Evaluation of the outcomes of biliary-enteric reconstruction in robotic radical resection of hilar cholangiocarcinoma: a single-centre propensity score matching analysis

doi:10.21203/rs.3.rs-3986740/v1

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Evaluation of the outcomes of biliary-enteric reconstruction in robotic radical resection of hilar cholangiocarcinoma: a single-centre propensity score matching analysis

https://doi.org/10.21203/rs.3.rs-3986740/v1

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Background

Although robotic radical resection for hilar cholangiocarcinoma(HCCA) has been reported in few cases in some large hepatobiliary centers, biliary-enteric reconstruction (BER) is still a critical step which restricts the success of the operation. This study aimed to evaluate the feasibility and quality of BER in robotic and laparoscopic radical resection of HCCA and propose technical recommendations.

Methods

A retrospective study was conducted on patients with HCCA who underwent minimally invasive radical resection at Zhejiang Provincial People’s Hospital from January 2016 to July 2023. A 1:2 propensity score matching (PSM), which is widely used to reduce selection bias, was performed to evaluate the surgical outcomes, especially BER-related data between robotic and laparoscopic surgery.

Results

46 HCCA patients were enrolled. After PSM at a ratio of 1:2, 10 and 20 patients were assigned to the robotic-assisted and laparoscopic groups, respectively. And the baseline characteristics of two groups were generally well balanced. The average time of liver resection in the robotic group was longer than that in the laparoscopic group( 139.5 ± 38.8 vs 108.1 ± 35.8, P = 0.036), but the former had less intraoperative blood loss(200(50–500) vs 310(100–850)), even though there was no statistical difference(P = 0.109). The biliary residuals number was 2.6 ± 1.3 and 2.7 ± 1.2(P = 0.795); the number of anastomoses were both 1.6 ± 0.7 in two groups(P = 0.965); the time of BER was 38.4 ± 13.6 and 59.1 ± 25.5 min(P = 0.024), 9.9 ± 2.8% and 15.4 ± 4.8% of the total operation time(P = 0.001). Although postoperative bile leakage incidence in laparoscopic group(40.0%)was higher than that in robotic group(10.0%), there was no significant difference between two groups(P = 0.204); 6.7 ± 4.4 and 12.1 ± 11.7 days for tube drawing(P = 0.019); anastomosis stenosis and calculus rate was 10.0% and 30.0% (P = 0.372), 0.0% and 15%(P = 0.532), respectively. Neither group had a hemorrhage or bile leakage-related death.

Conclusion

Robotic radical resection for HCCA may offer the comparable perioperative outcomes as conventional laparoscopic procedure, and tend to be associated with more advantages in terms of anastomosis time and quality, we are optimistic with its wide application in future with the improvement of surgical techniques and experience.

Biological sciences/Cancer

Health sciences/Gastroenterology

Health sciences/Oncology

Robotic

laparpscopic

hilar cholangiocarcinoma

biliary-enteric reconstruction

propensity score matching

Hilar cholangiocarcinoma(HCCA) is the most common malignant tumour of the bile duct^{[1, 2]} which with generally poor survival rate following resection^[3–5]. Radical resection has been recognized as the only curative treatment for this disease.Although some retrospective studies shown that laparoscopic radical resection of HCCA(LRRH) was safe and feasible which can achieve similar outcomes or even better than open surgery in lymph node dissection and intraoperative bleeding, which contribute to accelerate postoperative recovery for patients ^[6–8], the minimal invasiveness of LRRH remains controversial^[9–11]. In addition, laparoscopic approach has limited application in radical resection of HCCA because of the high technical requirements. Inherent disadvantages of laparoscopy make the BER as an important rate-limiting step in LRRH. Compared with traditional laparoscopy, robotic surgical system has a stable and high degree of freedom robotic arm and high-definition magnified 3D lens, allowing for flexible and precise surgical operations in narrow spaces ^{[12, 13]}. However, there is currently no single clinical study on the advantages and disadvantages of robotic surgery for BER in radical resection of HCCA. In response to these concerns, we performed a comparative study of BER, focusing on its time percentage and technical complexity in LRRH and RRRH, and the impact of BER on postoperative complications .

