Annals of Hematology

, Volume 96, Issue 11, pp 1873–1881 | Cite as

Clinical outcomes in patients with diffuse large B cell lymphoma with a partial response to first-line R-CHOP chemotherapy: prognostic value of secondary International Prognostic Index scores and Deauville scores

  • Hyewon Lee
  • Yu Ri Kim
  • Soo-Jeong Kim
  • Yong Park
  • Hyeon-Seok Eom
  • Sung Yong Oh
  • Hyo Jung Kim
  • Hye Jin Kang
  • Won-Sik Lee
  • Joon Ho Moon
  • Young-Woong Won
  • Tae-Sung Kim
  • Jin Seok KimEmail author
Original Article


After introducing a rituximab-containing chemoimmunotherapy (R-CHOP) for diffuse large B cell lymphoma (DLBCL), a partial response (PR) which is regarded as treatment failure is still observed. To investigate the prognostic factors for the DLBCL patients with a PR to R-CHOP, we retrospectively evaluated 758 newly diagnosed DLBCL patients. After R-CHOP, 88 (11.6%) achieved a PR. Three-year progression-free and overall survival rates measured from the date of PR achievement (PFS2 and OS2) were 57.4 and 67.8%, respectively. The secondary International Prognostic Index (IPI2) scores after R-CHOP were low (0–1) in 68.2% and high (2–3) in 31.8% of the patients. The Deauville scores from 18-fluorodeoxyglucose positron emission tomography after R-CHOP showed low (2–3) in 58.0% and high (4) in 42.0% of the patients. High IPI2 and high Deauville scores were associated with worse PFS2 (P < 0.001 and P = 0.009) and OS2 (P = 0.013 and P = 0.067). The high-risk group defined by the IPI2 and Deauville scores, whose scores were both high, showed significantly lower 3-year PFS2 (P < 0.001) and OS2 (P = 0.006) rates compared with those of the other groups. In multivariate analyses, the IPI score of ≥ 3 at diagnosis and bone marrow involvement at diagnosis were independent prognostic factors. In addition, high IPI2-Deauville score after R-CHOP was significantly associated with poor PFS2 (P = 0.009) and demonstrated a trend toward inferior OS2. In conclusion, DLBCL patients who partially responded to R-CHOP are still a heterogeneous group, for which IPI2 and Deauville scores should be evaluated for prediction of prognosis.


Diffuse large B cell lymphoma Partial response International Prognostic Index FDG-PET Deauville scores 



This study was accepted and presented in the form of a poster presentation at the 58th annual meeting of the American Society of Hematology, San Diego, CA, December 3–6, 2016.

