Disentangling the age-related manner in the associations between gut microbiome and women’s health: a multi-cohort microbiome study

References

• Langer A, Meleis A, Knaul FM, Atun R, Aran M, Arreola-Ornelas H, Bhutta ZA, Binagwaho A, Bonita R, Caglia JM, et al. Women and health: the key for sustainable development. Lancet. 2015;386(9999):1165–19. doi:10.1016/S0140-6736(15)60497-4.
   PubMed Web of Science ®Google Scholar
• Peters SAE, Woodward M, Jha V, Kennedy S, Norton R. Women’s health: a new global agenda. BMJ Glob Health. 2016;1:e000080. doi:10.1136/bmjgh-2016-000080.
   PubMedGoogle Scholar
• It’s time to expand the definition of ‘women’s health’. Nature. 2021;596(7870):7. doi:10.1038/d41586-021-02085-6.
   PubMed Web of Science ®Google Scholar
• Temmerman M, Khosla R, Laski L, Mathews Z, Say L. Women’s health priorities and interventions. BMJ. 2015;351:h4147. doi:10.1136/bmj.h4147.
   PubMedGoogle Scholar
• Short SE, Zacher M. Women’s health: population patterns and social determinants. Annu Rev Sociol. 2022;48(1):277–298. doi:10.1146/annurev-soc-030320-034200.
   PubMedGoogle Scholar
• Qi X, Yun C, Sun L, Xia J, Wu Q, Wang Y, Wang L, Zhang Y, Liang X, Wang L, et al. Gut microbiota–bile acid–interleukin-22 axis orchestrates polycystic ovary syndrome. Nat Med. 2019;25(8):1225–1233. doi:10.1038/s41591-019-0509-0.
   PubMed Web of Science ®Google Scholar
• Zhang C, Yin A, Li H, Wang R, Wu G, Shen J, Zhang M, Wang L, Hou Y, Ouyang H, et al. Dietary modulation of gut microbiota contributes to alleviation of both genetic and simple obesity in children. EBioMedicine. 2015;2(8):968–984. doi:10.1016/j.ebiom.2015.07.007.
   PubMed Web of Science ®Google Scholar
• Shobeiri P, Kalantari A, Teixeira AL, Rezaei N. Shedding light on biological sex differences and microbiota–gut–brain axis: a comprehensive review of its roles in neuropsychiatric disorders. Biol Sex Differ. 2022;13(1):12. doi:10.1186/s13293-022-00422-6.
   PubMed Web of Science ®Google Scholar
• Cox LM, Maghzi AH, Liu S, Tankou SK, Dhang FH, Willocq V, Song A, Wasén C, Tauhid S, Chu R, et al. Gut microbiome in progressive multiple sclerosis. Ann Neurol. 2021;89(6):1195–1211. doi:10.1002/ana.26084.
   PubMed Web of Science ®Google Scholar
• Paik D, Yao L, Zhang Y, Bae S, D’Agostino GD, Zhang M, Kim E, Franzosa EA, Avila-Pacheco J, Bisanz JE, et al. Human gut bacteria produce ΤΗ17-modulating bile acid metabolites. Nature. 2022;603(7903):907–12. doi:10.1038/s41586-022-04480-z.
   PubMed Web of Science ®Google Scholar
• Qi X, Yun C, Pang Y, Qiao J. The impact of the gut microbiota on the reproductive and metabolic endocrine system. Gut Microbes. 2021;13(1):1–21. doi:10.1080/19490976.2021.1894070.
   Web of Science ®Google Scholar
• Leonardi I, Gao IH, Lin WY, Allen M, Li XV, Fiers WD, De Celie MB, Putzel GG, Yantiss RK, Johncilla M, et al. Mucosal fungi promote gut barrier function and social behavior via type 17 immunity. Cell. 2022;185(5):831–46.e14. doi:10.1016/j.cell.2022.01.017.
   PubMed Web of Science ®Google Scholar
• Wang J, Thingholm LB, Skiecevičienė J, Rausch P, Kummen M, Hov JR, Degenhardt F, Heinsen F-A, Rühlemann MC, Szymczak S, et al. Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nat Genet. 2016;48(11):1396–1406. doi:10.1038/ng.3695.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–227. doi:10.1038/nature11053.
