Positron Emission Tomography in Modern Management of Lymphomas

REVIEWS , ,

IP Aslanidi, OV Mukhortova, TA Katunina, IV Ekaeva, MG Shavman

A.N. Bakulev Scientific Center of Cardiovascular Surgery, 135 Rublevskoe sh., Moscow, Russian Federation, 121552

For correspondence: Ol’ga Valentinovna Mukhortova, DSci, 135 Rublevskoe sh., Moscow, Russian Federation, 121552; Tel.: +7(495)414-77-31; e-mail: olgamukhortova@yandex.ru

For citation: Aslanidi IP, Mukhortova OV, Katunina TA, et al. Positron Emission Tomography in Modern Management of Lymphomas. Clinical oncohematology. 2015;8(1):13–25 (In Russ).

ABSTRACT

Objective. The objective is to determine areas of effective application of positron emission tomography (PET) with fluorodeoxyglucose labeled with 18-fluorine (18F-FDG) in patients with lymphomas.

Methods. 56 scientific papers published in 2005–2014 were examined. They analyzed results of recent large studies of PET in patients with lymphomas.

Results. 18F-FDG PET has become an essential part of a diagnostic algorithm for patients with lymphomas which are characterized by active accumulation of 18F-FDG. High precision of PET in patients with some types of lymphomas permit to use this method effectively in clinical practice for staging of the disease, assessment of the treatment efficacy, more precise diagnosis of the relapse prevalence, assessment of results of the anti-relapse therapy, as well as in case of suspected lymphoma transformation. The use of PET at other stages of treatment of lymphoma patients is still pending further scientific research. In case of indolent lymphomas with known low glycolytic activity or lymphomas of rare histological types, PET is used for assessment of the treatment efficacy only if baseline study results (before initiation of treatment) are available. The Deauville five-score scale criteria should be used for assessment of the treatment efficacy. Timely examination during antitumor treatment permits to increase the precision of the PET diagnosing significantly. Solitary foci found by PET are crucial for the choice of treatment and they should be verified by other diagnostic techniques. It is considered unreasonable to use PET for follow-up observation over patients in remission.

Conclusions. PET is a gold standard for staging and assessing the treatment efficacy of lymphomas characterized by active accumulation of 18F-FDG.

Keywords: PET, lymphoma, international guidelines, Deauville five-score scale.

