Primary Cutaneous Acral CD8 þ T-Cell Lymphoma
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1 Primary Cutaneous Acral CD8 þ T-Cell Lymphoma Vivian M. Hathuc, DO; Alexandra C. Hristov, MD; Lauren B. Smith, MD Primary cutaneous acral CD8 þ T-cell lymphoma is a new provisional entity in the 2016 revision of the World Health neoplasms. 6 Correct classification of this entity is essential to avoid unnecessary aggressive treatment. Organization classification of lymphoid neoplasms. This is a challenging diagnosis because of its rarity, as well as its morphologic and immunophenotypic overlap with other CLINICAL FEATURES Primary cutaneous acral CD8 þ T-cell lymphoma typically CD8 þ cytotoxic lymphoid proliferations. Appropriate occurs in adults older than 50 years, with a slight male classification of this entity is crucial because of its indolent predominance. 4 Most cases are characterized by a solitary, clinical behavior compared with other CD8 þ T-cell slow-growing nodule 7,8 without preceding patches or lymphomas. Knowledge of the clinical setting, sites of involvement, and morphologic features can aid in correct diagnosis. Here, we review the clinical and pathologic features of primary cutaneous acral CD8 þ T-cell lymphoma plaques, 5,9 but bilateral, symmetrical disease and recurrent disease have been reported. 2,4 Although most cases arise on the ear, other peripheral locations, particularly the nose, hands, and feet, have also been described as sites of with an emphasis on the differential diagnosis among other involvement. 2 5,8,10 These findings suggest that a local, C8 þ T-cell lymphomas. (Arch Pathol Lab Med. 2017;141: ; doi: antigenic stimulus specific to the ear is unlikely. 9 Because of the invariably indolent clinical course, there has also been /arpa RA) speculation that primary cutaneous acral CD8 þ T-cell lymphoma may represent a reactive process; however, the I frequent monoclonality and aberrant loss of T-cell antigens n 2007, Petrella and colleagues 1 described 4 cases of supports these lesions being a true lymphoproliferative cutaneous lymphomas, localized to the ear, with indolent disorder. 9 clinical behavior despite high-grade morphologic findings. Each patient presented with a slow-growing nodule PATHOLOGIC FEATURES localized to the ear, and all cases demonstrated an indolent The original series described by Petrella and colleagues 1 clinical course, regardless of treatment modality (surgery, showed a diffuse proliferation of monomorphic, intermediate-sized CD8 þ T-cells (Figure 1, A and B) involving the radiation, observation). This newly described entity, referred to as indolent CD8 þ lymphoid proliferation of the ear, could dermis and subcutis. Each case exhibited a well-defined not be classified into any existing type of cutaneous T-cell grenz zone without epidermotropism. The neoplastic cells lymphoma, and the clinical behavior was unusual for a had irregular, lymphoblast-like nuclei (Figure 1, C). primary cutaneous peripheral T-cell lymphoma, unspecified. Since the initial report, it is now known that indolent CD8 þ lymphoid proliferation may arise at other peripheral Immunoperoxidase studies showed expression of CD3, CD8, T-cell receptor bf1 (Figure 1, D) and T-cell intracytoplasmic antigen-1 (TIA-1; Figure 2, A) with a low sites. 2 4 With largely reproducible clinical and pathologic proliferation index (,10%) (Figure 2, B). 1 CD4, CD30, findings, in addition to an invariably indolent clinical course, CD56, granzyme B, and Epstein-Barr virus encoded small it seemed inappropriate to classify these lesions as RNA were negative with variable loss of other T-cell peripheral T-cell lymphoma, unspecified. 2,5 Consequently, primary cutaneous acral CD8 þ T-cell lymphoma has been added as a provisional entity in the 2016 revision of the antigens. 