Abstract
Objective
To evaluate the value of mesenteric approach for borderline resectable pancreatic head cancer (BRPHC).
Methods
According to the inclusion and exclusion criteria, the data of 203 patients with borderline resectable pancreatic head cancer (BRPHC) who underwent radical pancreatoduodenectomy in our center from January 2011 to December 2023 were retrospectively analyzed. After detecting the superior mesenteric artery in infracolic compartment to judge that there was vascular invasion but it met the borderline resection criteria, the blood supply was cut off first, then the tissues and organs were resected. And the invaded vessels were resected and reconstructed or replaced, then conventional anastomosis was performed. All patients were divided into mesenteric approach group and conventional approach group according to the operation method. The outcome measures were operation completion, perioperative conditions and overall prognosis. The follow-up time was up to February 2025.
Results
All 203 patients successfully completed the operation without perioperative death, and confirmed as pancreatic ductal adenocarcinoma by pathological examination. Overall and grouped prognosis: The overall survival rates and disease-free survival rates of 1-, 2-, and 5-year were 51.9%, 25.0%, 8.5% and 28.4%, 12.9%, 3.9% (Fig. 1). The 1-, 2-, and 5-year survival rates of patients in two groups were 62.1%, 40.3%, 21.7% and 44.1%, 14.7%, 1.8% (P = 0.000, X2 = 20.927) (Fig. 2A); The 1-, 2-, and 5-year disease-free survival rates in two groups were 44.9%, 24.5%, 8.2% and 20.8%, 7.5%, 1.9% (P = 0.006, X2 = 7.457) (Fig. 2B).
Conclusion
The mesenteric approach in infracolic compartment can improve the prognosis of patients with borderline resectable pancreatic head cancer, prolong the postoperative survival time of patients, and reduce the recurrence.
Keywords: Mesenteric approach, Radical pancreatoduodenectomy, Prognosis, Borderline resectable pancreatic head cancer
Introduction
Pancreatic adenocarcinoma remains a lethal malignancy, with 5-year survival rates below 5% for advanced stages. At present, the major treatment is still surgical resection [1]. The 5-year survival rate after radical pancreatoduodenectomy can reach 15%~25%, recent advances in multimodal therapy have improved 5-year survival to 30–43% [2]. According to the AJCC pancreatic cancer guidelines, it can be divided into stage 0 to IV [3–5]. According to the AJCC staging system, pancreatic malignancies are classified as follows: stage 0(carcinoma in situ), stages I-II(surgically resectable), and stages III-IV(unresectable). However, clinical practice frequently identifies cases with intermediate features between stages III and IV, categorized as borderline resectable pancreatic carcinoma. This entity is radiologically defined by any of the following criteria:①Limited hepatic artery involvement(sparing the celiac trunk) amenable to segmental resection with reconstruction; ②Superior mesenteric artery (SMA) invasion confined to ≤ 180° of the vessel circumference; ③Tumor encroachment on the superior mesenteric vein (SMV), portal vein, or their confluence, with feasibility of vascular resection and reconstruction.
However, the surgery for pancreatic cancer is difficult, and the anatomical relationship of organs surround the pancreatic head is complex [6]. Traditional surgical methods such as radical surgery and extended radical surgery for pancreatic cancer often have shortcomings such as incomplete tumor resection and high recurrence rate [7]. In order to achieve the radical resection, mesenteric approach in infracolic compartment is recommended, which firstly investigate the blood vessels and adjacent tissues, cut off the relevant blood supply, and then perform pancreatoduodenectomy [8].This study discussed the application value of mesenteric approach in infracolic compartment for surgical treatment of borderline resectable pancreatic head cancer.
Objective
To evaluate the clinical efficacy of the mesenteric approach in the borderline resectable pancreatic head cancer (BRPHC) by comparing its surgical outcomes, survival benefits, and recurrence rates with those of conventional surgical techniques, then assess the impact of early vascular control, R0 resection rates, and systematic neurovascular dissection on long-term prognosis and tumor recurrence.
Methods
Patient screening
Based on the 2022 National Comprehensive Cancer Network (NCCN) Guidelines for Pancreatic Adenocarcinoma [9] and AJCC 8th Edition Staging System [10], clinical records of individuals diagnosed with borderline resectable pancreatic head carcinoma (BRPHC) were retrospectively reviewed. The criteria for determining tumor resectability (borderline resectable pancreatic head cancer, BRPHC) described in the manuscript are Between 2011 and 2023, 203 patients underwent radical pancreatoduodenectomy at our center, with surgical strategies categorized into mesenteric approach group(n = 88) and conventional approach group(n = 115). The study protocol adhered to the Declaration of Helsinki and received formal approval from the Ethics Committee of Beijing Chaoyang Hospital(Approval No.2024-D-511). Written informed consent was secured from all participants and their legal representatives prior to data inclusion.
