Single-Stage Endoscopic Retrograde Cholangiopancreatography Combined with Laparoscopic Enucleation of Pancreatic Cystic Neoplasms

Summary

We describe a novel minimally invasive procedure involving single-stage endoscopic retrograde cholangiopancreatography combined with laparoscopic enucleation of pancreatic cystic neoplasms. This procedure preserves pancreatic function while avoiding injury to the main pancreatic duct. It also offers advantages such as minimal invasiveness, reduced hospital length of stay, and fewer complications.

Abstract

Pancreatic cystic neoplasms (PCNs) represent a heterogeneous group of lesions, with some specific subtypes harboring malignant potential or exhibiting low-grade malignancy. Surgical resection remains the primary treatment modality. Traditional pancreatoduodenectomy is associated with severe trauma and slow recovery, while minimally invasive methods like laparoscopic central pancreatectomy (LCP) mitigate these issues; Laparoscopic enucleation (LE), a common procedure in function-preserving surgery, carries a risk of postoperative pancreatic fistula (POPF) for PCNs adjacent to the main pancreatic duct (MPD). While laparoscopic enucleation paired with two-staged endoscopic retrograde cholangiopancreatography (ERCP-LE) can mitigate POPF, this approach increases the length of hospital stay (LOS). Thus, we applied single-stage ERCP-LE for the treatment of PCNs, fully leveraging the advantages of both techniques. This approach enables the simultaneous performance of ERCP-guided pancreatic duct mapping, transpapillary stent placement, and laparoscopic enucleation of the target lesion during a single operative session. The technique boasts prominent advantages and pioneering value: it completes multi-step procedures in one stage, avoiding interval pancreatitis associated with staged operations while shortening treatment duration, reducing the risks of repeated anesthesia, stent migration, and additional costs; ERCP-guided stent placement minimizes injury to the MPD, facilitates immediate repair if injury occurs, and diverts pancreatic juice to significantly lower the incidence of POPF and pancreatitis. As an innovative therapeutic approach for high-risk PCNs adjacent to the MPD, single-stage ERCP-LE overcomes the limitations of traditional surgery and two-staged ERCP-LE. It is therefore expected to become the standard treatment for PCNs adjacent to the MPD, enabling more precise minimally invasive therapy while significantly preserving pancreatic function.

Introduction

The detection rate of Pancreatic cystic neoplasms (PCNs) has risen markedly with advances in imaging techniques. These lesions, which exhibit diverse pathological subtypes, primarily comprising serous cystic neoplasms, mucinous cystic neoplasms, intraductal papillary mucinous neoplasms, and solid pseudopapillary neoplasms, each demonstrate distinct biological behavior and clinical manifestations¹. Most PCNs are asymptomatic in the early stages. As the neoplasm enlarges, symptoms such as epigastric pain, abdominal fullness, nausea, and vomiting may develop. In severe cases, the neoplasm can compress adjacent tissues, leading to organ dysfunction, or it may undergo malignant transformation, which can be life-threatening².

According to the 2015 American Gastroenterological Association (AGA) guidelines³, 2018 American College of Gastroenterology (ACG) guidelines⁴, 2018 European guidelines⁵, and 2024 International guidelines⁶, surgical resection is the standard curative treatment for PCNs that are symptomatic, exhibit malignant features such as mural nodules, solid components, or pancreatic duct dilation, or exceed a specified size threshold. However, there remains no consensus on the surgical techniques to be used, with significant heterogeneity in recommendations among existing guidelines. Traditional open surgical approaches, such as pancreatoduodenectomy, effectively resect tumors but are associated with substantial surgical trauma, prolonged postoperative recovery, and significant pancreatic function impairment, imposing physical distress and economic burden on patients. In contrast, minimally invasive techniques such as laparoscopic central pancreatectomy (LCP) may mitigate these adverse outcomes⁷. Pancreatic function-preserving surgery has become increasingly prevalent for benign or low-malignant pancreatic neoplasms, with Laparoscopic enucleation (LE) being a common approach, especially for lesions in the pancreatic head and body due to its advantage in preserving healthy pancreatic parenchyma. However, this procedure faces critical limitations: enucleation of tumors adjacent to the main pancreatic duct (MPD) is clinically challenging due to the high risk of postoperative pancreatic fistula (POPF), which often leads to severe complications such as abdominal infection and hemorrhage. Additionally, endoscopic retrograde cholangiopancreatography (ERCP) has emerged as indispensable in pancreatobiliary disease management amid technological advances. Stent placement through ERCP is capable of mitigating the risk of POPF⁸. Although two-staged ERCP combined with LE (ERCP-LE) with pancreatic duct stenting followed by enucleation is attempted to mitigate this risk, it prolongs the length of hospital stay (LOS) and carries the potential of ERCP-induced pancreatitis that may preclude subsequent enucleation.