Patients’ Cohort and Data Collection

Data for a consecutive series of patients who underwent radical resection for HCCA, by either robotic or laparoscopic approach between January 2016 and July 2023 were retrieved from Zhejiang Provincial People’s Hospital from a prospectively collected database. Patients enrolled for minimally invasive resection in our institution comply with three principles. The first is to meet the resectability and radicality requirements of RRRH or LRRH as described in previous studies ^{[6, 14]}. Concretely, HCCA with distant or intrahepatic metastasis, peritoneal seeding, and para-aortic lymph node metastasis is considered unresectable. The second is the absence of hepatic artery (HA) or/and portal vein(PV) invasion, which means no vascular resection and reconstruction are required. Finally, the patient can tolerate pneumoperitoneum and prolonged anesthesia. The patients with coexistence of other malignancies were excluded. The flow chart is shown in Fig. 1.

Data was recorded by a standard case report form, the Bismuth–Corlette classification of the patient was determined by using the intraoperative finding and post-operative pathology. The outcomes measured including the preoperative biochemical parameter, operation time, liver resection time, intraoperative blood loss and transfusion, total number of lymph nodes examined (TNLE), margin status (R0/R1/R2), drainage duration, postoperative length of hospitalization, postoperative morbidity and mortality. The severity of the post-operative complication was evaluated by Clavien–Dindo(CD) classification^[15] and CD ≥ III were defined as serious complications. Data related to BER were recorded in detail to meet this study’s purpose. Emphasis was on the number of biliary residuals and number of anastomoses, suture method, and time consumption. Postoperative complications mainly focused on bile leakage, anastomotic stenosis, anastomotic calculus and BER-related death.

Preoperative Management

Ultrasonography, computed tomography(CT), magnetic resonance cholangiopancreatography (MRCP) and 3-D image reconstruction were routinely performed to evaluate the resectability of HCCA including the tumor size, the involvement of surrounding blood vessels, and the extent of longitudinal involvement. 640-CT scan was carried out for the future liver remnant (FLR) as well as to ensure at least 40% was preserved. The function of FLR was assessed by liver function test and indocyanine green(ICG) assay. For patients with elevated serum total bilirubin(TB) level (> 80 µmol/l), percutaneous trans-hepatic biliary drainage (PTBD) was performed prior to operation to relieve the obstruction of biliary tract.

Surgical Procedure

The surgical process for patients admitted to the laparoscopic group follows the previous description^[6]. All robotic-assisted procedures were performed using da Vinci Xi Surgical System (Intuitive Surgical, Inc., Sunnyvale, USA). In this study, we use the example of left hemihepatectomy to show anatomical schematic diagrams of RRRH. The patients undergoing robotic surgery were placed in the reverse Trendelenburg position and a five-port method was used and the position of trocars is shown in Fig. 2. The surgical procedures were described as follows:

⒜ Intraoperative ultrasound was routinely performed to determine and evaluate the potential intrahepatic metastasis. Subsequent to Kocher maneuver for duodenum mobilization, transection of the bile duct at the upper border of the pancreatic head were performed to determine if the margin is negative(Fig. 3).

⒝ The hepatoduodenal ligament was skeletonized to remove all soft tissues and lymph nodes starting from the common hepatic artery in a clockwise direction, including Groups 5, 7, 8, and12 lymph nodes, and the process followed the previous description^[16]; the common hepatic artery, proper hepatic artery, and portal vein were adequately isolated(Fig. 4).

⒞ The left hepatic artery and left portal vein was occluded and divided successively which followed by cholecystectomy. The right hepatic duct need be cut off at a soft point and the negative margin should be confirmed by frozen section pathology. The determination of liver section relies on the middle hepatic vein orientation that determined by intraoperative ultrasound and ICG fluorescence imaging, then the left lobes and caudate lobe were completely mobilized and transected in an en bloc manner(Fig. 5).

