Top

European Journal of Nuclear Medicine and Molecular Imaging

Published in:

Open Access 06-08-2022 | Lymphoma | Original Article

The value of FDG PET/CT imaging in outcome prediction and response assessment of lymphoma patients treated with immunotherapy: a meta-analysis and systematic review

Authors: Zahra Kiamanesh, Narjess Ayati, Ramin Sadeghi, Eliza Hawkes, Sze Ting Lee, Andrew M. Scott

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 13/2022

Abstract

Purpose

Treatment strategies of lymphoid malignancies have been revolutionized by immunotherapy. Because of the inherent property of Hodgkin lymphoma and some subtypes of non-Hodgkin lymphoma as a highly FDG-avid tumor, functional ¹⁸F-FDG PET/CT imaging is already embedded in their routine care. Nevertheless, the question is whether it is still valuable in the context of these tumors being treated with immunotherapy. Herein, we will review the value of ¹⁸F-FDG PET/CT imaging lymphoid tumors treated with immunotherapy regimens.

Methods

A comprehensive literature search of the PubMed database was conducted on the value of the ¹⁸F-FDG PET/CT for immunotherapy response monitoring of patients with malignant lymphoma. The articles were considered eligible if they met all of the following inclusion criteria: (a) clinical studies on patients with different types of malignant lymphoma, (b) treatment with anti-CD20 antibodies, immune checkpoint inhibitors or immune cell therapies, (c) and incorporated PET/CT with ¹⁸F-FDG as the PET tracer.

Results

From the initial 1488 papers identified, 91 were ultimately included in our study. In anti-CD20 therapy, the highest pooled hazard ratios (HRs) of baseline, early, and late response monitoring parameters for progression-free survival (PFS) belong to metabolic tumor volume (MTV) (3.19 (95%CI: 2.36–4.30)), maximum standardized uptake value (SUVmax) (3.25 (95%CI: 2.08–5.08)), and Deauville score (DS) (3.73 (95%CI: 2.50–5.56)), respectively. These measurements for overall survival (OS) were MTV (4.39 (95%CI: 2.71–7.08)), DS (3.23 (95%CI: 1.87–5.58)), and DS (3.64 (95%CI: 1.40–9.43)), respectively. Early and late ¹⁸F-FDG PET/CT response assessment in immune checkpoint inhibitors (ICI) and immune cell therapy might be an effective tool for prediction of clinical outcome.

Conclusion

For anti-CD20 therapy of lymphoma, the MTV as a baseline ¹⁸F-FDG PET/CT-derived parameter has the highest HRs for PFS and OS. The DS as visual criteria in early and late response assessment has higher HRs for PFS and OS compared to the international harmonization project (IHP) visual criteria in anti-CD20 therapy. Early changes in ¹⁸F-FDG PET parameters may be predictive of response to ICIs and cell therapy in lymphoma patients.

Available only for authorised users

Vassilakopoulos TP, Chatzidimitriou C, Asimakopoulos JV, Arapaki M, Tzoras E, Angelopoulou MK, et al. Immunotherapy in Hodgkin lymphoma: present status and future strategies. Cancers (Basel). 2019;11(8):1071. https://doi.org/10.3390/cancers11081071.CrossRef

Lopci E, Meignan M. Current evidence on PET response assessment to immunotherapy in lymphomas. PET Clin. 2020;15:23–34. https://doi.org/10.1016/j.cpet.2019.08.011.PubMedCrossRef

Lin N, Song Y, Zhu J. Immune checkpoint inhibitors in malignant lymphoma: advances and perspectives. Chin J Cancer Res. 2020;32:303–18. https://doi.org/10.21147/j.issn.1000-9604.2020.03.03.PubMedPubMedCentralCrossRef

Rituximab (marketed as Rituxan) Information. U.S. Food and Drug Administration website. https://www.fda.gov/drugs/postmarket-drug-safety-information-patients-and-providers/rituximab-marketed-rituxan-information. Updated July 23, 2015. Accessed Aug 28, 2021.

Obinutuzumab. U.S. Food and Drug Administration website. https://www.fda.gov/drugs/resources-information-approved-drugs/obinutuzumab. Updated Feb 26, 2016. Accessed Aug 28, 2021.

Zelenetz AD, Salles G, Mason KD, Casulo C, Le Gouill S, Sehn LH, et al. Venetoclax plus R- or G-CHOP in non-Hodgkin lymphoma: results from the CAVALLI phase 1b trial. Blood. 2019;133:1964–76. https://doi.org/10.1182/blood-2018-11-880526.PubMedPubMedCentralCrossRef

Pembrolizumab (Keytruda) 5–10–2017. U.S. Food and Drug Administration website. https://www.fda.gov/drugs/resources-information-approved-drugs/pembrolizumab-keytruda-5-10-2017. Updated May 11, 2017. Accessed Aug 28, 2021.

Nivolumab (Opdivo) for Hodgkin Lymphoma. U.S. Food and Drug Administration website. https://www.fda.gov/drugs/resources-information-approved-drugs/nivolumab-opdivo-hodgkin-lymphoma. Updated May 17, 2016. Accessed Aug 28, 2021.

