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Ann Thorac Surg 2004;78:1777-1782
© 2004 The Society of Thoracic Surgeons

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Original article: general thoracic

Endoscopic Mucosal Resection as a Staging Technique to Determine the Depth of Invasion of Esophageal Adenocarcinoma

^a Department of Surgery, The University of Southern California, Keck School of Medicine, Los Angeles, California, USA
^b Department of Cardiothoracic Surgery, The University of Southern California, Keck School of Medicine, Los Angeles, California, USA

Accepted for publication April 20, 2004.

^* Address reprint requests to Dr DeMeester, 1510 San Pablo St, Suite 514, Los Angeles, CA, USA 90033
sdemeester{at}surgery.usc.edu

Presented at the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.

	Abstract

Top Abstract Introduction Material and Methods Results Comment DISCUSSION References

 
BACKGROUND: Endoscopic ablation and vagal-sparing esophagectomy offer the potential for reduced morbidity in patients with high-grade dysplasia or early esophageal adenocarcinoma, but neither includes a lymphadenectomy. Although adequate for intramucosal tumors, both are potentially inadequate for patients with submucosal tumor invasion given the high prevalence of nodal metastases with these lesions. Currently there is no test including endoscopic ultrasound that can accurately determine whether a small tumor is confined to the mucosa or has penetrated into the submucosa. The aim of this study was to compare the pathologic depth of invasion by endoscopic mucosal resection with findings and outcome after surgical resection to assess the accuracy and reliability of endoscopic mucosal resection for staging early esophageal adenocarcinoma.

METHODS: From 2001 to 2003, 7 patients presented with small, endoscopically visible adenocarcinomas. All underwent endoscopic mucosal resection followed by surgical resection.

RESULTS: Analysis of the resected specimens confirmed that the endoscopic mucosal resection had accurately determined the depth of tumor invasion in all patients, and had completely excised the lesion in all but 1 patient (86%). Lymph node dissection was included as part of the resection in 2 patients with submucosal invasion by endoscopic mucosal resection, and a vagal-sparing esophagectomy was used in the 5 patients with only intramucosal tumors. All patients are alive and disease-free at a median follow-up of 7 months.

CONCLUSIONS: Endoscopic mucosal resection accurately determines the depth of tumor invasion, and should be used as a staging procedure in patients with early esophageal cancer when therapies that do not include a lymphadenectomy are considered.

	Introduction

Top Abstract Introduction Material and Methods Results Comment DISCUSSION References

 
The incidence of adenocarcinoma of the esophagus is increasing at a dramatic rate, and this previously uncommon tumor has recently surpassed squamous cell to become the most common esophageal cancer in many Western countries [1]. Adenocarcinoma develops from a precursor lesion, Barrett's esophagus, and surveillance programs are identifying an increasing number of patients with high-grade dysplasia or intramucosal adenocarcinoma. Although esophagectomy is curative for these lesions, the associated morbidity and mortality discourage physician and patient acceptance of the procedure.

To minimize the potential morbidity of an esophagectomy we have increasingly used a vagal-sparing technique in selected patients. Because vagal preservation precludes a lymphadenectomy, this procedure has been restricted to patients with little or no chance of lymph node metastases such as those with benign disease or Barrett's with high-grade dysplasia. Expansion of a vagal-sparing technique to patients with a biopsy-proven adenocarcinoma raises the concern that potentially involved lymph nodes could be left behind. The likelihood of lymph node metastases has been shown to correlate with the depth of tumor invasion into the wall of the esophagus [2]. Whereas intramucosal tumors rarely have lymph node metastases, tumors that penetrate beyond the muscularis mucosa into the submucosa have a high likelihood of nodal involvement, and a vagal-sparing procedure is potentially inadequate in these patients.

Precise determination of the depth of tumor invasion is therefore critical to select the appropriate procedure, but no current nonresectional technique including endoscopic ultrasound (EUS) is able to reliably differentiate intramucosal from submucosal lesions. Endoscopic mucosal resection (EMR) excises a disc of esophageal wall down to the muscularis propria and provides a specimen for histologic review that includes both mucosa and submucosa. Using this technique small esophageal lesions can be excised and the depth of tumor invasion pathologically determined. The aim of this study was to compare the depth of invasion determined by EMR with findings and outcome after surgical resection to allow assessment of the accuracy and reliability of this approach for staging early esophageal adenocarcinoma.

