Review ArticleContinuing Education

Response Assessment Criteria and Their Applications in Lymphoma: Part 2

Mateen C. Moghbel, Erik Mittra, Andrea Gallamini, Ryan Niederkohr, Delphine L. Chen, Katherine Zukotynski, Helen Nadel and Lale Kostakoglu
Journal of Nuclear Medicine January 2017, 58 (1) 13-22; DOI: https://doi.org/10.2967/jnumed.116.184242

Article Figures & Data

Tables

  • TABLE 1

    Studies Investigating Predictive Ability of Interim PET Imaging in HL

    Results
    StudyPatient populationCycles completed before imagingPET+PET−
    Gallamini, 2007 (17)190 advanced-HL patients2 (ABVD)2-y PFS: 12.8%2-y PFS: 95.0%
    Cerci, 2010 (18)115 advanced-HL patients2 (ABVD)3-y EFS: 53.4%3-y EFS: 90.5%
    Barnes, 2011 (15)96 limited-HL patients2–4 (ABVD)4-y PFS: 87%*4-y PFS: 91%*
    Le Roux, 2011 (13)90 patients with HL (45 limited, 45 advanced)4 (ABVD)2-y PFS: 16%2-y PFS: 95%
    Straus, 2011 (49)99 limited-HL patients2 (doxorubicin, vinblastine, gemcitabine)2-y PFS: 54%2-y PFS: 88%
    Kostakoglu, 2012 (20)88 limited-HL patients2 (doxorubicin, vinblastine, gemcitabine)2-y PFS: 54% (IHP), 46% (D5PS), 62% (CT)2-y PFS: 88% (IHP), 87% (D5PS), 91% (CT)
    Markova, 2012 (14)69 advanced-HL patients4 (escalated BEACOPP)4-y PFS: 78%4-y PFS: 96%
    Biggi, 2013 (6)260 advanced-HL patients2 (ABVD)3-y FFS: 28%3-y FFS: 95%
    Filippi, 2013 (16)80 limited-HL patients2 (ABVD)3-y PFS: 100%*3-y PFS: 97%*
    Gallamini, 2014 (7)207 advanced-HL patients2 (ABVD)3-y PFS: 28%3-y PFS: 95%
    Hutchings, 2014 (12)126 HL patients (68 limited, 58 advanced)1–2 (ABVD)2-y PFS: 38.5% (PET-1), 23.1% (PET-2)2-y PFS: 98.3% (PET-1), 90.2% (PET-2)
    Oki, 2014 (19)229 HL patients (138 limited, 91 advanced)2–3 (ABVD)3-y PFS: 76.9% (limited), 20.0% (limited, bulky), 44.4% (advanced)3-y PFS: 95.9% (limited), 83.3% (limited, bulky), 71.0% (advanced)
    Rossi, 2014 (50)59 HL patients (22 limited, 37 advanced)2 (anthracycline-based chemotherapy)4-y PFS: 45%4-y PFS: 81%

    • ↵* Nonsignificant.

    • IHP = International Harmonization Project criteria; FFS = failure-free survival.

  • TABLE 2

    Studies Investigating Response-Adapted Therapy in HL

    Results
    StudyPatient populationMethodologyPET+PET−
    Gallamini, 2011 (51)165 HL patients (78 limited, 87 advanced)PET-2 (ABVD); PET− completed 6 more cycles; PET+ escalated to 4 cycles of BEACOPP, 4 cycles BEACOPP2-y FFS: 65%2-y FFS: 92%
    Raemaekers, 2014 (26)1,137 early-HL patients (444 favorable, 693 unfavorable)PET-2 (ABVD); PET− completed 2 more cycles if favorable, 4 more cycles if unfavorable; PET+ escalated to 2 cycles BEACOPP, radiotherapyNANA
    Casasnovas, 2015 (23)782 advanced/bulky-HL patientsPET-2 (BEACOPP); PET− deescalated to 4 cycles ABVD; PET+ completed 4 more cycles; controls completed 6 cycles BEACOPP2-y PFS: 72.9%2-y PFS: 92.8%
    Ganesan, 2015 (22)50 advanced/bulky-HL patientsPET-2 (ABVD); PET− completed 4 more cycles; PET+ escalated to 4 cycles BEACOPP2-y EFS: 50%2-y EFS: 82%
    Radford, 2015 (25)602 limited-HL patientsPET-3 (ABVD); PET− underwent radiotherapy or no therapy; PET+ completed 1 more cycle or radiotherapyPFS: 87.6%PFS: 92.3% (radiotherapy), 88.6% (no radiotherapy)
    Straus, 2015 (52)164 limited-HL patientsPET-2 (ABVD); PET− completed 2 more cycles; PET+ escalated to 2 cycles BEACOPP, radiotherapy3-y PFS: 66%3-y PFS: 92%
    Press, 2016 (24)358 advanced-HL patientsPET-2 (ABVD); PET− completed 2 more cycles; PET+ escalated to 6 cycles BEACOPP2-y PFS: 64%2-y PFS: 82%
    Zinzani, 2016 (53)519 advanced-HL patientsPET-2 (ABVD); PET− completed 4 more cycles; PET+ escalated to salvage therapy, ASCT2-y PFS: 76%2-y PFS: 81%

    • FFS = failure-free survival; NA = not applicable; EFS = event-free survival.

