Abstract
We herein present a novel combined posterior and left-sided superior mesenteric artery (SMA) first approach to facilitate the TRIANGLE operation for pancreatoduodenectomy (PD) or total pancreatectomy (TP) in pancreatic cancer. Patients who were diagnosed with resectable pancreatic ductal adenocarcinoma who underwent PD or TP using the combined posterior and left-sided SMA-first approach to the TRIANGLE operation between June 2021 and June 2024 were included in this study. General characteristics, technical details including operative techniques, short-term outcomes, and pathological results were analyzed retrospectively and compared with those from historic cohorts undergoing single SMA-first approach resections. Overall, 126 patients were analyzed (dual-approach PD-TP, n = 33; single-approach PD-TP, n = 93). The dual-approach resection yielded more lymph nodes than the single-approach (36.17 vs 26.53; p < 0.001). Additionally, the rate of tumor-positive resection margins, R1 (direct), was decreased. The duration of the operation was significantly longer, and blood loss was higher with the dual approach. There was no significant difference in postoperative mortality and complications between the two approaches. Utilizing the combined posterior and left-sided first approach to SMA in PD or TP with the TRIANGLE operation proved safe and effective for achieving R0 resection with favorable short-term outcomes in borderline resectable and locally advanced pancreatic cancer.
Keywords: TRIANGLE operation, Combined posterior and left-sided first approach, Pancreatoduodenectomy, Pancreatic cancer
INTRODUCTION
Local recurrence following surgical resection of pancreatic ductal adenocarcinoma (PDAC) is frequently observed and is linked to significantly worse prognosis compared to patients who remain recurrence-free. Among the top ten research priorities in pancreatic cancer is the determination of whether the extent of surgical resection—including en bloc removal of tissues adjacent to major vascular structures—affects both overall survival and health-related quality of life [1]. Introduced by Hackert et al. [2] in 2017, the TRIANGLE procedure represents a refinement of prior extended lymphadenectomy techniques by aiming to remove all soft tissue between the celiac axis (CA), superior mesenteric artery (SMA), and superior mesenteric vein (SMV)/portal vein (PV). This technique enables the complete removal of the lymphatic and neural structures draining from the pancreatic head. Given PDAC’s propensity for perineural invasion, R1 resections and local recurrences are often observed within this anatomical ‘TRIANGLE,’ highlighting the rationale for more radical dissection strategies along the SMA and CA [3]. Unlike conventional extended lymphadenectomy methods, the TRIANGLE operation specifically targets sites of microscopic tumor spread and frequent local tumor recurrence. It entails the excision of all soft tissue, lymphatics, and nerve plexus within the designated area. Although the TRIANGLE procedure yields an increased number of dissected lymph nodes (LNs), this should be regarded as a secondary outcome or surrogate parameter rather than the primary goal. This distinction is vital because extended lymphadenectomies alone have not demonstrated a survival benefit in meta-analyses of randomized trials and may increase morbidity [4,5]. Proficiency in the ‘artery-first approach’ methods is necessary for safely performing this technique. Yet, significant challenges arise due to extensive tumor infiltration and encasement around the mesenteric vessels. By integrating different approaches, we can exploit the advantages and minimize the disadvantages of each, ensuring optimal safety and oncological efficacy.
In our research, we aim to evaluate the feasibility, safety, and short-term efficacy of our novel technique for pancreatoduodenectomy (PD) or total pancreatectomy (TP). This technique includes a unique dual-first approach to SMA and TRIANGLE clearance for borderline resectable and locally advanced, or mesopancreas-invasive resectable pancreatic cancer.
MATERIALS AND METHODS
Data collection
Data collection and analysis were conducted in accordance with approval from the institutional ethics committee and adhered to the STROBE guidelines for observational research [6]. Written informed consent was obtained from all participants in the study. Following the approval of the Institutional Review Board, patients diagnosed with resectable PDAC exhibiting signs of meso-pancreas invasion, or those with borderline resectable locally advanced PDAC post-neoadjuvant chemotherapy, were assessed for the feasibility of resection; subsequently, they underwent PD or TP with TRIANGLE clearance using a combined posterior and left-sided SMA-first approach at Bach Mai Hospital, between June 2021 and June 2024 were included. A historical cohort was selected, comprising patients who underwent surgery between June 2021 and June 2024, utilizing a single first-approach for PD and TP without extended lymphadenectomy in the TRIANGLE region. Patients’ data were prospectively collected, including:
- General and preoperative information: This section encompassed demographic data, including sex, age, height, weight, body mass index (BMI), and medical history. The presence or absence of neoadjuvant chemotherapy, measurements of total bilirubin and directed bilirubin levels (μmol/L), and CA19-9 levels (U/mL) were also recorded.
