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Nuclear Medicine |
1 From the Departments of Radiology (E.M.M., S.S., E.F.P.) and Biostatistics and Bioinformatics (J.E.H.), Duke University Medical Center, Box 3808, Durham, NC 27710. Received June 29, 2001; revision requested August 16; revision received September 17; accepted October 10. Address correspondence to E.M.M. (e-mail: marom001@mc.duke.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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3 cm) lung cancers.
MATERIALS AND METHODS: One hundred eighty-five patients with 192 histopathologically proved T1 lung cancers underwent FDG PET imaging at the time of diagnosis. PET results were correlated with tumor size, histopathologic findings, and patient outcome by using the two-sample t test, exact 
2 test, and log rank test, respectively.
RESULTS: Of the 192 lesions, 183 (95%) that ranged in size from 0.5 to 3.0 cm in diameter (mean, 2.0 cm) were positive at PET (ie, demonstrated increased FDG uptake). Of the 192 lesions, nine (5%) that ranged in size from 0.3 to 2.5 cm in diameter (mean, 1.3 cm) were negative at PET (ie, demonstrated low FDG uptake). Patients with small tumors, as well as those with carcinoid tumors and bronchioloalveolar cell carcinoma, were more likely to have a negative PET scan (P = .004, P = .003, respectively). In addition, patients with a negative PET scan who subsequently proved to have cancer had significantly longer survival than did patients with a positive scan and cancer (P = .043).
CONCLUSION: Most T1 lung cancers show increased FDG uptake on PET scans.
© RSNA, 2002
Index terms: Lung neoplasms, diagnosis, 68.311, 68.321 • Lung neoplasms, PET, 68.12163
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Unfortunately, PET is neither uniformly specific nor sensitive, particularly if the abnormality is small. Small nodules (<3 cm) with increased FDG uptake are usually considered to be malignant until proved otherwise, although some of these abnormalities will prove to be benign. Small nodules with no marked FDG uptake are usually considered to be benign, although rarely some prove to be malignant. Management of lesions in which FDG PET scans are negative, however, can be problematic, as it has been suggested that small size may preclude an accurate diagnosis and adversely affect prompt treatment. While the literature is replete with studies on solitary nodules, to the best of our knowledge no studies have specifically focused on T1 lesions. Therefore, the purpose of this study was to determine the sensitivity of PET in patients with T1 (3 cm) lung cancers.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Imaging Studies
PET scanning.—As defined by the entrance criteria, all patients had undergone a PET examination at the time of diagnosis and before treatment. FDG PET imaging was performed with either a GE 4096 Plus or a GE Advance PET scanner (GE Medical Systems, Milwaukee, Wis). Patients were instructed to fast for at least 4 hours prior to intravenous administration of 145 µCi/kg (5.36 MBq/kg) of body weight (maximum dose, 20 mCi [740 MBq]) of fluorine 18–labeled FDG.
Between April 1992 and January 1993, 23 PET examinations were performed with the GE 4096 Plus. This scanner produced 6.5-mm-thick transaxial image planes (eight direct planes and seven cross planes) with full-width at half-maximum of 5 mm. The transverse field of view was 10.3 cm. Immediately after the radiopharmaceutical was administered, a two-bed-position, attenuation-corrected regional chest examination was performed. The examination consisted of two transmission sequences of 20 minutes each followed by two emission sequences, also of 20 minutes each. Image processing and reconstruction were performed with a VAX 4000-300 computer system and a VAX 3100 workstation (Digital Equipment, Marlboro, Mass).
After January 1993, 164 PET imaging studies were performed with the GE Advance. After FDG administration, there was a 30-minute uptake period. Non–attenuation-corrected emission scans were initially obtained in two-dimensional, high-sensitivity mode for 4 minutes per bed position, from the skull base through the midthighs. Immediately thereafter, a two-bed-position attenuation-corrected regional chest examination was performed, with 8 minutes for the emission sequence and 10 minutes for the transmission sequence at each bed position. The images were reconstructed in a 128 x 128 matrix by using a Hann filter with a cutoff of 0.71/cm. The resulting pixels were 3.5 x 3.5 mm with section spacing of 4.25 mm.
Both the 4096 Plus and the Advance scanners employ rotating germanium 68 pin sources for transmission scanning. Correction for scatter, random events, and dead-time losses was performed for each scanner with the manufacturer’s software.
