T-cell/Histiocyte-Rich Large B-cell Lymphoma in Pediatric Patients: an Under-Recognized Entity?
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1 Available online at T-cell/Histiocyte-Rich Large B-cell Lymphoma in Pediatric Patients: an Under-Recognized Entity? Gabriela Gheorghe 1, Hemalatha G Rangarajan 2, Bruce Camitta 3, Annette Segura 1, Steven Kroft 4, and James F. Southern 1 1 Department of Pathology and Laboratory Medicine, Children s Hospital of Wisconsin, Medical College of Wisconsin, Milwaukee, WI, 2 Pediatric Hematology/ Oncology/ Blood and Marrow Transplant, Nationwide Children s Hospital, Columbus, OH, 3 Pediatric Hematology/ Oncology/ Blood and Marrow Transplant, Medical College of Wisconsin, Milwaukee, WI and 4 Department of Pathology, Medical College of Wisconsin, Milwaukee, WI, USA Abstract. T-cell/histiocyte-rich large B-cell lymphoma (THRLBCL) is a distinct subtype of diffuse large B-cell lymphoma (DLBCL) under-recognized in the pediatric population. A meticulous workup is necessary to avoid a misdiagnosis of nodular lymphocyte-predominant Hodgkin lymphoma (NLPHL) or classical Hodgkin lymphoma (HL). A strong degree of suspicion and an emphasis on immunohistochemical staining are required to reach the diagnosis. Few children with advanced stage disease have been described to date. We report two pediatric patients with high stage THRLBCL and highlight their clinical and pathological features. Keywords: T-cell/histiocyte-rich Large B-cell lymphoma, pediatric, Hodgkin lymphoma, Nodular Lymphocyte Predominant Hodgkin Lymphoma, bone marrow. This material was presented as a poster at the Society for Pediatric Pathology meeting Sept 3-5, 2010 Banff, Canada. 73 Introduction T-cell/histiocyte-rich large B-cell lymphoma (THRLBCL) is a type of diffuse large B-cell lymphoma (DLBCL) most commonly seen in adults and rarely reported in children [1,2]. THRLBCL is currently under-recognized in the pediatric population. A strong degree of suspicion is required to reach the diagnosis. This entity is characterized by a limited number of malignant B-cells in a background containing numerous benign T lymphocytes and variable numbers of histiocytes. It is often misdiagnosed as classical Hodgkin lymphoma (HL) or nodular lymphocytepredominant Hodgkin lymphoma (NLPHL). Compared to adults, children respond better to therapy and have a better prognosis. Here we describe two children with THRLBCL and highlight their clinico-pathological features. Address correspondence to Gabriela Gheorghe, M.D., Department of Pathology, Children's Hospital of Wisconsin, 9000 West Wisconsin Avenue Milwaukee, WI 53226, USA; phone: ; fax: ; e mail: ggheorghe@mcw.edu Materials and Methods Institutional records (electronic databases) at the Children s Hospital of Wisconsin were searched for all in-house cases with a diagnosis of THRLBCL rendered from Two patients were identified (Table 1). Material submitted for pathological examination including hematoxylin- and eosin-stained sections, and immunohistochemical stains were reviewed for both cases. Diagnosis was confirmed by applying the 2008 World Health Organization (WHO) Classification of Tumors of Hematopoietic and Lymphoid Tissues [3]. Clinical and imaging records were available and retrieved in both cases. The study was conducted after the Childrens Hospital of Wisconsin Institutional Review Board approved Project , entitled Pediatric T-cell/histiocyte-rich large B-cell lymphoma: An under-recognized entity? Case 1. A 15-year-old, previously healthy male presented with one month of progressive back pain and weakness in the lower extremities. He denied fever, weight loss, and night sweats. CBC was unremarkable, and LDH was high at 1140IU/l (normal values: /15/ by the Association of Clinical Scientists, Inc.
