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J Thorac Cardiovasc Surg 2005;130:151-159
© 2005 The American Association for Thoracic Surgery
General Thoracic Surgery |
a Section of Thoracic Surgery, University of Alabama at Birmingham, and the Division of Cardio-Thoracic Surgery, Department of Surgery, Birmingham Veterans Administration Hospital, Birmingham, Ala
b Department of Epidemiology, School of Public Health, University of Alabama at Birmingham, Birmingham, Ala
d Department of Biostatistics, School of Public Health, University of Alabama at Birmingham, Birmingham, Ala
c Department of Nuclear Medicine, University of Alabama at Birmingham, Birmingham, Ala.
Received for publication July 15, 2004; revisions received November 1, 2004; accepted for publication November 9, 2004. * Address for reprints: Robert J. Cerfolio, MD, Associate Professor of Surgery, Chief of Thoracic Surgery, Division of Cardiothoracic Surgery, University of Alabama at Birmingham, 1900 University Blvd, THT 712, Birmingham, AL 35294 (Email: Robert.cerfolio{at}ccc.uab.edu).
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Abstract |
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METHODS: This is a retrospective review of a prospective database of patients with non-small cell lung cancer. Patients had dedicated positron emission tomography scanning with F-18 fluorodeoxyglucose, with the maximum standard uptake value measured. All suspicious nodal and systemic locations on computed tomographic and positron emission tomographic scanning underwent biopsy, and when indicated, resection with complete lymphadenectomy was performed.
RESULTS: There were 315 patients. Multivariate analysis showed patients with a high maximum standard uptake value (
10) were more likely to have poorly differentiated tumors (risk ratio, 1.5; P = .005) and advanced stage (risk ratio, 1.9; P = .010) and were less likely to have their disease completely resected (risk ratio, 3.7; P = .004). Maximum standard uptake value was the best predictor of disease-free survival (hazard ratio, 2.5; P = .039) and survival (hazard ratio, 2.8; P = .001). Stage-specific analysis showed that patients with stage IB and stage II disease with a maximum standard uptake value of greater than the median for their respective stages had a lower disease-free survival at 4 years (P = .005 and .044). The actual 4-year survival for patients with stage Ib non–small cell lung cancer was 80% versus 66% (P = .048), for stage II disease it was 64% versus 32% (P = .028), and for stage IIIa disease it was 64% versus 16% (P = .012) for the low and high maximum standard uptake value groups, respectively.
CONCLUSIONS: The maximum standard uptake value of a non-small cell lung cancer nodule on dedicated positron emission tomography is an independent predictor of stage and tumor characteristics. It is a more powerful independent predictor than the TNM stage for recurrence and survival for patients with early-stage resected cancer. This information might help guide treatment strategies.
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Introduction |
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The treatment of non–small cell lung cancer (NSCLC) depends on the stage.
1
Therefore the clinician spends significant time, effort, and money performing tests to assess the stage. Yet even after careful clinical staging followed by complete resection, the 5-year survival for patients with pathologic stage Ia, Ib, II, and IIIa disease is only 67%, 57%, 47%, and 23%, respectively.
1
Integrated positron emission tomography (PET)–computed tomography (CT) with F-18 fluorodeoxyglucose (FDG; FDG-PET/CT) or dedicated PET (FDG-PET) is an increasingly available noninvasive test that has been shown to be useful for the evaluation of an indeterminate pulmonary nodule, the staging of mediastinal lymph nodes, the evaluation of local nodal and distant metastases, and the response to chemoradiotherapy.
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In addition, there might be another not yet fully explored role. FDG-PET measures the standardized uptake value (SUV) of a pulmonary mass, which quantifies the glucose avidity of the tumor. This value is calculated by the software contained within the PET machine and is thus relatively consistent from one PET center to another. The objective of this study was to assess whether the maximum SUV, which is less variable than the mean SUV,
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represents a tumor’s in vivo virulence or a quantification of its biology.
