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Clin Colon Rectal Surg 2023; 36(02): 138-145
DOI: 10.1055/s-0042-1760675
Review Article

Preparing the Bowel (Microbiome) for Surgery: Surgical Bioresilience

Heidi Paine
1   Division of General Surgery, Imperial College Healthcare NHS Trust, London, United Kingdom
,
Faye Jones
2   Division of General Surgery, King Edward VII Hospital, London, United Kingdom
,
James Kinross
3   Division of Colorectal Surgery, Department of Surgery and Cancer, Imperial College London, London, United Kingdom
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Abstract

The preparation of the bowel for radical surgery is a corner stone of elective colorectal practice. The evidence for this intervention is of variable quality and it is often contradictory, yet there is now a global move toward the adoption of oral antibiotic therapy for the reduction of perioperative infective complications, such as surgical site infections. The gut microbiome is a critical mediator of the systemic inflammatory response to surgical injury, wound healing, and perioperative gut function. The loss of critical microbial symbiotic functions caused by bowel preparation and surgery has an adverse impact on surgical outcomes, yet the mechanisms through which this occurs are poorly defined. In this review, the evidence for bowel preparation strategies is critically appraised in the context of the gut microbiome. The impact of antibiotic therapy on the surgical gut microbiome and the importance of the intestinal “resistome” to surgical recovery is described. Data to support the augmentation of the microbiome through diet, probiotic and symbiotic approaches, as well as fecal transplantation are also appraised. Finally, we propose a novel strategy of bowel preparation defined as “surgical bioresilience” and define areas or prioritization in this emerging field. This describes the optimization of surgical intestinal homeostasis and core surgical exposome-microbiome interactions that regulate the wound immune microenvironment, the systemic inflammatory response to surgical injury, and gut function across the perioperative time course.

Keywords

bowel preparation - gut microbiome - surgical resistome - bioresilience

Supplementary Material



Publication History

Article published online:
03 February 2023

© 2023. Thieme. All rights reserved.

