EJCTS Click here for details of sales representative
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Eur J Cardiothorac Surg 2008;34:1223-1227. doi:10.1016/j.ejcts.2008.09.007
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Daniel L. Fortes
Mark S. Allen
Val J. Lowe
Dennis A. Wigle
Stephen D. Cassivi
Francis C. Nichols
Claude Deschamps
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Fortes, D. L.
Right arrow Articles by Deschamps, C.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Fortes, D. L.
Right arrow Articles by Deschamps, C.
Related Collections
Right arrow Lung - cancer

The sensitivity of 18F-fluorodeoxyglucose positron emission tomography in the evaluation of metastatic pulmonary nodules

Daniel L. Fortesa, Mark S. Allena,*, Val J. Loweb, Keh-Hsien Robert Shena, Dennis A. Wiglea, Stephen D. Cassivia, Francis C. Nicholsa, Claude Deschampsa

a Division of General Thoracic Surgery, Department of Surgery, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, MN 55905, United States
b Division of Nuclear Medicine, Department of Radiology, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, MN 55905, United States

Received 6 June 2008; received in revised form 28 August 2008; accepted 8 September 2008.

* Corresponding author. Tel.: +1 507 284 1517; fax: +1 507 284 0058. (Email: allen.mark{at}mayo.edu).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Statistics
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 
Objective: Pulmonary metastasectomy is beneficial in select patients. The sensitivity of 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) for pulmonary metastasis is unknown. The aims of the study were to determine the accuracy of FDG-PET in detecting pulmonary metastasis and identify factors affecting sensitivity. Methods: All patients undergoing metastasectomy from September 2002 through December 2006 who had both chest computed tomography (CT) and FDG-PET scans or a fused CT/FDG-PET within 6 weeks prior to surgery were reviewed. Univariate and multivariate analysis were performed to determine predictors of positivity. Results: There were 83 patients (41 men, 42 women) who had 104 resections. Median age was 61 years (range, 32–87). In total 154 nodules were resected; 1 nodule in 47 patients and multiple in 36. Histopathology was adenocarcinoma in 94 nodules, sarcoma in 18, squamous cell carcinoma in 15, renal cell carcinoma in 7 and other in 20. At least one nodule was FDG-PET positive in 68 patients (81.9%). True positive FDG-PET was found in 104 nodules (67.5%) while 50 were false negative (32.5%). Multivariate analysis revealed tumor diameter and grade correlated with increased sensitivity of FDG-PET. Conclusion: FDG-PET is positive in only 67.5% of metastatic pulmonary nodules. Nodule size and grade affect the sensitivity of FDG-PET for metastatic pulmonary nodules. FDG-PET is not a sensitive test in the evaluation of patients considered for pulmonary metastasectomy. Moreover, a negative FDG-PET should not be used to rule out metastatic disease.

Key Words: Pulmonary metastases • Positron emission tomography • Screening


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Statistics
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 
Cancer is responsible for one in every eight deaths worldwide and is the second leading cause of death in developed countries and the third leading cause of death in developing countries. The American Cancer Society estimates that more than 12 million new cases of cancer will be diagnosed in 2007, leading to the death of over 7.6 million people (about 20,000 cancer deaths per day) around the globe [1].

Resection of pulmonary metastasis has become an integral part of oncologic treatment in a select group of patients with controlled primary malignancies outside the thorax. During follow-up, these patients commonly undergo screening studies to detect recurrences or metastases. 18F-Fluorodeoxyglucose positron emission tomography (FDG-PET) is increasingly being used for screening purposes, often in conjunction with computed tomography scanning (CT).

