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Prognostic Value of Thoracic FDG PET Imaging After Treatment for Non-Small Cell Lung Cancer

¹ Department of Radiology, Duke University Medical Center, Box 3808, Durham, NC 27710
² Department of Radiology, Rush Medical Center, 1750 Harrison St., Chicago, IL 60612
³ Biometry Division, Duke University Medical Center, Box 3958, Durham, NC 27710

Received June 2, 1999; accepted after revision August 11, 1999.

 
Address correspondence to E. F. Patz, Jr.

Abstract

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OBJECTIVE. We determined the prognostic value of ¹⁸F-fluorodeoxyglucose (FDG) positron emission tomography (PET) for patients with treated lung cancer.

MATERIALS AND METHODS. We examined patients who underwent FDG PET after first-line treatment for non-small cell lung cancer. FDG PET results were correlated with survival rates to determine whether FDG PET findings were predictive of outcomes.

RESULTS. After initial therapy, 113 patients with non-small cell lung cancer underwent FDG PET. One hundred patients had positive FDG PET results and a median survival of 12 months (95% confidence interval, 9.2-15.4). Thirteen patients had negative FDG PET results, and 11 (85%) of these patients are still living at a median follow-up of 34 months. The difference in survival for patients with positive and negative FDG PET results was statistically significant (p = 0.002).

CONCLUSION. FDG PET has prognostic value and strongly correlates with survival rates of patients with treated lung cancer. Patients with positive FDG PET results have a significantly worse prognosis than patients with negative results. Additionally, FDG PET may be helpful in guiding therapeutic treatments.

Introduction

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Lung cancer is a major health problem in the United States and around the world [1]. Once a patient's condition is diagnosed as lung cancer, treatment options and prognosis are usually based on several factors, including stage at presentation and performance status.

After treatment starts, patients undergo imaging studies, including chest radiography and CT. Both imaging techniques reveal residual radiographic abnormalities and rely on changes in size and appearance to measure response to treatment. However, these features do not always provide accurate assessments of therapeutic effects on tumor cells and are not always diagnostic of malignancy. Therefore, a precise method of monitoring disease response and providing prognostic information is needed to guide treatment options.

Over the past several years, ¹⁸F-fluorodeoxyglucose (FDG) positron emission tomography (PET) has been used to evaluate focal pulmonary abnormalities and the stages of lung cancer [2,3,4,5,6,7,8,9]. We determined the prognostic value of FDG PET and its correlation with survival rates for patients with treated lung cancer.

Materials and Methods

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Patient Eligibility
Over 66 months, any patient treated and monitored at our institution for non-small cell lung cancer was eligible for our study. Not all eligible patients underwent FDG PET because of scheduling limitations and patient consent. Patients were treated using a variety of protocols according to disease stage, performance status, age, and associated medical conditions. Treatment included either single or multitechnique therapy with surgery, chemotherapy, and radiotherapy.

FDG PET Imaging
Patients fasted for 4 hr before undergoing FDG PET, which was performed on a GE 4096 Plus or an Advance tomography unit (General Electric Medical Systems, Milwaukee, WI). The GE 4096 produced 15 axial images with 6.5-mm image planes. Full width at half maximum was 5 mm, and the longitudinal field of view was 10.3 cm. The Advance system produced 35 axial images with 4.25-mm image planes. The full width at half maximum was 5 mm, and the axial field of view was 15 cm. Image processing was performed on a VAX 4000-300 computer system (Digital Equipment, Marlboro, MA). Image reconstruction was performed on a VAX 3100 workstation (Digital Equipment) or an HP735 workstation (Hewlett Packard, Palo Alto, CA). Transmission scans using a rotating ⁶⁸germanium pin source were performed before emission imaging through the thorax (three bed positions, GE 4096; two bed positions, GE Advance) using 10-min emission and 15-min transmission acquisition times at each bed position. Imaging was started at least 30 min after IV injection of 10.0 mCi (370 MBq) of FDG. FDG was synthesized for imaging using standard methods [10]. Cultures were obtained to assure sterility, and testing for pyrogens was performed to exclude endotoxins. Radiochemical purity was tested after each run with standardized high-pressure liquid chromatography.

