Author Affiliations: 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)

Corresponding Author: 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.

doi: 10.1016/S1499-3872(15)60372-1

Published online May 21, 2015.

 

 

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 first 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 benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

 

 

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

 

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 flaps 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 flap procedure in the prevention of pancreatic fistula and other complications.

 

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

 

CONCLUSIONS: Omental flaps around various anastomoses after pancreaticoduodenectomy can reduce the incidences of pancreatic fistula, biliary fistula, 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)

 

KEY WORDS: pancreaticoduodenectomy; omental flaps; periampullary neoplasms

Pancreaticoduodenectomy, a complex surgical procedure, provides the only chance of cure and long-term survival for patients with periampullary and pancreatic cancers. Pancreatic fistulae are the hallmark of complications after pancreaticoduodenectomy. The incidence of postoperative pancreatic fistula (POPF) after pancreaticoduodenectomy varies from 6.7% to 53.0%.^[1,2] The significant 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 fistula. Although the risk factors for POPF have been identified, 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 filling 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 fluid 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 fistula.^[7] In this study we describe our experience in using omental flaps around the sites of PJ, hepaticojejunostomy (HJ) and duodenojejunostomy (DJ) during pancreaticoduodenectomy to prevent the formation of fistula and other postoperative complications.

 

 

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.

 

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 flaps 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 flap was measured 3-4 cm in width and 8-10 cm in length. The right omental flap 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 omental flap 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 flap 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 first 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.

 

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 firm), biliary infection and pathological diagnosis. Information was also collected on concomitant procedures including portal vein resection. Postoperative data included postoperative complications (appearance of pancreatic fistula, biliary fistula, 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 fistula on or after the third postoperative day with an amylase content greater than 3 times the upper normal serum amylase value;^[10] The pancreatic fistulae were classified into 3 grades as per ISGPF criteria;^[10] (b) The leakage of biliary fluid 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) definition;^[12] (e) The period extending from the first 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 classified 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.

 

Data with continuous variables were presented as mean±standard deviation and compared with the data with a normal distribution using Student's t test. 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). A P value of <0.05 was considered statistically significant.

 

 

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

 

Relevant data on the health status of the patients included information about co-existing pathological factors and biochemical estimations. Group-wise analysis revealed no significant 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.

 

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 significant (all P<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 significant (P<0.001). Statistical significances between the 2 groups included those in pancreatic fistula (P=0.009), hemorrhage after pancreatectomy (P=0.029), biliary fistula (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 profile was significantly lower (P<0.001) in group A. Hospital stay was significantly 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 significant factors that influenced the incidence of pancreatic fistula after pancreaticoduodenectomy (Table 5).

 

 

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 fistula remains as one of the frequent causes of postoperative mortality. The most important pathophysiological factor involved in the pancreatic fistula 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 inflammation caused by pancreatic fistula 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 fistula.^{[17, 18]} Variations in individual experience, anastomosis and drainage influence the formation of pancreatic fistula. Nevertheless, the prevention of pancreatic fistula 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 flap also prevents the catastrophe associated with pancreatic fistula.^{[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 significant 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 fit any defect provide advantages that other flaps 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 influence 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 influence 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 difficult 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 flaps have been used as a protective device in various intestinal^{[19, 21]} and oesophageal^[3] operations. Omental flaps form an effective bridge that covers anastomotic defects during the first 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 flap in between the PJ and portal vein to cover the splanchnic vessels, thus reducing the incidence of post-pancreatectomy hemorrhage but failing to prevent pancreatic fistula. Kapoor et al^[2] used 2 omental flaps for the PJ and DJ and found that only 16% of PJ leaks are associated with omental flap 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 flap group.

 

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

 

Our study revealed that omental wrapping significantly reduced postoperative complications like delayed gastric emptying, biliary fistula formation, and post-pancreatectomy hemorrhage. Omental wrapping not only significantly reduced the incidence of pancreatic fistula, but also facilitated the separation and protection of splanchnic and pancreatic fistulae while preventing pancreatectomy hemorrhage. Similar findings were reported by Seyama et al,^[7] who found that omental graft prevented pancreatic fistula 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 flap must be intact while making the omentum flap. A piece of healthy greater omentum with an adequate blood supply should be taken to form a flap. To avoid pressure on the anastomosis by a hematoma, all bleeding points within the omental flap should be carefully ligated. And while making an omental flap, 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.

