Efficacy of an inulin-based treatment on intestinal colonization by multidrug-resistant E. coli: insight into the mechanism of action

References

• Campos-Madueno EI, Moradi M, Eddoubaji Y, Shahi F, Moradi S, Bernasconi OJ, Moser AI, Endimiani A. Intestinal colonization with multidrug-resistant Enterobacterales: screening, epidemiology, clinical impact, and strategies to decolonize carriers. Eur J Clin Microbiol Infect Dis. 2023;42(3):229–16. doi:10.1007/s10096-023-04548-2.
   PubMed Web of Science ®Google Scholar
• Sorbara MT, Dubin K, Littmann ER, Moody TU, Fontana E, Seok R, Leiner IM, Taur Y, Peled JU, van den Brink MRM. et al. Inhibiting antibiotic-resistant enterobacteriaceae by microbiota-mediated intracellular acidification. J Exp Med. 2019;216(1):84–98. doi:10.1084/jem.20181639.
   PubMed Web of Science ®Google Scholar
• Oliveira RA, Ng KM, Correia MB, Cabral V, Shi H, Sonnenburg JL, Huang KC, Xavier KB. Klebsiella michiganensis transmission enhances resistance to enterobacteriaceae gut invasion by nutrition competition. Nat Microbiol. 2020;5(4):630–641. doi:10.1038/s41564-019-0658-4.
   PubMed Web of Science ®Google Scholar
• Osbelt L, Wende M, Almási É, Derksen E, Muthukumarasamy U, Lesker TR, Galvez EJC, Pils MC, Schalk E, Chhatwal P. et al. Klebsiella oxytoca causes colonization resistance against multidrug-resistant K. pneumoniae in the gut via cooperative carbohydrate competition. Cell Host Microbe. 2021;29(11):1663–1679.e7. doi:10.1016/j.chom.2021.09.003.
   PubMed Web of Science ®Google Scholar
• Kim H-R, Eom Y-B. Synergistic activity of Equol and meropenem against Carbapenem-Resistant Escherichia coli. Antibiotics (Basel). 2021;10(2):161. doi:10.3390/antibiotics10020161.
   PubMed Web of Science ®Google Scholar
• Gjonbalaj M, Keith JW, Do MH, Hohl TM, Pamer EG, Becattini S. Antibiotic degradation by commensal microbes shields pathogens. Infect Immun. 2020;88(4):e00012–20. doi:10.1128/IAI.00012-20.
   PubMed Web of Science ®Google Scholar
• Léonard F, Andremont A, Leclerq B, Labia R, Tancrède C. Use of -lactamase-producing anaerobes to prevent ceftriaxone from degrading intestinal resistance to colonization. J Infect Dis. 1989;160(2):274–280. doi:10.1093/infdis/160.2.274.
   PubMed Web of Science ®Google Scholar
• Stiefel U, Nerandzic MM, Pultz MJ, Donskey CJ. Gastrointestinal colonization with a cephalosporinase-producing bacteroides species preserves colonization resistance against vancomycin-resistant enterococcus and clostridium difficile in cephalosporin-treated mice. Antimicrob Agents Chemother. 2014;58(8):4535–4542. doi:10.1128/AAC.02782-14.
   PubMed Web of Science ®Google Scholar
• Cubillos-Ruiz A, Alcantar MA, Donghia NM, Cárdenas P, Avila-Pacheco J, Collins JJ. An engineered live biotherapeutic for the prevention of antibiotic-induced dysbiosis. Nat Biomed Eng. 2022;6(7):910–921. doi:10.1038/s41551-022-00871-9.
   PubMed Web of Science ®Google Scholar
• Mensink MA, Frijlink HW, van der Voort Maarschalk K, Hinrichs WLJ. Inulin, a flexible oligosaccharide I: review of its physicochemical characteristics. Carbohydr Polym. 2015;130:405–419. doi:10.1016/j.carbpol.2015.05.026.
   PubMed Web of Science ®Google Scholar
• Baxter NT, Schmidt AW, Venkataraman A, Kim KS, Waldron C, Schmidt TM. Dynamics of human gut microbiota and short-chain fatty acids in response to dietary interventions with three fermentable fibers. mBio. 2019;10(1):e02566–18. doi:10.1128/mBio.02566-18.
   PubMed Web of Science ®Google Scholar
• Chijiiwa R, Hosokawa M, Kogawa M, Nishikawa Y, Ide K, Sakanashi C, Takahashi K, Takeyama H. Single-cell genomics of uncultured bacteria reveals dietary fiber responders in the mouse gut microbiota. Microbiome. 2020;8(1). doi:10.1186/s40168-019-0779-2.
