Sporadic Burkitt lymphomas of children and adolescents in Chinese: a clinicopathological study of 43 cases
© Bi et al.; licensee BioMed Central Ltd. 2012
Received: 8 April 2012
Accepted: 22 June 2012
Published: 22 June 2012
To investigate the clinical and pathologic features as well as the MYC translocations of childhood Burkitt lymphoma (BL) from China.
Fourty-three cases of childhood BL were retrospectively investigated in morphology, immunophenotype, genotype, treatments and survival analysis.
Clinically, there was a marked male predominance in sex distribution (M: F = 9.75:1); abdomen was the most frequent extranodal sites of involvement (46.5 %), followed by jaws and facial bones (16.3 %). Two third of the patients were in stageI ~ II. Morphologically, 69.76 % of the cases showed classical histologic features, while 30.24 % of them showed greater nuclear pleomorphism in size and shape. Five cases (11.6 %) were positive for EBER1/2. Thirty-one of the 40 cases (77.5 %) had the aberration of IGH/MYC translocation while 7 (17.5 %) had non-IGH/MYC translocation. Thirty patients (69.7 %) received operation and/or chemotherapy while 13 patients (30.3 %) received no treatment. Twenty-seven patients (62.8 %) died of the tumor, 16 alive, with the average survival time 4.9 and 48.7 months respectively. High IPI, advanced clinical stage, increased serum level of LDH and no chemotherapy received as well as tumor size ≥10 cm were related to the lower survival rates of the tumor.
Several differences were showed in this group of BL, including a much higher ratio of male patients, more cases in stageII, clinically inconsistent treatment and a very poor outcome.
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Burkitt lymphoma (BL) is defined by the updated WHO classification (2008) as a B-cell lymphoma with an extremely short doubling time that often presents in extranodal sites or as an acute leukemia . BL is a highly aggressive non-Hodgkin lymphoma (NHL) and characterized by C-MYC translocation. Three clinical variants of BL are recognized, including endemic BL, sporadic BL and immunodeficiency-associated BL. Sporadic BL is seen throughout the world, mainly in children and adolescents. Histologically, BL is characterized by diffuse infiltration of monomorphic medium-sized neoplastic cells with basophilic cytoplasm and numerous mitotic figures; some cases may have tumor cells with greater pleomorphism in shape and nuclear size, which was designated as “atypical BL” or “Burkitt like lymphoma” . Although the incidence of BL is low, accounting for only 1 ~ 2 % of all lymphomas in western countries, it is one of the most common types of malignant tumors in children and young adults . In the past decades, there were many reports of sporadic BL, including cases from Asian countries and areas [3, 4], However, only a few cases of Chinese BL has been reported in the English literature. In this study, 43 cases of BL of children and adolescents from southwest China were retrospectively investigated for the clinical and pathological features.
Patients and methods
Sixty cases of initially diagnosed Burkitt lymphoma of children and adolescents (age ≤18 years) were received from the Department of Pathology, West-China Hospital of Sichuan University between 1990 and 2006. The specimens fixed in 10 % neutral formalin (pH 7.2), were processed by routine methods and embedded in paraffin. All cases were reviewed by two expert heamatopathologists individually. The criteria used to select the cases were as follows: (1) cases diagnosed as Burkitt lymphoma (BL) with a typical growth pattern and a high proliferation index (PI) as established by Ki-67 staining (in general, >90 % nuclei positivity), occasionally with a some degree of pleomorphism in nuclear size and shape, in accordance with WHO classification (2008) ; (2) The neoplastic cells expressed B-cell differentiation antigens (CD20), germinal center markers of CD10 and /or BCL-6 but not BCL-2. 17 of 60 cases were excluded because of insufficient materials for further studies. Thus, total 43 cases were included in current study. The clinical history of each patient was reviewed for age at diagnosis, gender, number and location of the tumor, staging, performance status, treatment regimens, complete blood count (CBC), bone marrow aspiration/biopsy, serum level of lactate dehydrogenase (LDH) and international prognostic index (IPI). The staging was according to the system proposed by Murphy and Hustu and modified by Magrath . The protocol of this study was approved by the Institutional Review Board or ethical committee of West China Hospital of Sichuan University.