Compliance with ethical standards

Financial disclosure

The authors do not have any disclosures.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Swerdlow SHCE, Harris NL (2008) WHO classification of tumours of haematopoietic and lymphoid tissues, 4th edn. International Agency for Research on Cancer, LyonGoogle Scholar
  2. 2.
    Park HJ, Park EH, Jung KW, Kong HJ, Won YJ, Lee JY, Yoon JH, Park BK, Lee H, Eom HS, Park S (2012) Statistics of hematologic malignancies in Korea: incidence, prevalence and survival rates from 1999 to 2008. Korean J Hematol 47:28–38CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Lenz G, Wright GW, Emre NC, Kohlhammer H, Dave SS, Davis RE, Carty S, Lam LT, Shaffer AL, Xiao W, Powell J, Rosenwald A, Ott G, Muller-Hermelink HK, Gascoyne RD, Connors JM, Campo E, Jaffe ES, Delabie J, Smeland EB, Rimsza LM, Fisher RI, Weisenburger DD, Chan WC, Staudt LM (2008) Molecular subtypes of diffuse large B-cell lymphoma arise by distinct genetic pathways. Proc Natl Acad Sci U S A 105:13520–13525CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, Powell JI, Yang L, Marti GE, Moore T, Hudson J Jr, Lu L, Lewis DB, Tibshirani R, Sherlock G, Chan WC, Greiner TC, Weisenburger DD, Armitage JO, Warnke R, Levy R, Wilson W, Grever MR, Byrd JC, Botstein D, Brown PO, Staudt LM (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403:503–511CrossRefPubMedGoogle Scholar
  5. 5.
    (1993) A predictive model for aggressive non-Hodgkin’s lymphoma. The International Non-Hodgkin’s Lymphoma Prognostic Factors Project. N Engl J Med 329:987–994Google Scholar
  6. 6.
    Pfreundschuh M, Trumper L, Osterborg A, Pettengell R, Trneny M, Imrie K, Ma D, Gill D, Walewski J, Zinzani PL, Stahel R, Kvaloy S, Shpilberg O, Jaeger U, Hansen M, Lehtinen T, Lopez-Guillermo A, Corrado C, Scheliga A, Milpied N, Mendila M, Rashford M, Kuhnt E, Loeffler M (2006) CHOP-like chemotherapy plus rituximab versus CHOP-like chemotherapy alone in young patients with good-prognosis diffuse large-B-cell lymphoma: a randomised controlled trial by the MabThera International Trial (MInT) Group. Lancet Oncol 7:379–391CrossRefPubMedGoogle Scholar
  7. 7.
    Feugier P, Van Hoof A, Sebban C, Solal-Celigny P, Bouabdallah R, Ferme C, Christian B, Lepage E, Tilly H, Morschhauser F, Gaulard P, Salles G, Bosly A, Gisselbrecht C, Reyes F, Coiffier B (2005) Long-term results of the R-CHOP study in the treatment of elderly patients with diffuse large B-cell lymphoma: a study by the Groupe d’Etude des Lymphomes de l’Adulte. J Clin Oncol 23:4117–4126CrossRefPubMedGoogle Scholar
  8. 8.
    Coiffier B, Thieblemont C, Van Den Neste E, Lepeu G, Plantier I, Castaigne S, Lefort S, Marit G, Macro M, Sebban C, Belhadj K, Bordessoule D, Ferme C, Tilly H (2010) Long-term outcome of patients in the LNH-98.5 trial, the first randomized study comparing rituximab-CHOP to standard CHOP chemotherapy in DLBCL patients: a study by the Groupe d’Etudes des Lymphomes de l’Adulte. Blood 116:2040–2045CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Coiffier B, Lepage E, Briere J, Herbrecht R, Tilly H, Bouabdallah R, Morel P, Van Den Neste E, Salles G, Gaulard P, Reyes F, Lederlin P, Gisselbrecht C (2002) CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. N Engl J Med 346:235–242CrossRefPubMedGoogle Scholar
  10. 10.
    Kwak JY (2012) Treatment of diffuse large B cell lymphoma. Korean J Intern Med 27:369–377CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    National Comprehensive Cancer Network. Non-Hodgkin’s lymphomas (version 3.2016). Accessed October 24, 2016
  12. 12.
    Villela L, Lopez-Guillermo A, Montoto S, Rives S, Bosch F, Perales M, Ferrer A, Esteve J, Colomo L, Campo E, Montserrat E (2001) Prognostic features and outcome in patients with diffuse large B-cell lymphoma who do not achieve a complete response to first-line regimens. Cancer 91:1557–1562CrossRefPubMedGoogle Scholar
