Toward common response evaluation criteria for solid tumors and lymphomas: RECIL and RECIST?
Authors: V. Ribrag
Journal: Annals of Oncology (2017)

Simple and reproducible response criteria are crucial for the clinical evaluation of anticancer drugs. This is based on diagnostic imaging procedures that have the ability to be standardized and adapted to a second independent set of criteria or lecture. Their reproducibility, their simple use by groups conducting clinical trials and their adoption by pharmaceutical companies and regulatory agencies are necessary. Tumor response criteria have been modified during the last decades. These ongoing modifications and improvements were necessary because of the learning curve of the investigators who use these criteria in daily practice, as they have the knowledge of what remains to be improved and the solutions that might be implemented. In parallel, the development of new imaging techniques, such as PET, and their potential efficiency with respect to tumor response assessment led to better criteria especially for lymphoma. However, until now, some differences remained between tumor entities especially between lymphomas and solid tumors. In regard to lymphomas, the first response criteria were published in 1999 by the International Working Group [1.Cheson B.D. Horning S.J. 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: 1244Crossref PubMed Google Scholar]. These guidelines defined complete remission (CR), partial remission (PR), CR unconfirmed, stable disease (SD), relapsed disease, and progressive disease (PD), which were based on physical examination, chest X-ray, computed tomography (CT) scan, single photon emission CT gallium scans, and visual bone marrow evaluation. During the next decade, it became apparent that positron emission tomography (PET), as well as immunohistochemistry and flow cytometry of the bone marrow, could improve response assessment. As a result, the revised 2007 guidelines, which included PET as a component of response assessment primarily for Hodgkin lymphoma and diffuse large B-cell lymphoma (DLBCL), were proposed [2.Cheson B.D. Pfistner B. Juweid M.E. et al.Revised response criteria for malignant lymphoma.J Clin Oncol. 2007; 25: 579-586Crossref PubMed Scopus (3732) Google Scholar]. At that time, PET was recommended for the post-treatment assessment of DLBCL and HL in daily practice, but this approach was still considered exploratory for other lymphoma entities. Further experience with the interpretation of PET scan results subsequently led to the Lugano classification for staging and response assessment, which incorporated PET-CT as a standard component of both the staging and response assessment of FDG-avid histologies; however, CT evaluation for other subtypes was retained in this classification system [3.Cheson B.D. Fisher R.I. Barrington S.F. Australasian Leukaemia and Lymphoma Group Eastern Cooperative Oncology Group European Mantle Cell Lymphoma Consortium Italian Lymphoma Foundation European Organisation for Research Treatment of Cancer/Dutch Hemato-Oncology Group Grupo Español de Médula Ósea German High-Grade Lymphoma Study Group German Hodgkin's Study Group Japanese Lymphorra Study Group Lymphoma Study Association NCIC Clinical Trials Group Nordic Lymphoma Study Group Southwest Oncology Group United Kingdom National Cancer Research Institute et al.Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification.J Clin Oncol. 2014; 32: 3059-3068Crossref PubMed Scopus (2768) Google Scholar]. Despite real improvement in imaging techniques and PET-CT incorporation into the new Lugano classification, tumor burden is still measured on the basis of the sum of the product of tumor diameters in lymphomas, as described in the WHO criteria published in 1981 [4.Miller A.B. Hoogstraten B. Staquet M. Winkler A. Reporting results of cancer treatment.Cancer. 1981; 47: 207-214Crossref PubMed Scopus (7359) Google Scholar]. This bidimensional measurement was rapidly challenged in the field of oncology given the risk of measurement error (an increase of only 12% in each dimension would result in a 25% increase in tumor size); thus, the new RECIST criteria were adopted. Key features of RECIST, as published in 2000, include definitions of the minimum size of measurable lesions, instructions on how many lesions should be considered target lesions (up to 10; a maximum of 5 per organ site), and the use of unidimensional, rather than bidimensional, measures for overall evaluation of tumor burden [5.Therasse P. Arbuck S.G. Eisenhauer E.A. et al.New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada.J Natl Cancer Inst. 2000; 92: 205-216Crossref PubMed Scopus (14467) Google Scholar]. As is typically observed in ‘living’ response criteria, issues arose, and subsequent improvements were included in the new RECIST 1.1 criteria [6.Eisenhauer E.A. Therasse P. Bogaerts J. et al.New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1).Eur J Cancer. 