"Five steps four quadrants" modularized en bloc dissection technique for accessing hepatic hilum lymph nodes in laparoscopic pancreaticoduodenectomy

Xiao-Si Hu, Yong Wang, Hong-Tao Pan, Chao Zhu, Shi-Lei Chen, Hui-Chun Liu, Qing Pang, Hao Jin

Abstract BACKGROUND Although en bloc dissection of hepatic hilum lymph nodes has many advantages in radical tumor treatment, the feasibility and safety of this approach for laparoscopic pancreaticoduodenectomy (LPD) require further clinical evaluation and investigation.AIM To explore the application value of the "five steps four quadrants" modularized en bloc dissection technique for accessing hepatic hilum lymph nodes in LPD patients.METHODS A total of 52 patients who underwent LPD via the "five steps four quadrants" modularized en bloc dissection technique for hepatic hilum lymph nodes from April 2021 to July 2023 in our department were analyzed retrospectively. The patients' body mass index (BMI), preoperative laboratory indices, intraoperative variables and postoperative complications were recorded. The relationships between preoperative data and intraoperative lymph node dissection time and blood loss were also analyzed.RESULTS Among the 52 patients, 36 were males and 16 were females, and the average age was 62.2 ± 11.0 years. There were 26 patients with pancreatic head cancer, 16 patients with periampullary cancer, and 10 patients with distal bile duct cancer. The BMI was 22.3 ± 3.3 kg/m2, and the median total bilirubin (TBIL) concentration was 57.7 (16.0-155.7) μmol/L. All patients successfully underwent the "five steps four quadrants" modularized en bloc dissection technique without lymph node clearance-related complications such as postoperative bleeding or lymphatic leakage. Correlation analysis revealed significant associations between preoperative BMI (r = 0.3581, P = 0.0091), TBIL level (r = 0.2988, P = 0.0341), prothrombin time (r = 0.3018, P = 0.0297) and lymph node dissection time. Moreover, dissection time was significantly correlated with intraoperative blood loss (r = 0.7744, P < 0.0001). Further stratified analysis demonstrated that patients with a preoperative BMI ≥ 21.9 kg/m2 and a TIBL concentration ≥ 57.7 μmol/L had significantly longer lymph node dissection times (both P < 0.05).CONCLUSION The "five steps four quadrants" modularized en bloc dissection technique for accessing the hepatic hilum lymph node is safe and feasible for LPD. This technique is expected to improve the efficiency of hepatic hilum lymph node dissection and shorten the learning curve; thus, it is worthy of further clinical promotion and application.

Key Words: Five steps four quadrants; Hepatic hilum lymph node; Modularized en bloc clearance; Laparoscopic pancreaticoduodenectomy

INTRODUCTION

In recent years, with the advancements in surgical techniques and the renewal of treatment concepts,en blocresection has been widely regarded as a radical treatment for several malignant tumors, such as cholangiocarcinoma, periampullary carcinoma and pancreatic head cancer[1-3].En blocresection usually includes resection of the tumor and dissection of the regional lymph node and surrounding tissues.En blocdissection of the hepatic hilum lymph node refers to the dissection of the lymph node and neuroconnective tissues along the vascular axis [usually the common hepatic artery (CHA) and portal vein (PV)] during radical surgery and theen blocremoval of the lymph node and surrounding connective tissues around the vessel[4]. Compared with traditional selective dissection, this technique can thoroughly remove potential lymph nodes and micrometastases and increase the R0 resection rate[5,6]. Althoughen blocdissection of hepatic hilum lymph nodes has many advantages in radical tumor treatment, the feasibility and safety of this approach for laparoscopic pancreaticoduodenectomy (LPD) require further clinical evaluation and investigation. In recent years, based on long-term clinical practice, our center has summarized the "five steps four quadrants" approach for modular hepatic hilum lymph node dissection, which has been successfully applied during LPD surgery and initially shown satisfactory clinical efficacy. In this study, we summarize the relevant data as follows.

