Totally laparoscopic surgery for choledochal cysts with hand‑sewn Roux‑en‑Y reconstruction in a pediatric population
- Authors:
- Published online on: July 2, 2024 https://doi.org/10.3892/etm.2024.12633
- Article Number: 344
Abstract
Introduction
A choledochal cyst (CC) is a congenital biliary malformation characterized by cystic dilation of the biliary duct (1); it is more common in Asian countries than in Western countries and has an estimated incidence ranging from 1/100,000 to 1/1,000 (1,2). Approximately 80% of patients with CCs experience symptoms including abdominal pain, jaundice, or abdominal mass before the age of 10 years (3). Total CC excision with Roux-en-Y hepaticojejunostomy (RYHJ) is currently recommended for patients to avoid potential complications such as hepatic fibrosis, pancreatitis, perforation and biliary malignancy (4,5).
Minimally invasively surgery (MIS) procedures are increasingly being applied in pediatric surgeries (6), including esophageal repair (7), duodenoduodenostomy (8,9) and hepatobiliary surgeries (10,11), and have exhibited benefits for children and even newborns (7,8,10,12). In the past two decades, laparoscopic-assisted surgery has been the most popular procedure for CCs, because it is associated with less postoperative pain, decreased complications and better cosmesis than open surgery (3,5,12,13). The majority of laparoscopic surgeries for CCs involve laparoscopic procedures and extracorporeal Roux-en-Y construction (1,2). However, there are relatively few reports on totally laparoscopic surgery for CCs (TLCCs), due to the limited space in the pediatric abdominal cavity and the operative difficulty. During the last 3 years, some patients with CCs at the Department of Pediatric Surgery, Second Affiliated Hospital of Xi'an Jiaotong University (Xi'an, China) have undergone TLCCs due to the pursuit of their parents for better cosmesis and quality of life for these pediatric patients. In the present study, a retrospective analysis of TLCCs at the aforementioned hospital was conducted to evaluate its efficacy and explore how TLCCs can be performed safely in a pediatric population.
Patients and methods
Patients
TLCCs were performed in 28 out of 71 patients with CCs at the Department of Pediatric Surgery, Second Affiliated Hospital of Xi'an Jiaotong University (Xi'an, China) between June 2020 and June 2023. The enrolled patients consisted of 8 boys and 20 girls with a sex ratio of 1:2.5. The decision for whether or not to undertake the TLCC approach was made preoperatively based on the preferences of the parents and the surgeon. All surgeries were completed by the same experienced pediatric surgeon. Written informed consent was provided by the parents of the children before surgery. The present retrospective study was approved by the Ethics Committee of the Second Affiliated Hospital of Xi'an Jiaotong University (approval no. 2022274; Xi'an, China).
Methods
Clinical data including demographic characteristics, history of illness, laboratory test results and imaging findings, operative data and postoperative outcomes were collected from the electronic medical records and subjected to retrospective analysis. All laboratory test results analyzed in the study were obtained within 1 week before surgery. Operative data were acquired from the documentation recording the surgery, anesthesia and intraoperative care. Postoperative follow-up data were based on clinical records and telephone enquiries. Data are presented as the mean value ± standard deviation, which were calculated by Excel 2016 (Microsoft Corporation).
