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Non-Small Cell Lung Cancer: FDG PET for Nodal Staging in Patients with Stage I Disease¹

¹ From the Department of Radiology (M.A.F., H.P.M., E.F.P.) and the Biometry Division, Community and Family Medicine (J.E.H.), Box 3808, Duke University Medical Center, Erwin Rd, Durham, NC 27710. Received August 16, 1999; revision requested October 14; revision received October 25; accepted November 2. Address correspondence to E.F.P. (e-mail: patz0002 @mc.duke.edu).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To determine the accuracy of 2-[fluorine-18]fluoro-2-deoxy-D-glucose (FDG) positron emission tomography (PET) in the evaluation of regional lymph nodes in patients with stage I non–small cell lung cancer (NSCLC).

MATERIALS AND METHODS: Imaging and clinical findings obtained during 5 years in 84 patients (mean age, 66 years) were reviewed. Patients had thoracic computed tomographic findings of stage I NSCLC, an FDG PET study, and histopathologic proof of lung cancer. At the time of diagnosis, disease stage was assigned on the basis of FDG PET results and was compared with the histopathologic stage to determine the accuracy of PET.

RESULTS: When PET stage was compared with histopathologic stage, the disease in 72 (86%) patients was accurately staged with PET, understaged in two (2%), and overstaged in 10 (12%). The overall sensitivity, specificity, and positive and negative predictive values for PET of regional lymph nodal metastases were 82%, 86%, 47%, and 97%, respectively.

CONCLUSION: FDG PET enables accurate staging of regional lymph node disease in patients with stage I NSCLC. A negative PET scan in these patients suggests that mediastinoscopy is unnecessary and that these patients can proceed directly to thoracotomy.

Index terms: Fluorine, radioactive • Lung, CT, 60.12111, 60.12112 • Lung, PET, 60.12163 • Lung neoplasms, 60.321 • Lung neoplasms, staging, 60.12111, 60.12112, 60.12163 • Lymphatic system, neoplasms, 67.33, 996.33 • Lymphatic system, PET, 996.12963

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
The optimal staging approach in patients with non–small cell lung cancer (NSCLC) who have no evidence of regional lymph node or distant metastases at computed tomography (CT) is controversial (1–3). Unfortunately, CT is limited in the evaluation of nodal status because it provides only presumptive evidence of metastatic disease on the basis of size criteria. The sensitivity and specificity of CT in this regard are approximately 60% each, which is certainly not optimal for clinical decision making (4–6). Despite the fact that the prevalence of mediastinal nodal metastases is as high as 26% in this setting (7–10), many patients proceed directly to thoracotomy for primary resection with random hilar lymph nodal sampling. At other institutions, such patients routinely undergo mediastinoscopy before thoracotomy (1–3). A more accurate noninvasive means for determining lymph node status in patients with early-stage NSCLC would be extremely useful for assigning patients to the most appropriate staging procedure.

Positron emission tomography (PET) with 2-[fluorine-18]fluoro-2-deoxy-D-glucose (FDG) is a noninvasive imaging modality that provides metabolic information useful for tumor imaging (11,12). Increased glucose utilization by malignant cells results in increased FDG accumulation, which can help identify malignant abnormalities. The sensitivity and specificity of FDG PET in the detection of thoracic nodal metastases in patients with NSCLC are reported to be approximately 80% each (13–22). Although FDG PET may not be optimal, it is clearly better than CT and appears to be cost-effective (23,24). In addition, most of these data were derived from studies that included patients in all stages of NSCLC, not just those with early-stage disease. We performed this study to determine whether FDG PET is useful for evaluating regional lymph nodes in patients with clinical stage I NSCLC.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patients
We retrospectively reviewed imaging and clinical findings in all patients examined at our institution from September 1992 to February 1997 who (a) were classified as having stage I NSCLC at CT, (b) had undergone a complete FDG PET study of the thorax, and (c) had histopathologically proved lung cancer. CT stage IA or IB disease was defined according to the International System for Staging Lung Cancer criteria (25) as a peripheral primary lesion (T1 or T2) without evidence of regional lymph node (N0) or distant metastasis (M0). Eighty-four patients (45 men, 39 women; age range, 47–82 years; mean age, 66 years) met these entrance criteria and were included in the study.

