Laparoscopic Distal Pancreatectomy Using the Modified Prolonged Prefiring Compression Technique Reduces Pancreatic Fistula

Abstract

Background:

Pancreatic fistula (PF) is a common postoperative complication following distal pancreatectomy. The prolonged prefiring compression (PFC) technique to reduce PF has been described by Nakamura and colleagues in Japan. The present study assessed if this technique can be applied to the United Kingdom patient population in a tertiary referral center and replicate the low incidence of PF after the laparoscopic approach to distal pancreatectomy (Lap-DP).

Materials and Methods:

This is a retrospective study of all patients who underwent Lap-DP using the modified PFC technique by the senior author between June 2011 and July 2014. The modified PFC technique involved compression of the pancreatic parenchyma with an endo-stapler for a 3-minute period prior to firing and further 1-minute compression after firing prior to removal of the stapler, which is a small variant to the original technique of maintaining a 2-minute compression post firing.

Results:

Twenty patients (15 females; median age, 66 [range, 25–77] years) underwent Lap-DP using the PFC technique during the study period. Six patients had splenic-preserving Lap-DP. Median operating time was 240 minutes (range, 150–420 minutes) with a median length of hospital stay of 6 days (range, 3–22 days). Six patients (30%) developed Type A (biochemically noted as high drain fluid amylase) PF, and none of the patients had Type B/C PF. In the splenic preservation group, 1 patient had complete splenic infarction requiring laparoscopic splenectomy on Day 3, and 1 patient had partial infarction requiring prolonged hospital stay for pain relief. One patient required prolonged respiratory support due to severe preexisting lung disease. Overall mortality was zero.

Conclusions:

Our data confirm that the PFC technique is safe, feasible, and effective in reducing clinically significant PF post-Lap-DP in the United Kingdom patient population.

Introduction

The laparoscopic approach to distal pancreatectomy (Lap-DP) is being increasingly used and is likely to become the gold standard technique. It is a technically challenging procedure, with the most common complication reported being pancreatic fistula (PF).^1–4 Among the various techniques and methods that have been described to reduce PF, in 2011 Nakamura et al.⁵ described a prolonged prefiring compression (PFC) technique, which showed a reduction in PF rates. We adopted a modified version of this technique for our patients undergoing Lap-DP in an unselected group of patients from the United Kingdom population. We aimed to confirm the advantage of this technique in preventing postoperative PF.

Materials and Methods

All patients undergoing Lap-DP performed in our tertiary center were entered into a prospective database. The senior author introduced this technique in 2011, and it was the only technique used during the study period. Data recorded included patient demographics, clinical presentation, investigations, tumor staging, operative details, Day 3 drain fluid amylase, complications, length of stay, postoperative histology, and follow-up details. In all patients Lap-DP was performed using the modified PFC technique for parenchymal transection.

Data were analyzed retrospectively for median duration of surgery, overall morbidity, PF rate, re-operation rate, length of stay, and 90-day mortality.

Definition of PF

In our institution, we used the definition outlined by the International Study Group for Pancreatic Fistula (Table 1). According to this group, PFs are graded as A, B, or C. Grade A fistula is defined as the presence of >300 IU/L of amylase or three times the normal serum value of amylase in the drain fluid resulting in delay in drain removal (>6 and <21 days). Patients with Grade A PF do not require any radiological or surgical intervention and are discharged in less than 3 weeks. Patients with Grade B fistula require surgically placed drains for >22 days, radiological intervention for intraabdominal collection/abscess, or re-admission for fistula. Grade C patients require either total parental nutrition or re-operation for fistula.

Table 1.

