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FDG PET of Pleural Effusions in Patients with Non—Small Cell Lung Cancer

¹ All authors: Department of Radiology, Duke University Medical Center, Box 3808, Durham, NC 27710.

Received September 8, 1999; accepted after revision November 9, 1999.

 
Address correspondence to J. J. Erasmus.

Abstract

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OBJECTIVE. We determined the ability of ¹⁸F-fluorodeoxyglucose (FDG) positron emission tomography (PET) to differentiate benign and malignant pleural effusions in patients with non—small cell lung cancer.

MATERIALS AND METHODS. Over a 6-year period, we reviewed all patients with primary non—small cell lung cancer and a pleural effusion on staging CT who underwent FDG PET. We examined 25 patients (18 men and seven women; age range, 37-86 years; mean age, 65 years). FDG PET revealed positive findings if pleural activity was greater than background mediastinal activity; FDG PET revealed negative findings if pleural activity was the same as or less than background mediastinal activity. Results of FDG PET were correlated with pathologic diagnosis determined with thoracentesis or pleural biopsy.

RESULTS. All patients had effusions on the same side as the primary tumor. Twenty-two patients had a malignant pleural effusion confirmed with thoracentesis (n = 19) or biopsy (n = 3). FDG PET revealed positive findings in 21 patients and negative findings in one. Three patients had no evidence of malignancy in the pleural space determined with cytologic findings (n = 2) or biopsy results (n = 1). FDG PET uptake revealed positive findings in one of these patients and negative findings in two. Therefore, of 22 patients with positive findings on FDG PET, 21 had pleural metastases, and of three patients with negative findings on FDG PET, one had metastases. The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of FDG PET for detecting pleural metastases were 95%, 67%, 95%, 67%, and 92%, respectively.

CONCLUSION. This study suggests that FDG PET may be useful in improving staging evaluation in patients with non—small cell lung cancer and a pleural effusion. Increased pleural FDG uptake usually indicates pleural metastases; however, because the number of benign effusions studied was small, the relevance of negative findings on FDG PET in this setting is uncertain.

Introduction

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Pleural effusions are common in patients with non—small cell lung cancer. Many of these effusions are malignant, indicating pleural metastases and nonresectable disease; however, some are benign reactive fluid collections that do not preclude potentially curative surgery. It can be difficult to differentiate the two types of effusions because the absence of malignant cells in pleural fluid does not necessarily exclude pleural metastases.

Over the past several years, positron emission tomography (PET) has become a clinically useful, noninvasive study that complements conventional imaging in the examination of patients with non—small cell lung cancer. PET of patients with non—small cell lung cancer is typically performed with the radiopharmaceutical ¹⁸F-fluorodeoxy-glucose (FDG), a D-glucose analog. The metabolism of glucose by malignant cells is enhanced, resulting in increased uptake and accumulation of FDG. This allows differentiation between malignant and benign abnormalities. Studies show that FDG PET is accurate in detecting nodal and extrathoracic metastases in patients with non—small cell lung cancer, and in a single recently reported series, FDG PET was accurate in differentiating benign and malignant pleural disease [1,2,3,4,5,6,7,8,9,10,11].

We evaluated the ability of FDG PET to differentiate benign and malignant pleural effusions in patients with non—small cell lung cancer. We were particularly interested in determining the positive and negative predictive values of FDG PET of the pleura in these patients.

Materials and Methods

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From 1993 to 1999, all patients with non—small cell lung cancer, a pleural effusion, and FDG PET of the thorax at initial presentation were retrospectively identified. We examined 18 men and seven women (age range, 37-86 years; mean age, 65 years).?,?

View larger version (146K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —73-year-old man with non—small cell cancer and large left-sided pleural effusion. CT scan shows large left-sided pleural effusion and reveals diffuse and nodular thickening of left visceral (arrowheads) and parietal pleura, respectively. Note enlarged paracardiac and paraesophageal nodes (arrows).

View larger version (77K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —73-year-old man with non—small cell cancer and large left-sided pleural effusion. Axial positron emission tomographic image with 18F-fluorodeoxyglucose shows marked increased uptake in visceral and parietal pleura (arrowheads). Note increased mediastinal nodal uptake (arrows) suggestive of metastases. L = liver, V = vertebral body.

