Angioimmunoblastic T-cell lymphoma
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1 Unusual Presentation of Angioimmunoblastic T-cell Lymphoma as a Solitary Lymph Node N Ashalatha*, BN Kumarguru, BS Dayananda, AH Nagarajappa # Abstract Introduction: Angioimmunoblastic T-cell lymphoma (AITL) is an aggressive subtype of peripheral T-cell lymphoma (PTCL) characterized by systemic disease. It is a rare subtype of non-hodgkin s lymphomas. However, it forms a major subset of PTCL. Lymph node is the primary site of disease and virtually all patients present with generalized lymphadenopathy. Case report: A 42-year-old male presented with fever of short duration and a solitary axillary lymph node swelling on the right side. Systemic examination revealed moderate ascites and hepatosplenomegaly. Hematological investigations showed pancytopenia and abnormal liver function. Axillary lymph node showed histological features suggesting AITL and was confirmed by a panel of immunohistochemistry (IHC). Conclusion: AITL presenting as solitary axillary lymph node enlargement is unusual. Such atypical presentation mandates careful clinical and laboratory evaluation. IHC is an effective ancillary tool for confirmation of diagnosis of this distinct clinicopathological entity. Keywords: Angioimmunoblastic T-cell lymphoma, peripheral T-cell lymphoma, non-hodgkin s lymphoma, solitary axillary lymph node enlargement, pancytopenia, immunohistochemistry Angioimmunoblastic T-cell lymphoma (AITL) is a peripheral T-cell lymphoma (PTCL) characterized by systemic disease, a polymorphous infiltrate involving lymph nodes with a prominent proliferation of endothelial venules and follicular dendritic cells (FDCs). Spleen, liver, skin and bone marrow are also frequently involved. 1 Though, it is one of the more common specific subtypes of PTCL, accounting for approximately 20% of cases, it constitutes only 1-2% of all non-hodgkin s lymphoma. 1,2 It occurs in the middle-aged and elderly with an equal incidence in males and females. 1 Originally described in 1974, as immunoblastic lymphadenopathy by Rappaport and Lukes, AITL is recognized in the current World Health Organization (WHO) classification *Assistant Professor Tutor Professor # Professor and Head Dept. of Pathology Bangalore Medical College and Research Institute, Bangalore, Karnataka Address for correspondence Dr N Ashalatha Assistant Professor Dept. of Pathology Victoria Hospital, Bangalore Medical College and Research Institute Bangalore , Karnataka drbnkg007@hotmail.com as a PTCL with distinct clinicopathologic features. 3 The postulated normal counterpart is CD4+ follicular helper T-cell (TFH). 1 This subset of T-cell is located at the boundary between the mantle zone and germinal center light zone and is supposed to provide help to germinal center B-cells during their terminal differentiation. 4 The patients present with generalized lymphadenopathy (up to 90%), hepatosplenomegaly (50-79%), cutaneous rash (50%), hypergammaglobulinemia (50%), pleural effusion (37%) and autoimmune phenomena (20%). 5 The laboratory findings include circulating immune complexes, cold agglutinins with hemolytic anemia, positive rheumatoid factor and antismooth muscle antibodies. Epstein-Barr virus (EBV)-positive cells are nearly always present. Characteristically, the neoplastic cells show phenotype of normal TFH expressing CD10, CXCL13 and PD1 in % of cases. 1 Cytogenetic and molecular studies have consistently shown clonal chromosomal abnormalities and monoclonal or oligoclonal T-cell populations in most cases, which strongly supports a T-cell neoplasm. 6 Patients with AITL have a poor prognosis with conventional treatment, with a median overall survival <3 years. Patients achieving a good clinical response seem to benefit from a consolidation with high-dose therapy and autologous stem cell transplantation Indian Journal of Clinical Practice, Vol. 24, No. 11, April 2014
