Minimally Invasive Esophagectomy


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Minimally Invasive Esophagectomy

  1. 1. ORIGINAL ARTICLES Minimally Invasive Esophagectomy Lessons Learned From 104 Operations Ninh T. Nguyen, MD, FACS,* Marcelo W. Hinojosa, MD,* Brian R. Smith, MD,* Kenneth J. Chang, MD,† James Gray, BS,* and David Hoyt, MD, FACS* Objectives: To review the outcomes of 104 consecutive minimally invasive esophagectomy (MIE) procedures for the treatment of T he enthusiasm for minimally invasive surgery, which began with the first laparoscopic cholecystectomy, has since expanded to many other areas of abdominal and tho- benign and malignant esophageal disease. racic surgery. The speed by which adoption of a new mini- Summary Background Data: Although minimally invasive surgi- mally invasive operation evolves is often a reflection of the cal approaches to esophagectomy have been reported since 1992, degree of technical difficulty of the procedure and the fre- MIE is still considered investigational at most institutions. quency of the operation. For example, within only a few years Methods: This prospective study evaluates 104 MIE procedures of the first clinical report of laparoscopic cholecystectomy, performed between August 1998 and September 2007. Main out- the number of laparoscopic cholecystectomies performed in come measures include operative techniques, operative times, blood the United State exceeded that of open cholecystectomies. In loss, length of stay, conversion rates, morbidities, and mortalities. contrast, it took more than 5 years from the first report of Results: Indications for surgery were esophageal cancer (n 80), laparoscopic Roux-en-Y gastric bypass for the treatment of Barrett esophagus with high-grade dysplasia (n 6), recalcitrant morbid obesity before widespread dissemination of this com- stricture (n 8), gastrointestinal stromal tumor (n 3), and gastric plex operation occurred. It was not until 2004 that the number cardia cancer (n 7). Surgical approaches included thoracoscopic/ of laparoscopic gastric bypass operations exceeded that of laparoscopic esophagectomy with a cervical anastomosis (n 47), open gastric bypass.1,2 Open esophageal resection for benign minimally invasive Ivor Lewis esophagectomy (n 51), laparo- or malignant disease is another complex gastrointestinal op- scopic hand-assisted blunt transhiatal esophagectomy (n 5), and eration, and minimally invasive surgical approaches have laparoscopic proximal gastrectomy (n 1). There were 77 males. been reported since 1992.3 However, to date, there has been The mean age was 65 years. Three patients (2.9%) required conver- only 1 large study reporting outcomes of minimally invasive sion to a laparotomy. The median ICU and hospital stays were 2 and esophagectomy (MIE).4 Although every imaginable tech- 8 days, respectively. Major complications occurred in 12.5% of nique for MIE has been described in the literature, it is difficult to determine the best minimally invasive approach patients and minor complications in 15.4% of patients. The inci- for esophageal resection due to the limited experience with dence of leak was 9.6% and of anastomotic stricture was 26%. The this complex operation at most centers. We have been per- 30-day mortality was 1.9% with an in-hospital mortality of 2.9%. forming MIEs since 1998 and previously reported on an The mean number of lymph nodes retrieved was 13.8. initial experience of thoracoscopic and laparoscopic esopha- Conclusions: Minimally invasive esophagectomy is feasible with a gectomy performed on 46 consecutive patients with a mean low conversion rate, acceptable morbidity, and low mortality. Our follow-up of 26 months.5 Since that report, our surgical preferred operative approach is the laparoscopicthoracoscopic techniques have evolved, and we have made several impor- Ivor Lewis resection, which provides a tension-free intrathoracic tant technical and philosophical improvements. The current anastomosis. report describes lessons learned in performing MIE on 104 (Ann Surg 2008;248: 1081–1091) consecutive patients over a 9-year period. PATIENTS AND METHODS Patients From the Departments of *Surgery and †Medicine, University of California, Between August 1998 and September 2007, 104 con- Irvine Medical Center, Orange, California. Dr. Nguyen received an educational grant from Covidien. secutive patients underwent MIE at the Universities of Cali- Presented at the American College of Surgeons 93rd Annual Clinical fornia, Irvine and Davis Medical Centers. There were no open Congress, New Orleans, LA, October 9, 2007. esophagectomy performed during this time period. The first Reprints: Ninh T. Nguyen, MD, Department of Surgery, 333 City Blvd. 43 cases were performed at the University of California, West, Suite 850, Orange, CA 92868. E-mail: Copyright © 2008 by Lippincott Williams & Wilkins Davis Medical Center and all subsequent cases were per- ISSN: 0003-4932/08/24806-1081 formed at the University of California, Irvine Medical Center. DOI: 10.1097/SLA.0b013e31818b72b5 All operations were performed by a single surgeon. The Annals of Surgery • Volume 248, Number 6, December 2008 1081
