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Originally published as JCO Early Release 10.1200/JCO.2006.09.2403 on January 22 2007 © 2007 American Society of Clinical Oncology.
Revised Response Criteria for Malignant Lymphoma
From the Division of Hematology/Oncology, Georgetown University Hospital, Washington, DC; University of Cologne, Cologne; Department of Nuclear Medicine, University of Iowa, Iowa City, IA; Department of Pathology, British Columbia Cancer Agency and the University of British Columbia, Vancouver, British Columbia, Canada; Department of Oncology and Hematology, Rigshospitalet, Copenhagen University Hospital, Denmark; Division of Oncology and Department of Radiation Oncology, Stanford University, Stanford, CA; Department of Hematology, Hospices Civils de Lyon and Université Claude Bernard, Lyon, France; James P. Wilmot Cancer Center, University of Rochester, Rochester, NY; Academic Medical Center, Department of Hematology, Amsterdam, the Netherlands; Lymphoma Unit, Department of Medical Oncology, Oncology Institute of Southern Switzerland, Bellinzona, Switzerland; Lurie Cancer Center, Northwestern University, Chicago, IL; Department of Nuclear Medicine, University Hospital Gasthuisberg, Leuven, Belgium; Cancer Research UK Medical Oncology Unit, St Bartholomew's Hospital, London, United Kingdom; Department of Medicine III, University of Munich, Hospital Grosshadern, Munich, Germany; Hematology and Stem Cell Transplantation Division, National Cancer Center Hospital, Tokyo, Japan; Section of Hematology/Oncology, University of Nebraska Medical Center, Omaha, NE; and Dipartimento di Oncologia ed Ematologia, Università di Modena e Reggio Emilia, Modena, Italy Address reprint requests to Bruce D. Cheson, MD, Georgetown University Hospital, 3800 Reservoir Rd NW, Washington, DC 20007; e-mail: bdc4{at}georgetown.edu
Purpose Standardized response criteria are needed to interpret and compare clinical trials and for approval of new therapeutic agents by regulatory agencies. Methods The International Working Group response criteria (Cheson et al, J Clin Oncol 17:1244, 1999) were widely adopted, but required reassessment because of identified limitations and the increased use of [18F]fluorodeoxyglucose-positron emission tomography (PET), immunohistochemistry (IHC), and flow cytometry. The International Harmonization Project was convened to provide updated recommendations. Results New guidelines are presented incorporating PET, IHC, and flow cytometry for definitions of response in non-Hodgkin's and Hodgkin's lymphoma. Standardized definitions of end points are provided. Conclusion We hope that these guidelines will be adopted widely by study groups, pharmaceutical and biotechnology companies, and regulatory agencies to facilitate the development of new and more effective therapies to improve the outcome of patients with lymphoma.
Standardized response criteria provide uniform end points for clinical trials, allowing for comparisons among studies, facilitating the identification of more effective therapies, and aiding the approval process for new agents by regulatory agencies. Before 1999, response criteria for malignant lymphomas varied widely among study groups and cancer centers with respect to the size of a normal lymph node, the frequency of assessment and the time point the response assessment was made, the methods used to assess response, whether response was assessed prospectively or retrospectively, the percentage increase required for disease progression, and many other factors.1 Even relatively minor differences in the definition of normal size of a lymph node can have a major influence on response rates.2 In 1999, an international working group (IWG) of clinicians, radiologists, and pathologists with expertise in the evaluation and management of patients with non-Hodgkin's lymphoma (NHL) published guidelines for response assessment and outcomes measurement.1 These recommendations were adopted rapidly and widely by clinicians and regulatory agencies, and were used in the approval process for a number of new agents. However, they were subject to considerable inter- and intraobserver variation and recommended technologies, such as gallium scans, are no longer considered state-of-the-art. Several points were subject to misinterpretation, notably the application of the complete remission/unconfirmed (CRu), and the recommendations did not include assessment of extranodal disease. The widespread use of positron emission tomography (PET) scans and immunohistochemistry warranted a reassessment of the prior response criteria. Since the Hodgkin's lymphoma study groups had adopted these IWG criteria, any new recommendations needed to account for those patients as well. As a result, an International Harmonization Project was initiated by the German Competence Network Malignant Lymphoma to develop recommendations that were consistent across study groups.3 Subcommittees were organized on Response criteria, End Points for Clinical Trials, Imaging, Clinical Features, and Pathology/Biology, and the recommendations are reflected in this report.
