Morbidity and mortality of esophageal resection is

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1 Mucosal Tube Technique for Creation of Esophageal Anastomosis After Esophagectomy Robroy H. MacIver, MD, Sudhir Sundaresan, MD, Alberto L. DeHoyos, MD, Mark Sisco, MD, and Matthew G. Blum, MD Department of Surgery, Northwestern Memorial Hospital, Chicago, Illinois; Division of Thoracic Surgery, The Ottawa Hospital, Ottawa, Ontario, Canada; and Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York Background. The definitive treatment of esophageal cancer remains surgical resection. Morbidity and mortality are highly influenced by the success of the anastomosis created in the reconstruction of the resected esophagus. The results of an anastomotic technique that creates an esophageal mucosal tube are analyzed. Methods. The medical records of all patients undergoing esophagectomy at a single institution by 3 surgeons between January 2002 and July 2008 were reviewed. Patients who underwent a 2-layer, hand-sewn, esophageal anastomosis using a mucosal tube were included. The unique aspect of the anastomosis was the creation of an esophageal mucosal tube that facilitates a tensionfree, precise mucosal approximation. Results. Of the 61 patients who underwent esophageal reconstructions (60 gastric, 1 colonic), 49 (80%) had a diagnosis of esophageal neoplasm. Of those with cancer, 20 (41%) had neoadjuvant therapy before the resection. Two patients presented with perforation. The anastomoses were intrathoracic in 57 of 61 (93%) and cervical in 4 cervical. There were no operative deaths. All patients underwent contrast study at an average of 5 days postoperatively. The anastomotic leak rate was 2% (1 of 61). Postoperative dilations (mean, 1.3 dilations) were done in 12 of 61 patients (20%), using a low symptom threshold for endoscopy and dilation. Conclusions. The use of the esophageal mucosal tube and 2-layer anastomosis is a robust technique that results in a low leak rate. Strictures are minimal and easily dilated if they occur. Use of a gastrotomy larger than 2.5 cm may decrease stricture rates. (Ann Thorac Surg 2009;87:1703 7) 2009 by The Society of Thoracic Surgeons Morbidity and mortality of esophageal resection is strongly influenced by the success of the anastomosis of the esophageal-conduit anastomosis. A 2-layer sewn anastomosis described by Churchill and Sweet in 1942 has been used successfully by many surgeons [1, 2]; and more recently, groups have adopted a stapled technique [3]. Most studies have concluded equivalence between sewn and stapled techniques [4]. Even when a mechanical stapled technique is used routinely, some situations may warrant the use of a sutured anastomosis. This report details the results of a hand-sewn technique using an esophageal mucosal tube to facilitate accurate, tension free esophageal-conduit approximation in the construction of the anastomosis. Material and Methods After obtaining Investigational Review Board approval, the medical records of all patients undergoing esophagectomy at our institution (NMH) by 3 surgeons between January 2002 and July 2008 were reviewed retrospectively. Patients selected for this report underwent reconstruction with a conduit anastomosed in the chest or in the neck using a mucosal tube technique for esophageal Accepted for publication March 23, Address correspondence to Dr Blum, 676 N St. Clair, Ste 650, Chicago, IL 60611; mblum@nmh.org. colic and esophagogastric anastomoses as documented in a previous report [5, 6]. Data collected included sex, age, indication for procedure, histopathology, use of chemoradiation neoadjuvant therapy, anastomotic location, conduit type, and frequency of perioperative complications, including anastomotic leak. Records were also reviewed for indications, findings, and degree of dilation for patients who underwent esophagoscopy after operation. The stomach and esophagus were mobilized and a replacement conduit was prepared in a standard