FDA approves CAR-T cell therapy to treat adults with certain types of large B-cell lymphoma. U.S. Food and Drug Administration website. https://www.fda.gov/news-events/press-announcements/fda-approves-car-t-cell-therapy-treat-adults-certain-types-large-b-cell-lymphoma#:~:text=The%20U.S.%20Food%20and%20Drug,two%20other%20kinds%20of%20treatment. Updated Mar 21, 2018. Accessed Aug 28, 2021.

10.

McCarten KM, Nadel HR, Shulkin BL, Cho SY. Imaging for diagnosis, staging and response assessment of Hodgkin lymphoma and non-Hodgkin lymphoma. Pediatr Radiol. 2019;49:1545–64. https://doi.org/10.1007/s00247-019-04529-8.PubMedCrossRef

11.

Voltin CA, Mettler J, Grosse J, Dietlein M, Baues C, Schmitz C, et al. FDG-PET imaging for Hodgkin and diffuse large B-cell lymphoma-an updated overview. Cancers (Basel). 2020;12(3):601. https://doi.org/10.3390/cancers12030601.CrossRef

12.

Kirienko M, Sollini M, Chiti A. Hodgkin lymphoma and imaging in the era of anti-PD-1/PD-L1 therapy. Clinical and Translational Imaging. 2018;6:417–27.CrossRef

13.

Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Zucca E, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32:3059–68. https://doi.org/10.1200/JCO.2013.54.8800.PubMedPubMedCentralCrossRef

14.

Cheson BD, Ansell S, Schwartz L, Gordon LI, Advani R, Jacene HA, et al. Refinement of the Lugano Classification lymphoma response criteria in the era of immunomodulatory therapy. Blood. 2016;128:2489–96. https://doi.org/10.1182/blood-2016-05-718528.PubMedCrossRef

15.

Gundogan C, Guzel Y, Can C, Alabalik U, Komek H. False-positive 68Ga-fibroblast activation protein-specific inhibitor uptake of benign lymphoid tissue in a patient with breast cancer. Clin Nucl Med. 2021;46:e433–5. https://doi.org/10.1097/RLU.0000000000003594.PubMedCrossRef

16.

Adams HJ, de Klerk JM, Fijnheer R, Heggelman BG, Dubois SV, Nievelstein RA, et al. Prognostic superiority of the National Comprehensive Cancer Network International Prognostic Index over pretreatment whole-body volumetric-metabolic FDG-PET/CT metrics in diffuse large B-cell lymphoma. Eur J Haematol. 2015;94:532–9. https://doi.org/10.1111/ejh.12467.PubMedCrossRef

17.

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.

18.

Annunziata S, Cuccaro A, Tisi MC, Hohaus S, Rufini V. FDG-PET/CT at the end of immuno-chemotherapy in follicular lymphoma: the prognostic role of the ratio between target lesion and liver SUVmax (rPET). Ann Nucl Med. 2018;32:372–7. https://doi.org/10.1007/s12149-018-1243-2.PubMedCrossRef

19.

Bartlett NL, Herrera AF, Domingo-Domenech E, Mehta A, Forero-Torres A, Garcia-Sanz R, et al. A phase 1b study of AFM13 in combination with pembrolizumab in patients with relapsed or refractory Hodgkin lymphoma. Blood, J Am Soc Hematol. 2020;136:2401–9.

20.

Baudard M, Comte F, Conge AM, Mariano-Goulart D, Klein B, Rossi JF. Importance of [18F]fluorodeoxyglucose-positron emission tomography scanning for the monitoring of responses to immunotherapy in follicular lymphoma. Leuk Lymphoma. 2007;48:381–8. https://doi.org/10.1080/10428190601094354.PubMedCrossRef

21.

Casasnovas R-O, Ysebaert L, Thieblemont C, Bachy E, Feugier P, Delmer A, et al. FDG-PET–driven consolidation strategy in diffuse large B-cell lymphoma: final results of a randomized phase 2 study. Blood, J Am Soc Hematol. 2017;130:1315–26.

22.

Casasnovas R-O, Meignan M, Berriolo-Riedinger A, Bardet S, Julian A, Thieblemont C, et al. SUVmax reduction improves early prognosis value of interim positron emission tomography scans in diffuse large B-cell lymphoma. Blood, J Am Soc Hematol. 2011;118:37–43.

23.

Cashen AF, Dehdashti F, Luo J, Homb A, Siegel BA, Bartlett NL. 18F-FDG PET/CT for early response assessment in diffuse large B-cell lymphoma: poor predictive value of international harmonization project interpretation. J Nucl Med. 2011;52:386–92. https://doi.org/10.2967/jnumed.110.082586.PubMedCrossRef

24.

Castello A, Grizzi F, Qehajaj D, Rahal D, Lutman F, Lopci E. (18)F-FDG PET/CT for response assessment in Hodgkin lymphoma undergoing immunotherapy with checkpoint inhibitors. Leuk Lymphoma. 2019;60:367–75. https://doi.org/10.1080/10428194.2018.1488254.PubMedCrossRef

25.

