Minimally Invasive Surgery for Esophageal Cancer: Review of the Literature and Institutional Experience

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1 Several minimally invasive techniques for performing esophagectomy are now available. Samuel Bak. BK1484 Followers. Oil on canvas, 18ʺ 24ʺ. Minimally Invasive Surgery for Esophageal Cancer: Review of the Literature and Institutional Experience Maki Yamamoto, MD, Jill M. Weber, MPH, Richard C. Karl, MD, FACS, and Kenneth L. Meredith, MD, FACS Background: Esophageal cancer represents a major public health problem in the world. Several minimally invasive esophagectomy (MIE) techniques have been described and represent a safe alternative for the surgical management of esophageal cancer in selected centers with high volume and surgeons experienced in minimally invasive procedures. Methods: The authors reviewed the most recent and largest studies published in the medical literature that reported the outcomes for MIE techniques. Results: In larger series, MIE has proven to be equivalent in postoperative morbidity and mortality to the open esophagectomy. However, MIE has been associated with less blood loss, reduced postoperative pain, decreased time in the intensive care unit, and shortened length of hospital stay compared with the conventional open approaches. Despite limited data, no significant difference in survival stage for stage has been observed between open esophagectomy and MIE. Conclusions: The myriad of MIE techniques complicates the debate for defining the optimal surgical approach for the treatment of esophageal cancer. Randomized controlled trials comparing MIE with conventional open esophagectomy are needed to clarify the ideal procedure with the lowest postoperative morbidity, best quality of life after surgery, and long-term survival. Introduction Esophageal cancer is the eighth most common cancer in the world, with an estimated 482,300 new cases each year and 406,800 cancer deaths per year. 1 Survival is poor, with a high mortality-to-incidence rate From the Gastrointestinal Tumor Program at the H. Lee Moffitt Cancer Center & Research Institute, Tampa, Florida. Submitted March 6, 2012; accepted July 18, Address correspondence to Kenneth L. Meredith, MD, FACS, Gastrointestinal Tumor Program, Moffitt Cancer Center, Magnolia Drive, FOB-2 GI PROG, Tampa, FL Kenneth. Meredith@Moffitt.org No significant relationship exists between the authors and the companies/organizations whose products or services may be referenced in this article. ratio of 84. In the United States, approximately 17,460 patients are diagnosed with esophageal cancer each year, with a mortality of 15,070 (incidence and death rates are standardized to age for the 2000 US standard million population). 2 According to Surveillance, Epidemiology and End Results data, 5-year survival rates for esophageal cancer have improved modestly throughout the last 30 years, from 5% between 1975 and 1977 to 19% between 2001 and Surgical resection has been the gold standard for localized esophageal cancer for decades. However, due to a poor 5-year survival rate, which is approximately 36% in patients undergoing esophagectomy, numerous clinical trials have investigated 130 Cancer Control April 2013, Vol. 20, No. 2

2 the role for multimodality therapy. 3,4 A review of randomized controlled trials evaluating neoadjuvant chemoradiotherapy vs surgery alone demonstrated no major difference in overall survival. 5 However, all the studies in the review were inconsistent with their regimens of chemotherapy, doses of radiotherapy, timing of chemotherapy in conjunction with radiotherapy, surgical procedure performed, and histologic subtypes enrolled in the trials. Furthermore, esophagectomy has the highest mortality among all elective gastrointestinal surgery, with rates as high as 23%. 6 Reductions in surgical mortality up to 32% have been attributable to specialized high-volume centers. 7-9 Advances in surgical technology, staging, and perioperative care could further impact a reduction in surgical morbidity and mortality. Of these advances, minimally invasive esophagectomy (MIE) has the greatest potential to improve outcomes in patients who undergo esophageal surgery. Minimally invasive procedures involving laparoscopic surgery, thoracoscopic surgery, or both are the mainstay surgical approach for a variety of benign esophageal disorders and are associated with equivalent functional results compared with open procedures. 