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Nuclear Medicine |
1 From the Departments of Radiology and Institute of Radiation Medicine (J.M.G., J.G.I., K.H.D., J.B.S.) and Nuclear Medicine (J.S.Y., J.K.C.), Seoul National University Hospital, 28, Yongon-Dong, Chongno-Gu, Seoul, 110-744, South Korea; and the Department of Diagnostic Radiology, Ewha Womans University Mokdong Hospital, Seoul, South Korea (H.Y.K.). Received August 27, 1999; revision requested October 7; revision received November 2; accepted November 10. Address correspondence to J.G.I. (e-mail: imjg@radcom.snu.ac.kr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Ten consecutive patients who underwent PET and subsequently were proved to have pulmonary tuberculoma were analyzed. Tuberculosis was proved histopathologically in eight by means of wedge resection or lobectomy (n = 7) or needle biopsy (n = 1) and in two by means of clinical follow-up for more than 2 years. PET scans were evaluated by using peak standardized uptake values. Computed tomographic (CT) and histopathologic findings also were reviewed.
RESULTS: Nine of 10 tuberculomas showed FDG uptake at PET, and the mean peak standardized uptake value was 4.2 ± 2.2 (SD). FDG uptake (range, 1.9–3.7) in lesions adjacent to main abnormalities was demonstrated in four patients. On CT scans, the mean of the longest nodule diameters was 21 mm ± 8, and there were some areas of branching linear opacities or satellite nodules that suggested pulmonary tuberculosis in seven patients. Histopathologic findings were chronic granulomatous inflammation with caseation necrosis (n = 7) and healed tuberculosis with aspergilloma (n = 1).
CONCLUSION: Pulmonary tuberculoma commonly causes an increase in FDG uptake. These results suggest that in geographic regions with a high prevalence of granulomatous lesions, positive FDG PET results should be interpreted with caution in differentiating benign from malignant pulmonary abnormalities.
Index terms: Lung, CT, 60.12112, 60.12115 • Lung, diseases, 60.2056, 60.236 • Lung, granuloma, 60.20 • Lung, nodule, 60.3221 • Lung, PET, 60.12163 • Tuberculosis, pulmonary, 60.236
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Results of recent studies have shown that positron emission tomography (PET) with the glucose analogue 2-[fluorine 18]fluoro-2-deoxy-D-glucose (FDG) can be used to differentiate benign from malignant focal pulmonary abnormalities, including solitary pulmonary nodules and focal pulmonary masses (1–7). Although variations in uptake are known to exist among tumor types, elevated uptake of FDG has been demonstrated in all cell types of lung cancer (8,9). The sensitivities and specificities of those studies vary 83%–100% and 67%–90%, respectively (4,7,9–11). However, FDG is not a cancer-specific agent, and it has been reported that benign diseases related mainly to infection or inflammation also can show intense uptake, which causes difficulty in differentiating uptake due to benign disease from uptake due to malignant disease (4,5,7,11,12). The purpose of this study was to describe findings of pulmonary tuberculoma at FDG PET.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Among the 150 patients, the diagnosis of pulmonary tuberculoma was established in 10 patients (10 men; age range, 40–64 years; mean age, 53 years); pulmonary tuberculoma was diagnosed in eight patients on the basis of histopathologic findings and in two on the basis of clinical follow-up. The histopathologic diagnosis included wedge resection (n = 5), lobectomy (n = 2), and fine-needle aspiration (n = 1). The criteria for clinical diagnosis were based on CT findings suggestive of pulmonary tuberculosis (branching linear structures, satellite nodules, or a well-defined nodule with central calcification) that subsequently improved with the use of antituberculous chemotherapy during the follow-up of more than 2 years. Therefore, they were considered to have active pulmonary tuberculosis.
PET was performed with a scanner (ECAT EXACT 47; Siemens-CTI, Knoxville, Tenn) that has an intrinsic resolution of 5.2 mm and can image 47 contiguous, 3.4-mm-thick planes simultaneously for a longitudinal field of view of 16.2 cm. All patients fasted for at least 12 hours prior to the study; by means of skin marks, they were positioned carefully for each scan to ensure identical fields of view for transmission and emission scanning. Before administration of FDG, transmission scanning of the whole body, extending from the neck to the thigh, was performed by using a germanium 68 rod source for attenuation correction. Emission scans were obtained 60 minutes after the injection of 10 mCi (370 MBq) of FDG. Additional regional scans of the thorax were obtained for 30 minutes to image suspicious lesions. The acquired data were reconstructed by using standard back-projection techniques. PET images (257 transverse, 128 coronal, and 128 sagittal) were reconstructed by using measured attenuation correction and were corrected for decay.
