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Research Paper

Gut microbiota from patients with COVID-19 cause alterations in mice that resemble post-COVID symptoms

Viviani Mendes de Almeidaa Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Daiane F. Engelb Department of Clinical Analysis, School of Pharmacy, Universidade Federal de Ouro Preto - UFOP, Ouro Preto, BrazilView further author information
,
Mayra F. Riccia Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Clênio Silva Cruza Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Ícaro Santos Lopesc Laboratory of Virus Bioinformatics - Department of Biological Science, Center of Biotechnology and Genetics, Universidade Estadual de Santa Cruz - UESC, Ilhéus, BrazilView further author information
,
Daniele Almeida Alvesd Laboratory of RNA Interference and Antiviral Immunity - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Mirna d’ Auriole Laboratory of Toxicology - Department of Clinical and Toxicological Analysis, Faculty of Pharmacy, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
João Magalhãesa Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Elayne C. Machadoa Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Victor M. Rochaa Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Toniana G. Carvalhof Laboratory of Neurobiochemistry - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Larisse S. B. Lacerdag Center for Research and Development of Drugs - Department of Morphology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Jordane C. Pimentag Center for Research and Development of Drugs - Department of Morphology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Mariana Aganettia Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Giuliana S. Zuccolih Laboratory of Neuroproteomics - Department of Biochemistry and Tissue Biology, Institute of Biology, Universidade do Estado de Campinas - UNICAMP, Campinas, BrazilView further author information
,
Bradley J. Smithh Laboratory of Neuroproteomics - Department of Biochemistry and Tissue Biology, Institute of Biology, Universidade do Estado de Campinas - UNICAMP, Campinas, BrazilView further author information
,
Victor C. Carregarih Laboratory of Neuroproteomics - Department of Biochemistry and Tissue Biology, Institute of Biology, Universidade do Estado de Campinas - UNICAMP, Campinas, BrazilView further author information
,
Erika da Silva Rosaa Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Izabela Galvãoa Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Geovanni Dantas Cassalii Laboratory of Comparative Pathology - Department of Pathology, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Cristiana C. Garciaj Laboratory of Respiratory Viruses and Measles, Instituto Oswaldo Cruz - Fiocruz, Rio de Janeiro, BrazilView further author information
,
Mauro Martins Teixeirag Center for Research and Development of Drugs - Department of Morphology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Leiliane C. Andrée Laboratory of Toxicology - Department of Clinical and Toxicological Analysis, Faculty of Pharmacy, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Fabiola Mara Ribeirof Laboratory of Neurobiochemistry - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Flaviano S. Martinsk Laboratory of Biotherapeutic Agents - Department of Microbiology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Rafael Simone Saial Laboratory of Intestinal Physiology - Department of Physiology, Ribeirão Preto Medical School, Universidade de São Paulo, Ribeirão Preto, BrazilView further author information
,
Vivian Vasconcelos Costag Center for Research and Development of Drugs - Department of Morphology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilView further author information
,
Daniel Martins-de-Souzah Laboratory of Neuroproteomics - Department of Biochemistry and Tissue Biology, Institute of Biology, Universidade do Estado de Campinas - UNICAMP, Campinas, Brazil;m D’Or Institute for Research and Education, São Paulo, Brazil;n Experimental Medicine Research Cluster, Universidade do Estado de Campinas - UNICAMP, Campinas, Brazil;o National Institute of Biomarkers in Neuropsychiatry, National Council for Scientific and Technological Development, São Paulo, BrazilView further author information
,
Philip M. Hansbrop Centre for Inflammation, Centenary Institute and University of Technology Sydney, Sydney, AustraliaView further author information
,
João Trindade Marquesd Laboratory of RNA Interference and Antiviral Immunity - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, Brazil;q CNRS UPR9022, University of Strasbourg, Strasbourg, FranceView further author information
,
Eric R. G. R. Aguiarc Laboratory of Virus Bioinformatics - Department of Biological Science, Center of Biotechnology and Genetics, Universidade Estadual de Santa Cruz - UESC, Ilhéus, BrazilView further author information
&
Angélica T. Vieiraa Laboratory of Microbiota and Immunomodulation - Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, BrazilCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-4556-7671View further author information
ORCID Icon show all
Article: 2249146 | Received 24 Apr 2023, Accepted 14 Aug 2023, Published online: 05 Sep 2023

References

  • World Health Organization. COVID-19 weekly epidemiological update, 16 March 2023. 134th ed. 2023. https://apps.who.int/iris/handle/10665/366534.