1 Of the 3 cases examined by molecular analysis, all patients demonstrated a monoclonal T-cell c-gene rearrangement. 1 World Health Organization classification of lymphoid Using the Petrella et al 1 series as the prototype, additional cases have amassed in the literature, and it is apparent that the morphologic and immunophenotypic features for the Accepted for publication May 25, entity indolent CD8 þ lymphoid proliferation of acral sites are From the Sections of Hematopathology (Drs Hathuc and Smith) reproducible. 2,4,7,8,11 Additional features identified in later and Dermatopathology (Dr Hristov) in the Department of Pathology, University of Michigan Medical Center, Ann Arbor. case studies include the absence of necrosis, ulceration, and The authors have no relevant financial interest in the products or angiocentricity. 2,12 Although most cases exhibit similar companies described in this article. morphology to those originally described, variant features Presented in part at the New Frontiers in Pathology meeting; including a moderate proliferation index (30% 40%), focal October 13 15, 2016; Ann Arbor, Michigan. epidermotropism, Pautrier collections, and granzyme B Reprints: Lauren B. Smith, MD, Section of Hematopathology, Department of Pathology, University of Michigan Medical Center, expression have been reported. 2 Also, although most cases 5242 Medical Science 1, 1301 Catherine St, Ann Arbor, MI exhibit a monoclonal T-cell c-gene rearrangement, rare ( lbsmith@med.umich.edu). Arch Pathol Lab Med Vol 141, November 2017 negative cases have been observed. 1,2,4,5,7,9,13 Primary Cutaneous Acral CD8 þ T-Cell Lymphoma Hathuc et al 1469
2 Figure 1. Primary cutaneous acral CD8 þ T-cell lymphoma. A, Hematoxylin-eosin stained section showing a dense, monomorphic infiltrate within the subcutaneous tissue composed of intermediate-sized cells. B, CD8 showing diffuse positivity. C, Hematoxylin-eosin stained section showing grooved/folded nuclei, delicate chromatin, abundant cytoplasm, and small nucleoli. D, T-cell receptor bf1 showing diffuse coexpression with the CD8 þ population (original magnifications 3100 [A] and 3500 [C]; original magnification 3100 [B and D]). Recently, CD68 was described as a possible discriminatory marker in distinguishing primary cutaneous acral CD8 þ T- cell lymphoma from aggressive T-cell lymphomas with a cytotoxic CD8 þ phenotype. 3 Wobser and colleagues 3 investigated 44 cases of CD8 þ cutaneous T-cell lymphomas and identified 5 cases of primary cutaneous acral CD8 þ T-cell lymphoma. During immunohistochemical workup, all 5 cases of primary cutaneous acral CD8 þ T-cell lymphoma demonstrated unusual, dotlike perinuclear positivity for CD68 in the Golgi zone of neoplastic cells (Figure 2, C and D). None of the other CD8 þ cutaneous lymphomas expressed CD68, leading the authors to conclude that CD68 with a dotlike pattern may be helpful in identifying primary cutaneous acral CD8 þ T-cell lymphoma. 3 Although the preliminary data are promising, testing with more cases is warranted to substantiate the sensitivity of this marker. 11,14 DIFFERENTIAL DIAGNOSIS Knowledge of the clinical course and distribution of lesions in primary cutaneous acral CD8 þ T-cell lymphoma is instrumental in making the correct diagnosis. The indolent clinical course helps exclude rapidly progressing lymphomas, such as primary cutaneous aggressive epidermotropic CD8 þ cytotoxic T-cell lymphoma, peripheral cutaneous T- cell lymphoma, not otherwise specified, and primary cutaneous cd T-cell lymphoma. 2 5,7 10 The absence of preexisting patches and plaques helps to distinguish primary cutaneous acral CD8 þ T-cell lymphoma from CD8 þ mycosis fungoides. 4 There is no predilection for the subcutaneous tissue, as observed in subcutaneous panniculitis-like T-cell lymphoma. 