Surgical treatments of cystic neoplasms of the pancreas: an Asian university hospital experience

A retrospective study was performed of patients who had cystic neoplasms of the pancreas and underwent surgical removal by the first author at King Chulalongkorn Memorial Hospital, Bangkok, Thailand. The study period was from June 2000 to April 2013. Approval of the study was granted by the Institutional Review Board of the Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand. The research committee (IRB) provided an exemption for written patient’s approval for publication of their data in this retrospective study. All patients had provided informed consent for their surgery on admission.

During the study period, diagnosis of cystic neoplasms of the pancreas were made from CT and/ or MR imaging. In asymptomatic patients, diagnoses were made after routine medical check-up with abnormal findings on the pancreas on abdominal ultrasonography and subsequently confirmed by CT and/or MR imaging. Indications for surgical removal of the cystic neoplasms of the pancreas were 1. symptomatic cysts, and 2. suspicion of malignancy or premalignancy. The operations were conducted on an elective basis. Lesions at the pancreatic head underwent pancreaticoduodenectomy with or without preservation of the pylorus. Lesions at the pancreatic body and tail were removed by distal pancreatectomy with or without splenectomy. No patient underwent preoperative or intraoperative needle aspiration cytology, needle biopsy, or incisional biopsy. During the operations; after the surgical specimens were removed, a frozen section of the resected margin was performed when negative margin for malignancy was doubtful. When a frozen section revealed a cancer positive result, further resection of the pancreas was performed. In one patient, a positive result for malignancy from a frozen section of the transected pancreatic body after pancreaticoduodenectomy led to completion of the operation by total pancreatectomy. The final pathological reports for this patient revealed IPMN of the entire main pancreatic duct.

Postoperatively, pathological reports of all patients were examined and analyzed. Postoperative complications were searched and treated individually. On or after postoperative day 3, the drainage fluid from the abdominal drain was routinely sent for measurement of the amylase level simultaneously with measurement of the serum amylase activities. Diagnosis of pancreatic fistula was made when fluid from the abdominal drain contained amylase more than 3 times the serum amylase level [17]. Postoperative mortality was defined as death within one month of the operation. After the patients were discharged, follow-up was regularly done until April 2013 or until the patients died. Interval CT was performed every 3–6 months in patients who had malignant cystic neoplasms to detect recurrence. CT was performed at variable periods depending on risk of recurrence in patients who had premalignant cystic neoplasms. The management of such recurrent malignant cystic neoplasms was also described.

During a 13-year-period, 16 patients entered into the study. Thirteen were women, and 3 were men. Their age ranged from 34 to 92 years (median 59.5, mean 57.3 ± 17.6). Two patients were asymptomatic and diagnoses were made from routine medical checkup and subsequent imaging study. Fourteen had symptoms leading to diagnostic evaluation and imaging study. Five patients presented with symptom of abdominal discomfort due to pressure effect of large abdominal mass. Four presented with abdominal pain. The remaining 5 symptomatic patients presented with the findings shown in Table 1. Duration of symptoms ranged from 2 days to 6 years before cystic neoplasms of the pancreas were diagnosed and resected. All patients underwent pancreatic resection on elective basis. The operative procedures were as shown in Table 2. The operative time ranged from 150 to 450 minutes (median 300, mean 293 ± 98). The operative blood transfusion ranged from 0 to 5 units (median 1.5, mean 1.56 ± 1.59).

Table 1

Symptoms of patients presented with cystic neoplasms of the pancreas

Table 2

Operative procedures for resection of cystic neoplasms of the pancreas

The size of the cystic neoplasms measuring at the greatest dimension from the surgical specimens after pancreatic resections ranged from 2.2 to 17.5 cm (median 10, mean 9.2 ± 4.6). Two patients had small neoplastic cysts, 2.2 and 2.5 cm; one was asymptomatic, and one presented with epigastric pain for 6 years. The final pathological reports of both patients were IPMN of the pancreatic duct; one with severe dysplasia, one with carcinoma change. Definite diagnosis of the resected cystic neoplasms were as presented in Table 3.

Table 3

Definite pathological diagnoses of cystic neoplasms of the pancreas

Postoperative complications occurred in 3 patients; one had congestive heart failure, one had grade A pancreatic fistula, and one, who underwent total pancreatectomy, had diabetes mellitus. All had uneventful recovery after conservative treatment and appropriate medications. There was no postoperative mortality. The hospital stays ranged from 7 to 54 days (median 13, mean 17.9 ± 12.1). The follow-up time ranged from 1 to 155 months (median 69, mean 63.8 ± 54.8). Two patients died at 3.5 and 11 months postoperatively; one had poorly differentiated adenocarcinoma of the pancreas, the other had cystadenocarcinoma of the pancreas. Thirteen patients were alive and well without evidence of pancreatic malignancy at the time of preparing this manuscript. One patient who had IMPM with focal carcinoma change (the neoplastic cyst size 2.5 cm) had recurrence of the pancreatic remnant, 5 years after distal pancreatectomy and splenectomy. She underwent chemotherapy and radiotherapy and was well at last follow-up, 72 months after pancreatic resection.

