Gut Microbiota and Aging

  • Daria A. KashtanovaEmail author
  • Olga N. Tkacheva
  • Irina D. Strazhesko
  • Ekaterina N. Dudinskaya
  • Yu V. Kotovskaya
  • A. S. Popenko
  • A. V. Tyaht
  • D. G. Alexeev
Part of the Healthy Ageing and Longevity book series (HAL, volume 10)


Gut microbiota is an up-to date theme that is widely studied. Now it is obvious that microbiota could be considered as one of the factors affecting aging process. Some reports suggested the potential mechanisms by which gut microbes may influence human health span. Aging-related conditions are accompanied by decline in immune system functioning and low-grade inflammation, and our microbes play a certain role in these processes. Gut microbiota composition changes during the aging process may indicate a more pronounced aging-related health loss.


Microbiome Gut microbiota Longevity Butyrate Aging-associated diseases Short-chain fatty acids Low-grade inflammation Inflammaging Lipopolysaccharide 


  1. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J (2014) The placenta harbors a unique microbiome. Sci Transl Med. 6(237):237ra65PubMedPubMedCentralCrossRefGoogle Scholar
  2. Almeida Morais C, Oyama LM, de Oliveira JL, Carvalho Garcia M, de Rosso VV, Sousa Mendes Amigo L et al (2014) Jussara (Euterpe edulis Mart.) supplementation during pregnancy and lactation modulates the gene and protein expression of inflammation biomarkers induced by trans-fatty acids in the colon of offspring. Mediators Inflamm 2014:987927PubMedPubMedCentralCrossRefGoogle Scholar
  3. An HM, Baek EH, Jang S, Lee DK, Kim MJ, Kim JR et al (2010) Efficacy of Lactic Acid Bacteria (LAB) supplement in management of constipation among nursing home residents. Nutr J 9:5PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aroniadis OC, Brandt LJ (2013) Fecal microbiota transplantation: past, present and future. Curr Opin Gastroenterol 29(1):79–84PubMedCrossRefGoogle Scholar
  5. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR et al (2011) Enterotypes of the human gut microbiome. Nature 473(7346):174–180PubMedPubMedCentralCrossRefGoogle Scholar
  6. Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157(1):121–141PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bergstrom A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT et al (2014) Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol 80(9):2889–2900PubMedPubMedCentralCrossRefGoogle Scholar
  8. Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E et al (2010) Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 5(5):e10667PubMedPubMedCentralCrossRefGoogle Scholar
  9. Biagi E, Candela M, Fairweather-Tait S, Franceschi C, Brigidi P (2012) Aging of the human metaorganism: the microbial counterpart. Age (Dordr). 34(1):247–267PubMedCrossRefGoogle Scholar
  10. Biagi E, Candela M, Turroni S, Garagnani P, Franceschi C, Brigidi P (2013) Ageing and gut microbes: perspectives for health maintenance and longevity. Pharmacol Res 69(1):11–20PubMedCrossRefGoogle Scholar
  11. Buford TW, Carter CS, VanDerPol WJ, Chen D, Lefkowitz EJ, Eipers P et al (2018) Composition and richness of the serum microbiome differ by age and link to systemic inflammation. Geroscience 40:257PubMedPubMedCentralCrossRefGoogle Scholar
  12. Canani RB, Costanzo MD, Leone L, Bedogni G, Brambilla P, Cianfarani S et al (2011) Epigenetic mechanisms elicited by nutrition in early life. Nutr Res Rev 24(2):198–205PubMedPubMedCentralCrossRefGoogle Scholar
  13. Candela M, Guidotti M, Fabbri A, Brigidi P, Franceschi C, Fiorentini C (2011) Human intestinal microbiota: cross-talk with the host and its potential role in colorectal cancer. Crit Rev Microbiol 37(1):1–14PubMedCrossRefGoogle Scholar
  14. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336PubMedPubMedCentralCrossRefGoogle Scholar
