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Pediatric Surgery International https://doi.org/10.1007/s00383-021-04964-5

REVIEW ARTICLE

Laparoscopic vs open portoenterostomy in biliary atresia: a systematic review and meta‑analysis

David Eugenio Hinojosa‑Gonzalez1  · Luis C. Bueno1 · Andres Roblesgil‑Medrano1 · Gustavo Salgado‑Garza1 · Sofia Hurtado‑Arellano1 · Juan S. Farias1 · Mauricio Torres‑Martinez1 · Jaime A. Escarcega‑Bordagaray1 · Marcelo Salan‑Gomez1 · Eduardo Flores‑Villalba1,2,3

Accepted: 30 June 2021 © The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021

AbstractHepatoportoenterostomy remains the cornerstone of treatment for biliary atresia. Current employed techniques include laparoscopy and open surgery. This study aims to determine if either method provides an advantage. Following PRISMA guidelines, a systematic review was conducted. Nineteen studies were included. Mean operative time 34.98 (95% CI 20.10, 49.85; p ≤ 0.00001) was longer in laparoscopic while bleeding volumes − 16.63 (95% CI − 23.39, − 9.86; p ≤ 0.00001) as well as the time to normal diet − 2.42 (95% CI − 4.51, − 0.32; p = 0.02) were lower in the laparoscopic group. No differences were observed in mean length of stay − 0.83. Similar complication, transfusions, postoperative cholangitis 0.97, and transplant free survival rates 1.00 (0.63, 1.60; p = 0.99) were seen between groups. Laparoscopic portoenterostomy provides advantages on operative time and bleeding as well as to normal diet when compared to open procedures. Both procedures showed no differences in length of stay, complications, cholangitis, and importantly, native liver survival. Level of evidence: III.

Keywords Biliary atresia · Portoenterostomy · Minimally invasive · Kasai

Introduction

Biliary atresia (BA) is a progressive disease characterized by fibrosis of the biliary tree, leading to obstruction and consequently cirrhosis. Usually presenting in the neona‑tal period, leads to death within the second year of age if untreated [1, 2]. Incidence ranges from ~ 5 to 10/100,000 live births, depending on the region, being highest in Asia and Pacific Region. BA’s physiopathology is not completely understood, but is believed to be the result of a multifactorial origin with a complex interplay of genetic, infective, inflam‑matory, and toxic factors. Subtypes can be associated with congenital malformations of morphogenic etiology, biliary

atresia splenic malformation syndrome (BASM) of genetic or epigenetic etiology, or cystic biliary atresia, among oth‑ers [3, 4].

Destruction and fibrosis of the biliary tree occurs within the first 3–6 weeks of birth, and leads to cholestasis, which typically presents as the clinical triad of conjugated jaun‑dice, choluria, and acholic stools with accompanying hepa‑tomegaly and may progress to liver failure and/or cirrho‑sis [1–3, 5]. Diagnosis of BA is a combination of clinical, laboratory, and imaging studies. Typically ultrasonography reveals a shrunken gallbladder and hyperechogenic hepatic hilum, commonly denominated as “triangular cord sign,”. Other diagnostic applications include cholangiography, liver biopsy, and hepatobiliary scintigraphy [1]. Several screening methods have been proposed and tried, but none have been sufficiently effective, sensible, specific, or feasible.

Mainstay treatment includes portoenterostomy, also known as Kasai procedure, named after Dr. Morio Kasai who first performed the procedure in 1952, and liver trans‑plantation. Portoenterostomy radically changed outcomes of BA, as the usual fatal prognosis improved an overall survival rate of 90% [6]. However, liver transplantation is reserved for cases in which Kasai surgery has failed or

* Eduardo Flores‑Villalba eduardofloresvillalba@tec.mx

1 Tecnológico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Batallon San Patricio, Monterrey, Nuevo León, Mexico

2 Tecnológico de Monterrey, Escuela de Ingeniería y Ciencias, Monterrey, Nuevo León, Mexico

3 Laboratorio Nacional de Manufactura Aditiva y Digital (MADIT), Apodaca, Nuevo León, Mexico

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when complications of BA are present [1, 3]. Early interven‑tion with the Kasai procedure will offer a good prognosis, although two‑thirds of patients who undergo this procedure will eventually require a liver transplant [7]. Although neces‑sary for survival, this procedure is highly morbid. The most common surgical complications are ascending cholangitis, which occurs in 30–50% of patients.

