Morphological Definitions of Burkitt's Lymphoma

Classical:
The classical form of BL is seen in most endemic cases, and in a high percentage of sporadic BL cases, particularly in children.³ The medium-sized cells show a diffuse monotonous pattern of infiltration, although in rare instances colonization of germinal centers is identified.⁴ Sometimes after fixation the cells exhibit squared off borders with retracted cytoplasm and may appear cohesive, particularly in mercury-based fixatives. The nuclei are round with clumped chromatin and relatively clear parachromatin, and contain multiple basophilic medium sized, centrally situated nucleoli.^4-6 The cytoplasm is deeply basophilic and usually contains lipid vacuoles. Such cellular details are better perceived in imprints. The tumor has a high mitotic rate as well as a high rate of spontaneous cell death, leading to a starry sky pattern. The nuclei of the tumor cells approximate in size those of the admixed starry-sky histiocytes. Some cases can be associated with an epithelioid granulomatous reaction, a process that tends to be seen in patients with localized disease and good prognosis.⁷

BL with plasmacytoid differentiation
In this variant the tumor cells are often eccentrically located, with basophilic cytoplasm.⁸ Cells with single central nucleoli can be observed. Evidence of plasmacytoid differentiation is evidenced by monotypic intracytoplasmic immunoglobulin. This variant is more common in immunodeficiency states, such as HIV-associated BL, is often EBV-positive.⁹

Atypical BL
This variant is predominantly composed of medium-sized Burkitt cells and shows other features of BL (high degree of apoptosis, high mitotic index). However, in contrast to classical BL, the cells show greater pleomorphism in nuclear size and shape. Nucleoli are more prominent and fewer in number. The diagnosis requires a growth fraction of 100%, and the appropriate immunophenotype for BL. Because of imprecision in the cytological features, molecular studies to identify a c-myc translocation are highly desirable, if not required, for diagnosis.

The terminology of Burkitt-like lymphoma has been used both for cases of BL with variable cytology, as well as other high grade B-cell lymphomas resembling BL.¹⁰ The term Burkitt-like lymphoma was included in the REAL classification as a provisional category, and at the time, it was felt that criteria to distinguish atypical BL from DLBCL were not mature.^11,12 With additional data now available, the WHO classification recommended the use of the term "atypical BL" as being more precise.¹³ Similarly, the working formulation contained the category of "small non-cleaved cell lymphoma, non-Burkitt".¹⁴ This category was morphologically, not immunophenotypically defined, and was very heterogeneous. It was used for a wide variety of lymphoma types including atypical variants of BL, DLBCL composed of small centroblasts, the paraimmunoblastic variant of CLL/SLL, and even some peripheral T-cell lymphomas composed of medium-sized blasts.¹⁵ Most lymphomas classified as "small non-cleaved, non-Burkitt's" lacked evidence of the c-myc rearrangement.¹⁶

Clinical Variants of Burkitt's Lymphoma

Endemic BL
Burkitt's lymphoma was originally described in equatorial Africa, where it is the most common malignancy of childhood.^17,18 It has a peak incidence peak at 4 to 7 years and a male to female ratio of 2 to 1. In endemic regions there is a correlation between the geographical occurrence and some climatic factors (rainfall, altitude, etc), which correspond to the geographical distribution of endemic malaria. Endemic BL is Epstein-Barr virus (EBV) -positive in virtually 100% of cases. With the advent of the AIDS epidemic in Africa, the picture of BL in Africa has become more complex. A higher proportion of cases are now seen in adults, associated with HIV-infection.^19,20

Sporadic BL
Sporadic BL is seen throughout the world, mainly in children and young adults. The incidence is low, 1 to 2% of all lymphomas in Western Europe and in USA. BL accounts for approximately 30 to 50% of all childhood lymphoma. The median age of the adult patients is about 30 years.²¹ The male to female ratio is about 2 or 3 to 1. In some parts of the world, e.g. in South America and North Africa, the incidence is intermediate between true sporadic and endemic subtypes. Low socio-economic status and early EBV infection are associated with a higher prevalence of EBV positive BL, even in non-endemic regions.

Immunodeficiency associated BL
This subtype is seen primarily in association with HIV infection, occurring often as the initial manifestation of AIDS.^22-24 EBV is identified in 25 to 40% of the cases, usually associated with plasmacytoid features. BL is less often seen in other immunodeficiency states.

BL in Leukemic Phase
Some cases of BL may present with bone marrow and peripheral blood involvement, without detectable tumor masses.²⁵ This form of BL was included in the FAB leukemia classification as the L3 variant of acute lymphoblastic leukemia.²⁶ However, like other forms of BL, the cells have a mature B-cell phenotype. This clinical presentation can be seen in a variety of clinical setting, including pediatric patients and HIV-infection.^27,28

Immunophenotype of BL
BL has a mature B-cell phenotype with expression of CD19, CD20, CD22 and CD79a. The cells express surface IgM, with no predilection for kappa or lambda light chains. CD10 is consistently positive, and Bcl-2 protein is always negative in classical BL.²⁹ BCL-6 nuclear positivity is seen, consistent with a germinal center origin.³⁰ The growth fraction with Ki-67 should be 100% of the viable cells.³¹ CD21 positivity has been described in endemic but not sporadic BL; CD21 is the EBV-viral receptor.^4,32 BL usually has a very monomorphous appearance with few or no background inflammatory lymphocytes. Thus, CD3 stains only few cells. This appearance differs from that seen in most diffuse large B-cell lymphomas (DLBCL).

