Double loop reconstruction following pancreaticoduodenectomy for malignant tumor: Short-term outcome

Abstract

Background

To evaluate the use of a double loop reconstruction following pylorus preserving proximal pancreaticoduodenectomy (PPPPD).

Methods

Morbidity and mortality were evaluated in 55 patients undergoing PPPPD for malignant tumors, followed by a double loop reconstruction.

Results

The mean intra-operative blood loss was 908 mL ± 531. In-hospital mortality was 5.4% (3/55 pts). The mean length of hospital stay was 17 ± 5 days (range 12–45 days). Postoperative complications occurred in 25 patients (46.2%). Five patients developed an anastomotic leak, one biliary and four pancreatic (4/55; 7%). Delayed gastric emptying occurred in 8 patients (14.5%). Reoperation was required in two patients for hemorrhage.

Conclusions

A double loop alimentary reconstruction following PPPPD led to a low incidence of DGE and pancreatic fistula. Although mortality rate was higher than that reported by referral centres, this technique has been performed in a not specialized unit attaining acceptable results.

1. Introduction

Pancreaticoduodenectomy is proven and established treatment modality with a low mortality in periampullary cancer and chronic pancreatitis [1].

While the mortality of this operation has dramatically decreased to well below 5% in high volume centres morbidity is still high [2].

Pancreaticoduodenectomy is a difficult procedure including an initial resection stage followed by 3 anastomoses with a significant risk of leakage, most commonly the pancreatic anastomosis. It is also associated with infectious complications, sepsis and death [3].

Among different reported method of reconstruction following pancreaticoduodenectomy, the technique based on placing all the anastomoses along a single jejunal loop is the most commonly applied. On the other hand the use of two separate intestinal loops for the biliary and pancreatic anastomosis has been reported to have potentially significant advantages [4]^, [5].

In the current study, we present our experience with pylorus preserving proximal pancreaticoduodenectomy(PPPPD), followed by a double loop reconstruction to perform gastrointestinal and bilio-pancreatic anastomoses.

2. Materials and methods

Fifty-five pancreaticoduodenectomies were performed in a ten year period before 2006 for malignant tumors. All patients had thorough preoperative staging with endoscopic ultrasound scan (since it was available), computed tomography (CT) or magnetic resonance imaging (MRI) scan and a postoperative histological confirmation of diagnosis. Patients with distant metastasis, involvement of mesenteric vessels or common hepatic artery were not considered for resection.

2.1. Surgical technique

All patients underwent pylorus-preserving proximal pancreaticoduodenectomy (PPPPD) with potentially curative intent. A full exploration of abdominal cavity was performed to exclude any possible sign of metastatic spread together with a careful assessment of the local extent of the tumor. Frozen sections were performed routinely at the pancreatic resection margin in all patients. In case of positive frozen section further resection of pancreatic parenchyma was performed. Tissue dissection, vessel ligation, complete removal of lymph nodes and an adequate haemostasis were ensured with LigaSure^® (Valleylab^®, Boulder, USA) since it was available. Reconstruction was performed by means of duodeno-jejunostomy, choledoco-jejunostomy, and pancreatico-jejunostomy on a separate jejuneal loop. The duodenum was transected proximally about 2–3 cm below the pylorus and distally in correspondence of the first jejunal loop, away from the uncinate process of pancreas. The proximal duodenum and proximal jejuneum were anastomosed with either an end to end anastomosis using Valtrac^® ring (Sherwood medical Company, St. Louis, Missouri, USA) [6] or an end to side anastomosis done by using circular stapler (Premium Plus CEEA^® 25, Tyco Healthcare Group LP). About 10–15 cm downstream, on the same jejuneal loop, an anastomosis with common bile duct or hepatic duct was fashioned with an hand-sewn suture at the antimesenteric side, with a 3/0 absorbable monofilament suture. A pancreaticojejunostomy was performed approximately 60 cm beyond the biliary anastomosis, creating a Roux-en-Y limb, led through the mesocolon, and attached to the capsule of body of pancreas (Fig. 1). Approximately 40 cm below the pancreaticojejunostomy an end to side jejuno-jejuneal anastomosis was created by using Valtrac^® ring (Fig. 2). After surgery, medical treatment was based on intravenous electrolyte and balanced fluid solutions. To prevent pancreatic leakage, three daily doses of 100 μg octreotide were given as subcutaneous injections for the first postoperative week. Parenteral nutrition via central venous catheter started on the second postoperative day.

