Download PDF
Rofo 2020; 192(07): 657-668
DOI: 10.1055/a-1091-8897
Review
© Georg Thieme Verlag KG Stuttgart · New York

Criteria-Based Imaging and Response Evaluation of Lymphoma 20 Years After Cheson: What is New?

A Review of the Current Classifications Article in several languages: English | deutsch
Christopher Skusa
1   Institute of Diagnostic and Interventional Radiology, Pediatric Radiology and Neuroradiology, Rostock University Medical Center, Rostock, Germany
,
Marc-André Weber
1   Institute of Diagnostic and Interventional Radiology, Pediatric Radiology and Neuroradiology, Rostock University Medical Center, Rostock, Germany
,
Sebastian Böttcher
2   Department of Medicine, Clinic III – Hematology, Oncology, Palliative Medicine, Rostock University Medical Center, Rostock, Germany
,
Kolja M. Thierfelder
1   Institute of Diagnostic and Interventional Radiology, Pediatric Radiology and Neuroradiology, Rostock University Medical Center, Rostock, Germany
› Author Affiliations
Further Information

Publication History

07 September 2019

10 December 2019

Publication Date:
26 March 2020 (online)

Also available at
   Permissions and Reprints

Abstract

Background The rapid progress in oncology research requires numerous new scientific publications. This article aims to provide an overview of criteria-based imaging and response evaluation of lymphoma according to the current status of knowledge. In fact, common criteria for evaluating data, especially imaging response evaluation, are essential for comparability of studies. While criteria-based classifications of solid tumors have been established for some time, there are now increasing classifications of lymphoma diseases. The purpose of this review is to describe the development of criteria-based evaluation of lymphoma diseases with a special focus on imaging up to current guidelines.

Methods Literature review based on PubMed including the languages English and German was performed. This review article includes the most important criteria-based response evaluations of lymphoma published between January 1999 and July 2019.

Results and Conclusion The two latest classifications of response evaluation of lymphoma are: The Lugano classification, which has been steadily developed over the past 20 years and has been specially adapted to technical progress, as well as the evaluation method RECIL (Response Evaluation Criteria In Lymphoma), which is based on the RECIST (Response Evaluation Criteria in Solid Tumors) classification already established for solid tumors. Significant imaging components of both classifications are the anatomical measurement and measurement of the metabolic response of the manifestation of lymphoma using positron emission tomography (PET/CT).

Key Points: 

  • Standardized criteria-based response evaluations are essential for the objective and comparable analysis of new drugs for the treatment of lymphoma diseases.

  • The latest classification RECIL has significantly simplified treatment evaluation and has established a better comparability to the therapeutic evaluation of solid tumors according to RECIST.

  • Further studies will show the most appropriate classifications depending on study settings.

Citation Format

  • Skusa C, Weber M, Böttcher S et al. Criteria-Based Imaging and Response Evaluation of Lymphoma 20 Years After Cheson: What is New?. Fortschr Röntgenstr 2020; 192: 657 – 667