   PubMed Web of Science ®Google Scholar
• Le Bastard Q, Chapelet G, Javaudin F, Lepelletier D, Batard E, Montassier E. The effects of inulin on gut microbial composition: a systematic review of evidence from human studies. Eur J Clin Microbiol Infect Dis. 2020;39(3):403–413. doi:10.1007/s10096-019-03721-w.
   PubMed Web of Science ®Google Scholar
• Gregoire M, Berteau F, Bellouard R, Lebastard Q, Aubert P, Gonzales J, Javaudin F, Bessard A, Bemer P, Batard É. et al. A murine model to study the gut bacteria parameters during complex antibiotics like cefotaxime and ceftriaxone treatment. Comput Struct Biotechnol J. 2021;19:1423–1430. doi:10.1016/j.csbj.2021.02.019.
   PubMed Web of Science ®Google Scholar
• Zhu L, Qin S, Zhai S, Gao Y, Li L. Inulin with different degrees of polymerization modulates composition of intestinal microbiota in mice. FEMS Microbiol Lett. 2017;364(10). doi:10.1093/femsle/fnx075.
   Web of Science ®Google Scholar
• Rodriguez J, Hiel S, Neyrinck AM, Le Roy T, Pötgens SA, Leyrolle Q, Pachikian BD, Gianfrancesco MA, Cani PD, Paquot N. et al. Discovery of the gut microbial signature driving the efficacy of prebiotic intervention in obese patients. Gut. 2020;69(11):1975–1987. doi:10.1136/gutjnl-2019-319726.
   PubMed Web of Science ®Google Scholar
• Caballero S, Kim S, Carter RA, Leiner IM, Sušac B, Miller L, Kim GJ, Ling L, Pamer EG. Cooperating commensals restore colonization resistance to vancomycin-resistant Enterococcus faecium. Cell Host Microbe. 2017;21(5):592–602.e4. doi:10.1016/j.chom.2017.04.002.
   PubMed Web of Science ®Google Scholar
• Juhász J, Ligeti B, Gajdács M, Makra N, Ostorházi E, Farkas FB, Stercz B, Tóth Á, Domokos J, Pongor S. et al. Colonization Dynamics of Multidrug-Resistant Klebsiella pneumoniae Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic Analysis. Antibiotics (Basel). 2021;10(3):268. doi:10.3390/antibiotics10030268.
   PubMed Web of Science ®Google Scholar
• Wang L, Wang Z, Lan Y, Tuo Y, Ma S, Liu X. Inulin attenuates blood–brain barrier permeability and alleviates behavioral disorders by modulating the TLR4/MyD88/NF-κB pathway in mice with chronic stress. J Agric Food Chem. 2023;71(36):13325–13337. doi:10.1021/acs.jafc.3c03568.
   PubMedGoogle Scholar
• Hoving LR, Katiraei S, Pronk A, Heijink M, Vonk KKD, Amghar-el Bouazzaoui F, Vermeulen R, Drinkwaard L, Giera M, van Harmelen V. et al. The prebiotic inulin modulates gut microbiota but does not ameliorate atherosclerosis in hypercholesterolemic APOE*3-Leiden.CETP mice. Sci Rep. 2018;8(1):16515. doi:10.1038/s41598-018-34970-y.
   PubMedGoogle Scholar
• Le Guern R, Grandjean T, Stabler S, Bauduin M, Gosset P, Kipnis É, Dessein R. Gut colonisation with multidrug-resistant Klebsiella pneumoniae worsens Pseudomonas aeruginosa lung infection. Nat Commun. 2023;14(1):78. doi:10.1038/s41467-022-35767-4.
   PubMed Web of Science ®Google Scholar
• Stiefel U, Rao A, Pultz MJ, Jump RLP, Aron DC, Donskey CJ. Suppression of gastric acid production by proton pump inhibitor treatment facilitates colonization of the large intestine by vancomycin-resistant Enterococcus spp. And Klebsiella pneumoniae in clindamycin-treated mice. Antimicrob Agents Chemother. 2006;50(11):3905–3907. doi:10.1128/AAC.00522-06.
   PubMed Web of Science ®Google Scholar
• Ishnaiwer M, Bezabih Y, Javaudin F, Sassi M, Bemer P, Batard E, Dion M. In vitro and in vivo activity of new strains of Bacillus subtilis against ESBL-producing Escherichia coli: an experimental study. J Appl Microbiol. 2022;132(3):2270–2279. doi:10.1111/jam.15329.