Several papers have been published on the use of FDG-PET for the diagnosis and staging of indeterminate pulmonary nodules. Overall, in the setting of an indeterminate nodule greater than 1 cm, FDG-PET has a sensitivity of 96.8% and specificity of 77.8% in the detection of malignancy [2]. The vast majority of the published data comes from series of patients with non-small cell lung cancer and includes only a few patients with pulmonary metastases. Little is known about the accuracy of FDG-PET in detecting extrathoracic malignancies that have spread to the lungs. The aim of the current study was to determine the sensitivity and factors that affect the sensitivity of FDG-PET when used in patients with metastatic pulmonary nodules.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Statistics
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 
Patients who underwent lung resection for pulmonary metastases from extrathoracic malignancies at the Mayo Clinic, Rochester were eligible for the study. Between September 17, 2002, and December 27, 2006, there were 323 patients who underwent pulmonary metastasectomy. Five (2.2%) patients were excluded from the analysis because of refusal to participate in research. An FDG-PET plus a chest CT scan or a fused/integrated FDG-PET/CT scan was performed within 6 weeks of pulmonary metastasectomy as part of a metastatic evaluation in 83 patients and this group forms the basis of this analysis. The remaining 235 (72.8%) patients were excluded from analysis because they did not have both a CT and FDG-PET before their pulmonary resection or the imaging was performed greater than 6 weeks prior to their pulmonary resection. Seven patients underwent planned sequential metastasectomies and did not undergo a repeat FDG-PET/CT in the interval between operations. One patient underwent preoperative chemotherapy after the imaging studies and also did not undergo repeat FDG-PET/CT prior to his operation. Ten patients included in the analysis had a diagnosis of diabetes mellitus. The study was approved by the Mayo Foundation institutional review board.

Medical records were reviewed for age, gender, race, primary tumor type, chest CT and FDG-PET results, type of pulmonary resection, number, grade, and histopathology of the nodules removed. Chest CT results were transcribed based on the clinical report, as well as review of the images, with nodule measurement when necessary. Maximal nodule diameter measured by CT and pathology correlated well with each other (Fig. 1 ). FDG-PET imaging results were abstracted from the radiology reading at our institution even if the study was performed elsewhere. FDG-PET imaging was performed at our institution on a GE Advance PET tomograph or DLS/DRX combined PET/CT scanner (General Electric Medical Systems, Inc., Milwaukee, WI). The F-18 fluoride was produced by an on-site GE Trace Cyclotron (GE Medical Systems). FDG Synthesis was performed by standard methods. FDG was tested for sterility, pyrogenicity, and radiochemical purity on each production run.


Figure 1
View larger version (20K):
[in this window]
[in a new window]

  		Fig. 1. Nodule measurements by CT and pathology.

 
PET emission images of the body to include the infracranial head, neck, chest, and abdomen to at least the level of the iliac crest were obtained 60 min after intravenous injection of 740 MBq of FDG. After voiding, the patients were positioned on the tomographic gantry for imaging.

Emission images were reconstructed using iterative reconstruction. Attenuation correction was used on all data. The CT data used for attenuation correction in the PET/CT fusion scans and the uncorrected data were available for review. Emission data were corrected for scatter, random events, and deadtime losses using the manufacturer's software. Image pixel size was 4.25 mm, displayed in a 128-by-128 array. Standard orthogonal views, as well as maximum intensity projections, were reviewed during scan interpretation. FDG activity in lung nodules that was greater than mediastinal blood pool activity was identified as positive for disease.


   3. Statistics
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Statistics
4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 
The primary endpoint is the histopathology of the pulmonary nodule. Demographic and predictor variables were summarized in descriptive statistics (frequency, percentage). Univariate or multivariate analyses were first performed on all operations regardless of how many operations each patient had. Pearson chi-square test, Fisher's exact tests or logistic regression model were used as appropriate. A final multivariate analyses by fitting generalized estimating equations (GEE), where each patient with multiple operations and nodules was considered as a cluster, was adopted to verify predictors of FDG-PET positivity [3]. Pearson correlation coefficient was also used to measure the association between CT and pathology measurements. Statistical significance was predetermined as a p value of <0.05. All analyses were performed by the SAS/STAT version 9.1.3 software (SAS institute Inc. Cary, NC).