Key words

lymphoma - CT - PET-CT - staging
 

  • References

  • 1 Stiefelhagen P. Die Therapie der Lymphome ist im Wandel. InFo Hämatologie und Onkologie 2017; 2017: 62-63 . doi:10.1007/s15004-017-5763-z
    PubMedGoogle Scholar
  • 2 Cheson BD, Horning SJ, Coiffier B. et al. Report of an international workshop to standardize response criteria for non-Hodgkin’s lymphomas. NCI Sponsored International Working Group. J Clin Oncol 1999; 17: 1244 . doi:10.1200/JCO.1999.17.4.1244
    CrossrefPubMedGoogle Scholar
  • 3 Lister TA, Crowther D, Sutcliffe SB. et al. Report of a committee convened to discuss the evaluation and staging of patients with Hodgkin’s disease: Cotswolds meeting. J Clin Oncol 1989; 7: 1630-1636 . doi:10.1200/JCO.1989.7.11.1630
    CrossrefPubMedGoogle Scholar
  • 4 Dorfman RE, Alpern MB, Gross BH. et al. Upper abdominal lymph nodes: criteria for normal size determined with CT. Radiology 1991; 180: 319-322 . doi:10.1148/radiology.180.2.2068292
    CrossrefPubMedGoogle Scholar
  • 5 Einstein DM, Singer AA, Chilcote WA. et al. Abdominal lymphadenopathy: spectrum of CT findings. Radiographics 1991; 11: 457-472 . doi:10.1148/radiographics.11.3.1852937
    CrossrefPubMedGoogle Scholar
  • 6 Glazer GM, Gross BH, Quint LE. et al. Normal mediastinal lymph nodes: number and size according to American Thoracic Society mapping. Am J Roentgenol 1985; 144: 261-265 . doi:10.2214/ajr.144.2.261
    CrossrefPubMedGoogle Scholar
  • 7 Kiyono K, Sone S, Sakai F. et al. The number and size of normal mediastinal lymph nodes: a postmortem study. Am J Roentgenol 1988; 150: 771-776 . doi:10.2214/ajr.150.4.771
    CrossrefPubMedGoogle Scholar
  • 8 Steinkamp HJ, Hosten N, Richter C. et al. Enlarged cervical lymph nodes at helical CT. Radiology 1994; 191: 795-798 . doi:10.1148/radiology.191.3.8184067
    CrossrefPubMedGoogle Scholar
  • 9 Cheson BD, Pfistner B, Juweid ME. et al. Revised response criteria for malignant lymphoma. J Clin Oncol 2007; 25: 579-586 . doi:10.1200/JCO.2006.09.2403
    CrossrefPubMedGoogle Scholar
  • 10 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: 3048-3058 . doi:10.1200/JCO.2013.53.5229
    CrossrefPubMedGoogle Scholar
  • 11 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: 3059-3068 . doi:10.1200/JCO.2013.54.8800
    CrossrefPubMedGoogle Scholar
  • 12 Meignan M, Gallamini A, Meignan M. et al. Report on the First International Workshop on Interim-PET-Scan in Lymphoma. Leuk Lymphoma 2009; 50: 1257-1260 . doi:10.1080/10428190903040048
    CrossrefPubMedGoogle Scholar
  • 13 Barrington SF, Qian W, Somer EJ. et al. Concordance between four European centres of PET reporting criteria designed for use in multicentre trials in Hodgkin lymphoma. Eur J Nucl Med Mol Imaging 2010; 37: 1824-1833 . doi:10.1007/s00259-010-1490-5
    CrossrefPubMedGoogle Scholar
  • 14 Gallamini A, Tarella C, Viviani S. et al. Early Chemotherapy Intensification With Escalated BEACOPP in Patients With Advanced-Stage Hodgkin Lymphoma With a Positive Interim Positron Emission Tomography/Computed Tomography Scan After Two ABVD Cycles: Long-Term Results of the GITIL/FIL HD 0607 Trial. J Clin Oncol 2018; 36: 454-462 . doi:10.1200/JCO.2017.75.2543
    PubMedGoogle Scholar
  • 15 Spaepen K, Stroobants S, Dupont P. et al. Early restaging positron emission tomography with (18)F-fluorodeoxyglucose predicts outcome in patients with aggressive non-Hodgkin’s lymphoma. Ann Oncol 2002; 13: 1356-1363 . doi:10.1093/annonc/mdf256
    CrossrefPubMedGoogle Scholar
  • 16 Hutchings M, Mikhaeel NG, Fields PA. et al. Prognostic value of interim FDG-PET after two or three cycles of chemotherapy in Hodgkin lymphoma. Ann Oncol 2005; 16: 1160-1168 . doi:10.1093/annonc/mdi200
    CrossrefPubMedGoogle Scholar