   PubMed Web of Science ®Google Scholar
• Danylec N, Stoll DA, Göbl A, Huch M, Rasko D. Draft genome sequences of 13 isolates of adlercreutzia equolifaciens, Eggerthella lenta, and gordonibacter urolithinfaciens, isolated from human fecal samples in Karlsruhe, Germany. Microbiol Resour Announc. 2020;9(8):e00017–20. doi:10.1128/MRA.00017-20.
   PubMed Web of Science ®Google Scholar
• Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28(23):3150–3152. doi:10.1093/bioinformatics/bts565.
   PubMed Web of Science ®Google Scholar
• Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinf. 2012;13(1):134. doi:10.1186/1471-2105-13-134.
   PubMed Web of Science ®Google Scholar
• Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–2120. doi:10.1093/bioinformatics/btu170.
   PubMed Web of Science ®Google Scholar
• Lu J, Breitwieser FP, Thielen P, Salzberg SL. Bracken: estimating species abundance in metagenomics data. PeerJ Comput Sci. 2017;3:e104. doi:10.7717/peerj-cs.104.
   Google Scholar
• Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20(1):257. doi:10.1186/s13059-019-1891-0.
   PubMed Web of Science ®Google Scholar
• Beresford-Jones BS, Forster SC, Stares MD, Notley G, Viciani E, Browne HP, Boehmler DJ, Soderholm AT, Kumar N, Vervier K. et al. The mouse gastrointestinal bacteria catalogue enables translation between the mouse and human gut microbiotas via functional mapping. Cell Host Microbe. 2022;30(1):124–138.e8. doi:10.1016/j.chom.2021.12.003.
   PubMed Web of Science ®Google Scholar
• Yin X, Jiang X-T, Chai B, Li L, Yang Y, Cole JR, Tiedje JM, Zhang T. Args-OAP v2.0 with an expanded SARG database and hidden Markov models for enhancement characterization and quantification of antibiotic resistance genes in environmental metagenomes. Bioinformatics. 2018;34(13):2263–2270. doi:10.1093/bioinformatics/bty053.
   PubMed Web of Science ®Google Scholar
• Beghini F, McIver LJ, Blanco-Míguez A, Dubois L, Asnicar F, Maharjan S, Mailyan A, Manghi P, Scholz M, Thomas AM. et al. Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3. Elife. 2021;10:e65088. doi:10.7554/eLife.65088.
   PubMed Web of Science ®Google Scholar
• Caspi R, Billington R, Keseler IM, Kothari A, Krummenacker M, Midford PE, Ong WK, Paley S, Subhraveti P, Karp PD. et al. The MetaCyc database of metabolic pathways and enzymes - a 2019 update. Nucleic Acids Res. 2020;48(D1):D445–D453. doi:10.1093/nar/gkz862.
   PubMed Web of Science ®Google Scholar
• Drula E, Garron M-L, Dogan S, Lombard V, Henrissat B, Terrapon N. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res. 2022;50(D1):D571–D577. doi:10.1093/nar/gkab1045.
   PubMed Web of Science ®Google Scholar
• Moaligou C, Dion M, Ishnaiwer M, Dailly É, Batard É, Javaudin F. Pantoprazole promotes sustained intestinal carriage of multidrug-resistant Escherichia coli in amoxicillin-treated mice. J Appl Microbiol lxad. 2023;223(10). doi:10.1093/jambio/lxad223.
   Google Scholar
• Ni W, Cai X, Liang B, Cai Y, Cui J, Wang R. Effect of proton pump inhibitors on in vitro activity of tigecycline against several common clinical pathogens. PLOS ONE. 2014;9(1):e86715. doi:10.1371/journal.pone.0086715.
   PubMed Web of Science ®Google Scholar
• van den Bunt G, van Pelt W, Hidalgo L, Scharringa J, de Greeff SC, Schürch AC, Mughini-Gras L, Bonten MJM, Fluit AC. Prevalence, risk factors and genetic characterisation of extended-spectrum beta-lactamase and carbapenemase-producing enterobacteriaceae (ESBL-E and CPE): a community-based cross-sectional study, the Netherlands, 2014 to 2016. Euro Surveill. 2019;24(41):1800594. doi:10.2807/1560-7917.ES.2019.24.41.1800594.