  2. 2. Nguyen et al Annals of Surgery • Volume 248, Number 6, December 2008 following data were prospectively collected on a computer- curvature of the stomach was mobilized, preserving the right ized data form: demographics, tumor characteristics, indica- gastroepiploic vessels. If not divided at the time of laparo- tions for surgery, type of resection, performance of a pylo- scopic staging, the left gastric vessels were then isolated and roplasty, operative times, estimated blood loss, transfusion divided with a linear stapler. Lymph nodes along the celiac requirements, length of intensive care unit (ICU) stay, length axis were resected to remain en bloc with the surgical of hospital stay, histopathologic analysis of the surgical specimen. Laparoscopic pyloroplasty was performed with specimen, postoperative complications, and mortality. Post- interrupted sutures in the first 31 patients. A pyloroplasty was operative complications occurring within the first 30 days not performed in the latter cases as we changed our technique after surgery were categorized as either major or minor. Late to construction of a tubular gastric conduit. A gastric conduit complications were defined as any occurring after 30 days. was constructed by dividing the stomach, starting on the This retrospective review was approved by our Institutional lesser curvature and finishing at the angle of His. The tip of Review Board. the gastric conduit was then temporarily sutured to the esoph- ageal specimen. Preoperative Evaluation In the third stage, a horizontal neck incision was per- Preoperative workup for patients with esophageal or formed in the left neck, 1 fingerbreadth above the supraster- gastric cardia cancer included upper endoscopy with biopsy, nal notch. The cervical esophagus was mobilized to commu- barium swallow, endoscopic ultrasound, computed tomogra- nicate with the dissection plane achieved in the right chest. phy of the chest and abdomen, and positron emission tomog- The entire esophageal specimen with the attached gastric raphy. Cardiopulmonary evaluation included pulmonary conduit was then delivered up through the cervical incision. function testing and a 2-D echocardiogram. If patients were An esophagogastric anastomosis was constructed either with considered to be surgical candidates after these evaluations, a 21-mm circular stapler or a 2-layer hand-sewn technique. they would undergo laparoscopic staging and placement of a jejunostomy feeding catheter approximately 7 to 10 days Laparoscopic and Thoracoscopic Ivor Lewis before resection. At the time of laparoscopic staging, all Resection patients underwent placement of a 10F jejunostomy catheter An entirely laparoscopic and thoracoscopic Ivor Lewis and some patients in the latter part of this series (n 40) also resection was performed in 51 patients and consisted of 2 underwent gastric ischemic conditioning with division of the stages. In the first stage, the patient was placed in a supine left gastric pedicle using a linear stapler.6 Since implemen- position. Five abdominal ports were used. The greater curva- tation of gastric ischemic conditioning, preoperative laparo- ture of the stomach was mobilized by dividing the short scopic ligation of the left gastric vessels is even performed for gastric vessels. The left gastric vessels were then divided with patients with high-grade dysplasia and benign disease. In this a linear stapler. During construction of the gastric conduit, the series, a minimally invasive approach to esophagectomy was green stapler load is often used for the first application along not attempted in patients with T4 disease or morbid obesity. the lesser curvature of the stomach then blue stapler loads are used as the stomach thins out toward the angle of His (Fig. 1). Surgical Approach Thoracoscopic and Laparoscopic Esophagectomy With Cervical Anastomosis The entirely laparoscopic and thoracoscopic esopha- gectomy with cervical anastomosis was performed on 47 patients. Routine upper endoscopy was performed in the operating room immediately before surgical resection to de- termine the upper and lower extents of the cancer. The operation was conducted in 3 stages. In the first stage, the patient was placed in the left lateral decubitus position. Four thoracic trocars were introduced into the right chest. Carbon dioxide insufflation was not used during thoracoscopy. The lung was retracted anteriorly. The mediastinal pleura overly- ing the esophagus was divided to expose the intrathoracic esophagus, and the azygous vein was divided with a linear stapler. A Penrose drain was placed around the esophagus to facilitate retraction. The esophagus was then circumferen- tially mobilized from the esophageal hiatus up to the thoracic inlet. Paraesophageal lymph nodes were dissected and main- tained en bloc with the surgical specimen. A subcarinal lymph node dissection was performed. A 28-French chest tube was inserted at the 12-mm trocar site for postoperative drainage. In the second stage, the patient was rotated to a supine position. Five abdominal ports were inserted. The greater FIGURE 1. Laparoscopic construction of a gastric conduit. 1082 © 2008 Lippincott Williams & Wilkins
  3. 3. Annals of Surgery • Volume 248, Number 6, December 2008 Minimally Invasive Esophagectomy FIGURE 2. The tip of the gastric conduit is temporarily sutured to the surgical specimen in preparation for gastric pull-up. A Penrose drain is positioned around the esophagus in the medi- FIGURE 3. Trocar position for thoracoscopic esophagectomy. astinum for retrieval in the thorax. first 45 cases, the 25-mm anvil was placed transthoracically The tip of the gastric conduit was temporarily attached to the into the esophageal stump and secured with a purse-string surgical specimen with interrupted sutures. The esophagus suture (Fig. 7). In the most recent several cases, the anvil was was then circumferentially mobilized for a segment of 5 to 6 placed transorally using a pretilted anvil (Orvil; Autosuture, cm into the mediastinum. Finally, a Penrose drain was placed Norwalk, CT) that was developed specifically for the purpose around the distal esophagus for retrieval during the thoracic of transoral delivery. A gastrotomy is made at the tip of the portion of the operation (Fig. 2). gastric conduit. The 25-mm circular stapler was placed trans- In the second stage of the procedure, the patient was thoracically into the gastric conduit and construction of a repositioned to the left lateral decubitus position. Four tho- stapled esophagogastric anastomosis ensued (Fig. 8). The racic trocars were introduced in the right chest (Fig. 3). The 25-mm circular stapler was used for