Robotic-assisted minimally invasive esophagectomy for treatment of esophageal carcinoma Philip W. Chiu, Anthony Y. Teoh, Vivien W. Wong, Hon Chi Yip, Shannon M. Chan, Simon K. Wong & Enders K. Ng Journal of Robotic Surgery ISSN 1863-2483 J Robotic Surg DOI 10.1007/s11701-016-0644-2
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Author's personal copy J Robotic Surg DOI 10.1007/s11701-016-0644-2
ORIGINAL ARTICLE
Robotic-assisted minimally invasive esophagectomy for treatment of esophageal carcinoma Philip W. Chiu1,2,3 • Anthony Y. Teoh1,3 • Vivien W. Wong1,3 • Hon Chi Yip1,3 Shannon M. Chan1,3 • Simon K. Wong1,3 • Enders K. Ng1,2,3
•
Received: 24 April 2016 / Accepted: 10 October 2016 Ó Springer-Verlag London 2016
Abstract Minimally invasive esophagectomy (MIE) is technically challenging. Da Vinci Robotic system could improve surgical dissection with additional degree of freedom from robotic arms. This study aimed to assess the feasibility and safety of performing MIE using Da Vinci Robotic system among patients with esophageal cancers. From 2009 to 2013, consecutive patients with esophageal cancers who received robotic-assisted MIE were recruited. We excluded tumors with suspected invasion to adjacent organs. Preoperative staging included EUS, CT thorax and abdomen and bronchoscopy. We perform mobilization of thoracic esophagus with two-field lymphadenectomy using robotic system, followed by laparoscopic gastric mobilization and hand-sewn cervical esophagogastric anastomosis. A total of 20 patients were recruited (16 male and 4 female) with mean age of 64.2 ± 8.8 years. All patients
were successfully treated with robotic-assisted MIE with mean operative time of 499.5 ± 70 min and blood loss of 355.7 ± 329.6 mls. There was no pulmonary complication, while three patients sustained anastomotic leakage and managed conservatively. The mean hospital stay was 13 ± 6 days. Five patients had stage I tumors, five had stage II, and nine had stage III disease. One patient had complete response after neoadjuvant chemoradiotherapy. The number of lymph node dissection was 18.2 ± 13.2, and 2.8 ± 5.7 nodes involved. The follow-up period was 21 ± 9 months, and the overall survival was 75 %. Robotic-assisted MIE is feasible and safe for treatment of esophageal cancers. The surgical dissection can be enhanced by improved ergonomics from robotic arms and sense of depth from 3D images. Keywords Robotic esophagectomy Robotic surgery Minimally invasive esophagectomy Carcinoma of esophagus
This manuscript was partially presented as oral presentation during the annual meeting of the International Society of Disease of Esophagus in Venice, Italy 2012.
Electronic supplementary material The online version of this article (doi:10.1007/s11701-016-0644-2) contains supplementary material, which is available to authorized users. & Philip W. Chiu
[email protected] 1
CUHK Jockey Club Minimally Invasive Surgical Skills Center, The Chinese University of Hong Kong, Hong Kong, China
2
Chow Yuk Ho Technology Center for Innovative Medicine, The Chinese University of Hong Kong, Hong Kong, China
3
Division of Upper GI and Metabolic Surgery, Department of Surgery, The Chinese University of Hong Kong, Hong Kong, China
Introduction Although esophagectomy remained as the conventional treatment for esophageal cancer, it is associated with significant morbidities and mortality [1]. The perioperative mortality amounts to 2–4 %, while the overall morbidity rate was reported to be more than 50 % [2–4]. Of all the major morbidities, pneumonia is one of the most common complications. The rate of pulmonary complication can be up to 57 % if an open thoracotomy was adopted with single-lung ventilation [4, 5]. Recently, the development of minimal invasive esophagectomy (MIE) reduced the pain induced by thoracotomy where small incisions were employed to perform the occurrence of pneumonia [6].
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Minimal invasive esophagectomy can be difficult using conventional instruments, especially in the confined space within the thoracic cavity surrounded by rigid cage of ribs. The Da Vinci Robotic system can theoretically improve surgical dissection with higher degree of freedom from the robotic arms, as well as the three-dimensional images with augmented depth sensation. This is a pilot study to assess the feasibility and safety in performing MIE using Da Vinci Robotic system among patients with esophageal cancers.
