Originally published as JCO Early Release 10.1200/JCO.2005.02.4695 on March 27 2006

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Traditional Versus Up-Front [¹⁸F] Fluorodeoxyglucose–Positron Emission Tomography Staging of Non–Small-Cell Lung Cancer: A Dutch Cooperative Randomized Study

Gerarda J.M. Herder, Henk Kramer, Otto S. Hoekstra, Egbert F. Smit, Jan Pruim, Harm van Tinteren, Emile F. Comans, Paul Verboom, Carin A. Uyl-de Groot, Alle Welling, Marinus A. Paul, Maarten Boers, Pieter E. Postmus, Gerrit J. Teule, Harry J.M. Groen

From the Departments of Pulmonology, Nuclear Medicine and PET Research, Surgery, and Clinical Epidemiology and Biostatistics, VU University Medical Center; the Comprehensive Cancer Center, Amsterdam; Departments of Pulmonology, and Nuclear Medicine and PET-Center, University Medical Center, Groningen; Institute for Medical Technology Assessment, Erasmus MC, University Medical Center, Rotterdam: Department of Pulmonology, Medical Center–Alkmaar, Alkmaar, the Netherlands; and the POORT Study Group.

Address reprint requests to E.F. Smit, MD, PhD, Department of Pulmonology, VU University Medical Center, PO Box 7057, 1007 MB Amsterdam, the Netherlands; e-mail: ef.smit{at}vumc.nl

	ABSTRACT

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PURPOSE: We investigated whether application of positron emission tomography (PET) immediately after first presentation might simplify staging while maintaining accuracy, as compared with traditional strategy in routine clinical setting.

METHODS: At first presentation, patients with a provisional diagnosis of lung cancer without overt dissemination were randomly assigned to traditional work-up (TWU) according to international guidelines or early PET followed by histologic/cytologic verification of lesions, or imaging and follow-up. Patients with [¹⁸F] fluorodeoxyglucose (¹⁸FDG) –avid, noncentral tumors without suspicion of mediastinal or distant metastases on PET proceeded directly to thoracotomy. Follow-up in presumed benign lesions was at least 12 months. In patients treated with surgery or neoadjuvant therapy, the quality of staging was measured by comparing the clinical stage to the final stage (combination of peroperative staging and 6 months of follow-up). To investigate test substitution, we analyzed the number of (non)invasive tests to achieve clinical TNM staging, and its associated costs.

RESULTS: Between 1999 and 2001, 465 patients (233 TWU, 232 PET) were enrolled at 22 hospitals. The mean (standard deviation) number of procedures to finalize staging was equal in the TWU arm and the PET arm: 7.9 (2.0) v 7.9 (1.9), P = .90, respectively. Mediastinoscopies occurred significantly less often in the PET arm. Agreement between clinical and final stage was good in both arms ( = .85 v .78; P = .07). Costs did not differ significantly.

CONCLUSION: Up-front ¹⁸FDG-PET in patients with (suspected) lung cancer does not reduce the overall number of diagnostic test, but it maintains quality of TNM staging with the use of less invasive surgery.

	INTRODUCTION

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Evaluation of patients suspected of non–small-cell lung cancer (NSCLC) includes diagnosis and staging of the primary lesion and assessment of the extent of locoregional and metastatic spread. [¹⁸F] fluorodeoxyglucose positron emission tomography (¹⁸FDG-PET) provides useful information in NSCLC staging. The focus of research beyond accuracy measures focused on the added value of PET to conventional work-up if positioned just before surgery.^1-5 Results of accuracy studies suggest however, that application of PET up front in NSCLC diagnostic work-up could also be considered to simplify and improve staging and patient management. PET applied early in the diagnostic process might reduce the number of investigations, iatrogenic morbidity, and diagnostic delay, and facilitate rapid institution of curative or palliative therapy. Costs of diagnosis and therapy might be reduced if verification of a single decisive lesion suffices to assign appropriate treatment.

