Laparoscopic definitive surgery for choledochal cyst is performed safely and effectively in infants.

Background: Laparoscopic definitive surgery for choledochal cyst (CC) in infants requires advanced skills because of their small size. If patients with a prenatal diagnosis of CC have any biliary symptoms, they need semi-emergency definitive surgery. This study aimed to estimate whether laparoscopic definitive surgery for CC can be performed safely and effectively in infants, especially when emergency surgery is required. Patients and
Methods: From January 2006 to December 2019, 21 patients under 1 year of age underwent laparoscopically or open definitive surgery, and 16 patients aged 3-5 years underwent laparoscopic surgery for CC at our institution. In cases of prenatal diagnosis, elective surgery (EL) was performed at about 6 months of age for patients with no biliary symptoms; the semi-emergency surgery (EM) was performed when patients had any biliary symptoms. Surgical outcomes were retrospectively compared between the Lap <1 y and Op <1 y groups and between the Lap <1 y and Lap 3-5 y groups. In addition, the surgical outcomes of those who underwent EM were also evaluated.
Results: Operative time was significantly longer, and blood loss was significantly lower in the Lap <1 y group than in the Op <1 y group. All surgical outcomes were similar between the Lap <1 y and Lap 3-5 y groups and between the EM and EL groups.
Conclusion: Laparoscopic definitive surgery for CC in infants under 1 year of age is safe and feasible. Even semi-emergency laparoscopic surgery can be performed safely and effectively in small infants.

INTRODUCTION

Choledochal cyst (CC) is characterised by dilatation of the common bile duct and is associated with pancreaticobiliary maljunction. Complete excision of the extrahepatic bile duct and formation of an anastomosis between the hepatic duct and jejunum is needed for complete remission.[123] Definitive surgery for CC in infants requires expertise because of their small size. The timing of surgery for prenatal diagnosis of CC is not clearly defined, but if patients with a prenatal diagnosis of CC have any biliary symptoms, they require semi-emergency definitive surgery. When it is unavoidable to perform semi-emergency surgery on an infant with a small body size, there is a concern about the risk of surgery and complications. This study aimed to clarify whether laparoscopic surgery for CC in infants under 1 year of age can be performed safely and effectively compared to open surgery and laparoscopic surgery in children aged 3–5 years. We also investigated whether semi-emergency definitive surgery in smaller infants can be safely performed.

PATIENTS AND METHODS

From January 2006 to December 2019, 21 patients under 1 year of age underwent laparoscopically or open definitive surgery, and 16 patients aged 3–5 years underwent laparoscopic surgery for CC at our hospital. In cases of prenatal diagnosis, elective surgery (EL) was performed at about 6 months of age for patients with no biliary symptoms. Jaundice, acholic stool, abdominal pain and vomiting were defined as biliary symptoms. If patients had any biliary symptoms and did not improve with conservative therapy, they required semi-emergency surgery (EM). Patients were divided into three groups: Laparoscopic surgery for under 1 year of age (Lap <1 y group), open surgery for under 1 year of age (Op <1 y group), and laparoscopic surgery for those aged 3–5 years (Lap 3–5 y group). Further, the Lap <1 y group was divided into two subgroups: Patients who underwent EM (n = 6) and those who underwent EL (n = 8). Demographic and clinical data, including sex, age, Todani's classification, prenatal diagnosis, operative procedure, operative time, amount of blood loss, post-operative complications and length of hospital stay, were retrospectively collected from patients’ medical records. Surgical outcomes (operative time, blood loss, treatment of intrahepatic bile duct stenosis, post-operative complications and length of hospital stay) were retrospectively compared between the Lap <1 y and Op <1 y groups, and between the Lap <1 y and Lap 3–5 y groups. In addition, the surgical outcomes of those who underwent EM were also evaluated.

Continuous data were compared using the Wilcoxon rank-sum test, and categorical data were compared using Fisher's exact test. The differences with P < 0.05 were considered statistically significant. The study protocol was approved by the hospital medical ethics committee (approval number 2020-0200).