   PubMed Web of Science ®Google Scholar
• Claesson MJ, Cusack S, O’Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, Marchesi JR, Falush D, Dinan T, Fitzgerald G, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A. 2011;108(supplement_1):4586–91. doi:10.1073/pnas.1000097107.
   PubMed Web of Science ®Google Scholar
• Mariat D, Firmesse O, Levenez F, Guimarăes V, Sokol H, Doré J, Corthier G, Furet J-P. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009;9(1):123. doi:10.1186/1471-2180-9-123.
   PubMed Web of Science ®Google Scholar
• Bosco N, Noti M. The aging gut microbiome and its impact on host immunity. Genes Immun. 2021;22(5–6):289–303. doi:10.1038/s41435-021-00126-8.
   PubMed Web of Science ®Google Scholar
• Salazar N, Arboleya S, Fernández-Navarro T, Rde Los Eyes-Gavilán CG, Gonzalez S, Gueimonde M. Age-associated changes in gut microbiota and dietary components related with the immune system in adulthood and old age: a cross-sectional study. Nutrients. 2019;11(8):1765. doi:10.3390/nu11081765.
   PubMed Web of Science ®Google Scholar
• Thevaranjan N, Puchta A, Schulz C, Naidoo A, Szamosi JC, Verschoor CP, Loukov D, Schenck LP, Jury J, Foley KP, et al. Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host & Microbe. 2017;21(4):455–66.e4. doi:10.1016/j.chom.2017.03.002.
   PubMed Web of Science ®Google Scholar
• Duricova D, Burisch J, Jess T, Gower-Rousseau C, Lakatos PL. Age-related differences in presentation and course of inflammatory bowel disease: an update on the population-based literature. J Crohn’s Colitis. 2014;8(11):1351–61. On Behalf of E-E. doi: 10.1016/j.crohns.2014.05.006.
   Google Scholar
• Gacesa R, Kurilshikov A, Vich Vila A, Sinha T, Klaassen MAY, Bolte LA, Andreu-Sánchez 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.
   PubMed Web of Science ®Google Scholar
• De Filippis F, Pellegrini N, Vannini L, Jeffery IB, La Storia A, Laghi L, Serrazanetti DI, Di Cagno R, Ferrocino I, Lazzi C, et al. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut. 2016;65(11):1812–1821. doi:10.1136/gutjnl-2015-309957.
   PubMed Web of Science ®Google Scholar
• Vangay P, Johnson AJ, Ward TL, Al-Ghalith GA, Shields-Cutler RR, Hillmann BM, Lucas SK, Beura LK, Thompson EA, Till LM, et al. US immigration westernizes the human gut microbiome. Cell. 2018;175(4):962–72.e10. doi:10.1016/j.cell.2018.10.029.
   PubMed Web of Science ®Google Scholar
• Kuang Y-S, Li S-H, Guo Y, Lu J-H, He J-R, Luo B-J, Jiang F-J, Shen H, Papasian CJ, Pang H, et al. Composition of gut microbiota in infants in China and global comparison. Sci Rep. 2016;6(1):36666. doi:10.1038/srep36666.
   PubMedGoogle Scholar
• Marrs T, Jo JH, Perkin MR, Rivett DW, Witney AA, Bruce KD, Logan K, Craven J, Radulovic S, Versteeg SA, et al. Gut microbiota development during infancy: impact of introducing allergenic foods. J Allergy Clin Immunol. 2021;147(2):613–21.e9. doi:10.1016/j.jaci.2020.09.042.
   PubMed Web of Science ®Google Scholar
• Moore RE, Townsend SD. Temporal development of the infant gut microbiome. Open Biol. 2019;9(9):190128. doi:10.1098/rsob.190128.
   PubMed Web of Science ®Google Scholar
• Ramos Meyers G, Samouda H, Bohn T. Short chain fatty acid metabolism in relation to gut microbiota and genetic variability. Nutrients. 2022;14(24):5361. doi:10.3390/nu14245361.
   PubMed Web of Science ®Google Scholar
• Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: networks, competition, and stability. Sci. 2015;350(6261):663–666. doi:10.1126/science.aad2602.
