Efficacy of Pancreatic Dissection With a Triple-row Stapler in Laparoscopic Distal Pancreatectomy: A Retrospective Observational Study

Background: Postoperative pancreatic fistulas (POPFs) occur after 20% to 30% of laparoscopic distal pancreatectomies. This study aimed to evaluate the clinical efficacy of laparoscopic distal pancreatectomy using triple-row staplers in preventing POPFs. Methods: Between April 2016 and May 2023, 59 patients underwent complete laparoscopic distal pancreatectomies. There were more females (n=34, 57.6%) than males (n=25, 42.4%). The median age of the patients was 68.9 years. The patients were divided into slow-compression (n=19) and no-compression (n=40) groups and examined for pancreatic leakage. Both groups were examined with respect to age, sex, body mass index (BMI), pancreatic thickness at the pancreatic dissection site, pancreatic texture, diagnosis, operative time, blood loss, presence of POPF, date of drain removal, and length of hospital stay. In addition, risk factors for POPF were examined in a multivariate analysis. Results: Grade B POPFs were found in 9 patients (15.3%). Using univariate analysis, the operative time, blood loss, postoperative pancreatic fluid leakage, day of drain removal, and hospital stay were shorter in the no-compression group than in the slow-compression group. Using multivariate analysis, the absence of POPFs was significantly more frequent in the no-compression group (odds ratio, 5.69; 95% CI, 1.241-26.109; P=0.025). The no-compression pancreatic dissection method was a simple method for reducing POPF incidence. Conclusions: The method of quickly dissecting the pancreas without compression yielded better results than the method of slowly dissecting the pancreas with slow compression. This quick dissection without compression was a simple and safe method that minimized postoperative pancreatic fluid leakage, shortened the operative time and length of hospital stay, and reduced medical costs. Therefore, this method might be a clinically successful option.

(Surg Laparosc Endosc Percutan Tech 2024;34:295-300) D istal pancreatectomy (DP) is commonly performed for pancreatic tail tumors.2][3] Similarly, recent advances in medical technology have led to a decline in the incidence of complications after pancreatectomies.However, the rate of postoperative pancreatic fistula (POPF) formation after DPs is reportedly 20% to 40%. 1,4Pancreatic leakage causes intraabdominal abscesses, bleeding, wound infections, sepsis, delayed gastric emptying, and ileus, [5][6][7][8] resulting in longer hospital stays and increased medical costs. 9everal pancreatic transection and stump closure techniques have been proposed to reduce the incidence of POPF.These methods include hand-sewn closure, 10 stapled closure, 11 bipolar scissors, 12 ultrasound-guided transection, 13 LigaSure transection, 14 and fibrin glue application. 15Stapled closure has recently become the standard technique for pancreatic stump closure because of its technical simplicity, especially when performing Lap-DP.A triple-row stapler and slow parenchymal compression technique have been applied in recent years. 11,16However, even though most facilities standardly perform pancreatectomies using a triple-row stapler and a slow parenchymal compression technique, the reported rate of pancreatic fluid leakage is very high.Since the triple-row stapler and slow parenchymal compression techniques have been reported, further advances in pancreatectomy methods have rarely been reported.We believe that a simple and easy method is needed to further reduce pancreatic fluid leakage during pancreatectomies.Therefore, this study aimed to evaluate the clinical efficacy of Lap-DP using a triple-row stapler for pancreatic resections.
The following patient data were collected: age, sex, body mass index (BMI), pancreatic thickness at the pancreatic dissection site, pancreatic texture, pancreatic duct dilatation, diagnosis, surgical procedure (Lap-DP and laparoscopic spleen-preserving DP), operative time, blood loss, the occurrence of POPF, drain removal day, and hospital stay.POPF was defined according to the classification system of the International Study Group of DOI: 10.1097/SLE.0000000000001284