fashion. Removing the gastroesophagostomy specimen allowed easier manipulation of the esophagus during the subsequent creation of the esophageal anastomosis. To do this, the esophagus was transected with a linear stapler 2 to 3 cm distal to the site of the planned anastomosis. The esophageal mucosal tube was created by making a circumferential esophageal myotomy. The corners of the staple line were grasped with Allis clamps for retraction. A circumferential incision through the esophageal muscularis 1 to 2 cm proximal to the staple line was made (Fig 1A). With the resultant mucosal tube intact, the muscularis was swept further distally using a Kittner (Fig 1B). The mucosa was then sharply transected 1 to 2 cm distal from the myotomy site to create a mucosal sleeve (Figs 1C and D). The 2-layer end-to-side anastomosis was constructed by approximating an inner layer of esophageal mucosa to full-thickness stomach and an outer layer of esophageal 2009 by The Society of Thoracic Surgeons /09/$36.00 Published by Elsevier Inc doi: /j.athoracsur

2 1704 MACIVER ET AL Ann Thorac Surg MUCOSAL TUBE TECHNIQUE AFTER ESOPHAGECTOMY 2009;87: Fig 1. (A) Performing the myotomy with a knife. Allis clamps are used to grasp the staple line of the transected esophagus. The stapled transection of the esophagus is 2 to 3 cm distal to the intended level of anastomosis and allows removal of most of the gastroesophagostomy specimen. This also allows improved visualization of the esophagus, facilitating creation of the myotomy. Note the staple line is not the final margin. (Arrow esophageal mucosa * gastric conduit). (B) Sweeping the myotomy to clear the mucosal tube. (C) The mucosa is transected at the border of the distal muscularis to leave a 1- to 2-cm mucosal tube. (D) The cut mucosal tube before suturing the anastomosis. muscularis to a gastric seromuscular layer. The anastomosis was started by placing 4-0 silk sutures through opposite corners of the esophageal muscularis and seromuscular layers of the stomach at least 2 cm from the lesser curvature staple line (Fig 2A). These sutures defined the corners of the outer layer. The corners were far enough apart to allow a 2.5-cm gastrotomy. After placement of a back row of outer (esophageal muscularis to seromuscular stomach) sutures, the gastrotomy was opened with cautery (Fig 2B). The inner layer corner sutures were placed through the mucosal layer of the esophagus and full-thickness stomach (Fig 2C). Once both of these posterior rows were completed, the nasogastric tube was passed into the stomach (Fig 2D). The anterior inner and outer layers were then completed. When this technique is used with a colonic conduit, the anastomotic layers are the same (esophageal mucosa sewn to full-thickness colon and esophageal muscularis sewn to seromuscular colon). A jejunostomy tube was placed in most patients for feeding. Barium swallow studies were routinely performed in the first week after the operation. Postoperative esophagogastroduodenoscopy was liberally performed for patients who had any degree of dysphagia or complaints potentially referable to stricture, esophagitis, or ulceration, including regurgitation of food, excessive mucus production, and globus sensation, among others. Because causes of postoperative dysphagia may be multifactorial, and low-grade anastomotic stricturing is sometimes difficult to appreciate endoscopically, dilators were routinely passed to eliminate stricturing as a potential cause of symptoms. Results Esophageal reconstructions were done in 61 patients, 60 with gastric and 1 with a colonic conduit. The mean age Table 1. Patient Characteristics Variable No. (%); N 61 Gender Male 48 (79) Female 13 (21) Diagnosis Cancer 52 (85) Histology Adenocarcinoma 38 (81) Squamous 5 (11) GIST 1 (2) Neoadjuvant chemoradiation 20 (38) High-grade dysplasia 3 (6) Dysmotility 6 (10) Perforation 2 (3) Reflux 1 (2) Anastomosis location Thoracic 57 (93) Cervical 4 (7) GIST gastrointestinal stromal tumor.

