Safety and feasibility of robotic-assisted Ivor–Lewis esophagectomy

Safety and feasibility of robotic-assisted Ivor–Lewis esophagectomy SUMMARY Esophagectomy is associated with substantial morbidity. Robotic surgery allows complex resections to be performed with potential benefits over conventional techniques. We applied this technology to transthoracic esophagectomy to assess safety, feasibility, and reliability of this technology. A retrospective cohort study of all patients undergoing robotic-assisted Ivor–Lewis esophagectomy (RAIL) from 2009 to 2014 was conducted. Clinicopathologic factors and surgical outcomes were recorded and compared. All statistical tests were two-sided and a P-value of <0.05 was considered statistically significant. We identified 147 patients with an average age 66 ± 10 years. Neoadjuvant therapy was administered to 114 (77.6%) patients, and all patients underwent a R0 resection. The mean operating room (OR) time was 415 ± 84.6 minutes with a median estimated blood loss (EBL) of 150 (25–600) mL. Mean intensive care unit (ICU) stay was 2.00 ± 4.5 days, median length of hospitalization (LOH) was 9 (4–38) days, and readmissions within 90 days were low at 8 (5.5%). OR time decreased from 471 minutes to 389 minutes after 20 cases and a further decrease to mean of 346 minutes was observed after 120 cases. Complications occurred in 37 patients (25.2%). There were 4 anastomotic (2.7%) leaks. Thirty and 90-day mortality was 0.68% and 1.4%, respectively. This represents to our knowledge the largest series of robotic esophagectomies. RAIL is a safe surgical technique that provides an alternative to standard minimally invasive and open techniques. In our series, there was no increased risk of LOH, complications, or death and re-admission rates were low despite earlier discharge. INTRODUCTION Esophageal cancer continues to increase in incidence worldwide.1-3 In 2015, there were 16,980 new cases of esophageal cancer and 15,590 deaths from disease in the United States.2 The average age at the time of diagnosis also continues to rise with a peak incidence between 75 and 79 years of age. The long-term survival for patients with locally advanced esophageal cancer remains poor despite improvements in multimodality care over the last several decades. The current approach to locally advanced esophageal cancer includes neoadjuvant chemoradiation (NCR) followed by surgical resection.4 Minimally invasive esophagectomy (MIE) offers several potential advantages over traditional open esophagectomy. The MIE has been found to result in faster recovery time, substantial decrease in blood loss, decrease in postoperative complications and shorter hospitalization, with comparable oncologic outcome.5 Retrospective reviews have demonstrated that MIE does not compromise oncologic principles and is safe compared to traditional open esophagectomy for esophageal cancer.6-10 Moreover, the transthoracic or Ivor–Lewis approach when performed via a minimally invasive approach has the potential to significantly reduce pulmonary complications, a substantial morbidity associated with the open approach. Biere et al. demonstrated in their prospective trial in which patients were randomized to either open esophagectomy or MIE that patients undergoing MIE were less likely to have pulmonary complications and had shorter hospital stays compared to patients undergoing open esophagectomy.11 Robotic-assisted Ivor–Lewis esophagectomy (RAIL) is an emerging technique that allows the surgeon a broader and three-dimensional view of the operative field with the added benefit of improved instrument articulation over standard thoracoscopy. We have previously described the development and implementation of a robotic approach to esophagectomy.12 In this study, we sought to report our large series and examine the safety and feasibility of a robotic-assisted approach in patients undergoing an Ivor–Lewis esophagectomy. METHODS A retrospective cohort study of a prospective robotic esophageal database of 147 consecutive patients undergoing RAIL from 2009 to 2014 was conducted after obtaining study approval from our Institutional Review Board (IRB#15-onc-23). All patients, regardless of age, race, tumor stage, or location, or neoadjuvant therapy were included in the cohort. Patients were required to have a tissue diagnosis of high-grade dysplasia or cancer, but were not excluded based upon histologic variant. Basic demographics, tumor characteristics, operative details, and postoperative outcomes were recorded. Patients were included only if they underwent RAIL. Patients with mid-esophageal tumors who underwent Mckeown or transhiatal esophagectomy were excluded for this analysis. Endpoints and statistical analysis The primary endpoints/feasibility metrics were operating room (OR) time, estimated blood loss (EBL), intensive care unit (ICU) days following surgery, and length of hospitalization (LOH). Secondary end-points and safety metrics included perioperative adverse events (AE) (<90 days following surgery), including pneumonia, cardiac arrhythmia, deep vein thrombosis (DVT)/pulmonary embolism (PE), wound infection, anastomotic leak (AL), as well as 30 and 90-day mortality. Pneumonia was defined as infiltrates on chest radiograph and positive sputum culture. Anastomotic leaks were confirmed by an upper GI study or CT scan. Readmissions and outcomes with and without neoadjuvant therapy were also analyzed. Statistical analysis was performed using the SPSS® version 21.0 (IBM®, Chicago, IL). Continuous variables were compared using the Kruskal–Wallis or the ANOVA tests as appropriate. Pearson's Chi-square test was used to compare categorical variables. All statistical tests were two-sided and a P-value of <0.05 was considered statistically significant. Surgical technique Abdominal phase A single surgeon performed all operations. The surgeon has extensive experience with both open, laparoscopic and thoracoscopic approaches to esophageal resection. The abdomen is entered with a Veress needle supraumbilically. The camera is inserted into a 5-mm port and the abdomen is entered via an optiview technique. Once staging laparoscopy has demonstrated no evidence of metastatic disease, additional 8-mm ports are placed in the right lateral and left lateral positions. A robotic stapling port is placed in the right paramedian location. An assistant port (also to be used for jejunostomy) is placed in the left paramedian location (Fig. 1). A subxyphoid incision is made for the Nathanson liver retractor. The camera port is upsized to an 8 mm (DaVinci XI), or 10 mm (DaVinci SI). The robot is then docked. The gastrocolic attachments are incised inferior to the right gastroepiploic pedicle along the greater curve of the stomach. The vessel sealer is used to take the short gastric vessels. The left and right crural dissection is performed. The esophagus is encircled with a Penrose for retraction. The celiac lymphadenectomy is performed by exposing the left gastric and dissecting it to the celiac. The common hepatic and splenic arteries are also dissected. The left gastric vessels are transected with a robotic vascular stapler. A gastric conduit is fashioned with several green loads of the robotic stapler (current technique, previously an Echelon green load was used to fashion the gastric conduit). The conduit is then sutured to the gastric remnant. Botox is then injected in an anterior and posterior location in the pylorus. A 14fr jejunostomy tube (Kimberly-Clark) was placed in 125 (85%) of patients and brought out through the assistant port. A purse-string 000 silk is placed 15 cm distal to ligament of Treitz. The assistant port is removed and the Kimberly Clark percutaneous introducer is placed over a wire. The 14fr feeding tube is placed and the peel away catheter is removed. In 17 (11.6%) patients, the robot was de-docked and the tube is place via laparoscopic assistance with the T fasteners. Fig. 1 View largeDownload slide Port placed in the left paramedian location. Fig. 1 View largeDownload slide Port placed in the left paramedian location. Thoracic phase The thoracic phase is started with an 8-mm incision in the 7th intercostal space. Staging thoracoscopy confirms no evidence of metastatic deposits. Then, the robotic ports are placed including an 8-mm port in the posterior 10th interspace and an additional 8-mm port in the 3rd interspace. The extraction incision (5 cm) is made in the 9th interspace (Fig. 2). The robot is then docked. The pleura along the azygos vein is incised. The azygos vein is taken with the vascular stapler. The pleura is opened down to the previously placed Penrose, and this is used for retraction. The esophagus is mobilized to above the level of the azygos vein. It is then transected with a stapler. A lower mediastinal lymphadenectomy was performed to include level 7, 8, and 9 lymph