Inclusive criteria: (1) Age range (29–81 years old); (2) Postoperative pathology confirmed pancreatic ductal adenocarcinoma in the head of the pancreas; (3) No distant metastasis in preoperative comprehensive evaluation; (4) Preoperatively evaluated as borderline resectable according to the 2022 National Comprehensive Cancer Network(NCCN) guidelines [9]; (5) No contraindication in preoperative evaluation; (6) Informed consent of patients and their families; (7) Complete clinical and pathological data.
Exclusion criteria: (1) Patients with resectable or unresectable pancreatic head cancer evaluated according to NCCN guidelines(2022); (2) Patients without pancreatic cancer confirmed by postoperative pathological examination; (3) New adjuvant treatment before operation; (4) Incomplete clinical and pathological data.
Patient grouping and definition
Participants were stratified into two cohorts based on operative techniques: mesenteric approach cohort(n = 88) and conventional approach cohort(n = 115). The time period we included spans from 2011 to 2023. To mitigate temporal bias, patients enrolled during this 13-year period were divided into an early cohort (2011–2016, n = 55) and a late cohort (2017–2023, n = 148) for inter-group comparison. The infracolic mesenteric approach procedure involved the following steps: ①Abdominal access: A supraumbilical transverse arcuate incision was created for exploratory laparotomy. ②Mesenteric exposure: The serosal layer at the mesenteric root was incised to expose the infracolic compartment. ③Vascular dissection: The SMA was systematically dissected and mobilized from the tumor bed, followed by ligation of the first jejunal artery and inferior pancreaticoduodenal artery. ④Radical clearance: En bloc resection included complete excision of station 14 lymph nodes and retroperitoneal neurovascular connective tissues. If the SMA could be completely stripped to the root of the abdominal aorta smoothly, it was preliminarily judged that the tumor could achieve radical resection. If SMA was found to be seriously involved which could not be completely stripped, it was difficult to achieve radical resection. Surgical strategies were individualized based on intraoperative anatomical and pathological assessments. Following this, the gastrocolic ligament was divided, and the anterior layer of the transverse mesocolon was mobilized to access the lesser sac. Subsequent evaluation confirmed that superior mesenteric vein (SMV) involvement was limited to < 180° of the vascular circumference. Moreover, the gastric body, pancreatic body, jejunum and bile duct were removed in turn, then end to end anastomosis or vascular replacement was performed after the affected segment of SMV was resected. Finally, pancreaticojejunostomy, cholangiojejunostomy, gastrointestinal anastomosis and enteroenterostomy were performed in turn.
The conventional approach procedure employed a Kocher maneuver to assess tumor resectability. Key steps included: ①Pancreatic head mobilization: The pancreatic head was dissected from surrounding structures.②Vascular skeletonization: Sequential dissection of the gastric and colonic trunks, common hepatic artery, celiac axis, and superior mesenteric artery (SMA) was performed to isolate major vascular pedicles.③Lymphadenectomy: Systematic clearance of perivascular lymphatic tissues was conducted to achieve oncological radicality. What’s more, cut off the stomach, pancreas, jejunum and bile duct respectively, then performed end-to-end anastomosis or vascular replacement after cutting off the affected segment of SMV. Finally, pancreaticojejunostomy, cholangiojejunostomy, gastrointestinal anastomosis and enteroenterostomy were performed successively.
Parameters and follow-up
Postoperative evaluation: histopathological analysis, documented complications, and functional recovery status were recorded.
Follow-up protocols: telephonic interviews and outpatient clinical assessments, with longitudinal monitoring extending through February 2025.
Statistical analysis
Continuous variables with normal distribution were presented as mean ± standard deviation, whereas nonparametric data were denoted by median (interquartile range). For categorical comparisons, Fisher’s exact test was applied. Normally distributed continuous variables were analyzed using independent two-sample t-tests, while non-normally distributed metrics were evaluated via the Mann-Whitney U test. Kaplan Meier method was used to calculate the survival curve. Log rank test was used to compare the survival rate between the two groups. The P < 0.05 meant the difference was statistically significant. All data were analyzed by SPSS 24.0 software. No AI tools were used at any stage of research or preparation of manuscripts.