PET PET using [18F]fluorodeoxyglucose (FDG), has emerged as a powerful functional imaging tool for staging, restaging, and response assessment of lymphomas.4-24,25 The advantage of PET over conventional imaging techniques such as computed tomography (CT) or magnetic resonance imaging is its ability to distinguish between viable tumor and necrosis or fibrosis in residual mass(es) often present after treatment.9,11,26-28 This information may have important clinical consequences. Juweid et al20 evaluated the impact of integrating PET into the IWG criteria in a retrospective study of 54 patients with diffuse large B-cell NHL who had been treated with an anthracycline-based regimen. PET increased the number of complete remission (CR) patients, eliminated the CRu category, and enhanced the ability to discern the difference in progression-free survival (PFS) between patients experiencing CR and partial remission (PR). Such findings provided rationale for incorporating PET into revised criteria. However, a number of issues with PET need to be considered. The technique for performing and interpreting PET has only recently been standardized.29 There is variability among readers and equipment. PET is also associated with false-positive findings due to rebound thymic hyperplasia, infection, inflammation, sarcoidosis, or brown fat. Diffusely increased bone marrow uptake is often observed after treatment or administration of hematopoietic growth factors.19,29,33,34 There are also false-negative results with PET relating to the resolution of the equipment, technique, and variability of FDG avidity among histologic subtypes.10,29-32 These and other considerations regarding interpretation of PET scans have recently been addressed.29 Recommendations for the use of PET or PET/CT. Current recommendations for the use of PET scans reflect the FDG avidity of the lymphoma subtype, and the relevant end points of the clinical trial (Table 1).
Timing of PET scans after therapy. Post-therapy inflammatory changes may persist for up to 2 weeks after chemotherapy alone in lymphoma patients and for up to 2 to 3 months or longer after radiation therapy or chemotherapy plus radiation. To minimize the frequency of these potentially confounding interpretation finding, PET scans should not be performed for at least 3 weeks, and preferably 6 to 8 weeks, after completion of therapy.29 Definition of a positive PET scan. Visual assessment currently is considered adequate for determining whether a PET scan is positive, and use of the standardized uptake value is not necessary.29 A more extensive description of interpretation of PET scans is provided in the consensus guidelines of the Imaging Subcommittee.29 In brief, a positive scan is defined as focal or diffuse FDG uptake above background in a location incompatible with normal anatomy or physiology, without a specific standardized uptake value cutoff.29 Other causes of false-positive scans should be ruled out. Exceptions include mild and diffusely increased FDG uptake at the site of moderate- or large-sized masses with an intensity that is lower than or equal to the mediastinal blood pool, hepatic or splenic nodules 1.5 cm with FDG uptake lower than the surrounding liver/spleen uptake, and diffusely increased bone marrow uptake within weeks after treatment. Specific criteria for lung nodules based on lesion size have been developed.29 Bone Marrow Assessment Restaging bone marrow examinations are commonly used to assess response to therapy. The determination of involvement may be difficult, given that no universally accepted standards exist. The usual approach to response determination relies on morphologic assessment of the bone marrow biopsy, and clot section if adequate and available, whereas ancillary studies using immunohistochemistry, flow cytometry, and polymerase chain reaction methodology are largely ignored or underused. Moreover, a direct comparison of these studies and their respective sensitivity and specificity for the detection of occult but clinically meaningful involvement are lacking. Thus, recommendations regarding the use of these strategies and their interpretation are largely empiric at this time. The recommendation for bone marrow response is that histologically normal bone marrows with a small (< 2%) clonal B-cell population detected by flow cytometry should be considered normal, given that definitive clinical studies that demonstrate an inferior outcome are lacking. Immunohistochemistry has a clear role in