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Ann Thorac Surg 1999;67:790-797
© 1999 The Society of Thoracic Surgeons

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Original Articles

Evaluation of fluorine-18-fluorodeoxyglucose whole body positron emission tomography imaging in the staging of lung cancer

^a The Clinical PET Centre, United Medical and Dental Schools of Guy’s and St. Thomas’ Hospitals, London, England, UK
^b Department of Cardiothoracic Surgery, United Medical and Dental Schools of Guy’s and St Thomas’ Hospitals, London, England, UK

Accepted for publication July 24, 1998.

Address reprint requests to Dr Saunders, Dept of Nuclear Medicine and Ultrasound, Bankstown Lidcombe Hospital, Eldridge Rd, Bankstown, NSW Australia

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Background. Surgical resection of lung cancer remains the treatment of choice in appropriately staged disease, but conventional imaging techniques have limitations. Positron emission tomography (PET) may improve staging accuracy.

Methods. We studied whole body and localized thoracic PET in staging lung cancer. Standardized uptake value was calculated for the primary lesion. Ninety-seven patients under consideration for surgical resection were included. PET, computed tomography, and clinical staging were compared to stage at operation, biopsy, or final outcome. Mean follow up was 17.5 months.

Results. PET detected all primary lung cancers with two false-positive primary sites. Sensitivity and specificity for N2 and N3 mediastinal disease was 20% and 89.9% for computed tomography and 70.6% and 97% for PET. PET correctly altered stage in 26.8%, nodal stage in 13.4%, and detected distant metastases in 16.5%. PET missed 7 of 10 cerebral metastases. PET altered management in 37% of patients. PET staging (p < 0.0001) and standardized uptake value (p < 0.001) were the best predictors of time to death apart from operative staging.

Conclusions. PET provides significant staging and prognostic information in lung cancer patients considered operable by standard criteria. Routine use of PET will prevent unnecessary operation and may be cost effective.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Lung cancer is one of the most common fatal tumors with an incidence of approximately 32,000 new cases per annum in England [1]. The Thames Cancer Registry (South-Eastern England) quote a rate of 49.67 per 100,000 in men and an increasing rate of 21.24 per 100,000 in women (Thames Cancer Registry, personal communication, 1993). Surgical resection remains the treatment of choice in appropriately staged disease but conventional imaging techniques all have limitations.

Computerized tomography (CT) and magnetic resonance imaging provide excellent anatomic information; however, they have limitations differentiating benign and malignant lesions. Reliance on size criteria results in difficulty in the assessment of malignant lymph node involvement by CT and magnetic resonance imaging [2, 3]. Normal-sized lymph nodes may contain metastases, whereas enlarged lymph nodes may be attributable to benign causes. Staging CT normally extends from the base of the neck to the level of the adrenals and therefore, distant metastases may be missed. Additional staging investigations may include a bone scan and cerebral CT scan in stage II or III disease [4]. If a patient is considered fit for lung resection it is important that any apparent contraindication to resection is proved, as false positives are common in staging investigations.

Mediastinoscopy is the accepted standard for staging of the mediastinum, although a recent study by the Canadian Lung Oncology Group [5] suggested that the use of CT in comparison with mediastinoscopy in all patients produced fewer unnecessary thoracotomies. Mediastinoscopy has been recently shown to have a sensitivity of 72%, specificity of 100%, and accuracy of 89% [6], although previous reports quote up to 91% sensitivity [7]. It is an invasive procedure and has recognized morbidity.

Positron emission tomography (PET) with fluorodeoxyglucose (FDG) may overcome some of the limitations of conventional staging of lung cancer. Malignant cells are characterized by higher glucose consumption than normal cells and FDG is a useful marker of this metabolism. PET imaging using FDG labeled with the positron emitter fluorine-18 provides useful information to differentiate benign from malignant lesions in the lung [8]. It has been suggested that whole body FDG PET can improve the diagnostic accuracy in the staging of non-small cell lung cancer particularly in assessing mediastinal lymph node involvement [9–12]. Whole body PET imaging also permits detection of distant metastases without any further increase in radiation exposure to the patient. This ability to define both local and distant disease has been shown to significantly alter management in patients with non-small cell lung cancer [13], and may prove to be the most cost-effective first-line imaging in staging of lung cancer [14].