Grading System Used by the International Study Group for Pancreatic Fistula

Grade of leak	Duration	Clinical impact	Investigation findings and clinical management	Clinical condition
A	“Transient fistula”	No clinical impact	No peripancreatic collections on CT scan; little/no change in management	Clinically well; no sepsis; no prolongation of hospital stay; slow removal of operatively placed drains
B		Clinical impact	Peripancreatic drains in place or repositioned to drain collections; change in management required	Clinically fairly well; degree of infection requiring specific treatment; prolongation of hospital stay; patients often discharged with drains in situ and observed in outpatient setting
C		Severe clinical impact	Worrisome peripancreatic collections that require percutaneous drains; major change in management usually in ICU setting; possible resurgery to salvage a difficult situation (completion pancreatectomy, etc.)	Clinically unwell; associated sepsis requiring aggressive antibiotics, octreotide, and other intensive care support; major prolongation of hospital stay; associated complications and possibility of mortality

CT, computed tomography; ICU, intensive care unit.

Surgical technique

An Echelon™ 75 ENDOPATH stapler (Ethicon Endo-Surgery, Cincinnati, OH) with the green cartridge was used for the pancreatic parenchymal transection where the consistency of the pancreas was noted to be firm as a subjective measure by the operating surgeon, and in cases where it was noted as soft/normal, a white (vascular) cartridge was used. The pancreas was initially compressed with the stapler for a 3-minute period prior to firing. After firing, compression was maintained for a further 1 minute prior to removal of the stapler. This is a slight modification to the technique described by Nakamura et al.,⁵ who described a 2-minute period of maintaining compression postfiring. All patients had a 20 French Robinson's latex drain inserted close to the transected edge of the pancreas at the end of the procedure.

In patients in whom splenic conservation was attempted, this was done either by direct inspection and conservation of the splenic vessels or with the use of the Warshaw technique,⁶ when conservation of splenic vessels was not technically possible, by the preservation of the short gastric vessels to maintain splenic vascularity.

Results

In total, 20 patients were identified for the study period of June 2011–July 2014 (5 males and 15 females) with a median age of 66 (range, 25–77) years. The patient demographics are summarized in Table 2. In the majority of patients, the pancreatic lesion was detected following investigation for nonspecific abdominal complaints (n = 9, 45%). Seven patients (35%) presented with abdominal pain. The other presentations included hypoglycemia (n = 2, 10%), dyspepsia (n = 1, 5%) and recurrent pancreatitis (n = 1, 5%) (Table 2).

Table 2.

Patient Characteristics, Operative Findings, and Peri- and Postoperative Outcomes

Age (years)	Gender	Presentation	ASA score	Other procedure in addition to Lap-DP	Pancreas consistency	Transection line in relationship to SMV	Grade of leak	Other complications	Length of hospital stay (days)	Tumor histology
55	F	Dyspepsia	2	Splenectomy	Normal	Left of SMV			7	Neuroendocrine tumor
65	F	Abdominal pain	2	Spleen preserved	Normal	Left of SMV		Splenic infarction requiring splenectomy	10	Intraductal papillary mucinous neoplasm
63	F	Incidental	2	Splenectomy	Normal	Left of SMV			5	Serous cystadenoma
60	M	Incidental	2	Splenectomy	Normal	Left of SMV	Grade A		6	Intraductal papillary mucinous neoplasm
53	M	Recurrent pancreatitis	2	Splenectomy	Firm	Left of SMV			6	Intraductal papillary mucinous neoplasm
66	F	Hypoglycemia	2	Spleen preserved	Normal	Left of SMV			6	Neuroendocrine tumor
77	M	Incidental	2	Splenectomy	Firm	Left of SMV	Grade A		6	Pseudocyst
67	F	Abdominal pain	2	Splenectomy	Firm	Left of SMV	Grade A	Respiratory failure due to COPD requiring prolonged ventilation in the ITU	22	Pancreatitis
71	F	Incidental	2	Spleen preserved	Firm	On SMV			4	Serous cystadenoma
66	F	Incidental	2	Spleen preserved	Firm	Left of SMV			6	Serous cystadenoma
78	M	Abdominal pain	3	Splenectomy and cholecystectomy	Normal	Left of SMV			8	Neuroendocrine tumor
56	F	Incidental	2	Splenectomy	Firm	On SMV			4	Serous cystadenoma
25	F	Incidental	1	Spleen preserved	Normal	Left of SMV	Grade A	Re-admission with pain	5	Mucinous cystic neoplasm
50	M	Abdominal pain	2	Splenectomy and hemicolectomy (pancreatic lesion adherent to splenic flexure)	Firm	Left of SMV			5	Pseudocyst
72	F	Incidental	2	Spleen preserved (Warshaw technique) + cholecystectomy	Normal	Left of SMV		Partial splenic infarction (managed conservatively)	12	Mucinous cystic neoplasm
71	F	Incidental	3	Splenectomy	Normal	Left of SMV	Grade A		6	Neuroendocrine tumor
72	F	Abdominal pain	3	Splenectomy	Normal	Left of SMV			7	Ductal adenosquamous
75	F	Hypoglycemia	3	Cuff of stomach removed	Soft	Left of SMV			3	Neuroendocrine tumor
69	F	Abdominal pain	3	Splenectomy	Soft	On SMV			6	Intraductal papillary mucinous neoplasm
71	M	Abdominal pain	3	Spleen preserved	Normal	Left of SMV	Grade A		9	Intraductal papillary mucinous neoplasm

