Transthoracic Single Port with Peroral Assistance: An Animal Experiment to Assess a Less Invasive Technique for Human Esophageal Atresia Repair

Introduction

The first successful one-stage surgical correction of esophageal atresia (EA) ¹ was described by Haight and Towsley, in 1943. After this report, many other studies succeeded, and posterolateral right extrapleural thoracotomy became the gold standard correction of EA. ¹ In 1999, with advances of technology, knowledge, and surgical skills, the first thoracoscopic repair of EA without tracheoesophageal fistula (TEF) was performed at the International Pediatric Surgical Endoscopy meeting, in Berlin. ² One year later, Rothenberg ³ performed the first thoracoscopic correction of EA with TEF. Since then, many other authors have adopted the surgical correction of EA by the thoracoscopic approach, and it is already the gold standard in many centers.^4,5 After laparoscopy and thoracoscopy, a new paradigm shift was beginning to emerge: natural orifice translumenal endoscopic surgery (NOTES). Several complex surgeries like cholecystectomy ⁶ or nephrectomy ⁷ have been described by our group in experimental porcine models. Roughly 10 years later, NOTES could be the next evolution step to correct this anomaly.

The transition of NOTES to humans has been limited by the inability to safely close the viscera wall. ⁸ Increasing numbers of reports are describing the use of hybrid NOTES or laparoscopy assisted by NOTES in humans. ⁹ Regarding pediatric surgery, the peroral route to thoracic procedures seems to be a very attractive approach. Our group previously showed in an adult porcine model that an esophagoesophageal anastomosis could be performed by hybrid NOTES using a peroral and thoracoscopic approach. ¹⁰ However, this study was designed to simulate a surgery in human adults and not to explore the feasibility of performing an esophagoesophageal anastomosis in a newborn with EA. In the present work, we tested the possibility of performing hybrid thoracoscopic and peroral NOTES in a rabbit model to simulate the human newborn.

Materials and Methods

Ergonomics

The layout of the room is represented in Figure 1. The animal was positioned at one end of the surgical table in the prone position. The thoracoscopic operator stood at one side of the operating table. The anesthetist and the peroral operator were positioned each one at one end side of the table. Monitors were positioned in front of each operator.

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FIG. 1.

(A and B) Layout of the operating room. Monitor 1 was for the peroral operator; Monitor 2 was for the thoracoscopic operator.

Results

Surgical procedure

The surgical procedure is summarized step-by-step in Figure 2 and Supplementary Video (Supplementary Data are available online at www.liebertpub.com/lap). The lower end of the right scapula revealed an ideal access point to introduce the trocar. The location of the transthoracic port associated with the animal in the prone position and CO₂ insufflation permitted us to obtain a good visualization of the esophagus without the need of other instruments or techniques. For the first three stitches, the peroral dissector was helpful in two aspects: (1) to put the distal esophageal end close to the proximal esophageal end and (2) to include all the layers of the esophageal wall in the sutures. The first stitch, in particular, was the most difficult to perform because of the lack of stability of the esophagus (Fig. 2F). A nasogastric tube was inserted after the first two to three stitches, turning the anastomosis easier and faster to perform (Fig. 2I and J). However, the insertion of the nasogastric tube was again a challenging step, requiring an optimal coordination between the thoracoscopic and peroral operators. The anastomosis procedure was completed dominantly by the transthoracic needle holder helped by peroral rotation of the esophagus. Extracorporeal knots were performed with a 3-mm knot-pusher inserted through the thoracoscope (Fig. 2G). This technique permitted us to obtain an optimal view of the knotting process, easily controlling the pressure applied to each knot, and to decrease operative time. The remaining wire was cut transthoracically without any difficulty. Pearls and pitfalls of the protocol identified by the group are summarized in Table 1. The mean time to perform the surgical procedure in the eight rabbits—including dissection, esophagotomy, and anastomosis—was 85 minutes (range, 62–137 minutes). At the end of the procedure, the final aspect of the anastomosis was properly checked (Fig. 2L). Additional stitches were performed as much as necessary. The manipulation of the instruments needs to be cautious because of the proximity with the intercostal vascular structures. After sacrificing the animals, we performed a segmental esophagectomy to study the anastomosis closely. We verified a complete anastomosis in all cases, with the incorporation of the mucosa in all stitches (Fig. 3).

