Minimally Invasive Advanced Surgery for Esophageal Atresia with Tracheoesophageal Fistula and Biliary Atresia

Minimally invasive surgery in children has evolved to the extent that complex procedures can be performed with safety, with comparable outcomes to open surgery and with the advantages of minimal postoperative scarring and lesser pain. In this article, we describe the latest thoracoscopic and laparoscopic techniques used at Juntendo University Hospital, for treating patients with advanced surgery, focusing on esophageal atresia with tracheoesophageal fistula and biliary atresia.


Introduction
A combination of innovative technology use and growing patient awareness has meant that minimally invasive surgery (MIS) for needed pediatric advanced surgery such as esophageal atresia with tracheoesophageal fistula (EA with TEF), biliary atresia (BA), congenital diaphragmatic hernia, choledochal cyst, imperforate anus and Hirsch-sprungʼ s disease, had to be made available as a treatment option, limited only by availability and the preference and confidence on the part of surgeons. Such procedures are performed routinely at our institution. They involve surgical intervention requiring surgeons to have a mastery over complex skills and an exhaustive knowledge of anatomical variations, while parents of pediatric patients expect comparative advantages, such as, better cosmesis, less requirement for analgesia, a more rapid return to baseline functional status, quicker return to social life, and less postoperative adhesion.
Here, we focus on the special features of our thoracoscopic repair for EA with TEF and laparoscopic treatment for BA.

Esophageal atresia with tracheoesophageal fistula Our surgical technique 1)
General endotracheal anesthesia is administered and the subject is positioned semiprone on the operating table. To begin, a 5-mm port is created with CO2 pressure at 4 mmHg using a short 5 mm, 30°scope. Initially, there is usually a period of desaturation and a rise in pCO2, requiring careful adjustment of ventilation. However, stabilization is rapid and within several minutes, two more 5-mm ports can be created, one in the axilla and one more posteriorly and in line with the two already created (Figure-1).
The azygos vein is then divided using Ligasure ® (Valley lab, Boulder, CO), and the distal esophagus is mobilized circumferentially as close as possible to the trachea. Dissection of the distal esophagus should be minimal in order to maintain good blood supply to the proximal end of the distal esophagus. The fistula is clipped using a 5-mm titanium clip ENDO-CLIP ® (Covidien, Mansfield, MA) and divided to leave the lateral 1/5 intact, a maneuver that prevents circumferential retraction of the mucosa from the esophageal muscles and also prevents retraction of the distal esophagus (Figure-2). Attention is then given to dissecting the upper pouch. The upper pouch can be more easily identified when the anesthetist gently pushes on the Replogle ® tube. The upper pouch is then mobilized enough to allow an anastomosis to be performed without undue tension. The tip of the pouch is excised with gentle traction to create an opening 1.5-2 times the size of the distal end for esophagostomy leaving the lateral 1/5 of the tip of the upper pouch untouched to prevent circumferential retraction of the mucosa from the esophageal muscles. With the two esophageal ends mobilized, the anastomosis is performed using 5-0 or 6-0 absorbable suture on a small needle (Figure-3). The back wall is secured first (five to six sutures), with the knots being intraluminal. A small tube is

Figure-1 Trocar locations
The initial trocar is introduced in the 4th intercostal space in the mid-axial line. The other two trocars are then introduced in the posterior-axial line one interspace below the first one, and in the mid-axial line one interspace above the first one.

Figure-2 Tracheoesopageal fistula
The fistula (asterisk) is clipped using a 5-mm titanium clip and divided to leave the lateral 1/5 intact, a maneuver that prevents circumferential retraction of the mucosa from the esophageal muscles and also prevents retraction of the distal esophagus. U: upper pouch esophagus. L: lower esophagus.

Figure-3 Esophagoesophagostomy
With the two esophageal ends mobilized, the anastomosis is performed using 5-0 or 6-0 absorbable sutures on a small needle. The sutures are placed in an interrupted fashion. U: upper pouch esophagus. L: lower esophagus.
then passed under direct viewing through the anastomosis into the stomach. The anterior wall is then completed with the nasogastric tube acting as a guide to prevent incorporation of the posterior wall and to ensure patency of the anastomosis. Adequate bits of tissue are needed to prevent the sutures from tearing the esophagus. Also it is imperative to incorporate the mucosa in every stitch. Once the anastomosis is complete, a chest drain is inserted under direct viewing with the tip adjacent to the anastomosis.

