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J Thorac Cardiovasc Surg 1997;114:817-823
© 1997 Mosby, Inc.
GENERAL THORACIC SURGERY |
Received for publication May 6, 1997 revisions requested June 2, 1997; revisions received July 1, 1997 accepted for publication July 17, 1997. Address for reprints: James D. Luketich, MD, University of Pittsburgh Medical Center, 300 Kaufmann Building, 3471 Fifth Ave., Pittsburgh, PA 15213.
Abstract
Objective: Endoscopic ultrasonography is frequently used to locally stage esophageal cancer, but few studies exist to validate its accuracy for lymph node metastases. Our objective was to compare endoscopic ultrasonography with video-assisted thoracoscopic and laparoscopic staging in evaluating lymph node metastases in esophageal cancer. Methods: Twenty-six patients with potentially resectable esophageal cancer were identified by conventional imaging. Endoscopic ultrasonography was performed followed by laparoscopic and thoracoscopic staging, and locoregional staging was compared. Results: In eight patients endoscopic ultrasonography indicated N0 disease, but laparoscopy and thoracoscopy documented N1 disease in six. In five of 26 (19%) obstruction prevented endoscopic ultrasonography; three had N1 by laparoscopy and thoracoscopy. Thirteen patients had N1 disease according to endoscopic ultrasonography, and 12 of 13 (92%) had N1 disease by laparoscopy and thoracoscopy. The sensitivity and specificity of endoscopic ultrasonography for nodal evaluation were 65% and 66%, respectively. Sensitivity decreased to 44% for lymph node metastases less than 1 cm. No instances of T4 disease were found by surgical staging when endoscopic ultrasonography indicated T3 disease. Endoscopic ultrasonography revealed no distant metastases in any patient, but in four of 26 (15%) laparoscopy identified liver metastases. Conclusions: The accuracy of endoscopic ultrasonography in the diagnosis of lymph node metastases in esophageal cancer was 65% and only 44% for lymph node metastases less than 1 cm diameter. Laparoscopy and thoracoscopy improved the accuracy of staging lymph node metastases in esophageal cancer and had the advantage of evaluating the thoracic and abdominal cavities for metastases.
The incidence of adenocarcinoma of the distal esophagus in the United States is increasing at an alarming rate.
1 The prognosis remains poor with an overall 5-year survival of 5% to 10%. Randomized trials of multimodality regimens have not been uniformly successful in improving survival over that obtained with surgery alone. 2 One of the problems in the design of previous trials is that accurate pretreatment staging has not been available. Conventional imaging modalities have been shown to be inaccurate in detecting limited metastatic disease in esophageal cancer compared with minimally invasive surgical staging by video-assisted thoracoscopy (VATS) and laparoscopy (LAP). 3,4
Endoscopic ultrasonography (EUS) has been shown to accurately assess the depth of tumor penetration into the esophageal wall (T status), but accuracy in assessing lymph node metastases has been questioned. 5-7 Another limitation of EUS is that in 20% to 38% of patients with esophageal cancer a high-grade malignant stricture precludes passage of an echoendoscope. Dilation and subsequent EUS in this setting has a significant risk of perforation. 7 LAP/VATS has now been reported by several investigators as superior to conventional imaging modalities, but investigations comparing LAP/VATS and EUS for assessing lymph node metastases are limited. The objective of this study was to further investigate the accuracy of EUS and LAP/VATS in the detection of lymph node metastases in patients with esophageal cancer.
Methods
This was a prospective study of consecutive patients evaluated at the Pittsburgh Cancer Institute for potentially resectable esophageal cancer between July 1, 1995, and December 1, 1997. Resectability was determined by the Thoracic Surgery Service on the basis of conventional staging, which included computed tomography of the chest, abdomen, and head and bone scan. Patients with limited locoregional disease and no distant metastases were included. Patients with multiple enlarged lymph nodes with obliteration of normal tissue planes, considered too extensive for complete resection, or those with distant metastases by conventional scanning were excluded. EUS was performed on an outpatient basis. VATS/LAP staging was performed within 1 week of EUS.
EUS.