All patients underwent staging thoracic CT. Although CT scans were obtained using a variety of techniques, most were obtained on a HiSpeed Advantage scanner (General Electric Medical Systems, Milwaukee, WI) using a 10-mm collimation and a pitch ratio of 1:1. Twelve CT scans were obtained with and 13 CT scans were obtained without IV contrast material. CT scans were reviewed by two thoracic radiologists for the size and location of primary tumor; presence and location of enlarged lymph nodes; presence and location of thoracic, hepatic, bone, or adrenal metastases; and presence, size, and location of pleural mass, thickening, or effusion. The size of pleural effusions was defined as small (<1 cm anteroposterior depth on supine CT images), moderate (1-3 cm anteroposterior depth on supine CT images), or large (>3 cm anteroposterior depth on supine CT images). Results were reached by consensus.

FDG PET was performed in patients either as part of a research protocol or when a clinical suspicion of metastatic disease was present. FDG PET was performed in all patients within 21 days of thoracentesis or pleural biopsy. FDG PET was performed using a variety of techniques; however, most imaging was performed on an Advance tomographic scanner (General Electric Medical Systems) with an axial field of view of 15.2 cm that produced 35 image planes (18 direct planes and 17 cross planes) spaced by 4.25 mm. Transmission scans were obtained over the chest and upper abdomen using rotating germanium-68 pin sources either before or after FDG administration. Emission images of the chest and upper abdomen were obtained starting 1 hr after the IV administration of approximately 10 mCi (370 MBq) of FDG. Transmission images were reconstructed using a filtered backprojection with a Hann window width of 7 mm. Emission images were reconstructed using a filtered backprojection with a Hann window width of 5 mm. Emission data were corrected for scatter, random events, and deadtime losses using manufacturer's software. Imaging pixel size was 3.0 mm in a 128 array.

FDG PET studies were reviewed in axial and coronal format by two experienced observers to assess focal or diffuse uptake of FDG by the pleura. FDG uptake was considered positive if pleural activity was greater than background mediastinal activity and negative if pleural activity was the same as or less than background mediastinal activity. Results were reached by consensus. Results of FDG PET were correlated with pathologic diagnoses made with thoracentesis or pleural biopsy. The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of FDG PET for detecting pleural metastases were calculated, and for each parameter, the 95% confidence intervals (CIs) were determined.

Results

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Malignant Effusions
Twenty-two patients had pleural metastases confirmed with cytologic evaluation of the pleural fluid (n = 19) or pleural biopsy (n = 3). Pleural effusions were exudative in all 12 patients in whom biochemical analysis of the effusions was performed.

CT showed that all the effusions were on the same side as the primary non—small cell lung cancer. The effusions were classified as small (n = 10), medium (n = 6), or large (n = 6). The pleural surface was normal in 11 patients. In the remaining 11 patients, the pleura was abnormal and was either nodular (n = 4) or diffusely thickened (n = 7). CT suggested the presence of intrathoracic metastases in 18 patients and extrathoracic metastases in seven patients.

We noted increased pleural FDG uptake in 21 of 22 patients (Fig. 2A,2B,2C). PET in the remaining patient showed marked increased FDG uptake in the primary lung mass and mediastinal nodes but no abnormal uptake in the pleura. CT in this patient showed a large pleural effusion but no focal or diffuse pleural thickening. The effusion was exudative according to criteria of Light [12]. Follow-up CT 5 months later showed progression of intrathoracic malignancy and increase in the size of the effusion.

View larger version (176K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —65-year-old man with non—small cell cancer who presented with dyspnea and large left-sided pleural effusion. Cytologic evaluation of pleural fluid obtained by thoracentesis revealed negative findings for malignancy. CT scan shows large left-sided pleural effusion. Note lack of focal or diffuse pleural thickening, either of which would be suggestive of metastases. E = pleural effusion.

View larger version (103K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —65-year-old man with non—small cell cancer who presented with dyspnea and large left-sided pleural effusion. Cytologic evaluation of pleural fluid obtained by thoracentesis revealed negative findings for malignancy. Axial positron emission tomographic image with 18F-fluorodeoxyglucose shows focal increased uptake in parietal pleura (arrowheads). Note effusion (asterisks). H = heart with normal uptake in myocardium, L = liver, V = vertebral body.

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —65-year-old man with non—small cell cancer who presented with dyspnea and large left-sided pleural effusion. Cytologic evaluation of pleural fluid obtained by thoracentesis revealed negative findings for malignancy. CT scan obtained 4 months after left-sided pneumonectomy shows recurrent malignancy surrounding surgical sutures (arrowheads). Note lobular pleural thickening suggestive of pleural metastases (arrows).

