Laparoscopic spleen-preserving total pancreatectomy for the treatment of low-grade malignant pancreatic tumors: Two case reports and review of literature

Abstract

BACKGROUND

Function-preserving pancreatectomy can improve the long-term quality of life of patients with benign or low-grade malignant tumors, such as intraductal papillary mucinous neoplasms (IPMNs) and mucinous cystic neoplasms. However, there is limited literature on laparoscopic spleen-preserving total pancreatectomy (L-SpTP) due to technical difficulties.

CASE SUMMARY

Patient 1 was a 51-year-old male diagnosed with IPMN based on preoperative imaging, showing solid nodules in the pancreatic head and diffuse dilation of the main pancreatic duct with atrophy of the distal pancreas. We performed L-SpTP with preservation of the splenic vessels, and the postoperative pathology report revealed IPMN with invasive carcinoma. Patient 2 was a 60-year-old male with multiple cystic lesions in the pancreatic head and body. L-SpTP was performed, and intraoperatively, the splenic vein was injured and required ligation. Postoperative pathology revealed a mucinous cystic tumor of the pancreas with low-grade dysplasia. Both patients were discharged on postoperative day 7, and there were no major complications during the perioperative period.

CONCLUSION

We believe that L-SpTP is a safe and feasible treatment for low-grade malignant pancreatic tumors, but more case studies are needed to evaluate its safety, efficacy, and long-term outcomes.

Key Words: Complete laparoscopic surgery; Spleen-preserving total pancreatectomy; Low-grade malignant pancreatic tumors; Function-preserving pancreatectomy; Case report

Core Tip: Spleen-preserving total pancreatectomy (SpTP) can provide patients with a higher long-term quality of life for benign or low-grade malignant pancreatic tumors. However, there is limited literature on laparoscopic SpTP due to technical difficulties. This article reports two cases of laparoscopi SpTP (LSpTP). The postoperative pathology reports showed intraductal papillary mucinous neoplasms and mucinous cystic neoplasm, respectively. Both patients had no major complications during the perioperative period. We believe that LSpTP is a safe and feasible treatment for low-grade malignant pancreatic tumors.

INTRODUCTION

Function-preserving pancreatectomy, such as preserving the pylorus, spleen, and duodenum, contributes to better quality of life in the long term for patients with benign or low-grade malignant pancreatic tumors, such as intraductal papillary mucinous neoplasm (IPMN) and mucinous cystic neoplasm (MCN)[1,2]. Spleen-preserving total pancreatectomy (SpTP) has been reported as a treatment for low-grade malignant pancreatic tumors and even pancreatic cancer[3,4]. Additionally, with the widespread use of minimally invasive techniques such as laparoscopy and robotics, laparoscopic pancreaticoduodenectomy and laparoscopic total pancreatectomy have been recommended for patients with pancreatic tumors, including pancreatic cancer. These minimally invasive approaches have been proven to be safe, feasible and less invasive. However, laparoscopic SpTP (LSpTP) is still limited in its application due to technical difficulties, and there are only scattered case reports in the literature. This article reports two cases of SpTP performed under complete laparoscopic surgery, providing a valuable reference and supporting the safety and efficacy of this procedure.

CASE PRESENTATION

Chief complaints

Case 1: A 51-year-old male patient with a history of abnormal liver function for more than 4 months and the discovery of a pancreatic mass for 5 d was admitted to the Peking Union Medical Collage Hospital (PUMCH) in March 2022.

Case 2: A 60-year-old male patient with a history of upper abdominal discomfort for 1 month and the discovery of a pancreatic mass for 10 d was admitted to PUMCH in November 2023.

History of present illness

Case 1: Four months before admission, the patient had abnormal liver function test results, including alanine transaminase levels of 265.24 U/L, aspartate transaminase levels of 74.50 U/L, gamma-glutamyl transpeptidase levels of 575.30 U/L, and a total bilirubin (Tbil) level of 14.40 µmol/L. There were no symptoms of jaundice. More than 1 month before admission, the patient experienced dark urine and an increased frequency of bowel movements, approximately 4-5 times per day, with loose stools. The patient also gradually lost weight, with a decrease of approximately 10 kg over a period of 3 months. 5 d before admission, the patient visited our outpatient department and underwent an enhanced abdominal computed tomography (CT) scan, which revealed a nodular lesion in the pancreatic head measuring approximately 2.1 cm 1.8 cm. The boundary between the common bile duct and the pancreatic lesion was unclear, and there was obvious dilation of the intrahepatic and extrahepatic bile ducts, with a width of approximately 1.7 cm at the widest point. There was local interruption of the pancreatic duct and significant dilation in the distal region of the pancreatic duct, with a width of approximately 2.5 cm at the widest point. The pancreatic parenchyma appeared atrophic (Figure 1). Liver function retesting revealed a TBil of 49.1 μmol/L, DBil of 35.9 μmol/L, and CA19-9, a tumor marker, of 230 U/mL. The patient’s pancreatic head lesion was most likely an IPMN, and local malignant lesions could not be ruled out.

