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© 2003 American Society for Clinical Oncology Positron Emission Tomography Is Superior to Computed Tomography Scanning for Response-Assessment After Radical Radiotherapy or Chemoradiotherapy in Patients With Non–Small-Cell Lung Cancer
1 From the Department of Radiation Oncology, Department of Diagnostic Imaging, Statistical Centre and Department of Medical Oncology, Peter MacCallum Cancer Institute, Melbourne, Victoria, Australia, and the University of Turku, Turku, Finland. Address reprint requests to Michael Mac Manus, MD, Department of Radiation Oncology, Peter MacCallum Cancer Institute, St Andrew’s Place, East Melbourne, Victoria 3000, Australia; email: mmanus{at}petermac.unimelb.edu.au.
Purpose: To prospectively study the capacity of positron emission tomography (PET) and computed tomography (CT) to determine response soon after radical radiotherapy or chemoradiotherapy and, thereby, predict survival. PET is known to provide a more accurate estimate of true extent of disease than CT when used to stage non–small-cell lung cancer (NSCLC). Patients and Methods: Seventy-three patients with NSCLC underwent [18F]fluorodeoxyglucose PET and CT scans before and after radical radiotherapy (n = 10) or chemoradiotherapy (n = 63). Follow-up PET scans were performed at a median of 70 days after radiotherapy. The median PET-CT interval was 1 day. Each patient had determinations of response to therapy made with PET and CT, categorized as complete response, partial response, no response, progressive disease, or nonassessable. Responses were correlated with subsequent survival. Results: Median survival after follow-up PET was 24 months. There was poor agreement between PET and CT responses (weighted kappa = 0.35), which were identical in only 40% of patients. There were significantly more complete responders on PET (n = 34) than CT (n = 10), whereas fewer patients were judged to be nonresponders (12 patients on PET v 20 on CT) or nonassessable (zero patients on PET v six on CT) by PET. Both CT and PET responses were individually significantly associated with survival duration; but on multifactor analysis that included the known prognostic factors of CT response, performance status, weight loss, and stage, only PET response was significantly associated with survival duration (P < .0001). Conclusion: In NSCLC, a single, early, posttreatment PET scan is a better predictor of survival than CT response, stage, or pretreatment performance status.
STRUCTURAL IMAGING, using computed tomography (CT) or magnetic resonance imaging (MRI), is the cornerstone of the assessment of response to treatment of malignant tumors treated with radiotherapy and/or chemotherapy. Serial measurements of tumor dimensions are made, and criteria, such as the World Health Organization (WHO) criteria,1 are applied to categorize the outcome as complete response (CR), partial response (PR), no response (NR), or progressive disease (PD). These categories have prognostic significance and may determine the need for further therapy.2 Structural imaging has significant limitations in non–small-cell lung cancer (NSCLC) after treatment with radical radiotherapy or chemoradiotherapy. Selected patients with NSCLC have a chance for long-term survival and even cure with radical radiotherapy,3,4 provided distant metastases are absent and the disease is not too extensive for high-dose irradiation. Although results have been improved by combining chemotherapy with radiotherapy,5,6 survival has remained poor. Most patients relapse with local recurrence, distant metastases, or both. Accurate early assessment of response to radical radiotherapy for patients with NSCLC could be invaluable by identifying patients who have responded poorly at a time when the course of the disease could potentially be influenced by further treatment. The limitations of structural imaging in NSCLC are well established. Tumors may be obscured by atelectasis and, after radiotherapy, may be obscured by radiation pneumonitis.7 Noninvasive determination of tumor involvement of intrathoracic lymph nodes is based on lymph node size.8 Nodes larger than 1 cm are denoted as containing tumor. However, lymph node enlargement commonly results from benign reactive hyperplasia, and nodes less than 1 cm often contain tumor when examined histopathologically. In addition, tumors often regress gradually over several months, mandating serial measurements to assess response. Despite having been controlled by treatment, some lesions may never regress radiologically.9 Initially-enlarged lymph nodes may still contain active tumor despite reduction in size to less than 1 cm. Functional imaging with [18F]fluorodeoxyglucose (FDG) positron emission tomography (PET) may facilitate more accurate early assessment of response to treatment of NSCLC than structural imaging. FDG is a glucose analog that is taken up and trapped at a high rate by malignant tumor cells, especially those of NSCLC.10 After intravenous injection of FDG labeled with the positron-emitting isotope 18F, most lung cancers can be imaged using a PET scanner.11 Changes in FDG uptake after therapy may precede changes in tumor volume.12,13 PET is more sensitive and specific than CT in detecting intrathoracic lymph node metastasis,14–16 and it frequently detects previously unsuspected distant metastases.17–20 At our institution, approximately 30% of radical radiotherapy candidates become ineligible for potentially curative therapy after PET staging.21 Use of FDG-PET staging has been instrumental in achieving a near doubling in median survival for patients with NSCLC treated with radical radiation or chemoradiation at our center22 as a result of superior patient selection. PET scanning is a powerful predictor of survival in patients with suspected recurrence of NSCLC more than 3 months after completion of potentially curative treatment.23 This study is the first prospective comparison of the prognostic value of early posttreatment FDG-PET and CT scanning in a cohort of patients with NSCLC treated with radical radiotherapy.