Fig. 1.

Isolated Roux-en-Y reconstruction technique after pancreaticoduodenectomy.

Fig. 2.

Isolated Roux loop pancreaticojejunostomy performed by using Valtrac^® ring for the end to side jejuno-jejuneal anastomosis (Sherwood medical Company, St. Louis, Missouri, USA).

2.2. Postoperative evaluation

All complications were recorded together with in-hospital deaths, reinterventions and duration of hospital stay. Specifically, the incidence of overall complications, infectious complications, wound infection, intra-abdominal collection or abscess, biliary leak, pancreatic leak and sepsis was recorded. Postoperative Pancreatic fistula (POPF), was defined as a drain output of any measurable volume of fluid on or after postoperative day 3 with an amylase content greater than 3 times the serum amylase activity. Three different grades of POPF (grades A, B, C) were defined according to the clinical impact on the patient's hospital course [7]. Postoperative delayed gastric emptying (DGE) was defined as the inability to return to a standard diet by the end of the first postoperative week with prolonged intubation of the patient providing that a mechanical cause of gastric obstruction was excluded by means of either endoscopy or radiographic contrast. Three different grades of postoperative delayed gastric emptying (grades A, B, C) were defined based on impact on the patient's clinical course and postoperative management [8]. Postpancreatectomy hemorrhage (PPH) was defined according to the International Study Group of Pancreatic Surgery based on the onset (early = ≤ 24 h or late= >24 h), location (intraluminal or extraluminal) and severity (mild or severe) of bleeding. Three different grades of PPH (grades A, B, C) were defined based on the time of onset, site of bleeding, severity and clinical impact [9]. Statistical analysis was carried out using SPSS for Windows (version17.0, SPSS Inc., Chicago, IL). Results are expressed as either median (range) or mean ± sd.

3. Results

There were 31 males and 24 females, with a median age of 61 years (range 41–71). All patients underwent a PPPPD with isolated Roux-en-Y limb pancreaticojejunostomy. Thirty-nine patients had adenocarcinoma of pancreas; 8 patients had an ampullary of Vater tumor, 3 patients had a distal bile duct tumor, 3 patients had a cystic adenocarcinoma and 2 had a neuroendocrine tumor (Table 1). The mean intra-operative blood loss was 908 mL ± 531 (range 400–2400), and the mean operative time was 343 ± 27 min (range 280–400). Among 52 patients who survived the operation, the mean length of hospital stay was 17 ± 5 days (range 12–45 days). Postoperative complications occurred in 25 patients (46.2%) (Table 1). Five patients developed an anastomotic leak, one from biliary and four from pancreatic anastomosis (4/55; 7%). Three patients developing grade A (n = 2) or B (n = 1) pancreatic fistula were treated conservatively; one patient developing a grade C fistula was treated surgically. Delayed gastric emptying occurred in 8 patients (14.5%). Seven patients developing DGE grade A (n = 4) or B (n = 3) were treated conservatively with reinsertion of nasogastric tube and parenteral nutrition. One patient developing DGE grade C underwent relaparotomy for associated complication as grade C fistula and grade C postpancreatectomy hemorrhage (PPH). The PPH aroused from an unidentified source on the 13th postoperative day with disruption of the pancreaticojejunal anastomosis and fresh blood in the proximal jejunum. Technically, it was not possible to reconstruct a new pancreaticojejunostomy because the pancreatic stump was grossly oedematous and pancreatic duct non-dilated. Completion pancreatectomy, with spleen preservation and over sewing of the jejunum was performed with a complete achieved hemostasis; patient was discharged home 15 days later. An other patient required re-operation for PPH manifested as a early postoperative arterial bleeding caused by a sloughing of a ligature. The overall in-hospital mortality rate was 5.4% (3 out of 55 patients): two patients died in the intensive care unit twenty days after the operation for multiple organ failure, whereas one expired 1 day after surgery for a massive pulmonary embolism (Table 1).

Table 1.

Histopathologic diagnosis, intra-operative and post-operative outcome in 55 patients undergoing double loop reconstruction after pylorus preserving proximal pancreaticoduodenectomy (PPPPD).

