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Review

Gut microbiome in healthy aging versus those associated with frailty

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Article: 2278225 | Received 15 Mar 2023, Accepted 27 Oct 2023, Published online: 15 Nov 2023

References

  • United Nations. 2022. Department of economic and social affairs, population division. World population prospects 2022: summary of results. Report No.: UN DESA/POP/2022/TR/NO.3.
  • Garmany A, Yamada S, Terzic A. Longevity leap: mind the healthspan gap. NPJ Regen Med. 2021;6:57. doi:10.1038/s41536-021-00169-5.
  • Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell. 2013;153(6):1194–18. doi:10.1016/j.cell.2013.05.039.
  • Campisi J, Kapahi P, Lithgow GJ, Melov S, Newman JC, Verdin E. From discoveries in ageing research to therapeutics for healthy ageing. Nature. 2019;571(7764):183–192. doi:10.1038/s41586-019-1365-2.
  • Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K. Frailty in elderly people. Lancet. 2013;381(9868):752–762. doi:10.1016/S0140-6736(12)62167-9.
  • Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol. 2015;31(1):69–75. doi:10.1097/MOG.0000000000000139.
  • Buford TW. (Dis)trust your gut: the gut microbiome in age-related inflammation, health, and disease. Microbiome. 2017;5(1):80. doi:10.1186/s40168-017-0296-0.
  • Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214. doi:10.1038/nature11234.
  • Gacesa R, Kurilshikov A, Vich Vila A, Sinha T, Klaassen MAY, Bolte LA, Andreu-Sanchez S, Chen L, Collij V, Hu S, et al. Environmental factors shaping the gut microbiome in a Dutch population. Nature. 2022;604(7907):732–739. doi:10.1038/s41586-022-04567-7.
  • Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T, Mujagic Z, Vila AV, Falony G, Vieira-Silva S, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Sci. 2016;352(6285):565–569. doi:10.1126/science.aad3369.
  • Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder MJ, Valles-Colomer M, Vandeputte D, et al. Population-level analysis of gut microbiome variation. Sci. 2016;352(6285):560–564. doi:10.1126/science.aad3503.
  • McDonald D, Hyde E, Debelius JW, Morton JT, Gonzalez A, Ackermann G, Aksenov AA, Behsaz B, Brennan C, Chen Y, et al. American gut: An open platform for citizen science microbiome research. mSystems. 2018;3(3):e00031–18. doi:10.1128/mSystems.00031-18.
  • Wilmanski T, Diener C, Rappaport N, Patwardhan S, Wiedrick J, Lapidus J, Earls JC, Zimmer A, Glusman G, Robinson M, et al. Gut microbiome pattern reflects healthy ageing and predicts survival in humans. Nat Metab. 2021;3(2):274–286. doi:10.1038/s42255-021-00348-0.
  • He Y, Wu W, Zheng HM, Li P, McDonald D, Sheng HF, Chen MX, Chen ZH, Ji GY, Zheng ZD, et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat Med. 2018;24(10):1532–1535. doi:10.1038/s41591-018-0164-x.
  • Biagi E, Franceschi C, Rampelli S, Severgnini M, Ostan R, Turroni S, Consolandi C, Quercia S, Scurti M, Monti D, et al. Gut microbiota and extreme longevity. Curr Biol. 2016;26(11):1480–1485. doi:10.1016/j.cub.2016.04.016.
  • Kong F, Hua Y, Zeng B, Ning R, Li Y, Zhao J. Gut microbiota signatures of longevity. Curr Biol. 2016;26(18):R832–R833. doi:10.1016/j.cub.2016.08.015.
  • Lim MY, Hong S, Bang SJ, Chung WH, Shin JH, Kim JH, Nam YD, David LA. Gut microbiome structure and association with host factors in a Korean population. mSystems. 2021;6(4):e0017921. doi:10.1128/mSystems.00179-21.
  • Park J, Kato K, Murakami H, Hosomi K, Tanisawa K, Nakagata T, Ohno H, Konishi K, Kawashima H, Chen YA, et al. Comprehensive analysis of gut microbiota of a healthy population and covariates affecting microbial variation in two large Japanese cohorts. BMC Microbiol. 2021;21(1):151. doi:10.1186/s12866-021-02215-0.
