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Meta-Analysis
. 2025 Mar 26;3(3):CD010533.
doi: 10.1002/14651858.CD010533.pub3.

Positron emission tomography-adapted therapy for first-line treatment in adults with Hodgkin lymphoma

Nina Kreuzberger  1   2 , Marius Goldkuhle  1   2 , Bastian von Tresckow  3   4 , Carsten Kobe  5 , Marie-Therese Sickinger  6 , Ina Monsef  1   2 , Nicole Skoetz  1   2
Affiliations
Meta-Analysis

Positron emission tomography-adapted therapy for first-line treatment in adults with Hodgkin lymphoma

Nina Kreuzberger et al. Cochrane Database Syst Rev. .

Abstract

Background: Hodgkin lymphoma (HL) is one of the most curable cancers worldwide. Treatment options comprise more- or less-intensified regimens of chemotherapy plus radiotherapy depending on the disease stage. An interim-[18F]-fluorodeoxy-D-glucose (FDG)-positron emission tomography (PET), a procedure to illustrate a tumour's metabolic activity, stage and progression, could be used during treatment to distinguish between individuals who are good or poor early responders to therapy. Subsequent therapy could be de-escalated in PET-negative individuals (good responders) or escalated in those who are PET-positive (poor responders).

Objectives: To assess the effects of interim [18F]-FDG-PET-imaging treatment modification in previously untreated individuals with HL.

Search methods: For this review update, we searched MEDLINE, the Cochrane Central Register of Controlled Trials (CENTRAL), Embase, clinicaltrials.gov and the WHO ICTRP up to 17 November 2023.

Selection criteria: We included randomised controlled trials (RCTs) comparing interim-FDG-PET-adapted therapy with non-adapted standard treatment in adults with untreated HL of all stages.

Data collection and analysis: Two review authors independently screened results for inclusion, extracted data into a standardised data extraction sheet and assessed the risk of bias according to the Cochrane risk of bias tool. We collected (modified) intention-to-treat effect estimates for the predefined outcomes: overall survival (OS), progression-free survival (PFS), treatment-related mortality (TRM), adverse events (AE) including secondary malignancies and quality of life (QoL), where available, and used random-effects models for meta-analysis. We analysed early, intermediate and advanced stage HL and PET-negative versus PET-positive participants separately. We used the GRADE approach to rate our certainty in the evidence.

