Journal of Clinical Oncology, Vol 17, Issue 10
(October), 1999: 3201-3206
© 1999 American Society for Clinical Oncology
Prognostic Importance of the Standardized Uptake Value on 18F-Fluoro-2-Deoxy-Glucose–Positron Emission Tomography Scan in Non–Small-Cell Lung Cancer: An Analysis of 125 Cases
Johan F. Vansteenkiste,
Sigrid G. Stroobants,
Patrick J. Dupont,
Paul R. De Leyn,
Erik K. Verbeken,
Georges J. Deneffe,
Luc A. Mortelmans,
Maurits G. Demedts,
and the Leuven Lung Cancer Group
From the Department of Pulmonology, Respiratory Oncology Unit and Departments of Nuclear Medicine, Thoracic Surgery, and Pathology, University Hospital Gasthuisberg, Catholic University, Leuven, Belgium.
Address reprint requests to J. Vansteenkiste, MD, PhD, Respiratory Oncology Unit, Department of Pulmonology, University Hospital Gasthuisberg, Catholic University, Herestraat, B-3000 Leuven, Belgium; email johan.vansteenkiste{at}uz.kuleuven.ac.be
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ABSTRACT
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PURPOSE: The amount of radio-labeled 18F-fluoro-2-deoxy-glucose (FDG) uptake, a measurement of the increased glucose metabolism of non–small-cell lung cancer (NSCLC) cells, has recently been correlated with proliferation capacity. The Standardized Uptake Value (SUV), a semi-quantitative measurement of FDG uptake on positron emission tomography (PET) scan, could thus be of prognostic significance.
PATIENTS AND METHODS: We analyzed the follow-up of 125 potentially operable NSCLC patients, previously included in three of our prospective PET protocols. Performance status, maximal tumor diameter, tumor-cell type, SUV, and final staging were analyzed for their possible association with survival.
RESULTS: Sixty-five patients had stage I or II NSCLC, 37 had stage IIIA, and 23 had stage IIIB. Treatment was complete resection in 91 cases. In a univariate analysis, performance status (P = .002), stage (P = .001), tumor diameter (P = .06), tumor-cell type (P = .03), and SUV greater than 7 (P = .001) were correlated with survival. For SUV, group dichotomy with a cut-off SUV of 7 had the best discriminative value for prognosis, both in the total and surgical cohort. A multivariate Cox analysis identified performance status (P = .02), stage (P = .01), and SUV (P = .007) as important for the prognosis. In the surgical group, patients with a resected tumor less than 3 cm had an expected 2-year survival of 86%, if the SUV was below 7, and 60%, if above 7. Nearly all resected tumors larger than 3 cm had SUV's greater than 7 and an expected 2-year survival of 43%.
CONCLUSION: We conclude that the FDG uptake in primary NSCLC on PET has an important prognostic value and could be complementary to other well-known factors in the decision on adjuvant treatment protocols.
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INTRODUCTION
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THE TUMOR-NODE-metastasis (TNM) staging system is the most important tool used by clinical oncologists to make estimates of prognosis and to choose the best combination of treatment modalities such as surgery, radiation, and chemotherapy. The clinical or pathologic TNM-staging, however, does not always give a satisfactory explanation for differences in survival. Resected stage I non–small-cell lung cancer (NSCLC) is a typical example; many patients are cured, but some have an early relapse and die.
Recent advances in molecular biology1 help to understand more about different patterns of survival in resected stage I NSCLC.2,3 For instance, based on a molecular-biologic staging including angiogenesis, proto-oncogene erbB-2, suppressor gene p53, and the proliferation marker KI-67, Harpole et al found a 5-year survival of 81% in resected stage I NSCLC patients without any adverse markers but only 49% in patients with three or more markers.4
NSCLC is also characterized by carbohydrate metabolic derangements, which also have been identified as independent prognostic factors correlated with poor treatment response and survival.5 Increased glycolysis results in upregulation of glucose transporter proteins (especially subtype Glut-1) and increased hexokinase activity.6 These glucose metabolism derangements can be measured quantitatively in vivo by positron emission tomography (PET) after administration of 18F-fluoro-2-deoxy-glucose (FDG). Recently, the FDG uptake in NSCLC cells has also been correlated with growth rate and proliferation capacity.7
Based on these findings, we analyzed the survival of the patients previously included in our prospective NSCLC PET studies. The aim of the study was to evaluate if the Standardized Uptake Value (SUV), a semi-quantitative measurement of FDG uptake in the tumor, was predictive of the prognosis after treatment.
