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Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging 2/2015

01.02.2015 | Original Article

PET/CT before autologous stem cell transplantation predicts outcome in refractory/relapsed follicular lymphoma

verfasst von: Marion Alcantara, Jehan Dupuis, Sylvain Mareschal, Anne Julian, Anne Ségolène Cottereau, Stéphanie Becker, Sydney Dubois, Lucie Oberic, Anne Huynh, Michel Meignan, Guy Laurent, Hervé Tilly, Corinne Haioun, Loïc Ysebaert

Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging | Ausgabe 2/2015

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Abstract

Purpose

Salvage of young patients with follicular lymphoma (FL) after R-CHOP includes salvage immunochemotherapy followed by autologous stem cell transplantation (ASCT). Previous studies dealing with relapsed Hodgkin lymphoma have shown the prognostic value of PET/CT prior to ASCT.

Methods

We retrospectively analysed 59 patients with refractory/relapsed FL after first-line R-CHOP who were chemosensitive (as evaluated by CT) to the salvage treatment and who proceeded to ASCT. The role of PET/CT in this setting to define chemosensitivity is not definitely established. So we focused on the prognostic value of PET/CT performed after salvage treatment, before ASCT.

Results

The estimated 3-year progression-free survival (PFS) and overall survival were 63.1 % (50.9–78.3 %) and 90.5 % (82.8 – 98.8 %), respectively, and did not differ significantly according to their Follicular Lymphoma International Prognostic Index at relapse, conditioning regimen, or type of salvage. PFS was significantly lower in PET/CT-positive patients, according to the International Harmonization Project revised response criteria, with a 3-year PFS of 45.5 % (26.6 – 77.8 %) versus 72.6 % (58.5 – 90.0 %; p = 0.039). To better refine prognosis, we applied two types of throsholds: a Deauville five-point scale positive threshold of ≥3 (3-year PFS of 74.9 %, range 61.0 – 92.1 % %, versus 42.8 %, range 24.7 – 74.4 %; p = 0.02), and a ≥70 % ∆SUVmax threshold between presalvage and pre-ASCT PET/CT (3-year PFS of 72.4 %, range 57.5 – 91.3 % versus 13.3 %, 2.2 – 81.7 %; p < 10−3). The PET/CT findings before ASCT were independently correlated with PFS in our series.