the assessment of the bone marrow at diagnosis and restaging after therapy. When antibodies are used to detect CD20 and CD3 expression, morphologically normal bone marrows can often be shown to harbor disease. Sensitivity can be increased with the use of subtype-specific antibody panels directed at CD5, cyclin D1, CD23, CD10, DBA44, and kappa and lambda light chains. Less common lymphoma subtypes with occult bone marrow disease are particularly well suited to this approach, including splenic marginal zone B-cell lymphomas and a number of subtypes of DLBCL (ie, intravascular large B-cell lymphoma and HIV-related DLBCL). Indolent B-cell lymphomas and chronic lymphocytic leukemia are more difficult to assess, given that the distinction from reactive lymphoid aggregates and nodular partial remissions in the bone marrow can be difficult to assess because of the frequent admixture of reactive T cells in these diseases. Immunohistochemistry using anti-CD5 and anti-CD23 can be helpful in this setting, as are stains for kappa and lambda light chains that can detect surface membrane immunoglobulin in paraffin sections. Similarly, antibodies to cyclin D1 and CD10 are useful for recognizing subtle bone marrow involvement in mantle-cell lymphoma and follicular lymphoma, respectively. In the future, antibodies to Bcl-6 may improve detection of occult follicular lymphoma in the bone marrow; however, technical problems preclude their general use at this time. In fact, many routinely used immunohistochemical reagents can be difficult to apply consistently to the evaluation of bone marrow samples, largely due to subtleties in fixation methods and decalcification techniques. Caution is recommended when interpreting biopsies post-therapy for residual disease. The use of rituximab may lead to a false-negative interpretation of residual B-cell disease, despite the fact that the widely used commercial anti-CD20 (L26) recognizes a cytoplasmic epitope of CD20, in contrast to the surface epitope recognized by rituximab. The judicious use of another pan–B-cell antibody, CD79a, is strongly recommended when evaluating post-treatment samples. Similar caution is required when interpreting CD20 flow cytometric data for several months after therapy with rituximab, given that surface epitopes may be blocked. The availability of clot sections allows for immunohistochemical analysis without the influence of decalcification and may be useful for the post-treatment evaluation of bone marrow involvement. Lastly, the role of molecular genetic analyses in the determination of response to therapy is difficult to resolve. Assay techniques and sensitivity vary enormously between laboratories, making systematic recommendations impossible. Residual clonal disease may exist without morphologic evidence of lymphoma (ie, gastric mucosa-associated lymphoid tissue [MALT] lymphoma after therapy). In aggregate, these data suggest that the disappearance of the molecular clone may lag behind the disappearance of morphologic evidence of disease. Alternatively, these findings may represent the persistence of residual disease or potentially repopulating lymphoma stem cells in biopsies lacking morphologic evidence of lymphoma. These distinctions need to be reconciled before molecular testing can be considered routine, particularly when the findings affect treatment decisions. Sensitive and sophisticated diagnostic approaches such as flow cytometry and/or molecular genetic analyses should be incorporated into clinical trials to determine their relevance and potential utility for directing therapy. However, for routine practice we do not recommend that clinical decision making be based solely on flow cytometry and/or molecular genetic analyses that indicate a residual small (< 2% of gated or live events) B-cell clone in the absence of other supportive findings from morphology and immunohistochemistry. We strongly encourage investigators to collect these data together with clinical correlative data that might eventually support their routine use for the assessment of response criteria for lymphoid malignancies.
CR The designation of CR requires the following (Table 2):
1. Complete disappearance of all detectable clinical evidence of disease and disease-related symptoms if present before therapy. 2a. Typically FDG-avid lymphoma: in patients with no pretreatment PET scan or when the PET scan was positive before therapy, a post-treatment residual mass of any size is permitted as long as it is PET negative.
