The Role of 18FDG-PET/CT in Malignant Lymphomas: Clinical Implications

  • Theodoros P. Vassilakopoulos
  • Vassilios K. Prassopoulos


PET/CT has a key role in final response assessment after treatment in most types of malignant lymphomas, as well as in baseline staging and interim (mid-treatment) evaluation. Its application is widely established in Hodgkin lymphoma (HL) and aggressive B-cell lymphomas, including diffuse large B-cell lymphoma (DLBCL), primary mediastinal large B-cell lymphoma (PMLBCL), and other related subtypes. Although recent recommendations suggest the use of PET/CT for baseline staging and response assessment in follicular lymphomas, mantle cell lymphoma (MCL), Burkitt lymphoma, and “nodal” T-cell lymphomas [anaplastic large cell (ALCL), peripheral T-cell (PTCL), and angioimmunoblastic T-cell lymphoma (AITL)], the accumulated clinical experience with these subtypes is considerably less. The role of PET/CT is much more controversial in non-follicular low-grade lymphomas and primary extranodal lymphomas other than DLBCL.


  1. 1.
    Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Lister TA et al (2014) Recommendations for the initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol 32:3059–3067PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Barrington SF, Mikhaeel GN, Kostakoglu L, Meignan M, Hutchings M, Müeller SP et al (2014) 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 32:3048–3058PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Ngeow JY, Quek RH, Ng DC et al (2009) High SUV uptake on FDG-PET/CT predicts for an aggressive B-cell lymphoma in a prospective study of primary FDG-PET/CT staging in lymphoma. Ann Oncol 20:1543–1547PubMedCrossRefGoogle Scholar
  4. 4.
    Weiler-Sagie M, Bushelev O, Epelbaum R et al (2010) 18F-FDG avidity in lymphoma readdressed: a study of 766 patients. J Nucl Med 51:25–30PubMedCrossRefGoogle Scholar
  5. 5.
    Barrington SF, Kirkwood AA, Franceschetto A, Fulham MJ, Roberts TH, Almquist H et al (2016) PET-CT for staging and early response: results from the response-adapted therapy in advanced Hodgkin lymphoma study. Blood 127:1531–1538PubMedCrossRefGoogle Scholar
  6. 6.
    Angelopoulou MK, Mosa E, Pangalis GA, Rondogianni P, Chatziioannou S, Prassopoulos V et al (2017) The significance of PET/CT in the initial staging of Hodgkin lymphoma: Experience outside clinical trials. Anticancer Res 37:5727–5736PubMedGoogle Scholar
  7. 7.
    Eichenauer DA, Engert A, Andre M, Federico M, Illidge T, Hutcghings M et al (2014) Hodgkin’s lymphoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 25(Suppl 3):70–75CrossRefGoogle Scholar
  8. 8.
    El-Galaly TC, d’Amore F, Mylam KJ et al (2012) Routine bone marrow biopsy has little or no therapeutic consequence for positron emission tomography/computed tomography-staged treatment-naïve patients with Hodgkin lymphoma. J Clin Oncol 30:4508–4514PubMedCrossRefGoogle Scholar
  9. 9.
    Vassilakopoulos TP, Rondogianni P, Prassopoulos V, Chatziioannou S, Moschogiannis M, Poziopoulos C et al (2014) Comparative assessment of bone marrow involvement (BMI) by bone marrow biopsy (BMB) or positron emission tomography/computed tomography (PET/CT) in Hodgkin lymphoma (HL). Haematologica 99(Suppl 1):401 (abstr. 1050)Google Scholar
  10. 10.
    Zwarthoed C, El-Galaly TC, Canepari M, Ouvrier MJ, Viotti J, Ettaiche M (2017) Prognostic value of bone marrow tracer uptake pattern in baseline PET scans in Hodgkin lymphoma: Results from an international collaborative study. J Nucl Med 58:1249–1254PubMedCrossRefGoogle Scholar
  11. 11.
    Adams HJ, Kwee TC, de Keizer B, Fijnheer R, de Klerk JM, Littooij AS et al (2014) Systematic review and meta-analysis on the diagnostic performance of FDG-PET/CT in detecting bone marrow involvement in newly diagnosed Hodgkin lymphoma: is bone marrow biopsy still necessary? Ann Oncol 25:921–927PubMedCrossRefGoogle Scholar
  12. 12.
