Preoperative Staging of Non–Small-Cell Lung Cancer with Positron-Emission Tomography
Remge M. Pieterman, M.D., John W.G. van Putten, M.D., Jacobus J. Meuzelaar, M.D., Eduard L. Mooyaart, M.D., Willem Vaalburg, Ph.D., Gerard H. Koëter, M.D., Vaclav Fidler, Ph.D., Jan Pruim, M.D., and Harry J.M. Groen, M.D.
Background Determining the stage of non–small-cell lungcancer often requires multiple preoperative tests and invasiveprocedures. Whole-body positron-emission tomography (PET) maysimplify and improve the evaluation of patients with this tumor.
Methods We prospectively compared the ability of a standardapproach to staging (computed tomography [CT], ultrasonography,bone scanning, and, when indicated, needle biopsies) and oneinvolving PET to detect metastases in mediastinal lymph nodesand at distant sites in 102 patients with resectable non–small-celllung cancer. The presence of mediastinal metastatic diseasewas confirmed histopathologically. Distant metastases that weredetected by PET were further evaluated by standard imaging testsand biopsies. Patients were followed postoperatively for sixmonths by standard methods to detect occult metastases. Logistic-regressionanalysis was used to evaluate the ability of PET and CT to identifymalignant mediastinal lymph nodes.
Results The sensitivity and specificity of PET for the detectionof mediastinal metastases were 91 percent (95 percent confidenceinterval, 81 to 100 percent) and 86 percent (95 percent confidenceinterval, 78 to 94 percent), respectively. The correspondingvalues for CT were 75 percent (95 percent confidence interval,60 to 90 percent) and 66 percent (95 percent confidence interval,55 to 77 percent). When the results of PET and CT were adjustedfor each other, only PET results were positively correlatedwith the histopathological findings in mediastinal lymph nodes(P<0.001). PET identified distant metastases that had notbeen found by standard methods in 11 of 102 patients. The sensitivityand specificity of PET for the detection of both mediastinaland distant metastatic disease were 95 percent (95 percent confidenceinterval, 88 to 100 percent) and 83 percent (95 percent confidenceinterval, 74 to 92 percent), respectively. The use of PET forclinical staging resulted in a different stage from the onedetermined by standard methods in 62 patients: the stage waslowered in 20 and raised in 42.
Conclusions PET improves the rate of detection of local anddistant metastases in patients with non–small-cell lungcancer.
The occurrence of distant metastases and metastases to mediastinallymph nodes profoundly affects the prognosis of non–small-celllung cancer, making accurate staging crucial for selecting appropriatetreatment. When used alone, the results of most staging methods,such as computed tomography (CT), ultrasonography, and radionuclidebone scanning, are far from ideal. Whole-body positron-emissiontomography (PET) with 18F-fluorodeoxyglucose (fludeoxyglucoseF 18) as a tracer is a new metabolic imaging technique thatrelies on the fact that there is increased metabolism of glucosein tumor cells.1,2 Pulmonary tumors actively metabolize thetracer, and several studies have shown that the method has about95 percent sensitivity for detecting primary bronchial tumors3,4and mediastinal lymph-node metastases.5,6,7 Within the body,the method has a lower limit of resolution of 1 to 1.2 cm. Thespecificity of this method is not optimal, because the uptakeof 18F-fluorodeoxyglucose is increased by the presence of inflammatoryprocesses in the lungs. Another limitation is that histopathologicalverification of the results of the PET scan is often conductedonly on "hot spots" (areas in which the uptake of 18F-fluorodeoxyglucoseis much greater than the background uptake in all areas butthe heart, brain, and urinary tract) and does not include lymphnodes whose uptake of the radioactive glucose is not increased.The use of PET to identify distant metastases in patients withnon–small-cell lung cancer has been investigated in afew small studies.8,9 Therefore, we prospectively investigatedthe role of PET in evaluating the mediastinum and detectingdistant metastases in such patients.
