Skip to main content
  • Research article
  • Open access
  • Published:

Braun anastomosis lowers the incidence of delayed gastric emptying following pancreaticoduodenectomy: a meta-analysis

Abstract

Background

Delayed gastric emptying (DGE) is one of the most frequent complications following pancreaticoduodenectomy. This meta-analysis aimed to evaluate the impact of Braun enteroenterostomy on DGE following pancreaticoduodenectomy.

Methods

A systematic review of the literature was performed to identify relevant studies. Statistical analysis was carried out using Review Manager software 5.3.

Results

Eleven studies involving 1672 patients (1005 in Braun group and 667 in non-Braun group) were included in the meta-analysis. Braun enteroenterostomy was associated with a statistically significant reduction in overall DGE (odds ratios [OR] 0.32, 95% confidence intervals [CI] 0.24 to 0.43; P <0.001), clinically significant DGE (OR 0.27, 95% CI 0.15 to 0.51; P <0.001), bile leak (OR 0.50, 95% CI 0.29 to 0.86; Pā€‰=ā€‰0.01), and length of hospital stay (weighted mean difference -1.66, 95% CI -2.95 to 00.37; Pā€‰=ā€‰0.01).

Conclusions

Braun enteroenterostomy minimizes the rate and severity of DGE following pancreaticoduodenectomy.

Peer Review reports

Background

Delayed gastric emptying (DGE) is one of the most frequent morbidity following pancreaticoduodenectomy with the reported incidence of 14ā€“61% [1]. Although DGE is not life-threatening, it may prolong the length of hospital stay and increase the medical cost. In addition, severe DGE may delay adjuvant therapies for patients with cancer.

To prevent DGE, Braun enteroenterostomy between the afferent and efferent limbs distal to the gastroenterostomy site was introduced and two meta-analyses of several non-randomized controlled trials (NRCTs) demonstrated that it could reduce the occurrence of DGE [2, 3]. However, recent three randomized controlled trials (RCTs) failed to confirm this finding [4,5,6]. It seems that controversies still exist concerning the effect of Braun enteroenterostomy on DGE. The aim of the present meta-analysis is to provide an updated evaluation on this issue.

Methods

The study was conducted following the Preferred Reporting Items for Systematic Reviews and Meta- Analyses (PRISMA) [7]. The protocol of PRISMA consists of a 17-item checklist intended to facilitate the preparation and reporting of a robust protocol for the systematic review and meta- analyses that summarize aggregate data from studies, particularly the evaluations of the effects of interventions.

Study selection

A comprehensive search was performed on electronic databases (PUBMED, EMBASE and Cochrane Library) from inception until May 2017 to identify relevant studies using the key words ā€œpancreaticoduodenectomy,ā€ ā€œBraun enteroenterostomyā€ and ā€œdelayed gastric emptying.ā€ Bibliography of retrieved papers was further manually searched for additional studies. Studies that evaluated the influence of Braun enteroenterostomy on DGE after pancreaticoduodenectomy were considered for inclusion. Non-English language articles, animal studies, abstracts, letters, proceedings from scientific meetings, editorials and expert opinions, duplicates, and noncomparative studies or case series were excluded.

Outcome measures

The primary endpoint was the rate of patients with overall DGE and clinically relevant (grade B-C according to the International Study Group of Pancreatic Surgery [ISGPS] classification) DGE [8]. The secondary endpoints were operative details, clinical parameters related to DGE, other complications like pancreatic fistula, mortality and length of hospital stay.

Data extraction

Two independent reviewers (ZY and SX) respectively assessed each eligible study. Disagreements were resolved by discussion. The standard information extracted from each included study was as follows: first author, year of publication, sample sizes, characteristics of the studies, and endpoints.

Assessment of methodological quality

NRCTs were evaluated using Newcastle-Ottawa quality assessment scale [9]. The quality scale ranges from 0 to 9 stars, and studies with 6 stars or greater were considered to be of high quality. RCTs were scored using the Jadad composite scale [10]. The quality scale ranges from 0 to 5 points, and studies with 3 or more scores were considered to be of high quality.

