Optimization of diagnosis and treatment of Burkitt’s lymphoma in children, adolescents, and young adults

T.T. Valiyev1, Ye.A. Baryakh2, P.A. Zeynalova3, A.M. Kovrigina2, S.K. Kravchenko2, T.N. Obukhova2, N.А. Falaleyeva3, A.I. Senderovich3, I.N. Serebryakova3, I.V. Kaminskaya1, A.S. Levashov1, and G.L. Mentkevich1

1 Pediatric Oncology and Hematology Research Institute, N.N. Blokhin Russian Cancer Center, Moscow, Russian Federation

2 Hematology Research Center, RF Ministry of Health, Moscow, Russian Federation

3 Clinical Oncology Research Institute, N.N. Blokhin Russian Cancer Research Center, Moscow, Russian Federation


ABSTRACT

We present the combined experience of the leading centers in diagnosis and treatment of Burkitt’s lymphoma (BL) in children, adolescents, and young adults, that is the first one in the national scientific literature. It includes immunolomorphologic and cytogenetic criteria of BL. The clinical features of BL in various age groups and treatment outcomes according to B-NHL-BFM 90/95 and CODOX-M/IVAC programs are described. Also, the treatment outcomes according to the original national LB-M-04 protocol are shown. The place of rituximab in BL treatment is discussed.


Keywords: Burkitt’s lymphoma, children, adolescents, young adults, clinical features, diagnosis, treatment.