- Intraoperative data and short-term outcomes: Relevant intraoperative variables included blood loss, operative duration, intraoperative complications, type of pancreatic resection (PD/TP), extent of surgical resection involving adjacent organs, tumor size, and pancreatic reconstruction technique. Postoperative assessments involved length of hospital stay, occurrence of postoperative complications, and in-hospital mortality. Complications arising within 30 days postoperatively were graded according to the Clavien-Dindo classification [7], with only complications of grade II or higher being included. The frequencies of early (< 30 days) and overall graft thrombosis, postoperative lymphorrhea as defined by Besselink’s classification [8,9], postpancreatectomy hemorrhage [10], and postoperative pancreatic fistula (POPF) [11], were recorded based on International Study Group on Pancreatic Surgery (ISGPS) guidelines. Only clinically significant (grade B and C) complications were analyzed. While routine reporting of diarrhea was not part of the prospective database, it was evaluated during the patient’s postoperative hospital stay. Diarrhea was defined as more than three defecations per day accompanied by continuous use of antidiarrheal agents in the second postoperative week [12].
- Histopathological data: The tumor site, resected margins, and LNs were labeled and measured by the operating surgeon at the back table in the operating room. The collected data encompassed tumor grade, total number of retrieved LNs, count of metastatic LNs, involvement of left-sided LNs along the SMA, and pathological staging according to the 8th edition of the AJCC/UICC TNM classification [13]. Margin status assessments were as follows: R0—no tumor cells detected microscopically within 1 mm of any resection margin; R1—microscopic presence of tumor at or within 1 mm of a margin based on the Royal College of Pathologists criteria; and R2—macroscopic residual tumor identified during surgery [14].
Surgical procedure: The TRIANGLE operation employs a combined posterior and left-sided first approach to the SMA
An upper abdominal incision is made to explore the peritoneum and rule out metastases. We employ a distinctive dual-first technique for the SMA, combining posterior and left-sided approaches (Supplementary Video 1):
- For the posterior approach, the Kocher and Cattell-Braasch maneuvers are executed. LNs in groups 16a2 and 16b1 are dissected, revealing the aortic vein, left renal vein, and aorta. The left renal vein is manipulated, and the right sympathetic ganglion is isolated directly above it. The right crus of the diaphragm is incised to display and mobilize the SMA root from a posterior perspective (Fig. 1). The SMA is separated from the aorta by approximately 3 to 4 cm, typically within an avascular plane. Efforts are made to prevent damage to the right hepatic artery if it arises from the SMA.
Fig. 1.
The posterior SMA approach: The SMA is separated from the aorta approximately 3–4 cm away, typically within an avascular plane. SMA, superior mesenteric artery; IVC, inferior vena cava; LRV, left renal vein.
- In the left-sided approach, the mesenteric peritoneum is incised, and the SMA and SMV are manipulated beneath the mesentery, while preserving the ileocolic artery, which branches off from the SMA anteriorly towards the SMV. The SMA is traced anteriorly and toward the left, with ligation of the middle colic artery performed close to its origin. Dissection proceeds by clearing the connective tissue along the artery’s left aspect until the previously exposed SMA base is encountered. The first jejunal loop artery is ligated, and division of the first jejunal loop with its associated mesentery is achieved using a stapling device. Subsequent dissection of the SMA entails removal of surrounding connective tissue on the left posterior side (Fig. 2). The inferior pancreaticoduodenal artery is entirely ligated posterior to the SMA. The operation proceeds with dissection of the right border of the maximal artery up to its point of origin. The transverse colon mesentery is then detached from the pancreatic head.
Fig. 2.
Left-sided SMA approach: The connective tissue surrounding the artery on its left side is carefully dissected. RCA, right colic artery; SMA, superior mesenteric artery; SMV, superior mesenteric vein.
