Preparing the Bowel (Microbiome) for Surgery: Surgical Bioresilience

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

Publikationsverlauf

Artikel online veröffentlicht:
03. Februar 2023

• References

• 1 Güenaga KF, Matos D, Wille-Jørgensen P. Mechanical bowel preparation for elective colorectal surgery. Cochrane Database Syst Rev 2011; 2011 (09) CD001544
• 2 Scott WJ. Water relations of Staphylococcus aureus at 30 degrees C. Aust J Biol Sci 1953; 6 (04) 549-564
• 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
• 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
• 5 Jalanka J, Salonen A, Salojärvi J. et al. Effects of bowel cleansing on the intestinal microbiota. Gut 2015; 64 (10) 1562-1568
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 19 Wexler HM. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 2007; 20 (04) 593-621
• 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
• 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
• 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
• 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
• 24 Ma C, Vasu R, Zhang H. The role of long-chain fatty acids in inflammatory bowel disease. Mediators Inflamm 2019; 2019: 8495913
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 36 Zeevi D, Korem T, Zmora N. et al. Personalized nutrition by prediction of glycemic responses. Cell 2015; 163 (05) 1079-1094
• 37 Nutrition SACo. Carbohydrates and health In; 2015
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 45 O'Toole PW, Marchesi JR, Hill C. Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nat Microbiol 2017; 2: 17057
• 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
• 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
• 48 In, NIH Clinical trials: Clinical trials.gov
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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