2 74 Table 1. Patient s characteristics. Case # Age/ Clinical Nodal-Extranodal Bone Preliminary Outcome Gender Symptoms Involvement Marrow Diagnosis Involvement 1 15/M Back pain Lymphadenopathy: Yes Hodgkin Complete remission Lower extremity -Axillary Lymphoma 3 years after weakness -Retroperitoneal initial diagnosis -Hepatic Liver involvement Extradural mass (T5) 2 17/F Weight loss Lymphadenopathy: No Hodgkin Complete remission Fatigue -Mediastinal (negative Lymphoma 10 years after Night sweats -Splenic bilateral initial diagnosis -Mesenteric bone marrow -Hepatic biopsies) Liver involvement IU/l). Clinical examination revealed signs of spinal cord compression. Magnetic resonance imaging (MRI) showed an extradural mass at T5-T6. X-ray computed tomography (CT) of the chest, abdomen, and pelvis revealed axillary and retroperitoneal adenopathy, multiple liver lesions, and splenomegaly. All lesions had positive uptake by positron emission tomography (PET). Dexamethasone was begun and the patient underwent emergent laminectomy with excision of the extradural mass. The patient was diagnosed with stage IV-A THRLBCL and was treated, as per Children's Oncology Group (COG) Protocol ANH01P1, with rituximab, prednisone, cyclophosphamide, cytosine arabinoside, doxorubicin, etoposide, and high-dose methotrexate. He remains in remission three years after completion of therapy. Case 2. A 17-year-old female presented with a fivemonth history of fatigue, weight loss, night sweats, and chest pain. CBC showed normal findings, and LDL was high at 780IU/l. A chest x-ray revealed a mediastinal mass. Further imaging showed multiple liver lesions with hepatic, splenic, and mesenteric adenopathy. A liver biopsy and an excisional biopsy of a mediastinal lymph node confirmed the diagnosis of THRLBCL. The patient was diagnosed with stage III-B THRLBCL and was treated, as per COG protocol 9317, with intravenous and intrathecal methotrexate, cyclophosphamide, intravenous cytosine arabinoside, vincristine, etoposide, ifosfamide, and doxorubicin. She remains in complete remission more than 10 years after therapy. Pathology findings. The two cases had similar pathological findings. Both cases showed diffuse lymphoid infiltration. The extradural mass (Figure 1) had a number of large atypical cells spread in the background of small lymphocytes. These atypical cells displayed large, lobulated nuclei with dispersed chromatin that were CD45+, CD20+, epithelial membrane antigen (EMA)+, CD3-, CD30-, and CD15-. The background cellular infiltrate showed numerous benign CD3+ T lymphocytes intermixed with few histiocytes. Large collections of histiocytes were not seen. CD21 showed absence of a dendritic cell meshwork, confirming the diffuse nature of the process. Only rare cells were CD57+. Bone marrow examination showed extensive involvement by a malignant process composed of similar large atypical cells in a background of benign T lymphocytes and few histiocytes. CSF was normal. The liver mass (Case 2) showed findings similar to those described in Case 1 and was negative for EMA. BM and CSF were negative for disease. Standard cytogenetics were performed on the epidural mass (Case 1) and showed a normal male karyotype. Cytogenetic studies on the periaortic lymph node (Case 2) revealed 19 cells with normal chromosomal counts and two that were tetraploid without consistent abnormalities. Molecular studies (IgH, TCR gene rearrangements) were not performed in any of the cases. Discussion According to WHO 2008 classification, THRLBCL is currently considered a distinctive pathological entity distinguished by a limited number of atypical/malignant large B-lymphoid cells in a background of abundant reactive T lymphocytes and variable numbers of histiocytes [3]. The true