3 Ann Thorac Surg MACIVER ET AL 2009;87: MUCOSAL TUBE TECHNIQUE AFTER ESOPHAGECTOMY 1705 Fig 2. (A) Outer corner sutures are placed in the seromuscular tissue of the stomach and the muscular esophagus. The dotted line shows line of gastrotomy. (B) The posterior outer suture line has been completed. (C) The posterior inner layer has been partially completed. Two corner sutures are placed first (one tied and cut and one untied in the diagram) to ensure that there is no infolding of the mucosa and facilitate accurate mucosal approximation. (D) Completed posterior rows with nasogastric tube in place. of the patients was 61 years, and their characteristics are detailed in Table 1. There were no operative deaths. Complications are described in Table 2. Average postoperative length of stay was 10 days (range, 5 to 37 days). One patient had undergone long esophageal myotomy, and the anastomosis was created within the myotomized esophagus without complications. Average follow-up was 546 days (range, 16 to 1990 days). All patients underwent a contrast study on postoperative day 5 (range 3 to 23 days). One (1.6%) esophageal-gastric anastomotic leak noted by postoperative study was treated by drainage while feeding through a jejunal tube. This was due to an inadequate repair after a nasogastric tube was inadvertently directed through the Table 2. Complications in the 61 Patients Complications Total No. Pneumonia 5 Anastomotic leak 1 Gastric necrosis 1 Bleeding requiring reoperation 1 Jejunostomy tube revision 1 Local wound infection 1 Pneumothorax 1 Respiratory failure 1 Chylothorax 1 Pyloroplasty leak 1 Pleural effusion 1 freshly completed anastomoses. Gastric necrosis in 1 patient required resection of the gastric conduit. Owing to the low symptom threshold, 12 of the 61 patients (20%) underwent postoperative endoscopy and dilation. The average time to endoscopy was 62 days. In 1 patient, a small ulcer in the gastric conduit near the suture line resolved without therapy other than proton pump inhibitors. The endoscope passed without resistance in all patients before dilation. The average final dilator diameter was 19 mm. Most patients required only a single dilation (mean, 1.3). Two patients had two dilations of esophagogastric strictures that have not recurred in the 15 months after their last dilation. The patient with an esophagocolic anastomosis required three dilations in the first 4 months postoperatively but has been stricture free for 6 years. Only 1 of the last 17 patients has required dilation. This may be because a gastrotomy larger than 2.5 cm was deliberately created in the more recent patients. Comment The creation of an intact anastomosis resistant to stricture is an important element to a successful esophageal reconstruction. There is no clear evidence in the literature that a stapled or hand-sewn anastomosis has an advantage in all situations [4, 7 11]. Our technique compares favorably with reported esophagogastrostomy leak rates of 3.5% to 21% using hand-sewn, circular stapled, or side-to-side stapled anastomotic techniques [9, 12 20].

4 1706 MACIVER ET AL Ann Thorac Surg MUCOSAL TUBE TECHNIQUE AFTER ESOPHAGECTOMY 2009;87: The best technique can always be defeated with lack of attention to detail. The only leak developed in a patient in whom the nasogastric tube was placed after the anastomosis was completed. During placement, before chest closure, the tube passed between the anastomotic sutures. Reinforcing sutures were placed in the outer layer. In retrospect, these were insufficient, and the anastomosis should have been reconstructed to allow precise reclosure of the mucosal layer. No anastomotic technique will overcome general gastric necrosis, which occurred in the proximal third of the stomach in 1 patient. The demarcation line of necrosis was 3 cm distal to the anastomosis, so placement of the gastrotomy was not thought to have caused the necrosis. Despite being completely surrounded by necrotic stomach, the anastomosis was intact at the time of the swallow study on postoperative day 4. Even at the time of gastric resection on postoperative day 10, the anastomosis had maintained most of its integrity, with most leaking material coming from a perforation at the necrotic gastric tip. Accurate mucosal apposition is essential for anastomotic healing without leak or stricture. Animal studies have shown that the mechanism of mucosal approximation can result in differences in the amount of granulation tissue and stricture formation. Caporossi and colleagues [21] investigated hand-sewn vs stapled esophageal anastomoses in a dog model. They showed that the healing was by secondary intention at the mucosal level in most of the animals treated with stapled