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Ann Thorac Surg 2004;78:1017-1023
© 2004 The Society of Thoracic Surgeons
a Section of Thoracic Surgery, University of Alabama at Birmingham, and Division of Cardiothoracic Surgery, Department of Surgery, Birmingham Veterans Administration Hospital, Birmingham, Alabama, USA
b Department of Epidemiology, University of Alabama at Birmingham, School of Public Health, Birmingham, Alabama, USA
c Division of Clinical Nuclear Medicine, University of Alabama at Birmingham, Birmingham, Alabama, USA
d Department of Biostatistics, University of Alabama at Birmingham, School of Public Health, Birmingham, Alabama, USA
Accepted for publication February 18, 2004.
* Address reprint requests to Dr Cerfolio, Division of Cardiothoracic Surgery, University of Alabama at Birmingham, 1900 University Blvd, THT 712, Birmingham, AL, USA 35294
robert.cerfolio{at}ccc.uab.edu
Presented at the Fiftieth Annual Meeting of the Southern Thoracic Surgical Association, Bonita Springs, FL, Nov 13–15, 2003.
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Abstract |
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 Top Abstract IntroductionPatients and methodsResultsCommentDiscussionReferences |
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METHODS: A prospective blinded trial was performed on a consecutive series of patients with NSCLC. Patients underwent integrated PET-CT scanning with 2-[18F]-fluoro-2-deoxy-D-glucose (FDG-18). A radiologist assigned the T, N and M status. No sooner than 2 weeks the same radiologist read the dedicated PET alone, without the integrated CT images and a T, N and M status was assigned again. The most recent CT scan was available and visually correlated with both studies. All patients underwent biopsies of suspicious N2 or N3 lymph node or distant metastases and if negative, pulmonary resection with lymphadenectomy was performed.
RESULTS: There were 129 patients. Integrated PET-CT is a better predictor than PET for all stages of cancer and achieved statistical significance for stage I (52% versus 33%, p = 0.03) and for stage II (70% versus 36%, p = 0.04). It also is a better overall predictor for T status (70% versus 47%, p = 0.001) and the N status (78% versus 56%, p = 0.008). Nodal analysis shows that integrated PET-CT was more accurate for the total N2 nodes (96% versus 93%, p = 0.01) and for the total N1 nodes (90% versus 80%, p = 0.001). It was also more sensitive, specific, and had a higher positive predictive value for both N2 and N1 nodes (p < 0.05 for all). Integrated PET-CT is significantly more sensitive at the 4R, 5, 7, 10L and 11 stations and more accurate at the 7 and 11 lymph nodes stations than dedicated PET.
CONCLUSIONS: Integrated PET-CT using FDG-18 better predicts stage I and II disease as well as the T and N status of patients with NSCLC when compared with dedicated PET alone. It is more accurate at some nodal stations but still only achieves an accuracy of 96% and 90% for the N2 and N1 nodes, respectively.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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Inclusion criteria into this study required patient age of 19 years or greater, a whole body integrated PET-CT scan performed at our institution within 4 weeks of surgery, a chest CT scan performed within 4 weeks of surgery, and histopathologically proven NSCLC either before scanning or after surgical resection. In addition, patients who underwent preoperative chemotherapy were included in this study if they were restaged after the completion of their therapy with a repeat integrated PET-CT and CT scans. Patient who had a history of type 1 diabetes, who underwent preoperative radiotherapy, had PET scanning performed elsewhere, or who had a benign pulmonary nodule resected were excluded.
Imaging
Patients were asked to fast for 4 hours and then subsequently received 555 MBq (15 mCi) of FDG intravenously, and CT images followed by PET scans were obtained after 1 hour. These images constituted the integrated PET-CT aspect of this study. They were prospectively analyzed by one nuclear radiologist (B.O.). He assigned a T, N, and M status based on the integrated PET-CT images using the International System for Staging [1]. No sooner than 2 weeks later, the same radiologist, masked to any pathologic or surgical results, reloaded the images and read the PET portion alone without the CT images and assigned a T, N, and M status. These images constituted the dedicated PET aspect of this study. The radiologist had the most recent CT scan of the chest available when he read both the PET and the PET-CT and used it to visually correlate his findings.
All N2 stations were numbered on the reports. The only N1 nodes specifically numbered were the 10 and 11 stations. Lymph nodes were considered malignant if the maximum standardized uptake value (SUV) was greater than 2.5. Similarly, lesions in distant metastatic (M) sites that had a maximum SUV of 2.5 or greater were also called positive.
