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Evaluation of the combined laparoscopic and mediastinoscopic esophagectomy technique
V. V. Bintintan, A. Mehrabi, H. Fonouni, M. Golriz, J. Köninger, A. Kashfi, Gh. Funariu, M.W. Buechler, C. Ciuce, C.N. Gutt (Chirurgia, 104 (2): 187-194)
Introduction
Laparoscopic transhiatal esophagectomy was proven to be feasible more than a decade ago (1, 2). Compared with the conventional technique advocated by Orringer (3) it offers visual control on the operative field and has the potential to allow sampling of mediastinal lymph nodes. However, these advantages were shadowed by the difficulty of the procedure and the long and steep learning curve (4). Therefore, laparos-copic esophageal resection was frequently abandoned, often after the first attempts, in favor of the combined laparoscopic and thoracoscopic approach (4, 5).
The most difficult phase during laparoscopic esophagectomy is dissection in the upper mediastinum due to the restricted working space and limitations imposed by the narrow hiatus. However, this area is accessible to mediastinoscopy, a surgical procedure used mainly as a diagnostic or surgical staging tool for upper mediastinal masses. With a combined laparoscopic and mediastinoscopic technique the entire length of the esophagus can be accessed easier for a safe and complete totally endoscopic esophageal resection without trans-thoracic access. Although the perspective is promising, the experience published in the literature with this approach is limited (6, 7).
Equipped with long and articulated instruments and elaborated optical devices, robotic surgical systems allow a wide range of complex movements to be performed easily and with improved accuracy even in tiny and remote areas. The technique of robotic-assisted transhiatal esophagectomy has been recently reported in the literature but the experience accumulated in this field is still limited (8, 9).
The aim of the present experimental study, conducted in a porcine animal model, was to study the feasibility,
advantages and limitations of the combined laparoscopic and mediastinoscopic esophagectomy technique, to evaluate the new perspective that the transhiatal robotic-assisted approach can bring to the procedure and to compare these two minimally-invasive techniques with the open approach in terms of safety, reproducibility, ease of performance, presence of intraoperative incidents and satisfaction offered to the operative team.

Materials and methods
Study design
Transhiatal esophagectomy was performed on German Landrace pigs (n = 21) in deep anesthesia. Animals were divided into three different groups:
- group A consisting of 9 pigs operated on using a combined laparoscopic and mediastinoscopic technique;
- group B in which 4 pigs were operated with a robotic-assisted transhiatal approach. These operations were performed in a rented surgical facility which provided the special equipment. Due to financial considerations, experiments were stopped once the procedure was proven to be feasible and valid conclusions could be drawn. Therefore the number of operations was lower compared with the other two groups.
- group C in which 8 pigs underwent a conventional “open” transhiatal esophagectomy procedure.
Anesthesia protocol
After premedication with azaperon (1-2 mg/kg i.m.) and midazolam (0.5-0.7 mg/kg i.m.), narcosis was induced with intravenous midazolam (1-1.5 mg/kg) and ketamine (10 mg/kg). Animals were intubated and anaesthesia was maintained using an isoflurane enriched O2/air mixture. Fentanyl (500 g/h i.v.) was used for analgesia and pancuronium (0.25 mg/kg/h) for muscle relaxation. The common carotid artery and internal jugular vein were catheterized and connected to membranous pressure transducers for continuous measurement of mean arterial pressure (MAP) and central venous pressure (CVP), respectively. Ringer lactate solution was infused continuously during the operation at a rate of 20 ml/kg/h. Heart rate and rhythm were continuously monitored by a surface electrocardiogram. Temperature was monitored with a rectal thermometer and maintained at 37°C throughout the operation using a heated blanket placed under the animals. Blood samples were withdrawn repeatedly during the experiment and analyzed in a blood gas analyzer (ABL50; Radiometer, Copenhagen, Denmark). Variations in O2 and CO2 blood gas pressure and saturation directed the fine tuning of ventilatory parameters. At the end of the experiment, while animals were still in deep anesthesia, a central venous injection of 80 mmol potassium chloride was administered to produce cardiac arrest and death.