3 T Cell Histiocyte Rich Large B Cell Lymphoma in Pediatric Patients: an Under Recognized Entity? 75 Diagnosis is occasionally challenging since it may be confused with NLPHL and HL (particularly mixed cellularity type), peripheral T-cell lymphomas, and reactive processes [2,8,11-13]. NLPHL transforming into THRLBCL has been reported [3]. Cases with overlapping features between THRLBCL and NLPHL have been described and are diagnostically challenging [14]. incidence is unknown but is considered to be less than 10% of DLBCL cases [4]. Historically, seven cases were first described by Mirchandani et al in 1985 [5]. Ramsay et al coined the term T-cell rich B-cell lymphoma in 1988 [6]. The WHO proposed the designation of T-cell-rich large B-cell lymphoma was proposed in 2001, but it was still considered a histological variant of DLBCL [7]. THRLBCL tends to occur in younger adult males [3,17]. Rare cases have been observed in children [1,2,18]. Advanced-stage disease, extra-nodal involvement, and B symptoms were more frequently observed in reported adults and children in contrast to other types of DLBCL [1,3,12-13,15-17]. In contrast, cases of NLPHL are usually at a lower stage at diagnosis, with most pediatric patients presenting with isolated cervical or inguinal lymphadenopathy. Although pediatric NLPHL tends to occur predominantly in adolescents, rare cases are also reported in smaller children. We (S. Gupta et al) recently published a report on a 5-year-old patient with NLPHL who eventually developed lung involvement by NLPHL and coexistent mycobacterium avium intracellulare [22]. Figure 1. MRI of the spine with paraspinal mass. Pathology from the paraspinal mass showed a proliferation of large atypical cells which are CD45+, C20+ and EMA+ in a background containing numerous CD3+ lymphocytes and many histiocytes. There is extensive BM involvement (large atypical cells in the BM highlighted by PAX5).
4 76 Table 2. Differential diagnosis with NLPHL and Classical HL. THRLBCL NLPHL Classical Hodgkin Lymphoma Morphology Centroblasts, immunoblasts, LP ( popcorn ) cells. Reed Sternberg cells and LP cells variants Immunophenotype: CD CD /+ CD CD /- EMA +/- +/- - BOB OCT Architecture Diffuse (most cases) Nodular (most cases) No follicular dendritic No follicular dendritic Expanded follicular cell meshworks cell meshworks dendritic cell meshworks as assessed by CD21/CD23 EBV association No EBV association No EBV association Common EBV association Cases of NLPHL in children are rare, and a benign clinical course is expected in most cases. Recurrences may be common. Accurate diagnosis of THRLBCL depends on careful immunohistochemical analysis of tumor cells and the inflammatory microenvironment [4,9]. In the Children s Cancer Group (CCG-5961) study, immunophenotyping contributed to recognition and accurate diagnosis in most cases [1]. A panel of immunostains to include CD45, CD20, CD3, CD30, and CD15 should distinguish THRLBCL from HL in the majority of cases. BOB1 and OCT 2 (which are negative in classical HL but positive in THRLBCL and NLPHL) are currently being used to confirm the diagnosis in most difficult cases. Bcl- 6 and Bcl-2 are positive in THRLBCL and frequently negative in classical HL. The background cellular infiltrate is extremely helpful in differential diagnosis with classical HL. Most cases of HL have a milieu composed of a significant number of small lymphocytes and other inflammatory cells, including eosinophils, neutrophils, and plasma cells. This inflammatory milieu is distinctly uncommon in THRLBCL. Positive staining by in situ hybridization of Epstein Barr Virus (EBV), encoded nuclear RNA (EBER) favors HL. Neither of our cases were EBER-positive. Another valuable marker is EMA. EMA positivity in the large atypical cells essentially rules out classical Hodgkin lymphoma. EMA was positive only in Case 1. Distinguishing THRLBCL from NLPHL can be challenging. The architectural background in NLPHL is composed of expanded follicular dendritic cell meshworks filled with a mixture of B lymphocytes and CD4+/CD57+ T lymphocytes. In contrast, the large majority of THRLBCL cases have no residual dendritic cell meshwork. Unlike NLPHL cases, most cases of THRLBCL have a diffuse rather than nodular pattern of involvement. The presence of residual meshwork of follicular dendritic cells as assessed by dendritic cell markers (CD21, CD23 and/or CD35) along with increased number of activated T cells (as assessed by CD57) favors NLPHL. Rare cases of diffuse variant of NLPHL have been reported and are virtually indistinguishable from THRLBCL. Some experts think that NLPHL and THRLBCL likely represent a spectrum of the same disease process. Marafioti et al reported that leukocyte-specific phosphoprotein 1 (LSP-1) and the B-cell transcriptional factor PU.1 are two useful markers for distinguishing THRLBCL from NLPHL [21]. However, these markers are not commonly used in clinical practice.
