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Gut microbiota and bacterial translocation in digestive surgery: the impact of probiotics

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Abstract

Purpose

It is conceivable that manipulation of the gut microbiota could reduce the incidence or magnitude of surgical complications in digestive surgery. However, the evidence remains inconclusive, although much effort has been devoted to randomized controlled trials (RCTs) and meta-analyses on probiotics. Furthermore, the mechanism behind the protective effects of probiotics appears elusive, our understanding of probiotic actions being fragmentary. The objective of this review is to assess the clinical relevance of the perioperative use of probiotics in major digestive surgery, based on a comprehensive view of the gut microbiota, bacterial translocation (BT), and host defense system.

Methods

The first part of this article describes the pathophysiological events associated with the gut microbiota. Results of RCTs for the perioperative use of probiotics in major digestive surgery are reviewed in the latter part.

Results

The development of the structural and functional barrier to protect against BT primarily results from the generally cooperative interactions between the host and resident microbiota. There is a large body of evidence indicating that probiotics, by enhancing beneficial interactions, reinforce the host defense system to limit BT. The perioperative use of probiotics in patients undergoing hepatobiliary and pancreatic surgery is a promising approach for the prevention of postoperative infectious complications, while the effectiveness in colorectal surgery remains controversial due to substantial heterogeneity among the RCTs with small sample populations.

Conclusions

Further studies, such as multi-center RCTs with a larger sample size, are necessary to confirm the clinical relevance of probiotic agents in major digestive surgery.

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References

  1. Jeppsson B, Mangell P, Thorlacius H (2011) Use of probiotics as prophylaxis for postoperative infections. Nutrients 3:604–612

    Article  PubMed  PubMed Central  Google Scholar 

  2. Correia MI, Liboredo JC, Consoli ML (2012) The role of probiotics in gastrointestinal surgery. Nutrition 28:230–234

    Article  PubMed  Google Scholar 

  3. He D, Wang HY, Feng JY et al (2013) Use of pro-/synbiotics as prophylaxis in patients undergoing colorectal resection for cancer: a meta-analysis of randomized controlled trials. Clin Res Hepatol Gastroenterol 37:406–415

    Article  PubMed  Google Scholar 

  4. Wang W, Xu S, Ren Z et al (2015) Gut microbiota and allogeneic transplantation. J Transl Med 13:275

    Article  PubMed  PubMed Central  Google Scholar 

  5. Gerritsen J, Smidt H, Rijkers GT et al (2011) Intestinal microbiota in human health and disease: the impact of probiotics. Genes Nutr 6:209–240

    Article  PubMed  PubMed Central  Google Scholar 

  6. Arumugam S, Lau CS, Chamberlain RS (2016) Probiotics and synbiotics decrease postoperative sepsis in elective gastrointestinal surgical patients: a meta-analysis. J Gastrointest Surg 20:1123–1131

    Article  PubMed  Google Scholar 

  7. Lytvyn L, Quach K, Banfield L et al (2016) Probiotics and synbiotics for the prevention of postoperative infections following abdominal surgery: a systematic review and meta-analysis of randomized controlled trials. J Hosp Infect 92:130–139

    Article  CAS  PubMed  Google Scholar 

  8. Wu XD, Liu MM, Liang X, et al (2016) Effects of perioperative supplementation with pro-/synbiotics on clinical outcomes in surgical patients: a meta-analysis with trial sequential analysis of randomized controlled trials. Clin Nutr http://www.ncbi.nlm.nih.gov/pubmed/27836310

  9. Yang Z, Wu Q, Liu Y, et al (2016a) Effect of perioperative probiotics and synbiotics on postoperative infections after gastrointestinal surgery: a systematic review with meta-analysis. JPEN J Parenter Enteral Nutr http://www.ncbi.nlm.nih.gov/pubmed/26950947

  10. Geuking MB, Koller Y, Rupp S et al (2014) The interplay between the gut microbiota and the immune system. Gut Microbes 5:411–418

    Article  PubMed  PubMed Central  Google Scholar 

  11. Sassone-Corsi M, Raffatellu M (2015) No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J Immunol 194:4081–4087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Velasquez-Manoff M (2015) Gut microbiome: the peacekeepers. Nature 518:S3–11

    Article  CAS  PubMed  Google Scholar 

  13. Britton RA, Young VB (2014) Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology 146:1547–1553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Buffie CG, Pamer EG (2013) Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 13:790–801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Lawley TD, Walker AW (2013) Intestinal colonization resistance. Immunology 138:1–11

