Comparison of postoperative results between types of pancreaticoenteral anastomosis after pancreaticoduodenectomy

Introduction

Study background, rationale and knowledge

Pancreaticoduodenectomy (PD) and other pancreatectomies are fundamental procedures for pancreatic disease treatment but are associated with high risk. The integrity of the pancreaticoenteral anastomosis is a key factor affecting outcomes. Despite improved surgical techniques and suturing materials, complications such as postoperative pancreatic fistula (POPF) and intra-abdominal abscesses (IAA) remain major concerns due to their impact on morbidity, mortality, and healthcare costs (1). POPF has been extensively studied over the past decade (2). Although techniques like pancreaticojejunostomy (PJ) and pancreaticogastrostomy (PG) have been refined, complication rates vary (3,4), and the enzymatic activity of the remnant pancreas remains a challenge (5). Various PJ techniques—two-layer anastomosis (6), Kakita (7), and Blumgart procedures (8)—have been developed. In Japan, a modified Blumgart method has become common (9), potentially influencing POPF rates. The International Study Group on Pancreatic Surgery (ISGPS) established standardized definitions to enable better outcome comparisons (10). Studies have emphasized risk factors including soft pancreatic texture, small ducts, and technical aspects (11,12).

Objective

New approaches like intraperitoneal drainage and antibiotics are being investigated to reduce POPF (13,14). IAA, delayed gastric emptying (DGE), and severe infections are often linked to anastomotic failure, reinforcing the need for tailored strategies (15). The principal author previously performed five types of pancreaticoenteral anastomosis—PG from 1994–1999 and PJ from 2000–2024—based on evolving trends. The Blumgart technique may offer benefits due to simplicity and adhesion area, though outcomes at our institute are yet to be confirmed. Thus, this study aims (I) to review 365 cases of five anastomosis types; (II) to assess POPF and IAA incidence; and (III) to identify related clinical and surgical factors for future improvement. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-380/rc).

Methods

Participants

This retrospective study included 365 patients treated consecutively by the principal author: 159 at Nagasaki University (1994–2015) and 206 at University of Miyazaki (2015–2024). The principal author directly managed all patients, and data were collected from institutional charts. The sample size was based on available patient data from two institutions. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study protocol was approved by the two institutions, and the study design was approved by the Ethics Review Boards of Nagasaki University (approval number: #25022005, approval date: February 20, 2025) and University of Miyazaki (approval number: #O-1623, approval date: October 29, 2024). Informed consent was obtained from all participants. Patient data were obtained from anesthetic records, hospital charts, and electronic medical records for initial hospitalization. Outcomes were determined by the co-author’s review of collected data.

Operative procedures and anastomosis techniques

Pancreatectomy types

Among the 365 patients, classical PD (Whipple) with distal gastrectomy was performed in 73 cases (20%), subtotal stomach-preserving PD (SSPPD) in 217 cases (60%) (16), pylorus-preserving PD (PPPD) in 72 cases (19%) (17), and central pancreatectomy in 3 cases (1%). For pancreatoenteric anastomosis, five methods were used consecutively: (I) PG via invagination (1994–1999, 24 cases) (Figure 1); (II) end-to-end invagination PJ (1997–1999; 8 cases; group PJI; 2%) (Figure 2); (III) two-layer PJ (2001–2010; 96 cases; group PJT; 26%) (Figure 3); (IV) Kakita PJ (2009–2015, 55 cases, group K, 15%) (Figure 4); and (V) modified Blumgart PJ (2015–2024, 182 cases, group B, 50%) (Figure 5). Inclusion criteria were clinically radical operations, and all consecutive patient data were collected by the principal author as the leading operator. Exclusion criteria were macroscopically non-radical PD.

Figure 1 PG with invagination method accompanied with one-layer suturing (group PG). This figure has obtained authorization from L&K Medical Art Creators, Inc. PG, pancreaticogastrostomy.

Figure 2 PJ with end-to-endo invagination method (group PJI). This figure has obtained authorization from L&K Medical Art Creators, Inc. PJ, pancreaticojejunostomy.

Figure 3 PJ with end-to-side adhere method accompanied with two-layer suturing (group PJT). This figure has obtained authorization from L&K Medical Art Creators, Inc. PJ, pancreaticojejunostomy.

Figure 4 Kakita PJ anastomosis (group K). This figure has obtained authorization from L&K Medical Art Creators, Inc. PJ, pancreaticojejunostomy.

