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Eur J Cardiothorac Surg 2000;17:702-709
© 2000 Elsevier Science NL

Esophagectomy and staged reconstruction

^a Department of Thoracic and Cardiovascular Surgery, The Center for Swallowing and Esophageal Disorders, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195-5066, USA
^b Department of Biostatistics and Epidemiology, The Cleveland Clinic Foundation, Cleveland, OH, USA

Corresponding author. Tel.: +1-216-444-1921; fax: +1-216-445-6876
e-mail: ricet{at}ccf.org

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Variables considered... References

 
Objective: Esophageal resection with diversion and staged reconstruction of the upper gastrointestinal (GI) tract is an option in the management of complex problems. This study characterizes circumstances, indications, outcomes and their predictors for staged reconstruction, and estimates the optimal timing for reconstruction. Methods: Between October 1981 and March 1999, 43 patients were identified with planned staged reconstruction. Twenty-six had esophageal cancer, and 17 had complications of benign disease. Primary diversion with esophageal resection was needed in 16 patients, and secondary diversion with takedown of previous esophageal reconstruction was needed in 27. Common indications were failed esophageal anastomosis and esophageal perforation. Death before and death after reconstruction were considered as competing risks. Multivariable analyses were used to estimate the optimal timing of reconstruction. Results: The survival was 75, 21 and 9% at 3 months, 5 and 10 years, with survival only somewhat better (P=0.06) among patients having benign versus malignant disease. A similar proportion of patients died before reconstruction as underwent reconstruction, resulting in only 17 reconstructions, typically 9 months after diversion. The risk factors for death included cancer and primary diversion. The survival was best for benign disease when reconstruction was early. The survival was poor after reconstruction in the few patients with malignant disease. Conclusions: Patients requiring staged esophageal reconstruction are heterogeneous, with malignant or benign disease, and primary or secondary diversion. The outcome is poor, and is influenced by the pathology and timing of diversion. Patients with benign disease should be reconstructed as early as feasible; reconstruction is rarely indicated for patients with cancer.

Key Words: Esophagectomy • Esophagostomy • Esophageal diversion • Esophageal perforation

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Variables considered... References

 
Esophagectomy almost always implies reconstruction of the upper gastrointestinal (GI) tract, following excision of the esophagus. Typically, this occurs immediately following excision of the esophagus as part of the operation (esophagectomy and reconstruction). However, on occasion, immediate reconstruction is not feasible because of complex problems, and is planned for a later date (staged reconstruction). The purposes of this study were to: (1), characterize the population; (2), define indications; (3), assess the outcome; (4), identify predictors of the outcome; and (5), estimate the optimal timing for the reconstruction of patients undergoing esophagectomy and staged reconstruction.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Variables considered... References

 
2.1. Characterization of the population
From our prospective database of patients undergoing esophageal surgery at The Cleveland Clinic Foundation, our pathology database and our tumor registry, 43 patients were identified who were managed by planned staged esophageal reconstruction between 1 October 1981 and 1 March 1999.

Of the 43 patients, 25 (58%) were men. The age ranged from 37 to 90 years (mean±SD, 62±12 years; median, 65 years). The primary esophageal pathology was diverse and included one or more of the following: esophageal cancer (26 patients), gastro-esophageal reflux disease (GERD; 16 patients), spontaneous perforation (three patients), end-stage achalasia (two patients), caustic stricture (two patients), Barrett's ulcer (two patients), and/or primary esophago-bronchial fistula (one patient). The esophageal cancer was early-stage (pathologic stage, 0–II) in 14 patients, and late-stage (pathologic stage, III–IV) in 12. Other non-esophageal cancers in the 43 patients were colon cancer in three, and in one patient each, cancer of the lung, larynx, breast and mediastinum. Associated GI conditions included peptic ulcer disease in eight patients (19%), diverticulosis or diverticulitis in four (15%), cirrhosis in two (5%), paraesophageal hernia in one (2%), and Zollinger–Ellison syndrome in one (2%).

After resection of the esophagus or takedown of the failed anastomosis, an end-cervical-esophagostomy was fashioned at the lower end of a left neck incision. When possible, the esophagogastric junction was transected and the full stomach preserved. However, with failed anastomoses, any necrotic gastric tissue was excised. A Stamm gastrostomy was constructed in the mid-gastric body and this was sutured to the anterior abdominal wall in the left upper quadrant. The gastrostomy tube was used for alimentation after recovery from the diversion and before reconstruction. This allowed patients to be discharged before reconstruction.

The timing of this diversion was either primary or secondary. In 16 patients, primary esophagectomy and esophagostomy were performed with the intent of later reconstruction. In 27 patients, a secondary esophagostomy was performed after prior esophagectomy and reconstruction. This required takedown of the prior reconstruction with the intent of later reconstruction. The time interval between prior esophagectomy and the secondary esophagostomy ranged from 1 day to 13.8 years, with a median 2.4 months, with 25% at 11 days or less and 25% at 1.2 years or more.

