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Ann Thorac Surg 2001;71:1073-1079
© 2001 The Society of Thoracic Surgeons
a Division of Thoracic Surgery, University of Maryland Medical System, Baltimore, Maryland, USA
b Division of Thoracic Surgery, CALGB/Duke University Statistical Center, Raleigh, North Carolina, USA
Address reprint requests to Dr Krasna, Division of Thoracic Surgery, University of Maryland Medical System, 22 South Greene St, Baltimore, MD 21201
e-mail: mkrasna{at}smail.umaryland.edu
Presented at the Forty-sixth Annual Meeting of the Southern Thoracic Surgical Association, San Juan, Puerto Rico, Nov 4–6, 1999.
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Abstract |
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 Top Abstract IntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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Patients and Methods. From February 1995 to September 1999, 134 patients were entered in the study. This study represents the analysis of final data on 113 patients. TS/LS was considered feasible if TS and 1 LN sampled at least 3 LN by LS; a confirmed positive node was found; or T4 or M1 disease was documented. If this was accomplished in more than 70% of patients, TS/LS was believed to be feasible.
Results. The LN stations most frequently sampled in the thorax (134 patients) were levels 2 (33%), 3 (38%), 4 (40%), 7 (76%), 8 (69%), 9 (55%), and 10 (43%) and in the abdomen levels 17 (70%) and 20 (55%). The frequency of positive LN by level were as follows: 2 (10%), 3 (8%), 4 (10%), 7 (10%), 8 (25%), 9 (10%), 10 (10%), 17 (34%), and 20 (27%). Noninvasive tests (computed tomographic scan, magnetic resonance imaging, esophageal ultrasound scan) each incorrectly identified TN staging as noted by missed positive or false-negative LN or metastatic disease found at TS/LS staging in 50%, 40%, and 30% of patients, respectively. Median operating time was 210 minutes (range, 40 to 865 minutes). Median postoperative hospital stay was 3 days (range, 1 to 35 days). There were no deaths or major complications. Seventy-three percent of patients met the definition for feasibility. In 30 patients TS was not feasible. Positive LN disease was found in 43 patients; 32 were deemed N0. Ten patients had T4/M1 disease. Of the 32 potentially resectable N0 patients, 14 patients had preoperative induction therapy; 13 patients went directly to operation with N0 confirmed in 9 patients, NX in 1 and N1 in 3. Three patients were unresectable, 1 patient died, and 1 was lost to follow-up.
Conclusions. In summary, the feasibility of TS/LS was confirmed. It doubled the number of positive LNs identified by conventional, noninvasive staging. The overall accuracy remains to be defined by analysis of the LN negative group in follow-up. Although the positive predictive value was high, further study is warranted to confirm the role of TS/LS in the staging algorithm of esophageal cancer.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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CALGB 9380 was a prospective, multiinstitutional, National Cancer Institute-funded phase II trial to study the feasibility of minimally invasive surgical staging for esophageal cancer. The primary objective of this study was to evaluate the feasibility of preoperative staging using thoracoscopy/laparoscopy for esophageal cancer. A secondary goal was to assess the accuracy of lymph node (LN) staging by thoracoscopy/laparoscopy (TS/LS) through comparison to final resection pathologic staging. It was also planned to assess the benefit of TS/LS when added to clinical staging and compare the efficacy of noninvasive to minimally invasive techniques. Finally, data were collected regarding the costs of TS/LS LN staging and the possible savings of avoiding unnecessary esophagectomy. This is a preliminary report of the results of that study.
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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Informed consent
Each patient was aware of the neoplastic nature of his or her disease process and willingly consented after being informed of the investigational procedure to be undertaken, alternatives, potential benefits, side effects, risks, and discomforts. The human protection committee at each institution approved this protocol.
Technique
The technique of TS/LS LN has been described elsewhere in detail [5]. Briefly, a right thoracoscopy was done unless otherwise indicated by CT scan or EUS. Thoracoscopy yielded individually sampled and labeled biopsies at designated nodal stations according to a standard LN map (Fig 2).
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If laparoscopy was not technically feasible due to adhesions, a minilaparotomy was performed with an incision less than 8 cm. Laparoscopy and biopsy of abdominal LN and celiac axis LNs was required for all tumors. In the supine or modified lithotomy position the patient was prepared for a standard laparotomy. The procedure was performed with three/four ports. An angled laparoscope (30 degrees or greater) or operating scope was used for exposure of the operative field. After thorough exploration of the peritoneal cavity the surface of the liver was inspected and gross lesions were biopsied and sent for frozen section. The lesser curvature of the stomach was inspected for evidence of LNs and the lesser sac entered using sharp dissection through the lesser omentum, just to the right of the esophagus. Exposure of the celiac axis was obtained by elevation of the lesser curve of the stomach near the gastroesophageal junction. The left gastric artery was identified as it projects straight up from the celiac axis and enters the posterior wall of the stomach. The fat and areolar tissue containing LNs at the origin of the celiac axis was dissected and the nodes were harvested.
Esophagectomy
Surgeons were strongly urged to refer patients who were LN negative by TS/LS LN directly to surgical resection. Patients with positive LNs were treated as per the surgeon’s preference. Extent and approach of surgical resection was dictated by location of primary tumor at time of diagnosis. Upper thoracic esophageal cancers (20 to 24 cm) were resected using combined abdomen, chest, and neck incisions. Midesophageal and gastroesophageal junction cancers (> 24 cm) were approached through a left or right chest and abdomen; or right chest, abdomen, and neck approach. Transhiatal esophagectomy with celiac lymphadenectomy was acceptable only for lesions below 34 cm. For the purpose of this protocol, transhiatal esophagectomy was discouraged to optimize pathologic staging and LN dissection. Staging lymphadenectomy was required for all resections. At a minimum, 3 thoracic and 1 abdominal node were examined at the time of exploration.
Statistics
Feasibility was defined as successful TS/LS LN sampling in more than 70% of patients. Surgical staging in each patient was considered feasible (ie, successful) if one of the following held true: (1) at least 3 LNs are sampled by thoracoscopy and at least 1 LN sampled by laparoscopy; (2) a single positive LN was found that was confirmed by frozen section (gross surgical impression was not sufficient); (3) disease was proven unresectable due to either T4 tumor or metastatic disease; and (4) no major complications occurred (defined as morbidity or mortality occurring within 30 days of the staging procedure).
Based on 25 patients per year entering this trial, it was expected that accrual would be complete between 3 and 4 years from activation. In fact, although the study was activated in February 1995, it was not fully funded until October 1997 and not opened to the Eastern Cooperative Oncology Group (ECOG) until February 1998. The average accrual over the last 2 years was 2 to 4 patients per month.
Sample size
The multiple testing procedure proposed by Fleming [6] was used with three stages and a total sample size of 98 patients. Patients were entered in groups of 30, 30, and 38. This procedure would allow for early closure after 30 or 60 patients were entered onto the trial if the preoperative staging procedure, TS/LS, did not seem feasible. To increase the number of LN negative patients going directly to operation, the total number was increased to 134 patients after a preliminary analysis.
When assessing the results of TS/LS LN staging, this technique was compared to the highest, best noninvasive clinical stage that was recorded prospectively by noninvasive testing before the procedure.
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Results |
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TopAbstractIntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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Sixty-nine percent of patients had adenocarcinomas and 31% had squamous cell cancer. There were 110 men and 24 women; 81% of the patients were white and 19% were African-American or Hispanic. The median age was 62 years (range, 38 to 85 years). As of this writing, 107 eligible patients had sufficient information to be available for feasibility testing. Median operating room time was 210.5 minutes (range, 40 to 865 minutes). Median postoperative hospital stay was 3 days (range, 1 to 35 days). The mean duration of chest tube drainage was 1 day (range, 0 to 18 days). The mean number of disposable instruments used was 2 per patient (range, 0 to 37). There were no deaths or major complications.
Seventy-seven of the 107 evaluable patients met the definition for feasibility (73%; 95% confidence interval = 0.63–0.84). In 30 patients TS was not feasible. The LN stations most frequently sampled in the thorax in these patients were level 2 (33%), 3 (38%), 4 (40%), 7 (76%), 8 (69%), 9 (55%), and 10 (43%), and in the abdomen levels 17 (70%) and 20 (55%). Positive LNs were found in 56% of patients. T4 tumors invading the aorta or airway were noted in 8 patients. Two patients had M1 disease found at LS and no further LN staging was done. Forty-two percent of patients were LN negative. Positive LNs were found in 10% of level 2, 8% level 3, 10% level 4, 10% level 7, 25% level 8, 10% level 9, 10% level 10, 34% level 17, and 27% in level 20. Noninvasive tests (CT, MRI, and EUS) failed to detect positive LN identified by TS/LS in 16 patients. Esophageal ultrasound scan was performed in 57 patients. It was false-negative in 9 patients and false-positive in 10. Of the 32 potentially resectable N0 patients, 14 patients had preoperative induction therapy; 13 patients went directly to operation with N0 confirmed in 9, NX in 1 and N1 in 3. Three patients were unresectable, 1 patient died before curative resection, and 1 was lost to follow-up.
