title: Thirty-Month Complete Response as a Surrogate End Point in First-Line Follicular Lymphoma Therapy: An Individual Patient-Level Analysis of Multiple Randomized Trials.
abstract: Purpose Follicular lymphoma (FL) is an indolent cancer, with effective but rarely curative treatment options. As a standard study end point for first-line FL therapy, progression-free survival (PFS) requires extended follow-up (median PFS, > 7 years). To provide patients with earlier access to newer therapies, an earlier end point to expedite clinical trials is needed. Our objective was to formally assess the complete response rate at 30 months (CR30) after initiation of induction therapy as a potential surrogate end point for PFS in first-line FL therapy. Patients and Methods We analyzed individual patient data from 13 randomized multicenter trials of induction and maintenance regimens in first-line FL therapy published after 1990 and with sufficient data to evaluate whether CR30 could predict treatment effects on PFS. Correlation of the CR30 odds ratio with the PFS hazard ratio was evaluated by both linear regression (R2WLS) and bivariate copula (R2Copula) models. Prespecified criteria for surrogacy required either R2WLSor R2Copula≥ 0.80, with a lower-bound 95% CI > 0.60. Results Data from eight induction and five maintenance randomized trials in 3,837 evaluable patients were analyzed. The prespecified surrogacy threshold was met, with an R2WLSof 0.88 (95% CI, 0.77 to 0.96) and an R2Copulaof 0.86 (95% CI, 0.72 to 1.00). Multiple sensitivity and supplemental analyses supported the robustness of the findings. A minimum 11% absolute improvement in CR30 from a 50% control rate predicted a significant treatment effect on PFS (hazard ratio, 0.69). Conclusion This large, prospective, pooled analysis of randomized chemotherapy, immunotherapy, and chemoimmunotherapy trials demonstrates that CR30 is a surrogate end point for PFS in first-line FL treatment trials. Use of this end point may expedite therapeutic development with the intent of bringing novel therapies to this patient population years before PFS results are mature.
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Qian
authors.initials: Q
authors.lastname: Shi
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Christopher R
authors.initials: CR
authors.lastname: Flowers
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Wolfgang
authors.initials: W
authors.lastname: Hiddemann
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Robert
authors.initials: R
authors.lastname: Marcus
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Michael
authors.initials: M
authors.lastname: Herold
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Anton
authors.initials: A
authors.lastname: Hagenbeek
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Eva
authors.initials: E
authors.lastname: Kimby
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Howard
authors.initials: H
authors.lastname: Hochster
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Umberto
authors.initials: U
authors.lastname: Vitolo
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Bruce A
authors.initials: BA
authors.lastname: Peterson
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Gyan
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Michele
authors.initials: M
authors.lastname: Ghielmini
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Tina
authors.initials: T
authors.lastname: Nielsen
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Sabine
authors.initials: S
authors.lastname: De Bedout
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Tommy
authors.initials: T
authors.lastname: Fu
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Nancy
authors.initials: N
authors.lastname: Valente
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Nathan H
authors.initials: NH
authors.lastname: Fowler
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Eva
authors.initials: E
authors.lastname: Hoster
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Marco
authors.initials: M
authors.lastname: Ladetto
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Franck
authors.initials: F
authors.lastname: Morschhauser
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Emanuele
authors.initials: E
authors.lastname: Zucca
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Gilles
authors.initials: G
authors.lastname: Salles
authors.affiliation: Qian Shi and Daniel J. Sargent, Mayo Clinic, Rochester; Bruce A. Peterson, University of Minnesota, Minneapolis, MN; Christopher R. Flowers, Winship Cancer Institute of Emory University, Atlanta, GA; Wolfgang Hiddemann and Eva Hoster, Ludwig-Maximilians University Hospital, Munich; Michael Herold, HELIOS Kliniken, Erfurt, Germany; Robert Marcus, Addenbrooke's Hospital, Cambridge, United Kingdom; Anton Hagenbeek, Academic Medical Center, Amsterdam, the Netherlands; Eva Kimby, Karolinska Institutet, Stockholm, Sweden; Howard Hochster, Yale Cancer Center, New Haven, CT; Umberto Vitolo, Azienda Ospedaliero-Universitaria Città della Salute e della Scienza di Torino, Turin; Marco Ladetto, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy; Emmanuel Gyan, University Hospital, Tours; Franck Morschhauser, Service Université de Lille 2, Lille; Gilles Salles, Université Claude Bernard, Pierre Bénite, France; Michele Ghielmini and Emanuele Zucca, Oncology Institute of Southern Switzerland, Bellinzona; Michele Ghielmini and Emanuele Zucca, Swiss Group for Clinical Cancer Research, Bern; Tina Nielsen, F. Hoffmann-La Roche, Basel; Sabine De Bedout, Celgene, Boudry, Switzerland; Tommy Fu, Celgene, Summit, NJ; Nancy Valente, Genentech, South San Francisco, CA; and Nathan H. Fowler, University of Texas MD Anderson Cancer Center, Houston, TX.
authors.forename: Daniel J
authors.initials: DJ
authors.lastname: Sargent
mesh_terms: D000328:Adult; D000368:Aged; D000369:Aged, 80 and over; D017326:Clinical Trials, Phase III as Topic; D018572:Disease-Free Survival; D005260:Female; D006801:Humans; D060828:Induction Chemotherapy / Q000379:methods*; D008224:Lymphoma, Follicular / Q000188:drug therapy*; D060046:Maintenance Chemotherapy / Q000379:methods*; D008297:Male; D008875:Middle Aged; D015337:Multicenter Studies as Topic; D017063:Outcome Assessment, Health Care / Q000379:methods / Q000706:statistics & numerical data; D016016:Proportional Hazards Models; D016032:Randomized Controlled Trials as Topic; D012074:Remission Induction; D013997:Time Factors; D055815:Young Adult