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J Thorac Cardiovasc Surg 1995;110:130-140
© 1995 Mosby, Inc.
GENERAL THORACIC SURGERY |
Durham, N.C.
Address for reprints: Walter G. Wolfe, MD, Duke University Medical Center, Box 3507, Durham, NC 27710.
Abstract
Positron emission tomography (PET), with the glucose analog F-18 fluorodeoxyglucose (FDG), takes advantage of the enhanced glucose uptake observed in neoplastic cells. We examined whether the detection of preferential FDG uptake with PET permits differentiation between benign and malignant focal pulmonary lesions in patients with suspected primary or recurrent lung cancer. Between November 1991 and September 1993, 100 patients with indeterminate focal pulmonary abnormalities including 16 patients who had previous lung resections for cancer were prospectively studied. Tissue diagnosis was obtained by transbronchial or percutaneous biopsy (n = 49) and open biopsy or resection (n = 35). Three patients underwent extended observation (>2 years) alone. Excluded were 13 patients lacking firm pathologic diagnoses and less than 2-year follow-up. FDG activity in the lesion was expressed as a calculated standardized uptake ratio. Mean standardized uptake ratio (±standard deviation) was 6.6 (±3.1) in 59 patients with cancer versus 2.0 (±1.6) in 28 with benign disease (p = 0.0001; unpaired t test, two-sided). With a standardized uptake ratio 2.5 used for detecting malignancy, sensitivity, specificity, and accuracy were 97% (57/59), 82% (23/28), and 92% (80/87), respectively. Notably, in patients evaluated for pulmonary abnormalities after lung resection for cancer, all chest recurrences were correctly identified. The exceptional sensitivity of FDG PET demonstrates that malignant pulmonary lesions preferentially accumulate FDG, which results in a standardized uptake ratio 2.5. PET may be useful for distinguishing recurrent tumor from postoperative, or postradiation, changes. If performed in all patients before open biopsy, PET increases the diagnostic yield by reducing the number of patients who have benign lesions at operation. Moreover, by lowering expenditures for hospitalization and other diagnostic procedures, FDG PET may significantly reduce health care costs. (J THORAC CARDIOVASC SURG1995;110:130-40)
Focal pulmonary abnormalities frequently present a diagnostic challenge. In particular, radiographic lesions that arise in the setting of preexisting lung disease or treatment-induced soft tissue changes often require invasive biopsy for diagnosis. Because the risk of complications and death resulting from surgery may be substantial in certain high-risk patients, less invasive chest imaging techniques are commonly used. Unfortunately, chest radiography and computed tomography (CT) have varying sensitivities ranging from 52% to 80% and lack sufficient specificity to provide a definitive diagnosis.
1, 2 Consequently, increasing interest has focused on imaging techniques that rely on metabolic rather than anatomic properties of lung cancer as a means to guide medical therapy. One example is positron emission tomography (PET).
PET, using the glucose analog fluorine-18-fluorodeoxyglucose (FDG), takes advantage of the enhanced glucose uptake observed in neoplastic cells. First appreciated by Warburg, Wind, and Negleis 3 in 1923, the increased activity of key glycolytic enzymes in malignant tumor cells has since been verified by others. 4 Entering the cell through facilitated transport, FDG is phosphorylated by hexokinase and trapped intracellularly. Because FDG-6-phosphate is metabolized slowly, its rate of appearance within the cell correlates directly with glycolytic flux. 4 PET quantitates FDG activity in vivo and identifies those lesions with increased glycolytic activity suggestive of malignancy.
This study examined the diagnostic accuracy of FDG PET in differentiating between benign and malignant focal pulmonary lesions in patients with indeterminate pulmonary abnormalities after chest radiography and CT, as well as suspected primary or recurrent lung cancer. On the basis of the results from this study, a rational strategy incorporating PET imaging in the work-up of indeterminate pulmonary abnormalities is suggested, with special emphasis placed on detecting recurrent cancer after previous lung resection and irradiation. Finally, because of the financial expense associated with PET imaging, issues regarding health care costs are also addressed.
PATIENTS AND METHODS
Between November 1991 and September 1993, patients referred to the Duke University Medical Center chest medicine and thoracic surgery clinics with indeterminate focal pulmonary abnormalities by chest radiography and CT were eligible for enrollment into the study. Protocol design was approved by the institutional review board, and informed consent was obtained in all participants. Reasons for study exclusion included age less than 18 years, pregnancy, scheduling constraints resulting from immediacy of operation, and patient refusal.
All patients fasted for 4 hours before the study. The patients were positioned in the PET unit so that the pulmonary lesions were near the center of the longitudinal field of view. The PET unit (4096 Plus; General Electric Medical Systems, Milwaukee, Wis.) comprised eight detector rings positioned in a cylindric array. This produced 15 axial images along a 97 mm longitudinal field with a spatial resolution of about 5 mm. 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, a second PET unit was added (Advance; General Electric Medical Systems) containing 18 detector rings and producing 35 axial images along a 150 mm longitudinal field; image processing and reconstruction were performed with a Hewlett-Packard Apollo Series 765 (Hewlett-Packard Company, Andover, Mass.). Transmission scans were performed with germanium 68 pin sources to correct for soft tissue attenuation and to facilitate localizing the radiographic abnormality. Emission images were obtained over a 20-minute period starting 30 minutes after intravenous injection of 10 mCi (370 MBq) of FDG. In our later experience, emission images were acquired beginning 60 minutes after FDG injection on the basis of studies using dynamic PET imaging that determined the best scanning protocol to discriminate benign from malignant pulmonary lesions. 5 FDG was synthesized in ourlaboratory by means of standard methods. 6 A region of interest (ROI), usually measuring more than 1 cm in diameter, was selected on the emission images to include the highest intensity of FDG activity in the area of the corresponding transmission or radiographic abnormalities. The mean ROI activity was corrected for radioactive decay, and a standardized uptake ratio (SUR) was calculated according to the following formula:
SUR = mean ROI activity (mCi [mBq]/ml/injected dose
mCi [MBq])/body weight (kg)
To minimize observer bias, the ROI was selected and SUR calculated by a nuclear medicine physician (V.J.L.) without prior knowledge of the patient's clinical history, physical examination, or laboratory studies (including all cytology and biopsy reports).
A histologic diagnosis was obtained in 84 patients from transbronchial or percutaneous biopsy (n = 49) and open biopsy or resection (n = 35) Three patients underwent extended observation (>2 years) alone without change, or gradual resolution, of the radiographic abnormality. Thirteen patients without a definitive pathologic diagnosis and less than 2 years of follow-up were excluded.
Sensitivity, specificity, accuracy, and likelihood ratios were calculated with the use of standard equations. Comparison of SUR values between groups with benign and malignant disease was performed by means of a two-sided, unpaired Student's t test. The null hypothesis was rejected at the 
= 0.05 significance level. The mean ± standard deviation are reported.
RESULTS
One hundred patients with focal pulmonary lesions that were indeterminate after chest radiography and CT underwent FDG PET imaging. The male/female ratio was 3:2, and mean age was 58 ± 4 years. Seventy-nine patients had solitary pulmonary nodules (defined as a focal abnormality 
4 cm in diameter), and 11 had pulmonary masses (>4 cm in diameter). Mean diameter of pulmonary nodules and masses was 2.2 ± 0.8 and 5.2 ± 0.8 cm, respectively. Ten patients had ill-defined pulmonary infiltrates. Included in this study were 16 patients who had previous lung resections for cancer (7 solitary nodules and 9 ill-defined opacities).
Eighty-seven patients had histologic confirmation or extended follow-up to exclude malignancy. A histologic diagnosis of bronchogenic carcinoma was made in 59 patients. The mean (±SD*) SUR was 6.6 ± 3.1 for this group (Fig. 1). Carcinoma was found in 45 of 67 solitary pulmonary nodules (67%), with a mean (±SD) diameter of 2.3 ± 0.8 cm; 10 of 11 pulmonary masses (91%) with a mean (±SD) diameter of 5.2 ± 0.8 cm; and 4 of 9 pulmonary infiltrates (44%). The mean (±SD) SURs for malignant solitary nodules, masses, and infiltrates were 5.5 ± 2.1, 8.7 ± 3.8, and 5.1 ± 2.0 (range 3.4 to 7.4), respectively.
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The true-positive rate (sensitivity) and false-positive rate (1 -specificity) of FDG PET for the diagnosis of malignancy were determined at several SUR levels (Fig. 2). The ideal diagnostic test represents the upper left-hand corner of this plot, where the true-positive rate is 1.00 and the false-positive rate is 0.00. From this curve, an SUR 
2.5 was selected as the best cutoff (the point nearest the upper left-hand corner) in terms of minimizing diagnostic error when prevalence of malignancy approximated 50%. An SUR 2.5 criterion for malignancy achieved a sensitivity, specificity, and accuracy of 97% (57/59), 82% (23/28), and 92% (80/87), respectively. For lesions 3 cm in diameter or smaller (n = 47), sensitivity, specificity, and accuracy were 100% (31/31), 81% (13/16), and 94% (44/47), respectively.