Attenuated corrected FDG PET images were interpreted by at least two physicians. FDG PET images had positive results for tumor if there was any focal area of abnormal FDG accumulation greater than background mediastinal activity in the thorax including the chest wall, soft tissue, and bony structures. Images had negative results if abnormal areas of FDG accumulation were not present [11].

Statistical Considerations
Patient survival times were defined as the time between FDG PET and the last follow-up or death date. The Kaplan-Meier survival curve was used to estimate survival probabilities in strata defined by the FDG PET results and disease stage. Because there were few patients with stage II non-small cell lung cancer, such patients were combined with the stage I patients for analysis.

We used the long-rank test to compare survival rates of patients with and without positive FDG PET results. We used the Cox proportional hazards model to examine the effects of FDG PET, stage, and previous treatment on survival. We used the Wilcoxon's signed rank test to compare the stage distribution of patients having positive FDG PET results with patients having negative FDG PET results.

Results

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Patient Characteristics
Our study included 76 men and 37 women (age range, 29-83 years; mean age, 63 years). Forty-two patients had squamous cell carcinoma, 43 patients had adenocarcinoma, seven patients had bronchoalveolar cell carcinoma, seven patients had large cell carcinoma, 13 patients had non-small cell carcinoma, and one patient had a combination of large cell and adenocarcinoma. A summary of patient characteristics is shown in Table 1.

FDG PET Results and Survival
FDG PET was performed a median of 8.1 months after first line therapy was complete (range, 2 days-108 months) (Table 2). The type of therapy and corresponding FDG PET results are shown in Table 3. A cross-tabulation of stage and FDG PET results are shown in Table 4.

Of 1·13 patients, 100 (88%) had positive FDG PET results and a median survival of 12.1 months (95% confidence interval [CI], 9.2-15.4). Thirteen patients (12%) had negative FDG PET results, and 11 of these patients (85%) are still living at a median of 34.2 months (range, 3.7-60.9 months). Two patients, both with stage IIIA disease, died at 28 and 43 months after undergoing FDG PET (Table 5). Both patients had no evidence of disease at the time of the initial follow-up FDG PET. However, one patient developed bone and liver metastases 14 months later and subsequently developed recurrence in the thorax. The other patient developed recurrent lung cancer in the chest 28 months later (Figs. 1A,1B and 2A,2B,2C).

View larger version (149K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —67-year-old man with history of stage I non-small cell lung carcinoma. Posteroanterior chest radiograph shows postoperative changes in right hemithorax. Note slight lobular fullness (arrows) adjacent to surgical clips.

View larger version (98K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —67-year-old man with history of stage I non-small cell lung carcinoma. Axial 18F-fluorodeoxyglucose positron emission tomography image in same region as A shows no evidence of recurrence. Patient had no evidence of disease 24 months after resection.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —56-year-old woman with history of stage II non-small cell lung cancer. Posteroanterior chest radiograph shows minimum heterogeneous opacity (arrow) in left hemithorax after thoracotomy.

View larger version (97K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —56-year-old woman with history of stage II non-small cell lung cancer. Axial CT image confirms minimum streaky opacity in left base (arrow).

View larger version (95K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —56-year-old woman with history of stage II non-small cell lung cancer. Axial 18F-fluorodeoxyglucose (FDG) positron emission tomography image reveals significant FDG uptake in poorly defined residual opacity (arrows). This patient had recurrent lung cancer.

Statistical Analysis
The difference in survival for patients with positive FDG PET results and patients with negative FDG PET results was statistically significant (p = 0.002) (Fig. 3). Patients with positive FDG PET results had a risk ratio of 10.3 (95% CI, 2.5-42.4).

View larger version (10K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —Survival curves for patients with positive and negative findings on 18F-fluorodeoxyglucose positron emission tomography (PET) after treatment for non-small cell lung cancer. Solid line = negative PET results, dotted line = positive PET results.

There was a significant relationship between disease stage and FDG PET results. Most early stage patients had negative FDG PET results; fewer had positive FDG PET results (Table 4). Furthermore, the effect of FDG PET results remained statistically significant after adjustment for other potentially significant prognostic variables (including disease stage and treatment). No other variable had a statistically significant relationship to survival.

