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Long-term survey of survival time, histological transformation, and secondary malignancies in Japanese patients with advanced-stage follicular lymphoma in the rituximab era: Hokkaido Hematology Study Group

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Abstract

Following the introduction of rituximab, the long-term overall survival (OS) rate of advanced-stage follicular lymphoma (FL) cases was expected to improve after the introduction of rituximab: however, there is a lack of large-scale survey data in Asia due to the relatively low incidence of FL. We conducted a retrospective survey to assess the treatment outcomes in patients with newly diagnosed advanced-stage FL in 29 institutions in Hokkaido from January 2001 to December 2010. The total number of patients was 443 (men 47.6 %, women 52.4 %), with a median age of 55 years (range 20–80 years). Of the cases examined, 42.2 % had stage III and 57.8 % had stage IV disease. Furthermore, 62.5, 19.7, 9.2, 5.2, and 3.4 % had performance statuses of 0, 1, 2, 3, and 4, respectively. The 5-year OS was 91.2 %, and no survival plateau was observed. Seventeen patients experienced secondary malignancies (six hematological diseases and 11 solid cancers; 5-year probability, 4.2 %). Eighteen patients experienced transformation (5-year probability, 4.5 %). The overall survival at 5 years after therapy for transformation was 50 %. Before the introduction of rituximab, the 5- to 10-year OS of advanced-stage FL patients in Japan was reported to be about 30–60 %. Although these data are limited, improvement in OS has been observed in Japan during the rituximab era.

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References

  1. The non-Hodgkin’s lymphoma Classification Project. A clinical evaluation of International Lymphoma Study Group classification of non-Hodgkin’s lymphoma. Blood. 1997;89:3909–15.

    Google Scholar 

  2. Lymphoma study group of Japanese pathologists. The world health organization classification of malignant lymphomas in japan: incidence of recently recognized eitities. Pathol Int. 2000;50:696–702.

    Article  Google Scholar 

  3. Hiddemann W, Kneba M, Dreyling M, Schmitz N, Lengfelder E, Schmits R, et al. Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group. Blood. 2005;106:3725–32.

    Article  CAS  PubMed  Google Scholar 

  4. Marcus R, Imrie K, Solal-Celigny P, Catalano JV, Dmoszynska A, Raposo JC, et al. Phase III study of R-CVP compared with cyclophosphamide, vincristine, and prednisone alone in patients with previously untreated advanced follicular lymphoma. J Clin Oncol. 2008;26:4579–86.

    Article  CAS  PubMed  Google Scholar 

  5. Swenson WT, Wooldridge JE, Lynch CF, Forman-Hoffman VL, Chrischilles E, Link BK. Improved survival of follicular lymphoma patients in the United States. J Clin Oncol. 2005;23:5019–26.

    Article  PubMed  Google Scholar 

  6. Tobinai K, Ogura M, Itoh K, Kinoshita T, Hotta T, Watanabe T, et al. Randomized phase II study of concurrent and sequential combinations of rituximab plus CHOP chemotherapy in untreated indolent B-cell non-Hodgkin lymphoma: 7-year follow up results. Cancer Sci. 2010;101:2579–85.

    Article  PubMed  Google Scholar 

  7. Watanabe T, Tobinai K, Shibata T, Tsukasaki K, Morishima Y, Maseki N, et al. Phase II/III study of R-CHOP-21 versus R-CHOP-14 for untreated indolent B-cell non-Hodgkin’s lymphoma: JCOG 0203 trial. J Clin Oncol. 2011;29:3990–8.

    Article  PubMed  Google Scholar 

  8. Nagai H, Yano T, Watanabe T, Uike N, Okamura S, Hanada S, et al. Remission induction therapy containing rituximab markedly improved the outcome of untreated mature B cell lymphoma. Br J Haematol. 2008;143:672–80.

