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Journal of Gastrointestinal Surgery

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01-09-2013 | Original Article

Significant Changes in the Intestinal Environment After Surgery in Patients with Colorectal Cancer

Authors: Seiji Ohigashi, Kazuki Sudo, Daiki Kobayashi, Takuya Takahashi, Koji Nomoto, Hisashi Onodera

Published in: Journal of Gastrointestinal Surgery | Issue 9/2013

Abstract

Background

There have been very few detailed reports of the intestinal environment after surgical treatment for colorectal cancer (CRC). We analysed faecal microbiota, organic acids and pH to investigate the influence of colorectal surgery on the intestinal environment.

Methods

Faecal samples from 81 CRC patients were collected before the start of pre-operative preparation the day before surgery, as well as 7 days or more after surgery. Thirteen groups of intestinal microbiota, eight types of organic acids, and pH were measured using 16S rRNA-targeted reverse transcription-quantitative PCR, high-performance liquid chromatography and a pH meter, respectively.

Results

Total bacterial counts (10.3 ± 0.6 vs. 9.4 ± 1.2 log₁₀ cells/g; p < 0.001) and the numbers of 6 groups of obligate anaerobes were significantly decreased after surgery. In contrast, the populations of Enterobacteriaceae, Enterococcus, Staphylococcus and Pseudomonas were significantly increased. Post-operatively, the concentration of total organic acids was lower (77.9 ± 40.1 vs. 50.1 ± 37.0 μmol/g; p < 0.001) than the pre-operative concentration, and a significant reduction in short-chain fatty acids (SCFAs) was observed.

Conclusion

Significant changes in the intestinal environment, including marked decreases in obligate anaerobes, increases in pathogenic bacteria, and reductions in SCFAs, were detected after surgery for CRC.

Pendlimari R, Cima RR, Wolff BG, Pemberton JH, Huebner M. Diagnoses influence surgical site infections (SSI) in colorectal surgery: a must consideration for SSI reporting programs? J Am Coll Surg. 2012; 214(4):574–580; discussion 580–581PubMedCrossRef

Gervaz P, Bandiera-Clerc C, Buchs NC, Eisenring MC, Troillet N, Perneger T, Harbarth S. Scoring system to predict the risk of surgical-site infection after colorectal resection. Br J Surg. 2012;99(4):589–595.PubMedCrossRef

Kashimura N, Kusachi S, Konishi T, Shimizu J, Kusunoki M, Oka M, Wakatsuki T, Sumiyama Y. Impact of surgical site infection after colorectal surgery on hospital stay and medical expenditure in Japan. Surg Today. 2012;42(7):639–645.PubMedCrossRef

Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–1359.PubMedCrossRef

Neish AS. Microbes in gastrointestinal health and disease. Gastroenterology. 2009;136(1):65–80.PubMedCrossRef

Hooper LV, Gordon JI. Commensal host–bacterial relationships in the gut. Science. 2001;292(5519):1115–1118.PubMedCrossRef

Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol. 2001;108(4):516–520.PubMedCrossRef

Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–1031.PubMedCrossRef

Rawls JF. Enteric infection and inflammation alter gut microbial ecology. Cell Host Microbe. 2007;2(2):73–74.PubMedCrossRef

10.

Candela M, Guidotti M, Fabbri A, Brigidi P, Franceschi C, Fiorentini C. Human intestinal microbiota: cross-talk with the host and its potential role in colorectal cancer. Crit Rev Microbiol. 2011;37(1):1–14.PubMedCrossRef

11.

Ohigashi S, Sudo K, Kobayashi D, Takahashi O, Takahashi T, Asahara T, Nomoto K, Onodera H. Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer. Dig Dis Sci. 2013;58(6):1717–1726.

12.

Lassen K, Soop M, Nygren J, Cox PB, Hendry PO, Spies C, von Meyenfeldt MF, Fearon KC, Revhaug A, Norderval S, Ljungqvist O, Lobo DN, Dejong CH. Consensus review of optimal perioperative care in colorectal surgery: Enhanced Recovery After Surgery (ERAS) Group recommendations. Arch Surg. 2009;144(10):961–969.PubMedCrossRef

13.

Liu Z, Qin H, Yang Z, Xia Y, Liu W, Tang J, Jiang Y, Zhang H, Yang A, Wang Y, Zheng Q. 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. 2011;33(1):50–63.PubMedCrossRef

14.

Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol. 2004;70(12):7220–7228.PubMedCrossRef

15.

Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635–1638.PubMedCrossRef

16.