 

 

1 Maeda A, Ebata T, Kanemoto H, Matsunaga K, Bando E, Yamaguchi S, et al. Omental flap in pancreaticoduodenectomy for protection of splanchnic vessels. World J Surg 2005;29:1122- 1126. PMID: 16132400

2 Kapoor VK, Sharma A, Behari A, Singh RK. Omental flaps in pancreaticoduodenectomy. JOP 2006;7:608-615. PMID: 17095840

3 Ohwada S, Ogawa T, Kawate S, Koyama T, Yamada T, Yoshimura S, et al. Omentoplasty versus no omentoplasty for cervical esophagogastrostomy following radical esophagectomy. Hepatogastroenterology 2002;49:181-184. PMID: 11941948

4 Bennett WH. A case of perforating gastric ulcer in which the opening being otherwise intractable was closed by means of an omental plug: recovery. Lancet 1896;2:310-311.

5 Zhang QX, Magovern CJ, Mack CA, Budenbender KT, Ko W, Rosengart TK. Vascular endothelial growth factor is the major angiogenic factor in omentum: mechanism of the omentum-mediated angiogenesis. J Surg Res 1997;67:147-154. PMID: 9073561

6 Bikfalvi A, Alterio J, Inyang AL, Dupuy E, Laurent M, Hartmann MP, et al. Basic fibroblast growth factor expression in human omental microvascular endothelial cells and the effect of phorbol ester. J Cell Physiol 1990;144:151-158. PMID: 1694858

7 Seyama Y, Kubota K, Kobayashi T, Hirata Y, Itoh A, Makuuchi M. Two-staged pancreatoduodenectomy with external drainage of pancreatic juice and omental graft technique. J Am Coll Surg 1998;187:103-105. PMID: 9660033

8 Shah OJ, Gagloo MA, Khan IJ, Ahmad R, Bano S. Pancreaticoduodenectomy: a comparison of superior approach with classical Whipple's technique. Hepatobiliary Pancreat Dis Int 2013;12:196-203. PMID: 23558075

9 Sikora SS, Posner MC. Management of the pancreatic stump following pancreaticoduodenectomy. Br J Surg 1995;82:1590- 1597. PMID: 8548218

10 Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 2005;138:8-13. PMID: 16003309

11 Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, 1999. Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol 1999;20:250-280. PMID: 10219875

12 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;142:20-25. PMID: 17629996

13 Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2007;142:761-768. PMID: 17981197

14 Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240: 205-213. PMID: 15273542

15 Choi SB, Park SW, Kim KS, Choi JS, Lee WJ. The survival outcome and prognostic factors for middle and distal bile duct cancer following surgical resection. J Surg Oncol 2009;99:335- 342. PMID: 19226533

16 van Berge Henegouwen MI, Allema JH, van Gulik TM, Verbeek PC, Obertop H, Gouma DJ. Delayed massive haemorrhage after pancreatic and biliary surgery. Br J Surg 1995;82:1527-1531. PMID: 8535810

17 Friess H, Malfertheiner P, Isenmann R, Kühne H, Beger HG, Büchler MW. The risk of pancreaticointestinal anastomosis can be predicted preoperatively. Pancreas 1996;13:202-208. PMID: 8829190

18 Hamanaka Y, Nishihara K, Hamasaki T, Kawabata A, Yamamoto S, Tsurumi M, et al. Pancreatic juice output after pancreatoduodenectomy in relation to pancreatic consistency, duct size, and leakage. Surgery 1996;119:281-287. PMID: 8619183

19 Agnifili A, Schietroma M, Carloni A, Mattucci S, Caterino G, Lygidakis NJ, et al. The value of omentoplasty in protecting colorectal anastomosis from leakage. A prospective randomized study in 126 patients. Hepatogastroenterology 2004;51: 1694-1697. PMID: 15532807

20 Adams W, Ctercteko G, Bilous M. Effect of an omental wrap on the healing and vascularity of compromised intestinal anastomoses. Dis Colon Rectum 1992;35:731-738. PMID: 1379531

21 Nikfarjam M, Kimchi ET, Gusani NJ, Shah SM, Sehmbey M, Shereef S, et al. A reduction in delayed gastric emptying by classic pancreaticoduodenectomy with an antecolic gastrojejunal anastomosis and a retrogastric omental patch. J Gastrointest Surg 2009;13:1674-1682. PMID: 19548039

22 Fix RJ, Vasconez LO. Use of the omentum in chest-wall reconstruction. Surg Clin North Am 1989;69:1029-1046. PMID: 2781445

23 Schmidt CM, Turrini O, Parikh P, House MG, Zyromski NJ, Nakeeb A, et al. Effect of hospital volume, surgeon experience, and surgeon volume on patient outcomes after pancreaticoduodenectomy: a single-institution experience. Arch Surg 2010;145:634-640. PMID: 20644125

24 Collins D, Hogan AM, O'Shea D, Winter DC. The omentum: anatomical, metabolic, and surgical aspects. J Gastrointest Surg 2009;13:1138-1146. PMID: 19291335