  • TABLE 3

    Studies Investigating Predictive Ability of Interim PET Imaging in NHL

    Results
    StudyPatient populationCycles completed before imagingPET+PET−
    Lin, 2007 (54)92 DLBCL patients (11 limited, 81 advanced)2 (CHOP, R-CHOP, ACVBP, R-ACVBP)2-y EFS: 51%2-y EFS: 79%
    Casasnovas, 2011 (55)102 NHL patients2–4 (R-ACVBP, R-CHOP)2-y PFS: 73% (IHP), 79% (D5PS)2-y PFS: 77% (IHP), 88% (D5PS)
    Cashen, 2011 (56)50 advanced-DLBCL patients2 (R-CHOP)2-y EFS: 63%2-y EFS: 85%
    Yang, 2011 (57)161 DLBCL patients (94 limited, 67 advanced)3–4 (R-CHOP)3-y PFS: 52.5%3-y PFS: 88.3%
    Yoo, 2011 (28)155 DLBCL patients (68 limited, 87 advanced)2–4 (R-CHOP)3-y PFS: 66%*3-y PFS: 84%*
    Dupuis, 2012 (33)121 follicular lymphoma patients4 (R-CHOP)2-y PFS: 61%2-y PFS: 86%
    Pregno, 2012 (29)88 DLBCL patients (29 limited, 59 advanced)2–4 (R-CHOP)2-y PFS: 72%*2-y PFS: 85%*
    Safar, 2012 (58)112 DLBCL patients (21 limited, 91 advanced)2 (R-CHOP, R-ACVBP)3-y PFS: 47%3-y PFS: 84%
    Itti, 2013 (59)114 DLBCL patients2 (rituximab)3-y PFS: 59%3-y PFS: 81%
    Carr, 2014 (60)61 DLBCL patients (24 limited, 37 advanced)2–3 (R-CHOP)2-y EFS: 58%; 2-y OS: 72%2-y EFS: 90%; 2-y OS: 93%
    Khong, 2014 (31)24 natural killer/T-cell lymphoma patients2 −3 (SMILE)2-y PFS: 17%; 2-y OS: 17%2-y PFS: 62%; 2-y OS: 81%
    Nols, 2014 (61)73 DLBCL patients (23 limited, 50 advanced)3–4 (R-CHOP, ACVBP)PFS: 47% (D5PS)PFS: 84% (D5PS)
    Huang, 2015 (30)32 DLBCL patients (9 limited, 23 advanced)2 (R-CHOP)2-y PFS: 82%*2-y PFS: 88%*
    Fukumoto, 2015 (32)79 natural killer/T-cell lymphoma patients2–45-y PFS: 9.2%5-y PFS: 66%
    Mamot, 2015 (8)138 DLBCL patients (64 limited, 74 advanced)2 (R-CHOP)2-y EFS: 48%; 2-y OS: 88%*2-y EFS: 74%; 2-y OS: 91%*

    • ↵* Nonsignificant.

    • ACVBP = adriamycin, cyclophosphamide, vindesine, bleomycin, and prednisone; R-ACVBP = rituximab, adriamycin, cyclophosphamide, vindesine, bleomycin, and prednisone; EFS = event-free survival; IHP = International Harmonization Project criteria; SMILE = dexamethasone, methotrexate, ifosfamide, l-asparaginase, and etoposide; OS = overall survival.