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  • References

  • 1 Güenaga KF, Matos D, Wille-Jørgensen P. Mechanical bowel preparation for elective colorectal surgery. Cochrane Database Syst Rev 2011; 2011 (09) CD001544
    PubMedGoogle Scholar
  • 2 Scott WJ. Water relations of Staphylococcus aureus at 30 degrees C. Aust J Biol Sci 1953; 6 (04) 549-564
    CrossrefPubMedGoogle Scholar
  • 3 Tropini C, Moss EL, Merrill BD. et al. Transient osmotic perturbation causes long-term alteration to the gut microbiota. Cell 2018; 173 (07) 1742-1754.e17
    CrossrefPubMedGoogle Scholar
  • 4 Strocchi A, Bond JH, Ellis C, Levitt MD. Colonic concentrations of hydrogen and methane following colonoscopic preparation with an oral lavage solution. Gastrointest Endosc 1990; 36 (06) 580-582
    CrossrefPubMedGoogle Scholar
  • 5 Jalanka J, Salonen A, Salojärvi J. et al. Effects of bowel cleansing on the intestinal microbiota. Gut 2015; 64 (10) 1562-1568
    CrossrefPubMedGoogle Scholar
  • 6 Lindsay S, Oates A, Bourdillon K. The detrimental impact of extracellular bacterial proteases on wound healing. Int Wound J 2017; 14 (06) 1237-1247
    CrossrefPubMedGoogle Scholar
  • 7 Migaly J, Bafford AC, Francone TD. et al; Clinical Practice Guidelines Committee of the American Society of Colon and Rectal Surgeons. The American Society of Colon and Rectal Surgeons clinical practice guidelines for the use of bowel preparation in elective colon and rectal surgery. Dis Colon Rectum 2019; 62 (01) 3-8
    CrossrefPubMedGoogle Scholar
  • 8 Duff SE, Battersby CLF, Davies RJ. et al. The use of oral antibiotics and mechanical bowel preparation in elective colorectal resection for the reduction of surgical site infection. Colorectal Dis 2020; 22 (04) 364-372
    CrossrefPubMedGoogle Scholar
  • 9 Liu Z, Yang M, Zhao Z-X. et al. Current practice patterns of preoperative bowel preparation in colorectal surgery: a nation-wide survey by the Chinese Society of Colorectal Cancer. World J Surg Oncol 2018; 16 (01) 134-134
    CrossrefPubMedGoogle Scholar
  • 10 Scarborough JE, Mantyh CR, Sun Z, Migaly J. Combined mechanical and oral antibiotic bowel preparation reduces incisional surgical site infection and anastomotic leak rates after elective colorectal resection: an analysis of colectomy-targeted ACS NSQIP. Ann Surg 2015; 262 (02) 331-337
    CrossrefPubMedGoogle Scholar
  • 11 Oshima T, Takesue Y, Ikeuchi H. et al. Preoperative oral antibiotics and intravenous antimicrobial prophylaxis reduce the incidence of surgical site infections in patients with ulcerative colitis undergoing IPAA. Dis Colon Rectum 2013; 56 (10) 1149-1155
    CrossrefPubMedGoogle Scholar
  • 12 Li X, Lin H, Zhu L. et al. The clinical effectiveness of wound edge protectors in reducing surgical site infection after abdominal surgery: meta-analysis. BJS Open 2022; 6 (03) zrac065
    CrossrefPubMedGoogle Scholar
  • 13 Koskenvuo L, Lehtonen T, Koskensalo S. et al. Mechanical and oral antibiotic bowel preparation versus no bowel preparation for elective colectomy (MOBILE): a multicentre, randomised, parallel, single-blinded trial. Lancet 2019; 394 (10201): 840-848
    CrossrefPubMedGoogle Scholar
  • 14 Espin Basany E, Solís-Peña A, Pellino G. et al. Preoperative oral antibiotics and surgical-site infections in colon surgery (ORALEV): a multicentre, single-blind, pragmatic, randomised controlled trial. Lancet Gastroenterol Hepatol 2020; 5 (08) 729-738
    CrossrefPubMedGoogle Scholar
  • 15 Woodfield JC, Clifford K, Schmidt B, Turner GA, Amer MA, McCall JL. Strategies for antibiotic administration for bowel preparation among patients undergoing elective colorectal surgery: a network meta-analysis. JAMA Surg 2022; 157 (01) 34-41
