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Nuclear Medicine |
1 From the Departments of Radiology (E.M.M., H.P.M., J.J.E., P.C.G., R.E.C., E.F.P.) and Medicine (J.E.H.), Duke University Medical Center, Box 3808, Durham, NC 27710; and the Department of Radiology, Veterans Affairs Medical Center, Durham, NC (D.K.C.). Received July 27, 1998; revision requested September 24; final revision received December 9; accepted March 29, 1999. Address reprint requests to E.F.P.
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: Within 20 months, 100 patients with newly diagnosed bronchogenic carcinoma underwent whole-body FDG PET and chest CT. Ninety of these patients underwent radionuclide bone scintigraphy, and 70 patients underwent brain CT or MR imaging. For each patient, all examinations were completed within 1 month. A radiologic stage was assigned by using PET and conventional imaging independently and was compared with the pathologic stage. The accuracy, sensitivity, specificity, and negative and positive predictive values were calculated.
RESULTS: PET staging was accurate in 83 (83%) patients; conventional imaging staging was accurate in 65 (65%) patients (P < .005). Staging with mediastinal lymph nodes was correct by using PET in 67 (85%) patients and by using CT in 46 (58%) patients (P < .001). Nine (9%) patients had metastases demonstrated by using PET that were not found with conventional imaging, whereas 10 (10%) patients suspected of having metastases because of conventional imaging findings were correctly shown with PET to not have metastases.
CONCLUSION: Whole-body PET was more accurate than thoracic CT, bone scintigraphy, and brain CT or MR imaging in staging bronchogenic carcinoma.
Index terms: Bronchi, neoplasms, 60.3211, 60.3212, 60.3214, 60.3216, 60.3217 • Lung neoplasms, emission CT (ECT), 60.12163 • Lung neoplasms, staging, 60.3211, 60.3212, 60.3214, 60.3216, 60.3217
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Positron emission tomography (PET) by using 2-[fluorine 18]fluoro-2-deoxy-D-glucose (FDG) has been shown to be an accurate imaging modality that complements conventional studies in evaluating patients with bronchogenic carcinoma. Previous studies have examined the utility of PET for imaging the primary tumor, regional lymph nodes, and distant disease (3–8). The purpose of this study was to compare the accuracy of whole-body FDG PET imaging to the accuracies of other routine conventional imaging studies used in staging newly diagnosed bronchogenic carcinoma.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Radiologic Staging
One hundred patients (58 men, 42 women; mean age, 63 years; age range, 25–83 years) underwent whole-body PET and thoracic CT. Ninety of the 100 patients underwent radionuclide bone scintigraphy, and 78 patients underwent brain CT or MR imaging. All studies were completed within 1 month of the diagnosis and before treatment.
PET Imaging
All 100 patients underwent whole-body FDG PET, as requested for staging of newly diagnosed lung cancer at our institution. Studies were performed with an Advance (GE Medical Systems, Milwaukee, Wis) PET scanner (9). Patients fasted for at least 4 hours before receiving the intravenous administration of 145 µCi/kg (5,365 kBq/kg; maximum, 20 mCi [740 MBq]) FDG. Thirty minutes following the injection, a 4-minute acquisition in the brain was performed by using the three-dimensional acquisition mode (9). The system was switched to the two-dimensional acquisition mode, and non–attenuation-corrected scans were obtained for 4 minutes per bed position from the level of the base of the brain through the middle of the thighs. A two–bed-position, attenuation-corrected regional chest scan was then obtained by using 8 minutes for emission scanning and 10 minutes for transmission scanning at each bed position. The emission brain scan was corrected for attenuation by using a calculated attenuation correction (10). The images were reconstructed by using a Hann filter, with a cutoff of 0.71/cm. Reconstructed images were displayed in a 128 x 128 matrix with 35 sections, which contained 3.5 x 3.5 x 4.25-mm voxels.