   4. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Statistics
 4. Results
5. Discussion
 6. Conclusion
 Appendix A
 References
 
There were 41 men and 42 women whose median age was 61 years old (range, 32–87 years). A total of 104 pulmonary operations were performed, 53 on the right lung, 47 on the left and 4 bilaterally at the same operative setting; 100 operations were done through a standard posterior lateral thoracotomy and 4 through a median sternotomy. A single operation was performed in 68 patients, two in 8, three in 4, and four in 2 patients. Planned sequential thoracotomies were performed in seven patients and the median interval between the FDG-PET and the second operation was 42 days (range, 18–84 days). The resections performed were a wedge excision in 84, a segmentectomy in 5, a lobectomy in 10, a pneumonectomy in 1, and a combination of resections in 4. There were 154 malignant nodules removed; 88 on the right and 66 on the left. There was 1 nodule resected from 47 patients, 2 from 14, 3 from 12, 4 from 7, and 5 in 3 patients. The histopathology of the nodules was adenocarcinoma in 94 (colorectal in 70, endometrium in 8, parotid in 5, pancreas and uterus in 4 each and breast, esophagus and lung in 1 each), sarcoma in 18 (leiomyosarcoma in 10, fibrosarcoma and synovial sarcoma in 4 each), squamous cell in 15, renal cell in 7, papillary thyroid carcinoma in 5, melanoma and chronic lymphocytic leukemia in 4 each, hepatocellular, and transitional cell carcinomas in 2 each, and Hürthle cell carcinoma, adrenocortical carcinoma and cholangiocarcinoma in 1 each (Table 1 ).


View this table:
[in this window]
[in a new window]

  		Table 1 Cell type frequency and FDG-PET positivity.
 
At least 1 nodule was FDG-PET positive in 68 patients (81.9%). Of all 154 malignant nodules, FDG-PET was positive in 104 (67.5%) and negative in 50 (32.5%). The overall sensitivity was 67.5%. There was 1 FDG-PET positive nodule in 44 patients, 2 in 14, 3 in 8 and 4 in 2. The most frequent location of a resected metastatic nodule was in the right upper lobe. There was no statistical difference in the FDG-PET sensitivity by location of the metastasis. The maximum diameter of the resected nodules ranged from 1 mm to 94 mm (median 13 mm) by pathologic examination (two of the resected nodules were not sized by pathology). By comparison, on CT, the nodule sizes ranged from 0 mm (13 nodules were not seen on CT) to 80 mm (median 11 mm). There was a significant correlation between the size of the nodule and the sensitivity of the FDG-PET (Fig. 2 ). For nodules ranging from 1 mm to 5 mm the sensitivity of FDG-PET was 23.5% (4/17); however, for nodules greater than 25 mm in diameter the sensitivity of FDG-PET was 88.5% (23/26) p < 0.001. Sensitivity of FDG-PET also varied by grade (Table 2 ); however, there was no statistically significant difference between the sensitivities among the four grades. Sensitivity of FDG-PET varied with the cell type (Table 1). Cholangiocarcinoma, adrenocortical carcinoma and Hürthle cell carcinoma all had 100% sensitivity whereas, sarcomas overall had a sensitivity of only 44.4% and no patient with a pulmonary nodule from a fibrosarcoma or synovial sarcoma had a positive FDG-PET.


Figure 2
View larger version (21K):
[in this window]
[in a new window]

  		Fig. 2. FDG-PET positivity versus nodule size.

 

View this table:
[in this window]
[in a new window]

  		Table 2 PET sensitivity by grade of tumor.
 
Univariate analysis revealed that squamous cell carcinoma tumor type, histopathologic grade, and nodule diameter by either CT or pathologic measurement were found to be statistically significant predictors of FDG-PET positivity (Table 3 ). Multivariate logistic model analysis revealed that maximum tumor diameter by CT and histologic grade correlated with increased sensitivity of FDG-PET (p = 0.0106 and < 0.0001, respectively). GEE model also indicates the same trend (p = 0.0308 and < 0.0001, respectively) after adjusting for patient differences.


View this table:
[in this window]
[in a new window]

  		Table 3 Univariate analysis.
 