To address these unmet needs, this report details a novel single-stage ERCP-LE procedure for PCNs, with a representative case provided as an example. A 75-year-old female patient presented with a 10-year history of epigastric pain and was admitted for evaluation. Two years prior, an abdominal computed tomography (CT) scan had revealed a pancreatic cystic lesion measuring approximately 30 mm x 37 mm, which was managed conservatively. Recently, the recurrence of symptoms prompted further investigation. Magnetic resonance imaging (MRI) demonstrated progression to a 40 mm x 50 mm cystic neoplasm in the pancreatic neck. The cystic neoplasm was about 1 mm away from the MPD (Figure 1). Given tumor growth confirmed by imaging studies and persistent clinical symptoms such as pain and neurological deficits, surgical intervention was indicated. Key procedural steps included ERCP-guided MPD mapping, transpapillary pancreatic stent placement, and immediate laparoscopic enucleation of the lesion under direct vision. The 220-min procedure achieved preservation of the MPD with minimal blood loss (10 mL), and only a clinically mild, grade A POPF occurred.

Protocol

This study was approved by the Ethics Committee of the Fifth Affiliated Hospital, Southern Medical University. Written informed consent was obtained from the patient before the procedure.

1. Patient selection

1. Confirm indication for surgery by performing imaging studies and considering persistent clinical symptoms such as pain and neurological deficits.

2. Informed consent

1. Provide detailed counseling on the surgical procedure and its inherent risks, including POPF, hemorrhage, and infection, to the patient and the family. Discuss alternative treatment options, such as open surgery. Obtain a written informed consent after a comprehensive discussion and confirmation of comprehension.

3. Preoperative workup

1. Perform hematological assessment, including a complete blood count, blood type, coagulation tests, hepatic function tests, renal function tests, electrolyte levels, and blood glucose. Perform these assessments to evaluate the patient's overall health status and surgical tolerance. Additionally, evaluate tumor markers, including carbohydrate antigen 19-9 (CA19-9).
2. Employ advanced imaging techniques, including advanced ultrasonography, abdominal CT, and MRI, to delineate the pancreatic cystic neoplasm's dimensions, location, morphology, and spatial relationships to adjacent structures, while characterizing internal architecture, septations, and calcifications (Figure 1).
3. Cardiopulmonary evaluation: Conduct preoperative cardiopulmonary risk stratification, including electrocardiography (ECG), thoracic CT, pulmonary function tests (PFTs), and transthoracic echocardiography (TTE). Perform these evaluations to assess cardiopulmonary function and confirm physiological tolerance for surgery.

4. Preoperative preparation and anesthesia

1. Fasting protocol: Have the patient fast (nil per os, NPO) for at least 8 h for solid foods and at least 4 h for clear liquids. Do this to mitigate aspiration risk during anesthesia induction.
2. General anesthesia management. Induce anesthesia intravenously using propofol, fentanyl, and a neuromuscular blocking agent, specifically rocuronium, followed by endotracheal intubation and mechanical ventilation to maintain adequate respiratory function and hemodynamic stability.
3. Ensure intraoperative monitoring, including continuous hemodynamic surveillance, respiratory assessment, and maintenance of anesthetic depth, throughout the procedure.