    Article  CAS  PubMed  Google Scholar 

  16. Ammori BJ, Leeder PC, King RF et al (1999) Early increase in intestinal permeability in patients with severe acute pancreatitis: correlation with endotoxemia, organ failure, and mortality. J Gastrointest Surg 3:252–262

    Article  CAS  PubMed  Google Scholar 

  17. Deitch EA (1990) The role of intestinal barrier failure and bacterial translocation in the development of systemic infection and multiple organ failure. Arch Surg 125:403–404

    Article  CAS  PubMed  Google Scholar 

  18. Deitch EA (2012) Gut-origin sepsis: evolution of a concept. Surgeon 10:350–356

    Article  PubMed  PubMed Central  Google Scholar 

  19. Brenchley JM, Douek DC (2012) Microbial translocation across the GI tract. Annu Rev Immunol 30:149–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. MacFie J, O’Boyle C, Mitchell CJ et al (1999) Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity. Gut 45:223–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hotchkiss RS, Karl IE (2003) The pathophysiology and treatment of sepsis. N Engl J Med 348:138–150

    Article  CAS  PubMed  Google Scholar 

  22. MacFie J, Reddy BS, Gatt M et al (2006) Bacterial translocation studied in 927 patients over 13 years. Br J Surg 93:87–93

    Article  CAS  PubMed  Google Scholar 

  23. Britton RA, Young VB (2012) Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends Microbiol 20:313–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Marteyn B, Scorza FB, Sansonetti PJ et al (2011) Breathing life into pathogens: the influence of oxygen on bacterial virulence and host responses in the gastrointestinal tract. Cell Microbiol 13:171–176

    Article  CAS  PubMed  Google Scholar 

  25. Duncan SH, Louis P, Thomson JM et al (2009) The role of pH in determining the species composition of the human colonic microbiota. Environ Microbiol 11:2112–2122

    Article  PubMed  Google Scholar 

  26. Kamiya S, Nagino M, Kanazawa H et al (2004) The value of bile replacement during external biliary drainage: an analysis of intestinal permeability, integrity, and microflora. Ann Surg 239:510–517

    Article  PubMed  PubMed Central  Google Scholar 

  27. Deitch EA (1989) Simple intestinal obstruction causes bacterial translocation in man. Arch Surg 124:699–701

    Article  CAS  PubMed  Google Scholar 

  28. Shiomi H, Shimizu T, Endo Y et al (2007) Relations among circulating monocytes, dendritic cells, and bacterial translocation in patients with intestinal obstruction. World J Surg 31:1806–1812

    Article  PubMed  Google Scholar 

  29. Komatsu S, Panes J, Grisham MB et al (1997) Effects of intestinal stasis on intercellular adhesion molecule 1 expression in the rat: role of enteric bacteria. Gastroenterology 112:1971–1978

    Article  CAS  PubMed  Google Scholar 

  30. Stavrou G, Kotzampassi K (2017) Gut microbiome, surgical complications and probiotics. Ann Gastroenterol 30:45–53

    PubMed  Google Scholar 

  31. Guttman JA, Finlay BB (2009) Tight junctions as targets of infectious agents. Biochim Biophys Acta 1788:832–841

    Article  CAS  PubMed  Google Scholar 

  32. Gordon JI, Hermiston ML (1994) Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr Opin Cell Biol 6:795–803

    Article  CAS  PubMed  Google Scholar 

  33. Johansson ME (2012) Fast renewal of the distal colonic mucus layers by the surface goblet cells as measured by in vivo labeling of mucin glycoproteins. PLoS One 7:e41009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Louis P, Young P, Holtrop G et al (2010) Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol 12:304–314

    Article  CAS  PubMed  Google Scholar 

  35. Mortensen PB, Clausen MR (1996) Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenterol Suppl 216:132–148

    Article  CAS  PubMed  Google Scholar 

  36. Gantois I, Ducatelle R, Pasmans F et al (2006) Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72:946–949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Valenzano MC, DiGuilio K, Mercado J et al (2015) Remodeling of tight junctions and enhancement of barrier integrity of the CACO-2 intestinal epithelial cell layer by micronutrients. PLoS One 10:e0133926

    Article  PubMed  PubMed Central  Google Scholar 

  38. Furusawa Y, Obata Y, Fukuda S et al (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446–450

    Article  CAS  PubMed  Google Scholar 

  39. Inan MS, Rasoulpour RJ, Yin L et al (2000) The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line. Gastroenterology 118:724–734

    Article  CAS  PubMed  Google Scholar 

  40. Kankainen M, Paulin L, Tynkkynen S et al (2009) Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein. Proc Natl Acad Sci U S A 106:17193–17198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Panda S, El khader I, Casellas F et al (2014) Short-term effect of antibiotics on human gut microbiota. PLoS One 9:e95476