anastomoses. The dogs that had a hand-sewn anastomosis healed by primary intention. Healing by secondary intention led to a higher amount of granulation tissue at the anastomotic site. The authors speculated that their findings correlated with clinical data of other investigators who revealed a higher incidence of delayed stricture formation in patients undergoing a stapled anastomosis, which may be secondary to an overabundance of granulation tissue at the anastomotic site [22]. Another principle for minimizing anastomotic complications is eliminating anastomotic tension. A myotomy can decrease the tension at the anastomotic site. In an animal study of piglets, a myotomy decreased the tension by 66% [23]. The mucosal tube technique results in a mucosal layer that is completely tension free because the outer layer carries any stress on the anastomosis. Multiple methods of creating mucosal apposition exist. The apposition can be performed either partially, such as in a single layer or Collard type anastomosis, or completely (stapled alone) blind. The method we have used places each suture under direct visualization. In theory, precise mucosa-to-mucosa apposition that prevents exposure of the submucosa and muscularis can help prevent stricture formation. Our esophagoscopy and stricture rate was relatively high for anastomoses that were not complicated by leak. One reason might have been that patients who had any solid dysphagia underwent esophagoscopy. Many of them had minimal or no stricturing. A second potential issue is that patients mild early postoperative dysphagia might be more likely to develop when the anastomosis is created with a smaller gastrotomy. Our technique has evolved to intentionally use a larger gastrotomy and may account for the decreased stricture rate in more recent patients. A good technique should be reproducible and teachable. Most of these anastomoses were done by residents and fellows. After the initial description and creating one anastomosis, residents could clearly recreate the technique. Argumentsfavoring various anastomotic techniques cite differences in stenosis and leak rate. The method of anastomosis chosen should ultimately be one that best matches the patient s physiologic disease and the surgeon s comfort with the technique. A nonstricturing, nonleaking anastomosis depends on basic tenets of surgical technique of precise apposition of tissues, lack of tension, and maintenance of blood flow. The precise apposition of mucosa to mucosa in a tension-free manner had been shown to improve both leak and stricture rates after anastomosis. The described mucosal tube technique allows highly accurate mucosal apposition with no tension on the mucosal layer and the resultant successful anastomosis. References 1. Churchill ED, Sweet RH. Transthoracic resection of tumors of the stomach and esophagus. Ann Surg 1942;115: Mathisen DJ, Grillo HC, Wilkins EW Jr, et al. Transthoracic esophagectomy: a safe approach to carcinoma of the esophagus. Ann Thorac Surg 1988;45: Santos RS, Raftopoulos Y, Singh D, et al. Utility of total mechanical stapled cervical esophagogastric anastomosis after esophagectomy: a comparison to conventional anastomotic techniques. Surgery 2004;136: Blackmon SH, Correa AM, Wynn B, et al. Propensitymatched analysis of three techniques for intrathoracic esophagogastric anastomosis. Ann Thorac Surg 2007;83: ; discussion Sundaresan S. Colon swing for esophageal replacement. Operat Tech in Thorac Cardiovasc Surg 1999;4: Ashrafi AS. Transhiatal esophagectomy. In: Kaiser LR, Kron IL, Spray TL, eds. Mastery of cardiothoracic surgery. 2nd ed; Philadelphia: Lippincott, Williams and Wilkins; 2007: Behzadi A, Nichols FC, Cassivi SD, et al. Esophagogastrectomy: the influence of stapled versus hand-sewn anastomosis on outcome. J Gastrointest Surg 2005;9: ; discussion Law S, Fok M, Chu KM, Wong J. Comparison of hand-sewn and stapled esophagogastric anastomosis after esophageal resection for cancer: a prospective randomized controlled trial. Ann Surg 1997;226: Law S, Suen DT, Wong KH, Kwok KF, Wong J. A singlelayer, continuous, hand-sewn method for esophageal anastomosis: prospective evaluation in 218 patients. Arch Surg 2005;140: Orringer MB, Marshall B, Iannettoni MD. Eliminating the cervical esophagogastric anastomotic leak with a side-toside stapled anastomosis. J Thorac Cardiovasc Surg 2000;119: Singh D, Maley RH, Santucci T, et al. Experience and technique of stapled mechanical cervical esophagogastric anastomosis. Ann Thorac Surg 2001;71: Ancona E, Cagol M, Epifani M, et al. Surgical complications do not affect longterm survival after esophagectomy for carcinoma of the thoracic esophagus and cardia. J Am Coll Surg 2006;203:661 9.