Benign Effusions
Three patients had benign effusions proven with cytology (n = 2) or cytology and biopsy (n = 1). Biochemical analysis of the effusions was available in only one of these patients and the effusion was transudative. CT showed one patient with a pleural effusion on the same side as the primary malignancy and two patients with bilateral effusions. The effusions were classified as small (n = 1) or large (n = 2). The pleural surface was normal, without pleural thickening or nodularity, in all three patients. CT suggested the presence of intrathoracic metastases in all three patients, and we found no evidence of extrathoracic metastases.

Pleural FDG PET uptake was normal in two patients and increased in one. In the patient with increased FDG uptake, the effusion was large and uptake was focal (Fig. 2A,2B,2C). Pleural fluid cytologic analysis and open biopsy of the pleura were negative for malignancy. Biochemical analysis of the effusion was not performed. Both patients with normal pleural FDG uptake had bilateral pleural effusions. Fluid from thoracentesis, obtained from the pleural effusions on the same side as the primary malignancy, were insufficient for chemical analysis in one patient and transudative in the other patient. One patient had pulmonary edema and moderate right-sided and large left-sided pleural effusions that resolved with diuretic therapy (Fig. 3A,3B). The second patient had small bilateral effusions. After treatment with chemotherapeutic agents, a chest radiograph obtained 2 years later revealed resolution of the effusions but progression of pulmonary and intrathoracic nodal malignancy. FDG PET for detecting pleural metastases had a sensitivity of 95% (CI, 77-100%), specificity of 67% (CI, 9-99%), positive predictive value of 95% (CI, 77-100%), negative predictive value of 67% (CI, 9-99%), and accuracy of 92% (CI, 74-99%).

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —73-year-old man with non—small cell cancer in left lung (not shown) who presented with pulmonary edema and bilateral pleural effusions. CT scan shows medium right-sided and large left-sided pleural effusions. Note lack of focal or diffuse pleural thickening, either of which would be suggestive of metastases. Also note focal pleural calcification (arrow) caused by prior trauma.

View larger version (107K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —73-year-old man with non—small cell cancer in left lung (not shown) who presented with pulmonary edema and bilateral pleural effusions. Axial positron emission tomographic image with 18F-fluorodeoxyglucose (FDG) shows normal mediastinal and cardiac activity without increased FDG uptake in pleura. After thoracentesis of left-sided effusion, cytologic evaluation revealed negative findings for malignant cells. Both effusions resolved after patient's cardiac failure was treated with diuretic therapy. H = heart with normal uptake in myocardium, M = mediastinum, V = vertebral body.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
Pleural metastases and malignant effusions are common in patients with non—small cell lung cancer. As many as one third of patients with non—small cell lung cancer have pleural metastases at presentation. However, not all pleural effusions in these patients are malignant, and benign effusions sometimes develop in response to the tumor [13, 14]. Because a malignant effusion precludes curative resection, it is important to distinguish benign and malignant effusions in patients with potentially resectable non—small cell lung cancer [13]. The importance of this evaluation is emphasized by our study in which seven of 22 patients had potentially resectable disease if their pleural effusions were benign.

Pleural thickening or nodularity on CT is suggestive of metastatic pleural disease [15]. However, these findings can appear with benign effusions. Furthermore, because the absence of pleural thickening or nodularity does not exclude pleural metastases, it is often difficult, on the basis of CT findings alone, to predict the patients in whom tumors are resectable. MR imaging signal characteristics have been used to differentiate malignant and benign pleural effusions; however, thoracentesis is usually required to confirm the diagnosis [16,17,18]. Unfortunately, although thoracentesis is usually simple to perform, cytologic evaluation reveals positive results in only 66% of patients with non—small cell lung cancer who have a malignant pleural effusion [14]. Repeated thoracentesis has been reported to identify an additional 30% of patients with malignant effusions and is typically advocated before proceeding to pleural biopsy [19].

Biochemical analysis of pleural effusions provides an additional means of distinguishing malignant and benign effusions by determining whether the fluid is transudative or exudative. The criteria proposed by Light [12, 20] (pleural lactate dehydrogenase level >66% higher than serum lactate dehydrogenase level, ratio of pleural fluid—to—serum lactate dehydrogenase levels > 0.6, or ratio of pleural fluid—to—serum protein levels > 0.5) can be used to diagnose an exudative effusion. Malignant effusions are almost always exudative and virtually never transudative [12, 20]. Transudative effusions suggest the absence of malignancy in the pleura; therefore, these tests are useful in the staging of patients with non—small cell lung cancer [20, 21]. However, Light's criteria can occasionally misclassify a benign transudative effusion as an exudate [22, 23]. Therefore, patients with potentially resectable non—small cell lung cancer and negative findings on cytologic analysis but exudative effusions should be further examined to exclude pleural metastases [20].

