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Clinical Investigations |
1 Division of Nuclear Medicine, Department of Radiology, Weill Medical College of Cornell University and New York Presbyterian Hospital, New York, New York
2 Center for Lymphoma and Myeloma, Division of Hematology and Oncology, Department of Medicine, Weill Medical College of Cornell University and New York Presbyterian Hospital, New York, New York
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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0.001). The PFS and 18F-FDG PET results obtained after the first cycle correlated better than those obtained after the completion of chemotherapy (r2 = 0.45 vs. 0.17). 18F-FDG PET had more false-negative results after the last cycle (6/17 cases, or 35%) than after the first cycle (2/13 cases, or 15%). Thus, 18F-FDG PET had greater sensitivity and positive predictive values after the first cycle (82% vs. 45.5% and 90% vs. 83%, respectively) than after the last cycle. Conclusion: 18F-FDG PET after 1 cycle of chemotherapy is predictive of 18-mo outcome in patients with aggressive NHL and HD and may earlier identify patients who would benefit from more intensive treatment programs.
Key Words: lymphoma • chemotherapy • posttherapy • 18F-FDG PET
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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67Ga imaging has also been reported to be an independent predictor of outcome after 1–2 cycles of chemotherapy (6,10). Nevertheless, 67Ga imaging is less efficacious than 18F-FDG PET for intraabdominal tumors and may be less sensitive in detecting disease in some instances of aggressive lymphoma or Hodgkin’s disease (HD) (11).
Over the past few years, a large body of evidence has confirmed the potential role of 18F-FDG PET, including both dedicated and coincidence PET systems, in the staging and monitoring of lymphomas (12–16). There is a paucity of data, however, defining the role of 18F-FDG PET at the earliest possible time to predict the response to therapy. Although a change in 18F-FDG uptake at multiple early times during chemotherapy has been described, this change was only marginally predictive of outcome (17). The predictive value of 18F-FDG PET at the completion of chemotherapy has also been evaluated (18). The response after 1 cycle of chemotherapy, however, has not yet been evaluated using 18F-FDG PET in non-Hodgkin’s lymphoma (NHL) and HD. We performed this study to assess the potential of early 18F-FDG PET to predict PFS and ultimate clinical outcome. We also compared the efficacy of 18F-FDG PET performed early with that performed after the completion of chemotherapy in patients with aggressive NHL and HD.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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18F-FDG PET Coincidence Imaging
All 30 patients underwent a whole-body 18F-FDG PET study before therapy and after the first cycle of chemotherapy. Twenty-three of 30 patients also had 18F-FDG PET studies at the completion of therapy. Coincidence images were obtained using a dual-head gamma camera with attenuation correction (MCD-AC; ADAC Laboratories, Milpitas, CA). The in-plane spatial resolution was 4.8 mm in full width at half maximum at the center of the field of view, with an axial field of view of 38 cm. In the transverse plane, the spatial resolution was constant radially as well as tangentially at any distance from the center to the edge of a transverse slice. In the axial direction, the spatial resolution (full width at half maximum) was approximately twice that of the transverse. All patients fasted at least 4–6 h before the start of the study. Serum glucose level was determined at the time of 18F-FDG injection using a glucometer. All patients had a serum glucose level of <130 mg/dL. Sixty minutes after the intravenous administration of 185 MBq 18F-FDG, a whole-body MCD-AC 18F-FDG PET imaging study consisting of 3 segments (pelvis, abdomen, and chest/neck) was acquired using a matrix size of 128 x 128 x 16, an acquisition time of 40 s per frame, and a scan overlap of 30% in an orbit of 180°. Ten-minute transmission scans were obtained using 153Gd sources after completion of the emission scans for attenuation correction. The images were reconstructed into transverse cross-sectional images by means of an iterative method and a Wiener filter with a cutoff frequency of 0.75 cycle per projection. The data from the whole-body acquisition were stacked in a 3-dimensional volume to allow viewing as a rotating cine display of 48 images as well as transverse or reconstructed coronal or sagittal images.
