Imaging for Oncologic Response Assessment in Lymphoma

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1 Special Articles Review Kulkarni et al. Use of CT and PET for Response Assessment in Lymphoid Malignancies Special Articles Review Naveen M. Kulkarni 1 Daniella F. Pinho 2 Srikala Narayanan 3 Avinash R. Kambadakone 4 Jeremy S. Abramson 5 Dushyant V. Sahani 4 Kulkarni NM, Pinho DF, Narayanan S, Kambadakone AR, Abramson JS, Sahani DV Keywords: DWI, International Working Group criteria, Lugano criteria, lymphoma, PET DOI: /AJR Received January 14, 2016; accepted after revision July 27, D. V. Sahani has received research grant support from GE Healthcare, but none of the support is related to this study. 1 Division of Abdominal Imaging, Medical College of Wisconsin, Milwaukee, WI. 2 University of Texas Southwestern Medical Center, Dallas, TX. 3 Children s Hospital of Pittsburgh of UPMC, Pittsburgh, PA. 4 Division of Abdominal Imaging and Intervention, Massachusetts General Hospital, Harvard Medical School, 55 Fruit St, White 270, Boston, MA Address correspondence to D. V. Sahani (dsahani@partners.org). 5 Cancer Center, Massachusetts General Hospital, Harvard Medical School, Boston, MA. AJR 2017; 208: X/17/ American Roentgen Ray Society Imaging for Oncologic Response Assessment in Lymphoma OBJECTIVE. The purpose of this article is to examine the role of different imaging biomarkers, focusing in particular on the use of updated CT and PET response criteria for the assessment of oncologic treatment effectiveness in patients with lymphoma but also discussing other potential functional imaging methods and their limitations. CONCLUSION. Lymph nodes are commonly involved by metastatic solid tumors as well as by lymphoma. Evolving changes in cancer therapy for lymphoma and metastases have led to improved clinical outcomes. Imaging is a recognized surrogate endpoint that uses established criteria based on changes in tumor bulk to monitor the effects of treatment. With the introduction of targeted therapies and novel antiangiogenic drugs, the oncologic expectations from imaging assessment are changing to move beyond simple morphologic methods. Molecular and functional imaging methods (e.g., PET, perfusion, DWI, and dual-energy CT) are therefore being investigated as imaging biomarkers of response and prognosis. The role of these advanced imaging biomarkers extends beyond measuring tumor burden and therefore might offer insight into early predictors of therapeutic response. Despite the potential benefits of these exciting imaging biomarkers, several challenges currently exist. P rimary malignancies involving the lymph nodes, such as lymphoma, are common [1]. In 2011, approximately 66,000 new cases of non-hodgkin lymphoma (NHL) and 8800 new cases of Hodgkin lymphoma (HL) were diagnosed in the United States [1, 2]. Lymph node size currently serves as an important criterion for the differentiation of benign nodes from malignant nodes on cross-sectional imaging, because larger lymph nodes are more likely to be malignant [3, 4]. Unlike metastases to other organs, lymph nodes are normal anatomic structures that have a measurable size. Even when lymph nodes are involved, their size may be normal, and they may be difficult to differentiate from abnormal nodes. Moreover, unlike solid-organ tumors (either metastatic or primary), the involved malignant nodes can shrink to normal or nearly normal size rather than disappear completely. Hence, the use of size criteria alone for differentiating benign nodes from malignant nodes has been a big challenge. World Health Organization (WHO) and Response Evaluation Criteria in Solid Tumors (RECIST) criteria that were developed for solid tumors [5 7] have been applied to lymphoid malignancies, but potential limitations exist. In 1999, these limitations led to the introduction of CT-based response assessment criteria for NHL developed by the International Working Group (IWG); these criteria, which were also used for HL, were soon adapted as a standard approach for imaging for response assessment in primary lymphoid malignancies [8]. The shortcomings of a CT-based response assessment method, including a lack of functional or molecular information, became evident as experience using these criteria in clinical trials increased [4, 5]. Moreover, these deficiencies associated with conventional approaches became more pronounced with the use of targeted therapies, for which molecular and physiologic changes in the tumor precede the morphologic response [7]. Advances in imaging technologies have improved the physiologic and functional capabilities of imaging. Newer imaging techniques now possess the ability to detect changes in the tumor microenvironment and the tissue cytoarchitecture by capturing alterations in perfusion, oxygenation, and metabolism. Among these techniques, 18 FDG PET, which provides an indication of the 18 AJR:208, January 2017

2 Use of CT and PET for Response Assessment in Lymphoid Malignancies metabolic and proliferative activity within tumors, is most widely used for oncologic response assessment of FDG-avid tumors. In 2007, the International Harmonization Project (IHP) revised the CT-based IWG response assessment criteria by incorporating FDG PET/CT, which was further updated in the Lugano classification to provide more recent recommendations for lymphoma response assessment [9]. Other functional imaging techniques include DWI, which assesses cellularity and its integrity; dynamic contrast-enhanced CT and dynamic contrast-enhanced MRI, which assess the biodistribution of contrast material within tumors to evaluate tissue microvascular changes; MR spectroscopy, which is used to quantify the relative chemical composition of tissue; and dual-energy CT, which helps in tissue characterization [10 13]. This article highlights the use of morphologic and functional techniques, focusing in particular on updated CT and PET response criteria for response assessment in lymphoma. Primary Lymphoma Lymphomas, which are the most common primary hematopoietic malignancies, consist of a heterogeneous collection of lymphoid neoplasms, each of which has unique characteristics in terms of genetic and molecular features, clinical presentation, and treatment approaches and outcome. Lymphomas are divided into two broad groups: HL and NHL. With the use of current chemotherapy regimens, HL and many histologic subtypes of NHL can potentially be cured [1, 14, 15]. Accurate response assessment during the treatment cycle is essential to guide the treating physicians in their management decisions. Although certain clinical, pathologic, and genetic features are used for risk stratification and prognostication, these characteristics cannot predict the prospective