Current State of Knowledge on Implications of Gut Microbiome for Surgical Conditions

  • Edmund B. Chen
  • Cori Cason
  • Jack A. Gilbert
  • Karen J. Ho
Review Article

Abstract

The role of the microbiome in human health has become a central tenant of current medical research, infiltrating a diverse disciplinary base whereby microbiology, computer science, ecology, gastroenterology, immunology, neurophysiology and psychology, metabolism, and cardiovascular medicine all intersect. Traditionally, commensal gut microbiota have been assumed to play a significant role only in the metabolic processing of dietary nutrients and host metabolites, the fortification of gut epithelial barrier function, and the development of mucosal immunity. However, over the last 20 years, new technologies and renewed interest have uncovered a considerably broader influence of the microbiota on health maintenance and disease development, many of which are of particular relevance for surgeons. This article provides a broad overview of the current state of knowledge and a review of the technology that helped in their formation.

Keywords

Microbiota Gastrointestinal tract Medicine 

Notes

Author Contributions

All authors contributed to the conception, acquisition, and analysis of data; drafting and critical revision of the manuscript; gave final approval to the manuscript; and accept accountability for all aspects of the work.

References

  1. 1.
    Sender R, Fuchs S, Milo R. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell. 2016;164:337–340CrossRefPubMedGoogle Scholar
  2. 2.
    Cho I, Blaser MJ. The human microbiome: At the interface of health and disease. Nat Rev Genet. 2012;13:260–270CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–214CrossRefGoogle Scholar
  4. 4.
    Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355–1359CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Hutkins RW, Krumbeck JA, Bindels LB, Cani PD, Fahey G, Jr., Goh YJ, et al. Prebiotics: Why definitions matter. Curr Opin Biotechnol. 2016;37:1–7CrossRefPubMedGoogle Scholar
  7. 7.
    Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11:506–514CrossRefPubMedGoogle Scholar
  8. 8.
    Fraher MH, O'Toole PW, Quigley EM. Techniques used to characterize the gut microbiota: A guide for the clinician. Nat Rev Gastroenterol Hepatol. 2012;9:312–322CrossRefPubMedGoogle Scholar
  9. 9.
    Matsen FAt. Phylogenetics and the human microbiome. Syst Biol. 2015;64:e26–41CrossRefGoogle Scholar
  10. 10.
    Sweeney TE, Morton JM. The human gut microbiome: A review of the effect of obesity and surgically induced weight loss. JAMA Surg. 2013;148:563–569CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Magouliotis DE, Tasiopoulou VS, Sioka E, Chatedaki C, Zacharoulis D. Impact of bariatric surgery on metabolic and gut microbiota profile: A systematic review and meta-analysis. Obes Surg. 2017;27:1345–1357CrossRefPubMedGoogle Scholar
  12. 12.
    Bashiardes S, Shapiro H, Rozin S, Shibolet O, Elinav E. Non-alcoholic fatty liver and the gut microbiota. Molecular Metabolism. 2016;5:782–794CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Leung C, Rivera L, Furness JB, Angus PW. The role of the gut microbiota in nafld. Nat Rev Gastroenterol Hepatol. 2016;13:412–425CrossRefPubMedGoogle Scholar
  14. 14.
    Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases. Gastroenterology. 2014;146:1513–1524CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell host & microbe. 2014;15:317–328CrossRefGoogle Scholar
  16. 16.
    Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol. 2014;12:661–672CrossRefPubMedGoogle Scholar
  17. 17.
    Gagniere J, Raisch J, Veziant J, Barnich N, Bonnet R, Buc E, et al. Gut microbiota imbalance and colorectal cancer. World J Gastroenterol. 2016;22:501–518CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Guyton K, Alverdy JC. The gut microbiota and gastrointestinal surgery. Nat Rev Gastroenterol Hepatol. 2017;14:43–54CrossRefPubMedGoogle Scholar
  19. 19.
    Chassaing B, Darfeuille-Michaud A. The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology. 2011;140:1720–1728CrossRefPubMedGoogle Scholar
  20. 20.
    Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: Current status and the future ahead. Gastroenterology. 2014;146:1489–1499CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Manichanh C, Borruel N, Casellas F, Guarner F. The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol. 2012;9:599–608CrossRefPubMedGoogle Scholar
  22. 22.
    Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Folsch UR, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53:685–693Google Scholar
  23. 23.
    Tang WH, Kitai T, Hazen SL. Gut microbiota in cardiovascular health and disease. Circ Res. 2017;120:1183–1196CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America. 2005;102:11070–11075CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    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;444:1027–1031CrossRefPubMedGoogle Scholar
