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Ann Thorac Surg 2005;80:1001-1006
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Locally Recurrent Esophageal Carcinoma: When is Re-Resection Indicated?

Paul H. Schipper, MD, Stephen D. Cassivi, MD * , Claude Deschamps, MD, David C. Rice, MD, Francis C. Nichols, III, MD, Mark S. Allen, MD, Peter C. Pairolero, MD

Division of General Thoracic Surgery, Mayo Clinic College of Medicine, Rochester, Minnesota

Accepted for publication March 23, 2005.

* Address reprint requests to Dr Cassivi, Division of General Thoracic Surgery, Mayo Clinic, 200 First St SW, Rochester, MN 55905 (Email: cassivi.stephen{at}mayo.edu).

Presented at the Forty-first Annual Meeting of The Society of Thoracic Surgeons, Tampa, FL, Jan 24–26, 2005.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
BACKGROUND: Limited locally recurrent esophageal carcinoma is rare, and little is known regarding effectiveness of re-resection.

METHODS: Medical records of 27 consecutive patients with locally recurrent esophageal carcinoma who underwent reoperation at our institution between February 1974 and January 2003 were analyzed.

RESULTS: The original and recurrent cancer cell types were identical in all patients. Median disease-free interval was 19.4 months (range, 2.5 to 170 months). Recurrence was at the anastomosis in 23 patients (85%), esophageal remnant in 3 (11%), and stomach in 1 (4%). Ten patients had completion gastrectomy and partial esophagectomy, and 9 had resection of the anastomosis. The remaining 8 patients were found intraoperatively to have unresectable disease and underwent biopsy only. Re-resection was complete in 15 of the 19 patients resected (79%). Four patients had microscopic cancer at the resection margins. Reconstruction was with colon in 10 patients and esophagogastrostomy in 9. There were 2 deaths (operative mortality, 7%). Complications occurred in 16 patients (59%). Arrhythmia and anastomotic leak were the most common complications and each occurred in 7 patients (26%). Factors favorably associated with survival were disease-free interval greater than 2 years (p ≤ 0.05) and complete re-resection (p ≤ 0.02). Two-, three-, and five-year survival for patients completely re-resected was 62%, 44%, and 35%, respectively. Survival for patients who had incomplete re-resections was 18% at 2 years and zero at 3 years.

CONCLUSIONS: Re-resection of locally recurrent esophageal carcinoma is associated with considerable morbidity. However, long-term survival is possible in patients with a long disease-free interval or a complete re-resection.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Esophageal carcinoma continues to have a poor prognosis. Although 5-year survival for early stage, completely resected disease has been reported to be between 79% and 94% [1–3], 5-year survival for all stages range between 25% and 41% [1, 2, 4]. First recurrence, in the majority of patients, occurs as distant metastases. In a few patients, however, recurrence is localized and limited to the site of previous resection [1, 2, 4–9].

Treatment options for locally recurrent esophageal carcinoma are limited. Preliminary reports suggest a potential survival benefit from re-resection. These reports, however, are limited to between 1 and 9 patients [10–13]. The purpose of this study is to evaluate the outcomes of our patients who underwent re-resection for recurrent esophageal cancer to better define the role of surgery in this clinical situation.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 Acknowledgments
 References
 
All patients who underwent re-resection of recurrent esophageal carcinoma at our institution between February 1974 and January 2003 were identified from a prospectively maintained surgical database. Only patients who had their initial surgery and re-resection at our institution were included. The medical records of these patients were reviewed for patient demographics, characteristics of the first and recurrent cancers, type of operation performed initially and at reoperation for recurrence, adjuvant and neoadjuvant therapy, disease-free interval, postoperative morbidity and mortality, length of hospitalization after second operation, presenting symptoms of recurrent cancer, diagnostic procedures used to evaluate recurrent cancer, stages of first and recurrent cancers, last follow-up visit or date of death, disease status at follow-up or death, and cause of death. Recurrence, resectability, and operability were identified by history and physical examination combined with esophagogastroduodenoscopy and biopsy, endoscopic ultrasound, computed tomography, barium swallow, and positron emission tomography. All patients were staged for esophageal cancer using the Union Internationale Contre le Cancer staging system [14]. Survival and mortality data were verified with the Social Security Death Index. For the purposes of our analysis, we divided the surgical procedures into those undergoing re-resection and those with unresectable disease determined intraoperatively. We classified the re-resection procedures as either complete resection (R0) or incomplete resection (R1) if microscopic examination of the surgical margins revealed the presence of residual cancer. Operative mortality included patients who died within 30 days after operation or at any time during their initial postoperative hospitalization.

