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Eur J Cardiothorac Surg 2001;20:324-329
© 2001 Elsevier Science NL

Validation of FDG positron emission tomography for differentiation of unknown pulmonary lesions

^a Department of Thoracic Surgery, Universitätsklinikum Freiburg, Hugstetterstrasse 55, D-79106 Freiburg, Germany
^b Department of Radiology, Division of Nuclear Medicine, University of Freiburg, Freiburg, Germany

Received 11 October 2000; received in revised form 8 May 2001; accepted 14 May 2001.

Corresponding author. Tel.: +49-761-2702401; fax: +49-761-2702499
e-mail: imdahl{at}chir.ukl.uni-freiburg.de

	Abstract

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A. Conference... References

 
Objective: The impact of the (2-(fluorine-18)-fluoro-2-2deoxy-D-glucose)-positron emission tomography (¹⁸F-FDG-PET) for discrimination of pulmonary lesions was evaluated in a single centre prospective study. Methods: In the study, 109 patients with pulmonary lesions of unknown origin verified by computed tomography were enrolled consecutively (April 1999–May 2000). They were subject to ¹⁸F-FDG-PET diagnostics. ¹⁸F-FDG-PET images were interpreted by two independent nuclear medicine physicians who were blinded to the results of other imaging procedures. In 87 patients, surgery was applied followed by histological investigation, which served as the gold standard. In 22 other patients, extensive tumour load or assumed benign dignity of the lesions prevented surgery. Results: Overall sensitivity of ¹⁸F-FDG-PET in 87 resected patients was 0.86. Differentiation in malignant (n=69) and benign lesions (n=18) revealed sensitivities of 0.9 and 0.72, respectively. Sensitivity of ¹⁸F-FDG-PET in inflammatory lesions was markedly lower (0.43) than in benign tumours (0.91). Standard uptake values were significantly increased in malignant tumours compared with benign lesions (9.9 and 1.6, respectively; P=0.035). There was a clear correlation of sensitivity with tumour size with a failure rate of 27% in lesions 1 cm (n=15), 10% (n=20) in lesions between 1 and 2 cm and 12% (n=45) above 2 cm. In primary bronchial carcinoma, a clear correlation of sensitivity was observed with regard to tumour grading (G1, three out of five; G2, 24 out of 27; G3, 26 out of 26; and G4, one out of one). Lymph node involvement was correctly suggested in 10 out of 19 (52.6%) patients. However, false positive lymph node enhancement was indicated in one out of 18 (5.5%) operated patients with benign lesions and eight out of 39 (20.5%) with bronchial carcinoma. Conclusion: ¹⁸F-FDG-PET at present does not serve as the gold standard for early detection of small and well-differentiated tumours. However, it contributes efficiently to the detection of malignancy in tumours >1 cm, which are moderately or poorly differentiated. Positive lymph node imaging must not preclude surgery but requires histological proof. Discrimination of benign and malignant pulmonary tumours by ¹⁸F-FDG-PET appears to be hampered in inflammatory lesions.

Key Words: Pulmonary lesion • FDG-PET • Tumour grading • Tumour size

	1. Introduction

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A. Conference... References

 
Pulmonary focal lesions are frequently diagnosed incidentally. It has been estimated that 30–50% of these pulmonary lesions are malignant; this rate increases even further in a previous history of malignancy of the patient [1]. For treatment strategy, the dignity of the lesions needs to be clarified before therapy [2]. In benign lesions operative procedure may be postponed or a less-invasive procedure may be applied. However, all non-invasive diagnostic procedures lack specificity and sensitivity with regard to the potential malignancy of the lesion [3]. Computed tomography (CT) is a sensitive imaging technique but cannot prove malignancy. In multiple series, 25–40% of malignant nodules were misclassified as benign [4]. In some cases ultrasound- or CT-guided fine-needle aspiration may clarify the malignant nature of the lesion, but this may be misleading in negative findings [5]. Bronchoscopy with transbronchial biopsy in peripheral lesions under fluoroscopy is very helpful, but can fail to achieve a reliable histology. Frequently, video-assisted thoracoscopy or thoracotomy are needed for diagnosis and will serve as treatment at the same time. However, operative strategies bear some risk and are expensive.