    Puccini B, Nassi L, Minoia C, Volpetti S, Ciancia R, Riccomagno PC et al (2017) Role of bone marrow biopsy in staging of patients with classical Hodgkin’s lymphoma undergoing positron emission tomography/computed tomography. Ann Hematol. PubMedCrossRefGoogle Scholar
  13. 13.
    Vassilakopoulos TP, Angelopoulou MK, Constantinou N et al (2005) Development and validation of a clinical prediction rule for bone marrow involvement in patients with Hodgkin lymphoma. Blood 105:1875–1880PubMedCrossRefGoogle Scholar
  14. 14.
    Sehn LH, Scott DW, Chhanabhai M et al (2011) Impact of concordant and discordant bone marrow involvement on outcome in diffuse large B-cell lymphoma treated with R-CHOP. J Clin Oncol 29:1452–1457PubMedCrossRefGoogle Scholar
  15. 15.
    Paone G, Itti E, Haioun C et al (2009) Bone marrow involvement in diffuse large B-cell lymphoma: correlation between FDG-PET uptake and type of cellular infiltrate. Eur J Nucl Med Mol Imaging 36:745–750PubMedCrossRefGoogle Scholar
  16. 16.
    Hong J, Lee Y, Park Y et al (2012) Role of FDG-PET/CT in detecting lymphomatous bone marrow involvement in patients with newly diagnosed diffuse large B-cell lymphoma. Ann Hematol 91:687–695PubMedCrossRefGoogle Scholar
  17. 17.
    Cerci JJ, Gyorke T, Fanti S, Paez D, Meneghetti JC, Redondo F et al (2014) Combined PET and biopsy evidence of marrow involvement improves prognostic prediction in diffuse large B-cell lymphoma. J Nucl Med 55:1591–1597PubMedCrossRefGoogle Scholar
  18. 18.
    Berthet L, Cochet A, Kanoun S, Berriolo-Riedinger A, Humbert O, Toubeau M et al (2013) In newly diagnosed diffuse large B-cell lymphoma, determination of bone marrow involvement with 18F-FDG PET/CT provides better diagnostic performance and prognostic stratification than does biopsy. J Nucl Med 54:1244–1250PubMedCrossRefGoogle Scholar
  19. 19.
    Adams HJA, Kwee TC, Finjnheer R, Dubois SV, Nievelstein AJR, de Klerk JMH (2014) Bone marrow 18F-fluoro-2-deoxy-D-glucose positron emission tomography/computed tomography cannot replace bone marrow biopsy in diffuse large B-cell lymphoma. Am J Hematol 89:726–731PubMedCrossRefGoogle Scholar
  20. 20.
    Khan AB, Barrington SF, Mikhaeel NG, Hunt AA, Cameron L, Morris T et al (2013) PET-CT staging of DLBCL accurately identifies and provides new insight into the clinical significance of bone marrow involvement. Blood 122:61–67PubMedCrossRefGoogle Scholar
  21. 21.
    Adams HJA, Kwee TC (2015) Do not abandon the bone marrow biopsy yet in diffuse large B-cell lymphoma. J Clin Oncol 33:1217PubMedCrossRefGoogle Scholar
  22. 22.
    Andreou JA, Kosmidis PA, Gouliamos AD, Prassopoulos V, Vassilakopoulos TP, Vrakidou E (eds) (2016) PET/CT in lymphomas: a case-based Atlas. Springer International Publishing, Switzerland. CrossRefGoogle Scholar
  23. 23.
    Vassilakopoulos TP, Prassopoulos V, Rondogianni P, Chatziioannou S, Konstantopoulos K, Angelopoulou MK (2015) Role of FDG-PET/CT in staging and first-line treatment of Hodgkin and aggressive B-cell lymphomas. MEMO 8:105–114CrossRefGoogle Scholar
  24. 24.
    Vassilakopoulos TP, Pangalis GA, Katsigiannis A et al (2012) Rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone with or without radiotherapy in primary mediastinal large B-cell lymphoma: the emerging standard of care. Oncologist 17:239–249PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Martelli M, Ceriani L, Zucca E, Zinzani PL, Ferreri AJ, Vitolo U et al (2014) [18F] fluorodeoxyglucose positron emission tomography predicts survival after chemoimmunotherapy for primary mediastinal large B-cell lymphoma: results of the International Extranodal Lymphoma Study Group IELSG-26 study. J Clin Oncol 32:1769–1775PubMedCrossRefGoogle Scholar
  26. 26.
    Meignan M, Itti E, Gallamini A, Younes A (2015) FDG PET/CT imaging as a biomarker in lymphoma. Eur J Nucl Med Mol Imaging 42:623–633PubMedCrossRefGoogle Scholar
  27. 27.