The efficacy of each individual nodal station was determined by calculating sensitivity, specificity, positive predictive value, negative predictive value, and accuracy. Biopsies were obtained of suspicious N2 and N3 nodes by either mediastinoscopy to assess the 2s, 4s, and proximal 7 lymph nodes, transesophageal ultrasound with fine-needle aspirate for mid and distal 7, 8, and 9 nodes, and left video-assisted thoroscopy (VATS) or Chamberlin for the 5 and 6 nodes. Any N3 disease was assessed on all patients who underwent mediastinoscopy. If patients were N2 or N3 negative, they underwent thoracotomy, pulmonary resection, and complete thoracic lymphadenectomy. If they were N2 positive, they underwent neoadjuvant therapy and then were restaged at the completion of their therapy with a repeat PET-CT and CT scan. If resected, the most recent scans were used for this study. All suspicious metastatic M1 lesions were biopsied unless tumor was suspected in the bone or brain, in which case magnetic resonance imaging (MRI) was considered the gold standard.
Procedures and surgery
Operations were performed in a university setting (University of Alabama at Birmingham) by one general thoracic surgeon (R.J.C.). Nodes completely removed in the right chest included the 2R, 4R, 7, 8, 9, and 10R stations along with the rest of the N1 nodes contained in the part of the lung that was resected (11, 12, 13, and 14). In the left chest, the lymph nodes completely resected included the 5, 6, 7, 8, 9, and 10L stations and the rest of the N1 nodes contained in the part of the lung resected (11, 12, 13, and 14). The N1 nodes were defined as nodes 10, 11, 12, 13, and 14. The N2 nodes were defined as any single digit node in the ipsilateral chest. Pathologic review was performed using standard techniques and immunohistochemical staining was employed when appropriate.
Statistical analysis
Information was entered into a prospective database. Histopathologic staging information was stored in a separate file. These two files were merged at the conclusion of the study.
Analysis for the tumor (T status), N (nodal), and metastatic (M status) was performed as a patient analysis. In addition, we performed a nodal analysis for each lymph node station. We did not do a separate analysis for the individual M sites because the numbers were too low.
Sensitivity, specificity, positive predicted value, negative predictive value, and accuracy were compared using the binomial approximation test. The 
2 test or Fisher's exact test was used to compare all other variables. A p value of 0.05 or less was considered statistically significant. The SAS version 8.02 (SAS Institute, Cary, NC) and Epi Info 2000 (CDC, Atlanta, GA) were used for the statistical analysis. The University of Alabama at Birmingham Institutional Review Board approved this study, and individual patient consent was obtained to be in this prospective database.
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Results |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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Table 2 shows that integrated PET-CT was more accurate than dedicated PET for each stage, and this achieved statistical significance for stages I and II. A separate analysis was performed excluding 33 patients who underwent neoadjuvant chemotherapy. The same results were obtained. A third analysis that examined only these 33 patients found a statistical advantage for PET-CT over PET for patients with stage Ib and II disease only.
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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The terminology for PET software and hardware is confusing and is summarized in Table 1. We were very interested in the results of patients with T2, T3, and N1 disease because this information may be important to know before surgery given some recent reports [6] and several ongoing national and international trials.
The patient analysis found that integrated PET-CT was a better predictor of stage I and II disease than dedicated PET and also a better predictor for the overall T and N status. The separate nodal analysis shows that integraeted PET-CT was more accurate for the total N2 nodes (96% versus 93%, p = 0.01) and for the total N1 nodes (90% versus 80%, p = 0.001), more sensitive at the 4R, 5, 7, 10L, and 11 stations, and more accurate at the 7 and 11 lymph nodes stations than dedicated PET. This study is unique in that it specifically addresses the individual T status of integrated PET-CT and the accuracy of individual N1 and N2 nodal stations. In 2003 Lardinois and associates [16] described the superiority of integrated PET-CT over dedicated PET, but that study only had 50 patients, not all underwent full staging, and a separate T, N or M or nodal analyses was not performed.
Patient analysis is quite different from a nodal analysis, and the distinction is important. For example, consider a patient with an integrated PET-CT report that predicted a T2N2M0 lesion in the right upper lobe, and it predicted the 2R lymph node station as the only site of metastatic cancer. If the patient underwent resection and was found to have metastatic N2 disease in the 9 lymph node station only, the PET-CT would be considered correct by patient analysis—the patient was T2N2M0—yet it was incorrect at both the 2R and the 9 stations. Thus, the nodal analysis is a more precise method of evaluating the accuracy of a test. Few reports have used this type of data analysis (Table 6).
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Interestingly, we found that integrated PET-CT was more accurate at determining patients who were complete responders than was dedicated PET alone. These patients may benefit the most from surgical resection. This information may be important for the medical oncologists to help assess the effectiveness of the neoadjuvant therapy and help guide further treatment plans.