ASA, American Society of Anesthesiologists; COPD, chronic obstructive pulmonary disease; F, female; ITU, intensive therapy unit; Lap-DP, laparoscopic distal pancreatectomy; M, male; SMV, superior mesenteric vein.

Staging by contrast-enhanced multidetector computed tomography scan was performed in all patients, with further investigation by endoscopic ultrasound in 10 patients (50%), of whom 6 patients underwent preoperative endoscopic ultrasound–guided biopsy. Pancreatic duct dilatation was identified in 4 patients (20%). Enhanced preoperative health assessment was carried out in 5 patients (25%) in the form of cardiopulmonary exercise testing, and a median American Society of Anesthesiologists score of 2 was recorded (range, 1–3). All except 1 patient were admitted on the day of the surgery.

The median operating time was 240 minutes (range, 150–420 minutes). All patients were completed laparoscopically with no conversion to open surgery. The pancreas consistency was noted to be “normal” in 13 patients (65%) and “firm” in 7 patients (35%). There were no patients in whom the pancreas was too hard in consistency that led to failure of the ability to use the stapler, as reported in the literature.⁵ The pancreas was divided to the left of the confluence of the splenic vein with the superior mesenteric vein in 17 patients (85%) and in 3 patients (15%) in line with the superior mesenteric vein and portal vein.

Six patients (30%) underwent Lap-DP with spleen preservation. Two patients in the splenic preservation group had splenic infarction: 1 had complete infarction requiring laparoscopic splenectomy on Day 3, and 1 had partial splenic infarction and was managed conservatively. Further morbidity arose from a patient with a background of severe underlying lung disease who required prolonged respiratory support in the intensive care for 18 days and was finally discharged on postoperative Day 22.

Drain fluid amylase was assessed in 7 (35%) patients. It was not possible to check drain fluid amylase in the remaining 13 (65%) of patients as there was no fluid in the drain, or the small amount of fluid was blood stained and hence not able to be processed by the laboratory. Six patients (30%) developed a Grade A (biochemically noted as high drain fluid amylase) leak, with no Grade B or Grade C PF noted in this study. In the absence of a confirmed leak the drains were removed on postoperative Day 3. The leaks were reported in 3 patients in whom the consistency of the pancreas was noted to be “normal” and in the other 3 in whom it was noted to be “firm.”

The median postoperative hospital stay was 6 days (range, 3–22 days). The details of final histology included intraductal papillary mucinous neoplasm (n = 5), mucinous cystic neoplasm (n = 2), neuroendocrine tumors (n = 5), serous cyst adenoma (n = 4), pseudocyst (n = 2), ductal adenosquamous carcinoma (n = 1), and pancreatitis (n = 1). All patients were reviewed in the outpatient clinic at 4–6 weeks from discharge. Further follow-up at 6-month intervals was given to patients with a malignant histology. The median follow-up for these patients was 3 years (range, 1–4 years), with no patients noted to require re-admission for complications.

