Dirk Hasenclever, Ph.D., Volker Diehl, M.D., James O. Armitage, David Assouline, Magnus Björkholm, Ercole Brusamolino, George P. Canellos, Patrice Carde, Derek Crowther, David Cunningham, Houchingue Eghbali, Christophe Ferm, Richard I. Fisher, John H. Glick, Bengt Glimelius, Paolo G. Gobbi, Harald Holte, Sandra J. Horning, T. Andrew Lister, Dan L. Longo, Franco Mandelli, Aaron Polliack, Stephen J. Proctor, Lena Specht, John W. Sweetenham, Gillian Vaughan Hudson, for The International Prognostic Factors Project on Advanced Hodgkin's Disease
Background Two thirds of patients with advanced Hodgkin's diseaseare cured with current approaches to treatment. Prediction ofthe outcome is important to avoid overtreating some patientsand to identify others in whom standard treatment is likelyto fail.
Methods Data were collected from 25 centers and study groupson a total of 5141 patients treated with combination chemotherapyfor advanced Hodgkin's disease, with or without radiotherapy.The data included the outcome and 19 demographic and clinicalcharacteristics at diagnosis. The end point was freedom fromprogression of disease. Complete data were available for 1618patients; the final Cox model was fitted to these data. Datafrom an additional 2643 patients were used for partial validation.
Results The prognostic score was defined as the number of adverseprognostic factors present at diagnosis. Seven factors had similarindependent prognostic effects: a serum albumin level of lessthan 4 g per deciliter, a hemoglobin level of less than 10.5g per deciliter, male sex, an age of 45 years or older, stageIV disease (according to the Ann Arbor classification), leukocytosis(a white-cell count of at least 15,000 per cubic millimeter),and lymphocytopenia (a lymphocyte count of less than 600 percubic millimeter, a count that was less than 8 percent of thewhite-cell count, or both). The score predicted the rate offreedom from progression of disease as follows: 0, or no factors(7 percent of the patients), 84 percent; 1 (22 percent of thepatients), 77 percent; 2 (29 percent of the patients), 67 percent;3 (23 percent of the patients), 60 percent; 4 (12 percent ofthe patients), 51 percent; and 5 or higher (7 percent of thepatients), 42 percent.
Conclusions The prognostic score we developed may be usefulin designing clinical trials for the treatment of advanced Hodgkin'sdisease and in making individual therapeutic decisions, buta distinct group of patients at very high risk could not beidentified on the basis of routinely documented demographicand clinical characteristics.
Source Information
From the Institute of Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig (D.H.); and Clinic I for Internal Medicine, University of Cologne, Cologne (V.D.) — both in Germany. Other authors were James O. Armitage, David Assouline, Magnus Björkholm, Ercole Brusamolino, George P. Canellos, Patrice Carde, Derek Crowther, David Cunningham, Houchingue Eghbali, Christophe Fermé, Richard I. Fisher, John H. Glick, Bengt Glimelius, Paolo G. Gobbi, Harald Holte, Sandra J. Horning, T. Andrew Lister, Dan L. Longo, Franco Mandelli, Aaron Polliack, Stephen J. Proctor, Lena Specht, John W. Sweetenham, and Gillian Vaughan Hudson.
Address reprint requests to Dr. Hasenclever at IMISE, University of Leipzig, Liebigstr. 27, D-04103 Leipzig, Germany.
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(2006). Plasma Epstein-Barr Virus (EBV) DNA Is a Biomarker for EBV-Positive Hodgkin's Lymphoma. Clin. Cancer Res.
12: 460-464
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Gobbi, P. G., Broglia, C., Levis, A., La Sala, A., Valentino, F., Chisesi, T., Sacchi, S., Corbella, F., Cavanna, L., Iannitto, E., Pavone, V., Molica, S., Corazza, G. R., Federico, M.
(2006). MOPPEBVCAD Chemotherapy with Limited and Conditioned Radiotherapy in Advanced Hodgkin's Lymphoma: 10-Year Results, Late Toxicity, and Second Tumors. Clin. Cancer Res.