   5. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Statistics
 4. Results
 5. Discussion
6. Conclusion
 Appendix A
 References
 
We have shown that FDG-PET is only positive in 67.5% of malignant metastatic nodules and that 19% of patients will have a negative FDG-PET despite having at least one metastatic nodule present. The factors identified in this study that affect the sensitivity of FDG-PET for pulmonary metastases are nodule size and cell type. For small nodules (i.e. ≤10 mm) the sensitivity was only 29.6%; whereas, for nodules larger than 10 mm the sensitivity was 87.8%. A similar discrepancy was seen for cell type: only 44% of sarcomas were FDG-PET positive, yet over 93% of squamous cell carcinomas were found to be positive.

The idea of whole body cancer surveillance is very appealing and has, for some, compelled the use of FDG-PET as a screening tool for recurrence of various malignancies. While much has been published about the sensitivity of FDG-PET for pulmonary nodules in primary lung cancer, little information has been available on the sensitivity of PET for metastatic pulmonary lesions from extrathoracic malignancies. Our findings of a sensitivity of only 68% highlight the need for caution when using FDG-PET to screen for the presence of otherwise occult pulmonary metastases. The use of FGD-PET for this purpose is not supported for use in sarcomas or in patients with pulmonary nodules less than 1 cm.

Since lung is the second most common site for tumor metastasis after the liver and 20–54% of oncologic patients will have a pulmonary metastasis diagnosed at some point in the natural history of their disease, some form of surveillance of the lungs is recommended [4]. Computed tomography, with the addition of maximum intensity images (MIP), is an excellent surveillance modality [5]. This should be the initial means for routine follow-up of the lung for patients that are at risk for developing metastases. If the CT shows pulmonary nodules, FDG-PET may be used to identify extrathoracic disease with the caveat that the interpretation of FDG-PET negative pulmonary nodules should be made cautiously.

Pulmonary metastasectomy is a standard therapeutic procedure in carefully selected patients with metastasis to the lung. Survival rates with resection are far better than expected after chemotherapy or radiotherapy alone [6]. Complete pulmonary resection has been shown to improve long-term survival with actuarial survival at 5 years of 30% to 50% for various types of tumors. This is in striking contrast to patients who have an incomplete resection where survivals figures are 0–13% at 5 years. To find and remove all pulmonary metastases is therefore important, thus relying on FDG-PET with its low sensitivity is not an adequate exam to detect all pulmonary nodules, when resection for cure is being considered. Survival after pulmonary metastasectomy is also influenced by factors other than completeness of resection. Shorter disease free interval (DFI), increasing number of metastatic nodules, and positive lymph nodes at the time of resection have all been shown to worsen overall prognosis [6–8].

The limited sensitivity of FDG-PET for small nodules that we found has been previously reported by others. Gould published a meta-analysis of 1474 pulmonary nodules evaluated by FDG-PET, and concluded that FDG-PET has an overall high specificity but variable sensitivity for nodules less than 1 cm [2]. More recently, Nomori and colleagues prospectively looked at 136 benign and malignant nodules less than 3 cm in diameter which had been referred for surgical treatment [9]. They found that all malignant nodules less than 1 cm were falsely negative on FDG-PET. If the lesion in question was a ground-glass opacity (GGO), the accuracy of FDG-PET was also poor, with 90% of malignant GGOs being falsely negative and four of five inflammatory GGOs being falsely positive [9]. In another report, Reinhardt and colleagues analyzed 438 metastatic pulmonary lesions with diameters of 3–60 mm utilizing a fused FDG-PET/CT scan [10]. Overall, they showed that only 174 nodules (39.7%) were positive by FDG-PET. No nodules smaller than 5 mm were positive on FDG-PET but if the nodule diameter was greater than 13 mm, sensitivity was 100%. They concluded that FDG-PET sensitivity is significantly reduced for lesions with a diameter less than 11 mm. In another report, De Wever and colleagues found integrated FDG-PET/CT had a sensitivity of 100% compared to 83% for PET alone in nodules <10 mm, the majority of these nodules were 5–10 mm in diameter. In this particular study, the remarkably increased sensitivity came at the cost of a significant lowering of the specificity to only 5% [11].