Methods This is a retrospective review on a prospectively collected database of patients with esophageal cancers who received surgical treatment at university affiliated hospital from 2009 to 2013. The objective of this study was to investigate the feasibility and safety of performing minimally invasive esophagectomy using Da Vinci Robotic system. Patients who were diagnosed to have esophageal cancer were assessed at the multi-disciplinary gastrointestinal cancer clinic of the Prince of Wales Hospital, Chinese University of Hong Kong. Those who received Da Vinci robotic-assisted minimally invasive esophagectomy (RAMIE) were reviewed. Patients who were age more than 75 years, ASA grade of greater than IV, or those who were unfit for general anesthesia and one-lung ventilation would not be considered for esophagectomy. A standardized protocol for preoperative workup and staging included EUS, CT thorax and abdomen and bronchoscopy. The study was conducted and reported according to the Declaration of Helsinski.
Surgical approach: RAMIE Thoracic stage All the procedures of robotic-assisted MIE were standardized to three-staged esophagectomy. The first stage was transthoracic mobilization of esophagus using Da Vinci Robotic system. The patient was placed in a semiprone position, and one-lung ventilation was induced using the technique of bronchial blockage or double lumen tube (Fig. 1). The 3D laparoscope port (12 mm) was placed at mid-axillary line at 6th intercostal space, while two working ports (8 mm) would be inserted at 5th intercostal space over anterior and posterior axillary line. A minithoracotomy of 30 mm in size was opened at 4th intercostal space over anterior axillary line adjacent to the nipple. After adequate collapse of the right lung, the intrathoracic esophageal mobilization was first started over
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anterior side of esophagus around right main bronchus. The subcarinal lymph nodes were dissected en-bloc with the esophagus. The inferior mediastinal pleura was opened above and below the arch of azygos, and the arch of azygos would be transected using endostapling device. Para-aortic lymph node dissection was then performed, with positive identification of the thoracic duct (Fig. 2). The proximal and distal ends of thoracic duct were controlled with three hem-o-lock clips or metal clips before transection (Fig. 3). The thoracic duct was dissected en-bloc with the periesophageal nodes. After full mobilization of the thoracic esophagus was completed, the Da Vinci Robotic system would be undocked. Gastric mobilization The second stage would be mobilization of the stomach for gastric pullup. At the initial two cases RAMIE, gastric mobilization was performed by open laparotomy. After the success of robotic-assisted esophageal dissection, gastric mobilization was standardized to laparoscopic approach. The techniques of laparoscopic gastric mobilization included dissection over gastrocolic ligament, transection of the left gastroepiploic artery and short gastric arteries, mobilization of the lesser omentum and control of the left gastric artery. Lymph node dissection would be performed at stations seven and nine. The esophagus would be mobilized at the cervical level with synchronous two team approach. After transection of the cervical esophagus, the esophagus would be pulled down into the abdomen. The specimen together with the fully mobilized stomach would be exteriorized through a 3-cm horizontal incision over the right subcostal region. The esophagus would be transected together with lymph nodes over lesser curvature, left gastric artery, and coeliac axis. The gastric tube would be performed using endostapling techniques (Fig. 4). After performance of pyloroplasty, the gastric tube would be delivered back into the peritoneal cavity. The stomach would be pulled up to the neck for anastomosis under direct laparoscopic view. Cervical phase An oblique left incision would be performed over the anterior border of the sternocleidomastoid muscle. The omohyoid muscle was routinely ligated and transected, and the cervical part of esophagus was exposed after dissection medial to the carotid sheath. The left recurrent laryngeal nerve would be positivity identified, protected, and confirmed using facilities for intraoperative nerve monitoring. After complete mobilization of the cervical esophagus, the distal part was transected 5 cm below cricopharyngeus. After delivery of the gastric tube from the abdomen to the
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Fig. 1 Patient position and port placement for robotic MIE
Fig. 2 Robotic MIE with two-field nodal dissection at para-aortic lymph nodes
Fig. 4 Formation of gastric tube after laparoscopic mobilization of stomach
Perioperative management and follow-up
Fig. 3 Control of thoracic duct above diaphragm with clips
cervical incision, esophagogastric anastomosis would be performed using hand sewing technique over the cervical incision.