Main results: We included 10 studies covering early (1 RCT, 667 participants), intermediate (1 RCT, 651 participants), early-to-intermediate (3 RCTs, 1639 participants) and advanced-stage HL (5 RCTs; 3629 participants). We did not identify eligible ongoing studies. Generally, the risk of bias was low or, sometimes, unclear except for detection bias, which was rated as high for all studies for subjective outcomes such as PFS, TRM and AE due to the lack of blinding. PET-based adaptation in early-stage PET-negative participants The effect of treatment adaptation (omission of radiotherapy with or without additional chemotherapy) on OS and PFS is uncertain (HR 0.84, 95% CI 0.13 to 5.32; and HR 4.52, 95% CI 0.72 to 28.41, 1034 participants). Adaptation may have little to no effect on the incidence of secondary malignancies (RR 0.83, 95% CI 0.46 to 1.50; 984 participants; low-certainty). No studies reported on TRM, serious adverse events (SAE) or QoL. PET-based adaptation in intermediate-stage PET-negative participants Treatment adaptation by omission of radiotherapy (with or without additional chemotherapy) may have little effect on OS (HR 0.91, 95% CI 0.42 to 1.96; 1073 participants; low-certainty) and PFS (HR 1.59, 95% CI 0.95 to 2.67; 1073 participants; low-certainty) compared to standard therapy. The effect on TRM is very uncertain. De-escalation may have little effect on the incidence of SAE (RR 1.01, 95% CI 0.84 to 1.21; 1096 participants, low-certainty) and secondary malignancies (RR 1.01, 95% CI 0.57 to 1.82; 1515 participants; low-certainty). No studies reported on QoL. PET-based de-escalation in advanced-stage PET-negative participants Three RCTs examined interim-PET-based de-intensification of chemotherapy compared with standard in advanced-stage PET-negative participants; this probably increases OS (HR 0.65, 95% CI 0.40 to 1.07; 2633 participants, moderate-certainty), although the confidence interval included the possibility of no effect, while it has probably little effect on PFS (HR 0.98, 95% CI 0.78 to 1.25; 2633 participants, moderate-certainty). Treatment de-escalation may reduce TRM (RR 0.21, 95% CI 0.06 to 0.73; 2761 participants, low-certainty) and the incidence of secondary malignancy (RR 0.87, 95% CI 0.60 to 1.26; 2757 participants; low-certainty), although for this latter finding, the CI included the possibility of no effect. No studies reported SAE and QoL. Two RCTs considered combined modality treatment as standard for advanced stages and de-escalated by omitting radiotherapy. De-escalation may increase OS (HR 0.63, 95% CI 0.11 to 3.69; 296 participants; low-certainty), PFS (HR 0.78, 95% CI 0.43 to 1.43; 412 participants; low-certainty), and may reduce the incidence of secondary malignancy (RR 0.41, 95% CI 0.08 to 2.09; 349 participants; low-certainty), although for all these findings, the CI included the possibility of no effect. No studies reported TRM, SAE and QoL. PET-based escalation in mixed early-and-intermediate-stage, PET-positive participants One study compared intensified chemotherapy (BEACOPPescalated) and radiotherapy with standard chemotherapy (ABVD) and radiotherapy based on positive interim-PET after two cycles in early-to-intermediate-stage HL. Treatment escalation may increase OS (HR 0.92, 95% CI 0.43 to 1.97; 260 participants; low-certainty) and PFS (0.67, 95% CI 0.37 to 1.20; 260 participants; low-certainty), although the CI included the possibility of no effect. The effect on secondary malignancies is very uncertain (RR 1.23, 95% CI 0.43 to 3.55; 234 participants, very low-certainty). No studies reported TRM, SAE and QoL. PET-based escalation in advanced-stage, PET-positive participants Two studies examined interim-PET-based escalation of PET-positive participants with rituximab in addition to chemotherapy in advanced-stage HL, which likely does not increase OS (HR 1.39, 95% CI 0.74 to 2.63; 795 participants; moderate-certainty) or PFS (HR 1.03, 95% CI 0.68 to 1.54; 582 participants; moderate-certainty). It may increase TRM (RR 4.00, 95% CI 0.45 to 35.5; 434 participants; very low-certainty), although the CI included the possibility of no effect. Escalation probably increases the number of participants with SAE (RR 1.61, 95% CI 1.00 to 2.60; 148 participants, moderate-certainty), and may reduce the number of participants with secondary malignancy (RR 0.67, 95% CI 0.28 to 1.60; 582 participants; low-certainty), although for this latter finding, the CI included the possibility of no effect. No study reported QoL.

Authors' conclusions: In early-stage HL, the effect of interim-PET-based treatment adaptation by omission of radiotherapy is uncertain. No effect was seen on long-term adverse events, although the follow-up of around five years may be too short to see an effect. In intermediate-stage HL, omission of radiotherapy may have little effect on both overall and progression-free survival, serious adverse events and secondary malignancies. In advanced-stage HL, reducing chemotherapy upon negative interim-PET has the potential to increase overall survival while not negatively affecting progression-free survival and long-term adverse events. If combined modality treatment is opted for, omitting radiotherapy may increase both overall and progression-free survival, while reducing the negative effect of radiotherapy on secondary malignancies. Interim-PET-positive treatment intensification by providing more chemotherapy in early-to-intermediate stage HL may be beneficial, while adding rituximab to standard chemotherapy in advanced-stage HL does not result in the expected improvement, but increases adverse events.

Trial registration: ClinicalTrials.gov NCT01358747 NCT00433433 NCT00795613 NCT00784537 NCT00736320 NCT01356680 NCT00515554 NCT00678327 NCT00943423 NCT00025259 NCT01132807 NCT01118026 NCT01712490 NCT03517137 NCT01652261 NCT02661503 NCT03226249 NCT03712202 NCT05922904 NCT04685616 NCT04866654 NCT00822120.

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References

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References to studies excluded from this review

