Advanced search
Publication Cover
Gut Microbes Volume 15, 2023 - Issue 2
Submit an article Journal homepage
1,198
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Diet-induced shifts in the gut microbiota influence anastomotic healing in a murine model of colonic surgery

Sonja Boatmana Department of Surgery, University of Minnesota, Minneapolis, MN, USAORCID Iconhttps://orcid.org/0000-0002-1071-8249View further author information
ORCID Icon,
Thomas Kaisera Department of Surgery, University of Minnesota, Minneapolis, MN, USA;b BioTechnology Institute, University of Minnesota, St. Paul, MN, USAView further author information
,
Harika Nalluri-Butza Department of Surgery, University of Minnesota, Minneapolis, MN, USAORCID Iconhttps://orcid.org/0000-0001-5652-5058View further author information
ORCID Icon,
Mohammad Haneef Khana Department of Surgery, University of Minnesota, Minneapolis, MN, USA;b BioTechnology Institute, University of Minnesota, St. Paul, MN, USAORCID Iconhttps://orcid.org/0000-0001-9603-7593View further author information
ORCID Icon,
Matthew Dietza Department of Surgery, University of Minnesota, Minneapolis, MN, USA;b BioTechnology Institute, University of Minnesota, St. Paul, MN, USAView further author information
,
Julia Kohna Department of Surgery, University of Minnesota, Minneapolis, MN, USAORCID Iconhttps://orcid.org/0000-0002-2266-5113View further author information
ORCID Icon,
Abigail J Johnsonc School of Public Health, University of Minnesota, Minneapolis, MN, USAORCID Iconhttps://orcid.org/0000-0002-5998-4724View further author information
ORCID Icon,
Wolfgang B Gaertnera Department of Surgery, University of Minnesota, Minneapolis, MN, USA;d Division of Colon and Rectal Surgery, University of Minnesota, Minneapolis, MN, USAView further author information
,
Christopher Staleya Department of Surgery, University of Minnesota, Minneapolis, MN, USA;b BioTechnology Institute, University of Minnesota, St. Paul, MN, USAORCID Iconhttps://orcid.org/0000-0002-2309-0083View further author information
ORCID Icon &
Cyrus Jahansouza Department of Surgery, University of Minnesota, Minneapolis, MN, USA;d Division of Colon and Rectal Surgery, University of Minnesota, Minneapolis, MN, USACorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-7884-2799View further author information
ORCID Icon show all
Article: 2283147 | Received 01 Jun 2023, Accepted 09 Nov 2023, Published online: 22 Nov 2023

References

  • Morris AM, Regenbogen SE, Hardiman KM, Hendren S. Sigmoid diverticulitis: A systematic review. JAMA. 2014;311(3):287–18. doi:10.1001/jama.2013.282025.
  • Anaya DA, Flum DR. Risk of emergency colectomy and colostomy in patients with diverticular disease. Arch Surg. 2005;140(7):681–685. doi:10.1001/archsurg.140.7.681.
  • Society of Gastrointestinal and Endoscopic Surgeons. Colon resection surgery patient information from sages. 2015 [accessed 2023 May 23]. https://www.sages.org/publications/patient-information/patient-information-for-laparoscopic-colon-resection-from-sages/.
  • Krarup PM, Nordholm-Carstensen A, Jorgensen LN, Harling H. Association of comorbidity with anastomotic leak, 30-day mortality, and length of stay in elective surgery for colonic cancer: a nationwide cohort study. Dis Colon Rectum. 2015;58(7):668–676. doi:10.1097/DCR.0000000000000392.
  • Lee SW, Gregory D, Cool CL. Clinical and economic burden of colorectal and bariatric anastomotic leaks. Surg Endosc. 2020;34(10):4374–4381. doi:10.1007/s00464-019-07210-1.
