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Ann Thorac Surg 2005;80:1202-1206
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Robotic-Assisted Thoracoscopic Surgery (RATS) for Benign and Malignant Esophageal Tumors

Johannes C. Bodner, MD a , Matthias Zitt, MD a , Harald Ott, MD b , Gerold J. Wetscher, MD a , Heinz Wykypiel, MD a , Paolo Lucciarini, MD a , Thomas Schmid, MD a , *

a Clinical Department of ?General and Transplant Surgery, Innsbruck Medical University, Innsbruck, Austria
b Clinical Department of Cardiac Surgery, Innsbruck Medical University, Innsbruck, Austria

Accepted for publication March 16, 2005.

* Address reprint requests to Dr Schmid, Department of General and Transplant Surgery, Innsbruck Medical University, Anichstrasse 35, A-6020 Innsbruck, Austria (Email: thomas.schmid{at}uibk.ac.at).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Robotic surgical systems are most effective for operations in areas that are small and difficult to reach. Ideal indications for this new technology have yet to be established. The esophagus possesses attributes that are interesting for general thoracic robotic surgeons.

METHODS: Robotic-assisted thoracoscopic surgery (RATS) using the da Vinci system (Intuitive Surgical, Inc, Mountain View, CA) was performed in six patients with esophageal tumors. This comprised the dissection of the intrathoracic esophagus including lymph node dissection in four patients suffering from esophageal cancer and the extirpation of a benign lesion (one leiomyoma and one foregut cyst) in the remaining two patients.

RESULTS: All procedures were completed successfully with the robot. The median overall operating time was 173 (160–190) minutes in the oncologic cases and 121 minutes in the benign cases, including the robotic act of 147 (135–160) minutes and 94 minutes, respectively. There were no intraoperative complications. One patient had to undergo a redo thoracoscopy because of a persistent lymph fistula. One cancer patient died after 12 months due to tumor progression and another patient had to be stented due to local tumor recurrence 19 months postoperatively.

CONCLUSIONS: This first small series of various esophageal pathologies treated by robotic-assisted thoracoscopic surgery supports the impression that the esophagus is an ideal organ for a robotic approach. The potential of the da Vinci system, especially for oncologic indications, remains to be proven in future clinical trials.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Minimally invasive approaches have become increasingly popular in esophageal operations [1]. However, these procedures are advanced and require experienced surgeons with a particular set of skills. Standard laparoscopic instruments are rigid and provide a finite freedom of movement. Visualization of the operating field is flat and in only two dimensions.

Robotic surgical systems were developed to overcome these limitations. The high-definition, three-dimensional image of the da Vinci robotic system (Surgical Intuitive, Mountain View, CA) facilitates identification of anatomy and dissection during surgery. The full range of motion of the multiarticulated instruments is beneficial in completing complex laparoscopic tasks such as suturing and intracorporal knot tying. Tremor filtration and motion scaling allow for more precise movements [2].

These benefits of robotic procedure are most advantageous when operating in remote areas which are difficult to reach, whereas procedures requiring frequent instrument changes in an open operating field are less suitable [3, 4]. Thus in general surgery, appropriate indications are limited, although the esophagus may prove to be an ideal organ for robotic procedure. The robotic esophageal interventions analyzed in this report were designed to test this hypothesis.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
From March 2002 to May 2004 thoracoscopic esophageal interventions were performed with the da Vinci robotic system in six patients. This consisted of dissection of the entire esophagus as part of an abdomino-cervical procedure for esophageal cancer in four patients and the extirpation of an esophageal leiomyoma and a foregut cyst in one patient each. The da Vinci surgical system was approved by our local ethics committee and informed consent was obtained from all patients. In this initial series, patient selection for the robotic procedure was not randomized. The patient characteristics are given in Table 1.


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  		Table 1. Patient Characteristics
 
All procedures were performed from the right. For esophageal dissection, patients were placed in an over-wound left lateral decubitus position. Complete left lateral decubitus position was used in the patients with the leiomyoma and the foregut cyst. A double-lumen endotracheal tube was employed to selectively ventilate the left lung.

