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Ann Thorac Surg 2000;70:1154-1159
© 2000 The Society of Thoracic Surgeons
a Division of Cardiothoracic Surgery, University of California, Davis, Sacramento, California, USA
b Northern California PET Imaging Center, Sacramento, California, USA
Address reprint requests to Dr Roberts, Division of Cardiothoracic Surgery, University of California, Davis, 2221 Stockton Blvd, 2nd floor, Sacramento, CA 95817
e-mail: peter.roberts{at}ucdmc.ucdavis.edu
Presented at the Thirty-sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 31–Feb 2, 2000.
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Abstract |
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Methods. A retrospective review was performed of 100 patients with early stage non-small cell lung cancer referred for positron emission tomography scan evaluation. All had pathologic confirmation of their disease. Positron emission tomography scans, radiology records, operative reports, and pathology results were reviewed. Patients with positron emission tomography scans interpreted as positive for mediastinal involvement and negative pathology at operation were selected.
Results. Seven patients were found to have a false-positive positron emission tomography evaluation for mediastinal metastases. All but 1 patient had a concurrent inflammatory process or an anatomic factor associated with the false positive. The sensitivity and specificity in detecting involved mediastinal nodes was 87.5% and 90.7%, respectively. The negative predictive value was 95.8%.
Conclusions. Although positron emission tomography has been established as an accurate modality to stage non-small cell lung cancer, false-positive evaluation of mediastinal metastases can occur in the setting of concurrent inflammatory lung diseases or for centrally located tumors. Pathologic evaluation of mediastinal disease should be pursued whenever suggested by a positive positron emission tomography scan especially in the face of those factors described.
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Introduction |
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Computed tomography (CT) is well entrenched as a tool in the armamentarium in the preoperative staging of lung cancer. It is a vital study in defining the anatomy of the pathologic growth of the tumor. Unfortunately, the size of mediastinal lymph nodes does not always correlate with their tumor involvement [6]. One centimeter is often used as a size criterion in predicting involvement with tumor. However, 21% of nodes less than 1 cm may contain cancer [7], whereas as many as 40% of those greater than 1 cm may not [8]. Mediastinoscopy, mediastinotomy, and thoracotomy remain as definitive means by which tissue is obtained, but are invasive. Presently, magnetic resonance imaging has little role in evaluating the mediastinum. Currently, there is no widely accepted, single, noninvasive way to assess the entire body in a physiologic sense.
Positron emission tomography (PET) with 2-(18F)fluoro-2-deoxy-D-glucose as a tracer (FDG-PET) is gaining use as a means of physiologically assessing tumor spread. PET is based on the fact that malignant cells have a higher rate of glycolysis than most surrounding normal structures. FDG competes with glucose for uptake into cells and as it accumulates in areas involved with tumor a higher activity is seen. Glucose is also avidly metabolized by tissues involved in a granulomatous or inflammatory processes, and therefore, there will be some false-positive results. Despite this notion, there have been published studies claiming 100% accuracy [9] and nearly perfect specificity [10]. Overall, PET is gaining a record better than CT scan in predicting mediastinal involvement. This has been found in multiple studies including a metaanalytic comparison of 14 PET studies and 29 CT studies. This demonstrated the sensitivity and specificity of PET to be 79% and 89%, respectively, versus 60% and 77% for CT scan [11]. This included a range in sensitivity from 62% to 97% and specificity from 79% to 99%. However, there have been few reports of the causes of false-positive PET findings. The use of PET scan and its availability are increasing. Its use, in combination with the other studies noted, in staging lung cancer has tremendous variability from practice to practice and across specialties such as family practice, pulmonary medicine, oncology, and thoracic surgery. False-positive results on PET scans have the potential to result in the unnecessary administration of chemotherapy before a curative resection or worse, in the potential denial for a chance at a surgical cure. We reviewed our PET scan experience with the intent of revealing some factors that may influence these results.
