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Peripheral blood lymphocyte to monocyte ratio identifies high-risk adult patients with sporadic Burkitt lymphoma

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Abstract

Adult sporadic Burkitt lymphoma (BL) is a rare subtype of lymphoma. In this retrospective study, we investigated the prognostic value of pretreatment lymphocyte to monocyte ratio (LMR) in a cohort of 62 patients. Using LMR <2.6 as the optimal cutoff point, 24 patients (38.7 %) had LMR <2.6. The complete response rates in high-LMR group and low-LMR group were 90.9 and 65.0 %, respectively (P = 0.019). At a median follow-up time of 41 months, the 3-year progression-free survival (PFS) rate and overall survival (OS) rates were 76 and 80 %, respectively. In a multivariate Cox regression model, it was found that the presence of bone marrow infiltration and low LMR were independently adverse prognostic factors for both PFS and OS. In the whole group, the addition of rituximab to treatment did not benefit patients significantly in PFS and OS. In subgroup analysis, in patients with high LMR, addition of rituximab can significantly improve survival outcomes (P = 0.046). In conclusion, we firstly found that low LMR (<2.60) was an independently adverse prognostic factor in adult patients with sporadic BL. Intensive chemotherapy could cure the majority of patients in our study, and the pretreatment LMR might predict the value of rituximab in this age population.

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References

  1. Said J, Lones M, Yea S (2014) Burkitt lymphoma and MYC: what else is new? Adv Anat Pathol 21(3):160–165. doi:10.1097/PAP.0b013e3182a92cde

    Article  PubMed  Google Scholar 

  2. Jacobson C, LaCasce A (2014) How I treat Burkitt lymphoma in adults. Blood 124(19):2913–2920. doi:10.1182/blood-2014-06-538504

    Article  CAS  PubMed  Google Scholar 

  3. Wasterlid T, Brown PN, Hagberg O, Hagberg H, Pedersen LM, D’Amore F, Jerkeman M (2013) Impact of chemotherapy regimen and rituximab in adult Burkitt lymphoma: a retrospective population-based study from the Nordic Lymphoma Group. Ann Oncol Off J Eur Soc Med Oncol/ESMO 24(7):1879–1886. doi:10.1093/annonc/mdt058

    Article  CAS  Google Scholar 

  4. Rowe M, Fitzsimmons L, Bell AI (2014) Epstein-Barr virus and Burkitt lymphoma. Chin J Cancer 33(12):609–619. doi:10.5732/cjc.014.10190

    PubMed Central  CAS  PubMed  Google Scholar 

  5. Satou A, Asano N, Nakazawa A, Osumi T, Tsurusawa M, Ishiguro A, Elsayed AA, Nakamura N, Ohshima K, Kinoshita T, Nakamura S (2014) Epstein-Barr virus (EBV)-positive sporadic Burkitt lymphoma: an age-related lymphoproliferative disorder? Am J Surg Pathol. doi:10.1097/PAS.0000000000000332

    Google Scholar 

  6. Todeschini G, Bonifacio M, Tecchio C, Balter R, Carli G, Stefani PM, Adami F, Zamo A, Dei Tos AP, Marino F, Gherlinzoni F, Marradi P, Semenzato G, Pizzolo G (2012) Intensive short-term chemotherapy regimen induces high remission rate (over 90 %) and event-free survival both in children and adult patients with advanced sporadic Burkitt lymphoma/leukemia. Am J Hematol 87(1):22–25. doi:10.1002/ajh.22189

    Article  PubMed  Google Scholar 

  7. Dunleavy K, Pittaluga S, Shovlin M, Steinberg SM, Cole D, Grant C, Widemann B, Staudt LM, Jaffe ES, Little RF, Wilson WH (2013) Low-intensity therapy in adults with Burkitt’s lymphoma. N Engl J Med 369(20):1915–1925. doi:10.1056/NEJMoa1308392

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Mead GM, Barrans SL, Qian W, Walewski J, Radford JA, Wolf M, Clawson SM, Stenning SP, Yule CL, Jack AS, Group UKNCRILCS, Australasian L, Lymphoma G (2008) A prospective clinicopathologic study of dose-modified CODOX-M/IVAC in patients with sporadic Burkitt lymphoma defined using cytogenetic and immunophenotypic criteria (MRC/NCRI LY10 trial). Blood 112(6):2248–2260. doi:10.1182/blood-2008-03-145128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Moleti ML, Testi AM, Giona F, Malandruccolo L, Pescarmona E, Martino P, Paoloni F, Barberi W, Palumbo G, Mandelli F, Foa R (2007) CODOX-M/IVAC (NCI 89-C-41) in children and adolescents with Burkitt’s leukemia/lymphoma and large B-cell lymphomas: a 15 year monocentric experience. Leuk Lymphoma 48(3):551–559. doi:10.1080/10428190601078944