Surgical Procedures
The procedures were performed by 2 hepatobiliary surgeons with 20 and 15 years of experience, respectively.Every patient was in the open-leg position, with the surgeon on the patient's right side, the assistant on the patient's left side, and the scopist standing between the patient's legs.Five ports were used, with a 12 mm port used only on the lower left side of the patient and 5 mm ports used on the other sites.The stomach was elevated in the epigastric region using Nathanson Hook Liver Retractors (Yufu Itonaga Co., Ltd.).The pancreas was dissected using the Powered ECHELON FLEX (Johnson & Johnson) 60 mm green cartridge.The excised specimen was removed through a 4 to 5 cm transverse incision above the pubis.The patients were divided into 2 groups according to the time of surgical procedure: the slow-compression group [slow compression for 5âmin followed by slow dissection for another 5âmin using the Powered ECHELON FLEX; from April 2016 to June 2018 (first half)] and the no-compression group [immediate and quick dissection without compression; from July 2018 to May 2023 (second half)].No additional treatment or covering of the pancreatic stump remnant, such as omental wrapping, was performed.

Perioperative Management
Drain amylase levels were measured on postoperative days 1 and 3. Patients were encouraged to start eating on postoperative day 1.If the color of the drainage fluid on day 3 and the amylase levels were normal, the drain was removed on day 3. Somatostatin analogs were not used.Antibiotics were only administered during surgery.

Statistical Analyses
All statistical data were analyzed using SPSS version 26.0 for Windows (IBM).Continuous variables are expressed as means ± SD.The significance of differences in the distribution of values was tested using the Shapiro-Wilk test.
Comparisons between the 2 groups were performed using the Mann-Whitney U test.Statistical significance was determined using the paired t test.For dichotomous variables, we used the χ 2 or Fisher exact tests, as appropriate.Variables with P < 0.5 were entered into a multivariate logistic regression analysis to determine independent risk factors for clinical pancreatic fistulas.The independent risk factors for the variables are expressed as odds ratios (ORs) with 95% CIs.Statistical significance was set at P < 0.05.

RESULTS
Table 1 shows the clinical characteristics and surgical details of the patients.All patients were Japanese, and there were more females (n = 34, 57.6%) than males (n = 25, 42.4%).The median age of the patients was 68.9 years.Pancreatic cancer was the primary cause of death (50.8%).The mean operative time was 194.5 minutes, and the mean blood loss was 125.6 mL.There were 9 cases of main pancreatic duct dilation, with duct diameters ranging from 1 to 7.5 mm and a mean diameter of 1.54 mm.Lap-DP was performed in 52 patients (88.1%), and the spleen was preserved in 7 patients (11.9%).In addition, 9 patients (15.3%) had Grade B POPFs.None of the patients died or developed grade C POPFs.The median number of days to drain removal was 13.3 days, and the mean hospital stay was 9.4 days.No complications other than pancreatic leakage above Clavien-Dindo â¢a were observed.
Table 2 presents the characteristics of the slow-compression and no-compression groups.Sex, BMI, pancreatic thickness at the pancreatic dissection site, pancreatic texture, pancreatic duct dilatation, pancreatic duct diameter, and diagnoses were not significantly different between the 2  groups.However, univariate analysis showed that the operative time (218.7 vs. 183.0min, P = 0.004), blood loss (165.8 vs. 106.5 mL, P = 0.047), postoperative pancreatic fluid leakage (31.6% vs. 7.5%, P = 0.017), day of drain removal (23.2 vs. 8.5 d, P ≤ 0.001), and hospital stay (11.1 vs. 8.6 d, P = 0.006) were lower in the no-compression group than in the slow-compression group.The no-compression group was older than the slow-compression group (63.5 vs. 71.5 y, P = 0.003).
Characteristics were also compared between patients with and without POPF (POPF and no-POPF groups, respectively) (Table 3).In the univariate analysis, sex and BMI were not significantly different between the 2 groups.There were also no significant differences in the thickness of the pancreas at the dissection level, pancreatic texture, pancreatic duct dilatation, pancreatic duct diameter, operative time, or intraoperative blood loss.However, the number of days until drain removal (58 vs. 5.1 d, P < 0.001) and hospital stay (14.4 vs. 8.5 d, P < 0.001) were significantly shorter in the no-POPF group and significantly shorter in the no-compression group (P = 0.017).The median age was higher in the no-POPF group than in the POPF group (59.3 vs. 70.7,P = 0.016).
The receiver operating characteristic (ROC) curve showed the relationship between the thickness of the pancreatic dissection and pancreatic leakage (Fig. 2).The area under the curve was 0.661 (95% CI, 0.486-0.837),with P = 0.072.ROC curve analysis of the thickness of the pancreatic dissection for the occurrence of POPF indicated a cutoff value of 14.3 mm (sensitivity, 67%; specificity, 56%).