10 These techniques offer the potential advantages of enhanced recovery, a reduction in pain, and a quicker return to normal function, although larger studies are needed to provide definitive evidence of these benefits. The application of minimally invasive surgery has been explored and found to be feasible in the management of esophageal cancer, although concern has been expressed about its safety, efficacy, oncologic value, and other advantages that justify longer operative times and higher costs. This article discusses MIE indications, techniques, and outcomes in the management of esophageal cancer. Indications for Minimally Invasive Surgery in Esophageal Cancer Patient selection represents the most important factor in MIE. At our institution, all patients with esophageal carcinoma undergo staging with endoscopic ultrasonography, computed tomography (CT) of the thorax and abdomen, and whole-body positron emission tomography/ct scans. Thoracoscopic staging, laparoscopic staging, or both are performed in selected patients who are found to have advanced locoregional disease on imaging studies. The utility of laparoscopy in staging is more relevant with adenocarcinomas of the lower esophagus compared with more proximal tumors. 11 Laparoscopy has been reported to be more sensitive and specific than CT scans in detecting lymph node, peritoneal, and liver metastases. This procedure is safe with low morbidity and avoids unnecessary operative procedures. 12 However, some studies have reported a small yield. 13,14 Therefore, minimally invasive techniques for staging purposes are used mainly at the time of planned surgical extirpation. MIE is indicated in patients with early-stage esophageal cancer and in patients who are diagnosed with Barrett s esophagus with high-grade dysplasia. Neoadjuvant chemotherapy and radiation are routinely recommended for patients with locally advanced esophageal cancer. We and other investigators 15,16 have found that MIE can be safely performed in patients who have received neoadjuvant therapy, while others do not recommend the procedure in patients with prior radiation. 17,18 The impact of neoadjuvant therapy has been evaluated in several randomized studies demonstrating that chemoradiotherapy does not significantly increase the morbidity, mortality, or oncologic outcome compared with conventional surgery Therefore, the current standard for patients with locally advanced esophageal cancer who receive neoadjuvant chemoradiation is esophagectomy, and the minimally invasive approach may be offered to these patients without compromising surgical or oncologic outcomes. Contraindications for MIE Contraindications to thoracoscopy include extensive pleural adhesions, prior pneumonectomy, bulky tumors, and locally infiltrative tumors, especially those with airway involvement. Adequate cardiac and pulmonary function is necessary for thoracoscopic MIE due to prolonged single-lung ventilation. 22 Relative contraindications to laparoscopy may include prior abdominal operations and major gastric resections. MIE Techniques Several surgical techniques for the treatment of esophageal cancer are available, and the choice of technique depends on tumor location, extent of lymphadenectomy, and surgeon s preference. The two most frequent open techniques are the transhiatal esophagectomy (THE) and transthoracic (Ivor Lewis) esophagectomy (TTE). 23 Classic THE involves a laparotomy to mobilize the stomach from its vascular attachments and a celiac/left gastric lymphadenectomy, while still preserving the right gastroepiploic vessel for which the future gastric conduit relies on. Variations, including the pyloric drainage procedure, feeding jejunal tube placement, and mobilization (Kocher maneuver) of the duodenum, can be performed during the laparotomy. However, we do not routinely perform pyloric drainage and the Kocher maneuver at our institution. With adequate gastric mobilization, the gastric conduit will routinely have sufficient length without additional duodenal mobilization. In addition, prospective randomized trials have not yielded any long-term benefits from surgical pyloric drainage procedures, 24,25 specifically pyloromyotomy or April 2013, Vol. 20, No. 2 Cancer Control 131