Conclusion

PET/CT negativity before ASCT is a desirable and achievable goal in the management of chemosensitive FL relapsing after first-line R-CHOP.
Literatur
1.
Zurück zum Zitat Swerdlow SH. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon, France: International Agency for Research on Cancer; 2008. Swerdlow SH. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon, France: International Agency for Research on Cancer; 2008.
3.
Zurück zum Zitat Brice P, Bastion Y, Lepage E, Brousse N, Haïoun C, Moreau P, et al. Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: a randomized study from the Groupe d'Etude des Lymphomes Folliculaires. Groupe d'Etude des Lymphomes de l'Adulte. J Clin Oncol. 1997;15:1110–7.PubMed Brice P, Bastion Y, Lepage E, Brousse N, Haïoun C, Moreau P, et al. Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: a randomized study from the Groupe d'Etude des Lymphomes Folliculaires. Groupe d'Etude des Lymphomes de l'Adulte. J Clin Oncol. 1997;15:1110–7.PubMed
4.
Zurück zum Zitat Hiddemann W, Kneba M, Dreyling M, Schmitz N, Lengfelder E, Schmits R, et al. Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group. Blood. 2005;106:3725–32.PubMedCrossRef Hiddemann W, Kneba M, Dreyling M, Schmitz N, Lengfelder E, Schmits R, et al. Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group. Blood. 2005;106:3725–32.PubMedCrossRef
5.
Zurück zum Zitat Salles G, Seymour JF, Offner F, López-Guillermo A, Belada D, Xerri L, et al. Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial. Lancet. 2011;377:42–51.PubMedCrossRef Salles G, Seymour JF, Offner F, López-Guillermo A, Belada D, Xerri L, et al. Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial. Lancet. 2011;377:42–51.PubMedCrossRef
6.
Zurück zum Zitat Wöhrer S, Jaeger U, Kletter K, Becherer A, Hauswirth A, Turetschek K, et al. 18 F-fluoro-deoxy-glucose positron emission tomography (18 F-FDG-PET) visualizes follicular lymphoma irrespective of grading. Ann Oncol. 2006;17:780–4.PubMedCrossRef Wöhrer S, Jaeger U, Kletter K, Becherer A, Hauswirth A, Turetschek K, et al. 18 F-fluoro-deoxy-glucose positron emission tomography (18 F-FDG-PET) visualizes follicular lymphoma irrespective of grading. Ann Oncol. 2006;17:780–4.PubMedCrossRef
7.
Zurück zum Zitat Trotman J, Fournier M, Lamy T, Seymour JF, Sonet A, Janikova A, et al. Positron emission tomography-computed tomography (PET-CT) after induction therapy is highly predictive of patient outcome in follicular lymphoma: analysis of PET-CT in a subset of PRIMA trial participants. J Clin Oncol. 2011;29:3194–200.PubMedCrossRef Trotman J, Fournier M, Lamy T, Seymour JF, Sonet A, Janikova A, et al. Positron emission tomography-computed tomography (PET-CT) after induction therapy is highly predictive of patient outcome in follicular lymphoma: analysis of PET-CT in a subset of PRIMA trial participants. J Clin Oncol. 2011;29:3194–200.PubMedCrossRef
8.
Zurück zum Zitat Luminari S, Biasoli I, Versari A, Rattotti S, Bottelli C, Rusconi C, et al. The prognostic role of post-induction FDG-PET in patients with follicular lymphoma: a subset analysis from the FOLL05 trial of the Fondazione Italiana Linfomi (FIL). Ann Oncol. 2014;25:442–7.PubMedCrossRef Luminari S, Biasoli I, Versari A, Rattotti S, Bottelli C, Rusconi C, et al. The prognostic role of post-induction FDG-PET in patients with follicular lymphoma: a subset analysis from the FOLL05 trial of the Fondazione Italiana Linfomi (FIL). Ann Oncol. 2014;25:442–7.PubMedCrossRef
9.
Zurück zum Zitat Barrington SF, Mikhaeel NG, Kostakoglu L, Meignan M, Hutchings M, Müeller SP, et al. Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol. 2014. doi:10.1200/JCO.2013.53.5229 Barrington SF, Mikhaeel NG, Kostakoglu L, Meignan M, Hutchings M, Müeller SP, et al. Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol. 2014. doi:10.​1200/​JCO.​2013.​53.​5229
10.
Zurück zum Zitat Dupuis J, Berriolo-Riedinger A, Julian A, Brice P, Tychyj-Pinel C, Tilly H, et al. Impact of [(18)F]fluorodeoxyglucose positron emission tomography response evaluation in patients with high-tumor burden follicular lymphoma treated with immunochemotherapy: a prospective study from the Groupe d’Etudes des Lymphomes de l’Adulte and GOELAMS. J Clin Oncol. 2012;30:4317–22.PubMedCrossRef Dupuis J, Berriolo-Riedinger A, Julian A, Brice P, Tychyj-Pinel C, Tilly H, et al. Impact of [(18)F]fluorodeoxyglucose positron emission tomography response evaluation in patients with high-tumor burden follicular lymphoma treated with immunochemotherapy: a prospective study from the Groupe d’Etudes des Lymphomes de l’Adulte and GOELAMS. J Clin Oncol. 2012;30:4317–22.PubMedCrossRef
