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Randomized Controlled Trial of the Role of Positron Emission Tomography in the Management of Stage I and II Non-Small-Cell Lung Cancer

From the Centre for Health Economics Research and Evaluation, University of Technology, Sydney; Medical Oncology Unit, Sydney Cancer Centre; Cardiothoracic Surgical Unit, PET Unit, and Department of PET and Nuclear Medicine, Royal Prince Alfred Hospital; and Faculty of Medicine, University of Sydney, Sydney, Australia

Address reprint requests to Rosalie Viney, Centre for Health Economics Research and Evaluation, University of Technology, Sydney, PO Box 123, Broadway, Sydney, NSW 2007, Australia; e-mail: rosalie.viney{at}chere.uts.edu.au

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
PURPOSE: Positron emission tomography (PET) is a costly new technology with potential to improve preoperative evaluation for patients with non–small-cell lung cancer (NSCLC). There is increasing pressure for PET to be included in standard diagnostic work-up before decisions about surgical management of NSCLC. The resource implications of its widespread use in staging NSCLC are significant.

METHODS: A randomized controlled trial was conducted to investigate the impact of PET on clinical management and surgical outcomes for patients with stage I-II NSCLC. The primary hypothesis was that PET would reduce the proportion of patients with stage I-II NSCLC who underwent thoracotomy by at least 10% through identification of patients with inoperable disease.

RESULTS: One hundred eighty-four patients with stage I-II NSCLC were recruited and randomly assigned; 92% had stage I disease. Following exclusion of one ineligible patient, 92 patients were assigned to no PET and 91 to PET. Compared with conventional staging, PET upstaged 22 patients, confirmed staging in 61 and staged two patients as benign. Stage IV disease was rarely detected (two patients). PET led to further investigation or a change in clinical management in 13% of patients and provided information that could have affected management in a further 13% of patients. There was no significant difference between the trial arms in the number of thoracotomies avoided (P = .2).

CONCLUSION: For patients who are carefully and appropriately staged as having stage I-II disease, PET provides potential for more appropriate stage-specific therapy but may not lead to a significant reduction in the number of thoracotomies avoided.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
Non–small-cell lung cancer (NSCLC) accounts for approximately 80% of all lung cancer. At presentation, approximately 25% of patients have disease suitable for surgical resection.¹ Following surgical resection, up to 40% of patients with clinical stage I disease and 60% of patients with clinical stage II disease ultimately experience relapse, implying that they had occult metastatic disease at the time of presentation. Such patients do not benefit from surgery, and the ability to identify them could save an unnecessary thoracotomy.

Positron emission tomography (PET) is a relatively new imaging technology with potential to improve preoperative staging. Many malignant tumors show increased glucose utilization when compared with normal tissues.² Whole body PET with [¹⁸F]fluorodeoxyglucose (FDG) can identify regions of increased glucose metabolism in nonenlarged structures, allowing detection of tumor metastases earlier than with anatomic imaging methods. Data suggest PET may improve the accuracy of preoperative staging of NSCLC, but, in general, these are from small, retrospective, uncontrolled series.^3–5 A recent prospective uncontrolled study reported sensitivity and specificity of PET for detection of mediastinal and distant metastatic disease of 95% and 83%, respectively.⁶

PET is costly, and resource implications of its widespread use in staging NSCLC are significant. There is increasing pressure for PET to be included in the standard diagnostic workup before decisions about surgical management of NSCLC.^7,8

Randomized trials are considered the most appropriate and reliable way of assessing the efficacy and safety of most medical interventions. Although concerns exist about whether this methodology is ideal for the evaluation of new health technology,⁹ randomized trials can provide useful information on the impact of PET on management of patients, outcomes of care and resource use.¹⁰ A recent randomized controlled trial demonstrated that PET reduced futile thoracotomies in patients with stages I-III NSCLC.¹¹ However, prognosis and management of patients with stages I-II disease differs from that of patients with stage III disease.^12,13 We have conducted a randomized controlled trial to investigate the impact of FDG PET on clinical management. At the time this trial was designed, anecdotal evidence suggested that FDG PET identified moderately large numbers of patients with clinical stage I-II NSCLC who were harboring occult metastases. We therefore chose as a primary end point of the study the proportion of patients who were able to avoid a thoracotomy as a consequence of the findings on FDG PET.