Figure 5 The modified Blumgart PJ anastomosis (group B). This figure has obtained authorization from L&K Medical Art Creators, Inc. PJ, pancreaticojejunostomy.

Postoperative management and POPF definitions

Follow-up was conducted during hospitalization. Patients resumed oral intake gradually. Stress ulcer prophylaxis was administered with H2 blockers or omeprazole. Drainage tubes were continued or repositioned in grade B or C POPF per ISGPS (2,10). Octreotide was used regardless of its intestinal effects until fistulas resolved. DGE was defined by NG tube use >7 days or inability to resume a full diet within 14 days (18). Although grades B and C had different definitions, we evaluated both grades B and C together to indicate the clinically remarkable POPF in the present study simply. As the grade A of POPF was not clinically significant, non-POPF and grade A were examined as the non-clinical POPF in this study.

Tumor markers and histology

Preoperative blood samples were taken when patients were stable. Tumor markers were compared with pathology from resected specimens. Pancreatic cancer (PC) and bile duct cancer (BDC) were classified per the 7th editions of the respective General Rules by the Japan Pancreas Society (19) and Japanese Society of Hepato-Biliary-Pancreatic Surgery (20).

Statistical analysis

Categorical differences were analyzed using chi-square, Fisher’s exact, or Dunnett’s test (Tables 1,2). Continuous variables were evaluated using t-test or Mann-Whitney test. A P value of less than 0.05 was considered statistically significant in the univariate analysis. For the multivariate analysis, logistic regression identified independent risk factors with 95% confidence interval (CI) (Tables 2,3). Significance was set at P<0.05. Variables with univariate significance were used in multivariate analysis. SPSS version 23 (Chicago, IL, USA) was used.

Results

Perioperative parameters

The basic patient data of 365 patients were indicated as follows: male gender was 238 (65%) and a mean age of 68.0±10.3 years at the time of surgery (median 68, ranging from 14 to 87 years old). The disease was PC in 129 (35%), BDC in 94 (25%), ampullary cancer in 53 (15%), intraductal papillary mucin-producing cancer in 35 (10%), duodenal cancer in 15 (4%), neuroendocrine neoplasm in 15 (4%), gastrointestinal neoplasm in five, gall bladder cancer in five, pancreatitis in five, pancreatic metastasis (renal cancer) in three, obstructive cholangitis in two, trauma in two, and others in two. Background: The pancreatic architecture was normal in 241 patients (66%), accompanied by pancreatitis in 108 (30%), fragile fatty pancreas in 13 (3%), and chronic pancreatitis in three. Diabetes was observed in 101 patients (28%), and 149 patients (41%) were smokers. Preoperative laboratory data showed hemoglobin (mean 12.0±2.1 g/dL) and prothrombin activity (mean 94%±18%), total protein level (mean 6.7±0.6 g/dL), albumin level (mean 3.8±0.5 g/dL), alkaline phosphatase level (mean 406±438 U/L), choline esterase level (mean 234±91 U/L), amylase level (mean 137±184 mg/dL), total cholesterol level (mean 180±50 mg/dL), C-reactive protein (mean 0.48±1.04 mg/dL), hemoglobin A1c level (mean 5.8%±1.0%), and the preoperative nutrition index (mean 38±6).

Concerning pancreatectomy, the conventional Whipple procedure was performed in 73 patients, followed by SSPPD in 217, and pylorus-preserving PD in 75. Hepatectomy was simultaneously performed in three patients (1%) and combined vascular resection in 24 patients (7%). The mean blood loss was 1,223±872 mL. The mean operative time was 586±149 min. Red blood transfusions were administered to 129 patients (35%). Lymphadenectomies were performed as follows: D1 dissection in 23 patients (6%), D2 dissection in 284 (78%), and D3 dissection in 58 (16%). The suturing thread for the central pancreatic duct was 4-0 absorbable PDS (polydioxanone suture) II (J&J MedTech, New Brunswick, NJ, USA) in 103 patients (28%), 5-0 PDS in 215 (59%) and continuous suture by the non-absorbable 4-0 Prolene suture (J&J MedTech) in 47 (13%). Complete external tube drainage was performed in 15 patients (4%), partial external tube drainage in 206 (56%), and inner lost stent tube drainage in 144 (40%). Gastrojejunostomy, Billroth type 1, was performed in six (2%), type 2 in 347 patients (94%), and Roux-en-Y in 12 (4%), which included the antecolic approach in 348 (95%) and the retrocolic approach in 17 (5%). Jejunojejunostomy bypass was performed in 269 (74%) patients. Glue sealants were administered to 105 patients (29%). The resected specimens showed a soft pancreas in 237 patients (65%), fragile pancreas in 10 (3%), and stiff pancreas in 118 (32%). A dilated main pancreatic duct measuring >3 mm was observed in 109 (30%) patients.