2b. Variably FDG-avid lymphomas/FDG avidity unknown: in patients without a pretreatment PET scan, or if a pretreatment PET scan was negative, all lymph nodes and nodal masses must have regressed on CT to normal size ( 3. The spleen and/or liver, if considered enlarged before therapy on the basis of a physical examination or CT scan, should not be palpable on physical examination and should be considered normal size by imaging studies, and nodules related to lymphoma should disappear. However, determination of splenic involvement is not always reliable because a spleen considered normal in size may still contain lymphoma, whereas an enlarged spleen may reflect variations in anatomy, blood volume, the use of hematopoietic growth factors, or causes other than lymphoma. 4. If the bone marrow was involved by lymphoma before treatment, the infiltrate must have cleared on repeat bone marrow biopsy. The biopsy sample on which this determination is made must be adequate (with a goal of > 20 mm unilateral core). If the sample is indeterminate by morphology, it should be negative by immunohistochemistry. A sample that is negative by immunohistochemistry but that demonstrates a small population of clonal lymphocytes by flow cytometry will be considered a CR until data become available demonstrating a clear difference in patient outcome.
CRu
PR
In patients with follicular lymphoma or mantle-cell lymphoma, a PET scan is only indicated with one or at most two residual masses that have regressed by more than 50% on CT; those with more than two residual lesions are unlikely to be PET negative and should be considered partial responders.
Stable Disease
Relapsed Disease (after CR)/Progressive Disease (after PR, SD)
Measurable extranodal disease should be assessed in a manner similar to that for nodal disease. For these recommendations, the spleen is considered nodal disease. Disease that is only assessable (eg, pleural effusions, bone lesions) will be recorded as present or absent only, unless, while an abnormality is still noted by imaging studies or physical examination, it is found to be histologically negative. In clinical trials where PET is unavailable to the vast majority of participants, or where PET is not deemed necessary or appropriate for use (eg, a trial in patients with MALT lymphoma), response should be assessed as above, but only using CT scans. However, residual masses should not be assigned CRu status, but should be considered partial responses.
Primary CNS Lymphomas
Primary Gastric Lymphoma Interpretation of residual lymphoid infiltrates in post-treatment gastric biopsies can be difficult, with no uniform criteria for the definition of histologic remission. Older assessment systems have not been adopted uniformly.40,41 A histologic grading system proposed by the Groupe d'Etude des Lymphomes de l'Adulte may be an improvement over prior schemes, but will require additional validation.42,43
Follow-Up Evaluation In a clinical trial, uniformity of reassessment is necessary to ensure comparability among studies with respect to the major end points of event-free survival, disease-free survival, and PFS. It is obvious, for example, that a protocol requiring re-evaluation every 2 months will produce different results compared with one requiring the same testing annually, even if the true times to events are the same. One recommendation has been to assess patients on clinical trials after completion of treatment at a minimum of every 3 months for 2 years, then every 6 months for 3 years, and then annually for at least 5 years.1 Few recurrences occur beyond that point for patients with diffuse large-cell NHL or Hodgkin's lymphoma. However, the risk of relapse for patients with follicular and other indolent histologies is continuous. These intervals may vary with specific treatments, duration of treatment, protocols, or unique drug characteristics. Recently, the National Comprehensive Cancer Network published recommendations for follow-up of patients with Hodgkin's and NHL:49,50 for patients with Hodgkin's lymphoma in an initial CR, an interim history and physical examination every 2 to 4 months for 1 to 2 years, then every 3 to 6 months for the next 3 to 5 years, with annual monitoring for late effects after 5 years. For follicular or other indolent histology lymphoma patients in a CR, the recommendation for follow-up was every 3 months for a year then every 3 to 6 months. For diffuse large B-cell NHL, the guidelines proposed follow-up every 3 months for 24 months then every 6 months for 36 months.49,50 Patients with a follicular or low-grade NHL who are being managed with a so-called watch and wait approach should be monitored for the development of disease-related symptoms or signs of organ involvement. No consensus regarding the frequency of follow-up of such patients exists and the interval should be specified in the protocol. Otherwise, imaging studies should be individualized based on the location of the disease and informed by the behavior of palpable disease.