Read in PDF(RUS)pdficon


REFERENCES

  1. Kasili E.G. Paediatric malignancy in tropical Africa — a growing concern. East. Afr. Med. J. 1986; 63: 685–6.
  2. Thomas D., Cortes J., O’Brien S. et al. Hyper-CVAD program in Burkitt’s type adult acute lymphoblastic leukemia. J. Clin. Oncol. 1999; 17(8): 2461–70.
  3. Ferry J.A. Burkitt’s Lymphoma: Clinicopathologic Features and Differential Diagnosis. Oncologist 2006; 11: 375–83.
  4. Swerdlow S.H., Campo E., Lee H.N. et al. WHO Classification of Tumours of Haematopoetic and Lymphoid tissues, 4th edn. Lyon: IARC Press, 2008: 439.
  5. Agugua N.E., Okeahialam T. Malignant diseases of childhood seen at the University of Nigeria Teaching Hospital, Enugu, Nigeria. East. Afr. Med. J. 1986; 63: 717–23.
  6. Oguonu T., Emodi E., Kaine W. Epidemiologie of Burkitt’s lymphoma in Enugu, Nigeria. Ann. Trop. Paediatr. 2002; 22: 369–74.
  7. Amusa Y.B., Adediran I.A., Akinpelu V.O. et al. Burkitt’s lymphoma of the head and neck region in a Nigeria tertiary hospital. East. Afr. J. Med. 2005; 24(3): 139–42.
  8. Kittivorapart J., Chinthammitr Y. Incidence and risk factors of bone marrow involvement by non-Hodgkin lymphoma. J. Med. Assoc. Thai. 2011; 94(Suppl. 1): S239–45.
  9. Барях Е.А., Кравченко С.К., Обухова Т.Н. и др. Лимфома Беркитта: клиника, диагностика, лечение. Клин. онкогематол. 2009; 2(2): 137–46. [Baryakh Ye.A., Kravchenko S.K., Obukhova T.N., et al. Burkitt’s lymphoma: clinical presentation, diagnosis, management. Klin. onkogematol. 2009; 2(2): 137–47. (In Russ.)].
  10. Blum K.A., Lozansky G., Byrd J. Adult Burkitt’s leukemia and lymphoma. Blood 2004; 20: 32–7.
  11. Braziel R.M., Arber D.A., Slovac M.L. et al. The Burkitt-like lymphoma: a Southwest Oncologie Group study delineating phenotypic, genotypic and clinical features. Blood 2001; 97(12): 3713–20.
  12. Martinez-Maza O., Breen E.C. B-cell activation and lymphoma in patients with HIV. Curr. Opin. Oncol. 2002; 14: 528–32.
  13. Magrath I.T. Malignant Non-Hodgkin’s Lymphomas in Children. Pediatr. Oncol. 2002; 119: 661–705.
  14. Zeigler J. Burkitt’s lymphoma. N. Engl. J. Med. 1981; 305: 735–45.
  15. Kelly G., Bell A., Rickinson A. Epstein-Barr virus-associated Burkitt lymphoma genesis selects for down-regulation of the nuclear antigen EBNA2. Nat. Med. 2002; 8(10): 1098–104.
  16. Гурцевич В.Э. Роль вируса Эпштейна—Барр в онкогематологиче- ских заболеваниях человека. Клин. онкогематол. 2010; 3(3): 222–35. [Gurtsevich V.E. Role of Epstein—Barr virus in human hematological malignancies. Klin. onkogematol. 2010; 3(3): 222–35. (In Russ.)].
  17. Magrath I. Epidemiology: clues to the pathogenesis of Burkitt lymphoma. Br. J. Haematol. 2012; 156(6): 744–56.
  18. Croce C. Role of chromosome translocations in human neoplasia. Cell 1987; 49(2): 155–6.
  19. Zech L., Haglund U., Nilsson K., Klein G. Characteristic chromosomal abnormalities in biopsies and lymphoid-cell lines from patients with Butkitt and non-Burkitt lymphomas. Int. J. Cancer 1976; 17: 47–56.
  20. Обухова Т.Н., Барях Е.А., Капланская И.Б. и др. Выявление диагности- ческих для лимфомы Беркитта транслокаций методом флюоресцентной in situ гибридизации на гистологических срезах парафиновых блоков. Тер. арх. 2007; 79(7): 80–3. [Obukhova T.N., Baryakh Ye.A., Kaplanskaya I.B., et al. Detection of translocations typical for Burkitt’s lymphoma using fluorescent hydrydization in situ in histological slices from paraffin blocks. Ter. arkh. 2007; 79(7): 80–3. (In Russ.)]
  21. Green T.M., Nielsen O., de Stricker K. et al. High levels of nuclear MYC protein predict the presence of MYC rearrangement in diffuse large B-cell lymphoma. Am. J. Surg. Pathol. 2012; 36(4): 612–9.
  22. Ben-Neriah S., Woods R., Steidl C. et al. Lymphomas with concurrent BCL2 and MYC translocations: the critical factors associated with survival. Blood 2009; 114: 2273–9.
  23. Tagawa H., Ikeda S., Sawada K. Role of microRNA in the pathogenesis of malignant lymphoma. Cancer Sci. 2013; 10; 121–6.
  24. Mead G.M., Sydes M.R., Walewski J. et al. An international evaluation of CODOX-M and CODOX-M alternating with IVAC in adult Burkitt’s lymphoma: results of United Kingdom Lymphoma Group LY06 study. Ann. Oncol. 2002; 13(8): 1264–74.