Postoperative pancreatic complications were observed in 163 (45%) patients, including grade B or C POPF according to the ISGPS classification in 65 (18%) patients, intra-abdominal hemorrhage in nine (3%) patients, long-term ascites in 35 (10%) patients, IAA formation around the anastomotic site over seven days after surgery in 30 (8%) patients, and DGE in 37 (10%) patients. The median and mean days of postoperative oral intake were 6 and 10.8±11.7 days, respectively (range, 2–95 days). Re-operation was necessary in 10 (3%) patients during hospitalization, and the mean postoperative hospitalization period was 29.9±15.9 days, respectively. Insulin injections for diabetes were necessary at hospital discharge in 78 (22%) patients. Mortality was observed in one patient with cholangitis, which led to sepsis. During the 7 days after surgery, the lowest total protein and albumin levels were 5.0±0.7 and 2.6±0.4 g/dL, respectively. The highest total amylase level was 272±487 U/L. The lowest choline esterase and cholesterol levels were 152±78 U/L and 120±39 mg/dL, respectively.

Postoperative complications

Complications occurred in 163 (45%) patients: grade B/C POPF (65, 18%), hemorrhage (9, 3%), ascites (35, 10%), IAA (30, 8%), and DGE (37, 10%). Oral intake resumed in a median of 6 days (mean 10.8±11.7 days). Reoperation was required in 10 (3%). Median and mean hospital stays were 26 and 29.9±15.9 days. At discharge, 78 patients (22%) required insulin. One patient died of cholangitis-induced sepsis. Postoperative lowest protein/albumin: 5.0±0.7/2.6±0.4 g/dL; peak amylase 272±487 U/L; lowest cholinesterase/cholesterol: 152±78 U/L and 120±39 mg/dL.

Correlation between various clinicopathological, intraoperative, and postoperative parameters and the incidence of grade B/C POPF and prolonged ascites

Based on the above results, postoperative POPF and prolonged ascites associated with the types of anastomotic procedures were noted to analyze their relationship with the perioperative parameters shown in Table 1. With respect to risk factors for grade B/C POPF, statistical differences in demographics and clinical conditions tended to be observed between patients with grade B or C POPF and those with no or grade A POPF in terms of male sex (P=0.059); however, this difference was not significant. Habitual alcohol consumption was significantly associated with an increased risk of grade B or C POPF (P=0.008), suggesting its potential impact on pancreatic tissue fragility. As for preoperative laboratory data, higher creatinine levels were significantly associated with POPF development (P=0.047), and higher bilirubin levels tended to be observed with an increased risk of grade B/C POPF (P=0.09); however, this did not reach statistical significance. Regarding surgical records, the type of pancreatoenterostomy significantly influenced the risk of grade B/C POPF (P=0.007). Group B had the lowest POPF incidence, whereas groups PG and PJI showed the highest incidence rates. External pancreatic drainage was significantly more frequent in the complete drainage procedure group than in the other groups (P=0.008). Longer operative time was not significantly associated with grade B/C POPF (P=0.052). A soft or fatty pancreatic texture and a smaller main pancreatic duct were also significantly associated with grade B/C POPF (P<0.05). Pancreatic duct-to-mucosa anastomosis with Prolene running suture was significantly associated with grade B/C POPF (P<0.001). With respect to postoperative parameters, a longer period of oral intake (>4 days) and increased postoperative amylase levels (within 7 days) were significantly associated with grade B/C POPF (P<0.001). Patients with grade B/C POPF had significantly longer duration of hospital stay than those with none or grade A POPF (P<0.001).

