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Prognostic Value of Fluorine-18 Fluorodeoxyglucose Positron Emission Tomography Imaging in Patients With Advanced-Stage Non–Small-Cell Lung Carcinoma

Jenny K. Hoang, Luke F. Hoagland, R. Edward Coleman, April D. Coan, James E. Herndon, II, Edward F. Patz, Jr

From the Departments of Radiology and Pharmacology and Cancer Biology, and Cancer Center Biostatistics, Duke University Medical Center, Durham, NC

Corresponding author: Edward F. Patz Jr, MD, Department of Radiology, Duke University Medical Center, Erwin Rd, Durham, NC 27710; e-mail: patz0002{at}mc.duke.edu

	ABSTRACT

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Purpose To determine whether the amount of fluorine-18 fluorodeoxyglucose (FDG) uptake in the primary lung cancer on positron emission tomography (PET) imaging at the time of presentation has prognostic significance in patients with advanced-stage non–small-cell lung cancer (NSCLC).

Patients and Methods A retrospective review identified 214 patients with advanced-stage NSCLC (stage IIIA, IIIB, and IV) who underwent FDG PET study at the time of diagnosis. Extensive clinical data, including tumor histologic cell type, pathologic stage at presentation, and treatment, were recorded. The maximum standardized uptake value (SUV_max) in the primary tumor on FDG PET on survival was examined using Cox proportional hazards regression.

Results One hundred fifty-eight (74%) of the 214 patients died and 56 patients were reported alive at 27 months (range, 3 to 140 months) after the diagnosis of NSCLC. Using the median SUV_max of 11.1, the patient population was subdivided. The median survival of the 106 patients with the primary tumor having an SUV_max less than 11.1 was 16 months (95% CI, 12 to 21 months), whereas the median survival of the 108 patients with the primary tumor having an SUV_max 11.1 was 12 months (95% CI, 10 to 15 months). Univariate and multivariate analysis did not provide evidence that survival for patient subgroups defined by the median SUV_max were significantly different (univariate P = .11; multivariate P = .45).

Conclusion FDG uptake of the primary lesions in patients with a new diagnosis of advanced-stage NSCLC does not have a significant relationship with survival.

	INTRODUCTION

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Lung cancer is the leading cause of cancer death in both men and women in the United States.¹ The majority of patients present with advanced-stage disease (stage III and IV) and are inoperable. The overall 5-year survival rate is less than 9%,² although there is a subset of these patients who have prolonged survival.^3-5 A method of selecting patients who have a better prognosis could influence treatment decisions and potentially reduce therapeutic toxicity, with the ultimate goal of improving survival.

The variation in survival and response to treatment is multifactorial, but stage at presentation, performance status, and more recently, genomic patterns all seem to influence outcome.^6-9 A number of studies have found that metabolic activity on fluorine-18 fluorodeoxyglucose positron emission tomography (FDG PET) in patients with early-stage non–small-cell lung cancer (NSCLC) is correlated with tumor doubling time and survival.^10-22 However, for patients with advanced-stage NSCLC, studies have been limited by small number of patients.^19,22,23 It remains uncertain whether FDG PET in patients with advanced-stage NSCLC will provide prognostic information. We performed a retrospective review of 214 patients with stage III and IV NSCLC who underwent FDG PET at initial presentation to determine whether maximum standardized uptake values (SUV_max) are correlated with survival.

	PATIENTS AND METHODS

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Patient Population
This study was approved by our institutional review board. We retrospectively reviewed the tumor registry at our institution and identified all patients diagnosed with advanced-stage NSCLC (stage III and IV) between January 1992 and December 2000. Patients were required to have undergone an FDG PET study at the time of establishing a pathologic diagnosis, to have received no treatment before the study, and to have had at least 3 months of follow-up.

There were 214 patients, 84 women and 130 men, with a mean age of 63.1 years (range, 37 to 89 years), who met these criteria. Two hundred five patients had histologic confirmation before FDG PET, with a median interval of 22 days (range, 0 to 92 days). There were nine patients who underwent PET before histologic diagnosis, with a median interval of 13 days (range, 1 to 91 days).