The ability to detect a lesion by FDG-PET is dependent upon the presence of a sufficient number of metabolically active cells. This is explained by the physical mechanisms by which FDG-PET scanning is possible. 18F-Fluorodeoxyglucose has an excess in protons and as a consequence, it is unstable. Its decay occurs by releasing the excess protons, which collide with electrons, emitting two 511 keV photons in 180° opposing directions. The detection of these photons by the PET camera generates the image. The concomitant detection of background gamma photons limits the spatial resolution of small nodules [12,13]. In vitro the minimal detection limit of FDG-PET is about 106 cells, which corresponds to a tumor diameter of 1 mm. Therefore, other factors (i.e. respiratory movement, thickness of surrounding soft tissue and other structures, etc.) play a major role in limiting FDG-PET sensitivity, especially in the lower lung fields. [14] Intense research is being undertaken to minimize artifacts caused by respiratory motion in the acquisition of FDG-PET images, but no single technique has yet proven satisfactory. Thus FDG-PET remains unreliable for nodules less than 10 mm in maximum diameter.

The degree of FDG activity is directly related to glucose metabolism, which is increased in malignant cells. This has been confirmed in laboratory studies where cancerous pulmonary nodules have been shown to over-express Glut-1 (glucose transporter protein type I) and HK-II (hexokinase II) [15]. The over-expression of these molecules correlated with FDG-PET activity. In the same study, Mamede also demonstrated that progressive tumor differentiation led to decreased FDG-PET activity and that primary lung adenocarcinomas had lower FDG uptake than squamous cell carcinoma or metastatic adenocarcinoma. This data reinforces our own findings, at least in part, as we showed that squamous cell carcinoma and higher tumor grade metastases were associated with increased FDG-PET sensitivity.

We found by multivariate analysis that both cell type and nodule size affected the sensitivity of FDG-PET. In a recently published series from South Korea no such correlation was found. The authors tried to identify the contributing factors that explain why some malignant nodules ≤1 cm had low or absent 18F-FDG uptake [16]. One hundred and twenty-one (121) patients were analyzed in three groups: solitary versus multiple nodules, presence or absence of additional benign nodules, and imperceptible versus faint 18F-FDG uptake. On multiple regression analysis, none of the variables were statistically significant in distinguishing benign versus malignant nodules.


   6. Conclusion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Statistics
 4. Results
 5. Discussion
 6. Conclusion
Appendix A
 References
 
In conclusion, FDG-PET correctly detected at least one metastatic nodule in 80.9% of patients with proven metastatic pulmonary nodules. We found that 32.5% of malignant nodules were not detected by FDG-PET, thus the sensitivity was only 67.5%. High tumor grade and pulmonary metastasis greater than 10 mm measured by CT scan, or by pathology are independent predictors of FDG-PET positivity. However in patients with a history of an extrathoracic malignancy and newly diagnosed small pulmonary nodules, FDG-PET is not sensitive enough to dictate treatment. FDG-PET should be used as an adjunct to detect extrathoracic recurrence and thus help in proper selection of patients for pulmonary metastasectomy. Furthermore, as a screening tool for pulmonary metastases in patients with a prior cancer, FDG-PET does not provide the necessary sensitivity to supplant CT as the most useful tool currently available for these purposes.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Statistics
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
References
 
Conference discussion

Dr D. Wood (Seattle, WA): I am not surprised that PET doesn’t have a higher sensitivity, but I guess I am a little surprised by the degree of lack of specificity. Is there anything in your patient population that you think might affect this? Is it because of a high degree of sensitivity in picking up nodules that might not otherwise be detected and then are negative on PET? Does it relate to your patient population having other diseases like fungal disease in the chest that may confound the reading of PET imaging? Do you have any reasons to think that some of this might be related to your patient population?

Dr Fortes: I think in a way it could be. Most of these patients had a dedicated CT of the chest performed, and we know that a dedicated CT with fine cuts is far better in detecting nodules than the FDG-PET combined CT scan. So I think that is one possibility.