construction of the right lung was retracted anteriorly for exposure of the medi- thoracic esophagogastric anastomosis as the thoracic esoph- astinal esophagus. The mediastinal pleura overlying the agus seems to accommodate this larger size stapler in com- esophagus was divided. The Penrose drain was identified and parison to the cervical esophagogastric anastomosis, which used for retraction and mobilization of the esophagus from often can only accommodate a 21-mm circular stapler. The the esophageal hiatus up to the level of the azygous vein (Fig. gastrotomy was then stapled closed with a linear stapler (Fig. 4). The azygous vein was isolated and divided with a linear 9). A 28-French chest tube and a Jackson Pratt drain were stapler (Fig. 5). The esophageal specimen and the attached placed for postoperative chest drainage (Fig. 10). gastric conduit were then pulled into the right thoracic cavity. The esophagus was divided at the level of the azygous vein Laparoscopic Proximal Esophagogastrectomy (Fig. 6). The specimen was placed into a protective bag and The laparoscopic proximal esophagogastrectomy was removed through a 4-cm thoracic incision without rib resec- performed in 1 patient with a gastric cardia cancer. The tion. The esophagogastric anastomoses were performed with patient was placed in a supine position. Pneumoperitoneum the linear stapler, hand-sewn, or circular stapler technique was established, and 5 abdominal ports were placed. The with the circular stapler being the preferred technique. In the greater curvature of the stomach was mobilized with preser- © 2008 Lippincott Williams & Wilkins 1083
  4. 4. Nguyen et al Annals of Surgery • Volume 248, Number 6, December 2008 FIGURE 5. Thoracoscopic division of the azygous vein. performed and the mid- and proximal-esophagus was bluntly FIGURE 4. Thoracoscopic esophageal mobilization using the mobilized transhiatally. The esophageal specimen was re- Penrose drain to retract the esophagus. moved through a cervical incision, and a hand-sewn cervical esophagogastric anastomosis was constructed. Although a total laparoscopic transhiatal esophagectomy is feasible, the vation of the right gastroepiploic vessels. The left gastric limiting aspect of this operation is laparoscopic transhiatal vessels were then divided. The gastric conduit was created by mobilization of the middle-third and proximal-third esopha- dividing the stomach, starting on the lesser curvature, and gus. The hand-assisted approach was used in this series to ending at the midaspect on the greater curvature. The distal facilitate mobilization of the mediastinal esophagus. esophagus was circumferentially mobilized through the esophageal hiatus. The esophagus was divided 3 to 4 cm Postoperative Care and Follow-up above the gastroesophageal junction with a linear stapler. The Most patients were extubated in the operating room esophagus was sutured to the left and right cruses of the before transfer to the ICU for cardiorespiratory monitoring. diaphragm to prevent cephalad retraction. A 2-layer hand- Postoperative analgesia was provided by patient-controlled sewn esophagogastric anastomosis was performed. A naso- analgesia. A Gastrograffin contrast study was performed on gastric tube was guided into position in the gastric conduit. postoperative days 3 to 6. The chest tube and nasogastric tube The surgical specimen was placed into a protective bag and were removed when the contrast study demonstrated an intact removed through an enlarged trocar incision. anastomosis. The patient was discharged home with the Jackson Pratt drain in place for removal at the first clinic visit. Hand-Assisted Laparoscopic Transhiatal Supplemental jejunostomy tube feeding was given for 2 to 3 Esophagectomy weeks and the tube was removed thereafter. Patients were The hand-assisted laparoscopic transhiatal esophagec- seen for follow-up at 3-month intervals for a year and yearly tomy was performed in 5 patients. Each patient was placed in thereafter. Computed tomography scans of the chest and a supine position and pneumoperitoneum was established. abdomen were performed yearly after surgery for patients The gastric conduit was constructed, and the distal esophagus with cancer. Pathologic staging was based on histologic was circumferentially mobilized through the esophageal hia- examination of the resected specimen and categorized ac- tus. At this point, an 8-cm subxiphoid midline incision was cording to the TNM staging system of the American Joint 1084 © 2008 Lippincott Williams & Wilkins
  5. 5. Annals of Surgery • Volume 248, Number 6, December 2008 Minimally Invasive Esophagectomy FIGURE 7. The anvil is placed within the esophageal stump and a gastrotomy is performed at the tip of the gastric conduit. FIGURE 6. Thoracoscopic division of the proximal esophagus at the level of the azygous vein using a linear stapler. Commission on Cancer. Anastomotic stricture was defined as patient’s symptoms of dysphagia and/or postprandial vomit- ing in combination with an endoscopy showing a narrowed esophagogastric anastomosis, which impedes the passage of a 9.8-mm endoscope. Statistical Analysis Data are expressed as mean SD. Differences in blood loss and operative time in the first 50 cases compared with latter cases were determined using 2-sample t-tests. For categorical data, differences were analyzed using 2 tests. Statistical analysis was performed using Statistix software, version 8 (Tallahassee, FL). A P value of less than or equal to 0.05 was considered statistically significant. RESULTS Patient Demographics Of the 104 patients, there were 77 males and 27 females with a mean age of 65 years. The indications for an esopha- gectomy are listed in Table 1. Esophageal resections were performed for esophageal cancer (n 78), Barrett esophagus FIGURE 8. The 25-mm circular stapler is placed transthoraci- with high-grade dysplasia (n 8), gastric cardia cancer (n 7), cally into the gastric conduit in preparation for construction gastrointestinal stromal tumor (n 3), and benign stricture of the esophagogastric anastomosis. © 2008 Lippincott Williams & Wilkins 1085
