Composite Recurrent Hodgkin Lymphoma and Diffuse Large B-Cell Lymphoma One Clone, Two Faces
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1 Hematopathology / COMPOSITE RECURRENT HL AND DLBCL Composite Recurrent Hodgkin Lymphoma and Diffuse Large B-Cell Lymphoma One Clone, Two Faces Qin Huang, MD, PhD, Sharon P. Wilczynski, MD, PhD, Karen L. Chang, MD, and Lawrence M. Weiss, MD Key Words: Composite lymphoma; Lymphoma; Hodgkin lymphoma; Diffuse large B-cell lymphoma; Epstein-Barr virus Abstract We describe a composite lymphoma with recurrent Hodgkin lymphoma and diffuse large B-cell lymphoma components manifesting as a single, perforated small intestinal tumor in a 56-year-old man with a history of classical Hodgkin lymphoma and recent relapse in the bone marrow. The resected mass had 2 morphologically and immunophenotypically distinct components; 1 showed a pleomorphic cellular infiltrate with fibrosis and contained numerous, large Hodgkin/Reed- Sternberg like cells and variants. The tumor cells were CD30+ and focally positive for CD15 but CD20, CD79a, and PAX-5. In situ hybridization for Epstein- Barr virus (EBV) was strongly positive in the large pleomorphic tumor cells. The adjacent component displayed sheets of relatively uniform, large lymphoid cells with typical morphologic features of diffuse large cell lymphoma. The tumor cells showed uniform expression of tested B-cell antigens, absence of CD30 or CD15, and complete absence of EBV-encoded RNA. Separate molecular studies with immunoglobulin heavy and κ light chain gene rearrangements clearly demonstrated an identical rearrangement pattern, indicating derivation from the same clone, which was confirmed by direct DNA sequencing analysis. Such distinctly different morphology, immunophenotype, and EBV status in different components within a clonally related single tumor mass is striking. Classical Hodgkin lymphoma and non-hodgkin lymphoma coexisting in the same patient are not common. They may occur synchronously or metachronously. 1-8 The term composite lymphoma generally refers to 2 different lymphoma entities occurring simultaneously in the same anatomic location of a patient and usually refers to 2 different non-hodgkin lymphomas. 4 Coexistence of a classical Hodgkin lymphoma and a non-hodgkin lymphoma in the same anatomic location has been reported occasionally; they may be clonally related (ie, derived from the same lymphoid progenitors) or not related (ie, different lymphoid progenitors). 1-9 Controversy about this issue may reflect the lack of a full understanding of the pathogenesis of these lymphomas or the heterogeneity of Hodgkin and non-hodgkin lymphomas. 2,3,5,6,8,10 We describe a rare case of a composite, recurrent Hodgkin lymphoma and diffuse large B-cell lymphoma occurring as a single, perforated small intestinal tumor in a 56- year-old man with a remote history of classic Hodgkin lymphoma and recent relapse in the bone marrow. The resected intestinal tumor mass had 2 distinctive but ill-separated components with 2 morphologically different and immunophenotypically distinct populations of malignant lymphoma cells, corresponding to recurrent classical Hodgkin lymphoma and diffuse large B-cell lymphoma. Positive Epstein-Barr virus encoded RNA (EBER) in situ hybridization was limited to the recurrent classical Hodgkin lymphoma component. Immunoglobulin gene rearrangements and direct DNA sequencing analysis performed on DNA from the 2 microdissected components clearly demonstrated identical immunoglobulin heavy and κ light chain gene rearrangements, indicating classical Hodgkin lymphoma and diffuse large B-cell lymphoma present as a clonally related composite lymphoma. 222 Am J Clin Pathol 2006;126: Downloaded 222 from