In terms of fungal infections, if we are talking about other diagnoses that could give a false negative FDG-PET, we would be looking at specificity. In our study we didn’t look at that at all. We wanted to focus on FDG-PET being used as a screening tool, and as a screening tool, sensitivity is mostly important. So I don’t think confounding diseases were an issue here.

Dr F. Detterbeck (New Haven, CT): Interesting study. I want to perhaps challenge you. There is not really an accepted standard of what should be used for PET for smaller nodules. Some people use mediastinal background, some people use the lung, the background of normal lung, some people use attenuation-corrected images, some people use non-attenuation-corrected images. We just heard earlier that perhaps we should be looking at PET at two hours. There are many factors, and as we start looking at PET in smaller lesions, I think we need to explore these other factors. I imagine you haven’t done that, but I wanted to stimulate you to perhaps go back and look at your results and see if other factors could improve that sensitivity to a higher degree.

Dr H. Kim (Seoul, Korea): I wonder how much percent of the nodules include GGO lesions. Were they solid nodules or did they contain the GGO pattern?

Dr Fortes: These were all solid nodules. There were no GGOs included.

Dr Kim: 100% solid nodules?

Dr Fortes: Correct.

Dr H. Kara (Istanbul, Turkey): Did you know the data about the false negativity of the PET scan for distant metastases, because PET scans, as you stated, were from head to thigh, and obviously tibia and femur were omitted. Did you have any data about the false negativity?

Dr Fortes: No, we did not look at extrapulmonary metastases, only at pulmonary metastases.

Dr Wood: Just to follow up on that question, a major reason that we are using PET in the consideration of metastatic disease of the lung is to exclude metastatic disease elsewhere before we consider a patient for metastasectomy. Can you potentially impute what your conclusions from sensitivity within the chest might correspond to outside of the chest and how much reliability we can have on it for screening for extrathoracic metastatic disease?

Dr Fortes: That is definitely the mentality of our group in that, for these patients, FDG-PET should be used as a screening modality for extrathoracic disease in order to properly select patients for metastasectomy. In terms of the reliability of FDG-PET for that purpose, of course it will depend on the type of primary tumor, location, and the way it metastasizes. I can’t give you specific numbers, but we know that FDG-PET has supplanted other modalities, including CT scan, for metastases of the abdomen, and also bone scans. So I think it is possible that the sensitivities for disease inside and outside of the chest are related, but in terms of definite numbers, I really can’t quote you that.


   Footnotes
 
{star} Presented at the 16th European Conference on General Thoracic Surgery, Bologna, Italy, June 8–11, 2008.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Statistics
 4. Results
 5. Discussion
 6. Conclusion
 Appendix A
 References
 