nodes. The specimen is extracted through the extraction incision and brought up to the field. Once margins are negative on frozen section, the 25 mm anvil is then brought out through an esophagotomy. ICY-Green (12.5 mg) (performed on last 30 cases) is injected intravenously to evaluate the gastric conduit. Once a suitable vascularized area is chosen, a gastrotomy is then made. The circular stapler is introduced and passed into the chest for an intracorporeal anastomosis. The opening used to introduce the stapler is transected with an EndoGIA. An omental pedicle flap is then wrapped securely around the anastomosis. A single chest tube is placed in the posterior location and brought out through the 10th interspace port site. A nasogastric tube is placed routinely. Fig. 2 View largeDownload slide Thoracic port sites. Fig. 2 View largeDownload slide Thoracic port sites. Postoperative care Patients were placed on an accelerated care pathway designated for esophagectomy patients. Patients are started on tube feeds on postoperative day (POD) 2 and continued until they are tolerating oral intake (POD 4–5). All patients undergo upper gastrointestinal series with gastrograffin followed by barium on POD number 4. If no leak is identified, the patient's NGT’s are discontinued and they are placed on liquids with volume restriction. They are slowly advanced until they are tolerating a soft diet (POD 6–7) when they are discharged. The chest tube is usually removed on POD 5. Patients are not routinely discharged home on tube feeds. If patients are diagnosed with delayed gastric emptying (DGE), they are placed on a DGE protocol. This includes promotility agents, volume restriction, and home tube feeds. RESULTS Patient and tumor characteristics We identified 147 patients. Of these, 116 were men (78.9%) and 31 were female (21.1%). The average patient age was 66 ± 10 years. There were n = 139 (94.6%) Caucasian, 6 (4.1%) Black, 1 (0.68%) Indian, and 1 (0.68%) Hispanic patients. The mean ASA classification was 2.6 ± 0.4 and the mean body mass index (BMI) was 27.8 ± 5.1 kg/m². Adenocarcinoma was the predominant histology and was diagnosed in 126 (85.7%) patients. Fourteen (9.5%) patients had squamous cell carcinoma, 3 (2%) neuroendocrine, 2 (1.4%) high-grade dysplasia, 1 (0.68%) adeno-signet, and 1 (0.68%) with granular cell. There were 39 (26.5%) stage 1, 40 (27.2%) stage 2, 56 (38.1%) stage 3, and 2 (1.4%) high-grade dysplasia tumors. Ten patients (6.8%) had unknown preoperative stage due to institution of neoadjuvant therapy prior to surgical referral (Table 1). Table 1 Patient demographics (N = 147) Variable N (%) Age, year, mean ± SD 66.4 ± 10.1 Gender  Male 116 (78.9)  Female 31 (21.1) Race  White 139 (94.6)  Black 6 (4.1)  Indian 1 (0.68)  Hispanic 1 (0.68) BMI, kg/m², mean ± SD 27.8 ± 5.1 ASA, mean ± SD 2.6 ± 0.5 Pre-operative Stage  1 39 (26.5)  2 40 (27.2)  3 56 (38.1)  HGD 2 (1.4)  Unknown 10 (6.8) Histology  Adeno 126 (85.7)  Squamous 14 (9.5)  Neuroendocrine 3 (2)  HGD 2 (1.4)  Adeno-signet 1 (0.68)  Granular cell 1 (0.68) R0 147 (100) Lymph nodes, mean ± SD 20.4 ± 8.9 Neoadjuvant therapy  Yes 114 (77.6)  No 33 (22.4) Response to NT  Complete 54 (47.4)  Partial 39 (34.2)  None 21 (18.4) Variable N (%) Age, year, mean ± SD 66.4 ± 10.1 Gender  Male 116 (78.9)  Female 31 (21.1) Race  White 139 (94.6)  Black 6 (4.1)  Indian 1 (0.68)  Hispanic 1 (0.68) BMI, kg/m², mean ± SD 27.8 ± 5.1 ASA, mean ± SD 2.6 ± 0.5 Pre-operative Stage  1 39 (26.5)  2 40 (27.2)  3 56 (38.1)  HGD 2 (1.4)  Unknown 10 (6.8) Histology  Adeno 126 (85.7)  Squamous 14 (9.5)  Neuroendocrine 3 (2)  HGD 2 (1.4)  Adeno-signet 1 (0.68)  Granular cell 1 (0.68) R0 147 (100) Lymph nodes, mean ± SD 20.4 ± 8.9 Neoadjuvant therapy  Yes 114 (77.6)  No 33 (22.4) Response to NT  Complete 54 (47.4)  Partial 39 (34.2)  None 21 (18.4) ASA, American Society of Anesthesiologists classification; BMI, body mass index; HGD, high-grade dysplasia; NT, neoadjuvant treatment. View Large Table 1 Patient demographics (N = 147) Variable N (%) Age, year, mean ± SD 66.4 ± 10.1 Gender  Male 116 (78.9)  Female 31 (21.1) Race  White 139 (94.6)  Black 6 (4.1)  Indian 1 (0.68)  Hispanic 1 (0.68) BMI, kg/m², mean ± SD 27.8 ± 5.1 ASA, mean ± SD 2.6 ± 0.5 Pre-operative Stage  1 39 (26.5)  2 40 (27.2)  3 56 (38.1)  HGD 2 (1.4)  Unknown 10 (6.8) Histology  Adeno 126 (85.7)  Squamous 14 (9.5)  Neuroendocrine 3 (2)  HGD 2 (1.4)  Adeno-signet 1 (0.68)  Granular cell 1 (0.68) R0 147 (100) Lymph nodes, mean ± SD 20.4 ± 8.9 Neoadjuvant therapy  Yes 114 (77.6)  No 33 (22.4) Response to NT  Complete 54 (47.4)  Partial 39 (34.2)  None 21 (18.4) Variable N (%) Age, year, mean ± SD 66.4 ± 10.1 Gender  Male 116 (78.9)  Female 31 (21.1) Race  White 139 (94.6)  Black 6 (4.1)  Indian 1 (0.68)  Hispanic 1 (0.68) BMI, kg/m², mean ± SD 27.8 ± 5.1 ASA, mean ± SD 2.6 ± 0.5 Pre-operative Stage  1 39 (26.5)  2 40 (27.2)  3 56 (38.1)  HGD 2 (1.4)  Unknown 10 (6.8) Histology  Adeno 126 (85.7)  Squamous 14 (9.5)  Neuroendocrine 3 (2)  HGD 2 (1.4)  Adeno-signet 1 (0.68)  Granular cell 1 (0.68) R0 147 (100) Lymph nodes, mean ± SD 20.4 ± 8.9 Neoadjuvant therapy  Yes 114 (77.6)  No 33 (22.4) Response to NT  Complete 54 (47.4)  Partial 39 (34.2)  None 21 (18.4) ASA, American Society of Anesthesiologists classification; BMI, body mass index; HGD, high-grade dysplasia; NT, neoadjuvant treatment. View Large Metrics of feasibility: operative outcomes Operative times, conversion rates, and reoperations are listed in Table 2. Operative time was calculated from skin incision to skin closure. The longest case was the first case at 694 minutes. The mean OR time was 415 ± 84.6 minutes with a median EBL of 150 (25–600) mL. Mean OR time decreased from 471 minutes to 389 minutes after first 20 cases (P = 0.04). Further decrease in OR time to mean of 346 minutes was observed after 120 cases (P < 0.001) (Fig. 3). One (0.68%) patient was converted to an open laparotomy and there were no conversions to open in the thoracic phase. Intraoperative complications occurred in 2 (1.4%) patients. These included a bronchial injury (managed robotically), and short gastric artery bleeding (converted to open laparotomy, thoracic phase completed robotically). One (0.68%) patient required re-operation for anastomotic leak. Fig. 3 View largeDownload slide Time relationship with case numbers and operative time. Fig. 3 View largeDownload slide Time relationship with case numbers and operative time. Table 2 Operative information Variable N = 147 OR time, min, mean ± SD 415.4 ± 84.6 EBL, mL, mean ± SD 158.3 ± 107.3 Length of ICU stay, day, mean ± SD 2.00 ± 4.5 LOH, day, median (range) 9 (4–38) Conversion, n (%) 1 (0.68) Re-operation, n (%) 1 (0.68) Variable N = 147 OR time, min, mean ± SD 415.4 ± 84.6 EBL, mL, mean ± SD 158.3 ± 107.3 Length of ICU stay, day, mean ± SD 2.00 ± 4.5 LOH, day, median (range) 9 (4–38) Conversion, n (%) 1 (0.68) Re-operation, n (%) 1 (0.68) EBL, estimated blood loss; ICU, intensive care unit; LOH, length of hospitalization; OR, operating room. View Large Table 2 Operative information Variable N = 147 OR time, min, mean ± SD 415.4 ± 84.6 EBL, mL, mean ± SD 158.3 ± 107.3 Length of ICU stay, day, mean ± SD 2.00 ± 4.5 LOH, day, median (range) 9 (4–38) Conversion, n (%) 1 (0.68) Re-operation, n (%) 1 (0.68) Variable N = 147 OR time, min, mean ± SD 415.4 ± 84.6 EBL, mL, mean ± SD 158.3 ± 107.3 Length of ICU stay, day, mean ± SD 2.00 ± 4.5 LOH, day, median (range) 9 (4–38) Conversion, n (%) 1 (0.68) Re-operation, n (%) 1 (0.68) EBL, estimated blood loss; ICU, intensive care unit; LOH, length of hospitalization; OR, operating room. View Large All patients underwent a complete resection (R0). The median tumor length was 3.0 (0.1–15.1) cm. Mean number of retrieved lymph nodes was 20.4 ± 8.9. Neoadjuvant therapy was administered to 114 (77.6%) patients. Of those, 54 patients had complete response (47.4%), 39 patients had partial response (34.2%) and 21 patients had no response (18.4%) (Table 1). Metrics of safety: postoperative complications Postoperative complications occurred in 37 patients (25.2%) (Table 3). There were 4 (2.7%) anastomotic leaks and 1 (0.68%) gastric staple line leak. All leaks were managed nonoperatively with endoscopic stenting, however 1 anastomotic leak failed endoscopic management and was managed with a re-operation. Other complications were as follows: chyle leak (n = 5, 3.4%), cardiac arrhythmias (n = 17, 11.6%), pneumonia (n = 10, 6.8%), respiratory failure requiring tracheostomy (n = 2, 1.4% (due to aspiration)), deep venous thrombus n = 2 (1.4%), and pulmonary embolus (n = 1, 0.68%). Complications occurred n = 24 (21%) of the patients who received neoadjuvant treatment whereas n = 13 (40%) of patients who did not have neoadjuvant treatment had complications (P = 0.04). Complications became less frequent as more cases were performed. There were 9 (31%) complications in the first 29 cases, and 28 (23.7%) in the subsequent cases (P = 0.01) (Fig. 4). The mean ICU stay was 2.00 ± 4.5 days and the median length of hospital stay (LOH) for all patients was 9 (4–38) days (Table 2). The median LOH for patients who did not experience a complication was 8 (4–17) days and 14.5 (7–38) days for those who experienced a complication (P < 0.001). Neither patient who suffered an intraoperative complication experienced a postoperative complication and both were discharged at 9 and 11 days, respectively. Mortalities were low for the entire cohort. There was 1 (0.6%) 30-day mortality and 2 (1.4%) 90-day mortalities. Fig. 4 View largeDownload slide Complications decreased with increasing surgeries performed. Fig. 4 View largeDownload slide Complications decreased with increasing surgeries performed. Table 3 Complications Complication N (%) Patients 37 (25.2) Wound infection 1 (0.68) Cardiac arrhythmias 17 (11.6) Anastomotic leak 4 (2.7) Gastric staple line leak 1 (0.68) Chyle leak 5 (3.4) Pneumonia 10 (6.8) Pulmonary embolism/DVT 3 (2.0)  DVT 2 (1.4)  PE 1 (0.68)  Respiratory failure requiring tracheostomy 2 (1.4) Pneumothorax 2 (1.4) Mortality  30-day 1(0.68)  90-day 2(1.4) Complication N (%) Patients 37 (25.2) Wound infection 1 (0.68) Cardiac arrhythmias 17 (11.6) Anastomotic leak 4 (2.7) Gastric staple line leak 1 (0.68) Chyle leak 5 (3.4) Pneumonia 10 (6.8) Pulmonary embolism/DVT 3 (2.0)  DVT 2 (1.4)  PE 1 (0.68)  Respiratory failure requiring tracheostomy 2 (1.4) Pneumothorax 2 (1.4) Mortality  30-day 1(0.68)  90-day 2(1.4) DVT, deep venous thromboembolism; PE, pulmonary embolism. View Large Table 3 Complications Complication N (%) Patients 37 (25.2) Wound infection 1 (0.68) Cardiac arrhythmias 17 (11.6) Anastomotic leak 4 (2.7) Gastric staple line leak 1 (0.68) Chyle leak 5 (3.4) Pneumonia 10 (6.8) Pulmonary embolism/DVT 3 (2.0)  DVT 2 (1.4)  PE 1 (0.68)  Respiratory failure requiring tracheostomy 2 (1.4) Pneumothorax 2 (1.4) Mortality  30-day 1(0.68)  90-day 2(1.4) Complication N (%) Patients 37 (25.2) Wound infection 1 (0.68) Cardiac arrhythmias 17 (11.6) Anastomotic leak 4 (2.7) Gastric staple line leak 1 (0.68) Chyle leak 5 (3.4) Pneumonia 10 (6.8) Pulmonary embolism/DVT 3 (2.0)  DVT 2 (1.4)  PE 1 (0.68)  Respiratory failure requiring tracheostomy 2 (1.4) Pneumothorax 2 (1.4) Mortality  30-day 1(0.68)  90-day 2(1.4) DVT, deep venous thromboembolism; PE, pulmonary embolism. View Large Readmission rate at 90 days was 5.4% (n = 8). Reasons for readmission included: Pulmonary embolus or DVT (n = 3), pneumonia (n = 2), dysphagia (n = 1), anxiety attack (n = 1), nausea/vomiting (n = 1). Readmissions were higher in the patients who experienced a postoperative adverse event. There were 3 (8.1%) readmissions in patients who experienced a postoperative complication, and 5 (4.5%) in those patients who did not experience an adverse event postoperatively, P = 0.4. DISCUSSION We report our series of 147 robotic-assisted Ivor–Lewis esophagectomies. The length of operation is a significant concern in patients undergoing robotic procedures. However, we have demonstrated that the length of operation decreases steadily as more cases are performed. The mean operative time was decreased to 346 minutes after 120 cases. This time is comparable to our series with thoracoscopic and laparoscopic approaches at 320 minutes.1 The EBL was low at 150 mL and the mean ICU stay was only 2 days. The LOH was 9 days and 14.5 days if patients experienced a complication. Oncologic outcomes as measured by R0 resection rates and lymph node harvest were also comparable if not better than other approaches to esophagectomy. All of our patients underwent R0 resections and the mean LN harvest was 20.4 despite 77.5% of patients undergoing neoadjuvant therapy. Complications occurred in only 37 patients (25.2%) and occurred less frequently in those patients treated with neoadjuvant therapy (21% vs. 40%, P = 0.042). Additionally, complications occurred less frequently later in our series after the learning curve was surpassed 31% versus 23.7% (P = 0.01). Readmission rates were low at 5.4% and did increase to 8.1% if a patient experienced a postoperative complication. Surgical resection is an integral part of the treatment algorithm for early stage and locally advanced esophageal cancer. The morbidity associated with esophagectomy can be as high as 60% even in tertiary centers.13,14 Pulmonary and cardiovascular complications such as atelectasis, pneumonia, atrial fibrillation, wound infection, anastomotic leak, and chylothorax are among the most commonly seen postoperative complications and may increase the risk of mortality.14 Patients who were treated with neoadjuvant therapy had a lower complication rate including anastomotic leak (AL). Several authors have reported similar findings associated with neoadjuvant therapy. Tapias et al. demonstrated that in patients who received NCR, there was a low incidence of AL in open Ivor–Lewis esophagectomy and RAIL (1.4% and 0%, respectively).15 Our results mimic the Tapias study where we report 0.9% AL in NCR who underwent RAIL. We hypothesize that NCR may increase the vascularity of tissues and increase serum vascular endothelial growth factor (VEGF) levels. This was demonstrated in a pathologic analysis of 92 esophagectomy specimens where mean tumor vessel density and VEGF staining were higher in NCR patients resulting in increased serum VEGF levels.16 The increase in VEGF levels might potentially result from vascularized stromal fibroblast, and the resultant increase in granulation may increase healing and result in decreased AL.17 The most common complication in our series was cardiovascular-related complications, including 1 acute myocardial infarction leading to death. Other cardiovascular complications were nonlethal and were mostly arrhythmias. The second most common complication in our series was pneumonia although low at 6.8%. Cardiopulmonary complications occur less commonly in minimal invasive esophagectomy compared to open techniques.7-9 We have demonstrated a similar trend with the robotic approach. However, there are no data currently as to whether pulmonary complications differ between robotic techniques versus other minimal invasive approaches. There are numerous series comparing outcomes of minimally invasive Ivor–Lewis esophagectomy to the open approach. Cardiopulmonary complications, blood loss, ICU stay as well as hospital stay are shown to be reduced in minimal invasive techniques.11,18,19 In addition, 30 day mortality and leak rates are low at 0–6.6%20 and 0–10%, respectively, for the minimal invasive approach.20-23 In our series the mortality was 1.3% and the anastomotic leak rate was 2.7%, which is in the lower range of what has been reported for minimal invasive techniques. Lymph node retrieval is similar between the open and minimal invasive approach.20-24 Moreover, the number of lymph nodes harvested in the current report is 20 which is also within the range that has been reported for minimal invasive techniques.23,25-27 Therefore we conclude that robotic surgery, in experienced hands, is not inferior to other minimal invasive or open techniques in terms of complications, perioperative and oncologic outcomes. Multiple authors have reported their results with robotic-assisted esophagectomy.28-30 Robotic assisted or completely robotic esophagectomies are performed via transhiatal, McKeown, or Ivor–Lewis approaches. They report leak rates varying between 10 and 33%28,29,31-33 which is high compared to other minimally invasive techniques. Operative times also vary greatly (180–556 min) although techniques are not uniform. The number of resected lymph nodes varied between 14 and 36 and blood loss was as high as 1600 mL in some series.32 Our experience with robotic esophagectomy demonstrates lower anastomotic leaks, complications, EBL, and operative times emphasizing that our operative outcomes, morbidity, and mortality rates are low compared to what has been reported in the literature for the robotic Ivor–Lewis approach.28,29,31,33,34 The robotic approach does require technical expertise by the operating surgeon and an OR team familiar with the intricacies of using the robot such as set-up, docking, and instrument exchange. Efficacy and feasibility of robotic surgery for complex esophageal surgery has been evaluated and found to offer enhanced three-dimensional visualization and advanced articulation with wrist-like motion. The potential obstacle to adoption of this technique is the long learning curve required to achieve proficiency. In our experience, there was a significant reduction in operative time after completing 20 cases (514 minutes vs. 397 minutes, P < 0.005). In this study, we have demonstrated that OR time decreased further to 346 minutes after 120 cases. During our initial