Research progress of gut microbiome influences on anastomotic leakage following gastrointestinal surgery_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LIU Yuwei ¹ , XU Yujie ² ,  LI Ka ² , WANG Ziqiang ¹ , YANG Jie ¹ , JIANG Lili ¹

1. Department of Gastrointestinal Surgery, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. College of Nursing, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

LI Ka, Email: lika127@126.com

Keywords：

gut microbiome; anastomotic leakage; gastrointestinal surgery

DOI：

10.7507/1007-9424.201905087

Video：

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Objective To explore gut microbiome influences on anastomotic healing following gastrointestinal surgery and its mechanism.Method The relevant literatures about gut microbiome and its impact on healing of gastrointestinal anastomosis and their mechanisms were reviewed.Results Several symbiotic intestinal microbiota such as the Enterococcus faecalis, Pseudomonas aeruginosa, Serratia marcescens, etc. could transform into the pathogenic bacteria with high toxic phenotype in an inflammatory environment in the body, and dissolve the extracellular matrix by degrading collagen or activating matrix metalloproteinase 9, resulting in the anastomotic leak.Conclusion In general, exploring of effect of intestinal microbiome on healing process of anastomotic stoma is just beginning, conditions and mechanisms for transformation of bacteria from symbiotic to pathogenic still need to be explored.

Citation： LIU Yuwei, XU Yujie, LI Ka, WANG Ziqiang, YANG Jie, JIANG Lili. Research progress of gut microbiome influences on anastomotic leakage following gastrointestinal surgery. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(2): 216-220. doi: 10.7507/1007-9424.201905087 Copy

