Application of Robot-assisted Pancreaticobiliary Junction Resection in Benign Duodenal Tumors

Summary

The current protocol delineates the use of robot-assisted pancreaticobiliary junction resection for the surgical management of benign duodenal tumors. This approach provides an effective solution for treating these tumors while minimizing duodenal loss and reducing associated complications.

Abstract

Robot-assisted pancreaticobiliary junction resection is a surgical technique employed to treat benign duodenal tumors. The procedure involves several key steps: making a longitudinal incision in the duodenum, excising the tumor at the pancreaticobiliary junction, inserting a biliary stent, connecting the biliary and duodenal mucosa, and suturing the duodenal incision during phase I. The robotic system enhances visibility, facilitates precise operations, minimizes duodenal traction injuries to the duodenum and surgical trauma, ensures accurate suture and fixation of bile duct stents, connects the bile duct and duodenal mucosa and reduces postoperative recovery time. Given the complexity of the operation and the associated risk of postoperative duodenal fistula, a thorough preoperative evaluation and meticulous perioperative preparation are crucial. Prior to the procedure, a comprehensive assessment was conducted, integrating the patient's medical history, family history, serological tests, and imaging studies. Special emphasis was placed on determining the benign or malignant nature of the tumor and evaluating the status of the duodenal artery blood supply network to ascertain the feasibility and efficacy of the surgery. During the operation, efforts were made to minimize duodenal trauma and avoid compromising the duodenal artery blood supply network. Additionally, the use of bile duct stents was considered essential to prevent biliary strictures, facilitate bile discharge, and mitigate biliary complications. Postoperatively, real-time monitoring of amylase and jaundice indicators in drainage fluid informed the timely removal of drainage tubes in accordance with the enhanced recovery after surgery (ERAS) protocol. Subsequent follow-up indicated a successful recovery, characterized by a notable reduction in preoperative abdominal pain, the absence of long-term complications, and no evidence of tumor recurrence. Consequently, robot-assisted pancreaticobiliary junction resection demonstrates a safe and effective surgical approach for the treatment of benign duodenal tumors.

Introduction

Duodenal tumors are relatively rare, exhibiting a low incidence, and can be classified as benign or malignant. Primary duodenal tumors (PTD) are the most common, while secondary tumors are less frequent^1,2. Common benign tumors in the duodenum include adenoma, stromal cell tumor, lipoma, fibroma, and hemangioma, with adenoma being the most prevalent and possessing the potential for malignant transformation^3,4,5. The disease typically presents insidiously, with early stages often being asymptomatic or displaying non-specific symptoms such as upper abdominal fullness, dull pain, and discomfort. As the disease progresses, symptoms may include anemia, jaundice, gastrointestinal bleeding, fever, abdominal mass, and intestinal obstruction, thus posing a significant threat to public health⁶. Surgical resection remains the preferred treatment for benign neoplasms in the duodenum⁷.

The generalized pancreaticobiliary junction encompasses the pancreatic head, the duodenal wall segment of the common bile duct, the pancreatic segment, the descending part of the duodenum, and the surrounding tissue of the pancreatic head. More specifically, it is defined as the point where the common bile duct terminates, the main pancreatic duct opens, and the area between the duodenal papilla anatomically referred to as the ampulla of Vater or the papilla⁸. Tumors at this junction can obstruct the outflow of fluids, leading to increased pressure within the ducts, dilation, stasis, and stone formation. Additionally, these tumors can disrupt fluid flow, leading to reflux, inflammation, and further tumor growth^9,10. In recent years, laparoscopic biliary and pancreatic surgeries have gained popularity and success due to advancements in minimally invasive techniques. Traditional treatment methods for benign tumors of the duodenal papilla include endoscopic resection, local transduodenal resection, and pancreaticoduodenectomy^11,12.

Although laparoscopy has been widely adopted in surgical practice, there have been few reports on the resection of benign duodenal tumors, particularly those involving the duodenal papilla^11,13,14. In this study, an innovative treatment method was employed, involving robot-assisted pancreaticobiliary junction resection and duodenal anastomosis following biliary stent implantation. The overall goal of this approach is to restore bile duct patency while excising the tumor, preserving digestive system function, and minimizing the risk of complications. The rationale for this approach lies in its capacity to merge the precision of robotic surgery with the advantages of minimally invasive techniques. This method provides enhanced visualization, increased dexterity, and improved control during complex dissections, especially in delicate anatomical regions such as the pancreaticobiliary junction. By integrating an advanced robotic system, this approach not only facilitates lesion removal but also restores bile duct patency, preserves digestive system functionality, and minimizes complications such as bile leakage, pancreatic leakage, bleeding, and infection, ultimately demonstrating positive clinical outcomes.

