PET-Based Staging Reduces the Prognostic Impact of Early Disease Progression in Patients with Follicular Lymphoma

Connie L. Batlevi, MD, PhD1,*, Fushen Sha, MD1,*, Anna Alperovich, MD1,*, Ai Ni, PhD2, Katy Smith, MBChB BSc1, Zhitao Ying, MD1, John F. Gerecitano, MD, PhD1, Paul A. Hamlin, MD1, Steve M. Horwitz, MD1, Erel Joffe, MD1, Anita Kumar, MD1, Matthew J. Matasar, MD1, Alison J. Moskowitz, MD1, Craig H. Moskowitz, MD1, Ariela Noy, MD1, Colette Owens, MD1, M. Lia Palomba, MD1, David Straus, MD1, Gottfried von Keudell, MD1, Andrew D. Zelenetz, MD, PhD1, Venkatraman E Seshan, PhD2, Stefano Luminari, MD3,4, Luigi Marcheselli, MS5, Massimo Federico, MD3, Anas Younes, MD1 1Department of Medicine, Lymphoma Service, Memorial Sloan Kettering Cancer Center, New York, NY

[1]  D. Scott,et al.  Early progression after BR is associated with high risk of transformation in advanced stage follicular lymphoma. , 2019, Blood.

[2]  P. Barr,et al.  How I treat early-relapsing follicular lymphoma. , 2019, Blood.

[3]  Scott E. Smith,et al.  The prognostic significance of PFS24 in follicular lymphoma following firstline immunotherapy: A combined analysis of 3 CALGB trials , 2018, Cancer medicine.

[4]  S. Barrington,et al.  Baseline Suvmax Did Not Predict Histological Transformation from Follicular Lymphoma to Aggressive Lymphoma in the Phase III GALLIUM Study , 2018, Blood.

[5]  G. Lenz,et al.  Long-Term Efficacy and Safety from the Copanlisib CHRONOS-1 Study in Patients with Relapsed or Refractory Indolent B-Cell Lymphoma , 2018, Blood.

[6]  W. Hiddemann,et al.  Prognostic value of end-of-induction PET response after first-line immunochemotherapy for follicular lymphoma (GALLIUM): secondary analysis of a randomised, phase 3 trial. , 2018, The Lancet. Oncology.

[7]  E. Kimby,et al.  Rituximab and the risk of transformation of follicular lymphoma: a retrospective pooled analysis. , 2018, The Lancet. Haematology.

[8]  F. Angrilli,et al.  Long-Term Results of the FOLL05 Trial Comparing R-CVP Versus R-CHOP Versus R-FM for the Initial Treatment of Patients With Advanced-Stage Symptomatic Follicular Lymphoma. , 2017, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[9]  D. Langer,et al.  [18F]‐FDG PET/CT in the staging and management of indolent lymphoma: A prospective multicenter PET registry study , 2017, Cancer.

[10]  P. Zinzani,et al.  Phase II study of copanlisib, a PI3K inhibitor, in relapsed or refractory, indolent or aggressive lymphoma , 2017, Annals of oncology : official journal of the European Society for Medical Oncology.

[11]  G. Salles,et al.  Idelalisib is effective in patients with high-risk follicular lymphoma and early relapse after initial chemoimmunotherapy. , 2017, Blood.

[12]  K. Foon,et al.  MAGNIFY: Phase IIIb Randomized Study of Lenalidomide Plus Rituximab (R2) Followed By Lenalidomide Vs. Rituximab Maintenance in Subjects with Relapsed/Refractory Follicular, Marginal Zone, or Mantle Cell Lymphoma , 2016 .

[13]  J. Cerhan,et al.  Early event status informs subsequent outcome in newly diagnosed follicular lymphoma , 2016, American journal of hematology.

[14]  G. Salles,et al.  Risk Factors and Outcomes for Patients With Follicular Lymphoma Who Had Histologic Transformation After Response to First-Line Immunochemotherapy in the PRIMA Trial. , 2016, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[15]  J. Gribben,et al.  Obinutuzumab plus bendamustine versus bendamustine monotherapy in patients with rituximab-refractory indolent non-Hodgkin lymphoma (GADOLIN): a randomised, controlled, open-label, multicentre, phase 3 trial. , 2016, The Lancet. Oncology.