All the patients who received esophagectomy for treatment of esophageal cancer would be assessed and regularly follow-up at the Gastrointestinal Cancer Clinic (GICC) of the Prince of Wales Hospital, The Chinese University of Hong Kong. For each clinical follow-up, the patients would be assessed clinically for evidence of cancer recurrence, and regular CT thorax and abdomen would be performed at 2 years after surgery for detection of local and system recurrence. Regular blood tests including complete blood picture, renal and liver function tests would be performed at three monthly intervals.
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Author's personal copy J Robotic Surg Table 1 Baseline demographics and operative outcomes for RAMIE
Table 1 continued
Robotic-assisted minimally invasive esophagectomy (n = 20)
Number of lymph node dissected
18.2 ± 13.2
Age (mean)
64.2 ± 8.8
Number of lymph node involved
2.8 ± 5.7
Gender (male to female)
16:4
Clearance of resection margins
20 (100 %)
Number of comorbidities (median [range])
1 (0–2)
Mean follow-up (months)
21 ± 9
Preoperative FEV1 (mean ± SD)
2.25 ± 0.51
Overall survival at 24 months
15 (75 %)
Dysphagia
18 (90 %)
Regurgitation
3 (15 %)
Outcome assessment
Clinical symptoms on presentation
Gastrointestinal bleeding
2 (10 %)
Weight loss
10 (50 %)
Dysphagia score (median [range])
1 (1–3)
Location of the squamous esophageal cancer (upper/middle/lower)
0/7/13
Mean tumor length (cm) (mean ± SD)
5.2 ± 2.1
Circumferential involvement of tumor on OGD
10 (50 %)
Results
Tumor biopsy Squamous cell carcinoma
17
Adenocarcinoma
3
Robotic thoracic esophageal dissection
18
Conversion to open thoracotomy
2
Reasons for conversion Difficulty in dissection Failure for transoral anastomosis Laparoscopic gastric mobilization
1 1 16
Reasons for open gastric mobilization First two cases of robotic MIE
2
Cases of conversion to thoracotomy
2
Total operative time (mean ± SD) (min)
499.5 ± 70.1
Blood loss (mean ± SD)
335.7 ± 329.6
ICU stay (mean ± SD) (days)
1.7 ± 1.2
Hospital stay (mean ± SD) (days)
13 ± 6
30 days mortality (%)
1/20
Cause of mortality
Acute myocardial infarction on day 4
Morbidities Pneumonia Pleural effusion
1 (5 %) 8 (40 %)
Anastomotic leakage
3 (15 %)
Chylous leakage
1 (5 %)
Conduit ischemia
0 (0 %)
Recurrent laryngeal nerve palsy (transient)
5 (25 %)
Pathology T1bN0
3
T1bN1
2
T2N0
4
T2N1
1
T3N1 T3N2
5 2
T3N3
2
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The outcomes parameters were prospectively collected by research nurses at the gastrointestinal cancer clinic from the first attendance to the latest follow-up. These parameters included baseline demographics, preoperative investigations, tumor staging, operative, and clinical outcomes.
From 2009 to 2013, a total of 20 patients who were diagnosed to have esophageal cancers received robotic-assisted MIE. There were 16 male and 4 female patients with a mean age was 64.2 ± 8.8 years (Table 1). Most patients complained of dysphagia (90 %) as primary symptom, while half of the patients sustained significant weight loss before operation. The median dysphagia score before operation was 1 (1–3) indicating that most patients can tolerate semisolid food. The preoperative mean FEV1 was 2.25 ± 0.5, and the mean FVC was 2.96 ± 0.67. Upper endoscopy showed the average length of the tumor was 5.2 ± 2.1 cm, and 50 % of patients were having circumferential tumor involvement. Biopsies and histopathology confirmed squamous esophageal cancers in 17 of the 20 patients, while 3 patients were having adenocarcinoma. Majority of the tumors were located at mid and lower esophagus. All the patients successfully received robotic-assisted MIE except two patients who required conversion to open thoracotomy. One patient had dense tumor adhesion to the trachea requiring conversion for dissection, and intra-thoracic anastomosis using orvil circular stapling device failed for another patient due to anatomotical limits at superior mediastinum. The mean total operative time was 499.5 ± 70.1 min, and the mean blood loss was 355.7 ± 329.6 mls. Majority of the patients stayed in the intensive care unit (ICU) for only 1 day, and the mean hospital stay was 13 ± 6 days. Only one patient succumbed within 30 days after surgery due to massive acute myocardial infarction. Concerning morbidities, one patient had pneumonia after operation, while eight patients suffered from pleural effusion. Three patients sustained anastomotic leakage, which were successfully managed by conservative approach with endoscopic stenting, control of
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sepsis and total parental nutrition. Five patients sustained transient recurrent laryngeal nerve palsy, and these occurred at the initial phase of the study. With the introduction of routine intraoperative monitoring, the rate of recurrent laryngeal nerve palsy had significantly reduced. Although the first five patients receiving robotic MIE were having early stage esophageal cancers, most of the patients in the study were having advanced esophageal cancer with nodal metastasis. The mean number of lymph node dissected was 18.3, and the average involved lymph node was 2.5. All patients had clear resection margins. The mean follow-up period was 21 ± 9 months, and 15 patients (75 %) survived and remained disease free.
