Implementation of the gut microbiota prevents anastomotic leaks in laparoscopic colorectal surgery for cancer:the results of the MIRACLe study.
Anastomotic leak
Colorectal cancer
Colorectal surgery
Laparoscopy
Microbiota
Journal
Updates in surgery
ISSN: 2038-3312
Titre abrégé: Updates Surg
Pays: Italy
ID NLM: 101539818
Informations de publication
Date de publication:
Aug 2022
Aug 2022
Historique:
received:
23
03
2022
accepted:
17
05
2022
pubmed:
24
6
2022
medline:
3
8
2022
entrez:
23
6
2022
Statut:
ppublish
Résumé
The aim of this pilot study was to evaluate the effects of a novel perioperative treatment for the implementation of the gut microbiota, to prevent anastomotic fistula and leakage (AL) in patients undergoing laparoscopic colorectal resections for cancer. A series of 60 patients who underwent elective colorectal surgery at S. Eugenio Hospital (Rome-Italy) between December 1, 2020 and November 30, 2021 and received a novel perioperative preparation following the MIRACLe (Microbiota Implementation to Reduce Anastomotic Colorectal Leaks) protocol (oral antibiotics, mechanical bowel preparation and perioperative probiotics), was compared to a group of 500 patients (control group) operated on between March 2015 and November 30, 2020, who received a standard ERAS protocol. In the MIRACLe Group only 1 anastomotic leak was registered. In this group the incidence of AL was just 1.7% vs. 6.4% in the control group (p = 0.238) and the incidence of surgical site infections (1.7% vs. 3.6%; p = 0.686), reoperations (1.7% vs. 4.2%; p = 0.547) and postoperative mortality (0% vs. 2.2%; p = 0.504) were lower. The postoperative outcomes were also better: the times to first flatus, to first stool and to oral feeding were shorter (1 vs. 2, 2 vs. 3 and 2 vs. 3 days, respectively; p < 0.001). Additionally, the postoperative recovery was faster, with a shorter time to discharge (4 vs. 6 days; p < 0.001). In this pilot study, the MIRACLe protocol appeared to be safe and considerably reduced anastomotic leaks in elective laparoscopic colorectal surgery for cancer, even if not statistically significant, due to the small number of cases.
Identifiants
pubmed: 35739383
doi: 10.1007/s13304-022-01305-6
pii: 10.1007/s13304-022-01305-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1253-1262Informations de copyright
© 2022. Italian Society of Surgery (SIC).
Références
AIOM. I Numeri del cancro in Italia 2021, 11th edition. https://www.aiom.it/wp-content/uploads/2021/10/2021_NumeriCancro_web
Hazebroek EJ, The Color Study Group (2002) Color. Surg Endosc. https://doi.org/10.1007/s00464-001-8165-z
doi: 10.1007/s00464-001-8165-z
pubmed: 12165825
Tjandra JJ, Chan MK (2006) Systematic review on the short-term outcome of laparoscopic resection for colon and rectosigmoid cancer. Colorectal Dis. https://doi.org/10.1111/j.1463-1318.2006.00974.x
doi: 10.1111/j.1463-1318.2006.00974.x
pubmed: 16970571
Kuhry E, Schwenk WF, Gaupset R, Romild U, Bonjer HJ (2008) Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD003432.pub2
doi: 10.1002/14651858.CD003432.pub2
pubmed: 18425886
pmcid: 7017639
Rahbari NN, Weitz J, Hohenberger W et al (2010) Definition and grading of anastomotic leakage following anterior resection of the rectum: a proposal by the International Study Group of Rectal Cancer. Surgery. https://doi.org/10.1016/j.surg.2009.10.012
doi: 10.1016/j.surg.2009.10.012
pubmed: 21134548
Shogan BD, Carlisle EM, Alverdy JC, Umanskiy K (2013) Do we really know why colorectal anastomoses leak? J Gastrointest Surg. https://doi.org/10.1007/s11605-013-2227-0