Reconstruction in 17 patients used the colon in 12 and the stomach in five. Colon reconstructions were left in six patients and right in six. The blood supply in colonic grafts was the middle colic in nine patients, the left colic in two, and the facial artery via microsurgical free vascular graft anastomosis in one. Sixteen proximal anastomoses were performed in the neck and one in the chest. Of the 12 colonic distal anastomoses, four were Roux-en-y colojejunostomy and eight were cologastric. Fourteen conduits were placed in a substernal tunnel, two in a subcutaneous tunnel and one in the posterior mediastinum.

2.2. Indications and presentation
The indication for staged reconstruction was related to the anastomotic site of a previous reconstruction in 22 patients; early anastomotic failure in 13 patients, anastomotic fistula in eight and anastomotic recurrence in one. For the remaining 21 patients, perforation was the indication in 14 (iatrogenic in nine, spontaneous in three and perforated ulcer in two), Barrett's ulcer in stomach grafts in two, intraoperative complications in four and graft dysfunction in one patient.

The indications and pathology presentations for primary diversion and staged reconstruction in 16 patients are presented in Table 1, and those for secondary diversion and staged reconstruction in 27 patients are presented in Table 2.

Patient status was determined from clinical records and by telephone interview during the second quarter of 1999. All patients but one were traced. This one exception was alive and contacted in 1996, 2 years after esophagostomy for benign disease and reconstruction one month later. The study group has been followed for a total of 78 patient-years. The median follow-up for survivors was 1.8 years, and maximum survival was 10 years. Three have survived more than 5 years.

Patients alive after reconstruction completed a questionnaire to define GI function. Symptom scores of 0 (absent), 1 (mild), 2 (moderate), 3 (severe) and 4 (incapacitating) were used at the time of follow-up to assess abnormal GI function, as described by dysphagia, regurgitation and acid reflux. The procedures required to treat these symptoms were recorded. Dietary restrictions were also recorded. Patients were asked if they would undergo reconstruction again. Complete symptom follow-up was obtained before death in ten of 17 reconstructed patients (only one living patient after reconstruction could not be contacted).

Non-parametric estimates of freedom from various time-related outcomes were estimated by the non-parametric method of Kaplan and Meier [1]. The instantaneous risk of events across time (the hazard function) was estimated using a parametric method that resolved the number of hazard phases, identified the shape of the hazard function and estimated its parameters [2].

2.4. Identification of the predictors of outcome
Preliminary exploration of the association of variables with respect to each event included Chi-square testing of frequency and the Student's t-test for continuous variables. Correlations were sought between variables. Life tables, stratified by categorical variables, were explored. The calibration of continuous and naturally ordered variables to each event was achieved by the appropriate transformation of scale, with the aid of decile risk analyses.

2.4.1. Multivariable analyses
Potential risk factors (variables) were entered into the various analyses (Appendix A). Because of the high probability of model over-determination from the small sample size and low number of events, those variables for which three or fewer events were associated were eliminated for each analysis. A directed technique of the stepwise entry of variables into the multivariable risk factor models was then used [3]. This was supplemented for each model by bootstrap resampling, whereby 1000 random samples of the data were drawn with replacement, and an automated forward stepwise analysis was performed with a P-value criterion of 0.05 for retaining variables. The relative frequency of occurrence of variables in these 1000 models for each endpoint was used to inform the final selection of variables [4]. The P-value criterion for the retention of variables in the final models was 0.1. Regression coefficients are presented plus or minus one standard error.

2.4.2. Competing risks analysis
Proper interpretation of the data required simultaneous consideration of reconstruction and death before reconstruction as competing risks. The competing risks analysis was of three mutually exclusive, time-related outcomes: (1), alive without reconstruction; (2), death before reconstruction; and (3), reconstruction [5,6]. The common time interval to each event was the time to the earliest event, or censoring alive without reconstruction. Non-parametric competing risk estimates employed the generalized Kaplan–Meier multi-decrement method. Parametric competing risk estimates were obtained using the hazard function for death before reconstruction and reconstruction, and then performing numerical integration of the effects of these acting simultaneously across time on those alive without reconstruction. Risk-adjusted, parametric competing risk estimates utilized the multivariable hazard function equations from the above analyses, solved for a specific set of values for variables and integrated numerically across time.

2.5. Optimal timing of reconstruction
To determine the optimal time for reconstruction, the multivariable equations for death before and after reconstruction were applied across a continuous spectrum of times to reconstruction, ranging from 0 to 2 years. Survival initially followed the curve for death before reconstruction until the moment of reconstruction, and then it followed the curve for survival after reconstruction. The impact of the timing of reconstruction was assessed by integrating the area under the survival curve from esophagostomy to 10 years, thereby obtaining the total number of years of lifetime accumulated within this 10-year time frame.