AHOD0031 {published data only}
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CALGB 50604 {published data only}
    1. NCT01132807. Chemotherapy based on positron emission tomography scan in treating patients with stage I or stage II Hodgkin lymphoma. https://clinicaltrials.gov/study/NCT01132807 (first submitted 27 May 2010).
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CALGB50801 {published data only}
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    1. Bartlett NL, Straus DJ, Dlugosz-Danecka M, Alekseev S, Illes A, Lech-Maranda E, et al. Brentuximab Vedotin with chemotherapy for stage 3/4 classical Hodgkin lymphoma (cHL): 4-Year update of the Echelon-1 study. Blood 2019;134 Suppl 1:4026. [DOI: 10.1182/blood-2019-124116] - DOI - PubMed
    1. Connors JM, Jurczak W, Straus DJ, Ansell SM, Kim WS, Center M, et al. Brentuximab vedotin plus doxorubicin, vinblastine, dacarbazine (A+AVD) as frontline therapy demonstrates superior modified progression-free survival versus ABVD in patients with previously untreated stage III or IV Hodgkin lymphoma (HL): the phase 3 Echelon-1 study. Blood 2017;130(Suppl 1):6. [DOI: 10.1182/blood.V130.Suppl_1.6.6] - DOI
    1. Crosswell HE, LaCasce AS, Bartlett NL, Straus DJ, Savage KJ, Zinzani PL, et al. Brentuximab vedotin with chemotherapy in adolescents and young adults (AYAS) with stage III or IV Hodgkin lymphoma: a subgroup analysis from the phase 3 ECHELON-1 study. Hematological Oncology 2021;39 Suppl 2:76-7. [DOI: 10.1002/hon.2879] - DOI
EORTC‐COBRA {published data only}
    1. Diepstra A, Visser L, Fortpied C, Noordzij W, Loft A, Arens A, et al. FDG-PET and serum Tarc levels after one cycle of Bv-AVD in advanced stage Hodgkin lymphoma patients: results from the very early PET-response adapted EORTC-COBRA trial. HemaSphere 2022;6 Suppl 5:1.
    1. NCT03517137. Very early PET-response adapted targeted therapy for advanced Hodgkin lymphoma: a single -arm phase II study. https://clinicaltrials.gov/study/NCT03517137 (first submitted 24 April 2018).
FIL {published data only}
    1. EUCTR2016-002509-21-IT. A randomized, open-label, multicenter, phase III, 2-arm study comparing efficacy and tolerability of the intensified variant ‘dose-dense/dose-intense ABVD’ (ABVD DD-DI) with an interim PET response-adapted ABVD program as upfront therapy in advanced-stage classical Hodgkin Lymphoma (HL) [Studio randomizzato, open-label, multicentrico, di fase III a 2 bracci di confronto dell’efficacia e della tollerabilità della variante intensificata ‘dose-dense/dose-intense ABVD’ (ABVD DD-DI) e un programma terapeutico con ABVD a dosi standard per 2 cicli e successivamente orientato in base alla risposta PET, come trattamento di prima linea di pazienti con Linfoma di Hodgkin classico (HL) in stadio avanzato]. https://www.clinicaltrialsregister.eu/ctr-search/trial/2016-002509-21/IT (first posted 2017).
    1. NCT03159897. FIL study on ABVD DD-DI as upfront therapy in HL. https://clinicaltrials.gov/show/NCT03159897 (first submitted 18 May 2017).
GATLA LH‐05 {published data only}
    1. Ciliberti E, Fernandez I, Kurgansky N, Prates V, Zoppegno L, Negri P, et al. Safety and efficacy analysis of elderly patients treated within the GATLA HL-05 clinical trial: PET adapted therapy after 3 cycles of ABVD for all stages of Hodgkin lymphoma. Hematological Oncology 2017;35 Suppl 2:168-9. [DOI: 10.1002/hon.2438] - DOI
    1. Iorio J, Eleta M, Plates V, Fiad L, Riddick M, Pavlovsky A. MTV, TLG and Suv max as promising parameters to predict early response in patients with HL treated with ABVD. A retrospective sub-analysis of the GATLA LH-05 trial. Hematological Oncology 2021;39 Suppl 2:283-4. [DOI: 10.1002/hon.2880] - DOI
    1. Pavlovsky A, Fernandez I, Kurgansky N, Prates V, Zoppegno L, Negri P, et al. PET-CT adapted therapy after 3 cycles of ABVD to all stages of Hodgkin lymphoma. GATLA trial HL-05. Haematologica 2016;101 Suppl 1:5. [PMID: ] - PubMed
