Journal of Clinical Oncology, Vol 22, No 16 (August 15), 2004: pp. 3255-3260
© 2004 American Society of Clinical Oncology.
DOI: 10.1200/JCO.2004.11.109
Preoperative F-18 Fluorodeoxyglucose-Positron Emission Tomography Maximal Standardized Uptake Value Predicts Survival After Lung Cancer Resection
Robert J. Downey,
Timothy Akhurst,
Mithat Gonen,
Alain Vincent,
Manjit S. Bains,
Steven Larson,
Valerie Rusch
From the Thoracic Surgery Service, the Division of Nuclear Medicine, and the Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY
Address reprint requests to Robert J. Downey, MD, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021; e-mail: downeyr{at}mskcc.org
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ABSTRACT
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PURPOSE: A retrospective review of surgically treated lung cancer patients imaged preoperatively by F-18 fluorodeoxyglucose–positron emission tomography ([18F]FDG-PET) to determine if the primary tumor standardized uptake value (SUV) predicts survival.
PATIENTS AND METHODS: Non–small-cell lung cancer or carcinoid pT1–4, N0–2, M0 patients treated by R0 surgical resection alone were imaged with computed tomography scan and PET within 90 days before surgery. Prognostic variables were assessed by log-rank test; survival was assessed by the method of Kaplan and Meier.
RESULTS: One hundred consecutive patients (48 men, 52 women) were retrospectively reviewed. Median follow-up for surviving patients was 28 months (range, 16 to 81 months). Median maximal SUV (SUVMAX) was 9. The 2-year survival for patients with SUVMAX more than 9 was 68% and for those with SUVMAX less than 9, it was 96% (P < .01, log-rank test). In a multivariate analysis including pathologic tumor size, involved nodes, histology, and SUVMAX, only tumor size (T) more than 3 cm and SUVMAX more than 9 and their interaction were significant predictors of survival (P = .01, 0.02, and < 0.01, respectively). The 3-year survivals for patients with both T less than 3 cm and SUVMAX less than 9 was 97%; for those with T less than 3 cm and SUVMAX more than 9, it was 94%; for those with T more than 3 cm and SUVMAX less than 9, it was 93%; and for those with T more than 3 cm and SUVMAX more than 9, it was 47% (P < .01).
CONCLUSION: In surgically managed lung cancer patients, SUV is a predictor of overall survival after resection. The addition of SUVMAX to pathologic tumor size identifies a subgroup of patients at highest risk for death as a result of recurrent disease after resection.
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INTRODUCTION
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F-18 fluorodeoxyglucose ([18F]FDG) positron emission tomography (PET) is a novel imaging technique based on the increased rate of glucose use commonly seen in malignancy. The earliest application of PET imaging in oncology has been in clinical staging, suggesting that PET could identify potential sites of disease undetected by standard imaging studies.1 More recently, the rate of [18F]FDG uptake in the primary site of a non–small-cell lung cancer (NSCLC) has been correlated with tumor doubling time2 and proliferation rates3,4 which, in turn, are known to correlate with tumor aggressiveness.5-7 On the basis of these observations, it has been suggested that the intensity of [18F]FDG uptake as measured by PET imaging (the maximal standardized uptake value [SUVMAX]) in the primary tumor may predict overall survival.
To better understand the potential contribution of SUV to determining prognosis, we reviewed the records of the first 100 patients with surgically treated lung cancer after PET imaging at Memorial Sloan-Kettering Cancer Center (MSKCC). Data were analyzed to determine whether SUV predicted the likelihood of lymph node involvement and of prolonged survival after resection, and if so, whether SUV was an independent prognostic factor for survival from components of pathologic tumor-node-metastasis system staging.
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PATIENTS AND METHODS
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The medical records of 100 consecutive patients meeting the following criteria comprised the study population. Patients had to have histologically proven NSCLC or carcinoid pathologic T1–4, N0–2, M0 treated by R0 resection, including wedge resections, with either mediastinal lymph node sampling or dissection; no neoadjuvant or adjuvant therapy; survived the postoperative period; no metachronous lung cancers treated for at least 2 years before or after the study period; computed tomography (CT) scan and PET imaging performed within 90 days of lung cancer surgery; PET imaging performed at MSKCC only; and follow-up for survival analysis of at least 16 months. In addition, patients with nonlung malignancies were eligible unless either the disease would make PET difficult to interpret (for example, mediastinal lymphoma) or the treatment included chemotherapy or thoracic radiation therapy within 2 years of treatment for lung cancer.
