The surgical treatment of pancreatic tumors includes pancreaticoduodenectomy (PD), distal pancreatectomy (DP), and total pancreatectomy. However, it is a hot topic of current research to preserve the organ function and maintain physiological access while reducing the incidence of postoperative complications and quality of life after surgical intervention for benign or malignant tumors of the pancreas. For benign and junctional tumors of the pancreas, restrictive pancreatic resection procedures, namely, middle pancreatectomy (MP), local enucleation, and subtotal resection with preservation of the mid-pancreatic segment, have been proposed to obtain better functional outcomes without compromising the radicality of the tumor in the treatment of benign or low-grade malignant tumors (1, 2). However, in the treatment of benign and junctional tumors of the pancreas, laparoscopic MP offers less experience to draw from because of its surgical difficulty and the limited number of cases. To this end, investigations were hereby carried out over the short- and long-term outcomes of organ-preserving laparoscopic pancreatectomy for benign or low-grade malignant pancreatic tumors performed at our center, and experiences of the center with laparoscopic MP were provided. In view of this, a retrospective analysis was conducted to summarize the short- and long-term outcomes of MP for benign or low-grade malignant pancreatic tumors performed at a single center over the past 5 years.

With the development of imaging techniques, an increasing number of benign and low-grade malignant tumors of the pancreas are being identified, and MP resection seems to be more suitable for the abovementioned lesions than PD with PD or even expanded PD, which preserves more normal pancreatic tissues. Although MP is considered to have a high incidence of POPF as well as a high bleeding rate, it is indeed an acknowledged technique for pancreatic resection, and results in long-term outcomes showing good endocrine function are especially encouraging. Since Baca and Bokan reported the first application of laparoscopic MP for the treatment of chronic pancreatitis in 2003 (11), the relevant literature has also elaborated on the use of laparoscopic, robotic MP for the treatment of benign and junctional tumours in the neck and body of the pancreas (3, 12–17). Although MP is a surgical procedure for benign or low-grade malignant tumors located in the neck or body of the pancreas, and seems to be more reasonable for benign tumors, for low-grade malignant or malignant tendencies, for example, PanIN-3, IPMN in combination with the presence of high-risk stigmata or worrisome features, and it is important to examine the pancreatic lesions preoperatively with histological examination and end-stage dissection, as well as to examine the pancreatic lesions (18). In a study of seven recurrent cases of open MP, two patients with a final pathology of MD-IPMC had positive margins and were eventually received treatment again, whereas the BD-IPMcis had no recurrence, a result that suggests that BD-IPMN appears to be more suitable for MP (19). In addition, the application of MP in early Pancreatic ductal adenocarcinoma (PDAC) is being initially explored (20).

High incidence of complications after MP has attracted the attention from many physicians. POPF remains one of the major causes of postoperative pancreatic risk events, and its risk factors are mainly affected by the texture of the pancreas and the diameter of the pancreatic duct (21). Compared with DP and PD, MP is associated with higher rates of POPF and postoperative bleeding (22, 23). In a previous meta-analysis, the MP group also had a high rate of postoperative-related clinical pancreatic fistula and a higher incidence of postoperative bleeding compared with the DP group (24). Crippa et al. (19) carried out a study of MP with the largest sample size study at that time and observed a higher rate of pancreatic fistula and complications in MP. However, the difference was not statistically significant compared to the same group of the pancreatic corporal tail resection group, and the endocrine and exocrine insufficiency rate was significantly lower in the MP group. A single-center empirical study involving 50 cases with low-grade malignancy concluded that MP was effective in preserving cephalic and distal pancreatic remnants without significantly increasing postoperative complications compared with conventional pancreatic resection (25). In the application of laparoscopic MP, Safi Dokmak et al. (26) reported the results indicating a postoperative complication rate of 74% and a CR-POPF rate of 22%. However, the main reasons for the high incidence of pancreatic fistula after MP might include the following: (1) compared to malignant tumors, benign and junctional tumors have soft pancreatic parenchyma; (2) there is often no obstruction in benign and junctional tumors, and the pancreatic duct is not dilated and has a small diameter; (c) there are two pancreatic sections in the middle pancreatic resection.

Reconstruction of the middle pancreatic resection Gastrointestinal (GI) tract mainly includes pancreatic-intestinal anastomosis, pancreatic-gastric anastomosis and “Ω” anastomosis. However, there is no definite conclusion upon the choice of pancreatic middle resection GI reconstruction. Herein, all of the 17 cases were closed by proximal suture and distal pancreatojejunostomy (PJ). According to the criteria of pancreatic fistula (5), there were nine cases of grade A fistula, three of grade B fistula and no grade C fistula, and the incidence of pancreatic fistula was 69%, while that of CR-POPF was 17%. In addition, it is similar to the reported laparoscopic MP, and the incidence of grade C fistula was lower (27). The incidence of POPF was likewise not increased compared to open MP (24, 28). All grade B fistulas were discharged from the hospital after recovery from good drainage, drain flushing, and nutritional support therapy. In terms of nutritional support therapy, Andrew A et al. suggested that patients in the comprehensive management of pancreatic cancer should not only consider anti-inflammatory diets, dietary supplements, and lifestyle modifications but also proposed a combination of traditional Chinese and Western medicine. Although it is a complex process, it helps to some extent in the treatment as well as recovery of the patient (29). In addition to PJ, the ability of PG anastomosis to reduce the incidence of POPF was also reported in other literature. In a randomized controlled study, pancreatic gastric anastomosis and pancreatico-enteric anastomosis were shown to have no difference in the incidence of pancreatic leakage as well as postoperative effects on endocrine and exocrine function, and the operative time was less (30). What is more noteworthy is that cross-disciplinary developments have also attracted the attention of pancreatic surgeons, and a technique called the “Huscher technique” has been applied to pancreatic surgery, resulting in easier pancreatic-enteric anastomosis, a relatively low incidence of POPF, and little or no impairment of exocrine function (31).