  • Augustin M, Schommers P, Stecher M, Dewald F, Gieselmann L, Gruell H, Horn C, Vanshylla K, Di Cristanziano V, Osebold L. Post-COVID syndrome in non-hospitalised patients with COVID-19: a longitudinal prospective cohort study. Lancet Reg Heal. 2021;6:100122. doi:10.1016/j.lanepe.2021.100122.
  • Lopez-Leon S, Wegman-Ostrosky T, Perelman C, Sepulveda R, Rebolledo PA, Cuapio A, Villapol S. More than 50 long-term effects of COVID-19: a systematic review and meta-analysis. Sci Rep. 2021;11(1):16144. doi:10.1038/s41598-021-95565-8.
  • Subramanian A, Nirantharakumar K, Hughes S, Myles P, Williams T, Gokhale KM, Taverner T, Chandan JS, Brown K, Simms-Williams N. Symptoms and risk factors for long COVID in non-hospitalized adults. Nat Med. 2022;28(8):1706–22. doi:10.1038/s41591-022-01909-w.
  • Hikmet F, Méar L, Edvinsson Å, Micke P, Uhlén M, Lindskog C. The protein expression profile of ACE2 in human tissues. Mol Syst Biol. 2020;16:e9610. doi:10.15252/msb.20209610.
  • Sencio V, Gallerand A, Gomes Machado M, Deruyter L, Heumel S, Soulard D, Barthelemy J, Cuinat C, Vieira AT, Barthelemy A, et al. Influenza virus infection impairs the gut’s barrier properties and favors secondary enteric bacterial infection through reduced production of short-chain fatty acids. Infect Immun. 2021;89(9):e0073420. doi:10.1128/IAI.00734-20.
  • Yeoh YK, Zuo T, Lui GY, Zhang F, Liu Q, Li AY, Chung AC, Cheung CP, Tso EY, Fung KS, et al. Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut [Internet]. 2021;70(4):698–706. doi:10.1136/gutjnl-2020-323020.
  • Zuo T, Liu Q, Zhang F, Lui GCY, Tso EYK, Yeoh YK, Chen Z, Boon SS, Chan FKL, Chan PKS, et al. Depicting SARS-CoV-2 faecal viral activity in association with gut microbiota composition in patients with COVID-19. Gut. 2021;70:276–284. doi:10.1136/gutjnl-2020-322294.
  • Chen Y, Gu S, Chen Y, Lu H, Shi D, Guo J, Wu WR, Yang Y, Li Y, Xu KJ, et al. Six-month follow-up of gut microbiota richness in patients with COVID-19. Gut. 2022;71(1):222–225. doi:10.1136/gutjnl-2021-324090.
  • Cullen BR. MicroRNAs as mediators of viral evasion of the immune system. Nat Immunol. 2013;14(3):205–210. doi:10.1038/ni.2537.
  • Wu Y, Cheng X, Jiang G, Tang H, Ming S, Tang L, Lu J, Guo C, Shan H, Huang X. Altered oral and gut microbiota and its association with SARS-CoV-2 viral load in COVID-19 patients during hospitalization. Npj Biofilms Microbio [Internet]. 2021;7(1):61. doi:10.1038/s41522-021-00232-5.
  • Liu Q, Mak JWY, Su Q, Yeoh YK, Lui GCY, Ng SSS, Zhang F, Li AYL, Lu W, Hui DSC, et al. Gut microbiota dynamics in a prospective cohort of patients with post-acute COVID-19 syndrome. Gut [Internet]. 2022;71(3):544–552. doi:10.1136/gutjnl-2021-325989.