5 T Cell Histiocyte Rich Large B Cell Lymphoma in Pediatric Patients: an Under Recognized Entity? 77 Table 2 shows the differences between THRLBCL, NLPHL, and classical HL. In the CCG 5961 study of 86 children with NHL, Lones found 20 cases (23%) of DLBCL and six cases (7%) of THRLBCL [1]. All patients with THRLBCL were males aged years. Three patients were stage III; none had BM or CNS disease. All cases were diagnostic problems at presentation, including three initially suspected to be HL. Tiemann et al identified 16 children with THRLBCL in their review [2]. Only one patient had BM involvement (stage IV) at diagnosis. Four patients were stage III. Two patients were misdiagnosed and treated as NLPHL with BFM HD95; both relapsed. One was rescued by an autologous stem cell transplant (ASCT), while the other died due to recurrent disease. The remaining patients were treated as per NHL-BFM 95. At a median follow-up of 23 months the event-free survival (EFS) was 86% and overall survival (OS) was 94%. THRLBCL appears to be under-recognized in children and adolescents due to a high incidence of HL in this age group and histological similarity between these two entities. BM involvement by THRLBCL can be missed on aspirate histology alone. A high degree of suspicion with emphasis on immunohistochemistry of any atypical lymphoid infiltrate involving the bone marrow is paramount in establishing the diagnosis. If BM is the primary site of biopsy, differential diagnosis with HL involving the BM can be challenging [16]. Molecular information on THRLBCL is sparse. Studies on gene expression profiling reveal that THRLBCL has a distinct pattern when compared to classical HL. Analysis of the microenvironment also shows a unique host immune response not seen with NHLPL [14]. When adult THRLBCL patients are treated with anthracycline-based chemotherapy, most series demonstrate outcomes similar to DLBCL patients [4,19]. Three year OS is estimated to be 50-64% and five year OS is 45-58%. Patients misdiagnosed as HL or NLPHL had a worse prognosis with minimal response to salvage therapies [8,20]. Advancedstage disease was found to be associated with poor prognosis [9]. Pediatric patients described in the literature received treatment used for aggressive non-hodgkin large B-cell lymphomas and have fared better than adults [8,12,15]. Addition of rituximab to chemotherapy in children may improve outcomes [19]. Autologous stem cell rescue following high dose chemotherapy or allogeneic BMT may be considered for relapsed patients, but only a few have received this therapy to date [2]. Future therapies will likely target the relationship of the tumor cells to the inflammatory microenvironment [4]. Conclusion. THRLBCL can be used as a paradigm to underline the difficulties in defining specific subtypes of DLBCL and differentiating them from classical HL and NLPHL, peripheral T-cell lymphomas, and reactive processes. THRLBCL is currently under-recognized in the pediatric population. Accurate diagnosis requires careful examination of tumor cells and the background cellular infiltrate. Although molecular clonality may be helpful, it is limited by the small number of malignant B-cells. As evidenced by our patients, children respond well to chemotherapy and have a good prognosis. References 1. Lones MA, Cairo MS, Perkins SL. T-cell-rich large B-cell lymphoma in children and adolescents: a clinicopathologic report of six cases from the Children's Cancer Group Study CCG Cancer. 