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Ann Thorac Surg 1997;64:757-764
© 1997 The Society of Thoracic Surgeons

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Original Article: General Thoracic

Colon Interposition for Esophageal Replacement: Current Indications and Long-Term Function

Department of Thoracic Surgery, University of Marseille, Marseille, France

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
Background. In contrast to the use of the stomach as an esophageal substitute, the use of the colon is becoming uncommon.

Methods. From 1985 to 1995, 60 patients underwent colon interposition for esophageal cancer (n = 37), benign stricture (n = 13), iatrogenic fistula (n = 5), achalasia (n = 3), or necrosis of a previous substitute (n = 2). A long isoperistaltic conduit based on the left colonic artery could be used in 52 patients (86.7%). The surgical route used was through the esophageal bed in 38 patients (63.3%), under the sternum in 21 patients, and under the skin in 1 patient.

Results. Colon interposition represented 18.5% of all operations performed for esophageal substitution during the study period. The choice of the colon resulted from an inadequate stomach in 33 cases (55%). The operative mortality rate was 8.3%. Seven patients (13.5%) required dilation of the esophagocolonic anastomosis. At last follow-up, 34 patients (65.4%) had no difficulty eating. Multivariate analysis identified the conduit position in the posterior mediastinum as the sole independent predictor of a good functional result (p = 0.002).

Conclusions. Colon interposition for esophageal substitution, usually performed when the stomach is not available, provides satisfactory function when placed in the esophageal bed.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
See also page 764.

In 1911, Vuillet [1] and Kelling [2] independently described the anatomic and surgical bases for the use of the colon as an esophageal substitute. Three years later, Von Hacker [3] reported the first clinical success, and colon interposition became the technique of choice for several decades. Work by Akiyama and colleagues [4] that revealed the extraordinary plasticity and stretchability of the stomach, as well as the richness of its submucosal vasculature, challenged this dogma. Recently, technologic advances made in mechanical stapling have allowed the dramatic simplification of formerly time-consuming procedures of gastric lengthening [5]. As a result, gastric tubulization has received wide acceptance by most teams involved in esophageal surgery.

Our experience, grounded in more than 1,000 patients who have undergone an esophageal substitution procedure since 1966 [6], clearly illustrates this evolution; whereas 328 colon interpositions were done between 1975 and 1985 at our institution, only 60 were performed between 1985 and 1995. This change obviously reflects highly selective use of the colon as an esophageal substitute, and has led us to review our recent experience to identify the current indications for this procedure, and to determine what effect, if any, several variables have on its long-term alimentary comfort.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
Patients
Data from 60 consecutive patients who underwent colon interposition for esophageal replacement or bypass between January 1985 and May 1995 were reviewed. There were 12 women and 48 men ranging in age from 24 to 78 years (mean, 52 ± 12 years). Their indications for operation are listed in Table 1.

Nonmalignant esophageal diseases were the sequelae of caustic injury in 9 patients (including 2 patients who required emergency esophagectomy), peptic reflux in 3 patients (including 1 secondary to an Ivor Lewis operation for esophageal leiomyoma), and chronic mycosis in 1 patient. All these patients previously had undergone repeated dilations. Esophageal fistulas were secondary to miscellaneous causes: anastomotic leakage after completion gastrectomy with a Roux-en-Y loop for cancer, esotracheal fistula related to the implantation of a phonic prosthesis after laryngectomy for cancer, esotracheal fistula resulting from radiation therapy for adenoid cystic tracheal carcinoma (cylindroma), esophagobronchial fistula at the site of the intrathoracic anastomosis after an Ivor Lewis operation for esophageal cancer, and postirradiation esophagopleural fistula as a late complication of right completion pneumonectomy for lung cancer.

Failure of a previous esophageal substitute required subsequent colon interposition in 2 patients who had received a free cutaneous flap after circular pharyngectomy and laryngectomy for cancer (n = 1), and a gastric tube for restoring continuity after esogastrectomy for high-grade dysplasia developed on Barrett's esophagus (n = 1). Finally, 44 patients underwent esophageal replacement with previous (n = 6) or synchronous (n = 38) esophagectomy, whereas 16 patients underwent bypass operation.