Standardized uptake values were obtained by placing a circular region of interest within the visible margin of the lesion in an area of abnormal FDG accumulation on the attenuation-corrected PET images in the axial plane that best showed the lung abnormality to include the most intense area of FDG accumulation (11). Activity concentration was averaged over the circular region of interest. After correction for radioactive decay, the standardized uptake value was calculated by dividing the mean activity in the lesion by the administered FDG dose per kilogram of body weight (11).
All PET studies were interpreted independently on film hard copy in combination with an interactive video display by two experienced nuclear medicine physicians. Disagreements in interpretation were resolved by consensus. Images were correlated with the chest CT scans. Bone and brain images were not available for comparison.
PET images were read as positive or negative at the primary site (T status), regional lymph nodes (N status), and distant metastases (M status). Lung lesions were considered positive when uptake was greater than the mediastinal blood pool activity. If visual uptake in the lung lesion was similar to that in the mediastinal blood pool, a standardized uptake value was obtained; the lesion was considered malignant if the value obtained was greater than 2.5 (11). Areas of accumulations greater than that in the surrounding normal tissue were considered abnormal for regions outside of the lungs. A PET stage based on the TNM status was assigned according to the revised International System for Staging Lung Cancer (12).
CT Imaging
Sixty-one patients underwent chest CT at our institution with a model 9800 CT HiSpeed Advantage scanner (GE Medical Systems) by using 10-mm collimation (pitch = 1) from the lung apex through the liver. The remaining 39 patients underwent examinations (n = 39) outside our institution with a variety of scanners and either 7- or 10-mm collimation (pitch = 1) from the lung apices through the liver. Intravenous contrast material was administered in 72 patients (72%).
All contrast-enhanced and nonenhanced chest CT scans were interpreted independently by at least two experienced thoracic radiologists (E.M.M., H.P.M., J.J.E., P.C.G., D.K.C., E.F.P.), and a CT stage was assigned by using TNM descriptors according to the revised International System for Staging Lung Cancer (12,13). We did not make a distinction between contrast-enhanced and nonenhanced scans in view of our prior experience (13). Disagreements in interpretation were resolved by consensus. Lymph nodes greater than 1 cm in the short axis were considered positive. The bone scintigrams and PET scans were not available at the time of interpretation.
Brain CT and MR Imaging
Seventy-eight (78%) patients underwent conventional imaging of the brain as routine staging for newly diagnosed lung cancer at our institution: 58 patients, brain CT; 15 patients, brain MR imaging; and five patients, brain CT and MR imaging. Brain CT examinations were performed with contrast material (100 mL of iopamidol [Isovue 300; Bracco Diagnostics, Princeton, NJ]) and a model 9800 CT HiSpeed Advantage scanner (GE Medical Systems) by using 5-mm collimation (pitch = 1) through the posterior fossa and 10-mm collimation (pitch = 1) through the rest of the brain.
Axial T1-weighted nonenhanced (500/20) and gadolinium-enhanced (500/20; Magnevist [gadopentetate dimeglumine]; Berlex, Wayne, NJ; dose, 0.1 mmol per kg of body weight), T2-weighted (2,500/80), and intermediate-weighted (2,500/30) MR images and coronal gadolinium-enhanced T1-weighted MR images (500/20) were obtained with a 1.5-T imager (GE Medical Systems; Signa 5X platform).
All brain studies were interpreted by an experienced neuroradiologist, and sites of metastatic disease were recorded. The PET scans were not available at the time of interpretation.
Bone Scintigraphy
Ninety (90%) patients underwent radionuclide bone scintigraphy as routine staging for newly diagnosed lung cancer at our institution. Whole-body images were obtained in the anterior and posterior projections starting 2–3 hours following the intravenous injection of 430 µCi/kg (15,910 kBq/kg; 30.0 mCi [1,110 MBq] maximum) of technetium 99m methylene diphosphonate. Either a Bodyscan (Nuclear Medicine Group, Siemens Medical Systems, Hoffman Estates, Ill) or a T-22 Twin Detector Nuclear Imaging System (SMV, Twinsburg, Ohio) was used for the radionuclide bone imaging studies.