Ceriani L, Gritti G, Cascione L. baseline metabolic heterogeneity and metabolic tumor volume in DLBCL prognostic model. Blood Adv. 2020;4(6):1082–92.PubMedPubMedCentralCrossRef

26.

Ceriani L, Martelli M, Gospodarowicz MK, Ricardi U, Ferreri AJ, Chiappella A, et al. Positron emission tomography/computed tomography assessment after immunochemotherapy and irradiation using the Lugano classification criteria in the IELSG-26 study of primary mediastinal B-cell lymphoma. Int J Radiat Oncol Biol Phys. 2017;97:42–9.PubMedCrossRef

27.

Chang CC, Cho SF, Chuang YW, Lin CY, Chang SM, Hsu WL, et al. Prognostic significance of total metabolic tumor volume on (18)F-fluorodeoxyglucose positron emission tomography/ computed tomography in patients with diffuse large B-cell lymphoma receiving rituximab-containing chemotherapy. Oncotarget. 2017;8:99587–600. https://doi.org/10.18632/oncotarget.20447.PubMedPubMedCentralCrossRef

28.

Chen A, Mokrane FZ, Schwartz L, Morschhauser F, Stamatoullas A, Schiano de Colella JM, et al. Early (18)F-FDG PET/CT response predicts survival in relapsed/refractory Hodgkin lymphoma treated with nivolumab. J Nucl Med. 2019 https://doi.org/10.2967/jnumed.119.232827.

29.

Chen Y, Zhou M, Liu J, Huang G. Prognostic value of bone marrow FDG uptake pattern of PET/CT in newly diagnosed diffuse large B-cell lymphoma. J Cancer. 2018;9:1231.PubMedPubMedCentralCrossRef

30.

Chen-Liang TH, Martín-Santos T, Jerez A, Rodríguez-García G, Senent L, Martínez-Millán C, et al. Bone marrow biopsy superiority over PET/CT in predicting progression-free survival in a homogeneously-treated cohort of diffuse large B-cell lymphoma. Cancer Med. 2017;6:2507–14.PubMedPubMedCentralCrossRef

31.

Cottereau AS, Nioche C, Dirand AS, Clerc J, Morschhauser F, Casasnovas O, et al. (18)F-FDG PET dissemination features in diffuse large B-cell lymphoma are predictive of outcome. J Nucl Med. 2020;61:40–5. https://doi.org/10.2967/jnumed.119.229450.PubMedPubMedCentralCrossRef

32.

Cottereau AS, Lanic H, Mareschal S, Meignan M, Vera P, Tilly H, et al. Molecular profile and FDG-PET/CT total metabolic tumor volume improve risk classification at diagnosis for patients with diffuse large B-cell lymphoma. Clin Cancer Res. 2016;22:3801–9. https://doi.org/10.1158/1078-0432.CCR-15-2825.PubMedCrossRef

33.

Cui Q, Vari F, Cristino AS, Salomon C, Rice GE, Sabdia MB, et al. Circulating cell-free miR-494 and miR-21 are disease response biomarkers associated with interim-positron emission tomography response in patients with diffuse large B-cell lymphoma. Oncotarget. 2018;9:34644.PubMedPubMedCentralCrossRef

34.

Delfau-Larue M-H, van der Gucht A, Dupuis J, Jais J-P, Nel I, Beldi-Ferchiou A, et al. Total metabolic tumor volume, circulating tumor cells, cell-free DNA: distinct prognostic value in follicular lymphoma. Blood Adv. 2018;2:807–16.PubMedPubMedCentralCrossRef

35.

de Oliveira Costa R, Neto AH, Siqueira S, Lage LAdPC, de Paula HM, Coutinho AM, et al. Interim fluorine-18 fluorodeoxyglucose PET-computed tomography and cell of origin by immunohistochemistry predicts progression-free and overall survival in diffuse large B-cell lymphoma patients in the rituximab era. Nucl Med Commun. 2016;37:1095.CrossRef

36.

Dercle L, Seban RD, Lazarovici J, Schwartz LH, Houot R, Ammari S, et al. (18)F-FDG PET and CT scans detect new imaging patterns of response and progression in patients with Hodgkin lymphoma treated by anti-programmed death 1 immune checkpoint inhibitor. J Nucl Med. 2018;59:15–24. https://doi.org/10.2967/jnumed.117.193011.PubMedCrossRef

37.

Derlin T, Schultze-Florey C, Werner RA, Möhn N, Skripuletz T, David S, et al. 18 F-FDG PET/CT of off-target lymphoid organs in CD19-targeting chimeric antigen receptor T-cell therapy for relapsed or refractory diffuse large B-cell lymphoma. Ann Nucl Med. 2021;35:132–8.PubMedCrossRef

38.

Dührsen U, Müller S, Hertenstein B, Thomssen H, rg Kotzerke J, Mesters R, et al. Positron emission tomography-guided therapy of aggressive non-Hodgkin lymphomas PETAL: a multicenter, randomized phase III trial. J Clin Oncol. 2018;36:2024–34.PubMedCrossRef

39.

