Background Although many patients with intermediate-grade orhigh-grade (aggressive) non-Hodgkin's lymphoma are cured bycombination chemotherapy, the remainder are not cured and ultimatelydie of their disease. The Ann Arbor classification, used todetermine the stage of this disease, does not consistently distinguishbetween patients with different long-term prognoses. This projectwas undertaken to develop a model for predicting outcome inpatients with aggressive non-Hodgkin's lymphoma on the basisof the patients' clinical characteristics before treatment.
Methods Adults with aggressive non-Hodgkin's lymphoma from 16institutions and cooperative groups in the United States, Europe,and Canada who were treated between 1982 and 1987 with combination-chemotherapyregimens containing doxorubicin were evaluated for clinicalfeatures predictive of overall survival and relapse-free survival.Features that remained independently significant in step-downregression analyses of survival were incorporated into modelsthat identified groups of patients of all ages and groups ofpatients no more than 60 years old with different risks of death.
Results In 2031 patients of all ages, our model, based on age,tumor stage, serum lactate dehydrogenase concentration, performancestatus, and number of extranodal disease sites, identified fourrisk groups with predicted five-year survival rates of 73 percent,51 percent, 43 percent, and 26 percent. In 1274 patients 60or younger, an age-adjusted model based on tumor stage, lactatedehydrogenase level, and performance status identified fourrisk groups with predicted five-year survival rates of 83 percent,69 percent, 46 percent, and 32 percent. In both models, theincreased risk of death was due to both a lower rate of completeresponses and a higher rate of relapse from complete response.These two indexes, called the international index and the age-adjustedinternational index, were significantly more accurate than theAnn Arbor classification in predicting long-term survival.
Conclusions The international index and the age-adjusted internationalindex should be used in the design of future therapeutic trialsin patients with aggressive non-Hodgkin's lymphoma and in theselection of appropriate therapeutic approaches for individualpatients.
Source Information
The following persons are members of the International Non-Hodgkin's Lymphoma Prognostic Factors Project: M.A. Shipp (Dana-Farber Cancer Institute and Harvard Medical School, Boston) and D.P. Harrington (Dana-Farber Cancer Institute and Harvard Medical School, Boston; Eastern Cooperative Oncology Group, Denver), chairpersons; J.R. Anderson (Nebraska Lymphoma Study Group, Omaha; Cancer and Leukemia Group B, Lebanon, N.H.); J.O. Armitage (Nebraska Lymphoma Study Group, Omaha); G. Bonadonna (Istituto Nazionale Tumori, Milan, Italy); G. Brittinger (Bundesministerium fur Forschung und Technologie Study, Essen, Germany); F. Cabanillas (M.D. Anderson Cancer Center, Houston); G.P. Canellos (Dana-Farber Cancer Institute and Harvard Medical School, Boston); B. Coiffier (Groupe d'Etude des Lymphomes de l'Adulte, Paris); J.M. Connors (British Columbia Cancer Agency, Vancouver); R.A. Cowan and D. Crowther (Manchester Lymphoma Group, Manchester, United Kingdom); S. Dahlberg (Southwest Oncology Group, San Antonio, Tex.); M. Engelhard (Bundesministerium fur Forschung und Technologie Study, Essen, Germany); R.I. Fisher (Southwest Oncology Group, San Antonio, Tex.); C. Gisselbrecht (Groupe d'Etude des Lymphomes de l'Adulte, Paris); S.J. Horning (Stanford University, Stanford, Calif.); E. Lepage (Groupe d'Etude des Lymphomes de l'Adulte, Paris); T.A. Lister (St. Bartholomew's Hospital, London); J.H. Meerwaldt (Lymphoma Cooperative Group, European Organisation for Research on Treatment of Cancer, Brussels, Belgium); E. Montserrat (Hospital Clinic i Provincial de Barcelona, Barcelona, Spain); N.I. Nissen (Finsen Institute, Copenhagen, Denmark); M.M. Oken (Eastern Cooperative Oncology Group, Denver); B.A. Peterson (Cancer and Leukemia Group B, Lebanon, N.H.); C. Tondini (Istituto Nazionale Tumori, Milan, Italy); W.A. Velasquez (M.D. Anderson Cancer Center, Houston); and B.Y. Yeap (Dana-Farber Cancer Institute and Harvard Medical School, Boston; Eastern Cooperative Oncology Group, Denver).