  • Yan H, Qin Q, Yan S, Chen J, Yang Y, Li T, Gao X, Ding S. Comparison of the gut microbiota in different age groups in China. Front Cell Infect Microbiol. 2022;12:877914. doi:10.3389/fcimb.2022.877914.
  • Zhang X, Zhong H, Li Y, Shi Z, Ren H, Zhang Z, Zhou X, Tang S, Han X, Lin Y, et al. Sex- and age-related trajectories of the adult human gut microbiota shared across populations of different ethnicities. Nat Aging. 2021;1(1):87–100. doi:10.1038/s43587-020-00014-2.
  • Evert J, Lawler E, Bogan H, Perls T. Morbidity profiles of centenarians: survivors, delayers, and escapers. J Gerontol A Biol Sci Med Sci. 2003;58:232–237. doi:10.1093/gerona/58.3.M232.
  • Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56:M146–M156. doi:10.1093/gerona/56.3.M146.
  • Mitnitski A, Howlett SE, Rockwood K. Heterogeneity of human aging and its assessment. J Gerontol A Biol Sci Med Sci. 2017;72(7):877–884. doi:10.1093/gerona/glw089.
  • Dent E, Kowal P, Hoogendijk EO. Frailty measurement in research and clinical practice: a review. Eur J Intern Med. 2016;31:3–10. doi:10.1016/j.ejim.2016.03.007.
  • Searle SD, Mitnitski A, Gahbauer EA, Gill TM, Rockwood K. A standard procedure for creating a frailty index. BMC Geriatr. 2008;8(1):24. doi:10.1186/1471-2318-8-24.
  • Hoogendijk EO, Afilalo J, Ensrud KE, Kowal P, Onder G, Fried LP. Frailty: Implications for clinical practice and public health. Lancet. 2019;394:1365–1375. doi:10.1016/S0140-6736(19)31786-6.
  • Xu Y, Wang Y, Li H, Dai Y, Chen D, Wang M, Jiang X, Huang Z, Yu H, Huang J, et al. Altered fecal microbiota composition in older adults with frailty. Front Cell Infect Microbiol. 2021;11:696186. doi:10.3389/fcimb.2021.696186.
  • Lim MY, Hong S, Kim JH, Nam YD, Le Couteur D. Association between gut microbiome and frailty in the older adult population in Korea. J Gerontol A Biol Sci Med Sci. 2021;76:1362–1368. doi:10.1093/gerona/glaa319.
  • Jackson MA, Jeffery IB, Beaumont M, Bell JT, Clark AG, Ley RE, O’Toole PW, Spector TD, Steves CJ. Signatures of early frailty in the gut microbiota. Genome Med. 2016;8(1):8. doi:10.1186/s13073-016-0262-7.
  • Haran JP, Zeamer A, Ward DV, Dutta P, Bucci V, McCormick BA, Le Couteur D. The nursing home older adult gut microbiome composition shows time-dependent dysbiosis and is influenced by medication exposures, age, environment, and frailty. J Gerontol A Biol Sci Med Sci. 2021;76:1930–1938. doi:10.1093/gerona/glab167.
  • Larson PJ, Zhou W, Santiago A, Driscoll S, Fleming E, Voigt AY, Chun OK, Grady JJ, Kuchel GA, Robison JT, et al. Associations of the skin, oral and gut microbiome with aging, frailty and infection risk reservoirs in older adults. Nat Aging. 2022;2(10):941–955. doi:10.1038/s43587-022-00287-9.
  • Almeida HM, Sardeli AV, Conway J, Duggal NA, Cavaglieri CR. Comparison between frail and non-frail older adults’ gut microbiota: A systematic review and meta-analysis. Ageing Res Rev. 2022;82:101773. doi:10.1016/j.arr.2022.101773.
  • Hwang HS, Kwon IS, Park BJ, Cho B, Yoon JL, Won CW. The validity and reliability of Korean frailty index. J Korean Geriatr Soc. 2010;14(4):191–202. doi:10.4235/jkgs.2010.14.4.191.