Dunleavy K, Fanale MA, Abramson JS, Noy A, Caimi PF, Pittaluga S, et al. A prospective multicenter phase 2 study of dose-adjusted-EPOCH-R in untreated MYC-rearranged aggressive B-cell lymphoma. The Lancet Haematology. 2018;5:e609.PubMedPubMedCentralCrossRef

40.

El-Galaly TC, Villa D, Michaelsen TY, Hutchings M, Mikhaeel NG, Savage KJ, et al. The number of extranodal sites assessed by PET/CT scan is a powerful predictor of CNS relapse for patients with diffuse large B-cell lymphoma: an international multicenter study of 1532 patients treated with chemoimmunotherapy. Eur J Cancer. 2017;75:195–203.PubMedCrossRef

41.

El-Galaly TC, Villa D, Alzahrani M, Hansen JW, Sehn LH, Wilson D, et al. Outcome prediction by extranodal involvement, IPI, R-IPI, and NCCN-IPI in the PET/CT and rituximab era: AD anish–C anadian study of 443 patients with diffuse-large B-cell lymphoma. Am J Hematol. 2015;90:1041–6.PubMedCrossRef

42.

Esfahani SA, Heidari P, Halpern EF, Hochberg EP, Palmer EL, Mahmood U. Baseline total lesion glycolysis measured with 18F-FDG PET/CT as a predictor of progression-free survival in diffuse large B-cell lymphoma: a pilot study. Am J Nucl Med Mol Imaging. 2013;3:272.PubMedPubMedCentral

43.

Gallicchio R, Mansueto G, Simeon V, Nardelli A, Guariglia R, Capacchione D, et al. F-18 FDG PET/CT quantization parameters as predictors of outcome in patients with diffuse large B-cell lymphoma. Eur J Haematol. 2014;92:382–9. https://doi.org/10.1111/ejh.12268.PubMedCrossRef

44.

Giulino-Roth L, O’Donohue T, Chen Z, Bartlett NL, LaCasce A, Martin-Doyle W, et al. Outcomes of adults and children with primary mediastinal B-cell lymphoma treated with dose-adjusted EPOCH-R. Br J Haematol. 2017;179:739–47.PubMedPubMedCentralCrossRef

45.

Han EJ, Joo Hyun O, Yoon H, Jung SE, Park G, Choi BO, et al. FDG PET/CT response in diffuse large B-cell lymphoma: reader variability and association with clinical outcome. Medicine. 2016;95.

46.

Han HS, Escalon MP, Hsiao B, Serafini A, Lossos IS. High incidence of false-positive PET scans in patients with aggressive non-Hodgkin’s lymphoma treated with rituximab-containing regimens. Ann Oncol. 2009;20:309–18. https://doi.org/10.1093/annonc/mdn629.PubMedCrossRef

47.

Hart D, Avivi I, Thomson K, Peggs K, Morris E, Goldstone A, et al. Use of 18F-FDG positron emission tomography following allogeneic transplantation to guide adoptive immunotherapy with donor lymphocyte infusions. Br J Haematol. 2005;128:824–9.PubMedCrossRef

48.

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

49.

Jeon YW, O JH, Park KS, Min GJ, Park SS, Yoon JH, et al. Prognostic impact of interim positron emission tomography in mantle cell lymphoma patients treated with frontline R-CHOP. Bri J Haematol. 2020;188:860–71.CrossRef

50.

Khan AB, Barrington SF, Mikhaeel NG, Hunt AA, Cameron L, Morris T, et al. PET-CT staging of DLBCL accurately identifies and provides new insight into the clinical significance of bone marrow involvement. Blood. 2013;122:61–7.PubMedCrossRef

51.

Kim SJ, Yi HK, Lim CH, Cho YS, Choi JY, Choe YS, et al. Intra-patient variability of FDG standardized uptake values in mediastinal blood pool, liver, and myocardium during R-CHOP chemotherapy in patients with diffuse large B-cell lymphoma. Nucl Med Mol Imaging. 2016;50:300–7. https://doi.org/10.1007/s13139-016-0432-y.PubMedPubMedCentralCrossRef

52.

Kim J, Hong J, Kim SG, Hwang KH, Kim M, Ahn HK, et al. Prognostic value of metabolic tumor volume estimated by 18 F-FDG positron emission tomography/computed tomography in patients with diffuse large B-cell lymphoma of stage II or III disease. Nucl Med Mol Imaging. 2014;48:187–95.PubMedPubMedCentralCrossRef

53.

Kim TM, Paeng JC, Chun IK, Keam B, Jeon YK, Lee SH, et al. Total lesion glycolysis in positron emission tomography is a better predictor of outcome than the International Prognostic Index for patients with diffuse large B cell lymphoma. Cancer. 2013;119:1195–202. https://doi.org/10.1002/cncr.27855.PubMedCrossRef

54.

Kitajima K, Okada M, Yoshihara K, Tokugawa T, Sawada A, Yoshihara S, et al. Predictive value of interim FDG-PET/CT findings in patients with diffuse large B-cell lymphoma treated with R-CHOP. Oncotarget. 2019;10:5403–11. https://doi.org/10.18632/oncotarget.27103.PubMedPubMedCentralCrossRef

55.