Address reprint requests to Dr. Margaret A. Shipp at the Dana-Farber Cancer Institute, 44 Binney St., Boston, MA 02115.
Bone Marrow Transplantation versus Chemotherapy in Non-Hodgkin's Lymphoma
Seymour J. F., Flecknoe-Brown S., Mross K., Burke H. B., Nimer S. D., Zelenetz A., Portlock C., Finckh W., Fielding A. K., Pearce R. M., Goldstone A. H., Selwyn M. R., Verdonck L. F., van Putten W. L.J., Hagenbeek A., Walker A. M.
Extract |
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N Engl J Med 1995;
333:727-730, Sep 14, 1995.
Correspondence
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Marcus, R., Imrie, K., Solal-Celigny, P., Catalano, J. V., Dmoszynska, A., Raposo, J. C., Offner, F. C., Gomez-Codina, J., Belch, A., Cunningham, D., Wassner-Fritsch, E., Stein, G.
(2008). Phase III Study of R-CVP Compared With Cyclophosphamide, Vincristine, and Prednisone Alone in Patients With Previously Untreated Advanced Follicular Lymphoma. JCO
26: 4579-4586
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Geisler, C. H., Kolstad, A., Laurell, A., Andersen, N. S., Pedersen, L. B., Jerkeman, M., Eriksson, M., Nordstrom, M., Kimby, E., Boesen, A. M., Kuittinen, O., Lauritzsen, G. F., Nilsson-Ehle, H., Ralfkiaer, E., Akerman, M., Ehinger, M., Sundstrom, C., Langholm, R., Delabie, J., Karjalainen-Lindsberg, M.-L., Brown, P., Elonen, E., for the Nordic Lymphoma Group,
(2008). Long-term progression-free survival of mantle cell lymphoma after intensive front-line immunochemotherapy with in vivo-purged stem cell rescue: a nonrandomized phase 2 multicenter study by the Nordic Lymphoma Group. Blood
112: 2687-2693
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Habermann, T. M., Wang, S. S., Maurer, M. J., Morton, L. M., Lynch, C. F., Ansell, S. M., Hartge, P., Severson, R. K., Rothman, N., Davis, S., Geyer, S. M., Cozen, W., Chanock, S. J., Cerhan, J. R.
(2008). Host immune gene polymorphisms in combination with clinical and demographic factors predict late survival in diffuse large B-cell lymphoma patients in the pre-rituximab era. Blood
112: 2694-2702
[Abstract][Full Text]
Mead, G. M., Barrans, S. L., Qian, W., Walewski, J., Radford, J. A., Wolf, M., Clawson, S. M., Stenning, S. P., Yule, C. L., Jack, A. S., on behalf of the UK National Cancer Research Insti,
(2008). A prospective clinicopathologic study of dose-modified CODOX-M/IVAC in patients with sporadic Burkitt lymphoma defined using cytogenetic and immunophenotypic criteria (MRC/NCRI LY10 trial). Blood
112: 2248-2260
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International T-Cell Lymphoma Project,
(2008). International Peripheral T-Cell and Natural Killer/T-Cell Lymphoma Study: Pathology Findings and Clinical Outcomes. JCO
26: 4124-4130
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Sacchi, S., Marcheselli, L., Bari, A., Marcheselli, R., Pozzi, S., Gobbi, P. G., Angrilli, F., Brugiatelli, M., Musto, P., Federico, M.