Methods
Patients
Patients with potentially resectable non–small-cell lungcancer who were being evaluated with standard tests and proceduresin the outpatient department of pulmonary diseases at GroningenUniversity Hospital in Groningen, the Netherlands, were eligiblefor the study. Patients were excluded if they had hyperglycemia(defined as a serum glucose level of more than 180 mg per deciliter[10 mmol per liter]) before the PET study, since in a pilotstudy, such levels seemed to affect the quality of the PET imagesadversely, or had undergone cervical mediastinoscopy or parasternalmediastinotomy. All patients were evaluated by means of a historytaking, physical examination, blood count, measurement of electrolytes,tests of renal and liver function, bronchoscopy, cervical mediastinoscopy,and CT of the chest, including the upper abdomen. In patientswith symptoms or signs suggestive of distant metastases, appropriateadditional imaging tests and biopsies were performed. The combinationof tests and invasive procedures leading to clinical classificationaccording to the tumor–node–metastasis (TNM) stagingsystem of the American Joint Committee on Cancer10 was consideredtraditional staging. Every two months for at least six monthsafter thoracotomy, the patients underwent a physical examinationand chest radiography (as well as additional tests in patientssuspected of having distant metastases).
All patients gave written informed consent. The study was approvedby the medical ethics committee of Groningen University Hospital.
Surgery
Cervical mediastinoscopies, parasternal mediastinotomies, andexplorative thoracotomies were performed by four thoracic surgeons.Cervical mediastinoscopy was considered adequate when it included,at a minimum, biopsy specimens of the paratracheal and tracheobronchiallymph nodes on the right and left sides, and subcarinal lymphnodes. Mediastinal lymph nodes were dissected during thoracotomy,with thorough attention paid to the superior and inferior lymphnodes on the right side or the superior and inferior mediastinaland aortic lymph nodes on the left. Surgeons were strongly encouragedto dissect both normal-appearing lymph nodes and those thatappeared enlarged on CT. Lymph nodes were labeled accordingto the classification of Mountain and Dresler11 and sent forhistopathological examination, which included staining withhematoxylin and eosin.
Whole-Body PET
PET was performed with a scanner (ECAT model 951/31, Siemens/CTI,Knoxville, Tenn.) that had a field of view of 10.8 cm and afull width of 6 mm at half-maximal resolution. Data were reconstructediteratively12 into coronal, sagittal, and transverse sectionsand a three-dimensional rotating projection. 18F-fluorodeoxyglucosewas synthesized according to the method of Hamacher et al.13by a high-performance liquid chromatography controlled-synthesismodule.14 Patients were instructed to fast for six hours beforethe PET study, but they were allowed to drink water and to taketheir usual medications. 18F-fluorodeoxyglucose (370 MBq) wasadministered intravenously.
Before the prospective study, we performed a pilot study inseven patients with non–small-cell lung cancer to determinethe optimal scanning protocol, especially with regard to themediastinum. Static (i.e., isolated rather than dynamic) emissionscans were performed 30, 60, 90, and 120 minutes after the injectionof 18F-fluorodeoxyglucose. Imaging reconstruction was performedafter 2.5, 5, 8, and 10 minutes in each position for both emissionscans (which measure only 18F-fluorodeoxyglucose uptake) andtransmission scans (source, germanium-68). The results of post-emissiontransmission scans were used to correct for attenuation of the18F-fluorodeoxyglucose signal. The emission scans performed90 minutes after the injection of 18F-fluorodeoxyglucose, withreconstructions made after eight minutes in each position, wereconsidered to have provided the best images with respect tothe extent of contrast between hot spots and the backgroundlevel in mediastinal lymph-node levels. Both types of scanswere performed from the level of the first cervical vertebrato the level of the fifth lumbar vertebra. All clinicians involvedin the care of the patients were unaware of the results of PET.
CT of the Chest
CT of the chest and upper abdomen including the adrenal glandswas performed with a 120-KV, 125-mA tomoscan (model SR 7000,Philips Medical Systems, Enthoven, the Netherlands) with a slicethickness of 10 mm and a scanning time of one second per slice.During CT, 200 ml of contrast medium (Omnipaque, iohexol, Nycomed,Amersham, Princeton, N.J.) was administered intravenously ata rate of 1.5 ml per second. In 13 patients no contrast mediumwas used.
