Pancreaticogastrostomy following distal pancreatectomy prevents ...

J Hepatobiliary Pancreat Sci (2014) 21:473–478 DOI: 10.1002/jhbp.59

ORIGINAL ARTICLE

Pancreaticogastrostomy following distal pancreatectomy prevents pancreatic fistula-related complications Hiroaki Yanagimoto · Sohei Satoi · Hideyoshi Toyokawa · Tomohisa Yamamoto · Satoshi Hirooka · Jun Yamao · So Yamaki · Hironori Ryota · Yoichi Matsui · A-Hon Kwon

Published online: 15 December 2013 © 2013 Japanese Society of Hepato-Biliary-Pancreatic Surgery

Abstract Background The most common postoperative complication after distal pancreatectomy (DP) is still postoperative pancreatic fistula (POPF), which is closely associated with other major complications and remains an unsolved problem. Methods This retrospective study included 47 consecutive patients who underwent a distal pancreatectomy with (DP-PG group, n = 21) or without (DP group, n = 26) duct-to-mucosa pancreaticogastrostomy from June 2010 to May 2012. Clinical data including POPF-related complications (POPF, fluid collection, intra-abdominal abscess, bleeding and delayed gastric emptying) as a primary endpoint were compared between the two groups. Results The frequencies of POPF-related complications as well as overall POPF and complications in the DP-PG group were lower than in the DP group (P = 0.037, P < 0.001, respectively). The 30 days morbidity after hospital discharge in the DP-PG group was less than in the DP group (P = 0.014). In both groups median hospital stay was similar. Although additional time needed for pancreaticogastrostomy was 35 (20–55) min, there was no difference in operative times. Patients in the DP group had a higher medical cost for hospitalization than the DP-PG group (P = 0.048). Conclusion Pancreaticogastrostomy as an additional procedure following distal pancreatectomy was associated with a reduced rate of POPF-related complications that resulted in relatively lower medical cost for hospitalization. H. Yanagimoto · S. Satoi (*) · H. Toyokawa · T. Yamamoto · S. Hirooka · J. Yamao · S. Yamaki · H. Ryota · Y. Matsui · A-H. Kwon Department of Surgery, Kansai Medical University, 2-5-1 Shin-machi, Hirakata, Osaka 573-1010, Japan e-mail: [email protected]

Keywords Distal pancreatectomy · Medical cost · Pancreatic fistula-related complication · Pancreaticogastrostomy

Introduction Distal pancreatectomy (DP) is a standard procedure for benign and malignant lesions in the body or tail of the Pancreas. With recent advances in surgical techniques and perioperative management, the mortality rate after distal pancreatectomy has decreased and is now less than 2% in high volume centers [1–3]. However, the morbidity rate remains as high as 10% to 47% [4–6]. Postoperative pancreatic fistula (POPF) is still the most common (up to 60.9%, mostly 10%–26%) [1, 3–9] and sometimes clinically relevant complication, resulting in development of further complications (intra-abdominal abscess, delayed gastric emptying (DGE), post-pancreatectomy hemorrhage (PPH), intra-abdominal fluid collection, and sepsis). Various surgical techniques have been used for the management of the pancreatic stump such as the use of a scalpel and ligation of the pancreatic duct [10] or bipolar scissors [11], staple closure [12], ultrasonic dissector [13], ultrasonically activated scalpel [14], radio-frequency [15], fibrin glue sealing [16], or serosal patches [17]. However, clinically significant pancreatic fistula remains and varies between 10 to 25%. Theoretically, the increased pressure of the pancreatic duct after distal pancreatectomy in patients with preserved sphincter can be one of the contributing factors to development of POPF. Therefore, draining the pancreatic juice from the main pancreatic duct on the surgical stump into the stomach was considered as a procedure that would decrease the rate of POPF-related complications after distal pancreatectomy.