Statistical methods

Meta-analysis was carried out using Review Manager (RevMan) software 5.3 (Cochrane Collaboration). For categorical variables, statistical analysis was carried out using the weighted mean difference (WMD) with 95% confidence intervals (CI). For dichotomous variables, statistical analysis was carried out using the odds ratios (OR) with 95% CI. Heterogeneity was evaluated by I2 test. The random-effects model was used to analyze data if there was significant heterogeneity (I2ā€‰ā‰„ā€‰50%) between studies; otherwise, the fixed-effects model was used. Risk for bias was evaluated using a funnel plot based on the result of DGE.

Results

Eligible studies

The process of identifying eligible studies is shown in Fig.Ā 1. The search strategy generated 11 articles [4,5,6, 11,12,13,14,15,16,17,18] that fulfilled the inclusion criteria with a total of 1672 patients (1005 in Braun group and 667 in non-Braun group). The characteristics of the included studies are shown in TableĀ 1.

Fig. 1
figure 1

Study flow chart

Table 1 Baseline characteristics of studies included in the meta-analysis

Outcome assessment

The outcomes are shown in TableĀ 2.

Table 2 Results of a meta-analysis

Primary outcomes

Both overall DGE and clinically significant DGE in Braun group were significantly lower than those in non-Braun group (OR 0.32, 95% CI 0.24 to 0.43 and OR 0.27, 95% CI 0.15 to 0.51, both Pā€‰<ā€‰0.001) (Fig.Ā 2-3). No complication directly attributable to Braun enteroenterostomy such as anastomotic leakage or bleeding was reported in any eligible study.

Fig. 2
figure 2

Results of the meta-analysis on delayed gastric emptying

Fig. 3
figure 3

Results of the meta-analysis on clinically significant delayed gastric emptying

Secondary outcomes

Regarding operative details, no significant difference was observed in operative time, estimated blood loss, and requirement of blood transfusion between the two groups.

DGE-related clinical parameters were all significantly lower in the Braun group, including the incidence of vomiting (OR 0.42, 95% CI 0.27 to 0.65; P <0.001), nasogastric tube reinsertion (OR 0.43, 95% CI, 0.23 to 0.81; Pā€‰=ā€‰0.009), and the use of prokinetics or antiemetics (OR 0.58, 95% CI, 0.34 to 1.00; Pā€‰=ā€‰0.05).

In Braun group, the number of bile fistulas was significantly lower (OR 0.50, 95% CI, 0.29 to 0.86; Pā€‰=ā€‰0.01). There was no significant difference in other postoperative complications and mortality. Following Braun enteroenterostomy, the length of hospital stay was estimated to be 1.66ā€‰days shorter than that for patients with no Braun enteroenterostomy (WMD -1.66, 95% CI, āˆ’ā€‰2.95 to āˆ’ā€‰0.37; Pā€‰=ā€‰0.01).

Publication bias

Funnel plots based on the DGE is shown in Fig.Ā 4. Only one study lay outside the limits of the 95% CI, indicating weak evidence of publication bias.

Fig. 4
figure 4

Funnel plot analysis of publication bias. The outcome was the overall delayed gastric emptying

Discussion

With refinements in surgical techniques and advancements in postoperative management, the mortality rate after pancreaticoduodenectomy has fallen below 5% in specialized centers around the world, but the morbidity rate remains high as 30ā€“65% [19]. One major cause of morbidity is that DGE occurs at a frequency of 14ā€“61% [1]. Risk factors for DGE include perioperative diabetes and postoperative complications such as pancreatic fistula [20]. Several surgical techniques for reducing the incidence of DGE have been attempted, including the type of pancreaticoduodenectomy (pylorus-resecting pancreaticoduodenectomy vs. pylorus-preserving pancreaticoduodenectomy) [1], the reconstruction type of gastrojejunostomy (Billroth II vs. Roux-en-Y) [21], and the route of gastro- or duodenojejunostomy (antecolic vs. retrocolic) [22]. Unfortunately, RCTs on these technical measures are scarce. As a result, there is no universal agreement regarding one particular variation being less prone to DGE than the others.