Data Analysis
Thirty patients after the first cycle of chemotherapy (within 10 d; range, 3–10 d) and 23 patients after the completion of chemotherapy (within 1 mo) were evaluated by a whole-body 18F-FDG PET study. All 18F-FDG PET scans were interpreted by 2 clinical reviewers without any knowledge of the clinical or CT data. All scans were scored either as positive or as negative. A positive result was defined as focal activity relatively higher than that of the surrounding background tissue, with no similar activity seen on the contralateral side, or increased activity in a location incompatible with normal anatomy. A negative result was defined as no pathologic 18F-FDG uptake at any site, including all sites of previously increased pathologic 18F-FDG uptake. 18F-FDG uptake that was equal to the mediastinum for lymph nodes originally located in the mediastinum was considered negative; however, the same intensity of uptake in other locations was considered positive. Before and after therapy, disease was evaluated site by site for the involved lymph nodes.
Patients who underwent both 18F-FDG PET studies (after the first and last cycles) and who either entered the study at relapse or had poor prognostic features at initial staging were categorized into a different subgroup (Table 2) to evaluate the predictive value of 18F-FDG PET when the prognostic factors were not favorable.
PFS was defined as the interval without progression of disease from the start of treatment. Treatment failure was defined as the inability to achieve a complete response, progression of disease, or recurrence of disease after a complete response. The inability to achieve a complete response or PFS was determined by a combination of clinical (residual palpable lymph nodes or other tumors), laboratory (rising lactate dehydrogenase levels or B symptoms), and imaging findings, such as CT findings (lack of resolution of lymphadenopathy or continuously enlarging lymph nodes). The primary aim of this study was to evaluate the role of 18F-FDG PET in predicting PFS after 1 cycle of chemotherapy compared with after the completion of chemotherapy
Statistical Analysis
Statistical analysis was performed using a software package (StatView 5.0; SAS Institute, Cary, NC). PFS curves were calculated by Kaplan-Meier survival analysis, and groups were compared using the log-rank test. The Kruskal-Wallis test (for multiple groups) or the Mann-Whitney test (for 2 groups) was used for pairwise comparison of the first-cycle 18F-FDG PET results with the end-therapy 18F-FDG PET data. In post hoc analysis, Bonferroni/ Dunn correction was applied when necessary, with a probability value of < 0.0167 (significance < 5%).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Overall Analysis.
The sensitivity, specificity, and overall accuracy of 18F-FDG PET performed after the first cycle for predicting 18-mo outcome were 87%. The positive and negative predictive values of 18F-FDG PET were also 87% (Table 3). There was a statistically significant difference in PFS between patients with negative (median PFS not reached) and those with positive (median PFS, 0 mo) 18F-FDG PET results after the first cycle of therapy (P < 0.0001) (Fig. 1).
18F-FDG PET Data Obtained Late After Chemotherapy
There were 23 patients who underwent 18F-FDG PET both after the first cycle and at the completion of therapy. Of these, 6 showed residual abnormal 18F-FDG uptake, and the studies of 17 were considered negative for residual lymphoma (Table 4).
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Negative 18F-FDG PET Results.
Of the 17 patients with negative 18F-FDG PET results, 11 are still in complete remission (65%) after a median follow-up of 19 mo (range, 18–24 mo). The remaining 6 patients (4 NHL, 2 HD) experienced disease relapse at the original site, with a median PFS of 6.5 mo (range, 5–18 mo). The disease was in the head or neck in 2 patients and in the chest in 4 patients. Of 6 patients with false-negative results, 4 had a brief clinical complete response (1 HD, PFS = 5 mo; 3 NHL, PFS = 6, 6, and 7 mo, respectively), but their disease eventually relapsed. In 2 patients, the disease recurred at 10 and 18 mo, respectively, after the completion of therapy. Of 6 patients with false-negative 18F-FDG PET findings, CT was indeterminate for residual lymphoma in 5 and revealed partial remission based on size criteria in 1.