2 Hematopathology / CASE REPORT The finding supports the view that they are derived from the same lymphoid progenitors, probably of late germinal center based B cells. 6,11 Case Report The patient was a 56-year-old man with a history of stage IVB classical Hodgkin lymphoma, nodular sclerosing type, which was diagnosed in He was treated with mechlorethamine, vincristine [Oncovin], procarbazine, and prednisone/doxorubicin [Adriamycin], bleomycin, vinblastine, and dacarbazine chemotherapy at an outside hospital. The patient initially achieved a remission, but relapse occurred 3 years later. At that time, he underwent autologous stem cell transplantation with fractionated total body irradiation, cyclophosphamide, and etoposide. In August 2005 (almost 9 years after the relapse), the patient sought care at the City of Hope National Medical Center (Duarte, CA) with B symptoms and generalized lymphadenopathy. A computed tomography scan of the chest, abdomen, and pelvis showed multiple pulmonary nodules, multiple hepatic lesions, and mediastinal, porta hepatis, retroperitoneal, and mesenteric lymphadenopathy, consistent with recurrent Hodgkin lymphoma. Bone marrow biopsy was performed at this time and revealed bilateral involvement (20%) by recurrent Hodgkin lymphoma, with tumor cells strongly positive for CD30 and Epstein-Barr virus (EBV) latent membrane protein (LMP) Image 1. Twelve days later, an endoscopic examination revealed gastric intestinal ulcers with bleeding. Two weeks after admission, a chest radiograph showed large amounts of free air in the intra-abdominal region, and the patient was thought to have a bowel perforation. An immediate exploratory abdominal procedure was performed and a large, obstructive mass with a small perforation was identified in the midportion of the small intestine. The lesion was resected completely. Extensive retroperitoneal and mesenteric lymphadenopathy also was identified but not biopsied during the procedure. The patient s postoperative hospital course was complicated by sepsis, acute renal failure, liver failure, and coagulopathy. Despite intensive supportive therapy, the patient died on the sixth postoperative day, which was 20 days after admission to City of Hope National Medical Center. Permission for an autopsy was not granted. Materials and Methods Morphologic Evaluation The small intestinal mass resection specimen was fixed in 10% neutral buffered formalin. Paraffin sections were stained with H&E for routine histologic examination. Immunohistochemical Staining Immunohistochemical staining was performed on formalin-fixed, paraffin-embedded tissue sections using an automated immunostainer (DAKO, Carpinteria, CA), as described previously. 12 The following primary antibodies were used: CD3 (1:200 dilution; DAKO), CD10 (1:40 dilution; Vector, Burlingame, CA), CD15 (1:20 dilution; BD Biosciences, San Jose, CA), CD20 (1:500 dilution; DAKO), CD30 (1:120 dilution; DAKO), CD43 (1:10 dilution; Ventana, Tucson, AZ), A B Image 1 Histologic and immunophenotypic features of recurrent Hodgkin lymphoma in the bone marrow. A, The bone marrow clot section shows a lymphoid aggregate with scattered large atypical cells (H&E, 200). B, CD30 immunohistochemical staining highlights Hodgkin cells ( 200). Downloaded from Am J Clin Pathol 2006;126:
3 Huang et al / COMPOSITE RECURRENT HL AND DLBCL CD45RB (1:200 dilution; DAKO), CD79a (1:200 dilution; DAKO), CD138 (1:160; Serotec, Raleigh, NC), bcl-2 (1:50 dilution, DAKO), bcl-6 (1:10 dilution; DAKO), MUM-1 (1:20 dilution; DAKO), PAX-5 (1:80 dilution; BD Biosciences), and EBV-LMP (1:600 dilution; DAKO). Antibody detection was performed using the DAKO EnVision+ System and 3,3'- diaminobenzidine as a chromogen. Appropriate positive and negative tissue control samples were used with each run. Molecular Studies Genomic DNA was isolated from 2 dissected paraffinembedded tissue samples of the recurrent Hodgkin lymphoma and diffuse large B-cell lymphoma components in the small intestinal mass. Polymerase chain reaction (PCR) procedures were performed for analysis of immunoglobulin heavy and κ light chain rearrangements. For immunoglobulin heavy chain gene rearrangement, 3 sets of primers were used as forward primers, as follows: framework 3a primer: 5' TET-GAG GAC ACG GCT GTA TAT TAC TGT 3'; framework 2a primer: 5' HEX-TGG (A/G)TC CG(C/A) CAG (G/C)C(T/C) (T/C) CN GGG 3'; and framework 2b primer: 5' FAM-GTC CTG CAG GC(C/T) (C/T)CC GG(A/G) AA(A/G) (A/G)GT CTG GAG TGG 3'; and VLJHa as the reverse primer: 5' CAC CTG AGG AGA CGG TGA CC 3'. The amplified PCR products were visualized by capillary electrophoresis on an ABI310 genetic analyzer (PE Applied Biosystems, Foster City, CA) according to the manufacturer s recommendations, with subsequent software analysis using ABI Gene Scan 3.1 software. The amplified PCR products using identical, nonfluorescence primers subsequently were purified and subjected to direct DNA sequencing. For immunoglobulin κ light chain gene rearrangement, primers for Fr3k and immunoglobulin κ light chain joint region 3 (CDR3) were used as follows: Fr3k 5' TTC AG(C/T) GGC AGC GG(A/G) TCT GGG 3' and JK 5' CA(G/C) CTT (G/T)GT CCC (C/T)TG GCC GAA 3'. The amplified PCR products were electrophoresed in an 8% acrylamide gel and visualized with ethidium bromide staining. EBV in situ hybridization was performed on paraffin-embedded tissue samples by using a 30- base-pair oligonucleotide probe specific for EBER-1 RNA of the EBV (EBV probe: 5' AGA CAC CGT CCT CAC CAC CCG GGA CTT (G/C/T)TA 3', as described previously. 12,15 A poly T probe and a non-ebv probe were used as internal positive and negative control probes, respectively. Results Histologic Examination A 30.4-cm-long segment of the small bowel was received from the resection procedure. By gross examination, an obstructive mass with a 4.0-cm circumference was identified with a small area of perforation. The segment of small bowel proximate to the mass was dilated. The cut surface of the tumor revealed mucosal ulceration and hemorrhage. The low-power view of the H&E-stained sections of the resected small intestinal tumor showed a diffuse lymphoid infiltrate with surface ulceration but without recognizable morphologic differences in the tumor Image 2A. However, high-power magnification of the tumor displayed 2 areas with distinctive histomorphologic features Image 2C and Image 2D : one area showed a pleomorphic cellular infiltrate with fibrosis and contained numerous large atypical lymphoid cells, including Reed-Sternberg like cells and its variants (Image 2C), whereas the other area exhibited a homogeneously uniform population of large lymphoid cells with morphologic features of a typical diffuse large cell lymphoma (Image 2D). Both areas showed transmural infiltration. No obvious well-defined boundary separating the 2 areas was identified. Immunohistochemical Studies The immunohistochemical studies showed 2 distinct and opposite staining patterns in the 2 different morphologic components of the tumor Image 3A, Image 3B, Image 3C, Image 3D, Image 3E, Image 3F, and Table 1. The tumor cells in the pleomorphic area stained for CD30, bcl-2, and MUM-1 and focally for CD15 but did not stain for CD20, CD79a, PAX-5, or bcl-6. Some of the large tumor cells were positive for CD45RB. In contrast, the tumor cells in the more uniform area were strongly and uniformly positive for CD20, CD79a, PAX-5, bcl-6, and CD45RB but were completely negative for CD30, CD15, bcl-2, and MUM-1 (Images 3A-F, Table 1). Molecular Studies EBV in situ hybridization was performed to examine the status of the EBV infection in the small intestinal tumor because the relapsed Hodgkin