	Methods

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
PREOPERATIVE EVALUATION OF THE COLON.
Preoperative evaluation of the colon was performed in patients aged 45 years or older to detect any inflammatory or tumoral colonic pathology, and included either a barium enema or colonoscopy. No patients underwent preoperative mesenteric arteriography. An endoscopic diagnosis was made and resection of adenomatous polyps was performed in 2 patients.

BOWEL PREPARATION.
In patients in whom oral feeding was still possible, bowel preparation consisted of 5 days of an appropriate diet, followed by oral mechanical cleansing and two mild water enemas the day before operation. Patients who were receiving total parenteral nutrition underwent solely repeated water enemas, the number of which was adapted to the aspect of the washing. All patients received perioperative antibioprophylaxis with metronidazole.

SURGICAL TECHNIQUE.
The surgical technique of choice was the long isoperistaltic colon interposition supplied by the left colonic vessels. Initially, almost the entire colon was freed from its congenital attachments and mobilized widely so that it could be placed outside the abdominal cavity for inspection of its vascular blood supply by palpation and transillumination of the mesentery (Fig 1). The left colonic artery was identified and chosen as the preferred pedicle for the transposed colonic segment. Thorough evaluation of the marginal vessels and the venous drainage is mandatory. After incising windows into the mesocolon to isolate the different vessels, atraumatic vascular clamps were placed on the base of the middle and right colonic arteries, and on the marginal artery at the end points of the proposed bowel transections. For the right bowel transection, the colonic segment was chosen voluntarily to be "too" long so as to preserve a generous safety margin at the upper end of the conduit. When blood flow was adequate, as ascertained by the presence of a pulsatile flow in the marginal artery, the clamped vessels were divided and tied. The colon was transected at its ascending part as well as at the splenic flexure using a mechanical stapler, and then was elevated to the neck through a tunnel created either behind the sternum or within the posterior mediastinum when the esophagus had been removed. It was positioned snugly, avoiding tension, twisting, or redundancy. The upper portion in excess of the elevated colon was resected, and the proximal anastomosis was performed using a hand-suturing single-layer technique. The musculomucosal layer of the esophagus and the seromuscular layer of the colon were approximated with 3-0 absorbable interrupted sutures to correct problems associated with discrepancy in lumen size. When the stomach was available, the distal anastomosis was performed at the posterior side of the gastric antrum (Fig 2A). A pyloroplasty was performed routinely, and a double-lumen gastric tube was inserted into the fundus through the colon transplant. In the absence of stomach, distal continuity of the alimentary tract was reestablished by colojejunostomy or coloduodenostomy (Fig 2B).

View larger version (74K): [in this window] [in a new window]   Fig 1. . Examination of the vascular supply by transillumination of the mesentery.

View larger version (97K): [in this window] [in a new window]   Fig 2. . Radiologic examination of the conduit with a water-soluble contrast medium. Isoperistaltic long-segment colic interposition. (A) Anastomosis of the distal colon to the posterior wall of the stomach (profile view). Note the straightness of the conduit along its substernal route and the absence of a siphon at the level of the cologastric anastomosis. (B) Colon interposition placed in the esophageal bed. Anastomosis of the distal colon to the duodenum (front view).

FUNCTIONAL ASSESSMENT.
Long-term results were investigated in 55 patients who survived operation, with 100% follow-up (mean, 20 months; maximum, 106 months). For the patients who survived the operation but had died by the time of the study, the functional result was assessed by review of outpatient records, with special reference to the presence of gastrointestinal symptoms and the need for repeated dilations, hospitalizations, or reoperations.

Patients who were alive at the time of the study were interviewed for the presence of foregut symptoms according to a standard questionnaire, similar to that given by Collard and associates [7] to patients who have undergone gastric interposition, which included the following questions: Do you complain of dysphagia? How many meals do you take per day? Are you disabled by arrhythmia, sweating, early thoracic or epigastric fullness or pain, regular regurgitations, heartburn, or false passages at or just after meals? Do you have diarrhea (more than three motions per day or liquid stools)? How high is your current body weight in reference to the weight you had after operation? Can you rate your current alimentary comfort, if your condition before you began having esophageal problems was rated as 10 points?

Finally, the patient's alimentary function was graded as good if the patient could eat without any gastrointestinal symptoms, fair if the patient complained occasionally (less than two times per week) of at least one of the major disabling symptoms (dysphagia, regurgitation, or vomiting), and poor if the patient had more frequent complaints.