  6. 6. Nguyen et al Annals of Surgery • Volume 248, Number 6, December 2008 TABLE 1. Indications for Minimally Invasive Esophagectomy Indications for Esophagectomy n Carcinoma or premalignant lesion Lower-third esophagus cancer 58 Middle-third esophagus cancer 14 Upper-third esophagus cancer 6 Gastric cardia cancer 7 Barrett esophagus with high-grade dysplasia 8 Gastrointestinal stromal tumor 3 Total 96 Benign recalcitrant stricture End-stage gastroesophageal reflux disease 5 Corrosive injury from lye ingestion 3 Total 8 (n 8). Of the 78 patients with esophageal cancer, 11 patients (14%) had squamous cell carcinoma, 1 patient had adenosquamous cancer, and 66 patients (85%) had adenocar- cinoma. The location of esophageal cancer was predomi- nately in the lower-third esophagus (58 patients). Fourteen patients had middle-third esophageal cancer and 6 patients had proximal-third esophageal cancer. Seven patients had FIGURE 9. The tip of the gastric conduit is closed with a lin- gastric cardia cancer. Thirty-five (40%) of 87 patients with ear stapler. esophageal or gastric cardia cancer had preoperative chemo- radiation therapy. Eight patients underwent esophagectomy for benign recalcitrant stricture; 3 of these patients developed a severe stricture from lye ingestion; and the other 5 patients developed grade 4 strictures as a complication of gastro- esophageal reflux. All patients with benign recalcitrant stric- tures underwent multiple unsuccessful attempts at endoscopic dilatation before surgical therapy. Forty (38%) of 104 pa- tients had prior abdominal surgery, 5 patients had prior gastric or esophageal surgery, and 1 patient had a prior Roux-en-Y gastric bypass for the treatment of morbid obesity. The 4 types of MIEs performed in this series are listed in Table 2. The preferred MIE operation changed in this series. In the first 50 cases, 41 of the 50 operations were the thoracoscopic and laparoscopic esophagectomy with a cervi- cal anastomosis. After the 50th case, the approach in 46 of 54 operations was the entirely laparoscopic and thoracoscopic Ivor Lewis esophagectomy. The first 31 patients had a pylo- roplasty, whereas a pyloroplasty was not performed in the latter cases. The stomach was used as the esophageal substi- TABLE 2. Types of Minimally Invasive Esophagectomy Procedures n 104 Laparoscopic and thoracoscopic Ivor Lewis 51 resection Thoracoscopic and laparoscopic esophagectomy 47 with a cervical anastomosis FIGURE 10. Final intraoperative view showing a reinforced Hand-assisted laparoscopic blunt transhiatal 5 gastric conduit staple line. A nasogastric tube is positioned esophagectomy within the gastric conduit, and a chest tube is placed in the Laparoscopic proximal gastrectomy 1 pleural space for postoperative drainage. 1086 © 2008 Lippincott Williams & Wilkins
  7. 7. Annals of Surgery • Volume 248, Number 6, December 2008 Minimally Invasive Esophagectomy tute in 102 (98%) of 104 patients. The remaining 2 patients blood transfusions during or after operation. The most com- had colonic interposition. mon reason for perioperative transfusion was a low preoper- ative blood count. The median length of ICU stay was 2 days Operative Data (range, 1– 43), and the median length of hospital stay was 8 The mean overall operative time was 291 88 minutes days (range, 4 – 60). Compared with the initial 50 cases, (range, 150 –520). The mean operative time for thoracoscopic operative experience in the latter cases was associated with a and laparoscopic esophagectomy with a cervical anastomosis shorter operative time (242 vs. 350 minutes, respectively) and was 333 75 minutes, and the mean operative time for lower blood loss (142 vs. 300 mL, respectively); however, laparoscopic and thoracoscopic Ivor Lewis resection was there are no significant differences between groups with 249 72 minutes (Table 3). The mean estimated blood loss regard to length of stay, morbidity, and mortality. was 220 224 mL (range, 50 –1000 mL). Thoracoscopy was unsuccessful as a result of dense pulmonary adhesions in 1 Morbidity patient and that patient underwent a laparoscopic hand-as- Major complications are shown in Table 4. Major sisted blunt transhiatal esophagectomy. Three (2.9%) of 104 complications occurred in 13 (12.5%) of 104 patients (includ- patients underwent conversion from laparoscopy to laparot- ing the 3 surgical deaths). Six patients had a gastrointestinal omy; 1 patient had bleeding during division of the left gastric leak requiring reoperation; 4 patients had an anastomotic vessels, 1 patient required a colonic interposition, and the last intrathoracic leak requiring thoracoscopic or thoracotomy patient had bleeding at the splenic hilum requiring iatrogenic drainage; 1 patient had a leak at the body of the gastric splenectomy. There were no conversions from thoracoscopy conduit from a nasogastric tube perforation; and the last to thoracotomy. Thirteen (12.5%) of 104 patients required patient developed a leak at the gastric conduit staple-line. Prolonged respiratory failure occurred in 1 patient. Pulmo- nary embolism occurred in 2 patients. One patient developed TABLE 3. Outcomes According to Type of Minimally intraabdominal hemorrhage on postoperative day 6, when Invasive Esophagectomy (MIE) heparin was started for rate-controlled atrial fibrillation. There was no significant difference in the leak rate between Demographics and MIE With Cervical MIE With Thoracic patients who underwent gastric ischemic conditioning com- Outcomes Anastomosis* Anastomosis pared with patients who did not undergo gastric ischemic No. operations 47 51 conditioning (5% vs. 9.4%, respectively, P .7). There was Gender: males (%) 83 65 also no significant difference in the leak rate between