Feasibility and outcomes of laparoscopic enucleation for pancreatic neoplasms

Traditionally, benign or borderline malignant pancreatic tumors have been treated by major standard resections such as pancreaticoduodenectomy (PD) and distal pancreatectomy (DP) with or without splenectomy [1]. Although these procedures can be performed with low morbidity and mortality rate, resection of a large amount of normal pancreas can be associated with an increased risk of endocrine or exocrine insufficiency [2]. In this matter, some authors reported that enucleation can be considered as an alternative surgical procedure [3, 4, 5]. Compared with major resections, enucleation is charaterized by extensive parenchymal preservation, less operation time, and faster recovery [6]. With the advancement of laparoscopic techniques and instruments, laparoscopic approach for pancreatic lesions has become an increasingly used procedure. Although prospective randomized controlled study is absent, several reports documented the feasibility, safety, and effectiveness of laparoscopic enucleation (LE) in benign or borderline malignant pancreatic tumors [1, 5, 7, 8]. However, these reports included case reports and small series. Therefore, the purpose of this study was to present the surgical experience in our institution and to analyze the postoperative outcome of LE for benign or borderline malignant tumors of the pancreas.

In particular, there is very limited information on the outcomes of LE compared with laparoscopic distal pancreatectomy (LDP). Therefore, we investigated clinical outcomes to evaluate the safety and efficacy of LE compared with LDP in benign or borderline malignant tumors of the pancreas.

After Soonchunhyang University Bucheon Hospital Institutional Review Board's approval, from May 2005 to December 2011, 11 consecutive patients who underwent LE for benign or borderline malignant tumors of the pancreas were recruited into the current study. We retrospectively analyzed the medical rescords and this study conformed to the ethical guidelines of the Declaration of Helsinki.

In all cases, ultrasonography (USG), CT, and MRI including magnetic resonance cholangiopancreatography (MRCP) were routinely performed before operation. The indications of LE were followed: (1) preoperative evaluations strongly suggesting benign or borderline malignant nature tumor, (2) no involvement of the main pancreatic duct, and (3) outwardly growing tumor with small tumor bed. For small benign or borderline malignant lesions (less than 2 cm), we recommended close observation. However, if the lesion had solid portion or if the patient strongly wanted surgery, we performed operation. Complete tumor removal with clear margins was the management principle in each case. The following characteristics were collected and analyzed on each patient: age, sex, body mass index (BMI), presentation, preoperative pancreatitis, preoperative diagnosis, tumor location, tumor size, final pathology, complication, and recent follow-up details. In addition, the perioperative outcomes such as operation time, blood loss, return to normal bowel movement, return to adequate oral intake, length of postoperative hospital stay, pancreatic fistula rate, overall postoperative mortality, and recurrence rate were analyzed. According to the International Study Group of Pancreatic Fistula (ISGPF) criteria, pancreatic fistula was defined as any measurable drainage from an operatively placed drain on or after postoperative day 3, with an amylase content greater than 3 times the upper limit of normal serum amylase levels [9].

All patients underwent regular follow-up examinations postoperatively every 6 months for 5 years and annually thereafter. The mean follow-up period was 44.3 ± 23.9 months. This included a clinical examination, blood tests, CT of the abdomen, and chest radiography. Medical records and survival data were obtained for all patients.

LE procedure

After general anesthesia patients were placed in a right semilateral decubitus position. Under preparing and drapping in the usual sterile manner, the surgeon, the camera assistant, and the scrub nurse were positioned to the right side of the patient, and the first assistant stood to the left side of the patient. A 12-mm balloon trocar (telescope route) was first inserted through an infraumbilical minilaparotomy wound and pneumoperitoneum (12 mmHg) was achieved by CO₂ insufflation. Under the laparoscopy-providing vision, three other trocars were inserted into the following locations: the epigastrium (5 mm) for the left hand of the surgeon; the midclavicular line below the costal arch (12 mm) for the right hand of the surgeon; the left flank (5 mm) for assistance (Fig. 1).

