Primary Mediastinal (Thymic) Large B-Cell Lymphoma
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1 Resident Short Review Primary Mediastinal (Thymic) Large B-Cell Lymphoma A Short Review With Brief Discussion of Mediastinal Gray Zone Lymphoma N (PMBCL) is a subtype of diffuse large B-cell lymphoma (DLBCL). It commonly presents as a bulky lesion in the anterior-superior mediastinum with symptoms related to local invasion or compression. Microscopic examination typically shows infiltration of medium-large cells surrounded by collagen fibrosis. The neoplastic cells express B-cell markers, and CD30 often shows heterogeneous staining. Comparative genomic hybridization has identified gains in loci of 9p24 and 2p15 as well as Xp and Xq Amplification of REL and BCL11A at 2p as well as elevated expression of JAK2, PDL1, and PDL2 at 9p has been demonstrated. Nodular sclerosis classic Hodgkin lymphoma needs to be differentiated from PMBCL and cases with overlapped features have been described as mediastinal gray zone lymphoma. Primary mediastinal (thymic) large B-cell lymphoma carries a favorable prognosis in comparison to conventional DLBCL. (Arch Pathol Lab Med. 2011;135: ) (PMBCL) is a subtype of diffuse large B-cell lymphoma (DLBCL) arising in the thymus. It accounts for approximately 5% of non-hodgkin lymphomas. 1,2 First described in the 1980s, 3 it tends to occur in younger adults with female predominance; the median age ranges from 30 to 40 years and the male to female ratio is about 1:2. 1 While the thymic medullary B cell is thought to be the normal counterpart of PMBCL, the pathogenesis of this neoplasm remains to be elucidated despite many experimental studies. Overlapping expression signatures of PMBCL and classic Hodgkin lymphoma, nodular sclerosis type (chl-ns), have been demonstrated, raising the possibility of linkage between these 2 neoplasms. 4,5 We review the clinical presentation, histopathology, pathogenesis, and management of PMBCL with a brief discussion of mediastinal gray zone lymphoma (MGZL). Accepted for publication March 3, From the Department of Pathology, Duke University Medical Center, Durham, North Carolina. The authors have no relevant financial interest in the products or companies described in this article. Reprints: Charles Blake Hutchinson, MD, Department of Pathology, DUMC Box 3712, Duke University Medical Center, Durham, NC ( blake.hutchison@duke.edu). Charles Blake Hutchinson, MD; Endi Wang, MD, PhD CLINICAL FEATURES usually presents as a bulky lesion in the anterior-superior mediastinum. The symptoms are usually related to local invasion or compression 6 and include dyspnea, cough, chest pain, and dysphagia. Hoarseness is frequently present due to laryngeal or phrenic nerve palsy. Patients will often show signs of venous obstruction, most frequently in the superior vena cava. Radiographic imaging usually reveals enlarged mediastinal contours in the anterior-superior compartment (Figure 1). Owing to lymphatic blockage or the direct invasion of local organs, pleural effusion and/or pericardial effusion are sometimes seen. The mass tends to be confined to the thorax without involvement of lymph nodes or other lymphoid organs at initial diagnosis. Extrathoracic or extranodal involvement is more frequent at relapse. Bone marrow involvement is extremely rare, even in cases of recurrence. 1 HISTOPATHOLOGY Fluoroscopy- or computed tomography guided needle biopsies often yield sufficient tissue for diagnostic workup, providing paraffin-fixed tissue sections for histologic examination and immunohistochemical analysis. Microscopic examination typically shows sclerotic fibrosis with an infiltration of intermediate to large lymphoid cells. The infiltrating cells are often entrapped in compartments surrounded by collagen fibrosis, forming so-called compartmentalizing alveolar fibrosis (Figure 2, A). These infiltrating cells have variable nuclear features ranging from regular, round nuclear contours to irregular, multilobulated forms. In addition, they usually contain prominent pale to clear cytoplasm. In certain cases, the neoplastic cells have pleomorphic nuclei with large prominent eosinophilic nucleoli resembling Reed-Sternberg cells or their variants. In addition, some have abundant clear cytoplasm reminiscent of so-called lacunar cells seen in chl-ns (Figure 2, B). While thymic remnants may be seen focally, a lobular thymic architecture with Hassall corpuscles is typically absent. By immunohistochemistry, the neoplastic cells are commonly positive for B-cell antigen markers, including CD20 (Figure 2, C) and CD79a. They are also frequently positive for MUM1 (75%), BCL6 (46%), BCL2 (78%), and CD23 (70%). 7,8 CD10 staining is variable. 7 Staining with CD30 is seen in more than 80% of cases but often at low levels and with heterogeneous 394 Arch Pathol Lab Med Vol 135, March 2011 Primary Mediastinal Large B-Cell Lymphoma Hutchinson & Wang