(2008). Second malignancies after treatment of diffuse large B-cell non-Hodgkin's lymphoma: a GISL cohort study. haematol
93: 1335-1342
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Kim, T. M., Lee, S. -Y., Jeon, Y. K., Ryoo, B. -Y., Cho, G. J., Hong, Y. S., Kim, H. J., Kim, S.-Y., Kim, C. S., Kim, S., Kim, J. S., Sohn, S. K., Song, H. H., Lee, J. L., Kang, Y. K., Yim, C. Y., Lee, W. S., Yuh, Y. J., Kim, C. W., Heo, D. S., for the Lymphoma Subcommittee of the Korean Cancer,
(2008). Clinical heterogeneity of extranodal NK/T-cell lymphoma, nasal type: a national survey of the Korean Cancer Study Group. Ann Oncol
19: 1477-1484
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Yamaguchi, M., Nakamura, N., Suzuki, R., Kagami, Y., Okamoto, M., Ichinohasama, R., Yoshino, T., Suzumiya, J., Murase, T., Miura, I., Ohshima, K., Nishikori, M., Tamaru, J.-i., Taniwaki, M., Hirano, M., Morishima, Y., Ueda, R., Shiku, H., Nakamura, S.
(2008). De novo CD5+ diffuse large B-cell lymphoma: results of a detailed clinicopathological review in 120 patients. haematol
93: 1195-1202
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Tarella, C., Zanni, M., Magni, M., Benedetti, F., Patti, C., Barbui, T., Pileri, A., Boccadoro, M., Ciceri, F., Gallamini, A., Cortelazzo, S., Majolino, I., Mirto, S., Corradini, P., Passera, R., Pizzolo, G., Gianni, A. M., Rambaldi, A.
(2008). Rituximab Improves the Efficacy of High-Dose Chemotherapy With Autograft for High-Risk Follicular and Diffuse Large B-Cell Lymphoma: A Multicenter Gruppo Italiano Terapie Innnovative nei Linfomi Survey. JCO
26: 3166-3175
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Shimada, K., Matsue, K., Yamamoto, K., Murase, T., Ichikawa, N., Okamoto, M., Niitsu, N., Kosugi, H., Tsukamoto, N., Miwa, H., Asaoku, H., Kikuchi, A., Matsumoto, M., Saburi, Y., Masaki, Y., Yamaguchi, M., Nakamura, S., Naoe, T., Kinoshita, T.
(2008). Retrospective Analysis of Intravascular Large B-Cell Lymphoma Treated With Rituximab-Containing Chemotherapy As Reported by the IVL Study Group in Japan. JCO
26: 3189-3195
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Savage, K. J., Harris, N. L., Vose, J. M., Ullrich, F., Jaffe, E. S., Connors, J. M., Rimsza, L., Pileri, S. A., Chhanabhai, M., Gascoyne, R. D., Armitage, J. O., Weisenburger, D. D., for the International Peripheral T-Cell Lymphoma P,
(2008). ALK- anaplastic large-cell lymphoma is clinically and immunophenotypically different from both ALK+ ALCL and peripheral T-cell lymphoma, not otherwise specified: report from the International Peripheral T-Cell Lymphoma Project. Blood
111: 5496-5504
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Khouri, I. F., McLaughlin, P., Saliba, R. M., Hosing, C., Korbling, M., Lee, M. S., Medeiros, L. J., Fayad, L., Samaniego, F., Alousi, A., Anderlini, P., Couriel, D., de Lima, M., Giralt, S., Neelapu, S. S., Ueno, N. T., Samuels, B. I., Hagemeister, F., Kwak, L. W., Champlin, R. E.
(2008). Eight-year experience with allogeneic stem cell transplantation for relapsed follicular lymphoma after nonmyeloablative conditioning with fludarabine, cyclophosphamide, and rituximab. Blood
111: 5530-5536
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Malumbres, R., Chen, J., Tibshirani, R., Johnson, N. A., Sehn, L. H., Natkunam, Y., Briones, J., Advani, R., Connors, J. M., Byrne, G. E., Levy, R., Gascoyne, R. D., Lossos, I. S.
