Feasibility of endoscopic transumbilical thoracic sympathectomy in a porcine model

Abstract

OBJECTIVES

Thoracoscopic sympathectomy is an effective treatment for palmar hyperhidrosis. Current methods are associated with risks of chronic neuropathic pain and a visible chest scar. We developed a novel surgical technique for the performance of sympathectomy by embryonic natural orifice transumbilical endoscopic surgery with a flexible endoscope in a porcine model.

METHODS

Transumbilical flexible endoscopic thoracic sympathectomies were performed in seven farm pigs (three acute and four 4-week survivals). Under general anaesthesia, animals were intubated and mechanically ventilated with a dual lumen endotracheal tube through tracheostomy. A newly developed long transabdominal trocar was placed through the umbilicus. After insertion of a gastroscope through this trocar, a small incision was created on both sides of the diaphragm by a needle-knife. Then the gastroscope was inserted into the thoracic cavity, and the sympathetic chain was identified at the desired thoracic level and ablated. Operation time, safety and feasibility were recorded in all animals.

RESULTS

The transumbilical thoracic sympathectomies were successfully completed in all pigs with a mean operation time of 66.7 ± 9.4 min. Intraoperative bleeding occurred in one pig during the electrosurgical incision of diaphragm tissue, which was successfully controlled by hot biopsy forceps. No other acute intraoperative complications were observed in any cases. In the acute group, the length of the diaphragm incision ranged from 4 to 5 mm in three pigs. In the survival group, the animals recovered promptly from surgery. In three pigs, a small pneumothorax was found in the postoperative chest X-ray, but all of them were completely resolved with conservative treatment. Autopsy showed all bilateral T3 sympathetic chains were successfully ablated and no evidence of vital structure injury or diaphragmatic hernia.

CONCLUSIONS

Transumbilical flexible endoscopic thoracic sympathectomy is technically feasible, simple and safe in a porcine model. This technique can be used as a novel experimental platform for studies of natural orifice transluminal endoscopic surgery (NOTES) for intrathoracic surgery.

INTRODUCTION

Primary hyperhidrosis (PH), which is sweating in excess of that required for normal thermoregulation, is a condition that usually begins in either childhood or adolescence. The sites most commonly affected are the palms, soles and axillae. Severe PH may, in some cases, cause extreme embarrassment or discomfort and can result in significant social disability. PH treatment varies, including topical medications, iontophoresis, botulinum toxin injections, systemic medications and surgery [1]. However, non-operative management has very limited success and is of short duration, if effective at all. Thoracoscopic sympathetic ganglion resection via one to two incisions on the left and right chest is the only effective and sustainable surgical method for the treatment of palmar hyperhidrosis [2–4]. Needlescopic video-assisted thoracic sympathectomy generally requires two to three small ports on each side of the chest. And the procedures can also be performed through a single 10-mm port on each side of the chest with a 5-mm thoracoscope. However, chronic postoperative problems including chronic pain, numbness and dysaesthesia are present in 31.4% of patients [5]. In order to avoid these disadvantages, Turner et al. [6] conducted an animal study using the technique of natural orifice transluminal endoscopic surgery (NOTES) to perform endoscopic thoracic sympathetic (ETS) trunk resection via the oesophagus. NOTES is an exciting area of surgical development, which accesses the peritoneal or thoracic spaces through internal, transvisceral incisions instead of transabdominal or chest incisions. The novel procedure has the potential benefits of decreasing postoperative pain and wound complications, improving cosmesis, and decreasing the physiological and immune response to surgery [7]. However, several key obstacles currently impede its widespread adoption for clinical application. Many procedures have been tested in animal models, but very few have confirmed their safety and feasibility in humans [8–10].

An alternative and competing technology to NOTES is embryonic natural orifice transumbilical endoscopic surgery (E-NOTES), which is performed by inserting surgical instruments via the umbilicus, the ‘natural orifice’ of the embryonic period. E-NOTES has emerged as an attempt to further enhance cosmetic benefits and reduce the morbidity of minimally invasive surgery, is much simpler and technically easier and has similar cosmetic results, but shorter complete recovery than NOTES [11, 12]. E-NOTES has managed to fill the present void left by the lack of applicability of NOTES in the immediate future [12].

In this article, we report our initial experience with E-NOTES for thoracic sympathectomy in a pig model with a detailed description of the technique.

MATERIALS AND METHODS

Experimental animal model

This research protocol was approved by the Animal Experiment Ethics Committee of Fujian Medical University. Seven large pigs with a mean weight of 42.8 ± 1.2 kg were used in this study. Each pig was fasted for 24 h before surgery without refraining from water intake. A premedication by intramuscular injection comprising 7 ml ketamine and 3 ml azaperone was administered 1 h before surgery. Induction of anaesthesia was performed using pentobarbital (20 mg/kg). In semi-Fowler's position, the pigs were intubated and mechanically ventilated with a dual lumen endotracheal tube through tracheostomy. Pentobarbital sodium was used for maintenance of anaesthesia. Monitoring included central temperature, electrocardiography, arterial blood pressure, SpO₂, airway pressures and ETCO₂ every 5 min. Unilateral ventilation was realized by obstructing left and right tracheal separately.