1.	Russ AJ, Casillas MA. Gut microbiota and colorectal surgery: impact on postoperative complications. Clin Colon Rectal Surg, 2016, 29(3): 253-257.
2.	Sciuto A, Merola G, De Palma GD, et al. Predictive factors for anastomotic leakage after laparoscopic colorectal surgery. World J Gastroenterol, 2018, 24(21): 2247-2260.
3.	Lee JA, Chico TJA, Renshaw SA. The triune of intestinal microbiome, genetics and inflammatory status and its impact on the healing of lower gastrointestinal anastomoses. FEBS J, 2018, 285(7): 1212-1225.
4.	Cohn I Jr, Rives JD. Antibiotic protection of colon anastomoses. Ann Surg, 1955, 141(5): 707-717.
5.	Schardey HM, Kamps T, Rau HG, et al. Bacteria: a major pathogenic factor for anastomotic insufficiency. Antimicrob Agents Chemother, 1994, 38(11): 2564-2567.
6.	Schardey HM, Joosten U, Finke U, et al. The prevention of anastomotic leakage after total gastrectomy with local decontamination. A prospective, randomized, double-blind, placebo-controlled multicenter trial. Ann Surg, 1997, 225(2): 172-180.
7.	Binnebösel M, Junge K, Kaemmer DA, et al. Intraperitoneally applied gentamicin increases collagen content and mechanical stability of colon anastomosis in rats. Int J Colorectal Dis, 2009, 24(4): 433-440.
8.	Guyton K, Alverdy JC. The gut microbiota and gastrointestinal surgery. Nat Rev Gastroenterol Hepatol, 2017, 14(1): 43-54.
9.	van Praagh JB, de Goffau MC, Bakker IS, et al. Intestinal microbiota and anastomotic leakage of stapled colorectal anastomoses: a pilot study. Surg Endosc, 2016, 30(6): 2259-2265.
10.	van Praagh JB, de Goffau MC, Bakker IS, et al. Mucus microbiome of anastomotic tissue during surgery has predictive value for colorectal anastomotic leakage. Ann Surg, 2019, 269(5): 911-916.
11.	Reddy RM, Weir WB, Barnett S, et al. Increased variance in oral and gastric microbiome correlates with esophagectomy anastomotic leak. Ann Thorac Surg, 2018, 105(3): 865-870.
12.	Shogan BD, Smith DP, Christley S, et al. Intestinal anastomotic injury alters spatially defined microbiome composition and function. Microbiome, 2014, 2: 35.
13.	Shogan BD, Belogortseva N, Luong PM, et al. Collagen degradation and MMP9 activation by Enterococcus faecalis contribute to intestinal anastomotic leak. Sci Transl Med, 2015, 7(286): 286ra68.
14.	Shakhsheer BA, Versten LA, Luo JN, et al. Morphine promotes colonization of anastomotic tissues with collagenase—Producing Enterococcus faecalis and causes leak. J Gastrointest Surg, 2016, 20(10): 1744-1751.
15.	Komen N, Slieker J, Willemsen P, et al. Polymerase chain reaction for Enterococcus faecalis in drain fluid: the first screening test for symptomatic colorectal anastomotic leakage. The Appeal-study: analysis of parameters predictive for evident anastomotic leakage. Int J Colorectal Dis, 2014, 29(1): 15-21.
16.	Olivas AD, Shogan BD, Valuckaite V, et al. Intestinal tissues induce an SNP mutation in Pseudomonas aeruginosa that enhances its virulence: possible role in anastomotic leak. PLoS One, 2012, 7(8): e44326.
17.	Hyoju SK, Klabbers RE, Aaron M, et al. Oral polyphosphate suppresses bacterial collagenase production and prevents anastomotic leak due to Serratia marcescens and Pseudomonas aeruginosa. Ann Surg, 2018, 267(6): 1112-1118.
18.	Zaborin A, Smith D, Garfield K, et al. Membership and behavior of ultra-low-diversity pathogen communities present in the gut of humans during prolonged critical illness. MBio, 2014, 5(5): e1361-e1314.
19.	Brownlee AR, Bromberg E, Roslin MS. Outcomes in patients with Helicobacter pylori undergoing laparoscopic sleeve gastrectomy. Obes Surg, 2015, 25(12): 2276-2279.
20.	Skowron KB, Lapin B, Rubin M, et al. Clostridium difficile infection in ulcerative colitis: can alteration of the gut-associated microbiome contribute to pouch failure? Inflamm Bowel Dis, 2016, 22(4): 902-911.
21.	Pricolo VE, Chao S, Gregorian A. Clostridium difficile pouchitis after proctocolectomy with ileal pouch-anal anastomosis. Am Surg, 2011, 77(11): E214-E215.
22.	de La Serre CB, Ellis CL, Lee J, et al. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol, 2010, 299(2): G440-G448.
23.	LeBlanc JG, Chain F, Martín R, et al. Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb Cell Fact, 2017, 16(1): 79.
24.	Lopez-Siles M, Duncan SH, Garcia-Gil LJ, et al. Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J, 2017, 11(4): 841-852.
25.	Bloemen JG, Schreinemacher MH, de Bruine AP, et al. Butyrate enemas improve intestinal anastomotic strength in a rat model. Dis Colon Rectum, 2010, 53(7): 1069-1075.
26.	Mathew AJ, Wann VC, Abraham DT, et al. The effect of butyrate on the healing of colonic anastomoses in rats. J Invest Surg, 2010, 23(2): 101-104.
27.	Mao J, Zaborin A, Poroyko V, et al. De novo synthesis of phosphorylated triblock copolymers with pathogen virulence-suppressing properties that prevent infection-related mortality. ACS Biomater Sci Eng, 2017, 3(9): 2076-2085.
28.	Wiegerinck M, Hyoju SK, Mao J, et al. Novel de novo synthesized phosphate carrier compound ABA-PEG20k-Pi20 suppresses collagenase production in Enterococcus faecalis and prevents colonic anastomotic leak in an experimental model. Br J Surg, 2018, 105(10): 1368-1376.
29.	Stern JR, Olivas AD, Valuckaite V, et al. Agent-based model of epithelial host-pathogen interactions in anastomotic leak. J Surg Res, 2013, 184(2): 730-738.
30.	Gershuni VM, Friedman ES. The microbiome-host interaction as a potential driver of anastomotic leak. Curr Gastroenterol Rep, 2019, 21(1): 4.
31.	Kawada K, Sakai Y. Preoperative, intraoperative and postoperative risk factors for anastomotic leakage after laparoscopic low anterior resection with double stapling technique anastomosis. World J Gastroenterol, 2016, 22(25): 5718-5727.
32.	Bosmans JW, Jongen AC, Bouvy ND, et al. Colorectal anastomotic healing: why the biological processes that lead to anastomotic leakage should be revealed prior to conducting intervention studies. BMC Gastroenterol, 2015, 15: 180.
33.	Skowron KB, Shogan BD, Rubin DT, et al. The new frontier: the intestinal microbiome and surgery. J Gastrointest Surg, 2018, 22(7): 1277-1285.
34.	Bachmann R, Leonard D, Delzenne N, et al. Novel insight into the role of microbiota in colorectal surgery. Gut, 2017, 66(4): 738-749.
35.	Gaines S, Shao C, Hyman N, et al. Gut microbiome influences on anastomotic leak and recurrence rates following colorectal cancer surgery. Br J Surg, 2018, 105(2): e131-e141.