2000;88: Tiemann M, Riener MO, Claviez A, et al. Proliferation rate and outcome in children with T-cell rich B-cell lymphoma: a clinicopathologic study from the NHL-BFM-study group. Leuk Lymphoma. 2005;46: Swerdlow SH, International Agency for Research on Cancer., World Health Organization. WHO classification of tumors of hematopoietic and lymphoid tissues. Lyon, France: International Agency for Research on Cancer; 2008: Abramson JS. T-cell/histiocyte-rich B-cell lymphoma and the paradox of the host immune response. Leuk Lymphoma. 2007;48: Mirchandani I, Palutke M, Tabaczka P, et al. B-cell lymphomas morphologically resembling T-cell lymphomas. Cancer. 1985;56: Ramsay AD, Smith WJ, Isaacson PG. T-cell-rich B-cell lymphoma. Am J Surg Pathol. 1988;12: Jaffe ES. Pathology and genetics of tumors of hematopoietic and lymphoid tissues: IARC Press; 2001: Rodriguez J, Pugh WC, Cabanillas F. T-cell-rich B-cell lymphoma. Blood. 1993;82: Greer JP, Macon WR, Lamar RE, et al. T-cell-rich B-cell lymphomas: diagnosis and response to therapy of 44 patients. J Clin Oncol. 1995;13: Camilleri-Broet S, Molina T, Audouin J, et al. Morphological variability of tumor cells in T-cell-rich B-cell lymphoma. A histopathological study of 14 cases. Virchows Arch. 1996;429:
6 Ng CS, Chan JK, Hui PK, et al. Large B-cell lymphomas with a high content of reactive T cells. Hum Pathol. 1989;20: Aki H, Tuzuner N, Ongoren S, et al. T-cell-rich B-cell lymphoma: a clinicopathologic study of 21 cases and comparison with 43 cases of diffuse large B-cell lymphoma. Leuk Res. 2004;28: El Weshi A, Akhtar S, Mourad WA, et al. T-cell/histiocyte-rich B-cell lymphoma: Clinical presentation, management and prognostic factors: report on 61 patients and review of literature. Leuk Lymphoma. 2007;48: Pittaluga S, Jaffe ES. T-cell/histiocyte-rich large B-cell lymphoma. Haematologica. 2010;95: Achten R, Verhoef G, Vanuytsel L, et al. T-cell/histiocyte-rich large B-cell lymphoma: a distinct clinicopathologic entity. J Clin Oncol. 2002;20: Hsi ED. Hematopathology: Churchill Livingstone Elsevier; : Ripp JA, Loiue DC, Chan W, et al. T-cell rich B-cell lymphoma: clinical distinctiveness and response to treatment in 45 patients. Leuk Lymphoma. 2002;43: Stenhammar L, Masreliez V. T-cell-rich B-cell lymphoma in a child with celiac disease. J Pediatr Gastroenterol Nutr. 1993;17: Bouabdallah R, Mounier N, Guettier C, et al. T-cell/histiocyte-rich large B-cell lymphomas and classical diffuse large B-cell lymphomas have similar outcome after chemotherapy: a matched-control analysis. J Clin Oncol. 2003;21: McBride JA, Rodriguez J, Luthra R, et al. T-cell-rich B largecell lymphoma simulating lymphocyte-rich Hodgkin's disease. Am J Surg Pathol. 1996;20: Marafioti T, Mancini C, Ascani S, Sabattini E, Zinzani PL, Pozzobon M, Pulford K, Falini B, Jaffe ES, Müller-Hermelink HK, Mason DY, Pileri SA. Leukocyte-specific phosphoprotein-1 and PU.1: two useful markers for distinguishing T-cellrich B-cell lymphoma from lymphocyte-predominant Hodgkin's disease. Haematologica Aug;89(8): Gupta S, Cogbill CH, Gheorghe G, Rao AR, Kumar S, Havens PL, Camitta BM, Warwick AB.Mycobacterium avium intracellulare infection coexistent with nodular lymphocyte predominant Hodgkin lymphoma involving the lung. J Pediatr Hematol Oncol Apr;33(3):e doi: / MPH.0b013e3181faf89a.
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