dynamic changes within tumors during treatment [14, 15]. An accurate prediction of the long-term outcome might help identify patients for whom treatment is likely to fail and might therefore allow the treating physician to modify treatment regimens early to improve the likelihood and duration of remission. Likewise, early functional assessments of patients with a favorable response to therapy might allow deintensification of therapy with the goal of preserving treatment efficacy and minimizing treatment-associated toxicity. Historical Background of Response Assessment The invention of MDCT and, subsequently, FDG PET/CT has significantly contributed to the evolution of the staging and response assessment of lymphoma. Before 1999, many major cooperative cancer treatment groups followed different approaches to monitor the response of lymphomas to therapy, including the use of different size thresholds for normal and enlarged nodes and different frequencies of imaging, which led to inconsistent outcome and also precluded comparison of treatment effectiveness among different studies [16 18]. In 1999, the National Cancer Institute created the IWG, which consisted of hematologists, medical oncologists, radiation oncologists, radiologists, and pathologists with expertise in the evaluation and management of patients with NHL and which published guidelines for response assessment that primarily relied on changes in the size of enlarged lymph nodes or other tumor lesions on CT [8, 9]. As experience using these CT-based criteria in clinical trials increased, the shortcomings of this approach, such as the inability of CT to differentiate fibrotic tissue from residual tumor and the lack of functional information, became evident. In 2007, the IHP provided new recommendations by incorporating PET/CT in an effort to improve response assessment. In the IHP criteria, FDG avidity of the lymph nodes was defined relative to the mediastinal blood pool, and visual analysis of FDG activity was considered sufficient for the assessment of the therapeutic response. This led to ambiguity in the interpretation of FDG activity, which is an important shortcoming of the IHP criteria. More recently, the Lugano classification was published, providing important updates to the IHP criteria from 2007 [8, 9]. The Lugano Classification In 2011 and 2013, leading representatives of clinical and imaging subcommittees on lymphoma presented their findings at the International Conference on Malignant Lymphoma, and the most recent Lugano classification was published soon thereafter [9]. This new classification provided important updates to previous IWG and IHP criteria for response assessment and also to the Ann Arbor staging system for lymphomas, with the goal of developing simple unambiguous TABLE 1: Revised Response Criteria for Lymphoma: Lugano Classification PET/CT for FDG-Avid Histologic Findings a Complete Response a Partial Response No Response or Stable Disease Progressive Disease Score of 4 or 5 with increase (from baseline) in intensity of uptake at nodal or extranodal sites, with new FDG-avid foci consistent with lymphoma, or with both findings Score of 4 or 5 without significant change in uptake Score of 4 or 5 with decreased uptake compared with baseline and with residual mass(es) of any size Score of 1, 2, or 3 with or without residual mass nodal or extranodal site(s) New or recurrent FDG-avid bone marrow foci No change in bone marrow uptake from baseline and no new FDG-avid lymphoma No FDG-avid disease in bone marrow Residual bone marrow uptake at involved site that is higher than that of normal marrow but reduced from levels noted at baseline; in the setting of nodal response, any persistent focal changes in marrow are to be evaluated with MRI, tissue sampling, or follow-up scan No new FDG-avid lymphoma No new FDG-avid lymphoma (Table 1 continues on next page) AJR:208, January

3 Kulkarni et al. TABLE 1: Revised Response Criteria for Lymphoma: Lugano Classification (continued) CT-Based Response for Non FDG-Avid Histologic Findings and for When CT Is Performed for Measurement of Lesion Size (for Any Type of Lymphoma) b Complete Response c Partial Response d No Response or Stable Disease Progressive Disease Complete resolution of disease evidence Decrease of 50% in sum of product of perpendicular dimensions of target lesions (six target nodal and extranodal sites) Nodal sites must regress to 1.5 cm in longest diameter If extranodal lesions are selected as target lesions, they should disappear completely Any organ that is enlarged at baseline should regress to normal size Spleen size should decrease more than 50% in length from normal length Decrease of < 50% in sum of product of perpendicular dimensions of target lesions (six target nodal or extranodal target lesions) from baseline, provided no criteria for disease progression are met Progressive disease requires that at least one of the following criteria be met and may be based on single dominant lesion: No new lesions suggesting lymphoma 1. An individual node or lesion must be abnormal: No new lesions suggesting lymphoma No increase in organ enlargement or nonmeasured lesions in a manner consistent with lymphoma Nonmeasured lesions: absent or normal, regressed, but no increase a. Longest diameter > 1.5 cm b. The product of the perpendicular diameters has increased by 50% from the nadir No new lesions suggesting lymphoma are noted c. An increase in the longest diameter or the shortest axis perpendicular to the longest diameter from the nadir (an increase of 0.5 cm for lesions 2 cm and an increase of 1 cm for lesions > 2 cm) Absent nonmeasured lesions 2. Splenomegaly: a. With known splenomegaly, the splenic length must increase by > 50% of the extent of its prior increase beyond the length noted at baseline (e.g., a splenic length of 16 cm [which is 3 cm greater than baseline splenomegaly of 13 cm] increases to 18 cm [i.e., 5 cm longer than the length at baseline]) b. In the absence of prior splenomegaly, length must increase by at least 2 cm c. New or recurrent splenomegaly 3. New or progressing nonmeasured lesions 4. Regrowth of previously resolved lesions 5. New extranodal lesion of > 1.0 cm (if < 1 cm, it must be unequivocally attributable to lymphoma) 6. New node > 1.5 cm in any axis 7. Assessable disease of any size unequivocally attributable to lymphoma Note Table provides an overview of the Lugano classification [9]. Readers may refer to the original publication [9] for details, because this is a condensed version. Nonmeasured lesions were defined as any nodal or extranodal masses that either were not selected as target lesions or did not meet the requirements for measurability (but were considered abnormal) or any suspected disease that was difficult to quantitate (e.g., pleural effusions, ascites, bone lesions, or leptomeningeal disease). Scores assigned using a 5-point scale for visual assessment were defined as follows: 1 denoted no FDG uptake above background; 2, uptake less than or equal to that of the mediastinum; 3, uptake greater than that noted in the mediastinum but less than or equal to that in the liver; 4, uptake moderately greater than that in the liver; and 5, uptake markedly higher than that in the liver, the presence of new lesions, or both findings. An additional category (X) indicating new areas of uptake unlikely to be related to lymphoma was also designated. a See Figs. 3 and 4. b See Figs c See Fig. 1. d See Fig AJR:208, January 2017