- The hepatic pedicle is meticulously explored, with resection of neural tissue encasing the common hepatic artery, proper hepatic artery, and the right half of the celiac artery (to level 3 according to Inoue’s classification) [15]. The PV is fully exposed and mobilized with gentle manipulation to achieve control. The jejunal loop is repositioned to the right; at this stage, the duodeno-pancreatic mass is attached to the SMA by a small tissue section, which is subsequently transected (to level 3 as per Inoue’s classification) [16]. During this procedure, the nerve plexus surrounding the SMA (plSMA) is dissected from the 5 to 11 o’clock positions, encompassing a semicircular arc of 180 degrees. In selected cases, a more extensive clearance—ranging from this semicircular approach up to a full 360-degree resection of lymphatic tissue and nerve plexus around the SMA, referred to as ‘periarterial divestment’—may be undertaken, depending on the surgeon’s judgment. This maneuver also facilitates a circumferential (360-degree) dissection around the SMV. Additionally, the complete dissection of all soft tissue within the TRIANGLE formed by the CA, SMA, and PV is achieved (Fig. 3).
Fig. 3.
The TRIANGLE operation: The entire soft tissue delineated by the celiac artery, SMA, and portal vein is completely dissected. CHA, common hepatic artery; IVC, inferior vena cava; MCA, middle colic artery; SMV, superior mesenteric vein; SMA, superior mesenteric artery.
In our protocol, the mesopancreas is systematically resected en bloc with the entire pancreaticoduodenal mass. The size of the meso-pancreas is carefully documented for this case and all other PD cases we perform. An extended lymphadenectomy is performed in all cases, targeting LN stations 5, 6, 8a, 8p, 12b1, 12b2, 12c, 12p, 13a, 13b, 14a, 14b, 17a, and 17b following the New Japanese Classification and the ISGPS consensus [17,18], along with LN stations 7, 9, 11, and 14c, 14d [19].
Control intervention (single SMA-first approach PD or TP)
Patients in the control groups underwent a single (posterior or left-sided) SMA-first approach PD or TP, including total mesopancreas dissection to level 2, as defined by Inoue’s classification [16,20]. These procedures adhered to established standards outlined in the New Japanese Classification and ISGPS consensus statements [17,18], without implementation of the TRIANGLE dissection, and were reserved for resectable PDAC cases without evidence of mesopancreas invasion (Fig. 4).
Fig. 4.
Single posterior SMA-first approach with comprehensive mesopancreas dissection. IPDA, inferior pancreaticoduodenal artery; SMA, superior mesenteric artery; SMV, superior mesenteric vein; MP, meso-pancreas.
Treatments in both groups
The reconstructive procedure was standardized for both groups: Reconstruction commenced with a pancreatojejunostomy, utilizing a double-layer, end-to-side anastomosis as per a modified Blumgart technique. A hepaticojejunostomy was constructed approximately 20 cm distal to the pancreatojejunostomy using a single-layer method, followed by an antecolic gastrojejunostomy positioned about 60 cm distal to the hepaticojejunostomy. Where indicated to ensure negative margins, venous resections (including PV or SMV) and multi-visceral resections were performed. Likewise, arterial resections or periarterial divestment were conducted in both treatment groups as required for oncologic clearance [21]. Throughout the study period, the standard oncologic approach involved upfront surgical resection for tumors classified as resectable. For patients with borderline resectable or locally advanced PDAC, six cycles of the neoadjuvant FOLFIRINOX regimen were administered prior to surgery. Following upfront resection, adjuvant chemotherapy (AC) was advised for all PDAC patients, regardless of their pathological stage. Standard regimens for both neoadjuvant and adjuvant treatment included 5-fluorouracil with folinic acid, gemcitabine, or FOLFIRINOX.
Management of postoperative diarrhea
For patients experiencing more than five episodes of watery diarrhea daily, in the absence of bacterial enteritis, initial treatment involved administration of non-opioid antidiarrheal agents, such as natural aluminum silicate (6–12 g/day). In cases where symptoms persisted, an opioid antidiarrheal agent (opium tincture) was started at a dose of 0.9 mg before each meal daily. Dosages were titrated according to patient response, targeting a reduction to three or fewer stools per day, maintaining solid or soft stool consistency. Post-discharge, antidiarrheal therapy continued in the outpatient setting, with careful evaluation for possible dose reduction or cessation as symptom resolution occurred.