evaluation of outcomes after our first fifty-two cases, we reported one case of anastomotic leak and no deaths. After 29 cases, the complications decreased from 31% to 23.8% with an overall complication rate at 26.9%. Additionally, there were no conversions to open thoracotomy and all patients in the series received an R0 resection.12 The range of operative time in minimal invasive techniques is reported to be between 249 and 535 minutes.23,25-27,35 Sarkaria and Rizk reported a similar learning curve. Their initial average operative time for the first 15 patients was 600 minutes, which came down to average of 370 minutes for the last 5 patients in their cohort.29 Unfortunately, there are no randomized data comparing the robotic trans-thoracic approach to conventional minimally invasive techniques. van der Sluis et al have proposed the first randomized trial comparing the open approach to robotic assisted minimally invasive thoracolaparoscopic esophagectomy for resectable esophageal cancer (ROBOT trial).36 We would expect similar results to Bierre's randomized trial comparing thoracoscopic esophageal resection to the conventional open approach.11 The ROBOT trial will perhaps provide additional data over benefits compared to open approaches however it will not aid us in determining an optimal minimally invasive approach. We acknowledge the potential limitations of this study due to the retrospective nature of this review. There is significant potential for selection bias in retrospective studies. Additionally, the causal and temporal relationship among variables can be difficult to assess. This cohort includes all consecutive patients undergoing RAIL at a single institution. All procedures were performed by a single surgeon thereby minimizing variation in operative technique or learning curve as a factor in analyzing outcome data. Thus, these factors serve to minimize potential biases. CONCLUSION To our knowledge, this represents the largest series of robotic Ivor–Lewis esophagectomies performed to date. We have demonstrated that RAIL is a safe surgical technique, which has comparable early outcomes to traditional minimal invasive esophagectomy approaches. This is evidenced by operative times, length of time in an ICU, overall hospitalization, and risk of complications or death. The learning curve is long and requires specialized training. This need for advanced training, long learning curves, and cost remain substantial barriers to the implementation of a robotic esophageal program. However robotic surgery is an advancing technology that provides surgeons with improved visualization and more ergonomic instruments thus enhancing the versatility over conventional approaches. Randomized trials are necessary and are in process to enable us to make more precise conclusions about the superiority of one surgical technique over the other. Disclosures Drs. K. Meredith, O. Andacoglu, R. Shridhar, and Ms. Huston have no conflicts of interest or financial ties to disclose. Notes Specific author contributions: Kenneth Meredith participated in the study design, analysis and interpretation of data, and drafting and critical revision of the manuscript. Jamie Huston participated in the study design and data collection. Oya Andacoglu participated in data collection, and drafting and critical revision of the manuscript. Ravi Shridhar participated in the study design, analysis and interpretation of data, and critical revision of the manuscript. All authors read and approved the final manuscript. Source of Funding: None. References 1 Yamamoto S , Kawahara K , Maekawa T et al. Minimally invasive esophagectomy for stage I and II esophageal cancer . Trials 2005 ; 80 : 1421 – 6 . 2 Jemal A , Siegel R , Ward E et al. Cancer statistics, 2008 . CA Cancer J Clin 2008 ; 58 : 71 – 96 . Google Scholar CrossRef Search ADS PubMed 3 McLoughlin J M , Melis M , Siegel E M et al. Are patients with esophageal cancer who become PET negative after neoadjuvant chemoradiation free of cancer ? J Am Coll Surg 2008 ; 206 : 879 – 86 ; discussion 86–7 . Google Scholar CrossRef Search ADS PubMed 4 NCCN Clinical Practice Guidelines in Oncology: Esophageal and Esophagogastric Junction Cancers . 2013 , https://www.nccn.org/. Accessed October 23, 2016 . 5 Luketich J , Pennathur A , Awais O et al. Outcomes after minimally invasive esophagectomy: review of over 1000 patients . Ann Surg 2012 ; 256 : 95 – 103 . Google Scholar CrossRef Search ADS PubMed 6 Santillan A A , Farma J M , Meredith K L et al. Minimally invasive surgery for esophageal cancer . J Natl Compr Canc Netw 2008 ; 6 : 879 – 84 . Google Scholar CrossRef Search ADS PubMed 7 Verhage R , Hazebroek E , Boone J et al. Minimally invasive surgery for esophageal cancer . Minerva Chir 2009 ; 64 : 135 – 46 . Google Scholar PubMed 8 Safranek P , Cubitt J , Booth M et al. Review of open and minimal access approaches to oesophagectomy for cancer . Br J Surg 2010 ; 97 : 1845 – 53 . Google Scholar CrossRef Search ADS PubMed 9 Singh R , Pham T , Diggs B et al. Minimally invasive esophagectomy provides equivalent oncologic outcomes to open esophagectomy for locally advanced (stage II or III) esophageal carcinoma . Arch Surg 2011 ; 146 : 711 – 4 . Google Scholar CrossRef Search ADS PubMed 10 Straatman J , van der Wielen N , Cuesta M et al. Minimally invasive versus open esophageal resection: three-year follow-up of the previously reported randomized controlled trial: the TIME trial . Ann Surg 2017 ; 266 : 232 – 36 . Google Scholar CrossRef Search ADS PubMed 11 Biere S , Van Berge Henegouwen M , Maas K et al. Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial . Lancet 2012 ; 379 : 1887 – 92 . Google Scholar CrossRef Search ADS PubMed 12 Hernandez J , Dimou F , Weber J et al. Defining the learning curve for robotic-assisted esophagogastrectomy . J Gastrointest Surg 2013 ; 17 : 1346 – 51 . Google Scholar CrossRef Search ADS PubMed 13 Karl R , Schreiber R , Boulware D et al. Factors affecting morbidity, mortality, and survival in patients undergoing Ivor–Lewis esophagogastrectomy . Ann Surg 2000 ; 231 : 635 – 43 . Google Scholar CrossRef Search ADS PubMed 14 Atkins B , Shah A , Hutcheson K et al. Reducing hospital morbidity and mortality following esophagectomy . Ann Thorac Surg 2004 ; 78 : 1170 – 76 . Google Scholar CrossRef Search ADS PubMed 15 Tapias L F , Mathisen D J , Wright C D et al. Outcomes with open and minimally invasive Ivor–Lewis esophagectomy after neoadjuvant therapy . Ann Thorac Surg 2016 ; 101 : 1097 – 103 . Google Scholar CrossRef Search ADS PubMed 16 McDonnell C O , Bouchier-Hayes D J , Toomey D et al. Effect of neoadjuvant chemoradiotherapy on angiogenesis in oesophageal cancer . Br J Surg 2003 ; 90 : 1373 – 8 . Google Scholar CrossRef Search ADS PubMed 17 Dvorak H F . Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing . N Engl J Med 1986 ; 315 : 1650 – 9 . Google Scholar CrossRef Search ADS PubMed 18 Pham T H , Perry K A , Dolan J P et al. Comparison of perioperative outcomes after combined thoracoscopic-laparoscopic esophagectomy and open Ivor–Lewis esophagectomy . Am J Surg 2010 ; 199 : 594 – 8 . Google Scholar CrossRef Search ADS PubMed 19 Sihag S , Wright C , Wain J et al. Comparison of perioperative outcomes following open versus minimally invasive Ivor–Lewis oesophagectomy at a single, high-volume centre . Eur J Cardiothorac Surg 2012 ; 42 : 430 – 7 . Google Scholar CrossRef Search ADS PubMed 20 Luketich J D , Alvelo-Rivera M , Buenaventura P O et al. Minimally invasive esophagectomy: outcomes in 222 patients . Ann Surg 2003 ; 238 : 486 – 94 ; discussion 94–5 . Google Scholar PubMed 21 Bizekis C , Kent M S , Luketich J D et al. Initial experience with minimally invasive Ivor–Lewis esophagectomy . Ann Thorac Surg 2006 ; 82 : 402 – 6 ; discussion 06–7 . Google Scholar CrossRef Search ADS PubMed 22 Tapias L , Morse C . A preliminary experience with minimally invasive Ivor–Lewis esophagectomy . Dis Esophagus 2012 ; 25 : 449 – 55 . Google Scholar CrossRef Search ADS PubMed 23 Thomay A , Snyder J , Edmondson D et al. Initial results of minimally invasive Ivor–Lewis esophagectomy after induction chemoradiation (50.4 gy) for esophageal cancer . Innovations (Phila) 2012 ; 7 : 421 – 8 . Google Scholar PubMed 24 Nguyen N , Hinojosa M , Smith B et al. Minimally invasive esophagectomy: lessons learned from 104 operations . Ann Surg 2008 ; 248 : 1081 – 91 . Google Scholar CrossRef Search ADS PubMed 25 Merritt R . Initial experience of total thoracoscopic and laparoscopic Ivor–Lewis esophagectomy . J Laparoendosc Adv Surg Tech A 2012 ; 22 : 214 – 9 . Google Scholar CrossRef Search ADS PubMed 26 Nguyen N , Roberts P , Follette D et al. Thoracoscopic and laparoscopic esophagectomy for benign and malignant disease: lessons learned from 46 consecutive procedures . J Am Coll Surg 2003 ; 197 : 902 – 13 . Google Scholar CrossRef Search ADS PubMed 