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doi: 10.1097/MPA.0b013e3181b57705
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Pancreatic Leakage After Pancreaticoduodenectomy: The Impact of the Isolated Jejunal Loop Length and Anastomotic Technique of the Pancreatic Stump

Fragulidis, Georgios P. MD, PhD; Arkadopoulos, Nikolaos MD, PhD; Vassiliou, Ioannis MD, PhD; Marinis, Athanasios MD, PhD; Theodosopoulos, Theodosios MD, PhD; Stafyla, Vaia MD, PhD; Kyriazi, Maria MD; Karapanos, Konstantinos MD; Dafnios, Nikolaos MD, PhD; Polydorou, Andreas MD, PhD; Voros, Dionysios MD, PhD; Smyrniotis, Vassilios MD, PhD

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From the Second Department of Surgery, Aretaieion University Hospital, Athens Medical School, University of Athens, Athens, Greece.

Received for publication September 23, 2008; accepted June 17, 2009.

Reprints: Georgios P. Fragulidis, MD, PhD, 23 El. Venizelos Str, 16675 Athens, Greece (e-mail: foreo@otenet.gr).

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Abstract

Objectives: To evaluate the impact of the length of the isolated jejunal loop and the type of pancreaticojejunostomy on pancreatic leakage after pancreaticoduodenectomy.

Methods: One hundred thirty-two consecutive patients who underwent a pancreaticoduodenectomy were studied according to the length of the isolated jejunal loop (short loop, 20-25 cm vs long loop, 40-50 cm) and the type of pancreaticojejunostomy (invagination vs duct to mucosa).

Results: The use of the long isolated jejunal loop was associated with a significantly lower pancreatic leakage rate compared with the use of a short isolated jejunal loop (4.34% vs 14.2%, P < 0.05). In addition, the use of duct-to-mucosa technique was associated with significantly lower incidence of postoperative pancreatic fistula compared with the invagination technique (4.2% vs 14.5%, P < 0.05). Finally, patients with a short isolated jejunal loop compared with patients with a long loop had increased morbidity (50.7% vs 27.5%, P < 0.05) and prolonged hospital stay (16.3 ± 1.9 days vs 10.2 ± 2.3 days, P < 0.05). Overall mortality rate was 1.5%.

Conclusions: The use of a long isolated jejunal loop and a duct-to-mucosa pancreaticojejunostomy is associated with decreased pancreatic leakage rate after pancreaticoduodenectomy.

Pancreaticoduodenectomy (PD) is an established surgical procedure for the treatment of malignant and benign diseases of the pancreas and periampullary lesions. Because of continuous improvements in surgical techniques and perioperative management, the mortality rate has decreased below 5%.1-5 However, morbidity is still high (30%-50%), and leakage from the pancreatic remnant accounts for most postoperative complications. Pancreatic leakage occurs in 5% to 29% of patients undergoing PD and is a major cause of morbidity and mortality in these patients.5-12

Although various techniques have been proposed to prevent pancreatic stump-related complications effectively, management of the pancreatic remnant is still controversial. Simple closure of the pancreatic duct by means of suture ligation or occlusion with glue and external drainage of the duct have not been shown to reduce pancreatic leakage-related complications and may precipitate pancreatic insufficiency and postoperative insulin-dependent diabetes.13-20 In addition, efforts to minimize pancreatic leakage from the pancreaticoenteric anastomosis resulted in the development of a variety of techniques for the construction of pancreaticojejunostomies (PJs) and to a lesser extent pancreaticogastrostomies.4,21-30 Pancreatic anastomosis with a jejunal loop (PJ) is probably the most favorable and well-established procedure of reconstruction of the pancreatic stump after PD.4,29,30-39 Based on the type of restoration of the biliary enteric route, PJ can be performed either in a common jejunal loop of reconstruction of the digestive tract or by isolating the PJ in a single loop fashioned in a Roux-en-Y configuration. The use of an isolated jejunal loop for the pancreatic anastomosis has been advocated by many surgeons,40-50 and this method of reconstruction is routinely applied in our department with very good results.45 However, the length of the isolated jejunal loop has not been studied as a potential risk factor for pancreatic leakage after PD. Therefore, we designed the present study with the aim to evaluate the impact of the length of the isolated jejunal loop on postoperative pancreatic leakage after PD with the use of 2 different methods of PJ anastomosis (invagination vs duct to mucosa).

