Higher World Health Organization grades of follicular lymphoma correlate with better outcome in two Nordic Lymphoma Group trials of rituximab without chemotherapy

References

• Fisher RI, LeBlanc M, Press OW, et al. New treatment options have changed the survival of patients with follicular lymphoma. J Clin Oncol 2005;23:8447–8452.
   PubMed Web of Science ®Google Scholar
• Liu Q, Fayad L, Cabanillas F, et al. Improvement of overall and failure-free survival in stage IV follicular lymphoma: 25 years of treatment experience at The University of Texas M.D. Anderson Cancer Center. J Clin Oncol 2006;24:1582–1589.
   Web of Science ®Google Scholar
• Friedberg JW, Taylor MD, Cerhan JR, et al. Follicular lymphoma in the United States: first report of the national LymphoCare study. J Clin Oncol 2009;27:1202–1208.
   PubMed Web of Science ®Google Scholar
• Salles G, Seymour JF, Offner F, et al. Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial. Lancet 2011;377:42–51.
   PubMed Web of Science ®Google Scholar
• Martinelli G, Schmitz SF, Utiger U, et al. Long-term follow-up of patients with follicular lymphoma receiving single-agent rituximab at two different schedules in trial SAKK 35/98. J Clin Oncol 2010;28: 4480–4484.
   PubMed Web of Science ®Google Scholar
• Hainsworth JD, Burris HA, 3rd, Morrissey LH, et al. Rituximab monoclonal antibody as initial systemic therapy for patients with low-grade non-Hodgkin lymphoma. Blood 2000;95:3052–3056.
   PubMed Web of Science ®Google Scholar
• Colombat P, Salles G, Brousse N, et al. Rituximab (anti-CD20 monoclonal antibody) as single first-line therapy for patients with follicular lymphoma with a low tumor burden: clinical and molecular evaluation. Blood 2001;97:101–106.
   PubMed Web of Science ®Google Scholar
• Witzig TE, Vukov AM, Habermann TM, et al. Rituximab therapy for patients with newly diagnosed, advanced-stage, follicular grade I non-Hodgkin's lymphoma: a phase II trial in the North Central Cancer Treatment Group. J Clin Oncol 2005;23:1103–1108.
   PubMed Web of Science ®Google Scholar
• Ghielmini M, Schmitz SF, Cogliatti SB, et al. Prolonged treatment with rituximab in patients with follicular lymphoma significantly increases event-free survival and response duration compared with the standard weekly x 4 schedule. Blood 2004;103:4416–4423.
   PubMed Web of Science ®Google Scholar
• Harris NL, Swerdlow SH, Jaffe ES, et al. Follicular lymphoma. In: Swerdlow SH, Campo E, Harris NL, et al., editors. WHO classification of tumours of haematopoietic and lymphoid tissues. 4th ed. Lyon: IARC; 2008. pp. 220–226.
   Google Scholar
• Wahlin BE, Yri OE, Kimby E, et al. Clinical significance of the WHO grades of follicular lymphoma in a population-based cohort of 505 patients with long follow-up times. Br J Haematol 2012;156:225–233.
   PubMed Web of Science ®Google Scholar
• Vitolo U, Ferreri AJ, Montoto S. Follicular lymphomas. Crit Rev Oncol Hematol 2008;66:248–261.
   PubMed Web of Science ®Google Scholar
• Kimby E, Jurlander J, Geisler C, et al. Long-term molecular remissions in patients with indolent lymphoma treated with rituximab as a single agent or in combination with interferon alpha-2a: a randomized phase II study from the Nordic Lymphoma Group. Leuk Lymphoma 2008;49:102–112.
   PubMed Web of Science ®Google Scholar
• Wahlin BE, Sundstrom C, Holte H, et al. T cells in tumors and blood predict outcome in follicular lymphoma treated with rituximab. Clin Cancer Res 2011;17:4136–4144.
   PubMed Web of Science ®Google Scholar
• Harris NL, Jaffe ES, Diebold J, et al. World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting-Airlie House, Virginia, November 1997. J Clin Oncol 1999;17:3835–3849.
   PubMed Web of Science ®Google Scholar
• Nathwani BN, Harris NL, Weisenberger DD, et al. Follicular lymphoma. In: Jaffe ES, Harris NL, Stein H, et al., editors. World Health Organization classification of tumours. Pathology & genetics of tumours of haematopoietic and lymphoid tissues. Lyon: IARC Press; 2001. pp. 162–167.
   Google Scholar
• Mann RB, Berard CW. Criteria for the cytologic subclassification of follicular lymphomas: a proposed alternative method. Hematol Oncol 1983;1:187–192.
   PubMedGoogle Scholar
• Solal-Celigny P, Roy P, Colombat P, et al. Follicular lymphoma international prognostic index. Blood 2004;104:1258–1265.
   PubMed Web of Science ®Google Scholar
• Marcus R, Imrie K, Belch A, et al. CVP chemotherapy plus rituximab compared with CVP as first-line treatment for advanced follicular lymphoma. Blood 2005;105:1417–1423.
   PubMed Web of Science ®Google Scholar
• Metter GE, Nathwani BN, Burke JS, et al. Morphological subclassification of follicular lymphoma: variability of diagnoses among hematopathologists, a collaborative study between the Repository Center and Pathology Panel for Lymphoma Clinical Studies. J Clin Oncol 1985;3:25–38.
   PubMed Web of Science ®Google Scholar
• Wahlin BE, Sander B, Christensson B, Kimby E. CD8 + T-cell content in diagnostic lymph nodes measured by flow cytometry is a predictor of survival in follicular lymphoma. Clin Cancer Res 2007;13:388–397.