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PATIENTS AND METHODS
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Patients
Patient data used in this analysis were obtained from two of our prospective PET protocols on lymph node staging in potentially operable NSCLC8,9 and one protocol on the use of PET in solitary pulmonary nodules.10 Because of slight overlap in inclusion between the two lymph node imaging studies and after omission of patients in the third series who were found to have benign nodules, a total of 125 cases were available for this study.
Patient characteristics prospectively recorded at baseline included age, sex, Eastern Cooperative Oncology Group (ECOG) performance status, tumor-cell type (squamous, adenocarcinomatous, or undifferentiated), maximal tumor diameter as determined on computed tomography (CT) scan, tumor side (right or left), and localization (upper lobe, including middle lobe on the right side, or lower lobe). Distant metastases were excluded by clinical history and physical examination, blood tests including a complete blood count, serum calcium, and liver function tests. To avoid equivocal findings, all patients had a thoracic CT, including the upper abdomen, a brain CT, in case of clinical signs or of nonsquamous histology, and a bone scintigraphy, in case of clinical signs, completed by bone radiographs or a bone CT. Surgical mediastinal staging was performed in all patients except those with a T1 squamous cell tumor without enlarged mediastinal adenopathy on CT.11 The staging consisted of cervical mediastinoscopy (examining levels 1, 2R, 2L, 3, 4R, 4L, and 7 of the Naruke mediastinal lymph node map12) and was completed by left anterior mediastinotomy in left upper lobe tumors with enlarged adenopathy in the subaortic level. Based on these examinations, a clinical TNM category and stage (according to the 1997 staging system13) were determined. In the operated patients, a systematic mediastinal nodal dissection was performed, as described in a previous report,8 and the pathologic TN category and stage were recorded. For the analysis of the stage factor, the pathologic stage was used in the surgical cases, the clinical stage in the others. The survival status was retrieved from our medical records or from a query to the referring physicians by the data nurses.
FDG-PET
The inclusion and exclusion criteria and the technique have been described previously in detail.8 In short, patients fasted for at least 6 hours before the PET. Attenuation-corrected images were acquired with a CTI-Siemens (Iselin, NJ) 931/08/12 PET scanner (axial field of view of 10.1 cm and resolution of approximately 8 mm) between 50 and 70 minutes after injection of FDG 6.5 MBq/kg (maximum dose, 555 MBq). Interpretation was performed prospectively by a nuclear medicine physician (S.G.S.) and a respiratory oncologist (J.F.V.) and blinded to surgical staging or pathology data. For the determination of the SUV of the primary tumor, regions of interest (ROIs) were manually drawn on the transaxial images around the focal FDG-uptake zones in the primary tumor. FDG uptake in these ROIs was quantified by calculating the SUV in each pixel according to the following formula: SUV = activity concentration / (injected dose / body weight).14 To minimize partial volume effects, the maximum SUV within an ROI was used for further calculations.
Statistics
Survival time was defined as the time interval from the date of pathologic diagnosis until death or the last follow-up date. Survival was calculated with the Kaplan-Meier method, and groups were compared with the log-rank test.
Multivariate analysis was carried out with the Cox proportional hazards model. Categorical covariates were dichotomized in one model or treated with the deviation method in another.15 A significance level of 0.10 was used for covariate entry. In the tables, the median survival time, with its 95% confidence interval (CI), and the 2-year survival percentages were presented. Numerical data were presented as mean ± SD.
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RESULTS
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The characteristics of the 125 patients are listed in Table 1. Their mean age was 62 years (SD = 9 years; range, 33 to 83 years). The distributions of the TNM stage subsets and treatments are listed in Table 2. In general, most patients in stages I, II, IIIA to T3N1, IIIA to "unforeseen" N2 (N2 found at thoracotomy after a negative mediastinoscopy), and some patients in IIIB to T4N0 were treated with surgery. When stage IIIA to N2 was found at mediastinoscopy, treatment usually consisted of induction chemotherapy followed by definitive locoregional treatment, either surgery or radiotherapy. For patients in stage IIIB to N3, treatment varied depending on extent of disease and general condition. A total of 91 patients underwent surgical resection.
Follow-up data were retrieved in all patients, with a mean follow-up of 19 months (SD = 11 months; range, 1 to 40 months) at the time of analysis.