    Article  PubMed  Google Scholar 

  9. Basic resident register in Japan. http://www.stat.go.jp/data/idou/2011np/kihon/pdf/gaiyou.pdf.

  10. Torimoto Y, Sato K, Ikuta K, Hayashi T, Hirayama Y, Inamura J, et al. A retrospective clinical analysis of Japanese patients with peripheral T-cell lymphoma not otherwise specified: Hokkaido Hematology Study Group. Int J Hematol. 2013;98(1):71–8.

    Google Scholar 

  11. Kurosawa M, Yonezumi M, Hashino S, Tanaka J, Nishio M. Epidemiology and treatment outcome of invasive fungal infections in patients with hematological malignancies. Int J Hematol. 2012;96:748–57.

    Article  PubMed  Google Scholar 

  12. Onozawa M, Hashino S, Haseyama Y, Hirayama Y, Iizuka S, et al. Incidence and risk of post herpetic neuralgia after varicella zoster virus infection in hematopoietic cell transplantation recipients: Hokkaido Hematology Study Group. Biol Blood Marrow Transplant. 2009;15:724–9.

    Article  PubMed  Google Scholar 

  13. Solal-Céligny P, Roy P, Colombat P, White J, Armitage JO, Arranz-Saez R, et al. Follicular lymphoma international prognostic index. Blood. 2004;104:1258–65.

    Article  PubMed  Google Scholar 

  14. Brice P, Bastion Y, Lepage E, Brousse N, Haïoun C, et al. Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: a randomized study from the Groupe d’Etude des Lymphomes Folliculaires. Groupe d’Etude des Lymphomes de l’Adulte. J Clin Oncol. 1997;15:1110–7.

    CAS  PubMed  Google Scholar 

  15. Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982;5:649–55.

    Article  CAS  PubMed  Google Scholar 

  16. Cheson BD, Horning SJ, Coiffier B, Shipp MA, Fisher RI, NCI Sponsored International Working Group, et al. Report of an international workshop to standardize response criteria for non-Hodgkin’s lymphomas. J Clin Oncol. 1999;17:1244–53.

    CAS  PubMed  Google Scholar 

  17. Keegan TH, McClure LA, Foran JM, Clarke CA. Improvements in survival after follicular lymphoma by race/ethnicity and socioeconomic status: a population-based study. J Clin Oncol. 2009;27:3044–51.

    Article  PubMed Central  PubMed  Google Scholar 

  18. LaCasce AS, Kho ME, Friedberg JW, Niland JC, Abel GA, Rodriguez MA, et al. Comparison of referring and final pathology for patients with non-Hodgkin’s lymphoma in the National Comprehensive Cancer Network. J Clin Oncol. 2008;26:5107–12.

    Article  PubMed Central  PubMed  Google Scholar 

  19. Kahl B. Is there a role for “watch and wait” in follicular lymphoma in the rituximab era? Hematology Am Soc Hematol Educ Progr. 2012;2012:433–8.

    Google Scholar 

  20. Niitsu N, Umeda M. Prognostic factors of follicular lymphoma treated with combination chemotherapy. Jpn J Clin Hematol. 1997;38:496–504.

    CAS  Google Scholar 

  21. Hiroo K. Clinical studies on 53 cases of follicular lymphomas. Tokyo Jikei Med J. 1993;108:11–30.

    Google Scholar 

  22. Toshyyuki T, Kazumi S, Umihiro S, et al. Follicular lymphoma in Japan: retrospective study on natural history and therapeutic results in 50 cases collected from 4 institutions. Jpn J Clin Oncol. 1989;30:2123–8.

    Google Scholar 

  23. Kondo E, Ogura M, Kagami Y, Taji H, Miura K, et al. Assessment of prognostic factors in follicular lymphoma patients. Int J Hematol. 2001;73:363–8.

