primary bone lymphoma

Primary Bone Lymphomas: 18F-FDG PET and PET-CT as Methods of Diagnosis and Efficacy Estimation of Antitumor Treatment

AUTOIMMUNE THROMBOCYTOPENIA , , ,

AK Smol’yaninova1, ER Moskalets2, GA Yatsyk1, IE Kostina1, AS Bogolyubskaya3, NG Gabeeva1, EG Gemdzhian1, SA Tatarnikova1, DS Badmadzhapova1, EE Zvonkov1

1 National Research Center for Hematology, 4 Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167

2 European Medical Center, 35 Shchepkina str., Moscow, Russian Federation, 129090

3 NI Pirogov Russian National Research Medical University, 1 Ostrovityanova str., Moscow, Russian Federation, 117997

For correspondence: Anna Konstantinovna Smol’yaninova, MD, PhD, 4 Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167; Tel.: +7(926)912-31-16; e-mail: annmo8@mail.ru

For citation: Smol’yaninova AK, Moskalets ER, Yatsyk GA, et al. Primary Bone Lymphomas: 18F-FDG PET and PET-CT as Methods of Diagnosis and Efficacy Estimation of Antitumor Treatment. Clinical oncohematology. 2020;13(1):33–49 (In Russ).

DOI: 10.21320/2500-2139-2020-13-1-33-49

ABSTRACT

Background. Primary bone lymphoma (PBL) is a rare malignant tumor. Initial examination aimed at detecting all primary lesions is an indispensable prerequisite for the choice of optimal antitumor treatment. Standard methods of diagnosis (X-ray, CT, and MRI) are not always adequate to measure the real tumor mass. Another well-known characteristic feature of PBL is a challenge in evaluating the effect of its treatment because of residual changes in the bones of most patients. However, the data on using 18F-FDG PET, another method of metabolic imaging, in PBL are rather rare in accessible literature.

Aim. To study the specific use of PET with 18F-FDG at initial examination and efficacy estimation of PBL treatment.

Materials & Methods. The trial included 21 PBL patients who received PET with 18F-FDG at initial examination and a month after the end of treatment. The results of 18F-FDG PET imaging were compared with the data obtained by means of structural diagnostic methods (CT and MRI) and the analysis of biopsy samples with pathologic lesions.

Results. Intensive uptake of 18F-FDG (SUVmax 8.6–40.1, mean SUVmax 23.5), according to PET data, was reported in all patients in those tumor lesions which were identified by the structural diagnostic methods and confirmed by biopsies. Besides, each of 21 cases showed pathologic infiltration of adjacent soft tissues with high metabolic activity. In PET-CT with 18F-FDG 13 further tumor localizations were revealed in 8 (38 %) patients. On completing the therapy, according to CT and MRI data, residual changes were observed in all (n = 21, 100 %) patients. The residual metabolic activity in the involved bones was identified in 13 (62 %) patients (SUVmax 2.91–8.7, mean SUVmax 4.2). In 4 of them the residual lesions were subjected to biopsy. None of 4 cases was reported to show tumors. Only in 1 out of 13 patients with residual metabolic changes a tumor relapse was detected. Overall 10-year survival in the groups of patients with and without FDG+ residual changes was 91 % and 100 %, respectively, with insignificant differences (p = 0.39).

Conclusion. PET-CT with 18F-FDG is a highly sensitive technique for evaluating the primary lesion volumes in PBL patients. In 100 % of bone and soft tissue lesions an intensive uptake of 18F-FDG was observed. At the same time our study showed persistent metabolic activity on completing antitumor treatment in more than a half of patients, and in most of them it was not caused by tumor. Therefore, in our view, ongoing residual metabolic activity in PBL cannot always be regarded as an indication for continued treatment or consolidation radiotherapy.

Keywords: primary bone lymphoma, survival, positron emission tomography, diagnosis, efficacy estimation of antitumor treatment.

Received: August 2, 2019

Accepted: December 5, 2019

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REFERENCES

  1. Matikas A, Briasoulis A, Tzannou I, et al. Primary bone lymphoma: a retrospective analysis of 22 patients treated in a single tertiary center. Acta Haematol. 2013;130(4):291–6. doi: 10.1159/000351051.

  2. Bacci G, Jaffe N, Emiliani E, et al. Therapy for primary non-Hodgkin’s lymphoma of bone and a comparison of results with Ewing’s sarcoma. Ten year’s experience at the Istituto Ortopedico Rizzoli. Cancer. 1986;57(8):1468–72. doi: 10.1002/1097-0142(19860415)57:8<1468::aid-cncr2820570806>3.0.co;2-0.

  3. Fidias P, Spiro I, Scobczak ML, et al. Long-term results of combined modality therapy in primary bone lymphomas. Int J Radiat Oncol Biol Phys. 1999;45(5):1213–38. doi: 10.1016/s0360-3016(99)00305-3.

  4. Messina C, Ferreri AJ, Govi S, et al. Clinical features, management and prognosis of multifocal primary bone lymphoma: a retrospective study of the international Extranodal Lymphoma Study Group (the IELSG 14 study). Br J Haematol. 2014;164(6):834–40. doi: 10.1111/bjh.12714.

  5. Морозова А.К., Звонков Е.Е., Мамонов В.Е. и др. Первичные лимфатические опухоли костей и мягких тканей: сравнительная оценка результатов лечения. Терапевтический архив. 2012;84(7):42–9.

