Composite B-Cell and T-Cell Non-Hodgkin Lymphoma of the Tibia
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1 Hematopathology / COMPOSITE B-CELL AND T-CELL LYMPHOMA Composite B-Cell and T-Cell Non-Hodgkin Lymphoma of the Tibia Zahid Kaleem, MD, Michael H. McGuire, MD, Adrian C. Caracioni, MD, Ronald L. Leonard, DO, M. Hanif Pathan, MD, Ellen A. Lessmann, MT(ASCP), and Wing C. Chan, MD Key Words: Composite; Non-Hodgkin; Lymphoma; Bone; Tibia; B-cell; T-cell DOI: 0.09/P6LUADHRL9TXFWM Abstract We report a unique case of de novo composite lymphoma in the tibia of a 5-year-old man who presented with increasingly frequent and intense pain in the right upper leg. He was otherwise healthy without significant medical history. A plain radiograph of the right leg showed a permeative lesion with alternating areas of radiolucency and radiodensity in the upper third of the tibia. Magnetic resonance imaging showed a large, heterogeneous enhancing lesion involving the medullary and cortical bone of the proximal tibia with cortical disruption and extension into the adjacent soft tissue. A biopsy showed sheets and clusters of large cells, punctuated by clusters of small, irregular lymphocytes. Flow cytometry and immunohistochemical analysis showed composite lymphoma: diffuse large B- cell lymphoma (DLBCL) and peripheral T-cell non- Hodgkin lymphoma with predominantly small cell morphologic features. The DLBCL expressed CD9, CD0, CD79a, CD5, CD0, CD, CD8, CD7, bcl-, and bcl-6, with monotypic expression of immunoglobulin κ light chain. The T cells expressed CD, CD, CD5, CD7, and CD8, with partial loss of CD. Clonal rearrangement of T-cell receptor γ chain gene was found. Neither the large B cells nor the small T cells expressed Epstein-Barr virus encoded RNA. Physical examination and radiologic studies showed no evidence of lymphadenopathy, organomegaly, or other mass lesions in the body. No peripheral lymphocytosis or bone marrow involvement was present. A composite lymphoma is the rare occurrence of or more distinct lymphoma types at the same anatomic site. The combination might include a Hodgkin lymphoma with a B- cell or a T-cell non-hodgkin lymphoma (NHL), a B-cell NHL with a T-cell NHL, or distinct B-cell or T-cell NHLs at the same anatomic site. Most of the reported cases included a combination of a classic Hodgkin lymphoma with an NHL, usually of the B-cell type. - The presence of distinct B-cell NHLs in the same tissue or organ also has been reported and might represent clonal evolution, in at least some cases. 5,6 The occurrence of a B-cell and a T-cell NHL, however, is a rare and enigmatic phenomenon. Most of the reported cases of composite B-cell and T-cell NHL included cases of cutaneous T-cell lymphoma (mycosis fungoides) with B-cell small lymphocytic lymphoma/chronic lymphocytic leukemia, either lymphoma type antedating the other. 7-9 Simultaneous occurrence of a B-cell and a T-cell NHL, other than a cutaneous T- cell lymphoma, also has been reported, including cases of an angiocentric T-cell lymphoma with a diffuse large B-cell lymphoma (DLBCL) 0, and other peripheral T-cell NHLs with low grade B-cell NHLs. 8 We describe a very unusual and hitherto unreported case of a primary composite lymphoma that arose in the upper tibia and was composed of a diffuse large B-cell NHL and a peripheral T-cell NHL with predominantly small cell morphologic features. Case Report A 5-year-old man with no significant medical history was evaluated for intolerable pain in his right leg. He described the onset of pain some 5 years ago with intermittent episodes, Am J Clin Pathol 005;:5-5 5 DOI: 0.09/P6LUADHRL9TXFWM 5