Univariate Survival Analysis of the Total Group
The overall median survival time (MST) was 30 months (95% CI, 25 to 35), and the 2-year survival rate was 55%. The univariate survival analysis results are listed in Table 3. ECOG performance status, stage, and tumor-cell type proved to be significant at the .05 level. The influence of tumor FDG uptake was explored for various SUV cutoff values (Fig 1). The most discriminative cutoff point for prognosis proved to be at an SUV of 7, although dichotomization with a broad range of SUVs, between 6 and 11, gave significantly discriminative log-rank P values. Patients with an SUV of 7 or less had a much better survival than patients with an SUV above 7 (P = .001, Table 3, Fig 2).
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Fig 1. Relationship between various SUV cutoff values and their discriminative value for survival, as assessed by the log-rank test. A broad range of SUVs, between 6 and 11, gave log-rank P values < .05.
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Fig 2. Survival graph of the 125 patients according to the SUV of the primary tumor (bars are SE bars).
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Univariate Survival Analysis of the Surgical Group
Ninety-one patients underwent surgical resection; 44 for stage I, 18 for stage II, 21 for stage IIIA (after a negative preoperative mediastinoscopy or after induction chemotherapy in case of positive mediastinoscopy), and eight for stage IIIB to T4N0-1. Their MST was 34 months (95% CI, 27 to 41), and the 2-year survival rate was 63%.
The influence of the same factors on survival was analyzed. Factors with a log-rank P value below .05 were performance status (P = .004), stage (P = .03), and tumor diameter (P = .04).
The influence of tumor FDG uptake was explored for various SUV cutoff values, and the most discriminative cutoff point was again found at an SUV of 7. The operated patients with an SUV of 7 or less had a much better survival rate than patients with an SUV above 7 (P = .002).
The survival stratified for tumor size and FDG uptake is depicted in Fig 3. Patients with a resected tumor less than 3 cm had an expected 2-year survival of 86% if the SUV was below 7, and 60% if above 7; all but four patients with resected tumors larger than 3 cm had SUVs of more than 7 and an expected 2-year survival of 43%.
Multivariate Survival Analysis
The joint effects and interactions of the factors with a log-rank significance (P) below 0.10 were examined in Cox proportional hazards models. In a first model, variables were dichotomized, both categorical variables (performance status between 0 and 1 v 2, stage I to II v III, and cell type squamous v nonsquamous) and the numeric variable (SUV below v above 7). In this model, ECOG performance status (P = .02), stage (P = .01), and SUV (P = .007) were significantly correlated with survival. The relative risks associated with these factors are listed in Table 4.
In a second model, the categorical variables, performance status, stage, and cell type, were analyzed with the deviation method, and the numeric variable, SUV, was entered as a continuous value. In this model, performance status (P = .003), stage (P = .008), and SUV (P = .01) were significantly correlated with survival.
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DISCUSSION
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In this survival analysis of 125 potentially operable NSCLC patients, who underwent FDG-PET in the context of three of our previous prospective protocols, we were able to demonstrate that FDG uptake in NSCLC, as measured by the SUV, has a significant and independent prognostic value. An SUV of 7 proved to have the best discriminative value for survival. In the operated patients, this parameter seemed to be more important than the tumor diameter.
NSCLC is a major health problem, and better understanding of the prognosis could lead to more adequate use of surgical adjuvant treatments and hopefully better treatment outcome.
Clinicoradiologic factors (including mediastinoscopy) determine the TNM-based staging, which is the most important prognostic factor. Most of the patients with an operated T1N0 tumor are cured, but some have an early systemic relapse. Better understanding of the molecular biology of NSCLC recently led to identification of factors that could explain the more aggressive behavior of some tumors.1
Another molecular-biologic derangement in NSCLC is the altered glucose metabolism,16 mainly because of increased glycolysis, upregulation of glucose transporter proteins (especially Glut-1), and increased hexokinase activity.6 This biologic derangement has also been related to treatment response and survival.5 FDG-PET combines the unique opportunity of a good staging examination17 and measurement of these glucose derangements. Glucose derangements can be measured mathematically using the glucose flux constants18 or, clinically more feasible, using the SUV, a semi-quantitative measurement of FDG uptake.19
The FDG uptake in NSCLC has been correlated with tumor growth rate and proliferation capacity.7 On the other hand, overexpression of the Glut-1 transporter, an important feature of the glucose disturbance in NSCLC, was linked to a worse prognosis.20 All these findings could explain the relationship between FDG uptake on PET and biologic aggressiveness, and thus prognosis, in NSCLC.
Recently, a group from Duke University examined FDG uptake of NSCLC and reported an SUV of more than 10 to be of significant adverse prognostic importance.21 When they used the cutoff point of 10, 76% of the patients fell below this value. In our experience, using the cutoff point of 7, 75% of the patients were above this value. It seems reasonable to hypothesize that there is no true cutoff point, but rather a transition zone, where the prognosis gradually worsens. This was further substantiated by the relationship between cutoff SUV and prognostic discrimination, as illustrated in Fig 1, where the discriminatory values were situated between an SUV of 6 and 11.