Two physicians experienced in reading PET scans interpreted all scans together in consensus. Chest computed tomographic (CT) scans were used to localize the abnormality before the PET study was performed; however, the physicians were blinded to the final diagnosis. The images were reconstructed in all three standard planes and were reviewed on hard copy film in combination with an interactive video display. PET images were interpreted as positive or negative at the primary site and for regional lymph node involvement and distant metastases (9). Lung lesions and lymph nodes were considered positive when FDG uptake was greater in them than in the mediastinal blood pool. Lesions outside the thorax were considered positive when they showed greater focal FDG accumulation than did the surrounding normal tissue.
Conventional imaging.—All patients underwent a thoracic CT examination at the time of diagnosis and before treatment. One hundred thirty-five patients underwent chest CT performed at our institution with a GE 9800 HiSpeed Advantage CT scanner or a QXi LightSpeed CT scanner (GE Medical Systems). Fifty-seven patients underwent chest CT performed at outside institutions with a variety of scanners that typically used 7–10-mm collimation (pitch, 1) from the lung apex through the adrenal glands. Intravenous contrast material was administered in the imaging of 95 (49%) of the 192 lung cancers (10).
All chest CT scans were interpreted at our institution together and in consensus by two experienced thoracic radiologists who were blinded to the PET study results and to the final diagnosis. The size (ie, T status) of the primary lesion and all other abnormalities was recorded.
Seventy-eight patients (42%) also underwent imaging of the brain at our institution for staging within 1 month of diagnosis— brain CT (n = 62), brain magnetic resonance (MR) imaging (n = 15), or brain CT and brain MR imaging (n = 1). CT of the brain was performed with contrast material (100 mL of iopamidol, Isovue 300; Bracco Diagnostics, Princeton, NJ) and a 9800 HiSpeed Advantage CT scanner (GE Medical Systems), with 5-mm collimation (pitch, 1) through the posterior fossa and 10-mm collimation (pitch, 1) through the rest of the brain. MR imaging was performed with a GE 1.5-T imager (GE Medical Systems, x5 platform). T1-weighted MR images were obtained in the transverse plane before and after the administration of contrast material (gadolinium chelate); T2- and intermediate-weighted MR images were obtained in the transverse plane; and T1-weighted, postcontrast MR images were obtained in the coronal plane. All brain images were interpreted by an experienced neuroradiologist, and sites of metastatic disease were recorded.
Eighty patients (43%) underwent radionuclide bone examinations at our institution for staging within 1 month of diagnosis. Whole-body images were obtained in anterior and posterior projections starting 2–3 hours after the intravenous injection of 430 µCi/kg (15.9 MBq/kg) (maximum dose, 30 mCi [1,110 MBq]) of technetium 99m methylene diphosphonate. Either a Body-Scan (Siemens Medical Systems, Hoffman Estates, Ill) or a T-22 unit (SMV, Twinsburg, Ohio) was used for the radionuclide bone imaging studies. Bone scans were interpreted by an experienced nuclear medicine physician, and sites of metastatic disease were recorded.
Clinical-Pathologic Correlation
Histopathologic features.—All 192 lung tumors in the 185 patients were histopathologically proved to be primary lung cancer. Biopsy specimens were obtained with a transbronchial needle (n = 42) or transthoracic needle (n = 47) or with mediastinoscopy (n = 7), thoracotomy (n = 131), or video-assisted thoracoscopy (n = 6). Some tumors were evaluated with more than one biopsy technique (n = 38).
Tumor size.—The size of each of the 192 primary lesions was recorded as the largest diameter at surgical resection in cases in which a diameter was provided on the pathology report (n = 125, 65%) or on the basis of CT measurement in the remainder of the cases (n = 67, 35%).
Stage at patient presentation.—Radiologic findings and biopsy results were used to assign a final clinical-pathologic stage according to the revised international system for staging lung cancer (11).
Survival data.—Up-to-date survival data were available from our tumor registry. At the completion of this study, 111 (60%) of the 185 patients were still alive at a mean follow-up of 29.4 months (range, 1–88 months; SD, 21.8).