474 Fig. 1 Duct-to-mucosa pancreaticogastrostomy after distal pancreatectomy (a) indicates general view of pancreaticogastrostomy. (b) indicates a sectioned drawing of pancreaticogastrostomy. The outer sutures are placed between the pancreatic parenchyma and the gastric seromuscular layer (two 4-0 non-absorbable interrupted penetrating stitches). The inner sutures are placed between the pancreatic duct and the gastric mucosal layer (Eight interrupted 6-0 absorbable interrupted stitches) without a stenting tube

J Hepatobiliary Pancreat Sci (2014) 21:473–478

a

b

The aim of this retrospective study was to evaluate the safety and efficacy of duct-to-mucosa pancreaticogastrostomy (PG) after DP.

an experienced pancreatic surgeon (S.S.). All complications were prospectively entered into a pancreatic database, and the incidence was calculated.

Patients and methods

Surgical technique

From June 2010 to May 2012, distal pancreatectomy was performed on 50 consecutive patients for indications including pancreatic neoplasms at Kansai Medical University Hospital. Three distal pancreatectomies with en bloc celiac axis resections (DP-CAR) for locally advanced pancreatic cancer were excluded from this analysis. Pancreaticogastrostomy after DP was included since June 2010. DP-PG was performed in 21 patients with written informed consent. Exclusion criteria for DP-PG were previous gastrectomy, use of immunosuppressive agent, the presence of active peptic ulcer, and a subtotal distal pancreatectomy that needed dissection or resection of the gastroduodenal artery. The DP group consisted of 26 patients who had a previous gastrectomy (n = 4), steroidal therapy (n = 3), patient’s choice (n = 16) and laparoscopic DP (n = 3). All patients received prophylactic antibiotics intraoperatively and postoperatively for one day. Peri-pancreatic drainage fluid was collected and the amylase level was measured and monitored on postoperative days (POD) 3, 6 and every 3 days thereafter as needed. Our policy [18] was to remove drains early between 3 and 6 days after the operation in patients without infection-induced systemic inflammatory response syndrome (SIRS) when POPF defined by the International Study Group on Pancreatic Fistula (ISGPF) [9] was absent or grade A, or when fluid drained was less than 200 ml/day. Prophylactic Octreotide to prevent PF and thromboembolic prophylaxis with low molecular weight heparin were not administered in all patients. All surgical procedures were performed by or under the supervision of

The pancreatic parenchyma was transected using an ultrasonically activated scalpel and the remnant pancreatic stump was anastomosed to the posterior wall of the stomach (DP-PG group). Briefly, an incision equal to the longer axis of the cut stump of the pancreas was first made on the posterior gastric wall. To make a gastric pocket, the seromuscular layer was peeled out of the gastric mucosa. An approximation of the gastric wall and the pancreatic stump with two 4-0 non-absorbable interrupted penetrating stitches was made. Eight interrupted 6-0 absorbable interrupted stitches were placed between the gastric mucosa and any size of the main pancreatic duct (Fig. 1a,b). A pancreaticogastric stenting tube was not inserted for internal or external drainage of the pancreatic juice into the stomach. In the DP group, the pancreatic parenchyma was transected using an ultrasonically activated scalpel and the pancreatic duct was closed with a transfixion suture. The cut stump of the pancreas was not closed using the “fish-mouth” technique.

Definition of postoperative complication The overall POPF-related complication consisted of POPF, fluid collection, intra-abdominal abscess, DGE [19] and PPH [20]. We recorded the variables of SIRS criteria in patients every day. Sepsis was considered if a patient had any complication involving clinical symptoms of infectioninduced SIRS that continued for more than 2 inpatient days. Clinical symptoms of SIRS within the first 4 postoperative days were excluded as a systemic response to surgical stress.