	Material and Methods

Top Abstract Introduction Material and Methods Results Comment DISCUSSION References

 
This study is a retrospective review of 7 patients who presented to a single surgeon (S.R.D.) at the University of Southern California from 2001 to 2003 with a small (<1.5 cm) visible lesion and a biopsy showing adenocarcinoma. Patients presenting during the same period with only high-grade dysplasia (n = 1), a biopsy positive for adenocarcinoma with no endoscopically identifiable lesion (n = 1), or an adenocarcinoma 1.5 cm or greater in size (n = 25) were excluded. In addition, patients who underwent an EMR but no subsequent resection (n = 3) were also excluded. This study was approved by the Institutional Review Board of the University of Southern California Keck School of Medicine.

Upper endoscopy with multiple biopsies was performed in all patients. Five patients underwent endoscopic ultrasound using a 7.5-MHz and 12-MHz probe. All patients underwent EMR using a standard technique with either a hard, straight 13.9-mm or a soft, oblique 18-mm Olympus cap [3, 4]. Briefly, the lesion was injected with 0.5 mL of methylene blue to aid subsequent identification, and in some cases the squamous esophageal mucosa was stained with Lugol's solution to facilitate identification of areas of columnar mucosa. Dilute epinephrine in saline was then injected circumferentially around the lesion in four quadrants (2 to 4 mL per quadrant) to elevate the mucosa and submucosa off of the muscularis propria. The appropriate Olympus cap was taped securely to the end of the endoscope and inserted into the esophagus. In an area away from the lesion, the snare wire was manipulated into position around the end of the cap. Once the wire was in position, the endoscope was advanced until the lesion to be removed was identified. The lesion was then sucked up into the cap, the snare tightened, and the suction released. Electrical cautery was applied in bursts to the snare, and when the specimen had been separated from the esophagus, it was suctioned back into the cap and the endoscope removed. Gross inspection of the specimen confirmed in all cases the presence of mucosa and submucosa and the absence of esophageal muscle. The specimen was then pinned out and fixed by the pathologist for subsequent histologic analysis. Each patient underwent EMR on only one occasion, although in several patients more than one disc of tissue was excised during the procedure to ensure that the lesion had been adequately sampled or removed. The procedures were all performed in the operating room with the patients under general anesthesia, and all patients were discharged home later that same day. Subsequently all patients underwent surgical resection.

	Results

Top Abstract Introduction Material and Methods Results Comment DISCUSSION References

 
There were 6 men and 1 woman. The median age was 69 years. All patients presented for evaluation of high-grade dysplasia or invasive adenocarcinoma. Upper endoscopy findings are shown in Table 1. Biopsies in all patients showed invasive adenocarcinoma, but at the time of endoscopy 2 patients were thought to have only high-grade dysplasia. The 5 patients with known tumors at the time of endoscopy also underwent EUS, and the depth of tumor invasion and the presence of enlarged or abnormal-appearing lymph nodes was carefully evaluated.

	Comment

Top Abstract Introduction Material and Methods Results Comment DISCUSSION References

 
The management of early stage esophageal cancer is evolving. Increasingly less-invasive techniques that promise decreased morbidity and mortality are being advocated, including endoscopic therapies. Efforts to reduce morbidity and make the option of esophagectomy more appealing to patients have prompted the development of a laparoscopic vagal-sparing esophagectomy procedure. However, both endoscopic ablation and vagal-sparing esophagectomy are limited by the fact that few or no lymph nodes are removed, and thus these procedures are suited only to patients with a very low likelihood of nodal involvement. Whereas this is true for high-grade dysplasia and intramucosal cancer in which the prevalence of lymph node metastases is 2% to 6%, once an adenocarcinoma penetrates into the submucosa, the likelihood of lymph node involvement increases to 30% to 50% [5, 6]. Because of the high prevalence of nodal involvement with submucosal or deeper invasion, therapies that do not address potential node metastases are considered inadequate.

