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Ann Thorac Surg 2007;83:1273-1278
© 2007 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Surgical Outcome of Colon Interposition by the Posterior Mediastinal Route for Thoracic Esophageal Cancer

Satoru Motoyama, MDa,b,*, Michihiko Kitamura, MDa,b, Reijiro Saito, MDa,b,c, Kiyotomi Maruyama, MDa,b, Yusuke Sato, MDa,b, Kaori Hayashi, MDa,b, Hajime Saito, MDa,b, Yoshihiro Minamiya, MDa,b, Jun-ichi Ogawa, MDa,b

a Department of Surgery, Akita University School of Medicine, Akita, Japan
b Department of Surgery, Iwate Prefectural Isawa Hospital, Mizusawa, Japan
c Department of Thoracic Surgery, Municipal Sakata Hospital, Sakata, Japan

Accepted for publication November 16, 2006.

* Address correspondence to Dr Motoyama, Department of Surgery, Akita University School of Medicine, 1-1-1 Hondo, Akita City 010-8543, Japan (Email: motoyama{at}doc.med.akita-u.ac.jp).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: For thoracic esophageal cancer patients with a history of gastrectomy, esophageal reconstruction using segments of colon was often accomplished using the anterior mediastinal route to avoid fatal complications related to colon necrosis. Our aim was to review our experience with reconstruction by the posterior mediastinal route and assess the surgical outcomes.

Methods: Between 1989 and August 2006, 34 esophageal cancer patients at Akita University Hospital underwent esophageal reconstruction accomplished by colon interposition by the posterior mediastinal route. Data from these patients were reviewed.

Results: Colon conduits consisted of left colon segments in 4 patients and right colon segments in 30. The grafts were supplied with blood by the left colonic artery in 13 patients, the middle colonic artery in 20, and the right colonic artery in 1. The esophagocolic (pharyngocolic) anastomosis was located in the neck in 33 patients (97%) and in the thorax in 1. No patient died during the initial hospital stay. There were no instances of colon necrosis. An anastomotic fistula occurred in 3 patients (9%). Proximal anastomotic strictures occurred in 2 patients (6%). No late graft redundancies resulting in significant dysphagia occurred. Reductions in body weight did not differ from those seen when the gastric tube was used for reconstruction, and alimentary function was good after surgery. The 1-, 2-, 3-, and 5-year survival rates were 66%, 52%, 48%, and 48%, respectively.

Conclusions: Colon interposition by the posterior mediastinal route provides a good outcome and is considered the route of first choice.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
The use of the stomach as an esophageal substitute after esophagectomy in cases of thoracic esophageal cancer has received wide acceptance by most surgeons around the world. The advantageous features of the stomach include its extraordinary plasticity and elasticity, as well as the richness of its submucosal vasculature [1]. But for thoracic esophageal cancer patients with a history of gastrectomy (for gastric cancer or ulcer) or for patients with cancer in both the esophagus and stomach, we usually reconstruct using long segments of colon transposed on a vascular pedicle. The first successful clinical use of the colon as an esophageal substitute was reported in 1914, after which colon interposition was the technique of choice for several decades [2, 3]. The advantageous features of the colon include its long length, acid resistance, and excellent blood supply. When compared with gastric pull-up, its disadvantages include the long operating time related to mobilization of the colon and the additional anastomosis, which increases surgical stress, and the frequency of late redundancy. Moreover, reconstruction by the subcutaneous route or retrosternal route is used in many hospitals because with the posterior mediastinal (orthopedics) route, anastomotic leakage or necrosis of the colon graft can lead to severe bacterial infection and septic events [4–7]. On the other hand, the posterior mediastinal route provides better long-term functional outcomes after surgery than the anterior mediastinal route [8–11].