Results
General data
The general data between the two groups were shown in Table 1. Preoperative condition: There were 203 patients in this group, including 109 males and 94 females, age 62(54,68)years(range:29 ~ 81years), 51 patients had smoking history and 65 patients had diabetes history. The first symptoms mainly included 72 cases of jaundice(61 patients were treated with preoperative biliary drainage, including 25 patients with ERCP biliary stent implantation and 36 patients with PTBD catheter drainage), 96 cases of abdominal pain, 10 cases of atypical gastrointestinal symptoms, and 25 cases of physical examination. 133 patients received neoadjuvant therapy. There was a similar distribution of gender, age, smoking history, diabetes history, preoperative biliary drainage, neoadjuvant therapy and CA199 between the two groups(p > 0.05). Operation completion: All patients was successfully completed the operation without perioperative death. The hemorrhage was 600(50-4000)ml(range:50-4000 ml), blood transfusion was performed in 116 patients, and the operation time was (13.1 ± 3.1)h(range:7–26 h). Postoperative condition: All patients were confirmed as pancreatic ductal adenocarcinoma by pathological examination. The tumor differentiation degree showed that poorly differentiated 80 cases(39.4%), moderately-well differentiated 123 cases(60.6%). The tumor size was (4.0 ± 1.8)cm(range: 1.5–13.0 cm). The lymph node dissection number was 26(19,33) (range: 3–73), and 146 patients(71.9%) were positive. There were 178 patients(87.7%) with radical(R0) resection, 12 patients(5.9%) with positive margin of bile duct, 10 patients(4.9%) with positive margin of pancreatic stump, and 3 patients(1.5%) with positive margin of superior mesenteric vein. All patients exhibited venous involvement, defined as tumor infiltration of the SMV/PV or confluence with ≤ 180° circumferential involvement. The limited extent of vascular invasion allowed curative resection and reconstruction (via end-to-end anastomosis or graft replacement), qualifying as Borderline Resectable with Portal Vein Involvement(BR-PV). These cases were subclassified per our center’s proprietary venous invasion classification system (Chaoyang Classification Criteria) for vascular invasion of pancreatic cancer, including 14 cases of type I(6.9%), 89 cases of type II(43.8%), 87 cases of type III(42.9%), and 13 cases of type IV(6.4%). Our center’s Chaoyang Classification Criteria categorizes cases into four distinct types, each requiring tailored reconstruction strategies: Type I: Tumor involvement limited to the lateral wall of the portal vein (PV).The Chaoyang classification of portal vein system invasion proposed by our center divides it into four types: Type I tumors invade the lateral wall of the portal vein, and direct suturing or patch like allogeneic vein reconstruction is used to avoid vascular stenosis after direct suturing. Type II tumors invade segmental blood vessels, and end-to-end anastomosis or tubular allogeneic vein reconstruction is used to avoid concerns about excessive anastomotic tension and insufficient resection range. Type III tumors invade the confluence of the portal vein system, and a branch of allogeneic vein is used to completely reconstruct the portal vein, splenic vein, and superior mesenteric vein to avoid regional portal hypertension. Type IV tumors invade the confluence of the portal vein system upwards and the branches of the superior mesenteric vein downwards, and are reconstructed by extracorporeal shaping and splicing of allogeneic branch blood vessels. Additionally, 33 patients presented with Borderline Resectable with Arterial Involvement(BR-A), accounting for approximately 14.3%, 13 patients exhibited hepatic artery(HA) invasion while 20 patients demonstrated superior mesenteric artery (SMA) involvement. No significant differences were observed in the inter-group comparisons between the two time-stratified cohorts.
Table 1.