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MATERIALS AND METHODS

From January 1998 to December 2007, 132 consecutive patients who underwent a PD were studied. The patients had either a classic Whipple resection (n = 98) or pylorus-preserving PD (n = 34), according to the decision of the attending surgeon. All patients were thoroughly informed about the procedure, and consent was obtained.

Preoperative evaluation consisted of an extensive imaging workup including computed tomography (CT) or magnetic resonance imaging to rule out metastatic disease or encasement of the superior mesenteric vessels. Transduodenal fine needle biopsy and endoscopic biliary stenting were occasionally used whenever required. The final assessment of the resectability of the tumor (in case of malignancy) was made intraoperatively, based upon findings such as liver metastases not identified preoperatively and involvement or encasement of superior mesenteric vessels or portal vein. All patients received perioperative antibiotic prophylaxis and antithrombotic prophylaxis (low-molecular weight heparin) was administered for 4 weeks. None of the patients received octreotide analogue preoperatively or postoperatively.

The isolated jejunal loop used for reconstruction after PD was considered as either (1) short (20 to 25 cm) or (2) long (40 to 50 cm) whereas the PJ anastomotic technique used was either (a) invagination or (b) duct to mucosa. Based on these variables, patients were divided into 4 groups: group 1a (short loop + invagination, n = 32), group 1b (short loop + duct to mucosa, n = 31), group 2a (long loop + invagination, n = 30), and group 2b (long loop + duct to mucosa, n = 39). Patient allocation to each group was completed during laparotomy in an alternating way, as soon as the PD was deemed appropriate. Epidemiological, operative, and histological data are presented in Table 1.

Table 1
Table 1
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Surgical Technique

After completion of the standard PD and thorough hemostasis, the first segment of the jejunum designated to drain the pancreatic stump was divided to obtain an isolated jejunal loop with a length of either 20 to 25 cm (short loop) or 40 to 50 cm (long loop). Afterwards, the pancreatic remnant was mobilized for approximately 1.5 cm, and a PJ anastomosis was performed with either one of the 2 following techniques, regardless of the diameter of the pancreatic duct, (a) the conventional invagination technique created with 2 rows of continuous or interrupted sutures Prolene 3-0 (Ethicon, Somerville, NJ) between the cut edge of the jejunum and the pancreatic parenchyma, directing the end of the pancreas to invaginate into the jejunum and (b) the end-to-side duct-to-mucosa PJ anastomosis created with the use of interrupted 5-0 or 6-0 PDS (Ethicon) sutures between the pancreatic duct and the mucosa of the jejunum and reinforced by seromuscular sutures Prolene 3-0 (Ethicon) from the jejunum to the cutting edge of the pancreatic parenchyma.

After performing the PJ anastomosis, the rest of the jejunum was pulled up to restore the drainage of bile (hepaticojejunostomy) and gastric content (gastrojejunostomy or duodenojejunostomy in case of pylorus-preserving PD) by 2 consecutive hand-sewn anastomoses with a distance of approximately 10 to 15 cm between them. The rerouting of the pancreatic secretions from the isolated jejunal loop to the main alimentary stream was secured by a hand-sewn jejunojejunostomy anastomosis 15 cm distally from the gastro or duodenal-jejunal anastomosis in a Roux-en-Y configuration (Fig. 1). Finally, a closed suction tube was placed near the PJ anastomosis and exteriorized through the right lateral abdominal wall.

Figure 1
Figure 1
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Perioperative Management-Data Collection

All patients received a standard perioperative management. Details of surgical procedure and complications were recorded by individuals who were unaware of the group allocation. Drain fluid volume and amylase levels were monitored daily. Nasogastric tube was removed, and feeding was introduced as soon as adequate gastric emptying was reestablished. The drain tube was removed 6 to 10 days postoperatively provided that amylase levels in the drainage fluid did not exceed serum levels by more than 3 times. When intra-abdominal collections were suspected, an abdominal CT was used and percutaneous aspiration was carried out for fluid culture and biochemical analysis. A percutaneous tube for drainage under CT guidance was inserted when pancreatic collections reoccurred or an intra-abdominal abscess developed.