STATISTICS.
Survival information was obtained by correspondence with the patient, his or her family or referring physician, and the city hall registry. The probability of survival with its confidence interval of patients with cancer was estimated using the product-limited method of Kaplan and Meier from the date of the operation, and included the operative mortality.

Univariately, ² (log likelihood ratio) tests were used for weighting each variable potentially correlated with the functional result of the operation. Multivariately, the full-step logistic regression model was used to assess simultaneously the impact of these factors on alimentary comfort. Liberal criteria (p of entry <0.40) were used for variable inclusion. The SAS statistical package (Statistical Analysis System Institute, Cary, NC) was used for all analyses. Statistical significance was accepted as a p value less than 0.05.

	Results

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
Choice of the Colon
During the study period, 265 operations using the stomach were performed, so that use of the colon represented only 18.5% of all esophageal replacement interventions. Colon interposition was performed in 33 patients because of inability to use the stomach (55%) as a result of a previous (n = 7) or synchronous gastric resection (n = 20), the presence of a dense peritoneal fusion in the submesocolic area as a consequence of prior operations (n = 4), the presence of a nonresectable tumor of the gastroesophageal junction (n = 1), or an unfavorable anatomic conformation (n = 1). In 17 patients (28.3%), the need to replace the entire esophagus together with the pharynx dictated the use of a long colon conduit. The colon was the conduit of choice in 10 patients (16.7%). Reasons included the presence of a benign disease in 8 patients with a substantial life expectancy (undilatable caustic [n = 4] or peptic stricture [n = 1], and megaesophagus [n = 3]), and the need for a bypass operation to maintain the esophageal drainage into the stomach in 2 patients (radical esopleural fistula after right pneumonectomy for bronchial carcinoma [n = 1], and esotracheal fistula after radiation for tracheal cylindroma [n = 1]).

	Type of Colon Transplant

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
Performance of the colon interposition always was technically possible, although the preoperative strategy had to be changed during the operation in a few cases. The left colon was used in 53 patients (88.3%) and the right colon was used in 7 patients (11.7%). The blood supply was ensured by the left colonic artery in 52 patients, the middle colonic artery in 3, the right colonic artery in 3, the pelvic colonic artery in 1, and the ileocolonic artery in 1. Reasons that led the surgeon to choose blood supply other than the left colonic artery were its absence in 3 patients (5%), the absence of a marginal artery or its accidental transection on the occasion of a previous operation in 3 patients (5%), the presence of an aortic aneurysm with thrombosis of the inferior mesenteric artery in 1 patient (1.7%), and an unfavorable anatomy with impaction of the splenic flexure in the hypochon-drium as a consequence of a previous operation in 1 patient.

An anisoperistaltic colon interposition had to be performed in 4 patients (6.7%) because of some of the vascular problems mentioned previously. The transplant was placed in the esophageal bed in 38 patients (63.3%), below the sternum in 21 patients (35%), and in front of the sternum in 1 patient with a very compromised status.

The surgical approaches used were a combined laparotomy and left cervicotomy in 42 cases (70%); a right thoracotomy, laparotomy, and cervicotomy in 10 cases (16.7%); and a combined abdominal and thoracic approach in 8 cases (13.3%). The esocolic anastomosis was located in the neck in 52 patients (86.7%) and in the thorax in 8 patients (13.3%); it was placed at the level of the lower pulmonary vein in 5 patients, and at the top of the thorax in 3 patients. The anastomosis was performed using a hand-suturing technique in 55 patients (91.7%) and mechanical staplers in 5 (8.3%). In the absence of stomach, distal continuity of the alimentary tract was reestablished by end-to-end coloduodenostomy in 6 patients and by end-to-side colojejunostomy in 16 (en- loop in 11 cases, Roux-en-Y loop in 5 cases).

	Associated Procedures

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
An esophagectomy was performed in 38 patients for cancer (n = 31), caustic (n = 3) or mycotic (n = 1) strictures, or megaesophagus (n = 3). A total (n = 15) or partial (n = 5) gastrectomy was performed in 20 patients. A laryngectomy was undertaken in 13 patients at the same operative session.

