Reconsideration of Laparoscopic Kasai Operation for Biliary Atresia

Abstract

Introduction:

Minimal invasive surgery for all kinds of surgical diseases had been practiced for years. The laparoscopic Kasai operation is one of the most challenging procedures and remains controversial for treating biliary atresia (BA).

Purpose:

This work presented the initial experience of our Institute and compared the outcomes of open and laparoscopic Kasai operations for BA.

Materials and Methods:

Patients 18 years old and younger, and were operated in our Institute for BA from January 2011 to August 2017, were included in this study. General and operative data and outcomes from open and laparoscopic groups were retrospectively collected and analyzed.

Results:

A total of 23 patients (13 for conventional open operation and 10 for the laparoscopic procedure) received Kasai portoenterostomy. The mean operative age and body weight in the open versus laparoscopic groups were 57.15 ± 20.14 days old and 4.03 ± 0.69 kg versus 57.70 ± 43.06 days old and 4.49 ± 1.48 kg, respectively, and no statistical difference was observed. The mean operative times were 209.62 ± 60.40 and 293.50 ± 39.09 minutes in the open and laparoscopic groups, respectively. The mean follow-up durations were 54.62 ± 22.00 and 23.30 ± 11.87 months for the open and laparoscopic patients, correspondingly. No statistically significant differences were observed for hospital stay and outcomes (including early jaundice clearance rate, episodes of cholangitis, and 2-year native liver survival rate) between the open and the laparoscopic Kasai operations.

Conclusion:

Experienced pediatric laparoscopic surgeons may reconsider the laparoscopic Kasai operation for application to BA treatment.

Introduction

Biliary atresia (BA) is a disease characterized by progressive obliteration and inflammation of extrahepatic bile ducts; the estimated highest incidence recorded was 0.86–1.51 per 10,000 live births in East Asian countries, including Japan and Taiwan.¹ Early diagnosis and prompt surgical intervention with the standard procedure, that is, Kasai portoenterostomy, was attempted to improve outcomes, but approximately two-thirds or even more of the patients require liver transplantation.^1–3

Although minimally invasive surgery is currently popular even for children, laparoscopic Kasai operation (first presented by Esteves in 2002)⁴ is one of the most challenging procedure and remains controversial for treating BA. The laparoscopic Kasai operation attained unfavorable results with lower rates of early jaundice clearance (0%–50% vs. 62%–80% in open surgery), lower native liver survival (NLS) rates (22%–50% vs. 50%–81% in open surgery), and early liver transplantation within 1 year after the Kasai operation (66% vs. 24% in open surgery) in several studies^3,5–9 than the conventional open surgery. Furthermore, no evidence shows that the laparoscopic Kasai operation may prevent adhesions and facilitate subsequent liver transplantation.^5,10 By contrast, the laparoscopic Kasai operation obtained encouraging outcomes with higher jaundice clearance (73%–100% vs. 46%–52% in open surgery) and NLS rates (52%–83% vs. 23%–45% in open surgery) than open Kasai operation,^11–16 even in patients receiving laparoscopic revision Kasai operation for treating BA.¹⁷

In Taiwan, Lin et al. reported that a significant decrease in the annual incidence of BA was observed after introducing rotavirus vaccination.¹⁸ Improved outcomes with a 5-year NLS rate of up to 53.7%–64.9% were observed after the national implementation of the infant stool card screening program, thereby enhancing early referral to surgery since 2004,^19–22 but no publication exists for the laparoscopic Kasai operation presently. This work presented the initial experience of our Institute and compared the outcomes of the open and laparoscopic Kasai operations for BA in the recent 5 years.

Methods

A retrospective study of patients who underwent the Kasai operation in our Institute to treat BA was performed from January 2011 to December 2015. The age, gender, and body weight (BW) of the patients and serum bilirubin and liver enzyme levels before and after the operation were reviewed. Early jaundice clearance was defined as serum total bilirubin level less than 2 mg/dL within 1 month after the Kasai operation. The operative complications and frequency of cholangitis episodes were reviewed. The 2-year NLS rate and the requirement for liver transplantation were recorded. Ethical approval was obtained from our institutional review board.