The advent of (2-(fluorine-18)-fluoro-2-2deoxy-D-glucose) positron emission tomography (¹⁸F-FDG-PET) has made it possible to demonstrate sites of increased glycolysis due to cancer [6,7]. It has been shown that ¹⁸F-FDG-PET is a useful, non-invasive technique for observing changes of tumour metabolism after chemotherapy [8] or for distinguishing chronic inflammation from cancer [9,10]. The glucose analogue FDG is supposed to enter the cell in the same manner as glucose. However, in contrast to glucose, it is trapped within the cell after phosphorylation, as it is not further metabolized. Therefore, intracellular FDG concentration reflects intracellular glucose metabolism [11].

The purpose of this prospective non-randomized investigation was to evaluate the clinical impact of ¹⁸F-FDG-PET for the differentiation of benign and malignant pulmonary lesions. The obtained results were compared with histology in operated patients and with other imaging procedures in conservatively treated patients.

	2. Materials and methods

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A. Conference... References

 
2.1. Patients
In this study, 109 patients with pulmonary lesions of unknown origin verified by CT were subject to ¹⁸F-FDG-PET. Of these, 33 revealed a history of a previous malignant disease (eight bronchial carcinoma, 25 extrapulmonary cancer). Before application of ¹⁸F-FDG-PET bronchoscopy, transbronchial biopsy and/or fine-needle aspiration (n=43) failed to confirm a reliable diagnosis, apart from four patients in whom malignancy was proven before ¹⁸F-FDG-PET. Mean age of the 76 men and 33 women was 61 years (range 26–86 years). Patients were enrolled consecutively between April 1999 and May 2000. All but two patients received ¹⁸F-FDG-PET of the thorax and the upper abdomen, two patients received a whole body investigation. Patients were informed about the study and gave written consent. In 22 patients, operation was not performed due to extensive tumour load, functional inoperability or apparent benign disease. In 87 patients, operation was performed later on. Histology of the resected specimen was correlated with PET findings.

2.2. PET protocol
The isotope and the radiopharmaceutical were produced and synthesized as previously reported by Wieland et al. [12]. ¹⁸F-FDG-PET investigation was performed at least 6 weeks after the last chemotherapy or more than 3 months after the completion of radiotherapy in patients with a previous malignancy.

After a 12-h fasting period, 5 MBq FDG/kg body weight were injected into a peripheral vein. Plasma glucose concentrations were measured prior to FDG injection. In eight patients, an elevated fasting plasma glucose level (>6.0 mmol/l) was normalized using fast-acting insulin (1 unit/0.5 mmol/l glucose) before FDG injection. Patients rested during the 90 min of FDG uptake. Static whole body ¹⁸F-FDG-PET imaging was performed with an ECAT-EXACT 921/31 tomograph (distributed by Siemens, manufactured by CTI, Knoxville, TN, USA). Coronal, sagittal and transaxial images were produced as described elsewhere [13].

2.3. Image interpretation
The images were reviewed on hard copy and on a computer workstation (SUNSparc 20; SUN Microsystems, Palo Alto, CA, USA). The PET images were interpreted by two experienced independent investigators, who were blinded to clinical data and results of other imaging procedures. Lesions were identified and subjectively characterized in relationship to normal anatomy and surrounding tissue uptake. For semiquantitative evaluations of FDG uptake, regions of interest (ROI) were defined around suspicious FDG accumulations in transaxial slices. The maximum counts in a selected ROI were chosen for calculation of standard uptake values (SUV) [14]. A lesion was classified as potentially malignant by (a) a focally increased radiotracer uptake which exceeded normal limits of regional uptake in the respective area, or (b) an SUV greater than 4. This cut-off criterion is based on a prolonged uptake period of the radiopharmaceutical prior to the delayed image acquisition which enabled an improved lesion-to-background ratio [15]. In case of disagreement about the nature or the location of a lesion, a consensus was achieved and this interpretation was used to determine the overall PET performance.

Results of ¹⁸F-FDG-PET were correlated with the histology of the resected specimen. For comparison of SUVs in benign and malignant lesions, Student's t-test was used. A P-value <0.05 was considered as statistically significant.

2.4. Further diagnostic procedures
All procedures were performed routinely. CT of the chest and of the upper abdomen had been performed prior to the ¹⁸F-FDG-PET either at our hospital or at other institutions. CT was performed according to standard protocols. The criteria used for assessment of pulmonary lesions, lymph nodes and adrenal glands have been described elsewhere [16]. Image interpretation was not performed under study conditions. CT scans were evaluated by the thoracic surgeons. Patients who had had no bronchoscopy prior to the ¹⁸F-FDG-PET because of small size and subpleural location underwent either rigid or fibre-optic bronchoscopy before resection.

