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Braun enteroenterostomy during pancreaticoduodenectomy decreases postoperative delayed gastric emptying Bin Xu, M.D.a,b, Hongbo Meng, M.D.a, Mingping Qian, M.D.a, Haijiang Gu, M.D.b, Bo Zhou, M.D.a,*, Zhenshun Song, M.D.a,* a

Department of General Surgery, Shanghai Tenth People’s Hospital, Tongji University School of Medicine, 301 Yanchang Road, Shanghai 200072, China; bDepartment of General Surgery, Shuangjiang Autonomous County People’s Hospital, Lincang, Yunnan Province 677300, China

KEYWORDS: Pancreaticoduodenectomy; Delayed gastric emptying; Braun enteroenterostomy; Child reconstruction; Pancreatic cancer

Abstract BACKGROUND: Modified digestive reconstruction during pancreaticoduodenectomy (PD) may affect the postoperative incidence of delayed gastric emptying (DGE). The purpose of this study is to investigate whether Braun enteroenterostomy following PD can reduce the incidence of DGE. METHODS: Four hundred seven patients who received PD with child reconstruction from June 2000 to March 2013 were divided into 2 groups: 206 patients with Braun enteroenterostomy (Child-Braun group) and 201 patients without Braun enteroenterostomy (Child-non-Braun group). Clinical data were retrospectively extracted; univariate and multivariate analyses were performed to investigate the association between Braun enteroenterostomy and DGE. RESULTS: DGE was less frequent in the Child-Braun group than in the Child-non-Braun group (6.7% vs 26.87%, P , .001). The multivariate logistic regression analysis showed that Braun enteroenterostomy was the only significant independent factor associated with the reduced DGE after PD with Child reconstruction, with an odds ratio of 4.485 (95% confidence interval: 2.372 to 8.482, P , .001). CONCLUSION: Braun enteroenterostomy reduces the incidence of postoperative DGE associated with PD. Ó 2014 Elsevier Inc. All rights reserved.

Pancreaticoduodenectomy (PD) is the standard and effective treatment for pancreatic cancer and periampullary adenocarcinoma, but the incidence of postoperative The authors declare no conflicts of interest. Supported by the National Natural Science Foundation of China (81001007) and the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry (SRF for ROCS, SEM). * Corresponding authors. Tel.: 186-021-66307347; fax: 186-02166307405. E-mail addresses: [email protected], [email protected] Manuscript received November 27, 2013; revised manuscript April 8, 2014 0002-9610/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2014.06.035

complications remains high, up to 60%.1 Postoperative pancreatic fistula (POPF) and delayed gastric emptying (DGE) are the 2 most troublesome complications. DGE is a paresis (partial paralysis) of the stomach, resulting in food remaining in the stomach for a longer time than normal. DGE is not a fatal complication after PD, but it may significantly prolong the hospital stay and increase the hospitalization cost.2 Because DGE symptoms may be misunderstood among patients and their families, in China the incidence of medical complications may well be higher in DGE patients than in those without DGE. The reported incidence of DGE is 38% to 57%.3–5

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Therefore, a high priority for surgeons is the search for ways to reduce DGE after PD. Several factors may contribute to the frequency and severity of DGE after PD: gastric dysrhythmias because of intra-abdominal complications,6,7 obstruction of the reconstructed alimentary tract,8 surgical technique,3,6,9,10 and continuous enteral nutrition.4 The method of alimentary reconstruction of duodenojejunostomy or gastrojejunostomy strongly influences the occurrence of DGE. Some authors11,12 have reported a lower incidence of DGE after Braun reconstruction or Roux-en-Y reconstruction, but others have found no difference in incidence between either of the 2 procedures following PD and classic PD.3 Until now, few articles with very small sample size have focused on the influence of Braun anastomosis (between the afferent and efferent jejunal loops) following PD on the incidence of DGE. Thus, the objective of our study was to determine the clinical impact of Braun enteroenterostomy on the occurrence of DGE after PD.

reconstruction with added Braun enteroenterostomy in distal gastrectomy for gastric cancer, and concluded that the added Braun procedure probably resulted in better patients’ recovery and less DGE. Thus, from April 2009 to March 2013, we performed a Braun enteroenterostomy as part of the PD operation in 201 patients. Altogether there were 259 men and 159 women in our series, with an average age of 58.0 6 11.03 years. Diseases included 161 pancreatic cancers, 27 pancreatic cystadenomas and cystadenocarcinomas, 39 bile duct cancers, 18 intraductal papillary mucinous neoplasms, 109 ampullary or duodenal cancers, 14 neuroendocrine tumors or carcinoid tumors, 1 gallbladder or cystic duct cancer, 6 pancreatic solid pseudopapillary tumors, 4 gastrointestinal stromal tumors, 1 metastatic cancer, 11 cases of pancreatitis or autoimmune diseases, 1 common bile duct adenoma, 4 duodenal adenomas, and 22 other diseases. Review of patients’ records was approved by our hospital’s institutional review board.