    Article  PubMed  PubMed Central  Google Scholar 

  42. Watanabe M, Murakami M, Nakao K et al (2010) Randomized clinical trial of the influence of mechanical bowel preparation on faecal microflora in patients undergoing colonic cancer resection. Br J Surg 97:1791–1797

    Article  CAS  PubMed  Google Scholar 

  43. Jalanka J, Salonen A, Salojarvi J et al (2015) Effects of bowel cleansing on the intestinal microbiota. Gut 64:1562–1568

    Article  PubMed  Google Scholar 

  44. Reddy BS, Gatt M, Sowdi R et al (2006) Surgical manipulation of the large intestine increases bacterial translocation in patients undergoing elective colorectal surgery. Color Dis 8:596–600

    Article  CAS  Google Scholar 

  45. Ozban M, Aydin C, Cevahir N et al (2015) The effect of melatonin on bacterial translocation following ischemia/reperfusion injury in a rat model of superior mesenteric artery occlusion. BMC Surg 15:18

    Article  PubMed  PubMed Central  Google Scholar 

  46. Karabeyoglu M, Unal B, Bozkurt B et al (2008) The effect of ethyl pyruvate on oxidative stress in intestine and bacterial translocation after thermal injury. J Surg Res 144:59–63

    Article  CAS  PubMed  Google Scholar 

  47. Su Y, Pan H, Guo Z et al (2015) Bacterial translocation and endotoxemia after pringle maneuver in cirrhotic rats. Dig Dis Sci 60:414–419

    Article  PubMed  Google Scholar 

  48. Kasravi FB, Wang L, Wang XD et al (1996) Bacterial translocation in acute liver injury induced by D-galactosamine. Hepatology 23:97–103

    CAS  PubMed  Google Scholar 

  49. Morowitz MJ, Babrowski T, Carlisle EM et al (2011) The human microbiome and surgical disease. Ann Surg 253:1094–1101

    Article  PubMed  PubMed Central  Google Scholar 

  50. Alverdy J, Holbrook C, Rocha F et al (2000) Gut-derived sepsis occurs when the right pathogen with the right virulence genes meets the right host: evidence for in vivo virulence expression in Pseudomonas aeruginosa. Ann Surg 232:480–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kanazawa H, Nagino M, Kamiya S et al (2005) Synbiotics reduce postoperative infectious complications: a randomized controlled trial in biliary cancer patients undergoing hepatectomy. Langenbeck’s Arch Surg 390:104–113

    Article  Google Scholar 

  52. Reddy BS, Macfie J, Gatt M et al (2007) Randomized clinical trial of effect of synbiotics, neomycin and mechanical bowel preparation on intestinal barrier function in patients undergoing colectomy. Br J Surg 94:546–554

    Article  CAS  PubMed  Google Scholar 

  53. Liu Z, Qin H, Yang Z et al (2011) Randomised clinical trial: the effects of perioperative probiotic treatment on barrier function and post-operative infectious complications in colorectal cancer surgery—a double-blind study. Aliment Pharmacol Ther 33:50–63

    Article  CAS  PubMed  Google Scholar 

  54. Usami M, Miyoshi M, Kanbara Y et al (2011) Effects of perioperative synbiotic treatment on infectious complications, intestinal integrity, and fecal flora and organic acids in hepatic surgery with or without cirrhosis. JPEN J Parenter Enteral Nutr 35:317–328

    Article  PubMed  Google Scholar 

  55. Tanaka K, Yano M, Motoori M et al (2012) Impact of perioperative administration of synbiotics in patients with esophageal cancer undergoing esophagectomy: a prospective randomized controlled trial. Surgery 152:832–842

    Article  PubMed  Google Scholar 

  56. Zhang JW, Du P, Gao J et al (2012) Preoperative probiotics decrease postoperative infectious complications of colorectal cancer. Am J Med Sci 343:199–205

    Article  PubMed  Google Scholar 

  57. Sadahiro S, Suzuki T, Tanaka A et al (2014) Comparison between oral antibiotics and probiotics as bowel preparation for elective colon cancer surgery to prevent infection: prospective randomized trial. Surgery 155:493–503

    Article  PubMed  Google Scholar 

  58. Yokoyama Y, Nishigaki E, Abe T et al (2014) Randomized clinical trial of the effect of perioperative synbiotics versus no synbiotics on bacterial translocation after oesophagectomy. Br J Surg 101:189–199