This review was performed after approval had been obtained from the MSKCC Institutional Review Board, and in accord with an assurance filed with and approved by the Department of Health and Human Services.
Technique of [18F]FDG Whole-Body PET
PET was performed on a conventional full-ring, high-resolution dedicated positron emission tomograph, the GE Advance (GEMS, Milwaukee, WI; n = 96) or the CTI Biograph scanner (CTI, Knoxville, TN; n = 4). The patients were injected with pyrogen-free [18F]FDG 10 to 15 mCi and were instructed previously to fast for at least 6 hours before scanning. All images were iteratively reconstructed using postemission transmission attenuation-corrected data sets. Region of interest analysis tools, shipped with the scanners, were used to calculate the maximal [18F]FDG concentration within the primary tumor mass. SUVMAX values were obtained by correcting for the injected dose and the patient’s weight, again using the standard software tools provided with the scanners. For the purposes of this study, only uptake in the primary site was analyzed.
Staging
After review of all available clinical information including the surgical pathology reports, patients were assigned a T, N, and overall tumor-node-metastasis system stage according to the American Joint Committee on Cancer staging system.8 Tumor size and histologic type also were determined from postresection pathology reports.
Statistical Analysis
Overall survival was defined as the time interval from date of R0 resection until death as a result of any cause or date of last follow-up. Survival probabilities were estimated by the method of Kaplan and Meier. Prognostic variables were assessed by using receiver operating curves analysis and the area under the curves was calculated using the trapezoidal rule. The prognostic variables tumor size and SUVMAX were stratified by the median values to minimize the likelihood of inadvertent bias that could result using data-driven cutoffs. Significance of the differences between groups with respect to size or SUV was assessed using the Wilcoxon rank sum test. A multivariate model was built using proportional hazards regression. The assumption of proportional hazards was checked using weighted residuals.9
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RESULTS
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Patient Characteristics
From April 1996 and May 2001, 100 consecutive patients (48 men and 52 women) meeting the eligibility criteria for this study had PET imaging performed at MSKCC. The median follow-up for surviving patients was 28 months (range, 16 to 81 months). Additional staging included bone scan in 61 patients, brain imaging (either CT or magnetic resonance imaging) in 61 patients, and mediastinoscopy in 26 patients. A pneumonectomy was performed in five patients, lobectomy in 87 patients, bilobectomy in three patients, and wedge or segmentectomy in five patients. Additional components of the resection were rib resection and reconstruction in three patients, sternal resection and reconstruction in one patient, and diaphragmatic resection in one patient. The histology was squamous cell carcinoma in 24 patients, adenocarcinoma (including bronchoalveolar carcinoma) in 67 patients, adenosquamous cell carcinoma in two patients, large-cell carcinoma in three patients, and carcinoid in four patients.
PET and Pathologic Characteristics of Primary Site of Malignancy Related to Nodal Status and Survival
Uptake in squamous cell carcinomas tended to be higher than in adenocarcinomas (Figs 1A and 1B). The median SUVMAX of the squamous cell carcinomas (n = 24) was 13.3 ± 6.4 and the median SUVMAX of the adenocarcinomas (including bronchoalveolar carcinoma; n = 67) was 8.6 ± 6.0 (P < .01). Similarly, uptake in patients with pathologic nodal involvement also was higher than in those patients who were N0 (Figs 2A, 2B, and 2C). The mean SUV in N0 patients (n = 75) was 8.9 ± 6.3 and the mean SUV in N1–2 patients (n = 25) was 13.6 + 6.9 (P < .01).
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Fig 1. Histograms of distribution of standardized uptake value (SUV) of the primary tumor site in patients with (A) adenocarcinoma and (B) squamous cell carcinoma.
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Fig 2. Histograms of distribution of standardized uptake value (SUV) of the primary tumor site in (A) N0 patients, (B) N1 patients, and (C) N2 patients.