CASE PRESENTATION:
This study presents a 66-year-old female patient who was admitted to the hospital due to abdominal pain persisting for over a month. A CT scan revealed a 13 mm x 13 mm mass in the duodenal papillary area, characterized by a distinct boundary (see Figure 1). Preoperative gastroscopy indicated an enlarged duodenal papilla with surface congestion and erosion (see Figure 2A-B). Additionally, ultrasound gastroscopy demonstrated an occupied duodenal papilla measuring approximately 19.1 mm x 15.4 mm, extending to the end of the main pancreatic duct (see Figure 2C-D). Pathological analysis using Hematoxylin and Eosin (HE) staining confirmed the presence of a duodenal papillary villous tubular adenoma (see Figure 3). The patient had no significant medical history, and her physical examination findings and laboratory results were unremarkable.

Protocol

The operation is routine and has received ethical approval. The research content and methods meet the medical ethics norms and requirements. The Ethics Committee of the Six Affiliated Hospitals of Sun Yat-sen University approved this study. The patient provided written informed consent.

1. Patient selection

1. Use the following inclusion criteria: benign duodenal tumors, including adenoma, stromal cell tumor, lipoma, fibroma, and hemangioma.
2. Use the following exclusion criteria: malignant tumors of the duodenum, including adenocarcinoma, leiomyosarcoma, malignant lymphoma, carcinoid, etc. Additionally, patients with severe comorbidities such as heart disease and diabetes, coagulation disorders or predispositions to bleeding, severe systemic infections, or a poor overall health status that renders them unsuitable for surgery are excluded. Furthermore, patients who have personally declined the surgical procedure will also be excluded.

2. Preoperative preparation, operative position, and anesthesia

1. Ask the patient to adhere to a low-fat, low-salt, and low-sugar diet the day before the surgical operation and to refrain from consuming food or water for at least 8 h prior to the surgery.
2. Place the patient in a supine position with the head elevated and slightly tilted to the left.
3. Administer general anesthesia using 1%-4% sevoflurane, cyclopofol (10 mg/mL), cisatracurium (2 mg/mL), and sufentanil (5 µg/mL). Perform endotracheal intubation. Evaluate the anesthetic effect based on the patient's post-anesthesia and intraoperative conditions, including the presence of a complete anesthesia block, the absence of additional drugs during the procedure, and the stability of vital signs.

3. Surgical procedure

1. Make a vertical incision 1 cm below the navel and insufflate carbon dioxide using a Veress needle into the abdominal cavity to create a pneumoperitoneum. This causes the abdomen to inflate, providing a larger and clearer surgical field, which facilitates the procedure. Then, insert a 10 mm trocar and introduce the laparoscope (the third arm of the robot) after establishing the pneumoperitoneum.
2. Explorate the intraperitoneal organs to observe that there were no ascites (identified as fluid visible inside the abdomen) and there were no signs of tumor implantation or metastasis. If there are signs of tumor implantation or metastasis, nodules or lesions will be visible in areas outside the primary tumor site on the camera.
3. Place the other three trocars in the following positions: a 10 mm trocar in the right anterior axillary line level (the first arm of the robot), a 10 mm trocar in the medial to the intersection of the umbilical level and the midclavicular line (the second arm of the robot), a 10 mm trocar in the 5 cm above the umbilicus, at the left midclavicular line (the fourth arm of the robot). Additionally, prepare two 12 mm auxiliary ports located on the vertical line at the midpoint between trocars numbered 2 and 3 and medial to the left midclavicular line (see Figure 4).
4. Connect to the robot operating lever and perform the laparoscopic operation with the robot's assistance (see Figure 5).
5. Mobilize the descending and horizontal parts of the duodenum through a Kocher incision.
6. Use an ultrasonic knife to dissect the descending part of the duodenum of about 8 cm (see Figure 6) and identify the duodenal papillary mass.
7. Use an ultrasonic knife to incise the duodenal fold and muscle layer with a cut depth of 3-5 mm around the tumor. Fully excise the tumor and freeze the specimens immediately to examine. The results revealed no malignant evidence in the duodenal papillary adenoma.
8. Use a 4-0 absorbable line to anastomose discontinuously the incised duodenal fold, muscle layer, and the stump of the confluent part of the biliary pancreatic duct.
9. Place the stent tube to support them (see Figure 7). Use 4-0 priline to suture and place the stent into the distal part of the duodenum (see Figure 8).
   NOTE: The diameter and length of the stent tube were 2.67 mm and 10 cm, respectively. (see Table of Materials).
10. Suture intermittently the mucosal layer of the duodenal incision and the plasma muscle layer to bury the wound using 3-0 putis (see Figure 9).
11. Rinse the abdominal cavity with saline to check for any bleeding points and place a drain at Winslow foramena and para duodenum, respectively. Finally, use 4-0 silk to suture the incision, and the operation is concluded.