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Variables considered... References

 
3.1. Descriptive outcomes
3.1.1. Morbidity and mortality of diversion
Six patients died (14%) in-hospital after diversion. Twenty-eight percent of patients experienced respiratory failure (Table 3).

3.1.3. Reconstruction
Reconstruction has been achieved to date in 17 (40%) of the 43 patients. Two (12%) died in-hospital after reconstruction. The morbidity of the reconstruction is detailed in Table 5 which shows that half of the patients experienced anastomotic leaks.

Seven of the ten deaths after reconstruction were in patients with esophageal cancer. Two of the seven died in-hospital after reconstruction due to a cologastric anastomosis leak in one patient that resulted in abscess and sepsis, and devascularization of the native right colon in the other patient that resulted in necrosis with abscess and sepsis. Four patients died of cancer progression; one patient died from sepsis, secondary to recurrent anastomotic complications.

Of the ten patients dying after reconstruction, three had primary diversions. Of these three patients, one died from metastatic prostate cancer, one of failure to thrive and one of early aspiration. The remaining seven patients had secondary diversion; two died in-hospital, four died of cancer and one died of anastomotic complications.

Of 15 patients surviving reconstruction, five had no anastomotic stricture, seven had strictures requiring five or fewer dilations, and three had resistant strictures requiring up to 15 dilations.

Reoperation after reconstruction was required in six patients. Two patients had anastomotic fistula, for which one was diverted and later closed, and one had unsuccessful primary closure. Two patients had delayed proximal anastomoses until graft viability was demonstrated at 3 and 6 months post-reconstruction. Two patients developed abdominal complications that resulted in hospital deaths.

3.2. Time-related outcomes
3.2.1. Survival
The overall survival after esophagostomy was 75, 56, 42, 21 and 9% at 3 months and 1, 2, 5 and 10 years. It was somewhat better in patients with benign disease (84, 71, 60, 39 and 21% at 3 months and 1, 2, 5 and 10 years) than in those with malignant disease (70, 47, 30, 11 and 2% at 3 months and 1, 2, 5 and 10 years), P(logrank)=0.06, but similar before risk-adjustment for primary and secondary diversion, P=0.3. The overall survival before reconstruction was 77, 61, 52 and 42% at 3 months and 1, 2 and 3 years after diversion. The overall survival after reconstruction was 83, 57, 45, 41 and 39% at 3 months and 1, 2, 3 and 4 years after reconstruction. It was better in those with benign disease (93, 79, 70, 66 and 64% at 3 months and 1, 2, 3 and 4 years) than in those with malignant disease (71, 33, 19, 15 and 13% at 3 months and 1, 2, 3 and 4 years), P=0.03.

3.2.2. Reconstruction
Reconstruction was 19, 52 and 70% at 6 months and 1 and 2 years.

3.2.3. Competing risks of death and reconstruction
The rates of migration from the category of alive without reconstruction (sometimes termed as event-free survival) to: (1), reconstruction; or (2), death before reconstruction are shown in Fig. 1a. The rate of reconstruction peaked about 8 months after esophagostomy, falling rapidly over the next 2 years. In contrast, the risk of death before reconstruction was highest immediately after esophagostomy, fell to its lowest level about a year later, and then steadily rose. The net effect of these two competing rates on the percentage of patients in each category across time is depicted in a non-risk-adjusted fashion in Fig. 1b. At 1 year, approximately one-third of the patients were still awaiting reconstruction, one-third died before reconstruction and one-third were reconstructed.

View larger version (24K): [in this window] [in a new window]   Fig. 1. Competing risks of death and reconstruction after esophagostomy. (a) Transition rates from alive without reconstruction (hazard functions) to the two competing risks of reconstruction and death before reconstruction. (b) Percent of patients across time: (•), remaining alive without reconstruction; (), dying before reconstruction; and (), being reconstructed. The symbols represent non-parametric, so-called multiple decrement estimates, and the solid lines represent the parametric competing risks estimates from the transition rates of Fig. 1a. At all points across time, the sum of the percentage of patients in each category is 100%.

The risk factors for death before reconstruction included older age at esophagostomy, late-stage cancer, neoadjuvant chemoradiotherapy before esophagostomy, and primary diversion (Table 6). Patients presenting with empyema were at less risk of death before reconstruction.

No factors were associated with reconstruction.

The interplay between death before reconstruction and achieving reconstruction varied with the patient characteristics. Fig. 2a illustrates the competing risks in a 60-year-old patient with esophageal perforation and empyema with benign disease, for whom a primary diversion was performed. Such a patient has a low, but steadily rising risk of death before reconstruction, and a high likelihood of being reconstructed. In contrast, Fig. 2b illustrates the competing risks of another 60-year-old patient with late-stage cancer who received neoadjuvant chemoradiotherapy. Death before reconstruction dominates the risk and few patients like this survive to have reconstruction.