Genetics of BL
The cells have clonal rearrangements of the immunoglobulin (Ig) heavy and light chain genes, with somatic mutation of the Ig genes, consistent with a germinal center stage of differentiation.^33,34 The molecular hallmark of BL is a translocation of C-MYC at band q24 from chromosome 8 to the Ig heavy chain region on chromosome 14 [t(8;14)] at band q32 or less commonly to light chain loci on 2q11 [t(2;8)] or 22q11[t(8;22)].^35,36 In endemic cases, the breakpoint on chromosome 14 involves the heavy chain-joining region (early B-cell) whereas in sporadic cases, the translocation involves the Ig switch region (later stage of B-cell).³⁷ The C-MYC gene is constitutively expressed secondary to the influence of the promoters of the Ig genes on chromosomes 14, 2 or 22, encoding for immunoglobulin heavy chain, or the light chains lambda or kappa, respectively. Classical cytogenetics, FISH, or Southern blot hybridization can detect c-myc translocations.³⁸ PCR-based strategies are generally not effective, due to variations in the breakpoints.³⁹ The deregulation of c-myc influences both cellular proliferation and apoptosis. Mutations in c-myc may further enhance its tumorigenicity.^40,41 . Other genetic lesions in BL include inactivation of p53, in up to 30% of sporadic and endemic BL.^42,43 p53 expression is associated with a worse prognosis.

EBV genomes can be demonstrated in the tumor cells in nearly all endemic cases and in 25-40% of immunodeficiency-associated cases, but are less frequent in sporadic cases (<30%). The frequency of EBV in sporadic BL correlates with age of initial infection and socio-economic status. ⁴⁴ A latency I phenotype is seen, with expression of EBNA1, but without expression of other latency genes (LMP-1 negative.)⁴⁵

Differential Diagnosis

Diffuse Large B-cell Lymphoma (DLBCL)
Some cases of DLBCL have a high proliferative fraction and a prominent starry sky, raising the differential diagnosis with atypical variants of BL. Because a diagnosis of BL has therapeutic implications, usually necessitating more aggressive treatment approaches, it is important to differentiate among these conditions. The cells of DLBCL are larger, more variable in appearance, with more open chromatin and more prominent eosinophilic nucleoli. The cytologic appearance is typically that of a centroblast. One should not be dissuaded from making a diagnosis of DLBCL, even if the centroblasts are smaller than typically seen. In DLBCL there is usually a more prominent stromal reaction, with increased numbers of background lymphocytes.

Immunophenotypically, the cells have a growth fraction usually less than 100% with Ki-67, and may be Bcl-2-positive and CD10-negative. ^29,46,47 However, a Bcl-2-negative/ CD10-positive phenotype can be seen in some cases of DLBCL. In DLBCL the expression of CD10 correlates with the presence of a BCL-2 rearrangement.^48,49 A c-myc translocation may be seen in DLBCL, with or without a BCL-2 rearrangement.^50,51 Cases bearing a "double-hit" (BCL-2 and C-MYC translocation positive) have an especially poor prognosis.^52,53

C-MYC translocation in other B-cell malignancies
While the C-MYC translocation is the hallmark of BL, it may occur as a secondary event in other lymphomas, including follicular lymphoma, mantle cell lymphoma, and DLBCL.^52,54 In follicular lymphoma, secondary C-MYC translocations have been associated with high grade transformations showing Burkitt-like and lymphoblastic cytologies. ^55-57 Mantle cell lymphomas with C-MYC deregulation are aggressive or blastic in appearance.⁵⁸

Lymphoblastic Lymphoma/ Leukemia (LBL)
Especially in children, the differential diagnosis of BL may include precursor B-cell and precursor T-cell lymphoblastic lymphoma/ leukemia.⁵⁹ LBL are composed of blast cells with finely distributed chromatin, inconspicuous nucleoli, and sparse cytoplasm. While pre-B LBL are CD10-positive, the cells generally lack CD20 and surface immunoglobulin, and are TDT-positive. ⁶⁰

Acknowledgement:
This review is based on the WHO description of Burkitt Lymphoma, as published in the WHO monograph. I would like to acknowledge the contributions of Drs. Jacques Diebold and Martine Raphael, who were primarily responsible for preparing that chapter for publication. (J. Diebold, E.S. Jaffe, M. Raphael, R.A. Warnke: Burkitt Lymphoma, pp. 181-184, in Jaffe ES, Harris NL, Stein H, Vardiman J. Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. World Health Organization Classification of Tumours. Lyon, France: IARC Press; 2001)

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