Operative procedures
All of patients were intubated under general anesthesia in the supine position and underwent TLCCs in the reverse Trendelenburg position. In step 1, a 5-mm umbilical trocar was inserted using the open method and fixed. The CO2 pneumoperitoneum pressure was maintained at 8-12 mmHg based on the age and weight of the patient (1,14). Another 5-mm trocar and two 3-mm trocars were inserted at the right upper abdomen, and the right and left subcostal margins under the laparoscopic view, respectively (Fig. 1). In step 2, a stay suture was placed at the neck of the gallbladder (Fig. 2A) to suspend the liver for splaying of the liver hilum and dissection of the cyst. Meanwhile, the duodenum was constricted downward using laparoscopic forceps by an assistant. The proximal end of the CC was dissected at the level of the common hepatic duct and removed, leaving a stump at ~5 mm from the bifurcation of the common hepatic duct. Bile, protein plugs, or calculi within the cyst were suctioned and washed out. The CC was dissected down to the distal end using a monopolar electrocautery hook and ligated. The total cyst was then removed. In step 3, the Treitz ligament was identified under laparoscopy and the jejunum was cut transversely using a LigaSure (Covidien LLC; Medtronic, Inc.) at 10-20 cm distal to the ligament (Fig. 2B) with management of the mesenteric vascular arch. The distal section of the jejunum was closed using 5-0 polydioxanone (PDS) continuous sutures (Fig. 2C). The Roux-en-Y limb reached the liver hilum in a tensionless manner through a window in the transverse mesocolon. A hand-sewn end-to-side jejunojejunostomy (Fig. 2D), consisting of an all-layer suture with a continuous locking method in the posterior wall and continuous sutures on the seromuscular layer in the anterior wall, was performed laparoscopically. In step 4, an end-to-side hepaticojejunostomy (Fig. 2E) was performed with 5-0 PDS continuous sutures. Mesenteric defects in the jejunum and transverse colon were closed with 5-0 absorbable sutures (Fig. 2F). In step 5, the gallbladder was dissected and removed from its bed. Finally, a drainage tube was placed through the right subcostal trocar incision.
Postoperative management
The urinary catheter was removed on the day after surgery upon normal output of urine. Water intake was commenced at 24 h after surgery and gradually increased every 2-3 h. The nasogastric tube was removed on the following day of onset of water intake if the patient had no abdominal bloating or vomiting. A liquid diet was started on the evidence of recovery of bowel motility. The drainage tube was removed at 5-7 days after surgery when the abdominal ultrasound was negative. Hospital discharge was considered when patients ate normally without any discomfort.
Results
A total of 28 patients with CCs, including Todani types I and IV, underwent TLCCs at our institution. The characteristics of the patients are revealed in Table I. The ratio of male to female patients was 1:2.5. The mean age at operation was 4.2 years (range, 1 month to 12.3 years) and the mean weight was 15.9 kg (range, 4.6-43 kg). Intermittent abdominal pain was the most frequent symptom followed by jaundice, nausea and vomiting. A total of 6 patients were asymptomatic, including 4 patients diagnosed on prenatal ultrasonography and 2 cases discovered accidentally. There was also an uncommon case involving an 11-year-old girl from a remote area who had undergone extrahepatic bile duct drainage for 10 years and visited the aforementioned hospital for further treatment.
Prior to surgery, 3 children had hyperbilirubinemia and 5 had elevated transaminase levels. Ultrasound was the first choice to identify CCs in all patients, and magnetic resonance cholangiopancreatography was performed preoperatively to obtain further information. On imaging, the mean cyst diameter and length were 1.74±0.76 cm and 3.85±1.25 cm, respectively.
As presented in Table II, TLCCs were performed through four operative ports with a mean intraoperative blood loss of 21.0±20.4 ml and a mean operative time of 214±43.8 min. The urethral catheter and nasogastric tube were removed at 1.02±0.70 days and 2.08±1.24 days after surgery, respectively. The mean time to intake of an oral diet was 2.89±1.23 days after surgery. The drainage tube was left for a mean period of 6.25±2.32 days.
Bile leakage occurred in a 4.5-year-old girl on postoperative day 4 and the patient was treated conservatively by drainage and parenteral nutrition for 9 days. A 5-year-old girl experienced an infection in the incision where the drainage tube was placed, which was cured by wound care and antibiotics. The other 26 patients had an uneventful recovery after surgery. The mean hospital stay for postoperative recovery after TLCCs was 6.82±2.12 days. No further complications occurred during a median follow-up period of 18 months (range, 4-42 months) based on clinic visits and telephone enquiries.