   PubMed Web of Science ®Google Scholar
• Ojima MN, Jiang L, Arzamasov AA, Yoshida K, Odamaki T, Xiao J, Nakajima A, Kitaoka M, Hirose J, Urashima T, et al. Priority effects shape the structure of infant-type Bifidobacterium communities on human milk oligosaccharides. ISME J. 2022;16(9):2265–2279. doi:10.1038/s41396-022-01270-3.
   PubMed Web of Science ®Google Scholar
• He S, Li H, Yu Z, Zhang F, Liang S, Liu H, Chen, H., Lü, M. et al. The gut microbiome and sex hormone-related diseases. Front Microbiol. 2021;12:711137. doi:10.3389/fmicb.2021.711137.
   PubMed Web of Science ®Google Scholar
• Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121–141. doi:10.1016/j.cell.2014.03.011.
   PubMed Web of Science ®Google Scholar
• Hohman LS, Osborne LC. A gut-centric view of aging: Do intestinal epithelial cells contribute to age-associated microbiota changes, inflammaging, and immunosenescence? Aging Cell. 2022;21(9):e13700. doi:10.1111/acel.13700.
   PubMed Web of Science ®Google Scholar
• Ghosh TS, Shanahan F, O’Toole PW. The gut microbiome as a modulator of healthy ageing. Nat Rev Gastro Hepat. 2022;19(9):565–584. doi:10.1038/s41575-022-00605-x.
   PubMed Web of Science ®Google Scholar
• López-Almela I, Romaní-Pérez M, Bullich-Vilarrubias C, Benítez-Páez A, Gómez Del Pulgar EM, Francés R, Liebisch G, Sanz Y. Bacteroides uniformis combined with fiber amplifies metabolic and immune benefits in obese mice. Gut Microbes. 2021;13(1):1–20. doi:10.1080/19490976.2020.1865706.
   PubMed Web of Science ®Google Scholar
• Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4):289–306. doi:10.4161/gmic.19897.
   PubMed Web of Science ®Google Scholar
• Shi F, Liu G, Lin Y, Guo CL, Han J, Chu ESH, Shi C, Li Y, Zhang H, Hu C, et al. Altered gut microbiome composition by appendectomy contributes to colorectal cancer. Oncogene. 2023;42(7):530–540. doi:10.1038/s41388-022-02569-3.
   PubMed Web of Science ®Google Scholar
• Companys J, Gosalbes MJ, Pla-Pagà L, Calderón-Pérez L, Llauradó E, Pedret A, Valls RM, Jiménez-Hernández N, Sandoval-Ramirez BA, Del Bas JM, et al. Gut microbiota profile and its association with clinical variables and dietary intake in overweight/obese and lean subjects: a cross-sectional study. Nutrients. 2021;13(6):2032. doi:10.3390/nu13062032.
   PubMed Web of Science ®Google Scholar
• Mueller NT, Differding MK, Zhang M, Maruthur NM, Juraschek SP, Miller ER 3rd, Appel LJ, Yeh H-C. Metformin affects gut microbiome composition and function and circulating short-chain fatty acids: a randomized trial. Diab Care. 2021;44(7):1462–71. doi:10.2337/dc20-2257.
   PubMed Web of Science ®Google Scholar
• Lloyd-Price J, Arze C, Ananthakrishnan AN, Schirmer M, Avila-Pacheco J, Poon TW, Andrews E, Ajami NJ, Bonham KS, Brislawn CJ, et al. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature. 2019;569(7758):655–662. doi:10.1038/s41586-019-1237-9.
   PubMed Web of Science ®Google Scholar
• Schirmer M, Franzosa EA, Lloyd-Price J, McIver LJ, Schwager R, Poon TW, Ananthakrishnan AN, Andrews E, Barron G, Lake K, et al. Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nature Microbiology. 2018;3(3):337–346. doi:10.1038/s41564-017-0089-z.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Smith EA, Macfarlane GT. Enumeration of amino acid fermenting bacteria in the human large intestine: effects of pH and starch on peptide metabolism and dissimilation of amino acids. FEMS Microbiol Ecol. 1998;25(4):355–368. doi:10.1111/j.1574-6941.1998.tb00487.x.
   Web of Science ®Google Scholar
• Jakubovics NS, Brittan JL, Dutton LC, Jenkinson HF. Multiple adhesin proteins on the cell surface of Streptococcus gordonii are involved in adhesion to human fibronectin. Microbiol. 2009;155(11):3572–3580. doi:10.1099/mic.0.032078-0.