Kocurek A, Malkowski B, Giza A, Jurczak W. Primary mediastinal B-cell lymphoma - metabolic and anatomical features in 18FDG-PET/CT and response to therapy. Contemp Oncol (Pozn). 2016;20:297–301. https://doi.org/10.5114/wo.2016.61849.

56.

Kong Y, Qu L, Li Y, Liu D, Lv X, Han J. Predictive significance of a new prognostic score for patients with diffuse large B-cell lymphoma in the interim-positron emission tomography findings. Med. 2016;95:e2808.CrossRef

57.

Kostakoglu L, Martelli M, Sehn LH, Belada D, Carella A-M, Chua N, et al. End-of-treatment PET/CT predicts PFS and OS in DLBCL after first-line treatment: results from GOYA. Blood Adv. 2021;5:1283–90.PubMedPubMedCentralCrossRef

58.

Lepik KV, Fedorova LV, Kondakova EV, Zalyalov YR, Babenko EV, Lepik EE, et al. A phase 2 study of nivolumab using a fixed dose of 40 mg (Nivo40) in patients with relapsed/refractory Hodgkin lymphoma. HemaSphere. 2020;4:e480.PubMedPubMedCentralCrossRef

59.

Leppä S, Jørgensen J, Tierens A, Meriranta L, Østlie I, de Nully BP, et al. Patients with high-risk DLBCL benefit from dose-dense immunochemotherapy combined with early systemic CNS prophylaxis. Blood Adv. 2020;4:1906–15.PubMedPubMedCentralCrossRef

60.

Mamot C, Klingbiel D, Hitz F, Renner C, Pabst T, Driessen C, et al. Final results of a prospective evaluation of the predictive value of interim positron emission tomography in patients with diffuse large B-cell lymphoma treated with R-CHOP-14 (SAKK 38/07). J Clin Oncol. 2015;33:2523–9.PubMedCrossRef

61.

Mayerhoefer ME, Staudenherz A, Kiesewetter B, Weber M, Simonitsch-Klupp I, Gibbs P, et al. Pre-therapeutic total lesion glycolysis on [(18)F]FDG-PET enables prognostication of 2-year progression-free survival in MALT lymphoma patients treated with CD20-antibody-based immunotherapy. Mol Imaging Biol. 2019;21(6):1192. https://doi.org/10.1007/s11307-019-01329-2.PubMedPubMedCentralCrossRef

62.

Mayerhoefer ME, Riedl CC, Kumar A, Gibbs P, Weber M, Tal I, et al. Radiomic features of glucose metabolism enable prediction of outcome in mantle cell lymphoma. Eur J Nucl Med Mol Imaging. 2019;46:2760–9. https://doi.org/10.1007/s00259-019-04420-6.PubMedPubMedCentralCrossRef

63.

Mayerhoefer ME, Raderer M, Jaeger U, Staber P, Kiesewetter B, Senn D, et al. Ultra-early response assessment in lymphoma treatment: [(18)F]FDG PET/MR captures changes in glucose metabolism and cell density within the first 72 hours of treatment. Eur J Nucl Med Mol Imaging. 2018;45:931–40. https://doi.org/10.1007/s00259-018-3937-z.PubMedPubMedCentralCrossRef

64.

Mayerhoefer ME, Karanikas G, Kletter K, Kiesewetter B, Weber M, Rausch I, et al. Can interim 18F-FDG PET or diffusion-weighted MRI predict end-of-treatment outcome in FDG-avid MALT lymphoma after rituximab-based therapy? A preliminary study in 15 patients. Clin Nucl Med. 2016;41:837–43. https://doi.org/10.1097/RLU.0000000000001395.PubMedCrossRef

65.

Melani C, Advani R, Roschewski M, Walters KM, Chen CC, Baratto L, et al. End-of-treatment and serial PET imaging in primary mediastinal B-cell lymphoma following dose-adjusted EPOCH-R: a paradigm shift in clinical decision making. Haematologica. 2018;103:1337–44. https://doi.org/10.3324/haematol.2018.192492.PubMedPubMedCentralCrossRef

66.

Micallef IN, Maurer MJ, Wiseman GA, Nikcevich DA, Kurtin PJ, Cannon MW, et al. Epratuzumab with rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone chemotherapy in patients with previously untreated diffuse large B-cell lymphoma. Blood, J Am Soc Hematol. 2011;118:4053–61.

67.

Mikhaeel NG, Smith D, Dunn JT, Phillips M, Moller H, Fields PA, et al. Combination of baseline metabolic tumour volume and early response on PET/CT improves progression-free survival prediction in DLBCL. Eur J Nucl Med Mol Imaging. 2016;43:1209–19. https://doi.org/10.1007/s00259-016-3315-7.PubMedPubMedCentralCrossRef

68.

Minamimoto R, Fayad L, Advani R, Vose J, Macapinlac H, Meza J, et al. Diffuse large B-cell lymphoma: prospective multicenter comparison of early interim FLT PET/CT versus FDG PET/CT with IHP, EORTC, Deauville, and PERCIST criteria for early therapeutic monitoring. Radiology. 2016;280:220–9.PubMedCrossRef

69.