  • 17 Hutchings M, Loft A, Hansen M. et al. FDG-PET after two cycles of chemotherapy predicts treatment failure and progression-free survival in Hodgkin lymphoma. Blood 2006; 107: 52-59 . doi:10.1182/blood-2005-06-2252
    CrossrefPubMedGoogle Scholar
  • 18 Cerci JJ, Pracchia LF, Linardi CC. et al. 18F-FDG PET after 2 cycles of ABVD predicts event-free survival in early and advanced Hodgkin lymphoma. J Nucl Med 2010; 51: 1337-1343 . doi:10.2967/jnumed.109.073197
    CrossrefPubMedGoogle Scholar
  • 19 Borchmann P, Goergen H, Kobe C. et al. 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 2018; 390: 2790-2802 . doi:10.1016/S0140-6736(17)32134-7
    PubMedGoogle Scholar
  • 20 Duhrsen U, Muller S, Hertenstein B. et al. Positron Emission Tomography-Guided Therapy of Aggressive Non-Hodgkin Lymphomas (PETAL): A Multicenter, Randomized Phase III Trial. J Clin Oncol 2018; 36: 2024-2034 . doi:10.1200/JCO.2017.76.8093
    CrossrefPubMedGoogle Scholar
  • 21 Le Roux PY, Gastinne T, Le Gouill S. et al. Prognostic value of interim FDG PET/CT in Hodgkin’s lymphoma patients treated with interim response-adapted strategy: comparison of International Harmonization Project (IHP), Gallamini and London criteria. Eur J Nucl Med Mol Imaging 2011; 38: 1064-1071 . doi:10.1007/s00259-011-1741-0
    CrossrefPubMedGoogle Scholar
  • 22 Kajary K, Molnar Z, Gyorke T. et al. Comparison of the International Harmonization Project, London and Gallamini criteria in the interpretation of 18F-FDG PET/CT examinations after first-line treatment in Hodgkin’s lymphoma. Nucl Med Commun 2014; 35: 169-175 . doi:10.1097/MNM.0000000000000024
    CrossrefPubMedGoogle Scholar
  • 23 Fallanca F, Alongi P, Incerti E. et al. Diagnostic accuracy of FDG PET/CT for clinical evaluation at the end of treatment of HL and NHL: a comparison of the Deauville Criteria (DC) and the International Harmonization Project Criteria (IHPC). Eur J Nucl Med Mol Imaging 2016; 43: 1837-1848 . doi:10.1007/s00259-016-3390-9
    CrossrefPubMedGoogle Scholar
  • 24 Abrey LE, Batchelor TT, Ferreri AJ. et al. Report of an international workshop to standardize baseline evaluation and response criteria for primary CNS lymphoma. J Clin Oncol 2005; 23: 5034-5043 . doi:10.1200/JCO.2005.13.524
    CrossrefPubMedGoogle Scholar
  • 25 Zucca E, Copie-Bergman C, Ricardi U. et al. Gastric marginal zone lymphoma of MALT type: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2013; 24 (Suppl. 06) vi144-vi148 . doi:10.1093/annonc/mdt343
    CrossrefPubMedGoogle Scholar
  • 26 Olsen EA, Whittaker S, Kim YH. et al. Clinical end points and response criteria in mycosis fungoides and Sezary syndrome: a consensus statement of the International Society for Cutaneous Lymphomas, the United States Cutaneous Lymphoma Consortium, and the Cutaneous Lymphoma Task Force of the European Organisation for Research and Treatment of Cancer. J Clin Oncol 2011; 29: 2598-2607 . doi:10.1200/JCO.2010.32.0630
    CrossrefPubMedGoogle Scholar
  • 27 Hallek M, Cheson BD, Catovsky D. et al. iwCLL guidelines for diagnosis, indications for treatment, response assessment, and supportive management of CLL. Blood 2018; 131: 2745-2760 . doi:10.1182/blood-2017-09-806398
    CrossrefPubMedGoogle Scholar
  • 28 Cheson BD, Ansell S, Schwartz L. et al. Refinement of the Lugano Classification lymphoma response criteria in the era of immunomodulatory therapy. Blood 2016; 128: 2489-2496 . doi:10.1182/blood-2016-05-718528
    PubMedGoogle Scholar
  • 29 Cheson BD. Rethinking clinical response and outcome assessment in a biologic age. Curr Oncol Rep 2015; 17: 27 . doi:10.1007/s11912-015-0452-2
    CrossrefPubMedGoogle Scholar