Examination of this small case series taught us useful information regarding cystic neoplasms of the pancreas. First, the prognosis of frank malignancy is poor even after an intentionally curative resection. Second, resection of premalignant or malignant cystic tumors may reduce the chance of tumor transformation into invasive cancer and enhance survival. Third, pancreatic resection may be performed safely by experienced surgical teams. The first author has performed more than 100 pancreaticoduodenectomies during his surgical career with 2% mortality and 44% morbidity rates [18]. Familiarity contributed greatly to rational decision making when unexpected findings were encountered. Traditionally, surgery is recommended in symptomatic cysts, large cysts, and suspected premalignant or malignant cystic neoplasms [6, 19-22]. However, when a decision has to be made for whether operation should be performed or not in high risk patients e.g. very old age or patients with serious comorbidity, the likelihood of malignancy and the surgeons’ experience should be factors included into the decision. Pancreatic resection is a major operation, which may result in serious postoperative complications, even in centers with experienced surgeons and in high-volume surgical centers [13]. Of the 16 patients in our case series, 14 had definite indications for surgery by criteria of symptoms, size, and imaging appearance of the cystic neoplasms suggestive of premalignancy or malignancy. The remaining two patients had small cysts measuring 2.2 and 2.5 cm in diameter when first diagnosed with cystic neoplasms of the pancreas. The first patient, a woman aged 48 years, had a 2.2 cm cyst at the uncinate process of the pancreas with mild symptoms of epigastric discomfort. She was followed for 6 years until there were definite changes of the pancreatic lesion on her most recent CT with thickening of the cyst wall and demonstration of new intracystic nodules. Pylorus preserving pancreaticoduodenectomy was performed and the pathological reports revealed IPMN with moderate to severe dysplasia. She was well when this manuscript was prepared, 17 months after surgery. A second patient, a woman aged 69 years, had a 2.5 cm asymptomatic cyst on the body of her pancreas. Although the indication for surgery was not reached by size (<3 cm), surgery was performed without delay because of ERCP diagnosis of dilated pancreatic duct with intraductal filling defects [23]. She underwent distal pancreatectomy with splenectomy. The pathological reports were IPMN with focal carcinoma changes. She had recurrent carcinoma at the pancreatic remnant 5 years later and underwent chemotherapy and radiotherapy. She was alive and well at the time of preparing this manuscript, 72 months after pancreatic resection.

Regarding surgical techniques for pancreatic resection, we had acceptable results with low postoperative complications and no perioperative mortality. We had demonstrated in our previous reports of pancreaticoduodenectomy, that meticulous surgical techniques were important when performing these complex surgical procedures. Furthermore, external drainage of the pancreatic remnant, with an external pancreatic stent, may help lessen the occurrence of a postoperative pancreatic fistula [18, 24, 25]. When performing a distal pancreatectomy, the main pancreatic duct at the pancreatic stump must be identified and ligated to prevent a postoperative pancreatic fistula. The authors routinely used double suture-ligations of the main pancreatic duct with nonabsorbable suture number 4-0. Of the 8 patients who underwent distal pancreatectomy, 6 also had splenectomy and 2 had not. The advantages of keeping the spleen intact were preserving its immunological functions and avoidance of creating a raw surface and potential space after splenectomy, which might be associated with postoperative fluid collection or infection [26]. However, splenic preserving distal pancreatectomy should be conducted only when technically feasible and the oncologic margins are not compromised.

Efforts to obtain a definite preoperative diagnosis of cystic neoplasms of the pancreas included imaging appearance by EUS, CT, and MRI; cystic fluid cytology and measurement of CEA, CA19-9 levels; and of measurement of serum biomarkers, e.g. CEA, CA19-9 [3, 8, 27]. However, definite preoperative diagnosis was still inconclusive in a large number of asymptomatic cysts incidentally found during abdominal imaging. The medical and surgical teams discuss the cases and come to a decision of whether to resect or to observe. This creates a continuing dilemma [28]. Current evidence-based reviews support safe observation for asymptomatic cysts <2 cm with no demonstrable intracystic nodule on CT or MRI [27, 29]. Resection is recommended when changes or progression in size, symptoms, serum tumor markers, imaging appearance, and cystic fluid analysis are found during observation [27, 29, 30].

In conclusion, surgical treatment of cystic neoplasms of the pancreas has been presented. Definite indications for surgery were obtained in symptomatic cysts, large cysts, or strong imaging appearances suggesting malignancy (n = 14). In two asymptomatic small cysts, resections were performed and revealed premalignant and malignant pathology. We concluded also that pancreatic resection should be performed for symptomatic and/or large cystic neoplasms. Imaging appearance suggestive of premalignancy or malignancy is a definite indication for surgery. A small asymptomatic cyst may be safely observed and followed-up. Any changes or progression of the cyst during the observation should result in resection. Meticulous surgical techniques are important during pancreatic resections for these cystic neoplasms in order to lessen postoperative complications.