Mir F, Barrington SF, Brown H, Nielsen T, Sahin D, Meignan M, et al. Baseline SUVmax did not predict histological transformation in follicular lymphoma in the phase 3 GALLIUM study. Blood. 2020;135:1214–8. https://doi.org/10.1182/blood.2019001091.PubMedPubMedCentralCrossRef

70.

Mokrane F-Z, Chen A, Schwartz LH, Morschhauser F, Stamatoullas A, Schiano de Colella J-M, et al. Performance of CT compared with 18F-FDG PET in predicting the efficacy of nivolumab in relapsed or refractory Hodgkin lymphoma. Radiology. 2020;295:651–61.PubMedCrossRef

71.

Morschhauser F, Feugier P, Flinn IW, Gasiorowski R, Greil R, Illés Á, et al. A phase 2 study of venetoclax plus R-CHOP as first-line treatment for patients with diffuse large B-cell lymphoma. Blood, J Am Soc Hematol. 2021;137:600–9.

72.

Moskowitz CH, Schöder H, Teruya-Feldstein J, Sima C, Iasonos A, Portlock CS, et al. Risk-adapted dose-dense immunochemotherapy determined by interim FDG-PET in advanced-stage diffuse large B-cell lymphoma. J Clin Oncol. 2010;28:1896.PubMedPubMedCentralCrossRef

73.

Oñate-Ocaña LF, Cortés V, Castillo-Llanos R, Terrazas A, Garcia-Perez O, Pitalúa-Cortes Q, et al. Metabolic tumor volume changes assessed by interval 18fluorodeoxyglucose positron emission tomography-computed tomography for the prediction of complete response and survival in patients with diffuse large B-cell lymphoma. Oncol Lett. 2018;16:1411–8.PubMedPubMedCentral

74.

Pinnix CC, Ng AK, Dabaja BS, Milgrom SA, Gunther JR, Fuller CD, et al. Positron emission tomography–computed tomography predictors of progression after DA-R-EPOCH for PMBCL. Blood Adv. 2018;2:1334–43.PubMedPubMedCentralCrossRef

75.

Rutherford SC, Herold M, Hiddemann W, Kostakoglu L, Marcus R, Martelli M, et al. Impact of bone marrow biopsy on response assessment in immunochemotherapy-treated lymphoma patients in GALLIUM and GOYA. Blood Adv. 2020;4:1589–93. https://doi.org/10.1182/bloodadvances.2019001261.PubMedPubMedCentralCrossRef

76.

Sasanelli M, Meignan M, Haioun C, Berriolo-Riedinger A, Casasnovas RO, Biggi A, et al. Pretherapy metabolic tumour volume is an independent predictor of outcome in patients with diffuse large B-cell lymphoma. Eur J Nucl Med Mol Imaging. 2014;41:2017–22. https://doi.org/10.1007/s00259-014-2822-7.PubMedCrossRef

77.

Schmitz C, Hüttmann A, Müller SP, Hanoun M, Boellaard R, Brinkmann M, et al. Dynamic risk assessment based on positron emission tomography scanning in diffuse large B-cell lymphoma: post-hoc analysis from the PETAL trial. Eur J Cancer. 2020;124:25–36.PubMedCrossRef

78.

Senjo H, Hirata K, Izumiyama K, Minauchi K, Tsukamoto E, Itoh K, et al. High metabolic heterogeneity on baseline 18FDG-PET/CT scan as a poor prognostic factor for newly diagnosed diffuse large B-cell lymphoma. Blood Adv. 2020;4:2286–96.PubMedPubMedCentralCrossRef

79.

Shah NN, Nagle SJ, Torigian DA, Farwell MD, Hwang WT, Frey N, et al. Early positron emission tomography/computed tomography as a predictor of response after CTL019 chimeric antigen receptor -T-cell therapy in B-cell non-Hodgkin lymphomas. Cytotherapy. 2018;20:1415–8. https://doi.org/10.1016/j.jcyt.2018.10.003.PubMedCrossRef

80.

Song G-Y, Yoon SE, Kim SJ, Kim JS, Koh Y, Moon J-H, et al. Prognostic significance of interim PET/CT response for the treatment of advanced-stage marginal zone lymphoma in the post-rituximab era. Sci Rep. 2020;10:1–8.

81.

Song MK, Yang DH, Lee GW, Lim SN, Shin S, Pak KJ, et al. High total metabolic tumor volume in PET/CT predicts worse prognosis in diffuse large B cell lymphoma patients with bone marrow involvement in rituximab era. Leuk Res. 2016;42:1–6. https://doi.org/10.1016/j.leukres.2016.01.010.PubMedCrossRef

82.

Song YS, Lee WW, Lee JS, Kim SE. Prediction of central nervous system relapse of diffuse large B-cell lymphoma using pretherapeutic [18F] 2-fluoro-2-deoxyglucose (FDG) positron emission tomography/computed tomography. Medicine. 2015;94:e1978.PubMedPubMedCentralCrossRef

83.