POPF was defined according to ISGPF criteria [9]. Abdominal abscess, including liver abscess, was defined as a collection of pus or infected fluid confirmed by ultrasound, computed tomographic-guided aspiration and culture, or a second laparotomy. DGE and Hemorrhagic complication was defined according to ISGPF criteria [19, 20]. In-hospital death of a patient for any reason was recorded. The discharge of the patient from hospital depended on the following: the patient could eat at least half of a meal, was afebrile, and their C-reactive protein (CRP) levels had decreased over time to less than 5 mg/dl. Postoperative complications before hospital discharge, 30-days morbidity after discharge and rate of re-admission were recorded. When patients suffered from abdominal pain, discomfort, or distention, computed tomography (CT) scan or abdominal ultrasonography was performed to detect the presence of accumulated intraabdominal fluid. Statistical analysis Patients’ demographics, surgical and peri-operative parameters, postoperative complications before hospital discharge, 30-days morbidity after discharge, rate of re-admission and total medical cost for hospitalization were retrospectively compared between the two groups. The primary endpoint of this study was set as POPF-related complications. Continuous variables were expressed as median and range values. The countable data using Mann-Whitney U test, or the category data using Fisher’s exact test or chi-square test were compared between the two groups. Results were considered significant at P < 0.05. Statistical analyses were performed using SPSS Version 18.0 for Windows (Chicago, IL, USA).

475 Table 1 Patients characteristics DP (n = 26)

DP-PG (n = 21)

P = 0.043

Sex Male

15 (58%)

Female Age (years)

6 (29%)

11 (42%)

15 (71%)

62 (16–85)

69 (34–78)

23 (88%)

19 (90%)

III-IV Body mass index

P = 0.170 P = 0.772

ASA I-II

P-value

3 (12%) 21.5 (17.4–24.4)

>25 kg/m2

2 (10%) 23.6 (18.8–27.7)

0 (0%)

6 (29%)

P = 0.021 P = 0.035

5.3 (2.6–11.1)

P = 0.386

12.4 (8.8–15.0)

12.7 (10.4–14.8)

P = 0.600

4.2 (3.1–5.1)

4.2 (3.0–5.0)

P = 0.863

Malignant disease

13 (50%)

14 (67%)

Benign tumors

13 (50%)

7 (33%)

Chronic pancreatitis

0 (0%)

1 (4.8%)

IPMN

5 (19%)

7 (33%)

MCN

2 (7.7%)

2 (9.5%)

NET

2 (7.7%)

2 (9.5%)

Others

6 (23%)

1 (4.8%)

21 (81%)

19 (90%)

P = 0.352

Diabetes mellitus

7 (27%)

4 (19%)

P = 0.526

Previous Surgery

9 (31%)

8 (38%)

P = 0.805

WBC (×1,000/μl) Hb (g/dl) Albumin (g/dl)

5.9 (3–8.9)

Indication for operation

Comorbidity

P = 0.373

ASA American Society of Anesthesiologists, IPMN intraductal papillary mucinous neoplasm, MCN mucinous cystic neoplasm, NET neuroendocrine tumor Data are number (% of group total) or median (range)

Table 2 Comparison of surgical and peri-operative factors

Results As shown in Table 1, the proportion of females and BMI (body mass index) in the DP-PG group were significantly higher than in the DP group (P = 0.043, P = 0.021). Except for pancreatic duct diameter, no difference in surgical and peri-operative parameters was found between the two groups (Table 2). Pancreatic duct diameter in the DP-PG group was smaller than in the DP group (P = 0.031). Although a longer median time of 35 minutes was needed for PG, there was no difference in operative times. No difference in the frequency of previous surgery was found between the two groups (P = 0.805). The primary endpoint of this study was the frequency of POPF-related complications which consisted of POPF, fluid collection, intra-abdominal abscess, PPH and DGE. POPF developed in 24% of the DP-PG group and in 54% of the DP group (P = 0.037). The incidence of fluid collection in the DP-PG group (5%) was significantly lower than in the DP

Parameters

DP (n = 26)

DP-PG (n = 21)

P-value

Surgical time (min)

261 (104–486)

286 (197–538)

P = 0.314

Time needed for PG (min) Extent of blood loss (ml)

35 (20–55) 421 (25–8709)

388 (76–2170)

P = 0.948

Pancreatic parenchyma (soft/hard)

22/4

21/0

P = 0.515

Pancreatic duct diameter (mm)

2.0 (2.0–5.0)

1.5 (1.0–2.5)

P = 0.031

Thickness of the stump (mm)

14 (10–27)

12 (10–21)