doi: 10.1007/s11605-013-2227-0
pubmed: 23690209
Okada M, Bothin C, Kanazawa K, Midtvedt T (1999) Experimental study of the influence of intestinal flora on the healing of intestinal anastomoses. Br J Surg. https://doi.org/10.1046/j.1365-2168.1999.01161.x
doi: 10.1046/j.1365-2168.1999.01161.x
pubmed: 10504368
Cohn I Jr, Rives JD (1955) Antibiotic protection of colon anastomoses. Ann Surg 141(5):707–717
doi: 10.1097/00000658-195505000-00016
Guyton K, Alverdy JC (2016) The gut microbiota and gastrointestinal surgery. Nat Rev Gastroenterol Hepatol. https://doi.org/10.1038/nrgastro.2016.139
doi: 10.1038/nrgastro.2016.139
pubmed: 27729657
Shogan BD, Smith DP, Christley S, Gilbert JA, Zaborina O, Alverdy JC (2014) Intestinal anastomotic injury alters spatially defined microbiome composition and function. Microbiome. https://doi.org/10.1186/2049-2618-2-35
doi: 10.1186/2049-2618-2-35
pubmed: 25250176
pmcid: 4171717
https://www.clinicaltrials.gov/ct2/show/NCT05164887?term=miracle&draw=2&rank=4
Clavien PA, Barkun J, de Oliveira ML et al (2009) The Clavien-Dindo classifications of surgical complications. Five-years experiences. Ann Surg 250:187–196
doi: 10.1097/SLA.0b013e3181b13ca2
Grieco M, Pernazza G, Gasparrini M et al (2019) The “Lazio network” experience. The first Italian regional research group on the enhanced recovery after surgery (ERAS) program. A collective database with 1200 patients in 2016–2017. Ann Ital Chir 90:157–161
pubmed: 31182694
Grieco M, Lorenzon L, Pernazza G, Carlini M, Brescia A, Santoro R, Crucitti A, Palmieri RM, Santoro E, Stipa F, Sacchi M, Persiani R (2020) Impact of implementation of the ERAS program in colorectal surgery: a multi-center study based on the “Lazio network” collective database. Int J Colorectal Dis. https://doi.org/10.1007/s00384-019-03496-8
doi: 10.1007/s00384-019-03496-8
pubmed: 31897650
Boyce SA, Harris C, Stevenson A, Lumley J, Clark D (2017) Management of low colorectal anastomotic leakage in the laparoscopic era: more than a decade of experience. Dis Colon Rectum 60(8):807–814
doi: 10.1097/DCR.0000000000000822
Lee SW, Gregory D, Cool CL (2020) Clinical and economic burden of colorectal and bariatric anastomotic leaks. Surg Endosc. https://doi.org/10.1007/s00464-019-07210-1
doi: 10.1007/s00464-019-07210-1
pubmed: 33201313
pmcid: 7644542
Grieco M, Cassini D, Spoletini D, Soligo E, Grattarola E, Baldazzi G, Testa S, Carlini M (2019) Laparoscopic resection of splenic flexure colon cancers: a retrospective multi-center study with 117 cases. Updates Surg. https://doi.org/10.1007/s13304-018-0601-x
doi: 10.1007/s13304-018-0601-x
pubmed: 30406933
Grieco M, Cassini D, Spoletini D, Soligo E, Grattarola E, Baldazzi G, Testa S, Carlini M (2019) Intracorporeal versus extracorporeal anastomosis for laparoscopic resection of the splenic flexure colon cancer: a multicenter propensity score analysis. Surg Laparosc Endosc Percutan Tech. https://doi.org/10.1097/SLE.0000000000000653
doi: 10.1097/SLE.0000000000000653
pubmed: 30817694
Grieco M, Spoletini D, Marcasciano M, Grattarola E, Shihab V, Carlini M (2020) Subcuticular sutures in laparoscopic colorectal surgery: a comparative study to evaluate wound infection rates and cosmetic results. Updates Surg. https://doi.org/10.1007/s13304-020-00740-7
doi: 10.1007/s13304-020-00740-7
pubmed: 32306277
Grieco M, Apa D, Spoletini D, Grattarola E, Carlini M (2018) Major vessel sealing in laparoscopic surgery for colorectal cancer: a single-center experience with 759 patients. World J Surg Oncol. https://doi.org/10.1186/s12957-018-1402-x
doi: 10.1186/s12957-018-1402-x
pubmed: 29859101
