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Colon Interposition for Staged Esophageal Reconstruction Andrew C. Chang, MD While the gastric conduit has been the method of choice for esophageal replacement for most surgeons, 1,2 the colon also is well-suited for use as an esophageal substitute. The colon s segmental vascular anatomy, supplied by the right colic, middle colic, and inferior mesenteric arteries, interconnected by the marginal artery of Drummond, allows for short or long interposition segments. Our practice has been to utilize the colon interposition conduit for esophageal reconstruction following esophagectomy with total gastrectomy for large Siewert type 2 or 3 carcinomas, laryngopharyngoesophagogastrectomy for cervical carcinomas, or in patients with esophageal discontinuity, having had, for example, a history of gastric necrosis requiring completion gastrectomy and end esophagostomy. 3 Colon interposition has been an option for esophageal replacement since its successful clinical introduction in 1911. 4,5 Advantages to using the colon as an esophageal substitute include its length and excellent blood supply. Functionally, patients with a colon interposition may have less regurgitation than those with a gastric conduit. When compared with the gastric conduit, relative disadvantages for colon interposition include longer operating time and increased technical complexity, as well as the long-term complication of graft redundancy. 6-8 The timing for reoperation is determined electively, once the patient has stabilized medically and nutritionally, typically at least 4 to 6 months following the initial operation. If the initial resection had been undertaken for esophageal or gastric malignancy, reevaluation for recurrent or metastatic disease is necessary before proceeding with major abdominal and thoracic reoperation. It is important to emphasize that the patient and/or family maintain patency of the end esophagostomy by frequent digital dilation during the interim between initial resection and planned reconstruction, to prevent stomal narrowing and stricture formation that would shorten the amount of esophagus available for re-anastomosis. Section of General Thoracic Surgery, University of Michigan Health System, Ann Arbor, Michigan. Address reprint requests to Andrew C. Chang, MD, Section of General Thoracic Surgery, University of Michigan Health System, TC2120G/5344, 1500 East Medical Center Drive, Ann Arbor, MI 48109. E-mail: andrwchg@umich.edu In addition to any necessary restaging studies, preoperative evaluation of the colon includes a barium enema particularly to determine whether the patient has extensive diverticular disease that would preclude use of that segment of colon for esophageal reconstruction. Since the mesenteric arcade will be evaluated for patency and continuity intraoperatively, our group does not perform mesenteric arteriogram routinely. Such preoperative imaging can be obtained for the patient with a history of tobacco use, or peripheral vascular disease, based on findings at preoperative physical examination. Before scheduling reoperation, patients are instructed that smoking cessation, regular exercise (ambulating 2 to 3 miles per day), and use of an incentive spirometer are absolute prerequisites. Nutrition is maintained via feeding tube, with monthly vitamin B12 replacement for patients with prior gastrectomy. Mechanical bowel preparation is recommended, and perioperative second-generation cephalosporin antibiotic prophylaxis is administered. Conduit Route In positioning an esophageal substitute for a cervical anastomosis, the posterior mediastinum (Fig. 1B) serves as the shortest and most direct route between the abdominal cavity and neck; the technique for this has been described previously. 9-11 In the reoperative setting, when the normal tissue planes in the posterior mediastinum have been obliterated following prior esophageal resection, retrosternal placement of the esophageal substitute (Fig. 1A) is our next preferred route. Retrosternal conduit placement also can be considered during esophageal resection for malignant disease if there is gross residual tumor (R2), for which postoperative radiation of the posterior mediastinal bed might be indicated, to limit radiation-induced injury to the esophageal substitute. 12 If the anterior mediastinum has been obliterated by prior cardiac surgery, particularly coronary artery bypass grafting, then a paramediastinal route can be utilized, either posterior or anterior to the pulmonary hilum. Operative Technique Abdominal Exploration Several questions should be addressed at initial exploration: whether the remnant stomach, if any, is adequate anatomi- 1522-2942/$-see front matter 2010 Elsevier Inc. All rights reserved. doi:10.1053/j.optechstcvs.2010.08.003 231