  • Kojima G. Prevalence of frailty in nursing homes: a systematic review and meta-analysis. J Am Med Dir Assoc. 2015;16(11):940–945. doi:10.1016/j.jamda.2015.06.025.
  • Burato S, Leonardi L, Antonazzo IC, Raschi E, Ajolfi C, Baraghini M, Chiarello A, Delmonte V, Di Castri L, Donati M, et al. Comparing the prevalence of polypharmacy and potential drug-drug interactions in nursing homes and in the community dwelling elderly of Emilia Romagna region. Front Pharmacol. 2020;11:624888. doi:10.3389/fphar.2020.624888.
  • Aguayo GA, Vaillant MT, Donneau AF, Schritz A, Stranges S, Malisoux L, Chioti A, Guillaume M, Muller M, Witte DR, et al. Comparative analysis of the association between 35 frailty scores and cardiovascular events, cancer, and total mortality in an elderly general population in England: an observational study. PLoS Med. 2018;15(3):e1002543. doi:10.1371/journal.pmed.1002543.
  • Liu H, Wang J, He T, Becker S, Zhang GL, Li DF, Ma X. Butyrate: A double-edged sword for health? Adv Nutr. 2018;9:21–29. doi:10.1093/advances/nmx009.
  • Ferrucci L, Fabbri E. Inflammageing: Chronic inflammation in ageing, cardiovascular disease, and frailty. Nat Rev Cardiol. 2018;15(9):505–522. doi:10.1038/s41569-018-0064-2.
  • De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA. 2010;107(33):14691–14696. doi:10.1073/pnas.1005963107.
  • Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. Linking long-term dietary patterns with gut microbial enterotypes. Sci. 2011;334(6052):105–108. doi:10.1126/science.1208344.
  • Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, Hallen A, Martens E, Bjorck I, Backhed F. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell Metab. 2015;22(6):971–982. doi:10.1016/j.cmet.2015.10.001.
  • Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, Rostron T, Cerundolo V, Pamer EG, Abramson SB, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife. 2013;2:e01202. doi:10.7554/eLife.01202.
  • Pedersen HK, Gudmundsdottir V, Nielsen HB, Hyotylainen T, Nielsen T, Jensen BA, Forslund K, Hildebrand F, Prifti E, Falony G, et al. Human gut microbes impact host serum metabolome and insulin sensitivity. Nature. 2016;535(7612):376–381. doi:10.1038/nature18646.
  • Leite AZ, Rodrigues NC, Gonzaga MI, Paiolo JCC, de Souza CA, Stefanutto NAV, Omori WP, Pinheiro DG, Brisotti JL, Matheucci Junior E, et al. Detection of increased plasma interleukin-6 levels and prevalence of Prevotella copri and Bacteroides vulgatus in the feces of type 2 diabetes patients. Front Immunol. 2017;8:1107. doi:10.3389/fimmu.2017.01107.
  • Tett A, Pasolli E, Masetti G, Ercolini D, Segata N. Prevotella diversity, niches and interactions with the human host. Nat Rev Microbiol. 2021;19(9):585–599. doi:10.1038/s41579-021-00559-y.
  • Tett A, Huang KD, Asnicar F, Fehlner-Peach H, Pasolli E, Karcher N, Armanini F, Manghi P, Bonham K, Zolfo M, et al. The Prevotella copri complex comprises four distinct clades underrepresented in westernized populations. Cell Host & Microbe. 2019;26(5):666–679.e7. doi:10.1016/j.chom.2019.08.018.
  • Cekanaviciute E, Yoo BB, Runia TF, Debelius JW, Singh S, Nelson CA, Kanner R, Bencosme Y, Lee YK, Hauser SL, et al. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc Natl Acad Sci USA. 2017;114(40):10713–10718. doi:10.1073/pnas.1711235114.
  • Zhang X, Zhang DY, Jia HJ, Feng Q, Wang DH, Liang D, Wu XN, Li JH, Tang LQ, Li Y, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21(8):895–905. doi:10.1038/nm.3914.
