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Positron Emission Tomography in Limited-Stage Small-Cell Lung Cancer: A Prospective Study

From the Departments of Radiation Oncology and Radiology, Mallinckrodt Institute of Radiology; Department of Internal Medicine; Division of Biostatistics; and the Alvin J. Siteman Cancer Center, Washington University School of Medicine, St Louis, MO

Address reprint requests to Jeffrey D. Bradley, MD, Department of Radiation Oncology, Washington University School of Medicine, 4921 Parkview Place, St Louis, MO 63110; e-mail: Bradley{at}radonc.wustl.edu

	ABSTRACT

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PURPOSE: To determine how often positron emission tomography with [¹⁸F]fluoro-2-deoxy-D-glucose (FDG-PET) detects extensive-stage small-cell lung cancer (SCLC) in patients considered to have limited-stage disease based on conventional staging procedures, and to determine the impact of PET on treatment planning for presumed limited-stage SCLC.

PATIENTS AND METHODS: We prospectively performed pretreatment FDG-PET on 24 patients determined by conventional staging methods to have limited-stage SCLC (defined as disease that could be encompassed within a reasonable radiotherapy portal, excluding bilateral supraclavicular disease). PET images were evaluated for evidence of extensive-stage disease. Tumor-node-metastasis system staging was also assigned for each patient, with and without PET information.

RESULTS: FDG-PET demonstrated findings consistent with extensive-stage SCLC in three of 24 patients. FDG-PET correctly upstaged two (8.3%) of 24 patients to extensive-stage disease (95% CI, 1.03% to 27.0%). PET correctly identified tumor in each SCLC mass (primary or nodal) that was suspected on computed tomography (CT) imaging, thus giving a lesion-based sensitivity relative to CT of 100%. PET identified unsuspected regional nodal metastasis in six (25%) of 24 patients, and the radiation therapy plan was significantly altered to include the PET-positive/CT-negative nodes within the high-dose region in each of these patients. Brain PET images in 23 patients disclosed no evidence of brain metastasis.

CONCLUSION: FDG-PET has high sensitivity for SCLC and appears to be of value for initial staging and treatment planning of patients with presumed limited-stage disease.

	INTRODUCTION

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Accurate staging of small-cell lung cancer (SCLC) is critical for patient treatment and prognosis. The most common staging system was adopted from the Veterans Affairs Research Service Lung Group.¹ In this simple two-stage system, limited-stage disease is defined as tumor confined to one hemithorax and the regional lymph nodes, whereas extensive-stage disease is defined as disease beyond these bounds. Patients with limited-stage disease are offered combination chemotherapy and concurrent thoracic radiation therapy. Patients with extensive-stage disease are offered combination chemotherapy without thoracic irradiation.

The routine staging of SCLC includes computed tomography (CT) of the chest to assess locoregional disease, as well as CT of the upper abdomen, CT or magnetic resonance imaging (MRI) of the brain, and bone scintigraphy to detect metastatic disease. Approximately 60% to 70% of patients initially diagnosed with SCLC will be shown to have extensive-stage disease on one or more of these studies.² The most common metastatic sites at diagnosis are bone (19% to 38%), liver (17% to 34%), adrenal glands (10% to 17%), and brain (0% to 14%).³

In contrast to the dependence primarily on anatomic imaging features, positron emission tomography (PET) depends on the metabolic characteristics of a tissue for the detection of disease. It is known that a feature of malignant tissue is its high rate of glycolysis, and this feature is exploited for oncologic imaging by PET with the glucose analog [¹⁸F]fluoro-2-deoxy-D-glucose (FDG). This tracer competes with glucose for uptake into cells, where it accumulates after phosphorylation by hexokinase. The amount of FDG accumulation over a fixed period is therefore proportional to the rate of cellular glucose metabolism and appears to be well correlated with the malignant potential of the tissue.⁴

There are few published studies on the utility of FDG-PET for staging of SCLC.^5-11 As expected, given the characteristically high cellular proliferation rate and short doubling time of these tumors, these studies show that SCLCs avidly accumulate FDG. SCLC has a lack of a "shoulder" on its cell survival curve relating to its rapid responsiveness to therapy. Other malignant tumors with rapid proliferation rates demonstrate avid FDG accumulation on PET; these tumors include non–small-cell lung cancers and lymphomas.^12,13 The use of FDG-PET for staging of these tumors is now standard care in institutions with access to this technology, but PET is not used routinely for staging of SCLC.

The primary objective of our study was to determine how often patients with limited-stage SCLC, based on conventional staging procedures, would be determined to have extensive-stage disease based on the findings of FDG-PET. We also sought to determine the impact of PET on treatment planning in patients with presumed limited-stage SCLC.