We aim to assess the impact and prognostic significance of PET scanning in the staging of patients with lung cancer who were considered operable and referred to a cardiothoracic surgeon.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
All patients referred to one surgeon for the consideration of resection for lung cancer in the period were studied. Ninety-seven patients were studied from November 1992 to July 1995. Follow-up continued to July 1996.

Entry criteria included (1) biopsy proved lung cancer (n = 84) or strong suspicion of cancer on clinical and CT criteria (n = 13); and (2) operability by clinical and CT staging with TNM stage 3a or less or equivocal evidence on other imaging of metastatic disease.

Imaging
Computerized tomography
The CT scans were performed at 10 referring hospitals. All were considered acceptable within current clinical practice. Two experienced observers reported CT scans. Discordance was resolved by a third experienced observer. Grading of lymph node involvement was based on size; nodes of less than 1 cm in the short axis on CT being classified as benign. Stage by CT criteria was recorded using consensus TNM stage definitions [16]. N2 disease was defined as metastasis to the ipsilateral mediastinal lymph nodes and subcarinal lymph nodes. N3 was defined as metastasis to contralateral mediastinal or hilar lymph nodes or ipsilateral or contralateral scalene or supraclavicular lymph nodes.

Positron emission tomography
18-Fluorine was produced in the Siemens RDS 112 cyclotron facility on site at The Clinical PET Centre. Imaging was performed on an ECAT 951/31R system (Siemens CTI, Knoxville, TN). Patients were instructed to fast for 6 hours before the study and baseline blood glucose level was recorded. Then, 350 MBq of FDG was injected intravenously and thoracic emission data acquired at a mean time of 81 minutes after injection. The scan protocol consisted of a half body scan acquired from the brain to mid-thigh followed by localized views of the thorax in all but 5 patients. A transmission scan using a germanium-68 source was obtained for attenuation correction of the thoracic images. Thirty-nine patients scanned in 1993 to 1994 had localized thoracic views performed before the half body study (45 minutes after injection). The spatial resolution of localized attenuation corrected thoracic images was 13 mm.

Images were reconstructed and viewed in transaxial, coronal, and sagittal slices on a SUN (Sun Microsystems, Palo Alta, CA) workstation and prospectively reported by two nuclear physicians blinded to patient history and outcome. Discordant reports were resolved by consensus or by a third reporter. The standardized uptake value (SUV) was calculated for each abnormal lesion identified in the attenuation corrected chest image; if the abnormality was less than 10 mm then an SUV was not recorded. Abnormal uptake in the mediastinum or hilar nodes was defined as an area of uptake greater than the surrounding tissue uptake. One observer positioned an 8-mm region of interest over the maximum pixel in the lesion and the average of two perpendicular diameters of the lesion was recorded. The SUV was calculated by the standard equation: the tissue concentration of FDG measured by PET was divided by the injected dose divided by body weight [16]. Primary lung lesions with an SUV of less than 2.5 were considered benign, nodal disease if of sufficient size used the same criteria.

Staging
Patients were staged by the consensus TNM stage definitions [15] based on CT alone, by clinical (physical examination, full hematologic screen, biochemical screen, and bronchoscopy) and CT criteria, and by PET.

Confirmation of stage and outcome
All patients were registered with the Thames Cancer Registry and tagged by the Office of National Statistics who notifies all deaths to the cancer registry. Final outcome was based on surgical findings, histopathology, and clinical follow-up. Bronchoscopy, transthoracic fine needle biopsy, or thoracotomy achieved proof of histology of the primary lung lesion. Confirmation of presence or absence of mediastinal metastases was achieved by biopsy at mediastinoscopy or thoracotomy (n = 84) in those with proved carcinoma. The remaining 13 patients had distant metastases confirmed by other means (biopsy, CT, follow-up). Mean length of follow-up was 17.5 months (range, 12 to 41 months). Median follow-up was 15 months.

Distant metastases were confirmed by biopsy in 9 patients. In 8 patients biopsy of abnormal PET sites was not feasible and follow-up imaging confirmed metastases at the previously suspicious site or negative imaging and absence of clinical disease 24 months after PET imaging was accepted as evidence against metastases.

Data analysis
Results of CT and PET scans were compared with the final diagnosis to determine diagnostic specificity, sensitivity, and accuracy of staging the mediastinum. Univariate analysis using Cox regressions for standard variables was used to correlate main variables (age, sex, SUV, clinical stage, CT stage, stage at operation, PET stage) and time to death. Multivariate analysis was also performed. A p value of less than 0.05 was considered significant. Hazard ratios were calculated. Kaplan Meir survival estimates were performed for CT stage, stage at operation, and PET stage.