	3. Results

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A. Conference... References

 
As histology served as gold standard for correlation with PET findings, results of operated patients only are presented (n=87). True positive (true negative) findings of ¹⁸F-FDG-PET were observed in 76 (87) patients, false negative (false positive) findings in 11 (87) investigations. Overall sensitivity of ¹⁸F-FDG-PET in patients with malignant (benign) lesions was 0.9 (0.72) (Table 1). There was no correlation with age or gender of the patients. SUVs were significantly higher in malignant lesions compared with benign lesions (P=0.035; Table 2).

In 58 out of 62 patients, ¹⁸F-FDG-PET indicated correctly a malignant disease. A false negative result was obtained in two out of 25 adenocarcinomas (8%), one out of 11 alveolar cell carcinomas (9%) and one out of 18 squamous cell carcinomas (5.5%). Among seven patients with metastases from extrapulmonary cancer, four were correctly detected by the ¹⁸F-FDG-PET (Fig. 1a ). SUVs were increased in primary pulmonary cancer compared with metastatic disease (10.14 vs. 4.38; P=0.14). Differences of SUV between squamous cell carcinoma (n=18; mean 20.49), adenocarcinoma (n=25; mean 7.51), large-cell carcinoma (n=5; mean 11.0) and bronchioloalveolar cell carcinoma (n=11; mean 9.09) in primary bronchial carcinoma were not significant.

View larger version (82K): [in this window] [in a new window]   Fig. 1. (a) Correct indication of a malignant lesion by the 18F-FDG-PET (four coronal slices) in a patient with a previous history of rectal cancer with liver metastases, which was resected some weeks earlier. 18F-FDG-PET indicated one more lesion as observed in CT (SUV 11.74). (b) Indication of a malignant lesion by the 18F-FDG-PET, which was also suggested by CT in a 53-year-old woman with a history of smoking. However, histology revealed after lobectomy pulmonary sarcoidosis (SUV 3.39). Later on, this diagnosis was reversed by the pathologist to tuberculosis due to PCR results.

An increase of tumour size as obtained by pathology (available in 66 specimens, mean 3.0 cm, range 0.6–8 cm) led to an increase in sensitivity of ¹⁸F-FDG-PET: seven out of 11 (64%) in tumours 1 cm, 15 out of 16 (94%) in tumours >1 cm and 2 cm; and 37 out of 39 (95%) in tumours >2 cm.

Tumour spread into lymph nodes was detected in 18 out of 62 patients with a primary pulmonary carcinoma and in one patient with a teratocarcinoma. There was pN1 disease in six, pN2 in 11 and pN3 in one patient, respectively. In 10 of them ¹⁸F-FDG-PET indicated lymph node involvement; however, it missed lymph node involvement in 10 patients. On the other hand, ¹⁸F-FDG-PET suggested malignant lymph node involvement incorrectly in one out of 18 patients with benign lesions and in eight out of 39 patients with a bronchial carcinoma.

Seven of 18 operated patients with a previous history of extrapulmonary cancer revealed a metastatic lesion (one thymus carcinoma, two breast cancer, one renal cell cancer, one Hodgkins disease, two colorectal cancer). In four of them (two colorectal cancer, one renal cancer, one Hodgkins disease) ¹⁸F-FDG-PET led to a correct suggestion of a benign lesion. Eleven patients suffered from a secondary bronchial carcinoma (¹⁸F-FDG-PET correct in all).

3.2. FDG-PET findings in benign lesions
A benign lesion was observed in 18 out of 87 patients (lobectomy in five and segmental or wedge resection in 13 cases). Seven of them had an inflammatory lesion whereas 11 patients had benign neoplasms.

In 14 out of 18 patients with a benign lesion, ¹⁸F-FDG-PET suggested a non-malignant lesion, but in four out of 18, a malignant lesion was incorrectly indicated (Fig. 1b). Differentiation of benign tumours (n=11) and inflammatory disease (tuberculoma (n=4), pulmonary sarcoidosis (n=1), sequestration (n=1), bronchiectasis (n=1)) showed a worse sensitivity in the latter (0.91 vs. 0.43).