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The ability of pathologic tumor size and SUVMAX to predict nodal status (N1–2 v N0) is depicted by the receiver operating curve shown in Figure 3. For the most part, tumor size and SUV contain similar predictive information with respect to nodal status. Using the median values of 3 cm for tumor size yields a sensitivity of 64% (95% CI, 45% to 83%) and specificity of 65% (95% CI, 54% to 76%). The median SUV value of 9 corresponds to sensitivity of 72% (95% CI, 53% to 91%) and specificity of 57% (95% CI, 46% to 68%). The area under the curve for tumor size was 67% and for SUV was 71%. Sensitivity and specificity of SUV using different cutoffs are given in Table 1.
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Fig 3. Receiver operating characteristics curves for using pathologic tumor size and standardized uptake value (SUV) to predict nodal involvement.
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Tumor size in centimeters used as a continuous variable was correlated with survival (P = .01, proportional hazards regression analysis). Stratification of patients by the median tumor size (3.0 cm) predicted survival; the 2-year survival for patients with a tumor size more than 3 cm was 68% and for patients with a tumor size less than 3 cm, the 2-year survival was 96% (P < .01, log-rank test; Fig 4).
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Fig 4. Kaplan-Meier analysis of the relationship between primary tumor size (dichotomized using median value of 3 cm) and survival.
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SUVMAX analyzed as a continuous variable was correlated with survival (P = .01, proportional hazards regression analysis). A one-unit increase in SUVMAX corresponded to a 7% increase in the risk of death. Stratification of patients by the median SUVMAX, which was 9, also predicted survival; the 2-year survival for patients with SUVMAX more than 9 was 68% and the 2-year survival for patients with SUVMAX less than 9 was 96% (P < .01, log-rank test; Fig 5). SUVMAX more than 9 was associated with a five-fold increase in the risk of death when compared with SUVMAX less than 9.
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Fig 5. Kaplan-Meier analysis of the relationshop between standardized uptake value (SUV; dichotomized using median value of 9 cm) and survival.
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Histology was another significant factor in univariate analysis (P = .02). Patients with squamous cell carcinomas had 3.2 times more risk of death (95% CI, 1.3 to 7.9) when compared with those who had adenocarcinomas. Two-year survivals were 86% and 68% for adenocarcinomas and squamous cell carcinomas, respectively.
By multivariable analysis, which in addition to tumor size and SUVMAX included the presence of involved nodes and histology, only T more than 3 cm and SUVMAX more than 9 and their interaction were significant predictors of survival (P = .01, .02, and < .01, respectively).
Combining the two stratification variables, the 3-year survivals for patients were the following: with both a T less than 3 cm and SUVMAX less than 9, 97%; with both T less than 3 cm and SUVMAX more than 9, 94%; with T more than 3 cm and SUVMAX less than 9, 93%; and with both T more than 3 cm and SUVMAX more than 9, 47% (P = .07; Fig 6). In particular, patients with both T more than 3 cm and SUVMAX more than 9 had an eight-fold risk of death when compared with those patients with a T less than 3 cm and SUVMAX more than 9, and a 12-fold increase when compared with those with T more than 3 cm and SUV less than 9 (Table 2) .
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Fig 6. Relationship between standardized uptake value (SUV), pathologic tumor size, and overall survival.
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DISCUSSION
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Because treatment of lung cancer by surgery alone often leads to disappointing results, current investigations are directed toward developing combined-modality therapy, most often induction chemotherapy and surgery. Identification of the patients at the highest risk for recurrence after surgery has largely been based on the tumor-node-metastasis staging system; because of their poor prognosis, patients with N2 lymph node metastases10,11 and with large T2 lesions12 have been considered candidates for induction therapy. Preoperative clinical stage often differs from pathologic stage. Operative findings such as involved N1 nodes, if known preoperatively, may have led to combined-modality therapy rather than surgery alone.
CT allows accurate assessment of some tumor-node-metastasis system components such as tumor size, which have been shown to be associated with prognosis,13 but inadequately assesses other aspects such as N1 nodal involvement. [18F]FDG-PET imaging is based on the rate of glucose metabolism; with preliminary data suggesting that the rate of tumor metabolic activity may correlate with tumor aggressiveness, PET is a promising modality to complement the prognostic information provided by CT.
