Transumbilical endoscopic cholecystectomy in a porcine model

PURPOSE: Natural orifice transluminal endoscopic surgery (NOTES) is a new technique. This study describes our initial experience of NOTES and investigates the feasibility of transumbilical endoscopic cholecystectomy (TUEC). METHODS: Eight domestic pigs were submitted to TUEC. After establishment of pneumoperitoneum, a bi-channel endoscope was placed through an infra-umbilical trocar. The gallbladder fundus was lifted by a grasper. The cystic duct and artery was dissected with a flexible hook and clipped by a clip fixing device. The specimen was extracted through the infra-umbilical trocar. RESULTS: The mean operation time was 114 minutes, ranging from 75 to 155 minutes. All the gallbladders were removed successfully. There was one case of subtotal resection, two cases of bleeding and three cases of bile leakage. CONCLUSION: Transumbilical endoscopic cholecystectomy is feasible although it needs more support of experiments and techniques before being applied on human subjects.


Introduction
For a long time, the advancement of surgical techniques has continued to allow surgery to minimize invasiveness, to decrease pain and to produce a cosmetic results 1 .The laparoscopic techniques also make significant progress in pursuit of less resultant trauma.Langenbuch performed the first cholecystectomy in 1882 through a subcostal incision 2 .Mouret undertook the first laparoscopic cholecystectomy using video technology in 1987 3 and laparoscopic cholecystectomy has been taken as the gold standard for gallbladder removal surgery since 1992 4 .
Nowadays, the use of minimally invasive surgery has increased.The modern development of minimally invasive surgery has opened up with the move from open to laparoscopic surgery by using multiple small incisions.Recent innovations have employed natural orifice transluminal endoscopic surgery (NOTES) to accomplish laparoscopic procedures.NOTES uses transvisceral access to the peritoneal cavity through the mouth, colon, urinary tract or vagina by using either rigid or flexible instruments 5 .
NOTES may minimize surgical trauma and postoperative pain, reduce wound infection rate, shorten the length of hospital stay, hasten recovery, and result in no ''visible'' scars from surgery 6,7 .
Nevertheless, NOTES is technically difficult and has been limited by concerns regarding the higher risk of abdominal infection and perforation of an organ 8 .Moreover, NOTES requires many special instruments 9 .Thus, for the concerns of these drawbacks, many surgeons consider the umbilicus as an alternative natural orifice due to its origin 10,11 .Meanwhile, the umbilicus is a well-known and standardized and direct site for access to the abdominal cavity for laparoscopic surgery 3  The animals were fasted except water for 48~72 hours before operation.On the day of operation, they were premeditated with intramuscular atropine (0.04 mg/kg), ketamine (10 mg/kg) and sumianxin (0.1 mL/kg), then intubated with an endotracheal tube and received isoflurane (2%) for maintenance of anesthesia.During the operation, scoline (0.1%) was administered for induction of anesthesia.Electrocardiogram leads were placed and connected to the monitor to record heart rate, blood pressure and operative time.

Surgical procedures
After establishment of pneumoperitoneum by CO 2 , the bi-channel endoscope was placed through a 1.5 cm infraumbilical trocar.The abdominal cavity was inspected and a fi ne grasper of 2 mm diameter was inserted through a 5mm trocar on the right upper abdomen.The surgeon performed the dissection by manipulating the control knobs on the endoscope, and the fi rst assistant maintained the position of the endoscope while retracting the gallbladder by grasping its fundus through the 5 mm port.
A second assistant stood on the opposite side of the table and controlled the fl exible endoscopic instruments, which included the hook and the forceps.After the left side was elevated 30 degree and the fundus of the gallbladder was lifted by the grasper, the vascular and cystic duct of gallbladder was exposed.The fl exible grasper and electrosurgical hook were passed through the endoscopic channels to separate the serosa on both sides of the cystic duct and artery, which was cut off after clipped by three hemostatic clips, leaving two clips on the nub (Figu re 2A).The gallbladder was peeled off from the liver by an electrosurgical hook (Figure 2B).The specimen was extracted through the infra-umbilical trocar (Figure 2C).The infra-umbilical incision was closed by subcutaneous stitches.FIGURE 2 -The surgical procedures of TUEC.The fl exible grasper and electrosurgical hook were passed through the endoscopic channels to separate the serosa on both sides of the cystic duct and artery, which was cut off after clipped by three hemostatic clips, leaving two clips on the nub (A).The gallbladder was peeled off from the liver by an electrosurgical hook (B).The specimen was extracted through the infra-umbilical trocar (C).The infra-umbilical incision was closed by subcutaneous stitches.

Postoperative management
Eight animals were sacrifi ced postoperatively immediately.Postmortem examinations of the specimen was carried out, and the blood and bile in the operative region were also investigated.