27 Cadiere G , Dapri G , Himpens J et al. Ivor– Lewis esophagectomy with manual esogastric anastomosis by thoracoscopy in prone position and laparoscopy . Surg Endosc 2010 ; 24 : 1482 – 5 . Google Scholar CrossRef Search ADS PubMed 28 Clark J , Sodergren M H , Purkayastha S et al. The role of robotic assisted laparoscopy for oesophagogastric oncological resection; an appraisal of the literature . Dis Esophagus 2011 ; 24 : 240 – 50 . Google Scholar CrossRef Search ADS PubMed 29 Sarkaria I , Rizk N . Robotic-assisted minimally invasive esophagectomy: the Ivor–Lewis approach . Thorac Surg Clin 2014 ; 24 : 211 – 22 . Google Scholar CrossRef Search ADS PubMed 30 Park S , Kim D , Do Y et al. The oncologic outcome of esophageal squamous cell carcinoma patients after robot-assisted thoracoscopic esophagectomy with total mediastinal lymphadenectomy . Ann Thorac Surg 2017 ; 103 : 1151 – 57 . Google Scholar CrossRef Search ADS PubMed 31 Anderson C , Hellan M , Kernstine K et al. Robotic surgery for gastrointestinal malignancies . Int J Med Robot 2007 ; 3 : 297 – 300 . Google Scholar CrossRef Search ADS PubMed 32 Galvani C , Horgan S . [Robots in general surgery: present and future] . Cirugia espanola 2005 ; 78 : 138 – 47 . Google Scholar CrossRef Search ADS PubMed 33 Puntambekar S , Rayate N , Joshi S et al. Robotic transthoracic esophagectomy in the prone position: experience with 32 patients with esophageal cancer . J Thorac Cardiovasc Surg 2011 ; 142 : 1283 – 4 . Google Scholar CrossRef Search ADS PubMed 34 Galvani C , Gorodner M , Moser F et al. Robotically assisted laparoscopic transhiatal esophagectomy . Surg Endosc 2008 ; 22 : 188 – 95 . Google Scholar CrossRef Search ADS PubMed 35 Campos G , Jablons D , Brown L et al. A safe and reproducible anastomotic technique for minimally invasive Ivor–Lewis oesophagectomy: the circular-stapled anastomosis with the trans-oral anvil . Eur J Cardiothorac Surg 2010 ; 37 : 1421 – 6 . Google Scholar CrossRef Search ADS PubMed 36 van der Sluis P , Ruurda J , van der Horst S et al. Robot-assisted minimally invasive thoracolaparoscopic esophagectomy versus open transthoracic esophagectomy for resectable esophageal cancer, a randomized controlled trial (ROBOT trial) . Trials 2012 ; 13 : 230 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of International Society for Diseases of the Esophagus. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Diseases of the Esophagus Oxford University Press

Safety and feasibility of robotic-assisted Ivor–Lewis esophagectomy

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The International Society for Diseases of the Esophagus
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© The Author(s) 2018. Published by Oxford University Press on behalf of International Society for Diseases of the Esophagus.
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1120-8694
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1442-2050
D.O.I.
10.1093/dote/doy005
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Abstract

SUMMARY Esophagectomy is associated with substantial morbidity. Robotic surgery allows complex resections to be performed with potential benefits over conventional techniques. We applied this technology to transthoracic esophagectomy to assess safety, feasibility, and reliability of this technology. A retrospective cohort study of all patients undergoing robotic-assisted Ivor–Lewis esophagectomy (RAIL) from 2009 to 2014 was conducted. Clinicopathologic factors and surgical outcomes were recorded and compared. All statistical tests were two-sided and a P-value of <0.05 was considered statistically significant. We identified 147 patients with an average age 66 ± 10 years. Neoadjuvant therapy was administered to 114 (77.6%) patients, and all patients underwent a R0 resection. The mean operating room (OR) time was 415 ± 84.6 minutes with a median estimated blood loss (EBL) of 150 (25–600) mL. Mean intensive care unit (ICU) stay was 2.00 ± 4.5 days, median length of hospitalization (LOH) was 9 (4–38) days, and readmissions within 90 days were low at 8 (5.5%). OR time decreased from 471 minutes to 389 minutes after 20 cases and a further decrease to mean of 346 minutes was observed after 120 cases. Complications occurred in 37 patients (25.2%). There were 4 anastomotic (2.7%) leaks. Thirty and 90-day mortality was 0.68% and 1.4%, respectively. This represents to our knowledge the largest series of robotic esophagectomies. RAIL is a safe surgical technique that provides an alternative to standard minimally invasive and open techniques. In our series, there was no increased risk of LOH, complications, or death and re-admission rates were low despite earlier discharge. INTRODUCTION Esophageal cancer continues to increase in incidence worldwide.1-3 In 2015, there were 16,980 new cases of esophageal cancer and 15,590 deaths from disease in the United States.2 The average age at the time of diagnosis also continues to rise with a peak incidence between 75 and 79 years of age. The long-term survival for patients with locally advanced esophageal cancer remains poor despite improvements in multimodality care over the last several decades. The current approach to locally advanced esophageal cancer includes neoadjuvant chemoradiation (NCR) followed by surgical resection.4 Minimally invasive esophagectomy (MIE) offers several potential advantages over traditional open esophagectomy. The MIE has been found to result in faster recovery time, substantial decrease in blood loss, decrease in postoperative complications and shorter hospitalization, with comparable oncologic outcome.5 Retrospective reviews have demonstrated that MIE does not compromise oncologic principles and is safe compared to traditional open esophagectomy for esophageal cancer.6-10 Moreover, the transthoracic or Ivor–Lewis approach when performed via a minimally invasive approach has the potential to significantly reduce pulmonary complications, a substantial morbidity associated with the open approach. Biere et al. demonstrated in their prospective trial in which patients were randomized to either open esophagectomy or MIE that patients undergoing MIE were less likely to have pulmonary complications and had shorter hospital stays compared to patients undergoing open esophagectomy.11 Robotic-assisted Ivor–Lewis esophagectomy (RAIL) is an emerging technique that allows the surgeon a broader and three-dimensional view of the operative field with the added benefit of improved instrument articulation over standard thoracoscopy. We have previously described the development and implementation of a robotic approach to esophagectomy.12 In this study, we sought to report our large series and examine the safety and feasibility of a robotic-assisted approach in patients undergoing an Ivor–Lewis esophagectomy. METHODS A retrospective cohort study of a prospective robotic esophageal database of 147 consecutive patients undergoing RAIL from 2009 to 2014 was conducted after obtaining study approval from our Institutional Review Board (IRB#15-onc-23). All patients, regardless of age, race, tumor stage, or location, or neoadjuvant therapy were included in the cohort. Patients were required to have a tissue diagnosis of high-grade dysplasia or cancer, but were not excluded based upon histologic variant. Basic demographics, tumor characteristics, operative details, and postoperative outcomes were recorded. Patients were included only if they underwent RAIL. Patients with mid-esophageal tumors who underwent Mckeown or transhiatal esophagectomy were excluded for this analysis. Endpoints and statistical analysis The primary endpoints/feasibility metrics were operating room (OR) time, estimated blood loss (EBL), intensive care unit (ICU) days following surgery, and length of hospitalization (LOH). Secondary end-points and safety metrics included perioperative adverse events (AE) (<90 days following surgery), including pneumonia, cardiac arrhythmia, deep vein thrombosis (DVT)/pulmonary embolism (PE), wound infection, anastomotic leak (AL), as well as 30 and 90-day mortality. Pneumonia was defined as infiltrates on chest radiograph and positive sputum culture. Anastomotic leaks were confirmed by an upper GI study or CT scan. Readmissions and outcomes with and without neoadjuvant therapy were also analyzed. Statistical analysis was performed using the SPSS® version 21.0 (IBM®, Chicago, IL). Continuous variables were compared using the Kruskal–Wallis or the ANOVA tests as appropriate. Pearson's Chi-square test was used to compare categorical variables. All statistical tests were two-sided and a P-value of <0.05 was considered statistically significant. Surgical technique Abdominal phase A single surgeon performed all operations. The surgeon has extensive experience with both open, laparoscopic and thoracoscopic approaches to esophageal resection. The