2 Kaleem et al / COMPOSITE B-CELL AND T-CELL LYMPHOMA but the intensity and frequency of the pain increased only about or years ago. He did not complain of any other symptoms, specifically no fevers, weight loss, or night sweats. Physical examination of the right leg showed a swollen knee with exquisite tenderness at the upper end of the tibia. The rest of the physical examination was normal with no evidence of lymphadenopathy or splenomegaly. A plain radiograph of the right leg showed a permeative lesion with alternating areas of radiolucency and radiodensity in the upper third of the tibia (metaphysis and proximal diaphysis) and a small effusion in the knee joint. The femur and fibula appeared normal Image A. Magnetic resonance imaging showed a large and heterogeneous enhancing lesion involving the medullary and cortical bone of the proximal tibia with cortical disruption and extension into the adjacent soft tissue Image B. Technetium 99m scanning of the tibia showed abnormally increased uptake in the proximal tibia consistent with the magnetic resonance imaging findings. Computed tomography scans of the chest, abdomen, and pelvis did not show any enlargement of the lymph nodes, spleen, or liver. Results of all pertinent laboratory tests were normal, including WBC count (8,00/µL [ /L] with a normal differential count), hemoglobin concentration (.0 g/dl [0 g/l]), platelet count (05 0 /µl [ /L]), and lactate dehydrogenase level (86 U/L). A curettage biopsy of the tibial lesion was performed. A Image A, A plain radiograph of the right leg showing a permeative lesion with alternating areas of radiolucency and radiodensity in the upper third of the tibia (metaphysis and proximal diaphysis). B, Magnetic resonance imaging showed a large and heterogeneous enhancing lesion involving the medullary and cortical bone of the proximal tibia with focal cortical disruption and slight extension into the adjacent soft tissue. B Materials and Methods Morphologic Examination The biopsy specimens were fixed in 0% buffered formaldehyde and embedded in paraffin, and 5-µm sections were cut and stained with H&E for light microscopic examination. Immunohistochemical Analysis Immunohistochemical analysis was performed on formalin-fixed, paraffin-embedded tissue samples as previously described. Antibodies were used against the following antigens: CDa, CD, CD5, CD0, CD0, CD0, CD, CD5, CD68, CD79a, CD99, bcl-, bcl-6, terminal deoxynucleotidyl transferase (TdT), myeloperoxidase, IgG, IgM, immunoglobulin κ and λ light chains, cytokeratin, S-00, neuron-specific enolase, and vimentin. Flow Cytometric Analysis Fresh tissue samples were transported immediately in RPMI solution to the flow cytometry laboratory, and cells were released by teasing followed by filtration of separated cells. Mononuclear cells were stained with various combinations of fluorescein isothiocyanate (FITC)-, phycoerythrin (PE)-, phycoerythrin cyanin-5 (PC5)-, or phycoerythrin Texas red (ECD)-labeled monoclonal antibodies against the following antigens: CD, CD, CD, CD5, CD7, CD8, CD0, CD9, CD0, CD, CD, CD8, CD5, CD7, HLA-DR, and immunoglobulin κ and λ light chains. The combinations included κ-fitc/λ-pe/cd9-ecd/cd5- PC5, CD5-FITC/CD-PE/CD9-ECD/CD5-PC5, CD8- FITC/CD0-PE/CD9-ECD/CD5-PC5, CD-FITC/CD0- PE/CD9-ECD/CD5-PC5, CD-FITC/CD7-PE/CD- ECD/CD5-PC5, CD8-FITC/CD7-PE/CD5-ECD, and CD8-FITC/CD-PE/CD-ECD/CD5-PC5. Intracytoplasmic evaluations for bcl- and intranuclear detection of TdT also were performed using permeabilization techniques. Four-color flow cytometric immunophenotyping was performed on a cytometer (Coulter XL Epic, Beckman Coulter, Miami, FL) by collecting 0,000 ungated list-mode events, selecting an appropriate gate on the combination of CD5 and side scatter, and analyzing cells within the most appropriate gate. An antigen was considered positively expressed when at least 5% of the gated cells expressed that antigen. B-cell clonality was defined when the immunoglobulin κ/immunoglobulin λ light chain ratio was more than : or less than 0.5: as described previously. Isotype controls were run in all cases. All antibodies were purchased from Beckman Coulter except for bcl-, which was obtained from DAKO (Carpinteria, CA), and used according to the manufacturers guidelines. 6 Am J Clin Pathol 005;:5-6 DOI: 0.09/P6LUADHRL9TXFWM