lymphoma in the bone marrow was intensely EBV+. Just as distinct as the immunohistochemical results, the EBV+ cells were limited to the pleomorphic infiltrate only, with almost all tumor cells EBV+, whereas the tumor cells from the more uniform area were completely devoid of EBER staining Image 3G and Image 3H. For molecular studies of immunoglobulin heavy and κ light gene rearrangements, we microdissected the paraffinembedded tumor tissue and isolated the DNA from the 2 components of the tumor separately. The microdissection was performed based on the immunohistochemical staining pattern (CD20, CD30, PAX-5, and MUM-1), in which the 2 components of the tumor were quite distinct in the immunostained slides Image 2B. The immunostained (CD20) slides were laid over unstained sections, and the 2 components were dissected carefully (at least 2 mm from the possible transitional zone ) to avoid possible contamination from the transition zone. 224 Am J Clin Pathol 2006;126: Downloaded 224 from
4 Hematopathology / CASE REPORT A B D H C D Image 2 Histologic examination and immunohistochemical staining of the small intestinal composite lymphoma. A, Low-power view of the tumor shows a diffuse lymphoid infiltrate with no recognizable transitional zone (H&E, 100). B, CD20 immunohistochemical staining of the tumor shows distinct positive and negative components ( 200). C, High-power view of one tumor component (from square H of Image 2A) shows a pleomorphic cellular infiltrate with fibrosis containing numerous large Hodgkin/Reed-Sternberg like cells (inset) and variants (H&E, 400; inset, H&E, 400). D, High-power view of the other tumor component (from square D of Image 2A) shows sheets of relatively uniform large lymphoid cells with typical morphologic features of diffuse large B-cell lymphoma (H&E, 400). PCR analysis from the 2 morphologically and immunohistochemically distinct areas of the tumor clearly demonstrated 3 identical peaks corresponding to the framework 3a (position 102), 2a (position 258), and 2b (position 255) regions of the immunoglobulin heavy chain gene Image 4 in the 2 different areas. The identity of the amplified PCR products was confirmed further by direct DNA sequencing (data not shown). PCR analysis from the 2 areas for κ light chain gene rearrangement also yielded an identical result (data not shown). These results provide strong evidence that the 2 distinct populations of the tumor cells were derived from the same clone. Discussion This unique composite tumor displayed 2 distinct but coexisting components. One component, recurrent Hodgkin lymphoma, was characterized by a pleomorphic lymphoid infiltrate with numerous large atypical cells, which showed the same immunohistochemical staining pattern as the initially Downloaded from Am J Clin Pathol 2006;126:
5 Huang et al / COMPOSITE RECURRENT HL AND DLBCL A B C D Image 3 Immunohistochemical and Epstein-Barr virus (EBV) in situ hybridization characteristics of the composite lymphoma of the small intestine. A, C, E, and G, From the recurrent classical Hodgkin lymphoma component. diagnosed bone marrow classical Hodgkin lymphoma that recurred. Similar to most cases of relapsed Hodgkin lymphoma, recurrent Hodgkin lymphoma tends to have large clusters or aggregates of pleomorphic neoplastic cells but usually absence of the classical polymorphous inflammatory background. The detection of EBV-LMP by immunohistochemical analysis and EBV RNA by in situ hybridization in the large atypical cells provides further evidence for the diagnosis of recurrent Hodgkin lymphoma. 