  • Alexander M, Ang QY, Nayak RR, Bustion AE, Sandy M, Zhang B, Upadhyay V, Pollard KS, Lynch SV, Turnbaugh PJ. Human gut bacterial metabolism drives Th17 activation and colitis. Cell Host & Microbe. 2022;30(1):17–30.e9. doi:10.1016/j.chom.2021.11.001.
  • Zuo T, Zhang F, Lui GCY, Yeoh YK, AYL L, Zhan H, Wan Y, Chung ACK, Cheung CP, Chen N, et al. Alterations in gut microbiota of patients with COVID-19 during time of hospitalization. Gastroenterology. 2020;159:944–955.e8. doi:10.1053/j.gastro.2020.05.048.
  • Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60. doi:10.1038/nature11450.
  • Romano KA, Vivas EI, Amador-Noguez D, Rey FE, Blaser MJ. Intestinal microbiota composition modulates choline bioavailability from diet and accumulation of the proatherogenic metabolite trimethylamine-N-oxide. mBio. 2015;6(2):e02481. doi:10.1128/mBio.02481-14.
  • Spaiser SJ, Culpepper T, Nieves C Jr., Ukhanova M, Mai V, Percival SS, Christman MC, Langkamp-Henken B. Lactobacillus gasseri KS-13, Bifidobacterium bifidum G9-1, and Bifidobacterium longum MM-2 ingestion induces a less inflammatory cytokine profile and a potentially beneficial shift in gut microbiota in older adults: a randomized, double-blind, placebo-controlled, crossover study. J Am Coll Nutr. 2015;34:459–469. doi:10.1080/07315724.2014.983249.
  • Nilsson AG, Sundh D, Backhed F, Lorentzon M. Lactobacillus reuteri reduces bone loss in older women with low bone mineral density: a randomized, placebo-controlled, double-blind, clinical trial. J Intern Med. 2018;284(3):307–317. doi:10.1111/joim.12805.
  • Finamore A, Roselli M, Donini L, Brasili DE, Rami R, Carnevali P, Mistura L, Pinto A, Giusti A, Mengheri E. Supplementation with Bifidobacterium longum Bar33 and Lactobacillus helveticus Bar13 mixture improves immunity in elderly humans (over 75 years) and aged mice. Nutrition. 2019;63-64:184–192. doi:10.1016/j.nut.2019.02.005.
  • Kim CS, Cha L, Sim M, Jung S, Chun WY, Baik HW, Shin DM, Le Couteur D. Probiotic supplementation improves cognitive function and mood with changes in gut microbiota in community-dwelling older adults: a randomized, double-blind, placebo-controlled, multicenter trial. J Gerontol A Biol Sci Med Sci. 2021;76:32–40. doi:10.1093/gerona/glaa090.
  • Sanborn V, Azcarate-Peril MA, Updegraff J, Manderino L, Gunstad J. Randomized clinical trial examining the impact of lactobacillus rhamnosus gg probiotic supplementation on cognitive functioning in middle-aged and older adults. Neuropsychiatr Dis Treat. 2020;16:2765–2777. doi:10.2147/NDT.S270035.
  • Aljumaah MR, Bhatia U, Roach J, Gunstad J, Azcarate Peril MA. The gut microbiome, mild cognitive impairment, and probiotics: A randomized clinical trial in middle-aged and older adults. Clin Nutr. 2022;41:2565–2576. doi:10.1016/j.clnu.2022.09.012.
  • Sakurai K, Toshimitsu T, Okada E, Anzai S, Shiraishi I, Inamura N, Kobayashi S, Sashihara T, Hisatsune T. Effects of Lactiplantibacillus plantarum OLL2712 on memory function in older adults with declining memory: a randomized placebo-controlled trial. Nutrients. 2022;14(20):4300. doi:10.3390/nu14204300.
  • Sandionigi A, De Giani A, Tursi F, Michelotti A, Cestone E, Giardina S, Zampolli J, Di Gennaro P, Abbassi MS. Effectiveness of multistrain probiotic formulation on common infectious disease symptoms and gut microbiota modulation in flu-vaccinated healthy elderly subjects. Biomed Res Int. 2022;2022:1–16. doi:10.1155/2022/3860896.