Discussion

Lap-DP was first described in 1994 by Cuschieri,⁷ with the additional method of splenic conservation described by Gagner et al.⁸ in 1996. It currently accounts for more than 70% of laparoscopic pancreatic resections.⁹ A meta-analysis by Nakamura and Nakashima¹⁰ has shown that Lap-DP is a safe and a reliable technique in comparison with the established open approach, with advantages of reduction in postoperative pain, postoperative length of stay, and wound-related complications.^4,5,11–14

The most common complication after distal pancreatectomy is PF. Prior to June 2005 there was no uniform definition of PF. The International Study Group for Pancreatic Fistula published the definition of PF and graded PF based on severity into Grades A–C. PF is defined as existence of any fluid output after postoperative Day 3 with amylase content greater than three times the upper normal serum value.¹⁵ The overall fistula rates in the literature for the open and laparoscopic techniques range from 3.5% to 29%^4,16–21 and from 0% to 27%,¹ respectively. Multiple surgical techniques have been described for parenchymal transection to reduce the frequency of PF. Meta-analysis comparing staple versus suture closure demonstrated no difference in the leak rate.¹⁷ Several other approaches, including the use of fibrin glue, sealants, electrocautery, and sutures, have all been tested^4,20,21 with mixed results. Reinforcing of the staple line with sutures and the use of electrothermal bipolar vessels sealers have also been reported to help reduce pancreatic leak.^4,22 Bioabsorbable staple line reinforcement, such as SEAMGUARD^® [W.L. Gore & Associates (UK) Ltd., Livingston, Scotland, United Kingdom], has also been reported in the literature, with some authors showing a reduction in the PF rates,²³ whereas others showed an increase in PF rates.²⁴ It may prove to be an added advantage to use the PFC technique in units where the bioabsorbable staple line reinforcement is proving to be successful, to further reduce fistula rates.

In a large retrospective study of 462 patients who underwent open distal pancreatectomies, Ferrone et al.²¹ reported an overall PF rate of 29%. Just over half of patients with PF had Grade B, and 4% had Grade C PF. They did not find any difference in the grade of fistula rate among various techniques, which included covering of the pancreatic transection line with a falciform patch, fibrin glue, an omental patch, and division of the pancreas with an endovascular stapler. In our series, we observed an overall PF rate of 30%, and all patients had Grade A PF. This is in contrast to most of the published literature, where over half of reported PFs were Grade B and C. Risk factors for PF include a body mass index of >30 kg/m², male gender, pancreas texture, and additional organ resection. The thickness of the pancreas has been reported as a risk factor for an increased leak rate, with recommendation to reserve the stapler technique for a thin pancreas.^18,19

In our case series there were no leaks noted in the pancreas that were reported as “normal” in consistency; this may be related directly to the thickness or related to the use of the Echelon 75 ENDOPATH stapler with the vascular white cartridge. Due to the small number of cases we did not evaluate the role of various risk factors that were implicated in causation of PF. Previous studies by Sepesi et al.²⁵ have suggested that the use of the vascular cartridge (2.5 mm) would lead to a reduction in the PF rates in their population of patients.