EUS was performed with the use of the linear electronic array 5/7.5 MHz ultrasonic endoscope (FG-32 UA Echo Endoscope, Pentax Precision Instruments, Orangeburg, N.Y.). Patients were placed in the left lateral decubitus position. Meperidine (INN: pethidine) and midazolam were used to induce conscious sedation and a topical anesthetic (Cetacaine) was used for local anesthesia of the oropharynx. The echoendoscopic probe was then placed in the esophagus. The ultrasonic balloon was filled with water and 7.5 MHz frequency delivered. The entire length of the esophagus was evaluated sonographically to assess lymph nodes in the periesophageal, celiac, and gastrohepatic regions. The tumor was also examined carefully to determine layer of origin, degree of esophageal wall invasion, and relationship to adjacent structures. Classification of tumor stage by EUS was based on the TNM staging classification. 8 Depth of tumor penetration (T status) was assigned by the same gastroenterologist (R.K.) who performed the EUS in all cases as follows: T1, wall thickening involving only mucosa and submucosa; T2, tumor infiltration into muscularis propria, with a smooth outer margin; T3, tumor infiltration through muscularis propria, with an irregular outer margin; T4, tumor invasion of periesophageal tissue or adjacent organs. Lymph nodes were considered "positive" if they fulfilled one or more of the following criteria: distinct borders, rounded appearance, hypoechogenicity, and size larger than 1 cm.
Minimally invasive staging (LAP/VATS).
At the time of LAP and VATS, bronchoscopic and esophagogastoduodenoscopic examinations were also performed. In addition, all patients also had placement of a double-lumen Infuse-A-Port device (Strato/Infusaid, Norwood, Mass.) for chemotherapy.
LAP staging was performed first with the patient in the supine position. Five access ports were used. Two 10 mm ports were placed just to the right and left of the midline midway between the umbilicus and the xiphoid process. The port to the left of the midline was used for the telescope and the one to the right was used for dissecting instruments. Two additional 5 mm ports were placed along the right costal margin, the lower right port being used for liver retraction and the upper for dissection (Fig. 1) One additional 5 mm port was placed along the left costal margin for the assistant to provide countertraction. Initially a visual inspection was performed to rule out intraabdominal metastases. Next, the gastrohepatic ligament was opened and lymph nodes were dissected. This dissection was extended into the periesophageal and retroesophageal planes until either a diseased (positive) lymph node was detected by frozen section analysis or several benign lymph nodes were histologically verified. Once a positive intraabdominal node was verified by frozen section analysis we proceeded to VATS analysis.
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Results
Twenty-six patients with potentially resectable esophageal cancer were identified during the study period. Adenocarcinoma of the gastroesophageal junction was present in 24 patients. Two patients had squamous cell carcinoma of the esophagus located 25 to 30 cm from the incisors. EUS was possible in 21 patients. In five (19%), a high-grade malignant stricture prevented passage of the echoendoscope. In three of these, LAP/VATS documented N1 disease. In no cases did LAP/VATS identify a T4 lesion when T3 was diagnosed by EUS.
LAP/VATS documented lymph node metastases in 21 of 26 patients (81%). Of the 21 patients in whom EUS was technically possible, N1 status was assigned in 12 (62%) but LAP/VATS results were positive in 18 (86%). In 13 patients, N1 disease was diagnosed by EUS and was confirmed by LAP/VATS in 12 of the 13 (92%). In eight patients, EUS indicated stage N0 but LAP/VATS showed lymph node metastases in six. Compared with LAP/VATS for detecting lymph node metastases, EUS had a sensitivity of 65%, a specificity of 66%, and an accuracy of 65%. In all six cases in which EUS indicated stage N0 and LAP/VATS stage N1, the lymph nodes were less than 1 cm in diameter (range 0.2 to 1.0 cm).
EUS did not detect metastatic disease in any case. In four of 26 cases, LAP/VATS identified small liver metastases. In three of these, the metastasis was in the left lobe of the liver and was less than 0.5 cm in diameter (Fig. 3).
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Table I). The only major complication occurring after LAP was a small bowel obstruction on postoperative day 3; this occurred as a result of a herniated loop of small bowel at a 10 mm port site. The hernia was reduced and repaired with no sequelae. The average operative time for LAP/VATS staging was 4.2 hours (range 1 to 6 hours). The average length of hospital stay was 3.4 days (range 1 to 11 days). The operative time and hospital stay decreased during the course of the study (Table II).
