Supplementary materials can be found via https://doi.org/10.7602/jmis.2023.26.3.155.

Recently, the incidence and diagnosis of benign and low-grade malignant pancreatic neoplasms have increased [1]. With the development of diagnostic technologies, and accumulated knowledge on the histopathologic characteristics and natural course of these neoplasms, there has been an increased interest in organ- and function-preserving surgical procedures. Central pancreatectomy (CP) is an uncommon surgical procedure because of its rare indication, technical difficulty, and higher complication rate than that of distal pancreatectomy (DP) [2,3]. However, CP could be an appropriate surgical option for preserving pancreatic exocrine and endocrine functions in patients with proximal body tumors, which alternatively requires subtotal DP (STDP). STDP usually results in a loss of 70% to 80% of the pancreatic volume [4]. However, as reported, a large number of islet cells are placed in the pancreatic body portion, and the incidence of new-onset diabetes after STDP is reported to be 64.7% to 73.3% [5–7].

CP is associated with a high postoperative morbidity related to postoperative pancreatic fistula (POPF) owing to the presence of two pancreatic cut surfaces. Nevertheless, with technological advances in minimally invasive surgery, more surgeons are concerned about the long-term quality of life of patients as well as perioperative outcomes. Recently, the number of laparoscopic approaches for pancreatic surgery, including pancreaticoduodenectomy (PD) and DP, has significantly increased [6]. However, the laparoscopic approach for CP is still technically challenging because of the difficulty in preserving the splenic vasculatures and reconstruction of the remnant distal pancreas. Especially, reconstruction during CP is extremely difficult in a laparoscopic environment. The technical difficulties in the reconstruction phase include the followings: (1) poor operative view and a narrow working space between the remnant proximal and distal pancreas, (2) smaller pancreatic duct, and (3) the target point of the laparoscopic view being changed to the far lateral side from the pancreatic neck to the pancreatic body portion. A change in the target makes the reconstruction procedure harder under the non-articulating nature of the laparoscopic instruments. Therefore, a robotic surgical system is considered helpful in performing such elaborate procedures.

However, the limited body of literature on robotic CP (R-CP) indicates that this complex surgery requires technical expertise. The current study aimed to introduce the surgical technique in detail, and to describe the perioperative and follow-up outcomes.

This study reports the experience of a single surgeon who performed R-CP from May 2016 to June 2021. Indications for R-CP were as follows: (1) benign or borderline malignant neoplasm, (2) lesions located at the pancreatic neck and proximal body, (3) preserved distal pancreatic parenchyma and endocrine function, 4) no involvement of splenic vessels, and (5) appropriate health status (grade of ≤3 according to the American Society of Anesthesiologists [ASA]).

Patient demographics, operative data, perioperative outcomes, pathological diagnoses, and follow-up data were collected retrospectively.

Postoperative complications were categorized according to the Clavien-Dindo classification. POPF was defined according to the International Study Group of Pancreatic Surgery definition.