Statistical analysis
Categorical variables were presented as percentages within each group. Discrete data were displayed as absolute numbers within a specified numerical range. Continuous variables were summarized as either the mean or median, depending on distribution, along with the corresponding range. The Wilcoxon rank-sum test was utilized for analysis of continuous variables. For comparisons of categorical data, the chi-square test or Fisher’s exact test was applied as appropriate. All analyses were completed using IBM SPSS for Windows, version 26.0 (IBM Corp.). All tests were two-sided, with a p-value of < 0.05 denoting statistical significance. Considering the study’s exploratory character, results were interpreted with caution; p-values were considered descriptive.
RESULTS
During the period from June 2021 to June 2024, a total of 126 patients were enrolled. Of these, 33 patients underwent PD or TP utilizing the combined posterior and left-sided SMA-first approach to the TRIANGLE operation at our institution and were compared with a historical cohort (n = 93) who received a single SMA-first approach PD or TP without TRIANGLE dissection.
Patients’ demographics, preoperative laboratory results, and intraoperative data
The baseline characteristics were similar across the groups. The study population consisted of 67 males and 59 females, with a mean age of 59.38 ± 11.54 years (range 12–83 years). The mean BMI was 20.8 ± 2.35 kg/m² (range 14.22–26.06 kg/m²), and the distribution of ASA status was as follows: ASA I (n = 78), ASA II (n = 36), and ASA III (n = 12).
Total mesopancreas excision was performed in all cases. In every patient, a pancreaticojejunostomy was achieved using the modified Blumgart anastomosis. The duration of operation was significantly longer in dual-approach groups compared to single-approach groups (dual-approach: 301.39 ± 59.65 min versus single-approach: 289.86 ± 92.37 min, p = 0.02). Additionally, intraoperative blood loss was significantly higher in the dual-approach groups than in the single-approach groups (dual-approach: 219.23 mL [60–1,500 mL] vs single-approach: 124.85 mL [30–800 mL]; p = 0.049). SMV/PV resection was executed in 17 cases (51.5%), and CA/SMA resection or periarterial/sub-adventitial dissection was performed in eight cases (24.2%) in the dual-approach groups, which were significantly higher compared to single-approach groups (p < 0.001) (Table 1).
Table 1.
General preoperative information and intraoperative data categorized by the type of approach
| Index | Dual-approach (n = 33) | Single-approach (n = 93) | p-value |
|---|---|---|---|
| Sex ratio (male/female) | 25:8 (76:24) | 42:51 (45:55) | 0.002* |
| Age (yr) | 61.7 ± 11.32 | 58.56 ± 11.57 | 0.483 |
| BMI (kg/m2) | 20.57 ± 2.38 | 20.95 ± 2.35 | 0.96 |
| ASA classification | 0.382 | ||
| ASA 1 | 18 (54.5) | 60 (64.5) | |
| ASA 2 | 10 (30.3) | 26 (28.0) | |
| ASA 3 | 5 (15.2) | 7 (7.5) | |
| Median CA19-9 (U/mL) | 280.36 | 256.15 | 0.586 |
| Total bilirubin (μmol/L) | 112.15 ± 100.71 | 88.26 ± 81.39 | 0.282 |
| Directed bilirubin (μmol/L) | 79.50 ± 74.65 | 63.82 ± 61.95 | 0.602 |
| Medical history | 0.13 | ||
| Diabetes | 7 (21.2) | 11 (22.0) | |
| Hypertension | 2 (6.1) | 15 (30.0) | |
| Chronic pancreatitis | 6 (18.2) | 9 (18.0) | |
| Operative time (min) | 301.39 ± 59.65 | 289.86 ± 92.37 | 0.02* |
| Vascular resection/divestment | |||
| PV/SMV | 17 (51.5) | 3 (3.2) | < 0.001* |
| CHA/SMA resection/divestment | 8 (24.2) | 2 (2.2) | < 0.001* |
| Estimated blood loss (mL) | 219.23 ± 299.29 (60–1,500) | 124.85 ± 134.88 (30–800) | 0.049* |
Values are presented as mean ± standard deviation, number (%), or mean ± standard deviation (min–max).
BMI, body mass index; PV, portal vein; SMV, superior mesenteric vein; CHA, common hepatic artery; SMA, superior mesenteric artery.
Statistically significant (*p < 0.05).