Patients and Methods Clinical data Data of 418 patients who had undergone PD between June 2000 and March 2013 were retrospectively retrieved by chart review. The first 217 patients, operated from June 2000 to March 2009, had a standard antecolic gastroenterostomy with PD. Those patients had a high incidence of DGE. By communication with other surgeons, we realized that the addition of Braun enteroenterostomy might decrease the incidence of postoperative DGE. We also retrospectively reviewed our data on Billroth Ⅱ reconstruction or Billroth Ⅱ

Pancreaticoduodenectomy procedures The following PD procedures were performed: distal gastrectomy, resection of the duodenum, removal of the gallbladder and common bile duct, removal of the lesion, and resection of the pancreatic head, neck, and uncinate process. Standard PD was performed in 418 patients: 201 cases with Child reconstruction (Fig. 1A), 206 cases with Child reconstruction plus Braun jejunojejunostomy after gastrojejunostomy (Fig. 1B), and 11 cases with Cattell reconstruction with Braun jejunojejunostomy (Fig. 1C). The jejunum was brought up to do pancreatojejunostomy and bilioenteric anastomosis in a retrocolic manner through a defect created in the colon mesentery. Double-layer

Figure 1 Pancreaticoduodenectomy with different digestive reconstructions. A, Child reconstruction; B, Child reconstruction plus Braun jejunojejunostomy after gastrojeunostomy; C, Cattell reconstruction with Braun jejunojejunostomy.

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Braun enteroenterostomy reduces DGE

pancreatojejunostomy was performed with the dunking method and gastrojejunostomy was performed in an antecolic manner in all patients. Prophylactic jejunostomy tubes were used only in severely malnourished patients, when need for extra nutritional requirements was anticipated.

Postoperative management A drain was inserted behind the bilioenteric anastomosis and beside the pancreatojejunostomy. The drainage fluid was intermittently suctioned. The nasogastric tube was removed after recovery of intestinal function. The gastric tube was reinserted if the patient complained of nausea and vomiting, and/or if severe distention of the stomach was observed on abdominal radiographs. Postoperative treatments included antibiotics, gastric acid inhibitors, water–electrolyte balance, nutritional support, and palliative treatments.

Definition of outcome measures POPF was defined as amylase concentration in the drain fluid, obtained on or after postoperative day (POD) 3, greater than 3 times the upper range of serum amylase concentration.13 POPF was classified into 3 grades: grade A, a transient fistula with patient in good condition; grade B, fistula leading to infections requiring persistent drainage; and grade C, fistula resulting in bad prognosis and reoperation. A grade B or C fistula was considered as clinically relevant POPF. We applied the definition of DGE after pancreatic surgery suggested by the International Study Group of Pancreatic Surgery (ISGPS)14 DGE was graded as follows: grade A, inability to tolerate solid oral intake by POD 7 and usually without vomiting; grade B, inability to tolerate solid oral intake by POD 14 with/without vomiting; and grade C, inability to tolerate solid oral intake by POD 21 with/without vomiting. DGE grade A defined by the ISGPS14 results in only a transient variation in the standard postoperative course of patients after pancreatic surgery, has no major clinical impact, and leads only to a slight deviation of the clinical pathway. In the studies of Sakamoto et al3 and Nikfarjam et al,11 grade A was not considered to be a clinically relevant complication because it could be affected by the timing of serving food, which was influenced by the surgeon’s preference, and the time of removing the nasogastric tube (based on recovery of intestinal function) also was subjective and arbitrary. Moreover, DGE grade A is not associated with a major delay in the patient’s hospital discharge.14 Therefore, we considered only grade B and C DGE to be clinically relevant complications. Other complications were defined according to the classification of Dindo et al.15

Statistical analysis Statistical analysis was performed using SPSS 13.0 for windows. All continuous data were presented as mean 6

3 standard deviation. Categorical variables were compared by the chi-square test or Fisher’s exact test. The independent samples t-test was used to compare the means of the 2 groups. Logistic regression analysis was performed to identify independent risk factors. P less than .05 was considered to be statistically significant.