In the Duke University experience, lesion size and lesion SUV provided additional information in the multivariate survival analysis. In our stratified analysis of surgical cases (Fig 3), tumor diameter was of far less prognostic significance compared with tumor SUV. We have no solid explanation for this difference. One of the differences between the two series is that 62% of the patients from the Duke series had a tumor less than 3 cm, whereas this was only 42% in our series. One might speculate that the diameter of the primary tumor was less important in our series because the greater proportion of patients with larger tumors diminished the significance of this finding.
At present, relationships have been documented in NSCLC between prognosis and molecular-biologic features of proliferation, apoptosis, and angiogenesis.2-4 In addition, both the Duke experience and our own study established a relationship in NSCLC between prognosis and glucose metabolism derangements, as measured in vivo on FDG-PET. Studies now need to concentrate on whether the above-mentioned glucose disturbances and molecular-biologic aberrations in NSCLC are independent or linked findings and what the contribution is of each of these features to the prognosis. Several questions need an answer in this respect. What is the correlation between the glucose metabolism measured by FDG-PET and the biomarkers of proliferation/apoptosis? What is the correlation between glucose metabolism measured by FDG-PET and tumor angiogenesis and perfusion? What is the prognostic significance of each of these molecular-biologic markers individually, their possible mutual relationship, and their relationship with standard clinical prognostic factors such as stage? Undoubtedly, future studies will unravel the independent and related aspects of the prognostic significance of this fascinating in vivo imaging test of tumor metabolism.
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ACKNOWLEDGMENTS
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We thank B. Anrijs and D. Strens for their dedicated assistance in obtaining the survival data. We also thank other involved members of the Leuven Lung Cancer Group: T. Lerut, K. Nackaerts, D. Van Raemdonck.
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REFERENCES
|
|---|
1.
Salgia R, Skarin AT: Molecular abnormalities in lung cancer. J Clin Oncol16:1207-1217, 1998[Abstract]
2.
Harpole DH, Herndon JE, Wolfe WG, et al: A prognostic model of recurrence and death in stage I non-small cell lung cancer utilizing presentation, histopathology, and oncoprotein expression. Cancer Res55:51-56, 1995[Abstract/Free Full Text]
3.
Apolinario RM, van der Valk P, de Jong JS, et al: Prognostic value of the expression of p53, bcl-2, and bax oncoproteins, and neovascularization in patients with radically resected non-small-cell lung cancer. J Clin Oncol15:2456-2466, 1997[Abstract/Free Full Text]
4.
Harpole DH, Richards WG, Herndon JE, et al: Angiogenesis and molecular biologic substaging in patients with stage I non-small cell lung cancer. Ann Thorac Surg61:1470-1476, 1996[Abstract/Free Full Text]
5.
Stanley KE: Prognostic factors for survival in patients with inoperable lung cancer. J Natl Cancer Inst65:25-32, 1980
6.
Nelson CA, Wang JQ, Leav I, et al: The interaction among glucose transport, hexokinase, and glucose-6-phosphatase with respect to 3H-2-deoxyglucose retention in murine tumor models. Nucl Med Biol23:553-541, 1996
7.
Duhaylongsod FG, Lowe VJ, Patz EF Jr, et al: Lung tumor growth correlates with glucose metabolism measured by fluoride-18 fluorodeoxyglucose positron emission tomography. Ann Thorac Surg60:1348-1352, 1995[Abstract/Free Full Text]
8.
Vansteenkiste JF, Stroobants SG, De Leyn PR, et al: Lymph node staging in non-small cell lung cancer with FDG-PET scan: A prospective study on 690 lymph node stations from 68 patients. J Clin Oncol16:2142-2149, 1998[Abstract]
9.
Vansteenkiste JF, Stroobants SG, Dupont PJ, et al: FDG-PET scan in potentially operable non-small cell lung cancer: Do anatometabolic PET-CT fusion images improve the localisation of regional lymph node metastases? Eur J Nucl Med25:1495-1501, 1998[Medline]
10.
Nackaerts K, Stroobants S, Vansteenkiste J, et al: The use of positron emission tomography (PET) in the differential diagnosis of indeterminate solitary pulmonary lesions. Eur Respir J 10:425S, 1997 (abstr)
11.
