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A case of GI Burkitt-like lymphoma
A case of GI Burkitt-like lymphoma Sayoko Shimazu, MD, Michiya Kobayashi, MD, Takehiro Okabayashi, MD, Takeki Sugimoto, MD, Tsutomu Namikawa, MD, Ken Okamoto, MD, Keijiro Araki, MD
The category of Burkitt-like lymphoma (BLL) was proposed by the International Lymphoma Study Group in the Revised European-American Lymphoma Classification (1994) to signify one of the highly aggressive non-Hodgkin’s lymphomas.1,2 It is extremely rare for BLL to occur in the alimentary tract.3,4 Patients with this lymphoma have an especially poor prognosis.2,4-7 No effective therapy for alimentary BLL has been established. CASE REPORT A 76-year-old man with general fatigue of 2 months’ duration was referred for evaluation and treatment. Examination revealed no palpable mass in the abdomen, ascites, or superficial lymphadenopathy; the conjunctiva were pale. Laboratory test results included the following: total protein, 5.8 g/dL (normal: 6.5-8.0 g/dL); total cholesterol, 103 mg/dL (130-230 mg/dL); cholinesterase, 76 IU/L (200-440 IU/L); albumin, 2.3 g/dL (3.8-5.1 g/dL); hematocrit, 25.0% (40.5%-51.5%); and Hb, 7.4 g/dL (13.918.1 g/dL). Other laboratory tests, including a blood smear, tumor markers (carcinoembryonic antigen, carbohydrate 19-9, and carbohydrate 15-3), and serologic tests for viral infection, including Ebstein-Barr virus (EBV), were within normal ranges. Barium contrast radiography of the stomach demonstrated a lesion on the greater curvature/posterior wall of the antrum that had the appearance of a type 2 cancer (Fig. 1). At upper endoscopy, a deep ulcer was noted in the posterior wall of the antrum (Fig. 2A and B). Biopsy specimens revealed an infiltrate of atypical lymphocytes in the mucosa. A diagnosis of malignant lymphoma was made, and the patient underwent surgery 2 weeks later. At the operation, analysis of a frozen section from the main tumor revealed lymphoma, and distal gastrectomy and D1 lymph node dissection were carried out. Nine tumors were also discovered in the small intestine intra-operatively; 5 that invaded the serosa were resected (Fig. 3). Evaluation of the resection specimen revealed a 5 3 4cm tumor in the stomach that had infiltrated into the subserosal layer. The tumors in the small intestine varied from 1 cm to 8 cm in size. Histopathologic assessment revealed a monotonous pattern of undifferentiated lymCurrent affiliations: Department of Surgery, Kochi Medical School, Nankoku-City, Kochi, Japan. Reprint requests: Dr. Michiya Kobayashi, Department of Surgery, Kochi Medical School, Kohasu-Okocho, Nankoku-City, Kochi 783-8505, Japan. Copyright Ó 2004 by the American Society for Gastrointestinal Endoscopy 0016-5107/$30.00 PII: S0016-5107(04)01530-5 152
GASTROINTESTINAL ENDOSCOPY
Figure 1. Barium contrast radiography showing a lesion on greater curvature/posterior wall of gastric antrum. phoid cells of unequal shape and size, with regular round nuclei and scant cytoplasm, the typical ‘‘starry sky appearance’’ of Burkitt-like lymphoma. The B-cell marker L-26 was positive, and UCHL-1 (T-cell marker) and CD10 were negative. Therefore, this case fulfilled the diagnostic criteria for primary BLL in the GI tract. The patient underwent multiple courses of chemotherapy (3 different protocols) but died 13 months later.
DISCUSSION Burkitt-like lymphoma is a non-Hodgkin’s lymphoma. The mortality rate for patients with BLL is high.1,2 Burkitt lymphoma (BL) occurs during childhood as an extra nodal lymphoma, whereas BLL occurs in adults as a nodal lymphoma.8-11 With respect to non-Hodgkin’s lymphoma, BL accounts for 1.1% of cases and BLL accounts for 0.5%.12 Burkitt-like lymphoma and BL have similar histopathologic features: granular nuclear chromatin, and a marked and well-defined rim of basophilic cytoplasm, within which small lipid droplets may be visible.3,13,14 One histopathologic feature of both BLL and BL is the so-called starry sky appearance, which can be appreciated on low-power microscopy. In highpower views, the size and the shape of the cells are much more variable in BLL compared with BL.3,13 GI lymphomas are commonly extranodal and almost always of the non-Hodgkin’s type.3,15 It is extremely rare for BLL and BL to occur in the alimentary tract. In most reports, patients with BLL presented with abdominal pain and obstructive VOLUME 60, NO. 1, 2004
A case of GI Burkitt-like lymphoma
S Shimazu, M Kobayashi, T Okabayashi, et al.