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
Study Design
The primary hypothesis of this study was that PET would reduce the proportion of patients with stage I-II NSCLC based on conventional staging who underwent thoracotomy by at least 10% through identification of patients with inoperable disease. A secondary objective was to determine the impact of PET on health system resource use for patients with stage I-II NSCLC. Results relating to cost and resource use will be reported elsewhere.

The study protocol was approved by the ethics committee of each participating institution. Patients were recruited between April 1999 and December 2000 from six participating surgeons at four metropolitan tertiary referral hospitals in Sydney, Australia.

Eligible patients were randomized to surgical resection (no-PET), or to an FDG-PET before surgery (PET). Randomization was based on a computer-generated random number list and was assigned by a data manager, who was independent of and remote from the participating hospitals and surgeons.

Participants
Eligibility criteria were age 18 to 90 years; histologically or cytologically established diagnosis of NSCLC; assessed ability to tolerate the planned surgical procedure; no significant biochemical or hematologic abnormalities; not receiving experimental cancer therapy; absence of pregnancy; and capability of completing study questionnaires. All patients were staged with a chest x-ray, and CT scan of the thorax, upper abdomen and brain. Mediastinoscopy was not mandated before randomization, because in Australia this is a rarely performed procedure in patients with stage I or II NSCLC on clinical and radiologic evaluation.

Scans and x-rays were reviewed by a radiologist and the patient's surgeon and must have been assessed as demonstrating stage I or II disease. Bone scans were only performed in patients with symptoms or signs of bony metastatic disease. All patients gave written informed consent.

Study Procedures
FDG-PET scans were scheduled for the earliest available date before surgery. All scans were performed at one center using an ECAT 951R whole body scanner, with bismuth germanate detectors (CTI-Siemens, Knoxville, TN). The scanner was made in 1992. Scans extended from the base of the skull to the upper thighs. Patients fasted for 6 hours before the PET scan but were allowed to drink water and take usual medications. All patients had blood glucose levels measured before scanning. Blood glucose levels were not manipulated by the use of insulin. No patients had blood glucose levels greater than 10 mmol/L. FDG (5–7 MBq/kg) was administered intravenously, and a urinary catheter was placed before commencement of the study. Emission and transmission data were acquired simultaneously after an uptake period of 50 minutes, with scan duration of 64 minutes.¹⁴ Scans were interpreted on a computer monitor by a single experienced PET physician (M.J.F.) and reported using the tumor-node-metastasis staging system of the American Joint Committee on Cancer.¹³ CT images were available to the PET physician but not used in interpretation of the PET scans. The reporter was aware that the patients were eligible for and participating in a trial that required the mediastinum to appear normal on CT scan.

Based on the results of the PET scan, the provisional diagnosis and planned management was reviewed by the referring surgeon. Further management, including mediastinoscopy, surgery, and postsurgical therapy, was at the discretion of the surgeon. Local or distant metastatic disease detected by PET was confirmed by biopsy. If abnormalities detected by PET were unable to be confirmed, patients proceeded to thoracotomy. For patients randomly assigned to no PET, thoracotomy was arranged for the earliest available date.

Clinical classification of disease at each point in the trial was made using tumor-node-metastasis system classification.¹³ All patients were assigned a stage based on conventional staging at the initial consultation. Patients randomly assigned to PET were assigned a "PET stage" based on the results of the PET scan. Patients proceeding to surgery or who underwent biopsy were assigned a "definitive stage." All PET reports and postsurgical pathology reports were independently reviewed by one of the authors (M.J.B.) on separate occasions. In the case of postsurgical pathology, this independent review was undertaken blinded to randomization.

Statistical Analysis
A total sample size of 174 patients (87 patients in each arm) was required to detect a 10% change in the proportion of patients undergoing thoracotomy with 80% power and a type I error of 0.05 (two-tail test). Analysis was by intention to treat. The clinical and sociodemographic characteristics of patients at randomization were compared using t-tests for continuous variables and Fisher's exact test for categoric variables. All tests were two-tailed with a significance level of 5%.

