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(Chest. 2002;122:1918-1924.)
© 2002 American College of Chest Physicians

Clinical Role of F-18 Fluorodeoxyglucose Positron Emission Tomography Imaging in Patients With Lung Cancer and Suspected Malignant Pleural Effusion*

Naresh C. Gupta, MD; John S. Rogers, MD; Geoffrey M. Graeber, MD; Jessica L. Gregory, MS; Usman Waheed, MD; David Mullet, BA and Melany Atkins, BA

* From the West Virginia University - Departments of Nuclear Medicine (Dr. Gupta), Medicine (Dr. Rogers), Surgery (Drs. Graeber and Waheed), and School of Medicine (Ms. Gregory, Mr. Mullet, and Ms. Atkins), Morgantown, WV.

Correspondence to: Naresh C. Gupta, MD, West Virginia University PET Center, Robert C. Byrd Health Sciences Center-South, Morgantown, WV 26506; e-mail address: ngupta{at}wvu.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: The goals of this study were to determine the sensitivity, specificity, and predictive accuracy of F-18 fluorodeoxyglucose positron emission tomography (PET-FDG) imaging in detecting metastatic disease involvement of pleura and/or presence of malignant pleural effusion in patients with proven lung cancer. We wanted to compare efficacy of PET-FDG imaging to CT scanning in differentiating benign pleural effusion from malignant effusion and/or pleural involvement in patients with lung cancer.

Methods: We studied 35 patients with biopsy-proven lung cancer and abnormal findings on CT scanning for presence of pleural effusion (n = 34) and/or pleural thickening or nodular involvement (n = 4). The results of positron emission tomography and CT scanning were compared to pleural cytology (n = 31), histologic findings of pleural biopsy (n = 3), and/or clinical follow-up (n = 3) for at least 1 year for presence or absence of malignant pleural effusion.

Results: PET-FDG imaging correctly detected the presence of malignant pleural effusion and malignant pleural involvement in 16 of 18 patients and excluded malignant effusion or pleural metastatic involvement in 16 of 17 patients (sensitivity, specificity, and accuracy of 88.8%, 94.1%, and 91.4% respectively).

Conclusion: PET-FDG imaging is a highly accurate and reliable noninvasive test to differentiate malignant from benign pleural effusion and/or pleural involvement in patients with lung cancer and findings of suspected malignant pleural effusion on CT scanning.

Key Words: F-18 fluorodeoxyglucose positron emission tomography • lung cancer • pleural effusion


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Pleural effusions are common in patients with non-small cell lung cancer. Many of these pleural effusions are benign and may represent benign reactive fluid collections that do not preclude curative surgery. As many as one third of patients with lung cancer have been reported to have pleural metastases at presentation.1 2 Thus, it is important to accurately differentiate benign from malignant effusion.

Several diagnostic tests have been utilized to accurately detect malignant effusion, such as CT scanning, MRI, thoracocentesis, biochemical parameters, pleural biopsy, and thoracoscopy.3 However, most of these tests are inaccurate or invasive tests, which limit their routine clinical use in differentiating benign from malignant pleural effusions. Improved accuracy can be achieved in the diagnosis of malignant effusion using thoracoscopy to directly view and sample the pleura.4 Pleural fluid analysis is also dependant on obtaining fluid by biopsy by thoracocentesis. F-18 fluorodeoxyglucose positron emission tomography (PET-FDG) imaging has already been shown to be a highly reliable and accurate test for detection and staging of lung cancer with accuracy superior to CT scanning.5 6 7 8 9 10 11 Recently, there have been anecdotal reports that PET-FDG imaging may be used as a noninvasive test in differentiating malignant from benign effusion in cases. Thus, potentially, it may become a complementary test to thoracocentesis in patients with lung cancer.

Several research studies have been directed toward determining the status of mediastinal lymph nodes or presence of node disease. There has been relatively little investigation of the relative accuracy of staging of tumor involvement or tumor disease. We performed this study to determine whether positron emission tomography (PET) imaging, by its ability to detect malignant pleural effusion, can offer a reliable test in the staging of non-small cell lung cancer. Thus, we wanted to compare accuracy of PET to CT scanning in evaluating pleural involvement or presence of malignant pleural effusion.