De Leyn P, Vansteenkiste J, Cuypers P, et al: Role of cervical mediastinoscopy in staging of non-small cell lung cancer without enlarged mediastinal lymph nodes on CT scan. Eur J Cardiothorac Surg12:706-712, 1997[Abstract]
12.
Naruke T, Suemasu K, Ishikawa S: Lymph node mapping and curability at various levels of metastasis in resected lung cancer. J Thorac Cardiovasc Surg76:832-837, 1978[Abstract]
13.
Mountain CF: Revisions in the International System for Staging Lung Cancer. Chest111:1710-1717, 1997[Abstract/Free Full Text]
14.
Woodard HQ, Bigler RE, Freed B, et al: Expression of tissue isotope distribution. J Nucl Med16:958-959, 1975
15.
Norusis MJ (ed): Cox regression, in SPPS Advanced Statistics. Chicago, IL, SPSS Inc, 1994, pp 291-328
16.
Vansteenkiste JF, Simons JP, Wouters EF, et al: Hormonal treatment in advanced non-small cell lung cancer: Fact or fiction? Eur Respir J9:1707-1712, 1996[Abstract]
17.
Lewis P, Griffin S, Marsden P, et al: Whole-body 18F-fluorodeoxyglucose positron emission tomography in preoperative evaluation of lung cancer. Lancet344:1265-1266, 1994[Medline]
18.
Patlak CS, Blasberg RG: Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data: Generalizations. J Cereb Blood Flow Metab5:584-590, 1985[Medline]
19.
Lowe VJ, Hoffman JM, DeLong DM, et al: Semiquantitative and visual analysis of FDG-PET images in pulmonary abnormalities. J Nucl Med35:1771-1776, 1994[Abstract/Free Full Text]
20.
Younes M, Brown RW, Stephenson M, et al: Overexpression of Glut1 and Glut3 in stage I non-small cell lung carcinoma is associated with poor survival. Cancer80:1046-1051, 1997[Medline]
21.
Ahuja V, Coleman RE, Herndon J, et al: The prognostic significance of fluorodeoxyglucose positron emission tomography imaging for patients with nonsmall cell lung carcinoma. Cancer83:918-924, 1998[Medline]
Submitted April 6, 1999;
accepted June 10, 1999.
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|
K.-H. Lee, S.-H. Lee, D.-W. Kim, W. J. Kang, J.-K. Chung, S.-A. Im, T.-Y. Kim, Y. W. Kim, Y.-J. Bang, and D. S. Heo
High fluorodeoxyglucose uptake on positron emission tomography in patients with advanced non-small cell lung cancer on platinum-based combination chemotherapy.
Clin. Cancer Res.,
July 15, 2006;
12(14):
4232 - 4236.
[Abstract]
[Full Text]
[PDF]
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K.-i. Watanabe, H. Nomori, T. Ohtsuka, T. Naruke, A. Ebihara, H. Orikasa, K. Yamazaki, K. Uno, T. Kobayashi, and T. Goya
[F-18]Fluorodeoxyglucose Positron Emission Tomography Can Predict Pathological Tumor Stage and Proliferative Activity Determined by Ki-67 in Clinical Stage IA Lung Adenocarcinomas
Jpn. J. Clin. Oncol.,
July 1, 2006;
36(7):
403 - 409.
[Abstract]
[Full Text]
[PDF]
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S. Prevost, L. Boucher, P. Larivee, R. Boileau, and F. Benard
Bone Marrow Hypermetabolism on 18F-FDG PET as a Survival Prognostic Factor in Non-Small Cell Lung Cancer
J. Nucl. Med.,
April 1, 2006;
47(4):
559 - 565.
[Abstract]
[Full Text]
[PDF]
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S. Leboulleux, C. Dromain, G. Bonniaud, A. Auperin, B. Caillou, J. Lumbroso, R. Sigal, E. Baudin, and M. Schlumberger
Diagnostic and Prognostic Value of 18-Fluorodeoxyglucose Positron Emission Tomography in Adrenocortical Carcinoma: A Prospective Comparison with Computed Tomography
J. Clin. Endocrinol. Metab.,
March 1, 2006;
91(3):
920 - 925.
[Abstract]
[Full Text]
[PDF]
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D. L. Chen and F. Dehdashti
Advances in Positron Emission Tomographic Imaging of Lung Cancer
Proceedings of the ATS,
December 1, 2005;
2(6):
541 - 544.
[Abstract]
[Full Text]
[PDF]
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C. J. Hoekstra, S. G. Stroobants, E. F. Smit, J. Vansteenkiste, H. van Tinteren, P. E. Postmus, R. P. Golding, B. Biesma, F. J.H.M. Schramel, N. van Zandwijk, et al.