	PATIENTS AND METHODS

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We prospectively studied patients with newly diagnosed, untreated, histologically or cytologically confirmed SCLC. The protocol was approved by our institutional review board, and each patient gave written informed consent before participating in the study. Eligible patients were required to have (1) completed standard staging procedures, including history and physical examination, chest radiography, CT of chest, CT of upper abdomen to include the adrenal glands, bone scintigraphy, and either contrast-enhanced CT or MRI of the brain; and (2) no evidence of disease beyond one hemithorax and the mediastinum. Patients with bilateral hilar involvement were defined to have limited-stage disease. Patients with ipsilateral supraclavicular adenopathy on physical examination or CT were also eligible for inclusion in the study. The protocol required that all conventional staging procedures be completed within 4 weeks before PET. The American Joint Committee on Cancer system was used to assign a tumor-node-metastasis system stage for each patient, with and without the PET information.¹⁴

PET Imaging and Interpretation
FDG-PET was performed following a minimum 4-hour fast. To exclude fasting hyperglycemia (ie, diabetes-related), a blood sample for determination of the blood glucose level was obtained by glucometer before FDG administration, and PET was not performed if the fasting blood glucose concentration exceeded 150 mg/dL. The patients were positioned supine, with both arms comfortably positioned over the head whenever possible. Beginning 50 minutes after intravenous injection of 10 to 15 mCi of FDG, a series of overlapping transmission and emission scans (2-minute transmission and 5-minute two-dimensional emission scans at each bed position) were performed to image the region from the upper/mid neck to the upper thigh with a CTI/Siemens ECAT HR+ scanner (Siemens-CTI, Knoxville, TN). The emission images of the body were reconstructed with an ordered-subset estimation-maximization iterative algorithm with segmented attenuation correction. Transmission images and non–attenuation-corrected images were reconstructed by filtered back projection. After completion of body imaging, FDG-PET of the brain was performed as a separate acquisition (10 minutes in three-dimensional mode). The brain images were reconstructed by filtered back projection with a mathematical attenuation correction.

FDG-PET images were interpreted prospectively by subjective visual assessment (with use of a receiver-operating-characteristic grading scheme) for the presence of abnormal accumulation of FDG. Two experienced nuclear physicians first independently interpreted the PET images blinded to the results of conventional imaging studies. These observers then reread the PET images in combination with the conventional imaging studies. The independent readings from each of the two nuclear physicians were recorded for both the blinded PET and the unblinded PET readings for each patient. This was done to determine if the combined interpretation of FDG-PET and conventional imaging studies was more accurate than the interpretation of FDG-PET separately, and to determine the extent of interobserver variability. The final PET interpretation was based on a consensus of the two observers for the unblinded readings.

To obtain data about the avidity of SCLC for FDG, the PET images also were evaluated semiquantitatively by determination of the maximum standardized uptake value (SUV_max) for the primary tumor and for up to five sites of mediastinal metastatic disease.¹⁵ For each patient, the average SUV_max of the primary tumor and the mediastinal sites was computed.

Further Patient Evaluation and Therapy
The management of the patients enrolled in this study after the completion of FDG-PET was left to the discretion of the referring physician. However, confirmation of potential extensive-stage disease (ie, extrathoracic areas of abnormally increased FDG uptake) by biopsy was encouraged. For the rare exception of an FDG-avid lesion that was not seen on dedicated diagnostic images, biopsy was not required. The following specific approaches for further evaluation or biopsy were outlined in the protocol, which allowed for the fact that biopsy would not always be possible (eg, for lesions that are not visible on anatomic imaging or are too small [< 1 cm] to biopsy).

PET-positive intrapulmonary parenchymal metastases that were considered outside a reasonable radiotherapy portal by the radiation oncologist were to undergo biopsy to confirm metastatic disease. Thin-cut CT-guided or ultrasonography-guided fine-needle aspiration was suggested for biopsy of lesions where these approaches were technically feasible. If a liver abnormality was detected by FDG-PET, biopsy or fine-needle aspiration cytology was recommended to confirm metastatic disease. Any adrenal lesion detected on FDG-PET was to be biopsied to confirm metastatic disease. Bone abnormalities that were seen on FDG-PET were to be further evaluated by appropriate imaging studies (conventional radiographs, CT, MRI, or repeat bone scintigraphy, if considered clinically appropriate) or by biopsy in order to exclude metastatic disease. In cases where multiple bone metastases were suspected, diagnostic imaging with bone scintigraphy or MRI was satisfactory.