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FIG. 2.

Major steps executed during the protocol. Dissection was performed by the transthoracic operator, whereas the peroral operator accessed the esophageal lumen with a flexible endoscope, permitting him to take lateral movements and (A) up and (B) down movements. Complete esophagotomy was achieved by a peroral scissor (C) helped by a transthoracic grasper, which held the distal esophageal portion in the end of the section (D). After the peroral operator grasped the distal section of the esophagus (E), the transthoracic operator started the anastomosis with the first stitch (F) and ended the extracorporeal knot with a knot-pusher (G). (H) The excess wire was cut by a transthoracic scissors. A nasogastric tube was introduced through the mouth to achieve the sectioned esophagus. A transthoracic forceps hold the nasogastric tube (I) and manipulated it to the intraluminal space of the distal esophageal portion (J). The anastomosis process was continued (K) until it was completed (L).

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FIG. 3.

(A) External and (B) internal views of the esophageal anastomosis.

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Table 1.

Pearls and Pitfalls of the Protocol Identified by This Study

Pearls	Transthoracic trocar at the lower end of the right scapula
	Coordination between operators
	Peroral use of conventional 3-mm instruments
	Esophageal dissection helped by peroral endoscope
Pitfalls	First stitch
	Introduction of the nasogastric tube
	Intercostal vessels' proximity to surgical maneuvers

Discussion

Thoracoscopic repair of EA includes obvious advantages like better visualization of the surgical field, less postoperative pain, better cosmesis, and fewer musculoskeletal sequelae. ⁴ Some studies, including one multicenter analysis, suggested that thoracoscopic correction of EA with TEF can be safely performed by experienced surgeons and had comparable outcomes with thoracotomy. ⁴ Currently, this surgical technique is becoming the gold standard for EA correction in several centers.^4,5 However, a new era is emerging, and three or four transthoracic ports might be too much for a 21st century minimally invasive procedure. Although the first NOTES approach was a transvaginal procedure described by Decker and Cherry ¹¹ in 1944, the enthusiasm about this technique only started six decades later. Starting in 2004 with a human transgastric appendectomy performed by Reddy and Rao, ¹² NOTES brought a new set of opportunities. All possible approaches were explored: transgastric, ¹³ transvesical, ¹⁴ transcolonic, ¹⁵ and transesophageal ¹⁶ accesses. The potential advantages of NOTES over laparoscopy and thoracoscopy might include (1) reduction of general anesthesia use, (2) decrease in hospitalization time and postoperative pain, (3) prevention of skin incision complications (wound infection and hernias), (4) increment of outpatient regimen, (5) faster return of bowel function, (6) better cosmetic outcomes, and (7) increase in overall patient satisfaction. ⁹ Besides all these advantages, pure NOTES still has some limitations in the present.

A pure peroral approach might have some disadvantages like the extreme difficulty of creating triangulation, the precarious view of the work field, and, concomitantly, the increased risk of leakage resulting from an incomplete esophageal closure. Hybrid NOTES represents the best of the two fields—thoracoscopy and NOTES—because it allows a reduction of the number of transthoracic ports and overrides some of the limitations of pure NOTES. Using a transthoracic access combined with a peroral route, triangulation and countertraction can be achieved. Moreover, the excellent thoracoscopic visualization of the work field is profitable, and the thoracic incision can be used to place a drainage tube postoperatively.