	Results

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Ninety-seven patients (64 men) were included in the study. The mean age was 63.3 years (range, 36 to 77 years). There was histologically proved malignancy in 84 patients before PET imaging, whereas 13 had suspicion of cancer, which was subsequently proved in 11. Histologic subtypes are summarized in Table 1.

There were three (two in retrospect) false-positive PET scans of the primary site. Two benign lesions had FDG uptake; a right hilar mass in an asbestos worker and low level uptake (SUV = 4.5) in a new lung lesion in a previously healthy man. Biopsy revealed pneumoconiosis (24 months follow-up) and in the second patient mycobacterial infection was confirmed and treated (30 months follow-up). The final benign lesion had histology from fine needle aspiration confirming malignancy (SCC); however, open biopsy of the lesion in the lingula revealed granulomatous inflammation. The initial PET reported uptake near the heart; however, on retrospective analysis no discrete lesion was seen.

Mediastinal staging
Eighty-four patients had mediastinal sampling at mediastinoscopy or thoracotomy. We compared the ability of CT and PET to detect N2 and N3 (supraclavicular nodes) disease. Sensitivity, specificity, and accuracy for CT were 20%, 89.9%, and 77.4% and for PET were 70.6%, 97%, and 91.6%, respectively (Table 2). PET reduced false-negative and false-positive rates compared to CT improving sensitivity, specificity, and accuracy. Figure 1 is an example of falsely negative mediastinal disease on CT. Low CT sensitivity is partly explained by selection criteria bias as patients with mediastinal adenopathy on CT scan were excluded. All patients (n = 5) that had false-negative nodal disease on PET were also negative on CT. The two false-positive PET patients had normal-sized lymph nodes on CT: one due to pneumoconiosis and the second had low level axillary lymph node uptake that was related to a recent flu injection (but this patient had another site of distant metastasis shown on PET and confirmed in the contralateral lung on repeat CT).

View larger version (82K): [in this window] [in a new window]   Fig 1. Fluoride-18-fluorodeoxyglucose study detected the right mid-zone primary with further foci in the right paratracheal region (A), and in a mid-thoracic vertebral body (B). Transaxial computed tomographic scan (C) demonstrated a large right hilar mass involving the right upper lobe bronchus with a plane of cleavage between the tumor and the ascending aorta, the superior vena cava, and the pericardium. This image (C) demonstrates small lymph nodes in the mediastinum, which are less than 1 cm, and by computed tomographic criteria are negative for malignancy. No other abnormality was seen on the computed tomographic scan.

View larger version (89K): [in this window] [in a new window]   Fig 2. Fluoride-18-fluorodeoxyglucose study with uptake in the primary right lung carcinoma and right adrenal bed in the coronal section (A). Fine needle biopsy of the right adrenal was negative and the patient underwent thoracotomy and excision of the primary. A follow-up positron emission tomographic study 3.5 months later demonstrates growth of the right adrenal metastasis and local recurrence (B). Computed tomographic scan showed no abnormality in the right adrenal but confirmed a right lung primary.

Management was altered by the PET study in 37% (36 of 97 patients); 6 required further investigation, 15 had planned operation canceled, 11 had operation enabled due to the exclusion of distant metastatic disease or local mediastinal nodal spread (n = 11), and 4 patients had operation enabled as the diagnosis was established. The benefit was greater in patients without confirmation of malignancy before PET.

At the end of the follow-up period 46 patients were alive and disease free. Of these patients PET predicted stage 0 to 2 disease in 82.6% (38 of 46 patients), stage 3 disease in 4, and stage 4 disease in 4 patients. PET stage 4 disease was confirmed at biopsy in 2 patients who remain alive. Six patients were alive but had recurrent disease. Preoperative PET detected higher stage disease in 2 patients. Three patients developed cerebral metastases (from 6 to 14 months) and one bone metastases after 12 months.

Forty-five patients died; 38 from disseminated malignancy and 7 from other causes (ischemic heart disease, pneumonia, second malignancy after operation). PET stage was greater than stage 3a in 44.7% (17 of 38 patients) of lung cancer deaths over the study period and in 59.3% (16 of 27) in the first 12 months after operation. There were 21 deaths from lung cancer with PET stage 2 or less, 11 occurred within the first 12 months. Eleven lung cancer deaths occurred more than 18 months after PET (mean, 23.4 months; range, 18 to 34 months); 10 had PET stage 2 or less. Ten patients developed documented cerebral metastases and 3 were detected by PET. Twelve-month mortality rates subdivided by TNM staging at baseline, PET, and operation are summarized in Table 5.