3 pyloroplasty. We routinely perform percutaneous intraoperative injection of 300 U botulinum toxin into the pylorus, which is less invasive than traditional pyloric drainage procedures and improves short-term outcomes. Martin et al 26 retrospectively evaluated 48 patients who underwent intrapyloric botulinum toxin injection during esophagectomy and examined their rate of early vs late delayed gastric emptying. Two patients developed clinically significant delayed gastric emptying in the early postoperative period, while 3 patients developed late symptoms (> 3 months postoperatively) that resolved with endoscopic therapies (dilatation vs endoscopic botulinum injection). This minimally invasive technique eliminates the small but devastating complication of duodenal leak seen in more invasive surgical drainage procedures. Subsequent blunt dissection of the thoracic esophagus is considered an advantage, particularly in patients with poor lung function who may not be able to tolerate thoracotomy. The anastomosis is created with a left cervical incision to form the final cervical esophagogastric anastomosis. 7 By contrast, TTE has an identical abdominal portion of the operation. The blunt thoracic esophageal dissection is replaced with right thoracotomy and meticulous radial dissection around the thoracic esophagus with its surrounding mediastinal lymphatic tissue. The anastomosis is created within the thoracic space rather than the neck. The theoretical advantage with the thoracic approach is the oncologic resection of mediastinal lymph nodes and a wider radial margin of the primary tumor. 27 Other modifications of these two classic approaches include left thoracotomy, thoracoabdominal incision, and the 3-field approach (McKeown procedure). 28,29 Determining which esophagectomy technique will result in less morbidity and increased survival is controversial. Hulscher et al 30 reported their data from a randomized trial involving 220 patients assigned to THE or TTE with extended en-bloc lymphadenectomy. They concluded that perioperative morbidity was higher after TTE but saw no significant difference in in-hospital mortality. THE was associated with a shorter operative time (3.5 vs 6.0 hours), lower median blood loss (1.0 vs 1.9 L), fewer pulmonary complications, decreased chylous leaks, shorter duration of mechanical ventilation, and shorter stay in the intensive care unit (ICU) and hospital. However, after a median follow-up of nearly 5 years, no significant difference was seen in overall survival between the THE and TTE groups (29% and 39%, respectively). A meta-analysis involving 7,527 patients from 50 studies demonstrated no significant difference in morbidity, mortality, or long-term survival. 31 In this analysis, TTE had a higher risk for pulmonary complications, chylous leaks, and wound infection, while THE was associated with an increased incidence of anastomotic leaks and recurrent laryngeal nerve injury. Because no clear consensus has established the ideal surgical resection, MIE has been explored in both TTE and THE approaches with the purpose of overcoming their intrinsic limitations. Multiple minimally invasive approaches to esophagectomy have been described that combine thoracoscopic procedures, laparoscopic procedures, or both with various operative positions for the patient and anastomotic techniques (Table 1). MIE for the management of esophageal cancer was first described by Cuschieri et al 32 in 1992, and it was later refined by Collard et al 33 in These first efforts involved thoracoscopic esophageal mobilization with subsequent laparotomy for gastric mobilization and a cervical anastomosis. This approach avoids the morbidity of thoracotomy and permits a complete and thorough mediastinal dissection. Several groups have reported their experience with excellent results with this technique, which currently represents the most popular MIE technique Refinements in the thoracoscopic technique have been pioneered by Luketich et al, 16,39 who have described thoracolaparoscopic esophagectomy. This technique involves video-assisted thoracoscopic esophageal mobilization in the left lateral decubitus position, followed by supine laparoscopic gastric mobilization and preparation of the gastric conduit with a standard cervical anastomosis. This combination offers the potential benefit of avoiding the need for Table 1. Minimally Invasive Esophagectomy (MIE) Techniques Surgical Technique Abdominal Portion Thoracic Portion Anastomosis Open transthoracic (Ivor Lewis) Open Open Intrathoracic Open transhiatal Open NA Cervical Open 3-field (McKeown) Hybrid transthoracic Open Open Cervical Laparoscopic or hand-assisted Open Intrathoracic Hybrid transthoracic Open Thoracoscopic Intrathoracic Hybrid 3-field Open Thoracoscopic Cervical MIE 3-field MIE transthoracic MIE transhiatal NA = not applicable. Laparoscopic or hand-assisted Laparoscopic or hand-assisted Laparoscopic or hand-assisted Thoracoscopic Thoracoscopic NA Cervical Intrathoracic Cervical 132 Cancer Control April 2013, Vol. 20, No. 2

