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Ann Thorac Surg 2006;82:1857-1862
© 2006 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Use of Pedicled Omentum in Esophagogastric Anastomosis for Prevention of Anastomotic Leak

M. Akbar Bhat, MS, MCh*, M. Ashraf Dar, MS, Ghulam Nabi Lone, MS, MCh, A. Majid Dar, MCh

Department of Cardiovascular and Thoracic Surgery, Sher-i-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India

Accepted for publication May 31, 2006.

* Address correspondence to Dr Bhat, PB No. 1061, GPO, Srinagar 190001, Jammu and Kashmir, India. (Email: drmakbarbhat{at}yahoo.co.uk; drmakbarbhat{at}gmail.com).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Esophagogastrectomy for carcinoma of the esophagus is the standard surgical treatment for cure or palliation. Esophagogastric anastomotic leakage is a life-threatening postoperative complication, more so if the leakage occurs in the chest.

METHODS: A prospective, randomized study was conducted on 238 patients treated for carcinoma of the esophagus between January 2000 and January 2006. The study excluded 44 patients (18.49%) who were inoperable. The patients were assigned to two treatment groups of 97 each (A and B) according to a restricted permuted block randomization plan. Group A patients underwent esophagogastrectomy with wrapping of the pedicled omentum around the esophagogastric anastomosis. Group B patients underwent esophagogastrectomy without using the omental graft. An Ivor-Lewis type esophagogastrectomy (TTE) was done in 122 patients (62.89%) and a transhiatal esophagogastrectomy (THE) was done in 72 (37.11%).

RESULTS: Anastomotic leaks occurred in 3 group A patients (3.09%) and in 14 (14.43%) group B patients. In group A, 54 patients underwent THE and 43 had TTE, with anastomotic leakage in 2 (3.70%) and 1 (2.33%) patients, respectively. In group B, 48 patients had THE and 49 had TTE, with anastomotic leakage in 8 (16.26%) and 6 (12.24%), respectively. The difference in the incidence of leakage was statistically significant (p = 0.005). There was no complication related to the omental graft technique nor was there a significant difference in the mortality between the two groups.

CONCLUSIONS: The pedicled omental transposition for reinforcing the anastomotic suture line significantly reduces the incidence of leakage after esophagogastrectomy for carcinoma of the esophagus, thus decreasing the morbidity and mortality of the procedure.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Resection for carcinoma of the esophagus or cardia with immediate reconstruction is now considered the standard surgical treatment for cure or palliation [1]. The anastomosis between the residual esophagus and the stomach substitute is made in the chest or in the neck. The prognosis of the patients with carcinoma of the esophagus is poor, but treatment can provide useful palliation by restoring the ability to swallow. It is possible to achieve 5-year survival rates of 43% to 54% in those patients who have had resection for node-negative disease [1–3].

The incidence of anastomotic leakage, although lower, remains significant as reported in the recent literature [4]. The mortality and morbidity also remain high, particularly with intrathoracic anastomotic leaks [4, 5]. Although anastomotic leakage is more frequent with cervical anastomosis than with a chest anastomosis, most of the leaks at the former site heal spontaneously with conservative management [6, 7]. Implicated in anastomotic leakage are anatomic factors such as lack of serosa, inadequate blood supply, and fragile muscle layer lying longitudinally; comorbidities such as diabetes, cirrhosis, and cardiac and pulmonary disorders; and faulty surgical technique, such as tension in suture line, infection or impaired blood supply to esophageal wall [8, 9]. Use of pedicled omentum in the esophagogastric anastomosis has been reported to decrease the incidence of postoperative anastomotic leakage, but its utility has not been evaluated in prospective controlled trials.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Between January 2001 and January 2006, 238 patients with carcinoma of the esophagus were operated on at our institute. Among these, 178 patients (74.79%) had squamous cell carcinoma and 60 (25.21%) had adenocarcinoma. The study excluded 44 patients (18.49%) who were inoperable. Esophagogastrectomy was performed in 194 patients.

The institute's ethics committee approved the study before randomization. Informed consent was obtained from all the patients before surgical intervention. Patients who withheld consent for the omental wrap technique were excluded from the study. A restricted randomization plan was used to randomly assign the patients to two treatment groups (A and B). The patients were randomly assigned to permuted blocks of 4 or 6 patients, such that the number of patients in each group was equal after each block. The length of the permuted blocks was varied randomly to overcome the bias caused by possible prediction of the length of the block.