  26. 26.
    Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: Human gut microbes associated with obesity. Nature. 2006;444:1022–1023CrossRefPubMedGoogle Scholar
  27. 27.
    Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541–546CrossRefPubMedGoogle Scholar
  28. 28.
    Pallister T, Jackson MA, Martin TC, Glastonbury CA, Jennings A, Beaumont M, et al. Untangling the relationship between diet and visceral fat mass through blood metabolomics and gut microbiome profiling. Int J Obes (Lond). 2017;41:1106–1113CrossRefPubMedCentralGoogle Scholar
  29. 29.
    Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, et al. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe. 2015;17:681–689CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Liu R, Hong J, Xu X, Feng Q, Zhang D, Gu Y, et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat Med. 2017;23:859–868Google Scholar
  31. 31.
    Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110:9066–9071CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Serino M, Luche E, Gres S, Baylac A, Berge M, Cenac C, et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut. 2012;61:543–553CrossRefPubMedGoogle Scholar
  33. 33.
    Neyrinck AM, Van Hee VF, Bindels LB, De Backer F, Cani PD, Delzenne NM. Polyphenol-rich extract of pomegranate peel alleviates tissue inflammation and hypercholesterolaemia in high-fat diet-induced obese mice: Potential implication of the gut microbiota. Br J Nutr. 2013;109:802–809CrossRefPubMedGoogle Scholar
  34. 34.
    Anhe FF, Roy D, Pilon G, Dudonne S, Matamoros S, Varin TV, et al. A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased akkermansia spp. Population in the gut microbiota of mice. Gut. 2015;64:872–883CrossRefPubMedGoogle Scholar
  35. 35.
    Buchwald H, Estok R, Fahrbach K, Banel D, Sledge I. Trends in mortality in bariatric surgery: A systematic review and meta-analysis. Surgery. 2007;142:621–632; discussion 632-625CrossRefPubMedGoogle Scholar
  36. 36.
    Liou AP, Paziuk M, Luevano JM, Jr., Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5:178ra141CrossRefGoogle Scholar
  37. 37.
    Tremaroli V, Karlsson F, Werling M, Stahlman M, Kovatcheva-Datchary P, Olbers T, et al. Roux-en-y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab. 2015;22:228–238CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: Links with metabolic and low-grade inflammation markers. Diabetes. 2010;59:3049–3057CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009;106:2365–2370CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Samuel BS, Gordon JI. A Humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proceedings of the National Academy of Sciences of the United States of America. 2006;103:10011–10016CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Jahansouz C, Staley C, Bernlohr DA, Sadowsky MJ, Khoruts A, Ikramuddin S. Sleeve gastrectomy drives persistent shifts in the gut microbiome. Surgery for obesity and related diseases: official journal of the American Society for Bariatric Surgery. 2017;13:916–924CrossRefGoogle Scholar
  42. 42.
    Rinella ME. Nonalcoholic fatty liver disease: A systematic review. JAMA. 2015;313:2263–2273CrossRefPubMedGoogle Scholar
  43. 43.
    Dawes EA, Foster SM. The formation of ethanol in Escherichia coli. Biochimica et biophysica acta. 1956;22:253–265CrossRefPubMedGoogle Scholar
  44. 44.
    Zhu L, Baker SS, Gill C, Liu W, Alkhouri R, Baker RD, et al. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: A connection between endogenous alcohol and nash. Hepatology. 2013;57:601–609CrossRefPubMedGoogle Scholar
  45. 45.
    Cope K, Risby T, Diehl AM. Increased gastrointestinal ethanol production in obese mice: Implications for fatty liver disease pathogenesis. Gastroenterology. 2000;119:1340–1347CrossRefPubMedGoogle Scholar
  46. 46.
    Adachi Y, Moore LE, Bradford BU, Gao W, Thurman RG. Antibiotics prevent liver injury in rats following long-term exposure to ethanol. Gastroenterology. 1995;108:218–224CrossRefPubMedGoogle Scholar
  47. 47.
    Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472:57–63CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Kucera O, Cervinkova Z. Experimental models of non-alcoholic fatty liver disease in rats. World J Gastroenterol. 2014;20:8364–8376CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Dumas M-E, Barton RH, Toye A, Cloarec O, Blancher C, Rothwell A, et al. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proceedings of the National Academy of Sciences. 2006;103:12511–12516CrossRefGoogle Scholar
  50. 50.
    Peterson LW, Artis D. Intestinal epithelial cells: Regulators of barrier function and immune homeostasis. Nature reviews. Immunology. 2014;14:141–153CrossRefPubMedGoogle Scholar
  51. 51.