  • Zollner A, Koch R, Jukic A, Pfister A, Meyer M, Rössler A, Kimpel J, Adolph TE, Tilg H. Postacute COVID-19 is characterized by gut viral antigen persistence in inflammatory bowel diseases. Gastroenterol [Internet]. 2022;163(2):495–506.e8. doi:10.1053/j.gastro.2022.04.037.
  • Bowerman KL, Rehman SF, Vaughan A, Lachner N, Budden KF, Kim RY, Wood DLA, Gellatly SL, Shukla SD, Wood LG, et al. Disease-associated gut microbiome and metabolome changes in patients with chronic obstructive pulmonary disease. Nat Commun [Internet]. 2020;11(1):5886. doi:10.1038/s41467-020-19701-0.
  • Fernández-de-Las-Peñas C, Palacios-Ceña D, Gómez-Mayordomo V, Cuadrado ML, Florencio LL. Defining post-COVID symptoms (post-acute COVID, long COVID, persistent post-COVID): an integrative classification. Int J Environ Res Public Health. 2021;18(5):18. doi:10.3390/ijerph18052621.
  • Caugant DA, Levin BR, Selander RK. Distribution of multilocus genotypes of escherichia coli within and between host families. J Hyg (Lond). 1984;92(3):377–384. doi:10.1017/S0022172400064597.
  • Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, et al. Cohabiting family members share microbiota with one another and with their dogs. Elife. 2013;2. doi:10.7554/eLife.00458.
  • Souza DG, Vieira AT, Soares AC, Pinho V, Nicoli JR, Vieira LQ, Teixeira MM. The essential role of the intestinal microbiota in facilitating acute inflammatory responses. J Immunol. 2004;173(6):4137–4146. doi:10.4049/jimmunol.173.6.4137.
  • M C CC, L NL, C M F, J L G, D A, C G, G C, S H P, C M, F S M, et al. Comparing the effects of acute alcohol consumption in germ-free and conventional mice: the role of the gut microbiota. BMC Microbiol. 2014;14(1):240. doi:10.1186/s12866-014-0240-4.
  • Rungue M, Melo V, Martins D, Campos PC, Leles G, Galvão I, Mendes V, Aganetti M, Pedersen Á, Assis NRG, et al. NLRP6-associated host microbiota composition impacts in the intestinal barrier to systemic dissemination of brucella abortus. PLoS Negl Trop Dis. 2021;15(2):e0009171. doi:10.1371/journal.pntd.0009171.
  • Zhang F, Wan Y, Zuo T, Yeoh YK, Liu Q, Zhang L, Zhan H, Lu W, Xu W, Lui GCY, et al. Prolonged impairment of short-chain fatty acid and L-Isoleucine biosynthesis in gut microbiome in patients with COVID-19. Gastroenterol. 2022;162(2):548–561.e4. doi:10.1053/j.gastro.2021.10.013.
  • Galvão I, Tavares LP, Corrêa RO, Fachi JL, Rocha VM, Rungue M, Garcia CC, Cassali G, Ferreira CM, Martins FS, et al. The metabolic sensor GPR43 receptor plays a role in the control of Klebsiella pneumoniae infection in the lung. Front Immunol. 2018;9. http://journal.frontiersin.org/article/10.3389/fimmu.2018.00142/full.
  • Vieira AT, Rocha VM, Tavares L, Garcia CC, Teixeira MM, Oliveira SC, Cassali GD, Gamba C, Martins FS, Nicoli JR. Control of klebsiella pneumoniae pulmonary infection and immunomodulation by oral treatment with the commensal probiotic bifidobacterium longum 51A. Microbes Infect. 2016;18(3):180–189. doi:10.1016/j.micinf.2015.10.008.