  • Turrentine FE, Denlinger CE, Simpson VB, Garwood RA, Guerlain S, Agrawal A, Friel CM, LaPar DJ, Stukenborg GJ, Jones RS. Morbidity, mortality, cost, and survival estimates of gastrointestinal anastomotic leaks. J Am Coll Surg. 2015;220(2):195–206. doi:10.1016/j.jamcollsurg.2014.11.002.
  • Midura EF, Hanseman D, Davis BR, Atkinson SJ, Abbott DE, Shah SA, Paquette IM. Risk factors and consequences of anastomotic leak after colectomy: a national analysis. Dis Colon Rectum. 2015;58(3):333–338. doi:10.1097/DCR.0000000000000249.
  • Nikolian VC, Kamdar NS, Regenbogen SE, Morris AM, Byrn JC, Suwanabol PA, Campbell DA Jr., Hendren S. Anastomotic leak after colorectal resection: a population-based study of risk factors and hospital variation. Surgery. 2017;161(6):1619–1627. doi:10.1016/j.surg.2016.12.033. PMCID: PMC5433895.
  • Choi HK, Law WL, Ho JW. Leakage after resection and intraperitoneal anastomosis for colorectal malignancy: analysis of risk factors. Dis Colon Rectum. 2006;49(11):1719–1725. doi:10.1007/s10350-006-0703-2.
  • Hyman N, Manchester TL, Osler T, Burns B, Cataldo PA. Anastomotic leaks after intestinal anastomosis: It’s later than you think. Ann Surg. 2007;245(2):254–258. doi:10.1097/01.sla.0000225083.27182.85. PMCID: PMC1876987.
  • Zarnescu EC, Zarnescu NO, Costea R. Updates of risk factors for anastomotic leakage after colorectal surgery. Diagnostics. 2021;11(12):1–15. doi:10.3390/diagnostics11122382.
  • Bakker IS, Grossmann I, Henneman D, Havenga K, Wiggers T. Risk factors for anastomotic leakage and leak-related mortality after colonic cancer surgery in a nationwide audit. Br J Surg. 2014;101(4):424–432. doi:10.1002/bjs.9395.
  • Kryzauskas M, Bausys A, Degutyte AE, Abeciunas V, Poskus E, Bausys R, Dulskas A, Strupas K, Poskus T. Risk factors for anastomotic leakage and its impact on long-term survival in left-sided colorectal cancer surgery. World J Surg Oncol. 2020;18(1):1–9. doi:10.1186/s12957-020-01968-8.
  • Karliczek A, Harlaar NJ, Zeebregts CJ, Wiggers T, Baas PC, van Dam GM. Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis. 2009;24(5):569–576. doi:10.1007/s00384-009-0658-6.
  • Mulders RJ, de Git KCG, Schéle E, Dickson SL, Sanz Y, Adan RAH. Microbiota in obesity: interactions with enteroendocrine, immune and central nervous systems. Obes Rev. 2018;19(4):435–451. doi:10.1111/obr.12661.
  • Maslowski KM, Mackay CR. Diet, gut microbiota and immune responses. Nat Immunol. 2011;12(1):5–9. doi:10.1038/ni0111-5.
  • Gaines S, Shao C, Hyman N, Alverdy JC. Gut microbiome influences on anastomotic leak and recurrence rates following colorectal cancer surgery. Br J Surg. 2018;105(2):e131–e141. doi:10.1002/bjs.10760. PMCID: PMC5903685.
  • Gershuni VM, Friedman ES. The microbiome-host interaction as a potential driver of anastomotic leak. Curr Gastroenterol Rep. 2019;21(1):4. doi:10.1007/s11894-019-0668-7. PMCID: PMC9041531.
  • Palmisano S, Campisciano G, Iacuzzo C, Bonadio L, Zucca A, Cosola D, Comar M, de Manzini N. Role of preoperative gut microbiota on colorectal anastomotic leakage: preliminary results. Updates Surg. 2020;72(4):1013–1022. doi:10.1007/s13304-020-00720-x.