	RESULTS

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Figure 1 shows the trial profile. A total of 276 patients with stage I-II NSCLC presented to the six participating cardiothoracic surgeons. Twenty-eight patients were inoperable—either not fit for surgery or nonresectable because of tumor location—and 49 were ineligible because they had undergone a PET scan before the first surgical consultation. Of the 199 eligible patients, 184 were recruited and randomly assigned. The majority (65%) were assessed by one surgeon (B.C. McC.). One patient in the no-PET arm was found to be ineligible after randomization because of brain metastases detected on a prerandomization brain CT scan and was excluded from analysis. Thus, 92 patients were assigned to no PET and 91 to PET. Table 1 shows the baseline demographic and clinical characteristics of trial participants. There were no statistically significant differences.

View larger version (28K): [in this window] [in a new window]   Fig 1. Trial profile. NSCLC, non–small-cell lung cancer. PET, positron emission tomography.

Compared with conventional staging, PET suggested a different stage in 24 patients. Stage IIIA disease was suggested in 13 patients, stage IIIB in six patients, stage IV in three patients, and benign disease in two patients. Stage as assessed by FDG PET was unchanged from that indicated by conventional staging in 61 cases. Of the 13 patients in whom PET suggested stage IIIA disease, one underwent mediastinoscopy, which confirmed the PET assigned stage. The remaining 12 went to thoracotomy without further preoperative evaluation, on the basis of the surgeon's judgment that it would be possible to completely resect all disease. Based on the pathologic findings at surgery, 10 of these patients had stage IIIA disease, one had stage I disease, and one had stage IIIB disease.

All six patients in whom the PET scan suggested the presence of stage IIIB disease underwent mediastinoscopy, which confirmed the PET findings in only one patient, who did not undergo thoracotomy. The remaining five patients underwent thoracotomy. The pathologic findings were silicosis in one patient; a superior mediastinal node involved by a second unsuspected malignancy (thyroid); a contralateral scalene node detected on PET that could not be confirmed at biopsy (although this patient represented with disseminated disease 3 months after surgery); a presumed ipsilateral scalene node lesion that was not confirmed on biopsy, has persisted, and remains undiagnosed 21 months after the initial PET scan, but with no other evidence of malignancy; and one patient with stage I disease on definitive staging.

All three patients identified as PET stage IV had further evaluation. Metastatic disease was confirmed in two of these patients. A solitary adrenal metastasis was resected in one of these patients, followed by a thoracotomy. In the other patient, metastatic disease could not be confirmed.

All patients who were PET stage I-II (n = 61) proceeded to thoracotomy, including two of the patients described previously, who were found to have benign disease. Six of these patients were stage IIIA on pathologic staging. Table 2 compares the PET-assigned stage with subsequent staging (pathologic stage for patients undergoing surgery or staging based on additional diagnostic tests following PET for the two patients who did not undergo thoracotomy).

Four patients were randomly assigned without a histologic or cytologic diagnosis of malignancy (in contravention of the study protocol). All of these patients were randomly assigned to PET. PET identified one of these patients as having benign disease, and thoracotomy was avoided. In another patient, PET suggested benign disease, but a thoracotomy was performed as definitive management for a lung abscess. A third patient had a PET scan that was interpreted as showing malignancy, and a fourth patient did not have a PET scan; each underwent a thoracotomy, and the postsurgical diagnosis for both was benign disease. One other patient, with a preoperative diagnosis of malignancy, had a PET scan interpreted as stage IA disease but at thoracotomy was found to have benign disease.

There was no significant difference between the arms in the number of thoracotomies avoided (Table 3; P = .2). In the PET arm, four patients did not undergo thoracotomy. This included one patient randomly assigned to PET who did not undergo a PET scan but was found to have metastatic disease on additional diagnostic testing undertaken subsequent to randomization. Two patients in the no-PET arm did not undergo thoracotomy. One was found to have metastatic disease on a bone scan undertaken because of development of bone pain after randomization. The other patient declined surgery. Follow-up revealed this patient subsequently had surgery off-study (performed by a nonstudy surgeon at a different hospital).