Discussion
CCs are more common in Asian countries than in Western countries, and arise through congenital anomalous development of the biliary system (2). Currently, the most common surgical procedure for CCs is performed with laparoscopic assistance, and the Roux-en-Y anastomosis is performed extracorporeally (3,5). With recent advances in laparoscopic techniques and instruments, TLCCs has been reported as an MIS procedure associated with rapid recovery of gastrointestinal function and reduced hospital stay (1). However, the intracorporeal jejunojejunostomy was completed using an Endo-GIA instrument (1,11,15-18) with an additional 12-mm port (1,11,17,18) and increased hospitalization costs (1). Given the rich experience with laparoscopic surgery in pediatric patients at the institution of the authors, the technique of laparoscopic duodenoduodenostomy was applied for the jejunojejunal anastomosis in TLCCs. In the present study, the hand-sewn jejunojejunal anastomosis under laparoscopy was performed intracorporeally based on sophisticated laparoscopic techniques. As well as the advantages of laparoscopic surgery aforementioned, TLCCs are associated with less trauma and smaller incisions without significantly increased costs, and also meets the expectations of the children and their parents for MIS.
During the intracorporeal jejunojejunostomy, the intestine can remain relaxed in the natural position without extracorporeal exposure during the anastomosis. This can reduce intestinal stretching and avoid the possibility of mesenteric vessels being incarcerated by the incision. Consequently, the risk of intestinal injury and postoperative adhesions is theoretically decreased and the recovery of intestine motility can benefit from this approach (1). Compared with previous reports on TLCCs, a running hand-sewn approach was used at the Second Affiliated Hospital of Xi'an Jiaotong University instead of a mechanical anastomosis (endo-GIA) and was applied intracorporeally during the jejunojejunostomy procedure. The present study demonstrated improved results than previous studies regarding operative time, time until oral intake and postoperative hospital stay (Table III). As revealed in Table III, complications including intestinal obstruction and necrosis were reported in 0-7% of cases and were caused by herniation of the distal biliary jejunum into the defect in the transverse mesocolon (1,11), while bile leakage and wound infection occurred in 2 of the patients without bowel obstruction.
In gastrointestinal surgery, mechanical anastomosis with a stapler has been widely used in adult populations (1,11,15,19,20) but rarely used in pediatric populations (15,17,18). Compared with the hand-sewn method, use of a stapler significantly reduced the operative time in digestive anastomoses (20), but some shortcomings other than high cost (20) should be noted, especially in children. It was reported that adverse events associated with stapler use occurred in up to 17.3% of cases, including leakage or dehiscence, bleeding and infection (19), while serosal laceration of the stomach was found in 46% of cases in animal experiments on pigs (21). An additional 12-mm trocar is always required when introducing a stapler device, and it is difficult to operate in the limited space of the pediatric abdominal cavity, thus increasing the trauma to the abdomen and the expense of hospitalization (1,15,16).
On the contrary, laparoscopic manual continuous sutures have been safely used for digestive anastomoses (1,11,22,23), including intestinal anastomoses (11,22), which have been applied in RYHJ (1,11), and require less time than interrupted sutures (8). Moreover, the hand-sewn method has been used to close the hole after side-to-side anastomosis with the use of a stapler and repair the mesenteric defects to prevent intestinal obstruction due to internal herniation (1,11). Nevertheless, it should be considered that manual laparoscopic anastomosis is technically challenging and may increase the operative duration (11,17).
The following methods were selected to minimize the complications of TLCCs in the pediatric patients. First, the length of the Roux-en-Y limb was measured from the hepatic hilum to the umbilicus to avoid a redundant loop. Second, the transverse cut of the jejunum was performed using a LigaSure device, which can achieve temporary closure of the jejunal stoma and reduce contamination of the abdominal cavity (Fig. 2B and C). Third, single-layered continuous sutures were used to close the distal stoma and complete the end-to-side jejunojejunostomy and hepaticojejunostomy. The technique has been applied in bowel anastomosis with lower incidence of anastomotic leak, reduced time duration and lower costs compared with double-layered sutures (24). Fourth, it was important to provide proper tension while suturing and tightening the stitches through an assistant (Fig. 2D), because the jejunum is mobile.
To the best of the authors' knowledge, the present study included the largest number of pediatric patients who underwent TLCCs with manual sutures reported to date. However, the limitations of the retrospective review and the lack of a comparison with conventional laparoscopic surgery for CCs must be acknowledged. Controlled prospective studies will be necessary to determine the safety and superiority of this approach for pediatric CCs.