FDG-PET scanning was performed as part of a prospective study of the value of functional imaging in NSCLC at the Peter MacCallum Cancer Institute (Melbourne, Australia). This study was initiated in 1996 after approval by the institutional clinical research and ethics committees and was in accordance with the Helsinki Declaration of 1975 (revised in 1983). Patients eligible for analysis were consecutive patients with NSCLC treated with radical radiotherapy or chemoradiotherapy who had staging PET and CT scans and elective posttreatment PET and CT scans. Patients with clear evidence of disease progression or who died before undergoing follow-up PET and CT scans were not included in this analysis; such patients constituted less than 10% of those treated with radical RT for NSCLC. The 1998 revision of the International Union Against Cancer staging system24 was used. In the first year, unconfirmed PET-apparent extensive disease did not preclude an attempt at radical treatment. With confirmation of the high accuracy of PET, it was subsequently considered unethical to give radical therapy to patients with previously unsuspected PET-apparent extensive disease. Follow-up imaging was performed after completion of radical radiotherapy after a planned interval of 4 to 12 weeks. Scans were occasionally performed outside these limits because of unavailability of FDG or transportation problems for patients residing at distant locations.
Treatment Policy
PET Scanning Acquisition and Processing
Assessment of Treatment Response Radiation-induced inflammatory changes in the lungs and pleura had a different distribution from tumor uptake and were not scored as persistent or progressive disease. These inflammatory changes conformed to the volume of irradiated lung and could be readily distinguished from persistent tumor uptake by their distribution. The majority of scans were read by one physician (R.H.), who also trained the other PET physicians who participated in the study. Scans not read by R.H. were checked and countersigned by him or by another senior PET physician. Results of studies of the reproducibility of this assessment method are not yet available. Single posttreatment CT scans were assessed for response using WHO response criteria.1 A CR was recorded if there was no evidence of a mass lesion at the location of the primary tumor, no lymph node enlargement more than 1 cm, and no evidence of progression elsewhere. When tumor diameters had not been recorded prospectively at the time of the CT scan, measurements were made retrospectively by a radiologist (A.McK.) blinded to the patient outcome and to the PET response. Patients were allocated to CR, PR, NR, and PD categories according to WHO criteria. Scans were considered nonassessable if bidimensional tumor measurements could not be made because the tumor site was obscured by atelectasis and/or pneumonitis or the tumor could not be visualized on the initial CT scan.
Statistical Methods Survival estimates were obtained using the Kaplan-Meier method and compared using the Cox proportional hazards regression model. The prognostic significance of individual factors has been summarized using hazard ratios representing the relative death rate for a given group relative to a baseline group. Ninety-five percent confidence intervals (95% CIs) have been given for the main results. Two-sided P values have been reported throughout, with no adjustment for multiple comparisons.
Characteristics of Study Patients Seventy-three eligible NSCLC patients treated with radical radiotherapy had elective posttreatment PET and CT scans between May 1997 and September 2000. There were 56 males and 17 females. The median age was 67 years (range, 49 to 80 years). Twenty-one patients had weight loss before treatment. The ECOG performance status was grade 0 in 13 patients, grade 1 in 49 patients, and grade 2 in 11 patients. The histology was squamous in 45 patients, adenocarcinoma in 17 patients, large cell in nine patients, and mixed NSCLC in two patients. The pretreatment stage was I in 13 patients, II in 14 patients, III in 46 patients, and IV in zero patients before the PET scan. After PET, the pretreatment stage was I in nine patients, II in 10 patients, III in 52 patients, and IV in two patients. All patients but two, who received 50 Gy, received 60 Gy of external-beam radiotherapy. In all but 10 (14%) patients treated with radiotherapy alone, RT was given concurrently with platinum-based chemotherapy (single-agent carboplatin, n = 47; cisplatin/taxol, n = 6; cisplatin/fluorouracil, n = 9; and cisplatin/VP-16, n = 1). During the study period, standard chemotherapy was single-agent carboplatin, but a number of patients in this study were enrolled onto phase I/II clinical trials with other platinum-based combinations mentioned above.