4 Use of CT and PET for Response Assessment in Lymphoid Malignancies and standardized response assessment and providing a staging system for reporting. The new Lugano classification provides updated FDG PET/CT based and CT-based response evaluation of lymphoma that guides clinical trials and clinical management on the basis of imaging. As a functional imaging tool, FDG PET can provide insight into the dynamic response of tumor during the course and end of treatment, which is an advantage over CT. From the perspective of staging, monitoring the response to treatment, and achieving a meaningful clinical effect from FDG PET/CT, the lymphoma entity has to be FDG avid. Most common types of lymphoma (e.g., diffuse large B-cell NHL, follicular NHL, mantle cell NHL, and HL) are routinely FDG avid [19 22]. Although PET is generally performed with low-dose unenhanced CT for attenuation correction and anatomic localization, diagnostic CT (which can be part of PET/CT for FDG-avid lymphomas) is recommended at baseline staging for anatomic assessment. On the other hand, for lymphoma with a low or variable FDG uptake, CT is used for staging and response evaluation. It should be noted that these guidelines are primarily deployed in the realm of clinical trials and guide clinical management rather than academic exercise for tumor burden or standardized uptake value (SUV) measurement [8, 18 21]. CT-Based Response Assessment CT-based response assessment is preferred in the following instances: for lymphoma subtypes with low or variable uptake, when PET/CT is unavailable (as in certain parts of the world), and for any reason that PET/CT cannot be performed. Guidelines are provided for assessing the effect of treatment on imaging time points, and outcome can be categorized as follows: complete response, partial response, stable disease, or progressive disease. Figures 1 and 2 show examples of complete and partial response, as determined on the basis of CT criteria only, and Figures 3 and 4 show examples of complete response, as determined on the basis of PET/CT criteria. Table 1 provides details about each response category [9]. For response evaluation, tumor burden is calculated at baseline by choosing up to six of the largest measurable target lesions (e.g., the largest nodes, nodal mass, or extranodal deposits in solid organs) representing different body regions and overall disease burden and then performing follow-up evaluations after treatment. Lymph nodes larger than 1.5 cm and extranodal lesions larger than 1.0 cm along their longest diameter are considered to be target lesions. Although it is preferable that the target nodal lesions represent the largest dominant lesion and, if possible, are from disparate regions of the body, to avoid inconsistencies in the evaluation, it is best to choose well-defined isolated lesions suitable to allow accurate repeated measurements. In the case of a confluent lesion, an effort should be made to exclude adjacent normal structures. The overall objective assessment is performed by measuring the target lesion area as the product of the perpendicular diameters (i.e., the diameter of the long axis multiplied by the diameter of the short axis) and then calculating the sum of the product of the perpendicular diameters of all considered target lesions [9]. For example, for three lymph nodes measuring 3 2 cm, 4 3 cm, and 4 5 cm, the calculated sum of the product of the perpendicular diameters will be (3 2) + (4 3) + (4 5) = = 38. Nonmeasurable disease includes lesions too small to be considered measurable, bony skeleton lesions, ascites, pleural and pericardial effusion, spread of lymphangitis, and leptomeningeal disease. Considerations in Specific Situations Confluent Lesions If previously measured target lesions become confluent with adjacent lesions, the products of the greatest perpendicular diameters of the resulting mass can be calculated and recorded under the original measurable lesion. An increase of more than 50% in the product of the perpendicular diameters of a confluent mass compared with the product of the perpendicular diameters of individual nodes is indicative of disease progression. When lesions that become confluent belong to different types (such as a measurable nodal and extranodal lesion), an attempt should be made to consistently assess the original lesion quantitatively when possible [9]. Splitting Nodal Mass When a previously identified lymph nodal mass separates to form discrete nodes, the product of the perpendicular diameters of each split node should be summed to represent the product of the perpendicular diameters of split nodal lesions and should be added to the remaining target lesions to determine response [9]. Despite the benefits of CT, there are some limitations to the evaluation of tumor burden with the use of CT. Notable among these limitations is the presence of fibrotic changes or scarring presenting as a residual mass on CT scans acquired after treatment, a finding that is likely to be observed in approximately 40% of patients with NHL and in an even higher number of patients with HL. Active tumor tissue is likely to be present in 10 20% of such patients with residual masses, but it is not possible to separate cases with and without residual disease on CT [8, 23, 24]. Another limitation is the definition of a target lesion, which requires that the longest nodal diameter be greater than 1.5 cm. However, one must be aware that even a smaller lymph node may be involved (Fig. 5). Other pitfalls include variability in assessing the enlargement and involvement of extranodal lymphoid organs (e.g., the liver and spleen) because of the lack of standardization of scanning technique, the manifestation of lymphoma in ways that elude traditional imaging techniques (e.g., diffuse infiltration of the viscera), bone or bone marrow involvement without focal lesions but with an overall increase in size or disruption of the architecture of those structures on imaging, and difficulty in assessing bone marrow, small