12: 529-535
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Raanani, P., Shasha, Y., Perry, C., Metser, U., Naparstek, E., Apter, S., Nagler, A., Polliack, A., Ben-Bassat, I., Even-Sapir, E.
(2006). Is CT scan still necessary for staging in Hodgkin and non-Hodgkin lymphoma patients in the PET/CT era?. Ann Oncol
17: 117-122
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Gospodarowicz, M. K., Meyer, R. M.
(2006). The Management of Patients with Limited-Stage Classical Hodgkin Lymphoma. ASH Education Book
2006: 253-258
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Navarro, W. H., Kaplan, L. D.
(2006). AIDS-related lymphoproliferative disease. Blood
107: 13-20
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Hutchings, M., Loft, A., Hansen, M., Pedersen, L. M., Buhl, T., Jurlander, J., Buus, S., Keiding, S., D'Amore, F., Boesen, A.-M., Berthelsen, A. K., Specht, L.
(2006). FDG-PET after two cycles of chemotherapy predicts treatment failure and progression-free survival in Hodgkin lymphoma. Blood
107: 52-59
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Gobbi, P. G., Levis, A., Chisesi, T., Broglia, C., Vitolo, U., Stelitano, C., Pavone, V., Cavanna, L., Santini, G., Merli, F., Liberati, M., Baldini, L., Deliliers, G. L., Angelucci, E., Bordonaro, R., Federico, M.
(2005). ABVD Versus Modified Stanford V Versus MOPPEBVCAD With Optional and Limited Radiotherapy in Intermediate- and Advanced-Stage Hodgkin's Lymphoma: Final Results of a Multicenter Randomized Trial by the Intergruppo Italiano Linfomi. JCO
23: 9198-9207
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Carde, P.
(2005). The Chemotherapy/Radiation Balance in Advanced Hodgkin's Lymphoma: Overweight Which Side?. JCO
23: 9058-9062
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Klimm, B., Reineke, T., Haverkamp, H., Behringer, K., Eich, H. T., Josting, A., Pfistner, B., Diehl, V., Engert, A.
(2005). Role of Hematotoxicity and Sex in Patients With Hodgkin's Lymphoma: An Analysis From the German Hodgkin Study Group. JCO
23: 8003-8011
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Martin, W. G., Ristow, K. M., Habermann, T. M., Colgan, J. P., Witzig, T. E., Ansell, S. M.
(2005). Bleomycin Pulmonary Toxicity Has a Negative Impact on the Outcome of Patients With Hodgkin's Lymphoma. JCO
23: 7614-7620
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Duwe, B. V., Sterman, D. H., Musani, A. I.
(2005). Tumors of the Mediastinum. Chest
128: 2893-2909
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Connors, J. M.
(2005). State-of-the-Art Therapeutics: Hodgkin's Lymphoma. JCO
23: 6400-6408
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Weihrauch, M. R., Manzke, O., Beyer, M., Haverkamp, H., Diehl, V., Bohlen, H., Wolf, J., Schultze, J. L.
(2005). Elevated Serum Levels of CC Thymus and Activation-Related Chemokine (TARC) in Primary Hodgkin's Disease: Potential for a Prognostic Factor. Cancer Res.
65: 5516-5519
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Hutchings, M., Mikhaeel, N. G., Fields, P. A., Nunan, T., Timothy, A. R.
(2005). Prognostic value of interim FDG-PET after two or three cycles of chemotherapy in Hodgkin lymphoma. Ann Oncol
16: 1160-1168
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Re, D., Thomas, R. K., Behringer, K., Diehl, V.
(2005). From Hodgkin disease to Hodgkin lymphoma: biologic insights and therapeutic potential. Blood
105: 4553-4560
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Sup, S. J., Alemany, C. A., Pohlman, B., Elson, P., Malhi, S., Thakkar, S., Steinle, R., Hsi, E. D.
(2005). Expression of bcl-2 in Classical Hodgkin's Lymphoma: An Independent Predictor of Poor Outcome. JCO
23: 3773-3779
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Hohaus, S., Di Ruscio, A., Di Febo, A., Massini, G., D'Alo', F., Guidi, F., Mansueto, G., Voso, M. T., Leone, G.