    CrossrefPubMedGoogle Scholar
  • 16 Alexander J, Poynter L, Scott A. et al. A prospective multi-centered analysis of the rectal cancer mucosal microbiome during neoadjuvant long course chemoradiotherapy. Dis Colon Rectum 2017; 60 (06) E118-E118
    PubMedGoogle Scholar
  • 17 Kinross J, Mirnezami R, Alexander J. et al. A prospective analysis of mucosal microbiome-metabonome interactions in colorectal cancer using a combined MAS 1HNMR and metataxonomic strategy. Sci Rep 2017; 7 (01) 8979-8979
    CrossrefPubMedGoogle Scholar
  • 18 Hagan T, Cortese M, Rouphael N. et al. Antibiotics-driven gut microbiome perturbation alters immunity to vaccines in humans. Cell 2019; 178 (06) 1313-1328.e13
    CrossrefPubMedGoogle Scholar
  • 19 Wexler HM. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 2007; 20 (04) 593-621
    CrossrefPubMedGoogle Scholar
  • 20 Zarrinpar A, Chaix A, Xu ZZ. et al. Antibiotic-induced microbiome depletion alters metabolic homeostasis by affecting gut signaling and colonic metabolism. Nat Commun 2018; 9 (01) 2872
    CrossrefPubMedGoogle Scholar
  • 21 Thomas JP, Modos D, Rushbrook SM, Powell N, Korcsmaros T. The emerging role of bile acids in the pathogenesis of inflammatory bowel disease. Front Immunol 2022; 13: 829525
    CrossrefPubMedGoogle Scholar
  • 22 Lavelle A, Sokol H. Gut microbiota-derived metabolites as key actors in inflammatory bowel disease. Nat Rev Gastroenterol Hepatol 2020; 17 (04) 223-237
    CrossrefPubMedGoogle Scholar
  • 23 Jia M, Zhang Y, Gao Y, Ma X. Effects of medium chain fatty acids on intestinal health of monogastric animals. Curr Protein Pept Sci 2020; 21 (08) 777-784
    CrossrefPubMedGoogle Scholar
  • 24 Ma C, Vasu R, Zhang H. The role of long-chain fatty acids in inflammatory bowel disease. Mediators Inflamm 2019; 2019: 8495913
    PubMedGoogle Scholar
  • 25 Cabral DJ, Wurster JI, Korry BJ, Penumutchu S, Belenky P. Consumption of a western-style diet modulates the response of the murine gut microbiome to ciprofloxacin. mSystems 2020; 5 (04) e00317-20
    CrossrefPubMedGoogle Scholar
  • 26 Lee J-Y, Cevallos SA, Byndloss MX. et al. High-fat diet and antibiotics cooperatively impair mitochondrial bioenergetics to trigger dysbiosis that exacerbates pre-inflammatory bowel disease. Cell Host Microbe 2020; 28 (02) 273-284.e6
    CrossrefPubMedGoogle Scholar
  • 27 England PH. Health matters: antimicrobial resistance. In; 2015 England PH. Health matters: antimicrobial resistance. https://www.gov.uk/government/publications/health-matters-antimicrobial-resistance
    PubMedGoogle Scholar
  • 28 Bartolini I, Risaliti M, Ringressi MN. et al. Role of gut microbiota-immunity axis in patients undergoing surgery for colorectal cancer: focus on short and long-term outcomes. World J Gastroenterol 2020; 26 (20) 2498-2513
    CrossrefPubMedGoogle Scholar
  • 29 Schmitt FCF, Schneider M, Mathejczyk W. et al. Postoperative complications are associated with long-term changes in the gut microbiota following colorectal cancer surgery. Life (Basel) 2021; 11 (03) 246
    PubMedGoogle Scholar
  • 30 Dey N, Wagner VE, Blanton LV. et al. Regulators of gut motility revealed by a gnotobiotic model of diet-microbiome interactions related to travel. Cell 2015; 163 (01) 95-107
    CrossrefPubMedGoogle Scholar
  • 31 Clayton TA, Baker D, Lindon JC, Everett JR, Nicholson JK. Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc Natl Acad Sci U S A 2009; 106 (34) 14728-14733
    CrossrefPubMedGoogle Scholar
  • 32 Zhang J, Deji C, Fan J. et al. Differential alteration in gut microbiome profiles during acquisition, extinction and reinstatement of morphine-induced CPP. Prog Neuropsychopharmacol Biol Psychiatry 2021; 104: 110058