⒟ Lastly, the BER was performed using end-to-side anastomosis between segmental ducts and Roux-en-Y jejunal loop without any stent. Ductoplasty of intrahepatic bile ducts was performed if necessary before intrahepatic cholangiojejunostomy(Fig. 6). Drainage tubes were routinely placed close to the hepaticojejunostomy and the cutting face of the liver, respectively.

Postoperative Management

Blood tests and liver function tests were performed every 3 days after operation. The level of bilirubin in drainage fluid was measured. Bile leakage was defined according to the criteria proposed by International Study Group of Liver Surgery^[17]. Morbidity was classified according to the Clavien–Dindo classification. Drainage tubes were removed if contrast-enhanced CT did not show any fluid accumulation in peritoneal cavity. Those who cannot remove the drainage tube with continuous bile drainage should be kept for two months at least until the sinus tract forms firmly and clamped the tube for seven days. Then the drainage tube can be removed after the patient has no effusion identified by CT and no abdominal pain or fever.

PSM analysis

PSM, which has been widely used in the medical literature ^[18], was performed to minimize the bias between the robotic and laparoscopic groups in the study. In this study, potential factors associated with the intraoperative and postoperative outcomes after radical resection in HCCA were matched, included gender, age, body mass index (BMI), American Society of Anesthesiologists (ASA) classification, TB, indocyaninegreen retention at 15minutes(ICG R15), preoperative biliary drainage and reinfusion, tumor size, tumor stage, and Bismuth-Corlette classifications. The propensity score for each patient was calculated through logistic regression modeling and then patients were matched at a ratio of 1:2 by using the method of “nearest.” The baseline features of patients were adjusted to balance after matching.

Statistical Analysis

SPSS statistical software (IBM SPSS, Inc., Chicago, IL, version 27) and Graphpad Prism(version 9.5.1)were used for statistical analysis. Categorical variables which were presented as absolute numbers (percentage) were compared between groups by the χ2 test or Fisher’s exact test. Normally distributed continuous variables presented as mean ± standard deviation(SD) were compared between groups using Student’s t test. Continuous variables not following normal distribution are presented as medians with interquartile range (IQR) or content and were analyzed using the Mann-Whitney U test. P < 0.05 was considered to be statistically significant difference.

Ethical approval

Written informed consent was obtained from all enrolled patients. The study was approved by the Ethics Committee of Zhejiang Provincial People’s Hospital and followed the principle of declaration of Helsinki.

Baseline and Pathological Characteristics Before and After PSM

A total of 46 patients who underwent radical resection for HCCA were enrolled, including 10 patients treated with robotic-assisted resection and 36 patients treated with laparoscopic surgery. There was no patient in two groups was converted to laparotomy. The clinicopathological features of patients were summarized and compared (Table 1). There was no significant disparity between the RRRH and LRRH group, including gender, age, BMI, ASA classification, preoperative biliary drainage, bile reinfusion, ICG R15, Bismuth–Corlette classifications, tumor size, and T stage. However, the average of TB in RRRH group was lower than LRRH group(P=0.047). After PSM at a ratio of 1:2, 10 patients were assigned to the RRRH group and 20 patients were assigned to the LRRH group, and there was no significant difference between two groups in all data. All patients were treated with extrahepatic bile duct resection, regional lymphadenectomy, hemihepatectomy combined with caudate lobectomy and EBR, except for the patient of Bismuth type I who accepted extrahepatic bile duct resection only. All patients with T-Bil>80µmol/L underwent PTBD. A total of 28 patients in both groups did not experience bile reinfusion due to the resistance of the jejunal nutrient tube implement or patient rejection.