(2008). Paraffin-based 6-gene model predicts outcome in diffuse large B-cell lymphoma patients treated with R-CHOP. Blood
111: 5509-5514
[Abstract][Full Text]
Wilson, W. H., Dunleavy, K., Pittaluga, S., Hegde, U., Grant, N., Steinberg, S. M., Raffeld, M., Gutierrez, M., Chabner, B. A., Staudt, L., Jaffe, E. S., Janik, J. E.
(2008). Phase II Study of Dose-Adjusted EPOCH and Rituximab in Untreated Diffuse Large B-Cell Lymphoma With Analysis of Germinal Center and Post-Germinal Center Biomarkers. JCO
26: 2717-2724
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Persky, D. O., Unger, J. M., Spier, C. M., Stea, B., LeBlanc, M., McCarty, M. J., Rimsza, L. M., Fisher, R. I., Miller, T. P.
(2008). Phase II Study of Rituximab Plus Three Cycles of CHOP and Involved-Field Radiotherapy for Patients With Limited-Stage Aggressive B-Cell Lymphoma: Southwest Oncology Group Study 0014. JCO
26: 2258-2263
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Mercadal, S., Briones, J., Xicoy, B., Pedro, C., Escoda, L., Estany, C., Camos, M., Colomo, L., Espinosa, I., Martinez, S., Ribera, J.M., Martino, R., Gutierrez-Garcia, G., Montserrat, E., Lopez-Guillermo, A., On behalf of the Grup per l'Estudi dels Limfomes d,
(2008). Intensive chemotherapy (high-dose CHOP/ESHAP regimen) followed by autologous stem-cell transplantation in previously untreated patients with peripheral T-cell lymphoma. Ann Oncol
19: 958-963
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Dierlamm, J., Murga Penas, E. M., Bentink, S., Wessendorf, S., Berger, H., Hummel, M., Klapper, W., Lenze, D., Rosenwald, A., Haralambieva, E., Ott, G., Cogliatti, S. B., Moller, P., Schwaenen, C., Stein, H., Loffler, M., Spang, R., Trumper, L., Siebert, R., for the Deutsche Krebshilfe Network Project "Molec,
(2008). Gain of chromosome region 18q21 including the MALT1 gene is associated with the activated B-cell-like gene expression subtype and increased BCL2 gene dosage and protein expression in diffuse large B-cell lymphoma. haematol
93: 688-696
[Abstract][Full Text]
Mourad, N., Mounier, N., Briere, J., Raffoux, E., Delmer, A., Feller, A., Meijer, C. J. L. M., Emile, J.-F., Bouabdallah, R., Bosly, A., Diebold, J., Haioun, C., Coiffier, B., Gisselbrecht, C., Gaulard, P.
(2008). Clinical, biologic, and pathologic features in 157 patients with angioimmunoblastic T-cell lymphoma treated within the Groupe d'Etude des Lymphomes de l'Adulte (GELA) trials. Blood
111: 4463-4470
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Canellos, G. P.
(2008). What Constitutes "Improved Prognosis"?. JCO
26: 1913-1914
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Ladetto, M., De Marco, F., Benedetti, F., Vitolo, U., Patti, C., Rambaldi, A., Pulsoni, A., Musso, M., Liberati, A. M., Olivieri, A., Gallamini, A., Pogliani, E., Scalabrini, D. R., Callea, V., Di Raimondo, F., Pavone, V., Tucci, A., Cortelazzo, S., Levis, A., Boccadoro, M., Majolino, I., Pileri, A., Gianni, A. M., Passera, R., Corradini, P., Tarella, C., for Gruppo Italiano Trapianto di Midollo Osseo (GI,
(2008). 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
111: 4004-4013
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Ziepert, M., Schmits, R., Trumper, L., Pfreundschuh, M., Loeffler, M., On behalf of the German High-Grade Non-Hodgkin's L,
(2008). Prognostic factors for hematotoxicity of chemotherapy in aggressive non-Hodgkin's lymphoma. Ann Oncol
19: 752-762
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Thieblemont, C., Grossoeuvre, A., Houot, R., Broussais-Guillaumont, F., Salles, G., Traulle, C., Espinouse, D., Coiffier, B.