The aims of the present study were to review our experiences with using the posterior mediastinal route and long colon pedicle for esophageal reconstruction in patients with thoracic esophageal cancer during a 17-year period and to assess the surgical outcomes.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
This retrospective study was reviewed and approved by our Institutional Review Board; individual patient consent was waived. Between 1989 and August 2006, 578 consecutive patients with thoracic esophageal cancer underwent right transthoracic esophagectomy with extensive lymph node dissection at Akita University Hospital. Of the 43 patients (7.4%) who underwent esophageal reconstruction using long-segment colon interposition, 34 (79%) were reconstructed by pulling up the colon by the posterior mediastinal route (orthopedics). Data from these 34 patients were studied. The remaining 9 patients underwent esophageal reconstruction by the anterior mediastinal route and were excluded from this study. In 2 of those patients, ischemic changes occurred in the interposited colons during the operation. We therefore changed the route of reconstruction from posterior to subcutaneous and performed a supercharge using microvascular surgery. Owing to direct invasion of the trachea or left main bronchus, 2 patients were treated with neoadjuvant chemoradiotherapy and after esophagectomy. We wrapped the fragile structures with a muscle flap using the latissimus dorsi muscle, and reconstructed by the retrosternal or subcutaneous route. In 2 patients, the operation had to be staged owing to liver cirrhosis, and the reconstruction was by the subcutaneous route. Two patients were reconstructed by the subcutaneous route owing to their generally poor condition, which included liver cirrhosis or severe anemia. One patient had multiple colon diverticula, so we reconstructed by the subcutaneous route to avoid diverticulitis in the mediastinum.

The patients studied included 32 men and 2 women, ranging in age from 43 to 75 years, with a mean of 62 (±7 SD). All were treated surgically for esophageal carcinoma. Three patients were treated with neoadjuvant chemoradiotherapy, and 1 patient was treated with neoadjuvant chemotherapy to address direct invasion (T4) of the trachea. The remaining 30 patients received surgery without preoperative treatment. Preoperative nutritional makers, including body mass index, serum total protein, serum albumin, and hemoglobin, were 19.9 ± 2.9, 6.7 ± 0.5 g/dL, 4.0 ± 0.3 g/dL, and 11.7 ± 1.5 g/dL (means ± SD), respectively.

The tumors were located in the cervical–upper thoracic esophagus in 6 patients, in the upper thoracic esophagus in 4 patients, in the middle thoracic esophagus in 20 patients, and in the lower thoracic esophagus in 2 patients (Table 1). Two patients had multiple esophageal cancers, the one with tumors in the upper and lower thoracic esophagus, the other with tumors in the middle and lower thoracic esophagus.


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  		Table 1 Patient Backgrounds
 
The reasons for using the colon for esophageal reconstruction were as follows. Eighteen patients had a history of gastrectomy for an earlier gastric cancer or gastric ulcer (5 total gastrectomies and 13 distal gastrectomies); 12 patients had a synchronous gastric cancer; 1 patient had a benign gastric tumor; and 3 patients wished to preserve the stomach (Table 2).


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  		Table 2 Reasons for Using the Colon
 
Preoperative evaluation of selective mesenteric angiography of the celiac axis, superior mesenteric artery, and inferior mesenteric artery was performed routinely from 1989 to 1996; thereafter, we did not do this evaluation routinely. A total colonoscopy or barium enema, or both, was performed routinely to rule out the presence of a colon tumor or inflammatory bowel disease. For patients for whom oral feeding was still possible, mechanical preparation of the colon consisted of a clear liquid diet for 1 day and an antegrade colonic lavage. Patients receiving total parenteral nutrition underwent repeated water enemas. Since 2003, all patients also received perioperative antibioprophylaxis with metronidazole.

After the thoracic surgical procedure, the colon was exposed using a laparotomy, usually with an upper midline approach. The retroperitoneal attachments of the colon were incised, freeing the transverse colon, splenic flexure, and descending colon for left colon grafts; or the terminal ileum, ascending colon, and transverse colon for right colon grafts. The colic arteries were identified in the mesentery by palpation and transillumination. For left colon grafts, the ascending branch of the left colic artery was isolated, and the main trunk of the middle colic artery was clamped to assess the adequacy of the circulation to the intervening colon. For right colon grafts, the main trunk of the middle colic artery was isolated, and the right branch of the middle colic artery or the right colic, or both, or ileocolic arteries, or both, were clamped in an analogous maneuver. The colon was then transected using a stapling device after determining the length of conduit needed. The conduit was then carefully transposed while wrapped in a vinyl sheet that surrounded the graft, which enabled transposition with minimal traction through the posterior mediastinum, avoiding entry into the pleural space.

Esophagocolic or pharyngocolic anastomosis was performed in an end-to-end fashion using two layers of interrupted suture or in an end-to side fashion using an autosuture device. Cologastric or coloduodenal anastomosis was performed end to end using two layers of suture material or side to end using an autosuture device. Finally, a colocolostomy or ileocolostomy was performed between the residual segments of colon using two layers of suture material or an autosuture device, and the mesocolic defect was closed. A feeding jejunostomy was routinely used to provide enteral nutrition postoperatively.