    Gäbele E, Dostert K, Hofmann C, Wiest R, Schölmerich J, Hellerbrand C, et al. DSS induced colitis increases portal LPS levels and enhances hepatic inflammation and fibrogenesis in experimental NASH. Journal of Hepatology. 2011;55:1391–1399CrossRefPubMedGoogle Scholar
  52. 52.
    Mencin A, Kluwe J, Schwabe RF. Toll-like receptors as targets in chronic liver diseases. Gut. 2009;58:704–720CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology. 2009;49:1877–1887CrossRefPubMedGoogle Scholar
  54. 54.
    Keusch GT. Opportunistic infections in colon carcinoma. Am J Clin Nutr. 1974;27:1481–1485CrossRefPubMedGoogle Scholar
  55. 55.
    Waisberg J, Matheus Cde O, Pimenta J. Infectious endocarditis from streptococcus bovis associated with colonic carcinoma: Case report and literature review. Arquivos de gastroenterologia. 2002;39:177–180CrossRefPubMedGoogle Scholar
  56. 56.
    Abdulamir AS, Hafidh RR, Bakar FA. Molecular detection, quantification, and isolation of streptococcus gallolyticus bacteria colonizing colorectal tumors: Inflammation-driven potential of carcinogenesis via IL-1, cox-2, and IL-8. Molecular Cancer. 2010;9:249CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Wang X, Allen TD, May RJ, Lightfoot S, Houchen CW, Huycke MM. Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect. Cancer research. 2008;68:9909–9917CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Soler AP, Miller RD, Laughlin KV, Carp NZ, Klurfeld DM, Mullin JM. Increased tight junctional permeability is associated with the development of colon cancer. Carcinogenesis. 1999;20:1425–1432CrossRefPubMedGoogle Scholar
  59. 59.
    Vizcaino MI, Crawford JM. The colibactin warhead crosslinks DNA. Nat Chem. 2015;7:411–417CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Bernstein H, Bernstein C, Payne CM, Dvorak K. Bile acids as endogenous etiologic agents in gastrointestinal cancer. World J Gastroenterol. 2009;15:3329–3340CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Reddy BS. Types and amount of dietary fat and colon cancer risk: Prevention by omega-3 fatty acid-rich diets. Environmental Health and Preventive Medicine. 2002;7:95–102CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Sanapareddy N, Legge RM, Jovov B, McCoy A, Burcal L, Araujo-Perez F, et al. Increased rectal microbial richness is associated with the presence of colorectal adenomas in humans. Isme J. 2012;6:1858–1868CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Nakatsu G, Li X, Zhou H, Sheng J, Wong SH, Wu WK, et al. Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat Commun. 2015;6:8727CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Gao Z, Guo B, Gao R, Zhu Q, Qin H. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol. 2015;6:20PubMedPubMedCentralGoogle Scholar
  65. 65.
    Yu J, Feng Q, Wong SH, Zhang D, Liang QY, Qin Y, et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut. 2015Google Scholar
  66. 66.
    Alves A, Panis Y, Trancart D, Regimbeau J-M, Pocard M, Valleur P. Factors associated with clinically significant anastomotic leakage after large bowel resection: Multivariate analysis of 707 patients. World Journal of Surgery. 2002;26:499–502CrossRefPubMedGoogle Scholar
  67. 67.
    Cohn I, Jr., Rives JD. Antibiotic protection of colon anastomoses. Ann Surg. 1955;141:707–717CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Schardey HM, Joosten U, Finke U, Staubach KH, Schauer R, Heiss A, et al. The prevention of anastomotic leakage after total gastrectomy with local decontamination. A prospective, randomized, double-blind, placebo-controlled multicenter trial. Annals of Surgery. 1997;225:172–180CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Olivas AD, Shogan BD, Valuckaite V, Zaborin A, Belogortseva N, Musch M, et al. Intestinal tissues induce an SNP mutation in pseudomonas aeruginosa that enhances its virulence: Possible role in anastomotic leak. PloS one. 2012;7:e44326CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Shogan BD, Belogortseva N, Luong PM, Zaborin A, Lax S, Bethel C, et al. Collagen degradation and mmp9 activation by Enterococcus faecalis contribute to intestinal anastomotic leak. Science Translational Medicine. 2015;7:286ra268-286ra268Google Scholar
  71. 71.
    de Lange KM, Barrett JC. Understanding inflammatory bowel disease via immunogenetics. Journal of autoimmunity. 2015;64:91–100CrossRefPubMedGoogle Scholar
  72. 72.
    Sepehri S, Kotlowski R, Bernstein CN, Krause DO. Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease. Inflammatory bowel diseases. 2007;13:675–683CrossRefPubMedGoogle Scholar
  73. 73.
    Martinez C, Antolin M, Santos J, Torrejon A, Casellas F, Borruel N, et al. Unstable composition of the fecal microbiota in ulcerative colitis during clinical remission. Am J Gastroenterol. 2008;103:643–648CrossRefPubMedGoogle Scholar
  74. 74.