DISCUSSION
This study demonstrated that the method of quickly dissecting the pancreas without compression yielded better results than the method of slowly dissecting the pancreas with slow compression.Our method is safe and simple and can be performed by anyone.Kawai et al 18 reported a 12.4% incidence of grade B POPF in DPs reinforced with staplers in a multicenter cohort study.In our report, the incidence of grade B POPF was 7.5%; therefore, our no-compression method was safe and simple.
Various pancreatic dissection methods have been devised and widely reported.Kleeff et al 5 concluded that pancreatic leakage was greater with a stapler than with other methods.However, they used a 2-row stapler instead of a 3-row stapler.Ban et al 19 reported that pancreatic dissection using a 3-row stapler resulted in less pancreatic leakage than without a stapler.Although the actual pancreatic dissection method was not described, the authors concluded that pancreatic dissection using a stapler is safe and simple.However, whether a 2-row or 3-row stapler should be used clinically remains debatable because reports on the frequency of pancreatic leakage vary. 7,20Nevertheless, the key point is the efficient closure of both the main and microscopic pancreatic ducts.Chong et al 21 reported that pancreatic leakage was the same regardless of whether stapled closure or suture closure was used, with an incidence of ~20%. 21While it is generally reported that pancreatic leakage occurs in ~20% of cases, we were able to reduce the rate to 7.5% using our new method.
Our method of pancreatic dissection using a stapler successfully reduced pancreatic leakage for the following reasons.The staples are wide enough to allow for slow compression and time-consuming dissection, resulting in impaired blood flow to the pancreatic fragment, which in turn leads to necrosis of the fragment and increased leakage of  23 necrosis and pancreatic leakage also occurred after hand-sewn pancreatic parenchymal closure, although the pressure at the transection level was higher than in stapler closure.In contrast, Chikamoto et al 24 found no changes in the histopathologic findings of pancreatic fragments, regardless of whether the pancreas was slowly compressed, not compressed, or crushed and dissected.However, they noted that the pressure at the pancreatic fragment was highest in the timeless group, which may have prevented pancreatic leakage.Our no-compression method of immediate dissection without crushing the pancreatic ducts was able to close not only the main pancreatic ducts but also the microscopic pancreatic ducts with sufficient pressure.Consequently, pancreatic juice leakage was reduced.
Various risk factors for pancreatic leakage have been reported.Pancreatic thickness at the level of pancreatectomy, [25][26][27] high BMI, [27][28][29][30] high volume blood loss, 30 and long operative time 30 have been reported as risk factors for pancreatic leakage; however, in our study, there were no significant differences.In our study, younger age was a risk factor for developing POPF in the multivariate analysis.Yoshioka et al 31 also reported that younger age is a risk factor for POPF.This indicates an age-related decline in pancreatic exocrine function and reduced pancreatic regenerative function after DP may explain why the POPF rate after DP is lower in older patients.
In the present study, comparing the surgical time between the no-compression and slow-compression groups, the operative time was significantly shorter in the no-compression group.Our no-compression method was expected to shorten the time by ~10 minutes compared to the conventional slow-compression method, but it actually shortened the time by ~30 minutes.This outcome may be related to the learning curve of the team.The team had 2 surgeons, with one being the assistant and the other being the main surgeon.The operative time may have been shorter than it actually was in the no-compression group in the second half of the study because of the increased experience of the team.The difference in blood loss between the 2 groups was likely also due to the learning curve.

FIGURE 1 .
FIGURE 1. Between April 2016 and May 2023, 96 patients underwent distal pancreatectomies at the Tokai University Hachioji Hospital.

FIGURE 2 .
FIGURE 2. The ROC curve shows the relationship between the thickness of the pancreatic dissection and pancreatic leakage.

TABLE 2 .
Comparison of Different Pancreatic Dissection Methods

TABLE 3 .
Comparison Between POPF and no-POPF Groups

TABLE 4 .
Risk Factors of Clinical Pancreatic Fistula NS indicates not significant.