Our goals in the present study were to determine the sensitivity, specificity, and accuracy of PET-FDG imaging in detecting malignant pleural effusion and differentiating it from benign reactive pleural effusions in patients with proven lung cancer. We wanted to calculate the reliability, positive predictive value, and negative predictive value of PET-FDG imaging in detecting pleural involvement in patients with lung cancer. We also wanted to compare the efficacy of PET to CT scanning in detecting malignant involvement of pleura and/or pleural effusion.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Patient Population
We identified 35 consecutive patients with proven lung cancer who underwent PET-FDG imaging for suspected malignant pleural effusion or pleural metastases. All these patients either had conclusive pleural fluid cytology or clinical follow-up for at least 12 months, which confirmed the malignant or benign nature of etiology. Patients who did not have pleural cytology or definitive evidence of malignancy or benignity on follow-up were excluded from our study; therefore, patients with unsuccessful pleural tap or insufficient fluid were excluded. We examined 25 men and 10 women (age range, 33 to 84 years; mean ± SD age, 69.7 ± 9.38 years). All 35 patients included in our study had biopsy-proven lung cancer. All patients were undergoing evaluation for staging of the known lung cancer. Only patients with abnormalities on CT that were suggestive of presence of malignant pleural effusion were eligible for our study. The suspected malignant pleural effusion was based on presence of at least one of the criteria for malignant pleural thickening: presence of nodularity, and irregularity or pleural thickness > 1 cm with presence of a pleural effusion. All patients underwent chest CT and whole-body PET scanning as part of staging workup.

PET Imaging
All patients were asked to fast for at least 4 h prior to undergoing the FDG-PET study. FDG-PET imaging was performed using a GE Advance scanner (GE Medical Systems; Waukesha, WI) of whole-body capability in the two-dimensional mode with an axial field of view of 14.6 cm. This scanner has a transaxial in-plane resolution of 4.7 mm. By performing four to five bed positions, PET imaging included the entire field of view from the neck to the pelvis floor. Emission scans were obtained with an acquisition time of 5 min per field of view. Transmission scans were obtained for 3 min in each bed position.

Emission scanning was performed 60 min after administration of 10 mCi of F-18 fluorodeoxyglucose (FDG). Transmission scanning was performed following the emission scanning for attenuation correction. All patients received 10 mCi of FDG, which was produced on site using GE Trace Cyclotron (GE Medical Systems). The acquired data were reconstructed by using standard back-projection technique. Axial views and images were reoriented into coronal and sagittal views.

CT Imaging
CT was performed using GE 9800 systems (GE Medical Systems). All studies were performed after IV injection of 100 to 200 mL of contrast (hypaque) material. One-centimeter-thick contiguous image sections were obtained.

Scan Interpretation
All studies were interpreted prospectively independently, and findings were classified as positive or negative according to established criteria. An experienced chest radiologist interpreted CT scans. CT scans were reviewed for presence of primary tumor, enlarged lymph nodes, presence and location of extra thoracic metastases, and presence, size, and location of pleural mass, thickening, or pleural effusion. The pleural effusions were graded as small, moderate, or large in amount of fluid as well as unilateral or bilateral. Experienced nuclear medicine physicians reviewed the PET scans. Interpretation of PET scans was performed without knowledge of results of other imaging studies or other surgical results. Interpretation of the PET studies included review of the uncorrected and attenuation corrected scans. A 5-point visual scoring system was used to interpret PET abnormalities: 1, no detectable or very mild uptake; 2, uptake less than background mediastinal activity; 3, uptake equal to background liver uptake; 4, uptake greater than background mediastinal uptake; 5, uptake much greater in intensity than background mediastinal activity. FDG uptake scores of 4 and 5 were classified as malignant, and scores of 1 to 3 were benign. In case of equivocal findings, standard uptake values were considered to make the final decision. Quantitation of FDG uptake was also performed using the region of interest analysis. A region of interest was carefully drawn to include entire extent of the lesion, and maximum values of the standard uptake values were determined using counts in equivocal cases only (values > 3 were considered as malignant). PET imaging studies were initially read without knowledge of CT scans or histology results and were reinterpreted (or reread) with the comparison of PET findings and CT scans.

