Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Gastrointestinal surgery and the gut microbiome: a systematic literature review

European Journal of Clinical Nutrition volume 75, pages 12–25 (2021)Cite this article

Subjects

Abstract

Background/objectives

The impact of gastrointestinal surgery on the profile of the human gut microbiome is not fully understood. This review aimed to identify whether there is a change to the profile of the gut microbiome as a result of gastrointestinal surgery.

Subjects/methods

In August 2018, a systematic literature search was conducted in Medline, PreMedline, Embase, CINAHL and The Cochrane Register of Clinical Trials, identifying and critically appraising studies which investigated changes to gut microbiome pre- and post-gastrointestinal surgery.

Results

Of 2512 results, 14 studies were included for analysis. All studies reported post-surgical change to the microbiome. In 9 of the 14 studies, prevalence of specific bacteria had significantly changed after surgery. Improved outcome was associated with higher levels of beneficial bacteria and greater microbiome diversity post-surgery.

Conclusion

There were methodological limitations in the included studies leading to uncertainty regarding the impact of gastrointestinal surgery alone on the microbiome profile. An ideal future model for research should encompass case-controlled or cohort design with longer term follow-up in a homogeneous patient group. Future research should seek to clarify the gold standard testing method and standardised timing for post-surgical microbiome sample collection. It is imperative that controls for confounders be put in place to attempt to identify the true association between gastrointestinal surgery and changes to gut microbiome.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1

Similar content being viewed by others

References

  1. Whelan K. Modification of the gastrointestinal microbiota and its application to clinical nutrition. J Hum Nutr Diet. 2012;25:297–9.

    PubMed  Google Scholar 

  2. Peat CM, Kleiman SC, Bulik CM, Carroll IM. The intestinal microbiome in bariatric surgery patients. Eur Eat Disord Rev. 2015;23:496–503.

    PubMed  PubMed Central  Google Scholar 

  3. Singh RK, Chang H-W, Yan D, Lee KM, Ucmak D, Wong K, et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med. 2017;15:73.

    PubMed  PubMed Central  Google Scholar 

  4. Sidhu M, van der Poorten D. The gut microbiome. Aust Fam Physician 2017;46:206–11.

    PubMed  Google Scholar 

  5. Bäckhed F, Fraser Claire M, Ringel Y, Sanders ME, Sartor RB, Sherman PM, et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe 2012;12:611–22.

    PubMed  Google Scholar 

  6. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–14.

    Google Scholar 

  7. Hollister EB, Gao C, Versalovic J. Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology. 2014;146:1449–58.

    PubMed  Google Scholar 

  8. Zheng S, Shao S, Qiao Z, Chen X, Piao C, Yu Y, et al. Clinical parameters and gut microbiome changes before and after surgery in thoracic aortic dissection in patients with gastrointestinal complications. Sci Rep. 2017;7:15228.

    PubMed  PubMed Central  Google Scholar 

  9. Zhang Y-J, Li S, Gan R-Y, Zhou T, Xu D-P, Li H-B. Impacts of gut bacteria on human health and diseases. Int J Mol Sci. 2015;16:7493–519.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. McIlroy J, Ianiro G, Mukhopadhya I, Hansen R, Hold GL. Review article: the gut microbiome in inflammatory bowel disease—avenues for microbial management. Aliment Pharmacol Ther. 2018;47:26–42.

    CAS  PubMed  Google Scholar 

  11. Wexler HM. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev. 2007;20:593–621.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Duvallet C, Gibbons SM, Gurry T, Irizarry RA, Alm EJ. Meta-analysis of gut microbiome studies identifies disease-specific and shared responses. Nat Commun. 2017;8:1784.

    PubMed  PubMed Central  Google Scholar 

  13. Guyton K, Alverdy JC. The gut microbiota and gastrointestinal surgery. Nat Rev Gastroenterol Hepatol. 2016;14:43–54.

    PubMed  Google Scholar 

  14. Scotti E, Boué S, Lo Sasso G, Zanetti F, Belcastro V, Poussin C, et al. Exploring the microbiome in health and disease: implications for toxicology. Toxicol Res Appl. 2017;1:1–37.

    Google Scholar 

  15. Galperin MY. Genome diversity of spore-forming firmicutes. Microbiol Spectr. 2013; 1: TBS-0015-2012. https://doi.org/10.1128/microbiolspectrum.TBS-0015-2012.

  16. Mizuta M, Endo I, Yamamoto S, Inokawa H, Kubo M, Udaka T, et al. 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. 2016;35:77–87.

    CAS  PubMed  Google Scholar 

  17. Neut C, Guillemot F, Colombel JF. Nitrate-reducing bacteria in diversion colitis: a clue to inflammation? Dig Dis Sci. 1997;42:2577–80.

