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Ann Thorac Surg 1998;66:886-893
© 1998 The Society of Thoracic Surgeons
a Department of Surgery, Department of Radiology, University Hospital, Zürich, Switzerland
b Division of Nuclear Medicine, Department of Radiology, University Hospital, Zürich, Switzerland
Address reprint requests to Dr Weder, Department of Surgery, University Hospital, Rämistr 100, CH-8091 Zürich, Switzerland
Presented at the Thirty-fourth Annual Meeting of The Society of Thoracic Surgeons, New Orleans, LA, Jan 26–28, 1998.
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Abstract |
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Methods. One hundred patients underwent clinical evaluation, chest and upper abdominal computed tomography scan, mediastinoscopy (lymph nodes greater than 1 cm on computed tomography), and routine laboratory tests. In 94 patients with stage IIIa or less and 6 with suspected N3 a whole-body FDG PET was performed. If clinical signs of ETMs were present additional diagnostic methods were applied. All findings in the FDG PET were confirmed histologically or radiologically.
Results. Unexpected ETMs were detected in 13 (14%) of 94 patients (stage IIIa or less) at 14 sites. In addition 6 of 94 patients were restaged up to N3 after PET. The suspected N3 disease (stage IIIb) on computed tomography was confirmed by PET in all 6 patients. There was no false positive finding of ETM. Weight loss was correlated with the occurrence of ETM: more than 5 kg, 5 of 13 patients (38%); more than 10 kg, 4 of 6 patients (67%). Pathologic laboratory findings were not predictive for ETM.
Conclusions. Whole-body FDG PET improves detection of ETMs in patients with non–small cell lung cancer otherwise elegible for operation. In 14% of patients (stage IIIa or less), ETMs were detected, and in total, 20% of the patients were understaged.
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Introduction |
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Current modalities used in preoperative staging of NSCLC include noninvasive imaging techniques, such as chest roentgenography, computed tomography (CT), and if clinically indicated, magnetic resonance imaging (MRI), bone scintigraphy, and ultrasonography, as well as bronchoscopy and mediastinoscopy.
Positron emission tomography (PET) is a well-established imaging technique, which does not depict the anatomic morphology as well as CT and MRI, but detects local differences in tissue metabolism. This principle is used to examine tissue types with high metabolism, eg, brain, heart, and malignant tumors.
Warburg [1] described in 1930 the high glucose metabolism of malignant tumors. With the radioactive labeled glucose analogue 2-[18F]fluoro-2-deoxy-D-glucose (FDG) it is possible to visualize glucose metabolism in vivo. Therefore, FDG PET can be used effectively for differentiation of malignant and nonmalignant tissue. Especially in lung cancer, excellent FDG uptake has been described previously [2, 3].
In our previous study N staging in NSCLC with FDG PET proved to be highly accurate in 96% of cases with a sensivity of 89% and a specifity of 99% [4]. The positive predictive value was 96%, and the negative predictive value was 97%. We reviewed the data and expanded our prospective study to determine the value of FDG PET in preoperative M staging in NSCLC. Furthermore, we evaluated whether a positive correlation between patient data (history, physical examination, tumor characteristics, histology, and N staging) and metastatic disease could be found to facilitate selection of candidates for operation by FDG PET.
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Material and methods |
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In 2 patients definitive histologic diagnosis revealed small cell lung cancer, and 5 patients were excluded because of incomplete data. Preoperative staging included history, physical examination, and blood tests as well as chest x-ray films in two planes and CT scan of the thorax and upper abdomen. Clinical signs for metastases were further investigated with bone scintigraphy, MRI of the brain, or other diagnostic modalities. Enlarged mediastinal lymph nodes (>1 cm) on CT scan were further evaluated by mediastinoscopy. Therefore, data from 100 patients were used for analysis. Ninety-four patients were in stage IIIa or less and 6 were in suspected stage IIIb before the whole-body FDG PET. These included 80 men aged 39 to 80 years (mean, 61 years) and 20 women aged 41 to 79 years (mean, 58 years).
Positron emission tomography imaging
Whole-body FDG PET scanning was performed with a commercially available instrument (Advance; GE Medical Systems, Milwaukee, WI) with the whole-body mode implemented as standard software. The evaluation extended from head to pelvis. Emission and transmission scans were obtained with an acquisition time of 6 minutes per field of view. The total examination time per patient was about 1 hour. To suppress myocardial glucose utilization, patients were asked to fast for at least 4 hours before undergoing whole-body FDG PET.