232 A.C. Chang Figure 1 Potential locations for the colon interposition conduit during esophageal reconstruction include: (A) retrosternal or anterior mediastinal; (B) posterior mediastinal or orthotopic. cally for use as an esophageal substitute or as the site for distal colonic anastomosis and whether the colon has continuity of its vascular arcade via the marginal artery of Drummond. The patient is positioned supine, with the head turned to the right and a shoulder roll placed posteriorly to extend the neck. An upper midline incision, extending several centimeters below the umbilicus, is made (Fig. 2). For patients who have had prior abdominal surgery, and for whom the stomach is still being considered as a possible conduit, dissection of adherent greater omentum from the abdominal wall must proceed with caution, to avoid injury to the greater curvature of the stomach and the right gastroepiploic artery. If the remnant stomach is of adequate length and has an intact right gastroepiploic arcade, then reconstruction can be performed with this conduit. Alternatively, the remnant can be used for the distal colonic anastomosis or completion gastrectomy can be performed. Our preference, to reduce biliary reflux or other complications arising from incomplete gastric emptying, is to perform completion gastrectomy with a roux-en-y distal colojejunostomy (Fig. 3). The greater omentum is divided from its adhesions to the transverse colon. In the setting of prior gastrectomy or gastric mobilization, if there is no residual right gastroepiploic arcade, the greater omentum should be amputated. The colon is mobilized from its lateral attachments, with care taken to preserve the mesenteric vessels within the mesocolon, which may have been distorted due to prior upper abdominal surgery (Fig. 4). Before proceeding further, once the middle and right colic arteries are identified, these should be occluded temporarily using small vascular clamps (Fig. 5A). Continuity of the collateral mesenteric vessels (marginal artery) is determined by palpation and Doppler flow probe interrogation of vasculature to the most proximal colon segment being considered for esophageal reconstruction (Fig. 5B).

Colon interposition for staged esophageal reconstruction 233 Figure 2 Surface anatomy and possible locations for placement of an end esophagostomy.

234 A.C. Chang Figure 3 Completed Roux-en-Y colojejunal anastomosis with feeding jejunostomy.

Colon interposition for staged esophageal reconstruction 235 Figure 4 Vascular supply to the colon with potential points of division for the interposition conduit. a. artery; v. vein.

236 A.C. Chang Figure 5 Assessment of the marginal artery. After serial occlusion of the middle colic vessels (A), a Doppler flow probe (B) is used to assess for pulsatile arterial flow within the marginal artery. Mobilization of the Esophagostomy The skin surrounding the cervical esophagostomy is incised circumferentially and the remnant cervical and upper thoracic esophagus is freed from its surrounding attachments along the prior subcutaneous tunnel (Fig. 6). A 32-French Maloney dilator is passed perorally and through the esophagostomy to aid this mobilization. To prevent compression of the colon interposition graft as it passes through the thoracic inlet, the left clavicular head, medial articulation of the first rib, and left half of the manubrium are resected (Fig. 7). An extrapleural dissection is undertaken to avoid injury/disruption of the underlying internal thoracic vessels. Patients should be forewarned that resection of the sternoclavicular joint can result in minor impairment of ipsilateral shoulder function. 13 The xiphoid process is resected and the underlying diaphragm is divided from its attachment to the xiphisternum. The retrosternal tunnel is created by gradual manual dissection, working from the abdominal and cervical incisions. Conduit length is estimated by laying an umbilical tape from the upper aspect of the abdominal incision to the base of the neck. The colon is divided distally at the level of the vascular pedicle, which will supply the conduit, and proximally at the appropriate length. A penrose drain is secured to the proximal end of the colon conduit at the antimesenteric taenia coli and used to guide the conduit. In this process, the conduit is introduced through the subxiphoid space and advanced gently without traction through the retrosternal tunnel.