2 Case Report A 42-year-old male presented with fever of 4 days duration and easy fatigability. General physical examination revealed a solitary lymph node in the right axilla measuring cm. No other lymph nodes were enlarged. Abdominal examination revealed moderate ascites, hepatomegaly and massive splenomegaly. Blood investigations were done. Hemoglobin was decreased (5.4 g/dl), leukocyte count was reduced (2,300 cells/mm 3 ), platelet count was reduced (62,000/mm 3 ). Peripheral smear also suggested pancytopenia. Coomb s test was negative. Bone marrow examination did not reveal any pathological findings. Human immunodeficiency virus (HIV) was negative and hepatitis B surface antigen (HBsAg) was nonreactive. Biochemical investigations showed increased levels of postprandial glucose (150 mg/dl), total proteins (11 g/dl), alkaline phosphatase (207 U/L) and lactate dehydrogenase (LDH) (693 U/L). Serum albumin was reduced (3.3 g/dl). Ultrasonography of abdomen showed moderate ascites mild hepatomegaly and massive splenomegaly. Considering these features the present case corresponds to Ann Arbor Stage III ES, International Prognostic Index (IPI) score of four and prognostic index for PTCL/unspecified (PIT) score of 2. The axillary node was excised and sent for histopathological examination. Grossly the lymph node measured cm. Cut section showed Figure 1. Photomicrograph of tissue section showing effacement of lymph node architecture (H&E, x40). Figure 2. Photomicrograph of lymph node section showing post-capillary venules lined by plump endothelial cells (arrows) (H&E, x400). Figure 3. Photomicrograph of lymph node section showing tumor cells having convoluted nuclear borders and prominent nucleoli and good number of mitotic figures (arrows) (H&E, x400). Figure 4. Photomicrograph of lymph node section showing background of reactive lymphocytes, eosinophils, plasma cells and histiocytes (H&E, x400). Indian Journal of Clinical Practice, Vol. 24, No. 11, April
3 Figure 5. Photomicrograph of lymph node section showing diffuse immunopositivity for CD3 neoplastic cells (IHC, x400). Figure 6. Photomicrograph of lymph node section showing diffuse immunopositivity for CD10 neoplastic cells (IHC, x200). Figure 7. Photomicrograph of lymph node section showing scattered immunopositivity for CD30 neoplastic cells (IHC, x 400). Figure 8. Photomicrograph of lymph node section showing CD20+ reactive residual B-cells (IHC, x200). homogeneous grey-white appearance. Sections from the lymph node showed effacement of architecture and follicular depletion (Fig. 1). Prominent arborising postcapillary venules lined by plump endothelial cells were seen (Fig. 2). Clusters of tumor cells having vesicular nuclei and prominent nucleoli, showed vaguely convoluted borders, clear to pale cytoplasm and mitotic figures (Fig. 3). Mature lymphocytes, plasma cells, histiocytes and significant number of eosinophils were also seen in the background of patchy hyaline material (Fig. 4). Immunohistochemistry (IHC) was performed, which showed neoplastic cells as diffusely distributed CD3+ cells (Fig. 5) and CD10+ cells (Fig. 6). CD30+ cells were scattered and comparatively scant (Fig. 7). Residual reactive B lymphocytes were CD20+ (Fig. 8). These findings confirmed the histological diagnosis of AITL. Discussion AITL is a rare and complex lymphoproliferative disorder, clinically characterized by widespread lymphadenopathy, extranodal disease, immune-mediated hemolysis and polyclonal hypergammaglobulinemia. 3 It represents a distinct clinicopathological entity among nodal PTCLs. 4 AITL is a systemic disease involving lymph nodes, spleen and bone marrow. 6 AITL was first described by Ree et al who reported progression of two such cases into typical AITL. 6 It is an aggressive PTCL whose natural history is poorly understood. 5 Mourad et al 4 recorded the median age of 62 years while Cho et al 7 recorded the median age of 58.5 years in their studies. AITL occurs in middle-aged and elderly with an equal incidence in males and females. 1 Rodriguez-Justo et al 5 and Attygalle et al 6 observed 1040 Indian Journal of Clinical Practice, Vol. 24, No. 11, April 2014
4 occurrence of AITL in middle-aged and elderly with male preponderance. Lymph node is the primary site of disease and virtually all patients present with generalized lymphadenopathy. 1,3,5,6 Cho et al 7 recorded generalized lymphadenopathy as commonest presentation (91%) in their study. In contrast, the middle-aged patient in the present case presented with solitary right axillary lymph node. Lymph node enlargement was accompanied by an episode of fever and easy fatigability. Rodriguez- Justo et al 5 observed organomegaly (hepatomegaly or splenomegaly) in 33% of cases. Attygalle et al 6 and Cho et al 7 also observed hepatosplenomegaly in their studies. Mourad et al 4 observed pleural effusion or ascities or edema in 16% of cases in their study. Even in the present case, the patient had hepatosplenomegaly, deranged liver function and ascities. Most of the cases present at an advanced stage (III-IV). 