Statistical Analysis
An exact 2 test was used to evaluative the relationship between histopathologic findings and PET results. Both parametric (two-sample t) and nonparametric (Wilcoxon signed rank) tests were used to compare the distribution of tumor size among patients with and patients without a positive PET scan. The Kaplan-Meier product limit estimator was used to describe graphically the survival experience of patient subgroups that were defined by the findings at PET (ie, whether a scan was positive or negative at the primary site). The log rank test was used to compare the survival experience of patient subgroups. Each patient was represented only once in these survival analyses. For those patients with metachronous lung cancers who underwent multiple PET studies, the date of the first PET study was used in the survival analysis. For patients with histopathologically proved synchronous lung cancers, the PET scan was considered positive if either of the lesions showed increased FDG activity. The PET scan was considered negative if none of the lesions had increased FDG uptake.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Tumor Size
Tumor size ranged from 0.3 to 3.0 cm in diameter (mean, 2.0 cm; SD, 0.7). Of note, 11 (6%) of the tumors were less than 1.0 cm in diameter.
Stage at Patient Presentation
The stage distribution for the T1 lesions was as follows: stage IA, n = 113 (59%); stage IIA, n = 14 (7%); stage IIIA, n = 20 (10%); stage IIIB, n = 6 (3%); and stage IV, n = 30 (16%). There were nine patients with small cell lung cancer; six (3%) had limited disease, whereas three (2%) had extensive disease.
Positive PET Scans
The PET scan was positive (ie, tumor uptake of FDG was greater than mediastinal uptake) in 183 (95%) of the 192 primary lesions (Fig 1). PET results did not differ significantly with the use of different PET scanners (P > .999). The size of the tumors ranged from 0.5 to 3.0 cm (mean, 2.0 cm). The stage at patient presentation and cell-type distribution are shown in Tables 1 and 2.
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Negative PET Scans
The PET scan was interpreted as negative (ie, tumor uptake of FDG was less than or equal to mediastinal uptake) in nine (5%) of the primary lesions (Fig 2). The size of the tumors ranged from 0.3 to 2.5 cm (mean, 1.3 cm). The stage at patient presentation and cell-type distribution are shown in Tables 1 and 2. Of note, all of the tumors with a negative PET scan were classified as stage IA at the time of diagnosis.
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Two (22%) of the nine patients who had a negative PET scan died. One of these patients had a synchronous lesion that was positive at PET and died within 18 months with metastatic disease; the other had a paraneoplastic syndrome and died of cardiac arrest while hospitalized. The cause of death was not determined. The remaining seven patients were without evidence of disease at a mean follow-up of 43 months (range, 21–70 months).
Statistical Considerations
The association between tumor size and FDG uptake at PET was statistically significant with parametric (P = .004, t test) and nonparametric (P = .030, Wilcoxon signed rank test) statistical methods. That is, smaller lung cancers were more likely to have negative scans than were larger tumors.
An exact 2 test showed that there was a significant difference among histopathologic groups in the proportion of patients with a negative PET scan (P = .003). The proportion of patients with a negative PET scan was highest among patients who had carcinoid tumors or bronchioloalveolar cell carcinoma (Table 2).
In addition, survival differed significantly between those patients with a positive PET result and those with a negative PET result (P = .043). Patients who had a negative PET scan had more indolent tumors than did patients who had a positive PET scan (Fig 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Many patients and physicians, however, do not want to wait because lung cancer is of concern. Patients often become anxious, and, theoretically, any marked delay in the diagnosis and treatment of lung cancer could affect outcome. On the other hand, biopsy or resection of all pulmonary nodules is not only impractical and expensive but also has associated morbidity and mortality and is not always diagnostic.
Over the past several years, FDG PET has become an additional option in the evaluation of patients with indeterminate lung lesions and has led to changes in the work-up of indeterminate pulmonary nodules. Numerous studies have shown PET to be effective in the differentiation of benign from malignant lesions, with an overall sensitivity, specificity, and accuracy estimated to be 96%, 88%, and 94%, respectively (1–7,16).
These studies have suggested that patients with increased FDG uptake should undergo histopathologic sampling of the lesion because of the concern for cancer. Patients who have a focal lung lesion that does not show significant FDG uptake, however, are often monitored because the lesions are most likely benign. Rarely, false-negative scans (ie, negative PET scans of lesions that prove to be malignant) have been reported, although none of these studies focused on smaller tumors, and most entailed the imaging of only patients with lesions larger than 10 mm (2,4,17–23).
