Omental faps reduces complications after pancreaticoduodenectomy

Kashmir, India

Omental faps reduces complications after pancreaticoduodenectomy

Omar J Shah, Sadaf A Bangri, Manmohan Singh, Reyaz A Lattoo and Mohammad Y Bhat

Kashmir, India

BACKGROUND: Major complications after pancreaticoduodenectomy are usually caused by a leaking pancreaticojejunal anastomosis. Omental faps around various anastomoses were used to prevent the formation of fstula.

METHODS: We reviewed 147 patients who had undergone pancreaticoduodenectomy between March 2006 and March 2012. The patients were divided into 2 groups according to the application of omental faps around various anastomoses: group A (101 patients) who underwent omental wrapping procedure; group B (46 patients) who did not undergo the omental wrapping procedure. Perioperative data of the two groups were reviewed to assess the effectiveness of omental fap procedure in the prevention of pancreatic fstula and other complications.

RESULTS: No differences were observed in the clinical characteristics between the 2 groups. The incidences of pancreatic fstula (4.0% vs 17.4%), post-pancreatectomy hemorrhage (0 vs 6.5%), biliary fstula (1.0% vs 13.0%), and delayed gastric emptying (4.0% vs 17.4%) were signifcantly less frequent in group A. The overall morbidity (18.8% vs 47.8%) and hospital stay (8.3 vs 9.6 days) were also signifcantly lower in group A than in group B.

CONCLUSIONS: Omental faps around various anastomoses after pancreaticoduodenectomy can reduce the incidences of pancreatic fstula, biliary fstula, post-pancreatectomy hemorrhage and delayed gastric emptying. This procedure is simple and effective to reduce the overall morbidity after pancreaticoduodenectomy.

(Hepatobiliary Pancreat Dis Int 2015;14:313-319)

pancreaticoduodenectomy; omental faps; periampullary neoplasms

Introduction

Pancreaticoduodenectomy, a complex surgical procedure, provides the only chance of cure and longterm survival for patients with periampullary and pancreatic cancers. Pancreatic fstulae are the hallmark of complications after pancreaticoduodenectomy. The incidence of postoperative pancreatic fstula (POPF) after pancreaticoduodenectomy varies from 6.7% to 53.0%.[1,2]The signifcant risk factors including soft pancreatic parenchyma, small pancreatic duct size, requirement of blood transfusion, postoperative bleeding and older age are related to the formation of pancreatic fstula. Although the risk factors for POPF have been identifed, no consensus has been reached on the best method for reconstructing the pancreatic enteric anastomosis to reduce the incidence of POPF. Thus, efforts should be made to lower the incidence of POPF and improve the outcome of the patient.

The omentum plays a role in reconstructive procedures. In thoracic surgery, the omental tissue is used widely for flling the dead spaces while dealing with chronic empyema, mediastinits and chest wall defects after resection and also for strengthening a main bronchial stump after failure of a pneumonectomy. In abdominal surgery, Ohwada et al[3]reported that omental wrapping after cervical oesophagogastrostomy and radical oesophagectomy reduced anastomotic leak. Bennett[4]used the omentum to plug a perforated gastric ulcer. The omentum is believed to deliver vascular endothelial growth factor which accelerates neovascularization across anastomotic lines.[5,6]It is known to assist healing of surgical wounds besides promoting serosal fuid re-absorption and macrophagic migration in septic foci.

In pancreatic surgery, omental wrapping of pancreaticojejunostomy (PJ) anastomosis has been applied to prevent the formation of pancreatic fstula.[7]In this study we describe our experience in using omental faps around the sites of PJ, hepaticojejunostomy (HJ) and duodenojejunostomy (DJ) during pancreaticoduodenectomy to prevent the formation of fstula and other post-operative complications.

Methods

Patients

The records of 153 patients who had been subjected to pancreaticoduodenectomy for periampullary malignancy at our institute between March 2006 and March 2012 were retrospectively analyzed. Of these patients, 6 who had undergone a two-stage pancreaticoduodenectomy or total pancreatectomy were excluded from the study. The remaining 147 patients were divided into two groups： group A comprised 101 patients who had undergone pancreaticoduodenectomy from October 2008 to March 2012 and group B included 46 patients who had undergone pancreaticoduodenectomy from March 2006 to September 2008. Patients in group A received omental wrapping around the anastomotic sites, and those in group B did not.

Surgical technique

Fig. 1.Sketch demonstrating omental vessels and dotted line showing the plain of dissection for making three omental flaps. St： stomach; GEA： gastroepiploic arcade; AOV： accessory omental vessel; Rt OV： right omental vessel; MOV： middle omental vessel; Lt OV： left omental vessel.