patients Age (yrs) 65 10 64 12 who had a pyloroplasty compared with patients who did not Operative time (min) 333 75† 249 72 undergo pyloroplasty (9.7% vs. 6.8%, respectively; P 0.7). Estimated blood loss (mL) 263 179† 146 117 Minor complications occurred in 15.4% of patients Length of hospital stay (d) 12.1 12.2 9.7 8.1 (Table 5). Four patients with cervical leak were controlled Length of ICU stay (d) 4.8 9.1 2.9 4.4 with neck wound drainage without the need for reoperation. Major complications (%) 12.8 11.8 One patient with a colonic interposition developed a loculated Patients requiring 12.8 9.8 intrathoracic abscess not communicating with the anastomo- transfusion (%) sis. The abscess was drained percutaneously and resolved Anastomotic stricture (%) 23.4 27.5 with antibiotics. Late complications occurred in 32.7% of Leaks (%) 6.4 9.8 patients. The most frequent late complication was anasto- *Hand-assisted procedures were excluded from this group. † motic stricture (26.0%). There were no significant differences P 0.05 compared to MIE Ivor Lewis, 2-sample t tests. in the stricture rate between patients who underwent cervical TABLE 4. Major Complications Patient No. Complications Cause Management Outcome 6 Pulmonary embolism Venous thrombosis Anticoagulation Resolved 9 Respiratory failure Pneumonia Mechanical ventilation Improved 13 Cervical anastomotic leak Ischemia/tension Thoracotomy drainage Improved 21 Intrathoracic anastomotic leak Ischemia Thoracotomy drainage Resolved 22 Intra-abdominal sepsis Bowel obstruction Bowel resection Expired 34 Leak at body of gastric conduit Nasogastric tube Diversion Improved 41 Myocardial infarction Myocardial ischemia Medical support Expired 44 Intra-abdominal bleeding Heparin induced Laparotomy drainage Resolved 64 Gastric conduit staple-line leak Ischemia/tension Diversion Improved 73 Respiratory insufficiency Pneumonia Respiratory support Resolved 74 Intrathoracic anastomotic leak Ischemia/tension Thoracotomy drainage Resolved 98 Intrathoracic anastomotic leak Nasogastric tube Esophageal stent Resolved 102 Pulmonary embolism Venous thrombosis Anticoagulation Expired © 2008 Lippincott Williams & Wilkins 1087
  8. 8. Nguyen et al Annals of Surgery • Volume 248, Number 6, December 2008 TABLE 5. Minor and Late Complications showed a large saddle pulmonary embolus. Attempts at percutaneous embolectomy were unsuccessful, and the pa- Complications n tient ultimately expired. Minor complications Cervical anastomotic leak 4 Pathology and Follow-up Hoarseness 2 The mean number of lymph nodes harvested in malig- Pleural effusion requiring thoracentesis 2 nant cases was 13.8 8.6. There were no significant differ- Pneumonia 2 ences in the number of lymph node retrieved between oper- Wound infection 2 ative approaches with cervical or thoracic anastomosis. The Urinary tract infection 1 number of harvested lymph nodes was also similar between Intrathoracic abscess 1 malignant and benign cases (13.8 8.6 vs. 10.1 10.9, Dislodged jejunostomy tube 1 respectively; P 0.2). Of the 96 patients with carcinoma or Bilateral adrenal hemorrhage 1 Barrett esophagus with high-grade dysplasia, 1 patient had a Total 16 (15.4%) positive distal surgical margin for cancer. This patient had a Late complications large distal esophagus cancer with involvement of gastric Anastomotic stricture 27 cardia along the lesser curvature and underwent a laparo- Delayed gastric emptying 6 scopic and thoracoscopic Ivor Lewis resection. Esophageal diaphragmatic herniation 1 Nine (25.7%) of 35 patients who underwent neoadju- Jejunostomy site enterocutaneous fistula 1 vant therapy had a complete response with no viable tumor Total 35 (33.7%) remaining in the surgical specimen. Two additional patients had complete response in the esophageal specimen but had metastatic residual disease present in the surrounding lymph nodes. According to the postsurgical pathology, there were 11 esophagogastrostomy using hand-sewn versus circular stapler patients with stage 0 disease (including patients with Barrett technique. Twenty-five (92.6%) of 27 patients with stricture esophagus and high-grade dysplasia or carcinoma in situ), 14 had good relief with endoscopic balloon dilatation. Two patients with stage I, 32 patients with stage II, 31 patients patients required endoscopic placement of a temporary cov- ered stent. Another frequent late complication was delayed with stage III, and 5 patients with stage IV disease. At a mean gastric emptying. One (3.2%) of 31 patients who had a follow-up of 54 months (range, 8 –114 months), the 5-year pyloroplasty developed delayed gastric emptying, whereas 5 survival for stages 0 and I, II, III, and IV were 96%, 69%, (6.8%) of 73 patients without a pyloroplasty developed de- 20%, and 0%, respectively, as shown in the Kaplan-Meier layed gastric emptying symptoms. All patients with delayed survival curve (Fig. 11). At follow-up, there had been no gastric emptying were successfully treated with endoscopic tumor recurrence at the thoracic or cervical surgical incisions. balloon dilatation with or without Botulinum toxin injection. One patient developed an abdominal wound cancer recur- One patient who maintained the jejunostomy tube for a rence in conjunction with distant disease. prolonged period of time for nutritional support while obtain- ing postoperative chemotherapy developed a jejunal-cutane- DISCUSSION ous fistula at the jejunostomy site. In this series of 104 consecutive patients, MIE is demonstrated to be technically feasible, safe, associated with Mortality a low conversion rate (2.9%), short length of hospital stay The 30-day morality rate was 1.9%, and the in-hospital (median 8 days), and acceptable morbidity and mortality mortality rate was 2.9%. One patient who underwent a (2.9%). The most important lesson learned in this series was thoracoscopic and laparoscopic esophagectomy with a cervi- the detail of the operative technique