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Biol Blood Marrow Transplant. 2015 Dec;21(12):2091-2099. doi: 10.1016/j.bbmt.2015.07.028. Epub 2015 Aug 4.

Reduced-Intensity Allografting as First Transplantation Approach in Relapsed/Refractory Grades One and Two Follicular Lymphoma Provides Improved Outcomes in Long-Term Survivors.

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Department for Stem Cell Transplantation, University Cancer Center Hamburg, Hamburg, Germany.
Department for Hematology and Internal Oncology, Georg August University Göttingen, Göttingen, Germany.
Center for International Blood and Marrow Transplant Research (CIBMTR), Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin.
Center for International Blood and Marrow Transplant Research (CIBMTR), Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin; Division of Biostatistics, Institute for Health and Society, Medical College of Wisconsin, Milwaukee, Wisconsin.
Bone and Marrow Transplant Program, University of Minnesota Medical Center, Minneapolis, Minnesota.
Blood and Marrow Transplant Program at Northside Hospital, Atlanta, Georgia.
Department of Hematology and Medical Oncology, Winship Cancer Institute, Emory University School of Medicine, Atlanta, Georgia.
South Texas Veterans Health Care System and University of Texas Science Center San Antonio, San Antonio, San Antonio, Texas.
Hematology Research Centre, Division of Experimental Medicine, Department of Medicine, Imperial College London, London, United Kingdom.
Blood and Marrow Transplantation, Division of Hematology and Oncology, University of Kansas Medical Center, Kansas City, Kansas.
Department of Haematology, Prince of Wales Hospital, Randwick NSW, Australia.
Clinical Research Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.
Department of Blood and Marrow Transplantation, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida.
Divison of Hematology/Oncology, Department of Medicine, Tufts Medical Center, Boston, Massachusetts.
Division of Blood and Marrow Transplantation, Department of Medicine, University of California, San Diego, San Diego, California.
Division of Bone Marrow Transplantation, Stanford Hospital and Clinics, Stanford, California.
Seidman Cancer Center, University Hospitals Case Medical Center, Cleveland, Ohio.
Department of Oncology, Baylor University Medical Center, Dallas, Texas.
S.C. Ematologia e Trapianto Midollo Osseo, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy; Università degli Studi di Milano, Milan, Italy.
Division of Therapeutic Immunology, Department of Laboratory Medicine, Karolinska Institutet, Stockholm, Sweden; Centre for Clinical Research Sörmland, Uppsala University, Uppsala, Sweden.
The International Center for Cell Therapy and Cancer Immunotherapy, Tel Aviv, Israel.
Department of Hematology, Medical Oncology, Levine Cancer Institute, Carolinas HealthCare System, Charlotte, North Carolina.
Division of Hematology and Oncology, Washington University School of Medicine, St. Louis, Missouri.
Division of Hematology/Oncology, Department of Medicine, University of North Carolina, Chapel Hill, North Carolina.
Servei d'Hematologia, Institut Català d'Oncologia, Hospital Duran i Reynals, Barcelona, Spain; European Group for Blood and Marrow Transplantation.
Section of Hematology/Oncology, University of Chicago, Chicago, Illinois.
Center for International Blood and Marrow Transplant Research (CIBMTR), Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin. Electronic address:


This study was conducted to compare long-term outcomes in patients with refractory/relapsed grades 1 and 2 follicular lymphoma (FL) after allogeneic (allo) versus autologous (auto) hematopoietic cell transplantation (HCT) in the rituximab era. Adult patients with relapsed/refractory grades 1 and 2 FL undergoing first reduced-intensity allo-HCT or first autograft during 2000 to 2012 were evaluated. A total of 518 rituximab-treated patients were included. Allo-HCT patients were younger and more heavily pretreated, and more patients had advanced stage and chemoresistant disease. The 5-year adjusted probabilities, comparing auto-HCT versus allo-HCT groups for nonrelapse mortality (NRM) were 5% versus 26% (P < .0001); relapse/progression: 54% versus 20% (P < .0001); progression-free survival (PFS): 41% versus 58% (P < .001), and overall survival (OS): 74% versus 66% (P = .05). Auto-HCT was associated with a higher risk of relapse/progression beyond 5 months after HCT (relative risk [RR], 4.4; P < .0001) and worse PFS (RR, 2.9; P < .0001) beyond 11 months after HCT. In the first 24 months after HCT, auto-HCT was associated with improved OS (RR, .41; P < .0001), but beyond 24 months, it was associated with inferior OS (RR, 2.2; P = .006). A landmark analysis of patients alive and progression-free at 2 years after HCT confirmed these observations, showing no difference in further NRM between both groups, but there was significantly higher risk of relapse/progression (RR, 7.3; P < .0001) and inferior PFS (RR, 3.2; P < .0001) and OS (RR, 2.1; P = .04) after auto-HCT. The 10-year cumulative incidences of second hematological malignancies after allo-HCT and auto-HCT were 0% and 7%, respectively. Auto-HCT and reduced-intensity-conditioned allo-HCT as first transplantation approach can provide durable disease control in grades 1 and 2 FL patients. Continued disease relapse risk after auto-HCT translates into improved PFS and OS after allo-HCT in long-term survivors.


Autologous hematopoietic cell transplantation; Grade 1 and 2 follicular lymphoma; Long-time survival; Reduced-intensity allogeneic hematopoietic cell transplantation

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