Comparison of general data between the two groups
| Parameters | Mesenteric approach group (n = 88) | Conventional approach group (n = 115) | Statistical value | P value |
|---|---|---|---|---|
| Gender Male/Female | 64.0%/36.0% | 58.3%/41.7% | 0.397 | 0.529 |
| Age(range, year) | 59[37–81] | 63[29–81] | 1.424 | 0.155 |
| Smoking Yes/No | 18.0%/82.0% | 27.8%/72.2% | 1.557 | 0.212 |
| Diabetes Yes/No | 40.0%/60.0% | 25.0%/75.0% | 2.751 | 0.097 |
| Biliary drainage Yes/No | 20.0%/80.0% | 22.2%/77.8% | 0.087 | 0.768 |
|
CA19-9(U/ml) ≤ 37/>37 |
28/60 | 25/90 | 2.625 | 0.105 |
| Neoadjuvant therapy Yes/No | 62/26 | 71/44 | 1.676 | 0.195 |
| Hemorrhage(range, ml) | 600[200–4000] | 800[50-2800] | 0.286 | 0.775 |
| Blood transfusion Yes/No | 49/39 | 68/47 | 0.243 | 0.622 |
| Operative time(h) | 12[7–18] | 12[6–26] | 0.445 | 0.656 |
| Tumor diameter(cm) | 4.2[1.5–13.0] | 3.9[1.5–12.0] | 1.327 | 0.184 |
| Tumor differentiation poorly/moderately-well | 37/51 | 43/72 | 0.452 | 0.501 |
| Adjuvant therapy Yes/No | 46.0%/54.0% | 41.7%/58.3% | 3.657 | 0.056 |
| Postoperative hospitalization time (d) | 21[11–82] | 22[12–106] | 0.562 | 0.574 |
| Lymph nodes harvested | 27[5–73] | 25[3–57] | 2.153 | 0.031 |
| Lymph node metastasis Yes/No | 61/27 | 85/30 | 0.521 | 0.470 |
| Perineural invasion Yes/No | 98.0%/2.0% | 98.6%/1.4% | 1.452 | 0.228 |
|
Nature of resection (R0*,R1) |
84/4 | 94/21 | 8.684 | 0.003 |
| TNM stage | 0.135 | 0.713 | ||
| II | 49 | 67 | ||
| III | 39 | 48 | ||
| Vascular invasion classification | 3.405 | 0.333 | ||
| I | 3 | 11 | ||
| II | 42 | 47 | ||
| III | 38 | 49 | ||
| IV | 5 | 8 | ||
| BR-A* | 15 | 18 | 0.071 | 0.790 |
| Application time early/late cohort | 21/67 | 34/81 | 0.820 | 0.365 |
*R0 resection: Defined as microscopically negative margins (≥ 1 mm clearance).
BR-A: Limited hepatic artery involvement(sparing the celiac trunk) amenable to segmental resection with reconstruction; Superior mesenteric artery(SMA) invasion confined to ≤ 180°of the vessel circumference.
According to Table 2, no statistically significant difference was observed in adjuvant therapy initiation rates between the two groups (54.5% vs. 45.2%, P = 0.195), suggesting that surgical approach selection may not substantially influence postoperative adjuvant therapy decision timing. The mesenteric approach group demonstrated a higher treatment completion rate (68.8% vs. 59.6%, P = 0.342), while not statistically significant, was accompanied by significantly fewer treatment discontinuations due to disease progression (12.5% vs. 26.9%, P = 0.042).
Table 2.
Intergroup comparison of adjuvant therapy
| Parameter | Mesenteric Approach Group (n = 88) | Conventional Approach Group (n = 115) | Statistical value | P-value |
|---|---|---|---|---|
| Adjuvant therapy initiation rate | 54.5% (48/88) | 45.2% (52/115) | 1.68 | 0.195 |
| Median time to initiation (days) | 45 [32–78] | 48 [35–90] | 1.06 | 0.287 |
| Treatment completion rate (≥ 6 cycles) | 68.8% (33/48) | 59.6% (31/52) | 0.91 | 0.342 |
| Primary reasons for discontinuation | ||||
| Disease progression | 12.5% (6/48) | 26.9% (14/52) | 4.13 | 0.042 |
| Toxicity | 18.8% (9/48) | 13.5% (7/52) | 0.57 | 0.452 |
Complications
The complications were shown in Table 3. All postoperative complications were prospectively graded according to the Clavien-Dindo classification. 87 cases(42.9%) had postoperative complications. Postoperative pancreatic fistula occurred in 20 cases(9.9%), including 9 cases(4.4%) of biochemical fistula, 3 case(1.5%) of grade B pancreatic fistula, and 8 cases(3.9%) of grade C pancreatic fistula. There were 23 cases(11.3%) of gastric emptying disorder, 17 cases(8.4%) of abdominal infection, 8 cases(3.9%) of abdominal hemorrhage, 8 cases(3.9%) of gastrointestinal hemorrhage, 8 cases(3.9%) of diarrhea and et al. The median postoperative hospitalization time was 24(18,36) days(range 2-106 days).
Table 3.