P = 0.116

Splenic preservation

4 (15%)

1 (5%)

P = 0.240

Blood transfusion

2 (8%)

0 (0%)

P = 0.194

The day to initiate Per Os (day)

3 (1–6)

3 (3–4)

P = 0.542

Period of PAA (day)

1 (1–2)

1 (1–2)

P = 0.957

Postoperative day of drain removal (day)

3 (1–34)

3 (3–6)

P = 0.700

Duration of in-hospital stay (postoperative day)

9 (4–135)

8 (7–21)

P = 0.177

PAA prophylactic antibiotics administration Data are number (% of group total) or median (range)

476


Table 3 Comparison of postoperative complication DP (n = 26) Overall comp. before hospital discharge POPF related comp. Pancreatic fistula Grade B ± C DGE Intra-abdominal abscess Intra-abdominal fluid collection Drain AMY on POD3 (U/L) Wound infection Post-pancreatectomy hemorrhage Clavien–Dindo classification Grade I Grade II Grade III Grade V Mortality 30 days morbidity after discharge Re-admission Medical cost for hospitalization (yen)

DP-PG (n = 21)

20 (77%) 17 (65%) 14 (54%) 3 (12%) 1 (4%) 1 (4%) 10 (38%) 558 (19–21214) 1 (4%) 1 (4%)

5 (24%) 5 (24%) 5 (24%) 1 (5%) 1 (5%) 1 (5%) 1 (5%) 103 (53–642) 0 (0%) 0 (0%)

3 (12%) 4 (15%) 2 (8%) 1 (4%) 1 (4%) 6 (24%) 3 (12%) 930,000 (454,000–9389,000)

2 (10%) 1 (5%) 1 (5%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 744,000 (650,000–1432,000)

P-value P < 0.001 P = 0.005 P = 0.037 P = 0.407 P = 0.877 P = 0.877 P = 0.006 P = 0.015 P = 0.360 P = 0.360 P = 0.581

P = 0.360 P = 0.014 P = 0.100 P = 0.048

DGE Delayed Gastric Emptying, ISGPF International Study Group on Pancreatic Fistula, POD postoperative day Data are number (% of group total) or median (range) Re-admission was defined within 30 days after hospital discharge

group (38%; P = 0.006). In the DP-PG group and the DP group, 5% and 4% patients had intra-abdominal abscess, respectively. One patient in the DP group occurred PPH. DGE was observed one patient in each group. As shown in Table 3, the number of POPF-related complications in the DP-PG group was lower than in the DP group (5/21 vs 17/26, P = 0.005). Especially, the frequencies of overall POPF and intra-abdominal fluid accumulation were less in the DP-PG group, relative to the DP group (P = 0.037, P = 0.006). Although the frequency of grade B/C in the DP-PG group had a lower tendency relative to the DP group, there was no difference between them. Median amylase level in drainage fluid on the 3rd postoperative days was less in the DP-PG group than in the DP group (P = 0.015). The overall morbidity in the DP-PG group (5/21) was less than in the DP group (20/26, P < 0.001). Of three patients (12%) in the DP group who had clinically relevant POPF, one needed exchange of intraabdominal drain, one had radiological intervention of arterial embolization of splenic artery because of an intraabdominal bleeding, and the third needed re-operation for abdominal abscess. One patient who had POPF B in the DP-PG group was treated with intravenous antibiotics. One patient in the DP group died on postoperative day 48, because of aspiration pneumonia. Duration of in-hospital

stay was comparable between the groups (DP group: 9 days vs DP-PG group: 8 days; P = 0.117). The 30 days morbidity after hospital discharge and re-admission rate were followed. The 30 days morbidity after discharge in the DP-PG group was lower than in the DP group (0/21 vs 6/26, P = 0.014). The 6 in the DP group consisted of ischemic colitis in one, adhesional ileus in one, intra-abdominal abscess and grade B POPF in one and intra-abdominal fluid accumulation in three patients. The frequency of re-admission in the DP-PG group had a low tendency, relative to the DP group (0/21 vs. 3/26, P = 0.10). The reasons for re-admission in the DP group were ischemic colitis in one, intra-abdominal abscess in one, and adhesional ileus in the last patient. Patients in the DP group had a higher treatment cost (930,000 (454,000–9,389,000) yen) when compared with the DP-PG group (744,000 (650,000–1,432,000) yen, P = 0.048).