(2008). Non-Hodgkin's lymphoma in very elderly patients over 80 years. A descriptive analysis of clinical presentation and outcome. Ann Oncol
19: 774-779
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Zinzani, P. L., Tani, M., Fanti, S., Stefoni, V., Musuraca, G., Castellucci, P., Marchi, E., Farsad, M., Fina, M., Pellegrini, C., Alinari, L., Derenzini, E., de Vivo, A., Bacci, F., Pileri, S., Baccarani, M.
(2008). A phase II trial of CHOP chemotherapy followed by yttrium 90 ibritumomab tiuxetan (Zevalin) for previously untreated elderly diffuse large B-cell lymphoma patients. Ann Oncol
19: 769-773
[Abstract][Full Text]
Pfreundschuh, M., Zwick, C., Zeynalova, S., Duhrsen, U., Pfluger, K.-H., Vrieling, T., Mesters, R., Mergenthaler, H.-G., Einsele, H., Bentz, M., Lengfelder, E., Trumper, L., Rube, C., Schmitz, N., Loeffler, M., On behalf of the German High-Grade Non-Hodgkin's L,
(2008). Dose-escalated CHOEP for the treatment of young patients with aggressive non-Hodgkin's lymphoma: II. Results of the randomized high-CHOEP trial of the German High-Grade Non-Hodgkin's Lymphoma Study Group (DSHNHL). Ann Oncol
19: 545-552
[Abstract][Full Text]
Overman, M. J., Feng, L., Pro, B., McLaughlin, P., Hess, M., Samaniego, F., Younes, A., Romaguera, J. E., Hagemeister, F. B., Kwak, L., Cabanillas, F., Rodriguez, M. A., Fayad, L. E.
(2008). The addition of rituximab to CHOP chemotherapy improves overall and failure-free survival for follicular grade 3 lymphoma. Ann Oncol
19: 553-559
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Morel, P., Gaulard, P., Gisselbrecht, C., Ferme, C., Salles, G., Tilly, H., Briere, J., Copin, M. C., Lederlin, P., Hermine, O., Theate, I., Haioun, C., Mounier, N.
(2008). Autologous stem-cell transplantation as consolidation therapy for diffuse large B-cell lymphoma patients with overexpression of bcl-2 protein. Results of the Groupe d'Etude des Lymphomes de l'Adulte (GELA) trial LNH98-B2. Ann Oncol
19: 560-565
[Abstract][Full Text]
Trumper, L., Zwick, C., Ziepert, M., Hohloch, K., Schmits, R., Mohren, M., Liersch, R., Bentz, M., Graeven, U., Wruck, U., Hoffmann, M., Metzner, B., Hasenclever, D., Loeffler, M., Pfreundschuh, M., On behalf of the German High-Grade Non-Hodgkin's L,
(2008). Dose-escalated CHOEP for the treatment of young patients with aggressive non-Hodgkin's lymphoma: I. A randomized dose escalation and feasibility study with bi- and tri-weekly regimens. Ann Oncol
19: 538-544
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Traverse-Glehen, A., Baseggio, L., Bauchu, E. C., Morel, D., Gazzo, S., Ffrench, M., Verney, A., Rolland, D., Thieblemont, C., Magaud, J.-P., Salles, G., Coiffier, B., Berger, F., Felman, P.
(2008). Splenic red pulp lymphoma with numerous basophilic villous lymphocytes: a distinct clinicopathologic and molecular entity?. Blood
111: 2253-2260
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Ryan, G., Martinelli, G., Kuper-Hommel, M., Tsang, R., Pruneri, G., Yuen, K., Roos, D., Lennard, A., Devizzi, L., Crabb, S., Hossfeld, D., Pratt, G., Dell'Olio, M., Choo, S. P., Bociek, R. G., Radford, J., Lade, S., Gianni, A. M., Zucca, E., Cavalli, F., Seymour, J. F.
(2008). Primary diffuse large B-cell lymphoma of the breast: prognostic factors and outcomes of a study by the International Extranodal Lymphoma Study Group. Ann Oncol
19: 233-241
[Abstract][Full Text]
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