Thoracic CT
CT examinations at our institution were performed with an Advantage scanner (GE Medical Systems, Milwaukee, Wis). Fifty-four patients underwent nonenhanced CT from the lung apices through the adrenal glands by using 10-mm collimation at 10-mm intervals. Nine patients underwent contrast material–enhanced CT 25 seconds after intravenous administration of 150 mL of iopamidol (Isovue 300; Bracco Diagnostics, Princeton, NJ) at a rate of 3 mL/sec. Twenty-one patients underwent CT at outside institutions with various techniques, most commonly 10-mm collimation at 10-mm intervals after intravenous administration of contrast material. All CT studies were reviewed in consensus by at least two experienced thoracic radiologists (M.A.F., H.P.M., E.F.P.), and stage I disease was confirmed.

FDG PET
FDG PET was performed with a 4096 Plus or Advance tomograph (GE Medical Systems, Milwaukee, Wis). The 4096 Plus unit produced 6.5-mm-thick image planes (eight direct planes and seven cross planes). The resolution of the scanner at full width at half maximum was 5 mm, and the longitudinal field of view was 10.3 cm. The Advance tomograph produced 4.25-mm-thick image planes (18 direct and 17 cross planes). The transverse field of view was 15 cm, and the intrinsic scanner resolution at full width at half maximum was 5 mm. Image processing and reconstruction were performed with several computer systems (VAX 4000-300 or 3100, Digital Equipment Corporation, Marlboro Mass; HP735, Hewlett Packard, Palo Alto, Calif).

All patients fasted for at least 4 hours before imaging. Transmission scans were obtained before emission scans by using a rotating germanium 68 pin source. Transverse emission scans of the thorax were then obtained 30–90 minutes after injection of 10.0 mCi (370 MBq) of FDG. One or two bed positions were used as needed.

FDG accumulation within the regional lymph nodes on attenuated corrected images was graded independently on hard-copy images and reviewed by at least two experienced readers (M.A.F., H.P.M., E.F.P.), and consensus scores were recorded. Hilar or mediastinal nodes were determined to be positive if activity was increased relative to that of adjacent normal mediastinal and soft-tissue structures; the nodes were judged to be negative if the activity was equal to or less than that of adjacent mediastinal or soft-tissue structures (26). Lymph node location was classified as N1 if the positive node was located in the ipsilateral hilum, N2 if it was in the ipsilateral mediastinum, and N3 if it was in the contralateral hilum or mediastinum. All patients were assigned a PET stage on the basis of FDG PET findings. The PET stage was defined according to the International System for Staging Lung Cancer criteria (25).

Nodal Status and Clinical-Histopathologic Stage
At the time of presentation, the N (nodal) status was determined for each patient on the basis of findings at mediastinoscopy (n = 20 [24%]) or thoracotomy (n = 64 [76%]). Complete standard mediastinal nodal sampling was performed at mediastinoscopy, and ipsilateral hilar and mediastinal sampling was performed during thoracotomy. A clinical-histopathologic stage was then assigned to each patient on the basis of the surgical findings and the TNM classification according to the International System for Staging Lung Cancer criteria (25).

	RESULTS

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Clinical-Histopathologic Stage
At the time of presentation, stage I disease was diagnosed in 73 of the 84 patients (stage IA disease in 56, stage IB disease in 17); stage II disease, in seven (stage IIA disease in six, stage IIB disease in one); and stage IIIA disease, in four. Histologic subtypes included adenocarcinoma (n = 33), squamous cell carcinoma (n = 32), large cell carcinoma (n = 7), bronchioloalveolar carcinoma (n = 6), adenosquamous carcinoma (n = 5), and sarcomatous carcinoma (n = 1). The primary lesions occurred in the left upper (n = 31), right upper (n = 26), right lower (n = 11), left lower (n = 12), and right middle (n = 4) lobes.

