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Ann Thorac Surg 2003;75:231-236
© 2003 The Society of Thoracic Surgeons
a Department of Thoracic and Cardiovascular Surgery, Homburg/Saar, Germany
b Department of Nuclear Medicine, Homburg/Saar, Germany
c Department of Internal Medicine V (Pneumology), Saarland University Medical School, Homburg/Saar, Germany
* Address reprint requests to Dr Graeter, Department of Thoracic and Cardiovascular Surgery, Saarland University Medical School, 66421 Homburg, Germany.
e-mail: dl5ban{at}t-online.de
Presented at the Thirty-eighth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2002.
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Abstract |
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METHODS: From March 1997 to June 2001, 102 patients (86 male,16 female, age 62 ± 9 years) underwent both PET and mediastinoscopy for radiologically suspected mediastinal lymph node disease in bronchogenic carcinoma. Total body emission scans were acquired 90 to 150 minutes after injection of 230 MBq of F-18 fluorodeoxyglucose. Mediastinoscopic evaluation of lymph node stations was performed according to the method of Mountain and Dresler (1R,1L, 2L, 2R, 4L, 4R,7). Patients were eligible if surgical staging was performed within 6 weeks after the PET scan.
RESULTS: Of the 102 patients, benign lesions were diagnosed in 15. In 87 patients malignant disease was proven by histology, and bronchogenic carcinoma was found in 82. Of 469 nodal stations analyzed, malignancy was documented by histology in 84. In PET analysis 79 true-positive and 304 true-negative samples were found. Five lymph node stations were false negative, and 81 samples were false positive. False-positive findings in PET frequently were seen in inflammatory lung disease. The sensitivity of PET was 94.1%, specificity was 79% with a diagnostic accuracy of 81.6%. The positive predictive value of PET was 49.3%, and the negative predictive value was 98.4%.
CONCLUSIONS: In patients with positive PET scan results histologic verification appears necessary for exact lymph node staging. In view of the negative predictive value mediastinoscopy can be omitted in patients with bronchogenic carcinoma whose PET scan results were negative.
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Introduction |
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By contrast, positron emission tomography (PET) with the metabolic tracer F-18-fluorodeoxyglucose allows for functional characterization of tissues. Because malignant tissue, particularly non–small cell lung cancer, is characterized by increased glucose metabolism, PET permits the visualization not only of the primary tumor but also of metastatic spread [3]. F-18-fluorodeoxyglucose PET has been shown to be of value in the evaluation of primary lesions in lung cancer, detection of extrathoracic metastasis, or tumor recurrence [1]. Measuring the amount of accumulated radioactivity in suspected lesions using standardized uptake values (SUV) has helped improve the F-18-fluorodeoxyglucose PET results further, particularly in diagnosing tumor recurrence [4, 5]. Only limited data are available on the use of F-18-fluorodeoxyglucose PET in mediastinal lymph node staging [6–8].
The purpose of our study was to evaluate whether PET can predict malignant involvement of mediastinal lymph nodes in patients with suspected bronchogenic carcinoma. In a retrospective analysis, the results of PET were compared with those of surgical staging.
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Material and methods |
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After overnight fasting a blood glucose concentration of less than 160 mg/dL was verified. Imaging from neck to hips using an ECAT ART scanner (CTI, Knoxville, TN) was performed 90 to 150 minutes after intravenous injection of 220 ± 20 MBq of F-18-fluorodeoxyglucose. Additional transmission scans for correction of attenuation were acquired using rotating 68Ge/68Ga rod sources (before February 1998) or 137Cs point sources (since February 1998) [11]. Images were iteratively reconstructed using the attenuation-weighted ordered subset expectation maximization (OSEM) technique [12].
Images were visually interpreted using a display of three orthogonal sections and maximum intensity projections. Two experienced nuclear medicine physicians, who were masked to the results of computed tomography, read the PET images. Lesions were regarded as malignant if their intensity was higher than that of the mediastinal blood pool. Standardized uptake values were calculated as the ratio of the regional radioactivity concentration divided by the injected amount of radioactivity normalized to body weight [13]. Peak SUV in all lymph nodes was measured with a region-of-interest technique. If a lymph node was visible on the PET image by increased activity, the region was positioned around that particular node and the peak value measured. In patients with no apparent localized increase of radioactivity, the region of interest was positioned in the typical area for the lymph node station. The accumulation of F-18-fluorodeoxyglucose in the mediastinal lymph nodes was scored visually as a semiquantitative measurement. For quantitative assessment, the maximum SUV in each lymph node station was measured. For technical reasons, SUV data were calculated only in the more recent patient cohort.