An increase of tumour size as obtained by pathology (available in seven specimens, mean 2.8 cm, range 0.8–9.5 cm) led to a reduction of sensitivity of ¹⁸F-FDG-PET in benign lesions: four out of four in lesions <1 cm, three out of four in tumours <1 and <2 cm, and three out of six in tumours >2 cm.

	4. Discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A. Conference... References

 
Solitary pulmonary coin lesions are identified in some 130,000 patients/year in the US [1]. Radiographic evaluation is often performed with chest CT. However, frequently it is difficult to estimate from the image whether the lesion is likely to be malignant or non-malignant. In a lesion which is unlikely to be malignant, it may be justified to observe the patient for some weeks to detect a change of diameter before operation is planned. This holds especially true in patients at high surgical risk. On the other hand, many patients presenting with solitary pulmonary lesions are at high risk for cancer either because of a history of smoking (primary bronchial carcinoma) or because of a previous extrapulmonary malignancy (metastases). For the operative strategy it is of great help to know about the dignity of the lesion. In a non-malignant-appearing peripheral lesion a video-assisted approach may be chosen, but in a malignant-appearing lesion a thoracotomy is preferred.

The advent of the ¹⁸F-FDG-PET provides the opportunity to detect malignant lesions in the whole body with one investigation due to the metabolic activity of the neoplastic cells. Malignant cells show an increased glucose turnover compared to normal tissue. This increased glycolysis is caused by an enhanced glucose transporter expression, an increased transmembrane transfer of glucose and an increased hexokinase activity [11]. However, the increased glucose metabolism is not specific for malignant cells, but also observed within inflammatory tissue [17]. The relevance of ¹⁸F-FDG-PET imaging has been shown in various other tumours and tumour recurrences [6,7]. The purpose of this study was to evaluate the impact of ¹⁸F-FDG-PET for the discrimination of unknown pulmonary lesions.

The usefulness of the ¹⁸F-FDG-PET for differentiation of benign and malignant pulmonary lesions has been investigated in various studies [3,18–20,25,26]. The reported sensitivity and specificity of the ¹⁸F-FDG-PET ranges between 0.75 and 1.0. SUVs were significantly increased in malignant lesions compared to benign lesions [21], but a clear cut-off level for discrimination of benign and malignant pulmonary lesions does not exist. The differences in absolute values compared with the presented results may be explained by different uptake times. However, with regard to SUV indices, our results indicate that delayed image acquisition does not improve differential diagnosis between cancer and benign lesions based upon semiquantitative evaluation. Therefore, SUV continues to represent a matter of dispute.

We observed some false negative findings by ¹⁸F-FDG-PET in our series in primary bronchial carcinomas. The false negative results may be explained by grading or small size of the tumours. Size was reported in some studies to be a factor responsible for false negative indications of ¹⁸F-FDG-PET in tumours smaller than 1.2 cm. All seven of the 67 lesions reported as false negative have been <1.2 cm in diameter [3]. However, in another study, no differences of sensitivity of the ¹⁸F-FDG-PET have been observed between tumours >1.5 cm and tumours between 0.7 and 1.5 cm [23]. Tumour grading is probably related to the activity of the metabolism and, therefore, in low grading tumours, accumulation of FDG was not detected. However, whether well-differentiated tumours exhibit a lower glucose turnover than less-differentiated tumours leading to a better detection by ¹⁸F-FDG-PET in the latter remains a matter of speculation.

In primary bronchial carcinoma, false negative ¹⁸F-FDG-PET scans have been reported to occur in carcinoid tumours and in bronchoalveolar cell cancers [1,22]. We observed only one false negative result in 11 patients with bronchoalveolar cell cancers.

Interestingly, overall sensitivity of the ¹⁸F-FDG-PET was reduced in seven patients included with pulmonary metastases. This probably correlates to the metabolic activity of the individual metastases. Further on, there seems to be a relation to the primary malignancy. Usually, high FDG accumulation has been observed in metastases of melanoma or colorectal cancer [3], whereas FDG accumulation has appeared to be low in metastases of renal cell carcinoma or thyroid cancer [20]. In another study ¹⁸F-FDG-PET has shown pulmonary metastases of colorectal cancer for the first time in 6.5% of the investigated patients [10]. Seven out of 45 malignant lesions were not detected by ¹⁸F-FDG-PET; all of them turned out to be metastatic lesions due to extrapulmonary cancer [3]. Therefore, for the interpretation of an ¹⁸F-FDG-PET scan, the type of primary tumour should be considered in lesions with low FDG uptake and a previous history of extrapulmonary cancer.