Results of FDG-PET were correlated with pathologic diagnoses made with thoracocentesis or pleural biopsy. Pleural fluid cytology was obtained in 32 of 35 patients in our study using the pleural fluid collected by thoracocentesis. Three patients also underwent pleural biopsy. In three patients with no histologic results, follow-up CT scans were reviewed over a 1-year clinical follow-up. Serial CT and PET studies over the next 1 year were reviewed for increase or decrease in size and extent of pleural effusion and pleural thickening. Simultaneously, the course of other malignant lesions was also recorded; therefore, progression or regression of effusion or metastatic disease was used to determine benign or malignant nature of pleural effusion.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
We studied 35 patients with radiographic findings of pleural effusion and/or pleural nodular involvement on chest radiography and/or CT with proven lung cancer at the time of study or previously. Of 35 patients, 18 patients had evidence of malignant effusion either on histology and clinical follow-up (n = 16) or clinical follow-up (n = 2), while 17 patients had either negative histology (n = 16) or clinical follow-up (n = 1) [Table 1 ].


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  		Table 1.. Summary of CT, PET, and Pathology Findings in 35 Patients*

 
Histologic Findings
All 35 patients had biopsy-proven primary lung cancer. The histologic cell types of primary lung malignancy were as follows: adenocarcinoma (n = 20), small cell carcinoma (n = 8), poorly differentiated cell carcinoma (n = 1), and squamous cell carcinoma (n = 6).

Pleural fluid cytology was performed in 31 of 35 patients. Two patients had pleural metastases confirmed on pleural biopsy. One of these two patients also had positive pleural cytologic findings (Fig 1 ). In 15 of 31 patients, cytologic findings were positive for the presence of malignant cells. One patient had malignant pleural involvement on pleural biopsy alone, while one patient had positive biopsy and cytology results. One patient showed evidence of fibrosis on pleural biopsy. In all, three patients underwent pleural biopsy.



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  		Figure 1.. A 54-year-old woman with poorly differentiated lung carcinoma and left-sided pleural effusion and pleural nodularity in the left upper lung. Pleural fluid cytologic findings were negative; on follow-up, there was regression of pleural abnormalities in the left lung. CT scans (top, A, middle, B) showed left-sided pleural effusion in the left lung base (A, arrow), with a left hilar mass as well as thickening and nodular abnormality in the left upper lung posterior pleura (B, arrow). PET scans (bottom) showed hypermetabolic areas consistent with tumor sites in the left hilum and the left upper lung (arrows) with only mild uptake (grade 2 uptake) in the pleural effusion and/or upper lobe posterior parietal pleura.

 
Cytologic findings were negative for the presence of malignant cells in 16 of 31 patients. The final cytologic findings in these patients are as follows: reactive mesothelial cells and acute inflammatory cells (n = 5), inflammatory cells and occasional mesothelial cells (n = 2), acute and chronic inflammatory cells (n = 2), and negative for malignant cells (n = 7). In three patients (three of these last seven patients with negative cytologic findings), pleural effusion was probably secondary to congestive heart failure.

Two other patients had malignant effusion established on clinical follow-up alone, as cytology failed to confirm malignant involvement due to insufficient pleural fluid in the specimen. Another patient refused to undergo a pleural tap. Two patients showed regression of pleural fluid confirming benign etiology, while one patient had marked progression consistent with malignant involvement.

One of the three patients with benign effusion had a recent myocardial infarct. In all patients with negative pleural cytologic findings, PET-FDG study was read as negative for abnormal FDG uptake in pleura or pleural metastatic involvement (Fig 3 ).



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  		Figure 3.. A 62-year-old man with history of lung cancer was admitted to the hospital with a large left pleural effusion. Top, A: CT scanning showed a large, left-sided pleural effusion (arrow) without any clearly defined lung or pleural mass. Bottom, B: Whole-body PET-FDG study (coronal view) demonstrates no FDG uptake in the left pleural cavity or pleura itself. There was no focal hypermetabolic abnormality seen. There was a general void in the region corresponding to the pleural effusion. Pleural cytologic findings showed inflammatory cells with no malignant cells seen. The patient’s condition improved over the next 2 weeks, and the pleural effusion resolved over 2 to 3 weeks.