  1. Society AC. American Cancer Society. Global Cancer Facts and Figures 2007; 2007.
  2. Gould MK, Maclean CC, Kuschner WG, Rydzak CE, Owens DK. Accuracy of positron emission tomography for diagnosis of pulmonary nodules and mass lesions: a meta-analysis. JAMA 2001;285:914-924[see comment].[Abstract/Free Full Text]
  3. Hanley JA, Negassa A, Edwardes, MD, Forrester JE. Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol 2003;157:364-375[see comment].[Abstract/Free Full Text]
  4. Rodriguez E, Cohn HH, Friedberg JS. In: Selke FW, Nido PJd, Swanson SJ, editors. Secondary lung tumors. Philadelphia: Elsevier Saunders; 2005. pp. 337-354.
  5. Bradley JD, Nofal AN, El Naqa IM, Lu W, Liu J, Hubenschmidt J, Low DA, Drzymala RE, Khullar D. Comparison of helical, maximum intensity projection (MIP), and averaged intensity (AI) 4D CT imaging for stereotactic body radiation therapy (SBRT) planning in lung cancer. Radiother Oncol 2006;81:264-268.[CrossRef][Medline]
  6. Pastorino U, Buyse M, Friedel G, Ginsberg RJ, Girard P, Goldstraw P, Johnston M, McCormak P, Pass H, Putnam JB. Long-term results of lung metastasectomy: prognostic analyses based on 5206 cases. The International Registry of Lung Metastases. J Thorac Cardiovasc Surg 1997;113:37-49.[Abstract/Free Full Text]
  7. Ercan S, Nichols 3rd FC, Trastek VF, Deschamps C, Allen MS, Miller DL, Schleck CD, Pairolero PC. Prognostic significance of lymph node metastasis found during pulmonary metastasectomy for extrapulmonary carcinoma. Ann Thorac Surg 2004;77:1786-1791.[Abstract/Free Full Text]
  8. Cerfolio RJ, Allen MS, Deschamps C, Daly RC, Wallrichs SL, Trastek VF, Pairolero PC. Pulmonary resection of metastatic renal cell carcinoma. Ann Thorac Surg 1994;57:339-344.[Abstract]
  9. Nomori H, Watanabe K, Ohtsuka T, Naruke T, Suemasu K, Uno K. Evaluation of F-18 fluorodeoxyglucose (FDG) PET scanning for pulmonary nodules less than 3 cm in diameter, with special reference to the CT images. Lung Cancer 2004;45:19-27[see comment].[CrossRef][Medline]
  10. Reinhardt MJ, Wiethoelter N, Matthies A, Joe AY, Strunk H, Jaeger U, Biersack HJ. PET recognition of pulmonary metastases on PET/CT imaging: impact of attenuation-corrected and non-attenuation-corrected PET images. Eur J Nucl Med Mol Imaging 2006;33:134-139.[CrossRef][Medline]
  11. De Wever W, Meylaerts L, De Ceuninck L, Stroobants S, Verschakelen JA. Additional value of integrated PET-CT in the detection and characterization of lung metastases: correlation with CT alone and PET alone. Eur Radiol 2007;17:467-473.[CrossRef][Medline]
  12. Vansteenkiste JF, Stroobants SG. The role of positron emission tomography with 18F-fluoro-2-deoxy-D-glucose in respiratory oncology. Eur Respir J 2001;17:802-820.[Abstract/Free Full Text]
  13. Yamamoto S, Matsumoto K, Sakamoto S, Tarutani K, Minato K, Senda M. An intra-operative positron probe with background rejection capability for FDG-guided surgery. Ann Nucl Med 2005;19:23-28.[CrossRef][Medline]
  14. Fischer BM, Olsen MW, Ley CD, Klausen TL, Mortensen J, Hojgaard L, Kristjansen PE. How few cancer cells can be detected by positron emission tomography? A frequent question addressed by an in vitro study. Eur J Nucl Med Mol Imaging 2006;33:697-702.[CrossRef][Medline]
  15. Mamede M, Higashi T, Kitaichi M, Ishizu K, Ishimori T, Nakamoto Y, Yanagihara K, Li M, Tanaka F, Wada H, Manabe T, Saga T. [18F]FDG uptake and PCNA, Glut-1, and hexokinase-II expressions in cancers and inflammatory lesions of the lung. Neoplasia (New York) 2005;7:369-379.
  16. O JH, Yoo Ie R, Kim SH, Sohn HS, Chung SK. Clinical significance of small pulmonary nodules with little or no 18F-FDG uptake on PET/CT images of patients with nonthoracic malignancies. J Nucl Med 2007;48:15-21.[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 Ann. Thorac. Surg.Home page
L. Erhunmwunsee and T. A. D'Amico
Surgical management of pulmonary metastases.
Ann. Thorac. Surg., December 1, 2009; 88(6): 2052 - 2060.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Daniel L. Fortes
Mark S. Allen
Val J. Lowe
Dennis A. Wigle
Stephen D. Cassivi
Francis C. Nichols
Claude Deschamps
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Fortes, D. L.
Right arrow Articles by Deschamps, C.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Fortes, D. L.
Right arrow Articles by Deschamps, C.
Related Collections
Right arrow Lung - cancer

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS