules appear at different sites. Hence, it is common to see subcutaneous nodules at various stages of healing and areas of lipoatrophy after regression of the nodules. Prodromal symptoms include fever, chills, weight loss, and myalgias. 7 More than 50% of patients have cytopenias; however, in most instances laboratory abnormalities are not severe. A minority of patients may have lymphadenopathy or hepatosplenomega- Arch Pathol Lab Med Vol 133, February 2009 Subcutaneous Panniculitis-like T-Cell Lymphoma Parveen & Thompson 303
2 Table 1. Comparison of Clinicopathologic Features of T-Cell Receptor (TCR) and TCR Subcutaneous Panniculitis-like T-Cell Lymphoma (SPTCL)* TCR SPTCL TCR SPTCL Age at presentation Younger (median age, 36 y) Older (median age, 59 y) Clinical presentation Subcutaneous nodules, B-symptoms /, cytopenias /, commonly associated with other autoimmune disorders Same presentation as TCR SPTCL; however, the B- symptoms and laboratory abnormalities are more common and severe Lesions Self-healing subcutaneous plaques and nodules without ulceration Disseminated plaques, ulceronecrotic nodules Histology Predominant infiltration of subcutaneous tissue by medium to large lymphocytes with mild pleomorphism, minimal tumor invasion in superficial dermis, mild to moderate apoptosis, patchy necrosis Immunophenotype CD3, CD4, CD8, most CD56, cytotoxic proteins, F1, TCR -1, CD30 Clinical course Treatment Prolonged course with recurrent panniculitis, HPS uncommon (17%), metastasis rare Long-term control with high-dose systemic corticosteroids, recurrent or resistant cases treated with CHOP or CHOP-like chemotherapy Infiltration of subcutaneous tissue with medium to large blastlike lymphocytes with significant pleomorphism, involves entire dermis, angioinvasion common, extensive apoptosis, massive necrosis CD3, CD4, CD8, most CD56, cytotoxic proteins, F1, TCR -1, many CD30 Rapid clinical deterioration, HPS common (45%), metastasis common (lungs, liver, kidneys, CNS, and oral mucosa) Multiagent chemotherapy; however, most have poor response to therapy, including allogenic stem cell transplantation Prognosis Excellent without HPS Poor with or without HPS Five-year overall survival 82% 11% * Data derived in part from Willemze et al. 7 HPS indicates hemophagocytic syndrome; CNS, central nervous system; and CHOP, cyclophosphamide, doxorubicin, vincristine, and prednisone. ly. Clinically, however, these patients do not usually have any evidence of lymphoma outside the subcutis. Metastatic disease or visceral involvement is uncommon in SPTCL. Only cases with TCR phenotype tend to have metastasis to various organs, including lungs, liver, kidneys, and the central nervous system. 7,9,10 Most cases described in the literature before the recent WHO-EORTC classification of cutaneous T-cell lymphomas recognized 2 distinct clinical courses. Hemophagocytic syndrome (HPS) was observed in more aggressive cases showing TCR phenotype and was fatal in most cases, whereas TCR phenotype had long clinical remissions and a favorable outcome. Hemophagocytic syndrome is present in both TCR SPTCL (17%) and TCR phenotype (45%) cases, but the disease is more aggressive in the TCR phenotype. 7 HISTOPATHOLOGIC, IMMUNOPHENOTYPIC, AND MOLECULAR FEATURES The diagnosis of SPTCL is based on the combination of clinical presentation, pathologic examination of skin/subcutaneous tissue, immunohistochemical staining pattern, and molecular analysis. The diagnosis can be difficult, and repeated biopsies may be required once there is clinical suspicion of lymphoma. Histologically, dense lymphoid infiltrate of small- to medium- to large-sized lymphocytes is present preferentially in the subcutaneous tissue, predominantly in lobular pattern (Figure 1, a). Septal pattern is uncommon and represents secondary spillage of neoplastic lymphocytes from the lobules (Figure 1, b). In most cases, dermal invasion is minimal, and it is rare to see neoplastic cells in superficial dermis or epidermis (Figure 2). 