Discussion This retrospective study showed PG as an additional procedure after DP could prevent POPF-related complications, in spite of the higher BMI and smaller diameter of main pancreatic duct that were found in the DP-PG group relative to the DP group. Moreover, the frequencies of overall


morbidity and POPF, and intra-abdominal fluid accumulation in the DP-PG group were decreased relative to the DP group. Although there was no difference in duration of in-hospital stay, total medical cost for hospitalization and 30 days-morbidity after hospital discharge in the DP-PG group was significantly lower than in the DP group. A systematic review [7] shows evidence that POPF formation represents a major source of postoperative morbidity (13–60.9%), and is associated with several further complications, resulting in twice as much expenditures relative to patients without POPF [21]. Several surgical techniques for resection and closure of the pancreatic remnant have been proposed in an attempt to reduce these fistulas: hand-sewn suture techniques or stapled closure [12], ultrasonic dissection devices [13], pancreaticoenteric anastomosis, application of meshes [22], jejunal seromuscular or gastric serosal patches [17], or sealing with fibrin glue [16]. Leakage of pancreatic juice after distal pancreatectomy can originate from the main pancreatic duct as well as branch ducts at the cut surface of the pancreas [23, 24]. Cutting the pancreas parenchyma using an ultrasonic activated device [14] or stapler [12], or sealing with an absorbable fibrin sealant patch [16] may prevent leakage from the pancreatic duct on the stump. Our retrospective study [13], the DISPACT trial [12] and the Italian Tachosil Study Group [25] failed to prove the clinical efficacy of these devices. In general, the main pancreatic duct is sutured during distal pancreatectomy. If some factors during or after distal pancreatectomy induce the contraction of the sphincter of Oddi, an increase in pancreatic ductal pressure can increase resistance to outflow of pancreatic juice toward the duodenum [26]. In this situation, it is important to control the reflux of pancreatic juice to the cut surface of the pancreas for preventing POPF. Three options have been explored: use of prophylactic transpapillary pancreatic stents [24, 27], pancreaticojejunostomy [28], and pancreaticogastrostomy [29]. Very recently, Frozanpor et al. [27] reported results of a prospective controlled trial that did not show a beneficial effect of prophylactic transpapillary pancreatic stent insertion on rate of clinically significant POPF. Two prospective cohort studies of pancreaticojejunostomy [28] and pancreaticogastrostomy [29] showed 0% of clinically relevant POPF in a small population. Pancreaticojejunostomy needs a double anastomosis for Roux-en Y and a longer surgical time. Therefore, our choice was pancreaticogastrostomy using duct-to-mucosa without stenting. The results from this study clearly showed less POPF-related complications in the DP-PG group than in the DP group. Drain amylase level on postoperative day 3 in the DP-PG group was significantly lower than in the DP group, which might indicate better control of reflux of pancreatic juice in the DP-PG group. Moreover, this type of anastomosis can also be useful even in a thick and/or hard pancreas which can fracture during staple jaw closure,

477

resulting in POPF. Although the 30-days morbidity after hospital discharge and readmission were found in 6 and 3 of 26 patients in the DP group, no events were recorded in the DP-PG group. This can indicate that DP-PG is a promising surgical technique for preventing POPF-related complications. However, approximately 10 % of patients suffered from epigastralgia which might be caused by fixation of the stomach to the pancreas (data not shown). This symptom occurs mostly one month after a surgical procedure. This symptom resolved spontaneously and did not require any medication or intervention. Three randomized control trials are currently in progress on prophylactic transpapillary pancreatic stents (NCT00671463) in the USA, pancreaticojejunostomy (UMIN000005722) in Japan and pancreatigogastrostomy (UMIN000008519) in Japan including our center. As the costs for health care continue to increase, surgeons should consider the cost benefit for introducing a new surgical technique or strategy. Introduction of DP-PG was also associated with lower medical cost for hospitalization, relative to DP. We recognize that this study was limited in the retrospective nature of the analysis, small number of patients, and a few unbalanced clinical backgrounds between the two groups. The population analyzed was relatively homogeneous with regard to most of clinical backgrounds, underlying diseases, clinical diagnosis, and type of operation. It should be noted that a common staff followed standardized peri-operative management procedures throughout the relatively short study period. In conclusion, duct-to-mucosa PG following DP was shown to be a safe and effective technique for preventing POPF-related complications, resulting in lower medical cost for hospitalization. Conflict of interest

