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Laparoscopic and thoracoscopic esophagectomy

      Esophagectomy is a challenging combination of anatomic resective surgery and reconstructive, function-restoring surgery. It is not only a technically demanding operation, but patients may have associated comorbid problems related to malnutrition, chronic illness, cancer immunosuppression, recovery from chemotherapy, radiation therapy, and other underlying systemic illness that may accompany advanced age. These associated comorbidities may contribute to the morbidity of the operation. There continues to be debate over the best approach to esophagectomy.
      The most widely used approach today is the transhiatal resection of the esophagus with gastric pull up and anastomosis to the cervical esophagus, popularized by Orringer. This approach aims to decrease the morbidity of esophageal resection by avoiding the problems associated with thoracotomy and intrathoracic anastomotic leaks. In exchange, the oncologic completeness of the operation may be compromised by incomplete visualization of the esophagus in the chest along with limited access to lymphatic tissue resection. A recent review of all esophagectomies performed in the United States showed that mortality of open esophagectomy remains at an alarming rate, ranging from 8 to 23%, depending on the clinical volume of a given center. While it has been established that this mortality rate can be lower in centers specializing in esophageal surgery, less invasive alternatives of traditional esophagectomy continue to be evaluated and include photodynamic therapy, endomucosal resection, and definitive chemo-radiation without surgery. In some centers, minimally invasive approaches to esophagectomy have shown some promise.
      Minimally invasive esophageal resection (MIE) using a combined laparoscopic and thoracoscopic approach has the potential to offer an oncologically complete operation, while taking advantage of the benefits of minimally invasive surgery, which may translate into less overall morbidity. On the other hand, MIE is a very technically challenging operation with a very steep learning curve and only performed in a few centers across the US and the world. Although there have been descriptions of MIE using a transabdominal, laparoscopic approach, we prefer a three-field thoracoscopic/laparoscopic approach. We briefly review the technical aspects of this operation and discuss along the way the possible pitfalls associated with the dissection and reconstruction.
      Before accepting a patient for MIE, an evaluation is performed to review the indications and to assess the risk for surgery. In cases of resections for malignancy, a complete staging, including computerized tomography, endoscopic ultrasound, and sometimes laparoscopic or thoracoscopic staging will take place.

      Surgical technique

      Figure thumbnail GR1
      1At the time of surgery, the surgeon stands posterior to the patient as shown. An on-the-table esophagogastroduodenoscopy is performed by the surgical team as a final assessment of tumor extent and gastric involvement. If the tumor is in the mid-thoracic location, an on-the-table bronchoscopy is also performed. If any concerns remain over resectability, a quick laparoscopic and/or thoracoscopic staging may be performed if not already done. If extension of the tumor onto the stomach or lesser curvature limits the ability of the surgeon to obtain a negative margin while maintaining enough length for pull-up into the neck, an alternative approach should be considered such an intrathoracic anastomosis or choosing an alternate conduit. In our practice, this is not a common occurrence. Patient positioning in the typical case of a planned resection with gastric pull-up to the neck starts in the left lateral decubitus position. The arm is placed on a padded suspension device.
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      2The usual position of the thoracic ports is shown. The lower ports and the anterosuperior port are all 10 mm. The port just inferior and posterior to the tip of the scapula is 5 mm; the lower posterior port is 10 mm and is near the 8th intercostal space at the posterior axillary line. These two posterior ports are the working ports for the surgeon. The other lower 10-mm port is anteriorly, near the 9th intercostal space, and offers excellent visualization of the entire length of the thoracic esophagus, using the 30-degree scope. The anterosuperior port is located near the 5th intercostal space and is for the assistant to provide retraction, suction, and exposure. Port localization may vary somewhat based on individual patient anatomy.