Animal care
Approval for the experimental procedure was obtained from the German Committee on Animal Care, Regierungspräsidium Karlsruhe. During the experiments, all animals received care in compliance with the European Regulations for Animal Experiments (10) and the United States National Research Council’s criteria as outlined in "Guide for the Care and Use of Laboratory Animals" prepared by the National Institution of Health (NIH publication no. 86-23, revised 1985).
Operative technique
The laparoscopic and mediastinoscopic operations were performed using a Karl Storz minimally invasive surgical unit (Karl-Storz Co., Tuttlingen, Germany) with a 30º scope and standard instrumentation. The robotic-assisted procedures were done with the three-arm da VinciTM robotic surgical system (Intuitive Surgical® Inc., Mountain View, CA). All experiments were performed by two surgeons experienced in laparoscopic and robotic-assisted surgical techniques.
Combined laparoscopic and mediastinoscopic transhiatal esophagectomy
Laparoscopic transhiatal dissection
Four trocars were used, a 10-mm optic trocar placed in an “umbilical” position, two 5-mm trocars for the working instruments (grasper, hook cautery, Ligasure) inserted in the mid-clavicular line, two fingerbreadths under the costal margin and an additional 10-mm trocar introduced in the left flank for manipulation of the stomach or esophagus. Retraction of the liver was done with a Nathanson retractor placed in a subxyphoidal position (Fig. 1a). Dissection started at the lesser omentum and progressed through the pars flacida towards the esophageal hiatus. After division of the phrenoesophageal ligament and identification of the abdominal esophagus, the latter was surrounded with a tape to aid for further manipulation. The hiatus was dissected completely and enlarged by a 2 cm antero-superior cut and partial myomectomy of the right and left diaphragmatic pillars. Whenever necessary, the phrenic vein crossing above the superior pole of the hiatus was clipped and divided. The laparoscope and working instruments were advanced together through the enlarged hiatus to continue with mediastinal dissection. The esophageal hiatus was maintained open by the shafts of the dissecting laparos-copic instruments while pneumomediastinum and further non-traumatic manipulation of the dissected segment of the esophagus provided exposure of the operative field. The attachments of the esophagus to aorta, pleurae, pericardium, hilus of the lungs and trachea were divided under visual control, esophageal arteries being identified and coagulated individually. Attempts were made to identify periesophageal and infracarinal lymph nodes and include them in the resection specimen (Fig. 2a). Upward mediastinal dissection advanced under view as much as possible until the length of the instruments became insufficient or their manipulation into the narrow space was no longer considered safe. In every experiment the aim was to dissect the esophagus at least up to the level of the tracheal bifurcation.
Figure 1A
Figure 1B

Mediastinoscopic dissection
The left side of the neck and chest were prepared and draped. Through a standard longitudinal left cervical incision the esophagus was identified posterior to the trachea and its loose attachments were divided with both sharp and blunt finger dissection to create a virtual periesophageal working space. Two 5-mm trocars were inserted 2 cm lateral and caudal from the upper and lower poles of the cervical incision under visual and tactile control. After placement of the 10-mm optic trocar in its superior pole, the incision was closed with a running 3.0 polypropylene suture and CO2 was insufflated into the virtual chamber at a pressure of 5-mmHg (Fig. 1b). Dissection of the esophagus from the surrounding structures including membranous trachea, pleura, arch of the azygos vein and the longitudinal vertebral ligament was performed using conventional minimally-invasive techniques until the upper limit of the laparoscopic transhiatal dissection was joined (Fig. 2b).
Robotic-assisted transhiatal esophagectomy
The technique of robotic-assisted transhiatal esophagectomy was similar with the laparoscopic phase of the combined laparoscopic and mediastinoscopic approach. Trocars were placed in an identical position with the exception of a fan-shaped liver retractor which was introduced in the right flank through a 10-mm trocar. Transhiatal dissection progressed cranially as much as possible, well beyond the carina (Fig. 2c). Through a standard left cervical incision the cervical esophagus was identified and dissected bluntly until it was freed completely from the surrounding attachments.

Figure 2A
Figure 2B
Figure 2C

Open transhiatal total esophagectomy
Through a midline laparotomy and standard left cervical incision dissection was done according to the conventional technique described by Orringer (3).
