Alterations in gut virome are associated with cognitive function and minimal hepatic encephalopathy cross-sectionally and longitudinally in cirrhosis

References

• Bloom PP, Tapper EB, Young VB, Lok AS. Microbiome therapeutics for hepatic encephalopathy. J Hepatol. 2021;75(6):1452–14. doi:10.1016/j.jhep.2021.08.004.
   PubMed Web of Science ®Google Scholar
• Smith ML, Wade JB, Wolstenholme J, Bajaj JS. Gut microbiome-brain-cirrhosis axis. Hepatology. 2023; Publish Ahead of Print. doi:10.1097/HEP.0000000000000344.
   Web of Science ®Google Scholar
• Tranah TH, Edwards LA, Schnabl B, Shawcross DL. Targeting the gut-liver-immune axis to treat cirrhosis. Gut. 2021;70(5):982–994. doi:10.1136/gutjnl-2020-320786.
   PubMed Web of Science ®Google Scholar
• Hsu CL, Schnabl B. The gut–liver axis and gut microbiota in health and liver disease. Nat Rev Microbiol. 2023;21(11):719–733. doi:10.1038/s41579-023-00904-3.
   PubMed Web of Science ®Google Scholar
• Vilstrup H, Amodio P, Bajaj J, Cordoba J, Ferenci P, Mullen KD, Weissenborn K, Wong P. Hepatic encephalopathy in chronic liver disease: 2014 Practice Guideline by the American Association for the Study of Liver Diseases and the European Association for the Study of the Liver. Hepatology. 2014;60(2):715–735. doi:10.1002/hep.27210.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Fagan A, White MB, Wade JB, Hylemon PB, Heuman DM, Fuchs M, John BV, Acharya C, Sikaroodi M, et al. Specific gut and salivary microbiota patterns are linked with different cognitive testing strategies in minimal hepatic encephalopathy. Am J Gastroenterol. 2019;114(7):1080–1090. doi:10.14309/ajg.0000000000000102.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Shamsaddini A, Fagan A, McGeorge S, Gavis E, Sikaroodi M, Brenner LA, Wade JB, Gillevet PM. Distinct gut microbial compositional and functional changes associated with impaired inhibitory control in patients with cirrhosis. Gut Microbes. 2021;13(1):1953247. doi:10.1080/19490976.2021.1953247.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Pena-Rodriguez M, La Reau A, Phillips W, Fuchs M, Davis BC, Sterling RK, Sikaroodi M, Fagan A, Shamsaddini A, et al. Longitudinal transkingdom gut microbial approach towards decompensation in outpatients with cirrhosis. Gut. 2023;72(4):759–771. doi:10.1136/gutjnl-2022-328403.
   PubMed Web of Science ®Google Scholar
• Hsu CL, Duan Y, Fouts DE, Schnabl B. Intestinal virome and therapeutic potential of bacteriophages in liver disease. J Hepatol. 2021;75(6):1465–1475. doi:10.1016/j.jhep.2021.08.003.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Sikaroodi M, Shamsaddini A, Henseler Z, Santiago-Rodriguez T, Acharya C, Fagan A, Hylemon PB, Fuchs M, Gavis E, et al. Interaction of bacterial metagenome and virome in patients with cirrhosis and hepatic encephalopathy. Gut. 2021;70(6):1162–1173. doi:10.1136/gutjnl-2020-322470.
   PubMed Web of Science ®Google Scholar
• Weissenborn K, Ennen JC, Schomerus H, Ruckert N, Hecker H. Neuropsychological characterization of hepatic encephalopathy. J Hepatol. 2001;34(5):768–773. doi:10.1016/S0168-8278(01)00026-5.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Hafeezullah M, Franco J, Varma RR, Hoffmann RG, Knox JF, Hischke D, Hammeke TA, Pinkerton SD, Saeian K, et al. Inhibitory control test for the diagnosis of minimal hepatic encephalopathy. Gastroenterology. 2008;135(5):1591–600 e1. doi:10.1053/j.gastro.2008.07.021.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Heuman DM, Sterling RK, Sanyal AJ, Siddiqui M, Matherly S, Luketic V, Stravitz RT, Fuchs M, Thacker LR, Gilles H. Validation of EncephalApp, smartphone-based Stroop test, for the diagnosis of covert hepatic encephalopathy. Clin Gastroenterol Hepatol. 2015;13(10):1828–1835.