Assessment of Metastases
Hot Spots Inside the Mediastinum
A positive PET scan was one that had at least one hot spot.All imaging studies were analyzed by two independent observerswho were not aware of the patients' clinical data. If they couldnot reach a consensus, the opinion of a third observer was sought.
The gold standard for the diagnosis of mediastinal metastasesis surgical exploration of the mediastinum and histopathologicalexamination of mediastinal lymph-node compartments (stations).Because the degree of anatomical resolution of mediastinal lymphnodes with PET is limited, we broadened the lymph-node categoriesin the classification of Mountain and Dresler11 in order tocompare the results of CT, PET, and histopathological analysis(Figure 1). For the interpretation of the CT findings, the mediastinallymph nodes were divided in two categories: those with a diameterof less than 1 cm in the shortest axis were considered normalin size and those with a diameter of 1 cm or more were consideredto be enlarged.
Figure 1. Mediastinal Lymph-Node Levels Used to Compare the Results of PET, CT, and Histopathological Analysis.
Level 1 included the superior mediastinum; level 2, the right side of the paratracheal and tracheobronchial areas; level 3, the left side of the paratracheal and tracheobronchial areas; level 4, the subaortic and paraaortic areas; level 5, the subcarinal area; level 6, the right side of the paraesophageal area and the pulmonary ligament; and level 7, the left side of the paraesophageal area and the pulmonary ligament.
Hot Spots Outside the Mediastinum
Hot spots outside the mediastinum were described according totheir anatomical locations and were related to data obtainedby traditional staging methods, including the data obtainedduring the six-month follow-up in the case of lesions that hadnot been detected previously by traditional staging methods.If there was a clinical suspicion of distant metastases duringthe follow-up period, biopsies or imaging tests were performed.The results of PET were considered to be falsely positive ifno metastases became apparent at a hot spot during follow-up.
Statistical Analysis
The study was designed to detect with a power of 0.85 and atwo-sided level of 0.05 a difference of 35 percent betweenthe sensitivity of PET and that of CT (whose sensitivity wasassumed to be 60 percent). In order to identify such a difference,the study required a minimum of 30 patients with mediastinalmetastases. Assuming that mediastinal metastases are presentin about 30 percent of patients with resectable non–small-celllung cancer, a minimum of 100 patients had to be enrolled.
We determined the sensitivity, specificity, and diagnostic accuracyof each imaging method and of the combination of PET and CT.
The degree of agreement between observers was quantified withthe kappa statistic. The two-sided sign test was used to comparethe differences between the TNM class identified by PET andthat identified by traditional methods of staging. Logistic-regressionanalysis was performed to evaluate the relative ability of PETand CT to identify metastatic cancer in mediastinal lymph nodes.A P value of less than 0.05 was considered to indicate statisticalsignificance. Statistical analysis was carried out with SPSSsoftware.
Results
Patients
Between September 1996 and December 1998, we evaluated 110 consecutivepatients. Non–small-cell lung cancer was diagnosed in102 patients: 58 had squamous-cell carcinoma, 28 had adenocarcinoma,13 had large-cell carcinoma, 2 had adenosquamous carcinoma,and 1 had a neuroendocrine tumor. We excluded two patients withsolitary metastases from melanoma and breast cancer, respectively;one with tuberculosis; one with sarcoidosis; and four in whommediastinal dissection was inadequate. The characteristics ofthe 102 patients who were evaluated are shown in Table 1.
Table 1. Characteristics of the 102 Patients with Resectable Non–Small-Cell Lung Cancer Who Could Be Evaluated.
Surgery
All patients underwent a cervical mediastinoscopy that exploredlymph-node levels 1, 2, 3, and 5 (Figure 1). In patients whounderwent a right-sided thoracotomy, mediastinal lymph nodesat levels 1, 2, 5, and 6 were dissected, and in those who underwenta left-sided thoracotomy, lymph nodes at levels 1, 3, 4, 5,and 7 were dissected. Six patients with solitary parenchymalmetastasis were considered to have resectable tumors. In threepatients with solitary brain metastases, curative lobectomywas performed after the removal of the brain lesion. In twopatients with two primary tumors in two lobes of the same lung,a curative pneumonectomy was performed. One patient with a non–small-celllung cancer of stage T2N2M1 had a double tumor and microscopictumor invasion of the subcarinal lymph nodes, all three of whichwere completely resected. In the group as a whole, 97 percentof the mediastinal lymph-node levels that could be reached weredissected (Table 1). At each level a median of 7 separate lymphnodes (range, 1 to 18) were dissected. Histopathological analysisshowed that a total of 37 mediastinal lymph-node levels containedmetastatic tumor.