View larger version (20K): [in this window] [in a new window]   Fig. 2. Competing risks of death and reconstruction after esophagostomy for two different patient characteristics; (a), a 60-year-old patient with benign pathology, presenting with empyema, and undergoing a diversion operation and takedown of a previous reconstruction; (b), a 60-year-old patient with late-stage esophageal cancer, who had prior esophagectomy and reconstruction and neoadjuvant chemotherapy and radiotherapy.

Of six patients reconstructed with early cancer, three maintained or gained weight on an unrestricted oral diet, one required supplemental tube feedings and two died in-hospital. Of the three patients on oral diet, two had no dysphagia, regurgitation or heartburn, and one had mild heartburn. All would choose to undergo reconstruction again. Two patients with late-stage cancer tolerated an oral diet, but required supplemental tube feedings.

3.5. Optimal timing of reconstruction
Because of the small data-set, the inferences about optimal timing are hampered by wide confidence limits. However, for patients with benign disease, the survival is maximized if reconstruction is performed early (Fig. 3). The survival decreases with delay of reconstruction. In contrast, patients with esophageal carcinoma do best with late reconstruction (Fig. 3).

View larger version (15K): [in this window] [in a new window]   Fig. 3. The duration of survival in the next 10 years following esophagostomy for a patient with benign disease and one with malignant disease according to the timing of reconstruction. The various times of reconstruction are given along the horizontal axis.

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Variables considered... References

This strategy has been previously reported; however, these patients have been included only as a small part of a larger series of esophageal surgery without specific details or results [7–12]. Therefore, the patient characteristics, indications, results and optimum timing of reconstruction are not known. Although this surgical approach provides time to recover from complications, surgical trauma and comorbidities, the transient, but perhaps permanent inability to swallow is a significant, and sometimes prohibitive morbidity. With reluctance, we have considered and used this treatment option, but have had little information to guide these decisions. This series provides an insight into this surgical strategy and now directs our use of this procedure in complex problems.

As expected, these patients are a heterogeneous group. Patients with malignant esophageal disease and those who undergo diversion at the time of esophageal resection (primary diversion) are unlikely to benefit from this procedure, and will probably die without reconstruction. Although multiple complex problems may be managed by resection, diversion and delayed reconstruction, the majority of patients have either had an anastomotic complication following reconstruction, or delayed recognition, or severe complication of an esophageal perforation. The survival of patients is poor and there is significant morbidity and mortality, no doubt a reflection of the complexities that necessitate this drastic surgery. For patients with benign esophageal disease, reconstruction should be undertaken as soon as recovery allows. Patients with malignant esophageal disease usually succumb to recurrent or distant cancer, or complications of surgery. In these patients, reconstruction should be delayed until freedom from recurrent cancer can be assured; therefore, few patients will undergo reconstruction.

We continue to use resection and diversion in the management of complex problems when it is necessary to save a patient's life, and consider delayed reconstruction only when recovery is adequate and the patient will benefit from the restoration of GI continuity. However, patients are informed that although the intent is for staged reconstruction, the odds are that this goal will not be realized.

	Footnotes

 
Presented at the 13th Annual Meeting of the European Association for Cardio-thoracic Surgery, Glasgow, Scotland, UK, September 5–8, 1999.

	Appendix A. Variables considered in multivariable analyses

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Variables considered... References

 
Demography: age at esophagostomy, gender.

Previous esophageal procedures: hiatal hernia repair, Heller myotomy, dilation of stricture, previous perforation repair, previous esophageal reconstruction, interval between previous reconstruction and esophagostomy.

Presentation: empyema, dysphagia, pneumonia.

Esophageal carcinoma: location (upper or middle, lower), type (adenocarcinoma, squamous cell cancer), pathological stage, T status, N status, neoadjuvant chemoradiotherapy.

Other esophageal morbidity: GERD, GERD with stricture, GERD with Barrett's disease, GERD with Barrett's high-grade dysplasia, dysmotility, iatrogenic perforation, spontaneous perforation.

Other GI conditions: peptic ulcer disease, diverticulosis or diverticulitis, cholecystectomy.

Non-GI history and conditions: diabetes, smoking, hypertension, myocardial infarction, previous coronary revascularization, non-esophageal cancers.

Operative details: primary vs. secondary diversion, date of operation.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Variables considered... References

 

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12. Altorjay A., Kiss J., Voros A., Sziranyi E. The role of esophagectomy in the management of esophageal perforations. Ann Thorac Surg 1998;65:1433-1436.[Abstract/Free Full Text]

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