pmcid: 5984822
Edomskis P, Goudberg MR, Sparreboom CL, Menon AG, Wolthuis AM, D’Hoore A, Lange JF (2021) Matrix metalloproteinase-9 in relation to patients with complications after colorectal surgery: a systematic review. Int J Colorectal Dis. https://doi.org/10.1007/s00384-020-03724-6
doi: 10.1007/s00384-020-03724-6
pubmed: 32865714
Riccio P, Rossano R (2020) The human gut microbiota is neither an organ nor a commensal. FEBS Lett. https://doi.org/10.1002/1873-3468.13946
doi: 10.1002/1873-3468.13946
pubmed: 33011965
Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature. https://doi.org/10.1038/nature11552
doi: 10.1038/nature11552
pubmed: 22972297
Flint HJ, Scott KP, Louis P, Duncan SH (2012) The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. https://doi.org/10.1038/nrgastro.2012.156
doi: 10.1038/nrgastro.2012.156
pubmed: 22945443
Bachmann R, Leonard D, Delzenne N, Kartheuser A, Cani PD (2017) Novel insight into the role of microbiota in colorectal surgery. Gut 66(4):738–749
doi: 10.1136/gutjnl-2016-312569
Earley ZM, Akhtar S, Green SJ, Naqib A, Khan O, Cannon AR, Hammer AM, Morris NL, Li X, Eberhardt JM, Gamelli RL, Kennedy RH, Choudhry MA (2015) Burn injury alters the intestinal microbiome and increases gut permeability and bacterial translocation. PLoS ONE 10(7):e0129996
doi: 10.1371/journal.pone.0129996
Shimizu K, Ogura H, Asahara T, Nomoto K, Matsushima A, Hayakawa K, Ikegawa H, Tasaki O, Kuwagata Y, Shimazu T (2015) Gut microbiota and environment in patients with major burns—a preliminary report. Burns. https://doi.org/10.1016/j.burns.2014.10.019
doi: 10.1016/j.burns.2014.10.019
pubmed: 25465986
Seal JB, Morowitz M, Zaborina O, An G, Alverdy JC (2010) The molecular Koch’s postulates and surgical infection: a view forward. Surgery. https://doi.org/10.1016/j.surg.2010.03.008
doi: 10.1016/j.surg.2010.03.008
pubmed: 20494210
Shogan BD, Belogortseva N, Luong PM, Zaborin A, Lax S, Bethel C, Ward M, Muldoon JP, Singer M, An G, Umanskiy K, Konda V, Shakhsheer B, Luo J, Klabbers R, Hancock LE, Gilbert J, Zaborina O, Alverdy JC (2015) Collagen degradation and MMP9 activation by Enterococcus faecalis contribute to intestinal anastomotic leak. Sci Transl Med. 7(286):286ra68
doi: 10.1126/scitranslmed.3010658
Olivas AD, Shogan BD, Valuckaite V, Zaborin A, Belogortseva N, Musch M, Meyer F, Trimble WL, An G, Gilbert J, Zaborina O, Alverdy JC (2012) Intestinal tissues induce an SNP mutation in Pseudomonas aeruginosa that enhances its virulence: possible role in anastomotic leak. PLoS ONE. https://doi.org/10.1371/journal.pone.0044326
doi: 10.1371/journal.pone.0044326
pubmed: 22952955
pmcid: 3432121
van Praagh JB, de Goffau MC, Bakker IS, Harmsen HJ, Olinga P, Havenga K (2016) Intestinal microbiota and anastomotic leakage of stapled colorectal anastomoses: a pilot study. Surg Endosc. https://doi.org/10.1007/s00464-015-4508-z
doi: 10.1007/s00464-015-4508-z
pubmed: 26385781
van Praagh JB, de Goffau MC, Bakker IS, van Goor H, Harmsen HJM, Olinga P, Havenga K (2019) Mucus microbiome of anastomotic tissue during surgery has predictive value for colorectal anastomotic leakage. Ann Surg 269(5):911–916
doi: 10.1097/SLA.0000000000002651
Alverdy JC, Hyman N, Gilbert J, Luo JN, Krezalek M (2017) Preparing the bowel for surgery: learning from the past and planning for the future. J Am Coll Surg 225(2):324–332
doi: 10.1016/j.jamcollsurg.2017.05.005
Kiran RP, Murray AC, Chiuzan C, Estrada D, Forde K (2015) Combined preoperative mechanical bowel preparation with oral antibiotics significantly reduces surgical site infection, anastomotic leak, and ileus after colorectal surgery. Ann Surg 262(3):416–425