The aim of this randomized trial was to investigate whether application of PET as an up-front whole-body test improves the process of staging patients suspected to have NSCLC without losing accuracy at reasonable costs.

	METHODS

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Patients
Immediately after clinical suspicion of lung cancer had arisen based on history, physical examination, and chest x-ray, patients were invited to participate. Additional inclusion criteria were absence of clinically overt disseminated disease at first presentation, age greater than 18 years, and being medically fit for staging and surgery. Exclusion criteria were pregnancy and diabetes. Patients had to give written informed consent according to local ethics committee regulations. Twenty community hospitals and two university hospitals recruited patients.

Procedures
Patients were randomly assigned to "traditional" (TWU) or "PET up-front" work-up (PET), centrally by computer, by a permuted block design, stratified by institute and (Eastern Cooperative Oncology Group [ECOG]) performance score (0 or 1 v 2 or 3). Patients allocated to TWU underwent imaging (without ¹⁸FDG-PET) and invasive procedures to establish diagnosis and assess operability and resectability according to international guidelines.⁶ Staging in the PET group started with a ¹⁸FDG-PET scan, which was interpreted in conjunction with available clinical information and chest x-ray. PET scans were performed within 1 week after random assignment. In either arm, suspected locoregional and hematogenous metastases had to be verified by biopsy, or when this was not possible, by imaging and follow-up. In the PET arm, invasive confirmation was advised if PET suggested mediastinal lymph node involvement but no distant metastases. Mediastinoscopy was advised if the primary tumor appeared adjacent to the mediastinum at PET, for the reasoning that the spatial resolution of PET does not allow separation of neighboring mediastinal nodes and primary tumor.^7,8 Surgery was recommended if the primary lung lesion was ¹⁸FDG avid without evidence of mediastinal involvement and distant metastases.⁷ Since ¹⁸FDG-PET is relatively insensitive for brain metastases, clinicians were instructed to perform computed tomography (CT) or magnetic resonance imaging of the brain if clinically indicated. A "wait-and-see" policy was acceptable if the primary lung lesion was negative at ¹⁸FDG-PET. However, when clinicians still wanted further diagnostic information they were instructed to perform staging procedures according to standard practice. All tests and procedures other than PET, including treatment and follow-up, were performed in the referring hospitals. Follow-up (up to 1 year after random assignment) consisted of 3 monthly visits, including at least physical examination, chest x-rays, or imaging of indicator lesions in case of a "wait-and-see" policy. Figure 1 summarizes the study design. Stages were recorded using the TNM system.⁹

View larger version (10K): [in this window] [in a new window]   Fig 1. (A) Random assignment; (B) positron emission tomography (PET) strategy: mediastinum [18F] fluorodeoxyglucose (18FDG) –positive; (C) PET strategy: mediastinum 18FDG-negative. NSCLC, non–small-cell lung cancer; CT/MRI, computed tomography/magnetic resonance imaging; M, metastases; 4R, right tracheobronchial lymph node; 4L, left tracheobronchial lymph node; 7, carinal lymph node.

Data Analysis
In each patient, clinical stage assigned by the attending clinician was compared to the final TNM stage established at surgery and/or follow-up. The attending physician assigned a "clinical stage" (c-TNM) using the results of pretherapeutic diagnostic tests. This "c-TNM" stage was compared with the final stage as established by (1) biopsy and/or imaging test results and 6 months follow-up (typically patients with stage IIIB/IV), (2) a combination of surgicopathologic staging and 6 months' follow-up (thoracotomy patients), (3) the results at 12 months after random assignment in patients with a provisional diagnosis of a benign primary lesion. In patients who had no thoracotomy due to presumed distant metastasis, and in whom imaging rather than pathology results had been used to establish the final stage, an adjudication committee of three experienced pulmonary physicians (P.P.O., A.W., H.J.G.) reviewed the records to decide whether this clinical classification had been appropriate. We considered staging of lung lesions proving to be metastasis from a primary tumor not identified at clinical work-up as incorrect. If the presenting lung lesion proved to be a single metastasis from a previously known tumor, clinical stage was considered correct provided that no new metastases of the same malignancy became apparent within 6 months. All tests were recorded including procedures to assess resectability and operability (medical fitness). We classified tests as noninvasive (laboratory, functional tests [including ventilation/perfusion scintigraphy, lung and cardiological function tests], and imaging) and invasive (biopsies, surgical procedures).