Colon interposition for staged esophageal reconstruction 237 Figure 6 Mobilization of an anterior thoracic end esophagostomy (A), beginning with circumferential incision of the stoma (B) and mobilization of the remaining upper and cervical esophagus (C).

238 A.C. Chang Figure 7 Excision of the left sternoclavicular joint, including the posterior prominence of the clavicular head, opens the thoracic inlet and limits compression of the esophageal substitute as it passes through the anterior mediastinal or left paramediastinal space.

Colon interposition for staged esophageal reconstruction 239 Figure 8 Once the colon conduit is passed through the mediastinal space, any redundant colon is reduced gently back into the peritoneal cavity (A) to prevent kinking or twisting of the intrathoracic portion. The colojejunal anastomosis is performed first (B) to prevent any distension by mucosal secretions within the interposition conduit. The colojejunal anastomosis is placed in a retrocolic position (C).

240 A.C. Chang Figure 9 A Wützel feeding jejunostomy is placed in the afferent (biliary drainage) limb and passed across the jejunal anastomosis, to limit potential distal obstruction of the colojejunal anastomosis.

Colon interposition for staged esophageal reconstruction 241 Figure 10 A side-to-side semistapled esophagocolic anastomosis is completed. After (A) making a vertical colotomy, (B-C) 3-0 polyglycolic stay sutures are placed and a linear stapler is deployed, with the larger cartridge passed into the esophagus. (D-E) The remaining anterior hood of the esophagocolostomy is closed in two layers.