    CAS  PubMed  Google Scholar 

  18. Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, et al. Genomics of actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev. 2007;71:495–548.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, et al. Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev. 2015;80:1–43.

    PubMed  PubMed Central  Google Scholar 

  20. Stavrou G, Kotzampassi K. Gut microbiome, surgical complications and probiotics. Ann Gastroenterol. 2017;30:45–53.

    PubMed  Google Scholar 

  21. Chen YPL. Bioinformatics for whole-genome shotgun sequencing of microbial communities. PLoS Comput Biol. 2005;1:e24.

    PubMed Central  Google Scholar 

  22. Morgan XC, Huttenhower C. Meta’omic analytic techniques for studying the intestinal microbiome. Gastroenterology. 2014;146:1437–48.e1.

    CAS  PubMed  Google Scholar 

  23. Valdes AM, Walter J, Segal E, Spector TD. Role of the gut microbiota in nutrition and health. Br J Med. 2018;361(Supp 1):36–44.

    Google Scholar 

  24. Joanna Briggs Institute. Critical appraisal tools. 2018. http://joannabriggs.org/research/critical-appraisal-tools.html. Accessed 2 Oct 2018.

  25. Joanna Briggs Institute. The JBI approach. 2018. http://joannabriggs.org/jbi-approach.html#tabbed-nav=Levels-of-Evidence. Accessed 2 Oct 2018.

  26. Almeida MG, Kiss DR, Zilberstein B, Quintanilha AG, Teixeira MG, Habr-Gama A. Intestinal mucosa-associated microflora in ulcerative colitis patients before and after restorative proctocolectomy with an ileoanal pouch. Dis Colon Rectum. 2008;51:1113–9.

    PubMed  Google Scholar 

  27. Neut C, Bulois P, Desreumaux P, Membre JM, Lederman E, Gambiez L, et al. Changes in the bacterial flora of the neoterminal ileum after ileocolonic resection for Crohn’s disease. Am J Gastroenterol. 2002;97:939–46.

    PubMed  Google Scholar 

  28. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán 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 USA. 2008;105:16731–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Marteau P, Lémann M, Seksik P, Laharie D, Colombel JF, Bouhnik Y, et al. Ineffectiveness of Lactobacillus johnsonii LA1 for prophylaxis of postoperative recurrence in Crohn’s disease: a randomised, double blind, placebo controlled GETAID trial. Gut. 2006;55:842–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. De Cruz P, Kang S, Wagner J, Buckley M, Sim WH, Prideaux L, et al. Association between specific mucosa-associated microbiota in Crohn’s disease at the time of resection and subsequent disease recurrence: a pilot study. J Gastroenterol Hepatol. 2015;30:268–78.

    PubMed  Google Scholar 

  31. Dey N, Soergel DA, Repo S, Brenner SE. Association of gut microbiota with postoperative clinical course in Crohn’s disease. BMC Gastroenterol. 2013;13:131.

    PubMed  PubMed Central  Google Scholar 

  32. Laffin M, Perry T, Park H, Gillevet P, Sikaroodi M, Kaplan GG, et al. Endospore-forming bacteria are associated with maintenance of remission following intestinal resection in Crohn’s disease. Gastroenterology. 2017;152:S192–3.

    Google Scholar 

  33. Wright EK, Kamm MA, Wagner J, Teo SM, De Cruz P, Hamilton AL, et al. Microbial factors associated with postoperative Crohn’s disease recurrence. J Crohns Colitis. 2017;11:191–203.

    PubMed  Google Scholar 

  34. Mondot S, Lepage P, Seksik P, Allez M, Tréton X, Bouhnik Y, et al. The GETAID group. Structural robustness of the gut mucosal microbiota is associated with Crohn’s disease remission after surgery. Gut. 2016;65:954–6.

    CAS  PubMed  Google Scholar 

  35. Feng X, Su Y, Jiang J, Ning L, Weiwei D, Zhiming W, et al. Changes in fecal and colonic mucosal microbiota of patients with refractory constipation after a subtotal colectomy. Am J Surg. 2015;81:198–206.

    Google Scholar 

  36. Ohigashi S, Sudo K, Kobayashi D, Takahashi T, Nomoto K, Onodera H. Significant changes in the intestinal environment after surgery in patients with colorectal cancer. J Gastrointest Surg. 2013;17:1657–64.

    PubMed  Google Scholar 

  37. Mangell P, Thorlacius H, Syk I, Ahrne S, Molin G, Olsson C, et al. Lactobacillus plantarum 299v does not reduce enteric bacteria or bacterial translocation in patients undergoing colon resection. Dig Dis Sci. 2012;57:1915–24.