4. Postoperative nursing and monitoring

1. Perform ECG monitoring and administer low-flow oxygen post-operation.
2. Encourage the patient to consume a semi-liquid diet and engage in bed exercises on the 1^st day after surgery.
3. Administer anti-inflammatory, hemostatic, analgesic, albumin, and acid suppression treatments.
4. Monitor changes in amylase and bilirubin levels in the drainage tube on the 1^st, 2^nd, 3^rd, 5^th, 7^th, and 9^th day post-operation.
   NOTE: It is crucial to maintain the patency of the drainage tube and to ensure the early recovery of gastrointestinal function.

Results

On January 14, 2024, a robot-assisted pancreaticobiliary junction resection was performed at the hospital, followed by biliary stent implantation and anastomosis of the bile duct and duodenum. Postoperative pathology results were consistent with the preoperative findings from other hospitals. Postoperative drainage amylase and bilirubin levels showed a significant decrease (see Table 1), and the patient experienced a smooth recovery following surgery. We have conducted follow-ups for over 6 months post-surgery.

The representative results demonstrate the efficacy and safety of the technique. These findings highlight several key metrics that reflect both surgical outcomes and patient recovery. Firstly, the procedure was completed in 3.5 h, with a minimal intraoperative bleeding volume of 30 mL, eliminating the need for a blood transfusion, indicating that the robotic approach facilitates a precise and controlled surgical procedure. Importantly, no short-term complications were observed, and the patient's postoperative recovery was successful, suggesting that the technique is not only effective but also safe, thereby minimizing immediate surgical risks. The total duration of the hospital stay was 21 days, with 12 days specifically allocated to postoperative care, indicating a moderate recovery period typical for major abdominal surgeries. Notably, the drain amylase levels decreased from 8855 U/L on postoperative day 2 to 49.96 U/L on postoperative day 9. The drain total bilirubin levels decreased from 27.45 µmol/L on postoperative day 3 to 9.30 µmol/L on postoperative day 9. The drain direct bilirubin levels decreased from 6.91 µmol/L on postoperative day 3 to 2.70 µmol/L on postoperative day 9 (see Table 1). These indicators are crucial for the early detection of potential complications, such as leakage or infection, and their normalizing values provide reassurance of a controlled recovery. Postoperative images can be seen in Figure 10. The post-surgical removal of the duodenal tumor can be observed, along with the placement of the biliary stent. Postoperative pathological findings of the tumor can be seen in Figure 11. Pathological analysis confirmed the presence of a duodenal papillary villous tubular adenoma.

Figure 1: Preoperative images. Preoperative CT coronal view imaging. In this image, the location of the duodenal papillary tumor in the patient before surgery can be observed. Please click here to view a larger version of this figure.

Figure 2: Gastroscopic and Ultrasound gastroscopy results. A-B. Gastroscopic results. C-D. Ultrasound gastroscopy results. Please click here to view a larger version of this figure.

Figure 3: Tumor pathology. Preoperative pathological findings of the tumor. The results are from HE staining at 100x. Please click here to view a larger version of this figure.

Figure 4: The layout of trocars. There were 6 trocars in total, including one observation port numbered 3, three operating ports numbered 1, 2, and 4, and two auxiliary ports numbered 5 and 6. Please click here to view a larger version of this figure.

Figure 5: Robot device connected successfully. Connect the four arms of the robot to the four trocars numbered 1-4 in Figure 4. The numbers 1 and 4 refer to the robotic arms connected to the system. The other two numbers correspond to the auxiliary ports, which are operated by the first assistant surgeon and do not need to be connected to the robot. Please click here to view a larger version of this figure.

Figure 6: Incise the duodenum longitudinally. Dissect the descending part of the duodenum longitudinally about 8 cm. Please click here to view a larger version of this figure.

Figure 7: Placement of the biliary stent. Place the stent tube to support them. Please click here to view a larger version of this figure.

Figure 8: Place the stent into the distal part of the duodenum. Use 4-0 priline to suture and place the stent into the distal part of the duodenum. Please click here to view a larger version of this figure.

Figure 9: Suture intermittently the duodenal incision. Suture intermittently the mucosal layer of duodenal incision, and the plasma muscle layer to bury the wound using 3-0 putis. Please click here to view a larger version of this figure.