Intraoperative Assessments
Operative incidents, injuries of mediastinal structures and variations of cardiopulmonary parameters during intra-thoracic dissection were recorded during the procedure along with total and phase-specific operative time and the amount of operative blood loss. At the end of the operation a right thoracotomy was performed to assess the extent of lesions or to identify additional injuries that were not recognized intraoperatively. The surgeon was also asked to fill in an evaluation chart on a scale from 1 to 10 (10 representing the highest score) which evaluates a number of subjective parameters: difficulty of the procedure, accuracy of dissection, the feeling of safety related to the surgical procedure and satisfaction for the specific technique.

Results
Experiments from group A proved that the technique is feasible and reproducible. The level of tracheal bifurcation was reached in all cases during both laparoscopic and mediastinoscopic phases of the operation. Progressing in controlled steps under constant visual control, dissection was highly accurate. Adjoining anatomical structures such as pleura, aorta, inferior pulmonary veins, posterior pericardium, tracheal bifurcation, the arch of azygos vein or membraneous trachea were identified intraoperatively while individual coagulation of periesophageal vessels minimized blood loss. However, the procedure was also technically demanding, especially when transhiatal dissection progressed above the level of tracheal bifurcation. It was in this phase of the operation, where laparoscopy has reached its limits, that mediastinoscopy brought its contribution to the success of the operation.
Intraoperative incidents included liver and spleen injuries caused by the liver retractor or by instruments that were advanced through the hiatus without visual control in two and one cases, respectively. In another case there was light injury of the right lung parenchyma (depth <1cm) caused by the hook cautery. The bleeding either stopped spontaneously or was managed by electrocoagulation. The inferior diaphragmatic vein was injured in one case during enlargement of the hiatus; clips were used to stop the bleeding. Minor hemorrhage occurred in three cases during mediastinoscopy and was arrested using monopolar coagulation. Pleural injuries, either on the right or left side, were encountered at least once in each of all nine laparoscopic dissections and in five additional cases during mediastino-scopy. In six laparoscopic and two mediastinoscopic procedures tension pneumothorax was accompanied by pulmonary (hypercapnia, hypoxia and respiratory acidosis) and cardiovascular disturbances (tachycardia and arterial hypotension). When these complications occurred the operation was stopped, CO2 was released from the abdomen and ventilatory parameters were adjusted: increase of oxygen concentration (FiO2) and minute frequency and use of positive end-expiratory pressure (PEEP). Cardiopulmonary parameters returned to normal in a variable amount of time ranging from 5-15 min and the operation was resumed.
The robotic-assisted operations from group B were also successful. Dissection proceeded smoothly beyond the tracheal bifurcation in all cases and therefore mediastinoscopy was no longer necessary. Intraoperative incidents were minor. In one case malfunction of the robotic cautery required replacement of the device while in another experiment minor liver injury during robotic set-up was managed with electrocoagulation. Pleural injuries were present in three cases, in two of them being associated with the same pattern of cardiopulmonary disturbances described in group A.
Operations in group C were performed easy and quick. However the technique described by Orringer (3) could not be reproduced entirely due to the narrow esophageal hiatus which, even enlarged to the limit of opening of the pericardial cavity, could not accommodate more than three fingers of the operating hand. Therefore the thoracic esophagus was pulled down into the abdomen where a large part of its flimsy attachments were divided. Dissection of the segment which still remained into the thorax was done after finalization of the cervical part of the operation by a combination of stripping and blunt dissection with the three operating fingers. In one case the mass effect caused by the dissecting hand determined anterior displacement and mechanical stimulation of the heart with consequent reduction in blood inflow and arrhythmia leading to clinically relevant hypotension and tachycardia. Other intraoperative incidents recorded were hypoxia, hypercapnia and bradycardia during mediastinal dissection in one case and a minor bleeding episode from a spleen laceration in another experiment.
The final evaluation performed at the end of the procedure through a right thoracotomy did not identify any additional injuries from the ones already recorded intra-operatively in groups A and B while in group C it revealed pleural injuries in all eight cases (Table 1). The subjective evaluation filled-in by the surgeon at the end of the operation has shown that the minimally-invasive procedures were considered to be significantly more difficult compared with the open approach. At the same time, they were also seen to be safer and offered more satisfaction to the operative team due to the constant visual control over the operative field (Table 2).