2,4,5 Peripheral blood picture suggested pancytopenia. However, bone marrow did not show tumor infiltration and Coomb s test was negative. Thirty-three percent of cases had hemolytic autoimmune anemia in study conducted by Rodriguez-Justo et al. 5 Mourad et al 4 recorded anemia in 65% of cases and positive Coomb s test in 33% of cases. Rodriguez-Justo et al 5 and Cho et al 7 observed bone marrow involvement in 22% cases and 70% cases in their studies. Mourad et al 4 observed bone marrow involvement in 38% of anemic patients. Serum lactate dehydrogenase (LDH) level was elevated in the present case. Similar elevations of serum LDH were noted in studies conducted by Mourad et al 4 and Cho et al. 7 Mourad et al 4 considered five criteria for histological diagnosis: Partial or diffuse effacement of the nodal architecture, vascular proliferation with prominent arborization of high endothelial venules, extrafollicular meshwork of FDCs, atypical population of CD3+ T-cells and large CD20+ B-cells. Similar criteria were considered in the present case. But CD20+ B-cells were present as reactive residual component of the lesion. The constellation of microscopic features of this case corresponded with pattern II of AITL described by Attygalle et al. 6 In the present case, neoplastic cells were diffusely positive for CD3 and CD10. CD30+ cells showed scattered positivity and were comparatively scant. CD20+ cells represented reactive residual B-cells. Mourad et al 4 observed that neoplastic cells were CD3 in 100% cases and CD10 in 71% cases in their study. Cho et al 7 noted that CD3 and CD5 were strongly positive and aberrant expression of CD10 was observed in 65% of cases. Attygalle et al 6 observed that CD10 identified the tumor cells in 90% of AITL. In contrast, Rodriguez-Justo et al 5 observed that only small proportion of neoplastic cells (5-10%) expressed CD10. CD30 staining was done in only three cases and was positive in all the three cases. 5 The etiology and pathogenesis of AITL are unknown. In a high percentage of cases the diagnosis is preceded by allergic reactions, infections and/or exposure to drugs, particularly antibiotics. 2 EBV and Human herpes virus (HHV6 and HHV8) may play a role in pathogenesis of AITL and this might explain its response to antiviral therapy with valacyclovir. 5 Although, it has not been thoroughly investigated, it was suggested that the increase in T-cell immunoblasts would indicate transformation into a PTCL/unspecified. An increase in EBV infected B-cells may also occur and in rare cases, an overt diffuse large B-cell lymphoma develops. 4 The physiologic role of CD10 is thought to involve hydrolysis of polypeptides such as inflammatory mediators in the extracellular milieu. Expression of CD10 may regulate apoptosis by interfering with negative or positive signals present in the extracellular environment. It is possible that aberrant CD10 expression in neoplastic T-cells in AITL may be an indicator of disturbed apoptotic cell death. 6 Interestingly, it has been suggested that production of interleukin-21 by TFH is responsible for B-cell activation and hypergammaglobulinemia seen in AITL. 5 It has been recently shown that CXCL13, a chemokine critically involved in B-cell migration into germinal centers, was highly upregulated in the TFH subset. 4 It was hypothesized that the clinical effects of AITL are due to marked dysregulation of the immune system rather than to direct complications of tumor growth. 4 Peculiar histologic features of AITL, where tumor cells are greatly outnumbered by the surrounding reactive cells and found in intimate contact with the expanding meshwork of FDCs. Hence, AITL can be considered as an immunologically functional disease in which the clinical behavior is determined by the resultant cross-talk between the malignant cells and the immunologic microenvironment. 4 T-cell receptor genes show clonal rearrangement in 75-90% of cases. Clonal immunoglobulin gene rearrangement may be found in 25-30% cases. Trisomy 3 and 5 and an additional X-chromosome are the most frequent cytogenetic abnormalities detected in AITL. 1,2 Conclusion Solitary axillary lymph node enlargement is an unusual presentation of AITL. In view of such Indian Journal of Clinical Practice, Vol. 24, No. 11, April