abdomen is entered with a Veress needle supraumbilically. The camera is inserted into a 5-mm port and the abdomen is entered via an optiview technique. Once staging laparoscopy has demonstrated no evidence of metastatic disease, additional 8-mm ports are placed in the right lateral and left lateral positions. A robotic stapling port is placed in the right paramedian location. An assistant port (also to be used for jejunostomy) is placed in the left paramedian location (Fig. 1). A subxyphoid incision is made for the Nathanson liver retractor. The camera port is upsized to an 8 mm (DaVinci XI), or 10 mm (DaVinci SI). The robot is then docked. The gastrocolic attachments are incised inferior to the right gastroepiploic pedicle along the greater curve of the stomach. The vessel sealer is used to take the short gastric vessels. The left and right crural dissection is performed. The esophagus is encircled with a Penrose for retraction. The celiac lymphadenectomy is performed by exposing the left gastric and dissecting it to the celiac. The common hepatic and splenic arteries are also dissected. The left gastric vessels are transected with a robotic vascular stapler. A gastric conduit is fashioned with several green loads of the robotic stapler (current technique, previously an Echelon green load was used to fashion the gastric conduit). The conduit is then sutured to the gastric remnant. Botox is then injected in an anterior and posterior location in the pylorus. A 14fr jejunostomy tube (Kimberly-Clark) was placed in 125 (85%) of patients and brought out through the assistant port. A purse-string 000 silk is placed 15 cm distal to ligament of Treitz. The assistant port is removed and the Kimberly Clark percutaneous introducer is placed over a wire. The 14fr feeding tube is placed and the peel away catheter is removed. In 17 (11.6%) patients, the robot was de-docked and the tube is place via laparoscopic assistance with the T fasteners. Fig. 1 View largeDownload slide Port placed in the left paramedian location. Fig. 1 View largeDownload slide Port placed in the left paramedian location. Thoracic phase The thoracic phase is started with an 8-mm incision in the 7th intercostal space. Staging thoracoscopy confirms no evidence of metastatic deposits. Then, the robotic ports are placed including an 8-mm port in the posterior 10th interspace and an additional 8-mm port in the 3rd interspace. The extraction incision (5 cm) is made in the 9th interspace (Fig. 2). The robot is then docked. The pleura along the azygos vein is incised. The azygos vein is taken with the vascular stapler. The pleura is opened down to the previously placed Penrose, and this is used for retraction. The esophagus is mobilized to above the level of the azygos vein. It is then transected with a stapler. A lower mediastinal lymphadenectomy was performed to include level 7, 8, and 9 lymph nodes. The specimen is extracted through the extraction incision and brought up to the field. Once margins are negative on frozen section, the 25 mm anvil is then brought out through an esophagotomy. ICY-Green (12.5 mg) (performed on last 30 cases) is injected intravenously to evaluate the gastric conduit. Once a suitable vascularized area is chosen, a gastrotomy is then made. The circular stapler is introduced and passed into the chest for an intracorporeal anastomosis. The opening used to introduce the stapler is transected with an EndoGIA. An omental pedicle flap is then wrapped securely around the anastomosis. A single chest tube is placed in the posterior location and brought out through the 10th interspace port site. A nasogastric tube is placed routinely. Fig. 2 View largeDownload slide Thoracic port sites. Fig. 2 View largeDownload slide Thoracic port sites. Postoperative care Patients were placed on an accelerated care pathway designated for esophagectomy patients. Patients are started on tube feeds on postoperative day (POD) 2 and continued until they are tolerating oral intake (POD 4–5). All patients undergo upper gastrointestinal series with gastrograffin followed by barium on POD number 4. If no leak is identified, the patient's NGT’s are discontinued and they are placed on liquids with volume restriction. They are slowly advanced until they are tolerating a soft diet (POD 6–7) when they are discharged. The chest tube is usually removed on POD 5. Patients are not routinely discharged home on tube feeds. If patients are diagnosed with delayed gastric emptying (DGE), they are placed on a DGE protocol. This includes promotility agents, volume restriction, and home tube feeds. RESULTS Patient and tumor characteristics We identified 147 patients. Of these, 116 were men (78.9%) and 31 were female (21.1%). The average patient age was 66 ± 10 years. There were n = 139 (94.6%) Caucasian, 6 (4.1%) Black, 1 (0.68%) Indian, and 1 (0.68%) Hispanic patients. The mean ASA classification was 2.6 ± 0.4 and the mean body mass index (BMI) was 27.8 ± 5.1 kg/m². Adenocarcinoma was the predominant histology and was diagnosed in 126 (85.7%) patients. Fourteen (9.5%) patients had squamous cell carcinoma, 3 (2%) neuroendocrine, 2 (1.4%) high-grade dysplasia, 1 (0.68%) adeno-signet, and 1 (0.68%) with granular cell. There were 39 (26.5%) stage 1, 40 (27.2%) stage 2, 56 (38.1%) stage 3, and 2 (1.4%) high-grade dysplasia tumors. Ten patients (6.8%) had unknown preoperative stage due to institution of neoadjuvant therapy prior to surgical referral (Table 1). Table 1 Patient demographics (N = 147) Variable N (%) Age, year, mean ± SD 66.4 ± 10.1 Gender  Male 116 (78.9)  Female 31 (21.1) Race  White 139 (94.6)  Black 6 (4.1)  Indian 1 (0.68)  Hispanic 1 (0.68) BMI, kg/m², mean ± SD 27.8 ± 5.1 ASA, mean ± SD 2.6 ± 0.5 Pre-operative Stage  1 39 (26.5)  2 40 (27.2)  3 56 (38.1)  HGD 2 (1.4)  Unknown 10 (6.8) Histology  Adeno 126 (85.7)  Squamous 14 (9.5)  Neuroendocrine 3 (2)  HGD 2 (1.4)  Adeno-signet 1 (0.68)  Granular cell 1 (0.68) R0 147 (100) Lymph nodes, mean ± SD 20.4 ± 8.9 Neoadjuvant therapy  Yes 114 (77.6)  No 33 (22.4) Response to NT  Complete 54 (47.4)  Partial 39 (34.2)  None 21 (18.4) Variable N (%) Age, year, mean ± SD 66.4 ± 10.1 Gender  Male 116 (78.9)  Female 31 (21.1) Race  White 139 (94.6)  Black 6 (4.1)  Indian 1 (0.68)  Hispanic 1 (0.68) BMI, kg/m², mean ± SD 27.8 ± 5.1 ASA, mean ± SD 2.6 ± 0.5 Pre-operative Stage  1 39 (26.5)  2 40 (27.2)  3 56 (38.1)  HGD 2 (1.4)  Unknown 10 (6.8) Histology  Adeno 126 (85.7)  Squamous 14 (9.5)  Neuroendocrine 3 (2)  HGD 2 (1.4)  Adeno-signet 1 (0.68)  Granular cell 1 (0.68) R0 147 (100) Lymph nodes, mean ± SD 20.4 ± 8.9 Neoadjuvant therapy  Yes 114 (77.6)  No 33 (22.4) Response to NT  Complete 54 (47.4)  Partial 39 (34.2)  None 21 (18.4) ASA, American Society of Anesthesiologists classification; BMI, body mass index; HGD, high-grade dysplasia; NT, neoadjuvant treatment. View Large Table 1 Patient demographics (N = 147) Variable N (%) Age, year, mean ± SD 66.4 ± 10.1 Gender  Male 116 (78.9)  Female 31 (21.1) Race  White 139 (94.6)  Black 6 (4.1)  Indian 1 (0.68)  Hispanic 1 (0.68) BMI, kg/m², mean ± SD 27.8 ± 5.1 ASA, mean ± SD 2.6 ± 0.5 Pre-operative Stage  1 39 (26.5)  2 40 (27.2)  3 56 (38.1)  HGD 2 (1.4)  Unknown 10 (6.8) Histology  Adeno 126 (85.7)  Squamous 14 (9.5)  Neuroendocrine 3 (2)  HGD 2 (1.4)  Adeno-signet 1 (0.68)  Granular cell 1 (0.68) R0 147 (100) Lymph nodes, mean ± SD 20.4 ± 8.9 Neoadjuvant therapy  Yes 114 (77.6)  No 33 (22.4) Response to NT  Complete 54 (47.4)  Partial 39 (34.2)  None 21 (18.4) Variable N (%) Age, year, mean ± SD 66.4 ± 10.1 Gender  Male 116 (78.9)  Female 31 (21.1) Race  White 139 (94.6)  Black 6 (4.1)  Indian 1 (0.68)  Hispanic 1 (0.68) BMI, kg/m², mean ± SD 27.8 ± 5.1 ASA, mean ± SD 2.6 ± 0.5 Pre-operative Stage  1 39 (26.5)  2 40 (27.2)  3 56 (38.1)  HGD 2 (1.4)  Unknown 10 (6.8) Histology  Adeno 126 (85.7)  Squamous 14 (9.5)  Neuroendocrine 3 (2)  HGD 2 (1.4)  Adeno-signet 1 (0.68)  Granular cell 1 (0.68) R0 147 (100) Lymph nodes, mean ± SD 20.4 ± 8.9 Neoadjuvant therapy  Yes 114 (77.6)  No 33 (22.4) Response to NT  Complete 54 (47.4)  Partial 39 (34.2)  None 21 (18.4) ASA, American Society of Anesthesiologists classification; BMI, body mass index; HGD, high-grade dysplasia; NT, neoadjuvant treatment. View Large Metrics of feasibility: operative outcomes Operative times, conversion rates, and reoperations are listed in Table 2. Operative time was calculated from skin incision to skin closure. The longest case was the first case at 694 minutes. The mean OR time was 415 ± 84.6 minutes with a median EBL of 150 (25–600) mL. Mean OR time decreased from 471 minutes to 389 minutes after first 20 cases (P = 0.04). Further decrease in OR time to mean of 346 minutes was observed after 120 cases (P < 0.001) (Fig. 3). One (0.68%) patient was converted to an open laparotomy and there were no conversions to open in the thoracic