Currently no nonresectional procedure or test can accurately identify invasion beyond the muscularis mucosa into the submucosa. The accuracy of standard 7.5-MHz and 12-MHz endoscopic ultrasound probes to distinguish intramucosal or submucosal (T1) lesions from lesions that penetrate into the muscularis propria is only approximately 50% to 60%, and any attempt to define intramucosal versus submucosal invasion is purely a chance estimate [7, 8]. High-frequency 20-MHz or greater probes offer better definition of the esophageal wall, but the accuracy for evaluating penetration beyond the mucosa into the submucosa remains problematic [9, 10]. Limitations in the accuracy of endoscopic ultrasound occur in part because of peritumoral edema that suggests invasion into the submucosa, or unrecognized microscopic invasion beyond the muscularis mucosa that leads to understaging of the lesion.

We have found EMR to be a highly effective technique to pathologically determine the depth of tumor invasion in early esophageal cancer. The resection plane occurs consistently at the interface between the submucosa and the muscularis propria. Thus, from an EMR specimen a pathologist can accurately determine whether the tumor has breached the muscularis mucosa and entered into the submucosa. Using the large cap for EMR, lesions up to 1.5 cm in size can be excised with one application. However, piecemeal excision of a lesion is also acceptable. If the EMR is only done for staging and a surgical resection is planned, then the EMR resection margins are not important, and as long as an adequate portion of the tumor is excised to be confident of the depth of invasion no further efforts at excision are necessary. However, many patients find it reassuring during the remainder of their workup to know that their tumor has been removed. Using this technique, we found that the EMR accurately determined the depth of tumor invasion in all cases, and had completely excised the target lesion in 86% of patients, usually with only a single application.

One patient had an incomplete resection with the EMR procedure, and residual cancer was found in the resected esophagus. This patient had tumor present up to the cauterized edge of the EMR specimen. All patients with negative margins on the EMR specimen had no evidence of tumor at the EMR site on pathologic assessment of the resected specimen. Thus negative margins are a reliable indicator of complete excision with EMR. However, tumor at the cauterized margin of the specimen indicates the potential for residual tumor at the site, and if surgical resection is not planned then repeat EMR or other ablative technique is warranted in these patients.

Endoscopic mucosal resection may be adequate therapy for patients with intramucosal cancer who have medical comorbidities making the risk of resection prohibitive. However, in 2 of 7 patients (29%), we found an additional cancer in the resected specimen that had not been detected despite multiple preoperative endoscopies. This is not surprising as numerous reports have confirmed that 30% to 50% of patients who undergo an esophagectomy for high-grade dysplasia are found to have an undetected adenocarcinoma in the surgical specimen [11, 12]. Thus, if EMR is used as primary therapy in patients with adenocarcinoma, continued careful surveillance of the residual Barrett's is necessary. This concept has been confirmed recently in a German series in which 57 patients with high-grade dysplasia or intramucosal cancer were primarily treated with EMR. Within 11 months of the procedure, 9 patients (16%) had local recurrence or development of a metachronous cancer [13]. In an effort to reduce this risk, Buttar and colleagues [7] combined EMR with photodynamic therapy to ablate the residual Barrett's. Using this approach, they reported that no new or recurrent cancers developed in 16 patients during a median follow-up of 13 months, although residual Barrett's was present in 47% of the patients.

It is important to realize that the use of EMR to precisely stage the depth of tumor invasion is necessary only if endoscopic therapy or a vagal-sparing esophagectomy is contemplated for the patient. Transhiatal or other traditional esophagectomies include a lymphadenectomy, and thus the distinction between intramucosal and submucosal lesions is not important. However, the morbidity of a traditional esophagectomy, although acceptable when death from cancer is a significant concern, is a barrier to physician and patient acceptance for therapy of high-grade dysplasia and intramucosal cancer. This sentiment is reflected in the literature by statements such as "surgery remains radical prophylaxis... offering a massive macroscopic morbid solution for a microscopic mucosal problem" [14]. To increase patient acceptance and reduce the long-term morbidity of an esophagectomy, we have refined a vagal-sparing technique and applied it increasingly to patients with high-grade dysplasia [15]. However, the inability to accurately determine intramucosal from submucosal invasion, and prior data indicating that 75% of small endoscopically visible lesions have invaded into the submucosa, discouraged application of the vagal-sparing technique in patients with early adenocarcinoma [12]. By incorporating EMR to determine the precise depth of tumor invasion, the benefits of a vagal-sparing procedure can now be confidently extended to a larger group of patients. Likely, the advantages of complete removal of the diseased esophagus with preservation of the vagus nerves and no dumping or diarrhea will compare favorably in the long term with results using photodynamic therapy or other endoscopic procedures in these patients.