  25. Costa L.J., Xavier A.C., Wahlquist A.E. еt al. Trends in survival of patients with Burkitt lymphoma/leukemia in the USA: an analysis of 3691 cases. Blood 2013; 121(24): 4861–6.
  26. Fayad L., Thomas D., Romaguera J. Update of the M.D.Anderson Cancer Center experience with hyper-CVAD and rituximab for the treatment of mantle cell and Burkitt-type lymphomas. Clin. Lymph. Myel. 2007; 8(2): 57–62.
  27. Rizzieri D.A., Johnson J.L., Byrd J.C. et al. Efficacy and toxicity of rituximab and brief duration, high intensity chemotherapy with filgrastim support for Burkitt or Burkitt-like leukemia/lymphoma: Cancer and Leukemia Group B (CALGB) Study 10002 (abstract). Blood 2010; 116: Abstract 858.
  28. Dunleavy K., Pittaluga S., Wayne A.S. et al. MYC+ aggressive B-cell lymphomas: A novel therapy of untreated Burkitt lymphoma (BL) and MYC+ diffuse large B-cell lymphoma (DLBCL) with DA-EPOCH-R (abstract). Ann. Oncol. 2011; 22(4): Abstract 71.
  29. Griffin T.C., Weitzman S., Weinstein H. et al. A study of rituximab and ifosfamide, carboplatin, and etoposide chemotherapy in children with recurrent/ refractory B-cell (CD20+) non-Hodgkin lymphoma and mature B-cell acute lymphoblastic leukemia: A report from the Childrens Oncology Group. Pediatr. Blood Cancer 2009; 52: 177–81.
  30. Российские клинические рекомендации по диагностике и лечению лимфопролиферативных заболеваний. Под ред. И.В. Поддубной, В.Г. Савченко. М.: Медиа Медика, 2013: 102. [Rossiyskie klinicheskie rekomendatsii po diagnostike i lecheniyu limfoproliferativnykh zabolevaniy. Pod red. I.V. Poddubnoy, V.G. Savchenko (Russian clinical guidelines for diagnosis and treatment of lymphoproliferative disorders. Ed. by: I.V. Poddubnaya, V.G. Savchenko) M.: Media Medika, 2013: 102.]
  31. Барях Е.А., Валиев Т.Т., Яцков К.В. и др. Интенсивная терапия лимфомы Беркитта: описание двух клинических случаев. Гематол. и транс- фузиол. 2007; 52(1): 41–3. [Baryakh Ye.A., Valiyev T.T., Yatskov K.V., et al. Intensive therapy for Burkitt’s lymphoma: presentation of two clinical cases. Gematol. i transfuziol. 2007; 1: 41–3. (In Russ.)].
  32. Барях Е.А., Звонков Е.Е., Кременецкая А.М. Лечение беркиттопо- добной лимфомы взрослых. Тер. арх. 2006; 7: 53. [Baryakh Ye.A., Zvonkov Ye.Ye., Kremenetskaya A.M. Management of adult Burkitt-like lymphoma. Ter. arkh. 2006; 7: 53. (In Russ.)].
  33. Rosenfeld A., Arrington D., Miller J. et al. A review of childhood and adolescent craniopharyngiomas with particular attention to hypothalamic obesity. Pediatr. Neurol. 2014; 50(1): 4–10. doi: 10.1016/j.pediatrneurol.2013.09.003. Epub 2013 Nov 1.
  34. Senerchia A.A., Ribeiro K.B., Rodriguez-Galindo C. Trends in incidence of primary cutaneous malignancies in children, adolescents, and young adults: A population-based study. Pediatr. Blood Cancer 2014; 61(2): 211–6. doi: 10.1002/pbc.24639. Epub 2013 Oct 30.
  35. Тур А.Ф., Тарасов О.Ф., Шабалов Н.П. и др. Детские болезни, 2-е изд. М.: Медицина, 1985. [Tur A.F., Tarasov O.F., Shabalov N.P., et al. Detskiye bolezni, 2-e izd. (Pediatric disorders. 2nd ed.) M.: Meditsina, 1985]
  36. Bleyer A., Viny A., Barr R. Cancer in 15- to 29-year-olds by primary site. Oncologist 2006; 11(6): 590–601.
  37. Bleyer A. Young adult oncology: the patients and their survival challenges. СА Cancer J. Clin. 2007; 57(4): 242–55.
  38. Wood W.A., Lee S.J. Malignant hematologic diseases in adolescents and young adults. Blood 2011; 117: 5803–15.
  39. Sandlund J.T. Should adolescents with NHL be treated as old children or young adults? Hematol. Am. Soc. Hematol. Educ. Progr. 2007; 2007(1): 297–303.
  40. Cairo M.S., Sposto R., Gerrard M. et al. Advanced stage, increased, lactate dehydrogenase, and primary site, but not adolescent age (³ 15 years)are associated with an increased risk of treatment failure in children and adolescents with mature B-cell non-Hodgkins lymphoma: results of FAB LMB 96 Study. J. Clin. Oncol. 2012; 30(4): 387–93.
  41. Coiffier B. State-of-the-art therapeutics: diffuse large B-cell lymphoma. J. Clin. Oncol. 2005; 23(26): 6387–93.
  42. Pfreundschuh M., Trumper L., Osterborg A. et al. CHOP-like chemotherapy plus rituximab versus CHOP-like chemotherapy alone in young patients with good prognosis diffuse large B-cell lymphoma: a randomized controlled trial by the MabThera International Trial (MinT). Lancet Oncol. 2006; 7(5): 379–91.