11 Neoplastic cells may be found in deeper dermis and surrounding the sweat glands and hair follicles (Figure 3). 7 The lymphocytes show slight atypical features, including hyperchromatic, angulated nuclei and indistinct cell borders (Figure 4). 12 Admixed benign histiocytes, plasma cells, and neutrophils are present, which may give a false appearance of a benign panniculitis (Figure 5). Some cases have features of vague granuloma formation, which may lead to a misdiagnosis of granulomatous panniculitis (Figure 6). Scattered mitoses are common to see, as are apoptotic cells, karyorrhectic debris, and focal areas of fat necrosis (Figure 7). 12 Rimming of individual fat cells by neoplastic cells is a useful diagnostic clue. 13,14 However, this finding should be interpreted with caution, as rimming of the fat Table 2. World Health Organization European Organization for Research and Treatment of Cancer Classification of Cutaneous T-Cell and Natural Killer (NK) Cell Lymphomas* Mycosis fungoides Mycosis fungoides variants and subtypes Folliculotropic mycosis fungoides Pagetoid reticulosis Granulomatous slack skin Sezary syndrome Adult T-cell leukemia/lymphoma Primary cutaneous CD30 lymphoproliferative disorders Primary cutaneous anaplastic large cell lymphoma Lymphomatoid papulosis Subcutaneous panniculitis-like T-cell lymphoma Extranodal NK/T-cell lymphoma, nasal type Primary cutaneous peripheral T-cell lymphoma, unspecified Primary cutaneous aggressive epidermotropic CD8 T-cell lymphoma (provisional) Cutaneous T-cell lymphoma (provisional) Primary cutaneous CD4 small/medium-sized pleomorphic T-cell lymphoma (provisional) * Reprinted with permission. This research was originally published in Willemze et al. WHO EORTC classification for cutaneous lymphomas. Blood. 2005;105: The American Society of Hematology. 304 Arch Pathol Lab Med Vol 133, February 2009 Subcutaneous Panniculitis-like T-Cell Lymphoma Parveen & Thompson
3 Figure 1. a, Subcutaneous panniculitis-like T-cell lymphoma: low magnification showing neoplastic lymphoid cells infiltrating mainly lobular areas of subcutaneous tissue (hematoxylin-eosin, original magnification 50). b, Higher power showing predominant lobular pattern with spillage of neoplastic cells into the septal areas (hematoxylin-eosin, original magnification 100). Figure 2. Same case as in Figure 1. The epidermis and superficial dermis are not involved by the lymphoma cells (hematoxylin-eosin, original magnification 100). Figure 3. Neoplastic lymphocytes in the deeper dermis surrounding the sweat glands (hematoxylin-eosin, original magnification 100). Figure 4. Medium- to large-sized neoplastic lymphocytes with hyperchromatic (a) and angulated (b) nuclei (hematoxylin-eosin, original magnifications 400). Arch Pathol Lab Med Vol 133, February 2009 Subcutaneous Panniculitis-like T-Cell Lymphoma Parveen & Thompson 305
4 Figure 5. Neoplastic lymphocytes admixed with plasma cells and histiocytes can mimic benign panniculitis (hematoxylin-eosin, original magnification 400). Figure 6. Subcutaneous panniculitis-like T-cell lymphoma with vague granuloma formation can resemble granulomatous panniculitis (hematoxylin-eosin, original magnification 400). Figure 7. Apoptotic cells and karyorrhectic debris admixed with atypical lymphocytes and histiocytes (hematoxylin-eosin, original magnification 400). Figure 8. The lymphoma cells are CD4 (a), CD8 (b), with rare CD20 (c) nonneoplastic cells present in the background. Rimming of adipocytes by CD8 (b) neoplastic cells is a characteristic finding in subcutaneous panniculitis-like T-cell lymphoma (immunoperoxidase stains, original magnifications 400). 306 Arch Pathol Lab Med Vol 133, February 2009 Subcutaneous Panniculitis-like T-Cell Lymphoma Parveen & Thompson