2 Figure 1. Chest computed tomography scan. At the level of the aortic arch, there is a lobulated mass in the anterior mediastinum. staining intensity (Figure 2, D).7,9 CD15 staining is typically negative.7 The B-cell transcriptional factors BOB.1, OCT-2 (Figure 2, E), and PU.1 are also expressed7 and the proliferation index may vary from 10% to 60% by Ki-67 staining.10 LABORATORY STUDIES In most cases, flow cytometric analysis demonstrates an abnormal B-cell population expressing CD19 and CD22, in addition to the markers detected by immunohistochemical analysis as stated above. Despite the expression of multiple mature B-cell antigens, the neoplastic cells typically display defective production of surface immunoglobulins.11 Thus, the monoclonal nature cannot be assessed by evaluation of surface k and l light chains. In some cases, neoplastic B cells are completely absent, probably owing to destruction during tissue preparation or to a poor yield because of sclerotic fibrosis. Cytogenetics generally detects a diploid karyotype and gains of chromosome arms 9p and 2p have been identified with comparative genomic hybridization. In addition, gains in Xp and Xq24-26 have been reported.12 Immunoglobulin genes in the neoplastic cells are clonally rearranged, as shown by southern blot analysis of fresh tissue or polymerase chain reaction (PCR) based studies of fresh or formalin-fixed, paraffin-embedded tissue. One study13 demonstrated 8 of 13 cases with lymphomaspecific immunoglobulin transcripts that almost invariably lacked immunoglobulin protein expression. These Figure 2. A, Infiltrating cells entrapped in compartments surrounded by collagen fibrosis, forming so-called compartmentalizing alveolar fibrosis. B, Lacunar cells are seen in a background of smaller lymphocytes. C, Large cells are positive for CD20 (original magnification 3400). D, Many large cells are positive for CD30 with typical membrane Golgi zone staining pattern (original magnification 3400). E, Large cells are positive for OCT-2 with nuclear staining (original magnification 3400) (hematoxylin-eosin, original magnifications 3600 [A] and 3100 [B]). Arch Pathol Lab Med Vol 135, March 2011 Primary Mediastinal Large B-Cell Lymphoma Hutchinson & Wang 395
3 findings suggest the immunoglobulin-negative phenotype of PMBCL may be extrinsically regulated. Interphase fluorescence in situ hybridization has identified amplifications of REL and BCL11A at 2p, 12,14 while gene expression array analysis showed an elevated expression of JAK2, PDL1, and PDL2 at 9p. 4,15 Of note, delayed degradation of JAK2 has been suggested by others. 16 Unlike other B-cell neoplasms, rearrangements of BCL2, BCL6, and MYC genes are absent to rare in PMBCL. 4 REL gene, which encodes a protein belonging to the NF-kB family, seems to promote cell survival and inhibit apoptosis in PMBCL. 17 BCL11A encodes a zinc finger transcriptional repressor essential to lymphoid development. JAK2 encodes a protein involved in the JAK/STAT cytokine-dependent signaling pathway, which regulates cell growth and survival. PDL1 and PDL2 (which encode regulators for T-cell response) are overexpressed in PMBCL. Particularly, overexpression of PDL2 in PMBCL is considered a discriminating factor from conventional DLBCL. 18 The target genes MAL and FIG1 have been identified on gene expression profiling of PMBCL and are both shown to have significantly enhanced expression as compared with that in conventional DLBCL. 4 While the mechanism of PMBCL remains unclear, investigation of the pathogenesis has been focused on uncontrolled cell proliferation, enhanced cell survival, and disrupted cell differentiation. 