15 The frequent acral localization and solitary nature of these lesions make lymphomatoid papulosis less likely. 2 5,7 9 Although some authors describe the infiltrates of primary cutaneous acral CD8 þ T-cell lymphoma as more monomorphic than those of primary cutaneous small/ medium-sized pleomorphic cutaneous T-cell lymphoma, the 2 entities may be morphologically indistinguishable. 10 Furthermore, there is striking overlap in clinical features, such as an adult patient population, a predilection for the face and neck, solitary tumors lacking ulceration, and 1470 Arch Pathol Lab Med Vol 141, November 2017 Primary Cutaneous Acral CD8 þ T-Cell Lymphoma Hathuc et al
3 Figure 2. Primary cutaneous acral CD8 þ T-cell lymphoma. A, T-cell intracytoplasmic antigen 1 (TIA-1) expression in the neoplastic cells. B, Ki-67 showing a low proliferation index. C and D, CD68 highlighting the neoplastic cells with dotlike perinuclear positivity localized to the Golgi zone (original magnification 3500 [A]; original magnification 3100 [B]; original magnifications 3100 [C] and 3500 [D]). indolent clinical behavior. 8,16 Althoughitmaybereasonable to regard primary cutaneous acral CD8 þ T-cell lymphoma as a CD8 þ analogue to CD4 þ primary cutaneous small/medium-sized pleomorphic cutaneous T-cell lymphoma, studies have shown that the neoplastic CD4 þ T cells in the latter coexpress programmed death receptor-1 (PD-1), B-cell lymphoma 6 (BCL6), chemokine ligand 13 (CXCL13), and inducible T-cell costimulator (CD278), indicating a follicular helper T-cell phenotype. 5,7,12,17 These markers have been negative in primary cutaneous acral C8 þ T-cell lymphoma. 2,9 Fortunately, primary cutaneous small/medium-sized pleomorphic cutaneous T-cell lymphoma and primary cutaneous acral CD8 þ T-cell lymphoma are defined by, and are readily distinguished by, expression of CD4 or CD8, respectively. The main morphologic clue in distinguishing primary cutaneous acral CD8 þ T-cell lymphoma from CD8 þ variants of mycosis fungoides, CD8 þ aggressive T-cell lymphoma, and type D lymphomatoid papulosis, is epidermotropism Although rare cases of primary cutaneous acral CD8 þ T-cell lymphoma have exhibited epidermotropism and single intraepidermal Pautrier collections, most cases demonstrate epidermal sparing with a discrete grenz zone. 2 Immunoperoxidase studies are effective in distinguishing primary cutaneous acral CD8 þ T-cell lymphoma from morphologic mimickers. Primary cutaneous cd lymphoma is excluded by the presence of T-cell receptor bf1 expression and the lack of association with Epstein-Barr virus excludes cutaneous extranodal natural killer/t-cell lymphoma. 5 The absence of CD30 excludes primary cutaneous CD30 þ lymphoproliferative disorders, such as cutaneous anaplastic large cell lymphoma and lymphomatoid papulosis. 4,10 The morphologic and immunophenotypic overlap between primary cutaneous acral CD8 þ T-cell lymphoma and subcutaneous panniculitis-like T-cell lymphoma present a formidable diagnostic challenge. Classic features of subcutaneous panniculitis-like T-cell lymphoma, such as lobular infiltration with septal sparing (Figure 3, A) and adipocyte rimming (Figure 3, B), may not be evident in a limited biopsy specimen. 7,8,10,15 Although CD68 is ex- Arch Pathol Lab Med Vol 141, November 2017 Primary Cutaneous Acral CD8 þ T-Cell Lymphoma Hathuc et al 1471