In patients with submucosal invasion, the risk of lymph node metastases has precluded endoscopic therapies or vagal-sparing esophagectomy even though the majority of these patients (50% to 70%) will be found not to have nodal involvement after complete resection and lymphadenectomy. A recent series from Japan described the use of EMR for tumors invading into the muscularis mucosa or initial one third of the submucosa in patients who were unfit for or refused surgical resection. Only 2 of the 26 patients (7.7%) died of cancer at a median follow-up of 45 months, and the overall survival of this group was not significantly different from a comparison group of patients with similar tumors who underwent surgical resection with lymphadenectomy [16]. Two important considerations about this study are that these were all squamous tumors rather than adenocarcinoma, and the proportion of patients who had submucosal invasion was not provided. Nonetheless, this study suggests that in patients unfit for surgery, EMR of early tumors is an option, but death as a result of metastatic cancer will occur in some patients, and perhaps EMR should be combined with radiotherapy in patients with submucosal invasion, particularly if EUS raises suspicion of lymph node metastases. For patients able to undergo surgery, ideally techniques will be developed, perhaps as an extension of the sentinel node concept, that will permit accurate identification of those patients with submucosal invasion who need a lymphadenectomy.

In conclusion, EMR is a valuable adjunct to EUS to accurately determine intramucosal from submucosal tumor invasion. This allows patients with visible lesions that are confined to the mucosa to undergo therapy that does not include lymphadenectomy with little risk that involved lymph nodes will be left untreated. Future studies comparing the morbidity, mortality, and long-term quality of life in a larger group of patients after endoscopic therapy or esophagectomy with and without vagal preservation will be necessary to fully assess the pros and cons of each approach.

	DISCUSSION

Top Abstract Introduction Material and Methods Results Comment DISCUSSION References

 
DR NASSER K. ALTORKI (New York, NY): Steve, I enjoyed that presentation, and I think going forward, just looking 5 to 10 years from now, we all are going to be challenged to find less invasive treatments for cancer in general. I have been thinking a lot about what you have done here, and you have shown that if the cancer is intramucosal, you virtually have no lymph node metastases. That has been shown by your group, by ours, and by many others. I think the next logical step, and I see that you mentioned it somehow with skepticism in your conclusion, is if you have an intramucosal cancer, why is mucosectomy not enough?

DR DEMEESTER: Thanks, Nasser. I did not present in this series the group of patients I have who have been treated only with endoscopic mucosal resection, and I have some of those, patients who are at high risk for surgical resection or other factors. My conclusion related to patients with long-segment Barrett's and multifocal high-grade dysplasia. I think those patients remain at very high risk for recurrent cancers. There is a German series that has been following these types of patients with repeated endoscopic mucosal resections with reasonable success, and that is something to be considered, but a young patient with high-grade dysplasia, you are committing that patient to frequent surveillance endoscopies and multiple procedures and not eliminating the risk of cancer death, whereas a vagal-sparing esophagectomy eliminates that and I think will compare favorably long term to endoscopic treatment in these patients. Short-segment Barrett's is a different story, and endoscopic alternatives to resection may be reasonable in some situations.

DR WAYNE HOFSTETTER (Los Angeles, CA): Doctor DeMeester, you continue to be a mentor and your unit continues to be a mentor to this young surgeon's career, and I appreciate that and I very much enjoyed your talk today.

Previously you discussed being able to visualize a lesion as being an indicator that that was maybe a submucosal lesion versus a more superficial lesion. Two questions come out of this. In patients who have just high-grade dysplasia, how are you choosing where to biopsy? Are you using your endoscopic ultrasound as an indicator? And the second question is, when you did see a visible lesion in the cases that you did, did it hold true that those visible lesions led to a deeper invasion?