4 thoracotomy and laparotomy, while minimizing pain in the postoperative period and possibly leading to rapid recovery. A minimally invasive THE was initially described by DePaula et al 40 in 1995 and then by Swanstrom and Hansen 41 in 1997 as the first totally laparoscopic esophagectomy. This procedure has been utilized by other groups and has undergone several modifications The main advantage is direct visualization of the lower mediastinum without blind dissection. Using this technique, a laparotomy is avoided. To facilitate the abdominal procedure, some groups use a laparoscopic-assisted hand-port system, which provides more tactile control and may potentially decrease operative time. 45 Furthermore, a handassisted system may be used in the thoracoscopic phase of the procedure to facilitate exposure into the right thoracic cavity (hand-assisted laparoscopic and thoracoscopic surgery). 46 Other modifications to this technique include a thoracoscopic mobilization of the esophagus and mediastinal lymphadenectomy in the prone position. 47 The main advantages described for prone thoracoscopic mobilization of the esophagus are shorter anesthesia time and better postoperative respiratory function compared with the left lateral position. 47 Additional modifications to MIE involve the use of mediastinoscopic methods to aid superior mediastinal dissection. 48,49 This has been explored in conventional THE and laparoscopic esophagectomy. A mediastinoscope is used for dissection of the upper mediastinum. The utility of this approach is limited by the extent of possible lymph node dissection. Other techniques to aid mediastinal dissection involve placing the laparoscopic trocars into the neck to facilitate esophageal mobilization of the upper mediastinum. 50,51 The mediastinoscopic technique is not routinely performed due to technical limitations and rarely offers any additional benefit. Robotic Esophagectomy Some limitations of the laparoscopic and thoracoscopic approaches to esophagectomy include instrumentation, the narrow field of the mediastinum, and the two-dimensional view of conventional equipment. Robotic systems provide the possibility to overcome some of these limitations. Some groups have reported their early experience with robotically assisted THE This involves laparoscopic gastric mobilization, mediastinal robotic dissection, and conventional transhiatal dissection through the cervical incision. This technique allows three-dimensional visualization, improved magnification, and a greater range of instrument motion. This potentially could diminish intraoperative complications during the esophageal dissection in the mediastinum. At our institution, we have begun to utilize this technology with our approach to esophagectomy. The robotic technique can be performed during the thoracic dissection of the esophagus, gastric mobilization, and intrathoracic anastomosis. It can also be performed in combination with laparoscopic, hand-assisted laparoscopic, or thoracoscopic approaches. For the robotic abdominal approach, three 8-mm ports are placed, one in the right subcostal location and two in the left subcostal position. The camera is placed in the supraumbilical position and a 10-mm assistant port is placed in the right paramedian location. A Nathanson liver retractor is placed through a small stab incision in the subxiphoid area. The laparoscopic approach has a similar location as the ports (with the 8-mm ports exchanged for 5-mm ports), and only one is placed in the right subcostal and one is placed in the left subcostal region. The assistant and camera ports are in the same location. The hand-assisted approach requires a 5-cm right subcostal incision, which allows for the placement of the GelPort device (Applied Medical, Rancho Santa Margarita, CA). Two additional 5-mm trocars are placed in the left subcostal and left paramedian locations. The feeding jejunostomy is brought out through a port site on the left for all approaches, thus eliminating an additional incision. After insufflation is performed, the abdomen is inspected for evidence of metastatic or locally unresectable disease. The stomach is mobilized away from its vascular attachments, protecting the right gastroepiploic pedicle. The short gastric vessels are transected using a Harmonic scalpel. The left gastric vessels are dissected down to the origin of the celiac artery and transected using a vascular stapler to complete the upper abdominal lymphadenectomy. The pylorus is then injected with botulinum toxin. The gastric conduit is created using several firings of the surgical stapler. A feeding jejunostomy tube is placed through one of the left abdominal