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Ann Thorac Surg 2004;78:1152-1160
© 2004 The Society of Thoracic Surgeons
a Departments of Thoracic and Cardiovascular Surgery, Houston, TX, USA
b Radiology, Houston, TX, USA
c Gastrointestinal Oncology, Houston, TX, USA
d GI Medicine and Nutrition, Houston, TX, USA
e Radiation Oncology, Houston, TX, USA
f Nuclear Medicine, Houston, TX, USA
g Pathology, University of Texas M. D. Anderson Cancer Center, Houston, Texas, USA
Accepted for publication April 12, 2004.
* Address reprint requests to Dr Swisher, Department of Thoracic and Cardiovascular Surgery, University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd, Unit 445, Houston, TX 77030, USA
sswisher{at}mdanderson.org
Presented at the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.
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Abstract |
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METHODS: One hundred three sequential patients with locoregionally advanced esophageal cancer, who were treated with CRT and esophageal resection between May 2001 and November 2003 at the University of Texas M.D. Anderson Cancer Center, were retrospectively reviewed. PET, EUS, and CT were performed before (pre) or after (post) CRT and before surgical resection. PET standardized uptake value (SUV) was defined as maximal uptake in primary tumor.
RESULTS: Most patients were male (91 [88%]) with adenocarcinoma (90 [87%]). Pretreatment clinical stages were: IIA (42 [41%]), IIB (5 [5%]), III (50 [49%]), and IVA (6 [6%]). At the time of surgery, 58 patients (56%) had a pathologic response to CRT (
10% viable cells). Post-CRT measurements that correlated with pathologic response were: CT esophageal wall thickness (13.3 vs 15.3 mm, p = 0.04), EUS mass size (0.7 vs 1.7 cm, p = 0.01) and PET SUV (3.1 vs 5.8, p = 0.01). Post-CRT PET SUV equal to or greater than 4 had the highest accuracy for pathologic response (76%). Univariate and multivariate Cox regression analysis demonstrated that a post-CRT PET SUV equal to or greater than 4 was an independent predictor of survival (HR, 3.5, p = 0.04).
CONCLUSIONS: The FDG-PET SUV is the most accurate noninvasive test to predict long-term survival after preoperative CRT and before surgical resection. Post-CRT FDG-PET cannot, however, rule out residual microscopic disease so esophagectomy should remain a therapeutic option even if the post-CRT imaging modalities are normal.
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Introduction |
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Material and Methods |
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Treatment Plan
All patients were treated either on institutional protocols (n = 46) with induction chemotherapy followed by concurrent CRT or off-protocol (n = 57) with concurrent CRT alone. Patients treated on institutional protocols received up to two cycles of CPT-11 (45 mg/m2), taxotere (33 mg/m2), and 5-fluorouracil (2 g/m2 as a 24-hour infusion). This was followed by concurrent radiotherapy (50.4 Gy in 28 fractions) and CPT-11 (30 mg/m2 per week for 5 weeks), taxotere (20 mg/m2 per week for 5 weeks) and 5-fluorouracil (300 mg/m2 per day). Patients treated off-protocol received concurrent CRT consisting of radiotherapy (50.4 Gy in 28 fractions) and chemotherapy consisting of either cisplatin and 5-fluorouracil, or taxol and carboplatin.
Patients were evaluated before (pre-CRT) or after (post-CRT) chemoradiation with EUS, CT of the chest and abdomen, and FDG-PET imaging. These noninvasive studies were obtained 3 to 5 weeks after the completion of CRT. Surgical resection was performed 5 to 8 weeks after completion of CRT. The type of esophagectomy performed was dependent on the tumor's location and individual surgeon's preference. Either a transthoracic approach (Ivor-Lewis, or total) or a transhiatal approach was used to resect the tumor. Mediastinal and celiac lymph nodes were resected in all patients who underwent surgery. Only lower mediastinal lymph nodes were removed by transhiatal resection.
Pathologic responses were determined at the primary tumor site at the time of resection: complete response (no viable tumor), microscopic residual (> 0% to 10% viable), or macroscopic residual (> 10% viable). These criteria for pathologic response were utilized because of previous experience demonstrating that they identified a subset of patients with increased long-term survival [4, 16]. Pathologic responders were defined as those having equal to or less than 10% viable cancer cells at the primary malignancy (ie, complete response and microscopic residual), whereas nonresponders were defined as those having more than 10% viable cancer cells at the primary malignancy (macroscopic residual).