  • van Praagh JB, de Goffau MC, Bakker IS, van Goor H, Harmsen HJM, Olinga P, Havenga K. Mucus microbiome of anastomotic tissue during surgery has predictive value for colorectal anastomotic leakage. Ann Surg. 2019;269(5):911–916. doi:10.1097/SLA.0000000000002651.
  • Hyoju SK, Adriaansens C, Wienholts K, Sharma A, Keskey R, Arnold W, van Dalen D, Gottel N, Hyman N, Zaborin A, et al. Low-fat/high-fibre diet prehabilitation improves anastomotic healing via the microbiome: an experimental model. Br J Surg. 2020;107(6):743–755. doi:10.1002/bjs.11388. PMCID: PMC7875206.
  • Gaines S, van Praagh JB, Williamson AJ, Jacobson RA, Hyoju S, Zaborin A, Mao J, Koo HY, Alpert L, Bissonnette M, et al. Western diet promotes intestinal colonization by collagenolytic microbes and promotes tumor formation after colorectal surgery. Gastroenterology. 2020;158(4):958–970 e952. doi:10.1053/j.gastro.2019.10.020. PMCID: PMC7062578.
  • Shogan BD, Belogortseva N, Luong PM, Zaborin A, Lax S, Bethel C, Ward M, Muldoon JP, Singer M, An G, et al. Collagen degradation and mmp9 activation by enterococcus faecalis contribute to intestinal anastomotic leak. Sci Transl Med. 2015;7(286):286ra268. doi:10.1126/scitranslmed.3010658. PMCID: PMC5027898.
  • Kopp W. How Western diet and lifestyle drive the pandemic of obesity and civilization diseases. Diabetes Metab Syndr Obes. 2019;12:2221–2236. doi:10.2147/DMSO.S216791. PMCID: PMC6817492.
  • Shi Z. Gut microbiota: an important link between western diet and chronic diseases. Nutrients. 2019;11(10):2287. doi:10.3390/nu11102287. PMCID: PMC6835660.
  • Mearin F, Barbara G, Gwee KA, Stollmann N. Non-cardiac chest pain: a review of environmental exposure-associated comorbidities and biomarkers. Eur Med J Gastroenterol. 2018;7:103–112.
  • Rawla P, Sunkara T, Barsouk A. Epidemiology of colorectal cancer: Incidence, mortality, survival, and risk factors. Prz Gastroenterol. 2019;14(2):89–103. doi:10.5114/pg.2018.81072. PMCID: PMC6791134.
  • Wastyk HC, Fragiadakis GK, Perelman D, Dahan D, Merrill BD, Yu FB, Topf M, Gonzalez CG, Van Treuren W, Han S, et al. Gut-microbiota-targeted diets modulate human immune status. Cell. 2021;184(16):4137–4153 e4114. doi:10.1016/j.cell.2021.06.019. PMCID: PMC9020749.
  • Kelly CR, Khoruts A, Staley C, Sadowsky MJ, Abd M, Alani M, Bakow B, Curran P, McKenney J, Tisch A, et al. Effect of fecal microbiota transplantation on recurrence in multiply recurrent clostridium difficile infection: A randomized trial. Ann Intern Med. 2016;165(9):609–616. doi:10.7326/M16-0271. PMCID: PMC5909820.
  • Staley C, Halaweish H, Graiziger C, Hamilton MJ, Kabage AJ, Galdys AL, Vaughn BP, Vantanasiri K, Suryanarayanan R, Sadowsky MJ, et al. Lower endoscopic delivery of freeze-dried intestinal microbiota results in more rapid and efficient engraftment than oral administration. Sci Rep. 2021;11(1):1–9. doi:10.1038/s41598-021-84152-6.
  • Staley C, Kaiser T, Vaughn BP, Graiziger CT, Hamilton MJ, Kabage AJ, Khoruts A, Sadowsky MJ. Encapsulated fecal microbiota transplantation to treat clostridium difficile infection. mBio. 2019;10(4):e01586–01519. doi:10.1128/mBio.01586-19.