The major end points of clinical trials should reflect the histology, clinical situation (eg, initial treatment v salvage), and objectives of the study (Table 3). It is important that consistent definitions of end points are used, and we hope that this document will harmonize the use of those definitions.
End points based on tumor measurements are greatly influenced by response criteria. Overall and complete response rates usually can be assessed accurately in single-arm as well as randomized trials. However, response rates do not necessarily influence other measures of overall clinical benefit or outcome in patients with lymphoma,51 and are not considered as important as other end points. Exceptions are phase II trials of novel new agents, in which identification of biologic activity is of interest. Durable complete responses, if associated with measures of clinical benefit, may also be relevant.
Overall Survival
PFS
Event-Free Survival
Time to Progression
Disease-Free Survival
Response Duration
Lymphoma-Specific Survival
Time to Next Treatment
Clinical Benefit We hope that these revised guidelines will improve comparability among studies, and facilitate new agent development leading to improved therapies for patients with lymphoma.
The authors indicated no potential conflicts of interest.
Conception and design: Bruce D. Cheson, Beate Pfistner, Volker Diehl Administrative support: Beate Pfistner, Volker Diehl Collection and assembly of data: Bruce D. Cheson, Malik E. Juweid, Randy D. Gascoyne, Sandra J. Horning Data analysis and interpretation: Bruce D. Cheson, Malik E. Juweid, Randy D. Gascoyne, Lena Specht, Sandra J. Horning, Bertrand Coiffier, Richard I. Fisher, Anton Hagenbeek, Sigrid Stroobants, T. Andrew Lister, Martin Dreyling, Joseph M. Connors, Massimo Federico, Volker Diehl Manuscript writing: Bruce D. Cheson, Beate Pfistner, Malik E. Juweid, Randy D. Gascoyne, Lena Specht, Sandra J. Horning, Bertrand Coiffier, Richard I. Fisher, Anton Hagenbeek, Emanuele Zucca, Steven T. Rosen, Sigrid Stroobants, T. Andrew Lister, Richard T. Hoppe, Martin Dreyling, Kensei Tobinai, Julie M. Vose, Joseph M. Connors, Massimo Federico, Volker Diehl Final approval of manuscript: Bruce D. Cheson, Beate Pfistner, Malik E. Juweid, Randy D. Gascoyne, Lena Specht, Sandra J. Horning, Bertrand Coiffier, Richard I. Fisher, Anton Hagenbeek, Emanuele Zucca, Steven T. Rosen, Sigrid Stroobants, T. Andrew Lister, Richard T. Hoppe, Martin Dreyling, Kensei Tobinai, Julie M. Vose, Joseph M. Connors, Massimo Federico, Volker Diehl
We thank our other colleagues who provided input into these guidelines: Lauren Abrey, Ralph Meyer, Otto S. Hoekstra, Gregory Wiseman, Markus Dietlein, Sven Reske, Ali Guermazi, Markus Schwaiger, Mary Gospodarowicz, Michael Pfreundschuh and the German High-Grade Lymphoma Study Group, Myriam Mendila, David Schenkein, Nancy Valente, Daphne de Jong, the EORTC Lymphoma Group, and the Nordic Lymphoma Study Group, Josée Zijlstra, Michinori Ogura, and the JCOG Lymphoma Study Group, A.J. Ferreri, and C. Copie-Bergmann.
published online ahead of print at www.jco.org on January 22, 2007. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2007 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
1.5 cm in their greatest transverse diameter for nodes > 1.5 cm before therapy). Previously involved nodes that were 1.1 to 1.5 cm in their long axis and more than 1.0 cm in their short axis before treatment must have decreased to 
50% in their SPD or, for single nodules, in the greatest transverse diameter. 