    1. Pavlovsky A, Fernandez I, Kurgansky N, Prates V, Zoppegno L, Negri P, et al. PET-adapted therapy after three cycles of ABVD for all stages of Hodgkin lymphoma: results of the GATLA LH-05 trial. British Journal of Haematology 2019;185(5):865-73. [DOI: 10.1111/bjh.15838] - DOI - PubMed
    1. Pavlovsky A, Fiad L, Fernandez I, Prates V, Kurgansky N, Cerutti A, et al. PET-adapted therapy after three cycles of ABVD for all stages of Hodgkin lymphoma: long term follow up of the GATLA Lh-05 trial. Hematological Oncology 2021;39 Suppl 3:276-7. [DOI: 10.1002/hon.2880] - DOI
H11 {published data only}2011‐005473‐22
    1. NCT01652261. Very early FDG-PET/CT-response adapted therapy for advanced Hodgkin lymphoma (H11). https://clinicaltrials.gov/search?term=NCT01652261 (first received 2012).
HD15 {published data only}
    1. Buerkle C, Goergen H, Muller H, Brockelmann P, Kreissl S, Fuchs M, et al. Patient preferences - survey of Hodgkin lymphoma survivors on treatment-associated burden and side effects. Haematologica 2016;101 Suppl 1:146-7.
    1. Eich HT, Kobe C, Dietlein M, Kriz J, Haverkamp H, Fuchs M, et al. Role of radiotherapy after assessment of residual bulky tumor using FDG-PET in patients with advanced-stage Hodgkin lymphoma: final report of the GHSG HD15 trial. International Journal of Radiation Oncology, Biology, Physics 2011;1:2-3.
    1. Eich HT, Kobe C, Kriz J, Baues C, Haverkamp H, Fuchs M, et al. Assessment of residual bulky tumor using FDG-PET in patients with advanced-stage Hodgkin Lymphoma after completion of chemotherapy: final report of the GHSG HD15 trial. Strahlentherapie und Onkologie 2011;1:48. [DOI: 10.1007/s00066-011-1001-z] - DOI
    1. Eich HT, Kriz J, Reinartz G, Kobe C, Kuhnert G, Haverkamp U, et al. Relapse analysis after radiation therapy of PET-positive residual tumors of patients with advanced stage Hodgkin lymphoma treated in the HD15 trial of the German Hodgkin Study Group (GHSG). International Journal of Radiation Oncology, Biology, Physics 2013;1:5-6. [DOI: 10.1016/j.ijrobp.2013.06.021] - DOI
    1. Eichenauer DA, Haverkamp H, Behringer K, Halbsguth T, Fuchs M, Diehl V, et al. Secondary MDS/AML in Hodgkin lymphoma patients treated within German Hodgkin Study Group (GHSG) clinical trials after introduction of the BEACOPP protocol. Blood 2010;116:21. [PMID: ]
HD21 {published data only}ACTRN12617000087358
    1. ACTRN12617000087358. Treatment optimisation trial in the first-line treatment of advanced stage Hodgkin lymphoma: comparison of 6 cycles of escalated BEACOPP with 6 cycles of BrECADD. https://anzctr.org.au/Trial/Registration/TrialReview.aspx?ACTRN=ACTRN126... (date submitted 12 June 2016).
    1. Borchmann P, Moccia A, Greil R, Herzberg M, Fossa A, Huttmann A, et al. Treatment related morbidity in patients with classical Hodgkin lymphoma: results of the ongoing, randomized phase III HD21 trial by the German Hodgkin Study Group. HemaSphere 2022;6 Suppl 5:1-2. [PMID: ]
    1. Greil R, Melchardt T. HD21 Treatment optimization trial in the first-line treatment of advanced-stage Hodgkin lymphoma: comparison of 6 cycles of escalated BEACOPP with 6 cycles of BrECADD. Magazine of European Medical Oncology 2017;10 Suppl 1:39-40. [PMID: ]
    1. Greil R. GHSG-HD21: treatment optimization trial in the first-line treatment of advanced stage Hodgkin lymphoma: comparison of 4-6 cycles of escalated BEACOPP with 4-6 cycles of BrECADD. Magazine of European Medical Oncology 2022;15:S61. [PMID: ]
    1. NCT02661503. HD21 for advanced stages. https://clinicaltrials.gov/study/NCT02661503 (first submitted 19 January 2016).
JCOG1305 {published data only}
    1. UMIN000019868. JCOG1305: Interim response adapted strategy for the advanced stage of Hodgkin Lymphoma. https://jrct.niph.go.jp/latest-detail/jRCTs031180218 (date of registration 8 March 2019).
NCT03226249 {published data only}
    1. Allen PB, Lu X, Chen Q, O'Shea K, Chmiel JS, Slonim LB, et al. Sequential pembrolizumab and AVD are highly effective at any PD-L1 expression level in untreated Hodgkin lymphoma. Blood Advances 2023;7(12):2570-6. [DOI: 10.1182/bloodadvances.2022008116] - DOI - PMC - PubMed