Tumor histologic cell type, stage at presentation, site of metastasis, and treatment were recorded from the patient's medical record. Histologic diagnosis was made by transthoracic needle aspiration or transbronchial biopsy. A clinical stage at presentation was assigned according to the new International Staging System.^2,24,25 Cases of malignant pleural effusion were designated as wet stage IIIB NSCLC. Dry stage III included all stage IIIA and stage IIIB without malignant pleural effusion.

PET Imaging
All patients were instructed to fast for at least 4 hours before intravenous administration of 145 µCi/kg (maximum of 20 µCi) of F-18 FDG. Blood sugar levels were obtained on all patients and were required to be less than 200 mg/dL before the intravenous administration of the FDG. Imaging of the chest was begun at 1 hour (±15 minutes) after injection of the radiopharmaceutical. Between January 1992 and January 1993, PET scans were performed using a GE 4096 Plus (General Electric Medical Systems, Milwaukee, WI). After January 1993, PET imaging was performed on a GE Advance unit (General Electric Medical Systems). Attenuation-corrected images of the chest were obtained using a germanium-68 transmission source and protocols in routine use at the time.

The images were reviewed on an interactive video display provided by the equipment manufacturer. The maximum standardized uptake value (SUV_max) was quantitatively used to determine FDG PET activity. SUV_max was defined as maximum tumor concentration of FDG divided by the injected dose, corrected for the body weight of the patient: (SUV_max = maximum activity concentration/[injected dose/body weight]). To obtain the SUV_max, all images were analyzed by a single investigator (J.K.H.) using a circular region of interest of 1.3 ± 0.2 cm² was placed over the lung primary tumor on the transaxial attenuation-corrected emission image at the site of maximum visualized FDG uptake. For larger tumors, the region of interest was moved over several sites within the mass to ensure that the true SUV_max was obtained.

Treatment and Follow-Up
After the PET study and a definitive diagnosis, 146 patients were treated with chemotherapy, 151 patients were treated with radiotherapy, and 48 patients were treated with surgical excision of the primary tumor. Of the patients who had surgical treatment, 16 received neoadjuvant chemotherapy, radiotherapy, or both. Twenty-nine patients received no treatment. Survival data were obtained from the tumor registry and verified on review of the medical records. Survival time was defined as the date from histologic diagnosis to date of death or last follow-up.

Data Analysis
Integer values between 5 and 20, as reported in prior studies, were evaluated with log-rank probability values to determine a prognostic cutoff point for SUV_max. Because no statistically significant value was found, SUV_max was dichotomized at its median of 11.1. Univariate Cox proportional hazards modeling was used to quantify the risk for death as a function of sex, stage, age, histology, treatment, and dichotomized SUV_max. Multivariate Cox proportional hazards models were used to assess the potential independent effects for SUV_max after adjustment for the effects of other significant variables. From these models, risk estimates, estimated by hazards ratios (HR), and 95% CIs were calculated. Kaplan-Meier methods were used to estimate survival probabilities.

	RESULTS

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Patient Follow-Up and SUV
Of the 214 patients enrolled, 158 patients had died and 56 patients were reported alive with a median follow-up of 27 months (range, 3 to 140 months). In this population of 214 patients, SUV_max ranged between 2.3 and 39.5, with a mean of 12.4 (standard deviation [SD] = 6.2) and a median of 11.1. Given that there was no discriminative cutoff SUV_max for prognosis, the study population was divided into two groups determined by the median primary tumor SUV_max of 11.1 (mean = 12.3; SD = 6.1; range, 2.3 to 39.5). Mean SUV_max of variables, age, sex, histology, stage, and treatment are listed in Table 1. Descriptive statistics for the two groups (SUV_max < 11.1, SUV_max 11.1) are listed in Tables 1 and 2.