  • Wu T, Xu F, Su C, Li H, Lv N, Liu Y, Gao Y, Lan Y, Li J. Alterations in the gut microbiome and cecal metabolome during klebsiella pneumoniae-induced pneumosepsis. Front Immunol. 2020;11:1331. doi:10.3389/fimmu.2020.01331.
  • Douaud G, Lee S, Alfaro-Almagro F, Arthofer C, Wang C, McCarthy P, Lange F, Andersson JLR, Griffanti L, Duff E. SARS-CoV-2 is associated with changes in brain structure in UK biobank. Nature. 2022;604(7907):697–707. doi:10.1038/s41586-022-04569-5.
  • Hartung TJ, Neumann C, Bahmer T, Chaplinskaya-Sobol I, Endres M, Geritz J, Haeusler KG, Heuschmann PU, Hildesheim H, Hinz A. Fatigue and cognitive impairment after COVID-19: a prospective multicentre study. EClinicalMed. 2022;53:101651. doi:10.1016/j.eclinm.2022.101651.
  • Heine J, Schwichtenberg K, Hartung TJ, Rekers S, Chien C, Boesl F, Rust R, Hohenfeld C, Bungenberg J, Costa AS. Structural brain changes in patients with post-COVID fatigue: a prospective observational study. Eclinicalmed. 2023;58. doi:10.1016/j.eclinm.2023.101874.
  • Andrade SP, Campolina-Silva GH, Queiroz-Junior CM, de Oliveira LC, de Lacerda L, Gaggino JCP, de Souza FRO, de Meira Chaves I, Passos IB, Teixeira DC, et al. A biosafety level 2 mouse model for studying betacoronavirus-induced acute lung damage and systemic manifestations. J Virol. 2021;95(22). doi:10.1128/JVI.01276-21.
  • da Silva JGV, Vieira AT, Sousa TJ, Viana MVC, Parise D, Sampaio B, da Silva AL, de Jesus LCL, de Carvalho PKRML, de Castro Oliveira L, et al. Comparative genomics and in silico gene evaluation involved in the probiotic potential of Bifidobacterium longum 51A. Gene. 2021;795:145781. doi:10.1016/j.gene.2021.145781.
  • Xu E, Xie Y, Al-Aly Z. Long-term gastrointestinal outcomes of COVID-19. Nat Commun [Internet]. 2023;14(1):983. doi:10.1038/s41467-023-36223-7.
  • Livanos AE, Jha D, Cossarini F, Gonzalez-Reiche AS, Tokuyama M, Aydillo T, Parigi TL, Ladinsky MS, Ramos I, Dunleavy K, et al. Intestinal host response to SARS-CoV-2 infection and COVID-19 outcomes in patients with gastrointestinal symptoms. Gastroenterol [Internet]. 2021;160(7):2435–2450.e34. doi:10.1053/j.gastro.2021.02.056.
  • Merad M, Blish CA, Sallusto F, Iwasaki A. The immunology and immunopathology of COVID-19. Science (80-) [Internet]. 2022;375(6585):1122–1127. doi:10.1126/science.abm8108.
  • Wu Y, Cheng X, Jiang G, Tang H, Ming S, Tang L, Lu J, Guo C, Shan H, Huang X. Author correction: altered oral and gut microbiota and its association with SARS-CoV-2 viral load in COVID-19 patients during hospitalization. Npj Biofilms Microbio [Internet]. 2021;7(1):90. doi:10.1038/s41522-021-00262-z.
  • Langford BJ, So M, Simeonova M, Leung V, Lo J, Kan T, Raybardhan S, Sapin ME, Mponponsuo K, Farrell A. Antimicrobial resistance in patients with COVID-19: a systematic review and meta-analysis. Lancet Microbe. 2022. doi:10.2139/ssrn.4099404.
  • Langford BJ, Soucy JP, Leung V, So M, Kwan ATH, Portnoff JS, Bertagnolio S, Raybardhan S, MacFadden D, Daneman N. Antibiotic resistance associated with the COVID-19 pandemic: a systematic review and meta-analysis. Clin Microbiol Infect 2022;29(3):302–309. doi: 10.1016/j.cmi.2022.12.006.