As for risk factors for prolonged ascites, diabetes and habitual alcohol consumption tended to be associated with prolonged ascites. Regarding surgical records, group PJI had the highest rate of prolonged ascites (P=0.04). Increased blood loss (>1,000 mL) and related blood transfusions were significantly associated with prolonged ascites (P=0.007). Pancreatic duct-to-mucosa anastomosis with Prolene running suture was significantly associated with prolonged ascites (P<0.05). Patients with prolonged ascites were not significantly associated with the length of hospital stay compared with those without prolonged ascites.

Correlation with POPF and ascites

Correlation with POPF and ascites was indicated in Table 2. Grade B/C POPF was associated with alcohol use (P=0.008), elevated creatinine (P=0.043), soft/fatty pancreas (P<0.001), small ducts (P=0.02), and Prolene suture (P<0.001). POPF correlated with delayed oral intake (>4 days) and higher postoperative amylase (P<0.001). POPF patients had longer hospital stays (P<0.001). Prolonged ascites was linked to diabetes, alcohol, PJI anastomosis (P<0.001), blood loss >1,000 mL, transfusion (P=0.007), and Prolene sutures (P=0.047). Hospital stay was not significantly prolonged in these cases.

Independent risk parameters for Grade B/C POPF

Independent Risk Parameters for Grade B/C POPF were indicated in Table 3. Thirteen factors (P<0.10) were entered into logistic regression: male sex, alcohol use, high creatinine/bilirubin, PG or K anastomosis, complete drainage, long operative time, soft/fatty pancreas, small duct, Prolene suture, and delayed oral intake. In multivariate analysis, alcohol use, Kakita procedure (group K), soft/fatty pancreas, and delayed oral intake (>4 days) were independent risk factors for grade B/C POPF.

Discussion

PD is the standard for treating pancreatic head malignancies. Kurahara et al. reported no significant difference in postoperative albumin levels between SSPPD and PPPD, though body weight and albumin decreased for 6 months postoperatively (16,17). Recently, non-alcoholic steatohepatitis (NASH) has been associated with poor nutritional recovery after PD due to impaired lipid absorption and reduced blood flow (21). In this study, we analyzed risk factors and outcomes for grade B/C POPF and prolonged ascites after pancreatic surgery using five anastomotic techniques developed over nearly 30 years. Similar to prior studies (22-24), various perioperative variables were examined. Univariate and multivariate analyses confirmed habitual alcohol consumption, elevated bilirubin, soft pancreatic texture, and anastomotic method as independent risk factors for POPF (25). During the present series, the detection device of POPF and the enhanced recovery of surgery (ERAS) have been changed. For example, multi-slice detection computed tomography has been changed to 4-row since 2004, 16-row since 2008, and 64-row since 2014. Early drainage removal at postoperative day 4 and oral intake at day 3 have been begun since 2016. The oral food intake was given even during the occurrence of POPF. Before this period, the drainage removal period was defined by the decrease in amount at around day 7, and oral intake was not given during the POPF was found. These perioperative management may influence grade B/C POPF or its period. These changes would affect the hospitalization. However, hospitalization duration may be longer due to delayed ERAS, post-operative rehabilitation, or the problem of a too-generous health insurance system in our country in comparison with other countries, as shown by the present results of this study.

Kakita (group K) showed ~4× higher POPF risk compared to Blumgart (36% vs. 9%), likely due to differences in contact area—linear (Kakita) vs. broader surface (Blumgart) (26,27). The inadequate adhesion gap promotes pancreatic juice pooling and enzymatic inflammation, causing leaks (28). Prolonged ascites occurred more in the end-to-end invagination (PG) group, likely linked to low albumin or hepatic dysfunction. Although no severe cases occurred, jejunal juice leakage was observed under pressure. The method showed limited benefit in POPF prevention and had technical challenges aligning the pancreatic stump and jejunal opening (29). Our results support optimizing anastomotic technique and drainage. Blumgart showed better outcomes than Kakita, likely due to its broader tissue adhesion. As shown in Table 1, several clinicopathological and perioperative factors were associated with grade B/C POPF and ascites. Alcohol, but not smoking or diabetes (2,5,10,30,31), correlated with POPF, suggesting a direct link to parenchymal fragility. Elevated creatinine also indicated impaired healing.