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FDG PET accurately differentiates benign from malignant focal pulmonary abnormalities. In this study, an SUR 2.5 identified malignant lesions with 97% sensitivity, 82% specificity, and 92% accuracy. Conversely, an SUR <2.5 demonstrated 82% sensitivity and 97% specificity for detecting benign disease. False-positive diagnoses, that is, benign lesions with SURs 2.5, were occasionally encountered in active infections having FDG uptake similar to neoplasms (Fig. 7, B). A recent report has demonstrated that the rate of accumulation of FDG in inflammatory cells may be different from that in tumor cells.* Thus technical improvements in emission acquisition time may enhance separation between benign and malignant lesions and reduce the false-positive rate.* Because the relationship between the SUR and cancer risk is not dichotomous but rather continuously distributed, the SUR may be interpreted as a likelihood ratio, or odds, that at a given level of SUR, a certain likelihood of malignancy exists (Table I). For example, from Table I, a lesion with an SUR 6.0 has a greater than fifteenfold likelihood of being malignant than benign; alternatively, a lesion with an SUR <1.5 is always benign. FDG PET provides a quantitative estimate of relative cancer risk for any pulmonary lesion and guides appropriate therapy.
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7-9 In particular, for malignantlesions measuring 3 to 4 cm in diameter, Wallace and Deutsch 9 reported that bronchoscopy had a sensitivity of only 56%, which dropped to 25% for lesions less than 2 cm in diameter. In contrast, the overall 97% sensitivity of FDG PET for detecting malignant lesions rose to 100% when limited to lesions smaller than 3 cm in diameter. For benign disease, bronchoscopy with brushings and transbronchial biopsy established a specific diagnosis in only 12.5% of nodules later proved benign. 7 As the primary role of biopsy is to verify benign disease and thereby avoid a nontherapeutic thoracotomy, bronchoscopy offers little to the overall management of indeterminate focal pulmonary abnormalities.
Transthoracic needle aspiration biopsy is highly accurate in the diagnosis of bronchogenic carcinoma and metastatic disease, with several series reporting greater than 95% sensitivity. 10-12 However, for specific benign disease, such as granuloma and hamartoma, sensitivity drops to 40% to 50%, with studies ranging from 12% to 69%. 12,13 Although higher sensitivity rates are reported in studies that combined specific and nonspecific benign diagnoses, few would equate a nonspecific nonmalignant biopsy with confirmed benign disease in view of the potential sampling error. 14 Thus transthoracic needle aspiration biopsy and FDG PET have comparable sensitivities for the diagnosis of malignancy, but PET may be preferred for the diagnosis of benignancy. Furthermore, transthoracic needle aspiration biopsy has several disadvantages, including (1) a small but definite risk of complications, including a 5% to 10% risk of symptomatic pneumothorax and a 1% to 10% risk of minor hemoptysis 14 ; (2) a delay in the diagnosis of benign disease while awaiting the results of permanent sections, special stains, or cultures; and (3) its relatively high cost (Table II). In contrast, FDG PET has no known morbidity (apart from that attributable to modest radiation exposure), confers a rapid diagnosis, and costs significantly less than transthoracic needle aspiration biopsy (Table II). Thus, by demonstrating superior sensitivity in the diagnosis of benign disease, combined with immediate results, lower morbidity, and less cost, FDG PET may be preferable to transthoracic needle aspiration biopsy as the procedure of choice in selected patients with focal pulmonary abnormalities.