Comparison of complications between the two groups
| Parameters | Mesenteric approach group (n = 88) | Conventional approach group (n = 115) | Statistical value | P value |
|---|---|---|---|---|
| Postperative complications Yes/No | 37/51 | 40/75 | 1.117 | 0.291 |
| Biochemical leakage | 5 | 4 | 0.571 | 0.450 |
| Grade B pancreatic fistula | 1 | 2 | 0.124 | 0.724 |
| Grade C pancreatic fistula | 4 | 4 | 0.150 | 0.699 |
| Gastric emptying disorder | 12 | 11 | 0.823 | 0.365 |
| Abdominal infection | 8 | 9 | 0.104 | 0.747 |
| Abdominal hemorrhage | 4 | 4 | 0.150 | 0.699 |
| Portal vein thrombosis | 1 | 2 | 0.124 | 0.724 |
| Liver or kidney failure | 1 | 2 | 0.124 | 0.724 |
| Biliary fistula | 1 | 1 | 0.036 | 0.849 |
| Intestinal fistula | 0 | 2 | 1.546 | 0.214 |
| Pulmonary infection | 1 | 2 | 0.124 | 0.724 |
| Lymphatic fistula | 2 | 2 | 0.074 | 0.786 |
| Gastrointestinal hemorrhage | 3 | 5 | 0.116 | 0.733 |
| Diarrhea* | 3 | 5 | 0.116 | 0.733 |
| Myocardial infarction | 1 | 3 | 0.560 | 0.455 |
*Diarrhea was defined as the passage of > 3 watery stools (Bristol Stool Scale type 6 or 7) per day persisting for > 48 h postoperatively, requiring therapeutic intervention (e.g., antidiarrheal agents, electrolyte replacement), according to the Clavien-Dindo criteria.
Overall long term prognosis
Patients were monitored longitudinally through February 2025, with a median observation duration of 38 months. Within this period, adjuvant therapy was administered to 100 participants (49.3%). The calculated median overall survival and disease-free survival were 13 months and 7 months respectively, and the overall survival rates and disease-free survival rates of 1-, 2-, and 5-year were 51.9%, 25.0%, 8.5% and 28.4%, 12.9%, 3.9% (Fig. 1).
Fig. 1.
Long-term prognosis of patients with borderline resectable pancreatic head cancer undergoing radical pancreatoduodenectomy (n = 203). A, overall survival curve; B, tumor-free survival curve
Grouping long term prognosis
As of February 2025, the median overall survival of patients in the mesenteric approach group and the conventional approach group was 17 months and 10 months respectively, and the 1-, 2-, and 5-year survival rates of patients in two groups were 62.1%, 40.3%, 21.7% and 44.1%, 14.7%, 1.8% (P = 0.000, X2 = 20.927) (Fig. 2A); The median disease-free survival of mesenteric approach group and conventional approach group was 10 months and 6 months respectively, and the 1-, 2-, and 5-year disease-free survival rates in two groups were 44.9%, 24.5%, 8.2% and 20.8%, 7.5%, 1.9% (P = 0.006, X2 = 7.457) (Fig. 2B).
Fig. 2.
Long-term prognosis of patients with borderline resectable pancreatic head cancer undergoing radical pancreatoduodenectomy in the mesenteric approach group (n = 88) and the conventional approach group (n = 115). A, overall survival curve; B, tumor-free survival curve
Univariate analysis and multivariate analysis
Prognostic factors influencing long-term survival and recurrence-free outcomes in pancreatic head carcinoma patients were analyzed through univariable and multivariable analysis, with comprehensive results tabulated in Tables 4 and 5. In the univariate analysis, age, tumor differentiation, nature of resection, Lymph node metastasis, adjuvant therapy, mesenteric approach, TNM stage had significant effect on long-term survival; tumor differentiation, nature of resection, lymph node metastasis, mesenteric approach had significant effect on disease-free survival of patients. Then these indicators were included into multivariate analysis respectively. Then the result showed that age, tumor differentiation, nature of resection, lymph node metastasis, mesenteric approach and TNM stage could influence long-term survival of patients; tumor differentiation, nature of resection, lymph node metastasis and mesenteric approach could influence recurrence of patients.
Table 4.