  15. Carlsson M, Gustafson Y, Haglin L, Eriksson S (2009) The feasibility of serving liquid yoghurt supplemented with probiotic bacteria, Lactobacillus rhamnosus LB 21, and Lactococcus lactis L1A–a pilot study among old people with dementia in a residential care facility. J Nutr Health Aging 13(9):813–819PubMedCrossRefGoogle Scholar
  16. Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C et al (2017) Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging 49:60–68PubMedCrossRefGoogle Scholar
  17. Chen T, Zhou Q, Zhang D, Jiang F, Wu J, Zhou JY et al (2018) Effect of faecal microbiota transplantation for treatment of clostridium difficile infection in patients with inflammatory bowel disease: a systematic review and meta-analysis of cohort studies. J Crohns Colitis 12(6):710–717PubMedCrossRefGoogle Scholar
  18. Ciccocioppo R, Di Sabatino A, Luinetti O, Rossi M, Cifone MG, Corazza GR (2002) Small bowel enterocyte apoptosis and proliferation are increased in the elderly. Gerontology 48(4):204–208PubMedCrossRefGoogle Scholar
  19. Claesson MJ, Cusack S, O’Sullivan O, Greene-Diniz R, de Weerd H, Flannery E et al (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A 108(Suppl 1):4586–4591CrossRefGoogle Scholar
  20. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S et al (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410):178–184CrossRefGoogle Scholar
  21. Clark RI, Salazar A, Yamada R, Fitz-Gibbon S, Morselli M, Alcaraz J et al (2015) Distinct shifts in microbiota composition during drosophila aging impair intestinal function and drive mortality. Cell Rep 12(10):1656–1667PubMedPubMedCentralCrossRefGoogle Scholar
  22. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P et al (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44(4):812–826PubMedCrossRefPubMedCentralGoogle Scholar
  23. Costello SP, Soo W, Bryant RV, Jairath V, Hart AL, Andrews JM (2017) Systematic review with meta-analysis: faecal microbiota transplantation for the induction of remission for active ulcerative colitis. Aliment Pharmacol Ther 46(3):213–224PubMedCrossRefPubMedCentralGoogle Scholar
  24. Danikowski KM, Jayaraman S, Prabhakar BS (2017) Regulatory T cells in multiple sclerosis and myasthenia gravis. J Neuroinflamm, p 14Google Scholar
  25. Debebe T, Biagi E, Soverini M, Holtze S, Hildebrandt TB, Birkemeyer C et al (2017) Unraveling the gut microbiome of the long-lived naked mole-rat. Sci Rep 7(1):9590PubMedPubMedCentralCrossRefGoogle Scholar
  26. Egshatyan L, Kashtanova D, Popenko A, Tkacheva O, Tyakht A, Alexeev D et al (2016) Gut microbiota and diet in patients with different glucose tolerance. Endocr Connect 5(1):1–9PubMedCrossRefPubMedCentralGoogle Scholar
  27. Faty A, Ferre P, Commans S (2012) The acute phase protein Serum Amyloid A induces lipolysis and inflammation in human adipocytes through distinct pathways. PLoS One 7(4):e34031PubMedPubMedCentralCrossRefGoogle Scholar
  28. Fedintsev A, Kashtanova D, Tkacheva O, Strazhesko I, Kudryavtseva A, Baranova A et al (2017) Markers of arterial health could serve as accurate non-invasive predictors of human biological and chronological age. Aging-US 9(4):1280–1292CrossRefGoogle Scholar
  29. Felice VD, Quigley EM, Sullivan AM, O’Keeffe GW, O’Mahony SM (2016) Microbiota-gut-brain signalling in Parkinson’s disease: implications for non-motor symptoms. Parkinsonism Relat Disord 27:1–8PubMedCrossRefPubMedCentralGoogle Scholar
  30. Fitzgerald KA, Rowe DC, Golenbock DT (2004) Endotoxin recognition and signal transduction by the TLR4/MD2-complex. Microbes Infect 6(15):1361–1367PubMedCrossRefGoogle Scholar
  31. Fransen F, van Beek AA, Borghuis T, Aidy SE, Hugenholtz F, van der Gaast-de Jongh C et al (2017) Aged gut microbiota contributes to systemical inflammaging after transfer to germ-free mice. Front Immunol 8:1385PubMedPubMedCentralCrossRefGoogle Scholar