Overall Analysis.
The sensitivity, specificity, and overall accuracy of 18F-FDG PET performed after the completion of chemotherapy for predicting 18-mo outcome were 45.5%, 92%, and 70%, respectively. The positive and negative predictive values of 18F-FDG PET were 83% and 65%, respectively (Table 5). There was a statistically significant difference in PFS between the patients with negative (median PFS not reached) and those with positive (median PFS, 0 mo) 18F-FDG PET results after the completion of therapy (P < 0.001) (Fig. 2)
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Discordant Results.
In 5 of 6 patients with discordant results, 18F-FDG PET results after the first cycle of therapy accurately predicted relapse whereas all 5 18F-FDG PET studies at the completion of chemotherapy were false-negative for residual disease in all patients (Fig. 3). The disease relapsed in these 5 patients, with a median PFS of 7 mo (range, 5–18 mo). There was 1 HD patient in whom 18F-FDG PET after 1 cycle of chemotherapy was false-negative in the mediastinum whereas 18F-FDG PET after the completion of chemotherapy was true-positive in predicting disease recurrence. This patient had disease relapse in the mediastinum after a PFS of 4 mo.
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18F-FDG PET results obtained after the first cycle and after the completion of chemotherapy using the logistic regression for 23 patients indicated a statistically significant difference in PFS between patients with negative and those with positive 18F-FDG PET results (P 0.001) (Figs. 2 and 5); however, PFS and 18F-FDG PET correlated better after the first cycle of therapy than after the completion of therapy (r2 = 0.45 vs. 0.17; 
2 = 14.2 vs. 4.36). The 18-mo actuarial PFS rates after 1 cycle and after the completion of chemotherapy for patients with negative 18F-FDG PET results were 85% and 65%, respectively, compared with 10% and 17%, respectively, for patients with positive 18F-FDG PET results.
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The results of 18F-FDG PET after the first cycle and at the completion of chemotherapy were concordant in 12 of 18 patients (positive concordance in 5 patients, negative concordance in 7 patients) and discordant in 6 patients. Among 6 patients with discordant results, the relapse that occurred in 5 had been predicted by 18F-FDG PET after the first cycle of therapy, whereas 18F-FDG PET after the last cycle had been false-negative in all 6 (Fig. 3). In these 5 patients, median PFS was 7 mo (range, 5–18 mo). In 1 discordant case, 18F-FDG PET after 1 cycle was false-negative in the mediastinum and converted to true-positive at the completion of therapy. The disease of this patient relapsed after a PFS of 4 mo. Of 5 patients with concordant positive 18F-FDG PET studies, 4 never achieved remission (PFS, 0 mo). In 1 patient with thymic hyperplasia, both 18F-FDG PET studies were false-positive. Among 7 concordant negative studies, 6 were of patients whose disease was in complete remission during a median follow-up of 19.5 mo (range, 18–24 mo). There was 1 false-negative study for a patient whose disease relapsed at 6 mo.
Overall Comparative Analysis
The comparative statistical values between data obtained for 18F-FDG PET after the first cycle and at the completion of chemotherapy were similar to those obtained for the entire patient group (Table 5). Sensitivity, specificity, negative predictive value, positive predictive value, and accuracy for 18F-FDG PET after the first cycle versus at the completion of chemotherapy were 82% versus 45.5%, 86% versus 86%, 75% versus 50%, 90% versus 83%, and 83% versus 61%, respectively.