phase. Intraoperative complications occurred in 2 (1.4%) patients. These included a bronchial injury (managed robotically), and short gastric artery bleeding (converted to open laparotomy, thoracic phase completed robotically). One (0.68%) patient required re-operation for anastomotic leak. Fig. 3 View largeDownload slide Time relationship with case numbers and operative time. Fig. 3 View largeDownload slide Time relationship with case numbers and operative time. Table 2 Operative information Variable N = 147 OR time, min, mean ± SD 415.4 ± 84.6 EBL, mL, mean ± SD 158.3 ± 107.3 Length of ICU stay, day, mean ± SD 2.00 ± 4.5 LOH, day, median (range) 9 (4–38) Conversion, n (%) 1 (0.68) Re-operation, n (%) 1 (0.68) Variable N = 147 OR time, min, mean ± SD 415.4 ± 84.6 EBL, mL, mean ± SD 158.3 ± 107.3 Length of ICU stay, day, mean ± SD 2.00 ± 4.5 LOH, day, median (range) 9 (4–38) Conversion, n (%) 1 (0.68) Re-operation, n (%) 1 (0.68) EBL, estimated blood loss; ICU, intensive care unit; LOH, length of hospitalization; OR, operating room. View Large Table 2 Operative information Variable N = 147 OR time, min, mean ± SD 415.4 ± 84.6 EBL, mL, mean ± SD 158.3 ± 107.3 Length of ICU stay, day, mean ± SD 2.00 ± 4.5 LOH, day, median (range) 9 (4–38) Conversion, n (%) 1 (0.68) Re-operation, n (%) 1 (0.68) Variable N = 147 OR time, min, mean ± SD 415.4 ± 84.6 EBL, mL, mean ± SD 158.3 ± 107.3 Length of ICU stay, day, mean ± SD 2.00 ± 4.5 LOH, day, median (range) 9 (4–38) Conversion, n (%) 1 (0.68) Re-operation, n (%) 1 (0.68) EBL, estimated blood loss; ICU, intensive care unit; LOH, length of hospitalization; OR, operating room. View Large All patients underwent a complete resection (R0). The median tumor length was 3.0 (0.1–15.1) cm. Mean number of retrieved lymph nodes was 20.4 ± 8.9. Neoadjuvant therapy was administered to 114 (77.6%) patients. Of those, 54 patients had complete response (47.4%), 39 patients had partial response (34.2%) and 21 patients had no response (18.4%) (Table 1). Metrics of safety: postoperative complications Postoperative complications occurred in 37 patients (25.2%) (Table 3). There were 4 (2.7%) anastomotic leaks and 1 (0.68%) gastric staple line leak. All leaks were managed nonoperatively with endoscopic stenting, however 1 anastomotic leak failed endoscopic management and was managed with a re-operation. Other complications were as follows: chyle leak (n = 5, 3.4%), cardiac arrhythmias (n = 17, 11.6%), pneumonia (n = 10, 6.8%), respiratory failure requiring tracheostomy (n = 2, 1.4% (due to aspiration)), deep venous thrombus n = 2 (1.4%), and pulmonary embolus (n = 1, 0.68%). Complications occurred n = 24 (21%) of the patients who received neoadjuvant treatment whereas n = 13 (40%) of patients who did not have neoadjuvant treatment had complications (P = 0.04). Complications became less frequent as more cases were performed. There were 9 (31%) complications in the first 29 cases, and 28 (23.7%) in the subsequent cases (P = 0.01) (Fig. 4). The mean ICU stay was 2.00 ± 4.5 days and the median length of hospital stay (LOH) for all patients was 9 (4–38) days (Table 2). The median LOH for patients who did not experience a complication was 8 (4–17) days and 14.5 (7–38) days for those who experienced a complication (P < 0.001). Neither patient who suffered an intraoperative complication experienced a postoperative complication and both were discharged at 9 and 11 days, respectively. Mortalities were low for the entire cohort. There was 1 (0.6%) 30-day mortality and 2 (1.4%) 90-day mortalities. Fig. 4 View largeDownload slide Complications decreased with increasing surgeries performed. Fig. 4 View largeDownload slide Complications decreased with increasing surgeries performed. Table 3 Complications Complication N (%) Patients 37 (25.2) Wound infection 1 (0.68) Cardiac arrhythmias 17 (11.6) Anastomotic leak 4 (2.7) Gastric staple line leak 1 (0.68) Chyle leak 5 (3.4) Pneumonia 10 (6.8) Pulmonary embolism/DVT 3 (2.0)  DVT 2 (1.4)  PE 1 (0.68)  Respiratory failure requiring tracheostomy 2 (1.4) Pneumothorax 2 (1.4) Mortality  30-day 1(0.68)  90-day 2(1.4) Complication N (%) Patients 37 (25.2) Wound infection 1 (0.68) Cardiac arrhythmias 17 (11.6) Anastomotic leak 4 (2.7) Gastric staple line leak 1 (0.68) Chyle leak 5 (3.4) Pneumonia 10 (6.8) Pulmonary embolism/DVT 3 (2.0)  DVT 2 (1.4)  PE 1 (0.68)  Respiratory failure requiring tracheostomy 2 (1.4) Pneumothorax 2 (1.4) Mortality  30-day 1(0.68)  90-day 2(1.4) DVT, deep venous thromboembolism; PE, pulmonary embolism. View Large Table 3 Complications Complication N (%) Patients 37 (25.2) Wound infection 1 (0.68) Cardiac arrhythmias 17 (11.6) Anastomotic leak 4 (2.7) Gastric staple line leak 1 (0.68) Chyle leak 5 (3.4) Pneumonia 10 (6.8) Pulmonary embolism/DVT 3 (2.0)  DVT 2 (1.4)  PE 1 (0.68)  Respiratory failure requiring tracheostomy 2 (1.4) Pneumothorax 2 (1.4) Mortality  30-day 1(0.68)  90-day 2(1.4) Complication N (%) Patients 37 (25.2) Wound infection 1 (0.68) Cardiac arrhythmias 17 (11.6) Anastomotic leak 4 (2.7) Gastric staple line leak 1 (0.68) Chyle leak 5 (3.4) Pneumonia 10 (6.8) Pulmonary embolism/DVT 3 (2.0)  DVT 2 (1.4)  PE 1 (0.68)  Respiratory failure requiring tracheostomy 2 (1.4) Pneumothorax 2 (1.4) Mortality  30-day 1(0.68)  90-day 2(1.4) DVT, deep venous thromboembolism; PE, pulmonary embolism. View Large Readmission rate at 90 days was 5.4% (n = 8). Reasons for readmission included: Pulmonary embolus or DVT (n = 3), pneumonia (n = 2), dysphagia (n = 1), anxiety attack (n = 1), nausea/vomiting (n = 1). Readmissions were higher in the patients who experienced a postoperative adverse event. There were 3 (8.1%) readmissions in patients who experienced a postoperative complication, and 5 (4.5%) in those patients who did not experience an adverse event postoperatively, P = 0.4. DISCUSSION We report our series of 147 robotic-assisted Ivor–Lewis esophagectomies. The length of operation is a significant concern in patients undergoing robotic procedures. However, we have demonstrated that the length of operation decreases steadily as more cases are performed. The mean operative time was decreased to 346 minutes after 120 cases. This time is comparable to our series with thoracoscopic and laparoscopic approaches at 320 minutes.1 The EBL was low at 150 mL and the mean ICU stay was only 2 days. The LOH was 9 days and 14.5 days if patients experienced a complication. Oncologic outcomes as measured by R0 resection rates and lymph node harvest were also comparable if not better than other approaches to esophagectomy. All of our patients underwent R0 resections and the mean LN harvest was 20.4 despite 77.5% of patients undergoing neoadjuvant therapy. Complications occurred in only 37 patients (25.2%) and occurred less frequently in those patients treated with neoadjuvant therapy (21% vs. 40%, P = 0.042). Additionally, complications occurred less frequently later in our series after the learning curve was surpassed 31% versus 23.7% (P = 0.01). Readmission rates were low at 5.4% and did increase to 8.1% if a patient experienced a postoperative complication. Surgical resection is an integral part of the treatment algorithm for early stage and locally advanced esophageal cancer. The morbidity associated with esophagectomy can be as high as 60% even in tertiary centers.13,14 Pulmonary and cardiovascular complications such as atelectasis, pneumonia, atrial fibrillation, wound infection, anastomotic leak, and chylothorax are among the most commonly seen postoperative complications and may increase the risk of mortality.14 Patients who were treated with neoadjuvant therapy had a lower complication rate including anastomotic leak (AL). Several authors have reported similar findings associated with neoadjuvant therapy. Tapias et al. demonstrated that in patients who received NCR, there was a low incidence of AL in open Ivor–Lewis esophagectomy and RAIL (1.4% and 0%, respectively).15 Our results mimic the Tapias study where we report 0.9% AL in NCR who underwent RAIL. We hypothesize that NCR may increase the vascularity of tissues and increase serum vascular endothelial growth factor (VEGF) levels. This was demonstrated in a pathologic analysis of 92 esophagectomy specimens where mean tumor vessel density and VEGF staining were higher in NCR patients resulting in increased serum VEGF levels.16 The increase in VEGF levels might potentially result from vascularized stromal fibroblast, and the resultant increase in granulation may increase healing and result in decreased AL.17 The most common complication in our series was cardiovascular-related complications, including 1 acute myocardial infarction leading to death. Other cardiovascular complications were nonlethal and were mostly arrhythmias. The second most common complication in our series was pneumonia although low at 6.8%. Cardiopulmonary complications