Song MK, Chung JS, Shin HJ, Lee SM, Lee SE, Lee HS, et al. Clinical significance of metabolic tumor volume by PET/CT in stages II and III of diffuse large B cell lymphoma without extranodal site involvement. Ann Hematol. 2012;91:697–703. https://doi.org/10.1007/s00277-011-1357-2.PubMedCrossRef

84.

Song MK, Chung JS, Shin HJ, Moon JH, Lee JO, Lee HS, et al. Prognostic value of metabolic tumor volume on PET / CT in primary gastrointestinal diffuse large B cell lymphoma. Cancer Sci. 2012;103:477–82. https://doi.org/10.1111/j.1349-7006.2011.02164.x.PubMedPubMedCentralCrossRef

85.

Sun H, Yu Z, Ma N, Zhou J, Tian R, Zhao M, et al. Risk stratification of diffuse large B-cell lymphoma with interim PET/CT by combining Deauville scores and International Prognostic Index. Cancer Manag Res. 2019;11:9449–57. https://doi.org/10.2147/CMAR.S218678.PubMedPubMedCentralCrossRef

86.

Swinnen LJ, Li H, Quon A, Gascoyne R, Hong F, Ranheim EA, et al. Response-adapted therapy for aggressive non-Hodgkin’s lymphomas based on early [18F] FDG-PET scanning: ECOG-ACRIN Cancer Research Group study (E3404). Br J Haematol. 2015;170:56–65.PubMedPubMedCentralCrossRef

87.

Takasaki H, Yamamoto W, Ishii Y, Takahashi H, Watanabe R, Harada T, et al. Post-treatment PET–CT findings may predict the prognosis of DLBCL with a bulky mass. Indian Journal of Hematology and Blood Transfusion. 2015;31:346–51.PubMedCrossRef

88.

Tateishi U, Tatsumi M, Terauchi T, Ando K, Niitsu N, Kim WS, et al. Prognostic significance of metabolic tumor burden by positron emission tomography/computed tomography in patients with relapsed/refractory diffuse large B-cell lymphoma. Cancer Sci. 2015;106:186–93.PubMedPubMedCentralCrossRef

89.

Toledano MN, Vera P, Tilly H, Jardin F, Becker S. Comparison of therapeutic evaluation criteria in FDG-PET/CT in patients with diffuse large-cell B-cell lymphoma: Prognostic impact of tumor/liver ratio. PLoS ONE. 2019;14:e0211649. https://doi.org/10.1371/journal.pone.0211649.PubMedPubMedCentralCrossRef

90.

Trotman J, Barrington SF, Belada D, Meignan M, MacEwan R, Owen C, et al. Prognostic value of end-of-induction PET response after first-line immunochemotherapy for follicular lymphoma (GALLIUM): secondary analysis of a randomised, phase 3 trial. Lancet Oncol. 2018;19:1530–42. https://doi.org/10.1016/S1470-2045(18)30618-1.PubMedCrossRef

91.

Vaxman I, Bernstine H, Kleinstern G, Hendin N, Shimony S, Domachevsky L, et al. FDG PET/CT as a diagnostic and prognostic tool for the evaluation of marginal zone lymphoma. Hematol Oncol. 2019;37:168–75. https://doi.org/10.1002/hon.2578.PubMedCrossRef

92.

Vercellino L, Cottereau A-S, Casasnovas O, Tilly H, Feugier P, Chartier L, et al. High total metabolic tumor volume at baseline predicts survival independent of response to therapy. Blood, J Am Soc Hematol. 2020;135:1396–405.

93.

Vercellino L, Di Blasi R, Kanoun S, Tessoulin B, Rossi C, D’Aveni-Piney M, et al. Predictive factors of early progression after CAR T-cell therapy in relapsed/refractory diffuse large B-cell lymphoma. Blood Adv. 2020;4:5607–15.PubMedPubMedCentralCrossRef

94.

Voltin C-A, Mettler J, Mueller H, Fuchs M, Baues C, Dietlein M, et al. Metabolic tumor volume for early response assessment in early-stage unfavorable Hodgkin lymphoma treated with nivolumab in the GHSG Nivahl phase II trial. American Society of Hematology Washington, DC; 2019.

95.

Wang J, Hu Y, Yang S, Wei G, Zhao X, Wu W, et al. Role of fluorodeoxyglucose positron emission tomography/computed tomography in predicting the adverse effects of chimeric antigen receptor T cell therapy in patients with non-Hodgkin lymphoma. Biol Blood Marrow Transplant. 2019;25:1092–8.PubMedCrossRef

96.

Wang R, Xu B, Liu C, Guan Z, Zhang J, Li F, et al. Prognostic value of interim fluorodeoxyglucose and fluorothymidine PET/CT in diffuse large B-cell lymphoma. Br J Radiol. 2018;91:20180240.PubMedPubMedCentralCrossRef

97.

Wei Z, Li J, Cheng Z, Yuan L, Liu P. A single center experience: rituximab plus cladribine is an effective and safe first-line therapy for unresectable bronchial-associated lymphoid tissue lymphoma. J Thorac Dis. 2017;9:1081–92. https://doi.org/10.21037/jtd.2017.03.81.PubMedPubMedCentralCrossRef

98.