  32. Gangloff SC, Hijiya N, Haziot A, Goyert SM (1999) Lipopolysaccharide structure influences the macrophage response via CD14-independent and CD14-dependent pathways. Clin Infect Dis 28(3):491–496PubMedCrossRefGoogle Scholar
  33. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M et al (2009) Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58(7):1509–1517PubMedPubMedCentralCrossRefGoogle Scholar
  34. Gareau MG, Wine E, Rodrigues DM, Cho JH, Whary MT, Philpott DJ et al (2011) Bacterial infection causes stress-induced memory dysfunction in mice. Gut 60(3):307–317PubMedCrossRefGoogle Scholar
  35. Guillemard E, Tondu F, Lacoin F, Schrezenmeir J (2010) Consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114001 reduces the duration of respiratory infections in the elderly in a randomised controlled trial. Br J Nutr 103(1):58–68PubMedCrossRefGoogle Scholar
  36. Harig JM, Soergel KH, Komorowski RA, Wood CM (1989) Treatment of diversion colitis with short-chain-fatty acid irrigation. N Engl J Med 320(1):23–28PubMedCrossRefPubMedCentralGoogle Scholar
  37. Hickson M, D’Souza AL, Muthu N, Rogers TR, Want S, Rajkumar C et al (2007) Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: randomised double blind placebo controlled trial. BMJ 335(7610):80PubMedPubMedCentralCrossRefGoogle Scholar
  38. Jackson MA, Goodrich JK, Maxan ME, Freedberg DE, Abrams JA, Poole AC et al (2016) Proton pump inhibitors alter the composition of the gut microbiota. Gut 65(5):749–756PubMedCrossRefGoogle Scholar
  39. Jimenez E, Fernandez L, Marin ML, Martin R, Odriozola JM, Nueno-Palop C et al (2005) Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol 51(4):270–274PubMedCrossRefGoogle Scholar
  40. Kahn MS, Kranjac D, Alonzo CA, Haase JH, Cedillos RO, McLinden KA et al (2012) Prolonged elevation in hippocampal Abeta and cognitive deficits following repeated endotoxin exposure in the mouse. Behav Brain Res 229(1):176–184PubMedCrossRefGoogle Scholar
  41. Kashtanova D.A, ELV, Tkacheva ON (2015) The involvement of human gut microbiota in chronic systemic inflammation. Clin Microbiol Antimicrob 17(4):310–317Google Scholar
  42. Kashtanova D, Tkacheva O, Popenko A, Egshatyan L, Tyakht A, Alexeev D et al (2017) Gut microbiota and vascular biomarkers in patients without clinical cardiovascular diseases. Artery Res 18:41–48CrossRefGoogle Scholar
  43. Kee VR (2012) Clostridium difficile infection in older adults: a review and update on its management. Am J Geriatr Pharmacother 10(1):14–24PubMedCrossRefGoogle Scholar
  44. Klimenko NS, Tyakht AV, Popenko AS, Vasiliev AS, Altukhov IA, Ischenko DS, Shashkova TI, Efimova DA, Nikogosov DA, Osipenko DA, Musienko SV, Selezneva KS, Baranova A, Kurilshikov AM, Toshchakov SM, Korzhenkov AA, Samarov NI, Shevchenko MA, Tepliuk AV, Alexeev DG (2018) Microbiome responses to an uncontrolled short-term diet intervention in the frame of the citizen science project. Nutrients 10:576PubMedCentralCrossRefPubMedGoogle Scholar
  45. Kumari R, Ahuja V, Paul J (2013) Fluctuations in butyrate-producing bacteria in ulcerative colitis patients of North India. World J Gastroenterol 19(22):3404–3414PubMedPubMedCentralCrossRefGoogle Scholar
  46. Leffler DA, Lamont JT (2015) Clostridium difficile infection. N Engl J Med 373(3):287–288PubMedGoogle Scholar
  47. Liu AH, Redmon AH Jr (2001) Endotoxin: friend or foe? Allergy Asthma Proc 22(6):337–340PubMedGoogle Scholar
  48. Liu C, Finegold SM, Song Y, Lawson PA (2008) Reclassification of Clostridium coccoides, Ruminococcus hansenii, Ruminococcus hydrogenotrophicus, Ruminococcus luti, Ruminococcus productus and Ruminococcus schinkii as Blautia coccoides gen. nov., comb. nov., Blautia hansenii comb. nov., Blautia hydrogenotrophica comb. nov., Blautia luti comb. nov., Blautia producta comb. nov., Blautia schinkii comb. nov. and description of Blautia wexlerae sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 58(Pt 8):1896–1902PubMedCrossRefGoogle Scholar