    [Morozova AK, Zvonkov EE, Mamonov VE, et al. Primary lymphomas of bones and soft tissues: comparative assessment of treatment results. Terapevticheskii arkhiv. 2012;84(7):42–9. (In Russ)]

  6. Gabeeva NG, Zvonkov EE, Morozova AK, et al. Long-term follow-up of primary bone diffuse large B-cell lymphoma treated with m NHL-BFM-90. Blood. 2016;128(22):3025.

  7. Смольянинова А.К., Габеева Н.Г., Мамонов В.Е. и др. Первичная лимфома костей: 10-летние результаты проспективного исследования в одной клинике. Гематология и трансфузиология. 2018;63(S1):181.

    [Smol’yaninova AK, Gabeeva NG, Mamonov VE, et al. Primary bone lymphoma: 10-year results of a prospective single-center trial. Gematologiya i transfuziologiya. 2018;63(S1):181. (In Russ)]

  8. Lewis VO, Primus G, Anastasi J, et al. Oncologic outcomes of primary lymphomas of bone in adults. Clin Orthop Rel Res. 2003;415:90–7. doi: 10.1097/01.blo.0000093901.12372.ad.

  9. Ostrowski ML, Unni KK, Banks PM, et al. Malignant Lymphoma of Bone. Cancer. 1986;58(12):2646–55. doi: 10.1002/1097-0142(19861215)58:12<2646::aid-cncr2820581217>3.0.co;2-u.

  10. Смольянинова А.К., Габеева Н.Г., Мамонов В.Е. и др. Первичные лимфомы костей: долгосрочные результаты проспективного одноцентрового исследования. Клиническая онкогематология. 2019;12(3):247–62. doi: 10.21320/2500-2139-2019-12-3-247-262.

    [Smol’yaninova AK, Gabeeva NG, Mamonov VE, et al. Primary Bone Lymphomas: Long-Term Results of a Prospective Single-Center Trial. Clinical oncohematology. 2019;12(3):247–62. doi: 10.21320/2500-2139-2019-12-3-247-262. (In Russ)]

  11. Ueda T, Aozasa K, Ohsawa M, et al. Malignant lymphomas of bone in Japan. Cancer. 1989;64(11):2387–92. doi: 10.1002/1097-0142(19891201)64:11<2387::aid-cncr2820641132>3.0.co;2-1

  12. Meignan M, Barrington S, Itti E, et al. Report on the 4th international workshop on positron emission tomography in lymphoma held in Menton, France, 3–5 October 2012. Leuk Lymphoma. 2013;55(1):31–7. doi: 10.3109/10428194.2013.802784.

  13. Егорова Е.К., Габеева Н.Г., Мамонов В.Е. и др. Первичные лимфатические опухоли костей: описание двух случаев и обзор литературы. Онкогематология. 2008;3(4):5–10.

    [Egorova EK, Gabeeva NG, Mamonov VE, et al. Primary lymphatic tumors of bones: two case reports and a review of l Onkogematologiya. 2008;3(4):5–10. (In Russ)]

  14. Christie DR, Dear K, Le T, et al. Limited chemotherapy and shrinking field radiotherapy for osteolymphoma (primary bone lymphoma): results from the trans-Tasman Radiation Oncology Group 99.04 and Australasian Leukaemia and Lymphoma Group LY02 prospective trial. Int J Radiat Oncol Biol Phys. 2011;80(4):1164–70. doi: 10.1016/j.ijrobp.2010.03.036.

  15. Iwaya Y, Tekenaka K, Akamatsu T. Primary Gastric Diffuse Large B-cell Lymphoma with Orbital Involvement: Diagnostic Usefulness of 18-fluorodeoxyglucose Positron Emission Tomography. Intern Med. 2011;50(18):1953–6. doi: 10.2169/internalmedicine.50.5524.

  16. Demircay E, Hornicek J, Mankin HJ, at al. Malignant Lymphoma of Bone: A Review of 119 Patients. Clin Orthop Relat Res. 2013;471(8):2684–90. doi: 10.1007/s11999-013-2991-x.

  17. Fletcher CDM, Unni KK, Mertens F. (eds) Pathology and genetics of tumours of soft tissue and bone. World Health Organization Classification of Tumours. 3rd Edition. Lyon: IARC Press; 2002.

  18. Fletcher CDM. The evolving classification of soft tissue tumours: an update based on the new WHO classification. Histopathology. 2006;48(1):3–12. doi: 10.1111/j.1365-2559.2005.02284.x.

  19. Fletcher CDM, Bridge JA, Hogendoorn P, Mertens F. World health organization classification of tumours of soft tissue and bone. 4th edition. Lyon: IARC Press; 2013. 468 p.

  20. Krishnan А, Shirkhoda А, Tehranzadeh Т, et al. Primary Bone Lymphoma: Radiographic–MR Imaging Correlation. RadioGraph. 2003;23(6):1371–87. doi: 10.1148/rg.236025056.

  21. Mulligani ME, Kransdorf MJ. Sequestra in Primary Lymphoma of Bone: Prevalence and Radiologic Features. Am J Roentgenol. 1993;160(6):1245–8. doi: 10.2214/ajr.160.6.8498226.

  22. Canete AN, Bloem HL, Kroon HM. Primary bone tumors of the spine. Radiologia. 2016;58(Suppl 1):68–80. doi: 10.1016/j.rx.2016.01.001.

  23. Mikhaeel NG. Primary bone lymphoma. Clin Oncol. 2012;24(5):366–70. doi: 10.1016/j.clon.2012.02.006.

  24. Hicks DC, Gokan T, O’Keefe RJ, et al. Primary lymphoma of bone: correlation of magnetic resonance imaging features with cytokine production by tumor cells. Cancer. 1995;75(4):973–80. doi: 10.1002/1097-0142(19950215)75:4<973::aid-cncr2820750412>3.0.co;2-8.