Figure 3. Photomicrograph showing ‘‘starry sky’’ appearance of BLL lymphoma. The size and shape of the lymphoma cells are variable (H&E, orig. mag. 3200). Figure 2. A, Endoscopic view of ulcerated lesion in gastric antrum. B, Endoscopic view of deep ulcer.
features caused by ileocecal involvement.14,16,17 However, our patient did not have abdominal pain, and there were no obstructive symptoms. Although the BLL initially was discovered in the stomach of our patient, multiple lesions also were found in the small intestine at surgery. It is likely that this represents simultaneous occurrence of multiple primary lesions instead of metastasis of a primary lymphoma to the intestine, because the sizes of the tumors were similar. As with the characteristics of immunohistochemistry, the restructuring of the immunoglobulin (Ig) gene is seen in BLL.17-20 In the extensive antibody panel, there are different characteristics in serum IgM and B-cell associated antigen between BL and BLL.5,21,22 Ebstein-Barr virus is involved in the pathogenesis for almost all BL, but this is extremely rare in BLL.5 From the viewpoint of chromosome aberrations, the translocation of c-myc is not seen in BL, and the translocation of bcl-2 is seen in 30% of cases of BLL.5,20,23,24 Therefore, the pathogenesis of VOLUME 60, NO. 1, 2004
BLL and BL apparently are not the same. In the present case, where the starry sky appearance was seen, the size and the shape of lymphoma cells was unequal. Because L-26 (B-cell marker) was positive, and UCHL-1 (T-cell marker) and CD10 were negative, the diagnostic criteria for primary BLL of the alimentary tract were met. It is reported that surgical excision followed by chemotherapy is effective treatment for patients with BLL.5,19,25,26 In our patient, surgery was performed for tumor reduction with the expectation that subsequent chemotherapy would be effective. However, patients with BLL and BL, highly aggressive forms of non-Hodgkin’s lymphoma, have an extremely poor prognosis. Median survival is 6 months, and 90% of patients with GI BLL die within 1 year of diagnosis.5,6,27,28 It has been suggested that patients with BLL have a worse prognosis than those with BL.28,29 Despite aggressive chemotherapy after surgery, our patient died 13 months later. All lesions that could be palpated were resected, nevertheless, the prognosis was considered poor because the disease was widespread when it was discovered. GASTROINTESTINAL ENDOSCOPY
153
S Shimazu, M Kobayashi, T Okabayashi, et al.
REFERENCES 1. Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML, et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994;84:1361-92. 2. Braziel RM, Arber DA, Slovak ML, Gulley ML, Spier C, Kjeldsberg C, et al. The Burkitt-like lymphomas: a Southwest Oncology Group study delineating phenotypic, genotypic, and clinical features. Blood 2001;97:3713-20. 3. Isaacson PG. Gastrointestinal lymphoma. Hum Pathol 1994; 25:1020-9. 4. Evens AM, Gordon LI. Burkitt’s and Burkitt-like lymphoma. Curr Treat Options Oncol 2002;3:291-305. 5. Macpherson N, Lesack D, Klasa R, Horsman D, Connors JM, Barnett M, et al. Small noncleaved, non-Burkitt’s (Burkittlike) lymphoma: cytogenetics predict outcome and reflect clinical presentation. J Clin Oncol 1999;17:1558-67. 6. Yamagata H, Tominaga M, Yoshida Y, Aoyagi I, Kyojoin K, et al. Burkitt-like lymphoma of the stomach, report of a case. Stomach and Intestine 1996;31:1509-14. 7. Miyaguchi S, Hibi T, Kanai T, Tashiro H, Suematsu M, Guevara FM, et al. A case of Burkitt’s lymphoma of the stomach with unusual features. Endoscopy 1992;24:603. 8. Burkitt D. A sarcoma involving the jaws in African children. Br J Surg 1958;46:218-23. 9. Grogen TM, Warnke RA, Kaplan HS. A comparative study of Burkitt’s and non Burkitt’s ‘‘undifferentiated’’ malignant lymphoma. Cancer 1982;49:1817-28. 