Figure 10: Postoperative images. Postoperative CT coronal view imaging. In this image, the post-surgical removal of the duodenal tumor can be observed, along with the placement of the biliary stent. Please click here to view a larger version of this figure.

Figure 11: Tumor pathology. Postoperative pathological finding of the tumor. The result is from HE staining at 100x. Please click here to view a larger version of this figure.

Items	Results
Operation time (min)	210
Intraoperative bleeding volume (mL)	30
Blood transfusion volume (mL)	0
Postoperative complication	None
Duration of hospital stay (day)	21
Postoperative hospital stay (day)	12
Drain AMY on POD2 (U/L)	8855
Drain AMY on POD9 (U/L)	49.96
Drain TBIL on POD3 (µmol/L)	27.45
Drain TBIL on POD9 (µmol/L)	9.3
Drain DBIL on POD3 (µmol/L)	6.91
Drain DBIL on POD9 (µmol/L)	2.7

Table 1: Relevant outcomes of the patient. Abbreviations: POD = postoperative day; AMY = amylase; TBIL = total bilirubin; DBIL = direct bilirubin.

Discussion

Duodenal benign tumors are infrequent in clinical practice, yet they can lead to severe complications^1,15,16. The choice of treatment depends on factors such as the size, location, and tissue type of the lesion. Given the relatively fixed position of the duodenum, which is often situated posterior to the peritoneum and closely associated with the head of the pancreas and the ampulla of the bile pancreatic duct, intraoperative bleeding can present significant challenges due to their shared blood supply¹⁷. Additionally, perforation complicates suturing and clinical management. Therefore, surgical planning for duodenal benign tumors must take into account the unique anatomy of the duodenum as well as the characteristics of the tumor itself. For example, villous adenoma has a recurrence rate of 32%-43% following local resection, with a subsequent malignant transformation rate of 24%-50% after recurrence^18,19. Consequently, duodenal villous adenoma with a high malignant potential should be promptly addressed through surgical intervention upon detection.

In 1899, Halsted first described transduodenal papillectomy or ampullectomy, as a treatment for benign tumors of the duodenum²⁰. Perez et al. suggested that endoscopic removal could be considered for duodenal tumors smaller than 1 cm, while tumors larger than 2 cm may require surgical resection³. Furthermore, Cavallini et al. recommended pancreaticoduodenectomy for large villous adenomas²¹. Various surgical options have been employed historically, including endoscopic local tumor resection, laparoscopic or open duodenotomy local tumor resection, intestinal wedge resection, pancreato-sparing duodenectomy, and pancreaticoduodenectomy^{11,19,21,22,23}. Among these, local tumor resection for small benign duodenal masses has demonstrated lower postoperative complication rates, including pancreatic fistula, biliary fistula, infection, and bleeding, as well as reduced mortality rates^24,25,26,27. In 2003, Rosen et al. reported the first case of laparoscopic resection of a tubular villous adenoma in the ampulla¹¹. Laparoscopic transduodenal tumor resection, particularly involving the duodenal papilla, has been rarely reported^12,28. The introduction of robotic surgery has provided a three-dimensional, stable, and enlarged surgical field of view, along with enhanced instrument maneuverability, enabling fine and precise surgical procedures. Stephanie et al. presented the first multicenter experience of robot-assisted duodenectomy, demonstrating the feasibility and safety of the procedure²⁹.

When it comes to the significance with respect to existing methods, the surgical approach described in this study employs a novel technique that combines local tumor resection with robotic assistance. Robot-assisted techniques present several advantages over traditional open and laparoscopic surgeries, including enhanced precision, reduced blood loss, and shorter recovery times. The specific steps include a longitudinal incision in the duodenum to excise the pancreaticobiliary junction tumor, the placement of a bile duct stent, a mucosa-to-mucosa anastomosis between the bile duct and the duodenum, and suturing of the duodenal incision at stage I. The use of this system enhanced visualization, facilitated precise operations, reduced duodenal pull injury and surgical trauma, improved the accuracy of biliary stent suture fixation, and allowed for a more effective biliary-duodenal mucosa-to-mucosa anastomosis, ultimately resulting in a shorter postoperative recovery time. Furthermore, it is recommended to perform endoscopic ultrasonography prior to surgery to assess tumor depth and mitigate the risk of perforation. To minimize the risk of postoperative duodenal intestinal stenosis, it is advised to excise the tumor along the longitudinal axis of the duodenum as extensively as possible during local resection. Notably, due to the challenges associated with preoperative biopsy for malignancy determination, a pathological examination of frozen sections during surgery is preferred. If malignancy is suspected, pancreaticoduodenectomy should be considered³⁰. In instances where intraoperative frozen pathology results are benign but postoperative pathology results indicate cancer, pancreaticoduodenectomy may be employed as a corrective measure²¹.