    Article  CAS  PubMed  Google Scholar 

  10. Barnes JA, Lacasce AS, Feng Y, Toomey CE, Neuberg D, Michaelson JS, Hochberg EP, Abramson JS (2011) Evaluation of the addition of rituximab to CODOX-M/IVAC for Burkitt’s lymphoma: a retrospective analysis. Ann Oncol Off J Soc Med Oncol/ESMO 22(8):1859–1864. doi:10.1093/annonc/mdq677

    Article  CAS  Google Scholar 

  11. Mohamedbhai SG, Sibson K, Marafioti T, Kayani I, Lowry L, Goldstone AH, Linch DC, Ardeshna KM (2011) Rituximab in combination with CODOX-M/IVAC: a retrospective analysis of 23 cases of non-HIV related B-cell non-Hodgkin lymphoma with proliferation index >95 %. Br J Haematol 152(2):175–181. doi:10.1111/j.1365-2141.2010.08447.x

    Article  CAS  PubMed  Google Scholar 

  12. Wildes TM, Farrington L, Yeung C, Harrington AM, Foyil KV, Liu J, Kreisel F, Bartlett NL, Fenske TS (2014) Rituximab is associated with improved survival in Burkitt lymphoma: a retrospective analysis from two US academic medical centers. Ther Adv Hematol 5(1):3–12. doi:10.1177/2040620713514682

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Hoelzer D, Walewski J, Dohner H, Viardot A, Hiddemann W, Spiekermann K, Serve H, Duhrsen U, Huttmann A, Thiel E, Dengler J, Kneba M, Schaich M, Schmidt-Wolf IG, Beck J, Hertenstein B, Reichle A, Domanska-Czyz K, Fietkau R, Horst HA, Rieder H, Schwartz S, Burmeister T, Gokbuget N, German Multicenter Study Group for Adult Acute Lymphoblastic L (2014) Improved outcome of adult Burkitt lymphoma/leukemia with rituximab and chemotherapy: report of a large prospective multicenter trial. Blood 124(26):3870–3879. doi:10.1182/blood-2014-03-563627

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Intermesoli T, Rambaldi A, Rossi G, Delaini F, Romani C, Pogliani EM, Pagani C, Angelucci E, Terruzzi E, Levis A, Cassibba V, Mattei D, Gianfaldoni G, Scattolin AM, Di Bona E, Oldani E, Parolini M, Gokbuget N, Bassan R (2013) High cure rates in Burkitt lymphoma and leukemia: a Northern Italy Leukemia Group study of the German short intensive rituximab-chemotherapy program. Haematologica 98(11):1718–1725. doi:10.3324/haematol.2013.086827

    Article  PubMed Central  PubMed  Google Scholar 

  15. Anoceto Martinez A, Gonzalez Otero A, De Svarch Guerchicoff E, Arencibia Nunez A, Jaime JC, Dorticos E, Sarduy S, Gonzalez L (2012) Absolute lymphocyte count as a prognostic factor in children with acute lymphoblastic leukemia. An Pediatr 76(1):10 e11–16. doi:10.1016/j.anpedi.2011.07.001

    Google Scholar 

  16. Feng J, Wang Z, Guo X, Chen Y, Cheng Y, Tang Y (2012) Prognostic significance of absolute lymphocyte count at diagnosis of diffuse large B-cell lymphoma: a meta-analysis. Int J Hematol 95(2):143–148. doi:10.1007/s12185-011-0993-6

    Article  PubMed  Google Scholar 

  17. Hu P, Shen H, Wang G, Zhang P, Liu Q, Du J (2014) Prognostic significance of systemic inflammation-based lymphocyte- monocyte ratio in patients with lung cancer: based on a large cohort study. PLoS One 9(9), e108062. doi:10.1371/journal.pone.0108062

    Article  PubMed Central  PubMed  Google Scholar 

  18. Li J, Jiang R, Liu WS, Liu Q, Xu M, Feng QS, Chen LZ, Bei JX, Chen MY, Zeng YX (2013) A large cohort study reveals the association of elevated peripheral blood lymphocyte-to-monocyte ratio with favorable prognosis in nasopharyngeal carcinoma. PLoS One 8(12), e83069. doi:10.1371/journal.pone.0083069

    Article  PubMed Central  PubMed  Google Scholar 

  19. Milne K, Alexander C, Webb JR, Sun W, Dillon K, Kalloger SE, Gilks CB, Clarke B, Kobel M, Nelson BH (2012) Absolute lymphocyte count is associated with survival in ovarian cancer independent of tumor-infiltrating lymphocytes. J Transl Med 10:33. doi:10.1186/1479-5876-10-33