Posteroanterior chest radiographs and thoracic CT scans were used to localize the abnormality before PET was performed. A qualified nuclear medicine physician (J.S.Y., J.K.C.) who was unaware of pathologic results but was aware of CT findings interpreted the PET scans. Images were reviewed in transverse, coronal, and sagittal planes by using an interactive video display system (SPARC station 10; Sun Microsystems, Mountain View, Calif). Interpretation included the semiquantification of FDG uptake by using the peak standardized uptake value on the emission images obtained 46–56 minutes after injection of FDG. After visually finding an area of the highest FDG uptake, the physician outlined a region of interest on the area of highest uptake. A standardized uptake value normalized for injected dose and body weight was obtained in each pixel by using a previously described method (3–7,11): standardized uptake value = region of interest activity/(injected dose/body weight), where the region of interest activity is measured in millicuries per milliliter, the injected dose is measured in millicuries, and body weight is measured in grams. The maximum pixel value in the region of interest was chosen as the peak standardized uptake value. Lesions that had a standardized uptake value of 2.5 or more were considered potentially malignant (5–7,11).
CT examinations were performed with a Somatom Plus 4 (Siemens, Erlangen, Germany) or a HiSpeed Advantage (GE Medical Systems, Milwaukee, Wis) scanner. Eight-millimeter-thick spiral CT sections were obtained from the pulmonary apex to the adrenal glands in all 10 patients. In nine patients, 100 mL of iopromide (Ultravist 370; Schering, Berlin, Germany) was injected intravenously. Additional 1-mm-thick CT scans also were obtained in three of the 10 patients. Both mediastinal window (width, 400 HU; level, 10 HU) and lung window (width, 1,500 HU; level, -700 HU) scans were obtained. The number of nodules and the presence of satellite nodules were analyzed on chest radiographs. The diameter, margin, and location of the nodule; the presence of calcification in the nodule; the presence of satellite nodules; associated parenchymal change around the nodule; and mediastinal lymph node enlargement were assessed on CT images. Histopathologic findings obtained from transthoracic fine-needle aspiration (n = 8) or from surgical specimens (n = 7) were reviewed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Transthoracic fine-needle aspiration was performed in eight patients. In three patients, chronic granulomatous inflammation with caseation necrosis was seen at histologic examination, which was consistent with tuberculosis. In two of these three patients, wedge resection was performed because avid FDG uptake with standardized uptake values of 6.6 and 6.3 was observed at PET. The histologic findings at fine-needle aspiration in the remaining five patients were sheets of epithelioid cells and lymphocytes (n = 1), necrotic debris with scanty cells (n = 3), and a few macrophages (n = 1). Histopathologic findings in surgical specimens (n = 7) were chronic granulomatous inflammation with caseation necrosis (n = 6) and aspergilloma with fibrotic lesions and granuloma (n = 1), which was consistent with healed tuberculosis. In two of three cases in which Ziehl-Neelsen stain was used, acid-fast bacilli were found in the surgical specimens. Tuberculous lymphadenitis was found histopathologically in one patient.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Most solitary pulmonary nodules are benign (19); results from a surgical series showed that only one-third of solitary pulmonary nodules are bronchogenic carcinoma (20). Surgery is probably not warranted in the remaining two-thirds of solitary pulmonary nodules. Among these benign nodules, 54% are granuloma (20). The goals for imaging in patients with indeterminate pulmonary nodules are to distinguish between benign and malignant lesions in the least invasive way and to make a specific diagnosis.