Parameters	No.(%)
Histophatologic diagnosis
Pancreas	39(70.9)
Ampulla	8(14.5)
Distal bile duct	3(5.4)
Serous cystadenocarcinoma	3(5.4)
Neuroendocrine	2(3.6)
Intra-operative outcome
Operative time (minutes)
Mean (±SD)	343 ± 27
Median	5.3
Blood loss (mL)
Mean (±SD)	908 ±531
Median	750
Post-operative outcome
LHS (days)
Mean (± SD)	17 ± 5
Median	16
Overall complications	25(46.2)
Pleural effusion	1(1.8)
Acute pancreatitis	1(1.8)
Cholangitis	1(1.8)
IAA	1(1.8)
Wound infection	2(3.6)
Biliary leak	1(1.8)
Pancreatic leak	4(7.2)
Sepsis		2(3.6)
DGE		8(15.4)
PPH		2(3.6)
Pulmonary embolism		1(1.8)
MOF		1(1.8)
Mortality		3 (5.4)

LHS = length of hospital stay.

IAA = intra-abdominal abscess.

DGE = delayed gastric emptying.

PPH = postoperative hemorrhage.

MOF = multiple organ failure.

4. Discussion

Among the reconstruction techniques after pylorus-preserving proximal pancreaticoduodenectomy (PPPPD), the isolated roux-loop pancreaticojejunostomy has been claimed to carry a lower incidence of pancreatic fistula and to reduce the mortality rate from this complication [4]^, [5]^, [10]. It has been postulated that such technique by preventing the collection of a large volume of bilio-pancreatic secretion and the consequent increase of intraluminal pressure in a single loop may avoid an excessive tension on the new fashioned pancreaticobiliary anastomosis. It has also been suggested to reduce the activation of pancreatic juice by bile and intestinal contents and consequently the risk of anastomotic breakdown [11]. In a previous study, the use of this technique was associated with an adequate preservation of exocrine and endocrine function of the pancreatic gland [12]. Although in this study exocrine and endocrine function were not examined, a low rate of pancreatic fistula has been observed and the 3 deaths recorded were not related to pancreatic fistula. The observed rate of complications was in line with previous studies suggesting that PPPPD carries a significant morbidity regardless of the technique used [2]. On the other hand, a 5.4% mortality rate higher than that reported by specialized centres may reflect the associations observed for many surgical procedures between hospital volume and operative mortality are largely mediated by surgeons volume [13]. The use of octreotide, a synthetic long-acting somatostatin analogue with well recognized inhibitory effects on exocrine pancreatic secretion has been either associated with decreased overall complication rate after pancreaticoduodenectomy or defined as a cost effective strategy [14]^, [15]^, [16]^, [17]^, [18]. In the present study the postoperative administration of octreotide might have had an impact on postoperative outcome. A recent pilot trial showed a continuous postoperative infusion of Somatostatin-14 decreases postoperative pancreatic juice leakage from the pancreatic remnant [19]. Further well-designed studies with more patients are still needed to establish the impact of Somatostatin-14 and its analogues, particularly in terms of the timing and duration of application.

The isolation of the pancreatic and hepatic anastomoses on separate Roux loops has been previously reported as a surgical manoeuvre adding to the operative time [12]. Mechanical devices may contribute to simplify the reconstruction step and reduce prolonged operative time, previously reported as a risk factor (particularly if more than 8 h) associated with a significantly higher incidence of pancreatic leak following PD [20]. In this study, mechanical devices used in the restoration of continuity following PPPPD could have reduced mean operative time well below the above mentioned risky threshold. A reported danger of the isolated Roux-en-Y pancreaticoenteric anastomosis may be the temporary or partial obstruction of the distal duodenojejunal anastomoses secondary to edema with a potential risk of subsequent anastomotic leakage induced by the increase in intraluminal pressure [5]. In the current study, we did not observe any complications of gastrointestinal anastomoses. The PPPPD is a modification of the classical “Whipple” that avoids the resection of the distal part of the stomach. Since its initial publication by Watson in 1945 and Traverso- Longmire in 1978 [21]^, [22], it has been the preferred technique by many authors. Controversy exists regarding the impact of this surgical technique on the risk of DGE that represents almost half of all complications [23]^, [24]^, [25]^, [26]^, [27]^, [28]^, [29]. Recent prospective randomized controlled clinical trials have shown that Whipple procedure and PPPPD were associated with comparable incidence of DGE, operation time, blood loss, hospital stay and morbidity and mortality. Besides, even the overall long-term and disease-free survival were comparable in both groups [30]^, [31]^, [32].