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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Limited literature on the diagnostic value of MRI in esophageal carcinoma has shown no significant benefit of MRI over CT. The MRI has been helpful in differentiating benign from malignant lesions in the liver. A 1994 report by Templeton and Krasna [12], using gadolinium-enhanced MRI for esophageal cancer, showed no advantage over standard MRI or CT. Therefore, we have stopped using MRI routinely for staging of esophageal cancer.
Esophageal ultrasonography is a relatively new tool used for staging and is highly accurate in detecting the depth of tumor invasion [13]. It allows for superb imaging of the layers of the gastrointestinal tract, as well as of the chest and abdominal structures [14]. However, it is not sensitive in the overall detection of extraesophageal metastasis. It has likewise been difficult to distinguish large inflammatory LNs from metastatic disease. In expert hands, the accuracy of EUS for node status has been reported to be 84% to 88%, although EUS fails in a significant number of patients secondary to obstruction [15, 16]. Rice and colleagues [17] recently reported that the most important determinant of LN spread in esophageal cancer is the T stage and that obstruction preventing successful EUS is a poor prognosticator.
Pathologic staging of esophageal cancer is the most accurate method of stratifying patients by prognostic groups. Murray and coworkers [18] described routine preresection staging of esophageal cancer patients using mediastinoscopy and minilaparotomy. Five of 30 patients had LN metastases found at mediastinoscopy and 16 of 30 had positive LNs found at minilaparotomy. Lack of access to the thoracic LNs was the limiting factor to the efficacy of preoperative staging in this series.
Thoracoscopy has proven to be a useful means of staging mediastinal LNs [19], complementing mediastinoscopy. An early report by Krasna and McLaughlin [20] described the possible efficacy of thoracoscopic LN staging in esophageal cancer. Despite correct thoracic LN staging in 14 patients, 2 had celiac LNs found at the time of esophageal resection. Had laparoscopy been performed, these 2 patients would have been staged correctly. Laparoscopy has been used successfully to evaluate esophageal cancer patients for the presence of celiac LN or liver metastases [5, 21]. By combining thoracoscopy and laparoscopy/minilaparotomy, excellent surgical staging may be achieved using minimally invasive methods [22].
A recent report showed that TS/LS LN staging provided not only accurate pretreatment staging data but also tissue samples for immunohistochemical evaluation [23]. This has proven an enormous asset in allowing better prognostication of patients with esophageal cancer. Using P53 gene expression, it was shown that patients had better response to neoadjuvant therapy and improved survival times when P53 was not expressed in the pretreatment LN or primary tumors. Lesions that were P53 positive proved to have overall worse prognosis regardless of hematoxylin-eosin findings by pathology.
It was proposed in the design of this study that thoracoscopy/laparoscopy offers the potential to stage LNs in esophageal cancer as accurately as mediastinoscopy in lung cancer, thereby delineating which patients have early local disease amenable to surgical resection and which patients have advanced disease. The goal of this study was to define the feasibility, accuracy, and usefulness of thoracoscopic/laparoscopic staging in a prospective multiinstitutional trial.
TS/LS LN staging has been shown to be safe. There was no mortality and only minimal morbidity. Of note, this technique was "exported" to several centers and performed with similar efficacy. The duration of the procedure in certain patients does suggest a learning curve that should improve with experience. Although the cost analysis has yet to be done, it is intuitive that sparing a patient unnecessary surgical resection with the resultant hospitalization and morbidity/mortality will be shown to be worthwhile. Similarly, sparing a patient with early esophageal cancer, who has negative LN, from undergoing experimental trimodality therapy would also seem worthwhile. The final cost data will be reviewed when they are available.