The sensitivity and specificity of PET for identification of mediastinal disease was 73% (95% CI, 54% to 92%) and 90% (95% CI, 82% to 98%), respectively. Sensitivity and specificity for identification of metastatic disease was not calculated because of the small number of patients with stage IV disease. In patients who had a single lymph node involved, PET correctly identified 55% of cases (five of nine cases), and when multiple lymph nodes were involved, PET correctly identified 71% of cases (five of seven).

With a minimum of 12 months' follow-up, 80% (95% CI, 70% to 87%) of patients in the PET arm and 77% (95% CI, 67% to 85%) of patients in the no-PET arm were alive. Twelve-month survival by stage at presentation was 87% (95% CI, 69% to 95%) for stage IA, 78% (95% CI, 70% to 84%) for stage IB and 62% (95% CI, 31% to 82%) for stage IIB.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
Non–small-cell lung cancer remains a substantial cause of cancer morbidity and mortality. Selecting appropriate treatment for patients with early stage disease is an important goal of management. Early studies of FDG PET suggested that it could identify patients who had occult metastatic disease. The identification of such patients would improve treatment by preventing surgery in those who would not benefit from it. On the basis of these reports, we designed this study with the primary end point being the number of thoracotomies avoided.

PET scanning was successful in identifying mediastinal and, to a lesser extent, distant disease in our patients, and resulted in a change in stage in 18 patients (20%). The predominant finding was of ipsilateral mediastinal lymph node involvement, with only a small proportion of patients having distant metastatic disease detected. Despite the identification of disease that was greater than stage I or II, there was no reduction in the number of thoracotomies among patients who underwent FDG PET scans in addition to conventional staging. The treatment algorithm used by the surgeons participating in this study resulted in patients with stage IIIA disease and normal sized mediastinal nodes undergoing thoracotomy, and as this was the major group of patients identified by PET the overall rate of thoracotomy was no different in the two arms.

The optimal management of stage N2 disease remains controversial, with conflicting results from randomized controlled trials.^12,15,16 Current management approaches for N2 disease include surgery alone, induction chemo/radiotherapy followed by surgery, or chemo/radiotherapy alone. The most common management decision in this study was to proceed with thoracotomy, sometimes preceded by mediastinoscopy, reflecting the approach to management of microscopic (and thus resectable) N2 disease among participating surgeons.

Subsequent to this study, management practices have changed at participating hospitals, and patients with stage IIIA disease are now treated routinely with neoadjuvant chemotherapy.^12,15,16 Had the treatment algorithm during the time of the study involved the use of neoadjuvant chemotherapy or chemoradiotherapy, PET scanning could have had an impact on the management of up to 20% of the patients. Such a difference would have reached statistical significance. Thus, the value of FDG-PET for management of patients with clinical stage I-II NSCLC is dependent on the management strategy for stage IIIA disease.

Mediastinoscopy is rarely used in Australia in patients who have clinical stage I or II NSCLC and who are otherwise fit for thoracotomy. Consequently, the major effect of FDG-PET was identification of patients with stage IIIA disease (stage IIIB and stage IV disease was detected in only 4% of PET scans). Thirteen patients had N2 nodal involvement detected by PET where these nodes were not enlarged by CT criteria.

This study also demonstrates the potential for PET to exclude malignant disease; five patients did not have NSCLC. When both potential impacts of PET on management of patients are considered (thoracotomy avoided, induction chemotherapy followed by thoracotomy), PET could have changed management for 26% of patients (11 of 91 thoracotomies avoided, 13 of 91 treatments of induction chemotherapy followed by thoracotomy avoided).

We found the sensitivity and specificity of PET for the detection of mediastinal disease to be lower than that previously reported.^6,17 One possible explanation is that we were investigating a group of patients at lower risk of having mediastinal or metastatic disease than those included in previous studies. Furthermore, the volume of mediastinal disease present in our patients, who had already been clinically staged and found to have stage I-II disease would be expected to be low and possibly beyond the limit of resolution of the PET scan. These factors increase the likelihood of false-positive and negative findings.