Thirty-three patients received curative (R0) surgery, whereas 1 patient showed metastasis in a mesenteric lymph node (R2). Lymph node metastasis was present in 16 patients (47%). The pathology stages of the cancers were stage I in 12 patients, stage IIA in 2 patients, stage IIB in 1 patient, stage III in 11 patients (including 2 clinical T4N0 stage III patients), and stage IV in 8 patients (including 2 clinical T4N1 stage IV patients; Table 1). We performed esophagectomy in all 8 stage IV patients. The 2 clinical stage IV (T4N1) patients were treated with neoadjuvant chemoradiotherapy and after esophagectomy. Five pathology stage IV patients had lymph node metastasis involving the neck, and we performed a three-field lymph node dissection. One patient had mesenteric lymph node metastasis, which was not diagnosed preoperatively. Eighteen patients received adjuvant chemotherapy consisting of 5-fluorouracil and cisplatin after surgery.

Operative mortality included the 30-day mortality as well as any later deaths that occurred during the initial postoperative hospital stay. The proximal esophagocolonic anastomosis was checked routinely by radiography with water-soluble contrast medium on postoperative day 8 or later. All fistulas were counted, regardless of whether there was clinical evidence of leakage. A diagnosis of pneumonia was made when there were abnormalities on a chest roentgenogram, and the patients were administered antibiotics.

Long-term results were investigated in all patients, with 100% follow-up (mean, 43 months; maximum, 139). As a general rule, patients visited the hospital monthly for at least 5 years after their surgery. When a patient reported a problem with swallowing, we performed a barium swallowing examination and checked for proximal or distal anastomotic stricture, or late redundancy of the colon graft. Anastomotic stricture was defined based on the necessity for balloon dilation.

Body weight changes and duration of enteral nutrition through the jejunostomy were determined. Since 2000, 9 patients have survived more than 12 months after receiving esophagectomy and esophageal reconstruction using a colon graft by the posterior mediastinal route. The body weights of those 9 patients were compared with those of the 98 patients who were reconstructed using stomach pull-up by the posterior mediastinal route during the same period (from 2000 to 2004). In addition, the alimentary function of the same 9 patients was graded as good if they could eat without any gastrointestinal symptoms, fair if the patient complained occasionally (less than two times a week) of at least one major disabling symptom (dysphasia, regurgitation, or vomiting), and poor if the patient had more frequent complaints [8].

Categorical data were compared using the {chi}2 test, and continuous data were compared using the Mann-Whitney U test. Survival rates were estimated using the Kaplan-Meier method (Stat View J-5.0; Abacus Concepts, Berkeley, California). Values of p less than 0.05 were considered significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
The operations took an average of 723 ± 132 minutes, and blood losses averaged 1,056 ± 621 mL (means ± SD). The colon conduits were transposed by the posterior mediastinal route and consisted of left colon segments (transverse-descending colon) in 4 cases and right colon segments in 30 cases (25 ascending-transverse colons, 2 cecum-transverse colons, 3 ileum-transverse colons; Table 3, Fig 1). In only 2 cases, both right colon conduits, was augmentation of the distal arterial supply using a microvascular anastomosis to the cervical artery required. No anisoperistaltic colon interposition had to be performed. Blood was supplied to the grafted colon by the left colonic artery in 13 patients, the middle colonic artery in 20 patients (right branch in 10 and left branch in 10 patients), and the right colonic artery in 1 patient (Table 3). The esophagocolic (pharyngocolic) anastomosis was located in the neck in 33 patients (97%) and in the thorax (at the level of the bottom of the aortic arch) in 1 patient (3%). Among the 33 patients with an anastomosis in their neck, 3 had an esophagoileac anastomosis. The anastomosis was performed using a hand-suturing technique in 31 patients (91%) and a mechanical stapler in 3 (9%). The distal continuity of the alimentary tract was the residual stomach in 8 patients, the whole stomach (preservation) in 3, the duodenum in 17, and the jejunum in 6.


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  		Table 3 Reconstruction Using Colon
 

Figure 1
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  		Fig 1. Photographs taken during barium swallowing examinations of patients who were reconstructed using (A) the ascending-transverse colon or (B) the ileum-transverse colon by the posterior mediastinal route.