Descriptive statistics are reported using numbers (percent) for discrete data and median (range) for continuous data. Survival subsequent to discharge was estimated among the 25 reoperation patients who survived hospitalization using the Kaplan-Meier survival method. The association between patient survival and risk factors was examined using the log-rank test [15, 16]. The study was reviewed and approved by the Mayo Clinic College of Medicine Institutional Review Board.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 Acknowledgments
 References
 
Twenty-seven consecutive patients were identified (22 men and 5 women). Median age at the time of reoperation was 59 years (range, 28 to 78 years). Median disease-free interval from the first esophageal resection to the diagnosis of recurrence was 19.4 months (range, 2.5 to 170 months). Only 1 patient had a disease-free interval of less than 6 months. Symptoms were present in 20 patients (74%) and included dysphagia in 16 (59%), chest pain in 6 (22%), weight loss in 1 (4%), early satiety in 1 (4%), and symptoms of perforation in 1 (4%). Recurrence in the 7 asymptomatic patients (26%) was discovered on routine long-term surveillance at our institution. Preoperatively, recurrence was suggested by barium swallow alone in 2 patients (7%) and diagnosed by esophagogastroduodenoscopy with biopsy in 25 (93%). Additional evaluations included chest and abdomen computed tomography in 15 patients (56%), barium swallow in 13 (48%), endoscopic ultrasound in 7 (26%), and positron emission tomography in 2 (7%). Patient demographics and operative details are listed in Table 1. Pathologic staging is listed in Table 2.


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  		Table 1. Patient Characteristics and Operative Details
 

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  		Table 2. Pathologic Stage of Initial and Recurrent Esophageal Carcinoma
 
Hospital Course
Ten patients had completion gastrectomy and partial esophagectomy, and 9 had resection of the anastomosis. The remaining 8 patients were found intraoperatively to have unresectable disease and underwent biopsy only. Re-resection was complete in 15 of the 19 patients resected (79%). Four patients had microscopic cancer at the resection margins. Reconstruction was with colon in 10 patients and esophagogastrostomy in 9. Fifteen of these patients had complete (R0) resections; the remaining 4 had residual microscopic cancer at the margins of resection (R1). All re-resections and reconstructions were completed during the same operation.

Two patients died (operative mortality, 7.4%). Cause of death was multisystem organ failure at 30 days in 1 patient who was completely resected and exsanguination from an incompletely resected tumor eroding into the neck vessels at 23 days in another patient. Median hospitalization in the remaining 25 patients was 14 days (range, 2 to 64 days). Median hospitalization for those patients who were re-resected was 20 days (range, 8 to 64 days), as compared with only 8 days (range, 2 to 12 days) for those who were explored without re-resection. Complications occurred in 16 patients (59%) and are detailed in Table 3. Ten patients (37%) required an additional operation to treat a complication. Five patients had more than one additional operation. Reoperations for complications included drainage and diversion for anastomotic leaks in 4 patients, reexploration for bleeding in 2, pectoralis major muscle transposition to reinforce a cervical anastomosis in 2, ligation of thoracic duct in 2, tracheostomy and thyroplasty for bilateral vocal cord paralysis in 1, and exploratory laparotomy with lysis of adhesions for small bowel obstruction in 1.


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  		Table 3. Complications of Operation for Recurrent Esophageal Carcinoma
 
Long-Term Results
Follow-up was complete in 24 patients (89%) with a median follow-up of 10.5 months (range, 1 month to 6.1 years). One patient was lost to follow-up after 5 months, and 2 were lost after 4 years. Of the 15 patients completely re-resected, 3 are alive without evidence of recurrence at 0.4, 1.7, and 4 years, and 1 is alive with disease at 4.1 years. Eleven patients have died, 4 of recurrent carcinoma, 4 of other causes without evidence of cancer recurrence, and 3 of unknown causes. Of the 12 patients incompletely re-resected, 10 (83.3%) have died of recurrent carcinoma. Owing to incomplete cause of death data, disease-specific death could not be factored into the survival analysis.