4,15 18 DIFFERENTIAL DIAGNOSIS The clinical differential diagnosis of an anterior-superior mediastinal mass includes thymoma, lymphoma, germ cell tumors, and lung carcinoma. Histopathologic examination can generally exclude nonlymphoid neoplasms. Among lymphoid lesions, the separation of PMBCL and chl-ns is often problematic. Morphologic and immunophenotypic overlap between these 2 entities has been increasingly recognized, resulting in so-called mediastinal gray zone lymphoma. Other lymphomas in the differential diagnosis include conventional DLBCL with involvement of mediastinal lymph nodes, anaplastic large cell lymphoma (ALCL), and lymphoblastic lymphoma, especially precursor T cell type. Classic Hodgkin Lymphoma and Mediastinal Gray Zone Lymphoma and chl-ns, which both commonly occur in the anterior mediastinum, demonstrate many overlapping features including similar clinical presentation, similar anatomic location, and B-cell origin. In addition to a sclerotic background, chl-ns often demonstrates lacunar cells that often form aggregates as a subtype known as syncytial variant cells. Given that PMBCL is usually positive for CD30, distinction from a syncytial variant chl-ns is essential. In general, chl tends to lose some or all B-cell antigens and is frequently negative for CD45, whereas PMBCL is usually positive for these antigen markers (Table). In addition, approximately 80% of chls express CD15, a relatively specific antigen marker for chl, which is usually not expressed in PMBCL. Immunohistochemical panels including B-cell antigen markers such as OCT-2, BOB.1, PAX-5, and PU.1 are useful. chl and PMBCL carry distinct prognostic and therapeutic implications, emphasizing the need for separation of these 2 entities in diagnostic practice. Comparison of Immunophenotype Between Primary Mediastinal Large B-Cell Lymphoma (PMBCL) and Classic Hodgkin Lymphoma, Nodular Sclerosis Type (chl-ns) Antigen PMBCL chl-ns CD30 +/2 + CD15 2 +/2 CD20 + 2/+ CD79a + 2/+ PAX OCT BOB PU MAL + 2 c-rel + 2 Abbreviations: +, positive in more than 90% of the cases; +/2, positive in most cases; 2/+, positive in minority of the cases; 2, negative. There remain cases of mediastinal lymphoma of B-cell lineage that cannot be definitively classified despite extensive phenotypic and molecular studies. For instance, some cases are morphologically suggestive of chl-ns but are immunophenotypically consistent with PMBCL. By contrast, other cases may show a range of morphology in places suggestive of PMBCL but with immunophenotype typical for chl-ns. These cases have been called mediastinal gray zone lymphoma 16 and were recently categorized as B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and classical Hodgkin lymphoma in the 2008 World Health Organization classification. 19 Rare cases with concurrent and/or sequential PMBCL and chl have been reported and a common clonal origin has been documented with PCR-based immunoglobulin gene rearrangement studies in these cases. 20 These findings suggest a biologic continuum or transition between PMBCL and chl. The workup of MGZL may involve evaluation by histopathologic, immunohistochemical, and molecular analysis. The neoplastic cells often have morphologic features reminiscent of lacunar cells, frequently seen in chl-ns, which show a confluent sheetlike growth pattern in a fibrotic stroma. The cytologic features may show great variation in size and pleomorphism. The background cellularity may be mixed and eosinophils may be seen. Necrosis is common. 19 Immunohistochemically, the lymphoma cells demonstrate a phenotype with overlapping features of chl-ns and PMBCL. For instance, expression of CD20 and CD79a within the lymphoma population may be present concomitantly with CD30 as well as CD15. In addition, the B- cell markers OCT-2 and BOB.1 are often expressed. 19 At the molecular level, gene expression array analysis has shown that the expression profile in PMBCL is similar but not identical to that of chl. Expression of certain genes has been shown to be enhanced in PMBCL when compared to chl, 21 though the complexity of such assays precludes application in the clinical laboratory for diagnostic purposes. The importance of distinguishing MGZL from chl and PMBCL is underscored by its distinct clinical behavior. Mediastinal gray zone lymphoma follows a more aggressive clinical course and carries a worse prognosis than both chl and PMBCL. 20 Some studies 19 have suggested that more aggressive treatment, similar to that of conventional DLBCL, may be of benefit, while others Arch Pathol Lab Med Vol 135, March 2011 Primary Mediastinal Large B-Cell Lymphoma Hutchinson & Wang