242 A.C. Chang Sequence of Abdominal Anastomoses Once the conduit is passed through the mediastinal tunnel, gentle traction is applied to reduce any redundancy in the intrathoracic colonic segment (Fig. 8A). The distal colon is divided, taking care to preserve the vascular arcade between the left colic artery and marginal artery to the colon conduit. A point of division is selected in the jejunum 30 to 40 cm distal to the ligament of Treitz, where the jejunum is cleared of its mesenteric attachments for 1 cm, to allow placement of a gastrointestinal stapler. If a prior feeding jejunostomy has been maintained for preoperative enteral nutrition, this site is excised and can be used as the point of division. To reduce conduit distension, the distal colo-jejunal anastomosis is performed first. The distal staple line of the colonic interposition conduit is excised and anastomosed in an end-to-side fashion to the distal (efferent) jejunal limb. Our preference is to perform a 2-layered hand-sewn anastomosis using a running 3-0 chromic catgut mucosal layer and interrupted 3-0 silk Lembert outer seromuscular layer (Fig. 8B). Distal colic continuity is then reestablished such that the colojejunal anastomosis remains in the retrocolic position (Fig. 8C). The afferent jejunal limb is then anastomosed side-to-side, 60 cm distal to the colo-jejunal anastomosis. Titanium clips are placed to mark the intra-abdominal anastomoses for subsequent radiographic localization. A new feeding jejunostomy is placed in the afferent limb, using a Wützel technique, and guided across the jejunal anastomosis to provide postoperative supplemental enteric nutrition (Fig. 9). We use a 14-French red rubber catheter into which additional side holes have been cut. We have found that such a catheter is readily available and is easier for the patient and caregivers to maintain, rather than the more pervasive smaller caliber needle jejunostomy catheters that more frequently develop occlusions or inadvertently can be removed. The abdominal wound is closed after completion of the cervical anastomosis, so that appropriate positioning of the nasal drainage tube can be confirmed and further redundancy of the interposition conduit can be corrected. Cervical Esophagocolic Anastomosis Our technique for a stapled side-to-side cervical esophagogastric anastomosis has been described in detail elsewhere and is readily adaptable for an esophagocolic anastomosis. Once the esophagostomy and remnant proximal esophagus have been mobilized, the epithelialized segment is excised. A vertical colotomy is made in the taenia coli opposite the mesentery (Fig. 10A). A linear stapler is positioned, with the larger cartridge limb placed in the esophageal lumen and the narrower anvil placed in the colon, oriented along the axis of the proximal esophagus pointed to the patient s right ear and closed (Fig. 10B-C). Using 3-0 polyglycolic suture, seromuscular Lembert tacking sutures are placed between the colon interposition conduit and the esophagus. After the stapler is deployed and removed, a 16-French naso- gastric sump drainage tube is placed and positioned such that the distal end crosses the distal conduit anastomosis. The anterior wall of the esophagocolic anastomosis is closed in 2 layers, using a running 4-0 absorbable monofilament suture for mucosal apposition and interrupted 4-0 absorbable monofilament Lembert sutures for closure of the outer seromuscular layer (Fig. 10D-E). Metallic clips are placed to mark the cervical anastomosis. A closed suction drain is placed adjacent to the cervical esophagocolic anastomosis. Conclusions Intraoperative or perioperative use of alpha-agonists should be avoided, particularly if the patient is hypovolemic, to limit splanchnic vasoconstriction that would place not only the esophagocolic anastomosis but the entire colon interposition conduit at risk for ischemic complications, particularly conduit necrosis. 14 Other postoperative complications include wound infection, anastomotic leak or stricture, recurrent laryngeal nerve palsy, pneumonia, atrial dysrhythmia, intra-abdominal abscess, and abdominal fascial dehiscence. Nasogastric tube drainage is maintained for 7 days postoperatively, followed by a barium esophagogram to assess for anastomotic leak or distal obstruction. If no anastomotic leak is detected, both the nasogastric tube and the cervical drain are removed. Early patient ambulation and frequent use of an incentive spirometer are encouraged. Esophageal reconstruction using the colon interposition, particularly for the patient in discontinuity, is a challenging operation, for which preoperative patient education and assessment with appropriate rehabilitation and conditioning are essential. References 1. Motoyama S, Kitamura M, Saito R, et al: Surgical outcome of colon interposition by the posterior mediastinal route for thoracic esophageal cancer. Ann Thorac Surg 83:1273-1278, 2007 2. Orringer MB: Transhiatal esophagectomy without thoracotomy. Op Tech Thorac Cardiovasc Surg 10:63-83, 2005 3. Barkley C, Orringer MB, Iannettoni MD, et al: Challenges in reversing esophageal discontinuity operations. Ann Thorac Surg 76:989-994, 2003 4. Kelling GE: Oesophagoplastik mit Hilfe des Querkolons. Zentralbl Chir 38:1209-1212, 1911 5. Vuillet H: De l oesophagoplastie et des diverses modifications. Sem Med 31:529-534, 1911 6. Akiyama H, Miyazono H, Tsurumaru M, et al: Use of the stomach as an esophageal substitute. Ann Surg 188:606-610, 1978 7. DeMeester SR: Colon interposition following esophagectomy. Dis Esophagus 14:169-172, 2001 8. Renzulli P, Joeris A, Strobel O, et al: Colon interposition for esophageal replacement: a single-center experience. Langenbecks Arch Surg 389: 128-133, 2004 9. DeMeester SR: Colonic interposition for benign disease. Op Tech Thorac Cardiovasc Surg 11:232-249, 2006 10. Sundaresan SR: Left colon swing for esophageal replacement. Op Tech Thorac Cardiovasc Surg 4:222-238, 1999 11. Rice TW: Right colon interposition for esophageal replacement. Op Tech Thorac Cardiovasc Surg 4:210-221, 1999 12. Urschel JD, Urschel DM, Miller JD, et al: A meta-analysis of randomized controlled trials of route of reconstruction after esophagectomy for cancer. Am J Surg 182:470-475, 2001 13. Orringer MB: Reversing esophageal discontinuity. Sem Thorac Cardiovasc Surg 19:47-55, 2007 14. Wormuth JK, Heitmiller RF: Esophageal conduit necrosis. Thorac Surg Clin 16:11-22, 2006