In this study the rate of DGE after the pylorus preserving technique associated with a isolated roux-loop pancreaticojejunostomy was 14.5% that is lower than those previously reported [33]^, [34]^, [35]^, [36]. The relation between the choice of a specific reconstructive method, avoidance of postoperative complications and the occurrence of DGE is not clear [37]^, [38]. The reason of a low rate of DGE in our series (where no pro-motility drugs such erythromycin were administered) can be partly explain by the preservation of the duodenal pacemaker, which is located 0.5–1 cm distally from the pylorus as supported by experimental works on dogs [39]^, [40] and humans [41]^, [42]. On the other hand, whether the type of reconstruction performed in the current study was a contributing factor to avoid the onset of DGE remains theoretical. In this study, we observed two cases of postoperative hemorrhage with one presenting within 24 h after surgery (early bleeding) and the other one presenting after 24 h postoperatively (late bleeding). Although postoperative haemorrhage after pancreatic resection is a well-recognized complication, it is relatively uncommon [43]. As a result, its management remains unclear. Early postoperative hemorrhage after surgery is caused by a technical failure and generally needs immediate laparotomy as observed in our series. On the other hand, delayed postoperative hemorrhage, although uncommon, poses a serious problem in the postoperative period and carries a high mortality. The most appropriate management of this latter complication remains controversial [44]. Delayed arterial hemorrhage post PD occurs in 2–4% of cases and our experience is comparable with a frequency of 3.6%. In our case of late bleeding local complications such as disruption of the pancreaticojejunal anastomosis and intraabdominal sepsis potentially contributed to the development of delayed arterial hemorrhage. Emphasising that when present, contributing local complications of pancreatic resection should be identified and managed appropriately, in addition to targeted delayed arterial hemorrhage therapy. The present study has several limitations among which it seems mandatory to underline its descriptive nature with no reported comparison to other techniques. Another drawback is represented by the small number of patients described in this series. A randomized controlled trial comparing a single versus two separate intestinal loops for the biliary and pancreatic anastomosis after PPPPD might clarify if one strategy is superior to the other.

5. Conclusions

In this study, a double loop alimentary reconstruction assisted by the use of mechanical devices following PPPPD was associated with contained operative time, low incidence of both DGE and pancreatic fistula. Although mortality rate was higher than that reported by referral centres, this technique has been performed in a not specialized unit attaining acceptable results.

Authors contribution

Paolo Limongelli: Participated substantially in conception, design, and execution of the study and in the analysis and interpretation of data; also participated substantially in the drafting and editing of the manuscript.

Antonio D’Alessandro: Participated substantially in conception, design, and execution of the study and in the analysis and interpretation of data.

Simona Parisi: Participated substantially in conception, design, and execution of the study and in the analysis and interpretation of data; also participated substantially in the drafting and editing of the manuscript.

Raffaele Pirozzi: Participated substantially in conception, design, and execution of the study and in the analysis and interpretation of data; also participated substantially in the drafting and editing of the manuscript.

Maria Bondanese: Participated substantially in conception, design, and execution of the study and in the analysis and interpretation of data; also participated substantially in the drafting and editing of the manuscript.

Carmine Colella: Participated substantially in conception, design, and execution of the study and in the analysis and interpretation of data.

Giovanni Docimo: Participated substantially in conception, design, and execution of the study and in the analysis and interpretation of data.

Gianmattia del Genio: Participated substantially in conception, design, and execution of the study and in the analysis and interpretation of data.

Alberto del Genio: Participated substantially in conception,design, and execution of the study and in the analysis and interpretation of data.

Ludovico Docimo: Participated substantially in conception,design, and execution of the study and in the analysis and interpretation of data.

Conflicts of interest

All authors have no conflict of interests.

Sources of funding

All authors have no source of funding.

Ethical approval

This is a retrospective study based only on the analyses of recorded data and then no ethical approval was necessary.