	Operative Mortality

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
There were five postoperative deaths (8.3%) that occurred between days 7 and 77. The clinical features of the patients who died are given in Table 2. The last 3 cases responded to special situations requiring a salvage operation. Among patients who underwent elective operations, the operative mortality rate was 3.5%.

	Postoperative Complications

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

Anastomotic fistulas occurred in 6 cases; 2 were occult and diagnosed only at x-ray examination, whereas 4 patients had clinical evidence of leakage. Among the latter, 3 patients were treated with cervical debridement at the bedside, but 1 necessitated reoperation because of significant disruption of the anastomosis. None had a fatal outcome.

Among the 3 patients who had a colon necrosis, 1 never had further esophageal replacement because of early cancer recurrence, 1 successfully underwent a free jejunal graft 2 months later, and the remaining patient benefited from a right ileocolic esophagoplasty 8 months later.

	Survival

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
At last follow-up, of the 55 patients who survived the operation, 25 patients were alive and 30 were dead. For the 37 patients with esophageal cancer, the probability of survival was 43.6% (95% confidence interval, 26.5% to 60.6%) at 1 year, 22.2% (95% confidence interval, 7.1% to 37.2%) at 2 years, and 9% (95% confidence interval, 0% to 20.1%) at 5 years. There were 2 deaths unrelated to cancer in this group of patients. Among the 23 remaining patients, 3 died of miscellaneous causes, including other organ cancer (n = 1), suicide (n = 1), and pneumonitis (n = 1).

	Functional Results

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
NUMBER OF DEATHS AT LAST FOLLOW-UP.
Among the 30 patients who died during follow-up, 3 experienced postoperative necrosis of their initial colon interposition and were excluded from the functional study. At a median follow-up of 9 months, 2 patients (7.4%) required dilation of a nonmalignant stricture of their proximal anastomosis. Alimentary function was scored as good in 18 patients (66.7%) and as fair in 5 patients (18.5%) who underwent a pharyngolaryngectomy and who complained of regular regurgitation through the nose at swallowing. Alimentary function was poor in 4 patients (14.8%). In 1 case, alimentary dysfunction was related to chewing impairment resulting from high-dose radiation therapy rather than to the colon interposition itself. Functional impairment and cause of death were linked in 3 patients: chronic aspiration pneumonitis after anisoperistaltic colon interposition, instrumental perforation after endoscopic dilation of the proximal anastomosis, and suicide in 1 psychotic patient who refused repeated dilations.

NUMBER OF SURVIVORS AT LAST FOLLOW-UP.
At a median follow-up of 17 months, 5 (20%) of the 25 patients who were still living had required at least one dilation of the esophagocolonic anastomosis and 1 further patient had experienced one episode of alimentary blockade treated by endoscopic removal of the foreign body. Two patients complained of major swallowing impairment related to a laryngeal caustic burn; 1 underwent a laryngectomy and the other required a feeding jejunostomy. Follow-up body weight, as compared with the body weight immediately after operation, was unchanged or increased in all patients. Disabling residual symptoms are listed in Table 4. Alimentary function was scored as good in 16 patients (64%), fair in 8 patients (35%), and poor in 1 patient (4%). Finally, ratings given by the patients themselves regarding their alimentary comfort averaged 6.8 of 10 (±2) [2–10].

	Comment

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

Preoperative evaluation of the colon is necessary when the patient is at risk for associated colonic pathology such as chronic ischemia, cancer, or diverticulosis. Colonoscopy allows for the evaluation of mucosal trophicity in patients with atherosclerosis, and the opportunity to biopsy and treat unsuspected lesions, as in 2 of our patients. None of our patients underwent preoperative mesenteric arteriography. The routine use of this invasive technique, as advocated previously [12], seems somewhat excessive, because anatomic variations in the colonic vasculature rarely modify the planned operative procedure dramatically. However, elective indications remain when the patient complains of lower extremity claudication or presents with an aortic aneurysm. Another indication is a history of a previous abdominal operation during which major colonic vessels or the marginal artery may have been injured or ligated. This information is of paramount importance in patients in whom a long conduit and anastomosis at the neck are required. One of our patients illustrates this situation: resection of the marginal artery at a previous completion gastrectomy led to the performance of a short-segment interposition, which fortunately was sufficient in this case.