lung nodule, and changes in gastrointestinal wall thickening. PET/CT-Based Response Assessment PET is a noninvasive metabolic imaging technique based on positron-emitting radionuclide tracer, with FDG being the molecule most commonly used in clinical practice. FDG PET has been clearly shown to be quite sensitive for the detection of nodal and extranodal FDG-avid lymphoma before treatment as well as during the time of established or suspected relapse, but indications may vary regarding specific diagnosis and presentation [24 26]. Nevertheless, a baseline scan is always recommended to allow meaningful comparison with follow-up scans. In comparison with CT alone, combined FDG PET/CT has been found to be more accurate for response assessment, with PET having a sensitivity that exceeds 90% and a specificity of approximately 100%, values that are superior to those noted for CT (sensitivity, 88%; and specificity, 86%) [20 22, 27, 28]. Available data and extensive experience also indicate that PET has an advantage over CT in discrimination of residual active lymphoma from fibrotic and inflammatory posttreatment changes, with a reported sensitivity of 72 84%, a specificity of %, a AJR:208, January

5 Kulkarni et al. positive predictive value of 65%, and a negative predictive value of 90%. The lower positive predictive value results from postradiotherapy inflammation persisting for as long as 8 12 weeks [29 31]. Hence, caution must be used when assessing false-positive highsignal inflammatory uptake in residual masses after treatment. Response assessment with FDG PET is based on assessing changes in FDG uptake. The SUV serves as an objective measurement of tumor metabolic activity, but because many variables influence SUV measurement, objective assessment is not recommended for evaluation of response in patients with FDGavid lymphoma. Although the 2007 IWG guidelines recommended visual interpretation for response evaluation by comparing FDG uptake with uptake in the mediastinal blood pool, this approach leads to interobserver variability [8, 9, 24]. The new Lugano classification incorporates the Deauville 5-point scale, which was initially proposed for the assessment of lymphoma on interim FDG PET/CT images, for the interpretation of scans of lesions with FDG-avid histologic profiles. The 5-point scale includes the following scores and definitions: a score of 1 denotes no FDG uptake above background, 2 indicates that uptake is equal to or less than that in the mediastinum, 3 denotes that uptake is greater than that in the mediastinum but is equal to or less than that in the liver, 4 denotes that uptake is moderately greater than that in the liver, and 5 indicates that uptake is markedly greater than that in the liver, new lesions are present, or both findings have been noted. An additional category, denoted X, indicates that new areas of uptake are unlikely to be related to lymphoma [9]. The 5-point scale for FDG PET/CTbased response evaluation is recommended for both interim assessment (to assess early treatment response) and end-of-treatment assessment (to establish remission status). A score of 1 or 2 is interpreted as denoting a complete metabolic response, whereas a score of 4 or 5, which denoted treatment failure, indicates observation of signal intensity that is similar to or increased from that noted at baseline, the presence of new foci suggesting lymphoma on interim and end-oftreatment assessments, or both findings. At the interim assessment, a score of 4 or 5 with FDG uptake that has reduced from baseline is considered to represent a partial metabolic response. However, at the end of treatment, the presence of residual disease with a score of 4 or 5 (with uptake reduced from baseline) still represents treatment failure. A score of 3 at the interim assessment also likely represents a complete metabolic response and usually is considered to be a negative result. However, in clinical trials involving PET in which a strategy of deescalation of therapy is pursued, a score of 3 may be considered an inadequate response so as to avoid undertreatment. As with CT-based response assessment, four categories are assigned: complete response, partial response, stable disease, and progressive disease [9] (Table 1). Ideally a quantitative evaluation performed using FDG PET will provide consistency and eliminate interobserver variation related to subjective evaluation, even with the use of the recommended 5-point scale. Studies have shown that a 66 77% decrease in the measured SUV (based on the number of chemotherapy cycles) for diffuse large B-cell lymphoma indicates a favorable treatment response associated with better survival, but data for HL are less robust [32, 33]. However, different variables, such as type of disease, treatment, and timing of imaging, influence metabolic activity, and no sufficient evidence exists to recommend a precise cutoff for quantitative evaluation. Other Major Features and Recommendations of Lugano Classification PET for Staging FDG PET/CT is now formally included as reference standard imaging for the pretreatment staging of FDG-avid lymphomas (except for chronic lymphocytic leukemia [CLL] and small lymphocytic lymphoma, lymphoplasmacytic lymphoma and Waldenstrom macroglobulinemia, mycosis fungoides, and marginal zone NHLs, unless there is a suspicion of aggressive transformation), and it may also be applicable to primary extranodal diffuse large B-cell lymphoma. In comparison with CT alone, FDG PET/CT has been shown to significantly change the staging of NHL (resulting in downstaging in 1% of cases and upstaging in 30% of cases) and HL (resulting in downstaging in 16% of cases and upstaging in 31% of cases), thus possibly leading to a treatment change for large numbers of patients [21]. Bulky Disease CT (preferably performed with contrast enhancement) is considered for pretreatment staging of lesions with non FDG-avid histologic profiles and radiotherapy planning and in instances where measuring nodes is important. Because of its poor accuracy, a chest radiograph is no longer needed for lymphoma staging. For HL, tumor bulk (i.e., a single mass rather than a collection of smaller nodes) is defined as 10 cm or greater than one-third of the transverse diameter of the chest. For NHL, to our knowledge, no consistent definition for bulky disease has been determined, although it is hoped that a consistent definition will be available in the future [9]. Bone Marrow Biopsy On the basis of the available data, bone marrow aspiration or biopsy is no longer recommended for the routine staging of HL and, instead, it is needed only for those patients with diffuse large B-cell lymphoma with a negative PET scan result for whom identification of occult discordant