CT Stage
By definition, all 84 patients in this study were considered to have CT stage I disease. Of these 84 patients, 66 had stage IA (T1N0M0) disease and 18 had stage IB (T2N0M0) disease. When we compared the CT stage with the initial clinical-histopathologic stage, the disease was correctly staged with CT in 73 (87%) patients and understaged in 11 (13%). At surgery, seven patients had ipsilateral hilar nodal metastases (N1, clinical-histopathologic stage II), and four had ipsilateral mediastinal nodal metastases (N2, clinical-histopathologic stage IIIA).

FDG PET Stage
At PET, stage I disease was diagnosed in 65 patients, stage II disease in eight patients, stage IIIA disease in eight patients, stage IIIB disease in two patients, and stage IV disease in one patient. When we compared the PET stage with the clinical-histopathologic stage, 72 patients (86%) were correctly staged with PET (Tables 1, 2).

View larger version (131K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Images in a 52-year-old man who presented with a cough. (a) Transverse CT scan at the level of the carina demonstrates a 1.8-cm-diameter left hilar mass (arrow). No other abnormalities were identified. (b) Transverse PET scan through the same region as in a demonstrates substantial FDG uptake in the left hilar mass (arrow), which is suggestive of a malignancy. No other abnormalities were identified. After lobectomy, poorly differentiated adenocarcinoma was found in one of nine adjacent peribronchial lymph nodes positive for metastatic disease in the left upper lobe specimen. This represented a false-negative study.

View larger version (122K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Images in a 52-year-old man who presented with a cough. (a) Transverse CT scan at the level of the carina demonstrates a 1.8-cm-diameter left hilar mass (arrow). No other abnormalities were identified. (b) Transverse PET scan through the same region as in a demonstrates substantial FDG uptake in the left hilar mass (arrow), which is suggestive of a malignancy. No other abnormalities were identified. After lobectomy, poorly differentiated adenocarcinoma was found in one of nine adjacent peribronchial lymph nodes positive for metastatic disease in the left upper lobe specimen. This represented a false-negative study.

Six patients were classified as having PET stage III (N2 or N3) disease but had no evidence of hilar or mediastinal lymph nodal metastases at surgery or mediastinoscopy (N0, clinical-histopathologic stage I). Three of these six patients were alive without evidence of recurrence at 12, 20, and 67 months after resection, two died of unrelated causes at 4 and 10 months after resection without evidence of recurrence, and the sixth developed recurrence 12 months after resection.

One patient was classified as having PET stage IV (M1) disease because of a possible liver metastasis. Because the CT scan was negative at the time of presentation (and at review), this patient was considered to have clinical-histopathologic stage I disease and underwent surgery. Three months after resection, however, CT demonstrated a new 2.5-cm-diameter mass in the liver that corresponded in location to the initial finding at FDG PET. Subsequent CT scans demonstrated increasing enlargement of this lesion and new lesions, which was consistent with progressive metastatic disease (Fig 2).

View larger version (107K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Images in a 62-year-old woman with chronic obstructive pulmonary disease in whom a pulmonary nodule was found at chest radiography. (a) Transverse CT scan demonstrates a 2-cm-diameter nodule (arrow) in the right upper lobe. (b) Transverse PET scan demonstrates substantial FDG uptake (arrow), which is consistent with a malignancy. (c) Transverse PET scan obtained at the time of diagnosis demonstrates a focal area of increased FDG uptake (arrow) in the caudate lobe of the liver, which is suggestive of stage IV disease. There was no corresponding abnormality on the CT scan. The patient underwent primary resection. (d) Transverse CT scan obtained 3 months after resection shows that the patient developed a 2.5-cm-diameter lesion (arrow) in the caudate lobe of the liver. This lesion was seen to progressively increase in size on subsequent scans, a finding consistent with metastatic disease.