4 have suggested that a therapeutic regimen more similar to that of chl may be beneficial. There is currently no consensus on the optimal treatment and further study is warranted. 20 Conventional Diffuse Large B-Cell Lymphoma Involving Mediastinal Lymph Nodes Nodal or extrathoracic DLBCL can occasionally involve mediastinal lymph nodes. Histopathologic distinction of this entity from PMBCL is difficult, because of the similar morphology and immunophenotypic profile between these 2 B-cell neoplasms. In addition, DLBCL may occasionally lack surface immunoglobulin expression, similar to PMBCL. Recent studies with gene expression array analysis 4,5 demonstrated a molecular signature in PMBCL that was different from that of other DLBCLs, particularly the expression levels in JAK2, TRAF1, MAL, REL, and PDL2. Practically, the distinction would largely rely on the clinical presentation and radiographic survey for possible extrathoracic presentation. Anaplastic Large Cell Lymphoma As in PMBCL, ALCL usually has CD30 expression. While the staining of CD30 is usually weak and often heterogeneous in PMBCL, the expression is usually more uniform and strong in ALCL. Use of immunohistochemical stains for B-cell lineage, such as PAX-5, often clarifies the diagnosis without further workup. In addition, many ALCLs harbor t(2;5) or other variant rearrangements of the ALK1 gene. Anaplastic large cell lymphoma usually shows T-cell receptor gene rearrangement in a monoclonal fashion detected by Southern blot analysis or PCR-based assay. 23 Lymphoblastic Lymphoma Precursor T-cell lymphoblastic lymphoma often presents with an anterior-superior mediastinal mass. In contrast to PMBCL, the neoplastic cells in lymphoblastic lymphoma have a monomorphic, blastic appearance and their precursor T-cell immunophenotype can be identified without trouble by flow cytometric analysis or immunohistochemical studies. 24 TREATMENT AND PROGNOSIS carries a relatively favorable prognosis in comparison to conventional DLBCL. 15 Some studies 5,15,21 have shown that a particular molecular signature, similar to that seen in Hodgkin lymphoma, is also associated with a better survival. Cases with extension to adjacent organs or thoracic structures, pleural or pericardial effusion, or poor performance status have been associated with unfavorable clinical outcome. The optimal treatment of PMBCL is unknown at present. Response to therapy with cyclophosphamide, adriamycin, vincristine, and prednisone (CHOP regimen) in PMBCL has been based on the protocol used for conventional DLBCL. 15,18 Response to the CHOP regimen in PMBCL is comparable to that in conventional DLBCL, although 1 retrospective analysis demonstrated possible superior outcomes achieved with the thirdgeneration chemotherapy regimens. The addition of rituximab to chemotherapy for PMBCL seems to have a favorable impact according to some studies. 18 In cases of relapse, high-dose chemotherapy supported by autologous stem cell transplantation has been considered as the choice once a second remission is to be achieved. The role of mediastinal radiotherapy upon completion of chemotherapy remains a subject of debate, considering the potential long-term toxicity to the heart and lung. The complete remission rate ranges from 40% to 80%, and the overall 5-year survival is 50% to 80%. 25 CONCLUSION is a DLBCL arising in the mediastinum from thymic B cells. Often presenting as an anterior mediastinal mass, symptoms are related to local invasion and compression. Medium to large neoplastic cells surrounded by collagen fibrosis ( compartmentalizing alveolar fibrosis ) show expression of B-cell markers as well as heterogeneous CD30 expression. Immunoglobulin is not expressed, probably owing to defective protein production. Distinction of PMBCL from chl is important for prognostic and therapeutic reasons. Occasionally, however, there is considerable overlap of histologic and phenotypic features with chl-ns, resulting in so-called mediastinal gray zone lymphoma. Primary mediastinal (thymic) large B- cell lymphoma carries a favorable prognosis in comparison to conventional DLBCL. References 1. Cazals-Hatem D, Lepage E, Brice P, et al. Primary mediastinal large B-cell lymphoma: a clinicopathologic study of 141 cases compared with 916 nonmediastinal large B-cell lymphomas, a GELA ( Groupe d Etude des Lymphomes de l Adulte ) study. Am J Surg Pathol. 1996;20(7): Barth TF, Leithäuser F, Joos S, et al. Mediastinal (thymic) large B-cell lymphoma: where do we stand? Lancet Oncol. 2002;3(4): Lichtenstein AK, Levine A, Taylor CR, et al. Primary mediastinal lymphoma in adults. Am J Med. 1980;68(4): Savage KJ, Monti S, Kutok JL, et al. The molecular signature of mediastinal large B-cell lymphoma differs from that of other diffuse large B-cell lymphomas and shares features with classical Hodgkin lymphoma. Blood. 