MATERIALS AND METHODS

Patients

The clinical and surgical data of patients who underwent LPD in our department between April 2021 and July 2023 were retrospectively analyzed. The inclusion criteria were as follows: (1) ≥ 18 years of age; (2) diagnosed with periampullary carcinoma, distal bile duct carcinoma, or pancreatic head carcinoma preoperatively, and LPD was performed with the technique of "five steps four quadrants" modular hepatic hilum lymph node dissection; (3) Eastern Cooperative Oncology Group score 0-2; (4) without other malignancies; and (5) without a history of supreme abdominal surgery.

This study was performed in accordance with the Declaration of Helsinki and was approved by the Ethics Committee of the Second People's Hospital of Anhui Province (approval number: 2022-011). Written informed consent was obtained from the patients preoperatively.

Technique procedure

Kocher incision separation was performed routinely, and the jejunum was severed after the resectability of the tumor was determined (it should be noted that the inferior vena cava should be fully separated from the rear of the hepatic portal during Kocher incision separation to facilitate dissection of the hepatic hilum region after the operation). Furthermore, the stomach was severed, the hepatic hilum region was exposed, and the "five steps four quadrants" modularizeden blocdissection technique (Figure 1) was implemented as follows:

Figure 1 Visualization of the surgical fields after the completion of each surgical step via the five-step four-zone method. A: The common hepatic artery was exposed and suspended along the No. 8a lymph node; B: The surgical field after the dissection of the upper zone of the hepatic artery (HA)/portal vein (PV) axis; C: The surgical field after the dissection of the left zone of the HA/PV axis; D: The surgical field after the dissection of the right zone of the HA/PV axis;E: The surgical field after the dissection of the lower zone of the HA/PV axis; F: The surgical field of the hepatic hilum region after the completion of the dissection. LN 8a: No. 8a lymph node; CHA: Common hepatic artery; GDA: Gastroduodenal artery; RHA: Right hepatic artey; PHA: Proper hepatic artery; LN: Lymph node; LGA:Left gastric artery; CHD: Common hepatic duct; IVC: Inferior vena cave.

Step 1:The No. 8a lymph node was separated from the upper margin of the pancreas, after which the CHA was exposed and suspended, after which the inferior PV was exposed. Subsequently, the hepatic hilum region was bounded by the hepatic artery (HA)/PV axis and divided into four zones: upper, lower, left and right zones (Figure 1A).

Step 2:As shown in Figure 1B, Dissection of the upper zone of the HA/PV axis. The upper zone was separated toward the hepatic hilum along the 12-point position of the HA and PV surfaces, and the No. 12a and 8p lymph nodes and surrounding tissues were pushed to the left and right zones but were not severed by using the combination of blunt and sharp dissection. Then, the full course of the HA/PV axis was exposed, and the left and right hepatic arteries were also exposed [the right gastric artery (RGA) or gastroduodenal artery (GDA) could be automatically lapped and severed provided that the operation was significantly affected].

Step 3:As shown in Figure 1C, Dissection of the left zone of the HA/PV axis. First, the lower left zone was separated toward the abdominal trunk along the HA/PV axis. The No. 9 lymph node and surrounding tissues were dissected, above which the No. 7 lymph node and surrounding tissues were further dissected through the left gastric artery. Then, the upper left and left zones of the HA/PV axis were dissected successively in a counterclockwise direction until the left edge of the PV was completely exposed. The dissected tissues in the left zone were pushed behind the PV. The surgeon should focus on the anatomical variation, injury and bleeding of the left gastric vein (LGV). The LGV should be disconnected if it empties into the PV.

Step 4:As shown in Figure 1D, Dissection of the right zone of the HA/PV axis. The GDA was severed after it was determined that there was no variation in the right hepatic artery (RHA). The No. 12b lymph node and surrounding tissues in the right zone of the HA/PV axis were pushed to the middle and distal bile duct using the combination of blunt and sharp dissection until the right margin of the PV was completely exposed. Then, the RGA was severed, and the gallbladder was removed. The hepatic duct was separated for subsequent dissection from the upper margin of the confluence with the gallbladder duct.