for this complex, mini- cal anastomosis died on postoperative day 7 from a myocar- mally invasive operation. For esophageal and gastric cardia dial infarction. Another patient who underwent a thoraco- cancer, the choice of a particular minimally invasive ap- scopic and laparoscopic esophagectomy with a cervical proach to esophagectomy in this series was based on the anastomosis developed a bowel obstruction from a Richter location of the tumor and its extension. Our primary goal was hernia at the 12 mm, bladed trocar site requiring a small to achieve a negative macroscopic and microscopic resection bowel resection; this patient later developed an intraabdomi- margin. For patients with distal-third esophageal cancer, we nal leak at the small bowel anastomosis with intraabdominal initially preferred the combined thoracoscopic and laparo- sepsis and died of multiorgan failure on postoperative day 41. scopic approach with construction of a cervical anastomosis.5 We attributed this complication to the use of bladed trocars as This technique was chosen due to the inherent advantages we do not routinely close 12 mm, nonbladed trocar sites at the such as the ability to detect and treat an anastomotic leak in current time. The last patient underwent laparoscopic and the postoperative period. Additionally, a chest anastomosis thoracoscopic Ivor Lewis esophagogastrectomy developed was avoided due to the technical challenges of performing a bilateral adrenal hemorrhage on postoperative day 5 and was thoracoscopic esophagogastrostomy. However, construction treated conservatively with discontinuation of prophylactic of a neck anastomosis is not necessary a safer alternative. anticoagulation. Upon discharge on postoperative day 11, this Disadvantages of a neck esophagogastrostomy include exces- patient developed hypoxemia, respiratory insufficiency, and sive tension on the anastomosis, an ischemic tip of the gastric hemodynamic instability. A CT angiogram of the chest conduit resulting in a higher leak rate, risk for recurrent 1088 © 2008 Lippincott Williams & Wilkins
  9. 9. Annals of Surgery • Volume 248, Number 6, December 2008 Minimally Invasive Esophagectomy FIGURE 11. Kaplan-Meier survival plot, according to stage of disease, for 93 patients treated with minimally invasive esophagectomy for esopha- geal or gastric cardia cancer, or Bar- rett esophagus with high-grade dys- plasia. Survival plot includes surgical deaths. laryngeal nerve injury, and development of postoperative To date, the largest published study of MIE was re- oropharyngeal dysfunction. In 2000, we performed the first ported by Luketich et al.4 In that study, they reported the totally laparoscopic and thoracoscopic Ivor Lewis resection outcomes in 222 patients who underwent primarily the tho- in a patient with gastric cardia cancer, requiring resection of racoscopic and laparoscopic esophagectomy with a cervical the gastric cardia and fundus whereby a cervical anastomosis anastomosis. A cervical anastomosis was chosen, again, due is not a feasible option.7 Although feasible, the thoracoscopic to the ability to detect postoperative anastomotic leak and the construction of an intrathoracic anastomosis was technically technical challenges in performing a thoracoscopic anasto- challenging. By 2003, our technique evolved to predomi- mosis. They reported a conversion rate of 7.2% (5.4% to nately the laparoscopic and thoracoscopic Ivor Lewis ap- thoracotomy and 1.8% to laparotomy). The median ICU stay proach. This technique continues to be the current preferred was 1 day, and the median hospital stay was 7 days. The leak operation for distal esophageal and gastric cardia cancer even rate was 11.7% with a 30-day mortality of 1.4%. The in- if construction of a cervical anastomosis is feasible. However, hospital mortality was not reported. Luketich and coworkers9 the debate between transhiatal and transthoracic esophagec- subsequently published their results on 50 patients who un- tomy continues in the literature. Even esophagectomy for derwent a minimally invasive Ivor Lewis esophagectomy. benign disease, we favor the laparoscopic and thoracoscopic Construction of the esophagogastric anastomosis was per- Ivor Lewis resection with an intrathoracic anastomosis rather formed through a mini-thoracotomy in most cases with only than a transhiatal approach with a cervical anastomosis. 15 (30%) of 50 patients having a thoracoscopic construction Important advantages in construction of a chest anastomosis of the esophagogastric anastomosis. The leak rate in that include the ability to resect the tip of the gastric conduit, series was 6% with an operative mortality of 6%. In the which is the most ischemic portion, and that the anastomosis current study, all of the 51 patients who underwent laparo- is not under excessive tension.8 The Ivor Lewis approach is scopic and thoracoscopic Ivor Lewis esophagectomy had also less invasive as it avoids the need for exposure and construction of a thoracoscopic esophagogastric anastomosis resection of the cervical esophagus while avoiding a thora- without the need for conversion to a thoracotomy. cotomy. In this series, the entirely laparoscopic and thoraco- Other lessons learned with regard to the technical detail scopic Ivor Lewis resection was associated with a shorter of the operation include the use of preoperative gastric operative time and less blood loss compared with the thora- ischemic conditioning, omission of a pyloroplasty, technical coscopic and laparoscopic esophagectomy with cervical anas- detail for construction of the thoracoscopic esophagogastric tomosis. For long segment Barrett esophagus and proximal anastomosis, and suture inversion of the gastric conduit esophageal cancer, the thoracoscopic and laparoscopic staple-lines. There is a risk of gastric stasis and gastric outlet esophagectomy with a cervical anastomosis is the ap- obstruction after vagotomy associated with esophagectomy.10 proach of choice. Pyloroplasty is commonly performed during an open esoph- © 2008 Lippincott Williams & Wilkins 1089