A comparison of the 18F-FDG PET results obtained after the first cycle and at the completion of chemotherapy using logistic regression for 18 patients indicated a statistically significant difference in PFS between positive and negative 18F-FDG PET results at the completion of therapy (P 0.001). The 18-mo actuarial PFS rates for patients with negative 18F-FDG PET studies were 75% and 50%, compared with 10% and 17% for patients with positive 18F-FDG PET results, after 1 cycle and at the completion of chemotherapy, respectively.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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The disease activity may completely resolve after therapy, but residual masses may persist on CT because resolution of therapy-induced anatomic changes usually lags behind tumor cell mortality. 67Ga imaging is a standard procedure for the posttreatment evaluation of tumor viability. In previous studies, 67Ga imaging after 1 cycle of therapy has been found to be predictive of outcome in aggressive NHL and HD but, because of the physiologic excretion of 67Ga in the bowel, is less effective for the interpretation of abdominal involvement (6,10, 24). Furthermore, 67Ga imaging lacks sensitivity for deeply located small lesions. Various reports have shown the effectiveness of 18F-FDG PET in the posttreatment evaluation of lymphomas. The results of a previous study indicated that 18F-FDG PET was superior to 67Ga scintigraphy in accurately detecting disease sites in aggressive NHL and HD, with a sensitivity of 100% and 80.3%, respectively (11). Furthermore, 18F-FDG PET scans have a higher diagnostic and prognostic value than CT scans in the posttreatment evaluation of lymphomas (15). Thus, 18F-FDG PET has become the most helpful noninvasive modality in differentiating tumor recurrence from fibrosis when CT scans show a residual mass (12,15,22, 23,25,26).
In our data, the relapse rate when 18F-FDG PET at the completion of therapy had negative results was higher than that when 18F-FDG PET after the first cycle had negative results (35% vs. 15%). After the completion of therapy, there were 6 false-negative 18F-FDG PET studies, with relapses occurring at a median of 7 mo. Interestingly, in 5 of these 6 studies, 18F-FDG PET after the first cycle predicted relapse by showing residual 18F-FDG uptake in the tumor. In these studies, CT had no additional value in predicting recurrence. Other studies have also shown CT to offer no further benefit in predicting the outcome of lymphoma (7,18). The superior capability of 18F-FDG PET to predict outcome in patients with aggressive lymphoma and HD early during therapy is most likely the consequence of the sensitivity and rapid response characteristics of these lymphomas to chemotherapy. Our findings suggest that positive 18F-FDG PET results after 1 cycle reflect the metabolic activity of potentially resistant clones, which, although responding to chemotherapy, do so more slowly than do those homogeneously sensitive tumor cells. In a recent study, disease later relapsed in 20% of all lymphoma patients for whom 18F-FDG PET performed at the completion of therapy had negative findings (18). In contrast to the high false-negative rate observed with late 18F-FDG PET studies, only 2 early 18F-FDG PET studies had false-negative findings, which recurred after brief clinical remissions. This recurrence may possibly result from a small cluster of resistant clones that remained after the first cycle of therapy and escaped detection because of the resolution limits of the PET scanner.
The results for both the poor-prognosis group and the entire group after the first cycle of chemotherapy were similar, except that negative predictive value was lower for the poor-prognosis group (85% vs. 75%). This finding, however, may stem from the small size of the study group. Although the rate of relapse in patients with a poor prognosis is expected to be high, 18F-FDG PET was accurate in predicting remission. Indeed, 6 of 7 patients with concordant negative 18F-FDG PET findings both after the first cycle and at completion remain in complete remission with a median follow-up of 19.5 mo. Although the predictive value for remission was equal for both early and late studies, there is an advantage to assessing this poor-prognosis group early during chemotherapy, because early evidence of persistent disease may mandate an innovative intervention such as bone marrow transplantation. In this group, 18F-FDG PET may prove to be the imaging modality of choice for follow-up.