  • Liu L, Chen X, Liu L, Qin H. Clostridium butyricum potentially improves immunity and nutrition through alteration of the microbiota and metabolism of elderly people with malnutrition in long-term care. Nutrients. 2022;14(17):3546. doi:10.3390/nu14173546.
  • Fei Y, Wang R, Lu J, Peng S, Yang S, Wang Y, Zheng K, Li R, Lin L, Li M. Probiotic intervention benefits multiple neural behaviors in older adults with mild cognitive impairment. Geriatr Nurs. 2023;51:167–175. doi:10.1016/j.gerinurse.2023.03.006.
  • Alfa MJ, Strang D, Tappia PS, Graham M, Van Domselaar G, Forbes JD, Laminman V, Olson N, DeGagne P, Bray D, et al. A randomized trial to determine the impact of a digestion resistant starch composition on the gut microbiome in older and mid-age adults. Clin Nutr. 2018;37:797–807. doi:10.1016/j.clnu.2017.03.025.
  • Chung WSF, Walker AW, Bosscher D, Garcia-Campayo V, Wagner J, Parkhill J, Duncan SH, Flint HJ. Relative abundance of the Prevotella genus within the human gut microbiota of elderly volunteers determines the inter-individual responses to dietary supplementation with wheat bran arabinoxylan-oligosaccharides. BMC Microbiol. 2020;20(1):283. doi:10.1186/s12866-020-01968-4.
  • Ganda Mall JP, Fart F, Sabet JA, Lindqvist CM, Nestestog R, Hegge FT, Keita AV, Brummer RJ, Schoultz I. Effects of dietary fibres on acute indomethacin-induced intestinal hyperpermeability in the elderly: a randomised placebo controlled parallel clinical trial. Nutrients. 2020;12:1954. doi:10.3390/nu12071954.
  • Kim HK, Chijiki H, Nanba T, Ozaki M, Sasaki H, Takahashi M, Shibata S. Ingestion of Helianthus tuberosus at breakfast rather than at dinner is more effective for suppressing glucose levels and improving the intestinal microbiota in older adults. Nutrients. 2020;12(10):3035. doi:10.3390/nu12103035.
  • Kiewiet MBG, Elderman ME, El Aidy S, Burgerhof JGM, Visser H, Vaughan EE, Faas MM, de Vos P. Flexibility of gut microbiota in ageing individuals during dietary fiber long-chain inulin intake. Mol Nutr Food Res. 2021;65(4):e2000390. doi:10.1002/mnfr.202000390.
  • Manzoni MSJ, Rossi EA, Pauly-Silveira ND, Pinto RA, Roselino MN, Carlos IZ, Quilles MB, de Abreu Gloria MB, Cavallini DCU. Consumption effect of a synbiotic beverage made from soy and yacon extracts containing Bifidobacterium animalis ssp. lactis BB-12 on the intestinal polyamine concentrations in elderly individuals. Food Res Int. 2017;99:495–500. doi:10.1016/j.foodres.2017.06.005.
  • Cicero AFG, Fogacci F, Bove M, Giovannini M, Borghi C. Impact of a short-term synbiotic supplementation on metabolic syndrome and systemic inflammation in elderly patients: a randomized placebo-controlled clinical trial. Eur J Nutr. 2021;60(2):655–663. doi:10.1007/s00394-020-02271-8.
  • Bo C D, Bernardi S, Cherubini A, Porrini M, Gargari G, Hidalgo-Liberona N, Gonzalez-Dominiguez R, Zamora-Ros R, Peron G, Marino M, et al. A polyphenol-rich dietary pattern improves intestinal permeability, evaluated as serum zonulin levels, in older subjects: the maple randomised controlled trial. Clin Nutr. 2021;40:3006–3018. doi:10.1016/j.clnu.2020.12.014.
  • Peron G, Gargari G, Merono T, Minarro A, Lozano EV, Escuder PC, Gonzalez-Dominguez R, Hidalgo-Liberona N, Del Bo C, Bernardi S, et al. Crosstalk among intestinal barrier, gut microbiota and serum metabolome after a polyphenol-rich diet in older subjects with “leaky gut”: the MaPLE trial. Clin Nutr. 2021;40:5288–5297. doi:10.1016/j.clnu.2021.08.027.