doi: 10.1097/SLA.0000000000001416
Jalanka J, Salonen A, Salojärvi J, Ritari J, Immonen O, Marciani L, Gowland P, Hoad C, Garsed K, Lam C, Palva A, Spiller RC, de Vos WM (2015) Effects of bowel cleansing on the intestinal microbiota. Gut 64(10):1562–1568
doi: 10.1136/gutjnl-2014-307240
Slim K, Vicaut E, Panis Y, Chipponi J (2004) Meta-analysis of randomized clinical trials of colorectal surgery with or without mechanical bowel preparation. Br J Surg. https://doi.org/10.1002/bjs.4651
doi: 10.1002/bjs.4651
pubmed: 15449262
Slim K, Vicaut E, Launay-Savary MV, Contant C, Chipponi J (2009) Updated systematic review and meta-analysis of randomized clinical trials on the role of mechanical bowel preparation before colorectal surgery. Ann Surg 249(2):203–209
doi: 10.1097/SLA.0b013e318193425a
Nichols RL, Broido P, Condon RE et al (1973) Effect of preoperative neomycin-erythromycin intestinal preparation on the incidence of infectious complications following colon surgery. Ann Surg 178:453–462
doi: 10.1097/00000658-197310000-00008
Matheson DM, Arabi Y, Baxter-Smith D et al (1978) Randomized multicenter trial of oral bowel preparation and microbials for elective colorectal operations. BJS. https://doi.org/10.1002/bjs.1800650902
doi: 10.1002/bjs.1800650902
Migaly J, Baford AC, Francone TD et al (2019) 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 62(1):3–8
doi: 10.1097/DCR.0000000000001238
Ambe PC, Zarras K, Stodolski M, Wirjawan I, Zirngibl H (2019) Routine preoperative mechanical bowel preparation with additive oral antibiotics is associated with a reduced risk of anastomotic leakage in patients undergoing elective oncologic resection for colorectal cancer. World J Surg Oncol. https://doi.org/10.1186/s12957-019-1563-2
doi: 10.1186/s12957-019-1563-2
pubmed: 30651119
pmcid: 6335695
Zhang LM, Schuitevoerder D, White MG, Feldt S, Krishnan P, Hyman N, Shogan BD (2021) Combined mechanical and oral antibiotic bowel preparation is associated with prolonged recurrence-free survival following surgery for colorectal cancer. J Surg Oncol. https://doi.org/10.1002/jso.26619
doi: 10.1002/jso.26619
pubmed: 34918842
pmcid: 8453976
Mizuta M, Endo I, Yamamoto S, Inokawa H, Kubo M, Udaka T, Sogabe O, Maeda H, Shirakawa K, Okazaki E, Odamaki T, Abe F, Xiao JZ (2016) Perioperative supplementation with bifidobacteria improves postoperative nutritional recovery, inflammatory response, and fecal microbiota in patients undergoing colorectal surgery: a prospective, randomized clinical trial. Biosci Microbiota Food Health 35(2):77–87
doi: 10.12938/bmfh.2015-017
Kotzampassi K, Stavrou G, Damoraki G, Georgitsi M, Basdanis G, Tsaousi G, Giamarellos-Bourboulis EJ (2015) A four-probiotics regimen reduces postoperative complications after colorectal surgery: a randomized, double-blind, placebo-controlled study. World J Surg. https://doi.org/10.1007/s00268-015-3071-z
doi: 10.1007/s00268-015-3071-z
pubmed: 25894405
Cheng FS, Pan D, Chang B, Jiang M, Sang LX (2020) Probiotic mixture VSL#3: an overview of basic and clinical studies in chronic diseases. World J Clin Cases 8(8):1361–1384
doi: 10.12998/wjcc.v8.i8.1361
Grieco M, Marcellinaro R, Spoletini D, Menditto R, Lisi G, Russo G, Napoleone V, Carlini M (2022) Laparoscopic right colectomy: changes in surgical technique and perioperative management allow better postoperative results in a comparative series of 361 patients. Updates Surg. https://doi.org/10.1007/s13304-022-01287-5 (Epub ahead of print. PMID: 35412267)
doi: 10.1007/s13304-022-01287-5
pubmed: 35739383