  • de Nies L, Galata V, Martin-Gallausiaux C, Despotovic M, Busi SB, Snoeck CJ, Delacour L, Budagavi DP, Laczny CC, Habier J, et al. Altered infective competence of the human gut microbiome in COVID-19. Microbiome. 2023;11(1):46. doi:10.1186/s40168-023-01472-7.
  • Bernard-Raichon L, Venzon M, Klein J, Axelrad JE, Zhang C, Sullivan AP, Hussey GA, Casanovas-Massana A, Noval MG, Valero-Jimenez AM, et al. Gut microbiome dysbiosis in antibiotic-treated COVID-19 patients is associated with microbial translocation and bacteremia. Nat Commun [Internet]. 2022;13(1):5926. doi:10.1038/s41467-022-33395-6.
  • Kariyawasam RM, Julien DA, Jelinski DC, Larose SL, Rennert-May E, Conly JM, Dingle TC, Chen JZ, Tyrrell GJ, Ronksley PE, et al. Antimicrobial resistance (AMR) in COVID-19 patients: a systematic review and meta-analysis (November 2019–June 2021). Antimicrob Resist Infect Control [Internet]. 2022;11(1):45. doi:10.1186/s13756-022-01085-z.
  • López-Jácome LE, Fernández-Rodríguez D, Franco-Cendejas R, Camacho-Ortiz A, Morfin-Otero MDR, Rodríguez-Noriega E, Ponce-de-León A, Ortiz-Brizuela E, Rojas-Larios F, Velázquez-Acosta MDC, et al. Increment antimicrobial resistance during the COVID-19 pandemic: results from the invifar network. Microb Drug Resist. 2022;28(3):338–345. doi:10.1089/mdr.2021.0231.
  • Furlan L, Caramelli B. The regrettable story of the “covid kit” and the “early treatment of Covid-19” in Brazil. Lancet Reg Health Am. 2021;4:100089. doi:10.1016/j.lana.2021.100089.
  • Jeon K, Jeong S, Lee N, Park MJ, Song W, Kim HS, Kim HS, Kim JS. Impact of COVID-19 on antimicrobial consumption and spread of multidrug-resistance in bacterial infections. Antibiotic. 2022;11(4):11. doi:10.3390/antibiotics11040535.
  • Karami Z, Knoop BT, Dofferhoff ASM, Blaauw MJT, Janssen NA, van Apeldoorn M, Kerckhoffs APM, van de Maat JS, Hoogerwerf JJ, ten Oever J. Few bacterial co-infections but frequent empiric antibiotic use in the early phase of hospitalized patients with COVID-19: results from a multicentre retrospective cohort study in the Netherlands. Infect Dis. 2021;53(2):102–110. doi:10.1080/23744235.2020.1839672.
  • Van Laethem J, Wuyts S, Van Laere S, Koulalis J, Colman M, Moretti M, Seyler L, De Waele E, Pierard D, Lacor P, et al. Antibiotic prescriptions in the context of suspected bacterial respiratory tract superinfections in the COVID-19 era: a retrospective quantitative analysis of antibiotic consumption and identification of antibiotic prescription drivers. Intern Emerg Med [Internet]. 2022;17(1):141–151. doi:10.1007/s11739-021-02790-0.
  • Bazaid AS, Barnawi H, Qanash H, Alsaif G, Aldarhami A, Gattan H, Alharbi B, Alrashidi A, Al-Soud WA, Moussa S, et al. Bacterial coinfection and antibiotic resistance profiles among hospitalised COVID-19 patients. Microorgan. 2022;10(3):495. doi:10.3390/microorganisms10030495.
  • Russell CD, Fairfield CJ, Drake TM, Turtle L, Seaton RA, Wootton DG, Sigfrid L, Harrison EM, Docherty AB, de Silva TI, et al. Co-infections, secondary infections, and antimicrobial use in patients hospitalised with COVID-19 during the first pandemic wave from the ISARIC WHO CCP-UK study: a multicentre, prospective cohort study. The Lancet Microbe [Internet]. 2021;2(8):e354–65. doi:10.1016/S2666-5247(21)00090-2.