Discussions
The transhiatal minimally-invasive approach to esophageal resection
Surgical treatment for esophageal diseases is still accompanied by particularly high rates of morbidity and mortality (11, 12, 13). With an overall incidence of 20 to 30%, pulmonary complications are the most frequent cause of morbidity after open transthoracic esophagectomy and represent a considerable threat to the postoperative outcome of the patient (14, 15). A technique that causes minimal surgical stress and limited disturbance of respiratory function is therefore essential to provide a quick and uneventful recovery in patients with esophageal cancer, a disease with a grim overall prognosis, discovered frequently at an advanced stage and characterized by limited chance for long-term survival. The thoracoscopic approach to esophagectomy (16, 17) reduces operative trauma and fulfils the prerequisites of oncologic sound surgery but implies long periods of single-lung ventilation and has not managed to lower significantly the incidence of pulmonary complications (18, 19). The conventional transhiatal technique advocated by Orringer (3) maintains intraoperative bilateral lung ventilation and avoids the need for thoracotomy. It is now the preferred approach in high-risk patients. This procedure, however, implies blind dissection in the mediastinum and therefore has a high risk of intraoperative incidents. Furthermore, mediastinal lymphadenectomy above the level of pulmonary veins is impossible with this technique (20, 21). The laparoscopic transhiatal esophagectomy approach provides visual control on the operative field and avoids some of the limitations of the open procedure. It was proven to be feasible (1, 2) but did not gain wide acceptance due to limitations of working thorough the narrow esophageal hiatus, impaired dissection of the middle and upper esophagus, short length of laparoscopic instrumentation and a steep learning curve (4, 5).
Mediastinoscopy for dissection of the esophagus
By accessing the upper mediastinum, an area where laparoscopy has showed its limitations, mediastinoscopy may renew the interest in a technique that achieves a totally endos-copic mobilization of the esophagus without thoracic access. The role of cervical mediastinoscopy in esophageal surgery is not yet fully established. Following the development of endos-copic video equipment, Buess proposed the technique of endoscopic microsurgical dissection (EMDOE) (22) to dissect the upper esophagus in patients subjected to transhiatal eso-phagectomy. The feasibility and efficacy of the technique were demonstrated in experimental and clinical studies (23, 24) but, despite the initial success, it proved to be technically difficult (23) and failed to become a standard in esophageal surgery.
Combined laparoscopic and mediastinoscopic esophagectomy
The technique used for mediastinoscopy in the present experi-ments was described solely by Ikeda in few patients in which it was added either to a laparoscopic or thoracoscopic approach (6, 25). We have preferred this technical variant because it is simple, does not require additional special instrumentation and allows easy creation and maintenance of a proper working space and an acceptable freedom of movement for the working instruments. Our experience with the technique was positive. It offered good conditions for an accurate and safe dissection of the upper esophagus. The procedure uses principles and techniques common to the conventional laparoscopic techniques and therefore the learning curve was also less steep. Furthermore, it offered the possibility to visualize lymph nodes located in the upper mediastinum, an important feature considering that the lymph nodes along the recurrent nerve are the most frequently involved by metastasis in patients with thoracic esophageal cancer (26) and also seem to act as sentinel nodes for the cervical stations (27).
The laparoscopic stage of the operation achieved a highly accurate and almost bloodless dissection up to the level of tracheal bifurcation. However, the operation proved to be technically demanding and had its own risks. The first major difficulty was to pass the laparoscope and working instruments through the narrow and deeply situated hiatus. The close vicinity of the pleural and pericardial spaces prevented wide antero-superior enlargement of the hiatus, a partial resection of the muscular diaphragmatic pillars being necessary to gain additional space. The thoracic esophagus below the pulmonary veins was quite accessible for dissection and the corresponding periaortic tissue, including the lymph nodes, colud easily be included in the resection specimen. The infracarinal lymph nodes were also visible and available for sampling. However, as dissection progressed upwards, so did the difficulties. Orientation in the rather restricted mediastinal space and manipulation of the esophagus necessary to expose properly the dissecting plane became less facile in the vicinity of carina. Above this level, movements of the working instruments were severely restricted by the narrow hiatus and the laparoscopic approach had to be replaced by mediastinoscopy.