10. Hui PK, Feller AC, Lennert K. High-grade non-Hodgkin’s lymphoma of B-cell type. I. Histopathology. Histopathology 1988;12:127-43. 11. Henry K. Burkitt’s lymphoma. In: Symmers WSC, editor. Systemic pathology, 3rd ed. Edinburgh: Churchill Livingston; 1992. p. 719-30. 12. Lymphoma Study Group of Japanese Pathologists. The World Health Organization classification of malignant lymphomas in Japan: incidence of recently recognized entities. Pathol Int 2000;50:696-702. 13. The Non-Hodgkin’s Lymphoma Pathologic Classification Project. National Cancer Institute sponsored study of nonHodgkin’s lymphomas: summary and description of a working formulation for clonical usage. Cancer 1982;49:2112-35. 14. Zhang X, Beneck D, Bostwick HE, Weisberger J. Primary Burkitt-like lymphoma presenting as a solitary rectal polyp in a child: case report. Pediatr Dev Pathol 2003;6:182-6. 15. Johnson KA, Tung K, Mead G, Sweetenham J. The imaging of Burkitt’s and Burkitt-like lymphoma. Clin Radiol 1998; 53:835-41. 16. Klumb CE, Resende LM, Stefanoff CG, Vicuna CH, Renault IZ, Maia RC. Burkitt-like lymphoma in an infant: a case report. Rev Hosp Clin Fac Med Sao Paulo 2003;58: 33-6.
154
GASTROINTESTINAL ENDOSCOPY
A case of GI Burkitt-like lymphoma
17. Magrath IT, Shiramizu B. Biology and treatment of small non-cleaved cell lymphoma. Oncology 1989;3:41. 18. Yano T, van Krieken JH, Magrath IT, Longo DL, Jaffe ES, Raffeld M. Histogenetic correlations between subcategories of small noncleaved cell lymphomas. Blood 1992;79: 1282-90. 19. Cairo MS, Sposto R, Perkins SL, Meadows AT, Hoover-Regan ML, Anderson JR, et al. Burkitt’s and Burkitt-like lymphoma in children and adolescents: a review of the Children’s Cancer Group experience. Br J Haematol 2003;120:660-70. 20. Hutchison RE, Finch C, Kepner J, Fuller C, Bowman P, Link M, et al. Burkitt lymphoma is immunophenotypically different from Burkitt-like lymphoma in young persons. Ann Oncol 2000;1:35-8. 21. Garcia CF, Weiss LM, Warnke RA. Small noncleaved cell lymphoma: an immunophenotypic study of 18 cases and comparison with large cell lymphoma. Hum Pathol 1986;17: 454-61. 22. Pavlova Z, Parker JW, Taylor CR, Levine AM, Feinstein DI, Lukes RJ. Small noncleaved follicular center cell lymphoma: Burkitt’s and non-Burkitt’s variants in the US. II. Pathologic and immunologic features. Cancer 1987;59: 1892-902. 23. Spina D, Leoncini L, Megha T, Gallorini M, Disanto A, Tosi P, et al. Cellular kinetic and phenotypic heterogeneity in and among Burkitt’s and Burkitt-like lymphomas. J Pathol 1997; 182:145-50. 24. Brennscheidt U, Eick D, Kunzmann R, Martens U, Kiehntopf M, Mertelsmann R, et al. Burkitt-like mutations in the c-myc gene locus in prolymphocytic leukemia. Leukemia 1994;8: 897-902. 25. Ziegler JL. Chemotherapy of Burkitt’s lymphoma. Cancer 1972;30:1534-40. 26. Magrath IT, Lwanga S, Carswell W, Harrison N. Surgical reduction of tumour bulk in management of abdominal Burkitt’s lymphoma. BMJ 1974;2:308-12. 27. Sweetenham JW, Pearce R, Taghipour G, Blaise D, Gisselbrecht C, Goldstone AH. Adult Burkitt’s and Burkitt-like non-Hodgkin’s lymphoma: outcome for patients treated with high-dose therapy and autologous stem-cell transplantation in first remission or at relapse—results from the European Group for Blood and Marrow Transplantation. J Clin Oncol 1996;14:2465-72. 28. The Non-Hodgkin’s Lymphoma Classification Project: a clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin’s lymphoma. Blood 1997;89: 3909-18. 29. Levine AM, Pavlova Z, Pockros AW, Parker JW, Teitelbaum AH, Paganini-Hill A, et al. Small noncleaved follicular center cell (FCC) lymphoma: Burkitt and non-Burkitt variants in the United States. I. Clinical features. Cancer 1983;52: 1073-9.