  • Arcari G, Raponi G, Sacco F, Bibbolino G, Di Lella FM, Alessandri F, Coletti M, Trancassini M, Deales A, Pugliese F, et al. Klebsiella pneumoniae infections in COVID-19 patients: a 2-month retrospective analysis in an Italian hospital. Int J Antimicrob Agents. 2021;57(1):106245. doi:10.1016/j.ijantimicag.2020.106245.
  • Chong WH, Saha BK, Ramani A, Chopra A. State-of-the-art review of secondary pulmonary infections in patients with COVID-19 pneumonia. Infection [Internet]. 2021;49(4):591–605. doi:10.1007/s15010-021-01602-z.
  • Gerver SM, Guy R, Wilson K, Thelwall S, Nsonwu O, Rooney G, Brown CS, Muller-Pebody B, Hope R, Hall V. National surveillance of bacterial and fungal coinfection and secondary infection in COVID-19 patients in England: lessons from the first wave. Clin Microbiol Infect. 2021;27(11):1658–1665. doi:10.1016/j.cmi.2021.05.040.
  • Protonotariou E, Mantzana P, Meletis G, Tychala A, Kassomenaki A, Vasilaki O, Kagkalou G, Gkeka I, Archonti M, Kati S, et al. Microbiological characteristics of bacteremias among COVID-19 hospitalized patients in a tertiary referral hospital in Northern Greece during the second epidemic wave. FEMS Microbes [Internet]. 2022;2. doi:10.1093/femsmc/xtab021/6448474.
  • Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res [Internet]. 2020;30(6):492–506. doi:10.1038/s41422-020-0332-7.
  • Jang YO, Kim OH, Kim SJ, Lee SH, Yun S, Lim SE, Yoo HJ, Shin Y, Lee SW. High-fiber diets attenuate emphysema development via modulation of gut microbiota and metabolism. Sci Rep. 2021;11(1):7008. doi:10.1038/s41598-021-86404-x.
  • Sampson TR, Mazmanian SK. Control of brain development, function, and behavior by the microbiome. Cell Host & Microbe. 2015;17(5):565–576. doi:10.1016/j.chom.2015.04.011.
  • Bajinka O, Simbilyabo L, Tan Y, Jabang J, Saleem SA. Lung-brain axis. Crit Rev Microbiol [Internet]. 2022;48(3):257–269. doi:10.1080/1040841X.2021.1960483.
  • Hosang L, Canals RC, van der Flier FJ, Hollensteiner J, Daniel R, Flügel A, Odoardi F. The lung microbiome regulates brain autoimmunity. Nature [Internet]. 2022;603(7899):138–144. doi:10.1038/s41586-022-04427-4.
  • Monje M, Iwasaki A. The neurobiology of long COVID. Neuron [Internet]. 2022;110(21):3484–3496. doi:10.1016/j.neuron.2022.10.006.
  • Taquet M, Geddes JR, Husain M, Luciano S, Harrison PJ. 6-month neurological and psychiatric outcomes in 236 379 survivors of COVID-19: a retrospective cohort study using electronic health records. The Lancet Psych [Internet]. 2021;8(5):416–427. doi:10.1016/S2215-0366(21)00084-5.
  • Yang I, Arthur RA, Zhao L, Clark J, Hu Y, Corwin EJ, Lah J. The oral microbiome and inflammation in mild cognitive impairment. Exp Gerontol. 2021;147:111273. doi:10.1016/j.exger.2021.111273.
  • Erny D, Hrabě de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci [Internet]. 2015;18(7):965–977. doi:10.1038/nn.4030.
  • Dang AT, Marsland BJ. Microbes, metabolites, and the gut–lung axis. Mucosal Immunol [Internet]. 2019;12(4):843–850. doi:10.1038/s41385-019-0160-6.