  49. Lorea Baroja M, Kirjavainen PV, Hekmat S, Reid G (2007) Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clin Exp Immunol 149(3):470–479PubMedPubMedCentralCrossRefGoogle Scholar
  50. Ma HL, Napierata L, Stedman N, Benoit S, Collins M, Nickerson-Nutter C et al (2010) Tumor Necrosis Factor alpha Blockade Exacerbates Murine Psoriasis-like disease by enhancing Th17 function and decreasing expansion of Treg cells. Arthritis Rheum-Us 62(2):430–440CrossRefGoogle Scholar
  51. Man AL, Bertelli E, Rentini S, Regoli M, Briars G, Marini M et al (2015) Age-associated modifications of intestinal permeability and innate immunity in human small intestine. Clin Sci (Lond) 129(7):515–527CrossRefGoogle Scholar
  52. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D et al (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461(7268):1282–1286PubMedPubMedCentralCrossRefGoogle Scholar
  53. Matsumoto M, Kurihara S, Kibe R, Ashida H, Benno Y (2011) Longevity in mice is promoted by probiotic-induced suppression of colonic senescence dependent on upregulation of gut bacterial polyamine production. PLoS One 6(8):e23652PubMedPubMedCentralCrossRefGoogle Scholar
  54. Migita K, Eguchi K, Tsukada T, Kawabe Y, Takashima H, Mine M et al (1996) Increased circulating serum amyloid A protein derivatives in rheumatoid arthritis patients with secondary amyloidosis. Lab Invest 75(3):371–375PubMedGoogle Scholar
  55. Minato T, Maeda T, Fujisawa Y, Tsuji H, Nomoto K, Ohno K et al (2017) Progression of Parkinson’s disease is associated with gut dysbiosis: two-year follow-up study. PLoS One 12(11):e0187307PubMedPubMedCentralCrossRefGoogle Scholar
  56. Moayyedi P, Yuan Y, Baharith H, Ford AC (2017) Faecal microbiota transplantation for <em> Clostridium difficile </em> -associated diarrhoea: a systematic review of randomised controlled trials. Med J Aust 207(4):166–172PubMedCrossRefGoogle Scholar
  57. Moles L, Gomez M, Heilig H, Bustos G, Fuentes S, de Vos W et al (2013) Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS ONE 8(6):e66986PubMedPubMedCentralCrossRefGoogle Scholar
  58. Nicoletti C (2015) Age-associated changes of the intestinal epithelial barrier: local and systemic implications. Expert Rev Gastroenterol Hepatol 9(12):1467–1469PubMedCrossRefGoogle Scholar
  59. Ottaviani E, Ventura N, Mandrioli M, Candela M, Franchini A, Franceschi C (2011) Gut microbiota as a candidate for lifespan extension: an ecological/evolutionary perspective targeted on living organisms as metaorganisms. Biogerontology 12(6):599–609PubMedCrossRefGoogle Scholar
  60. Ou J, DeLany JP, Zhang M, Sharma S, O’Keefe SJ (2012) Association between low colonic short-chain fatty acids and high bile acids in high colon cancer risk populations. Nutr Cancer 64(1):34–40PubMedCrossRefPubMedCentralGoogle Scholar
  61. Ou J, Carbonero F, Zoetendal EG, DeLany JP, Wang M, Newton K et al (2013) Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr 98(1):111–120PubMedPubMedCentralCrossRefGoogle Scholar
  62. Piccirillo CA, Shevach EM (2004) Naturally-occurring CD4(+)CD25(+) immunoregulatory T cells: central players in the arena of peripheral tolerance. Semin Immunol 16(2):81–88PubMedCrossRefPubMedCentralGoogle Scholar
  63. Pitkala KH, Strandberg TE, Finne Soveri UH, Ouwehand AC, Poussa T, Salminen S (2007) Fermented cereal with specific bifidobacteria normalizes bowel movements in elderly nursing home residents. A randomized, controlled trial. J Nutr Health Aging 11(4):305–311PubMedPubMedCentralGoogle Scholar
  64. Pronio A, Montesani C, Butteroni C, Vecchione S, Mumolo G, Vestri A et al (2008) Probiotic administration in patients with ileal pouch-anal anastomosis for ulcerative colitis is associated with expansion of mucosal regulatory cells. Inflamm Bowel Dis 14(5):662–668PubMedCrossRefPubMedCentralGoogle Scholar