Intraoperative parameters and postoperative outcomes

Table 2 showed the perioperative outcomes of two groups after PSM. The surgery strategy for various Bismuth types of HCCA in our institution depends on the following principles. Bismuth type II and IIIb undergo left hemihepatectomy (LH) with caudate lobectomy (CL). Bismuth type IIIa undergoes right hemihepatectomy (RH) with CL. Bismuth type IV undergoes typical or extended LH or RH decided by the extent of tumor invasion to the left and right hepatic duct, residual liver volume, and ICG R15. Patients with FLR less than 40% received lobus quadratus resection (segment IVb+V) with CL. No significant difference of surgery type was observed between the two groups. Interestingly, although there was no significant difference in the total operation time between the two groups(P=0.931), the RRRH group's liver resection time was significantly longer than that of the LRRH group(139.5±38.8 vs 108.1±35.8, P=0.036), which may be related to the proficiency of the surgeon and the frequent replacement of hemostatic devices in the RRRH group. The RRRH group showed less intraoperative blood loss (200(50-500) vs 310(100-850)) which may caused by more delicate operation, but there was no significant difference(p=0.109). 6 patients in both groups didn’t received negative bile duct margin because extensive tumor invasion. Blood reinfusion, TNLE, resection margin, and the incidence of serve morbidity(CD≥III) were comparable between the groups. Mortality at 30 postoperative days and 90 postoperative days, as well as the postoperative days of hospital stay, did not differ significantly between the two groups.

Biliary-enteric reconstruction (BER) and relative complication

The details of outcomes of BER and relative complications were summarized in Table 3. Depending on different surgery types, the residuals range from 1 to 5, with the most residuals presented in lobus quadratus resection. The average number of the residuals in the RRRH and LRRH groups was 2.6±1.3 and 2.7±1.2, respectively (P=0.795). And the average diameter of residuals were comparable between the groups(P=0.138). In order to minimize the number of hepaticojejunostomy, cholangioplasty was usually performed on the adjacent bile duct stumps. Choledochojejunostomy ranges from 1 to 3, with a same mean of 1.6±0.7 in the both groups (P=0.965).

The suture method of hepaticojejunostomy was determined by the diameter of the residual bile duct. Very small bile ducts, such as with a diameter less than 1 mm ,was ligated directly. For intrahepatic bile duct residuals diameters less than 5 mm(or after cholangioplasty), end-to-side anastomoses were established through intermittent suture of anterior and posterior wall with 5-0 PDS. For the diameter from 5-8mm, the posterior wall was continuous sutured with 4-0 barded suture and the anterior wall was sutured intermittently with 5-0 PDS, respectively. And both the anterior and posterior wall were sutured continuously using 4-0 barbed suture for those with diameters above 8 mm. There was no statistical difference between the two groups in terms of anastomosis manner (P>0.999). The average time of BER in the RRRH and LRRH group was 38.4±13.6 and 59.1±25.5 min, respectively (P=0.024), which accounted for 9.9±2.8% and 15.4±4.8% of the total operation time in each group (P=0.001). These illustrated that the time consumption ratio is significantly higher in the LRRH group.

As one of the most common complications after EBR, there were 9 cases of postoperative bile leakage in two groups, one from the RRRH group with grade A, 8 cases from the LRRH group, including 3 grade A and 5 grade B, no grade C was observed. And only one patient with grade B caused local peritonitis due to the obstructed drainage which was cured by B-ultrasound guided percutaneous catheter drainage. Other patients were all cured by continuous abdominal drainage and without additional treatment. No patient with bile leakage received second surgery. Statistical analysis showed no difference of incidence of bile leakage in the two groups (p=0.204), and the mean days of tube drawing in RRRH groups was shorter than that in LRRH group(6.7±4.4 vs 12.1±11.7,P=0.019). There was 1 case of biliary-enteric anastomotic stenosis in RRRH group and 6 in LRRH group, these patients presented fever with delayed jaundice and confirmed by MRCP from 3 months to 2 years after surgery. Of those 6 cases in LRRH group, 3 cases combined with stone formation and were resolved by percutaneous transhepatic choledochoscopy (PTCS).

