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Indications and outcome of salvage surgery for oesophageal cancer

^a Department of Thoracic Surgery, Ste Marguerite University Hospital, Marseille, France
^b Intensive care Unit, Ste Marguerite University Hospital, Marseille, France
^c Department of Digestive Oncology, La Timone Hospital, Marseille, France
^d UMR 6020, IFR 48, University of the Mediterranean, Marseille, France

Received 30 July 2007; received in revised form 6 January 2008; accepted 16 January 2008.

^_* Corresponding author. Address: Department of Thoracic Surgery, Ste Marguerite Hospital, CHU Sud, 270 Bvd Ste Marguerite, 13274 Marseille Cedex 9, France. Tel.: +33 491 744 680; fax: +33 491 744 590. (Email: Pascal-alexandre.Thomas{at}mail.ap-hm.fr).

	Abstract

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A References

 
Objective: Some patients with localised oesophageal cancer are treated with definitive chemoradiotherapy (CRT) rather than surgery. A subset of these patients experiences local failure, relapse or treatment-related complication without distant metastases, with no other curative treatment option but salvage oesophagectomy. The aim of this study was to assess the benefit/risk ratio of surgery in such context. Methods: Review of a single institution experience with 24 patients: 18 men and 6 women, with a mean age of 59 years (±9). Histology was squamous cell carcinoma in 18 cases and adenocarcinoma in 6. Initial stages were cIIA (n = 5), cIIB (n = 1) and cIII (n = 18). CRT consisted of 2–6 sessions of the association 5-fluorouracil/cisplatin concomitantly with a 50–75 Gy radiation therapy. Salvage oesophagectomy was considered for the following reasons: relapse of the disease with conclusive (n = 11) or inconclusive biopsies (n = 7), intractable stenosis (n = 3), and perforation or severe oesophagitis (n = 3), at a mean delay of 74 days (14–240 days) following completion of CRT. Results: All patients underwent a transthoracic en-bloc oesophagectomy with 2-field lymphadenectomy. Thirty-day and 90-day mortality rates were 21% and 25%, respectively. Anastomotic leakage (p = 0.05), cardiac failure (p = 0.05), length of stay (p = 0.03) and the number of packed red blood cells (p = 0.02) were more frequent in patients who received more than 55 Gy, leading to a doubled in-hospital mortality when compared to that of patients having received lower doses. A R0 resection was achieved in 21 patients (87.5%). A complete pathological response (ypT0N0) was observed in 3 patients (12.5%). Overall and disease-free 5-year survival rates were 35% and 21%, respectively. There was no long-term survivor following R1–R2 resections. Functional results were good in more than 80% of the long-term survivors. Conclusion: Salvage surgery is a highly invasive and morbid operation after a volume dose of radiation exceeding 55 Gy. The indication must be carefully considered, with care taken to avoid incomplete resections. Given that long-term survival with a fair quality of life can be achieved, such high-risk surgery should be considered in selected patients at an experienced centre.

Key Words: Oesophageal neoplasms • Chemotherapy • Radiotherapy • Oesophagectomy

	1. Introduction

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A References

 
Ongoing controversy surrounds the question of whether locally advanced cancer of the oesophagus should be resected or treated with non-surgical methods. The largest and most complete meta-analysis of randomised neoadjuvant treatment trials done so far in patients with oesophageal cancer provides evidence supporting surgery following induction concurrent chemoradiation therapy (CRT) as the standard of treatment for fit patients with locally advanced oesophageal cancer, especially in cases of adenocarcinoma [1]. The role of surgery in the multimodal approach to locoregional oesophageal cancer, however, has recently been questioned. Results of two randomised trials suggest that in cases of squamous cell cancer there is no clear survival advantage favouring surgery, even if local tumour control is significantly improved after resection [2,3]. Furthermore, the risks of surgery in this context reflect a significant effect of CRT on postoperative mortality within 90 days, due to three main adverse events: respiratory complications, heart failure, and anastomotic leak [4]. As a result, the view that completion CRT is an alternative to surgery in patients with squamous-cell carcinomas who show a morphological response to induction CRT is growingly shared by oncologists, because such treatment strategy seems to produce a similar overall survival, but with less post-treatment morbidity, and last but not least, similar quality of life [5]. In other words, full-dose CRT (definitive CRT) tends to be preferred for responders to a half-dose of CRT as much as oesophagectomy, whereas oesophagectomy is likely to be preferred for non-responders.