  • Valentini L, Pinto A, Bourdel-Marchasson I, Ostan R, Brigidi P, Turroni S, Hrelia S, Hrelia P, Bereswill S, Fischer A, et al. Impact of personalized diet and probiotic supplementation on inflammation, nutritional parameters and intestinal microbiota - the “RISTOMED project”: randomized controlled trial in healthy older people. Clin Nutr. 2015;34:593–602. doi:10.1016/j.clnu.2014.09.023.
  • Ford AL, Nagulesapillai V, Piano A, Auger J, Girard SA, Christman M, Tompkins TA, Dahl WJ. Microbiota stability and gastrointestinal tolerance in response to a high-protein diet with and without a prebiotic, probiotic, and synbiotic: a randomized, double-blind, placebo-controlled trial in older women. J Acad Nutr Diet. 2020;120(4):500–516.e10. doi:10.1016/j.jand.2019.12.009.
  • Ghosh TS, Rampelli S, Jeffery IB, Santoro A, Neto M, Capri M, Giampieri E, Jennings A, Candela M, Turroni S, et al. Mediterranean diet intervention alters the gut microbiome in older people reducing frailty and improving health status: The NU-AGE 1-year dietary intervention across five European countries. Gut. 2020;69(7):1218–1228. doi:10.1136/gutjnl-2019-319654.
  • Igwe EO, Roodenrys S, Probst YC, Do Rosario V, Netzel ME, Hong HT, Netzel G, Phan ADT, Charlton KE. Low anthocyanin plum nectar does not impact cognition, blood pressure and gut microbiota in healthy older adults: a randomized crossover trial. Nutr Res. 2020;82:74–87. doi:10.1016/j.nutres.2020.08.003.
  • Mitchell SM, Milan AM, Mitchell CJ, Gillies NA, D’Souza RF, Zeng N, Ramzan F, Sharma P, Knowles SO, Roy NC, et al. Protein intake at twice the RDA in older men increases circulatory concentrations of the microbiome metabolite trimethylamine-N-oxide (TMAO). Nutrients. 2019;11:2207. doi:10.3390/nu11092207.
  • Mitchell SM, McKenzie EJ, Mitchell CJ, Milan AM, Zeng N, D’Souza RF, Ramzan F, Sharma P, Rettedal E, Knowles SO, et al. A period of 10 weeks of increased protein consumption does not alter faecal microbiota or volatile metabolites in healthy older men: a randomised controlled trial. J Nutr Sci. 2020;9:e25. doi:10.1017/jns.2020.15.
  • Fluitman KS, Wijdeveld M, Davids M, van Ruiten CC, Reinders I, Wijnhoven HAH, Keijser BJF, Visser M, Nieuwdorp M, IJ RG, et al. Personalized dietary advice to increase protein intake in older adults does not affect the gut microbiota, appetite or central processing of food stimuli in community-dwelling older adults: a six-month randomized controlled trial. Nutrients. 2023;15:332. doi:10.3390/nu15020332.
  • Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, et al. Expert consensus document. The International Scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506–514. doi:10.1038/nrgastro.2014.66.
  • Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14(8):491–502. doi:10.1038/nrgastro.2017.75.
  • Swanson KS, Gibson GR, Hutkins R, Reimer RA, Reid G, Verbeke K, Scott KP, Holscher HD, Azad MB, Delzenne NM, et al. The International Scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol. 2020;17(11):687–701. doi:10.1038/s41575-020-0344-2.
  • Li P, Ji B, Luo H, Sundh D, Lorentzon M, Nielsen J. One-year supplementation with Lactobacillus reuteri ATCC PTA 6475 counteracts a degradation of gut microbiota in older women with low bone mineral density. NPJ Biofilms Microbio. 2022;8(1):84. doi:10.1038/s41522-022-00348-2.
  • McLoughlin RF, Berthon BS, Jensen ME, Baines KJ, Wood LG. Short-chain fatty acids, prebiotics, synbiotics, and systemic inflammation: a systematic review and meta-analysis. Am J Clin Nutr. 2017;106(3):930–945. doi:10.3945/ajcn.117.156265.