The Kasai operation was performed either in the open or laparoscopic group under general anesthesia as the procedure prescribed by Kasai with extended dissection of porta hepatis and wide portoenterostomy anastomosis with Roux loop.^15,23,24 In the open group, laparotomy was performed through a transverse upper abdominal incision, and the procedure was performed similar to the patient in the following descriptions for the laparoscopic group.

In the laparoscopic group, the patient was positioned across the table (Fig. 1A), the surgeon at the feet of the patient, the assistant with the camera on the left, and the scrubbing nurse at the right. A 5 mm 30° laparoscope (KARL STORZ Endoscopy Taiwan Ltd.) was inserted through a transumbilical incision by using the open Hasson technique. The peritoneal cavity was insufflated with CO₂ at a pressure of 8–10 mm Hg and flow of 3–4 L/min. Two additional 3 mm or 5 mm ports were placed on the right subcostal and left upper quadrant for both hands of the surgeon, and the other port was placed between the umbilical and left upper quadrant ports for the right hand of the assistant to expose the porta hepatis. (Fig. 1B) A percutaneous stay-suture was also used to improve exposure by snaring the falciform ligament to the abdominal wall below the xyphoid process. Proximal jejunum at approximately 15 cm distal to the Treitz ligament was identified and exteriorized through the transumbilical wound after the wide dissection of porta hepatis with excision of the fibrotic band was completed. The length of the Roux limb was approximately 30–40 cm, and jejunojejunostomy was performed extracorporeally. Finally, antimesenteric enterotomy, approximately 1 cm in length, was built near the closed end of the Roux limb, and all returned to the peritoneal cavity. The Roux limb traversed a retrocolic window to the porta hepatis without tension. Portoenterostomy was performed with interrupted 5/O vicryl sutures.

FIG. 1.

(A) The position of the patient on the operative table and (B) the trocar design.

Statistical analysis was accomplished by a t test for the continuous data and Fisher's exact test and univariate relative risk analysis for comparing categorical data. P < .05 was considered statistically significant.

Results

A total of 23 patients (13 for open Kasai operation and 10 for the laparoscopic procedure) were included. Two patients in the laparoscopic group had type I BA, the other 21 patients had type III BA, and all were nonsyndromic. The age, gender, and BW of the patients and their preoperative serum total and direct bilirubin, γ-glutamyl transferase, alanine aminotransferase, and aspartate aminotransferase levels are summarized in Table 1, and no statistical difference was observed. In the open group, two patients underwent revision operation without exploring porta hepatis (adding 23 and 66 days before the true Kasai operation due to the first operation performed at other hospital), and one 110 day-old patient initially planned to undergo liver transplantation because of severe cirrhosis. In the laparoscopic group, two patients with type I BA were earlier detected by prenatal ultrasound with an extrahepatic cyst and nonicteric appearance (preoperative serum total bilirubin level 1.6 mg/dL), and the data without these two type I BA patients (only type III BA) are listed in the lower row of the laparoscopic group in Tables 1 –4.

Table 1.