In summary, TLCCs were safely performed in a cohort of patients with congenital CCs. The intracorporeal jejunojejunal anastomosis was anatomically natural and improved the recovery of bowel function compared with the conventional laparoscopic surgery approach for CCs, moreover, it was associated with less trauma and improved esthetic outcomes. The laparoscopic hand-sewn method was reliable and cost-effective. Therefore, TLCCs with manual sutures may be considered as an option for MIS in pediatric patients with CCs.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
The data generated in the present study may be requested from the corresponding author.
Authors' contributions
QL and JF participated in the study design and data collection, carried out the initial analyses and drafted the article. QY and PL participated in the study conception and design, analysis and interpretation of the data, and critical revisions of the article. QL and JF confirm the authenticity of all the raw data. All authors read and approved the final version of the manuscript and agree to be accountable for all aspects of the work.
Ethics approval and consent to participate
Ethics approval (approval no. 2022274) was obtained from the Ethics Committee of the Second Affiliated Hospital of Xi'an Jiaotong University (Xi'an, China). Written informed consent was provided from the parents of all the children who participated in the present study.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
References
Liu F, Xu X, Lan M, Tao B, Li L, Wu Q, Chai C and Zeng J: Total versus conventional laparoscopic cyst excision and Roux-en-Y hepaticojejunostomy in children with choledochal cysts: A case-control study. BMC Surg. 20(243)2020.PubMed/NCBI View Article : Google Scholar | |
Wen Z, Liang H, Liang J, Liang Q and Xia H: Evaluation of the learning curve of laparoscopic choledochal cyst excision and Roux-en-Y hepaticojejunostomy in children: CUSUM analysis of a single surgeon's experience. Surg Endosc. 31:778–787. 2017.PubMed/NCBI View Article : Google Scholar | |
Xie X, Li K, Wang J, Wang C and Xiang B: Comparison of pediatric choledochal cyst excisions with open procedures, laparoscopic procedures and robot-assisted procedures: A retrospective study. Surg Endosc. 34:3223–3231. 2020.PubMed/NCBI View Article : Google Scholar | |
Guan X, Li J, Wang Z, Zeng J, Zhong W and Yu J: Timing of operation in children with a prenatal diagnosis of choledochal cyst: A single-center retrospective study. J Hepatobiliary Pancreat Sci. 29:1308–1315. 2022.PubMed/NCBI View Article : Google Scholar | |
Section of Laparoscopic&Endoscopic Surgery; Branch of Pediatric Surgery; Chinese Medical Association. Guideline for laparoscopic hepatojejunostomy for choledochal cyst in children (2017). Chin J Pediatr Surg. 38:485–494. 2017. | |
Gil LA, Asti L, Apfeld JC, Sebastião YV, Deans KJ and Minneci PC: Perioperative outcomes in minimally-invasive versus open surgery in infants undergoing repair of congenital anomalies. J Pediatr Surg. 57:755–762. 2022.PubMed/NCBI View Article : Google Scholar | |
van Lennep M, Singendonk MMJ, Dall'Oglio L, Gottrand F, Krishnan U, Terheggen-Lagro SWJ, Omari TI, Benninga MA and van Wijk MP: Oesophageal atresia. Nat Rev Dis Primer. 5(26)2019.PubMed/NCBI View Article : Google Scholar | |
Oh C, Lee S, Lee SK and Seo JM: Laparoscopic duodenoduodenostomy with parallel anastomosis for duodenal atresia. Surg Endosc. 31:2406–2410. 2017.PubMed/NCBI View Article : Google Scholar | |
Chung PHY, Wong CWY, Ip DKM, Tam PKH and Wong KKY: Is laparoscopic surgery better than open surgery for the repair of congenital duodenal obstruction? A review of the current evidences. J Pediatr Surg. 52:498–503. 2017.PubMed/NCBI View Article : Google Scholar | |