  • Kim YA, Keogh JB, Clifton PM. Probiotics, prebiotics, synbiotics and insulin sensitivity. Nutr Res Rev. 2018;31(1):35–51. doi:10.1017/S095442241700018X.
  • Zmora N, Zilberman-Schapira G, Suez J, Mor U, Dori-Bachash M, Bashiardes S, Kotler E, Zur M, Regev-Lehavi D, Brik RB, et al. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell. 2018;174(6):1388–1405.e21. doi:10.1016/j.cell.2018.08.041.
  • Maldonado-Gomez MX, Martinez I, Bottacini F, O’Callaghan A, Ventura M, van Sinderen D, Hillmann B, Vangay P, Knights D, Hutkins RW, et al. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host & Microbe. 2016;20(4):515–526. doi:10.1016/j.chom.2016.09.001.
  • Willett WC, Sacks F, Trichopoulou A, Drescher G, Ferro-Luzzi A, Helsing E, Trichopoulos D. Mediterranean diet pyramid: a cultural model for healthy eating. Am J Clin Nutr. 1995;61(6):1402S–1406S. doi:10.1093/ajcn/61.6.1402S.
  • Talegawkar SA, Bandinelli S, Bandeen-Roche K, Chen P, Milaneschi Y, Tanaka T, Semba RD, Guralnik JM, Ferrucci L. A higher adherence to a Mediterranean-style diet is inversely associated with the development of frailty in community-dwelling elderly men and women. J Nutr. 2012;142(12):2161–2166. doi:10.3945/jn.112.165498.
  • Leon-Munoz LM, Guallar-Castillon P, Lopez-Garcia E, Rodriguez-Artalejo F. Mediterranean diet and risk of frailty in community-dwelling older adults. J Am Med Dir Assoc. 2014;15(12):899–903. doi:10.1016/j.jamda.2014.06.013.
  • Wu PY, Chen KM, Tsai WC. The Mediterranean dietary pattern and inflammation in older adults: a systematic review and meta-analysis. Adv Nutr. 2021;12:363–373. doi:10.1093/advances/nmaa116.
  • Loughrey DG, Lavecchia S, Brennan S, Lawlor BA, Kelly ME. The impact of the Mediterranean diet on the cognitive functioning of healthy older adults: a systematic review and meta-analysis. Adv Nutr. 2017;8:571–586. doi:10.3945/an.117.015495.
  • Wu M, Luo Q, Nie R, Yang X, Tang Z, Chen H. Potential implications of polyphenols on aging considering oxidative stress, inflammation, autophagy, and gut microbiota. Crit Rev Food Sci Nutr. 2021;61(13):2175–2193. doi:10.1080/10408398.2020.1773390.
  • Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol. 2011;17:1519–1528. doi:10.3748/wjg.v17.i12.1519.
  • Pothier K, Gana W, Bailly N, Fougere B. Associations between frailty and inflammation, physical, and psycho-social health in older adults: a systematic review. Front Psychol. 2022;13:805501. doi:10.3389/fpsyg.2022.805501.
  • Coelho-Junior HJ, Calvani R, Azzolino D, Picca A, Tosato M, Landi F, Cesari M, Marzetti E. Protein intake and sarcopenia in older adults: a systematic review and meta-analysis. Int J Environ Res Public Health. 2022;19:8718. doi:10.3390/ijerph19148718.
  • Coelho-Junior HJ, Marzetti E, Picca A, Cesari M, Uchida MC, Calvani R. Protein intake and frailty: a matter of quantity, quality, and timing. Nutrients. 2020;12(10):2915. doi:10.3390/nu12102915.
  • Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472(7341):57–63. doi:10.1038/nature09922.
  • Karakan T, Gundogdu A, Alagozlu H, Ekmen N, Ozgul S, Tunali V, Hora M, Beyazgul D, Nalbantoglu OU. Artificial intelligence-based personalized diet: a pilot clinical study for irritable bowel syndrome. Gut Microbes. 2022;14(1):2138672. doi:10.1080/19490976.2022.2138672.