5. Surgical technique

1. Initial ERCP procedure
   1. Patient positioning:
      1. Position the patient in the standard left lateral decubitus position according to ERCP protocols in order to optimize duodenoscopic access.
   2. Endoscopic navigation and papilla identification:
      1. Advance a duodenoscope through the esophagus and gastric lumen under direct vision. The major duodenal papilla, located along the medial wall of the descending duodenum, exhibited characteristic granular mucosa and showed dynamic changes in orifice patency during peristalsis.
   3. Selective cannulation and pancreatography:
      1. Achieve wire-guided selective pancreatic duct cannulation at the 1 o'clock position relative to the papilla.
      2. Perform contrast injection under X-ray guidance. This confirmed a smooth MPD contour without filling defects, and the pancreatic cystic neoplasm showed no communication with the MPD (Figure 2).
         NOTE: A complete pancreatographic visualization of the MPD and an assessment of tumor-duct communication are essential prerequisites for accurate diagnosis and treatment planning.
   4. Stent deployment technique:
      1. Advance a sphincterotome over the guidewire to perform a precision 2 mm sphincterotomy at the 1 o'clock axis. Achieve immediate hemostasis.
      2. Then, perform balloon dilation of the sphincter of Oddi and the MPD for 30 s. Deploy a modified nasobiliary stent (7.5 Fr, 16 cm) with its distal end positioned at least 4 cm beyond the tumor within the MPD (Figure 3).
         NOTE: Reconfigured nasobiliary catheters serve as viable alternatives when dedicated pancreatic stents are unavailable. Such distal extension beyond the lesion provides a critical tactile landmark to prevent iatrogenic MPD injury during dissection.
   5. Stent verification and surgical transition:
      1. Perform intraoperative fluoroscopy to confirm optimal stent placement, indicated by the distal marker located within the pancreatic body (Figure 4). Following this confirmation, reposition the patient to the supine position to undergo laparoscopic intervention.
2. Laparoscopic surgical procedure
   1. Patient positioning and preparation:
      1. Position the patient supine. After standard antiseptic draping was completed, connect the CO₂ insufflation system, the light source, and the laparoscopic camera.
   2. Place the trocars:
      1. Insert a 10 mm camera trocar 2 cm above the umbilicus to establish pneumoperitoneum (12 mmHg).
      2. Subsequently, deploy four additional trocars in a semicircular configuration: a 10 mm port at the left midclavicular line, a 12 mm port at the right midclavicular line, and two 5 mm ports, one on each side along the anterior axillary lines (Figure 5).
   3. Systematic abdominal exploration:
      1. Perform diagnostic laparoscopy to confirm the absence of metastatic deposits, ascites, or peritoneal carcinomatosis.
         NOTE: Atraumatic tissue handling is imperative to prevent enteric serosal injury. The discovery of metastatic nodes warrants modification of the intraoperative strategy.
   4. Tumor exposure technique:
      1. Incise the gastrocolic ligament along the greater curvature. Achieve gastric retraction using 4-0 polypropylene purse-string sutures, which are commonly employed to provide effective tissue traction, enabling full visualization of the pancreatic neck and body, and the cystic lesion of interest (Figure 6A).
         NOTE: Assess tumor-vascular relationships, invasion margins, and capsule integrity prior to dissection. If the tumor diameter is less than 2 cm, a laparoscopic ultrasound is required to locate the position of the tumor and the relative position between the tumor and the stent.
   5. Tumor enucleation:
      1. Use an ultrasound scalpel to incise the pancreatic capsule. Using a combination of blunt and sharp dissection with the ultrasound scalpel, meticulously dissect the cystic lesion from the pancreatic tissue.
      2. At the tumor base, maintain optimal tension to facilitate precise dissection until complete enucleation is achieved.
         NOTE: Gentle manipulation and meticulous hemostasis are essential to preserve the pancreatic parenchyma, and capsule rupture and MPD injury must be avoided. If intraoperative visualization of the pancreatic duct stent reveals an MPD injury, primary pancreatic duct repair may be performed first. For lateral wall injuries: select 5-0 or 6-0 Polydioxanone sutures for fine anastomosis, align the ductal edges accurately, and suture intermittently without excessive tension to preserve ductal patency. For severe MPD defects, middle pancreatectomy should be considered, and end-to-end pancreatic duct anastomosis or Roux-en-Y pancreaticojejunostomy should be performed as appropriate.
   6. Resection bed management:
      1. Irrigate the resection bed to confirm that there was no stent exposure or pancreatic leakage. Then, suture minor pancreatic duct leaks with interrupted 4-0 polypropylene sutures.
      2. Achieve hemostasis by bipolar coagulation. Apply fibrin sealant to reinforce the surface. Place a drainage catheter adjacent to the resection bed and exteriorize through the left lower quadrant trocar site (Figure 6B).
         NOTE: Small defects may be approximated with simple sutures. For defects greater than 3 cm, forced closure of the defect risks parenchymal tearing and duct distortion. Therefore, open drainage is preferred after achieving hemostasis. Deep and large defects with a high risk of POPF warrant surgical intervention, such as formal resection or Roux-en-Y reconstruction.
   7. Specimen processing:
      1. Place the intact cyst in an endoscopic retrieval bag and extract it through the main operating port (Figure 6C).
      2. Aspirate cyst fluid for biochemical analysis of amylase; tumor marker assays, including carcinoembryonic antigen (CEA) and CA19-9; and cytological examination. Submit the residual specimen for histopathological examination (Figure 7).
   8. Closure protocol:
      1. Irrigate the abdominal cavity thoroughly with saline. After evacuation of the pneumoperitoneum and following confirmation of surgical instrument counts, perform a layered closure of the incision.