1. Russ AJ, Casillas MA. Gut microbiota and colorectal surgery: impact on postoperative complications. Clin Colon Rectal Surg, 2016, 29(3): 253-257.
2. Sciuto A, Merola G, De Palma GD, et al. Predictive factors for anastomotic leakage after laparoscopic colorectal surgery. World J Gastroenterol, 2018, 24(21): 2247-2260.
3. Lee JA, Chico TJA, Renshaw SA. The triune of intestinal microbiome, genetics and inflammatory status and its impact on the healing of lower gastrointestinal anastomoses. FEBS J, 2018, 285(7): 1212-1225.
4. Cohn I Jr, Rives JD. Antibiotic protection of colon anastomoses. Ann Surg, 1955, 141(5): 707-717.
5. Schardey HM, Kamps T, Rau HG, et al. Bacteria: a major pathogenic factor for anastomotic insufficiency. Antimicrob Agents Chemother, 1994, 38(11): 2564-2567.
6. Schardey HM, Joosten U, Finke U, et al. The prevention of anastomotic leakage after total gastrectomy with local decontamination. A prospective, randomized, double-blind, placebo-controlled multicenter trial. Ann Surg, 1997, 225(2): 172-180.
7. Binnebösel M, Junge K, Kaemmer DA, et al. Intraperitoneally applied gentamicin increases collagen content and mechanical stability of colon anastomosis in rats. Int J Colorectal Dis, 2009, 24(4): 433-440.
8. Guyton K, Alverdy JC. The gut microbiota and gastrointestinal surgery. Nat Rev Gastroenterol Hepatol, 2017, 14(1): 43-54.
9. van Praagh JB, de Goffau MC, Bakker IS, et al. Intestinal microbiota and anastomotic leakage of stapled colorectal anastomoses: a pilot study. Surg Endosc, 2016, 30(6): 2259-2265.
10. van Praagh JB, de Goffau MC, Bakker IS, et al. Mucus microbiome of anastomotic tissue during surgery has predictive value for colorectal anastomotic leakage. Ann Surg, 2019, 269(5): 911-916.
11. Reddy RM, Weir WB, Barnett S, et al. Increased variance in oral and gastric microbiome correlates with esophagectomy anastomotic leak. Ann Thorac Surg, 2018, 105(3): 865-870.
12. Shogan BD, Smith DP, Christley S, et al. Intestinal anastomotic injury alters spatially defined microbiome composition and function. Microbiome, 2014, 2: 35.
13. Shogan BD, Belogortseva N, Luong PM, et al. Collagen degradation and MMP9 activation by Enterococcus faecalis contribute to intestinal anastomotic leak. Sci Transl Med, 2015, 7(286): 286ra68.
14. Shakhsheer BA, Versten LA, Luo JN, et al. Morphine promotes colonization of anastomotic tissues with collagenase—Producing Enterococcus faecalis and causes leak. J Gastrointest Surg, 2016, 20(10): 1744-1751.
15. Komen N, Slieker J, Willemsen P, et al. Polymerase chain reaction for Enterococcus faecalis in drain fluid: the first screening test for symptomatic colorectal anastomotic leakage. The Appeal-study: analysis of parameters predictive for evident anastomotic leakage. Int J Colorectal Dis, 2014, 29(1): 15-21.
16. Olivas AD, Shogan BD, Valuckaite V, et al. Intestinal tissues induce an SNP mutation in Pseudomonas aeruginosa that enhances its virulence: possible role in anastomotic leak. PLoS One, 2012, 7(8): e44326.
17. Hyoju SK, Klabbers RE, Aaron M, et al. Oral polyphosphate suppresses bacterial collagenase production and prevents anastomotic leak due to Serratia marcescens and Pseudomonas aeruginosa. Ann Surg, 2018, 267(6): 1112-1118.