Surgical procedure

After routine abdominal shaving and iodophor sterilization, a 5-mm curved incision was made within the umbilicus. A newly developed long trocar (equipment designed by the authors: 50 cm length, 5 mm internal diameter and 0.5 mm wall thickness) was placed through the umbilicus incision. Pneumoperitoneum was established by insufflation of compressed CO₂ via the trocar at 8–10 mmHg. After placement of the endoscope (GIF-XP260N: outer diameter 5.0 mm; instrumental channel diameter 2.0 mm; Olympus Medical Systems, Tokyo, Japan), the absence of intra-abdominal adhesion was confirmed visually, followed by bilateral T3 sympathectomy procedures as described below.

Under right-lung unilateral ventilation, a needle-knife (Alton Medical Equipment Co., Ltd, Shanghai, China) was used to make a 5-mm incision through the left diaphragm (Fig. 1). The endoscope was introduced into the left thoracic cavity via the diaphragm incision. The animal was turned to a right lateral decubitus position or kept prone for improved visualization of the anatomy posterior to the lung. The endoscope was advanced to identify the second, third and fourth intercostal spaces. Once the sympathetic chain was exposed (Fig. 2), hot biopsy forceps (Alton Medical Equipment Co., Ltd, Shanghai, China) were used to grasp and ablate the T3 ganglia (Fig. 3). With the endoscope in the retroflexed position, the incision of the diaphragm was viewed to make sure there was no haemorrhage (Fig. 4). After suctioning the remaining air in the left thoracic cavity, the endoscope was withdrawn to the abdomen and the left lung was reinflated. The animal was turned to a left lateral decubitus position. Then, the endoscope was moved to the right diaphragm. Under left-lung unilateral ventilation, a 5-mm incision was created on the right diaphragm. With similar protocol as the left T3 ablation, the right T3 thoracic sympathetic nerve was identified and ablated. After withdrawal of the endoscope into the abdominal cavity, the trocar was connected to the suction apparatus and bilateral lungs were inflated. The umbilical incision was sutured.

Figure 1:

Under right-lung unilateral ventilation, a needle-knife was used to incise the left diaphragm.

Figure 2:

Endoscopic image of the thoracic cavity. The sympathetic chain was identified running along the neck of the ribs close to the costovertebral junctions. L: lung; R: rib; S: sympathetic chain.

Figure 3:

The T3 ganglia was grasped and ablated with hot biopsy forceps (arrow): L: lung; S: sympathetic.

Figure 4:

Recurved endoscope to check up the incision of the diaphragm: G: gastroscope.

Animals in the preliminary experiment were euthanized after completion of the operating procedure.

Postoperative care (survival group)

At the end of the surgical intervention, all pigs received a single dose of buprenorphine (0.05 mg/kg, IM) and meloxicam (0.4 mg/kg, IM). Normal diet was started within the following 24 h, and oral antibiotics (300 mg of cephalexin) were given with the chow for the first 5 postoperative days. Chest radiography was performed on Day 2 after surgery to confirm the absence of pneumothorax. The animals were housed individually and closely monitored for any signs of postoperative complications, distress, behavioural changes, anorexia or weight loss. Four weeks after surgery, necropsy examination was then performed with particular attention to the site of thoracic sympathetic and diaphragmatic incision.

RESULTS

Transumbilical flexible endoscopic thoracic sympathectomies were successfully performed in all seven farm pigs. The mean operative time was 66.7 ± 9.4 min. As we have previously described, the diaphragm was easily identified when the gastroscope was introduced into the peritoneal cavity. The diaphragmatic incision was created easily with the needle-knife stabilized by the ultra-long trocar. In this procedure, diaphragmatic bleeding occurred in one pig (Pig 2), which was successfully controlled by electric coagulation using hot biopsy forceps. In the thorax, the lung, pericardium, chest wall and pleura were easily identified (Fig. 5). The prone approach and the CO₂ insufflation provided good exposure of the intrathoracic T3 ganglia without the need for additional retraction instruments. Sympathectomy was successfully ablated in all swines without the need for any extraumbilical skin incisions or conversion to standard thoracoscopy (Fig. 6).

Figure 5:

Endoscopic image of the thoracic cavity. The lung, pericardium, chest wall and pleura were easily identified.

Figure 6:

T3 ganglia was ablated by hot biopsy (arrow): S: sympathetic.