TS/LS LN staging identified patients who had positive LN that were not found by noninvasive testing. Likewise, there were patients who were found to have T4 tumors and pulmonary metastases. Although there was a physician bias toward treating patients on neoadjuvant protocols, there were patients who underwent operation alone. These patients represent a group that will now be examined to assess the final specificity, sensitivity, and accuracy of the staging procedure. In addition, future analysis of this data may reveal the ability to predict the number of positive LN as well, in any given patient. The staging system suggested by Skinner (WNM Classification) [24] and Ellis [25] and their colleagues reemphasized the importance of the number of LN on survival. This study set out to identify any positive LN, as that constituted N1 disease on the current staging system. For example, if a patient is found to be positive, it will be possible, in the future, to further inspect the LN stations and identify whether there are greater than 5 LN.
An important group that will be analyzed in the future are those patients who had adenocarcinomas. In these patients it is generally found that celiac LN positivity occurs in more than 75% of patients. The exact role of thoracic LN staging in predicting outcome in these patients remains to be seen. With recent data regarding the finding of occult microscopic positive LN in the neck using three-field lymphadenectomy, this information may further point to radical resection or more aggressive neoadjuvant treatment for these patients. Therefore, the finding of positive LN in the chest or abdomen pretreatment in a patient who is being treated for adenocarcinoma of the distal esophagus/gastroesophageal (GE) junction has important implications.
Newer techniques for staging esophageal cancer continue to be developed. The use of positron emission tomography scan and EUS-guided needle biopsy of periesophageal LN have stressed the importance of LN staging. Recent reports of high success rates of EUS-guided fine needle aspiration (FNA) staging of esophageal cancer suggest that an even less invasive technique may be available in the future. This is simply another means of accomplishing the same goal of pathologic pretreatment in staging. The ultimate utility of this technique will depend on the number of times it is abandoned due to obstruction and the number of false negatives when sampling is successful. This modality is currently being evaluated in a prospective fashion in several institutions [26, 27]. In one possible algorithm, when EUS–FNA is positive, no TS/LS is done, and when EUS–FNA is negative, further surgical staging is undertaken. What the ultimate role will be for these modalities and TS/LS remains to be determined.
The question of the value of precise pretreatment staging is very important and begs discussion here. If the feasibility of this technique and the accuracy of TS/LS LN or other minimally invasive techniques is sufficiently high, how can this information be used? One possibility is to change the paradigm of treating all esophageal cancers with similar stage-specific treatments. New protocols should be undertaken to determine the most appropriate use of these investigational modalities. For example, those patients who are LN negative and have only T1/T2 tumors have been shown to have 60% to 75% 5-year survival in operation alone series. These patients might then be referred for operation alone as the sole treatment. On the other hand, those patients with T4/M1 disease clearly should not undergo operation but rather should receive systemic therapy or palliative treatment. Finally, for the group that has positive LN or T3 disease, entry onto a protocol for combination chemo/radiation therapy possibly followed by operation would seem appropriate. This approach will limit the morbidity both from operation and from neoadjuvant therapy to the groups in whom there is the greatest chance of benefit. New paradigms for care such as these will ultimately result in better outcomes for esophageal cancer patients by treating patients in a stage-specific manner.
In conclusion, the feasibility of TS/LS was confirmed in this multiinstitutional intergroup trial. It doubled the number of positive LNs identified by conventional noninvasive staging. This paradigm of surgically instituted trials is the first successfully completed study, as the dissolution of the Lung Cancer Study Group to evaluate a surgical technique in a prospective cancer trial. Although further studies are needed to confirm the role of TS/LS in the staging algorithm of esophageal cancer, an important conclusion is that new surgical technology can be evaluated in multiinstitutional, prospective phase II trials.
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Appendix 1. Eligibility criteria for CALGB 9380 |
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TopAbstractIntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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18 years
Required laboratory tests
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Appendix 2. CALGB thoracic surgeons |
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TopAbstractIntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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Discussion |
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TopAbstractIntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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hours average and up to 11 hours, with an in-hospital stay of 3 days. I also realize that this study was conceived 5 years ago when technology was not what it is today, however, I would quickly remind you that endoscopic ultrasound-guided fine needle aspiration (FNA) or computerized axial tomography (CAT) scan-guided FNA can identify up to 20% of patients with advanced disease. I also recall the previous presentations that say that positron emission tomography (PET) scanning can also upstage approximately 20% of patients. In fact, in reviewing your conclusions I would challenge your statement that you would use such an invasive technique as a paradigm for future surgical trials. I would suggest that you use this data to create CAT scan-guided FNA or a PET scan-guided study. Finally, I would note that during your presentation the majority of lymph nodes that you sampled were subcarinal, inferior pulmonary ligament, or celiac axis nodes, all of which are readily accessible by these other less invasive techniques.