5 Ann Thorac Surg MACIVER ET AL 2009;87: MUCOSAL TUBE TECHNIQUE AFTER ESOPHAGECTOMY Crestanello JA, Deschamps C, Cassivi SD, et al. Selective management of intrathoracic anastomotic leak after esophagectomy. J Thorac Cardiovasc Surg 2005;129: Griffin SM, Lamb PJ, Dresner SM, Richardson DL, Hayes N. Diagnosis and management of a mediastinal leak following radical oesophagectomy. Br J Surg 2001;88: Martin LW, Swisher SG, Hofstetter W, et al. Intrathoracic leaks following esophagectomy are no longer associated with increased mortality. Ann Surg 2005;242:392 9; discussion Orringer MB, Marshall B, Iannettoni MD. Transhiatal esophagectomy: clinical experience and refinements. Ann Surg 1999;230: ; discussion Portale G, Hagen JA, Peters JH, et al. Modern 5-year survival of resectable esophageal adenocarcinoma: single institution experience with 263 patients. J Am Coll Surg 2006;202:588 96; discussion Rizk NP, Bach PB, Schrag D, et al. The impact of complications on outcomes after resection for esophageal and gastroesophageal junction carcinoma. J Am Coll Surg 2004;198: Sauvanet A, Baltar J, Le Mee J, Belghiti J. Diagnosis and conservative management of intrathoracic leakage after oesophagectomy. Br J Surg 1998;85: Whooley BP, Law S, Alexandrou A, Murthy SC, Wong J. Critical appraisal of the significance of intrathoracic anastomotic leakage after esophagectomy for cancer. Am J Surg 2001;181: Caporossi C CI, Aguilar-Nascimento JE, Venço F, Gama- Rodrigues JJ. Hand-sewn and stapled esophageal anastomosis: experimental study in dogs. Acta Cir Bras 2004;19: Livaditis A, Okmian L, Bjorck G, Ivemark B. Esophageal suture anastomosis. An experimental study in piglets. Scand J Thorac Cardiovasc Surg 1969;3: Livaditis A, Radberg L, Odensjo G. Esophageal end-to-end anastomosis. Reduction of anastomotic tension by circular myotomy. Scand J Thorac Cardiovasc Surg 1972;6: Requirements for Maintenance of Certification in 2009 Diplomates of the American Board of Thoracic Surgery (ABTS) who plan to participate in the Maintenance of Certification (MOC) process which will begin in 2009 must hold an unrestricted medical license in the locale of their practice and privileges in a hospital accredited by the JCAHO (or other organization recognized by the ABTS). In addition, a valid ABTS certificate is an absolute requirement for entrance into the Maintenance of Certification process. If your certificate has expired, the only pathway for renewal of a certificate is to take and pass the Part I (written) and the Part II (oral) certifying examinations. The names of individuals who have not maintained their certificate will no longer be published in the American Board of Medical Specialties directories. Diplomates names will be published upon successful completion of the Maintenance of Certification process. The CME requirements are 30 Category I credits earned during each year prior to application. At least half of these CME hours need to be in the broad area of thoracic surgery. Category II credits are not allowed. Interested individuals should refer to the Booklet of Information for Maintenance of Certification for a complete description of acceptable CME credits. Diplomates in the Maintenance of Certification process will be required to complete all sections of the SESATS self-assessment examination. It is not necessary for Diplomates to purchase SESATS individually because it will be sent to them after their application has been approved. Diplomates may apply for Maintenance of Certification in the year their certificate expires, or if they wish to do so, they may apply up to two years before it expires. However, the new certificate will be dated 10 years from the date of expiration of their original certificate or most recent recertification certificate. In other words, going through the Maintenance of Certification process early does not alter the 10-year validation. Diplomates certified prior to 1976 (the year that time-limited certificates were initiated) are also required to participate in MOC if they wish to maintain valid certificates. The deadline for submission of application for the Maintenance of Certification is May 10 of each year. All ABTS diplomates will receive a letter from the Board outlining their individual timeline and MOC requirements. A brochure outlining the rules and requirements for Maintenance of Certification in thoracic surgery is available upon request from the American Board of Thoracic Surgery, 633 North St. Clair St, Suite 2320, Chicago, IL 60611; telephone (312) ; fax (312) ; info@abts.org. This booklet is also published on the website: by The Society of Thoracic Surgeons Ann Thorac Surg 2009;87: /09/$36.00 Published by Elsevier Inc