Univariate analysis and multivariate analysis of long-term survival for patients with borderline resectable pancreatic head cancer
| Univariate analysis | Multivariate Cox regression analysis | |||||
|---|---|---|---|---|---|---|
| Factors | Median survival time(month) | χ2 value | P value | RR value | 95% CI | P value |
| Age(60 years old) | 13 | 4.763 | 0.029 | 1.573 | 1.125–2.199 | 0.008 |
| CA19-9(37U/ml) | 13 | 2.105 | 0.147 | |||
| Neoadjuvant therapy | 13 | 1.976 | 0.160 | |||
| Hemorrhage (500 ml) | 13 | 3.701 | 0.054 | |||
| Tumor differentiation | 13 | 10.019 | 0.002 | 1.666 | 1.211–2.291 | 0.002 |
|
Nature of resection (R0,R1) |
13 | 17.783 | 0.000 | 0.562 | 0.355–0.888 | 0.014 |
| Lymph nodes harvested(20) | 13 | 0.051 | 0.822 | |||
| Lymph node metastasis | 13 | 10.790 | 0.001 | 0.586 | 0.386–0.890 | 0.012 |
| Adjuvant therapy | 13 | 9.293 | 0.010 | 1.290 | 0.944–1.764 | 0.110 |
| Mesenteric approach | 13 | 20.927 | 0.000 | 1.621 | 1.155–2.275 | 0.005 |
| Vascular invasion classification | 13 | 0.083 | 0.994 | |||
| TNM stage | 13 | 32.007 | 0.000 | 1.450 | 1.015–2.027 | 0.041 |
| Postperative complications | 13 | 1.520 | 0.201 | |||
Table 5.
Univariate analysis and multivariate analysis of recurrence time for patients with borderline resectable pancreatic head cancer
| Univariate analysis | Multivariate Cox regression analysis | |||||
|---|---|---|---|---|---|---|
| Factors | Median survival time(month) | χ2 value | P value | RR value | 95% CI | P value |
| Age(60 years old) | 7 | 0.013 | 0.911 | |||
| CA19-9(37U/ml) | 7 | 0.525 | 0.469 | |||
| Neoadjuvant therapy | 7 | 0.015 | 0.904 | |||
| Tumor differentiation | 7 | 9.882 | 0.002 | 1.756 | 1.256–2.455 | 0.001 |
|
Nature of resection (R0,R1) |
7 | 11.022 | 0.001 | 0.439 | 0.275–0.701 | 0.001 |
| Lymph nodes harvested(20) | 7 | 0.223 | 0.636 | |||
| Lymph node metastasis | 7 | 10.869 | 0.001 | 0.554 | 0.374–0.820 | 0.003 |
| Adjuvant therapy | 7 | 3.861 | 0.145 | |||
| Mesenteric approach | 7 | 11.926 | 0.001 | 1.539 | 1.090–2.173 | 0.014 |
| Vascular invasion classification | 7 | 0.560 | 0.905 | |||
Discussion
In our study, we found the lymph node harvested and the R0 resection rate were greater in the mesenteric approach group, which might lead to the lower incidence of regional recurrence. Furthermore, our study showed age, tumor differentiation, nature of resection, mesenteric approach and TNM stage could influence long-term survival of patients; tumor differentiation, nature of resection and mesenteric approach could influence recurrence of patients. Finally, we observed the prolonged disease-free time and overall survival time in patients of mesenteric approach group.
According to the American Cancer Society (ACS, 2020), pancreatic head carcinoma exhibits a dismal 5-year survival rate of 9% [11]. Pancreatoduodenectomy remains the sole curative intervention for resectable cases, though achieving R0 resection poses significant challenges. Positive superior mesenteric artery (SMA) margins are strongly associated with local recurrence, as evidenced by a meta-analysis of 23 studies (n = 3,815) reporting recurrence rates of 7–69% and SMA margin positivity in 15–35% of cases [12]. Notably, patients with positive SMA margins demonstrated substantially higher recurrence rates compared to those with negative margins (66% vs. 45%, p = 0.005). Furthermore, anatomical variations in arterial origin or trajectory may predispose patients to intraoperative vascular injury, hemorrhagic complications, and postoperative ischemic sequelae affecting hepatic, intestinal, and biliary systems. And the postoperative survival rate is not ideal [13–15]. The artery-prioritized surgical strategy involves initial exploration and assessment of the superior mesenteric artery (SMA) within the infracolic compartment to determine tumor resectability. This approach systematically ligates tumor-associated vasculature prior to specimen resection, followed by standardized anastomotic reconstruction. By prioritizing vascular infiltration evaluation, this technique critically determines the feasibility of radical resection, thereby exerting substantial prognostic influence on patient outcomes. [16, 17].