[16]  R. Davis,et al.  Factors influencing outcome in advanced stage, low-grade follicular lymphoma treated at MD Anderson Cancer Center in the rituximab era. , 2016, Annals of oncology : official journal of the European Society for Medical Oncology.

[17]  M. Czuczman,et al.  Randomized Trial of Lenalidomide Alone Versus Lenalidomide Plus Rituximab in Patients With Recurrent Follicular Lymphoma: CALGB 50401 (Alliance). , 2015, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[18]  J. Cerhan,et al.  Early Relapse of Follicular Lymphoma After Rituximab Plus Cyclophosphamide, Doxorubicin, Vincristine, and Prednisone Defines Patients at High Risk for Death: An Analysis From the National LymphoCare Study. , 2015, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[19]  M. Dreyling,et al.  Abstract CT215: CHRONOS-1: Open-label, uncontrolled phase II trial of intravenous phosphatidylinositol-3 kinase alpha/delta inhibitor copanlisib in patients with relapsed, indolent Non-Hodgkin's lymphomas (iNHL) , 2015 .

[20]  G. Salles,et al.  PI3Kδ inhibition by idelalisib in patients with relapsed indolent lymphoma. , 2014, The New England journal of medicine.

[21]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[22]  M. Federico,et al.  The use of FDG-PET in the initial staging of 142 patients with follicular lymphoma: a retrospective study from the FOLL05 randomized trial of the Fondazione Italiana Linfomi. , 2013, Annals of oncology : official journal of the European Society for Medical Oncology.

[23]  F. Angrilli,et al.  R-CVP versus R-CHOP versus R-FM for the initial treatment of patients with advanced-stage follicular lymphoma: results of the FOLL05 trial conducted by the Fondazione Italiana Linfomi. , 2013, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[24]  R. Houot,et al.  Diagnostic and prognostic impact of 18F-FDG PET/CT in follicular lymphoma , 2010, European Journal of Nuclear Medicine and Molecular Imaging.

[25]  M. Gönen,et al.  The majority of transformed lymphomas have high standardized uptake values (SUVs) on positron emission tomography (PET) scanning similar to diffuse large B-cell lymphoma (DLBCL). , 2008, Annals of oncology : official journal of the European Society for Medical Oncology.

[26]  P. Moreau,et al.  Investigation of FDG-PET/CT imaging to guide biopsies in the detection of histological transformation of indolent lymphoma , 2008, Haematologica.

[27]  M. Calaminici,et al.  Risk and clinical implications of transformation of follicular lymphoma to diffuse large B-cell lymphoma. , 2007, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[28]  T. Nazeer,et al.  Role of fluorine‐18 fluoro‐deoxyglucose positron emission tomography scan in the evaluation and follow‐up of patients with low‐grade lymphomas , 2006, Cancer.

[29]  U. Jaeger,et al.  18F-fluoro-deoxy-glucose positron emission tomography (18F-FDG-PET) visualizes follicular lymphoma irrespective of grading. , 2006, Annals of oncology : official journal of the European Society for Medical Oncology.

[30]  D. Weisenburger,et al.  Lymphoma incidence patterns by WHO subtype in the United States, 1992-2001. , 2006, Blood.

[31]  Y. Erdi,et al.  Intensity of 18fluorodeoxyglucose uptake in positron emission tomography distinguishes between indolent and aggressive non-Hodgkin's lymphoma. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[32]  G. Salles,et al.  Incidence, predictive factors, and outcome of lymphoma transformation in follicular lymphoma patients. , 1997, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[33]  N. Dubrawsky.  Cancer statistics , 1989, CA: a cancer journal for clinicians.

[34]  R. Gray.  A Class of $K$-Sample Tests for Comparing the Cumulative Incidence of a Competing Risk , 1988 .

[35]  J R Anderson,et al.  Analysis of survival by tumor response. , 1983, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.