Evolution of concepts for diagnosis and treatment of Burkitt’s lymphoma

T.T. Valiev1 and E.A. Baryakh2

1 Pediatric Oncology and Hematology Institute, N.N. Blokhin Russian Cancer Research Center, RAMS, Moscow, Russian Federation

2 Hematology Research Center, RF MH, Moscow, Russian Federation


ABSTRACT

The issues of diagnosis and treatment of the most aggressive lymphoid tumor, namely, Burkitt’s lymphoma (BL), are presented in the historical context. The clinical and laboratory features of endemic and sporadic BL variants are described. Possible mechanisms of Epstein-Barr virus and Plasmodium falciparum involvement in BL pathogenesis are suggested. Also, the morphologic, immunologic and cytogenetic BL diagnostic criteria are described. Based on molecular and genetic features, the issues of differential diagnosis with the heterogeneous group of diffuse large B-cell and highly aggressive mature B-cell lymphomas with additional proto-oncogene aberrations («double» and «triple» hit lymphomas) are presented. BL therapy and the role of rituximab in it is emphasized.


Keywords: Burkitt’s lymphoma, clinical presentation, diagnosis, treatment.

Read in PDF (RUS)pdficon


REFERENCES

  1. Burkitt D. A sarcoma involving the jaws in African children. Br. J. Surg. 1958; 46: 218–23.
  2. O’Conor G.T. Malignant lymphoma in African children. A pathology entity. Cancer 1961; 14: 270–83.
  3. Young L.S., Mussay P.G. Epstein-Barr virus and oncogenesis: form latent genes to tumours. Oncogene 2003; 22: 5108–21.
  4. Gulley M.L. Molecular diagnosis of Epstein-Barr virus-related diseases. J. Mol. Diagn. 2001; 3: 1–10.
  5. Epstein M.A., Achong B.R., Barr Y.M. Virus particles in cultured lymphoblasts from Burkitt’s lymphoma. Lancet 1964; 1: 702–3.
  6. Dorfman R.S. Childhood lymphosarcoma in St. Louis, Missouri, clinically and histologically resembling Burkitt tumor. Cancer 1965; 18: 418–30.
  7. Rappapоrt H., Braylan R. Changing concepts in the classification of malignant neoplasms of the hemopoetic system. Int. Acad. Pathol. 1975; 16: 1–19.
  8. The non-Hodgkin’s lymphoma pathologic classification project. National Cancer Institute sponsored study of classification of non-Hodgkin’s lymphomas: summary and description of a working formulation for clinical usage. Cancer 1982; 49: 2112–35.
  9. Lennert K., Feller A.C. Histopathology of Non-Hodgkin’s lymphomas (Based on the Updated Kiel Classification). Berlin: Springer Verlag, 1992: 312.
  10. Harris N.L., Jaffe E.S., Dejbold J. et al. The World Health Organization Classification of Neoplastic Diseases of the Hematopoietic and Lymphoid Tissues. Ann. Oncol. 1999; 10: 1419–32.
  11. Swerdlow S.H., Campo E., Harris N.L. et al. WHO Classification of Tumours of Haematopoetic and Lymphoid tissues, 4th edn. Lyon: IARC Press, 2008: 439.
  12. Agugua N.E., Okeahialam T. Malignant diseases of childhood seen at the University of Nigeria Teaching Hospital, Enugu, Nigeria. East. Afr. Med. J. 1986; 63: 717–23.
  13. De The G. Epidemiologie of Burkitt’s lymphoma: evidence for a casual association with EBV. Epidemiol. Rev. 1979; 36: 692–8.
  14. Oguonu T., Emodi E., Kaine W. Epidemiologie of Burkitt’s lymphoma in Enugu, Nigeria. Ann. Trop. Paediatr. 2002; 22: 369–74.
  15. Kasili E.G. Paediatric malignancy in tropical Africa — a growing concern. East. Afr. Med. J. 1986; 63: 685–6.
  16. Parkin D.M., Stiller C.A., Draper G.J. et al. The international incidence of childhood cancer. Int. J. Cancer. 1988; 42: 511–20.
  17. Magrath I.T. Malignant Non-Hodgkin’s Lymphomas in Children. Pediatr. Oncol. 2002; 119: 661–705.
  18. Zeigler J. Burkitt’s lymphoma. N. Engl. J. Med. 1981; 305: 735–45.
  19. Shannon-Lowe C., Adland E., Bell A.I. et al. Features distinguishing EpsteinBarr virus infections of epithelial cells and B cells: viral genome expression, genome maintenance and genome amplification. J. Virol. 2009; 83: 7749–60.
  20. Richinson A. Epstein-Barr virus. Virus Res. 2002; 82: 109–13.
  21. Thorley-Lawson D.A. Epstein-Barr virus: exploiting the immune system. Nat. Rev. Immunol. 2001; 1: 75–82.
  22. Kelly G., Bell A., Rickinson A. Epstein-Barr virus-associated Burkitt lymphoma genesis selects for down-regulation of the nuclear antigen EBNA2. Nat Med. 2002; 8(10): 1098–104.
  23. Гурцевич В.Э. Роль вируса Эпштейна—Барр в онкогематологиче- ских заболеваниях человека. Клин. онкогематол. 2010; 3(3): 222–35. [Gurtsevich V.E. Role of Epstein—Barr virus in human hematological malignancies. Klin. onkogematol. 2010; 3(3): 222–35. (In Russ.)].
  24. Bornkamm G.W. Epstein-Barr virus and the pathogenesis of Burkitt’s lymphoma: more questions than answers. Int. J. Cancer. 2009; 124(8): 1745–55.