3 Hematopathology / CASE REPORT T-Cell and Immunoglobulin Heavy Chain Receptor Gene Rearrangements The T-cell receptor γ chain gene assay was performed as described by Lawnicki and coworkers. Data were analyzed using GeneScan software (Perkin Elmer Applied Biosystems, Foster City, CA). Only clonal peaks with a height greater than times the maximum height of the background polyclonal distribution in duplicate assays were interpreted as positive. The clonality analysis of the immunoglobulin heavy chain gene was performed as described by Lozano et al. 5 In Situ Hybridization for Epstein-Barr Virus Encoded RNA In situ hybridization was performed on paraffin-embedded sections according to the manufacturer s instructions using a Peptide Nucleic Acid ISH Detection kit and Epstein- Barr Virus encoded RNA peptide nucleic acid probe labeled with FITC (DAKO). 6 Results Image Biopsy specimen of the bone showing sheets of large cells with moderate amounts of cytoplasm and large nuclei. Scattered small lymphocytes and plasma cells also are seen. The large cells stained with B-cell markers (H&E, original magnification 00). Light Microscopic Examination The biopsy specimen showed replacement of the normal architecture of the bone and marrow by a tumor composed of a dual population of cells. About 0% to 50% of the tumor was composed of sheets of large cells with moderate to abundant amounts of pale cytoplasm and large nuclei with distinct nucleoli Image. Mitoses were frequent. Sheets of large cells often were punctuated by clusters of small cells with scant cytoplasm and irregular to cleaved nuclei without prominent nucleoli Image. In some areas, sheets of these small cells predominated, whereas in others, small cells often were intermixed with large cells Image. Areas of necrosis also were seen. Image An area composed predominantly of small lymphocytes with irregular to cleaved nuclei without prominent nucleoli. Only rare large cells are present. The area stained almost exclusively with T-cell markers (H&E, original magnification 00). Image This slide shows an intimate mixture of large and small lymphocytes. The large cells showed vesicular chromatin and are admixed with smaller cells with very irregular nuclei and coarse chromatin (H&E, original magnification,000). Am J Clin Pathol 005;:5-7 7 DOI: 0.09/P6LUADHRL9TXFWM 7
4 Kaleem et al / COMPOSITE B-CELL AND T-CELL LYMPHOMA Immunohistochemical Analysis The large cells stained positively for CD0, CD79a, CD0, CD8, bcl-, and bcl-6, whereas the small lymphocytes stained positively for CD, CD5, CD, and CD99 Image 5, Image 6, and Image 7. The staining pattern was mutually exclusive between large and small cells. The large cells showed weak and focal staining for CD5 (leukocyte Image 5 Immunohistochemical analysis showed an area of large cells with strong reactivity for CD0 next to an area that is composed predominantly of small lymphocytes and showed no staining for CD0 (CD0 immunostain, original magnification 00). common antigen). None of the tumor cells showed any staining for cytokeratin (AE/AE), CDa, CD0, TdT, neuronspecific enolase, S-00, and myeloperoxidase. Vimentin was positive in all tumor cells. Flow Cytometric Analysis Flow cytometric analysis of the tumor showed a dual population of cells, including a population of large cells (% of gated cells) that showed dim expression of CD5 and a population of small cells (7% of gated cells) with bright expression of CD5. The large cells showed expression of B-cell markers CD9 and CD0 with coexpression of CD5 (56%), CD0 (9%), CD (58%), CD8 (6%), CD7 (87% on CD8+ cells), and bcl- (96% on CD9+ cells), with monotypic surface expression of immunoglobulin κ light chain (κ/λ = ~0:). The small lymphocytes expressed CD (9%), CD (9%), CD5 (90%), CD7 (9%), and CD8 (0%) with partial loss of CD. Neither large nor small lymphocytes showed significant expression of CD or TdT Image 8. Gene Rearrangement Studies by Polymerase Chain Reaction Clonal T-cell receptor γ chain gene rearrangement was detected by polymerase chain reaction. No clonal rearrangement, however, could be detected for immunoglobulin heavy chain by DNA amplification using consensus primers for heavy chain gene variable (framework III) and joining regions. The DNA could not be amplified adequately using consensus primers for variable (framework II) and joining Image 6 This is the same area as seen in Image 5. Immunohistochemical analysis showed the small cells with strong reactivity for CD. The larger cells seen in Image 5 do not show any staining for CD (CD immunostain, original magnification 00). Image 7 Strong nuclear reactivity for bcl-6 in larger cells, confirming their follicle center cell origin (bcl-6 immunostain, original magnification 00). 8 Am J Clin Pathol 005;:5-8 DOI: 0.09/P6LUADHRL9TXFWM