Comparison of PET and CT Response Assessments
All PET scans were assessable, but the CT scan results were nonassessable in six patients because of atelectasis or pneumonitis. PET was readily able to determine the response in patients who were nonassessable by CT; PET responses in these patients were CR (n = 2), PR (n = 3), and PD (n = 1). For the 67 patients assessable by both PET and CT, there was poor agreement between the two assessments, with a weighted kappa value of 0.35 (95% CI, 0.14 to 0.56; Table 1
Overall Survival At the time of analysis, 30 of the 73 patients were known to have died. Estimated median follow-up duration was 18 months.28 An estimated 67% (SE, 6%) of patients survived 1 year after their follow-up PET scan, and 41% (SE 10%) survived 2 years (Table 2  ; Fig 1). The estimated median survival was 23 months from the date of the follow-up PET scan. The average interval between the start of treatment and the follow-up PET scan was 4 months. An example of discordant CT and PET response is shown in Fig 2.
Prognostic Significance of Response Assessments Both the PET and CT scan assessments of response were significantly associated with subsequent survival duration (Table 3 ; Fig 3A and 3B). In the subset of patients with assessable responses on CT scans (ie, in whom the tumor site was not obscured by atelectasis or pneumonitis), the response categories assessed by PET seemed to have a stronger association with prognosis than those assessed by CT imaging. Adjusting for ECOG performance status, weight loss, and stage at the time of commencement of treatment, the estimated relative death rate associated with each successive response category (CR, PR, NR, or PD) on PET imaging was 3.6 (95% CI, 2.0 to 6.3; P < .0001), compared with 2.3 (95% CI, 1.2 to 4.1; P = .0060) on CT imaging. Similarly, the estimated relative death rate for non-CR versus CR patients was 4.4 (95% CI, 1.8 to 11; P = .0003) on PET imaging, compared with 3.4 (95% CI, 0.8 to 15; P = .047) on CT imaging.
In a model studying the joint significance PET and CT responses adjusting for ECOG performance status, weight loss, and stage, each increasing category from CR to PR to NR or PD was associated with an estimated relative death rate of 1.9 (P = .052) for the CT responses adjusting for PET response and 3.1 (P < .0001) for the PET responses adjusting for CT response. There was no evidence of an interaction between the prognostic significance of the PET and CT responses when they were classified in this manner (P = .37). In the same model, ECOG performance status, weight loss, and disease stage were not significant factors on multivariate analysis (P = .69, .38, and .53, respectively). Likewise, adjusting for the PET response, patients who failed to achieve a CR on CT had an estimated relative death rate of 3.0 (P = .089) relative to those who achieved a CR, whereas, adjusting for CT response, patients who failed to achieve a CR on PET had an estimated relative death rate of 4.1 (P = .0009) relative to those who achieved a CR. Again, there was no evidence of an interaction between the prognostic significance of the PET and CT responses when classified in this manner (P = .64), and ECOG performance status, weight loss, and disease stage were not significant factors (P = .87, .50, and .96, respectively). Similar results were obtained when the stage after baseline PET was used in the multifactor analyses rather than the pre-PET stage. Thus, the PET responses seem to be stronger prognostic indicators than the CT responses. Of the 10 patients with a CT CR, six also had a PET CR, and the remainder had a PET PR. There were two deaths in this group: one was a result of pneumonia without lung cancer progression in a patient with CR on both PET and CT, and the other patient, who failed to achieve a PET CR in lymph node disease, died with progressive locoregional and metastatic tumor. In the 10 patients treated with radiotherapy alone, the PET response rates (CR, 50%; PR, 30%; and NR/PD, 20%) were similar to those observed in patients treated with chemoradiotherapy.