Operative Techniques
Esophageal dissection
The robotic cart was situated at the right upper side of the patient (Fig 1A). The trocars for the robot (one 10-mm trocar for the camera and two 8-mm trocars for the arms) were placed far caudally (camera trocar in the ninth intercostal space in the midaxillary line, left robotic arm in the ninth intercostal space in the posterior-axillary line, right robotic arm in the eighth intercostal space in the anterior-axillary line; Fig 1B). Two 10-mm auxiliary ports for suction and retraction of the deflated lung were positioned between the left robotic arm and the camera arm and in the fourth intercostal space medial to the anterior axillary line, respectively. The first (camera) port was inserted using an open technique; the other trocars were positioned under direct thoracoscopic vision after lung deflation. The right lung was retracted laterally, exposing the esophagus. The mediastinal pleura overlying the esophagus was divided and the entire esophagus was exposed. After division of the azygos vein, using a vascular endostapler, circumferential mobilization of the esophagus, including surrounding lymph nodes and periesophageal tissue, was performed from the diaphragmatic reflection to the thoracic inlet. To facilitate the dissection of the posterior aspect, the esophagus was intubated with a 12 French gastric tube and retracted anteriorly with a strap. The robotic thoracoscopic dissection of the esophagus was part of an abdomino-cervical procedure. The abdominal part and the anastomosis of the greater curvature tube with the cervical esophagus were performed openly.



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  		Fig 1. Adjustment in the operating room (A) and patient‘s placement with trocar positioning (B) of robotic esophageal dissection. {cjs2113} = right and left arm; {blacksquare} = camera trocar; {square} = auxiliary trocars. (S = surgeon; TS = tableside surgeon; AN = anesthetist; SN = scrub nurse.)

 
Esophageal leiomyoma (Fig 2)
Robotic cart positioning and trocar placement were identical to the esophageal dissection procedure. The tumor was deep to the azygos vein and the parietal pleura was incised to expose the esophagus. After division of the azygos vein using a vascular endostapler, a 270 degree mobilization of the esophagus over a distance of 10 cm was performed using the robotic cautery hook. Thereafter, the lesion was identified and an esophageal myotomy of approximately 6 cm was performed. The leiomyoma demonstrated the typical findings of an intact underlying mucosa and its location within the muscularis propria. The integrity of the mucosa was confirmed by simultaneous upper endoscopy and gas insufflation. The tumor was removed in an endobag and the myotomy was closed using single sutures (Fig 3).



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  		Fig 2. Esophageal leiomyoma (endoscopic image) before robotic-assisted thoracoscopic surgery–resection.

 


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  		Fig 3. Robotic single stitch closure of the myotomy after tumor enucleation.

 
Foregut cyst
The robotic cart was situated at a left lower angle to the patient. The three robotic trocars were placed in the fifth and seventh intercostal spaces between the midclavicular and the midaxillary line and no auxiliary port was needed. The lesion of about 5 cm diameter was located in the lower esophagus in the posterior phrenicocostal sinus and partially covered by the esophageal muscular layer. For better exposure, the diaphragm was intermediately fixed to the thoracic wall and the pulmonary ligament was divided with the cautery hook. The cyst was separated from adjacent muscular tissue, enucleated, and finally removed in an endobag (Fig 4). Again, the esophageal muscular layer was repaired in a single stitch fashion.



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  		Fig 4. Robotic enucleation of a foregut cyst.

 

   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
All procedures were completed entirely using the da Vinci robotic system. In the four cases of oncologic esophageal dissection the median overall operating time was 173 (160–190) minutes and the median time for the surgeon working at the robotic console (console time) was 147 (135–160) minutes. In the two benign cases the median overall operating time was 121 minutes and the median console time was 94 minutes. The times for each procedure are listed in Table 2. There was no relevant intraoperative blood loss in any of the patients, and no surgical complications occurred. The robotic system itself did not experience any technical failure.


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  		Table 2. Procedural Times and Postoperative Course for Each Patient
 
The postoperative courses were uneventful in 5 patients and chest tubes were removed on postoperative day 2 (2–;3). In patient No. 4 a persistent lymph fistula was clipped thoracoscopically in a redo operation on postoperative day 27. Postoperative hospital stay was 14 (10–42) days in the oncologic group and 7 days in the two benign patients. The prolonged hospital stay of the oncologic patients was due to the laparotomy (abdomino-cervical procedures), and in patient No. 4 additionally was due to the lymph fistula.

Pathology reports revealed three squamous cell carcinomas (patients Nos. 1, 3, and 4), one adenocarcinoma (Barrett‘s carcinoma, patient No. 2), one esophageal leiomyoma (patient No. 5), and one foregut cyst (patient No. 6). Histology confirmed in all 6 patients that the resection margins were free of tumor (R0). The mean number of retrieved mediastinal nodes was 12 (8–19). The staging of the four carcinoma cases are depicted in Table 3.