DR DEMEESTER: Thanks, Wayne. The previous paper that we published was on occult esophageal adenocarcinomas, and we did find that about 75% of small visible lesions had invaded into the submucosa. Because only those without submucosal invasion were candidates for a vagal-sparing esophagectomy, the conclusion of that paper was that the presence of a visible lesion should discourage the vagal-sparing approach. However, this study was done to take things one step further. The reality is that many of these early tumors are not into the submucosa, and we now have a technique other than just sort of guesswork to know how deep the tumor has invaded and select those patients who can have a non–lymph-node-removing vagal-sparing procedure very accurately.

Your second question again?

DR HOFSTETTER: Basically how did you know where to choose to biopsy on high-grade dysplasia when you do not have anything visible?

DR DEMEESTER: Patients with high-grade dysplasia were no different than anybody else. They get very closely spaced, 1-cm or 2-cm four-quadrant biopsies randomly, essentially, but any abnormality in the mucosa, nodule, and ulcer is carefully biopsied.

DR HOFSTETTER: But then will you do an endoscopic mucosal resection in the patients who had high-grade dysplasia or just routine jumbo biopsy forceps?

DR DEMEESTER: Just routine biopsies. Endoscopic resection is reserved for those patients with a visible lesion; otherwise it is no better than a biopsy, just a bigger piece.

DR DAVID V. SABORIO (Brooklyn, NY): That was a very nice presentation.

I saw that you did a couple cases with colon transposition. I would like to know why you chose that procedure instead of conventional esophagectomy with gastric pull-up for these early tumors.

DR DEMEESTER: There are some advantages to the colon interposition in that the entire innervated stomach is preserved, and these patients eat really very normally. The drawback to the gastric pull-up is that you do excise a portion of the stomach to tubulize it and you reduce some of the gastric volume. You preserve pyloric innervation, so there is no dumping in those patients, but it is not quite as physiologic as leaving the entire stomach in the abdomen and replacing the esophagus with the colon. So the colon is generally used in younger patients. Both those patients were in the 30-year-old to 40-year-old range and had a long life span ahead of them. The laparoscopic gastric pull-up I have been using in older patients. But it may be that that is the best way to go. That is one of the questions we are going to try to answer during the next year or two.

DR MEHDI FAKHRAI (Mission Hills, CA): In the multiple biopsies that you have done, were they evenly penetrating the submucosa or were they all in the mucosa or none penetrating deep, a different penetration area on different biopsies?

DR DEMEESTER: If you are referring to the endoscopic mucosal resection, it reliably cleaved at the interface between the submucosa and muscularis propria in all cases. You always get the mucosa and submucosa. If you are referring to standard biopsies, no, they generally just are in the mucosa. Occasionally you will see muscularis mucosa, but standard biopsies generally do not reach the submucosa.

DR JAMES D. LUKETICH (Pittsburgh, PA): Nice paper, Steve. The thoracic surgeons in your group do their own endoscopic ultrasounds; is that correct?

DR DEMEESTER: Correct.

DR LUKETICH: And you also do your own endoscopic mucosal resections?

DR DEMEESTER: Correct.

DR LUKETICH: What is the learning curve on the endoscopic mucosal resection? Have you seen complications before developing expertise? And how long does it take to do that? It looked pretty slick the way you popped the specimen out of there and obtained a nice pathologic result. I just wondered for the other surgeons in the group who might be considering taking this up, what do you think the learning curve is?

DR DEMEESTER: Well, thank you. It is an important question. I think one thing we have to learn from our cardiac colleagues is that you do not ever give up the minimally invasive approaches because that is the future, and, as surgeons, we need to stay in the forefront. Any surgeon who can do endoscopy can do endoscopic mucosal resection. It is really quite straightforward. The learning curve is minimal. The only important consideration is injecting the submucosa well to elevate the lesion, and then it is very, very safe to excise these. There is a potential for full-thickness bites, perforations, to occur, but if done appropriately it is very rare and very safe.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Mary S. Maish Steven R. DeMeester Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Maish, M. S. Articles by DeMeester, S. R. Search for Related Content PubMed PubMed Citation Articles by Maish, M. S. Articles by DeMeester, S. R. Related Collections Esophagus - cancer