11.
Zurück zum Zitat Metzner B, Pott C, Müller TH, Gebauer W, Casper J, Kraemer D, et al. Long-term clinical and molecular remissions in patients with follicular lymphoma following high-dose therapy and autologous stem cell transplantation. Ann Oncol. 2013;24:1609–15.PubMedCrossRef Metzner B, Pott C, Müller TH, Gebauer W, Casper J, Kraemer D, et al. Long-term clinical and molecular remissions in patients with follicular lymphoma following high-dose therapy and autologous stem cell transplantation. Ann Oncol. 2013;24:1609–15.PubMedCrossRef
12.
Zurück zum Zitat Brice P, Simon D, Bouabdallah R, Bélanger C, Haïoun C, Thieblemont C, et al. High-dose therapy with autologous stem-cell transplantation (ASCT) after first progression prolonged survival of follicular lymphoma patients included in the prospective GELF 86 protocol. Ann Oncol. 2000;11:1585–90.PubMedCrossRef Brice P, Simon D, Bouabdallah R, Bélanger C, Haïoun C, Thieblemont C, et al. High-dose therapy with autologous stem-cell transplantation (ASCT) after first progression prolonged survival of follicular lymphoma patients included in the prospective GELF 86 protocol. Ann Oncol. 2000;11:1585–90.PubMedCrossRef
13.
Zurück zum Zitat Schouten HC, Qian W, Kvaloy S, Porcellini A, Hagberg H, Johnsen HE, et al. High-dose therapy improves progression-free survival and survival in relapsed follicular non-Hodgkin’s lymphoma: results from the randomized European CUP trial. J Clin Oncol. 2003;21:3918–27.PubMedCrossRef Schouten HC, Qian W, Kvaloy S, Porcellini A, Hagberg H, Johnsen HE, et al. High-dose therapy improves progression-free survival and survival in relapsed follicular non-Hodgkin’s lymphoma: results from the randomized European CUP trial. J Clin Oncol. 2003;21:3918–27.PubMedCrossRef
14.
Zurück zum Zitat Sebban C, Brice P, Delarue R, Haioun C, Souleau B, Mounier N, et al. Impact of rituximab and/or high-dose therapy with autotransplant at time of relapse in patients with follicular lymphoma: a GELA study. J Clin Oncol. 2008;26:3614–20.PubMedCrossRef Sebban C, Brice P, Delarue R, Haioun C, Souleau B, Mounier N, et al. Impact of rituximab and/or high-dose therapy with autotransplant at time of relapse in patients with follicular lymphoma: a GELA study. J Clin Oncol. 2008;26:3614–20.PubMedCrossRef
15.
Zurück zum Zitat Le Gouill S, De Guibert S, Planche L, Brice P, Dupuis J, Cartron G, et al. Impact of the use of autologous stem cell transplantation at first relapse both in naive and previously rituximab exposed follicular lymphoma patients treated in the GELA/GOELAMS FL2000 study. Haematologica. 2011;96:1128–35.PubMedCentralPubMedCrossRef Le Gouill S, De Guibert S, Planche L, Brice P, Dupuis J, Cartron G, et al. Impact of the use of autologous stem cell transplantation at first relapse both in naive and previously rituximab exposed follicular lymphoma patients treated in the GELA/GOELAMS FL2000 study. Haematologica. 2011;96:1128–35.PubMedCentralPubMedCrossRef
16.
Zurück zum Zitat Laport GG. Changing role of stem cell transplantation in follicular lymphoma. Hematology Am Soc Hematol Educ Program. 2012;2012:417–25.PubMed Laport GG. Changing role of stem cell transplantation in follicular lymphoma. Hematology Am Soc Hematol Educ Program. 2012;2012:417–25.PubMed
17.
Zurück zum Zitat Bachy E, Salles G. Marrow-ablative treatment and autologous stem cell transplantation in follicular NHL. Best Pract Res Clin Haematol. 2011;24:257–70.PubMedCrossRef Bachy E, Salles G. Marrow-ablative treatment and autologous stem cell transplantation in follicular NHL. Best Pract Res Clin Haematol. 2011;24:257–70.PubMedCrossRef
18.
Zurück zum Zitat Montoto S, Corradini P, Dreyling M, Ghielmini M, Kimby E, López-Guillermo A, et al. Indications for hematopoietic stem cell transplantation in patients with follicular lymphoma: a consensus project of the EBMT-Lymphoma Working Party. Haematologica. 2013;98:1014–21.PubMedCentralPubMedCrossRef Montoto S, Corradini P, Dreyling M, Ghielmini M, Kimby E, López-Guillermo A, et al. Indications for hematopoietic stem cell transplantation in patients with follicular lymphoma: a consensus project of the EBMT-Lymphoma Working Party. Haematologica. 2013;98:1014–21.PubMedCentralPubMedCrossRef