Short-term outcomes
The median postoperative hospital stay was comparable between the two groups. In-hospital mortality for the entire cohort was 1.6%. Four patients experienced postoperative complications of grade III or higher. Among these, the duration of complications of grade III or higher was significantly longer in the dual-approach group compared to the single-approach group (p = 0.039). POPF occurred in 25.4% of all patients, predominantly classified as grade A or grade B, with no significant difference between the groups. Chyle leakage was identified in 32 patients (25.4%), necessitating percutaneous hepatic lymphangiography in 10 cases; the frequency was significantly greater in the dual-approach group than in the single-approach group (p = 0.036). Postoperative diarrhea developed in 24 patients (19.0%), with no significant intergroup difference (Table 2).
Table 2.
Postoperative morbidity and mortality rates categorized by the type of approach
| Index | Dual-approach (n = 33) | Single-approach (n = 93) | p-value |
|---|---|---|---|
| Complication | 0.039* | ||
| I, II | 23 (69.7) | 83 (89.2) | |
| IIIa | 6 (18.2) | 7 (7.5) | |
| IIIb | 1 (3.0) | 2 (2.2) | |
| IVa | 2 (6.1) | 0 | |
| IVb, V | 1 (3.0) | 1 (1.1) | |
| Type of postoperative complications | |||
| Pancreatic fistula | 7 (21.2) | 25 (26.9) | 0.52 |
| Diarrhea | 9 (27.3) | 15 (16.1) | 0.161 |
| Chyle leakage | 13 (39.4) | 19 (20.4) | 0.032* |
| Pancreatic fistula | 0.492 | ||
| Grade A/B | 5 (15.2) | 22 (23.7) | |
| Grade C | 2 (6.1) | 3 (3.2) | |
| Lymphatic leakage | 0.036* | ||
| Grade A | 5 (15.2) | 9 (9.7) | |
| Grade B | 6 (18.2) | 10 (10.8) | |
| Grade C | 2 (6.1) | 0 | |
| Diarrhea | 0.341 | ||
| Non-opioid antidiarrheal | 3 (9.1) | 8 (8.6) | |
| Opioid antidiarrheal | 6 (18.2) | 7 (7.5) | |
| Length of hospital stay | 19.67 ± 7.8 (10–50) | 18.95 ± 8.99 (9–75) | 0.695 |
| Reoperations | 2 (6.1) | 2 (2.2) | 0.271 |
| In-hospital mortality | 1 (3.0) | 1 (1.1) | 0.44 |
Values are presented as number (%) or mean ± standard deviation (min–max).
Statistically significant (*p < 0.05).
Pathological results
Histopathological examination of the full cohort identified 91 patients (72.22%) with moderately or highly differentiated tumors and 21 patients (16.67%) with poorly differentiated tumors, with no significant difference observed between the groups. The T status was significantly more advanced in the dual-approach group compared to the single-approach group, whereas N status did not differ between groups. R0 resection margins at the pancreatic parenchyma were achieved in all cases. Metastatic involvement of the mesopancreas or TRIANGLE region was detected microscopically in 32 cases (25.4%) across the cohort, with a higher incidence in the dual-approach group compared to the single-approach group (p = 0.001). The mean number of LNs harvested in the total cohort was 28.94 ± 11.45 (with a maximum of 74), and the average number of metastatic LNs was 2.21 (maximum 34), both of which were significantly higher in the dual-approach group than in the single-approach group (p ≤ 0.001). The rate of metastatic left-sided LN no. 14 in the cohort was 15.9%, with no difference found between groups (Table 3).
Table 3.