3,7,16,17 In contrast, the component of diffuse large B-cell lymphoma showed a uniform large lymphoid infiltrate, which had the immunophenotype of a non-hodgkin B-cell lymphoma. Identical immunoglobulin heavy and κ light chain gene rearrangements were seen in the 2 distinct areas, indicating that both components, despite their distinctly different morphologic features and immunophenotype, were indeed derived from the same clone. Thus, this tumor can be considered a true composite lymphoma with 2 distinctive faces. It is well established that the tumor cells (lymphocytic and histiocytic cells) in nodular lymphocyte predominant Hodgkin lymphoma are germinal center derived B cells with frequent expression of B cell associated antigens, immunoglobulin J chain and bcl-6. 7,18 Nodular lymphocyte predominant Hodgkin lymphoma has been shown to be related clonally to subsequent diffuse large B-cell lymphoma in many studies, suggesting transformation or a disease progression process. 7,18,19 However, the origin of the Hodgkin/Reed-Sternberg cells of classical Hodgkin lymphoma was a matter of debate for decades until molecular studies of dissected single cells revealed their clonality and lymphoid derivation. 1,5-8,10,17, Am J Clin Pathol 2006;126: Downloaded 226 from
6 Hematopathology / CASE REPORT E F G H B, D, F, and H, from the diffuse large B-cell lymphoma component. (A and B, CD20, 200; C and D, CD30, 200; E and F, PAX-5, 200; G and H, EBV in situ hybridization, 200). In the vast majority of cases, Hodgkin cells are unequivocally of B-cell origin and carry somatic mutations in their rearranged immunoglobulin variable region genes, a hallmark of germinal center B cells and their descendants. 1,5-8,10,21,22,24 It is believed that classical Hodgkin lymphoma cells have rearranged immunoglobulin genes but are somewhat defective for the gene transcription. 25 Studies of composite classical Hodgkin lymphoma and non-hodgkin lymphoma provided some insights for the clonal relationship and pathogenesis of those types of composite lymphomas. 1,2,4-6,9,21,22 Several composite lymphomas have been analyzed at the molecular level, and clonal relationships between Hodgkin lymphoma and non- Hodgkin lymphoma were established in most cases, if not all, indicating a clonal evolution. 5,6,10,14,22,23,25 The clonal relationships have been demonstrated in many cases in which classical Hodgkin lymphoma coexists with one of a variety of non-hodgkin lymphomas, including follicular lymphoma, small lymphocytic lymphoma, marginal zone B-cell lymphoma, mantle cell lymphoma, and diffuse large B-cell lymphoma. Many studies indicate that classical Hodgkin lymphoma and non-hodgkin lymphoma are derived from the same progenitors. 1,4-6,8,22,23 The differences in their subsequent behavior may be dependent on different subsequent lymphomagenic mutations or alteration of their respective signal transduction pathways. 5,7 In the present case, demonstrating that the recurrent Hodgkin lymphoma and diffuse large B-cell lymphoma are derived from the same clone indicates that both entities may arise from the same lymphoid precursors. Downloaded from Am J Clin Pathol 2006;126:
7 Huang et al / COMPOSITE RECURRENT HL AND DLBCL Table 1 Immunohistochemical and Molecular Features of the Composite Small Intestinal Lymphoma With Two Distinctive Components Recurrent Hodgkin Disease Diffuse Large B Cell Lymphoma CD3 CD10 CD15 + * CD20 + CD30 + CD43 + * CD45RB + * + CD79a + CD138 bcl-2 + bcl-6 + MUM-1 + PAX-5 + LMP + * EBER + IgH + + Immunoglobulin κ + + EBER, Epstein-Barr virus encoded RNA; IgH, immunoglobulin heavy chain; LMP, latent membrane protein; +, positive;, negative. * Focal or scattered large atypical cells were positive. It is interesting that, despite the fact that the recurrent classical Hodgkin lymphoma and diffuse large B-cell lymphoma in the present case shared the same clone, the EBV infection was limited to the recurrent classical Hodgkin lymphoma component. This finding suggests that the event of EBV infection (or reactivation) actually occurred at the same time or after the committed classical Hodgkin lymphoma transformation took place. This observation is consistent with those of many previous studies in which EBV infection was found preferentially in Reed-Sternberg cells or its variants in classical Hodgkin lymphoma but infrequently identified in non-hodgkin lymphoma associated with Hodgkin lymphoma. 