  25. Messina C, Christie D, Zucca E, et al. Primary and secondary bone lymphomas. Cancer Treat Rev. 2015;41(3):235–46. doi: 10.1016/j.ctrv.2015.02.001.

  26. Remier RR, Bruce AC, Yong RC, et al. Lymphoma Presenting in Bone. Results of Histopathology, Staging, and Therapy. Ann Inter Med. 1977;87(1):50–5. doi: 10.7326/0003-4819-87-1-50.

  27. Cheson BD, Fisher RI, Barrington SF, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32(27):3059–67. doi: 10.1200/JCO.2013.54.8800.

  28. Jawad MU, Schneiderbauer MM, Min ES, et al. Primary Lymphoma of Bone in Adult Patients. Cancer. 2010;116(4):871–9. doi: 10.1002/cncr.24828.

  29. Schaefer NG, Strobel K, Taverna C, et al. Bone involvement in patients with lymphoma: the role of FDG-PET/CT. Eur J Nucl Med Mol Imag. 2007;34(1):60–7. doi: 10.1007/s00259-006-0238-8.

  30. Ramadan KM, Shenkier T, Sehn LH, et al. 131 patients with primary bone lymphoma: a population-based study of successively treated cohorts from the British Columbia Cancer Agency. Ann Oncol. 2007;18(1):129–35. doi: 10.1093/annonc/mdl329.

  31. Park YH, Kim S, Choi SJ, et al. Clinical impact of whole-body FDG-PET for evaluation of response and therapeutic decision-making of primary lymphoma of bone. Ann Oncol. 2005;16(8):1401–2. doi: 10.1093/annonc/mdi234.

  32. Park YH, Choi SJ, Ryoo BY, et al. PET imaging with F-18 fluorodeoxyglucose for primary lymphoma of bone. Clin Nucl Med. 2005;30(2):131–4. doi: 10.1097/00003072-200502000-00020.

  33. Singh Т, Satheesh С, Lakshmaiah С, et al. Primary bone lymphoma: A report of two cases and review of the literature. J Cancer Res Ther. 2010;6(3):296–8. doi: 10.4103/0973-1482.73366.

  34. Wang LJ, Wu HB, Wang M, et al. Utility of F-18 FDG PET/CT on the evaluation of primary bone lymphoma. Eur J Radiol. 2015;84(11):2275–9. doi: 10.1016/j.ejrad.2015.09.011.

  35. Baar J, Burkes RL, Gospodarowicz M. Primary non-Hodgkin’s lymphoma of bone. Semin Oncol. 1999;26(3):270–5.

  36. Liu Y. The role of 18F-FDG PET/CT in staging and restaging primary bone lymphoma. Nucl Med Commun. 2017;38(4):319–24. doi: 10.1097/MNM.0000000000000652.

  37. Kim SY, Shin DY, Lee SS. Clinical characteristics and outcomes of primary bone lymphoma in Korea. Korean J Hematol. 2012;47(3):213–8. doi: 10.5045/kjh.2012.47.3.213.

  38. Milks KS, McLean TW, Anthony EY. Imaging of primary pediatric lymphoma of bone. Pediatr Radiol. 2016;46(8):1150–7. doi: 10.1007/s00247-016-3597-8.

  39. Zinzani PL, Carrillo G, Ascani S, et al. Primary bone lymphoma: experience with 52 patients. Haematologica. 2003;88(3):280–5.

  40. Baar J, Burkes R, Bell R. Primary Non-Hodgkin’s Lymphoma of Bone. A clinicopathologic study. Cancer. 1994;73(4):1194–9. doi: 10.1002/1097-0142(19940215)73:4<1194::aid-cncr2820730412>3.0.co;2-r.

  41. Choi J, Raghavan M. Diagnostic imaging and Image-Guided Therapy of Skeletal Metastases. Cancer Control. 2012;19(2):102–12. doi: 10.1177/107327481201900204.

  42. Hwang S. Imaging of lymphoma of musculoskeletal system. Magn Reson Imag Clin N Am. 2010;18(1):75–93. doi: 10.1016/j.mric.2009.09.006.

  43. Rapoport AP, Constine LS, Packman CH, et al. Treatment of Multifocal Lymphoma of Bone With Intensified Promace-Cytabom Chemotherapy and Involved Field Radiotherapy. Am J Hematol. 1998;58(1):1–7. doi: 10.1002/(SICI)1096-8652(199805)58:1<1::AID-AJH1>3.0.CO;2-X.

  44. Seymour JF. Extra-nodal lymphoma in rare localisations: bone, breast and testes. Hematol Oncol. 2013;31(Suppl 1):60–3. doi: 10.1002/hon.2081.

  45. Ng AP, Wirth A, Seymour JF, et al. Early therapeutic response assessment by (18)FDG-positron emission tomography during chemotherapy in patients with diffuse large B-cell lymphoma: Isolated residual positivity involving bone is not usually a predictor of subsequent treatment failure. Leuk Lymphoma. 2007;48(3):596–600. doi: 10.1080/10428190601099965.

  46. Rigacci L, Kovalchuk S, Berti V, et al. The use of Deauville 5-point score could reduce the risk of false-positive fluorodeoxyglucose-positron emission tomography in the posttherapy evaluation of patients with primary bone lymphomas. World J Nucl Med. 2018;17(3):157–65. doi: 10.4103/wjnm.WJNM_42_17.