histologic findings is clinically important. For other lymphoma variants, evaluation of bone marrow remains a standard test for staging [9, 34, 35]. Revised Ann Arbor Staging The Ann Arbor staging system (adopted in the 1970s), which is based on the anatomic extent of disease, was primarily developed for the staging of HL. However, because most patients are treated as though they have either limited or advanced disease and because of increased experience using this staging system, the Ann Arbor classification has been questioned. The Lugano classification recommends modification of the Ann Arbor classification for the anatomic description of the extent of disease. Patients now have disease more simply categorized as either limited disease (previously categorized as Ann Arbor stage I or II) or advanced disease (previously categorized as Ann Arbor stage III or IV). The designation of the absence (denoted by A ) or presence (denoted by B ) of disease-related symptoms is retained only for HL because symptoms direct treatment of that disease only [9]. Interim and End-of-Treatment Imaging for Predicting Response PET/CT performed as interim imaging (i.e., imaging performed after initiation but before completion of therapy) has emerged as a valuable tool for the prognostication of curable diseases like HL and diffuse large B-cell lymphoma. A decrease in metabolic activity, lesion size, or both characteristics on interim FDG PET/CT scans is in- 22 AJR:208, January 2017

6 Use of CT and PET for Response Assessment in Lymphoid Malignancies dicative of a response that is associated with improved outcomes [31, 36, 37]. Although currently under investigation, it has not yet been proven whether intensification or deintensification of treatment for patients with either a response or lack of response on interim PET scans will improve prognosis. This is an area of active ongoing investigation. False-positive PET scan results may occur more commonly during interim assessment, particularly for diffuse large B-cell lymphoma, for which one clinical trial found falsepositive results for more than one-half of the patients with positive interim PET scan results who then underwent biopsy for confirmation [38]. Patients with positive PET scan results but negative biopsy findings had outcomes similar to those of patients who had negative results of interim PET assessment. Accordingly, biopsy is recommended before altering therapy on the basis of the results of the interim PET assessment, particularly outside the context of a clinical trial [8, 31, 36, 39, 40]. Furthermore, changing chemotherapeutic regimens midway through treatment on the basis of interim PET/CT findings is not recommended because there are no data supporting an improved outcome [40]. On end-of-treatment PET/CT assessment of patients with HL and curable NHL histologic findings, such as diffuse large B-cell lymphoma, persistent FDG activity (score, 4 or 5) in a residual mass suggests treatment failure. Conversely, complete metabolic response is associated with a highly favorable long-term disease-free and overall survival in patients with these histologic findings [28, 29]. Therefore, in patients with residual disease at the end of treatment, additional therapy with radiation, alternative non cross-resistant chemotherapy regimens, stem cell transplantation, or a combination of these treatments may be indicated. Given the possibility of false-positive PET results after therapy, repeat biopsies of FDGavid foci are suggested before intensifying therapy for these patients, particularly given the toxicity associated with many of the therapies in this setting. For patients with indolent or otherwise incurable lymphoma (e.g., small lymphocytic lymphoma and marginal zone lymphoma), treatment response is assessed using CT-based criteria, but patients may not clinically require achievement of complete remission on the basis of imaging findings so long as any disease resulting in symptoms or organ or bone marrow impairment has been sufficiently relieved [21, 28, 30]. Routine surveillance scans are discouraged because of the higher rate of false-positive results (greater than 20%) associated with PET scans, which can lead to unnecessary investigations, biopsies, patient anxiety, and expense. In general, it is recommended that follow-up scans should be guided by the patient s clinical symptoms and signs, which usually provide the earliest evidence of recurrent disease. Surveillance CT is widely used but may not be necessary for all patients [41 43]. Other Response Assessment Criteria Unlike the IWG, IHP, and Lugano criteria previously described, which are specifically proposed for response evaluation of lymphoma, there are other response evaluation criteria, such as RECIST, EORTC, and PET Response Evaluation Criteria in Solid Tumors (PERCIST), that are applied to a wide group of malignancies (both primary and metastatic) and not necessarily lymphoma only. A detailed discussion of these criteria is beyond the scope of the present article, and readers are referred to appropriate information found elsewhere [43 45]. In brief, RECIST criteria indicate tumor response evaluation for solid tumors on the TABLE 2: Brief Overview of Other Relevant Response Assessment Criteria basis of unidimensional measurements made on CT along the longest axis of the tumor. RECIST guidelines were subsequently updated to RECIST 1.1 guidelines in 2009 [5, 6]. RECIST 1.1 recommends identifying five target lesions, with a maximum of two target lesions per organ, and it defines progressive disease as an absolute increase of 5 mm in the sum of the tumor diameters. Lymph nodes that are at least 15 mm along their short axis are considered to be target lesions. An important disadvantage of RECIST evaluation is its reliability with regard to tumor burden alone. For targeted therapies for which molecular and physiologic changes in the tumor precede morphologic response, RECIST may not predict early response. With respect to lymphoma, the main issues are related to residual masses that frequently comprise inflammatory, necrotic, and fibrotic tissue rather than residual disease. The PET-based EORTC criteria (released in 1999) are among the first guidelines to incorporate a functional imaging modality like FDG PET that provided important insight into tumor biology, creating an advantage for such criteria over CT-based tumor burden assessment. Although incorporation of FDG PET refined the response outcomes, important limitations of EORTC criteria became evident. Such limitations include the lack of information on the number of lesions that should be selected, the size of the ROI for SUV measurement, and the best cutoff values for the tumor SUV. In 2009, Wahl et al. [45] published