3,16,17,23,26,27 The diffuse large B-cell lymphoma component in the present case clearly exhibited a B-cell phenotype, with strong and uniform positivity for CD20, CD79a, and PAX- 5. The lymphoma cells also expressed bcl-6 but were completely negative for bcl-2 and MUM-1; thus, they fall in the category of a germinal center type of diffuse large B- cell lymphoma. 28 In contrast, the recurrent Hodgkin lymphoma showed strong expression of CD30, bcl-2, and MUM-1 in almost all large, atypical tumor cells but was completely negative for all B cell associated antigens, CD10, or bcl-6, mimicking the phenotype of late germinal center/post germinal center activated B cells. 11 These phenotypes correlate well with their respective histomorphologic features and reflect the characteristics of classical Hodgkin lymphoma and diffuse large B-cell lymphoma. The fact that EBV infection was limited to the Hodgkin lymphoma suggests that EBV infection not only seems to be a critical event in malignant transformation in classical Hodgkin lymphoma but also has an important role in the up-regulation of activating markers such as CD30, bcl-2, and MUM-1 and down-regulation of B cell associated antigens such as CD10, CD20, CD79a, and PAX-5 in the Hodgkin lymphoma component of this clonally related composite lymphoma. 3,16,17,23,26,27 From the Division of Pathology, City of Hope National Medical Center, Duarte, CA. A B Image 4 Molecular studies of the 2 dissected components of the composite lymphoma demonstrate clonal immunoglobulin heavy chain gene rearrangements. The asterisks indicate 3 peaks representing the rearranged polymerase chain reaction products from *Fr3a (position 102), **Fr2a (position 258), and ***Fr2b (position 255) regions of immunoglobulin heavy chain gene, respectively. A, DNA from the dissected recurrent Hodgkin lymphoma component. B, DNA from the dissected diffuse large B-cell lymphoma component. 228 Am J Clin Pathol 2006;126: Downloaded 228 from
8 Hematopathology / CASE REPORT Address reprint requests to Dr Huang: Division of Pathology, City of Hope National Medical Center, 1500 E Duarte Rd, Duarte, CA References 1. Brauninger A, Hansmann ML, Strickler JG, et al. Identification of common germinal center B-cell precursors in two patients with both Hodgkin s disease and non-hodgkin s lymphoma. N Engl J Med. 1999;340: Caleo A, Sanchez-Aguilera A, Rodriguez S, et al. Composite Hodgkin lymphoma and mantle cell lymphoma: two clonally unrelated tumors. Am J Surg Pathol. 2003;27: de Leval L, Vivario M, De Prijck B, et al. Distinct clonal origin in two cases of Hodgkin s lymphoma variant of Richter s syndrome associated with EBV infection. Am J Surg Pathol. 2004;28: 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. 1991;96: Jaffe ES, Zarate-Osorno A, Kingma DW, et al. The relationship between Hodgkin s disease and non-hodgkin s lymphomas. Ann Oncol. 1994;5: Marafioti T, Hummel M, Anagnostopoulos L, et al. Classical Hodgkin s disease and follicular lymphoma originating from the same germinal center B cell. J Clin Oncol. 1999;17: Stein H, Delsol G, Pileri S, et al. Classical Hodgkin lymphoma. In: Jaffe ES, Harris NL, Stein H, et al, eds. Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; 2001: World Health Organization Classification of Tumours. 8. ven den Berg A, Maggio E, Rust R, et al. Clonal relation in a case of CLL, ALCL, and Hodgkin composite lymphoma. Blood. 