Received: November 14, 2014

Accepted: November 18, 2014

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REFERENCES

  1. Wood KA, Hoskin PJ, Saunders MI. Positron Emission Tomography in Oncology: A Review. Clin Oncol. 2007;19(4):237–55. doi: 10.1016/j.clon.2007.02.001.
  2. Cheson BD. Role of functional imaging in the management of lymphoma. J Clin Oncol. 2011;29(14):1844–54. doi: 10.1200/jco.2010.32.5225.
  3. Collins CD. PET in lymphoma. Cancer Imaging. 2006;6:S63–S70. doi: 10.1102/1470-7330.2006.9013.
  4. Boellaard R, O’Doherty MJ, Weber WA, et al. FDG PET and PET/CT: EANM procedure guidelines for tumor PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37(7):181–200. doi: 10.1007/s00259-010-1459-4.
  5. Weiler-Sagie M, Bushelev O, Epelbaum R, et al. (18)F-FDG avidity in lymphoma readdressed: A study of 766 patients. J Nucl Med. 2010;51(1):25–30. doi: 10.2967/jnumed.109.067892.
  6. Kostakoglu L, Cheson D. State-of-the-art research on Lymphomas: role of molecular imaging for staging, prognostic evaluation, and treatment response. Front Oncol. 2013;3:212. doi: 10.3389/fonc.2013.00212.
  7. Cheson BD, Fisher RI, Barrington SF, et al. Recommendations for Initial Evaluation, Staging, and Response Assessment of Hodgkin and Non-Hodgkin Lymphoma: The Lugano Classification. J Clin Oncol. 2014;32(27):3059–67. doi: 10.1200/jco.2013.54.8800.
  8. Barrington SF, Mikhaeel NG, Kostakoglu L, et al. Role of Imaging in the Staging and Response Assessment of Lymphoma: Consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol. 2014;32(27):3048–58. doi: 10.1200/jco.2013.53.5229.
  9. Engert A, Haverkamp H, Kobe C, et al. 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. The Lancet. 2012;379(9828):1791–9. doi: 10.1016/s0140-6736(11)61940-5.
  10. Thomson KJ, Kayani I, Ardeshna K, et al. A response-adjusted PET-based transplantation strategy in primary resistant and relapsed Hodgkin lymphoma. Leukemia. 2013;27(6):1419–22. doi: 10.1038/leu.2012.318.
  11. Hutchings M. FDG-PET response-adapted therapy: is 18F-fluorodeoxyglucose positron emission tomography a safe predictor for a change of therapy? Hematol Oncol Clin North Am. 2014;28(1):87–103. doi: 10.1016/j.hoc.2013.10.008.
  12. Radford J, Barrington S, Counsell N, et al. Involved field radiotherapy vs no further treatment in patients with clinical stages IA and IIA Hodgkin lymphoma and a ‘negative’ PET scan after 3 cycles ABVD: results of the UK NCRI RAPID trial. Blood. 2012;120(21):547.
  13. Barrington SF, Mikhaeel NG. When should FDG-PET be used in the modern management of lymphoma? Br J Haematol. 2014;164(3):315–28. doi: 10.1111/bjh.12601.
  14. Omur O, Baran Y, Oral A, et al. Fluorine-18 fluorodeoxyglucose PET-CT for extranodal staging of non-Hodgkin and Hodgkin lymphoma. Diagn Interv Radiol. 2014;20(2):185–92. doi: 10.5152/dir.2013.13174.
  15. Luminari S, Biasoli I, Arcaini L, et al. The use of FDG-PET in the initial staging of 142 patients with follicular lymphoma: A retrospective study from the FOLL05 randomized trial of the Fondazione Italiana Linfomi. Ann Oncol. 2013;24(8):2108–12. doi: 10.1093/annonc/mdt137.
  16. Pelosi E, Pregno P, Penna D, et al. Role of whole-body [18F] fluorodeoxyglucose positron emission tomography/computed tomography (FDGPET/CT) and conventional techniques in the staging of patients with Hodgkin and aggressive non Hodgkin lymphoma. Radiol Med. 2008;113(4):578–90. doi: 10.1007/s11547-008-0264-7.
  17. Casulo C, Schoder H, Feeney J, et al. FDG PET in the staging and prognosis of T cell lymphoma. Leuk Lymphoma. 2013;54(10):2163–7. doi: 10.3109/10428194.2013.767901.
  18. Scott AM, Gunawardana DH, Wong J, et al. Positron emission tomography changes management, improves prognostic stratification and is superior to gallium scintigraphy in patients with low-grade lymphoma: results of a multicentre prospective study. Eur J Nucl Med Mol Imaging. 2009;36(3):347–53. doi: 10.1007/s00259-008-0958-z.
  19. Cortes-Romera M, Sabate-Llobera A, Mercadal-Vilchez S, et al. Bone marrow evaluation in initial staging of lymphoma: 18F-FDG PET/CT versus bone marrow biopsy. Clin Nucl Med. 2014;39(1):e46–52. doi: 10.1097/rlu.0b013e31828e9504.