Detection of Primary Tumor with PET
Every primary tumor was detected as an intense hot spot on PETscans (Figure 2). In one patient with two primary tumors, thesquamous-cell carcinoma appeared as a hot spot on PET, but surprisingly,the adenocarcinoma was not detected, although it was clearlyvisualized on CT.
Figure 2. CT and PET Findings in a Centrally Located Adenocarcinoma of the Left Lung and a Small Pretracheal Lymph Node in a Patient with Non–Small-Cell Lung Cancer.
On the axial CT scan of the chest (Panel A), the primary tumor (white arrow) is adjacent to the pulmonary artery; the lymph node is indicated by the dotted arrow. On the axial PET scan (Panel B) and coronal PET scan (Panel C), the primary tumor (white arrows) and lymph node (dotted arrows) show increased uptake of 18F-fluorodeoxyglucose. Physiologic uptake of 18F-fluorodeoxyglucose by the myocardium is also apparent.
Detection of Mediastinal Metastases with PET
Mediastinal lymph-node metastases were correctly detected byPET in 29 of 32 patients with positive results on histopathologicalanalysis (Table 2) and in 28 of the 37 mediastinal lymph-nodelevels that were positive for metastatic tumor on histopathologicalanalysis. PET correctly identified 60 of 70 patients who didnot have mediastinal lymph-node metastases on histopathologicalanalysis (Table 2). Distinguishing between intrapulmonary involvementand mediastinal lymph-node involvement is an important partof the process of deciding whether thoracotomy should be performed.The sensitivity and specificity of PET for detecting mediastinalmetastases were 91 percent (95 percent confidence interval,81 to 100 percent) and 86 percent (95 percent confidence interval,78 to 94 percent), respectively (Table 3). The overall negativepredictive value of the method was 95 percent (95 percent confidenceinterval, 90 to 100 percent), and the positive predictive valuewas 74 percent (95 percent confidence interval, 60 to 88 percent).Because of the presence of reactive hyperplasia in the mediastinallymph nodes of seven patients and of silicoanthracosis in three,PET produced a false positive result. False negative resultswere due to microscopic-tumor residue in two patients and tothe inability of the method to distinguish between paramediastinalprimary tumor and mediastinal lymph nodes in one patient. Thedegree of interobserver agreement (kappa value) in detectingmediastinal hot spots was 0.87 (95 percent confidence interval,0.64 to 1.0).
Table 3. Sensitivity, Specificity, and Accuracy of CT, PET, and Both CT and PET as Compared with Histopathological Analysis for the Mediastinal Evaluation of Patients with Resectable Non–Small-Cell Lung Cancer.
Detection of Distant Metastases with PET
In 20 of 102 patients, 29 hot spots were detected outside themediastinum (Figure 3). Three malignant satellite nodules inthe resected lobe were confirmed to be present during histologicexamination, and 17 of the 29 hot spots were diagnosed as metastasesduring the follow-up period — 3 by means of biopsy, 5on the basis of the detection of new, growing lesions on ultrasonography,5 by means of CT, and 4 on the basis of a finding of lytic lesionson radiographic imaging. Nine hot spots — four in thecolon, two in the lung, and one each in the liver, adrenal glands,and rib — were considered to be false positive results,since no metastases were identified in these areas during thefollow-up period.
Figure 3. Preoperative Axial CT and PET Findings in a Patient with Non–Small-Cell Lung Cancer.
The preoperative CT scan revealed no metastases in the liver (Panel A), whereas the PET scan showed three hot spots in the liver (Panel B). Liver metastases were confirmed during follow-up. In Panel B, the asterisk indicates diffuse uptake of 18F-fluorodeoxyglucose in the stomach wall as a result of gastritis.