    Article  CAS  PubMed  Google Scholar 

  24. Katsumata N, Matsuno Y, Nakayama H, Takenaka T, Kobayashi Y. Prognostic factors and a predictive model of follicular lymphoma: a 25-year study at a single institution in Japan. Jpn J Clin Oncol. 1996;26:445–54.

    Article  CAS  PubMed  Google Scholar 

  25. Freedman AS, Neuberg D, Mauch P. Long-term follow up of autologous bone marrow transplantation in patients with relapsed follicular lymphoma. Blood. 1999;94:3325–33.

    CAS  PubMed  Google Scholar 

  26. Ladetto M, De Marco F, Benedetti F, Vitolo U, Patti C, Rambaldi A, et al. Prospective, multicenter randomized GITMO/IIL trial comparing intensive (R-HDS) versus conventional (CHOP-R) chemoimmunotherapy in high-risk follicular lymphoma at diagnosis: the superior disease control of R-HDS does not translate into an overall survival advantage. Blood. 2008;111:4004–13.

    Article  CAS  PubMed  Google Scholar 

  27. Gyan E, Foussard C, Bertrand P, Michenet P, Le Gouill S, Berthou C, et al. High-dose therapy followed by autologous purged stem cell transplantation and doxorubicin-based chemotherapy in patients with advanced follicular lymphoma: a randomized multicenter study by the GOELAMS with final results after a median follow-up of 9 years. Blood. 2009;113:995–1001.

    Article  CAS  PubMed  Google Scholar 

  28. Lenz G, Dreyling M, Schiegnitz E, Forstpointner R, Wandt H, Freund M, et al. Myeloablative radiochemotherapy followed by autologous stem cell transplantation in first remission prolongs progression-free survival in follicular lymphoma: results of a prospective, randomized trial of the German Low-Grade Lymphoma Study Group. Blood. 2004;104:2667–74.

    Article  CAS  PubMed  Google Scholar 

  29. Ogura M. Recent therapeutic progress in non-Hodgkin lymphoma: focusing on diffuse large B-cell lymphoma and follicular lymphoma. Jpn J Clin Hematol. 2008;49:1434–50 (in Japanese).

    Google Scholar 

  30. Hirayama Y, Kohda K, Konuma Y, Hirata Y, Kuroda H, Fujimi Y, et al. Late onset neutropenia and immunoglobulin suppression of the patients with malignant lymphoma following autologous stem cell transplantation with rituximab. Intern Med. 2009;48:57–60.

    Article  PubMed  Google Scholar 

  31. Khouri IF, Saliba RM, Giralt SA, Lee MS, Okoroji GJ, Hagemeister FB, et al. Nonablative allogeneic hematopoietic transplantation as adoptive immunotherapy for indolent lymphoma: low incidence of toxicity, acute graft-versus-host disease, and treatment-related mortality. Blood. 2001;98:3595–9.

    Article  CAS  PubMed  Google Scholar 

  32. Federico M, Bellei M, Marcheselli L, Luminari S, Lopez-Guillermo A, Vitolo U, et al. Follicular lymphoma international prognostic index 2: a new prognostic index for follicular lymphoma developed by the international follicular lymphoma prognostic factor project. J Clin Oncol. 2009;27:4555–62.

    Article  PubMed  Google Scholar 

  33. Al-Tourah AJ, Gill KK, Chhanabhai PJ, Klasa KJ, Sehnkier TN, et al. Population-based analysis of incidence and outcome of transformed non-Hodgkin’s lymphoma. J Clin Oncol. 2008;26:5165–70.

    Article  PubMed  Google Scholar 

  34. Hubbard SM, Chabner BA, DeVita VT Jr, Simon R, Berard CW, Jones RB, et al. Histologic progression in non-Hodgkin’s lymphoma. Blood. 1982;59:258–64.

    CAS  PubMed  Google Scholar 

  35. Yuen AR, Kamel OW, Halpern J, Horning SJ. Long-term survival after histologic transformation of low-grade follicular lymphoma. J Clin Oncol. 1995;13:1726–33.