Mediastinoscopy was performed in all patients in the standard fashion [9] for radiographically enlarged lymph nodes. Lymph node stations biopsied were 1, 2, 4, and 7 according to the classification of Mountain and Dresler [10]. In addition to mediastinoscopy, 38 of these patients subsequently underwent thoracotomy. Mediastinal lymph node histology of stations 1, 2, 4, and 7 obtained at the time of thoracotomy was also used to validate the histologic database obtained by mediastinoscopy. The presence of normal lymph node tissue, inflammation, or metastatic involvement was noted for all lymph nodes sampled.
Statistical analysis
Positive PET findings without histologic proof of malignancy were defined as false positive; negative PET results in the presence of positive histology were regarded as false negative. The diagnostic value of PET scanning was compared to surgical lymph node assessment by calculating sensitivity, specificity, positive predictive value, negative predictive value, and accuracy. Sensitivity was calculated as (true positive)/(true positive + false negative), specificity as (true negative)/(true negative + false positive), positive predictive value as (true positive)/(true positive + false positive), negative predictive value as (true negative)/(true negative + false negative), and accuracy as (true positive + true negative)/total.
Values are reported as mean ± standard deviation. Differences in SUV between the groups of patients with and without metastases were analyzed using Student’s t test.
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Results |
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A total of 469 nodal stations were analyzed by PET and histology. Of these, 406 specimens were obtained at the time of mediastinoscopy. In addition, 63 specimens from lymph node dissection during thoracotomy were used for correlation with PET if no corresponding biopsy during mediastinoscopy was available.
The comparison of PET and histology resulted in 79 true-positive and 5 false-negative PET findings. The PET examination was true negative in 304 lymph nodes and false positive in 81 samples (Table 1). This resulted in a sensitivity of 94.1%, a specificity of 79%, an accuracy of 81.6%, a positive predictive value of 49.3%, and a negative predictive value of 98.4%. Standardized uptake values were significantly higher in lymph nodes with metastasis (7.41 ± 4.19; range 1.57 to 18.9; n = 32) compared with normal lymph nodes (2.38 ± 1.96; range 0.65 to 10.89; n = 69) (p < 0.05). Inflammatory lymph nodes were occasionally difficult to interpret, with SUV values of 2.84 ± 1.9 (range 0.95 to 9.2; n = 66). Analyzing only those lymph nodes obtained by mediastinoscopy and excluding those obtained by thoracotomy, PET resulted in a sensitivity of 92.9%, specificity of 77.4%, accuracy of 80.1%, positive predictive value of 46.1%, and negative predictive value of 98.1%. There were four lymph node biopsies that were true positive by PET scan but histologically false negative by mediastinoscopy, as shown by the histology obtained at thoracotomy.
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For the main group of patients with bronchogenic carcinoma (380 lymph nodes) the diagnostic test values were slightly better (sensitivity, 93.8%; specificity, 84.3%; accuracy, 86.3%; positive predictive value, 61.4%; negative predictive value, 98.1%) (Table 2).
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Comment |
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TopAbstractIntroductionMaterial and methodsResultsCommentDiscussionReferences |
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Mediastinoscopy remains the gold standard for assessing mediastinal lymph nodes. First described by Harkens and associates [9], this invasive procedure has a sensitivity of about 80% and a specificity of 100% [25, 26]. Because mediastinoscopy is associated with a low but present risk of serious complications in 0.5% of the patients, including hemorrhage, mediastinitis, pneumothorax, or vocal cord paralysis [14, 15], less invasive staging procedures have been proposed. Mediastinal lymph node staging by computed tomography or magnetic resonance imaging is standard in clinical practice today. It is generally accepted that lymph nodes of more than 1 cm are pathologically enlarged. For lymph nodes of this size, several groups have reported a sensitivity in the range of 60% to 70% and a specificity of 60% to 80% using computed tomography [2, 6, 14, 20]. Even the presence of larger lymph nodes, however, can be misleading. More than 35% of such lymph nodes have been found to be negative for tumor metastasis, especially in patients with postobstructive pneumonia [2]. Magnetic resonance imaging has been used more recently but currently does not offer substantial advantages over computed tomography [22]. For both procedures, large series have demonstrated striking inconsistencies between clinical and pathologic staging for bronchogenic carcinoma [16, 17].
F-18-fluorodeoxyglucose PET has been utilized increasingly in the diagnosis of lung cancer. It allows for noninvasive evaluation of lung lesions, with a sensitivity of 93% to 97% and specificity of 70% to 87% [1, 18, 28, 29]. In direct comparison with computed tomography, PET has been superior in detecting early metastatic disease in normal-sized lymph nodes because of their increased metabolism [19]. The limited spatial resolution of PET, however, can be a disadvantage of the technique. Especially in the presence of central lung tumors, the differentiation between tumor or mediastinal lymph node disease can be difficult.