Figure 1 Enhanced abdominal computed tomography scan of case 1. A nodular shadow (blue arrow) is visible in the pancreatic head region, with significant dilation of the intrahepatic and extrahepatic bile ducts. The local pancreatic duct is interrupted at the lesion site, and the distal pancreatic duct is significantly dilated. The pancreatic parenchyma shows atrophy. Red triangle: Main pancreatic duct; Yellow triangle: Common bile duct. A: Axial phase; B: Reconstruction of the biliary and pancreatic duct system.

Case 2: One month before admission, the patient experienced upper abdominal discomfort without any apparent cause. 10 d before admission, the patient developed jaundice of the skin and sclera, darkening of urine color, and lightening of stool color. Liver function tests revealed elevated bilirubin levels, with a TBil of 34.5 µmol/L. Magnetic resonance cholangiopancreatography revealed multiple cystic lesions in the pancreas, suggesting the possibility of IPMN and necessitating surgical treatment. The patient then visited our outpatient department, where tumor marker testing revealed a CA19-9 level of 76.1 U/mL. An abdominal enhanced CT scan revealed multiple cystic low-density lesions in the pancreatic head and body, with no significant contrast enhancement. The largest lesion had a diameter of approximately 27 mm × 24 mm. There was slight narrowing of the proximal end of the splenic vein. The pancreatic parenchyma appeared atrophic, and the main pancreatic duct showed diffuse and uneven dilation, with a width of approximately 11 mm at the widest point (Figure 2). The patient was admitted for surgical treatment.

Figure 2 Enhanced abdominal computed tomography scan of case 2. Multiple cystic low-density shadows are visible in the pancreatic head and body, with pancreatic parenchymal atrophy and dilation of the main pancreatic duct. Red triangle: Multiple cystic masses in the pancreatic head and body; Yellow arrow: Dilation of the main pancreatic duct. A: Axial phase; B: Reconstruction of the biliary and pancreatic duct system.

History of past illness

Case 1: The patient had a history of high fasting blood glucose levels for more than 4 years, with a fasting blood glucose of 7.5 mmol/L but no confirmed diagnosis of diabetes.

Case 2: The patient had been diagnosed with hypertension for several years and type 2 diabetes for 17 years, with poor blood sugar control despite insulin therapy.

Personal and family history

Case 1: He had a 30-year history of alcohol consumption, with a daily intake of 250 mL. The relevant family history included pancreatic tumors in his mother, but the specific details were unknown. There was no other significant medical history.

Case 2: The patient had a long history of heavy smoking and social drinking. His father passed away due to pancreatic cancer. There was no other significant medical history.

Physical examination

Case 1: Nothing special.

Case 2: Nothing special.

Laboratory examinations and imaging examinations

Case 1: The patient was admitted for surgical treatment. After admission, he underwent endoscopic ultrasound examination and fine-needle aspiration (EUS-FNA) of the pancreatic head nodule. Endoscopic ultrasound revealed a 22 mm 16 mm solid-cystic lesion in the pancreatic head, with dilation of the upstream bile duct measuring 1.9 cm and dilation of the pancreatic duct measuring approximately 1.7 cm. The wall of the duct showed a moderately echogenic nodule (Figure 3). Pathology of the EUS-FNA smear revealed epithelial cells with high-grade dysplasia, and some cells were suspicious for malignancy. Based on the patient's medical history, laboratory tests, imaging findings, and cytology diagnosis, our team considered the diagnosis of a pancreatic head mass with possible malignant transformation of IPMN.

Figure 3 Endoscopic ultrasound images of case 1. A: Significant dilation of the main pancreatic duct, approximately 1.7 cm; B: Isoechoic nodules in the ductal wall.

Case 2: The imaging and laboratory tests prior to admission have been described earlier. After admission, there were no other important imaging examination results.

FINAL DIAGNOSIS

Case 1

Postoperative pathology revealed an IPMN with high-grade dysplasia and evidence of infiltration (moderately differentiated adenocarcinoma). No lymph node metastases were observed (0/16).