View larger version (88K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Images in a 62-year-old woman with chronic obstructive pulmonary disease in whom a pulmonary nodule was found at chest radiography. (a) Transverse CT scan demonstrates a 2-cm-diameter nodule (arrow) in the right upper lobe. (b) Transverse PET scan demonstrates substantial FDG uptake (arrow), which is consistent with a malignancy. (c) Transverse PET scan obtained at the time of diagnosis demonstrates a focal area of increased FDG uptake (arrow) in the caudate lobe of the liver, which is suggestive of stage IV disease. There was no corresponding abnormality on the CT scan. The patient underwent primary resection. (d) Transverse CT scan obtained 3 months after resection shows that the patient developed a 2.5-cm-diameter lesion (arrow) in the caudate lobe of the liver. This lesion was seen to progressively increase in size on subsequent scans, a finding consistent with metastatic disease.

View larger version (96K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. Images in a 62-year-old woman with chronic obstructive pulmonary disease in whom a pulmonary nodule was found at chest radiography. (a) Transverse CT scan demonstrates a 2-cm-diameter nodule (arrow) in the right upper lobe. (b) Transverse PET scan demonstrates substantial FDG uptake (arrow), which is consistent with a malignancy. (c) Transverse PET scan obtained at the time of diagnosis demonstrates a focal area of increased FDG uptake (arrow) in the caudate lobe of the liver, which is suggestive of stage IV disease. There was no corresponding abnormality on the CT scan. The patient underwent primary resection. (d) Transverse CT scan obtained 3 months after resection shows that the patient developed a 2.5-cm-diameter lesion (arrow) in the caudate lobe of the liver. This lesion was seen to progressively increase in size on subsequent scans, a finding consistent with metastatic disease.

View larger version (117K): [in this window] [in a new window] [Download PPT slide]   Figure 2d. Images in a 62-year-old woman with chronic obstructive pulmonary disease in whom a pulmonary nodule was found at chest radiography. (a) Transverse CT scan demonstrates a 2-cm-diameter nodule (arrow) in the right upper lobe. (b) Transverse PET scan demonstrates substantial FDG uptake (arrow), which is consistent with a malignancy. (c) Transverse PET scan obtained at the time of diagnosis demonstrates a focal area of increased FDG uptake (arrow) in the caudate lobe of the liver, which is suggestive of stage IV disease. There was no corresponding abnormality on the CT scan. The patient underwent primary resection. (d) Transverse CT scan obtained 3 months after resection shows that the patient developed a 2.5-cm-diameter lesion (arrow) in the caudate lobe of the liver. This lesion was seen to progressively increase in size on subsequent scans, a finding consistent with metastatic disease.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Once the diagnosis of NSCLC is established, accurate staging is essential for therapeutic decision making and prognostication. The differentiation of resectable from nonresectable disease is the most important step in this process. Patients with stage I to stage IIIA disease typically are considered to be candidates for surgery, whereas patients whose disease is in an advanced stage are referred for chemotherapy or radiation therapy.

The limitations of CT for accurate staging of hilar and mediastinal lymph nodes are well known. Although a number of CT protocols are used to stage lung cancer, with or without the use of intravenous contrast material administration, this variability does not seem to substantially alter the stage or clinical management (27,28). The sensitivity, specificity, and negative predictive value of CT for regional lymph nodal metastases from NSCLC are all approximately 60% (4–6,29,30). In many patients, the disease is under- or overstaged when CT is the only modality used for staging. For these reasons, mediastinoscopy for nodal sampling is commonly performed before definitive resection in patients known to have or suspected of having NSCLC (1,3,31).

There is, however, no uniform consensus regarding the optimal approach in patients with early-stage (stage I) disease (1,3). If the CT scan is negative, many such patients are referred directly for thoracotomy, despite the fact that the prevalence of nodal metastases in this situation may be as high as 26% (7–10). In addition, up to 70% of patients with clinical stage I disease eventually die of their disease, which is further evidence that CT is not the optimal staging modality in these patients.