guidelines outlining PERCIST, which combine anatomic and metabolic information that make the guidelines distinct from EORTC. Important recommendations were made to standardize the PERCIST criteria (i.e., a maximum of five tumor foci of the highest FDG avidity, with up to two foci per organ; an in- Criteria Complete Response Partial Response Stable Disease Progressive Disease RECIST EORTC PERCIST Complete disappearance of all target lesions Complete disappearance of metabolically active tumor (decreased to background level) Decrease in FDG uptake similar to that seen in background blood pool Decrease of at least 30% in the sum of the target lesions Reduction of 15% in FDG uptake Reduction of minimum of 30% in peak SUL Not meeting criteria for partial response or progressive disease Not meeting criteria for partial response or progressive disease Not meeting criteria for partial response or progressive disease Increase of at least 20% in the sum of target lesions (must show absolute increase of 5 mm in the sum of the tumor diameters) Increase of 25% in FDG uptake Increase of > 30% in peak SUL Note RECIST = Response Evaluation Criteria in Solid Tumors, EORTC = European Organization for Research and Treatment of Cancer, PERCIST = PET Response Evaluation Criteria in Solid Tumors, SUL = standardized uptake value corrected to lean body mass. 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7 Kulkarni et al. terval of at least 10 days between acquisition of FDG PET scans and the completion of chemotherapy and the use of the SUV corrected to lean body mass rather than the SUV that is compared with liver uptake) [44, 45]. Table 2 provides a short overview of these response criteria. Response Assessment in Leukemia Like lymphoma, leukemia is a group of hematopoietic malignancies in which some of the subtypes, like chronic lymphocytic leukemia and certain leukemic transformations to lymphoma, are frequently associated with lymphadenopathy. Important factors affecting leukemia response are clinical, hematologic, and bone marrow findings. Response terminology and criteria are disease specific, and one should always refer to criteria for response in the specific protocol section [46]. Imaging is generally used as an adjunct to response evaluation. Currently, no specific guidelines exist on the use of imaging, including CT, to determine leukemia response. It generally is not required for the initial or follow-up evaluation [46]. The results of a recent study suggest that the presence of abdominal disease (splenomegaly or lymphadenopathy), as detected on CT evaluation of patients with CLL, predicts a more aggressive clinical course [47]. Therefore, for studies evaluating leukemia, the use of CT is encouraged. In general, the response criteria for leukemia define the following responses: complete response, which is defined by the disappearance of signs and symptoms of disease and normalization of peripheral blood counts; partial response, which is defined by a decrease in the WBC or peripheral lymphocyte count and a reduction in the size of enlarged organs; progressive disease, which is denoted by an increased WBC or platelet count (in chronic myelocytic leukemia [CML]), the appearance of new lymph nodes (in CLL), an increase in the size of the spleen or the liver (in CML or CLL), and findings of circulating blast cells in peripheral blood or more than 5% of bone marrow consisting of myeloblasts (in acute myelocytic leukemia or acute lymphoblastic leukemia). CT scans are used in the formal response criteria for CLL, whereas PET scans have no role in the response criteria for this disease, which is often only minimally FDG avid. Of note, CLL may transform into diffuse large B-cell lymphoma (i.e., Richter transformation), so where there is clinical suspicion of transformation, a PET scan may help identify a discordantly bright FDG-avid mass to guide the confirmatory biopsy [46, 47]. Other Emerging Methods DWI is a noninvasive technique that allows evaluation of the rate of microscopic water diffusion. Apparent diffusion coefficient (ADC) measurement can be calculated by acquiring images with a different gradient duration and amplitude (i.e., b values). Analyzing the diffusion properties of water molecules, certain tissue properties, and biologic findings has improved tissue characterization [48, 49]. Tumors typically have lower ADC values than normal tissues and benign lesions [48 50]. A previous study has validated the role of DWI in evaluating neoplastic and nonneoplastic lesions in the brain [51]. The evolution of technology and the increasing interest in DWI have further propelled the use of DWI for various indications in the body, including tumor imaging. In the recent past, the role of DWI has been extended to the monitoring of therapeutic effectiveness in solid tumors [52 55]. DWI has shown variable success in distinguishing between benign and malignant lymphadenopathy [56 59]. Initial DWI techniques were hampered by poor image quality because of respiratory motion, but the addition of respiratory triggering provided improved image quality at the cost of a prolonged scan time, making it unsuitable for whole-body imaging. However, introduction of whole-body DWI with background body signal suppression technique, which is feasible under free breathing, made whole-body DWI feasible. Because background signal is suppressed by the whole-body DWI with background body signal suppression technique, nodal and extranodal localizations of malignant lymphoma can be easily visualized, mimicking images like PET. Whole-body DWI with background body signal suppression is mostly evaluated qualitatively on inverted gray images with a single b value in the range of s/mm 2. It is recommended that DW images be interpreted in association with ADC maps. Nevertheless, it is worth mentioning that respiratory motion can still result in ADC errors for small focal lymph nodes in areas such as adjacent heart [48, 49]. In an experimental study of NHL xenografts in a mouse model, an increase in the ADC preceded T2 signal changes noted after chemotherapy [60]. In a subsequent clinical trial assessing NHL, Wu et al. [61] observed comparable performance between DWI and PET/CT in assessing anticancer effects on NHL. Similarly, Lin et al. [62] established a correlation between an increase in the ADC of residual diffuse B-cell lymphoma masses after treatment and FDG activity on PET. King et al. [63] investigated the role of posttreatment ADC changes in the metastatic lymph nodes of patients with head and neck squamous cell carcinoma as a potential predictor of response. Patients with a lower tumor ADC after treatment had higher rates of treatment failure [63]. Although many studies have shown the role of DWI in