Immunohistochemistry was performed on paraffin embedded tissue sections using the Envision method (Dako, Gene Ltd, China). Antigen retrieval techniques were applied as needed for each specific antibody. The following antibodies were used: CD20, CD45RO, CD10, BCL-6 (Zymed, Zhongshan, China); CD3ϵ, BCL-2, C-myc and TdT and Ki-67 (Neumarkers, Maixin, China). DAB was used as a substrate and the positive signal was dark brown in color. The Ki-67 stain was assigned a percentage value that was calculated by positive nuclei staining per 1000 tumor cell nuclei in each case.
In situ Hybridization for Epstein-Barr virus (EBV) encoded RNA
In situ hybridization (ISH) was carried out with a fluorescence-labeled oligonucleotide probe complementary to two Epstein-Barr virus-encoded small RNAs, EBER-1 and EBER-2 (EBER1/2, Dako, Denmark, No.Y520001). Rabbit anti-FITC antibody conjugated with alkaline phosphatase (Dako, Denmark) was used to combine with the probe, whereas NBT/BCIP was used as a substrate. The dark blue- purple hybridizing signal was located in cell nucleus. The tumor was considered positive for EBV encoded RNAs if more than 20 % of the tumor cells showing reactivity.
Fluorescence In situ Hybridization for IGH/MYC and non-IGH/MYC
Locus-specific interphase (LSI) fluorescence in situ hybridization (FISH) was performed on paraffin-embedded tissue sections. LSI MYC tri-color probe for the t(8;14) (Vysis, Gene Ltd, China) were used to detect IGH/MYC; LSI MYC dual color break apart rearrangement probe was used to detect split of MYC on chromosome 8 (Vysis, Gene Ltd, China). Lymphomas with MYC breakpoint without fusion of MYC to IGH locus were considered “other MYC translocations”. Specifically, deparaffinized sections were pretreated by pepsin digestion (30 min) in distilled water and subsequently incubated in pepsin solution (100ug/ml, 10–30 min) at 370 C to increase DNA accessibility. Sections were then fixed in 10 % neutral formalin for 5 min, dehydrated through increasing ethanol series and air-dried. 5ul of probe mix was applied to the tissue section and covered with a 10-mm cover slip. Both probe and target DNA were simultaneously denatured at 800 C for 10 min and incubated for up to 42 ~ 48 hours. Hybridization signals were analyzed under the fluorescent microscope (BX51, OLYMPUS) with appropriate filters. The images were captured using Applied imaging system. A total of 200 nuclei were scored, and any abnormal pattern which was present in excess of the cutoff limits (>10 % of cells) was considered significant. RAJI cell line was used as a positive control.
DNA extraction and polymerase chain reaction (PCR) for the t(14;18)
Genomic DNA from paraffin-embedded tissue samples was extracted by phenol-chloroform procedures. Successful DNA extraction was confirmed by amplification of 110 bp fragment of β-globin. The primers of BIOMED-2 system were used for the t(14;18)(BCL2/IGH) analysis. The experiment was according to the procedure of van Dongen et al. . The PCR products were electrophoresed in 10 % nondenaturing polyacrylamide gel (acrylamide:biacrylamide ratio of 29:1), and silver staining was applied in visualization of the results.
Follow up and statistical analysis
Clinical follow-up data were available for all of the forty-three patients. Lymphoma-specific survival time was calculated by determining the time from the date of diagnosis to the date of death or last follow-up, and was analyzed using the Kaplan-Meier method. For comparison of the various parameters, Fisher exact test was applied. A p value of 0.05 was considered statistically significant. All statistical analysis was performed using SPSS software for Windows, version 13.0.
Clinical features (n = 43)
Jaws and facial bones
superficial lymph node
peripheral blood & bone marrow
Lab findings (n = 34)
Increased WBC count
Increased PLT number
Increased serum level of LDH
Staging (n = 43, Jude and Murphy)
I / II
III / IV
IPI (n = 34)
Therapy (n = 30)
Surgery and chemotherapy
Follow up (n = 43, months)
62.8 (average 4.9 m)
37.2 (average 48.7 m)
Morphologic features (n = 43)
“Starry sky” pattern
Squared off feature
Greater nuclear pleomorphism
Tumor giant cells
Blood cell Lake
For the seven cases with lymph node involvement, the architecture of the node was completely effaced by diffuse infiltration of neoplastic lymphoid cells. The other morphologic features were similar as those described above.