  • TABLE 4

    Studies Investigating Response-Adapted Therapy in NHL

    Results
    StudyPatient populationMethodologyPET+PET−
    Moskowitz, 2006 (62)87 bulky/advanced-DLBCL patientsPET-4 (R-CHOP); PET− and PET+/biopsy− completed 3 cycles ICE; PET+/biopsy+ completed 3 cycles ICE, high-dose chemotherapy, ASCTEFS: 87%*EFS: 91%*
    Kasamon, 2009 (63)59 patients (56 DLBCL, 10 primary mediastinal large B-cell lymphoma, 2 follicular lymphoma, 1 peripheral T-cell; 20 limited, 39 advanced)PET-2 or PET-3; PET− completed standard therapy; PET+ escalated to salvage chemotherapy, ASCT2-y EFS: 67%2-y EFS: 89%
    Moskowitz, 2010 (64)98 DLBCL patients (15 limited/bulky, 83 advanced)PET-4 (R-CHOP); PET− and PET+/biopsy− completed 3 cycles ICE; PET+/biopsy+ completed 3 cycles ICE, high-dose chemotherapy, ASCTPFS: 60% (biopsy+), 79% (biopsy−)PFS: 86%
    Swinnen, 2012 (65)78 bulky/advanced-DLBCL patientsPET-3 or PET-4 (R-CHOP); PET− completed 2 more cycles; PET+ escalated to 4 cycles R-ICE2-y PFS: 45%2-y PFS: 77%
    Sehn, 2014 (66)155 DLBCL patients (50 limited, 105 advanced)PET-4 (R-CHOP); PET− completed 2 more cycles; PET+ escalated to 4 cycles R-ICE4-y PFS: 59%; 4-y OS: 73%4-y PFS: 91%; 4-y OS: 96%
    Swinnen, 2015 (67)80 DLBCL patients (8 limited, 72 advanced)PET-3 or PET-4 (R-CHOP); PET− completed 2 more cycles; PET+ escalated to 4 cycles R-ICE2-y PFS: 42%; 3-y OS: 69%2-y PFS: 76%; 3-y OS: 93%

    • ↵* Nonsignificant.

    • ICE = ifosfamide, carboplatin, etoposide; EFS = event-free survival; R-ICE = rituximab, ifosfamide, carboplatin, and etoposide; OS = overall survival.

  • TABLE 5

    Studies Investigating Predictive Ability of End-of-Treatment PET Imaging in HL

    Results
    StudyPatient populationTreatment regimenPET+PET−
    Spaepen, 2001 (68)60 HL patients (25 limited, 35 advanced)Stanford V, MOPP/ABV2-y PFS: 0%2-y PFS: 91%
    Weihrauch, 2001 (69)28 HL patients (10 limited, 18 advanced/relapsed)Nonuniform1-y DFS: 40%1-y DFS: 95%
    Kobe, 2008 (70)817 bulky/advanced-HL patients6–8 cycles (BEACOPP)2-y PFS: 86%2-y PFS: 96%
    Barnes, 2011 (15)96 limited-HL patients4 cycles (ABVD)4-y PFS: 54%4-y PFS: 94%
    Kobe, 2014 (21)739 advanced-HL patients6–8 cycles (BEACOPP)4-y PFS: 86.1%4-y PFS: 91.5%

    • MOPP/ABV = mechlorethamine, vincristine, procarbazine, prednisone, adriamycin, bleomycin, and vinblastine; DFS = disease-free survival.

  • TABLE 6

    Studies Investigating Predictive Ability of End-of-Treatment PET Imaging in NHL

    Results
    StudyPatient populationTreatment regimenPET+PET−
    Bishu, 2007 (71)31 FL patientsNonuniformMedian PFS: 5.8 moMedian PFS: 29.5 mo
    Zinzani, 2007 (72)45 FL patients6 cycles (R-FM, R-CHOP)2-y PFS: 20%2-y PFS: 90%
    Itti, 2009 (73)80 DLBCL patients (10 limited, 70 advanced)4 cycles (CHOP, R-CHOP, ACVBP/ACE, R-ACVBP)2-y EFS: 25%2-y EFS: 82%
    Le Dortz, 2010 (74)45 FL patients6 cycles (R-CHOP)Median PFS: 17.2 moMedian PFS: 48.0 mo
    Trotman, 2011 (9)122 FL patients (14 limited, 108 advanced)6 cycles (R-CHOP), 8 cycles (R-CVP)42-mo PFS: 32.9%42-mo PFS: 70.7%
    Dupuis, 2012 (33)121 FL patients6 cycles (R-CHOP)2-y PFS: 51%2-y PFS: 87%
    Pregno, 2012 (29)88 DLBCL patients (29 limited, 59 advanced)2–4 cycles (R-CHOP)2-y PFS: 64%2-y PFS: 83%
    Mato, 2012 (75)148 mantle cell lymphoma patientsR-HyperCVAD, rituximab-cytarabine/methotrexateMedian PFS: 11.1 mo; median OS: 56.9 moMedian PFS: not reached; median OS: not reached
    Zinzani, 2013 (76)142 intermediate- to high-risk FL patients6 cycles (R-FM)5-y PFS: 42%5-y PFS: 76%
    Khong, 2014 (31)24 natural killer/T-cell lymphoma patients6 cycles (SMILE)2-y PFS: 0%; 2-y OS: 0%2-y PFS: 68%; 2-y OS: 91%
    Lu, 2014 (39)47 indolent-FL patients6 cycles (R-CHOP)Median OS: 45.0 moMedian OS: 95.2 mo
    Luminari, 2014 (77)202 FL patients8 cycles (R-CVP), 6 cycles (R-CHOP, R-FM)3-y PFS: 35%3-y PFS: 66%
    Martelli, 2014 (78)115 PMLBCL patientsRituximab, anthracycline5-y PFS: 68%; 5-y OS: 83%5-y PFS: 99%; 5-y OS: 100%
    Tychyj-Pinel, 2014 (79)119 FL patients6 cycles (R-CHOP), 8 cycles (R-CVP)42-mo PFS: 25.0%42-mo PFS: 61.4%
    Priel, 2015 (40)33 Burkitt lymphoma patients6 cycles (GMALL B-ALL/NHL 2002 protocol)3-y OS: 30%3-y OS: 90%