staging, future larger-scale studies are required to establish the role of DWI in characterizing lymphoma residual tumors. Recognizing the benefits of DWI as a potential biomarker of response (Fig. 6), the National Cancer Institute has therefore proposed consensus guidelines and recommendations for DWI to ensure the optimal quality and reproducibility of the technique for use in clinical trials [64]. It is generally agreed that 1.5-T MRI systems are adequate for optimal DWI, but high-field MRI systems, such as 3-T scanners, can overcome some of the initial limitations of DWI. PET/MRI that allows the combined evaluation of anatomy and tissue metabolism is currently being used. Studies have shown that FDG PET/MRI has a high sensitivity and specificity for nodal involvement in metastatic disease and malignant lymphoma [65]. Initial results have implied that PET/MRI can be an effective modality in staging lymphoma and assessing response to treatment [65, 66]. Although FDG PET/CT currently is the modality of choice for lymphoma imaging, FDG PET/MRI is a promising alternative to PET/CT because of its reduced radiation exposure. This is especially relevant for patients who typically undergo several PET scans for staging and assessment of therapy response, such as patients with lymphoma. Other new imaging biomarkers, such as MR spectroscopy, dual-energy CT, and perfusion imaging (with CT and MRI), that can detect the tumor microenvironment have not been extensively studied in the context of lymphoma, but there are a few studies on perfusion imaging (showing decreased tumor perfusion values and normalization of peak tumor perfusion after treatment of lymphoma) [67, 68] and MR spectroscopy (indicating changes in the 31 P spectrum that can predict patients with treatment response versus patients with no response or a partial response) [69]. However, these studies of perfusion imaging and MR spectroscopy have not included all the steps of standardization and 24 AJR:208, January 2017

8 Use of CT and PET for Response Assessment in Lymphoid Malignancies TABLE 3: Advantages and Disadvantages of Various Imaging Biomarkers Imaging Method Imaging Biomarker Measured Advantage Disadvantage CT Tumor burden measurement by calculating Easy to use Lag time SPD Standardized Requires expertise and labor for volumetric measurement Quantitative Not suitable for capturing early directed Defined criteria therapies and targeted antiangiogenic changes FDG PET/CT Visual assessment of FDG uptake on the Defined criteria No available tumor-specific tracer basis of a 5-point scale (i.e., Lugano Tumor metabolism based Assessment is still based on qualitative classification) measurements More quantitative Available with all scanners Because of many variables, quantitative Precise overlap of morphologic and assessment is not well established functional (PET/CT) images DWI Apparent diffusion coefficient Simpler protocols and modeling Artifact Commercial software available with most Low signal-to-noise ratio scanners Quantitative Validation Reproducibility No defined criteria for response FDG PET/MRI Standardized uptake value High contrast enhancement from MRI and High cost high PET sensitivity provide robust evaluation Ability to combine use with other techniques, Still investigational in the research realm such as DWI and dynamic contrast-enhanced MRI Lack of additional radiation from CT No standard definition criteria CT perfusion Tissue perfusion Relatively simple protocols and modeling Ionizing radiation Blood volume Commercial software available with all Limited coverage scanners Transit time More quantitative Reproducibility and validation Permeability No defined criteria for response assessment MRI perfusion Initial AUC Superior contrast resolution Complex protocols and modeling Transfer and rate constant Quantitative Reproducibility Leakage space fraction Can be repeated frequently if mandated by Validation the protocol Fractional plasma volume Lack of ionizing radiation No defined criteria for response Tissue perfusion More coverage (entire organ) Permeability Dual-energy CT Iodine maps Easy to scan and use No defined criteria for response Standard tumor burden measurement and Requires intensive quantitative measurement quantitative measurement (i.e., with iodine maps) can be performed simultaneously Easy to standardize scanning protocols Scanners not widely available Note SPD = sum of product of perpendicular dimensions of target lesions. validation that are required. In particular, no cutoff values exist for any of the proposed parameters to differentiate between patients with a response to treatment and those with no response. With rapidly changing technology, however, these newer imaging tools hold promise for optimizing and personalizing therapies, and, in the future, they likely will play an increasingly important role in the management of lymphoma [70 73]. Table 3 provides an overview of the advantages and disadvantages associated with all techniques. Conclusion The role of imaging in the evaluation of lymphoid malignancies has advanced dramatically in recent years. With the improved understanding of tumor biology in lymphoma, novel approaches have been developed AJR:208, January

9 Kulkarni et al. for treatment, and there are growing expectations to develop imaging biomarkers for an early and accurate assessment of tumor response to therapy so that treatment may be customized to suit each individual patient. Relatively simple and established CT-based imaging biomarkers have been applied; however, the recognized limitations of tumor morphologic measurements have led to the introduction of novel imaging biomarkers for response assessment. A functional imaging method such as PET/CT has now assumed an important role in lymphoma evaluation, is already a part of the criteria for assessment of treatment response, and has an emerging role in prognostication. Familiarity with the recently introduced Lugano classification will help the radiologist guide the clinical oncology team in selecting the appropriate response evaluation for lymphoma. In addition, there has been growing research interest in evaluating advanced techniques such as DWI, perfusion imaging, and MR spectroscopy to monitor the effects of treatment on malignant lymph nodes. Although promising, these other new emerging imaging biomarkers have not gone through all steps of standardization and validation. However, with the rapid changes in treatment strategies, these newer imaging techniques hold promise for optimizing and personalizing therapies, and, in the future, they likely will play an increasingly important role in the management of lymphoma. References 1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, CA Cancer J Clin 2007; 57: Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 2011; 61: Dorfman RE, Alpern MB, Gross BH, Sandler MA. Upper abdominal lymph nodes: criteria for normal size determined with CT. 