Unfortunately, crude locoregional control rate remains quite poor with definitive CRT, and roughly half of the patients present with a persistent or a relapsing tumour at the primary site within 1 year [6,7]. Accordingly, oesophagectomy stands out as a possible opportunity of cure for fit patients without distant metastases. Besides, local complications of definitive CRT such as intractable strictures, ulcer or perforation, may lead to a rescue surgery. Finally, the debate over definitive CRT versus neoadjuvant CRT and surgery may be reworded in terms of salvage versus planned oesophagectomy. Although both types of surgery are done in the setting of previous CRT, one may anticipate that they are different in several ways. Very few studies have addressed this issue [8–12]. Preliminary data suggest that despite an increased morbidity and mortality, a subset of patients will be offered a second chance of cure [8–12]. The selection of the ‘winners’ however, remains challenging. The present report aims to add some information on the topic.

	2. Materials and methods

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A References

 
We conducted a retrospective review of all patients having undergone oesophageal resection (n = 268) between 1996 and 2006 at our institution, and selected those patients who received salvage surgery (n = 24). Patient charts were identified by screening of a database into which data were entered prospectively for any patient undergoing surgery for thoracic malignancy at our department. Salvage oesophagectomy was defined as an operation performed after definitive concurrent chemoradiation which included platinum-based chemotherapy and more than or equal to 50 Gy radiotherapy, and selectively indicated for isolated local failures and recurrences, or treatment-related complications. In almost all patients, the initial treatment was planned at an outside centre. Once referred at our institution, a multidisciplinary decision-making process was followed. The operation was proposed to patients who were deemed physiologically amenable to surgery, whose tumour was thought to be resectable and who had no evidence of distant metastases at the work-up revaluation.

Hospital records were reviewed for age, sex, body mass index, initial clinical stage of the disease, American Society of Anesthesiology risk classification, preoperative medical history, pulmonary function test performances, tumour location, histology, residual pathologic stage graded according to the TNM classification [13], and results of preoperative laboratory and imaging studies (Table 1 ). All medical charts were also reviewed for details regarding the initial CRT. There were 6 females and 18 males whose mean age was 59 ± 9 years (range: 33–70). Tumour types included 8 adenocarcinomas located to the lower oesophagus (classified as Siewert I and II) and 16 squamous cell carcinomas predominantly located in the middle (n = 9) and the lower oesophagus (n = 7). At pretreatment evaluation, 18 patients presented with a locally advanced stage cIIb or cIII disease. Three high-risk patients presented with a stage cIIA disease. One patient was classified as having a stage cIVB due to the presence of a single lung metastasis. In 2 cIIA patients, the justification of the first-line CRT was unclear. CRT consisted of the association of 5-fluorouracil and cisplatin, and concurrent radiotherapy. The average number of cycles was 2.88 (range: 2–6). The average dose of fractionated radiation delivered to the oesophagus was 56 Gy. This value served as cut-off to split the patients population in 2 groups: 14 patients had received 50–55 Gy, while 10 had received 56–75 Gy.

Medical and surgical complications were recorded. Respiratory complications were defined by all medical events concerning the lung parenchyma (i.e. pneumonia, airway congestion, atelectasis, acute lung injury, and acute respiratory distress syndrome) in the absence of surgical complications requiring reoperation. Surgical complications included anastomotic leakage, laryngeal paralysis, chylothorax, pleural effusion, empyema and bleeding. Early mortality was checked 30 and 90 days after surgery.

All patients were seen at the outpatient clinic at intervals of three months during the first two years and every six months thereafter. Symptoms, body weight and imaging findings were routinely recorded. A self-rated scale from 1 (worse results) to 10 (best results) was used to assess the patient's digestive comfort. For patients lost to medical follow-up, missing survival data were obtained by consulting the City Hall registry. Statistical analysis included the Mann-Whitney test, the Pearson ² test, and Fisher's exact test when appropriate. Overall survival was measured from the date of operation and survivorship calculated according to the Kaplan–Meier method, including the operative mortality. Disease-free survival was counted up to the date of first relapse or death with cancer. Software used included Excel (Microsoft Corporation, Redmond, Wash), and SPSS (SPSS Inc., Chicago, Ill).

	3. Results

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A References

 
3.1 Pathological findings
The absence of viable cancer cells was observed on the operative specimen in 3 patients (12.5%). Three additional patients (12.5%) had no residual oesophageal tumour but presented with invaded regional lymph nodes. A lung metastatic disease was found intraoperatively in three patients (stage yp IVB) and distant lymph node involvement was found in two (stage yp IVA). A complete R0 resection was achieved in 21 patients (87.5%). In all three cases of incomplete resection, the tumour was located above the level of the carina (Table 4).