FDG PET can demonstrate the glucose metabolism of a lesion, which can be helpful in differentiating between benign and malignant pulmonary lesions. Malignant cells demonstrate higher glucose metabolic activity than benign lesions do. A threshold standardized uptake value of 2.5 at FDG PET has been reported to provide optimal sensitivity (83%–100%) and specificity (67%–90%) in differentiating benign from malignant nodules in patients with solitary pulmonary nodules (4,7,9–11). However, by using this threshold, 90% of tuberculomas were false-positive for malignant nodules in our series. Only one tuberculoma, which was 8 mm in diameter, showed no identifiable FDG uptake. In South Korea, the prevalence of pulmonary tuberculosis on chest radiographs was 1.0% in 1995 (21). Our results substantiate that positive FDG PET results should be interpreted with caution in differentiating benign from malignant nodules, especially in patient groups with a high prevalence of tuberculosis.
Active granulomatous processes such as tuberculosis (5,7,12), fungal infections (4,11), and sarcoidosis (22) have been reported to accumulate FDG and cause PET scans false-positive for malignancy. However, most reported cases of uptake are in patients with lymphadenopathy, consolidation, or diffuse infiltrates, and the quantitative data concerning FDG uptake are available in only a few cases, to our knowledge. Knight et al (7) reported tuberculous pneumonia with a standardized uptake value of 9.3 and a tuberculoma with a standardized uptake value of 8.7. Gupta et al (11) reported that two granulomas with histoplasmosis showed FDG uptake with standardized uptake values of 1.92 and 3.38.
Granulomatous lesions are characterized by cellular infiltrates, granuloma formation, and macrophage proliferation. Activated inflammatory cells have markedly increased glycolysis, and the hexose monophosphate shunt is stimulated by phagocytosis, with increases of 20–30 times baseline values common in these stimulated cells (23). Even within tumors, the totality of FDG uptake is not completely within the tumor cells themselves. The newly formed granulation tissue around the tumor and the macrophages infiltrating heavily at the marginal areas surrounding the necrotic area of the tumor show a high uptake of FDG, and about 24% of the FDG concentration in a tumor mass is derived from nontumor tissue (24). FDG uptake is more rapid in inflammatory cells (25), and avid FDG uptake is the rule in inflammatory tissue, in which the uptake is predominantly in the cellular component. In tuberculosis, the cellular infiltrate is composed of lymphocytes and macrophages.
An experimental study on the tissue distribution of accumulated FDG in inflammatory tissue showed a maximum uptake was observed in the chronic phase, characterized histologically by chronic inflammation (26). Grain counting at microautoradiography of the abscess wall showed that the highest grain density was found in the marginal zone of young fibroblasts, endothelial cells of vessels, and phagocytes of neutrophils and macrophages (26). This suggests that macrophages and neutrophils in inflammatory tissue use glucose as an energy source for chemotaxis and phagocytosis, whereas fibroblasts use the same substance for proliferation.
In our series, FDG uptake (range, 1.9–3.7) within lesions adjacent to a main abnormality was demonstrated in four patients, and these areas of uptake correlated with the satellite nodules on CT scans. Lymph nodes that showed FDG uptake were found in three patients, and tuberculous lymphadenitis was demonstrated histopathologically in one. In one patient, FDG uptake was not identified in a pulmonary nodule, but the hilar lymph nodes showed uptake. We think that FDG uptake at PET can be considered indicative of active tuberculous lesions. Histopathologic findings suggested healed tuberculosis in one case, but the presence of aspergilloma may have caused the active inflammation.
In summary, our results show that tuberculomas can have increased FDG uptake at PET. FDG uptake within satellite lesions adjacent to a main abnormality or within lymph nodes also can occur. Therefore, positive results at FDG PET should be interpreted with caution in differentiating benign from malignant pulmonary abnormalities, especially in geographic regions with a high prevalence of granulomatous lesions.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, J.M.G., J.G.I., J.K.C.; study concepts, J.M.G., J.G.I., J.B.S.; study design, J.M.G., J.B.S.; definition of intellectual content, J.M.G., J.G.I., J.K.C.; literature research, J.M.G., K.H.D., H.Y.K.; clinical studies, J.M.G., J.G.I., K.H.D., J.B.S., J.S.Y., J.K.C.; data acquisition, K.H.D., J.S.Y., J.M.G.; data analysis, J.M.G., K.H.D., H.Y.K.; manuscript preparation, J.M.G., J.B.S.; manuscript editing, J.M.G., J.S.Y., J.G.I.; manuscript review, J.G.I., J.M.G., J.S.Y., H.Y.K., J.K.C.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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