PET correctly identified distant metastases in 11 of 102 patients(11 percent) in whom the usual methods of staging had foundnone. In three other patients, intrapulmonary metastases hadbeen detected by CT. In three patients without hot spots, distantmetastases developed during follow-up. No distant metastaseswere diagnosed during follow-up in 79 patients without hot spotson PET. The sensitivity and specificity of PET for detectingdistant metastases alone were 82 percent (95 percent confidenceinterval, 64 to 100 percent) and 93 percent (95 percent confidenceinterval, 88 to 98 percent), respectively. The degree of interobserveragreement was 0.98 (95 percent confidence interval, 0.73 to1.0).
CT of the Chest
In 20 of the 37 lymph-node levels that were positive for metastatictumor on histopathological analysis, CT revealed enlarged mediastinallymph nodes. CT correctly identified 46 of 70 patients who didnot have mediastinal metastases on histopathological analysisand 24 of 32 patients who did have mediastinal metastases (Table 2).In eight patients with mediastinal lymph-node metastases,the size of the lymph nodes was normal. The sensitivity of CTwas 75 percent (95 percent confidence interval, 60 to 90 percent),and the specificity was 66 percent (95 percent confidence interval,55 to 77 percent). An example of a mediastinal metastasis thatwas identified as a hot spot on PET but was deemed normal onCT is shown in Figure 4.
Figure 4. CT and PET Findings in a Patient with Squamous-Cell Carcinoma of the Right Lung.
No abnormal mediastinal lymph nodes were observed at level 2 on the CT scan (Panel A). On the corresponding axial PET scan (Panel B) and coronal PET scan (Panel C), the uptake of 18F-fluorodeoxyglucose was increased (arrows). The arrow in Panel A indicates the area of increased uptake in Panels B and C.
Overall Prognostic Value of PET
The overall sensitivity and specificity of PET, as comparedwith histopathological analysis, in detecting mediastinal anddistant metastatic disease were 95 percent (95 percent confidenceinterval, 88 to 100 percent) and 83 percent (95 percent confidenceinterval, 74 to 92 percent), respectively. Logistic-regressionanalysis revealed that the results of both PET and CT were significantlycorrelated with the results of histopathological analysis. Whenadjusted for each other, however, the correlation remained significantonly for PET (P<0.001). The use of PET for clinical stagingresulted in a different stage from the one arrived at by theusual methods in 62 of 102 patients. In 20 patients the stagedetermined by PET was lower, and in 42 patients it was higher(P<0.01 by the two-sided sign test).
Discussion
The ability of PET to identify tumors depends primarily on thedegree of uptake of 18F-fluorodeoxyglucose by malignant cells,the size of the tumor, and the presence or absence of inflammation.Non–small-cell lung-cancer cells avidly incorporate 18F-fluorodeoxyglucosebecause they have an increased rate of glycolysis and overexpressthe glucose transporter.15 At presentation, most non–small-celllung cancers are large enough to have hot spots on PET scans.Inflammation from an obstructing endobronchial tumor or otherinflammatory processes cause most of the false positive hotspots on PET scans. Previous studies have found that PET hasgood sensitivity and specificity for detecting mediastinal lymph-nodemetastases, but some of these investigations did not reportto what extent surgical exploration was used to confirm thepresence of such metastases.5,6,16 The sensitivity and specificityof this method can be misleadingly high if a biopsy of normal-sizedlymph nodes with minimal tumor is not performed. To relate PETdata to histopathological data, both normal-appearing and abnormal-appearinglymph nodes must undergo biopsy or be removed for further examination.In our study, 97 percent of the mediastinal lymph-node levelsthat could be reached surgically were dissected and underwenthistopathological analysis.
A disadvantage of PET is its limited anatomical resolution,which makes assessment of the extent of the primary tumor, especiallyif it invades the mediastinum, unreliable. For the same reason,mediastinal hot spots can be related only to lymph-node levelsand not to individual lymph nodes. We defined these levels duringthe preliminary part of the study to facilitate the interpretationof distinct hot spots in the mediastinum.