Our results confirm those of previous studies regarding the accuracy of FDG PET for demonstration of regional lymph nodal metastases in patients with NSCLC. In this study, FDG PET had a high sensitivity for mediastinal (N2 or N3) nodal metastases and, more important, a high negative predictive value. These results suggest that patients with T1 or T2 primary lesions in whom both CT and FDG PET studies are negative for mediastinal nodal metastases do not require mediastinoscopy but can proceed directly to thoracotomy.

The sensitivity of FDG PET for ipsilateral (N1) nodal metastases was not optimal, although the two patients in whom disease was understaged had central lesions with small contiguous lobar and peribronchial nodes. Because of the resolution of PET, the primary tumor and positive adjacent nodes could not be visualized separately. These findings, however, are of no real clinical importance because they do not affect nodal sampling procedures or preclude surgical resection.

When the FDG PET stage was compared with the clinical-histopathologic stage, we found that disease in 10 patients was overstaged with PET. Results of previous studies (14–17,19,22,32) have shown that reactive nodes may show increased FDG accumulation, and this appears to have been the case in several of our patients. It should be noted, however, that standard lymph nodal sampling and histopathologic evaluation, although considered the diagnostic standard of reference, are not always accurate. A sampling error at surgery or mediastinoscopy can result in understaging, particularly because many nodes that harbor metastatic deposits appear normal at surgery (33). In addition, microscopic metastases can be overlooked at conventional histopathologic examination, as demonstrated with the addition of immunohistochemical staining or polymerase chain reaction techniques (31,34–36).

In our study, the disease in three patients was overstaged with PET because the scans were suggestive of metastatic disease to the ipsilateral hilum that was not confirmed at surgery. These findings, as noted earlier, did not alter the surgical staging approach, because the mediastinum was negative and hilar nodal sampling was performed at resection. In addition, all three of these patients developed local recurrence or metastases within a year, which suggests that the initial histopathologic stage was incorrect (disease was understaged) and that the FDG PET stage may, in fact, have been correct.

In addition, the disease in seven patients was overstaged with PET because the scans were suggestive of metastatic disease to mediastinal nodes (N2, n = 6) or liver (M1, n = 1). Such findings obviously alter surgical management and suggest that a positive FDG PET scan cannot be accepted as definitive proof of metastases. Further staging procedures, including mediastinoscopy or biopsy, are usually required. It should be noted, however, that two of these patients eventually developed recurrent disease or metastases. This again suggests that the initial histopathologic stage may have been incorrect and that the FDG PET stage was correct. In fact, of the 10 patients in whom disease was considered to be overstaged with FDG PET, five (50%) developed metastases or died of their disease. It is likely that the FDG PET stage was more accurate than was initially suggested.

In summary, our retrospective data suggest that FDG PET can be used to assign patients in whom stage I NSCLC has been diagnosed at CT to the most appropriate staging procedure. Patients with positive mediastinal nodes at FDG PET can proceed to mediastinoscopy for biopsy, and those nodal stations determined to be worrisome for metastatic disease at PET can be targeted. Patients with a negative FDG PET scan of the mediastinum can proceed directly to thoracotomy. These preliminary data are encouraging and suggest that a larger prospective trial with complete nodal sampling and FDG PET correlation is needed before the full effect of this technology can be realized.

	Footnotes

 
Abbreviations: FDG = 2-[fluorine-18]fluoro-2-deoxy-D-glucose, NSCLC = non–small cell lung cancer

Author contributions: Guarantors of integrity of entire study, M.A.F., H.P.M., E.F.P.; study concepts, H.P.M., E.F.P.; study design, J.E.H., E.F.P.; definition of intellectual content, H.P.M., E.F.P.; literature research, M.A.F., H.P.M., E.F.P.; clinical studies, M.A.F., H.P.M., E.F.P.; data acquisition, M.A.F., E.F.P.; data analysis, M.A.F., J.E.H., E.F.P.; statistical analysis, J.E.H.; manuscript preparation, editing, and review, all authors.

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TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 

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