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      3Following port placement, a thorough thoracoscopic exploration is performed. Enlarged lymph nodes or other sites of potential disease that may impact on the operation are sent for frozen section. Next, a retraction suture is placed in the central tendon (Endostitch, U.S. Surgical, Norwalk, Connecticut) of the right hemidiaphragm. This suture is brought out percutaneously through a 2-mm nick in the skin near the costophrenic recess anteriorly. Traction on this suture provides excellent downward traction on the diaphragm and an excellent view of the distal extent of the thoracic esophagus. For the dissection, we prefer an ultrasonic dissecting instrument with a relatively sharp tip (U.S. Surgical); this limits thermal conductivity and is an excellent dissecting tool. Care must be taken with any ultrasonic device to avoid activation near areas of potential injury such as the posterior membranous trachea or bronchus, aorta, pulmonary vein, etc. The inferior pulmonary ligament is divided to the inferior pulmonary vein and a plane between the pericardium and periesophageal area is developed. This plane is developed toward the undersurface of the right mainstem bronchus. All lymph nodes and periesophageal fat are taken en bloc with the esophagus. The dissection plane continues along the pericardium and airway, contralateral pleura, aorta, azygos vein, and thoracic duct. The thoracic duct and azygos vein are not resected. To facilitate the more posterior dissection plane, the mediastinal pleura along the esophagus is opened toward the azygos vein and extended from the azygos vein to the diaphragm. A penrose drain is passed around the esophagus and used for retraction.
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      4The azygos vein is divided using a vascular stapler (Endo-GIA II, U.S. Surgical). Above the level of the azygos vein, the dissection plane is maintained directly onto the esophageal wall for tumors of the GE junction and no lymph node dissection is performed in the upper third of the chest. In our experience, lymph node dissection in the upper third of the chest may lead to injury to the recurrent nerves. This plane is continued cephalad toward the thoracic inlet, again staying directly on the esophagus at this point, well into the thoracic inlet and cervical area. This very cephalad dissection, performed under direct vision, facilitates the later neck dissection and we believe minimizes traction injury to the recurrent nerves as they are carefully dissected away from the esophagus. The mediastinal pleura above the azygos is preserved to help to seal the mediastinum around the gastric tube once it is pulled into place. The subcarinal lymph node packet and all surrounding peri-esophageal nodes, fat, and hiatal hernia sac is dissected en-block with the esophagus down to the diaphragmatic crus. The distal dissection continues until visualization of the crus has occurred. This will facilitate connecting the dissection plane during the laparoscopic portion of the operation.
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      5After the esophagus and the subcarinal nodes are separated from the airway, a retro-esophageal window will be apparent. A penrose drain is placed around the esophagus to facilitate retraction. The assistant or surgeon can retract the esophagus anterior to posterior periodically to allow a circumferential view as the dissection is performed. During dissection along the thoracic duct, we carefully search for branches and liberally apply metal clips with an endoscopic device (EndoClip, U.S. Surgical) to minimize damage or later chylous leaks. In addition, careful dissection and visualization of aortoesophageal vessels should be performed and larger branches clipped before division to minimize bleeding. After completion of the posterolateral dissection, the esophagus is lifted using the penrose and the medial attachments are divided. At the completion of the thoracoscopic dissection, the surgeon inspects the most cephalad and distal extents of the dissection plane. The upper dissection should be well into the thoracic inlet and the penrose drain is tucked into this plane to be retrieved later during the cervical dissection. A final inspection of the entire esophagus down to the diaphragmatic crura is performed to make sure all attachments have been divided and no bleeding, air leaks, or chyle leaks are present. Under direct vision, 1 to 2 mL of 0.5% bupivicaine with epinephrine solution is injected into each intercostal space using a long thoracoscopic needle. A single 28 French chest tube is placed for drainage. We have found this addition of local anesthetic provides 6 to 8 hours of good pain relief and may facilitate on-the-table extubation.
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      6The surgeon and assistant remain in the room to help with repositioning. We have found that with an organized team approach, the entire breakdown, repositioning, and reprep can be accomplished in under 10 minutes. During the reprep, the anesthesia team changes the double lumen endotracheal tube to a single lumen tube. This is less bulky and facilitates working in the neck; in addition, if the patient is not ready for extubation at the end of the operation, the single lumen is easier to manage, and also allows a routine toilet bronchoscopy at the end of the procedure before extubation. The position of the patient and operating team for laparoscopy is shown.
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      7Precise localization of the laparoscopic ports is made according to the patient’s body habitus. At our institution, we have performed multiple cases with previous abdominal surgery that require a very creative approach toward port placement, but the definitive port distribution generally approximates that shown in the figure. At least one 11-mm port is used, and it should be at the right epigastrium. This port will be used for access for stapling devices to create the gastric tube and for suturing. Another 10-mm port is placed on the right lower quadrant (not shown in the figure). This is used for identification of the ligament of Treitz and to facilitate suturing of the feeding jejunostomy tube. The upper abdominal ports should be high enough to be able to reach the upper abdomen with the surgical instruments, but low enough to have a reasonable view of the greater curve of the stomach along with the gastroepiploic arcade and the pylorus.
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      8The left lobe of the liver is retracted upward to expose the esophageal hiatus using a Diamond-Flex retractor and held in place with a self-retaining system (Mediflex) placed on the left side of the table. The laparoscopic dissection starts by dividing the hepatogastric ligament toward the right crus of the diaphragm. The right crus is exposed and dissected from the top of the hiatus to the decussation with the left crus. This plane is developed then cephalad along the left crus to develop a retro-esophageal window. Care is taken during the early steps of the dissection to avoid entry into the thoracic cavity as this will lead to loss of the abdominal pneumoperitoneum. If the thoracic cavity is inadvertently entered at this step, generally the stomach and periesophageal fat can be pushed into the opening to stop the leak. Other maneuvers may be necessary, such as placing the right chest tube on suction to avoid tension pneumothorax and massive subcutaneous emphysema. We have also found it helpful to lower the insufflating pressure in the abdomen to minimize these problems. In many cases, an adequate laparoscopic view can be maintained with insufflating pressures in the range of 6 to 8 mm Hg.
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      9Dissection is then taken to the top portion of the esophageal hiatus toward the upper portion of the left crus. In this area, division of the upper phrenogastric attachments toward the highest short gastric vessels will help with mobilization of the spleen and cardia area away from the diaphragm and generally makes the division of the upper short gastric vessels easier.
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      10At this point, the dissection is now directed toward the mid to upper great curve just outside of the gastroepiploic arcade and is directed cephalad toward the short gastrics. Once the short gastrics are all divided, the retro-esophageal plane is cleared more definitively as the greater curve of the stomach is rolled toward the right crus. The plane along the greater curve is developed and continued distally, care being taken to avoid injury to the major gastroepiploic arcade. Care should be taken to clearly identify and preserve this arcade, as it constitutes the major source of blood flow to the gastric tube. Dissection is continued along this plane dividing the connecting vessels to the omentum. Care should be taken to preserve enough tissue to keep a healthy arcade without leaving too much tissue that will result in excessive bulk of tissue on the gastric tube. Too much bulk along the greater curve makes the dissection plane more difficult, and can, in some cases, lead to close proximity to the transverse colon. Excess fat along the greater curve can also lead to tension on the arcade or make it difficult for the gastric tube to ascend through the hiatus along the left crus. The dissection along the greater curve continues toward the hepatoduodenal attachments. These are divided along the lateral duodenum and gallbladder area to complete the Kocher maneuver. This will allow enough mobility to this area to allow the pylorus to reach the upper right crus in a tension-free manner. If gentle lifting of the pylorus does not allow an easy, tension-free reach to the right crus, further retro-antral, retro-pyloric mobilization should be performed.
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      11The greater curve is lifted and all the retro-gastric attachments are divided. It is our practice to try not to handle the stomach by directly grasping it since this may compromise the fine intramural vascular plexus that helps to maintain the gastric tube viability. At this stage, the left gastric vascular complex including vein, artery, and lymph nodes will be apparent. The lymph nodes and fatty tissue of the celiac axis are dissected and mobilized upwards along the left gastric artery and vein. Once this area is cleared, the vessels are divided using an endoscopic vascular stapler (Endo-GIA II, U.S. Surgical). At this point, the stomach is ready for the creation of the gastric tube.
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      12An additional 11-mm port is placed in the right lower quadrant. It is used to place an atraumatic grasper (Snowden Pencer Instruments) on the pyloroantral portion of the stomach to facilitate downward traction on the stomach as the stapling loads are fired during creation of the gastric tube. Of note, simultaneously, the first assistant places another atraumatic grasper along the greater curve and gently stretches the stomach as the site for each firing is chosen and as the stapler is fired. This adds significant length and prevents tethering and spiraling of the tube along the lesser curve area. An area just above the first 2 to 3 arcades of the right gastric artery into the pyloro-antral area is chosen for firing the first stapler. The vascular load is used here to minimize bleeding. The first few arcades of the right gastric vessels into the pyloroantral area are spared and the stapler is fired in a perpendicular orientation to the lesser curve. As the construction of the gastric tube continues, care is taken to align the stapler parallel to the greater curve arcade. Again, we continue to apply gentle stretching of the stomach as the tube is constructed. As the gastric tube stapling progresses cephalad, the traction point is changed to the tip of the fundus, along the line of the short gastrics. These manipulations provide for effective tube length and attention to a line parallel to the greater curve avoids spiraling of the tube.
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      13Once the gastric conduit is completed, a pyloroplasty is performed. Initially, the pyloric muscle is identified by gently rolling the tip of the closed grasper over the pyloroduodenal area. The pyloric muscle is generally easy to palpate and visualize laparoscopically. Stay sutures are placed at the top and bottom of the anterior aspect of the muscle (A). Traction is placed on these sutures and the pylorus is gently elevated. The muscle is divided open along the length of the pyloric channel from the duodenal side until complete division of the muscle is visually evident (B). The gastric tube is suctioned clean through the pyloroplasty. The pyloric incision is closed transversely using nonabsorbable 2-0 sutures applied with an auto suture device (Endo-Stitch, U.S. Surgical) (C).
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      14The needle catheter jejunostomy is placed next. For the j-tube, the endoscope is placed in the 11-mm port just to the right of the midline, and using the 30-degree view, the surgeon explores the lower abdomen, pulls up the omentum, transverse colon and identifies the ligament of Treitz. A point approximately 30 cm distal to the ligament is chosen for the jejunostomy tube site. Next, the surgeon presses exteriorly on the abdominal wall in the area of the mid to lower left quadrant, and chooses a site for the needle catheter j-tube. A 25-gauge 1.5 inch needle is inserted through the skin into the peritoneal cavity at the chosen site, under direct view, and under laparoscopic view. Next, the jejunum is tacked to the abdominal wall near this needle entry site. The larger bore needle, which allows passage of the needle catheter (Compat Specialty Feeding Tube, 5French, Novartis, Minneapolis), is inserted through the abdominal wall percutaneously and enters the jejunum near the tacked site. Under laparoscopic view, the catheter is threaded into the jejunum for a distance of 20 cm. Two additional sutures are placed to secure the jejunum to the peritoneal wall. A final endo-stitch is placed several centimeters away from the tacked site to avoid torsion of the bowel around a single focal point. Under direct vision, 10 mL of air is rapidly injected through the needle catheter into the small bowel, immediate distention confirms endoluminal placement. If any doubt about this exists, an on-the-table gastrograffin injection of the j-tube is performed.
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      15Next, mobilization at the hiatus into the thoracic cavity, in a circumferential manner is performed. The tip of the gastric tube is sewn to the lower end of the lesser curve staple line on the side of the specimen.
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      16At this point, we turn our attention to the area of the neck. A low cervical collar incision is performed and carried through the platysma to the deep cervical visceral space to the prevertebral fascia. Platysmal skin flaps are developed. Lateral dissection of the cervical esophagus is accomplished and the penrose drain left at the thoracic inlet is generally easily visualized and retrieved and used for retraction of the cervical esophagus. The high dissection performed well into the cervical esophageal area during the final portion of the thoracoscopic mobilization makes it much easier to retrieve the cervical esophagus with minimal dissection and in our experience lowers the risk to the recurrent laryngeal nerves. At this point, the surgeon stays at the neck to pull up the gastric tube as the abdomen is insufflated and the laparoscopic view is reestablished allowing direct visualization as it ascends through the hiatus. The resected esophagogastric specimen is removed through the neck incision and the gastric tube is pulled up to the neck. Care is taken to maintain a view on the laparoscopic side and simultaneously, a view of the cervical neck incision to assure proper orientation of the gastroepiploic arcade toward the left crus to avoid spiraling of the gastric tube. Care should be taken to avoid tension on the gastroepiploic arcade as the conduit traversed the hiatal opening. If the hiatal opening appears to restrict the passage of the gastric conduit, the right and left crus are incised 0.5 cm to 1.0 cm to allow a tension-free passage.
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      17The gastric tube is assessed for viability and adequate tension-free length. The method of anastomosis varies: hand sewn, side to side stapled, or end-to-side stapled; this last one being our preferred method. As the specimen is pulled out of the neck, slight tension is placed on the remaining cervical esophageal attachments. Once the cervical esophagus is adequately mobilized, it is placed on slight tension and a 45-mm, auto-purse string device is fired across the esophagus just distal to the cricopharyngeus. The esophagus is divided distal to the purse string device and the specimen is sent for frozen section analysis. The cervical anastomosis is performed high to minimize the residual esophagus which on occasion may have Barrett’s extending quite high. Additionally, we have found that if the cervical esophageal length extends much beyond the cricopharyngeus, the anastomosis tends to lie toward the thoracic inlet. If a leak occurs at or near the thoracic inlet, there is a potential for tracking into the right thoracic cavity along the previous thoracoscopically mobilized plane. Performing the anastomosis very high in the neck has allowed us to avoid this complication. Next, the purse string device is removed and the esophagus is lubricated, and gently dilated. Generally a 25-mm EEA anvil is easily inserted into the cervical esophageal stump. Generally a 25-mm EEA anvil is easily inserted into the cervical esophageal stump; then the purse string is tied. Next the gastric conduit is again assessed for viability, the fundic tip is opened and the gastric tube is suctioned clean. A 25-mm end-to-end stapler (EEA, U.S. Surgical) is passed through this opening. Depending on length, we generally exit the point of the EEA out of the posterior gastric tube, avoiding the area of the short gastrics posteriorly and avoiding too close a proximity to the lesser curve staple line. The EEA device is now docked with the anvil and fired. A nasogastric tube is inserted under direct visualization across the anastomosis and the tip should lie in the gastric tube above the pyloroplasty. The opening in the tip of the gastric tube is closed with a linear stapling instrument, taking care to preserve as much of the line of the short gastric vessels as possible and removing the distal 6 to 8 cm of the tube, again, depending on the length available.
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      18As a final step, the gastric tube is gently grasped near the pylorus and downward traction is applied until any redundancy pulled up into the chest cavity is reduced back into the abdomen. Generally, this is best assessed by the assistant observing the anastomosis in the neck as it starts to move downward as traction is applied from the laparoscopic ports. The gastric tube is tacked to the diaphragmatic hiatus to prevent herniation of other abdominal viscera. The first stitch is placed on the greater curve of the stomach and attached to the left crus. The anterior portion of the tube is tacked to the anterior crus. Next, the lesser curve of the tube is sutured to the right crus. The liver retractor is withdrawn and the 10-mm port fascial defects are closed under direct vision. The abdomen is deflated and the skin approximated with subcuticular absorbable sutures. The neck is closed without reapproximating the platysma. A flexible toilet bronchoscopy is performed before extubation to clean up the airway.

      Conclusion

      Minimally invasive esophagectomy is a very complex and technically demanding procedure. The variety of disease processes that constitute the indications for esophagectomy add their own component of complexity by either affecting the patient’s physiologic status or by anatomic alterations associated with the disease process. Treatment strategies that constitute alternatives or adjuvants to surgery can also make this procedure more challenging by altering the normal state of the esophagus before surgery. After our extensive experience with 222 minimally invasive esophagectomies, it is our opinion that the most important aspects for this surgery to be successful and for good outcomes are to minimize handling of the stomach before creating the gastric tube, to carefully identify and protect the gastroepiploic arcade, to perform complete mobilization of the stomach to the medial second portion of the duodenum to prevent tension, and to very carefully handle the gastric tube after its creation. All of these measures will ensure that the gastric tube will be healthy to sustain the initial postoperative period until the capillary plexuses develop along the length of the tube. Due to the complexity of the procedure and the steep learning curve associated with it, we recommend that it be performed only in selected centers with high volume of patients. We also believe that there is a critical amount of open experience that is necessary to be able to facilitate the learning of this procedure. In conclusion, MIE is a less invasive procedure that has the advantage of providing quick recovery and in our opinion lowers morbidity, and, in our experience, was associated with a 1.4% mortality rate. The procedure, as described, is oncologically sound and includes en block resection of mediastinal lymph nodes under direct visualization. Preliminary reports show decreased hospital stay and mortality when compared with most open esophagectomy series.
      • Luketich J.D
      • Alvelo-Rivera M
      • Buenaventura P.O
      • et al.
      Minimally invasive esophagectomy Outcomes in 222 patients.
      ,
      • Orringer M.B
      • Marshall B
      • Iannettoni M.D
      Transhiatal esophagectomy for treatment of benign and malignant esophageal disease.
      ,
      • Bailey S.H
      • Bull D.A
      • Harpole D.H
      • et al.
      Outcomes after esophagectomy A ten year prospective cohort.
      ,
      • Swanstrom L.L
      • Hansen P
      Laparoscopic total esophagectomy.
      ,
      • Nguyen N.T
      • Follette D.M
      • Wolfe B.M
      • et al.
      Comparison of minimally invasive esophagectomy with transthoracic and transhiatal esophagectomy.

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