Fig. 1
Trocar placement for laparoscopic enucleation.

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The gastrocolic ligament was divided for entrance to the pancreas using harmonic scalpel (Ethicon, Cincinnati, OH, USA) and electrocautery. Laparoscopic USG probe was used through a 12-mm trocar and applied directly to the anterior surface of the pancreas to confirm the location of the tumor and identify its relationship to the splenic vessels and main pancreatic duct. Pancreatic dissection was performed using harmonic scalpel and bleeding between tumor and normal parenchyma was controlled by a 5-mm bipolar electrocoagulation instrument (Ethicon).

The specimen was then placed in a LapBag (SJM, Paju, Korea) and removed through a minimally extended umbilical port incision. One closed suction drain was placed in the site of the enucleation.

During the study period, 11 patients underwent LE (Table 1). There were 10 women (91%) and 1 man (9%) with a mean age of 43.1 ± 11.9 years, and the mean BMI was 25.1 ± 6.4 kg/m². The most common presentation was incidental finding (n = 8, 73%), followed by abdominal pain (n = 2, 18%), and abdominal mass (n = 1, 9%). Also, there were no patients with preoperative pancreatitis. The tumors that had no symptoms (incidental finding) were detected by routine health checkup. All 11 patients who underwent LE were completed laparoscopically without conversion. In two patients (case 7 and case 9), cystic fluid was spilled during operation. The tumors were located in the body (n = 5, 45%) and tail (n = 6, 55%) of the pancreas. The mean operation time was 97.4 ± 16.6 minutes, and mean blood loss was 35.9 ± 11.9 mL. The final histopathological diagnoses included 4 mucinous cystadenomas, 4 serous cystadenomas, 1 solid pseudopapillary neoplasm (SPN), 1 simple cyst, and 1 Castleman disease. The mean diameter of the resected tumors was 4.0 ± 3.3 cm. One patient (9%) developed postoperative complication. This patient had pancreatic fistula and recovered with conservative management. The mean length of postoperative hospital stay was 5.5 ± 1.7 days, and the mean follow-up period was 44.3 ± 23.9 months. All of the patients are alive and disease-free (Table 2).

Table 1
Clinical feature and characteristics of the laparoscopic enucleation group

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Table 2
Pathologic summary and follow-up data of the laparoscopic enucleation group

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With the introduction of newer sophisticated abdominal imaging techniques, benign or borderline pancreatic tumors such as pancreatic cystic neoplasms are being detected with increasing frequency [4]. Although most of these lesions are tumors benign in nature, they have malignant potential [3]. Thus, many surgeons have been performing major standard resections such as PD and DP with or without splenectomy [1]. Although these procedures can now be performed with low morbidity and mortality rates, resection of a large amount of normal pancreas can be associated with increasing risk of endocrine or exocrine insufficiency [2]. Especially, DP can induce diabetes when pancreatic resection exceeds 75% [1]. For these reasons, parenchyma-sparing procedures such as enucleation or central pancreatectomy have been performed with increasing frequency [1, 3, 4, 5, 6].

Enucleation of pancreatic tumors is a well established parenchyma-sparing and function-preserving surgical procedure for pancreatic lesions such as endocrine tumors, serous or mucinous cystadenomas, and SPN [3, 4, 5, 6, 7, 8]. Moreover, several reports documented the feasibility, safety, and effectiveness of LE in benign or borderline malignant pancreatic tumors [1, 7, 8]. The current study included 4 mucinous cystadenomas, 4 serous cystadenomas, 1 SPN, 1 simple cyst, and 1 Castleman disease. All 11 patients who underwent LE were completed laparoscopically without conversion and no recurrences were recorded after surgery. Although further evaluation should be conducted, our study shows that LE is a clinically safe and effective procedure for benign or borderline malignant pancreatic tumors.