  25. Raab-Traub N., Flynn K. The structure of the termini of the Epstein-Barr virus as a marker of clonal cellular proliferation. Cell 1986; 47: 883–9.
  26. Klein U., Klein G., Ehlin-Henriksson B. et al. Burkitt’s lymphoma is a malignancy of mature B-cells expressing somatically mutated V region genes. Mol. Med. 1995; 1: 495–506.
  27. Henderson S., Rowe M., Gregory C. et al. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 1991; 65(7): 1107–15.
  28. Preudhomme C., Dervite I., Wattel E. et al. Clinical significance of p53 mutations in newly diagnosed Burkitt’s lymphoma and acute lymphoblastic leukemia: a report of 48 cases. J. Clin. Oncol. 1995; 13: 812–20.
  29. Schoch C., Reider H., Stollman-Gibbels B. et al. 17p anomalies in lymphoid malignancies: Diagnostic and prognostic implications. Leuk. Lymphoma 1995; 17: 271–9.
  30. Mawanda O.W. Aspects of epidemiological and clinical features of patients with central nervous system Burkitt’s lymphoma in Kenya. East. Afr. Med. J. 2004; 8: 97–103.
  31. Mawanda O.W. Clinical characteristics of Burkitt’s lymphoma seen in Kenyan patients. East. Afr. Med. J. 2004; 8: 78–89.
  32. Donati D., Zhang L.P., Chene A. et al. Identification of a polyclonal B-cell activator in Plasmodium falciparum. Infect. Immun. 2004; 72: 5412–8.
  33. Chene A., Donati D., Guerreiro-Cacais A.O. et al. A molecular link between malaria and Epstein-Barr virus reactivation. PLoS Pathog. 2007; 3: 80.
  34. Magrath I. Epidemiology: clues to the pathogenesis of Burkitt lymphoma. Br. J. Haematol. 2012; 156(6): 744–56.
  35. Morrow R.H., Gutensohn N., Smith P.G. Epstein-Barr virus-malaria interaction models for Burkitt’s lymphoma: implications for preventive trials. Cancer Res. 1976; 36: 667–9.
  36. Amusa Y.B., Adediran I.A., Akinpelu V.O. et al. Burkitt’s lymphoma of the head and neck region in a Nigeria tertiary hospital. East. Afr. J. Med. 2005; 24(3): 139–42.
  37. Blum K.A., Lozansky G., Byrd J. Adult Burkitt’s leukemia and lymphoma. Blood 2004; 20: 32–7.
  38. Warnke R., Weiss L., Chan J. et al. Atlas of Tumor Pathologie. Tumors of the Lymph Nodes and Spleen. Washington: Armed Forces Institute of Pathology, 1999: 221–32.
  39. Kittivorapart J., Chinthammitr Y. Incidence and risk factors of bone marrow involvement by non-Hodgkin lymphoma. J. Med. Assoc. Thai. 2011; 94(Suppl. 1): S239–45.
  40. Ziegler J.L., Morrow R.H., Fass L. et al. Treatment of Burkitt’s lymphoma tumor with cyclophosphamide. Cancer 1970; 26(2): 474–84.
  41. Janota I. Involvement of the nervous system in malignant lymphoma in Nigeria. Br. J. Cancer 1966; 20: 47.
  42. Booth K., Burkitt D.P., Basset D.J. et al. Burkitt lymphoma in Papua, New Guinea. Br. J. Cancer 1967; 21: 657–64.
  43. Sariban E., Edwards S., Janus C. et al. Central nervous system involvement in American Burkitt’s lymphoma. J. Clin. Oncol. 1983; 1: 677–80.
  44. Wright D.H. Burkitt’s tumor. A post modern study of 50 cases. Br. J. Surg. 1964; 51: 245.
  45. Thomas D., Cortes J., O’Brien S. et al. Hyper-CVAD program in Burkitt’s type adult acute lymphoblastic leukemia. J. Clin. Oncol. 1999; 17: 2461–70.
  46. Murphy S., Fairclough D., Hutchison R. et al. Non-Hodgkin’s lymphoma in childhood: An analysis of the histology, staging and response to the treatment of 338 cases at a single institution. J. Clin. Oncol. 1989; 7: 186–93.
  47. Klumb C.E., Resende L.M., Stefanoff C.G. et al. Burkitt-like lymphoma in an infant: a case report. Rev. Hosp. Clin. Fac. Med. S. Paulo. 2003; 58(1): 33–6.
  48. Hutchinson R.E., Murphy S.B., Fairclough D.L. et al. Diffuse small noncleaved cell lymphoma in children, Burritt’s versus non-Burritt’s types. Results from the Реdiatric Oncology Group and St. Jude Children’s Research Hospital. Cancer 1989; 64: 23–8.
  49. Ferry J.A. Burkitt’s Lymphoma: Clinicopathologic Features and Differential Diagnosis. Oncologist 2006; 11: 375–83.
  50. Shad A., Magrath I. Non-Hodgkin’s lymphoma. Pediatr. Clin. N. Am. 1997; 44: 863–90.
  51. Boerma E.G., van Imhoff G.W., Appel I.M. et al. Gender and age-related differences in Burkitt lymphoma—epidemiological and clinical data from The Netherlands. Eur. J. Cancer 2004; 40: 2781–7.
  52. Huisman T., Tschirch F., Schneider J.F. et al. Burkitt’s lymphoma with bilateral cavernous sinus and mediastinal involvement in a child. Pediatr. Radiol. 2003; 33: 719–21.
  53. Braziel R.M., Arber D.A., Slovac M.L. et al. The Burkitt-like lymphoma: a Southwest Oncologie Group study delineating phenotypic, genotypic and clinical features. Blood 2001; 97(12): 3713–20.
  54. Cheung C.W., Burton C., Smith P. Central nervous system chemoprophylaxis in non-Hodgkin’s lymphoma: current practice in the UK. Br. J. Haematol. 2005; 13(2): 193–200.