View larger version (36K): [in this window] [in a new window]   Fig. 1. Overall and disease-free survival curves, including operative mortality (Kaplan–Meier method).

	4. Discussion

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A References

 
Our results, combined to those of the available literature (Table 5 ), clearly show that salvage oesophagectomy is a highly morbid operation, providing an early mortality ranging from 15% to 25% at 3 months. Two types of complications dominate the spectrum of postoperative adverse events: anastomotic fistulas and pulmonary complications.

Severe pulmonary complications exceed 30–40% in incidence commonly in this setting. Respiratory complications remain the major concern after oesophagectomy, with or without previous chemoradiation. Reasons for this pulmonary morbidity are multifaceted, and those due specifically to the neoadjuvant treatment are probably very difficult to segregate from those due to the surgical procedure, to the perioperative anaesthetic management, to the patient himself and to the toxicity of the preoperative treatment. However, concurrent CRT was shown to be associated with significant worsening of the diffusion capacity of the lung for carbon monoxide (DLCO) [17]. In a recent retrospective study, dosimetric factors but not clinical factors were found to be strongly associated with the incidence of postoperative pulmonary complications. The volume of the lung spared from doses of 5 Gy and higher was the only independent factor in multivariate analysis [18]. As hypothesised for anastomotic complications, this suggests that restraining the radiation fields thus ensuring an adequate volume of lung unexposed to radiation might reduce the incidence of postoperative pulmonary complications.

Given the high risks associated with surgery in this setting, the question arises of which categories of patients can benefit from such a hazardous operation. Our results suggest that oesophagectomy should probably be avoided whenever possible in case of treatment-related local complications since 90-day mortality reached 50% in this patient group. Aside from these particular circumstances, one selection approach would be to avoid operating on patients without a proven residual or recurrent disease. Unfortunately, diagnosis of complete pathological response by imaging is difficult and often possible merely by oesophageal resection. The only easily reproducible modality for determination of response is endoscopic visualisation with biopsies of suspicious areas. Obviously, endoscopy alone cannot detect a viable disease confined to the regional lymph nodes, a frequent event even in the absence of any residual oesophageal tumour as demonstrated by the present series. Endoscopy also failed to provide conclusive tissue biopsies in 7 of the 18 patients (39%) in whom the analysis of the operative specimen found viable cells inside the oesophageal wall. The assessment of locoregional tumour extension by EUS-FNA is thought currently the most reliable method. FDG PET guided EUS FNA is advocated in PET-positive nodes, particularly at the coeliac region [19]. A recent study, however, demonstrated that a complete absence of PET signal cannot be equated with a complete pathological response: the accuracy of the 100% reduction in maximum standardised uptake value after neoadjuvant treatment as a predictor of a complete pathological response was only 15% [20]. When combining imaging modalities with FDG PET, CT, and EUS it is not possible to confirm the absence of residual viable disease in the primary site in 25–40% of the cases [21].

In most series, long-term survival reaches roughly 30–35% at 5 years, a non-negligible rate in such a disastrous disease. Functional aspects of the surgical results are seldom addressed. Even if our functional evaluation method was approximate, our data suggest that the quality of oral intake was fair in more than 80% of the patients. Health-related quality of life seemed to be predominantly impaired by progression of the disease. We found that the residual TNM was not an accurate prognosticator although the small number of patients precluded a comprehensive analysis of survival. Basically, patients who may benefit most from surgery are those in whom a complete R0 resection could be performed. Indeed, R0 resection can serve as an immediate surrogate for outcome since patients who are left with gross or microscopic residual tumour will almost always die promptly from progressive disease, as in our experience. The link between local recurrence and margin of normal tissue surrounding a resected cancer is well established. In contrast with longitudinal clearance which is easily predictable on the basis of both endoscopic inspection with Lugol's stain screening for a multifocal disease, and EUS examination of the proximal oesophagus looking at submucosal spreading, circumferential clearance is hard to anticipate. In the absence of serosa, there is no specific fascial boundary to circumferential spread of oesophageal cancer. In a prospective study, the finding of a tumour within 1 mm of the circumferential margin of the fixed resection specimen of patients undergoing what would have been regarded as a potentially curative resection was found as a highly significant predictor of both local recurrence and survival [22]. The role of the surgeon should therefore be to resect the oesophagus with as wide a margin of uninterrupted normal tissue as possible around it. This goal is amenable in most cancers located below the level of the carina, even in cases of bulky tumours. In contrast, the upper and middle oesophagus is surrounded closely by vital structures that cannot be resected en-bloc. EUS does not add to the estimation of locoregional respectability after RCT because of disorganising fibrotic sequelae at the level of the tumour and its surroundings [23]. We set up our decision to operate or not on the basis of CT scan and barium swallow findings mainly, with a high suspicion index of unresectability in cases of lumen deviation, tumour height >5 cm, aortic contact >90°, loss of the fat plane between tumour and neighbouring organ, or tumour indenting neighbouring organ at CT scan, as thoroughly described after neoadjuvant CRT by Piessen et al. [24]. As a result, our 87.5% R0 resection rate compares favourably with those of the literature.