Step 5:As shown in Figure 1E, Dissection of the lower zone of the HA/PV axis. The pancreatic neck and uncinate process were successively severed, and the PV was subsequently separated from the No. 12p lymph node and surrounding tissues behind the PV. Subsequently, from the right rear side, the above dissected tissues in the left zone and the dissected tissues in the rear zone of the HA/PV axis were pulled out below the PV. The posterosuperior tissues in the right zone were separated from the hepatic hilum and finally attached to the common hepatic duct. The surrounding tissues of the inferior common hepatic duct were severed, the common hepatic duct was severed, anden blocdissection of the hepatic hilum region was completed (Figure 1F).

Observation indicators

Sex, age, body mass index (BMI), preoperative total bilirubin (TBIL), albumin (ALB), prothrombin time (PT), platelet count (PLT), carbohydrate antigen 19-9 (CA19-9), carcinoembryonic antigen (CEA), carbohydrate antigen 125 (CA125) and other laboratory indices were collected. Intraoperative lymph node dissection time, blood loss, postoperative blood loss, lymphatic leakage and other related complications were also analyzed. The correlations between preoperative data and intraoperative dissection time and blood loss were also analyzed.

Statistical analysis

SPSS 25.0 statistical software was used to process and analyze the data. Continuous variables are expressed as the mean ± SD or median (interquartile range) and were compared by using thettest or Wilcoxon test. Categorical data are expressed as frequencies and were compared by using theχ2test or Fisher's exact probability method. Pearson correlation analysis was performed to assess the correlation between two variables.P< 0.05 was considered to indicate statistical significance.

RESULTS

Characteristics of the study population

A total of 52 patients were included, all of whom underwent LPDviathe technique of "five steps four quadrants" modular hepatic hilum lymph node dissection. All the operations were performed by the same team. Among them, 36 were males and 16 were females. The mean age of the patients was 62.2 ± 11.0 years, the mean BMI was 22.3 ± 3.3 kg/m2, and the median TIBL concentration was 57.7 (16.0-155.7) μmol/L. Twenty-six lesions were located in the pancreatic head, 16 were in the periampulla, and 10 were in the distal bile duct. The median lymph node dissection time, dissection number, and intraoperative blood loss were 50 (41-54) min, 6 (6-7), and 25.0 (20.0-33.8) mL, respectively. The baseline information of the patients is shown in Table 1.

Table 1 Patient baseline information

Analysis of factors associated with lymph node dissection time

The correlation analysis showed that preoperative BMI (r= 0.3581,P= 0.0091), TIBL level (r= 0.2988,P= 0.0341) and PT (r= 0.3018,P= 0.0297) were significantly associated with intraoperative lymph node dissection time (Figure 2). In addition, the lymph node dissection time was significantly correlated with intraoperative blood loss (Figure 2D;r= 0.7744,P< 0.0001).

Figure 2 Correlations between body mass index, total bilirubin level, prothrombin time, blood loss and lymph node dissection time. A:Body mass index; B: Total bilirubin; C: Prothrombin time; D: Blood loss. BMI: Body mass index; TBIL: Total bilirubin; PT: Prothrombin time.

Further stratification according to BMI showed that patients with a preoperative BMI ≥ 21.9 kg/m2had significantly longer lymph node dissection times than did those with a BMI < 21.9 kg/m2(Figure 3A; 51.92 ± 9.94vs45.00 ± 13.73 min,t= 2.082,P= 0.042). Stratified analysis according to TBIL showed that patients with preoperative TBIL ≥ 57.5 μmol/L had significantly longer lymph node dissection times than did those with TBIL < 57.5 μmol/L (Figure 3B; 52.04 ± 11.03vs44.88 ± 12.81 min,t= 2.158,P= 0.036).

Figure 3 The effects of body mass index and total bilirubin on lymph node dissection time. A: Body mass index; B: Total bilirubin. aP < 0.05. BMI:Body mass index; TBIL: Total bilirubin.