 
CT Findings
CT scanning showed presence of pleural effusion in 34 of 35 patients. One patient had nodular thickening of pleura without pleural effusion. Three patients also had diffuse thickening of pleura along with pleural effusion (Figs 1 2 3 ). Based on CT findings, malignant involvement was considered possible in all 35 patients. In 31 of 34 patients, pleural effusion was unilateral and on the same side as primary lung cancer. In three patients, the pleural effusions were bilateral (Fig 2) , and all of these three patients had advanced stage IV lung cancer with bilateral lung lesions. Of three patients with bilateral effusions, two had large pleural effusion and one patient had a small effusion. In 31 patients with unilateral effusion, effusion was classified as small (n = 7), moderate (n = 13), and large (n = 11). Two patients with nodular pleural thickening had small pleural effusion, and another patient with moderate effusion had thickened pleura. Based on CT findings, the primary lung cancer was staged as follows: stage I (n = 1), stage II (n = 20), stage III (n = 2); stage IV disease was present in 12 patients. Three patients with stage II disease on CT were found to have stage III disease on PET, and four patients had unsuspected metastases on whole-body PET-FDG imaging. In all patients, the presence of malignant effusion was believed to be important to be established for staging and further management.



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  		Figure 2.. A 46-year-old man with a large right and small left pleural effusion. CT scanning (top, A) showed pleural effusions bilaterally (arrows) as well as airspace disease in the right lung. In addition, there was infiltrate and/or atelectasis seen in the right mid and lower lung. Whole-body PET-FDG imaging (bottom, B) showed enhanced FDG uptake in the right pleura and pleural effusion (arrow). Additionally, there was increased uptake in right mid-lung parenchyma. Pleural cytologic findings were positive for malignant cells suggestive of adenocarcinoma of the lung. The pleural effusion slowly resolved from the left thorax.

 
Clinical Follow-up
In 3 of 35 patients, pleural fluid cytology or biopsy results were not available because biopsy was either refused (n = 1) or unsuccessful (n = 2). In these three patients, repeat CT and PET studies were available over the next 1 year. In one patient, repeat studies showed progression in size of pleural effusion as well as spread of disease, and had evidence of pleural nodularity on repeat studies suggestive of metastatic disease. Two patients had complete regression of pleural effusion, and effusion was believed to be due to associated inflammatory process. These three patients with no histologic or cytologic results did not receive any therapy during or before the follow-up interval.

PET-FDG Findings
We noted increased FDG pleural uptake in 17 of 35 patients. In 14 of these patients, there was histologic evidence of malignant pleural effusion (n = 13) or nodular pleural metastatic involvement (n = 1). Two patients with malignant pleural effusions were read to be negative for pleural uptake on PET scans. Both of these patients had small pleural effusions and showed mild uptake that was believed to be less intense than uptake characteristic of malignancy. In both patients, PET showed primary lung cancer as well as mediastinal nodes. In 15 of 16 patients with negative pleural histologic findings, PET-FDG uptake was normal in pleura. In one patient with benign effusion, findings of the initial PET-FDG study were considered to be positive for pleural involvement. On a repeat study, this patient showed regression of pleural effusion and pleural cytologic findings were negative. The exact cause of pleural effusion remained unknown in this patient, and biochemical analysis was not performed due to insufficient fluid. Thus, PET-FDG was found to have a sensitivity of 88.8%, a specificity of 94.1%, and a predictive accuracy of 91.4% for detecting malignant pleural effusion or metastatic pleural involvement. The positive predictive value of PET-FDG was 94.1%, and negative predictive value was 88.8%.

In 15 of 16 patients with lung cancer but benign pleural effusion, CT findings had suggested malignant pleural effusion. However histology confirmed that 9 of these 16 patients had inflammatory cause while no evidence of malignancy was seen on cytology in the other 7 patients. These seven patients also showed regression of pleural effusion on follow-up. In three patients, etiology was assumed to be congestive heart failure. Two patients with no cytology showed complete regression of fluid on follow-up and were presumed to have inflammatory process. The final etiology in two other patients remained unclear on follow-up. PET-FDG accurately characterized nonmalignant etiology in 15 of 16 patients with nonmalignant pleural effusion on cytology and/or follow-up.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
Pleural involvement is not an uncommon finding in patients with lung carcinoma. However, differentiation between benign and malignant effusion may be critical for accurate determination of the resectable status of the lung tumor. Most lung cancer patients may have potentially unresectable disease in the presence of malignant pleural effusions. Similarly it is very useful to diagnose the benign etiology of pleural effusion to prevent delay in the surgical treatment of resectable lung cancer.

Pleural thickening or nodularity on CT scanning may be suggestive of metastatic pleural disease.12 Findings of multiple pleural nodules and nodular pleural thickening may also be seen in empyemas and may not definitely differentiate between malignancy and empyema.13 Thus, presence of these findings with pleural effusion can be seen with benign causes. CT findings alone are not conclusive of benignity or malignant nature of pleural disease. Similarly, other diagnostic tests including MRI imaging have failed to show high accuracy in differentiating benign from malignant pleural effusions.14 Clinicians often have to resort to invasive thoracocentesis to establish the diagnosis of malignant pleural effusion;15 16 however, thoracocentesis may also fail to reveal positive results in 30 to 40% of patients with malignant pleural effusion.