 
None of the patients died during their initial hospital stay (Table 4). Colon necrosis did not occur in anyone. An anastomotic fistula occurred in 3 patients (9%), but healed with conservative therapy; no second operations were necessary. Pneumonia was the most common acute complication, occurring in 7 patients (20%) still in hospital. Most of those became sick during adjuvant chemotherapy. Late complications occurring among the 34 patients included proximal anastomotic strictures in 2 patients (6%), both of whom improved after treatment consisting of a few balloon dilations. Distal anastomotic stenosis was seen in 1 patient (3%), who improved after treatment with balloon dilation. No late graft redundancy resulting in significant dysphasia was seen, and ileus was seen in 2 patients (6%).


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  		Table 4 Surgical Complications
 
Figure 2 shows that 3 months after surgery, the body weights of the 9 patients reconstructed using a colon graft by the posterior mediastinal route since 2000 had declined to 90% of their presurgical levels. By 12 months after surgery, the body weights in this group had recovered to 92% of their presurgical levels. There was no significant difference in the body weights of this group and those of the 98 patients reconstructed using the gastric tube during the same period (92% at 3 months, 90% at 12 months). Two patients (22%) required nutritional support though a parenteral tube for more than 12 months after esophageal reconstruction using colon, as compared with 14% requiring such nutritional support after reconstruction using the gastric tube. Again, there was no significant difference between the two methods of reconstruction (p = 0.6207). Alimentary function was scored as good in 7 patients (78%) and fair in 2 patients (22%) 3 months after surgery, and as good in 8 patients (89%) and fair in 1 patient (11%) 12 months after surgery.


Figure 2
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  		Fig 2. Comparison of the changes in body weight seen in esophageal cancer patients after esophageal reconstruction using colon (open squares) or stomach (open circles) by the posterior mediastinal route. Values are expressed as percentages of the body weights before surgery. There was no significant difference between the two groups. (Mo = months.)

 
At last follow-up (October 2006), 14 patients (41%) were alive and 20 (59%) were dead. The 1-, 2-, 3- and 5-year survival rates were 66%, 52%, 48%, and 48%, respectively (Fig 3). Thirteen patients died of their esophageal cancer, and 7 died of unrelated causes, which included 5 deaths due to other malignancies (2 laryngeal cancer, 1 gastric cancer, 1 prostate cancer, 1 malignant lymphoma), 1 due to suicide, and 1 due to pulmonary dysfunction.


Figure 3
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  		Fig 3. Five-year overall survival rate among thoracic esophageal cancer patients after esophageal reconstruction using colon by the posterior mediastinal route.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
We have shown that long-segment colon interposition by the posterior mediastinal route can be performed with no operative mortality and at low risk. In our series, there were no instances of colon necrosis, a 9% incidence of anastomotic leakages, which were cured without surgical treatment, no late redundancy, and good late alimentary function. Thus, colon interposition by the posterior mediastinal route provides good outcomes that compare favorably with esophageal reconstruction by other routes [4–9, 12–16].

The clinical decision making in the treatment of esophageal cancers is a process of balancing the risk of treatment against the potential benefits gained in terms of survival and quality of life. Ideally, colon conduits should have a length adequate to reach the cervical esophagus and a reliable blood supply, and should allow good swallowing function. The use of colon interposition is safe in high volume centers; however, surgical problems such as anastomotic leakage and septic events due to colon necrosis have been common [4–9, 12–16]. For that reason, many surgeons elect to use a retrosternal or subcutaneous route [4–7]. When anastomotic leakage occurs after use of the posterior mediastinal route, the resultant abscess can extend to the mediastinum and lead to severe mediastinitis, which sometimes necessitates placement of drains. If colon necrosis occurs, the patient can fall into a septic state and require a second operation. Bearing that in mind, we favor placement of the conduit in the esophageal bed when using the posterior mediastinal route because it is a shorter and more direct route that avoids tension or redundancy of the transplant. Furthermore, better function of the alimentary tract is obtained with this approach than with others [8, 9].

Because anastomotic leakage is most often the result of an inadequate blood supply to the conduit, selection of the feeding artery and drainage vein for the colon graft is very important. We favor using a right colon graft fed by the middle colic artery, even though the left colon is favored by many surgeons. There is a deficiency in the vascular network in the region of the colon between the ileocolic and right colic artery, and in the region between the middle colic and left colic arteries. Using a right colon graft supplied with blood by the middle colic artery enables us to avoid those regions [14, 15].