19.
Zurück zum Zitat Decaudin D, Mounier N, Tilly H, Ribrag V, Ghesquières H, Bouabdallah K, et al. (90)Y ibritumomab tiuxetan (Zevalin) combined with BEAM (Z -BEAM) conditioning regimen plus autologous stem cell transplantation in relapsed or refractory low-grade CD20-positive B-cell lymphoma. A GELA phase II prospective study. Clin Lymphoma Myeloma Leuk. 2011;11:212–8.PubMedCrossRef Decaudin D, Mounier N, Tilly H, Ribrag V, Ghesquières H, Bouabdallah K, et al. (90)Y ibritumomab tiuxetan (Zevalin) combined with BEAM (Z -BEAM) conditioning regimen plus autologous stem cell transplantation in relapsed or refractory low-grade CD20-positive B-cell lymphoma. A GELA phase II prospective study. Clin Lymphoma Myeloma Leuk. 2011;11:212–8.PubMedCrossRef
20.
Zurück zum Zitat Cheson BD, Horning SJ, Coiffier B, Shipp MA, Fisher RI, Connors JM, et al. Report of an international workshop to standardize response criteria for non-Hodgkin’s lymphomas. NCI Sponsored International Working Group. J Clin Oncol. 1999;17:1244.PubMed Cheson BD, Horning SJ, Coiffier B, Shipp MA, Fisher RI, Connors JM, et al. Report of an international workshop to standardize response criteria for non-Hodgkin’s lymphomas. NCI Sponsored International Working Group. J Clin Oncol. 1999;17:1244.PubMed
21.
Zurück zum Zitat Cheson BD, Pfistner B, Juweid ME, Gascoyne RD, Specht L, Horning SJ, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007;25:579–86.PubMedCrossRef Cheson BD, Pfistner B, Juweid ME, Gascoyne RD, Specht L, Horning SJ, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007;25:579–86.PubMedCrossRef
22.
Zurück zum Zitat Meignan M, Gallamini A, Meignan M, Gallamini A, Haioun C. Report on the First International Workshop on Interim-PET-Scan in Lymphoma. Leuk Lymphoma. 2009;50:1257–60.PubMedCrossRef Meignan M, Gallamini A, Meignan M, Gallamini A, Haioun C. Report on the First International Workshop on Interim-PET-Scan in Lymphoma. Leuk Lymphoma. 2009;50:1257–60.PubMedCrossRef
23.
Zurück zum Zitat Lin C, Itti E, Haioun C, Petegnief Y, Luciani A, Dupuis J, et al. Early 18F-FDG PET for prediction of prognosis in patients with diffuse large B-cell lymphoma: SUV-based assessment versus visual analysis. J Nucl Med. 2007;48:1626–32.PubMedCrossRef Lin C, Itti E, Haioun C, Petegnief Y, Luciani A, Dupuis J, et al. Early 18F-FDG PET for prediction of prognosis in patients with diffuse large B-cell lymphoma: SUV-based assessment versus visual analysis. J Nucl Med. 2007;48:1626–32.PubMedCrossRef
24.
Zurück zum Zitat Peduzzi P, Concato J, Feinstein AR, Holford TR. Importance of events per independent variable in proportional hazards regression analysis. II. Accuracy and precision of regression estimates. J Clin Epidemiol. 1995;48:1503–10.PubMedCrossRef Peduzzi P, Concato J, Feinstein AR, Holford TR. Importance of events per independent variable in proportional hazards regression analysis. II. Accuracy and precision of regression estimates. J Clin Epidemiol. 1995;48:1503–10.PubMedCrossRef
25.
Zurück zum Zitat Moskowitz AJ, Yahalom J, Kewalramani T, Maragulia JC, Vanak JM, Zelenetz AD, et al. Pretransplantation functional imaging predicts outcome following autologous stem cell transplantation for relapsed and refractory Hodgkin lymphoma. Blood. 2010;116:4934–7.PubMedCentralPubMedCrossRef Moskowitz AJ, Yahalom J, Kewalramani T, Maragulia JC, Vanak JM, Zelenetz AD, et al. Pretransplantation functional imaging predicts outcome following autologous stem cell transplantation for relapsed and refractory Hodgkin lymphoma. Blood. 2010;116:4934–7.PubMedCentralPubMedCrossRef
26.
Zurück zum Zitat Juweid ME, Stroobants S, Hoekstra OS, Mottaghy FM, Dietlein M, Guermazi A, et al. Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol. 2007;25:571–8.PubMedCrossRef Juweid ME, Stroobants S, Hoekstra OS, Mottaghy FM, Dietlein M, Guermazi A, et al. Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol. 2007;25:571–8.PubMedCrossRef
27.