Short-term outcome after surgery including pathologic response was collected prospectively and long-term outcome information regarding overall survival was obtained from hospital records, patient follow-up, and The University of Texas M.D. Anderson tumor registry.
Treatment Evaluation: FDG-PET, CT, EUS
The FDG-PET images were obtained on a Siemens HR+ tomograph (Siemens Medical Systems, Hoffman Estates, IL; resolution, 4.5x4.5x4.5 mm; full width half maximum [FWHM]). All patients fasted for at least 4 hours before PET. Imaging was performed 45 to 60 minutes after intravenous injection of FDG (15 to 20 mCi). The area imaged extended from the middle of the neck to the upper thighs. Transmission scanning was done over the chest and abdomen from 5 or 6 overlapping bed positions and using a rotating germanium-68 pin source, corresponding emission images were also obtained. The PET images were reconstructed by software running standard vendor-provided reconstruction algorithms, and by ordered subset expectation maximization (OSEM). Emission data were corrected for scatter, random events, and dead-time losses using Siemens's software, and images were reconstructed both with and without attenuation correction. Images were analyzed visually and quantitatively to determine the standardized uptake value (SUV) for local malignancy and metastases. To determine the sensitivity, specificity, and accuracy of FDG-PET in identifying residual disease after preoperative CRT and before esophagectomy, PET images were interpreted retrospectively by an experienced nuclear medicine specialist (H.M.) and radiologist (J.J.E.), both were blinded to all clinical data and their findings were recorded by consensus. Images were reviewed in all standard planes along with maximum intensity projection images. PET scans were reviewed in combination with CTs whenever possible. On visual analysis, an abnormality was defined as any instance when FDG uptake was substantially greater than mediastinal blood pool activity on the attenuation-corrected images. Maximum intensity of FDG uptake in the primary tumor, locoregional nodal involvement, and distant sites was assessed as present or absent. Attempts were made to assess local and total tumor burden by measuring the maximal value in each area. A pixelated region of interest (ROI) was outlined within any region of increased FDG uptake and, after correction for radioactive decay, analyzed semiquantitatively according to the following formula:
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All CT scans of the chest and abdomen and pelvis were performed on a HiSpeed or Lightspeed Advantage scanner (General Electrical Medical Systems, Milwaukee, WI). Oral (2% barium sulfate) and intravenous (150 mL Optiray 320, 3 mL/s) contrast material was administered. CT scans of the chest and abdomen were performed 25 seconds and 55 to 65 seconds after contrast administration, respectively. Collimation of 3.75 to 7 mm (chest) and 7 to 7.5 mm (abdomen), and a pitch ratio of 1.5:1 was used. CT images of the chest and abdomen were reviewed on a picture archiving and communication system (PACS) workstation and measurements of maximal dimension of the primary tumor/esophageal wall thickness were performed retrospectively and independently by two observers (M.M., J.J.E.) using electronic calipers. The cross -sectional diameter of the thickest part of the lesion was identified and divided by two. Locoregional nodal involvement (> 10 mm in diameter) was noted. The clinical stage was defined according to the EUS assessment for the primary tumor and regional lymph nodes. Biopsies were not obtained of enlarged nodes. No distant metastases were documented in this study since patients were selected for the review only if they underwent surgery and demonstrated resectable disease following preoperative CRT. Observers were blinded to clinical data and findings were recorded by consensus.
Statistical Analysis
Survival probability analyses were performed using the Kaplan-Meier method. Survival was calculated from the date of surgery to the date of death or most recent follow-up contact. Analysis of survival excluded patients who died of noncancer-related causes within 30 days after surgery. Statistical significance was assessed by log-rank test. Independent predictive factors for survival were determined by Cox regression analysis. Univariate analyses were performed by X2 analysis. Two-tailed p values of equal to or less than 0.05 were considered significant. Data analysis was performed by our departmental biostatistician (A.M.C.) with SPSS (SPSS, Chicago, IL) and Graph Pad Prism (Graph Pad Prism, San Diego, CA) software. Statistical significance was accepted as p less than 0.05.
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10% viable cells in primary malignancy), although 45 patients (44%) were nonresponders (> 10% viable cells in primary malignancy).