Evaluating the quality of the functional result over the long term is somewhat difficult. That is because it depends not only on the conduit, but also on the ability to chew and swallow, as well as on preservation of a gastric reservoir. Generally, colonic conduits are reported to have active peristalsis and to provide good long-term swallowing function. Patients also experience less reflux with colonic conduits even when reconstruction is by the posterior mediastinal route. This finding is noteworthy because long-term reflux has attendant pulmonary complications. For example, 1 of our thoracic esophageal cancer patients had a history of total gastrectomy and suffered from severe reflux that induced frequent pneumonia. We therefore employed an ileocecal–right colon graft to avoid reflux of duodenal juice. After the operation, the patient’s reflux disappeared completely.

One disadvantage of using the posterior mediastinal route for esophageal reconstruction is that it is difficult to treat a second primary cancer occurring in the grafted colon. In that regard, the incidence of second primary cancers is increasing and is becoming a major prognostic factor [17, 18]. We therefore perform annual endoscopic examinations to detect any cancer occurring in the reconstructed colonic graft.

Based on our findings, we conclude that when the stomach is not available, colon interposition by the posterior mediastinal route carries a low risk and provides good functional results in cases of thoracic esophageal cancer. We consider the posterior mediastinal route to be the route of first choice for esophageal reconstruction using colon conduits.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Akiyama H, Miyazono H, Tsurumaru M, Hashimoto C, Kawamura T. Use of the stomach as an esophageal substitute Ann Surg 1978;188:606-610.[Medline]
  2. Von Hacker V. Uber oesophagoplastik in allgemeinen under uber den ersatz der speiserohre durch antethorakle hautdickdarmschlauchbildung im besonderen Arch Klin Chir 1914;105:973-1018.
  3. May IA, Samson PC. Esophageal reconstruction and replacements Ann Thorac Surg 1969;7:249-277.[Medline]
  4. Wain JC, Wright CD, Kuo EY, et al. Long-segment colon interposition for acquired esophageal disease Ann Thorac Surg 1999;67:313-317.[Abstract/Free Full Text]
  5. Wada H, Doki Y, Nishioka K, et al. Clinical outcome of esophageal cancer patients with history of gastrectomy J Surg Oncol 2005;89:67-74.[Medline]
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  7. Cerfolio RJ, Allen MS, Deschamps C, Trastek VF, Pairolero PC. Esophageal replacement by colon interposition Ann Thorac Surg 1995;59:1382-1384.[Abstract/Free Full Text]
  8. Thomas P, Fuentes P, Giudicelli R, Reboud E. Colon interposition for esophageal replacement: current indications and long-term function Ann Thorac Surg 1997;64:757-764.[Abstract/Free Full Text]
  9. Cense HA, Visser MR, van Sandick JW, et al. Quality of life after colon interposition by necessity for esophageal cancer replacement J Surg Oncol 2004;88:32-38.[Medline]
  10. Gawad KA, Hosch SB, Bumann D, et al. How important is the route of reconstruction after esophagectomy: a prospective randomized study Am J Gastroenterol 1999;94:1490-1496.[Medline]
  11. Bartels H, Thorban S, Siewert JR. Anterior versus posterior reconstruction after transhiatal oesophagectomy: a randomized controlled trial Br J Surg 1993;80:1141-1144.[Medline]
  12. van Lanschot JJB, van Blankenstein M, Oei HY, Tilanus HW. Randomized comparison of prevertebral and retrosternal gastric tube reconstruction after resection of oesophageal carcinoma Br J Surg 1999;86:102-108.[Medline]
  13. DeMeester SR. Colon interposition following esophagectomy Dis Esophagus 2001;14:169-172.[Medline]
  14. Davis PA, Law S, Wong J. Colonic interposition after esophagectomy for cancer Arch Surg 2003;138:303-308.[Abstract/Free Full Text]
  15. Mansour KA, Bryan FC, Carlson GW. Bowel interposition for esophageal replacement: twenty-five–year experience Ann Thorac Surg 1997;64:752-756.[Abstract/Free Full Text]
  16. Furst H, Hartl WH, Lohe F, Schildberg FW. Colon interposition for esophageal replacement: an alternative technique based on the use of the right colon Ann Surg 2000;231:173-178.[Medline]
  17. Motoyama S, Saito R, Kitamura M, Ogawa J. Outcome of active surgery during intensive follow-up for second primary malignancy after esophagectomy for thoracic squamous cell esophageal carcinoma J Am Coll Surg 2003;197:914-920.[Medline]
  18. Sato Y, Motoyama S, Maruyama K, Okuyama M, Ogawa J. A second malignancy is the major cause of death among thoracic squamous cell esophageal cancer patients negative for lymph node involvement J Am Coll Surg 2005;201:188-193.[Medline]

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