Outcome Measures
Primary outcome measure was the number of tests and procedures to finalize staging and to define operability. Quality of staging was assessed with the number of correctly clinically staged patients compared with the final stage as determined at surgery and/or follow-up. Secondary outcome measures included duration of diagnostic processes, morbidity due to complications of diagnostic procedures, and costs of diagnostic and therapeutic processes.

Costs
We calculated total costs from a hospital perspective, implying that only direct medical costs were taken into account. These costs consisted of diagnostic tests (ie, investigations to assess functional operability, staging procedures), therapeutic interventions (ie, thoracotomy, chemotherapy, radiotherapy), outpatient visits, and hospital admissions.

The full costs of the various diagnostic and therapeutic procedures were calculated using the microcosting approach,¹¹ including costs of personnel, materials, depreciation, and overhead, calculated as average costs from one general and one university hospital based on 2003 Dutch prices. The costs of ¹⁸FDG-PET included costs of personnel, depreciation and maintenance, ¹⁸FDG, and overhead.³

Research Support
This study was supported by a grant of ZonMw Program the Netherlands Organization for Health Research and Development, Health Care Efficiency Research Program.

Statistical Analysis
The primary end point was reduction of number of diagnostic investigations. In an earlier observational study in two participating hospitals, at least three (mean, 3.2; standard deviation [SD], 1.6) diagnostic procedures in half of the patients were performed on top of bronchoscopy, chest x-ray, laboratory, lung function and cardiovascular tests, and thoracotomy.¹² Here, we considered the PET up-front strategy clinically useful if the proportion of patients needing at least three tests would be reduced from 50% to 30%. Furthermore, we anticipated to include 30% with other histologies (eg, small-cell lung cancer, benign lung diseases) for which PET might have a different impact. Therefore, to sufficiently reliably assess the impact in the patient sample of interest its size was increased by 30%, to a total of 465. Differences in the number of different combinations of tests and duration of diagnostic processes were tested with a t test.

Decreasing the number of diagnostic procedures should not result in reduction of quality of staging. The latter was measured by overall agreement between clinical and final TNM stage using statistics. Considering NSCLC patients only, we applied weighted statistics ( has a maximum of 1.0 with perfect agreement; zero indicates no agreement better than chance). Costs data were compared with two-sided Wilcoxon-Mann-Whitney tests.

	RESULTS

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Baseline Characteristics
Between September 1999 and June 2001, 2,114 potential patients were seen in the 22 participating hospitals, of which 465 (22%) were enrolled in this study, 233 in the TWU group, and 232 in the PET group. One patient allocated to TWU declined further investigations after random assignment. Two patients allocated to PET declined PET, and nine allocated to TWU underwent PET. All patients were included in the "intention-to-diagnose" analysis. Baseline characteristics such as age, sex, ECOG performance scores, weight loss, comorbidity, and history of malignancy were well balanced in both groups (Tables 1 and 2). Initial clinical staging did not differ significantly between TWU and PET group (Tables 2 and 3). In the 38 reviewed records of patients with presumed stage IV, in whom imaging rather than pathology results established the final stage, classification was considered to be appropriate.

