Abstract
Purpose
The aim of the present study was to evaluate the outcomes and preventive techniques for gastric venous congestion (GVC) following total pancreatectomy (TP), with a focus on gastric venous drainage reconstruction.
Methods
This retrospective single-center study included patients who underwent TP between January 2019 and June 2024, encompassing both primary one-step TP and planned elective completion pancreatectomy following either pancreatoduodenectomy (PD) or distal pancreatectomy (DP). Intraoperative evaluation and reconstruction of gastric venous drainage were performed when GVC was observed. Demographic, clinical, technical, perioperative, and postoperative data were analyzed.
Results
Sixteen patients underwent either one-step TP (n = 4) or elective completion pancreatectomy (n = 12), including four following DP and eight following PD. Intraoperative GVC was detected in two patients, necessitating portal vein (PV)-right gastroepiploic vein (RGEV) side-to-side anastomosis. No major complications occurred in these patients, and no GVC was observed during the postoperative follow-up period (mean: 39.8 months, range: 2.1–60.7 months).
Conclusion
In cases where preservation of gastric drainage veins is not feasible, PV-RGEV side-to-side anastomosis can be a convenient and useful option to resolve intraoperative GVC.
Supplementary Information
The online version contains supplementary material available at 10.1007/s00423-025-03702-y.
Keywords: Total pancreatectomy, Elective completion pancreatectomy, Gastric venous congestion, Gastric venous drainage reconstruction
Introduction
Total pancreatectomy (TP) was historically associated with high morbidity and mortality [1, 2]. Advances in managing pancreatic exocrine and endocrine insufficiency, including autologous islet transplantation, have made TP safer [3–5]. However, gastric venous congestion (GVC) remains a critical complication, with reported incidence rates ranging from 5 to 28% and an associated increase in postoperative mortality [6–8]. When TP is performed, all gastric venous drainage routes, including the right gastric vein (RGV), right gastroepiploic vein (RGEV), short gastric veins, left gastroepiploic vein and left gastric vein (LGV), may be ligated, as preservation of the LGV may not always be feasible depending on its point of inflow. Sacrificing the LGV for oncologic or anatomical reasons significantly increases the risk of GVC [8].
Although gastrectomy has been reported to be effective in managing GVC after total pancreatectomy [7, 8], it is not favorable from the perspective of long-term nutritional status. A few studies have suggested the potential utility of venous reconstruction to prevent GVC, mainly using LGV [6, 9–13]. We consider RGEV to be more suitable than LGV for venous reconstruction to prevent GVC, as it offers superior mobility and allows for a wider anastomotic diameter through side-to-side anastomosis. The aim of the present study was to evaluate the outcomes and preventive techniques for GVC following TP, with a focus on gastric venous drainage reconstruction using portal vein (PV)-RGEV side-to-side anastomosis.
Materials and methods
Patients
This study included consecutive patients who underwent TP between January 2019 and June 2024 at Juntendo University Hospital. All patients who underwent elective TP were included, encompassing both primary one-step TP and planned elective completion pancreatectomy following either PD or DP. We retrospectively reviewed patients’ medical records retrieved from prospectively maintained databases and included demographic data, indications for surgery, and peri-operative data (such as surgical technique, hospital mortality, and morbidity) were recorded. This study was conducted in accordance with the ethics code of the World Medical Association (Declaration of Helsinki). The present study satisfied the consensus of the Juntendo University Hospital Institutional Review Board and was subsequently approved with the approval number: E24-0378.
Surgery
All the patients underwent initial TP or elective completion pancreatectomy for remnant pancreatic tumors. All procedures in the present study were performed by one attending surgeon (A.S.), who is the head of the department. Gastric venous drainage was evaluated intraoperatively by the surgeon, and reconstruction of the gastric drainage vein was performed only when GVC was evident. Intraoperative GVC was defined by the presence of congested gastric or perigastric veins, livid (bluish) discoloration of the stomach, gastric wall edema, and serosal petechiae [8]. Postoperatively, computed tomography and endoscopy were used to assess the stomach for any signs of GVC, including persistent venous congestion, discoloration, wall edema, or serosal petechiae. All patients were checked for GVC during surgery and postoperatively until discharge from the hospital. Postoperative delayed gastric emptying was defined based on the International Study Group guidelines [14]. Other postoperative complications were defined based on the Clavien-Dindo classification [15].