At times, a repeat thoracocentesis may be required to exclude malignancy.17 The belief that malignant effusions are almost always exudative and virtually never transudative may not be true. Investigators have documented that up to 20% of pleural effusions occurring in patients with malignant disease may be transudates. Also Light’s criteria can occasionally misclassify a benign transudative effusion as an exudate.18 Thus, some investigators recommend that cytopathologic examination of the pleural fluids should be included in the workup of all new pleural effusions. Since it may be difficult to confirm a malignant effusion, TNM staging allows this diagnosis to be made on the basis of subjective criteria alone. Also various biochemical parameters using biochemical analysis of pleural fluids have generally yielded disappointing results in differentiating benign and malignant effusions.19 It is in this setting that a new noninvasive test such as PET-FDG may be clinically useful in detecting malignant pleural effusion.

PET-FDG may be more accurate and reliable (accuracy, sensitivity, and specificity of 91%, 88%, and 94%, respectively) than thoracocentesis when thoracocentesis is unsuccessful or results are questionable.20 Furthermore, it may provide a noninvasive alternate method to differentiate benign from malignant effusion. The accuracy of PET-FDG in our study and one previously published study is greater than pleural fluid cytology.15 In our study, PET accurately classified 32 of 35 patients (91.4%). PET findings were false-negative in two patients. Both these patients had small pleural effusion where intensity of uptake was not considered to be high enough to indicate malignant involvement. In both these patients, ipsilateral pleural effusion was positive on cytologic evaluation. However, PET findings were true-negative in 15 of 16 patients with benign effusions. Only one patient with increased FDG uptake showed negative cytologic findings and regression of pleural fluid on clinical follow-up. While underlying etiology was not known, inflammatory process could have been the most likely cause based on clinical follow-up. The major contribution of PET was its high negative predictive value, thereby preventing repeat thoracocentesis or thoracoscopic biopsy in patients with negative PET findings and benign effusion. In the majority of patients, CT findings were indeterminate for exact etiology of pleural disease or pleural effusion. Our study included a greater number of benign effusion than in the published study by Erasmus et al.20 The larger sample size probably accounts for the high specificity of PET found in our study; therefore, we believe that PET imaging can play a significant role in lung cancer patients with pleural effusion and normal or equivocal involvement of pleural surface on CT scanning. PET provides a useful noninvasive alternate prior to consideration of thoracoscopic biopsy. If PET and cytologic results are concordant, those patients should be managed accordingly due to the high accuracy shown in our study. While we shall await confirmation of our results by other similar study, there appears to be sufficient evidence for clinical application of PET imaging in patients with questionable cytologic results.

One limitation of our study may be the small number of patients (2 of 35 patients) who underwent thoracoscopic biopsy. This may not be necessary in patients with positive cytologic findings. Although patients with negative PET and negative cytologic findings could potentially still have positive malignant involvement of pleura with or without malignant effusion, there was no clinical evidence of progression of pleural effusion or disease on repeat CT and PET scanning studies. In fact, regression of pleural fluid on follow-up studies confirmed nonmalignant etiology in most of these patients.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
In summary, PET-FDG may be a useful noninvasive diagnostic test for evaluation of pleural effusions in patients with lung cancer. Incorporation of PET-FDG imaging in the diagnostic algorithm used for differentiating benign from malignant effusion may improve the accuracy of staging of patients with lung cancer. PET-FDG may provide a useful alternate diagnostic method to invasive tests in patients with suspected malignant pleural effusion especially in patients with equivocal findings on CT or negative results of pleural cytology on thoracocentesis but clinical or radiographic suspicion.


   Footnotes
 
Abbreviations: FDG = F-18 fluorodeoxyglucose; PET = positron emission tomography; PET-FDG = F-18 fluorodeoxyglucose positron emission tomography

Received for publication October 19, 2001. Accepted for publication July 10, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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  12. Trail, ZC, Davies, RJ, Gleeson, FV Thoracic computed tomography in patients with suspected malignant pleural effusions. Clin Radiol 2001;56,193-196[CrossRef][ISI][Medline]
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