4 Figure 3. Subcutaneous panniculitis-like T-cell lymphoma. A, Hematoxylin-eosin stained section showing an atypical lymphoid infiltrate confined to the subcutaneous tissue. Lobular involvement with septal sparing is characteristic. B, Hematoxylin-eosin stained section showing atypical lymphocytes rimming individual adipocytes. C, CD8 highlighting the neoplastic cells (original magnifications 320 [A] and 3400 [B]; original magnification 3200 [C]). pressed in the neoplastic cells of primary cutaneous acral CD8 þ T-cell lymphoma in an unusual, dotlike perinuclear pattern localized to the Golgi zone, 3 subcutaneous panniculitis-like T-cell lymphoma may have abundant histiocytes, 7,8,10,15 making assessment of the neoplastic cells challenging. Although both entities are known to have a cytotoxic immunophenotype (Figure 3, C) and often show aberrant loss of T-cell markers (Figure 4, A), granzyme B is typically negative in primary cutaneous acral CD8 þ T-cell lymphoma and positive in most subcutaneous panniculitis-like T-cell lymphomas (Figure 4, B). 4,18 Fat necrosis is frequently a prominent feature in subcutaneous panniculitis-like T-cell lymphoma (Figure 4, C), whereas it is absent in primary cutaneous acral CD8 þ T- cell lymphoma. 2,7,9,10,12 Possibly, the most helpful distinguishing finding is Ki-67. The proliferation index in subcutaneous panniculitis-like T-cell lymphoma is high (Figure 4, D), whereas primary cutaneous acral CD8 þ T-cell lymphoma typically exhibits a proliferation rate of less than 20%. 4 A clinical history of autoimmune disease, 7,10 lupus erythematosus panniculitis, 7,10 and the presence of indurated violaceous plaques 7 or subcutaneous nodules 8,15 is associated with the diagnosis of subcutaneous panniculitislike T-cell lymphoma. A summary of clinical, morphologic, and immunophenotypic findings for CD8 þ cutaneous T-cell lymphomas is provided in the Table PROGNOSIS AND TREATMENT Despite the high-grade morphologic features and cytotoxic immunophenotype, the clinical course for primary cutaneous acral CD8 þ T-cell lymphoma is invariably indolent. Although there have been cases of cutaneous relapse, there are no reports of extracutaneous disease at diagnosis, and no staging investigations have shown progression to systemic disease during follow-up periods of 3 to 168 months, regardless of treatment modality (topical steroids, radiotherapy, surgical excision, or simple observation). 4 Interferon, psoralen-ultraviolet A phototherapy, and methotrexate have been used in patients with multifocal cutaneous disease to minimize the occurrence of relapse with varying degrees of success. 4, Arch Pathol Lab Med Vol 141, November 2017 Primary Cutaneous Acral CD8 þ T-Cell Lymphoma Hathuc et al
5 Skin Lesions CD8 þ cutaneous lymphomas Primary cutaneous acral CD8 þ T-cell lymphoma Primary cutaneous aggressive epidermotropic CD8 þ cytotoxic T-cell lymphoma Subcutaneous panniculitis-like T- cell lymphoma Solitary, slowgrowing erythematous nodule; head and neck (especially ear), hands, feet Rapidly growing, generalized, and ulcerated papules, plaques, nodules; trunk, extremities, face; rapidly disseminated lesions to visceral sites Solitary or multiple, deeply seated plaques or subcutaneous nodules; often extremities Differential Diagnosis of CD8 þ Cutaneous T-Cell Lymphomas Cell Size Small medium Epidermotropism Loss of T-Cell Markers TCRbF1 Cytotoxic Markers PD-1 þ Cells Potentially Distinguishing Features þ þ þ Monotonous infiltration of the dermis with a grenz zone below the unaffected epidermis; CD68 localized to Golgi zone Medium þ þ þ þ N/A Prominent epidermotropism, folliculotropism common Small medium, rarely large CD8 variants of CD4 or null cutaneous lymphomas Mycosis fungoides, cytotoxic Cutaneous anaplastic large cell lymphoma Peripheral cutaneous T-cell lymphoma, not otherwise specified Primary cutaneous small/mediumsized pleomorphic cutaneous T-cell lymphoma Generalized, scaly patches and plaques, ulcerated nodules; predilection for buttocks and sunprotected areas Solitary or grouped ulcerating nodules that can regress but often recur; head, extremities Scattered or diffuse, ulcerating nodules with rapid dissemination and systemic involvement; no specific site Usually solitary, erythematous nodules on face, neck, or upper trunk þ/ þ þ N/A Only