Histopathological findings categorized by the type of approach
| Index | Dual-approach (n = 33) | Single-approach (n = 93) | p-value |
|---|---|---|---|
| T status | 0.005* | ||
| T1 | 2 (6.1) | 2 (2.2) | |
| T2 | 4 (12.1) | 35 (37.6) | |
| T3 | 23 (69.7) | 42 (45.2) | |
| T4 | 3 (9.1) | 1 (1.1) | |
| N status | 0.574 | ||
| N0 | 13 (39.4) | 41 (44.1) | |
| N1 (1–3 PLNs) | 12 (36.4) | 26 (28.0) | |
| N2 (≥ 4 PLNs) | 7 (21.2) | 13 (14.0) | |
| Grading | 0.072 | ||
| Well-differentiated | 1 (3.0) | 16 (17.2) | |
| Moderate-differentiated | 25 (75.8) | 49 (52.7) | |
| Poor-differentiated | 6 (18.2) | 15 (16.1) | |
| LNs harvested | 36.17 ± 16.31 | 26.53 ± 8.06 | < 0.001* |
| Metastatic LN | 3.97 ± 7.24 | 1.62 ± 3.25 | 0.001* |
| Metastatic LN no. 14 | 8 (24.2) | 12 (12.9) | 0.162 |
| Metastatic mesopancreas | 16 (48.5) | 16 (17.2) | 0.001* |
| Meso-pancreatic margin | |||
| R0 | 26 (78.8) | 84 (90.3) | 0.005* |
| R1 | 7 (21.2) | 4 (4.3) |
Values are presented as number (%) or mean ± standard deviation (min–max).
Pathological TNM staging according to the eighth edition of the AJCC/UICC system of pancreatic ductal adenocarcinoma.
TNM, tumor-node-metastatic; PLN, positive lymph nodes; LN, lymph node; no. 14, along the superior mesenteric artery; R0, microscopically (within 1 mm of resection margin) curative resection; R1, microscopically positive resection margin or less than 1 mm tumor-free margin.
Statistically significant (*p < 0.05).
DISCUSSION
PDAC is an aggressive malignancy with a poor prognosis, often characterized by its propensity to invade peripancreatic nerve plexuses—including the first and second plexuses of the pancreatic head (collectively referred to as the mesopancreas) and the nerve plSMA. Hence, achieving an R0 resection margin might necessitate extended dissection of the plSMA, especially in cases of borderline resectable or locally advanced tumors. Nevertheless, such extensive nerve plexus resections are linked with a considerable risk of severe postoperative diarrhea, which can impede the delivery of adjuvant therapy. Thus, a delicate balance must be struck between attaining oncological clearance and preserving nerve structures to avoid debilitating complications. In this study, all patients underwent the TRIANGLE procedure, which aligns with at least level-3 (L3) or extended level-3 (E-L3) total meso-pancreas dissection, as defined by Inoue et al. [22]. E-L3 total mesopancreas dissection entails expanding the plSMA resection beyond 180 degrees. Additionally, in our study, there were 10 cases in the entire cohort where the periarterial divestment technique was utilized, indicating a complete circumferential plSMA resection. In these 10 patients with SMA divestment, seven cases have shown no signs of tumor cells in directed SMA margin (R1 resection < 1 mm), and three cases incurred R1-directed SMA margin. For postoperative complications, there was a case of a SMA pseudoaneurysm, which was successfully managed with interventional stent placement in the SMA. The decision to perform divestment or resection of the SMA must be determined intraoperatively by the pancreatic surgeon, as preoperative computed tomography and magnetic resonance imaging cannot reliably distinguish between vascular encasement and true arterial wall infiltration [21]. Importantly, arterial divestment is associated with a potentially higher rate of R1 resections compared to arterial resection. However, this decision should be guided by multiple considerations: existing evidence indicates that arterial divestment may lower perioperative morbidity and mortality relative to arterial resection, and R1 resections at the SMA margin can still yield a clinically acceptable prognosis [21].
Pessaux et al. [23] introduced the first study on integrating multiple SMA-first approaches in 2009, utilizing a combination of the posterior and anterior approaches, which was named the “hanging maneuver.” Subsequently, Pittau et al. [24] reported another combination in 2023, involving both anterior and superior approaches to the SMA. The most renowned methodology, termed the Heidelberg technique, combined the posterior and anterior SMA-first approaches and was published by Schneider et al. [25] in 2019. In contrast to the Heidelberg technique, our study employed an alternative dual SMA-first approach: the associated posterior and left-sided SMA-first approaches. This approach is designed to enhance the efficacy of L3/E-L3 total mesopancreas dissection and periarterial divestment, providing multiple advantages by integrating and reducing the drawbacks of each method.
- Initiating the SMA approach from the left side exposes the SMV posteriorly, enabling its dissection up to the confluence with the splenic vein. This approach increases the safety of SMV division and ensures a comprehensive removal of the mesopancreas.