  55. McWilliams N., Hatfield W., Jackson R. Epidemiological notes and reports on Burkitt’s lymphoma. Winchester, Virginia. Morbil. Mortal. Wkly. 1997; 46: 4674–8.
  56. Барях Е.А., Кравченко С.К., Обухова Т.Н. и др. Лимфома Беркитта: клиника, диагностика, лечение. Клин. онкогематол. 2009; 2(2): 137–47. [Baryakh Ye.A., Kravchenko S.K., Obukhova T.N et al. Burkitt’s lymphoma: clinical presentation, diagnosis, management. Klin. onkogematol. 2009; 2(2): 137–47. (In Russ.)].
  57. Malani A.K., Gupta C., Weigand R.T. et al. Spinal Burkitt’s lymphoma in adults. Clin. Lymph. Myel. 2006; 6(4): 333–6.
  58. Mizugami T., Mikata A., Hajikano H. et al. Primary spinal epidural Burkitt’s lymphoma. Surg. Neurol. 1987; 28(2): 158–62.
  59. Ses E., N’dri Oka D., Varlet G. et al. Medullary compression by Burkitt lymphoma. Analysis of 7 cases. Neurochirurgie 2001; 47(6): 552–6.
  60. Wilkening A., Brack M., Brandis A. et al. Unusual presentation of a primary spinal Burkitt’s lymphoma. J. Neurol. Neurochirurg. Psychiatry 2001; 70(6): 794–7.
  61. Holland J., Cada M., Ling S. et al. Melena: a rare presentation of childhood Burkitt’s lymphoma. CMAJ 2005; 173(3): 247–8.
  62. Saton S., Saito T., Akiba J. et al. Burkitt lymphoma occurring as a primary lymphomatous effusion. Rinsho Ketsueki 2000; 41(4): 329–33.
  63. Blanc S., Bertrand Y., Lorthois-Ninou S. et al. Burkitt’s lymphoma revealed by a rectal tumor. Arch. Pediatr. 2002; 9(10): 1056–8.
  64. Rakoto-Ratsimba H.N., Razafimahandry H.J.C., Samison L.H. et al. A case of anal Burkitt’s lymphoma. Ann. Chir. 2003; 128(4): 265–7.
  65. Meshref M., Sassolas F., Schell M. et al. Primary cardiac Burkitt lymphoma in a child. Pediatr. Blood Cancer 2004; 42(4): 380–3.
  66. Baloglu H., Turken O., Turuncu L., Kizilkaya E. 24-year-old female with amenorhea: bilateral primary ovarian Burkitt lymphoma. Gynecol. Oncol. 2003; 91(2): 449–51.
  67. Grassi M., Lee A.G. Lymphomatous meningitis of the Burkitt type presenting with multiple cranial neuropathies. Am. J. Ophthalmol. 2002; 133(3): 424–5.
  68. Ardekian L., Rachmiel A., Rosen D. et al. Burkitt’s lymphoma of the oral cavity in Israel. J. Craniomaxillofac. Surg. 1999; 27(5): 294–7.
  69. Барях Е.А., Красильникова Б.Б. Поражение лицевого скелета при спорадическом варианте лимфомы Беркитта. В кн.: Редкие гематологические болезни и синдромы. Под ред. М.А. Волковой. М.: Практическая медицина, 2011: 311–9. [Baryakh Ye.A., Krasilnikova B.B. Porazheniye litsevogo skeleta pri sporadicheskom variante limfomy Berkitta. V kn.: Redkiye gematologicheskiye bolezni i sindromy. Pod red. M.A. Volkovoy (Involvement of facial skeleton in sporadic variant of Burkitt’s lymphoma. In: Rare hematological disorders and syndromes. Ed. by: M.A. Volkova). M.: Prakticheskaya meditsina, 2011: 311–9.]
  70. Banthia V., Jen A., Kacker A. Sporadic Burkitt’s lymphoma of the head and neck in the pediatric population. Int. J. Pediatr. Otorhinolaryngol. 2003; 67(1): 59–65.
  71. Bauer G.P., Volk M.S., Siddiqui S. Burkitt’s lymphoma of the parapharingeal space. Arch. Otolaryngol. Head Neck Surg. 1993; 119(1): 117–20.
  72. Барях Е.А., Валиев Т.Т., Звонков Е.Е. и др. Интенсивная терапия лимфомы Беркитта: описание двух клинических случаев. Гематол. и транс- фузиол. 2007; 1: 41–3. [Baryakh Ye.A., Valiyev T.T., Zvonkov Ye.Ye. et al. Intensive therapy for Burkitt’s lymphoma: presentation of two clinical cases. Gematol. i transfuziol. 2007; 1: 41–3. (In Russ.)].
  73. Shukla N., Trippett T. Non-Hodgkin’s lymphoma in children and adolescents. Curr. Oncol. Rep. 2006; 8(5): 387–94.
  74. Evans J.A., Gribb D.M., Holland F.J. et al. Malignancies in UK in children with HIV infection acquired from mother to child transmission. Arch. Dis. Child. 1997; 76: 330–3.
  75. Subar M., Neri A., Inghirami G. et al. Frequent c-myc oncogene activation and infrequent presence of Epstein-Barr virus genome in AIDS-associated lymphoma. Blood 1988; 72: 667–71.
  76. Beral V., Petrman T., Berkelman R. et al. AIDS-associated non-Hodgkin’s lymphoma. Lancet 1991; 337: 805–9.
  77. Carbone A., Gloghini A., Gaidano G. et al. AIDS-related Burkitt’s lymphoma. Morphologic and immunophenotypic study of biopsy specimens. Am. J. Clin. Pathol. 1995; 103: 561–7.
  78. Kasamon Y.L., Swinnen L.J. Treatment advances in adult Burkitt lymphoma and leukemia. Curr. Opin. Oncol. 2004; 16: 429–35.
  79. Knowles D.M. Etiology and pethogenesis of AIDS-related non-Hodgkin’s lymphoma. Hematol. Oncol. Clin. N. Am. 2003; 17: 785–820.
  80. Martinez-Maza O., Breen E.C. B-cell activation and lymphoma in patients with HIV. Curr. Opin. Oncol. 2002; 14: 528–32.
  81. Mbulaiteye S.M., Clarke C.A., Morton L.M. Burkitt lymphoma risk in U.S. solid organ transplant recipients. Am. J. Hematol. 2013; 88: 245.