5 Hematopathology / CASE REPORT A B C 5,000,000 Forward Scatter κ FITC 00 0 I CD5 FITC 00 0 I Side Scatter ,000 λ PE ,000 CD PE D E F,000,000, CD8 FITC 0 I ,000 CD0 PE CD9 ECD 0 J ,000 bcl- FITC ,000 CD ECD Image 8 A, Side scatter vs forward scatter showing a population of larger cells and a population of smaller lymphocytes. B, The larger cells showed monotypic expression of immunoglobulin κ. C, The larger cells showed coexpression of CD5 and CD. D, The larger cells showed coexpression of CD0 and CD8. E, Expression of bcl- in large B cells. F, The smaller T cells showed expression of CD and CD7. ECD, phycoerythrin Texas red; FITC, fluorescein isothiocyanate; PE, phycoerythrin. CD7 PE G regions. The analytic sensitivity of the assay was only about 70% with this technique. In Situ Hybridization for Epstein-Barr Virus Encoded RNA The test result was negative in large and small lymphocytes. Discussion We have described a rare case of a composite lymphoma composed of a DLBCL and a peripheral T-cell lymphoma with predominantly small cell morphologic features. The lymphoma is unique among other reported cases because it arose primarily in the tibia without evidence of a B-cell or a T-cell NHL elsewhere. Many other features of this lymphoma merit discussion. The coexpression of CD5, CD0, and CD among B-cell NHLs is an unusual phenomenon, reported only in rare cases of DLBCL and less commonly in follicular lymphomas. CD5, a T cell associated antigen, is expressed by a subset of prefollicular B cells and is absent from follicular germinal center B cells, which express CD0. Rare cases of mantle cell lymphoma and follicular lymphoma exist that express both CD5 and CD0. 7,8 Simultaneous expression of CD5, CD0, and CD in B-cell lymphomas, however, is very rare. No single normal B-cell population is known to express CD5, CD0, and CD together. Thus, this immunophenotype in lymphomas is the result of aberrant expression of at least antigen. DLBCLs do not show a consistent immunophenotype. Most cases lack expression of CD5, CD0, or CD; a small percentage express CD0 and an even smaller number of cases Am J Clin Pathol 005;:5-9 9 DOI: 0.09/P6LUADHRL9TXFWM 9
6 Kaleem et al / COMPOSITE B-CELL AND T-CELL LYMPHOMA express CD5 or CD. Thus, the expression of CD5, CD0, and CD in this lymphoma represents an unusual phenotype. The expression of bcl-6 in large B-cells (DLBCL) indicates a follicle center cell origin of this component of the composite lymphoma. 9 Extranodal follicular lymphomas and DLBCL of follicle center cell origin occur in sites such as skin, thyroid, intestine, orbit, and others. These sites can show benign follicular lymphoid hyperplasia, and, hence, the development of follicular lymphoma or DLBCL of follicle center cell origin is conceivable and might represent clonal expansion of a resident transformed follicle center cell. The expression of CD7 (c-kit) in this lymphoma also is unusual. CD7 is a class III receptor tyrosine kinase and has an important role in the differentiation of immature hematopoietic and lymphoid cells. 0 Its normal expression is limited to immature myeloid cells, T-lymphoid blasts, and a subset of natural killer cells but not B cells. The expression of CD7 in large B-lymphoma cells in this case represents aberrant expression of this antigen. This phenomenon is observed rarely. Bravo et al described only case of B-cell NHL with t(;8) that showed high expression of CD7. Although only rarely reported, evaluation of CD7 expression in B-cell neoplasms might identify a subset of lymphomas that express this antigen and might benefit from anti-cd7 antibodies. A composite lymphoma is defined as the presence of at least distinct lymphoma types at the same anatomic site and might represent a chance occurrence or a de novo lymphoma with clones (divergent clones evolved from an initial single neoplastic clone or clones developed from independent mutational hits in separate