    Scanlan PD, Shanahan F, O'Mahony C, Marchesi JR. Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn’s disease. J Clin Microbiol. 2006;44:3980–3988CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology. 2004;127:412–421CrossRefPubMedGoogle Scholar
  76. 76.
    Lapaquette P, Glasser AL, Huett A, Xavier RJ, Darfeuille-Michaud A. Crohn’s disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly. Cellular microbiology. 2010;12:99–113CrossRefPubMedGoogle Scholar
  77. 77.
    Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE, et al. Reduced paneth cell alpha-defensins in ileal Crohn’s disease. Proc Natl Acad Sci U S A. 2005;102:18129–18134CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Barnich N, Carvalho FA, Glasser AL, Darcha C, Jantscheff P, Allez M, et al. Ceacam6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J Clin Invest. 2007;117:1566–1574CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Bringer MA, Glasser AL, Tung CH, Meresse S, Darfeuille-Michaud A. The Crohn’s disease-associated adherent-invasive Escherichia coli strain lf82 replicates in mature phagolysosomes within j774 macrophages. Cellular microbiology. 2006;8:471–484CrossRefPubMedGoogle Scholar
  80. 80.
    Glasser AL, Boudeau J, Barnich N, Perruchot MH, Colombel JF, Darfeuille-Michaud A. Adherent invasive Escherichia coli strains from patients with Crohn’s disease survive and replicate within macrophages without inducing host cell death. Infect Immun. 2001;69:5529–5537CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Ohkusa T, Sato N, Ogihara T, Morita K, Ogawa M, Okayasu I. Fusobacterium varium localized in the colonic mucosa of patients with ulcerative colitis stimulates species-specific antibody. Journal of gastroenterology and hepatology. 2002;17:849–853CrossRefPubMedGoogle Scholar
  82. 82.
    Ohkusa T, Okayasu I, Ogihara T, Morita K, Ogawa M, Sato N. Induction of experimental ulcerative colitis by fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis. Gut. 2003;52:79–83CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, et al. Low counts of faecalibacterium prausnitzii in colitis microbiota. Inflammatory bowel diseases. 2009;15:1183–1189CrossRefPubMedGoogle Scholar
  84. 84.
    Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105:16731–16736CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Llopis M, Antolin M, Carol M, Borruel N, Casellas F, Martinez C, et al. Lactobacillus casei downregulates commensals’ inflammatory signals in Crohn’s disease mucosa. Inflammatory bowel diseases. 2009;15:275–283CrossRefPubMedGoogle Scholar
  86. 86.
    Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, et al. The microbial metabolites, short chain fatty acids, regulate colonic treg cell homeostasis. Science (New York, N.Y.). 2013;341: https://doi.org/10.1126/science.1241165
  87. 87.
    Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome biology. 2012;13:R79CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Wright SD, Burton C, Hernandez M, Hassing H, Montenegro J, Mundt S, et al. Infectious agents are not necessary for murine atherogenesis. The Journal of experimental medicine. 2000;191:1437–1442CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Tang WH, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, et al. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med. 2013;368:1575–1584CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, et al. Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med. 2013;19:576–585CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Gregory JC, Buffa JA, Org E, Wang Z, Levison BS, Zhu W, et al. Transmission of atherosclerosis susceptibility with gut microbial transplantation. The Journal of biological chemistry. 2015;290:5647–5660CrossRefPubMedGoogle Scholar
  92. 92.
    Ghosh SS, Bie J, Wang J, Ghosh S. Oral supplementation with non-absorbable antibiotics or curcumin attenuates western diet-induced atherosclerosis and glucose intolerance in ldlr−/− mice—role of intestinal permeability and macrophage activation. PLoS One. 2014;9:e108577CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Karlsson FH, Fak F, Nookaew I, Tremaroli V, Fagerberg B, Petranovic D, et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Cason CA, Dolan KT, Sharma G, Tao M, Kulkarni R, Helenowski IB, et al. Plasma microbiome-modulated indole- and phenyl-derived metabolites associate with advanced atherosclerosis and post-operative outcomes. J Vasc Surg. 2017Google Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2018

Authors and Affiliations

  • Edmund B. Chen
    • 1
  • Cori Cason
    • 1
  • Jack A. Gilbert
    • 2
  • Karen J. Ho
    • 1
    • 3
  1. 1.Department of Surgery, Feinberg School of MedicineNorthwestern UniversityChicagoUSA
  2. 2.Department of SurgeryUniversity of ChicagoChicagoUSA
  3. 3.Division of Vascular Surgery, Feinberg School of MedicineNorthwestern UniversityChicagoUSA

Personalised recommendations