  • Reisinger KW, Schellekens DH, Bosmans JW, Boonen B, Hulsewe KW, Sastrowijoto P, Derikx JP, Grootjans J, Poeze M. Cyclooxygenase-2 is essential for colorectal anastomotic healing. Ann Surg. 2017;265(3):547–554. doi:10.1097/SLA.0000000000001744.
  • Bosmans JW, Jongen AC, Birchenough GM, Nystrom EE, Gijbels MJ, Derikx JP, Bouvy ND, Hansson GC. Functional mucous layer and healing of proximal colonic anastomoses in an experimental model. Br J Surg. 2017;104(5):619–630. doi:10.1002/bjs.10456.
  • Guo Z, Guo D, Gong J, Zhu W, Zuo L, Sun J, Li N, Li J. Preoperative nutritional therapy reduces the risk of anastomotic leakage in patients with crohn’s disease requiring resections. Gastroenterol Res Pract. 2016;2016:5017856. doi:10.1155/2016/5017856. PMCID: PMC4706910.
  • Foppa C, Ng SC, Montorsi M, Spinelli A. Anastomotic leak in colorectal cancer patients: new insights and perspectives. Eur J Surg Oncol. 2020;46(6):943–954. doi:10.1016/j.ejso.2020.02.027.
  • Hyoju SK, Klabbers RE, Aaron M, Krezalek MA, Zaborin A, Wiegerinck M, Hyman NH, Zaborina O, Van Goor H, Alverdy JC. Oral polyphosphate suppresses bacterial collagenase production and prevents anastomotic leak due to serratia marcescens and pseudomonas aeruginosa. Ann Surg. 2018;267(6):1112–1118. doi:10.1097/SLA.0000000000002167. PMCID: PMC5540820.
  • Gustafsson UO, Scott MJ, Hubner M, Nygren J, Demartines N, Francis N, Rockall TA, Young-Fadok TM, Hill AG, Soop M, et al. Guidelines for perioperative care in elective colorectal surgery: enhanced recovery after surgery (eras((r))) society recommendations: 2018. World J Surg. 2019;43(3):659–695. doi:10.1007/s00268-018-4844-y.
  • Staley C, Khoruts A, Sadowsky MJ. Contemporary applications of fecal microbiota transplantation to treat intestinal diseases in humans. Arch Med Res. 2017;48(8):766–773. doi:10.1016/j.arcmed.2017.11.006.
  • Napolitano M, Covasa M. Microbiota transplant in the treatment of obesity and diabetes: Current and future perspectives. Front Microbiol. 2020;11:590370. doi:10.3389/fmicb.2020.590370. PMCID: PMC7693552.
  • Halaweish HF, Boatman S, Staley C. Encapsulated fecal microbiota transplantation: Development, efficacy, and clinical application. Front Cell Infect Microbiol. 2022;12:826114. doi:10.3389/fcimb.2022.826114. PMCID: PMC8968856.
  • Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van Treuren W, Ren B, Schwager E, Knights D, Song SJ, Yassour M, et al. The treatment-naive microbiome in new-onset crohn’s disease. Cell Host & Microbe. 2014;15(3):382–392. doi:10.1016/j.chom.2014.02.005. PMCID: PMC4059512.
  • Schmitt FCF, Brenner T, Uhle F, Loesch S, Hackert T, Ulrich A, Hofer S, Dalpke AH, Weigand MA, Boutin S. Gut microbiome patterns correlate with higher postoperative complication rates after pancreatic surgery. BMC Microbiol. 2019;19(42):1–13. doi:10.1186/s12866-019-1399-5.
  • Liu Y, Geng R, Liu L, Jin X, Yan W, Zhao F, Wang S, Guo X, Ghimire G, Wei Y. Gut microbiota-based algorithms in the prediction of metachronous adenoma in colorectal cancer patients following surgery. Front Microbiol. 2020;11(June):1–11. doi:10.3389/fmicb.2020.01106.