cells). It is likely that some cases represent the first scenario of chance coexistence and might more aptly be called collision composite lymphoma, whereas the others belong to the latter category and truly signify a composite lymphoma. Although the term composite lymphoma is used without qualifiers to include both categories, it might be useful to distinguish the two categories. This term was first coined by Custer in 95 to describe a lymphoma with more than one histologic pattern in organs or within the same organ. It now is accepted generally that this term be limited to or more distinct lymphoma patterns in the same tissue. The presence of distinct lymphoma types in different organs might be classified more correctly as synchronous lymphomas rather than composite lymphoma. Also, the report by Custer predates the development of commercially available antibodies, and it is unclear whether the case described by Custer indeed was true composite lymphoma or transformation of a preexisting lymphoma. In 977, Kim et al expanded the definition of a composite lymphoma to include cases of Hodgkin lymphoma with NHL. Several subsequent reports, however, indiscriminately used this term to include cases of transformation of a preexisting lymphoma. Cases of usual transformations such as Richter transformations in small lymphocytic lymphoma and large cell transformation in follicular lymphomas must not be included under the rubric of composite lymphoma because transformed lymphomas pathogenetically represent a clonal evolution and generally pursue an aggressive and rapid course, whereas a de novo composite lymphoma might not exhibit an aggressive clinical course. We prefer to differentiate among various groups described under this term to identify true de novo composite lymphoma from cases that represent unusual transformations and development of unrelated lymphomas to convey pathogenetic information and the clinical significance of these cases. The development of a distinct but clonally related lymphoma arising in an anatomic site already involved by a lymphoma, such as Burkitt lymphoma evolving in a follicular lymphoma, might be termed more appropriately transformation composite lymphoma. A case reported by Tsang et al 6 of a mantle cell lymphoma arising in a patient with follicular lymphoma might be included under this category. Clonally unrelated lymphomas that arise asynchronously in different sites but happen to involve the same anatomic site at some point during the disease might be referred to as collision composite lymphomas because they conceptually are different from de novo composite lymphoma, and each lymphoma type bears its own prognosis. Unlike transformation composite lymphoma, each component of a collision composite lymphoma also involves a separate anatomic site, such as small lymphocytic lymphoma in the bone marrow and a T-cell lymphoma of the skin. Several reported cases fall under this group. 9,5 It is in this context that we would like to redefine a de novo composite lymphoma as follows: a lymphoma that is composed of or more distinct lymphoma types, each with its own clone arising at the same anatomic site and clinically identified at the same time, without any history of lymphoma elsewhere in the body. This narrow definition of de novo composite lymphoma excludes cases of collision composite lymphoma and transformation composite lymphoma and ensures that each category conveys its own prognosis and defines a distinct clinicopathologic scenario. From the Departments of Pathology, Surgery, and Medicine, Creighton University Medical Center, and Pathology and Microbiology, University of Nebraska Medical Center, Nebraska Medical Center, Omaha. Address reprint requests to Dr Kaleem: Dept of Pathology, Creighton University Medical Center, 60 N 0th St, Omaha, NE 68. References. Gonzalez CL, Medeiros LJ, Jaffe ES. Composite lymphoma: a clinicopathologic analysis of nine patients with Hodgkin s disease and B-cell non-hodgkin s lymphoma. Am J Clin Pathol. 99;96: Am J Clin Pathol 005;:5-0 DOI: 0.09/P6LUADHRL9TXFWM