  65. Qi Y, Goel R, Kim S, Richards EM, Carter CS, Pepine CJ et al (2017) Intestinal permeability biomarker Zonulin is elevated in healthy aging. J Am Med Dir Assoc 18(9):810 e1–e4CrossRefGoogle Scholar
  66. Rera M, Clark RI, Walker DW (2012) Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proc Natl Acad Sci U S A 109(52):21528–21533PubMedPubMedCentralCrossRefGoogle Scholar
  67. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL et al (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341(6150):1241214PubMedCrossRefPubMedCentralGoogle Scholar
  68. Sanchez AM, Yang YP (2011) The role of natural regulatory T cells in infection. Immunol Res 49(1–3):124–134PubMedPubMedCentralCrossRefGoogle Scholar
  69. Santoro A, Ostan R, Candela M, Biagi E, Brigidi P, Capri M et al (2018) Gut microbiota changes in the extreme decades of human life: a focus on centenarians. Cell Mol Life Sci 75(1):129–148PubMedPubMedCentralCrossRefGoogle Scholar
  70. Scheepers LE, Penders J, Mbakwa CA, Thijs C, Mommers M, Arts IC (2015) The intestinal microbiota composition and weight development in children: the KOALA birth cohort study. Int J Obes (Lond). 39(1):16–25CrossRefGoogle Scholar
  71. Serra-Prat M, Palomera E, Clave P, Puig-Domingo M (2009) Effect of age and frailty on ghrelin and cholecystokinin responses to a meal test. Am J Clin Nutr 89(5):1410–1417PubMedCrossRefGoogle Scholar
  72. Serra-Prat M, Mans E, Palomera E, Clave P (2013) Gastrointestinal peptides, gastrointestinal motility, and anorexia of aging in frail elderly persons. Neurogastroenterol Motil 25(4):291–e45PubMedCrossRefGoogle Scholar
  73. Shen Q, Shang N, Li P (2011) In vitro and in vivo antioxidant activity of Bifidobacterium animalis 01 isolated from centenarians. Curr Microbiol 62(4):1097–1103PubMedCrossRefGoogle Scholar
  74. Shinkai S, Toba M, Saito T, Sato I, Tsubouchi M, Taira K et al (2013) Immunoprotective effects of oral intake of heat-killed Lactobacillus pentosus strain b240 in elderly adults: a randomised, double-blind, placebo-controlled trial. Br J Nutr 109(10):1856–1865PubMedCrossRefGoogle Scholar
  75. Simons JP, Al-Shawi R, Ellmerich S, Speck I, Aslam S, Hutchinson WL et al (2013) Pathogenetic mechanisms of amyloid A amyloidosis. P Natl Acad Sci USA 110(40):16115–16120CrossRefGoogle Scholar
  76. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ et al (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105(43):16731–16736PubMedCrossRefGoogle Scholar
  77. Stein JH, Korcarz CE, Hurst RT, Lonn E, Kendall CB, Mohler ER et al (2008) Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: a consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Endorsed by the society for vascular medicine. J Am Soc Echocardiogr 21(2):93–111; quiz 89–90PubMedCrossRefGoogle Scholar
  78. Sun MF, Zhu YL, Zhou ZL, Jia XB, Xu YD, Yang Q et al (2018) Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson’s disease mice: gut microbiota, glial reaction and TLR4/TNF-alpha signaling pathway. Brain Behav Immun 70:48–60PubMedCrossRefGoogle Scholar
  79. Tacke D, Wisplinghoff H, Kretzschmar A, Farowski F, Koehler P, Herweg J et al (2015) First implementation of frozen, capsulized faecal microbiota transplantation for recurrent Clostridium difficile infection into clinical practice in Europe. Clin Microbiol Infect 21(11):e82–e84PubMedCrossRefGoogle Scholar
  80. Thevaranjan N, Puchta A, Schulz C, Naidoo A, Szamosi JC, Verschoor CP et al (2017) Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host Microb 21(4):455–66 e4CrossRefGoogle Scholar
  81. Tiihonen K, Tynkkynen S, Ouwehand A, Ahlroos T, Rautonen N (2008) The effect of ageing with and without non-steroidal anti-inflammatory drugs on gastrointestinal microbiology and immunology. Br J Nutr 100(1):130–137PubMedCrossRefGoogle Scholar