All animals appeared to tolerate the procedure very well. In the survival group, the pigs resumed and tolerated a normal liquid and solid diet on the first postoperative day. All pigs survived well after surgery for 4 weeks without adverse consequences. A small pneumothorax was found in the postoperative chest X-ray in three pigs, but all of them were completely resolved with conservative treatment. Postoperative autopsy confirmed that bilateral T3 ganglias were identified accurately, and cauterization was successful in all pigs. In the acute group, the length of the diaphragm incision ranged from 4 to 5 mm in three pigs (Table 1). In the survival group, adhesions were found between diaphragm, stomach and omental in all animals (Table 2), and no evidence of vital structure injury or diaphragmatic hernia, and no signs of infection in both thoracic and peritoneal cavities were seen.

Table 1:

Results of three acute experiments

Animal no.	Body weight (kg)	Operation time (min)	Length of diaphragm incision (mm)	Success of procedures	Intraoperative complications
1	42.3	76	4	Yes	None
2	43.6	80	5	Yes	Minor bleeding
3	40.8	55	5	Yes	None

Table 2:

Results of four survival experiments

Animal no.	Body weight (kg)	Operation time (min)	Intraoperative complication	Perioperative complications	Necropsy finding
4	42.1	72	None	Mild pneumothorax	Abdominal adhesions
5	44.6	64	None	None	Abdominal adhesions
6	42.7	58	None	Mild pneumothorax	Abdominal adhesions
7	43.5	62	None	Mild pneumothorax	Abdominal adhesions

DISCUSSION

ETS surgery using video-assisted thoracoscope is being established as a safe and effective treatment. However, in the ETS procedure, chest wall incisions can be associated with chronic neuropathic pain and paraesthesia [13]. Despite the use of 2-mm or 3-mm needlescopic equipment and instruments, the postoperative chest pain and paresthesia may not be completely alleviated [14]. In order to avoid these disadvantages, Turner et al. and Yang et al. reported transoesophageal and transoral endoscopic sympathectomy [6, 15]. In spite of the substantial work in the NOTES field, it is clear that there is a long way to go from the present animal experiments to clinical practice [16].

Compared with NOTES, the use of E-NOTES can prevent almost all existing problems associated with the NOTES technique. It provides not only significantly lower technical difficulty but also greatly improved safety, which may facilitate a wider application of this approach that leaves less pain and discomfort. Currently, E-NOTES is the most feasible ‘scarless surgery’ technique available and represents a transition period and an evolution from NOTES in the development of current endoscopic surgery [11, 12].

The present study showed that E-NOTES thoracic sympathectomy was technically feasible and overcomes the shortcomings of transoesophageal ETS ganglionectomy while retaining the advantages of NOTES surgery. It avoids the risk of oesophageal puncture-site fistula and greatly reduces surgical difficulty.

The critical step of the study is to choose the appropriate site of the diaphragmatic incision. In our study, the anterior costophrenic angle was selected as the incision site, which provided the following advantages: (i) convenience for the gastroscope to enter into the thoracic cavity, locate the target organ and perform the surgical operation; (ii) avoidance of large blood vessels in the diaphragm and (iii) ample distance from the heart and pericardium. As the needle-knife penetrates through the diaphragm, the abdominal positive pressure gas enters the thoracic cavity and pushes away the lung tissue, which prevents injury to the lung tissue. Provided that the diaphragmatic incision is ≤5 mm in diameter, there is no concern about postoperative diaphragmatic hernia. Compared with laparoscopy or thoracoscopy, flexible endoscopes lack sufficient support when they enter the thoraco-abdominal cavity, hindering accurate positioning. We used an ultra-long trocar to solve this problem. The trocar can guide and stabilize the endoscope body as it reaches the operating position.

Owing to the special tracheal structure of pigs, it is very difficult to perform double-lumen endotracheal intubation on them. Therefore, we performed left and right tracheal obstruction separately through tracheotomy in order to realize unilateral ventilation. Another difficulty of this surgery was to accurately identify and locate the ganglia. We changed the position of the pigs' body or tilted the operating table during surgery so that the lungs were inclined downward and toward the contralateral side by gravity. As a result, the T3 sympathetic ganglion was exposed very well. When necessary, the ultra-long trocar could be used to push the lung tissue aside to help expose the ganglion. Levels were determined by locating the first rib and counting sequentially down the spine.

Limitations to this study included the small sample size and short-term survival. Although no complication of diaphragmatic hernia was observed in all pigs, there was no denying that it was a potential problem of this technique. Moreover, we could not observe all side effects or complications of the technique as animals cannot report on the amount of pain they are feeling.

In conclusion, transumbilical thoracic sympathectomy is safe and feasible in a porcine model when performed using the currently available endoscopes and instruments. In the following year, we will conduct further developments and larger studies to establish its future value in patient care. Based on the positive experience with this study, we also plan to carry out preclinical studies of transumbilical thoracic sympathectomy on human subjects after obtaining approval from the institutional review board.

Conflict of interest: none declared.