All patients staged as I/II and IIIa in the TWU arm underwent recommended tests (laboratory tests, chest x-ray, and CT of chest through liver and adrenals). In patients with stage I/II invasive mediastinal mediastinoscopy staging was performed in 66% (56 of 85; 95% CI, 0.55 to 0.76), and in 45% at least one test procedure (except CT of chest through liver and adrenals) was done to identify distant metastases (38 of 85; 95% CI, 0.34 to 0.56). In patients with clinical stage IIIa invasive mediastinal mediastinoscopy staging was performed in 74% (14 of 19; 95% CI, 0.49 to 0.91), at least one additional test to screen for distant metastases (except CT of chest through liver and adrenals) in 42% (eight of 19; 95% CI, 0.20 to 0.67).

Functional tests were evenly distributed among the two groups (Table 4) , as were tests aiming at diagnosis and staging. In the PET arm, clinicians used two tests less per ten patients specifically aiming at distant metastases compared with the TWU arm (excluding PET and initial chest CT; mean [SD]: 0.85 [1.09] and 0.63 [1.07]; TWU and PET, respectively; P = .018). The number of patients that required at least one invasive procedure for mediastinal staging was significantly lower (P < .0001) in favor of the PET arm. The total number of procedures for locoregional staging (bronchoscopy, chest CT, PET, mediastinal staging, thoracotomy) was similar in both groups (mean [SD] 3.8 [1.1] and mean [SD] 3.9 [1.2]; for TWU and PET, respectively; P = .081).

Follow-Up
In either group, one of the primaries presumed benign proved to be malignant during follow-up. Three and six (TWU; PET) patients clinically staged as I/II NSCLC had distant relapses within 6 months after random assignment (ie, 5%; nine of 177) of all stage I/II patients. Of these, three and four (TWU; PET) relapsed after apparently curative surgery (two did not undergo surgery). Of the patients (TWU, n = 19; PET, n = 16) with pathologically proven stage IIIA, one and three patients (TWU; PET) were diagnosed as having stage IV disease within 6 months after random assignment.

Secondary Outcomes
Staging in the TWU and PET group in 22 different hospitals required a median of 23 days (range, 1 to 193) and 14 days (range, 1 to 106; P < .0001). Patients in the TWU (n = 88) and PET (n = 96) group underwent thoracotomy after clinical staging at a median of 16 (range, 4 to 116) and 18 days (range, 1 to 152), respectively (excluding delayed surgery due to presumed benign lesions in four patients). Other reasons for "delayed" surgery included patient refusal (n = 1) and comorbidity (n = 1). Morbidity due to staging procedures other than surgery was evenly distributed. Morbidity due to thoracotomy (including cardiac and cerebral events, renal insufficiency, prolonged mechanical ventilation, bleeding, and infections) was observed in 41% and 30% (TWU and PET, respectively; P = .17). Seven TWU (8%) and 11 PET (11%) patients required surgical reintervention for bleeding, bronchopleural fistula, irradical resection, cardiac tamponade, or empyema. Sixteen (18%) and 21 (22%) patients (TWU and PET, respectively) were readmitted to the general ward or intensive-care unit within 30 days after surgery. Surgical mortality occurred in four TWU (4.5%) and two PET patients (2.1%).

Costs
Estimated cost of ¹⁸FDG-PET was $1,557. Costs of diagnostic and therapeutic procedures were $11,351 in the TWU group and $12,581 in the PET group (P = .14; Table 6).

	DISCUSSION

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The randomized design and the participation of physicians and patients from 22 predominantly community based hospitals strengthens the external validity of the study. From data of the National Cancer Registry we estimate that 22% of all patients diagnosed with NSCLC (stage I to IV) in participating hospitals were randomized, which is substantially higher than the 5% to 9% quoted in therapy trials in lung cancer but markedly lower than the 65% in a former ¹⁸FDG-PET trial.^2,16,17 A limitation of our study was that the level of clinical experience with ¹⁸FDG-PET was variable among institutions. Further, due to the up-front positioning of PET, PET scans were not read in conjunction with CT which is known to improve the accuracy of either test.¹⁰ This practice was enforced by the multicentric nature of the study with ¹⁸FDG-PET and CT being performed ‘on-site’ (allowing coreading of scans) in only two of 22 hospitals.