Another problem with PET is that 18F-fluorodeoxyglucose accumulatesas part of the physiologic process in the brain and urinarytract, which makes an evaluation of metastases at these sitesdifficult. A qualitative analysis of PET images can serve onlyto rule out the presence of such metastases and not to identifythem.7,17 This point brings the usefulness of transmission scanningfor this purpose into question, although the results of mediastinaland hepatic scanning are slightly improved after correctionfor attenuation of the 18F-fluorodeoxyglucose signal. The useof CT together with PET may help to pinpoint the anatomicallocation of the hot spot, especially in the case of intrapulmonarylymph nodes, which are located close to the mediastinum andthus can be mistaken for mediastinal lymph nodes.18 However,in one study, computerized fusion of the two types of imagesseemed to be only marginally more beneficial than simple visualcorrelation of the PET scan and CT scan in terms of pinpointingmetastases in thoracic lymph nodes.19 We also found that combiningCT with PET did not significantly improve sensitivity and specificity.
The high negative predictive value of PET for mediastinal lymph-nodemetastases can be used to advantage in the approach to patientswith non–small-cell lung cancer, because invasive proceduresare probably not necessary in a patient with negative findingson PET in the mediastinum. However, our finding of a positivepredictive value of 74 percent means that patients in whom amediastinal hot spot is found on PET will need to undergo acervical mediastinoscopy as part of the workup for non–small-celllung cancer. The positive predictive value will be lower inpatients with inflammatory changes.20,21
Frequent sites of distant metastasis in patients with non–small-celllung cancer are the liver, adrenal glands, bone, and brain.Whole-body PET can replace other types of imaging for all thesesites except the brain, where the degree of uptake of 18F-fluorodeoxyglucoselacks specificity. The use of PET to identify distant metastasesin patients with non–small-cell lung cancer has not beenextensively studied, but the method may offer better resultsfor bone metastases than bone scanning.8 If we had not alsoperformed invasive procedures in our study, 17 percent of patientswould have been denied potentially curative surgery becauseof false positive mediastinal or distant hot spots or both.For this reason, a positive PET result requires an evaluationinvolving mediastinoscopy and, if indicated for distant lesions,additional procedures.
Our study confirms that, as compared with traditional stagingmethods, PET can result in a more accurate classification ofthe stage of disease in patients with resectable non–small-celllung cancer. The increased accuracy may improve survival, butthis outcome was not the primary end point of our study. Therefore,a randomized study is necessary to determine whether a diagnosticstrategy that includes PET can improve survival. However, somesmall studies have suggested that the use of standardized uptakevalues for the primary tumor has independent prognostic value.22,23
Concurrent detection of mediastinal and distant metastases by18F-fluorodeoxyglucose PET will decrease the number of testsand invasive procedures required in the evaluation of patientswith non–small-cell lung cancer. Implementing PET at thestart of the staging process may improve the efficiency of theworkup, but at this time the procedure is not cost effective,given the limited availability of dedicated PET cameras.
Supported by a grant for data management from Groningen UniversityHospital.
Source Information
From the Departments of Pulmonary Diseases (R.M.P., J.W.G.P., G.H.K., H.J.M.G.), Thoracic Surgery (J.J.M.), Radiology (E.L.M.), and Biostatistics and Epidemiology (V.F.) and the Positron-Emission Tomography Center (R.M.P., W.V., J.P.), Groningen University Hospital, Groningen, the Netherlands. Presented in part at the International Conference of the American Thoracic Society–American Lung Association, San Diego, Calif., April 23–28, 1999, and at the Annual Meeting of the American Society of Clinical Oncology, Atlanta, May 15–18, 1999.
Address reprint requests to Dr. Groen at the Department of Pulmonary Diseases, Groningen University Hospital, Hanzeplein 1, 9700 RB Groningen, the Netherlands, or at h.j.m.groen{at}int.azg.nl.
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125: 2300-2308
[Abstract][Full Text]
level of 0.05 a difference of 35 percent between the sensitivity of PET and that of CT (whose sensitivity was assumed to be 60 percent). In order to identify such a difference, the study required a minimum of 30 patients with mediastinal metastases. Assuming that mediastinal metastases are present in about 30 percent of patients with resectable non–small-cell lung cancer, a minimum of 100 patients had to be enrolled. 
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