In this study, a single, early, posttreatment PET scan provided powerful prognostic information for patients with NSCLC treated with radical radiotherapy, stratifying patients into groups with widely differing survival probabilities. In this setting, PET response was more significant than the established prognostic indices of disease stage, performance status, and weight loss. A single CT scan showed comparatively worse ability to predict survival. Most patients were categorized as partial responders, and response was nonassessable in 8% of patients. PET remained the most important prognostic factor even when corrected for CT response. All but 14% of patients in this series had a residual mass lesion apparent on their posttreatment CT scan. CT would almost certainly have performed better had serial scans been performed to evaluate changes in these residual mass lesions over time. However, this would have frustrated the aim of this study, in which we sought to evaluate the ability of a single scan performed at a relatively early time after therapy to predict survival. When first introduced, CT caused a revolution in oncology. It represented a major advance on plain radiographic studies for imaging solid tumors,29 permitting tumor visualization and measurement in three dimensions and allowing previously undetectable lesions to be seen. CT became a de facto standard assessment tool in oncology, supplemented more recently by MRI. Structural imaging became enshrined in definitions of tumor response. Although superior to earlier imaging techniques,30 CT and MRI31 have significant limitations at anatomic sites such as the lung and pleura. Irregular tumor shapes may be difficult to measure, and poor contrast at the interface between tumor and normal thoracic structures or consolidated lung may make it impossible to determine tumor response. The Response Evaluation Criteria in Solid Tumors32 have been introduced and do not require that lesions should be measurable in two dimensions. This system may increase the number of patients with assessable disease but cannot overcome the limitations of structural imaging. Preliminary reports indicate that FDG PET can usefully assess response in lung cancer33–36 and other tumors, including head and neck carcinoma,37 esophageal cancers,38 breast cancer,39 and lymphomas.40–41 Nevertheless, the value of PET compared with other modalities has been unclear. In this study, a simple qualitative approach was applied that did not require calculation of SUVs or complex assessments of total-lesion glycolysis.35 The latter methods take no account of qualitative factors, such as shape and distribution of activity, and have not been proven to give more useful results than a qualitative reading of scans. Qualitative readings of scans may, however, be operator dependent and reflect the experience and training of the individual nuclear medicine physician. Further information could potentially be obtained by integrating quantitative and qualitative data, but this area requires more research. There are no published validated criteria for visual PET response assessment with wide applicability in NSCLC. The EORTC PET response criteria were developed by consensus between a range of PET experts and currently represent the most authoritative SUV-based recommendations. The CR, PR, NR, and PD categories of our own criteria correspond closely with the same metabolic response categories in the EORTC document. Our own criteria could potentially serve as a benchmark against which alternative methods of assessment may be compared. It would be of interest to see whether results similar to those presented here could be reproduced at other centers. PET may have wide application in measuring treatment response in oncology. Because prognostic information can be obtained at a relatively early time point, therapies could potentially be modified depending on completeness of PET response. Furthermore, PET response represents a promising intermediate end point in trials evaluating novel approaches to chemoradiation in locally advanced NSCLC. CT scanning may underestimate the activity of novel antitumor agents, and this could lead to potentially useful pharmaceuticals being inappropriately discarded. Additional study is necessary to determine the optimum timing of PET scans after therapy. Longer follow-up will be required to determine the true significance of a PET CR in NSCLC, but it seems likely that most of the long-term survivors will emerge from this group of patients. It is possible that PET response could be used to rationally investigate the benefit of further therapy after chemoradiation in NSCLC. Patients with locoregionally persistent disease who would otherwise be destined to fail could potentially benefit from salvage therapies. Alternatively, patients with CRs, having demonstrated that they have sensitive disease, could potentially achieve more durable remissions with additional treatment. Longer follow-up is required to determine the natural history of patients in the PET CR and PR categories. Preliminary data from our own center indicate that patients with PET CRs have a reduced rate of subsequent distant metastasis.42 Prognostic information from PET scanning may be useful to the patients who wish to base plans for their future on the best available survival estimate. Finally, improved understanding of the role of locoregional disease control may help to define research priorities for future investigations in NSCLC.
Presented in part at the Forty-Third Annual Meeting of the American Society for Therapeutic Radiology and Oncology, San Francisco, CA, November 6–8, 2001, and the Thirty-Sixth Annual Meeting American Society for Clinical Oncology in New Orleans, LA, May 19–23, 2000.
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Copyright © 2003 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
PR 