  13. 13.
    Cunningham D, Hawkes EA, Jack A, Qian W, Smith P, Mouncey P, Pocock C, Ardeshna KM, Radford JA, McMillan A, Davies J, Turner D, Kruger A, Johnson P, Gambell J, Linch D (2013) Rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisolone in patients with newly diagnosed diffuse large B-cell non-Hodgkin lymphoma: a phase 3 comparison of dose intensification with 14-day versus 21-day cycles. Lancet 381:1817–1826CrossRefPubMedGoogle Scholar
  14. 14.
    Cheson BD, Pfistner B, Juweid ME, Gascoyne RD, Specht L, Horning SJ, Coiffier B, Fisher RI, Hagenbeek A, Zucca E, Rosen ST, Stroobants S, Lister TA, Hoppe RT, Dreyling M, Tobinai K, Vose JM, Connors JM, Federico M, Diehl V (2007) Revised response criteria for malignant lymphoma. J Clin Oncol 25:579–586CrossRefPubMedGoogle Scholar
  15. 15.
    Cheson BD (2007) The International Harmonization Project for response criteria in lymphoma clinical trials. Hematol Oncol Clin North Am 21:841–854CrossRefPubMedGoogle Scholar
  16. 16.
    Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Zucca E, Lister TA (2014) Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol 32:3059–3068CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Itti E, Meignan M, Berriolo-Riedinger A, Biggi A, Cashen AF, Vera P, Tilly H, Siegel BA, Gallamini A, Casasnovas RO, Haioun C (2013) An international confirmatory study of the prognostic value of early PET/CT in diffuse large B-cell lymphoma: comparison between Deauville criteria and DeltaSUVmax. Eur J Nucl Med Mol Imaging 40:1312–1320CrossRefPubMedGoogle Scholar
  18. 18.
    Barrington SF, Mikhaeel NG, Kostakoglu L, Meignan M, Hutchings M, Mueller SP, Schwartz LH, Zucca E, Fisher RI, Trotman J, Hoekstra OS, Hicks RJ, O'Doherty MJ, Hustinx R, Biggi A, Cheson BD (2014) Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol 32:3048–3058CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Lister TA, Crowther D, Sutcliffe SB, Glatstein E, Canellos GP, Young RC, Rosenberg SA, Coltman CA, Tubiana M (1989) Report of a committee convened to discuss the evaluation and staging of patients with Hodgkin’s disease: Cotswolds meeting. J Clin Oncol 7:1630–1636CrossRefPubMedGoogle Scholar
  20. 20.
    Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, Pan Z, Farinha P, Smith LM, Falini B, Banham AH, Rosenwald A, Staudt LM, Connors JM, Armitage JO, Chan WC (2004) Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood 103:275–282CrossRefPubMedGoogle Scholar
  21. 21.
    Meignan M, Gallamini A, Haioun C, Polliack A (2010) Report on the Second International Workshop on interim positron emission tomography in lymphoma held in Menton, France, 8–9 April 2010. Leuk Lymphoma 51:2171–2180CrossRefPubMedGoogle Scholar
  22. 22.
    Meignan M, Gallamini A, Haioun C (2009) Report on the first international workshop on interim-PET scan in lymphoma. Leuk Lymphoma 50:1257–1260CrossRefPubMedGoogle Scholar
  23. 23.
    Sauter CS, Matasar MJ, Meikle J, Schoder H, Ulaner GA, Migliacci JC, Hilden P, Devlin SM, Zelenetz AD, Moskowitz CH (2015) Prognostic value of FDG-PET prior to autologous stem cell transplantation for relapsed and refractory diffuse large B-cell lymphoma. BloodGoogle Scholar
  24. 24.
    Hung MH, Yu YB, Huang YC, Liu HT, Hong YC, Hsiao LT, Liu JH, Gau JP, Chiou TJ, Chen PM, Tzeng CH, Liu CY (2012) Patients with diffuse large B cell lymphoma in partial response or stable disease after first-line R-CHOP: the prognostic value of the absolute lymphocyte count and impact of autologous stem cell transplantation. Ann Hematol 91:1907–1915CrossRefPubMedGoogle Scholar
  25. 25.