Operative techniques

The patient was positioned in the supine and reverse Trendelenburg position with a slight elevation on the left side. The robotic camera port was located at the umbilicus, and two 8-mm and one 8-mm robotic trocars were placed on the right and left side of the abdomen, respectively. The assistant surgeon worked through the left side 12-mm trocar (Fig. 1). The main instruments for resection were monopolar curved scissors (trocar 1), Maryland dissector (trocar 2), and precision bipolar forceps (trocar 3) (Intuitive Surgical, Inc.). The two left robotic trocars were inserted slightly above the umbilicus level to avoid collisions of the working instruments with the robotic camera view (asterisk in Fig. 1A). After dissection of the gastrocolic ligament, the stomach was retracted using 2-0 nylon suturing of the posterior wall of the stomach by extracorporeal needling and tying up (Supplementary Video 1). The lesion and tumor margins were identified and confirmed using direct visualization and laparoscopic ultrasonography. The pancreatic neck portion was dissected the first and a complete window was made at the pancreatic neck and encircled with a nylon tape. The proximal portion of the lesion, usually the pancreatic neck, was divided using a laparoscopic linear stapler via the 12-mm assistant port. The stump of the specimen site was then sutured using a rubber band (Supplementary Video 1). The distal pancreas was retracted upward laterally using the robotic third arm, and the splenic vessels were carefully dissected to control the small tributaries. The sterilized elastic rubber band was helpful in compensating for forceful retraction owing to the lack of haptic feedback of the robotic instrument to avoid iatrogenic injuries during the procedure. After obtaining an appropriate distal resection margin, the distal portion of the pancreas was resected using harmonic curved shears (Intuitive Surgical, Inc.). Occasionally, the distal margin was resected using a laparoscopic linear surgical stapler first, in cases where spillage of pancreatic juice had to be avoided, such as in Supplementary Video 1. The acting blades of the harmonic shears first proceed into the pancreatic parenchyma, and then the blade was gradually closed, to allow the small vessels to be denatured by heat. After approaching the center of the pancreas, the pancreatic parenchyma was carefully dissected using the ultrasonic vibration energy of the acting blades of the ultrasonic shears to identify the pancreatic duct, keeping it fresh, and to facilitate a secure duct-to-mucosa anastomosis. Once the pancreatic duct was identified, it was resected using scissors. After the division of the pancreas, the specimen was inserted into a plastic bag. The proximal jejunum was then divided at approximately 15 to 20 cm from the ligament of Treitz using a laparoscopic linear stapler, and the distal limb was pulled up to the dead space of the resected pancreas through the new opening of the mesocolon. We used the conventional interrupted suture anastomosis for pancreaticojejunostomy. Two layered end-to-side duct-to-mucosa anastomosis was made using non-absorbable 5-0 monofilament for out-layer and absorbable 5-0 monofilament for duct-to-mucosa anastomosis with a short silicone internal stent. Jejunojejunostomy was performed in a side-to-side manner using intracorporeal suturing or laparoscopic linear stapling. A two-armed Jackson Pratt drain was inserted around the pancreaticojejunostomy and the proximal pancreatic stump. The specimen was retrieved through the umbilical wound (Fig. 1).

General demographics of patients

Six patients who underwent R-CP were included in this study (Table 1). Four patients were female and two were male, with a median age of 47 years (range, 28–67 years). The patients’ median body mass index was 22.49 kg/m² (range, 20.08–25.56 kg/m²) and all patients had ASA grade II or II disease. None of the patients had diabetes mellitus (DM) diagnosed before surgery. The final pathologic diagnoses were solid pseudopapillary neoplasms, neuroendocrine tumor, and intraductal papillary neoplasm in two patients each. Fig. 2 shows the preoperative images of the patients who were indicated for CP. The median tumor size was 3.05 cm (range, 1.4–3.8 cm).

Perioperative outcomes

Table 2 shows the surgical outcomes of the six patients who underwent R-CP. The median operative time and estimated amount of blood loss were 267.5 minutes (range, 250–290 minutes) and 85 mL (range, 40–160 mL), respectively. None of the patients received blood transfusions. One patient experienced grade B POPF, while the others experienced biochemical leakage. There were two postoperative complications, cystitis (grade II) and pseudocyst (grade IIIa), which were related to grade C POPF and were successfully managed by endoscopic internal drainage (Fig. 3). The median hospital stay was 8.5 days (range, 7–16 days). All patients achieved a complete negative resection margin and the median length of the resected pancreas was 4.75 cm (range, 3.2–5.5 cm).

Follow-up after robotic central pancreatectomy

The median follow-up duration after R-CP was 15 months (range, 10–62 months). Follow-up data are presented in Table 3. No patient experienced new-onset DM or recurrence during the follow-up period. The median fasting blood glucose level was 99.5 mg/dL (range, 95–110 mg/dL). Fig. 4 illustrates the last follow-up computed tomography images, demonstrating a well-preserved remnant distal pancreas in all cases. However, case 3 showed mild pancreatic duct dilatation and slight shrinkage of the remnant pancreas, suggesting an anastomotic stricture, but the patient had good endocrine function without hyperglycemia.

The clinical benefits of CP are controversial because of the higher complication rates than those of DP and the uncertainty regarding the long-term outcomes of preservation of pancreatic function [7]. Besides providing evidence regarding the long-term outcome of the preserved remnant pancreas, the current study demonstrated that the R-CP technique could be safely performed with accumulated experience in minimally invasive pancreatic surgeries. In our series, there was one major complication (grade IIIa) related to grade B POPF. However, there was no new-onset or aggravated DM or recurrence during the median follow-up period of 15 months (range, 10–62 months).