  47. Juweid ME, Wiseman GA, Vose JM, et al. Response assessment of aggressive non-Hodgkin’s lymphoma by integrated International Workshop Criteria and fluorine-18-fluorodeoxyglucose positron emission tomography. J Clin Oncol. 2005;23(21):4652–61. doi: 10.1200/JCO.2005.01.891.

  48. Cheson BD, Pfistner B, Juweid ME, et al. International Harmonization Project for malignant lymphoma. J Clin Oncol. 2007;25(5):579–86. doi: 10.1200/JCO.2006.09.2403.

  49. Juweid ME, Stroobants S, Hoekstra OS, et al. Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol. 2007;25(5):571–8. doi: 10.1200/JCO.2006.08.2305.

  50. Albano D, Agnello F, Patti C, et al. Whole-body magnetic resonance imaging and FDG-PET/CT for lymphoma staging: Assessment of patient experience. Egypt J Radiol Nucl Med. 2017;48(4):1043–7. doi: 1016/j.ejrnm.2017.06.002.

  51. Wang D, Huo Y, Chen S et al. Whole-body MRI versus 18F-FDG PET/CT for pretherapeutic assessment and staging of lymphoma: a meta-analysis. OncoTarg Ther. 2018;11:3597–608. doi: 10.2147/OTT.S148189.

  52. Galia M, Albano D, Tarella C, et al. Whole body magnetic resonance in indolent lymphomas under watchful waiting: the time is now. Eur Radiol. 2017;28(3):1187–93. doi: 10.1007/s00330-017-5071-x.

  53. Toledano-Massiah S, Luciani A, Itti E, et al. Whole-Body Diffusion-weighted Imaging in Hodgkin Lymphoma and Diffuse Large B-Cell Lymphoma. RadioGraph. 2015;35(3):747–64. doi: 10.1148/rg.2015140145.

  54. Koh D, Collins DJ. Diffusion-Weighted MRI in the Body: Applications and Challenges in Oncology. Am J Roentgenol. 2007;188(6):1622–35. doi: 10.2214/AJR.06.1403.

Primary Bone Lymphomas: Long-Term Results of a Prospective Single-Center Trial

LYMPHOID TUMORS , ,

AK Smol’yaninova, NG Gabeeva, VE Mamonov, SA Tatarnikova, LG Gorenkova, DS Badmadzhapova, AM Kovrigina, EG Gemdzhian, EE Zvonkov

National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167

For correspondence: Anna Konstantinovna Smol’yaninova, MD, PhD, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167; Tel.: +7(495)612-23-61, +7(926)912-31-16; e-mail: annmo8@mail.ru

For citation: Smol’yaninova AK, Gabeeva NG, Mamonov VE, et al. Primary Bone Lymphomas: Long-Term Results of a Prospective Single-Center Trial. Clinical oncohematology. 2019;12(3):247–62 (In Russ).

doi: 10.21320/2500-2139-2019-12-3-247-262

ABSTRACT

Background. Primary bone lymphomas (PBL) are rare extranodal lymphomas. In more than 90 % of cases they are reported as diffuse large B-cell lymphomas (DLBCL). At local (IE) stage of PBL the standard R-CHOP immunotherapy demonstrates efficacy over 90 %. If, however, such poor prognostic factors (PPF) as multiple bone lesions (IVЕ stage), increased lactate dehydrogenase (LDH) activity, B-symptoms, and large tumor mass are identified, R-CHOP efficacy tends to decrease. There is currently no optimal regimen for treatment of PBL patients with PPF. We suggest intensified multi-agent chemotherapy for this category of patients.

Aim. To assess long-term results of prospective single-center trial on the use of high-dose mNHL-BFM-90 program in patients with primary bone DLBCL and PPF.

Materials & Methods. The trial included 33 patients with primary bone DLBCL followed-up at the National Medical Hematology Research Center from 2006 to 2018. The median age of patients was 44 years (range 16–78 years). The spectrum of assessed data included main clinical, laboratory, X-ray and MRI tumor characteristics as well as survival rates and prognostic factors.

Results. PPF were identified in 29 (88 %) patients, out of them 20 (61 %) patients had an advanced stage (˃ IE), 20 (59 %) patients showed an increased LDH activity, B-symptoms were identified in 15 (45 %) patients, and large tumor mass was reported in 23 (71 %) patients. High-dose antitumor treatment (mNHL-BFM-90) was administered in 27 out of 33 patients. Overall and progression-free survival within the period of 5 years was 92 %. None of PPF significantly influenced survival rates.

Conclusion. The use of high-dose mNHL-BFM-90 program in PBL with poor prognosis achieves long-term remissions in 92 % patients. We recommend mNHL-BFM-90 as a therapy of choice for PBL patients with poor prognosis.

Keywords: primary bone lymphoma, diffuse large B-cell lymphoma, high-dose intensified multi-agent mNHL-BFM-90 program.

Received: January 25, 2019

Accepted: May 12, 2019

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REFERENCES

  1. Matikas A, Briasoulis A, Tzannou I, et al. Primary bone lymphoma: a retrospective analysis of 22 patients treated in a single tertiary center. Acta Haematol. 2013;130(4):291–6. doi: 10.1159/000351051.

  2. Bacci G, Jaffe N, Emiliani E, et al. Therapy for primary non-Hodgkin’s lymphoma of bone and a comparison of results with Ewing’s sarcoma. Ten year’s experience at the Istituto Ortopedico Rizzoli. Cancer. 1986;57(8):1468–72. doi: 10.1002/1097-0142(19860415)57:8<1468::aid-cncr2820570806>3.0.co;2-0.