Operative procedure

The patient was placed in the supine position. For laparoscopic procedure, a Mercedes incision was made in the umbilicus.[4] Longitudinal incisions were made in the linea alba and peritoneum, and a multichannel port with a 5-mm camera port was inserted through the incision. Two 3- or 5-mm ports were inserted into the right paraumbilical and left upper abdomen and one 3-mm port was inserted into the right upper abdomen. All manipulations were performed using 3- and 5-mm forceps. The abdominal cavity was inflated at 8 mmHg. The dilated common bile duct was transected transversely, and the contents of the cysts were evacuated to enlarge the working space. Cyst dissection was continued to the pancreaticobiliary junction in the pancreas using monopolar electrocautery. The common bile duct was ligated just before it joined the pancreatic duct. Subsequently, the proximal bile duct was dissected up to the hepatic hilum. The intrahepatic bile ducts were sufficiently observed using a laparoscope to examine whether intrahepatic stenosis existed. Bile ductoplasty was performed if intrahepatic bile duct stenosis was present. The septal stenosis was incised or excised [Figure 1]. The membranous stenosis was cut or excised, and the cut surface was sutured with 5-0 or 6-0 monofilament absorbable sutures [Figure 2]. After creating a Roux-en-Y limb with exteriorization via the umbilical incision, end-to-side hepaticojejunostomy was performed laparoscopically with a single layer of interrupted 5-0 monofilament absorbable sutures.

Figure 1

(a) Septal stenosis (arrowhead) is observed. (b) The septum has been incised (case of a 3-month-old girl)

Figure 2

(a) Membranous stenosis (arrowhead) is observed in the right intrahepatic bile duct. (b) Another membranous stenosis is observed. (c) The lumen of the bile duct has been expanded after intrahepatic bile ductoplasty (case of a 1-month-old girl)

Open procedures were performed under the right subcostal incision. Cyst dissection was continued to the pancreaticobiliary junction in the pancreas using monopolar electrocautery, and the common bile duct was ligated just before it joined the pancreatic duct in the same manner as in laparoscopic surgery. The intrahepatic bile ducts were sufficiently observed to examine whether intrahepatic stenosis existed under direct view. Bile ductoplasty was performed if intrahepatic bile duct stenosis was present. After creating a Roux-en-Y limb with exteriorisation, end-to-side hepaticojejunostomy was performed with a single layer of interrupted 5-0 monofilament absorbable sutures.

RESULTS

Fourteen patients under 1 year of age underwent laparoscopic surgery (Lap <1 y group), and seven patients underwent open surgery (Op <1 y group). Patients’ demographic data are summarised in Table 1. Age at the time of definitive surgery; Todani's classification, including type Ia and IV; and the diameter of the common bile ducts were similar between the Lap <1 y and Op <1 y groups. Prenatal diagnosis of CC was performed in eight (57%) and three (43%) patients (P = 0.66) at 27 and 19 weeks (P = 0.13) for the Lap <1 y and Op <1 y groups, respectively. Semi-emergency surgery was required because the biliary symptoms did not improve with conservative therapy in six (43%) and two (29%) patients (P = 0.66) of the Lap <1 y and Op <1 y groups, respectively.

Table 1

Patients characteristics of the laparoscopy (Lap <1 y) and laparotomy (Op <1 y) groups

	Lap <1 y (n=14)	Op <1 y (n=7)	P
Age at surgery (month)	3 (2.8-4.8)	6 (5-8)	0.08
Body weight at surgery (kg)	5.6 (4.6-7.4)	7.1 (5.6-7.9)	0.26
Sex (male), n (%)	2 (14)	1 (14)	1.00
Todani’s classification
Ia	4	0	0.26
IV-A	10	7
Diameter of CBD	34 (24-46)	31 (28-53)	0.79
Prenatal diagnosis, n (%)	8 (57)	3 (43)	0.66
Gestational age at diagnosis (week)	27 (20-31)	19 (19-28)	0.13
Symptom, n (%)	7 (50)	5 (71)	0.64
Jaundice	4 (29)	5 (71)	0.16
Acholic stool	4 (29)	4 (57)	0.35
Vomiting	3 (21)	1 (14)	1.00
Emergency operation (cases), n (%)	6 (43)	2 (29)	0.66

CBD: Common bile duct

The comparison of surgical outcomes between the Lap <1 y and Op <1 y groups is summarised in Table 2. The operative time was significantly longer in the Lap <1 y group (358 min vs. 243 min, P < 0.05); however, the amount of blood loss/body weight ratio was significantly lower in the Lap <1 y group (2.9 mL/kg vs. 12.6 mL/kg, P < 0.05). There was no difference in the cases of blood transfused. Intrahepatic bile ductoplasty for bile duct stenosis was performed in 12 (86%) and 7 (100%) patients of the Lap <1 y and Op <1 y groups, respectively (P = 0.53). The occurrence of post-operative complications was similar in both groups. Anastomotic leakage occurred in two patients in the Lap <1 y group (P = 0.53), but improved with conservative therapy in both cases. There were no cases of anastomotic stricture. The pancreatic fistula was observed in one patient in the Op <1 y group (P = 0.33).