A systematic review and meta-analysis by Iacono et al. [2] illustrated the comparison of immediate postoperative and long-term outcomes between CP and DP. In their analysis, CP was associated with a higher POPF rate (30.8% [CP] vs. 14.3% [DP], p < 0.001) and overall morbidity (46.0% [CP] vs. 26.6% [DP], p = 0.002) than DP, as well as a longer operation time and hospital stay. CP showed better long-term outcomes in terms of pancreatic functional preservation. Another systematic review by Regmi et al. [4] confirmed the same outcome. Song et al. [8] reported similar results regarding the laparoscopic approach. The laparoscopic CP (L-CP) group had a higher overall postoperative complication rate than the laparoscopic STDP (L-STDP) group; however, there was no significant difference in major complications of ≥grade III or clinically relevant POPF (CR-POPF) between the two groups. Notably, L-CP yielded better preservation of endocrine function than L-STDP (postoperative new-onset diabetes, 8% [L-CP] vs. 30.8% [L-STDP]; p = 0.037).

Although L-CP is feasible with a controllable burden of postoperative morbidity and POPF, it is technically demanding, especially in the reconstruction phase. Even for surgeons over the learning curve of laparoscopic PD, the reconstruction procedure during L-CP is difficult. First, the operative target was moved far from the pancreatic neck. Changes in the operative target made the surgery difficult in the laparoscopic setting. Second, we preferred pancreaticojejunostomy over panceaticogastrostomy for reconstruction of the remnant distal pancreas because of atrophic changes in the preserved pancreas in patients who underwent pancreaticogastrostomy [7]. However, the Roux-en-Y limb of the jejunum that was placed in the dead space of the resected central pancreas hid the remnant distal pancreas, resulting in a poor operative view of the pancreatic cut surface. Third, the pancreatic duct size was smaller at the distal pancreas in patients with normal pancreas than that of the pancreatic neck in PD. Finally, the remnant distal pancreas drops into the deeper posterolateral abdominal cavity after resection of the central pancreas due to gravity by the spleen, which makes it difficult to manage the anastomosis by the conventional straight laparoscopic instruments.

Because of these limitations in L-CP, the robotic surgical system is speculated to be advantageous in overcoming the technical difficulties related to this reconstruction procedure, and resection procedure requires delicate management for splenic vessel preservation. Chen et al. [9] conducted a randomized controlled trial to compare R-CP and open CP in 50 patient pairs. They showed that R-CP could be performed safely with a lower incidence of POPF than open CP (18% [R-CP] vs. 36% [open CP], p = 0.043) and favorable outcomes with shorter hospital stays, shorter operative time, and lesser blood loss. Recently, the only systematic review and meta-analysis of R-CP by Rompianesi et al. [10] also demonstrated that the robotic approach was associated with a low rate of major complications (9.4%) and de novo diabetes (0.3%), but a high rate of CR-POPF (42.3%). Our data also showed reliable perioperative outcomes and satisfied the short-term requirements of the remnant pancreas.

However, this current study was based on a small number of cases. We did not compare the outcomes between patients who underwent DP and CP because of the limited data on patients who had comparable tumoral characteristics. Nevertheless, we focused on introducing the technical aspects of R-CP in this study.

It cannot be concluded whether CP is a superior surgical option compared to DP because of the paucity of data worldwide. Nevertheless, our interim experience with R-CP showed that the robotic surgical system could provide potential positive benefits and enhance the quality of life of patients with benign and borderline malignant tumors in the pancreatic neck or proximal body, due to the acceptable postoperative complications and pancreatic function preservation.

Ethical statements

This study was approved by the Institutional Review Board of CHA Bundang Medical Center (No. 2022-09-004) and was conducted according to the ethical standards of the Institutional Committee on Human Experimentation, Declaration of Helsinki. The need for patient consent was waived.

Authors’ contributions

Conceptualization: All authors

Data curation, Methodology: EHC, SHC

Formal analysis, Validation: SHC

Visualization: All authors

Writing–original draft: All authors

Writing–review & editing: All authors

All authors read and approved the final manuscript.

Conflict of interest

All authors have no conflicts of interest to declare.

Funding/support

None.

Data availability

The data presented in this study are available on request from the corresponding author.

General demographics and pathologic data of patients

Perioperative outcomes

Follow-up data after surgery