  3. Fidias P, Spiro I, Scobczak ML, et al. Long-term results of combined modality therapy in primary bone lymphomas. Int J Radiat Oncol Biol Phys. 1999;45(5):1213–8. doi: 10.1016/s0360-3016(99)00305-3.

  4. Lewis VO, Primus G, Anastasi J, et al. Oncologic outcomes of primary lymphomas of bone in adults. Clin Orthop Rel Res. 2003;415:90–7. doi: 10.1097/01.blo.0000093901.12372.ad.

  5. Ostrowski ML, Unni KK, Banks PM, et al. Malignant Lymphoma of Bone. Cancer. 1986;58(12):2646–55. doi: 10.1002/1097-0142(19861215)58:12<2646::aid-cncr2820581217>3.0.co;2-u.

  6. Ramadan KM, Shenkier T, Sehn LH, et al. A clinicopathological retrospective study of 131 patients with primary bone lymphoma: a population-based study of successively treated cohorts from the British Columbia Cancer Agency. Ann Oncol. 2006;18(1):129–35. doi: 10.1093/annonc/mdl329.

  7. Ueda T, Aozasa K, Ohsawa M, et al. Malignant lymphomas of bone in Japan. Cancer. 1989;64(11):2387–92. doi: 10.1002/1097-0142(19891201)64:11<2387::aid-cncr2820641132>3.0.co;2-1.

  8. Звонков Е.Е., Красильникова Б.Б., Махиня В.А. и др. Первый опыт применения модифицированной программы NHL-BFM-90 у взрослых больных первичной диффузной В-крупноклеточной лимфосаркомой желудка с неблагоприятным прогнозом. Терапевтический архив. 2006;78(7):38–46.

    [Zvonkov EE, Krasil’nikova BB, Makhinya VА, et al. Pilot experience with the modified program NHL–BFM–90 in adult patients with primary diffuse large В-cell gastric lymphosarcoma with unfavorable prognosis. Terapevticheskii arkhiv. 2006;78(7):38–46. (In Russ)]

  9. Кравченко С.К., Барях Е.А., Замятина В.И. и др. Высокодозная терапия лимфомы Беркитта у больных старше 40 лет. Терапевтический архив. 2008;80(7):9–18.

    [Kravchenko SK, Baryakh EA, Zamyatina VI, et al. High–dose therapy of Berkitt’s lymphoma in patients over 40 years of age. Terapevticheskii arkhiv. 2008;80(7):9–18. (In Russ)]

  10. Магомедова А.У., Кравченко С.К., Кременецкая А.М. и др. Модифицированная программа NHL-BFM-90 для лечения больных диффузной В-крупноклеточной лимфосаркомой. Терапевтический архив. 2006;78(10):44–7.

    [Magomedova AU, Kravchenko SK, Kremenetskaya AM, et al. The modified program NHL-BFM-90 in the treatment of patients with diffuse large B-cell lymphosarcoma. Terapevticheskii arkhiv. 2006;78(10):44–7. (In Russ)]

  11. Горенкова Л.Г., Кравченко С.К., Мисюрин А.В. и др. Клиническая и молекулярная оценки эффективности высокодозной химиотерапии при анаплазированной Т-крупноклеточной АЛК-позитивной лимфоме у взрослых. Гематология и трансфузиология. 2012;57(3):43.

    [Gorenkova LG, Kravchenko SK, Misyurin AV, et al. Clinical and molecular evaluation of the efficacy of high-dose chemotherapy in adult patients with anaplastic large T-cell ALK-positive lymphoma. Gematologiya i transfuziologiya. 2012;57(3):43. (In Russ)]

  12. Морозова А.К., Звонков Е.Е., Кременецкая А.М. и др. Первый опыт применения модифицированной программы NHL-BFM-90 при лечении первичной диффузной B-крупноклеточной лимфосаркомы костей и мягких тканей с факторами неблагоприятного прогноза. Терапевтический архив. 2009;81(7):61–5.

    [Morozova AK, Zvonkov EE, Kremenetskaya AM, et al. Initial experience with using modified NHL-BFM-90 program in management of primary diffuse large B-cell lymphosarcoma of bones and soft tissues with unfavorable prognostic factors. Terapevticheskii arkhiv. 2009;81(7):61–5. (In Russ)]

  13. Морозова А.К., Звонков Е.Е., Мамонов В.Е. и др. Первичные лимфатические опухоли костей и мягких тканей: сравнительная оценка результатов лечения. Терапевтический архив. 2012;84(7):42–9.

    [Morozova AK, Zvonkov EE, Mamonov VE, et al. Primary lymphomas of bones and soft tissues: comparative assessment of treatment results. Terapevticheskii arkhiv. 2012;84(7):42–9. (In Russ)]

  14. Gill P, Wenger D, Inwards D. Primary lymphomas of bone. Clin Lymph Myel. 2005;6(2):140–2. doi: 10.3816/CLM.2005.n.041.

  15. Cheson BD, Horning SJ, Coiffier B, et al. Report of an international workshop to standardize response criteria for non-Hodgkin’s lymphomas. NCI Sponsored International Working Group. J Clin Oncol. 1999;17(4):1244. doi: 10.1200/JCO.1999.17.4.1244.

  16. Juweid ME, Wiseman GA, Vose JM, et al. Response assessment of aggressive non-Hodgkin’s lymphoma by integrated International Workshop Criteria and fluorine-18-fluorodeoxyglucose positron emission tomography. J Clin Oncol. 2005;23(21):4652–61. doi: 10.1200/JCO.2005.01.891.