Discussion Esophagectomy is considered as one of the surgeries in ultra-major scale that carries significant morbidity and mortality [1]. The outcome of esophagectomy is directly related to surgeons’ experience and hospital volume. One of the important complications after esophagectomy is pneumonia due to one-lung ventilation, prolonged collapse of the lung and significant pain induced from open thoracotomy. Hulscher et al. conducted a prospective randomized trial to compare transthoracic against transhiatal esophagectomy for adenocarcinoma of esophagus [4]. The rate of pulmonary complication was significant lower for the transhiatal esophagectomy group when compared to those receiving transthoracic esophagectomy (27 % compared to 57 %; p \ 0.001). Through transhiatal esophagectomy avoided one-lung ventilation, subgroup analysis showed that 5-year locoregional disease free survival was significantly better for transthoracic group with 1–8 lymph nodes in the resection specimen when compared to transhiatal group (64 vs 23 %; p = 0.02) [5]. Minimal invasive esophagectomy (MIE) aimed to achieve transthoracic esophagectomy and adequate lymph node dissection while reducing morbidities related to open thoracotomy [6–9]. Luketich et al. reported excellent outcomes of more than 1000 patients receiving MIE, with 481 patients receiving McKeown three-staged MIE and 530 patients receiving Ivor Lewis three-staged MIE [6]. The median number of lymph node dissected was 21, and the operative mortality was 1.68 %. Smithers et al. compared the results of 309 patients who received thoracoscopic-assisted esophagectomy, 23 patients who received total MIE to 114 patients who received open esophagectomy [10]. Results showed that MIE was associated with significantly lower blood loss, shorter length of stay with no difference in the number of lymph node dissected. Dunst and Swanstrom summarized the clinical outcomes of open esophagectomy against MIE [11]. The incidence of
pneumonia was generally lower for patients receiving MIE then open esophagectomy. Another meta-analysis including 12 comparative studies between MIE and Open esophagectomy showed that MIE achieved a significantly lower rate of pneumonia, lower blood loss and shorter hospital stay [12]. A recent review on the Hospital Episode Statistics in United Kingdom demonstrated a significant increase in the adoption of MIE for treatment of esophageal cancer among 18,673 esophagectomies performed over a 12-year period [13]. Although MIE conveyed better perioperative results, there are several barriers to utilization and adoption of such approach. Osugi et al. studied the learning curve for MIE among 80 patients comparing the outcomes of first 34 patients to the last 46 patients [14]. There was a significantly longer operative time, higher blood loss and incidence of pneumonia as well as lower mediastinal nodes dissected in the first group when compared to second group. A learning curve of at least 50 cases of MIE was reported [11]. Ideally, MIE should be practiced by surgeons with high volume and experienced in both advanced laparoscopy and thoracoscopy. The dissection remained a surgical challenge using rigid instruments especially within the confined thoracic cavity. Theoretically, Da Vinci Robotic Surgical System might enhance transthoracic MIE through improvement in ergonomics from the robotic arms and the sensation of depth through three-dimensional images [15]. These features improved the surgical dissection and suturing within a confined body cavity and reduce the learning curve for clinical application of MIE. Our study demonstrated that robotic-assisted MIE is feasible and safe for treatment of patients with esophageal cancers. Among patients who received robotic-assisted MIE, the total operative time was 500 min, and the average postoperative stay in ICU was less than 2 days. Although the operative time was slightly longer than the reported series, the anesthetic preparation and repositioning of the patients after transthoracic stage was included into the timing, which typically took 30–40 min. Only one of the twenty patients after robotic MIE developed pneumonia. The low rate of pneumonia is likely related to the minimally invasive approach with small incisions and reduced pain, early extubation and minimal manipulation of the collapsed right lung during the procedure. 40 % of patients had pleural effusion on the contralateral side. This was likely related to extensive mediastinal nodal dissection leading to fluid collection over the left pleural cavity. The use of robotic system greatly enhanced mediastinal nodal dissection as the mean number of lymph node dissected as 18.2 ± 13.2. Five patients sustained transient recurrent laryngeal nerve injury at cervical stage. After routine use of intraoperative recurrent laryngeal nerve monitoring, the rate of RLN injury significantly reduced.