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To assess the economic impact of FDG PET on the diagnosis and management of benign and malignant focal pulmonary lesions, we performed a cost analysis using two alternative strategies: (1) immediate thoracotomy and (2) FDG PET. The PET strategy was further subdivided into two arms on the basis of the SUR result; SUR >2.5 led to thoracotomy and SUR <2.5 warranted observation with periodic chest films to assess the nodule's rate of growth. To simplify the model, we made several conditions and assumptions: (1) all lesions were indeterminate, by chest radiography and CT, solitary pulmonary nodules less than 3 cm in diameter; (2) the pretest probability of malignancy was 50%; (3) the sensitivity and specificity of FDG PET for diagnosis of malignant disease were 97% and 82%, respectively; (4) the complication rate for thoracotomy was zero; and (5) the total hospital stay for thoracotomy was 5 days— that is, patients were discharged on the fourth postoperative day. The hospital charges and cost analysis for a group of 100 patients are shown in 
Tables II and III. The strategy using FDG PET resulted in 41 fewer nontherapeutic operations and reduced overall costs by about 25% (Table III). This is a conservative estimate, however, that excludes the added cost of a longer hospitalization; perioperative complications that prolong the length of hospital stay, require intensive care unit management, or result in long-term disability or death; the discomfort and lost wages incurred after nontherapeutic thoracotomy; and the expense of transbronchial biopsy, transthoracic needle aspiration biopsy, or other procedures that might otherwise have been used. In our model, one malignant lesion was not detected on PET and its resection was delayed. Options to reduce the false-negative rate may include lowering the SUR criterion for malignancy or repeating the FDG PET at a later date. By reducing the number of patients in whom benign disease is found during an operation, PET increases the diagnostic yield with thoracotomy. By lowering overall expenditures for hospitalization and other diagnostic procedures, FDG PET may significantly reduce health care costs.*
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Although FDG PET is highly accurate for detecting pulmonary malignant tumors, its ultimate role remains undefined. Before widespread application of PET can be advocated, studies must first establish its cost-effectiveness. The financial impact of FDG PET for indeterminate solitary pulmonary nodules is currently being investigated in a prospective, multicenter clinical trial. Meanwhile, continuing studies will focus on improving the diagnostic accuracy of currently used semiquantitative tumor uptake indices, evaluating the accuracy of FDG PET in smaller lesions (<1 cm diameter), and studying the relationship between FDG activity and tumor growth rate and clinical outcome.
Appendix: DISCUSSION
Dr. Robert J. McKenna, Jr. (Los Angeles, Calif.).
This new technology looks very exciting. Rather than being the gallium scan of the 1990s, it probably will play an important role in the diagnosis and staging of lung cancer. I have a few questions regarding the PET scan evaluation of the primary tumor and metastatic sites, and I also want to make a comment on your cost analysis.
You categorized the primary tumors as benign versus cancer and included in the benign category both inflammatory and benign tumors. What was the sensitivity for benign tumors versus malignant tumors? Do you know the sensitivity of PET scan for different cell types of lung cancer and primary versus metastatic tumors?
Dr. Duhaylongsod.
We had 28 benign lesions in the study, only one of which was a benign tumor and it was a chondromatous hamartoma. It gave an SUR value of 6.0, so by our criteria it was a false-positive diagnosis. We cannot comment any further because of the small sample size.
Dr. McKenna.
How small a tumor volume can the PET scan detect?
Dr. Duhaylongsod.
The resolution of current PET technology is 5 mm; however, one of our false-negative diagnoses was a tumor that was approximately 4 mm located in a pleural rind in a patient who had had resection. The size is a consideration, and it is an area of active research.
Dr. McKenna.
Were there other patients who had nodal metastases from their primary tumor? If so, do you have a sense yet of how good a job this can do in staging the nodal metastases?
Dr. Duhaylongsod.
Although this preliminary study was primarily designed to test benign versus malignant, we noted many patients having mediastinal involvement as well as involvement in the adrenal gland and involvement in the liver. The best way to study that would be in a prospective fashion. Since the termination of this study we are prospectively enrolling patients to do correlative mapping studies of the PET scans versus operative findings.
Dr. McKenna.
I also want to make a quick comment about the cost of the open lung biopsy. Your numbers seem a bit high. For example, last week I did a lobectomy on a patient from Hong Kong. My hospital wanted cash up front and accepted $9,000 for a right upper lobectomy. The patient was home in 3 days.
Dr. Duhaylongsod.
To use the automobile analogy, if you are willing to pay cash, the price falls, but this was a very simple model. One assumption was that all patients undergoing thoracotomies had no complications. A second assumption was that the length of stay was 5 days. Obviously there are going to be variations.
Dr. Donald Hopkins (Sacramento, Calif.).
In my practice, the PET scan has been used in the management of 75 patients over the past 18 months. It has been a fascinating experience.