The glucose analogue FDG initially was produced at an outlying facility and later in our own radiopharmaceutical laboratory by using techniques described before [5]. Transmission scanning began immediately after administration of 300 to 400 MBq of FDG. Emission scanning followed at 40 minutes after administration of FDG. The acquired data were reconstructed by using standard back-projection techniques in axial sections and then were reformatted into coronal and sagittal views. The scans were documented using a color laser printer with a digital interface (Agfa Multimedia 315; A & S Kopiersysteme, Münster, Germany). Because the primary substrate for brain metabolism is glucose, which supplies more than 95% of brain requirements, we used FDG uptake in the brain as the "reference" uptake value [6]. A lesion was defined as a focus of increased FDG uptake greater than the intensity of the surrounding activity, excluding the renal pelvis, urinary bladder, and myocardium, if present. A lesion with intense FDG uptake comparable to the physiologically high FDG uptake in the brain and additionally demonstrating nodular appearance was defined as malignant. Each PET finding fulfilling the previously mentioned properties was confirmed as malignant either histologically, by another imaging method (ultrasonography, bone scan, CT, or MRI), or by follow-up.
The PET scans were interpreted independently and prospectively by an experienced nuclear physician without knowledge of any histopathologic or radiologic data. For all patients exact histopathologic diagnosis was assessed.
Correlation of positron emission tomography with clinical findings and laboratory data
Case histories of all patients were reviewed for indicators of metastases (weight loss, pain, enlarged lymph nodes, or neurologic deficiencies). Radiologic data (preoperative chest roentgenogram and CT scan of the chest and upper abdomen) were examined for bone, liver, and pararenal metastases. In addition all pathologic laboratory parameters were registered.
The staging was done according to the American Thoracic Society TMN system [7] and the staging classifications of the American Joint Committee [8].
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Extrathoracic metastases
Unexpected ETM were detected at 14 sites in 13 (14%) of the patients, who were stage IIIa or less before PET (Figs 1–4). In all 6 patients with suspected N3 (stage IIIb) by conventional staging, metastatic disease was confirmed by PET. Thus, with respect to the entire study population, in 19 patients ETMs were suspected with the whole-body PET in 24 locations (13 bone, 3 liver, 4 adrenal gland, 3 supraclavicular lymph nodes, and 1 central nervous system).
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No correlation of age with the occurrence of ETM was found (with ETM, 58 years; range, 39 to 79 years; no ETM, 62 years; range, 41 to 80 years).
Correlation of positron emission tomography with histologic findings and n and m staging
The correlation of histologic type and metastatic disease demonstrated that patients with primary adenocarcinoma of the lung had the highest frequency of ETMs (Table 2).
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Of the 69 patients conventionally staged as N0/N1, 6 (9%) had a positive ETM finding in PET. Seven (28%) of the 25 patients with N2 stage and 6 (100%) of the 6 with stage N3 were positive for ETMs.
Of importance is the finding that 13 (14%) patients of the 94 with stage IIIa or less (diagnosed according to the described workup) had unexpected ETMs detected by PET. In addition in these 94 patients, previously unknown N3 disease was detected in 6 patients (6.4%). All of them had mediastinal lymph nodes less than 1 cm in the chest CT scan.
In conclusion, of 94 patients who qualified for radical surgical treatment (stage IIIa or less) with the applied preoperative staging methods, on the basis of the new findings in whole-body PET imaging 19 (20%) patients were upstaged to stage IIIb or IV (accordingly N3 Mx or Nx M1) (Table 3).
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Analysis of pathologic laboratory findings were not predictive for ETM (hemoglobin, hematocrit, glutamic-oxaloacetic transaminase, glutamic-pyruvate transaminase, 
-glutamyl transferase, alkaline phosphatase, C-reactive protein). Forty-four (54%) patients with M0 and 12 (63%) of those with M1 showed pathologic laboratory findings. Thirty-two (73%) of those with M0 had an elevated C-reactive protein level, as did 9 (75%) with M1. Hemoglobin and hematocrit were reduced in 22 (50%) of the M0 patients, whereas they were reduced in 9 (75%) with M1. Elevated liver enzymes were found in 6 (14%) patients without metastatic disease, but only in 1 (8%) who was staged M1. The frequency of an increased alkaline phosphatase level was similar in both groups (7 [16%] in M0 and 2 [17%] in M1) (Table 4).
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Comment |
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In this previously published study a high accuracy in detecting malignant lesions in the mediastinum could be achieved. This might be related to our highly qualified team of nuclear physicians and a low rate of inflammatory disease in our study population. However, mediastinal staging by mediastinoscopy is still the method of choice with the highest accuracy. In addition it provides histologic confirmation of lymph node metastases and allows differentiation from nodal enlargement caused by reactive inflammatory hyperplasia (eg, poststenotic pneumonia) and other nonmalignant disease (eg, sarcoidosis, histiocytosis). Moreover, it is difficult to distinguish hilar (N1) from mediastinal (N2) disease at the tracheobronchial angle by PET. However, the continuous evaluation of the data made clear that the role of FDG PET in detecting ETMs is at least equally important. Of the 94 patients (stage IIIa or less) with NSCLC enrolled in this study, 13 patients (14%) demonstrated metastatic findings in the whole-body FDG PET. This is in accordance with the study of Valk and associates [9], which described a detection of previously unsuspected distant metastasis in 11 (11%) of 99 patients with NSCLC.