subcutis involved; associated with autoimmune disorders (nearly 20%); lobular infiltration with septal sparing, adipocyte rimming; necrosis and granulomas common Variable þ þ þ /þ /þ Pautrier microabscesses, intraepidermal vesiculation, cerebriform nuclei, haloed lymphocytes Large /þ þ þ þ N/A Markedly atypical CD30 þ cells Medium large Small medium þ þ þ /þ Advanced clinical stage at presentation; significant immunophenotypic aberrations þ/ þ þ CD4 þ, follicular helper T-cell phenotype Ki-67 Frequently low (,10); some low moderate (,20) High Moderate high Varies with stage of disease High High Low to low moderate (5% 20%) Abbreviations: þ, positive;, negative; þ/, variable but more frequently positive; /þ, variable but more frequently negative; N/A, not available; PD- 1, programmed death-1; TCR, T-cell receptor. Arch Pathol Lab Med Vol 141, November 2017 Primary Cutaneous Acral CD8 þ T-Cell Lymphoma Hathuc et al 1473
6 Figure 4. Subcutaneous panniculitis-like T-cell lymphoma. A, CD5 showing diminished expression within the neoplastic cells. B, Granzyme highlighting a subset of the neoplastic cells. C, Lysozyme highlighting abundant histiocytes within areas of fat necrosis. D, Ki-67 showing a high proliferation index (original magnification 3200 [A]; original magnification 3200 [B]; original magnification 3200 [C]; original magnification 3100 [D]). CONCLUSIONS Correct diagnosis of primary cutaneous acral CD8 þ T-cell lymphoma is essential because the prognostic and therapeutic implications are distinct among other CD8 þ cytotoxic lymphoid proliferations. Aggressive epidermotropic cutaneous CD8 þ lymphoma and primary cutaneous peripheral T- cell lymphoma, not otherwise specified (NOS) warrant staging investigations and aggressive therapy. 3 In contrast, primary cutaneous acral CD8 þ T-cell lymphoma can be managed conservatively and tends to follow an indolent clinical course regardless of treatment modality. 4 Knowledge of the clinical setting and morphologic and immunophenotypic features can aid in correct diagnosis. References 1. Petrella T, Maubec E, Cornillet-Lefebvre P, et al. Indolent CD8-positive lymphoid proliferation of the ear a distinct primary cutaneous T-cell lymphoma? Am J Sur Pathol. 2007;31(12): Greenblatt D, Ally M, Child F, et al. Indolent CD8 þ lymphoid proliferation of acral sites: a clinicopathologic study of six patients with some atypical features. J Cutan Pathol. 2012;40(2): Wobser M, Roth S, Reinartz T, Rosenwald A, Goebeler M, Geissinger E. CD68 expression is a discriminative feature of indolent cutaneous CD8-positive lymphoid proliferation and distinguishes this lymphoma subtype from other CD8- positive cutaneous lymphomas. Br J Dermatol. 2015;172(6): Kluk J, Kai A, Koch D, et al. Indolent CD8-positive lymphoid proliferation of acral sites: three further cases of a rare entity and an update on a unique patient. J Cutan Pathol. 2015;43(2): Kempf W, Kazakov DV, Cozzio A, et al. Primary cutaneous CD8 þ small- to medium-sized lymphoproliferative disorder in extrafacial sites. Am J Dermatopathol. 2013;35(2): Swerdlow SH, Campo E, Pileri SA, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood. 2016;127(20): Magro CM, Crowson AN, Mihm MC. The Cutaneous Lymphoid Proliferations: A Comprehensive Textbook of Lymphocytic Infiltrates of the Skin. Hoboken, NJ: John Wiley & Sons Inc.; Cerroni L. Skin Lymphoma: The Illustrated Guide. Chichester, England: Wiley Blackwell; Wobser M, Petrella T, Kneitz H, et al. Extrafacial indolent CD8-positive cutaneous lymphoid proliferation with unusual symmetrical presentation involving both feet. J Cutan Pathol. 2013;40(11): Jaffe ES, Arber DA, Campo E, Harris NL, Quintanilla-Martinez L. Hematopathology. Philadelphia, PA: Elsevier; Goodlad J. Indolent CD8-positive lymphoid proliferation of acral sites: identifying the sheep in wolf s clothing [comment]. Br J Dermatol. 2015;172(6): Swick BL, Baum CL, Venkat AP, Liu V. Indolent CD8 þ lymphoid proliferation of the ear: report of two cases and review of the literature. J Cutan Pathol. 2010;38(2): Arch Pathol Lab Med Vol 141, November 2017 Primary Cutaneous Acral CD8 þ T-Cell Lymphoma Hathuc et al