    PubMed  Google Scholar 

  38. Guimaraes Quintanilha AG, Azevedo dos Santos MA, Avila-Campos MJ, Saad WA, Pinotti HW, Zilberstein B. Chagasic megacolon and proximal jejunum microbiota. Scandanivian J Gastroenterol. 2000;35:632–6.

    CAS  Google Scholar 

  39. Mariat D, Firmesse O, Levenez F, Guimaraes VD, Sokol H, Dore J, et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009;9:123.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Kabeerdoss J, Sankaran V, Pugazhendhi S, Ramakrishna BS. Clostridium leptum group bacteria abundance and diversity in the fecal microbiota of patients with inflammatory bowel disease: a case-control study in India. BMC Gastroenterol. 2013;13:20

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Toprak NU, Gulluoglu BM, Cakici O, Akin LM, Demirkalem P, Celenk T, et al. Do antimicrobial susceptibility patterns of colonic isolates of Bacteroides species change after antibiotic prophylaxis with cefoxitine during elective abdominal surgery? World J Surg. 2005;29:1311–5.

    PubMed  Google Scholar 

  42. Okazaki M, Matsukuma S, Suto R, Miyazaki K, Hidaka M, Matsuo M, et al. Perioperative synbiotic therapy in elderly patients undergoing gastroenterological surgery: a prospective, randomized control trial. Nutrition. 2013;29:1224–30.

    PubMed  Google Scholar 

  43. Vaughn BP, Moss AC. Prevention of post-operative recurrence of Crohn’s disease. World J Gastroenterol. 2014;20:1147–54.

    PubMed  PubMed Central  Google Scholar 

  44. Vuik FER, Dicksved J, Lam SY, Fuhler GM, van der Laan LJW, van de Winkel A, et al. Composition of the mucosa-associated microbiota along the entire gastrointestinal tract of human individuals. United Eur Gastroenterol J. 2019;7:897–907.

    CAS  Google Scholar 

  45. Conlon MA, Bird AR. The impact of diet and lifestyle on gut microbiota and human health. Nutrients. 2014;7:17–44.

    PubMed  PubMed Central  Google Scholar 

  46. Vandeputte D, Tito RY, Vanleeuwen R, Falony G, Raes J. Practical considerations for large-scale gut microbiome studies. FEMS Microbiol Rev. 2017;41(Supp 1):S154–67.

    PubMed  PubMed Central  Google Scholar 

  47. Wu GD, Lewis JD, Hoffmann C, Chen YY, Knight R, Bittinger K, et al. Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiol. 2010;10:206.

    PubMed  PubMed Central  Google Scholar 

  48. Bahl MI, Bergström A, Licht TR. Freezing fecal samples prior to DNA extraction affects the Firmicutes to Bacteroidetes ratio determined by downstream quantitative PCR analysis. FEMS Microbiol Lett. 2012;329:193–7.

    CAS  PubMed  Google Scholar 

  49. Cowan ST. SK. Manual for idenfication of medical bacteria 2nd ed. New York: Cambridge University Press; 1974.

    Google Scholar 

  50. Sutter VLCD, Finegold SM. Wadsworth anaerobic bacteriology manual. 3rd ed. St. Louis: Mosby; 1980.

  51. Holdeman LVCE, Moore WE. Anaerobic laboratory manual. 4th ed. Blacksburg: Virginia Polytechnics Institute and State University; 1977.

    Google Scholar 

  52. Kang S, Denman SE, Morrison M, Yu Z, McSweeney C. An efficient RNA extraction method for estimating gut microbial diversity by polymerase chain reaction. Current Microbiology. 2009;58:464–71.

    CAS  PubMed  Google Scholar 

  53. Zoetendal EG, Akkermans AD, De Vos WM. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol. 1998;64:3854–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Quednau M, Ahrne S, Petersson AC, Molin G. Identification of clinically important species of Enterococcus within 1 day with randomly amplified polymorphic DNA (RAPD). Curr Microbiol. 1998;36:332–6.

    CAS  PubMed  Google Scholar 

  55. Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev. 1998;11:589–603.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Wagner J, Short K, Catto-Smith AG, et al. Identification and characterisation of Pseudomonas 16S ribosomal DNA from ileal biopsies of children with Crohn’s disease. PLoS ONE. 2008;3:e3578.

    PubMed  PubMed Central  Google Scholar 

  57. Hudault S, Guignot J, Servin AL. Escherichia coli strains colonising the gastrointestinal tract protect germfree mice against Salmonella typhimurium infection. Gut.2001;49:47–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Yoshida N, Emoto T, Yamashita T, Watanabe H, Hayashi T, Tabata T, et al. Bacteroides vulgatus and Bacteroides dorei reduce gut microbial lipopolysaccharide production and inhibit atherosclerosis. Circulation. 2018;138:2486–98.