18. Zaborin A, Smith D, Garfield K, et al. Membership and behavior of ultra-low-diversity pathogen communities present in the gut of humans during prolonged critical illness. MBio, 2014, 5(5): e1361-e1314.
19. Brownlee AR, Bromberg E, Roslin MS. Outcomes in patients with Helicobacter pylori undergoing laparoscopic sleeve gastrectomy. Obes Surg, 2015, 25(12): 2276-2279.
20. Skowron KB, Lapin B, Rubin M, et al. Clostridium difficile infection in ulcerative colitis: can alteration of the gut-associated microbiome contribute to pouch failure? Inflamm Bowel Dis, 2016, 22(4): 902-911.
21. Pricolo VE, Chao S, Gregorian A. Clostridium difficile pouchitis after proctocolectomy with ileal pouch-anal anastomosis. Am Surg, 2011, 77(11): E214-E215.
22. de La Serre CB, Ellis CL, Lee J, et al. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol, 2010, 299(2): G440-G448.
23. LeBlanc JG, Chain F, Martín R, et al. Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb Cell Fact, 2017, 16(1): 79.
24. Lopez-Siles M, Duncan SH, Garcia-Gil LJ, et al. Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J, 2017, 11(4): 841-852.
25. Bloemen JG, Schreinemacher MH, de Bruine AP, et al. Butyrate enemas improve intestinal anastomotic strength in a rat model. Dis Colon Rectum, 2010, 53(7): 1069-1075.
26. Mathew AJ, Wann VC, Abraham DT, et al. The effect of butyrate on the healing of colonic anastomoses in rats. J Invest Surg, 2010, 23(2): 101-104.
27. Mao J, Zaborin A, Poroyko V, et al. De novo synthesis of phosphorylated triblock copolymers with pathogen virulence-suppressing properties that prevent infection-related mortality. ACS Biomater Sci Eng, 2017, 3(9): 2076-2085.
28. Wiegerinck M, Hyoju SK, Mao J, et al. Novel de novo synthesized phosphate carrier compound ABA-PEG20k-Pi20 suppresses collagenase production in Enterococcus faecalis and prevents colonic anastomotic leak in an experimental model. Br J Surg, 2018, 105(10): 1368-1376.
29. Stern JR, Olivas AD, Valuckaite V, et al. Agent-based model of epithelial host-pathogen interactions in anastomotic leak. J Surg Res, 2013, 184(2): 730-738.
30. Gershuni VM, Friedman ES. The microbiome-host interaction as a potential driver of anastomotic leak. Curr Gastroenterol Rep, 2019, 21(1): 4.
31. Kawada K, Sakai Y. Preoperative, intraoperative and postoperative risk factors for anastomotic leakage after laparoscopic low anterior resection with double stapling technique anastomosis. World J Gastroenterol, 2016, 22(25): 5718-5727.
32. Bosmans JW, Jongen AC, Bouvy ND, et al. Colorectal anastomotic healing: why the biological processes that lead to anastomotic leakage should be revealed prior to conducting intervention studies. BMC Gastroenterol, 2015, 15: 180.
33. Skowron KB, Shogan BD, Rubin DT, et al. The new frontier: the intestinal microbiome and surgery. J Gastrointest Surg, 2018, 22(7): 1277-1285.
34. Bachmann R, Leonard D, Delzenne N, et al. Novel insight into the role of microbiota in colorectal surgery. Gut, 2017, 66(4): 738-749.
35. Gaines S, Shao C, Hyman N, et al. Gut microbiome influences on anastomotic leak and recurrence rates following colorectal cancer surgery. Br J Surg, 2018, 105(2): e131-e141.

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Research progress of gut microbiome influences on anastomotic leakage following gastrointestinal surgery

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