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Methods |
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Imaging
FDG-PET scans were performed on a dedicated ECAT EXACT PET scanner (CTI, Knoxville, Tenn) or on an integrated PET-CT scanner (GE Discovery LS PET-CT Scanner, Milwaukee, Wis). Patients were asked to fast for 4 hours and then subsequently received 555 MBq (15 mCi) of FDG intravenously followed by PET after 1 hour. The scans were performed from the skull base to the midthigh level. Attenuation correction of PET images for the ECAT system was performed with standard transmission scanning by using 68 Germanium sources (3 rods). The scanning time for emission PET was 6 minutes, and transmission with 68 Germanium rods was 4 minutes per bed position. For the Discovery system, a CT examination was used for attenuation correction of PET images. The scanning time for emission PET was 5 minutes per bed position. Iterative reconstruction with CT attenuation correction was performed. The most recent CT scan of the chest was available for visual correlation. Maximum SUV was determined by drawing regions of interest on the attenuation-corrected FDG-PET images around the primary tumor. It was then calculated by using the software contained within the PET or PET-CT scanner by using the following formula
10
:
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Procedures, Staging, and Surgical Intervention
Patients were meticulously staged. All suspicious N2, N3, or M1 areas (maximum SUV, >2.5) underwent biopsy before pulmonary resection. Mediastinoscopy was used for biopsy of suspicious lymph nodes in the paratracheal area (stations 2R, 4R, 2L, and 4L), and endoscopic transesophageal ultrasonography was used for biopsy of suspicious posterior aorta-pulmonary window nodes (6), subcarinal nodes (7), periesophageal nodes (8), and inferior pulmonary ligament nodes (9).
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Patients with suspected M1 disease in the liver, adrenal gland, or contralateral lung underwent definitive biopsy to prove or disprove M1 cancer. If the bone or brain was suspected to harbor metastases, magnetic resonance imaging was considered the standard reference. If patients had biopsy-proved N3 or M1 disease, the stage was recorded, but they were excluded from the disease-free analysis. If there was no evidence of N2 or higher disease, patients underwent thoracotomy, pulmonary resection, and complete thoracic lymphadenectomy. Pathologic review was performed by using standard techniques, and immunohistochemical staining was used when appropriate. The pathologic stage was assessed by the international staging system.
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Patients were followed for cancer recurrence and survival. Follow-up data were obtained every 3 months for the first 2 years and every 6 months afterward. A chest radiograph was performed every 3 months, and a chest CT with intravenous contrast was performed every 6 months. FDG-PET was also used at 6 months in selected patients. In addition, if patients became symptomatic, appropriate testing (ie, bone and brain scanning) was performed as well. Information was obtained from clinic letters, hospital computer information systems, treatment updates, letters from oncology clinics and other physicians, social security death indexes, and telephone calls. The University of Alabama at Birmingham’s institutional review board approved both the prospective database used for this study and this trial.
Statistics: Definitions
The maximum SUV was evaluated statistically by 3 methods. The first method evaluated the SUV as a continuous value, irrespective of the patient’s stage. The second method was the maximum SUV within each stage of NSCLC, termed the stage-specific maximum SUV. In this method, after patients were pathologically staged, they were divided into 1 of 2 groups. If they had a maximum SUV greater than or equal to the median maximum SUV for that stage, they were placed in the high group for that stage, and if the value was lower, they were placed in the low group. The outcomes of these 2 groups in the same stage were then compared. The third method used maximum SUV as a binary variable. A cutoff point was identified by the log-rank test and a generalized Wilcoxon test.
In the disease-free survival analysis, failure (or recurrence of NSCLC) was defined as biopsy-proved NSCLC. If the biopsies were performed at outside institutions, pathology reports were obtained. Disease-free survival was defined as patients who were alive without recurrence. Operative mortality was defined as a patient who died before hospital discharge or within 30 days of the operative procedure.