General Data and Preoperative Laboratory Data of the Patients

		Laparoscopic (all)
	Open	Laparoscopic (type III)	P value
Patient No.	13	10
Patient No.	13	8
Redo surgery No. (prior surgery at other hospital)	2	1	1.000
Redo surgery No. (prior surgery at other hospital)	2	2	1.000
Sex	8F/5M	4F/4M	.673
Sex	8F/5M	6F/4M	1.000
Age (day old)	57.15 ± 20.14 (28–90)	67.75 ± 42.50 (18–139)	.447
Age (day old)	57.15 ± 20.14 (28–90)	57.70 ± 43.06 (19–139)	.968
Symptom duration (before op., day)	29.62 ± 17.35 (10–63)	37.14 ± 40.82 (6–119)	.567
Symptom duration (before op., day)	29.62 ± 17.35 (10–63)	32.44 ± 36.56 (6–119)	.809
BW (kg)	4.03 ± 0.69 (2.28–5.13)	4.90 ± 1.33 (2.87–6.54)	.060
BW (kg)	4.03 ± 0.69 (2.28–5.13)	4.49 ± 1.48 (2.42–6.54)	.330
T-bilirubin (mg/dL)	7.84 ± 2.55 (5.1–12.4)	10.09 ± 5.78 (4.2–23.4)	.232
T-bilirubin (mg/dL)	7.84 ± 2.55 (5.1–12.4)	10.75 ± 5.30 (4.2–23.4)	.093
D-bilirubin (mg/dL)	4.42 ± 1.53 (2.5–7.1)	5.34 ± 3.22 (1.9–12.8)	.388
D-bilirubin (mg/dL)	4.42 ± 1.53 (2.5–7.1)	4.59 ± 3.25 (1.6–12.8)	.871
γ-GT (U/L)	753.85 ± 622.41 (142–2376)	849.75 ± 296.70 (313–1131)	.690
γ-GT (U/L)	753.85 ± 622.41 (142–2376)	898.10 ± 331.95 (313–1467)	.515
AST (U/L)	160.77 ± 90.09 (65–426)	202.13 ± 128.15 (42–346)	.395
AST (U/L)	160.77 ± 90.09 (65–426)	168.70 ± 133.21 (29–346)	.866
ALT (U/L)	116.31 ± 56.64 (41–225)	158.25 ± 125.45 (17–356)	.305
ALT (U/L)	116.31 ± 56.64 (41–225)	130.80 ± 124.86 (17–356)	.713

AST (U/L), aspartate transaminase (normal range 8–38 U/L); AST (U/L), aspartate transaminase (normal range 8–38 U/L); BW, body weight, F, female; γ-GT (U/L), γ-glutamyltransferase (normal range 4–63 U/L); M, male.

Table 2.

Perioperative Data of the Patients in Open and Laparoscopic Groups

		Laparoscopic (all)
	Open	Laparoscopic (type III)	P value
Operative time (minutes)	209.62 ± 60.40 (150–380)	285.00 ± 38.82 (240–360)	.005
Operative time (minutes)	209.62 ± 60.40 (150–380)	293.50 ± 39.09 (240–360)	.001
Blood loss (mL/kg)	4.36 ± 6.92 (0–26.4)	4.85 ± 5.25 (0–15.3)	.866
Blood loss (mL/kg)	4.36 ± 6.92 (0–26.4)	4.44 ± 4.75 (0–15.3)	.973
Blood transfusion (mL/kg)	2.03 ± 7.32 (0–26.4)	3.56 ± 5.63 (0–15.3)	.620
Blood transfusion (mL/kg)	2.03 ± 7.32 (0–26.4)	2.85 ± 5.19 (0–15.3)	.768
Days to start oral feeding	2.31 ± 0.48 (2–3)	3.88 ± 1.36 (2–6)	.001
Days to start oral feeding	2.31 ± 0.48 (2–3)	3.80 ± 1.23 (2–6)	.0006
ICU stay rate.	15.4% (2/13)	87.5% (7/8)	.002
ICU stay rate.	15.4% (2/13)	80% (8/10)	.003
Days to remove drainage tube	5.31 ± 0.75 (4–7)	6.00 ± 1.51 (4–8)	.176
Days to remove drainage tube	5.31 ± 0.75 (4–7)	5.90 ± 1.37 (4–8)	.199
Hospital stay (day)	14.62 ± 9.40 (6–34)	18.00 ± 6.35 (10–29)	.382
Hospital stay (day)	14.62 ± 9.40 (6–34)	20.20 ± 10.82 (10–46)	.200
Perioperative complication rate	15.4% (2^*/13)	25% (2/8)	.618
Perioperative complication rate	15.4% (2^*/13)	30% (3^**/10)	.618
Diameter of bile duct of porta hepatis (μm)	273.64 ± 224.87 (21.3–800)	307.88 ± 297.53 (75–938)	.768
Diameter of bile duct of porta hepatis (μm)	273.64 ± 224.87 (21.3–800)	326.30 ± 281.51 (75–938)	.623

In open surgery group: one with intestinal obstruction requiring surgery, and one with gastrointestinal bleeding.

