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Open Access 01-12-2024 | Research

Altered colonic microflora and its metabolic profile in mice with acute viral myocarditis induced by coxsackievirus B3

Authors: Yimin Xue, Shirong Lin, Mingguang Chen, Jun Ke, Jiuyun Zhang, Qiaolian Fan, Yimei Chen, Feng Chen

Published in: Virology Journal | Issue 1/2024

Abstract

Mounting evidence suggests that the gut-heart axis is critical in the pathogenesis of cardiovascular diseases. The gut serves as the primary pathway through which Coxsackievirus B3 (CVB3) infects its host, leading to acute viral myocarditis (AVMC). However, little is known about the role of gut microflora and its metabolites in the development of AVMC. The AVMC model was established by intraperitoneal injection of CVB3 in mice. Then, 16S ribosomal RNA (16S rRNA) gene sequencing and ultra-high-performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS) untargeted metabolomics profiling were performed to analyze the microflora composition and metabolic profile of colonic contents. Compared to the Control mice, the AVMC mice displayed a significant reduction in gut microflora richness and diversity, as revealed by an increased abundance of Proteobacteria and a decreased abundance of Cyanobacteria and Desulfobacterota. LEfSe analysis indicated that the main genera differing between the two groups were Escherichia-Shigella, Lactobacillus, Clostridium_sensu_stricto_1, Prevotellaceae_UCG-001, and Odoribacter. Based on the criterion of OPLS-DA VIP ≥ 1.0 and p-value < 0.05, a total of 198 differential metabolites (DMs) were identified in the gut, including 79 upregulated and 119 downregulated metabolites, of which lipids and lipid-like molecules accounted for the largest proportion. Notably, both altered gut bacterial taxa and metabolites were significantly enriched in the Lipid metabolism pathway, with Traumatic acid (TA), Alpha-Linolenic acid (ALA), Eicosapentaenoic acid (EPA), and Docosahexaenoic acid (DHA) being the key DMs in the pathway. Additionally, significant positive correlations (|r| > 0.80 and p < 0.05) were found between TA levels and Anaerotruncus and Bilophila abundance, between EPA levels and Clostridium_sensu_stricto_1 abundance, and between DHA levels and Escherichia-Shigella abundance, respectively. CVB3 infection leads to notable alterations in gut microflora composition and its metabolic profile, which may participate in AVMC development. Our findings provide important clues for future in-depth studies on AVMC etiology.

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Gupta S, Markham DW, Drazner MH, Mammen PP. Fulminant myocarditis. Nat Clin Pract Cardiovasc Med. 2008;5(11):693–706. https://doi.org/10.1038/ncpcardio1331CrossRefPubMed

Sharma AN, Stultz JR, Bellamkonda N, Amsterdam EA. Fulminant myocarditis: epidemiology, pathogenesis, diagnosis, and management. Am J Cardiol. 2019;124(12):1954–60. https://doi.org/10.1016/j.amjcard.2019.09.017CrossRefPubMed

Zhou N, Zhao Y, Jiang J, Shen L, Li J, Wan J, Ma X, Zhang J, Ammirati E, Wang DW. Impact of mechanical circulatory support and immunomodulation therapy on outcome of patients with fulminant myocarditis: Chinese registry of fulminant myocarditis. Signal Transduct Target Ther. 2021;6(1):350. https://doi.org/10.1038/s41392-021-00700-6CrossRefPubMedPubMedCentral

Farinha IT, Miranda JO. Myocarditis in paediatric patients: unveiling the progression to dilated cardiomyopathy and heart failure. J Cardiovasc Dev Dis. 2016;3(4):31. https://doi.org/10.3390/jcdd3040031CrossRefPubMedPubMedCentral

Qian Q, Xiong S, Xu W. Manipulating intestinal immunity and microflora: an alternative solution to viral myocarditis? Future Microbiol. 2012;7(10):1207–16. https://doi.org/10.2217/fmb.12.96CrossRefPubMed

Caricilli AM, Castoldi A, Câmara NO. Intestinal barrier: a gentlemen’s agreement between microbiota and immunity. World J Gastrointest Pathophysiol. 2014;5(1):18–32. https://doi.org/10.4291/wjgp.v5.i1.18CrossRefPubMedPubMedCentral

Valdes AM, Walter J, Segal E, Spector TD. Role of the gut microbiota in nutrition and health. BMJ. 2018;361:k2179. https://doi.org/10.1136/bmj.k2179CrossRefPubMedPubMedCentral

Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121–41. https://doi.org/10.1016/j.cell.2014.03.011CrossRefPubMedPubMedCentral

Wang Z, Zhao Y. Gut microbiota derived metabolites in cardiovascular health and disease. Protein Cell. 2018;9(5):416–31. https://doi.org/10.1007/s13238-018-0549-0CrossRefPubMedPubMedCentral

10.

Din AU, Hassan A, Zhu Y, Yin T, Gregersen H, Wang G. Amelioration of TMAO through probiotics and its potential role in atherosclerosis. Appl Microbiol Biotechnol. 2019;103(23–24):9217–28. https://doi.org/10.1007/s00253-019-10142-4CrossRefPubMed

11.

Suzuki T, Heaney LM, Jones DJ, Ng LL. Trimethylamine N-oxide and risk stratification after acute myocardial infarction. Clin Chem. 2017;63(1):420–8. https://doi.org/10.1373/clinchem.2016.264853CrossRefPubMed

12.

Chen K, Zheng X, Feng M, Li D, Zhang H. Gut microbiota-dependent metabolite trimethylamine N-Oxide contributes to cardiac dysfunction in western diet-induced obese mice. Front Physiol. 2017;8:139. https://doi.org/10.3389/fphys.2017.00139CrossRefPubMedPubMedCentral

13.

Tang WH, Wang Z, Fan Y, Levison B, Hazen JE, Donahue LM, Wu Y, Hazen SL. Prognostic value of elevated levels of intestinal microbe-generated metabolite trimethylamine-N-oxide in patients with heart failure: refining the gut hypothesis. J Am Coll Cardiol. 2014;64(18):1908–14. https://doi.org/10.1016/j.jacc.2014.02.617CrossRefPubMed

14.

Hu T, Wu Q, Yao Q, Jiang K, Yu J, Tang Q. Short-chain fatty acid metabolism and multiple effects on cardiovascular diseases. Ageing Res Rev. 2022;81:101706. https://doi.org/10.1016/j.arr.2022.101706CrossRefPubMed

15.

Lymperopoulos A, Suster MS, Borges JI. Short-chain fatty acid receptors and cardiovascular function. Int J Mol Sci. 2022;23(6):3303. https://doi.org/10.3390/ijms23063303CrossRefPubMedPubMedCentral

16.

Yao Y, Cai X, Fei W, Ye Y, Zhao M, Zheng C. The role of short-chain fatty acids in immunity, inflammation and metabolism. Crit Rev Food Sci Nutr. 2022;62(1):1–12. https://doi.org/10.1080/10408398.2020.1854675CrossRefPubMed

17.

Pushpass RG, Alzoufairi S, Jackson KG, Lovegrove JA. Circulating bile acids as a link between the gut microbiota and cardiovascular health: impact of prebiotics, probiotics and polyphenol-rich foods. Nutr Res Rev. 2022;35(2):161–80. https://doi.org/10.1017/S0954422421000081CrossRefPubMed

18.

Desai MS, Shabier Z, Taylor M, Lam F, Thevananther S, Kosters A, Karpen SJ. Hypertrophic cardiomyopathy and dysregulation of cardiac energetics in a mouse model of biliary fibrosis. Hepatology. 2010;51(6):2097–107. https://doi.org/10.1002/hep.23585CrossRefPubMed

19.

Bui TVA, Hwangbo H, Lai Y, Hong SB, Choi YJ, Park HJ, Ban K. The gut-heart axis: updated review for the roles of microbiome in cardiovascular health. Korean Circ J. 2023;53(8):499–518. https://doi.org/10.4070/kcj.2023.0048CrossRefPubMedPubMedCentral

20.

Hu XF, Zhang WY, Wen Q, Chen WJ, Wang ZM, Chen J, Zhu F, Liu K, Cheng LX, Yang J, Shu YW. Fecal microbiota transplantation alleviates myocardial damage in myocarditis by restoring the microbiota composition. Pharmacol Res. 2019;139:412–21. https://doi.org/10.1016/j.phrs.2018.11.042CrossRefPubMed

21.

Kong Q, Chen L, Zeng X, Lu F, Huang Y, Wu W. Alterations of the gut microbiome and metabolic profile in CVB3-induced mice acute viral myocarditis. BMC Microbiol. 2023;23(1):139. https://doi.org/10.1186/s12866-023-02863-4CrossRefPubMedPubMedCentral

22.

Xue Y, Ke J, Zhang J, Chen M, Zeng L, Fan Q, Zheng C, Chen F. Analysis of long noncoding RNAs and messenger RNAs expression profiles in the hearts of mice with acute viral myocarditis. J Med Virol. 2023;95(2):e28473. https://doi.org/10.1002/jmv.28473CrossRefPubMed

23.

Grabie N, Delfs MW, Westrich JR, Love VA, Stavrakis G, Ahmad F, Seidman CE, Seidman JG, Lichtman AH. IL-12 is required for differentiation of pathogenic CD8 + T cell effectors that cause myocarditis. J Clin Invest. 2003;111(5):671–80. https://doi.org/10.1172/JCI16867CrossRefPubMedPubMedCentral

24.

Chen S, Zhou Y, Chen Y, Gu J. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884–90. https://doi.org/10.1093/bioinformatics/bty560CrossRefPubMedPubMedCentral

25.

Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27(21):2957–63. https://doi.org/10.1093/bioinformatics/btr507CrossRefPubMedPubMedCentral

26.

Edgar RC, Flyvbjerg H. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics. 2015;31(21):3476–82. https://doi.org/10.1093/bioinformatics/btv401CrossRefPubMed

27.

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. 2013;41(Database issue):D590–6. https://doi.org/10.1093/nar/gks1219CrossRefPubMed

28.

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. https://doi.org/10.1038/nmeth.f.303CrossRefPubMedPubMedCentral

29.

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. https://doi.org/10.1186/gb-2011-12-6-r60CrossRefPubMedPubMedCentral

30.

Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31(9):814–21. https://doi.org/10.1038/nbt.2676CrossRefPubMedPubMedCentral

31.

Want EJ, Masson P, Michopoulos F, Wilson ID, Theodoridis G, Plumb RS, Shockcor J, Loftus N, Holmes E, Nicholson JK. Global metabolic profiling of animal and human tissues via UPLC-MS. Nat Protoc. 2013;8(1):17–32. https://doi.org/10.1038/nprot.2012.135CrossRefPubMed

32.

Dai W, Xie D, Lu M, Li P, Lv H, Yang C, Peng Q, Zhu Y, Guo L, Zhang Y, Tan J, Lin Z. Characterization of white tea metabolome: comparison against green and black tea by a nontargeted metabolomics approach. Food Res Int. 2017;96:40–5. https://doi.org/10.1016/j.foodres.2017.03.028CrossRefPubMed

33.

Worley B, Powers R. Multivariate analysis in metabolomics. Curr Metabolomics. 2013;1(1):92–107. https://doi.org/10.2174/2213235X11301010092CrossRefPubMedPubMedCentral

34.

Xia J, Wishart DS. MetPA: a web-based metabolomics tool for pathway analysis and visualization. Bioinformatics. 2010;26(18):2342–4. https://doi.org/10.1093/bioinformatics/btq418CrossRefPubMed

35.

Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4):837–48. https://doi.org/10.1016/j.cell.2006.02.017CrossRefPubMed

36.

Zhou Q, Deng J, Pan X, Meng D, Zhu Y, Bai Y, Shi C, Duan Y, Wang T, Li X, Sluijter JP, Xiao J. Gut microbiome mediates the protective effects of exercise after myocardial infarction. Microbiome. 2022;10(1):82. https://doi.org/10.1186/s40168-022-01271-6CrossRefPubMedPubMedCentral

37.

Li J, Zhao F, Wang Y, Chen J, Tao J, Tian G, Wu S, Liu W, Cui Q, Geng B, Zhang W, Weldon R, Auguste K, Yang L, Liu X, Chen L, Yang X, Zhu B, Cai J. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5(1):14. https://doi.org/10.1186/s40168-016-0222-xCrossRefPubMedPubMedCentral

38.

Luedde M, Winkler T, Heinsen FA, Rühlemann MC, Spehlmann ME, Bajrovic A, Lieb W, Franke A, Ott SJ, Frey N. Heart failure is associated with depletion of core intestinal microbiota. ESC Heart Fail. 2017;4(3):282–90. https://doi.org/10.1002/ehf2.12155CrossRefPubMedPubMedCentral

39.

Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015;33(9):496–503. https://doi.org/10.1016/j.tibtech.2015.06.011CrossRefPubMed

40.

Wu Y, Ran L, Yang Y, Gao X, Peng M, Liu S, Sun L, Wan J, Wang Y, Yang K, Yin M, Chunyu W. Deferasirox alleviates DSS-induced ulcerative colitis in mice by inhibiting ferroptosis and improving intestinal microbiota. Life Sci. 2023;314:121312. https://doi.org/10.1016/j.lfs.2022.121312CrossRefPubMed

41.

Liu Q, Yu Z, Tian F, Zhao J, Zhang H, Zhai Q, Chen W. Surface components and metabolites of probiotics for regulation of intestinal epithelial barrier. Microb Cell Fact. 2020;19(1):23. https://doi.org/10.1186/s12934-020-1289-4CrossRefPubMedPubMedCentral

42.

Morgan KL. Infection, illness, and fenugreek seeds: was illness a good enough proxy for infection in the 2011 outbreak of shiga toxin-producing Escherichia coli O104:H4 in France? Clin Infect Dis. 2013;56(7):1055–6. https://doi.org/10.1093/cid/cis1023CrossRefPubMed

43.

De la Fuente M, Franchi L, Araya D, Díaz-Jiménez D, Olivares M, Álvarez-Lobos M, Golenbock D, González MJ, López-Kostner F, Quera R, Núñez G, Vidal R, Hermoso MA. Escherichia coli isolates from inflammatory bowel diseases patients survive in macrophages and activate NLRP3 inflammasome. Int J Med Microbiol. 2014;304(3–4):384–92. https://doi.org/10.1016/j.ijmm.2014.01.002CrossRefPubMedPubMedCentral

44.

Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C, Ferrari C, Guerra UP, Paghera B, Muscio C, Bianchetti A, Volta GD, Turla M, Cotelli MS, Gennuso M, Prelle A, Zanetti O, Lussignoli G, Mirabile D, Bellandi D, Gentile S, Belotti G, Villani D, Harach T, Bolmont T, Padovani A, Boccardi M, Frisoni GB. INDIA-FBP Group. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging. 2017;49:60–8. https://doi.org/10.1016/j.neurobiolaging.2016.08.019CrossRefPubMed

45.

Liu J, Li T, Wu H, Shi H, Bai J, Zhao W, Jiang D, Jiang X. Lactobacillus rhamnosus GG strain mitigated the development of obstructive sleep apnea-induced hypertension in a high salt diet via regulating TMAO level and CD4 + T cell induced-type I inflammation. Biomed Pharmacother. 2019;112:108580. https://doi.org/10.1016/j.biopha.2019.01.041CrossRefPubMed

46.

Cervantes-Barragan L, Chai JN, Tianero MD, Di Luccia B, Ahern PP, Merriman J, Cortez VS, Caparon MG, Donia MS, Gilfillan S, Cella M, Gordon JI, Hsieh CS, Colonna M. Lactobacillus reuteri induces gut intraepithelial CD4 + CD8αα + T cells. Science. 2017;357(6353):806–10. https://doi.org/10.1126/science.aah5825CrossRefPubMedPubMedCentral

47.

Geng Y, Yue Y, Guan Q, Ren Y, Guo L, Fan Y, Lu ZM, Shi JS, Xu ZH. Cereal vinegar sediment alleviates spontaneous Ulcerative Colitis in Il-10 deficient mice. Mol Nutr Food Res. 2021;65(24):e2001227. https://doi.org/10.1002/mnfr.202001227CrossRefPubMed

48.

Li W, Yang H, Zhao Q, Wang X, Zhang J, Zhao X. Polyphenol-Rich Loquat Fruit Extract prevents Fructose-Induced nonalcoholic fatty liver disease by modulating glycometabolism, lipometabolism, oxidative stress, inflammation, intestinal barrier, and gut microbiota in mice. J Agric Food Chem. 2019;67(27):7726–37. https://doi.org/10.1021/acs.jafc.9b02523CrossRefPubMed

49.

Yue Y, Zhang Q, Wang J. Integrated gas chromatograph-mass spectrometry (GC/MS) and MS/MS-based molecular networking reveals the analgesic and anti-inflammatory phenotypes of the sea slater Ligia exotica. Mar Drugs. 2019;17(7):395. https://doi.org/10.3390/md17070395CrossRefPubMedPubMedCentral

50.

Ramanathan S, Ravindran D, Arunachalam K, Arumugam VR. Inhibition of quorum sensing-dependent biofilm and virulence genes expression in environmental pathogen Serratia marcescens by petroselinic acid. Antonie Van Leeuwenhoek. 2018;111(4):501–15. https://doi.org/10.1007/s10482-017-0971-yCrossRefPubMed

51.

Huang W, Yan Y, Wu M, Hu J, Zhao J, Chen X, Liu W, Liu K, Li C. Preoperative fasting confers protection against intestinal ischaemia/reperfusion injury by modulating gut microbiota and their metabolites in a mouse model. Br J Anaesth. 2022;128(3):501–12. https://doi.org/10.1016/j.bja.2021.11.025CrossRefPubMed

52.

Yang RP, Cai DK, Chen YX, Gang HN, Wei M, Zhu DQ, Li SM, Yang JM, Luo SN, Bi XL, Sun DM. Metabolic insight into the neuroprotective effect of Tao-He-Cheng-Qi (THCQ) decoction on ICH rats using untargeted metabolomics. Front Pharmacol. 2021;12:636457. https://doi.org/10.3389/fphar.2021.636457CrossRefPubMedPubMedCentral

53.

Sinha SR, Haileselassie Y, Nguyen LP, Tropini C, Wang M, Becker LS, Sim D, Jarr K, Spear ET, Singh G, Namkoong H, Bittinger K, Fischbach MA, Sonnenburg JL, Habtezion A. Dysbiosis-induced secondary bile acid deficiency promotes intestinal inflammation. Cell Host Microbe. 2020;27(4):659–e6705. https://doi.org/10.1016/j.chom.2020.01.021CrossRefPubMedPubMedCentral

54.

Feng P, Li Q, Liu L, Wang S, Wu Z, Tao Y, Huang P, Wang P. Crocetin prolongs recovery period of DSS-induced colitis via altering intestinal microbiome and increasing intestinal permeability. Int J Mol Sci. 2022;23(7):3832. https://doi.org/10.3390/ijms23073832CrossRefPubMedPubMedCentral

55.

Yates CM, Calder PC, Ed Rainger G. Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacol Ther. 2014;141(3):272–82. https://doi.org/10.1016/j.pharmthera.2013.10.010CrossRefPubMed

56.