Braun enteroenterostomy was first reported about 100ā€‰years ago and has gained favor in recent years as a potential means to reduce the incidence of DGE following pancreaticoduodenectomy. Theoretically, Braun enteroenterostomy potentially stabilizes the afferent and efferent limbs of the gastrojejunostomy. The gastrojejunostomy itself becomes more stabilized, with a low tendency to twist and angulate [12]. In addition, Braun enteroenterostomy adequately diverts a substantial amount of bile from the afferent limb, thereby decreasing the likelihood of reflux gastritis. It also reduces tension on the anastomosis [11, 12]. However, there are limited studies on the effectiveness of Braun enteroenterostomy on DGE following pancreaticoduodenectomy and the results are conflicting [4,5,6, 11,12,13,14,15,16,17,18]. Meta-analysis provides a way to increase statistical power and resolve inconsistencies. Our pooling data have shown that Braun enteroenterostomy can reduce the rate and severity of DGE compared with non-Braun enteroenterostomy after pancreaticoduodenectomy. As expected, Braun enteroenterostomy also showed advantages in terms of clinical parameters related to DGE and length of hospital stay. These results are comparable to previous results from two earlier meta-analyses [2, 3]. The strength of the present study lies in its large number of patients.

In contrast to two previously published meta-analyses that found no significant difference in bile fistula between the two groups [2, 3], the present update has demonstrated a statistically significant association between Braun enteroenterostomy and a decreased rate of this complication. The incidence of pancreatic fistula also tended to be lower in Braun group with marginal statistical significance (Pā€‰=ā€‰0.06). The weight of three recent RCTs seems important in these findings and participated to increase the measured magnitude of effect size [4,5,6]. It could be hypothesized that Braun enteroenterostomy can decrease biliopancreatic limb pressures, thus decreasing the risk of biliary and pancreatic fistula.

The present analysis has some limitations. First, significant statistical heterogeneity was detected between studies for some outcomes including the analysis of clinically significant DGE (I2ā€‰=ā€‰55%), largely due to the fact that there are significant variations in each clinical setting regarding surgical technique and perioperative care. Second, the level of evidence is low, for a considerable number of data came from NRCTs, knowing that NRCTs have inherent risk of bias. More larger-size RCTs are required to confirm our finding. Finally, long-term outcomes such as the nutritional status were not analyzed in this meta-analysis due to the limited data.

Conclusions

The present meta-analysis shows that Braun anastomosis is associated with a less severe and lower incidence of DGE following pancreaticoduodenectomy.

Abbreviations

95% CI:

95% confidence interval

DGE:

Delayed gastric emptying

ISGPS:

International Study Group of Pancreatic Surgery

NRCTs:

Non-randomised controlled trials

NT:

Nasogastric tube

OR:

Odds ratio

PRISMA:

Preferred reporting items for systematic reviews and meta-analyses

RCTs:

Randomised controlled trials

WMD:

Weighted mean difference

References

  1. Zhou Y, Lin L, Wu L, et al. A case-matched comparison and meta-analysis comparing pylorus-resecting pancreaticoduodenectomy with pylorus-preserving pancreaticoduodenectomy for the incidence of postoperative delayed gastric emptying. HPB (Oxford). 2015;17:337ā€“43. https://doi.org/10.1111/hpb.12358.

    ArticleĀ  Google ScholarĀ 

  2. Huang MQ, Li M, Mao JY, et al. Braun enteroenterostomy reduces delayed gastric emptying: a systematic review and meta-analysis. Int J Surg. 2015;23:75ā€“81. https://doi.org/10.1016/j.ijsu.2015.09.038.