Despite the use of integrated PET-CT routinely in our practice, we have noted that our clinical stage often differs from the pathologic stage. There remain significant false positives and negatives. We believe that integrated PET-CT helps direct one toward targets for biopsies to rule out nodal or systemic disease. All suspicious areas should be biopsied, but the practice of calling a positive PET or PET-CT scan definite evidence of cancer is absolutely wrong.
The future of PET-CT is promising. New machines with improved resolution are around the corner, along with new radiopharmaceutical agents. Each new agent must be carefully assessed in order to determine its accuracy at each nodal station and at each metastases site.
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Discussion |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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At the end of your presentation, you mentioned the ongoing induction therapy trials, but I think we have to be skeptical that they are going to be very helpful. The studies that show a benefit are flawed, and there are more and more data that it is really adjuvant therapy that is going to be more useful. Thus, knowing the precise TNM stage is not so valuable because you are going to have the pathologic stage anyway.
So in light of that, I wonder if you could take your results and put them in the framework that Pieterman did in the New England Journal of Medicine paper, that Kalff did in the JCO paper and that Van Tinteren did in the Lancet paper and say how many of the patients with PET-CT would you really have done anything different? You certainly wouldn't have done anything different if you knew they were T1 versus T2, but you might have if you had known they were T4. So in how many of the patients did the difference demonstrated by integrated PET-CT change what you had done?
Secondly, who reads the CT portion of your PET-CTs? Is it you, is it the nuclear medicine physician; does it have to be then transmitted electronically back to the non-nuclear diagnostic radiologists for reading, and do they get reimbursed for that?
Lastly, you mentioned in your methods that this was somehow randomized. Maybe you misspoke. It didn't look like there was a randomization.
DR CERFOLIO: It was blinded and prospective not randomized.
DR D'AMICO:Good. I thought it was an excellent study and it will be a great contribution to the literature.
DR CERFOLIO: Dr D'Amico, thank you very much for your kind comments—coming from you that means a lot to me, I appreciate that.
You have three questions, the last one I have already answered—it is obviously not randomized but is blinded and prospective.
Your second question is who reads the CT scan. This is an extremely important question. In general, nuclear radiologists do not have much knowledge of radiologic chest anatomy, especially compared to a CT chest radiologist. This becomes important if one asks them to number the lymph nodes according to a classification system, which is a necessary and critical step if one is to assess the accuracy at each nodal station. Since we have done many prospective studies on PET and are involved in others, this issue is important. We required one nuclear radiologist who reads all the studies in this series and in the other papers to learn how to read chest CT scans first. He did this for several months and at first did it combined with one of our four chest radiologists. After about 3–4 months, he is very good and he does it independently now. In general though, for other centers I would recommend that a nuclear radiologist and a chest radiologist read them together.
Your final question is about the number of patients for whom integrated PET-CT changed the care of patients. The data from Depierre is provocative and we are very active participants in the S9900 trial and have placed over 80 patients in that trial already. I believe that trial will better answer the question about pre-operative chemotherapy for patients with N1 and T2 or T3 lesions—I would not be so quick to dismiss this concept. In fact, I suspect that future studies may show that neoadjuvant therapy followed by resection followed by adjuvant therapy will be superior to resection followed by adjuvant therapy alone. If there is survival benefit for these patients, then the integrated PET-CT will affect many patients' pre-operative care. If one only talks about the M1 and N2, the integrated PET-CT still led to significant changes in pre-operative patient management since we found that it was more accurate for both N2 and M1 disease. As far as comparisons to the other articles you have mentioned, we had more rigorous criteria and, unlike in those manuscripts, all of our patients had every node removed. Thank you for your kind comments and good questions.
DR TODD L. DEMMY (Buffalo, NY): The question is related to this technology and the institutions that want to adopt it. One concern is that the combined scanner does not have the new upgrades in CT scanning, so that patients have to undergo another spiral CT. And what about technology that can fuse CT images with the best available PET scan? Is that a better technology for institutions to invest in or should they go with integrated units?
DR CERFOLIO: It is a great question. I can't answer that because I haven't done a prospective trial. But I don't think the fusion technology where the patients are in different settings and get different examinations and there is artifact and other factors is going to be as accurate. But I don't know that. That is an opinion. Beware of the surgeon with an opinion.
Your second question is about the CT scans, and it depends on the logistics and how your center is set up, but I think if you want to have PET, and we get a lot of e-mails, if you are going to get a PET and sink $2 million, I would say get an integrated PET over a PET alone. Another advantage of an integrated PET-CT machine is that if there are no patients to PET, one can use the machine to do CT scanning. This compares favorable to PET alone where the room and staff will sit idle. Thank you.
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