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15 % of patients developed anastomotic leakage, while all of these were managed conservatively by adequate cervical drainage and endoscopic stenting without the need of reoperation. Kernstein et al. reported the first robotic esophagectomy with three field lymphadenectomy in 14 patients. There was a technical evolvement within those 14 patients, with the last 8 patients receiving a complete robotic esophagectomy [15]. The patients positioning was similar to this study where patients were placed into a semi-prone position during thoracic part. Majority of the studies on MIE reported an advantage of prone position during the thoracic phase as the collapsed right lung could be retracted naturally by gravity. Moreover, traction from the pulmonary attachments to mediastinum would open up spaces and enhance mediastinal dissection [9, 14]. Since the development of MIE at our unit, we have adopted the semiprone positioning. This is a compromised position between anesthetists and surgeons to facilitate surgical dissection through retraction pull to expose the mediastinum from the collapse lung while providing access for anesthetic assessment during the procedure. Kim et al. reported the performance of robotic-assisted thoracoscopic esophagectomy in prone position by a surgical oncologist on 21 patients with esophageal cancer without prior experience in thoracoscopic esophagectomy [16]. The number of lymph nodes dissected was 38.0 ± 14.2, while the robotic console time significantly reduced after the first 8 patients. This study illustrated the advantage of the robotic system in performing esophagectomy as illustrated by the steep learning curve with shortening of console time. Suda et al. conducted a prospective study on robotic-assisted against thoracoscopic radical esophagectomy on 36 patients with squamous esophageal cancer [17]. The authors found that robotic assistance significantly reduced the incidence of vocal cord palsy and hoarseness as compared to thoracoscopic esophagectomy. This could be attributed to improved surgical ergonomics and dissection through the robotic arms and 3D visualization of the operative field. Cerfolio et al. reported the performance of Robotic Ivor Lewis esophagectomy with robotic-assisted double layer hand-sewn esophagogastric anastomosis in 22 patients [18]. Only one patient sustained anastomotic leakage and the authors preferred intrathoracic anastomosis to avoid left recurrent laryngeal nerve injury and reduced conduit ischemia. We have considered the performance of robotic Ivor Lewis esophagectomy at the start of our study. However, since majority of the esophageal cancers in our locality were squamous esophageal cancers, at least half of our patients will required the performance of three-staged esophagectomy for treatment. Therefore, we decided to develop the techniques of robotic-assisted three-staged MIE and performed cervical anastomosis.
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There are several limitations of this study. First, this is a retrospective cohort study on a single center experience in performing robotic-assisted MIE. There would be significant bias in patients’ selection for suitability of roboticassisted MIE. Second, the results may not be applied generally as all the procedures were performed by single surgeon with good experience and check record for MIE. Thirdly, the mean follow-up period was only 21 months. A long-term study is necessary to assess the oncological outcomes and survival. In conclusion, this is a pilot prospective study to confirm the feasibility and safety of robotic-assisted MIE for treatment of squamous esophageal cancer. Further clinical studies should be conducted with long-term follow-up to assess the oncological clearance, recurrence and survival after receiving robotic-assisted MIE for treatment of esophageal carcinoma. Compliance with ethical standards Conflict of interest Philip Chiu, Anthony Teoh, Vivien Wong, HC Yip, Shannon Chan, Simon Wong and Enders Ng declare that they have no conflict of interest.
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