Results Clinical results A total of 418 patients underwent PD. Their mean age was 58 years (95% confidence interval [CI]: 56.96 to 59.08). Perioperative mortality, defined as death within 30 days after operation, was 1.20%. Intra-abdominal infections occurred in 33 patients (7.9%): 15 in noneDGE group and 18 in DGE group. The overall incidence of postoperative complications, excluding grade A DGE, was 41.6%; details of the postoperative complications are summarized in Table 1. Anastomotic leaks, DGE, wound infections, and intra-abdominal infections accounted for most of the perioperative complications. Leakage from the pancreatic anastomosis occurred in 20.1% of patients and DGE (grade B or C) occurred in 16.3%. Reoperation was done in 2.2% of patients. Overall mean hospital stay was 18.5 6 10.5 days. Mean postoperative hospital stay of patients without clinically relevant DGE (non–CR-DGE group) was shorter than that of patients with CR-DGE (grades B and C, CR-DGE group) (15.7 6 6.90 vs 31.3 6 15.1, P , .01). There was no significant difference in perioperative mortality between the non–CR-DGE group and the CR-DGE group (1.14% vs

Table 1 patients

Summary of postoperative complications of 418 PD

Complication

n

Frequency (%)

Postoperative pancreatic fistula Grade A Grade B Grade C Delayed gastric emptying Grade A Grade B Grade C Bile leakage Wound infection Postoperative bleeding Intra-abdominal bleeding Digestive tract bleeding Others Pneumonia Intra-abdominal infection Diarrhea Urinary tract infection Reoperation

84 33 41 10 227 159 18 50 20 36 32 6 19 7 15 33 9 10 9

20.10 7.90 9.80 2.40 54.31 38.03 4.30 11.96 4.78 8.61 7.65 1.43 4.54 1.67 3.58 7.89 2.15 2.39 2.15

PD 5 pancreaticoduodenectomy.

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1.47%, P 5 .82). The mean time of removal of gastric tubes in DGE groups A, B, and C and non-DGE group was 4.51, 18.72, 33.06, and 3.52 days, respectively. Statistical evaluation regarding the mean time of removal of gastric tubes was as follows: mean time in DGE grade C group greater than mean time in DGE grade B group greater than mean time in DGE grade A group or non-DGE group. There was no significant difference between DGE grade A group and non-DGE group concerning the mean time of gastric tube removal. Details were outlined in Supplementary Tables 1 and 2.

grade of POPF, bile leakage, and digestive reconstruction (non-Braun or Braun) (Table 2). Higher clinically relevant POPF (grades B and C) was identified more frequently in the CR-DGE group than in the non–CR-DGE group (25.3% vs 9.71%, P 5 .001). Multivariate analysis was then performed using the significant factors from the univariate analysis. It revealed that clinically relevant POPF and bile leakage were not independent risk factors for CR-DGE, whereas digestive reconstruction (non-Braun or Braun) was the only independent risk factor (Table 3), with an odds ratio of 4.485 (95% CI: 2.372 to 8.482, P , .001) in patients who had undergone classical PD with Child reconstruction and 4.746 (95% CI: 2.513 to 8.963, P , .001) in all PD patients.

Univariate and multivariate analysis of risk factors for clinically relevant delayed gastric emptying The univariate analysis of risk factors for CR-DGE was performed using the following clinicopathological variables: age, sex, diabetes mellitus, disease (pancreatic cancer vs others), size of the main pancreatic duct (R3 and ,3 mm), surgical procedures (Child or Cattell), digestive reconstruction (non-Braun or Braun), operative time, intraoperative blood loss, and the grade of POPF. Univariate analysis showed that there were no differences in sex, disease, surgical procedures, operative time, or intraoperative blood loss between the CR-DGE group and the non–CR-DGE group, but DGE was associated with the

Table 2

Braun anastomosis reduced delayed gastric emptying Gastrojejunostomy was performed in an antecolic manner in all patients. To eliminate the influence of different types of PD on the incidence of DGE, further analysis was performed in 407 patients who underwent classical PD with Child reconstruction. They were divided into 2 groups: classical PD with Child reconstruction but no Braun anastomosis (Child-non-Braun group) and classical PD with Child reconstruction plus Braun anastomosis (Child-Braun group). There was no significant difference

Univariate analysis of risk factors for CR-DGE (grades B and C)

Characteristics Sex Male Female Age (years) Diabetes mellitus Disease Pancreatic cancer Others Surgical procedures Child Cattell Digestive reconstruction Non-Braun Braun MPD (S3 mm) Operating time (hours) Estimated blood loss Pancreatic leakage (POPF) Grade A Grade B Grade C Bile leakage Postoperative GI bleeding Intra-abdominal bleeding