occur less commonly in minimal invasive esophagectomy compared to open techniques.7-9 We have demonstrated a similar trend with the robotic approach. However, there are no data currently as to whether pulmonary complications differ between robotic techniques versus other minimal invasive approaches. There are numerous series comparing outcomes of minimally invasive Ivor–Lewis esophagectomy to the open approach. Cardiopulmonary complications, blood loss, ICU stay as well as hospital stay are shown to be reduced in minimal invasive techniques.11,18,19 In addition, 30 day mortality and leak rates are low at 0–6.6%20 and 0–10%, respectively, for the minimal invasive approach.20-23 In our series the mortality was 1.3% and the anastomotic leak rate was 2.7%, which is in the lower range of what has been reported for minimal invasive techniques. Lymph node retrieval is similar between the open and minimal invasive approach.20-24 Moreover, the number of lymph nodes harvested in the current report is 20 which is also within the range that has been reported for minimal invasive techniques.23,25-27 Therefore we conclude that robotic surgery, in experienced hands, is not inferior to other minimal invasive or open techniques in terms of complications, perioperative and oncologic outcomes. Multiple authors have reported their results with robotic-assisted esophagectomy.28-30 Robotic assisted or completely robotic esophagectomies are performed via transhiatal, McKeown, or Ivor–Lewis approaches. They report leak rates varying between 10 and 33%28,29,31-33 which is high compared to other minimally invasive techniques. Operative times also vary greatly (180–556 min) although techniques are not uniform. The number of resected lymph nodes varied between 14 and 36 and blood loss was as high as 1600 mL in some series.32 Our experience with robotic esophagectomy demonstrates lower anastomotic leaks, complications, EBL, and operative times emphasizing that our operative outcomes, morbidity, and mortality rates are low compared to what has been reported in the literature for the robotic Ivor–Lewis approach.28,29,31,33,34 The robotic approach does require technical expertise by the operating surgeon and an OR team familiar with the intricacies of using the robot such as set-up, docking, and instrument exchange. Efficacy and feasibility of robotic surgery for complex esophageal surgery has been evaluated and found to offer enhanced three-dimensional visualization and advanced articulation with wrist-like motion. The potential obstacle to adoption of this technique is the long learning curve required to achieve proficiency. In our experience, there was a significant reduction in operative time after completing 20 cases (514 minutes vs. 397 minutes, P < 0.005). In this study, we have demonstrated that OR time decreased further to 346 minutes after 120 cases. During our initial evaluation of outcomes after our first fifty-two cases, we reported one case of anastomotic leak and no deaths. After 29 cases, the complications decreased from 31% to 23.8% with an overall complication rate at 26.9%. Additionally, there were no conversions to open thoracotomy and all patients in the series received an R0 resection.12 The range of operative time in minimal invasive techniques is reported to be between 249 and 535 minutes.23,25-27,35 Sarkaria and Rizk reported a similar learning curve. Their initial average operative time for the first 15 patients was 600 minutes, which came down to average of 370 minutes for the last 5 patients in their cohort.29 Unfortunately, there are no randomized data comparing the robotic trans-thoracic approach to conventional minimally invasive techniques. van der Sluis et al have proposed the first randomized trial comparing the open approach to robotic assisted minimally invasive thoracolaparoscopic esophagectomy for resectable esophageal cancer (ROBOT trial).36 We would expect similar results to Bierre's randomized trial comparing thoracoscopic esophageal resection to the conventional open approach.11 The ROBOT trial will perhaps provide additional data over benefits compared to open approaches however it will not aid us in determining an optimal minimally invasive approach. We acknowledge the potential limitations of this study due to the retrospective nature of this review. There is significant potential for selection bias in retrospective studies. Additionally, the causal and temporal relationship among variables can be difficult to assess. This cohort includes all consecutive patients undergoing RAIL at a single institution. All procedures were performed by a single surgeon thereby minimizing variation in operative technique or learning curve as a factor in analyzing outcome data. Thus, these factors serve to minimize potential biases. CONCLUSION To our knowledge, this represents the largest series of robotic Ivor–Lewis esophagectomies performed to date. We have demonstrated that RAIL is a safe surgical technique, which has comparable early outcomes to traditional minimal invasive esophagectomy approaches. This is evidenced by operative times, length of time in an ICU, overall hospitalization, and risk of complications or death. The learning curve is long and requires specialized training. This need for advanced training, long learning curves, and cost remain substantial barriers to the implementation of a robotic esophageal program. However robotic surgery is an advancing technology that provides surgeons with improved visualization and more ergonomic instruments thus enhancing the versatility over conventional approaches. Randomized trials are necessary and are in process to enable us to make more precise conclusions about the superiority of one surgical technique over the other. Disclosures Drs. K. Meredith, O. Andacoglu, R. Shridhar, and Ms. Huston have no conflicts of interest or financial ties to disclose. Notes Specific author contributions: Kenneth Meredith participated in the study design, analysis and interpretation of data, and drafting and critical revision of the manuscript. Jamie Huston participated in the study design and data collection. Oya Andacoglu participated in data collection, and drafting and critical revision of the manuscript. Ravi Shridhar participated in the study design, analysis and interpretation of data, and critical revision of the manuscript. All authors read and approved the final manuscript. Source of Funding: None. References 1 Yamamoto S , Kawahara K , Maekawa T et al. Minimally invasive esophagectomy for stage I and II esophageal cancer . Trials 2005 ; 80 : 1421 – 6 . 2 Jemal A , Siegel R , Ward E et al. Cancer statistics, 2008 . CA Cancer J Clin 2008 ; 58 : 71 – 96 . Google Scholar CrossRef Search ADS PubMed 3 McLoughlin J M , Melis M , Siegel E M et al. Are patients with esophageal cancer who become PET negative after neoadjuvant chemoradiation free of cancer ? J Am Coll Surg 2008 ; 206 : 879 – 86 ; discussion 86–7 . Google Scholar CrossRef Search ADS PubMed 4 NCCN Clinical Practice Guidelines in Oncology: Esophageal and Esophagogastric Junction Cancers . 2013 , https://www.nccn.org/. Accessed October 23, 2016 . 5 Luketich J , Pennathur A , Awais O et al. 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Ivor– Lewis esophagectomy with manual esogastric anastomosis by thoracoscopy in prone position and laparoscopy . Surg Endosc 2010 ; 24 : 1482 – 5 . Google Scholar CrossRef Search ADS PubMed 28 Clark J , Sodergren M H , Purkayastha S et al. The role of robotic assisted laparoscopy for oesophagogastric oncological resection; an appraisal of the literature . Dis Esophagus 2011 ; 24 : 240 – 50 . Google Scholar CrossRef Search ADS PubMed 29 Sarkaria I , Rizk N . Robotic-assisted minimally invasive esophagectomy: the Ivor–Lewis approach . Thorac Surg Clin 2014 ; 24 : 211 – 22 . Google Scholar CrossRef Search ADS PubMed 30 Park S , Kim D , Do Y et al. The oncologic outcome of esophageal squamous cell carcinoma patients after robot-assisted thoracoscopic esophagectomy with total mediastinal lymphadenectomy . Ann Thorac Surg 2017 ; 103 : 1151 – 57 . Google Scholar CrossRef Search ADS PubMed 31 Anderson C , Hellan M , Kernstine K et al. Robotic surgery for gastrointestinal malignancies . 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Google Scholar CrossRef Search ADS PubMed 36 van der Sluis P , Ruurda J , van der Horst S et al. Robot-assisted minimally invasive thoracolaparoscopic esophagectomy versus open transthoracic esophagectomy for resectable esophageal cancer, a randomized controlled trial (ROBOT trial) . Trials 2012 ; 13 : 230 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of International Society for Diseases of the Esophagus. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Diseases of the EsophagusOxford University Press

Published: May 1, 2018

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