ECP meeting, Lisbon, september 2012 Slide seminar New and old challenges in the diagnosis of peripheral T-cell lymphomas
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1 ECP meeting, Lisbon, september 2012 Slide seminar New and old challenges in the diagnosis of peripheral T-cell lymphomas Philippe Gaulard, Dept of Pathology, INSERM U955, Hôpital Henri Mondor, Créteil, France philippe.gaulard@hmn.aphp.fr Case 2: Case history: A 60-year-old woman Caucasian presented with waxing and waning lymphadenopathies measuring up to 3.5 cm. She had no B symptoms. A first lymph node biopsy was considered suspicious for a lymphoma but without definitive diagnosis. Persistent generalized lymphadenopathies resulted in a second lymph node biopsy in the occipital region. Staging with CT scan disclosed multiple adenopathies without hepatosplenomegaly. The bone marrow biopsy did not show tumor involvement. Biological tests were unremarkable: blood cell counts were normal without lymphocytosis, LDL level was normal and there was no hypergammaglobulinemia. Coombs test was negative The lymph nodes spontaneously regressed and the patient was followed for 4 years without therapy. Two episodes of recurrent adenopathies occurred : relapses with similar pathological features in two lymph node biopsies were documented. Four years after initial diagnosis, she relapsed again with multiple adenopathies and B symptoms. A lymph node biopsy was performed and polychemotherapy was started. The images are from the second lymph node biopsy. Histologic and phenotypic findings - The lymph node was significantly enlarged. On histopathology, its architecture appeared effaced by irregular large nodules without germinal centers, composed of small mature lymphocytes. Ill-defined aggregates or clusters or small to medium-sized cells with more or less irregular nuclei are dispersed within the nodules. These slightly atypical cells showed an abundant clear cytoplasm. A few large cells (immunoblasts) were seen. A few hyperplastic veinules were present in the internodular areas. Overall, there were neither eosinophils nor plasma cells.
2 - Immunohistochemistry performed on paraffin-embedded material was essential for the diagnosis, helping to identify an atypical T-cell population with a peculiar phenotypic profile and a peculiar preferential distribution within B-cell nodules. 1) The nodules were composed of a majority of small CD20+, CD79a+ IgD+ small B- cells (mantle cells); to note, these B-cell follicles contained CD20-negative areas; 2) These CD20-negative areas corresponded to aggregates or sheets (sometimes mimicking reactive germinal centers) of atypical T cells, with small to medium-sized more or less irregular nuclei, better emphasized by CD3 and CD5 stainings; they had the following phenotype: - CD3+, CD5+, CD2+, CD7-; - CD4+, CD8-; - CD10+, bcl-6+ (weak), CD57- - with expression of the TFH markers CXCL13 and PD1. 3) A few large EBV-infected CD20+, CD79a+, CD30+/- B-blasts were present. These B- blasts were surrounded by the atypical CD3+, PD1+, CXCL13+ T cells forming rosettes. Molecular findings - PCR studies for TCR-γ chain gene rearrangement performed on DNA extracted from the lymph node disclosed a clonal T-cell population. The same T-cell clone was observed in 3 subsequent biopsies. - EBV was negative both by immunohistochemistry (LMP-1) ; by in situ hybridization, rare scattered large cells (most likely the B-blasts) were observed. - FISH study for translocation t(5;9) using probes for ITK and SYK did not evidence rearrangements of ITK- SYK. Cytogenetics - Conventional cytogentics: 46,XX, dup (3) (q21;q26), add(19) (q13.3à (in 2 subsequent biopsies) - FISH study for translocation t(5;9) using probes for ITK and SYK did not evidence rearrangements of ITK- SYK. Diagnosis:
3 Peripheral T-cell lymphoma, not otherwise specified, follicular variant Discussion 1 - Peripheral T-cell lymphomas, not otherwise specified (PTCL, NOS), reported as the most common PTCL entity, is defined by default for cases not fulfilling the criteria for more «specific» entities, and de facto the most heterogeneous entity. Presentation is usually nodal but can affect any site. The median age of patients is in the seventh decade, and 65% of the patients have stage IV disease. The patients have an overall poor outcome (20-30% 5-year survival). Morphology is highly variable. PTCL, NOS typically contain a mixture of small and large atypical pleomorphic cells expressing CD3 with frequent loss of T-cell antigens, most often CD7. Most cases are CD4+CD8-. A few morphological variants are recognized. These include the rare lymphoepithelioid variant (also designated Lennert s lymphoma) of PTCL, NOS, characterized by an abundant background of histiocytes, made of neoplastic small CD8+ cytotoxic T cells, and the also rare - group of PTCL with a follicular pattern designated as follicular variant of PTCL, NOS (F-PTCL). 