While this technique presents numerous advantages, it also has certain limitations. The learning curve associated with mastering robotic systems can be steep, necessitating extensive training and experience. Furthermore, the high cost and limited availability of robotic equipment may hinder widespread adoption, especially in resource-constrained environments^31,32. Additionally, there are potential risks linked to robotic surgery, including equipment malfunctions and the necessity to convert to open surgery in the event of complications.

To sum up, robot-assisted pancreaticobiliary junction resection for benign tumors of the duodenal papilla is a feasible procedure, as evidenced by the successful recovery of the patient in this case. The critical steps of the protocol include a longitudinal incision of the duodenum, tumor removal at the pancreaticobiliary junction, placement of a bile duct stent, bile duct mucosa-to-mucosa anastomosis with the duodenum, and stage I suturing of the duodenal incision. Modifications to the technique may be necessary to accommodate patient-specific anatomy or tumor characteristics. In our experience, adjustments to the positioning of robotic arms can enhance access to challenging areas. For example, altering the angle of the camera port can improve visualization of the duodenal papilla. Close post-operative monitoring and timely intervention are essential to minimize complications. This approach not only eliminates the need for resections of the pancreatic head and biliary tract but also reduces the risk of pancreatic and biliary fistulas that may occur with digestive tract reconstruction following resection while avoiding damage to adjacent organs. It enhances surgical safety, accelerates patient recovery, decreases complications, and shortens hospital stays.

Furthermore, the potential future applications of robot-assisted pancreaticobiliary junction resection are extensive. This technique may be adapted for more complex pancreaticobiliary surgeries, including those involving malignant tumors. Further research could investigate the integration of robotic systems with augmented reality and artificial intelligence to enhance surgical planning and execution. Such innovations hold promises for improving surgical outcomes and broadening the scope of minimally invasive surgery. However, given the limited scope of this study, which involves only one case and the relatively underutilized nature of robot-assisted procedures, further research is warranted to validate the advantages of robot-assisted pancreaticobiliary junction resection.

Materials

List of materials used in this article

Name	Company	Catalog Number	Comments
Abdominal instrument button	Johnson & Johnson	/	/
Abdominal instrument cap	Johnson & Johnson	/	/
Abdominal instrument collar	Johnson & Johnson	/	/
Abdominal instrument connector	Johnson & Johnson	/	/
Barbs	Johnson & Johnson	/	/
Blade	Johnson & Johnson	/	/
Blood pad	Johnson & Johnson	/	/
Cloth towel forceps	Johnson & Johnson	/	/
Da Vinci robot (IV)	Intuitive Surgical, USA	/	/
Disposable drainage tube	Johnson & Johnson	412280	10 cm x 2.67 mm
Electric knife head	Johnson & Johnson	/	/
Forceps	Johnson & Johnson	/	/
Hilt	Johnson & Johnson	/	/
Holding flask	Johnson & Johnson	/	/
Intestinal forceps	Johnson & Johnson	/	/
Laparoscope	Johnson & Johnson	/	/
Laparoscopic instruments	Johnson & Johnson	/	/
Long curved forceps	Johnson & Johnson	/	/
Medium curved forceps	Johnson & Johnson	/	/
Needle holders	Johnson & Johnson	/	/
Ovoid forceps	Johnson & Johnson	/	/
Paraffin oil	Johnson & Johnson	/	/
Purse string forceps	Johnson & Johnson	/	/
Right angled forceps	Johnson & Johnson	/	/
Right angled forceps	Johnson & Johnson	/	/
Scissors	Johnson & Johnson	/	/
Siphonhead	Johnson & Johnson	/	/
Small cup	Johnson & Johnson	/	/
Small curved forceps	Johnson & Johnson	/	/
Sonotome keyhole	Johnson & Johnson	/	/
Steel ruler	Johnson & Johnson	/	/
Straight forceps	Johnson & Johnson	/	/
Suction needle plate	Johnson & Johnson	/	/
Suture needle	Johnson & Johnson	Vcp397H	/
Syringe	Johnson & Johnson	/	/
Syringe needle	Johnson & Johnson	/	/
Tissue forceps	Johnson & Johnson	/	/
Trocar(XCEL)	Ethicon Endo-Surgery	695C71	/
Ultrasonic knife spacers	Johnson & Johnson	/	/
Ultrasound knife	Johnson & Johnson	/	/
Yarn ball	Johnson & Johnson	/	/