All procedures were completed without conversion to
an open operation or introduction of any additional trocars.The mean operative time was 114 min, ranging from 75 to 155 min.All the gallbladders were removed successfully.There was one case of subtotal resection, two cases of bleeding from the gallbladder bed and stopped by electric coagulation, one case of bleeding from the artery and stopped by clip, three cases of bile leakage including two cases of perforation of gallbladder during dissection and one case of cystic gall duct clipped incompletely.Postmortem examination revealed that the clips on the cystic duct and artery were secure, without bleeding and bile leakage (Table 1).In recent years, Julianov et al. 15 , Hong et al. 16 and Zhu et al.  operation is much safer and can also reach the effect of minimally invasive surgery with no scar.Therefore, we chose the umbilical approach to accomplish the cholecystectomy.The result of this study proved that TUEC was feasible.However, NOTES also presents certain disadvantages, such as an unstable surgical platform that required multiple operators manipulating the endoscope and controlling the wheels in conjunction with endoscopic instruments 19 .Our operation time was longer than traditional laparoscopic operations and not shortened obviously during the whole experiment.Thus, there must be a long learning curve.The operator should accumulate lots of experience to grasp this technique exactly.
Surgeons get used to perform laparoscopic surgery in a larger view.However, the circular endoscopic view is not stable for the surgeons because of the difficult control of the movement of the endoscope.The surgeon with the basis of endoscope experience should be able to adapt quickly.Some reports 20 show that multiple cameras can be used to obtain suitable view.For example, "R" type endoscope whose second band can be locked so that endoscope can be fixed in the right position and the surgeon can adjust the first bend to operate.
In our study, the additional trocar must be inserted through a small skin incision on the right upper abdomen where the grasping forceps was placed to expose the operation site.This step cannot be ignored with current instruments.Leroy et al. 21finish the first per-anal sigmoidectomy in 2008, during the operation he put a bar magnet inside the sigmoid colon, while putting another bar magnet on the abdomen wall to draw colon to achieve good surgical exposure.This method may be considered to be used in TUEC.
However, the surgical instruments we used were still simple, and the grasping forceps and electrosurgical hook were still used in this study.Since TUEC was more difficult than laparoscopic surgery, bleeding or bile leakage may happen in the early stage 22 .In this study, there was 1 case that the gallbladder was broken by the grasping forceps, which was attributed to the shortage of the instruments.Thus, all the instruments, including those used for the exposure of operative field, such as grasping forceps, hemostatic clips and suction, should be improved further in order to make operation convenient.The right way to deal with the cystic duct and artery was the most important step during the operation 23 . Moreover, transumbilical endoscopic cholecystectomy (TUEC) can be performed with standard laparoscopic instruments.Cholecystectomy is the most commonly performed laparoscopic procedure in the world and the first NOTES cholecystectomy was performed in 2007.Since then, variations have been employed in clinical practice, and NOTES cholecystectomy has been successfully performed via the transgastric route 1 .However, little literature was published on TUEC.For these reasons, the aim of this study is to know which advantages, difficulties and limitations are involved in performing TUEC.Methods The procedures were in accord with the Ethical Committee on Human Experimentation of Renji Hospital, Shanghai Jiaotong University School of Medicine.The use of laboratory animals follow the Council for International Organization of Medical Sciences (CIOMS) ethical code for animal experimentation.Eight domestic pigs weighed 25 to 30 kg were presented for TUEC.

17
report successful cases of transumbilical cholecystectomy due to the diffi culties of procedures in NOTES.However, they fi nish the operation with the rigid laparoscopic instrument which is exactly so-called single-incision laparoscopic skill.Palanvielu et al.18 first present a hybrid technique for cholecystectomy in 2008, namely the combination of a flexible transumbilical bi-channel endoscope and a 3-mm rigid transcutaneous trocar placed in the right hypochondrium for liver retraction.It seems more promising for clinical application than former standard NOTES.Currently, the natural orifices for NOTES include stomach, vagina, colon, anus, bladder and others.Surgical risks of NOTES are evident when the visceral incision is closed and severe postoperative complications such as abdominal abscess, gastrointestinal leakage, and bleeding appeared.Transumbilical . Otherwise, once bleeding or bile leakage happened, it would bring a lot of troublesome, even lead to conversion to an open operation.Because the cystic duct and artery of the pigs are longer than those of human, it can be exposed easily.However, their anatomical position are too closed to be separated.We separated the serosa on both sides of the cystic duct and artery as much as possible and clipped them together exactly by three hemostatic clips, leaving two clips on the nub.While peeling the gallbladder off by using electrosurgical hook, the operator should distinguish the anatomic levels to avoid bleeding from gallbladder bed, and perforation of the gallbladder wall.Once bleeding, the operator should distinguished the site in time and clip or fulgurate it in order to stop the bleeding.There are several trocars in traditional laparoscopic surgery.Suction and operation can be performed at the same time.However, there was only one free trocar in TUEC.Bleeding and bile leakage will greatly affect the view which maybe result in biliary injury.We put the suction through the trocar on the right upper abdomen to suck the bile or b1ood away.If the bleeding volume was more, additional trocars were introduced to perform the suction and hemostasis.Of course, the open operation was still one of choices which make the operation safe.We propose that TUEC is entirely feasible while it needs improved equipment and more skill.In recent years, as NOTES still has several technical difficulties to be solved, new concepts of minimally invasive surgery are proposed, including laparoendoscopic single-site surgery (LESS) and 'Da Vinci' robotic surgery, which have been applied on human subjects and developed rapidly.Hernadez et al.24 follow 150 patients undergoing LESS cholecystectomy and consider the learning curve of LESS cholecystectomy is definable, short and safe, and the key point of the surgery is similar to multi-incision surgery.Furthermore, another new technique 'Da Vinci Robot', which could help surgeons accomplish various complicated operations such as resection of gastric carcinoma, right hemicolectomy, pancreatoduodenectomy and others.Although it is feasible in our experiment, the future of TUEC is uncertain because of its technical difficulties and the existing problems compared to LESS.
*Case 1: Gallbladder subtotal resection Discussion NOTES has hitherto been performed in several institutions.Swain et al. 12 report the experimental data of transgastic cholecystectomy on swine in 2004.Marescaux et al. 13 report their fi rst transvaginal endoscopic cholecystectomy in Strasburg on April 2007, which is the fi rst real clinical NOTES.