  82. Gong J.Z., Stenzel T.T., Bennet E.R. et al. Burkitt’s lymphoma arising in organ transplant recipients: a clinicopathologic study of five cases. Am. J. Surg. Pathol. 2003; 27(6): 818–27.
  83. Davi F., Delecluse H.J., Guiet P. et al. Burkitt-like lymphomas in AIDS patients: characterisation within a series of 103 human immunodeficiency virusassociated non-Hodgkin’s lymphomas. Burkitt’s Lymphoma Study Group. J. Clin. Oncol. 1998; 16: 3788–95.
  84. Барях Е.А., Кравченко С.К., Кременецкая А.М. и др. Лейкоз/лимфома Беркитта: клинические особенности, диагностические критерии, терапевтическая тактика. Клин. онкогематол. 2010; 3(2): 138–43. [Baryakh Ye.A., Kravchenko S.K., Kremenetskaya A.M. et al. Burkitt’s lymphoma: clinical features, diagnostic criteria, therapeutic approach. Klin. onkogematol. 2010; 3(2): 138–43. (In Russ.)].
  85. Валиев Т.Т., Морозова О.В., Попа А.В. и др. Результаты лечения лимфомы Беркитта у детей. Гематол. и трансфузиол. 2012: 57(3): 34–5. [Valiyev T.T., Morozova O.V., Popa A.V. et al. Therapeutic outcomes in childhood Burkitt’s lymphoma. Gematol. i transfuziol. 2012: 57(3): 34–5. (In Russ.)].
  86. Ковригина А.М., Пробатова Н.А. Лимфома Ходжкина и крупноклеточные лимфомы. М.: МИА, 2007: 212. [Kovrigina A.M., Probatova N.A. Limfoma Khodzhkina i krupnokletochnye limfomy (Hodgkin’s lymphoma and large-cell lymphomas). M.: MIA, 2007: 212.]
  87. Тупицын Н.Н., Шолохова Е.Н., Андреева Л.Ю. и др. Иммунодиагностика лимфом. Совр. онкол. Экстравыпуск 2002: 4–12. [Tupitsyn N.N., Sholokhova Ye.N., Andreyeva L.Yu. et al. Immunodiagnosis of lymphomas. Sovr. onkol. Ekstravypusk 2002: 4–12. (In Russ.)].
  88. Луговская С.А., Почтарь М.Е., Тупицын Н.Н. Иммунофенотипиро- вание в диагностике гемобластозов. М., 2005. [Lugovskaya S.A., Pochtar M.Ye., Tupitsyn N.N. Immunofenotipirovaniye v diagnostike gemoblastozov (Immunophenotyping in diagnosis of hematological malignancies). M., 2005.]
  89. Zech L., Haglund U., Nilsson. et al. Characteristic chromosomal abnormalities in biopsies and lymphoid-cell lines from patients with Butkitt and non-Burkitt lymphomas. Int. J. Cancer 1976; 17: 47–56.
  90. Croce C. Role of chromosome translocations in human neoplasia. Cell 1987; 49(2): 155–6.
  91. Showe L.C., Moore R.C., Erikson J. et al. MYC oncogene involved in a t(8;22) chromosome translocation is not altered in it’s putative regulatory regions. Proc. Natl. Acad. Sci. U S A 1987; 84(9): 2824–8.
  92. Tagawa H., Ikeda S., Sawada K. Role of microRNA in the pathogenesis of malignant lymphoma. Cancer Sci. 2013; 10: 121–6.
  93. Sander S., Calado D.P., Srinivasan L. et al. Synergy between PI3K signaling and MYC in Burkitt lymphomagenesis. Cancer Cell 2012; 22(2): 167–79.
  94. Love C., Sun Z., Jima D. The genetic landscape of mutations in Burkitt lymphoma. Nat. Genet. 2012; 44(12): 1321–5.
  95. Green T.M., Nielsen O., de Stricker K. et al. High levels of nuclear MYC protein predict the presence of MYC rearrangement in diffuse large B-cell lymphoma. Am. J. Surg. Pathol. 2012; 36(4): 612–9.
  96. Aukema S.M., Siebert R., Schuuring E. et al. Double-hit B-cell lymphomas. Blood 2011; 117(8): 2319–31.
  97. Ben-Neriah S., Woods R., Steidl C. et al. Lymphomas with concurrent BCL2 and MYC translocations: the critical factors associated with survival. Blood 2009; 114: 2273–9.
  98. Johnson N.A., Savage K.J., Ludkovski O. et al. Lymphomas with concurrent BCL2 and MYC translocations: the critical factors associated with survival. Blood 2009; 114: 2273–9.
  99. Aukema S.M., Siebert R., Schuuring E. et al. Double-hit B-cell lymphomas. Blood 2011; 117: 2319–31.
  100. Niitsu N., Okamoto M., Miura I. et al. Clinical features and prognosis of de novo diffuse large B-cell lymphoma with t(14;18) and 8q24/c-MYC translocations. Leukemia 2009; 23: 777–83.
  101. Salaverria I., Siebert R. The gray zone between Burkitt’s lymphoma and diffuse large B-cell lymphoma from a genetics perspective. J. Clin. Oncol. 2011; 29: 1835–43.
  102. Snuderl M., Kolman O., Chen Y. et al. B-cell Lymphomas with Concurrent IGH-BCL2 and MYC Rearrangements Are Aggressive Neoplasms with Clinical and Pathologic Features Distinct from Burkitt Lymphoma and Diffuse Large B-cell Lymphoma. Am. J. Surg. Pathol. 2010; 34(3): 327–40.
  103. Tomita N. BCL2 and MYC Dual-Hit Lymphoma/Leukemia. J. Clin. Exp. Hematopathol. 2011; 51(1): 7–12.
  104. Pillai R.K., Sathanoori M., Van Oss S.B. Double-hit B-cell Lymphomas With BCL6 and MYC Translocations Are Aggressive, Frequently Extranodal Lymphomas Distinct From BCL2 Double-hit B-cell Lymphomas. Am. J. Surg. Pathol. 2013; 37(3): 323–32.
  105. Nakayama S., Yokote T., Iwaki K. Triple-hit B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma associated with a novel complex karyotype including t(2;3)(q21;q27), t(8;14)(q24;q32) and t(14;18)(q32;q21). Br. J. Haematol. 2013; 160(5): 569.