Statistical Methods
Although limited-stage SCLC is a relatively uncommon condition, a target of 25 patients over 2 years was achievable at our institution. This limited prospective study was designed to assess whether the frequency of upstaging was at least 10%; this was judged to be a clinically relevant upstaging frequency that would be worthy of further investigation in a multicenter study. If no cases of extensive-stage disease were found in a sample of 25 patients, the 95% confidence limits (CLs) for the yield of PET in this setting would extend from 0% to 11%. The corresponding 95% CLs for detection of one, two, and three patients with extensive-stage disease are 0.1% to 20%, 1% to 26%, and 3% to 31%, respectively. Therefore, the detection of two or three patients with extensive-stage disease would provide evidence that PET can correctly upstage at least 1% and perhaps as many as 25% to 30% of patients.

	RESULTS

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Twenty-five eligible patients (11 men and 14 women aged 33 to 90 years; mean, 60 years) consented to participate in the study between February 2001 and March 2003. One patient refused to undergo PET after giving consent, and withdrew from the study. The results for the remaining 24 patients are reported here.

Table 1 describes the tumor-node-metastasis system staging changes that occurred as a direct result of FDG-PET, as well as the average of the maximum SUV_max values measured for each patient.

FDG-PET demonstrated findings consistent with extensive-stage SCLC in three of the 24 patients. Metastatic disease was confirmed in one of these patients, in whom PET demonstrated increased FDG uptake in the femur and ischium (Fig 1). This patient had had negative bone scintigraphy 1 week before the PET study. These metastases were confirmed by subsequent bone scintigraphy 2 months later. In the second patient, PET demonstrated bilateral supraclavicular lymphadenopathy. The presence of contralateral supraclavicular disease was defined as extensive-stage disease for the purposes of the study. Therefore, this patient was scored as having extensive-stage disease. At the discretion of the treating physician, this particular patient received definitive chemotherapy and radiation therapy and currently remains disease-free 15 months after therapy completion. The third patient had a positive PET reading in a contralateral lung nodule. This contralateral nodule was subsequently diagnosed as a fungal infection based on a high-resolution CT. This patient did not develop a cancer mass in this location on subsequent follow-up, and the PET result was thus considered falsely positive. Accordingly, in our study population, FDG-PET correctly upstaged two (8.3%) of 24 patients to extensive-stage disease (95% CLs, 1.03% to 27.0%). The positive predictive value of FDG-PET for extensive-stage disease was 66.7% (two of three patients).

View larger version (94K): [in this window] [in a new window]   Fig 1. A 69-year-old woman with small-cell lung cancer. Initial bone scintigraphy was negative for osseous metastasis. Positron emission tomography with [18F]fluoro-2-deoxy-D-glucose (FDG) showed intense FDG uptake in the primary tumor and mediastinal metastases, as well as focally increased FDG uptake (arrows) in the right femur and ischium. Repeat bone scintigraphy 2 months later confirmed these metastases. (A) Anterior; (B) posterior.

View larger version (103K): [in this window] [in a new window]   Fig 2. A 53-year-old woman presenting with a superior vena caval syndrome. Computed tomography (CT) demonstrated a right upper lobe mass with ipsilateral hilar and bilateral mediastinal nodal metastases, and biopsy confirmed small-cell lung cancer. Positron emission tomography with [18F]fluoro-2-deoxy-D-glucose also demonstrated bilateral supraclavicular disease that was not appreciated on CT. (A) Anterior; (B) posterior.

There was complete interobserver agreement of the unblinded PET/CT interpretation in 23 patients. The one interobserver disagreement occurred in a patient with a peripheral lung density on CT, which one observer interpreted as malignancy and the other interpreted as an indeterminate lesion. There was no disagreement between the two observers with regard to stage (limited v extensive).

Twenty-three patients underwent FDG-PET of the brain. As required by the protocol, all of these patients had previously negative CT or MRI of the brain. PET showed no findings suggestive of brain metastasis in these 23 patients.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors’ Disclosures of... REFERENCES

 
The primary purpose of this prospective study was to determine how often FDG-PET would detect distant metastasis in patients with SCLC who had been carefully staged by conventional imaging. In 24 patients with limited-stage SCLC by conventional staging, the addition of FDG-PET detected two patients with extensive-stage disease. One received definitive chemotherapy and radiation therapy for bilateral supraclavicular disease and remains free of disease with 15 months of follow-up. The other did not receive thoracic radiation therapy. FDG-PET was falsely positive for extensive-stage disease in a third patient. Accordingly, it is advisable that distant metastatic disease detected on PET be confirmed, ideally by biopsy, before a patient is denied definitive therapy for limited-stage disease.