The majority of patients (92%) recruited onto this study had stage I disease based on conventional assessment. This is in contrast to the PLUS multicenter randomized trial by van Tinteren et al¹¹, in which 64% of patients had stage I disease, 6% had stage II, and 30% had stage III disease or greater (one patient had stage IV disease). This may explain the different conclusions of the two studies. Van Tinteren et al concluded that addition of PET to conventional workup may prevent unnecessary surgery in 20% of their patient group. It is likely that this result was dominated by patients with stage III disease. Our results do not contradict this; rather, they suggest that the use of FDG-PET does not identify metastatic disease in many patients with stage I NSCLC.

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Acknowledgment

 
We thank surgeons Paul Bannon, Matthew Bayfield, Bruce French, Nick Hendel, and Michael Wilson; hospital staff Bonny Foye, Kim Silver, Jodie Brackenreg, Chris Constable, Scott Hawkins, and Hamda Saleh; research nurses Vera Cvetanovksi and Sandra Wojcinski; Anastasia Lowin; the patients who participated; and the staff of the participating hospitals.

	NOTES

 
Supported by a National Health and Medical Research Council Project Grant.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

	REFERENCES

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3. Wahl RL, Quint LE, Greenough RL, Meyer CR, White RI, Orringer MB: Staging of mediastinal non-small cell lung cancer with FDG PET, CT, and fusion images: Preliminary prospective evaluation. Radiology 191:371–377, 1994[Abstract/Free Full Text]

4. Weder W, Schmid RA, Bruchhaus H, Hillinger S, von Schulthess GK, Steinert HC. Detection of extrathoracic metastases by positron emission tomography in lung cancer. Ann Thorac Surg 66:886–892, 1998[Abstract/Free Full Text]

5. Saunders CA, Dussek JE, O'Doherty MJ, Maisey MN: Evaluation of fluorine-18-fluorodeoxyglucose whole body positron emission tomography imaging in the staging of lung cancer. Ann Thorac Surg 67:790–797, 1999[Abstract/Free Full Text]

6. Pieterman RM, van Putten JW, Meuzelaar JJ, et al: Preoperative staging of non-small-cell lung cancer with positron-emission tomography. N Engl J Med 343:254–261, 2000[Abstract/Free Full Text]

7. Berlangieri SU, Scott AM: Metabolic staging of lung cancer. N Engl J Med 343:290–292, 2000[Free Full Text]

8. Robert G, Milne R: A Delphi study to establish national cost-effectiveness research priorities for positron emission tomography. Eur J Radiol 30:54–60, 1999[CrossRef][Medline]

9. Hojgaard L: Are health technology assessments a reliable tool in the analysis of the clinical value of PET in oncology? Who audits the auditors? Eur J Nucl Med Mol Imaging 30:637–641, 2003[Medline]

10. Balk E, Lau J: PET scans and technology assessment: Deja vu? [editorial]. JAMA 285:936–937, 2001[Free Full Text]

11. van Tinteren H, Hoekstra OS, Smit EF, et al: Effectiveness of positron emission tomography in the preoperative assessment of patients with suspected non-small-cell lung cancer: The PLUS multicentre randomised trial. Lancet 359:1388–1393, 2002[CrossRef][Medline]

12. Rosell R, Gomez-Codina J, Camps C, et al: A randomized trial comparing preoperative chemotherapy plus surgery with surgery alone in patients with non-small-cell lung cancer. N Engl J Med 330:153–158, 1994[Abstract/Free Full Text]

13. Mountain CF: Revisions in the International System for Staging Lung Cancer. Chest 111:1710–1717, 1997[Abstract/Free Full Text]

14. Meikle SR, Bailey DL, Hooper PK, et al: Simultaneous emission and transmission measurements for attenuation correction in whole-body PET. J Nucl Med 36:1680–1688, 1995[Abstract/Free Full Text]

15. Roth JA, Fossella F, Komaki R, et al: A randomized trial comparing perioperative chemotherapy and surgery with surgery alone in resectable stage IIIA non-small-cell lung cancer. J Natl Cancer Inst 86:673–680, 1994[Abstract/Free Full Text]

16. Depierre A, Milleron B, Moro-Sibilot D, et al: Preoperative chemotherapy followed by surgery compared with primary surgery in resectable stage I (except T1N0), II, and IIIa non-small-cell lung cancer. J Clin Oncol 20:247–253, 2002[Abstract/Free Full Text]

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Submitted April 17, 2003; accepted March 27, 2004.

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