  17. Cheson BD, Pfistner B, Juweid ME, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007; 25(5):579–86. doi: 10.1200/JCO.2006.09.2403.

  18. Juweid ME, Stroobants S, Hoekstra OS, et al. Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol. 2007;25(5):571–8. doi: 10.1200/JCO.2006.08.2305.

  19. Common Terminology Criteria for Adverse Events, version 3.0 (CTCAE). Published August 9, 2006. Available at: http://ctep.cancer.gov/protocolDevelopment/electronic_applications/docs/ctcaev3.pdf. (accessed 14.04.2019).

  20. Hans CP, Weisenburger DD, Greiner TC, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004;103(1):275–82. doi: 10.1182/blood-2003-05-1545.

  21. Messina C, Ferreri AJ, Govi S, et al. Clinical features, management and prognosis of multifocal primary bone lymphoma: a retrospective study of the international Extranodal Lymphoma Study Group (the IELSG 14 study). Br J Haematol. 2014;164(6):834–40. doi: 10.1111/bjh.12714.

  22. Reddy N, Greer JP. Primary bone lymphoma: a set of unique problems in management. Leuk 2009;51(1):1–2. doi: 10.3109/10428190903470877.

  23. Baar J, Burkes R, Bell R, et al. Primary Non-Hodgkin’s Lymphoma of Bone. A clinicopathologic study. Cancer. 1994;73(4):1194–9. doi: 10.1002/1097-0142(19940215)73:4<1194::aid-cncr2820730412>3.0.co;2-r.

  24. Bacci G, Ferraro A, Casadei R, et al. Primary lymphoma of bone: Long term results in patients treated with vincristine–adriamycin–cyclophosphamide and local radiation. J Chemother. 1991;3(3):189–93. doi: 10.1080/1120009x.1991.11739091.

  25. Jones D, Kraus MD, Dorfman DM. Lymphoma presenting as a solitary bone lesion. Am J Clin Pathol. 1999;111(2):171–8. doi: 10.1093/ajcp/111.2.171.

  26. Limb D, Dreghorn C, Murphy JK, Mannion R. Primary lymphoma of bone. Int Orthop. 1994;18(3):180–3. doi: 10.1007/bf00192476.

  27. Govi S, Christie D, Messina C, et al. The clinical features, management and prognostic effects of pathological fractures in a multicenter series of 373 patients with diffuse large B-cell lymphoma of the bone. Ann Oncol. 2013;25(1):176–81. doi: 10.1093/annonc/mdt482.

  28. Pilorge S, Harel S, Ribrag V, et al. Primary bone diffuse large B-cell lymphoma: a retrospective evaluation on 76 cases from French institutional and LYSA studies. Leuk Lymphoma. 2016;57(12):2820–6. doi: 10.1080/10428194.2016.1177180.

  29. Christie DR, Barton MB, Bryant G, et al. Osteolymphoma (primary bone lymphoma): An Australian review of 70 cases. Australasian Radiation Oncology Lymphoma Group (AROLG). Aust N Z J Med. 1999;29(2):214–9. doi: 10.1111/j.1445-5994.1999.tb00686.x.

  30. Santini D, Vincenzi B, Hannon RA, et al. Phase II trial evaluating the palliative benefit of second-line zoledronic acid in breast cancer patients with either a skeletal-related event or progressive bone metastases despite first-line bisphosphonate therapy. J Clin Oncol. 2006;24(30):4895–900. doi: 10.1200/JCO.2006.05.9212.

  31. Shoji H, Miller TR. Primary reticulum cell sarcoma of bone: Significance of clinical features upon the prognosis. Cancer. 1971;28(5):1234–44. doi: 10.1002/1097-0142(1971)28:5<1234::aid-cncr2820280522>3.0.co;2-l.

  32. Hayase E, Kurosawa M, Suzuki H, et al. Primary Bone Lymphoma: A Clinical Analysis of 17 Patients in a Single Institution. Acta Haematol. 2015;134(2):80–5. doi: 10.1159/000375437.

  33. Tao R, Allen PK, Rodriguez A, et al. Benefit of consolidative radiation therapy for primary bone diffuse large B-cell lymphoma. Int J Radiat Oncol Biol Phys. 2015;92(1):122–9. doi: 10.1016/j.ijrobp.2015.01.014.

  34. Ali SM, Demers LM, Leitzel K, et al. Baseline serum NTx levels are prognostic in metastatic breast cancer patients with bone-only metastasis. Ann Oncol. 2004;15(3):455–9. doi: 10.1093/annonc/mdh089.

  35. Doll C, Wulff B, Rossler J, et al. Primary B-cell lymphoma of bone in children. Eur J Pediatr. 2001;160(4):239–42. doi: 10.1007/s004310000711.

  36. Dosoretz DE, Murphy GF, Raymond AK, et al. Radiation Therapy for Primary Lymphoma of Bone. Cancer. 1983;51(1):44–6. doi: 10.1002/1097-0142(19830101)51:1<44::aid-cncr2820510111>3.0.co;2-d.

  37. Kransdorf MJ. Malignant soft-tissue tumors in a large referral population: distribution of diagnoses by age, sex, and location. Am J Roentgenol. 1995;164(1):129–34. doi: 10.2214/ajr.164.1.7998525.

  38. Wang CC. Treatment of primary reticulum-cell sarcoma of bone by radiation. N Engl J Med. 1968;278(24):1331–2. doi: 10.1056/NEJM196806132782407.

  39. Jacobs AJ, Michels R, Stein J, et al. Socioeconomic and demographic factors contributing to outcomes in patients with primary lymphoma of bone. J Bone Oncol. 2015;4(1):32–6. doi: 10.1016/j.jbo.2014.11.002.