(2005). Glutathione S-transferase P1 Genotype and Prognosis in Hodgkin's Lymphoma. Clin. Cancer Res.
11: 2175-2179
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Josting, A., Nogova, L., Franklin, J., Glossmann, J.-P., Eich, H. T., Sieber, M., Schober, T., Boettcher, H.-D., Schulz, U., Muller, R.-P., Diehl, V., Engert, A.
(2005). Salvage Radiotherapy in Patients With Relapsed and Refractory Hodgkin's Lymphoma: A Retrospective Analysis From the German Hodgkin Lymphoma Study Group. JCO
23: 1522-1529
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Vassilakopoulos, T. P., Angelopoulou, M. K., Constantinou, N., Karmiris, T., Repoussis, P., Roussou, P., Siakantaris, M. P., Korkolopoulou, P., Kyrtsonis, M.-C., Kokoris, S. I., Dimopoulou, M. N., Variamis, E., Viniou, N.-A., Konstantopoulos, K., Dimitriadou, E. M., Androulaki, A., Patsouris, E., Doussis-Anagnostopoulou, I. A., Panayiotidis, P., Boussiotis, V. A., Kittas, C., Pangalis, G. A.
(2005). Development and validation of a clinical prediction rule for bone marrow involvement in patients with Hodgkin lymphoma. Blood
105: 1875-1880
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Alvaro, T., Lejeune, M., Salvado, M. T., Bosch, R., Garcia, J. F., Jaen, J., Banham, A. H., Roncador, G., Montalban, C., Piris, M. A.
(2005). Outcome in Hodgkin's Lymphoma Can Be Predicted from the Presence of Accompanying Cytotoxic and Regulatory T Cells. Clin. Cancer Res.
11: 1467-1473
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Ballova, V., Ruffer, J.-U., Haverkamp, H., Pfistner, B., Muller-Hermelink, H. K., Duhmke, E., Worst, P., Wilhelmy, M., Naumann, R., Hentrich, M., Eich, H. T., Josting, A., Loffler, M., Diehl, V., Engert, A.
(2005). A prospectively randomized trial carried out by the German Hodgkin Study Group (GHSG) for elderly patients with advanced Hodgkin's disease comparing BEACOPP baseline and COPP-ABVD (study HD9elderly). Ann Oncol
16: 124-131
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Walewski, J., Lampka, E., Kraszewska, E., Osiadacz, W., Tajer, J., Konecki, R., Romejko-Jarosinska, J., Zwolinski, J., Meder, J.
(2004). CHOP Chemotherapy for Unfavorable or Advanced Hodgkin's Lymphoma. A Pilot Study.. ASH ANNUAL MEETING ABSTRACTS
104: 1311-1311
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Hudis, C. A., Van Belle, S., Chang, J., Muenstedt, K.
(2004). rHuEPO and Treatment Outcomes: the Clinical Experience. The Oncologist
9: 55-69
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Dispenzieri, A., Gertz, M. A., Kyle, R. A., Lacy, M. Q., Burritt, M. F., Therneau, T. M., Greipp, P. R., Witzig, T. E., Lust, J. A., Rajkumar, S. V., Fonseca, R., Zeldenrust, S. R., McGregor, C. G.A., Jaffe, A. S.
(2004). Serum Cardiac Troponins and N-Terminal Pro-Brain Natriuretic Peptide: A Staging System for Primary Systemic Amyloidosis. JCO
22: 3751-3757
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Czyz, J., Dziadziuszko, R., Knopinska-Postuszuy, W., Hellmann, A., Kachel, L., Holowiecki, J., Gozdzik, J., Hansz, J., Avigdor, A., Nagler, A., Osowiecki, M., Walewski, J., Mensah, P., Jurczak, W., Skotnicki, A., Sedzimirska, M., Lange, A., Sawicki, W., Sulek, K., Wach, M., Dmoszynska, A., Kus, A., Robak, T., Warzocha, K.