PG showed higher POPF incidence than PJI or PJT. In PG, we used invagination without duct-to-mucosa suturing, which likely contributed to higher POPF rates (6,32). For small ducts (<2 mm), complete duct-to-mucosa suturing is difficult, especially with external drainage. Though vascular-like running sutures were attempted, they increased POPF and should be avoided. Early oral intake under ERAS protocols is ideal even post-PD (33), and our study suggests resuming nutrition within 7–10 days is beneficial. For ascites, low pre/postoperative protein and albumin were significant predictors, highlighting the importance of nutritional and hepatic status (34). Malnutrition from disease, diabetes, or alcohol abuse likely contributed. High blood loss and transfusions also increased the risk of ascites, probably due to increased infusion volume and third-space fluid shift. Low cholesterol postoperatively was associated with prolonged ascites, reflecting impaired lipid metabolism.

Prolonged ascites did not extend hospital stay, likely due to effective nutrition and diuretic management. In contrast, grade B/C POPF significantly lengthened stays and worsened outcomes, justifying our multivariate analysis (Table 3).

Independent risk factors for grade B/C POPF included: (I) anastomosis type (Kakita or PG), (II) soft pancreas texture, (III) small ducts, (IV) Prolene running sutures, (V) delayed oral intake. A soft, fatty pancreas or small duct—especially in alcohol users—was prone to leaks. In such cases, Blumgart’s tight, interrupted sutures with wide adhesion are safer than Kakita’s linear method. Pancreatic soft texture and small main duct were essential and independent risk factors of grade B/C POPF, as in the present study. Intraoperative ultrasound was a useful evaluation method to define the risk of anastomosis in a recent article (35). Anastomotic procedure can be selected during the operation using such a useful technology. Furthermore, the proper technique for small pancreatic duct patients using tiny coronary artery stents can be applied for any anastomosis to prevent pancreatic fistula (36). Prior reports confirm these findings (21,24,37,38). The modified Blumgart technique with duct-to-mucosa sutures is currently preferred (8,9,37,38). Our PG technique lacked precise mucosa-to-duct alignment, possibly increasing POPF. Better outcomes have been reported using layered anastomoses in PG (39-41). Today, we use interrupted absorbable sutures in Blumgart anastomosis for any pancreatic background. Oral intake should resume within 4 days, and high-risk patients may benefit from personalized techniques and close monitoring.

Limitations

This study’s problems include large sample size, consistent surgical technique by a single operator, and robust statistical methods. Comparing multiple anastomotic types yielded practical insights for surgical planning and complication prevention, emphasizing complete drainage and early nutrition. The retrospective design and evolving institutional protocols over 30 years introduce bias. Being a single-center study, external validation is needed. Long-term outcomes, such as nutritional recovery and quality of life, were not addressed. Lastly, despite statistical adjustments, residual confounders (e.g., surgeon experience, perioperative care differences) may affect interpretation. In the five groups, the group with the small number was included. In this situation, propensity score matching must be performed; however, the authors would like to show the real-world data despite the limited number. We specifically aimed to demonstrate the POPF-related problems in PG via invagination and end-to-end invagination PJ (n=8). To clarify statistically, although propensity score matching procedure would be considered, we selected to show the real-world actual data in this paper. In general, the number of operations was relatively limited per year; we selected the operations for which the principal author operated the leading operator. Considering these limitations, although we recommend selecting the anastomotic procedure, the POPF remarkably decreased compared with others. Therefore, we still believe that the weak recommendation can be achieved. Randomizing or collecting for the multi-institute examination would be difficult because such five anatomical procedures might be impossible.

Conclusions

This study found that habitual alcohol use, high bilirubin, soft pancreas, and certain anastomotic methods (PG without duct-to-mucosa or Kakita) increased POPF risk. Delayed oral intake predicted grade B/C POPF in 365 pancreatectomy patients. High blood loss, vascular resection, and low albumin prolonged ascites. In contrast, complete external drainage and early oral intake were protective. Surgeons should focus on blood conservation, nutrition, and optimal anastomosis. Future prospective studies are needed to confirm these results and refine prevention strategies.

Acknowledgments

We would like to thank Elsevier for English editing (reference number ASLESTD1101123 on February 20, 2024) and also thank L&K Medical Art Creators, Inc. (Tokyo, Japan) for the illustration of pancreatic enteric anastomosis.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-380/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-380/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-380/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-380/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study protocol was approved by the two institutions, and the study design was approved by the Ethics Review Boards of Nagasaki University (approval number: #25022005, approval date: February 20, 2025) and University of Miyazaki (approval number: #O-1623, approval date: October 29, 2024). Informed consent was obtained from all participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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