Group A patients underwent esophagogastrectomy along with reinforcement of the anastomosis with the pedicled omentum. Group B patients underwent esophagogastrectomy without using the omentum around the anastomosis. A manual end-to-side anastomosis was performed in all patients. Ivor-Lewis type transthoracic esophagogastrectomy (TTE) with esophagogastric anastomosis in the chest was done in 122 (62.89%) patients, and 72 (37.11%) had transhiatal esophagogastrectomy (THE) with the esophagogastric anastomosis fashioned in the left side of the neck. Among the patients who had omental wrap around the anastomosis (group A), 43 underwent TTE and 54 patients had THE; whereas in the control group (group B), 49 patients underwent TTE and 48 patients had THE.

The mean age of the patients was 52.5 years. The sex ratio showed a clear male preponderance with male-to-female ratio of 3:1.8. None of the patients had a history of alcoholism, steroid intake, or radiation therapy. One hundred forty-four were smokers, and 32 had given up smoking 1 year before the admission. Fourteen patients had type 2 diabetes mellitus that was controlled with oral hypoglycemic agents, and 35 patients had hypertension that was controlled with antihypertensive drugs. None of the patients had severe pulmonary insufficiency, but 21 patients (12.88%) had moderate pulmonary dysfunction on spirometry defined as vital capacity of less than 50%, a forced expiratory volume in 1 second of less than 70%, and maximum voluntary ventilation of less than 50% of normal.

Exclusion criteria were previous or coexisting cancer, previous gastric or esophageal surgery, neoadjuvent chemotherapy or radiation therapy, recurrent laryngeal nerve palsy, and tumor invading the periesophageal tissues.

All the patients were operated on in consideration with standard procedures for radical surgery. After giving written consent, a restricted randomization plan was used 1 to 3 weeks before surgery to assign the patients to one of the study groups. Two of the 6 surgeons in the department operated all the patients. The surgeons performed esophagogastrectomy with omental wrap (group A) or without omental wrap (group B) according to the randomization process. The surgeon only knew inside the operating theater whether a patient belonged to the study group or the control group.

The surgical procedure in all the patients of the operable group included removal of lymph nodes along the lesser curve, left gastric artery and celiac axis. Forty-four inoperable patients (18.49%), who had unresectable lesions or metastasis to liver, greater omentum, mesentery, or pelvis, or a combination, had exploratory procedures only and were excluded from the study. Because all the patients with stage IV disease were excluded from the study and none of the patients had stage I diseases, all the studied patients either had stage II or stage III carcinoma of the esophagus.

Ninety-two patients (47.42%) underwent subtotal esophagogastrectomy along with intrathoracic esophagogastric anastomosis above the azygos vein. A combined laparotomy and right thoracotomy was used in almost all of these patients (Table 1). In 102 patients (52.58%) who underwent transhiatal esophagogastrectomy, thoracotomy was not performed. Instead, the esophagus was mobilized with blunt dissection, and the pleural spaces were drained by chest-tube thoracostomy if mediastinal pleura were breached during the procedure.


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  		Table 1. Procedures Performed
 
In group A patients, omental mobilization was done such that 4 to 6 cm of omental flap on a base of 6 to 8 cm remained attached to the mobilized stomach on the distal gastroepiploic arcade near the prospective gastric resection line (Fig 1). Because the left gastroepiploic vessels and the gastrosplenic vessels are divided during mobilization of stomach, the pedicled omental flap is perfused by the right gastroepiploic artery.


Figure 1
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  		Fig 1. Line diagram shows technique of harvesting the omental graft. 1 = right gastroepiploic vessels; 2 = omentum; 3 = pedicled omental graft.

 
A Heineke-Mikulicz pyloroplasty and a feeding jejunostomy were performed in all the patients. The newly constructed gastric tube was then carefully guided through the posterior mediastinum to the cervical area (or chest) for anastomosis. A Foley catheter introduced into the gastric tube at the prospective anastomotic site and secured with a purse-string suture aided in the maneuver. The esophagogastric anastomosis was performed end-to-side on the anterior wall of stomach after closure of resection line of the stomach. The anastomosis was performed in single layer by using interrupted 3-0 silk sutures. A Ryles tube was introduced intraoperatively across the esophagogastric anastomosis and into the stomach for postoperative passive suction to avoid bloating and suture line tension. The pedicled omentum was wrapped around the anastomosis and sutured loosely by 5-0 interrupted proline sutures passing through superficial muscular and serosal layers near the anastomotic suture line.

Feeding through the jejunostomy tube was started on postoperative day 3 or 4, once the presence of bowel sounds was confirmed. A water-soluble contrast study was performed in all the patients on postoperative day 6 or 7 to assess the integrity of the neoesophagus before they resumed an oral diet. Operative mortality was calculated on 30-day postoperative period basis.