    Rovira J, Valera A, Colomo L, Setoain X, Rodriguez S, Martinez-Trillos A, Gine E, Dlouhy I, Magnano L, Gaya A, Martinez D, Martinez A, Campo E, Lopez-Guillermo A (2015) Prognosis of patients with diffuse large B cell lymphoma not reaching complete response or relapsing after frontline chemotherapy or immunochemotherapy. Ann Hematol 94:803–812CrossRefPubMedGoogle Scholar
  26. 26.
    Yoo C, Lee DH, Kim JE, Jo J, Yoon DH, Sohn BS, Kim SW, Lee JS, Suh C (2011) Limited role of interim PET/CT in patients with diffuse large B-cell lymphoma treated with R-CHOP. Ann Hematol 90:797–802CrossRefPubMedGoogle Scholar
  27. 27.
    Han HS, Escalon MP, Hsiao B, Serafini A, Lossos IS (2009) High incidence of false-positive PET scans in patients with aggressive non-Hodgkin’s lymphoma treated with rituximab-containing regimens. Ann Oncol 20:309–318CrossRefPubMedGoogle Scholar
  28. 28.
    Philip T, Hartmann O, Biron P, Cahn JY, Pein F, Bordigoni P, Souillet G, Gartner M, Lasset C, Chauvin F (1988) High-dose therapy and autologous bone marrow transplantation in partial remission after first-line induction therapy for diffuse non-Hodgkin’s lymphoma. J Clin Oncol 6:1118–1124CrossRefPubMedGoogle Scholar
  29. 29.
    Philip T, Guglielmi C, Hagenbeek A, Somers R, Van der Lelie H, Bron D, Sonneveld P, Gisselbrecht C, Cahn JY, Harousseau JL et al (1995) Autologous bone marrow transplantation as compared with salvage chemotherapy in relapses of chemotherapy-sensitive non-Hodgkin’s lymphoma. N Engl J Med 333:1540–1545CrossRefPubMedGoogle Scholar
  30. 30.
    Gisselbrecht C, Glass B, Mounier N, Singh Gill D, Linch DC, Trneny M, Bosly A, Ketterer N, Shpilberg O, Hagberg H, Ma D, Briere J, Moskowitz CH, Schmitz N (2010) Salvage regimens with autologous transplantation for relapsed large B-cell lymphoma in the rituximab era. J Clin Oncol 28:4184–4190CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Stiff PJ, Unger JM, Cook JR, Constine LS, Couban S, Stewart DA, Shea TC, Porcu P, Winter JN, Kahl BS, Miller TP, Tubbs RR, Marcellus D, Friedberg JW, Barton KP, Mills GM, LeBlanc M, Rimsza LM, Forman SJ, Fisher RI (2013) Autologous transplantation as consolidation for aggressive non-Hodgkin’s lymphoma. N Engl J Med 369:1681–1690CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Hyewon Lee
    • 1
  • Yu Ri Kim
    • 2
  • Soo-Jeong Kim
    • 3
  • Yong Park
    • 4
  • Hyeon-Seok Eom
    • 1
  • Sung Yong Oh
    • 5
  • Hyo Jung Kim
    • 6
  • Hye Jin Kang
    • 7
  • Won-Sik Lee
    • 8
  • Joon Ho Moon
    • 9
  • Young-Woong Won
    • 10
  • Tae-Sung Kim
    • 11
  • Jin Seok Kim
    • 3
    Email author
  1. 1.Center for Hematologic MalignancyNational Cancer CenterGoyangSouth Korea
  2. 2.Department of Internal MedicineYonsei University College of Medicine, Gangnam Severance HospitalSeoulSouth Korea
  3. 3.Division of Hematology, Department of Internal MedicineYonsei University College of Medicine, Severance HospitalSeoulSouth Korea
  4. 4.Division of Hematology-Oncology, Department of Internal MedicineKorea University College of MedicineSeoulSouth Korea
  5. 5.Department of Internal MedicineDong-A University College of MedicineBusanSouth Korea
  6. 6.Division of Hematology-Oncology, Department of Internal Medicine, College of MedicineHallym University, Hallym University Sacred Heart HospitalAnyangSouth Korea
  7. 7.Division of Hematology-Oncology, Department of Internal Medicine, Korea Cancer Center HospitalKorea Institute of Radiological and Medical SciencesSeoulSouth Korea
  8. 8.Division of Hematology-Oncology, Department of Internal Medicine, Busan Paik HospitalInje University College of MedicineBusanSouth Korea
  9. 9.Department of Hematology and Medical OncologyKyungpook National University HospitalDaeguSouth Korea
  10. 10.Department of Internal MedicineHanyang University College of MedicineSeoulSouth Korea
  11. 11.Department of Nuclear MedicineNational Cancer CenterGoyangSouth Korea

Personalised recommendations