Minimally invasive surgery has evolved, and so have their advantages over open surgery, such as lower bleeding vol‑ume, shorter hospital stay, a shorter period of recovery, and surgical technique precision by experienced surgeons. The initial laparoscopic Kasai procedure was first performed by Esteves in 2002 [8]. While minimally invasive approaches are favorable in treating various other conditions, prior lit‑erature in the setting of biliary atresia showed that the Kasai procedure under an open approach remains the gold standard [9–11].

Methods

Search strategy and screening

Following the Preferred Instrument for Systematic Reviews and Meta‑Analysis (PRISMA), a systematic database search was performed in November 2020 with no limit on date search (Fig. 1) [12]. Studies comparing open versus lapa‑roscopic portoenterostomy as treatment for biliary atresia were identified through the search engines/databases Pub‑Med, Web of Science, and Google Scholar. The search was performed for studies that included in their Title or Abstract the following search terms: “Biliary Atresia”, “Portoenter‑ostomy”, “Kasai” and “Laparoscopic” and/or “Open”. No restrictions were applied to manuscript age and only manu‑scripts in either English or Spanish language were included. The identified manuscripts were further independently screened by two authors/reviewers (MTM, JEX) for pos‑sible inclusion, evidence grading, and data extraction. Any discrepancy between identified data was mediated by a third reviewer (DEHG). Additional articles identified through related articles were also screened.

Fig. 1 Displays the PRISMA flow chart for systematic review Records identified through

database searching (n = 305)

Scre

ening

Includ

edEligibility

Iden

tifica

tion Additional records identified

through other sources (n = 47)

Records after duplicates removed (n =314)

Records screened (n = 314)

Records excluded (n = 284)

Full-text articles assessed for eligibility

(n = 30)

Full-text articles excluded, with reasons

(n =11) 2 Meta-analysis

1 Review 5 Laparoscopic Only

3 Included non-BA only patients Studies included in

qualitative synthesis (n = 19)

Studies included in quantitative synthesis

(meta-analysis) (n = 19)

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Study inclusion

Included studies statistically compared relevant outcomes of patients grouped into either open or laparoscopic as surgical intervention for biliary atresia in humans. Reporting data on total bilirubin, operative time, intraoperative bleeding, trans‑fusions, length of hospital stay, time to a normal diet, time to drain removal, transplant‑free survival, and complications (including cholangitis) were included. General demographic data including patient age and weight was also included. No restrictions were applied for study type or patient age. Stud‑ies with possible patient cohort overlap of less than 50% of inclusion time period were kept, otherwise were discarded. Studies in languages other than english were screened for tables and abstract for data extraction. Only case reports and case series of fewer than 8 patients were excluded.

Data extraction

As previously mentioned, manuscripts were assessed inde‑pendently by two reviewers for inclusion and data extraction. Data relevant to this meta‑analysis besides authorship and year of publication were as follows: for operative parame‑ters, operative time and intraoperative bleeding were consid‑ered; for postoperative values, time to a normal diet, length of stay, transfusions, time to drain removal, total bilirubin, and complications (including cholangitis) were considered. General demographic data including patient age and weight was also included. Studies providing data in median and ranges were used to estimate mean and standard deviation using Wan’s method. [13].