7 13. Beltraminelli H, Mullegger R, Cerroni L. Indolent CD8 þ lymphoid proliferation of the ear: a phenotypic variant of the small-medium pleomorphic cutaneous T-cell lymphoma? J Cutan Pathol. 2010;37(1): Lecamwasam K, Mathew B, Gilson D, Burton C, Laws P. Correspondence article regarding CD68 as a marker of CD8 þ lymphoid proliferation suggested by Wobser, et al. Br J Dermatol. 2016;174(5): Tomasini D, Berti E. Subcutaneous panniculitis-like T-cell lymphoma. G Ital Dermatol Venereol. 2013;148: Beltraminelli H, Leinweber B, Kerl H, et al. Primary cutaneous CD4 þ 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(4): Lan TTH, Brown NA, Hristov AC. Controversies and considerations in the diagnosis of primary cutaneous CD4 small/medium T-cell lymphoma. Arch Pathol Lab Med. 2014;138(10): Takeshita M, Okamura S, Oshiro Y, et al. Clinicopathologic differences between 22 cases of CD56-negative and CD56-positive subcutaneous panniculitis-like lymphoma in Japan [published correction appears in Hum Pathol. 2004;35(3):388].Hum Pathol. 2004;35(2): Bekkenk MW. Peripheral T-cell lymphomas unspecified presenting in the skin: analysis of prognostic factors in a group of 82 patients. Blood. 2003;102(6): Dewar R, Andea AA, Guitart J, Arber DA, Weiss LM. Best practices in diagnostic immunohistochemistry: workup of cutaneous lymphoid lesions in the diagnosis of primary cutaneous lymphoma. Arch Pathol Lab Med. 2015;139(3): Diamantidis MD, Myrou AD. Perils and pitfalls regarding differential diagnosis and treatment of primary cutaneous anaplastic large-cell lymphoma. ScientificWorldJournal. 2011;11: Dummer R, Michie SA, Kell D, et al. Expression of bcl-2 protein and Ki-67 nuclear proliferation antigen in benign and malignant cutaneous T-cell infiltrates. J Cutan Pathol. 1995;22(1): Hsu Y-J, Su L-H, Hsu Y-L, Tsai T-H, Hsiao C-H. Localized lymphomatoid papulosis. J Am Acad Dermatol. 2010;62(2): James E, Sokhn JG, Gibson JF, et al. CD4 primary cutaneous small/ medium-sized pleomorphic T-cell lymphoma: a retrospective case series and review of literature. Leuk Lymphoma. 2014;56(4): Merrill ED, Agbay R, Miranda RN, et al. Primary cutaneous T-Cell lymphomas showing gamma-delta (cd) phenotype and predominantly epidermotropic pattern are clinicopathologically distinct from classic primary cutaneous cd T-Cell lymphomas. Am J Sur Pathol. 2017;41(2): 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 Haematopathology Workshop. Am J Clin Pathol. 2013;139(4): Robson A, Assaf C, Bagot M, et al. Aggressive epidermotropic cutaneous CD8 lymphoma: a cutaneous lymphoma with distinct clinical and pathological features: report of an EORTC Cutaneous Lymphoma Task Force Workshop. Histopathology. 2015;67(4): Sxen F, Rassidakis GZ, Jones D, Medeiros LJ. Apoptosis and proliferation in subcutaneous panniculitis-like T-cell lymphoma. Mod Pathol. 2002;15(6): Willemze R. WHO-EORTC classification for cutaneous lymphomas. Blood. 2005;105(10): Willemze R, Meijer CJLM. Classification of cutaneous T-cell lymphoma: from Alibert to WHO-EORTC. J Cutan Pathol. 2006;33(S1): Wood GS, Strickler JG, Deneau DG, Egbert B, Warnke RA. Lymphomatoid papulosis expresses immunophenotypes associated with T cell lymphoma but not inflammation. J Am Acad Dermatol. 1986;15(3): Friedmann D. Primary cutaneous pleomorphic small T-cell lymphoma. Arch Derm. 1995;131(9):1009. Arch Pathol Lab Med Vol 141, November 2017 Primary Cutaneous Acral CD8 þ T-Cell Lymphoma Hathuc et al 1475
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