Prognostic Relevance of Response Evaluation Using [18F]-2-Fluoro-2-Deoxy-D-Glucose Positron Emission Tomography in Patients With Locally Advanced Non-Small-Cell Lung Cancer
J. Clin. Oncol.,
November 20, 2005;
23(33):
8362 - 8370.
[Abstract]
[Full Text]
[PDF]
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H. Schoder, A. Noy, M. Gonen, L. Weng, D. Green, Y. E. Erdi, S. M. Larson, and H. W.D. Yeung
Intensity of 18Fluorodeoxyglucose Uptake in Positron Emission Tomography Distinguishes Between Indolent and Aggressive Non-Hodgkin's Lymphoma
J. Clin. Oncol.,
July 20, 2005;
23(21):
4643 - 4651.
[Abstract]
[Full Text]
[PDF]
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R. M. Lindell, T. E. Hartman, S. J. Swensen, J. R. Jett, D. E. Midthun, M. A. Nathan, and V. J. Lowe
Lung Cancer Screening Experience: A Retrospective Review of PET in 22 Non-Small Cell Lung Carcinomas Detected on Screening Chest CT in a High-Risk Population
Am. J. Roentgenol.,
July 1, 2005;
185(1):
126 - 131.
[Abstract]
[Full Text]
[PDF]
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L. K. Shankar and D. C. Sullivan
Functional Imaging in Lung Cancer
J. Clin. Oncol.,
May 10, 2005;
23(14):
3203 - 3211.
[Abstract]
[Full Text]
[PDF]
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G. R. Simon, S. Sharma, A. Cantor, P. Smith, and G. Bepler
ERCC1 Expression Is a Predictor of Survival in Resected Patients With Non-small Cell Lung Cancer
Chest,
March 1, 2005;
127(3):
978 - 983.
[Abstract]
[Full Text]
[PDF]
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R. Sasaki, R. Komaki, H. Macapinlac, J. Erasmus, P. Allen, K. Forster, J. B. Putnam, R. S. Herbst, C. A. Moran, D. A. Podoloff, et al.
[18F]Fluorodeoxyglucose Uptake by Positron Emission Tomography Predicts Outcome of Non-Small-Cell Lung Cancer
J. Clin. Oncol.,
February 20, 2005;
23(6):
1136 - 1143.
[Abstract]
[Full Text]
[PDF]
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D. Hellwig, T. P. Graeter, D. Ukena, T. Georg, C.-M. Kirsch, and H.-J. Schafers
Value of F-18-fluorodeoxyglucose positron emission tomography after induction therapy of locally advanced bronchogenic carcinoma
J. Thorac. Cardiovasc. Surg.,
December 1, 2004;
128(6):
892 - 899.
[Abstract]
[Full Text]
[PDF]
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R. J. Cerfolio, A. S. Bryant, T. S. Winokur, B. Ohja, and A. A. Bartolucci
Repeat FDG-PET After Neoadjuvant Therapy is a Predictor of Pathologic Response in Patients With Non-Small Cell Lung Cancer
Ann. Thorac. Surg.,
December 1, 2004;
78(6):
1903 - 1909.
[Abstract]
[Full Text]
[PDF]
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F. C. Detterbeck, J. F. Vansteenkiste, D. E. Morris, C. A. Dooms, A. H. Khandani, and M. A. Socinski
Seeking a Home for a PET, Part 3: Emerging Applications of Positron Emission Tomography Imaging in the Management of Patients With Lung Cancer
Chest,
November 1, 2004;
126(5):
1656 - 1666.
[Abstract]
[Full Text]
[PDF]
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E. M. Kamel, M. Thumshirn, K. Truninger, M. Schiesser, M. Fried, B. Padberg, D. Schneiter, S. J. Stoeckli, G. K. von Schulthess, and K. D.M. Stumpe
Significance of Incidental 18F-FDG Accumulations in the Gastrointestinal Tract in PET/CT: Correlation with Endoscopic and Histopathologic Results
J. Nucl. Med.,
November 1, 2004;
45(11):
1804 - 1810.
[Abstract]
[Full Text]
[PDF]
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L. Schrevens, N. Lorent, C. Dooms, and J. Vansteenkiste
The Role of PET Scan in Diagnosis, Staging, and Management of Non-Small Cell Lung Cancer
Oncologist,
November 1, 2004;
9(6):
633 - 643.