Kwon H, Lee JY, Cho YJ, Kim DY, Kim SC and Namgoong JM: How to safely perform laparoscopic liver resection for children: A case series of 19 patients. J Pediatr Surg. 54:2579–2584. 2019.PubMed/NCBI View Article : Google Scholar | |
Gander JW, Cowles RA, Gross ER, Reichstein AR, Chin A, Zitsman JL, Middlesworth W and Rothenberg SS: Laparoscopic excision of choledochal cysts with total intracorporeal reconstruction. J Laparoendosc Adv Surg Tech A. 20:877–881. 2010.PubMed/NCBI View Article : Google Scholar | |
Soares KC, Goldstein SD, Ghaseb MA, Kamel I, Hackam DJ and Pawlik TM: Pediatric choledochal cysts: Diagnosis and current management. Pediatr Surg Int. 33:637–650. 2017.PubMed/NCBI View Article : Google Scholar | |
Yin T, Chen S, Li Q, Huang T, Li L and Diao M: Comparison of outcomes and safety of laparoscopic and robotic-assisted cyst excision and hepaticojejunostomy for choledochal cysts: A systematic review and meta-analysis. Ann Med Surg (Lond). 75(103412)2022.PubMed/NCBI View Article : Google Scholar | |
Liu Q, Fu J, Yu Q, Gong W, Li P and Guo X: Laparoscopic surgery of intra-abdominal lymphatic malformation in children. Exp Ther Med. 24(581)2022.PubMed/NCBI View Article : Google Scholar | |
Urushihara N, Fukuzawa H, Fukumoto K, Sugiyama A, Nagae H, Watanabe K, Mitsunaga M and Miyake H: Totally laparoscopic management of choledochal cyst: Roux-en-Y Jejunojejunostomy and wide hepaticojejunostomy with hilar ductoplasty. J Laparoendosc Adv Surg Tech A. 21:361–366. 2011.PubMed/NCBI View Article : Google Scholar | |
Murakami M, Kaji T, Nagano A, Matsui M, Onishi S, Yamada K and Ieiri S: Complete laparoscopic choledochal cyst excision and hepaticojejunostomy with laparoscopic Roux-Y reconstruction using a 5-mm stapler: A case of a 2-month-old infant. Asian J Endosc Surg. 14:824–827. 2021.PubMed/NCBI View Article : Google Scholar | |
Ahn SM, Jun JY, Lee WJ, Oh JT, Han SJ, Choi SH and Hwang EH: Laparoscopic total intracorporeal correction of choledochal cyst in pediatric population. J Laparoendosc Adv Surg Tech A. 19:683–686. 2009.PubMed/NCBI View Article : Google Scholar | |
Jang JY, Kim SW, Han HS, Yoon YS, Han SS and Park YH: Totally laparoscopic management of choledochal cysts using a four-hole method. Surg Endosc. 20:1762–1765. 2006.PubMed/NCBI View Article : Google Scholar | |
Kuthe A, Haemmerle A, Ludwig K, Falck S, Hiller W, Mainik F, Freys S, Dubovoy L, Jaehne J and Oldhafer K: Multicenter prospective evaluation of a new articulating 5-mm endoscopic linear stapler. Surg Endosc. 30:1883–1893. 2016.PubMed/NCBI View Article : Google Scholar | |
Korolija D: The current evidence on stapled versus hand-sewn anastomoses in the digestive tract. Minim Invasive Ther Allied Technol. 17:151–154. 2008.PubMed/NCBI View Article : Google Scholar | |
Hasegawa S, Nakayama S, Hida K, Kawada K and Sakai Y: Effect of tri-staple technology and slow firing on secure stapling using an endoscopic linear stapler. Dig Surg. 32:353–360. 2015.PubMed/NCBI View Article : Google Scholar | |
Mentessidou A and Saxena AK: Laparoscopic repair of duodenal atresia: Systematic review and meta-analysis. World J Surg. 41:2178–2184. 2017.PubMed/NCBI View Article : Google Scholar | |
Qin R, Kendrick ML, Wolfgang CL, Edil BH, Palanivelu C, Parks RW, Yang Y, He J, Zhang T, Mou Y, et al: International expert consensus on laparoscopic pancreaticoduodenectomy. Hepatobiliary Surg Nutr. 9:464–483. 2020.PubMed/NCBI View Article : Google Scholar | |
Aniruthan D, Pranavi AR, Sreenath GS and Kate V: Efficacy of single layered intestinal anastomosis over double layered intestinal anastomosis-an open labelled, randomized controlled trial. Int J Surg. 78:173–178. 2020.PubMed/NCBI View Article : Google Scholar |