In 15 patients ETMs were confirmed histologically or radiologically in at least one location. In 4 patients positive findings by PET were not confirmed at the time of diagnosis. But in 2 of these patients ETMs became clinically manifest during follow-up. These results indicate that whole-body FDG PET is a highly sensitive method for detection of unknown ETMs in NSCLC. Similar to previous studies [10, 11], 6 patients without enlarged mediastinal lymph nodes were upstaged to N3 after whole-body PET and confirmed histologically.
Conventional imaging methods for tumor staging include CT scan and MRI, ultrasonography, and bone scintigraphy. Ultrasonography, MRI, and CT are applied for the examination of a selected anatomic region. Bone scan is a sensitive but rather unspecific method and furthermore is limited to the specific organ system. In contrast, whole-body PET imaging with FDG allows scanning the entire body including all organ systems.
Although the incidence of metastatic disease in NSCLC is high, routine staging of all patients with skeletal scintigraphy and CT scan of the head and the abdomen is not routinely applied, because the likelihood of a true positive finding in bone or CT scan in an asymptomatic patient is small [10]. Using skeletal scintigraphy as a routine diagnostic method, only 14% of the positive solitary findings in patients with cancer were caused by a metastasis of the known tumor [12]. Also, the metaanalysis by Silvestri and coworkers [13] demonstrated that the negative predictive value for detecting metastatic disease in the CT scan in patients with NSCLC is not higher than the clinical evaluation.
Based on this experience, in current clinical practice preoperative staging in bronchogenic carcinoma is symptom based. However, in our study skeletal metastases were detected with the whole-body FDG PET in 13 patients. In 10 of these patients skeletal scintigraphy was not performed previously because of lack of clinical symptoms.
In contrast to conventional imaging modalities the rate of positive findings for M1 in our series is surprisingly high. Moreover, the patients underwent FDG PET without clearly defined clinical symptoms of metastases.
Whole-body FDG PET allows screening of the entire body for metastatic disease with a single examination and can detect even small, asymptomatic metastases (4 to 5 mm). In 3 of our patients a metastasis in cervical or supraclavicular lymph nodes was detected by PET imaging, of whom 2 had a completely inconspicuous physical examination even with the knowledge of the PET finding. This illustrates the high resolution power of a modern PET scanner of about 4 to 5 mm.
Also in the ability to distinguish solitary benign pulmonary nodules from malignant tumors FDG PET has proved to be highly sensitive (93%) and specific (88%) [14, 15]. However, increased FDG uptake is of course not specific for malignant tissue and is seen in infectious and inflammatory processes [15, 16]. In our series only patients with confirmed diagnosis of NSCLC were enrolled in the study. All additional infectious sites detected in our series could be differentiated from malignant lesions. Previous studies comparing the specifity of FDG PET and CT scan to detect metastases in the liver and the adrenal gland demonstrated that the FDG PET has a higher sensitivity and specifity than CT [9, 17].
Our results indicate that patients with M1 disease can be diagnosed effectively with the whole-body FDG PET. Therefore, a negative PET finding for M and N3 stage indicates a high positive predictive value for a curable resection.
This could lead to the conclusion that PET would be the ideal screening method to detect metastatic disease in NSCLC or other thoracic tumors [18]; however, in current clinical practice the availability and cost of the equipment limits the application of this method. The use of PET for the evaluation of all patients with NSCLC is currently not feasible for most centers.
Based on the experience in our studies, we currently use FDG PET as an additional tool to exclude patients with M1 disease in patients with borderline indications from the physiologic standpoint (limited pulmonary function, coronary artery disease), and in patients with suspected advanced disease such as severe weight loss, locally advanced disease, solitary brain metastases, and local recurrence that might qualify for reoperation. The aim is to avoid extensive or futile surgical resections in these high-risk groups. How these guidelines influence the treatment strategy and costs, or whether whole-body PET should be applied as a screening tool for metastases in all lung cancer patients, needs further investigation.
In conclusion, our results indicate that whole-body FDG PET is an excellent method to detect unknown ETMs in NSCLC, as 13 (14%) of 94 patients selected to undergo operation with conventional methods were not eligible for radical surgical treatment after PET imaging because of newly detected stage M1 disease.
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R. M. Pieterman, J. W.G. van Putten, J. J. Meuzelaar, E. L. Mooyaart, W. Vaalburg, G. H. Koeter, V. Fidler, J. Pruim, and H. J.M. Groen Preoperative Staging of Non-Small-Cell Lung Cancer with Positron-Emission Tomography N. Engl. J. Med., July 27, 2000; 343(4): 254 - 261. [Abstract] [Full Text] [PDF]
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