False positive PET scans deserve special attention. Most of these false positive findings are related to inflammatory lesions rather than true benign tumours such as harmatomas. Inflammatory lesions such as tuberculoma, histoplasmosis [24], abscesses, sarcoidosis [3] or necrotizing granuloma [26] have been reported as false positive results. Therefore, in patients suspected of inflammatory disease or with bilateral positive ¹⁸F-FDG-PET findings, a false positive result may be considered. The one false positive result in a patient with a harmatoma was possibly caused by some inflammatory reaction of the surrounding pulmonary tissue.

A typical example of a false positive ¹⁸F-FDG-PET finding is given in Fig. 1b, presenting a 53-year-old woman with a history of smoking. As CT scan and ¹⁸F-FDG-PET scan suggested malignancy, an upper lobectomy was performed, but histology revealed a pulmonary sarcoidosis as first line. Later on, this diagnosis was reversed by the pathologist to atypical tuberculosis due to PCR results.

The results of ¹⁸F-FDG-PET in this study with regard to lymph node involvement in malignant lesions were disappointing. This is contrary to some studies which investigated mediastinal lymph nodes containing malignancy, suggesting that FDG-PET was more accurate than CT. The ranges of sensitivity, specificity and accuracy were 66–100, 81–100 and 80–100%, respectively [1]. Several reasons may explain our results. The presented study was not designed for staging of proven bronchial carcinomas but for pulmonary lesion of unknown origin. In contrast to the cited results, which have been obtained as results of specially designed studies, the data presented in this study can be regarded as results of routine investigation. Further on, correct indication of ¹⁸F-FDG-PET may be dependent on lymph node stage. In seven out of 10 false negative results, lymph nodes were involved in the N1 position localized next to the lesion. Because of the close neighbourhood of the primary tumour and N1 regional lymph nodes, intense activity spill over may frequently disclose separate detection of both lesions resulting in a single hot spot. As the rate of false positive lymph node involvement indicated by ¹⁸F-FDG-PET was rather high in patients with bronchial carcinoma (25%), PET positive lymph nodes will not preclude surgery but will require surgical proof.

In conclusion, ¹⁸F-FDG-PET at present does not serve as the gold standard for early detection of small and well-differentiated tumours. However, it contributes efficiently to the detection of malignancy in tumours >1 cm, which are moderately or poorly differentiated. Positive lymph node imaging must not preclude surgery but requires histological proof. Discrimination of benign and malignant pulmonary tumours by ¹⁸F-FDG-PET appears to be hampered in inflammatory lesions.

	Footnotes

 
Presented at the 14th Annual Meeting of the European Association for Cardio-thoracic Surgery, Frankfurt, October 7–11, 2000.

	Appendix A. Conference discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A. Conference... References

 
Dr A. Lerut (Leuven, Belgium): I would just like to go back to your last slide where you had an algorithm with PET. Shouldn't you not do PET plus CT? As far as I understand, you are always performing CT as well, right?

Dr A. Imdahl: I agree. Of course.

Dr Lerut: Because I think the combination of the two will probably help you even more in getting more accurate and specific.

Dr Imdahl: I think you are absolutely right, but we could not calculate our CT results because CT scans, not all of them, were performed in our hospital. Patients usually come and bring a CT scan from different practitioners and therefore we couldn't correlate it.

Dr D. Van Raemdonck (Leuven, Belgium): We know from previous studies that carcinoids have low SUV. Were there any carcinoids in this series and, if so, did you classify them as benign lesions or as malignant lesions?

Dr Imdahl: I think I would put them in the malignant lesions, but unfortunately we had no carcinoids in this series. But I agree. I know that there are some data published that carcinoids are a problem, that's true.

Dr Van Raemdonck: Did you say these are benign lesions?

Dr Imdahl: No, I would say that they are malignant lesions.

Dr J. Thorpe (Leeds, UK): One of the main advantages of PET scan is to find lesions outside the thorax. Did you find any surprise lesions outside the chest?

Dr Imdahl: I didn't talk about the 22 patients treated conservatively. There were a few patients with lesions of the adrenals as well. But I can't tell you the exact figure as to how many patients in which we did not know of the lesion before.

	References

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