2009; 45: 228-247Abstract Full Text Full Text PDF PubMed Scopus (18101) Google Scholar]. When we compared the newer criteria with the previous RECIST criteria, major changes were observed in RECIST 1.1, including the number of targeted lesions to be assessed (reduced from a maximum of 10 to a maximum of 5 total (and from 5 to 2 per organ, maximum). A second major point for hematology, especially lymphomas, was the introduction of the assessment of pathological lymph nodes. It was then proposed that nodes with a short axis of 15 mm are considered measurable and assessable as target lesions. The short-axis measurement should be included in the sum of lesions in the calculation of tumor response. Nodes that shrink to a short axis of <10 mm are considered normal [7.Schwartz L.H. Bogaerts J. Ford R. et al.Evaluation of lymph nodes with RECIST 1.1.Eur J Cancer. 2009; 45: 261-267Abstract Full Text Full Text PDF PubMed Scopus (211) Google Scholar]. The introduction of pathological lymph nodes as robust targets in RECIST 1.1 after the assessment of a large data sample (>6500 patients) as well as simulation studies and literature reviews has strongly suggested that the use of unidimensional measurements of lymph nodes might be an acceptable method of evaluation (Table 1).Table 1Comparison between the response criteria used and the new RECIL 2017 (taken from Younes et al. [8.Younes A. Hilden P. Coiffier B. et al.International Working Group consensus response evaluation criteria in lymphoma (RECIL 2017).Ann Oncol. 2017; 28: 1436-1447Abstract Full Text Full Text PDF PubMed Scopus (164) Google Scholar])RECIST 1.1LuganoRECIL 2017Number of target lesionsUp to 5Up to 6Up to 3Measurement methodUnidimensional: long diameter of non-nodal lesions, short diameter of lymph nodesBidimensional: perpendicular diametersUnidimensional: long diameter of any target lesionIncorporates PET results to describe CRMay be considered to confirm CR and/or to declare PD based on detecting new lesionsYesYesMinor responseNoNoYes, reduction in sum of long diameters between ≥10% and <30%Stable disease−29% to + 20%−50% to + 50%Decrease <10% to increase ≤20%Progression of diseaseIncrease in sum of diameters by 20%Increase in the sum of products of perpendicular diameters by > 50%, or any single lesion by > 50%Increase in sum of the longest diameters by 20%. For relapse from CR, at least one lesion should measure 2 cm in the long axis with or without PET activity Open table in a new tab The work by Younes et al. in this issue of Annals of Oncology clearly illustrates this point [8.Younes A. Hilden P. Coiffier B. et al.International Working Group consensus response evaluation criteria in lymphoma (RECIL 2017).Ann Oncol. 2017; 28: 1436-1447Abstract Full Text Full Text PDF PubMed Scopus (164) Google Scholar]. The measurement and assessment of only a single dimension was compared with bidimensional measurements with the same cutoff as the RECIST criteria for CR and PR. This study was carried out on 47 828 imaging measurements from 2983 individual lymphoma patients who were enrolled in 10 multicenter clinical trials. The main results of this comparison were that the use of unidimensional measures gave the same results in terms of tumor size modification or PFS during therapy. In the era of targeted therapy drug development, where patients with solid tumors and lymphomas are included in the same trials, this ‘single’ drug response assessment model may represent important progress. Several points still require improvement in the next steps: the role of PET-CT in solid tumors and the development of a common response assessment for immune oncology drugs, which currently differ [9.Seymour L. Bogaerts J. Perrone A. et al.iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics.Lancet Oncol. 2017; 18: e143-e152Abstract Full Text Full Text PDF PubMed Scopus (1169) Google Scholar, 10.Cheson B.D. Ansell S. Schwartz L. et al.Refinement of the Lugano Classification lymphoma response criteria in the era of immunomodulatory therapy.Blood. 2016; 128: 2489-2496Crossref PubMed Scopus (265) Google Scholar]. None declared.