  • Peled JU, Gomes ALC, Devlin SM, Littmann ER, Taur Y, Sung AD, Weber D, Hashimoto D, Slingerland AE, Slingerland JB, et al. Microbiota as predictor of mortality in allogeneic hematopoietic-cell transplantation. N Engl J Med. 2020;382(9):822–834. doi:10.1056/nejmoa1900623.
  • Ren Z, Li A, Jiang J, Zhou L, Yu Z, Lu H, Xie H, Chen X, Shao L, Zhang R, et al. Gut microbiome analysis as a tool towards targeted non-invasive biomarkers for early hepatocellular carcinoma. Gut. 2019;68(6):1014–1023. doi:10.1136/gutjnl-2017-315084.
  • Qin N, Yang F, Li A, Prifti E, Chen Y, Shao L, Guo J, Le Chatelier E, Yao J, Wu L, et al. Alterations of the human gut microbiome in liver cirrhosis. Nature. 2014;513(7516):59–64. doi:10.1038/nature13568.
  • Schmitt FCF, Schneider M, Mathejczyk W, Weigand MA, Figueiredo JC, Li CI, Shibata D, Siegel EM, Toriola AT, Ulrich CM, et al. Postoperative complications are associated with long-term changes in the gut microbiota following colorectal cancer surgery. Life (Basel). 2021;11(3):246. doi:10.3390/life11030246. PMCID: PMC8002283.
  • Hajjar R, Gonzalez E, Fragoso G, Oliero M, Alaoui AA, Calve A, Vennin Rendos H, Djediai S, Cuisiniere T, Laplante P, et al. Gut microbiota influence anastomotic healing in colorectal cancer surgery through modulation of mucosal proinflammatory cytokines. Gut. 2023;72(6):1143–1154. doi:10.1136/gutjnl-2022-328389.
  • Parker BJ, Wearsch PA, Veloo ACM, Rodriguez-Palacios A. The genus alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health. Front Immunol. 2020;11:906. doi:10.3389/fimmu.2020.00906. PMCID: PMC7296073.
  • Abdugheni R, Wang WZ, Wang YJ, Du MX, Liu FL, Zhou N, Jiang CY, Wang CY, Wu L, Ma J, et al. Metabolite profiling of human‐originated lachnospiraceae at the strain level. iMeta. 2022;1(4):e58. doi:10.1002/imt2.58.
  • Puertollano E, Kolida S, Yaqoob P. Biological significance of short-chain fatty acid metabolism by the intestinal microbiome. Current Opinion In Clinical Nutrition & Metabolic Care. 2014;17(2):139–144. doi:10.1097/MCO.0000000000000025.
  • Sanna S, van Zuydam NR, Mahajan A, Kurilshikov A, Vich Vila A, Vosa U, Mujagic Z, Masclee AAM, Jonkers D, Oosting M, et al. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat Genet. 2019;51(4):600–605. doi:10.1038/s41588-019-0350-x. PMCID: PMC6441384.
  • Zheng L, Kelly CJ, Battista KD, Schaefer R, Lanis JM, Alexeev EE, Wang RX, Onyiah JC, Kominsky DJ, Colgan SP. Microbial-derived butyrate promotes epithelial barrier function through il-10 receptor-dependent repression of claudin-2. J Immunol. 2017;199(8):2976–2984. doi:10.4049/jimmunol.1700105. PMCID: PMC5636678.
  • Bloemen JG, Schreinemacher MH, de Bruine AP, Buurman WA, Bouvy ND, Dejong CH. Butyrate enemas improve intestinal anastomotic strength in a rat model. Dis Colon Rectum. 2010;53(7):1069–1075. doi:10.1007/DCR.0b013e3181d881b7.
  • Bosmans JW, Jongen AC, Boonen BT, van Rijn S, Scognamiglio F, Stucchi L, Gijbels MJ, Marsich E, Bouvy ND. Comparison of three different application routes of butyrate to improve colonic anastomotic strength in rats. Int J Colorectal Dis. 2017;32(3):305–313. doi:10.1007/s00384-016-2718-z. PMCID: PMC5316396.