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Treatment Evaluation
Multiple retrospective assessments were performed with pre-CRT and post-CRT evaluations including CT scan of esophageal wall thickness and assessment of TNM stage); EUS of the length of mucosal involvement and assessment of TNM stage; and PET assessment of SUV of primary malignancy, primary + regional + distant. Analyses were performed both of the post-CRT measurement and the relative percent change with treatment [(pre-post)/pre]x100. The measurements that correlated most closely with pathologic response are listed in Table 2. Table 2 demonstrates the post-CRT evaluation was able to distinguish responders from nonresponders more consistently than the percent decrease with pre-CRT and post-CRT studies although this study was not powered to prove this statistically. Assessments of TNM status were not useful (data not shown). From the post-CRT evaluations (Table 2) we developed thresholds for each modality to differentiate pathologic responders from nonresponders (CT [esophageal thickness, 
14.5 mm]; EUS [mucosal mass length, 1cm]; PET [primary SUV, 4]; and PET [primary + regional + distant SUV, 6]). We then utilized these thresholds to assess the sensitivity, specificity and accuracy of each modality for pathologic nonresponse. Post-CRT PET SUV of the primary was the most accurate (76%) in assessment of pathologic nonresponse (Table 3).
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Comment |
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Our study resulted in several important findings. First, we confirmed in a larger group of patients that FDG-PET imaging could identify patients who have a large amount of residual disease (macroscopic residual, >10% viable, pathologic nonresponse) after preoperative CRT. Although FDG-PET imaging is unable to distinguish microscopic residual (<10% viable) disease from a complete pathologic response, it is able to separate out a group of patients with macroscopic residual disease (Table 2). Interestingly, both CT scans and EUS were also able to separate these groups to some extent when esophageal thickness (CT) and mucosal tumor size (EUS) were utilized. Several authors have described changes in size of the mass correlating with response in EUS but none have utilized mucosal mass length [18, 19]. As noted by others, assessment of TNM status by CT or EUS does not appear to correlate with pathologic response [14, 15]. This may be because these studies do not assess viability and cannot distinguish between fibrosis and viable cancer. Although FDG-PET scans can distinguish viable from nonviable tissue, false positive results can occur because metabolically active leukocytes and macrophages associated with post-CRT inflammation can lead to an elevated SUV [20, 22]. Despite this limitation, FDG-PET imaging is more accurate at identifying pathologic nonresponders (Table 3) when compared with the other modalities.
Several authors have suggested that two serial FDG-PET or EUS studies are needed to predict outcome because this allows the percent decrease relative to the baseline to be determined [11–13, 18, 19, 23, 24]. Our study suggests, however, that a single post-CRT PET, EUS or CT scan may be sufficient to differentiate pathologic responders from nonresponders. This observation requires further analysis in a prospective study since the threshold values in our study were determined in a retrospective fashion based on analyzed data. Our findings also suggest that post-CRT evaluation may be applicable to a broad range of patients treated with a variety of CRT regimens since our study evaluated patients treated both on and off-protocol with concurrent chemoradiation alone or induction chemotherapy followed by concurrent chemoradiation. In this regard, the timing of the imaging may be more important than the type of CRT so that the impact of post-CRT inflammation and tumor size remains a constant.
Another important observation was that only FDG-PET imaging was able to predict both the responses to preoperative CRT and poor prognosis (Figs 1–3, Tables 4 and 5). In our study patients who had a post-CRT FDG-PET SUV of equal to or greater than 4 had significantly worse 2-year survival than did those with an SUV of less than 4 (34% vs 64%, p = 0.01). The multivariable observation that CT scan esophageal thickness also correlated with survival (Table 5) may be a statistical abnormality since neither the univariate analysis nor the Kaplan-Meier evaluation revealed a CT scan esophageal thickness correlation with long-term outcome (Fig 3, Table 4). In fact, post-CRT FDG-PET SUV was the only preoperative factor we evaluated that could predict survival except histology in a univariate fashion (Table 4). Other smaller studies in esophageal cancer have produced similar preliminary findings [11–13]. Because no other imaging modality can accurately predict prognosis before surgical resection, the importance of these observations cannot be emphasized enough. In this regard we have recently observed that many patients who receive induction chemotherapy before concurrent chemoradiation appear to have a higher pathologic response and a better prognosis [16]. Accordingly, if FDG-PET imaging could reliably identify CRT response then multimodality therapy could be tailored to individual patients to minimize treatment-related morbidity while maximizing therapeutic benefit. Recently it has been reported that PET imaging can predict pathologic response two weeks after initiating therapy [23–25]. This would be clinically useful as changes in induction therapy could be initiated before the completion of radiation therapy although this would have to be balanced by the increased toxicity of additional treatment. Additionally, if these observations are borne out in future trials then therapeutic strategies incorporating multiple regimens could be utilized based on early FDG-PET response.
