Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Langenbeck's Archives of Surgery
Published in: Langenbeck's Archives of Surgery 3/2017

01-05-2017 | REVIEW ARTICLE

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

Authors: Shunichiro Komatsu, Yukihiro Yokoyama, Masato Nagino

Published in: Langenbeck's Archives of Surgery | Issue 3/2017

Login to get access

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.
Literature
1.
2.
Correia MI, Liboredo JC, Consoli ML (2012) The role of probiotics in gastrointestinal surgery. Nutrition 28:230–234CrossRefPubMed
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 37:406–415CrossRefPubMed
4.
5.
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 20:1123–1131CrossRefPubMed
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 92:130–139CrossRefPubMed
8.
9.
10.
11.
Sassone-Corsi M, Raffatellu M (2015) No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J Immunol 194:4081–4087CrossRefPubMedPubMedCentral
12.
13.
14.
15.
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 3:252–262CrossRefPubMed
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 125:403–404CrossRefPubMed
18.
19.
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 45:223–228CrossRefPubMedPubMedCentral
21.
Hotchkiss RS, Karl IE (2003) The pathophysiology and treatment of sepsis. N Engl J Med 348:138–150CrossRefPubMed
22.
MacFie J, Reddy BS, Gatt M et al (2006) Bacterial translocation studied in 927 patients over 13 years. Br J Surg 93:87–93CrossRefPubMed
23.
Britton RA, Young VB (2012) Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends Microbiol 20:313–319CrossRefPubMedPubMedCentral
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 13:171–176CrossRefPubMed
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 11:2112–2122CrossRefPubMed
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 239:510–517CrossRefPubMedPubMedCentral
27.
Deitch EA (1989) Simple intestinal obstruction causes bacterial translocation in man. Arch Surg 124:699–701CrossRefPubMed
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 31:1806–1812CrossRefPubMed
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 112:1971–1978CrossRefPubMed
30.
Stavrou G, Kotzampassi K (2017) Gut microbiome, surgical complications and probiotics. Ann Gastroenterol 30:45–53PubMed
31.
Guttman JA, Finlay BB (2009) Tight junctions as targets of infectious agents. Biochim Biophys Acta 1788:832–841CrossRefPubMed
32.
Gordon JI, Hermiston ML (1994) Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr Opin Cell Biol 6:795–803CrossRefPubMed
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:e41009CrossRefPubMedPubMedCentral
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 12:304–314CrossRefPubMed
35.
Mortensen PB, Clausen MR (1996) Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenterol Suppl 216:132–148CrossRefPubMed
36.
Gantois I, Ducatelle R, Pasmans F et al (2006) Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72:946–949CrossRefPubMedPubMedCentral
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:e0133926CrossRefPubMedPubMedCentral
38.
Furusawa Y, Obata Y, Fukuda S et al (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446–450CrossRefPubMed
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 118:724–734CrossRefPubMed
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 106:17193–17198CrossRefPubMedPubMedCentral
41.
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 97:1791–1797CrossRefPubMed
43.
Jalanka J, Salonen A, Salojarvi J et al (2015) Effects of bowel cleansing on the intestinal microbiota. Gut 64:1562–1568CrossRefPubMed
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 8:596–600CrossRef
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 15:18CrossRefPubMedPubMedCentral
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 144:59–63CrossRefPubMed
47.
Su Y, Pan H, Guo Z et al (2015) Bacterial translocation and endotoxemia after pringle maneuver in cirrhotic rats. Dig Dis Sci 60:414–419CrossRefPubMed
48.
Kasravi FB, Wang L, Wang XD et al (1996) Bacterial translocation in acute liver injury induced by D-galactosamine. Hepatology 23:97–103PubMed
49.
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 232:480–489CrossRefPubMedPubMedCentral
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 390:104–113CrossRef
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 94:546–554CrossRefPubMed
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 33:50–63CrossRefPubMed
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 35:317–328CrossRefPubMed
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 152:832–842CrossRefPubMed
56.
Zhang JW, Du P, Gao J et al (2012) Preoperative probiotics decrease postoperative infectious complications of colorectal cancer. Am J Med Sci 343:199–205CrossRefPubMed
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 155:493–503CrossRefPubMed
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 101:189–199CrossRefPubMed
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 46:479–490CrossRefPubMed
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 252:1013–1019CrossRefPubMed
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 259:477–484CrossRefPubMed
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 74:123–127CrossRefPubMed
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 5:125–130CrossRefPubMed
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 244:706–714CrossRefPubMedPubMedCentral
65.
Nomura T, Tsuchiya Y, Nashimoto A et al (2007) Probiotics reduce infectious complications after pancreaticoduodenectomy. Hepato-Gastroenterology 54:661–663PubMed
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 246:36–41CrossRefPubMedPubMedCentral
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 35:9–16CrossRefPubMed
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 201:498–502CrossRefPubMed
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 262:31–37CrossRefPubMed
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 67:457–462CrossRefPubMed
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 33:220–229CrossRefPubMed
72.
Backhed F, Ley RE, Sonnenburg JL et al (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920CrossRefPubMed
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 16:167–175CrossRefPubMedPubMedCentral
74.
Horvat M, Krebs B, Potrc S et al (2010) Preoperative synbiotic bowel conditioning for elective colorectal surgery. Wien Klin Wochenschr 122(Suppl 2):26–30CrossRefPubMed
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 57:1915–1924CrossRefPubMed
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 97:117–126CrossRefPubMed
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):S57CrossRefPubMedPubMedCentral
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 39:2776–2783CrossRefPubMed
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 15:34CrossRefPubMedPubMedCentral
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 40:1114–1121CrossRefPubMed
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 29:56–62PubMedPubMedCentral
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 7:8432–8440PubMedPubMedCentral
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:e1286CrossRef
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 250:712–719CrossRefPubMed
85.
Bongaerts GP, Severijnen RS (2016) A reassessment of the PROPATRIA study and its implications for probiotic therapy. Nat Biotechnol 34:55–63CrossRefPubMed
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 43:777–781CrossRefPubMed
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 47:437–439CrossRefPubMed
Metadata
Title
Gut microbiota and bacterial translocation in digestive surgery: the impact of probiotics
Authors
Shunichiro Komatsu
Yukihiro Yokoyama
Masato Nagino
Publication date
01-05-2017
Publisher
Springer Berlin Heidelberg
Published in
Langenbeck's Archives of Surgery / Issue 3/2017
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI
https://doi.org/10.1007/s00423-017-1577-6

Other articles of this Issue 3/2017

Langenbeck's Archives of Surgery 3/2017 Go to the issue

ORIGINAL ARTICLE

Risk factors for delayed gastric emptying after esophagectomy

ORIGINAL ARTICLE

Preoperative radiographic vascular involvement score predicts the prognosis of resected pancreatic head adenocarcinoma

ORIGINAL ARTICLE

Intensive care and health outcomes of open abdominal treatment: long-term results of vacuum-assisted wound closure and mesh-mediated fascial traction (VAWCM)

ORIGINAL ARTICLE

Distal pancreatectomy associated with multivisceral resection: results from a single centre experience

ORIGINAL ARTICLE

Comparison of two- and three-dimensional display for performance of laparoscopic total gastrectomy for gastric cancer

ORIGINAL ARTICLE

Successful ablation of lymph nodes using irreversible electroporation (IRE) in a porcine survival model