  • Nalluri-Butz H, Bobel MC, Nugent J, Boatman S, Emanuelson R, Melton-Meaux G, Madoff RD, Jahansouz C, Staley C, Gaertner WB. A pilot study demonstrating the impact of surgical bowel preparation on intestinal microbiota composition following colon and rectal surgery. Sci Rep. 2022;12(1):10559. doi:10.1038/s41598-022-14819-1. PMCID: PMC9217797.
  • Appert O, Garcia AR, Frei R, Roduit C, Constancias F, Neuzil-Bunesova V, Ferstl R, Zhang J, Akdis C, Lauener R, et al. Initial butyrate producers during infant gut microbiota development are endospore formers. Environ Microbiol. 2020;22(9):3909–3921. doi:10.1111/1462-2920.15167.
  • Ma L, Shen Q, Lyu W, Lv L, Wang W, Yu M, Yang H, Tao S, Xiao Y, Claesen J. Clostridium butyricum and its derived extracellular vesicles modulate gut homeostasis and ameliorate acute experimental colitis. Microbiol Spectr. 2022;10(4):e0136822. doi:10.1128/spectrum.01368-22. PMCID: PMC9431305.
  • Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, Kayser BD, Levenez F, Chilloux J, Hoyles L, et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut. 2016;65(3):426–436. doi:10.1136/gutjnl-2014-308778.
  • Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, et al. Cross-talk between akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110(22):9066–9071. doi:10.1073/pnas.1219451110. PMCID: PMC3670398.
  • Chelakkot C, Choi Y, Kim DK, Park HT, Ghim J, Kwon Y, Jeon J, Kim MS, Jee YK, Gho YS, et al. Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions. Experimental & Molecular Medicine. 2018;50(2):e450. doi:10.1038/emm.2017.282. PMCID: PMC5903829.
  • Alam A, Leoni G, Quiros M, Wu H, Desai C, Nishio H, Jones RM, Nusrat A, Neish AS. The microenvironment of injured murine gut elicits a local pro-restitutive microbiota. Nat microbiol. 2016;1(2):15021. doi:10.1038/nmicrobiol.2015.21. PMCID: PMC5076466.
  • Wexler HM. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev. 2007;20(4):593–621. doi:10.1128/CMR.00008-07. PMCID: PMC2176045.
  • So Gun Hong NS, Legrand F, Gadkari M, Makiya M, Stokes K, Howe KN, Yu SJ, Nathaniel Seth Linde RRC, Hunt T, Hu Z, et al. Franco4 aLM. Glucocorticoid-induced eosinopenia results from cxcr4-dependent bone marrow migration. Blood. 2020;136(23):2667–2678. doi:10.1182/blood.2020005161.
  • Hansen BC. Progressive nature of obesity and diabetes in nonhuman primates. Obesity (Silver Spring). 2017;25(4):663–664. doi:10.1002/oby.21818.
  • Vasiliu EC, Zarnescu NO, Costea R, Neagu S. Review of risk factors for anastomotic leakage in colorectal surgery. Chirurgia (Bucur). 2015;110:319–326.
  • Jahansouz C, Staley C, Bernlohr DA, Sadowsky MJ, Khoruts A, Ikramuddin S. Sleeve gastrectomy drives persistent shifts in the gut microbiome. Surg Obes Relat Dis. 2017;13(6):916–924. doi:10.1016/j.soard.2017.01.003.
  • Jahansouz C, Staley C, Kizy S, Xu H, Hertzel AV, Coryell J, Singroy S, Hamilton M, DuRand M, Bernlohr DA, et al. Antibiotic-induced disruption of intestinal microbiota contributes to failure of vertical sleeve gastrectomy. Ann Surg. 2019;269(6):1092–1100. doi:10.1097/SLA.0000000000002729.