A pancreatic fistula as a result of pancreatic leakage was defined as a drainage volume of more than 50 mL after postoperative day 8 with an amylase level greater than 1000 IU/mL or greater than 3 times the serum amylase levels, in accordance to the definition of the International Study Group of Pancreatic Fistula.51 When a diagnosis of a pancreatic fistula was established, the tube remained in place until the fistula volume was reduced to a level less than 50 mL per day. The severity of pancreatic leakage was graded as follows: (1) grade A, when it subsided without intervention; (2) grade B, when a nonsurgical intervention was applied to resolve the complication by using percutaneous CT-guided drainage and appropriate antibiotic therapy; and (3) grade C, when operative intervention was required.

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Study End Points

The primary outcome measure of the impact of the length of the isolated jejunal loop and the technique of the PJ anastomosis was postoperative pancreatic leakage rate. Secondary end points were morbidity, mortality, and length of hospital stay.

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Statistical Analysis

Continuous data are expressed as mean ± SD. Comparisons of categorical and continuous variables were assessed by the χ2 and t tests, respectively. An α level = 0.05 of statistical significance was used. The statistical software Minitab (version 14; Mintab Inc, State College, Pa) was used for the statistical analysis.

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RESULTS

All 132 patients were eligible for final analysis. All groups were comparable regarding epidemiological, histological, and intraoperative data (Table 1).

Pancreatic leakage incidence in relation to the length of the isolated jejunal loop and the PJ anastomotic technique is presented in Table 22 test). The use of the long isolated jejunal loop was associated with a significantly lower pancreatic leakage rate compared with the use of a short isolated jejunal loop (4.34% vs 14.2%, P = 0.047). The duct-to-mucosa technique was associated with better anastomotic integrity than invagination as manifested by the lower rates of postoperative pancreatic fistula (4.2% vs 14.5%, P = 0.041). Overall, the group of patients in which a long isolated jejunal loop and a duct-to-mucosa PJ anastomotic technique was used (group 2b), had a statistically significant lower pancreatic leakage rate compared with group 1a (0% vs 18.75%, P = 0.005), group 1b (0% vs 9.67%, P = 0.047), and group 2a (0% vs 10%, P = 0.043) with a likelihood ratio of 0.016 (Fig. 2).

Figure 2
Figure 2
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Table 2
Table 2
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Postoperative complications, morbidity, hospitalization stay, and mortality are presented in Table 3. Two patients from group 1a developed a grade C pancreatic fistula (International Study Group of Pancreatic Fistula classification) and were reoperated; the disruption of the PJ anastomosis that was found in both cases was managed by means of staple closure of the isolated jejunal loop and external drainage of the pancreatic stump. Four more patients in group 1a, 3 patients in group 1b, and 3 patients in group 2a developed grade A/B fistulas that were managed nonoperatively (CT-guided percutaneous aspiration and protracted drainage and antibiotics in cases of grade B fistulas).

Table 3
Table 3
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Overall morbidity was significantly increased in patients with a short jejunal loop and invagination of the pancreatic stump compared with all other groups (Table 3). In addition, patients with a short isolated jejunal loop (groups 1a and 1b combined) had higher morbidity compared with those with a long isolated jejunal loop (groups 2a and 2b combined; 50.7% vs 27.5%, P = 0.006). However, if we compare the 2 different techniques for the PJ anastomosis, no difference in overall morbidity is found (46.7% in invagination technique vs 31.4% in duct-to-mucosa technique, P = 0.071) despite the difference in pancreatic leakage rate in favor of the duct-to-mucosa technique (Table 2).

The length of hospital stay was significantly increased in patients with the short isolated jejunal loop in comparison to patients using the long isolated loop (P < 0.01).

Overall mortality rate in our study was 1.5%. One patient died in each of groups 1a and 1b because of disruption of the hepaticojejunal anastomosis (necrosis of the isolated jejunal loop) and disruption of the PJ anastomosis, respectively. Differences in mortality between the various subgroups were not statistically significant (Table 3).