The side-effects of tension pneumothorax accompanying pleural injuries was the only significant intraoperative complication in group A. The susceptibility of pigs to tension pneumothorax was recognized in previous studies and could be caused by the presence of a single pleural space and therefore an increased area available for CO2 absorption or the side-effects of increased intrapleural pressure including restriction of pulmonary movements and reduced venous return (28, 29). Moreover, this complication seems to be specific for the experimental setting. In a study of 25 patients operated with laparoscopic esophagectomy in whom pleura on both sides of the esophagus was included in the resection specimen there were no significant intraoperative complications (30) while a further study about the anaesthesiological hazards during laparoscopic esophagectomy has drawn the conclusion that the technique is safe and carries no increased risk compared to the conventional approach (31).
In summary, a combination of laparoscopic and mediastinoscopic techniques achieved accurate dissection of the entire esophagus offering constant view on the operative field, improved hemostasis, possibility of lymph node sampling and reduced operative trauma. This may be one of the least stressful approaches to esophageal resection. The difficulties encountered at the beginning decline considerably as experience is accumulated and operative steps become more familiar. This technique may emerge as a feasible alternative to the open approach, being probably best suited to patients with high operative risks or cases with metastases in the periesophageal lymph nodes when intraoperative sampling may improve staging. It is however a difficult procedure which should be reserved for centers with broad expertise in minimally-invasive and esophageal surgery.
Robotic-assisted transhiatal esophagectomy
The robotic approach retained all the advantages of the laparoscopic procedure to which it added enhanced technical possibilities. Articulated actuator instruments, three-dimensional view, comfortable position at the console and stable camera platform were all features that simplified the intra-thoracic stage of the operation and provided a more relaxed procedure with a shorter learning curve. Articulated robotic instruments, longer than the laparoscopic counterparts, offered extended maneuverability in remote areas and less dependability on the size of the esophageal hiatus. Therefore, robotic-assisted dissection advanced well beyond the tracheal bifurcation without a major increase in the difficulty and was joined by the standard cervical dissection. In summary, the technique of robotic-assisted transhiatal esophagectomy brought significant advantages to the combined laparoscopic and mediastinoscopic procedure that may justify the significant increase in costs. In the future, this procedure may become the minimally-invasive alternative to the open transhiatal approach, initial clinical experience being already published in the literature (8, 9).
Conventional transhiatal esophagectomy
Operations in group C could not reproduce exactly the clinical situation because the narrow hiatus enlarged to the limit of the pericardial cavity could not accommodate the operating hand. Dissection in these cases was facilitated by presence of poorly vascularized loose attachments of the esophagus to surrounding structures which could be ruptured easily without causing major hemorrhage and allowed significant elongation of the esophagus towards the abdomen, simplifying significantly the mediastinal stage of the operation. Therefore, operative time was shorter and intraoperative incidents occured even less frequently than in groups A and B. Although this data suggest not only that the conventional approach retained its place as the standard procedure for transhiatal esophagectomy but also that it is superior to its minimally-invasive counterparts it is biased by the differences between the animal model and the clinical situation. The study from van den Broek et al. (30) sustains this conclusion by finding a significant difference of blood loss and stay in the intensive care unit in favor of the laparoscopic group in a case-controlled study of 25 patients operated with a laparoscopic approach compared with a historical group in whom a conventional open transhiatal procedure was used. Moreover, the major drawback of the open approach remains the lack of visual control over the mediastinal operative field, the main reason why this technique offered the least satisfaction to the operative team.
In conclusion, the open approach remains the standard in transhiatal esophageal surgery to which other technical variants should be compared. The combined laparoscopic and mediastinoscopic esophagectomy technique is feasible and can be safely performed by teams with experience in minimally-invasive surgery. It offers significant advantages over the open approach but is also more technically difficult. The robotic-assisted approach is an emerging viable alternative whose major disadvantages at the moment are the high costs and limited availability of the robotic system. Further studies are required to establish whether the advantages of minimally-invasive approach compensate for increased technical difficulty and prolonged operative time.

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