    • FL = follicular lymphoma; R-FM = rituximab, fludarabine, and mitoxantrone; PMLBCL = primary mediastinal large B-cell lymphoma; ACVBP/ACE = adriamycin, cyclophosphamide, vindesine, bleomycin, prednisone/adriamycin, cyclophosphamide, etoposide; R-ACVBP = rituximab, adriamycin, cyclophosphamide, vindesine, bleomycin, and prednisone; EFS = event-free survival; R-CVP = rituximab, cyclophosphamide, vincristine, prednisone; R-HyperCVAD = rituximab, cyclophosphamide, doxorubicin, vincristine, dexamethasone alternating with cytarabine, and methotrexate; OS = overall survival; SMILE = dexamethasone, methotrexate, ifosfamide, l-asparaginase, and etoposide; GMAL B-ALL/NHL 2002 protocol = rituximab, high-dose methotrexate, high-dose cytosine arabinoside, cyclophosphamide, etoposide, iphosphamide, corticosteroid, triple-intrathecal therapy.

  • TABLE 7

    Studies Investigating Predictive Ability of Pretransplant PET Imaging

    Results
    StudyPatient populationPET acquisitionPET+PET−
    Schot, 2006 (46)39 patients (11 HL, 28 NHL)Before second-line chemotherapy, 2 cycles into treatment, and before ASCT2-y PFS: 27% (PET-2), 18% (PET-3)2-y PFS: 71% (PET-2), 60% (PET-3)
    Svoboda, 2006 (80)50 patients (19 HL, 31 NHL)After 2 cycles of salvage chemotherapy and before ASCTMedian PFS: 5 moMedian PFS: 19 mo
    Filmont, 2007 (47)60 patients (10 HL, 50 NHL)After consolidative chemotherapy and before ASCT1-y EFS: 43% (pre-ASCT), 25% (post-ASCT)1-y EFS: 80% (pre-ASCT), 81% (post-ASCT)
    Jabbour, 2007 (81)211 HL patientsAfter high-dose chemotherapy and before ASCT3-y PFS: 23%; 3-y OS: 58%3-y PFS: 69%; 3-y OS: 87%
    Crocchiolo, 2008 (82)53 patients (14 HL, 39 NHL)Before ASCT3-y PFS: 55%; 5-y OS: 55%3-y PFS: 79%; 5-y OS: 90%
    Dickinson, 2010 (83)39 DLBCL patientsBefore ASCT3-y PFS: 35%3-y PFS: 81%
    Moskowitz, 2010 (84)153 HL patientsAfter ICE-based salvage chemotherapy and high-dose chemotherapy, and before/after ASCT5-y EFS: 31%5-y EFS: 75%
    Qiao, 2010 (48)31 NHL patientsBefore/after ASCT1-y PFS: 28.6% (pre-ASCT), 23.1% (post-ASCT)1-y PFS: 88.2% (pre-ASCT), 88.9% (post-ASCT)
    Mocikova, 2011 (85)76 HL patientsAfter salvage chemotherapy and before ASCT2-y PFS: 36.1%; 2-y OS: 61.4%2-y PFS: 72.7%; 2-y OS: 90.3%
    Moskowitz, 2012 (86)97 HL patientsAfter salvage chemotherapyEFS: 28.6%EFS: > 80%
    Cohen, 2013 (87)29 mantle cell lymphoma patientsBefore ASCT2-y PFS: 64%; 2-y OS: 60%2-y PFS: 87%; 2-y OS: 100%

    • EFS = event-free survival; OS = overall survival.

Additional Files

Back to top

In this issue

Print
Download PDF
Article Alerts
Email Article
Citation Tools
Bookmark this article

Jump to section

Keywords