    Kanoun S, Rossi C, Berriolo-Riedinger A, Dygai-Cochet I, Cochet A, Humbert O et al (2014) Baseline metabolic tumor volume is an independent prognostic factor in Hodgkin lymphoma. Eur J Nucl Med Mol Imaging 41:1735–1743PubMedCrossRefGoogle Scholar
  28. 28.
    Song MK, Chung JS, Lee JJ, Jeong SY, Lee SM, Hong JS et al (2013) Metabolic tumor volume by positron emission tomography/computed tomography as a clinical parameter to determine therapeutic modality for early stage Hodgkin’s lymphoma. Cancer Sci 104:1656–1661PubMedCrossRefGoogle Scholar
  29. 29.
    Song MK, Chung JS, Shin HJ, Lee SM, Lee SE, Lee HS et al (2012) 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 91:697–703PubMedCrossRefGoogle Scholar
  30. 30.
    Sasanelli M, Meignan M, Haioun C, Berriolo-Riedinger A, Casasnovas RO, Biggi A et al (2014) Pretherapy metabolic tumor volume is an independent predictor of outcome in diffuse large B-cell lymphoma. Eur J Nucl Med Mol Imaging 41:2017–2022PubMedCrossRefGoogle Scholar
  31. 31.
    Mikhaeel NG, Smith D, Dunn JT, Phillips M, Møller H, Fields PA et al (2016) 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 43:1209–1219PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Song MK, Yang DH, Lee GW, Lim SN, Shin S, Pak KJ et al (2016) 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 42:1–6PubMedCrossRefGoogle Scholar
  33. 33.
    Cottereau AS, Lanic H, Mareschal S, Meignan M, Vera P, Tilly H et al (2016) 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 22:3801–3809PubMedCrossRefGoogle Scholar
  34. 34.
    Kim TM, Paeng JC, Chun IK, Keam B, Jeon YK, Lee SH et al (2013) 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 119:1195–1202PubMedCrossRefGoogle Scholar
  35. 35.
    Zhou M, Chen Y, Huang H, Zhou X, Liu J, Huang G (2016) Prognostic value of total lesion glycolysis of baseline 18F-fluorodeoxyglucose positron emission tomography/computed tomography in diffuse large B-cell lymphoma. Oncotarget 7:83544–83553PubMedPubMedCentralGoogle Scholar
  36. 36.
    Ceriani L, Martelli M, Zinzani PL et al (2015) Utility of baseline 18FDG PET/CT functional parameters in defining prognosis of primary mediastinal (thymic) large B-cell lymphoma. Blood 126:950–956PubMedCrossRefGoogle Scholar
  37. 37.
    Meignan M, Cottereau AS, Versari A, Chartier L, Dupuis J, Boussetta S et al (2016) Baseline metabolic tumor volume predicts outcome in high-tumor-burden follicular lymphoma: a pooled analysis of three multicenter studies. J Clin Oncol 34:3618–3626PubMedCrossRefGoogle Scholar
  38. 38.
    Cottereau AS, Becker S, Broussais F, Casasnovas O, Kanoun S, Roques M et al (2016) Prognostic value of baseline total metabolic tumor volume (TMTV0) measured on FDG-PET/CT in patients with peripheral T-cell lymphoma (PTCL). Ann Oncol 27:719–724PubMedCrossRefGoogle Scholar
  39. 39.
    Chang Y, Fu X, Sun Z, Xie X, Wang R, Li Z et al (2017) Utility of baseline, interim and end-of-treatment 18F-FDG PET/CT in extranodal natural killer/T-cell lymphoma patients treated with L-asparaginase/pegaspargase. Sci Rep 7:41057PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Juweid ME, Wiseman GA, Vose JM et al (2005) Response assessment of aggressive non-Hodgkin’s lymphoma by integrated International Workshop Criteria and fluorine-18-fluorodeoxyglucose positron emission tomography. J Clin Oncol 23:4652–4661PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Cheson BD, Pfistner B, Juweid ME et al (2007) Revised response criteria for malignant lymphoma. J Clin Oncol 10:579–586CrossRefGoogle Scholar
  42. 42.
    Juweid ME, Stroobants S, Hoekstra OS et al (2007) Use of positron emission tomography for response assessment of lymphoma: consensus of the Imaging Subcommittee of International Harmonization Project in Lymphoma. J Clin Oncol 10:571–5783CrossRefGoogle Scholar
  43. 43.