Biliary atresia Our surgical technique 2)
Under general anesthesia, patients are placed in the reverse Trendelenburg position. A 30°5-mm or 10-mm laparoscope is inserted through GelPOINT ® mini Access Platform (Applied Medical, Rancho Santa Margarita, USA) through a 2-cm umbilical incision. Pneumoperitoneum is created with CO2 pressure at 8 mmHg, and increased to 12 mmHg if required, using CO2 gas at a flow rate of 0.5-1.0 L min. Two additional 5 mm trocars are inserted, one in the right upper quadrant and one in the left upper quadrant. Adequate exposure of the porta hepatis is crucial, and is achieved by elevating the liver using a percutaneous stay suture just below the xiphoid process to snare the falciform ligament and retract the liver. Two additional percutaneous stay sutures are placed one each in the parenchyma of the right and left lobes to elevate the liver for further exposure of the porta hepatis. The use of a Nathanson retractor (Teleflex Medical, UK), placed through the epigastrium, has also proven effective for exposing the porta hepatis for anastomosis. The cystic duct and the mid-to-distal biliary remnant are dissected using a combination of hook diathermy, Ligasure ® (Valley lab, Boulder, CO) and tissue forceps. The fibrotic biliary remnant is then transected distally at the superior border of the duodenum. The distal end of the biliary remnant is elevated to enable the right and left hepatic arteries, and the bifurcation of the main portal vein, to be clearly visible. When dissecting the fibrotic biliary remnant, special attention must be given to the small vertical branches of the portal veins located around the biliary remnant at 3, 6, and 9 oʼclock; these drain into the caudate lobe. Our approach is unique in that we do not use high-power hook diathermy to divide these branches because we believe diathermy causes extensive lateral thermal injury that could extend as far as the fibrotic biliary cone and damage any viable microscopic-size bile ducts that may be present. Instead, we use a Ligasure ® device because it generates far less lateral thermal energy, and to prevent any risk of secondary complications caused by direct pressure and heat on the right or left portal veins, such as portal vein thrombosis. The Ligasure ® device is guided through the existing para-umbilical port, or by an extra 5 mm trocar inserted into the epigastrium to ensure that only the tips of the device make contact with the tissue to be sealed (portal vein branches); the device can be inserted into the abdomen almost vertically. The level of transection closely follows the Kasaiʼs original procedure description, leaving the liver parenchyma intact.
The ligament of Treitz is identified and the jejunum 15-cm distal of the ligament is exteriorized through the umbilical port site to create the Roux-en-Y jejunal loop extracorporally. Pneumoperitoneum is paused and the jejunum is divided; the length of the Roux limb is determined by bringing it up to above the xiphoid process on the anterior abdominal wall. All our Roux limbs are customized and we never predetermine a Roux limb to be 30, 40, or 50 cm in length, for if we predetermined wrongly and it were to be too long for the patient, it could become tortuous as the patientʼs body grows and develops, leading to stasis in the Roux limb and cholangitis. A jejunojejunostomy is performed extracorporally. The customized Roux limb is approximated to the native jejunum for 8 cm cranially to prevent intestinal contents of the native jejunum from refluxing into the Roux limb. The jejunojejunostomy should fit naturally into the splenic flexure after the anastomosis is complete 3) . Finally, an antimesenteric enterotomy is performed near the closed end of the Roux limb and the jejunum returned to the abdominal cavity, the pneumoperitoneum is reestablished, and the jejunal limb is passed through a retrocolic window to lie tensionfree at the porta hepatis. For the enterotomy, a scalpel should be used for creating the enterotomy in the jejunum to prevent burning of the jejunal wall that will be used for the portoenterostomy anastomosis; we never use diathermy with coagulation mode for the enterotomy, since it is associated with burning and can cause scarring along the anastomotic line of the portoenterostomy. If an enterotomy were to be performed slightly more on the anterior side in the jejunum rather than on the anti-mesenteric side, the hepaticojejunostomy would be easier, since the mucosa in the posterior wall in the jejunum could be easily identified while performing the anastomosis.
Anastomotic sutures (5/0 or 6/0 PDS) are placed between the enterotomy and the liver parenchyma around the margin with the transected portal plate. To minimize microbile duct injury during the anastomosis, we did not place sutures in the liver parenchyma at 2 and 10 oʼclock, where the right and left bile ducts should be, but suture the connective tissue around the 2 and 10 oʼclock positions at the porta hepatis (Figure-4). Also, all sutures for the anastomosis are deliberately shallow, especially at the 2 and 10 oʼclock positions, but deep enough to prevent leakage.
A tube drain is inserted in the foramen of Winslow. The gallbladder is extracted through the umbilical wound. The trocars are removed and the wound incisions are closed.