Even though the present study did not aim to measure impact on patient outcomes, it appears that there was a trend towards less futile surgery (benign lesions, per- or postoperative upstaging) in the TWU arm (20%) than in our previous experience.^2,12 In the PLUS trial, where addition of ¹⁸FDG-PET to TWU was studied, futile surgery was observed in 30% of patients in the conventional arm at 6 months after random assignment. Our ¹⁸FDG-PET data are difficult to compare with other studies^2,5,7,18 since our key issue was substitution rather than added value of PET.

In conclusion, even though up-front ¹⁸FDG-PET in patients with (suspected) lung cancer does not simplify staging, it still provides good quality TNM staging with the use of less invasive surgery. Further research should determine whether up-front positioning of PET-CT (rather than PET and CT alone) might be a cost-effective alternative for current practices.

	Appendix

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The POORT study group participants

G.M. Wittebrood-Smit, E.M. Mathijssen- de Ruiter (Comprehensive Cancer Center Amsterdam, Amsterdam)

N. van Zandwijk (Antoni van Leeuwenhoek ziekenhuis, Amsterdam)

B. Biesma (Bosch MediCentrum, 's Hertogenbosch)

W.F.M. Strankinga (Boven I.J. ziekenhuis, Amsterdam)

J. Kraan (Delfzicht ziekenhuis, Delfzijl)

J.Ph.G. Kaajan (Deventer ziekenhuis, Deventer)

P.C. Dekker (Gemini ziekenhuis, Den Helder)

P.J. Teengs, M.A. Sulzer (Kennemer Gasthuis, Haarlem)

G.D. Nossent (Martini ziekenhuis, Groningen)

J. Nabers (Medisch Centrum Leeuwarden, Leeuwarden)

J. Schouwink (Medisch Spectrum Twente, Enschede)

P. Eppinga (Nij Smellinghe, Drachten)

H.B. Kwa (Onze Lieve Vrouwe Gasthuis, Amsterdam)

W. de Kanter Koppenol (Rode Kruis Ziekenhuis, Beverwijk)

C. Jie (Sint Lucas/Andreas, Amsterdam)

G. Visschers (Slotervaart ziekenhuis, Amsterdam)

F.J.M. van Breukelen, A.H.M. van der Heijden (Spaarne ziekenhuis, Haarlem)

R.A.L.M. Stallaert (West Fries Gasthuis, Hoorn)

J. Berkovits (Ziekenhuis Amstelveen, Amstelveen)

P.J.H. Janssen (Ziekenhuis Hilversum, Hilversum)

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Author Contributions

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

 

Conception and design: Otto S. Hoekstra, Egbert F. Smit, Harm van Tinteren, Carin A. Uyl-de Groot, Maarten Boers, Pieter E. Postmus, Gerrit J. Teule, Harry J. Groen Administrative support: Gerarda J. Herder, Henk Kramer, Emile F. Comans Provision of study materials or patients: Gerarda J. Herder, Emile F. Comans, Alle Welling, Marinus A. Paul Collection and assembly of data: Gerarda J. Herder, Paul Verboom Data analysis and interpretation: Gerarda J. Herder, Otto S. Hoekstra, Egbert F. Smit, Harm van Tinteren, Harry J. Groen Manuscript writing: Gerarda J. Herder, Otto S. Hoekstra, Egbert F. Smit, Harry J. Groen Final approval of manuscript: Otto S. Hoekstra, Egbert F. Smit, Jan Pruim, Maarten Boers, Pieter E. Postmus, Gerrit J. Teule, Harry J. Groen

 

	NOTES

 
Supported by a grant from the ZonMw Program, the Netherlands Organization for Health Research and Development, and the Health Care Efficiency Research Program.

Presented orally at the 40th Annual Meeting of the American Society of Clinical Oncology, June 5-8, 2004.

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

	REFERENCES

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Submitted April 24, 2005; accepted October 26, 2005.

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