trocar sites. The patient is then placed in the left lateral decubitus position and the right lung is deflated. The thorax is entered into the fifth intercostal space using a 10-mm port. Two additional ports are placed, one in the ninth intercostal space (4-cm incision to be shared by the assistant and one of the robot arms) and another in the third intercostal space. The azygos vein is isolated and transected using a vascular stapler. The esophagus is meticulous dissected en bloc with surrounding mediastinal lymph nodes. The specimen is removed and margins are checked with pathology. The final intrathoracic anastomosis has been described with a variety of stapled vs sewn techniques. 55 The recent introduction of a transoral circular stapler has obviated the need for the technical expertise in securing a free anvil in the esophageal remnant. The anastomotic leak rate (0%9.8%) with April 2013, Vol. 20, No. 2 Cancer Control 133

5 this new technique is comparable with other stapled techniques. 56,57 An omental pedicle flap is then placed over the anastomosis. MIE Outcomes Major intraoperative complications, including bleeding, tracheobronchial injury, and recurrent laryngeal nerve injury, have been reported with MIE Conversion to open surgery is required in approximately 10% of patients. 16,34,39 As surgical techniques improve, incidence of intraoperative complications could potentially decrease. MIE is a technically advanced surgical procedure with a prolonged learning curve. Technical complications are known to be operator-, technique-, and instrument-dependent. It has been reported that a minimum of 17 cases were necessary to acquire MIE skills, and more than 35 cases were needed to see an outcomes difference. 22,62 Most of the major complications in MIE were described in initial experience series; therefore, the full potential may not have been realized. Finally, because of the multitude of existing MIE techniques, the ability to compare results with those of conventional esophagectomy is difficult (Table 2). 16,35,47,62-67 In theory, obviating the need of a thoracotomy, laparotomy, or both may reduce postoperative pain, wound infections, ventilator dependence, cardiopulmonary complications, ICU and hospital stays, and mortality rates. However, a clear advantage with MIE over conventional esophagectomy has not been demonstrated. 63 Reasons for a lack in difference in postoperative outcomes may result from an inability to detect differences in small series and historic control comparisons. The lack of well-designed trials, publication bias of satisfactory outcomes, and the myriad of MIE techniques complicate this debate. Smithers et al 64 reported outcomes after esophagectomy and compared 114 patients with open procedures, 309 patients with a thoracoscopic-assisted approach, and 23 patients with a total thoracoscopic/ laparoscopic approach. Operative time was not sig- Table 2. Review of Minimally Invasive Esophagectomy (MIE) Studies Study Surgical Technique No. of Patients EBL (cc) Operative Time (min) Length of Hospital Stay (d) Morbidity (%) Anastomotic Leak (%) Mortality (%) 5-yr Survival (%) Luketich 16 MIE Nguyen 65 MIE a Osugi 62 T Yamamoto 35 T Palanivelu 47 T/L prone a Smithers 64 Open a T MIE Meredith 63 Open (Ivor Lewis) MIE (TH) Hybrid Luketich 66 MIE (Ivor Lewis) MIE (3-field) Sihag 67 Open MIE EBL = estimated blood loss, L = lymphadenectomy, MIE = combined thoracoscopic and laparoscopic esophagectomy, T = thoracoscopic esophagectomy, THE = transhiatal esophagectomy. a 3-year overall survival. 134 Cancer Control April 2013, Vol. 20, No. 2

6 nificantly different for the open and thoracoscopicassisted groups; however, the total laparoscopic approach took significantly longer than the other two procedures. The total laparoscopic and thoracoscopic-assisted groups were associated with a significant decrease in blood loss and transfusions as well as a shorter length of stay in the ICU and overall hospitalization. Nonetheless, overall complication rates were similar. The incidence of respiratory infections was not different, nor was the need to return to the ICU. The mortality rate was 2.6% in the open group, 2.2% in the thoracoscopic-assisted group, and 0% in the total laparoscopic group. We previously reported our MIE experience with the use of a hand-assist port and recently updated our series to include the hybrid approach (laparoscopic abdominal and minithoracotomy; Table 2). 