In laparoscopic surgery group: one with intestinal obstruction requiring surgery, one with internal bleeding requiring surgery, and one with Y-anastomotic leak requiring surgery.

Conversion from laparoscopic to open surgery: one case due to bleeding (blood loss 15.3 mL/kg).

ICU, intensive care unit.

Table 3.

Outcomes of the Patients Receiving Open and Laparoscopic Kasai Operations

		Laparoscopic (all)
	Open	Laparoscopic (type III)	P value
Follow-up duration (month)	54.62 ± 22.00 (5–73)	20.38 ± 10.88 (7–41)	.0006
Follow-up duration (month)	54.62 ± 22.00 (5–73)	23.30 ± 11.87 (7–42)	.0006
Early jaundice clearance rate (one month after Kasai operation)	30.8% (4/13)	50% (4/8)	.646
	30.8% (4/13)	50% (5/10)	.417
Jaundice-free rate	69.2% (9/13)	62.5% (5/8)	1.000
Jaundice-free rate	69.2% (9/13)	70% (7/10)	1.000
Days to being jaundice free	35.30 ± 24.93 (17–100)	46.67 ± 42.65 (18–128)	.508
Days to being jaundice free	35.30 ± 24.93 (17–100)	40.38 ± 38.22 (12–128)	.738
Postoperative cholangitis rate (pt. no.)	69.2% (9/13)	75% (6/8)	1.000
Postoperative cholangitis rate (pt. no.)	69.2% (9/13)	70% (7/10)	1.000
Liver transplantation rate (pt. no.)	23.1% (3/13)	37.5% (3/8)	.631
Liver transplantation rate (pt. no.)	23.1% (3/13)	30% (3/10)	1.000
Interval to liver transplantation (month)	7.67 ± 4.16 (3–11)	5.33 ± 2.52 (3–8)	.453
Interval to liver transplantation (month)	7.67 ± 4.16 (3–11)	5.33 ± 2.52 (3–8)	.453
2-year native liver survival rate	69.2%	62.5%	1.000
2-year native liver survival rate	69.2%	70.0%	1.000

Table 4.

The Results of Univariate Relative Risk Analysis for Failure of Being Jaundice Free (Serum Total Bilirubin Level Less Than 2 mg/dL) Over 6 months After the Kasai Operation

	Univariate analysis
	RR (95% CI) - all
Variables	RR (95% CI) - type III	P value
Gender, male	0.53 (0.132–2.149)	.377
Gender, male	0.62 (0.152–2.548)	.510
Operative age >60 days	1.22 (0.363–4.089)	.749
Operative age >60 days	1.41 (0.412–4.795)	.586
Laparoscopic surgery	1.22 (0.363–4.089)	.749
Laparoscopic surgery	0.98 (0.280–3.401)	.968
Delayed jaundice clearance (>30 days)	1.54 (0.386–6.135)	.542
Delayed jaundice clearance (>30 days)	0.62 (0.152–2.548)	.510
Persistence of elevated liver enzymes	11.54 (0.744–178.962)	.008
Persistence of elevated liver enzymes	13.85 (0.882–217.271)	.061
Repeated cholangitis	3.00 (0.443–20.315)	.260
Repeated cholangitis	2.63 (0.384–17.936)	.325
Smaller hilum bile duct size (<200 μm)	1.00 (0.295–3.395)	1.000
Smaller hilum bile duct size (<200 μm)	1.17 (0.337–4.035)	.808

RR, risk ratio; CI, confidence interval.

The operative duration, intraoperative estimated blood loss, operative complications, postoperative hospital stay, and mean follow-up duration are listed in Table 2. The mean operative time in the laparoscopic group (293.50 ± 39.09 minutes) is longer than the open group (209.62 ± 60.40 minutes). The actual CO₂ insufflation time in the laparoscopic group was about 200 minutes, which is consistent with other series (126–546 minutes; mean = 253 minutes; total 134 patients).⁸ A prolonged interval to start oral feeding and high ICU stay rate in the laparoscopic group may be attributed to delayed extubation in the routine postoperative care for neonatal laparoscopic surgery in our institute. No statistically significant difference was observed for the operative complications between the open (one patient with intestinal obstruction underwent relaparotomy and another patient with gastrointestinal bleeding was resolved after medical treatment) and laparoscopic groups (one patient with jejunojejunostomy leak underwent laparotomy).