  • 30 Younes A, Hilden P, Coiffier B. et al. International Working Group consensus response evaluation criteria in lymphoma (RECIL 2017). Ann Oncol 2017; 28: 1436-1447 . doi:10.1093/annonc/mdx097
    CrossrefPubMedGoogle Scholar
  • 31 Eisenhauer EA, Therasse P, Bogaerts J. et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009; 45: 228-247 . doi:10.1016/j.ejca.2008.10.026
    CrossrefPubMedGoogle Scholar
  • 32 Fournier L, Ammari S, Thiam R. et al. Imaging criteria for assessing tumour response: RECIST, mRECIST, Cheson. Diagn Interv Imaging 2014; 95: 689-703 . doi:10.1016/j.diii.2014.05.002
    CrossrefPubMedGoogle Scholar
  • 33 Assouline S, Meyer RM, Infante-Rivard C. et al. Development of adapted RECIST criteria to assess response in lymphoma and their comparison to the International Workshop Criteria. Leuk Lymphoma 2007; 48: 513-520 . doi:10.1080/10428190601078126
    CrossrefPubMedGoogle Scholar
  • 34 Lewis E, Bernardino ME, Salvador PG. et al. Post-therapy CT-detected mass in lymphoma patients: is it viable tissue?. J Comput Assist Tomogr 1982; 6: 792-795
    CrossrefPubMedGoogle Scholar
  • 35 Ganten MK, Weber MA, Ganten TM. Cellular mechanisms of tumor response: clinical demands. Radiologe 2008; 48: 820-831 . doi:10.1007/s00117-008-1739-1
    CrossrefPubMedGoogle Scholar
  • 36 Kovacs G, Robrecht S, Fink AM. et al. Minimal Residual Disease Assessment Improves Prediction of Outcome in Patients With Chronic Lymphocytic Leukemia (CLL) Who Achieve Partial Response: Comprehensive Analysis of Two Phase III Studies of the German CLL Study Group. J Clin Oncol 2016; 34: 3758-3765 . doi:10.1200/JCO.2016.67.1305
    CrossrefPubMedGoogle Scholar
  • 37 Erasmus JJ, Gladish GW, Broemeling L. et al. Interobserver and intraobserver variability in measurement of non-small-cell carcinoma lung lesions: implications for assessment of tumor response. J Clin Oncol 2003; 21: 2574-2582 . doi:10.1200/JCO.2003.01.144
    CrossrefPubMedGoogle Scholar
  • 38 Hopper KD, Kasales CJ, Van Slyke MA. et al. Analysis of interobserver and intraobserver variability in CT tumor measurements. Am J Roentgenol 1996; 167: 851-854 . doi:10.2214/ajr.167.4.8819370
    CrossrefPubMedGoogle Scholar
  • 39 Wessling J, Puesken M, Koch R. et al. MSCT follow-up in malignant lymphoma: comparison of manual linear measurements with semi-automated lymph node analysis for therapy response classification. Röfo 2012; 184: 795-804 . doi:10.1055/s-0032-1312751
    Article in Thieme ConnectPubMedGoogle Scholar
  • 40 Wessling J, Schulke C, Koch R. et al. Therapy response evaluation of malignant lymphoma in a multicenter study: comparison of manual and semiautomatic measurements in CT. Röfo 2014; 186: 768-779 . doi:10.1055/s-0033-1356424
    PubMedGoogle Scholar
  • 41 Winter KS, Hofmann FO, Thierfelder KM. et al. Towards volumetric thresholds in RECIST 1.1: Therapeutic response assessment in hepatic metastases. Eur Radiol 2018; 28: 4839-4848 . doi:10.1007/s00330-018-5424-0
    CrossrefPubMedGoogle Scholar
  • 42 Afaq A, Fraioli F, Sidhu H. et al. Comparison of PET/MRI With PET/CT in the Evaluation of Disease Status in Lymphoma. Clin Nucl Med 2017; 42: e1-e7 . doi:10.1097/RLU.0000000000001344
    CrossrefPubMedGoogle Scholar
  • 43 Atkinson W, Catana C, Abramson JS. et al. Hybrid FDG-PET/MR compared to FDG-PET/CT in adult lymphoma patients. Abdom Radiol (NY) 2016; 41: 1338-1348 . doi:10.1007/s00261-016-0638-6
    CrossrefPubMedGoogle Scholar
  • 44 Lavin PT. An alternative model for the evaluation of antitumor activity. Cancer Clin Trials 1981; 4: 451-457
    PubMedGoogle Scholar
  • 45 Royston P, Altman DG, Sauerbrei W. Dichotomizing continuous predictors in multiple regression: a bad idea. Stat Med 2006; 25: 127-141 . doi:10.1002/sim.2331
    CrossrefPubMedGoogle Scholar