Postoperative complications caused by lymph node dissection

None of the patients had postoperative complications caused by lymph node dissection, such as postoperative blood transfusion or long-term catheter catheterization caused by hemorrhage and lymphatic leakage.

DISCUSSION

In recent years, with the continuous improvement of minimally invasive technology and the widespread popularization of minimally invasive approaches, LPD has been promoted and applied in an increasing number of centers. However, it remains difficult to grasp surgical quality control[7-9]. An increasing number of scholars are concerned about how to streamline and modularize the complex process of LPD to achieve homogeneity of curative effects. Hilar lymph node dissection is a key procedure in the surgical process of LPD[10,11]. Traditionally, according to the anatomical distribution, we locally locate and remove lymph node tissues in batches. However, due to the diverse distributions of lymph nodes in the hepatic hilum, there may be anatomical variation and incomplete dissection of lymph node tissues during surgery, which can affect the treatment efficacy of surgery[12].

En blocresection of hepatic hilum lymph nodes is a relatively new technique that has been used in radical surgery for periampullary carcinoma, cholangiocarcinoma, and pancreatic head carcinoma in recent years. In this technique,en blocdissection is used to remove lymph node tissues from the hepatic hilum region as a whole to ensure thoroughness of the lymph node dissection. Studies have shown that, compared with traditional methods,en blocdissection of regional lymph nodes improves the number, integrity and efficiency of lymph node dissection and thus increases the radical resection rate[6,13]. However,en blochepatic hilum lymph node dissection also increases the difficulty and risk of surgery and has high surgical requirements.

On the basis of long-term clinical practice, we used the "five steps four quadrants" technique for en bloc resection of the hepatic hilar region. This technique started with the isolation of the No. 8a lymph node[14]. Then, according to the boundary of the HA/PV axis, the hepatic hilum region was divided into four zones: upper, lower, left and right. The four zones were dissected separately, and theen blocwas removed. The technique follows the concept of "simplification of complex problems and modularization of simple problems", thus allowing the dissection of hepatic hilum lymph node tissues more smoothly and thoroughly. Compared with traditional methods, the "five steps four quadrants" technique can be used to dissect lymph node tissues more completely. In addition, this technique avoids residual lymph nodes, increases the number of dissected lymph nodes, and thus improves the effectiveness of radical resection. Moreover, the concept of this technology is simple and easy to master. This technology is expected to shorten the learning curve and has potential value for popularization and application.

The results of the present study showed that,viathe use of "five steps four quadrants", the median number of dissected lymph nodes was six, which meets the standards required by experts and guidelines[15-18]. Moreover, this technique significantly improved lymph node dissection and allowed more thorough dissection of lymph node tissues in the hepatic hilum region. However, the postoperative pathological results suggested that the proportion of patients with positive lymph nodes was relatively low (23.1%, 12/52). However, long-term, multicenter studies with larger sample sizes are needed to explore whether these methods could improve patient prognosis. Furthermore, the median lymph node dissection and intraoperative blood loss were 50 min and 25 mL, respectively, indicating that proficiency in this technique can improve surgical efficiency and control intraoperative risk. Our study further showed that higher BMI, TBIL and PT may increase the difficulty of lymph node dissection. Therefore, to improve surgical confidence, beginners can select appropriate cases according to the three indicators. Due to the complete removal and thorough dissection of lymph nodes, none of the patients in this study experienced postoperative complications such as blood transfusion or long-term catheter implantation, which further confirmed the safety of this technique.

Although this study showed that the application of the "five steps four quadrants" technique in LPD patients is safe and effective, there are still some limitations. First, this was a single-center study with a relatively small sample size, which may have led to selection bias and statistical bias. Second, the effect of this technique on postoperative survival and recurrence could not be assessed due to the short follow-up time. Third, as surgical videos of previous patients without the implementation of the ''five steps four quadrants'' modularizeden blocdissection technique were missing, the control group was absent from this study. Therefore, multicenter, large-sample randomized controlled studies are needed to further verify the superiority of this technique. In addition, as a new surgical technique, "five steps four quadrants" still need to be further perfected and optimized. In clinical practice, this technique may be affected by complex anatomic variations, tumor invasion, preoperative biliary drainage, and other factors. In this study, there were 3 patients with relatively significant intraoperative blood loss. Further analysis of surgical video data showed that all of them had accidental tears of PV variant branches. Therefore, this technology requires that surgeons and assistants have a wealth of surgical experience. A more accurate preoperative evaluation is also necessary. The operating specifications and training system of this technology should be further improved in the future to ensure the stability and replicability of the technical path.