Survival
Factors not significantly affecting survival included age, preoperative chemotherapy and radiation therapy, presence or absence of symptoms, complications, and site of local recurrence. One-, three-, and five-year survival for the 25 patients surviving operation was 46%, 23%, and 19%, respectively. Median survival for this group was 1 year. Factors significantly associated with longer survival were disease-free interval greater than 2 years (p ≤ 0.05) and complete (R0) resection (p ≤ 0.02). Patient survival was not significantly associated with age younger than or older than 60 years (p = 0.13), preoperative chemotherapy (p = 0.38) and radiation therapy (p = 0.38), presence or absence of symptoms (p = 0.88), complications (p = 0.41), or site of local recurrence (p = 0.37).

One-, three-, and five-year survival for the completely resected patients (R0) was 62%, 44%, and 35%, respectively. Survival for incomplete resection was 27% at 1 year, 18% at 2 years, and none by 3 years (Fig 1).



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  		Fig 1. Survival (death from any cause) in 15 patients who underwent complete resection (solid line) compared with 12 patients who had incomplete resection (dotted line) of locally recurrent esophageal carcinoma. Zero time on abscissa represents date of reoperation to treat recurrence.

 
The effect of stage at the time of re-resection is detailed in Figure 2. Although a trend toward better survival with earlier stage of recurrence was observed, this did not reach statistical significance (p ≤ 0.07).



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  		Fig 2. Survival (death from any cause) by stage of locally recurrent esophageal carcinoma in 27 patients who underwent reoperation. Zero time on abscissa represents date of reoperation to treat recurrence.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 Acknowledgments
 References
 
Esophageal carcinoma continues to have a poor prognosis despite aggressive surgical intervention. Recurrent cancer is the leading cause of death in patients undergoing surgical resection and most commonly presents as distant metastases. Median survival after the diagnosis of recurrence is 2.7 to 7 months [4, 9]. Whereas most recurrences are either to regional lymph nodes or disseminated distant metastases, approximately one third of resected patients will present with recurrent cancer at the esophageal anastomosis [5, 6]; fewer than half, however, will be isolated local recurrences [4, 5, 9]. Treatment options for anastomotic recurrence are limited. Palliation of esophageal obstruction may be achieved with endoprostheses, endoscopic recanalization, photodynamic therapy, chemotherapy and radiation therapy, or surgical bypass [17–19]. Improvement in long-term survival, however, has been limited [20, 21].

Staging recurrent esophageal cancer is problematic and poorly defined in the literature. We elected to use the Union Internationale Contre le Cancer guidelines for esophageal carcinoma with the understanding that the depth of recurrent tumor invasion at the site of a previous anastomosis may be difficult to accurately define. Nevertheless, the stage of disease at the time of re-resection did not significantly affect survival, although a trend toward longer survival was observed with a pathologic stage I recurrence.

Although curative surgical resection of locally recurrent cancer is common practice in certain tumors, such as hepatocellular [22, 23], breast [24, 25], and rectal carcinoma [26, 27], reports of re-resection for locally recurrent esophageal cancer are either anecdotal [10, 11, 28, 29] or limited to only a few (9 or fewer) patients [12, 13, 30]. The present study, involving 27 consecutive patients collected during a 29-year period, provides the largest reported series that demonstrates the potential for significant long-term survival after a long disease-free interval and complete re-resection.

Reoperation for resection of locally recurrent esophageal cancer can be technically challenging. Not only is the approach made more difficult by scar tissue from the previous resection, but often the operative field has been irradiated a number of months or even years previously. Specific care must also be taken to avoid compromise of the previously transposed conduit to not endanger its vascular supply. This is especially true if the conduit is to be used again to ensure alimentary tract continuity. As well, protection of the recurrent nerves in either the chest or neck can prove to be similarly hazardous. Preoperative assessment of vocal cord function would identify patients with previous injury from earlier surgery.