	Comment

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
A recent consensus statement from the American Thoracic Society and European Respiratory Society [17] on the pretreatment evaluation of non-small cell carcinoma of the lung suggests that PET is in its early stages of development and not readily available outside academic centers and therefore, at present, has little role to play in the management of this group of patients. This contrasts heavily with the suggestion by Gambhir and colleagues [14] that incorporation of PET into an assessment of these patients is extremely cost effective. Our findings support the view that: (1) 18-F FDG PET detected all primary tumors and differentiated N2 and N3 mediastinal involvement with a higher sensitivity, specificity, and accuracy than CT in our selected population; (2) PET detected unsuspected distant metastases in 16.5%; (3) PET staging and SUV were the best noninvasive prognostic indicators of time to death; and (4) PET findings altered management in 37% of patients.

FDG PET detected all primary lung cancers, which is a similar finding to other reports of up to 100% sensitivity in detecting malignant lung lesions [9]. Absent FDG uptake at the site of CT abnormality is good evidence against malignancy. There were two false-positive PET scans at the primary site; therefore, histologic confirmation of a positive site is required. FDG is a nonspecific marker of malignancy and uptake can be seen at sites of active, acute inflammation. This is thought to be attributable to uptake by activated macrophages and inflammatory cells [18]. Specificity of FDG PET [8] in early reports was high (80% to 88%), but a recent study found lower specificity (52%) [12]. Higher incidence of granulomatous disease within the population studied may reduce specificity.

PET confirmed the diagnosis of a malignancy in 11 of 13 patients who had an undiagnosed lung lesion before scanning. Two patients, with subsequently confirmed cancer, had failed percutaneous biopsy attempts before PET. PET may be useful if there is high clinical suspicion of a malignant lung lesion or metastatic disease where fine needle biopsy is negative or fails. Figure 2 illustrates that a negative fine needle aspiration may not exclude malignancy.

An important finding of this study was that PET was more accurate than CT in detecting N2 and N3 disease and correctly altered nodal stage in 13.4% of patients (Figs 1 and 3). Recent studies have also shown that PET correctly altered nodal stage in up to 21% and was superior to CT in staging of the mediastinum with sensitivity of 76% to 100%, specificity of 81% to 98%, and accuracy of 80% to 93% [10, 11, 19]. We found lower sensitivity (70.6%) in detection of N2 and N3 disease but excellent specificity (97%) and accuracy (91.6%). Presumably the volume of disease in the false-negative cases on PET was below the resolution of the PET system. It is also possible that delayed imaging of the mediastinum will allow higher accumulation of FDG in this region to allow a higher discrimination of metastatic disease. The lower sensitivity may be partly attributable to selection criteria excluding patients with mediastinal adenopathy on CT. PET improved the selection of patients with negative mediastinal and distant disease and therefore, improved the 1-year mortality to 7.5% for stage 1 disease compared with our previously published figures (for the same surgeon) of 14%; the stage 2, 3, and 4 mortality figures were similar to the previous figures [20].

View larger version (104K): [in this window] [in a new window]   Fig 3. Fluoride-18-fluorodeoxyglucose study demonstrating uptake in the right lower lobe primary malignancy with no evidence of mediastinal or distant metastases. Coronal (A) and sagittal (B) slices.

Three patients had operable disease by CT staging; however, clinical features raised suspicion of a more advanced stage. One patient had a long-standing skin lesion historically, thought to be a sebaceous cyst; the second had pain in the biceps after trauma, clinically consistent with hematoma, and the third had weight loss. PET was positive at distant sites in these patients and disease proved at biopsy. Therefore, PET provided evidence of metastatic disease and identified sites amenable to biopsy for histologic confirmation.

Physiologic uptake of FDG can cause difficulties in the interpretation of PET scans. Three possible adrenal lesions were seen on CT and were negative on PET. Malignant involvement was excluded by biopsy and outcome in 1 patient but 2 patients died of disseminated disease. Therefore, these are presumed false-negative sites. FDG is excreted in urine and pelvicalyceal hold up of FDG can make interpretation of the adrenal region difficult. We are currently using intravenous furosemide to increase urine flow rates, dilute the concentration of FDG in urine, and improve drainage of the renal collecting systems. Scanning the adrenal region later may also assist. Physiologic cardiac and bowel uptake can be marked but did not appear to cause significant difficulties in interpretation.