  40. Dos Santos TM, Zumarraga JP, Reaes FM, et al. Primary bone lymphomas: retrospective analysis of 42 consecutive cases. Acta Ortop Bras. 2018;26(2):103–7. doi: 10.1590/1413-785220182602185549.

  41. Wu H, Zhang L, Shao M, Sokol L, et al. Prognostic Significance Of Soft Tissue Involvement, International Prognostic Index In Primary Bone Lymphoma: A Single Institutional Experience. Br J Haematol. 2014;166(1):60-8. doi: 10.1111/bjh.12841.

  42. Zhang HY, Zhu J, Song YQ, et al. Clinical characterization and outcome of primary bone lymphoma: a retrospective study of 61 Chinese patients. Sci Rep. 2016;6(1):28834. doi: 10.1038/srep28834.

  43. Alencar A, Pitcher D, Byrne G at al. Primary bone lymphoma – the University of Miami Experience. Leuk Lymphoma. 2009;51(1):39–49. doi. 10.3109/10428190903308007.

  44. Kim SY, Shin DY, Lee SS. Clinical characteristics and outcomes of primary bone lymphoma in Korea. Korean J Hematol. 2012;47(3): 213–8. doi: 10.5045/kjh.2012.47.3.213.

  45. Held G, Zeynalova S, Murawski N, et al. Impact of rituximab and radiotherapy on outcome of patients with aggressive B-cell lymphoma and skeletal involvement. J Clin Oncol. 2013;31(32):4115–22. doi: 10.1200/JCO.2012.48.0467.

  46. Zhu Y, Yue C, Wu B, et al. Clinical characteristics and outcomes of 31 patients with primary bone lymphoma. Nan Fang Yi Ke Da Xue Xue Bao. 2013;33(3):444–7.

  47. Barbieri E, Cammellin C, Mauro F et al. Primary Non-Hodgkin lymphoma of the bone: treatment and analysis of prognostic factors. Int J Radiat Oncol Biol Phys. 2004;59(3):760–4. doi: 10.1016/j.ijrobp.2003.11.020.

  48. Fairbanks RK, Bonner JA, Inwards CY, et al. Treatment stage 1E primary lymphoma of bone. Int J Radiat Oncol Biol Phys. 1994;28(2):363–72. doi. 10.1016/0360-3016(94)90059-0.

  49. Marshall DT, Amdur RJ, Scarborough MT, et al. Stage 1E primary non Hodgkin’s lymphoma of bone. Clin Orthop Rel Res. 2002;405:216–22. doi: 10.1097/00003086-200212000-00028.

  50. Remier RR, Chabner BA, Yong RC, et al. Lymphoma Presenting in Bone. Results of Histopathology, Staging, and Therapy. Ann Intern Med. 1977;87(1):50–5. doi: 10.7326/0003-4819-87-1-50.

  51. Singh Т, Satheesh С, Lakshmaiah С, et al. Primary bone lymphoma: A report of two cases and review of the literature. J Cancer Res Ther. 2010;6(3):296–8. doi: 10.4103/0973-1482.73366.

  52. Coley BL, Higinbotham NL, Groesbeck HP. Primary reliculum-cell sarcoma of bone. Radiology. 1950;55(5):641–58. doi: 10.1148/55.5.641.

  53. Francis KC, Higinbotham NL, Coley BL. Primary reticulum cell sarcoma of bone; report of 44 cases. Surg Gynecol Obstet. 1954;99(2):142–6.

  54. Badoo S, Sidhu GS. Primary Bone Lymphoma (PBL): Impact Of Novel Treatment On Need For Radiation Therapy (RT), a Population Based Study. Blood. 2013;122(21):3059.

  55. Гаврилина О.А., Звонков Е.Е., Паровичникова Е.Н. и др. Лечение больных диффузной В-крупноклеточной лимфомой с факторами неблагоприятного прогноза по протоколу R-DA-EPOCH/R-HMA: первые результаты российского пилотного многоцентрового исследования. Гематология и трансфузиология. 2016;61(1, прил. 1):38.

    [Gavrilina OA, Zvonkov EE, Parovichnikova EN, et al. Treatment of diffuse large B-cell lymphoma patients with poor prognosis factors using R-DA-EPOCH/R-HMA regimen: first results of the Russian pilot multi-center trial. Gematologiya i transfuziologiya. 2016;61(1, Suppl 1):38. (In Russ)]

  56. Meignan M, Barrington S, Itti E, et al. Report on the 4th international workshop on positron emission tomography in lymphoma held in Menton, France, 3–5 October 2012. Leuk 2014;55(1):31–7. doi: 10.3109/10428194.2013.802784.

  57. Rigacci L, Kovalchuk S, Berti V, et al. The use of Deauville 5-point score could reduce the risk of false-positive fluorodeoxyglucose-positron emission tomography in the posttherapy evaluation of patients with primary bone lymphomas. W J Nucl Med. 2018;17(3):157–65. doi: 10.4103/wjnm.WJNM_42_17.

  58. Cheson BD, Fisher RI, Barrington SF, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: The Lugano classification. J Clin Oncol. 2014;32(27):3059–67. doi: 1200/JCO.2013.54.8800.

  59. Reddy N, Greer JP. Primary bone lymphoma: a set of unique problems in management. Leuk 2009;51(1):1–2. doi: 10.3109/10428190903470877.

  60. Borst AJ, States LJ, Reilly AF, et al. Determining response and recurrence in pediatric B-cell lymphomas of the bone. Pediatr Blood Cancer. 2013;60(8):1281–6. doi: 10.1002/pbc.24523.