  20. Adams HJ, Kwee TC, Vermoolen MA, et al. Whole-body MRI for the detection of bone marrow involvement in lymphoma: prospective study in 116 patients and comparison with FDG-PET. Eur Radiol. 2013;23(8):2271–8. doi: 10.1007/s00330-013-2835-9.
  21. Castellucci P, Nanni C, Farsad M, et al. Potential pitfalls of 18F-FDG PET in a large series of patients treated for malignant lymphoma: prevalence and scan interpretation. Nucl Med Comm. 2005;26(8):689–94. doi: 10.1097/01.mnm.0000171781.11027.bb.
  22. Storto G, Di Giorgio E, De Renzo A, et al. Assessment of metabolic activity by PET-CT with F-18-FDG in patients with T-cell lymphoma. Br J Haematol. 2010;151(2):195–7. doi: 10.1111/j.1365-2141.2010.08335.x.
  23. Ansell SM, Armitage JO. Positron Emission Tomographic Scans in Lymphoma: Convention and Controversy. Mayo Clin Proc. 2012;87(6):571–80. doi: 10.1016/j.mayocp.2012.03.006.
  24. Araf S, Montoto S. The use of interim 18F-fluorodeoxyglucose PET to guide therapy in lymphoma. Fut Oncol. 2013;9(6):807–15. doi: 10.2217/fon.13.55.
  25. Zinzani PL, Rigacci L, Stefoni V, et al. Early interim 18F-FDG PET in Hodgkin’s lymphoma: Evaluation on 304 patients. Eur J Nucl Med Mol Imaging. 2012;39(1):4–12. doi: 10.1007/s00259-011-1916-8.
  26. Moulin-Romsee G, Hindie E, Cuenca X, et al. (18) F-FDG PET/CT bone/bone marrow findings in Hodgkin’s lymphoma may circumvent the use of bone marrow trephine biopsy at diagnosis staging. Eur J Nucl Med Mol Imaging. 2010;37(6):1095–105. doi: 10.1007/s00259-009-1377-5.
  27. Hamilton R, Andrews I, McKay P, et al. Loss of utility of bone marrow biopsy as a staging evaluation for Hodgkin lymphoma in the positron emission tomography-computed tomography era: a West of Scotland study. Leuk Lymphoma. 2014;55(5):1049–52. doi: 10.3109/10428194.2013.821201.
  28. Berthet L, Cochet A, Kanoun S, et al. 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. 2013;54(8):1244–50. doi: 10.2967/jnumed.112.114710.
  29. El-Galaly TC, d’Amore F, Mylam KJ, et al. Routine bone marrow biopsy has little or no therapeutic consequence for positron emission tomography/computed tomography-staged treatment-naive patients with Hodgkin lymphoma. J Clin Oncol. 2012;30(36):4508–14. doi: 10.1200/jco.2012.42.4036.
  30. El-Galaly TC, Hutchings M, Mylam KJ, et al. Impact of 18F-FDG PET/CT Staging in Newly Diagnosed Classical Hodgkin Lymphoma: Less Cases with Stage I Disease and More with Skeletal Involvement. Leuk Lymphoma. 2014;55(10):2349–55. doi: 10.3109/10428194.2013.875169.
  31. Cheng G, Alavi A. Value of 18F-FDG PET versus iliac biopsy in the initial evaluation of bone marrow infiltration in the case of Hodgkin’s disease: a meta-analysis. Nucl Med Commun. 2013;34(1):25–31. doi: 10.1097/mnm.0b013e32835afc19.
  32. Chen YK, Yeh CL, Tsui CC, et al. F-18 FDG PET for evaluation of bone marrow involvement in non-Hodgkin lymphoma: A meta-analysis. Clin Nucl Med. 2011;36(7):553–9. doi: 10.1097/rlu.0b013e318217aeff.
  33. Мухортова О.В., Асланиди И.П., Шурупова И.В. и др. Применение позитронно-эмиссионной томографии для оценки поражения костного мозга у больных злокачественными лимфомами. Медицинская радиология и радиационная безопасность. 2010;2:43–52.
    [Mukhortova OV, Aslanidi IP, Shurupova IV, et al. Use of positron emission tomography for assessment of bone marrow damage in patients with malignant lymphomas. Meditsinskaya radiologiya i radiatsionnaya bezopasnost’. 2010;2:43–52. (In Russ)]
  34. Kashyap R, Lau E, George A, et al. High FDG activity in focal fat necrosis: a pitfall in interpretation of posttreatment PET/CT in patients with non-Hodgkin lymphoma. Eur J Nucl Med Mol Imaging. 2013;40(9):1330–6. doi: 10.1007/s00259-013-2429-4.
  35. Hutchings M, Barrington SF. PET/CT for Therapy Response Assessment in Lymphoma. J Nucl Med. 2009;50(Suppl 1):21S–30S. doi: 10.2967/jnumed.108.05719.
  36. Dabaja BS, Phan J, Mawlawi O, et al. Clinical implications of positron emission tomography – negative residual computed tomography masses after chemotherapy for diffuse large B-cell lymphoma. Leuk Lymphoma. 2013;54(12):2631–8. doi: 10.3109/10428194.2013.784967.
  37. Gallamini A, Barringtom S, Biggi A, et al. 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. 2014;99(6):1107–13. doi: 10.3324/haematol.2013.103218.
  38. Fuertes S, Setoain X, Lopez-Guillermo A, et al. Interim FDG PET/CT as a prognostic factor in diffuse large B-cell lymphoma. Eur J Nucl Med Mol Imaging. 2013;40(4):496–504. doi: 10.1007/s00259-012-2320-8.