   PubMed Web of Science ®Google Scholar
• Mankai A, Bordron A, Renaudineau Y, et al. Purine-rich box-1-mediated reduced expression of CD20 alters rituximab-induced lysis of chronic lymphocytic leukemia B cells. Cancer Res 2008;68: 7512–7519.
   PubMed Web of Science ®Google Scholar
• Mankai A, Buhe V, Hammadi M, et al. Improvement of rituximab efficiency in chronic lymphocytic leukemia by CpG-mediated upregulation of CD20 expression independently of PU.1. Ann NY Acad Sci 2009;1173:721–728.
   PubMed Web of Science ®Google Scholar
• Bezombes C, Fournie JJ, Laurent G. Direct effect of rituximab in B-cell-derived lymphoid neoplasias: mechanism, regulation, and perspectives. Mol Cancer Res 2011;9:1435–1442.
   PubMed Web of Science ®Google Scholar
• Beers SA, French RR, Chan HT, et al. Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection. Blood 2010;115:5191–5201.
   PubMed Web of Science ®Google Scholar
• Lim SH, Vaughan AT, Ashton-Key M, et al. Fc gamma receptor IIb on target B cells promotes rituximab internalization and reduces clinical efficacy. Blood 2011;118:2530–2540.
   PubMed Web of Science ®Google Scholar
• Alduaij W, Illidge TM. The future of anti-CD20 monoclonal antibodies: are we making progress?. Blood 2011;117:2993–3001.
   PubMed Web of Science ®Google Scholar
• McLaughlin P, Grillo-Lopez AJ, Link BK, et al. Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program. J Clin Oncol 1998;16:2825–2833.
   PubMed Web of Science ®Google Scholar
• Harris NL, Jaffe ES, Stein H, et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994;84:1361–1392.
   PubMed Web of Science ®Google Scholar
• Coiffier B, Haioun C, Ketterer N, et al. Rituximab (anti-CD20 monoclonal antibody) for the treatment of patients with relapsing or refractory aggressive lymphoma: a multicenter phase II study. Blood 1998;92:1927–1932.
   PubMed Web of Science ®Google Scholar
• Piccaluga PP, Califano A, Klein U, et al. Gene expression analysis provides a potential rationale for revising the histological grading of follicular lymphomas. Haematologica 2008;93:1033–1038.
   PubMed Web of Science ®Google Scholar
• Horn H, Schmelter C, Leich E, et al. Follicular lymphoma grade 3B is a distinct neoplasm according to cytogenetic and immunohistochemical profiles. Haematologica 2011;96:1327–1334.
   PubMed Web of Science ®Google Scholar
• Hiddemann W, Kneba M, Dreyling M, 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;106:3725–3732.
   PubMed Web of Science ®Google Scholar
• Herold M, Haas A, Srock S, et al. Rituximab added to first-line mitoxantrone, chlorambucil, and prednisolone chemotherapy followed by interferon maintenance prolongs survival in patients with advanced follicular lymphoma: an East German Study Group Hematology and Oncology Study. J Clin Oncol 2007;25:1986–1992.
   PubMed Web of Science ®Google Scholar
• Salles G, Mounier N, de Guibert S, et al. Rituximab combined with chemotherapy and interferon in follicular lymphoma patients: results of the GELA-GOELAMS FL2000 study. Blood 2008;112: 4824–4831.
   PubMed Web of Science ®Google Scholar
• van Oers MH, Van Glabbeke M, Giurgea L, et al. Rituximab maintenance treatment of relapsed/resistant follicular non-Hodgkin’s lymphoma: long-term outcome of the EORTC 20981 phase III randomized intergroup study. J Clin Oncol 2010;28:2853–2858.
   PubMed Web of Science ®Google Scholar
• Cartron G, Trappe RU, Solal-Celigny P, Hallek M. Interindividual variability of response to rituximab: from biological origins to individualized therapies. Clin Cancer Res 2011;17:19–30.
   PubMed Web of Science ®Google Scholar
• Hilchey SP, Hyrien O, Mosmann TR, et al. Rituximab immunotherapy results in the induction of a lymphoma idiotype-specific T-cell response in patients with follicular lymphoma: support for a “vaccinal effect” of rituximab. Blood 2009;113:3809–3812.
   PubMed Web of Science ®Google Scholar
• Cartron G, Dacheux L, Salles G, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 2002;99:754–758.
   PubMed Web of Science ®Google Scholar
• Ghielmini M, Rufibach K, Salles G, et al. Single agent rituximab in patients with follicular or mantle cell lymphoma: clinical and biological factors that are predictive of response and event-free survival as well as the effect of rituximab on the immune system: a study of the Swiss Group for Clinical Cancer Research (SAKK). Ann Oncol 2005;16:1675–1682.
   PubMed Web of Science ®Google Scholar
• Weng WK, Levy R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol 2003;21:3940–3947.
   PubMed Web of Science ®Google Scholar
• Carlotti E, Palumbo GA, Oldani E, et al. FcgammaRIIIA and FcgammaRIIA polymorphisms do not predict clinical outcome of follicular non-Hodgkin's lymphoma patients treated with sequential CHOP and rituximab. Haematologica 2007;92:1127–1130.
   PubMed Web of Science ®Google Scholar
• Federico M, Bellei M, Marcheselli L, 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;27:4555–4562.
   PubMed Web of Science ®Google Scholar
• Feuerlein K, Zucca E, Ghielmini M. First-line treatment of follicular lymphoma: a patient-oriented algorithm. Leuk Lymphoma 2009;50:325–334.
   PubMed Web of Science ®Google Scholar