PV-RGEV side-to-side anastomosis technique (video)
Before anastomosis, the tissue surrounding the RGEV was trimmed, carefully separated and isolated from the right gastroepiploic artery, and then skeletonized to the necessary length for anastomosis. The anastomosis between the RGEV and PV was performed in a side-to-side fashion. The PV was side-clamped, and the RGEV was also clamped. A venotomy was then performed on the anterior wall of the RGEV. Regarding the PV, rather than a simple vertical incision, a rectangular fenestration was created to ensure sufficient space for the anastomotic site and to prevent the anastomotic stricture after reperfusion (Fig. 1a). After placing a stitch at both edges of the PV and RGEV using 6–0 non-absorbable monofilament thread, anastomosis using the running suture was begun from the left side (Fig. 1b). The posterior wall was sutured intraluminally in a continuous fashion while leaving the stitches untightened. The stitches were then carefully tightened from both sides after the running suture of the posterior wall had been completed. Then, a running suture using an over-and-over technique of the anterior wall was conducted from the left side in the usual manner. Finally, the thread was tied with a growth factor equivalent to that of the anastomosed PV and RGEV (Fig. 1c). Following venous reconstruction, decompression was confirmed through both pressure measurements and macroscopic findings. Intraoperative pressure assessments demonstrated a reduction in venous pressure after reconstruction, indicating successful decompression. The resolution of GVC was further confirmed by the immediate disappearance of congestion-related macroscopic changes following the release of vascular clamps. A representative video of the PV-RGEV side-to-side anastomosis is provided (Supplementary material).
Fig. 1.
Intraoperative photographs and schematic representation of the venous reconstruction with the portal vein (PV)- right gastric epiploic vein (RGEV) side-to-side anastomosis. (a) Preparation for the PV-RGEV reconstruction. A venotomy was made on the anterior wall of the RGEV (large arrow), and a rectangular fenestration was created on the anterior surface of the PV (small arrow). (b) These schematic diagrams illustrate the running suture technique. A stitch is placed at both edges of the PV and RGEV using a 6 − 0 non-absorbable monofilament thread (Left). The posterior wall is sutured intraluminally in a continuous manner, leaving the thread on the left side untied (Middle). Finally, an over-and-over running suture technique is applied to the anterior wall, starting from the left side in the usual manner (Right). (c) The suture thread is tied with consideration for the growth factor, completing the PV-RGEV reconstruction (arrowhead)
Results
Patient demographics
During the study period, a total of 16 patients underwent one-step TP (n = 4) or elective completion pancreatectomy (n = 12). The patient baseline characteristics are detailed in Table 1. Of these patients, 9 (56.2%) were men and 7 (43.7%) were women. The median age was 72 years (range: 52–84). Of the elective completion pancreatectomies, four were performed following DP (25%) and eight following PD (50%). Regardless of whether a one-step TP or a completion pancreatectomy was performed, the extent of gastric resection in all cases followed the resection line of a subtotal stomach-preserving PD. Splenectomy was performed in all cases, indicating that no spleen- and splenic vessel-preserving TP was performed, and two cases involved PV and SMV resections. Additionally, intraoperative GVC was identified in two patients (12.5%), leading to PV-RGEV side-to-side anastomosis. One patient underwent completion pancreatectomy following DP and the other underwent one-step TP.
Table 1.
Demographic characteristics of patients
| Variables | All (n = 16) |
|---|---|
| Age, years, (MD, range) | 72.0 (52–84) |
| Sex, n (%) | |
| Male | 9 (56.2) |
| Female | 7 (43.7) |
| BMI, kg/m2, (MD, range) | 19.1 (15.0-22.8) |
| ASA-PS, n (%) | |
| I-II | 13 (81.2) |
| III-IV | 3 (18.8) |
| Preoperative diagnosis, n (%) | |
| Malignant | |
| PDAC | 9 (56.2) |
| Metastases | 1 (6.2) |
| Non-malignant | |
| IPMN | 4 (25.0) |
| SCN | 1 (6.2) |
| Others | 1 (6.2) |
| Operative procedure, n (%) | |
| Total pancreatectomy | 4 (25.0) |
| Elective completion pancreatectomy | 12 (75.0) |
| Following DP | 4 (25.0) |
| Following PD | 8 (50.0) |
| PV/SMV resection, n (%) | 2 (12.5) |
| Intraoperative GVC, n (%) | |
| Yes | 2 (12.5) |
| No | 14 (87.5) |
| RGEV reconstruction, n (%) | |
| Yes | 2 (12.5) |
| No | 14 (87.5) |
Abbreviations: ASA-PS, American Society of Anesthesiologists–Physical Status; BMI, body mass index; DP, distal pancreatectomy; GVC, gastric venous congestion; IPMN, intraductal papillary mucinous neoplasm; MD, median; N, number; SCN, serous cystic neoplasm; SMV, superior mesenteric vein; PD, pancreatoduodenectomy; PDAC, pancreatic ductal adenocarcinoma; PV, portal vein, RGEV, right gastroepiploic vein
GVC
All 16 patients were classified based on intraoperative GVC and the number of gastric drainage veins preserved after TP, as summarized in Table 2. None of the cases preserved two or more of the three gastric drainage veins, including the LGV, RGV, and RGEV. Two cases in which no gastric drainage veins could be preserved developed intraoperative GVC and underwent PV-RGEV side-to-side anastomosis, which effectively improved GVC. No cases of GVC were observed during the postoperative follow-up period (mean duration: 39.8 months, range: 2.1–60.7 months).