Bone scintigrams were interpreted by two nuclear medicine physicians, and sites of metastatic disease were recorded. The PET scans were not available at the time of interpretation.
Clinical-Pathologic Correlation
All 100 patients had histologic confirmation of lung cancer. Transbronchial needle biopsy (n = 41), transthoracic needle biopsy (n = 38), mediastinoscopy (n = 26), thoracotomy (n = 41), or video-assisted thoracoscopic biopsy (n = 1) was performed. In 47 patients, histologic confirmation of lung cancer was obtained by using more than one of these methods.
Of the 100 patients, 79 patients had clinical-pathologic lymph node status assigned following biopsy (n = 48) or imaging follow-up with CT (n = 31) for a mean of 12.8 months (range, 1–49 months). Those patients with clinical follow-up had lymph nodes recorded as pathologic if there was a substantial change in size (>5 mm) at follow-up examinations relative to the baseline size. Twenty-one patients did not undergo nodal sampling or did not have sufficient follow-up because of distant metastatic disease or T4 lesions. Fourteen patients with metastases suggested on imaging studies underwent biopsy of distant sites.
Biopsy specimens from outside institutions were reviewed by an experienced pulmonary pathologist at our institution. A final pathologic stage was assigned after correlation of the radiologic findings and biopsy specimens.
Patients were followed up by reviewing their medical charts and radiologic studies for a mean of 10.7 months ± 7.4 (SD; range, 1–49 months). Radiologic follow-up intervals and imaging varied according to staging and treatment, but follow-up included a combination of chest or abdominal CT, radionuclide bone scintigraphy, brain CT or MR imaging, and chest or musculoskeletal radiography.
Statistical Analysis
The McNemar test was used to compare the accuracies of PET with those of conventional imaging modalities for nodal disease, M status, and site-specific metastases to the brain, bone, adrenal glands, liver, and lungs. Sensitivity, specificity, and positive and negative predictive values were calculated for PET, chest CT, bone scintigraphy, and brain CT and MR imaging for mediastinal nodal staging and staging of metastases by sites.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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PET staging was correct in 83 patients (83%), as compared with correct conventional imaging staging in 65 patients (65%; P < .005). PET correctly indicated that disease was unresectable in 12 (12%) patients in whom disease had been understaged and considered resectable at conventional imaging. Conventional imaging indicated that disease was unresectable in four (4%) patients in whom disease had been understaged and considered resectable at PET. PET correctly indicated disease was resectable in 11 (11%) patients in whom disease had been overstaged and considered unresectable at conventional imaging (Fig 1), whereas conventional imaging indicated disease was resectable in only two (2%) patients in whom disease had been overstaged and considered unresectable at PET. The distribution and correlation of the conventional imaging stages, PET stages, and clinical-pathologic stages are shown in Table 1.
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Lymph Node Status
PET correctly indicated the N status in 67 patients (85%), and CT correctly indicated the N status in 46 patients (58%; P < .001). Most important, for differentiation of surgical and nonsurgical candidates with N3 disease, the sensitivity of PET was 92% and that of CT was 25%; the specificity of PET was 93% and that of CT was 98% (P = .005). The distribution and correlation of lymph node status according to CT findings, PET findings, and clinical-pathologic confirmations are shown in Table 2.