The most disastrous complication is necrosis of the colon. Because anatomic variations in the number, size, and distribution of the colonic arteries are the rule, meticulous dissection and extensive mobilization of the colon is required with the guidance of transillumination of the mesentery, palpation of pulsatile flow in the vessels, or intraoperative Doppler examination, when necessary, particularly in patients with a fatty mesentery [13]. Our preference for a left colonic segment lies in the near-invariability of the left colonic artery (which has been present in 95% of cases in our experience), in contrast to the vascular pattern of the right side of the colon [14]; the better plasticity of its mesocolon; and its smaller lumen. Other vessels to be divided and ligated, particularly the midcolonic artery, should be isolated from their outset to supply the marginal artery through their first branches of division. After selection of the segment of bowel for interposition, we leave bulldog clamps in place for a minimum of 10 minutes before ligation. This practice allowed us to identify a case of thrombosis of the inferior mesenteric artery in which pulsatile beats were due to counterflow originating from the superior mesenteric artery. Obviously, adequacy of the blood supply also is ensured by bleeding visualized at the edges of the colonic segment after transection. When the colon is elevated into the thorax, constant checking of the position of the vessels is required, because minimal twisting that does not impede the arterial supply may represent a significant obstacle to the venous flow, which is thought to be the usual precipitating event for necrosis [15].

In our study, the mortality rate for colon interposition ranged from 4% to 10% and the morbidity rate ranged from 25% to 65% (Table 6). Death occurred mainly in those patients who had severe problems requiring a salvage operation. Although it usually is devastating, ischemic colonic necrosis was managed successfully in all cases with early diagnosis and prompt removal. In these situations, however, the restoration of enteric continuity is a major challenge when neither the remaining colon nor the stomach is available for reconstruction, as in 1 of our patients, in whom a free jejunal transfer was used in a fashion similar to that reported by Carlson and colleagues [18]. In contrast, we never had to deal with subacute colic ischemia as demonstrated by delayed long narrowing of the transplant with foci of necrosis, as described by Cheng and associates [19]. In accordance with the literature, postoperative morbidity mainly consisted of anastomotic leaks, pulmonary complications, and sepsis.

In our experience, the treatment of caustic injuries was not satisfactory, as shown by the occurrence of anastomotic stricture in 3 patients, the presence of swallowing difficulty resulting from laryngeal burns in 2 patients, the loss of capacity of the gastric reservoir in 5 patients, and major psychological problems leading to suicide in 1 patient. However, this was not identified by our statistical analysis to be a predictor of a poor functional result, probably because of the small sample size. Indeed, the multifocality of the injuries to the upper alimentary tract and their frequent association with laryngeal burns, the high incidence of anastomotic stenoses that are difficult to treat and often recur, and the psychotic patient profile are well-known characteristics of this condition [20, 21]. The functional importance of placing the conduit in the esophageal bed, added to the risk of malignant degeneration within the scarred esophagus in patients with repeatedly dilated caustic strictures [22], leads us to favor resection over bypass in this subset of patients.

In conclusion, the choice of the colon as an esophageal substitute results primarily from the unavailability of the stomach. Nevertheless, the colon provides durable and satisfactory alimentary comfort, with an acceptable operative risk in selected cases. The strongest predictor of a good functional result is placement of the conduit in the esophageal bed. Our findings suggest that (1) we should expand the use of colon interposition in patients with a substantial life expectancy, and (2) we should remove, whenever possible, nonmalignant strictures to avoid bypass operations and to place the conduit in the posterior mediastinum.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 
Presented at the Thirty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Feb 3-5, 1997.

Address reprint requests to Dr Thomas, Service de Chirurgie Thoracique et des Maladies de l'Oesophage, Hôpital Sainte Marguerite, 270 Bd Sainte Marguerite, F13274 Marseille, Cedex 9, France

	References

Top Footnotes Abstract Introduction Patients and Methods Methods Results Type of Colon Transplant Associated Procedures Operative Mortality Postoperative Complications Survival Functional Results Comment References

 

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This Article Abstract 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): Pascal Thomas Pierre Fuentes Roger Giudicelli Eugène Reboud Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Thomas, P. Articles by Reboud, E. Search for Related Content PubMed PubMed Citation Articles by Thomas, P. Articles by Reboud, E. Related Collections Related Article