In the original PFC article by Nakamura et al.⁵ 42 patients successfully underwent Lap-DP with one conversion in their series due to the texture of pancreas being too hard to be amenable for stapler transection. The cases were divided into the no-PFC versus the PFC group, with 25 cases and 17 cases in each group, respectively. The two groups showed no significant differences in terms of age, gender, diabetes mellitus, prior abdominal surgery, or spleen conservation. Their results showed no PF in the PFC group in comparison with 28% in the non-PFC group, which was a significant difference (P < .05). In addition, they showed no significant differences when comparing the incidence of PF in relation to texture and transection position, which is also supported in our case series. The hypothesis for the leak is thought to occur from the transection end of the pancreatic ductules rather than simply from the main duct, as suggested by Yamaguchi et al.²⁶ and Sugiyama et al.²⁷ Hence the mechanical stapling technique, which is able to seal the pancreatic ductules, is seen as more advantageous. However, the stapling technique without the PFC technique by Nakamura et al.⁵ showed a similar rate of PF to previously reported rates in open distal pancreatectomy. The added advantage of the PFC technique is thought to be due to the ability to be able to achieve maximal flattening and hence better compression of the ductules prior to stapling; this minimizes the pancreatic parenchymal trauma and a better sealed staple line.

The limitations of our study are related to retrospective analysis of data even though the data were collected prospectively, which is further compounded by the small case numbers in this series. The use of the green versus the white cartridge for the stapler depending on the pancreatic consistency is an added variable that may influence the leak rate.

In conclusion, Lap-DP can be performed safely in a tertiary hepatopancreatic-biliary center. The use of the PFC technique is associated with a low risk of PF post-Lap-DP. This is the first study to confirm this finding in an unselected patient group from the United Kingdom population. The study highlights the need for a randomized controlled trial to compare the various pancreatic transection techniques and also the type of staplers used.

Footnotes

Disclosure Statement

No competing financial interests exist.

A.V.A. and S.A. collected the data and drafted, reviewed, and modified the manuscript.

References

Nakamura

, Uchida

, Aimoto

, Matsumoto

, Yoshida

, Tajiri

. Clinical outcome of laparoscopic distal pancreatectomy. J Hepatobiliary Pancreat Surg, 2009; 16:35–41.

Kuroki

, Tajima

, Kanematsu

. Surgical management for the prevention of pancreatic fistula following distal pancreatectomy. J Hepatobiliary Pancreat Surg, 2005; 12:283–285.

Mabrut

, Fernandez-Cruz

, Azagra

, Bassi

, Delvaux

, Weerts

, Fabre

, Boulez

, Baulieux

, Peix

, Gigot

. Laparoscopic pancreatic resection: Results of a multicenter European study of 127 patients. Surgery, 2005; 137:597–605.

Iacobone

, Citton

, Nitti

. Laparoscopic distal pancreatectomy: Up-to-date and literature review. World J Gastroenterol, 2012; 18:5329–5337.

Nakamura

, Ueda

, Kohno

, Aly

, Takahata

, Shimizu

, Tanaka

. Prolonged peri-firing compression with a linear stapler prevents pancreatic fistula in laparoscopic distal pancreatectomy. Surg Endosc, 2011; 25:867–871.

Warshaw

. Conservation of the spleen with distal pancreatectomy. Arch Surg, 1988; 123:550–553.

Cuschieri

. Laparoscopic surgery of the pancreas. J R Coll Surg Edinb, 1994; 39:178–184.

Gagner

, Pomp

, Herrera

. Early experience with laparoscopic resections of islet cell tumors. Surgery, 1996; 120:1051–1054.

Addeo

, Giulianotti

. Update on laparoscopic pancreatectomy in 2010. Minerva Chir, 2010; 65:655–666.

10.

Nakamura

, Nakashima

. Laparoscopic distal pancreatectomy and pancreatoduodenectomy: Is it worthwhile? A meta-analysis of laparoscopic pancreatectomy. J Hepatobiliary Pancreat Sci, 2013; 20:421–428.

11.

Mehta

, Doumane

, Mura

, Nocca

, Fabre

. Laparoscopic versus open distal pancreatectomy: A single-institution case-control study. Surg Endosc, 2012; 26:402–407.

12.

Venkat

, Edil

, Schulick

, Lidor

, Makary

, Wolfgang

. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: A systematic review and meta-analysis. Ann Surg, 2012; 255:1048–1059.

13.