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Material and methods |
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PET scan imaging was obtained with a dedicated ECAT EXACT 921 PET system manufactured by CTI (Knoxville, TN) and distributed by Siemans Medical Systems (Iselin, NJ). Data acquisition, reconstruction, and display were performed using standard software. The system has an axial field of view of 16.2 cm with an intrinsic transverse resolution of 6.0 mm and axial resolution of 5.5 mm. All patients fasted for at least 4 hours before the intravenous administration of 0.143 mCi/kg FDG. After a 30- to 45-minute latent period, a six-bed attenuation corrected whole body scan was acquired. Projection and tomographic images in the axial, coronal, and sagittal planes were reconstructed with and without attenuation correction. The studies were immediately read by one or two nuclear medicine physicians with specialty in interpreting PET scan images. The reading physicians had a targeted clinical history and the pertinent CT scans available for review in virtually all patients. Standardized uptake value (SUV) was determined for all primary lesions, but used less consistently in assessing the mediastinum. Standardized uptake value is a semiquantitative method of measuring the uptake of a given lesion. It is obtained by dividing maximum activity in a lesion (micro-Curies per milliliter) by the injected dose corrected for body weight (micro-Curies per gram). Standardized uptake values were inconsistently applied to mediastinal lesions because of resolution limitations resulting from the small size of many mediastinal foci [12]. Mediastinal nodes were believed to be positive if their activity was slightly, but definitely above, mediastinal activity. This corresponded to an SUV of 2.0 or greater in most patients. Specific lymph node stations were not identified. Foci were described as being present on the right or left side and contained within the mediastinum or hilar area. Midline foci were considered ipsilateral to the tumor.
All lymph node tissue obtained from the mediastinum was obtained by mediastinoscopy, mediastinotomy, or thoracotomy. In no patient was bronchoscopic or fine needle aspiration used as a definitive staging tool. All visible and technically accessible lymph nodes were removed. At thoracotomy only ipsilateral nodes were removed. On the right, this typically included stations 4, 7, 8, 9, and 10. When performing a left thoracotomy, stations 5, 8, 9, and 10 were removed and occasionally 6 and 7 according to the American Thoracic Society classification of nodal systems [13]. Pathologic reports were reviewed to determine whether any of the mediastinal lymph nodes contained cancer. The histories and roentgenograms of those patients with false-positive results were then specifically examined to determine whether there were common elements leading to the false result. The sensitivity, specificity, accuracy, and positive and negative predictive values of PET for mediastinal lymph node involvement were calculated in the usual way.
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Results |
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All 7 patients underwent thoracotomy. Five of 7 patients underwent mediastinoscopy before the thoracotomy. One patient did not undergo mediastinoscopy because of a previous mediastinoscopy and the other because of inaccessibility. A summary of the 7 patients is given in Table 1. In two of the seven false-positive results, CT scans were also read as positive by size criterion for mediastinal adenopathy. In the other 5 patients, there were no CT findings of mediastinal adenopathy. In 2 patients, the positive PET scan results were associated with significant atelectasis seen on CT and also with mediastinal adenopathy in 1 patient. One patient had a significant history of bronchiectasis and also had mediastinal adenopathy on CT scan. A fourth patient had hemoptysis and chest wall pain secondary to invasion. All 4 of these patients had symptoms of cough and mild to moderate symptoms of bronchitis before their studies. One patient had a right lower lobe lesion with marked tracer uptake (SUV 6.0) and mediastinal activity corresponding to an SUV of 3.2. The lung nodule was diagnosed as small cell cancer and the positive mediastinal lymph nodes were found to be secondary to the patient’s longstanding rheumatoid disease. One false-positive result was believed to be the incorrect interpretation of primary tumor activity adjacent to the mediastinum. The last patient had undergone a thoracotomy 11 years previously for a squamous cell cancer but no specific factors could be identified to explain the false-positive result in the patient’s new adenocarcinoma. Figure 1 shows representative scans from three patients.
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Comment |
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In our study, results were based on surgical staging yielding a sensitivity and specificity of approximately 90%. Our results correlate with previously reported studies that used CT scanning as a complimentary study [11]. The most impressive result in our series is a negative predictive value of 95.8%. Our false-positive cases echo some of the difficulty PET imaging has had with primary lung tumors.
Bakheet and Powe [15] listed 19 causes for false-positive results in lung parenchyma on PET images. These included processes that induce an inflammatory response such as pneumonia, bronchiectasis, and active tuberculosis. Just as inflammation in the lung can produce false-positive results in the parenchyma, our patients illustrate that these processes may cause increased tracer uptake in the mediastinum. Given this notion, it is reasonable to believe that any of the factors described by Bakheet and Powe may be associated with false-positive mediastinal uptake. Because the incidence of some of these processes may vary geographically, such as aspergillosis and histoplasmosis, the incidence of false-positive results may also vary. Our patients also illustrate one additional cause of false positivity associated with a primary tumor in close proximity to the mediastinum. In this case there was no mediastinal invasion by the tumor or involvement of the lymph nodes as the PET scan predicted. Whether this effect was secondary to resolution issues and shadowing from an intense emission source or a true physiologically active lymph node is unclear. Nevertheless, centrally located tumors may cause false-positive results as do inflammatory processes (Table 2).