  82. Tsukamoto H, Fukudome K, Takao S, Tsuneyoshi N, Kimoto M (2010) Lipopolysaccharide-binding protein-mediated Toll-like receptor 4 dimerization enables rapid signal transduction against lipopolysaccharide stimulation on membrane-associated CD14-expressing cells. Int Immunol 22(4):271–280PubMedCrossRefGoogle Scholar
  83. Tsun JGS, Shiu SWM, Wong Y, Yung S, Chan TM, Tan KCB (2013) Impact of serum amyloid A on cellular cholesterol efflux to serum in type 2 diabetes mellitus. Atherosclerosis 231(2):405–410PubMedCrossRefGoogle Scholar
  84. Tuovinen E, Keto J, Nikkila J, Matto J, Lahteenmaki K (2013) Cytokine response of human mononuclear cells induced by intestinal Clostridium species. Anaerobe 19:70–76PubMedCrossRefGoogle Scholar
  85. Tyakht AV, Manolov AI, Kanygina AV, Ischenko DS, Kovarsky BA, Popenko AS, Pavlenko AV, Elizarova AV, Rakitina DV, Baikova JP, Ladygina VG, Kostryukova ES, Karpova IY, Semashko TA, Larin AK, Grigoryeva TV, Sinyagina MN, Malanin SY, Shcherbakov PL, Kharitonova AY, Khalif IL, Shapina MV, Maev IV, Andreev DN, Belousova EA, Buzunova YM, Alexeev DG, Govorun VM (2018) Genetic diversity of Escherichia coli in gut microbiota of patients with Crohn’s disease discovered using metagenomic and genomic analyses. BMC Genom 19(1):968. Scholar
  86. Vernia P, Cittadini M, Caprilli R, Torsoli A (1995) Topical treatment of refractory distal ulcerative colitis with 5-ASA and sodium butyrate. Dig Dis Sci 40(2):305–307PubMedCrossRefGoogle Scholar
  87. Verstockt B, Ferrante M, Vermeire S, Van Assche G (2018) New treatment options for inflammatory bowel diseases. J Gastroenterol 53(5):585–590PubMedPubMedCentralCrossRefGoogle Scholar
  88. Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF et al (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143(4):913–6 e7PubMedCrossRefGoogle Scholar
  89. Wang F, Huang G, Cai D, Li D, Liang X, Yu T et al (2015) Qualitative and semiquantitative analysis of fecal bifidobacterium species in centenarians living in Bama, Guangxi China. Curr Microbiol 71(1):143–149PubMedCrossRefGoogle Scholar
  90. Wilkinson IB, McEniery CM, Schillaci G, Boutouyrie P, Segers P, Donald A et al (2010) ARTERY society guidelines for validation of non-invasive haemodynamic measurement devices: part 1, arterial pulse wave velocity. Artery Res 4(2):34–40CrossRefGoogle Scholar
  91. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334(6052):105–108PubMedPubMedCentralCrossRefGoogle Scholar
  92. Yang HY, Liu SL, Ibrahim SA, Zhao L, Jiang JL, Sun WF et al (2009) Oral administration of live Bifidobacterium substrains isolated from healthy centenarians enhanced immune function in BALB/c mice. Nutr Res 29(4):281–289PubMedCrossRefGoogle Scholar
  93. Zhang H, Lu N, Feng C, Thurston SW, Xia Y, Zhu L et al (2011) On fitting generalized linear mixed-effects models for binary responses using different statistical packages. Stat Med 30(20):2562–2572PubMedPubMedCentralCrossRefGoogle Scholar
  94. Zhang L, Qin Q, Liu M, Zhang X, He F, Wang G (2018) Akkermansia muciniphila can reduce the damage of gluco/lipotoxicity, oxidative stress and inflammation, and normalize intestine microbiota in streptozotocin-induced diabetic rats. Pathog Dis 76(4):fty028CrossRefGoogle Scholar
  95. Zijlmans MA, Korpela K, Riksen-Walraven JM, de Vos WM, de Weerth C (2015) Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology 53:233–245PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Daria A. Kashtanova
    • 1
    Email author
  • Olga N. Tkacheva
    • 1
  • Irina D. Strazhesko
    • 2
  • Ekaterina N. Dudinskaya
    • 1
  • Yu V. Kotovskaya
    • 1
  • A. S. Popenko
    • 3
  • A. V. Tyaht
    • 3
  • D. G. Alexeev
    • 3
  1. 1.Russian Clinical Research Center for Gerontology, Pirogov Russian National Research Medical UniversityMoscowRussia
  2. 2.Medical Scientific and Educational Center, Lomonosov Moscow State UniversityMoscowRussia
  3. 3.Atlas Health Europe LimitedLondonUK

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