2002;100: Zettl A, Rudiger T, Marx A, et al. Composite marginal zone B-cell lymphoma and classical Hodgkin s lymphoma: a clinicopathological study of 12 cases. Histopathology. 2005;46: Stein H, Hummel M. Cellular origin and clonality of classic Hodgkin s lymphoma: immunophenotypic and molecular studies. Semin Hematol. 1999;36: Bai M, Panoulas V, Papoudou-Bai A, et al. B-cell differentiation immunophenotypes in classical Hodgkin lymphomas. Leuk Lymphoma. 2006;47: Huang Q, Chang KL, Gaal K, et al. KSHV/HHV8 associated lymphoma simulating anaplastic large cell lymphoma. Am J Surg Pathol. 2004;28: Gong JZ, Zheng S, Chiarle R, et al. Detection of immunoglobulin κ light chain rearrangements by polymerase chain reaction: an improved method for detecting clonal B-cell lymphoproliferative disorders. Am J Pathol. 1999;155: Segal GH, Jorgensen T, Masih AS, et al. Optimal primer selection for clonality assessment by polymerase chain reaction analysis, I: low grade B-cell lymphoproliferative disorders of nonfollicular center cell type. Hum Pathol. 1994;25: Chang KL, Chen YY, Shibata D, et al. Description of an in situ hybridization methodology for detection of Epstein-Barr virus RNA in paraffin-embedded tissues, with a survey of normal and neoplastic tissues. Diagn Mol Pathol. 1992;1: Bechtel D, Kurth J, Unkel C, et al. Transformation of BCRdeficient germinal-center B cells by EBV supports a major role of the virus in the pathogenesis of Hodgkin and posttransplantation lymphomas. Blood. 2005;106: Kim LH, Nadarajah VS, Peh SC, et al. Expression of bcl-2 family members and presence of Epstein-Barr virus in the regulation of cell growth and death in classical Hodgkin s lymphoma. Histopathology. 2004;44: Huang JZ, Weisenburger DD, Vose JM, et al. Diffuse large B- cell lymphoma arising in nodular lymphocyte predominant Hodgkin lymphoma; a report of 21 cases from the Nebraska Lymphoma Study Group. Leuk Lymphoma. 2003;44: Braeuninger A, Kuppers R, Strickler JG, et al. Hodgkin and Reed-Sternberg cells in lymphocyte predominant Hodgkin disease represent clonal populations of germinal center derived tumor B cells. Proc Natl Acad Sci U S A. 1997;94: Foss HD, Reusch R, Demel G, et al. Frequent expression of the B-cell specific activator protein in Reed-Sternberg cells of classical Hodgkin s disease provides further evidence for its B-cell origin. Blood. 1999;94: Kanzler H, Kuppers R, Hansmann ML, et al. Hodgkin and Reed-Sternberg cells in Hodgkin s disease represent the outgrowth of a dominant tumor clone derived from (crippled) germinal center B-cells. J Exp Med. 1996;184: Kuppers R, Sousa AB, Baur AS, et al. Common germinal center B-cell origin of the malignant cells in two composite lymphomas, involving classical Hodgkin s disease and either follicular lymphoma or B-CLL. Mol Med. 2001;7: Tinguely M, Rosenquist R, Sundstrom C, et al. Analysis of a clonally related mantle cell and Hodgkin lymphoma indicates Epstein-Barr virus infection of a Hodgkin/Reed-Sternberg cell precursor in a germinal center. Am J Surg Pathol. 2003;27: Hummel M, Marafioti T, Stein H. Clonality of Reed-Sternberg cells in Hodgkin s disease [letter]. N Engl J Med. 1999;340: Vatabe Y, Oka K, Asai J, et al. Poor correlation between clonal immunoglobulin gene rearrangement and immunoglobulin gene transcription in Hodgkin s disease. Am J Pathol. 1996;149: Gandhi MK, Tellam JT, Khanna R. Epstein-Barr virus associated Hodgkin s lymphoma. Br J Haematol. 2004;125: Kingma DW, Medeiros LJ, Barletta J, et al. Epstein-Barr virus is infrequently identified in non-hodgkin s lymphoma associated with Hodgkin s disease. Am J Surg Pathol. 1994;18: Pans CP, Weisenburger DD, Greiner TC, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004;103: Downloaded from Am J Clin Pathol 2006;126:
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