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Porrata LF, Ristow K, Habermann TM, Ozsan N, Dogan A, Macon W, Colgan JP, Witzig TE, Inwards DJ, Ansell SM, Micallef IN, Johnston PB, Nowakowski GS, Thompson C, Markovic SN (2012) Absolute monocyte/lymphocyte count prognostic score is independent of immunohistochemically determined cell of origin in predicting survival in diffuse large B-cell lymphoma. Leuk Lymphoma 53(11):2159–2165. doi:10.3109/10428194.2012.690605

    Article  PubMed  Google Scholar 

  21. Li YL, Pan YY, Jiao Y, Ning J, Fan YG, Zhai ZM (2014) Peripheral blood lymphocyte/monocyte ratio predicts outcome for patients with diffuse large B cell lymphoma after standard first-line regimens. Ann Hematol 93(4):617–626. doi:10.1007/s00277-013-1916-9

    Article  CAS  PubMed  Google Scholar 

  22. Huang JJ, Jiang WQ, Lin TY, Huang Y, Xu RH, Huang HQ, Li ZM (2011) Absolute lymphocyte count is a novel prognostic indicator in extranodal natural killer/T-cell lymphoma, nasal type. Ann Oncol Off J Eur Soc Med Oncol/ESMO 22(1):149–155. doi:10.1093/annonc/mdq314

    Article  CAS  Google Scholar 

  23. Nitta H, Terui Y, Yokoyama M, Mishima Y, Nishimura N, Ueda K, Kusano Y, Tsuyama N, Takeuchi K, Kanda Y, Hatake K (2015) Absolute peripheral monocyte count at diagnosis predicts central nervous system relapse in diffuse large B-cell lymphoma. Haematologica 100(1):87–90. doi:10.3324/haematol.2014.114934

    Article  PubMed Central  PubMed  Google Scholar 

  24. Porrata LF, Ristow KM, Habermann TM, Witzig TE, Colgan JP, Inwards DJ, Ansell SM, Micallef IN, Johnston PB, Nowakowski G, Thompson CA, Markovic SN (2014) Peripheral blood absolute lymphocyte/monocyte ratio during rituximab, cyclophosphamide, doxorubicin, vincristine and prednisone treatment cycles predicts clinical outcomes in diffuse large B-cell lymphoma. Leuk Lymphoma 55(12):2728–2738. doi:10.3109/10428194.2014.893313

    Article  CAS  PubMed  Google Scholar 

  25. Huang JJ, Li YJ, Xia Y, Wang Y, Wei WX, Zhu YJ, Lin TY, Huang HQ, Jiang WQ, Li ZM (2013) Prognostic significance of peripheral monocyte count in patients with extranodal natural killer/T-cell lymphoma. BMC Cancer 13:222. doi:10.1186/1471-2407-13-222

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Porrata LF, Ristow KM, Habermann TM, Macon WR, Witzig TE, Colgan JP, Inwards DJ, Ansell SM, Micallef IN, Johnston PB, Nowakowski G, Thompson CA, Markovic SN (2013) Peripheral blood absolute lymphocyte/monocyte ratio recovery during ABVD treatment cycles predicts clinical outcomes in classical Hodgkin lymphoma. Blood Cancer J 3, e110. doi:10.1038/bcj.2013.8

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Leoncini L, Raphael M, Stein H, Harris NL, Jaffe ES, Kluin PM (2008) Burkitt lymphoma. In: Swerdlow SH, Campo E, Harris NL et al (eds) WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon, France: IARC., pp 262–264

    Google Scholar 

  28. Juweid ME, Stroobants S, Hoekstra OS, Mottaghy FM, Dietlein M, Guermazi A, Wiseman GA, Kostakoglu L, Scheidhauer K, Buck A, Naumann R, Spaepen K, Hicks RJ, Weber WA, Reske SN, Schwaiger M, Schwartz LH, Zijlstra JM, Siegel BA, Cheson BD, Imaging Subcommittee of International Harmonization Project in L (2007) Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol Off J Am Soc Clin Oncol 25(5):571–578. doi:10.1200/JCO.2006.08.2305

    Article  Google Scholar 

  29. Cheson BD, Horning SJ, Coiffier B, Shipp MA, Fisher RI, Connors JM, Lister TA, Vose J, Grillo-Lopez A, Hagenbeek A, Cabanillas F, Klippensten D, Hiddemann W, Castellino R, Harris NL, Armitage JO, Carter W, Hoppe R, Canellos GP (1999) Report of an international workshop to standardize response criteria for non-Hodgkin’s lymphomas. NCI Sponsored International Working Group. J Clin Oncol Off J Am Soc Clin Oncol 17(4):1244

    CAS  Google Scholar 

  30. Mead GM, Sydes MR, Walewski J, Grigg A, Hatton CS, Pescosta N, Guarnaccia C, Lewis MS, McKendrick J, Stenning SP, Wright D, Collaborators UL (2002) 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 Off J Eur Soc Med Oncol/ESMO 13(8):1264–1274