Statistical analysis

Gathered data were analyzed using Review Manager V5.3 (Cochrane). Heterogeneity was measured using I2%, with studies obtaining values over 50% being considered het‑erogeneous and analyzed through random effects models, while studies with values under 50% were considered homo‑geneous and were analyzed through fixed‑effects models. Continuous data including patient length of stay, time to normal diet, time to drain removal, operative bleeding, operative time, total bilirubin, weight, and age were esti‑mated using Mean Difference with 95% confidence inter‑vals (CI). Dichotomous data such as complications (includ‑ing complications with cholangitis) and transfusions were reported using Odds Ratios (OR) with 95% CI. Studies were subgrouped into subsets according to the time period in which the study was performed as reported in methodol‑ogy and grouped intro prior to 2010 and after 2010. Studies with a wide range overlapping both timesets were grouped to the after 2010 cohort. Studies not describing analyzed time period were grouped according to its publication year.

Resulting values with associated p values < 0.05 were con‑sidered significant. HRs were estimated from Kaplan–Meier curves using Tierney’s method. [14].

Results

Overall

A total of 19 studies met inclusion criteria, totaling 1266 patients, out of which 590 underwent Laparoscopic proce‑dures and 676 underwent open surgery. Findings are sum‑marized in Tables 1 and 2.

Demographic/baseline characteristics

Age

A total of 16 studies described age, totaling 492 patients in the laparoscopic group and 535 patients in the open group. Meta Analysis of this data revealed a mean difference of − 4.39 (95% CI − 10.10, 1.32; p = 0.13), showing similar ages in the included cohorts allocated to each group. These findings are displayed in Fig. 2a.

Weight

A total of seven studies described weight, totaling 333 patients in the laparoscopic group and 264 patients in the open group. Meta Analysis of this data revealed a mean dif‑ference of − 0.15 (95% CI − 0.49, 0.18; p = 0.36, showing no differences in weight between patients allocated to each group. These findings are displayed in Fig. 2b.

Total bilirubin

A total of 10 studies described preoperative total bilirubin, totaling 213 patients in the laparoscopic group and 393 in the open group. Meta Analysis of this data revealed a mean difference of 0.90 (95% CI − 2.05, 3.85; p = 0.55), showing no differences in total bilirubin levels between patients allo‑cated to each group. These findings are displayed in Fig. 2c.

Operative parameters

Operative time

A total of 15 studies described operative time, totaling 535 patients in the laparoscopic group and 589 in the open group. Meta Analysis of this data revealed a mean difference of 34.98 (95% CI 20.10, 49.85; p ≤ 0.00001), concluding sig‑nificant decreased operative time in the open group. These findings are displayed in Fig. 3a. Subgroup analysis reveals

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Table 1 Summary of meta‑analysis

Outcomes # of included studies

Laparoscopic Open MD/OR*(95%CI) p value Heterogeneity

I2% p value

Demographic Age 16 492 535 − 4.39 (− 10.10, 1.32) 0.13 86 < 0.00001 Weight 7 333 264 − 0.15 (− 0.49, 0.18) 0.36 66 0.008

Preoperative parameters Total bilirubin 10 213 393 0.90 (− 2.05, 3.85) 0.55 91 < 0.00001

Operative parameters Operative time 14 509 547 35.28 (19.68, 50.88) < 0.00001 93 < 0.00001 Operative bleeding 9 220 407 − 16.63 (− 23.39, − 9.86) < 0.00001 95 < 0.00001 Transfusions 3 27 66 0.20 (0.03, 1.63) 0.13 78 0.01 Complications 6 256 265 2.33 (0.64, 8.48) 0.20 70 0.006

Postoperative parameters Length of hospital stay 5 107 231 − 0.83 (− 2.08, 0.42) 0.19 0 0.56 Time to normal diet 7 316 299 − 2.42 (− 4.51, − 0.32) 0.02 97 < 0.00001 Time to drain removal 3 59 84 0.48 (− 1.22, 2.18) 0.58 85 0.001 Postoperative cholangitis 11 413 409 0.97 (0.70, 1.32) 0.83 33 0.14 Jaundice clearance rate 14 499 525 1.04 (0.78, 1.38) 0.79 43 0.05 Transplant free survival (survival curve) 9 377 230 1.00 (0.63, 1.60) 0.99 57 0.02 Transplant free survival at 12–24 months 14 273 437 0.93 (0.67, 1.30) 0.68 51 0.01