Radical resection of HCCA has long been praised as the most challenging procedure in biliary surgery, requiring the completion of extensive liver resection including caudate lobe resection, whole regional lymph node dissection, high bile-enteric anastomosis and even vascular resection and reconstruction. With the continuous progress of surgical theory technology and the rapid development of surgical instruments, LRRH has been carried out in some large hepatobiliary surgery centers, Xiong^[19] compared Laparoscopic and open group, displaying that intraoperative bleeding volume(P=0.426), the number of lymph nodes retrieved(P=0.706), bile leakage (P=0.781), and liver failure(P>0.99) were similar in the two groups. Ma^[20] found no significant differences of the surgical outcomes between the open and laparoscopic surgery groups, but the overall survival rate and disease-free survival rate were significantly higher in open group (P=0.0057, P=0.043). Zhang^[6] reported that laparoscopic radical resection of HCCA was significantly better than the traditional open surgery in intraoperative bleeding and postoperative hospital stay, with no statistical difference in postoperative long-term survival. However, due to the inherent insurmountable shortcomings of laparoscopy, such as inflexible operation, poor device mobility, fulcrum effect, anti-ergonomics and long learning curve^[21,22], limited its wide application in HCCA.

On the contrary, the robotic surgery system can overcome the disadvantages of traditional laparoscopy in complex anatomical and anastomotic surgeries, and may have potential advantages in minimally invasive surgery for HCCA. Robotic radical resection for HCCA was first reported by Giulianotti ^[23] in 2010. In 2012, Liu^[24] reported a series of robotic surgeries for HCCA, only three patients underwent hepatectomy, and the others were treated with local excision in combination with biliary reconstruction. However, there is still controversy about the application of robots in HCCA. Xu^[25]reported 10 cases of robotic surgery for HCCA, the patients had a longer operative duration and larger blood loss volume, and the authors concluded that the practice of robotic surgery for HCCA was not supported by their results. Huang^[26] evaluated the short-term outcomes of robotic-assisted radical resection for HCCA, showed that the robotic group tended to have a lower intraoperative blood loss ( 125 vs 350 mL, P=0.067), blood transfusion rates (30.0% vs 70.0%, P=0.056), and post-operative overall morbidities (30.0% vs 70.0%, P=0.056) than the open group, even though the differences were not statistically significant. Cou^[27] compared the robotic and open surgery, revealed that there was no difference whatever in the short-term or long-term effects after resection of HCCA between two groups. The consistent results were obtained in this study, the RRRH group showed less intraoperative blood loss ((200(50-500)vs310(100-850),P=0.109), postoperative hospital stay(9.3±2.2 vs 11.1±3.8, P=0.166), similar total operation time and complications compared with the LRRH group. Accordingly, a robotic approach is technically achievable in selected patients, and enthusiasm for robotic procedures in HCCA should be encouraged.

The very important advantage of the robotic surgical system in the radical resection of HCCA was mainly reflected in the high biliary tract reconstruction. The complex Roux-en-Y hepaticojejunostomy was always considered as the very difficult and important rate-limiting step in LRRH . First, the obstruction caused by the hilar liver tumor generally made the tube wall of the distal dilated bile duct thin, and tissue of bile duct wall was often fragile due to impaired liver function and patient nutritional status and inflammatory response. Limited suture angle caused by the straight instruments of laparoscopy, which always lead to anastomotic tear in the reconstruct process because of the uncontrollable suture strength; Second, Although the negative bile duct margin could finally be confirmed by rapid intraoperative pathological examination, it was still difficult to determine the high bile duct disconnection point during surgery. Whether the texture of the bile duct was soft can be judged approximately by the tactile feedback of the hand in open surgery, which was absent in laparoscopic surgery and always lead the surgeon to choose higher bile ducts unconsciously for negative margin, resulting in thinner bile ducts at the anastomotic site objectively; In addition, a large majority of patients had two or even more anastomoses in the radical resection of HCCA, the previously finished anastomosis occupied the space for the subsequent anastomosis, which often lead to the subsequent anastomosis being more difficult and increased the time and inaccuracy of the anastomosis. So it was still difficult to overcome the inherent angle defects of laparoscopy to achieve satisfactory anastomosis even for doctors with rich surgical experience and proficient suture techniques, which may lead to postoperative biliary fistula, anastomotic stenosis, and even other serious complications. Liu^[28] compared BER in laparoscopic and laparotomy radical resection of HCCA, one significant discrepancy is the anastomosis time (65.67±21.53 vs 42.5±19.77 min, P<0.05)and time consumption ratio of BER(15.08±3.64% vs 11.76±2.54%, P<0.05) in laparoscopic group is longer than in laparotomy group, which mainly stems from the complexity of the BER in laparoscopic surgery. However, in a systematic review, Guerra^[29] concluded that robotic surgery had become the trend of treatment for the surgery of the biliary tract in selected centres. The benefits of the robotic technology accelerated this transformation. Procedures (eg, hepaticojejunostomy) which required microanastomosis and extreme accuracy were the best indications for the application of the robotic approach. Besides, the robotic surgical system can ensure the surgeon in a sitting position and comfortable suture state, improving the operation accuracy subjectively, which is conducive to safe and reliable biliary reconstruction. Our research confirmed this conclusion, in our study, the average time of BER in the RRRH and LRRH group was 38.4±13.6 and 59.1±25.5 min, respectively (P=0.024), which accounted for 9.9±2.8% and 15.4±4.8% of the total operation time in each group (P=0.001).