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10 cance of bone marrow involvement. Blood 2013; Wedeen VJ, Meuli R. Understanding diffusion MR H, et al. Diffusion-weighted MRI in early chemotherapy response evaluation of patients with diffuse Use of CT and PET for Response Assessment in Lymphoid Malignancies 122:61 67 imaging techniques: from scalar diffusion-weighted 36. Haioun C, Itti E, Rahmouni A, et al. [ 18 F]fluoro- 2-deoxy-d-glucose positron emission tomography (FDG-PET) in aggressive lymphoma: an early prognostic tool for predicting patient outcome. Blood 2005; 106: Terasawa T, Lau J, Bardet S, et al. Fluorine-18-fluorodeoxyglucose positron emission tomography for interim response assessment of advancedstage Hodgkin s lymphoma and diffuse large B-cell lymphoma: a systematic review. J Clin Oncol 2009; 27: Moskowitz CH, Schöder H, Teruya-Feldstein J, et al. Risk-adapted dose-dense immunochemotherapy determined by interim FDG-PET in Advancedstage diffuse large B-Cell lymphoma. 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Eur J Cancer 1999; 35: Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumors. J Nucl Med 2009; 50(suppl 1):122S 150S 46. Hallek M, Cheson BD, Catovsky D, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute Working Group 1996 guidelines. Blood 2008; 111: Muntañola A, Bosch F, Arguis P, et al. Abdominal computed tomography predicts progression in patients with Rai stage 0 chronic lymphocytic leukemia. J Clin Oncol 2007; 25: Hagmann P, Jonasson L, Maeder P, Thiran JP, imaging to diffusion tensor imaging and beyond. RadioGraphics 2006; 26(suppl 1):S205 S Jacobs MA, Ibrahim TS, Ouwerkerk R. AAPM/ RSNA physics tutorials for residents: MR imaging brief overview and emerging applications. RadioGraphics 2007; 27: Vandecaveye V, De Keyzer F, Nuyts S, et al. 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Eur Radiol 2016 Apr 5[Epub ahead of print] 66. Schwenzer NF, Pfannenberg AC. PET/CT, MR, and PET/MR in lymphoma and melanoma. Semin Nucl Med 2015; 45: Dugdale PE, Miles KA, Bunce I, Kelley BB, Leggett DA. CT measurement of perfusion and permeability within lymphoma masses and its ability to assess grade, activity, and chemotherapeutic response. J Comput Assist Tomogr 1999; 23: Spira D, Vogel W, Bares R, Horger M. Volumeperfusion CT as an adjunct to whole-body contrastenhanced CT for monitoring response to therapy in lymphoma. Br J Haematol 2010; 151: Griffiths JR, Tate AR, Howe FA, Stubbs M. Magnetic resonance spectroscopy of cancer-practicalities of multi-centre trials and early results in non- Hodgkin s lymphoma. Eur J Cancer 2002; 38: Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000; 407: Hsu CY, Shen YC, Yu CW, et al. Dynamic contrast-enhanced magnetic resonance imaging biomarkers predict survival and response in hepatocellular carcinoma patients treated with sorafenib and metronomic tegafur/uracil. J Hepatol 2011; 55: Jiang T, Kambadakone A, Kulkarni NM, Zhu AX, Sahani DV. Monitoring response to antiangiogenic treatment and predicting outcomes in advanced hepatocellular carcinoma using image biomarkers, CT perfusion, tumor density, and tumor size (RECIST). Invest Radiol 2012; 47: Kaza RK, Platt JF, Cohan RH, Caoili EM, Al-Hawary MM, Wasnik A. Dual-energy CT with single- and dual-source scanners: current applications in evaluating the genitourinary tract. RadioGraphics 2012; 32: (Figures start on next page) AJR:208, January

11 Kulkarni et al. A C Fig year-old man with non-hodgkin lymphoma. A and B, Axial contrast-enhanced CT images of thorax obtained before treatment show multiple enlarged mediastinal lymph nodes (arrows). C and D, Contrast-enhanced CT scans obtained 1 month after completion of chemotherapy show complete resolution of lymph node mass, resulting in categorization of outcome as complete response. Fig year-old man with non-hodgkin lymphoma. A and B, Contrast-enhanced CT scans obtained at baseline show multiple retroperitoneal lymph nodes (arrows). A B D B (Fig. 2 continues on next page) 28 AJR:208, January 2017

12 Use of CT and PET for Response Assessment in Lymphoid Malignancies C Fig. 2 (continued) 50-year-old man with non-hodgkin lymphoma. C and D, Contrast-enhanced CT scans obtained after treatment show reduction of greater than 50% in lymph node tumor burden (arrows), resulting in categorization of outcome as partial response. A Fig year-old woman with diffuse large B-cell lymphoma who underwent PET/CT. A and B, Pretherapy contrast-enhanced CT image (A) shows bulky retroperitoneal lymphadenopathy (arrows), and pretherapy PET image (B) shows avid FDG uptake in mass (arrow). (Fig. 3 continues on next page) D B AJR:208, January

13 Kulkarni et al. C Fig. 3 (continued) 52-year-old woman with diffuse large B-cell lymphoma who underwent PET/CT. C and D, Contrast-enhanced CT image (C) from PET/CT examination performed after completion of six cycles of chemotherapy shows residual tumor mass (arrows), but corresponding PET image (D) shows lack of FDG uptake in residual mass (arrow). This case highlights benefit of metabolic imaging with PET versus CT in response assessment. On basis of CT only, patient will be categorized as having partial response, whereas assessment of response on basis of PET indicates complete response. A B Fig year-old woman with diffuse large B-cell lymphoma. A, Pretreatment PET image shows evident avid FDG uptake (arrows) in supradiaphragmatic and infradiaphragmatic lymph node chain. B, Whole-body PET image obtained after completion of six cycles of chemotherapy shows complete metabolic response (arrows). D 30 AJR:208, January 2017

14 Fig year-old man with non-hodgkin Use of CT and PET for Response Assessment in Lymphoid lymphoma. Malignancies A and B, PET/CT examination produced PET scan (A) which shows 7-mm left axillary lymph node (arrow) considered to be positive for non-hodgkin lymphoma. On CT image (B) alone, based on its size lymph node (arrow) would have been considered to be normal. A C A B B D Fig year-old man with nodal involvement by lymphoma. A and B, Pretreatment DW image (A) and apparent diffusion coefficient map (ADC) (B) show periportal lymph nodal mass (arrows) with restricted diffusion and lower ADC. C and D, Posttreatment DW image (C) and ADC map (D) show decrease in restricted diffusion (arrow, C) and increase in ADC (by 33%) (arrow, D) suggestive of favorable response to treatment. Lesion appears grossly stable in size, suggesting advantage of functional imaging over morphologic tumor burden assessment. AJR:208, January

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