In this paper, the operative time was 393.2 ± 57.9 min (range: 225–497 min), the amount of intraoperative bleeding was 211.7 ± 113.9 ml (range: 50–500 ml), and the period for postoperative hospital stay was 19.4 ± 7.6 days (range: 8–37 days). In a review of the reported literature on laparoscopic MP (14, 23, 32–35), the operative times were 225–480 min (median operative time: 380 min), 120–285 min (median operative time: 200 min), 350 ± 63.4 min, intraoperative bleeding 50–800 ml, 477.1 ± 388.2 ml, and postoperative hospitalization time, 13.8 ± 7.3 days. In this study, the choice of pancreatic–intestinal anastomosis possible explained the relatively long operative time (15), while the relatively low amount of intraoperative bleeding (13, 14, 33) might be attributed to the relationship between the tumor and blood vessels and the existence of vascular variants. In terms of hospitalization time, the postoperative hospitalization time was 19.2 ± 7.6 days in this paper, relatively longer compared to that reported in other literature (13), which might be related to postoperative management, including the choice of time for postoperative feeding, the choice of time for drainage tube removal, and the fact that all pancreatic fistula patients were managed in hospital and discharged after complete healing. However, no case of abdominal infection, impaired gastric emptying, postoperative bleeding, bile leak, reoperation, or death was hereby reported.

MP maximized the preservation of normal physiological function of the pancreas while performing tumor resection, resulting in better preservation of endocrine function, which was significantly lower than other types of pancreatic surgery in comparison and could improve the postoperative quality of life of the patients (1, 2, 23, 33–36). In terms of endocrine function, the persistence of NODM was observed in benign or malignant tumors after PD with similar incidence. In terms of exocrine function, the presence of PEI after sexual PD in patients with benign and malignant tumors was 25.2% and 49.1%, respectively (37). Compared with DP, MP still had a lower incidence of endocrine dysfunction (25).

Herein, one of the cases involved a diabetic patient. By monitoring random blood glucose, the postoperative random blood glucose of the patients for the first 3 days was 7.4 ± 1.0 mmol/l in all cases, while, in comparison, the highest random blood glucose was 8.1 ± 1.0 mmol/l on the first day postoperatively, and the highest random blood glucose was 11.3 mmol/l for diabetic patients. The monitored fasting blood glucose 3 days after feeding and three postprandial blood glucose was 6.8 ± 1.0mmol/l. In comparison, the highest blood glucose on the first day after feeding was 6.8 ± 1.2 mmol/l, and the highest random blood glucose was 12.1 mmol/l, which was still a random postprandial blood glucose in diabetic patients. In this paper, none of the above cases with elevated blood glucose was treated with insulin or did not change the original glucose–lowering regimen, and no endocrine dysfunction was observed, which is consistent with other reports. The higher blood glucose on the first postoperative day and the first day after feeding may be attributed to surgical stress, parenteral nutrition and the diet. In terms of exocrine function, postoperative–formed fecal PEI was checked to be 479.6 ± 114.3 µg/g feces (296.4–677.5 µg/g feces) by hospitalization, and all patients did not show any decrease in PEI or signs of exocrine dysfunction such as diarrhea. In the discharge and outpatient follow–up, all patients did not have diarrhea or oral pancreatic enzyme drug–related treatment after discharge. Laparoscopic resection of the middle part of the pancreas did not cause any significant effect on the endocrine function of the pancreas.

Under strict control of clinical indications, the laparoscopic MP is proven to be safe and feasible in the treatment of benign or low–grade malignant tumors in the body of the pancreatic neck, causing no increased risk of intraoperative and postoperative complications and endocrine dysfunction of the pancreas. However, this thesis is still restricted by a limited sample size as well as a short period of case follow–up. Further breakthroughs could be made in these areas. In addition, with the emergence of artificial intelligence (38), more precise resection with preservation of parenchymal organs is expected to receive increasing attention. There will be more multi–center and large sample studies.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/supplementary material.

The studies involving humans were approved by Hunan Provincial People’s Hospital/First Affiliated Hospital of Hunan Normal University. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study. Written informed consent was obtained from the individual(s) for the publication of any potentially identifiable images or data included in this article.

YaL and WZ are mainly responsible for data analysis and paper writing and revision. YaL and MD are mainly responsible for paper revision, translation and embellishment. WZ and JZ are mainly responsible for data collection and processing analysis. YW is mainly responsible for data collection. XH is mainly responsible for paper ethics. YiL was mainly responsible for the design of the paper, data analysis, and paper revision. WC was mainly responsible for providing design input, data processing analysis, and paper revision of the paper. All authors contributed to the article and approved the submitted version.