Matsuda K, Tsuji H, Asahara T, Kado Y, Nomoto K. Sensitive quantitative detection of commensal bacteria by rRNA-targeted reverse transcription-PCR. Appl Environ Microbiol. 2007;73(1):32–39.PubMedCrossRef

17.

Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. 2006;40(3):235–243.PubMedCrossRef

18.

Shimizu K, Ogura H, Goto M, Asahara T, Nomoto K, Morotomi M, Yoshiya K, Matsushima A, Sumi Y, Kuwagata Y, Tanaka H, Shimazu T, Sugimoto H. Altered gut flora and environment in patients with severe SIRS. J Trauma. 2006;60(1):126–133.PubMedCrossRef

19.

MacFie J, O’Boyle C, Mitchell CJ, Buckley PM, Johnstone D, Sudworth P. Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity. Gut. 1999;45(2):223–228.PubMedCrossRef

20.

Sugawara G, Nagino M, Nishio H, Ebata T, Takagi K, Asahara T, Nomoto K, Nimura Y. Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg. 2006;244(5):706–714.PubMedCrossRef

21.

Clark JA, Coopersmith CM. Intestinal crosstalk: a new paradigm for understanding the gut as the “motor” of critical illness. Shock. 2007;28(4):384–393.PubMedCrossRef

22.

Scheppach W. Effects of short chain fatty acids on gut morphology and function. Gut. 1994;35(1 Suppl):S35-38.PubMedCrossRef

23.

Augenlicht LH, Mariadason JM, Wilson A, Arango D, Yang W, Heerdt BG, Velcich A. Short chain fatty acids and colon cancer. J Nutr. 2002;132(12):3804S-3808S.PubMed

24.

Shimizu K, Ogura H, Asahara T, Nomoto K, Morotomi M, Tasaki O, Matsushima A, Kuwagata Y, Shimazu T, Sugimoto H. Probiotic/synbiotic therapy for treating critically ill patients from a gut microbiota perspective. Dig Dis Sci. 2013;58(1):23–32.PubMedCrossRef

25.

Pitsouni E, Alexiou V, Saridakis V, Peppas G, Falagas ME. Does the use of probiotics/synbiotics prevent postoperative infections in patients undergoing abdominal surgery? A meta-analysis of randomized controlled trials. Eur J Clin Pharmacol. 2009;65(6):561–570.PubMedCrossRef

26.

Reddy BS, Macfie J, Gatt M, Larsen CN, Jensen SS, Leser TD. Randomized clinical trial of effect of synbiotics, neomycin and mechanical bowel preparation on intestinal barrier function in patients undergoing colectomy. Br J Surg. 2007;94(5):546–554.PubMedCrossRef

27.

Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, Nieuwenhuijs VB, Bollen TL, van Ramshorst B, Witteman BJ, Rosman C, Ploeg RJ, Brink MA, Schaapherder AF, Dejong CH, Wahab PJ, van Laarhoven CJ, vam der Harst E, van Eijck CH, Cuesta MA, Akkermans LM, Gooszen HG. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet. 2008;371(9613):651–659.PubMedCrossRef

28.

Pineda CE, Shelton AA, Hernandez-Boussard T, Morton JM, Welton ML. Mechanical bowel preparation in intestinal surgery: a meta-analysis and review of the literature. J Gastrointest Surg. 2008;12(11):2037–2044.PubMedCrossRef

29.

Harrell L, Wang Y, Antonopoulos D, Young V, Lichtenstein L, Huang Y, Hanauer S, Chang E. Standard colonic lavage alters the natural state of mucosal-associated microbiota in the human colon. PLoS One. 2012;7(2):e32545.PubMedCrossRef

30.

Bucher P, Gervaz P, Egger JF, Soravia C, Morel P. Morphologic alterations associated with mechanical bowel preparation before elective colorectal surgery: a randomized trial. Dis Colon Rectum. 2006;49(1):109–112.PubMedCrossRef

Title: Significant Changes in the Intestinal Environment After Surgery in Patients with Colorectal Cancer
Authors: Seiji Ohigashi
Kazuki Sudo
Daiki Kobayashi
Takuya Takahashi
Koji Nomoto
Hisashi Onodera
Publication date: 01-09-2013
Publisher: Springer US
Published in: Journal of Gastrointestinal Surgery / Issue 9/2013
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI: https://doi.org/10.1007/s11605-013-2270-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Significant Changes in the Intestinal Environment After Surgery in Patients with Colorectal Cancer

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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