2 Cases of PTCL with a follicular pattern - ie a pattern of growth intimately related to follicular structures - have been recently reported. They may show a truly follicular pattern, mimicking follicular lymphoma, a perifollicular growth pattern mimicking marginal zone lymphoma or may involve expanded mantle zones or large primary follicles, resembling progressive transformation of germinal centers. The neoplastic cells are CD3+ CD4+ αβ T cells expressing T FH markers (PD1+ ICOS+ CXCL13+ BCL6+, CD10 +/- CD57-/+), therefore indicating that both this variant and angioimmunoblastic T-cell lymphoma (AITL) share a common cell of origin from follicular helper T cells (T FH) cells. F-PTCL may show overlapping clinical and pathological features with AITL, in particular the presence of EBVpositive B-cell blasts that may have Reed-Sternberg-like features (and therefore mimic classical Hodgkin lymphoma). Therefore a relationship to AITL is questionable, also supported by the observation that patients with F-PTCL may present with recurrent lesions as AITL and vice-versa. A chromosomal translocation t(5;9)(q33;q22) involving ITK and SYK tyrosine kinase, is found in about 20% of F-PTCL and yet has been rarely reported in other T- cell lymphoma entities. It has been shown that ITK-SYK has transforming properties in vitro, and induces a T-cell lymphoproliferative disease in mice resembling human PTCL through a signal that mimics activation of the TCR. Clinical presentation seems variable from case to
4 case. As in the current case, some F-PTCL have been reported to have a more localized disease at presentation without B symptoms and a more indolent outcome whereas most cases seems to be characterized with more disseminated disease and features close to other PTCL,NOS, sometimes with features more specific for AITL (skin manifestations, hypergammaglobulinemia). Overall, there is more evidence that F-PTCL may not be a distinct entity but may represent part of the spectrum of AITL. The reason why in most cases the neoplastic T FH cells spread outward in an inter/perifollicular distribution (AITL) and in a small minority remain predominantly within follicles (folliculotropic) (PTCL-F) remains to be clarified.. 3 Whatever their relationship with other PTCL entities is, the peculiar histologic appearances of F-PTCL generates a list of differential diagnoses. PTCL with follicular growth patterns should be distinguished from reactive conditions, some B-cell lymphomas and Hodgkin lymphomas. At low power magnification, they could be mistaken at least in some cases - as a follicular lymphoma. Follicles in both diseases have decreased numbers of tingible body macrophages, attenuated mantle / marginal zones, and neoplastic cells could be both BCL6 and CD10 positive. Lack of cytologic characteristics of centrocytes, abundant clear cytoplasm, and expression of T-cell markers in addition to T FH antigens such as CXCL13 and PD-1 argue for a diagnosis of PTCL. In other cases, irregular nodules in the background or diffuse infiltrates should be distinguished from progressive transformation of germinal centers or nodular lymphocyte predominance Hodgkin lymphoma and other small B-cell lymphomas such as mantle cell lymphomas and marginal zone lymphomas. The abnormal T-cell phenotype together with the expression of T FH markers in abnormal cells and salient morphology of background B cell infiltrates could help in making a correct diagnosis. However, it must be emphasized that presence of activated T cells with the phenotype of T FH cells is common in nodular lymphocyte predominance Hodgkin lymphoma as well as it may be seen in classical Hodgkin lymphoma and this should not be regarded alone as a diagnostic criteria. Since presence of EBV+ or more rarely EBV-negative B-blasts that can show RS-like features has been reported in some cases, the diagnosis with classical Hodgkin lymphoma, especially in the lymphocyte-rich variant might be confusing; in these circumstances, attention should be paid to the phenotype of the T-cell population and integration with the clinical and biological features is important. Finally, in some cases like the present observation, the morphology with presence of follicles and some paracortical