   PubMedGoogle Scholar
• Willems RPJ, van Dijk K, Ket JCF, Vandenbroucke-Grauls CMJE. Evaluation of the association between gastric acid suppression and risk of intestinal colonization with multidrug-resistant microorganisms: a systematic review and meta-analysis. JAMA Internal Medicine. 2020;180(4):561–571. doi:10.1001/jamainternmed.2020.0009.
   PubMed Web of Science ®Google Scholar
• Raffelsberger N, Buczek DJ, Svendsen K, Småbrekke L, Pöntinen AK, Löhr IH, Andreassen LLE, Simonsen GS, Sundsfjord A, Gravningen K. et al. Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolates. mSphere. 2023;8(4):e0002523. doi:10.1128/msphere.00025-23.
   PubMed Web of Science ®Google Scholar
• Le Bastard Q, Berthelot L, Soulillou J-P, Montassier E. Impact of non-antibiotic drugs on the human intestinal microbiome. Expert Rev Mol Diagn. 2021;21(9):911–924. doi:10.1080/14737159.2021.1952075.
   PubMed Web of Science ®Google Scholar
• O’Donoghue C, Solomon K, Fenelon L, Fitzpatrick F, Kyne L. Effect of proton pump inhibitors and antibiotics on the gut microbiome of hospitalised older persons. J Infect. 2016;72(4):498–500. doi:10.1016/j.jinf.2016.01.015.
   PubMed Web of Science ®Google Scholar
• Liu W, Li X, Zhao Z, Pi X, Meng Y, Fei D, Liu D, Wang X. Effect of chitooligosaccharides on human gut microbiota and antiglycation. Carbohyd Polym. 2020;242:116413. doi:10.1016/j.carbpol.2020.116413.
   PubMed Web of Science ®Google Scholar
• Chung YW, Gwak H-J, Moon S, Rho M, Ryu J-H, Dong Q. Functional dynamics of bacterial species in the mouse gut microbiome revealed by metagenomic and metatranscriptomic analyses. PloS One. 2020;15(1):e0227886. doi:10.1371/journal.pone.0227886.
   PubMed Web of Science ®Google Scholar
• Smith BJ, Miller RA, Schmidt TM, Suen G. Muribaculaceae genomes assembled from metagenomes suggest genetic drivers of differential response to acarbose treatment in mice. mSphere. 2021;6(6):e0085121. doi:10.1128/msphere.00851-21.
   PubMed Web of Science ®Google Scholar
• Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, De Angelis M. The controversial role of human gut lachnospiraceae. Microorganisms. 2020;8(4):E573. doi:10.3390/microorganisms8040573.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ormerod KL, Wood DLA, Lachner N, Gellatly SL, Daly JN, Parsons JD, Dal’molin CGO, Palfreyman RW, Nielsen LK, Cooper MA. et al. Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals. Microbiome. 2016;4(1). doi:10.1186/s40168-016-0181-2.
   PubMedGoogle Scholar
• Wu G, Zhang C, Wang J, Zhang F, Wang R, Shen J, Wang L, Pang X, Zhang X, Zhao L. et al. Diminution of the gut resistome after a gut microbiota-targeted dietary intervention in obese children. Sci Rep. 2016;6(1):24030. doi:10.1038/srep24030.
   PubMedGoogle Scholar
• Montassier E, Valdés-Mas R, Batard E, Zmora N, Dori-Bachash M, Suez J, Elinav E. Probiotics impact the antibiotic resistance gene reservoir along the human GI tract in a person-specific and antibiotic-dependent manner. Nat Microbiol. 2021;6(8):1043–1054. doi:10.1038/s41564-021-00920-0.
   PubMed Web of Science ®Google Scholar
• Mayo B, Vázquez L, Flórez AB. Equol: a bacterial metabolite from the Daidzein Isoflavone and its presumed beneficial health effects. Nutrients. 2019;11(9):E2231. doi:10.3390/nu11092231.
   PubMed Web of Science ®Google Scholar
• Yu Z-T, Yao W, Zhu W-Y. Isolation and identification of equol-producing bacterial strains from cultures of pig faeces. FEMS Microbiol Lett. 2008;282(1):73–80. doi:10.1111/j.1574-6968.2008.01108.x.
   PubMed Web of Science ®Google Scholar
• Liang W, Zhao L, Zhang J, Fang X, Zhong Q, Liao Z, Wang J, Guo Y, Liang H, Wang L. et al. Colonization potential to reconstitute a microbe community in pseudo germ-free mice after fecal microbe transplant from equol Producer. Front Microbiol. 2020;11:1221. doi:10.3389/fmicb.2020.01221.
   PubMed Web of Science ®Google Scholar