5 atypical presentation and taking into consideration the aggressive nature of this distinct clinicopathological entity, careful clinical and laboratory evaluation is necessary. Immunophenotyping serves as an effective auxiliary weapon for the confirmation of diagnosis. Acknowledgment We sincerely thank Dr Clementina Ramarao, Professor of Pathology, Kidwai Institute of Medical Oncology, Bangalore for the kind cooperation extended to us for diagnosing this rare entity. References 1. Dogan A, Gaulard P, Jaffe ES, et al. Angioimmunoblastic T-cell lymphoma. In: World Health Organization Classification of Tumors of Haematopoietic and Lymphoid Tissues. 4th edition, Campo E, Harris NL, Jaffe ES, et al (Eds.). Swerdlow SJ. IARC Press: Lyon 2008:p Iannitto E, Ferrari AJ, Minardi V, Tripodo C, Kreipe HH. Angioimmunoblastic T-cell lymphoma. Crit Rev Oncol Hematol 2008;68(3): Alizadeh AA, Advani RH. Evaluation and management of angioimmunoblastic T-cell lymphoma: a review of current approaches and future strategies. Clin Adv Hematol Oncol 2008;6(12): Mourad N, Mounier N, Brière J, Raffoux E, Delmer A, Feller A, et al; Groupe d Etude des Lymphomes de l Adulte. Clinical, biologic, and pathologic features in 157 patients with angioimmunoblastic T-cell lymphoma treated within the Groupe d Etude des Lymphomes de l Adulte (GELA) trials. Blood 2008;111(9): Rodriguez-Justo M, Attygalle AD, Munson P, Roncador G, Marafioti T, Piris MA. Angioimmunoblastic T-cell lymphoma with hyperplastic germinal centres: a neoplasia with origin in the outer zone of the germinal centre? Clinicopathological and immunohistochemical study of 10 cases with follicular T-cell markers. Mod Pathol 2009;22(6): Attygalle A, Al-Jehani R, Diss TC, Munson P, Liu H, Du MQ, et al. Neoplastic T cells in angioimmunoblastic T-cell lymphoma express CD10. Blood 2002;99(2): Cho YU, Chi HS, Park CJ, Jang S, Seo EJ, Huh J. Distinct features of angioimmunoblastic T-cell lymphoma with bone marrow involvement. Am J Clin Pathol 2009;131(5): Alprolix Approved by US FDA for Hemophilia B The US Food and Drug Administration (FDA) has recently approved the first long-lasting recombinant coagulation factor IX product, Alprolix, for use in children and adults with hemophilia B. The drug will help control and prevent bleeding episodes, manage bleeding during surgical procedures and prevent or reduce the frequency of bleeding episodes. The FDA stated that this is the first hemophilia B treatment that requires less frequent injections when used to prevent or diminish the frequency of bleeding. Supporting previous reports linking arterial stiffness to the amount of β-amyloid (Aβ) present in the brain of nondemented elderly patients, a new study has reported that arterial stiffness is also strongly associated with the accumulation of AΒ over almost 2 years in these adults. The study is published online March 31 in JAMA Neurology. The study included participants from the Pittsburgh site of the Ginkgo Evaluation of Memory Study (GEMS). At baseline 48% of 91 participants were AΒ positive, 75% of these participants were Aβ positive at follow-up. Imatinib Facilitates Allogeneic Transplant in Ph+ ALL The routine incorporation of a tyrosine kinase inhibitor (TKI), such as imatinib, into the initial treatment of patients with Philadelphia chromosome positive acute lymphoblastic leukemia (Ph+ ALL) has improved clinical outcomes such that some have questioned the need for routine allogeneic hematopoietic cell transplantation (allo-hct) in this population. An analysis of a large prospective intergroup trial evaluated the outcomes of patients with Ph+ ALL treated with induction chemotherapy before and after a protocol amendment to incorporate imatinib [1]. Although imatinib resulted in a higher complete remission rate and superior overall survival at four years, the survival benefit appeared to reflect the ability of patients taking imatinib to maintain complete remission long enough to proceed with allo-hct, supporting the approach of imatinib followed by allo-hct. Further studies are needed to determine whether allo-hct can be omitted in a subset of patients with Ph+ ALL, such as those who achieve a rapid response with no detectable minimal residual disease. ( Indian Journal of Clinical Practice, Vol. 24, No. 11, April 2014
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