63 We found no difference in the median operative time between the MIE, hybrid, and open groups (242, 320, and 289 minutes, respectively; P =.059). However, there was a trend toward longer operative times in the hybrid cohort. In addition, we found no differences in blood loss between the MIE and open groups (150, 125, and 250 ml; P =.45). Our data support the concept that MIE is safe and comparable to open surgery. One of the most controversial issues with MIE is whether its disease-free and overall survival rates are comparable with conventional surgery. The role of MIE in esophageal cancer has been questioned because the extent of lymphadenectomy may be compromised. Nevertheless, the largest randomized trial comparing open approaches proved no significant difference in survival between THE and TTE with extended en-bloc lymphadenectomy. 30 With multiple MIE techniques, the quality of lymph node dissection is difficult to evaluate, and many series fail to report on lymph node dissection. The only prospective study that compared this outcome between the open approach and MIE demonstrated no significant difference in the number and location of harvested lymph nodes. 64 Other concerns include the adequacy of microscopically negative (R0) resection, inadequate staging, local recurrence due to inadequate margins, port-site recurrence, and tumor dissemination during MIE. A retrospective study investigated the recurrence patterns in patients undergoing open TTE compared with patients undergoing a thoracoscopic-assisted approach and demonstrated no difference in recurrence rates (local, regional, or distant). 68 In addition, no differences were seen in the ability to achieve R0 margins with either approach. More importantly, comparable long-term survival has been reported in the majority of series when their results are compared with historic controls or to open surgery. 22,34 Smithers et al 64 reported no difference in 3-year survival when open, thoracoscopic-assisted, and total thoracoscopic/ laparoscopic approaches were compared stage for stage. It is clear that surgical oncologic principles, such as adequate margin resections and lymphadenectomy, are feasible with refinements of MIE and the increasing experience of surgeons. In addition, Luketich et al 16 found that at a mean follow-up of 19 months, patients who underwent MIE had quality of life scores comparable with preoperative values. Robotic Outcomes Since robotic technology is relatively recent, data regarding the safety and, more importantly, the oncologic efficacy of this technique are limited. At our institution, the first 50 patients who underwent robotic-assisted TTE were analyzed. 69 Although longterm survival has not been studied, a substitute for oncologic efficacy through the mean number of lymph nodes retrieved (26 ± 9.3) and the percentage of microscopically negative margins (100%) would indicate that robotic approaches are at least equivalent to the open approach. A steep learning curve was illustrated in the decrease in mean operative time (479 minutes for the first half of cases vs 428 minutes for the second half; P <.05) and a decrease in morbidity after 28 cases (35% vs 13%; P =.04). Due to the technologic expertise required for this procedure, this technique should be limited to high-volume centers with surgeons who have substantial experience in both the open approach and MIE. Learning curves associated with historical minimally invasive approaches may also apply to the robotic approach. Conclusions Several minimally invasive esophagectomy (MIE) techniques have been described and represent safe alternatives for the surgical management of esophageal cancer in centers with high volume and surgeons experienced in MIE. In larger series, MIE has proven to have equivalent postoperative morbidity and mortality rates to open esophagectomy. MIE has also been associated with less blood loss, less postoperative pain, and shorter length of stay in the intensive care unit and hospital. Despite limited data, no significant difference in survival has been observed between open approaches and MIE. The myriad of MIE techniques complicates the debate of defining the optimal approach for the treatment of esophageal cancer. Randomized controlled trials comparing MIE with open esophagectomy are needed to clarify the ideal procedure with the lowest postoperative morbidity, the best quality of life, and the longest long-term survival. Robotic approaches may offer advantages over conventional approaches to MIE. However, similar to MIE, these techniques should be performed at high-volume centers by surgeons who have sufficient experience with the open and MIE techniques. April 2013, Vol. 20, No. 2 Cancer Control 135

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