Previous studies have found PET to have a sensitivity of 87% to 90% and a specificity around 85% in detecting mediastinal lymph node metastasis [6, 14]. Most published reports had fewer than 50 cases [7, 8]. Results of those studies suggest a high sensitivity and specificity in detecting malignant disease, but the role of PET in staging mediastinal disease in patients with bronchogenic carcinoma is not well defined. When our data were compared with those published for mediastinal lymh node staging by PET, the results were similar [14, 16, 21].
Measuring SUVs has helped to improve the PET results in diagnosing tumor recurrence [4, 5]. A SUV cut-off value of 2.5 for optimal discrimination between recurrence or freedom from disease has been reported by Duhaylongsod and associates [5] resulting in a sensitivity of 94% and a specificity of 93% [27]. In our series, lymph nodes with metastastatic involvement had a significantly higher SUV. Nevertheless, because of the range of SUV in false-positive lymph nodes (0.95 to 9.2) this variable was not able to accurately predict malignancy in our series.
The sensitivity or specificity can be misleading if the number of predictably negative samples is inadequate. To correlate histology and PET data, all accessible lymph node stations must undergo biopsy. In our study, all patients with suspected mediastinal lymph node disease, identified by computed tomography, had a PET scan and mediastinoscopy for staging purposes. This might represent a bias, as most of these patients had diseased lymph nodes; however, the sample size of 4.6 lymph node stations per patient, including 385 lymph nodes free of malignancy, seems sufficient to eliminate this problem.
In 29 patients, the lambda sign (bilateral and paratracheal F-18-fluorodeoxyglucose accumulation) as an indicator of inflammatory changes was found by PET [23]. This pattern was especially prominent in coal miners with silicosis, sarcoidosis, or tuberculosis. In 13 of these patients F-18-fluorodeoxyglucose PET gave false-positive N3 stages because of intense F-18-fluorodeoxyglucose uptake. Those nodes were less than stage N2 by mediastinoscopy. In these patients specificity was extremely poor, a well-known problem [24]. Because of these patients with inflammatory changes, the positive predictive value of PET in our series was low, a problem encountered by others as well [20]. Our data indicate a definite need to biopsy all questionable lymph nodes. Conversely, the highly favorable negative predictive value of PET scans in lung cancer probably allows clinicians to proceed with other therapeutic options in patients with negative mediastinal lymph nodes without invasive staging.
The excellent negative predictive value of F-18-fluorodeoxyglucose PET for the evaluation of mediastinal lymph nodes permits omission of mediastinoscopy in PET-negative patients with bronchogenic carcinoma. In patients with positive PET scans, histologic verification appears necessary for exact lymph node staging [30].
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Discussion |
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Lung cancer continues to be the main cause of cancer deaths in the United States and worldwide. In the United States alone, 150,000 to 160,000 people will die this year from lung cancer. This exceeds the total number from breast cancer, colon cancer, and prostate cancer added together. Clearly, thoracic surgeons need to address this significant public health concern.
One pathway to increasing survival is by improving staging so that each patient can have the appropriate operation. For years, staging has been limited to history and physical examination, chest X-ray, blood test, and computed tomography of the chest. Recently, positron emission tomography, or PET scanning, has been applied to lung cancer staging. Theoretically, PET scanning has the advantage of measuring metabolism, usually of glucose, of the malignancy rather than just morphologic appearance, as in computed tomographic scan. The disadvantage, of course, is that it is very expensive. Machine costs are in the neighborhood of $20 million, and patients are billed almost $3,000 for each scan. Therefore, it is imperative that we use this new and expensive modality appropriately. For lung cancer, the opportunities for use include determining whether a nodule is malignant or benign. PET scanning has been used to determine the T stage of lung cancer, the N stage, and to look for metastatic disease, or the M stage.
This study tries to assess its use in N staging and looks at a specific patient population, that is, patients with a radiographic suspicion of N2 or N3 disease. It compares PET to mediastinoscopy and concludes that if the PET result is negative, then there is little or no chance of any positive mediastinal lymph nodes. If the PET result is positive, however, there could be a false-positive result, which requires histologic confirmation.
I am concerned that what you compared the PET scan with is not very accurate. You did a thoracotomy in only 38% of your patients, and you did not specify whether you did a complete lymphadenectomy, a lymph node sampling, or just re-examination of the areas that were not biopsied at mediastinoscopy. When you did a mediastinoscopy, did you remove all of the lymph nodes you could find or did you just take samples from each lymph node station? Similarly, at thoracotomy, did you remove all the lymph nodes or just sample some areas or just sample the areas that were not sampled at mediastinoscopy? I would like you also to clarify whether we should use a PET scan to stage patients with clinical N0 or N1 cancers. Is it worth the added expense in every patient with a suspected lung cancer?