Wong-Sefidan I, Byrtek M, Zhou X, Friedberg JW, Flowers CR, Zelenetz AD, et al. [18F] Positron emission tomography response after rituximab-containing induction therapy in follicular lymphoma is an independent predictor of survival after adjustment for FLIPI in academic and community-based practice. Leuk Lymphoma. 2017;58:809–15.PubMedCrossRef

99.

Yim SK, Yhim H-Y, Han Y-H, Jeon S-Y, Lee N-R, Song E-K, et al. Early risk stratification for diffuse large B-cell lymphoma integrating interim Deauville score and International Prognostic Index. Ann Hematol. 2019;98:2739–48.PubMedCrossRef

100.

Younes A, Oki Y, McLaughlin P, Copeland AR, Goy A, Pro B, et al. Phase 2 study of rituximab plus ABVD in patients with newly diagnosed classical Hodgkin lymphoma. Blood, J Am Soc Hematol. 2012;119:4123–8.

101.

Zhang YY, Song L, Zhao MX, Hu K. A better prediction of progression-free survival in diffuse large B-cell lymphoma by a prognostic model consisting of baseline TLG and %DeltaSUVmax. Cancer Med. 2019;8:5137–47. https://doi.org/10.1002/cam4.2284.PubMedPubMedCentralCrossRef

102.

Zhang X, Fan W, Xia Z-J, Hu Y-Y, Lin X-P, Zhang Y-R, et al. Use of subsequent PET/CT in diffuse large B-cell lymphoma patients in complete remission following primary therapy. Chin J Cancer. 2015;34:70–8.PubMedPubMedCentralCrossRef

103.

Zhao P, Yu T, Pan Z. Prognostic value of the baseline 18F-FDG PET/CT metabolic tumour volume (MTV) and further stratification in low-intermediate (LI) and high-intermediate (HI) risk NCCNIPI subgroup by MTV in DLBCL MTV predict prognosis in DLBCL. Ann Nucl Med. 2021;35:24–30.PubMedCrossRef

104.

Zhou Y, Zhao Z, Li J, Zhang B, Sang S, Wu Y, et al. Prognostic values of baseline, interim and end-of therapy (18)F-FDG PET/CT in patients with follicular lymphoma. Cancer Manag Res. 2019;11:6871–85. https://doi.org/10.2147/CMAR.S216445.PubMedPubMedCentralCrossRef

105.

Zhou M, Chen Y, Huang H, Zhou X, Liu J, Huang G. Prognostic value of total lesion glycolysis of baseline 18F-fluorodeoxyglucose positron emission tomography/computed tomography in diffuse large B-cell lymphoma. Oncotarget. 2016;7:83544–53. https://doi.org/10.18632/oncotarget.13180.PubMedPubMedCentralCrossRef

106.

Zinzani PL, Gandolfi L, Broccoli A, Argnani L, Fanti S, Pellegrini C, et al. Midtreatment 18F-fluorodeoxyglucose positron-emission tomography in aggressive non-Hodgkin lymphoma. Cancer. 2011;117:1010–8. https://doi.org/10.1002/cncr.25579.PubMedCrossRef

107.

Moher D, Liberati A, Tetzlaff J, Group P. Altman DG Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS medicine. 2009;6:e1000097.PubMedPubMedCentralCrossRef

Title: The value of FDG PET/CT imaging in outcome prediction and response assessment of lymphoma patients treated with immunotherapy: a meta-analysis and systematic review
Authors: Zahra Kiamanesh
Narjess Ayati
Ramin Sadeghi
Eliza Hawkes
Sze Ting Lee
Andrew M. Scott
Publication date: 06-08-2022
Publisher: Springer Berlin Heidelberg
Keywords: Lymphoma
Non-Hodgkin Lymphoma
Anti-CD20 Antibody
Checkpoint Inhibitors
Published in: European Journal of Nuclear Medicine and Molecular Imaging / Issue 13/2022
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI: https://doi.org/10.1007/s00259-022-05918-2

At a glance: The STEP trials

Springer Medicine

The value of FDG PET/CT imaging in outcome prediction and response assessment of lymphoma patients treated with immunotherapy: a meta-analysis and systematic review

Abstract

Purpose

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 13/2022

18F-FDG PET/CT findings of mesenchymal hamartoma of the liver in an adolescent

Radionuclide imaging and therapy directed towards the tumor microenvironment: a multi-cancer approach for personalized medicine

Noninvasive photoacoustic computed tomography/ultrasound imaging to identify high-risk atherosclerotic plaques

Presence of non-Newtonian fluid in invasive pulmonary mucinous adenocarcinomas impacts fluorescence during intraoperative molecular imaging of lung cancer

Preclinical and first-in-human evaluation of 18F-labeled D-peptide antagonist for PD-L1 status imaging with PET

X-ray multiscale 3D neuroimaging to quantify cellular aging and neurodegeneration postmortem in a model of Alzheimer’s disease