Statistical Analyses
The primary end point was survival, which was from the date of surgical intervention to the date of the last follow-up or death. Patients who were still alive at the end of our study were censored. Disease-free survival was measured only for those who underwent complete R0 resection. A univariate analysis of all variables was performed initially to assess for differences among the maximum SUV, survival, and disease-free survival for variables. Univariate analyses were performed with a 2-sided log-rank test.
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A 
2 analysis was used for discrete variables, with a P value of less than .05 according to the 2-tailed Fisher exact test used to select factors with potential significance. Analysis of variance was used for discreet nondichotomous variables. For continuous variables, the Student t test or the Mann-Whitney U test was used to compare means for nonnormally distributed variables. All comparisons were 2 sided. Variables with the potential for a significant difference between groups on the basis of the results of the univariate analyses were entered as candidate variables in a multivariate analysis with a Cox proportional-hazards model with both forward and backward stepwise inclusion of factors, with an inclusion criterion of a P value of .05 or less. Survival analysis for differences among the high-SUV and low-SUV groups was performed by using the Kaplan-Meier method. All statistical analysis was performed with SAS v. 8.02 software (SAS Institute, Inc, Cary, NC).
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Results |
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Maximum SUV as a Predictor of Survival
Figure 2
shows the Kaplan-Meier survival curves for all patients in this study irrespective of stage or treatment stratified by maximum SUV of greater than or equal to 10 and less than 10. The mean survival for the group with a maximum SUV of less than 10 was 3.2 years, whereas it was 1.6 years for those with a maximum SUV of 10 or greater (P < .001).
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Discussion |
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and with stage IIIa disease might increase survival.
14–17
Very recently, the pendulum has begun to swing toward adjuvant therapy after a study reported in the New England Journal of Medicine
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and 2 oral presentations concerning 2 separate multi-institutional trials presented at the American Society of Clinical Oncology meeting in June 2004. All 3 of these reports suggest a survival benefit for adjuvant therapy. Yet despite all these data, the identification of patients who benefit the most from neoadjuvant therapy, adjuvant therapy, or both still remains unknown. If one believes that preoperative stage is now irrelevant and that all patients should receive adjuvant therapy, it is widely known that many patients are unable to complete this therapy. If one was able to identify patients who are at high risk of recurrence after resection, one might be more likely to push that patient toward completion. However, if one considers neoadjuvant therapy to be better than adjuvant therapy, the failure of clinical stage to predict pathologic stage is well known. Maximum SUV might be a better guide than the proposed clinical stage. Finally, if one believes that oncogenes, tumor serum markers, and protein expression that portends a worse survival
19–23
are the best markers, this type of risk stratification information is often not known before resection (unlike the maximum SUV on a PET scan) and thus cannot guide the decision for neoadjuvant therapy. Even if it could be determined from a preoperative needle biopsy, few centers currently evaluate it. Thus we believe that these data presented above have significant clinical importance.
Our report has shown that the maximum SUV of NSCLC is positively correlated to the T status, N status, and M status and is an independent predictor of stage. It also independently predicts the likelihood of lymphovascular invasion, which might be a critical element for metastatic disease. This finding is consistent with pathophysiology. For example, Glut 1, a critical cellular component of glucose transfer that is overexpressed in patients with NSCLC, has been associated with a worse prognosis.
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This might explain the increase in glucose avidity and thus the high maximum SUV in patients with aggressive tumors. Some of these findings have been corroborated in previous studies (Ahuja and colleagues
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in 1998, Vansteenkiste and associates
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in 1999, Dhital and coworkers
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in 2000, Jeong and colleagues
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in 2002, Higashi and associates
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in 2002, Sasaki and coworkers
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in 2003, and Downey and colleagues
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in 2004), some of which are summarized in Table 6. Our study has also shown that maximum SUV is actually a better predictor of survival and disease-free recurrence than the current TNM staging system. We found the best value for the cutoff point of the maximum SUV to be 10. The cutoff values found in the other articles cited above were as follows: 5 from Sasaki and coworkers,
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7 from Jeong and colleagues,
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and 10 from Downey and colleagues.