- The posterior SMA approach facilitates early identification of the arterial root, allowing for quick evaluation of arterial invasion and extensive dissection of retroperitoneal LNs. The left-sided approach, meanwhile, provides direct access to the rest of the artery, ensuring complete 360-degree control over the SMA from its origin, which enhances the dissection of LNs surrounding the SMA and permits extension of the SMA perivascular nerve sheath (e.g., E-L3 and periarterial divestment) when necessary.
- It is crucial to preserve the right hepatic artery, especially in cases where it originates from the SMA, to account for anatomical variations.
Consequently, this dual SMA-first approach technique encompasses not only a systematic mesopancreatic dissection along the SMA but also includes dissection of the CT. This standardized approach facilitates the clearance of tumor-infiltrated lymphatic and neural tissues located in the triangle formed by the CT, SMA, and SMV/PV, potentially reducing the risk of local recurrence of PDAC. In our study, SMV/PV resection was conducted in 17 cases (51.5%), and CA/SMA resection or periarterial/sub-adventitia divestment was performed in eight cases (24.2%) in the dual-approach group, which were significantly higher compared to those in the single-approach group (p < 0.001).
For short-term outcomes, POPF occurred in 25.4% of all cases, predominantly of grade A or grade B, with no significant difference between the two groups. In our research, the dual approach was selected for patients with more locally advanced pancreatic cancer, which may account for the longer operative times and increased blood loss. Chyle leakage was observed in 32 cases (25.4%), necessitating percutaneous hepatic lymphangiography in 10 cases. This incidence was significantly higher in the dual-approach group compared to the single-approach group (p = 0.036). A total of 24 cases (19.0%) developed postoperative diarrhea, with no significant difference between the groups. Another pivotal aspect of our approach was the proactive management of postoperative diarrhea. Previous studies have often regarded plSMA dissection as a surgical risk or a barrier to AC [26,27]. However, these discussions frequently lacked systematic criteria for dissection extent and an effective method to control diarrhea. In recent studies, the majority of PDAC patients, including those undergoing E-LV3 dissection, reported well-managed diarrhea, facilitating the successful initiation of postoperative chemotherapy in nearly 90% of patients [22,28]. This percentage is notably higher compared to earlier clinical reports. The primary reasons for shortened AC were early recurrence due to undetected micro-metastases or aggressive tumor biology. Our strategy of tailoring the dose of antidiarrheal medication based on the frequency of watery diarrhea proved to be simple and effective, leading to stable postoperative recovery and minimal discontinuation of AC (the rate of patients extending beyond 12 weeks or discontinuing AC was approximately 20%, comparable to other studies [22]), regardless of the dissection extent.
We acknowledge the limitations of this study and the necessity to address these in future research. As a single-institution cohort study, its scope is insufficient to definitively validate the efficacy of our method. Given that the short-term outcomes of our approach appear promising, we aim to expand our study population to more robustly evaluate its feasibility in future studies. Additionally, in our research, the dual approach was reserved for patients with more locally advanced pancreatic cancer. This significant disparity in the baseline characteristics between groups might introduce potential selection bias.
In conclusion, the TRIANGLE operation is an innovative technique that provides an additional surgical option for patients with borderline resectable or locally advanced pancreatic cancer. By combining two arterial-first approaches, from the posterior and left posterior sides, it enhances exposure and facilitates the dissection of the TRIANGLE region. Our research, supported by surgical video, underscores the technique’s advantages, feasibility, and safety in the treatment of pancreatic cancer.
SUPPLEMENTARY DATA
Supplementary data related to this article can be found at https://doi.org/10.14701/ahbps.25-064.
ACKNOWLEDGEMENTS
The authors would like to thank to all the colleagues of the Center of Digestive Surgery, Bach Mai Hospital, Hanoi, Vietnam for their assistance during the time of our patients’ in-hospital observation.
Funding Statement
FUNDING None.
Footnotes
CONFLICT OF INTEREST
No potential conflict of interest relevant to this article was reported.
AUTHOR CONTRIBUTIONS
TKN contributed as first author, the main doctors to conceive the original idea, design and operate the patients; HHN, the main doctors to conceive the original idea, design and operate the patients; THL performed the operations, analyzed the data and wrote the manuscript; VDL, VAD, DTD performed the operations and collected the data; PC, HQP conceived the original idea, summed up, revised manuscript. All authors have discussed the results together and contributed to the final manuscript.
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