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DISCUSSION

Drainage of the pancreatic remnant to the gastrointestinal (GI) tract has been thoroughly investigated, and various techniques have been reported. Despite sporadic reports describing low rates of pancreatic leakage (from 0%-3% up to 14.3%) after pancreaticogastrostomy, no valid conclusions can be drawn regarding its superiority against PJ and further randomized controlled studies are required.4,23,34,52,53 Pancreaticojejunostomy is still the most commonly used method of restoring pancreaticoenteric continuity after PD, and its technical improvements are essential to reduce the pancreatic leakage rate.27

Among the different variants of pancreatic stump drainage, anastomosis with an isolated Roux loop has demonstrated the most favorable results in retrospective series. Papadimitriou et al45 reported no PJ anastomotic leakage in a series of 105 consecutive patients who underwent subtotal PD for pancreatic cancer, where the pancreatic remnant was anastomosed to an isolated jejunal loop in a Roux-en-Y configuration. Similar results with Roux-en-Y PJ anastomosis have been reported by Kingsnorth40 and Khan et al44 in a series of 52 and 41 patients, respectively. Recently, Sutton et al42 reported a series of 61 patients with zero leakage rate from a PJ anastomosis that was constructed using a defunctionalized jejunal loop approximately 40 cm long. Although the reasons remain unclear, the incidence of pancreatic leakage seems to be lower when isolated Roux-en-Y loops are used.

Our study is the first to specifically address the issue of the length of the isolated jejunal loop in relation to pancreatic leakage. We have shown that drainage of the pancreatic secretions through a short isolated jejunal loop (20-25 cm) was associated with a pancreatic leakage rate 3 times greater than the rate associated with the use of a long isolated loop.

Regarding anastomotic technique used for reconstruction between the pancreatic cut surface and the jejunum, both end-to-side duct-to-mucosa anastomosis or end-to-end invagination techniques have been extensively investigated. Recent studies seem to imply that duct-to-mucosa anastomosis may be related with a lower leakage rate than invagination anastomosis.26,29,32,34,39,54,55 Initially used by Cattel in 1943, duct-to-mucosa anastomosis allows direct contact of the pancreatic duct with the jejunal mucosa and was previously recommended only for patients with a dilated pancreatic duct. In a meta-analysis of 2361 patients with PD collected from the literature before 1991, a significantly higher incidence of pancreatic fistula was found with end-to-side invagination anastomosis (26%) compared with duct-to-mucosa anastomosis (16%).56 In addition, a number of nonrandomized studies demonstrated that duct-to-mucosa anastomosis is related with a lower leakage rate compared with invagination technique.6,55 Matsumoto et al57 found a pancreatic fistula rate of 4.2% after duct-to-mucosa anastomosis versus 26.4% after invagination anastomosis in a retrospective study of 100 patients. Hosotani et al29 reported that only PJ anastomotic technique ended up to be an independent risk factor using multivariate analysis. The authors assumed that duct-to-mucosa PJ anastomosis reduced the risk of pancreatic leakage after PD (odds ratio, 4.15). In a single surgeon's experience report including 56 patients with PD, the author concluded that duct-to-mucosa anastomosis was a safer technique than invagination anastomosis.58 Similarly, Suzuki et al59 reported that duct-to-mucosa anastomosis was related to significantly reduced leakage rate (6.25% vs 19.5%), although this result was associated with pancreatic texture and size of the pancreatic duct. In accordance with the previous reports, our study confirmed that duct-to-mucosa anastomosis is associated with a lower leakage rate compared with the invagination technique regardless of the length of the isolated loop.

In conclusion, our data suggest that the best way to reduce pancreatic leakage rate after PD is to use a combination of a long isolated jejunal Roux loop for rerouting of pancreatic secretions with the duct-to-mucosa technique for the PJ anastomosis. The underlying mechanism of the association between isolated loop length and PJ protection has not been addressed in this study and may be related with the effects of bile reflux to the anastomosis and the activation of pancreatic proenzymes, as suggested by other investigators.40-44 Further experimental studies are needed to clarify this issue.

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ACKNOWLEDGMENT

The authors thank Dimitropoulou, P., RN, Surgical Intensive Care Unit, Second Department of Surgery, Aretaieion University Hospital, Athens Medical School, University of Athens, for her invaluable assistance with data collection.

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Keywords:

pancreaticoduodenectomy; pancreatic leakage; pancreatic fistula; isolated jejunal loop; Roux en Y; pancreaticojejunostomy

© 2009 Lippincott Williams & Wilkins, Inc.

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