  39. Bodet-Milin C, Touzeau C, Leux C, et al. Prognostic impact of 18F-fluorodeoxyglucose positron emission tomography in untreated mantle cell lymphoma: a retrospective study from the GOELAMS group. Eur J Nucl Med Mol Imaging. 2010;37(9):1633–42. doi: 10.1007/s00259-010-1469-2.
  40. Cahu X, Bodet-Milin C, Brissot E, et al. 18F-fluorodeoxyglucose-positron emission tomography before, during and after treatment in mature T/NK lymphomas: a study from the GOELAMS group. Ann Oncol. 2011;22(3):705–11. doi: 10.1093/annonc/mdq415.
  41. Lee H, Kim SK, Kim YI, et al. Early Determination of Prognosis by Interim 3¢-Deoxy-3¢-18F-Fluorothymidine PET in Patients with Non-Hodgkin Lymphoma. J Nucl Med. 2014;55(2):216–22. doi: 10.2967/jnumed.113.124172.
  42. Le Dortz L, De Guibert S, Bayat S, et al. Diagnostic and prognostic impact of 18F-FDG PET/CT in follicular lymphoma. Eur J Nucl Med Mol Imaging. 2010;37(12):2307–14. doi: 10.1007/s00259-010-1539-5.
  43. Lopci E, Zanoni L, Chiti A, et al. FDG PET/CT predictive role in follicular lymphoma. Eur J Nucl Med Mol Imaging. 2012;39(5):864–71. doi: 10.1007/s00259-012-2079-y.
  44. Oki Y, Chuang H, Chasen B, et al. The prognostic value of interim positron emission tomography scan in patients with classical Hodgkin lymphoma. Br J Haematol. 2014;165(1):112–6. doi: 10.1111/bjh.12715.
  45. Bodet-Milin C, Eugene T, Gastinne T. FDG-PET in Follicular Lymphoma Management. J Oncol. 2012:370272. doi: 10.1155/2012/370272.
  46. Sucak GT, Ozkurt ZN, Suyani E, et al. Early post-transplantation positron emission tomography in patients with Hodgkin lymphoma is an independent prognostic factor with an impact on overall survival. Ann Hematol. 2011;90(11):1329–36. doi: 10.1007/s00277-011-1209-0.
  47. Biggi A, Gallamini A, Chauvie S, et al. International validation study for interim PET in ABVD-treated, advanced-stage Hodgkin lymphoma: Interpretation criteria and concordance rate among reviewers. J Nucl Med. 2013;54(5):683–90. doi: 10.2967/jnumed.112.110890.
  48. Nols N, Mounier N, Bouazza S, et al. Quantitative and qualitative analysis of metabolic response at interim PET-scan combined with IPI is highly predictive of outcome in diffuse large B-cell lymphoma. Leuk Lymphoma. 2014;55(4):773–80. doi: 10.3109/10428194.2013.831848.
  49. Gallamini A, Kostakoglu L. Positron emission tomography/computed tomography surveillance in patients with lymphoma: a fox hunt? Haematologica. 2012;97(6):797–9. doi: 10.3324/haematol.2012.063909.
  50. Yoo C, Lee DH, Kim JE, et al. Limited role of interim PET/CT in patients with diffuse large B-cell lymphoma treated with R-CHOP. Ann Hematol. 2011;90(7):797–802. doi: 10.1007/s00277-010-1135-6.
  51. Pregno P, Chiappella A, Bello M, et al. Interim 18-FDG-PET/CT failed to predict the outcome in diffuse large B-cell lymphoma patients treated at the diagnosis with rituximab-CHOP. Blood. 2012;119(9):2066–73. doi: 10.1182/blood-2011-06-359943.
  52. Safar V, Dupuis J, Itti E, et al. Interim [18F]fluorodeoxyglucose positron emission tomography scan in diffuse large B-cell lymphoma treated with anthracycline-based chemotherapy plus rituximab. J Clin Oncol. 2012;30(2):184–90. doi: 10.1200/JCO.2011.38.2648.
  53. Terasawa T, Dahabreh IJ, Nihashi T. Fluorine-18-Fluorodeoxyglucose positron emission tomography in response assessment before high-dose chemotherapy for lymphoma: a systematic review and meta-analysis. The Oncologist. 2010;15(7):750–9. doi: 10.1634/theoncologist.2010-0054.
  54. Sucak GT, Ozkurt ZN, Suyani E, et al. Early post-transplantation positron emission tomography in patients with Hodgkin lymphoma is an independent prognostic factor with an impact on overall survival. Ann Hematol. 2011;90(11):1329–36. doi: 10.1007/s00277-011-1209-0.
  55. Von Tresckow B, Engert A. The emerging role of PET in Hodgkin lymphoma patients receiving autologous stem cell transplant. Expert Rev Hematol. 2012;5(5):483–6. doi: 10.1586/ehm.12.41.
  56. Bodet-Milin C, Kraeber-Bodere F, Moreau P, et al. Investigation of FDG-PET/CT imaging to guide biopsies in the detection of histological transformation of indolent lymphoma. Haematologica. 2008;93(3):471–2. doi: 10.3324/haematol.12013.