To date, the literature on the prognostic value of PET in surgically treated patients has been limited to NSCLC, and the published series, with one exception, mix surgically and medically treated patients. First, in 1998, Ahuja et al14 reported on 155 patients with newly diagnosed NSCLC imaged with PET and treated with multimodality therapy that included surgery in an unspecified number of patients. The median follow-up for surviving patients was 20.9 months. By multivariate analysis, the combination of SUV and lesion size was examined. Patients with lesions larger than 3 cm and an SUV more than 10 had a median survival less than 6 months, which was significantly worse than patients without both of these risk factors. Vansteenkiste et al15 retrospectively reviewed 125 untreated NSCLC patients imaged with PET. There were 82 patients treated with surgery alone (n = 82), but survival of this group was not analyzed separately. Surgical patients with a resected tumor less than 3 cm had a 2-year survival of 86% if the SUV was below 7 and 60% if the SUV was above 7. There were only four patients with an SUV more than 7 and a size less than 3 cm, and their 2-year survival was not specified. Patients with both an SUV more than 7 and a size more than 3 cm had a 2-year survival of 43%. Dhital et al16 retrospectively reviewed 77 patients with untreated lung cancer imaged with PET. PET imaging of the thorax only was performed and there were no details given about either the tumor-node-metastasis system stage of these patients or their treatment. The authors noted a correlation between SUVMAX of the primary tumor and survival, with the likelihood of survival at 12 months being 75% if the SUV was less than 10, and 16% if the SUV was greater than 20. Higashi et al17 reviewed 57 patients with NSCLC staged with thoracic PET before surgical resection. The median follow-up for all patients was 14 months, and the median follow-up for surviving patients was 33 months. The series included only eight patients with squamous cell carcinoma, and the authors did not comment whether they considered histology as a variable. The authors found that stratifying patients by an SUV of 5 was a better prognostic variable than pathologic tumor-node-metastasis system staging. Most recently, Jeong et al18 reviewed 73 patients with NSCLC who underwent whole-body PET imaging before treatment, which included surgery in 67 patients. The authors found that although the SUVMAX of squamous cell carcinoma was higher than that of adenocarcinomas, there were no significant differences between the SUVMAX of each histology if corrected for stage. The authors also found that, by multivariate analysis, only tumor-node-metastasis system staging and SUVMAX more than 7 were independent prognostic variables; histology was not a prognostic factor.
We found results that support and extend the findings of these four articles. In a carefully defined group of patients with NSCLC or carcinoid treated with complete resection alone after whole-body PET imaging, two variables (SUVMAX and pathologic maximal tumor size, which are readily obtainable by noninvasive preoperative imaging) were found to provide excellent independent prognostic discrimination. The combination of SUVMAX and tumor size together identified a subgroup of patients with extremely poor prognosis who would be appropriate targets for trials of induction therapy.
Our study is limited in that the number of available patients did not allow analysis of more variables, most notably histology. We chose to stratify patients above and below the median tumor size and SUVMAX because this appeared most likely to avoid inadvertent bias. Additional larger and prospective studies are needed both to avoid the biases inherent in retrospective studies, and to determine the optimal points of stratification to maximize the sensitivity and specificity of discrimination between groups of patients with different outcomes after surgery alone.
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Authors’ Disclosures of Potential Conflicts of Interest
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The following authors or their immediate family members have indicated a financial interest. No conflict exists for drugs or devices used in a study if they are not being evaluated as part of the investigation. Acted as a consultant within the last 2 years: Steven Larson, Pfizer, GEMS, Amersham, Siemens, CTI/CPS. Performed contract work within the last 2 years: Steven Larson, GEMS. Served as an officer or member of the Board of a company: Steven Larson, Imanet, CTI. Received more than $2,000 a year from a company for either of the last 2 years: Steven Larson, Imanet, CTI.
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NOTES
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Authors’ disclosures of potential conflicts of interest are found at the end of this article.
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Submitted November 18, 2003;
accepted April 28, 2004.
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C. C. Riedl, T. Akhurst, S. Larson, S. F. Stanziale, S. Tuorto, A. Bhargava, H. Hricak, D. Klimstra, and Y. Fong
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TOP
ABSTRACT
INTRODUCTION