    Vassilakopoulos TP, Pangalis GA, Boutsikas G et al (2012) Prognostic factors in patients with Hodgkin lymphoma (HL) and a negative PET/CT after ABVD chemotherapy: potential applications for the design of follow-up strategies. Haematologica 97(Suppl 1):87 (abstr. 218)Google Scholar
  44. 44.
    Engert A, Haverkamp H, Kobe C et al (2012) Reduced-intensity chemotherapy and PET-guided radiotherapy in patients with advanced stage Hodgkin’s lymphoma (HD15 trial): a randomised, open-label, phase 3 non-inferiority trial. Lancet 379:1791–1799PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Barnes JA, LaCasce AS, Zukotynski K et al (2011) End-of-treatment but not interim PET scan predicts outcome in nonbulky limited stage Hodgkin’s lymphoma. Ann Oncol 22:910–915PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Sher DJ, Mauch PM, van den Abbeele A, LaCasce AS, Czerminski J, Ng AK (2009) Prognostic significance of mid- and post-ABVD PET imaging in Hodgkin’s lymphoma: the importance of involved field radiotherapy. Ann Oncol 20:1848–1845PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Radford J, Illidge T, Counsell L et al (2015) Results of a trial of PET-directed therapy for early-stage Hodgkin’s lymphoma. N Engl J Med 372:1598–1607PubMedCrossRefGoogle Scholar
  48. 48.
    Hartridge-Lambert SK, Schoder H, Lim RC, Maragulia JC, Portlock CS (2013) ABVD alone and a PET scan complete remission negates the need for radiologic surveillance in early-stage, nonbulky Hodgkin lymphoma. Cancer 119:1203–1209PubMedCrossRefGoogle Scholar
  49. 49.
    Vassilakopoulos TP, Rontogianni P, Pangalis GA et al (2012) Outcome and prognostic factors in patients with Hodgkin lymphoma (HL) who remain PET/CT-positive after ABVD combination chemotherapy: potential applications for the design of subsequent treatment. Haematologica 97(Suppl 1):562 (abstr. 1404)Google Scholar
  50. 50.
    Radford J, Illidge T, Counsell N, Hancock B, Pettengell R, Johnson P et al (2015) PET score following 3 cycles ABVD has greater prognostic value than pre-treatment risk stratification in the RAPID trial in early stage Hodgkin lymphoma (HL). Hematol Oncol 33(S1):144 (abstr. 082)Google Scholar
  51. 51.
    Kobe C, Kuhnert G, Kahraman D, Haverkamp H, Eich HT, Franke M et al (2014) Assessment of tumor size reduction improves outcome prediction of positron emission tomography/computed tomography after chemotherapy in advanced-stage Hodgkin lymphoma. J Clin Oncol 32:1776–1781PubMedCrossRefGoogle Scholar
  52. 52.
    Vassilakopoulos TP, Pangalis GA, Chatziioannou S et al (2016) PET/CT in patients with primary mediastinal large B-cell lymphoma responding to Rituximab-CHOP: an analysis of 106 patients regarding prognostic significance and implications for subsequent radiotherapy. Leukemia 30:238–242PubMedCrossRefGoogle Scholar
  53. 53.
    Pinnix CC, Dabaja B, Ahmed MA, Chuang HH, Castelloe C, Wogan CF et al (2015) Single-institution experience in the treatment of primary mediastinal B cell lymphoma treated with immunochemotherapy in the setting of response assessment by 18fluorodeoxyglucose positron emission tomography. Int J Radiat Oncol Biol Phys 92:113–121PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Filippi AR, Piva C, Giunta F et al (2013) Radiation therapy in primary mediastinal B-cell lymphoma with positron emission tomography positivity after rituximab chemotherapy. Int J Radiat Oncol Biol Phys 87:311–316PubMedCrossRefGoogle Scholar
  55. 55.
    Savage KJ, Yenson PR, Shenkier T et al (2012) The outcome of primary mediastinal large B-cell lymphoma (PMBCL) in the R-CHOP treatment era. Blood (ASH Annual Meeting Abstracts) 120:Abstract 303Google Scholar
  56. 56.