  • Doifode T, Giridharan VV, Generoso JS, Bhatti G, Collodel A, Schulz PE, Forlenza OV, Barichello T. The impact of the microbiota-gut-brain axis on Alzheimer’s disease pathophysiology. Pharmacol Res. 2021;164:105314. doi:10.1016/j.phrs.2020.105314.
  • Saia RS, Giusti H, Luis-Silva F, Pedroso K, Auxiliadora-Martins M, Morejón KML, Degiovani AM, Cadelca MR, Basile-Filho A. Clinical investigation of intestinal fatty acid-binding protein (I-FABP) as a biomarker of SARS-CoV-2 infection. Int J Infect Dis [Internet]. 2021;113:82–86. doi:10.1016/j.ijid.2021.09.051.
  • Mańkowska-Wierzbicka D, Zuraszek J, Wierzbicka A, Gabryel M, Mahadea D, Baturo A, Zakerska-Banaszak O, Slomski R, Skrzypczak-Zielinska M, Dobrowolska A. Alterations in gut microbiota composition in patients with COVID-19: a pilot study of whole hypervariable 16S rRNA gene sequencing. Biomed. 2023;11(2):11. doi:10.3390/biomedicines11020367.
  • Al Bataineh MT, Henschel A, Mousa M, Daou M, Waasia F, Kannout H, Khalili M, Kayasseh MA, Alkhajeh A, Uddin M. Gut microbiota interplay with COVID-19 reveals links to host lipid metabolism among middle eastern populations. Front Microbiol. 2021;12:12. doi:10.3389/fmicb.2021.761067.
  • Jang SE, Lim SM, Jeong JJ, Jang HM, Lee HJ, Han MJ, Kim DH. Gastrointestinal inflammation by gut microbiota disturbance induces memory impairment in mice. Mucosal Immunol. 2018;11(2):369–379. doi:10.1038/mi.2017.49.
  • Kim N, Jeon SH, Ju IG, Gee MS, Do J, Oh MS, Lee JK. Transplantation of gut microbiota derived from alzheimer’s disease mouse model impairs memory function and neurogenesis in C57BL/6 mice. Brain Behav Immun [Internet]. 2021;98:357–365. doi:10.1016/j.bbi.2021.09.002.
  • Vieira AT, Galvão I, Amaral FA, Teixeira MM, Nicoli JR, Martins FS. Oral treatment with bifidobacterium longum 5 1A reduced inflammation in a murine experimental model of gout. Benef Microbes [Internet]. 2015;6(6):799–806. doi:10.3920/BM2015.0015.
  • Alharbi KS, Singh Y, Hassan Almalki W, Rawat S, Afzal O, Alfawaz Altamimi AS, Kazmi I, Al-Abbasi FA, Alzarea SI, Singh SK, et al. Gut microbiota disruption in COVID-19 or post-COVID illness association with severity biomarkers: a possible role of pre/pro-biotics in manipulating microflora. Chem Biol Interact. 2022;358:109898. doi:10.1016/j.cbi.2022.109898.
  • Mukhopadhya I, Segal JP, Carding SR, Hart AL, Hold GL. The gut virome: the “missing link” between gut bacteria and host immunity? Therap Adv Gastroenterol. 2019;12:1756284819836620. doi:10.1177/1756284819836620.
  • Yuan L, Hensley C, Mahsoub HM, Ramesh AK, Zhou P. Microbiota in viral infection and disease in humans and farm animals. Prog Mol Biol Transl Sci. 2020;171:15–60. doi:10.1016/bs.pmbts.2020.04.005.
  • Lu ZH, Zhou HW, Wu WK, Fu T, Yan M, He Z, Sun SW, Ji ZH, Shao Z. Alterations in the composition of intestinal DNA virome in patients with COVID-19 [Internet]. Front Cell Infect Microbiol. 2021;11:11. doi:10.3389/fcimb.2021.790422.