The definition of limited-stage SCLC continues to be a matter of debate. The Veterans Affairs Research Service Lung Group¹ system continues to have relevance because of its simplicity and reliable prognostic value.^16,17 Limited-stage SCLC is defined as tumor confined to one hemithorax and regional lymph nodes. This system does not specifically address stage assignments for patients with contralateral hilar nodal involvement, contralateral supraclavicular nodal involvement, or malignant pleural effusions, leaving it up to the treating radiation oncologist to decide. For the purposes of this study, we prospectively defined limited-stage disease to include patients with bilateral hilar nodal involvement and to exclude patients with contralateral supraclavicular nodal involvement. Our report reflects this definition.

The principal value of PET in our study population was the detection of additional sites of disease within the thorax. The radiation therapy volume was enlarged in 29% of our population in order to treat the PET-detected adenopathy or primary within the high-dose region. Other studies have demonstrated this effect for NSCLC.^18-23 More recently, Kamel et al¹¹ have reported results similar to ours in a study of patients with SCLC (published after completion of our study). They reported that FDG-PET led to a radiotherapy field extension in five (29%) of 17 patients judged to have limited-stage disease before PET.

Our results differ from those reported by Schumacher et al.⁷ These investigators retrospectively reviewed the initial diagnostic PET studies in 26 patients with SCLC. Of the 14 patients with limited-stage disease by conventional imaging, seven (50%) were found to have extensive-stage disease by PET. In four of these patients, the metastatic disease was confirmed; in one patient it was disproved, and in two patients, the status of the tumor remained unverified. The lower frequency of PET-detected distant metastasis in our study is likely as a result of the stringent criteria for enrollment. Patients with questionable equivocal findings for metastasis on bone scintigraphy or CT were not enrolled. By comparison with the findings of Schumacher et al, our results are more similar to those recently reported by Kamel et al¹¹; three (18%) of their 17 patients with limited-stage SCLC by conventional staging were upstaged to extensive-stage disease by FDG-PET. Their study design was quite similar to ours in that conventional staging procedures were completed and a presumptive stage declared before the patient underwent PET.

Evidence is mounting that PET has diagnostic value in SCLC. These tumors are clearly FDG avid; the mean SUV_max for primary and mediastinal nodal lesions of SCLC in our study is similar to that reported for advanced non–small-cell lung cancers.²⁴ The sensitivity of PET relative to CT was 100% in our population. For detection of extensive-stage disease, the sensitivity was 100% (two of two patients) and the specificity was 95.5% (21 of 22 patients). There are four other reported series showing similar results. Chin et al⁸ reported a prospective trial that included 18 patients with SCLC (seven limited-stage and eight extensive-stage). FDG-PET agreed with conventional staging in 15 (83%) of 18 patients. Two patients with limited-stage disease by conventional staging were upstaged to extensive disease. One of these patients had the PET-detected metastases confirmed by subsequent bone scintigraphy. The third patient was downstaged to limited disease by PET. Therefore, FDG-PET accurately staged at least 16 patients (89%). There are no data to confirm or deny the accuracy of the staging PET in the other two. Shen et al⁹ reported a retrospective analysis of 25 patients with SCLC. The sensitivities of PET were 100%, 91%, and 92% for the primary tumor, regional nodes, and distant metastases, respectively. There were three false-positive studies and one false-negative study. Of the 10 patients who had limited-stage disease by conventional imaging, one was upstaged to extensive-stage disease by PET. Pandit et al¹⁰ reported a retrospective analysis of 46 patients with SCLC, including 38 previously treated patients. The sensitivity of PET was 100%, with pathologic correlation. In the eight untreated patients, the results of PET agreed with those of conventional staging in each of them (four limited-stage and four extensive-stage disease).

In conclusion, FDG-PET has high sensitivity for SCLC. The addition of FDG-PET to conventional imaging for patients with limited-stage disease detected distant metastases in two of 24 patients (95% CI, 1.03% to 27.0%). However, PET identified cancer in regional lymph nodes that were negative on CT, altering the therapy in six additional patients. False-positive results with PET are not infrequent. Accordingly, further evaluation with imaging or biopsy should be performed to clarify PET results before patient management is altered. PET interpretation is aided by viewing the CT images of the area(s) in question. There was good interobserver agreement of PET interpretations. Imaging of the brain with PET is not indicated if contrast-enhanced MRI or CT is normal.

	Authors’ Disclosures of Potential Conflicts of Interest

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The following authors or their immediate family members have indicated a financial interest. No conflict exists for drugs or devices used in a study if they are not being evaluated as part of the investigation. Acted as a consultant within the last 2 years: Jeffrey D. Bradley, CPS Innovations.

	NOTES

 
This work was funded by an American Cancer Society Institutional Research Grant (ACS-IRG-58-010-44).

Authors’ disclosures of potential conflicts of interest are found at the end of this article.

	REFERENCES

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Submitted November 17, 2003; accepted May 24, 2004.

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