Esophageal atresia with tracheoesophageal fistula
Table-1 shows the summary of the outcomes of our cases in comparison with the previous large series. In our cases, the body weight and age at operation varied widely. The operative times ranged from 180 to 300 minutes. There were no known major intraoperative complications. The gap distance between the proximal and distal esophagus ranged from zero to three vertebral bodies. Three patients (13.6%) suffered anastomotic leakage, which healed following conservative management. Four patients (18.1%) developed anastomotic stricture. Endoscopic dilatation was successful in all cases. Recurrent TEF developed in one infant (4.5%), whom required surgical closure of the recurrent TEF. Tracheomalacia requiring prolonged intubation and aortopexy was not performed in any of the patients. Three patients with gastroesophageal reflux disease (13.6%) later required fundoplication.
In evaluating the outcomes of the current series, the overall mortality rate was similar to that of previous reports (Table-1). The incidence of leakage, the recurrent TEF, and the later fundoplication also favorably compare with the previous thoracoscopic and open serie 4)-6) . These data are consistent with the results of a recent metaanalysis that indicated that thoracoscopic repair of    7) . According to our experience, the handling of the wider gap is different and primary anastomosis is possible after excessive mobilization of the proximal and distal esophagus in most cases of EA/TEF. As the thoracoscopic approach have made deep neck dissection possible under direct viewing, there was no vocal cord paralysis even after excessive dissection in the current series. This may be another advantage of the thoracoscopic approach. The most obvious advantage of thoracoscopic approach is that direct mechanical manipulation of the lungs is eliminated resulting in fewer postoperative respiratory tractrelated complications and smooth recovery 8) . Finally the primary advantages of the thoracoscopic approach lie in the potential for a reduction in the musculoskeletal sequelae that often develop following thoracotomy in the newborn. Previous reports described a high incidence of significant musculoskeletal deformities, including a winged scapula, asymmetry of the thoracic wall, and severe scoliosis 9) . As there were no long-term negative outcomes during the present study, we were unable to evaluate any complications. Long-term follow-up is necessary to evaluate the degree and incidence of any musculoskeletal deformities.

Biliary atresia
We began using laparoscopy to perform Kasai portoenterostomy clinically in 2009, encouraged by improvements in technology patient awareness of MIS and successful trials. Since then, several other institutions in Japan have started performing laparoscopic portoenterostomy (lap-PE) with inconsistent results. We attribute our results to a close adaptation of the surgical principles of Kasaiʼs original procedure. We are currently reviewing 15 of our lap-portoenterostomy cases, focusing on jaundice clearance (JC)(total bilirubin ≤1.2 mg/dl) and rates of survival with the native liver (SNL) as indicators of success. JC was 92.8% (13 out of 14 cases). Postoperative cholangitis complicated 7 out of 14 cases (50.0%). Five cases required liver transplantation (LTx), resulting in an SNL ratio of 9/14 (64.2%). In these LTx cases, intra-abdominal adhesions were much milder than in LTx performed following open Kasai, thus shortening operating times. All SNL cases are currently jaundice free with cosmetically aesthetic wounds; however, in one case, a 5-year-old boy is currently having percutaneous transhepatic cholangio drainage for a bile leak at the porta hepatis. To date, we have been able to perform lap-PE safely in all cases, with high SNL to JC ratios, even though the operative times for lap-PE have been long ([up to] 8 hours 50 minutes). We expect operating times to shorten with experience gained from performing more surgeries.
Our efforts 10)-12) to resurrect Kasai portoenterostomy as a laparoscopic procedure since 2009 hoping to emulate the original procedure so masterfully developed by Kasai and achieve the SNL and JC results he achieved safely with his open procedure, have been highly encouraging. Despite lengthy operative times, our lap-PE would appear to be as effective as conventional Kasai portoenterostomy based on comparisons with historical reports in the literature, and lap-PE series from elsewhere 13) . This is an important point, because early diagnosis and appropriate surgical intervention greatly influence outcomes of BA. In addition, we believe that limited dissection, performed carefully following Kasaiʼs original instructions, is what probably lead to better results. The latter is what we greatly attribute the success of our lap-PE to.

Conclusions
In the hands of experts, both thoracoscopic repair for EA with TEF and laparoscopic portoenterostomy for BA are safe and effective procedures for children. The operative times are comparable, post-operative recovery is faster and morbidities are less frequent as a result of the method, than those after open surgery. With the advance of technology and the use of finer instruments, robotic-assisted procedures for EA with TEF and BA are likely to be adopted as alternatives in the future. However, higher quality and longer follow up studies are now required to more definitily and comprehensively determine the role of thoracoscopic repair for EA with TEF and laparoscopic portoenterostomy for BA.