None declared.

Author contribution Study design: Sohei Satoi. Acquisition of data: Hiroaki Yanagimoto and Sohei Satoi. Analysis and interpretation: Hiroaki Yanagimoto and Hideyoshi Toyokawa. Manuscript drafted by: Hiroaki Yanagimoto and Sohei Satoi. Revision: Tomohisa Yamamoto and Satoshi Hirooka and Jun Yamao and So Yamaki and Hironori Ryota and Yoichi Matsui and A-Hon Kwon. Statistical advice: A-Hon Kwon.

References 1. Lillemoe KD, Kaushal S, Cameron JL, Sohn TA, Pitt HA, Yeo CJ. Distal pancreatectomy: indications and outcomes in 235 patients. Ann Surg. 1999;229:693–700. 2. Balcom JH, Rattner DW, Warshaw AL, Chang Y, Fernandez-del Castillo C. Ten-year experience with 733 pancreatic resections: changing indications, older patients, and decreasing length of hospitalization. Arch Surg. 2001;136:391–8. 3. Kleeff J, Diener MK, Z’graggen K, Hinz U, Wagner M, Bachmann J, et al. Distal pancreatectomy: risk factors for surgical failure in 302 consecutive cases. Ann Surg. 2007;245:573–82.

478 4. Fahy BN, Frey CF, Ho HS, Beckett L, Bold RJ. Morbidity, mortality, and technical factors of distal pancreatectomy. Am J Surg. 2002;183:237–41. 5. Fabre JM, Houry S, Manderscheid JC, Huguier M, Baumel H. Surgery for left-sided pancreatic cancer. Br J Surg. 1996;83:1065– 70. 6. Pannegeon V, Pessaux P, Sauvanet A, Vullierme MP, Kianmanesh R, Belghiti J. Pancreatic fistula after distal pancreatectomy: predictive risk factors and value of conservative treatment. Arch Surg. 2006;141:1071–6. 7. Knaebel HP, Diener MK, Wente MN, Büchler MW, Seiler CM. Systematic review and meta-analysis of technique for closure of the pancreatic remnant after distal pancreatectomy. Br J Surg. 2005;92:539–46. 8. Kuroki T, Tajima Y, Kanematsu T. Surgical management for the prevention of pancreatic fistula following distal pancreatectomy. J Hepatobiliary Pancreat Surg. 2005;12:283–5. 9. Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, et al. International Study Group on Pancreatic Fistula Definition. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138:8–13. 10. Bilimoria MM, Cormier JN, Mun Y, Lee JE, Evans DB, Pisters PW. Pancreatic leak after left pancreatectomy is reduced following main pancreatic duct ligation. Br J Surg. 2003;90:190–6. 11. Kawai M, Tani M, Yamaue H. Transection using bipolar scissors reduces pancreatic fistula after distal pancreatectomy. J Hepatobiliary Pancreat Surg. 2008;15:366–72. 12. Diener MK, Seiler CM, Rossion I, Kleeff J, Glanemann M, Butturini G, et al. Efficacy of stapler versus hand-sewn closure after distal pancreatectomy (DISPACT): a randomised, controlled multicentre trial. Lancet. 2011;377:1514–22. 13. Yui R, Satoi S, Toyokawa H, Yanagimoto H, Yamamoto T, Hirooka S, et al. Less morbidity after introduction of a new departmental policy for patients who undergo open distal pancreatectomy. J Hepatobiliary Pancreat Sci. 2014;21:72–77. 14. Sugo H, Mikami Y, Matsumoto F, Tsumura H, Watanabe Y, Futagawa S. Comparison of ultrasonically activated scalpel versus conventional division for the pancreas in distal pancreatectomy. J Hepatobiliary Pancreat Surg. 2001;8:349–52. 15. Blansfield JA, Rapp MM, Chokshi RJ, Woll NL, Hunsinger MA, Sheldon DG, et al. Novel method of stump closure for distal pancreatectomy with a 75% reduction in pancreatic fistula rate. J Gastrointest Surg. 2012;16:524–8. 16. Suzuki Y, Kuroda Y, Morita A, Fujino Y, Tanioka Y, Kawamura T, et al. Fibrin glue sealing for the prevention of pancreatic fistulas following distal pancreatectomy. Arch Surg. 1995;130:952–5. 17. Oláh A, Issekutz A, Belágyi T, Hajdú N, Romics L Jr. Randomized clinical trial of techniques for closure of the pancreatic remnant following distal pancreatectomy. Br J Surg. 2009;96: 602–7.