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Brain Imaging
Five of the 78 patients who underwent conventional imaging of the brain had metastases at presentation that were confirmed with biopsy (n = 2) or with progression on follow-up CT scans (n = 3; mean follow-up, 3 months; range of follow-up, 1–6 months). PET showed brain metastases in three of the five patients with brain metastases. The other two patients had normal PET studies and had understaged disease; one proved to have a 5-mm lesion in the pons and the other had leptomeningeal disease. One patient had disease overstaged with PET, as increased uptake in the junction between gray matter and white matter was interpreted as metastatic disease, but no disease was found at initial and 8-month-follow-up brain MR imaging. The accuracy of PET for brain M staging was 96% (n = 75) and that of conventional imaging was 100% (n = 78; P = .248). The sensitivity, specificity, and positive and negative predictive values of PET for brain metastases were 60%, 99%, 75%, and 97%, respectively, and those of conventional imaging were 100%, 100%, 100%, and 100%, respectively.
Bone Imaging
Twelve patients had bone metastases at presentation proved with biopsy (n = 4) or clinical follow-up (n = 8) that showed progression on bone scintigrams obtained at a mean follow-up of 3 months (range, 1–8 months). Staging was correct with PET in 88 of the 90 patients who underwent bone scintigraphy, with an accuracy of 98%. Bone metastases were correctly identified with PET in 11 (92%) patients with bone metastases. One patient had disease that was understaged and had a metastasis to the distal femur, a region not included in the whole-body PET study, confirmed with biopsy. One patient had disease overstaged with PET, which demonstrated a focal thoracic vertebral body abnormality. There was no abnormality on CT scans, bone scintigrams, or conventional radiographs at the time of diagnosis, and 23 months after resection, the patient had no evidence of disease.
Bone metastases were correctly staged with bone scintigraphy in 78 of the 90 patients who underwent bone scintigraphy, with an accuracy of 87%. Bone metastases were correctly identified with bone scintigraphy in six of the 12 patients who had bone metastases, although disease was understaged in six patients, as the bone scintigrams were interpreted as normal. Six patients had disease that was overstaged or had equivocal bone scintigrams for metastatic disease, which was confirmed with a mean of 12 months of bone scintigraphic and/or radiographic follow-up (range, 9–15 months). PET was significantly more accurate than bone scintigraphy (P = .016). The sensitivity, specificity, and positive and negative predictive values of PET were 92%, 99%, 92%, and 99%, respectively, and those of bone scintigraphy were 50%, 92%, 50%, and 92%, respectively (Tables 3, 4).
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Liver Imaging
Six patients had liver metastases at presentation that were confirmed with CT follow-up, which showed interval growth over a mean of 6.8 months (range, 3–17 months). All hepatic lesions (100%) were correctly identified with PET. There were no false-positive liver lesions seen at PET. All six patients with liver metastases were correctly identified with CT. With CT, however, five benign liver lesions were overstaged as metastases, which was confirmed with CT follow-up (mean, 11.8 months; range, 4–18 months). Therefore, CT liver M staging was accurate in 95 (95%) patients in comparison to 100 (100%) patients with PET (P < .074). On follow-up CT scans, three additional patients developed new liver metastases. All had known distant metastases at other sites at the time of staging. One developed the metastases 14 months after staging, and the remaining two had liver metastases diagnosed at 9 and 15 months; however, each had a CT scan 3 months prior to development of the metastases that was negative. In two of the six patients with liver metastases at presentation, there were no other distant metastases at the time of presentation. The diameter ranged from 8 to 50 mm (mean ± SD, 18.7 mm ± 4.4). The sensitivity, specificity, and positive and negative predictive values of PET for liver metastases detection were 100%, 100%, 100%, and 100%, respectively; those of CT were 100%, 95%, 55%, and 100%, respectively.