Discussion

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An estimated 178,000 Americans will be diagnosed with lung cancer this year, approximately 3 million people will be diagnosed worldwide, and the annual incidence of lung cancer continues to rise [1]. After diagnosis and pathologic sampling, patients are placed in therapeutic protocols according to a number of clinical, radiologic, and pathologic characteristics. Currently, stage at presentation is the most important prognostic determinant, although other factors including performance status, weight loss, histology, and, more recently, molecular markers have been used to predict the biologic behavior of tumors [12,13,14,15,16,17,18,19,20,21,22,23]. Unfortunately, patients with similar features exhibit variable responses and survival rates [24,25,26]. Thus the search continues to find a more precise method of stratifying patients for treatment protocols. Equally important is the development of an accurate method to assess response to therapy, because tumor measurements and determining time to progression are probably inadequate if a significant effect on survival is to be realized. Although CT or MR imaging provides significant anatomic and morphologic information, they cannot differentiate lesions with different biologic behaviors. A noninvasive study capable of providing this type of information would have tremendous clinical use.

Over the last several years, FDG PET has been used in diagnosing and staging lung cancer [2, 3, 27,28,29]; a recent report suggests FDG PET has prognostic value in newly diagnosed non-small cell lung cancer [30]. Theoretically, FDG PET takes advantage of increased glucose metabolism, a basic property of tumor cells, in differentiating benign and malignant abnormalities.

Our study focused on the prognostic value of FDG PET as an indicator for survival. Our data suggest that patients with positive FDG PET results after first-line treatment, independent of disease stage or type of therapeutic intervention, have a significantly worse prognosis than those with negative FDG PET results. The median survival for patients with positive FDG PET results was 12.1 months; whereas, 85% of those with negative FDG PET results are still living at a median of 34.2 months after FDG PET. The relative risk ratio was greater than 10.

Our data may be useful in several clinical scenarios. Patients with stage I or II disease and positive FDG PET results after surgery may benefit from postoperative chemotherapy, radiotherapy, or both. Currently, no data support adjuvant therapy in this setting; however, if a high-risk group could be identified, survival rates may improve.

Patients with advanced stage III or IV disease and positive FDG PET results (after several cycles of chemotherapy or radiotherapy) may benefit from a change in therapeutic regimen, analogous to the use of gallium imaging in lymphoma [31,32,33,34,35]. Further studies must determine if this approach would improve survival rates.

We recognize this is a retrospective feasibility study with several limitations. First, because of the large number of patients at our institution, we did not study sequential patients. Although this factor may introduce a selection bias, no effort was made to recruit a specific group, and this study is representative of a general lung cancer population. Second, we did not designate specific time intervals after therapy to perform FDG PET. This factor could be addressed in a future study to determine the time at which FDG PET is most predictive of disease response. However, in some ways, this is an advantage of our study because not all patients are placed in treatment protocols or need scanning at specific intervals. Therefore, this factor does not limit the scope or applicability of our results; our study suggests that FDG PET is a predictor of survival, independent of the time studied or treatment options. Third, although there was a statistically significant difference in survival rates between patients with positive and negative FDG PET results, there were fewer patients (n = 13) with negative results. Therefore, our findings should be confirmed in a larger trial. Fourth, we analyzed only FDG PET results from the thorax. Although some patients may have had good local control, they may have had disease at distant sites not included on their FDG PET image. This may affect survival rates, particularly in patients with negative thoracic FDG PET results. However, we believe the design of our study enabled us to answer a specific question: do patients with treated lung cancer whose FDG PET results are positive in the thorax have a poor prognosis? Given our hypothesis that positive FDG PET results would portend a poor outcome, our results support our conclusions.

In summary, the data from our study indicate that FDG PET has prognostic value and strongly correlates with survival rates in patients treated for lung cancer. FDG PET results may be important in deciding when to continue or alter therapy. Future studies should determine the clinical use of FDG PET in changing therapeutic treatment for patients with lung cancer.

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