J Hepatobiliary Pancreat Sci (2014) 21:473–478 18. Yamaki S, Satoi S, Toyokawa H, Yanagimoto H, Yamamoto T, Hirooka S, et al. The clinical role of critical pathway implementation for pancreaticoduodenectomy in 179 patients. J Hepatobiliary Pancreat Sci. 2013;20:271–8. 19. Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2007;142:761–8. 20. Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, et al. Postpancreatectomy hemorrhage (PPH)–an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery. 2007;142:20–5. 21. Rodríguez JR, Germes SS, Pandharipande PV, Gazelle GS, Thayer SP, Warshaw AL, et al. Implications and cost of pancreatic leak following distal pancreatic resection. Arch Surg. 2006;141: 361–5. 22. Hamilton NA, Porembka MR, Johnston FM, Gao F, Strasberg SM, Linehan DC, et al. Mesh reinforcement of pancreatic transection decreases incidence of pancreatic occlusion failure for left pancreatectomy: a single-blinded, randomized controlled trial. Ann Surg. 2012;255:1037–42. 23. Truty MJ, Sawyer MD, Que FG. Decreasing pancreatic leak after distal pancreatectomy: saline-coupled radiofrequency ablation in a porcine model. J Gastrointest Surg. 2007;11:998–1007. 24. Abe N, Sugiyama M, Suzuki Y, Yamaguchi Y, Yanagida O, Masaki T, et al. Preoperative endoscopic pancreatic stenting for prophylaxis of pancreatic fistula development after distal pancreatectomy. Am J Surg. 2006;191:198–200. 25. Montorsi M, Zerbi A, Bassi C, Capussotti L, Coppola R, Sacchi M, et al. Efficacy of an absorbable fibrin sealant patch (TachoSil) after distal pancreatectomy: a multicenter, randomized, controlled trial. Ann Surg. 2012;256:853–9. 26. Hashimoto Y, Traverso LW. After distal pancreatectomy pancreatic leakage from the stump of the pancreas may be due to drain failure or pancreatic ductal back pressure. J Gastrointest Surg. 2012;16:993–1003. 27. Frozanpor F, Lundell L, Segersvärd R, Arnelo U. The effect of prophylactic transpapillary pancreatic stent insertion on clinically significant leak rate following distal pancreatectomy. results of a prospective controlled clinical trial. Ann Surg. 2012;255:1032–6. 28. Wagner M, Gloor B, Ambühl M, Worni M, Lutz JA, Angst E, et al. Roux-en-Y drainage of the pancreatic stump decreases pancreatic fistula after distal pancreatic resection. J Gastrointest Surg. 2007; 11:303–8. 29. Sudo T, Murakami Y, Uemura K, Hayashidani Y, Hashimoto Y, Nakashima A, et al. Distal pancreatectomy with duct to mucosa pancreaticogastrostomy: a novel technique for preventing postoperative pancreatic fistula. Am J Surg. 2011;202:77–81.