You used nodal stations as the denominator in your analysis. I think it would be better to use patients as the denominator, because this way we can understand how the PET scan affects patients. I wonder whether you could tell us the percentage of patients in which the PET scan was correct rather than the percentage of lymph node stations in which the PET scan was correct.
A PET scan is less accurate when the primary cancer is centrally located because it can overlap the mediastinal nodes and obscure the signal from the mediastinum. In what percentage of your patients was the cancer centrally versus peripherally located, and was there a difference in accuracy between these two locations?
DR GRAETER: Starting with the last question first, whenever we have a central bronchogenic carcinoma, a PET scan might have difficulty assessing whether we have mediastinal lymph node disease, as the anatomic resolution sometimes is not good enough. I would say in about 30 of our patients we had centrally located tumors.
To the question about what percentage of patients the PET scan was correct, if you look at the 29 patients who had marked inflammatory disease, the PET scan was incorrect in 13 of them in assessing whether they had N2 or N3 disease versus N0 or N1. It incorrectly gave a higher stage to those patients. That is one of the reasons why we advise a histologic verification whenever the PET scan is positive.
The PET scan only costs about $1000 in Germany, so we are a little more liberal in ordering it. Nevertheless, I think that if you have no suspicion whatsoever regarding N1 or N0 disease, I would omit it, but the second you have the suspicion that you have N2 or N3 disease, the PET scan adds very important information. It is our clinical procedure that whenever the PET scan is negative, we do not do a mediastinoscopy.
Finally, regarding the lymphadenectomy, when we did the mediastinoscopy, we sampled every position regardless of whether it was positive in the PET scan. So we had an average of 4.6 lymph node samples per patient. I would have preferred a number above five, but because we had three different surgeons, that was difficult to do. At thoracotomy we sampled all levels of lymph nodes, but we did not use those that could not be assessed by mediastinoscopy for this paper, as we basically wanted to do the mediastinal lymph node staging.
DR ROBERT J. CERFOLIO (Indian Springs, AL): I enjoyed your presentation and your work. You should be congratulated. I have a few questions for you. First of all, false-positive results are a big problem for us in the southeastern United States as well. For you it seemed like it was secondary to silicosis; for us it is histoplasmosis, and I wonder whether you have any experience with histoplasmosis. Can you tell us how you are able to use SUVs to differentiate and distinguish inflammatory disease from cancer?
My second question concerns our PET experience, which we will be presenting later this week at this meeting. We have found that PET scans seem to be slighty less sensitive in certain locations, eg, the no. 7 subcarinal lymph node stations. Moreover, large tumors obscure N1 disease. We have had a significant number of false negatives, and the false negatives, especially the false N2 negatives, are critical and harmful to the patient. We have also seen several false negatives in the 4R and 2R positions as well as in station 7. All of these patients have had microscopic N2 disease. Is your PET less accurate in the subcarinal area?
Third, we have also found, as Dr. Allen alluded, that large tumors can obscure N1 and N2 disease, and I wonder whether you have any comments on computed tomographic PET. We are about to open our new computed tomographic PET center, do you have any words of wisdom about interpreting it and using it versus the conventional dedicated PET? Our hope and impression is that we are going to have better resolution and avoid this obscuring phenomenon. Have you found this to be true and do you have any tricks for us?
My final question is cell type. We, like others, have found that with some slow growing tumors, especially carcinoids or bronchoalveolar or slow growing adenocarcinomas, there are false-negative results not only in the mass but in the nodes as well. Could you comment on that? Thank you and your presentation was great.
DR GRAETER: Starting with the last question first, the bronchoalveolar carcinoma is well known for its problems with PET, and as we had no patients with bronchoalveolar carcinoma in this group, this was not a problem here, but over the past 3 years we had 5 patients with bronchoalveolar carcinoma that were PET negative. So that is a problem, and we do not really have a good solution for that.
With computed tomographic PET, I have no experience. Sorry about that.
Our false-negative results with PET usually occurred in patients where two lymph nodes that were positive but close together and could not be differentiated by PET. Therefore that was no change in the N staging, but when looking at the lymph node samples, it was still incorrect.
There was no location that was preferable; three of those were paratracheal and two were subcarinal. So this is hard to say.
Regarding histoplasmosis, that is no problem in Germany whatsoever, but we live in a coal mining area, and so silicosis is a problem. Tuberculosis and some sarcoidosis cases gave us the same problems, and I do not think you have much choice than to biopsy these patients.
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