   Web of Science ®Google Scholar
• Allampati S, Duarte-Rojo A, Thacker LR, Patidar KR, White MB, Klair JS, John B, Heuman DM, Wade JB, Flud C, et al. Diagnosis of minimal hepatic encephalopathy using Stroop EncephalApp: a multicenter US-Based, norm-based study. Am J Gastroenterol. 2016;111(1):78–86. doi:10.1038/ajg.2015.377.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Sikaroodi M, Shamsaddini A, Henseler Z, Santiago-Rodriguez T, Acharya C, Fagan A, Hylemon PB, Fuchs M, Gavis E, et al. Interaction of bacterial metagenome and virome in patients with cirrhosis and hepatic encephalopathy. Gut. 2020;70(6):1162–1173. doi:10.1136/gutjnl-2020-322470.
   PubMed Web of Science ®Google Scholar
• Martin M Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads.
   Google Scholar
• O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, Smith-White B, Ako-Adjei D, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2016;44(D1):D733–45. doi:10.1093/nar/gkv1189.
   PubMed Web of Science ®Google Scholar
• Al-Ghalith G, Knights D. BURST enables optimal exhaustive DNA alignment for big data. 2017.
   Google Scholar
• Ajami NJ, Wong MC, Ross MC, Lloyd RE, Petrosino JF. Maximal viral information recovery from sequence data using VirMAP. Nat Commun. 2018;9(1):3205. doi:10.1038/s41467-018-05658-8.
   PubMedGoogle Scholar
• Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, et al. Vegan: community ecology package. R package version. 2019.
   Google Scholar
• Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. doi:10.1186/gb-2011-12-6-r60.
   PubMed Web of Science ®Google Scholar
• Naqvi A, Rangwala H, Keshavarzian A, Gillevet P. Network-based modeling of the human gut microbiome. Chem Biodivers. 2010;7(5):1040–1050. doi:10.1002/cbdv.200900324.
   PubMed Web of Science ®Google Scholar
• Blackmer-Raynolds LD, Sampson TR. The gut-brain axis goes viral. Cell Host & Microbe. 2022;30(3):283–285. doi:10.1016/j.chom.2022.02.013.
   PubMed Web of Science ®Google Scholar
• Mayneris-Perxachs J, Castells-Nobau A, Arnoriaga-Rodriguez M, Garre-Olmo J, Puig J, Ramos R, Martínez-Hernández F, Burokas A, Coll C, Moreno-Navarrete JM, et al. Caudovirales bacteriophages are associated with improved executive function and memory in flies, mice, and humans. Cell Host & Microbe. 2022;30(3):340–56 e8. doi:10.1016/j.chom.2022.01.013.
   PubMed Web of Science ®Google Scholar
• Turner D, Shkoporov AN, Lood C, Millard AD, Dutilh BE, Alfenas-Zerbini P, van Zyl LJ, Aziz RK, Oksanen HM, Poranen MM, et al. Abolishment of morphology-based taxa and change to binomial species names: 2022 taxonomy update of the ICTV bacterial viruses subcommittee. Arch Virol. 2023;168(2):74. doi:10.1007/s00705-022-05694-2.
   PubMed Web of Science ®Google Scholar
• Dinan TG, Stilling RM, Stanton C, Cryan JF. Collective unconscious: how gut microbes shape human behavior. J Psychiatr Res. 2015;63:1–9. doi:10.1016/j.jpsychires.2015.02.021.
   PubMed Web of Science ®Google Scholar
• Enge S, Fleischhauer M, Gartner A, Reif A, Lesch KP, Kliegel M, Strobel A. Brain-derived neurotrophic factor (Val66Met) and serotonin transporter (5-HTTLPR) polymorphisms modulate plasticity in inhibitory control performance over time but Independent of inhibitory control training. Front Hum Neurosci. 2016;10:370. doi:10.3389/fnhum.2016.00370.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Zhai H, Geng J, Yu R, Ren H, Fan H, Shi P. Large-scale survey of gut microbiota associated with MHE via 16S rRNA-based pyrosequencing. Am J Gastroenterol. 2013;108(10):1601–1611. doi:10.1038/ajg.2013.221.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Hylemon PB, Ridlon JM, Heuman DM, Daita K, White MB, Monteith P, Noble NA, Sikaroodi M, Gillevet PM, et al. Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Am J Physiol Gastrointest Liver Physiol. 2012;303(6):G675–85. doi:10.1152/ajpgi.00152.2012.