Preoperatively and intraoperatively, the following fators should be considered for performing LE: localization of the tumor, malignancy potential of the tumor, distance between a lesion and the main pancreatic duct, and growing pattern of the tumor.

One of the most important concerns during LE is the localization of the tumor. With the advancement of preoperative imaging techniques and intraoperative localization with laparoscopic USG, open exploration with bimanual palpation of the pancreas may not be absolutely necessary [8]. Recent reports on the use of laparoscopic USG have shown a success rate of 80% to 100% in localizing and outlining the margins of pancreatic tumors [10, 11]. In our study, laparoscopic USG was routinely performed and pancreatic lesions were localized in all 11 cases.

The malignant potency of pancreatic cystic tumors is another issue of concern. Preoperative noninvasive imaging techniques such as USG, CT, and MRI are unreliable to accurately distinguish among the different pancreatic cysts [4]. Recently, endoscopic ultrasound (EUS) guided fine-needle aspiration (FNA) has been suggested as a method to differentiate between benign and malignant lesions [3, 4, 12]. However, EUS guided FNA has the risk of malignant cell spillage into the peritoneum with subsequent seeding and reduced survival [4]. For these reasons, our institution does not recommend preoperative EUS guided FNA. Intraoperative frozen-section examination is an important method to obtain the information on the nature of cystic mass [5]. So, in our institution, we routinely used frozen-section examination to clarify a preoperative confusing diagnosis.

The distance between a lesion and the main pancreatic duct has been considered to affect the risk of main duct damage and pancreatic leak [1, 5, 6]. Some authors suggested that, for enucleation to be performed safely, the lesion should be at least 2-3 mm from the main pancreatic duct and not too deep in the parenchyma [1, 5]. Preoperative MRCP can measure the distance between a lesion and the main pancreatic duct and assists in the decision to perform enucleation. In the current study, MRCP was routinely performed and the patients were considered candidates for enucleation if their lesion did not involve the main pancreatic duct and had a pattern of growing outwardly with a small tumor bed.

Pancreatic fistula is the most serious complication in all pancreatic surgeries. The incidence of pancreatic fistula after open enucleation has been reported to range from 18.2% to 50% [3, 4, 5, 6]. However, the reported incidence of pancreatic fistula after LE was lower (range, 9.1%-13%) than that reported after open enucleation [1, 13]. Dedieu et al. [1] suggested that this improvement in pancreatic duct control could be explained by the slower and more meticulous pancratic enucleation. In the current study, 1 patient (9%) had pancreatic fistula according to the definition of ISGPF, and this patient recovered with conservative management. This results in precise selection of patients, which includes a superficial lesion that does not involve the main pancratic duct and has an outgrowing aspect with small tumor bed.

Short operation time, less blood loss, and more rapid recovery are often cited as the prominant advantages of enucleation [6]. Especially, extensive preservation of the normal pancreatic tissues is an another merit of enucleation. Reported data show that pancreatic enucleation preserve pancreatic exocrine and endocrine function [5]. In our study, there was no evidence of new-onset exocrine and endocrine insufficiency. Also, when compared to LDP group (from July 2007 to February 2012, 41 patients underwent LDP in our institution for benign or borderline malignant tumor of the pancreas), the LE group had statistically significant shorter postoperative hospital stays with short operation time and less blood loss (Table 3).

Table 3
Comparison of perioperative outcomes between LE and LDP group

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In conclusion, the results of this study show that LE in patients with a benign or borderline malignant tumor of the pancreas is a safe and effective procedure. On the basis of our results and considering the general advantages of laparoscopic surgery, LE should be considered as a treatment option for benign or borderline malignant pancreatic lesions that do not involve the main pancratic duct and have an outgrowing aspect with small tumor bed. But, our study has some limitations. It was a retrospective study and LE group was only 11 patients, which is relatively small. So, further evaluation, including prospective randomized clinical trials are needed to confirm these results.