The outcomes, including early jaundice clearance within 1 month after the Kasai operation, interval to being jaundice free after the Kasai operation, frequency of cholangitis episodes within 1 year after the operation, 2-year NLS rate, and patient number with liver transplantation, are presented in Table 3. All patients survived during the follow-up period, except for one patient in the open group who died of child abuse 5 months after the Kasai operation. The mean follow-up duration was longer in the open group (59.54 ± 22.83 months) than the laparoscopic group (29.4 ± 12.05 months) because the laparoscopic Kasai operation had been performed in our Institute since 2014. No statistically significant differences were observed for hospital stay and outcomes (including early jaundice clearance rate, days to being jaundice free after the Kasai operation, episodes of cholangitis, and 2-year NLS rate) between the open and laparoscopic Kasai operations.

Table 4 shows the results of univariate relative risk analysis for the failure of being jaundice free, which is defined as the serum total bilirubin level >2 mg/dL at 6 months after the Kasai operation. The operative age of more than 60 days, persistence of elevated liver enzymes (especially high preoperative total bilirubin level), and delayed jaundice clearance (>30 days) indicate high risk ratios. Only delayed jaundice clearance exhibited statistical significance, and laparoscopic surgery is obviously not a risk factor.

Discussion

The NLS rate at 1–3 years ranged from 20% to 75%, at 10 years from 24% to 52%, and at 20 years from only 14% to 23%, although liver transplantation may increase the overall survival rate of BA patients by more than 90%.^1,24–27 The most important issues in BA patients are still early detection and the Kasai operation, attempting to achieve improved outcomes.^1,19,24 In this study, the operative age >60 days old had a relatively high risk for the short-term outcome. The factors that influence long-term outcomes will be evaluated by collecting further clinical data.

The laparoscopic treatment of BA may potentially be minimize invasive surgery, including the avoidance of muscle splitting incision, decreased pain, improved cosmetics, improved visualization by magnification, and minimal intra-abdominal adhesions.^2,11,12,27 The magnification of the hepatic hilum offered a clear vision of the minimal remnants of the right and left hepatic ducts (Fig. 2), which may be unobserved in the conventional surgery, and a precise control of bleeders with minimal damage of microscale bile ducts.^13,15,16 BA should not be treated by laparoscopic surgery because low jaundice clearance rate, low native survival rate, and early failure of the Kasai operation were reported in many articles, and the International Pediatric Endosurgery Group abandoned laparoscopic portoenterostomy in 2007.^2–7,10 A limited range of motions for laparoscopic instruments, thermal injury of small bile ducts, and temporary pneumatic pressure for possible liver parenchyma damage may be attributed to unfavorable results.^1–6,9 However, encouraging outcomes were achieved in the series with large patient volume and laparoscopic-modified portoenterostomy technique with shallow dissection and sutures of hepatic hilum using ligature device for hemostasis and customized Roux limb.^13–16 In this study, the laparoscopic group had an outcome similar to the open group. The poor outcome in several studies may be related to the learning curve for the complex laparoscopic biliary surgery, variability of surgical techniques, including hepatic hilar dissection and suturing, or even inconsistency of postoperative steroid therapy.^{16,17,28–30}

FIG. 2.

(A) Under the laparoscopic vision, the small remnants of right and left hepatic ducts (arrows) over the hepatic hilum were magnified and identified. (B) Little of yellow bile (arrows) drained out from the small right and (C) left hepatic duct after the fibrotic band was transected.

In conclusion, experienced pediatric laparoscopic surgeons may reconsider the laparoscopic Kasai operation for application to BA treatment, and this procedure may be reevaluated by additional clinical experiences.

Footnotes

Acknowledgment

This work was supported by Taichung Veterans General Hospital (Project numbers TCVGH-1055401C and TCVGH-1065401C).

Disclosure Statement

The authors disclose no financial or nonfinancial conflicts of interest.

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