Jin

, Altaf

, Xiong

, Huang

, Javed

, Mai

, Liu

, Hu

, Xia

. A systematic review and meta-analysis of studies comparing laparoscopic and open distal pancreatectomy. HPB (Oxford), 2012; 14:711–724.

14.

Stauffer

, Rosales-Velderrain

, Goldberg

, Bowers

, Asbun

. Comparison of open with laparoscopic distal pancreatectomy: A single institution's transition over a 7-year period. HPB (Oxford), 2013; 15:149–155.

15.

Bassi

, Dervenis

, Butturini

, Fingerhut

, Yeo

, Izbicki

, Neoptolemos

, Sarr

, Traverso

, Buchler

. Postoperative pancreatic fistula: An international study group (ISGPF) definition. Surgery, 2005; 138:8–13.

16.

Mabrut

, Fernandez-Cruz

, Azagra

, Bassi

, Delvaux

, Weerts

, Fabre

, Boulez

, Baulieux

, Peix

, Gigot

. Laparoscopic pancreatic resection: Results of a multicenter European study of 127 patients. Surgery, 2005; 137:597–605.

17.

Zhou

, Lv

, Wang

, Mou

, Cai

, Herr

. Stapler vs suture closure of pancreatic remnant after distal pancreatectomy: A meta-analysis. Am J Surg, 2010; 200:529–536.

18.

Eguchi

, Nagano

, Tanemura

, Takeda

, Marubashi

, Kobayashi

, Wada

, Umeshita

, Mori

, Doki

. A thick pancreas is a risk factor for pancreatic fistula after a distal pancreatectomy: Selection of the closure technique according to the thickness. Dig Surg, 2011; 28:50–56.

19.

Tan-Tam

, Chung

. Minireview on laparoscopic hepatobiliary and pancreatic surgery. World J Gastrointest Endosc, 2014; 6:60–67.

20.

Harris

, Abdollahi

, Newhook

, Sauter

, Crawford

, Chojnacki

, Rosato

, Kennedy

, Yeo

, Berger

. Optimal technical management of stump closure following distal pancreatectomy: A retrospective review of 215 cases. J Gastrointest Surg, 2010; 14:998–1005.

21.

Ferrone

, Warshaw

, Rattner

, Berger

, Zheng

, Rawal

, Rodriguez

, Thayer

, Fernandez-del Castillo

. Pancreatic fistula rates after 462 distal pancreatectomies: Staplers do not decrease fistula rates. J Gastrointest Surg, 2008; 12:1691–1697; discussion 1697–1698.

22.

Sartori

, Baiocchi

. Transecting the pancreas neck with electrothermal bipolar vessel sealer (LigaSure) in laparoscopic left pancreatectomy: Case report. Surg Laparosc Endosc Percutan Tech, 2009; 19:e175–e176.

23.

Yamamoto

, Hayashi

, Nguyen

, McCloud

, Imagawa

. Use of Seamguard to prevent pancreatic leak following distal pancreatectomy. Arch Surg, 2009; 144:894–899.

24.

Guzman

, Nelson

, Kim

, Pigazzi

, Trisal

, Paz

, Di Ellenhorn

. Increased incidence of pancreatic fistulas after the introduction of a bioabsorbable staple line reinforcement in distal pancreatic resections. Am Surg, 2009; 75:954–957.

25.

Sepesi

, Moalem

, Galka

, Salzman

, Schoeniger

. The influence of staple size on fistula formation following distal pancreatectomy. J Gastrointest Surg, 2012; 16:267–274.

26.

Yamaguchi

, Chijiwa

, Shimizu

, Yokohata

, Tanaka

. Litmus paper helps detect potential pancreatoenterostomy leakage. Am J Surg, 1998; 175:227–228.

27.

Sugiyama

, Abe

, Izumisato

, Tokuhara

, Masaki

, Mori

, Atomi

. Pancreatic transection using ultrasonic dissector in pancreatoduodenectomy. Am J Surg, 2001; 182:257–259.