5 spaces may also be seen in other primary and secondary cutaneous lymphomas, as well as in lobular panniculitis. 15 In SPTCL, the cells that rim the fat spaces are CD8,and immunohistochemistry is very useful in identifying these cells (Figure 8, a and b). 13 Occasional vasculitis has been reported, but angiocentricity or angiodestruction is not a feature of SPTCL. Immunophenotypically, the neoplastic cells are cytotoxic T cells that are CD3, CD4, CD8, and CD56. 7,8 Scattered sparse, benign CD20 cells can be identified in the background (Figure 8, c). 12 The tumor cells express cytotoxic granular proteins, such as TIA-1, perforin, and granzyme A. All cases are F1 positive and TCR -1 negative. 7 Epstein-Barr virus is not detected and does not appear to play a role in the pathogenesis of this lymphoma. DIFFERENTIAL DIAGNOSIS Subcutaneous panniculitis-like T-cell lymphoma can be misdiagnosed as benign panniculitis, leading to a wrong or delayed diagnosis. Most commonly, this is due to both the clinical presentation as well as histologic picture. Since in the initial phase of the disease the subcutaneous lesions resolve spontaneously and generally respond well to steroid therapy, this may mimic the clinical presentation of benign panniculitis. Histologically, the presence of a mixed inflammatory infiltrate of lymphohistiocytic cells, plasma cells, and neutrophils may give the impression of a benign process. In addition, the lymphoid infiltrate in most cases is without overt atypia. 9 In benign panniculitis, in contrast to SPTCL, aggregates of CD20 B cells are present, mixed with CD3 cells that are both CD4 and CD8 in equal proportions and with a slight predominance of CD4 cells; cells that are TIA-1 are only occasionally seen. 12 Cases showing vacuolar interface change and abundant interstitial mucin deposition may mimic lupus erythematosus panniculitis. 8,9,16 Histologically, unlike SPTCL, lupus erythematosus panniculitis does not show rimming of individual fat cells with CD8 T cells and, immunophenotypically, lupus erythematosus panniculitis shows a predominance of CD4 cell collection with germinal center formation. 17 The presence of germinal centers is usually seen in reactive processes. It is not known whether lupus erythematosus panniculitis progresses to SPTCL, but it is thought that in some cases benign panniculitis may progress to SPTCL, and it has been proposed to call these cases atypical lymphocytic lobular panniculitis. 18 Another important differential diagnosis includes primary cutaneous CD56 natural killer like T-cell lymphoma, which may show clonal TCR gene rearrangement and may express T-cell associated and cytotoxic antigens. However, CD56 natural killer like T-cell lymphoma shows angiocentricity and angiodestruction, a predominantly dermal infiltrate, and Epstein-Barr virus positivity. 19 Other cutaneous lymphomas should be in the differential diagnosis. In most cutaneous lymphomas also involving the subcutaneous tissue, lymphoid infiltrate is usually in the form of dense sheets, and rimming of individual fat spaces by CD8 T cells is usually not seen. 12 TREATMENT AND PROGNOSIS In the past, before SPTCL was restricted to the category of TCR phenotype only, patients were treated with doxorubicin-based chemotherapy, radiotherapy, and/or bone marrow transplantation. However, since it has been observed that TCR SPTCL behaves in an indolent fashion, recent studies suggest that these patients can have long-term remission with high-dose systemic corticosteroids. Most patients with aggressive disease who fail with initial immunosuppressive therapy are treated with anthracycline-based and anthracenedione-based chemotherapy with combined cyclophosphamide, doxorubicin, vincristine, and prednisone. In localized disease without hemophagocytic syndrome, radiation can produce longterm remissions. In addition, radiation therapy can be used for palliative purposes. High-dose chemotherapy and stem cell transplantation has been shown to be very effective, with a high complete remission rate. 7 Therefore, high-dose chemotherapy and stem cell transplantation is usually considered in primary refractory or recurrent cases. SUMMARY Subcutaneous panniculitis-like T-cell lymphoma is a rare cytotoxic T-cell lymphoma that can be misdiagnosed as a benign panniculitis due to histologic similarities between the 2 entities. Subcutaneous panniculitis-like T-cell lymphoma is a clonal lymphoproliferative disorder characterized by infiltration of subcutaneous tissue by CD3, CD4, CD8, and CD56 cells. It is important to recognize the clinical, pathologic, and molecular features of SPTCL and limit cases in this entity to subcutaneous lymphomas expressing TCR phenotype based on the recent WHO- EORTC classification. Long-term follow-up of these patients is important to monitor the course of disease. References 1. 