    Article  CAS  Google Scholar 

  31. Boerma EG, van Imhoff GW, Appel IM, Veeger NJ, Kluin PM, Kluin-Nelemans JC (2004) Gender and age-related differences in Burkitt lymphoma—epidemiological and clinical data from The Netherlands. Eur J Cancer 40(18):2781–2787. doi:10.1016/j.ejca.2004.09.004

    Article  CAS  PubMed  Google Scholar 

  32. Evens AM, Carson KR, Kolesar J, Nabhan C, Helenowski I, Islam N, Jovanovic B, Barr PM, Caimi PF, Gregory SA, Gordon LI (2013) A multicenter phase II study incorporating high-dose rituximab and liposomal doxorubicin into the CODOX-M/IVAC regimen for untreated Burkitt’s lymphoma. Ann Oncol Off J Eur Soc Med Oncol/ESMO 24(12):3076–3081. doi:10.1093/annonc/mdt414

    Article  CAS  Google Scholar 

  33. Landskron G, De la Fuente M, Thuwajit P, Thuwajit C, Hermoso MA (2014) Chronic inflammation and cytokines in the tumor microenvironment. J Immunol Res 2014:149185. doi:10.1155/2014/149185

    Article  PubMed Central  PubMed  Google Scholar 

  34. Sarraf KM, Belcher E, Raevsky E, Nicholson AG, Goldstraw P, Lim E (2009) Neutrophil/lymphocyte ratio and its association with survival after complete resection in non-small cell lung cancer. J Thorac Cardiovasc Surg 137(2):425–428. doi:10.1016/j.jtcvs.2008.05.046

    Article  PubMed  Google Scholar 

  35. Li ZM, Huang JJ, Xia Y, Sun J, Huang Y, Wang Y, Zhu YJ, Li YJ, Zhao W, Wei WX, Lin TY, Huang HQ, Jiang WQ (2012) Blood lymphocyte-to-monocyte ratio identifies high-risk patients in diffuse large B-cell lymphoma treated with R-CHOP. PLoS One 7(7), e41658. doi:10.1371/journal.pone.0041658

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Thomas DA, Faderl S, O’Brien S, Bueso-Ramos C, Cortes J, Garcia-Manero G, Giles FJ, Verstovsek S, Wierda WG, Pierce SA, Shan J, Brandt M, Hagemeister FB, Keating MJ, Cabanillas F, Kantarjian H (2006) Chemoimmunotherapy with hyper-CVAD plus rituximab for the treatment of adult Burkitt and Burkitt-type lymphoma or acute lymphoblastic leukemia. Cancer 106(7):1569–1580. doi:10.1002/cncr.21776

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

Liang Wang received grant support from the National Natural Science Foundation of China (contract/grant number: 81400159), Medical Research Foundation of Guangdong Province (grant number: B2014158), Young Teachers’ Cultivation Project of Sun Yat-sen University (No. 12ykpy54), and Outstanding Young Talents Project of Sun Yat-sen University Cancer Center (No. 04190101#). Yue Lu received grants from the National Natural Science Foundation of China (contract/grant number: 30471976 and 81272620) and Science and Technology Projects of Guangdong Province (contract/grant number: 2010B031600233 and 2010A090200019)

Conflict of interest

The authors declare that they have no conflicts of interest relevant to the manuscript submission.

Author contributions

Y.L. designed this study. L.W. and H.W. collected and analyzed the data and wrote the paper. Z.J.X, H.Q.H, T.Y.L, and W.Q.J. contributed to the cases and performed data analysis. All authors have read the paper and approved it to be published.

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    Authors and Affiliations

    1. State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, 510060, Guangdong, People’s Republic of China

      Liang Wang, Hua Wang, Zhong-Jun Xia, Hui-Qiang Huang, Wen-Qi Jiang, Tong-Yu Lin & Yue Lu

    2. Department of Hematologic Oncology, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Guangzhou, 510060, Guangdong, People’s Republic of China

      Liang Wang, Hua Wang, Zhong-Jun Xia & Yue Lu

    3. Department of Hematologic Oncology, Sun Yat-sen University Cancer Center, Guangzhou, 510060, Guangdong, People’s Republic of China

      Hui-Qiang Huang, Wen-Qi Jiang & Tong-Yu Lin

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    1. Liang Wang
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    Correspondence to Yue Lu.

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    Liang Wang and Hua Wang contributed equally to this work.

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    Wang, L., Wang, H., Xia, ZJ. et al. Peripheral blood lymphocyte to monocyte ratio identifies high-risk adult patients with sporadic Burkitt lymphoma. Ann Hematol 94, 1645–1654 (2015). https://doi.org/10.1007/s00277-015-2427-7

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