   PubMed Web of Science ®Google Scholar
• Martin R, Rios-Covian D, Huillet E, Auger S, Khazaal S, Bermudez-Humaran LG, Sokol H, Chatel J-M, Langella P. Faecalibacterium: a bacterial genus with promising human health applications. FEMS Microbiol Rev. 2023;47(4):47. doi:10.1093/femsre/fuad039.
   Web of Science ®Google Scholar
• Kong C, Liu G, Kalady MF, Jin T, Ma Y. Dysbiosis of the stool DNA and RNA virome in Crohn’s disease. J Med Virol. 2023;95(2):e28573. doi:10.1002/jmv.28573.
   PubMed Web of Science ®Google Scholar
• Miller-Ensminger T, Mormando R, Maskeri L, Shapiro JW, Wolfe AJ, Putonti C, Ling Z. Introducing Lu-1, a Novel Lactobacillus jensenii Phage Abundant in the Urogenital Tract. PLoS ONE. 2020;15(6):e0234159. doi:10.1371/journal.pone.0234159.
   PubMed Web of Science ®Google Scholar
• Bosoi CR, Zwingmann C, Marin H, Parent-Robitaille C, Huynh J, Tremblay M, Rose CF. Increased brain lactate is central to the development of brain edema in rats with chronic liver disease. J Hepatol. 2014;60(3):554–560. doi:10.1016/j.jhep.2013.10.011.
   PubMed Web of Science ®Google Scholar
• Riggio O, Varriale M, Testore GP, Di Rosa R, Di Rosa E, Merli M, Romiti A, Candiani C, Capocaccia L. Effect of lactitol and lactulose administration on the fecal flora in cirrhotic patients. J Clin Gastroenterol. 1990;12(4):433–436. doi:10.1097/00004836-199008000-00016.
   PubMed Web of Science ®Google Scholar
• Seo SU, Kweon MN. Virome-host interactions in intestinal health and disease. Curr Opin Virol. 2019;37:63–71. doi:10.1016/j.coviro.2019.06.003.
   PubMed Web of Science ®Google Scholar
• Dahlman S, Avellaneda-Franco L, Barr JJ. Phages to shape the gut microbiota? Curr Opin Biotechnol. 2021;68:89–95. doi:10.1016/j.copbio.2020.09.016.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Schubert CM, Heuman DM, Wade JB, Gibson DP, Topaz A, Saeian K, Hafeezullah M, Bell DE, Sterling RK, et al. Persistence of cognitive impairment after resolution of overt hepatic encephalopathy. Gastroenterology. 2010;138(7):2332–2340. doi:10.1053/j.gastro.2010.02.015.
   PubMed Web of Science ®Google Scholar
• Wortelboer K, de Jonge PA, Scheithauer TPM, Attaye I, Kemper EM, Nieuwdorp M, Herrema H. Phage-microbe dynamics after sterile faecal filtrate transplantation in individuals with metabolic syndrome: a double-blind, randomised, placebo-controlled clinical trial assessing efficacy and safety. Nat Commun. 2023;14(1):5600. doi:10.1038/s41467-023-41329-z.
   PubMed Web of Science ®Google Scholar
• Gedgaudas R, Bajaj JS, Skieceviciene J, Valantiene I, Kiudeliene E, Bang C, Franke A, Schreiber S, Kupcinskas J. Sterile fecal filtrate from a healthy donor improves microbial diversity in patients with hepatic encephalopathy. J Gastrointestin Liver Dis. 2023;32(3):332–338. doi:10.15403/jgld-4906.
   PubMed Web of Science ®Google Scholar
• Bajaj JS, Kassam Z, Fagan A, Gavis EA, Liu E, Cox IJ, Kheradman R, Heuman D, Wang J, Gurry T, et al. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: a randomized clinical trial. Hepatology. 2017;66(6):1727–1738. doi:10.1002/hep.29306.
   PubMed Web of Science ®Google Scholar