Table 2.
Number of gastric drainage veins preserved after total pancreatectomy
| Operative procedures | Number of gastric drainage veins* | |||
|---|---|---|---|---|
| 3/3 | 2/3 | 1/3 | 0/3 | |
| Intraoperative GVC | ||||
| Yes | 0 | 0 | 0 | 2 |
| No | 0 | 0 | 14 | 0 |
*: Includes the left gastric vein, right gastric vein, and right gastroepiploic vein
Abbreviations: GVC, gastric venous congestion
Perioperative outcome after TP or elective completion pancreatectomy
The perioperative clinical characteristics of the patients are shown in Table 3. The overall major morbidity rate, defined as Clavien-Dindo classification grade ≥ IIIa, was 25% (n = 4), including bile leakage (n = 1), postoperative hematemesis (n = 1), pleural effusion with ascites (n = 1), and portal vein thrombosis (n = 1). The postoperative hematemesis was attributed to a rupture from esophageal varices, which had already been present preoperatively and had necessitated endoscopic variceal ligation. Esophagogastroduodenoscopy at the time of bleeding revealed no gastric varices. One patient, an 84-year-old male, died postoperatively from septic shock with pneumonia on postoperative day 88. No major complications were observed among two patients who underwent PV-RGEV anastomosis for GVC, with only one patient experiencing grade B delayed gastric emptying. Contrast-enhanced computed tomography one year after surgery in the case of gastric drainage vein reconstruction with PV-RGEV side-to-side anastomosis demonstrated good patency, adequate blood flow through the anastomotic site, and no evidence of GVC (Fig. 2).
Table 3.
Surgical outcome
| Variables | All (n = 16) |
|---|---|
| Operation time, min, (MD, range) | 387 (189–708) |
| Blood loss, mL, (MD, range) | 220 (100–2215) |
| Clavien–Dindo grade ≥ IIIa (%) | 4 (25.0) |
| Bile leakage, n (%) | 1 (6.2) |
| Postoperative hematemesis, n (%) | 1 (6.2) |
| Pleural effusion with ascites, n (%) | 1 (6.2) |
| Portal vein thrombosis, n (%) | 1 (6.2) |
| Postoperative stay, day, (MD, range) | 34 (17–166) |
Abbreviations: GVC, gastric venous congestion; MD, median; N, number
Fig. 2.
Postoperative imaging findings. Contrast-enhanced computed tomography scan with intravenous contrast one year after surgery shows good patency of the portal vein-right gastroepiploic vein (RGEV) side-to-side anastomosis (arrowhead) and good blood flow of RGEV (arrow), with no evidence of postoperative gastric venous congestion
Discussion
This study introduced the PV-RGEV side-to-side anastomosis technique for managing intraoperative GVC. TP can be performed with low mortality rates (0–3%) and an acceptable major morbidity rate of 39.9% (range 0–72%) in specialized high-volume centers [16–19]. In addition, it is reported that an annual TP-volume of > 20 was associated with reduced major morbidity (odds ratio = 0.225, 95% confidence interval, 0.097–0.521; p < 0.001) [7]. However, GVC remains a serious potential complication with a reported incidence of 5–28% [6, 9] and a potential link to elevated mortality, with a 90-day mortality rate of 7.4% in patients with GVC and 2.8% in those without GVC (p = 0.014) [8].
It has also been demonstrated that venous drainage may be compromised after TP, resulting in GVC and the need for partial or total gastrectomy to prevent gastric perforation [8]. When performing TP, it is crucial to consider the venous drainage pathways of the stomach, as inadequate drainage can lead to GVC. While postoperative changes or venous obstruction may necessitate consideration of collateral routes [20], preserving or reconstructing the gastric drainage veins is essential to prevent GVC. In the present series, intraoperative GVC was observed exclusively in cases where all gastric drainage veins were resected. Notably, no instances of GVC were detected following the reconstruction of these drainage routes. Although our results show a longer hospital stay, this is due to Japan’s healthcare system [21, 22] and our rigorous postoperative management, including strict glycemic control, which necessitates determining the final insulin dosage after stable oral intake is achieved.
