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

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.

• Anna Konstantinovna Smol’yaninova National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
• N.G. Gabeeva National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
• V.E. Mamonov National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
• S.A. Tatarnikova National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
• L.G. Gorenkova National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
• D.S. Badmadzhapova National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
• A.M. Kovrigina National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
• E.G. Gemdzhian National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
• E.E. Zvonkov National Medical Hematology Research Center, 4a Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «НМИЦ гематологии» Минздрава России, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167

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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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.
9. [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)]
10. 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.
11. [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)]
12. 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.
13. [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)]
14. 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.
15. [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)]
16. 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.
17. [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)]
18. 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.
19. [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)]
20. 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. DOI: https://doi.org/10.3816/CLM.2005.n.041
21. 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. DOI: https://doi.org/10.1200/JCO.1999.17.4.1244
22. 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. DOI: https://doi.org/10.1200/JCO.2005.01.891
23. 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. DOI: https://doi.org/10.1200/JCO.2006.09.2403
24. 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. DOI: https://doi.org/10.1200/JCO.2006.08.2305
25. 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).
26. 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. DOI: https://doi.org/10.1182/blood-2003-05-1545
27. 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. DOI: https://doi.org/10.1111/bjh.12714
28. Reddy N, Greer JP. Primary bone lymphoma: a set of unique problems in management. Leuk 2009;51(1):1–2. doi: 10.3109/10428190903470877. DOI: https://doi.org/10.3109/10428190903470877
29. 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. DOI: https://doi.org/10.1002/1097-0142(19940215)73:4<1194::AID-CNCR2820730412>3.0.CO;2-R
30. 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. DOI: https://doi.org/10.1080/1120009X.1991.11739091
31. 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. DOI: https://doi.org/10.1093/ajcp/111.2.171
32. Limb D, Dreghorn C, Murphy JK, Mannion R. Primary lymphoma of bone. Int Orthop. 1994;18(3):180–3. doi: 10.1007/bf00192476. DOI: https://doi.org/10.1007/BF00192476
33. 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. DOI: https://doi.org/10.1093/annonc/mdt482
34. 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. DOI: https://doi.org/10.1080/10428194.2016.1177180
35. 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. DOI: https://doi.org/10.1111/j.1445-5994.1999.tb00686.x
36. 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. DOI: https://doi.org/10.1200/JCO.2006.05.9212
37. 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. DOI: https://doi.org/10.1002/1097-0142(1971)28:5<1234::AID-CNCR2820280522>3.0.CO;2-L
38. 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. DOI: https://doi.org/10.1159/000375437
39. 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. DOI: https://doi.org/10.1016/j.ijrobp.2015.01.014
40. 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. DOI: https://doi.org/10.1093/annonc/mdh089
41. 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. DOI: https://doi.org/10.1007/s004310000711
42. 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. DOI: https://doi.org/10.1002/1097-0142(19830101)51:1<44::AID-CNCR2820510111>3.0.CO;2-D
43. 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. DOI: https://doi.org/10.2214/ajr.164.1.7998525
44. 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. DOI: https://doi.org/10.1056/NEJM196806132782407
45. 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. DOI: https://doi.org/10.1016/j.jbo.2014.11.002
46. 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. DOI: https://doi.org/10.1590/1413-785220182602185549
47. 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. DOI: https://doi.org/10.1111/bjh.12841
48. 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. DOI: https://doi.org/10.1038/srep28834
49. 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. DOI: https://doi.org/10.3109/10428190903308007
50. 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. DOI: https://doi.org/10.5045/kjh.2012.47.3.213
51. 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. DOI: https://doi.org/10.1200/JCO.2012.48.0467
52. 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.
53. 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. DOI: https://doi.org/10.1016/j.ijrobp.2003.11.020
54. 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. DOI: https://doi.org/10.1016/0360-3016(94)90059-0
55. 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. DOI: https://doi.org/10.1097/00003086-200212000-00028
56. 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. DOI: https://doi.org/10.7326/0003-4819-87-1-50
57. 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. DOI: https://doi.org/10.4103/0973-1482.73366
58. Coley BL, Higinbotham NL, Groesbeck HP. Primary reliculum-cell sarcoma of bone. Radiology. 1950;55(5):641–58. doi: 10.1148/55.5.641. DOI: https://doi.org/10.1148/55.5.641
59. Francis KC, Higinbotham NL, Coley BL. Primary reticulum cell sarcoma of bone; report of 44 cases. Surg Gynecol Obstet. 1954;99(2):142–6.
60. 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. DOI: https://doi.org/10.1182/blood.V122.21.3059.3059
61. 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.
62. [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)]
63. 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. DOI: https://doi.org/10.3109/10428194.2013.802784
64. 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. DOI: https://doi.org/10.4103/wjnm.WJNM_42_17
65. 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. DOI: https://doi.org/10.1200/JCO.2013.54.8800
66. Reddy N, Greer JP. Primary bone lymphoma: a set of unique problems in management. Leuk 2009;51(1):1–2. doi: 10.3109/10428190903470877. DOI: https://doi.org/10.3109/10428190903470877
67. 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. DOI: https://doi.org/10.1002/pbc.24523
68. 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. DOI: https://doi.org/10.3109/07357909809032885
69. 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. DOI: https://doi.org/10.1016/j.ctrv.2015.02.001
70. 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. DOI: https://doi.org/10.1111/j.1349-7006.2011.02139.x
71. 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. DOI: https://doi.org/10.1002/hon.2081
72. 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. DOI: https://doi.org/10.1111/j.1365-2141.2012.09247.x
73. 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. DOI: https://doi.org/10.1002/1097-0142(19820901)50:5<1009::AID-CNCR2820500532>3.0.CO;2-0
74. 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. DOI: https://doi.org/10.1038/bjc.1992.322
75. 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. DOI: https://doi.org/10.1016/S0360-3016(97)00106-5
76. 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. DOI: https://doi.org/10.1177/106689690201000403
77. Zinzani PL, Carrillo G, Ascani S, et al. Primary bone lymphoma: experience with 52 patients. Haematologica. 2003;88(3):280–5.
78. Bayrakci K, Yildiz Y, Saglik Y, et al. Primary lymphoma of bones. Int Orthop. 2001;25(2):123–6. doi: 10.1007/s002640100224. DOI: https://doi.org/10.1007/s002640100224
79. 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. DOI: https://doi.org/10.3892/ijo.28.6.1571
80. 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. DOI: https://doi.org/10.1080/10428190802404030
81. 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. DOI: https://doi.org/10.1136/jcp.2008.063156
82. 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. DOI: https://doi.org/10.1002/cncr.24828
83. 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.
84. 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. DOI: https://doi.org/10.1016/j.ijrobp.2010.03.036
85. 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. DOI: https://doi.org/10.1016/j.ijrobp.2011.06.1976
86. 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. DOI: https://doi.org/10.1634/theoncologist.2013-0249
87. 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.
88. 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.