    1. Allen PB, Savas H, Evens AM, Advani R, Palmer B, Pro B, et al. Pembrolizumab followed by AVD in untreated early unfavorable and advanced stage classical Hodgkin lymphoma. Blood 2020;137(10):1318-26. [DOI: 10.1182/blood.2020007400] - DOI - PMC - PubMed
    1. NCT03226249. PET-directed therapy with pembrolizumab and combination chemotherapy in treating patients with previously untreated classical Hodgkin lymphoma. https://ClinicalTrials.gov/show/NCT03226249 (first submitted 19 July 2017).
NCT03712202 {published data only}
    1. NCT03712202. Brentuximab vedotin and nivolumab in treating participants with early stage classic Hodgkin lymphoma. https://clinicaltrials.gov/show/NCT03712202 (first submitted 6 August 2018).
NCT05922904 {published data only}
    1. NCT05922904. PET adapted brentuximab vedotin and pembrolizumab in combination with doxorubicin and dacarbazine in classic Hodgkin lymphoma. https://classic.clinicaltrials.gov/show/NCT05922904 (first submitted 28 June 2023).
RADAR {published data only}
    1. NCT04685616. Brentuximab vedotin in early stage Hodgkin lymphoma. https://clinicaltrials.gov/show/NCT04685616 (first submitted 27 November 2020).
    1. Radford J, Adedayo T, Ardavan A, Barrington SF, Berkahn L, Chauvie S, et al. RADAR: an international phase III, PET response adapted, randomised trial in progress, comparing ABVD +/- LSRT with brentuximab vedotin +AVD +/- LSRT in patients with previously untreated limited-stage classical Hodgkin lymphoma. HemaSphere 2022;6 Suppl 5:12-3.
RAFTING {published data only}
    1. Bergesio F, Meignan M, Cottereau AS, Guerra L, Versari A, Maggi AD, et al. An example of prospective application of imaging biomarker: set-up of the first worldwide prospective phase III Onco-Hematological clinical trial using TMTV for patient stratification. Physica Medica 2022;104 Suppl 1:126-7.
    1. Gallamini 2023. Revisiting the predictive role of 18F-fluorodeoxyglucose positron emission tomography/computerized tomography on treatment outcome in early-stage favorable Hodgkin lymphoma. Hematological Oncology 2023;441(4):608-11. [DOI: 10.1002/hon.3158] - DOI - PubMed
    1. Gallamini A, Picardi M, Filonenko K, Gotti M, Cespedes JN, Rossi A, et al. Radiation-free therapy as the initial treatment of good-prognosis early non-bulky Hodgkin lymphoma, defined by a low metabolic tumor volume and a negative PET-2 - RAFTING trial. HemaSphere 2022;6 Suppl 5:10-1. [PMID: ]
    1. NCT04866654. Radiation free chemotherapy for early Hodgkin lymphoma. https://ClinicalTrials.gov/show/NCT04866654 (first submitted 22 April 2021).
SWOG S0816 {published data only}
    1. Danilov AV, Li H, Press OW, Shapira I, Swinnen LJ, Noy A, et al. Feasibility of interim PET-adapted therapy in HIV-positive patients with advanced Hodgkin lymphoma (HL): sub-analysis of SWOG S0816 phase 2 trial. Blood 2015;126(23):1498. [PMID: ] - PMC - PubMed
    1. Danilov AV, Li H, Press OW, Shapira I, Swinnen LJ, Noy A, et al. Feasibility of interim positron emission tomography (PET)-adapted therapy in HIV-positive patients with advanced Hodgkin lymphoma (HL): a sub-analysis of SWOG S0816 Phase 2 trial. Leukemia & Lymphoma 2017;58(2):461-5. [PMID: ] - PMC - PubMed
    1. NCT00822120. S0816 Fludeoxyglucose F 18-PET/CT imaging and combination chemotherapy with or without additional chemotherapy and G-CSF in treating patients with stage III or stage IV Hodgkin lymphoma. https://ClinicalTrials.gov/show/NCT00822120 (first submitted 13 January 2009).
    1. Press OW, LeBlanc M, Rimsza LM, Schoder H, Friedberg JW, Evens AM, et al. A phase II trial of response-adapted therapy of stages III-IV Hodgkin lymphoma using early interim FDG-PET imaging: US Intergroup S0816. Hematological Oncology 2013;1:137-8. [DOI: 10.1002/hon.2057] - DOI
    1. Press OW, Li H, Schoder H, Straus DJ, Moskowitz CH, LeBlanc M, et al. US intergroup trial of response-adapted therapy for stage III to IV Hodgkin lymphoma using early interim fluorodeoxyglucose-positron emission tomography imaging: Southwest Oncology Group S0816. Journal of Clinical Oncology 2016;34(17):2020-7. [PMID: ] - PMC - PubMed

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