Nevertheless, our firm belief is that the indication for salvage surgery should be limited to patients with an initially resectable tumour. Current treatment strategies for locally advanced cancers currently favour neoadjuvant chemotherapy or chemoradiotherapy followed by surgery for adenocarcinomas, but chemoradiotherapy alone in patients with SCC who have shown a morphological response after induction treatment [25]. We want to add a word of caution concerning salvage oesophagectomy that should not be regarded as a routine rescue procedure in case of failure of definitive CRT. In turn, indications for non-surgical treatment strategies should be decided on solid grounds, and reserved to those patients thoroughly investigated with EUS FNA and integrated PET-scan, and presenting with a supracarinal oesophageal tumour deemed consensually to be non-resectable. We, as oesophageal surgeons inside a multidisciplinary team, should be pivotal partners of the primary decision to keep surgery or not in the treatment plan, as we are when a salvage surgery is evoked.

In conclusion, this study confirmed increased morbidity and mortality after salvage oesophagectomy performed after definitive chemoradiation therapy. The increased risks seemed to be predominantly related to radiotherapy delivery modalities, and the management of local treatment-related complications is indubitably the worse situation in which such risky operation may be performed. Nevertheless, some patients were cured, and long-term survival appeared to be associated primarily with R0 resection. These data suggest that salvage oesophagectomy is an elective therapeutic option for carefully selected patients at experienced referral centres.

	Appendix A

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A References

 
Conference discussion

Dr R. Berrisford (Exeter, UK): I would just like to ask the audience to put your hand up when you consider a patient for oesophagectomy you use this kind of concept of salvage oesophagectomy (very few members of the audience raised their hand). That is reassuring because in our MDTs we don’t usually use that concept. I was very interested to see that in your definition of these you include patients who had chemotherapy who are node positive. We include patients who are node positive after chemotherapy quite routinely but we don’t think that they are salvage patients, maybe we should do. So what do you think your definition of salvage oesophagectomy should really include?

Dr D’Journo: Thank you very much for your question. It is a problem of definition. Firstly it is important to note that all these patients were initially treated at an outside institution so we didn’t participate in the initial treatment strategies. We included patients with a persistence or relapse of tumour after definitive chemoradiotherapy. We believe that in this very selected subgroups of patients, surgery provides the unique alternative option to rescue them from a fatal issue. In fact there is no other possibility of treatment such as a palliative chemotherapy. The unique curative option is just surgery.

The main result of our study is probably that morbidity and mortality were related to volume of radiation. So when you propose a patient for a salvage oesophagectomy, maybe you have to look on the volume of radiation. For a volume dose of radiation up to 50 Gy, the operative risk is probably prohibitive.

Dr J. Duffy (Nottingham, UK): Just looking at the group you operated on, 2 of them with an oesophageal perforation. Did they survive?

Dr D’Journo: No.

Dr Duffy: So you are quite hard on yourself in your results. I am sure many other series would have excluded the patients with oesophageal perforation.

The second question is, why did these patients have chemoradiotherapy as opposed to surgery in the first place and why wasn’t surgery part of that plan of treatment?

Dr D’Journo: I don’t know because the treatment strategy was given at another institution. We didn’t participate in the initial discussion. The patients were referred to our hospital, maybe 3 or 6 months after completion of the definitive chemoradiotherapy.

Dr Duffy: In your 5-year survival are you including surgical mortality?

Dr D’Journo: Yes, we included the operative mortality. But it is difficult to draw some conclusions on long-term survival because it's a very small series.

	Footnotes

 
Presented at the 15th European Conference on General Thoracic Surgery, Leuven, Belgium, June 3–6, 2007.

	References

Top Abstract 1. Introduction 2. Materials and methods 3. Results 4. Discussion Appendix A 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): Christophe Doddoli Roger Giudicelli Pierre A. Fuentes Pascal A. Thomas Permission Requests Citing Articles Citing Articles via Google Scholar Google Scholar Articles by D’Journo, X.-B. Articles by Thomas, P. A. Search for Related Content PubMed PubMed Citation Articles by D’Journo, X.-B. Articles by Thomas, P. A. Related Collections Esophagus - cancer