Our study implemented an infracolic superior mesenteric artery (SMA)-first surgical protocol [18], aligning with contemporary evidence from Vallance et al. [19], where posterior SMA-prioritized dissection in 80 patients yielded superior 6-month survival compared to conventional techniques (95% vs. 80%). This survival advantage parallels our observations. Furthermore, corroborating findings from Du et al. [20] demonstrated enhanced R0 resection rates (85.7% vs. 62.5%) and reduced postoperative recurrence (7.1% vs. 28.1%) with artery-first strategies, substantiating our clinical outcomes.
The mesenteric approach for pancreatoduodenectomy, pioneered by Nakao et al. [21], introduced a paradigm shift in surgical oncology. This technique initiates dissection from non-neoplastic tissue planes, enabling precise assessment of disease-free margins and resectability prior to performing comprehensive perimesenteric arterial lymphadenectomy. Key procedural advantages include early vascular control that proximal ligation of the inferior pancreaticoduodenal artery and dorsal pancreatic arterial branches originating from the SMA; Radical neurolysis that complete en bloc excision of the mesopancreas complex, encompassing the secondary neural plexus of the pancreatic head. Similar to our study, the mesenteric approach was to explore along the artery in turn, dissect the perivascular tissue and lymph node dissection during the exploration. Besides, the artery-prioritized technique demonstrated distinct oncological advantages, this approach facilitated more extensive nodal basin dissection, achieving higher R0 resection rates (85.7% vs. 62.5%) through complete tumor microenvironment clearance, thereby minimizing residual lesions and recurrence risks. Moreover, the strategy effectively decreased mechanical tumor cell dispersion, correlating with improved disease-free survival (DFS: 62.8% vs. 40.4%, P = 0.003) and overall prognosis by limiting intraoperative manipulation of tissues.
While previous studies have reported on mesenteric approach, we acknowledge the foundational work of Hirono S et al. published in Annals of Gastroenterological Surgery (2017) [22] and the ongoing Trials, our investigation demonstrates several distinct advantages. Firstly, our study builds upon but significantly extends prior research on the mesenteric approach for pancreaticoduodenectomy, particularly in borderline resectable pancreatic head cancer. Secondly, we took technical refinements that basic SMA-first approach combined neurovascular sheath dissection and standardized venous reconstruction. Third, our study demonstrated a remarkable survival benefit with the mesenteric approach, achieving a 5-year overall survival rate of 21.7%, doubling the historical benchmarks (typically < 10%). Therefore, our work does not duplicate but rather advances prior research by: Focusing exclusively on BR-PDAC with updated surgical techniques; Providing the first evidence that optimized mesenteric approaches can overcome historical BR-PDAC survival barriers; Establishing a framework for integrating surgical quality with systemic therapy efficacy. These contributions justify independent publication while properly contextualizing prior work.
Furthermore, pancreatic cancer with vascular invasion was a loss of opportunity for surgery in the past [23]. But nowadays, the proposal of borderline resectable pancreatic head cancer and the application of mesenteric approach have enabled most patients with vascular invasion of pancreatic cancer to continue their lives [24]. Pancreatic head is located in a special position and connected with a variety of important vascular structures, including the celiac trunk, hepatic artery, superior mesenteric artery, portal vein system, etc., which makes it vulnerable to vascular invasion and metastasis [25–27]. The characteristic of borderline resectable pancreatic head cancer is that the tumor has vascular invasion but can be resected and reconstructed. Before carrying out routine whipple, it is necessary to evaluate whether there is vascular invasion or distant metastasis, and whether the involved vessels can be resected and reconstructed. All above directly determines if the surgical principles, surgical resection scope and R0 resection can be achieved, which is of great significance for the survival and prognosis of patients. The mesenteric approach in infracolic compartment can well realize the exploration of vascular invasion and metastasis before whipple, so as to determine whether the operation continues. If the exploration finds that the tumor invades the celiac trunk artery, or the invasion of the superior mesenteric artery exceeds 180°, or it is judged that the involved artery cannot be removed and reconstructed, the opportunity for surgery has been lost. Moreover, if any of the following three conditions are found during exploration: firstly, the tumor invades a short segment of hepatic artery but not the celiac trunk artery; secondly, the invasion range of the superior mesenteric artery does not exceed 180°;third, it invades the superior mesenteric vein, portal vein, or the junction but whipple with vascular resection, reconstruction and replacement are feasible to achieve R0 resection.In the process of mesenteric approach, the blood supply of the resected tissue can be ligated to cut the segment preferentially, which facilitates the subsequent organ resection, reduces the number of removal of the resected organ, and reduces the spread of tumor cells caused by removal. At the same time, it can clean the lymphatic tissue around its blood vessels more comprehensively to achieve thoroughly radical cure. For the surgeon, the mesenteric approach facilitates the judgment of its anatomical structure, and also increases the accuracy of the operation.