Table 2 Summary of included studies

Author Year #Laparoscopic portoen‑terostomy patients

#Open portoenter‑ostomy patients

Type of study Survival curve maxi‑mum follow‑up time

NOS score

1 Xuelai [15] 2006 26 34 Retrospective2 Aspelund [16] 2007 5 24 Retrospective 53 Wong [17] 2008 9 63 Retrospective 64 Ure [18] 2011 12 28 Prospective 2 years 65 Chan [10] 2012 16 16 Retrospective 5 years 56 Oetzmann von

Sochaczewski [19]2012 8 11 Retrospective 5

7 Xu [20] 2012 44 47 Prospective8 Wada [21] 2014 12 11 Prospective 8 years 69 Murase [22] 2015 12 65 Retrospective 410 Nakamura [23] 2015 13 13 Prospective 611 Sun [24] 2015 44 47 Prospective 712 Chan [25] 2018 11 20 Retrospective 10 years 413 Huang [26] 2018 10 13 Retrospective 414 Yanan Li [27] 2018 49 40 Retrospective 8.3 years 415 Razumovskiy [28] 2019 45 24 Retrospective16 Murase [29] 2019 21 106 Retrospective 1 year 617 Sato [30] 2019 28 25 Retrospective 518 Shirota [31] 2019 30 46 Retrospective 419 Ji [32] 2020 195 43 Retrospective 10 years/4.1 years 5

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Fig. 2 Displays forest plot of meta‑analysis of the following variables: a age, b weight, c total bilirubin

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an increase in mean difference between groups during the studied time periods.

Operative bleeding

A total of nine studies described operative bleeding, totaling 220 patients in the laparoscopic group and 407 in the open group. Meta Analysis of this data revealed a mean differ‑ence of − 16.63 (95% CI − 23.39, − 9.86; p ≤ 0.00001), concluding significant decreased operative blood loss in the laparoscopic group. These findings are displayed in Fig. 3b. Subgroup analysis reveals significant differences in operative bleeding are mainly driven by studies performed after 2010.

Transfusions

A total of three studies described the need for transfusions, totaling 224 in the laparoscopic group and 174 in the open group. Meta Analysis of this data revealed an odds ratio of 0.20 (95% CI 0.03, 1.63; p = 0.13), concluding similar transfusion odd rates between procedures. These findings are displayed in Fig. 3c.

Complications

A total of six studies described complications, totaling 256 patients in the laparoscopic group and 265 in the open group. Meta Analysis of this data revealed an odds ratio of 2.33 (95% CI 0.64, 8.48; p = 0.20), concluding similar complica‑tion rates between procedures. These findings are displayed in Fig. 3d. Subgroup analysis reveals significant differences in complication rates were only present in studies performed prior to 2010.

Postoperative parameters

Length of stay

A total of five studies described length of stay, totaling 107 patients in the laparoscopic group and 231 patients in the open group. Meta Analysis of this data revealed a mean dif‑ference of − 0.83 (95% CI − 2.08, 0.42; p = 0.19). This sug‑gests patients undergo a similar length of hospital stay time after any surgical approach. These findings are displayed in Fig. 3e.

Fig. 3 Displays forest plot of meta‑analysis of the following variables: a operative time, b operative bleeding, c transfusions, and d complica‑tions, e length of stay, f time to normal diet

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Time to normal diet

A total of seven studies described the time of progression to a normal diet, totaling 316 patients in the laparoscopic group and 299 in the open group. Meta Analysis of this data revealed a mean difference of − 2.42 (95% CI − 4.51, − 0.32; p = 0.02), concluding a shorter time to normal diet in the laparoscopic approach group. These findings are displayed in Fig. 3f. Subgroup analysis reveals significant differences in time to normal diet are mainly driven by studies performed after 2010.