[Abstract]
[Full Text]
[PDF]
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H. Nomori, K. Watanabe, T. Ohtsuka, T. Naruke, K. Suemasu, T. Kobayashi, and K. Uno
Fluorine 18-tagged fluorodeoxyglucose positron emission tomographic scanning to predict lymph node metastasis, invasiveness, or both, in clinical T1 N0 M0 lung adenocarcinoma
J. Thorac. Cardiovasc. Surg.,
September 1, 2004;
128(3):
396 - 401.
[Abstract]
[Full Text]
[PDF]
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R. J. Downey, T. Akhurst, M. Gonen, A. Vincent, M. S. Bains, S. Larson, and V. Rusch
Preoperative F-18 Fluorodeoxyglucose-Positron Emission Tomography Maximal Standardized Uptake Value Predicts Survival After Lung Cancer Resection
J. Clin. Oncol.,
August 15, 2004;
22(16):
3255 - 3260.
[Abstract]
[Full Text]
[PDF]
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A. K. Buck, G. Glatting, and S. N. Reske
Quantification of 18F-FDG Uptake in Non-Small Cell Lung Cancer: A Feasible Prognostic Marker?
J. Nucl. Med.,
August 1, 2004;
45(8):
1274 - 1276.
[Full Text]
[PDF]
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H. Vesselle, E. Turcotte, L. Wiens, R. Schmidt, J. E. Takasugi, T. Lalani, E. Vallieres, and D. E. Wood
Relationship between Non-Small Cell Lung Cancer Fluorodeoxyglucose Uptake at Positron Emission Tomography and Surgical Stage with Relevance to Patient Prognosis
Clin. Cancer Res.,
July 15, 2004;
10(14):
4709 - 4716.
[Abstract]
[Full Text]
[PDF]
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H. Schoder, Y. E. Erdi, K. Chao, M. Gonen, S. M. Larson, and H. W.D. Yeung
Clinical Implications of Different Image Reconstruction Parameters for Interpretation of Whole-Body PET Studies in Cancer Patients
J. Nucl. Med.,
April 1, 2004;
45(4):
559 - 566.
[Abstract]
[Full Text]
[PDF]
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G. Halter, A. K. Buck, H. Schirrmeister, I. Wurziger, F. Liewald, G. Glatting, B. Neumaier, L. Sunder-Plassmann, S. N. Reske, and M. Hetzel
[18F] 3-deoxy-3'-fluorothymidine positron emission tomography: Alternative or diagnostic adjunct to 2-[18F]-fluoro-2-deoxy-D-glucose positron emission tomography in the workup of suspicious central focal lesions?
J. Thorac. Cardiovasc. Surg.,
April 1, 2004;
127(4):
1093 - 1099.
[Abstract]
[Full Text]
[PDF]
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H. Zhang, K. Yoshikawa, K. Tamura, T. Tomemori, K. Sagou, M. Tian, S. Kandatsu, T. Kamada, H. Tsuji, T. Suhara, et al.
[11C]Methionine Positron Emission Tomography and Survival in Patients with Bone and Soft Tissue Sarcomas Treated by Carbon Ion Radiotherapy
Clin. Cancer Res.,
March 1, 2004;
10(5):
1764 - 1772.
[Abstract]
[Full Text]
[PDF]
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K. Ott, U. Fink, K. Becker, A. Stahl, H.-J. Dittler, R. Busch, H. Stein, F. Lordick, T. Link, M. Schwaiger, et al.
Prediction of Response to Preoperative Chemotherapy in Gastric Carcinoma by Metabolic Imaging: Results of a Prospective Trial
J. Clin. Oncol.,
December 15, 2003;
21(24):
4604 - 4610.
[Abstract]
[Full Text]
[PDF]
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K. H. Kernstine
Positron emission tomography with 2-[18F]fluoro-2-deoxy-D-glucose: can it be used to accurately stage the mediastinum in non-small cell lung cancer as an alternative to mediastinoscopy?
J. Thorac. Cardiovasc. Surg.,
December 1, 2003;
126(6):
1700 - 1703.
[Full Text]
[PDF]
|
|
|
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A. K. Buck, G. Halter, H. Schirrmeister, J. Kotzerke, I. Wurziger, G. Glatting, T. Mattfeldt, B. Neumaier, S. N. Reske, and M. Hetzel
Imaging Proliferation in Lung Tumors with PET: 18F-FLT Versus 18F-FDG
J. Nucl. Med.,
September 1, 2003;
44(9):
1426 - 1431.
[Abstract]
[Full Text]
[PDF]
|
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M. P. Mac Manus, R. J. Hicks, J. P. Matthews, A. McKenzie, D. Rischin, E. K. Salminen, and D. L. Ball
Positron Emission Tomography Is Superior to Computed Tomography Scanning for Response-Assessment After Radical Radiotherapy or Chemoradiotherapy in Patients With Non-Small-Cell Lung Cancer
J. Clin. Oncol.,
April 1, 2003;
21(7):
1285 - 1292.