VOLUME 60, NO. 1, 2004
The category of Burkitt-like lymphoma (BLL) was proposed by the International Lymphoma Study Group in the Revised European-American Lymphoma Classification (1994) to signify one of the highly aggressive non-Hodgkin’s lymphomas.1,2 It is extremely rare for BLL to occur in the alimentary tract.3,4 Patients with this lymphoma have an especially poor prognosis.2,4-7 No effective therapy for alimentary BLL has been established. CASE REPORT A 76-year-old man with general fatigue of 2 months’ duration was referred for evaluation and treatment. Examination revealed no palpable mass in the abdomen, ascites, or superficial lymphadenopathy; the conjunctiva were pale. Laboratory test results included the following: total protein, 5.8 g/dL (normal: 6.5-8.0 g/dL); total cholesterol, 103 mg/dL (130-230 mg/dL); cholinesterase, 76 IU/L (200-440 IU/L); albumin, 2.3 g/dL (3.8-5.1 g/dL); hematocrit, 25.0% (40.5%-51.5%); and Hb, 7.4 g/dL (13.918.1 g/dL). Other laboratory tests, including a blood smear, tumor markers (carcinoembryonic antigen, carbohydrate 19-9, and carbohydrate 15-3), and serologic tests for viral infection, including Ebstein-Barr virus (EBV), were within normal ranges. Barium contrast radiography of the stomach demonstrated a lesion on the greater curvature/posterior wall of the antrum that had the appearance of a type 2 cancer (Fig. 1). At upper endoscopy, a deep ulcer was noted in the posterior wall of the antrum (Fig. 2A and B). Biopsy specimens revealed an infiltrate of atypical lymphocytes in the mucosa. A diagnosis of malignant lymphoma was made, and the patient underwent surgery 2 weeks later. At the operation, analysis of a frozen section from the main tumor revealed lymphoma, and distal gastrectomy and D1 lymph node dissection were carried out. Nine tumors were also discovered in the small intestine intra-operatively; 5 that invaded the serosa were resected (Fig. 3). Evaluation of the resection specimen revealed a 5 3 4cm tumor in the stomach that had infiltrated into the subserosal layer. The tumors in the small intestine varied from 1 cm to 8 cm in size. Histopathologic assessment revealed a monotonous pattern of undifferentiated lymCurrent affiliations: Department of Surgery, Kochi Medical School, Nankoku-City, Kochi, Japan. Reprint requests: Dr. Michiya Kobayashi, Department of Surgery, Kochi Medical School, Kohasu-Okocho, Nankoku-City, Kochi 783-8505, Japan. Copyright Ó 2004 by the American Society for Gastrointestinal Endoscopy 0016-5107/$30.00 PII: S0016-5107(04)01530-5 152
GASTROINTESTINAL ENDOSCOPY
Figure 1. Barium contrast radiography showing a lesion on greater curvature/posterior wall of gastric antrum. phoid cells of unequal shape and size, with regular round nuclei and scant cytoplasm, the typical ‘‘starry sky appearance’’ of Burkitt-like lymphoma. The B-cell marker L-26 was positive, and UCHL-1 (T-cell marker) and CD10 were negative. Therefore, this case fulfilled the diagnostic criteria for primary BLL in the GI tract. The patient underwent multiple courses of chemotherapy (3 different protocols) but died 13 months later.
DISCUSSION Burkitt-like lymphoma is a non-Hodgkin’s lymphoma. The mortality rate for patients with BLL is high.1,2 Burkitt lymphoma (BL) occurs during childhood as an extra nodal lymphoma, whereas BLL occurs in adults as a nodal lymphoma.8-11 With respect to non-Hodgkin’s lymphoma, BL accounts for 1.1% of cases and BLL accounts for 0.5%.12 Burkitt-like lymphoma and BL have similar histopathologic features: granular nuclear chromatin, and a marked and well-defined rim of basophilic cytoplasm, within which small lipid droplets may be visible.3,13,14 One histopathologic feature of both BLL and BL is the so-called starry sky appearance, which can be appreciated on low-power microscopy. In highpower views, the size and the shape of the cells are much more variable in BLL compared with BL.3,13 GI lymphomas are commonly extranodal and almost always of the non-Hodgkin’s type.3,15 It is extremely rare for BLL and BL to occur in the alimentary tract. In most reports, patients with BLL presented with abdominal pain and obstructive VOLUME 60, NO. 1, 2004
A case of GI Burkitt-like lymphoma
S Shimazu, M Kobayashi, T Okabayashi, et al.