All patients were followed-up by the operating surgeons at 3-month intervals for the first 3 years after operation and every 4 to 6 months thereafter. The median follow-up of surviving patients was 22 months (range, 3 to 52 months). All the patients underwent chemoradiation protocol after surgery.

The statistical analysis of the data was done by using {chi}2 test and the Fisher exact test. These test statistics were two-sided. Values of p < 0.05 were taken to be statistically significant. The analysis of the data was performed with SPSS 10.0 statistics software (SPSS, Chicago, IL) for Windows (Microsoft Corp, Redmond, WA).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Of 194 patients who had operations, 135 (69.59%) were discharged from hospital within 15 days of surgery. Laparotomy wound infection, which responded to conservative management, developed in 13 patients, who were discharged after 22 ± 2 days. Postoperative atelectasis developed in 23 patients (11.86%), and they were managed conservatively with antibiotics, bronchodilators, and chest physiotherapy. Two patients died of severe pulmonary insufficiency, despite ventilatory support, on postoperative days 8 and 10. Postoperative jaundice developed in 1 patient on postoperative day 4. Ultrasonography revealed sludge in the gallbladder that had not been detected preoperatively. The patient was managed conservatively and was discharged after 23 days of hospital stay.

Nine patients (4.64%) were readmitted with aspiration pneumonia within a week after discharge. All were managed with antibiotics and chest physiotherapy and discharged within next 2 weeks (Table 2).


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  		Table 2. Subset Distribution and Statistical Analysis of Group A and Group B THE and TTE Patients
 
Anastomotic leakage developed in 14 group B patients (14.43%) but occurred in only 3 group A patients (3.09%). In group A, anastomotic leakage occurred in 2 (3.70%) of 54 patients who underwent THE and in 1 (2.33%) of 43 patients who had TTE. In group B, anastomotic leakage occurred in 8 (16.26%) of 48 patients who had THE and in 6 (12.24%) of 49 who had TTE (Table 2). Among the patients who had leakage, 10 had undergone THE, and 7 had undergone TTE. The leakage in the THE group occurred on days 4 to 7 in 8 patients. On postoperative days 10 and 11, leaks developed in 2 patients who were already taking a liquid diet at that time. The leaks in the TTE group were suspected on postoperative day 3 when the chest tube drainage continued to exceed 200 mL per day. Patients in the THE group with were managed conservatively.

Two patients with intrathoracic anastomotic leakage needed reexploration with refashioning of the esophagogastric anastomosis. One died of systemic sepsis 4 days after reexploration for anastomotic leakage. One patient died of perioperative myocardial infarction on postoperative day 2, 1 of intracerebral hemorrhage on day 8, 2 of progressive pulmonary insufficiency on days 8 and 10, despite ventilatory support, and 1 patient died on postoperative day 14 of pulmonary thromboembolism (Table 3). All other patients were discharged 22 ± 6 days postoperatively. The hospital mortality rate was recorded based on a 30-day postoperative period. Three deaths occurred in each study group for a 3.09% mortality rate.


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  		Table 3. Comparative Mortality After Esophagogastrectomy in Patients Undergoing TTE and THE
 
None of the patients had dehiscence of abdomen, chylous leakage, or significant hemorrhage. Anastomotic strictures caused moderate dysphagia in 17 patients (8.76%). Eight patients underwent occasional dilatations for moderate dysphagia, and 9 patients required regular esophageal dilatations. The overall 2-year survival was 47%, and 5-year survival was 23%. Table 4 summarizes the comparative postoperative morbidity and mortality in patients who had transthoracic or transhiatal resection.


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  		Table 4. Comparative Morbidity and Mortality in Patients Undergoing Esophagogastrectomy, with and without Omental Graft Around the Anastomosis
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Successful resection of esophageal cancer is worthwhile: palliation is superior to that obtained with radiotherapy [9], cure is likely for in situ or early lesions [10], and a few patients with carcinoma of the esophagus without lymph node metastasis have a chance for 5-year survival [2, 3]. The difficulty with surgical treatment has been the high postoperative morbidity and mortality directly attributable to pulmonary complications or anastomotic leakage [4, 5, 7].

Pulmonary morbidity of esophagectomy has been associated with increased age, tobacco abuse, malnutrition, host immune deficiency, baseline pulmonary dysfunction, and diminished performance status. Anastomotic leakage remains the most serious complication of esophagogastrectomy [11, 12]. Swallowing disorders (especially in the early postoperative period) and injury to the recurrent laryngeal nerve make the patient prone to aspiration pneumonitis. THE patients are more prone to recurrent laryngeal nerve injury during mobilization of the esophagus in the neck. In the current series, only 10 patients (5.15%) were demonstrated to have laryngeal nerve injury, of which 7 (70%) occurred in THE patients. These have been a major cause of operative deaths and strictures.