5 expansion can be easily missed as a reactive process. The presence of aggregates of atypical medium-sized T cells within the follicles suggest the possibility of a neoplastic disease. Demonstration of an aberrant phenotype, CD10 expression and T FH markers are useful to highlight the presence of aggregates of atypical T cells into hyperplastic follicles. Demonstration of a clonal T-cell population is of value, almost when the same clonal population is found in subsequent biopsies and/or different sites as in the current case. Legends to figures Histopathology of the lymph node (H&E staining) (figures 1 to 3): -Figure 1 The architecture of the lymph node is effaced with a vague nodular growth pattern without reactive germinal centers; to note, presence of some scattered pale areas Fig 2a and 2b: at a higher power, these pale areas contain aggregates of slightly atypical small to medium-sized cells with slightly abundant pale cytoplasm. A few larger cells are present. - Figure 3 : Immunohistochemistry of the lymph node. presence within B-cell follicles of sheets or aggregates of atypical CD3+ T cells with some irregular nuclei (a), that lack CD7 b), and disclose expression of CD10 (c) and the TFH marker PD1 (d). References Attygalle A, Cabeçadas J, Gaulard P, et al: Peripheral T- and NK-cell lymphomas and their mimics: taking a step forward - Report on the Lymphoma Workshop of the XVI meeting of the European Association for Haematopathology in Lisbon Histopathology in press, 2013 de Leval L, Savilo E, Longtine J, et al: Peripheral T-cell lymphoma with follicular involvement and a CD4+/bcl-6+ phenotype. Am J Surg Pathol 25: , 2001 de Leval L, Rickman DS, Thielen C, et al: The gene expression profile of nodal peripheral T- cell lymphoma demonstrates a molecular link between angioimmunoblastic T-cell lymphoma (AITL) and follicular helper T (TFH) cells. Blood 109: , 2007 Dupuis, J., K. Boye, et al. (2006). "Expression of CXCL13 by neoplastic cells in angioimmunoblastic T-cell lymphoma (AITL): a new diagnostic marker providing evidence that AITL derives from follicular helper T cells." Am J Surg Pathol 30(4): Gaulard P, de Leval L: Follicular helper T cells: implications in neoplastic hematopathology. Semin Diagn Pathol 28:202-13, 2011 Hatano, B., T. Fukushima, et al. (2002). "Peripheral T-cell lymphoma with a nodular growth pattern." Pathol Int 52(5-6): Huang Y, Moreau A, Dupuis J, et al: Peripheral T-cell lymphomas with a follicular growth pattern are derived from follicular helper T cells (TFH) and may show overlapping features with angioimmunoblastic T-cell lymphomas. Am J Surg Pathol 33:682-90, 2009 Ikonomou, I. M., A. Tierens, et al. (2006). "Peripheral T-cell lymphoma with involvement of the expanded mantle zone." Virchows Arch 449(1):
6 Jiang, L., D. Jones, et al. (2005). "Peripheral T-cell lymphoma with a "follicular" pattern and the perifollicular sinus phenotype." Am J Clin Pathol 123(3): Moroch J, Copie-Bergman C, de Leval L, et al: Follicular peripheral T-cell lymphoma expands the spectrum of classical Hodgkin lymphoma mimics. Am J Surg Pathol 36: , 2012 Nicolae A, Pittaluga S, Venkataraman G, et al: Peripheral T-cell lymphomas of follicular T- helper cell derivation with Hodgkin/Reed-Sternberg cells of B-cell lineage: both EBVpositive and EBV-negative variants exist. Am J Surg Pathol 37:816-26, 2013 Pechloff K, Holch J, Ferch U, et al: The fusion kinase ITK-SYK mimics a T cell receptor signal and drives oncogenesis in conditional mouse models of peripheral T cell lymphoma. J Exp Med 207: , 2010 Rudiger, T., R. Ichinohasama, et al. (2000). "Peripheral T-cell lymphoma with distinct perifollicular growth pattern: a distinct subtype of T-cell lymphoma?" Am J Surg Pathol 24(1): Sohani AR, Jaffe ES, Harris NL, et al. Nodular lymphocyte-predominant hodgkin lymphoma with atypical T cells: a morphologic variant mimicking peripheral T-cell lymphoma. Am J Surg Pathol. 2011Nov;35(11): Streubel B, Vinatzer U, Willheim M, et al: Novel t(5;9)(q33;q22) fuses ITK to SYK in unspecified peripheral T-cell lymphoma. Leukemia 20:313-8, 2006 Swerdlow S, Campo E, Harris N, et al: WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Lyon, IARC Press, 2008 Uherova, P., C. W. Ross, et al. (2002). "Peripheral T-cell lymphoma mimicking marginal zone B-cell lymphoma." Mod Pathol 15(4):
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