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Currently, no single noninvasive imaging modality or invasive procedure is an ideal staging method for esophageal cancer. An ideal modality should accurately assess for locoregional and distant metastases and should limit costs. Computed tomography has recently been shown to be inaccurate in up to 40% of cases when followed by LAP and VATS. 3,4 However, LAP and VATS are associated with minor morbidity and significant cost. Positron emission tomography has been shown by our group to demonstrate distant metastases in 20% of cases in which results of computed tomography and bone scanning were negative, but it shows only a 45% sensitivity for lymph node metastases that are less than 1 cm in diameter. 4 EUS offers the advantage of less cost than minimally invasive surgical staging, but its accuracy in detecting lymph node metastases has been questioned. 5-7
In the current study, we demonstrated that the accuracy of EUS was only 65% compared with minimally invasive surgical staging. The overall incidence of lymph node metastases when staged by LAP and VATS was 81%, which agrees with the results from pathologic analysis of radical esophagectomy studies reported elsewhere in similar populations of patients. 9-11 This similarity suggests that our lymph node sampling at the time of minimally invasive surgical staging was adequate. The operative times and associated cost for minimally invasive staging limits routine clinical application outside of protocol settings. However, these operative times included bronchoscopy, esophagoscopy, and placement of an Infuse-A-Port device. In addition, we also included the time required for placement of a double-lumen endotracheal tube and repositioning. The actual time for LAP and VATS was less than 1 hour for each procedure in our last 10 cases. The time required to perform minimally invasive surgical staging decreased significantly as experience increased (
Table II). A prospective cost analysis was not performed, but average total charges for EUS are between $2,000 and $2,500 compared with $20,000 and $25,000 for total charges for a 1- to 2-day hospital stay for VATS/LAP staging. In our series, 24 of 26 patients had an adenocarcinoma located at or near the gastroesophageal junction. The relevance of the findings of the current study to tumors at different locations or different cell types is not known. It is possible that thoracoscopic staging could be omitted in most cases of gastroesophageal junction adenocarcinomas inasmuch as we found only three cases of 26 in which LAP was negative for both lymph node metastases and distant metastases and VATS was positive for lymph node metastases. However, in cases of a negative LAP exploration of the abdomen, VATS should be performed to assure accurate staging.
We are currently investigating the role of fine needle aspiration of lymph nodes at the time of EUS. If N1 disease can be histologically verified by EUS, a much less extensive surgical staging procedure would be required. In the setting of documented lymph node metastases, presumably the only role for LAP or VATS would be to rule out distant metastases missed by conventional staging, although some investigators have shown that documenting the mere presence of N1 disease is not adequate to accurately assess prognosis. For example, the number of lymph nodes involved 9-11 and their location above and below the diaphragm 12 may be important prognostic factors. For adenocarcinomas of the gastroesophageal junction, we found no cases of intrathoracic distant metastases missed by conventional scanning but did identify four cases of occult liver metastases. Confirmation by larger prospective studies will be required to determine the role of VATS in this setting.
In conclusion, current criteria for defining lymph node metastases by EUS in the setting of esophageal cancer are inaccurate. We use EUS as a complimentary diagnostic procedure that accurately assesses tumor depth of penetration and in some cases allows tissue diagnosis by fine needle aspiration. For accurate assessment of lymph node metastases and to rule out occult metastases in the patient with esophageal cancer, histologic verification is required in most cases by minimally invasive surgical staging.
Appendix: Discussion
Dr. Thomas W. Rice (Cleveland, Ohio).
Esophageal carcinoma is no longer a single entity with a uniformly dismal prognosis. Early-stage cancers can be detected because of the epidemic of adenocarcinoma in middle-aged and elderly white men, a growing appreciation of the malignant potential of Barrett's esophagus, and the increasing use of surveillance endoscopy. The spectrum of the disease is now obvious. In the selection of surgical candidates, pretreatment staging is crucial and allows modification of therapy for locally advanced tumors.
EUS is a superb staging tool. We have used endosonography in staging the disease of our patients for the past decade. The goal of clinical staging is to identify T3 and N1 disease, because patients with this stage of disease have a poor surgical survival. Esophageal endosonography is the best clinical instrument for the evaluation of T stage. If T3 or T4 disease is found, the patient has locally advanced disease, and identification of N1 disease is an added luxury but not essential for treatment.