    Dunleavy K, Pittaluga S, Maeda LS et al (2013) Dose-adjusted EPOCH-rituximab therapy in primary mediastinal B-cell lymphoma. N Engl J Med 368:1408–1416PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Filippi AR, Piva C, Levis M, Chiapella A, Caracciolo D, Bello M et al (2016) Prognostic role of pre-radiotherapy FDG-PET for primary mediastinal B-cell lymphomas treated with R-CHOP or R-CHOP-like chemotherapy plus radiation. Int J Radiat Oncol Biol Phys 95:1239–1243PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Ceriani L, Martelli M, Gospodarowicz MK, Ricardi U, Ferreri AJM, Chiapella A et al (2017) PET/CT 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 97:42–49PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Vassilakopoulos TP, Pangalis GA, Polliack A (2015) A “PET” topic in primary mediastinal large B-cell lymphoma: positive or negative, and how to handle it in the end. Leuk Lymphoma 56:3–5PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Kanemasa Y, Shimoyama T, Sasaki Y, Tamura M, Sawada T, Omuro Y et al (2017) Analysis of prognostic value of complete response by PET-CT and further stratification by clinical and biological markers in DLBCL patients. Med Oncol 34:29PubMedCrossRefGoogle Scholar
  61. 61.
    Thomas A, Gingrich RD, Smith BJ et al (2010) 18-fluoro-deoxyglucose positron emission tomography report interpretation as predictor of outcome in diffuse large B-cell lymphoma including analysis of “indeterminate” reports. Leuk Lymphoma 51:439–446PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Dabaja BS, Phan J, Mawlawi O, Medeiros LJ, Etzel C, Liang FW et al (2013) Clinical implications of positron emission tomography-negative residual computed tomography masses after chemotherapy for diffuse large B-cell lymphoma. Leuk Lymphoma 54:2631–2638PubMedCrossRefGoogle Scholar
  63. 63.
    Sehn LH, Klasa R, Shenkier T, Villa D, Slack GW, Gascoyne RD et al (2013) Long-term experience with PET-guided consolidative radiation therapy (XRT) in patients with advanced stage diffuse large B-cell lymphoma (DLBCL) treated with R-CHOP. Hematol Oncol 31(Suppl.1):137 (abstr. 123)Google Scholar
  64. 64.
    Vassilakopoulos TP, Kanellopoulos A, Papageorgiou S, Pangalis GA, Anastasopoulou A, Moschogianni M et al (2014) Clinical implications and prognostic significance of positron emission tomography (PET/CT) in patients with diffuse large B-cell lymphoma (DLBCL) after R-CHOP chemoimmunotherapy. Haematologica 99(Suppl 1):702 (abstr. 1831)Google Scholar
  65. 65.
    Witzig TE, Tobinai K, Rigacci L, Ikeda T, Vanazzi A, Hino M et al (2018) Adjuvant everolimus in high-risk diffuse large B-cell lymphoma: final results from the PILLAR-2 randomized phase III trial. Ann Oncol 29:707–714PubMedCrossRefGoogle Scholar
  66. 66.
    Mamot C, Klingbiel D, Hitz F, Renner C, Pabst T, Driessen C et al (2015) 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 33:2523–2529PubMedCrossRefGoogle Scholar
  67. 67.
    Raemaekers JM, André MP, Federico M, Girinsky T, Oumedaly R, Brusamolino E et al (2014) Omitting radiotherapy in early positron emission tomography-negative stage I/II Hodgkin lymphoma is associated with an increased risk of early relapse: clinical results of the preplanned interim analysis of the randomized EORTC/LYSA/FIL H10 trial. J Clin Oncol 32:1188–1194PubMedCrossRefGoogle Scholar
  68. 68.
    André MP, Girinsky T, Federico M, Reman O, Fortpied C, Gotti M et al (2017) Early positron emission tomography response-adapted treatment in stage I and II Hodgkin lymphoma: final results of the randomized EORTC/LYSA/FIL H10 trial. J Clin Oncol 35:1786–1794PubMedCrossRefGoogle Scholar
  69. 69.
    Picardi M, De Renzo A, Pane F et al (2007) Randomized comparison of consolidation radiation versus observation in bulky Hodgkin’s lymphoma with post-chemotherapy negative positron emission tomography scans. Leuk Lymphoma 48:1721–1727PubMedCrossRefGoogle Scholar
  70. 70.
    Hutchings M, Loft A, Hansen M et al (2006) FDG-PET after two cycles of chemotherapy predicts treatment failure and progression-free survival in Hodgkin lymphoma. Blood 107:52–59PubMedCrossRefGoogle Scholar
  71. 71.