7 Hematopathology / CASE REPORT. Paulli M, Rosso R, Kindl S, et al. Nodular sclerosing Hodgkin s disease and large cell lymphoma: immunophenotypic characterization of a composite case. Virchows Arch A Pathol Anat Histopathol. 99;: Steinhoff M, Hummel M, Assaf C, et al. Cutaneous T cell lymphoma and classic Hodgkin lymphoma of the B cell type within a single lymph node: composite lymphoma. J Clin Pathol. 00;57:9-.. Mittal BB, Nalesnik M. Composite lymphoma (Hodgkin s and non-hodgkin s) of the spleen in a previously untreated patient. Acta Haematol. 986;76: Pescarmona E, Pignoloni P, Orazi A, et al. Composite lymphoma, lymphoplasmacytoid and diffuse large B-cell lymphoma of the spleen: molecular-genetic evidence of a common clonal origin. Virchows Arch. 999;5: Tsang P, Pan L, Cesarman E, et al. A distinctive composite lymphoma consisting of clonally related mantle cell lymphoma and follicle center cell lymphoma. Hum Pathol. 999;0: Hull PR, Saxena A. Mycosis fungoides and chronic lymphocytic leukemia: composite T-cell and B-cell lymphomas presenting in the skin. Br J Dermatol. 000;: Liu YC, Tomashefski JF Jr, Cleveland RP, et al. Composite cutaneous T-cell lymphoma and small B-cell lymphocytic lymphoma: morphologic, immunologic, and molecular genetic documentation of concurrent lymph node involvement. Mod Pathol. 99;7: Volk AL, Vannucci SA, Cook W, et al. Composite mycosis fungoides and B-cell chronic lymphocytic leukemia. Ann Diagn Pathol. 00;6: Xu Y, McKenna RW, Hoang MP, et al. Composite angioimmunoblastic T-cell lymphoma and diffuse large B-cell lymphoma: a case report and review of the literature. Am J Clin Pathol. 00;8: Chen Y-K, Huang E, Lin C-C, et al. Composite lymphoma: angiocentric T-cell lymphoma (CD8+ cytotoxic/suppressor T-cell) and diffuse large B-cell lymphoma associated with EBV, and presenting clinically as a midfacial necrotizing lesion. Oral Oncol. 00;0: Kaleem Z, Lind AC, Humphrey PA, et al. Concurrent Ki-67 and p5 immunostaining in cutaneous melanocytic neoplasms: an adjunct for recognition of the vertical growth phase in malignant melanomas? Mod Pathol. 000;:7-.. Kaleem Z, White G, Vollmer RT. Critical analysis and diagnostic usefulness of limited immunophenotyping of B-cell non-hodgkin lymphomas by flow cytometry. Am J Clin Pathol. 00;5:6-.. Lawnicki LC, Rubocki RJ, Chan WC, et al. The distribution of gene segments in T-cell receptor gamma gene rearrangements demonstrates the need for multiple primer sets. J Mol Diagn. 00;5: Lozano MD, Tierens A, Greiner TC, et al. Clonality analysis of B-lymphoid proliferations using polymerase chain reaction. Cancer. 996;77: Grinstein S, Preciado MV, Gattuso P, et al. Demonstration of Epstein-Barr virus in carcinoma of various sites. Cancer Res. 00;6: Dong HY, Gorczyca W, Liu Z, et al. B-cell lymphomas with coexpression of CD5 and CD0. Am J Clin Pathol. 00;9: Barry TS, Jaffe ES, Kingma DW, et al. CD5+ follicular lymphoma: a clinicopathologic study of three cases. Am J Clin Pathol. 00;8: Onizuka T, Moriyama M, Yamochi T, et al. bcl-6 gene product, a 9- to 98-kd nuclear phosphoprotein, is highly expressed in germinal center B cells and their neoplastic counterparts. Blood. 995;86: Ishii N, Asao H, Sugamura K. Cytokine receptors: section report. In: Kishimoto T, Kikutani H, von dem Borne A, et al, eds. Leukocyte Typing IV: White Cell Differentiation Antigens. New York, NY: Garland Publishing; 998: Bravo P, Agustin BD, Bellas C, et al. Expression of high amounts of the CD7 molecule in a case of B-cell non- Hodgkin s lymphoma carrying the t(:8) translocation. Am J Hematol. 000;6:6-9.. Custer RP. Pitfalls in the diagnosis of lymphoma and leukemia from the pathologist s point of view. In: Proceedings From the nd National Cancer Conference. New York, NY: American Cancer Society; 95: Kim H, Hendrickson MR, Dorfman R. Composite lymphoma. Cancer. 977;0: De Jong D, Voetdijk BM, Beverstock GC, et al. Activation of c-myc oncogene in a precursor B-cell blast crisis of follicular lymphoma, presenting as composite lymphoma. N Engl J Med. 988;8: Wlodarska I, Delabie J, De Wolf-Peeters C, et al. T-cell lymphoma developing in Hodgkin s disease: evidence for two clones. J Pathol. 99;70:9-8. Am J Clin Pathol 005;:5- DOI: 0.09/P6LUADHRL9TXFWM
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