There were a limit number of researches about hepaticojejunostomy with Roux-en-Y reconstruction in robotic approach^[28,30,31]. Regarding the method of biliary intestinal suture in study, intermittent suture and continuous suture or a combination of two methods would be choose according to the diameter of the bile duct and the thickness of the bile duct wall. For bile ducts with a diameter less than 5mm, it appropriate to use intermittent suture on both the anterior and posterior walls, which can prevent tearing and postoperative stenosis effectively; When diameter greater than 8mm, continuous suture had obvious advantage on suturing speed and economical surgical operation time; And the combination of intermittent and continuous suture was suitable for bile ducts with a diameter form 5 to 8mm. Continuous suture can be used for thick bile duct walls, while intermittent suture was suitable for the opposite. This study displayed that the incidence of biliary fistula(10.0% vs 40.0%,P=0.204), anastomotic stenosis(10.0% vs 30.0%,P=0.372), and stone formation(0.0% vs 10.0%,P=0.532) in the RRRH group was lower than that in the LRRH group, indicating that the robotic surgery was better in terms of the quality of biliary-enteric anastomosis and had a lower incidence of long-term complications, which is attributed to the more refined robotic suturing.

Although the application prospects of robotic surgery in HCCA were affirmed, data on the long-term outcomes of RRRH were still lacking. A previous study reported that the median tumor-free survival of HCCA patients treated with robot-assisted radical resection was 15.5 months (range, 6-60 months) ^[25]. However, most studies on robotic-assisted radical resection of HCCA only analysed the short-term outcomes ^{[14, 32]}. Therefore, more large randomized controlled trials are still needed to evaluate its long-term efficacy.

To our knowledge, this is the only study comparing BER related results in robotic and laparoscopic surgery of HCCA. However, some limitations must be noted. First, this study was a single-center retrospective study with a relatively small sample size, which may lead to biased results. Second, due to the late start of the RRRH in our center, data on long-term efficacy were deficient. The effectiveness of RRRH needs to be further explored by large prospective multicenter trials.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

The study was supported by the Natural Science Foundation of Zhejiang Province [LY21H160050]; the Zhejiang Medical and Health Department Project [2023KY487]; and the Zhejiang Traditional Chinese Medicine Science and Technology Project

[2020ZA014,2022ZB042]

The authors declare no conflicts of interest.

Author contributions

Liu Jie and Dou Changwei wrote the main manuscript text, Chen Jian and Lu Yi prepared figures 1-6, Liang Lei and Wei Fangqiang prepared tables 1-3, Zhang Chengwu provide technical support and guidance. All authors contributed to the article and approved the submitted version.

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Tables 1-3 are available in the Supplementary Files section.

No competing interests reported.

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Evaluation of the outcomes of biliary-enteric reconstruction in robotic radical resection of hilar cholangiocarcinoma: a single-centre propensity score matching analysis

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Figures

Introduction

Material and Method

Patients’ Cohort and Data Collection

Preoperative Management

Surgical Procedure

Postoperative Management

PSM analysis

Statistical Analysis

Results

Discussion

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1