When looking at other options for locally recurrent esophageal cancer, long-term survival results of re-resection, when it is possible, compare favorably with results obtained with either external beam radiation or combined chemotherapy and radiotherapy. In a recent study of patients with locally recurrent esophageal cancer after curative-intent surgical resection, 1- and 3-year survival rates were 33% and 12%, respectively, similar to our results for patients with incomplete re-resections and far less than our patients obtaining complete re-resection [31]. Similarly, combined chemotherapy and radiotherapy showed 1- and 3-year survival rates of 47% and 4%, respectively [32].

Despite reasonable operative mortality, re-resection of recurrent esophageal cancer is associated with potentially significant morbidity. In addition, one third of patients in whom resection was attempted were ultimately found to be unresectable despite extensive preoperative evaluation and staging. A further 15% of patients who underwent re-resection were found to have microscopic residual disease (R1). Only 55% of our series of patients were deemed completely resected after surgery.

In conclusion, re-resection of locally recurrent esophageal carcinoma can result in considerable morbidity. However, long-term survival is possible and more likely in patients with a long disease-free interval and those who have had a complete resection of the recurrent tumor.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
Acknowledgments
 References
 
DR SANDRO MATTIOLI (Bologna, Italy): I have three questions for you. First, did you check if the resection margin was positive at the first operation? Second, 89% were adenocarcinomas. Did you check the grading of these adenocarcinomas and did you put in relation the grading and the modality of recurrence? Third, were those recurrences macroscopic or microscopic such as in case of a small nodule at the level of the anastomosis with cancer at histhology of the endoscopic biopsy?

Thank you.

DR SCHIPPER: In answering your question about grading and staging of the initial and recurrent cancers, we did make an attempt to stage the recurrent cancer. This is of course with the understanding that T-staging for recurrent esophageal cancer is not well delineated in the literature, and in the presence of an anastomosis may not be completely accurate. What we found, though, was that there was no significant difference in stage versus survival. This was the case with either the stage of the first cancer or the stage of the second cancer. We did not compare grade of first the cancer or second cancer to survival or site of recurrence.

DR DAVID W. JOHNSTONE (Lebanon, NH): How about the margins?

DR SCHIPPER: The margins of the initial resection were verified and were negative. One patient who had a recurrence at 2-1/2 months following initial resection did have a negative margin at his first resection. The disease free interval in this case however is fairly short and raises the suspicion of occult positive margins. In all other patients, the disease-free interval was greater than 6 months.

DR DANIEL L. MILLER (Atlanta, GA): I would like to congratulate you on an excellent presentation.

As you present this series, which is a very difficult group of patients, you only had a very small percentage of them who had complete resection. As you look back at a large series over 30 years or so, I think we have to make new guidelines of how to handle this. From your review of this, what would you recommend now that we should do in the future when you have a re-resection? I know you’ve brought up some things about a longer disease-free interval would be helpful. Also, almost 50% of your patients had neoadjuvant treatment. Was that really necessary in this group of patients, and if it was, was there any correlation with a complete pathologic response like we’ve seen with first-time cases? So I think a lot of this information is good, but I think as we put it together, we’ve got to come home with a take-home message, and for a lot of us, I would say that we probably would not re-resect these patients because of their high mortality and morbidity.

I have one last question. You had a very low number of PET scans on these patients. I think a lot of us would do very extensive staging prior to this procedure to make sure they don’t have distant disease.

Thank you.

DR SCHIPPER: I think your last point is a good point. This study spanned 29 years. Therefore, what constituted a complete preoperative clinical staging workup during the course of this study was clearly different. Later on in the series more patients were subjected to newer more sensitive staging modalities such as PET scans, CT scans, spiral CT scans and so forth. Given the differences attributable to staging modalities available at different time periods of this study, in all patients who underwent an operation were felt to have a clinically isolated local recurrence and the operation planned was a complete resection.

It is difficult to make a blanket recommendation from this data set. Clearly every patient needs to be evaluated individually as to their medical suitability for surgery with the understanding that re-resection can be a difficult operation to under-go with significant potential morbidity. The take home message is that re-resection should be a consideration, and that in selected cases it can be associated with significantly prolonged survival.

DR JAMES C. JONES (Scranton, PA): I have a problem with your definition of recurrence. I see that some of your patients had disease-free intervals of greater than 10 years. To my mind, an interval greater than 10 years suggests that a patient probably had a new primary rather than a recurrence. Could you address that point?