The median survival of 108 patients (77%) with the primary tumor having SUV_max 11.1 was 12 months (95% CI, 10 to 15 months). Twenty-five (23%) of the 108 patients with SUV_max 11.1 who were alive at follow-up had a median follow-up period of 25 months (range, 3 to 88 months).

Kaplan-Meier survival curves for SUV_max subgroups (SUV < 11.1, SUV 11.1) are shown in Fig 1. Survival difference between patients with SUV_max less than 11.1 and SUV_max 11.1 were not statistically significant (P = .11). The effect of an uncategorized SUV_max on survival was also not statistically significant (P = .77).

View larger version (10K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Survival among patients with advanced-stage non–small-cell lung cancer patients stratified by maximum standardized uptake value (SUVmax). There was no statistically significant difference in survival for patients with SUVmax less than 11.1 and SUVmax 11.1 (P = .11).

The difference in survival of patients with dry stage III disease stratified by median SUV_max of 11.1 was not statistically significant (P = .067; Fig 2). The difference in survival of patients with wet stage IIIB/IV disease also categorized by median SUV_max of 11.1 was not statistically significant (P = .55; Fig 3). On multivariate Cox proportional hazards models, assessing the joint effects of stage of disease (dry stage III, wet stage IIIB/IV) and SUV_max on survival was not significant (P = .086 for categorized SUV_max, P = .64 for continuous SUV_max).

View larger version (13K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Survival in patients with dry stage III non–small-cell lung cancer patients stratified by maximum standardized uptake value (SUVmax).

View larger version (12K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 3. Survival in patients with wet stage IIIB/IV non–small-cell lung cancer stratified by maximum standardized uptake value (SUVmax).

	DISCUSSION

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Lung cancer has been the most common cancer in the world since 1985 and is increasing globally.²⁶ By 2002, there were 1.35 million new cases, representing 12.4% of all new cancers.²⁷ It is a highly lethal disease and is the most common cause of death from cancer.^1,27 The long-term survival of patients with advanced NSCLC remains poor and is typically less than 9% at 5 years, with a reported 4- to 6-month median survival.^2,28,29 New diagnostic and treatment strategies are essential to impact survival rates of patients with lung cancer. This study specifically focused on the role of FDG PET in providing prognostic information for patients with advanced-stage NSCLC.

FDG PET has become a valuable tool for evaluating patients with NSCLC.³⁰ It has proved valuable in differentiating benign from malignant pulmonary nodules and in staging patients. Studies have also demonstrated that PET can stratify patients with early-stage NSCLC, and the amount of FDG uptake can predict overall survival.^10-22

The current study shows that for patients with advanced-stage III and IV NSCLC, no correlation was found between survival and FDG PET activity, as measured by SUV_max in the primary tumor. Further distinction between wet stage IIIB/stage IV disease treated with palliative management versus dry stage III patients who could be treated with radical intent also shows that SUV_max has no prognostic value. These data are in contrast with several studies reporting a significant relationship between cutoff SUV of between 5 and 20 and adverse prognosis.^10-22 Because the current study focused only on advanced-stage NSCLC, the patient population could explain differences in results. Only a minority of other small series investigating FDG PET for NSCLC prognosis included stage IV disease. One of these studies by Ahuja et al²³ stratified FDG uptake and survival results by stage but was limited by the small number of patients with advanced NSCLC. The study included 55 patients with stage III and 31 patients with stage IV disease. Kaplan-Meier curves for these groups seem to show a statistical trend, but the significance for advanced-stage disease was not reported.

A recently published report by Vesselle et al¹⁹ also was in contrast with the other studies and concluded that FDG uptake did not provide prognostic information. The authors believe the main difference in their study was that a size correction was applied to the tumor SUV to more accurately account for partial volume effect of PET resolution in small tumors. Although our study did not consider tumor size or apply this correction, we also find that FDG PET provides no prognostic information. An alternate explanation for Vesselle's results may also be a difference in the study population, which consisted of 49% stage III and IV NSCLC that was not analyzed separately from the early-stage NSCLC. If there were a relationship between SUV and survival in early-stage disease, combining all stages may diminish the correlation between SUV and survival.