(2004). Outcome and prognostic factors in advanced Hodgkin's disease treated with high-dose chemotherapy and autologous stem cell transplantation: a study of 341 patients. Ann Oncol
15: 1222-1230
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Bredenfeld, H., Franklin, J., Nogova, L., Josting, A., Fries, S., Mailander, V., Oertel, J., Diehl, V., Engert, A.
(2004). Severe Pulmonary Toxicity in Patients With Advanced-Stage Hodgkin's Disease Treated With a Modified Bleomycin, Doxorubicin, Cyclophosphamide, Vincristine, Procarbazine, Prednisone, and Gemcitabine (BEACOPP) Regimen Is Probably Related to the Combination of Gemcitabine and Bleomycin: A Report of the German Hodgkin's Lymphoma Study Group. JCO
22: 2424-2429
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Bendandi, M., Pileri, S. A., Zinzani, P. L.
(2004). Challenging paradigms in lymphoma treatment. Ann Oncol
15: 703-711
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Montalban, C., Garcia, J. F., Abraira, V., Gonzalez-Camacho, L., Morente, M. M., Bello, J. L., Conde, E., Cruz, M. A., Garcia-Sanz, R., Garcia-Larana, J., Grande, C., Llanos, M., Martinez, R., Flores, E., Mendez, M., Ponderos, C., Rayon, C., Sanchez-Godoy, P., Zamora, J., Piris, M. A.
(2004). Influence of Biologic Markers on the Outcome of Hodgkin's Lymphoma: A Study by the Spanish Hodgkin's Lymphoma Study Group. JCO
22: 1664-1673
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Sanchez-Aguilera, A., Delgado, J., Camacho, F. I., Sanchez-Beato, M., Sanchez, L., Montalban, C., Fresno, M. F., Martin, C., Piris, M. A., Garcia, J. F.
(2004). Silencing of the p18INK4c gene by promoter hypermethylation in Reed-Sternberg cells in Hodgkin lymphomas. Blood
103: 2351-2357
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Marshall, N. A., Christie, L. E., Munro, L. R., Culligan, D. J., Johnston, P. W., Barker, R. N., Vickers, M. A.
(2004). Immunosuppressive regulatory T cells are abundant in the reactive lymphocytes of Hodgkin lymphoma. Blood
103: 1755-1762
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Sieber, M., Tesch, H., Pfistner, B., Rueffer, U., Paulus, U., Munker, R., Hermann, R., Doelken, G., Koch, P., Oertel, J., Roller, S., Worst, P., Bischof, H., Glunz, A., Greil, R., von Kalle, K., Schalk, K. P., Hasenclever, D., Brosteanu, O., Duehmke, E., Georgii, A., Engert, A., Loeffler, M., Diehl, V.
(2004). Treatment of advanced Hodgkin's disease with COPP/ABV/IMEP versus COPP/ABVD and consolidating radiotherapy: final results of the German Hodgkin's Lymphoma Study Group HD6 trial. Ann Oncol
15: 276-282
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Laskar, S., Gupta, T., Vimal, S., Muckaden, M.A., Saikia, T.K., Pai, S.K., Naresh, K.N., Dinshaw, K.A.
(2004). Consolidation Radiation After Complete Remission in Hodgkin's Disease Following Six Cycles of Doxorubicin, Bleomycin, Vinblastine, and Dacarbazine Chemotherapy: Is There a Need?. JCO
22: 62-68
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Meyer, R. M., Ambinder, R. F., Stroobants, S.
(2004). Hodgkin's Lymphoma: Evolving Concepts with Implications for Practice. ASH Education Book
2004: 184-202
[Abstract][Full Text]
Leitch, H. A., Gascoyne, R. D., Chhanabhai, M., Voss, N. J., Klasa, R., Connors, J. M.
(2003). Limited-stage mantle-cell lymphoma. Ann Oncol
14: 1555-1561
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Hohaus, S., Massini, G., D'Alo', F., Guidi, F., Putzulu, R., Scardocci, A., Rabi, A., Di Febo, A. L., Voso, M. T., Leone, G.
(2003). Association between Glutathione S-Transferase Genotypes and Hodgkin's Lymphoma Risk and Prognosis. Clin. Cancer Res.
9: 3435-3440
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