In addition to its advantages in achieving radical resection, the mesenteric approach may also exert a positive influence on adjuvant therapy. In our study, the mesenteric approach group demonstrated a higher treatment completion rate (68.8% vs. 59.6%, χ²=0.91, P = 0.342). Although this difference did not reach statistical significance, when combined with the analysis of discontinuation reasons, the mesenteric approach group showed significantly fewer treatment interruptions due to disease progression (12.5% vs. 26.9%, χ²=4.13, P = 0.042). This finding may reflect the oncological advantages conferred by the mesenteric approach technique, it may indicated that optimization of surgical techniques can enhance the efficacy of adjuvant therapy.
In summary, while the mesenteric approach technique did not significantly improve adjuvant therapy acceptance rates, it may have enhanced treatment effectiveness by improving local tumor control (reduced risk of intraoperative dissemination and more thorough resection). This provides new clinical evidence supporting the theory that “surgical quality affects systemic treatment outcomes.” Future prospective studies should standardize adjuvant treatment protocols and further analyze the synergistic mechanisms between surgical techniques and systemic therapies.
This study has several limitations inherent to its retrospective, single-center design. First, the non-randomized allocation of surgical techniques may introduce selection bias, despite comparable baseline characteristics between groups. Additionally, the rate of adjuvant therapy administration after surgery is notably low at 49.3%. The 49.3% adjuvant therapy rate warrants careful interpretation. While lower than contemporary trials (e.g., PRODIGE-24: 79%), this may reflect: Delayed initiation due to higher-grade complications (8.4% abdominal infections); Selection bias where R0-resected patients were deemed lower-risk. Finally, the technical complexity of the mesenteric approach requires specialized expertise, potentially restricting generalizability to low-volume centers. Future prospective, multicenter randomized trials are warranted to corroborate these findings and standardize procedural protocols.
Conclusions
To sum up, the mesenteric approach in infracolic compartment can improve the prognosis, prolong the postoperative survival time and reduce recurrence.
Acknowledgements
We will thank the patients for their great help in this report. This paper is supported by Dr. LSC and Dr. HQ.
Author contributions
LSC proposed the study. WFF performed the research and wrote the first draft. All authors contributed to the design and interpretation of the study and to further drafts. LSC is the guarantor.
(I)Conception and design: Fangfei Wang (II) Administrative support: Qiang He; (III) Provision of study materials: Shaocheng Lyu; (IV) Collection and assembly of data: Fangfei Wang, (V) Data analysis and interpretation: Fangfei Wang, Shaocheng Lyu; (VI) Manuscript writing: All authors.
Funding
No.
Data availability
The datasets supporting the findings of the current study are available from the corresponding author on reasonable request. The data are not publicly available due to patient privacy regulations. Restrictions were confirmed by the Ethics Committee of Beijing Chaoyang Hospital, which can be contacted at Department of Respiratory Medicine, Beijing Chaoyang Hospital, No. 8 Gongti South Road, Chaoyang District.
Declarations
Ethics approval and consent to participate
Our research was approved by the Ethics Committee of Beijing Chaoyang Hospital with the approval number of 2024-D-511.
Ethical approval
Yes.
Competing interests
No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.
Acknowledgements:
Footnotes
The original online version of this article was revised: The first author (Fang-Fei Wang) and second author (Qiang He) were inadvertently omitted. The complete and correct author list is Fang-Fei Wang, Qiang He, Shao-Cheng Lyu.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Change history
9/11/2025
The original online version of this article was revised: The first author (Fang-Fei Wang) and second author (Qiang He) were inadvertently omitted. The complete and correct author list is Fang-Fei Wang, Qiang He, Shao-Cheng Lyu.
Change history
9/18/2025
A Correction to this paper has been published: 10.1007/s00423-025-03875-6
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets supporting the findings of the current study are available from the corresponding author on reasonable request. The data are not publicly available due to patient privacy regulations. Restrictions were confirmed by the Ethics Committee of Beijing Chaoyang Hospital, which can be contacted at Department of Respiratory Medicine, Beijing Chaoyang Hospital, No. 8 Gongti South Road, Chaoyang District.