  • Freitag TL, Hartikainen A, Jouhten H, Sahl C, Meri S, Anttila VJ, Mattila E, Arkkila P, Jalanka J, Satokari R. Minor effect of antibiotic pre-treatment on the engraftment of donor microbiota in fecal transplantation in mice. Front Microbiol. 2019;10:2685. doi:10.3389/fmicb.2019.02685. PMCID: PMC6881239.
  • Kaiser T, Nalluri H, Zhu Z, Staley C. Donor microbiota composition and housing affect recapitulation of obese phenotypes in a human microbiota-associated murine model. Front Cell Infect Microbiol. 2021;11:614218. doi:10.3389/fcimb.2021.614218. PMCID: PMC7937608.
  • Nagata N, Tohya M, Fukuda S, Suda W, Nishijima S, Takeuchi F, Ohsugi M, Tsujimoto T, Nakamura T, Shimomura A, et al. Effects of bowel preparation on the human gut microbiome and metabolome. Sci Rep. 2019;9(1):4042. doi:10.1038/s41598-019-40182-9. PMCID: PMC6411954.
  • Gates KV, Alamaw E, Jampachaisri K, Huss MK, Pacharinsak C. Efficacy of supplemental diet gels for preventing postoperative weight loss in mice (mus musculus). J Am Assoc Lab Anim Sci. 2023;62(1):87–91. doi:10.30802/AALAS-JAALAS22-000030. PMCID: PMC9936848.
  • Shogan BD, Smith DP, Christley S, Gilbert J, Zaborin A, Alverdy JC. Intestinal anastomotic injury alters spatially defined microbiome composition and function. Microbiome. 2014;2(1):1–10. doi:10.1186/2049-2618-2-35. PMCID: PMC4171717.
  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. Ultra-high-throughput microbial community analysis on the illumina hiseq and miseq platforms. ISME J. 2012;6(8):1621–1624. doi:10.1038/ismej.2012.8. PMCID: PMC3400413.
  • Gohl DM, Vangay P, Garbe J, MacLean A, Hauge A, Becker A, Gould TJ, Clayton JB, Johnson TJ, Hunter R, et al. Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies. Nat Biotechnol. 2016;34(9):942–949. doi:10.1038/nbt.3601.
  • Schloss PD. Reintroducing mothur: 10 years later. Appl Environ Microbiol. 2020;86(2):1–13. doi:10.1128/AEM.02343-19.
  • Aronesty E. Comparison of sequencing utility programs. Open Bioinforma J. 2013;7(1):1–8. doi:10.2174/1875036201307010001.
  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO. Silva: a comprehensive online resource for quality checked and aligned ribosomal rna sequence data compatible with arb. Nucleic Acids Res. 2007;35(21):7188–7196. doi:10.1093/nar/gkm864. PMCID: PMC2175337.
  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. Uchime improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27(16):2194–2200. doi:10.1093/bioinformatics/btr381. PMCID: PMC3150044.
  • Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, et al. The ribosomal database project: improved alignments and new tools for rrna analysis. Nucleic Acids Res. 2009;37(Database issue):D141–D145. doi:10.1093/nar/gkn879. PMCID: PMC2686447.
  • Knights D, Kuczynski J, Charlson ES, Zaneveld J, Mozer MC, Collman RG, Bushman FD, Knight R, Kelley ST. Bayesian community-wide culture-independent microbial source tracking. Nat Methods. 2011;8(9):761–763. doi:10.1038/nmeth.1650. PMCID: PMC3791591.
  • Bray J, Curtis J. An ordination of the upland forest communities of southern wisconsin. Ecol Monogr. 1957;27(4):325–349. doi:10.2307/1942268.
  • Anderson MJ, Willis TJ. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology. 2003;84(2):511–525. doi:10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2.
  • Clarke KR. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol. 1993;18(1):117–143. doi:10.1111/j.1442-9993.1993.tb00438.x.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.