   PubMedGoogle Scholar
• Poppleton DI, Duchateau M, Hourdel V, Matondo M, Flechsler J, Klingl A, Beloin, C., Gribaldo, S., et al. Outer membrane proteome of Veillonella parvula: A diderm Firmicute of the human microbiome. Front Microbiol. 2017;8:1215. doi:10.3389/fmicb.2017.01215.
   PubMed Web of Science ®Google Scholar
• Jie Z, Xia H, Zhong SL, Feng Q, Li S, Liang S, Zhong H, Liu Z, Gao Y, Zhao H, et al. The gut microbiome in atherosclerotic cardiovascular disease. Nat Commun. 2017;8(1):845. doi:10.1038/s41467-017-00900-1.
   PubMed Web of Science ®Google Scholar
• Schirmer M, Smeekens SP, Vlamakis H, Jaeger M, Oosting M, Franzosa EA, Ter Horst R, Jansen T, Jacobs L, Bonder MJ, et al. Linking the human gut microbiome to inflammatory cytokine production capacity. Cell. 2016;167(4):1125–36.e8. doi:10.1016/j.cell.2016.10.020.
   PubMed Web of Science ®Google Scholar
• Keyashian K, Dehghan M, Sceats L, Kin C, Limketkai BN, Park KT. Comparative incidence of inflammatory bowel disease in different age groups in the United States. Inflamm Bowel Dis. 2019;25(12):1983–1989. doi:10.1093/ibd/izz092.
   PubMed Web of Science ®Google Scholar
• Pasvol TJ, Horsfall L, Bloom S, Segal AW, Sabin C, Field N, Rait G. Incidence and prevalence of inflammatory bowel disease in UK primary care: a population-based cohort study. BMJ Open. 2020;10(7):e036584. doi:10.1136/bmjopen-2019-036584.
   PubMed Web of Science ®Google Scholar
• Pasolli E, Schiffer L, Manghi P, Renson A, Obenchain V, Truong DT, Beghini F, Malik F, Ramos M, Dowd JB, et al. Accessible, curated metagenomic data through ExperimentHub. Nat Methods. 2017;14(11):1023–1024. doi:10.1038/nmeth.4468.
   PubMed Web of Science ®Google Scholar
• Xiao L, Zhao F. Microbial transmission, colonisation and succession: from pregnancy to infancy. Gut. 2023;72(4):772–786. doi:10.1136/gutjnl-2022-328970.
   PubMed Web of Science ®Google Scholar
• Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods. 2013;10(1):57–9. doi:10.1038/nmeth.2276.
   PubMed Web of Science ®Google Scholar
• Leek JT, Scharpf RB, Bravo HC, Simcha D, Langmead B, Johnson WE, Geman D, Baggerly K, Irizarry RA. Tackling the widespread and critical impact of batch effects in high-throughput data. Nat Rev Genet. 2010;11(10):733–9. doi:10.1038/nrg2825.
   PubMed Web of Science ®Google Scholar
• Ma S, Shungin D, Mallick H, Schirmer M, Nguyen LH, Kolde R, Franzosa E, Vlamakis H, Xavier R, Huttenhower C, et al. Population structure discovery in meta-analyzed microbial communities and inflammatory bowel disease using MMUPHin. Genome Biol. 2022;23(1):208. doi:10.1186/s13059-022-02753-4.
   PubMed Web of Science ®Google Scholar
• Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, Benezra A, DeStefano J, Meier MF, Muegge BD, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510(7505):417–421. doi:10.1038/nature13421.
   PubMed Web of Science ®Google Scholar
• Rynazal R, Fujisawa K, Shiroma H, Salim F, Mizutani S, Shiba S, Yachida S, Yamada T. Leveraging explainable AI for gut microbiome-based colorectal cancer classification. Genome Biol. 2023;24(1):21. doi:10.1186/s13059-023-02858-4.
   PubMed Web of Science ®Google Scholar
• Jacob C. A power primer. Psychol Bull. 1992;112(1):155–59. doi:10.1037/0033-2909.112.1.155.
   PubMed Web of Science ®Google Scholar