In our group of patients, for negative 18F-FDG PET findings after the first and last cycles, relapse rates were 15% (2/11 patients) and 35% (6/17 patients), respectively. The relapse rates after the last cycle of chemotherapy in our data appear to be higher than those reported for a prior study (18). The prior study included only patients evaluated at initial staging who underwent first-line therapy and included patients with low-grade lymphoma. Our series included both patients at initial staging and patients at relapse before salvage therapy, who were at a higher risk of disease recurrence. In our data, we investigated only aggressive NHL and HD because both types of lymphoma are sensitive to chemotherapy and potentially curable and may benefit from earlier more intensive treatment programs if tumor resistance is detected. In the previous study, the minimal follow-up period in some patients was 12 mo, whereas the minimal follow-up period in our study was 18 mo. Hence, by virtue of our study design, higher relapse rates than those observed in the prior study were anticipated.
Romer et al. (17) reported that 18F-FDG PET studies performed 7–42 d after therapeutic intervention had some predictive value in a small number of patients with high-grade NHL. In this study, chemotherapy caused a rapid decrease in tumor 18F-FDG uptake as early as 7 d after treatment, and 18F-FDG uptake continued to decline during therapy. During a follow-up of 16 ± 4 mo, 50% of patients continued to show remission. Our findings were similar to those obtained in this previous study except that remission rates in our series were higher. In our series, 85% of patients with complete disappearance of 18F-FDG uptake after 1 cycle of chemotherapy were in remission during a median follow-up of 19 mo. The differences in remission rates between our study and the previous study can be attributed to differences in study design. The previous study evaluated only 11 patients, and the main objectives were to determine the extent and time course of changes in 18F-FDG use in response to therapy and whether these changes in early uptake predicted the outcome of therapy. In our study, we evaluated 30 patients and our main objective was to determine whether 18F-FDG PET could determine the outcome of therapy after the first cycle of therapy versus after the completion of therapy.
If abnormal 18F-FDG uptake is seen after the first cycle of chemotherapy, the chances for relapse are significantly high; thus, close follow-up is mandatory in this group of patients. Negative 18F-FDG PET results after the first cycle were highly suggestive of long-term remission, whereas negative results after the completion of chemotherapy were less accurate. Although tumor progression or disease relapse may still develop in a few patients with negative 18F-FDG PET results early during treatment, 18F-FDG PET after the first cycle of chemotherapy remains far more predictive of outcome than is late 18F-FDG PET.
Patients with relapsed or refractory aggressive NHL or HD (appropriate candidates) generally receive second-line chemotherapy, and if the disease is sensitive to second-line chemotherapy, randomized trials have shown a survival benefit from high-dose chemotherapy and stem cell transplantation (27). If sufficient data were available that persistent positive 18F-FDG PET results after 1 cycle of chemotherapy portend a poor prognosis, one could argue either that one should switch the treatment to second-line chemotherapy and stem cell transplantation without completing a full course of initial chemotherapy or that one should, contrary to the usual procedure, repeat the 18F-FDG PET after 2–3 cycles and, if the findings are still positive, repeat the tumor biopsy or push for an earlier switch to an alternative dose-intense treatment. Our study provides a strong argument for consideration of a follow-up trial in which 18F-FDG PET is performed after 1 cycle to evaluate a potential subsequent change in treatment based on the results. Patients with negative 18F-FDG PET findings after 1 cycle and thus a good prognosis would continue with a full course of their first-line treatment, whereas patients with positive 18F-FDG PET findings after 1 cycle and thus a less favorable prognosis could be randomized to receive a full course of first-line treatment.
Of note, this study used a dual-head coincidence camera with attenuation correction instead of a dedicated full-ring PET system. Coincidence cameras have one third the sensitivity of dedicated PET systems. With the added benefit of attenuation correction, however, the detection rate of coincidence PET has been reported to increase from 60% to 80% for lesions 2 cm (28). Given the superior sensitivity of dedicated PET systems, it is even more impressive that the prognostic value of 18F-FDG imaging early during therapy was so readily shown in this study.
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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FOOTNOTES |
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For correspondence or reprints contact: Lale Kostakoglu, MD, New York Presbyterian Hospital, Weill Cornell Medical Center, 525 E. 68th St., Starr: 221, New York, NY 10021.
E-mail: lak2005{at}mail.med.cornell.edu
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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