Case 2

Postoperative pathology revealed a MCN of the pancreas with low-grade dysplasia. The surrounding pancreatic tissue showed features of chronic pancreatitis, with low-grade epithelial neoplasia (PanIN1) in the ducts. No lymph node metastases were observed (0/25).

TREATMENT

Case 1

Surgical treatment was performed using a laparoscopic approach. Due to the patient's extensive dilation of the main pancreatic duct and atrophy of the distal pancreatic parenchyma, a decision was made to perform a total pancreatectomy to ensure complete resection. The conventional procedure involved removal of the gallbladder; dissection of the distal stomach, proximal duodenum, and distal common bile duct; and a Kocher incision to mobilize the posterior aspect of the pancreatic head and the duodenum. The posterior artery-first approach was used to dissect the superior mesenteric artery branches, including the inferior pancreaticoduodenal artery. During the dissection of the distal pancreas, adhesions were observed between the pancreas and the splenic vessels, but separation was still feasible. An ultrasonic scalpel was used to carefully dissect the pancreatic body and tail from the splenic vessels, preserving the integrity of the vessels. Finally, the distal pancreas was flipped to the right side, and the portal vein-superior mesenteric vein (PV-SMV) was pulled to the left side before separating the PV-SMV branches from the uncinate process of the pancreas. After complete resection and removal of the specimen, cholangiojejunostomy and gastrojejunostomy were performed sequentially. Drainage tubes were placed at the cholangiojejunostomy and gastrojejunostomy sites and brought out through the abdominal wall. The total operative time was 250 min, with an intraoperative blood loss of 100 mL. The surgical diagram is shown in Figure 4, the intraoperative view is shown in Figure 5A, and the resected specimen is shown in Figure 5B.

Figure 4 Surgical schematic diagram for case 1. A: Before resection; B: After resection and reconstruction. SpA: Splenic artery; SpV: Splenic vein; PV: Portal vein; SMV: Superior mesenteric vein.

Figure 5 Tumor information for case 1. A: Intraoperative view after resection of the tumor in case 1; B: Gross specimen from case 1. CHA: Common hepatic artery; SpA: Splenic artery; SpV: Splenic vein; PV: Portal vein; SMV: Superior mesenteric vein; IMV: Inferior mesenteric vein.

Case 2

A complete laparoscopic SpTP was performed. The main surgical procedures were similar to those in patient 1. However, in this patient, there was significant adhesion between the splenic vein and the cystic lesion in the pancreatic body, leading to venous injury and hemorrhage during the separation process. The splenic vein was ligated, while the splenic artery was preserved. The total operative time was 200 min, with an intraoperative blood loss of 150 mL. The intraoperative view is shown in Figure 6A, and the image of the resected specimen is shown in Figure 6B. The patient achieved a smooth postoperative recovery, and the cholangiojejunostomy drainage tube was removed on the third day after surgery, followed by removal of the gastrojejunostomy drainage tube on the fifth day. The patient was discharged on the seventh day after surgery.

Figure 6 Tumor information for case 2. A: Intraoperative view after resection of the tumor in case 2; B: Gross specimen from case 2. CHA: Common hepatic artery; GDA: Gastroduodenal artery; SpA: Splenic artery; SpV: Splenic vein; PV: Portal vein; SMV: Superior mesenteric vein.

OUTCOME AND FOLLOW-UP

Case 1

Following surgery, the patient received chemotherapy with gemcitabine and S-1. At a follow-up visit 20 months after surgery, there was no evidence of tumor recurrence, and the patient tolerated insulin therapy and pancreatic enzyme supplementation well.

Case 2

At the 3-month follow-up after surgery, the patient presented good short-term recovery.

DISCUSSION

In the surgical treatment of benign or low-grade malignant tumors of the pancreas, such as IPMN and MCN, surgeons need to consider the curative effect of tumor resection, the preservation of organ function, and the long-term quality of life for patients due to the good prognosis and long survival period associated with these tumors. Multiple low-grade malignant tumor lesions in the head, neck, and body of the pancreas, as well as IPMN with full-length dilation of the main pancreatic duct, are indications for total pancreatectomy. Traditional total pancreatectomy often includes splenectomy (total pancreatectomy with splenectomy). However, as the spleen is an immune organ of the human body, removal of the spleen may increase the risk of postoperative infection, thromboembolic events and the development of certain malignancies[5-7]. Previous studies have shown that compared to laparoscopic distal pancreatectomy with splenectomy (LDPS), laparoscopic spleen-preserving distal pancreatectomy (LSpDP) may reduce the incidence of postoperative abdominal infection and abdominal abscess[8]. Moreover, for small benign pancreatic tumors, LSpDP is associated with a lower incidence of postoperative pancreatic fistula, less intraoperative blood loss, and a lower rate of conversion than LDPS[9]. An increasing number of pancreatic surgeons have started to perform SpTP, and there is even research supporting the selective use of SpTP in certain pancreatic cancer patients[3,4,10]. Common spleen-preserving techniques include preserving the splenic vessels (Kimura method) and dividing the splenic vessels (Warshaw method), with the Kimura method requiring greater technical requirements but having a lower incidence of postoperative complications such as splenic ischemia.