Figure 3. Photomicrograph showing ‘‘starry sky’’ appearance of BLL lymphoma. The size and shape of the lymphoma cells are variable (H&E, orig. mag. 3200). Figure 2. A, Endoscopic view of ulcerated lesion in gastric antrum. B, Endoscopic view of deep ulcer.
features caused by ileocecal involvement.14,16,17 However, our patient did not have abdominal pain, and there were no obstructive symptoms. Although the BLL initially was discovered in the stomach of our patient, multiple lesions also were found in the small intestine at surgery. It is likely that this represents simultaneous occurrence of multiple primary lesions instead of metastasis of a primary lymphoma to the intestine, because the sizes of the tumors were similar. As with the characteristics of immunohistochemistry, the restructuring of the immunoglobulin (Ig) gene is seen in BLL.17-20 In the extensive antibody panel, there are different characteristics in serum IgM and B-cell associated antigen between BL and BLL.5,21,22 Ebstein-Barr virus is involved in the pathogenesis for almost all BL, but this is extremely rare in BLL.5 From the viewpoint of chromosome aberrations, the translocation of c-myc is not seen in BL, and the translocation of bcl-2 is seen in 30% of cases of BLL.5,20,23,24 Therefore, the pathogenesis of VOLUME 60, NO. 1, 2004
BLL and BL apparently are not the same. In the present case, where the starry sky appearance was seen, the size and the shape of lymphoma cells was unequal. Because L-26 (B-cell marker) was positive, and UCHL-1 (T-cell marker) and CD10 were negative, the diagnostic criteria for primary BLL of the alimentary tract were met. It is reported that surgical excision followed by chemotherapy is effective treatment for patients with BLL.5,19,25,26 In our patient, surgery was performed for tumor reduction with the expectation that subsequent chemotherapy would be effective. However, patients with BLL and BL, highly aggressive forms of non-Hodgkin’s lymphoma, have an extremely poor prognosis. Median survival is 6 months, and 90% of patients with GI BLL die within 1 year of diagnosis.5,6,27,28 It has been suggested that patients with BLL have a worse prognosis than those with BL.28,29 Despite aggressive chemotherapy after surgery, our patient died 13 months later. All lesions that could be palpated were resected, nevertheless, the prognosis was considered poor because the disease was widespread when it was discovered. GASTROINTESTINAL ENDOSCOPY
153
S Shimazu, M Kobayashi, T Okabayashi, et al.
REFERENCES 1. Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML, et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994;84:1361-92. 2. Braziel RM, Arber DA, Slovak ML, Gulley ML, Spier C, Kjeldsberg C, et al. The Burkitt-like lymphomas: a Southwest Oncology Group study delineating phenotypic, genotypic, and clinical features. Blood 2001;97:3713-20. 3. Isaacson PG. Gastrointestinal lymphoma. Hum Pathol 1994; 25:1020-9. 4. Evens AM, Gordon LI. Burkitt’s and Burkitt-like lymphoma. Curr Treat Options Oncol 2002;3:291-305. 5. Macpherson N, Lesack D, Klasa R, Horsman D, Connors JM, Barnett M, et al. Small noncleaved, non-Burkitt’s (Burkittlike) lymphoma: cytogenetics predict outcome and reflect clinical presentation. J Clin Oncol 1999;17:1558-67. 6. Yamagata H, Tominaga M, Yoshida Y, Aoyagi I, Kyojoin K, et al. Burkitt-like lymphoma of the stomach, report of a case. Stomach and Intestine 1996;31:1509-14. 7. Miyaguchi S, Hibi T, Kanai T, Tashiro H, Suematsu M, Guevara FM, et al. A case of Burkitt’s lymphoma of the stomach with unusual features. Endoscopy 1992;24:603. 8. Burkitt D. A sarcoma involving the jaws in African children. Br J Surg 1958;46:218-23. 9. Grogen TM, Warnke RA, Kaplan HS. A comparative study of Burkitt’s and non Burkitt’s ‘‘undifferentiated’’ malignant lymphoma. Cancer 1982;49:1817-28. 10. Hui PK, Feller AC, Lennert K. High-grade non-Hodgkin’s lymphoma of B-cell type. I. Histopathology. Histopathology 1988;12:127-43. 11. Henry K. Burkitt’s lymphoma. In: Symmers WSC, editor. Systemic pathology, 3rd ed. Edinburgh: Churchill Livingston; 1992. p. 719-30. 12. Lymphoma Study Group of Japanese Pathologists. The World Health Organization classification of malignant lymphomas in Japan: incidence of recently recognized entities. Pathol Int 2000;50:696-702. 13. The Non-Hodgkin’s Lymphoma Pathologic Classification Project. National Cancer Institute sponsored study of nonHodgkin’s lymphomas: summary and description of a working formulation for clonical usage. Cancer 1982;49:2112-35. 14. Zhang X, Beneck D, Bostwick HE, Weisberger J. Primary Burkitt-like lymphoma presenting as a solitary rectal polyp in a child: case report. Pediatr Dev Pathol 2003;6:182-6. 15. Johnson KA, Tung K, Mead G, Sweetenham J. The imaging of Burkitt’s and Burkitt-like lymphoma. Clin Radiol 1998; 53:835-41. 16. Klumb CE, Resende LM, Stefanoff CG, Vicuna CH, Renault IZ, Maia RC. Burkitt-like lymphoma in an infant: a case report. Rev Hosp Clin Fac Med Sao Paulo 2003;58: 33-6.