With the increasing use of helical chest CT and the improved ability to reveal smaller nodules, PET imaging will almost certainly have a more central role in characterizing these lesions. The current study evaluated only patients with T1 lesions, and we determined that the number of false-negative interpretations of PET results in patients with newly diagnosed lung cancer is actually low (5%). In addition, there was no minimal size criterion for the nodules, which could have contributed to some of the false-negative PET scans. Three of the nine false-negative PET scans were of lesions 3.0–4.0 mm in diameter, one of which was not detected at CT and was an incidental finding in a resected lobe in a patient with synchronous lung cancer.
The exact size at which a pulmonary lesion is seen on PET images has not been clearly established and varies depending on a number of factors. Some investigators have suggested that PET does not depict small nodules because of limitations in spatial resolution, partial volume effects, and the paucity of tumor cells within small abnormalities (24). However, eight (73%) of the 11 nodules in this series that ranged in size from 5.0 to 8.0 mm in diameter (mean, 6.0 mm) were positive at PET.
Cell type also appeared to influence FDG uptake. Those cancers that can behave in a more indolent fashion, such as carcinoid tumors and bronchioloalveolar cell carcinoma, demonstrated less FDG activity than did other non–small cell lung cancers (2,4,17,18,25–27). It should be remembered, however, that 44% of the lesions that had negative PET scans were non–small cell lung cancers (ie, non–bronchioloalveolar cell carcinoma and non-carcinoid tumors), though they too tended to be biologically indolent.
Perhaps of greater concern is the importance of false-negative interpretations of low FDG uptake on PET scans and the possibility that a lung cancer will be interpreted as benign. Our data confirm results of previous studies and suggest that patients with a negative PET scan can be followed up with conventional imaging (eg, chest radiography or CT) to monitor any growth of the lesion. If the lesion remains stable over 2 years or resolves, then no further evaluation is necessary. If the nodule grows, then a biopsy should be performed. Results of the current study suggest that this type of close follow-up does not adversely affect patient outcome. All of the patients with a negative PET scan who subsequently proved to have lung cancer had stage IA disease, and, in fact, their survival was significantly better than the survival of those patients whose PET scans showed increased FDG uptake and who had immediate diagnosis and treatment. These data support the findings of previous studies that demonstrated patients with lesions with lower FDG uptake had longer survival than those with lesions with higher FDG uptake (28–31).
We recognize several potential limitations of this study. First, we assessed only those patients with histopathologically proved lung cancers who underwent a PET examination. Although we suggest follow-up of all patients with a pulmonary nodule and a negative PET scan, it is possible that lung cancer in some patients in our study who had a nodule and a negative scan has not yet been diagnosed. We do not believe this occurred in a large number of patients because these patients should have been identified in the follow-up period as having growing lesions. One may consider the lack of use of standard uptake ratios in this retrospective study as a second potential limitation. However, standard uptake ratios, activity ratios, and visual evaluation are each equally accurate methods of data analysis at FDG PET for differentiating malignant from benign focal pulmonary abnormalities (9). When standard uptake ratios are used in the determination of whether a nodule is malignant, nodules that have ratios greater than or equal to 2.5 are usually considered malignant (32). However, because mediastinal blood pool regions generally have a standard uptake ratio of about 2.0–2.5, the mediastinum provides a distinct reference point (9). Therefore, reliance on standard uptake ratios should not have created more accuracy. An additional limitation is that the true accuracy of PET in the identification of all small (<10 mm) nodules remains uncertain because many of these lesions are not evaluated with PET due to their small size. A prospective study evaluating all small nodules will be invaluable for establishing the true accuracy of PET in the detection of very small lesions that are commonly detected at CT.
In conclusion, our data show that the majority of patients with pathologically proved T1 lung cancer have a positive PET scan. False-negative PET scans were seen in only 5% of all such lesions and in only 3% of such lesions if the lesion was greater than 5 mm in diameter. The excellent long-term survival for patients with a negative PET scan who subsequently prove to have lung cancer suggests that these tumors behave indolently and supports the management decision to follow up such lesions with conventional imaging to determine interval tumor growth.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, E.M.M., E.F.P.; study concepts and design, E.M.M., E.F.P., J.E.H.; literature research, E.M.M., E.F.P.; clinical studies, E.M.M., E.F.P., S.S.; data acquisition, E.M.M., S.S.; data analysis/interpretation, all authors; statistical analysis, J.E.H.; manuscript preparation, E.M.M., E.F.P., J.E.H.; manuscript definition of intellectual content and editing, E.M.M., E.F.P.; manuscript revision/review and final version approval, E.M.M., E.F.P., J.E.H.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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