Fig. 2.Operative photograph showing three omental flaps for wrapping around anastomoses of hepaticojejunostomy (HJ), pancreaticojejunostomy (PJ) and duodenojejunostomy (DJ).

Fig. 3.Operative photograph demonstrating omental faps rolled around anastomoses of hepaticojejunostomy (HJ), pancreaticojejunostomy (PJ) and duodenojejunostomy (DJ). Col： colon; St：stomach.

All patients were subjected to pylorus preserving pancreaticoduodenectomy (PPPD) through the superior approach.[8]After resection, reconstruction was accomplished by a single loop of the jejunum via all types of anastomoses in all patients. PJ was performed by the end-to-end dunking method as described by Sikora and Posner.[9]HJ was carried out by the end-to-side method. In all patients, DJ (end-to-side method) was done in an antecolic fashion： 3 pedicle omental faps were used by dividing the greater omentum longitudinally over an avascular area and at the same time preserving 1 or 2 omental branches of gastroepiploic vessels (Figs. 1, 2). Each omental fap was measured 3-4 cm in width and 8-10 cm in length. The right omental fap was pulled and wrapped loosely around HJ anastomosis and kept in place by a few stitches connecting the omentum and the seromuscular layer of the jejunum. The middle omen-tal fap was pulled between the posterior surface of PJ and the portal vein and rolled over the anterior surface of PJ. The rolled up omentum was anchored by a few silk stitches. The left omental fap was wrapped loosely around the DJ anastomosis in a circumferential manner and held in place by a few interrupted sutures (Fig. 3). A surgical drain was inserted near the PJ anastomosis and exteriorized on the right side of abdominal wall. The nasogastric tube was removed on the frst postoperative day and oral feeding was started when the patient showed a good recovery. Apart from omental wrapping which was exclusively performed in group A, the operative procedure was similar in both groups. No patient received prophylactic octreotide. This study was approved by the Institutional Review Board of SKIMS and informed consent was obtained from all the patients. All of the surgical procedures were performed by senior pancreatic surgeons assisted by 3 other surgeons.

Perioperative data collection

Preoperative data collected from both groups of patients included information on age, gender, liver function test (LFT) results, body mass index (BMI), the American Society of Anesthesiologists (ASA) scoring, presence or absence of preoperative biliary drainage and presence of comorbidity if any. Intraoperative data comprised information on the type of pancreaticoduodenectomy performed, operative time, operative blood loss, intraoperative blood transfusion, pancreatic duct diameter (at cut margin of the pancreas), pancreatic texture (soft, intermediate or frm), biliary infection and pathological diagnosis. Information was also collected on concomitant procedures including portal vein resection. Postoperative data included postoperative complications (appearance of pancreatic fstula, biliary fstula, postoperative hemorrhage and delayed gastric emptying), in-hospital mortality, re-operation, and re-admission.

The purposes of this study were as follows： (a) The drain output of any measurable volume was treated as pancreatic fstula on or after the third postoperative day with an amylase content greater than 3 times the upper normal serum amylase value;[10]The pancreatic fstulae were classifed into 3 grades as per ISGPF criteria;[10](b) The leakage of biliary fuid with high bilirubin content exceeding 3 times the serum level and lasting for more than 5 days was considered as bile leakage; (c) Culture positive purulent collection and wound infection as per surgical site infection (SSI) guidelines were pronounced as intra-abdominal abscess;[11](d) Hemorrhage occurring in less than 24 hours after the index operation was described as early and that occurring after 24 hours was treated as late post-pancreatectomy hemorrhage as per International Study Group of Pancreatic Surgery (ISGPF) defnition;[12](e) The period extending from the frst postoperative day until the day of discharge from the hospital determined the length of hospital stay; (f) Deaths occurring within the hospital admission period or within 30 days after surgery were counted for postoperative mortality; and (g) when nasogastric tube was continued for 3 postoperative days or a need arose for its reinsertion after the third postoperative day or when the patient was unable to digest solid food after the seventh postoperative day, it was pronounced as delayed gastric emptying.[13]

Postoperative complications were classifed as per Clavien and Dindo criteria.[14]The primary study end point was the presence or absence of POPF. The secondary end points were the overall complication rate, length of hospital stay and operative mortality.

Statistical analysis

Data with continuous variables were presented as mean±standard deviation and compared with the data with a normal distribution using Student'sttest. Categorical variables were compared using the Chi-square test or Fisher's exact test as appropriate, and logistic regression was used for univariate analysis. Statistical analysis was made using SPSS version 20.0 (SPSS Inc., Chicago, IL, USA). APvalue of <0.05 was considered statistically signifcant.