[Abstract]
[Full Text]
[PDF]
|
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M. D. Brundage, D. Davies, and W. J. Mackillop
Prognostic Factors in Non-small Cell Lung Cancer* : A Decade of Progress
Chest,
September 1, 2002;
122(3):
1037 - 1057.
[Abstract]
[Full Text]
[PDF]
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C. Franzius, S. Bielack, S. Flege, J. Sciuk, H. Jurgens, and O. Schober
Prognostic Significance of 18F-FDG and 99mTc-Methylene Diphosphonate Uptake in Primary Osteosarcoma
J. Nucl. Med.,
August 1, 2002;
43(8):
1012 - 1017.
[Abstract]
[Full Text]
[PDF]
|
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A. K. Buck, H. Schirrmeister, M. Hetzel, M. von der Heide, G. Halter, G. Glatting, T. Mattfeldt, F. Liewald, S. N. Reske, and B. Neumaier
3-Deoxy-3-[18F]Fluorothymidine-Positron Emission Tomography for Noninvasive Assessment of Proliferation in Pulmonary Nodules
Cancer Res.,
June 1, 2002;
62(12):
3331 - 3334.
[Abstract]
[Full Text]
[PDF]
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G. Bepler, A. Gautam, L. M. McIntyre, A. F. Beck, D. S. Chervinsky, Y.-C. Kim, D. M. Pitterle, and A. Hyland
Prognostic Significance of Molecular Genetic Aberrations on Chromosome Segment 11p15.5 in Non-Small-Cell Lung Cancer
J. Clin. Oncol.,
March 1, 2002;
20(5):
1353 - 1360.
[Abstract]
[Full Text]
[PDF]
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A. S. Allal, P. Dulguerov, M. Allaoua, C.-A. Haenggeli, E. A. El Ghazi, W. Lehmann, and D. O. Slosman
Standardized Uptake Value of 2-[18F] Fluoro-2-Deoxy-D-Glucose in Predicting Outcome in Head and Neck Carcinomas Treated by Radiotherapy With or Without Chemotherapy
J. Clin. Oncol.,
March 1, 2002;
20(5):
1398 - 1404.
[Abstract]
[Full Text]
[PDF]
|
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E. Salminen and M. Mac Manus
FDG-PET imaging in the management of non-small-cell lung cancer
Ann. Onc.,
March 1, 2002;
13(3):
357 - 360.
[Abstract]
[Full Text]
[PDF]
|
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K. H. Kernstine, K. A. McLaughlin, Y. Menda, N. P. Rossi, D. J. Kahn, D. L. Bushnell, M. M. Graham, C. K. Brown, and M. T. Madsen
Can FDG-PET reduce the need for mediastinoscopy in potentially resectable nonsmall cell lung cancer?
Ann. Thorac. Surg.,
February 1, 2002;
73(2):
394 - 402.
[Abstract]
[Full Text]
[PDF]
|
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K. Higashi, Y. Ueda, Y. Arisaka, T. Sakuma, Y. Nambu, M. Oguchi, H. Seki, S. Taki, H. Tonami, and I. Yamamoto
18F-FDG Uptake as a Biologic Prognostic Factor for Recurrence in Patients with Surgically Resected Non-Small Cell Lung Cancer
J. Nucl. Med.,
January 1, 2002;
43(1):
39 - 45.
[Abstract]
[Full Text]
[PDF]
|
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N. Ramnath, F. J. Hernandez, D.-F. Tan, J. A. Huberman, N. Natarajan, A. F. Beck, A. Hyland, I. T. Todorov, J. S.J. Brooks, and G. Bepler
MCM2 Is an Independent Predictor of Survival in Patients With Non-Small-Cell Lung Cancer
J. Clin. Oncol.,
November 15, 2001;
19(22):
4259 - 4266.
[Abstract]
[Full Text]
|
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R. M. Pieterman, J. W.G. van Putten, J. J. Meuzelaar, E. L. Mooyaart, W. Vaalburg, G. H. Koeter, V. Fidler, J. Pruim, and H. J.M. Groen
Preoperative Staging of Non-Small-Cell Lung Cancer with Positron-Emission Tomography
N. Engl. J. Med.,
July 27, 2000;
343(4):
254 - 261.
[Abstract]
[Full Text]
[PDF]
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TOP
ABSTRACT
INTRODUCTION