Thank you.
DR KRASNA: Thank you very much, Jay. Let me first clarify the final sentence on the conclusion slide. It is not that this should be the paradigm for all esophageal cancer treatment. What it said was that a phase II prospective trial should be the paradigm for evaluating all new surgical technology. I think one of the problems that occurred in the first 5 years after the revolution of thoracoscopic surgery is that members of all the associations, including this one, approached the reported results with skepticism, as they were basically collections of retrospective data. To evaluate any new technology we should do it carefully, in a controlled fashion. You are right, although it takes 3 years to get a study like this up and running through the National Cancer Institute, the data are therefore all the more compelling.
In terms of your comments regarding the operating room time, one of the things that we are going to analyze is looking at duration of procedure per-surgeon over time and determine whether there was in fact a learning curve. Needless to say, some of the members of this group who performed thoracoscopy most frequently can do the operation usually under an hour and a half for both the chest and belly procedures.
I would like to spend a little time on your most important question, which is the current role of this technology and the role of other newer evolving technologies. To put it into perspective, let me also tell you what we currently do at Maryland. If a patient has a positive PET scan with esophageal cancer, which we now do routinely, and if that PET scan is compelling in that both the primary as well as multiple other sites are "hot," we will probably accept that and go ahead and do a needle biopsy of some other distant site to document positive metastatic disease. I think that the recent report by Luketich and colleagues actually emphasized that it was for metastatic disease the PET scan seems to be the most helpful.
If, on the other hand, the PET scan or an esophageal ultrasound are suspicious for an enlarged lymph node and that lymph node is accessible by an EUS-guided biopsy, then, as Dr Reed and others have shown in the past, we would first try an EUS-guided FNA, which our gastroenterologist does with us. Frankly, that is only positive 40% of the time. If we have an EUS-negative biopsy, we are not going to accept it as a negative, but will go ahead and perform a staging operation. Now that this study is completed, that will probably be the algorithm at our institution.
Finally, your unasked question is, how are we going to use this information regarding lymph nodes, however it is obtained pretreatment. I think at this point the answer is still up in the air. Having talked to many of you in the audience, I know that surgery remains the gold standard for treating esophageal cancer, and I absolutely agree that it is correct, because so far there is no compelling prospective randomized data to change that.
On the other hand, if you have up-front information of a very large tumor, like a T3 or a T4, with positive lymph nodes, that will probably allow you to allocate the patient to a neoadjuvant treatment protocol. Perhaps this information will make you feel more comfortable putting a patient with N0 disease on the randomized "ICE-T" study (Intergroup Cancer of the Esophagus Trial), which will evaluate the role of other therapy in addition to operation.
DR THOMAS A. D’AMICO (Durham, NC): Mark, I would also like to congratulate you on driving this study to completion. I think it is the first thoracoscopic study that was finished in the CALGB. I would like to ask you one particular question. In terms of looking at patients with T3 tumors, which is most of what we see as esophageal surgeons, if you look at the survival curves from Memorial, T3N0 patients have the exact same survival as T3N1 in that series. In terms of the utility of this technique in selecting T3N0 from T3N1, do you think that those curves are real? Do you think that all T3 patients are at least microscopic N1, or do you think that there is actually a difference that this particular technique could actually elicit in the future?
DR Krasna: I do not think all T3s are the same, and I think that, again, there have been a lot of good reports to document this. Dr Zwischenberger pointed out Akiyama’s data; it is somewhat older. If you look at Dr Ellis’ most recent review, I think it was the final review of 480 patients from the Lahey Clinic, all those patients had only operation. If you look at the breakdown of patients by stage, there was clearly a significant difference between all the stages. Obviously, in North America we do not see many T1N0 cancers, but I do think there are T3N0s, and those patients do fare better than the others.
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TopAbstractIntroductionPatients and methodsResultsCommentAppendix 1. Eligibility criteria...Appendix 2. CALGB thoracic...DiscussionReferences |
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