  10. 10. Nguyen et al Annals of Surgery • Volume 248, Number 6, December 2008 agectomy to prevent the risk of delayed gastric emptying in transhiatal esophagectomy to avoid the chest, where thora- the postoperative period. We performed a pyloroplasty in our coscopy with adhesiolysis is a difficult and time-consuming initial 31 MIE cases with 1 patient (3.2%) developing delayed task. If a surgical option is proposed for a patient with T4 gastric emptying. Our technique has since evolved to con- disease, a thoracotomy is still the procedure of choice. Pre- struct a tubular gastric conduit rather than leaving a large vious gastric surgery is not a contraindication to MIE. In this gastric reservoir. Construction of the gastric conduit into a series, 1 patient had a prior Roux-en-Y gastric bypass for the tube improves gastric emptying. Bemelman et al11 reported treatment of morbid obesity and another patient had a prior that patients with a tubulized stomach without pyloroplasty laparoscopic Nissen fundoplication. Both of these patients have the lowest incidence of delayed gastric emptying com- underwent successful laparoscopic and thoracoscopic Ivor pared with patients with whole stomach as the conduit (3% Lewis resections without the need for conversion to open vs. 38%, respectively). In our series of 73 cases without a surgery. In the patient with a history of Roux-en-Y gastric pyloroplasty, there was a 6.8% rate of delayed gastric emp- bypass, the esophagus, the gastrojejunostomy, and the entire tying. However, treatment consisting of endoscopic balloon Roux limb were resected. The gastric remnant was then used dilatation, with or without Botulinum toxin injection, was to reestablish intestinal continuity.14 During the period of this successful in all cases. Hence, pyloroplasty during MIE is no study, only 1 patient was advised to undergo definitive longer routinely performed as its benefits (improves gastric chemoradiation therapy or an open esophagectomy because emptying) does not outweigh its risks (leak at surgical site) of liver cirrhosis with portal hypertension. and increase in operating time. We have also adopted the The outcomes of MIE in this series seem to be compa- practice of preoperative ischemic gastric conditioning.6 This rable to those of transthoracic and transhiatal series.15–22 practice arose from the work of Akiyama et al,12 who per- Operative times in this series have improved from 350 min- formed preoperative embolization of the left gastric and utes in the first 50 cases to 242 minutes in the latter cases, splenic vessels and found a significant improvement in gastric which is now shorter than most reports for open esophagec- blood flow within the conduit at the time of esophagectomy. tomy (256 –331 minutes). The improvement in operative time Additionally, Holscher et al13 reported that laparoscopic isch- in this series is attributed to standardization of the steps of the emic conditioning of the gastric conduit is feasible and safe operation and the surgeon’s improvement in laparoscopic and and may contribute to the reduction of postoperative morbid- thoracoscopic skills. The rate of major complications in ity and mortality after 83 esophagogastrectomy with gastric this series was 12.5% with an anastomotic leak rate of pull-up. In this study, some patients in the latter part of our 9.6%. These leak rates are comparable to the leak rates for series underwent laparoscopic staging with interruption of the open transthoracic and transhiatal esophagectomies (4.6%- left gastric vessels. With regard to the technical detail of 16%).15–22 The types of major complications observed in our construction of a thoracic anastomosis, the thoracoscopic series are also similar to those following open esophagec- esophagogastric anastomosis had been constructed using tomy. Therefore, we do not believe that major complications hand-sewn, linear stapler, and circular stapler techniques. However, the current preferred anastomotic technique is the are necessarily related to the laparoscopic or thoracoscopic use of a circular stapler with the anvil placed transorally to techniques. There were 2 emergent intraoperative conver- position in the esophageal stump.8 The circular stapler is sions to laparotomy due to bleeding during division of the left placed transthoracically between the ribs, through the tip of gastric vessels in 1 patient and the short gastric vessels in the opened gastric conduit, for construction of an end-to-side another patient with a history of Child’s C liver cirrhosis. In esophagogastric anastomosis. A gastrotomy is performed at this series, anastomotic strictures occurred in 26% of patients. the tip of the gastric conduit, the most ischemic portion of the The rate of anastomotic stricture after open esophagectomy conduit, and is then resected with a linear stapler. This has been reported to be 10% to 36%.16 –18,22 Finally, the technique was developed from our experience with laparo- in-hospital mortality in this series was 2.9%, which is com- scopic construction of an end-to-side gastrojejunostomy us- parable to that of open esophagectomy (2.1%-6% from large ing the 25-mm circular stapler during laparoscopic gastric published series).22,23 A major determinant of outcome after bypass for the treatment of morbid obesity. We routinely esophagectomy is the annual hospital’s volume. Patti et al24 oversew the circular anastomosis with several interrupted, reported that hospital performing more than 6 esophagecto- tension, relieving sutures. Finally, although uncommon, an- mies per year have a 4.8% mortality compared with a mor- other reason for postoperative leaks is breakdown of the tality rate of 16% in hospital performing less than 6 opera- gastric conduit staple-lines. In this series, 1 