Table 2

Surgical outcomes, Lap <1 y versus Op <1 y

	Lap <1 y (n=14)	Op <1 y (n=7)	P
Operative time (min)	358 (323-452)	243 (237-331)	<0.05
Amount of blood loss/body weight ratio (mL/kg)	2.9 (1.1-6.4)	12.6 (7.5-15)	<0.05
Intrahepatic bile ductoplasy (cases), n (%)	12 (86%)	7 (100%)	0.53
Complications, n (%)
Total	4 (29)	1 (14)	0.62
Anastomotic leakage	2 (14)	0	0.53
Anastomotic stricture	0	0	-
Pancreatic fistula	0	1 (14)	0.33
Hepatolithiasis	0	0	-
Chylous ascites	1 (7.1)	0	0.53
Abdominal fluid collection	1 (7.1)	0	0.53
Length of hospital stay (days)	10 (8-16)	13 (10-15)	0.26

The comparison of surgical outcomes between the Lap <1 y and Lap 3–5 y groups is summarised in Table 3. The operative time and amount of blood loss/body weight ratio were not significantly different between the groups (358 min vs. 360 min, P = 0.97; 2.9 mL/kg vs. 2.8 mL/kg, P = 0.74). Post-operative complications occurred in four (29%) and five (31%) patients (P = 1.00), of the Lap <1 y and Lap 3–5 y groups, respectively.

Table 3

Surgical outcomes, Lap <1 y versus Lap 3-5 y

	Lap <1 y (n=14)	Lap 3-5 y (n=16)	P
Body weight at surgery (kg)	5.6 (4.6-7.4)	15 (13-17)	<0.05
Operative time (min)	358 (323-452)	360 (329-440)	0.97
Amount of blood loss/body weight ratio (mL/kg)	2.9 (1.1-6.7)	2.8 (21.1-4.6)	0.74
Intrahepatic bile ductoplasy (cases), n (%)	12 (86)	10 (63)	0.23
Complications, n (%)
Total	4 (29)	5 (31)	1.00
Anastomotic leakage	2 (14)	0	0.21
Pancreatic fistula	0	2 (13)	0.49
Chylous ascites	1 (7.1)	0	0.47
Abdominial fluid collection	1 (7.1)	1 (6.2)	1.00
Port site hernia	0	1 (6.2)	1.00
Length of hospital stay (days)	10 (8-16)	11 (8-13)	0.90

Finally, the Lap <1 y group was further divided into two groups to compare the surgical outcomes of patients who underwent EL and EM [Table 4]. At the time of surgery, age and body weight were significantly lower in the EM group (P < 0.05). The operative time and amount of blood loss/body weight ratio were similar between the groups (350 min vs. 389 min, P = 0.25; 2.5 mL/kg vs. 2.9 mL/kg, P = 0.56). Intrahepatic bile ductoplasty was performed at a high rate of 80% in both EM and EL groups. Post-operative complications occurred at similar rates between the two groups. Anastomotic leakage occurred in one patient in each group (1 [17%] vs. 1 [13%], P = 1.00). Chylous ascites occurred in one patient in the EM group, but it improved with conservative therapy. The post-operative length of hospital stay was similar between the groups (10 days vs. 11 days, P = 0.90).

Table 4

Surgical outcomes, emergency operation versus elective operation (in Lap <1 y)

	EM (n=6)	EL (n=8)	P
Age at surgery (month)	2.5 (0.8-3.3)	4.0 (3-7.8)	<0.05
Body weight at surgery (kg)	4.6 (3.7-5.5)	7.2 (5.0-8.1)	<0.05
Operative time (min)	350 (303-375)	389 (327-547)	0.25
Amount of blood loss/body weight (mL/kg)	2.5 (0.6-7.9)	2.9 (1.7-5.6)	0.56
Intrahepatic bile ductoplasty (cases), n (%)	5 (83)	7 (88)	1.00
Complications, n (%)
Total	2 (33)	2 (25)	1.00
Anastomotic leakage	1 (17)	1 (13)	1.00
Chylous ascites	1 (17)	0	0.43
Abdominal fluid collection	0	1 (13)	1.00
Length of hospital stay (days)	10 (8.0-18)	11 (8.3-18)	0.90

EM: Emergency operation, EL: Elective operation

DISCUSSION

CC is characterised by pancreaticobiliary maljunction with dilatation of the common bile duct. Complete excision of the common bile duct and hepaticoenterostomy is commonly performed.[5]