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In fact, the maximum SUV might be not only a supplement to the current TNM staging system but also might aid in filling in some of the shortcomings of the current system. For example, patients with T4 and N3 disease are all labeled as having stage IIIb disease. Yet the outcomes vary for patients who have T4 disease from a malignant pleural effusion, T4 disease from having 2 nodules of the same type in the same lobe, and N3 disease. The current TNM classification system does not demonstrate the differences in recurrence and survival, but in this study the maximum SUV did. Of the 15 patients that had stage IIIb disease, 3 had N3 disease, and their median maximum SUV was 19.1, but the 4 patients who had T4 disease because of 2 cancers of the same histology in the same lobe had a median maximum SUV of only 5.1. In our practice we now choose to report a patient’s clinical or pathologic stage as, for example, T2(11.2) N1 M0, with the maximum SUV provided in parentheses after the T status.
These findings, if further corroborated by other centers, raise several questions that are best and maybe only truly answered with multi-institutional prospective randomized trials. For instance, does a patient with a completely resected stage Ia, Ib, or II NSCLC who has a high maximum SUV benefit more from adjuvant therapy than one with a low maximum SUV? Is such a patient one who might also benefit from neoadjuvant therapy? Should the maximum SUV, instead of just the clinical stage, be part of the equation that aids in that decision? Should a patient with a high maximum SUV but with an early clinically staged tumor receive other staging tests before resection (eg, brain magnetic resonance imaging or mediastinoscopy) to ensure his or her clinical stage is correct? Will he or she benefit from closer postoperative surveillance? Can tumor or gene markers be correlated with a high SUV and, if so, which ones? Can one identify an absolute number for the maximum SUV that is consistent across centers that is a marker for poor survival, or should it be stage specific?
In this report we chose to use the maximum SUV instead of the mean SUV because it is less variable,
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less subjective, and more reproducible and provides more information about the aggressiveness of a tumor. It does not change despite changes in technique, time between injection and scanning, or the individual reading the PET scan. For this study to have universal applicability, the patient’s maximum SUVs should be the same or very similar at different PET centers. Most dedicated PET and integrated PET-CT scanners and all new machines have software packages that automatically calculate the maximum SUV, accounting for the various techniques used. Thus, the divergence of maximum SUV across centers should be small and will be even less problematic over time.
In conclusion, this is the largest report to show that the maximum SUV of a pulmonary nodule on FDG-PET scanning is an independent predictor of an NSCLC’s biologic aggressiveness or its in vivo virulence. The maximum SUV independently predicts an NSCLC’s likelihood of metastasizing to regional, hilar, and mediastinal lymph nodes, as well as to distant metastatic sites. It also predicts its propensity for lymphovascular invasion and recurrence rates. It more accurately predicts recurrence rates for stage Ib and II NSCLC and survival for patients with stage Ib, II, or IIIa NSCLC than the currently used TNM staging system. These provocative data should be verified by other centers, and then prospective randomized trials are required before one can fully assess the effect that maximum SUV will have on treatment strategies for patients with NSCLC. Although this article and its conclusions must obviously be confined to patients with NSCLC, some of its findings might be applicable to patients with other types of solid-organ cancers that feature squamous cell carcinoma or adenocarcinoma.
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A. S. Bryant, R. J. Cerfolio, K. M. Klemm, and B. Ojha Maximum Standard Uptake Value of Mediastinal Lymph Nodes on Integrated FDG-PET-CT Predicts Pathology in Patients with Non-Small Cell Lung Cancer Ann. Thorac. Surg., August 1, 2006; 82(2): 417 - 423. [Abstract] [Full Text] [PDF]
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R. J. Cerfolio and A. S. Bryant Survival and Outcomes of Pulmonary Resection for Non-Small Cell Lung Cancer in the Elderly: A Nested Case-Control Study Ann. Thorac. Surg., August 1, 2006; 82(2): 424 - 430. [Abstract] [Full Text] [PDF]
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