A third important observation of this study is that imaging with FDG-PET, CT, and EUS is unable to confirm the absence of residual viable disease in the primary tumor (Table 2, 3). Our study evaluated pathologic response and distinguished macroscopic residual disease (>10%, responder) from microscopic residual and complete response (0% to 10% viable, nonresponder). We observed that the accuracy decreased dramatically when an attempt is made to distinguish microscopic residual disease (1% to 10% viable) from a complete (0% viable) pathologic response (data not shown). The clinical implication of these observations is that there is currently no imaging modality that can confirm a complete response after preoperative CRT. Consequently, patients with an apparent complete response after CRT can have residual disease and should not be precluded from additional therapeutic management.
In summary, our study is a retrospective study but suggests that post-CRT FDG-PET imaging may be useful for identifying a subset of esophageal cancer patients who have failed to respond to CRT and whose prognosis is poor. These results need to be confirmed in a prospective multi-institutional setting but preliminary findings suggest that no modality not even FDG-PET can rule out the presence of residual microscopic disease after CRT. Therefore, esophagectomy should remain a therapeutic option even when the post-CRT imaging modalities are normal. [21]
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Discussion |
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My question for you is regarding your summary, but really what you haven't told us, which is your conclusion. Your institution recently has advocated doing only salvage esophagectomy for patients after chemoradiation. I wonder if you are now accepting that not only is path CR, complete path CR going to be the predictor for best long-term prognosis, but even basically partial response is a predictor for long-term prognosis. Does this mean now that you are going to go back and do more esophagectomies on patients postchemorad, or do you still believe in this concept of salvage esophagectomy?
DR SWISHER: Thank you, Dr Krasna. You brought up some very interesting points. Our institution does not put forward the concept that we should proceed with salvage esophagectomy after chemoradiation as first line therapy. We still think that this is something that needs to be tested. At our institution, if patients are in good physiologic condition and have locoregionally advanced esophageal cancer, we typically treat them with preoperative chemoradiation and surgery. Having said that, we had hoped very much that the PET scan might be able to pick out those people who had a complete pathologic response without viable tumor who might be candidates to avoid surgery in. Unfortunately, the PET scan is not able to rule out microscopic residual and is not, therefore, going to be able to definitively tell you that there is no viable cancer without surgical resection.
DR THOMAS A. D'AMICO (Durham, NC): Dr Swisher, this is an excellent study. I have a couple of questions on the use of the PET. First of all, have you looked at the pretreatment PET regarding survival and the predictability of whether someone would be sterilized by chemoradiation? If you look at lung cancer, the pretreatment PET actually tells you all you a great deal about relative survival. It doesn't change our decision to operate or not operate, but you get a lot of information on that pretreatment PET. Have you analyzed that?
Number two, with regard to sterilization, it has been shown that the most important aspect of sterilization is if the lymph nodes are sterilized. Now, you have carefully analyzed both the SUV (standardized uptake value) and microscopic versus complete sterilization of the primary, but do you think PET is sensitive or specific enough to look at the lymph node status only, because that appears to be more closely linked to survival.
Lastly, are you advocating restaging PET for all patients after therapy with esophagus cancer? Currently that's fundable for lung cancer patients, but in esophagus cancer, it's one patient, one PET. Do you think everybody should be able to get two PETs?
Thanks. That was a great presentation.
DR SWISHER: Thank you, Dr D'Amico. For time purposes, I did not show you all the multiple analyses that we performed, but one of them included the PET SUV of the primary and another one combined the PET SUV of the primary with the regional lymph nodes. We found that there was no added benefit to adding the SUV of the regional lymph nodes. Additionally, the pretreatment PET did not predict responders to chemoradiation only the posttreatment PET after the chemoradiation had been delivered.
We do not advocate restaging PET for all patients at this time until further data can confirm these results. In the future, it may be possible to add additional preoperative therapy if the PET SUV does not show response after initial chemoradiation.