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  		Table 3. Clinical and Pathologic Staging and Number of Retrieved Lymph Nodes (Oncologic Cases)
 
Patient No. 1 died 12 months postoperatively due to tumor progression. Patient No. 2 required an esophageal stent due to local tumor recurrence 19 months postoperatively. The other two cancer patients (Nos. 3 and 4) as well as the two patients (Nos. 5 and 6) with benign lesions are in complete remission after a mean follow-up of 5 (3–29) months.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
The aim of this study was to examine whether a robot might contribute to esophageal operations in the future. Our small number of robotic-assisted esophageal procedures does not permit statistical analysis. However, at this early stage it is important for the evolving robotic community to stay informed, even on preliminary findings.

With regard to conventional thoracoscopic esophagectomies, various groups have already experienced large series [1, 5, 6]. A benefit has already been demonstrated in terms of patient comfort and early morbidity and mortality [7–10].The question whether this new technique follows the basic oncologic tenets, has not yet been answered completely: Interestingly, Luketich and colleagues [5] describe impaired survival in their stage II patients, as compared with a representative open series of Swanson and colleagues [11]. A possible explanation for this observation might be a limited accuracy of the lymph node dissection. According to Nigro and colleagues [12], the number of retrieved lymph nodes is crucial, especially for T2 tumors which bear an 80% risk of lymph node involvement.

The da Vinci robotic system provides the benefits of minimally invasive approaches without compromising the dexterity, precision, and ability of intuitive maneuvers in open surgical procedures [2]. The limitations of conventional thoracoscopy are overcome, which allows the surgeon to execute more complex tasks in remote areas with precision. The combination of superior visual control and EndoWrist (Surgical Intuitive, Mountain View, CA) maneuverability permitted nearly bloodless thoracoscopic dissection of the esophagus and retrieval of 12 (8–19) mediastinal lymph nodes in our series. This figure does not fully reflect what could have been achieved since the tumor stage was advanced in three of our four patients. We are truly convinced that the da Vinci enables more accurate dissection from the thoracic inlet to the diaphragmatic reflection, as compared with conventional video-assisted thoracoscopic surgery (VATS).

Encouraged by the robot's potential, Horgan and colleagues [13] introduced a transhiatal technique for distal esophageal cancer. He recently reported on excellent early results in his first nine patients [14]. The robot's accuracy permitted oncologic lymph node dissection of the entire lower and middle field. More recently, Kernstine [14, 15] executed a robotic two-stage modified McKeown technique with a three-field lymphadenectomy in 14 patients.

Esophagectomy using a conventional minimally invasive approach is an advanced surgical procedure with a long learning curve. Thus, its routine application is still reserved to a few highly experienced centers [16, 17]. We have observed increasing dexterity after only a few robotic cases and feel that dissection with the da Vinci is safer and easier.

For resection of benign intramural esophageal lesions, the three-dimensional view with enhanced magnification provides a clear distinction between anatomic layers and minimizes the risks of mucosal perforation [18]. The motion scaling system translates large hand movements into precise surgical maneuvers and facilitates safe dissection of delicate anatomic structures. One of our cases included a leiomyoma, which is the most common benign mesenchymal esophageal tumor. It is localized mainly in the mid to distal thirds, and the standard treatment consists of open local extirpation. A minimally invasive procedure is feasible, although difficult to accomplish by conventional VATS [18–21]. The delicate enucleation of the intramural tumor without damaging the mucosal tube and the closure of the myotomy were easily performed with the robot.

The drawbacks of the da Vinci robotic system are evident: high costs, longer operating times (at least at the beginning of the learning curve), and the lack of haptic feedback. The latter bears the risk of damaging tumor tissue or involved lymph nodes, but can easily be compensated by the system's superior vision control.