    Gallamini A, Hutchings M, Rigacci L et al (2007) Early interim 2-[18F]fluoro-2-deoxy-D-glucose positron emission tomography is prognostically superior to international prognostic score in advanced-stage Hodgkin’s lymphoma: a report from a joint Italian-Danish study. J Clin Oncol 25:3746–3752PubMedCrossRefGoogle Scholar
  72. 72.
    Moskowitz CH, Schoder H, Teruya-Feldstein J et al (2010) Risk-adapted dose-dense immunochemotherapy determined by interim FDG-PET in advanced-stage diffuse large B-cell lymphoma. J Clin Oncol 28:1896–1903PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Gallamini A, Barrington SF, Biggi A, Chauvie S, Kostakoglou L, Gregianin M et al (2014) The predictive role of interim positron emission tomography for Hodgkin lymphoma treatment outcome is confirmed using the interpretation criteria of the Deauville five-point scale. Haematologica 99:1107–1113PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Kostakoglu L, Schoder H, Johnson JL et al (2012) Interim FDG PET imaging in stage I/II non bulky Hodgkin lymphoma: would using combined PET and CT criteria better predict response than each test alone? Leuk Lymphoma 53:2143–2150PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Casasnovas O, Brice P, Bouabdallah R, Salles GA, Stamatoullas A, Dupuis J et al (2015) Randomized phase III study comparing an early PET driven treatment de-escalation to a not PET-monitored strategy in patients with advanced stages Hodgkin lymphoma: interim analysis of the AHL2011 Lysa study. Blood 126:577 (abstract)Google Scholar
  76. 76.
    Borchmann P, Haverkamp H, Lohri A, Mey U, Kreissl S, Greil R et al (2017) Progression free survival of early interim PET positive patients with advanced stage Hodgkin’s lymphoma treated with BEACOPPescalated alone or in combination with rituximab (HD18): an open-label, international, randomized phase 3 study by the German Hodgkin Study Group. Lancet Oncol 18:454–463PubMedCrossRefGoogle Scholar
  77. 77.
    Gallamini A, Patti C, Viviani S et al (2011) Early chemotherapy intensification with BEACOPP in advanced-stage Hodgkin lymphoma patients with a interim-PET positive after two ABVD courses. Br J Haematol 152:551–560PubMedCrossRefGoogle Scholar
  78. 78.
    Johnson P, Federico M, Kirkwood A, Fossa A, Berkahn L, Carella A et al (2016) Adapted treatment guided by interim PET-CT scan in advanced Hodgkin’s lymphoma. N Engl J Med 374:2419–2429PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Press O, Li H, Schoder H, Straus DJ, Moskowitz CA, LeBlanc M et al (2016) 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. J Clin Oncol 34:2020–2027PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Gallamini A, Tarella C, Viviani S, Rossi A, Patti C, Mulé A et al (2018) Early chemotherapy intensification with escalated BEACOPP in patients with advanced-stage Hodgkin lymphoma with a positive interim positron rmission tomography/computed tomography scan after two ABVD cycles: long-term results of the GITIL/FIL HD 0607 trial. J Clin Oncol 36:454–462PubMedCrossRefGoogle Scholar
  81. 81.
    Ganesan P, Rajendranath R, Kannan K, Radhakrishnan V, Ganesan TS, Udupa K et al (2015) Phase II study of interim PET-CT-guided response-adapted therapy in advanced Hodgkin’s lymphoma. Ann Oncol 26:1170–1174PubMedCrossRefGoogle Scholar
  82. 82.
    Vassilakopoulos T, Rondogianni F, Boutsikas G, Assimakopoulos I, Chatziioannou S, Moschogiannis M et al (2015) PET/CT for the early interim evaluation of response in advanced Hodgkin lymphoma after ABVDx2: effective salvage with BEACOPP but low negative predictive value for stage IV. Hematol Oncol 33(S1):313 (abstr. 463)Google Scholar
  83. 83.
    Vassilakopoulos TP, Johnson PWM (2016) Treatment of advanced-stage Hodgkin lymphoma. Semin Hematol 53:171–179PubMedCrossRefGoogle Scholar
  84. 84.
    Zinzani PL, Broccoli A, Gioia D, Castagnoli A, Ciccone G, Evangelista A et al (2016) Interim positron emission tomography response-adapted therapy in advanced-stage Hodgkin lymphoma: final results of the phase II part of the HD0801 study. J Clin Oncol 34:1376–1385PubMedCrossRefGoogle Scholar
  85. 85.