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There is still no clear consensus on defining a positive node. Some groups have chosen a strict SUV value [16], whereas most use a scale relative to the background intensity of the mediastinum [12]. The implications on sensitivity and specificity by setting a SUV too high or too low are obvious. Furthermore, because of technical limitations, it is not possible to accurately determine the SUV in lesions that are less than 2 cm in diameter [12].
Many factors will cause variability in resolution and accuracy from scanner to scanner. These should be considered when evaluating this extremely high technology-dependent tool. Particularly, the difference in technique and data acquisition between dedicated PET scanners and dual head gamma cameras placed in the coincidence mode may be significant. There are relatively little data on comparison of dedicated PET to dual head gamma camera scans. At least two recent studies showed decreased sensitivity of dual head gamma camera scans with lesions less than 1.5 to 2 cm [17, 18]. This resolution is critical in assessing the mediastinum. Although most studies performed appear to be at large centers with dedicated PET scanners, the number of dual head gamma camera scanners from all vendors is likely to exceed the number of PET scanners very soon [19]. Dual head gamma camera scanners permit centers to do FDG imaging at a lower cost by allowing them to also use the equipment for general nuclear medicine purposes. Rapidly evolving software also affects resolution, creating clear differences in scan quality from center to center. This is analogous to the difference between a high-resolution spiral CT of today and a conventional CT from just a few years ago. We will need to determine whether dual head gamma camera scans can stand on their own, or whether larger comparison trials will be needed. The American College of Surgeons Oncology Group is examining the utility of positron emission scanning in lung cancer (Z0050). They have chosen to include only dedicated PET scanners. When this is complete, the data may not be directly applicable to physicians practicing in areas that have access only to converted gamma counters for their PET scan studies.
There are data suggesting that using CT and PET data together improves accuracy of either alone [20]. Combining PET and CT data for mediastinal staging will improve anatomic localization of some PET abnormalities, but is unlikely to change a positive or negative result in the absence of the factors we have described. Positive PET findings should not be disregarded on the basis of a negative CT scan. PET can demonstrate metastatic involvement of normal sized lymph nodes in some patients, and for this reason has a higher sensitivity than CT. With a high negative predictive value, a negative study stands on its own. Negative PET findings in enlarged lymph nodes on CT effectively exclude metastasis as PET can be expected to detect tumor focus that is of sufficient volume to cause nodal enlargement.
The physiologic information obtained by PET scanning will likely remain a complimentary study to the anatomic details of CT scans for some time. Improvements in technology may some day allow one stop staging for lung cancer. The transmission portion of routine scans may be modified and improved so dramatically that anatomic pictures could be created while emission information provides physiologic detail. This would all be accomplished in one 1-hour scan.
It is clear that PET scanning will have some role in staging lung cancer. At distant sites, false-positive PET findings are less common than in the mediastinum, resulting in a positive predictive value of 93% (14 of 15 patients) in this study. PET is also more sensitive for distant metastasis than conventional staging, demonstrating unsuspected distant disease in 14% of our patients. This may be reason enough to obtain PET on all patients with non-small cell lung cancer.
We have shown that false-positive results do occur in the mediastinum and have identified factors that contribute to this. We believe the trend of some practitioners to use PET scanning to bypass surgical staging en route to the oncologist is wrong. With the current technology, no patient should ever be denied treatment with curative intent or should definitive plans be made based on a positive PET and other imaging studies only. Because of a positive predictive value of only 75%, we believe a positive PET should be confirmed by mediastinoscopy and biopsy.
PET imaging may have greater usefulness in its negative predictive value. In our series, this was greater than 95% and this amount will likely increase further as scanning resolution improves. PET appears to miss only the most limited microscopic spread. This must also occur with currently applied, widely accepted, invasive staging algorithms contributing to the relatively poor survival rate for the earliest stage lung cancers. In the face of a PET scan without evidence of mediastinal or distant disease, we proceed to a very limited thoracotomy and extensive mediastinal dissection with frozen sections. If there is no tumor identified, we undertake resection in a standard fashion. Multicenter trials, such as the ACOSOG Z0050 trial, should help define this modality and resolve some of the issues regarding the variability in imaging devices. When this work and cost analysis has been completed, integrating PET into a definitive algorithm for the diagnosis and staging of non-small cell lung cancer may be possible.
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