The main prognostic factor in our study was still tumor stage. Stage IIIA and stage IIIB disease were compared with stage IV, with hazard ratios of 0.38 and 0.53, respectively. The risk of dying among patients with wet stage IIIB/IV was 2.1 times greater than patients with dry stage III disease.

We recognize several limitations of this study. Most notably is that it was a retrospective review over a long period of time with variations in treatment protocols. The nonuniform management, however, is unlikely to impact on our results, because several studies show that the prognosis of advanced NSCLC has not changed significantly over the study period and beyond.^31-33 There may have been selection bias, which is reflected in our overall favorable survival results compared with those reported in the published literature. There may also be variability in obtaining SUVs in newly diagnosed lung cancer, as has been recently reported by Marom et al.³⁴ Some of this variability may be due to factors including blood glucose, time to imaging, and reconstruction algorithms, but we attempted to limit variability by assuring glucose levels less than 200 mg/dL, using studies obtained 45 to 75 minutes after injection of the FDG, identifying the maximal uptake in the nodule, using SUV_max, and having a single observer to perform the analysis. Marom et al reported excellent interobserver and intraobserver agreement in the study environment.³⁴ Tumor size before treatment could not be documented, because for most cases, the computed tomography was not digitized and had been lost or destroyed. However, for advanced disease, the tumor size was large and partial volume effect described by Veselle¹⁹ was not an issue. In some cases, central necrosis or cavitation may have given a falsely low PET value.

In conclusion, there is insufficient evidence to suggest that the amount of FDG accumulation in advanced primary NSCLC provides prognostic information. Prior studies demonstrating a correlation between survival and FDG uptake were focused on patients with early-stage NSCLC. For advanced disease, decisions regarding management options should not be made based on level of metabolic activity of the primary tumor on FDG PET. We find that stage of NSCLC even in the advanced stage is still the best predictor of survival.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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Although all authors completed the disclosure declaration, the following author(s) indicated a financial or other interest that is relevant to the subject matter under consideration in this article. Certain relationships marked with a "U" are those for which no compensation was received; those relationships marked with a "C" were compensated. For a detailed description of the disclosure categories, or for more information about ASCO's conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors.

Employment or Leadership Position: None Consultant or Advisory Role: R. Edward Coleman, General Electric Healthcare (C) Stock Ownership: R. Edward Coleman, RCOA Honoraria: R. Edward Coleman, Alliance Imaging Research Funding: R. Edward Coleman, General Electric Healthcare Expert Testimony: None Other Remuneration: None

	AUTHOR CONTRIBUTIONS

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Conception and design: Jenny K. Hoang, Edward F. Patz Jr

Administrative support: Jenny K. Hoang, Luke F. Hoagland, R. Edward Coleman, Edward F. Patz Jr

Provision of study materials or patients: Jenny K. Hoang, Luke F. Hoagland, R. Edward Coleman, Edward F. Patz Jr

Collection and assembly of data: Jenny K. Hoang, Luke F. Hoagland, R. Edward Coleman, Edward F. Patz Jr

Data analysis and interpretation: Jenny K. Hoang, R. Edward Coleman, April D. Coan, James E. Herndon II, Edward F. Patz Jr

Manuscript writing: Jenny K. Hoang, R. Edward Coleman, April D. Coan, James E. Herndon II, Edward F. Patz Jr

Final approval of manuscript: Jenny K. Hoang, R. Edward Coleman, April D. Coan, James E. Herndon II, Edward F. Patz Jr

	NOTES

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

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Submitted September 8, 2007; accepted December 3, 2007.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hoang, J. K. Articles by Patz, E. F. Search for Related Content PubMed PubMed Citation Articles by Hoang, J. K. Articles by Patz, E. F., Jr Social Bookmarking                            What's this?