2003;102(12): Rosenwald A, Wright G, Leroy K, et al. Molecular diagnosis of primary mediastinal B cell lymphoma identifies a clinically favorable subgroup of diffuse large B cell lymphoma related to Hodgkin lymphoma. J Exp Med. 2003;198(6): Lazzarino M, Orlandi E, Paulli M, et al. Treatment outcome and prognostic factors for primary mediastinal (thymic) B-cell lymphoma: a multicenter study of 106 patients. J Clin Oncol. 1997;15(4): Pileri S, Zinzani P, Gaidano G, et al. Pathobiology of primary mediastinal B- cell lymphoma. Leuk Lymphoma. 2003;44(suppl 3):S21 S Calaminici M, Piper K, Lee AM, et al. CD23 expression in mediastinal large B-cell lymphomas. Histopathology. 2004;45(6) Higgins JP, Warnke RA. CD30 expression is common in mediastinal large B-cell lymphoma. Am J Clin Pathol. 1999;112(2): Möller P, Lämmler B, Eberlein-Gonska M, et al. Primary mediastinal clear cell lymphoma of B-cell type. Virchows Arch A Pathol Anat Histopathol. 1986; 409(1): Pileri SA, Gaidano G, Zinzani PL, et al. Primary mediastinal B-cell lymphoma: high frequency of BCL-6 mutations and consistent expression of the transcription factors OCT-2, BOB.1, and PU.1 in the absence of immunoglobulins. Am J Pathol. 2003;162: Joos S, Otaño-Joos MI, Ziegler S, et al. Primary mediastinal (thymic) B-cell lymphoma is characterized by gains of chromosomal material including 9p and amplification of the REL gene. Blood. 1996;87(4): Leithauser F, Bauerle M, Huyhn MQ, et al. Isotype-switched immunoglobulin genes with a high load of somatic hypermutation and lack of ongoing mutational activity are prevalent in mediastinal B-cell lymphoma. Blood. 2001; 98(9): Weniger MA, Pulford K, Gesk S, et al. Gains of the proto-oncogene BCL11A and nuclear accumulation of BCL11A(XL) protein are frequent in primary mediastinal B-cell lymphoma. Leukemia. 2006;20(10): Savage KJ. Primary mediastinal large B-cell lymphoma. Oncologist. 2006; 11(5): Melzner I, Bucur AJ, Brüderlein S, et al. Biallelic mutation of SOCS-1 impairs JAK2 degradation and sustains phospho-jak2 action in the MedB-1 mediastinal lymphoma line. Blood. 2005;105(6): Feuerhake F, Kutok JL, Monti S, et al. NF kappa B activity, function, and target-gene signatures in primary mediastinal large B-cell lymphoma and diffuse large B-cell lymphoma subtypes. Blood. 2005;106(4): Johnson PW, Davies AJ. Primary mediastinal B-cell lymphoma. Hematology Am Soc Hematol Educ Program. 2008;2008: Arch Pathol Lab Med Vol 135, March 2011 Primary Mediastinal Large B-Cell Lymphoma Hutchinson & Wang 397
5 19. Jaffe ES, Stein H, Swerdlow SH, et al. B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and classical Hodgkin lymphoma. In: Swerdlow SH, Campo E, Harris NL, et al, eds. Tumours of Haematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; 2008: World Health Organization Classification of Tumours; vol Traverse-Glehen A, Pittaluga S, Gaulard P, et al. Mediastinal gray zone lymphoma: the missing link between classic Hodgkin s lymphoma and mediastinal large B-cell lymphoma. Am J Surg Pathol. 2005;29(11): Calvo KR, Traverse-Glehen A, Pittaluga S, Jaffe ES. Molecular profilingprovides evidence of primary mediastinal large B-cell lymphoma as a distinct entity related to classic Hodgkin lymphoma: implications for mediastinal gray zone lymphomas as an intermediate form of B-cell lymphoma. Adv Anat Pathol. 2004;11(5): Cazals-Hatem D, Andre M, Mounier N, et al. Pathologic and clinical features of 77 Hodgkin s lymphoma patients treated in a lymphoma protocol (LNH87): a GELA study. Am J Surg Pathol. 2001;25(3): Stein H, Foss HD, Durkop H, et al. CD30+ anaplastic large cell lymphoma: a review of its histopathologic, genetic, and clinical features. Blood. 2000;96(12): Borowitz MJ, Chan JKC. T lymphoblastic leukemia/lymphoma. In: Swerdlow SH, Campo E, Harris NL, et al, eds. Tumours of Haematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; 2008: World Health Organization Classification of Tumours; vol Martelli M, Ferreri AJ, Johnson P. Primary mediastinal large B-cell lymphoma. Crit Rev Oncol Hematol. 2008;68(3): Submissions Now Accepted for CAP 11 Abstract Program Abstracts and case studies are now being accepted for the College of American Pathologists (CAP) 2011 meeting, which will be held September 11th through the 14th in Grapevine, Texas. Submissions for the CAP 11 Abstract Program will be accepted through Friday, April 1, Accepted submissions will appear in the September 2011 issue of the Archives of Pathology & Laboratory Medicine. Visit the CAP 11 Web site at for specific abstract program information. 398 Arch Pathol Lab Med Vol 135, March 2011 Primary Mediastinal Large B-Cell Lymphoma Hutchinson & Wang
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