Zurück zum Zitat Seymour JF, Trotman J, Hofman MS. Evaluating the place of FDG PET scanning in primary staging and beyond in patients with follicular lymphoma. Leuk Lymphoma. 2013;54:2093–5.PubMedCrossRef Seymour JF, Trotman J, Hofman MS. Evaluating the place of FDG PET scanning in primary staging and beyond in patients with follicular lymphoma. Leuk Lymphoma. 2013;54:2093–5.PubMedCrossRef
28.
Zurück zum Zitat Itti E, Meignan M, Berriolo-Riedinger A, Biggi A, Cashen AF, Véra P, et al. An international confirmatory study of the prognostic value of early PET/CT in diffuse large B-cell lymphoma: comparison between Deauville criteria and ΔSUVmax. Eur J Nucl Med Mol Imaging. 2013;40:1312–20.PubMedCrossRef Itti E, Meignan M, Berriolo-Riedinger A, Biggi A, Cashen AF, Véra P, et al. An international confirmatory study of the prognostic value of early PET/CT in diffuse large B-cell lymphoma: comparison between Deauville criteria and ΔSUVmax. Eur J Nucl Med Mol Imaging. 2013;40:1312–20.PubMedCrossRef
29.
Zurück zum Zitat Itti E, Juweid ME, Haioun C, Yeddes I, Hamza-Maaloul F, El Bez I, et al. Improvement of early 18F-FDG PET interpretation in diffuse large B-cell lymphoma: importance of the reference background. J Nucl Med. 2010;51:1857–62.PubMedCrossRef Itti E, Juweid ME, Haioun C, Yeddes I, Hamza-Maaloul F, El Bez I, et al. Improvement of early 18F-FDG PET interpretation in diffuse large B-cell lymphoma: importance of the reference background. J Nucl Med. 2010;51:1857–62.PubMedCrossRef
30.
Zurück zum Zitat Kothari J, Peggs KS. Bird A, Thomson KJ, Morris E, Virchis AE, et al. Autologous stem cell transplantation for follicular lymphoma is of most benefit early in the disease course and can result in durable remissions, irrespective of prior rituximab exposure. Br J Haematol. 2014;164:334–40.CrossRef Kothari J, Peggs KS. Bird A, Thomson KJ, Morris E, Virchis AE, et al. Autologous stem cell transplantation for follicular lymphoma is of most benefit early in the disease course and can result in durable remissions, irrespective of prior rituximab exposure. Br J Haematol. 2014;164:334–40.CrossRef
31.
Zurück zum Zitat Evens AM, Vanderplas A, LaCasce AS, Crosby AL, Nademanee AP, Kaminski MS, et al. Stem cell transplantation for follicular lymphoma relapsed/refractory after prior rituximab: a comprehensive analysis from the NCCN lymphoma outcomes project. Cancer. 2013;119:3662–71PubMed Evens AM, Vanderplas A, LaCasce AS, Crosby AL, Nademanee AP, Kaminski MS, et al. Stem cell transplantation for follicular lymphoma relapsed/refractory after prior rituximab: a comprehensive analysis from the NCCN lymphoma outcomes project. Cancer. 2013;119:3662–71PubMed
33.
Zurück zum Zitat Westin JR, Chu F, Zhang M, Fayad LE, Kwak LW, Fowler N, et al. Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial. Lancet Oncol. 2014;15:69–77.PubMedCentralPubMedCrossRef Westin JR, Chu F, Zhang M, Fayad LE, Kwak LW, Fowler N, et al. Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial. Lancet Oncol. 2014;15:69–77.PubMedCentralPubMedCrossRef
34.
Zurück zum Zitat Pettengell R, Schmitz N, Gisselbrecht C, Smith G, Patton WN, Metzner B, et al. Rituximab purging and/or maintenance in patients undergoing autologous transplantation for relapsed follicular lymphoma: a prospective randomized trial from the lymphoma working party of the European group for blood and marrow transplantation. J Clin Oncol. 2013;31:1624–30.PubMedCrossRef Pettengell R, Schmitz N, Gisselbrecht C, Smith G, Patton WN, Metzner B, et al. Rituximab purging and/or maintenance in patients undergoing autologous transplantation for relapsed follicular lymphoma: a prospective randomized trial from the lymphoma working party of the European group for blood and marrow transplantation. J Clin Oncol. 2013;31:1624–30.PubMedCrossRef
Metadaten
Titel
PET/CT before autologous stem cell transplantation predicts outcome in refractory/relapsed follicular lymphoma
verfasst von
Marion Alcantara
Jehan Dupuis
Sylvain Mareschal
Anne Julian
Anne Ségolène Cottereau
Stéphanie Becker
Sydney Dubois
Lucie Oberic
Anne Huynh
Michel Meignan
Guy Laurent
Hervé Tilly
Corinne Haioun
Loïc Ysebaert
Publikationsdatum
01.02.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nuclear Medicine and Molecular Imaging / Ausgabe 2/2015
Print ISSN: 1619-7070
Elektronische ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-014-2896-2

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