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: 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: 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: Jaffe ES, Harris NL, Stein H, Vardiman JW, eds. Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; World Health Organization Classification of Tumours. 5. Takeshita M, Okamura S, Oshiro Y, et al. Clinicopathologic differences between 22 cases of CD56-negative and CD56-positive subcutaneous panniculitislike lymphoma in Japan. Hum Pathol. 2004;35: Willemze R, Jaffe ES, Burg G, et al. WHO EORTC classification for cutaneous lymphomas. Blood. 2005;105: Willemze R, Jansen PM, Cerroni L, 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: Cassis TB, Fearneyhough PK, Callen JP. Subcutaneous panniculitis-like T-cell lymphoma with vacuolar interface dermatitis resembling lupus erythematosus panniculitis. J Am Acad Dermatol. 2004;50: Ma L, Bandarchi B, Glusac EJ. Fatal subcutaneous panniculitis-like T-cell lymphoma with interface change and dermal mucin, a dead ringer for lupus erythematosus. J Cutan Pathol. 2005;32: Guizzardi M, Hendrickx IA, Mancini LL, Monti M. Cytotoxic gamma/delta subcutaneous panniculitis-like T-cell lymphoma: report of a case with pulmonary involvement unresponsive to therapy. J Eur Acad Dermatol Venereol. 2003;17: Wang CY, Su WP, Kurtin PJ. Subcutaneous panniculitic T-cell lymphoma. Int J Dermatol. 1996;35: Kumar S, Krenacs L, Medeiros J, et al. Subcutaneous panniculitic T-cell lymphoma is a tumor of cytotoxic T lymphocytes. Hum Pathol. 1998;29: 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: Yamazaki K. An ultrastructural study of cutaneous panniculitis-like T-cell lymphoma: cytoplasmic granules and active cellular and cell-to-matrix interaction mimic cytotoxic T-cells. Ultrastruct Pathol. 2002;26: Lozzi GP, Massone C, Citarella L, Kerl H, Cerroni L. Rimming of adipocytes Arch Pathol Lab Med Vol 133, February 2009 Subcutaneous Panniculitis-like T-Cell Lymphoma Parveen & Thompson 307
6 by neoplastic lymphocytes: a histopathologic feature not restricted to subcutaneous T-cell lymphoma. Am J Dermatopathol. 2006;28: Gonzalez EG, Selvi E, Lorenzini S, et al. Subcutaneous panniculitis-like T-cell lymphoma misdiagnosed as lupus erythematosus panniculitis. Clin Rheumatol. 2007;26: Magro CM, Crowson AN, Kovatich AJ, Burns F. Lupus profundus, indeterminate lymphocytic lobular panniculitis and subcutaneous T-cell lymphoma: a spectrum of subcuticular T-cell lymphoid dyscrasia. J Cutan Pathol. 2001;28: Magro CM, Crowson AN, Byrd JC, Soleymani AD, Shendrik I. Atypical lymphocytic lobular panniculitis. J Cutan Pathol. 2004;31: Yamashita Y, Tsuzuki T, Nakayama A, Fujino M, Mori N. A case of natural killer/t cell lymphoma of the subcutis resembling subcutaneous panniculitis-like T cell lymphoma. Pathol Int. 1999;49:241. Prepare Now for the CAP 09 Abstract Program Plan now to submit abstracts and case studies for the CAP 09 meeting, which will be held October 11th through the 14th in Washington, DC. Submissions for the CAP 09 Abstract Program will be accepted from: Monday, February 2, 2009, through Friday, March 27, Accepted submissions will appear in the October 2009 issue of the Archives of Pathology & Laboratory Medicine. Visit the CAP 09 Web site at for additional abstract program information. 308 Arch Pathol Lab Med Vol 133, February 2009 Subcutaneous Panniculitis-like T-Cell Lymphoma Parveen & Thompson
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