CONCLUSION

In general, the "five steps four quadrants" modularizeden blocdissection technique for hepatic hilum lymph nodes is safe and feasible for LPD. This method is expected to improve the efficiency of hepatic hilum lymph node dissection and shorten the learning curve and thus is worthy of further clinical promotion and application.

ARTICLE HIGHLIGHTS

Research background

Although theen-blocdissection of hepatic hilum lymph node shows many advantages in the radical treatment of several malignant tumors such as cholangiocarcinoma, periampullary carcinoma and pancreatic head cancer, the feasibility and safety of which for laparoscopic pancreaticoduodenectomy (LPD) require further clinical evaluation and investigation.

Research motivation

The motivation behind this article is to provide the emerging and valuable technique of the "five steps four quadrants" modularizeden-blocdissection in the field of hepatic hilum lymph node dissection of LPD.

Research objectives

The objective of this study is to explore the application value of the "five steps four quadrants" modularizeden-blocdissection technique for accessing hepatic hilum lymph nodes in LPD patients.

Research methods

A total of 52 patients who underwent LPD with the technique of "five steps four quadrants" modularizeden-blocdissection technique of hepatic hilum lymph node from April 2021 to July 2023 in our department were analyzed retrospectively.

Research results

There were 26 cases of pancreatic head cancer, 16 cases of periampullary cancer, and 10 cases of distal bile duct cancer. All patients successfully underwent the "five steps four quadrants" modularizeden-blocdissection technique without lymph node clearance-related complications such as postoperative bleeding or lymphatic leakage. Correlation analysis revealed significant associations between preoperative body mass index (BMI,r= 0.3581,P= 0.0091), total bilirubin (TBIL,r= 0.2988,P= 0.0341), prothrombin time (r= 0.3018,P= 0.0297) and lymph node dissection time. Moreover, dissection time was significantly correlated with intraoperative blood loss (r= 0.7744,P< 0.0001). Further stratified analysis demonstrated that patients with preoperative BMI ≥ 21.9 kg/m2 and TBIL ≥ 57.7 μmol/L had significantly longer lymph node dissection time (bothP< 0.05).

Research conclusions

In general, the "five steps four quadrants" modularizeden blocdissection technique for hepatic hilum lymph nodes is safe and feasible for LPD.

Research perspectives

This method is expected to improve the efficiency of hepatic hilum lymph node dissection and shorten the learning curve and thus is worthy of further clinical promotion and application.

FOOTNOTES

Co-corresponding authors:Qing Pang and Hao Jin.

Author contributions:Jin H and Pang Q contributed to the study concepts and design; Hu XS and Pang Q contributed to the manuscript preparation; Wang Y and Pan HT helped to perform the statistical analysis and the literature research; Zhu C and Chen SL contributed to data collection and analysis; Liu HC and Jin H edited the manuscript.

Supported byHealth Research Program of Anhui, No. AHWJ2022b032.

Institutional review board statement:This study received approval from the Ethics Committee of Anhui No. 2 Provincial People’s Hospital (approval No. 2022-011).

Informed consent statement:All study participants, or their legal guardian, provided informed written consent prior to operation.

Conflict-of-interest statement:All the authors report no relevant conflicts of interest for this article.

Data sharing statement:Participants gave informed consent for data sharing.

Open-Access:This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/

Country/Territory of origin:China

ORCID number:Qing Pang 0000-0001-8170-5085.

S-Editor:Yan JP

L-Editor:A

P-Editor:ZhangYL