    CAS  PubMed  Google Scholar 

  36. Link BK, Maurer MJ, Nowakowski GS, Ansell SM, Macon WR. Rates and outcomes of follicular lymphoma transformation in the immunochemotherapy era: a report from the University of Iowa/MayoClinic Specialized Program of Research Excellence Molecular Epidemiology Resource. J Clin Oncol. 2013;31:3272–8.

    Article  PubMed  Google Scholar 

  37. Friedberg JW, Cohen P, Chen L, Robinson KS, Forero-Torres A, La Casce AS, et al. Bendamustine in patients with rituximab-refractory indolent and transformed non-Hodgkin’s lymphoma: results from a phase II multicenter, single-agent study. J Clin Oncol. 2008;26:204–10.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Kiyohiko Hatake for the helpful advices.

Author information

Authors and Affiliations

  1. Department of Hematology Oncology, Higashi Sapporo Hospital, Sapporo, Japan

    Yasuo Hirayama

  2. Hokkaido Hematology Study Group, Sapporo, Japan

    Shuithi Ota, Mitsutoshi Kurosawa, Takeshi Kondo, Rishu Takimoto, Akio Mori, Hajime Sakai, Yoshihiro Torimoto, Satoshi Yamamoto, Kazuya Sato, Hiroshi Iwasaki, Kyuhei Kohda, Tadao Ishida, Yasuhiro Kakinoki & Takashi Fukuhara

  3. Division of Palliative Care, Higashi Sapporo Hospital, Sapporo, Japan

    Kunihiko Ishitani

  4. Department of Hematology, Sapporo Hokuyu Hospital, Sapporo, Hokkaido, Japan

    Shuithi Ota

  5. Department of Hematology, Hokkaido Cancer Center, National Hospital Organization, Sapporo, Japan

    Mitsutoshi Kurosawa

  6. Department of Hematology, Hokkaido University Hospital, Sapporo, Japan

    Takeshi Kondo

  7. Department of Medical Oncology/Hematology, Sapporo Medical University School of Medicine, Sapporo, Japan

    Rishu Takimoto & Junji Kato

  8. Department of Internal Medicine, Aiiku Hospital, Sapporo, Japan

    Akio Mori

  9. Department of Hematology, Teine Keijinkai Hospital, Sapporo, Japan

    Hajime Sakai

  10. Oncology Center, Asahikawa Medical University Hospital, Asahikawa, Japan

    Yoshihiro Torimoto

  11. Department of Hematology, Sapporo City General Hospital, Sapporo, Japan

    Satoshi Yamamoto

  12. Department of Hematology/Oncology, Asahikawa Kosei Hospital, Asahikawa, Japan

    Kazuya Sato

  13. Department of Hematology/Oncology, Sapporo Kosei Hospital, Sapporo, Japan

    Hiroshi Iwasaki

  14. Department of Hematology and Oncology, Asahikawa Red Cross Hospital, Asahikawa, Japan

    Kyuhei Kohda

  15. Department of Gastroenterology, Rheumatology and Clinical Immunology, Sapporo Medical University, Sapporo, Japan

    Tadao Ishida

  16. Department of Hematology, Asahikawa City General Hospital, Asahikawa, Japan

    Yasuhiro Kakinoki

  17. Palliative Care Center, Sapporo Kosei General Hospital, Sapporo, Japan

    Takashi Fukuhara

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  1. Yasuo Hirayama
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Correspondence to Yasuo Hirayama.

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Hirayama, Y., Ishitani, K., Ota, S. et al. Long-term survey of survival time, histological transformation, and secondary malignancies in Japanese patients with advanced-stage follicular lymphoma in the rituximab era: Hokkaido Hematology Study Group. Int J Hematol 100, 281–289 (2014). https://doi.org/10.1007/s12185-014-1629-4

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  • DOI: https://doi.org/10.1007/s12185-014-1629-4

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