  • Natarajan A, Zlitni S, Brooks EF, Vance SE, Dahlen A, Hedlin H, Park RM, Han A, Schmidtke DT, Verma R, et al. Gastrointestinal symptoms and fecal shedding of SARS-CoV-2 RNA suggest prolonged gastrointestinal infection. Med [Internet]. 2022;3(6):371–387.e9. doi:10.1016/j.medj.2022.04.001.
  • Coryell MP, Iakiviak M, Pereira N, Murugkar PP, Rippe J, Williams DB, Heald-Sargent T, Sanchez-Pinto LN, Chavez J, Hastie JL, et al. A method for detection of SARS-CoV-2 RNA in healthy human stool: a validation study. Lancet Microbe. 2021;2(6):e259–66. doi:10.1016/S2666-5247(21)00059-8.
  • Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi:10.1038/s41587-019-0209-9.
  • Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. doi:10.7717/peerj.2584.
  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41(D1):D590–6. doi:10.1093/nar/gks1219.
  • Love M, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):10–1186. doi:10.1186/s13059-014-0550-8.
  • Blighe K, Sharmila Rana ML. Enhanced volcano: publication-ready volcano plots with enhanced colouring and labeling. R Packag Version 1. 2019. https://bioconductor.org/packages/devel/bioc/vignettes/EnhancedVolcano/inst/doc/EnhancedVolcano.html.
  • Assis GBN, Pereira FL, Zegarra AU, Tavares GC, Leal CA, Figueiredo HCP. Use of MALDI-TOF mass spectrometry for the fast identification of gram-positive fish pathogens. Front Microbiol. 2017;8. doi:10.3389/fmicb.2017.01492.
  • Vieira AT, Macia L, Galvão I, Martins FS, Canesso MCC, Amaral FA, Garcia CC, Maslowski KM, De Leon E, Shim D, et al. A role for gut microbiota and the metabolite-sensing receptor GPR43 in a murine model of gout. Arthritis & Rheumatol. 2015;67(6):1646–1656. doi:10.1002/art.39107.
  • Garcia CC, Russo RC, Guabiraba R, Fagundes CT, Polidoro RB, Tavares LP, Salgado APC, Cassali GD, Sousa LP, Machado AV, et al. Platelet-activating factor receptor plays a role in lung injury and death caused by influenza a in mice. PLoS Pathog. 2010;6(11):e1001171. doi:10.1371/journal.ppat.1001171.
  • Horvat JC, Beagley KW, Wade MA, Preston JA, Hansbro NG, Hickey DK, Kaiko GE, Gibson PG, Foster PS, Hansbro PM. Neonatal chlamydial infection induces mixed T-cell responses that drive allergic airway disease. Am J Respir Crit Care Med. 2007;176(6):556–564. doi:10.1164/rccm.200607-1005OC.
  • Profeta R, Seyffert N, Tiwari S, Viana MVC, Jaiswal AK, Caetano AC, Bücker DH, Tavares de Oliveira L, Santos R, Gala-Garcia A, et al. Comparative genomics with a multidrug-resistant Klebsiella pneumoniae isolate reveals the panorama of unexplored diversity in Northeast Brazil. Gene. 2021;772:145386. doi:10.1016/j.gene.2020.145386.
  • Melo HM, Seixas da Silva GS, Sant’ana MR, Teixeira CVL, Clarke JR, Miya Coreixas VS, de Melo BC, Fortuna JTS, Forny-Germano L, Ledo JH, et al. Palmitate is increased in the cerebrospinal fluid of humans with obesity and induces memory impairment in mice via pro-inflammatory TNF-α. Cell Rep. 2020;30(7):2180–2194.e8. doi:10.1016/j.celrep.2020.01.072.
  • Santos SS, Miranda VC, Trindade LM, Cardoso VN, Reis DC, Cassali GD, Nicoli JR, Cara DC, Martins FS. Bifidobacterium longum subsp. longum 51A attenuates signs of inflammation in a murine model of food allergy. Probiotics Antimicrob Proteins [Internet]. 2021;15(1):63–73. doi:10.1007/s12602-021-09846-9.

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