  106. Deibold J. Burkitt lymphoma. In: Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. Ed. by E. Jaffe, N. Harris et al. Washington: IARC Press, 2001: 181–4.
  107. Baccarani M., Corbelli G., Amadori S. et al. Adolescent and adult lymphoblastic leukemia: prognostic features outcome of therapy — a study of 293 patients. Blood 1982; 60: 677–84.
  108. Gill P.S., Meyer P.R., Pavlova Z. et al. B-cell acute lymphoblastic leukemia in adults: clinical, morphologic and immunologic findings. J. Clin. Oncol. 1986; 4: 737–43.
  109. Bernstein J.I., Coleman C.N., Strickler J.G. et al. Combined modality therapy for adult with small noncleaved cell lymphoma (Burkitt and Burkitt-like type). J. Clin. Oncol. 1986; 4: 847–58.
  110. Reiter A., Schrappe M., Tiemann M. et al. Improved treatment results in childhood B-cell neoplasms with tailored intensification of therapy: a report of the Berlin-Frankfurt-Munster Group Trial NHL-BFM-90. Blood 1999; 94(10): 3294–306.
  111. Schwenn M., Blattner S., Lynch E. et al. HiC-COM: a 2-month intensive chemotherapy regimen for children with stage III and IV Burkitt’s lymphoma and B-cell acute lymphoblastic leukemia. J. Clin. Oncol. 1991; 9: 133–8.
  112. Bowman W.P., Shuster J.J., Cook B. et al. Improved survival for children with B-cell acute lymphoblastic leukemia and stage IV small noncleaved-cell lymphoma: a pediatric oncology group study. J. Clin. Oncol. 1996; 14(4): 1252–61.
  113. Patte C., Philip T., Rodary C. et al. High survival rate in advanced-stage B-cell lymphomas and leukemias without CNS involvement with a short intensive polychemotherapy: results from the French Pediatric Oncology Society of a randomized trial of 216 children. J. Clin. Oncol. 1991; 9: 123–32.
  114. Patte C., Michon J., Frappaz D. et al. Therapy of Burkitt and other Bcell acute lymphoblastic leukaemia and lymphoma: experience with the LMB protocols of the SFOP (French Paediatric Oncology Society) in children and adults. Baillieres Clin. Haematol. 1994; 7(2): 339–48.
  115. Magrath I., Adde M., Shad A. et al. Adults and children with small noncleaved-cell lymphoma have similar excellent outcome when treated with the same chemotherapy regimen. J. Clin. Oncol. 1996; 14: 925–34.
  116. Mead G.M., Sydes M.R., Walewski J. et al. An international evaluation of CODOX-M and CODOX-M alternating with IVAC in adult Burkitt’s lymphoma: results of United Kingdom Lymphoma Group LY06 study. Ann. Oncol. 2002; 13(8): 1264–74.
  117. Барях Е.А., Кравченко С.К. Протокол терапии лимфомы Беркитта взрослых по программе ЛБ-М-04. В кн. Программное лечение заболеваний системы крови. Т. II. Под ред. В.Г. Савченко. М.: Практика, 2012: 720–34. [Baryakh Ye.A., Kravchenko S.K. Protokol terapii limfomy Berkitta vzroslykh po programme LB-M-04. V kn. Programmnoye lecheniye zabolevaniy sistemy krovi. T. II. Pod red. V.G. Savchenko (Protocol of therapy for adult Burkitt’s lymphoma in accordance with LB-M-04 program. In: Program therapy for hematological malignancies. Vol. II. Ed. by: V.G. Savchenko). M.: Praktika, 2012: 720–34.]
  118. Thomas D.A., Faderl S., O’Brien S. et al. Chemoimmunotherapy with hyper-CVAD plus rituximab for the treatment of adult Burkitt and Burkitt-type lymphoma or acute lymphoblastic leukemia. Cancer 2006; 106(7): 1569–80.
  119. Fayad L., Thomas D., Romaguera J. Update of the M.D. Anderson Cancer Center experience with hyper-CVAD and rituximab for the treatment of mantle cell and Burkitt-type lymphomas. Clin. Lymph. Myel. 2007; 8(2): 57–62.
  120. Bence Z., Kovacs G., Jakab Z. et al. Lymphomas in adolescents: are childhood lymphoma therapy protocols suitable for this patient group? Magy Onkol. 2008; 52(4): 357–62.
  121. Cairo M.S., Sposto R., Gerrard M. et al. Advanced Stage, Increased Lactate Dehydrogenase, and Primary Site, but Not Adolescent Age (³ 15 Years), Are Associated With an Increased Risk of Treatment Failure in Children and Adolescents With Mature B-Cell Non-Hodgkin’s Lymphoma: Results of the FAB LMB 96 Study. J. Clin. Oncol. 2012; 30(4): 387–93.
  122. Woessmann W., Reiter A. Re-induction approaches to relapsed/ refractory childhood and adolescent non Hodgkin’s lymphoma: BFM perspective. Br. J. Haematol. 2012; 159(1): 41.
  123. Griffin T.C., Weitzman S., Weinstein H. et al. A study of rituximab and ifosfamide, carboplatin, and etoposide chemotherapy in children with recurrent/ refractory B-cell (CD20+) non-Hodgkin lymphoma and mature B-cell acute lymphoblastic leukemia: A report from the Childrens Oncology Group. Pediatr. Blood Cancer 2009; 53: 177–81.
  124. Harris N., Jaffe E., Stein H. et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994; 84: 1361–92.