Management was altered in 37%, which is similar to our previous findings (41%) in a smaller series [14]. Staging by PET scan and SUV of the primary lesion were the best prognostic indicators of time to death other than operative staging. A direct relation between tumor doubling time and FDG uptake (measured by SUV) in lung cancer has been shown [23], but the prognostic value of SUV and PET stage has not been previously defined. Semiquantitative evaluation is currently possible on lesions in the attenuation corrected thoracic views. Soon it will be possible to routinely perform attenuation corrected whole body studies; therefore, SUV can be determined for all abnormal sites. This may improve lesion resolution and detection of metastases.

In conclusion, it is likely that the use of PET as an initial evaluation of all patients with non-small cell lung cancer should allow those patients with distant disease and with inoperable mediastinal disease to be identified. It is a noninvasive test with prognostic value. Further studies are required to assess the appropriate timing of PET in the decision tree of lung cancer staging and the cost effectiveness of its routine use. A possible algorithm is shown (Fig 4). This will form the basis of another study.

View larger version (25K): [in this window] [in a new window]   Fig 4. Proposed algorithm for the use of positron emission tomography in patients with proved lung cancer. Note: Computed tomographic scan is not necessary before positron emission tomogram if the patient has an intrapulmonary lesion. Computed tomographic scan is nessary to assess lesions close to the mediastinum or chest wall to assess local invasion.

	Acknowledgments

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 

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				G J Herder, H van Tinteren, E F Comans, O S Hoekstra, G J Teule, P E Postmus, U Joshi, and E F Smit Prospective use of serial questionnaires to evaluate the therapeutic efficacy of 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET) in suspected lung cancer Thorax, January 1, 2003; 58(1): 47 - 51. [Abstract] [Full Text] [PDF]

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				J B Bingham Where can FDG-PET contribute most to anatomical imaging problems? Br. J. Radiol., November 1, 2002; 75(90009): S39 - 52. [Full Text] [PDF]

				M. Nosotti, L. Santambrogio, M. Gasparini, A. Baisi, N. Bellaviti, and L. Rosso Role of 99mTc-Hexakis-2-Methoxy-Isobutylisonitrile in the Diagnosis and Staging of Lung Cancer Chest, October 1, 2002; 122(4): 1361 - 1364. [Abstract] [Full Text] [PDF]

				H. Vesselle, J. M. Pugsley, E. Vallieres, and D. E. Wood The impact of fluorodeoxyglucose F 18 positron-emission tomography on the surgical staging of non-small cell lung cancer J. Thorac. Cardiovasc. Surg., September 1, 2002; 124(3): 511 - 519. [Abstract] [Full Text] [PDF]

				M. A. Seltzer, C. S. Yap, D. H. Silverman, J. Meta, C. Schiepers, M. E. Phelps, S. S. Gambhir, J. Rao, P. E. Valk, and J. Czernin The Impact of PET on the Management of Lung Cancer: The Referring Physician's Perspective J. Nucl. Med., June 1, 2002; 43(6): 752 - 756. [Abstract] [Full Text] [PDF]

				E. Salminen and M. Mac Manus FDG-PET imaging in the management of non-small-cell lung cancer Ann. Onc., March 1, 2002; 13(3): 357 - 360. [Abstract] [Full Text] [PDF]

				J.F. Vansteenkiste Imaging in lung cancer: positron emission tomography scan Eur. Respir. J., February 1, 2002; 19(35_suppl): 49S - 60s. [Abstract] [Full Text] [PDF]

				S F Barrington Whole body applications of positron emission tomography in oncology Imaging, September 1, 2001; 13(3): 185 - 196. [Abstract] [Full Text] [PDF]

				G Laking and P Price 18-Fluorodeoxyglucose positron emission tomography (FDG-PET) and the staging of early lung cancer Thorax, September 1, 2001; 56(90002): ii38 - 44. [Full Text] [PDF]

				S. S. Gambhir, J. Czernin, J. Schwimmer, D. H. S. Silverman, R. E. Coleman, and M. E. Phelps A Tabulated Summary of the FDG PET Literature J. Nucl. Med., May 1, 2001; 42(90050): 1S - 93. [Full Text] [PDF]

J.F. Vansteenkiste and S.G. Stroobants The role of positron emission tomography with 18F-fluoro-2-deoxy-D-glucose in respiratory oncology