It has been helpful in three areas. The first area is in the evaluation and management of pulmonary nodules, masses, and indeterminant densities. Our experience closely parallels the Duke results. We also use the SUR value of 2.5 as the best number to separate benign from malignant densities. I would like to emphasize that a negative on a PET scan (that is, a zero SUR), even for nodules of 1 cm or less, has indicated to us that the density in question is not malignant. It is very helpful to have negative information on a solitary nodule or when multiple nodules are present either in one or both of the lungs.
Second, the PET scan is an accurate way of demonstrating the presence or absence of recurrent malignancy in a suspicious clinical setting.
Third, we have been encouraged at how helpful the PET scan technique is in staging bronchogenic carcinoma. Our numbers are small, but PET has been more accurate than CT scanning in predicting mediastinal N2 disease. Our experience with 37 patients with newly diagnosed lung cancer has shown positive and negative predictive values for the mediastinal and hilar nodes of 90% and 93%, respectively, whereas our CT scan values were only 50% and 78%, respectively. These were all confirmed by mediastinal lymphadenectomy at the time of thoracotomy or by mediastinoscopy biopsy. In identifying M1, stage IV disease, an "up-front" PET scan has demonstrated unsuspected metastatic lesions at a variety of unusual locations. Those pesky 2 to 3 cm adrenal gland nodules seen on the CT scan can be evaluated accurately with the PET scan. Isotope bone scan and osseous x-ray lesions are easily evaluated by PET scan. The same is true for hepatic lesions. Though valuable information about the brain can be obtained with the PET scan, the magnetic resonance image with gadolinium still remains the most sensitive way to demonstrate intracranial metastatic lesions.
Your fiscal analysis is pertinent and is the kind of information that should be presented to Medicare and insurance carriers. PET scanning is an expensive technology and reimbursement is needed. The bottom line, I believe, is that PET scanning when used appropriately, and the term appropriate has to be worked out with continued experience, will not only prove to be cost-effective, but more importantly will contribute to improved patient care. I would urge all the members of our association to become interested and informed and to take an active part in the clinical use of the PET scan.
Dr. Ahmed El Gamel (Manchester, United Kingdom).
I have one question. Because you do not have 100% accuracy or 100% specificity, how frequently are you going to follow up the patients? You have to compare the follow-up cost of this procedure with that of other procedures.
Dr. Duhaylongsod.
Because our specificity is not 100%, patients with an SUR < 2.5 obviously need to be followed up. We recommend repeating the PET scan over a 2 to 3 month period, although one may choose transbronchial biopsy or needle aspiration biopsy instead after the FDG PET scan. One thing that has been interesting in the evolution of this technology is that initially all patients who were referred to our institution had transbronchial biopsies or needle aspiration biopsies before they arrived. However, since the closure of this study, the practice patterns of our pulmonologists have changed. Now, all they order are FDG PET studies, and patients are going directly to the operating room with the result of a PET scan. I think that this is a very interesting change in behavior.
Footnotes
From the Departments of Surgerya and Radiology,b Duke University Medical Center, Durham, N.C. 
Read at the Twentieth Annual Meeting of The Western Thoracic Surgical Association, Olympic Valley, Calif., June 22-25, 1994.
*Lowe VJ, DeLong DM, Hoffman JM, Coleman RE. Optimum scanning protocol for FDG PETevaluation of focal pulmonary abnormalities. Unpublished data.
*The effectiveness of video-assisted thoracoscopic surgery (VATS) lobectomy over acceptedoperative techniques has not been documented in randomized trials. Thus, in the management ofindeterminate solitary pulmonary nodules, the only accepted role for VATS is as a diagnostic tool.We believe, like others (Ann Thorac Surg 1993;56:825-32), that all positive thoracoscopic biopsiesshould be followed by thoracotomy unless the patient is enlisted in a clinical research protocol.Using the same conditions and assumptions enumerated above, the VATS strategy (about $12,180per procedure) applied to 100 patients with focal pulmonary abnormalities would cost over$2,000,000 [(100 x $12,180) + (50 x $15,982) = $2,017,100], or nearly $800,000 more than the FDG PET arm.
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K. S. Virgo, K. S. Naunheim, L. W. McKirgan, M. E. Kissling, J. C. Lin, and F. E. Johnson COST OF PATIENT FOLLOW-UP AFTER POTENTIALLY CURATIVE LUNG CANCER TREATMENT J. Thorac. Cardiovasc. Surg., August 1, 1996; 112(2): 356 - 363. [Abstract] [Full Text]
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