The consequences of leaks in the neck are far less disastrous than with those with intrathoracic leaks, where mortality after leaks approaches 50%. A cervical anastomosis carries a higher risk of anastomotic leakage than an intrathoracic anastomosis, but the risk of highly lethal mediastinitis diminishes when leakage occurs [11–14]. Most cervical leaks are subclinical; that is, are only seen radiologically and do not require surgical exploration because they resolve spontaneously 10 to 35 days postoperatively. When surgical drainage is required, opening the cervical incision usually provides sufficient drainage. Only 5 patients in our study needed surgical drainage for the collection in the incision area despite a corrugated rubber drain being present in the cervical incision site.

Anastomotic leakage occurred in 10 patients (13.89%) who had THE and in 7 patients (5.74%) who had TTE (Table 1); however, the difference is not statistically significant (p = 0.589). Various authors have reported similar or higher anastomotic leaks when neck anastomoses were compared with intrathoracic anastomoses [14–16]. Ando and colleagues [11] reported 58 anastomotic leaks (13.8%) in a series of 419 patients studied over a period of 15 years.

Leaks at esophagogastric anastomosis are due to three well-established factors: no serosa, segmental blood supply, and tension [8]. The absence of the serosa makes the watertight suturing of the anastomosis difficult [8]. Various innovative technical modifications have been used to prevent leaks, including stapling devices [8, 17], the Luke well technique, wrapping the anastomosis with stomach, tunnel esophagogastrostomy [14], and wrapping the anastomosis with omental graft [14, 17].

Many authors [14, 17–20] have reported the use of omental graft in the alimentary tract. However, the use of mobilized omentum wrapped around the anastomosis has not been evaluated in a prospective, homogenous patient population. Our clinical experience has proven that anastomotic leakage can be markedly reduced with the help of a pedicled omental graft technique (Table 4).

The omentum has been known as the "policeman of the abdomen" because of its unique role in localizing potentially dangerous inflammatory processes and gastrointestinal perforations. The ability of the omentum to induce neovascularization in areas that are avascular and to function in the presence of established infection makes it a unique structure for preventing esophagogastric anastomotic leaks [17, 19]. Goldsmith [19] successfully patched the intestinal anastomotic defects purposefully left over after esophageal resection with pedicled omentum.

Pedicled omentum rapidly forms adhesions and new blood vessel networks to the underlying tissues, thereby helping in sealing microscopic leaks and in tissue remodeling. The mobile pool of histiocytes, monocytes, and granulocytes in the omentum, by their phagocytic action, contain the local infective process and thereby protect the anastomosis. The omental graft is a very useful adjunct to hand-sewn anastomosis after esophagogastrectomy for carcinoma of the esophagus [20].

In the present study, there was no difference in the mortality between the A and B groups. None of the complications in group A could be ascribed to the use of the omentum (Table 4). The reduction in the anastomotic leakage that occurred in group A patients was not due chance (p = 0.005), indicating the potential utility of omentum to seal microscopic leaks (Table 4).

The subgroup analysis shows that the reduction in the incidence of leaks in group A could not be ascribed to exclusion of THE patients from the study in a significant proportion (Table 2). Comparative statistical analysis of TTE and THE patients in the A and B study arms shows no significant difference in the incidence of leakage (p = 0.598, Tables 2 and 5),Go although there are studies that document higher incidence of leakage in THE patients [21].


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  		Table 5. Comparative Postoperative Mortality and Complications in Patients Who Had Transthoracic and Transhiatal Resection
 
Omentum increases collateral blood flow and induces neovascularization by its lipid angiogenic factor, thus making it an ideal tissue to be used in areas that have a compromised vascular supply [22]. Based on these inferences, we recommend use of pedicled omental transposition for prevention of anastomotic leaks in carcinoma of the esophagus. Only minor modification of the surgical technique is needed while the stomach is mobilized for transposition. Omental transposition should not, however, be used as a false security in situations of technical flaws or compromised bowel vascularity.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Swanson SJ, Batirel HF, Bueno R, et al. Transthoracic esophagectomy with radical mediastinal and abdominal lymph node dissection and cervical esophagogastrostomy for esophageal carcinoma Ann Thorac Surg 2001;72:1918-1924.[Abstract/Free Full Text]
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  18. Liu K, Zhang GC, Cai ZJ. Avoiding anastomotic leakage following esophagogastrectomy J Thorac Cardiovasc Surg 1983;86:142-145.[Abstract]
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