CR-DGE group (n 5 68)

Non-CR-DGE group (n 5 350)

39 29 58.65 6 9.93 6

220 130 57.89 6 11.25 35

23 45

138 212

68 0

339 11

54 14 9 4.37 6 .86 330.75 6 240.54

147 203 72 4.58 6 1.41 323.34 6 316.47

9 12 5 7 4 1

24 29 5 13 12 5

Statistical value (t/c2)

P value

.732

.392

2.514 .089 .755

.607 .765 .382

2.195

.224

31.92

,.001*

1.961 1.185 .220 19.72

.161 .237 .826 .001*

5.411 .931 .001

.020* .335 .979

CR-DGE 5 clinically relevant delayed gastric emptying; GI 5 gastrointestinal; MPD 5 main pancreatic duct; POPF 5 postoperative pancreatic fistula. *P , .05.

B. Xu et al. Table 3

Braun enteroenterostomy reduces DGE

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Multivariate logistic regression to seek independent risk factors for DGE (grades B and C)

Variables

Wald

Clinically relevant POPF Group A Group B Bile leakage Group A Group B Digestive reconstruction Group A Group B

Odds ratio

95% CI

P value

3.517 3.575

1.949 1.963

.970–3.916 .976–3.949

.061 .059

1.938 1.869

2.092 2.061

.740–5.914 .731–5.814

.164 .172

23.041 21.313

4.746 4.485

2.513–8.963 2.372–8.482

,.001* ,.001*

CI 5 confidence interval; DGE 5 delayed gastric emptying; group A 5 all PD patients; group B 5 patients who received classical PD with child reconstruction; PD 5 pancreaticoduodenectomy; POPF 5 postoperative pancreatic fistula. *P , .05.

in demographic characteristics and perioperative mortality between the 2 groups. Characteristics of the 2 groups are summarized in Table 4. Operating time was shorter in the Child-non-Braun group. The incidence of DGE was significantly lower in the Child-Braun group (6.7% vs 26.9%, P , .001) and the rate of clinically relevant POPF (grade B 1 C) was also significantly lower (5.34%). The overall postoperative complication rate was significantly lower in the Child-Braun anastomosis group than in the Child-nonBraun anastomosis group (35.0% vs 50.2%, P 5 .002).

Comments Although the reported mortality rate of PD is less than 2% in high-volume centers,3 the morbidity rate has remained high (30% to 60%).5 POPF and DGE are the leading complications reported after PD,3 with DGE in

Table 4

approximately 19% to 57% of patients.5 Even in large pancreatic surgical centers performing standard operative and reconstruction techniques, there has been high variability in the incidence of DGE, partly because of a different definition of DGE.11 Actually, the incidence of DGE probably would be higher than previously reported if it were strictly defined according to ISGPS criteria.7,16,17 DGE can result in longer hospital stay and an increased financial burden. Numerous attempts have been made to prevent DGE, but there is lack of convincing evidence of improved outcomes with any of these efforts. In our series of 418 patients, Braun enteroenterostomy following PD was associated with a significantly reduced incidence of DGE. The incidence of CR-DGE was 16.3% for all our patients and 16.7% for patients who received classic PD. No significant difference was identified in baseline characteristics between the DGE and non-DGE groups. Univariate analysis showed that CR-DGE was

Comparison of characteristics between the Child-Braun group and Child-non-Braun group

Characteristics

Braun group (n 5 206)

Non-Braun group (n 5 201)

Sex Male Female Age (years) Operating time (hours) Estimated blood loss Hospital stay Clinically relevant POPF DGE Grade B Grade C Bile leakage Total complications Postoperative bleeding Enterogastric bleeding Intra-abdominal bleeding Perioperative mortality

124 82 57.88 6 10.61 4.84 6 1.24 357.47 6 300.65 17.33 6 9.89 11 14 1 13 7 72 14 9 3 3

128 73 58.13 6 11.26 4.53 6 1.16 327.62 6 301.76 19.36 6 11.04 39 54 17 37 13 101 17 9 3 2

Statistical value (t/c2) .525

DGE 5 delayed gastric emptying; POPF 5 postoperative pancreatic fistula. *P , .05.