Results

Clinicopathological characteristics

The characteristics of the 2 groups of patients included mean age, male/female ratio, BMI value and ASA score. These characteristics were not statistically signifcant (Table 1).

Relevant data on the health status of the patients included information about co-existing pathological factors and biochemical estimations. Group-wise analysis revealedno signifcant difference between the two groups (Table 2). In the 2 groups of patients, 64.4% suffered from pancreatic cancer, 34.7% from ampullary cancer, 12.9% from distal cholangiocarcinoma, and 8.2% from duodenal adenocarcinoma.

Table 1.Variables of the two groups

Perioperative results

Intraoperative data indicated that the pathological distribution was similar in the 2 groups except for operative time, operative blood loss and blood transfusion requirement, which were lower in group A (Table 3). These differences between the two groups were statistically signifcant (allP<0.001).

Relevant data on postoperative complications determined the morbidity of the 2 groups (Table 4). The variation in overall morbidity of patients, which was 18.8% in group A and 47.8% in group B, was statistically signifcant (P<0.001). Statistical signifcances between the2 groups included those in pancreatic fstula (P=0.009), hemorrhage after pancreatectomy (P=0.029), biliary fstula (P=0.004), delayed gastric emptying (P=0.009), and intra-abdominal abscess (P=0.091). Whereas the difference of mortality was not statistically different in the 2 groups, the overall morbidity profle was signifcantlylower (P<0.001) in group A. Hospital stay was signifcantly shorter in group A compared with group B (8.3± 2.8 vs 9.6±3.7,P<0.05). For management, data of POPF and postoperative pancreatic hemorrhage (POPH) refer to the cascade (Fig. 4). There were 3 (2.0%) deaths in this series： 2 deaths (1-POPF, 1-POPH) in group B and 1 death in group A because of postoperative myocardial infarction. Univariate analysis revealed that BMI >25 kg/ m2, serum bilirubin >10 mg/dL, ASA (III/IV), preoperative biliary stenting, soft pancreas, pancreatic duct diameter≤3 mm, operative time, omental wrapping, intra-abdominal infections, delayed gastric emptying, re-operation and length of hospital stay were statistical signifcant factors that infuenced the incidence of pancreatic fstula after pancreaticoduodenectomy (Table 5).

Table 2.Variables of the two groups before operation

Table 3.Intraoperative variables of the two groups

Table 4.Postoperative conditions of the two groups (n, %)

Fig. 4.Cascade depicting management of cases of POPF and POPH. POPF： postoperative pancreatic fstula; POPH： postoperative pancreatic hemorrhage.

Table 5.Univariate analysis of factors associated with postoperative pancreatic fstula

Discussion

Pancreaticoduodenectomy is a technically demanding intervention associated with substantial postoperative morbidity and mortality. However, recent advances in surgical techniques and appropriate management of postoperative complications have improved clinical outcome. The postoperative mortality after pancreaticoduodenectomy has decreased to 5%.[15]However, pancreatic fstula remains as one of the frequent causes of postoperative mortality. The most important pathophysiological factor involved in the pancreatic fstula is the leakage of pancreatic juice which is rich in proteases, causes digestion of tissues and leads to partial or complete anastomotic dehiscence. Moreover, local infammation caused by pancreatic fstula sometimes erodes the wall of a major vessel near the pancreatic bed resulting in formation of pseudoaneurysm and/or sloughing of an arterial stump.[16]

Pancreatic tissue consistency, exocrine function of pancreatic remnant and diameter of the pancreatic duct are important determinants of pancreatic fstula.[17,18]Variations in individual experience, anastomosis and drainage infuence the formation of pancreatic fstula. Nevertheless, the prevention of pancreatic fstula has been a major concern with pancreatic surgeons. Several attempts have been made to reduce this avoidable complication; the use of omental wrap around the anastomosis area is promising. This method prevents anastomotic leak and also provides a source of granulation tissue and neovascularization for prompt healing.[19,20]Additionally by protecting major vessels, omental fap also prevents the catastrophe associated with pancreatic fstula.[1,2]Another complication is delayed gastric emptying. The interposition of antecolic gastrojejunal anastomosis distances the principal anastomosis from the pancreas and thereby minimizes the possibility of jejunal kinking or angulation, which allows greater mobility of the stomach and jejunum and therefore prevents delayed gastric emptying. An omental roll around the anastomosis separates the anastomosis from the PJ and reduces the possibility of an associated pancreatic leak. It also promotes neovascularization of the anastomosis which in turn can reduce the chances of ischemia. The decreased incidence of delayed gastric emptying and various types of leaks observed with omental wrapping technique lead to a shorter hospital stay and virtually prevent hospital re-admission. Nikfarjam et al[21]performed a classic pancreaticoduodenectomy combined with antecolic anastomosis and retrogastric vascular omental patch and achieved a signifcant reduction in delayed gastric emptying and the related hospital readmission. However, the role of vascular omental patch was not elucidated in that study.