The evaluation of numerous biochemical parameters (serum-effusion albumin gradient, interferon-, cholesterol, bilirubin levels), assessment of tumor markers, and performance of flow cytometry have been advocated to improve the characterization of pleural fluid but have yielded generally disappointing results [20, 24,25,26,27,28]. Because it can be difficult to confirm a malignant effusion, the TNM (tumor node metastasis) staging system allows this diagnosis to be made on the basis of subjective criteria. For instance, a nonresectable (T4) classification can be assigned if there is a strong clinical suspicion of a malignant effusion, even in the absence of positive fluid cytology [13, 29]. The presence of an effusion can also be disregarded in the staging evaluation when clinical judgment indicates that the effusion is unrelated to the tumor [13, 30].

Unfortunately, the volume of fluid obtained for biochemical analysis is occasionally inadequate, as was the case in one of the three patients in our study in whom cytologic analysis of fluid revealed negative findings for malignancy. Pleural biopsy can be performed in these patients in an attempt to establish the diagnosis. However, closed-needle biopsy of the pleura is accurate in revealing pleural metastases in only 54-60% of patients with malignant effusions [14, 31]. Improved accuracy (>95%) in the diagnosis of malignant effusions can be achieved using thoracoscopy to directly view and biopsy the pleura [14, 32].

Pleural fluid analysis is dependent on obtaining fluid by thoracentesis. FDG PET overcomes this limitation and may provide an accurate, noninvasive means to evaluate pleural disease when performance of thoracentesis is impossible or when the results of thoracentesis are questionable (accuracy, sensitivity, and specificity of malignancy of 92%, 100%, and 78%, respectively) [1]. In our study, FDG PET provided similar results to those of Bury et al. [1] in distinguishing benign and malignant effusions. The accuracy of PET in both studies is greater than that of cytologic evaluation and is similar to that of thoracoscopic biopsy [14, 32]. In our study, 21 of 22 patients with a malignant pleural effusion had increased pleural uptake of FDG. FDG PET was falsely negative in one patient with a large ipsilateral exudative effusion that revealed positive findings on cytologic analysis. In this patient, FDG PET was one of the initial studies performed at our institution, and the images obtained were of lower resolution than those of more recent studies. This may account for the false-negative result. We also had one false-positive finding on FDG PET. This patient had a large ipsilateral pleural effusion that was cytologically negative, and pleural biopsy performed at the time of pneumonectomy also revealed negative findings for malignancy. However, CT scans obtained 4 months after pneumonectomy revealed extensive pleural metastases (Fig. 2A,2B,2C), suggesting that the cytologic and histologic findings were false-negative. Therefore, we believe that patients with increased FDG uptake in the pleura on PET should be examined for pleural metastases even if cytologic results of the pleural effusion are negative for malignancy. If the lesions are potentially resectable, these patients should undergo thoracoscopic biopsy to confirm pleural metastases before undergoing surgery.

Because, in general, it is not difficult to determine that an effusion is benign (i.e., transudative) using the criteria of Light [12, 22], PET would need to have a 100% negative predictive value to completely replace thoracentesis. Only three benign pleural effusions (two of which were correctly identified) were examined in our study, and this small number prevents any meaningful clinical extrapolation of the significance of our negative predictive value. However, the real clinical problem is the tendency to underdiagnose pleural metastases when the effusion is exudative and cytologic findings are negative. FDG PET is particularly valuable in this setting because it identifies patients in whom additional staging examination, such as thoracoscopic biopsy, is required.

In summary, FDG PET is typically used as a complementary study to conventional imaging in staging patients with non—small cell lung cancer. The increased use of PET and the frequent development of pleural effusions in patients with non—small cell lung cancer make it important to determine the significance of FDG uptake by the pleura. In our study, increased FDG uptake by the pleura was highly suggestive of pleural metastases. However, because false-positive studies do occur, we recommend confirmation of pleural malignancy with thoracentesis in some cases. If the effusion is exudative but cytologic analysis reveals negative findings, then the patient should be assessed with thoracoscopic-directed biopsy of the pleura. The incorporation of FDG PET findings into the algorithm used to evaluate pleural effusions may improve the accuracy of tumor node metastasis staging in patients with a pleural effusion and non—small cell lung cancer.

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