The confirmation of N1 disease becomes critical when it affects treatment and survival. An accuracy of 80% or greater in the determination of regional lymph node status is reported by most centers with an extensive experience with EUS.
The following practical lessons have improved the endosonographic detection of N1 disease in our practice: (1) The instrument you chose, a sector scanner, is better suited for diagnosis than staging. (2) A dedicated endosonographer should perform all studies with pathologic verification of clinical staging when possible. It takes at least 50 to 100 examinations to become competent in technique and interpretation of EUS. A malignant stricture, which you found, as we did, precludes EUS in 20% of patients, is the most accurate predictor of advanced disease. Ninety percent of patients in whom the scope cannot be advanced will have stage III or IV disease. Another accurate predictor of N1 disease is the proximity of the regional node to the tumor. The relationship of T to N1 is helpful because 80% of patients with T3 and T4 disease have N1 disease. The comparison of the echo characteristics of the tumor and the node is most useful, and the standard criteria of a malignant node, size, shape, border, and internal echo patterns augment this list. Finally, in the assessment of the indeterminate node, EUS-directed fine needle aspiration further refines clinical staging by adding tissue sampling to these EUS findings.
In our patients EUS is an outpatient procedure that adds 10 to 20 minutes to endoscopic examination of the upper gastrointestinal tract, and the patient is charged $1000. This must be compared with the combination of LAP and VATS, which requires hospitalization, a general anesthetic, a 4- to 5-hour operation, and an average stay of 3 days, with the potential of an 11-day stay. Some of these statistics are equivalent to those of esophagectomy.
This procedure also potentially violates the tumor and requires dissection of the vascular supply of the stomach. The effects on future resection and reconstruction are unknown.
We rely on EUS for clinical staging and use VATS and LAP as adjuncts to answer specific questions not addressed by noninvasive staging techniques.
Dr. Luketich.
Thank you, Dr. Rice, for your comments. As I mentioned, we do share the concern over cost. One of the biggest advantages of LAP and VATS is that it allows the physician to evaluate for distant metastatic disease, which we found in between 15% and 20% of cases, which avoids the major morbidity and cost of esophagectomy.
Regarding the accuracy of EUS, for T2 N0 cases, when results of EUS have been negative we have found positive lymph nodes in six of our eight cases. However, I think that you are right for T3, bulky tumors. Most of those patients are going to have N1 disease, and in some studies this has been confirmed by surgical follow-up. However, EUS findings have not been well documented by lymph node mapping in most series but simply confirmed as "N," after surgical resection. I know you would agree that I could arbitrarily stage most bulky T3 tumors as N1 and I would probably be right in about 80% of cases. I am not sure that most physicians can use EUS to specifically identify metastatic nodes; they may just be seeing nodes and calling them positive. Lymph node mapping and further studies need to be done to determine whether EUS can identify the extent and location of metastatic lymph nodes that may be important prognostically.
We are ready to start up a new trial working with our endoscopist. We are doing intraoperative EUS: When a lymph node appears positive by EUS, it is injected with methylene blue and surgically dissected to more closely evaluate EUS and its accuracy. Clearly from a cost standpoint, EUS is attractive and it is unparalleled in its ability to assess T status. Our goal is to more closely evaluate EUS accuracy for lymph node metastasis and not to exclude EUS from our practice.
Dr. Nasser K. Altorki (New York, N.Y.).
You have made a powerful case against EUS, at least for detection of nodal metastases. I am not sure your case is quite as persuasive for staging of minimally invasive disease. We have stopped using EUS to evaluate nodal metastases. We use it primarily to evaluate the T status. We examined the correlation between T status and what we found at operation. If the lesion is stage T2, the prevalence of positive nodes is 50%. If the lesion is stage T3, whether it is constricting or not, the prevalence of positive nodes goes up to 80%. Therefore, if the lesion is not stage T1, we consider that the probability of nodal metastases is very high. Have you made any correlation between the T status and the prevalence of nodal disease?
Dr. Luketich.