    CrossrefPubMedGoogle Scholar
  • 33 Alexander JL, Wilson ID, Teare J, Marchesi JR, Nicholson JK, Kinross JM. Gut microbiota modulation of chemotherapy efficacy and toxicity. Nat Rev Gastroenterol Hepatol 2017; 14 (06) 356-365
    CrossrefPubMedGoogle Scholar
  • 34 Beattie AH, Prach AT, Baxter JP, Pennington CR. A randomised controlled trial evaluating the use of enteral nutritional supplements postoperatively in malnourished surgical patients. Gut 2000; 46 (06) 813-818
    CrossrefPubMedGoogle Scholar
  • 35 Amer MA, Smith MD, Herbison GP, Plank LD, McCall JL. Network meta-analysis of the effect of preoperative carbohydrate loading on recovery after elective surgery. Br J Surg 2017; 104 (03) 187-197
    CrossrefPubMedGoogle Scholar
  • 36 Zeevi D, Korem T, Zmora N. et al. Personalized nutrition by prediction of glycemic responses. Cell 2015; 163 (05) 1079-1094
    Google Scholar
  • 37 Nutrition SACo. Carbohydrates and health In; 2015
    PubMed
  • 38 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 (06) 1112-1118
    CrossrefPubMedGoogle Scholar
  • 39 Kinross JM, Markar S, Karthikesalingam A. et al. A meta-analysis of probiotic and synbiotic use in elective surgery: does nutrition modulation of the gut microbiome improve clinical outcome?. JPEN J Parenter Enteral Nutr 2013; 37 (02) 243-253
    CrossrefPubMedGoogle Scholar
  • 40 Chen Y, Qi A, Teng D. et al. Probiotics and synbiotics for preventing postoperative infectious complications in colorectal cancer patients: a systematic review and meta-analysis. Tech Coloproctol 2022; 26 (06) 425-436
    CrossrefPubMedGoogle Scholar
  • 41 Amitay EL, Carr PR, Gies A, Laetsch DC, Brenner H. Probiotic/synbiotic treatment and postoperative complications in colorectal cancer patients: systematic review and meta-analysis of randomized controlled trials. Clin Transl Gastroenterol 2020; 11 (12) e00268
    CrossrefPubMedGoogle Scholar
  • 42 Komatsu S, Sakamoto E, Norimizu S. et al. Efficacy of perioperative synbiotics treatment for the prevention of surgical site infection after laparoscopic colorectal surgery: a randomized controlled trial. Surg Today 2016; 46 (04) 479-490
    CrossrefPubMedGoogle Scholar
  • 43 O'Mahony C, Scully P, O'Mahony D. et al. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog 2008; 4 (08) e1000112
    CrossrefPubMedGoogle Scholar
  • 44 Zhang JW, Du P, Gao J, Yang BR, Fang WJ, Ying CM. Preoperative probiotics decrease postoperative infectious complications of colorectal cancer. Am J Med Sci 2012; 343 (03) 199-205
    CrossrefPubMedGoogle Scholar
  • 45 O'Toole PW, Marchesi JR, Hill C. Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nat Microbiol 2017; 2: 17057
    CrossrefPubMedGoogle Scholar
  • 46 Quraishi MN, Widlak M, Bhala N. et al. Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment Pharmacol Ther 2017; 46 (05) 479-493
    CrossrefPubMedGoogle Scholar
  • 47 van Nood E, Vrieze A, Nieuwdorp M. et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 2013; 368 (05) 407-415
    CrossrefPubMedGoogle Scholar
  • 48 In, NIH Clinical trials: Clinical trials.gov
    PubMed
  • 49 Mocanu V, Zhang Z, Deehan EC. et al. Fecal microbial transplantation and fiber supplementation in patients with severe obesity and metabolic syndrome: a randomized double-blind, placebo-controlled phase 2 trial. Nat Med 2021; 27 (07) 1272-1279
    CrossrefPubMedGoogle Scholar
  • 50 El-Salhy M, Winkel R, Casen C, Hausken T, Gilja OH, Hatlebakk JG. Efficacy of fecal microbiota transplantation for patients with irritable bowel syndrome at 3 years after transplantation. Gastroenterology 2022; 163 (04) 982-994.e14
    CrossrefPubMedGoogle Scholar