Lung Imaging
Eighteen patients had lung metastasis proved with biopsy (n = 2) or had conventional imaging follow-up findings (n = 16) of interval growth during a mean of 3.5 months (range, 1–8 months). PET staging of the lung for metastases was correct in 98 (98%) of the 100 patients. PET helped identify 17 of the 18 patients with lung metastases (94%) at presentation. PET findings resulted in underestimation of disease in one patient (1%) with lymphangitic spread that had progressed in the 4-month conventional imaging follow-up interval and in overestimation of disease as metastatic in one (1%) patient whose region of FDG uptake was retrospectively thought to represent inflammation, as it had resolved on the follow-up 5-month PET scan and CT scan, while sites of metastatic disease showed progression. Lung metastases were correctly staged with CT in 91 (91%) of the 100 patients (P = .070). Fourteen (78%) of the 18 patients with lung metastases at presentation were identified at CT, with underestimation in the remaining four patients, which was proved by interval growth on CT follow-up scans (mean follow-up, 5.5 months; range, 4–8 months), and overstaging in five additional patients, which was proved by the stability of indeterminate lung nodules at CT over a mean of 8.5 months (range, 7–10 months). The sensitivity, specificity, and positive and negative predictive values of PET for lung metastases detection were 94%, 99%, 94%, and 99%, respectively, and those of CT were 78%, 94%, 74%, and 95%, respectively.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The new staging system and the TNM descriptors were designed for conventional imaging. They were constructed to reflect size and sites of disease, and this anatomic information is not always relevant for PET imaging. Describing the conventional T status is more problematic with PET than CT because of spatial resolution. As seen in this study, however, PET is adequate, and rare changes in the T status did not have a substantial effect on overall stage.
PET clearly demonstrates an advantage over CT in determining the N status. In a recent study, CT had only a 63% sensitivity and 57% specificity for mediastinal lymph node metastases, and 24% of normally sized nodes contained metastases (15). Thoracic CT provides only presumptive, not definitive, evidence for nodal disease. Its current utility is as a road map for guiding lymph node sampling, as small nodes may harbor tumor and large nodes may be reactive.
As conventional imaging is less than optimal, most thoracic surgeons still perform cervical mediastinoscopy (15), although this procedure alone cannot always be used to sample all pertinent lymph node groups. The addition of scalene lymph node biopsy has routinely been abandoned; however, in a recent study, Lee and Ginsberg (16) demonstrated that 15% of patients with N2-staged lung cancer harbored occult nonpalpable supraclavicular disease, which upstaged disease to N3 and resulted in an alteration in treatment. Evaluation of other nodal stations, including prevascular or paraesophageal stations, requires an additional procedure (17).
PET could have a substantial effect on nodal sampling. Whole-body studies demonstrate all lymph node stations and in some cases obviate mediastinoscopy. Because the negative predictive value of PET for N3 disease is identical to that of mediastinoscopy, which is 96% (15), patients with negative mediastinal PET findings could go directly to surgical resection of the primary lesion. Patients with a positive PET study in the mediastinum could undergo a single procedure guided by areas of abnormal FDG uptake.
PET also has an advantage over the combination of other routine studies required to determine the M status. Forty percent of patients with newly diagnosed lung cancer have distant metastases at presentation (1), although clinical and laboratory indicators for metastases are nonspecific, with an accuracy of only approximately 50% (18,19). Conventional imaging with thoracic CT, bone scintigraphy, or brain CT or MR is also less than optimal.
Overall, PET showed greater accuracy than conventional imaging in the detection of distant metastases. In nine patients (9%) not suspected of having metastases at conventional imaging, PET showed metastases. This result is similar to those of other studies (1,5).
When evaluating metastases by site, PET was almost uniformly superior to other conventional imaging modalities. PET was 92% sensitive and 99% specific for bone metastasis as compared to bone scintigraphy, with 50% sensitivity and 92% specificity. The whole-body PET study can eliminate the need for staging bone scintigraphy, as PET findings resulted in overstaging in only one patient and in understaging in one patient (98% accuracy). Understaging of a bone metastasis at PET may have been avoided by inclusion of the whole leg within the scanning plane, as the distal femur metastasis was not imaged with PET and therefore was missed.