DR JOHNSTONE: The patients who have a long disease-free interval, do you regard those as a new primary, or how do you prove that this is a recurrence of the original?

DR SCHIPPER: We regarded cases with disease at the anastomosis or in the bed of a previous resection and with the same tumor histology as recurrences.

DR JOSEPH I. MILLER (Atlanta, GA): I congratulate the authors on a very excellent series. You’ve just brought up probably one of the most difficult groups of patients in general thoracic surgery that you take care of.

I have one question and one comment. In those 15 patients who you did a complete resection on, how many had had neoadjuvant therapy? When they have had neoadjuvant therapy with radiation to 4,500 rads, unless you’re going back early, I have found it technically sometimes almost impossible to get the stomach out. If you had an Ivor-Lewis, it’s plastered on the back wall of the trachea. It’s very difficult. So I congratulate you in doing that.

So the technical question would be how many of those patients had had neoadjuvant therapy? And it might be something that Dr. Allen or one of your other colleagues might answer. The other thing, when you have had an anastomotic recurrence, we have found that photodynamic therapy in that area followed by brachytherapy is very useful, with a very low complication rate, and provides about the same short-term survival that you have presented.

I congratulate the authors.

DR SCHIPPER: The percentage of patients receiving neoadjuvant therapy before their second resection was 44%. This was 44% of the whole group and not solely the complete resection group.

DR JOHNSTONE (Lebanon, NH): Did that correlate with complete resections? Was there a higher preponderance of patients who got preoperative therapy in the complete resection group?

DR SCHIPPER: We did not have large enough groups to make that comparison. This was therefore not included in the statistical analysis. This got into sub-groups that were too small in size to allow for a useful analysis.

DR FRANCIS C. NICHOLS III (Rochester, MN): Dr Schipper, I think both Dr Joseph and Daniel Millers’ points are very good. Did the patients get neoadjuvant, and I’ll use the term "neoadjuvant" meaning chemo and radiation therapy, with the intent of downstaging the patients before re-resection or were these patients that were referred to you after they had failed chemo and radiation therapy still having significant dysphagia? Leading to Dr Dan Miller’s second question, what would you do today if you saw these people, since it basically was 27 patients over 30 years.

DR SCHIPPER: These patients were referred to us already having received chemotherapy and radiation therapy. We were not able to discern what the intent of the gastroenterologists was in delivering this therapy. With regard to our current recommendations, we would favor in most cases to proceed with resection and not give pre-operative therapy. However, this is our recommendation only, since there are not direct data to favor one approach over the other.

DR WAYNE HOFSTETTER (Houston, TX): I want to congratulate you on a well-presented presentation.

There is not so much information on this topic in general, and I think as we learn more about this, it would be nice to ferret out some of these issues in terms of what patient population we’re looking at. My opinion is that we’re going to tend to see more and more of these patients over time, especially as we’re operating on younger patients with high-grade dysplasia or early disease, and many of these patients have undergone Ivor-Lewis esophagectomies or have had gastric pull-ups and we’re seeing significant dysplastic changes in the esophagus within a couple years of their resection. So the question that really comes up is what are we doing with these patients who are not so much recurrent but they are having a second primary within a short period of time within the residual esophagus.

In your data you mentioned that 56% of the patients that you saw who had recurred, recurred after an Ivor-Lewis esophagectomy. Did the pattern of recurrence that you see lead you to change your surveillance, or what is your surveillance that you’re performing?

DR NICHOLS: Dr. Hofstetter basically wants to know about Ivor-Lewis esophagogastrectomy and our resection margins in that regard and surveillance.

DR SCHIPPER: The post-resection surveillance for esophageal cancer at the Mayo Clinic is carried out by the thoracic surgeons in concert with a gastroenterologist or the patient’s primary care doctors. Over the 29 year period, there was no standard template for surveillance. We cannot therefore draw any specific oonclusions or recommendations regarding the optimal form of post-resection surveillance. The primary goal of this study was to see if re-resection/esophagectomy is a reasonable option for patients with recurrence.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
References
 
The authors acknowledge the expert advice and statistical assistance of W. Scott Harmsen, Master Statistician, and Brian S. Crownhart from the Department of Biostatistics at the Mayo Clinic College of Medicine.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

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