Radzikowska U, Rinaldi AO, Çelebi Sözener Z, Karaguzel D, Wojcik M, Cypryk K, Akdis M, Akdis CA, Sokolowska M. The influence of dietary fatty acids on immune responses. Nutrients. 2019;11(12):2990. https://doi.org/10.3390/nu11122990CrossRefPubMedPubMedCentral

57.

Watson H, Mitra S, Croden FC, Taylor M, Wood HM, Perry SL, Spencer JA, Quirke P, Toogood GJ, Lawton CL, Dye L, Loadman PM, Hull MA. A randomised trial of the effect of omega-3 polyunsaturated fatty acid supplements on the human intestinal microbiota. Gut. 2018;67(11):1974–83. https://doi.org/10.1136/gutjnl-2017-314968CrossRefPubMed

58.

Lim RRX, Park MA, Wong LH, Haldar S, Lim KJ, Nagarajan N, Henry CJ, Jiang YR, Moskvin OV. Gut microbiome responses to dietary intervention with hypocholesterolemic vegetable oils. NPJ Biofilms Microbiomes. 2022;8(1):24. https://doi.org/10.1038/s41522-022-00287-yCrossRefPubMedPubMedCentral

59.

Siracusa R, Impellizzeri D, Cordaro M, Gugliandolo E, Peritore AF, Di Paola R, Cuzzocrea S. Topical application of adelmidrol + trans-traumatic acid enhances skin wound healing in a streptozotocin-induced diabetic mouse model. Front Pharmacol. 2018;9:871. https://doi.org/10.3389/fphar.2018.00871CrossRefPubMedPubMedCentral

60.

Zhao Q, Yu J, Zhou H, Wang X, Zhang C, Hu J, Hu Y, Zheng H, Zeng F, Yue C, Gu L, Wang Z, Zhao F, Zhou P, Zhang H, Huang N, Wu W, Zhou Y, Li J. Intestinal dysbiosis exacerbates the pathogenesis of psoriasis-like phenotype through changes in fatty acid metabolism. Signal Transduct Target Ther. 2023;8(1):40. https://doi.org/10.1038/s41392-022-01219-0CrossRefPubMedPubMedCentral

61.

An L, Wuri J, Zheng Z, Li W, Yan T. Microbiota modulate doxorubicin induced cardiotoxicity. Eur J Pharm Sci. 2021;166:105977. https://doi.org/10.1016/j.ejps.2021.105977CrossRefPubMed

62.

Luo Y, Zhang Y, Han X, Yuan Y, Zhou Y, Gao Y, Yu H, Zhang J, Shi Y, Duan Y, Zhao X, Yan S, Hao H, Dai C, Zhao S, Shi J, Li W, Zhang S, Xu W, Fang N, Gong Y, Li Y. Akkermansia muciniphila prevents cold-related atrial fibrillation in rats by modulation of TMAO induced cardiac pyroptosis. EBioMedicine. 2022;82:104087. https://doi.org/10.1016/j.ebiom.2022.104087CrossRefPubMedPubMedCentral

63.

Kim ES, Yoon BH, Lee SM, Choi M, Kim EH, Lee BW, Kim SY, Pack CG, Sung YH, Baek IJ, Jung CH, Kim TB, Jeong JY, Ha CH. Fecal microbiota transplantation ameliorates atherosclerosis in mice with C1q/TNF-related protein 9 genetic deficiency. Exp Mol Med. 2022;54(2):103–14. https://doi.org/10.1038/s12276-022-00728-wCrossRefPubMedPubMedCentral

Title: Altered colonic microflora and its metabolic profile in mice with acute viral myocarditis induced by coxsackievirus B3
Authors: Yimin Xue
Shirong Lin
Mingguang Chen
Jun Ke
Jiuyun Zhang
Qiaolian Fan
Yimei Chen
Feng Chen
Publication date: 01-12-2024
Publisher: BioMed Central
Published in: Virology Journal / Issue 1/2024
Electronic ISSN: 1743-422X
DOI: https://doi.org/10.1186/s12985-024-02571-z

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