  61. Ferreri AJ, Reni M, Ceresoli GL, et al. Therapeutic management with adriamycin-containing chemotherapy and radiotherapy of monostotic and polyostotic primary non-Hodgkin’s lymphoma of bone in adults. Cancer Invest. 1998;16(8):554–61. doi: 10.3109/07357909809032885.

  62. Messina C, Christie D, Zucca E, et al. Primary and secondary bone lymphomas. Cancer Treat Rev. 2015;41(3):235–46. doi: 10.1016/j.ctrv.2015.02.001.

  63. Tomita N, Yokoyama M, Yamamoto W, et al. Central nervous system event in patients with diffuse large B-cell lymphoma in the rituximab era. Cancer Sci. 2012;103(2):245–51. doi: 10.1111/j.1349-7006.2011.02139.x.

  64. Seymour JF. Extra-nodal lymphoma in rare localisations: bone, breast and testes. Hematol Oncol. 2013;31(Suppl 1):60–3. doi: 10.1002/hon.2081.

  65. Guirguis HR, Cheung MC, Mahrous M, et al. Impact of central nervous system (CNS) prophylaxis on the incidence and risk factors for CNS relapse in patients with diffuse large B-cell lymphoma treated in the rituximab era: a single center experience and review of the literature. Br J Haematol. 2012;159(1):39–49. doi: 10.1111/j.1365-2141.2012.09247.x.

  66. Dosoretz DE, Raymond AK, Murphy GF, et al. Primary lymphoma of bone. The relationship of morphologic diversity to clinical behavior. Cancer. 1982;50(5):1009–14. doi: 10.1002/1097-0142(19820901)50:5<1009::aid-cncr2820500532>3.0.co;2-0.

  67. Rathmell AJ, Gospodarowicz MK, Sutcliffe SB, et al. Localised lymphoma of bone: prognostic factors and treatment recommendations. The Princess Margaret Hospital Lymphoma Group. Br J Cancer. 1992;66(3):603–6. doi: 10.1038/bjc.1992.322.

  68. Dubey P, Ha CS, Besa PC, et al. Localized primary malignant lymphoma of bone. Int J Radiat Oncol Biol Phys. 1997;37(5):1087–93. 10.1016/S0360-3016(97)00106-5.

  69. Gianelli U, Patriarca C, Moro A, et al. Lymphomas of the bone: a pathological and clinical study of 54 cases. Int J Surg Pathol 2002;10(4):257–66. doi: 1177/106689690201000403.

  70. Zinzani PL, Carrillo G, Ascani S, et al. Primary bone lymphoma: experience with 52 patients. Haematologica. 2003;88(3):280–5.

  71. Bayrakci K, Yildiz Y, Saglik Y, et al. Primary lymphoma of bones. Int Orthop. 2001;25(2):123–6. doi: 10.1007/s002640100224.

  72. Horsman JM, Thomas J, Hough R, Hancock BW. Primary bone lymphoma: a retrospective analysis. Int J Oncol. 2006;28(6):1571–5. doi: 10.3892/ijo.28.6.1571.

  73. Catlett JP, Williams SA, O’Connor SC, et al. Primary lymphoma of bone: an institutional experience. Leuk 2008;49(11):2125–32. doi: 10.1080/10428190802404030.

  74. Heyning FH, Hogenndoorn PC, Kramer MH, et al. Primary lymphoma of bone: extranodal lymphoma with favourable survival independent of germinal centre, post-germinal centre or indeterminate phenotype. J Clin Pathol. 2009;62(9):820–4. doi: 10.1136/jcp.2008.063156.

  75. Jawad MU, Schneiderbauer MM, Min ES, et al. Primary Lymphoma of Bone in Adult Patients. Cancer. 2010;116(4):871–9. doi: 10.1002/cncr.24828.

  76. Nasiri MR, Varshoee F, Mohtashami S, et al. Primary bone lymphoma: a clinicopathological retrospective study of 28 patients in a single institution. J Res Med Sci. 2011;16(6):814–20.

  77. Christie DR, Dear K, Le T, et al. Limited chemotherapy and shrinking field radiotherapy for Osteolymphoma (primary bone lymphoma): results from the trans-Tasman Radiation Oncology Group 99.04 and Australasian Leukaemia and Lymphoma Group LY02 prospective trial. Int J Radiat Oncol Biol Phys. 2011;80(4):1164–70. doi: 10.1016/j.ijrobp.2010.03.036.

  78. Cai L, Stauder MC, Zhang YJ, et al. Early-stage primary bone lymphoma: a retrospective, multicenter rare cancer network (RCN) study. Int J Radiat Oncol Biol Phys. 2012;83(1):284–91. doi: 10.1016/j.ijrobp.2011.06.1976.

  79. Ventre BM, Ferreri AJM, Gospodarowicz M, et al. Clinical features, management, and prognosis of an international series of 161 patients with limited-stage diffuse large B-cell lymphoma of the bone (the IELSG-14 study). Oncologist. 2014;19(3):291–8. doi: 10.1634/theoncologist.2013-0249.

  80. Jamshidi K, Jabalameli MD, Hoseini MG, et al. Stage IE Primary Bone Lymphoma: Limb Salvage for Local Recurrence. Arch Bone Jt Surg. 2015;3(1):39–44.

  81. Ayed BC, Laabidi S, Said N, et al. Primary bone lymphoma: tunisian multicentric retrospective study about 32 cases. Tunis Med. 2018;96(5):269–72.