    Oki Y, Chuang H, Chasen B, Jessop A, Pan T, Fanale M et al (2014) The prognostic value of interim positron emission tomography scan in patients with classical Hodgkin lymphoma. Br J Haematol 165:112–116PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Cimino G, Zaucha JM, Cirillo S, Saviolo C, Hutchings M, El-Galaly TC et al (2014) The complementary prognostic role of baseline and interim PET in predicting treatment outcome in advanced-stage Hodgkin lymphoma. Blood (ASH Annual Meeting Abstracts) 124:Abstr. 4405Google Scholar
  87. 87.
    Agostinelli C, Gallamini A, Stracqualursi L, Agati P, Tripodo C, Fuligni F et al (2016) The combined role of biomarkers and interim PET scan in prediction of treatment outcome in classical Hodgkin’s lymphoma: a retrospective, European, multicenter cohort study. Lancet Hematol 3:e467–e479CrossRefGoogle Scholar
  88. 88.
    Borchmann P, Goergen H, Kobe C, Lohri A, Greil R, Eichenauer DA et al (2018) PET-guided treatment in patients with advanced-stage Hodgkin’s lymphoma (HD18): final results of an open-label, international, randomised phase 3 trial by the German Hodgkin Study Group. Lancet 390:2790–2802CrossRefGoogle Scholar
  89. 89.
    Itti E, Meignan M, Berriolo-Riedinger A, Biggi A, Cashen AF, Verra P et al (2013) 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 40:1312–1320PubMedCrossRefGoogle Scholar
  90. 90.
    Casasnovas RO, Meignan M, Berriolo-Riedinger A et al (2011) SUVmax reduction improves early prognosis value of interim positron emission tomography scans in diffuse large B-cell lymphoma. Blood 118:37–43PubMedCrossRefGoogle Scholar
  91. 91.
    Duehrsen U, Müller S, Rekowski J, Hertenstein B, Franzius C, Mesters R et al (2016) Positron emission tomography (PET) guided therapy of aggressive lymphomas – interim PET-based outcome prediction and treatment changes in patients with B cell lymphomas participating in the PETAL trial. Blood. (ASH Annual Meeting Abstracts) 128:Abstr. 1857Google Scholar
  92. 92.
    Pardal E, Coronado M, Martín A, Grande C, Marín-Niebla A, Panizo C et al (2014) Intensification treatment based on early FDG-PET in patients with high-risk diffuse large B-cell lymphoma: a phase II GELTAMO trial. Br J Haematol 167:327–336PubMedCrossRefGoogle Scholar
  93. 93.
    Safar V, Dupuis J, Itti E, Jardin F, Fruchart C, Bardet S et al (2012) Interim [18F]fluorodeoxyglucose positron emission tomography scan in diffuse large B-cell lymphoma treated with anthracycline-based chemotherapy plus rituximab. J Clin Oncol 30:184–190PubMedCrossRefGoogle Scholar
  94. 94.
    Hertzberg M, Gandhi MK, Trotman J, Butcher B, Taper J, Johnston A et al (2017) Early treatment intensification with R-ICE and 90Y-ibritumomab tiuxetan (Zevalin)-BEAM stem cell transplantation in patients with high-risk diffuse large B-cell lymphoma patients and positive interim PET after 4 cycles of R-CHOP-14. Haematologica 102:356–363PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Swinnen LJ, Li H, Quon A, Gascoyne R, Hong F, Ranheim EA et al (2015) 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 170:56–65PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Sehn LH, Hardy ELG, Gill KK, Al-Tourah AJ, Shustik J, Macpherson MA et al (2014) Phase 2 trial of interim PET scan-tailored therapy in patients with advanced stage diffuse large B-cell lymphoma (DLBCL) in British Columbia (BC). Blood (ASH Annual Meeting Abstracts) 124:Abstr. 392Google Scholar
  97. 97.
    Moskowitz C, Hamlin PA, Maragulia J, Meikle J, Zelenetz AD (2010) Sequential dose-dense RCHOP followed by ICE consolidation (MSKCC protocol 01-142) without radiotherapy for patients with primary mediastinal large B-cell lymphoma. Blood 116:abstr. 420CrossRefGoogle Scholar
  98. 98.
    Avigdor A, Sirotkin T, Kedmi M, Ribakovsy E, Berkowicz M, Davidovitz Y et al (2014) The impact of R-VACOP-B and interim FDG-PET/CT on outcome in primary mediastinal large B cell lymphoma. Ann Hematol 93:1297–1304PubMedCrossRefGoogle Scholar
  99. 99.