DR FRANK C. DETTERBECK (Chapel Hill, NC): I enjoyed your presentation. We have looked at the issue of restaging as well and found that neither CT nor endoscopy and biopsy predicted who was a complete responder, in other words, in whom we could avoid surgery because they had already responded. My interpretation of what you've said is that you agree with that and furthermore that PET is also not able to predict a complete response.
The converse, though, is also of interest. You imply that a PET that is still positive predicts patients that still have tumor present, and that perhaps we should not operate on those patients or we should do something in addition. But the key issue in being able to apply this logic to an individual patient is definition of the false positive rate of a posttreatment PET scan. What is your false-positive rate for PET? In other words, if you have a positive PET, how many of those patients actually had no viable tumor at the time of resection? If this rate is low enough, then perhaps we can say that they need additional treatment, but, if not, then I'm not so sure we can. I bring this question up because this is after radiation, and, of course, radiation causes PET to be positive for a while. In addition, could you comment on what interval after finishing the radiation treatment you think the PET should be done in order to avoid that?
DR SWISHER: Thank you very much Dr Detterbeck. Those are very important points. We performed these PET scans 4 to 6 weeks after the completion of radiation therapy to try and keep consistency, but there clearly still is a false-positive from inflammation due to radiation that throws us off a little bit. The false-positive rate is about 34% when we look at this closely, and some of that is due to postchemoradiation changes such as esophagitis. These are clearly false-positives. It is interesting that there have been some recent reports from Europe in which they have performed PET scans 2 weeks after starting chemotherapy rather than after the completion of therapy and they seem to have a much lower false-positive rate. This early time point still appears to be predictive of long-term survival and pathologic response so this may be able to allow clinicians to change therapy if the patient's do not appear to be responding. The problem now is that there are few alternative treatments to try but in the future with the advent of the new biological therapies this may change.
DR JEFFREY A. HAGEN (Los Angeles, CA): I would like to follow-up Dr Detterbeck's question with a suggestion and then pose a different question.
If you have the chance to revise this manuscript, you might consider reporting the positive and negative predictive values rather than simply the sensitivity and specificity values. This would give the reader more useful information, providing a better estimate of the false-positive and false-negative rates.
My question is, since most of the literature would suggest that the benefit, if any, of chemoradiation therapy is in the group of patients who are complete responders, I wonder if you could explain the rationale behind choosing to include both complete and partial responders as the endpoint to your study?
Thanks for a nice presentation.
DR SWISHER: Thank you, Dr Hagen. We have found in our experience that there tends to be three groups of patients. There are patients who have a complete pathologic response that do the best, and their long-term survival is about 60% to 70%. There is another group with macroscopic residual (>50% viable tumor), and those do the least well and they have about a 20% long-term survival. Those patients, however, who have a microscopic residual disease (<50% viable tumor) fall somewhere in between and have about a 40% long-term survival so we tend to group the microscopic residuals and the pathologic complete responders together as responders to chemoradiation.
DR JAMES D. LUKETICH (Pittsburgh, PA): I enjoyed your study. Did you have trouble interpreting the EUS postchemoradiation? Is this why you just chose not to present the T status pretreatment and posttreatment? Since it is problematic to delineate the esophageal layers postchemoradiation, how were you measuring the lesion, the volume size? I notice you were presenting a lesion size. How were you certain the visible lesion was viable tumor and not scar tissue? And after you made those measurements, did you individually look at the pathology specimen and see how close that EUS assessment of viable tumor was indeed viable tumor? We have had a lot of trouble interpreting EUS postchemoradiation.
DR SWISHER: Thank you Dr Luketich. You bring up some very good points. We looked at a variety of different things with the EUS, and as has been previously reported the posttreatment stage by EUS following chemoradiation is not very helpful because one cannot differentiate between fibrosis and residual viable tumor. The measurement that we used was mucosal mass size which was reproducible and could be very easily reported and followed. As I mentioned before, we had been hopeful that the PET scan would be able to get over some of the problems with EUS and CT in differentiating between fibrosis and viable cancer. Unfortunately, I do not think that the PET is sensitive enough to differentiate microscopic residual disease from fibrosis since both have low PET SUV uptake. The PET SUV does appear to pick up macroscopic residual disease and this is what is allowing a survival prediction since these patients tend to do poorly.
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