2.235 2.609 .999 21.905 18.672 29.446 15.2968 13.8164 2.052 9.741 .399 .003 .001 .178

P value .469

.814 .009* .318 .052 ,.001* ,.001* ,.001* ,.001* .152 .002* .528 .957 .976 .613

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associated with Braun enteroenterostomy and multivariate analysis supported Braun enteroenterostomy as the only significant independent factor associated with reduced DGE after PD with Child reconstruction, with an odds ratio of 4.485 (95% CI: 2.372 to 8.482, P , .001). Thus, our results suggest that the Child’s procedure plus Braun enteroenterostomy is beneficial for patients. The cause of postoperative DGE is still controversial and needs to be investigated further. Possible causes include pyloric, antral, and duodenal ischemia18; abdominal complications6,19,20; imbalance of hormonal and neuronal factors21–23; and obstruction and technical factors in the digestive tract reconstruction.11,24 DGE has also been reported to be associated with preoperative diabetes,20 but we did not find such an association and further study of this issue is needed. It has been reported that postoperative complications, such as POPF and bile leakage, are significantly associated with increased risk of DGE,3,6 an opinion that our results seemed to support. However, when we used multivariate analysis, POPF and bile leakage were not identified as independent risk factors for DGE, whereas Braun enteroenterostomy was. Therefore, POPF and bile leakage might have a weaker and less direct influence on DGE than does the Braun anastomosis. Some modified digestive reconstructive procedures have been reported to reduce the incidence of DGE. Nikfarjam et al3,6,25 found that a classic PD combined with an antecolic anastomosis and retrogastric vascular omental patch resulted in a significant reduction in the incidence of DGE.5 Kelemen et al26 changed the double-layer pancreatojejunostomy and retrocolic reconstruction to singlelayer implantation pancreatojejunostomy and antecolic reconstruction with Braun anastomosis; the rate of pancreatic fistula was reduced from 17.6% to 5.9% and the frequency of DGE from 10.2% to 2.1%, thus indicating that the Braun anastomosis might affect both POPF and DGE. In our series, all patients received antecolic reconstruction. Because various surgical procedures might affect the postoperative result differently,19,27 to minimize statistical bias from confounding factors, we excluded 11 cases of Cattell reconstruction when evaluating the relationship between Braun enteroenterostomy and DGE; results of this adjustment did not change our conclusion that Braun enteroenterostomy was the key factor in reducing DGE after PD (P , .001). CR-DGE might be initiated by obstruction, such as anastomotic edema or stenosis,5 limb volvulus, gastric irritant effects, and adhesions. In addition, any potential obstruction at the level of gastroenterostomy after a standard reconstruction could increase biliary and pancreatic anastomotic outflow pressures and result in increased risk of pancreatic and biliary fistula and intra-abdominal sepsis. Braun enteroenterostomy between the afferent and efferent limbs distal to the gastroenterostomy potentially stabilizes the gastroenterostomy and helps prevent twisting and angulation. This anastomosis may also reduce edema and kinking at the gastroenterostomy and divert food from the

afferent limb. In addition, it has been reported that Braun anastomosis might decrease bile reflux through the bypass28 and direct pancreatic and biliary juice away from the stomach, thus reducing exposure of the gastric mucosa to irritants. Braun enteroenterostomy reportedly reduces loop obstruction29 and facilitates the passage of the food. It can also decrease biliopancreatic limb pressures and reduce the likelihood of pressure developing in the limb. Therefore, Braun enteroenterostomy may reduce the incidence or severity of POPF and other postoperative complications, which could also help reduce the risk of DGE. We admit that our study suffered from bias inherent in most nonrandomized retrospective trials. Also, the operations were performed during 2 separate time periods. Some centers have reported that DGE rates have decreased over time, in association with increased experience of surgeons. However, our surgeon is an experienced professor, especially in pancreatic and hepatic operations, and has already done a lot of pancreaticoduodenectomies before the onset of this study. Moreover, operative blood loss and most other complications were the same in the 2 patient groups, suggesting there was uniformity in operative techniques during the 2 time periods. Nonetheless, we recommend that the efficacy of the Braun anastomosis in PD be tested in well-designed prospective trials. We also are aware that Lee et al30 have reported that gastric reflux after the Roux-en-Y procedure was significantly less frequent than after a Braun anastomosis, so the question of which of these operations in association with PD would be preferable deserves investigation. In conclusion, the addition of Braun enteroenterostomy to PD operations was an independent risk factor for reducing DGE. It appears to be beneficial for patients and probably should be recommended, although additional testing of the procedure is needed.

Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.amjsurg.2014.06.035.

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Braun enteroenterostomy reduces DGE

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Braun enteroenterostomy during pancreaticoduodenectomy decreases postoperative delayed gastric emptying.

Modified digestive reconstruction during pancreaticoduodenectomy (PD) may affect the postoperative incidence of delayed gastric emptying (DGE). The pu...
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