Reports focusing on gastric venous reconstruction for GVC after TP are limited. A systematic literature search was conducted using the PubMed database on October 11, 2024, to identify published reports on gastric venous reconstruction for GVC after TP. The search terms used were as follows: “total pancreatectomy” AND “gastric venous congestion.” This search identified six English-language reports describing venous reconstruction for GVC. The characteristics of these reports, along with our case, are summarized in Table 4 [6, 9–13]. There were nine cases of venous reconstruction in total, with the LGV and RGEV most frequently used for reconstruction. Various anastomoses were performed: LGV–PV anastomosis, LGV–splenic vein anastomosis, LGV–inferior mesenteric vein anastomosis plus RGEV–colic vein anastomosis, and LGV–RGEV anastomosis. End-to-end anastomoses were most common, while side-to-side anastomosis was performed in only one case, specifically RGEV–left renal vein side-to-side anastomosis. No cases involved an RGEV–PV side-to-side anastomosis. To the best of our knowledge, this is the first report to suggest the efficacy and safety of PV-RGEV side-to-side anastomosis for improving GVC.
Table 4.
Summary of previous reports on gastric venous drainage reconstruction to improve gastric venous congestion
| Reference | Year | Type | Reconstruction case | Operative procedure | Venous reconstruction technique | |
|---|---|---|---|---|---|---|
| TP | CP | |||||
| Barbier et al. | 2013 | Original article | 3 | N/D | N/D | 1. Reconstruction of SpV |
| 2. Reconstruction of LGV | ||||||
| 3. Reconstruction of LGV+RGV | ||||||
| Hackert et al. | 2014 | Case report | 1 | N/D | N/D | LGV-PV end-to-side anastomosis |
| Nakao et al. | 2018 | Original article | 1 | 1 | 0 | RGEV-LOV end-to-end anastomosis |
| Kagota et al. | 2020 | Case report | 1 | 0 | 1 | LGV-SpV end-to-end anastomosis |
| Hatai et al. | 2023 | Case series | 1 | 1 | 0 | RGEV-LRV side-to-side anastomosis |
| Reddy et al. | 2024 | Case series | 2 | 2 | 0 | 1. LGV-IMV end-to-end anastomosis + RGEV-colic vein end-to-end anastomosis |
| 2. LGV-RGEV end-to-end anastomosis | ||||||
| Present cases | 2024 | Original article | 2 | 1 | 1 | RGEV-PV side-to-side anastomosis |
Abbreviations: CP, completion pancreatectomy; IMV, inferior mesenteric vein; LGV, left gastric vein; LOV, left ovarian vein; LRV, left renal vein; N/D, no data; PV, portal vein; RGEV, right gastroepiploic vein; RGV, right gastric vein; SpV, splenic vein; TP, total pancreatectomy
In the present study, the selection of the PV and RGEV for venous reconstruction was based on several technical advantages over other anastomosis options. First, the RGEV provides sufficient length, facilitating optimal exposure and access to the anastomosis site, which eliminates the need for extensive dissection and additional mobilization, simplifying the procedure. Additionally, the anatomical proximity between the PV and RGEV minimizes unnecessary tension on the anastomosis, supporting the long-term patency of the reconstruction. Furthermore, the RGEV was greatly dilated due to gastric congestion, which made it easier to perform a secure anastomosis. The side-to-side anastomosis technique offered distinct benefits, allowing for a larger anastomotic diameter that facilitated smoother venous outflow and, consequently, more effective reduction of gastric venous congestion. In addition, venous drainage of the gastric cardia is supported by the left inferior phrenic vein and the mucosal venous plexus at the gastroesophageal junction [23, 24]. Therefore, it may be reasonable to consider reconstructing the gastric venous drainage on the pyloric side via the right gastroepiploic vein. Rafael et al. reported a successful case of liver allograft inflow reconstruction with the PV-RGEV anastomosis for portal vein thrombosis in liver transplantation [25]. Further research is needed to evaluate the long-term patency and outcomes of RGEV-PV side-to-side anastomosis.
This study had several limitations. First, as a single-center, retrospective study with a small sample size, the findings may lack generalizability. Larger prospective, multicenter studies are needed to more accurately assess the effectiveness of gastric venous drainage reconstruction for GVC and to allow for robust comparisons between various anastomosis techniques, including RGEV-PV anastomosis. Additionally, although the operative records were detailed and accurate, the retrospective design of the study may introduce limitations in fully capturing nuances of vascular anatomy and resection, which could lead to potential underestimation of certain procedural details. Finally, as this study relies on a retrospective review, there is also an inherent risk of selection and reporting biases that may influence the observed outcomes.
Conclusion
In conclusion, the present study showed a novel gastric venous drainage technique in the event of intraoperative GVC during TP. In cases where preservation of gastric drainage veins is not feasible, PV-RGEV side-to-side anastomosis can be a convenient and useful option to resolve intraoperative GVC.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Acknowledgements
The authors wish to state that there are no acknowledgements for this study.
Author contributions
All authors contributed to the study’s conception and design. Material preparation, data collection and analysis were performed by K.A., R.Y. and A.S. The first draft of the manuscript was written by K.A. and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Data availability
No datasets were generated or analysed during the current study.
Declarations
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
No datasets were generated or analysed during the current study.