Classical Burkitt Lymphoma and Variants: Strategies for Accurate Diagnosis
Elaine S. Jaffe
National Cancer Institute, NIH
The WHO classification recognizes several variants of Burkitt's lymphoma (BL), all of which share
deregulation of the c-myc gene leading to the characteristic histological and clinical features of
BL.1 This molecular lesion results in a high grade lymphoma which, in addition to a growth
fraction of 100%, is associated with certain clinical features, such as a risk of central nervous
involvement, that necessitate therapeutic strategies distinct from diffuse large B-cell lymphoma
(DLBCL).2 The three clinical variants of BL are associated with different clinical settings:
endemic BL, sporadic BL, and AIDS-associated BL. In addition, three
morphological variants are defined: classical BL, atypical BL, and BL with
plasmacytoid differentiation. The last variant is most often seen in association with
HIV-infection, whereas the other two variants can be encountered in both endemic and sporadic clinical
settings. The distinction of Burkitt's lymphoma (BL) from morphologically similar aggressive B-cell
lymphomas has been problematic for pathologists and clinicians. The category of small non-cleaved cell
lymphoma, non-Burkitt, in the working formulation was biologically and clinically heterogeneous. In
addition, the c-myc translocation as a secondary event is not associated with identical clinical
consequences. Current strategies use immunophenotypic and molecular methods to diagnose BL as a
homogeneous biological and clinical entity.
Morphological Definitions of Burkitt's Lymphoma
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
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
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 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
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
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
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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