Time to drain removal

A total of three studies described time to drain removal, totaling 59 patients in the laparoscopic group and 84 in the open group. Meta Analysis of this data revealed a mean dif‑ference of 0.48 (95% CI − 1.22, 2.18 p = 0.58), conclud‑ing no difference in time to drain removal between groups. These findings are displayed in Fig. 4a.

Postoperative cholangitis

A total of 10 studies described postoperative complications with cholangitis, totaling 413 patients in the laparoscopic group and 409 in the open group. Meta Analysis of this data revealed an odds ratio of 0.97 (95% CI 0.70, 1.32; p = 0.83),

Fig. 4 Displays forest plot of meta‑analysis of the following variables: a time to drain removal, b postoperative cholangitis

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suggesting similar postoperative cholangitis rates in both procedures. These findings are displayed in Fig. 4b.

Jaundice clearance

Jaundice resolution within 6 months of intervention was described in 499 studies totalling 525 laparoscopic patients and 525 open patients. No differences were found in the odds of jaundice clearance OR 1.04 (0.78, 1.38) p = 0.079. These findings are displayed in Fig. 5a.

Transplant free survival

A total of nine studies described transplant free survival, totalling 377 patients in the laparoscopic group and 230 in the open group. Meta Analysis of this data revealed a hazard ratio of 1.00 (0.63, 1.60; p = 0.99), suggesting similar trans‑plant free survival rates in both procedures. These findings are displayed in Fig. 5b. Subgroup analysis reveals an inter‑est finding. Studies prior to 2010 had higher survival in open groups [HR 2.17 (1.22, 3.89) p = 0.009], while newer studies suggest the opposite [HR 0.62 (0.46, 0.84) p = 0.002].

In addition, 14 studies provided 12–24 postoperative patient transplant free survival for a total of 273 laparo‑scopic patients and 437 open patients. Analysis of this time‑frame revealed similar trends as the survival curve analy‑sis. Older studies favored survival in open procedures [OR 0.35 (0.20, 0.61) p = 0.0002], while newer studies favored survival in minimally invasive procedures [OR 0.93 (0.67, 1.30) p = 0.00001]. Overall, no differences in 12–24‑month transplant free survival are seen when pooling all studies together [OR 0.93 (0.67, 1.30) p = 0.68]. These findings are displayed in Fig. 5c.

Discussion

The high morbidity and mortality from the aggressive fibrous obliteration of bile ducts and its resulting liver dysfunction necessitates an early, effective interventions. Liver transplan‑tation poses logistical, medical and availability challenges, thus, due to its convenience and effectiveness, Kasai’s pro‑cedure has been considered the gold standard for decades [33]. Over the years, adaptations and implementations of new technology such as minimally invasive surgery and modifications to Kasai’s original technique have attempted to improve patient outcomes. MIS has featured widespread adoption in surgical procedures due to its decreased opera‑tive bleeding, length of stay, complications, and pain scores [34]. These advantages come at a cost of decreased dexterity of exteroception; however, most surgeons are able to over‑come these limitations with adequate training [35]. These advantages, however, have not been replicated to the same

degree of success in prior meta‑analysis of the laparoscopic Kasai procedures, in which no advantages were identified in bleeding, length of stay, or complications, with additional prolongation of operative time and decreased survival. These authors have advised against laparoscopic approaches, sug‑gesting caution, stemming from their findings [11, 36].

Some authors [18] theorized this phenomenon might be a result of steep learning curves and low‑case availability; however, other authors argue that both approaches suf‑fer from low case volume [25, 37]. Detrimental effects of prolonged pneumoperitoneum’s damage on liver‑cell and increased hepatic sensitivity have been proposed by Ure et al., as well as suggested by various animal models [18, 38]. Nakamura et al. [39], who identified pneumoperito‑neum flow as the detrimental factor, suggesting instead a 0.5–1.0 L/min flow and a pneumoperitoneum pressure of 8 mmHg for optimal results.