Immunophenotype and EBV status
Results of IHC, EBER-ISH, PCR and FISH
IHC (n = 43)
EBER-ISH (n = 43)
BCL-2/IGH by PCR (n = 39)
FISH (n = 40)
Other MYC translocation
MYC gene translocation and BCL-2/IGH gene rearrangement analysis
The FISH study was successfully performed in 40 cases, the results are also summarized in Table 3. Of all 38 cases showing signal split with C-MYC break-apart FISH probes, 31 (77.5 %) were positive for IGH/MYC fusion FISH signals, indicating the t(8;14)(q24;q32) translocation; 7 (17.5 %) were negative for IGH/MYC, suggesting IGL/MYC fusion or other rare translocation with MYC(Figures 4b and 4c); in two cases the tumors were negative for both probes. The t(14;18) (BCL-2/IGH) t(14;18) analysis by DNA amplification using PCR method was performed in 39 cases and no BCL-2/IGH translocation was identified.
Treatment, Follow-up and Survival Analysis
Clinical treatment information were collected for all of the 43 patients. Nineteen patients (23.3 %) received surgical resection, nine with combined chemotherapy subsequently. Eleven patients (25.6 %) received chemotherapy alone, whereas, unfortunately, the remaining 13 patients (30.4 %) received no further treatment after the diagnosis was established by biopsy. Among 20 patients who received chemotherapy, ten patients received CHOP-like regimen as initial therapy, while the remaining ten patients received intensive regimen including HYPER-CVAD or LMB. Among 20 patients who received chemotherapy with or without surgical resection, complete remissions (CR) and partial remissions (PR) were achieved in 11 and 4 patients respectively, whereas the remaining 5 patients failed to show any response to chemotherapy.
Herein, we reported clinicopathological features of 43 cases of pediatric BL from Southwest China. Pediatric BL accounts for 7.1 % of all childhood lymphomas at our hospital. It showed classical pathological features of BL with typical morphology, immunohistochemical findings, cytogenetic changes, and clinical features. However, our study showed that a relatively lower incidence of BL in a representative pediatric population in Southwest China, marked male predominance, and particularly poorer survival, partially due to insufficient therapy.
BL accounts for about 30 ~ 50 % of childhood lymphomas in the Western countries . The reason for lower incidence in our cohort is currently unknown. Cairo et al.  reviewed 470 patients from USA, the male to female ratio was 4:1 in that cohort. Chuang et al.  studied 17 pediatric BL from Taiwan, the male to female ratio was 1.8:1; whereas in current study, all patients but four were boys, the ratio of male to female was 9.75:1. The gender ratio of newborns in this part of China was about 1.2:1, and there was no gender bias in patient selection. Our findings may suggest BL were more prone to affect boy in this area. Further larger scale of study is required to confirm this finding.
Majority of sporadic BL present with abdominal masses, whereas jaw is rarely affected; majority of BL patients (70 %) present at advanced stages .Whereas in our study, close to one-thirds of patients presented with head and neck lesions, together with the patients with superficial lymph node involvement, resulting in a higher percentage of cases in stage I/II in our cohort.
BL is a neoplasm of mature B-cell lineage, which was thought to arise from germinal center B-cells . Therefore, the tumor cells often express germinal center associated markers, such as CD10 and Bcl-6. Ki-67 index are always nearly 100 % . In current study, expression of CD10 and BCL-6 were 100 % and 93 %, respectively, and Ki-67 index was all beyond 90 %. No BCL-2 expression or BCL-2/IGH gene rearrangement was detected in all examined cases. The results are similar to that reported in the literatures. The MYC translocation is a hallmark of Burkitt lymphoma. The most common type of MYC translocation is the t(8;14)(q24;q32), accounting for 80 % of BL; In the remaining 20 %, one of two variants is identified: t(2;8)(p12;q24) or t(8;22)(q24;q11) . In this study, MYC translocation was found in 95 % of the cases, including 77.5 % of IGH/MYC and 17.5 % of other translocations. Although MYC translocation detection by FISH was thought to be the “gold criterion”, 9 % ~ 14 % of the cases may lack a detectable MYC translocation by FISH, the explanation for which is uncertain [10–12].