In recent years, with the popularization of the abovementioned concept and the continuous development of minimally invasive techniques such as laparoscopy and robotic assistance, LSpTP has gradually been reported in the literature. However, due to the technical challenges associated with this procedure, case reports are still the main source of evidence, and the number of cases is limited. In 2011, Kim et al[11] reported the first case of laparoscopic-assisted pylorus-preserving SpTP for the treatment of IPMN, with reconstruction of the digestive tract performed under open direct vision and spleen preservation using the Warshaw method[11]. Since then, several surgical teams have reported a number of cases of LSpTP for the treatment of low-grade malignant pancreatic tumors[12-16]. The spleen-preserving techniques used include the Kimura method and the Warshaw method. In addition to spleen preservation, LSpTP with preservation of the pylorus and duodenum has also been reported. A summary of the reported cases of LSpTP in the literature is shown in Table 1. Although the surgical approaches in these reports vary, overall, the surgical time, intraoperative blood loss, and perioperative complication rates are acceptable, supporting the safety and feasibility of LSpTP for low-grade malignant pancreatic tumors. Furthermore, robot-assisted minimally invasive surgical techniques have also undergone rapid development in recent years, and the safety and feasibility of robotic SpTP have been preliminarily validated in the literature[13,17].

Table 1 Summary of clinical data on reported laparoscopic spleen-preserving total pancreatectomy in the literature.

Year	Ref.	Gender	Age (yr)	Pathology	Surgical procedure	Spleen-preserving technique	Operating time (min)	Intraoperative blood loss (mL)	Morbidity
2011	Kim et al[11]	Female	72	IPMN	LPpSpTP	Warshaw	450	800	Marginal ulcer
2012	Choi et al[14]	Female	74	IPMN	LPpSpTP	Warshaw	450	800	Marginal ulcer
2012	Choi et al[14]	Male	69	IPMN	LPpSpTP	Warshaw	410	160
2012	Choi et al[14]	Female	77	IPMN	LPpSpTP	Warshaw	410	490
2017	Chapman et al[12]	Male	66	IPMN	LSpTP	Kimura	270	150
2017	Wang et al[13]	Female	68	IPMN	LPpSpTP	Kimura	450	300	DGE
2017	Wang et al[13]	Male	74	IPMN	LPpSpTP	Kimura	480	400	DGE, melena
2019	Wu et al[15]	Female	68	IPMN	LDpSpTP	Kimura	270	250
2022	Bartos et al[16]	NM	40	IPMN	LSpTP	Kimura	NM	NM
2024	Case 1	Male	51	IPMN	LSpTP	Kimura	250	100	-
2024	Case 2	Male	60	MCN	LSpTP	Kimura with SpV resection	200	150	-

IPMN: Intraductal papillary mucinous neoplasms; NM: Not mentioned; LPpSpTP: Laparoscopic pylorus-preserving spleen-preserving total pancreatectomy; DpSpTP: Laparoscopic duodenum-preserving spleen-preserving total pancreatectomy; DGE: Delayed gastric emptying.

In this study, we present two cases of LSpTP. Compared to previous reports in the literature, both of these cases involved shorter surgical times, less blood loss, and no serious perioperative complications. In Case 1, postoperative pathology revealed invasive carcinoma, but there was no tumor recurrence at a follow-up of 20 months. In Case 2, the splenic vein was severed during surgery while preserving the splenic artery, which poses a risk of regional portal hypertension and gastrointestinal bleeding in the future. At the time of submission, there were no related events at a follow-up of 3 months, but further long-term follow-up is still needed.

CONCLUSION

In conclusion, LSpTP is a feasible surgical option for patients with benign or low-grade malignant tumors of the pancreas requiring total pancreatectomy. It can also be selectively performed with caution in some patients with malignant pancreatic tumors.