Thus far, only single case reports exist on robotic esophageal procedures [18, 22–25]. This small series of various esophageal entities treated by robotic-assisted thoracoscopic surgery (RATS) supports the hypothesis that the esophagus is a major organ of interest for robotic surgeons. Robotic procedures will continue to evolve as an important adjunct to complex thoracoscopic procedures. From our experience we believe that the robotic approach has some advantages with regard to oncologic tenets, as compared to VATS. This appraisal remains to be proven in future clinical trials. We will continue to evaluate the efficacy and potential of RATS into the future.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
The authors thank Emeritus Professor Ernst Bodner, MD, for his vision and endeavors, which enabled the acquisition of the da Vinci robot for the Department of Surgery, Innsbruck University Hospital.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Nguyen NT, Roberts P, Follette DM, Rivers R, Wolfe BM. Thoracoscopic and laparoscopic esophagectomy for benign and malignant diseaselessons learned from 46 consecutive procedures. J Am Coll Surg 2003;197:902-913.[Medline]
  2. Schmid T. Robotic surgery Eur Surg 2002;3:155-157.
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  4. Hazey JW, Melvin WS. Robot-assisted general surgery Semin Laparosc Surg 2004;11:107-112.[Medline]
  5. Luketich JD, Alvelo-Rivera M, Buenaventura PO, et al. Minimally invasive esophagectomyoutcomes in 222 patients. Ann Surg 2003;238:486-494.[Medline]
  6. Osugi H, Takemura M, Higashino M, et al. Learning curve of video-assisted thoracoscopic esophagectomy and extensive lymphadenectomy for squamous cell cancer of the thoracic esophagus and results Surg Endosc 2003;17:515-519.[Medline]
  7. Lee RB, Miller JI. Esophagectomy for cancer Surg Clin North Am 1997;77:1169-1196.[Medline]
  8. Fernando HC, Christie NA, Luketich JD. Thoracoscopic and laparoscopic esophagectomy Semin Thorac Cardiovasc Surg 2000;12:195-200.[Medline]
  9. Nguyen NT, Follette DM, Wolfe BM, Schneider PD, Roberts P, Goodnight Jr JE. Comparison of minimally invasive esophagectomy with transthoracic and transhiatal esophagectomy Arch Surg 2000;135:920-925.[Abstract/Free Full Text]
  10. Taguchi S, Osugi H, Higashino M, et al. Comparison of three-field esophagectomy for esophageal cancer incorporating open or thoracoscopic thoracotomy Surg Endosc 2003;17:1445-1450.[Medline]
  11. Swanson SJ, Batirel HF, Bueno R, et al. Transthoracic esophagectomy with radical mediastinal and abdominal lymph node dissection and cervical esophagogastrostomy for esophageal carcinoma Ann Thorac Surg 2001;72:1918-1924.[Abstract/Free Full Text]
  12. Nigro JJ, Hagen JA, DeMeester TR, et al. Prevalence and location of nodal metastases in distal esophageal adenocarcinoma confined to the wallimplications for therapy. J Thorac Cardiovasc Surg 1999;117:16-23.[Abstract/Free Full Text]
  13. Horgan S, Berger RA, Elli EF, Espat NJ. Robotic-assisted minimally invasive transhiatal esophagectomy Am Surg 2003;69:624-626.[Medline]
  14. Kernstine KH. Robotics in thoracic surgery Am J Surg 2004;188:89S-97S.[Medline]
  15. Kernstine KH, DeArmond DT, Karimi M, et al. The robotic two-stage three-field esophagolymphadenectomy J Thorac Cardiovasc Surg 2004;127:1847-1849.[Free Full Text]
  16. Schuchert MJ, Luketich JD, Fernando HC. Complications of minimally invasive esophagectomy Semin Thorac Cardiovasc Surg 2004;16:133-141.[Medline]
  17. Litle VR, Buenaventura PO, Luketich JD. Minimally invasive resection for esophageal cancer Surg Clin North Am 2002;82:711-728.[Medline]
  18. Elli E, Espat NJ, Berger R, Jacobsen G, Knoblock L, Horgan S. Robotic-assisted thoracoscopic resection of esophageal leiomyoma Surg Endosc 2004;18:713-716.[Medline]
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  20. Swanstrom LL, Hansen P. Laparoscopic total esophagectomy Arch Surg 1997;132:943-947.[Abstract/Free Full Text]
  21. Roviaro GC, Maciocco M, Varoli F, Rebuffat C, Vergani C, Scarduelli A. Videothoracoscopic treatment of oesophageal leiomyoma Thorax 1998;53:190-192.[Abstract/Free Full Text]
  22. Shah J, Rockall T, Darzi A. Robot-assisted laparoscopic Heller's cardiomyotomy Surg Laparosc Endosc Percutan Tech 2002;12:30-32.[Medline]
  23. Gould JC, Melvin WS. Telerobotic foregut and esophageal surgery Surg Clin North Am 2003;83:1421-1427.[Medline]
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