    Article  CAS  PubMed  Google Scholar 

  59. Komatsu S, Sakamoto E, Norimizu S et al (2016) Efficacy of perioperative synbiotics treatment for the prevention of surgical site infection after laparoscopic colorectal surgery: a randomized controlled trial. Surg Today 46:479–490

    Article  CAS  PubMed  Google Scholar 

  60. Mizuno T, Yokoyama Y, Nishio H et al (2010) Intraoperative bacterial translocation detected by bacterium-specific ribosomal rna-targeted reverse-transcriptase polymerase chain reaction for the mesenteric lymph node strongly predicts postoperative infectious complications after major hepatectomy for biliary malignancies. Ann Surg 252:1013–1019

    Article  PubMed  Google Scholar 

  61. Nishigaki E, Abe T, Yokoyama Y et al (2014) The detection of intraoperative bacterial translocation in the mesenteric lymph nodes is useful in predicting patients at high risk for postoperative infectious complications after esophagectomy. Ann Surg 259:477–484

    Article  PubMed  Google Scholar 

  62. Rayes N, Seehofer D, Hansen S et al (2002) Early enteral supply of lactobacillus and fiber versus selective bowel decontamination: a controlled trial in liver transplant recipients. Transplantation 74:123–127

    Article  PubMed  Google Scholar 

  63. Rayes N, Seehofer D, Theruvath T et al (2005) Supply of pre- and probiotics reduces bacterial infection rates after liver transplantation--a randomized, double-blind trial. Am J Transplant 5:125–130

    Article  PubMed  Google Scholar 

  64. Sugawara G, Nagino M, Nishio H et al (2006) Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg 244:706–714

    Article  PubMed  PubMed Central  Google Scholar 

  65. Nomura T, Tsuchiya Y, Nashimoto A et al (2007) Probiotics reduce infectious complications after pancreaticoduodenectomy. Hepato-Gastroenterology 54:661–663

    PubMed  Google Scholar 

  66. Rayes N, Seehofer D, Theruvath T et al (2007) Effect of enteral nutrition and synbiotics on bacterial infection rates after pylorus-preserving pancreatoduodenectomy: a randomized, double-blind trial. Ann Surg 246:36–41

    Article  PubMed  PubMed Central  Google Scholar 

  67. Diepenhorst GM, van Ruler O, Besselink MG et al (2011) Influence of prophylactic probiotics and selective decontamination on bacterial translocation in patients undergoing pancreatic surgery: a randomized controlled trial. Shock 35:9–16

    Article  PubMed  Google Scholar 

  68. Eguchi S, Takatsuki M, Hidaka M et al (2011) Perioperative synbiotic treatment to prevent infectious complications in patients after elective living donor liver transplantation: a prospective randomized study. Am J Surg 201:498–502

    Article  PubMed  Google Scholar 

  69. Rammohan A, Sathyanesan J, Rajendran K et al (2015) Synbiotics in surgery for chronic pancreatitis: are they truly effective? A single-blind prospective randomized control trial. Ann Surg 262:31–37

    Article  PubMed  Google Scholar 

  70. Sommacal HM, Bersch VP, Vitola SP et al (2015) Perioperative synbiotics decrease postoperative complications in periampullary neoplasms: a randomized, double-blind clinical trial. Nutr Cancer 67:457–462

    Article  CAS  PubMed  Google Scholar 

  71. Yokoyama Y, Miyake T, Kokuryo T et al (2016) Effect of perioperative synbiotic treatment on bacterial translocation and postoperative infectious complications after pancreatoduodenectomy. Dig Surg 33:220–229

    Article  PubMed  Google Scholar 

  72. Backhed F, Ley RE, Sonnenburg JL et al (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920

    Article  PubMed  Google Scholar 

  73. Gianotti L, Morelli L, Galbiati F et al (2010) A randomized double-blind trial on perioperative administration of probiotics in colorectal cancer patients. World J Gastroenterol 16:167–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Horvat M, Krebs B, Potrc S et al (2010) Preoperative synbiotic bowel conditioning for elective colorectal surgery. Wien Klin Wochenschr 122(Suppl 2):26–30

    Article  PubMed  Google Scholar 

  75. Mangell P, Thorlacius H, Syk I et al (2012) Lactobacillus plantarum 299v does not reduce enteric bacteria or bacterial translocation in patients undergoing colon resection. Dig Dis Sci 57:1915–1924

    Article  PubMed  Google Scholar 

  76. Liu ZH, Huang MJ, Zhang XW et al (2013) The effects of perioperative probiotic treatment on serum zonulin concentration and subsequent postoperative infectious complications after colorectal cancer surgery: a double-center and double-blind randomized clinical trial. Am J Clin Nutr 97:117–126