    CAS  PubMed  Google Scholar 

  59. Hehemann JH, Kelly AG, Pudlo NA, Martens EC, Borastona AB. Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci USA. 2012;109:19786–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Slattery C, Cotter PD, O’Toole PW. Analysis of health benefits conferred by Lactobacillus species from kefir. Nutrients. 2019;11:1252–76.

    CAS  PubMed Central  Google Scholar 

  61. Cools P, Melin P. Group B Streptococcus and perinatal mortality. Res Microbiol. 2017;168:793–801.

    PubMed  Google Scholar 

  62. NB Corrêa, LA Filho Péret, Penna FJ, Lima FM, Nicoli JR. A randomized formula controlled trial of Bifidobacterium lactis and Streptococcus thermophilus for prevention of antibiotic-associated diarrhea in infants. J Clin Gastroenterol. 2005;39:385–9.

    Google Scholar 

  63. Eberhard J, Stumpp N, Winkel A, Schrimpf C, Bisdas T, Orzak P, et al. Streptococcus mitis and Gemella haemolysans were simultaneously found in atherosclerotic and oral plaques of elderly without periodontitis-a pilot study. Clin Oral Investig. 2017;21:447–52.

    CAS  PubMed  Google Scholar 

  64. Adam EL, Siciliano RF, Gualandro DM, Calderaro D, Issa VS, Rossi F, et al. Case series of infective endocarditis caused by Granulicatella species. Int J Infect Dis. 2015;31:56–58.

    PubMed  Google Scholar 

  65. Cuiv PO, Klaassens ES, Durkin AS, Harkins DM, Foster L, McCorrison J, et al. Draft genome sequence of Turicibacter sanguinis PC909, isolated from human feces. J Bacteriol. 2011;193:1288–9.

    CAS  PubMed  Google Scholar 

  66. Bibbò S, Riccardo Lopetuso L, Ianiro G, Di Rienzo T, Gasbarrini A, et al. Role of microbiota and innate immunity in recurrent Clostridium difficile infection. J Immunol Research. 2014;2014:462740.

    Google Scholar 

  67. Kanauchi O, Matsumoto Y, Matsumura M, Fukuoka M, Bamba T. The beneficial effects of microflora, especially obligate anaerobes, and their products on the colonic environment in inflammatory bowel disease. Curr Pharm Des. 2005;11:1047–53.

    CAS  PubMed  Google Scholar 

  68. de la Cuesta-Zuluaga J, Mueller NT, Corrales-Agudelo V, Velásquez-Mejía EP, Carmona JA, Abad JM, et al. Metformin is associated with higher relative abundance of mucin-degrading Akkermansia muciniphila and several short-chain fatty acid–producing microbiota in the gut. Diabetes Care. 2017;40:54–62.

    PubMed  Google Scholar 

  69. Workneh M, Wang F, Romagnoli M, Simner PJ, Carroll K. Bypass graft infection and bacteremia caused by Anaerostipes caccae: First report of human infection caused by a recently described gut anaerobe. Anaerobe. 2016;42:98–100.

    PubMed  Google Scholar 

  70. Schwiertz A, Hold GL, Duncan SH, Gruhl B, Collins MD, Lawson PA, et al. Anaerostipes caccae gen. nov., sp. nov., a new saccharolytic, acetate-utilising, butyrate-producing bacterium from human faeces. Syst Appl Microbiol. 2002;25:46–51.

    CAS  PubMed  Google Scholar 

  71. Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, et al. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst. 2013;105:1907–11.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Linares DM, Ross P, Stanton C. Beneficial microbes: the pharmacy in the gut. Bioengineered. 2015;7:11–20.

    PubMed Central  Google Scholar 

  73. Buchanan M. Sizing up bacteria. Nat Phys. 2014;10:788.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. University of Sydney, Sydney, NSW, Australia

    Suzie Ferrie, Amy Webster & Sharon Carey

  2. Royal Prince Alfred Hospital, Sydney, NSW, Australia

    Suzie Ferrie, Charis Tan & Sharon Carey

  3. St George Hospital, Sydney, NSW, Australia

    Betty Wu

Authors
  1. Suzie Ferrie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amy Webster
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Betty Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charis Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sharon Carey
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SC was responsible for conceptualisation of the study. AW, SF and SC were responsible for designing study. SC, SF and AW conducted the search, quality assessments and analysis of results. BW, SF and CT were responsible for reviewing the analysis. SF led the interpretation of results with all authors having involvement. AW and SF drafted the paper and all authors contributed to reviewing the paper.

Corresponding author

Correspondence to Sharon Carey.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ferrie, S., Webster, A., Wu, B. et al. Gastrointestinal surgery and the gut microbiome: a systematic literature review. Eur J Clin Nutr 75, 12–25 (2021). https://doi.org/10.1038/s41430-020-0681-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41430-020-0681-9

Search

Advanced search

Quick links