154
GASTROINTESTINAL ENDOSCOPY
A case of GI Burkitt-like lymphoma
17. Magrath IT, Shiramizu B. Biology and treatment of small non-cleaved cell lymphoma. Oncology 1989;3:41. 18. Yano T, van Krieken JH, Magrath IT, Longo DL, Jaffe ES, Raffeld M. Histogenetic correlations between subcategories of small noncleaved cell lymphomas. Blood 1992;79: 1282-90. 19. Cairo MS, Sposto R, Perkins SL, Meadows AT, Hoover-Regan ML, Anderson JR, et al. Burkitt’s and Burkitt-like lymphoma in children and adolescents: a review of the Children’s Cancer Group experience. Br J Haematol 2003;120:660-70. 20. Hutchison RE, Finch C, Kepner J, Fuller C, Bowman P, Link M, et al. Burkitt lymphoma is immunophenotypically different from Burkitt-like lymphoma in young persons. Ann Oncol 2000;1:35-8. 21. Garcia CF, Weiss LM, Warnke RA. Small noncleaved cell lymphoma: an immunophenotypic study of 18 cases and comparison with large cell lymphoma. Hum Pathol 1986;17: 454-61. 22. Pavlova Z, Parker JW, Taylor CR, Levine AM, Feinstein DI, Lukes RJ. Small noncleaved follicular center cell lymphoma: Burkitt’s and non-Burkitt’s variants in the US. II. Pathologic and immunologic features. Cancer 1987;59: 1892-902. 23. Spina D, Leoncini L, Megha T, Gallorini M, Disanto A, Tosi P, et al. Cellular kinetic and phenotypic heterogeneity in and among Burkitt’s and Burkitt-like lymphomas. J Pathol 1997; 182:145-50. 24. Brennscheidt U, Eick D, Kunzmann R, Martens U, Kiehntopf M, Mertelsmann R, et al. Burkitt-like mutations in the c-myc gene locus in prolymphocytic leukemia. Leukemia 1994;8: 897-902. 25. Ziegler JL. Chemotherapy of Burkitt’s lymphoma. Cancer 1972;30:1534-40. 26. Magrath IT, Lwanga S, Carswell W, Harrison N. Surgical reduction of tumour bulk in management of abdominal Burkitt’s lymphoma. BMJ 1974;2:308-12. 27. Sweetenham JW, Pearce R, Taghipour G, Blaise D, Gisselbrecht C, Goldstone AH. Adult Burkitt’s and Burkitt-like non-Hodgkin’s lymphoma: outcome for patients treated with high-dose therapy and autologous stem-cell transplantation in first remission or at relapse—results from the European Group for Blood and Marrow Transplantation. J Clin Oncol 1996;14:2465-72. 28. The Non-Hodgkin’s Lymphoma Classification Project: a clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin’s lymphoma. Blood 1997;89: 3909-18. 29. Levine AM, Pavlova Z, Pockros AW, Parker JW, Teitelbaum AH, Paganini-Hill A, et al. Small noncleaved follicular center cell (FCC) lymphoma: Burkitt and non-Burkitt variants in the United States. I. Clinical features. Cancer 1983;52: 1073-9.
VOLUME 60, NO. 1, 2004