Prior authors concluded laparoscopic approaches pro‑vided no short‑term advantages and worse long‑term out‑comes, acknowledging limitations derived from a small number of available studies for analysis [11, 36]. This is contrasted with our own findings, in which laparoscopic approaches proved decreased operative blood loss, and time to a normal diet, with similar transfusion, complica‑tion, and cholangitis rates when compared to the stand‑ard open approaches. These advantages must be weighed against increased case‑length, which was shorter in open approaches. More importantly, our survival curve analysis revealed no differences in transplant‑free survival hazard ratios. These new findings possibly reflect increased expe‑rience, as trends in variables such as operative blood loss show more recent studies individual findings favor laparo‑scopic approaches.

These findings might also reflect modifications to the technique and attempted standardization of the laparoscopic approach by Li and Huang [26, 36]. The original proce‑dure entailed mobilization of the liver and portal identifi‑cation with extensive extrahepatic fibrotic remnants exci‑sion peripheral to where the portal vein enters the hepatic parenchyma followed creation of a conduit allowing hepatic drainage into the intestine through a Roux‑en‑Y loop [40]. Li’s own conclusion from their training analysis revealed possible benefits from improved anatomical exposure by the suspension of the liver edge and ligamentum teres hepatis, careful dissection of periportal fibrous tissue without cauter‑ization, adequate resection and, high‑resolution laparoscope [36]. Huang et al., found favorable outcomes when employ‑ing shallow dissections and sutures of the hepatic hilum, ligature devices for hemostasis, and modified roux limbs [26]. More recently, Yi Ji et al., published their comparison of modified laparoscopic technique to traditional laparo‑scopic and open. They found favorable results when limit‑ing dissection of the main trunk of the portal vein, hepatic

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artery, and their branches as well as choledochus within the hepatoduodenal ligament [32]. This is followed by hilar fibrous cone exploration, with proximal end severing above the level of the hepatic artery bifurcation and sparing of the small vessels of the fibrous cone stemming from the portal vein and hepatic artery [32]. With their approach, they found improved native liver survival in patients treated with lapa‑roscopic surgery when compared against an open approach. Whether the result of technical refinement, increased expe‑rience or both, subgroup analysis by year in which studies were performed reveals interesting insights. Notably, while laparoscopic Kasai remains a slower procedure than its open counterpart, significant reductions in blood loss were consistently achieved in more recent studies. This phenom‑enon is also seen to time to normal diet. Complication rates have also decreased in the laparoscopic group with time, as only older cohorts detected higher complications in laparo‑scopic groups. Most significantly; however, transplant free survival in newer cohorts favors laparoscopic procedures, as opposed to older studies that favored open procedures. Whether this important finding is exclusively attributable to laparoscopic interventions or confounded by improvements in care requires further high quality dedicated studies.

This review and analysis face various limitations, first, included studies are primarily retrospective, as no rand‑omized controlled trials have been conducted, the wide chronograph range of included studies presents another possible bias stemming from technical evolution. Included studies providing longer term outcomes on native liver sur‑vival had heterogeneous postoperative management; how‑ever, analysis of baseline characteristics such as age revealed the overall cohort of included patients was non‑different. In addition, another important limitation arises from high inter‑study heterogeneity was found in most comparisons, stemming from varying levels of performance and experi‑ence from publishing centers. Importantly, included studies themselves are small, thus necessitating further large‑quality studies.

Conclusion

Laparoscopic portoenterostomy provides advantages on operative time and bleeding as well as time to normal diet when compared to open procedures. Both procedures showed no differences in length of stay, complications, cholangitis, and importantly, native liver survival. However, trends from more recent studies suggest laparoscopic pro‑cedures have better rates of transplant free survival. Further adoption of modified laparoscopic techniques could provide additional benefits. High‑quality studies from higher volume centers are needed to confirm these findings.

Funding No funding was received for this study.

Declarations

Conflict of interest None to disclose.

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