    Huttmann A, Müller SP, Rekowski J, Hertenstein B, Franzius C, Franzke A et al (2016) Positron emission tomography (PET) guided therapy of aggressive lymphomas – interim PET-based outcome prediction and treatment changes in patients with T cell lymphomas participating in the PETAL trial. Blood. (ASH Annual Meeting Abstracts) 128:Abstr. 185Google Scholar
  100. 100.
    Schot BW, Zijlstra JM, Sluiter WJ et al (2007) Early FDG-PET assessment in combination with clinical risk scores determines prognosis in recurring lymphoma. Blood 109:486–491PubMedCrossRefGoogle Scholar
  101. 101.
    Terasawa T, Dahabreh I, Nihashi T (2010) Fluorine-18-fluorodeoxyglycose positron emission tomography in response assessment before high-dose chemotherapy for lymphoma: a systematic review and meta-analysis. Oncologist 15:750–759PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Poulou LS, Thanos L, Ziakas PD (2010) Unifying the predictive value of pretransplant FDG PET in patients with lymphoma: a review and meta-analysis of published trials. Eur J Nucl Med Mol Imaging 37:156–162PubMedCrossRefGoogle Scholar
  103. 103.
    Angelopoulou MK, Moschogiannis M, Rondogianni P, Tsirkinidis P, Nikaki A, Chatziioannou S et al (2013) PET/CT in the setting of autologous stem cell transplantation (ASCT) for relapsed/refractory Hodgkin lymphoma (HL): performance of various interpretation systems. Haematologica 98(s2):Abstr. P119Google Scholar
  104. 104.
    Moskowitz AJ, Yahalom J, Kewalramani T et al (2010) Pretransplantation functional imaging predicts outcome following autologous stem cell transplantation for relapsed and refractory Hodgkin lymphoma. Blood 116:4934–4937PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Adams HJA, Kwee TC (2016) Prognostic value of pretransplant FDG-PET in refractory/relapsed Hodgkin lymphoma treated with autologous stem cell transplantation: systematic review and meta-analysis. Ann Hematol 95:695–706PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Moskowitz C, Nademanee A, Masszi T, Agura E, Holowiecki J, Abidi M et al (2015) Brentuximab vedotin as consolidation therapy after autologous stem-cell transplantation in patients with Hodgkin’s lymphoma at risk of relapse or progression (AETHERA): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 385:1853–1862PubMedCrossRefGoogle Scholar
  107. 107.
    Younes A, Santoro A, Shipp M, Zinzani P, Timmerman J, Ansell S et al (2016) Nivolumab for classical Hodgkin’s lymphoma after failure of both autologous stem-cell transplantation and brentuximab vedotin: a multicentre, multicohort, single-arm phase 2 trial. Lancet Oncol 17:1283–1294PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Chen R, Zinzani PL, Fanale MA, Armand P, Johnson NA, Brice P et al (2017) Phase II study of the efficacy and safety of pembrolizumab for relapsed/refractory classic Hodgkin lymphoma. J Clin Oncol 35:2125–2132PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Zinzani PL, Ribrag V, Moskowitz CH, Michot JM, Kuruvilla J, Balakumaran A et al (2017) Safety and tolerability of pembrolizumab in patients with relapsed/refractory primary mediastinal large B-cell lymphoma. Blood 130:267–270PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Cheson BD, Ansell S, Schwartz L, Gordon LI, Advani R, Jacene HA et al (2016) Refinement of the Lugano Classification response criteria in the era of immunomodulatory therapy. Blood 128:2489–2496PubMedCrossRefGoogle Scholar
  111. 111.
    Armand P, Engert A, Younes A, Fanale M, Santoro A, Zinzani PL (2018) Nivolumab for relapsed/refractory classic Hodgkin lymphoma after failure of autologous hematopoietic cell transplantation: extended follow-up of the multicohort single-arm phase II CheckMate 205 trial. J Clin Oncol. PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Younes A, Hilden P, Coiffier B, Hagenbeek A, Salles G, Wilson W et al (2017) International Working Group consensus response evaluation criteria in lymphoma (RECIL 2017). Ann Oncol 28: 1436–1447.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Theodoros P. Vassilakopoulos
    • 1
  • Vassilios K. Prassopoulos
    • 2
  1. 1.Department of HaematologyNational and Kapodistrian University of Athens, Laikon General HospitalAthensGreece
  2. 2.Departments of Nuclear Medicine and PET/CTHygeia HospitalAthensGreece

Personalised recommendations