    ArticleĀ  PubMedĀ  Google ScholarĀ 

  3. Xu B, Zhu YH, Qian MP, et al. Braun Enteroenterostomy following Pancreaticoduodenectomy: a systematic review and Meta-analysis. Medicine (Baltimore). 2015;94:e1254. https://doi.org/10.1097/MD.0000000000001254.

    ArticleĀ  Google ScholarĀ 

  4. Kakaei F, Beheshtirouy S, Nejatollahi SM, et al. Effects of adding Braun jejunojejunostomy to standard Whipple procedure on reduction of afferent loop syndrome - a randomized clinical trial. Can J Surg. 2015;58:383ā€“8.

    ArticleĀ  Google ScholarĀ 

  5. Hwang HK, Lee SH, Han DH, et al. Impact of Braun anastomosis on reducing delayed gastric emptying following pancreaticoduodenectomy: a prospective, randomized controlled trial. J Hepatobiliary Pancreat Sci. 2016;23:364ā€“72. https://doi.org/10.1002/jhbp.349.

    ArticleĀ  PubMedĀ  Google ScholarĀ 

  6. Fujieda H, Yokoyama Y, Hirata A, et al. Does Braun anastomosis have an impact on the incidence of delayed gastric emptying and the extent of Intragastric bile reflux following Pancreatoduodenectomy? - a randomized controlled study. Dig Surg. 2017. https://doi.org/10.1159/000455334 [Epub ahead of print].

    ArticleĀ  CASĀ  Google ScholarĀ 

  7. Moher D, Liberati A, Tetzlaff J, et al. The PRISMA group. Preferred reporting items for systematic reviews and Meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.

    ArticleĀ  Google ScholarĀ 

  8. Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the international study Group of Pancreatic Surgery (ISGPS). Surgery. 2007;142:761ā€“8.

    ArticleĀ  Google ScholarĀ 

  9. Athanasiou T, Al-Ruzzeh S, Kumar P, et al. Off-pump myocardial revascularization is associated with less incidence of stroke in elderly patients. Ann Thorac Surg. 2004;77:745ā€“53.

    ArticleĀ  Google ScholarĀ 

  10. Jadad AR, Moore RA, Carroll D, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17:1ā€“12.

    ArticleĀ  CASĀ  Google ScholarĀ 

  11. Hochwald SN, Grobmyer SR, Hemming AW, et al. Braun enteroenterostomy is associated with reduced delayed gastric emptying and early resumption of oral feeding following pancreaticoduodenectomy. J Surg Oncol. 2010;101:351ā€“5. https://doi.org/10.1002/jso.21490.

    ArticleĀ  PubMedĀ  Google ScholarĀ 

  12. Nikfarjam M, Houli N, Tufail F, et al. Reduction in delayed gastric emptying following non-pylorus preserving pancreaticoduodenectomy by addition of a Braun enteroenterostomy. JOP. 2012;13:488ā€“96. https://doi.org/10.6092/1590-8577/800.

    ArticleĀ  PubMedĀ  Google ScholarĀ 

  13. Cordesmeyer S, Lodde S, Zeden K, et al. Prevention of delayed gastric emptying after pylorus-preserving pancreatoduodenectomy with antecolic reconstruction, a long jejunal loop, and a jejuno-jejunostomy. J Gastrointest Surg. 2014;18:662ā€“73. https://doi.org/10.1007/s11605-013-2446-4.

    ArticleĀ  CASĀ  PubMedĀ  Google ScholarĀ 

  14. Wang L, Ap S, Zhang Y, et al. Reduction of alkaline reflux gastritis and marginal ulcer by modified Braun enteroenterostomy in gastroenterologic reconstruction after pancreaticoduodenectomy. J Surg Res. 2014;189:41ā€“7. https://doi.org/10.1016/j.jss.2014.01.025.

    ArticleĀ  PubMedĀ  Google ScholarĀ 

  15. Zhang XF, Yin GZ, Liu QG, et al. Does Braun enteroenterostomy reduce delayed gastric emptying after pancreaticoduodenectomy? Medicine (Baltimore). 2014;93:e48. https://doi.org/10.1097/MD.0000000000000048.