Approximately two-thirds of the adrenal masses detected with conventional imaging in patients with lung cancer are reported to be benign (20,21). Our findings are in agreement with those of prior studies, as eight (57%) of 14 adrenal masses indeterminate at conventional imaging were benign. This low positive predictive value (43% in this study) leads to unnecessary adrenal biopsy, which is not without risk and is not always diagnostic. In a review of 83 adrenal biopsies, Mody et al (22) reported an 8.4% rate of complications, including pneumothorax, pain, perinephric hemorrhage, intrahepatic hematoma, and hepatic needle-track metastasis. The rate of false-negative percutaneous biopsy findings ranges from 2% to 8.6% (23–26).
In this study, the positive predictive value of PET for adrenal metastases detection was 100%. The high specificity (100%) in this study, when compared to that in a prior PET adrenal study (80%) (27), may be due to sampling error in the prior study's percutaneous biopsies because those patients with "false-positive" PET findings died shortly after the study, with no prior or follow-up imaging for comparison.
The normal brain has substantial glucose uptake, and a focal area of abnormal accumulation in the brain due to metastasis may be difficult to detect with PET. The low sensitivity (60%) is problematic when staging lung carcinoma, as the brain is a common site of metastatic disease; 5.5%–16.3% of patients with brain metastases are asymptomatic (28,29). Although brain imaging in whole-body PET lengthens the examination by 4 minutes, it is probably unnecessary because of PET's low sensitivity. Abnormalities likely to influence clinical management prospectively were not identified with PET (7), and PET should not replace conventional imaging for routine staging in the brain.
In this limited series, PET proved useful for hepatic metastases, as it showed no false-positive or, to our knowledge, false-negative liver lesions. This is in comparison with eight indeterminate abnormalities at CT. The true sensitivity and specificity still need to be evaluated further in a detailed study that would compare PET with a dedicated contrast-enhanced liver CT examination with sequential follow-up; however, preliminary study findings have shown PET to be superior to conventional imaging in the detection of liver metastases (30–34). Findings of this study suggest that the whole-body PET examination appears to complement conventional imaging in the liver, particularly when lesions are indeterminate.
From a clinical and radiologic perspective, one of the most important decisions is to determine if the patient is a surgical candidate. Disease that is stage IIIa or less is potentially resectable, while disease that is stage IIIB or higher is not. In this study, PET findings indicated that 12% of patients had disease mistakenly understaged and considered resectable at conventional imaging, whereas conventional imaging findings indicated that only 4% of the study patients considered surgical candidates at PET had disease understaged.
The cost-effectiveness of FDG PET in staging lung cancer has been studied in comparison to only that of chest CT. FDG PET, combining improved patient care with reduced treatment cost, has been found to be decisively more cost-effective than CT (35,36). When PET was considered as an addition to conventional staging procedures, the ratio of savings to cost was greater than 2:1. When PET was considered as replacing CT and bone scintigraphy, the ratio was greater than 3:1. PET was effective in reducing management costs even when it was an add-on procedure (35).
In conclusion, we believe whole-body PET is very useful in staging newly diagnosed lung cancer. There is marked improvement in staging the thorax with PET than with CT, with a predicted reduction in the morbidity rate and cost associated with unnecessary interventional procedures. PET appears to be more accurate than other modalities in differentiating resectable from nonresectable disease. Radionuclide bone scintigraphy may be eliminated, although brain imaging is still required if clinically indicated.
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Footnotes |
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Author contributions: Guarantors of integrity of entire study, E.M.M., J.J.E., P.C.G.; study concepts, R.E.C., E.F.P., J.J.E., H.P.M., P.C.G.; study design, E.F.P.; definition of intellectual content, J.J.E., H.P.M., P.C.G., E.F.P.; literature research, E.M.M., E.F.P.; clinical studies, all authors; data acquisition and analysis, E.M.M., D.K.C., E.F.P.; statistical analysis, J.E.H.; manuscript preparation, editing, and review, all authors
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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