EA can be an excellent congenital malformation candidate for peroral hybrid NOTES. At present, the upper esophageal pouch is only used for the introduction of the nasogastric tube, but in our opinion the upper esophageal pouch could potentially be a route for the thoracic cavity. Rolanda et al. ¹⁰ described a peroral esophageal segmentectomy and an anastomosis with a single 12-mm transthoracic trocar in an adult porcine model. The authors demonstrated the reliability of performing this technique in a large animal model. In the present study, we demonstrated the feasibility of combining the peroral and transthoracic routes to perform an esophagoesophageal anastomosis in rabbits. This animal model perfectly simulates the human newborn and is a well-established model to train pediatric surgeons in neonatal minimally invasive procedures. ¹⁷ The anatomic constitution of the rabbit simulates the newborn size, allowing the use of 3-mm instruments in a very limited space, as happens in human newborns. In this work, we explored the prone position of the animal to amplify our field of work. The prone position is being explored in patients in order to easily manipulate the esophagus. ¹⁸ This approach was previously explored in our department by Rolanda et al., ¹⁰ stating the advantage to easily access the mediastinum with the help of the gravity, to use lower CO₂ pressures, and to decrease the time of the procedure. In thoracoscopic repair of EA, different centers are using the partially prone position of the patient at 30–45°,^4,19 and a fourth port is sometimes applied to retract the lungs.^4,19 A completely prone position may be more helpful than a partial one.

The great innovation of this study is the possibility of performing an EA correction with just one transthoracic port, in contrast to the classic thoracoscopy, which uses three or four trocars.^4,19 The use of a 10-mm trocar might be considered more invasive than three 5-mm trocars but still is a single incision. This trocar size was used to introduce the camera with the working channel. We might anticipate that the miniaturization of this kind of telescope will allow the use of smaller trocars in the future. The peroral flexible endoscope allowed us to achieve the esophageal lumen without difficulties and to easily mobilize it. The three-dimensional movements of the flexible endoscope allowed us to surpass the inconvenience of using just one transthoracic trocar to perform esophageal dissection. In a human newborn with EA, we might anticipate that this peroral approach could facilitate transthoracic dissection of the upper esophageal pouch. Additionally, cutting the proximal pouch with peroral scissors could be of great help in human newborns. Again, the possibility of grasping the lower pouch using this access can be useful for the first esophageal stitch. In this study, the mean operative time was 85 minutes. The average surgical time for thoracoscopic repair of EA with TEF is 130 minutes, as was reported by a multi-institutional study. ⁴ In the present study we did not perform dissection and ligation of the distal TEF, but we could anticipate that using a peroral gasper combined by a transthoracic dissector, it would be possible to perform this step. We demonstrated the feasibility of an esophageal anastomosis using a single transthoracic trocar with a similar time interval as using three or four transthoracic trocars. This surgical technique, combining peroral and transthoracic approaches, demands a well-synchronized performance between the surgeon and the first assistant to guarantee optimal results. Whereas in thoracoscopy or laparoscopy the same surgeon performs all the movements with both hands, in hybrid NOTES it is necessary to have an operator in each port. A good coordination between them is essential, permitting them to obtain synchronized movements as if the hands of each operator belonged to the same surgeon. Our team has already proved in other procedures, namely, cholecystectomy ⁶ and nephrectomy, ⁷ that the coordination between two operators is demanding but can be achieved with training.

We identified some limitations in the present study: (1) tracheostomy to ventilate rabbits and (2) lack of a true EA with TEF, the most common type of EA. During our learning curve, we abandoned the endotracheal intubation and started to perform tracheostomy to ventilate the animal. An endotracheal tube would make hard to introduce other instrumentation through the peroral route. To overcome this problem in humans, we suggest a nasotracheal tube, instead of using an orotracheal tube. The present work was a non-survival study using normal rabbits without EA. This fact did not allow us to explore the feasibility and safety of performing some technical procedures like TEF ligation. It might be important to simulate a TEF in an animal model or, ideally, translate this study to a deceased newborn with EA and distal TEF. Nevertheless, we believe in the viability of this approach in a human newborn because ligation of TEF is performed by many groups with a simple clip, ⁴ a maneuver that could be easily performed using transthoracic and peroral routes. This approach would imply a change in the surgical human routine—the first step would be the dissection and opening of the upper esophageal pouch to establish the peroral trocar before performing distal esophageal dissection and TEF ligation.

In conclusion, this is a proof-of-principle study that demonstrates the feasibility of performing an esophageal anastomosis combining a single transthoracic port with a peroral port in a rabbit model that simulates the human newborn. This study provides several important insights into the translation of hybrid NOTES repair for human newborns with EA. We anticipate that in the near future, the peroral route will replace at least one, if not two, transthoracic trocars.