The frequency of EBV infection in sporadic BL varied largely according to geographical distributions, e.g. 0 % to 8 % in Japan; 25 % of reported Taiwanese cases; 34 % of Israel; 47 % of Argentina; 52.6 % of Brazil; 80 % of India [13–16]. Some researchers suggested that general conditions of health and social economic status may play a role. In our study, 11.6 % of the cases were positive for EBER1/2 by in situ hybridization, and it is lower than that of average level (20 % ~ 40 %) of EBV infection reported . Although EBV could be detected in almost all the endemic BL, to date, its significance in pathogenesis of the sporadic BL is still controversy. In addition, Bellan  studied the cell origin of BL by semi-nested PCR to amplify the VDJ rearrangement of IG heavy chain (V H ) genes and sequencing analysis, the results suggested that EBV-positive and EBV-negative BL may originate from two distinct subsets of B-cells, pointing to a particular role for the germinal center reaction in the pathogenesis of the tumor. Thorley’s research showed the similar results as well .
Although BL was less common in adults and the present study mainly focused on children and adolescents, pediatric and adult sporadic BLs shared similar phenotypic and genotypic features . A study based on gene expression profiling by Klapper et al.  showed the same results, that no differences were detectable between pediatric and adult molecular BL with regard to gene expression and chromosomal imbalances.
The following morphologic features, such as sheets of monomorphic and medium-sized neoplastic cells, “starry sky” growth pattern, numerous mitotic figures as well as apoptotic bodies favor the diagnosis of BL. Molecular profiling studies also showed that the histomorphological diagnosis of classical Burkitt lymphoma is quite robust [11, 21]. Furthermore, in combination with immunohistochemistry, MYC translocation by FISH, diagnosis of BL is usually easy to make in most instances. However, the neoplastic cells of BL may also display a variety degree of pleomorphism in nuclear size and shape, which was described as Burkitt like lymphoma (BLL) and categorized as a variant of BL in WHO Classifications of 2001 . The major problem is to distinguish BL with greater pleomorphism from DLBCL. Gene-expression profiling has confirmed that BL is a homogenous molecular phenotype clearly distinct from other B-NHL including DLBCL [8, 11, 21, 22]. Nevertheless, it is currently impractical for us to use gene-expression profiling analysis in routine diagnosis. Some tumors with histomorphological and immunohistochemical features intermediate between BL and DLBCL, so called “gray zone lymphoma” are present and further studies are wanted for understanding the pathogenesis of this group of tumors as well as their effective therapy.
Review and comparison of the major clinical manifestations, treatment and outcome of BL
H & N (%)
Os or EFS (years)
Reiter A (1995) 
EFS 79 %(1y)
EFS 79 %(2y)
Ertem U (1996) 
Ziegler’s and intensive protocol*
Os 60.0 %(1y)
Os 57.8 %(2y)
Cario MS (2003) 
Os 70.0 (1y)
EFS 60.0 %(1y)
Os 64.5 % (2y)
EFS 58.5 %(2y)
Boerma EG (2004) 
Hassan R (2008) 
Chuang SS (2008) 
Os 80 %(1y)
Modified BFM regimen
Os 66.7 % (2y)
Mbulaiteye SM (2009) 
The current study
Os 39.5 %(1y)
LMB/ HD-MTX + Ara-c
Os 39.5 %(2y)
In conclusion, we described 43 cases of childhood BL. Compared with that reported in the literature, some differences were presented in our cohort, including the higher ratio of male patients and higher percentage of patients presented with lower stages, clinically insufficient treatment and management as well as a very poor outcome of the tumor. Because BL was not common in mainland China, It is necessary for us to ameliorate the management and treatment of the tumor to improve the prognosis in the near future.
This work was sponsored in part by grants from the National Natural Science Foundation of China (N0. 30971113; 30470747), the Ph.D. Programs Foundation of Ministry of Education of China (N0. 20070610141) and Specific Foundation of Ministry of Health for Scientific Research (N0. 200802011).
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