    ArticleĀ  Google ScholarĀ 

  16. Xu B, Meng H, Qian M, et al. Braun enteroenterostomy during pancreaticoduodenectomy decreases postoperative delayed gastric emptying. Am J Surg. 2015;209:1036ā€“42. https://doi.org/10.1016/j.amjsurg.2014.06.035.

    ArticleĀ  PubMedĀ  Google ScholarĀ 

  17. Meng HB, Zhou B, Wu F, et al. Continuous suture of the pancreatic stump and Braun enteroenterostomy in pancreaticoduodenectomy. World J Gastroenterol. 2015;21:2731ā€“8. https://doi.org/10.3748/wjg.v21.i9.2731.

    ArticleĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  18. Watanabe Y, Ohtsuka T, Kimura H, et al. Braun enteroenterostomy reduces delayed gastric emptying after pylorus-preserving pancreatoduodenectomy: a retrospective review. Am J Surg. 2015;209:369ā€“77. https://doi.org/10.1016/j.amjsurg.2014.05.007.

    ArticleĀ  PubMedĀ  Google ScholarĀ 

  19. Figueras J, Sabater L, Planellas P, et al. Randomized clinical trial of pancreaticogastrostomy versus pancreaticojejunostomy on the rate and severity of pancreatic fistula after pancreaticoduodenectomy. Br J Surg. 2013;100:1597ā€“605. https://doi.org/10.1002/bjs.9252.

    ArticleĀ  CASĀ  PubMedĀ  Google ScholarĀ 

  20. Qu H, Sun GR, Zhou SQ, et al. Clinical risk factors of delayed gastric emptying in patients after pancreaticoduodenectomy: a systematic review and meta-analysis. Eur J Surg Oncol. 2013;39:213ā€“23. https://doi.org/10.1016/j.ejso.2012.12.010.

    ArticleĀ  CASĀ  PubMedĀ  Google ScholarĀ 

  21. Shimoda M, Kubota K, Katoh M, et al. Effect of billroth II or roux-en-Y reconstruction for the gastrojejunostomy on delayed gastric emptying after pancreaticoduodenectomy: a randomized controlled study. Ann Surg. 2013;257:938ā€“42. https://doi.org/10.1097/SLA.0b013e31826c3f90.

    ArticleĀ  PubMedĀ  Google ScholarĀ 

  22. Zhou Y, Lin J, Wu L, et al. Effect of antecolic or retrocolic reconstruction of the gastro/duodenojejunostomy on delayed gastric emptying after pancreaticoduodenectomy: a meta-analysis. BMC Gastroenterol. 2015;15:68. https://doi.org/10.1186/s12876-015-0300-8.

    ArticleĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

Download references

Acknowledgements

We thank Doctor Yanfang Zhao (Department of Health Statistics, Second Military Medical University, Shanghai, China) for her critical revision of the meta-analysis section.

Funding

The project was supported by Natural Science Foundation of Fujian province (2015ā€‰J01561) and Major Diseases Joint Research Program of Xiamen City (3502Z20170943).

Availability of data and materials

Input data for the analyses are available from the corresponding author on request.

Author information

Authors and Affiliations

Authors

Contributions

HB and ZY participated in the design and coordination of the study, carried out the critical appraisal of studies and wrote the manuscript. HB, WK, and XS developed the literature search, carried out the extraction of data, assisted in the critical appraisal of included studies and assisted in writing up, WK and ZY carried out the statistical analysis of studies. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yanming Zhou.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisherā€™s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, Y., Hu, B., Wei, K. et al. Braun anastomosis lowers the incidence of delayed gastric emptying following pancreaticoduodenectomy: a meta-analysis. BMC Gastroenterol 18, 176 (2018). https://doi.org/10.1186/s12876-018-0909-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12876-018-0909-5

Keywords