Laparoscopic cystic excision of CCs was first conducted in 1995 by Farrello, and there have been numerous reports since then.[678910] The most recently reported meta-analysis showed that laparoscopic cystic excision is a safe, valid and feasible alternative to open excision.[11] It has been reported that laparoscopic surgery in newborns and infants can be performed safely.[121314] However, 1 of 10 cases required redo hepaticojejunostomy because of bile leakage after laparoscopic surgery,[14] whereas 2 of 14 cases required a shift from laparoscopic surgery to laparotomy.[12] These facts indicate that laparoscopic surgery for CC in newborns and infants may not be completely safe. In the present study, we investigated whether laparoscopic surgery, including intrahepatic bile duct formation and complete resection of the intrapancreatic bile ducts, could be safely performed in infants aged ≤1 year. First, the surgical outcomes of laparoscopic definitive surgery in patients aged ≤1 year were compared with those of open surgery, followed by a comparison with the surgical outcomes of laparoscopic surgery in patients aged 3–5 years. Finally, surgical outcomes of laparoscopic EM required for biliary symptoms were also compared with those of laparoscopic EL. There were neither any significant differences in post-operative complications and length of hospital stay between the Lap <1 y and Op <1 y groups, nor were there any differences in the surgical outcomes (operative time, amount of blood loss/body weight ratio, post-operative complications and length of hospital stay) of the Lap <1 y and Lap 3–5 y groups.

In recent years, the rate of prenatal diagnosis of CC through routine maternal ultrasonography has been increasing.[1516] Many patients identified in the prenatal period are asymptomatic, but some have obstructive jaundice, rupture of the common bile duct and vomiting due to the increased intraductal pressure of the pancreaticobiliary tract.[1217] The optimal timing of definitive surgery for prenatally diagnosed cases is controversial. Many studies, following Japanese guidelines, recommend elective surgery for asymptomatic cases.[51618] For asymptomatic cases, it is better to wait until the infants are 3–6 months old in order to avoid the risk of ruptured sutures or anastomotic stricture, both of which are attributed to the small diameter of their bile ducts.[5] However, some studies have reported that surgery could be performed during the neonatal period.[1319] It should also be noted that the grade of liver fibrosis may increase with age.[19] Our treatment policy is to perform elective surgery in patients with no biliary symptoms at the age of approximately 6 months. If biliary tract symptoms, such as jaundice, acholic stool, abdominal pain or vomiting occur and do not improve with conservative therapy, semi-emergency surgery is performed. There was no difference in surgical outcomes between the EM and EL groups. Therefore, semi-emergency laparoscopic surgery for infants with CC can be safely and effectively performed.

Surgery for CC has two main issues. First, intrahepatic calculi occurred in 7%–10% of patients after open excision of the CC.[2021] The main cause of intrahepatic calculi formation is thought to be intrahepatic bile duct stenosis, which includes membranous and septal stenoses rather than anastomotic stenosis.[22] It should be treated from the divided end of the common hepatic duct during the initial operation for CCs.[23] Bile ductoplasty under laparoscopic surgery has also been reported.[2425] Stenosis of the intrahepatic bile duct was present in 75 (80.6%) of 93 patients with CC in the previous report.[22] In the present study, intrahepatic bile duct stenosis was observed, and intrahepatic ductoplasty could be performed laparoscopically in 12 of 14 patients under 1 year of age (similar to that in the previous report). The reason for many cases of intrahepatic bile duct formation in the Op group is believed to be because of the inclusion of many cases of type IV-A. Post-operative hepatolithiasis was not present in the Lap <1 y group, but it should be examined in the future in these patients.

The other issue with surgery for CC involves residual cysts in the pancreas, which are closely related to pancreatitis and pancreatic stones.[262728] Moreover, carcinoma arising in residual cysts has also been reported.[29] Based on the consensus that complete intrapancreatic cyst excision for CCs should be performed,[35] it could have been performed in all cases of the Lap groups. However, there were no cases of residual intrapancreatic bile ducts.

This study has a few limitations. First, the number of cases in this study was small, as it was limited to patients under 1 year of age. In particular, the number of cases in the laparotomy group was limited due to the retrospective nature of this study. The results of the statistical analyses had little significance owing to the small sample size; therefore, it is necessary to consider increasing the number of cases in the future. Second, this was a retrospective study, and the follow-up period of the Lap group was short. Long-term follow-up is necessary to observe the occurrence of hepatolithiasis as a post-operative complication.

CONCLUSION

Laparoscopic definitive surgery for CC in infants under 1 year of age is safe and feasible compared to open surgery in patients of the same age group and laparoscopic surgery in patients aged 3–5 years. Even semi-emergency laparoscopic surgery, which may be required due to any biliary symptoms, can also be performed safely and effectively in small infants.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.