The omentum has proved to be an organ of exceptional versatility. Its ample blood supply, its angiogenic and immunogenic properties, its ease of harvesting, and its property of malleability to ft any defect provide ad-vantages that other faps do not have.[22]The omentum is rich in vascular and lymphatic plexuses and possesses great mobility. It can easily adhere to a site of contamination or injury within the peritoneal cavity. Besides contributing to neovascularization, it increases oxygen tension in tissues. It participates directly in containment of bacterial infection, in the transport of phagocytes, and in the absorption of foreign material.

The potential infuence of learning curve might exist in the present study given the longitudinal nature of data capture. The sole surgeon involved in this study was beyond 60 independent cases at the commencement of data collection for this analysis. Studies examining the infuence of the learning curve on pancreaticoduodenectomy outcomes conclude that it generally requires up to 60 cases before a surgeon plateaus and outcomes become equivalent to those obtained by more experienced surgeons.[23]Moreover, it is diffcult to improve outcomes once reaching the standard of a high-volume pancreatic surgeon.[23]Therefore, learning curve might not affect the outcome of this cohort.

Omental faps have been used as a protective device in various intestinal[19,21]and oesophageal[3]operations. Omental faps form an effective bridge that covers anastomotic defects during the frst 48 hours after surgery and provides a bulk of granulation tissue thereafter.[20]In a series of 100 patients, Maeda et al[1]placed omental fap in between the PJ and portal vein to cover the splanchnic vessels, thus reducing the incidence of postpancreatectomy hemorrhage but failing to prevent pancreatic fstula. Kapoor et al[2]used 2 omental faps for the PJ and DJ and found that only 16% of PJ leaks are associated with omental fap and that a mortality of 80% in the non-omental group was related to PJ leak. There was no major vascular bleeding in the omental fap group.

In studies on omental fap for PJ anastomosis, some reported the successful use of additional omental fap for DJ anastomosis. Besides using omental faps for PJ and DJ cases, we have introduced the use of a third omental fap for HJ site.

Our study revealed that omental wrapping signifcantly reduced postoperative complications like delayed gastric emptying, biliary fstula formation, and postpancreatectomy hemorrhage. Omental wrapping not only signifcantly reduced the incidence of pancreatic fstula, but also facilitated the separation and protection of splanchnic and pancreatic fstulae while preventing pancreatectomy hemorrhage. Similar fndings were reported by Seyama et al,[7]who found that omental graft prevented pancreatic fstula and intra-abdominal infection and reduced postoperative mortality.

This study may highlight the role of vascularized omental graft in reducing postoperative morbidity of patients after pancreaticoduodenectomy and their hospital stay and cost. However, surgeons should recognize that the vascular net in the greater omentum does not have a uniform distribution pattern in all cases.[24]Hence the main vessels offering blood supply to the pedicled greater omentum fap must be intact while making the omentum fap. A piece of healthy greater omentum with an adequate blood supply should be taken to form a fap. To avoid pressure on the anastomosis by a hematoma, all bleeding points within the omental fap should be carefully ligated. And while making an omental fap, caution should be taken to prevent bleeding from capillaries, which may otherwise lead to the formation of tardous hematoma. The anastomosis should not be wrapped tightly to avoid hampering of blood circulation and stenosis of the anastomosis.

Acknowledgements:We thank Rayees A Dar, Statistician SKIMS, for providing the statistical analysis for this paper.

Contributors:SOJ proposed the study. SOJ, BSA and SM performed research and wrote the frst draft. LRA and BMY collected and analyzed the data. All authors contributed to the design and interpretation of the study and to further drafts. SOJ is the guarantor.

Funding:None.

Ethical approval:This study was approved by the Institutional Review Board of SKIMS and informed consent was obtained from all the patients.

Competing interest:No benefts in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

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Received August 15, 2014

Accepted after revision March 5, 2015

AuthorAffliations:Department of Surgical Gastroenterology, Sher-i-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India (Shah OJ, Bangri SA, Singh M, Lattoo RA and Bhat MY)

Omar J Shah, MS, FICS, Kral-Sangri, Brein, Nishat, Srinagar, Kashmir, India (Tel/Fax： +91-0194-2471898; Email： omarjshah@ yahoo.com)

© 2015, Hepatobiliary Pancreat Dis Int. All rights reserved.

10.1016/S1499-3872(15)60372-1

Published online May 21, 2015.