6. Postoperative care

1. Monitoring: Monitor heart rate, blood pressure, respiratory rate, temperature, and abdominal signs such as tenderness and swelling; perform daily blood tests; and observe the fluid from the drain.
2. Nutritional support: Ensure the patient remains NPO for 24 h postoperatively and initiate enteral nutrition only after the return of bowel function, indicated by the passage of flatus.
3. Pain management: Administer analgesics based on patient pain assessment scores to ensure a smooth recovery.
4. Rehabilitation guidance: Encourage patients to engage in early ambulation to prevent deep vein thrombosis.
5. Follow-up:
   1. Conduct regular outpatient visits at specified intervals after surgery, and perform appropriate imaging (such as ultrasound or CT) and laboratory tests if epigastric pain occurs at any time postoperatively.
   2. Additionally, remove the pancreatic drainage stent endoscopically 3 months after surgery.
      1. Locate the stent under endoscopy and extract it using specialized instruments, followed by a brief inspection to ensure no residual or complications.

7. Documentation and quality control

1. Medical records: Document all surgical procedures, postoperative care, and patients' physiological and recovery responses thoroughly to ensure comprehensive and accurate medical records, which are essential for effective patient management and continuity of care.
2. Information security: Strictly adhere to patient information privacy principles, and ensure the security of patient information.

Results

Studies indicate that LCP demonstrates the following outcomes: an operative time of 226.59 ± 158.73 min; intraoperative blood loss of 137.91 ± 195.69 mL; a major morbidity rate of 14.2% (18/127); a POPF B/C rate of 27.3% (73/267); and a length of hospital stay of 19.08 ± 12.03 days (Table 1 )⁹. In contrast, LE yields: operative time 137.34 ± 149.22 min, blood loss 59.06 ± 70.50 mL, major morbidity 17.8% (23/129), POPF B/C rate 21.2% (24/113), and length of hospital stay 8.16 ± 14....

Discussion

Traditional open surgery long dominated the management of PCNs but was limited by significant trauma and prolonged recovery. Since Gagner et al.'s first report of laparoscopic pancreatic surgery in 1994¹², the laparoscopic approach has demonstrated superior safety and efficacy over open procedures, reducing intraoperative blood loss and shortening hospital stays¹³. This advancement has progressively expanded to diverse pancreatic resections. For PCNs at different locations ...

Materials

List of materials used in this article

Name	Company	Catalog Number	Comments
Cannulating Sphincterotome	Boston Scientific	M00583100	Duodenal papillary sphincterotomy
Drainage catheter	Zhongkangshun	C-Fr18	Postoperative drainage
Esophagogastroduodenoscopy	Olympus Optical Co	TJF-260	ERCP treatment
Fibrin sealant	Glubran	G-NB-2 1ml	Microvascular hemostasis
Laparoscopic needle driver	Mindray	221-56426	Laparoscopic surgery
Laparoscopic suction/irrigation system	Kangji	102Y 202	Laparoscopic surgery
Nasobiliary catheter	Boston Scientific	M00540130 7.5 Fr, 16 cm	Post-ERCP temporary drainage
Suture material	Ethicon	W8557 4-0 polypropylene	Incision suturing
Trocar	Ethicon	5 mm, 10 mm, 12 mm	Puncturing the abdominal wall
Ultrasonic surgical scalpel	Innolcon	OSG35	Dissection and hemostasis
Wireguided	Boston Scientific	M00558610	Duodenal papilla dilatation