We made a very similar observation. Our concern is, of course, looking at those lesions that are stage N0 by EUS, which have a high likelihood or at least a potential for periesophageal lymph node metastasis and might be stratified to pretreatment chemotherapy. Inasmuch as neoadjuvant therapy has not been proven in most studies to add any benefit to surgical resection, we think it is important to definitively stage the disease before multimodality treatment protocols. For bulky T3 tumors, you can make an argument for going right ahead with your treatment strategies. However, because of our disappointment over recent multimodality results, if minimally invasive staging changes the stage of T3 or T2 tumors or identifies radiographically occult metastases in even 20% of patients, this may help us to more closely evaluate response rates, downstaging, and the impact of multimodality therapy on subsets of patients. As EUS develops in terms of the fine-needle aspiration capability, histologic verification would allow accurate staging before randomizing patients to different treatment regimens. This still does not address radiographically occult metastases, which have been reported in about 20% of series that include minimally invasive surgical staging.
Dr. Mark J. Krasna (Baltimore, Md.).
I think the reason your operating room times were twice as long as mine is that you are very meticulous and are getting more lymph nodes. This discussion on lymph node spread is probably very good. Whether EUS, VATS, LAP, or en bloc esophagectomy with two or three fields is used, I think finally people are getting the message, that we can prognosticate esophageal cancer by simply proving whether or not lymph nodes are involved. That is a lesson that was taught to me by Dr. Ellis years ago, and we have been proving it true ever since. Unfortunately, as you said, this matter will not be clear in time for the next intergroup trial, and that trial probably will lump together all patients and all stages of esophageal cancer; however, ideally it will at least stratify up front by the different stages. I do think, though, that in the future we will be able to tell, whether by EUS or VATS or LAP, whether the lymph nodes are involved or not, and make the decision on that basis for a radical resection versus perhaps multimodality therapy.
In your abstract, you listed a number of patients who had positive lymph nodes overall. Can you break down how many of those positive nodes were abdominal lymph nodes versus thoracic lymph nodes? Also, do you know how many patients eventually went on to resection?
Dr. Luketich.
Thank you, Dr. Krasna. Of the 21 patients who could undergo EUS, approximately 40% had positive lymph nodes according to LAP and VATS, another 40% had LAP-positive nodes only, with VATS results being negative, and only a small number in our series, 20%, had LAP-negative results with VATS then identifying a small metastatic periesophageal lymph node.
Dr. Malcolm M. DeCamp, Jr. (Boston, Mass.).
As someone who is doing this myself, I am always perplexed at when to decide that the diagnosis is "negative." Could you comment on those patients with small nodes, those patients in whom your suspicion is low clinically? How much dissection you do and how many nodes do you sample before you decide that the stage is N0 and quit?
Dr. Luketich.
I think that is why the range of time is variable. When we go into the abdomen and we find a gastrohepatic node that is easily dissectable, it is a 30-minute procedure. However, when that gastrohepatic node is histologically negative, we continue to dissect out nodes. Early on in our experience we were not meticulous enough, and even minor bleeding makes lymph node identification difficult. A bloodless field is essential for retroesophageal and celiac nodal identification. That is a challenge laparoscopically and takes more time. The more cases I do, the more reluctant I am to leave the abdomen with a gastroesophageal junction tumor that is at the T3 level and call it N0. I cannot specify a time. However, we certainly dissect nodes at the gastrohepatic ligament as well as periesophageal, retroesophageal, and celiac nodes before we will decide that it is a laparoscopically negative case.
At VATS, we mobilize the distal esophagus and take out periesophageal nodes. I have personally found that to be most rewarding in terms of dissection. Black anthracotic nodes are not of much help, because they are easy to get out but they often do not have the metastatic deposit. You can take out the subcarinal and the infrapulmonary ligament lymph nodes because they are easy to resect, but they are usually negative in our experience. For the gastroesophageal junction tumors, to get a positive node in the chest it is necessary to resect a periesophageal node, and that requires opening the pleura. As Dr. Rice mentioned, opening the pleura may be disadvantageous. In our more recent patients, we have tried to stay linear with the pleural opening and close it with an endoscopic suture.
We have found that after minimally invasive staging and multimodality therapy, resection at a later date is a more difficult dissection.
Footnotes
Read at the Seventy-seventh Annual Meeting of The American Association for Thoracic Surgery, Washington, D.C., May 4-7, 1997. 
References
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