  • 51 Alverdy JC, Hyman N, Gilbert J, Luo JN, Krezalek M. Preparing the bowel for surgery: learning from the past and planning for the future. J Am Coll Surg 2017; 225 (02) 324-332
    CrossrefPubMedGoogle Scholar
  • 52 Eskenazi A, Lood C, Wubbolts J. et al. Combination of pre-adapted bacteriophage therapy and antibiotics for treatment of fracture-related infection due to pandrug-resistant Klebsiella pneumoniae. Nat Commun 2022; 13 (01) 302
    CrossrefPubMedGoogle Scholar
  • 53 Sanchez BC, Heckmann ER, Green SI. et al. Development of phage cocktails to treat E. coli catheter-associated urinary tract infection and associated biofilms. Front Microbiol 2022; 13: 796132
    CrossrefPubMedGoogle Scholar
  • 54 Barbier AJ, Jiang AY, Zhang P, Wooster R, Anderson DG. The clinical progress of mRNA vaccines and immunotherapies. Nat Biotechnol 2022; 40 (06) 840-854
    CrossrefPubMedGoogle Scholar
  • 55 Suresh MK, Vasudevan AK, Biswas L, Biswas R. Protective efficacy of Alum adjuvanted Amidase protein vaccine against Staphylococcus aureus infection in multiple mouse models. J Appl Microbiol 2022; 132 (02) 1422-1434
    CrossrefPubMedGoogle Scholar
  • 56 Takesue Y, Yokoyama T, Akagi S. et al. A brief course of colon preparation with oral antibiotics. Surg Today 2000; 30 (02) 112-116
    CrossrefPubMedGoogle Scholar
  • 57 Ishida H, Yokoyama M, Nakada H, Inokuma S, Hashimoto D. Impact of oral antimicrobial prophylaxis on surgical site infection and methicillin-resistant Staphylococcus aureus infection after elective colorectal surgery. Results of a prospective randomized trial. Surg Today 2001; 31 (11) 979-983
    CrossrefPubMedGoogle Scholar
  • 58 Lewis RT. Oral versus systemic antibiotic prophylaxis in elective colon surgery: a randomized study and meta-analysis send a message from the 1990s. Can J Surg 2002; 45 (03) 173-180
    PubMedGoogle Scholar
  • 59 Espin-Basany E, Sanchez-Garcia JL, Lopez-Cano M. et al. Prospective, randomised study on antibiotic prophylaxis in colorectal surgery. Is it really necessary to use oral antibiotics?. Int J Colorectal Dis 2005; 20 (06) 542-546
    CrossrefPubMedGoogle Scholar
  • 60 Kobayashi M, Mohri Y, Tonouchi H, Miki C, Nakai K, Kusunoki M. Mie Surgical Infection Research Group. Randomized clinical trial comparing intravenous antimicrobial prophylaxis alone with oral and intravenous antimicrobial prophylaxis for the prevention of a surgical site infection in colorectal cancer surgery. Surg Today 2007; 37 (05) 383-388
    CrossrefPubMedGoogle Scholar
  • 61 Roos D, Dijksman LM, Oudemans-van Straaten HM, de Wit LT, Gouma DJ, Gerhards MF. Randomized clinical trial of perioperative selective decontamination of the digestive tract versus placebo in elective gastrointestinal surgery. Br J Surg 2011; 98 (10) 1365-1372
    CrossrefPubMedGoogle Scholar
  • 62 Ikeda A, Konishi T, Ueno M. et al. Randomized clinical trial of oral and intravenous versus intravenous antibiotic prophylaxis for laparoscopic colorectal resection. Br J Surg 2016; 103 (12) 1608-1615
    CrossrefPubMedGoogle Scholar
  • 63 Hata H, Yamaguchi T, Hasegawa S. et al. Oral and parenteral versus parenteral antibiotic prophylaxis in elective laparoscopic colorectal surgery (JMTO PREV 07-01): a phase 3, multicenter, open-label, randomized trial. Ann Surg 2016; 263 (06) 1085-1091
    CrossrefPubMedGoogle Scholar
  • 64 Anjum N, Ren J, Wang G. et al. A randomized control trial of preoperative oral antibiotics as adjunct therapy to systemic antibiotics for preventing surgical site infection in clean contaminated, contaminated, and dirty type of colorectal surgeries. Dis Colon Rectum 2017; 60 (12) 1291-1298
    CrossrefPubMedGoogle Scholar