patient developed tions per year. Although this study did not compare the a large dehiscence of the gastric conduit staple-line. Routine outcome of minimally invasive to that of open surgery, our suture inversion of the gastric conduit staple-line is now a group previously compared the outcomes of MIE to that of standard practice at our institution. open transhiatal and transthoracic esophagectomy and found There are few relative contraindications for MIE, which that patients who underwent MIE had shorter operative times, include morbid obesity and T4 cancers. Thoracoscopy is less blood loss, fewer transfusions, and shortened intensive technically challenging to perform in morbidly obese patients care unit and hospital courses than patients who underwent (body mass index greater than 40). In the obese and in transthoracic or blunt transhiatal esophagectomy.25 However, patients with a previous right thoracotomy, we favor the additional studies including a prospective, multicenter, ran- hybrid approach using the laparoscopic hand-assisted blunt domized trial comparing the outcomes of minimally inva- 1090 © 2008 Lippincott Williams & Wilkins
  11. 11. Annals of Surgery • Volume 248, Number 6, December 2008 Minimally Invasive Esophagectomy sive esophagectomy to that of open esophagectomy are 6. Nguyen NT, Longoria M, Sabio A, et al. Preoperative laparoscopic needed. ligation of the left gastric vessels in preparation for esophagectomy. Ann Thorac Surg. 2006;81:2318 –2320. 7. Nguyen NT, Follette DM, Lemoine PH, et al. Minimally invasive Ivor CONCLUSION Lewis esophagectomy. Ann Thorac Surg. 2001;72:593–596. Minimally invasive esophagectomy is safe and effec- 8. Nguyen NT, Longoria M, Chang K, et al. Thoracolaparoscopic modifi- tive and offers a reasonable alternative to the conventional cation of the Ivor Lewis esophagogastrectomy. J Gastrointest Surg. 2006;10:450 – 454. open esophagectomy. The low morbidity and mortality in this 9. Bizekis C, Kent MS, Luketich JD, et al. Initial experience with mini- series compares favorably with that observed for an open mally invasive Ivor Lewis esophagectomy. Ann Thorac Surg. 2006;82: esophagectomy. Although controversy continues as to the 402– 407. best operative approach for open esophagectomy (transhiatal 10. Fok M, Cheng SW, Wong J. Pyloroplasty versus no drainage in gastric vs. transthoracic), lessons learned from this large experience replacement of the esophagus. Am J Surg. 1991;162:447– 452. 11. Bemelman WA, Taat CW, Slors JF, et al. Delayed postoperative emp- of minimally invasive esophagectomy favor the entirely lapa- tying after esophageal resection is dependent on the size of the gastric roscopic and thoracoscopic Ivor Lewis resection with con- substitute. J Am Coll Surg. 1995;180:461– 464. struction of a tension-free, intrathoracic esophagogastric 12. Akiyama S, Kodera Y, Sekiguchi H, et al. Preoperative embolization anastomosis using a circular stapler. The stomach is the pre- therapy for esophageal operation. J Surg Oncol. 1998;69:219 –223. ferred conduit and a pyloroplasty can be safely omitted. Because 13. Holscher AH, Schneider PM, Gutschow C, et al. Laparoscopic ischemic of the technical complexity of this challenging gastrointestinal conditioning of the stomach for esophageal replacement. Ann Surg. 2007;245:241–246. operation, minimally invasive esophagectomy has not been 14. Nguyen NT, Tran CL, Gelfand DV, et al. Laparoscopic and thoraco- widely adopted. Surgeons interested in learning this complex scopic Ivor Lewis esophagectomy after Roux-en-Y gastric bypass. operation should attend a mini-fellowship with an appropriate J Gastrointest Surg. 2006;82:1910 –1913. balance of lectures, laboratory, and clinical experience. Mini- 15. Swanson SJ, Batirel H, Bueno R, et al. Transthoracic esophagectomy mally invasive esophagectomy should continue to be performed with radical mediastinal and abdominal lymph node dissection and cervical esophagogastrostomy for esophageal carcinoma. Ann Thorac at centers with a high volume of open and laparoscopic esoph- Surg. 2001;72:1918 –1925. ageal surgery and by surgeons with experience in advanced 16. Millikan KW, Silverstein J, Hart V, et al. A 15-year review of esopha- laparoscopic and thoracoscopic techniques. Lastly, similar to the gectomy for carcinoma of the esophagus and cardia. Arch Surg. 1995; development of other minimally invasive surgical operations, 130:617– 624. there certainly will be scrutiny by the surgical community, 17. Graham AJ, Finley RJ, Clifton JC, et al. Surgical management of adenocarcinoma of the cardia. Am J Surg. 1998;175:418 – 421. particularly during the developmental stage. The evolution of 18. Gluch L, Smith RC, Bambach CP, et al. Comparison of outcomes minimally invasive esophagectomy will surely follow a similar following transhiatal or Ivor Lewis esophagectomy for esophageal path and only time will ensure that the most logical and least carcinoma. World J Surg. 1999;23:271–275. invasive approach to esophagectomy will prevail. 19. Orringer MB, Marshall B, Iannettoni MD. Transhiatal esophagectomy: clinical experience and refinements. Ann Surg. 1999;230:392– 400. REFERENCES 20. Anikin VA, McManus KG, Graham AN, et al. Total thoracic esopha- 1. Nguyen NT, Root J, Zainabadi K, et al. Accelerated growth of bariatric gectomy for esophageal cancer. J Am Coll Surg. 1997;185:525–529. surgery with the introduction of minimally invasive surgery. Arch Surg. 21. Lozac’h P, Topart P, Perramant M. Ivor Lewis procedure for epidermoid 2005;140:1198 –1202. carcinoma of the esophagus. A series of 264 patients. Semin Surg Oncol. 2. Nguyen NT, Silver M, Robinson M, et al. Result of a national audit of 1997;13:238 –244. bariatric surgery performed at academic centers: a 2004 university health 22. Karl RC, Schreiber R, Boulware D, et al. Factors affecting morbidity, system consortium benchmarking project. 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