    Article  CAS  PubMed  Google Scholar 

  77. Pellino G, Sciaudone G, Candilio G et al (2013) Early postoperative administration of probiotics versus placebo in elderly patients undergoing elective colorectal surgery: a double-blind randomized controlled trial. BMC Surg 13(Suppl 2):S57

    Article  PubMed  PubMed Central  Google Scholar 

  78. Kotzampassi K, Stavrou G, Damoraki G et al (2015) A four-probiotics regimen reduces postoperative complications after colorectal surgery: a randomized, double-blind, placebo-controlled study. World J Surg 39:2776–2783

    Article  PubMed  Google Scholar 

  79. Liu Z, Li C, Huang M et al (2015) Positive regulatory effects of perioperative probiotic treatment on postoperative liver complications after colorectal liver metastases surgery: a double-center and double-blind randomized clinical trial. BMC Gastroenterol 15:34

    Article  PubMed  PubMed Central  Google Scholar 

  80. Consoli ML, da Silva RS, Nicoli JR et al (2016) Randomized clinical trial: impact of oral administration of Saccharomyces boulardii on gene expression of intestinal cytokines in patients undergoing colon resection. JPEN J Parenter Enteral Nutr 40:1114–1121

    Article  PubMed  Google Scholar 

  81. Theodoropoulos GE, Memos NA, Peitsidou K et al (2016) Synbiotics and gastrointestinal function-related quality of life after elective colorectal cancer resection. Ann Gastroenterol 29:56–62

    PubMed  PubMed Central  Google Scholar 

  82. Yang Y, Xia Y, Chen H et al (2016b) The effect of perioperative probiotics treatment for colorectal cancer: short-term outcomes of a randomized controlled trial. Oncotarget 7:8432–8440

    PubMed  PubMed Central  Google Scholar 

  83. Watt DG, McSorley ST, Horgan PG et al (2015) Enhanced recovery after surgery: which components, if any, impact on the systemic inflammatory response following colorectal surgery?: a systematic review. Medicine (Baltimore) 94:e1286

    Article  CAS  Google Scholar 

  84. Besselink MG, van Santvoort HC, Renooij W et al (2009) Intestinal barrier dysfunction in a randomized trial of a specific probiotic composition in acute pancreatitis. Ann Surg 250:712–719

    Article  PubMed  Google Scholar 

  85. Bongaerts GP, Severijnen RS (2016) A reassessment of the PROPATRIA study and its implications for probiotic therapy. Nat Biotechnol 34:55–63

    Article  CAS  PubMed  Google Scholar 

  86. Meini S, Laureano R, Fani L et al (2015) Breakthrough Lactobacillus rhamnosus GG bacteremia associated with probiotic use in an adult patient with severe active ulcerative colitis: case report and review of the literature. Infection 43:777–781

    Article  PubMed  Google Scholar 

  87. Thygesen JB, Glerup H, Tarp B (2012) Saccharomyces boulardii fungemia caused by treatment with a probioticum. BMJ Case Rep 2012

  88. Vahabnezhad E, Mochon AB, Wozniak LJ et al (2013) Lactobacillus bacteremia associated with probiotic use in a pediatric patient with ulcerative colitis. J Clin Gastroenterol 47:437–439

    Article  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Takashi Asahara and Koji Nomoto in Yakult Central Institute for their valuable comments on the manuscript. We are also grateful to Kenta Murotani in the Division of Biostatistics, Clinical Research Center, Aichi Medical University, for valuable comments on the statistics in the previous studies of meta-analysis.

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Authors and Affiliations

  1. Department of Gastroenterological Surgery, Aichi Medical University, 1-1 Yazakokarimata, Nagakute, Aichi, 480-1195, Japan

    Shunichiro Komatsu

  2. Division of Surgical Oncology, Department of Surgery, Nagoya University Graduate School of Medicine, Nagoya, Japan

    Yukihiro Yokoyama & Masato Nagino

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  1. Shunichiro Komatsu
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  2. Yukihiro Yokoyama
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  3. Masato Nagino
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S. Komatsu: drafting of manuscript; Y. Yokoyama and M. Nagino: critical revision of manuscript.

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Correspondence to Shunichiro Komatsu.

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Komatsu, S., Yokoyama, Y. & Nagino, M. Gut microbiota and bacterial translocation in digestive surgery: the impact of probiotics. Langenbecks Arch Surg 402, 401–416 (2017). https://doi.org/10.1007/s00423-017-1577-6

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